Skip to main content
SpringerLink
Log in

Extracellular Matrix and Its Role in Spermatogenesis

  • Chapter
Molecular Mechanisms in Spermatogenesis

Part of the book series: Advances in Experimental Medicine and Biology ((volume 636))

Abstract

In adult mammalian testes, such as rats, Sertoli and germ cells at different stages of their development in the seminiferous epithelium are in close contact with the basement membrane, a modified form of extracellular matrix (ECM). In essence, Sertoli and germ cells in particular spermatogonia are “resting” on the basement membrane at different stages of the seminiferous epithelial cycle, relying on its structural and hormonal supports. Thus, it is not entirely unexpected that ECM plays a significant role in regulating spermatogenesis, particularly spermatogonia and Sertoli cells, and the blood-testis barrier (BTB) constituted by Sertoli cells since these cells are in physical contact with the basement membrane. Additionally, the basement membrane is also in close contact with the underlying collagen network and the myoid cell layers, which together with the lymphatic network, constitute the tunica propria. The seminiferous epithelium and the tunica propria, in turn, constitute the seminiferous tubule, which is the functional unit that produces spermatozoa via its interaction with Leydig cells in the interstitium. In short, the basement membrane and the underlying collagen network that create the acellular zone of the tunica propria may even facilitate cross-talk between the seminiferous epithelium, the myoid cells and cells in the interstitium. Recent studies in the field have illustrated the crucial role of ECM in supporting Sertoli and germ cell function in the seminiferous epithelium, including the BTB dynamics. In this chapter, we summarize some of the latest findings in the field regarding the functional role of ECM in spermatogenesis using the adult rat testis as a model. We also high light specific areas of research that deserve attention for investigators in the field.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. de Kretser DM, Kerr JB. The cytology of the testis. In: Knobil E, Neill J, eds. The Physiology of Reproduction. Raven Press, 1988:837–932.

    Google Scholar 

  2. Cheng CY, Mruk DD. Cell junction dynamics in the testis: Sertoli-germ cell interactions and male contraceptive development. Physiol Rev 2002; 82:825–874.

    CAS  PubMed  Google Scholar 

  3. 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.

    Article  CAS  PubMed  Google Scholar 

  4. Fawcett DW, Leak LV, Heidger PM. Electron microscopic observations on the structural components of the blood-testis barrier. J Reprod Fertil 1970; (Suppl 10):105–122.

    Google Scholar 

  5. 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.

    CAS  PubMed  Google Scholar 

  6. Dym M. The fine structure of the monkey (Macaca) Sertoli cell and its role in maintaining the blood-tesis barrier. Anat Rec 1973; 175:639–656.

    Article  CAS  PubMed  Google Scholar 

  7. Dym M. Basement membrane regulation of Sertoli cells. Endocr Rev 1994; 15:102–115.

    CAS  PubMed  Google Scholar 

  8. Siu MK, Cheng CY. Dynamic cross-talk between cells and the extracellular matrix in the testis. Bioessays 2004; 26:978–992.

    Article  CAS  PubMed  Google Scholar 

  9. Siu MK, Cheng CY. Extracellular matrix: Recent advances on its role in junction dynamics in the seminiferous epithelium during spermatogenesis. Biol Reprod 2004; 71:375–391.

    Article  CAS  PubMed  Google Scholar 

  10. Lehmann D, Temminck B, Da Rugna D et al. Role of immunological factors in male infertility. Immunohistochemical and serological evidence. Lab Invest 1987; 57:21–28.

    CAS  PubMed  Google Scholar 

  11. Salomon F, Saremaslani P, Jakob M et al. Immune complex orchitis in infertile men: Immunoelectron microscopy of abnormal basement membrane structures. Lab Invest 1982; 47:555–567.

    CAS  PubMed  Google Scholar 

  12. Li MW, Xia W, Mruk DD et al. Tumor necrosis factor α reversibly disrupts the blood-testis barrier and impairs Sertoli-germ cell adhesion in the seminiferous epithelium of adult rat testes. J Endocrinol 2006; 190:313–329.

    Article  CAS  PubMed  Google Scholar 

  13. Siu MK, Cheng CY. Interactions of proteases, protease inhibitors, and the β1 integrin/laminin γ3 protein complex in the regulation of ectoplasmic specialization dynamics in the rat testis. Biol Reprod 2004; 70:945–964.

