Spermatogenesis and Cycle of the Seminiferous Epithelium

Abstract

Spermatogenesis is a complex biological process of cellular transformation that produces male haploid germ cells from diploid spermatogonial stem cells. This process has been simplified morphologically by recognizing cellular associations or ‘stages’ and ‘phases’ of spermatogenesis, which progress through precisely timed and highly organized cycles. These cycles of spermatogenesis are essential for continuous sperm production, which is dependent upon numerous factors, both intrinsic (Sertoli and germ cells) and extrinsic (androgens, retinoic acids), as well as being species-specific.

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References

  1. 1.
    Hess R, França LR. History of the sertoli cell discovery. In: Griswold M, Skinner M, eds. Sertoli Cell Biology, New York: Academic Press, 2005.Google Scholar
  2. 2.
    Russell LD, Griswold MD, eds. The Sertoli Cell. Clearwater: Cache River Press, 1993.Google Scholar
  3. 3.
    Hess R, França LR. Structure of the Sertoli cell. In: Griswold M, Skinner M, eds. Sertoli Cell Biology. New York: Academic Press, 2005.Google Scholar
  4. 4.
    Russell LD, Ettlin RA, Sinha Hikim AP et al. Histological and Histopathological Evaluation of the Testis. Clearwater: Cache River Press, 1990.Google Scholar
  5. 5.
    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.PubMedCrossRefGoogle Scholar
  6. 6.
    Hess RA. Quantitative and qualitative characteristics of the stages and transitions in the cycle of the rat seminiferous epithelium: Light microscopic observations of perfusion-fixed and plastic-embedded testes. Biol Reprod 1990; 43(3):525–542.PubMedCrossRefGoogle Scholar
  7. 7.
    de Rooij DG, Russell LD. All you wanted to know about spermatogonia but were afraid to ask. J Androl 2000; 21(6):776–798.PubMedGoogle Scholar
  8. 8.
    Chiarini-Garcia H, Hornick JR, Griswold MD et al. Distribution of type A spermatogonia in the mouse is not random. Biol Reprod 2001; 65(4):1179–1185.PubMedCrossRefGoogle Scholar
  9. 9.
    Chiarini-Garcia H, Russell LD. High-resolution light microscopic characterization of mouse spermatogonia. Biol Reprod 2001; 65(4):1170–1178.PubMedCrossRefGoogle Scholar
  10. 10.
    Hess RA, Cooke PS, Hofmann MC et al. Mechanistic insights into the regulation of the spermatogonial sterm cell niche. Cell Cycle 2006; 5(11):1164–1170.PubMedGoogle Scholar
  11. 11.
    Cooke PS, Hess RA, Simon L et al. The transcription factor Ets-related molecule (ERM) is essential for spermatogonial stem cell maintenance and self-renewal. Anim Reprod 2006; 3(2):98–107.Google Scholar
  12. 12.
    Chen C, Ouyang W, Grigura V et al. ERM is required for transcriptional control of the spermatogonial stem cell niche. Nature 2005; 436(7053):1030–1034.PubMedCrossRefGoogle Scholar
  13. 13.
    Ryu BY, Orwig KE, Avarbock MR et al. Stem cell and niche development in the postnatal rat testis. Dev Biol 2003; 263(2):253–263.PubMedCrossRefGoogle Scholar
  14. 14.
    Brinster RL. Germline stem cell transplantation and transgenesis. Science 2002; 296(5576):2174–2176.PubMedCrossRefGoogle Scholar
  15. 15.
    Dobrinski I. Germ cell transplantation and testis tissue xenografting in domestic animals. Anim Reprod Sci 2005; 89(1–4):137–145.PubMedCrossRefGoogle Scholar
  16. 16.
    Ogawa T, Ohmura M, Ohbo K. The niche for spermatogonial stem cells in the mammalian testis. Int J Hematol 2005; 82(5):381–388.PubMedCrossRefGoogle Scholar
  17. 17.
    Oatley JM, Brinster RL. Spermatogonial stem cells. Methods Enzymol 2006; 419:259–282.PubMedCrossRefGoogle Scholar
  18. 18.
