Identification of melatonin-regulated genes in the ovine pituitary pars tuberalis, a target site for seasonal hormone control

Endocrinology

Volumn 149, Issue 11, 2008, Pages 5527-5539

  Dupré, Sandrine M ^a   Burt, Dave W ^b   Talbot, Richard ^b   Downing, Alison ^b   Mouzaki, Daphne ^b   Waddington, David ^b   Malpaux, Benoit ^c   Davis, Julian R E ^a   Lincoln, Gerald A ^d   Loudon, Andrew S I ^a,e  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UMR85 PHYSIOLOGIE DE LA REPRODUCTION ET DES COMPORTEMENTS   (France)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

^e Faculty of Life Sciences   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; MELATONIN; MELATONIN RECEPTOR; NEUROGENIC DIFFERENTIATION FACTOR; PER1 PROTEIN; POTASSIUM CHANNEL KCNQ; PROLACTIN; TRANSCRIPTION FACTOR CLOCK; TRANSCRIPTOME; VISFATIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CRY1 GENE; DNA MICROARRAY; FEMALE; GENE; GENE CLUSTER; GENE EXPRESSION; GENE FUNCTION; HORMONAL REGULATION; HYPOPHYSIS PARS TUBERALIS; IN SITU HYBRIDIZATION; LIGHT DARK CYCLE; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHOTOPERIODICITY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROLACTIN RELEASE; SHEEP;

ANIMALS; CIRCADIAN RHYTHM; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; MALE; MELATONIN; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOTOPERIOD; PITUITARY GLAND; PITUITARY HORMONES; SEASONS; SHEEP;

EID: 50849121031     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2008-0834     Document Type: Article

References (74)

1. Bartness TJ, Powers JB, Hastings MH, Bittman EL, Goldman BD 1993 The timed infusion paradigm for melatonin delivery: what has it taught us about the melatonin signal, its reception, and the photoperiodic control of seasonal responses? J Pineal Res 15:161-190
2. Curlewis JD 1992 Seasonal prolactin secretion and its role in seasonal reproduction: a review. Reprod Fertil Dev 4:1-23
3. Morgan PJ, Williams LM 1996a The pars tuberalis of the pituitary: a gateway for neuroendocrine output. Rev Reprod 1:153-161
4. Graham ES, Webster CA, Hazlerigg DG, Morgan PJ 2002 Evidence for the biosynthesis of a prolactin-releasing factor from the ovine pars tuberalis, which is distinct from thyrotropin-releasing hormone. J Neuroendocrinol 14:945-954
5. Morgan PJ, Webster CA, Mercer JG, Ross AW, Hazlerigg DG, MacLean A, Barrett P 1996 The ovine pars tuberalis secretes a factor(s) that regulates gene expression in both lactotropic and nonlactotropic pituitary cells. Endocrinology 137:4018-4026
6. Stirland JA, Johnston JD, Cagampang FR, Morgan PJ, Castro MG, White MR, Davis JR, Loudon AS 2001 Photoperiodic regulation of prolactin gene expression in the Syrian hamster by a pars tuberalis-derived factor. J Neuroendocrinol 13:147-157
7. Hazlerigg DG, Hastings MH, Morgan PJ 1996 Production of a prolactin releasing factor by the ovine pars tuberalis. J Neuroendocrinol 8:489-492
8. Lincoln GA, Clarke IJ 1994 Photoperiodically-induced cycles in the secretion of prolactin in hypothalamo-pituitary disconnected rams: evidence for translation of the melatonin signal in the pituitary gland. J Neuroendocrinol 6:251-260