    Article  CAS  PubMed  Google Scholar 

  14. Siu MK, Lee WM, Cheng CY. The interplay of collagen IV, tumor necrosis factor-α, gelatinase B (matrix metalloprotease-9), and tissue inhibitor of metalloproteases-1 in the basal lamina regulates Sertoli cell-tight junction dynamics in the rat testis. Endocrinology 2003; 144:371–387.

    Article  CAS  PubMed  Google Scholar 

  15. Siu MK, Mruk DD, Lee WM et al. Adhering junction dynamics in the testis are regulated by an interplay of β1-integrin and focal adhesion complex-associated proteins. Endocrinology 2003; 144:2141–2163.

    Article  CAS  PubMed  Google Scholar 

  16. Siu MK, Wong CH, Lee WM et al. Sertoli-germ cell anchoring junction dynamics in the testis are regulated by an interplay of lipid and protein kinases. J Biol Chem 2005; 280:25029–25047.

    Article  CAS  PubMed  Google Scholar 

  17. Hadley MA, Dym M. Immunocytochemistry of extracellular matrix in the lamina propria of the rat testis: Electron microscopic localization. Biol Reprod 1987; 37:1283–1289.

    Article  CAS  PubMed  Google Scholar 

  18. Lian G, Miller KA, Enders GC. Localization and synthesis of entactin in seminiferous tubules of the mouse. Biol Reprod 1992;47:316–325.

    Article  CAS  PubMed  Google Scholar 

  19. Vogl A, Pfeiffer D, Redenbach D et al. Sertoli cell cytoskeleton. In: Russell L, Griswold M, eds. The Sertoli Cell. Cache River Press, 1993:39–86.

    Google Scholar 

  20. Russell LD, Malone JP. A study of Sertoli-spermatid tubulobulbar complexes in selected mammals. Tissue Cell 1980; 12:263–285.

    Article  CAS  PubMed  Google Scholar 

  21. Guttman JA, Obinata T, Shima J et al. Non-muscle cofilin is a component of tubulobulbar complexes in the testis. Biol Reprod 2004; 70:805–812.

    Article  CAS  PubMed  Google Scholar 

  22. Russell L. Desmosome-like junctions between Sertoli and germ cells in the rat testis. Am J Anat 1977; 148:301–312.

    Article  CAS  PubMed  Google Scholar 

  23. Alberts B, Johnson A, Lewis J et al. Cell junctions, cell adhesion, and the extracellular matrix. Molecular Biology of the Cell. 4th ed., New York: Garland Science, 2002:1065–1126.

    Google Scholar 

  24. Pellertier R. The tight junctions in the testis, epididymis, and vas deferens. In: Cereijido M, Anderson J, eds. Tight Junctions CRC Press, 2001:599–628.

    Google Scholar 

  25. Timpl R, Brown JC. Supramolecular assembly of basement membranes. Bioessays 1996; 18:123–132.

    Article  CAS  PubMed  Google Scholar 

  26. Hudson BG, Reeders ST, Tryggvason K. Type IV collagen: Structure, gene organization, and role in human diseases: Molecular basis of Goodpasture and Alport syndromes and diffuse leiomyomatosis. J Biol Chem 1993; 268:26033–26036.

    CAS  PubMed  Google Scholar 

  27. Ortega N, Werb Z. New functional roles for non-collagenous domains of basement membrane collagens. J Cell Sci 2002; 115:4201–4214.

    Article  CAS  PubMed  Google Scholar 

  28. Davis CM, Papadopoulos V, Sommers CL et al. Differential expression of extracellular matrix components in rat Sertoli cells. Biol Reprod 1990; 43:860–869.

    Article  CAS  PubMed  Google Scholar 

  29. Enders GC, Kahsai TZ, Lian G et al. Developmental changes in seminiferous tubule extracellular matrix components of the mouse testis: α3(IV) collagen chain expressed at the initiation of spermatogenesis. Biol Reprod 1995; 53:1489–1499.

    Article  CAS  PubMed  Google Scholar 

  30. Frojdman K, Pelliniemi LJ, Virtanen I. Differential distribution of type IV collagen chains in the developing rat testis and ovary. Differentiation 1998; 63:125–130.

