Daily changes in GT1-7 cell sensitivity to gnrh secretagogues that trigger ovulation

Neuroendocrinology

Volumn 89, Issue 4, 2009, Pages 448-457

  Zhao, Sheng ^a   Kriegsfeld, Lance J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Gonadotropin releasing hormone; Kisspeptin; Reproduction; Vasoactive intestinal polypeptide

Indexed keywords

BMAL 1 PROTEIN; GONADORELIN; KISSPEPTIN; PER2 PROTEIN; UNCLASSIFIED DRUG; VASOACTIVE INTESTINAL POLYPEPTIDE;

ANIMAL CELL; ARTICLE; CIRCADIAN RHYTHM; CONCENTRATION RESPONSE; GENE EXPRESSION REGULATION; GONADORELIN RELEASE; MOUSE; NERVE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; OVULATION INDUCTION; PRIORITY JOURNAL; PROESTRUS; SUPRACHIASMATIC NUCLEUS; THERMOREGULATION; TRANSCRIPTION REGULATION;

BIOLOGICAL CLOCKS; CELL LINE, TRANSFORMED; CIRCADIAN RHYTHM; FEMALE; GONADOTROPIN-RELEASING HORMONE; HUMANS; NEURONS; OVULATION; TUMOR SUPPRESSOR PROTEINS; VASOACTIVE INTESTINAL PEPTIDE;

EID: 67650233305     PISSN: 00283835     EISSN: None     Source Type: Journal    
DOI: 10.1159/000192370     Document Type: Article

References (88)

