Fold induction of metabolites in sRNA mutants and controls upon C. higginsianum infection.
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",isbn:"978-1-83880-679-8",printIsbn:"978-1-83880-678-1",pdfIsbn:"978-1-83880-680-4",doi:null,price:0,priceEur:0,priceUsd:0,slug:null,numberOfPages:0,isOpenForSubmission:!0,hash:"dfe986c764d6c82ae820c2df5843a866",bookSignature:"Prof. Petra Surlin",publishedDate:null,coverURL:"https://cdn.intechopen.com/books/images_new/9493.jpg",keywords:"Periodontal Morphology, Periodontal Anatomy, Disease Pathogenesis, Periodontal Immunology, Periodontal Examination, Periodontal Instruments, Gingivitis, Periodontal Abscess, Periodontitis, Periodontal Therapy",numberOfDownloads:null,numberOfWosCitations:0,numberOfCrossrefCitations:null,numberOfDimensionsCitations:null,numberOfTotalCitations:null,isAvailableForWebshopOrdering:!0,dateEndFirstStepPublish:"September 8th 2020",dateEndSecondStepPublish:"December 14th 2020",dateEndThirdStepPublish:"February 12th 2021",dateEndFourthStepPublish:"May 3rd 2021",dateEndFifthStepPublish:"July 2nd 2021",remainingDaysToSecondStep:"a month",secondStepPassed:!0,currentStepOfPublishingProcess:3,editedByType:null,kuFlag:!1,biosketch:"Prof. Petra Surlin, DMD, Ph.D., is a member of the European Federation of Periodontology (EFP) and the International Association of Dental Research (IADR). 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They mediate gene silencing, a gene regulation mechanism acting on a transcriptional (transcriptional gene silencing (TGS)) and post‐transcriptional level (post‐transcriptional gene silencing (PTGS)). In general, sRNA molecules originate from the transcription of endogenous microRNA (miRNA genes), other genomic sRNA loci, aberrant RNA produced by transposons as well as invasive viral RNA [2]. Plants carry two main classes of sRNAs grouped according to their size, function and biogenesis, namely microRNAs (miRNA) and short‐interfering RNAs (siRNA) [3]. Such sRNAs are generated through various mechanisms; within the miRNA biogenesis pathway, miRNA precursors derived from MIR genes are processed in the nucleus by Dicer‐like protein 1 (DCL1) and exportin‐like protein (HYL1) into mature miRNA duplexes of 20–22 nucleotides in length. Mature miRNAs are then methylated at the 3′ terminus by HEN1 (small RNA methyltransferase) and exported to the cytoplasm. One strand of the duplex is incorporated into an argonaute protein (AGO) protein to form an RNA‐induced‐silencing complex (RISC) [4]. The siRNAs, however, originate from long dsRNA that can be derived from transgenes, viruses, transposons and natural sense‐antisense transcripts. Such long dsRNA is recognized and cleaved by a certain type of DCL proteins; thereby siRNA classes with different sizes are generated. Like miRNAs, siRNAs are loaded into an AGO protein‐containing RISC that controls gene expression patterns through the degradation of mRNA or the repression of translation of fully/partly complementary sequences of mRNAs, as well through epigenetic changes via mediation of DNA and histone methylation [5, 6].
Gene silencing is not only important for the maintenance of genome integrity by silencing transposons or by degrading the viral RNA but also important during host immune responses of both plants and animals [7–9]. The recognition of pathogens by plants leads to the activation of a multi‐layered immune system that comprises the establishment of a complex network of inducible defences including pathogen‐associated molecular pattern (PAMP)‐triggered immunity (PTI) and effector‐triggered immunity (ETI) [10, 11]. The entire signalling process involves the regulation of defence gene expression, the release of plant hormones and/or the induction of secondary metabolites [12]. Over the past few years, plant sRNA pathways were recognized as important players during PTI and ETI [13, 14]. In Arabidopsis, bacteria‐induced miRNAs were identified to orchestrate components of plant hormone signalling, including auxin, abscisic acid (ABA), jasmonic acid (JA) and salicylic acid (SA) [15, 16]. A canonical example of an miRNA regulating plant defence is miR393. It is up‐regulated upon treatment with a bacterial PAMP, and negatively regulates auxin signalling and therefore contributes to SA‐mediated PTI responses in Arabidopsis [17].
Although the important role of sRNAs in plant defence against viruses and bacteria is documented [8, 13], their function as components of the plants’ defence response against fungi is less clear. Advances in genome‐wide studies revealed a massive adaptation of host miRNA expression patterns after infection by fungal pathogens such as Fusarium virguliforme [18], Erysiphe graminis [19], Verticillium dahliae [20], Cronartium quercuum [21], as well as the oomycete Phytophthora sojae [22]. The alterations in sRNA expression profiles upon fungal attack suggest that gene silencing also contributes to antifungal defence; however, up to date there are no putative mechanisms deciphered. Besides orchestrating plant defence, sRNA could also act as direct antifungal molecules, as some plant miRNAs could share complementarity to fungal genes. This possibility has already been demonstrated by engineering transgenic plants expressing dsRNA targeting fungal genes and exhibiting enhanced resistance to different fungi. For instance, this mechanism named host‐induced gene silencing (HIGS) was successfully applied for various plant‐fungi pathosystems such as silencing of the Blumeria graminis effector Avra10 [23], or CYP51 genes of F. graminearum [24].
In this study, we aim to elucidate the role of sRNAs in regulating susceptibility to Colletotrichum spp.; hence we congregated results from two compatible pathosystems: C. higginsianum, which infects plants from the Brassicaceae family such as Arabidopsis thaliana (Figure 1) and C. graminicola, which is a devastating pathogen of the industrially important crop Zea mays (Figure 2). Both ascomycetes use a multistage hemibiotrophic strategy to infect their host and also share close genetic similarities making them tractable models to compare fungal pathogenicity in both dicot and monocot models [25–28]. In Arabidopsis, C. higginsianum employs first a biotrophic stage limited to a confined array of first invaded cells, from where the fungus develops secondary hyphae to switch to necrotrophic growth into surrounding cells. C. graminicola extends the biotrophic lifespan into many host cells, persisting biotrophic at the margins, whereas the centre of infection becomes necrotrophic. C. graminicola is a major worldwide threat for corn cultures, as it affects all parts of the plants, either as leaf blight or as stalk rot [29]. Depending on specific corn hybrids and culture conditions, C. graminicola can result in up to 40% yield loss where endemic.
Arabidopsis thaliana leaves infected by Colletotrichum higginsianum, 6 days post inoculation.
Zea mays leaf (left) and root (right) infected with Colletotrichum graminicola.
During the first step, a selection of sRNA mutants and two fully and intermediate fungal susceptible accessions of A. thaliana was examined in order to dissect possible defence defects caused by mutations in sRNA biogenesis pathways. Thus, we analysed the accumulation of phytohormones that are known to mediate Arabidopsis resistance against C. higginsianum [30] and secondary metabolites that function as direct defences [31]. We show that some Arabidopsis sRNA mutants display an altered susceptibility against C. higginsianum, together with a defective setup of chemical defences. Moreover, to better understand the role of sRNA during infection with Colletotrichum spp., we performed an miRNA expression profiling to obtain a deeper insight into adaptations of the sRNA transcriptome in different C. graminicola‐infected maize tissues. The miRNA profiling demonstrated that the vast majority of altered miRNAs were targeting genes that are not directly linked to antifungal‐defence pathways, suggesting that antifungal‐defence responses are not regulated by specifically induced miRNAs.
