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Circadian rhythms in leukocyte trafficking

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Abstract

A broad range of immunological processes oscillates over the course of a day. Recent findings have identified a molecular basis for the circadian clock in the regulation of the immune system. These rhythms manifest themselves in oscillatory behavior of immune cells and proinflammatory mediators, which causes a time-dependent sensitivity in the reaction to pathogens. This rhythmicity impacts disease manifestations and severity and provides an option for therapy that incorporates chronopharmacological considerations. This review will focus on the current knowledge and relevance of rhythmic immune cell trafficking. It will provide an overview of the molecular clock machinery and its interrelations with leukocyte migration and the immune response.

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References

  1. Panda S, Antoch MP, Miller BH, Su AI, Schook AB, Straume M, Schultz PG, Kay SA, Takahashi JS, Hogenesch JB (2002) Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 109:307–320

    PubMed  CAS  Google Scholar 

  2. Storch KF, Lipan O, Leykin I, Viswanathan N, Davis FC, Wong WH, Weitz CJ (2002) Extensive and divergent circadian gene expression in liver and heart. Nature 417:78–83

    PubMed  CAS  Google Scholar 

  3. Dibner C, Schibler U, Albrecht U (2010) The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu Rev Physiol 72:517–549

    PubMed  CAS  Google Scholar 

  4. Asher G, Schibler U (2011) Crosstalk between components of circadian and metabolic cycles in mammals. Cell Metab 13:125–137

    PubMed  CAS  Google Scholar 

  5. Bass J, Takahashi JS (2010) Circadian integration of metabolism and energetics. Science 330:1349–1354

    PubMed Central  PubMed  CAS  Google Scholar 

  6. Dunlap JC (1999) Molecular bases for circadian clocks. Cell 96:271–290

    PubMed  CAS  Google Scholar 

  7. Darlington TK, Wager-Smith K, Ceriani MF, Staknis D, Gekakis N, Steeves TD, Weitz CJ, Takahashi JS, Kay SA (1998) Closing the circadian loop: CLOCK-induced transcription of its own inhibitors per and tim. Science 280:1599–1603

    PubMed  CAS  Google Scholar 

  8. 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 U S A 95:5474–5479

    PubMed Central  PubMed  CAS  Google Scholar 

  9. Ueda HR, Hayashi S, Chen W, Sano M, Machida M, Shigeyoshi Y, Iino M, Hashimoto S (2005) System-level identification of transcriptional circuits underlying mammalian circadian clocks. Nat Genet 37:187–192

    PubMed  CAS  Google Scholar 

  10. Bunger MK, Wilsbacher LD, Moran SM, Clendenin C, Radcliffe LA, Hogenesch JB, Simon MC, Takahashi JS, Bradfield CA (2000) Mop3 is an essential component of the master circadian pacemaker in mammals. Cell 103:1009–1017

    PubMed Central  PubMed  CAS  Google Scholar 

  11. ** X, Shearman LP, Weaver DR, Zylka MJ, de Vries GJ, Reppert SM (1999) A molecular mechanism regulating rhythmic output from the suprachiasmatic circadian clock. Cell 96:57–68

    PubMed  CAS  Google Scholar 

  12. Griffin EA Jr, Staknis D, Weitz CJ (1999) Light-independent role of CRY1 and CRY2 in the mammalian circadian clock. Science 286:768–771

    PubMed  CAS  Google Scholar 

  13. Gekakis N, Staknis D, Nguyen HB, Davis FC, Wilsbacher LD, King DP, Takahashi JS, Weitz CJ (1998) Role of the CLOCK protein in the mammalian circadian mechanism. Science 280:1564–1569

    PubMed  CAS  Google Scholar 

  14. Preitner N, Damiola F, Lopez-Molina L, Zakany J, Duboule D, Albrecht U, Schibler U (2002) The orphan nuclear receptor REV-ERBalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell 110:251–260

    PubMed  CAS  Google Scholar 

  15. O’Neill JS, Reddy AB (2011) Circadian clocks in human red blood cells. Nature 469:498–503

    PubMed Central  PubMed  Google Scholar 

  16. O’Neill JS, van Ooijen G, Dixon LE, Troein C, Corellou F, Bouget FY, Reddy AB, Millar AJ (2011) Circadian rhythms persist without transcription in a eukaryote. Nature 469:554–558

