Toxicants target cell junctions in the testis: Insights from the indazole-carboxylic acid model

References

• Wong EWP, Cheng, CY. Impacts of environmental toxicants on male reproductive dysfunction. Trends Pharmacol Sci 2011; 32:290-9; PMID:21324536; http://dx.doi.org/10.1016/j.tips.2011.01.001
   PubMed Web of Science ®Google Scholar
• Wong EWP, et al. Cell junctions in the testis as targets for toxicants. In: Comprehensive Toxicology. 2nd Edition (McQueen CA, Ed; Series Editor); Vol. 11 Reproductive and Endocrine Toxicology. Hoyer PB, Richburg JH. (Ed.); Oxford: Academic Press, Elseiver, 2010; pp. 167-88.
   Google Scholar
• Atchison WD. Effects of neurotoxicants on synaptic transmission: lessons learned from electrophysiological studies. Neurotoxicol Teratol 1988; 10:393-416; PMID:2854607; http://dx.doi.org/10.1016/0892-0362(88)90001-3
   PubMedGoogle Scholar
• Siu ER, Mruk DD, Porto CS, Cheng CY. Cadmium-induced testicular injury. Toxicol Appl Pharmacol 2009; 238:240-9; PMID:19236889; http://dx.doi.org/10.1016/j.taap.2009.01.028
   PubMed Web of Science ®Google Scholar
• Mruk DD, Cheng CY. Environmental contaminants. Is male reproductive health at risk? Spermatogenesis 2011; 1:283-90; PMID:22332111; http://dx.doi.org/10.4161/spmg.1.4.18328
   PubMedGoogle Scholar
• Cheng CY, Wong EW, Lie PP, Li MW, Su L, Siu ER, Yan HH, Mannu J, Mathur PP, Bonanomi M, Silvestrini B, et al. Environmental toxicants and male reproductive function. Spermatogenesis 2011; 1:2-13; PMID:21866273; http://dx.doi.org/10.4161/spmg.1.1.13971
   PubMedGoogle Scholar
• Prozialeck W. Evidence that E-cadherin may be a target for cadmium toxicity in epithelial cells. Toxicol Appl Pharmacol 2000; 164:231-49; PMID:10799334; http://dx.doi.org/10.1006/taap.2000.8905
   PubMed Web of Science ®Google Scholar
• Prozialeck WC, Edward JR. Cell adhesion molecules in chemical-induced renal injury. Pharmacol Ther 2007; 114:74-93; PMID:17316817; http://dx.doi.org/10.1016/j.pharmthera.2007.01.001
   PubMed Web of Science ®Google Scholar
• Prozialeck WC, Grunwald GB, Dey PM, Reuhl KR, Parrish AR. Cadherins and NCAM as potential targets in metal toxicity. Toxicol Appl Pharmacol 2002; 182:255-65; PMID:12183105; http://dx.doi.org/10.1006/taap.2002.9422
   PubMed Web of Science ®Google Scholar
• Prozialeck WC, Lamar PC, Lynch SM. Cadmium alters the localization of N-cadherin, E-cadherin, and b-catenin in the proximal tubule epithelium. Toxicol Appl Pharmacol 2003; 189:180-95; PMID:12791303; http://dx.doi.org/10.1016/S0041-008X(03)00130-3
   PubMed Web of Science ®Google Scholar
• Xiao X, Mruk DD, Tang EI, Wong CK, Lee WM, John CM, Turek PJ, Silvestrini B, Cheng CY. 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; PMID:24532171; http://dx.doi.org/10.1093/humrep/deu011
   PubMed Web of Science ®Google Scholar
• Trosko JE. Commentary on “Toxicity testing in the 21st century: a vision and a strategy”: stem cells and cell-cell communication as fundamental targets in assessing the potential toxicity of chemicals. Hum Exp Toxicol 2010; 29:21-9; PMID:20061464; http://dx.doi.org/10.1177/0960327109354663
   PubMed Web of Science ®Google Scholar
• Trosko JE, Chang CC, Upham B, Wilson M. Epigenetic toxicology as toxicant-induced changes in intracellular signalling leading to altered gap junctional intercellular communication. Toxicol Lett 1998; 102-103:71-8; PMID:10022235; http://dx.doi.org/10.1016/S0378-4274(98)00288-4
   PubMed Web of Science ®Google Scholar
• Wan HT, Mruk DD, Wong CKC, Cheng CY. 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; PMID:24169556; http://dx.doi.org/10.1210/en.2013-1657
   PubMed Web of Science ®Google Scholar
• Pointis G, Gilleron J, Carette D, Segretain D. Testicular connexin 43, a precocious molecular target for the effect of environmental toxicants on male fertility. Spermatogenesis 2011; 1:303-17; PMID:22332114; http://dx.doi.org/10.4161/spmg.1.4.18392
   PubMedGoogle Scholar
• Fiorini C, Tilloy-Ellul A, Chevalier S, Charuel C, Pointis G. Sertoli cell junctional proteins as early targets for different classes of reproductive toxicants. Reprod Toxicol 2004; 18:413-21; PMID:15082077; http://dx.doi.org/10.1016/j.reprotox.2004.01.002
   PubMed Web of Science ®Google Scholar
• Li MWM, Mruk DD, Lee WM, Cheng CY. 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; PMID:19497385; http://dx.doi.org/10.1016/j.biocel.2009.05.016
   PubMedGoogle Scholar
• Janecki A, Jakubowiak A, Steinberger A. Effect of cadmium chloride on transepithelial electrical resistance of Sertoli cell monolayers in two-compartment cultures - a new model for toxicological investigations of the “blood-testis” barrier in vitro. Toxicol Appl Pharmacol 1992; 112:51-7; PMID:1733048; http://dx.doi.org/10.1016/0041-008X(92)90278-Z
