Sertoli cells are the target of environmental toxicants in the testis – a mechanistic and therapeutic insight

Bibliography

• Kilchevsky A, Honig S. Male factor infertility in 2011: semen quality, sperm selection and hematospermia. Nat Rev Urol 2012;9:68-70
   PubMed Web of Science ®Google Scholar
• Carlsen E, Giwercman A, Keiding N, et al. Evidence for decresing quality of semen during past 50 years. BMJ 1992;6854:609-13
   Google Scholar
• Geoffroy-Siraudin C. Loundou Ad, Romain F, et al. Decline of semen quality among 10932 males consulting for couple infertility over a 20-year period in Marseille, France. Asian J Androl 2012;14:584-90
   PubMed Web of Science ®Google Scholar
• Jorgensen N, Vierula M, Jacobsen R, et al. Recent adverse trends in semen quality and testis cancer incidence among Finnish men. Int J Androl 2011;34:e37-48
   Google Scholar
• Saidi JA, Chang DT, Goluboff ET, et al. Declining sperm counts in the United States? A critical review. J Urol 1999;161:460-2
   PubMed Web of Science ®Google Scholar
• Jorgensen N, Andersen AG, Eustache F, et al. Regional differences in semen quality in Europe. Hum Reprod 2001;16:1012-19
   PubMed Web of Science ®Google Scholar
• Nordkap L, Joensen UN, Blomberg JM, et al. Regional differences and temporal trends in male reproductive health disorders: semen quality may be a sensitive marker of environmental exposures. Mol Cell Endocrinol 2012;355:221-30
   PubMed Web of Science ®Google Scholar
• Mehrpour O, Karrari P, Zamani N, et al. Occupational expxosure to pesticides and consequences on male semen and ferility: a review. Toxicol Lett 2014;230:146-56
   PubMed Web of Science ®Google Scholar
• Kovac JR, Pastuszak AW, Lamb DJ. The use of genomics, proteomics and metabolomics in identifying biomarkers of male infertility. Fertil Sertil 2013;99:998-1007
   PubMed Web of Science ®Google Scholar
• Luevano J, Damodaran C. A review of molecular events of cadmium-ineduced carcinogenesis. J Environ pathol Toxicol Oncol 2014;33:183-94
   PubMed Web of Science ®Google Scholar
• Feki-Tounsi M, Hamza-Chaffai A. Cadmium as a possible cause of bladder cancer: a review of accumulated evidence. Environ Sci Pollut Res Int 2014;21:10561-73
   Google Scholar
• Chang ET, Adami HO, Boffetta P, et al. A critical review of perfluorooctanoate and perfluorooctanesulfonate exposure and cancer risk in humans. Crit Rev Toxicol 2014;44(Suppl 1):1-81
   PubMedGoogle Scholar
• Wong EWP, Cheng CY. Impacts of environmental toxicants on male reproductive dysfunction. Trends Pharmacol Sci 2011;32:290-9
   PubMed Web of Science ®Google Scholar
• Aitken RJ, Smith TB, Jobling MS, et al. Oxidative stress and male reproductive health. Asian J Androl 2014;16:31-8
   PubMed Web of Science ®Google Scholar
• Boekelheide K, Fleming SL, Allio T, et al. 2,5-Hexanedione-induced testicular injury. Annu Rev Pharmacol Toxciol 2003;43:125-47
   PubMed Web of Science ®Google Scholar
• Johnson KJ. Testicular histopathology associated with disruption of the Sertoli cell cytoskeleton. Spermatogenesis 2014;4:e979106
   PubMedGoogle Scholar
• Xiao X, Mruk DD, Tang EI, et al. Environmental toxicants perturb human Serotli cell adhesive function via changes in F-actin organization medicated by actin regulatory proteins. Hum Reprod 2014;29:1279-91
   Google Scholar
• Cheng CY, Wong EWP, Lie PPY, et al. Environmental toxicants and male reproductive function. Spermatogenesis 2011;1:2-13
   PubMedGoogle Scholar
• Wan HT, Mruk DD, Wong CKC, et al. Targeting testis-specific proteins to inhibit spermatogenesis - lession from endocrine disrupting chemicals. Expert Opin Ther Targets 2013;17:839-55
