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Androgen Receptor Roles in Spermatogenesis and Fertility: Lessons from Testicular Cell-Specific Androgen Receptor Knockout Mice

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Wang, Ruey-Sheng, Yeh, Shuyuan, Tzeng, Chii-Ruey, Chang, Chawnshang·2009·Endocrine Reviews
DOI 10.1210/er.2008-0025
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Abstract

Androgens are critical steroid hormones that determine the expression of the male phenotype, including the outward development of secondary sex characteristics as well as the initiation and maintenance of spermatogenesis. Their actions are mediated by the androgen receptor (AR), a member of the nuclear receptor superfamily. AR functions as a ligand-dependent transcription factor, regulating expression of an array of androgen-responsive genes. Androgen and the AR play important roles in male spermatogenesis and fertility. The recent generation and characterization of male total and conditional AR knockout mice from different laboratories demonstrated the necessity of AR signaling for both external and internal male phenotype development. As expected, the male total AR knockout mice exhibited female-typical external appearance (including a vagina with a blind end and a clitoris-like phallus), the testis was located abdominally, and germ cell development was severely disrupted, which was similar to a human complete androgen insensitivity syndrome or testicular feminization mouse. However, the process of spermatogenesis is highly dependent on autocrine and paracrine communication among testicular cell types, and the disruption of AR throughout an experimental animal cannot answer the question about how AR in each type of testicular cell can play roles in the process of spermatogenesis. In this review, we provide new insights by comparing the results of cell-specific AR knockout in germ cells, peritubular myoid cells, Leydig cells, and Sertoli cells mouse models that were generated by different laboratories to see the consequent defects in spermatogenesis due to AR loss in different testicular cell types in spermatogenesis. Briefly, this review summarizes these results as follows: 1) the impact of lacking AR in Sertoli cells mainly affects Sertoli cell functions to support and nurture germ cells, leading to spermatogenesis arrest at the diplotene primary spermatocyte stage prior to the accomplishment of first meiotic division; 2) the impact of lacking AR in Leydig cells mainly affects steroidogenic functions leading to arrest of spermatogenesis at the round spermatid stage; 3) the impact of lacking AR in the smooth muscle cells and peritubular myoid cells in mice results in similar fertility despite decreased sperm output as compared to wild-type controls; and 4) the deletion of AR gene in mouse germ cells does not affect spermatogenesis and male fertility. This review tries to clarify the useful information regarding how androgen/AR functions in individual cells of the testis. The future studies of detailed molecular mechanisms in these in vivo animals with cell-specific AR knockout could possibly lead to useful insights for improvements in the treatment of male infertility, hypogonadism, and testicular dysgenesis syndrome, and in attempts to create safe as well as effective male contraceptive methods.

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Research works printed but not linked: 113

  1. Chang, 1988, Molecular cloning of human and rat complementary DNA encoding androgen receptors., Science, 240, 324, 10.1126/science.3353726 · DOI · Paper page
