Chrono-immunology: Progress and challenges in understanding links between the circadian and immune systems

Immunology

Volumn 146, Issue 3, 2015, Pages 349-358

  Geiger, Sarah S ^a   Fagundes, Caio T ^b   Siegel, Richard M ^a  

^a NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

^b FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

Author keywords

Circadian; Cytokines; Immunity; Metabolism; Sleep

Indexed keywords

ARTICLE; CELL MIGRATION; CIRCADIAN RHYTHM; CYTOKINE PRODUCTION; CYTOTOXICITY; HUMAN; IMMUNE SYSTEM; IMMUNITY; IMMUNOCOMPETENT CELL; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; INFLAMMATORY DISEASE; NONHUMAN; NUTRITION; OSCILLATION; PRIORITY JOURNAL; RISK; SLEEP; ANIMAL; BIOLOGICAL MODEL; BIOSYNTHESIS; GENETICS; MAMMAL; PHYSIOLOGY;

CYTOKINE; TRANSCRIPTION FACTOR ARNTL;

ANIMALS; ARNTL TRANSCRIPTION FACTORS; CIRCADIAN CLOCKS; CIRCADIAN RHYTHM; CYTOKINES; HUMANS; IMMUNE SYSTEM; IMMUNOLOGIC MEMORY; MAMMALS; MODELS, IMMUNOLOGICAL; NUTRITIONAL PHYSIOLOGICAL PHENOMENA; SLEEP;

EID: 84943620007     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/imm.12525     Document Type: Article

References (84)