   PubMed Web of Science ®Google Scholar
• Chung NPY, Cheng CY. Is cadmium chloride-induced inter-Sertoli tight junction permeability barrier disruption a suitable in vitro model to study the events of junction disassembly during spermatogenesis in the rat testis? Endocrinology 2001; 142:1878-88; PMID:11316753
   PubMed Web of Science ®Google Scholar
• Steinberger A, Klinefelter G. Sensitivity of Sertoli and Leydig cells to xenobiotics in in vitro model. Reprod Toxicol 1993; 7 (Suppl 1):23-37; PMID:8400637; http://dx.doi.org/10.1016/0890-6238(93)90066-G
   PubMedGoogle Scholar
• Grima J, Cheng C. Testin induction: the role of cyclic 3’,5’-adenosine monophosphateprotein kinase A signaling in the regulation of basal and lonidamine-induced testin expression by rat Sertoli cells. Biol Reprod 2000; 63:1648-60; PMID:11090432; http://dx.doi.org/10.1095/biolreprod63.6.1648
   PubMed Web of Science ®Google Scholar
• Qiu L, Zhang X, Zhang X, Zhang Y, Gu J, Chen M, Zhang Z, Wang X, Wang SL. Sertoli cell is a potential target for perfluorooctane sulfonate-induced reproductive dysfunction in male mice. Toxicol Sci 2013; 135:229-40; PMID:23761298; http://dx.doi.org/10.1093/toxsci/kft129
   PubMed Web of Science ®Google Scholar
• Lui WY, Wong CH, Mruk DD, Cheng CY. TGF-b3 regulates the blood-testis barrier dynamics via the p38 mitogen activated protein (MAP) kinase pathway: an in vivo study. Endocrinology 2003; 144:1139-42; PMID:12639893; http://dx.doi.org/10.1210/en.2002-0211
   PubMed Web of Science ®Google Scholar
• Wong CH, Mruk DD, Lui WY, Cheng CY. Regulation of blood-testis barrier dynamics: an in vivo study. J Cell Sci 2004; 117:783-98; PMID:14734653; http://dx.doi.org/10.1242/jcs.00900
   PubMed Web of Science ®Google Scholar
• Hew KW, Heath GL, Jiwa AH, Welsh MJ. Cadmium in vivo causes disruption of tight junction-associated microfilaments in rat Sertoli cells. Biol Reprod 1993; 49:840-9; PMID:8218650; http://dx.doi.org/10.1095/biolreprod49.4.840
   PubMed Web of Science ®Google Scholar
• Wiebe J, Kowalik A, Gallardi R, Egeler O, Clubb B. Glycerol disrupts tight junction-associated actin microfilaments, occludin, and microtubules in Sertoli cells. J Androl 2000; 21:625-35; PMID:10975408
   PubMed Web of Science ®Google Scholar
• Setchell BP, Waites GMH. Changes in the permeability of the testicular capillaries and of the “blood-testis barrier” after injection of cadmium chloride in the rat. J Endocrinol 1970; 47:81-6; PMID:5428920; http://dx.doi.org/10.1677/joe.0.0470081
   PubMed Web of Science ®Google Scholar
• Wong CH, Mruk DD, Siu MKY, Cheng CY. Blood-testis barrier dynamics are regulated by a2-macroglobulin via the c-Jun N-terminal protein kinase pathway. Endocrinology 2005; 146:1893-908; PMID:15618353; http://dx.doi.org/10.1210/en.2004-1464
   PubMed Web of Science ®Google Scholar
• Puri P, Walker WH. The tyrosine phosphatase SHP2 regulates Sertoli cell junction complexes. Biol Reprod 2013; 88:59; PMID:23325809; http://dx.doi.org/10.1095/biolreprod.112.104414
   PubMed Web of Science ®Google Scholar
• Lui WY, Lee WM, Cheng CY. Transforming growth factor-b3 regulates the dynamics of Sertoli cell tight junctions via the p38 mitogen-activated protein kinase pathway. Biol Reprod 2003; 68:1597-612; PMID:12606350; http://dx.doi.org/10.1095/biolreprod.102.011387
   PubMed Web of Science ®Google Scholar
• Xiao X, Mruk DD, Lee WM, Cheng CY. c-Yes regulates cell adhesion at the blood-testis barrier and the apical ectoplasmic specialization in the seminiferous epithelium of rat testes. Int J Biochem Cell Biol 2011; 43:651-65; PMID:21256972; http://dx.doi.org/10.1016/j.biocel.2011.01.008
   PubMed Web of Science ®Google Scholar
• Xiao X, Mruk DD, Cheng FL, Cheng CY. c-Src and c-Yes are two unlikely partners of spermatogenesis and their roles in blood-testis barrier dynamics. Adv Exp Med Biol 2012; 763:295-317; PMID:23397631
   PubMed Web of Science ®Google Scholar
• Wan HT, Mruk DD, Wong CKC, Cheng CY. The apical ES-BTB-BM functional axis is an emerging target for toxicant-induced infertility. Trends Mol Med 2013; 19:396-405; PMID:23643465; http://dx.doi.org/10.1016/j.molmed.2013.03.006
   PubMedGoogle Scholar
• Wan HT, Mruk DD, Wong CKC, Cheng CY. Targeting testis-specific proteins to inhibit spermatogenesis - lession from endocrine disrupting chemicals. Expert Opin Ther Targets 2013; 17:839-55; PMID:23600530; http://dx.doi.org/10.1517/14728222.2013.791679
   PubMed Web of Science ®Google Scholar
