The circadian system: A regulatory feedback network of periphery and brain

Physiology

Volumn 31, Issue 3, 2016, Pages 170-181

  Buijs, Frederik N ^a,b   León Mercado, Luis ^a   Guzmán Ruiz, Mara ^d   Guerrero Vargas, Natali N ^d   Romo Nava, Francisco ^a,c   Buijs, Ruud M ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^c UNIVERSITY OF CINCINNATI   (United States)

^d UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; BEHAVIOR; CIRCADIAN RHYTHM; HUMAN; HYPOTHALAMUS; NERVOUS SYSTEM FUNCTION; PHYSIOLOGY; SUPRACHIASMATIC NUCLEUS;

ANIMALS; BEHAVIOR; CIRCADIAN CLOCKS; CIRCADIAN RHYTHM; HUMANS; HYPOTHALAMUS; NERVOUS SYSTEM PHYSIOLOGICAL PHENOMENA; SUPRACHIASMATIC NUCLEUS;

EID: 84983803995     PISSN: 15489213     EISSN: 15489221     Source Type: Journal    
DOI: 10.1152/physiol.00037.2015     Document Type: Review

References (122)

1. Albus H, Vansteensel MJ, Michel S, Block GD, Meijer JH. A GABAergic mechanism is necessary for coupling dissociable ventral and dorsal regional oscillators within the circadian clock. Curr Biol 15: 886-893, 2005.
2. An S, Harang R, Meeker K, Granados-Fuentes D, Tsai CA, Mazuski C, Kim J, Doyle FJ, III, Petzold LR, Herzog ED. A neuropeptide speeds circadian entrainment by reducing intercellular synchrony. Proc Natl Acad Sci USA 110: E4355-E4361, 2013.
3. Avery DH, Shah SH, Eder DN, Wildschiodtz G. Nocturnal sweating and temperature in depression. Acta Psychiatr Scand 100: 295-301, 1999.
4. 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.
5. Belle MD, Hughes AT, Bechtold DA, Cunningham P, Pierucci M, Burdakov D, Piggins HD. Acute suppressive and longterm phase modulation actions of orexin on the mammalian circadian clock. J Neurosci 34: 3607-3621, 2014.
6. Bellefontaine N, Chachlaki K, Parkash J, Vanacker C, Colledge W, d’Anglemont dT, X, Garthwaite J, Bouret SG, Prevot V. Leptin-dependent neuronal NO signaling in the preoptic hypothalamus facilitates reproduction. J Clin Invest 124: 3678, 2014.
7. Bonten TN, Snoep JD, Assendelft WJ, Zwaginga JJ, Eikenboom J, Huisman MV, Rosendaal FR, van der Bom JG. Timedependent effects of aspirin on blood pressure and morning platelet reactivity: a randomized cross-over trial. Hypertension 65: 743-750, 2015.
8. Bookout AL, de Groot MH, Owen BM, Lee S, Gautron L, Lawrence HL, Ding X, Elmquist JK, Takahashi JS, Mangelsdorf DJ, Kliewer SA. FGF21 regulates metabolism and circadian behavior by acting on the nervous system. Nat Med 19: 1147-1152, 2013.
9. Bothorel B, Barassin S, Saboureau M, Perreau S, Vivien-Roels B, Malan A, Pevet P. In the rat, exogenous melatonin increases the amplitude of pineal melatonin secretion by a direct action on the circadian clock. Eur J Neurosci 16: 1090-1098, 2002.
10. Brandstaetter R. Circadian lessons from peripheral clocks: is the time of the mammalian pacemaker up? Proc Natl Acad Sci USA 101: 5699-5700, 2004.
11. Brown SA, Zumbrunn G, Fleury-Olela F, Preitner N, Schibler U. Rhythms of mammalian body temperature can sustain peripheral circadian clocks. Curr Biol 12: 1574-1583, 2002.
12. Buijs FN, Cazarez F, Basualdo MC, Scheer FA, Perusquia M, Centurion D, Buijs RM. The suprachiasmatic nucleus is part of a neural feedback circuit adapting blood pressure response. Neuroscience 266: 197-207, 2014.
13. Buijs RM, Escobar C, Swaab DF. The circadian system and the balance of the autonomic nervous system. Handb Clin Neurol 117: 173-191, 2013.
