Altered differentiation and clustering of Sertoli cells in transgenic mice showing a Sertoli cell specific knockout of the connexin 43 gene

Differentiation

Volumn 82, Issue 1, 2011, Pages 38-49

  Weider, Karola ^a   Bergmann, Martin ^b   Giese, Sarah ^b   Guillou, Florian ^c   Failing, Klaus ^b   Brehm, Ralph ^a  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

^c UMR85 PHYSIOLOGIE DE LA REPRODUCTION ET DES COMPORTEMENTS   (France)

Author keywords

Cell cluster; Connexin 43; Differentiation; Knockout; Mouse; Sertoli

Indexed keywords

ANDROGEN RECEPTOR; CONNEXIN 43; MESSENGER RNA; MUELLERIAN INHIBITING FACTOR; TRANSCRIPTION FACTOR GATA 1; VIMENTIN;

AGE; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL FATE; CELL MATURATION; CELL PROLIFERATION; CELL SPECIFICITY; CONTROLLED STUDY; CX43 GENE; DOWN REGULATION; GERM CELL; MALE; MOUSE; NEWBORN; NONHUMAN; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PUBERTY; SERTOLI CELL;

ANIMALS; BLOTTING, WESTERN; CELL DIFFERENTIATION; CONNEXIN 43; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SERTOLI CELLS;

MUS; MUS MUSCULUS;

EID: 79958765541     PISSN: 03014681     EISSN: 14320436     Source Type: Journal    
DOI: 10.1016/j.diff.2011.03.001     Document Type: Article

References (56)

