Modulation of gonadotrophin-releasing hormone secretion by an endogenous circadian clock

Journal of Neuroendocrinology

Volumn 21, Issue 4, 2009, Pages 339-345

  Chappell, Patrick E ^a   Goodall, C P ^a   Tonsfeldt, K J ^a   White, R S ^a   Bredeweg, E ^a   Latham, K L ^a,b  

^a OREGON STATE UNIVERSITY   (United States)

^b WESTERN OREGON UNIVERSITY   (United States)

Author keywords

Circadian; Clock; GnRH; Oestradiol; Secretion; Surge

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; G PROTEIN COUPLED RECEPTOR; GONADORELIN; NEUROPEPTIDE; TRANSCRIPTION FACTOR CLOCK;

CELL MEMBRANE TRANSPORT; CIRCADIAN RHYTHM; CONFERENCE PAPER; ESTRUS CYCLE; GENE EXPRESSION REGULATION; GENE MUTATION; GONADORELIN RELEASE; HORMONE ACTION; HUMAN; HYPOTHALAMUS HYPOPHYSIS GONAD SYSTEM; LEYDIG CELL; MUTAGENESIS; NERVE CELL; NERVE CELL STIMULATION; NEUROMODULATION; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; SENSORY NERVE CONDUCTION; SIGNAL TRANSDUCTION; SPERMATOZOON MATURATION; STEROIDOGENESIS; TRANSCRIPTION REGULATION;

ANIMALS; BIOLOGICAL CLOCKS; BRAIN; CIRCADIAN RHYTHM; ESTRADIOL; FEEDBACK, BIOCHEMICAL; FEMALE; GONADOTROPIN-RELEASING HORMONE; MODELS, BIOLOGICAL; NEURONS; REPRODUCTION;

EID: 63549138810     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2009.01845.x     Document Type: Conference Paper

References (71)

