Luteinizing hormone causes MAP kinase-dependent phosphorylation and closure of connexin 43 gap junctions in mouse ovarian follicles: One of two paths to meiotic resumption

Development

Volumn 135, Issue 19, 2008, Pages 3229-3238

  Norris, Rachael P ^a   Freudzon, Marina ^a   Mehlmann, Lisa M ^a   Cowan, Ann E ^a   Simon, Alexander M ^b   Paul, David L ^c   Lampe, Paul D ^d   Jaffe, Laurinda A ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d Fred Hutchinson Cancer Research Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONNEXIN 43; LUTEINIZING HORMONE; MITOGEN ACTIVATED PROTEIN KINASE; SERINE; MITOGEN ACTIVATED PROTEIN KINASE KINASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COMMUNICATION; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; FLUORESCENCE; GAP JUNCTION; MEIOSIS; MOUSE; NONHUMAN; OOCYTE; OVARY FOLLICLE; PRIORITY JOURNAL; PROPHASE; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SOMATIC CELL; ANIMAL; CELL JUNCTION; CHEMISTRY; CUMULUS CELL; CYTOLOGY; DRUG EFFECT; GRANULOSA CELL; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; TISSUE CULTURE TECHNIQUE;

MAMMALIA;

ANIMALS; CELL MEMBRANE PERMEABILITY; CONNEXIN 43; CUMULUS CELLS; FEMALE; GAP JUNCTIONS; GRANULOSA CELLS; LUTEINIZING HORMONE; MEIOSIS; MICE; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; OOCYTES; OVARIAN FOLLICLE; PHOSPHORYLATION; SERINE; TISSUE CULTURE TECHNIQUES;

EID: 58149395024     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.025494     Document Type: Article

References (78)