    Ryu BY, Orwig KE, Oatley JM et al. Effects of aging and niche microenvironment on spermatogonial stem cell self-renewal. Stem Cells 2006; 24(6):1505–1511.PubMedCrossRefGoogle Scholar
  19. 19.
    Russell L. Movement of spermatocytes from the basal to the adluminal compartment of the rat testis. Am J Anat 1977; 148(3):313–328.PubMedCrossRefGoogle Scholar
  20. 20.
    Russell LD. Sertoli-germ cell interactions: A review. Gamete Res 1980; 3:179–202.CrossRefGoogle Scholar
  21. 21.
    Hess RA. STAGES: Interactive Software on Spermatogenesis. 2.2 ed. Champaign: Vanguard Productions and Cache River Press, 1998.Google Scholar
  22. 22.
    Franca LR, Cardoso FM. Duration of spermatogenesis and sperm transit time through the epididymis in the Piau boar. Tissue Cell 1998; 30(5):573–582.PubMedCrossRefGoogle Scholar
  23. 23.
    Franca LR, Avelar GF, Almeida FF. Spermatogenesis and sperm transit through the epididymis in mammals with emphasis on pigs. Theriogenology 2005; 63(2):300–318.PubMedCrossRefGoogle Scholar
  24. 24.
    Leblond CP, Clermont Y. Spermiogenesis of rat, mouse, hamster and guinea pig as revealed by the “periodic acid-fuchsin sulfurous acid” technique. Am J Anat 1952; 90:167–215.PubMedCrossRefGoogle Scholar
  25. 25.
    Hess RA, Miller LA, Kirby JD et al. Immunoelectron microscopic localization of testicular and somatic cytochromes c in the seminiferous epithelium of the rat [published erratum appears in Biol Reprod 1993; 49(2):439]. Biol Reprod 1993; 48(6):1299–1308.PubMedCrossRefGoogle Scholar
  26. 26.
    Franca LR, Ye SJ, Ying L et al. Morphometry of rat germ cells during spermatogenesis. Anat Rec 1995; 241(2):181–204.PubMedCrossRefGoogle Scholar
  27. 27.
    Perey B, Clermont Y, Leblond C. The wave of the seminiferous epithelium in the rat. Am J Anat 1961; 108:47–77.CrossRefGoogle Scholar
  28. 28.
    Yoshida S, Takakura A, Ohbo K et al. Neurogenin3 delineates the earliest stages of spermatogenesis in the mouse testis. Dev Biol 2004; 269(2):447–458.PubMedCrossRefGoogle Scholar
  29. 29.
    Braydich-Stolle L, Nolan C, Dym M et al. Role of glial cell line-derived neurotrophic factor in germ-line stem cell fate. Ann NY Acad Sci 2005; 1061:94–99.PubMedCrossRefGoogle Scholar
  30. 30.
    Hofmann MC, Braydich-Stolle L, Dettin L et al. Immortalization of mouse germ line stem cells. Stem Cells 2005; 23(2):200–210.PubMedCrossRefGoogle Scholar
  31. 31.
    Hofmann MC, Braydich-Stolle L, Dym M. Isolation of male germ-line stem cells; influence of GDNF. Dev Biol 2005; 279(1):114–124.PubMedCrossRefGoogle Scholar
  32. 32.
    Kanatsu-Shinohara M, Miki H, Inoue K et al. Long-term culture of mouse male germline stem cells under serum-or feeder-free conditions. Biol Reprod 2005; 72(4):985–991.PubMedCrossRefGoogle Scholar
  33. 33.
    Kanatsu-Shinohara M, Toyokuni S, Shinohara T. Genetic selection of mouse male germline stem cells in vitro: Offspring from single stem cells. Biol Reprod 2005; 72(1):236–240.PubMedCrossRefGoogle Scholar
  34. 34.
    Ballow D, Meistrich ML, Matzuk M et al. Sohlh1 is essential for spermatogonial differentiation. Dev Biol 2006; 294(1):161–167.PubMedCrossRefGoogle Scholar
  35. 35.