• Li JCH, Mruk DD, Cheng CY. The inter-Sertoli tight junction permeability barrier is regulated by the inter-play of protein phosphatases and kinases: an in vitro study. J Androl 2001; 22:847-56; PMID:11545299
   PubMed Web of Science ®Google Scholar
• Smith LB, Walker WH. The regulation of spermatogenesis by androgens. Semin Cell Dev Biol 2014; 30:2-13; PMID:24598768; http://dx.doi.org/10.1016/j.semcdb.2014.02.012 (in press)
   PubMed Web of Science ®Google Scholar
• Walker WH. Non-classical actions of testosterone and spermatogenesis. Philos Trans R Soc Lond B Biol Sci 2010; 365:1557-69; PMID:20403869; http://dx.doi.org/10.1098/rstb.2009.0258
   PubMed Web of Science ®Google Scholar
• Li MWM, Mruk DD, Cheng CY. Mitogen-activated protein kinases in male reproductive function. Trends Mol Med 2009; 15:159-68; PMID:19303360; http://dx.doi.org/10.1016/j.molmed.2009.02.002
   PubMed Web of Science ®Google Scholar
• Lie PPY, Cheng CY, Mruk DD. Coordinating cellular events during spermatogenesis: a biochemical model. Trends Biochem Sci 2009; 34:366-73; PMID:19535250; http://dx.doi.org/10.1016/j.tibs.2009.03.005
   PubMed Web of Science ®Google Scholar
• Lui WY, Cheng CY. Regulation of cell junction dynamics by cytokines in the testis - a molecular and biochemical perspective. Cytokine Growth Factor Rev 2007; 18:299-311; PMID:17521954; http://dx.doi.org/10.1016/j.cytogfr.2007.04.009
   PubMedGoogle Scholar
• LoPachin RM, Barber DS. Synaptic cysteine sulfhydryl groups as targets of electrophilic neurotoxicants. Toxicol Sci 2006; 94:240-55; PMID:16880199; http://dx.doi.org/10.1093/toxsci/kfl066
   PubMed Web of Science ®Google Scholar
• Cheng CY, Mruk D, Silvestrini B, Bonanomi M, Wong CH, Siu MK, Lee NP, Lui WY, Mo MY. AF-2364 [1-(2,4-dichlorobenzyl)-1H-indazole-3-carbohydrazide] is a potential male contraceptive: A review of recent data. Contraception 2005; 72:251-61; PMID:16181968; http://dx.doi.org/10.1016/j.contraception.2005.03.008
   PubMed Web of Science ®Google Scholar
• Cheng CY, Mruk DD. New frontiers in non-hormonal male contraception. Contraception 2010 82:476-82; PMID:20933122; http://dx.doi.org/10.1016/j.contraception.2010.03.017
   PubMed Web of Science ®Google Scholar
• Mruk DD, Cheng CY. Cell-cell interactions at the ectoplasmic specialization in the testis. Trends Endocrinol Metab 2004; 15:439-47; PMID:15519891; http://dx.doi.org/10.1016/j.tem.2004.09.009
   PubMed Web of Science ®Google Scholar
• Mok KW, Mruk DD, Lie PPY, Lui WY, Cheng CY. Adjudin, a potential male contraceptive, exerts its effects locally in the seminifeorus epithelium of mammalian testes. Reproduction 2011; 141:571-80; PMID:21307270; http://dx.doi.org/10.1530/REP-10-0464
   PubMed Web of Science ®Google Scholar
• Mruk DD, Silvestrini B, Cheng CY. Anchoring junctions as drug targets: role in contraceptive development. Pharmacol Rev 2008; 60:146-80; PMID:18483144; http://dx.doi.org/10.1124/pr.107.07105
   PubMed Web of Science ®Google Scholar
• Cheng CY, Mruk DD. The blood-testis barrier and its implication in male contraception. Pharmacol Rev 2012; 64:16-64; PMID:22039149; http://dx.doi.org/10.1124/pr.110.002790
   PubMed Web of Science ®Google Scholar
• Wolski KM, Perrault C, Tran-Son-Tay R, Cameron DF. Strength measurement of the Sertoli-spermatid junctional complex. J Androl 2005; 26:354-9; PMID:15867003; http://dx.doi.org/10.2164/jandrol.04142
   PubMed Web of Science ®Google Scholar
• Wolski KM, Mruk DD, Cameron DF. The Sertoli-spermatid junctional complex adhesion strength is affected in vitro by adjudin. J Androl 2006; 27:790-4; PMID:16809272; http://dx.doi.org/10.2164/jandrol.106.000422
   PubMed Web of Science ®Google Scholar
• Cheng CY, Lie PPY, Wong EWP, Mruk DD. Focal adhesion kinase and actin regulatorybinding proteins that modulate F-actin organization at the tissue barrier. Lession from the testis. Tissue Barriers 2013; 1:e24252; PMID:24665388; http://dx.doi.org/10.4161/tisb.24252
   PubMedGoogle Scholar
• Chen YM, Lee NPY, Mruk DD, Lee WM, Cheng CY. Fer kinaseFer T and adherens junction dynamics in the testis: an in vitro and in vivo study. Biol Reprod 2003; 69:656-72; PMID:12700184; http://dx.doi.org/10.1095/biolreprod.103.016881
   PubMed Web of Science ®Google Scholar
• Mok KW, Mruk DD, Lee WM, Cheng CY. Spermatogonial stem cells alone are not sufficient to re-initiate spermatogenesis in the rat testis following adjudin-induced infertility. Int J Androl 2012; 35:86-101; PMID:21696392; http://dx.doi.org/10.1111/j.1365-2605.2011.01183.x
   PubMed Web of Science ®Google Scholar
• Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P. Molecular Biology of the Cell, New York: Garland Science, 2002.