  2. Chang, 1988, Structural analysis of complementary DNA and amino acid sequences of human and rat androgen receptors., Proc Natl Acad Sci USA, 85, 7211, 10.1073/pnas.85.19.7211 · DOI · Paper page
  3. Lubahn, 1988, Cloning of human androgen receptor complementary DNA and localization to the X chromosome., Science, 240, 327, 10.1126/science.3353727 · DOI · Paper page
  4. Griffin, 1992, Androgen resistance—the clinical and molecular spectrum, N Engl J, Med326, 611
  5. La Spada, 1991, Androgen receptor gene mutations in X-linked spinal and bulbar muscular atrophy., Nature, 352, 77, 10.1038/352077a0 · DOI · Paper page
  6. McPhaul, 1999, Molecular defects of the androgen receptor., J Steroid Biochem Mol Biol, 69, 315, 10.1016/S0960-0760(99)00050-3 · DOI
  7. Quigley, 1995, Androgen receptor defects: historical, clinical, and molecular perspectives., Endocr Rev, 16, 271
  8. Schultz, 1962, Male pseudohermaphroditism diagnosed with aid of sex chromatin technique., J Am Vet Med Assoc, 140, 241
  9. Bardin, 1970, Pseudohermaphrodite rat: end organ insensitivity to testosterone., Science, 167, 1136, 10.1126/science.167.3921.1136 · DOI
  10. Goldstein, 1972, Studies on the pathogenesis of the pseudohermaphroditism in the mouse with testicular feminization., J Clin Invest, 51, 1647, 10.1172/JCI106966 · DOI
  11. Meyers-Wallen, 1989, Testicular feminization in a cat., J Am Vet Med Assoc, 195, 631, 10.2460/javma.1989.195.05.631 · DOI
  12. Saez, 1994, Leydig cells: endocrine, paracrine, and autocrine regulation., Endocr Rev, 15, 574, 10.1210/edrv-15-5-574 · DOI · Paper page
  13. Vogl, 2000, Unique and multifunctional adhesion junctions in the testis: ectoplasmic specializations., Arch Histol Cytol, 63, 1, 10.1679/aohc.63.1 · DOI · Paper page
  14. Mruk, 2004, Sertoli-Sertoli and Sertoli-germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis., Endocr Rev, 25, 747, 10.1210/er.2003-0022 · DOI · Paper page
  15. Griswold, 1988, Protein secretions of Sertoli cells., Int Rev Cytol, 110, 133, 10.1016/S0074-7696(08)61849-5 · DOI · Paper page
  16. Waites, 1982, Physiological significance of fluid secretion in the testis and blood-testis barrier., Physiol Rev, 62, 624, 10.1152/physrev.1982.62.2.624 · doi:10.1152/physrev.1982.62.2.624
  17. Skinner, 1985, Testicular peritubular cells secrete a protein under androgen control that modulates Sertoli cell functions., Proc Natl Acad Sci USA, 82, 114, 10.1073/pnas.82.1.114 · DOI · Paper page
  18. Norton, 1989, Regulation of Sertoli cell function and differentiation through the actions of a testicular paracrine factor P-Mod-S., Endocrinology, 124, 2711, 10.1210/endo-124-6-2711 · doi:10.1210/endo-124-6-2711
  19. Romano, 2005, The contractile phenotype of peritubular smooth muscle cells is locally controlled: possible implications in male fertility., Contraception, 72, 294, 10.1016/j.contraception.2005.03.009 · doi:10.1016/j.contraception.2005.03.009
  20. Skinner, 1989, Regulation of Sertoli cell differentiated function: testicular transferrin and androgen-binding protein expression., Endocrinology, 124, 3015, 10.1210/endo-124-6-3015 · doi:10.1210/endo-124-6-3015
  21. Anthony, 1989, Analysis of the androgen receptor in isolated testicular cell types with a microassay that uses an affinity ligand., Endocrinology, 125, 2628, 10.1210/endo-125-5-2628 · DOI
  22. Sar, 1990, Immunohistochemical localization of the androgen receptor in rat and human tissues., Endocrinology, 127, 3180, 10.1210/endo-127-6-3180 · DOI · Paper page
  23. Kimura, 1993, Immunocytochemical localization of androgen receptor with polyclonal antibody in paraffin-embedded human tissues., J Histochem Cytochem, 41, 671, 10.1177/41.5.8468448 · DOI · Paper page