1. Aschoff J. Die 24-Stunden-Periodik der Maus unter konstanten Umgebungsbedingungen. Naturwissenschaften 1951; 38:506-7.
2. Aschoff J. Exogenous and endogenous components in circadian rhythms. Cold Spring Harb Symp Quant Biol 1960; 25:11-28.
3. Brown SA, Zumbrunn G, Fleury-Olela F, Preitner N. Rhythms of mammalian body temperature can sustain peripheral circadian clocks. Curr Biol 2002; 12:1574-83.
4. Mistlberger RE, Marchant EG. Computational and entrainment models of circadian food-anticipatory activity: evidence from non-24-hr feeding schedules. Behav Neurosci 1995; 109:790-8.
5. Edmonds SC, Adler NT. Food and light as entrainers of circadian running activity in the rat. Physiol Behav 1977; 18:915-9.
6. Aschoff J, Fatranska M, Giedke H, Doerr P, Stamm D, Wisser H. Human circadian rhythms in continuous darkness: entrainment by social cues. Science 1971; 171:213-5.
7. Whitmore D, Foulkes NS, Sassone-Corsi P. Light acts directly on organs and cells in culture to set the vertebrate circadian clock. Nature 2000; 404:87-91.
8. Menaker M. Extraretinal light perception in the sparrow. I. Entrainment of the biological clock. Proc Natl Acad Sci USA 1968; 59:414-21.
9. Moore RY, Eichler VB. Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat. Brain Res 1972; 42:201-6.
10. Stephan FK, Zucker I. Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proc Natl Acad Sci USA 1972; 69:1583-6.
11. Husse J, Leliavski A, Tsang AH, Oster H, Eichele G. The light-dark cycle controls peripheral rhythmicity in mice with a genetically ablated suprachiasmatic nucleus clock. FASEB J 2014; 28:4950-60.
12. Keller M, Mazuch J, Abraham U, Eom GD, Herzog ED, Volk H-DD et al. A circadian clock in macrophages controls inflammatory immune responses. Proc Natl Acad Sci USA 2009; 106:21407-12.
13. Gekakis N, Staknis D, Nguyen HB, Davis FC, Wilsbacher LD, King DP et al. Role of the CLOCK protein in the mammalian circadian mechanism. Science 1998; 280:1564-9.
14. Hao H, Allen DL, Hardin PE. A circadian enhancer mediates PER-dependent mRNA cycling in Drosophila melanogaster. Mol Cell Biol 1997; 17:3687-93.
15. Ripperger JA, Schibler U. Rhythmic CLOCK-BMAL1 binding to multiple E-box motifs drives circadian Dbp transcription and chromatin transitions. Nat Genet 2006; 38:369-74.
16. Harding HP, Lazar MA. The orphan receptor Rev-ErbA α activates transcription via a novel response element. Mol Cell Biol 1993; 13:3113-21.
17. Giguere V, Tini M, Flock G, Ong E, Evans RM, Otulakowski G. Isoform-specific amino-terminal domains dictate DNA-binding properties of RORα, a novel family of orphan hormone nuclear receptors. Genes Dev 1994; 8:538-53.
18. Keesler GA, Camacho F, Guo Y, Virshup D. Phosphorylation and destabilization of human period I clock protein by human casein kinase Iε. NeuroReport 2000; 11:951-5.
19. Camacho F, Cilio M, Guo Y, Virshup DM, Patel K, Khorkova O et al. Human casein kinase Iδ phosphorylation of human circadian clock proteins period 1 and 2. FEBS Lett 2001; 489:159-65.
20. Ukai-Tadenuma M, Kasukawa T, Ueda HR. Proof-by-synthesis of the transcriptional logic of mammalian circadian clocks. Nat Cell Biol 2008; 10:1154-63.
21. Ueda HR, Hayashi S, Chen W, Sano M, Machida M. System-level identification of transcriptional circuits underlying mammalian circadian clocks. Nat Genet 2005; 37:187-92.
22. Krueger JM. Somnogenic activity of immune response modifiers. Trends Pharmacol Sci 1990; 11:122-6.
23. Späth-Schwalbe E, Hansen K, Schmidt F, Schrezenmeier H, Marshall L, Burger K et al. Acute effects of recombinant human interleukin-6 on endocrine and central nervous sleep functions in healthy men. J Clin Endocrinol Metab 1998; 83:1573-9.
24. Imeri L, Opp MR. How (and why) the immune system makes us sleep. Nat Rev Neurosci 2009; 10:199-210.
25. Toth LA, Krueger JM. Alteration of sleep in rabbits by Staphylococcus aureus infection. Infect Immun 1988; 56:1785-91.
26. Bryant PA, Trinder J, Curtis N. Sick and tired: does sleep have a vital role in the immune system? Nat Rev Immunol 2004; 4:457-67.
27. Krueger JM, Obál F, Fang J, Kubota T. The role of cytokines in physiological sleep regulation. Ann N Y Acad Sci 2001; 933:211-21.
28. Young MRI, Matthews JP. Circadian rhythmometry of serum interleukin-2, interleukin-10, tumor necrosis factor-α, and granulocyte-macrophage colony-stimulating factor in men. Chronobiol Int 1995; 12:19-27.
