Characteristics of the patients examined before treatment
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\r\n\t[5] N. C. Panoiu, W. E. I. Sha, D.Y. Lei, G.-C. Li. Nonlinear optics in plasmonic nanostructures. Journal of Optics, 20, 2018, pp. 1-36.
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\r\n\t
The immune synapse is the interface between an antigen-presenting cell and a lymphocyte [1-4] as well as the interface between different lymphocytes, Natural Killer cells, and target cells [5]. This intercellular connection serves as a focal point for exocytosis and endocytosis [6]. Numerous investigations have elucidated the structure of the immunological synapse. The synapse is composed of a central region: a central supramolecular activation complex SMAC [cSMAC], a T cell receptor (TCR) cluster and associated signaling proteins, and peripheral SMAC ( pSMAC) of a ring of tight adhesion between the reacting cells [7]. The separated space of SMAC is the place of exocytic and endocytic events in this site but the precise site of signaling is not known [8]. The early signaling process occurs in peripheral microclusters in the pSMAC and the cSMAC in T and B cell synapses [9-12]. CD4 T cells form long-lived synapses with APCs – the synapses live few hours. CD8 T cells form transient synapses, lasting only minutes, because the target cells are killed [13,14]. In this cytotoxic synapse, activated Src kinases were detected in the cSMAC [13]. The cSMACs play an important role not only in signaling but also in receptor recycling because endosomal compartments polarize to the point immediately beneath the cSMAC of the immunological synapse [15]. The endosome comes to lie underneath the cSMAC as polarization of the microtubule skeletons occurs during synapse formation. This polarization is antigen-dependent. The receptor activation leads to accumulation of actin across the synapse and formation of an outer ring around the synapse [16,17]. The cytotoxic reaction of lymphocytes CD8 is connected with release of specialized lysosomes containing the lytic pore-forming protein perforin, which enables gransymes to lead to rapid apoptosis of the target cell [17]; the centrosome in the lymphocytes is polarized right up to the plasma membrane containing the synapse cSMAC [18]. The lytic granules are delivered to a specialized secretory domain within the synapse by moving along the microtubules toward the centrosome. Granule contents are then released into a small cleft between the two cells [17]. Since the overall levels of surface and endocytosed proteins remain the same regardless of ICAM-1, this suggests that ICAM-1–LFA-1 engagement in the pSMAC acts to restrict and focus endocytic and exocytic events to the center of the synapse. Griffiths suggests that the centrosome may play a role in identifying a specialized area of membrane for focal endocytosis and exocytosis [6]. An important role in formation of the immunological synapse is played by the localization of mitochondria – the mitochondria can activate and terminate the activity of immune synapses [19]. The in vivo image of T cell activation is slightly more complex. In an experimental system that uses subcutaneous injection of labeled LPS-activated dendritic cells followed by intravenous injection of naive transgenic CD8+ T cells, behavior of these cells and a three-phase model for T cell activation were observed: [20]. Phase 1 includes initial transient T cell–DC interactions characterized by continued rapid T cell migration that can last from 30 min to 8 h depending on the pMHC density. Signals in phase 1 are integrated through kinapses. Phase 2 is a period of stable T cell–DC interactions lasting ∼12 h, during which cytokines such as IL-2 are produced. Signals in phase 2 are integrated through the immune synapse. Phase 3 is a return to transient T cell–DC interaction and rapid T cell migration during which the T cell divides multiple times and then exits the lymphoid tissue. The correct interpretation of these stop and go signals is critical for generation of effector and memory T cells [21,22].
The aim of the study is presentation of the ultrastructure of immune synapses between T- cells and plasma cells and target cells in vivo in autoimmune thyroid diseases.
A group of children and adolescents was chosen for the study to exclude the impact of aging processes and other diseases connected with age: circulatory disorders, arterial sclerosis, and drug use.
The study involved 90 children: 30 children affected with Graves’ disease, 30 children with Hashimoto’s thyroiditis and 30 children as a control group. The children were treated in the Department of Pediatric Endocrinology and Neurology in Lublin and in the Pediatric Department in Rzeszow in the years 1994 – 2007 and operated on in the Surgery Department of the Regional Hospital in Lublin and in the Regional Hospital in Rzeszow.
The investigation was accepted by the local Ethical Committee at the Medical University in Lublin.
The control group consisted of 30 children aged 6-19 who had died in accidents and of other non-autoimmune diseases; the thyroid specimens were taken during autopsy (n=25). Some specimens were taken during a surgical operation of thyroglossal cysts and during surgery of parathyroid glands (n=5). These were fragments of routinely sampled tissue specimens for standard pathologic investigations. All the children were in euthyreosis [Tab.1]. All children’s parents signed an informed consent before autopsy or surgical operation.
All patients’ parents signed an informed consent before these investigations.