1. Sarkar DK, Chiappa SA, Fink G, Sherwood NM. Gonadotropin-releasing hormone surge in pro-oestrous rats. Nature 1976; 264: 461-463.
2. Moenter SM, Brand RC, Karsch FJ. Dynamics of gonadotropin-releasing hormone (GnRH) secretion during the GnRH surge: Insights into the mechanism of GnRH surge induction. Endocrinology 1992; 130: 2978-2984.
3. Everett JW, Sawyer CH. A 24-hour periodicity in the 'LH-release apparatus' of female rats, disclosed by barbiturate sedation. Endocrinology 1950; 47: 198-218.
4. Legan SJ, Coon GA, Karsch FJ. Role of estrogen as initiator of daily LH surges in the ovariectomized rat. Endocrinology 1975; 96: 50-56.
5. Legan SJ, Karsch FJ. A daily signal for the LH surge in the rat. Endocrinology 1975; 96: 57-62.
6. Christian CA, Mobley JL, Moenter SM. Diurnal and estradiol-dependent changes in gonadotropin-releasing hormone neuron firing activity. Proc Natl Acad Sci USA 2005; 102: 15682-15687.
7. Bronson FH, Vom Saal FS. Control of the preovulatory release of luteinizing hormone by steroids in the mouse. Endocrinology 1979; 104: 1247-1255.
8. Krey LC, Parsons B. Characterization of estrogen stimuli sufficient to initiate cyclic luteinizing hormone release in acutely ovariectomized rats. Neuroendocrinology 1982; 34: 315-322.
9. Hrabovszky E, Steinhauser A, Barabas K, Shughrue PJ, Petersen SL, Merchenthaler I, Liposits Z. Estrogen receptor-beta immunoreactivity in luteinizing hormone-releasing hormone neurons of the rat brain. Endocrinology 2001; 142: 3261-3264.
10. Abraham IM, Han SK, Todman MG, Korach KS, Herbison AE. Estrogen receptor beta mediates rapid estrogen actions on gonadotropin-releasing hormone neurons in vivo. J Neurosci 2003; 23: 5771-5777.
11. Kallo I, Butler JA, Barkovics-Kallo M, Goubillon ML, Coen CW. Oestrogen receptor beta-immunoreactivity in gonadotropin releasing hormone-expressing neurones: Regulation by oestrogen. J Neuroendocrinol 2001; 13: 741-748.
12. Glidewell-Kenney C, Hurley LA, Pfaff L, Weiss J, Levine JE, Jameson JL. Nonclassical estrogen receptor alpha signaling mediates negative feedback in the female mouse reproductive axis. Proc Natl Acad Sci USA 2007; 104: 8173-8177.
13. Hu L, Gustofson RL, Feng H, Leung PK, Mores N, Krsmanovic LZ, Catt KJ. Converse regulatory functions of estrogen receptor-alpha and -beta subtypes expressed in hypothalamic gonadotropin-releasing hormone neurons. Mol Endocrinol 2008; 22: 2250-2259.
14. Mosko SS, Moore RY. Neonatal ablation of the suprachiasmatic nucleus. Effects on the development of the pituitary-gonadal axis in the female rat. Neuroendocrinology 1979; 29: 350-361.
15. Scott CJ, Jansen HT, Kao CC, Kuehl DE, Jackson GL. Disruption of reproductive rhythms and patterns of melatonin and prolactin secretion following bilateral lesions of the suprachiasmatic nuclei in the ewe. J Neuroendocrinol 1995; 7: 429-443.
16. Wiegand SJ, Terasawa E, Bridson WE, Goy RW. Effects of discrete lesions of preoptic and suprachiasmatic structures in the female rat. Alterations in the feedback regulation of gonadotropin secretion. Neuroendocrinology 1980; 31: 147-157.
17. Wiegand SJ, Terasawa E, Bridson WE. Persistent estrus and blockade of progesterone-induced LH release follows lesions which do not damage the suprachiasmatic nucleus. Endocrinology 1978; 102: 1645-1648.
18. Adachi S, Yamada S, Takatsu Y, Matsui H, Kinoshita M, Takase K, Sugiura H, Ohtaki T, Matsumoto H, Uenoyama Y, Tsukamura H, Inoue K, Maeda K. Involvement of anteroventral periventricular metastin/kisspeptin neurons in estrogen positive feedback action on luteinizing hormone release in female rats. J Reprod Dev 2007; 53: 367-378.
