Aquaporin 9 regulates Leydig cell steroidogenesis in diabetes

References

• Ahmad J. 2016. The diabetic foot. Diabetes Metab Syndr. 10(1):48–60.
   PubMedGoogle Scholar
• Ala M, Mohammad Jafari R, Hajiabbasi A, Dehpour AR. 2021. Aquaporins and diseases pathogenesis: from trivial to undeniable involvements, a disease-based point of view. J Cell Physiol. 236(9):6115–6135.
   PubMed Web of Science ®Google Scholar
• Alves MG, Martins AD, Rato L, Moreira PI, Socorro S, Oliveira PF. 2013. Molecular mechanisms beyond glucose transport in diabetes-related male infertility. Biochim Biophys Acta. 1832(5):626–635.
   PubMed Web of Science ®Google Scholar
• American Diabetes Association. 2013. Diagnosis and classification of diabetes mellitus. Diabetes Care. 36 (Suppl 1):S67–S74.
   PubMed Web of Science ®Google Scholar
• Andes LJ, Cheng YJ, Rolka DB, Gregg EW, Imperatore G. 2020. Prevalence of prediabetes among adolescents and young adults in the United States, 2005–2016. JAMA Pediatr. 174(2):e194498.
   PubMed Web of Science ®Google Scholar
• Arab HH, Gad AM, Reda E, Yahia R, Eid AH. 2021. Activation of autophagy by sitagliptin attenuates cadmium-induced testicular impairment in rats: targeting AMPK/mTOR and Nrf2/HO-1 pathways. Life Sci. 269:119031.
   PubMed Web of Science ®Google Scholar
• Azad AK, Raihan T, Ahmed J, Hakim A, Emon TH, Chowdhury PA. 2021. Human aquaporins: functional diversity and potential roles in infectious and non-infectious. Front Genet. 12(654865):654865.
   PubMedGoogle Scholar
• Badran HH, Hermo LS. 2002. Expression and regulation of aquaporins 1, 8, and 9 in the testis, efferent ducts, and epididymis of adult rats and during postnatal development. J Androl. 23(3):358–373.
   PubMedGoogle Scholar
• Barkabi-Zanjani S, Ghorbanzadeh V, Aslani M, Ghalibafsabbaghi A, Chodari L. 2020. Diabetes mellitus and the impairment of male reproductive function: possible signaling pathways. Diabetes Metab Syndr. 14(5):1307–1314.
   PubMed Web of Science ®Google Scholar
• Calamita G, Mazzone A, Bizzoca A, Svelto M. 2001. Possible involvement of aquaporin-7 and -8 in rat testis development and spermatogenesis. Biochem Biophys Res Commun. 288(3):619–625.
   PubMed Web of Science ®Google Scholar
• Carbrey JM, Gorelick-Feldman DA, Kozono D, Praetorius J, Nielsen S, Agre P. 2003. Aquaglyceroporin AQP9: solute permeation and metabolic control of expression in liver. Proc Natl Acad Sci USA. 100(5):2945–2950.
   PubMed Web of Science ®Google Scholar
• Chauvigne F, Boj M, Finn RN, Cerda J. 2015. Mitochondrial aquaporin-8-mediated hydrogen peroxide transport is essential for teleost spermatozoon motility. Sci Rep. 5:7789.
   PubMed Web of Science ®Google Scholar
• Clarke-Bland CE, Bill RM, Devitt A. 2022. Emerging roles for AQP in mammalian extracellular vesicles. Biochim Biophys Acta Biomembr. 1864(3):183826.
   PubMedGoogle Scholar
• Condorelli RA, La Vignera S, Mongioi LM, Alamo A, Calogero AE. 2018. Diabetes mellitus and infertility: different pathophysiological effects in type 1 and type 2 on sperm function. Front Endocrinol (Lausanne). 9:268.
   PubMed Web of Science ®Google Scholar
• da Silva IV, Soveral G. 2017. Aquaporins in obesity. Adv Exp Med Biol. 969:227–238.
   PubMed Web of Science ®Google Scholar
• Dajani S, Saripalli A, Sharma-Walia N. 2018. Water transport proteins-aquaporins (AQPs) in cancer biology. Oncotarget. 9(91):36392–36405.
