FSH induces the development of circadian clockwork in rat granulosa cells via a gap junction protein Cx43-dependent pathway

American Journal of Physiology - Endocrinology and Metabolism

Volumn 304, Issue 6, 2013, Pages

  Chen, Huatao ^a   Zhao, Lijia ^a   Chu, Guiyan ^a   Kito, Gakushi ^a   Yamauchi, Nobuhiko ^a   Shigeyoshi, Yasufumi ^b   Hashimoto, Seiichi ^c   Hattori, Masa aki ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b KINKI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

Carbenoxolone; Clock genes; Granulosa cell; Lindane

Indexed keywords

CARBENOXOLONE; CHORIONIC GONADOTROPIN; CONNEXIN 43; DEXAMETHASONE; FOLLITROPIN; GAP JUNCTION PROTEIN; LINDANE; NUCLEAR RECEPTOR NR1D1; PER2 PROTEIN; PROTEIN BMAL1; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; AGENTS AFFECTING WATER, MOLECULE OR ION TRANSPORT; CIRCADIAN RHYTHM SIGNALING PROTEIN; CONNEXIN 43 PROTEIN, RAT; GLUCOCORTICOID; LUTEINIZING HORMONE RECEPTOR; PER2 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL MATURATION; CIRCADIAN RHYTHM; FEMALE; GENE EXPRESSION; GRANULOSA CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARY; PRIORITY JOURNAL; RAT; REPORTER GENE; SIGNAL TRANSDUCTION; ANIMAL; BIOSYNTHESIS; CELL CULTURE; CELL DIFFERENTIATION; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; GAP JUNCTION; GENETICS; METABOLISM; TRANSGENIC RAT; UPREGULATION;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; CHORIONIC GONADOTROPIN; CIRCADIAN CLOCKS; CIRCADIAN RHYTHM SIGNALING PEPTIDES AND PROTEINS; CONNEXIN 43; DEXAMETHASONE; FEMALE; FOLLICLE STIMULATING HORMONE; GABA-A RECEPTOR ANTAGONISTS; GAP JUNCTIONS; GENES, REPORTER; GLUCOCORTICOIDS; GRANULOSA CELLS; MEMBRANE TRANSPORT MODULATORS; MICE; PERIOD CIRCADIAN PROTEINS; RATS; RATS, TRANSGENIC; RECEPTORS, LH; UP-REGULATION;

MLCS; MLOWN;

EID: 84877306589     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00432.2012     Document Type: Article

References (73)