    PubMed Central  PubMed  Google Scholar 

  17. Lucas RJ, Freedman MS, Munoz M, Garcia-Fernandez JM, Foster RG (1999) Regulation of the mammalian pineal by non-rod, non-cone, ocular photoreceptors. Science 284:505–507

    PubMed  CAS  Google Scholar 

  18. Ralph MR, Foster RG, Davis FC, Menaker M (1990) Transplanted suprachiasmatic nucleus determines circadian period. Science 247:975–978

    PubMed  CAS  Google Scholar 

  19. Silver R, LeSauter J, Tresco PA, Lehman MN (1996) A diffusible coupling signal from the transplanted suprachiasmatic nucleus controlling circadian locomotor rhythms. Nature 382:810–813

    PubMed  CAS  Google Scholar 

  20. Reppert SM, Weaver DR (2001) Molecular analysis of mammalian circadian rhythms. Annu Rev Physiol 63:647–676

    PubMed  CAS  Google Scholar 

  21. Brown SA, Zumbrunn G, Fleury-Olela F, Preitner N, Schibler U (2002) Rhythms of mammalian body temperature can sustain peripheral circadian clocks. Curr Biol 12:1574–1583

    PubMed  CAS  Google Scholar 

  22. Buijs RM, van Eden CG, Goncharuk VD, Kalsbeek A (2003) The biological clock tunes the organs of the body: timing by hormones and the autonomic nervous system. J Endocrinol 177:17–26

    PubMed  CAS  Google Scholar 

  23. Dickmeis T (2009) Glucocorticoids and the circadian clock. J Endocrinol 200:3–22

    PubMed  CAS  Google Scholar 

  24. Nader N, Chrousos GP, Kino T (2009) Circadian rhythm transcription factor CLOCK regulates the transcriptional activity of the glucocorticoid receptor by acetylating its hinge region lysine cluster: potential physiological implications. FASEB J 23:1572–1583

    PubMed Central  PubMed  CAS  Google Scholar 

  25. Elenkov IJ, Chrousos GP, Wilder RL (2000) Neuroendocrine regulation of IL-12 and TNF-alpha/IL-10 balance. Ann N Y Acad Sci 917:94–105

    PubMed  CAS  Google Scholar 

  26. Mukherji A, Kobiita A, Ye T, Chambon P (2013) Homeostasis in intestinal epithelium is orchestrated by the circadian clock and microbiota cues transduced by TLRs. Cell 153:812–827

    PubMed  CAS  Google Scholar 

  27. Scheiermann C, Kunisaki Y, Frenette PS (2013) Circadian control of the immune system. Nat Rev Immunol 13:190–198

    PubMed  CAS  Google Scholar 

  28. Arjona A, Silver AC, Walker WE, Fikrig E (2012) Immunity’s fourth dimension: approaching the circadian-immune connection. Trends Immunol 33:607–612

    PubMed Central  PubMed  CAS  Google Scholar 

  29. Kiel MJ, Morrison SJ (2008) Uncertainty in the niches that maintain haematopoietic stem cells. Nat Rev Immunol 8:290–301

    PubMed  CAS  Google Scholar 

  30. Kunisaki Y, Frenette PS (2012) The secrets of the bone marrow niche: enigmatic niche brings challenge for HSC expansion. Nat Med 18:864–865

    PubMed  CAS  Google Scholar 

  31. Nilsson SK, Dooner MS, Tiarks CY, Weier HU, Quesenberry PJ (1997) Potential and distribution of transplanted hematopoietic stem cells in a nonablated mouse model. Blood 89:4013–4020

    PubMed  CAS  Google Scholar 

  32. Zhang J, Niu C, Ye L, Huang H, He X, Tong WG, Ross J, Haug J, Johnson T, Feng JQ, Harris S, Wiedemann LM, Mishina Y, Li L (2003) Identification of the haematopoietic stem cell niche and control of the niche size. Nature 425:836–841

    PubMed  CAS  Google Scholar 

  33. Ding L, Saunders TL, Enikolopov G, Morrison SJ (2012) Endothelial and perivascular cells maintain haematopoietic stem cells. Nature 481:457–462

    PubMed Central  PubMed  CAS  Google Scholar 

  34. Sugiyama T, Kohara H, Noda M, Nagasawa T (2006) Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 25:977–988

    PubMed  CAS  Google Scholar 

  35. Mendez-Ferrer S, Michurina TV, Ferraro F, Mazloom AR, Macarthur BD, Lira SA, Scadden DT, Ma’ayan A, Enikolopov GN, Frenette PS (2010) Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 466:829–834