This chapter provides a multi‐omics analysis of sRNA‐mediated antifungal plant reactions on a phenotypic, metabolomic as well as transcriptomic point of view. Altogether, our data propose a rather indirect defensive role of sRNAs in calibrating metabolomic and transcriptomic balances during antifungal responses against Colletotrichum spp. Future putative applications of sRNA‐based fungal control strategies will be commented.
A. thaliana genotypes (hen1‐1, hyl1‐2, rdr6‐15, Col‐0 and Ler‐0) were germinated in soil maintained at 21°C day/20°C night, with 9 h of light (120 µE m−2s1) and 60% of relative humidity. Selected A. thaliana accession Ler‐0 was described to be susceptible to C. higginsianum infection, while Col‐0 showed intermediate resistance [31]. Ler‐0 is the wild‐type genetic background of hen1‐1 mutants; all other mutants have a Col‐0 genetic background. One week after germination, seedlings were individually transferred to 33‐mL Jiffy pellets and kept in the same conditions until the infections. Z. mays (variety Jubilee, West Coast Seeds,
C. higginsianum IMI34 349061‐GFP [26] was cultured on potato dextrose agar (PDA) in a growth chamber under permanent light at 25°C. For infections, a fungal spore suspension of 106 spores mL−1 was prepared from 2‐week‐old cultures. Four‐ to five‐week‐old A. thaliana plants were drop‐inoculated with 5 µL of the spore suspension. The plants were then incubated in darkness for 16 h at 25°C and 100% relative humidity. Post incubation, the growth condition of the plants was changed to long day (16 h/8h day/night cycle at 25°C). Control plants were treated only with sterile water. C. graminicola M1.001 was cultivated on PDA under permanent light at 25°C; infection assays were performed on 12‐day‐old maize plants as previously described [32].
In planta fungal growth of C. higginsianum was measured every 24 h post infection for 4 days. The infection sites of the green fluorescent protein‐expressing fungal strain were illuminated using a Nikon C‐SHG1 UV lamp. Images were captured using a Nikon DS‐L1 camera and the pictures were further analysed with the help of ImageJ (
For hormone analysis, salicylic acid, jasmonic acid and abscisic acid were quantified simultaneously from leaf material using UHPLC‐MS/MS as described [32]. Hormone measurements were performed 4 days post C. higginsianum infection. To analyse each Arabidopsis accession, three independent biological replicates per sample were generated, each replicate a pool of five plants.
For metabolomic analysis, 4‐week‐old Arabidopsis plants were infected with C. higginsianum. Metabolites were isolated and analysed 4 dpi as described [32]. Six technical replicates for each treatment were analysed, and each replicate consisted of a pool of four plants.
Confirmation of down‐regulation of maize genes putatively targeted by miRNAs was conducted as described [32], using ZmGAPc as normalizing gene. Primer sequences are as follows: ZmATPS_fw: tcgtattaatgctggtgcaaac, ZmATPS_rev: ctctgtggggtggctcat; ZmSAT_fw: ttataaaaaccctgttcttctgctc, ZmSAT_rev: aggacaccttcctcaagaacc; ZmGAPc_fw: gcatcaggaaccctgaggaa, ZmGAPc_rev: catgggtgcatctttgcttg.
For sRNA library preparation, six biological replicates were pooled and total RNA was isolated using Trizol (Invitrogen,
To identify conserved maize miRNAs, sequences of 4677 mature plant miRNAs were downloaded from miRBase (release 18.0, November 2011). Identical miRNA sequences identified in different species or duplicated loci in a genome were collapsed, resulting in a non‐redundant list consisting of 2228 unique miRNAs. Sequences belonging to the same miRNA family were further analysed by multiple alignment using ClustalW (
Putative targets of maize miRNAs were identified using the psRNATarget web server (
Variances of quantified levels of metabolites and fungal growth for multiple groups were analysed by a one‐way analysis of variance (ANOVA); a P‐value of <0.05 was considered significant. The Mann–Whitney U‐test was used to compare significant differences between two sample groups. All statistical analysis was performed using Sigma Plot 11.0 (
To test if a functional silencing machinery is required for a proper antifungal‐defence response, A. thaliana wild types Ler‐0 and Col‐0 showing lower and intermediate resistance, respectively, and sRNA pathway mutants were subjected to fungal infection assays to monitor the susceptibility to C. higginsianum. To cover important components of sRNA pathways, the loss of function mutants for the genes encoding HYL1, HEN1and RDR6 was analysed. The sRNA pathway mutants were infected with C. higginsianum‐GFP, and the disease progression was compared to the relative wild‐type ecotype, for hen1‐1 namely Landsberg erecta (Ler‐0), for all other mutants Columbia (Col‐0). Fungal growth was monitored at 24, 48, 72 and 96 h postinfection (hpi) (Figure 3). These time points were chosen to cover all known infection stages of C. higginsianum during hemibiotrophic growth on leaves [25, 29]. The infection assays showed an altered susceptibility of mutants (Figure 3). For hen1‐1, a significant higher susceptibility was only detected in late infection stages (96 hpi). Comparison of hyl1‐2 with Col‐0 yielded statistically significant differences of fungal growth at all time points (Figure 3(b)). The RNA mutant was found to be more susceptible to C. higginsianum compared to the wild type. By contrast, rdr6‐15 was infected by C. higginsianum as efficiently as the wild type (Figure 3(c)). Altogether, a defective sRNA machinery seems to render plants more susceptible to fungal attack. However, mutations in RDR6‐15 did not alter the susceptibility against the C. higginsianum.
Disease severity of C. higginsianum in A. thaliana sRNA mutants and wild‐type plants; (a). hen1-1 mutant, (b). hyl1-2 mutant, (c). rdr6-15 mutant, compared to the respective wild-type background. Fungal growth was determined by quantifying the fluorescent area of C. higginsianum‐GFP in mm2 at different time points in all A. thaliana mutants compared to wild type. Severity was determined as percentage of leaf area affected. For statistical analysis, a one‐way ANOVA was applied; asterisks indicate statistically significant differences (P < 0.05). Error bars indicate standard deviation (SD).
Hormone signalling is a key process that regulates stress responses. To evaluate the implication of sRNA pathways in hormone‐mediated plant defence against C. higginsianum, levels of salicylic acid, jasmonic acid and abscisic acid were quantified by HPLC‐MS/MS. All selected mutants and wild‐type accessions were analysed 4 days post C. higginsianum infection and hormone levels of both infected and mock were measured. In response to C. higginsianum attack, SA and JA were induced to different levels in all genotypes (Figure 4). Notably, SA and JA inductions were more pronounced in the mutants hen1‐1 and hyl1‐2 compared to their respective wild‐type (Ler and Col‐0) infected plants. For instance, in infected hen1‐1 plants, JA levels rose up to 589 ng/100 mg fresh weight, whereas in infected Ler plants, JA only reached 234 ng/100 mg fresh weight. However, rdr6‐15 did not appear to have significant differences of SA and JA levels compared to wild‐type‐infected plants (Figure 4(a)(b)). On the other hand, ABA levels were found to be induced during fungal infection in hyl1‐2 and hen1‐1 contrary to rdr6‐15 that show no significant changes in ABA quantity upon fungal infection (Figure 4(c)). These results suggest that the sRNA mutant rdr6‐15 is likely not implicated in the regulation of hormone levels during antifungal responses, whereas a functional HEN1 and HYL1 protein seems to be required to mount a full SA, JA and ABA response to fungal attack.