1. Alvarez JD, Hansen A, Ord T, Bebas P, Chappell PE, Giebultowicz JM, Williams C, Moss S, Sehgal A. The circadian clock protein BMAL1 is necessary for fertility and proper testosterone production in mice. J Biol Rhythms 23: 26-36, 2008.
2. Atkinson SE, Maywood ES, Chesham JE, Wozny C, Colwell CS, Hastings MH, Williams SR. Cyclic AMP signaling control of action potential firing rate and molecular circadian pacemaking in the suprachiasmatic nucleus. J Biol Rhythms 26: 210-220, 2011.
3. Balsalobre A. Clock genes in mammalian peripheral tissues. Cell Tissue Res 309: 193-199, 2002.
4. Balsalobre A, Brown SA, Marcacci L, Tronche F, Kellendonk C, Reichardt HM, Schutz G, Schibler U. Resetting of circadian time in peripheral tissues by glucocorticoid signaling. Science 289: 2344-2347, 2000.
5. Balsalobre A, Marcacci L, Schibler U. Multiple signaling pathways elicit circadian gene expression in cultured Rat-1 fibroblasts. Curr Biol 10: 1291-1294, 2000.
6. Berthoud VM, Hall DH, Strahsburger E, Beyer EC, Saez JC. Gap junctions in the chicken pineal gland. Brain Res 861: 257-270, 2000.
7. Beyer EC, Paul DL, Goodenough DA. Connexin family of gap junction proteins. J Membr Biol 116: 187-194, 1990.
8. Boden MJ, Varcoe TJ, Voultsios A, Kennaway DJ. Reproductive biology of female Bmal1 null mice. Reproduction 139: 1077-1090, 2010.
9. Caruso RL, Upham BL, Harris C, Trosko JE. Biphasic lindane-induced oxidation of glutathione and inhibition of gap junctions in myometrial cells. Toxicol Sci 86: 417-426, 2005.
10. Chen HT, Chu GY, Zhao LJ, Yamauchi N, Shigeyoshi Y, Hashimoto S, Hattori MA. Rev-erb alpha regulates circadian rhythms and StAR expression in rat granulosa cells as identified by the agonist GSK4112. Biochem Biophys Res Commun 420: 374-379, 2012.
11. Chu GY, Misawa I, Chen HT, Yamauchi N, Shigeyoshi Y, Hashimoto S, Hattori MA. Contribution of FSH and triiodothyronine to the development of circadian clocks during granulosa cell maturation. Am J Physiol Endocrinol Metab 302: E645-E653, 2012.
12. Chu GY, Yoshida K, Narahara S, Uchikawa M, Kawamura M, Yamauchi N, Xi YM, Shigeyoshi Y, Hashimoto S, Hattori MA. Alterations of circadian clockworks during differentiation and apoptosis of rat ovarian cells. Chronobiol Int 28: 477-487, 2011.
13. Colwell CS. Rhythmic coupling among cells in the suprachiasmatic nucleus. J Neurobiol 43: 379-388, 2000.
14. Defamie N, Mograbi B, Roger C, Cronier L, Malassine A, Brucker-Davies F, Fenichel P, Segretain D, Pointis G. 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, 2001.
15. Dey A, Kusljic S, Lang RJ, Exintaris B. Role of connexin 43 in the maintenance of spontaneous activity in the guinea pig prostate gland. Br J Pharmacol 161: 1692-1707, 2010.
16. Fahrenkrug J, Georg B, Hannibal J, Hindersson P, Gras S. Diurnal rhythmicity of the clock genes Per1 and Per2 in the rat ovary. Endocrinology 147: 3769-3776, 2006.
17. Gershon E, Plaks V, Dekel N. Gap junctions in the ovary: expression, localization and function. Mol Cell Endocrinol 282: 18-25, 2008.
18. Gittens JEI, Mhawi AA, Lidington D, Ouellette Y, Kidder GM. Functional analysis of gap junctions in ovarian granulosa cells: distinct role for connexin43 in early stages of folliculogenesis. Am J Physiol Cell Physiol 284: C880-C887, 2003.
19. Goldberg GS, Valiunas V, Brink PR. Selective permeability of gap junction channels. Biochim Biophys Acta 1662: 96-101, 2004.
