Diurnal expression of functional and clock-related genes throughout the rat HPA axis: System-wide shifts in response to a restricted feeding schedule

American Journal of Physiology - Endocrinology and Metabolism

Volumn 296, Issue 4, 2009, Pages

  Girotti, Milena ^a,b   Weinberg, Marc S ^a   Spencer, Robert L ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b Mays Cancer Center at UT Health San Antonio   (United States)

Author keywords

Circadian rhythms; Hypothalamic pituitary adrenal axis

Indexed keywords

CORTICOSTERONE; CORTICOTROPIN; CELL CYCLE PROTEIN; NUCLEAR PROTEIN; PER2 PROTEIN, RAT; PERIOD CIRCADIAN PROTEIN; SIGNAL PEPTIDE;

ANIMAL EXPERIMENT; ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; FOOD AVAILABILITY; GENE EXPRESSION; HORMONE RELEASE; MALE; MOLECULAR CLOCK; NONHUMAN; PHOTOPERIODICITY; PRIORITY JOURNAL; RAT; ANIMAL; ANIMAL DISEASE; BIOLOGICAL RHYTHM; BLOOD; CALORIC RESTRICTION; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION; GENETICS; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS SYSTEM; METABOLISM; PHYSIOLOGY; SECRETION; SPRAGUE DAWLEY RAT; SUPRACHIASMATIC NUCLEUS; TIME;

ADRENOCORTICOTROPIC HORMONE; ANIMALS; BIOLOGICAL CLOCKS; CALORIC RESTRICTION; CELL CYCLE PROTEINS; CIRCADIAN RHYTHM; CORTICOSTERONE; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; NUCLEAR PROTEINS; PHOTOPERIOD; PITUITARY-ADRENAL SYSTEM; RATS; RATS, SPRAGUE-DAWLEY; SUPRACHIASMATIC NUCLEUS; TIME FACTORS;

EID: 65649088719     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.90946.2008     Document Type: Article

References (59)