19. Herbison AE. Estrogen positive feedback to gonadotropin-releasing hormone (GnRH) neurons in the rodent: The case for the rostral periventricular area of the third ventricle (RP3V). Brain Res Rev 2008; 57: 277-287.
20. Jacobi JS, Martin C, Nava G, Jeziorski MC, Clapp C, Martinez de la Escalera G. 17-Beta-estradiol directly regulates the expression of adrenergic receptors and kisspeptin/GPR54 system in GT1-7 GnRH neurons. Neuroendocrinology 2007; 86: 260-269.
21. Kanda S, Akazome Y, Matsunaga T, Yamamoto N, Yamada S, Tsukamura H, Maeda K, Oka Y. Identification of KiSS-1 product kisspeptin and steroid-sensitive sexually dimorphic kisspeptin neurons in medaka (Oryzias latipes). Endocrinology 2008; 149: 2467-2476.
22. Roa J, Vigo E, Castellano JM, Gaytan F, Navarro VM, Aguilar E, Dijcks FA, Ederveen AG, Pinilla L, van Noort PI, Tena-Sempere M. Opposite roles of estrogen receptor (ER)-alpha and ERbeta in the modulation of luteinizing hormone responses to kisspeptin in the female rat: implications for the generation of the preovulatory surge. Endocrinology 2008; 149: 1627-1637.
23. Smith JT. Sex steroid control of hypothalamic Kiss1 expression in sheep and rodents: Comparative aspects. Peptides. 2008; 30: 94-102.
24. Smith JT. Kisspeptin signalling in the brain: Steroid regulation in the rodent and ewe. Brain Res Rev 2008; 57: 288-298.
25. Smith JT, Dungan HM, Stoll EA, Gottsch ML, Braun RE, Eacker SM, Clifton DK, Steiner RA. Differential regulation of KiSS-1 mRNA expression by sex steroids in the brain of the male mouse. Endocrinology 2005; 146: 2976-2984.
26. Gianetti E, Seminara S. Kisspeptin and KISS1R: A critical pathway in the reproductive system. Reproduction 2008; 136: 295-301.
27. Gottsch ML, Clifton DK, Steiner RA. Kisspepeptin-GPR54 signaling in the neuroendocrine reproductive axis. Mol Cell Endocrinol 2006; 254-255: 91-96.
28. Irwig MS, Fraley GS, Smith JT, Acohido BV, Popa SM, Cunningham MJ, Gottsch ML, Clifton DK, Steiner RA. Kisspeptin activation of gonadotropin releasing hormone neurons and regulation of KiSS-1 mRNA in the male rat. Neuroendocrinology 2004; 80: 264-272.
29. Liu X, Lee K, Herbison AE. Kisspeptin excites gonadotropin-releasing hormone neurons through a phospholipase C/calcium-dependent pathway regulating multiple ion channels. Endocrinology 2008; 149: 4605-4614.
30. Messager S, Chatzidaki EE, Ma D, Hendrick AG, Zahn D, Dixon J, Thresher RR, Malinge I, Lomet D, Carlton MB, Colledge WH, Caraty A, Aparicio SA. Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. Proc Natl Acad Sci USA 2005; 102: 1761-1766.
31. Seminara SB. Metastin and its G protein-coupled receptor, GPR54: critical pathway modulating GnRH secretion. Front Neuroendocrinol 2005; 26: 131-138.
32. Zhang C, Roepke TA, Kelly MJ, Ronnekleiv OK. Kisspeptin depolarizes gonadotropin-releasing hormone neurons through activation of TRPC-like cationic channels. J Neurosci 2008; 28: 4423-4434.
33. Dungan HM, Clifton DK, Steiner RA. Minireview: Kisspeptin neurons as central processors in the regulation of gonadotropin-releasing hormone secretion. Endocrinology 2006; 147: 1154-1158.
34. Popa SM, Clifton DK, Steiner RA. The role of kisspeptins and GPR54 in the neuroendocrine regulation of reproduction. Annu Rev Physiol 2008; 70: 213-238.
35. Smith JT, Clifton DK, Steiner RA. Regulation of the neuroendocrine reproductive axis by kisspeptin-GPR54 signaling. Reproduction 2006; 131: 623-630.