   PubMed Web of Science ®Google Scholar
• Wong EWP, Yan HHN, Li MWM, et al. Cell junctions in the testis as targets for toxicants. In: . editor. series editor Comprehensive toxicology. 2nd edition. Volume 11 Reproductive and Endocrine Toxicology. McQueen CAHoyer PB, Richburg JH, editor. Academic Press, Elseiver; Oxford: 2010. p. 167-88
   Google Scholar
• Byers S, Hadley MA, Djakiew D, et al. Growth and characterization of epididymal epithelial cells and Sertoli cells in dual environment culture chambers. J Androl 1986;7:59-68
   PubMed Web of Science ®Google Scholar
• Janecki A, Jakubowiak A, Steinberger A. Regulation of transepithelial electrical resistance in two-compartment Sertoli cell cultures: in vitro model of the blood-testis barrier. Endocrinology 1991;129:1489-96
   Google Scholar
• Cheng CY, Mruk DD. The blood-testis barrier and its implication in male contraception. Pharmacol Rev 2012;64:16-64
   PubMed Web of Science ®Google Scholar
• Mruk DD, Cheng CY. An in vitro system to study Sertoli cell blood-testis barrier dynamics. Methods Mol Biol 2011;763:237-52
   Google Scholar
• Wright W, Zabludoff S, Erickson-Lawrence M, et al. Germ cell-Sertoli cell interactions. Studies of cyclic protein-2 in the seminiferous tubule. Ann N Y Acad Sci 1989;564:173-85
   Google Scholar
• Johnson KJ, Heger NE, Boekelheide K. Of mice and men (and rats): phthalate-induced fetal testis endocrine disruption is species-dependent. Toxicol Sci 2012;129:235-48
   PubMed Web of Science ®Google Scholar
• Moroi S, Saitou M, Fujimoto K, et al. Occludin is concentrated at tight junctions of mouse/rat but not human/guinea pig Sertoli cells in testes. Am J Physiol Cell Physiol 1998;274:C1708-17
   PubMed Web of Science ®Google Scholar
• Kaitu’u-Lino TJ, Sluka P, Foo CF, et al. Claudin-11 expression and localisation is regulated by androgens in rat Sertoli cells in vitro. Reproduction 2007;133:1169-79
   Google Scholar
• Ahmed EA, Barten-van Rijbroek AD, Kal HB, et al. Proliferative activity in vitro and DNA repair indicate that adult mouse and human Sertoli cells are not terminally differentiated, quiescent cells. Biol Reprod 2009;80:1084-91
   Google Scholar
• Chui K, Trivedi A, Cheng CY, et al. Characterization and functionality of proliferative human Sertoli cells. Cell Transplant 2011;20:619-35
   PubMed Web of Science ®Google Scholar
• Hunt PA, Susiarjo M, Rubio C, et al. The bisphenol A experience: A primer for the analysis of environmental effects on mammalian reproduction. Biol Reprod 2009;81:807-13
   PubMed Web of Science ®Google Scholar
• Chapin RE, Adams J, Boekelheide K, et al. NTP-CERHR expert panel report on the reproductive and developmental toxicity of bisphenol A. Birth Defects Res B Dev Reprod Toxicol 2008;83:157-395
   PubMed Web of Science ®Google Scholar
• Hoekstra EJ, Simoneau C. Release of bisphenol A from polycarbonate: a review. Crit Rev Food Sci Nutr 2013;53:386-402
   PubMed Web of Science ®Google Scholar
• Vandenberg LN, Maffini MV, Sonnenschein C, et al. Bisphenol-A and the great divide: A review of controversies in the field of endocrine disruption. Endocr Rev 2009;30:75-95
   PubMed Web of Science ®Google Scholar
• Gao Y, Lee WM, Cheng CY. Thyroid hormone function in the rat testis. Front Endocrinol 2014;5:188
   Google Scholar
• Nakhla AM, Mather JP, Janne OA, et al. Estrogen and androgen receptors in Sertoli, Leydig, myoid, and epithelial cells: effects of time in culture and cell density. Endocrinology 1984;115:121-8
   PubMed Web of Science ®Google Scholar
