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Chronobiology International
The Journal of Biological and Medical Rhythm Research
Volume 32, 2015 - Issue 6
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Original Article

Integration of the nuclear receptor REV-ERBα linked with circadian oscillators in the expressions of Alas1, Ppargc1a, and Il6 genes in rat granulosa cells

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Pages 739-749 | Received 22 Dec 2014, Accepted 15 Apr 2015, Published online: 23 Jun 2015

References

  • Abrahamson EE, Moore RY. (2001). Suprachiasmatic nucleus in the mouse: Retinal innervation, intrinsic organization and efferent projections. Brain Res. 916:172–91
  • Alvarez JD, Hansen A, Ord T, et al (2008). The circadian clock protein BMAL1 is necessary for fertility and proper testosterone production in mice. J Biol Rhythms. 23:26–36
  • Boden MJ, Varcoe TJ, Voultsios A, Kennaway DJ. (2010). Reproductive biology of female Bmal1 null mice. Reproduction. 139:1077–90
  • Bugge A, Feng D, Everett LJ, et al. (2012). Rev-erbα and Rev-erbβ coordinately protect the circadian clock and normal metabolic function. Genes Dev. 26:657–67
  • Burris TP, Kojetin DJ. (2011). A role for Rev-erbα ligands in the regulation of adipogenesis. Curr Pharm Des. 17:320–4
  • Chen HT, Chu GY, Zhao LJ, et al. (2012). Rev-erbα regulates circadian rhythms and StAR expression in rat granulosa cells as identified by the agonist GSK4112. Biochem Biophys Res Commun. 420:374–9
  • Chen HT, Zhao LJ, Chu GY, et al. (2013a). FSH induces the development of circadian clockwork in rat granulosa cells via a gap junction protein Cx43-dependent pathway. Am J Physiol Endocrinol Metab. 304:E566–75
  • Chen HT, Zhao LJ, Kumazawa M, et al. (2013b). Downregulation of core clock gene Bmal1 attenuates expression of progesterone and prostaglandin biosynthesis-related genes in rat luteinizing granulosa cells. Am J Physiol Cell Physiol. 304:C1131–40
  • Chini CCS, Escande C, Nin V, Chini EN. (2013). DBC1 (Deleted in Breast Cancer 1) modulates the stability and function of the nuclear receptor Rev-erbα. Biochem J. 451:453–61
  • Cho H, Zhao X, Hatori M, et al. (2012). Regulation of circadian behaviour and metabolism by REV-ERB-α and REV-ERB-β. Nature. 485:123–7
  • Chomez P, Neveu I, Mansen A, et al. (2000). Increased cell death and delayed development in the cerebellum of mice lacking the rev-erbAα orphan receptor. Development. 127:1489–98
  • Chu GY, Misawa I, Chen HT, et al. (2012). Contribution of FSH and triiodothyronine to the development of circadian clocks during granulosa cell maturation. Am J Physiol Endocrinol Metab. 302:E645–53
  • Chu GY, Yoshida K, Narahara S, et al. (2011). Alterations of circadian clockworks during differentiation and apoptosis of rat ovarian cells. Chronobiol Int. 28:477–87
  • Crumbley C, Burris TP. (2011). Direct regulation of Clock expression by REV-ERB. PLoS One. 6:e17290
  • Dibner C, Schibler U, Albrecht U. (2010). The mammalian circadian timing system: Organization and coordination of central and peripheral clocks. Annu Rev Physiol. 72:517–49
  • Fahrenkrug J, Georg B, Hannibal J, et al. (2006). Diurnal rhythmicity of the clock genes Per1 and Per2 in the rat ovary. Endocrinology. 147:3769–76
  • Feng D, Liu T, Sun Z, et al. (2011). A circadian rhythm orchestrated by histone deacetylase 3 controls hepatic lipid metabolism. Science. 331:1315–9
  • Fontaine C, Dubois G, Duguay Y, et al. (2003). The orphan nuclear receptor Rev-Erbα is a peroxisome proliferator-activated receptor (PPAR) γ target gene and promotes PPARγ-induced adipocyte differentiation. J Biol Chem. 278:37672–80
  • Gerhart-Hines Z, Feng D, Emmett MJ, et al. (2013). The nuclear receptor Rev-erbα controls circadian thermogenic plasticity. Nature. 503:410–13
  • Gibbs JE, Blaikley J, Beesley S, et al. (2012). The nuclear receptor REV-ERBα mediates circadian regulation of innate immunity through selective regulation of inflammatory cytokines. Proc Natl Acad Sci USA. 109:582–7
