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The Chronological Evolution of Small Organic Molecular Fluorescent Chemical Science View Article Online REVIEW View Journal | View Issue The chronological evolution of small organic molecular fluorescent probes for thiols† Cite this: Chem. Sci.,2021,12, 1220 Yongkang Yue, a Fangjun Huo b and Caixia Yin *a Abnormal concentrations of biothiols such as cysteine, homocysteine and glutathione are associated withvariousmajordiseases.Inbiologicalsystems,the structural similarity and functional distinction of these three small molecular thiols has not only required rigorous molecular design of the fluorescent probes used to detect each thiol specifically, but it has also inspired scientists to uncover the ambiguous biological relationships between these bio-thiols. In this minireview, we will discuss the evolution of small organic molecular fluorescent probes for the detection of thiols over the past 60 years, highlighting the potent methodologies used in the design of thiol probes and their Received 8th September 2020 particular applications in the semi-quantification of cellular thiols and real-time labelling. At the same Accepted 13th November 2020 time, the present challenges that limit their further application will be discussed. We hope that this DOI: 10.1039/d0sc04960c minireview will promote future research to enable deeper insight into the crucial role of thiols in Creative Commons Attribution-NonCommercial 3.0 Unported Licence. rsc.li/chemical-science biological systems. Introduction the concentration of total Cys in plasma was later found to be directly proportional to the concentration of total Hcy and, in Detection of biological thiols has been going on for more than the blood samples of patients with coronary heart disease, total 16,17 100 years since the successive discoveries of cysteine (Cys), Cys and total Hcy are signicantly higher than normal levels. glutathione (GSH) and homocysteine (Hcy).1–3 During this time, Today, the total concentration of Hcy in plasma is a clinical it has been a real challenge, one that directly affects the accurate indicator of the risk of cardiovascular and cerebrovascular This article is licensed under a analysis of thiols, to make these optically inert molecules diseases. In another case, a higher GSH level was found to be 18 observable. Fortunately, thiols with nucleophilic reactivity are associated with the resistance to Melphalan. Furthermore, ffi Perry and co-workers reported the existence of higher levels of Open Access Article. Published on 15 2020. Downloaded 28-09-2021 21:34:04. able to react e ciently with electron de cient systems such as benzoquinone and N-ethyl maleimide resulting in the forma- GSH in primary breast tumors compared with normal breast tion of covalent bonds.3,4 Similarly, thiols can easily react with tissue and proposed the possibility that GSH levels act as 19 benzyl halide derivatives via nucleophilic substitution reac- a marker of breast cancer. Although the relation between these tions.5,6 These specic covalent bonding processes enabled diseases and the concentrations of thiols were well studied, it is revolutionary technical support allowing the physiological and still unknown whether the observed thiol concentrations are the pathological roles of thiols to be seen.7–10 At the same time, the consequence or the cause of these diseases. Effective detection importance of thiols, especially in pathological processes, and labelling techniques are urgently needed to explore new further increased the necessity to label and detect thiols areas of research. quantitatively. An appealing use for the quantitative detection Though the detection of thiols employing uorescent probes of thiols relates to homocystinuria, an inherited error in the emerged aer 1960, it has encountered a renaissance in the past metabolism of amino acids that results in an increased inci- 20 years promoted not only by the signicant improvement of dence of vascular injury and arterial thrombosis, discovered in laser scanning confocal microscopes, but also by the possibility 1962.11–14 Subsequently, a large number of studies reported that that we can rationally design uorescent probes to full specic the increase in total blood Hcy content was related to the onset requirements. Recently, several excellent reviews have summa- of cardiovascular and cerebrovascular diseases.15 Interestingly, rized the recent development of uorescent probes for the detection of thiols.20–24 In this minireview, we will discuss the chronological evolution of application-oriented small molec- a Key Laboratory of Chemical Biology and Molecular Engineering of Ministry of Education, Institute of Molecular Science, Shanxi University, Taiyuan 030006, ular uorescent probes for the detection of thiols over the last China. E-mail: [email protected] 60 years. We will also examine the present challenges and hope bResearch Institute of Applied Chemistry, Shanxi University, Taiyuan 030006, China to inspire the design of future uorescent probes to move from † Electronic supplementary information (ESI) available: Reaction schemes for the approaches that utilize trial and error to those that use