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Review

Testicular histopathology associated with disruption of the Sertoli cell cytoskeleton

Article: e979106 | Received 15 May 2014, Accepted 16 Oct 2014, Published online: 19 Feb 2015

References

  • Wong V, Russell LD. Three-dimensional reconstruction of a rat stage V Sertoli cell: I. Methods, basic configuration, and dimensions. Am J Anat 1983; 167:143-61; PMID:6351582; http://dx.doi.org/10.1002/aja.1001670202
  • Wang F, Zhang Q, Cao J, Huang Q, Zhu X. The microtubule plus end-binding protein EB1 is involved in Sertoli cell plasticity in testicular seminiferous tubules. Exp Cell Res 2008; 314:213-26; PMID:17964570; http://dx.doi.org/10.1016/j.yexcr.2007.09.022
  • Correa LM, Nakai M, Strandgaard CS, Hess RA, Miller MG. Microtubules of the mouse testis exhibit differential sensitivity to the microtubule disruptors Carbendazim and colchicine. Toxicol Scie 2002; 69:175-82; PMID:12215672; http://dx.doi.org/10.1093/toxsci/69.1.175
  • 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
  • Russell LD, Malone JP, MacCurdy DS. Effect of the microtubule disrupting agents, colchicine and vinblastine, on seminiferous tubule structure in the rat. Tissue Cell 1981; 13:349-67; PMID:7314074; http://dx.doi.org/10.1016/0040-8166(81)90010-0
  • Brieher WM, Yap AS. Cadherin junctions and their cytoskeleton(s). Curr Opin Cell Biol 2013; 25:39-46; PMID:23127608; http://dx.doi.org/10.1016/j.ceb.2012.10.010
  • Jaqaman K, Grinstein S. Regulation from within: the cytoskeleton in transmembrane signaling. Trends Cell Biol 2012; 22:515-26; PMID:22917551; http://dx.doi.org/10.1016/j.tcb.2012.07.006
  • 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.
  • Neely MD, Boekelheide K. Sertoli cell processes have axoplasmic features: an ordered microtubule distribution and an abundant high molecular weight microtubule-associated protein (cytoplasmic dynein). J Cell Biol 1988; 107:1767-76; PMID:2972729; http://dx.doi.org/10.1083/jcb.107.5.1767
  • Vogl AW. Changes in the distribution of microtubules in rat Sertoli cells during spermatogenesis. Anat Record 1988; 222:34-41; PMID:3056115; http://dx.doi.org/10.1002/ar.1092220107
  • Vaid KS, Guttman JA, Singaraja RR, Vogl AW. A kinesin is present at unique sertoli/spermatid adherens junctions in rat and mouse testes. Biol Reprod 2007; 77:1037-48; PMID:17855729; http://dx.doi.org/10.1095/biolreprod.107.063735
  • Vogl AW, Pfeiffer DC, Mulholland D, Kimel G, Guttman J. Unique and multifunctional adhesion junctions in the testis: ectoplasmic specializations. Arch Histol Cytol 2000; 63:1-15; PMID:10770585; http://dx.doi.org/10.1679/aohc.63.1
  • Richburg JH, Redenbach DM, Boekelheide K. Seminiferous tubule fluid secretion is a Sertoli cell microtubule-dependent process inhibited by 2,5-hexanedione exposure. Toxicol Appl Pharmacol 1994; 128:302-9; PMID:7940545; http://dx.doi.org/10.1006/taap.1994.1210
  • Fleming SL, Shank PR, Boekelheide K. gamma-Tubulin overexpression in Sertoli cells in vivo. II: Retention of spermatids, residual bodies, and germ cell apoptosis. Biol Reprod 2003; 69:322-30; PMID:12672672; http://dx.doi.org/10.1095/biolreprod.102.011817
  • 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
  • Mruk DD, Cheng CY. Sertoli-Sertoli and Sertoli-germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis. Endocrine Rev 2004; 25:747-806; PMID:15466940; http://dx.doi.org/10.1210/er.2003-0022
  • 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
  • Vogl AW, Du M, Wang XY, Young JS. Novel clathrin/actin-based endocytic machinery associated with junction turnover in the seminiferous epithelium. Semin Cell Dev Biol 2013;55-64; PMID:24280271