• Li MWM, Mruk DD, Lee WM, et al. Disruption of the blood-testis barrier integrity by bisphenol A in vitro: Is this a suitable model for studying blood-testis barrier dynamics? Int J Biochem Cell Biol 2009;41:2302-14
   PubMed Web of Science ®Google Scholar
• Salian S, Doshi T, Vanage G. Neonatal exposure of male rats to bisphenol A impairs fertility and expression of Sertoli cell junctional proteins in the testis. Toxicology 2009;265:56-67
   PubMed Web of Science ®Google Scholar
• Hengstler JG, Foth H, Gebel T, et al. Critical evaluation of key evidence on the human health hazards of exposure to bisphenol A. Crit Rev Toxicol 2011;41:263-91
   PubMed Web of Science ®Google Scholar
• Dobrzynska MM, Jankowska-Steifer EA, Tyrkiel EJ, et al. Comparison of the effecfts of bisphenol A alone and in a combination with X-irradiation on sperm count and quality in male adult and pubescent mice. Environ Toxicol 2014;29:1301-13
   PubMed Web of Science ®Google Scholar
• Thuillier R, Manku G, Wang Y, et al. Changes in MAPK pathway in neonatal and adult testis following fetal estrogen exposure and effects on rat testicular cells. Microsc Res Tech 2009;72:773-86
   PubMed Web of Science ®Google Scholar
• Li MWM, Mruk DD, Lee WM, et al. Connexin 43 is critical to maintain the homeostasis of blood-testis barrier via its effects on tight junction reassembly. Proc Natl Acad Sci USA 2010;107:17998-8003
   PubMed Web of Science ®Google Scholar
• Izumi Y, Yamaguchi K, Ishikawa T, et al. Molecular changes induced by bisphenol-A in rat Sertoli cell culture. Syst Biol Reprod Med 2011;57:228-32
   PubMed Web of Science ®Google Scholar
• Li MWM, Mruk DD, Cheng CY. Gap junctions and blood-tissue barriers. Adv Exp Med Biol 2012;763:260-80
   PubMed Web of Science ®Google Scholar
• Pointis G, Gilleron J, Carette D, et al. Testicular connexin 43, a precocious molecular target for the effect of environmental toxicants on male fertility. Spermatogenesis 2011;1:303-17
   PubMedGoogle Scholar
• Solan JL, Lampe PD. Specific Cx43 phosphorylation events regulate gap junciton turnoer in vivo. FEBS Lett 2014;588:1423-9
   Google Scholar
• Dunn CA, Lampe PD. Injury-triggered Akt phosphorylation of Cx43: a ZO-1-driven molecular switch that regulates gap junction size. J Cell Sci 2014;127:455-64
   Google Scholar
• Yogo K, Ogawa T, Akiyama M, et al. Identification and functional analysis of novel phosphorylation sites in Cx43 in rat primary granulosa cells. FEBS Lett 2002;531:132-6
   Google Scholar
• Lampe PD, TenBroek EM, Burt JM, et al. Phosphorylation of connexin43 on serine368 by protein kinase C regulates gap junctional communications. J Cell Biol 2000;149:1503-12
   PubMed Web of Science ®Google Scholar
• Li MWM, Mruk DD, Lee WM, et al. Connexin 43 and plakophilin-2 as a protein complex that regulates blood-testis barrier dynamics. Proc Natl Acad Sci USA 2009;106:10213-18
   PubMed Web of Science ®Google Scholar
• Iida H, Maehara K, Doiguchi M, et al. Bisphenol A-induced apoptosis of cultured rat Sertoli cells. Reprod Toxicol 2003;17:457-64
   Google Scholar
• Qi S, Fu W, Wang C, et al. BPA-induced apoptosis of rat Sertoli cells through Fas/FasL and JNKs/p38 MAPK pathways. Reprod Toxicol 2014;50:108-16
   PubMed Web of Science ®Google Scholar
• Wang C, Fu W, Quan C, et al. The role of Pten/Akt signaling pathway involved in BPA-induced apoptosis of rat sertoli cells. Environ Toxicol 2014; doi:10.1002/tox.21958
   Google Scholar
• Qian W, Zhu J, Mao C, et al. Involvement of CaM-CaMKII-ERK in bisphenol A-induced Sertoli cell apoptosis. Toxicology 2014;324:27-34
   Google Scholar