9. Lincoln GA, Clarke IJ, Hut RA, Hazlerigg DG 2006 Characterizing a mammalian circannual pacemaker. Science 314:1941-1944
10. Lincoln GA, Johnston JD, Andersson H, Wagner G, Hazlerigg DG 2005 Photorefractoriness in mammals: dissociating a seasonal timer from the circadian-based photoperiod response. Endocrinology 146:3782-3790
11. Chemineau P, Malpaux B, Pelletier J, Leboeuf B, Delgadillo JA, Deletang F, Pobel T, Brice G 1996 Emploi des implants de mélatonine et des traitements photopériodiques pour maîtriser la reproduction saisonnière chez les ovins et les caprins. INRA Prod Anim 9:46-60
12. Malpaux B, Daveau A, Maurice F, Gayrard V, Thiery JC 1993 Short-day effects of melatonin on luteinizing hormone secretion in the ewe: evidence for central sites of action in the mediobasal hypothalamus. Biol Reprod 48:752-760
13. Carr AJ, Johnston JD, Semikhodskii AG, Nolan T, Cagampang FR, Stirland JA, Loudon AS 2003 Photoperiod differentially regulates circadian oscillators in central and peripheral tissues of the Syrian hamster. Curr Biol 13:1543-1548
14. Grossmann S, Bauer S, Robinson PN, Vingron M 2007 Improved detection of overrepresentation of Gene-Ontology annotations with parent child analysis. Bioinformatics 23:3024-3031
15. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G 2000 Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25:25-29
16. Camon E, Magrane M, Barrell D, Lee V, Dimmer E, Maslen J, Binns D, Harte N, Lopez R, Apweiler R 2004 The Gene Ontology Annotation (GOA) Database: sharing knowledge in Uniprot with Gene Ontology. Nucleic Acids Res 32:D262-D266
17. Westfall PH, Young SS 1993 Resampling-based multiple testing: examples and methods for P-value adjustment. New York: John Wiley, Sons
18. Draghici S, Tarca AL, Yu L, Ethier S, Romero R 2008 KUTE-BASE: storing, downloading and exporting MIAME-compliant microarray experiments in minutes rather than hours. Bioinformatics 24:738-740
19. Kel AE, Gossling E, Reuter I, Cheremushkin E, Kel-Margoulis OV, Wingender E 2003 MATCH: A tool for searching transcription factor binding sites in DNA sequences. Nucleic Acids Res 31:3576-3579
20. Storey JD, Tibshirani R 2003 Statistical significance for genomewide studies. Proc Natl Acad Sci USA 100:9440-9445
21. Kijas JW, Menzies M, Ingham A 2006 Sequence diversity and rates of molecular evolution between sheep and cattle genes. Anim Genet 37:171-174
22. Su AI, Cooke MP, Ching KA, Hakak Y, Walker JR, Wiltshire T, Orth AP, Vega RG, Sapinoso LM, Moqrich A, Patapoutian A, Hampton GM, Schultz PG, Hogenesch JB 2002 Large-scale analysis of the human and mouse transcriptomes. Proc Natl Acad Sci USA 99:4465-4470
23. Lincoln G, Messager S, Andersson H, Hazlerigg D 2002 Temporal expression of seven clock genes in the suprachiasmatic nucleus and the pars tuberalis of the sheep: evidence for an internal coincidence timer. Proc Natl Acad Sci USA 99:13890-13895
24. Johnston JD, Ebling FJ, Hazlerigg DG 2005 Photoperiod regulates multiple gene expression in the suprachiasmatic nuclei and pars tuberalis of the Siberian hamster (Phodopus sungorus). Eur J Neurosci 21:2967-2974