1. Kriegsfeld LJ, Silver R: The regulation of neuroendocrine function: timing is everything. Horm Behav 2006;49:557-574.
2. Moore RY, Eichler VB: Loss of a circadian adrenal corticosterone rhythm following su-prachiasmatic lesions in the rat. Brain Res 1972;42:201-206.
3. Stephan FK, Zucker I: Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proc Nat l Acad Sci USA 1972;69:1583-1586.
4. Reppert SM, Weaver DR: Coordination of circadian timing in mammals. Nature 2002; 418:935-941.
5. Bradbury MJ, Akana SF, Cascio CS, Levin N, Jacobson L, Dallman MF: Regulation of basal ACTH secretion by corticosterone is mediated by both type I (MR) and type II (GR) receptors in rat brain. J Steroid Biochem Mol Biol 1991;40:133-142.
6. Bradbury MJ, Cascio CS, Scribner KA, Dallman MF: Stress-induced adrenocorticotropin secretion: diurnal responses and decreases during stress in the evening are not dependent on corticosterone. Endocrinology 1991;128:680-688.
7. Buijs RM, Wortel J, Van Heerikhuize JJ, Kalsbeek A: Novel environment induced inhibition of corticosterone secretion: physiological evidence for a suprachiasmatic nucleus mediated neuronal hypothalamo-adrenal cortex pathway. Brain Res 1997;758:229-236.
8. Perreau-Lenz S, Kalsbeek A, Garidou ML, Wortel J, van der Vliet J, van Heijningen C, Simonneaux V, Pevet P, Buijs RM: Suprachiasmatic control of melatonin synthesis in rats: inhibitory and stimulatory mechanisms. Eur J Neurosci 2003;17:221-228.
9. Jasper MS, Engeland WC: Splanchnic neural activity modulates ultradian and circadian rhythms in adrenocortical secretion in awake rats. Neuroendocrinology 1994;59: 97-109.
10. Buijs RM, Wortel J, Van Heerikhuize JJ, Feenstra MG, Ter Horst GJ, Romijn HJ, Kalsbeek A: Anatomical and functional demonstration of a multisynaptic suprachiasmatic nucleus adrenal (cortex) pathway. Eur J Neurosci 1999;11:1535-1544.
11. Buijs RM, la Fleur SE, Wortel J, Van Heyningen C, Zuiddam L, Mettenleiter TC, Kalsbeek A, Nagai K, Niijima A: The suprachiasmatic nucleus balances sympathetic and parasympathetic output to peripheral organs through separate preautonomic neurons. J Comp Neurol 2003;464:36-48.
12. Shibata S: Neural regulation of the hepatic circadian rhythm. Anat Rec 2004;280:901-909.
13. Terazono H, Mutoh T, Yamaguchi S, Kobayashi M, Akiyama M, Udo R, Ohdo S, Okamura H, Shibata S: Adrenergic regulation of clock gene expression in mouse liver. Proc Natl Acad Sci USA 2003;100:6795-6800.
14. Liu D, Peddada SD, Li L, Weinberg CR: Phase analysis of circadian-related genes in two tissues. BMC Bioinformatics 2006;7:87.
15. Nakahata Y, Grimaldi B, Sahar S, Hirayama J, Sassone-Corsi P: Signaling to the circadian clock: Plasticity by chromatin remodeling. Curr Opin Cell Biol 2007;19:230-237.
16. Kohsaka A, Bass J: A sense of time: how molecular clocks organize metabolism. Trends Endocrinol Metab 2007;18:4-11.
17. Liu AC, Welsh DK, Ko CH, Tran HG, Zhang EE, Priest AA, Buhr ED, Singer O, Meeker K, Verma IM, Doyle FJ 3rd, Takahashi JS, Kay SA: Intercellular coupling confers robustness against mutations in the SCN circadian clock network. Cell 2007;129:605-616.
18. 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 2004;14:2289-2295.
19. Kriegsfeld LJ, Silver R, Gore AC, Crews D: Vasoactive intestinal polypeptide contacts on gonadotropin-releasing hormone neurones increase following puberty in female rats. J Neuroendocrinol 2002;14:685-690.
20. Olcese J, Domagalski R, Bednorz A, Weaver DR, Urbanski HF, Reuss S, Middendorff R: Expression and regulation of mper1 in immortalized GnRH neurons. Neuroreport 2003;14:613-618.
21. Shieh KR: Distribution of the rhythm-related genes rPERIOD1, rPERIOD2, and rCLOCK, in the rat brain. Neuroscience 2003;118:831-843.
22. von Gall C, Garabette ML, Kell CA, Frenzel S, Dehghani F, Schumm-Draeger PM, Weaver DR, Korf HW, Hastings MH, Stehle JH: Rhythmic gene expression in pituitary depends on heterologous sensitization by the neurohormone melatonin. Nature Neurosci 2002;5:234-238.
23. Bittman EL, Doherty L, Huang L, Paroskie A: Period gene expression in mouse endocrine tissues. Am J Physiol 2003;285:R561-R569.
