Is the adult sertoli cell terminally differentiated?

Biology of Reproduction

Volumn 87, Issue 1, 2012, Pages 13-

  Tarulli, Gerard A ^a,b   Stanton, Peter G ^a,b   Meachem, Sarah J ^a,b  

^a HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b MONASH UNIVERSITY   (Australia)

Author keywords

Differentiation; Hormone; Male infertility; Mechanisms of hormone action; Sertoli cells

Indexed keywords

ACTIVIN RECEPTOR 2; ANDROGEN RECEPTOR; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 2; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE; COMPLEMENT; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYTOKINE; ENDOTOXIN; FOLLISTATIN; FOLLITROPIN; FOLLITROPIN RECEPTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; HORMONE; INHIBIN; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 6; OSTEOGENIC PROTEIN 1; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN KINASE C; PROTEIN P21; SMAD PROTEIN; TESTOSTERONE; THYROID HORMONE; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; UNINDEXED DRUG; CELL CYCLE PROTEIN;

ADULTHOOD; APOPTOSIS; ARTICLE; AUTOCRINE EFFECT; BIRTH; CELL CYCLE REGULATION; CELL DIFFERENTIATION; CELL FUNCTION; CELL JUNCTION; CELL MATURATION; CELL POPULATION; CELL PROLIFERATION; CELL SIZE; CLINICAL RESEARCH; CYTOKINE PRODUCTION; DEVELOPMENTAL STAGE; FERTILITY; GENE OVEREXPRESSION; GERM CELL; HAMSTER; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MALE INFERTILITY; MOLECULAR BIOLOGY; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PUBERTY; SERTOLI CELL; SIGNAL TRANSDUCTION; SPERMATOGENESIS; TESTIS; ANIMAL; BIOLOGICAL MODEL; CYTOLOGY; MALE; PHYSIOLOGY; REVIEW; SEASON; SEXUAL MATURATION;

CRICETINAE; MUS;

ANIMALS; AUTOCRINE COMMUNICATION; CELL CYCLE PROTEINS; CELL DIFFERENTIATION; CELL PROLIFERATION; HUMANS; INTERCELLULAR JUNCTIONS; MALE; MODELS, BIOLOGICAL; PARACRINE COMMUNICATION; PUBERTY; SEASONS; SERTOLI CELLS; SEXUAL MATURATION; SIGNAL TRANSDUCTION; SPERMATOGENESIS;

EID: 84869222564     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.111.095091     Document Type: Article

References (163)

1. Zhang Z, Shao S, Meistrich M. The radiation-induced block in spermatogonial differentiation is due to damage to the somatic environment, not the germ cells. J Cell Physiol 2007; 211:149-158.
2. Orth JM, Gunsalus GL, Lamperti AA. Evidence from Sertoli celldepleted rats indicates that spermatid number in adults depends on numbers of Sertoli cells produced during perinatal development. Endocrinology 1988; 122:787-794.
3. Ross AJ, Capel B. Signaling at the crossroads of gonad development. Trends Endocrinol Metab 2005; 16:19-25.
4. Hacker A, Capel B, Goodfellow P, Lovell-Badge R. Expression of Sry, the mouse sex determining gene. Development 1995; 121:1603-1614.
5. McLaren A. Germ and somatic cell lineages in the developing gonad. Mol Cell Endocrinol 2000; 163:3-9.
6. Mackay S. Gonadal development in mammals at the cellular and molecular levels. Int Rev Cytol 2000; 200:47-99.
7. Wilhelm D, Hiramatsu R, Mizusaki H, Widjaja L, Combes AN, Kanai Y, Koopman P. SOX9 regulates prostaglandin D synthase gene transcription in vivo to ensure testis development. J Biol Chem 2007; 282: 10553-10560.
8. Sharpe RM, McKinnell C, Kivlin C, Fisher JS. Proliferation and functional maturation of Sertoli cells, and their relevance to disorders of testis function in adulthood. Reproduction 2003; 125:769-784.
9. Josso N, Picard JY, Rey R, di Clemente N. Testicular anti-Mullerian hormone: history, genetics, regulation and clinical applications. Pediatr Endocrinol Rev 2006; 3:347-358.
10. Russell LD, Clermont Y. Degeneration of germ cells in normal, hypophysectomized and hormone treated hypophysectomized rats. Anat Rec 1977; 187:347-366.
11. McLachlan RI, Wreford NG, de Kretser DM, Robertson DM. The effects of recombinant follicle-stimulating hormone on the restoration of spermatogenesis in the gonadotropin-releasing hormone-immunized adult rat. Endocrinology 1995; 136:4035-4043.
12. Zhengwei Y, Wreford NG, Royce P, de Kretser DM, McLachlan RI. Stereological evaluation of human spermatogenesis after suppression by testosterone treatment: heterogeneous pattern of spermatogenic impairment. J Clin Endocrinol Metab 1998; 83:1284-1291.
13. McLachlan RI, O'Donnell L, Stanton PG, Balourdos G, Frydenberg M, de Kretser DM, Robertson DM. Effects of testosterone plus medroxyprogesterone acetate on semen quality, reproductive hormones, and germ cell populations in normal young men. J Clin Endocrinol Metab 2002; 87:546-556.