36. Estrada KM, Clay CM, Pompolo S, Smith JT, Clarke IJ. Elevated KiSS-1 expression in the arcuate nucleus prior to the cyclic preovulatory gonadotrophin-releasing hormone/lutenising hormone surge in the ewe suggests a stimulatory role for kisspeptin in oestrogen-positive feedback. J Neuroendocrinol 2006; 18: 806-809.
37. Franceschini I, Lomet D, Cateau M, Delsol G, Tillet Y, Caraty A. Kisspeptin immunoreactive cells of the ovine preoptic area and arcuate nucleus co-express estrogen receptor alpha. Neurosci Lett 2006; 401: 225-230.
38. Ramaswamy S, Guerriero KA, Gibbs RB, Plant TM. Structural interactions between kisspeptin and GnRH neurons in the mediobasal hypothalamus of the male rhesus monkey (Macaca mulatta) as revealed by double immunofluorescence and confocal microscopy. Endocrinology 2008; 149: 4387-4395.
39. Gu GB, Simerly RB. Projections of the sexually dimorphic anteroventral periventricular nucleus in the female rat. J Comp Neurol 1997; 384: 142-164.
40. Kauffman AS, Gottsch ML, Roa J, Byquist AC, Crown A, Clifton DK, Hoffman GE, Steiner RA, Tena-Sempere M. Sexual differentiation of Kiss1 gene expression in the brain of the rat. Endocrinology 2007; 148: 1774-1783.
41. Kauffman AS, Park JH, McPhie-Lalmansingh AA, Gottsch ML, Bodo C, Hohmann JG, Pavlova MN, Rohde AD, Clifton DK, Steiner RA, Rissman EF. The kisspeptin receptor GPR54 is required for sexual differentiation of the brain and behavior. J Neurosci 2007; 27: 8826-8835.
42. Christian CA, Moenter SM. Vasoactive intestinal polypeptide can excite gonadotropin-releasing hormone neurons in a manner dependent on estradiol and gated by time of day. Endocrinology 2008; 149: 3130-3136.
43. Miller BH, Olson SL, Levine JE, Turek FW, Horton TH, Takahashi JS. Vasopressin regulation of the proestrous luteinizing hormone surge in wild-type and Clock mutant mice. Biol Reprod 2006; 75: 778-784.
44. Palm IF, van der Beek EM, Wiegant VM, Buijs RM, Kalsbeek A. The stimulatory effect of vasopressin on the luteinizing hormone surge in ovariectomized, estradiol-treated rats is time-dependent. Brain Res 2001; 901: 109-116.
45. Funabashi T, Shinohara K, Mitsushima D, Kimura F. Gonadotropin-releasing hormone exhibits circadian rhythm in phase with arginine-vasopressin in co-cultures of the female rat preoptic area and suprachiasmatic nucleus. J Neuroendocrinol 2000; 12: 521-528.
46. Reppert SM. Cellular and molecular basis of circadian timing in mammals. Semin Perinatol 2000; 24: 243-246.
47. Reppert SM, Weaver DR. Coordination of circadian timing in mammals. Nature 2002; 418: 935-941.
48. Sato TK, Panda S, Miraglia LJ, Reyes TM, Rudic RD, McNamara P, Naik KA, FitzGerald GA, Kay SA, Hogenesch JB. A functional genomics strategy reveals Rora as a component of the mammalian circadian clock. Neuron 2004; 43: 527-537.
49. Triqueneaux G, Thenot S, Kakizawa T, Antoch MP, Safi R, Takahashi JS, Delaunay F, Laudet V. The orphan receptor Rev-erbalpha gene is a target of the circadian clock pacemaker. J Mol Endocrinol 2004; 33: 585-608.
50. Hogenesch JB, Panda S, Kay S, Takahashi JS. Circadian transcriptional output in the SCN and liver of the mouse. Novartis Found Symp 2003; 253: 171-180.
51. Panda S, Antoch MP, Miller BH, Su AI, Schook AB, Straume M, Schultz PG, Kay SA, Takahashi JS, Hogenesch JB. Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 2002; 109: 307-320.
52. Chappell PE, White RS, Mellon PL. Circadian gene expression regulates pulsatile gonadotropin-releasing hormone (GnRH) secretory patterns in the hypothalamic GnRH-secreting GT1-7 cell line. J Neurosci 2003; 23: 11202-11213.
53. Kennaway DJ, Boden MJ, Voultsios A. Reproductive performance in female Clock Delta19 mutant mice. Reprod Fertil Dev 2004; 16: 801-810.