1. Ahmed E.A., Barten-van Rijbroek A.D., Kal H.B., Sadri-Ardekani H., Mizrak S.C., van Pelt A.M., de Rooij D.G. 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.
2. Al-Attar L., Noël K., Dutertre M., Belville C., Forest M.G., Burgoyne P.S., Josso N., Rey R. Hormonal and cellular regulation of Sertoli cell anti-Müllerian hormone production in the postnatal mouse. J. Clin. Invest. 1997, 100:1335-1343.
3. Amlani S., Vogl A.W. Changes in the distribution of microtubules and intermediate filaments in mammalian Sertoli cells during spermatogenesis. Anat. Rec. 1988, 220:143-160.
4. Arambepola N.K., Bunick D., Cooke P.S. Thyroid hormone and follicle-stimulating hormone regulate Müllerian-inhibiting substance messenger ribonucleic acid expression in cultured neonatal rat Sertoli cells. Endocrinology 1998, 139:4489-4495.
5. Batias C., Defamie N., Lablack A., Thepot D., Fenichel P., Segretain D., Pointis G. Modified expression of testicular gap-junction connexin 43 during normal spermatogenic cycle and in altered spermatogenesis. Cell Tissue Res. 1999, 298:113-121.
6. Beau C., Rauch M., Joulin V., Jégou B., Guerrier D. GATA-1 is a potential repressor of anti-Müllerian hormone expression during the establishment of puberty in the mouse. Mol. Reprod. Dev. 2000, 56:124-138.
7. Bellvé A.R., Cavicchia J.C., Millette C.F., O'Brien D.A., Bhatnagar Y.M., Dym M. Spermatogenic cells of the prepubertal mouse. isolation and morphological characterization. J. Cell Biol. 1977, 74:68-85.
8. Bergmann M., Kliesch S. The distribution pattern of cytokeratin and vimentin immunoreactivity in testicular biopsies of infertile men. Anat. Embryol. 1994, 190:515-520.
9. Boujrad N., Hochereau-de Reviers M.T., Carreau S. Evidence for germ cell control of Sertoli cell function in three models of germ cell depletion in adult rat. Biol. Reprod. 1995, 53:1345-1352.
10. Brehm R., Marks A., Rey R., Kliesch S., Bergmann M., Steger K. Altered expression of connexins 26 and 43 in Sertoli cells in seminiferous tubules infiltrated with carcinoma-in-situ or seminoma. J. Pathol. 2002, 197:647-653.
11. Brehm R., Steger K. Regulation of Sertoli cell and Germ Cell Differentiation, Advances in Anatomy, Embryology and Cell Biology 2005, 181. Springer Verlag, Berlin.
12. Brehm R., Zeiler M., Rüttinger C., Herde K., Kibschull M., Winterhager E., Willecke K., Guillou F., Lécureuil C., Steger K., Konrad L., Biermann K., Failing K., Bergmann M. A sertoli cell-specific knockout of connexin43 prevents initiation of spermatogenesis. Am. J. Pathol. 2007, 171:19-31.
13. Bruzzone R., White T.W., Paul D.L. Connections with connexins: the molecular basis of direct intercellular signalling. Eur. J. Biochem. 1996, 238:1-27.
14. Bunick D., Kirby J., Hess R.A., Cooke P.S. Developmental expression of testis messenger ribonucleic acids in the rat following propylthiouracil-induced neonatal hypothyroidism. Biol. Reprod. 1994, 51:706-713.
15. Carette D., Weider K., Gilleron J., Giese S., Dompierre J., Bergmann M., Brehm R., Denizot J.P., Segretain D., Pointis G. Major involvement of connexin 43 in seminiferous epithelial junction dynamics and male fertility. Dev. Biol. 2010, 346:54-67.
16. Chaudhary J., Sadler-Riggleman I., Ague J.M., Skinner M.K. The helix-loop-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.
17. Dalgaard M., Hossaini A., Hougaard K.S., Hass U., Ladefoged O. Developmental toxicity of toluene in male rats: effects on semen quality, testis morphology, and apoptotic neurodegeneration. Arch. Toxicol. 2001, 75:103-109.
18. Decrouy X., Gasc J.M., Pointis G., Segretain D. Functional characterization of Cx43 based gap junctions during spermatogenesis. J. Cell Physiol. 2004, 200:146-154.
19. De Gendt K., Swinnen J.V., Saunders P.T., Schoonjans L., Dewerchin M., Devos A., Tan K., Atanassova N., Claessens F., Lécureuil C., Heyns W., Carmeliet P., Guillou F., Sharpe R.M., Verhoeven G. A Sertoli cell-selective knockout of the androgen receptor causes spermatogenic arrest in meiosis. Proc. Natl. Acad. Sci. USA 2004, 101:1327-1332.
20. Dirami G., Ravindranath N., Kleinman H.K., Dym M. Evidence that basement membrane prevents apoptosis of Sertoli cells in vitro in the absence of known regulators of Sertoli cell function. Endocrinology 1995, 136:4439-4447.
21. 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.
22. Gilleron J., Carette D., Durand P., Pointis G., Segretain D. Connexin 43 a potential regulator of cell proliferation and apoptosis within the seminiferous epithelium. Int. J. Biochem. Cell Biol. 2009, 41:1381-1390.
23. Gondos B., Berndston W.E. Postnatal and pubertal development. The Sertoli cell 1993, 115-154. Cache River Press, Clearwater. M.D. Griswold, L.D. Russell (Eds.).
24. Guitton N., Touzalin A.M., Sharpe R.M., Cheng C.Y., Pinon-Lataillade G., Méritte H., Chenal C., Jégou B. Regulatory influence of germ cells on sertoli cell function in the pre-pubertal rat after acute irradiation of the testis. Int. J. Androl. 2000, 23:332-339.
25. Handel M.A., Eppig J.J. Sertoli cell differentiation in the testes of mice genetically deficient in germ cells. Biol. Reprod. 1979, 20:1031-1038.
26. Johnson K.J., Hall E.S., Boekelheide K. 2,5-Hexanedione exposure alters the rat Sertoli cell cytoskeleton. I. Microtubules and seminiferous tubule fluid secretion. Toxicol. Appl. Pharmacol. 1991, 111:432-442.