design- uorescent probes presented in this minireview and information on the reviews of based molecular engineering. the reported thiols. See DOI: 10.1039/d0sc04960c 1220 | Chem. Sci.,2021,12, 1220–1226 © 2021 The Author(s). Published by the Royal Society of Chemistry View Article Online Review Chemical Science Evolution of fluorescent probes for Forprobesoftheprimarytype,thedistinctnucleophilic–SH moiety in biological thiols can readily react with electron-decient thiols centers and active halides via a nucleophilic addition (NAR) or Studies of the chemical reactions of thiols are the overall basis for a nucleophilic substitution reaction (NSR). For example, enabled the design of uorescent probes for thiols. The efficient capture by the speci c reaction between a maleimide moiety and thiols in of mercury ions by thiols and sulfur-containing proteins inspired aqueous solution, a uorescent probe based on a NAR mechanism 2 28–31 the synthesis of the uorescein-mercury compounds “di- was rst reported by Kanaoka in 1964 ( ). In this example, the acetoxymercuriuorescein and tetra-acetoxymercuriuorescein thiols reacted quickly with the maleimide moiety via aNAR (1)” as uorescent probes for the detection of thiols with process which induced a turn-on uorescent response. Speci - cally, for Cys, the amino moiety of the NAR product could further a decreased uorescent intensity initiated by the uorescent thiol detection.25–27 This became the hallmark of uorescent probes for attack the amido bond to form a six-membered ring product via an 29,32 thiols (Fig. 1). intramolecular rearrangement. The corresponding uores- cence regulation mechanism was fully illustrated by the Wang The uses of uorescent probes for the detection of thiols can 33 be roughly divided into two types: I. quantitative analysis based group in 2016. Over the past 40 years, other structures such as N- 4 34 8 35 on chromatographic separation in aqueous solution; II. in situ dansylaziridine ( ), Acrylodan ( ) and 4-oxobut-2-enoate deriv- 9 36 12 analysis of cellular thiols based on a specic reaction between atives ( ), and a variety of Michael acceptors (squaraine ( ), 7- the thiol and the probe. oxanorbornadiene, quinone, chromene and nitroole n) were then reported to detect thiols via the one step NAR process.37–40 Creative Commons Attribution-NonCommercial 3.0 Unported Licence. This article is licensed under a Open Access Article. Published on 15 2020. Downloaded 28-09-2021 21:34:04. Fig. 1 Chronological evolution of small organic molecular fluorescent probes for the detection of thiols over the last 60 years and their representative molecular structures. The corresponding mechanisms for the reactions of these probes with thiols are presented in the ESI.† © 2021 The Author(s). Published by the Royal Society of Chemistry Chem. Sci.,2021,12, 1220–1226 | 1221 View Article Online Chemical Science Review O-phthalaldehyde (OPA, 3) was found to react with both GSH thiols requires further chromatographic separation. This fact and Hcy in aqueous solutions with appropriate pH conditions makes it impossible to evaluate the different biological roles of eliciting dual channel turn-on uorescent responses and was cellular thiols in situ using the above probes. Further, due to the rst utilized for thiol detection by Cohn and coworkers in susceptibility to oxidation of biological thiols, cell lysis and 1966.41 The formation of isoindole derivatives proceeded further separation would magnify the test error. Fluorescent degradation of the reaction system.42,43 A uorescent adduct of probes that can discriminate between the three bio-thiols might a naphthalene-based derivative and GSH allowed the quanti- solve these limitations. cation of GSH in serum to identify sepsis and further predicted Fluorescent probes of the secondary type are those which mortality in patients with sepsis.43 Furthermore, a similar could discriminate thiols with different uorescent responses. reaction with OPA also proceeded with the co-existence of the This advance was realized utilizing insight into the differences thiols with other amino acids.44 between Cys, Hcy and GSH which mainly manifest in the Disuldes (5),45 monobromobimane (mBB, 6) derivatives5 following three aspects: I. they are small molecular thiols that and 4-chloro-7-nitro-1,2,3-benzoxadiazole (NBD–Cl) deriva- have distinct cellular concentrations (cGSH 1–10 mM, cCys 30–200 6,46,47 tives are a series of NSR-based uorescent probes. 17 years mM, cHcy 9–13 mM); II. the spacing between sulydryl and amino aer the rst report of the “Ellman reagent”,auorometric groups are different in each thiol; and III. the pKa values of the compound based on a disulde bond was synthesized for the sulydryl group induced distinct nucleophilic activities (pKa Cys 68–70 detection of thiols via interchange of the –S–S– and –SH ¼ 8.25, pKa Hcy ¼ 8.87 (10.0), pKa GSH ¼ 9.20). Using these groups.45,48,49 Today, disuldes species are one of the most differences, we can obtain a signature for each thiol. For important drug delivery systems that can be specically acti- example, Cys displays the highest nucleophilic activity when vated at thiol-abundant sites.
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