    Braydich-Stolle L, Kostereva N, Dym M et al. Role of Src family kinases and N-Myc in spermatogonial stem cell proliferation. Dev Biol 2007; 304(1):34–45.PubMedCrossRefGoogle Scholar
  36. 36.
    de Rooij DG. Rapid expansion of the spermatogonial stem cell tool box. Proc Natl Acad Sci USA 2006; 103(21):7939–7940.PubMedCrossRefGoogle Scholar
  37. 37.
    Kanatsu-Shinohara M, Inoue K, Miki H et al. Clonal origin of germ cell colonies after spermatogonial transplantation in mice. Biol Reprod 2006; 75(1):68–74.PubMedCrossRefGoogle Scholar
  38. 38.
    Kanatsu-Shinohara M, Inoue K, Igonuki N et al. Leukemia inhibitory factor enhances formation of germ cell colonies in neonatal mouse testis culture. Biol Reprod 2007; 76(1):55–62.PubMedCrossRefGoogle Scholar
  39. 39.
    Kierszenbaum AL. Cell-cycle regulation and mammalian gametogenesis: A lesson from the unexpected. Mol Reprod Dev 2006; 73(8):939–942.PubMedCrossRefGoogle Scholar
  40. 40.
    Naughton CK, Jain S, Strickland AM et al. Glial cell-line derived neurotrophic factor-mediated RET signaling regulates spermatogonial stem cell fate. Biol Reprod 2006; 74(2):314–321.PubMedCrossRefGoogle Scholar
  41. 41.
    Oatley JM, Avarbock MR, Telaranta AI et al. Identifying genes important for spermatogonial stem cell self-renewal and survival. Proc Natl Acad Sci USA 2006; 103(25):9524–9529.PubMedCrossRefGoogle Scholar
  42. 42.
    Payne C, Braun RE. Glial cell line-derived neurotrophic factor maintains a POZ-itive influence on stem cells. Proc Natl Acad Sci USA 2006; 103(26):9751–9752.PubMedCrossRefGoogle Scholar
  43. 43.
    Yoshida S, Sukeno M, Nakagawa T et al. The first round of mouse spermatogenesis is a distinctive program that lacks the self-renewing spermatogonia stage. Development 2006; 133(8):1495–1505.PubMedCrossRefGoogle Scholar
  44. 44.
    Ebisuno S, Kohjimoto Y, Tamura M et al. Histological observations of the adhesion and endocytosis of calcium oxalate crystals in MDCK cells and in rat and human kidney. Urol Int 1997; 58(4):227–231.PubMedCrossRefGoogle Scholar
  45. 45.
    Ehmcke J, Joshi B, Hergenrother SD et al. Aging does not affect spermatogenic recovery after experimentally induced injury in mice. Reproduction 2007; 133(1):75–83.PubMedCrossRefGoogle Scholar
  46. 46.
    Nakagawa T, Nabeshima Y, Yoshida S. Functional identification of the actual and potential stem cell compartments in mouse spermatogenesis. Dev Cell 2007; 12(2):195–206.PubMedCrossRefGoogle Scholar
  47. 47.
    Aponte PM, van Bragt MP, de Rooij DG et al. Spermatogonial stem cells: Characteristics and experimental possibilities. Apmis 2005; 113(11–12):727–742.PubMedCrossRefGoogle Scholar
  48. 48.
    Brinster RL. Male germline stem cells: From mice to men. Science 2007; 316(5823):404–405.PubMedCrossRefGoogle Scholar
  49. 49.
    Clermont Y. Kinetics of spermatogenesis in mammals: Seminiferous epithelium cycle and spermatogonial renewal. Physiol Rev 1972; 52(1):198–236.PubMedGoogle Scholar
  50. 50.
    Franca LR, Russell LD. The testis of domestic mammals. In: Martinez-Garcia F, Regadera J, eds. Male Reproduction: A Multidisciplinary Overview. Madrid: Churchill Communications Europe España, 1998:197–219.Google Scholar
  51. 51.
