The Sertoli Cell Cytoskeleton

  • A. Wayne Vogl
  • Kuljeet S. Vaid
  • Julian A. Guttman

Abstract

The cytoskeleton of terminally differentiated mammalian Sertoli cells is one of the most elaborate of those that have been described for cells in tissues. Actin filaments, intermediate filaments and microtubules have distinct patterns of distribution that change during the cyclic process of spermatogenesis. Each of the three major cytoskeletal elements is either concentrated at or related in part to intercellular junctions. Actin filaments are concentrated in unique structures termed ectoplasmic specializations that function in intercellular adhesion, and at tubulobulbar complexes that are thought to be involved with junction internalization during sperm release and movement of spermatocytes through basal junctions between neighboring Sertoi cells. Intermediate filaments occur in a perinuclear network which has peripheral extensions to desmosome-like junctions with adjacent cells and to small hemidesmosome-like attachments to the basal lamina. Unlike in most other epithelia where the intermediate filaments are of the keratin type, intermediate filaments in mature Sertoli cells are of the vimentin type. The function of intermediate filaments in Sertoli cells in not entirely clear; however, the pattern of filament distribution and the limited experimental data available are consistent with a role in maintaining tissue integrity when the epithelium is mechanically stressed. Microtubules are abundant in Sertoli cells and are predominantly oriented parallel to the long axis of the cell. Microtubules are involved with maintaining the columnar shape of Sertoli cells, with transporting and positioning organelles in the cytoplasm, and with secreting seminiferous tubule fluid. In addition, microtubule-based transport machinery is coupled to intercellular junctions to translocate and position adjacent spermatids in the epithelium. Although the cytoskeleton of Sertoli cells has structural and functional properties common to cells generally, there are a number of properties that are unique and that appear related to processes fundamental to spermatogenesis and to interfacing somatic cells both with similar neighboring somatic cells and with differentiating cells of the germ cell line.

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References

  1. 1.
    Amlani S, Vogl AW. Changes in the distribution of microtubules and intermediate filaments in mammalian Sertoli cells during spermatogenesis. Anat Rec 1988; 220:143–160.PubMedCrossRefGoogle Scholar
  2. 2.
    Winder SJ, Ayscough KR. Actin-binding proteins. J Cell Sci 2005; 118:651–654.PubMedCrossRefGoogle Scholar
  3. 3.
    Kovar DR. Molecular details of formin-mediated actin assembly. Curr Opin Cell Biol 2006; 18:11–7.PubMedCrossRefGoogle Scholar
  4. 4.
    Bos JL. Linking Rap to cell adhesion. Curr Opin Cell Biol 2005; 17:123–128.PubMedCrossRefGoogle Scholar
  5. 5.
    DeMali KA, Burridge K. Coupling membrane protrusion and cell adhesion. J Cell Sci 2003; 116:2389–2397.PubMedCrossRefGoogle Scholar
  6. 6.
    Pollard TD. Introduction to actin and actin-binding proteins. In: Kreis T, Vale R, eds. Guidebook to the Cytoskeletal and Motor Proteins. New York: Oxford University Press, 1999:3–11.Google Scholar
  7. 7.
    Mooseker MS, Cheney RE. Unconventional myosins. Annual Rev Cell Dev Biol 1995; 11:633–675.CrossRefGoogle Scholar
  8. 8.
    Pollard TD, Borisy GG. Cellular motility driven by assembly and disassembly of actin filaments. Cell 2003; 112:453–465.PubMedCrossRefGoogle Scholar
  9. 9.
    Zigmond S. Formin’ adherens junctions. Nature Cell Biol 2004; 6:12–14.PubMedCrossRefGoogle Scholar
  10. 10.
    Dym M, Fawcett DW. The blood-testis barrier in the rat and the physiological compartmentation of the seminiferous epithelium. Biol Reprod 1970; 3:308–326.PubMedGoogle Scholar
  11. 11.
    Russell LD, Peterson RN. Sertoli cell junctions: Morphological and functional correlates. Int Rev Cytol 1985; 94:177–211.PubMedCrossRefGoogle Scholar
  12. 12.
    Vogl AW. Distribution and function of organized concentrations of actin filaments in mammalian spermatogenic cells and Sertoli cells. Int Rev Cytol 1989; 119:1–56.PubMedCrossRefGoogle Scholar
  13. 13.
    Vogl A, Pfeiffer DC, Redenbach DM. Sertoli cell cytoskeleton: Influence on spermatogenic cells. In: Baccetti B, ed. Proceedings of the VI international congress on spermatology. Comparative Spermatology 20 years after. Italy, Serona Symposia: Raven Press, 1991:709–715.Google Scholar
  14. 14.