20. Granot I, Dekel N. Developmental expression and regulation of the gap junction protein and transcript in rat ovaries. Mol Reprod Dev 47: 231-239, 1997.
21. GrazulBilska AT, Reynolds LP, Redmer DA. Gap junctions in the ovaries. Biol Reprod 57: 947-957, 1997.
22. Guan XJ, Bonney WJ, Ruch RJ. Changes in gap junction permeability, gap junction number, and connexin43 expression in lindane-treated ratliver epithelial-cells. Toxicol Appl Pharmcol 130: 79-86, 1995.
23. Hattori MA, Sakamoto K, Fujihara N, Kojima I. Nitric oxide: a modulator for the epidermal growth factor receptor expression in developing ovarian granulosa cells. Am J Physiol Cell Physiol 270: C812-C818, 1996.
24. He PJ, Hirata M, Yamauchi N, Hashimoto S, Hattori MA. The disruption of circadian clockwork in differentiating cells from rat reproductive tissues as identified by in vitro real-time monitoring system. J Endocrinol 193: 413-420, 2007.
25. He PJ, Hirata M, Yamauchi N, Hashimoto S, Hattori MA. Gonadotropic regulation of circadian clockwork in rat granulosa cells. Mol Cell Biochem 302: 111-118, 2007.
26. Izumo M, Johnson CH, Yamazaki S. Circadian gene expression in mammalian fibroblasts revealed by real-time luminescence reporting: temperature compensation and damping. Proc Natl Acad Sci USA 100: 16089-16094, 2003.
27. Izumo M, Sato TR, Straume M, Johnson CH. Quantitative analyses of circadian gene expression in mammalian cell cultures. PLos Comput Biol 2: 1248-1261, 2006.
28. Johnson ML, Redmer DA, Reynolds LP, Bilski JJ, Grazul-Bilska AT. Gap junctional intercellular communication of bovine granulosa and thecal cells from antral follicles: effects of luteinizing hormone and folliclestimulating hormone. Endocrine 18: 261-270, 2002.
29. Juneja SC, Barr KJ, Enders GC, Kidder GM. Defects in the germ line and gonads of mice lacking connexin43. Biol Reprod 60: 1263-1270, 1999.
30. Kallen CB, Billheimer JT, Summers SA, Stayrook SE, Lewis M, Strauss JF. Steroidogenic acute regulatory protein (StAR) is a sterol transfer protein. J Biol Chem 273: 26285-26288, 1998.
31. Karman BN, Tischkau SA. Circadian clock gene expression in the ovary: Effects of luteinizing hormone. Biol Reprod 75: 624-632, 2006.
32. Ke FC, Fang SH, Lee MT, Sheu SY, Lai SY, Chen YJ, Huang FL, Wang PS, Stocco DM, Hwang JJ. Lindane, a gap junction blocker, suppresses FSH and transforming growth factor beta 1-induced con-nexin43 gap junction formation and steroidogenesis in rat granulosa cells. J Endocrinol 184: 555-566, 2005.
33. Kumar NM, Gilula NB. The gap junction communication channel. Cell 84: 381-388, 1996.
34. Lee Y, Lee J, Kwon I, Nakajima Y, Ohmiya Y, Son GH, Lee KH, Kim K. Coactivation of the CLOCK-BMAL1 complex by CBP mediates resetting of the circadian clock. J Cell Sci 123: 3547-3557, 2010.
35. Liu AC, Welsh DK, Ko CH, Tran HG, Zhang EE, Priest AA, Buhr ED, Singer O, Meeker K, Verma IM, Doyle FJ, Takahashi JS, Kay SA. Intercellular coupling confers robustness against mutations in the SCN circadian clock network. Cell 129: 605-616, 2007.
36. Lo CW. Genes, gene knockouts, and mutations in the analysis of gap junctions. Dev Genet 24: 1-4, 1999.
37. Long MA, Jutras MJ, Connors BW, Burwell RD. Electrical synapses coordinate activity in the suprachiasmatic nucleus. Nat Neurosci 8: 61-66, 2005.
38. Mayerhofer A, Garfield RE. Immunocytochemical analysis of the expression of gap junction protein connexin-43 in the rat ovary. Mol Reprod Dev 41: 331-338, 1995.