    Hess RA, Schaeffer DJ, Eroschenko VP et al. Frequency of the stages in the cycle of the seminiferous epithelium in the rat. Biol Reprod 1990; 43(3):517–524.PubMedCrossRefGoogle Scholar
  52. 52.
    Franca LR, Ogawa T, Avarbock MR et al. Germ cell genotype controls cell cycle during spermatogenesis in the rat. Biol Reprod 1998; 59(6):1371–1377.PubMedCrossRefGoogle Scholar
  53. 53.
    Zeng W, Avelar GF, Rathi R et al. The length of the spermatogenic cycle is conserved in porcine and ovine testis xenografts. J Androl 2006; 27(4):527–533.PubMedCrossRefGoogle Scholar
  54. 54.
    Hess RA, Chen P. Computer tracking of germ cells in the cycle of the seminiferous epithelium and prediction of changes in cycle duration in animals commonly used in reproductive biology and toxicology. J Androl 1992; 13(3):185–190.PubMedGoogle Scholar
  55. 55.
    Creasy DM. Evaluation of testicular toxicity in safety evaluation studies: The appropriate use of spermatogenic staging. Toxicol Pathol 1997; 25(2):119–131.PubMedCrossRefGoogle Scholar
  56. 56.
    Creasy DM. Evaluation of testicular toxicology: A synopsis and discussion of the recommendations proposed by the Society of Toxicologic Pathology. Birth Defects Res Part B Dev Reprod Toxicol 2003; 68(5):408–415.CrossRefGoogle Scholar
  57. 57.
    Liu Y, Nusrat A, Schnell FJ et al. Human junction adhesion molecule regulates tight junction resealing in epithelia. J Cell Sci 2000; 113(Pt 13):2363–2374.PubMedGoogle Scholar
  58. 58.
    Vilela DAR, Silva SGB, Peixoto MTD et al. Spermatogenesis in teleost; Insights from the Nile tilapia (Oreochromis niloticus) model. Fish Physiol Biochem 2003; 28:187–190.CrossRefGoogle Scholar
  59. 59.
    Russell LD, Chiarini-Garcia H, Korsmeyer SJ et al. Bax-dependent spermatogonia apoptosis is required for testicular development and spermatogenesis. Biol Reprod 2002; 66(4):950–958.PubMedCrossRefGoogle Scholar
  60. 60.
    Franca LR, Russell LD, Cummins JM. Is human spermatogenesis uniquely poor? ARBS 2002; 4:19–42.Google Scholar
  61. 61.
    Johnson L, Chaturvedi PK, Williams JD. Missing generations of spermatocytes and spermatids in seminiferous epithelium contribute to low efficiency of spermatogenesis in humans. Biol Reprod 1992; 47(6):1091–1098.PubMedCrossRefGoogle Scholar
  62. 62.
    Sharpe R. Regulation of spermatogenesis. In: Knobil E, Neill J, eds. The Physiology of Reproduction. 2nd ed. New York: Raven Press, 1994:1363–1434.Google Scholar
  63. 63.
    De Gendt K, Atanassova N, Tan KA et al. Development and function of the adult generation of Leydig cells in mice with Sertoli cell-selective or total ablation of the androgen receptor. Endocrinology 2005; 146(9):4117–4126.PubMedCrossRefGoogle Scholar
  64. 64.
    Sharpe RM, McKinnell C, Kivlin C et al. Proliferation and functional maturation of Sertoli cells, and their relevance to disorders of testis function in adulthood. Reproduction 2003; 125(6):769–784.PubMedCrossRefGoogle Scholar
  65. 65.
    van Haaster LH, De Jong FH, Docter R et al. The effect of hypothyroidism on Sertoli cell proliferation and differentiation and hormone levels during testicular development in the rat. Endocrinology 1992; 131(3):1574–1576.PubMedCrossRefGoogle Scholar
  66. 66.
    van Haaster LH, de Jong FH, Docter R et al. High neonatal triiodothyronine levels reduce the period of Sertoli cell proliferation and accelerate tubular lumen formation in the rat testis, and increase serum inhibin levels. Endocrinology 1993; 133(2):755–760.PubMedCrossRefGoogle Scholar
  67. 67.
