Open Access is an initiative that aims to make scientific research freely available to all. To date our community has made over 100 million downloads. It’s based on principles of collaboration, unobstructed discovery, and, most importantly, scientific progression. As PhD students, we found it difficult to access the research we needed, so we decided to create a new Open Access publisher that levels the playing field for scientists across the world. How? By making research easy to access, and puts the academic needs of the researchers before the business interests of publishers.
We are a community of more than 103,000 authors and editors from 3,291 institutions spanning 160 countries, including Nobel Prize winners and some of the world’s most-cited researchers. Publishing on IntechOpen allows authors to earn citations and find new collaborators, meaning more people see your work not only from your own field of study, but from other related fields too.
To purchase hard copies of this book, please contact the representative in India:
CBS Publishers & Distributors Pvt. Ltd.
www.cbspd.com
|
customercare@cbspd.com
This chapter describes the design of an imidazopyrazinone-type luciferin named as HuLumino1 by us and investigation of its luminescence properties. This luciferin was designed to generate bioluminescence by human serum albumin (HSA) rather than by luciferase derived from luminous organisms. HuLumino1 was developed by modifying a methoxy-terminated alkyl chain to the C-6 position and eliminating a benzyl group at the C-8 position of coelenterazine. To clarify the basis of light emission by HSA, the detailed kinetic properties of the HuLumino1/HSA pair were investigated using a calibrated luminometer. The enzymatic oxidation of HuLumino1 was observed only in the presence of HSA. Results of HSA quantification experiments using HuLumino1 agreed with less than 5% differences with those of enzyme-linked immunosorbent assays, suggesting HuLumino1 could be used for quantitative analysis of HSA levels in serum samples without any pretreatments. These results demonstrate the advantages of the coelenterazine analogue as a bioluminescence reagent to detect non-labeled proteins, which generally do not function as enzymes.
National Institute of Advanced Industrial Science and Technology (AIST), Japan
Kazuki Niwa
National Institute of Advanced Industrial Science and Technology (AIST), Japan
Tatsunosuke Tomita
National Institute of Advanced Industrial Science and Technology (AIST), Japan
Ryoji Kurita
National Institute of Advanced Industrial Science and Technology (AIST), Japan
University of Tsukuba, Japan
*Address all correspondence to: r.nishihara@aist.go.jp
1. Introduction
Luminous organisms, such as fireflies, Gaussia princeps, Oplophorus gracilirostris, and sea pansy Renilla reniformis, generate bioluminescence (BL), which is the light emission in the absence of external energy sources [1, 2]. In the core of BL, an enzymatic reaction occurs involving a bioluminescent substrate (luciferin) and enzyme (luciferase). In general, the enzymatic luminescence reaction proceeds between a specific luciferin-luciferase pair to allow for highly sensitive and specific detection/imaging of diverse molecular events in living subjects [2, 3, 4].
However, in some cases, bioluminescent or chemiluminescent substrates may induce enzymatic luminescence activity of non-bioluminescence enzymes. For example, CycLuc2, a synthetic analog of firefly luciferin, can be catalyzed to emit light by long-chain fatty acid acyl-CoA synthetase found in non-luminous insects [5, 6, 7]. In addition, the heme-containing enzyme myeloperoxidase, which is abundantly expressed in neutrophils and monocytes, can catalyze the luminescence reaction of xenobiotic luminol [8, 9]. These reports suggested that the introduction of appropriate exogenous luminescent substrates reveals luminous activity of non-bioluminescence enzymes, which can significantly differ from the conventional function of the enzyme and has potential for use in quantitative analysis of enzymes without any labeling procedures, including transgene introduction of luciferase from luminous organisms. Here, we describe the design and bioluminescence characterization of a luciferin analogue which was selectively catalyzed to exhibit bioluminescence by human serum albumin (HSA) [10]. Serum albumins perform various physiological functions; they maintain colloid osmotic blood pressure and transport several exogenous and endogenous molecules. However, they are not categorized in the list of EC number, indicating they are not considered typical enzymes. The bioluminescence system of HSA with the luciferin analogue synthesized by us is novel and different from the conventional luciferin-luciferase reaction systems.
