Skip to main content
Log in

Regulation of testicular function by cell-to-cell interaction

  • Review Article
  • Andrology
  • Published:
Reproductive Medicine and Biology

Abstract

Cell-to-cell interactions in the testis play important roles in regulating testicular function. Investigating the mechanism of such interactions is essential to elucidate the cause of spermatogenic dysfunction and to create a new treatment.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Philips LS, Vassilopoulou-Sellin R. Somatomedins.N Engl J Med 1980;302: 371–380.

    Google Scholar 

  2. Steinberger E. Hormonal control of mammalian spermatogenesis.Physiol Rev 1971;51: 1–22.

    CAS  Google Scholar 

  3. Clermont Y. Kinetics of spermatogenesis in mammals: seminiferous epithelium cycle and spermatogonial renewal.Physiol Rev 1972;52: 198–236.

    PubMed  CAS  Google Scholar 

  4. Bellvé AR, Zheng W. Growth factors as autocrine and paracrine modulators of male gonadal functions.J Reprod Fertil 1989;85: 771–793.

    PubMed  Google Scholar 

  5. Le Magueresse B, Jégou B. Paracrine control of immature Sertoli cells by adult germ cells, in the rat (an in vitro study). Cell-cell interactions within the testis.Mol Cell Endocrinol 1988;58: 65–72.

    Article  PubMed  CAS  Google Scholar 

  6. Saez JM, Perrard SM, Chatelain PG, Tabone E, Rivarola MA. Paracrine regulation of testicular function.J Steroid Biochem 1987;27: 317–329.

    Article  PubMed  CAS  Google Scholar 

  7. Sharpe RM. Paracrine control of the testis.Clin Endocrinol Metab 1986;15: 185–207.

    Article  PubMed  CAS  Google Scholar 

  8. Sharpe RM. Regulation of spermatogenesis. In: Knobil E, Niell JD, eds.The Physiology of Reproduction, 2nd edn. New York: Raven Press, 1994; 1363–1434.

    Google Scholar 

  9. Skinner MK. Cell-cell interactions in the testis.Endocr Rev 1991;12: 45–77.

    PubMed  CAS  Google Scholar 

  10. Sertoli E. e lesistenza di particulari cellule ramificate nei canalicoli seminiferi dell’testicolo umno.Morgagni 1865;7: 31.

    Google Scholar 

  11. Aoki A, Fawcett DW. Impermeability of sertoli cell junctions to prolonged exposure to preoxidase.Andrologia 1975;7: 63–76.

    PubMed  CAS  Google Scholar 

  12. 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.

    PubMed  CAS  Google Scholar 

  13. Gilula NB, Fawcett DW, Aoki A. The Sertoli cell occluding junctions and gap junctions in mature and developing mammalian testis.Dev Biol 1976;50: 142–168.

    Article  PubMed  CAS  Google Scholar 

  14. Hagënas I, Ploën I, Ritzen EM, Ekwall H. Blood-testis barrier: maintained function of inter-Sertoli cell junctions in experimental cryptorchidism in the rat, as judged by a simple lanthanum-immersion technique.Andrologia 1977;9: 250–254.

    PubMed  Google Scholar 

  15. Neaves WB. Permeability of Sertoli cell tight junctions to lanthanum after ligation of ductus deferens and ductuli efferentes.J Cell Biol 1973;59: 559–572.

    Article  PubMed  CAS  Google Scholar 

  16. Russell LD, Peyterson RN. Sertoli cell junctions: morphological and functional correlates.Int Rev Cytol 1985;94: 177–211.

    Article  PubMed  CAS  Google Scholar 

  17. de Kretser DM, Kerr IB. The cytology of the testis. In: Knobil E, Neil I, eds.The Physiology of Reproduction. New York: Raven Press, 1988; 837–932.

    Google Scholar 

  18. Leblond CP, Clermont Y. Definition of the stages of the cycle of the seminiferous epithelium in the rat.Ann NY Acad Sci 1952;55: 548–573.

    Article  PubMed  CAS  Google Scholar 

  19. Grove BD, Preiffer DC, Allen S, Vogl AW. Immunofluorescence localization of vinculin in ectoplasmic (‘junctional’) specializations of rat Sertoli cells.Am J Anat 1990;188: 44–56.

    Article  PubMed  CAS  Google Scholar 

  20. Russell LD. Observations on rat Sertoli ectoplasmic (‘junctional’) specializations in their association with germ cells of the rat testis.Tissue Cell 1977;9: 475–498.

    Article  PubMed  CAS  Google Scholar 

  21. Russell LD. Further observations on tubulobulbar complexes formed by late spermatids and Sertoli cells in the rat testeis.Anat Rec 1979;194: 213–232.