   PubMedGoogle Scholar
• Devasagayam TP, Tarachand U. 1987. Decreased lipid peroxidation in the rat kidney during gestation. Biochem Biophys Res Commun. 145(1):134–138.
   PubMed Web of Science ®Google Scholar
• Dludla PV, Joubert E, Muller CJF, Louw J, Johnson R. 2017. Hyperglycemia-induced oxidative stress and heart disease-cardioprotective effects of rooibos flavonoids and phenylpyruvic acid-2-O-β-D-glucoside. Nutr Metab (Lond). 14:45.
   PubMed Web of Science ®Google Scholar
• Faisal Lutfi M, Abdel-Moneim AH, Alsharidah AS, Mobark MA, Abdellatif AAH, Saleem IY, Al Rugaie O, Mohany KM, Alsharidah M. 2021. Thymoquinone lowers blood glucose and reduces oxidative stress in a rat model of diabetes. Molecules. 26(8):2348.
   PubMed Web of Science ®Google Scholar
• Galli M, Hameed A, Żbikowski A, Zabielski P. 2021. Aquaporins in insulin resistance and diabetes: more than channels! Redox Biol. 44:102027.
   PubMed Web of Science ®Google Scholar
• Guo Y, Zhang C, Wang C, Huang Y, Liu J, Chu H, Ren X, Kong L, Ma H. 2021. Thioredoxin-1 is a target to attenuate alzheimer-like pathology in diabetic encephalopathy by alleviating endoplasmic reticulum stress and oxidative stress. Front Physiol. 12:651105.
   PubMed Web of Science ®Google Scholar
• Guven H, Durmus N, Hocaoglu N, Guner O, Acar S, Akan P, Calan OG. 2021. Protective effects of wheat germ oil against erectile and endothelial dysfunction in streptozotocin-induced diabetic rats. Int J Impot Res.
   PubMed Web of Science ®Google Scholar
• Hattori Y, Kikuchi T, Ozaki KI, Onishi H. 2017. Evaluation of in vitro and in vivo therapeutic antitumor efficacy of transduction of polo-like kinase 1 and heat shock transcription factor 1 small interfering RNA. Exp Ther Med. 14(5):4300–4306.
   PubMed Web of Science ®Google Scholar
• Hogberg J, Larson RE, Kristoferson A, Orrenius S. 1974. NADPH-dependent reductase solubilized from microsomes by peroxidation and its activity. Biochem Biophys Res Commun. 56(3):836–842.
   PubMed Web of Science ®Google Scholar
• Hollborn M, Rehak M, Iandiev I, Pannicke T, Ulbricht E, Reichenbach A, Wiedemann P, Bringmann A, Kohen L. 2012. Transcriptional regulation of aquaporins in the ischemic rat retina: upregulation of aquaporin-9. Curr Eye Res. 37(6):524–531.
   PubMed Web of Science ®Google Scholar
• Hou J, Li Y, Ren X, Gao F, Chen Y, Yi Y, Kang L, Luo Y, Yang M. 2018. Similar aquaporin9 and mapk expression profiles in the liver of types 1 and 2 diabetes mellitus. Horm Metab Res. 50(5):414–421.
   PubMed Web of Science ®Google Scholar
• Hu B. 1974. Steroid dehydrogenase 3rd ed. New York: Academic Press. (Methods of Enzymatic Analysis).
   Google Scholar
• Huang HF, He RH, Sun CC, Zhang Y, Meng QX, Ma YY. 2006. Function of aquaporins in female and male reproductive systems. Hum Reprod Update. 12(6):785–795.
   PubMed Web of Science ®Google Scholar
• Ichiyama T, Nakatani E, Tatsumi K, Hideshima K, Urano T, Nariai Y, Sekine J. 2018. Expression of aquaporin 3 and 5 as a potential marker for distinguishing dry mouth from Sjögren’s syndrome. J Oral Sci. 60(2):212–220.
   PubMed Web of Science ®Google Scholar
• Jelen S, Wacker S, Aponte-Santamaría C, Skott M, Rojek A, Johanson U, Kjellbom P, Nielsen S, de Groot BL, Rützler M. 2011. Aquaporin-9 protein is the primary route of hepatocyte glycerol uptake for glycerol gluconeogenesis in mice. J Biol Chem. 286(52):44319–44325.