    CAS  PubMed  Google Scholar 

  31. Kahsai TZ, Enders GC, Gunwar S et al. Seminiferous tubule basement membrane: Composition and organization of type IV collagen chains, and the linkage of α3(IV) and α5(IV) chains. J Biol Chem 1997; 272:17023–17032.

    Article  CAS  PubMed  Google Scholar 

  32. Richardson LL, Kleinman HK, Dym M. Basement membrane gene expression by Sertoli and peritubular myoid cells in vitro in the rat. Biol Reprod 1995; 52:320–330.

    Article  CAS  PubMed  Google Scholar 

  33. Skinner MK, Tung PS, Fritz IB. Cooperativity between Sertoli cells and testicular peritubular cells in the production and deposition of extracellular matrix components. J Cell Biol 1985; 100:1941–1947.

    Article  CAS  PubMed  Google Scholar 

  34. Siu MK, Lee WM, Cheng CY. The interplay of collagen IV, tumor necrosis factor-α, gelatinase B (matrix metalloprotease-9) and tissue inhibitor of metalloproteases-1 in the basal lamina regulates Sertoli cell tight junction dynamics in the rat testis. Endocrinology 2003; 144:371–387.

    Article  CAS  PubMed  Google Scholar 

  35. Walsh SV, Hopkins AM, Nusrat A. Modulation of tight junction structure and function by cytokines. Adv Drug Deliv Rev 2000; 41:303–313.

    Article  CAS  PubMed  Google Scholar 

  36. Tartaglia LA, Goeddel DV. Two TNF receptors. Immunol Today 1992; 13:151–153.

    CAS  Google Scholar 

  37. De Cesaris P, Starace D, Starace G et al. Activation of Jun N-terminal kinase/stress-activated protein kinase pathway by tumor necrosis factor α leads to intercellular adhesion molecule-1 expression. J Biol Chem 1999; 274:28978–28982.

    Article  PubMed  Google Scholar 

  38. Pentikainen V, Erkkila K, Suomalainen L et al. TNFα downregulates the Fas ligand and inhibits germ cell apoptosis in the human testis. J Clin Endocrinol Metab 2001; 86:4480–4488.

    Article  CAS  PubMed  Google Scholar 

  39. Hong CY, Park JH, Ahn RS et al. Molecular mechanism of suppression of testicular steroidogenesis by proinflammatory cytokine tumor necrosis factor α. Mol Cell Biol 2004; 24:2593–2604.

    Article  CAS  PubMed  Google Scholar 

  40. Orth JM. Proliferation of Sertoli cells in fetal and postnatal rats: A quantitative auto radiographic study. Anat Rec 1982; 203:485–492.

    Article  CAS  PubMed  Google Scholar 

  41. Wang ZX, Wreford NG, de Kretser DM. Determination of Sertoli cell numbers in the developing rat testis by stereological methods. Int J Androl 1989; 12:58–64.

    Article  CAS  PubMed  Google Scholar 

  42. Weber JE, Russell LD, Wong V et al. Three-dimensional reconstruction of a rat stave V Sertoli cell. II. Morphometry of Sertoli-Sertoli and Sertoli-germ-cell relationships. Am J Anaet 1983; 167:163–179.

    Article  CAS  Google Scholar 

  43. Bartke A. Apoptosis of male germ cells, a generalized or a cell type-specific phenomenon? Endocrinology 1995; 136:3–4.

    Article  CAS  PubMed  Google Scholar 

  44. Clermont Y. The cycle of the seminiferous epithelium in man. Am J Anat 1963; 112:35–51.

    Article  CAS  PubMed  Google Scholar 

  45. Sinha Hikim AP, Swerdloff RS. Hormonal and genetic control of germ cell apoptosis in the testis. Rev Reprod 1999; 4:38–47.

    Article  CAS  PubMed  Google Scholar 

  46. Suominen JS, Wang Y, Kaipia A et al. Tumor necrosis factor-α (TNFα) promotes cell survival during spermatogenesis, and this effect can be blocked by infliximab, a TNF-α antagonist. Eur J Endocrinol 2004; 151:629–640.

    Article  CAS  PubMed  Google Scholar 

  47. Ren HP, Russell LD. Clonal development of interconnected germ cells in the rat and its relation-ship to the segmental and subsegmental organization of spermatogenesis. Am J Anat 1991; 192:121–128.