Quantification of phytohormones in A. thaliana sRNA mutants and wild‐type plants after C. higginsianum infection. (a). salicylic acid (SA), (b). jasmonic acid (JA), and (c). abscisic acid (ABA) in A. thaliana sRNA mutants (hen1‐1, hyl1‐2, and rdr6‐15) and wild‐type plants (Col‐0 and Ler) under two treatments: infected with C. higginsianum and control. Statistical significance was determined using one‐way ANOVA. Letters indicate statistically significant differences (P < 0.05). Error bars indicate standard deviation (SD).
To compare the changes in the metabolomic profile of sRNA mutants and wild‐type plants induced by C. higginsianum infection, an UHPLC‐QTOF‐based analysis of secondary metabolites was performed. The metabolomic fingerprinting provided a global view on the metabolic perturbations induced by C. higginsianum attack at 4 dpi. Comparison of the metabolome hen1‐1 and hyl1‐2 mutants by a principal component analysis (PCA) resulted in a clear separation of both control‐treated and ‐infected mutants and their respective wild types (Figure 5(a) and (b)). The PCA performed for rdr6‐15 grouped the mutants and wild type much closer (Figure 5(c)). The metabolomic fingerprinting allowed identifying groups of putative antifungal metabolites that were normally induced in the wild type, for which in turn the mutants showed an abnormal induction pattern. After PCA analysis, the compounds showing the greatest difference between wild type and mutants were selected for further identification (Table 1). Compounds were identified by exact mass, fragmentation spectrum and the retention time of the fragments using the online free databases Metlin, MassBank, Kegg and Aracyc and the in‐house database from the chemical analytical service of the University of Neuchatel. The metabolomic analysis revealed a group of glucosinolates, flavonols, phenylpropanoids and the phytoalexine camalexine that were differentially induced in mutants and wild‐type plants (Table 1). In response to C. higginsianum, hen1‐1 mutant showed lower fold induction of some glucosinolates like 7‐methylthioheptyl glucosinolate, glucoerucin, glucoiberin, glucoiberverin and glucolesquerellin. Moreover, glucobrassicin was not induced after infection in hen1‐1 plants. Kaempferol 3‐O‐rhamnoside‐7‐O‐rhamnoside (kaempferol 3‐rha‐7‐rha) and kaempferol 3‐O‐rhamnoside‐7‐O‐glucoside (kaempferol 3‐rha‐7‐glu), flavonols which are well‐described antifungal compounds [35], were down‐regulated in hen1‐1 and Ler plants as well as the phenylpropanoids sinapoyl malate and 1‐O‐β‐D‐glucopyranosyl sinapate. The phytoalexin camalexin was the most induced compound after infection in hen1‐1 and Ler plants. Ler showed 84.4‐fold induction of camalexin while infected hen1‐1 contained 10.7 more than mock‐treated plants. The hyl1‐2 mutant exhibited lower fold induction in most of the glucosinolate levels compared to Col‐0 (Table 1). Glucobrassicin, glucoiberin and glucoiberverin levels were higher in hyl1‐2 control and infected treatments than in wild type plants. Moreover, the induction of kaempferol 3‐rha‐7‐rha and kaempferol 3‐rha‐7‐glu was higher in Col‐0 than hyl1‐2 plants. Levels of sinapoyl malate and 1‐O‐β‐D‐glucopyranosyl sinapate were also lower in hyl1‐2 control and infected plants compared to Col‐0. Camalexin was 72.9‐fold induced in Col‐0 and 69.0‐fold induced in hyl1‐2. The rdr6‐15 mutant exhibited lower fold induction of all glucosinolates, flavonols and phenylpropanoids mentioned in Table 1 compared to Col‐0. The fold induction of camalexin was similar in rdr6‐15 mutant compared to Col‐0 plants. In summary, sRNA mutant hen1‐1 exhibited lower levels of pathogen‐induced camalexin, whereas the glucosinolates, flavonol and phenylpropanoid compounds were slightly less prominently induced in response to fungal infection in all the mutants compared to their respective wild‐type plants.
Metabolites distribution in sRNA mutants and wild‐type plants upon C. higginsianum infection and control treatment. Principal component analysis (PCA) score plot of the metabolome. of the sRNA mutants hen1‐1 (a), hyl1‐2 (b), rdr6‐15 (c) and the wild‐type Ler and Col‐0 upon 4 dpi with C. higginsianum infection and control treatment. The PCA analyses were performed using Marvis Filter and Cluster packages, following a Kruskal‐Wallis test (P < 0.05). Each data point represents one replicate of six independent biological replicates.
Compound | Mass | Fragments (M‐H)‐ | hen1‐1 FI | Ler FI | hyl1‐2 FI | rdr6‐15 FI | Col‐0 FI |
---|---|---|---|---|---|---|---|
Glucoberteroin | 434.0612 | 96.9603, 95.9523 | ‐ | ‐ | 0.4 | 0.9 | 1.9 |
Glucobrassicin | 447.0512 | 96.9601, 95.9523, 74.9914 | 0.8 | 1.7 | 2.0 | 0.6 | 2.4 |
Glucoerucin | 420.0457 | 96.9628, 95.9551, 74.9943 | 1.0 | 1.6 | 0.2 | 0.8 | 1.7 |
Glucoiberin | 422.0219 | 96.9619,95.9519, 74.9923 | 0.8 | 1.4 | 1.7 | 0.7 | 1.6 |
Glucoiberverin | 406.0301 | 96.9619, 95.9494, 74.9920 | 1.1 | 2.1 | 1.0 | 0.7 | 1.4 |
Glucolesquerellin | 448.0764 | 96.9590, 95.9513,74.9919 | 1.1 | 1.6 | 1.4 | 1.1 | 2.0 |
Gluconasturtiin | 422.0578 | 0.8 | 0.8 | 2.1 | |||
Glucoraphanin | 436.0406 | 372.0467, 178.0225 | 0.7 | 1.1 | 0.7 | 0.8 | 1.8 |
7‐Methylthioheptyl glucosinolate | 462.0958 | 95.9527, 74.9920 | 1.0 | 1.6 | 1.2 | 0.9 | 1.9 |
kaempferol 3‐O‐rhamnoside‐7‐O rhamnoside | 578.1552 | 431.0942, 285.0399, 283.0236 | 0.6 | 1.0 | 1.4 | 0.8 | 1.7 |
kaempferol 3‐rhamnoside‐7‐Glu | 593.1534 | 447.0905, 285.0410, 283.0240 | 0.6 | 0.9 | 0.8 | 0.7 | 1.4 |
Sinapoyl malate | 339.0745 | 223.0586, 164.0484, 149.0245 | 0.7 | 0.9 | 1.2 | 0.8 | 1.4 |
1‐O‐β‐D‐glucopyranosyl sinapate | 385.1147 | 265.0794, 190.0267, 175.0030 | 0.8 | 1.0 | 0.9 | 0.5 | 1.2 |
Camalexin | 199.0332 | 10.7 | 84.4 | 69.0 | 71.5 | 72.9 |
Fold induction of metabolites in sRNA mutants and controls upon C. higginsianum infection.