14. Cortes D, Muller J, Skakkebaek NE. Proliferation of Sertoli cells during development of the human testis assessed by stereological methods. Int J Androl 1987; 10:589-596.
15. Marshall GR, Plant TM. Puberty occurring either spontaneously or induced precociously in rhesus monkey (Macaca mulatta) is associated with a marked proliferation of Sertoli cells. Biol Reprod 1996; 54: 1192-1199.
16. Cool J, Capel B. Mixed signals: development of the testis. Semin Reprod Med 2009; 27:5-13.
17. Allan CM, Garcia A, Spaliviero J, Zhang FP, Jimenez M, Huhtaniemi I, Handelsman DJ. Complete Sertoli cell proliferation induced by folliclestimulating hormone (FSH) independently of luteinizing hormone activity: evidence from genetic models of isolated FSH action. Endocrinology 2004; 145:1587-1593.
18. Myers M, Ebling FJ, Nwagwu M, Boulton R, Wadhwa K, Stewart J, Kerr JB. Atypical development of Sertoli cells and impairment of spermatogenesis in the hypogonadal (hpg) mouse. J Anat 2005; 207:797-811.
19. Chausiaux OE, Abel MH, Baxter FO, Khaled WT, Ellis PJ, Charlton HM, Affara NA. Hypogonadal mouse, a model to study the effects of the endogenous lack of gonadotropins on apoptosis. Biol Reprod 2008; 78: 77-90.
20. Wreford NG, Rajendra Kumar T, Matzuk MM, de Kretser DM. Analysis of the testicular phenotype of the follicle-stimulating hormone betasubunit knockout and the activin type II receptor knockout mice by stereological analysis. Endocrinology 2001; 142:2916-2920.
21. Abel MH, Baker PJ, Charlton HM, Monteiro A, Verhoeven G, De Gendt K, Guillou F, O'Shaughnessy PJ. Spermatogenesis and sertoli cell activity in mice lacking sertoli cell receptors for follicle-stimulating hormone and androgen. Endocrinology 2008; 149:3279-3285.
22. Loss ES, Jacobus AP, Wassermann GF, Diverse FSH. and testosterone signaling pathways in the Sertoli cell. Horm Metab Res 2007; 39: 806-812.
23. Orth JM. The role of follicle-stimulating hormone in controlling Sertoli cell proliferation in testes of fetal rats. Endocrinology 1984; 115: 1248-1255.
24. Meachem SJ, Ruwanpura SM, Ziolkowski J, Ague JM, Skinner MK, Loveland KL. Developmentally distinct in vivo effects of FSH on proliferation and apoptosis during testis maturation. J Endocrinol 2005; 186:429-446.
25. Orth JM. Proliferation of Sertoli cells in fetal and postnatal rats: a quantitative autoradiographic study. Anat Rec 1982; 203:485-492.
26. Crepieux P, Marion S, Martinat N, Fafeur V, Vern YL, Kerboeuf D, Guillou F, Reiter E. The ERK-dependent signalling is stage-specifically modulated by FSH, during primary Sertoli cell maturation. Oncogene 2001; 20:4696-4709.
27. Ketelslegers JM, Hetzel WD, Sherins RJ, Catt KJ. Developmental changes in testicular gonadotropin receptors: plasma gonadotropins and plasma testosterone in the rat. Endocrinology 1978; 103:212-222.
28. Tsai-Morris CH, Aquilano DR, Dufau ML. Cellular localization of rat testicular aromatase activity during development. Endocrinology 1985; 116:38-46.
29. Boitani C, Stefanini M, Fragale A, Morena AR. Activin stimulates Sertoli cell proliferation in a defined period of rat testis development. Endocrinology 1995; 136:5438-5444.
30. Fragale A, Puglisi R, Morena AR, Stefanini M, Boitani C. Agedependent activin receptor expression pinpoints activin A as a physiological regulator of rat Sertoli cell proliferation. Mol Hum Reprod 2001; 7:1107-1114.
31. Dahia CL, Rao AJ. Regulation of FSH receptor, PKIbeta, IL-6 and calcium mobilization: possible mediators of differential action of FSH. Mol Cell Endocrinol 2006; 247:73-81.
32. Grasso P, Reichert LE. In vivo effects of follicle-stimulating hormonerelated synthetic peptides on the mouse estrous cycle. Endocrinology 1996; 137:5370-5375.
33. Wassermann GF, Bloch LM, Grillo ML, Silva FR, Loss ES, McConnell LL. Biochemical factors involved in the FSH action on amino acid transport in immature rat testes. Horm Metab Res 1992; 24:276-279.
34. Touyz RM, Jiang L, Sairam MR. Follicle-stimulating hormone mediatedcalcium signaling by the alternatively spliced growth factor type I receptor. Biol Reprod 2000; 62:1067-1074.
35. Dupont J, Musnier A, Decourtye J, Boulo T, Lecureuil C, Guillou H, Valet S, Fouchecourt S, Pitetti JL, Nef S, Reiter E, Crepieux P. FSHstimulated PTEN activity accounts for the lack of FSH mitogenic effect in prepubertal rat Sertoli cells. Mol Cell Endocrinol 2010; 315:271-276.
