Intercellular communication via connexin43 gap junctions is required for ovarian folliculogenesis in the mouse

Developmental Biology

Volumn 233, Issue 2, 2001, Pages 258-270

  Ackert, Cheryl L ^a,b   Gittens, Joanne E I ^a,b   O'Brien, Marilyn J ^c   Eppig, John J ^c   Kidder, Gerald M ^a,b  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b CHILDREN S HEALTH RESEARCH INSTITUTE   (Canada)

^c JACKSON LABORATORY   (United States)

Author keywords

Connexin43; Cx43; Folliculogenesis; Gap junctions; Gene targeting; Intercellular communication; Oogenesis; Ovary graft

Indexed keywords

CONNEXIN 32; CONNEXIN 43; CONNEXIN 45; GAP JUNCTION PROTEIN; NEUROMODULIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COMMUNICATION; FEMALE; FETUS; GAP JUNCTION; GRANULOSA CELL; IMMUNOREACTIVITY; LETHALITY; MOUSE; NEWBORN; NONHUMAN; OVARY FOLLICLE DEVELOPMENT; OVULATION; PRIORITY JOURNAL;

MAMMALIA;

EID: 0035873229     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.2001.0216     Document Type: Article

References (53)

1. Alcoléa S., Théveniau-Ruissy M., Jarry-Guichard T., Marics I., Tzouanacou E., Chauvin J.-P., Briand J.-P., Moorman A. F. M., Lamers W. H., Gros D. Downregulation of connexin45 gene products during mouse heart development. Circ. Res. 84:1999;1365-1379.
2. Al-Ubaidi M. R., White T. W., Ripps H., Poras I., Avner P., Gomès D., Bruzzone R. Functional properties, developmental regulation, and chromosomal localization of murine connexin36, a gap-junctional protein expressed preferentially in retina and brain. J. Neurosci. Res. 59:2000;813-826.
3. Bevans C. G., Kordel M., Rhee S. K., Harris A. L. Isoform composition of connexin channels determines selectivity among second messengers and uncharged molecules. J. Biol. Chem. 273:1998;2808-2816.
4. Brower P. T., Schultz R. M. Intercellular communication between granulosa cells and mouse oocytes: Existence and possible nutritional role during oocyte growth. Dev. Biol. 90:1982;144-153.
5. Bruzzone R., White T. W., Goodenough D. A. The cellular internet: On-line with connexins. BioEssays. 18:1996a;709-718.
6. Bruzzone R., White T. W., Paul D. L. Connections with connexins: The molecular basis of direct intercellular signalling. Eur. J. Biochem. 238:1996b;1-27.
7. Byskov A. G., Andersen C. Y., Hossaini A., Guoliang X. Cumulus cells of oocyte-cumulus complexes secrete a meiosis-activating substance when stimulated with FSH. Mol. Reprod. Dev. 46:1997;296-305.
8. Carabatsos M. J., Elvin J., Matzuk M. M., Albertini D. F. Characterization of oocyte and follicle development in growth differentiation factor-9-deficient mice. Dev. Biol. 204:1998;373-384.
9. Condorelli D. F., Parenti R., Spinella F., Salinaro A. T., Belluardo N., Cardile V., Cicirata F. Cloning of a new gap junction gene (Cx36) highly expressed in mammalian brain neurons. Eur. J. Neurosci. 10:1998;1202-1208.
10. Coskun S., Lin Y. C. Effects of transforming growth factors and activin-A on in vitro porcine oocyte maturation. Mol. Reprod. Dev. 38:1994;153-159.
11. Dahl E., Manthey D., Chen Y., Schwarz H.-J., Chang Y. S., Lalley P. A., Nicholson B. J., Willecke K. Molecular cloning and functional expression of mouse connexin-30, a gap junction gene highly expressed in adult brain and skin. J. Biol. Chem. 271:1996;17903-17910.
12. Derynck R., Zhang Y., Feng X.-H. Smads: Transcriptional activators of TGF-β responses. Cell. 95:1998;737-740.
13. Dierich A., Sairam M. R., Monaco L., Fimia G. M., 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. USA. 95:1998;13612-13617.
