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The functions of hydrogen sulfide on the urogenital system of both males and females: from inception to the present

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Abstract

Hydrogen sulfide (H2S) is known as a chemical gas in nature with both enzymatic and non-enzymatic biosynthesis in different human organs. A couple of studies have demonstrated the function of H2S in regulating the homeostasis of the human body. Additionally, they have shown its synthesis, measurement, chemistry, protective effects, and interaction in various aspects of scientific evidence. Furthermore, many researches have demonstrated the beneficial impacts of H2S on genital organs and systems. According to various studies, it is recognized that H2S-producing enzymes and the endogenous production of H2S are expressed in male and female reproductive systems in different mammalian species. The main goal of this comprehensive review is to assess the potential therapeutic impacts of this gasotransmitter in the male and female urogenital system and find underlying mechanisms of this agent. This narrative review investigated the articles that were published from the 1970s to 2022. The review’s primary focus is the impacts of H2S on the male and female urogenital system. Medline, CINAHL, PubMed, and Google scholar databases were searched. Keywords used in this review were “Hydrogen sulfide,” “H2S,” “urogenital system,” and “urogenital tract”. Numerous studies have demonstrated the therapeutic and protective effects of sodium hydrosulfide (Na-HS) as an H2S donor on male and female infertility disorders. Furthermore, it has been observed that H2S plays a significant role in improving different diseases such as ameliorating sperm parameters. The specific localization of H2S enzymes in the urogenital system provides an excellent opportunity to comprehend its function and role in various disorders related to this system. It is noteworthy that H2S has been demonstrated to be produced in endocrine organs and exhibit diverse activities. Moreover, it is important to recognize that alterations in H2S biosynthesis are closely linked to endocrine disorders. Therefore, hormones can be pivotal in regulating H2S production, and H2S synthesis pathways may aid in establishing novel therapeutic strategies. H2S possesses pharmacological effects on essential disorders, such as anti-inflammation, anti-apoptosis, and anti-oxidant activities, which render it a valuable therapeutic agent for human urogenital disease. Furthermore, this agent shows promise in ameliorating the detrimental effects of various male and female diseases. Despite the limited clinical research, studies have demonstrated that applying H2S as an anti-oxidant source could ameliorate adverse effects of different conditions in the urogenital system. More clinical studies are required to confirm the role of this component in clinical settings.

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References

  • Abdel Moneim AE, Othman MS, Aref AM (2014) Azadirachta indica attenuates cisplatin-induced nephrotoxicity and oxidative stress. BioMed Res Int 2014:647131

    Article  PubMed  PubMed Central  Google Scholar 

  • Abdellatief SA, Galal AA, Farouk SM, Abdel-Daim MM (2017) Ameliorative effect of parsley oil on cisplatin-induced hepato-cardiotoxicity: a biochemical, histopathological, and immunohistochemical study. Biomed Pharmacother 86:482–491

    Article  CAS  PubMed  Google Scholar 

  • Abe K, Kimura H (1996) The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci 16(3):1066–1071

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Agis-Torres Á, Recio P, López-Oliva ME, Martínez MP, Barahona MV, Benedito S, Bustamante S, Jiménez-Cidre MÁ, García-Sacristán A, Prieto D (2018) Phosphodiesterase type 4 inhibition enhances nitric oxide- and hydrogen sulfide-mediated bladder neck inhibitory neurotransmission. Sci Rep 8(1):4711

    Article  PubMed  PubMed Central  Google Scholar 

  • Akbarian F, Tavalaee M, Dattilio M, Nasr-Esfahani MH (2022) Down-regulated expression of cystathionine β-synthase and cystathionine γ-lyase in varicocele, and infertile men: a case-control study. Cell Journal (Yakhteh) 24(4):176

    Google Scholar 

  • Alexander BE, Coles SJ, Fox BC, Khan TF, Maliszewski J, Perry A, Pitak MB, Whiteman M, Wood ME (2015) Investigating the generation of hydrogen sulfide from the phosphonamidodithioate slow-release donor GYY4137. MedChemComm 6(9):1649–1655

    Article  CAS  Google Scholar 

  • Al-Jaghbeer M, Dealmeida D, Bilderback A, Ambrosino R, Kellum JA (2018) Clinical decision support for in-hospital AKI. J Am Soc Nephrol 29(2):654–660

    Article  PubMed  Google Scholar 

  • Aminzadeh MA, Vaziri ND (2012) Downregulation of the renal and hepatic hydrogen sulfide (H2S)-producing enzymes and capacity in chronic kidney disease. Nephrol Dialy Transplant 27(2):498–504

    Article  CAS  Google Scholar 

  • Andersson KE (1992) Clinical pharmacology of potassium channel openers. Pharmacol Toxicol 70(4):244–254

    Article  CAS  PubMed  Google Scholar 

  • Andersson K-E, Arner A (2004) Urinary bladder contraction and relaxation: physiology and pathophysiology. Physiol Rev 84(3):935–986

    Article  CAS  PubMed  Google Scholar 

  • Aubard Y, Darodes N, Cantaloube M (2000) Hyperhomocysteinemia and pregnancy—review of our present understanding and therapeutic implications. Eur J Obst Gynecol Reprod Biol 93(2):157–165

    Article  CAS  Google Scholar 

  • Azarbarz N, Shafiei Seifabadi Z, Moaiedi MZ, Mansouri E (2020) Assessment of the effect of sodium hydrogen sulfide (hydrogen sulfide donor) on cisplatin-induced testicular toxicity in rats. Environ Sci Poll Res 27(8):8119–8128

    Article  CAS  Google Scholar 

  • Azizi F, Seifi B, Kadkhodaee M, Ahghari P (2016) Administration of hydrogen sulfide protects ischemia reperfusion-induced acute kidney injury by reducing the oxidative stress. Irish J Med Sci 1971 185:649–654

    Article  CAS  Google Scholar 

  • Azizi F, Seifi B, Kadkhodaee M (2017) Different dose-dependent effects of hydrogen sulfide on ischemia-reperfusion induced acute kidney injury in rats. Tehran Univ Med J TUMS Public 75(9):653–657

    Google Scholar 

  • Bannenberg GL, Vieira HL (2009) Therapeutic applications of the gaseous mediators carbon monoxide and hydrogen sulfide. Expert Opin Ther Patents 19(5):663–682

    Article  CAS  Google Scholar 

  • Bellomo R, Kellum JA, Ronco C (2012) Acute kidney injury. The Lancet 380(9843):756–766

    Article  Google Scholar 

  • Belmabkhout Y, Bhatt PM, Adil K, Pillai RS, Cadiau A, Shkurenko A, Maurin G, Liu G, Koros WJ, Eddaoudi M (2018) Natural gas upgrading using a fluorinated MOF with tuned H2S and CO2 adsorption selectivity. Nat Energy 3(12):1059–1066

    Article  CAS  Google Scholar 

  • Benavides GA, Squadrito GL, Mills RW, Patel HD, Isbell TS, Patel RP, Darley-Usmar VM, Doeller JE, Kraus DW (2007) Hydrogen sulfide mediates the vasoactivity of garlic. Proc Nat Acad Sci 104(46):17977–17982

