Biological Effects of Fluorescein Photochemistry: Comparison
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Fluorescein is a fluorescent organic dye used as tra cer, contrasting agent or a diagnostic tool in various fields of medicine. Although fluorescein is a compound with relatively low toxicity, after photoactivation, it releases potentially toxic molecules, such as singlet oxygen and, as have been recently demonstrated, also carbon monoxide. Since both of these molecules are biologically active, it is essential to explore potential biological effects of fluorescein photochemistry and natural sciences in general.

  • fluorescein
  • irradiation
  • singlet oxygen
  • carbon monoxide
  • cytotoxicity
  • metabolism
  • proliferation

1.  Introduction

Fluorescein is a fluorescent small-molecule organic dye that is commonly employed inexhibits strong fluorescence at neutral and alkalic pH in aqueous media. In these conditions, its main absorption peak is at 490 nm (ε490 = 76 900 M−1 cm−1) and thell qular biology as a tracerantum yield of the subsequent fluorescence is 0.93[1]. It is sodium salt is widely us a dark orange powder soluble in water and when dissolved in clinical medicinproper conditions, emitting bright green fluorescence (with maximum emission at 515 nm[2]). It be,longs to a particularly as a diagnostic tool in ogroup of xanthene dyes that includes substances like eosin Y or rhodamine B. It was first synthesized by Adolf von Baeyer around 1871 by condensation of resorcinol and phthalmologyic anhydride catalyzed with zinc chloride[3][14].

2.  Application

Fluorescein Itis has also been studied for new therapeutica broadly applied substance in various fields. For instance, it is commonly employed as a tracer. Some examples of this fluorescein applications are utilization as a ground-water tracer[5], and use for investigating variousmolecular movement in the bone lacunar-canalicular system[6] or fields, or examining extravasation to study blood-spinal cord barrier permeability on animal models[7][8]. Fluoresch as urologyein can be also applied as a topical fluorescent contrast agent for microendoscopy of gastrointestinal[29] or urinary tract[310][4] and as neurosua pH sensitive corrosion indicator[11][12].

Morgeover, it is extensively employed in ophthalmology as a diagnostic tool[513][14][15][616]. Having an important role in the diagnostics of ocular diseases, fluorescein has been included on the List of Essential Medicines, published by the World Health Organization[717]. An example of a well-established and frequently used fluorescein diagnostic technique is fluorescein angiography[13][18][19]. During diagnostic procedures, it can be administered locally[820], orally[921], or intravenously[1022] with subsequent irradiation of the area of interest using blue light[113][323][424] (≈490 nm[1125][1226]).

A There are also sthoughudies that points to fluorescein is considered to be generally safe, it is a photoactive compound whose biological effects associated with this activity have been neglected to date. For example,’s utilization in the labeling of brain tumor tissue (high-grade gliomas) to obtain better results of its resection[27][28][29] . fFluorescein is known to photosensitize oxygen to form singlet oxygen (1O2)capable of accumulating in cerebral areas with damaged blood-brain barrier[1330][14]. and Furthermore, it has been recently demonstrated that a fluorescein analog, xanthene-9-carboxylicefore ensure better resection due to contrast-enhanced borderline of malignant and healthy tissue[28]. In acdditid, releases carbon monoxide (CO) upon photoactivation byon, there exist studies supporting use in urology, specifically, in bladder[31][23] and penile[24] cancer surgrery.

3.  New discoveries

Fluorescein Irradiation Produces Biologically Active Compounds

Fluorescen lighin it[15]self via decarbonylation s a relatively nontoxic substance (LD50 = 6.7 g/kg fofr trats[32], wheich is carboxyl group. Althoughalmost 20x greater than LD50 fluorescein caffeine[33] or 2x more than this structuravalue for NaClly[34]). diffHoweverent, it was hypothesized that it may also undergo the photodecarbonylation reaction. This hypothesis has been recen, it is a photoactive compound whose biological effects associated with this activity have been neglected to date. For example, fluorescein is known to photosensitize oxygen to form singlet oxygen (1O2)[35][36]. Additionaly confirmed,ly, Martinek et al.[37] asnd Srankova et al.[1638] had shown that carbon monoxide (CO) is produced through photochemical degradation of fluorescein in a relatively high chemical yield of 40%.