   Google Scholar
• Dym M. Basement membrane regulation of Sertoli cells. Endocr Rev 1994; 15:102-15; PMID:8156935
   PubMed Web of Science ®Google Scholar
• Siu MKY, Cheng CY. Dynamic cross-talk between cells and the extracellular matrix in the testis. BioEssays 2004; 26:978-92; PMID:15351968; http://dx.doi.org/10.1002/bies.20099
   PubMed Web of Science ®Google Scholar
• Tarakanov AO, Goncharova LB. Cell-cell nanotubes: Tunneling through several types of synapses. Commun Integr Biol 2009; 2:359-61; PMID:19721891; http://dx.doi.org/10.4161/cib.2.4.8289
   PubMedGoogle Scholar
• Lou E, Fujisawa S, Barlas A, Romin Y, Manova-Todorova K, Moore MA, Subramanian S. Tunneling nanotubes. A new paradigm for studying intercellular communication and therapeutics in cancer. Commun Integr Biol 2012; 5:399-403; PMID:23060969; http://dx.doi.org/10.4161/cib.20569
   PubMedGoogle Scholar
• Cheng CY, Mruk DD. A local autocrine axis in the testes that regulates spermatogenesis. Nature Rev Endocrinol 2010; 6:380-95; PMID:20571538; http://dx.doi.org/10.1038/nrendo.2010.71
   PubMed Web of Science ®Google Scholar
• Russell LD. Observations on rat Sertoli ectoplasmic (‘junctional’) specializations in their association with germ cells of the rat testis. Tissue Cell 1977; 9:475-98; PMID:929577; http://dx.doi.org/10.1016/0040-8166(77)90007-6
   PubMed Web of Science ®Google Scholar
• Vogl AW, Vaid KS, Guttman JA. The Sertoli cell cytoskeleton. Adv Exp Med Biol 2008; 636:186-211; PMID:19856169; http://dx.doi.org/10.1007/978-0-387-09597-4_11
   PubMed Web of Science ®Google Scholar
• Franca LR, Auharek SA, Hess RA, Dufour JM, Hinton BT. Blood-tissue barriers: morphofunctional and immunological aspects of the blood-testis and blood-epididymal barriers. Adv Exp Med Biol 2012; 763:237-59; PMID:23397628
   PubMed Web of Science ®Google Scholar
• Russell LD. Movement of spermatocytes from the basal to the adluminal compartment of the rat testis. Am J Anat 1977; 148:313-28; PMID:857632; http://dx.doi.org/10.1002/aja.1001480303
   PubMedGoogle Scholar
• Russell LD. Observations on the inter-relationships of Sertoli cells at the level of the blood-testis barrier: evidence for formation and resorption of Sertoli-Sertoli tubulobulbar complexes during the spermatogenic cycle of the rat. Am J Anat 1979; 155:259-79; PMID:474448; http://dx.doi.org/10.1002/aja.1001550208
   PubMedGoogle Scholar
• Russell LD, Peterson RN. Sertoli cell junctions: morphological and functional correlates. Int Rev Cytol 1985; 94:177-211; PMID:3894273; http://dx.doi.org/10.1016/S0074-7696(08)60397-6
   PubMed Web of Science ®Google Scholar
• Wong EWP, Mruk DD, Lee WM, Cheng CY. Par3Par6 polarity complex coordinates apical ectoplasmic specialization and blood-testis barrier restructuring during spermatogenesis. Proc Natl Acad Sci USA 2008; 105:9657-62; PMID:18621709; http://dx.doi.org/10.1073/pnas.0801527105
   PubMed Web of Science ®Google Scholar
• Mruk DD, Cheng CY. Testin and actin are key molecular targets of adjudin, an anti-spermatogenic agent, in the testis. Spermatogenesis 2011; 1:137-46; PMID:22319662; http://dx.doi.org/10.4161/spmg.1.2.16449
   PubMedGoogle Scholar
• Mruk DD, Lau ASN. RAB13 participates in ectoplasmic specialization dynamics in the rat testis. Biol Reprod 2009; 80:590-601; PMID:19074001; http://dx.doi.org/10.1095/biolreprod.108.071647
   PubMed Web of Science ®Google Scholar
• Qian X, Mruk DD, Wong EWP, Lie PPY, Cheng CY. Palladin is a regulator of actin filament bundles at the ectoplasmic specialization in the rat testis. Endocrinology 2013; 154:1907-20; PMID:23546604; http://dx.doi.org/10.1210/en.2012-2269
   PubMedGoogle Scholar
• Lie PPY, Mruk DD, Lee WM, Cheng CY. 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; PMID:19293393; http://dx.doi.org/10.1096/fj.06-070573
   PubMed Web of Science ®Google Scholar
• Lie PPY, Chan AYN, Mruk DD, Lee WM, Cheng CY. Restricted Arp3 expression in the testis prevents blood-testis barrier disruption during junction restructuring at spermatogenesis. Proc Natl Acad Sci USA 2010; 107:11411-6; PMID:20534520; http://dx.doi.org/10.1073/pnas.1001823107
   PubMed Web of Science ®Google Scholar
• Cheng CY, Lie PPY, Wong EWP, Mruk DD, Silvestrini B. Adjudin disrupts spermatogenesis via the action of some unlikely partners: Eps8, Arp23 complex, drebrin E, PAR6 and 14-3-3. Spermatogenesis 2011; 1;291-7; PMID:22332112; http://dx.doi.org/10.4161/spmg.1.4.18393