   PubMed Web of Science ®Google Scholar
• Kassab A, Piwowar A. 2012. Cell oxidant stress delivery and cell dysfunction onset in type 2 diabetes. Biochimie. 94(9):1837–1848.
   PubMed Web of Science ®Google Scholar
• Khalil ASM, Giribabu N, Yelumalai S, Shahzad H, Kilari EK, Salleh N. 2021. Myristic acid defends against testicular oxidative stress, inflammation, apoptosis: restoration of spermatogenesis, steroidogenesis in diabetic rats. Life Sci. 278:119605.
   PubMed Web of Science ®Google Scholar
• Khalil H. 2017. Diabetes microvascular complications-A clinical update. Diabetes Metab Syndr. 11 Suppl 1(Suppl 1):S133–S139.
   PubMedGoogle Scholar
• Lee HY, Gu M, Cheng J, Suh JW, Chae HJ. 2020. Ixeris dentata and Lactobacillus gasseri extracts improve salivary secretion capability in diabetes-associated dry mouth rat model. Nutrients. 12(5):1331.
   Web of Science ®Google Scholar
• Lei X, Huo P, Wang Y, Xie Y, Shi Q, Tu H, Yao J, Mo Z, Zhang S. 2020. Lycium barbarum polysaccharides improve testicular spermatogenic function in streptozotocin-induced diabetic rats. Front Endocrinol (Lausanne). 11:164.
   PubMed Web of Science ®Google Scholar
• Li Y, Zhou Y, Wu J, Li J, Yao H. 2021. Phelligridin D from Inonotus obliquus attenuates oxidative stress and accumulation of ECM in mesangial cells under high glucose via activating Nrf2. J Nat Med. 75(4):1021–1029.
   PubMed Web of Science ®Google Scholar
• Liu L, Kelly MG, Wierzbicki EL, Escober-Nario IC, Vollmer MK, Dore S. 2019. Nrf2 plays an essential role in long-term brain damage and neuroprotection of Korean Red Ginseng in a permanent cerebral ischemia model. Antioxidants (Basel). 8(8):273.
   Google Scholar
• Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. 1951. Protein measurement with the Folin phenol reagent. J Biol Chem. 193(1):265–275.
   PubMed Web of Science ®Google Scholar
• Malekiyan R, Abdanipour A, Sohrabi D, Jafari Anarkooli I. 2019. Antioxidant and neuroprotective effects of lycopene and insulin in the hippocampus of streptozotocin-induced diabetic rats. Biomed Rep. 10(1):47–54.
   PubMed Web of Science ®Google Scholar
• Maresch CC, Stute DC, Alves MG, Oliveira PF, de Kretser DM, Linn T. 2018. Diabetes-induced hyperglycemia impairs male reproductive function: a systematic review. Hum Reprod Update. 24(1):86–105.
   PubMed Web of Science ®Google Scholar
• Maresch CC, Stute DC, Ludlow H, Hammes HP, de Kretser DM, Hedger MP, Linn T. 2017. Hyperglycemia is associated with reduced testicular function and activin dysregulation in the Ins2Akita+/− mouse model of type 1 diabetes. Mol Cell Endocrinol. 446:91–101.
   PubMed Web of Science ®Google Scholar
• Marklund S, Marklund G. 1974. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem. 47(3):469–474.
   PubMedGoogle Scholar
• Mathur A, Pandey VK, Khan MF, Kakkar P. 2021. PHLPP1/Nrf2-Mdm2 axis induces renal apoptosis via influencing nucleo-cytoplasmic shuttling of FoxO1 during diabetic nephropathy. Mol Cell Biochem. 476(10):3681–3699.
   PubMed Web of Science ®Google Scholar
• Meli R, Pirozzi C, Pelagalli A. 2018. New perspectives on the potential role of aquaporins (AQPs) in the physiology of inflammation. Front Physiol. 9:101.
   PubMed Web of Science ®Google Scholar
• Milkovic LC, Gasparovic A. 2021. AQP3 and AQP5-potential regulators of redox status in breast cancer. Molecules. 26(9):2613.