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bigagli E, Luceri C, De Angioletti M, Chegaev K, D’ambrosio M, Riganti C, Gazzano E, Saponara S, Longini M, Luceri F (2018) New NO-and H2S-releasing doxorubicins as targeted therapy against chemoresistance in castration-resistant prostate cancer: in vitro and in vivo evaluations. Invest New Drugs 36:985–998

    Article  CAS  PubMed  Google Scholar 

  • Bikbov B, Purcell CA, Levey AS, Smith M, Abdoli A, Abebe M, Adebayo OM, Afarideh M, Agarwal SK, Agudelo-Botero M (2020) Global, regional, and national burden of chronic kidney disease, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017. The Lancet 395(10225):709–733

    Article  Google Scholar 

  • Bin-Jumah M, Abdel-Fattah A-FM, Saied EM, El-Seedi HR, Abdel-Daim MM (2021) Acrylamide-induced peripheral neuropathy: manifestations, mechanisms, and potential treatment modalities. Environ Sci Poll Res 28(11):13031–13046

    Article  CAS  Google Scholar 

  • Brading A (2006) Spontaneous activity of lower urinary tract smooth muscles: correlation between ion channels and tissue function. J Physiol 570(1):13–22

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Breza J, Soltysova A, Hudecova S, Penesova A, Szadvari I, Babula P, Chovancova B, Lencesova L, Pos O, Breza J (2018) Endogenous H2S producing enzymes are involved in apoptosis induction in clear cell renal cell carcinoma. BMC Cancer 18:1–8

    Article  Google Scholar 

  • Bucci M, Mirone V, Di Lorenzo A, Vellecco V, Roviezzo F, Brancaleone V, Ciro I, Cirino G (2009) Hydrogen sulphide is involved in testosterone vascular effect. Eur Urol 56(2):378–384

    Article  CAS  PubMed  Google Scholar 

  • Buckner SA, Milicic I, Daza A, Davis-Taber R, Scott VE, Sullivan JP, Brioni JD (2000) Pharmacological and molecular analysis of ATP-sensitive K+ channels in the pig and human detrusor. Eur J Pharmacol 400(2–3):287–295

    Article  CAS  PubMed  Google Scholar 

  • Cao X, Zhang W, Moore PK, Bian J (2019) Protective smell of hydrogen sulfide and polysulfide in cisplatin-induced nephrotoxicity. Int J Mol Sci 20(2):313

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen G, Chen H, Wang C, Peng Y, Sun L, Liu H, Liu F (2012) Rapamycin ameliorates kidney fibrosis by inhibiting the activation of mTOR signaling in interstitial macrophages and myofibroblasts. PloS One 7(3):e33626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen X, Xu W, Wang Y, Luo H, Quan S, Zhou J, Yang N, Zhang T, Wu L, Liu J (2014) Hydrogen sulfide reduces kidney injury due to urinary-derived sepsis by inhibiting NF-κB expression, decreasing TNF-α levels and increasing IL-10 levels. Exp Ther Med 8(2):464–470

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Y, Jin S, Teng X, Hu Z, Zhang Z, Qiu X, Tian D, Wu Y (2018) Hydrogen sulfide attenuates LPS-induced acute kidney injury by inhibiting inflammation and oxidative stress. Oxid Med Cell Longevity, 2018

  • Chevalier RL, Forbes MS, Thornhill BA (2009) Ureteral obstruction as a model of renal interstitial fibrosis and obstructive nephropathy. Kidney Int 75(11):1145–1152

    Article  PubMed  Google Scholar 

  • Christ GJ, Hodges S (2006) Molecular mechanisms of detrusor and corporal myocyte contraction: identifying targets for pharmacotherapy of bladder and erectile dysfunction. Br J Pharmacol 147(Suppl 2):S41

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chwatko G, Forma E, Wilkosz J, Głowacki R, Jóźwiak P, Różański W, Bryś M, Krześlak A (2013) Thiosulfate in urine as a facilitator in the diagnosis of prostate cancer for patients with prostate-specific antigen less or equal 10 ng/mL. Clin Chem Labor Med 51(9):1825–1831

    CAS  Google Scholar 

  • Cirino G, Fusco F, Imbimbo C, Mirone V (2006) Pharmacology of erectile dysfunction in man. Pharmacol Ther 111(2):400–423

    Article  CAS  PubMed  Google Scholar 

  • Cociba R (1971) Acute toxicologic and pathologic effects of cis-diamminedichloroplatinum (NSC-119875) in the male rat. Cancer Chemother Rep 55:1–8

    Google Scholar 

  • Dasari S, Tchounwou PB (2014) Cisplatin in cancer therapy: molecular mechanisms of action. Eur J Pharmacol 740:364–378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • di Villa d’Emmanuele, Bianca R, Sorrentino R, Maffia P, Mirone V, Imbimbo C, Fusco F, De Palma R, Ignarro LJ, Cirino G (2009) Hydrogen sulfide as a mediator of human corpus cavernosum smooth-muscle relaxation. Proc Nat Acad Sci 106(11):4513–4518

    Article  Google Scholar 

  • di Villa d’Emmanuele, Bianca R, Sorrentino R, Mirone V, Cirino G (2011) Hydrogen sulfide and erectile function: a novel therapeutic target. Nat Rev Urol 8(5):286–289

    Article  Google Scholar 

  • di Villa Bianca RD. E, Cirino G, Sorrentino R (2015) Hydrogen sulfide and urogenital tract. Chemistry, biochemistry and pharmacology of hydrogen sulfide, 111-136

  • Dinarello C (1997) Role of pro-and anti-inflammatory cytokines during inflammation: experimental and clinical findings. J Biol Reg Homeostatic Agents 11(3):91–103

    CAS  Google Scholar 

  • Djudjaj S, Chatziantoniou C, Raffetseder U, Guerrot D, Dussaule JC, Boor P, Kerroch M, Hanssen L, Brandt S, Dittrich A (2012) Notch-3 receptor activation drives inflammation and fibrosis following tubulointerstitial kidney injury. J Pathol 228(3):286–299

    Article  CAS  PubMed  Google Scholar 

  • Dombkowski RA, Doellman MM, Head SK, Olson KR (2006) Hydrogen sulfide mediates hypoxia-induced relaxation of trout urinary bladder smooth muscle. J Exp Biol 209(16):3234–3240

    Article  PubMed  Google Scholar 

  • Dugbartey GJ (2017) Diabetic nephropathy: A potential savior with ‘rotten-egg’smell. Pharmacol Rep 69(2):331–339

    Article  CAS  PubMed  Google Scholar 

  • Dugbartey GJ (2018) The smell of renal protection against chronic kidney disease: hydrogen sulfide offers a potential stinky remedy. Pharmacol Rep 70(2):196–205

    Article  CAS  PubMed  Google Scholar 

  • Eckardt K-U, Kasiske BL (2009) Kidney disease: improving global outcomes. Nat Rev Nephrol 5(11):650–657