39. Melton CM, Zaunbrecher GM, Yoshizaki G, Patino R, Whisnant S, Rendon A, Lee VH. Expression of connexin 43 mRNA and protein in developing follicles of prepubertal porcine ovaries. Comp Biochem Phys B 130: 43-55, 2001.
40. Michon L, Nlend RN, Bavamian S, Bischoff L, Boucard N, Caille D, Cancela J, Charollais A, Charpantier E, Klee P, Peyrou M, Populaire C, Zulianello L, Meda P. Involvement of gap junctional communication in secretion. Biochim Biophys Acta 1719: 82-101, 2005.
41. Morgan LW, Greene AV, Bell-Pedersen D. Circadian and light-induced expression of luciferase in Neurospora crassa. Fungal Genet Biol 38: 327-332, 2003.
42. Nakamura T, Sellix M, Kudo T, Nakao N, Yoshimura T, Ebihara S, Colwell C, Block G. Influence of the estrous cycle on clock gene expression in reproductive tissues: effects of fluctuating ovarian steroid hormone levels. Steroids 75: 203-212, 2010.
43. Nakao N, Yasuo S, Nishimura A, Yamamura T, Watanabe T, Anraku T, Okano T, Fukada Y, Sharp PJ, Ebihara S, Yoshimura T. Circadian clock gene regulation of steroidogenic acute regulatory protein gene expression in preovulatory ovarian follicles. Endocrinology 148: 3031-3038, 2007.
44. Nelson W, Tong YL, Lee JK, Halberg F. Methods for cosinor-rhythmometry. Chronobiologia 6: 305-323, 1979.
45. Noguchi T, Wang CW, Pan HY, Welsh DK. Fibroblast circadian rhythms of PER2 expression depend on membrane potential and intracellular calcium. Chronobiol Int 29: 653-664, 2012.
46. Nunez BS, Evans AN. Hormonal regulation of the steroidogenic acute regulatory protein (StAR) in gonadal tissues of the Atlantic croaker (Micropogonias undulatus). Gen Comp Endocrinol 150: 495-504, 2007.
47. 2+ signalling in mammalian circadian timekeeping. Biochem Soc Trans 40: 44-50, 2012.
48. Pulivarthy SR, Tanaka N, Welsh DK, De Haro L, Verma IM, Panda S. Reciprocity between phase shifts and amplitude changes in the mammalian circadian clock. Proc Natl Acad Sci USA 104: 20356-20361, 2007.
49. Reinhart AJ, Williams SC, Stocco DM. Transcriptional regulation of the StAR gene. Mol Cell Endocrinol 151: 161-169, 1999.
50. Sandhoff TW, McLean MP. Hormonal regulation of steroidogenic acute regulatory (StAR) protein messenger ribonucleic acid expression in the rat ovary. Endocrine 4: 259-267, 1996.
51. Schneider NL, Stengl M. Gap junctions between accessory medulla neurons appear to synchronize circadian clock cells of the cockroach Leucophaea maderae. J Neurobiol 95: 1996-2002, 2006.
52. Shimizu T, Hirai Y, Murayama C, Miyamoto A, Miyazaki H, Miyazaki K. Circadian Clock genes Per2 and clock regulate steroid production, cell proliferation, and luteinizing hormone receptor transcription in ovarian granulosa cells. Biochem Biophys Res Commun 412: 132-135, 2011.
53. Shinohara K, Funabashi T, Mitushima D, Kimura F. Effects of gap junction blocker on vasopressin and vasoactive intestinal polypeptide rhythms in the rat suprachiasmatic nucleus in vitro. Neurosci Res 38: 43-47, 2000.
54. Sommersberg B, Bulling A, Salzer U, Frohlich U, Garfield RE, Amsterdam A, Mayerhofer A. Gap junction communication and connexin 43 gene expression in a rat granulosa cell line: Regulation by follicle-stimulating hormone. Biol Reprod 63: 1661-1668, 2000.
55. Stocco DM, Clark BJ. Role of the steroidogenic acute regulatory protein (StAR) in steroidogenesis. Biochem Pharmacol 51: 197-205, 1996.
