Forced Desynchrony Reveals Independent Contributions of Suprachiasmatic Oscillators to the Daily Plasma Corticosterone Rhythm in Male Rats

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Wotus, Cheryl ^a   Lilley, Travis R ^b   Neal, Adam S ^a   Suleiman, Nicole L ^a   Schmuck, Stefanie C ^a   Smarr, Benjamin L ^b   Fischer, Brian J ^a   de la Iglesia, Horacio O ^b  

^a SEATTLE UNIVERSITY   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CORTICOSTERONE; CORTICOTROPIN;

ADRENERGIC SYSTEM; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CIRCADIAN RHYTHM; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; CORTICOSTERONE RELEASE; CORTICOTROPIN BLOOD LEVEL; EVOKED RESPONSE; HORMONAL REGULATION; HORMONE DETERMINATION; HORMONE SENSITIVITY; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LIGHT ADAPTATION; LOCOMOTION; MALE; NEUROMODULATION; NONHUMAN; OSCILLATION; RAT; SUPRACHIASMATIC NUCLEUS;

ADRENAL GLANDS; ANIMALS; CIRCADIAN RHYTHM; CORTICOSTERONE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MALE; MOTOR ACTIVITY; NEURONS; RATS; RATS, WISTAR; SPLANCHNIC NERVES; SUPRACHIASMATIC NUCLEUS;

EID: 84880647581     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068793     Document Type: Article

References (49)