    Article  PubMed  Google Scholar 

  • El Nahas AM, Bello AK (2005) Chronic kidney disease: the global challenge. The Lancet 365(9456):331–340

    Article  Google Scholar 

  • Fernandes VS, Ribeiro AS, Barahona MV, Orensanz LM, Martínez-Sáenz A, Recio P, Martínez AC, Bustamante S, Carballido J, García-Sacristán A (2013a) Hydrogen sulfide mediated inhibitory neurotransmission to the pig bladder neck: role of KATP channels, sensory nerves and calcium signaling. J Urol 190(2):746–756

  • Fernandes VS, Ribeiro AS, Martínez MP, Orensanz LM, Barahona MV, Martínez-Sáenz A, Recio P, Benedito S, Bustamante S, Carballido J (2013b) Endogenous hydrogen sulfide has a powerful role in inhibitory neurotransmission to the pig bladder neck. J Urol 189(4):1567–1573

  • Fernandes VS, Ribeiro AS, Martínez P, López-Oliva ME, Barahona MV, Orensanz LM, Martínez-Sáenz A, Recio P, Benedito S, Bustamante S (2014) Hydrogen sulfide plays a key role in the inhibitory neurotransmission to the pig intravesical ureter. PloS One 9(11):e113580

    Article  PubMed  PubMed Central  Google Scholar 

  • Florea A-M, Büsselberg D (2011) Cisplatin as an anti-tumor drug: cellular mechanisms of activity, drug resistance and induced side effects. Cancers 3(1):1351–1371

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fusco F (2012) d’Emmanuele di Villa Bianca Roberta, Mitidieri E, Cirino G, Sorrentino R, Mirone V: Sildenafil effect on the human bladder involves the L-cysteine/hydrogen sulfide pathway: a novel mechanism of action of phosphodiesterase type 5 inhibitors. Eur Urol 62:1174–1180

    Article  CAS  PubMed  Google Scholar 

  • Gai J-W, Wahafu W, Guo H, Liu M, Wang X-C, Xiao Y-X, Zhang L, Xin Z-C, Jin J (2013) Further evidence of endogenous hydrogen sulphide as a mediator of relaxation in human and rat bladder. Asian J Androl 15(5):692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geng B, Cui Y, Zhao J, Yu F, Zhu Y, Xu G, Zhang Z, Tang C, Du J (2007) Hydrogen sulfide downregulates the aortic L-arginine/nitric oxide pathway in rats. Am J Physiol-Reg Integr Comp Physiol 293(4):R1608–R1618

    Article  CAS  Google Scholar 

  • Gerő D, Torregrossa R, Perry A, Waters A, Le-Trionnaire S, Whatmore JL, Wood M, Whiteman M (2016) The novel mitochondria-targeted hydrogen sulfide (H2S) donors AP123 and AP39 protect against hyperglycemic injury in microvascular endothelial cells in vitro. Pharmacol Res 113:186–198

    Article  PubMed  PubMed Central  Google Scholar 

  • Gopalakrishnan M, Shieh C-C (2004) Potassium channel subtypes as molecular targets for overactive bladder and other urological disorders. Expert Opinion Tther Targets 8(5):437–458

    Article  CAS  Google Scholar 

  • Gratzke C, Streng T, Waldkirch E, Sigl K, Stief C, Andersson K-E, Hedlund P (2009) Transient receptor potential A1 (TRPA1) activity in the human urethra—evidence for a functional role for TRPA1 in the outflow region. Eur Urol 55(3):696–704

    Article  CAS  PubMed  Google Scholar 

  • Greabu M, Totan A, Miricescu D, Radulescu R, Virlan J, Calenic B (2016) Hydrogen sulfide, oxidative stress and periodontal diseases: a concise review. Antioxidants 5(1):3

    Article  PubMed  PubMed Central  Google Scholar 

  • Gump JM, Thorburn A (2011) Autophagy and apoptosis: what is the connection? Trends Cell Biol 21(7):387–392

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo H, Gai J-W, Wang Y, Jin H-F, Du J-B, Jin J (2012) Characterization of hydrogen sulfide and its synthases, cystathionine β-synthase and cystathionine γ-lyase, in human prostatic tissue and cells. Urology 79(2):483.e481-483.e485

    Article  Google Scholar 

  • Guzmán MA, Navarro MA, Carnicer R, Sarría AJ, Acín S, Arnal C, Muniesa P, Surra JC, Arbonés-Mainar JM, Maeda N (2006) Cystathionine β-synthase is essential for female reproductive function. Human Mol Gen 15(21):3168–3176

    Article  Google Scholar 

  • Hamidizad Z, Kadkhodaee M, Karimian SM, Ranjbaran M, Heidari F, Bakhshi E, Kianian F, Zahedi E, Seifi B (2022) Therapeutic effects of CORM3 and NaHS in chronic kidney disease induced cognitive impairment via the interaction between carbon monoxide and hydrogen sulfide on Nrf2/HO-1 signaling pathway in rats. Chemico-Biol Interact 368:110217

    Article  CAS  Google Scholar 

  • Hassanin A, Ahmed H, Kaddah A (2018) A global view of the pathophysiology of varicocele. Andrology 6(5):654–661

    Article  CAS  PubMed  Google Scholar 

  • Hayden L, Goeden H, Roth S (1990) Exposure to low levels of hydrogen sulfide elevates circulating glucose in maternal rats. J Toxicol Environ Health Part A Curr Issues 31(1):45–52

    Article  CAS  Google Scholar 

  • Hill J, Speer R (1982) Organo-platinum complexes as antitumor agents. Antican Res 2(3):173–186

    CAS  Google Scholar 

  • Isidori AM, Buvat J, Corona G, Goldstein I, Jannini EA, Lenzi A, Porst H, Salonia A, Traish AM, Maggi M (2014) A critical analysis of the role of testosterone in erectile function: from pathophysiology to treatment—a systematic review. Eur Urol 65(1):99–112

    Article  CAS  PubMed  Google Scholar 

  • Jacobs RL, House JD, Brosnan ME, Brosnan JT (1998) Effects of streptozotocin-induced diabetes and of insulin treatment on homocysteine metabolism in the rat. Diabetes 47(12):1967–1970

    Article  CAS  PubMed  Google Scholar 

  • Jacobs RL, Stead LM, Brosnan ME, Brosnan JT (2001) Hyperglucagonemia in rats results in decreased plasma homocysteine and increased flux through the transsulfuration pathway in liver. J Biol Chem 276(47):43740–43747

    Article  CAS  PubMed  Google Scholar 

  • Jiang D, Zhang Y, Yang M, Wang S, Jiang Z, Li Z (2014) Exogenous hydrogen sulfide prevents kidney damage following unilateral ureteral obstruction. Neurourol Urodyn 33(5):538–543

    Article  CAS  PubMed  Google Scholar 

  • Jupiter RC, Yoo D, Pankey EA, Reddy VV, Edward JA, Polhemus DJ, Peak TC, Katakam P, Kadowitz PJ (2015) Analysis of erectile responses to H2S donors in the anesthetized rat. Am J Physiol-Heart Circ Physiol 309(5):H835–H843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kabil O, Banerjee R (2014) Enzymology of H2S biogenesis, decay and signaling. Antioxidants Redox Signal 20(5):770–782