    Article  CAS  PubMed  Google Scholar 

  48. Fawcett DW. Intercellular bridges. Exp Cell Res 1961; 8:174–187.

    Article  PubMed  Google Scholar 

  49. Sternlicht MD, Werb Z. How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 2001; 17:463–516.

    Article  CAS  PubMed  Google Scholar 

  50. Tsilibary EC, Charonis AS, Reger LA et al. The effect of nonenzymatic glucosylation on the binding of the main noncollagenous NC1 domain to type IV collagen. J. Biol. Chem 1988; 263:4302–4308.

    CAS  PubMed  Google Scholar 

  51. Vogel W, Gish GD, Alves F et al. The discoidin domain receptor tyrosine kinases are activated by collagen. Mol Cell 1997; 1:13–23.

    Article  CAS  PubMed  Google Scholar 

  52. 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.

    Article  CAS  PubMed  Google Scholar 

  53. 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.

    Article  CAS  PubMed  Google Scholar 

  54. Lee NP, Mruk D, Lee WM et al. Is the cadherin/catenin complex a functional unit of cell-cell actin-based adherens junctions in the rat testis? Biol Reprod 2003; 68:489–508.

    Article  CAS  PubMed  Google Scholar 

  55. 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.

    Article  CAS  PubMed  Google Scholar 

  56. 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.

    Article  CAS  PubMed  Google Scholar 

  57. Yan HH, Cheng CY. Laminin α3 forms a complex with β3 and γ3 chains that serves as the ligand for α6β1-integrin at the apical ectoplasmic specialization in adult rat testes. J Biol Chem 2006; 281:17286–17303.

    Article  CAS  PubMed  Google Scholar 

  58. Sasaki T, Fassler R, Hohenester E. Laminin: The crux of basement membrane assembly. J Cell Biol 2004; 164:959–963.

    Article  CAS  PubMed  Google Scholar 

  59. Lee NP, Cheng CY. Protein kinases and adherens junction dynamics in the seminiferous epithelium of the rat testis. J Cell Physiol 2005; 202:344–360.

    Article  CAS  PubMed  Google Scholar 

  60. 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.

    Article  CAS  PubMed  Google Scholar 

  61. Palombi F, Salanova M, Tarone G et al. Distribution of β1 integrin subunit in rat seminiferous epithelium. Biol Reprod 1992; 47:1173–1182.

    Article  CAS  PubMed  Google Scholar 

  62. Giebel J, Loster K, Rune GM. Localization of integrin β1, α1, α5 and α9 subunits in the rat testis. Int J Androl 1997; 20:3–9.

    Article  CAS  PubMed  Google Scholar 

  63. Salanova M, Stefanini M, De Curtis I et al. Integrin receptor α6β1 is localized at specific sites of cell-to-cell contact in rat seminiferous epithelium. Biol Reprod 1995; 52:79–87.

    Article  CAS  PubMed  Google Scholar 

  64. 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.

    Article  CAS  PubMed  Google Scholar 

  65. Frojdman K, Pelliniemi LJ. Differential distribution of the α6 subunit of integrins in the development and sexual differentiation of the mouse testis. Differentiation 1994; 57:21–29.

    CAS  PubMed  Google Scholar 

  66. Juliano RL. Signal transduction by cell adhesion receptors and the cytoskeleton: Functions of integrins, cadherins, selectins, and immunoglobulin-superfamily members. Annu Rev Pharmacol Toxicol 2002; 42:283–323.

    Article  CAS  PubMed  Google Scholar 

  67. Mecham RP. Receptors for laminin on mammalian cells. FASEB J 1991; 5:2538–2546.

    CAS  PubMed  Google Scholar 

  68. Hallmann R, Horn N, Selg M et al. Expression and function of laminins in the embryonic and mature vasculature. Physiol Rev 2005; 85:979–1000.

    Article  CAS  PubMed  Google Scholar 

  69. Aumailley M, Bruckner-Tuderman L, Carter WG et al. A simplified laminin nomenclature. Matrix Biol 2005; 24:326–332.

    Article  CAS  PubMed  Google Scholar 

  70. Kuphal S, Bauer R, Bosserhoff AK. Integrin signaling in malignant melanoma. Cancer Metastasis Rev 2005; 24:195–222.

    Article  CAS  PubMed  Google Scholar 

  71. Carragher NO, Frame MC. Focal adhesion and action dynamics: A place where kinases and proteases meet to promote invasion. Trends Cell Biol 2004; 14:241–249.

