Three-dimensional analysis of connexin43 gap junction in the ex vivo rat seminiferous tubules: Short-term effects of hormonal effectors

Microscopy Research and Technique

Volumn 72, Issue 11, 2009, Pages 845-855

  Gilleron, Jerome ^a,b   Carette, Diane ^a,b,c   Carpentier, Francoise ^a,b   Segretain, Dominique ^a,b   Pointis, Georges ^a,c  

^a INSERM   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c CENTRE MÉDITERRANÉEN DE MÉDECINE MOLÉCULAIRE C3M   (France)

Author keywords

Connexin43; Coupling; FSH; Seminiferous tubules; Steroids; Three dimensional analysis

Indexed keywords

CELL CULTURE;

CONNEXIN 43; EX-VIVO; FSH; GAP-JUNCTIONS; GERM CELLS; SEMINIFEROUS TUBULES; SERTOLI CELLS; SHORT-TERM EFFECTS; STEROID; THREE-DIMENSIONAL ANALYSIS;

CELL DEATH;

CONNEXIN 43; CYCLIC AMP; ESTRADIOL; FOLLITROPIN; GONADOTROPIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; GAP JUNCTION; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; SEMINIFEROUS TUBULE; SERTOLI CELL; SPERMATOGENESIS; ANIMAL; CELL JUNCTION; CHEMISTRY; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

MYOIDA; RATTUS;

ANIMALS; CONNEXIN 43; GAP JUNCTIONS; GONADOTROPINS; MALE; RATS; RATS, SPRAGUE-DAWLEY; SEMINIFEROUS TUBULES; SPERMATOGENESIS;

EID: 70350532568     PISSN: 1059910X     EISSN: 10970029     Source Type: Journal    
DOI: 10.1002/jemt.20731     Document Type: Article

References (52)