2.1 Coelenterazine analogue with HSA-specific bioluminescence
Most luciferases from luminous marine organisms use coelenterazine (CTZ) as their luciferin to form coelenteramide in an excited state, with emission ranging from blue to green at approximately 400–500 nm (Figure 1) [11, 12]. CTZ is oxidized by bovine serum albumin (BSA) in addition to luciferase, and this has been considered as nonspecific reaction mainly occurs because of a simple luminescence reaction that requires only an oxygen molecule [1] (Figure 1).
Figure 1.
Chemical reaction of coelenterazine (CTZ)-dependent bioluminescence. The imidazopyrazinone structure and modifiable substituent are highlighted in red and blue, respectively.
The emission ability of CTZ is derived from the imidazopyrazinone ring, and the chemical structure of sidechains at the C-2, C-6, and C-8 position of the imidazopyrazinone core significantly affect enzyme recognition. For example, Cypridina luciferase oxidizes only Cypridina luciferin, which contains a basic guanidine moiety at the C-8 position of the imidazopyrazinone ring, not CTZ (Figure 2) [13]. A mutant Oplophorus luciferase (NanoLuc) uses furimazine rather than CTZ, and is known as a versatile reporter of BL (Figure 2) [14]. Thus, each bioluminescence probe has been individually developed with an imidazopyrazinone analogue that is suitable for the geometry of the active site in the pocket of mutant luciferase. We also reported that RLuc8.6-535SG, a mutant R. reniformis luciferase, utilizes BottleBlue2.3 (BBlue2.3), a CTZA that can permeate the cell membrane and emits bright visible luminescence suitable for deep-tissue imaging of cancer cells in vivo (Figure 3a) [15].
Figure 2.
Chemical structures of imidazopyrazinone-based analogues.
Figure 3.
Chemical structures of coelenterazine analogues (CTZAs) upon (a) C-2 and/or C-6 substitution. (b) Luminescence intensities obtained with serum albumin (0.1 mg/mL).
To clarify the potential enzymatic luminescence activity of human proteins, we focused on HSA, which accounts for approximately 65% of serum proteins in the human body [16]. This abundant protein is involved in a wide variety of physiological functions, such as maintaining osmotic pressure, buffering blood pH levels, and carrying ligands including hormones, amino acids, and fatty acids [17, 18]. In addition, HSA and some ligand complexes often possess enzymatic activities, such as Kemp elimination and hydrolysis of esters because of their unique ability to bind small hydrophobic molecules in some cavities; however, the potential enzymatic activities remain unclear [17, 19].
First, to obtain a rational luciferin with an imidazopyrazinone core for HSA-specific BL, we assayed CTZ and previously reported 18 CTZAs named as Bottle Blue (BBlue), where the p-hydroxy phenyl group at the C-6 position of CTZ was modified by alkylation (Figure 3), with serum albumins (fatty acid free HSA and BSA). In this chapter, except for in Section 2.2, luminescence measurements were performed using luminometers (GloMax20/20 Luminometer or GloMax Explorer Multimode Microplate Reader) manufactured by Promega (Madison, WI, USA). Next, BBlue2.3, a CTZA with a methoxy-terminated alkyl linker chain of three methylene units at the C-6 position, exhibited the brightest emission, which produced 16.6-fold higher luminescence when combined with HSA (i.e. BBlue2.3/HSA pair) compared to that of the CTZ/HSA pair (Figure 3).
Based on these results, we predicted that elimination of the benzyl group at the C-8 position of BBlue2.3 would relieve its steric hindrance with key amino acids in the substrate binding site of HSA and enhance the enzymatic luminescence reaction of HSA. We then designed and synthesized a novel CTZA, named as Human Luminophore 1 (HuLumino1) based on the synthetic procedures of BBlue2.3 [15] and an array of 5 CTZAs containing known analogues [20] to investigate the effect of substitution at the C-2, C-6, and C-8 positions of CTZ on serum albumin-dependent luminescence (Figure 4b–d). Moreover, the luminescence of commercially available CTZAs (DeepBlueC and MCLA) was compared with the synthesized CTZAs when fatty acid free HSA and BSA were added (Figure 4e). Although the autoluminescence levels in PB buffer of HuLumino1 was similar to that of CTZ, only HuLumino1 displayed significantly enhanced luminescence dependent on HSA (but not BSA containing fatty acid) concentrations, as indicated by the 14.1-fold higher emission compared with that of the BBlue2.3/HSA pair. Furthermore, the luminescence intensity of the HuLumino1/HSA pair was found to be 718-fold higher than that of the CTZ/BSA pair, which has been reported to produce luminescence [11, 12]. The HuLumino1/HSA pair exhibited flash-type luminescence with a peak wavelength of 432 nm. (Figure 4f). Unexpectedly, HuLumino1 selectively activated HSA by recognizing the subtle conformational difference in the substrate binding site, although the overall sequence homology between HSA and BSA is 75.6%.