    PubMed Central  PubMed  CAS  Google Scholar 

  36. Yamazaki S, Ema H, Karlsson G, Yamaguchi T, Miyoshi H, Shioda S, Taketo MM, Karlsson S, Iwama A, Nakauchi H (2011) Nonmyelinating Schwann cells maintain hematopoietic stem cell hibernation in the bone marrow niche. Cell 147:1146–1158

    PubMed  CAS  Google Scholar 

  37. Katayama Y, Battista M, Kao WM, Hidalgo A, Peired AJ, Thomas SA, Frenette PS (2006) Signals from the sympathetic nervous system regulate hematopoietic stem cell egress from bone marrow. Cell 124:407–421

    PubMed  CAS  Google Scholar 

  38. Greenbaum A, Hsu YM, Day RB, Schuettpelz LG, Christopher MJ, Borgerding JN, Nagasawa T, Link DC (2013) CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance. Nature 495:227–230

    PubMed Central  PubMed  CAS  Google Scholar 

  39. Kunisaki Y, Bruns I, Scheiermann C, Ahmed J, Pinho S, Zhang D, Mizoguchi T, Wei Q, Lucas D, Ito K, Mar JC, Bergman A, Frenette PS (2013) Arteriolar niches maintain haematopoietic stem cell quiescence. Nature 502(7473):637–643

    PubMed  CAS  Google Scholar 

  40. Lucas D, Scheiermann C, Chow A, Kunisaki Y, Bruns I, Barrick C, Tessarollo L, Frenette PS (2013) Chemotherapy-induced bone marrow nerve injury impairs hematopoietic regeneration. Nat Med 19:695–703

    PubMed Central  PubMed  CAS  Google Scholar 

  41. Maestroni GJ, Cosentino M, Marino F, Togni M, Conti A, Lecchini S, Frigo G (1998) Neural and endogenous catecholamines in the bone marrow. Circadian association of norepinephrine with hematopoiesis? Exp Hematol 26:1172–1177

    PubMed  CAS  Google Scholar 

  42. Casanova-Acebes M, Pitaval C, Weiss LA, Nombela-Arrieta C, Chevre R, A-González N, Kunisaki Y, Zhang D, van Rooijen N, Silberstein LE, Weber C, Nagasawa T, Frenette PS, Castrillo A, Hidalgo A (2013) Rhythmic modulation of the hematopoietic niche through neutrophil clearance. Cell 153:1025–1035

    PubMed  CAS  Google Scholar 

  43. Mendez-Ferrer S, Chow A, Merad M, Frenette PS (2009) Circadian rhythms influence hematopoietic stem cells. Curr Opin Hematol 16:235–242

    PubMed  CAS  Google Scholar 

  44. Mendez-Ferrer S, Lucas D, Battista M, Frenette PS (2008) Haematopoietic stem cell release is regulated by circadian oscillations. Nature 452:442–447

    PubMed  CAS  Google Scholar 

  45. Aiuti A, Webb IJ, Bleul C, Springer T, Gutierrez-Ramos JC (1997) The chemokine SDF-1 is a chemoattractant for human CD34+ hematopoietic progenitor cells and provides a new mechanism to explain the mobilization of CD34+ progenitors to peripheral blood. J Exp Med 185:111–120

    PubMed Central  PubMed  CAS  Google Scholar 

  46. Hanoun M, Frenette PS (2013) This niche is a maze; an amazing niche. Cell Stem Cell 12:391–392

    PubMed Central  PubMed  CAS  Google Scholar 

  47. Lucas D, Battista M, Shi PA, Isola L, Frenette PS (2008) Mobilized hematopoietic stem cell yield depends on species-specific circadian timing. Cell Stem Cell 3:364–366

    PubMed  CAS  Google Scholar 

  48. Shi PA, Isola LM, Gabrilove JL, Moshier EL, Godbold JH, Miller LK, Frenette PS (2013) Prospective cohort study of the circadian rhythm pattern in allogeneic sibling donors undergoing standard granulocyte colony-stimulating factor mobilization. Stem Cell Res Ther 4:30