36. van Haaster LH, De Jong FH, Docter R, De Rooij DG. The effect of hypothyroidism on Sertoli cell proliferation and differentiation and hormone levels during testicular development in the rat. Endocrinology 1992; 131:1574-1576.
37. De Franca LR, Hess RA, Cooke PS, Russell LD. Neonatal hypothyroidism causes delayed Sertoli cell maturation in rats treated with propylthiouracil: evidence that the Sertoli cell controls testis growth. Anat Rec 1995; 242:57-69.
38. Hess RA, Cooke PS, Bunick D, Kirby JD. Adult testicular enlargement induced by neonatal hypothyroidism is accompanied by increased Sertoli and germ cell numbers. Endocrinology 1993; 132:2607-2613.
39. Joyce KL, Porcelli J, Cooke PS. Neonatal goitrogen treatment increases adult testis size and sperm production in the mouse. J Androl 1993; 14: 448-55.
40. Jannini EA, Ulisse S, Piersanti D, Carosa E, Muzi P, Lazar J, D'Armiento M. Early thyroid hormone treatment in rats increases testis size and germ cell number. Endocrinology 1993; 132:2726-2728.
41. van Haaster LH, de Jong FH, Docter R, de Rooij DG. 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; 133:755-760.
42. Cooke PS, Zhao YD, Bunick D. Triiodothyronine inhibits proliferation and stimulates differentiation of cultured neonatal Sertoli cells: possible mechanism for increased adult testis weight and sperm production induced by neonatal goitrogen treatment. Biol Reprod 1994; 51: 1000-1005.
43. Simorangkir DR, Wreford NG, De Kretser DM. Impaired germ cell development in the testes of immature rats with neonatal hypothyroidism. J Androl 1997; 18:186-193.
44. Holsberger DR, Buchold GM, Leal MC, Kiesewetter SE, O'Brien DA, Hess RA, França LR, Kiyokawa H, Cooke PS. Cell-cycle inhibitors p27Kip1 and p21Cip1 regulate murine Sertoli cell proliferation. Biol Reprod 2005; 72:1429-1436.
45. Liang J, Slingerland JM. Multiple roles of the PI3K/PKB (Akt) pathway in cell cycle progression. Cell Cycle 2003; 2:339-345.
46. Maran RR. Thyroid hormones: their role in testicular steroidogenesis. Arch Androl 2003; 49:375-388.
47. St-Pierre N, Dufresne J, Rooney AA, Cyr DG. Neonatal hypothyroidism alters the localization of gap junctional protein connexin 43 in the testis and messenger RNA levels in the epididymis of the rat. Biol Reprod 2003; 68:1232-1240.
48. Gilleron J, Nebout M, Scarabelli L, Senegas-Balas F, Palmero S, Segretain D, Pointis G. A potential novel mechanism involving connexin 43 gap junction for control of sertoli cell proliferation by thyroid hormones. J Cell Physiol 2006; 209:153-161.
49. Rao JN, Liang JY, Chakraborti P, Feng P. Effect of thyroid hormone on the development and gene expression of hormone receptors in rat testes in vivo. J Endocrinol Invest 2003; 26:435-443.
50. Stock A, Sies H. Thyroid hormone receptors bind to an element in the connexin43 promoter. Biol Chem 2000; 381:973-979.
51. Tribulova N, Shneyvays V, Mamedova LK, Moshel S, Zinman T, Shainberg A, Manoach M, Weismann P, Kostin S. Enhanced connexin-43 and alpha-sarcomeric actin expression in cultured heart myocytes exposed to triiodo-L-thyronine. J Mol Histol 2004; 35:463-470.
52. Geng S, Sun B, Liu S, Wang J. Up-regulation of connexin 43 and gap junctional intercellular communication by Coleusin Factor is associated with growth inhibition in rat osteosarcoma UMR106 cells. Cell Biol Int 2007; 31:1420-1427.
53. Todorova MG, Soria B, Quesada I. Gap junctional intercellular communication is required to maintain embryonic stem cells in a nondifferentiated and proliferative state. J Cell Physiol 2008; 214:354-362.
54. Sridharan S, Simon L, Meling DD, Cyr DG, Gutstein DE, Fishman GI, Guillou F, Cooke PS. Proliferation of adult sertoli cells following conditional knockout of the Gap junctional protein GJA1 (connexin 43) in mice. Biol Reprod 2007; 76:804-812.
55. Lie PP, Cheng CY, Mruk DD. Coordinating cellular events during spermatogenesis: a biochemical model. Trends Biochem Sci 2009; 34: 366-373.
56. Tarulli GA, Stanton PG, Lerchl A, Meachem SJ. Adult sertoli cells are not terminally differentiated in the Djungarian hamster: effect of FSH onproliferation and junction protein organization. Biol Reprod 2006; 74: 798-806.
57. Tarulli GA, Meachem SJ, Schlatt S, Stanton PG. Regulation of testicular tight junctions by gonadotrophins in the adult Djungarian hamster in vivo. Reproduction 2008; 135:867-877.
58. McCabe MJ, Tarulli GA, Meachem SJ, Robertson DM, Smooker PM, Stanton PG. Gonadotropins regulate rat testicular tight junctions in vivo. Endocrinology 2010; 151:2911-2922.