1. Abe M, Herzog ED, Yamazaki S, Straume M, Tei H, Sakaki Y, Menaker M, Block GD. Circadian rhythms in isolated brain regions. J Neurosci 22: 350-356, 2002. (Pubitemid 34033512)
2. Amir S, Lamont EW, Robinson B, Stewart J. A circadian rhythm in the expression of PERIOD2 protein reveals a novel SCN-controlled oscillator in the oval nucleus of the bed nucleus of the stria terminalis. J Neurosci 24: 781-790, 2004. (Pubitemid 38146588)
3. Angeles-Castellanos M, Aguilar-Roblero R, Escobar C. c-Fos expression in hypothalamic nuclei of food-entrained rats. Am J Physiol Regul Integr Comp Physiol 286: R158-R165, 2004. (Pubitemid 38055905)
4. Asai M, Yoshinobu Y, Kaneko S, Mori A, Nikaido T, Moriya T, Akiyama M, Shibata S. Circadian profile of Per gene mRNA expression in the suprachiasmatic nucleus, paraventricular nucleus, and pineal body of aged rats. J Neurosci Res 66: 1133-1139, 2001. (Pubitemid 33135599)
5. 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.
6. Bittman EL, Doherty L, Huang L, Paroskie A. Period gene expression in mouse endocrine tissues. Am J Physiol Regul Integr Comp Physiol 285: R561-R569, 2003. (Pubitemid 37040564)
7. Buijs RM, van Eden CG, Goncharuk VD, Kalsbeek A. The biological clock tunes the organs of the body: timing by hormones and the autonomic nervous system. J Endocrinol 177: 17-26, 2003. (Pubitemid 36592583)
8. 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 11: 1535-1544, 1999.
9. Cascio CS, Shinsako J, Dallman MF. The suprachiasmatic nuclei stimulate evening ACTH secretion in the rat. Brain Res 423: 173-178, 1987. (Pubitemid 17157166)
10. Challet E, Caldelas I, Graff C, Pevet P. Synchronization of the molecular clockwork by light- and food-related cues in mammals. Biol Chem 384: 711-719, 2003. (Pubitemid 36747932)
11. Curran T, Morgan JI. Fos: an immediate-early transcription factor in neurons. J Neurobiol 26: 403-412, 1995.
12. Dallman MF, Akana SF, Cascio CS, Darlington DN, Jacobson L, Levin N. Regulation of ACTH secretion: variations on a theme of B. Recent Prog Horm Res 43: 113-173, 1987.
13. Dallman MF, Engeland WC, Rose JC, Wilkinson CW, Shinsako J, Siedenburg F. Nycthemeral rhythm in adrenal responsiveness to ACTH. Am J Physiol Regul Integr Comp Physiol 235: R210-R218, 1978.
14. Dallman MF, Strack AM, Akana SF, Bradbury MJ, Hanson ES, Scribner KA, Smith M. Feast and famine: critical role of glucocorticoids with insulin in daily energy flow. Front Neuroendocrinol 14: 303-347, 1993. (Pubitemid 23321823)
15. 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 14: 2950-2961, 2000.
16. Fahrenkrug J, Hannibal J, Georg B. Diurnal rhythmicity of the canonical clock genes Per1, Per2 and Bmal1 in the rat adrenal gland is unaltered after hypophysectomy. J Neuroendocrinol 20: 323-329, 2008.
17. Feillet CA, Mendoza J, Albrecht U, Pevet P, Challet E. Forebrain oscillators ticking with different clock hands. Mol Cell Neurosci 37: 209-221, 2008.
18. Fuller PM, Lu J, Saper CB. Differential rescue of light- and foodentrainable circadian rhythms. Science 320: 1074-1077, 2008.
19. Girotti M, Weinberg MS, Spencer RL. Differential responses of hypothalamus- pituitary-adrenal axis immediate early genes to corticosterone and circadian drive. Endocrinology 148: 2542-2552, 2007. (Pubitemid 46997027)
20. Gold PW, Goodwin FK, Chrousos GP. Clinical and biochemical manifestations of depression. Relation to the neurobiology of stress. N Engl J Med 319: 348-353, 1988.
21. Gooley JJ, Schomer A, Saper CB. The dorsomedial hypothalamic nucleus is critical for the expression of food-entrainable circadian rhythms. Nat Neurosci 9: 398-407, 2006. (Pubitemid 43290970)
22. Guilding C, Piggins HD. Challenging the omnipotence of the suprachiasmatic timekeeper: are circadian oscillators present throughout the mammalian brain? Eur J Neurosci 25: 3195-3216, 2007. (Pubitemid 46872769)
23. Hastings M, O'Neill JS, Maywood ES. Circadian clocks: regulators of endocrine and metabolic rhythms. J Endocrinol 195: 187-198, 2007. (Pubitemid 350143100)
24. Hastings MH, Reddy AB, Maywood ES. A clockwork web: circadian timing in brain and periphery, in health and disease. Nat Rev Neurosci 4: 649-661, 2003.
25. Honma S, Ikeda M, Abe H, Tanahashi Y, Namihira M, Honma K, Nomura M. Circadian oscillation of BMAL1, a partner of a mammalian clock gene Clock, in rat suprachiasmatic nucleus. Biochem Biophys Res Commun 250: 83-87, 1998. (Pubitemid 28448627)
26. Ishida A, Mutoh T, Ueyama T, Bando H, Masubuchi S, Nakahara D, Tsujimoto G, Okamura H. Light activates the adrenal gland: timing of gene expression and glucocorticoid release. Cell Metab 2: 297-307, 2005.
27. Jasper MS, Engeland WC. Splanchnic neural activity modulates ultradian and circadian rhythms in adrenocortical secretion in awake rats. Neuroendocrinology 59: 97-109, 1994.
28. Jasper MS, Engeland WC. Splanchnicotomy increases adrenal sensitivity to ACTH in nonstressed rats. Am J Physiol Endocrinol Metab 273: E363-E368, 1997.
29. Kalsbeek A, van Heerikhuize JJ, Wortel J, Buijs RM. Restricted daytime feeding modifies suprachiasmatic nucleus vasopressin release in rats. J Biol Rhythms 13: 18-29, 1998. (Pubitemid 128478943)
30. Krieger DT, Hauser H, Krey LC. Suprachiasmatic nuclear lesions do not abolish food-shifted circadian adrenal and temperature rhythmicity. Science 197: 398-399, 1977. (Pubitemid 8143839)
31. Lamont EW, Diaz LR, Barry-Shaw J, Stewart J, Amir S. Daily restricted feeding rescues a rhythm of period2 expression in the arrhythmic suprachiasmatic nucleus. Neuroscience 132: 245-248, 2005. (Pubitemid 40417900)