  • Franke WW, 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
  • 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
  • Russell L. 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
  • 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
  • Vogl AW, Colucci-Guyon E, Babinet C. Vimentin intermediate filaments are not necessary for the development of a normal differentiated phenotype by mature Sertoli cells. Mol Biology Cell 1996; 7:555a.
  • Richburg JH, Boekelheide K. Mono-(2-ethylhexyl) phthalate rapidly alters both Sertoli cell vimentin filaments and germ cell apoptosis in young rat testes. Toxicol Appl Pharmacol 1996; 137:42-50; PMID:8607140; http://dx.doi.org/10.1006/taap.1996.0055
  • Hall ES, Eveleth J, Boekelheide K. Two,5-Hexanedione exposure alters the rat Sertoli cell cytoskeleton. II. Intermediate filaments and actin. Toxicol Appl Pharmacol 1991; 111:443-53; PMID:1746025
  • Alam MS, Kurohmaru M. Disruption of Sertoli cell vimentin filaments in prepubertal rats: An acute effect of butylparaben in vivo and in vitro. Acta Histochem 2014; 682-7.
  • 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
  • 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
  • Lim J, 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
  • 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
  • Nakai M, Miller MG, Carnes K, Hess RA. Stage-specific effects of the fungicide carbendazim on Sertoli cell microtubules in rat testis. Tissue Cell 2002; 34:73-80; PMID:12165241; http://dx.doi.org/10.1016/S0040-8166(02)00006-X
  • Hess RA, Moore BJ, Forrer J, Linder RE, Abuel-Atta AA. The fungicide benomyl (methyl 1-(butylcarbamoyl)-2-benzimidazolecarbamate) causes testicular dysfunction by inducing the sloughing of germ cells and occlusion of efferent ductules. Fundam Appl Toxicol 1991; 17:733-45; PMID:1778360; http://dx.doi.org/10.1016/0272-0590(91)90181-3
  • Moffit JS, Bryant BH, Hall SJ, Boekelheide K. Dose-dependent effects of sertoli cell toxicants 2,5-hexanedione, carbendazim, and mono-(2-ethylhexyl) phthalate in adult rat testis. Toxicol Pathol 2007; 35:719-27; PMID:17763286; http://dx.doi.org/10.1080/01926230701481931
  • Hess RA, Nakai M. Histopathology of the male reproductive system induced by the fungicide benomyl. Histol Histopathol 2000; 15:207-24; PMID:10668211
  • Nakai M, Hess RA, Netsu J, Nasu T. Deformation of the rat Sertoli cell by oral administration of carbendazim (methyl 2-benzimidazole carbamate). J Androl 1995; 16:410-6; PMID:8575980
  • Leblond CP, Clermont Y. Definition of the stages of the cycle of the seminiferous epithelium in the rat. Ann New York Acad Sci 1952; 55:548-73; PMID:13139144; http://dx.doi.org/10.1111/j.1749-6632.1952.tb26576.x
  • Rao S, He L, Chakravarty S, Ojima I, Orr GA, Horwitz SB. Characterization of the Taxol binding site on the microtubule. Identification of Arg(282) in β-tubulin as the site of photoincorporation of a 7-benzophenone analogue of Taxol. J Biol Chem 1999; 274:37990-4; PMID:10608867; http://dx.doi.org/10.1074/jbc.274.53.37990
  • Schiff PB, Horwitz SB. Taxol stabilizes microtubules in mouse fibroblast cells. Proc Natl Acad Sci U S A 1980; 77:1561-5; PMID:6103535; http://dx.doi.org/10.1073/pnas.77.3.1561
  • Vogl AW, Linck RW, Dym M. Colchicine-induced changes in the cytoskeleton of the golden-mantled ground squirrel (Spermophilus lateralis) Sertoli cells. A J Anat 1983; 168:99-108; PMID:6637858; http://dx.doi.org/10.1002/aja.1001680110
  • Kerr JB, de Kretser DM. Proceedings: The role of the Sertoli cell in phagocytosis of the residual bodies of spermatids. J Reprod Fertil 1974; 36:439-40; PMID:4819326; http://dx.doi.org/10.1530/jrf.0.0360439