    Article  PubMed  CAS  Google Scholar 

  22. Russell LD. Spermatid-Sertoli tubulobulbar complexes as devices for elimination of cytoplasm from the head region of late spermatids of the rat.Anat Rec 1979;194: 233–246.

    Article  PubMed  CAS  Google Scholar 

  23. Enders GC, Millette CF. Pachytene spermatocyte and round spermatid binding to Sertoli cells in vitro.J Cell Sci 1988;90: 105–114.

    PubMed  Google Scholar 

  24. McGinley DM, Posalasky Z, Porvaznik M, Russell L. Gap junctions between Sertoli and germ cells of rat seminiferous tubules.Tissue Cell 1979;11: 741–754.

    Article  PubMed  CAS  Google Scholar 

  25. Pelletier RM. Cyclic modulation of Sertoli cell junctional complexes in a seasonal breeder: the mink (Mustela vison).Am J Anat 1988;183: 68–102.

    Article  PubMed  CAS  Google Scholar 

  26. Russell LD, Tallon DM, Weber JE, Wong V, Petersen RN. Three-dimensional reconstruction of a rat stage V Sertoli cell: III. A study of specific cellular relationships.Am J Anat 1983;167: 181–192.

    Article  PubMed  CAS  Google Scholar 

  27. Russell L, Clermont Y. Anchoring device between Sertoli cells and the late spermatids in rat seminiferous tubules.Anat Rec 1976;185: 259–278.

    Article  PubMed  CAS  Google Scholar 

  28. Fawcett DW. Interactions between Sertoli cells and germ cells. In: Macini RE, Martini L, eds.Male Fertility and Sterility. London: Academic Press, 1974; 13–20.

    Google Scholar 

  29. Ziparo E, Geremia R, Russo MA, Stefanini M. Surface interaction in vitro between Sertoli cells and germ cells at stages of spermatogenesis.Am J Anat 1980;159: 385–388.

    Article  PubMed  CAS  Google Scholar 

  30. Ziparo E, Siracusa G, Palombi F, Russo MA, Stefanini M.The Cell Biology of the Testis. New York: Academic Press, 1981.

    Google Scholar 

  31. Grootegoed JA, Jansen R, van der Molen HJ. The role of glucose, pyruvate and lactate in ATP production by rat spermatocytes and spermatids.Biochim Biophys Acta 1984;767: 248–256.

    Article  PubMed  CAS  Google Scholar 

  32. Setchell BP. The movement of fluids and substances in the testis.Aust J Biol Sci 1987;39: 193–207.

    Google Scholar 

  33. Cheng CY, Mather JP, Byer AL, Bardin CW. Identification of hormonally responsive proteins in primary Sertoli cell culture medium by anion-exchange high performance liquid chromatography.Endocrinology 1986;118: 480–488.

    PubMed  CAS  Google Scholar 

  34. Kissinger C, Skinner MK, Griswold MD. Analysis of Sertoli cell-secreted proteins by two-dimensional gel electrophoresis.Biol Reprod 1982;27: 233–240.

    Article  PubMed  CAS  Google Scholar 

  35. Wilson RM, Griswold MD. Secreted proteins from rat Sertoli cells.Exp Cell Res 1979;123: 127–135.

    Article  PubMed  CAS  Google Scholar 

  36. Wright WW, Musto NA, Mather JP, Bardin CW. Sertoli cells secrete both testis specific and serum proteins.Proc Natl Acad Sci USA 1981;78: 7565–7569.

    Article  PubMed  CAS  Google Scholar 

  37. Lacroix M, Parvinen M, Fritz IF. Localization of testicular plasminogen activator in discrete portions (stage VII and VIII) of the seminiferous tubule.Biol Reprod 1981;25: 143–146.

    Article  PubMed  CAS  Google Scholar 

  38. Parvinen M. Regulation of the seminiferous epithelium.Endocri Rev 1982;3: 404–417.

    CAS  Google Scholar 

  39. Shabanowitz RB, Dephilip RM, Crowell JA, Tres LL, Kierszenbaum AL. Temporal appearance and cyclic behaviour of Sertoli cell-specific secretory proteins during the development of the rat seminiferous tubule.Biol Reprod 1986;35: 745–760.

    Article  PubMed  CAS  Google Scholar 

  40. Skinner MK. Secretion of growth factors and other regulatory factors. In: Russell LD, Griswold MD, eds.The Sertoli Cell. Clearwater: Cache River Press, 1993; 237–247.

    Google Scholar 

  41. Sylvester SR, Skinner MK, Griswold MD. A sulfated glycoprotein synthesized by Sertoli cells and by epididymal cells is a component of the sperm membrane.Biol Reprod 1984;31: 1087–1101.