14. Buijs RM, Kalsbeek A. Hypothalamic integration of central and peripheral clocks. Nat Rev Neurosci 2: 521-526, 2001.
15. Buijs RM, Scheer FA, Kreier F, Yi C, Bos N, Goncharuk VD, Kalsbeek A. Chapter 20: Organization of circadian functions: interaction with the body. Prog Brain Res 153: 341-360, 2006.
16. Bunney BG, Bunney WE. Mechanisms of rapid antidepressant effects of sleep deprivation therapy: clock genes and circadian rhythms. Biol Psychiatry 73: 1164-1171, 2013.
17. Cailotto C, La Fleur SE, Van Heijningen C, Wortel J, Kalsbeek A, Feenstra M, Pevet P, Buijs RM. The suprachiasmatic nucleus controls the daily variation of plasma glucose via the autonomic output to the liver: are the clock genes involved? Eur J Neurosci 22: 2531-2540, 2005.
18. Cheng B, Anea CB, Yao L, Chen F, Patel V, Merloiu A, Pati P, Caldwell RW, Fulton DJ, Rudic RD. Tissue-intrinsic dysfunction of circadian clock confers transplant arteriosclerosis. Proc Natl Acad Sci USA 108: 17147-17152, 2011.
19. Cheng MY, Bullock CM, Li C, Lee AG, Bermak JC, Belluzzi J, Weaver DR, Leslie FM, Zhou QY. Prokineticin 2 transmits the behavioural circadian rhythm of the suprachiasmatic nucleus. Nature 417: 405-410, 2002.
20. Colwell CS. Linking neural activity and molecular oscillations in the SCN. Nat Rev Neurosci 12: 553-569, 2011.
21. 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.
22. Davis S, Mirick DK, Stevens RG. Night shift work, light at night, and risk of breast cancer. J Natl Cancer Inst 93: 1557-1562, 2001.
23. Dibner C, Schibler U. Circadian timing of metabolism in animal models and humans. J Intern Med 277: 513-527, 2015.
24. Doi M, Takahashi Y, Komatsu R, Yamazaki F, Yamada H, Haraguchi S, Emoto N, Okuno Y, Tsujimoto G, Kanematsu A, Ogawa O, Todo T, Tsutsui K, van der Horst GT, Okamura H. Salt-sensitive hypertension in circadian clock-deficient Cry-null mice involves dysregulated adrenal Hsd3b6. Nat Med 16: 67-74, 2010.
25. Farajnia S, Michel S, Deboer T, Vanderleest HT, Houben T, Rohling JH, Ramkisoensing A, Yasenkov R, Meijer JH. Evidence for neuronal desynchrony in the aged suprachiasmatic nucleus clock. J Neurosci 32: 5891-5899, 2012.
26. Gamble KL, Resuehr D, Johnson CH. Shift work and circadian dysregulation of reproduction. Front Endocrinol (Lausanne) 4: 92, 2013.
27. Gerkema MP, Groos GA, Daan S. Differential elimination of circadian and ultradian rhythmicity by hypothalamic lesions in the common vole, Microtus arvalis. J Biol Rhythms 5: 81-95, 1990.
28. Gibbs J, Ince L, Matthews L, Mei J, Bell T, Yang N, Saer B, Begley N, Poolman T, Pariollaud M, Farrow S, DeMayo F, Hussell T, Worthen GS, Ray D, Loudon A. An epithelial circadian clock controls pulmonary inflammation and glucocorticoid action. Nat Med 20: 919-926, 2014.
29. Goncharuk VD, Van Heerikhuize J, Dai JP, Swaab DF, Buijs RM. Neuropeptide changes in the suprachiasmatic nucleus in primary hypertension indicate functional impairment of the biological clock. J Comp Neurol 431: 320-330, 2001.
30. Granados-Fuentes D, Tseng A, Herzog ED. A circadian clock in the olfactory bulb controls olfactory responsivity. J Neurosci 26: 12219-12225, 2006.
31. Guerrero-Vargas NN, Guzman-Ruiz M, Fuentes R, Garcia J, Salgado-Delgado R, Basualdo MD, Escobar C, Markus RP, Buijs RM. Shift work in rats results in increased inflammatory response after lipopolysaccharide administration: a role for food consumption. J Biol Rhythms 30: 318-330, 2015.