Fold induction of identified compounds from the metabolome of the sRNA mutants hen1‐1, hyl1‐2, rdr6‐15 and the wild‐type Ler and Col‐0 upon C. higginsianum infection (4 dpi).
Using annotated maize miRNAs (zma), known miRNAs were classified in the different maize sRNA libraries. In order to determine biostress‐specific miRNAs and to quantify their expression level in the treated samples, the fold change expression was determined by calculating the relative difference of sequence reads in treated samples compared to the control libraries. Selected miRNAs showing a fold change of >2 are summarized in Table 2. Comparing biotrophic and necrotrophic fungal infection stages to mock, zma‐miR479, zma‐miR1318 and zma‐miR1432 were found to be up‐regulated; however, their fold induction was higher during the necrotrophic stage. Other miRNAs such as zma‐miR393, zma‐miR1120 and zma‐miR2092 showed an altered expression level exclusively during the biotrophic stage. By contrast, the expression of zma‐miR168, zma‐miR2916 and zma‐miR5205 was altered only during the necrotrophic stage. Notably, zma‐miR1432 and zma‐miR2092 were also up‐regulated in infected roots, suggesting that some miRNAs are regulated organ independently. Notably, infected roots showed also a distinct expression profile with zma‐miR166, zma‐miR169 and zma‐miR395 that were down‐regulated, whereas zma‐miR909 and zma‐miR2863 were up‐regulated. A different situation was found in systemic leaves upon leaf infection. Compared to local infected tissues, less miRNAs showed an altered expression. For instance, zma‐miR397, zma‐miR916 and zma‐miR5169 were up‐regulated. In systemic leaves upon root infection, zma‐miR1877 and zma‐miR2592 were down‐ and up‐regulated, respectively. Interestingly, zma‐mi395 was down‐regulated, and zma‐miR479 showed elevated expression levels; zma‐miR479 was also found to be up‐regulated in local leaf infections, whereas the down‐regulation of zma‐miR395 was also observed in infected roots. In summary, although some miRNAs were commonly regulated in both locally infected leaves and roots, the miRNA transcriptome was specific for a given infection stage and in addition also organ‐specific (Table 2). To confirm the deep‐sequencing results, Northern blots of a selected miRNA were performed. Due to the relatively high expression level and the remarkable difference between control and treated samples, zma‐miR395 was selected (Figure 6).
Northern blot analysis of miR395 expression. The signs + indicates C. graminicola infection, ‐ control tissue. H= herbivore (Spodoptera frugiperda, non‐fungus control). The tRNA and 5S rRNA are shown as a control for equal loading and were stained with ethidium bromide.
Library | miRNA | FI | Putative target genes |
---|---|---|---|
Inf L 24h | miR393 | 2.23 | Calmodulin‐binding protein MPCBP; cyclin‐like F‐box |
miR479 | 3 | Unknown | |
miR1120 | −3 | Unknown | |
miR1432 | 2.3 | Para‐hydroxybenzoate‐polyprenyltransferase (LOC100282174) | |
miR2092 | 7 | Unknown | |
Inf L 96h | miR168 | 2.7 | Argonaute and Dicer protein; ubiquitin carboxyl‐terminal hydrolase—Oryza sativa |
miR479 | 4 | Unknown | |
miR1432 | 18.3 | Para‐hydroxybenzoate‐polyprenyltransferase (LOC100282174) | |
miR2916 | 3.3 | Quinone reductase 2—Triticum monococcum; Zea mays 18S ribosomal RNA gene | |
miR5205 | −3.25 | Unknown | |
Inf R 96h | miR166 | −6.5 | MFS14 protein precursor; basic‐leucine zipper (bZIP) transcription factor; lipid‐binding |
miR169 | −3.8 | RAPB protein—Oryza sativa; allene oxide synthase—Zea mays | |
miR395 | −15.5 | ATP sulphurylase (LOC541653), mRNA | |
miR909 | 5 | Inhibin, beta B subunit; vinculin; heavy metal transport/detoxification protein | |
miR1432 | 4.5 | Para‐hydroxybenzoate‐polyprenyltransferase (LOC100282174) | |
miR2092 | 2.6 | Unknown | |
miR2863 | 3.5 | Unknown | |
Inf L sys L | miR397 | 2.2 | Laccase; multicopper oxidase; |
miR916 | 3.3 | Zein protein‐body ER membrane protein | |
miR5169 | 2.2 | Unknown | |
Inf R sys L | miR395 | −2.7 | ATP sulphurylase (LOC541653), mRNA |
miR479 | 3 | Unknown | |
miR1877 | −3 | Putative protein binding protein | |
miR2592 | 3 | Unknown |
Maize miRNAs differently regulated upon C. graminicola infection.
FI = fold induction compared to control libraries. Inf = infected, L = leaf, R = root, sys = systemic, zma = maize miRNAs.
As expected, zma‐miR395 showed a reduced expression level upon fungal infections in roots. The signal intensity also corresponded to the sequence reads in the different libraries, with the highest number of reads (93) in control roots. To examine the putative role of zma‐miR395 during root infections, the maize genome was analysed for putative target genes. Five known target genes were identified: two genes (dienelactone hydrolase and FMR1‐interacting) exhibit two mismatch positions for zma‐miR395. The other genes, ATP sulphurylase (APS) on chromosomes 1 and 5, and a sulphate anion transporter, perfectly matched to the zma‐miR395 sequence. To confirm the genotype of a reduced expression level of zma‐miR395 in infected maize roots, the gene expression of two zma‐miR395 putative target genes (ZmSAT and ZmATPS) was analysed (Figure 7).
Expression profile of ZmSAT and ZmATPS genes in C. graminicola‐infected roots.
It has been documented that plant sRNAs can act as regulators of gene expression during plant‐defence responses as reviewed in Ref. [36]. However, the mechanisms of sRNA‐mediated immunity remain largely elusive, especially for host‐fungi interactions. In rice cultivars that are susceptible to Magnaporthe oryzae, enhanced resistance could be achieved by overexpressing miR160 and miR398 [37]. MicroRNA160 targets auxin‐responsive factor 16 (ARF16), and miR398 regulates superoxide dismutase 2 (SOD2), both known defence‐related genes. In wheat, B. graminis infection was demonstrated to lead to massive adaptations of the miRNA expression profile, where miRNAs only induced in either resistant or susceptible cultivars where identified [19]. Various sRNA expression studies upon fungal infections point towards a role as fine‐tuners in the concert of setting up efficient and targeted antifungal defences, rather than having direct defensive impacts [38]. In this regard, it is not surprising that sRNAs were identified as regulators of basal immunity and R‐gene‐mediated resistance. In cotton, bioinformatic approaches revealed over 300 NBS‐LRR genes potentially controlled by the miR482 family [39], which cleave NBS‐LRR transcripts, resulting in the generation of secondary siRNAs that even enhance the silencing of multiple NBS‐LRR genes. V. dahliae infection leads to a down‐regulation of miR482, hence to a de‐repression of R‐genes.