59. Wagner MS, Wajner SM, Maia AL. The role of thyroid hormone in testicular development and function. J Endocrinol 2008; 199:351-365.
60. Bremner WJ, Millar MR, Sharpe RM, Saunders PT. Immunohistochemical localization of androgen receptors in the rat testis: evidence for stagedependent expression and regulation by androgens. Endocrinology 1994; 135:1227-1234.
61. You L, Sar M. Androgen receptor expression in the testes and epididymides of prenatal and postnatal Sprague-Dawley rats. Endocrine 1998; 9:253-261.
62. Weber MA, Groos S, Aumuller G, Konrad L. Post-natal development of the rat testis: steroid hormone receptor distribution and extracellular matrix deposition. Andrologia 2002; 34:41-54.
63. Rey RA, Musse M, Venara M, Chemes HE. Ontogeny of the androgen receptor expression in the fetal and postnatal testis: its relevance on Sertoli cell maturation and the onset of adult spermatogenesis. Microsc Res Tech 2009; 72:787-795.
64. Zhou X, Kudo A, Kawakami H, Hirano H. Immunohistochemical localization of androgen receptor in mouse testicular germ cells during fetal and postnatal development. Anat Rec 1996; 245:509-518.
65. Pelletier G. Localization of androgen and estrogen receptors in rat and primate tissues. Histol Histopathol 2000; 15:1261-1270.
66. Hill CM, Anway MD, Zirkin BR, Brown TR. Intratesticular androgen levels, androgen receptor localization, and androgen receptor expression in adult rat Sertoli cells. Biol Reprod 2004; 71:1348-1358.
67. Welsh M, Saunders PTK, Atanassova N, Sharpe RM, Smith LB. Androgen action via testicular peritubular myoid cells is essential for male fertility. FASEB J 2009; 23:4218-4230.
68. Buzek SW, Sanborn BM. Increase in testicular androgen receptor during sexual maturation in the rat. Biol Reprod 1998; 39:39-49.
69. Dierich A, Sairam MR, Monaco L, Fimia GM, Gansmuller A, LeMeur M, Sassone-Corsi P. Impairing follicle-stimulating hormone (FSH) signaling in vivo: targeted disruption of the FSH receptor leads to aberrant gametogenesis and hormonal imbalance. Proc Natl Acad Sci U S A 1998; 95:13612-13617.
70. Haywood M, Spaliviero J, Jimemez M, King NJ, Handelsman DJ, Allan CM. Sertoli and germ cell development in hypogonadal (hpg) mice expressing transgenic follicle-stimulating hormone alone or in combination with testosterone. Endocrinology 2003; 144:509-517.
71. Tan KA, De Gendt K, Atanassova N, Walker M, Sharpe RM, Saunders PT, Denolet E, Verhoeven G. 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; 146:2674-2683.
72. Welsh M, Saunders PT, Atanassova N, Sharpe RM, Smith LB. Androgen action via testicular peritubular myoid cells is essential for male fertility. FASEB J 2009; 23:4218-4230.
73. O'Shaughnessy PJ, Monteiro A, Verhoeven G, De Gendt K, Abel MH. Effect of FSH on testicular morphology and spermatogenesis in gonadotrophin-deficient hypogonadal mice lacking androgen receptors. Reproduction 2010; 139:177-184.
74. Buzzard JJ, Wreford NG, Morrison JR. Thyroid hormone, retinoic acid, and testosterone suppress proliferation and induce markers of differentiation in cultured rat sertoli cells. Endocrinology 2003; 144:3722-3731.
75. Meehan T, Schlatt S, O'Bryan MK, de Kretser DM, Loveland KL. Regulation of germ cell and Sertoli cell development by activin, follistatin, and FSH. Dev Biol 2000; 220:225-237.
76. Anderson RA, Sharpe RM. Regulation of inhibin production in the human male and its clinical applications. Int J Androl 2000; 23:136-144.
77. de Kretser DM, Buzzard JJ, Okuma Y, O'Connor AE, Hayashi T, Lin SY, Morrison JR, Loveland KL, Hedger MP. The role of activin, follistatin and inhibin in testicular physiology. Mol Cell Endocrinol 2004; 225:57-64.
78. Gold E, Jetly N, O'Bryan MK, Meachem S, Srinivasan D, Behuria S, Sanchez-Partida LG, Woodruff T, Hedwards S, Wang H, McDougall H, Casey V, et al. Activin C antagonizes activin A in vitro and overexpression leads to pathologies in vivo. Am J Pathol 2009; 174: 184-95.
79. Puglisi R, Montanari M, Chiarella P, Stefanini M, Boitani C. Regulatoryrole of BMP2 and BMP7 in spermatogonia and Sertoli cell proliferation in the immature mouse. Eur J Endocrinol 2004; 151:511-520.
80. Itman C, Loveland KL. SMAD expression in the testis: an insight into BMP regulation of spermatogenesis. Dev Dyn 2008; 237:97-111.
81. Huleihel M, Lunenfeld E. Regulation of spermatogenesis by paracrine/ autocrine testicular factors. Asian J Androl 2004; 6:259-268.