    Article  CAS  PubMed  Google Scholar 

  72. Caswell PT, Norman JC. In tegrin trafficking and the control of cell migration. Traffic 2006; 7:14–21.

    Article  CAS  PubMed  Google Scholar 

  73. Koch M, Olson PF, Albus A et al. Characterization and expression of the laminin γ3 chain: A novel, nonbasement membrane-associated, laminin chain. J Cell Biol 1999; 145:605–618.

    Article  CAS  PubMed  Google Scholar 

  74. Longin J, Guillaumot P, Chauvin MA et al. MT1-MMP in rat testicular development and the control of Sertoli cell proMMP-2 actvation. J Cell Sci 2001; 114:2125–2134.

    CAS  PubMed  Google Scholar 

  75. 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.

    Article  CAS  PubMed  Google Scholar 

  76. 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.

    Article  CAS  PubMed  Google Scholar 

  77. Mruk DD, Wong CH, Silvestrini B et al. A male contraceptive targeting germ cell adhesion. Nat Med 2006; 12:1323–1328.

    Article  CAS  PubMed  Google Scholar 

  78. Koshikawa N, Giannelli G, Cirulli V et al. Role of cell surface metalloprotease MT1-MMP in epithelial cell migration over laminin-5. J Cell Biol 2000; 148:615–624.

    Article  CAS  PubMed  Google Scholar 

  79. Udayakumar TS, Chen ML, Bair EL et al. Membrane type-1-matrix metalloproteinase expressed by prostate carcinoma cells cleaves human laminin-5 beta3 chain and induces cell migration. Cancer Res 2003; 63:2292–2299.

    CAS  PubMed  Google Scholar 

  80. Giannelli G, Falk-Marzillier J, Schiraldi O et al. Induction of cell migration by matrix metalloprotease-2 cleavage of laminin-5. Science 1997; 227:225–228.

    Article  Google Scholar 

  81. Gilles C, Polette M, Coraux C et al. Contribution of MT1-MMP and of human laminin-5 γ2 chain degradation to mammary epithelial cell migration. J Cell Sci 2001; 114: 2967–2976.

    CAS  PubMed  Google Scholar 

  82. Siu MK, Cheng CY. Interactions of proteases, protease inhibitors, and the β1 integrin/laminin γ3 protein complex in the regulation of ectoplasmic specialization dynamics in the rat testis. Biol Reprod 2004; 70:945–964.

    Article  CAS  PubMed  Google Scholar 

  83. Wine RN, Chapin RE. Adhesion and signaling proteins spatiotemporally associated with spermiation in the rat. J Androl 1999; 20:198–213.

    CAS  PubMed  Google Scholar 

  84. 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.

    Article  CAS  PubMed  Google Scholar 

  85. 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.

    CAS  PubMed  Google Scholar 

  86. Maekawa M, Toyama Y, Yasuda M et al. Fyn tyrosine kinase in Sertoli cells is involved in mouse spermatogenesis. Biol Reprod 2002; 66:211–221.

    Article  CAS  PubMed  Google Scholar 

  87. Cohen LA, Guan JL. Mechanisms of focal adhesion kinase regulation. Curr Cancer Drug Targets 2005; 5:629–643.

    Article  CAS  PubMed  Google Scholar 

  88. McLean GW, Carragher NO, Avizienyte E et al. The role of focal-adhesion kinase in cancer—A new therapeutic opportunity. Nat Rev Cancer 2005; 5:505–515.

    Article  CAS  PubMed  Google Scholar 

  89. Parsons JT. Focal adhesion kinase: The first ten years. J Cell Sci 2003; 116:1409–1416.

    Article  CAS  PubMed  Google Scholar 

  90. Iwahara T, Akagi T, Fujitsuka Y et al. CrkII regulates focal adhesion kinase activation by making a complex with Crk-associated substrate, p130Cas. Proc Natl Acad Sci USA 2004;101:17693–17698.

    Article  CAS  PubMed  Google Scholar 

  91. Tsuda M, Tanaka S, Sawa H et al. Signaling adaptor protein v-Crk activates Rho and regulates cell motility in 3Y1 rat fibroblast cell line. Cell Growth Differ 2002; 13:131–139.