• Urriola-Munoz P, Lagos-pCabre R, Moreno RD. A mechanism of male germ cell apoptosis induced by bisphenol-A and nonylphenol involving ADAM17 and p38 MAPK activation. PLoS ONE 2014;9:e113793
   Web of Science ®Google Scholar
• Lie PPY, Mruk DD, Mok KW, et al. Focal adhesion kinase-Tyr407 and -Tyr397 exhibit antagonistic effects on blood-testis barrier dynamics in the rat. Proc Natl Acad Sci USA 2012;109:12562-7
   PubMed Web of Science ®Google Scholar
• Siu ER, Mruk DD, Porto CS, et al. Cadmium-induced testicular injury. Toxicol Appl Pharmacol 2009;238:240-9
   PubMed Web of Science ®Google Scholar
• Thompson J, Bannigan J. Cadmium: toxic effects on the reproductive system and the embryo. Reprod Toxicol 2008;25:304-15
   PubMed Web of Science ®Google Scholar
• Parizek J, Zahor Z. Effect of cadmium salts on testicular tissue. Nature 1956;177:1036-7
   PubMed Web of Science ®Google Scholar
• Wong CH, Mruk DD, Siu MKY, et al. Blood-testis barrier dynamics are regulated by alpha2-macroglobulin via the c-Jun N-terminal protein kinase pathway. Endocrinology 2005;146:1893-908
   PubMed Web of Science ®Google Scholar
• Hew KW, Heath GL, Jiwa AH, et al. Cadmium in vivo causes disruption of tight junction-associated microfilaments in rat Sertoli cells. Biol Reprod 1993;49:840-9
   PubMed Web of Science ®Google Scholar
• Lui WY, Lee WM, Cheng CY. Transforming growth factor-beta3 regulates the dynamics of Sertoli cell tight junctions via the p38 mitogen-activated protein kinase pathway. Biol Reprod 2003;68:1597-612
   PubMed Web of Science ®Google Scholar
• Lui WY, Wong CH, Mruk DD, et al. TGF-beta3 regulates the blood-testis barrier dynamics via the p38 mitogen activated protein (MAP) kinase pathway: an in vivo study. Endocrinology 2003;144:1139-42
   PubMed Web of Science ®Google Scholar
• Wong CH, Mruk DD, Lui WY, et al. Regulation of blood-testis barrier dynamics: an in vivo study. J Cell Sci 2004;117:783-98
   PubMed Web of Science ®Google Scholar
• Yu X, Hong S, Faustman EM. Cadmium-induced activation of stress signaling pathways, disruption of ubiquitin-dependent protein degradation and apoptosis in primary rat Sertoli cell-gonocyte cocultures. Toxicol Sci 2008;104:385-96
   PubMed Web of Science ®Google Scholar
• Wan HT, Mruk DD, Tang EI, et al. Role of non-receptor protein tyrosine kinases in spermatid transport during spermatogenesis. Semin Cell Dev Biol 2014;30:65-74
   Google Scholar
• Siu ER, Wong EWP, Mruk DD, et al. Focal adhesion kinase is a blood-testis barrier regulator. Proc Natl Acad Sci USA 2009;106:9298-303
   PubMed Web of Science ®Google Scholar
• Siu ER, Wong EWP, Mruk DD, et al. An occludin-focal adhesion kinase protein complex at the blood-testis barrier: a study using the cadmium model. Endocrinology 2009;150:3336-44
   PubMed Web of Science ®Google Scholar
• Renner R. Growing concern over perfluorinated chemicals. Environ Sci Technol 2001;35:154A-60A
   PubMed Web of Science ®Google Scholar
• D’Hollander W, de Voogt P, De Coen W, et al. Perfluorinated substances in human food and other sources of human exposure. Rev Environ Contam Toxicol 2010;208:179-215
   PubMed Web of Science ®Google Scholar
• Olsen GW, Burris JM, Ehresman DJ, et al. Half-life of serum elimination of perfluorooctanesulfonate, perfluorohexanesulfonate, and perfluorooctanoate in retired fluorochemical production workers. Environ Health Perspect 2007;115:1298-305
   PubMed Web of Science ®Google Scholar
• Perez F, Nadal M, Navarro-Ortega A, et al. Accumulation of perfluoroalkyl substances in human tissues. Environ Int 2013;59:354-62
   PubMed Web of Science ®Google Scholar