   PubMedGoogle Scholar
• Lie PPY, Mruk DD, Mok KW, Su L, Lee WM, Cheng CY. 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; PMID:22797892; http://dx.doi.org/10.1073/pnas.1202316109
   PubMed Web of Science ®Google Scholar
• Cheng CY, Mruk DD. An intracellular trafficking pathway in the seminiferous epithelium regulating spermatogenesis: a biochemical and molecular perspective. Crit Rev Biochem Mol Biol 2009; 44:245-63; PMID:19622063; http://dx.doi.org/10.1080/10409230903061207
   PubMed Web of Science ®Google Scholar
• O’Donnell L, Nicholls PK, O’Bryan MK, McLachlan RI, Stanton PG. Spermiation: the process of sperm release. Spermatogenesis 2011; 1:14-35; PMID:21866274; http://dx.doi.org/10.4161/spmg.1.1.14525
   PubMedGoogle Scholar
• Russell LD. Spermatid-Sertoli tubulobulbar complexes as devices for elimination of cytoplasm from the head region in late spermatids of the rat. Anat Rec 1979; 194:233-46; PMID:464324; http://dx.doi.org/10.1002/ar.1091940205
   PubMedGoogle Scholar
• Vogl AW, Young JS, Du M. New insights into roles of tubulobulbar complexes in sperm release and turnover of blood-testis barrier. Int Rev Cell Mol Biol 2013; 303:319-55; PMID:23445814; http://dx.doi.org/10.1016/B978-0-12-407697-6.00008-8
   PubMed Web of Science ®Google Scholar
• Russell LD. Further observations on tubulobulbar complexes formed by late spermatids and Sertoli cells in the rat testis. Anat Rec 1979; 194:213-32; PMID:464323; http://dx.doi.org/10.1002/ar.1091940204
   PubMedGoogle Scholar
• Young JS, Guttman JA, Vaid KS, Vogl AW. Cortactin (CTTN), N-WASP (WASL), and clathrin (CLTC) are present at podosome-like tubulobulbar complexes in the rat testis. Biol Reprod 2009; 80:153-61; PMID:18799755; http://dx.doi.org/10.1095/biolreprod.108.070615
   PubMed Web of Science ®Google Scholar
• Young JS, Guttman JA, Vaid KS, Vogl AW. Tubulobulbar complexes are intercellular podosome-like structures that internalize intact intercellular junctions during epithelial remodeling events in the rat testis. Biol Reprod 2009; 80:162-74; PMID:18799754; http://dx.doi.org/10.1095/biolreprod.108.070623
   PubMed Web of Science ®Google Scholar
• Young JS, Takai YK, Kojic KL, Vogl AW. Internalization of adhesion junction proteins and their association with recycling endosome marker proteins in rat seminiferous epithelium. Reproduction 2012; 143:347-57; PMID:22157319; http://dx.doi.org/10.1530/REP-11-0317
   PubMed Web of Science ®Google Scholar
• Young JS, Vogl AW. Focal adhesion proteins zyxin and vinculin are co-distributed at tubulobulbar complexes. Spermatogenesis 2012; 2:63-8; PMID:22553491; http://dx.doi.org/10.4161/spmg.19391
   PubMedGoogle Scholar
• Du M, Young J, De Asis M, Cipollone J, Roskelley C, Takai Y, Nicholls PK, Stanton PG, Deng W, Finlay BB, et al. A novel subcellular machine contributes to basal junction remodeling in the seminiferous epithelium. Biol Reprod 2013; 88:60; PMID:23303684; http://dx.doi.org/10.1095/biolreprod.112.104851
   PubMed Web of Science ®Google Scholar
• Xiao X, Mruk DD, Wong EW, Lee WM, Han D, Wong CK, Cheng CY. Differential effects of c-Src and c-Yes on the endocytic vesicle-mediated trafficking events at the Sertoli cell blood-testis barrier. Am J Physiol Endocrinol Metab 2014; 307:E553-62; PMID:25117412; http://dx.doi.org/10.1152/ajpendo.00176.2014; (in press)
   PubMedGoogle Scholar
• Russell LD, Saxena NK, Turner TT. Cytoskeletal involvement in spermiation and sperm transport. Tissue Cell 1989; 21:361-79; PMID:2479117; http://dx.doi.org/10.1016/0040-8166(89)90051-7
   PubMed Web of Science ®Google Scholar
• Mruk DD, Cheng CY. Sertoli-Sertoli and Sertoli-germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis. Endocr Rev 2004; 25:747-806; PMID:15466940; http://dx.doi.org/10.1210/er.2003-0022
   PubMed Web of Science ®Google Scholar
• Yan HHN, Mruk DD, Lee WM, Cheng CY. Ectoplasmic specialization: a friend or a foe of spermatogenesis? BioEssays 2007; 29:36-48; PMID:17187371; http://dx.doi.org/10.1002/bies.20513
   PubMed Web of Science ®Google Scholar
• Tang EI, Mruk DD, Cheng CY. MAPmicrotubule affinity-regulating kinases, microtubule dynamics, and spermatogenesis. J Endocrinol 2013; 217:R13-23; PMID:23449618; http://dx.doi.org/10.1530/JOE-12-0586