    Vogl AW, Pfeiffer DC, Redenbach DM. Ectoplasmic (“junctional”) specializations in mammalian Sertoli cells: Influence on spermatogenic cells. Ann NY Acad Sci 1991; 637:175–202.PubMedCrossRefGoogle Scholar
  15. 15.
    Vogl AW, Pfeiffer DC, Redenbach DM et al. Sertoli cell cytoskeleton. In: Russell LD, Griswold MD, eds. The Sertoli Cell. Clearwater: Cache River Press, 1993:39–86.Google Scholar
  16. 16.
    Vogl AW, Pfeiffer DC, Mulholland D et al. Unique and multifunctional adhesion junctions in the testis: Ectoplasmic specializations. Arch Histol Cytol 2000; 63:1–15.PubMedCrossRefGoogle Scholar
  17. 17.
    Toyama Y, Maekawa M, Yuasa S. Ectoplasmic specializations in the Sertoli cell: New vistas based on genetic defects and testicular toxicology. Anat Sci Int 2003; 78:1–16.PubMedCrossRefGoogle Scholar
  18. 18.
    Lee NP, Cheng CY. Ectoplasmic specialization, a testis-specific cell-cell actin-based adherens junction type: Is this a potential target for male contraceptive development? Hum Reprod Update 2004; 10:349–369.PubMedCrossRefGoogle Scholar
  19. 19.
    Mruk DD, Cheng CY. Cell-cell interactions at the ectoplasmic specialization in the testis. Trends Endocrinol Metab 2004; 15:439–447.PubMedGoogle Scholar
  20. 20.
    Guttman JA, Mulholland DJ, Vogl AW. Plectin is concentrated at intercellular junctions and at the nuclear surface in morphologically differentiated rat Sertoli cells. Anat Rec 1999; 254:418–428.PubMedCrossRefGoogle Scholar
  21. 21.
    Romrell LJ, Ross MH. Characterization of Sertoli cell-germ cell junctional specializations in dissociated testicular cells. Anat Rec 1979; 193:23–41.PubMedCrossRefGoogle Scholar
  22. 22.
    Pelletier RM. Cyclic modulation of Sertoli cell junctional complexes in a seasonal breeder: The mink (Mustela vison). Am J Anat 1988; 183:68–102.PubMedCrossRefGoogle Scholar
  23. 23.
    Pelletier RM, Friend DS. The Sertoli cell junctional complex: Structure and permeability to filipin in the neonatal and adult guinea pig. Am J Anat 1983; 168:213–228.PubMedCrossRefGoogle Scholar
  24. 24.
    Palombi F, Salanova M, Tarone G et al. Distribution of β1 integrin subunit in rat seminiferous epithelium. Biol Reprod 1992; 47:1173–1182.PubMedCrossRefGoogle Scholar
  25. 25.
    Salanova M, Stefanini M, De Curtis I et al. Integrin receptor alpha 6 beta 1 is localized at specific sites of cell-to-cell contact in rat seminiferous epithelium. Biol Reprod 1995; 52:79–87.PubMedCrossRefGoogle Scholar
  26. 26.
    Ozaki-Kuroda K, Nakanishi H, Ohta H et al. Nectin couples cell-cell adhesion and the actin scaffold at heterotypic testicular junctions. Curr Biol 2002; 12:1145–1150.PubMedCrossRefGoogle Scholar
  27. 27.
    Gliki G, Ebnet K, Aurrand-Lions M et al. Spermatid differentiation requires the assembly of a cell polarity complex downstream of junctional adhesion molecule-C. Nature 2004; 431:320–324.PubMedCrossRefGoogle Scholar
  28. 28.
    Wine RN, Chapin RE. Adhesion and signaling proteins spatiotemporally associated with spermiation in the rat. J Androl 1999; 20:198–213.PubMedGoogle Scholar
  29. 29.
    Yan HH, Cheng CY. Blood-testis barrier dynamics are regulated by an engagement/disengagement mechanism between tight and adherens junctions via peripheral adaptors. Proc Natl Acad Sci USA 2005; 102:11722–11727.PubMedCrossRefGoogle Scholar
  30. 30.
    Sarkar O, Xia W, Mruk DD. Adjudin-mediated junction restructuring in the seminiferous epithelium leads to displacement of soluble guanylate cyclase from adherens junctions. J Cell Physiol 2006; 208:175–187.PubMedCrossRefGoogle Scholar
  31. 31.