All the patients received physical examination to assess the goiter and clinical signs and symptoms of thyroid disorders. The TSH (Thyroid-stimulating hormone), fT4 (free thyroxin) and TT3 (total triiodothyronine) hormones were assayed by MEIA (Abbott Kit, Langford, Ireland). The levels of TSH receptor antibodies were measured by RIA (TRAK assay BRAHMS Diagnostica GmbH, Berlin, Germany). The thyroperoxidase (TPO) and thyroglobulin (TG) antibodies were assayed by LIA (Lumitest BRAHMS Diagnostica GmbH, Berlin, Germany).
In the patients with Graves’ disease, symptoms of thyrotoxicosis: goiter, tachycardia, sleeplessness, anxiety, high diastolic/systolic blood pressure amplitude, an increase in fT4 (mean 3.8± 0.7 ng/dl) and TT3 (mean 363±175.3 ng/dl), and a decrease in TSH (mean 0.004±0.003 mU/l) were observed. The levels of antibodies against the TSH receptor (TRAB) (7-462U/ml) and the levels of TPO antibodies (21-6663U/ml) and TG antibodies (25-13351U/ml) were usually increased. The patients were treated with methimazole in initial doses 0.9-0.5 mg/kg b.w./day during 4-6 weeks and after that time, when in euthyreosis, they got maintenance doses c.a.0.1 mg/kg b.w./ day (mainly 5mg/day) in combination with a low dose of l-thyroxin (25μg/day) during 18-24 months. Children with Graves’ disease, whose early relapses of hyperthyreosis necessitated surgery treatment – thyroidectomy after 18-36 months, were qualified for the investigation [Tab. 1].
Hashimoto’s thyroiditis was recognized in patients with parenchymal or nodular large size goiter accompanied by pressure to other neck structures in the phase of euthyreosis or hypothyreosis, rarely in hyperthyreosis (Hashitoxicosis). In ultrasonography, a non-homogenous structure of the thyroid was observed. The levels of TPO Ab and TG Ab were increased, but the levels of the TRAb were in normal ranges. In histopathological examination, mononuclear lymphatic infiltrations in the thyroid parenchyma were detected, and Hashimoto’s thyroiditis was diagnosed. Before surgery, the patients were usually treated with l-thyroxin 25-100 µg/day. [Tab. 1].
\n\t\t\t | \n\t\t\t\tPatients number\n\t\t\t | \n\t\t\tAge [years] | \n\t\t\tTSH mIU/L | \n\t\t\tfT4 ng/dl | \n\t\t\tTPO Ab IU/L | \n\t\t\tTG Ab IU/L | \n\t\t\tTSI IU/L | \n\t\t
Graves’ disease | \n\t\t\t30 | \n\t\t\t5-19 | \n\t\t\t0,001-0,005 | \n\t\t\t3,3-5,1 | \n\t\t\t21-6663 | \n\t\t\t25-13351 | \n\t\t\t7-462 | \n\t\t
Hashimoto\'s thyroiditis | \n\t\t\t30 | \n\t\t\t8-19 | \n\t\t\t0,600-98,800 | \n\t\t\t0,1—2,3 | \n\t\t\t132-9856 | \n\t\t\t128-14567 | \n\t\t\t0-0,99 | \n\t\t
Control group | \n\t\t\t30 | \n\t\t\t6-19 | \n\t\t\t0,270-4,200 | \n\t\t\tx | \n\t\t\tx | \n\t\t\tx | \n\t\t\tx | \n\t\t
Normal ranges | \n\t\t\t\n\t\t\t | \n\t\t\t | 0,270-4,200 | \n\t\t\t0,8-2,3 | \n\t\t\t<34 | \n\t\t\t<115 | \n\t\t\t<1 | \n\t\t
Characteristics of the patients examined before treatment
Specimens for ultrastructural investigations were obtained during thyroidectomy. Small segments of thyroid were cut into 0,5mm³ pieces and fixed in 4% glutaraldehyde in 0,1 M cacodylate buffer, pH 7.4 for 24 h in 4ºC, post fixed in 2% OsO4 in the same buffer for 1h in room temperature, dehydrated in a graded series (up to 100%) of ethanol and embedded in 812 Epon. They were then polymerized at 60ºC. Five specimens were taken from every thyroid from each patient with Graves’ disease, Hashimoto’s thyroiditis, and from the control group. Epon blocks were cut with an RMC MT-7 ultramicrotome, USA. From every specimen were analyzed serial 10 slides. Ultrathin sections were contrasted with uranyl acetate and lead citrate and examined under the EM 900 Zeiss Germany Electron Microscope.