    PubMed Central  PubMed  CAS  Google Scholar 

  49. Dimitrov S, Benedict C, Heutling D, Westermann J, Born J, Lange T (2009) Cortisol and epinephrine control opposing circadian rhythms in T cell subsets. Blood 113:5134–5143

    PubMed Central  PubMed  CAS  Google Scholar 

  50. Scheiermann C, Kunisaki Y, Lucas D, Chow A, Jang JE, Zhang D, Hashimoto D, Merad M, Frenette PS (2012) Adrenergic nerves govern circadian leukocyte recruitment to tissues. Immunity 37:290–301

    PubMed Central  PubMed  CAS  Google Scholar 

  51. House SD, Ruch S, Koscienski WF 3rd, Rocholl CW, Moldow RL (1997) Effects of the circadian rhythm of corticosteroids on leukocyte-endothelium interactions in the AM and PM. Life Sci 60:2023–2034

    PubMed  CAS  Google Scholar 

  52. Arnold L, Henry A, Poron F, Baba-Amer Y, van Rooijen N, Plonquet A, Gherardi RK, Chazaud B (2007) Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J Exp Med 204:1057–1069

    PubMed Central  PubMed  CAS  Google Scholar 

  53. Serhan CN, Savill J (2005) Resolution of inflammation: the beginning programs the end. Nat Immunol 6:1191–1197

    PubMed  CAS  Google Scholar 

  54. Rankin SM (2010) The bone marrow: a site of neutrophil clearance. J Leukocyte Biol 88:241–251

    PubMed  CAS  Google Scholar 

  55. Martin C, Burdon PC, Bridger G, Gutierrez-Ramos JC, Williams TJ, Rankin SM (2003) Chemokines acting via CXCR2 and CXCR4 control the release of neutrophils from the bone marrow and their return following senescence. Immunity 19:583–593

    PubMed  CAS  Google Scholar 

  56. Chow A, Lucas D, Hidalgo A, Mendez-Ferrer S, Hashimoto D, Scheiermann C, Battista M, Leboeuf M, Prophete C, van Rooijen N, Tanaka M, Merad M, Frenette PS (2011) Bone marrow CD169+ macrophages promote the retention of hematopoietic stem and progenitor cells in the mesenchymal stem cell niche. J Exp Med 208:261–271

    PubMed Central  PubMed  CAS  Google Scholar 

  57. Christopher MJ, Rao M, Liu F, Woloszynek JR, Link DC (2011) Expression of the G-CSF receptor in monocytic cells is sufficient to mediate hematopoietic progenitor mobilization by G-CSF in mice. J Exp Med 208:251–260

    PubMed Central  PubMed  CAS  Google Scholar 

  58. Nguyen KD, Fentress SJ, Qiu Y, Yun K, Cox JS, Chawla A (2013) Circadian gene Bmal1 regulates diurnal oscillations of Ly6Chi inflammatory monocytes. Science; 341(6153):1483–1488

    PubMed  CAS  Google Scholar 

  59. Druzd D, Scheiermann C (2013) Immunology. Some monocytes got rhythm. Science 341:1462–1464

    PubMed  CAS  Google Scholar 

  60. Swirski F Monocyte trafficking in inflammation and cardiovascular disease.

  61. Sullivan DP, Muller WA (2013) Neutrophil and monocyte recruitment by PECAM, CD99, and other molecules via theLBRC. Semin Immunopathol. doi:10.1007/s00281-013-0412-6.

  62. Keller M, Mazuch J, Abraham U, Eom GD, Herzog ED, Volk HD, Kramer A, Maier B (2009) A circadian clock in macrophages controls inflammatory immune responses. Proc Natl Acad Sci U S A 106:21407–21412

    PubMed Central  PubMed  CAS  Google Scholar 

  63. Silver AC, Arjona A, Walker WE, Fikrig E (2012) The circadian clock controls toll-like receptor 9-mediated innate and adaptive immunity. Immunity 36:251–261

    PubMed Central  PubMed  CAS  Google Scholar 

  64. Arjona A, Sarkar DK (2006) The circadian gene mPer2 regulates the daily rhythm of IFN-gamma. J Interf Cytokine Res 26:645–649

    CAS  Google Scholar 

  65. Liu J, Malkani G, Shi X, Meyer M, Cunningham-Runddles S, Ma X, Sun ZS (2006) The circadian clock Period 2 gene regulates gamma interferon production of NK cells in host response to lipopolysaccharide-induced endotoxic shock. Infect Immun 74:4750–4756