    Holsberger DR, Cooke PS. Understanding the role of thyroid hormone in Sertoli cell development: A mechanistic hypothesis. Cell Tissue Res 2005; 322(1):133–140.PubMedCrossRefGoogle Scholar
  68. 68.
    Holsberger DR, Kiesewetter SE, Cooke PS. Regulation of neonatal Sertoli cell development by thyroid hormone receptor alpha1. Biol Reprod 2005; 73(3):396–403.PubMedCrossRefGoogle Scholar
  69. 69.
    Cooke PS, Arambepola NK, Kirby JD et al. Thyroid hormone regulation of the development of the testis and its constituent cell types. Polish J Endocrinol 1997; 48(Suppl. 3):43–58.Google Scholar
  70. 70.
    Cooke PS, Hess RA, Kirby JD et al. Neonatal propylthiouracil (PTU) treatment as a model system for studying factors controlling testis growth and sperm production. In: Bartke A, ed. Function of Somatic Cells in the Testis. New York: Springer-Verlag, 1994:400–407.Google Scholar
  71. 71.
    Hess RA, Cooke PS, Bunick D et al. Adult testicular enlargement induced by neonatal hypothyroidism is accompanied by increased Sertoli and germ cell numbers. Endocrinol 1993; 132(6):2607–2613.CrossRefGoogle Scholar
  72. 72.
    Cooke PS, Porcelli J, Hess RA. Induction of increased testis growth and sperm production in adult rats by neonatal administration of the goitrogen propylthiouracil (PTU): The critical period. Biol Reprod 1992; 46(1):146–154.PubMedCrossRefGoogle Scholar
  73. 73.
    Cooke PS, Hess RA, Porcelli J et al. Increased sperm production in adult rats after transient neonatal hypothyroidism. Endocrinol 1991; 129(1):244–248.CrossRefGoogle Scholar
  74. 74.
    Holsberger DR, Buchold GM, Leal MC et al. Cell-cycle inhibitors p27Kip1 and p21Cip1 regulate murine Sertoli cell proliferation. Biol Reprod 2005; 72(6):1429–1436.PubMedCrossRefGoogle Scholar
  75. 75.
    Franca LR, Hess RA, Cooke PS et al. Neonatal hypothyroidism causes delayed Sertoli cell maturation in rats treated with propylthiouracil: Evidence that the Sertoli cell controls testis growth. Anat Rec 1995; 242(1):57–69.PubMedCrossRefGoogle Scholar
  76. 76.
    Sharpe RM, Turner KJ, McKinnell C et al. Inhibin B levels in plasma of the male rat from birth to adulthood: Effect of experimental manipulation of Sertoli cell number. J Androl 1999; 20(1):94–101.PubMedGoogle Scholar
  77. 77.
    Petersen C, Soder O. The sertoli cell—A hormonal target and’ super’ nurse for germ cells that determines testicular size. Horm Res 2006; 66(4):153–161.PubMedCrossRefGoogle Scholar
  78. 78.
    Tan KA, De Gendt K, Atanassova N et al. The role of androgens in sertoli cell proliferation and functional maturation: Studies in mice with total or Sertoli cell-selective ablation of the androgen receptor. Endocrinology 2005; 146(6):2674–2683.PubMedCrossRefGoogle Scholar
  79. 79.
    Schulz RW, Menting S, Bogerd J et al. Sertoli cell proliferation in the adult testis—Evidence from two fish species belonging to different orders. Biol Reprod 2005; 73(5):891–898.PubMedCrossRefGoogle Scholar
  80. 80.
    McCoard SA, Wise TH, Lunstra DD et al. Stereological evaluation of Sertoli cell ontogeny during fetal and neonatal life in two diverse breeds of swine. J Endocrinol 2003; 178(3):395–403.PubMedCrossRefGoogle Scholar
  81. 81.
    Neves ES, Chiarini-Garcia H, Franca LR. Comparative testis morphometry and seminiferous epithelium cycle length in donkeys and mules. Biol Reprod 2002; 67(1):247–255.PubMedCrossRefGoogle Scholar
  82. 82.