In the control group of children without a thyroid disease, lymphocytes in the interstitium of the thyroid gland were observed sporadically. The lymphatic cells did not cross the basal membrane of thyroid follicles, were not in contact with thyrocytes and did not form groups. In Graves’ disease, T cells that crossed the basal membrane of the vesicles were observed to be in contact with thyrocytes. The lymphocytes migrated to thyroid follicles from capillary vessels or from lymphatic follicles. The migrating T-cells had numerous projections – lamellipodia on their surface. Polarization of cell organelles was already visible in narrow capillaries. The lamellipodia, mitochondria, and the Golgi system were located in the same part of the lymphocyte [Fig.1]. T cells, which penetrated across the basal membrane between thyrocytes, looked similar [Fig. 2]. The T- cells formed numerous junctions with thyrocytes. The structure of these connections was similar to zonula occludens with an area of cell membrane fusion and area of free spaces between cells, in which protein substances were secreted [Fig.2]. The T-cells were not polarized in those connections with thyrocytes. The thyrocytes were not damaged, but were active and had numerous mitochondria, secretory vesicles and a big amount of euchromatin in the nuclei [Fig. 2].
The lymphocyte migrating in the capillary vessel. Polarization of the lymphatic cell is visible: lamellipodia, mitochondria, and Golgi complex are present on the same side. N- nucleus, M- mitochondria, G-Golgi system, RBC- red blood cell. TEM magn. 15 000x
The lymphocyte between thyrocytes in the thyroid follicle in Graves’ disease. The lymphocyte formed numerous immune synapses with the thyrocyte. The immune synapses are limited by zonula occludens (pSMAC with fusion of cell membranes). The space (cSMAC) is visible in the center of the immune synapse. The thyrocytes are active without signs of damage. RER – rough endoplasmic reticulum, M-mitochondria, V-secretory vesicle, MB- basal membrane, IS- immune synapse. TEM magn. 15 000x.
In Hashimoto’s thyroiditis, the sites of contact between T-cells and lymphocytes had the character of an immune synapse, too. The synapse, however, looked different. The T-cells were polarized – the centrioles, mitochondria, Golgi system, and secretory vesicles were present in the part connected with the thyrocytes. The synapse was composed of a distal part – an adhesion zone, and a central part – a space in which electron dense substances were secreted [Fig.3]. The thyrocytes staying in contact with T-cells exhibited the features of apoptosis: dark, concentrated heterochromatin in the nucleus, swollen mitochondria, and enlarged cisterns of endoplasmic reticulum.
The lymphocyte between thyroid follicles in Hashimoto’s thyroiditis. The lymphocyte is connected with the thyrocyte by an immune synapse limited by zonula adherens without cell membrane fusion (pSMAC). The space (cSMAC) is visible in the center of the immune synapse. The lymphocyte organelles are polarized under the synapse: centriole, mitochondria, granules, and Golgi complex. Signs of damage are present in the thyrocyte: enlarged cisterns of rough endoplasmic reticulum. C-centriole, M-mitochondria, G-Golgi system, L-lysosome, RER- rough endoplasmic reticulum, N-nucleus. TEM magm.25 000x
In AITD, synapses between plasma cells and thyrocytes were observed. In Graves’ disease, synapses were formed in the distal part – zonula adherens - without fusion of thyrocyte and plasmocyte cell membranes and in the central part - the space between membrane of plasma cells and thyrocytes. Electron dense substances from the rough endoplasmic reticulum of the plasma cells – most probably immunoglobulins - were secreted to this space [Fig.4]. Immunoglobulins encrusted the basal membrane of thyrocytes.The thyroid cells staying in contact with plasma cells were active: with a big amount of euchromatin in the nucleus, numerous secretory vesicles, and abundant microvilli [Fig.4].
The plasma cells in contact with thyrocytes in Graves’ disease. a) The space of the immune synapse in which electron dense substances, probably antibodies, are secreted. Enlarged cisterns of endoplasmic reticulum were observed in the thyrocyte. RER-rough endoplasmic reticulum, CM cell membrane, * immunoglobulins. TEM magn. 25 000x. b)The advanced phase of the immune reaction: the deposits of immunoglobulins in the space between the thyrocyte and plasmocyte. The space of the immune synapse is limited by zonula adherens. CM – cell membrane, RER – rough endoplasmic reticulum, * immunoglobulins deposit. TEM magn. 25 000x
In Hashimoto’s thyroiditis, polarization of plasma cells was observed; the centrioles and Golgi system, mitochondria and well-developed rough endoplasmic reticulum were observed in the part connected with thyrocytes. In some areas of the contact places, secretion of substances with medium electron density from plasma cells to thyrocytes was observed [Fig.5]. The plasma cells adhered in a large area to thyrocytes, and the thyrocytes exhibited features of damage and destruction: fragmentation of the endoplasmic reticulum, edema of mitochondria, and condensation of the chromatin in the nucleus. In advanced stages, destruction and fragmentation of thyrocytes were observed.