25. Naya FJ, Stellrecht CM, Tsai MJ 1995 Tissue-specific regulation of the insulin gene by a novel basic helix-loop-helix transcription factor. Genes Dev 9:1009-1019
26. Lee JK, Cho JH, Hwang WS, Lee YD, Reu DS, Suh-Kim H 2000 Expression of neuroD/BETA2 in mitotic and postmitotic neuronal cells during the development of nervous system. Dev Dyn 217:361-367
27. Yokoyama M, Nishi Y, Miyamoto Y, Nakamura M, Akiyama K, Matsubara K, Okubo K 1996 Molecular cloning of a human neuroD from a neuroblastoma cell line specifically expressed in the fetal brain and adult cerebellum. Brain Res Mol Brain Res 42:135-139
28. Nilaweera KN, Ellis C, Barrett P, Mercer JG, Morgan PJ 2002 Hypothalamic bHLH transcription factors are novel candidates in the regulation of energy balance. Eur J Neurosci 15:644-650
29. Lamolet B, Poulin G, Chu K, Guillemot F, Tsai MJ, Drouin J 2004 Tpit-independent function of NeuroD1(BETA2) in pituitary corticotroph differentiation. Mol Endocrinol 18:995-1003
30. Naya FJ, Huang HP, Qiu Y, Mutoh H, DeMayo FJ, Leiter AB, Tsai MJ 1997 Diabetes, defective pancreatic morphogenesis, and abnormal enteroendocrine differentiation in BETA2/neuroD-deficient mice. Genes Dev 11:2323-2334
31. Mutoh H, Fung BP, Naya FJ, Tsai MJ, Nishitani J, Leiter AB 1997 The basic helix-loop-helix transcription factor BETA2/NeuroD is expressed in mammalian enteroendocrine cells and activates secretin gene expression. Proc Natl Acad Sci USA 94:3560-3564
32. Poulin G, Turgeon B, Drouin J 1997 NeuroD1/beta2 contributes to cell-specific transcription of the proopiomelanocortin gene. Mol Cell Biol 17:6673-6682
33. Samal B, Sun Y, Stearns G, Xie C, Suggs S, McNiece I 1994 Cloning and characterization of the cDNA encoding a novel human pre-B-cell colonyenhancing factor. Mol Cell Biol 14:1431-1437
34. Revollo JR, Grimm AA, Imai S 2007 The regulation of nicotinamide adenine dinucleotide biosynthesis by Nampt/PBEF/visfatin in mammals. Curr Opin Gastroenterol 23:164-170
35. Fukuhara A, Matsuda M, Nishizawa M, Segawa K, Tanaka M, Kishimoto K, Matsuki Y, Murakami M, Ichisaka T, Murakami H, Watanabe E, Takagi T, Akiyoshi M, Ohtsubo T, Kihara S, Yamashita S, Makishima M, Funahashi T, Yamanaka S, Hiramatsu R, Matsuzawa Y, Shimomura I 2005 Visfatin: a protein secreted by visceral fat that mimics the effects of insulin. Science 307:426-430
36. Chen MP, Chung FM, Chang DM, Tsai JC, Huang HF, Shin SJ, Lee YJ 2006 Elevated plasma level of visfatin/pre-B cell colony-enhancing factor in patients with type 2 diabetes mellitus. J Clin Endocrinol Metab 91:295-299
37. Oki K, Yamane K, Kamei N, Nojima H, Kohno N 2007 Circulating visfatin level is correlated with inflammation, but not with insulin resistance. Clin Endocrinol 67:796-800
38. Ando H, Yanagihara H, Hayashi Y, Obi Y, Tsuruoka S, Takamura T, Kaneko S, Fujimura A 2005 Rhythmic messenger ribonucleic acid expression of clock genes and adipocytokines in mouse visceral adipose tissue. Endocrinology 146:5631-5636
39. Rutter J, Reick M, Wu LC, McKnight SL 2001 Regulation of clock and NPAS2 DNA binding by the redox state of NAD cofactors. Science 293:510-514
40. Reick M, Garcia JA, Dudley C, McKnight SL 2001 NPAS2: an analog of clock operative in the mammalian forebrain. Science 293:506-509