1. Alcoléa, S., Théveniau-Ruissy, M., Jarry-Guichard, T., Marics, I., Tzonuanacou, E., Chauvin, J. P., Briand, J. P., Moorman, A. F. M., Lamers, W. H. and Gross, D. B. (1999). Downregulation of connexin 45 gene products during mouse heart development. Circ. Res. 84, 1365-1379.
2. Anderson, E., Wilkinson, R. F., Lee, G. and Meller, S. (1978). A correlative microscopical analysis of differentiating ovarian follicles of mammals. J. Morphol. 156, 339-366.
3. Beyer, E. C., Kistler, J., Paul, D. L. and Goodenough, D. A. (1989). Antisera directed against connexin43 pepticles react with a 43-kD protein localized to gap junctions in myocardium and other tissues. J. Cell Biol. 108, 595-605.
4. Borowczyk, E., Johnson, M. L., Bilski, J. J., Bilska, M. A., Redmer D. A., Reynolds, L. P. and Grazul-Bilska, A. T. (2007). Role of gap junctions in regulation of progesterone secretion by ovine luteal cells in vitro. Reproduction 133, 641-651.
5. Cooper, C. D. and Lampe, P. D. (2002). Casein kinase 1 regulates connexin-43 gap junction assembly. J. Biol. Chem. 277, 44962-44968.
6. s signaling pathway Biol. Reprod. 78, 667-672.
7. Doble, B. W., Dang, X., Ping, P., Fandrich, R. R., Nickel, B. E., Jin, Y., Cattini, P. A. and Kardami, E. (2004). Phosphorylation of serine 262 in the gap junction protein connexin-43 regulates DNA synthesis in cell-cell contact forming cardiomyocytes. J. Cell Sci. 117, 507-514.
8. Downs, S. M. and Eppig, J. J. (1987). Induction of mouse oocyte maturation in vivo by perturbants of purine metabolism. Biol. Reprod. 36, 431-437.
9. Downs, S. M. and Chen, J. (2008). EGF-like peptides mediate FSH-induced maturation of cumulus cell-enclosed mouse oocytes. Mol. Reprod. Dev. 75, 105-114.
10. Downs, S. M., Daniel, S. A. J. and Eppig, J. J. (1988). Induction of maturation in cumulus cell-enclosed mouse oocytes by follicle-stimulating hormone and epidermal growth factor: evidence for a positive stimulus of somatic cell origin. J. Exp. Zool. 245, 86-96.
11. Edwards, R. G. (11965). Maturation in vitro of mouse, sheep, cow, pig, rhesus monkey and human ovarian oocytes. Nature 208, 349-351.
12. Eppig, J. J. (1982). The relationship between cumulus cell-oocyte coupling, oocyte meiotic maturation, and cumulus expansion. Dev Biol. 89, 268-272.
13. Eppig, J. J. (1991). Maintenance of meiotic arrest and the induction of oocyte maturation in mouse oocyte-granulosa cell complexes developed in vitro from preantral follicles. Biol. Reprod. 45, 824-830.
14. Eppig, J. J., Viveiros, M. M., Marin-Bivens, C. and De La, Fuente, R. (2004). Regulation of mammalian oocyte maturation. In The Ovary, 2nd edn (ed, P. C. K. Leung and E. Y. Adash), pp. 113-129. San Diego: Elsevier/Academic Press.
15. Favata, M. F. et al. (1998). Identification of a novel inhibitor of mitogen-activated protein kinase kirvase. J. Biol. Chem. 273, 18623-18632.
16. s G protein. J. Cell Biol. 171, 255-265.
17. Galbraith, J. A. and Terasaki, M. (2003). Controlled damage in thick specimens by multiphoton.excitation. Mol. Biol. Cell 14, 1808-1817.
18. 5 subunit, a component of the plasma membrane and yolk platelet membranes. J. Cell Biol. 130, 275-284.
19. Gilufa, N. B., Epstein, M. L. and Beers, W. H. (1978). Cell-to-cell communication and ovulation. J. Cell Biol. 78, 58-75.
20. Gittens, J. E. I. and kidder, G. M. (2005). Differential contributions of connexin37 and connexin43 to oogenesis revealed in chimeric reaggregated mouse ovaries. J. Cell Sci. 118, 5071-5078.
21. Goliger, J. A. and Paul, D. L. (1994). Expression of gap junction proteins Cx26, Cx31. 1, Cx37, and Cx43 in developing and mature rat epidermis. Dev Dyn. 200, 1-13.
22. Granot I. and Dekel, N. (1994). Phosphorylation and expression of connexin-43 ovarian gap junction protein are regulated by luteinizing hormone. J. Biol. Chem. 269, 30502-30509.
23. Haccard, O. and Jessus, C. (2006). Redundant pathways for Cdc2 activation in Xenopus oocyte: either cyclin B or Mos synthesis. EMBO Rep. 7, 321-325.
24. Hambleton, R., Krall, J., Tikishvili, E., Honeggar, M., Ahmad, F., Manganiello, V. C. and Movsesian, M. A. (2005). Isoforms of cyclic nucleciticle phosphodiesterase PDE3 and their contribution to cAMP hydrolytic activity in subcellular fractions of human myocardium. J. Biol. Chem. 280, 39168-39174.
25. Helmchen, F. and Denk, W. (2005). Deep tissue two-photon microscopy. Nat. Meth. 2, 932-940
26. Hinckley, M., Vaccari S., Horner, K., Chen, R. and Conti, M. (2005) The G-protein-coupled receptors GPR3 and GPR12 are involved in cAMP signaling and maintenance of meiotic arrest in rodent oocytes. Dev Biol. 287, 249-261.
27. Horner, K., Livera, G., Hinckley, M., Trinh, K., Storm, D. and Conti, M. (2003). Rodent oocytes express an active adenylyl cyclase required for meiotic arrest. Dev Biol. 258, 385-396.