1. Batias C, Defamie N, Lablack A, Thepot D, Fenichel P, Segretain D, Pointis G. 1999. Modified expression of testicular gap-junction connexin 43 during normal spermatogenic cycle and in altered spermatogenesis. Cell Tissue Res 298:113-121. (Pubitemid 29460510)
2. Batias C, Siffroi JP, Fénichel P, Pointis G, Segretain D. 2000. Connexin43 gene expression and regulation in the rodent seminiferous epithelium. J Histochem Cytochem 48:793-805. (Pubitemid 30366614)
3. Bourdon V, Lablack A, Abbe P, Segretain D, Pointis G. 1998. Characterization of a clonal Sertoli cell line using adult PyLT transgenic mice. Biol Reprod 58:591-599. (Pubitemid 28099128)
4. 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. 2007. A sertoli cell-specific knockout of connexin43 prevents initiation of spermatogenesis. Am J Pathol 171:19-31. (Pubitemid 47339223)
5. Bruzzone R, White TW, Paul DL. 1996. Connections with connexins: The molecular basis of direct intercellular signaling. Eur J Biochem 238:1-27. (Pubitemid 26164180)
6. Cheng CY, Mruk DD. 2002. Cell junction dynamics in the testis: Sertoli-germ cell interactions and male contraceptive development. Physiol Rev 82:825-874.
7. Decrouy X, Gasc JM, Pointis G, Segretain D. 2004. Functional characterization of Cx43 based gap junctions during spermatogenesis. J Cell Physiol 200:146-154. (Pubitemid 38720630)
8. Defamie N, Mograbi B, Roger C, Cronier L, Malassine A, Brucker-Davis F, Fenichel P, Segretain D, Pointis G. 2001. Disruption of gap junctional intercellular communication by lindane is associated with aberrant localization of connexin43 and zonula occludens-1 in 42GPA9 sertoli cells. Carcinogenesis 22:1537-1542.
9. 2+ in gap-junction remodeling: Studies in humans and rats. Naunyn Schmiedeberg's Arch Pharmacol 377:125-138.
10. Dym M, Fawcett DW. 1970. The blood-testis barrier in the rat and the physiological compartmentation of the seminiferous epithelium. Biol Reprod 3:308-326.
11. Fiorini C, Decrouy X, Defamie N, Segretain D, Pointis G. 2006. Opposite regulation of connexin33 and connexin43 by LPS and IL-1α in spermatogenesis. Am J Physiol Cell Physiol 290:C733-C740.
12. Fiorini C, Gilleron J, Carette D, Valette A, Tilloy A, Chevalier S, Segretain D, Pointis G. 2008. Accelerated clathrin-dependent internalization of junctional proteins within endocytic vacuoles as an early event to the carcinogen DDT. Biochim Biophys Acta 1778:56-67.
13. Gilleron J, Nebout N, Scarabelli L, Senegas-Balas F, Palmero S, Segretain D, Pointis G. 2006. Involvement of the gap junction connexin43 in the control of sertoli cell proliferation by thyroid hormones. J Cell Physiol 209:153-161.
14. Gilleron J, Fiorini C, Carette D, Avondet C, Falk M, Segretain D, Pointis G. 2008. Molecular reorganization of the connexin 43. Zonula occludens-1 and c-Src complexes during gap junction plaque endocytosis in response to a non genomic carcinogen. J Cell Sci 121:4069-4078.
15. Gilula NB, Fawcett DW, Aoki A. 1976. The Sertoli cell occluding junctions and gap junctions in mature and developing mammalian testis. Dev Biol 50:142-168.
16. Gorczynska E, Spaliviero J, Handelsman DJ. 1994. The relationship between 3′,5′-cyclic adenosine monophosphate and calcium in mediating follicle-stimulating hormone signal transduction in sertoli cells. Endocrinology 134:293-300.
17. Grassi F, Monaco L, Fratamico G, Dolci S, Iannini E, Conti M, Eusebi F, Stefanini M. 1986. Putative second messengers affect cell coupling in the seminiferous tubules. Cell Biol Int Rep 10:631-639.
18. Haefliger JA, Bruzzone R, Jenkins NA, Gilbert DJ, Copeland NG, Paul DL. 1992. Four novel members of the connexin family of gap junction proteins. Molecular cloning, expression, and chromosome mapping. J Biol Chem 267:2057-2064.
19. Hennemann H, Dahl E, White JB, Schwarz HJ, Lalley PA, Chang S, Nicholson BJ, Willecke K. 1992. Two gap junction genes, connexin 31.1 and 30.3, are closely linked on mouse chromosome 4 and preferentially expressed in skin. J Biol Chem 267:17225-17233.
20. Herve JC, Pluciennik F, Verrecchia F, Bastide B, Delage B, Joffre M, Deleze J. 1996. Influence of the molecular structure of steroids on their ability to interrupt gap junctional communication. J Membr Biol 149:179-187.
21. Juneja SC, Barr KJ, Enders GC, Kidder GM. 1999. Defects in the germ line and gonads of mice lacking connexin43. Biol Reprod 60:1263-1270.
22. Kadle R, Zhang JT, Nicholson BJ. 1991. Tissue-specific distribution of differentially phosphorylated forms of Cx43. Mol Cell Biol 11:363-369. (Pubitemid 21895214)
23. Lablack A, Bourdon V, Defamie N, Batias C, Mesnil M, Fenichel P, Pointis G, Segretain D. 1998. Ultrastructural and biochemical evidence for gap junction and connexin 43 expression in a clonal Sertoli cell line: A potential model in the study of junctional complex formation. Cell Tissue Res 294:279-287.
24. Lee NP, Leung KW, Wo JY, Tam PC, Yeung WS, Luk JM. 2006. Blockage of testicular connexins induced apoptosis in rat seminiferous epithelium. Apoptosis 11:1215-1229. (Pubitemid 44035969)
25. Lucas TF, Siu ER, Esteves CA, Monteiro HP, Oliveira CA, Porto CS, Lazari MF. 2007. 17Beta-estradiol induces the translocation of the estrogen receptors ESR1 and ESR2 to the cell membrane. MAPK3/1 phosphorylation and proliferation of cultured immature rat sertoli cells. Biol Reprod 78:101-114.