    Siu MK, Cheng CY. Interactions of proteases, protease inhibitors, and the beta 1 integrin/laminin gamma3 protein complex in the regulation of ectoplasmic specialization dynamics in the rat testis. Biol Reprod 2004; 70:945–964.PubMedCrossRefGoogle Scholar
  32. 32.
    Grove BD, Pfeiffer DC, Allen S et al. Immunofluorescence localization of vinculin in ectoplasmic (“junctional”) specializations of rat Sertoli cells. Am J Anat 1990; 188:44–56.PubMedCrossRefGoogle Scholar
  33. 33.
    Xia W, Cheng CY. TGF-β3 regulates anchoring junction dynamics in the seminiferous epithelium of the rat testis via the Ras/ERK signaling pathway: An in vivo study. Dev Biol 2005; 280:321–343.PubMedCrossRefGoogle Scholar
  34. 34.
    Franke WW, Grund C, Fink A et al. Location of actin in the microfilament bundles associated with the junctional specializations between Sertoli cells and spermatids. Biol Cell 1978; 31:7–14.Google Scholar
  35. 35.
    Grove BD, Vogl AW. Sertoli cell ectoplasmic specializations: A type of actin-associated adhesion junction? J Cell Sci 1989; 93:309–323.PubMedGoogle Scholar
  36. 36.
    Bartles JR, Wierda A, Zheng L. Identification and characterization of espin, an actin-binding protein localized to the F-actin-rich junctional plaques of Sertoli cell ectoplasmic specializations. J Cell Sci 1996; 109:1229–1239.PubMedGoogle Scholar
  37. 37.
    Velichkova M, Guttman J, Warren C et al. A human homologue of Drosophila kelch associates with myosin-VIIa in specialized adhesion junctions. Cell Motil Cytoskeleton 2002; 51:147–164.PubMedCrossRefGoogle Scholar
  38. 38.
    Kai M, Irie M, Okutsu T et al. The novel dominant mutation Dspd leads to a severe spermiogenesis defect in mice. Biol Reprod 2004; 70:1213–1221.PubMedCrossRefGoogle Scholar
  39. 39.
    Hasson T, Walsh J, Cable J et al. Effects of shaker-1 mutations on myosin-VIIa protein and mRNA expression. Cell Motil Cytoskeleton 1997; 37:127–138.PubMedCrossRefGoogle Scholar
  40. 40.
    Vogl AW, Soucy LJ. Arrangement and possible function of actin filament bundles in ectoplasmic specializations of ground squirrel Sertoli cells. J Cell Biol 1985; 100:814–825.PubMedCrossRefGoogle Scholar
  41. 41.
    Guttman JA, Obinata T, Shima J et al. Nonmuscle cofilin is a component of tubulobulbar complexes in the testis. Biol Reprod 2004; 70; 805–812.PubMedCrossRefGoogle Scholar
  42. 42.
    Mulholland DJ, Dedhar S, Vogl AW. Rat seminiferous epithelium contains a unique junction (Ectoplasmic specialization) with signaling properties both of cell/cell and cell/matrix junctions. Biol Reprod 2001; 64:396–407.PubMedCrossRefGoogle Scholar
  43. 43.
    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; 64:1500–1508.PubMedCrossRefGoogle Scholar
  44. 44.
    Cheng CY, Silvestrini B, Grima J et al. Two new male contraceptives exert their effects by depleting germ cells prematurely from the testis. Biol Reprod 2001; 65:449–461.PubMedCrossRefGoogle Scholar
  45. 45.
    Cheng CY, Mruk D, Silvestrini B et al. AF-2364[1-(2,4-dichlorobenzyl)-1H-indazole-3-carbohydrazide] is a potential male contraceptive: A review of recent data. Contraception 2005; 72:251–261.PubMedCrossRefGoogle Scholar
  46. 46.
    O’Donnell L, McLachlan RI, Wreford NG et al. Testosterone withdrawal promotes stage-specific detachment of round spermatids from the rat seminiferous epithelium. Biol Reprod 1996; 55:895–901.PubMedCrossRefGoogle Scholar
  47. 47.
    Beardsley A, O’Donnell L. Characterization of normal spermiation and spermiation failure induced by hormone suppression in adult rats. Biol Reprod 2003; 68:1299–1307.PubMedCrossRefGoogle Scholar
  48. 48.
    Toyama Y, Hosoi I, Ichikawa S et al. β-estradiol 3-benzoate affects spermatogenesis in the adult mouse. Mol Cell Endocrinol 2001; 178:161–168.PubMedCrossRefGoogle Scholar
  49. 49.