24. Zylka MJ, Shearman LP, Weaver DR, Reppert SM: Three period homologs in mammals: differential light responses in the suprachiasmatic circadian clock and oscillating transcripts outside of brain. Neuron 1998;20:1103-1110.
25. Buijs RM, Chun SJ, Niijima A, Romijn HJ, Nagai K: Parasympathetic and sympathetic control of the pancreas: a role for the suprachiasmatic nucleus and other hypothalamic centers that are involved in the regulation of food intake. J Comp Neurol 2001;431:405-423.
26. Gerendai I, Toth IE, Boldogkoi Z, Medveczky I, Halasz B: CNS structures presumably involved in vagal control of ovarian function. J Auton Nerv Syst 2000;80:40-45.
27. Kreier F, Fliers E, Voshol PJ, Van Eden CG, Havekes LM, Kalsbeek A, Van Heijningen CL, Sluiter AA, Mettenleiter TC, Romijn JA, Sauerwein HP, Buijs RM: Selective parasympathetic innervation of subcutaneous and intra-abdominal fat - functional implications. J Clin Invest 2002;110:1243-1250.
28. Strack AM, Sawyer WB, Platt KB, Loewy AD: CNS cell groups regulating the sympathetic outflow to adrenal gland as revealed by transneuronal cell body labeling with pseudorabies virus. Brain Res 1989;491:274-296.
29. Bronson FH (ed): Mammalian Reproductive Biology. Chicago, University of Chicago Press, 1990.
30. Herbison AE: Physiology of the GnRH neuronal networks;in Knobil E, Neill JD (eds): Physiology of Reproduction, ed 3. San Diego, Elsevier, 2005, pp 1415-1482.
31. Levine JE: Gonadotropin-releasing hormone (GnRH); in Herny H, Normona A (eds): Encyclopedia of Hormones. San Diego, Academic Press, 2003, pp 157-165.
32. Van der Beek EM, Horvath TL, Wiegant VM, Van den Hurk R, Buijs RM: Evidence for a direct neuronal pathway from the suprachiasmatic nucleus to the gonadotropin-releasing hormone system: combined tracing and light and electron microscopic immunocy-tochemical studies. J Comp Neurol 1997;384: 569-579.
33. van der Beek EM, van Oudheusden HJ, Buijs RM, van der Donk HA, van den Hurk R, Wiegant VM: Preferential induction of c-fos immunoreactivity in vasoactive intestinal polypeptide-innervated gonadotropin-re-leasing hormone neurons during a steroidinduced luteinizing hormone surge in the female rat. Endocrinology 1994;134:2636-2644.
34. van der Beek EM, Swarts HJ, Wiegant VM: Central administration of antiserum to vasoactive intestinal peptide delays and reduces luteinizing hormone and prolactin surges in ovariectomized, estrogen-treated rats. Neuroendocrinology 1999;69:227-237.
35. Legan SJ, Karsch FJ: A daily signal for the LH surge in the rat. Endocrinology 1975;96:57-62.
36. Gray GD, Soderstein P, Tallentire D, Davidson JM: Effects of lesions in various structures of the suprachiasmatic-preoptic region on LH regulation and sexual behavior in female rats. Neuroendocrinology 1978;25: 174-191.
37. Nunez AA, Stephan FK: The effects of hypothalamic knife cuts on drinking rhythms and the estrus cycle of the rat. Behav Biol 1977;20:224-234.
38. van der Beek EM, Wiegant VM, van der Donk HA, van den Hurk R, Buijs RM: Lesions of the suprachiasmatic nucleus indicate the presence of a direct vasoactive intestinal polypeptide-containing projection to gonadotrophin- releasing hormone neurons in the female rat. J Neuroendocrinol 1993;5: 137-144.
39. Smith MJ, Jiennes L, Wise PM: Localization of the VIP2 receptor protein on GnRH neurons in the female rat. Endocrinology 2000; 141:4317-4320.
40. Olcese J, McArdle CA, Middendorff R, Greenland K: Pituitary adenylate cyclase-activating peptide and vasoactive intestinal peptide receptor expression in immortalized LHRH neurons. J Neuroendocrinol 1997;9: 937-943.
41. Ohtsuka S, Miyake A, Nishizaki T, Tasaka K, Tanizawa O: Vasoactive intestinal peptide stimulates gonadotropin-releasing hormone release from rat hypothalamus in vitro. Acta Endocrinol 1988;117:399-402.
42. Harney JP, Scarbrough K, Rosewell KL, Wise PM: In vivo antisense antagonism of vasoactive intestinal peptide in the suprachiasmatic nuclei causes aging-like changes in the estradiol-induced luteinizing hormone and prolactin surges. Endocrinology 1996;137: 3696-3701.