The plasma cell in contact with thyrocyte in Hashimoto’s thyroiditis. The immune synapse is composed of a surrounding adhesion zone (pSMAC) in the central part of the site of exocytosis of electron dense substances and vesicles from plasma cell. Polarization of the organelle is visible in the plasma cell: centrioles, lysosomes, and mitochondria in the region of immune synapse. The thyrocyte is damaged with edema of mitochondria and destruction of endoplasmic reticulum. C-centriole, M-mitochondrium, RER- rough endoplasmic reticulum, N-nucleus. TEM magm.25 000x
The immune synapses occurring in the thyroids of patients with Graves’ disease were similar to the synapse described by Dustin [23]. Dynamic studies with planar bilayers further showed that the immune synapse was formed through a nascent intermediate in which activating TCR clusters are formed first in the pSMAC and then move to the cSMAC region in an F-actin-dependent process in a few minutes to form the pattern [7].
In the connection between thyrocytes and T-cells, the zonula occludens in Graves’ disease and zonula adherens in Hashimoto’s thyroiditis seem to be the peripheral pSMAC and the space in the center can correspond to the central supramolecular activation complex cSMAC.
An interesting observation is the difference in polarization of lymphocytes in immune synapses. The lymphocyte stimulating thyrocytes in Graves’ disease were not polarized, but the cytotoxic lymphocytes in Hashimoto’s thyroiditis had polarized organelles in the cytoplasm.
The polarization of the T-cell, i.e. formation of a center with a centriole, mitochondria, and Golgi complex suggested special organization of the cellular tubules and filaments. Actin filaments (F-actin) play a critical role throughout the various stages of T cell activation. In the steady state, actin polymerization at the leading edge and cytoskeletal contraction at the lamelliopodium mediate rapid migration [24].The microtubule organizing center (MTOC) and microtubule network of the cell provide a molecular way for vesicle movement and structural support for polarized cell functions. Within seconds after TCR stimulation, the MTOC mobilizes and polarizes to the immune synapse in T cells. Polarization is important for efficient trafficking and directed secretion of cytolytic granules and cytokines for secretion at the synapse [25-27]
Previous studies [28-30] report that mitochondria accumulate at the immunological synapse following T-cell stimulation. The fusion factor DRP1 (dynamin-related protein 1) regulates mitochondria positioning close to the peripheral supramolecular activation cluster (pSMAC), which together with the central SMAC forms the immune synapse in T cells [19]. The immune synapse controls calcium signals and calcium-dependent T-cell functions [31]. Our observations in vivo are similar to pictures from the electron microscope from investigations in cell culture published by Tsun [32].
Probably, the polarization of organelles in the cytotoxic lymphocytes observed is connected with transport of cytotoxic substances from these cells to thyrocytes.
Stinchcombe [33] observed NK cells conjugated with B-cells with glycolipid-pulsed CD1-bearing targets. High-resolution electron micrographs of the immunological synapse formed between NK and iNKT cytolytic cells with their targets revealed that, in both NK and iNKT cells, the centrioles could be found associated (or \'docked\') with the plasma membrane within the immunological synapse. Secretory clefts were visible within the synapses formed by both NK and iNKT cells, and secretory lysosomes were polarized along microtubules leading towards the docked centrosome. The Golgi apparatus and recycling endosomes were also polarized towards the centrosome at the plasma membrane within the synapse [33]. It seems that the polarization process is connected with the cytotoxic interactions between T-cells and thyrocytes in Hashimoto’s thyroiditis.
The immune synapse between plasma cells and APCs has been seldom described. Batista described the immunological synapse between plasma cells and antigen presenting cells [34]. We observed two types of immune synapses between plasma cells and thyrocytes in AITD. In Graves’ disease, they are the stimulating synapses: immunoglobulins encrusting the basal membrane of the thyrocyte were secreted in the central space of the synapse and were probably connected with TSH- receptors. In the last phase of this process, deposits of immunoglobulins were visible. The similar change were observed in kidney [35,36]. In glomerulonephritis, subendothelial complement deposits [36,37] and sun epithelial (similar to situation in thyroid) immunoglobulins deposits [35, 36] were observed. In Hashimoto’s thyroiditis, the plasma cells were polarized and formed the microtubule organizing center (MTOC) consisting of centrioles, mitochondria and Golgi apparatus and probably microtubules and microfilaments. The peripheral zonula adherens surrounded the place of immunoglobulin secretion, but the immunoglobulins penetrated to thyrocytes and probably led to damage to these cells [38].
Immune synapses between T-cells and plasma cells with thyroid’s epithelial cells were found in AITD.
In the ultrastructure of the synapse, peripheral zonula occludens or zonula adherens and a central space were observed in all types of the immune synapses.
The lymphocytes forming the cytotoxic synapse were characterized by presence of a microtubule-organizing center.