  • Gorospe WC, Hughes FM, Jr Spangelo BL. (1992). Interleukin-6: Effects on and production by rat granulosa cells in vitro. Endocrinology. 130:1750–2
  • Grant D, Yin L, Collins JL, et al. (2010). GSK4112, a small molecule chemical probe for the cell biology of the nuclear heme receptor Rev-erbα. ACS Chem Biol. 5:925–32
  • Handschin C, Spiegelman BM. (2006). Peroxisome proliferator-activated receptor γ coactivator 1 coactivators, energy homeostasis, and metabolism. Endocr Rev. 27:728–35
  • He PJ, Hirata M, Yamauchi N, et al. (2007). Gonadotropic regulation of circadian clockwork in rat granulosa cells. Mol Cell Biochem. 302:111–18
  • Isayama K, Chen HT, Yamauchi N, Hattori M-A. (2014). REV-ERBα inhibits the PTGS2 expression in bovine uterus endometrium stromal and epithelial cells exposed to ovarian steroids. J Reprod Dev. 60:362–70
  • Isayama K, Zhao LJ, Chen HT, et al. (2015). Removal of REV-ERBα inhibition contributes to the prostaglandin G/H synthase 2 expression in rat endometrial stromal cells. Am J Physiol Endocrinol Metab. 308:E650–661
  • Jo MS, Gieske MC, Payne CE, et al. (2004). Development and application of a rat ovarian gene expression database. Endocrinology. 145:5384–96
  • Ju YF, Mizutani T, Imamichi Y, et al. (2012). Nuclear receptor 5A (NR5A) family regulates 5-aminolevulinic acid synthase 1 (ALAS1) gene expression in steroidogenic cells. Endocrinology. 153:5522–34
  • Kaasik K, Lee CC. (2004). Reciprocal regulation of haem biosynthesis and the circadian clock in mammals. Nature. 430:467–71
  • Karman BN, Tischkau SA. (2006). Circadian clock gene expression in the ovary: Effects of luteinizing hormone. Biol Reprod. 75:624–32
  • Kojetin D, Wang Y, Kamenecka TM, Burris TP. (2011). Identification of SR8278, a synthetic antagonist of the nuclear heme receptor REV-ERB. ACS Chem Biol. 6:131–4
  • Kumar N, Solt LA, Wang Y, et al. (2010). Regulation of adipogenesis by natural and synthetic REV-ERB ligands. Endocrinology. 151:3015–25
  • Laitinen S, Fontaine C, Fruchart JC, Staels B. (2005). The role of the orphan nuclear receptor Rev-erbα in adipocyte differentiation and function. Biochimie. 87:21–5
  • Liu C, Li SM, Liu TH, et al. (2007). Transcriptional coactivator PGC-1α integrates the mammalian clock and energy metabolism. Nature. 447:477–81
  • Machelon V, Emilie D, Lefevre A, et al. (1994). Interleukin-6 Biosynthesis in human preovulatory follicles: Some of its potential roles at ovulation. J Clin Endocrinol Metab. 79:633–42
  • Meng QJ, McMaster A, Beesley S, et al. (2008). Ligand modulation of REV-ERBα function resets the peripheral circadian clock in a phasic manner. J Cell Sci. 121:3629–35
  • Miyajima N, Horiuchi R, Shibuya Y, et al. (1989). Two erbA homologs encoding proteins with different T3 binding capacities are transcribed from opposite DNA strands of the same genetic locus. Cell. 57:31–9
  • Miyajima N, Kadowaki Y, Fukushige S, et al. (1988). Identification of two novel members of erbA superfamily by molecular cloning: The gene products of the two are highly related to each other. Nucleic Acids Res. 16:11057–74
  • Nakamura TJ, Sellix MT, Kudo T, et al. (2010). Influence of the estrous cycle on clock gene expression in reproductive tissues: Effects of fluctuating ovarian steroid hormone levels. Steroids. 75:203–12
  • Nakao N, Yasuo S, Nishimura A, et al. (2007). Circadian clock gene regulation of steroidogenic acute regulatory protein gene expression in preovulatory ovarian follicles. Endocrinology. 148:3031–8
  • Nelson W, Tong YL, Lee JK, Halberg F. (1979). Methods for cosinor-rhythmometry. Chronobiologia. 6:305–23
  • Phelan CA, Gampe RT, Lambert MH, et al. (2010). Structure of Rev-erbα bound to N-CoR reveals a unique mechanism of nuclear receptor-co-repressor interaction. Nat Struct Mol Biol. 17:808–15
  • Portaluppi F, Smolensky MH, Touitou Y. (2010). Ethics and methods for biological rhythm research on animals and human beings. Chronobiol Int. 27:1911–29