82. Petersen C, Froysa B, Soder O. Endotoxin and proinflammatory cytokines modulate Sertoli cell proliferation in vitro. J Reprod Immunol 2004; 61:13-30.
83. Stephan JP, Syed V, Jegou B. Regulation of Sertoli cell IL-1 and IL-6 production in vitro. Mol Cell Endocrinol 1997; 134:109-118.
84. Huleihel M, Lunenfeld E. Involvement of intratesticular IL-1 system in the regulation of Sertoli cell functions. Mol Cell Endocrinol 2002; 187: 125-132.
85. Hernandez-Rodriguez J, Segarra M, Vilardell C, Sanchez M, Garcia-Martinez A, Esteban MJ, Queralt C, Grau JM, Urbano-Marquez A, Palacin A, Colomer D, Cid MC. Tissue production of pro-inflammatory cytokines (IL-1beta, TNFalpha and IL-6) correlates with the intensity of the systemic inflammatory response and with corticosteroid requirements in giant-cell arteritis. Rheumatology (Oxford) 2004; 43:294-301.
86. Gerard N, Syed V, Bardin W, Genetet N, Jegou B. Sertoli cells are the site of interleukin-1 alpha synthesis in rat testis. Mol Cell Endocrinol 1991; 82:13-16.
87. Syed V, Khan SA, Lindh M, Ritzen EM. Mechanism of action of the factor(s) secreted by rat seminiferous tubules and inhibiting interstitial cell testosterone production in vitro. Acta Endocrinol (Copenh) 1998; 119:427-434.
88. Jonsson CK, Zetterstrom RH, Holst M, Parvinen M, Soder O. Constitutive expression of interleukin-1alpha messenger ribonucleic acid in rat Sertoli cells is dependent upon interaction with germ cells. Endocrinology 1999; 140:3755-3761.
89. Wahab-Wahlgren A, Holst M, Ayele D, Sultana T, Parvinen M, Gustafsson K, Granholm T, Soder O. Constitutive production of interleukin-1alpha mRNA and protein in the developing rat testis. Int J Androl 2000; 23:360-365.
90. Petersen C, Boitani C, Froysa B, Soder O. Interleukin-1 is a potent growth factor for immature rat sertoli cells. Mol Cell Endocrinol 2002; 186:37-47.
91. Sarkar O, Mathur PP, Cheng CY, Mruk DD. Interleukin 1 alpha (IL1A) is a novel regulator of the blood-testis barrier in the rat. Biol Reprod 2008; 78:445-454.
92. Kavanagh E, Buchert M, Tsapara A, Choquet A, Balda MS, Hollande F, Matter K. Functional interaction between the ZO-1-interacting transcription factor ZONAB/DbpA and the RNA processing factor symplekin. J Cell Sci 2006; 119:5098-5105.
93. Chaudhary J, Johnson J, Kim G, Skinner MK. Hormonal regulation and differential actions of the helix-loop-helix transcriptional inhibitors of differentiation (Id1, Id2, Id3, and Id4) in Sertoli cells. Endocrinology 2001; 142:1727-1736.
94. Norton JD. ID helix-loop-helix proteins in cell growth, differentiation and tumorigenesis. J Cell Sci 2000; 113:3897-3905.
95. Barone MV, Pepperkok R, Peverali FA, Philipson L. Id proteins control growth induction in mammalian cells. Proc Natl Acad Sci U S A 1994; 91:4985-4988.
96. Zebedee Z, Hara E. Id proteins in cell cycle control and cellular senescence. Oncogene 2001; 20:8317-8325.
97. Chaudhary J, Sadler-Riggleman I, Ague JM, Skinner MK. The helixloop-helix inhibitor of differentiation (ID) proteins induce post-mitotic terminally differentiated Sertoli cells to re-enter the cell cycle and proliferate. Biol Reprod 2005; 72:1205-1217.
98. Ahmed EA, Barten-van Rijbroek AD, Kal HB, Sadri-Ardekani H, Mizrak SC, van Pelt AM, de Rooij DG. Proliferative activity in vitro and DNA repair indicate that adult mouse and human Sertoli cells are not terminally differentiated, quiescent cells. Biol Reprod 2009; 80:1084-1091.
99. Chui K, Trivedi A, Cheng CY, Cherbavaz DB, Dazin PF, Huynh AL, Mitchell JB, Rabinovich GA, Noble-Haeusslein LJ, John CM. Characterization and functionality of proliferative human Sertoli cells. Cell Transplant 2011; 20:619-635.
100. Nalam RL, Andreu-Vieyra C, Braun RE, Akiyama H, Matzuk MM. Retinoblastoma protein plays multiple essential roles in the terminal differentiation of Sertoli cells. Mol Endocrinol 2009; 23:1900-1913.
101. Daugherty BL, Ward C, Smith T, Ritzenthaler JD, Koval M. Regulation of heterotypic claudin compatibility. J Biol Chem 2007; 282: 30005-30013.
102. Sato T, Ohkusa T, Honjo H, Suzuki S, Yoshida MA, Ishiguro YS, Nakagawa H, Yamazaki M, Yano M, Kodama I, Matsuzaki M. Altered expression of connexin43 contributes to the arrhythmogenic substrate during the development of heart failure in cardiomyopathic hamster. Am J Physiol Heart Circ Physiol 2008; 294:1164-1173.