43. Kimura F, Mitsugi N, Arita J, Akema T, Yoshida K: Effects of preoptic injections of gastrin, cholecystokinin, secretin, vasoactive intestinal peptide and phi on the secretion of luteinizing hormone and prolactin in ovariectomized estrogen-primed rats. Brain Res 1987;410:315-322.
44. Kinoshita M, Tsukamura H, Adachi S, Matsui H, Uenoyama Y, Iwata K, Yamada S, Inoue K, Ohtaki T, Matsumoto H, Maeda K: Involvement of central metastin in the regulation of preovulatory luteinizing hormone surge and estrous cyclicity in female rats. Endocrinology 2005;146:4431-4436.
45. Wintermantel TM, Campbell RE, Porteous R, Bock D, Grone HJ, Todman MG, Korach KS, Greiner E, Perez CA, Schutz G, Herbison AE: Definition of estrogen receptor pathway critical for estrogen positive feedback to gonadotropin- releasing hormone neurons and fertility. Neuron 2006;52:271-280.
46. Le WW, Attardi B, Berghorn KA, Blaustein J, Hoffman GE: Progesterone blockade of a luteinizing hormone surge blocks luteinizing hormone-releasing hormone fos activation and activation of its preoptic area affer-ents. Brain Res 1997;778:272-280.
47. Kriegsfeld LJ, Leak RK, Yackulic CB, LeSauter J, Silver R: Organization of suprachiasmatic nucleus projections in Syrian hamsters (Mesocricetus auratus): an anterograde and retrograde analysis. J Comp Neurol 2004; 468:361-379.
48. Levine JE: New concepts of the neuroendocrine regulation of gonadotropin surges in rats. Biology Reprod 1997;56:293-302.
49. Kotani M, Detheux M, Vandenbogaerde A, Communi D, Vanderwinden JM, Le Poul E, Brezillon S, Tyldesley R, Suarez-Huerta N, Vandeput F, Blanpain C, Schiffmann SN, Vassart G, Parmentier M: The metastasis suppressor gene KiSS-1 encodes kisspeptins, the natural ligands of the orphan G proteincoupled receptor GPR54. J Biol Chem 2001; 276:34631-34636.
50. Smith JT, Popa SM, Clifton DK, Hoffman GE, Steiner RA: Kiss1 neurons in the forebrain as central processors for generating the preovulatory luteinizing hormone surge. J Neurosci 2006;26:6687-6694.
51. Shahab M, Mastronardi C, Seminara SB, Crowley WF, Ojeda SR, Plant TM: Increased hypothalamic GPR54 signaling: a potential mechanism for initiation of puberty in primates. Proc Natl Acad Sci USA 2005;102: 2129-2134.
52. Ohtaki T, Shintani Y, Honda S, Matsumoto H, Hori A, Kanehashi K, Terao Y, Kumano S, Takatsu Y, Masuda Y, Ishibashi Y, Watanabe T, Asada M, Yamada T, Suenaga M, Kitada C, Usuki S, Kurokawa T, Onda H, Nishimura O, Fujino M: Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor. Nature 2001;411:613-617.
53. Han SK, Gottsch ML, Lee KJ, Popa SM, Smith JT, Jakawich SK, Clifton DK, Steiner RA, Herbison AE: Activation of gonadotropin-releasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty. J Neurosci 2005;25:11349-11356.
54. 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.
55. 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.
56. Gottsch ML, Cunningham MJ, Smith JT, Popa SM, Acohido BV, Crowley WF, Seminara S, Clifton DK, Steiner RA: A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology 2004; 145:4073-4077.
57. Balsalobre A, Damiola F, Schibler U: A serum shock induces circadian gene expression in mammalian tissue culture cells. Cell 1998;93:929-937.
58. 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.
59. Zhao S, Fernald RD: Comprehensive algorithm for quantitative real-time polymerase chain reaction. J Comput Biol 2005;12:1047-1064.
60. Reppert SM, Weaver DR: Molecular analysis of mammalian circadian rhythms. Annu Rev Physiol 2001;63:647-676.
61. Ripperger JA, Schibler U: Circadian regulation of gene expression in animals. Curr Opin Cell Biol 2001;13:357-362.
62. Schibler U, Ripperger J, Brown SA: Peripheral circadian oscillators in mammals: time and food. J Biol Rhy thms 2003;18:250-260.
63. 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.
64. Quaynor S, Hu L, Leung PK, Feng H, Mores N, Krsmanovic LZ, Catt KJ: Expression of a functional G protein-coupled receptor 54-kisspeptin autoregulatory system in hypothalamic gonadotropin-releasing hormone neurons. Mol Endocrinol 2007;21:3062-3070.
65. Pitts GR, Nunemaker CS, Moenter SM: Cycles of transcription and translation do not comprise the gonadotropin-releasing hormone pulse generator in GT1 cells. Endocrinology 2001;142:1858-1864.