    Wong CH, Xia W, Lee NP et al. Regulation of ectoplasmic specialization dynamics in the seminiferous epithelium by focal adhesion-associated proteins in testosterone-suppressed rat testes. Endocrinology 2005; 146:1192–1204.PubMedCrossRefGoogle Scholar
  50. 50.
    Zhang J, Wong CH, Xia X et al. Regulation of Sertoli-germ cell adherens junction dynamics via changes in protein-protein interactions of the N-cadherin-β-catenin protein complex which are possibly mediated by c-Src and myotubularin-related protein 2: An in vivo study using an androgen suppression model. Endocrinology 2005; 146:1268–1284.PubMedCrossRefGoogle Scholar
  51. 51.
    Kobielak A, Pasolli HA, Fuchs E. Mammalian formin-1 participates in adherens junctions and polymerization of linear actin cables. Nat Cell Biol 2004; 6:21–30.PubMedCrossRefGoogle Scholar
  52. 52.
    Franchi E, Camatini M. Morphological evidence for calcium stores at Sertoli-Sertoli and Sertoli-spermatid interrelations. Cell Biol Int Rep 1985; 9:441–446.PubMedCrossRefGoogle Scholar
  53. 53.
    Pelletier R, Trifaro JM, Carbajal ME et al. Calcium-dependent actin filament-severing protein scinderin levels and localization in bovine testis, epididymis, and spermatozoa. Biol Reprod 1999; 60:1128–1136.PubMedCrossRefGoogle Scholar
  54. 54.
    Guttman JA, Janmey P, Vogl AW. Gelsolin—evidence for a role in turnover of junction-related actin filaments in Sertoli cells. J Cell Sci 2002; 115:499–505.PubMedGoogle Scholar
  55. 55.
    Vaid K, Guttman J, Vogl AW. A reevaluation of gelsolin at ectoplasmic specializations in Sertoli cells—The influence of serum in blocking buffers on staining patterns. Mol Biol Cell 2004; 15:427a.Google Scholar
  56. 56.
    Witke W, Sharpe AH, Hartwig JH et al. Hemostatic, inflammatory, and fibroblast responses are blunted in mice lacking gelsolin. Cell 1995; 81:41–51.PubMedCrossRefGoogle Scholar
  57. 57.
    Russell LD, Goh JC, Rashed RM et al. 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; 39:105–118.PubMedCrossRefGoogle Scholar
  58. 58.
    Weber JE, Turner TT, Tung KS et al. Effects of cytochalasin D on the integrity of the Sertoli cell (blood-testis) barrier. Am J Anat 1988; 182:130–147.PubMedCrossRefGoogle Scholar
  59. 59.
    Russell L, Clermont Y. Anchoring device between Sertoli cells and late spermatids in rat seminiferous tubules. Anat Rec 1976; 185:259–278.PubMedCrossRefGoogle Scholar
  60. 60.
    Russell LD. Further observations on tubulobulbar complexes formed by late spermatids and Sertoli cells in the rat testis. Anat Rec 1979; 194:213–232.PubMedCrossRefGoogle Scholar
  61. 61.
    Guttman JA, Takai Y, Vogl AW. Evidence that tubulobulbar complexes in the seminiferous epithelium are involved with internalization of adhesion junctions. Biol Reprod 2004; 71:548–559.PubMedCrossRefGoogle Scholar
  62. 62.
    Russell LD. Spermatid-Sertoli tubulobulbar complexes as devices for elimination of cytoplasm from the head region late spermatids of the rat. Anat Rec 1979; 194:233–246.PubMedCrossRefGoogle Scholar
  63. 63.
    Russell LD. Deformities in the head region of late spermatids of hypophysectomized-hormone-treated rats. Anat Rec 1980; 197:21–31.PubMedCrossRefGoogle Scholar
  64. 64.
    Kierszenbaum AL, Tres LL. The acrosome-acroplaxome-manchette complex and the shaping of the spermatid head. Arch Histol Cytol 2004; 67:271–284.PubMedCrossRefGoogle Scholar
  65. 65.
    Lock JG, Stow JL. Rab11 in recycling endosomes regulates the sorting and basolateral transport of E-cadherin. Mol Biol Cell 2005; 16:1744–1755.PubMedCrossRefGoogle Scholar
  66. 66.
    Le TL, Yap AS, Stow JL. Recycling of E-cadherin: A potential mechanism for regulating cadherin dynamics. J Cell Biol 1999; 146:219–232.PubMedGoogle Scholar
  67. 67.