    Article  PubMed  CAS  Google Scholar 

  42. Tres LL, Smith EP, Van Wyk JJ, Kierszenbaum AL. Immunoreactive sites and accumulation of somatomedin-C in rat Sertoli spermatogenic cell co-cultures.Exp Cell Res 1986;162: 33–50.

    Article  PubMed  CAS  Google Scholar 

  43. Parvinen M. Cyclic function of Sertoli cells. In: Russell LD, Griswold MD, eds.The Sertoli Cell. Clearwater: Cache River Press, 1993; 331–347.

    Google Scholar 

  44. Sharpe RM. Experimental evidence for Sertoli cell-germ cell and Sertoli-Leydig cell interactions. In: Russell LD, Griswold MD, eds.The Sertoli Cell. Clearwater: Cache River Press, 1993; 391–418.

    Google Scholar 

  45. Lubahn DBSMJ, Golding TS, Couse JF, Korach KS, Smithies O. Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene.Proc Natl Acad Sci USA 1993;90: 11162–11166.

    Article  PubMed  CAS  Google Scholar 

  46. Griswold MD. Unique aspects of the biochemistry and metabolism of Sertoli cells. In: Russell LD, Griswold MD, eds.The Sertoli Cell. Clearwater: Cache River Press, 1993; 485–492.

    Google Scholar 

  47. Jutte NH, Grootegoed JA, Rommerts FF, van der Molen HJ. Exogenous lactate is essential for metabolic activities in isolated rat spermatocytes and spermatids.J Reprod Fertil 1981;62: 399–405.

    Article  PubMed  CAS  Google Scholar 

  48. Jutte NH, Jansen R, Grootegoed JA, Rommerts FF, Clausen OP, van der Molen HJ. Regulation of survival of rat pachytene spermatocytes by lactate supply from Sertoli cells.J Reprod Fertil 1982;65: 431–438.

    PubMed  CAS  Google Scholar 

  49. Jutte NH, Jansen R, Grootegoed JA, Rommerts FF, van der Molen HJ. FSH stimulation of the production of pyruvate and lactate by rat Sertoli cells may be involved in hormonal regulation of spermatogenesis.J Reprod Fertil 1983;68: 219–226.

    PubMed  CAS  Google Scholar 

  50. Mita M, Hall PF. Metabolism of round spermatids from rat: lactate as the preferred substrate.Biol Reprod 1982;26: 445–455.

    Article  PubMed  CAS  Google Scholar 

  51. Fritz IB, Tung PS, Ailenberg M. Proteases and antiproteases in the seminiferous tubules. In: Russell LD, Griswold MD, eds.The Sertoli Cell. Clearwater: Cache River Press, 1993; 217–235.

    Google Scholar 

  52. Wright WW, Parvinen M, Musto NAet al. Identification of stage-specific proteins synthesized by rat seminiferous tubules.Biol Reprod 1983;29: 257–270.

    Article  PubMed  CAS  Google Scholar 

  53. Sylvester SR. Secretion of transport and binding proteins. In: Russell LD, Griswold MD, eds.The Sertoli Cell. Clearwater: Cache River Press, 1993; 201–216.

    Google Scholar 

  54. Holms SD, Bucci LR, Lipshultz LI, Smith RG. Transferrin binds specifically to pachytene spermatocytes.Endocrinology 1983;113: 1916–1918.

    Article  Google Scholar 

  55. Sylvester SR, Griswold MD. The testicular iron shuttle: a ‘nurse’ function of Sertoli cells.J Androl 1994;15: 381–385.

    PubMed  CAS  Google Scholar 

  56. Bernstein S. Hereditary hypotransferrinemia with hemosiderosis, a murine disorder resembling human atransferrinemia.J Lab Clin Med 1987;110: 690–705.

    PubMed  CAS  Google Scholar 

  57. Skinner MK. Sertoli cell-peritubular myoid cell interactions. In: Russell LD, Griswold MD, eds.The Sertoli Cell. Clearwater: Cache River Press, 1993; 477–483.

    Google Scholar 

  58. Vornberger W, Prins G, Musto NA, Suarez-Quian CA. Androgen receptor distribution in rat testis: new implications for androgen regulation of spermatogenesis.Endocrinology 1994;134: 2307–2316.

    Article  PubMed  CAS  Google Scholar 

  59. Sar M, Hall SH, Wilson EM, French FS. Androgen regulation of Sertoli cells. In: Russell LD, Griswold MD, eds.The Sertoli Cell. Clearwater: Cache River Press, 1993; 509–516.