  24. Bremner, 1994, Immunohistochemical localization of androgen receptors in the rat testis: evidence for stage-dependent expression and regulation by androgens., Endocrinology, 135, 1227, 10.1210/endo.135.3.8070367 · doi:10.1210/endo.135.3.8070367 · Paper page
  25. Vornberger, 1994, Androgen receptor distribution in rat testis: new implications for androgen regulation of spermatogenesis., Endocrinology, 134, 2307, 10.1210/endo.134.5.8156934 · doi:10.1210/endo.134.5.8156934 · Paper page
  26. Zhou, 1996, Immunohistochemical localization of androgen receptor in mouse testicular germ cells during fetal and postnatal development., Anat Rec, 245, 509, 10.1002/(SICI)1097-0185(199607)245:3<509::AID-AR7>3.0.CO;2-M · DOI
  27. Janssen, 1994, Immunohistochemical detection of the androgen receptor with monoclonal antibody F39.4 in routinely processed, paraffin- embedded human tissues after microwave pre-treatment., J Histochem Cytochem, 42, 1169, 10.1177/42.8.8027537 · DOI
  28. Arenas, 2001, Androgen receptor (AR), estrogen receptor-α (ER-α) and estrogen receptor-β (ER-β) expression in the testis of the newt, Triturus marmoratus marmoratus, during the annual cycle., J Anat, 199, 465, 10.1046/j.1469-7580.2001.19940465.x · DOI
  29. Solakidi, 2005, Estrogen receptors α and β (ERα and ERβ) and androgen receptor (AR) in human sperm: localization of ERβ and AR in mitochondria of the midpiece., Hum Reprod, 20, 3481, 10.1093/humrep/dei267 · DOI · Paper page
  30. Merlet, 2007, Male fetal germ cells are targets for androgens that physiologically inhibit their proliferation., Proc Natl Acad Sci USA, 104, 3615, 10.1073/pnas.0611421104 · DOI
  31. Aquila, 2007, Human sperm express a functional androgen receptor: effects on PI3K/AKT pathway., Hum Reprod, 22, 2594, 10.1093/humrep/dem243 · DOI
  32. Warikoo, 1986, Interactions among motility, fertilizing ability, and testosterone binding on spermatozoa of bonnet monkey (Macaca radiata)., Arch Androl, 16, 135, 10.3109/01485018608986933 · DOI
  33. Galena, 1974, Progesterone and androgen receptors in non-flagellate germ cells of the rat testis., J Endocrinol, 63, 223, 10.1677/joe.0.0630223 · doi:10.1677/joe.0.0630223
  34. Grootegoed, 1977, Absence of a nuclear androgen receptor in isolated germinal cells of rat testis., Mol Cell Endocrinol, 9, 159, 10.1016/0303-7207(77)90117-4 · DOI
  35. Suarez-Quian, 1999, Androgen receptor distribution in adult human testis., J Clin Endocrinol Metab, 84, 350
  36. Van Roijen, 1995, Androgen receptor immunoexpression in the testes of subfertile men., J Androl, 16, 510, 10.1002/j.1939-4640.1995.tb00571.x · DOI
  37. Pelletier, 2000, Localization of oestrogen receptor α, oestrogen receptor β and androgen receptors in the rat reproductive organs., J Endocrinol, 165, 359, 10.1677/joe.0.1650359 · DOI · Paper page
  38. Yeh, 2002, Generation and characterization of androgen receptor knockout (ARKO) mice: an in vivo model for the study of androgen functions in selective tissues., Proc Natl Acad Sci USA, 99, 13498, 10.1073/pnas.212474399 · DOI · Paper page
  39. Matsumoto, 2003, Androgen receptor functions from reverse genetic models., J Steroid Biochem Mol Biol, 85, 95, 10.1016/S0960-0760(03)00231-0 · DOI
  40. Holt, 1993, A novel phage λ replacement Cre-lox vector that has automatic subcloning capabilities., Gene, 133, 95, 10.1016/0378-1119(93)90230-Z · doi:10.1016/0378-1119(93)90230-z
  41. Chang, 2004, Infertility with defective spermatogenesis and hypotestosteronemia in male mice lacking the androgen receptor in Sertoli cells., Proc Natl Acad Sci USA, 101, 6876, 10.1073/pnas.0307306101 · DOI · Paper page