Insect molecular biology studies the molecular basis of biological processes in insects, including molecular synthesis, modification, mechanisms, and interactions [1]. Metabolites play key roles among all these aspects of insect molecular biology. Therefore, understanding the distribution of metabolites contributes to revealing the mechanisms of insect biology, including ontogeny, metabolism, and physiology. Research methodologies such as liquid chromatography-mass spectrometry (LC-MS) and immunofluorescence are generally used in visualizing the distribution of metabolites. However, all of them have their shortcomings. LC-MS or gas chromatography-mass spectrometry (GC-MS) usually uses the homogenate of a certain weight of specific tissue(s) or organ(s), resulting in losing in situ spatiotemporal information. Insect body sizes are mostly small, let alone certain tissues; so tissue-specific researches, in most case, consume a large number of insect individuals [2, 3, 4]. On the other hand, ordinary in situ characterization technologies such as immunofluorescence assay and fluorescence in situ hybridization (FISH) require labeling at specific biomolecules [5, 6, 7]. Hence, operating processes such as synthesizing probes and antibodies are usually time-consuming, inefficient, and limited to only one molecule.
\nAs a new molecular visualization technology, mass spectrometry imaging (MSI) has drawn more and more attention in recent years. MSI can visualize the spatial distribution of molecules in specific samples without any labeling and enable simultaneous evaluation and identification of hundreds of molecules in situ. In comparison with LC-MS and GC-MS, MSI requires only one sample for biomolecular localization, which makes it a powerful tool to visualize the changes in organism physiology and biochemistry. The basic principle of MSI is to scan target samples such as tissue slice for desorption and ionization of molecules or ions on the surface of samples by a laser or a high-energy ion beam [8]. Mass analyzer obtains mass-to-charge ratio (m/z) and ion intensity of the molecules or ions from pixels. Mass peaks are obtained from the database of imaging software such as FlexImaging and used to visualize one-dimensional linear profiling, two-dimensional spatial distribution of molecules, or three-dimensional anatomic structure [8]. MSI has been widely applied in life sciences, such as histology [9, 10]; pathology [11, 12]; pharmacology [13, 14]; food science [15]; botany [16, 17, 18, 19]; and microbiology [20, 21].
\nIn this chapter, we introduce the major types of in situ measurement by MSI and present an example of matrix-assisted laser desorption ionization (MALDI) to elucidate the operating processes. We also discuss the advances of MSI in insect physiology and biochemistry to better promote the research in entomology.
\nAmong all the MSI technologies, we can divide them into two major groups, vacuum ionization mass spectrometry imaging system and ambient ionization mass spectrometry imaging system, based on whether the environment of the instruments is a vacuum [8]. Based on desorption or ionization ion, vacuum ionization mass spectrometry imaging system can be further divided into different categories, namely MALDI [22], secondary ion mass spectrometry (SIMS) [23], surface-assisted laser desorption ionization (SALDI) [24], and laser desorption ionization (LDI) [25]; ambient ionization mass spectrometry imaging system can be further divided into different categories, namely desorption electrospray ionization (DESI) [26], laser ablation electrospray ionization (LAESI) [27], laser electrospray mass spectrometry (LEMS) [28], electrospray laser desorption ionization (ELDI) [28], atmospheric pressure matrix-assisted laser desorption ionization (AP-SMALDI) [29], and air flow-assisted ionization (AFAI) [30]. Among all these above-mentioned technologies, MALDI-MSI is the most popular technology in life science research because it not only can be applied to a wide range from inorganic ion, small molecules to proteins but also has the characteristics of high accuracy and sensitivity [31]. Here, we provide a further explanation of the basic principle of MADLI-MSI and elucidate the workflow for MALDI.
\nThe basic working principle of MALDI is that target analytes on the surface of tissue are crystallized with matrix (e.g., α-cyano-4-hydroxycinnamic acid and 2,5-dihydroxyacetophenone) to form a complex. When the complex is exposed by infrared laser at 2.94 or 10.6 μm and/or ultraviolet laser at 337, 355, or 266 nm, it absorbs the laser energy and converts these analytes into a phase of gas, which causes molecule ionization. The ionized molecules automatically enter a mass spectrometer where the molecules are detected and mapped [19].
\nA typical experimental workflow for MALDI is as follows (Figure 1):
Insect tissues are flash-frozen (with or without fixation) in an embedding media with gelatin, carboxymethylcellulose, or water;
Each sample is cryo-sectioned at 10–20 μm thickness and mounted onto glass slides coated with indium tin oxide, which is then lyophilized for tissue imaging;
The lyophilized slide is subject to three irregular fiducial markings on the surface of each sample for localization;
A digital image of the sample with fiducials is acquired;
A chemical matrix is applied to promote desorption and ionization. Matrix is coated by a sprayer/nebulizer or by solvent-free sublimation to acquire homogeneous matrix coverage over the entire tissue surface;
After matrix deposition, the target is inserted into the instrument, for which experimental parameters (e.g., laser energy, step size of plate movement, and a selected region of the tissue) are optimized to scan the image;
A laser beam is emitted for desorption to acquire mass spectra at every x and y grid points within the scanning area, so to visualize target ions and convert the ion’s intensity into a color scheme;
Hematoxylin-eosin staining is optional for displaying tissue localization.
MALDI-MSI imaging workflow.