    Franca LR, Silva Jr VA, Chiarini-Garcia H et al. Cell proliferation and hormonal changes during postnatal development of the testis in the pig. Biol Reprod 2000; 63(6):1629–1636.PubMedCrossRefGoogle Scholar
  83. 83.
    Leal MC, Franca LR. The seminiferous epithelium cycle length in the black tufted-ear marmoset (Callithrix penicillata) is similar to humans. Biol Reprod 2006; 74(4):616–624.PubMedCrossRefGoogle Scholar
  84. 84.
    Almeida FF, Leal MC, Franca LR. Testis morphometry, duration of spermatogenesis, and spermatogenic efficiency in the wild boar (Sus scrofa scrofa). Biol Reprod 2006; 75(5):792–799.PubMedCrossRefGoogle Scholar
  85. 85.
    Kluin PM, Kramer MF, de Rooij DG. Spermatogenesis in the immature mouse proceeds faster than in the adult. Int J Androl 1982; 5(3):282–294.PubMedCrossRefGoogle Scholar
  86. 86.
    Sharpe RM. Sertoli cell endocrinology and signal transduction: Androgen regulation. In: Griswold M, Skinner M, eds. Sertoli Cell Biology. New York: Academic Press, 2005:199–216.CrossRefGoogle Scholar
  87. 87.
    Ventela S, Ohta H, Parvinen M et al. Development of the stages of the cycle in mouse seminiferous epithelium after transplantation of green fluorescent protein-labeled spermagonial stem cells. Biol Reprod 2002; 66(5):1422–1429.PubMedCrossRefGoogle Scholar
  88. 88.
    Ismail N, Morales C, Clermont Y. Role of spermatogonia in the stage-synchronization of the seminiferous epithelium in vitamin-A-deficient rats. Am J Anat 1990; 188(1):57–63.PubMedCrossRefGoogle Scholar
  89. 89.
    Morales CR, Griswold MD. Variations in the level of transferrin and SGP-2 mRNAs in Sertoli cells of vitamin A-deficient rats. Cell Tissue Res 1991; 263(1):125–130.PubMedCrossRefGoogle Scholar
  90. 90.
    Ismail N, Morales CR. Effects of vitamin A deficiency on the inter-Sertoli cell tight junctions and on the germ cell population. Microsc Res Tech 1992; 20(1):43–49.PubMedCrossRefGoogle Scholar
  91. 91.
    van Pelt AM, van Dissel-Emiliani FM, Gaemers IC et al. Characteristics of A spermatogonia and preleptotene spermatocytes in the vitamin A-deficient rat testis. Biol Reprod 1995; 53(3):570–578.PubMedCrossRefGoogle Scholar
  92. 92.
    Bartlett JM, Weinbauer GF, Nieschlag E. Stability of spermatogenic synchronization achieved by depletion and restoration of vitamin A in rats. Biol Reprod 1990; 42(4):603–612.PubMedCrossRefGoogle Scholar
  93. 93.
    Chung SS, Sung W, Wang X et al. Retinoic acid receptor alpha is required for synchronization of spermatogenic cycles and its absence results in progressive breakdown of the spermatogenic process. Dev Dyn 2004; 230(4):754–766.PubMedCrossRefGoogle Scholar
  94. 94.
    Weber JE, Russell LD, Wong V et al. Three-dimensional reconstruction of a rat stage V Sertoli cell: II. Morphometry of Sertoli-Sertoli and Sertoli-germ-cell relationships. Am J Anat 1983; 167(2):163–179.PubMedCrossRefGoogle Scholar
  95. 95.
    Brinster RL, Avarbock MR. Germline transmission of donor haplotype following spermatogonial transplantation. Proc Natl Acad Sci USA 1994; 91(24):11303–11307.PubMedCrossRefGoogle Scholar
  96. 96.
    Russell LD, Franca LR, Brinster RL. Ultrastructural observations of spermatogenesis in mice resulting from transplantation of mouse spermatogonia. J Androl 1996; 17(6):603–614.PubMedGoogle Scholar
  97. 97.