  42. De Gendt, 2004, A Sertoli cell-selective knockout of the androgen receptor causes spermatogenic arrest in meiosis., Proc Natl Acad Sci USA, 101, 1327, 10.1073/pnas.0308114100 · DOI · Paper page
  43. Holdcraft, 2004, Androgen receptor function is required in Sertoli cells for the terminal differentiation of haploid spermatids., Development, 131, 459, 10.1242/dev.00957 · DOI · Paper page
  44. Wang, 2006, Androgen receptor in Sertoli cell is essential for germ cell nursery and junctional complex formation in mouse testes., Endocrinology, 147, 5624, 10.1210/en.2006-0138 · DOI · Paper page
  45. Xu, 2007, Infertility with defective spermatogenesis and steroidogenesis in male mice lacking androgen receptor in Leydig cells., Endocrine, 32, 96, 10.1007/s12020-007-9015-0 · DOI · Paper page
  46. Zhang, 2006, Oligozoospermia with normal fertility in male mice lacking the androgen receptor in testis peritubular myoid cells., Proc Natl Acad Sci USA, 103, 17718, 10.1073/pnas.0608556103 · DOI
  47. Tsai, 2006, Differential effects of spermatogenesis and fertility in mice lacking androgen receptor in individual testis cells., Proc Natl Acad Sci USA, 103, 18975, 10.1073/pnas.0608565103 · DOI · Paper page
  48. Weusten, 1987, Early time sequence in pregnenolone metabolism to testosterone in homogenates of human and rat testis., Endocrinology, 120, 1909, 10.1210/endo-120-5-1909 · DOI
  49. Fevold, 1989, Rat P450(17 α) from testis: characterization of a full-length cDNA encoding a unique steroid hydroxylase capable of catalyzing both Δ4- and Δ5-steroid-17,20-lyase reactions., Mol Endocrinol, 3, 968, 10.1210/mend-3-6-968 · DOI · Paper page
  50. Zhang, 1995, Serine phosphorylation of human P450c17 increases 17,20-lyase activity: implications for adrenarche and the polycystic ovary syndrome., Proc Natl Acad Sci USA, 92, 10619, 10.1073/pnas.92.23.10619 · DOI · Paper page
  51. Baker, 1999, Expression of 3β-hydroxysteroid dehydrogenase type I and type VI isoforms in the mouse testis during development., Eur J Biochem, 260, 911, 10.1046/j.1432-1327.1999.00245.x · DOI
  52. Sriraman, 2003, Evaluation of relative roles of LH and FSH in regulation of differentiation of Leydig cells using an ethane 1,2-dimethylsulfonate-treated adult rat model., J Endocrinol, 176, 151, 10.1677/joe.0.1760151 · doi:10.1677/joe.0.1760151
  53. Tong, 2004, Aberrant cholesterol transport and impaired steroidogenesis in Leydig cells lacking estrogen sulfotransferase., Endocrinology, 145, 2487, 10.1210/en.2003-1237 · DOI
  54. Huhtaniemi, 1992, Fetal Leydig cells: cellular origin, morphology, life span, and special functional features., Proc Soc Exp Biol Med, 201, 125, 10.3181/00379727-201-43493 · DOI · Paper page
  55. O'Shaughnessy, 2006, The foetal Leydig cell—differentiation, function and regulation., Int J Androl, 29, 90, 10.1111/j.1365-2605.2005.00555.x · DOI
  56. Payne, 1982, LH receptors and steroidogenesis in distinct populations of Leydig cells., Ann NY Acad Sci, 383, 174, 10.1111/j.1749-6632.1982.tb23168.x · doi:10.1111/j.1749-6632.1982.tb23168.x
  57. Tilmann, 2002, Cellular and molecular pathways regulating mammalian sex determination., Recent Prog Horm Res, 57, 1, 10.1210/rp.57.1.1 · DOI
  58. Vergouwen, 1991, Proliferative activity of gonocytes, Sertoli cells and interstitial cells during testicular development in mice., J Reprod Fertil, 93, 233, 10.1530/jrf.0.0930233 · DOI · Paper page
  59. Dong, 2007, Gene expression during development of fetal and adult Leydig cells., Ann NY Acad Sci, 1120, 16, 10.1196/annals.1411.016 · DOI
  60. Vergouwen, 1993, Postnatal development of testicular cell populations in mice., J Reprod Fertil, 99, 479, 10.1530/jrf.0.0990479 · DOI · Paper page