Notably, plant RNAi pathway components were shown in specific cases to be important for mounting proper antifungal‐defence responses. RDR6‐deficient plants were found to be more susceptible to Verticillium spp. but not to Botrytis cinerea, Alternaria brassicicola or Plectosphaerella cucumerina [40]. Similarly, ago4 mutants were discovered to be more susceptible to B. cinerea and P. cucumerina [41, 42], possibly due to the over‐induction of the SA‐defence pathway which leads to diminished JA‐defence responses that are important in controlling necrotrophic pathogens.
The present study widens the understanding of the putative role of sRNAs in fine‐tuning plant‐hormonal pathways during fungal infection. First of all, Arabidopsis sRNA pathway components were demonstrated to be required for antifungal responses against C. higginsianum. HYL1‐ and HEN1‐deficient plants were more susceptible than the wild type. The higher susceptibility was accompanied by a de‐regulated hormonal response. The sRNA mutants hen1‐1 and hyl1‐2 exhibited higher SA‐, JA‐ and ABA‐induction levels. The hormonal imbalance might explain the altered susceptibility to C. higginsianum, as enhanced SA is known to be important during biotrophic infections, whereas high JA levels are typical for defence against necrotrophs [43]. On the other hand, mutation of RDR6 did not affect the susceptibility against C. higginsianum suggesting that the tasiRNA (trans‐acting siRNA) pathway is not involved in antifungal responses. Recent studies demonstrated that RDR6‐deficient plants were more resistant to the hemibiotrophic pathogen Pseudomonas syringae DC3000, presumably by a constitutive activation of the SA‐dependent‐defence pathway. Hence, it was speculated that RDR6 acts as a negative regulator of PTI and basal defence in Arabidopsis [44]. Notably, the hormonal imbalance discovered in the sRNA mutants could only partially explain the altered susceptibility, as higher JA levels were found in hyl1‐2 mutants, which would lead to an enhanced resistance during the necrotrophic stage of C. higginsianum. This suggests that sRNAs act as putative‐defence coordinators beyond hormonal pathways. Consequently, the metabolomic analysis uncovered additional layers of sRNA‐regulated antifungal responses, namely the proper induction of defence‐related secondary metabolites. Especially hen1‐1 and hyl1‐2 mutants were found to exert a massively altered defence metabolome, and to a lesser extent also the analysed rdr6‐15 mutants. sRNAs are known to be directly involved in the regulation of secondary metabolites; overexpression of miR393 for instance was shown to increase levels of glucosinolates and decreases camalexin [45], which indicates that miR393 is involved in the re‐direction of the metabolic flows. Similarly, a possible link between miR163 and the biosynthesis of secondary metabolites was described [46]. Loss or overexpression of miR163 alters the transcription of target genes and the profiles of secondary metabolites after induction by the fungal elicitor alamethicin. On the other hand, rdr6‐15 mutants showed a wild‐type‐like metabolomic profile in both infected and control‐treated conditions, despite the levels of some compounds being slightly different in the mutant after infection. The minor differences in the metabolomic profile between rdr6‐15 and wild‐type plants might be explained by the complex redundancies between the members of these protein families [3, 47]. Notably, some sRNA mutants such as hen1‐1 exhibit developmental defects, thus the genetic and metabolomic phenotype observed in response to fungi might be significantly affected by developmental pathways. However, this issue underlies all genetic studies using knock‐out mutants with severe phenotypes. Using rigid statistical criteria for compound clustering, it is possible to partially differentiate developmental from antifungal responses, as shown in the PCA analysis of infected and control hen1‐1 mutants.
To extend the view on antifungal responses possibly linked to sRNA pathways, the miRNA transcriptome of the agricultural important model crop Z. mays infected with C. graminicola was analysed. During this interaction, maize was found to set‐up an organ‐specific miRNA profile. In the locally and systemically induced fungal‐specific miRNAs, only a few were found to target defence genes. In particular, zma‐miR1432, which targets a para‐hydroxybenzoate‐polyprenyl transferase, was found to be up‐regulated during both biotrophic and necrotrophic infection stages in maize leaves and roots. The miRNA target is essential in terpenoid‐quinone synthesis. Hence, it could be speculated that its down‐regulation could divert the flow of secondary metabolites from terpenoids towards flavonoid biosynthesis. This would be coherent with the fact that terpenoids play only minor roles during C. graminicola infection in maize [48]. The second identified miRNA linked to defence pathways was zma‐miR169. This miRNA is down‐regulated in response to fungal root infections, and it putatively targets a gene encoding an allene oxide synthase (AOS). AOS is a key enzyme in JA synthesis, thus it can be speculated that zma‐miR169 acts as a suppressor of JA signalling under non‐stressed conditions, whereas the down‐regulation of zma‐miR169 during fungal infection could promote JA synthesis. The enhanced JA levels in some Arabidopsis miRNA mutants support this hypothesis. Another yet intriguing altered miRNA was zma‐miR395, which was down‐regulated in C. graminicola‐infected maize roots and systemic leaves upon root infection. The down‐regulation of zma‐miR395 was accompanied by the up‐regulation of two of its putative targets in roots, one of them encoding an ATP sulphurylase. APS plays an important role in sulphate assimilation and glutathione synthesis; inhibiting glutathione synthesis in Arabidopsis was shown to trigger the suppression of miR395 [49], thus mimicking fungal infection. It can be speculated that the down‐regulation of zma‐miR395 positively regulates sulphate‐mediated defence and/or the glutathione pathway. Intriguingly, miR168 that targets AGO1 was induced upon leaf infection, consistent with recent work demonstrating a similar fold induction of miR168 in Arabidopsis treated with elicitors of F. oxysporum [50]. Thereby, a majority of elicitor‐responsive miRNAs were shown to be associated with development and miRNA homeostasis [50], corroborating the observation that sRNA pathways likely do not regulate direct‐defence pathways.
Although some sRNA pathways components were shown here to be required for battling C. higginsianum, they seem to act as fine‐tuner of defence schemes rather than to directly regulate defence genes and defensive compounds. A common picture found for sRNA mutants exhibiting higher susceptibility to C. higginsianum was rather a hormonal and metabolomic imbalance. Moreover, the absence of altered miRNAs targeting direct‐defence genes in maize suggested an indirect defensive role of sRNAs against Colletotrichum spp.
Altogether, the strategic outline of Arabidopsis and maize antifungal defence against Colletotrichum spp. points towards the concept that sRNAs are acting as fine‐tuners mediating the balance of multiple genetic and metabolomic‐defence layers. The sRNA‐orchestrated fine‐tuning of defensive layouts may provide a genetic flexibility allowing rapid and efficient adaptation of immune pathways. The question whether sRNA pathways are indispensable and pivotal antifungal‐defence regulators remains debatable. Despite various studies showing the altered susceptibility of sRNA mutants, the general trend is that the outcome of sRNA‐mediated defence strongly depends on a specific pathosystem. This chapter adds further highlights to this picture by showing that no miRNAs targeting classical defence pathways are de‐regulated upon C. graminicola infection in maize, and Arabidopsis sRNA mutants under fungal attack appear to have altered metabolomic profile compared to the wild‐type situation.