103. Griswold MD, Solari A, Tung PS, Fritz IB. Stimulation by folliclestimulating hormone of DNA synthesis and of mitosis in cultured Sertoli cells prepared from testes of immature rats. Mol Cell Endocrinol 1977; 7: 151-165.
104. Schlatt S, de Kretser DM, Loveland KL. Discriminative analysis of rat Sertoli and peritubular cells and their proliferation in vitro: evidence for follicle-stimulating hormone-mediated contact inhibition of Sertoli cell mitosis. Biol Reprod 1996; 55:227-235.
105. Brehm R, Zeiler M, Rü ttinger C, Herde K, Kibschull M, Winterhager E, Willecke K, Guillou F, Lécureuil C, Steger K, Konrad L, Biermann K, et al. Sertoli cell-specific knockout of connexin43 prevents initiation of spermatogenesis. Am J Pathol 2007; 171:19-31.
106. Mazaud-Guittot S, Meugnier E, Pesenti S, Wu X, Vidal H, Gow A, Le Magueresse-Battistoni B. Claudin 11 deficiency in mice results in loss of the Sertoli cell epithelial phenotype in the testis. Biol Reprod 2010; 82: 202-13.
107. Chung SS, Choi C, Wang X, Hallock L, Wolgemuth DJ. Aberrant distribution of junctional complex components in retinoic acid receptor alpha-deficient mice. Microsc Res Tech 2010; 73:583-96.
108. Braun KW, Tribley WA, Griswold MD, Kim KH. Follicle-stimulating hormone inhibits all-trans-retinoic acid-induced retinoic acid receptor alpha nuclear localization and transcriptional activation in mouse Sertoli cell lines. J Biol Chem 2000; 275:4145-4151.
109. Batias C, Siffroi JP, Fenichel P, Pointis G, Segretain D. Connexin43 gene expression and regulation in the rodent seminiferous epithelium. J Histochem Cytochem 2000; 48:793-805.
110. Bruce AF, Rothery S, Dupont E, Severs NJ. Gap junction remodelling in human heart failure is associated with increased interaction of connexin43 with ZO-1. Cardiovasc Res 2008; 77:757-765.
111. Hartsock A, Nelson WJ. Adherens and tight junctions: structure, function and connections to the actin cytoskeleton. Biochim Biophys Acta 2008; 1778:660-669.
112. Carette D, Weider K, Gilleron J, Giese S, Dompierre J, Bergmann M, Brehm R, Denizot JP, Segretain D, Pointis G. Major involvement of connexin 43 in seminiferous epithelial junction dynamics and male fertility. Dev Biol 2010; 346:54-67.
113. Balda MS, Garrett MD, Matter K. The ZO-1-associated Y-box factor ZONAB regulates epithelial cell proliferation and cell density. J Cell Biol 2003; 160:423-432.
114. Frankel P, Aronheim A, Kavanagh E, Balda MS, Matter K, Bunney TD, Marshall CJ. RalA interacts with ZONAB in a cell density-dependent manner and regulates its transcriptional activity. EMBO J 2005; 24: 54-62.
115. Sourisseau T, Georgiadis A, Tsapara A, Ali RR, Pestell R, Matter K, Balda MS. Regulation of PCNA and cyclin D1 expression and epithelial morphogenesis by the ZO-1-regulated transcription factor ZONAB/ DbpA. Mol Cell Biol 2006; 26:2387-2398.
116. Pannequin J, Delaunay N, Darido C, Maurice T, Crespy P, Frohman MA, Balda MS, Matter K, Joubert D, Bourgaux JF, Bali JP, Hollande F. Phosphatidylethanol accumulation promotes intestinal hyperplasia by inducing ZONAB-mediated cell density increase in response to chronic ethanol exposure. Mol Cancer Res 2007; 5:1147-1157.
117. Gilleron J, Fiorini C, Carette D, Avondet C, Falk MM, Segretain D, Pointis G. Molecular reorganization of Cx43, Zo-1 and Src complexes during the endocytosis of gap junction plaques in response to a nongenomic carcinogen. J Cell Sci 2008; 121:4069-4078.
118. Ikenoue T, Inoki K, Zhao B, Guan KL. PTEN acetylation modulates its interaction with PDZ domain. Cancer Res 2008; 68:6908-6912.
119. Wu Y, Dowbenko D, Spencer S, Laura R, Lee J, Gu Q, Lasky LA. Interaction of the tumor suppressor PTEN/MMAC with a PDZ domain of MAGI3, a novel membrane-associated guanylate kinase. J Biol Chem 2000; 275:21477-21485.
120. Sluka P, O'Donnell L, Bartles JR, Stanton PG. FSH regulates the formation of adherens junctions and ectoplasmic specialisations between rat Sertoli cells in vitro and in vivo. J Endocrinol 2006; 189:381-395.
121. Subauste MC, Nalbant P, Adamson ED, Hahn KM. Vinculin controls PTEN protein level by maintaining the interaction of the adherens junction protein beta-catenin with the scaffolding protein MAGI-2. J Biol Chem 2005; 280:5676-5681.