    Russell LD, Brinster RL. Ultrastructural observations of spermatogenesis following transplantation of rat testis cells into mouse seminiferous tubules. J Androl 1996; 17(6):615–627.PubMedGoogle Scholar
  98. 98.
    Ye SJ, Ying L, Ghosh S et al. Sertoli cell cycle: A re-examination of the structural changes during the cycle of the seminiferous epithelium of the rat. Anat Rec 1993; 237(2):187–198.PubMedCrossRefGoogle Scholar
  99. 99.
    Franca LR, Ghosh S, Ye SJ et al. Surface and surface-to-volume relationships of the Sertoli cell during the cycle of the seminiferous epithelium in the rat. Biol Reprod 1993; 49(6):1215–1228.PubMedCrossRefGoogle Scholar
  100. 100.
    McKinney TD, Desjardins C. Postnatal development of the testis, fighting behavior, and fertility in house mice. Biol Reprod 1973; 9(3):279–294.PubMedGoogle Scholar
  101. 101.
    Clermont Y, Perey B. Quantitative study of the cell population of the seminiferous tubules in immature rats. Am J Anat 1957; 100(2):241–267.PubMedCrossRefGoogle Scholar
  102. 102.
    Oakberg EF. Duration of spermatogenesis in the mouse and timing of stages of the cycle of the seminiferous epithelium. Am J Anat 1956; 99(3):507–516.PubMedCrossRefGoogle Scholar
  103. 103.
    van Haaster LH, de Rooij DG. Spermatogenesis is accelerated in the immature Djungarian and Chinese hamster and rat. Biol Reprod 1993; 49(6):1229–1235.PubMedCrossRefGoogle Scholar
  104. 104.
    Tan KA, Turner KJ, Saunders PT et al. Androgen regulation of stage-dependent cyclin D2 expression in Sertoli cells suggests a role in modulating androgen action on spermatogenesis. Biol Reprod 2005; 72(5):1151–1160.PubMedCrossRefGoogle Scholar
  105. 105.
    Zhang YQ, He XZ, Zhang JS et al. Stage-specific localization of transforming growth factor beta1 and beta3 and their receptors during spermatogenesis in men. Asian J Androl 2004; 6(2):105–109.PubMedGoogle Scholar
  106. 106.
    Xu J, Beyer AR, Walker WH et al. Developmental and stage-specific expression of Smad2 and Smad3 in rat testis. J Androl 2003; 24(2):192–200.PubMedGoogle Scholar
  107. 107.
    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(4):895–901.PubMedCrossRefGoogle Scholar
  108. 108.
    Sharpe RM, Maddocks S, Millar M et al. Testosterone and spermatogenesis: Identification of stage-specific, androgen-regulated proteins secreted by adult rat seminiferous tubules. J Androl 1992; 13(2):172–184.PubMedGoogle Scholar
  109. 109.
    Vihko KK, Toppari J, Parvinen M. Stage-specific regulation of plasminogen activator secretion in the rat seminiferous epithelium. Endocrinology 1987; 120(1):142–145.PubMedCrossRefGoogle Scholar
  110. 110.
    Liu D, Matzuk MM, Sung WK et al. Cyclin A1 is required for meiosis in the male mouse. Nat Genet 1998; 20(4):377–380.PubMedCrossRefGoogle Scholar
  111. 111.
    Shang E, Salazar G, Crowley TE et al. Identification of unique, differentiation stage-specific patterns of expression of the bromodomain-containing genes Brd2, Brd3, Brd4, and Brdt in the mouse testis. Genes Expr Patterns 2004; 4(5):513–519.CrossRefGoogle Scholar

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© Landes Bioscience and Springer Science+Business Media 2009

Authors and Affiliations

  1. 1.Reproductive Biology and Toxicology, Department of Veterinary BiosciencesUniversity of IllinoisUrbanaUSA
  2. 2.Department of MorphologyUniversidade Federal de Minas GeraisBelo HorizonteBrazil

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