Both 1O2 and CO are biologically active molecules that affect physiological processes in the human body[1739][1840][1941]. Over the past three decades, they have also been thoroughly studied for their use in the treatment of various diseases. 1O2 is a very reactive molecule, the cytotoxic properties of which are utilized in medicine, e.g., in photodynamic therapy[2042]. CO, is an important n low concentration, acts in the body as a gasotransmitter withmediating anti-inflammatory[2143], antiapoptotic[2244], and antiproliferative properties[23]. Its anticancer action was also studied in the researcher's laboratory, showing a positive effect on the survival rate of mice xenotransplanted with pancreatic cancer[2445]. Although  1O2  and CO are being investigated for their potential therapeutic applications, use in the treatment of various diseases, they both exert cytotoxicity at higher concentrations, particularly when their transport to target sites is not strictly controlled. While  1O2 causes oxidative damage and cell death[2546][2647][2748][2849], the toxicity of CO is related to its high binding affinity to blood hemoglobin[2950][3051][3152][3253] or the heme moiety of extravascular hemoproteins[3354][3455] such as cytochrome c oxidase[3556], affecting their oxygen carrier properties or enzymatic activities, respectively. In addition, CO can trigger oxidative stress[3657] and lipoperoxidation[3758].

2.  Impact of Fluorescein Irradiation on Biological Systems

CytFluorescein Irradiatoxicity of fluoresceinion Impacts Physiological Processes of HepG2 cells

Cytotoxicity of fluorescein irradiation

FluoreAscein is a relatively nontoxic compound (LD50 = 6.7 g/kg fo has been alr reats[38]), and it is widely used in medicine for diagnostic purposes, as it exhibits strongmentioned in this entry, fluorescence in aqueous media[1][2][4][6]. Thiin poss dye is also used as a fluorescent label in target tissues[1][5].ses relatively Llow toxicity was also observed for its stable photoproducts, created by exhaustive f. Intracellular fluorescein (administrated in the form of fluorescein diacetate (FDA) irradiation (FDA is used to study intracellular effects of fluorescein, as, which, unlike fluorescein, it is able to penetrate the cellular membrane where it is hydrolyzed to fluorescein [3959]) also showed minimal toxicity (Figure 1, graphs A and B). Low toxicity was also observed for its stable photoproducts (Figure 1, graphs C and D). However, simultaneous irradiation of cells treated with fluorescein led to a significant and time-dependent decrease in cell viability (Figure 1, graphs E and F), suggesting that one or more photoproducts formed during irradiation, which were not present in the solutions upon exhaustive irradiation (= stable photoproducts), were responsible for the observed cytotoxicity. This means that these species must be either volatile or short-lived (although reactive), pointing to CO and 1O2[1638].

Figure 1. Viability of HepG2 cells treated with solutions of non-irradiated FDA solution (A, B), solution of fluorescein photoproducts (C, D; tir = 24 h, I = 160 mW/cm2 prior to the treatment, FDA concentration = initial concentration of FDA prior irradiation), or simultaneously irradiated solutions of FDA (E, F; irradiation throughout the entire incubation time 2 or 24 h, I = 160 mW/cm2, FDA concentration = FDA initial concentration prior irradiation); *p ≤ 0.05 vs. untreated control.

This data was, however, obtained u

Effect on Krebs Cycle

Expon long irradiation times. Therefore, to obtain more clinically relevant data, as diagnostic fluorescein angiography lasts only a few minutes, sure of HepG2 cells treated with FDA or fluorescein were irradiated for 30 min, and analyzed immediately, or after further incubation for 2 or 24 h in the dark. Irradiation of cells treated with FDA showed a significant decrease in cell viability (≤ 80%) in the majority of the analyzed concentrations (19-300 μmol/l) for 2 and 24 h inco irradiation of intracellubation intervals; whereas this effect was much weaker when cells were treated with ar fluorescein[16].

Effect on Krebs Cycle

To, elucidate the effects of fluorescein irradiation on cellular metabolism, the concentrations of Krebs cycle intermediates and its anaplerotic pathways were analyzed in HepG2 cells. HepG2 cells treated with FDA were irradiated directly to find the immediate impact of the photochemical transformation of fluorescein to photoproducts, including 1O2 and CO. This urthermore, resulted in a significant decrease in the majority of metabolites, with the most significant changes in the concentrations of lactate, 2HG-hydroxyglutarate, 2OG-oxoglutarate, and citrate (<30% those of control)[1638]. This indicates that the above-mentioned biologically active by-products of fluorescein photoexcitation might affect the overall cellular energetic metabolism.