54. Miller BH, Olson SL, Turek FW, Levine JE, Horton TH, Takahashi JS. Circadian clock mutation disrupts estrous cyclicity and maintenance of pregnancy. Curr Biol 2004; 14: 1367-1373.
55. Boden MJ, Kennaway DJ. Circadian rhythms and reproduction. Reproduction 2006; 132: 379-392.
56. Bunger MK, Wilsbacher LD, Moran SM, Clendenin C, Radcliffe LA, Hogenesch JB, Simon MC, Takahashi JS, Bradfield CA. Mop3 is an essential component of the master circadian pacemaker in mammals. Cell 2000; 103: 1009-1017.
57. King DP, Vitaterna MH, Chang AM, Dove WF, Pinto LH, Turek FW, Takahashi JS. The mouse Clock mutation behaves as an antimorph and maps within the W19H deletion, distal of kit. Genetics 1997; 146: 1049-1060.
58. Vitaterna MH, King DP, Chang AM, Kornhauser JM, Lowrey PL, McDonald JD, Dove WF, Pinto LH, Turek FW, Takahashi JS. Mutagenesis and mapping of a mouse gene, Clock, essential for circadian behavior. Science 1994; 264: 719-725.
59. Vitaterna MH, Ko CH, Chang AM, Buhr ED, Fruechte EM, Schook A, Antoch MP, Turek FW, Takahashi JS. The mouse Clock mutation reduces circadian pacemaker amplitude and enhances efficacy of resetting stimuli and phase-response curve amplitude. Proc Natl Acad Sci USA 2006; 103: 9327-9332.
60. Gekakis N, Staknis D, Nguyen HB, Davis FC, Wilsbacher LD, King DP, Takahashi JS, Weitz CJ. Role of the clock protein in the mammalian circadian mechanism. Science 1998; 280: 1564-1569.
61. Allen GC, Farnell Y, Bell-Pedersen D, Cassone VM, Earnest DJ. Effects of altered Clock gene expression on the pacemaker properties of SCN2.2 cells and oscillatory properties of NIH/3T3 cells. Neuroscience 2004; 127: 989-999.
62. Navarro CE, Abdul Saeed S, Murdock C, Martinez-Fuentes AJ, Arora KK, Krsmanovic LZ, Catt KJ. Regulation of cyclic adenosine 3′,5′-monophosphate signaling and pulsatile neurosecretion by Gi-coupled plasma membrane estrogen receptors in immortalized gonadotropin-releasing hormone neurons. Mol Endocrinol 2003; 17: 1792-1804.
63. Chappell PE, Levine JE. Stimulation of gonadotropin-releasing hormone surges by estrogen. I. Role of hypothalamic progesterone receptors. Endocrinology 2000; 141: 1477-1485.
64. Herzog ED, Geusz ME, Khalsa SB, Straume M, Block GD. Circadian rhythms in mouse suprachiasmatic nucleus explants on multimicroelectrode plates. Brain Res 1997; 757: 285-290.
65. Weaver DR. The suprachiasmatic nucleus: A 25-year retrospective. J Biol Rhythms 1998; 13: 100-112.
66. Meredith AL, Wiler SW, Miller BH, Takahashi JS, Fodor AA, Ruby NF, Aldrich RW. BK calcium-activated potassium channels regulate circadian behavioral rhythms and pacemaker output. Nat Neurosci 2006; 9: 1041-1049.
67. Pace AJ, Lee E, Athirakul K, Coffman TM, O'Brien DA, Koller BH. Failure of spermatogenesis in mouse lines deficient in the Na(+)-K(+)-2Cl(-) cotransporter. J Clin Invest 2000; 105: 441-450.
68. Latham KL, White RS, Phillips W, Goodall CP, Fitzgerald K, Mellon PL, Chappell PE. In Vitro Steroid Treatment Modulates Temporal Protein Profiles of Large-Conductance Ca2+-Activated Potassium (BK) Channels in GT1-7 Cells, Correlated with Changes in GnRH Secretion. San Diego, CA: Society for Neuroscience, 2007.
69. Yamagishi K, Enomoto T, Ohmiya Y. Perfusion-culture-based secreted bioluminescence reporter assay in living cells. Anal Biochem 2006; 354: 15-21.
70. 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 2008; 23: 26-36.
71. Bebas P, Goodall CP, Majewska M, Neumann A, Giebultowicz JM, Chappell PE. Circadian clock and output genes are rhythmically expressed in extratesticular ducts and accessory organs of mice. FASEB J 2009; 23: 523-533.