   PubMed Web of Science ®Google Scholar
• Mirabella N, Pelagalli A, Liguori G, Rashedul MA, Squillacioti C. 2021. Differential abundances of AQP3 and AQP5 in reproductive tissues from dogs with and without cryptorchidism. Anim Reprod Sci. 228:106735.
   PubMed Web of Science ®Google Scholar
• Mori S, Kurimoto T, Miki A, Maeda H, Kusuhara S, Nakamura M. 2020. Aqp9 gene deletion enhances retinal ganglion cell (RGC) death and dysfunction induced by optic nerve crush: evidence that aquaporin 9 acts as an astrocyte-to-neuron lactate shuttle in concert with monocarboxylate transporters to support RGC function and survival. Mol Neurobiol. 57(11):4530–4548.
   PubMed Web of Science ®Google Scholar
• Nagarathna R, Bali P, Anand A, Srivastava V, Patil S, Sharma G, Manasa K, Pannu V, Singh A, Nagendra HR. 2020. Prevalence of diabetes and its determinants in the young adults Indian population-call for yoga intervention. Front Endocrinol (Lausanne). 11:507064.
   PubMed Web of Science ®Google Scholar
• Nasiri K, Akbari A, Nimrouzi M, Ruyvaran M, Mohamadian A. 2021. Safflower seed oil improves steroidogenesis and spermatogenesis in rats with type II diabetes mellitus by modulating the genes expression involved in steroidogenesis, inflammation and oxidative stress. J Ethnopharmacol. 275:114139.
   PubMed Web of Science ®Google Scholar
• Newsholme P, Keane KN, Carlessi R, Cruzat V. 2019. Oxidative stress pathways in pancreatic β-cells and insulin-sensitive cells and tissues: importance to cell metabolism, function, and dysfunction. Am J Physiol Cell Physiol. 317(3):C420–C433.
   PubMed Web of Science ®Google Scholar
• Nna VU, Bakar ABA, Ahmad A, Mohamed M. 2019. Down-regulation of steroidogenesis-related genes and its accompanying fertility decline in streptozotocin-induced diabetic male rats: ameliorative effect of metformin. Andrology. 7(1):110–123.
   PubMed Web of Science ®Google Scholar
• Nna VU, Ujah GA, Suleiman JB, Mohamed M, Nwokocha C, Akpan TJ, Ekuma HC, Fubara VV, Kekung-Asu CB, Osim EE. 2020. Tert-butylhydroquinone preserve testicular steroidogenesis and spermatogenesis in cisplatin-intoxicated rats by targeting oxidative stress, inflammation and apoptosis. Toxicology. 441:152528.
   PubMed Web of Science ®Google Scholar
• Oliveira CA, Carnes K, Franca LR, Hermo L, Hess RA. 2005. Aquaporin-1 and -9 are differentially regulated by oestrogen in the efferent ductule epithelium and initial segment of the epididymis. Biol Cell. 97(6):385–395.
   PubMed Web of Science ®Google Scholar
• Pan C, Zhou S, Wu J, Liu L, Song Y, Li T, Ha L, Liu X, Wang F, Tian J, et al. 2017. NRF2 plays a critical role in both self and EGCG protection against diabetic testicular damage. Oxid Med Cell Longev. 2017:3172692.
   PubMed Web of Science ®Google Scholar
• Papatheodorou K, Papanas N, Banach M, Papazoglou D, Edmonds M. 2016. Complications of Diabetes 2016. J Diabetes Res. 2016:6989453.
   PubMed Web of Science ®Google Scholar
• Pellavio G, Laforenza U. 2021. Human sperm functioning is related to the aquaporin-mediated water and hydrogen peroxide transport regulation. Biochimie. 188:45–51.
   PubMed Web of Science ®Google Scholar
• Pitteloud N, Hardin M, Dwyer AA, Valassi E, Yialamas M, Elahi D, Hayes FJ. 2005. Increasing insulin resistance is associated with a decrease in Leydig cell testosterone secretion in men. J Clin Endocrinol Metab. 90(5):2636–2641.
   PubMed Web of Science ®Google Scholar
• Qinna NA, Badwan AA. 2015. Impact of streptozotocin on altering normal glucose homeostasis during insulin testing in diabetic rats compared to normoglycemic rats. Drug Des Devel Ther. 9:2515–2525.