32. Leal AM, Moreira AC. Feeding and the diurnal variation of the hypothalamic- pituitary-adrenal axis and its responses to CRH and ACTH in rats. Neuroendocrinology 64: 14-19, 1996.
33. Leal AM, Moreira AC. Food and the circadian activity of the hypothalamic- pituitary-adrenal axis. Braz J Med Biol Res 30: 1391-1405, 1997.
34. Lemos DR, Downs JL, Urbanski HF. Twenty-four hour rhythmic gene expression in the rhesus macaque adrenal gland. Mol Endocrinol 20: 1164-1176, 2006.
35. Mendoza J. Circadian clocks: setting time by food. J Neuroendocrinol 19: 127-137, 2006.
36. Moore RY, Eichler VB. Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat. Brain Res 42: 201-206, 1972.
37. Mortola JF, Rasmussen DD, Yen SS. Alterations of the adrenocorticotropin- cortisol axis in normal weight bulimic women: evidence for a central mechanism. J Clin Endocrinol Metab 68: 517-522, 1989.
38. Oishi K, Amagai N, Shirai H, Kadota K, Ohkura N, Ishida N. Genome-wide expression analysis reveals 100 adrenal gland-dependent circadian genes in the mouse liver. DNA Res 12: 191-202, 2005.
39. Oster H, Damerow S, Hut RA, Eichele G. Transcriptional profiling in the adrenal gland reveals circadian regulation of hormone biosynthesis genes and nucleosome assembly genes. J Biol Rhythms 21: 350-361, 2006. (Pubitemid 44387427)
40. Oster H, Damerow S, Kiessling S, Jakubcakova V, Abraham D, Tian J, Hoffmann MW, Eichele G. The circadian rhythm of glucocorticoids is regulated by a gating mechanism residing in the adrenal cortical clock. Cell Metab 4: 163-173, 2006. (Pubitemid 44138721)
41. Owens MJ, Bartolome J, Schanberg SM, Nemeroff CB. Corticotropinreleasing factor concentrations exhibit an apparent diurnal rhythm in hypothalamic and extrahypothalamic brain regions: differential sensitivity to corticosterone. Neuroendocrinology 52: 626-631, 1990.
42. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates (4th ed.) San Diego, CA: Academic. 1998.
43. Reddy AB, Maywood ES, Karp NA, King VM, Inoue Y, Gonzalez FJ, Lilley KS, Kyriacou CP, Hastings MH. Glucocorticoid signaling synchronizes the liver circadian transcriptome. Hepatology 45: 1478-1488, 2007. (Pubitemid 46918332)
44. Reppert SM, Weaver DR. Coordination of circadian timing in mammals. Nature 418: 935-941, 2002.
45. Saper CB, Lu J, Chou TC, Gooley J. The hypothalamic integrator for circadian rhythms. Trends Neurosci 28: 152-157, 2005. (Pubitemid 40320761)
46. Son GH, Chung S, Choe HK, Kim HD, Baik SM, Lee H, Lee HW, Choi S, Sun W, Kim H, Cho S, Lee KH, Kim K. Adrenal peripheral clock controls the autonomous circadian rhythm of glucocorticoid by causing rhythmic steroid production. Proc Natl Acad Sci USA 105: 20970-20975, 2008.
47. Stephan FK. The "other" circadian system: food as a Zeitgeber. J Biol Rhythms 17: 284-292, 2002.
48. Stephan FK, Zucker I. Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proc Natl Acad Sci USA 69: 1583-1586, 1972.
49. Stokkan KA, Yamazaki S, Tei H, Sakaki Y, Menaker M. Entrainment of the circadian clock in the liver by feeding. Science 291: 490-493, 2001. (Pubitemid 32097074)
50. Torres-Farfan C, Valenzuela FJ, Ebensperger R, Mendez N, Campino C, Richter HG, Valenzuela GJ, Seron-Ferre M. Circadian cortisol secretion and circadian adrenal responses to ACTH are maintained in dexamethasone suppressed capuchin monkeys (Cebus apella). Am J Primatol 70: 93-100, 2008.
51. 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. Nat Neurosci 5: 234-238, 2002. (Pubitemid 34171136)
52. Wakamatsu H, Yoshinobu Y, Aida R, Moriya T, Akiyama M, Shibata S. Restricted-feeding-induced anticipatory activity rhythm is associated with a phase-shift of the expression of mPer1 and mPer2 mRNA in the cerebral cortex and hippocampus but not in the suprachiasmatic nucleus of mice. Eur J Neurosci 13: 1190-1196, 2001. (Pubitemid 32275756)
53. Watts AG, Swanson LW. Diurnal variations in the content of preprocorticotropin- releasing hormone messenger ribonucleic acids in the hypothalamic paraventricular nucleus of rats of both sexes as measured by in situ hybridization. Endocrinology 125: 1734-1738, 1989.
54. Watts AG, Tanimura S, Sanchez-Watts G. Corticotropin-releasing hormone and arginine vasopressin gene transcription in the hypothalamic paraventricular nucleus of unstressed rats: daily rhythms and their interactions with corticosterone. Endocrinology 145: 529-540, 2004. (Pubitemid 38183794)
55. Wilkinson CW, Shinsako J, Dallman MF. Daily rhythms in adrenal responsiveness to adrenocorticotropin are determined primarily by the time of feeding in the rat. Endocrinology 104: 350-359, 1979. (Pubitemid 9135843)
56. Williams G, Bing C, Cai XJ, Harrold JA, King PJ, Liu XH. The hypothalamus and the control of energy homeostasis: different circuits, different purposes. Physiol Behav 74: 683-701, 2001. (Pubitemid 34076616)
57. Yamamori E, Iwasaki Y, Taguchi T, Nishiyama M, Yoshida M, Asai M, Oiso Y, Itoi K, Kambayashi M, Hashimoto K. Molecular mechanisms for corticotropin-releasing hormone gene repression by glucocorticoid in BE(2)C neuronal cell line. Mol Cell Endocrinol 264: 142-148, 2007. (Pubitemid 46097309)
58. Yamamoto T, Nakahata Y, Tanaka M, Yoshida M, Soma H, Shinohara K, Yasuda A, Mamine T, Takumi T. Acute physical stress elevates mouse period1 mRNA expression in mouse peripheral tissues via a glucocorticoid-responsive element. J Biol Chem 280: 42036-42043, 2005. (Pubitemid 43023172)
59. 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. (Pubitemid 30241573)