Reproductive and Developmental Biology

The Korean Society of Animal Reproduction (한국동물번식학회)
권호 표지

Formation of Chimeric Gap Junction Channels in Mammalian Ovarian Follicle

  • Oh Seunghoon (Department of Physiology, College of Medicine, Dankook University)
  • Published : 2004.09.01
Download PDF
⟨ Previous Next ⟩

Abstract

The oocyte and its surrounding granulosa cells co-exist in a closed compartment called a follicle, although they receive many signals from other parts of the body. It is well established that the intercellular communications between the oocyte and granulosa cells are required for normal oocyte development and ovulation during folliculogenesis. Gap junctions are intercellular channels allowing the direct transmission of ions and small molecules between coupled cells. Several lines of studies have shown that multiple connexins (Cx, subunits of gap junction) are expressed in mammalian ovarian follicles. Among them, two major connexins Cx37 and Cx43 are expressed in different manner. While the gap junction channels formed by Cx37 are localized between the oocyte and encompassing granulosa cells, the intercellular channels by Cx43 are located between granulosa cells. In this review, I will summarize the general properties of gap junction channels and discuss their possible formation (or compatibility) of intercellular channels formed by the oocyte and granulosa cells.

Keywords

References

  1. Ackert CL, Gittens JEI, O'Brien MJ, Eppig JJ, Kidder GM (2001): Intercellular communication via connexin43 gap junctions is required for ovarian folliculogenesis in the mouse. Dev Biol 233:258-270
  2. Bevans CG, Kordel M, Rhee SK, Harris AL (1998): Isoform composition of connexin channels determines selectivity among second messengers and uncharged molecules. J Biol Chem 273:2808-2816 https://doi.org/10.1074/jbc.273.5.2808
  3. Beyer EC, Paul DL, Goodenough DA (1987): Connexin43: a protein from rat heart homologous to a gap junction protein from liver. J Cell Biol 105: 2621-2629 https://doi.org/10.1083/jcb.105.6.2621
  4. Brink PR, Cronin K, Banach K, Peterson E, Westphale EM, Seul KH, Ramanan SV, Beyer EC (1997): Evidence for heteromeric gap junction channels formed from rat connexin43 and human connexin37. Am J Physiol 273 (C1):386-396
  5. Brink PR, Dewey MM (1980): Evidence for fixed charge in the nexus. Nature 285:101-102 https://doi.org/10.1038/285101a0
  6. Bruzzone R, White TW, Paul DL (1996): Connections with connexins: the molecular basis of direct intercellular signaling. Eur J Biochem 238:1-27 https://doi.org/10.1111/j.1432-1033.1996.0001q.x
  7. Chang M, Werner R, Dahl G (1996): A role for an inhibitory connexin in testis? Dev Biol 175:50-56
  8. Elenes S, Rubart M, Moreno AP (1999): Junctional communication between isolated pairs of canine atrial cells is mediated by homogeneous and heterogeneous gap junction channels. J Cardiovasc Electrophysiol 10: 990-1004 https://doi.org/10.1111/j.1540-8167.1999.tb01270.x
  9. Eppig JJ (2001): Oocyte control of ovarian follicular development and function in mammals. Reprod 122: 829-838
  10. Flagg-Newton J, Simpson I, Loewenstein WR (1979): Permeability of the cell-to-cell membrane channels in mammalian cell junction. Science 205:404-407 https://doi.org/10.1126/science.377490
  11. Furshpan EJ, Potter DD (1959): Transmission at the giant motor synapses of the crayfish. J Physiol 145: 289-325 https://doi.org/10.1113/jphysiol.1959.sp006143