• Lau C, Anitole K, Hodes C, et al. Perfluoroalkyl acids: a review of monitoring and toxicological findings. Toxicol Sci 2007;99:366-94
   PubMed Web of Science ®Google Scholar
• Joensen UN, Bossi R, Leffers H, et al. Do perfluoroalkyl compounds impair human semen quality? Environ Health Perspect 2009;117:923-7
   PubMed Web of Science ®Google Scholar
• La Rocca C, Alessi E, Bergamasco B, et al. Exposure and effective dose biomarkers for perfluorooctane sulfonic acid (PFOS) and perfluorooctanoic acid (PFOA) in infertile subjects: preliminary results of the PREVIENI project. Int J Hyg Environ Health 2012;215:206-11
   PubMed Web of Science ®Google Scholar
• Wan HT, Mruk DD, Wong CKC, et al. Perfluorooctanesulfonate (PFOS) perturbs male rat Sertoli cell blood-testis barrier function by affecting F-actin organization via p-FAK-Tyr407 - an in vitro study. Endocrinology 2014;155:249-62
   PubMed Web of Science ®Google Scholar
• Zhang J, Liang J, Zhu H, et al. PFOS and PCB 153 have direct adverse effects on neonatal testis modeled using a coculture of primary gonocyte and Sertoli cells. Environ Toxicol 2013;28:322-31
   PubMed Web of Science ®Google Scholar
• Qiu L, Zhang X, Zhang X, et al. Sertoli cell is a potential target for perfluorooctane sulfonate-induced reproductive dysfunction in male mice. Toxicol Sci 2013;135:229-40
   PubMed Web of Science ®Google Scholar
• Aravindakshan J, Cyr DG. Nonylphenol alters connextin 43 levels and connexin 43 phosphorylation via an inhibition of the p38-mitogen-actived protein kinase pathway. Biol Reprod 2005;72:1232-40
   PubMed Web of Science ®Google Scholar
• Kaur G, Dufour JM. Cell lines. Valuable tools or useless artifacts. Spermatogenesis 2012;2:1-5
   PubMedGoogle Scholar
• Calalb MB, Polte TR, Hanks SK. Tyrosine phosphorylation of focal adhesion kinase at sites in the catalytic domain regulates kinase activity: a role for Src family kinases. Mol Cell Biol 1995;15:954-63
   PubMed Web of Science ®Google Scholar
• Schlaepfer DD, Hunter T. Evidence for in vivo phosphorylation of the Grb2 SH2-domain binding site on focal adhesion kinase by Src-family protein-tyrosine kinases. Mol Cell Biol 1996;16:5623-33
   PubMed Web of Science ®Google Scholar
• Mruk DD, Su L, Cheng CY. Emerging role for drug transporters at the blood-testis barrier. Trends Pharmacol Sci 2011;32:99-106
   Google Scholar
• Su L, Mruk DD, Cheng CY. Regulation of drug transporters in the testis by environmental toxicant cadmium, steroids and cytokines. Spermatogenesis 2012;2:285-93
   PubMedGoogle Scholar
• Cheng CY. Toxicants target cell junctions in the testis - insights from the indazole-carboxylic acid model. Spermatogenesis 2014;4(2):e981485
   PubMedGoogle Scholar
• Su L, Mruk DD, Lui WY, et al. P-glycoprotein regulates blood-testis barrier dynamics via its effects on the occludin/zonula occludens 1 (ZO-1) protein complex mediated by focal adhesion kinase (FAK). Proc Natl Acad Sci USA 2011;108:19623-8
   PubMedGoogle Scholar
• Su L, Mruk DD, Lee WM, et al. Drug transporters and blood-testis barrier function. J Endocrinol 2011;209:337-51
   Google Scholar
• Dalton TP, He L, Wang B, et al. Identification of mouse SLC39A8 as the transporter responsible for cadmium-induced toxicity in the testis. Proc Natl Acad Sci USA 2005;102:3401-6
   PubMed Web of Science ®Google Scholar
• Popovic M, Zaja R, Fent K, et al. Interaction of environmental contaminants with zebrafish organic anion transporting polypeptide, Oatp1d1 (Slco1d1). Toxicol Appl Pharmacol 2014;280:149-58
   Google Scholar
• Qian X, Mruk DD, Cheng YH, et al. Actin binding proteins, spermatid transport and spermiation. Semin Cell Dev Biol 2014;30:75-85