122. McClusky LM. Stage and season effects on cell cycle and apoptotic activities of germ cells and Sertoli cells during spermatogenesis in the spiny dogfish (Squalus acanthias). Reproduction 2005; 129:89-102.
123. Franca LR, Parreira GG, Gates RJ, Russell LD. Hormonal regulation of spermatogenesis in the hypophysectomized rat: quantitation of germ-cellpopulation and effect of elimination of residual testosterone after longterm hypophysectomy. J Androl 1998; 19:335-340; discussion 341-332.
124. Bartke A, Sinha HIkim AP, Russell L. Sertoli cell structure and function in seasonally breeding mammals. In: Russel LD, Griswold MD (eds.), The Sertoli Cell, 1st ed. Clearwater, FL: Cache River Press; 1993:349- 364.
125. Lerchl A, Sotiriadou S, Behre HM, Pierce J, Weinbauer GF, Kliesch S, Nieschlag E. Restoration of spermatogenesis by follicle-stimulating hormone despite low intratesticular testosterone in photoinhibited hypogonadotropic Djungarian hamsters (Phodopus sungorus). Biol Reprod 1993; 49:1108-1116.
126. Bergmann M. Photoperiod and testicular function in Phodopus sungorus. Adv Anat Embryol Cell Biol 1987; 105:1-76.
127. Schlatt S, De Geyter M, Kliesch S, Nieschlag E, Bergmann M. Spontaneous recrudescence of spermatogenesis in the photoinhibited male Djungarian hamster, Phodopus sungorus. Biol Reprod 1995; 53: 1169-1177.
128. Meachem SJ, Stanton PG, Schlatt S. Follicle-stimulating hormone regulates both Sertoli cell and spermatogonial populations in the adult photoinhibited Djungarian hamster testis. Biol Reprod 2005; 72: 1187-1193.
129. Niklowitz P, Lerchl A, Nieschlag E. In vitro fertilizing capacity of sperm from FSH-treated photoinhibited Djungarian hamsters (Phodopus sungorus). J Endocrinol 1997; 154:475-481.
130. Wolfe AM, Turek FW, Levine JE. Blockade of singular folliclestimulating hormone secretion and testicular development in photostimulated Djungarian hamsters (Phodopus sungorus) by a gonadotropinreleasing hormone antagonist. Biol Reprod 1995; 53:724-731.
131. Sinha Hikim AP, Bartke A, Russell LD. Morphometric studies on hamster testes in gonadally active and inactive states: light microscope findings. Biol Reprod 1988; 39:1225-1237.
132. Hochereau-de Reviers MT, Pelletier J, de Reviers MM. Effect of hemicastration on young and adult male rats. J Reprod Fertil 1972; 31: 519-520.
133. de Reviers M, Hochereau-de Reviers MT, Blanc MR, Brillard JP, Courot M, Pelletier J. Control of Sertoli and germ cell populations in the cock and sheep testes. Reprod Nutr Dev 1980; 20:241-249.
134. Hö tzel MJ, Markey CM, Walkden-Brown SW, Blackberry MA, Martin GB. Morphometric and endocrine analyses of the effects of nutrition on the testis of mature Merino rams. J Reprod Fertil 1998; 113:217-230.
135. Johnson L, Varner DD, Tatum ME, Scrutchfield WL. Season but not age affects Sertoli cell number in adult stallions. Biol Reprod 1991; 45: 404-410.
136. Meachem SJ, Schlatt S, Ruwanpura SM, Stanton PG. The effect of testosterone, dihydrotestosterone and oestradiol on the re-initiation of spermatogenesis in the adult photoinhibited Djungarian hamster. J Endocrinol 2007; 192:553-561.
137. Jarow JP, Budin RE, Dym M, Zirkin BR, Noren S, Marshall FF. Quantitative pathologic changes in the human testis after vasectomy: a controlled study. N Engl J Med 1985; 313:1252-1256.
138. Hentrich A, Wolter M, Szardening-Kirchner C, Lüers GH, Bergmann M, Kliesch S, Konrad L. Reduced numbers of Sertoli, germ, and spermatogonial stem cells in impaired spermatogenesis. Mod Pathol 2011; 10:1380-1389.
139. Johnson L, Petty CS, Neaves WB. Age-related variation in seminiferous tubules in men: a stereological evaluation. J Androl 1986; 7:316-322.
140. Steger K, Rey R, Kliesch S, Louis F, Schleicher G, and Bergmann M. Immunohistochemical detection of immature Sertoli cell markers in testicular tissue of infertile adult men: a preliminary study. Int J Androl 1996; 19:122-128.
141. Steger K, Rey R, Louis F, Kliesch S, Behre HM, Nieschlag E, Hoepffner W, Bailey D, Marks A, Bergmann M. Reversion of the differentiated phenotype and maturation block in Sertoli cells in pathological human testis. Hum Reprod 1999; 14:136-143.
142. Brehm R, Rey R, Kliesch S, Steger K, Marks A, Bergmann M. Mitotic activity of Sertoli cells in adult human testis: an immunohistochemical study to characterize Sertoli cells in testicular cords from patients showing testicular dysgenesis syndrome. Anat Embryol (Berl) 2006; 211: 223-236.