    Article  CAS  Google Scholar 

  • Kadlec M, Pintus E, Ros-Santaella JL (2022) The interaction of NO and H2S in boar spermatozoa under oxidative stress. Animals 12(5):602

    Article  PubMed  PubMed Central  Google Scholar 

  • Kajioka S, Nakayama S, Asano H, Seki N, Naito S, Brading AF (2008) Levcromakalim and MgGDP activate small conductance ATP-sensitive K+ channels of K+ channel pore 6.1/sulfonylurea receptor 2A in pig detrusor smooth muscle cells: uncoupling of cAMP signal pathways. J Pharmacol Exp Ther 327(1):114–123

    Article  CAS  PubMed  Google Scholar 

  • Kashfi K, Olson KR (2013) Biology and therapeutic potential of hydrogen sulfide and hydrogen sulfide-releasing chimeras. Biochem Pharmacol 85(5):689–703

    Article  CAS  PubMed  Google Scholar 

  • Khan MAH, Rao MV, Li Q (2019) Recent advances in electrochemical sensors for detecting toxic gases: NO2, SO2 and H2S. Sensors 19(4):905

    Article  PubMed  PubMed Central  Google Scholar 

  • Kimura H (2011) Hydrogen sulfide: its production, release and functions. Amino Acids 41(1):113–121

    Article  CAS  PubMed  Google Scholar 

  • Kimura H (2014) The physiological role of hydrogen sulfide and beyond. Nitric Oxide 41:4–10

    Article  CAS  PubMed  Google Scholar 

  • Lan A, Liao X, Mo L, Yang C, Yang Z, Wang X, Hu F, Chen P, Feng J, Zheng D (2011) Hydrogen sulfide protects against chemical hypoxia-induced injury by inhibiting ROS-activated ERK1/2 and p38MAPK signaling pathways in PC12 cells. PloS One 6(10):e25921

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee ZW, Zhou J, Chen C-S, Zhao Y, Tan C-H, Li L, Moore PK, Deng L-W (2011) The slow-releasing hydrogen sulfide donor, GYY4137, exhibits novel anti-cancer effects in vitro and in vivo. PloS One 6(6):e21077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee HJ, Feliers D, Barnes JL, Oh S, Choudhury GG, Diaz V, Galvan V, Strong R, Nelson J, Salmon A (2018) Hydrogen sulfide ameliorates aging-associated changes in the kidney. Geroscience 40:163–176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leslie SW, Sajjad H, Siref LE (2017) Varicocele

  • Li L, Whiteman M, Guan YY, Neo KL, Cheng Y, Lee SW, Zhao Y, Baskar R, Tan C-H, Moore PK (2008) Characterization of a novel, water-soluble hydrogen sulfide–releasing molecule (GYY4137) new insights into the biology of hydrogen sulfide. Circulation 117(18):2351–2360

    Article  CAS  PubMed  Google Scholar 

  • Li J, Li Y, Du Y, Mou K, Sun H, Zang Y, Liu C (2011) Endogenous hydrogen sulfide as a mediator of vas deferens smooth muscle relaxation. Fert Sterility 95(5):1833–1835

    Article  CAS  Google Scholar 

  • Li Y, Zang Y, Fu S, Zhang H, Gao L, Li J (2012) H2S relaxes vas deferens smooth muscle by modulating the large conductance Ca2+-activated K+ (BKCa) channels via a redox mechanism. J Sex Med 9(11):2806–2813

    Article  PubMed  Google Scholar 

  • Li L, Fox B, Keeble J, Salto-Tellez M, Winyard PG, Wood ME, Moore PK, Whiteman M (2013) The complex effects of the slow-releasing hydrogen sulfide donor GYY 4137 in a model of acute joint inflammation and in human cartilage cells. J Cell Mol Med 17(3):365–376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Li L, Zeng O, Liu JM, Yang J (2017) H2S improves renal fibrosis in STZ-induced diabetic rats by ameliorating TGF-β 1 expression. Renal Fail 39(1):265–272

    Article  CAS  Google Scholar 

  • Liang R, Yu W-D, Du J-B, Yang L-J, Shang M, Guo J-Z (2006) Localization of cystathionine β synthase in mice ovaries and its expression profile during follicular development. Chin Med J 119(22):1877–1883

    Article  CAS  PubMed  Google Scholar 

  • Liang R, Yu W-D, Du J-B, Yang L-J, Yang J-J, Xu J, Shang M, Guo J-Z (2007) Cystathionine β synthase participates in murine oocyte maturatione mediated by homocysteine. Reprod Toxicol 24(1):89–96

    Article  CAS  PubMed  Google Scholar 

  • Lin P-H, Aronson W, Freedland SJ (2015) Nutrition, dietary interventions and prostate cancer: the latest evidence. BMC Medicine 13(1):1–15

    Article  Google Scholar 

  • Lin S, Visram F, Liu W, Haig A, Jiang J, Mok A, Lian D, Wood ME, Torregrossa R, Whiteman M (2016) GYY4137, a slow-releasing hydrogen sulfide donor, ameliorates renal damage associated with chronic obstructive uropathy. J Urol 196(6):1778–1787

    Article  CAS  PubMed  Google Scholar 

  • Linden DR, Levitt MD, Farrugia G, Szurszewski JH (2010) Endogenous production of H2S in the gastrointestinal tract: still in search of a physiologic function. Antiox Redox Signal 12(9):1135–1146

    Article  CAS  Google Scholar 

  • Liu Y (2006) Renal fibrosis: new insights into the pathogenesis and therapeutics. Kidney Int 69(2):213–217

    Article  CAS  PubMed  Google Scholar 

  • Liu Y (2011) Cellular and molecular mechanisms of renal fibrosis. Nat Rev Nephrol 7(12):684–696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lobb I, Mok A, Lan Z, Liu W, Garcia B, Sener A (2012) Supplemental hydrogen sulphide protects transplant kidney function and prolongs recipient survival after prolonged cold ischaemia–reperfusion injury by mitigating renal graft apoptosis and inflammation. BJU International 110(11c):E1187–E1195

    Article  CAS  PubMed  Google Scholar 

  • Lobb I, Zhu J, Liu W, Haig A, Lan Z, Sener A (2014) Hydrogen sulfide treatment ameliorates long-term renal dysfunction resulting from prolonged warm renal ischemia-reperfusion injury. Canad Urol Assoc J 8(5–6):E413

    Article  Google Scholar 

  • Lobb I, Davison M, Carter D, Liu W, Haig A, Gunaratnam L, Sener A (2015) Hydrogen sulfide treatment mitigates renal allograft ischemia-reperfusion injury during cold storage and improves early transplant kidney function and survival following allogeneic renal transplantation. J Urol 194(6):1806–1815