  • Preitner N, Damiola F, Molina LL, et al. (2002). The orphan nuclear receptor REV-ERBα controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell. 110:251–60
  • Raghuram S, Stayrook KR, Huang PX, et al. (2007). Identification of heme as the ligand for the orphan nuclear receptors REV-ERBα and REV-ERBβ. Nat Struct Mol Biol. 14:1207–13
  • Ralph MR, Foster RG, Davis FC, Menaker M. (1990). Transplanted suprachiasmatic nucleus determines circadian period. Science. 247:975–8
  • Ratajczak CK, Boehle KL, Muglia LJ. (2009). Impaired steroidogenesis and implantation failure in Bmal1−/− Mice. Endocrinology. 150:1879–85
  • Rogers PM, Ying L, Burris TP. (2008). Relationship between circadian oscillations of Rev-erbα expression and intracellular levels of its ligand, heme. Biochem Biophys Res Commun. 368:955–8
  • Sato S, Sakurai T, Ogasawara J, et al. (2014). Direct and indirect suppression of interleukin-6 gene expression in murine macrophages by nuclear orphan receptor REV-ERBα. Sci World J. 2014:685854
  • Shimizu T, Hirai Y, Murayama C, et al. (2011). Circadian clock genes Per2 and Clock regulate steroid production, cell proliferation, and luteinizing hormone receptor transcription in ovarian granulosa cells. Biochem Biophys Res Commun. 412:132–5
  • Silver R, LeSauter J, Tresco PA, Lehman MN. (1996). A diffusible coupling signal from the transplanted suprachiasmatic nucleus controlling circadian locomotor rhythms. Nature. 382:810–13
  • Solt LA, Wang YJ, Banerjee S, et al. (2012). Regulation of circadian behaviour and metabolism by synthetic REV-ERB agonists. Nature. 485:62–8
  • Stephan FK, Zucker I. (1972). Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proc Natl Acad Sci USA. 69:1583–6
  • Tasaki H, Zhao LJ, Isayama K, et al. (2015). Inhibitory role of REV-ERBα in the expression of bone morphogenetic protein gene family in rat uterus endometrium stromal cells. Am J Physiol Cell Physiol. 308:C528--38
  • Tosini G, Menaker M. (1996). Circadian rhythms in cultured mammalian retina. Science. 272:419–21
  • Triqueneaux G, Thenot S, Kakizawa T, et al. (2004). The orphan receptor Rev-erbα gene is a target of the circadian clock pacemaker. J Mol Endocrinol. 33:585–608
  • Ueda HR, Chen WB, Adachi A, et al. (2002). A transcription factor response element for gene expression during circadian night. Nature. 418:534–9
  • Van der Hoek KH, Woodhouse CM, Brannstrom M, Norman RJ. (1998). Effects of interleukin (IL)-6 on luteinizing hormone- and IL-1β-induced ovulation and steroidogenesis in the rat ovary. Biol Reprod. 58:1266–71
  • Welsh DK, Logothetis DE, Meister M, Reppert SM. (1995). Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms. Neuron. 14:697–706
  • Wu N, Yin L, Hanniman EA, et al. (2009). Negative feedback maintenance of heme homeostasis by its receptor, Rev-erbα. Genes Dev. 23:2201–9
  • Wu ZD, Puigserver P, Andersson U, et al. (1999). Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell. 98:115–24
  • Yamazaki S, Numano R, Abe M, et al. (2000). Resetting central and peripheral circadian oscillators in transgenic rats. Science. 288:682–5
  • Yin L, Lazar MA. (2005). The orphan nuclear receptor Rev-erbα recruits the N-CoR/histone deacetylase 3 corepressor to regulate the circadian Bmal1 gene. Mol Endocrinol. 19:1452–9
  • Yin L, Wang J, Klein PS, Lazar MA. (2006). Nuclear receptor Rev-erbα is a critical lithium-sensitive component of the circadian clock. Science. 311:1002–5
  • Yin L, Wu N, Curtin JC, et al. (2007). Rev-erbα, a heme sensor that coordinates metabolic and circadian pathways. Science. 318:1786–9
  • Yoshikawa T, Sellix M, Pezuk P, Menaker M. (2009). Timing of the ovarian circadian clock is regulated by gonadotropins. Endocrinology. 150:4338–47
  • Zhang Q, Dong Z, Wu X, et al. (2013). Circadian clock gene Rev-erb-α deficiency prolongs female estrous cyclicity. Sheng Li Xue Bao. 65:395–401

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