41. Segawa K, Fukuhara A, Hosogai N, Morita K, Okuno Y, Tanaka M, Nakagawa Y, Kihara S, Funahashi T, Komuro R, Matsuda M, Shimomura I 2006 Visfatin in adipocytes is upregulated by hypoxia through HIF1α-dependent mechanism. Biochem Biophys Res Commun 349:875-882
42. Bae SK, Kim SR, Kim JG, Kim JY, Koo TH, Jang HO, Yun I, Yoo MA, Bae MK 2006 Hypoxic induction of human visfatin gene is directly mediated by hypoxia-inducible factor-1. FEBS Lett 580:4105-4113
43. Brahimi-Horn MC, Pouyssegur J 2005 The hypoxia-inducible factor and tumor progression along the angiogenic pathway. Int Rev Cytol 242:157-213
44. Hogenesch JB, Gu YZ, Jain S, Bradfield CA 1998 The basic-helix-loop-helix-PAS orphan MOP3 forms transcriptionally active complexes with circadian and hypoxia factors. Proc Natl Acad Sci USA 95:5474-5479
45. Ghorbel MT, Coulson JM, Murphy D 2003 Cross-talk between hypoxic and circadian pathways: cooperative roles for hypoxia-inducible factor 1α and CLOCK in transcriptional activation of the vasopressin gene. Mol Cell Neurosci 22:396-404
46. Michan S, Sinclair D 2007 Sirtuins in mammals: insights into their biological function. Biochem J 404:1-13
47. Yang H, Lavu S, Sinclair DA 2006 Nampt/PBEF/Visfatin: a regulator of mammalian health and longevity? Exp Gerontol 41:718-726
48. Messager S, Hazlerigg DG, Mercer JG, Morgan PJ 2000 Photoperiod differentially regulates the expression of Per1 and ICER in the pars tuberalis and the suprachiasmatic nucleus of the Siberian hamster. Eur J Neurosci 12:2865-2870
49. Johnston JD, Tournier BB, Andersson H, Masson-Pevet M, Lincoln GA, Hazlerigg DG 2006 Multiple effects of melatonin on rhythmic clock gene expression in the mammalian pars tuberalis. Endocrinology 147:959-965
50. Tournier BB, Dardente H, Simonneaux V, Vivien-Roels B, Pevet P, Masson-Pevet M, Vuillez P 2007 Seasonal variations of clock gene expression in the suprachiasmatic nuclei and pars tuberalis of the European hamster (Cricetus cricetus). Eur J Neurosci 25:1529-1536
51. Stehle JH, von Gall C, Korf HW 2002 Organisation of the circadian system in melatonin-proficient C3H and melatonin-deficient C57BL mice: a comparative investigation. Cell Tissue Res 309:173-182
52. Wagner GC, Johnston JD, Tournier BB, Ebling FJ, Hazlerigg DG 2007 Melatonin induces gene-specific effects on rhythmic mRNA expression in the pars tuberalis of the Siberian hamster (Phodopus sungorus). Eur J Neurosci 25:485-490
53. Ko CH, Takahashi JS 2006 Molecular components of the mammalian circadian clock. Hum Mol Genet 15:R271-R277
54. Johnston JD, Cagampang FR, Stirland JA, Carr AJ, White MR, Davis JR, Loudon AS 2003 Evidence for an endogenous per1- and ICER-independent seasonal timer in the hamster pituitary gland. FASEB J 17:810-815
55. Hazlerigg DG, Andersson H, Johnston JD, Lincoln G 2004 Molecular characterization of the long-day response in the Soay sheep, a seasonal mammal. Curr Biol 14:334-339
56. Dupre SM, Loudon AS 2007 Circannual clocks: annual timers unraveled in sheep. Curr Biol 17:R216-R217
57. Barrett P, Morris M, Choi WS, Ross A, Morgan PJ 1999 Melatonin receptors and signal transduction mechanisms. Biol Signals Recept 8:6-14