    Article  CAS  PubMed  Google Scholar 

  • Lorian K, Kadkhodaee M, Kianian F, Abdi A, Sadeghipour H, Seifi B (2019) Oxidative stress, nitric oxide and inflammation in the pathophysiology of varicocele and the effect of hydrogen sulfide as a potential treatment. Physiol Pharmacol 23(4):249–260

    Google Scholar 

  • Lorian K, Kadkhodaee M, Kianian F, Abdi A, Ranjbaran M, Ashabi G, Seifi B (2020a) Long-term NaHS administration reduces oxidative stress and apoptosis in a rat model of left-side varicocele. Andrologia 52(2):e13496

  • Lorian K, Kadkhodaee M, Kianian F, Abdi A, Seifi B (2020b) Administration of sodium hydrosulfide reduces remote organ injury by an anti-oxidant mechanism in a rat model of varicocele. Iran J Basic Med Sci 23(2):236

  • Lozano R, Naghavi M, Foreman K, Lim S, Shibuya, K (2010) Aboyans V et al.(2012). Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study

  • Luo Y, Liu X, Zheng Q, Wan X, Ouyang S, Yin Y, Sui X, Liu J, Yang X (2012) Hydrogen sulfide prevents hypoxia-induced apoptosis via inhibition of an H2O2-activated calcium signaling pathway in mouse hippocampal neurons. Biochem Biophys Res Commun 425(2):473–477

    Article  CAS  PubMed  Google Scholar 

  • Luo R, Hu S, Liu Q, Han M, Wang F, Qiu M, Li S, Li X, Yang T, Fu X (2019) Hydrogen sulfide upregulates renal AQP-2 protein expression and promotes urine concentration. The FASEB Journal 33(1):469

    Article  CAS  PubMed  Google Scholar 

  • Mahajan S, Jagtap S (2021) Nanomaterials-based resistive sensors for detection of environmentally hazardous H2S gas. J Electr Mater 50(5):2531–2555

    Article  CAS  Google Scholar 

  • Matsunami M, Miki T, Nishiura K, Hayashi Y, Okawa Y, Nishikawa H, Sekiguchi F, Kubo L, Ozaki T, Tsujiuchi T (2012) Involvement of the endogenous hydrogen sulfide/Cav3 2 T-type Ca2+ channel pathway in cystitis-related bladder pain in mice. Br J Pharmacol 167(4):917–928

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mayorga AJ, Lucki I (2001) Limitations on the use of the C57BL/6 mouse in the tail suspension test. Psychopharmacology 155:110–112

    Article  CAS  PubMed  Google Scholar 

  • Mazzei LJ, García IM, Altamirano L, Docherty NG, Manucha W (2012) Rosuvastatin preserves renal structure following unilateral ureteric obstruction in the neonatal rat. Am J Nephrol 35(2):103–113

    Article  CAS  PubMed  Google Scholar 

  • Mercado MG, Smith DK, Guard EL (2019) Acute kidney injury: diagnosis and management. Am Fam Phys 100(11):687–694

    Google Scholar 

  • Mikami Y, Shibuya N, Kimura Y, Nagahara N, Ogasawara Y, Kimura H (2011) Thioredoxin and dihydrolipoic acid are required for 3-mercaptopyruvate sulfurtransferase to produce hydrogen sulfide. Biochem J 439(3):479–485

    Article  CAS  PubMed  Google Scholar 

  • Miller RP, Tadagavadi RK, Ramesh G, Reeves WB (2010) Mechanisms of cisplatin nephrotoxicity. Toxins 2(11):2490–2518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mokhlis HA, Rashed MH, Saleh IG, Eldeib MG, El-Husseiny AA, Khidr EG, Gomaa MH, Gad HS, Aglan A (2022) Hydrogen sulfide alleviates acrylamide-induced testicular toxicity in male rats. Toxicol Environ Health Sci, 1-11

  • Oi Y, Imafuku M, Shishido C, Kominato Y, Nishimura S, Iwai K (2001) Garlic supplementation increases testicular testosterone and decreases plasma corticosterone in rats fed a high protein diet. J Nutr 131(8):2150–2156

    Article  CAS  PubMed  Google Scholar 

  • Olson KR (2015) Hydrogen sulfide as an oxygen sensor. Antiox Redox Signal 22(5):377–397

    Article  CAS  Google Scholar 

  • Ozbek E, Ilbey YO, Ozbek M, Simsek A, Cekmen M, Somay A (2009) Melatonin attenuates unilateral ureteral obstruction–induced renal injury by reducing oxidative stress, iNOS, MAPK, and NF-kB expression. J Endourol 23(7):1165–1173

    Article  PubMed  Google Scholar 

  • Patacchini R, Santicioli P, Giuliani S, Maggi CA (2004) Hydrogen sulfide (H2S) stimulates capsaicin-sensitive primary afferent neurons in the rat urinary bladder. Br J Pharmacol 142(1):31–34

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patacchini R, Santicioli P, Giuliani S, Maggi CA (2005) Pharmacological investigation of hydrogen sulfide (H2S) contractile activity in rat detrusor muscle. Eur J Pharmacol 509(2–3):171–177

    Article  CAS  PubMed  Google Scholar 

  • Patel P, Vatish M, Heptinstall J, Wang R, Carson RJ (2009) The endogenous production of hydrogen sulphide in intrauterine tissues. Reprod Biol Endocrinol 7(1):1–9

    Article  Google Scholar 

  • Petkov GV, Heppner TJ, Bonev AD, Herrera GM, Nelson MT (2001) Low levels of KATP channel activation decrease excitability and contractility of urinary bladder. Am J Physiol-Reg Integr Compar Physiol 280(5):R1427–R1433

    Article  CAS  Google Scholar 

  • Peyster E, Chen J, Feldman HI, Go AS, Gupta J, Mitra N, Pan Q, Porter A, Rahman M, Raj D (2017) Inflammation and arterial stiffness in chronic kidney disease: findings from the CRIC study. Am J Hyp 30(4):400–408

    Article  CAS  Google Scholar 

  • Pieretti JC, Junho CVC, Carneiro-Ramos MS, Seabra AB (2020) H2S-and NO-releasing gasotransmitter platform: a crosstalk signaling pathway in the treatment of acute kidney injury. Pharmacol Res 161:105121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Powell CR, Dillon KM, Matson JB (2018) A review of hydrogen sulfide (H2S) donors: chemistry and potential therapeutic applications. Biochem Pharmacol 149:110–123

    Article  CAS  PubMed  Google Scholar 

  • Pugsley D, Norris KC, Garcia-Garcia G, Agodoa L (2009) Global approaches for understanding the disproportionate burden of chronic kidney disease. Ethn Dis 19(Suppl 1):S1-1

    PubMed  Google Scholar 

  • Qiu X, Villalta J, Lin G, Lue TF (2012) Role of hydrogen sulfide in the physiology of penile erection. J Androl 33(4):529–535

    Article  CAS  PubMed  Google Scholar 

  • Qiu H, Chen X, Luo Z, Zhao L, Zhang T, Yang N, Long X, Xie H, Liu J, Xu W (2018) Inhibition of endogenous hydrogen sulfide production exacerbates the inflammatory response during urine-derived sepsis-induced kidney injury. Exp Ther Med 16(4):2851–2858