   PubMed Web of Science ®Google Scholar
• Rahimi G, Heydari S, Rahimi B, Abedpoor N, Niktab I, Safaeinejad Z, Peymani M, Seyed Forootan F, Derakhshan Z, Esfahani MHN, et al. 2021. A combination of herbal compound (SPTC) along with exercise or metformin more efficiently alleviated diabetic complications through down-regulation of stress oxidative pathway upon activating Nrf2-Keap1 axis in AGE rich diet-induced type 2 diabetic mice. Nutr Metab (Lond). 18(1):14.
   PubMed Web of Science ®Google Scholar
• Rato L, Alves MG, Dias TR, Lopes G, Cavaco JE, Socorro S, Oliveira PF. 2013. High-energy diets may induce a pre-diabetic state altering testicular glycolytic metabolic profile and male reproductive parameters. Andrology. 1(3):495–504.
   PubMed Web of Science ®Google Scholar
• Rehman K, Akash MSH. 2017. Mechanism of generation of oxidative stress and pathophysiology of type 2 diabetes mellitus: how are they interlinked? J Cell Biochem. 118(11):3577–3585.
   PubMed Web of Science ®Google Scholar
• Ribeiro JC, Alves MG, Yeste M, Cho YS, Calamita G, Oliveira PF. 2021. Aquaporins and (in)fertility: more than just water transport. Biochim Biophys Acta Mol Basis Dis. 1867(3):166039.
   PubMed Web of Science ®Google Scholar
• Rojek AM, Skowronski MT, Fuchtbauer EM, Fuchtbauer AC, Fenton RA, Agre P, Frokiaer J, Nielsen S. 2007. Defective glycerol metabolism in aquaporin 9 (AQP9) knockout mice. Proc Natl Acad Sci USA. 104(9):3609–3614.
   PubMed Web of Science ®Google Scholar
• Sadasivam M, Ramatchandirin B, Balakrishnan S, Prahalathan C. 2015. TNF-α-mediated suppression of Leydig cell steroidogenesis involves DAX-1. Inflamm Res. 64(7):549–556.
   PubMed Web of Science ®Google Scholar
• Saeedi P, Petersohn I, Salpea P, Malanda B, Karuranga S, Unwin N, Colagiuri S, Guariguata L, Motala AA, Ogurtsova K, et al. 2019. Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: results from the International Diabetes Federation Diabetes Atlas, 9th edition. Diabetes Res Clin Pract. 157:107843.
   PubMed Web of Science ®Google Scholar
• Schnabel B, Kuhrt H, Wiedemann P, Bringmann A, Hollborn M. 2020. Osmotic regulation of aquaporin-8 expression in retinal pigment epithelial cells in vitro: dependence on KATP channel activation. Mol Vis. 26:797–817.
   PubMed Web of Science ®Google Scholar
• Shannonhouse JL, Urbanski HF, Woo SL, Fong LA, Goddard SD, Lucas WF, Jones ER, Wu C, Morgan C. 2014. Aquaporin-11 control of testicular fertility markers in Syrian hamsters. Mol Cell Endocrinol. 391(1–2):1–9.
   PubMed Web of Science ®Google Scholar
• Shivanandappa T, Venkatesh S. 1997. A colorimetric assay method for 3beta-hydroxy-delta5-steroid dehydrogenase. Anal Biochem. 254(1):57–61.
   PubMed Web of Science ®Google Scholar
• Shoorei H, Khaki A, Khaki AA, Hemmati AA, Moghimian M, Shokoohi M. 2019. The ameliorative effect of carvacrol on oxidative stress and germ cell apoptosis in testicular tissue of adult diabetic rats. Biomed Pharmacother. 111:568–578.
   PubMed Web of Science ®Google Scholar
• Sies H. 2014. Role of metabolic H2O2 generation: redox signaling and oxidative stress. J Biol Chem. 289(13):8735–8741.
   PubMed Web of Science ®Google Scholar
• Singh R, Bhardwaj P, Sharma P. 2013. Antioxidant and toxicological evaluation of Cassia sopherain streptozotocin-induced diabetic Wistar rats. Pharmacognosy Res. 5(4):225–232.
   PubMedGoogle Scholar
• Sinha AK. 1972. Colorimetric assay of catalase. Anal Biochem. 47(2):389–394.