29. Fang J, Wang Y, Krueger JM. Effects of interleukin-1β on sleep are mediated by the type I receptor. Am J Physiol 1998; 274(3 Pt 2):R655-60.
30. Fang J, Wang Y, Krueger JM. Mice lacking the TNF 55 kDa receptor fail to sleep more after TNFα treatment. J Neurosci 1997; 17:5949-55.
31. Born J, Lange T, Hansen K, Mölle M, Fehm HL. Effects of sleep and circadian rhythm on human circulating immune cells. J Immunol 1997; 158:4454-64.
32. Dimitrov S, Lange T, Benedict C, Nowell MA, Jones SA. Sleep enhances IL-6 trans-signaling in humans. FASEB J 2006; 20:2174-6.
33. Born J, Rasch B, Gais S. Sleep to remember. Neuroscientist 2006; 12:410-24.
34. Lange T, Perras B, Fehm HL, Born J. Sleep enhances the human antibody response to hepatitis A vaccination. Psychosom Med 2003; 65:831-5.
35. Brown R, Pang G, Husband AJ, King MG. Suppression of immunity to influenza virus infection in the respiratory tract following sleep disturbance. Reg Immunol 1989; 2:321-5.
36. Dimitrov S, Benedict C, Heutling D, Westermann J, Born J, Lange T. Cortisol and epinephrine control opposing circadian rhythms in T cell subsets. Blood 2009; 113:5134-43.
37. Arjona A, Sarkar DK. Circadian oscillations of clock genes, cytolytic factors, and cytokines in rat NK cells. J Immunol 2005; 174:7618-24.
38. Halberg F, Johnson E, Brown B, Bittner J. Susceptibility rhythm to E. coli endotoxin and bioassay. Exp Biol Med 1960; 103:142-4.
39. Kowanko IC, Knapp MS, Pownall R. Domiciliary self-measurement in the rheumatoid arthritis and the demonstration of circadian rhythmicity. Ann Rheum Dis 1982; 41:453-5.
40. Scott JT. Morning stiffness in rheumatoid arthritis. Ann Rheum Dis 1960; 19:361-8.
41. Trousseau A. Clinique medicale de L'Hotel dieu Paris, Vol. 2. Paris: Bailliere, 1865:373.
42. Reinberg A, Gervais P, Levi F, Smolensky M, Del Cerro L, Ugolini C. Circadian and circannual rhythms of allergic rhinitis: an epidemiologic study involving chronobiologic methods. J Allergy Clin Immunol 1988; 81:51-62.
43. Clarke LL, Jessop DS, Hunt LP, Straub RH, Perry MG, Kirwan JR. Alleviation of morning joint stiffness by low-dose prednisone in rheumatoid arthritis is associated with circadian changes in IL-6 and cortisol. Int J Clin Rheumatol 2011; 6:241-9.
44. Petrovsky N, McNair P, Harrison LC. Diurnal rhythms of pro-inflammatory cytokines: regulation by plasma cortisol and therapeutic implications. Cytokine 1998; 10:307-12.
45. Alamili M, Bendtzen K, Lykkesfeldt J, Rosenberg J, Gogenur I. Pronounced inflammatory response to endotoxaemia during nighttime: a randomised cross-over trial. PLoS ONE 2014; 9:e87413.
46. Hrushesky WJ, Langevin T, Kim Y, Wood PA. Circadian dynamics of tumor necrosis factor α (cachectin) lethality. J Exp Med 1994; 180:1059-65.
47. Marpegan L, Leone MJ, Katz ME, Sobrero PM, Bekinstein TA, Golombek DA. Diurnal variation in endotoxin-induced mortality in mice: correlation with proinflammatory factors. Chronobiol Int 2009; 26:1430-42.
48. Nguyen KD, Fentress SJ, Qiu Y, Yun K, Cox JS, Chawla A. Circadian gene Bmal1 regulates diurnal oscillations of Ly6Chi inflammatory monocytes. Science 2013; 341:1483-8.
49. Carrillo-Vico A, Lardone PJ. Melatonin: buffering the immune system. Int J Mol Sci 2013; 14:8636-83.
50. Hayashi M, Shimba S, Tezuka M. Characterization of the molecular clock in mouse peritoneal macrophages. Biol Pharm Bull 2007; 30:621-6.
51. Lee JH, Sancar A. Regulation of apoptosis by the circadian clock through NF-κB signaling. Proc Natl Acad Sci USA 2011; 108:12036-41.
52. Petrzilka S, Taraborrelli C, Cavadini G. Clock gene modulation by TNF-α depends on calcium and p38 MAP kinase signaling. J Biol Rhythms 2009; 24:283-94.
53. Spengler ML, Kuropatwinski KK. Core circadian protein CLOCK is a positive regulator of NF-κB-mediated transcription. Proc Natl Acad Sci USA 2012; 109:E2457-65.
54. Gibbs JE, Blaikley J, Beesley S, Matthews L, Simpson KD, Boyce SH et al. The nuclear receptor REV-ERBα mediates circadian regulation of innate immunity through selective regulation of inflammatory cytokines. Proc Natl Acad Sci USA 2012; 109:582-7.
55. Hoffman AE, Zheng T, Stevens RG, Ba Y, Zhang Y. Clock-cancer connection in non-Hodgkin's lymphoma: a genetic association study and pathway analysis of the circadian gene cryptochrome 2. Cancer Res 2009; 69:3605-13.
56. Adams KL, Castanon-Cervantes O, Evans JA, Davidson AJ. Environmental circadian disruption elevates the IL-6 response to lipopolysaccharide in blood. J Biol Rhythms 2013; 28:272-7.