    PubMed  PubMed Central  Google Scholar 

  • Raj A, Ibrahim S, Jagannath A (2020) Combustion kinetics of H2S and other sulfurous species with relevance to industrial processes. Prog Energy Combust Sci 80:100848

    Article  Google Scholar 

  • Ratnam S, Maclean KN, Jacobs RL, Brosnan ME, Kraus JP, Brosnan JT (2002) Hormonal regulation of cystathionine β-synthase expression in liver. J Biol Chem 277(45):42912–42918

    Article  CAS  PubMed  Google Scholar 

  • Reiffenstein R, Hulbert WC, Roth SH (1992) Toxicology of hydrogen sulfide. Annual Rev Pharmacol Toxicol 32(1):109–134

    Article  CAS  Google Scholar 

  • Renders L, Mayer-Kadner I, Koch C, Schärffe S, Burkhardt K, Veelken R, Schmieder RE, Hauser IA (2001) Efficacy and drug interactions of the new HMG-CoA reductase inhibitors cerivastatin and atorvastatin in CsA-treated renal transplant recipients. Nephrol Dial Transplant 16(1):141–146

    Article  CAS  PubMed  Google Scholar 

  • Renga B (2011) Hydrogen sulfide generation in mammals: the molecular biology of cystathionine-β-synthase (CBS) and cystathionine-γ-lyase (CSE). Inflammation Allergy-Drug Targets (formerly current drug targets-inflammation & allergy)(discontinued), 10(2), 85-91

  • Rhyu DY, Yang Y, Ha H, Lee GT, Song JS, Uh S-T, Lee HB (2005) Role of reactive oxygen species in TGF-β1-induced mitogen-activated protein kinase activation and epithelial-mesenchymal transition in renal tubular epithelial cells. J Am Soc Nephrol 16(3):667–675

    Article  CAS  PubMed  Google Scholar 

  • Ries F, Klastersky J (1986) Nephrotoxicity induced by cancer chemotherapy with special emphasis on cisplatin toxicity. Am J Kidney Dis 8(5):368–379

    Article  CAS  PubMed  Google Scholar 

  • Robaire B, Hermo L (1988) Efferent ducts, epididymis, and vas deferens: structure, functions, and their regulation. Physiol Reprod 1:999–1080

    Google Scholar 

  • Rossi S, Hsu R, Blick C, Goh V, Nathan P, Nicol D, Fleming S, Sweeting M, Wilson E, Stewart G (2017) Meta-analysis of the prevalence of renal cancer detected by abdominal ultrasonography. J Br Surge 104(6):648–659

    Article  CAS  Google Scholar 

  • Roth KS, Carter WH Jr, Chan JC (2001) Obstructive nephropathy in children: long-term progression after relief of posterior urethral valve. Pediatrics 107(5):1004–1010

    Article  CAS  PubMed  Google Scholar 

  • Russo D (2000) Evidence that hydrogen sulphide can modulate hypothalamo-pituitary-adrenal axis function: in vitro and in vivo studies in the rat. J Neuroendocrinol 12(3):225–233

    Article  Google Scholar 

  • Santoso JT, Lucci JA, Coleman RL, Schafer I, Hannigan EV (2003) Saline, mannitol, and furosemide hydration in acute cisplatin nephrotoxicity: a randomized trial. Cancer Chemother Pharmacol 52:13–18

    Article  CAS  PubMed  Google Scholar 

  • Scales Jr CD, Smith AC, Hanley JM, Saigal CS, Project UDIA (2012) Prevalence of kidney stones in the United States. Eur Urol, 62(1), 160-165

  • Scammahorn JJ, Nguyen IT, Bos EM, Van Goor H, Joles JA (2021) Fighting oxidative stress with sulfur: hydrogen sulfide in the renal and cardiovascular systems. Antioxidants 10(3):373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schalinske KL (2003) Interrelationship between diabetes and homocysteine metabolism: hormonal regulation of cystathionine [beta]-synthase. Nutr Rev 61(4):136

    Article  PubMed  Google Scholar 

  • Shackelford RE, Abdulsattar J, Wei EX, Cotelingam J, Coppola D, Herrera GA (2017) Increased nicotinamide phosphoribosyltransferase and cystathionine-β-synthase in renal oncocytomas, renal urothelial carcinoma, and renal clear cell carcinoma. Antican Res 37(7):3423–3427

    CAS  Google Scholar 

  • Shafie A, Kianian F, Ashabi G, Kadkhodaee M, Ranjbaran M, Hajiaqaei M, Lorian K, Abdi A, Seifi B (2022) Beneficial effects of combination therapy with testosterone and hydrogen sulfide by reducing oxidative stress and apoptosis: rat experimental varicocele model. International J Reprod BioMed (IJRM), 941–954-941–954

  • Shibuya N, Kimura H (2013) Production of hydrogen sulfide from d-cysteine and its therapeutic potential. Front Endocrinol 4:87

    Article  Google Scholar 

  • Shibuya N, Koike S, Tanaka M, Ishigami-Yuasa M, Kimura Y, Ogasawara Y, Fukui K, Nagahara N, Kimura H (2013) A novel pathway for the production of hydrogen sulfide from D-cysteine in mammalian cells. Nat Commun 4(1):1366

    Article  PubMed  Google Scholar 

  • Shirazi MK, Azarnezhad A, Abazari MF, Poorebrahim M, Ghoraeian P, Sanadgol N, Bokharaie H, Heydari S, Abbasi A, Kabiri S (2019) The role of nitric oxide signaling in renoprotective effects of hydrogen sulfide against chronic kidney disease in rats: involvement of oxidative stress, autophagy and apoptosis. J Cell Physiol 234(7):11411–11423

    Article  CAS  PubMed  Google Scholar 

  • Shukla N, Rossoni G, Hotston M, Sparatore A, Del Soldato P, Tazzari V, Persad R, Angelini GD, Jeremy JY (2009) Effect of hydrogen sulphide-donating sildenafil (ACS6) on erectile function and oxidative stress in rabbit isolated corpus cavernosum and in hypertensive rats. BJU International 103(11):1522–1529

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sidhu R, Singh M, Samir G, Carson RJ (2001) L-cysteine and sodium hydrosulphide inhibit spontaneous contractility in isolated pregnant rat uterine strips in vitro. Pharmacol Toxicol 88(4):198–203

    Article  CAS  PubMed  Google Scholar 

  • Sluman C, Gudka, PM, McCormick K (2020). Acute kidney injury: pre-renal, intra-renal and post-renal. Renal Med Clin Pharm, 23-44

  • Sogutdelen E, Pacoli K, Juriasingani S, Akbari M, Gabril M, Sener A (2020) Patterns of expression of H2S-producing enzyme in human renal cell carcinoma specimens: Potential avenue for future therapeutics. In Vivo 34(5):2775–2781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song K, Wang F, Li Q, Shi Y-B, Zheng H-F, Peng H, Shen H-Y, Liu C-F, Hu L-F (2014) Hydrogen sulfide inhibits the renal fibrosis of obstructive nephropathy. Kidney Int 85(6):1318–1329