   PubMedGoogle Scholar
• Qian X, Mruk DD, Cheng YH, Cheng CY. Actin cross-linking protein palladin and spermatogenesis. Spermatogenesis 2013; 3:e23473; PMID:23687615; http://dx.doi.org/10.4161/spmg.23473
   PubMedGoogle Scholar
• Wan HT, Mruk DD, Tang EI, Xiao X, Cheng YH, Wong EW, Wong CK, Cheng CY, et al. Role of non-receptor protein kinases in spermatid transport during spermatogenesis. Sem Cell Dev Biol 2014; 30:65-74; PMID:24727349; http://dx.doi.org/10.1016/j.semcdb.2014.04.013; (in press)
   PubMedGoogle Scholar
• Guttman JA, Kimel GH, Vogl AW. Dynein and plus-end microtubule-dependent motors are associated with specialized Sertoli cell junction plaques (ectoplasmic specializations). J Cell Sci 2000; 113:2167-76; PMID:10825290
   PubMed Web of Science ®Google Scholar
• Lee NPY, Cheng CY. Ectoplasmic specialization, a testis-specific cell-cell actin-based adherens junction type: is this a potential target for male contraceptive development. Human Reprod Update 2004; 10:349-69; PMID:15192055; http://dx.doi.org/10.1093/humupd/dmh026
   PubMed Web of Science ®Google Scholar
• O’Donnell L, O’Bryan MK. Microtubules and spermatogenesis. Semin Cell Dev Biol 2014; 30:45-54; PMID:24440897; http://dx.doi.org/10.1016/j.semcdb.2014.01.003; (in press)
   PubMedGoogle Scholar
• Boekelheide K, Neely MD, Sioussat TM. The Sertoli cell cytoskeleton: a target for toxicant-induced germ cell loss. Toxicol Appl Pharmacol 1989; 101:373-89; PMID:2690397; http://dx.doi.org/10.1016/0041-008X(89)90188-9
   PubMed Web of Science ®Google Scholar
• Allard EK, Johnson KJ, Boekelheide K. Colchicine disrupts the cytoskeleton of rat testis seminiferous epithelium in a stage-dependent manner. Biol Reprod 1993; 48:143-53; PMID:8418902; http://dx.doi.org/10.1095/biolreprod48.1.143
   PubMedGoogle Scholar
• Nakai M, Hess RA. Morphological changes in the rat Sertoli cell induced by the microtubule poison carbendazim. Tissue Cell 1994; 26:917-27; PMID:7886678; http://dx.doi.org/10.1016/0040-8166(94)90041-8
   PubMed Web of Science ®Google Scholar
• Lim JP, Miller MG. The role of the benomyl metabolite carbendazim in benomyl-induced testicular toxicity. Toxicol Appl Pharmacol 1997; 142:401-10; PMID:9070363; http://dx.doi.org/10.1006/taap.1996.8042
   PubMed Web of Science ®Google Scholar
• Nakai M, Hess RA, Moore BJ, Guttroff RF, Strader LF, Linder RE. Acute and long-term effects of a single dose of the fungicide carbendazim (methyl 2-benzimidazole carbamate) on the male reproductive system in the rat. J Androl 1992; 13:507-18; PMID:1293130
   PubMed Web of Science ®Google Scholar
• Winder BS, Strandgaard CS, Miller MG. The role of GTP binding and microtubule-associated proteins in the inhibition of microtubule assembly by carbendazim. Toxicol Sci 2001; 59:138-46; PMID:11134553; http://dx.doi.org/10.1093/toxsci/59.1.138
   PubMed Web of Science ®Google Scholar
• Nakai M, Miller MG, Carnes K, Hess RA. Stage-specific effects of the fungicide carbendazim on Sertoli cell microtubules in rat testis. Tissue Cell 200; 34:73-80; PMID:12165241; http://dx.doi.org/10.1016/S0040-8166(02)00006-X
   PubMedGoogle Scholar
• Wiebe J, Barr K. The control of male fertility by 1,2,3-trihydroxypropane (THP; glycerol): rapid arrest of spermatogenesis without altering libido, accessory organs, gonadal steroidogenesis, and serum testosterone, LH, and FSH. Contraception 1984; 29:291-302; PMID:6428807; http://dx.doi.org/10.1016/S0010-7824(84)80009-8
   PubMed Web of Science ®Google Scholar
• Wiebe J, Barr K, Buckingham K. Sustained azoospermia in squirrel monkey, Saimiri sciureus, resulting from a single intratesticular glycerol injection. Contraception 1989; 39:447-57; PMID:2721196; http://dx.doi.org/10.1016/0010-7824(89)90122-4
   PubMedGoogle Scholar
• Boekelheide K, Fleming SL, Allio T, Embree-Ku ME, Hall SJ, Johnson KJ, Kwon EJ, Patel SR, Rasoulpour RJ, Schoenfeld HA, et al. 2,5-Hexanedione-induced testicular injury. Annu Rev Pharmacol Toxciol 2003; 43:125-47; PMID:12471174; http://dx.doi.org/10.1146/annurev.pharmtox.43.100901.135930
   PubMed Web of Science ®Google Scholar
• Johnson, KJ. Testicular histopathology associated with disruption of the Sertoli cell cytoskeleton. Spermatogenesis 2014; (in press).