    Akhtar N, Hotchin NA. RAC1 regulates adherens junctions through endocytosis of E-cadherin. Mol Biol Cell 2001; 12:847–862.PubMedGoogle Scholar
  68. 68.
    Ivanov AI, Nusrat A, Parkos CA. Endocytosis of epithelial apical junctional proteins by a clathrin-mediated pathway into a unique storage compartment. Mol Biol Cell 2004; 15:176–188.PubMedCrossRefGoogle Scholar
  69. 69.
    Izumi G, Sakisaka T, Baba T et al. Endocytosis of E-cadherin regulated by Rac and Cdc42 small G proteins through IQGAP1 and actin filaments. J Cell Biol 2004; 166:237–248.PubMedCrossRefGoogle Scholar
  70. 70.
    Shen L, Turner JR. Actin depolymerization disrupts tight junctions via caveolae-mediated endocytosis. Mol Biol Cell 2005; 16:3919–3936.PubMedCrossRefGoogle Scholar
  71. 71.
    Utech M, Ivanov AI, Samarin SN et al. Mechanism of IFN-γ-induced endocytosis of tight junction proteins: Myosin II-dependent vacuolarization of the apical plasma membrane. Mol Biol Cell 2005; 16:5040–5052.PubMedCrossRefGoogle Scholar
  72. 72.
    Paterson AD, Parton RG, Ferguson C et al. Characterization of E-cadherin endocytosis in isolated MCF-7 and chinese hamster ovary cells: The initial fate of unbound E-cadherin. J Biol Chem 2003; 278:21050–21057.PubMedCrossRefGoogle Scholar
  73. 73.
    Gaietta G, Deerinck TJ, Adams SR et al. Multicolor and electron microscopic imaging of connexin trafficking. Science 2002; 296:503–507.PubMedCrossRefGoogle Scholar
  74. 74.
    Berthoud VM, Minogue PJ, Laing JG, et al. Pathways for degradation of connexins and gap junctions. Cardiovasc Res 2004; 62:256–267.PubMedCrossRefGoogle Scholar
  75. 75.
    Matsuda M, Kubo A, Furuse M et al. A peculiar internalization of claudins tight junction-specific adhesion molecules, during the intercellular movement of epithelial cells. J Cell Sci 2004; 117:1247–1257.PubMedCrossRefGoogle Scholar
  76. 76.
    Polak-Charcon S, Ben-Shaul Y. Degradation of tight junctions in HT29, a human colon adenocarcinoma cell line. J Cell Sci 1979; 35:393–402.PubMedGoogle Scholar
  77. 77.
    Risinger MA, Larsen WJ. Endocytosis of cell-cell junctions and spontaneous cell disaggregation in a cultured human ovarian adenocarcinoma. (COLO 316). Tissue Cell 1981; 13:413–430.PubMedCrossRefGoogle Scholar
  78. 78.
    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; 155:259–279.PubMedCrossRefGoogle Scholar
  79. 79.
    Ng T, Shima D, Squire A et al. PKCα regulates β1 integrin-dependent cell motility through association and control of integrin traffic. EMBO J 1999; 18:3909–3923.PubMedCrossRefGoogle Scholar
  80. 80.
    Le TL, Joseph SR, Yap AS et al. Protein kinase C regulates endocytosis and recycling of E-cadherin. Am J Physiol Cell Physiol 2002; 283:C489–499.PubMedGoogle Scholar
  81. 81.
    Russell LD, Saxena NK, Turner TT. Cytoskeletal involvement in spermiation and sperm transport. Tissue Cell 1989; 21:361–379.PubMedCrossRefGoogle Scholar
  82. 82.
    Coulombe PA, Wong P. Cytoplasmic intermediate filaments revealed as dynamic and multipurpose scaffolds. Nat Cell Biol 2004; 6:699–706.PubMedCrossRefGoogle Scholar
  83. 83.
    Fudge DS, Gardner KH, Forsyth VT et al. The mechanical properties of hydrated intermediate filaments: Insights from hagfish slime threads. Biophys J 2003; 85:2015–2027.PubMedCrossRefGoogle Scholar
  84. 84.
    Kreplak L, Bar H, Leterrier JF et al. Exploring the mechanical behavior of single intermediate filaments. J Mol Biol 2005; 354:569–577.PubMedCrossRefGoogle Scholar
  85. 85.
    Fuchs E, Cleveland DW. A structural scaffolding of intermediate filaments in health and disease. Science 1998; 279:514–519.PubMedCrossRefGoogle Scholar
  86. 86.