Figure 4.
Chemical structures of coelenterazine analogues (CTZAs) upon (a) C-2, C-6, and C-8 substitutions, (b) HSA-specific substitution, (c) C-2 and C-6 substitution, and (d) C-2 or C-6 substitution. (e) Luminescence from serum albumins (0.1 or 1 mg/mL) treated with the indicated substrate (10 μM); error bars represent the standard deviations of three measurements. (f) Bioluminescence spectra of HuLumino1 in the presence or absence of HSA.
These results suggest “luciferase” activity of HSA catalyzes the enzymatic luminescence reaction of CTZAs to produce “bioluminescence”.
2.2 Quantitative evaluation of luminescence intensity
To characterize the enzymatic luminescence reaction with HSA, the bioluminescence intensity of CTZAs and HSA pairs was quantitatively evaluated. Bioluminescence intensity is generally determined by several reaction factors including the bioluminescence quantum yieldφBL of luciferin, turnover number (kcat), and active luciferase concentration. Kinetic parameters were determined using a custom-built luminometer with a photomultiplier tube (PMT) (H11890–01; Hamamatsu Photonics, Japan), and its absolute responsibility for total number of emitted photons in the instrument was calibrated for luminescence spectrum of each luciferin-luciferase pair [21, 22]. The absolute responsibility of the luminometer for the CTZ-utilizing bioluminescent system was determined as described previously [21]. The φBL values were calculated from the total number of emitted photons and total number of reacted luciferin molecules. To integrate all photons derived from the enzymatic reaction, the number of photons was monitored using the luminometer from before initiating the reaction to until the reaction was completed. The reaction was initiating by injection of fatty acid-free HSA PB solution (100 μg/mL or 10 mg/mL) into the preinstalled luciferin PB solution (20 nM) in the luminometer.
The Michaelis–Menten constant (Km) of luciferin was calculated from Lineweaver-Burk plots constructed using a standard method. The catalytic constant (kcat), which is the turnover number of the reaction for luciferin by a single luciferase molecule per second, was calculated from theφBL value and maximum velocity (Vmax) determined from the Lineweaver-Burk plots.
The apparent Km of the HuLumino1/HSA pair was 4.3 μM, which was comparable to that of the NanoLuc system [23]. In contrast, the kcat value of the NanoLuc system was 294-fold higher than that of the HuLumino1/HSA pair, and the catalytic efficiency of the luminescence reaction by HSA was lower than that of conventional luciferase [24]. However, in the luminescence system with HSA, HuLumino1 displayed a slightly higher Km value than CTZA-1, but its kcat value was approximately 3-fold higher (Table 1), resulting in 4.2-fold stronger light emission than that of CTZA-1 (Figure 4e). For luciferin with high enzyme affinity (e.g., CTZA −1), oxyluciferin, a product of the BL reaction, appears to competitively inhibit the luminescence reaction [25]. Moreover, HuLumino1 showed an enzyme affinity and bioluminescence quantum yield φBL of more than 5- and 100-fold higher than those of CTZ, respectively. The detailed luminescent profiles suggest that the structural properties of the alkyl linker chain modified at the C-6 position of the imidazopyrazinone core contribute to the efficient HSA-catalyzed emission reaction. Although the catalytic efficiency of HuLumino1/HSA is much lower than that of the NanoLuc system, HuLumino1 is a luciferin that is relatively more suitable for HSA than other existing luminescent substrates.