  61. O'Shaughnessy, 2002, Changes in Leydig cell gene expression during development in the mouse., Biol Reprod, 66, 966, 10.1095/biolreprod66.4.966 · DOI · Paper page
  62. Mendis-Handagama, 2001, Differentiation of the adult Leydig cell population in the postnatal testis., Biol Reprod, 65, 660, 10.1095/biolreprod65.3.660 · DOI · Paper page
  63. O'Shaughnessy, 2005, Neuroendocrine regulation of Leydig cell development., Ann NY Acad Sci, 1061, 109, 10.1196/annals.1336.013 · DOI
  64. Teerds, 1998, Development of the adult-type Leydig cell population in the rat is affected by neonatal thyroid hormone levels., Biol Reprod, 59, 344, 10.1095/biolreprod59.2.344 · doi:10.1095/biolreprod59.2.344
  65. Ariyaratne, 2000, Effects of thyroid hormone on Leydig cell regeneration in the adult rat following ethane dimethane sulphonate treatment., Biol Reprod, 63, 1115, 10.1095/biolreprod63.4.1115 · DOI
  66. Abney, 1999, The potential roles of estrogens in regulating Leydig cell development and function: a review., Steroids, 64, 610, 10.1016/S0039-128X(99)00041-0 · DOI · Paper page
  67. Hardy, 1990, Differentiation of Leydig cell precursors in vitro: a role for androgen., Endocrinology, 127, 488, 10.1210/endo-127-1-488 · doi:10.1210/endo-127-1-488
  68. Murphy, 1994, Abnormal Leydig cell development at puberty in the androgen-resistant Tfm mouse., Endocrinology, 135, 1372, 10.1210/endo.135.4.7925099 · doi:10.1210/endo.135.4.7925099
  69. Jones, 2003, Altered circulating hormone levels, endothelial function and vascular reactivity in the testicular feminised mouse., Eur J Endocrinol, 148, 111, 10.1530/eje.0.1480111 · DOI
  70. O'Shaughnessy, 2002, Failure of normal adult Leydig cell development in androgen-receptor-deficient mice., J Cell Sci, 115, 3491, 10.1242/jcs.115.17.3491 · DOI
  71. Blackburn, 1973, Testicular feminization in the mouse: studies of Leydig cell structure and function., Biol Reprod, 9, 9, 10.1093/biolreprod/9.1.9 · DOI
  72. De Gendt, 2005, Development and function of the adult generation of Leydig cells in mice with Sertoli cell-selective or total ablation of the androgen receptor., Endocrinology, 146, 4117, 10.1210/en.2005-0300 · DOI
  73. Morris, 1963, Further observations on the syndrome, “testicular feminization.”, Am J Obstet Gynecol, 87, 731
  74. Savage, 1978, Endocrine studies in male pseudohermaphroditism in childhood and adolescence., Clin Endocrinol (Oxf), 8, 219, 10.1111/j.1365-2265.1978.tb01498.x · DOI
  75. Hutson, 1997, Anatomical and functional aspects of testicular descent and cryptorchidism., Endocr Rev, 18, 259
  76. Tong, 1996, Does testosterone diffuse down the Wolffian duct during sexual differentiation?, J Urol, 155, 2057, 10.1016/S0022-5347(01)66107-X · doi:10.1016/s0022-5347(01)66107-x
  77. Ivell, 2003, The molecular basis of cryptorchidism., Mol Hum Reprod, 9, 175, 10.1093/molehr/gag025 · DOI
  78. Foresta, 2008, Role of hormones, genes, and environment in human cryptorchidism., Endocr Rev, 29, 560, 10.1210/er.2007-0042 · DOI · Paper page
  79. Klonisch, 2004, Molecular and genetic regulation of testis descent and external genitalia development., Dev Biol, 270, 1, 10.1016/j.ydbio.2004.02.018 · DOI · Paper page
  80. Hutson, 1986, Testicular feminization: a model for testicular descent in mice and men., J Pediatr Surg, 21, 195, 10.1016/S0022-3468(86)80830-2 · DOI · Paper page
  81. Sharpe, 2003, Proliferation and functional maturation of Sertoli cells, and their relevance to disorders of testis function in adulthood., Reproduction, 125, 769, 10.1530/rep.0.1250769 · DOI · Paper page