   Google Scholar
• Tang EI, Xiao X, Mruk DD, Qian XJ, Mok KW, Jenardhanan P, Lee WM, Mathur PP, Cheng CY. Microtubule affinity-regulated kinase 4 (MARK4) is a component of the ectoplasmic specialization in the rat testis. Spermatogenesis 2012; 2:117-26; PMID:22670221; http://dx.doi.org/10.4161/spmg.20724
   PubMedGoogle Scholar
• Thomason HA, Scothern A, McHarg S, Garrod DR. Desmosomes: adhesive strength and signalling in health and disease. Biochem J 2010; 429:419-33; PMID:20626351; http://dx.doi.org/10.1042/BJ20100567
   PubMed Web of Science ®Google Scholar
• Green K, Gaudry C. Are desmosomes more than tethers for intermediate filaments? Nat Rev Cell Biol 2000; 1:208-16; PMID:11252896; http://dx.doi.org/10.1038/35043032
   PubMedGoogle Scholar
• Green KJ, Simpson CL. Desmosomes: New perspectives on a classic. J Invest Dermatol 2007; 127:2499-515; PMID:17934502; http://dx.doi.org/10.1038/sj.jid.5701015
   PubMed Web of Science ®Google Scholar
• Cheng CY, Mruk DD. Cell junction dynamics in the testis: sertoli-germ cell interactions and male contraceptive development. Physiol Rev 2002; 82:825-74; PMID:12270945
   PubMed Web of Science ®Google Scholar
• Mruk DD, Cheng CY. Desmosomes in the testis. Moving into an unchartered territory. Spermatogenesis 2011; 1:47-51; PMID:21866275; http://dx.doi.org/10.4161/spmg.1.1.15443
   PubMedGoogle Scholar
• Lie PPY, Cheng CY, Mruk DD. The biology of the desmosome-like junction: A versatile anchoring junction and signal transducer in the seminiferous epithelium. Int Rev Cell Mol Biol 2011; 286:223-69; PMID:21199783 [http://dx.doi.org/10.1016/B978-0-12-385859-7.00005-7
   PubMed Web of Science ®Google Scholar
• Russell LD. Desmosome-like junctions between Sertoli and germ cells in the rat testis. Am J Anat 1977; 148:301-12; PMID:857631; http://dx.doi.org/10.1002/aja.1001480302
   PubMedGoogle Scholar
• Franke W, Grund C, Schmid E. Intermediate-sized filaments present in Sertoli cells are of the vimentin type. Eur J Cell Biol 1979; 19:269-75; PMID:385322
   PubMed Web of Science ®Google Scholar
• Green KJ, Getsios S, Troyanovsky S, Godsel LM. Intercellular junction assembly, dynamics, and homeostasis. Cold Spring Harb Perspect Biol 2010; 2:a000125; PMID:20182611; http://dx.doi.org/10.1101/cshperspect.a000125
   PubMed Web of Science ®Google Scholar
• Colucci-Guyon E, Portier MM, Dunia I, Paulin D, Pournin S, Babinet C. Mice lacking vimentin develop and reproduce without an obvious phenotype. Cell 1994; 79:679-94; PMID:7954832; http://dx.doi.org/10.1016/0092-8674(94)90553-3
   PubMedGoogle Scholar
• Li MWM, Mruk DD, Cheng CY. Gap junctions and blood-tissue barriers. Adv Exp Med Biol 2012; 763:260-80; PMID:23397629
   PubMed Web of Science ®Google Scholar
• Pointis G, Gilleron J, Carette D, Segretain D. Physiological and physiopathological aspects of connexins and communicating gap junctions in spermatogenesis. Philos Trans R Soc Lond B Biol Sci 2010; 365:1607-20; PMID:20403873; http://dx.doi.org/10.1098/rstb.2009.0114
   PubMed Web of Science ®Google Scholar
• Russell LD. Morphological and functional evidence for Sertoli-germ cell relationships. In: The Sertoli Cell. eds. Russell LD, Griswold MD. Clearwater: Cache River Press, 1993, 365-90.
   Google Scholar
• Hall ES, Eveleth J, Boekelheide K. 2,5-Hexanedione exposure alters the rat Sertoli cell cytoskeleton. II. Intermediate filaments and actin. Toxicol Appl Pharmacol 1991; 111:443-53; PMID:1746025; http://dx.doi.org/10.1016/0041-008X(91)90249-E
   PubMedGoogle Scholar
• Chapin RE, Morgan KT, Bus JS. The morphogenesis of testicular degeneration induced in rats by orally administered 2,5-hexanedione. Exp Mol Pathol 1983; 38:149-69; PMID:6832342; http://dx.doi.org/10.1016/0014-4800(83)90082-5
   PubMed Web of Science ®Google Scholar
• Corsi G, Palazzo G, Germani C, Scorza Barcellona P, Silvestrini B. 1-Halobenzyl-1H-indazole-3-carboxylic acids. A new class of antispermatogenic agents. J Med Chem 1976; 19:778-83; PMID:950645; http://dx.doi.org/10.1021/jm00228a008
   PubMed Web of Science ®Google Scholar
• Cheng CY, Silvestrini B, Grima J, Mo MY, Zhu LJ, Johansson E, Saso L, Leone MG, Palmery M, Mruk D. Two new male contraceptives exert their effects by depleting germ cells prematurely from the testis. Biol Reprod 2001; 65:449-61; PMID:11466213; http://dx.doi.org/10.1095/biolreprod65.2.449
   PubMedGoogle Scholar
• Cheng CY, Mo My, Grima J, Saso L, Tita B, Mruk D, Silvestrini B. Indazole carboxylic acids in male contraception. Contraception 2002; 65:265-8; PMID:12020774; http://dx.doi.org/10.1016/S0010-7824(01)00318-3
   PubMed Web of Science ®Google Scholar
• Grima J, Silvestrini B, Cheng CY. Reversible inhibition of spermatogenesis in rats using a new male contraceptive, 1-(2,4-dichlorobenzyl)-indazole-3-carbohydrazide. Biol Reprod 2001; 64:1500-8; PMID:11319158; http://dx.doi.org/10.1095/biolreprod64.5.1500
   PubMed Web of Science ®Google Scholar
• Boekelheide K. Sertoli cell toxicants. In: The Sertoli Cell. eds. Russell L, Griswold M. Clearwater: Cache River Press, 1993, 551-75.