143. Brehm R, Ruttinger C, Fischer P, Gashaw I, Winterhager E, Kliesch S, Bohle RM, Steger K, Bergmann M. Transition from preinvasive carcinoma in situ to seminoma is accompanied by a reduction of connexin 43 expression in Sertoli cells and germ cells. Neoplasia 2006; 8:499-509.
144. Fink C, Weigel R, Hembes T, Lauke-Wettwer H, Kliesch S, Bergmann M, Brehm RH. Altered expression of ZO-1 and ZO-2 in Sertoli cells andloss of blood-testis barrier integrity in testicular carcinoma in situ. Neoplasia 2006; 8:1019-1027.
145. Young KA, Ball GF, Nelson RJ. Photoperiod-induced testicular apoptosis in European starlings (Sturnus vulgaris). Biol Reprod 2001; 64:706-713.
146. Zhang XS, Zhang ZH, Jin X, Wei P, Hu XQ, Chen M, Lu CL, Lue YH, Hu ZY, Sinha Hikim AP, Swerdloff RS, Wang C, et al. Dedifferentiation of adult monkey Sertoli cells through activation of extracellularly regulated kinase 1/2 induced by heat treatment. Endocrinology 2006; 147:1237-1245.
147. Brehm R, Steger K. Regulation of Sertoli cell and germ cell differentation. Adv Anat Embryol Cell Biol 2005; 181:1-93.
148. Means AR, Dedman JR, Tash JS, Tindall DJ, van Sickle M, Welsh MJ. Regulation of the testis sertoli cell by follicle stimulating hormone. Annu Rev Physiol 1980; 42:59-70.
149. Tindall DJ, Tash JS, Means AR. Factors affecting Sertoli cell function in the testis. Environ Health Perspect 1981; 38:5-10.
150. Baines H, Nwagwu MO, Hastie GR, Wiles RA, Mayhew TM, Ebling FJ. Effects of estradiol and FSH on maturation of the testis in the hypogonadal (hpg) mouse. Reprod Biol Endocrinol 2008; 29:4-6.
151. Walker WH, Cheng J. FSH and testosterone signaling in Sertoli cells. Reproduction 2005; 130:15-28.
152. Buzzard JJ, Farnworth PG, De Kretser DM, O'Connor AE, Wreford NG, Morrison JR. Proliferative phase sertoli cells display a developmentally regulated response to activin in vitro. Endocrinology 2003; 144:474-483.
153. Holsberger DR, Jirawatnotai S, Kiyokawa H, Cooke PS. Thyroid hormone regulates the cell cycle inhibitor p27Kip1 in postnatal murine Sertoli cells. Endocrinology 2003; 144:3732-3738.
154. Cupp AS, Dufour JM, Kim G, Skinner MK, Kim KH. Action of retinoids on embryonic and early postnatal testis development. Endocrinology 1999; 140:2343-2352.
155. Tamajusuku AS, Carrillo-Sepúlveda MA, Braganhol E, Wink MR, SarkisJJ, Barreto-Chaves ML, Battastini AM. Activity and expression of ecto-50-nucleotidase/CD73 are increased by thyroid hormones in vascular smooth muscle cells. Mol Cell Biochem 2006; 289:65-72.
156. Zamoner A, Bruno AN, Casali EA, Corbelini PF, Diniz GP, Barreto-Chaves ML, Silva FR, Sarkis JJ, Pessoa-Pureur R. Genomic-independent action of thyroid hormones on NTPDase activities in Sertoli cell cultures from congenital hypothyroid rats. Life Sci 2006; 80:51-58.
157. Filippini A, Riccioli A, De Cesaris P, Paniccia R, Teti A, Stefanini M, Conti M, Ziparo E. Activation of inositol phospholipid turnover and calcium signaling in rat Sertoli cells by P2-purinergic receptors: modulation of follicle-stimulating hormone responses. Endocrinology 1994; 134:1537-1545.
158. Foresta C, Rossato M, Bordon P, Di Virgilio F. Extracellular ATP activates different signalling pathways in rat Sertoli cells. Biochem J 1995; 311:269-274.
159. Don J, Stelzer G. The expanding family of CREB/CREM transcription factors that are involved with spermatogenesis. Mol Cell Endocrinol 2002; 187:115-124.
160. Di Vizio D, Cito L, Boccia A, Chieffi P, Insabato L, Pettinato G, Motti ML, Schepis F, D'Amico W, Fabiani F, Tavernise B, Venuta S, et al. Loss of the tumor suppressor gene PTEN marks the transition from intratubular germ cell neoplasias (ITGCN) to invasive germ cell tumors. Oncogene 2005; 24:1882-1894.
161. Chambard JC, Lefloch R, Pouyssegur J, Lenormand P. ERK implication in cell cycle regulation. Biochim Biophys Acta 2007; 1773:1299-1310.
162. Lindzey J, Kumar MV, Grossman M, Young C, Tindall DJ. Molecular mechanisms of androgen action. Vitam Horm 1994; 49:383-432.
163. Schmidt M, Fernandez de Mattos S, van der Horst A, Klompmaker R, Kops GJ, Lam EW, Burgering BM, Medema RH. Cell cycle inhibition by FoxO forkhead transcription factors involves downregulation of cyclin D. Mol Cell Biol 2002; 22:7842-7852.