  82. Johnson, 1984, Quantification of the human Sertoli cell population: its distribution, relation to germ cell numbers, and age-related decline., Biol Reprod, 31, 785, 10.1095/biolreprod31.4.785 · DOI · Paper page
  83. Orth, 1988, Evidence from Sertoli cell-depleted rats indicates that spermatid number in adults depends on numbers of Sertoli cells produced during perinatal development., Endocrinology, 122, 787, 10.1210/endo-122-3-787 · DOI · Paper page
  84. Baker, 2001, Role of gonadotrophins in regulating numbers of Leydig and Sertoli cells during fetal and postnatal development in mice., Reproduction, 122, 227, 10.1530/rep.0.1220227 · DOI · Paper page
  85. Johnston, 2004, Regulation of Sertoli cell number and activity by follicle-stimulating hormone and androgen during postnatal development in the mouse., Endocrinology, 145, 318, 10.1210/en.2003-1055 · DOI · Paper page
  86. Holsberger, 2005, Understanding the role of thyroid hormone in Sertoli cell development: a mechanistic hypothesis., Cell Tissue Res, 322, 133, 10.1007/s00441-005-1082-z · DOI · Paper page
  87. Hill, 2004, Intratesticular androgen levels, androgen receptor localization, and androgen receptor expression in adult rat Sertoli cells., Biol Reprod, 71, 1348, 10.1095/biolreprod.104.029249 · DOI
  88. McKinnell, 2001, Comparison of androgen receptor and oestrogen receptor β immunoexpression in the testes of the common marmoset (Callithrix jacchus) from birth to adulthood: low androgen receptor immunoexpression in Sertoli cells during the neonatal increase in testosterone concentrations., Reproduction, 122, 419, 10.1530/rep.0.1220419 · DOI
  89. Majdic, 1995, Immunolocalisation of androgen receptor to interstitial cells in fetal rat testes and to mesenchymal and epithelial cells of associated ducts., J Endocrinol, 147, 285, 10.1677/joe.0.1470285 · DOI
  90. You, 1998, Androgen receptor expression in the testes and epididymides of prenatal and postnatal Sprague-Dawley rats., Endocrine, 9, 253, 10.1385/ENDO:9:3:253 · DOI
  91. Warren, 1973, Testosterone in the fetal rat testis., Biol Reprod, 8, 560, 10.1093/biolreprod/8.5.560 · DOI
  92. Feldman, 1978, Developmental pattern of testosterone synthesis by fetal rat testes in response to luteinizing hormone., Endocrinology, 102, 999, 10.1210/endo-102-4-999 · DOI
  93. Zhou, 2005, Androgen-regulated transcripts in the neonatal mouse testis as determined through microarray analysis., Biol Reprod, 72, 1010, 10.1095/biolreprod.104.035915 · DOI
  94. Atanassova, 2005, Evidence that androgens and oestrogens, as well as follicle-stimulating hormone, can alter Sertoli cell number in the neonatal rat., J Endocrinol, 184, 107, 10.1677/joe.1.05884 · DOI
  95. Mu, 2006, Gene expression profiling of androgen receptor antagonists in the rat fetal testis reveals few common gene targets., J Biochem Mol Toxicol, 20, 7, 10.1002/jbt.20110 · DOI
  96. Tan, 2005, 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, 146, 2674, 10.1210/en.2004-1630 · DOI · Paper page
  97. Singh, 1995, Induction of spermatogenesis by androgens in gonadotropin-deficient (hpg) mice., Endocrinology, 136, 5311, 10.1210/endo.136.12.7588276 · doi:10.1210/endo.136.12.7588276 · Paper page
  98. Singh, 1996, The effects of recombinant FSH on testosterone-induced spermatogenesis in gonadotrophin-deficient (hpg) mice., J Androl, 17, 382, 10.1002/j.1939-4640.1996.tb01804.x · DOI
  99. Haywood, 2003, Sertoli and germ cell development in hypogonadal (hpg) mice expressing transgenic follicle-stimulating hormone alone or in combination with testosterone., Endocrinology, 144, 509, 10.1210/en.2002-220710 · DOI · Paper page
  100. Ghosh, 1991, Further observations of stage-specific effects seen after short-term hypophysectomy in the rat., Tissue Cell, 23, 613, 10.1016/0040-8166(91)90018-O · DOI