1. Moore RY, Eichler VB, (1972) Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat. Brain Res 42: 201-206. doi:10.1016/0006-8993(72)90054-6. PubMed: 5047187.
2. Kalsbeek A, van der Spek R, Lei J, Endert E, Buijs RM, et al. (2012) Circadian rhythms in the hypothalamo-pituitary-adrenal (HPA) axis. Mol Cell Endocrinol 349: 20-29. doi:10.1016/j.mce.2011.06.042. PubMed: 21782883.
3. Gomez F, Chapleur M, Fernette B, Burlet C, Nicolas JP, et al. (1997) Arginine vasopressin (AVP) depletion in neurons of the suprachiasmatic nuclei affects the AVP content of the paraventricular neurons and stimulates adrenocorticotrophic hormone release. J Neurosci Res 50: 565-574. doi:10.1002/(SICI)1097-4547(19971115)50:4. PubMed: 9404718.
4. Kalsbeek A, Buijs RM, van Heerikhuize JJ, Arts M, van der Woude TP, (1992) Vasopressin-containing neurons of the suprachiasmatic nuclei inhibit corticosterone release. Brain Res 580: 62-67. doi:10.1016/0006-8993(92)90927-2. PubMed: 1504818.
5. Buijs RM, Kalsbeek A, van der Woude TP, van Heerikhuize JJ, Shinn S, (1993) Suprachiasmatic nucleus lesion increases corticosterone secretion. Am J Physiol 264: R1186-R1192. PubMed: 8322972.
6. Kalsbeek A, van Heerikhuize JJ, Wortel J, Buijs RM, (1996) A diurnal rhythm of stimulatory input to the hypothalamo-pituitary-adrenal system as revealed by timed intrahypothalamic administration of the vasopressin V1 antagonist. J Neurosci 16: 5555-5565. PubMed: 8757267.
7. Dallman MF, Engeland WC, Rose JC, Wilkinson CW, Shinsako J, et al. (1978) Nycthemeral rhythm in adrenal responsiveness to ACTH. Am J Physiol 235: R210-R218. PubMed: 215040.
8. Akana SF, Cascio CS, Du JZ, Levin N, Dallman MF, (1986) Reset of feedback in the adrenocortical system: an apparent shift in sensitivity of adrenocorticotropin to inhibition by corticosterone between morning and evening. Endocrinology 119: 2325-2332. doi:10.1210/endo-119-5-2325. PubMed: 3021439.
9. Kaneko M, Hiroshige T, Shinsako J, Dallman MF, (1980) Diurnal changes in amplification of hormone rhythms in the adrenocortical system. Am J Physiol 239: R309-R316. PubMed: 6254377.
10. Wilkinson CW, Shinsako J, Dallman MF, (1981) Return of pituitary-adrenal function after adrenal enucleation or transplantation: diurnal rhythms and responses to ether. Endocrinology 109: 162-169. doi:10.1210/endo-109-1-162. PubMed: 6263583.
11. Ulrich-Lai YM, Arnhold MM, Engeland WC, (2006) Adrenal splanchnic innervation contributes to the diurnal rhythm of plasma corticosterone in rats by modulating adrenal sensitivity to ACTH. Am J Physiol Regul Integr Comp Physiol 290: R1128-R1135. PubMed: 16357102.
12. Jasper MS, Engeland WC, (1997) Splanchnicotomy increases adrenal sensitivity to ACTH in nonstressed rats. Am J Physiol 273: E363-E368. PubMed: 9277390.
13. Ulrich-Lai YM, Engeland WC, (2002) Adrenal splanchnic innervation modulates adrenal cortical responses to dehydration stress in rats. Neuroendocrinology 76: 79-92. doi:10.1159/000064426. PubMed: 12169769.
14. Buijs RM, Wortel J, Van Heerikhuize JJ, Feenstra MG, Ter Horst GJ, et al. (1999) Anatomical and functional demonstration of a multisynaptic suprachiasmatic nucleus adrenal (cortex) pathway. Eur J Neurosci 11: 1535-1544. doi:10.1046/j.1460-9568.1999.00575.x. PubMed: 10215906.
15. Ishida A, Mutoh T, Ueyama T, Bando H, Masubuchi S, et al. (2005) Light activates the adrenal gland: Timing of gene expression and glucocorticoid release. Cell Metab 2: 297-307. doi:10.1016/j.cmet.2005.09.009. PubMed: 16271530.
16. Moore RY, Speh JC, Leak RK, (2002) Suprachiasmatic nucleus organization. Cell Tissue Res 309: 89-98. doi:10.1007/s00441-002-0575-2. PubMed: 12111539.
17. Watanabe K, Hiroshige T, (1981) Phase relation between episodic fluctuations of spontaneous locomotor activity and plasma corticosterone in rats with suprachiasmatic nuclei lesions. Neuroendocrinology 33: 52-59. doi:10.1159/000123200. PubMed: 7254480.
18. Abe K, Kroning J, Greer MA, Critchlow V, (1979) Effects of destruction of the suprachiasmatic nuclei on the circadian rhythms in plasma corticosterone, body temperature, feeding and plasma thyrotropin. Neuroendocrinology 29: 119-131. doi:10.1159/000122913. PubMed: 503281.
19. Szafarczyk A, Ixart G, Malaval F, Nouguier-Soulé J, Assenmacher I, (1979) Effects of lesions of the suprachiasmatic nuclei and of p-chlorophenylalanine on the circadian rhythms of adrenocorticotrophic hormone and corticosterone in the plasma, and on locomotor activity of rats. J Endocrinol 83: 1-16. doi:10.1677/joe.0.0830001. PubMed: 230270.
20. de la Iglesia HO, Cambras T, Schwartz WJ, Díez-Noguera A, (2004) Forced desynchronization of dual circadian oscillators within the rat suprachiasmatic nucleus. Curr Biol 14: 796-800. doi:10.1016/j.cub.2004.04.034. PubMed: 15120072.
21. Schwartz MD, Wotus C, Liu T, Friesen WO, Borjigin J, et al. (2009) Dissociation of circadian and light inhibition of melatonin release through forced desynchronization in the rat. Proc Natl Acad Sci U S A 106: 17540-17545. doi:10.1073/pnas.0906382106. PubMed: 19805128.
22. Lee ML, Swanson BE, de la Iglesia HO, (2009) Circadian timing of REM sleep is coupled to an oscillator within the dorsomedial suprachiasmatic nucleus. Curr Biol 19: 848-852. doi:10.1016/j.cub.2009.03.051. PubMed: 19375313.
23. Cambras T, Weller JR, Anglès-Pujoràs M, Lee ML, Christopher A, et al. (2007) Circadian desynchronization of core body temperature and sleep stages in the rat. Proc Natl Acad Sci U S A 104: 7634-7639. doi:10.1073/pnas.0702424104. PubMed: 17452631.