28. Jaffe, L. A. and Terasaki, M. (2004), Quantitative microinjection of oocytes, eggs, and embryos. Meth. Cell Biol. 74, 219-242.
29. Jaffe, L. A., Norris, R. P., Freudzon. M., Ratzan, W. J. and Mehlmann, L. M. (2009). Microinjection of follicle-enclosed mouse oocytes. Methods Mol. Biol. (in press).
30. Johnson, M. T., Freeman, E. A., Gardner, D., K. and Hunt, P.A. (2007). Oxidative metabolism of pyruvate is required for meiotic maturation of murine oocytes in vivo. Biol. Reprod. 77, 2-8.
31. Jones, K. T. (2008). Meiosis in oocytes: predisposition to aneuploidy and its increased incidence with age. Hum. Reprod. Update 14, 143-158.
32. s protein-mediated pathway. Dev. Biol. 267, 1-13.
33. Kalma, Y., Granot, I., Gallani, D., Barash, A. and Dekel, N. (2004). Luteinizing hormone-induced connexin 43 down-regulation: inhibition of translation. Endocrinology 145, 1617-1624.
34. Khokha, M. K., Yeh, J., Grammer, T. C. and Harland, R. M. (20050-Depletion of three BMP antagonists from Spemann's organizer leads to a catastrophic loss of dorsal structures. Dev Cell 8, 401-411.
35. Kidder, G. M. and Mhawi, A. A. (2002). Gap junctions and ovarian folliculogenesis. Reproduction 123, 613-620.
36. Kirschner, M. and Gerhart, J. (1998). Evolvability. Proc. Natl. Acad. SLi. USA 95, 8420-8427.
37. Laird, D. W. (2006). Life cycle of connexins in health and disease. Biochem. J. 394, 527-543.
38. Lampe, P. D., TenBroek, E. M., Burt, J. M., Kurata, W. E., Johnson, R. G. and Lau, A. F. (2000). Phosphorylation of connexin43 on serine368 by protein kinase C regulates gap junctional communication. J. Cell Biol. 149, 1503-1512.
39. Lampe, P. D., Cooper, C. D., King, T. J. and Burt, J. M. (2006). Analysis of connexin43 phosphorylated at S325, S328 and S330 in normoxic and ischemic heart. J. Cell Sci. 119, 3435-3442.
40. Larsen, W. J., Tung, H. N. and Polking, C. (1981). Response of granulosa cell gap junctions to human chorionic gonadotropin (hCG) at ovulation. Biol. Reprod. 25, 1119-1134.
41. Larsen, W. J., Wert, S. E. and Brunner, G. D. (1987). Differential modulation of rat follicle cell gap junction populations at ovulation. Dev. Biol. 122, 61-71.
42. Ledent, C., Demeestere, I., Blum, D., Petermans, J., Hamalainen, T., Smits, G. and Vassart, G. (2005). Premature ovarian aging in mice deficient for Gpr3. Proc. Natl. Acad. Sci. USA 102, 8922-8926.
43. Li, T. Y., Colley, D., Barr, K. J., Yee, S. P. and Kidder, G. M. (2007). Rescue of oogenesis in Cx37-null mutant mice by oocyte-specific replacement with Cx43. J. Cell Sci. 120, 4117-4125.
44. Lin, R., Warn-Cramer, B. J., Kurata, W. E. and Lau A. F. (2001). v-Src phosphorylation of connexin 43 on Tyr247 and Tyr265 disrupts gap junctional conductance. J. Cell Biol. 154, 815-827.
45. Mantovani, A. (1999). The chemokine system: redundancy for robust outputs. Immunol. Today 20, 254-257.
46. Masciarelli, S., Horner, K., Liu, C., Park, S. H., Hinckley, M., Hockman, S., Nedachi, T., Jin, C., Conti, M. and Manganiello, V. (2004). Cyclic nucleotide phosphodiesterase 3A-deficient mice as a model of female infertility. J. Clin. Invest. 114, 196-205.
47. Mehlmann, L. M. (2005a). Stops and starts in mammalian oocytes: recent advances in understanding the regulation of meiotic arrest and oocyte maturation. Reproduction 130, 791-799.
48. Mehlmann, L. M. (2005b). Oocyte-specific expression of Gpr3 is required for the maintenance of meiotic arrest in mouse oocytes. Dev. Biol. 288, 397-404.
49. s protein in the oocyte. Science 297, 1343-1345.
50. s-linked receptor GPR3 maintains meiotic arrest in mammalian oocytes. Science 306, 1947-1950.
51. s signaling. Dev. Biol. 310, 240-249.
52. Okuma, A., Kuraoka, A., Iida, H., Inai, T., Wasano, K. and Shibata, Y. (1996). Colocalization of connexin 43 and connexin 45 but absence of connexin 40 in granulosa cell gap junctions of rat ovary. J. Reprod. Fertil. 107, 255-264.
53. Panigone, S., Hsieh, M., Fu, M., Persani, L. and Conti, M. (2008). LH signaling in preovulatory follicles involves early activation of the EGFR pathway. Mol. Endocrinol. 22, 924-936.
54. Pincus, G. and Enzmann, E. V. (1935). The comparative behavior of mammalian eggs in vivo and in vitro. J. Exp. Med. 62, 665-675.
55. Piontkewitz, Y. and Dekel, N. (1993). Heptanol, an alkanol that blocks gap junctions, induces oocyte maturation. Endocrine J. 1, 365-372.
56. Racowsky, C. and Satterlie, R. A. (1985). Metabolic, fluorescent dye and electrical coupling between hamster oocytes and cumulus cells during meiotic maturation in vivo and in vitro. Dev. Biol. 108, 191-202.