    Helfand BT, Chou YH, Shumaker DK et al. Intermediate filament proteins participate in signal transduction. Trends Cell Biol 2005; 15:568–570.PubMedCrossRefGoogle Scholar
  87. 87.
    Toivola DM, Tao GZ, Habtezion A et al. Cellular integrity plus: Organelle-related and protein-targeting functions of intermediate filaments. Trends Cell Biol 2005; 15:608–617.PubMedCrossRefGoogle Scholar
  88. 88.
    Lazarides E. Intermediate filaments as mechanical integrators of cellular space. Nature 1980; 283: 249–256.PubMedCrossRefGoogle Scholar
  89. 89.
    Worman HJ, Courvalin JC. Nuclear envelope, nuclear lamina, and inherited disease. Int Rev Cytol 2005; 246:231–279.PubMedCrossRefGoogle Scholar
  90. 90.
    Franke WW, Grund C, Schmid E. Intermediate-sized filaments present in Sertoli cells are of the vimentin type. Eur J Cell Biol 1979; 19:269–275.PubMedGoogle Scholar
  91. 91.
    Paranko J, Kallajoki M, Pelliniemi LJ et al. Transient coexpression of cytokeratin and vimentin in differentiating rat Sertoli cells. Dev Biol 1986; 117:35–44.PubMedCrossRefGoogle Scholar
  92. 92.
    Stosiek P, Kasper M, Karsten U. Expression of cytokeratins 8 and 18 in human Sertoli cells of immature and atrophic seminiferous tubules. Differentiation 1990; 43:66–70.PubMedCrossRefGoogle Scholar
  93. 93.
    Miettinen M, Virtanen I, Talerman A. Intermediate filament proteins in human testis and testicular germ-cell tumors. Am J Pathol 1985; 120:402–410.PubMedGoogle Scholar
  94. 94.
    Frojdman K, Pelliniemi LJ, Lendahl U et al. The intermediate filament protein nestin occurs transiently in differentiating testis of rat and mouse. Differentiation 1997; 61:243–249.PubMedGoogle Scholar
  95. 95.
    Moss SB, Burnham BL, Bellve AR. The differential expression of lamin epitopes during mouse spermatogenesis. Mol Reprod Dev 1993; 34:164–174.PubMedCrossRefGoogle Scholar
  96. 96.
    Vester B, Smith A, Krohne G et al. Presence of a nuclear lamina in pachytene spermatocytes of the rat. J Cell Sci 1993; 104:557–563.PubMedGoogle Scholar
  97. 97.
    Aumuller G, Steinbruck M, Krause W et al. Distribution of vimentin-type intermediate filaments in Sertoli cells of the human testis, normal and pathologic. Anat Embryol (Berl) 1988; 178:129–136.CrossRefGoogle Scholar
  98. 98.
    Getsios S, Huen AC, Green KJ. Working out the strength and flexibility of desmosomes. Nat Rev Mol Cell Biol 2004; 5:271–281.PubMedCrossRefGoogle Scholar
  99. 99.
    Nievers MG, Schaapveld RQ, Sonnenberg A. Biology and function of hemidesmosomes. Matrix Biol 1999; 18:5–17.PubMedCrossRefGoogle Scholar
  100. 100.
    Hahn BS, Labouesse M. Tissue integrity: Hemidesmosomes and resistance to stress. Curr Biol 2001; 11:R858–861.PubMedCrossRefGoogle Scholar
  101. 101.
    Russell L. Desmosome-like junctions between Sertoli and germ cells in the rat restis. Am J Anat 1977; 148:301–312.PubMedCrossRefGoogle Scholar
  102. 102.
    Johnson KJ, Boekelheide K. Dynamic testicular adhesion junctions are immunologically unique. II. Localization of classic cadherins in rat testis. Biol Reprod 2002; 66:992–1000.PubMedCrossRefGoogle Scholar
  103. 103.
    Johnson KJ, Boekelheide K. Dynamic testicular adhesion junctions are immunologically unique. I. Localization of p120 catenin in rat testis. Biol Reprod 2002; 66:983–991.PubMedCrossRefGoogle Scholar
  104. 104.
    Colucci-Guyon E, Portier MM, Dunia I et al. Mice lacking vimentin develop and reproduce without an obvious phenotype. Cell 1994; 79:679–694.PubMedCrossRefGoogle Scholar
  105. 105.
    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 Biol Cell 1996; 7:55a.Google Scholar
  106. 106.
    Allard EK, Johnson KJ, Boekelheide K. Colchicine disrupts the cytoskeleton of rat testis seminiferous epithelium in a stage-dependent manner. Biol Reprod 1993; 48:143–153.PubMedCrossRefGoogle Scholar
  107. 107.