Pair
φBLa×10−5
KmbμM
kcatcs−1
CTZ/HSA
0.32 ± 0.03
25.3 ± 5.2
2.75 ± 0.3
HuLumino1/HSA
30.9 ± 3.1
4.28 ± 1.24
0.30 ± 0.06
CTZA-4/HSA
42.2 ± 9.1
2.46 ± 0.40
0.11 ± 0.09
Table 1.
Luminescent profiles of CTZ and its analogues with HSA.
Errors represent standard error of the mean values for triplicate experiments.
Michaelis-Menten constant (Km) values were determined by Lineweaver-Burk plots via measurements of initial rates of light emission over a range 0.5 to 20 μM.
Turnover rate (kcat) values were calculated by dividing maximum velocity (Vmax) by the φBL. The Vmax were determined by Lineweaver-Burk plots.
2.3 Enzymatic reaction site of HSA
The crystal structure of HSA, with binding to a variety of drugs, clarified the two principal drug binding sites in different subdomains (site 1 in subdomain IIA and site 2 in subdomain IIIA) [26, 27]. To investigate the luminescent reaction site between HSA and HuLumino1, a competitive assay was conducted with two site-specific HSA drugs (warfarin-site1 and ibuprofen-site2) [27]. Fatty acid free HSA PB solution was pre-treated with the drugs (0–100 μM) to fill binding site 1 or 2 before adding HuLumino1. The luminescence of HuLumino1 was negligibly low in the presence of HSA-ibuprofen complex (Figure 5a). In contrast, HuLumino1 exhibited efficient luminescence with the HSA-warfarin complex, indicating that HuLumino1 selectivity binds to the site 2 cavity of HSA. In detailed analysis of the inhibitory kinetics, Lineweaver-Burk plots displayed that ibuprofen competitively inhibited the binding of HuLumino1 to HSA (Ki of ibuprofen was 6.3 nM) (Figure 5b). Therefore, the enzymatic reaction site of HuLumino1 was experimentally determined to be binding site 2. Next, docking simulation with the Molecular Operating Environment software package was carried out to predict the binding poses. The simulation displayed the specific binding of HuLumino1 to the hydrophobic cavity of site 2 by interacting with several amino acids including R410, K414, and L453 (Figure 5c–e). Particularly, R410, a key amino acid residue in the esterase activity of HSA [17], is also involved in the luminescence reaction (Figure 5e).
Figure 5.
(a) Luminescence response in the presence (I) vs. absence (I0) of the binding drug concentration (0–100μM). (b) Lineweaver-Burk plot indicating competitive inhibition by ibuprofen. V0 is defined as the luminescence intensity over the initial 30 s and [S] is the substrate concentration. The concentrations of ibuprofen were 1 nM (square) and 5 nM (triangle). Open circles indicate negative controls with no ibuprofen. (c) Ligand-binding site 2 of HSA with HuLumino1 as posed by the molecular operating environment software (d) magnified view of binding site 2. The ligand binding site in the blue region indicates the presence of the hydrophobic environment. (e) Predicted interaction between HuLumino1 and HSA.
Next, to investigate the effect of the steric structure of HSA on luminescence, HSA pretreated with 10 M guanidine hydrochloride, a reagent commonly used to induce denaturation of the α-helix structure of proteins [28], was prepared, and the luminescence of HuLumino1 was extremely low in the presence of denatured HSA (data not shown). Therefore, the enzymatic reaction of HuLumino 1 depends on the microenvironment and steric structure such as binding site 2 constructed by the folding structure of HSA. These results suggest that emission of HuLumino1/HSA is not a non-specific chemiluminescence commonly found in other imidazopyrazinone compounds.