32. Guerrero-Vargas NN, Salgado-Delgado R, Basualdo MC, Garcia J, Guzman-Ruiz M, Carrero JC, Escobar C, Buijs RM. Reciprocal interaction between the suprachiasmatic nucleus and the immune system tunes down the inflammatory response to lipopolysaccharide. J Neuroimmunol 273: 22-30, 2014.
33. Guilding C, Hughes AT, Brown TM, Namvar S, Piggins HD. A riot of rhythms: neuronal and glial circadian oscillators in the mediobasal hypothalamus. Mol Brain 2: 28-32, 2009.
34. Gumz ML, Stow LR, Lynch IJ, Greenlee MM, Rudin A, Cain BD, Weaver DR, Wingo CS. The circadian clock protein Period 1 regulates expression of the renal epithelial sodium channel in mice. J Clin Invest 119: 2423-2434, 2009.
35. Guo H, Brewer JM, Champhekar A, Harris RB, Bittman EL. Differential control of peripheral circadian rhythms by suprachiasmatic-dependent neural signals. Proc Natl Acad Sci USA 102: 3111-3116, 2005.
36. Guzman-Ruiz M, Saderi N, Cazarez-Marquez F, Guerrero-Vargas NN, Basualdo MC, Acosta-Galvan G, Buijs RM. The suprachiasmatic nucleus changes the daily activity of the arcuate nucleus alpha-MSH neurons in male rats. Endocrinology 155: 525-535, 2014.
37. Guzman-Ruiz MA, Ramirez-Corona A, Guerrero-Vargas NN, Sabath E, Ramirez-Placencia O, Fuentes-Romero JA, Leon-Mercado L, Basualdo MC, Buijs RM. The suprachiasmatic and arcuate nucleus orchestrate the diurnal temperature decrease in the rat. J Neurosci 35: 15419-15429, 2015.
38. Harmar AJ, Marston HM, Shen S, Spratt C, West KM, Sheward WJ, Morrison CF, Dorin JR, Piggins HD, Reubi JC, Kelly JS, Maywood ES, Hastings MH. The VPAC(2) receptor is essential for circadian function in the mouse suprachiasmatic nuclei. Cell 109: 497-508, 2002.
39. Hastings MH, Brancaccio M, Maywood ES. Circadian pacemaking in cells and circuits of the suprachiasmatic nucleus. J Neuroendocrinol 26: 2-10, 2013.
40. Hermida RC, Ayala DE, Fernandez JR, Calvo C. Chronotherapy improves blood pressure control and reverts the nondipper pattern in patients with resistant hypertension. Hypertension 51: 69-76, 2008.
41. Herzog ED, Schwartz WJ. A neural clockwork for encoding circadian time. J Appl Physiol 92: 401-408, 2002.
42. Hirao A, Tahara Y, Kimura I, Shibata S. A balanced diet is necessary for proper entrainment signals of the mouse liver clock. PLos One 4: e6909, 2009.
43. Howell MJ, Schenck CH. Treatment of nocturnal eating disorders. Curr Treat Options Neurol 11: 333-339, 2009.
44. Huang H, Kong D, Byun KH, Ye C, Koda S, Lee DH, Oh BC, Lee SW, Lee B, Zabolotny JM, Kim MS, Bjorbaek C, Lowell BB, Kim YB. Rho-kinase regulates energy balance by targeting hypothalamic leptin receptor signaling. Nat Neurosci 15: 1391-1398, 2012.
45. Hughes AT, Piggins HD. Feedback actions of locomotor activity to the circadian clock. Prog Brain Res 199: 305-336, 2012.
46. Innominato PF, Roche VP, Palesh OG, Ulusakarya A, Spiegel D, Levi FA. The circadian timing system in clinical oncology. Ann Med 46: 191-207, 2014.
47. 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.
48. Kalsbeek A, Buijs RM. Output pathways of the mammalian suprachiasmatic nucleus: coding circadian time by transmitter selection and specific targeting. Cell Tissue Res 309: 109-118, 2002.
49. Kalsbeek A, Vanheerikhuize JJ, Wortel J, Buijs RM. A diurnal rhythm of stimulatory input to the hypothalamo-pituitary-adrenal system as revealed by timed intrahypothalamic administration of the vasopressin V-1 antagonist. J Neurosci 16: 5555-5565, 1996.