Nevertheless, considering the fact that sRNA pathways are also involved in setting up proper abiotic stress responses, it might represent a multi‐valuable biotechnological approach to generate crops that are more efficient and variant in expressing their sRNA repertoire. Over the past years, a transgene‐based approach where pathogen‐targeting sRNAs are expressed in host species was repeatedly confirmed to efficiently control fungal diseases. This host‐induced gene‐silencing (HIGS) approach was successfully applied to a broader range of host‐pathogen systems, thus bearing a valuable industrial potential. Significant drawbacks with this technology are the restrictive acceptance of genetically modified crops, and the yet elusive question of how fast pathogens evolve tolerance or resistance. For instance, F. graminearum sRNA mutants are showing normal virulence in wheat infection assays [51]. A yet elusive question is the role of plant endogenous sRNAs in targeting the genes of their fungal parasites. B. cinerea has been demonstrated to hijack plant genes using sRNA effectors [52]; thus it could be possible that plant sRNA effectors are able to infiltrate fungal cells to act as antimicrobial molecules.
Recent studies from two different research groups demonstrate fungal control by exogenous application of sRNAs to F. graminearum [53] and B. cinerea [54]. The so‐called spray‐induced gene silencing (SIGS) might provide novel biotechnological opportunities to control fungal diseases. Although the data from both studies are promising, it remains elusive how efficient sRNAs are compared to classical biologicals, and how broadly this technology can be applied. For instance, Botrytis is one of the few fungal species known to require a functional sRNA machinery for proper infection, hence possibly representing a special situation in sRNA‐mediated plant‐pathogen interaction. Moreover, exogenous control by sRNAs was efficient in controlling fungal growth on vegetables and fruits, and not demonstrated on leaves [54], suggesting efficacy only in a very specific infection condition. Altogether, it remains to be elucidated how efficient SIGS could work in field conditions, and in particular also the application spectrum of this technology. So far, this new technology lacks confirmation by additional independent studies to allow fully evaluating its industrial potential.
Prospective investigations will help in further elucidating of the full potential of sRNA‐mediated antifungal defence. While the data presented here and in recent studies suggest that sRNAs are subtle players in the concert of mounted antifungal defence, and new approaches using exogenously applied sRNAs are promising, there remains challenging basic research to be completed first in order to truly understand sRNA trafficking and signalling in plant‐pathogen interactions.
We are grateful to Gaétan Glauser and Armelle Vallat‐Michel (Chemical Analytical Service of the University of Neuchâtel) for their technical assistance in metabolomics and hormone analysis. Financial support from the National Centre of Competence in Research ‘Plant Survival’ and grant number 31003A‐120197, both research programmes of the Swiss National Science Foundation, is gratefully acknowledged.
The perception of pain is an integral part of human existence. Although uncomfortable to the individual, the perception of pain is necessary to protect the body from harm. A painful sensation causes man to seek an explanation for the reason of this discomfort. A brief history of the origins of pain and the development of pain medications is presented, followed by the current understanding of the physiology of pain and modern concern about opioid use. In the second half of the twentieth century, synthetic opioids were introduced to achieve hemodynamic stability during anesthesia. Furthermore, combined with hypnotics and muscle relaxants, the opioids administration is considered a keystone of anesthesia. For instance, a prevalence of 30% of unwanted effects of opioids such as nausea, vomiting, dizziness and constipation has been reported [1]. An increased occurrence of confusion and postoperative delirium [2], respiratory depression, increased postoperative pain and opioids consumption with abuse, immunodepression, hyperalgesia and chronic postoperative pain have also been described. Of note, opioid tolerance to analgesia can occur after a single dose. Thus, the management of pain in surgery is currently moving in the direction of the reduction of opioid use preoperatively, perioperatively, and postoperatively. The modern multimodal anesthesia and analgesia with intraoperative hemodynamic stability, immobility and anticipation of postoperative analgesia can be achieved without opioids. The concept of opioid-free anesthesia (OFA) is based on the idea that hemodynamic stability can be obtained without opioids during anesthesia. In particular, OFA is a fascinating multimodal approach to anesthesia which provides the combination of hypnotics, N-methyl-D-aspartate (NMDA) antagonists, local anesthetics, anti-inflammatory drugs and alpha-2 agonists such as dexmedetomidine, and no intra-operative systemic, neuraxial, or intracavitary opioid is administered during anesthesia and the perioperative course. This strategy is aimed to prevent postoperative opioid-related adverse effects and to enhance recovery after surgery.
\nEarly theories of the origin of pain, especially from internal diseases, revolved around demonic and religious beliefs. Shamans and sorcerers treated patients with the use of amulets, magic sculptures, talismans, magic ceremonies and rituals to ward off demons and evil spirits. It was believed that spirits and demons should leave the body from the same way it entered, resulting in cultural scarifications to allow bad fluids, spirits and demons to escape. In Egypt, religious ceremonies and prayers were believed to help relieve pain. Incantations to God Horus and other deities were thought to relieve unilateral headaches [3].
\nAncient cultures have used leaves of cocoa plant and opium for religious and medical purposes. The earliest anthropological evidence of the use of cocoa leaves was from the pre-Inca culture in Peru, dated to 1300 B.C. The Peruvians used cocoa leaves as a local anesthetic in trepanation operations. Opium was introduced to Egypt around 1500–1300 B.C., and was used as a cream for external application and for the fumigation of toothaches. In India and China, opium was used for the treatment of toothache and joint pain. In these cultures, opium could not be separated from its “recreational” use [3].
\nIn the seventeenth century, physicians began to consider the human body as a machine with different parts in constant motion. The French philosopher Rene Descartes proposed one of the earliest concepts of modern physiology: a movement or touch initiated at the peripheral nerve endings propagated to the brain. This concept, which formed the basis of nineteenth century pain theories, is illustrated by Descartes famous figure [3] of a boy, whose foot is being stimulated by heat from a fire. Several scientific discoveries followed Descartes physiologic concept of pain, including that of Sir Humphrey Davy’s reports of pain relief from inhalation of nitrous oxide in 1800 and James Moore’s report of opium use for postoperative analgesia in 1784 [3].
\nWith a better understanding of the physiology and pathways of pain, pharmacologic discoveries, particularly of morphine, were made in the beginning of the nineteenth century. The German pharmacist Friedrich Wilhelm Adam Ferdinand Serturner was the first to isolate morphine from poppy in 1805. He named the substance after Morpheus, the Greek god of sleep. The invention of the hypodermic hollow needles and syringes by Charles Gabriel Pravaz and Alexander Wood in the 1850s allowed the ease of subcutaneous application. While this helped the widespread use of morphine, it also paved way for the use and abuse of morphine that spread rapidly during the American Civil War (1861–1865) and the French-German War (1870–1871). Opioid addiction became known as the “soldier’s disease” and spurred research efforts to find substances with a lower risk of abuse [3].
\nStemming from the discovery of morphine, scientists began to experiment and develop different forms of morphine. In 1874 Charles Adler Wright synthesized diacetyl-morphine, which in 1898 was registered under the name of heroin. This drug showed stronger cough suppression but lower analgesic effects when compared to morphine in animal models. Toward the beginning of the twentieth century, addiction to heroin became a growing problem in the USA, and in 1914, the government began implementing stricter regulations, limiting the maximum amount of heroin in preparations. These regulations also prohibited opium, morphine, cocaine, and several other substances from non-prescription preparations [3].