MSI can visualize the spatial and temporal distributions of molecules. Endogenous metabolites, exogenous metabolites, and insect-plant interactions are three main aspects of MSI application to insect tissue section for in situ characterization. Endogenous metabolites refer to lipids, neuropeptides, proteins, and defense compounds [32, 33, 34, 35]; exogenous metabolites are drugs and insecticides [36, 37]; insect-plant interactions are associated with the fate of plant secondary defense compounds in insects [38]. We summarize the major applications of MSI for a better understanding of insect physiology and metabolism (Table 1).
\nSpecies | \nTissue | \nMajor analyte | \nMethod | \nEmbedding medium | \nThickness (μm) | \nMatrix | \nRef. | \n
---|---|---|---|---|---|---|---|
Endogenous metabolites | \n\n | \n | \n | ||||
\nAnopheles stephensi\n | \nWhole-body | \nLipids | \nAP-SMALDI | \n5% CMC | \n20 | \nDHB | \n[42] | \n
\nAedes aegypti\n | \nOvarian follicles | \nLipids | \n3D-SIMS | \n/ | \n100 | \n/ | \n[41] | \n
\nApis mellifera\n | \nBrain | \nNeuropeptides | \nMALDI | \n/ | \n14 | \nCHCA | \n[51, 52] | \n
Brain | \nProtein | \nMALDI | \n/ | \n12 | \nCA | \n[32] | \n|
Brain | \nL-arginine | \nMALDI | \n/ | \n12 | \nDHB | \n[53] | \n|
Venom | \nVenom toxins | \nMALDI | \n/ | \n10 | \nCHCA | \n[54] | \n|
\nDrosophila melanogaster\n | \nBody | \nPeptide | \nMALDI | \nAgarose | \n10 | \nCHCA | \n[55] | \n
Brain | \nLipids | \nSIMS | \n10% Gelatin | \n15 | \n/ | \n[47] | \n|
Brain | \nPhospholipid | \nSIMS | \n10% Gelatin | \n12 | \n/ | \n[49] | \n|
Collar | \nLipids | \nSIMS | \n10% Gelatin | \n10 | \n/ | \n[46] | \n|
Brain & head | \nGABA | \nMALDI | \n4% CMC | \n15 | \nCHCA | \n[56] | \n|
Malpighian tubule | \nLipids | \nMALDI | \n5% CMC | \n12 | \nDHB、DAN | \n[48] | \n|
Surface | \nLipids | \nMALDI | \n/ | \n/ | \nLiDHB | \n[43] | \n|
Whole-body | \nNeuropeptides | \nAP-SMALDI | \n5% CMC | \n20 | \nDHB | \n[29] | \n|
Whole-body | \nLipids | \nMALDI | \n10% Gelatin | \n20 | \nDHB | \n[45] | \n|
Wing | \nLipids | \nSIMS | \nPBS | \n/ | \nDHB | \n[34, 44] | \n|
\nGraphosoma lineatum\n | \nHead to abdomen | \nNon-polar compounds | \nDAPPI | \n\n/\n | \n/ | \n/ | \n[57] | \n
\nPaederus riparius\n | \nWhole-body | \nDefensive compounds | \nAP-SMALDI | \n10% Tragacanth gum | \n16 | \nDHB | \n[35] | \n
\nPeriplaneta americana\n | \nBrain | \nNeuropeptides | \nMALDI | \nGelatin | \n14 | \nCHCA | \n[33] | \n
Neuro-endocrine tissues | \nNeuropeptides | \nMALDI | \nParaffin | \n20 | \nDHB | \n[58] | \n|
\nProrhinotermes simplex\n | \nHead to abdomen | \nNon-polar compounds | \nDAPPI | \n/ | \n/ | \n/ | \n[57] | \n
\nSolenopsis invicta\n | \nVenom | \nVenom proteins | \nMALDI | \nGelatin | \n14 | \nDHB | \n[59] | \n
Exogenous metabolites | \n|||||||
\nDrosophila melanogaster\n | \nWhole-body | \nInsecticide | \nMALDI | \n10% Gelatin | \n15 | \nDHB | \n[36] | \n
\nSchistocerca gregaria\n | \nWhole-body | \nDrugs | \nDESI | \n5% CMC | \n50 | \n/ | \n[37, 60] | \n
\nHelicoverpa armigera\n | \nWhole-body | \nBiopesticide | \nMALDI | \n/ | \n16 | \nDHB | \n[61] | \n
Insect-plant interaction system | \n|||||||
\nAphis glycines\n | \nFeeding leaf | \nMetabolites | \nMALDI | \n/ | \n/ | \nDHB、DAN | \n[62, 63] | \n
\nAthalia rosae\n | \nWhole-body | \nGlucosinolates | \nMALDI | \nWater | \n15 | \nCHCA | \n[64] | \n
\nChorthippus dorsatus\n | \nGut, feces | \nMetabolites | \nLDI | \n1% PBS | \n12 | \nDHB、DAN、CHCA | \n[38] | \n
Others | \n|||||||
\nAcromyrmex echinatior\n | \nNest | \nMicrobial | \nMALDI | \n/ | \n/ | \nDHB、CHCA | \n[65] | \n
Ants | \nPropleural plate | \nFungus | \nMALDI | \n/ | \n/ | \nDHB | \n[66] | \n
\nBombus terrestris\n | \nWhole-body | \n/ | \nMALDI | \npHPMA | \n12 | \nDHB、SA | \n[67] | \n
Overview of the application of MSI in insect sciences.