  • Russell LD, Ettlin RA, Sinha Hikim AP, Clegg ED. Histological and Histopathological Evaluation of the Testis. Clearwater, FL: Cache River Press, 1990.
  • Bryant BH, Yamasaki H, Sandrof MA, Boekelheide K. Spermatid head retention as a marker of 2,5-hexanedione-induced testicular toxicity in the rat. Toxicol Pathol 2008; 36:552-9; PMID:18467684; http://dx.doi.org/10.1177/0192623308317426
  • Russell LD. The perils of sperm release– ‘let my children go’. Int J Androl 1991; 14:307-11; PMID:1794915; http://dx.doi.org/10.1111/j.1365-2605.1991.tb01097.x
  • Markelewicz RJ, Jr., Hall SJ, Boekelheide K. Two,5-hexanedione and carbendazim coexposure synergistically disrupts rat spermatogenesis despite opposing molecular effects on microtubules. Toxicol Sci 2004; 80:92-100; PMID:15141104; http://dx.doi.org/10.1093/toxsci/kfh140
  • 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
  • Smith LB, Milne L, Nelson N, Eddie S, Brown P, Atanassova N, O’Bryan MK, O’Donnell L, Rhodes D, Wells S, et al. KATNAL1 regulation of sertoli cell microtubule dynamics is essential for spermiogenesis and male fertility. PLoS Genet 2012; 8:e1002697; PMID:22654668; http://dx.doi.org/10.1371/journal.pgen.1002697
  • Komada M, McLean DJ, Griswold MD, Russell LD, Soriano P. E-MAP-115, encoding a microtubule-associated protein, is a retinoic acid-inducible gene required for spermatogenesis. Genes Dev 2000; 14:1332-42; PMID:10837026
  • Boekelheide K, Fleming SL, Allio T, Embree-Ku ME, Hall SJ, Johnson KJ, Kwon EJ, Patel SR, Rasoulpour RJ, Schoenfeld HA, et al. Two,5-hexanedione-induced testicular injury. Ann Rev Pharmacol Toxicol 2003; 43:125-47; PMID:12471174; http://dx.doi.org/10.1146/annurev.pharmtox.43.100901.135930
  • 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
  • Wiebe JP, Kowalik A, Gallardi RL, Egeler O, Clubb BH. Glycerol disrupts tight junction-associated actin microfilaments, occludin, and microtubules in Sertoli cells. J Androl 2000; 21:625-35; PMID:10975408
  • Cooper JA. Effects of cytochalasin and phalloidin on actin. J Cell Biol 1987; 105:1473-8; PMID:3312229; http://dx.doi.org/10.1083/jcb.105.4.1473
  • Weber JE, Turner TT, Tung KS, Russell LD. Effects of cytochalasin D on the integrity of the Sertoli cell (blood-testis) barrier. Am J Anat 1988; 182:130-47; PMID:3400621; http://dx.doi.org/10.1002/aja.1001820204
  • Russell LD, Goh JC, Rashed RM, 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
  • Young JS, De Asis M, Guttman J, Vogl AW. Cortactin depletion results in short tubulobulbar complexes and spermiation failure in rat testes. Biol Open 2012; 1:1069-77; PMID:23213386; http://dx.doi.org/10.1242/bio.20122519
  • Weaver AM, Karginov AV, Kinley AW, Weed SA, Li Y, Parsons JT, Cooper JA. Cortactin promotes and stabilizes Arp2/3-induced actin filament network formation. Curr Biol : CB 2001; 11:370-4; PMID:11267876; http://dx.doi.org/10.1016/S0960-9822(01)00098-7
  • Johnson KJ, Hall ES, Boekelheide K. Two,5-Hexanedione exposure alters the rat Sertoli cell cytoskeleton. I. Microtubules and seminiferous tubule fluid secretion. Toxicol Appl Pharmacol 1991; 111:432-42; PMID:1746024; http://dx.doi.org/10.1016/0041-008X(91)90248-D
  • Lim J, Miller MG. Role of testis exposure levels in the insensitivity of prepubertal rats to carbendazim-induced testicular toxicity. Fundam Appl Toxicol 1997; 37:158-67; PMID:9242589; http://dx.doi.org/10.1006/faat.1997.2315
  • Carter SD, Hess RA, Laskey JW. The fungicide methyl 2-benzimidazole carbamate causes infertility in male Sprague-Dawley rats. Biol Reprod 1987; 37:709-17; PMID:3676414; http://dx.doi.org/10.1095/biolreprod37.3.709

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