    CAS  PubMed  Google Scholar 

  92. Goldberg GS, Alexander DB, Pellicena P et al. Src phosphorylates Cas on tyrosine 253 to promote migration of transformed cells. J Biol Chem 2003; 278:46533–46540.

    Article  CAS  PubMed  Google Scholar 

  93. Shin NY, Dise RS, Schneider-Mergener J et al. Subsets of the major tyrosine phosphorylation sites in Crk-associated substrate (CAS) are sufficient to promote cell migration. J Biol Chem 2004; 279:38331–38337.

    Article  CAS  PubMed  Google Scholar 

  94. Gu J, Sumida Y, Sanzen N et al. Laminin-10/11 and fibronectin differentially regulated integrin-dependent Rho and Rac activation via p130Cas-CrkII-DOCK180 pathway. J Biol Chem 2001; 276:27090–27097.

    Article  CAS  PubMed  Google Scholar 

  95. Grimsley CM, Kinchen JM, Tosello-Trampont AC et al. Dock180 and ELMO1 proteins cooperate to promote evolutionarily conserved Rac-dependent cell migration. J Biol Chem 2004; 279:6087–6097.

    Article  CAS  PubMed  Google Scholar 

  96. 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.

    Article  CAS  PubMed  Google Scholar 

  97. Wang CQ, Mruk DD, Lee WM et al. Coxsackie and adenovirus receptor (CAR) is a product of Sertoli and germ cells in rat testes which is localized at the Sertoli-Sertoli and Sertoli-germ cell interface. Exp Cell Res 2007; 313:1373–1392.

    Article  CAS  PubMed  Google Scholar 

  98. Raschperger E, Thyberg J, Pettersson S et al. The coxsackie-and adenovirus receptor (CAR) is an in vivo marker for epithelial tight junctions, with a potential role in regulating permeability and tissue homeostasis. Exp Cell Res 2006; 312:1566–1580.

    Article  CAS  PubMed  Google Scholar 

  99. Mirza M, Hreinsson J, Strand ML et al. Coxsackievirus and adenovirus receptor (CAR) is expressed in male germ cells and forms a complex with the differentiation factor JAM-C in mouse testis. Exp Cell Res 2006; 312:817–830.

    Article  CAS  PubMed  Google Scholar 

  100. 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; 320–324.

    Google Scholar 

  101. Yan HH, Cheng CY. Laminin α3 forms a complex with α3 and γ3 chains that serves as the ligand for α6β1-integrin at the apical ectoplasmic specialization in adult rat testes. J Biol Chem 2006; 281:17286–17303.

    Article  CAS  PubMed  Google Scholar 

  102. Sasaki T, Fassler R, Hohenester E. Laminin: The crux of basement membrane assembly. J Cell Biol 2004; 164:959–963.

    Article  CAS  PubMed  Google Scholar 

  103. Lee NP, Cheng CY. Protein kinases and adherens junction dynamics in the seminiferous epithelium of the rat testis. J Cell Physiol 2005; 202:344–360.

    Article  CAS  PubMed  Google Scholar 

  104. 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.

    Article  CAS  PubMed  Google Scholar 

  105. Palombi F, Salanova M, Tarone G et al. Distribution of β1 integrin subunit in rat seminiferous epithelium. Biol Reprod 1992; 47:1173–1182.

    Article  CAS  PubMed  Google Scholar 

  106. Giebel J, Loster K, Rune GM. Localization of integrin β1, α1, α5 and α9 subunits in the rat testis. Int J Androl 1997; 20:3–9.

    Article  CAS  PubMed  Google Scholar 

  107. Salanova M, Stefanini M, De Curtis I et al. Integrin receptor α6β1 is localized at specific sites of cell-to-cell contact in rat seminiferous epithelium. Biol Reprod 1995; 52:79–87.

    Article  CAS  PubMed  Google Scholar 

  108. 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.

    Article  CAS  PubMed  Google Scholar 

  109. Frojdman K, Pelliniemi LJ. Differential distribution of the α6 subunit of integrins in the development and sexual differentiation of the mouse testis. Differentiation 1994; 57:21–29.

    CAS  PubMed  Google Scholar 

  110. Juliano RL. Signal transduction by cell adhesion receptors and the cytoskeleton: Functions of integrins, cadherins, selectins, and immunoglobulin-superfamily members. Annu Rev Pharmacol Toxicol 2002; 42:283–323.