  12. Granot I, Bechor E, Barash A, Dekel N (2002): Connexin43 in rat oocytes: developmental modulation of its phosphorylation. BioI Reprod 66:568-573
  13. Grauzul-Bilska AT, Redmer DA, Bilski JJ, JablonkaShariff A, Doraiswamy V, Reynolds LP (1998): Gap junctional proteins, connexin 26, 32, and 43 in sheep ovaries throughout the estrous cycle. Endocrine 8: 269-279 https://doi.org/10.1385/ENDO:8:3:269
  14. Grauzul-Bilska AT, Reynolds LP, Redmer DA (1997): Gap junctions in the ovaries. Biol Reprod 57:947-957 https://doi.org/10.1095/biolreprod57.5.947
  15. 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 BioI Chem 267:17225-17233
  16. Hertzberg EL, Saez JC, Corpina RA, Roy C, Kessler JA (2000): Use of antibodies in the analysis of connexin 43 turnover and phosphorylation. Methods 20:129-139
  17. Hossain MZ, Ao P, Boynton AL (1998): Rapid disruption of. gap junctional communication and phosphorylation of connexin43 by platelet-derived growth factor in T51B rat liver epithelial cells expressing platelet-derived growth factor receptor. J Cell Physiol 174:66-77
  18. Hossain MZ, Jagdale AB, Ao P, Kazlauskas A, Boynton AL (1999): Disruption of gap junctional communication by the platelet-derived growth factor is mediated via multiple signaling pathways. J Biol Chem 274:10489-10496 https://doi.org/10.1074/jbc.274.15.10489
  19. Itahana K, Morikazu Y, Takeya T (1996): Differential expression of four connexin genes, Cx26, Cx3O.3, Cx32, and Cx43, in the porcine ovarian follicle. Endocrinol 137:5036-5044
  20. Jiang JX, Goodenough DA (1996): Heteromeric connexons in lens gap junction channels. Proc Natl Acad Sci USA 93:1287-1291 https://doi.org/10.1073/pnas.93.3.1287
  21. Johnson ML, Redmer DA, Reynolds LP, Crazul-Bilska AT (1999): Expression of gap junctional proteins connexin 43, 32, and 26 throughout follicular development and atresia in cows. Endocrine 10:43-51 https://doi.org/10.1385/ENDO:10:1:43
  22. 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 https://doi.org/10.1095/biolreprod60.5.1263
  23. Kidder GM, Mhawi AA (2002): Gap junctions and ovarian folliculogenesis. Reprod 123:613-620
  24. Kumar NM, Friend DS, Gilula NB (1995): Synthesis and assembly of human beta 1 gap junctions in BHK cells by DNA transfection with the human beta 1 cDNA. J Cell Sci 108:3725-3734
  25. Kumar NM, Gilula NB (1996): The gap junction communication channel. Cell 84:381-388 https://doi.org/10.1016/S0092-8674(00)81282-9
  26. Kuraoka A, Iida H, Hatae T, Shibata Y, Itoh M, Kurita T (1993): Localization of gap junction proteins, connexins 32 and 26, in rat and guinea pig liver as revealed by quick-freeze, deep-etch immunoelectron microscopy. J Histochem Cytochem 41: 971-980 https://doi.org/10.1177/41.7.8390496
  27. Laird DW, Puranam KL, Revel JP (1991): Turnover and phosphorylation dynamics of connexin43 gap junction protein in cultured cardiac myocytes. Biochem J 273:67-72 https://doi.org/10.1042/bj2730067
  28. Lau AF, Kanemitsu MY, Kurata WE, Danesh S, Boynton AL (1992): Epidermal growth factor disrupts gap-junctional communication and induces phosphorylation of connexin43 on serine. Mol Biol Cell 3:865-874 https://doi.org/10.1091/mbc.3.8.865
  29. Massas R, Korenstein R, Benayahu D (1998): Estrogen modulation of osteoblastic cell-to-cell communication. J Cell Biochem 69:282-290 https://doi.org/10.1002/(SICI)1097-4644(19980601)69:3<282::AID-JCB6>3.0.CO;2-N