66. Buijs RM, Scheer FA, Kreier F, Yi C, Bos N, Goncharuk VD, Kalsbeek A: Organization of circadian functions: interaction with the body. Prog Brain Res 2006;153:341-360.
67. Davidson AJ, London B, Block GD, Menaker M: Cardiovascular tissues contain independent circadian clocks. Clin Exp Hypertens 2005;27:307-311.
68. Levi F, Schibler U: Circadian rhythms: mechanisms and therapeutic implications. Annu Rev Pharmacol Toxicol 2007;47:593-628.
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 2000;288:682-685.
70. Damiola F, Le Minh N, Preitner N, Kornmann B, Fleury-Olela F, Schibler U: Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev 2000;14:2950-2961.
71. Hirao J, Arakawa S, Watanabe K, Ito K, Furukawa T: Effects of restricted feeding on daily fluctuations of hepatic functions including p450 monooxygenase activities in rats. J Biol Chem 2006;281:3165-3171.
72. Gillespie JM, Chan BP, Roy D, Cai F, Belsham DD: Expression of circadian rhythm genes in gonadotropin-releasing hormone-secreting GT1-7 neurons. Endocrinology 2003;144: 5285-5292.
73. Roy D, Angelini NL, Fujieda H, Brown GM, Belsham DD: Cyclical regulation of GnRH gene expression in GT1-7 GnRH-secreting neurons by melatonin. Endocrinology 2001; 142:4711-4720.
74. 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.
75. Palm IF, van der Beek EM, Wiegant VM, Buijs RM, Kalsbeek A: The stimulatory effect of vasopressin on the luteinizing hormone surge in ovariectomized, estradioltreated rats is time-dependent. Brain Res 2001;901:109-116.
76. Kallo I, Vida B, Kalamatianos T, Hrabovszky E, Caraty A, Liposits Z, Coen CW: Innervation of kisspeptin neurons by vasopressin-and VIP-immunoreactive fibers in the anteroventral periventricular and preoptic periventricular nuclei of the mouse. Poster Neuroscience Meeting, San Diego, 2007.
77. Leak RK, Moore RY: Topographic organization of suprachiasmatic nucleus projection neurons. J Comp Neurol 2001;433:312-334.
78. Hahn JD, Coen CW: Comparative study of the sources of neuronal projections to the site of gonadotrophin-releasing hormone perikarya and to the anteroventral periventricular nucleus in female rats. J Comp Neurol 2006;494:190-214.
79. Greives TJ, Mason AO, Scotti MA, Levine J, Ketterson ED, Kriegsfeld LJ, Demas GE: Environmental control of kisspeptin: implications for seasonal reproduction. Endocrinology 2007;148:1158-1166.
80. Franceschini I, Lomet D, Cateau M, Delsol G, Tillet Y, Carat y A: Kisspeptin i mmunore-active cells of the ovine preoptic area and arcuate nucleus co-express estrogen receptor alpha. Neurosci Lett 2006;401:225-230.
81. 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.
82. Smith JT: Kisspeptin signalling in the brain: steroid regulation in the rodent and ewe. Brain Res Rev 2008;57:288-298.
83. 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 est rogen positive feedback action on luteinizing hormone release in female rats. J Reprod Dev 2007;53:367-378.
84. Caraty A, Smith JT, Lomet D, Ben Said S, Morrissey A, Cognie J, Doughton B, Baril G, Briant C, Clarke IJ: Kisspeptin synchronizes preovulatory surges in cyclical ewes and causes ovulation in seasonally acyclic ewes. Endocrinology 2007;148:5258-5267.
85. Mason AO, Greives TJ, Scotti MA, Levine J, Frommeyer S, Ketterson ED, Demas GE, Kriegsfeld LJ: Suppression of kisspeptin expression and gonadotropic axis sensitivity following exposure to inhibitory day lengths in female Siberian hamsters. Horm Behav 2007;52:492-498.
86. Dhillo WS, Chaudhri OB, Thompson EL, Murphy KG, Patterson M, Ramachandran R, Nijher GK, Amber V, Kokkinos A, Donaldson M, Ghatei MA, Bloom SR: Kisspeptin-54 stimulates gonadotropin release most potently during the preovulatory phase of the menstrual cycle in women. J Clin Endocrinol Metab 2007;92:3958-3966.
87. Kriegsfeld LJ, Korets R, Silver R: Expression of the circadian clock gene Period 1 in neuroendocrine cells: an investigation using mice with a Per1::GFP transgene. Eur J Neurosci 2003;17:212-220.
88. Morse D, Cermakian N, Brancorsini S, Parvinen M, Sassone-Corsi P: No circadian rhythms in testis: Period1 expression is clock independent and developmentally regulated in the mouse. Mol Endocrinol 2003;17:141-151.