57. Racowsky, C. and Baldwin, K. V. (1989). In vitro and in vivo studies reveal that hamster oocyte meiotic arrest is maintained only transiently by follicular fluid, but persistently by membrana/cumulus granulosa cell contact. Dev. Biol. 134, 297-306.
58. Ríos-Cardona, D., Ricardo-González, R. R., Chawla, A. and Ferrell, J. E., Jr (2008). A role for GPRx, a novel GPR3/6/ 12-related G-protein coupled receptor, in the maintenance of meiotic arrest in Xenopus laevis oocytes. Dev. Biol. 317, 380-388.
59. Rozental, R., Srinivas, M. and Spray, D. C. (2001). How to close a gap junction channel. Meth. Mol. Biol. 154, 447-476.
60. Schultz, R. M., Montgomery, R. R. and Belanoff, J. R. (1983). Regulation of mouse oocyte meiotic maturation: implication of a decrease in oocyte cAMP and protein dephosphorylation in commitment to resume meiosis. Dev. Biol. 97, 264-273.
61. Sela-Abramovich, S., Chorev, E., Galiani, D. and Dekel, N. (2005). Mitogen-activated protein kinase mediates luteinizing hormone-induced breakdown of communication and oocyte maturation in rat ovarian follicles. Endocrinology 146, 1236-1244.
62. Sela-Abramovich, S., Edry, I., Galiani, D., Nevo, N. and Dekel, N. (2006). Disruption of gap junctional communication within the ovarian follicle induces oocyte maturation. Endocrinology 147, 2280-2286.
63. Sela-Abramovich, S., Galiani, D., Nevo, N. and Dekel, N. (2008). Inhibition of rat oocyte maturation and ovulation by nitric oxide: mechanism of action. Biol. Reprod. 78, 1111-1118.
64. Simon, A. M., Goodenough, D. A., Li, E. and Paul, D. L. (1997). Female infertility in mice lacking connexin 37. Nature 385, 525-529.
65. Simon, A. M., Chen, H. and Jackson, C. L. (2006). Cx37 and Cx43 localize to zona pellucida in mouse ovarian follicles. Cell Commun. Adhes. 13, 61-77.
66. Solan, J. L. and Lampe, P. D. (2008). Connexin43 in LA-25 cells with active v-src is phosphorylated on Y247, Y265, S262, S279/282 and S368 via multiple signaling pathways. Cell Commun. Adhes. 15, 75-84.
67. Solan, J. L., Marquez-Rosado, L., Sorgen, P. L., Thornton, P. J., Gafken, P. R. and Lampe, P. D. (2007). Phosphorylation at S365 is a gatekeeper event that changes the structure of Cx43 and prevents dowregulation by PKC. J. Cell Biol. 179, 1301-1309.
68. Sosinsky, G. E., Solan, J. L., Gaietta, G. M., Ngan, L., Lee, G. J., Mackey, M. R. and Lampe, P. D. (2007). The C-terminus of connexin-43 adopts different conformations in the Golgi and gap junction as detected with structure specific antibodies. Biochem. J. 408, 375-385.
69. Su, Y.-Q., Wigglesworth, K., Pendola, F. L., O'Brien, M. J. and Eppig, J. J. (2002). Mitogen-activated protein kinase activity in cumulus cells is essential for gonadotropin-induced oocyte meiotic resumption and cumulus expansion in the mouse. Endocrinol. 143, 2221-2232.
70. Su, Y.-Q., Denegre, J. M., Wigglesworth, K., Pendola, F. L., O'Brien, M. J. and Eppig, J. J. (2003). Oocyte-dependent activation of mitogen-activated protein kinase (ERK1/2) in cumulus cells is required for the maturation of the mouse oocyte-cumulus cell complex. Dev. Biol. 263, 126-138.
71. v-src-induced inhibition of communication. Cell Regul. 1, 989-1002.
72. Tong, D., Gittens, J. E., Kidder, G. M. and Bai, D. (2006). Patch-clamp study reveals that the importance of connexin43-mediated gap junctional communication for ovarian folliculogenesis is strain specific in the mouse. Am. J. Physiol. Cell. Physiol. 290, C290-C297.
73. Törnell, J., Billig, H. and Hillensjö, T. (1990). Resumption of rat oocyte meiosis is paralleled by a decrease in guanosine 3′, 5′-cyclic monophosphate (cGMP) and is inhibited by microinjection of cGMP. Acta. Physiol. Scand. 139, 511-517.
74. Törnell, J., Billig, H. and Hillensjö, T. (1991). Regulation of oocyte maturation by changes in ovarian levels of cyclic nucleotides. Hum. Reprod. 6, 411-422.
75. Veitch, G. I., Gittens, J. E. I., Shao, Q., Laird, D. W. and Kidder, G. M. (2004). Selective assembly of connexin37 into heterocellular gap junctions at the oocyte/granulosa cell interface. J. Cell Sci. 117, 2699-2707.
76. Warn-Cramer, B. J., Lampe, P. D., Kurata, W. E., Kanemitsu, M. Y., Loo, L. W. M., Eckhart, W. and Lau, A. F. (1996). Characterization of the mitogen-activated protein kinase phosphorylation sites on the connexin-43 gap junction protein. J. Biol. Chem. 271, 3779-3786.
77. Warn-Cramer, B. J., Cottrell, G. T., Burt, J. M. and Lau, A. F. (1998). Regulation of connexin-43 gap junctional intercellular communication by mitogen-activated kinase. J. Biol. Chem. 273, 9188-9196.
78. Weber, P. A., Chang, H.-C., Spaeth, K. E., Nitsche, J. M. and Nicholson, B. J. (2004). The permeability of gap junction channels to probes of different size is dependent on connexin composition and permeant-pore affinities. Biophys. J. 87, 958-973.