\nThe development of new opioid analgesics continued. Derivatives of morphine and codeine such as hydromorphone, dihydrocodeine, hydrocodone, oxymorphone, meperidine, and oxycodone emerged at the beginning of the twentieth century. Methadone was developed during World War II in Germany and was used primarily as a substitution therapy in drug addicts. Methadone is a μ-receptor agonist and a noncompetitive NMDA antagonist. The NMDA receptor is involved in the pathophysiology of neuropathic pain. Fentanyl was developed by Paul A.J. Janssen in 1953 and was proved to be approximately 40 times more active than morphine. Subsequently, similar compounds with stronger potency developed, including carfentanil, sufentanil, and alfentanil [3].
\nThe techniques for pain relief, such as spinal cord analgesia, knee surgeries, and different routes of administration for medications, began to develop after further research suggested opioid receptors in the human brain and the demonstration of endogenous opioids, the endorphins and enkephalins, constituting an internal system of pain modulation. Opioid receptors were found in high density in the substantia gelatinosa of the spinal cord, as well as the limbic system and periaqueductal gray area of the brainstem. This led to the reintroduction of spinal opioid application in clinical medicine. Peripheral opioid receptors were demonstrated in the late 1980s, and Stein and colleagues showed reduced operative pain following arthroscopy of the knee joint following intraarticular injection of morphine. Sustained release formula and transdermal route of administration provided a profound impact on the management of chronic pain. It made pain management much more comfortable for the patients, resulting in an improved quality of life. Morphine was available in the sustained release formula in 1983, while fentanyl was available in the transdermal system. Various opioids in sustained release formula and transdermal systems followed [3].
\nSurgical anesthesia experimentations in the nineteenth century allowed for major development in pain-free surgeries. One of particular note was the Dr. William Morton’s experimentation with ether as a local anesthetic for a surgical neck operation. The dentist Horace Wells previously used gas during teeth extraction procedures. The first surgical ether anesthetized procedure was by the dentist William Thomas Green Morton at Massachusetts General Hospital, Boston, in 1846. Dr. John C. Warren was the senior surgeon operating on a congenital vascular tumor on the neck of a young man, Gilbert Abbott. To the audience’s amazement, Abbott did not cry out in pain during the procedure, and this ushered in the era of pain-free surgery [3]. Painters Warren and Lucia Prosperi were commissioned in 2000 to immortalize this milestone in anesthetic surgery with a painting that became known as the Ether Dome painting.
\nFurther significant steps in anesthesia in surgical environments continued. The use of chloroform in the management of childbirth was introduced into the medical world by Sir James Young Simpson in 1847, the same year physiologist Marie Jean Pierre Flourens had discovered the anesthetic properties of chloroform in animals. Chloroform remained the preferred anesthetic until the end of the nineteenth century even though the use of chloroform resulted in significantly more deaths than with ether [3].
\nCocaine in local anesthesia marked another milestone in the advancement of pain management in surgery. During the nineteenth century, Albert Niemann, a scientist from Gottingen, isolated cocaine out of the mixture of alkaloids of the cocoa plant. The extracts became popular for conditions such as toothaches, digestive disorders, hysteria, and melancholia, as well as for being an aphrodisiac. Carl Koller experimented with cocaine as a local anesthetic on frog eyes, other animals, his assistants, and even himself. His paper, which demonstrated cocaine’s efficacy, was presented at the Heidelberg Ophthalmological Society in 1884 by his colleague Josef Brettauer. The presentation was widely received and others began experimenting with cocaine’s surgical applications [3].
\nAfter the Heidelberg presentation, scientists began experimenting with cocaine as a nerve block, in advanced cancer patients, and in spinal cord operations. American surgeon William Steward Halsted [4] began experimenting with cocaine as a nerve block, which opened up new possibilities in surgery anesthetics. Halsted and several of his colleagues eventually became addicted to cocaine during their experimentations with the drug. James Leonard Corning used cocaine as a spinal anesthetic in 1885. Dr. Herbert Snow was the first physician to incorporate cocaine into cancer pain treatment. In 1896, he administered cocaine with opium for pain relief to patients with advanced diseases. He later developed the “Brompton Cocktail,” a mixture containing morphine, cocaine, and alcohol. German surgeon August Bier and his colleagues published their clinical results of spinal anesthesia, including intrathecal injections on each other. He introduced intravenous regional anesthesia in 1908. Rudolph Matas administered the first morphine anesthetic to the spinal cord in 1909. Most of the nerve blocking techniques during this time period were developed for surgical anesthesia [3].
\nFurther experimentation with cocaine as an analgesic continued during the nineteenth century, resulting in the development of new local anesthetics including synthetic substitutes. Alfred Einhorn synthesized procaine in 1905. Lofgren and Lundqvist synthesized Lignocaine in 1943. Other local anesthetics followed including cinchocaine and amethocaine in the 1920s, mepivacaine, prilocaine, and bupivacaine in the late 1950s, etidocaine in the 1970s, and ropivacaine in the 1980s [3].
\nThe current understanding of the physiology of pain involves the activation of the nervous system. Noxious stimuli, including intense thermal, mechanical, or chemical stimuli, are recognized by nociceptors in the peripheral nervous system. The threshold for pain activation is relatively high, requiring a large stimulus for signal propagation. The signals either travel through Aδ-fibers, Aβ-fibers, or C-fibers. While the Aδ-fibers and Aβ-fibers are myelinated and transmit “acute, well-localized, fast pain,” the C-fibers are unmyelinated and transmit “slow” pain, often described as an ache. The signals travel to the dorsal root ganglion, are transmitted through the spinal cord and synapse on the somatosensory cortex and limbic system. The modification of this pathway by medications aims to reduce or eliminate pain [5].
\nAlthough opioids have historically been significant medications in the management of pain, opioids have also been the source of significant public health concern because of the addictive and destructive adverse effects of the medication. During the twentieth century, there were positive attitudes for the use of opioids, as a letter written to the New England Journal of Medicine underscored the safety and low addictive potential of opioid use in chronic pain patients, with subsequent letters and reviews supporting this perspective. With the impression that there was very little risk, particularly of addictive potential, in prescribing opioids for chronic pain, the demand for opioid use increased in clinical settings. However, by 2000, attitudes are beginning to shift and a reduction of opioid use is becoming the trend [5].
\nThe detrimental overuse, abuse and addiction of opioids can precipitate from prolonged treatment of opioids. Opioid tolerance occurs when there is a reduction in the analgesic and sedative effects of these medications. Tolerance to the euphoric effects also develop, further increasing the risk of addiction. Opioid dependence results from the overactivation of the somatomotor cortex and autonomic nervous system due to the increased signaling of the cells while on the inhibitory medications. Cessation of opioid use or the administration of opioid receptor antagonists such as naloxone or naltrexone cause the withdrawal symptoms, including diarrhea, vomiting, agitation, hyperalgesia, hyperthermia, and hypertension [5].
\nIn the United States, the opioid abuse has reached epidemic proportions and have become a public health issue. The treatment of opioid dependence is unclear, but there have been significant public health prevention efforts to combat the trends of increased abuse and overdose deaths [5]. On the topic of opioid epidemic, the United States Surgeon General Dr. Jerome Adams supports overdose education and awareness, and suggests co-prescribing naloxone to patients on high morphine milligram equivalent who are at risk [6]. Nearly all the U.S. states have laws supporting naloxone provision to lay persons. Further, the U.S. Department of Health and Human Services highlighted naloxone rescue kit access and emergency overdose as a priority to address the opioid crisis. The benefits of naloxone programming have been demonstrated in San Francisco, as well as in North Carolina, where a 70% decline in prescription opioid-related overdose death rates was observed from 2009 to 2010 [7].