  30. Moorby CD, Gherardi E (1999): Expression of a Cx43 deletion mutant in 3T3 A31 fibroblasts prevents PDGF-induced inhibition of cell communication and suppresses cell growth. Exp Cell Res 249:367-376 https://doi.org/10.1006/excr.1999.4485
  31. Moreno AP, Rook MB, Fishman GI, Spray DC (1994): Gap junction channels: distinct voltage-sensitive and -insensitive conductance states. Biophys J 67:113-119 https://doi.org/10.1016/S0006-3495(94)80460-6
  32. Musil LS, Goodenough DA (1993): Multisubunit assembly of an integral plasma membrane channel protein, gap junction connexin43, occurs after exit from the ER. Cell 74:1065-1077 https://doi.org/10.1016/0092-8674(93)90728-9
  33. Oh S, Abrams CK, Verselis VK, Bargiello TA (2000): Stoichiometry of transjunctional voltage-gating polarity reversal by a negative charge substitution in the amino terminus of a connexin32 chimera. J Gen Physiol 116:13-31
  34. Patino R, Kagawa H (1999): Regulation of gap junctions and oocyte maturational competence by gonadotropin and insulin-like growth factor-I in ovarian follicles of red seabream. Gen Camp Endocrinol 115:454-462 https://doi.org/10.1006/gcen.1999.7341
  35. Paul DL (1986): Molecular cloning of cDNA for rat liver gap junction protein. J Cell BioI 103:123-134
  36. Reaume A, De Sousa PA, Kulkarni S, Langille BL, Zhu D, Davies TC, Juneja SC, Kidder GM, Rossant J (1995): Cardiac malformation in neonatal mice lacking connexin 43. Science 267:1831-1834 https://doi.org/10.1126/science.7892609
  37. Simon AM, Goodenough DA, Li E, Paul DL (1997): Female infertility in mice lacking connexin 37. Nature 385:525-529 https://doi.org/10.1038/385525a0
  38. Simpson I, Rose B, Loewenstein WR (1977): Size limit of molecules permeating the junctional membrane channels. Science 195:294-296 https://doi.org/10.1126/science.831276
  39. Sohl G, Willecke K (2004): Gap junctions and the connexin protein family. Cardiovas Res 62:228-232
  40. Stauffer KA (1995): The gap junction proteins beta 1-connexin (connexin-32) and beta 2-connexin (connexin-26) can form heteromeric hemichannels. J Biol Chem 270:6768-6772
  41. Unger VM, Kumar NM, Gilula NB, Yeager M (1999): Three-dimensional structure of a recombinant gap junction membrane channel. Science 283:1176-1180 https://doi.org/10.1126/science.283.5405.1176
  42. Veitch GI, Gittens JEI, Shao Q, Laird DW, Kidder GM (2004): Selective assembly of connexin37 into heterocellular gap junctions at the oocyte/granulosa cell interface. J Cell Sci 117:2699-2707
  43. Verselis VK, Veenstra RD (2000): Gap junction channels: permeability and voltage gating. In; Advanced Molecular and Cell Biology, E.L. Hertzberg (Ed.), Vol. 30, JAI Press Inc., Stamford, USA. pp:129-192
  44. Waltzman MN (1996): Biophysical properties of rat connexin37 stably expressed in N2A cell lines. Ph.D. thesis. Albert Einstein College of Medicine of Yeshiva University, New York, USA
  45. Warn-Cramer BJ, Cottrell GT, Burt JM, Lau AF (1998): Regulation of connexin-43 gap junctional intercellular communication by mitogen-activated protein kinase. J Biol Chem 273:9188-9196 https://doi.org/10.1074/jbc.273.15.9188
  46. Warn-Cramer BJ, Lampe PD, Kurata WE, Kanemitsu MY, Loo LW, Eckhart W, Lau AF (1996): Characterization of the mitogen-activated protein kinase phosphorylation sites on the connexin-43 gap junction protein. J Biol Chem 271:3779-3786 https://doi.org/10.1074/jbc.271.7.3779