2.4 Bioluminescent assay for HSA
Low levels of HSA in the serum (<35 mg/mL) are biomarkers of several diseases such as malnutrition, cirrhosis, and chronic hepatitis [29]. In hospitals, HSA is evaluated using the colorimetric bromocresol green assay or ELISA. Both can provide a reliable assessment of albumin but require sample preparation and processing time (e.g. 3 h for ELISA) [30]. Therefore, an assay for the simple, accurate and rapid detection of HSA in the serum should be developed for clinical diagnosis. We demonstrated that the BL assay can be used to evaluate HSA based on the enzymatic luminescence reaction of HuLumino1. Regarding the selectivity of the reaction of HuLumino1, no reactivity with other proteins (BSA, β-galactosidase,β-lactoglobulin, catalase, α-chymotrypsinogen, hemoglobin, human IgG, porcine lipase, papain, pepsin, trypsin, γ-globulin, carbonic anhydrase, concanavalin A, glucosidase, histone, myoglobin, and RNase, 0.1 mg/mL) was observed, and only HSA led to distinct luminescence enhancement (Figure 6a). Although the coexistence of most proteins did not affect the enzymatic reaction of the HSA/Hulumino1 pair, a slight decrease in luminescence was observed in the presence of some proteins (data not shown). This indicates that HuLumino1 nonspecifically binds to other proteins but does not exhibit BL. Hence, HuLumino1 can be used to detect HSA without interference from other proteins, as it exhibited excellent selectivity for HSA even in a complicated biological system. The luminescence of HuLumino1 was enhanced in an HSA concentration-dependent manner and exhibited a constant intensity at HSA concentrations above 10 mg/mL (Figure 6b). A linear increase in luminescence, within the spiked HSA concentration range of 0–0.1 mg/mL in PBS-diluted serum, resulted in a detection limit of 8.6 μg/mL for HSA, which was comparable to the standard detection limit of HSA in physiological systems (Figure 6c) [31].
Figure 6.
(a) Variation in luminescence of HuLumino1 (10 μM) in the presence of proteins (0.1 mg/mL); error bars represent the standard deviations of three measurements. (b) Luminescence intensity of HuLumino1 (20 μM) containing various concentrations of HSA (0–17 mg/mL) in PBS and (c) HSA (0–17 mg/mL) in PBS-diluted plasma (100-fold, pH 7.4).
Finally, two HSA assays, including our developed BL-based assay and ELISA, were performed to evaluate human serum from male AB plasma. The HSA levels calculated with HuLumino1 agreed well with those estimated by ELISA within 5% error. The spike and recovery tests also showed results within the margin of 7% error (Table 2). Therefore, the BL-based HSA assay showed analytical capability with high sensitivity and could detect HSA within 10 min including the sample preparation and measurement times. In addition, we detected the expression of recombinant HSA in living COS-1 cells (data not shown), indicating that HuLumino1 can be used in molecular biology studies and in biomedical applications.
Conditions: HuLumino1 (20μM) in PBS-diluted serum (1000-fold, 10 mM, pH 7.4).
ND: Not Determined.
We designed and synthesized the first luciferin (HuLumino1), an analogue with C-6 and C-8 modification of CTZ, which exhibited bioluminescence with HSA. HuLumino1 rapidly detected HSA with high sensitivity and specificity, even in real human plasma containing various interfering biomolecules. Detailed kinetic investigation of the enzymatic reaction clarified the enzyme recognition of HuLumino1 from HSA drug binding site 2, resulting a highly selective reaction and revealing a reaction with both native HSA and recombinant HSA expressed in COS-1 cells. Therefore, the BL-based assay with HuLumino1, either used alone or coupled with ELISA, can be used for the early diagnosis of HSA-related diseases, enabling accurate and rapid detection of HSA in serum samples without pre-treatment. The information obtained through detailed investigation of the HuLumino1/HSA pair may be extended to protein assays based on a luminescent reaction without genetically engineered luciferases.
We acknowledge funding from JST, PRESTO Grant Number JPMJPR20EB, JSPS KAKENHI Grant Number 20 K15421, AMED under Grant Number JP191m0203012, Shimazu Science Foundation, Research Foundation for Opto-Science and Technology, and Nakatani Foundation for Advancement of Measuring Technologies in Biomedical Engineering, and DAICENTER project grant from DBT (Govt. of India) to Renu Wadhwa and special strategic grant from AIST (Japan).
We thank Dr. Tsukasa Ishihara (Biomedical Research Institute, National Institute of Advanced Industrial International Science and Technology) for his help with the docking simulation experiment.