To test the hypothesis that the produced CO is responsible for decreased cell metabolism, HepG2 cells were incubated in an atmosphere containing 100 ppm of CO. A significant decrease in the concentrations of the Krebs cycle intermediates (2HG-hydroxyglutarate, glutamate, 2OG-oxoglutarate, and citrate) was oalso observed following CO treatment for 2 h(enriched CO atmosphere, 100 ppm)[1638], confirming the key role of this molecule in the observed attenuatis processon of cell metabolism caused by fluorescein irradiation. These results correspond to those observed upon CO exposure that demonstrated the inhibition of respiration and glycolysis and a decrease in some Krebs cycle metabolites[4060]. On the other hand, some published data have proved that CO can promote oxidative phosphorylation[4161][4262], mitochondrial biogenesis[4363], and even an increase in cytochrome c oxidase activity[4464], suggesting that the effect of CO is concentration- and tissue-dependent and reflects the overall cell/tissue status or oxygen level. In case, significant inhibition of the Krebs cycle was observed, which coincided with a relatively high FDA concentration and a long exposure to generated and simultaneously irradiated fluorescein.

Effect on Cell Cycle

Irradiation of FDA-treated cells also resulted in a significant increase in the G0 phase and a simultaneous decrease in G2/M phase (18% decrease when compared to control) of cell cycle, indicating reduced proliferation and thus the antiproliferative and anticancer potential of fluorescein. To assess the functionNo significant effect of CO, an analogous experiment was performed under a (enriched CO atmosphere. No significant effect of CO , 100 ppm) was observed on cell cycle progression, indicating no involvement of the CO released during the photoreaction in this process[1638]. However, CO has been suggested to affect the cell cycle[4565][4666], showing that this effect might be both dose- and cell-dependent.

Comparison of Different Fluorescein Administration Modes

CompTrearing the effects of the two modes of ftment of cells with free fluorescein compared to treatment (free fluorescein and cell-targeted with FDA gave different results. Comparing the effects of these two modes of fluorescein in the form of FDA) in treatment helped to assess the biological effects of  1O2 and CO when produced both intra- and extracellularly. Comparisons of the cell viability indicated that when administered as a free acid, fluorescein’s negative impact on viability is significantly smaller[1638]. In this case, the 1O2 molecules released during the photoreaction do not necessarily reach the intracellular compartment because of the short half-life of 1O2 (τ1/2 = 3–4 μs[4767]). On the other hand, the long-lived CO (τ1/2 = 3–4 h) can freely pass through the plasma membrane and affect cellular processes when generated extracellularly, as shown by Lazarus et al.[4868], who studied the intra- vs. extracellular delivery of CO using two types of CO-releasing molecules (CORMs) differing in their cellular localization. They showed that extracellular CO production exhibited a lower toxic effect on cells, whereas anti-inflammatory cell signaling processes were similar to those of intracellular delivery.

Impact of O

2

Concentration on Cytotoxicity of Fluorescein Irradiation

EFluorescein irradiation cytotoxicity experiments performed in a hypoxic chamber (a 9% O2 level was set according to the measured O2 level in rat livers[49]) showed that hypoxia was associated with a significantly lower drop in the viability of cells treated with either fluorescein or FDA when hen compared with cellsto that under normoxic conditions. Three different ways of how the O2 level may influence this parameter were proposed. A lower O2 level can result in: a lower yield of 1O2 (fewer O2 molecules available for sensitization); reduced efficiency of the fluorescein photoreaction (if 1O2 is responsible for its degradation) and thus less efficient CO release; or a different cellular metabolic status, any of which ultimately affects the cell’s survival[1638].

34.  Conclusion and Outlook

IFluorescein is a widely used fluorradiation of escent dye that has found its application in many fields of natural sciences. Medicine is no exception, where fluorescein plays the role of a tracer, contrast compound or diagnostic agent, etc. For many of these applications is fluorescein resuirradiated to yield fluorescence. It was found that this irradiation results in the production of the biologically active molecules 1O2  and CO. These molecules might be responsible for the phoExperiments on HepG2 cells also showed cytotoxicity of fluorescein, which increases with increasing dosage, times of i, attenuation of metabolism and decreased proliferation as a result of fluorescein irradiation, and tissue oxygenation levels. Moreover, the . This may indicate that volatile and reactive molecules produced during fluorescein photochemical reaction pro, from which 1O2 anduc CO were idents affect cell metabolism and proliferation. As itified, are responsible for some adverse effects observed with fluorescein administration to patients. On the other hand, as fluorescein releases CO in substantial amounts, it might even be used therapeutically as a photoCORM to release CO into target tissues irradiate. Another possibility of application is to employ both bioactive molecules, 1O2 and wCO, for the therapeutith lightc action, for example, in the treatment of cancer.

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