24. Schwartz WJ, (2009) Circadian rhythms: a tale of two nuclei. Curr Biol 19: R460-R462. doi:10.1016/j.cub.2009.04.044. PubMed: 19515356.
25. Jasper MS, Engeland WC, (1991) Synchronous ultradian rhythms in adrenocortical secretion detected by microdialysis in awake rats. Am J Physiol 261: R1257-R1268. PubMed: 1951775.
26. Efron B, Tibshirani RJ, (1993) An Introduction to the Bootstrap; Hall Ca, eds. New York.
27. Kalsbeek A, van der Vliet J, Buijs RM, (1996) Decrease of endogenous vasopressin release necessary for expression of the circadian rise in plasma corticosterone: a reverse microdialysis study. J Neuroendocrinol 8: 299-307. PubMed: 8861286.
28. Smarr BL, Morris E, de la Iglesia HO, (2012) The dorsomedial suprachiasmatic nucleus times circadian expression of Kiss1 and the luteinizing hormone surge. Endocrinology 153: 2839-2850. doi:10.1210/en.2011-1857. PubMed: 22454148.
29. Wood CE, Shinsako J, Keil LC, Dallman MF, (1982) Adrenal sensitivity to adrenocorticotropin in normovolemic and hypovolemic conscious dogs. Endocrinology 110: 1422-1429. doi:10.1210/endo-110-4-1422. PubMed: 6277606.
30. Kaneko M, Kaneko K, Shinsako J, Dallman MF, (1981) Adrenal sensitivity to adrenocorticotropin varies diurnally. Endocrinology 109: 70-75. doi:10.1210/endo-109-1-70. PubMed: 6263595.
31. Dijkstra I, Binnekade R, Tilders FJ, (1996) Diurnal variation in resting levels of corticosterone is not mediated by variation in adrenal responsiveness to adrenocorticotropin but involves splanchnic nerve integrity. Endocrinology 137: 540-547. doi:10.1210/en.137.2.540. PubMed: 8593800.
32. Colwell CS, (2011) Linking neural activity and molecular oscillations in the SCN. Nat Rev Neurosci 12: 553-569. doi:10.1038/nrn3086. PubMed: 21886186.
33. Yan L, Takekida S, Shigeyoshi Y, Okamura H, (1999) Per1 and Per2 gene expression in the rat suprachiasmatic nucleus: circadian profile and the compartment-specific response to light. Neuroscience 94: 141-150. doi:10.1016/S0306-4522(99)00223-7. PubMed: 10613504.
34. Cascio CS, Shinsako J, Dallman MF, (1987) The suprachiasmatic nuclei stimulate evening ACTH secretion in the rat. Brain Res 423: 173-178. doi:10.1016/0006-8993(87)90837-7. PubMed: 2823985.
35. Alexander LD, Sander LD, (1994) Vasoactive intestinal peptide stimulates ACTH and corticosterone release after injection into the PVN. Regul Pept 51: 221-227. doi:10.1016/0167-0115(94)90068-X. PubMed: 7938706.
36. Loh DH, Abad C, Colwell CS, Waschek JA, (2008) Vasoactive intestinal peptide is critical for circadian regulation of glucocorticoids. Neuroendocrinology 88: 246-255. doi:10.1159/000140676. PubMed: 18562786.
37. Lilley TR, Wotus C, Taylor D, Lee JM, de la Iglesia HO, (2012) Circadian regulation of cortisol release in behaviorally split golden hamsters. Endocrinology 153: 732-738. doi:10.1210/en.2011-1624. PubMed: 22128030.
38. Ottenweller JE, Meier AH, (1982) Adrenal innervation may be an extrapituitary mechanism able to regulate adrenocortical rhythmicity in rats. Endocrinology 111: 1334-1338. doi:10.1210/endo-111-4-1334. PubMed: 6288356.
39. Jasper MS, Engeland WC, (1994) Splanchnic neural activity modulates ultradian and circadian rhythms in adrenocortical secretion in awake rats. Neuroendocrinology 59: 97-109. doi:10.1159/000126645. PubMed: 8127410.
40. Oster H, Damerow S, Kiessling S, Jakubcakova V, Abraham D, et al. (2006) The circadian rhythm of glucocorticoids is regulated by a gating mechanism residing in the adrenal cortical clock. Cell Metab 4: 163-173. doi:10.1016/j.cmet.2006.07.002. PubMed: 16890544.
41. Son GH, Chung S, Choe HK, Kim HD, Baik SM, et al. (2008) Adrenal peripheral clock controls the autonomous circadian rhythm of glucocorticoid by causing rhythmic steroid production. Proc Natl Acad Sci U S A 105: 20970-20975. doi:10.1073/pnas.0806962106. PubMed: 19091946.
42. Krieger DT, Hauser H, Krey LC, (1977) Suprachiasmatic nuclear lesions do not abolish food-shifted circadian adrenal and temperature rhythmicity. Science 197: 398-399. doi:10.1126/science.877566. PubMed: 877566.
43. Haus E, Smolensky M, (2006) Biological clocks and shift work: circadian dysregulation and potential long-term effects. Cancer Causes Control 17: 489-500. doi:10.1007/s10552-005-9015-4. PubMed: 16596302.
44. Sack RL, Blood ML, Lewy AJ, (1992) Melatonin rhythms in night shift workers. Sleep 15: 434-441. PubMed: 1455127.
45. Reinberg A, Ashkenazi I, (2008) Internal desynchronization of circadian rhythms and tolerance to shift work. Chronobiol Int 25: 625-643. doi:10.1080/07420520802256101. PubMed: 18622820.
46. Scheer FA, Hu K, Evoniuk H, Kelly EE, Malhotra A, et al. (2010) Impact of the human circadian system, exercise, and their interaction on cardiovascular function. Proc Natl Acad Sci U S A, 107: 20541-6. PubMed: 21059915.
47. Karlsson B, Knutsson A, Lindahl B, (2001) Is there an association between shift work and having a metabolic syndrome? Results from a population based study of 27,485 people. Occup Environ Med 58: 747-752. doi:10.1136/oem.58.11.747. PubMed: 11600731.
48. Kroenke CH, Spiegelman D, Manson J, Schernhammer ES, Colditz GA, et al. (2007) Work characteristics and incidence of type 2 diabetes in women. Am J Epidemiol 165: 175-183. PubMed: 17071844.
49. Morikawa Y, Nakagawa H, Miura K, Soyama Y, Ishizaki M, et al. (2007) Effect of shift work on body mass index and metabolic parameters. Scand J Work Environ Health 33: 45-50. doi:10.5271/sjweh.1063. PubMed: 17353964.