Lipids are basic cell components and play important roles in insect development and reproduction, such as maintenance of cell membrane structure and intra or extracellular signaling [39, 40, 41]. For example, glycerophospholipids, phosphatidylcholines, and phosphatidylethanolamines are basic components of cell and lysophospholipids have an important function in inflammation, abiotic stress, and biotic stress signal transmit [42]. MSI has been widely applied in many aspects in model insect Drosophila melanogaster, such as the neutral lipids three-dimensional spatial distribution on the surface adults [43, 44], body lipid distribution [45], brain lipid structure [46, 47], wing lipids [34, 44], Malpighian tubule phospholipid distribution [48], and phospholipids in the brain treated with cocaine [49]. Moreover, MSI detected and localized the composition and distribution of triacylglyceride in Aedes aegypti, phospholipid and phosphatidylcholine in Anopheles stephensi [42], and phospholipids in Schistocerca gregaria [37].
\nNeuropeptides, a kind of structurally diverse signaling molecules, can control and regulate fundamental physiological functions such as growth, reproduction, and environmental stress tolerance in animals [50]. MSI detected and localized the distribution of 14 neuropeptides in coronal brain sections in all development stages of D. melanogaster [29]. These neuropeptides play important roles in physiological processes (e.g., allatostatins and tachykinin-like peptides participate in odor perception and locomotor activity). Neuropeptides can act as transmitters or neuromodulators in the central nervous system [33]. Neuropeptides in the brain of Apis mellifera are related to the functional division of the population and their activities. Worker bees’ neuropeptide levels at the age of 0–15 d increased with the in-hive activities but decreased with out-hive activities (guarding and foraging) at 15–25 d [51]. Further study proved that allatostatin and tachykinin-related neuropeptides in the brain of worker bees were related to aggressiveness behaviors [52]. Neuropeptides distribution in the retrocerebral complex of Periplaneta Americana revealed the differentiation of prohormone processing and the distinctness of neuropeptides-based compartmentalization [33]. These studies proved that MSI has the advantages of sensitivity, which can facilitate to detect peptides in low abundance.
\nAs a kind of macromolecules, proteins are fundamental compounds of organisms and take part in important cellular processes, such as DNA replication and metabolisms. MSI can simultaneously and specifically detect the spatial distribution of massive proteins and overcome antibody cross-contamination. MSI system has been used to evaluate the negative impacts in the brain of A. mellifera exposing to a sublethal concentration of imidacloprid. The system has successfully visualized the distribution of 24 proteins (e.g., cytochrome P450s, glutathione S-transferases, and heat shock protein 70s). Besides, 8-day exposure to imidacloprid triggered biochemical changes in A. mellifera brain (e.g., up-regulated acetylcholinesterase and amyloid precursor-like protein and down-regulated cytochrome P450 and disulfide-isomerase protein). This could influence the well-being of A. mellifera (e.g., learning and memory acquisition, maintaining neuronal integrity, detoxification, and apoptosis) [32].
\nIn addition to lipids, neuropeptides, and proteins, MSI can also be used to visualize the distributions of defensive compounds, special proteins (e.g., venom allergens and toxins) and other small molecules (e.g., betaine and amino acids). Defensive compounds (e.g., pederin, pseudopederin, and pederon) were detected and localized in the organs of Paederus riparius [35]. Three venom allergens and two venom toxins were mapped in the honeybee [54]. Poison sac was the lactation of main venom proteins in Solenopsis invicta [59]. Nonpolar compounds (e.g., (E)-1-nitropentadec-1-ene and (E)-hex-2-enal) can be detected from the head to the abdomen in two model insects, Prorhinotermes simplex and Graphosoma lineatum. Gland openings and gland reservoirs were the most active areas in P. simplex and G. lineatum [57]. Other small molecules (e.g., betaine and amino acids) were detected in Schistocerca gregaria [37]. Semiochemicals were mapped on the surface of the adults of D. melanogaster [43]. Two male-specific sex pheromones were localized in the ejaculatory bulb of D. melanogaster [45]. MSI can also be used as a novel in situ metabonomic tool to study the metabolism of L-arginine of the honeybee brain in response to proboscis extension [53].