26. McGinley DM, Posalaky Z. 1986. Gap junctions between gonocytes and epithelial cells in the sex cords of the one day old rat. A freeze fracture study. J Submicrosc Cytol 18:75-84. (Pubitemid 16148935)
27. McLachlan RI, O'Donnell L, Meachem SJ, Stanton PG, de Kretser DM, Pratis K, Robertson DM. 2002. Identification of specific sites of hormonal regulation in spermatogenesis in rats, monkeys, and man. Recent Prog Horm Res 57:149-179.
28. Mograbi B, Corcelle E, Defamie N, Samson M, Nebout M, Segretain D, Fénichel P, Pointis G. 2003. Aberrant connexin 43 endocytosis by the carcinogen lindane involves activation of the ERK/mitogen-activated protein kinase pathway. Carcinogenesis 24:1415-1423.
29. Mruk DD, Cheng CY. 2004. Sertoli-sertoli and sertoli-germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis. Endo Rev 25:747-806.
30. Nagano T, Suzuki F. 1976. The postnatal development of the junctional complexes of the mouse sertoli cells as revealed by freezefracture. Anat Rec 185:403-417.
31. Nielsen PA, Kumar NM. 2003. Differences in expression patterns between mouse connexin-30.2 (Cx30.2) and its putative human orthologue, connexin-31.9. FEBS Lett 540:151-156.
32. Orth JM, Boehm R. 1990. Functional coupling of neonatal rat sertoli cells and gonocytes in coculture. Endocrinology 127:2812-2820.
33. Pahujaa M, Anikin M, Goldberg GS. 2007. Phosphorylation of connexin43 induced by Src: Regulation of gap junctional communication between transformed cells. Exp Cell Res 313:4083-4090.
34. Pelletier RM. 1995. 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 16:400-409.
35. Pluciennik F, Joffre M, Deleze J. 1994. Follicle-stimulating hormone increases gap junction communication in sertoli cells from immature rat testis in primary culture. J Membr Biol 139:81-96. (Pubitemid 24141947)
36. Pluciennik F, Verrecchia F, Bastide B, Herve JC, Joffre M, Deleze J. 1996. Reversible interruption of gap junctional communication by testosterone propionate in cultured sertoli cells and cardiac myocytes. J Membr Biol 149:169-177. (Pubitemid 26076102)
37. Plum A, Hallas G, Magin T, Dombrowski F, Hagendorff A, Schumacher B, Wolpert C, Kim J, Lamers WH, Evert M, Meda P, Traub O, Willecke K. 2000. Unique and shared functions of different connexins in mice. Curr Biol 10:1083-1091.
38. Pointis G, Segretain D. 2005. Role of connexin-based gap junction channels in testis. Trends Endocrinol Metab 16:300-306. (Pubitemid 41206636)
39. Risley MS. 2000. Connexin gene expression in seminiferous tubules of the Sprague-Dawley rat. Biol Reprod 62:748-754.
40. Risley MS, Tan IP, Roy C, Saez JC. 1992. Cell-, age- and stage-dependent distribution of connexin43 gap junctions in testes. J Cell Sci 103:81-96.
41. Rivedal E, Leithe E. 2005. Connexin43 synthesis, phosphorylation, and degradation in regulation of transient inhibition of gap junction intercellular communication by the phorbol ester TPA in rat liver epithelial cells. Exp Cell Res 302:143-152.
42. Russell LD. 1993. Morphological and functional evidence for sertoligerm cell relationships. In: Russell LD, Griswold MD, editors. The sertoli cell. Clearwater, FL: Cache River Press. pp.365-390.
43. Saez JC, Berthoud VM, Branes MC, Martinez AD, Beyer EC. 2003. Plasma membrane channels formed by connexins: Their regulation and functions. Physiol Rev 83:1359-1400.
44. Segretain D, Falk MM. 2004. Regulation of connexin biosynthesis, assembly, gap junction formation, and removal. Biochim Biophys Acta 1662:3-21. (Pubitemid 38366510)
45. Segretain D, Decrouy X, Dompierre J, Escalier D, Rahman N, Fiorini C, Mograbi B, Siffroi JP, Huhtaniemi I, Fenichel P, Pointis G. 2003. Sequestration of connexin43 in the early endosomes: An early event of Leydig cell tumor progression. Mol Carcinog 38:179-187. (Pubitemid 37523710)
46. Söderström KO, Parvinen M. 1978. Observations on living rat spermatogenic cells in different developmental stages. Acta Anat 100:557-572. (Pubitemid 8292257)
47. Sofikitis N, Giotitsas N, Tsounapi P, Baltogiannis D, Giannakis D, Pardalidis N. 2008. Hormonal regulation of spermatogenesis and spermiogenesis. J Steroid Biochem Mol Biol 109:323-330.
48. Söhl G, Willecke K. 2003. An update on connexin genes and their nomenclature in mouse and man. Cell Commun Adhes 10:173-180. (Pubitemid 38081368)
49. Sridharan S, Simon L, Meling DD, Cyr DG, Gutstein DE, Fishman GI, Guillou F, Cooke PS. 2007. Proliferation of adult sertoli cells following conditional knockout of the Gap junctional protein GJA1 (connexin 43) in mice. Biol Reprod 76:804-812.
50. Syed V, Stephan JP, Gerard N, Legrand A, Parvinen M, Bardin CW, Jegou B. 1995. Residual bodies activate sertoli cell interleukin-1 alpha (IL-1 alpha) release, which triggers IL-6 production by an autocrine mechanism, through the lipoxygenase pathway. Endocrinology 136:3070-3078.
51. Walker WH, Cheng J. 2005. FSH and testosterone signalling in sertoli cells. Reproduction 130:15-28. (Pubitemid 41015229)
52. Zhang JT, Nicholson BJ. 1989. Sequence and tissue distribution of a second protein of hepatic gap junctions, Cx26, as deduced from its cDNA. J Cell Biol 109:3391-3401.