    Google Scholar 

  60. Verhoeven G. Local control system within the testis. In: De Kretser DM, ed.The Testes. London: Baillière’s Clinical Endocrinology and Metabolism, 1992;6: 313.

    Google Scholar 

  61. Verhoeven G, Gailleau J. Testicular pertibular cells secrete a protein under androgen control that inhibits induction of aromatase activity in Sertoli cells.Endocrinoology 1988;123: 2100–2110.

    CAS  Google Scholar 

  62. Blanchard KT, Boekelheide K. Adenovirus-mediated gene transfer to rat testis in vivo.Biol Reprod 1997;56: 495–500.

    Article  PubMed  CAS  Google Scholar 

  63. Scobey M, Bertera S, Somers Jet al. Delivery of a cyclic adenosine 3′,5′-monophosphate response element-binding protein (creb) mutant to seminiferous tubules results in impaired spermatogenesis.Endocrinology 2001;142: 948–954.

    Article  PubMed  CAS  Google Scholar 

  64. Yamamoto H, Ochiya T, Tamamushi Set al. HST-l/FGF-4 gene activation induces spermatogenesis and prevents adriamycin-induced testicular toxicity.Oncogene 2002;21: 899–908.

    Article  PubMed  CAS  Google Scholar 

  65. Nakamura T, Nawa K, Ichihara A. Partial purification and characterization of hepatocyte growth factor from serum of hepatectomized rats.Biochem Biophys Res Commun 1984;122: 1450–1459.

    Article  PubMed  CAS  Google Scholar 

  66. Russel WE, Mcgowan JA, Bucher NL. Partial characterization of a hepatocyte growth factor from platelets.J Cell Physiol 1984;119: 183–192.

    Article  Google Scholar 

  67. Nakamura T, Nishizawa T, Hagiya Met al. Molecular cloning and expression of human hepatocyte growth factor.Nature 1989;342: 440–443.

    Article  PubMed  CAS  Google Scholar 

  68. Gherardi E, Gray J, Stoker Met al. Purification of scatter factor, a fibroblast-derived basic protein that modulates epithelial interactions and movement.Proc Natl Acad Sci USA 1989;86: 5844–5848.

    Article  PubMed  CAS  Google Scholar 

  69. Weidner KM, Arakaki N, Hartmann Get al. Evidence for the identity of human scatter factor and human hepatocyte growth factor.Proc Natl Acad Sci USA 1991;88: 7001–7005.

    Article  PubMed  CAS  Google Scholar 

  70. Wolf HK, Zarnagar R, Michalopoulos GK. Localization of hepatocyte growth factor in human and rat tissues: an immunohistochemical study.Hepatology 1991;14: 488–494.

    PubMed  CAS  Google Scholar 

  71. Depuydt CE, Zalata A, de Potter CRet al. The receptor encoded by the human C-MET oncogene is expressed in testicular tissue and on human spermatozoa.Mol Hum Reprod 1996;2: 2–8.

    Article  PubMed  CAS  Google Scholar 

  72. van der Wee K, Hofmann MC. An in vitro tubule assay identifies HGF as a morphogen for the formation of seminiferous tubules in the postnatal mouse testis.Exp Cell Res 1999;252: 175–185.

    Article  PubMed  Google Scholar 

  73. Catizone A, Ricci G, Galdieri M. Expression and functional role of hepatocyte growth factor receptor (C-MET) during postnatal rat testis development.Endocrinology 2001;142: 1828–1834.

    Article  PubMed  CAS  Google Scholar 

  74. Jegou B, Risbridger GP, de Kretser DM. Effects of experimental cryptorchidism on testicular function in adult rats.J Androl 1983;4: 88–94.

    PubMed  CAS  Google Scholar 

  75. Jegou B, Laws AO, de Kretser DM. The effect of cryptorchidism and subsequent orchidopexy on testicular function in adult rats.J Reprod Fertil 1983;69: 137–145.

    Article  PubMed  CAS  Google Scholar 

  76. Karpe B, Ploen L, Hagenas Let al. Recovery of testicular functions after surgical treatment of experimental cryptorchidism in the rat.Int J Androl 1981;4: 145–160.

    Article  PubMed  CAS  Google Scholar 

  77. Hall SJ, Bar-Chama N, Ta Set al. Direct exposure of mouse spermatogenic cells to high doses of adenovirus gene therapy vector does not result in germ cell transduction.Hum Gene Ther 2000;11: 1705–1712.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Masato Fujisawa.

About this article

Cite this article

Fujisawa, M. Regulation of testicular function by cell-to-cell interaction. Reprod Med Biol 5, 9–17 (2006). https://doi.org/10.1111/j.1447-0578.2006.00118.x

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1111/j.1447-0578.2006.00118.x

Key words

Navigation