58. Merks T, Schulze-Bonhage A, Wittkowski W 1993 Photoperiod- dependent changes in exocytotic activity in the hypophyseal pars tuberalis of the Djungarian hamster, Phodopus sungorus. Cell Tissue Res 273:287-291
59. Hazlerigg D, Loudon AS 2008 Seasonal life timers: new insights into ancient mechanisms. Curr Biol 18:R795-R804
60. Wittkowski W, Bockmann J, Kreutz MR, Bockers TM 1999 Cell and molecular biology of the pars tuberalis of the pituitary. Int Rev Cytol 185:157-194
61. Bockers TM, Bockmann J, Fauteck JD, Wittkowski W, Sabel BA, Kreutz MR 1996 Evidence for gene transcription of adenohypophyseal hormones in the ovine pars tuberalis. Neuroendocrinology 63:16-27
62. Klosen P, Bienvenu C, Demarteau O, Dardente H, Guerrero H, Pevet P, Masson-Pevet M 2002 The mt1 melatonin receptor and RORβ receptor are co-localized in specific TSH-immunoreactive cells in the pars tuberalis of the rat pituitary. J Histochem Cytochem 50:1647-1657
63. Dardente H, Klosen P, Pevet P, Masson-Pevet M 2003 MT1 melatonin receptor mRNA expressing cells in the pars tuberalis of the European hamster: effect of photoperiod. J Neuroendocrinol 15:778-786
64. Bockmann J, Bockers TM, Vennemann B, Niklowitz P, Muller J, Wittkowski W, Sabel B, Kreutz MR 1996 Short photoperiod-dependent down-regulation of thyrotropin-α and -β in hamster pars tuberalis-specific cells is prevented by pinealectomy. Endocrinology 137:1804-1813
65. Bockers TM, Niklowitz P, Bockmann J, Fauteck JD, Wittkowski W, Kreutz MR 1995 Daily melatonin injections induce cytological changes in pars tuberalis-specific cells similar to short photoperiod. J Neuroendocrinol 7:607-613
66. Hu W, Kieseier B, Frohman E, Eagar TN, Rosenberg RN, Hartung HP, Stuve O 2008 Prion proteins: physiological functions and role in neurological disorders. J Neurol Sci 264:1-8
67. Hu W, Rosenberg RN, Stuve O 2007 Prion proteins: a biological role beyond prion diseases. Acta Neurol Scand 116:75-82
68. Tobler I, Gaus SE, Deboer T, Achermann P, Fischer M, Rulicke T, Moser M, Oesch B, McBride PA, Manson JC 1996 Altered circadian activity rhythms and sleep in mice devoid of prion protein. Nature 380:639-642
69. Schroeder BC, Hechenberger M, Weinreich F, Kubisch C, Jentsch TJ 2000 KCNQ5, a novel potassium channel broadly expressed in brain, mediates M-type currents. J Biol Chem 275:24089-24095
70. + channel signaling in the arcuate nucleus. Endocrinology 148:4937-4951
71. Williams S, Johnston D 1988 Muscarinic depression of long-term potentiation in CA3 hippocampal neurons. Science 242:84-87
72. Nakao N, Ono H, Yamamura T, Anraku T, Takagi T, Higashi K, Yasuo S, Katou Y, Kageyama S, Uno Y, Kasukawa T, Iigo M, Sharp PJ, Iwasawa A, Suzuki Y, Sugano S, Niimi T, Mizutani M, Namikawa T, Ebihara S, Ueda HR, Yoshimura T 2008 Thyrotrophin in the pars tuberalis triggers photoperiodic response. Nature 452:317-322
73. Bechtold DA, Loudon AS 2007 Hypothalamic thyroid hormones: mediators of seasonal physiology. Endocrinology 148:3605-3607
74. Hanon EA, Lincoln G, Fustin JM, Dardente H, Masson-Pevet M, Morgan PJ, Hazlerigg D 2008 Ancestral TSH mechanism signals summer in a photoperiodic mammal. Curr Biol 18:1147-1152