References
1.Shimomura O. Bioluminescence: Chemical Principles and Methods. Bioluminescence: Chemical Principles and Methods. Singapore: World Scientific Publishing Company; 2006. 471 p
2.Badr C. Bioluminescent Imaging: Methods and Protocols. Bioluminescent Imaging: Methods and Protocols. New York: Springer; 2014. 1276 p
3.Rowe L, Dikici E, Daunert S. Engineering bioluminescent proteins: expanding their analytical potential. Analytical Chemistry. 2009;81(21):8662–8668. DOI: 10.1021/ac9007286
4.Ozawa T, Yoshimura H, Kim S. Advances in fluorescence and bioluminescence imaging. Analytical Chemistry. 2013;85(2):590–609. DOI: 10.1021/ac3031724
5.Mofford D, Reddy G, Miller S. Latent luciferase activity in the fruit fly revealed by a synthetic luciferin. Proceedings of the National Academy of Sciences of the United States of America. 2014;111(12):4443–4448. DOI: 10.1073/pnas.131900111
6.Mofford D, Liebmann K, Sankaran G, Reddy G, Reddy G, Miller S. Luciferase activity of insect fatty acyl-CoA synthetases with synthetic luciferins. ACS Chemical Biology. 2017;12(12):2946–2951. DOI: 10.1021/acdchembio.7b00813
7.Mofford D, Adams S, Reddy G, Reddy G, Miller S. Luciferin amides enable in vivo bioluminescence detection of endogenous fatty acid amide hydrolase activity. Journal of the American Chemical Society. 2015;137(27):8684–8687. DOI: 10.1021/jacs.5b04357
8.Liu R, Tang J, Xu Y, Dai Z. Bioluminescence imaging of inflammation in vivo based on bioluminescence and fluorescence resonance energy transfer using nanobubble ultrasound contrast agent. ACS Nano. 2019;13(5):5124–5132. DOI: 10.1021/acsnano.8b08359
9.Gross S, Gammon S, Moss B, Rauch D, Harding J, Heinecke J, et al. Bioluminescence imaging of myeloperoxidase activity in vivo. Nature Medicine. 2009;15(4):455–461. DOI: 10.1038/nm.1886
10.Nishihara R, Niwa K, Tomita T, Kurita R. Coelenterazine analogue with human serum albumin-specific bioluminescence. Bioconjugate Chemistry. 2020;31(12):2679–2684. DOI: 10.1021/acs.bioconjchem.0c00536
11.Vassel N, Cox C, Naseem R, Morse V, Evans R, Power R, et al. Enzymatic activity of albumin shown by coelenterazine chemiluminescence. Luminescence. 2012;27(3):234–241. DOI: 10.1002/bio.2357
12.Lindberg E, Mizukami S, Ibata K, Miyawaki A, Kikuchi K. Development of luminescent coelenterazine derivatives activatable by beta-galactosidase for monitoring dual gene expression. Chemistry-A European Journal. 2013;19(44):14970–14976. DOI: 10.1002/chem.201302002
13.Maguire C, Bovenberg M, Crommentuijn M, Niers J, Kerami M, Teng J, et al. Triple bioluminescence imaging for in vivo monitoring of cellular processes. Molecular Therapy-Nucleic Acids. 2013;2(6):e99. DOI: 10.1038/mtna.2013.25
14.Hall M, Unch J, Binkowski B, Valley M, Butler B, Wood M, et al. Engineered luciferase reporter from a deep sea shrimp utilizing a novel imidazopyrazinone substrate. ACS Chemical Biology. 2012;7(11):1848–1857. DOI: 10.1021/cb3002478
15.Nishihara R, Paulmurugan R, Nakajima T, Yamamoto E, Natarajan A, Afjei R, et al. Highly bright and stable NIR-BRET with blue-shifted coelenterazine derivatives for deep-tissue imaging of molecular events in vivo. Theranostics. 2019;9(9):2646–2661. DOI: 10.7150/thno.32219
16.Anderson N, Anderson N. The human plasma proteome: history, character, and diagnostic prospects. Molecular & Cellular Proteomics. 2002;1(11):845–867. DOI: 10.1074/mcp.r200007-mcp200