   PubMed Web of Science ®Google Scholar
• Song J, Gao X, Tang Z, Li H, Ruan Y, Liu Z, Wang T, Wang S, Liu J, Jiang H. 2020. Protective effect of Berberine on reproductive function and spermatogenesis in diabetic rats via inhibition of ROS/JAK2/NFκB pathway. Andrology. 8(3):793–806.
   PubMed Web of Science ®Google Scholar
• Spegel P, Chawade A, Nielsen S, Kjellbom P, Rutzler M. 2015. Deletion of glycerol channel aquaporin-9 (Aqp9) impairs long-term blood glucose control in C57BL/6 leptin receptor-deficient (db/db) obese mice. Physiol Rep. 3(9):e12538.
   PubMedGoogle Scholar
• Squillacioti C, Mirabella N, Liguori G, Germano G, Pelagalli A. 2021. Aquaporins are differentially regulated in canine cryptorchid efferent ductules and epididymis. Animals (Basel). 11(6):1539.
   PubMedGoogle Scholar
• Su W, Cao R, Zhang XY, Guan Y. 2020. Aquaporins in the kidney: physiology and pathophysiology. Am J Physiol Renal Physiol. 318(1):F193–F203.
   PubMed Web of Science ®Google Scholar
• Varadaraj K, Kumari SS. 2020. Lens aquaporins function as peroxiporins to facilitate membrane transport of hydrogen peroxide. Biochem Biophys Res Commun. 524(4):1025–1029.
   PubMed Web of Science ®Google Scholar
• Wang J, Feng L, Zhu Z, Zheng M, Wang D, Chen Z, Sun H. 2015. Aquaporins as diagnostic and therapeutic targets in cancer: how far we are? J Transl Med. 13:96.
   PubMed Web of Science ®Google Scholar
• Wang Y, Chen D, Liu Y, Zhang Y, Duan C, Otkur W, Chen H, Liu X, Xia T, Qi H, et al. 2021. AQP3-mediated H2 O2 uptake inhibits LUAD autophagy by inactivating PTEN. Cancer Sci. 112(8):3278–3292.
   PubMed Web of Science ®Google Scholar
• Wang-Fischer Y, Garyantes T. 2018. Improving the reliability and utility of streptozotocin-induced rat diabetic model. J Diabetes Res. 2018:8054073.
   PubMed Web of Science ®Google Scholar
• Wolpin BM, Bao Y, Qian ZR, Wu C, Kraft P, Ogino S, Stampfer MJ, Sato K, Ma J, Buring JE, et al. 2013. Hyperglycemia, insulin resistance, impaired pancreatic beta-cell function, and risk of pancreatic cancer. J Natl Cancer Inst. 105(14):1027–1035.
   PubMedGoogle Scholar
• Yu B, Huang Z. 2015. Variations in antioxidant genes and male infertility. Biomed Res Int. 2015:513196.
   PubMed Web of Science ®Google Scholar
• Yusupov M, Razzokov J, Cordeiro RM, Bogaerts A. 2019. Transport of reactive oxygen and nitrogen species across aquaporin: a molecular level picture. Oxid Med Cell Longev. 2019:2930504.
   PubMed Web of Science ®Google Scholar
• Zhang B, Zhang CY, Zhang XL, Sun GB, Sun XB. 2021. Guan Xin Dan Shen formulation protects db/db mice against diabetic cardiomyopathy via activation of Nrf2 signaling. Mol Med Rep. 24(1):531.
   PubMed Web of Science ®Google Scholar
• Zhang HB, Tu XK, Song SW, Liang RS, Shi SS. 2020. Baicalin reduces early brain injury after subarachnoid hemorrhage in rats. Chin J Integr Med. 26(7):510–518.
   PubMed Web of Science ®Google Scholar
• Zhao Y, Kong C, Chen X, Wang Z, Wan Z, Jia L, Liu Q, Wang Y, Li W, Cui J, et al. 2016. Repetitive exposure to low-dose X-irradiation attenuates testicular apoptosis in type 2 diabetic rats, likely via Akt-mediated Nrf2 activation. Mol Cell Endocrinol. 422:203–210.
   PubMed Web of Science ®Google Scholar