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Fluorescein Derivatives As Fluorescent Probes for Ph Monitoring Along Recent Biological Applications

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Fluorescein Derivatives As Fluorescent Probes for Ph Monitoring Along Recent Biological Applications International Journal of Molecular Sciences Review Fluorescein Derivatives as Fluorescent Probes for pH Monitoring along Recent Biological Applications Florent Le Guern 1,* , Vanessa Mussard 1, Anne Gaucher 1 , Martin Rottman 2,3 and Damien Prim 1 1 Institut Lavoisier de Versailles, CNRS, UVSQ, Université Paris-Saclay, 78035 Versailles, France; [email protected] (V.M.); [email protected] (A.G.); [email protected] (D.P.) 2 Faculté de Médecine Simone Veil, Université de Versailles St Quentin, INSERM UMR U1173, 2 Avenue de la Source de la Bièvre, 78180 Montigny le Bretonneux, France; [email protected] 3 Hôpital Raymond Poincaré, AP-HP, GHU Paris Saclay, 104 Bd Poincaré, 92380 Garches, France * Correspondence: fl[email protected] Received: 3 November 2020; Accepted: 1 December 2020; Published: 3 December 2020 Abstract: Potential of hydrogen (pH) is one of the most relevant parameters characterizing aqueous solutions. In biology, pH is intrinsically linked to cellular life since all metabolic pathways are implicated into ionic flows. In that way, determination of local pH offers a unique and major opportunity to increase our understanding of biological systems. Whereas the most common technique to obtain these data in analytical chemistry is to directly measure potential between two electrodes, in biological systems, this information has to be recovered in-situ without any physical interaction. Based on their non-invasive optical properties, fluorescent pH-sensitive probe are pertinent tools to develop. One of the most notorious pH-sensitive probes is fluorescein. In addition to excellent photophysical properties, this fluorophore presents a pH-sensitivity around neutral and physiologic domains. This review intends to shed new light on the recent use of fluorescein as pH-sensitive probes for biological applications, including targeted probes for specific imaging, flexible monitoring of bacterial growth, and biomedical applications. Keywords: fluorescein; pH-sensitive; probe; dyad; imaging; organelle; cell; bacteria; application 1. Introduction In chemistry, potential of hydrogen, or pH, is a data describing the acidity or the basicity of a medium [1]. Logarithmically obtained from H+ ion concentration, pH is one of the main physical characteristics used to describe an aqueous solution. Since the development of pH-meters, its measurement became inevitable across scientific fields, such as drinking water [2], industrial waste [3,4], global health [5], and agronomy [6]. As acidic or basic compounds are continuously released as outputs of cellular life, pH monitoring offered a unique opportunity to easily acquired data from biologic systems [7]. The relevance of pH in biological systems can be observed at different scales: the pH of biological fluids is well described and its regulation essential to the proper function of organs, since abnormal values are both the sign and cause of disease developments. pH regulation within biological systems relies on a sensitive equilibrium, called pH homeostasis. At the organism level, pH regulation is performed by the lungs through the elimination of CO2 and the kidney through the filtration of the HCO3− ion. In cells, where organic acids, such as lactic, pyruvic, or beta-hydroxybutyrate acids are produced along metabolic pathways, some membrane proteins compensate the decrease of pH by transporting protons outside the cytosol [8]. Thus, cellular pH monitoring leads to the understanding of key milestones within cells, such as proliferation [9], ion transport [10], or carcinogenesis [11]. For example, unchecked Int. J. Mol. Sci. 2020, 21, 9217; doi:10.3390/ijms21239217 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2020, 21, 9217 2 of 23 Int. J. Mol. Sci. 2020, 21, x FOR PEER REVIEW 2 of 23 biological processes occurring in malignant cells release a consequent amount of acid derivatives, leadingtissues [12]. to a pHIn microbiology, decrease in tumoral proliferations tissues [12 of]. aero In microbiology,bic bacteria also proliferations lead to a massive of aerobic production bacteria also of leadacidic to metabolites, a massive production which quickly of acidic induce metabolites, pH variations which quickly in medium induce pH[13]. variations Whereas in global medium pH [13 in]. Whereascytosol has global to be pHregulated, in cytosol each has organelle to be regulated, is fully effective each organelle in specific is fullyionic eenvironments,ffective in specific which ionic are environments,often correlated which to local are functions often correlated [14]. For to example, local functions the average [14]. pH For in example, lysosomes, the Golgi average