\nThe current trend in surgery is in the direction away from general anesthesia that traditionally requires opioids preoperatively, intraoperatively, and postoperatively, and toward a more multi-modal regimen approach with preoperatively patient education, specifically highlighting the interplay between opioids and the human body’s natural pain management system.
\nCurrently, many surgical operations have been traditionally performed under general anesthesia with adjunct opioid use. The main mechanism of action of opioids is the stimulation of μ receptors, which has inhibitory effects on the propagation of pain signals to the brain [8]. However, there are a wide variety of associated adverse effects of opioids including nausea, vomiting, constipation, postoperative sedation, dizziness, and addiction [9]. Opioid use also carries significant morbidity, prolong hospital stays, increase use of medications needed to reverse side effects, and decrease patient satisfaction [10, 11]. Further, opioids may also cause paradoxical hyperalgesia due to opioid-induced neural plasticity. This appears to affect both the central and peripheral nervous systems, and may lead to sensitization of the pain pathways [12].
\nIn addition to the wide variety of adverse effects, opioids use may also hamper the effects of the human body’s own natural pain killers, endorphins. Opioid administration reduces the production of beta-endorphins and impairs the function of mu-opioid receptors [13]. Beta-endorphins have significant natural analgesic effects and have been proposed to yield 18–33 times greater analgesic potency than morphine. Endorphin release is believed to enhance in response to a stressor, such as sharp pain, and can be quickly utilized to control the pain. The stressor causes the hypothalamus to release corticotrophin-releasing hormone (CRH), a peptide hormone and neurotransmitter, from the periventricular nucleus. CRH stimulates the cleavage of protein proopiomelanocortin (POMC) from basophilic cells, resulting in smaller proteins, one of them being beta-endorphin. In the peripheral nervous system, beta-endorphins bind to the μ receptors on both pre-synaptic and post-synaptic nerve terminals. The binding leads to the release of gamma-aminobutyric acid (GABA), which inhibits the release of substance P, a tachykinin protein involved in the transmission of pain. Endorphins not only have greater analgesic potency than morphine, but also enhances individuals’ mood and well-being, due to indirect elevation of dopamine [13]. In the central nervous system, beta-endorphins bind the μ receptors on the pre-synaptic nerve terminals and inhibit release of GABA, which normally inhibits the release of dopamine. The overall effect of beta-endorphins, which is decreased in opioid use, is a decrease in pain and an elevation in wellbeing.
\nOpioid-free anesthesia is an anesthetic technique without intraoperative systemic, neuraxial or intracavitary opioids, and that avoids perioperative opioids. There are a number of therapeutic uses and indications for opioid-free anesthesia including narcotic history (acute and chronic opioid addiction), opioid intolerance, morbidly obese patients with obstructive sleep apnea, hyperalgesia, history of chronic pain, immune deficiency, oncologic surgery, inflammatory disease, chronic obstructive pulmonary disease, and asthma [14].
\nPostoperative complications, such as respiratory depression, central muscle rigidity, pharyngeal muscle weakness, obstructed breathing, negative inotropism, nausea, vomiting, ileus and constipation, urinary retention, tolerance and addiction, dizziness, and excessive somnolence, can be reduced or prevented. Decrease histamine release (allergy/anaphylaxis), increase patient satisfaction, and enhanced recovery after surgery and anesthesia (ERAS) are other beneficial effects of opioid-free anesthesia [14, 15, 16].
\nOpioid-free anesthesia should be avoided in patients with allergy to any adjuvant drugs, and should be used cautiously in patients with disorders of autonomic failure, cerebrovascular disease, critical coronary stenosis, acute coronary ischemia, heart block, extreme bradycardia, non-stabilized hypovolemic shock or polytrauma patients, controlled hypotension for minimal blood loss, and elderly patients on beta-blockers.
\nInterest and use of adjuvant modalities, including ketamine, gabapentinoids, intravenous lidocaine, magnesium sulfate, alpha-2 adrenoreceptor agonists, and beta-blockers, is increasing because of enhanced recovery, particularly in specific patient populations like chronic pain and opioid dependent patients [15].
\nIn light of the serious adverse effects associated with opioids, many clinicians are forgoing prescribing opioids excessively and using opioid alternatives for postoperative pain control. These non-opioid alternatives, including acetaminophen, nonsteroidal anti-inflammatory drugs (NSAIDS)/cyclooxygenase-2 (COX-2) inhibitors, gabapentin, local anesthetic infusion pumps, paravertebral or transverse abdominis plane nerve blocks, long-acting local anesthetics, and botulinum toxins, have been shown to produce analgesic effects and decrease opioid use postoperatively. Combinations of non-opioid alternatives have been shown to be superior in the management of postoperative pain and opioid requirements. In 2008, Parsa demonstrated that gabapentin and celecoxib in combination preoperatively for subpectoral breast augmentation was significantly superior than celecoxib alone in reducing postoperative pain and opioid use [17]. Stephan and Parsa have extensive experience using non-opioid modalities of postoperative pain control, which has resulted in significant reduction in opioid administration postoperatively for patients undergoing various plastic surgery procedures [13].
\nSeveral other opioid reduction strategies in a surgical setting have been tested and shown to be effective in managing pain and decreasing opioid use. Preoperative patient education has shown to be effective in reducing the opioid requirement postoperatively. Sugai et al. demonstrated that preoperative oral and written education concerning the body’s response to pain reduced preoperative and postoperative opioid prescriptions [18]. When comparing patients that had opioid-free procedures to the patients receiving adjunct opioids, Parsa et al. found statistically significant reduction in time from end of operation to discharge, unplanned postoperative hospital admissions, and opioid use in the post-anesthesia care unit [19].
\nPain treatment and management has come a long way since ancient cultures. Several innovations during the nineteenth century made significant headway in opioid analgesics, and by the end of the twentieth century, hemodynamic stability during anesthesia was achievable through the application of opioids. However, in an era with significant opioid abuse, limiting opioid requirements in postoperative pain management is of greater importance. Opioids are associated with unwanted side effects, including nausea, vomiting, dizziness, constipation, and hyperalgesia. Not only are there several adverse effects with opioid use, including a high addictive potential, opioids also interfere with beta-endorphins, the human body’s potent natural analgesic. Opioid-free anesthesia provides a technique that can achieve intraoperative hemodynamic stability, immobility, and postoperative analgesia without opioids, and therefore, in the absence of the significant associated side effects. Judicious utilization of adjuvants like ketamine, gabapentinoids, intravenous lidocaine, magnesium sulfate, alpha-2 adrenoreceptor agonists, and beta-blockers contribute to enhanced recovery in specific patients with chronic pain and opioid dependence. Opioid-free anesthesia and other opioid-free pain relief strategies are essential in the control of the opioid crisis, are key in effective analgesia without unwanted opioid-related side effects, and are needed for postoperative recovery.
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\n\nWe have adopted the Protocol to increase the number of readers of our publications. All our Works are more widely accessible, with resulting benefits for scholars, researchers, students, libraries, universities and other academic institutions. Through this method of exposing metadata, IntechOpen enables citation indexes, scientific search engines, scholarly databases, and scientific literature collections to gather metadata from our repository and make our publications available to a broader academic audience.
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