    Article  CAS  PubMed  Google Scholar 

  • Song K, Li Q, Yin X-Y, Lu Y, Liu C-F, Hu L-F (2015) Hydrogen sulfide: a therapeutic candidate for fibrotic disease? Oxidat Med Cell Longevity 2015:1–10

    CAS  Google Scholar 

  • Song ZL, Zhao L, Ma T, Osama A, Shen T, He Y, Fang J (2022) Progress and perspective on hydrogen sulfide donors and their biomedical applications. Med Res Rev 42(5):1930–1977

    Article  CAS  PubMed  Google Scholar 

  • Sonke E, Verrydt M, Postenka CO, Pardhan S, Willie CJ, Mazzola CR, Hammers MD, Pluth MD, Lobb I, Power NE (2015) Inhibition of endogenous hydrogen sulfide production in clear-cell renal cell carcinoma cell lines and xenografts restricts their growth, survival and angiogenic potential. Nitric Oxide 49:26–39

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Srilatha B, Adaikan PG, Moore PK (2006) Possible role for the novel gasotransmitter hydrogen sulphide in erectile dysfunction—a pilot study. Eur J Pharmacol 535(1–3):280–282

    Article  CAS  PubMed  Google Scholar 

  • Srilatha B, Adaikan PG, Li L, Moore PK (2007) Hydrogen sulphide: a novel endogenous gasotransmitter facilitates erectile function. J Sex Med 4(5):1304–1311

    Article  CAS  PubMed  Google Scholar 

  • Srilatha B, Hu L, Adaikan GP, Moore PK (2009) Basic science: initial characterization of hydrogen sulfide effects in female sexual function. J Sex Med 6(7):1875–1884

    Article  CAS  PubMed  Google Scholar 

  • Srilatha B, Hu L, Adaikan GP, Moore PK (2009) Initial characterization of hydrogen sulfide effects in female sexual function. J Sex Med 6(7):1875–1884

    Article  CAS  PubMed  Google Scholar 

  • Stipanuk MH, Beck PW (1982) Characterization of the enzymic capacity for cysteine desulphhydration in liver and kidney of the rat. Biochem J 206(2):267–277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stone, E. (1996). Prostatic intraepithelial neoplasia: will it help doctors pinpoint early prostate cancer? In: Oxford University Press

  • Streng T, Axelsson HE, Hedlund P, Andersson DA, Jordt S-E, Bevan S, Andersson K-E, Högestätt ED, Zygmunt PM (2008) Distribution and function of the hydrogen sulfide–sensitive TRPA1 ion channel in rat urinary bladder. Eur Urol 53(2):391–400

    Article  CAS  PubMed  Google Scholar 

  • Su JS, Farber NJ, Vij SC (2021) Pathophysiology and treatment options of varicocele: an overview. Andrologia 53(1):e13576

    Article  PubMed  Google Scholar 

  • Sugiura Y, Kashiba M, Maruyama K, Hoshikawa K, Sasaki R, Saito K, Kimura H, Goda N, Suematsu M (2005) Cadmium exposure alters metabolomics of sulfur-containing amino acids in rat testes. Antiox Redox Signal 7(5–6):781–787

    Article  CAS  Google Scholar 

  • Taguchi T, Nazneen A, Abid MR, Razzaque MS (2005) Cisplatin-associated nephrotoxicity and pathological events. Cell Stress Resp Renal eases 148:107–121

    Article  CAS  Google Scholar 

  • Tang X, Lieske JC (2014) Acute and chronic kidney injury in nephrolithiasis. Curr Opin Nephrol Hyper 23(4):385

    Article  CAS  Google Scholar 

  • Tekşen Y, Kadıoğlu E, Koçak C, Koçak H (2019) Effect of hydrogen sulfide on kidney injury in rat model of crush syndrome. J Surgic Res 235:470–478

    Article  Google Scholar 

  • Tiranti V, Zeviani M (2013) Altered sulfide (H2S) metabolism in ethylmalonic encephalopathy. Cold Spring Harbor Perspect Biol 5(1):a011437

    Article  Google Scholar 

  • Ucero AC, Benito-Martin A, Izquierdo MC, Sanchez-Niño MD, Sanz AB, Ramos AM, Berzal S, Ruiz-Ortega M, Egido J, Ortiz A (2014) Unilateral ureteral obstruction: beyond obstruction. Int Urol Nephrol 46:765–776

    Article  PubMed  Google Scholar 

  • Wagner H, Cheng JW, Ko EY (2018) Role of reactive oxygen species in male infertility: an updated review of literature. Arab J Urol 16(1):35–43

    Article  PubMed  Google Scholar 

  • Wang J, Wang W, Li S, Han Y, Zhang P, Meng G, Xiao Y, Xie L, Wang X, Sha J (2018) Hydrogen sulfide as a potential target in preventing spermatogenic failure and testicular dysfunction. Antioxid Redox Signal 28(16):1447–1462

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Xing Q-Q, Tu J-K, Tang W-B, Yuan X-N, Xie Y-Y, Wang W, Peng Z-Z, Huang L, Xu H (2019) Involvement of hydrogen sulfide in the progression of renal fibrosis. Chinese Med J 132(23):2872–2880

    Article  CAS  Google Scholar 

  • Wang S, Liu X, Liu Y (2022) Hydrogen sulfide protects from acute kidney injury via attenuating inflammation activated by necroptosis in dogs. J Veterin Sci 23(5):e72

    Google Scholar 

  • Watanabe M, Osada J, Aratani Y, Kluckman K, Reddick R, Malinow MR, Maeda N (1995) Mice deficient in cystathionine beta-synthase: animal models for mild and severe homocyst (e) inemia. Proc Nat Acad Sci 92(5):1585–1589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Welch WJ, Blau J, Xie H, Chabrashvili T, Wilcox CS (2005) Angiotensin-induced defects in renal oxygenation: role of oxidative stress. Am J Physiol-Heart Circ Physiol 288(1):H22–H28

    Article  CAS  PubMed  Google Scholar 

  • Wu D, Luo N, Wang L, Zhao Z, Bu H, Xu G, Yan Y, Che X, Jiao Z, Zhao T (2017a) Hydrogen sulfide ameliorates chronic renal failure in rats by inhibiting apoptosis and inflammation through ROS/MAPK and NF-κ B signaling pathways. Sci Rep 7(1):455

  • Wu W, Hou C-L, Mu X-P, Sun C, Zhu Y-C, Wang M-J, Lv Q-Z (2017b) H2S donor NaHS changes the production of endogenous H2S and NO in D-galactose-induced accelerated ageing. Oxidative Med Cell Longevity 2017:1–14

  • Xia M, Chen L, Muh RW, Li P-L, Li N (2009) Production and actions of hydrogen sulfide, a novel gaseous bioactive substance, in the kidneys. J Pharmacol Exp Therap 329(3):1056–1062