27. Josso N., di Clemente N., Gouédard L. Anti-Müllerian hormone and its receptors. Mol. Cell. Endocrinol. 2001, 179:25-32.
28. Kanai Y., Kawakami H., Takata K., Kurohmaru M., Hirano H., Hayashi Y. Involvement of actin filaments in mouse testicular cord organization in vivo and in vitro. Biol. Reprod. 1992, 46:233-245.
29. Kliesch S., Behre H.M., Hertle L., Bergmann M. Alteration of Sertoli cell differentiation in the presence of carcinoma in situ in human testis. J. Urol. 1998, 160:1894-1898.
30. Kopecky M., Semecky V., Nachtigal P. Vimentin expression during altered spermatogenesis in rats. Acta Histochem. 2005, 107:279-289.
31. Kumar N.M., Gilula N.B. The gap junction communication channel. Cell 1996, 84:381-388.
32. Mason J.I., Howe B.E., Howie A.F., Morley S.D., Nicol M.R., Payne A.H. Promiscuous 3beta-hydroxysteroid dehydrogenases: testosterone 17beta-hydroxysteroid dehydrogenase activities of mouse type I and VI 3beta-hydroxysteroid dehydrogenases. Endocr. Res. 2004, 30:709-714.
33. 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, 82:202-213.
34. Pelletier R.M. The distribution of connexin 43 is associated with the germ cell differentiation and with the modulation of the Sertoli cell junctional barrier in continual (guinea pig) and seasonal breeders' (mink) testes. J. Androl. 1995, 16:400-409.
35. Pérez-Armendariz E.M., Lamoyi E., Mason J.I., Cisneros-Armas D., Luu-The V., Bravo-Moreno J.F. Developmental regulation of connexin43 expression in fetal mouse testicular cells. Anat. Rec. 2001, 264:237-246.
36. Reaume A.G., DeSousa P.A., Kulkarni S., Langille B.L., Zhu D., Davies T.C., Juneja S.C., Kidder G.M., Rossant J. Cardiac malformation in neonatal mice lacking connexin43. Science 1995, 267:1831-1834.
37. Richburg J.H., Boekelheide K. Mono-(2-ethylhexyl) phthalate rapidly alters both Sertoli cell vimentin filaments and germ cell apoptosis in young rat testes. Toxicol. Appl. Pharmacol. 1996, 137:42-50.
38. Risley M.S., Tan I.P., Roy C., Sáez J.C. Cell-, age- and stage-dependent distribution of connexin43 gap junctions in testes. J. Cell Sci. 1992, 103:81-96.
39. Rodriguez I., Ody C., Araki K., Garcia I., Vassalli P. An early and massive wave of germinal cell apoptosis is required for the development of functional spermatogenesis. EMBO J. 1997, 16:2262-2270.
40. Russell L.D., França L.R., Brinster R.L. Ultrastructural observations of spermatogenesis in mice resulting from transplantation of mouse spermatogonia. J. Androl. 1996, 17:603-614.
41. Sasso-Cerri E., Cerri P.S. Morphological evidences indicate that the interference of cimetidine on the peritubular components is responsible for detachment and apoptosis of Sertoli cells. Reprod. Biol. Endocrinol. 2008, 6:18.
42. Schrans-Stassen B.H., Saunders P.T., Cooke H.J., de Rooij D.G. Nature of the spermatogenic arrest in Dazl -/- mice. Biol. Reprod. 2001, 65:771-776.
43. Sharpe R.M., Millar M., McKinnell C. Relative roles of testosterone and the germ cell complement in determining stage-dependent changes in protein secretion by isolated rat seminiferous tubules. Int. J. Androl. 1993, 16:71-81.
44. Sharpe R.M. Regulation of spermatogenesis. The Physiology of Reproduction 1994, 1363-1434. Raven Press, New York. E. Knobil, J.D. Neill (Eds.).
45. Sharpe R.M., McKinnell C., Kivlin C., Fisher J.S. Proliferation and functional maturation of Sertoli cells, and their relevance to disorders of testis function in adulthood. Reproduction 2003, 125:769-784.
46. Söhl G., Willecke K. Gap junctions and the connexin protein family. Cardiovasc. Res. 2004, 62:228-232.
47. Sridharan S., Simon L., Meling D.D., Cyr D.G., Gutstein D.E., Fishman G.I., Guillou F., Cooke P.S. Proliferation of adult Sertoli cells following conditional knockout of the gap junctional protein gja1 (connexin 43). Biol. Reprod. 2007, 76:804-812.
48. Steger K., Rey R., Kliesch S., Louis F., Schleicher G., Bergmann M. Immunohistochemical detection of immature Sertoli cell markers in testicular tissue of infertile men: a preliminary study. Int. J. Androl. 1996, 19:122-128.
49. Steger K., Tetens F., Bergmann M. Expression of connexin 43 in human testis. Histochem. Cell Biol. 1999, 112:215-220.
50. Steger K., Rey R., Louis F., Kliesch S., Behre H.M., 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.
51. Tan K.A., De Gendt K., Atanassova N., Walker M., Sharpe R.M., Saunders P.T., 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.
52. Tarulli G.A., Stanton P.G., Lerchl A., Meachem S.J. Adult sertoli cells are not terminally differentiated in the Djungarian hamster: effect of FSH. Biol. Reprod. 2006, 74:798-806.
53. Van Haaster L.H., De Jong F.H., Docter R., De Rooij D.G. The effect of hypothyroidism on Sertoli cell proliferation and differentiation and hormone levels during testicular development in the rat. Endocrinology 1992, 131:1574-1576.
54. Vergouwen R.P., Huiskamp R., Bas R.J., Roepers-Gajadien H.L., Davids J.A., de Rooij D.G. Postnatal development of testicular cell populations in mice. J. Reprod. Fertil. 1993, 99:479-485.
55. Wang Z.Q., Watanabe Y., Toki A., Itano T. Altered distribution of Sertoli cell vimentin and increased apoptosis in cryptorchid rats. J. Pediatr. Surg. 2002, 37:648-652.
56. Yomogida K., Ohtani H., Harigae H., Ito E., Nishimune Y., Engel J.D., Yamamoto M. Developmental stage- and spermatogenic cycle-specific expression of transcription factor GATA-1 in mouse Sertoli cells. Development 1994, 120:1759-1766.