    Goldstein LS, Yang Z. Microtubule-based transport systems in neurons: The, roles of kinesins and dyneins. Annu Rev Neurosci 2000; 23:39–71.PubMedCrossRefGoogle Scholar
  108. 108.
    Higuchi H, Endow SA. Directionality and processivity of molecular motors. Curr Opin Cell Biol 2002; 14:50–57.PubMedCrossRefGoogle Scholar
  109. 109.
    Kamal A, Goldstein LS. Principles of cargo attachment to cytoplasmic motor proteins. Curr Opin Cell Biol 2002; 14:63–68.PubMedCrossRefGoogle Scholar
  110. 110.
    Brinkley BR. Microtubule organizing centers. Annu Rev Cell Biol 1985; 1:145–172.PubMedCrossRefGoogle Scholar
  111. 111.
    Schroer TA, Sheetz MP. Functions of microtubule-based motors. Annu Rev Physiol 1991; 53:629–652.PubMedCrossRefGoogle Scholar
  112. 112.
    Hyman A, Karsenti E. The role of nucleation in patterning microtubule networks. J Cell Sci 1998; 111 (Pt 15): 2077–2083.PubMedGoogle Scholar
  113. 112.
    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; 13:349–367.PubMedCrossRefGoogle Scholar
  114. 114.
    Vogl AW, Linck RW, Dym M. Colchicine-induced changes in the cytoskeleton of the golden-mantled ground squirrel (Spermophilus lateralis) Sertoli cells. Am J Anat 1983; 168:99–108.PubMedCrossRefGoogle Scholar
  115. 115.
    Vogl AW. Changes in the distribution of microtubules in rat Sertoli cells during spermatogenesis. Anat Rec 1988; 222:34–41.PubMedCrossRefGoogle Scholar
  116. 116.
    Vogl AW, Lin YC, Dym M et al. Sertoli cells of the golden-mantled ground squirrel (Spermophilus lateralis): A model system for the study of shape change. Am J Anat 1983; 168:83–98.PubMedCrossRefGoogle Scholar
  117. 117.
    Wenz JR, Hess RA. Characterization of stage-specific tyrosinated α-tubulin immunoperoxidase staining patterns in Sertoli cells of rat seminiferous tubules by light microscopic image analysis. Tissue Cell 1998; 30:492–501.PubMedCrossRefGoogle Scholar
  118. 118.
    Redenbach DM, Vogl AW. Microtubule polarity in Sertoli cells: A model for microtubule-based spermatid transport. Eur J Cell Biol 1991; 54:277–290.PubMedGoogle Scholar
  119. 119.
    Redenbach DM, Boekelheide K. Microtubules are oriented with their minus-ends directed apically before tight junction formation in rat Sertoli cells. Eur J Cell Biol 1994; 65:246–257.PubMedGoogle Scholar
  120. 120.
    Vogl AW, Weis M, Pfeiffer DC. The perinuclear centriole-containing centrosome is not the major microtubule organizing center in Sertoli cells. Eur J Cell Biol 1995; 66:165–179.PubMedGoogle Scholar
  121. 121.
    Guttman J, Lee LE, Vogl AW. Evidence that gmma tubulin is located peripherally in Sertoli cells. FASEB J 2002; 16:A1101.Google Scholar
  122. 122.
    Fleming SL, Shank PR, Boekelheide K. ψ-Tubulin overexpression in Sertoli cells in vivo: I. Localization to sites of spermatid head attachment and alterations in Sertoli cell microtubule distribution. Biol Reprod 2003; 69:310–321.PubMedCrossRefGoogle Scholar
  123. 123.
    Hermo L, Oko R, Hecht NB. Differential post-translational modifications of microtubules in cells of the seminiferous epithelium of the rat: A light and electron microscope immunocytochemical study. Anat Rec 1991; 229:31–50.PubMedCrossRefGoogle Scholar
  124. 124.
    Lawrence CJ, Dawe RK, Christie KR et al. A standardized kinesin nomenclature. J Cell Biol 2004; 167:19–22.PubMedCrossRefGoogle Scholar
  125. 125.
    Miki H, Setou M, Kaneshiro K et al. All kinesin superfamily protein, KIF, genes in mouse and human. Proc Natl Acad Sci USA 2001; 98:7004–7011.PubMedCrossRefGoogle Scholar
  126. 126.
    Ross JL, Wallace K, Shuman H et al. Processive bidirectional motion of dynein-dynactin complexes in vitro. Nat Cell Biol 2006; 8:562–570.PubMedCrossRefGoogle Scholar
  127. 127.