50. Kalsbeek A, Verhagen LA, Schalij I, Foppen E, Saboureau M, Bothorel B, Buijs RM, Pevet P. Opposite actions of hypothalamic vasopressin on circadian corticosterone rhythm in nocturnal versus diurnal species. Eur J Neurosci 27: 818-827, 2008.
51. Knutsson A, Kempe A. Shift work and diabetes: a systematic review. Chronobiol Int 31: 1146-1151, 2014.
52. Kolbe I, Dumbell R, Oster H. Circadian clocks and the interaction between stress axis and adipose function. Int J Endocrinol 2015: 693204, 2015.
53. Kreier F, Kap YS, Mettenleiter TC, Van Heijningen C, Van der Vliet J, Kalsbeek A, Sauerwein HP, Fliers E, Romijn JA, Buijs RM. Tracing from fat tissue, liver and pancreas: a neuroanatomical framework for the role of the brain in type 2 diabetes. Endocrinology 147: 1140-1147, 2005.
54. Lamia KA, Storch KF, Weitz CJ. Physiological significance of a peripheral tissue circadian clock. Proc Natl Acad Sci USA 105: 15172-15177, 2008.
55. 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.
56. Lee IT, Chang AS, Manandhar M, Shan Y, Fan J, Izumo M, Ikeda Y, Motoike T, Dixon S, Seinfeld JE, Takahashi JS, Yanagisawa M. Neuromedin s-producing neurons act as essential pacemakers in the suprachiasmatic nucleus to couple clock neurons and dictate circadian rhythms. Neuron 85: 1086-1102, 2015.
57. Lewy AJ, Lefler BJ, Emens JS, Bauer VK. The circadian basis of winter depression. Proc Natl Acad Sci USA 103: 7414-7419, 2006.
58. Li AJ, Wiater MF, Oostrom MT, Smith BR, Wang Q, Dinh TT, Roberts BL, Jansen HT, Ritter S. Leptin-sensitive neurons in the arcuate nuclei contribute to endogenous feeding rhythms. Am J Physiol Regul Integr Comp Physiol 302: R1313-R1326, 2012.
59. Li JZ, Bunney BG, Meng F, Hagenauer MH, Walsh DM, Vawter MP, Evans SJ, Choudary PV, Cartagena P, Barchas JD, Schatzberg AF, Jones EG, Myers RM, Watson SJ Jr, Akil H, Bunney WE. Circadian patterns of gene expression in the human brain and disruption in major depressive disorder. Proc Natl Acad Sci USA 110: 9950-9955, 2013.
60. Liu S, Chen XM, Yoda T, Nagashima K, Fukuda Y, Kanosue K. Involvement of the suprachiasmatic nucleus in body temperature modulation by food deprivation in rats. Brain Res 929: 26-36, 2002.
61. Lowrey PL, Takahashi JS. Genetics of the mammalian circadian system: photic entrainment, circadian pacemaker mechanisms, and posttranslational regulation. Annu Rev Genet 34: 533-562, 2000.
62. Malek ZS, Sage D, Pevet P, Raison S. Daily rhythm of tryptophan hydroxylase-2 messenger ribonucleic acid within raphe neurons is induced by corticoid daily surge and modulated by enhanced locomotor activity. Endocrinology 148: 5165-5172, 2007.
63. Marpegan L, Bekinschtein TA, Costas MA, Golombek DA. Circadian responses to endotoxin treatment in mice. J Neuroimmunol 160: 102-109, 2005.
64. Martino TA, Tata N, Belsham DD, Chalmers J, Straume M, Lee P, Pribiag H, Khaper N, Liu PP, Dawood F, Backx PH, Ralph MR, Sole MJ. Disturbed diurnal rhythm alters gene expression and exacerbates cardiovascular disease with rescue by resynchronization. Hypertension 49: 1104-1113, 2007.
65. Matsuo T, Yamaguchi S, Mitsui S, Emi A, Shimoda F, Okamura H. Control mechanism of the circadian clock for timing of cell division in vivo. Science 302: 255-259, 2003.
66. Meijer JH, Schaap J, Watanabe K, Albus H. Multiunit activity recordings in the suprachiasmatic nuclei: in vivo versus in vitro models. Brain Res 753: 322-327, 1997.