    Article  CAS  Google Scholar 

  • Xia Y-Q, Ning J-Z, Cheng F, Yu W-M, Rao T, Ruan Y, Yuan R, Du Y (2019) GYY4137 a H2S donor, attenuates ipsilateral epididymis injury in experimentally varicocele-induced rats via activation of the PI3K/Akt pathway. Iran J Basic Med Sci 22(7):729

    PubMed  PubMed Central  Google Scholar 

  • Xiong M, Gong J, Liu Y, Xiang R, Tan X (2012) Loss of vitamin D receptor in chronic kidney disease: a potential mechanism linking inflammation to epithelial-to-mesenchymal transition. Am J Physiol-Renal Physiol 303(7):F1107–F1115

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto J, Sato W, Kosugi T, Yamamoto T, Kimura T, Taniguchi S, Kojima H, Maruyama S, Imai E, Matsuo S (2013) Distribution of hydrogen sulfide (H 2 S)-producing enzymes and the roles of the H 2 S donor sodium hydrosulfide in diabetic nephropathy. Clin Exp Nephrol 17:32–40

    Article  CAS  PubMed  Google Scholar 

  • Yan L, Jiaqiong L, Yue G, Xiaoyong L, Xuexian T, Ming L, Yinglan L, Xinxue L, Zena H (2020) Atorvastatin protects against contrast-induced acute kidney injury via upregulation of endogenous hydrogen sulfide. Renal Fail 42(1):270–281

    Article  Google Scholar 

  • Yang G, Wu L, Jiang B, Yang W, Qi J, Cao K, Meng Q, Mustafa AK, Mu W, Zhang S (2008) H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine γ-lyase. Science 322(5901):587–590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang J, Minkler P, Grove D, Wang R, Willard B, Dweik R, Hine C (2019) Non-enzymatic hydrogen sulfide production from cysteine in blood is catalyzed by iron and vitamin B6. Commun Biol 2(1):1–14

    Article  CAS  Google Scholar 

  • Yeh CH, Chiang HS, Lai TY, Chien CT (2011) Unilateral ureteral obstruction evokes renal tubular apoptosis via the enhanced oxidative stress and endoplasmic reticulum stress in the rat. Neurourol Urodynam 30(3):472–479

    Article  CAS  Google Scholar 

  • Yetik-Anacak G, Dikmen A, Coletta C, Mitidieri E, Dereli M, Donnarumma E, di Villa BRDE, Sorrentino R (2016) Hydrogen sulfide compensates nitric oxide deficiency in murine corpus cavernosum. Pharmacol Res 113:38–43

    Article  CAS  PubMed  Google Scholar 

  • Yildiz O, Seyrek M, Irkilata HC, Yildirim I, Tahmaz L, Dayanc M (2009) Testosterone might cause relaxation of human corpus cavernosum by potassium channel opening action. Urology 74(1):229–232

    Article  PubMed  Google Scholar 

  • Yuksel S, Erginel B, Bingul I, Ozluk Y, Karatay H, Aydın F, Keskin E (2022) The effect of hydrogen sulfide on ischemi̇a/reperfusion injury in an experimental testicular torsion model. J Pediatric Urol 18(1):16.e11-16.e17

    Article  Google Scholar 

  • Yurinskaya M, Krasnov G, Kulikova D, Zatsepina O, Vinokurov M, Chuvakova L, Rezvykh A, Funikov S, Morozov A, Evgen’ev M (2020) H2S counteracts proinflammatory effects of LPS through modulation of multiple pathways in human cells. Inflam Res 69(5):481–495

    Article  CAS  Google Scholar 

  • Zeng O, Li F, Li Y, Li L, Xiao T, Chu C, Yang J (2016) Effect of novel gasotransmitter hydrogen sulfide on renal fibrosis and connexins expression in diabetic rats. Bioengineered 7(5):314–320

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Zhi L, Moochhala S, Moore PK, Bhatia M (2007) Hydrogen sulfide acts as an inflammatory mediator in cecal ligation and puncture-induced sepsis in mice by upregulating the production of cytokines and chemokines via NF-κB. Am J Physiol-Lung Cell Mol Physiol 292(4):L960–L971

    Article  CAS  PubMed  Google Scholar 

  • Zhang D, Du J, Tang C, Huang Y, Jin H (2017) H2S-induced sulfhydration: biological function and detection methodology. Front Pharmacol 8:608

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang W, Zhao Y, Zhang P, Hao Y, Yu S, Min L, Li L, Ma D, Chen L, Yi B (2018) Decrease in male mouse fertility by hydrogen sulfide and/or ammonia can be inheritable. Chemosphere 194:147–157

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Bai Z, Zhu L, Liang Y, Fan X, Li J, Wen H, Shi T, Zhao Q, Wang Z (2020) Hydrogen sulfide donors: Therapeutic potential in anti-atherosclerosis. Eur J Med Chem 205:112665

    Article  CAS  PubMed  Google Scholar 

  • Zhao Y, Pluth MD (2016) Hydrogen sulfide donors activated by reactive oxygen species. Angewandte Chemie 128(47):14858–14862

    Article  Google Scholar 

  • Zhao Y, Zhang W-D, Liu X-Q, Zhang P-F, Hao Y-N, Li L, Chen L, Shen W, Tang X-F, Min L-J (2016) Hydrogen sulfide and/or ammonia reduces spermatozoa motility through AMPK/AKT related pathways. Sci Rep 6(1):1–11

    Google Scholar 

  • Zhi L, Ang AD, Zhang H, Moore PK, Bhatia M (2007) Hydrogen sulfide induces the synthesis of proinflammatory cytokines in human monocyte cell line U937 via the ERK-NF-κB pathway. J Leukocyte Biol 81(5):1322–1332

    Article  CAS  PubMed  Google Scholar 

  • Zhou Y, Zhu X, Wang X, Peng Y, Du J, Yin H, Yang H, Ni X, Zhang W (2020) H2S alleviates renal injury and fibrosis in response to unilateral ureteral obstruction by regulating macrophage infiltration via inhibition of NLRP3 signaling. Exp Cell Res 387(1):111779

    Article  CAS  PubMed  Google Scholar 

  • Zhu X-Y, Gu H, Ni X (2011) Hydrogen sulfide in the endocrine and reproductive systems. Expert Rev of Clin Pharmacol 4(1):75–82

    Article  CAS  Google Scholar 

  • Zou S, Shimizu T, Shimizu S, Higashi Y, Nakamura K, Ono H, Aratake T, Saito M (2018) Possible role of hydrogen sulfide as an endogenous relaxation factor in the rat bladder and prostate. Neurourol Urodynam 37(8):2519–2526

    Article  CAS  Google Scholar 

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S.S. and K.L. wrote the main manuscript text and A.F.F., M.M., and A.M.B. prepared Figs. 1, 2, 3, 4 and 5. All authors reviewed the manuscript. The authors confirm that no paper mill and artificial intelligence was used.

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Salehiyeh, S., Faiz, A.F., Manzourolhojeh, M. et al. The functions of hydrogen sulfide on the urogenital system of both males and females: from inception to the present. Naunyn-Schmiedeberg's Arch Pharmacol (2024). https://doi.org/10.1007/s00210-024-03086-8

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