   Google Scholar
• Boekelheide K, Hall SJ. 2,5-Hexanedione exposure in the rat results in long-term testicular atrophy despite the presence of residual spermatogonia. J Androl 1991; 12:18-26; PMID:2010348
   PubMed Web of Science ®Google Scholar
• Boekelheide K, Johnson KJ, Richburg JH. Sertoli cell toxicants. In: Sertoli Cell Biology. Eds. Skinner MK, Griswold MD. New York: Elsevier Science, 2005, pp. 345-82.
   Google Scholar
• Cheng CY, Wong EWP, Yan HHN, Mruk DD. Regulation of spermatogenesis in the microenvironment of the seminiferous epithelium: new insights and advances. Mol Cell Endocrinol 2010; 315:49-56; PMID:19682538 [http://dx.doi.org/10.1016/j.mce.2009.08.004
   PubMed Web of Science ®Google Scholar
• Russell LD, Goh JC, Rashed RMA, Vogl AW. The consequences of actin disruption at Sertoli ectoplasmic specialization sites facing spermatids after in vivo exposure of rat testis to cytochalasin D. Biol Reprod 1988; 39:105-18; PMID:3207792; http://dx.doi.org/10.1095/biolreprod39.1.105
   PubMed Web of Science ®Google Scholar
• Palombi F, Salanova M, Tarone G, Farini D, Stefanini M. Distribution of b1 integrin subunit in rat seminiferous epithelium. Biol Reprod 1992; 47:1173-82; PMID:1283530; http://dx.doi.org/10.1095/biolreprod47.6.1173
   PubMed Web of Science ®Google Scholar
• Salanova M, Ricci G, Boitani C, Stefanini M, De Grossi S, Palombi F. Junctional contacts between Sertoli cells in normal and aspermatogenic rat seminiferous epithelium contain a6b1 integrins, and their formation is controlled by follicle-stimulating hormone. Biol Reprod 1998; 58:371-8; PMID:9475391; http://dx.doi.org/10.1095/biolreprod58.2.371
   PubMed Web of Science ®Google Scholar
• Siu MKY, Cheng CY. Interactions of proteases, protease inhibitors, and the b1 integrinlaminin g3 protein complex in the regulation of ectoplasmic specialization dynamics in the rat testis. Biol Reprod 2004; 70:945-64; PMID:14645107; http://dx.doi.org/10.1095/biolreprod.103.023606
   PubMed Web of Science ®Google Scholar
• Yan HHN, Cheng CY. Laminin name=a3 forms a complex with b3 and g3 chains that serves as the ligand for a6b1-integrin at the apical ectoplasmic specialization in adult rat testes. J Biol Chem 2006; 281:17286-303; PMID:16608848; http://dx.doi.org/10.1074/jbc.M513218200
   PubMed Web of Science ®Google Scholar
• Mok KW, Lie PP, Mruk DD, Mannu J, Mathur PP, Silvestrini B, Cheng CY. The apical ectoplasmic specialization-blood-testis barrier functional axis is a novel target for male contraception. Adv Exp Med Biol 2012; 763:334-55; PMID:23397633
   PubMed Web of Science ®Google Scholar
• Mruk DD, Wong CH, Silvestrini B, Cheng CY. A male contraceptive targeting germ cell adhesion. Nature Med 2006; 12:1323-8; PMID:17072312; http://dx.doi.org/10.1038/nm1420
   PubMed Web of Science ®Google Scholar
• Aoki A, Hoffer A. Re-examination of the lesions in rat testis caused by cadmium. Biol Reprod 1978; 18:579-91; PMID:207367; http://dx.doi.org/10.1095/biolreprod18.4.579
   PubMed Web of Science ®Google Scholar
• Taurog JD, Rival C, van Duivenvoorde LM, Satumtira N, Dorris ML, Sun M, Shelton JM, Richardson JA, Hamra FK, Hammer RE, et al. Autoimmune epididymo-porchitis is esential to the pathogenesis of male-specific spondyoarthritis in HLA-B27-transgenic rats. Arthritis Rheum 2012; 64:2518-28; PMID:22488218; http://dx.doi.org/10.1002/art.34480
   PubMedGoogle Scholar
• Tung KSK, Unanue ER, Dixon FJ. The immunopathology of experimental allergic orchitis. Am J Pathol 1970; 60:313-28; PMID:4918181
   PubMed Web of Science ®Google Scholar
• Zhang Y, Li N, Chen Q, Yan K, Liu Z, Zhang X, Liu P, Chen Y, Han D. Breakdown of immune homeostasis in the testis of mice lacking Tyro3, Axl and Mer receptor tyrosine kinases. Immunol Cell Biol 2013; 91:416-26; PMID:23689306; http://dx.doi.org/10.1038/icb.2013.22
   PubMedGoogle Scholar
• Wheeler KM, Tardif S, Rival C, Luu B, Bui E, Del Rio R, Teuscher C, Sparwasser T, Hardy D, Tung KS. Regulatory T cells control tolerance versus autoimmunity to sperm in vasectomy. Proc Nat Acad Sci U S A 2011; 108:7511-6; PMID:21502500; http://dx.doi.org/10.1073/pnas.1017615108
   PubMedGoogle Scholar