67. Meijer JH, Watanabe K, Schaap J, Albus H, Dθtβri L. Light responsiveness of the suprachiasmatic nucleus: long-term multiunit and singleunit recordings in freely moving rats. J Neurosci 18: 9078-9087, 1998.
68. Mendoza J, Graff C, Dardente H, Pevet P, Challet E. Feeding cues alter clock gene oscillations and photic responses in the suprachiasmatic nuclei of mice exposed to a light/dark cycle. J Neurosci 25: 1514-1522, 2005.
69. Mendoza J, Pevet P, Challet E. High-fat feeding alters the clock synchronization to light. J Physiol 586: 5901-5910, 2008.
70. Mohawk JA, Green CB, Takahashi JS. Central and peripheral circadian clocks in mammals. Annu Rev Neurosci 35: 445-462, 2012.
71. Moore RY, Eichler VB. Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat. Brain Res 42: 201-206, 1972.
72. Morrison SF, Nakamura K. Central neural pathways for thermoregulation. Front Biosci 16: 74-104, 2011.
73. Muller JE, Stone PH, Turi ZG. Circadian variation in the frequency of onset of acute myocardial infarction. N Engl J Med 313: 1315-1322, 1985.
74. Noman N, Monjo T, Moscato P, Iba H. Evolving robust gene regulatory networks. PLos One 10: e0116258, 2015.
75. Novakova M, Prasko J, Latalova K, Sladek M, Sumova A. The circadian system of patients with bipolar disorder differs in episodes of mania and depression. Bipolar Disord 17: 303-314, 2014.
76. Ohdo S, Koyanagi S, Suyama H, Higuchi S, Aramaki H. Changing the dosing schedule minimizes the disruptive effects of interferon on clock function. Nat Med 7: 356-360, 2001.
77. 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.
78. Owen BM, Bookout AL, Ding X, Lin VY, Atkin SD, Gautron L, Kliewer SA, Mangelsdorf DJ. FGF21 contributes to neuroendocrine control of female reproduction. Nat Med 19: 1153-1156, 2013.
79. Palm IF, Van Der Beek EM, Wiegant VM, Buijs RM, Kalsbeek A. Vasopressin induces a luteinizing hormone surge in ovariectomized, estradioltreated rats with lesions of the suprachiasmatic nucleus. Neuroscience 93: 659-666, 1999.
80. Partch CL, Green CB, Takahashi JS. Molecular architecture of the mammalian circadian clock. Trends Cell Biol 24: 90-99, 2014.
81. Paschos GK, FitzGerald GA. Circadian clocks and vascular function. Circ Res 106: 833-841, 2010.
82. Paschos GK, Ibrahim S, Song WL, Kunieda T, Grant G, Reyes TM, Bradfield CA, Vaughan CH, Eiden M, Masoodi M, Griffin JL, Wang F, Lawson JA, FitzGerald GA. Obesity in mice with adipocyte-specific deletion of clock component Arntl. Nat Med 18: 1768-1777, 2012.
83. Perreau-Lenz S, Kalsbeek A, Pevet P, Buijs RM. Glutamatergic clock output stimulates melatonin synthesis at night. Eur J Neurosci 19: 318-324, 2004.
84. Peters RV, Zoeller RT, Hennessey AC, Stopa EG, Anderson G, Albers HE. The control of circadian rhythms and the levels of vasoactive intestinal peptide messenger RNA in the suprachiasmatic nucleus are altered in spontaneously hypertensive rats. Brain Res 639: 217-227, 1994.
85. Ramsey KM, Yoshino J, Brace CS, Abrassart D, Kobayashi Y, Marcheva B, Hong HK, Chong JL, Buhr ED, Lee C, Takahashi JS, Imai SI, Bass J. Circadian clock feedback cycle through NAMPTmediated NAD+ biosynthesis. Science 324: 651-654, 2009.
86. Refinetti R, Menaker M. The circadian rhythm of body temperature. Physiol Behav 51: 613-637, 1992.
87. Reppert SM. Melatonin receptors: molecular biology of a new family of G protein-coupled receptors. J Biol Rhythms 12: 528-531, 1997.
88. Reppert SM, Weaver DR. Coordination of circadian timing in mammals. Nature 418: 935-941, 2002.
89. Romijn HJ, Sluiter AA, Pool CW, Wortel J, Buijs RM. Evidence from confocal fluorescence microscopy for a dense, reciprocal innervation between AVP-, somatostatin-, VIP/PHI-, GRP-, and VIP/PHI/GRP-immunoreactive neurons in the rat suprachiasmatic nucleus. Eur J Neurosci 9: 2613-2623, 1997.