57. Feigin RD, Middelkamp JN, Reed C. Circadian rhythmicity in susceptibility of mice to sublethal coxsackie B3 infection. Nature 1972; 240:57-8.
58. Silver AC, Arjona A, Walker WE, Fikrig E. The circadian clock controls toll-like receptor 9-mediated innate and adaptive immunity. Immunity 2012; 36:251-61.
59. Bellet MM, Deriu E, Liu JZ, Grimaldi B, Blaschitz C, Zeller M et al. Circadian clock regulates the host response to Salmonella. Proc Natl Acad Sci USA 2013; 110:9897-902.
60. Fortier EE, Rooney J, Dardente H. Circadian variation of the response of T cells to antigen. J Immunol 2011; 187:6291-300.
61. Lange T, Dimitrov S, Born J. Effects of sleep and circadian rhythm on the human immune system. Ann N Y Acad Sci 2010; 1193:48-59.
62. Abo T, Kawate T, Itoh K, Kumagai K. Studies on the bioperiodicity of the immune response. I. Circadian rhythms of human T, B, and K cell traffic in the peripheral blood. J Immunol 1981; 126:1360-3.
63. Pelegrí C, Vilaplana J, Castellote C. Circadian rhythms in surface molecules of rat blood lymphocytes. Am J Physiol Cell Physiol 2003; 284:C67-76.
64. Dodt C, Breckling U, Derad I, Fehm HL, Born J. Plasma epinephrine and norepinephrine concentrations of healthy humans associated with nighttime sleep and morning arousal. Hypertension 1997; 30(1 Pt 1):71-6.
65. Nichols CT, Tyler FH. Diurnal variation in adrenal cortical function. Annu Rev Med 1967; 18:313-24.
66. Scheiermann C, Kunisaki Y, Lucas D, Chow A, Jang J-EE, Zhang D et al. Adrenergic nerves govern circadian leukocyte recruitment to tissues. Immunity 2012; 37:290-301.
67. Kronfol Z, Nair M, Zhang Q, Hill EE, Brown MB. Circadian immune measures in healthy volunteers: relationship to hypothalamic-pituitary-adrenal axis hormones and sympathetic neurotransmitters. Psychosom Med 1997; 59:42-50.
68. Druzd D, de Juan A, Scheiermann C. Circadian rhythms in leukocyte trafficking. Semin Immunopathol 2014; 36:149-62.
69. Warburg O. On the origin of cancer cells. Science 1956; 123:309-14.
70. Krawczyk CM, Holowka T, Sun J, Blagih J, Amiel E, DeBerardinis RJ et al. Toll-like receptor-induced changes in glycolytic metabolism regulate dendritic cell activation. Blood 2010; 115:4742-9.
71. Hatori M, Vollmers C, Zarrinpar A, DiTacchio L. Time-restricted feeding without reducing caloric intake prevents metabolic diseases in mice fed a high-fat diet. Cell Metab 2012; 15:848-60.
72. Paschos GK, Ibrahim S, Song WL, Kunieda T. Obesity in mice with adipocyte-specific deletion of clock component Arntl. Nat Med 2012; 18:1768-77.
73. Kohsaka A, Laposky AD, Ramsey K, Estrada C, Joshu C, Kobayashi Y et al. High-fat diet disrupts behavioral and molecular circadian rhythms in mice. Cell Metab 2007; 6:414-21.
74. Patton DF, Katsuyama ÂM, Pavlovski I, Michalik M, Patterson Z, Parfyonov M et al. Circadian mechanisms of food anticipatory rhythms in rats fed once or twice daily: clock gene and endocrine correlates. PLoS ONE 2014; 9:e112451.
75. Pendergast JS, Nakamura W, Friday RC, Hatanaka F, Takumi T, Yamazaki S. Robust food anticipatory activity in BMAL1-deficient mice. PLoS ONE 2009; 4:e4860.
76. 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; 14:2950-61.
77. Stokkan KA, Yamazaki S, Tei H, Sakaki Y, Menaker M. Entrainment of the circadian clock in the liver by feeding. Science 2001; 291:490-3.
78. Hara R, Wan K, Wakamatsu H, Aida R, Moriya T, Akiyama M et al. Restricted feeding entrains liver clock without participation of the suprachiasmatic nucleus. Genes Cells 2001; 6:269-78.
79. Mohren DCL, Jansen NWH, Kant IJ. Prevalence of common infections among employees in different work schedules. J Occup Environ Med 2002; 44:1003-11.
80. Karlsson B, Knutsson A, Lindahl B. 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 2001; 58:747-52.
81. Pan A, Schernhammer ES, Sun Q, Hu FB. Rotating night shift work and risk of type 2 diabetes: two prospective cohort studies in women. PLoS Med 2011; 8:e1001141.
82. Danilenko KV, Cajochen C, Wirz-Justice A. Is sleep per se a zeitgeber in humans? J Biol Rhythms 2003; 18:170-8.
83. Hemmers S, Rudensky AY. The cell-intrinsic circadian clock is dispensable for lymphocyte differentiation and function. Cell Rep 2015; 11:1339-49.
84. Ieyasu A, Tajima Y, Shimba S. Clock gene Bmal1 is dispensable for intrinsic properties of murine hematopoietic stem cells. J Negat Results Biomed 2014; 13:4.