   PubMed Web of Science ®Google Scholar
• Tang EI, Mruk DD, Lee WM, et al. Cell-cell interactions, cell polarity, and the blood-testis barrier. In: Ebnet K, editor. Cell polarity. 1st Edition. Springer International Publishing; Geneva: 2015. p. 303-26
   Google Scholar
• Tang EI, Mruk DD, Cheng CY. MAP/microtubule affinity-regulating kinases, microtubule dynamics, and spermatogenesis. J Endocrinol 2013;217:R13-23
   Google Scholar
• Tang EI, Xiao X, Mruk DD, et al. Microtubule affinity-regulated kinase 4 (MARK4) is a component of the ectoplasmic specialization in the rat testis. Spermatogenesis 2012;2:117-26
   PubMedGoogle Scholar
• Wong EWP, Mruk DD, Lee WM, et al. Par3/Par6 polarity complex coordinates apical ectoplasmic specialization and blood-testis barrier restructuring during spermatogenesis. Proc Natl Acad Sci USA 2008;105:9657-62
   PubMed Web of Science ®Google Scholar
• Lie PPY, Chan AYN, Mruk DD, et al. Restricted Arp3 expression in the testis prevents blood-testis barrier disruption during junction restructuring at spermatogenesis. Proc Natl Acad Sci USA 2010;107:11411-16
   PubMed Web of Science ®Google Scholar
• Lie PPY, Mruk DD, Lee WM, et al. Epidermal growth factor receptor pathway substrate 8 (Eps8) is a novel regulator of cell adhesion and the blood-testis barrier integrity in the seminiferous epithelium. FASEB J 2009;23:2555-67
   PubMed Web of Science ®Google Scholar
• Qian X, Mruk DD, Wong EWP, et al. Palladin is a regulator of actin filament bundles at the ectoplasmic specialization in the rat testis. Endocrinology 2013;154:1907-20
   Google Scholar
• Gungor-Ordueri NE, Celik-Ozenci C, Cheng CY. Fascin 1 is an actin filament-bundling protein that regulates ectoplasmic specialization dynamics in the rat testis. Am J Physiol Endocrinol Metab 2014;307:E738-E53
   Google Scholar
• Cheng CY, Lie PPY, Wong EWP, et al. Adjudin disrupts spermatogenesis via the action of some unlikely partners: Eps8, Arp2/3 complex, drebrin E, PAR6 and 14-3-3. Spermatogenesis 2011;1:291-7
   PubMedGoogle Scholar
• Wan HT, Mruk DD, Li SYT, et al. p-FAK-Tyr397 regulates spermatid adhesion in the rat testis via its effects on F-actin organization at the ectoplasmic specialization. Am J Physiol Endocrinol Metab 2013;305:E687-E99
   PubMed Web of Science ®Google Scholar
• Siu MKY, Mruk DD, Lee WM, et al. Adhering junction dynamics in the testis are regulated by an interplay of beta1-integrin and focal adhesion complex (FAC)-associated proteins. Endocrinology 2003;144:2141-63
   PubMed Web of Science ®Google Scholar
• Beardsley A, Robertson DM, O’Donnell L. A complex containing alpha6beta1-integrin and phosphorylated focal adhesion kinase between Sertoli cells and elongated spermatids during spermatid release from the seminiferous epithelium. J Endocrinol 2006;190:759-70
   PubMed Web of Science ®Google Scholar
• Zhang J, Liang J, Zhu H, et al. PFOS and PCB 153 have direct adverse effects on neonatal testis modeled using a coculture of primary gonocyte and sertoli cells. Environ Toxicol 2013;28:322-31
   PubMed Web of Science ®Google Scholar
• Fiorini C, Tilloy-Ellul A, Chevalier S, et al. Sertoli cell junctional proteins as early targets for different classes of reproductive toxicants. Reprod Toxicol 2004;18:413-21
   PubMed Web of Science ®Google Scholar
• Yu X, Hong S, Faustman EM. Cadmium-induced activation of stress signaling pathways, disruption of ubiquitin-dependent protein degradation and apoptosis in primary rat Sertoli cell-gonocyte cocultures. Toxicol Sci 2008;385-96
   Google Scholar