    Article  CAS  PubMed  Google Scholar 

  111. Mecham RP. Receptors for laminin on mammalian cells. FASEB J 1991; 5:2538–2546.

    CAS  PubMed  Google Scholar 

  112. Hallmann R, Horn N, Selg M et al. Expression and function of laminins in the embryonic and mature vasculature. Physiol Rev 2005; 85:979–1000.

    Article  CAS  PubMed  Google Scholar 

  113. Aumailley M, Bruckner-Tuderman L, Carter WG et al. A simplified laminin nomenclature. Matrix Biol 2005; 24:326–332.

    Article  CAS  PubMed  Google Scholar 

  114. Kuphal S, Bauer R, Bosserhoff AK. Integrin signaling in malignant melanoma. Cancer Metastasis Rev 2005; 24:195–222.

    Article  CAS  PubMed  Google Scholar 

  115. Carragher NO, Frame MC. Focal adhesion and actin dynamics: A place where kinases and proteases meet to promote invasion. Trends Cell Biol 2004; 14:241–249.

    Article  CAS  PubMed  Google Scholar 

  116. Caswell PT, Norman JC. Integrin trafficking and the control of cell migration. Traffic 2006; 7:14–21.

    Article  CAS  PubMed  Google Scholar 

  117. Koch M, Olson PF, Albus A et al. Characterization and expression of the laminin β3 chain: A novel, nonbasement membrane-associated, laminin chain. J Cell Biol 1999; 145:605–618.

    Article  CAS  PubMed  Google Scholar 

  118. Longin J, Guillaumot P, Chauvin MA et al. MT1-MMP in rat testicular development and the control of Sertoli cell proMMP-2 activation. J Cell Sci 2001; 114:2125–2134.

    CAS  PubMed  Google Scholar 

  119. 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.

    Article  CAS  PubMed  Google Scholar 

  120. 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.

    Article  CAS  PubMed  Google Scholar 

  121. Mruk DD, Wong CH, Silvestrini B et al. A male contraceptive targeting germ cell adhesion. Nat Med 2006; 12:1323–1328.

    Article  CAS  PubMed  Google Scholar 

  122. Koshikawa N, Giannelli G, Cirulli V et al. Role of cell surface metalloprotease MT1-MMP in epithelial cell migration over laminin-5. J Cell Biol 2000; 148:615–624.

    Article  CAS  PubMed  Google Scholar 

  123. Udayakumar TS, Chen ML, Bair EL et al. Membrane type-1-matrix metalloproteinase expressed by prostate carcinoma cells cleaves human laminin-5 beta3 chain and induces cell migration. Cancer Res 2003; 63:2292–2299.

    CAS  PubMed  Google Scholar 

  124. Giannelli G, Falk-Marzillier J, Schiraldi O et al. Induction of cell migration by matrix metalloprotease-2 cleavage of laminin-5. Science 1997; 277:225–228.

    Article  CAS  PubMed  Google Scholar 

  125. Gilles C, Polette M, Coraux C et al. Contribution of MT1-MMP and of human laminin-5 β2 chain degradation to mammary epithelial cell migration. J Cell Sci 2001; 114:2967–2976.

    CAS  PubMed  Google Scholar 

  126. Siu MK, Cheng CY. Interactions of proteases, protease inhibitors, and the β1 integrin/laminin γ3 protein complex in the regulation of ectoplasmic specialization dynamics in the rat testis. Biol Reprod 2004; 70:945–964.

    Article  CAS  PubMed  Google Scholar 

  127. Wine RN, Chapin RE. Adhesion and signaling proteins spatiotemporally associated with spermiation in the rat. J Androl 1999; 20:198–213.

    CAS  PubMed  Google Scholar 

  128. 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.

    Article  CAS  PubMed  Google Scholar 

  129. 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.

    CAS  PubMed  Google Scholar 

  130. Maekawa M, Toyama Y, Yasuda M et al. Fyn tyrosine kinase in Sertoli cells is involved in mouse spermatogenesis. Biol Reprod 2002; 66:211–221.