  101. Kerr, 1992, Testosterone and FSH have independent, synergistic and stage-dependent effects upon spermatogenesis in the rat testis., Cell Tissue Res, 268, 179, 10.1007/BF00338067 · doi:10.1007/bf00338067
  102. Franca, 1998, Hormonal regulation of spermatogenesis in the hypophysectomized rat: quantitation of germ-cell population and effect of elimination of residual testosterone after long-term hypophysectomy., J Androl, 19, 335, 10.1002/j.1939-4640.1998.tb02012.x · DOI
  103. Hannema, 2006, Testicular development in the complete androgen insensitivity syndrome., J Pathol, 208, 518, 10.1002/path.1890 · DOI · Paper page
  104. Denolet, 2006, The effect of a Sertoli cell-selective knockout of the androgen receptor on testicular gene expression in prepubertal mice., Mol Endocrinol, 20, 321, 10.1210/me.2005-0113 · DOI
  105. Eacker, 2007, Transcriptional profiling of androgen receptor (AR) mutants suggests instructive and permissive roles of AR signaling in germ cell development., Mol Endocrinol, 21, 895, 10.1210/me.2006-0113 · DOI
  106. McLachlan, 1994, Effects of testosterone on spermatogenic cell populations in the adult rat., Biol Reprod, 51, 945, 10.1095/biolreprod51.5.945 · doi:10.1095/biolreprod51.5.945
  107. O'Donnell, 1994, Testosterone promotes the conversion of round spermatids between stages VII and VIII of the rat spermatogenic cycle., Endocrinology, 135, 2608, 10.1210/endo.135.6.7988449 · doi:10.1210/endo.135.6.7988449
  108. Hales, 1987, Testosterone inhibits cAMP-induced de novo synthesis of Leydig cell cytochrome P-450(17 α) by an androgen receptor-mediated mechanism., J Biol Chem, 262, 11200, 10.1016/S0021-9258(18)60944-5 · DOI
  109. Lyon, 1975, Normal spermatozoa from androgen-resistant germ cells of chimaeric mice and the role of androgen in spermatogenesis., Nature, 258, 620, 10.1038/258620a0 · DOI · Paper page
  110. Johnston, 2001, Murine germ cells do not require functional androgen receptors to complete spermatogenesis following spermatogonial stem cell transplantation., Endocrinology, 142, 2405, 10.1210/endo.142.6.8317 · DOI
  111. Justrabo, 1978, A complete form of testicular feminisation syndrome; a light and electron microscopy study., J Pathol, 126, 165, 10.1002/path.1711260305 · doi:10.1002/path.1711260305
  112. Rutgers, 1991, The androgen insensitivity syndrome (testicular feminization): a clinicopathologic study of 43 cases., Int J Gynecol Pathol, 10, 126, 10.1097/00004347-199104000-00002 · DOI · Paper page
  113. Shamblott, 1998, Derivation of pluripotent stem cells from cultured human primordial germ cells., Proc Natl Acad Sci USA, 95, 13726, 10.1073/pnas.95.23.13726 · DOI · Paper page

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Metadata

Authors
Wang, R.-S., Yeh, S., Tzeng, C.-R., & Chang, C.
Venue
Endocrine Reviews
Publisher
The Endocrine Society
Published
2009-04-01
Volume
30
Issue
2
Pages
119-132
ISSN
  • 0163-769X (ISSN-L)
  • 1945-7189
DOI
10.1210/er.2008-0025
OpenAlex
W2061564710
Cited by
465
References
11
FWCI
31.62
Type
journal article
Language
en
Open access
green

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Wang, R.-S., Yeh, S., Tzeng, C.-R., & Chang, C. (2009). Androgen Receptor Roles in Spermatogenesis and Fertility: Lessons from Testicular Cell-Specific Androgen Receptor Knockout Mice. Endocrine Reviews. https://doi.org/10.1210/er.2008-0025

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Bibliographic data: Semantic Scholar, OpenAlex, Crossref.

Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).

Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.