network, pH in lysosomes,and mitochondria Golgi network, are 4.7, 6.7, and and mitochondria 8 respectively. are 4.7,Thus, 6.7, pH and monitoring 8 respectively. of each Thus, organelle pH monitoring has helped of eachto determine organelle their has helpedfunction. to At determine an atomic their scale, function. all metabolism At an atomic pathways scale, allare metabolism directly correlated pathways to arepH directlysince enzymatic correlated activities to pH since and enzymatic kinetics activitiesdepend andon ionic kinetics environments. depend on ionicAnother environments. common Anotherexample commonis the classification example is of the essential classification amino of acids, essential according amino their acids, acidic according or basic their trends. acidic Thus, or basic pH trends.is an important Thus, pH physicochemical is an important datum, physicochemical which can attest datum, of biological which can activities attest of at biological different activitiesscales. In atorder diff erentto monitor scales. these In order fluctuations to monitor without these fluctuationsany physical without contact, anyfluorescent physical pH-sensitive contact, fluorescent probes pH-sensitivewere developed probes during were the developed last century. during Under the last specific century. light, Under these specific molecular light, theseprobes molecular re-emit probesphotons re-emit at another photons wavelength at another for wavelength which related for whichintensity related depends intensity on the depends surrounding on the pH surrounding [7]. Since pHoptical [7]. devices Since opticalare continuously devices are becoming continuously more becomingprecise, especially more precise, with the especially broad dissemination with the broad of disseminationoptic fibers, pH-sensitive of optic fibers, molecular pH-sensitive probes molecular are recurrent probes across are biological recurrent acrossstudies. biological studies. One of the most used pH probes is fluorescein fluorescein 1; its chemical structure is composed of a tricyclic xanthene flankedflanked by two hydroxyl groups and a bicyclic fused lactone fragment linked by a spiro carbon atom (Figure1 1).). Figure 1. Chemical structure of fluorescein fluorescein 1. This familyfamily ofof molecules molecules was was discovered discovered in in 1871 1871 by by Adolf Adolf von von Baeyer, Baeyer, and and has becomehas become one of one most of ubiquitousmost ubiquitous probes probes in biological in biological studies, studies, because be ofcause its intense of its fluorescence, intense fluorescence, reversible pHreversible sensitivity, pH chemicalsensitivity, stability, chemical and lackstability, of cytotoxicity and lack at of working cytotoxicity concentrations. at working For years,concentrations. fluorescein For1 has years, been usedfluorescein as a starting 1 has been material used to as create a starting novel material fluorescent to crea probeste novel revealing fluorescent specific probes biological revealing activities specific such asbiological enzymatic activities cleavage such [15 as]. enzymatic Fluorescein cleavage1 is still [15]. the focusFluorescein of interest 1 is fromstill the the focus scientific of interest community from forthe itsscientific intense community fluorescence for and its its intense sensitivity fluorescence to pH variations and its aroundsensitivity neutral to pH domain variations [16]. Asaround most biologicalneutral domain systems [16]. are As fully most effective biological at physiological systems are conditions fully effective (pH~7.3), at physiological fluorescein 1conditionsbecame a benchmark(pH~7.3), fluorescein for monitoring 1 became pH fluctuationsa benchmark in for cell monitoring cultures. Indeed, pH fluctuations every year, in acell substantial cultures. amountIndeed, ofevery new year, articles a substantial describes biologicalamount of studies new articles using describes fluorescein biological1 as pH-sensitive studies using probe fluorescein (Figure2)[ 117 as]. InpH-sensitive this review, probe we propose (Figure an 2) overview[17]. In this of fluoresceinreview, we1 proposeand its mainan overview derivatives of fluorescein complemented 1 and by its a surveymain derivatives of recent studies complemented using fluorescein by a surv1eyas of pH recent sensors studies for biological using fluorescein applications. 1 as pH sensors for biological applications. Figure 2. Number of articles with keywords “fluorescein, pH, probe, biology” during last fifty years [17]. Int. J. Mol. Sci. 2020, 21, x FOR PEER REVIEW 2 of 23 tissues [12]. In microbiology, proliferations of aerobic bacteria also lead to a massive production of acidic metabolites, which quickly induce pH variations in medium [13]. Whereas global pH in cytosol has to be regulated, each organelle is fully effective in specific ionic environments, which are often correlated to local
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