56. Sun JD, Liu Y, Yuan YH, Li J, Chen NH. Gap junction dysfunction in the prefrontal cortex induces depressive-like behaviors in rats. Neuropsychopharmacology 37: 1305-1320, 2012.
57. Teilmann SC. Differential expression and localisation of connexin-37 and connexin-43 in follicles of different stages in the 4-week-old mouse ovary. Mol Cell Endocrinol 234: 27-35, 2005.
58. Tetsuka M, Milne M, Simpson GE, Hillier SG. Expression of 11 beta-hydroxysteroid dehydrogenase, glucocorticoid receptor, and mineralocorticoid receptor genes in rat ovary. Biol Reprod 60: 330-335, 1999.
59. 2+/cAMP response element-binding protein (CREB)-dependent activation of Per1 is required for light-induced signaling in the Suprachiasmatic nucleus circadian clock. J Biol Chem 278: 718-723, 2003.
60. Torres-Farfan C, Mendez N, Abarzua-Catalan L, Vilches N, Valenzuela GJ, Seron-Ferre M. A circadian clock entrained by melatonin is ticking in the rat fetal adrenal. Endocrinology 152: 1891-1900, 2011.
61. Ueda HR, Chen WB, Adachi A, Wakamatsu H, Hayashi S, Takasugi T, Nagano M, Nakahama K, Suzuki Y, Sugano S, Iino M, Shigeyoshi Y, Hashimoto S. A transcription factor response element for gene expression during circadian night. Nature 418: 534-539, 2002.
62. Ueyama T, Krout KE, Van Nguyen X, Karpitskiy V, Kollert A, Mettenleiter TC, Loewy AD. Suprachiasmatic nucleus: a central autonomic clock. Nat Neurosci 2: 1051-1053, 1999.
63. Vandenpol AN, Dudek FE. Cellular communication in the circadian clock, the suprachiasmatic nucleus. Neuroscience 56: 793-811, 1993.
64. Wang JW, Zhou TS. cAMP-regulated dynamics of the mammalian circadian clock. Biosystems 101: 136-143, 2010.
65. Welsh DK, Yoo SH, Liu AC, Takahashi JS, Kay SA. Bioluminescence imaging of individual fibroblasts reveals persistent, independently phased circadian rhythms of clock gene expression. Curr Biol 14: 2289-2295, 2004.
66. Wilsbacher LD, Yamazaki S, Herzog ED, Song EJ, Radcliffe LA, Abe M, Block G, Spitznagel E, Menaker M, Takahashi JS. Photic and circadian expression of luciferase in mPeriod1-luc transgenic mice in vivo. Proc Natl Acad Sci USA 99: 489-494, 2002.
67. Wright CS, Becker DL, Lin JS, Warner AE, Hardy K. Stage-specific and differential expression of gap junctions in the mouse ovary: connexinspecific roles in follicular regulation. Reproduction 121: 77-88, 2001.
68. Yamamoto T, Nakahata Y, Soma H, Akashi M, Mamine T, Takumi T. Transcriptional oscillation of canonical clock genes in mouse peripheral tissues (Abstract). BMC Mol Biol 5: 18, 2004.
69. Yamazaki S, Numano R, Abe M, Hida A, Takahashi R, Ueda M, Block GD, Sakaki Y, Menaker M, Tei H. Resetting central and peripheral circadian oscillators in transgenic rats. Science 288: 682-685, 2000.
70. Yamazaki S, Takahashi JS. Real-time luminescence reporting of circadian gene expression in mammals. Method Enzymol 393: 288-301, 2005.
71. Yoo SH, Yamazaki S, Lowrey PL, Shimomura K, Ko CH, Buhr ED, Siepka SM, Hong HK, Oh WJ, Yoo OJ, Menaker M, Takahashi JS. PERIOD2::LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc Natl Acad Sci USA 101: 5339-5346, 2004.
72. Yoshikawa T, Sellix M, Pezuk P, Menaker M. Timing of the ovarian circadian clock is regulated by gonadotropins. Endocrinology 150: 4338-4347, 2009.
73. Zhang Y, Semple-Rowland SL. Rhythmic expression of clock-controlled genes in retinal photoreceptors is sensitive to 18-beta-glycyrrhetnic acid and 18-alpha-glycyrrhetnic acid-3-hemisuccinate. Mol Brain Res 135: 30-39, 2005.