    Vale RD. The molecular motor toolbox for intracellular transport. Cell 2003; 112:467–480.PubMedCrossRefGoogle Scholar
  128. 128.
    Goldstein LS, Philp AV. The road less traveled: Emerging principles of kinesin motor utilization. Annu Rev Cell Dev Biol 1999; 15:141–183.PubMedCrossRefGoogle Scholar
  129. 129.
    Hirokawa N. Kinesin and dynein superfamily proteins and the mechanism of organelle transport. Science 1998; 279:519–526.PubMedCrossRefGoogle Scholar
  130. 130.
    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; 107:1767–1776.PubMedCrossRefGoogle Scholar
  131. 131.
    Fawcett DW. Ultrastructure and function of the Sertoli cell. In: Greep RO, ed. Handbook of Physiology. 5 (7). Baltimore: Williams and Wilkins, 1975:21–55.Google Scholar
  132. 132.
    Hall ES, Hall SJ, Boekelheide K. 2,5-Hexanedione exposure alters microtubule motor distribution in adult rat testis. Fundam Appl Toxicol 1995; 24:173–182.PubMedCrossRefGoogle Scholar
  133. 133.
    Hall ES, Eveleth J, Jiang C et al. Distribution of the microtubule-dependent motors cytoplasmic dynein and kinesin in rat testis. Biol Reprod 1992; 46:817–828.PubMedCrossRefGoogle Scholar
  134. 134.
    Redenbach DM, Hall ES, Boekelheide K. Distribution of Sertoli cell microtubules, microtubule-dependent motors, and the Golgi apparatus before and after tight junction formation in developing rat testis. Microsc Res Tech 1995; 32:504–519.PubMedCrossRefGoogle Scholar
  135. 135.
    Miller MG, Mulholland DJ, Vogl AW. Rat testis motor proteins associated with spermatid translocation (dynein) and spermatid flagella (kinesin-II). Biol Reprod 1999; 60:1047–1056.PubMedCrossRefGoogle Scholar
  136. 136.
    Clermont Y, Perey B. The stages of the cycle of the seminiferous epithelium of the rat: Practical definitions in PA-Schiff-hematoxylin and hematoxylin-eosin stained sections. Rev Can Biol 1957; 16:451–462.PubMedGoogle Scholar
  137. 137.
    Clermont Y. Kinetics of spermatogenesis in mammals: Seminiferous epithelium cycle and spermatogonial renewal. Physiol Rev 1972; 52:198–236.PubMedGoogle Scholar
  138. 138.
    Perey B, Clermont Y, Leblond CP. The wave of the seminiferous epithelium in the rat. Am J Anat 1961; 108:47–77.CrossRefGoogle Scholar
  139. 139.
    Russell LD. Spermiation—The sperm release process: Ultrastructural observations and unresolved problems. In: Van Blerkom J, Motta PM, eds. Ultrastructure of Reproduction. Boston: Martinus Nijhoff, 1984:46–66.Google Scholar
  140. 140.
    Russell L. Observations on rat Sertoli ectoplasmic (‘junctional’) specializations in their association with germ cells of the rat testis. Tissue Cell 1977; 9:475–498.PubMedCrossRefGoogle Scholar
  141. 141.
    Redenbach DM, Boekelheide K, Vogl AW. Binding between mammalian spermatid-ectoplasmic specialization complexes and microtubules. Eur J Cell Biol 1992; 59:433–448.PubMedGoogle Scholar
  142. 142.
    Vogl AW. Spatially dynamic intercellular adhesion junction is coupled to a microtubule-based motility system: Evidence from an in vitro binding assay. Cell Motil Cytoskeleton 1996; 34:1–12.PubMedCrossRefGoogle Scholar
  143. 143.
    Beach SF, Vogl AW. Spermatid translocation in the rat seminiferous epithelium: Coupling membrane trafficking machinery to a junction plaque. Biol Reprod 1999; 60:1036–1046.PubMedCrossRefGoogle Scholar
  144. 144.
    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 (Pt 12):2167–2176.PubMedGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2009

Authors and Affiliations

  • A. Wayne Vogl
    • 1
  • Kuljeet S. Vaid
    • 1
  • Julian A. Guttman
    • 2
  1. 1.Department of Cellular and Physiological Sciences, Division of Anatomy and Cell Biology, Faculty of Medicine, Life Sciences CentreThe University of British ColumbiaVancouverCanada
  2. 2.Michael Smith LaboratoriesThe University of British ColumbiaVancouverCanada

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