90. Romo-Nava F, Alvarez-Icaza GD, Fresan-Orellana A, Saracco AR, Becerra-Palars C, Moreno J, Ontiveros Uribe MP, Berlanga C, Heinze G, Buijs RM. Melatonin attenuates antipsychotic metabolic effects: an eight-week randomized, doubleblind, parallel-group, placebo-controlled clinical trial. Bipolar Disord 16: 410-421, 2014.
91. Sabath E, Salgado-Delgado R, Guerrero-Vargas NN, Guzman-Ruiz MA, Del Carmen BM, Escobar C, Buijs RM. Food entrains clock genes but not metabolic genes in the liver of suprachiasmatic nucleus lesioned rats. FEBS Lett 588: 3104-3110, 2014.
92. Saderi N, Cazarez-Marquez F, Buijs FN, Salgado-Delgado RC, Guzman-Ruiz MA, Del Carmen BM, Escobar C, Buijs RM. The NPY intergeniculate leaflet projections to the suprachiasmatic nucleus transmit metabolic conditions. Neuroscience 246: 291-300, 2013.
93. Saeb-Parsy K, Dyball RE. Defined cell groups in the rat suprachiasmatic nucleus have different day/night rhythms of single-unit activity in vivo. J Biol Rhythms 18: 26-42, 2003.
94. Salgado-Delgado R, Angeles-Castellanos M, Saderi N, Buijs RM, Escobar C. Food intake during the normal activity phase prevents obesity and circadian desynchrony in a rat model of night work. Endocrinology 151: 1019-1029, 2010.
95. Salgado-Delgado RC, Saderi N, Basualdo MC, Guerrero-Vargas NN, Escobar C, Buijs RM. Shift work or food intake during the rest phase promotes metabolic disruption and desynchrony of liver genes in male rats. PLos One 8: e60052, 2013.
96. Schaap J, Meijer JH. Opposing effects of behavioural activity and light on neurons of the suprachiasmatic nucleus. Eur J Neurosci 13: 1955-1962, 2001.
97. Scheer FA, Michelson AD, Frelinger AL, III, Evoniuk H, Kelly EE, McCarthy M, Doamekpor LA, Barnard MR, Shea SA. The human endogenous circadian system causes greatest platelet activation during the biological morning independent of behaviors. PLos One 6: e24549, 2011.
98. Scheer FA, Pirovano C, van Someren EJ, Buijs RM. Environmental light and suprachiasmatic nucleus interact in the regulation of body temperature. Neuroscience 132: 465-477, 2005.
99. Scheer FA, van Montfrans GA, van Someren EJ, Mairuhu G, Buijs RM. Daily nighttime melatonin reduces blood pressure in male patients with essential hypertension. Hypertension 43: 192-197, 2004.
100. Shinohara K, Tominaga K, Isobe Y, Inouye ST. Photic regulation of peptides located in the ventrolateral subdivision of the suprachiasmatic nucleus of the rat: daily variations of vasoactive intestinal polypeptide, gastrin-releasing peptide, and neuropeptide Y. J Neurosci 13: 793-800, 1993.
101. Silver AC, Arjona A, Walker WE, Fikrig E. The circadian clock controls Toll-like receptor 9-mediated innate and adaptive immunity. Immunity 36: 251-261, 2012.
102. Slotten HA, Krekling S, Sicard B, Pevet P. Daily infusion of melatonin entrains circadian activity rhythms in the diurnal rodent Arvicanthis ansorgei. Behav Brain Res 133: 11-19, 2002.
103. Smarr BL, Morris E, de La Iglesia HO. The dorsomedial suprachiasmatic nucleus times circadian expression of Kiss1 and the luteinizing hormone surge. Endocrinology 153: 2839-2850, 2012.
104. Steylen PM, van der Heijden FM, Kok HD, Sijben NA, Verhoeven WM. Cardiometabolic comorbidity in antipsychotic treated patients: need for systematic evaluation and treatment. Int J Psychiatry Clin Pract 17: 125-130, 2013.