17.Kragh-Hansen U. Molecular and practical aspects of the enzymatic properties of human serum albumin and of albumin-ligand complexes. Biochimica Et Biophysica Acta-General Subjects. 2013;1830(12):5535–5544. DOI: 10.1016/j.bbagen.2013.03.015
18.Taverna M, Marie A, Mira J, Guidet B. Specific antioxidant properties of human serum albumin. Annals of Intensive Care. 2013;3(1):4. DOI: 10.1186/2110-5820-3-4
19.Hollfelder F, Kirby A, Tawfik D, Kikuchi K, Hilvert D. Characterization of proton-transfer catalysis by serum albumins. Journal of the American Chemical Society. 2000;122(6):1022–1029. DOI: 10.1021/ja993471y
20.Hirano T, Gomi Y, Takahashi T, Kitahara K, Qi C, Mizoguchi I, et al. Chemiluminescence of coelenterazine analogs - structures of emitting species. Tetrahedron Letters. 1992;33(39):5771–5774. DOI: 10.1016/0040-4039(92)89028-B
21.Ikeda Y, Tanaka M, Nishihara R, Hiruta Y, Citterio D, Suzuki K, et al. Quantitative evaluation of luminescence intensity from enzymatic luminescence reaction of coelenterazine and analogues. Journal of Photochemistry and Photobiology A Chemistry. 2020:112459. DOI: 10.1016/j.jphotochem.2020.112459
22.Ando Y, Niwa K, Yamada N, Enomot T, Irie T, Kubota H, et al. Firefly bioluminescence quantum yield and colour change by pH-sensitive green emission. Nature Photonics. 2008;2(1):44–47. DOI: 10.1038/nphoton.2007.251
23.Coutant E, Gagnot G, Hervin V, Baatallah R, Goyard S, Jacob Y, et al. Bioluminescence profiling of NanoKAZ/NanoLuc luciferase using a chemical library of coelenterazine analogues. Chemistry-A European Journal. 2020;26(4):948–958. DOI: 10.1002/chem.201904844
24.Yeh H, Karmach O, Ji A, Carter D, Martins-Green M, Ai H. Red-shifted luciferase-luciferin pairs for enhanced bioluminescence imaging. Nature Methods. 2017;14(10):971–974. DOI: 10.1038/nmeth.4400
25.Matthews JC, Hori K, Cormier MJ. Substrate and substrate analog binding properties of Renilla luciferase. Biochemistry. 1977;16(24):5217–5220. DOI: 10.1021/bi00643a009
26.Sugio S, Kashima A, Mochizuki S, Noda M, Kobayashi K. Crystal structure of human serum albumin at 2.5 A resolution. Protein Engineering. 1999;12(6):439–446. DOI: 10.1093/protein/12.6.439
27.Ghuman J, Zunszain P, Petitpas I, Bhattacharya A, Otagiri M, Curry S. Structural basis of the drug-binding specificity of human serum albumin. Journal of Molecular Biology. 2005;353(1):38–52. DOI: 10.1016/j.jmb.2005.07.075
28.Xu Y, Su M, Li H, Liu Q, Xu C, Yang Y, et al. A fluorescent sensor for discrimination of HSA from BSA through selectivity evolution. Analytica Chimica Acta. 2018;1043:123–131. DOI: 10.1016/j.aca.2018.09.010
29.Murch S, Winyard P, Koletzko S, Wehner B, Cheema H, Risdon R, et al. Congenital enterocyte heparan sulphate deficiency with massive albumin loss, secretory diarrhoea, and malnutrition. Lancet. 1996;347(9011):1299–1301. DOI: 10.1016/s0140-6736(96)90941-1
30.Luo Z, Lv T, Zhu K, Li Y, Wang L, Gooding J, et al. Paper-based ratiometric fluorescence analytical devices towards point-of-care testing of human serum albumin. Angewandte Chemie-International Edition. 2020;59(8):3131–3136. DOI: 10.1002/anie.201915046
31.Gao T, Yang S, Cao X, Dong J, Zhao N, Ge P, et al. Smart self-assembled organic nanoprobe for protein-specific detection: design, synthesis, application, and mechanism studies. Analytical Chemistry. 2017;89(18):10085–10093. DOI: 10.1021/acs.analchem.7b02923
Written By
Ryo Nishihara, Kazuki Niwa, Tatsunosuke Tomita and Ryoji Kurita
Submitted: 24 February 2021Reviewed: 15 March 2021Published: 19 April 2021
Open access peer-reviewed chapter