14. Dong J., Albertini D. F., Nishimori K., Kumar T. R., Lu N., Matzuk M. M. Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature. 383:1996;531-535.
15. Downs S. M. The influence of glucose, cumulus cells, and metabolic coupling on ATP levels and meiotic control in the isolated mouse oocyte. Dev. Biol. 167:1995;502-512.
16. Elvin J. A., Clark A. T., Wang P., Wolfman N. M., Matzuk M. M. Paracrine actions of growth differentiation factor-9 in the mammalian ovary. Mol. Endocrinol. 13:1999a;1035-1048.
17. Elvin J. A., Yan C., Wang P., Nishimori K., Matzuk M. M. Molecular characterization of the follicle defects in the growth differentiation factor 9-deficient ovary. Mol. Endocrinol. 13:1999b;1018-1034.
18. Eppig J. J. Intercommunication between mammalian oocytes and companion somatic cells. BioEssays. 13:1991;569-574.
19. Eppig J. J. Oocyte-somatic cell communication in the ovarian follicles of mammals. Semin. Dev. Biol. 5:1994;51-59.
20. Eppig J. J., O'Brien M., Wigglesworth K. Mammalian oocyte growth and development in vitro. Mol. Reprod. Dev. 44:1996;260-273.
21. Eppig J. J., Wigglesworth K. Development of mouse and rat oocytes in chimeric reaggregated ovaries after interspecific exchange of somatic and germ cell components. Biol. Reprod. 63:2000;1014-1023.
22. Fitzpatrick S. L., Sindoni D. M., Shughrue P. J., Lane M. V., Merchenthaler I. J., Frail D. E. Expression of growth differentiation factor-9 messenger ribonucleic acid in ovarian and nonovarian rodent and human tissues. Endocrinology. 139:1998;2571-2578.
23. Goldberg G. S., Bechberger J. F., Naus C. C. G. A pre-loading method of evaluating gap junctional communication by fluorescent dye transfer. BioTechniques. 18:1995;490-497.
24. Goldberg G. S., Lampe P. D., Nicholson B. J. Selective transfer of endogenous metabolites through gap junctions composed of different connexins. Nat. Cell Biol. 1:1999;457-459.
25. Granot I., Dekel N. Phosphorylation and expression of connexin-43 ovarian gap junction protein are regulated by luteinizing hormone. J. Biol. Chem. 269:1994;30502-30509.
26. Halpin D. M., Jones A., Fink G., Charlton H. M. Postnatal ovarian follicle development in hypogonadal (hpg) and normal mice and associated changes in the hypothalamic-pituitary ovarian axis. J. Reprod. Fertil. 77:1986;287-296.
27. Hayashi M., McGee E. A., Min G., Klein C., Rose U. M., van Duin M., Hsueh A. J. W. Recombinant growth differentiation factor-9 (GDF-9) enhances growth and differentiation of cultured early ovarian follicles. Endocrinology. 140:1999;1236-1244.
28. He D. S., Jiang J. X., Taffet S. M., Burt J. M. Formation of heteromeric gap junction channels by connexins 40 and 43 in vascular smooth muscle cells. Proc. Natl. Acad. Sci. USA. 96:1999;6495-6500.
29. Heller D. T., Cahill D. M., Schultz R. M. Biochemical studies of mammalian oogenesis: Metabolic cooperativity between granulosa cells and growing mouse oocytes. Dev. Biol. 84:1981;455-464.
30. Houghton F. D., Thönnissen E., Kidder G. M., Naus C. C. G., Willecke K., Winterhager E. Doubly mutant mice, deficient in connexin32 and -43, show normal prenatal development of organs where the two gap junction proteins are expressed in the same cells. Dev. Genet. 24:1999;5-12.
31. Itahana K., Tanaka T., Morikazu Y., Komatu S., Ishida N., Takeya T. Isolation and characterization of a novel connexin gene, Cx-60, in porcine ovarian follicles. Endocrinology. 139:1998;320-329.
32. Juneja S. C., Barr K. J., Enders G. C., Kidder G. M. Defects in the germ line and gonads of mice lacking connexin43. Biol. Reprod. 60:1999;1263-1270.