105. Su Y, Foppen E, Zhang Z, Fliers E, Kalsbeek A. Effects of 6-meals-a-day feeding and 6-meals-aday feeding combined with adrenalectomy on daily gene expression rhythms in rat epididymal white adipose tissue. Genes Cells 21: 6-24, 2016.
106. Sun Y, Shu J, Kyei K, Neal-Perry GS. Intracerebroventricular infusion of vasoactive intestinal Peptide rescues the luteinizing hormone surge in middle-aged female rats. Front Endocrinol (Lausanne) 3: 24, 2012.
107. 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 100: 6795-6800, 2003.
108. Tosini G, Menaker M. Circadian rhythms in cultured mammalian retina. Science 272: 419-421, 1996.
109. Van de Kar LD, Lorens SA. Differential serotonergic innervation of individual hypothalamic nuclei and other forebrain regions by the dorsal and median midbrain raphe nuclei. Brain Res 162: 45-54, 1979.
110. 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 immunocytochemical studies. J Comp Neurol 384: 569-579, 1997.
111. van Oosterhout F, Lucassen EA, Houben T, Vanderleest HT, Antle MC, Meijer JH. Amplitude of the SCN clock enhanced by the behavioral activity rhythm. PLos One 7: e39693, 2012.
112. Vancampfort D, De Hert M, Stubbs B, Ward PB, Rosenbaum S, Soundy A, Probst M. Negative symptoms are associated with lower autonomous motivation towards physical activity in people with schizophrenia. Compr Psychiatry 56: 128-132, 2015.
113. Viswambharan H, Carvas JM, Antic V, Marecic A, Jud C, Zaugg CE, Ming XF, Montani JP, Albrecht U, Yang Z. Mutation of the circadian clock gene Per2 alters vascular endothelial function. Circulation 115: 2188-2195, 2007.
114. Vreeburg SA, Hoogendijk WJ, DeRijk RH, van Dyck R, Smit JH, Zitman FG, Penninx BW. Salivary cortisol levels and the 2-year course of depressive and anxiety disorders. Psychoneuroendocrinology 38: 1494-1502, 2013.
115. Webb AB, Angelo N, Huettner JE, Herzog ED. Intrinsic, nondeterministic circadian rhythm generation in identified mammalian neurons. Proc Natl Acad Sci USA 106: 16493-16498, 2009.
116. Westgate EJ, Cheng Y, Reilly DF, Price TS, Walisser JA, Bradfield CA, FitzGerald GA. Genetic components of the circadian clock regulate thrombogenesis in vivo. Circulation 117: 2087-2095, 2008.
117. Wiater MF, Mukherjee S, Li AJ, Dinh TT, Rooney EM, Simasko SM, Ritter S. Circadian integration of sleep/wake and feeding requires NPY-receptor expressing neurons in the mediobasal hypothalamus. Am J Physiol Regul Integr Comp Physiol 301: R1569-R1581, 2011.
118. Wulff K, Gatti S, Wettstein JG, Foster RG. Sleep and circadian rhythm disruption in psychiatric and neurodegenerative disease. Nat Rev Neurosci 11: 589-599, 2010.
119. Yamaguchi Y, Suzuki T, Mizoro Y, Kori H, Okada K, Chen Y, Fustin JM, Yamazaki F, Mizuguchi N, Zhang J, Dong X, Tsujimoto G, Okuno Y, Doi M, Okamura H. Mice genetically deficient in vasopressin V1a and V1b receptors are resistant to jet lag. Science 342: 85-90, 2013.
120. Yamazaki S, Kerbeshian MC, Hocker CG, Block GD, Menaker M. Rhythmic properties of the hamster suprachiasmatic nucleus in vivo. J Neurosci 18: 10709-10723, 1998.
121. Yi CX, Challet E, Pevet P, Kalsbeek A, Escobar C, Buijs RM. A circulating ghrelin mimetic attenuates light-induced phase delay of mice and lightinduced Fos expression in the suprachiasmatic nucleus of rats. Eur J Neurosci 27: 1965-1972, 2008.
122. Yi CX, Foppen E, Abplanalp W, Gao Y, Alkemade A, La Fleur SE, Serlie MJ, Fliers E, Buijs RM, Tschop MH, Kalsbeek A. Glucocorticoid signaling in the arcuate nucleus modulates hepatic insulin sensitivity. Diabetes 61: 339-345, 2012.