    Article  CAS  PubMed  Google Scholar 

  131. Cohen LA, Guan JL. Mechanisms of focal adhesion kinase regulation. Curr Cancer Drug Targets 2005; 5:629–643.

    Article  CAS  PubMed  Google Scholar 

  132. McLean GW, Carragher NO, Avizienyte E et al. The role of focal-adhesion kinase in cancer—A new therapeutic opportunity. Nat Rev Cancer 2005; 5:505–515.

    Article  CAS  PubMed  Google Scholar 

  133. Parsons JT. Focal adhesion kinase: The first ten years. J Cell Sci 2003; 116:1409–1416.

    Article  CAS  PubMed  Google Scholar 

  134. Iwahara T, Akagi T, Fujitsuka Y et al. CrkII regulates focal adhesion kinase activation by making a complex with Crk-associated substrate, p130Cas. Proc Natl Acad Sci USA 2004; 101:17693–17698.

    Article  CAS  PubMed  Google Scholar 

  135. Tsuda M, Tanaka S, Sawa H et al. Signaling adaptor protein v-Crk activates Rho and regulates cell motility in 3Y1 rat fibroblast cell line. Cell Growth Differ 2002; 13:131–139.

    CAS  PubMed  Google Scholar 

  136. Goldberg GS, Alexander DB, Pellicena P et al. Src phosphorylates Cas on tyrosine 253 to promote migration of transformed cells. J Biol Chem 2003; 278:46533–46540.

    Article  CAS  PubMed  Google Scholar 

  137. Shin NY, Dise RS, Schneider-Mergener J et al. Subsets of the major tyrosine phosphorylation sites in Crk-associated substrate (CAS) are sufficient to promote cell migration. J Biol Chem 2004; 279:38331–38337.

    Article  CAS  PubMed  Google Scholar 

  138. Gu J, Sumida Y, Sanzen N et al. Laminin-10/11 and fibronectin differentially regulated integrin-dependent Rho and Rac activation via p130Cas-CrkII-DOCK180 pathway. J Biol Chem 2001; 276:27090–27097.

    Article  CAS  PubMed  Google Scholar 

  139. Grimsley CM, Kinchen JM, Tosello-Trampont AC et al. Dock180 and ELMO1 proteins cooperate to promote evolutionarily conserved Rac-dependent cell migration. J Biol Chem 2004; 279:6087–6097.

    Article  CAS  PubMed  Google Scholar 

  140. 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.

    Article  CAS  PubMed  Google Scholar 

  141. Wang CQ, Mruk DD, Lee WM et al. Coxsackie and adenovirus receptor (CAR) is a product of Sertoli and germ cells in rat testes which is localized at the Sertoli-Sertoli and Sertoli-germ cell interface. Exp Cell Res 2007; 313:1373–1392.

    Article  CAS  PubMed  Google Scholar 

  142. Raschperger E, Thyberg J, Pettersson S et al. The coxsackie-and adenovirus receptor (CAR) is an in vivo marker for epithelial tight junctions, with a potential role in regulating permeability and tissue homeostatis. Exp Cell Res 2006; 312:1566–1580.

    Article  CAS  PubMed  Google Scholar 

  143. Mirza M, Hreinsson J, Strand ML et al. Coxsackievirus and adenovirus receptor (CAR) is expressed in male germ cells and forms a complex with the differentiation factor JAM-C in mouse testis. Exp Cell Res 2006; 312:817–830.

    Article  CAS  PubMed  Google Scholar 

  144. 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; 320–324.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Pathology, Queen Mary Hospital, University of Hong Kong, Hong Kong, China

    Michelle K. Y. Siu

  2. Center for Biomedical Research, The Population Council, New York, New York, USA

    C. Yan Cheng

Authors
  1. Michelle K. Y. Siu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C. Yan Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michelle K. Y. Siu .

Editor information

Editors and Affiliations

  1. Center for Biomedical Research, The Population Council, New York, New York, USA

    C. Yan Cheng PhD

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Landes Bioscience and Springer Science+Business Media

About this chapter

Cite this chapter

Siu, M.K.Y., Cheng, C.Y. (2009). Extracellular Matrix and Its Role in Spermatogenesis. In: Cheng, C.Y. (eds) Molecular Mechanisms in Spermatogenesis. Advances in Experimental Medicine and Biology, vol 636. Springer, New York, NY. https://doi.org/10.1007/978-0-387-09597-4_5

Download citation

Publish with us

Policies and ethics

Search

Navigation