33. Krüger O., Plum A., Kim J.-S., Winterhager E., Maxeiner S., Hallas G., Kirchhoff S., Traub O., Lamers W. H., Willecke K. Defective vascular development in connexin45-deficient mice. Development. 127:2000;4179-4193.
34. Krutovskikh V., Yamasaki H. Connexin gene mutations in human genetic diseases. Mutat. Res. 462:2000;197-207.
35. Kumai M., Nishii K., Nakamura K., Takeda N., Suzuki M., Shibata Y. Loss of connexin45 causes a cushion defect in early cardiogenesis. Development. 127:2000;3501-3512.
36. Li R., Mather J. P. Lindane, an inhibitor of gap junction formation, abolishes oocyte directed follicle organizing activity in vitro. Endocrinology. 138:1997;4477-4480.
37. Manthey D., Bukauskas F., Lee C. G., Kozak C. A., Willecke K. Molecular cloning and functional expression of the mouse gap junction gene connexin-57 in human HeLa cells. J. Biol. Chem. 274:1999;14716-14723.
38. Mattson B. A., Albertini D. F. Oogenesis: Chromatin and microtubule dynamics during meiotic prophase. Mol. Reprod. Dev. 25:1990;374-383.
39. McGrath S. A., Esquela A. F., Lee S.-J. Oocyte-specific expression of growth/differentiation factor-9. Mol. Endocrinol. 9:1995;131-136.
40. Mitchell P. A., Burghardt R. C. The ontogeny of nexuses (gap junctions) in the ovary of the fetal mouse. Anat. Rec. 214:1986;283-288.
41. Nelles E., Bützler C., Jung D., Temme A., Gabriel H.-D., Dahl U., Traub O., Stümpel F., Jungermann K., Zielasek J., Toyka K. V., Dermietzel R., Willecke K. Defective propagation of signals generated by sympathetic nerve stimulation in the liver of connexin32-deficient mice. Proc. Natl. Acad. Sci. USA. 93:1996;9565-9570.
42. Okuma A., Kuraoka A., Iida H., Inai T., Wasano K., Shibata Y. Colocalization of connexin43 and connexin45 but absence of connexin40 in granulosa cell gap junctions of rat ovary. J. Reprod. Fertil. 107:1996;255-264.
43. Reaume A. G., De Sousa 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. 267:1995;1831-1834.
44. Simon A. M., Goodenough D. A., Li E., Paul D. L. Female infertility in mice lacking connexin37. Nature. 385:1997;525-529.
45. Simoni M., Gromoll J., Nieschlag E. The follicle-stimulating hormone receptor: Biochemistry, molecular biology, physiology, and pathophysiology. Endocr. Rev. 18:1997;739-773.
46. Sztein J. M., O'Brien M. J., Farley J. S., Mobraaten L. E., Eppig J. J. Rescue of oocytes from antral follicles of cryopreserved mouse ovaries: Competence to undergo maturation, embryogenesis, and development to term. Hum. Reprod. 15:2000;567-571.
47. Threadgill D. W., Dlugosz A. A., Hansen L. A., Tennenbaum T., Lichti U., Yee D., LaMantia C., Mourton T., Herrup K., Harris R. C., Barnard J. A., Yuspa S. H., Coffey R. J., Magnuson T. Targeted disruption of mouse EGF receptor: Effect of genetic background on mutant phenotype. Science. 269:1995;230-234.
48. Udoff L. C., Adashi E. Y. Autocrine/paracrine regulation of the ovarian follicle. Endocrinologist. 9:1999;99-106.
49. Unger V. M., Kumar N. M., Gilula N. B., Yeager M. Three-dimensional structure of a recombinant gap junction membrane channel. Science. 283:1999;1176-1180.
50. Valdimarsson G., De Sousa P. A., Kidder G. M. Coexpression of gap junction proteins in the cumulus-oocyte complex. Mol. Reprod. Dev. 36:1993;7-15.
51. Wassarman P. M. The biology and chemistry of fertilization. Science. 235:1987;553-560.
52. White T. W., Paul D. L. Genetic diseases and gene knockouts reveal diverse connexin functions. Annu. Rev. Physiol. 61:1999;283-310.
53. Wright C. S., Becker D. L., Lin J. S., Warner A. E., Hardy K. Stage-specific and differential expression of gap junctions in the mouse ovary: Connexin-specific roles in follicular regulation. Reproduction. 121:2000;77-88.