\nMSI can be applied to visualize the distribution of insecticides in insects and their negative influence on the target insects. Imidacloprid was used to study its distribution and accumulation in D. melanogaster. Based on laser irradiation, imidacloprid was found to be converted to guanidine-imidacloprid. It eventually accumulated and spread in the abdominal region [36]. Azadirachta indica is an economical tree that can be used to distract a biopesticide component, azadirachtin-A. It was only presented in the midgut of Helicoverpa armigera after application [61].
\nPharmacology model animals are crucial for scientists or pharmacologists to test the side effects of newly developed drugs before clinical trials on human beings. Common pharmacology model animal species include mice, rabbits, dogs, and monkeys. Insects, compared with the above-mentioned animals, have pros such as low costs, high fertility, and moral constraints. Locust has become a new model species for pharmacology test because of its high similarity with mammals. Antihistamine drug terfenadine was tested in locust to study the distribution of secondary metabolites. Terfenadine was gradually degraded from hemolymph to stomach and intestinal wall. However, terfenadine-related chemical compounds such as terfenadine acid, terfenadine glucoside, and terfenadine phosphate were distributed in the unexcreted feces in the intestine, which revealed a rapid discharge of metabolites through defecation [37]. Besides, the spatial and temporal distribution of midazolam was tested in locust. The results showed that midazolam was abundant in 30-min but only found in the feces after a 2-hour application. Midazolam glucoside was found in gut, gastric caeca, and feces after a 2-hour application, indicating that glucose conjugates are a major detoxification pathway to neutralize the effects caused by midazolam in locusts [60].
\nIn addition, D. melanogaster was used to test how cocaine, drug removal, and methylphenidate influence the brain lipids. The results showed that cocaine increased the level of phosphatidylcholines and decreased the levels of phosphatidylethanolamines and phosphatidylinositols. Methylphenidate-treated flies failed to rescue the levels of phosphatidylethanolamines and phosphatidylinositols, but enhanced the reversal of phosphatidylcholine levels [49].
\nPlants and herbivorous insects are co-evolved in nature. Plants activate defense reaction by releasing secondary metabolites when they are under attack by herbivorous insects, while herbivores trigger anti-defense systems for adapting and overcoming the side effects of secondary metabolites produced by plants [68]. Illuminating the changes of secondary metabolites during the interactions between insects and plants can contribute to a better understanding of plant resistance and insect adaptability.
\nChemical interaction between soybean (Glycine max) and aphid (Aphis glycines) was studied. The metabolite changes (e.g., phosphorylcholine and amino acid) were detected in the aphid-infested soybean leaves. The results suggested that secondary metabolites were produced by dead cells after aphid infestation. Moreover, other compounds such as pipecolic acid, salicylic acid, formononetin, and dihydroxyflavone were consistently detected in the plant regions infested by aphids [62]. It was also found that isoflavones can be accumulated in mesophyll cells or epidermis but were not present in the vasculature. The results indicated that isoflavones take part in non-phloem defense response [63].
\nIn addition, MSI can be used for physiological studies such as annihilation of the plant secondary metabolites by herbivores. Glucosinolate gradually changes in the distribution and metabolic sequestration were detected in the body of Athalia rosae that fed on host plants after different periods. The glucosinolate sinalbin was accumulated in the hemolymph and eventually circulated the Malpighian tubules. The results indicated that the insect gut plays a crucial role as a regulatory functional organ [64].
\nMoreover, MSI can be applied to the entire metabolic process of secondary metabolites in the plant-insect-soil system. The fate of the secondary metabolites produced by Dactylis glomerata was tracked in the different organs of herbivore Chorthippus dorsatus, and finally in the soil solution. After infestation by herbivores, levels of quinic acid, apigenin, and luteolin decreased, while those of flavonoids and rosmarinic acid increased in the leaf wounds of plants in 1 d. Quinic acid can be detected during the digestion process in the grasshoppers’ gut and unexcreted feces [38]. Overall, MSI is a useful tool to visualize plant defense and insect defense processes from the responses of plants infested by herbivores to insect defense systems responding to plant-derived metabolites.
\nMSI has been proved to be an effective and powerful tool to visualize molecules’ spatial distribution and temporal changes. In this chapter, we introduce the major types of MSI methodologies and describe the typical experimental workflow for MALDI-MSI. We also retrospect three major applications of MSI in insect physiology, for example, endogenous metabolites, exogenous metabolites, and insect-plant interaction. However, MSI still has some technical cons with limited application range that need to be optimized. In addition, MSI can cooperate with other genetic tools (e.g., proteomics, metabolomics, or lipidomics) for a better understanding of sophisticated insect biology.
\nThe work was supported by National Key R&D Program of China (2017YFD0200400), Special Key Project of Fujian Province (2018NZ01010013), Natural Science Foundation of Fujian Province (2019J01369) in China, and Innovation Fund of Fujian Agriculture and Forestry University (CXZX2018092, CXZX2016128, CXZX2017321 and 324-1122yb059).
\nThe authors declare no conflict of interest.
.
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