    PubMed Central  PubMed  CAS  Google Scholar 

  66. Narasimamurthy R, Hatori M, Nayak SK, Liu F, Panda S, Verma IM (2012) Circadian clock protein cryptochrome regulates the expression of proinflammatory cytokines. Proc Natl Acad Sci U S A 109:12662–12667

    PubMed Central  PubMed  CAS  Google Scholar 

  67. Delerive P, Monte D, Dubois G, Trottein F, Fruchart-Najib J, Mariani J, Fruchart JC, Staels B (2001) The orphan nuclear receptor ROR alpha is a negative regulator of the inflammatory response. EMBO Rep 2:42–48

    PubMed Central  PubMed  CAS  Google Scholar 

  68. Logan RW, Sarkar DK (2012) Circadian nature of immune function. Mol Cell Endocrinol 349:82–90

    PubMed  CAS  Google Scholar 

  69. Gibbs JE, Blaikley J, Beesley S, Matthews L, Simpson KD, Boyce SH, Farrow SN, Else KJ, Singh D, Ray DW, Loudon AS (2012) The nuclear receptor REV-ERBalpha mediates circadian regulation of innate immunity through selective regulation of inflammatory cytokines. Proc Natl Acad Sci U S A 109:582–587

    PubMed Central  PubMed  CAS  Google Scholar 

  70. Lam MT, Cho H, Lesch HP, Gosselin D, Heinz S, Tanaka-Oishi Y, Benner C, Kaikkonen MU, Kim AS, Kosaka M, Lee CY, Watt A, Grossman TR, Rosenfeld MG, Evans RM, Glass CK (2013) Rev-Erbs repress macrophage gene expression by inhibiting enhancer-directed transcription. Nature 498:511–515

    PubMed  CAS  Google Scholar 

  71. Sun Y, Yang Z, Niu Z, Peng J, Li Q, **ong W, Langnas AN, Ma MY, Zhao Y (2006) MOP3, a component of the molecular clock, regulates the development of B cells. Immunology 119:451–460

    PubMed Central  PubMed  CAS  Google Scholar 

  72. Yu X, Rollins D, Ruhn KA, Stubblefield JJ, Green CB, Kashiwada M, Rothman PB, Takahashi JS, Hooper LV (2013) TH17 cell differentiation is regulated by the circadian clock. Science 342:727–730

    PubMed  CAS  Google Scholar 

  73. Cavadini G, Petrzilka S, Kohler P, Jud C, Tobler I, Birchler T, Fontana A (2007) TNF-alpha suppresses the expression of clock genes by interfering with E-box-mediated transcription. Proc Natl Acad Sci U S A 104:12843–12848

    PubMed Central  PubMed  CAS  Google Scholar 

  74. Young MR, Matthews JP, Kanabrocki EL, Sothern RB, Roitman-Johnson B, Scheving LE (1995) Circadian rhythmometry of serum interleukin-2, interleukin-10, tumor necrosis factor-alpha, and granulocyte-macrophage colony-stimulating factor in men. Chronobiol Int 12:19–27

    PubMed  CAS  Google Scholar 

  75. Cutolo M, Straub RH (2008) Circadian rhythms in arthritis: hormonal effects on the immune/inflammatory reaction. Autoimmun Rev 7:223–228

    PubMed  CAS  Google Scholar 

  76. Haus E, Sackett-Lundeen L, Smolensky MH (2012) Rheumatoid arthritis: circadian rhythms in disease activity, signs and symptoms, and rationale for chronotherapy with corticosteroids and other medications. Bull NYU Hosp Joint Dis 70(Suppl 1):3–10

    Google Scholar 

  77. Panzer SE, Dodge AM, Kelly EA, Jarjour NN (2003) Circadian variation of sputum inflammatory cells in mild asthma. J Allergy Clin Immunol 111:308–312

    PubMed  Google Scholar 

  78. Atkinson G, Jones H, Ainslie PN (2010) Circadian variation in the circulatory responses to exercise: relevance to the morning peaks in strokes and cardiac events. Eur J Appl Physiol 108:15–29

    PubMed Central  PubMed  Google Scholar 

  79. Marques FZ, Campain AE, Davern PJ, Yang YH, Head GA, Morris BJ (2011) Genes influencing circadian differences in blood pressure in hypertensive mice. PLoS ONE 6:e19203

    PubMed Central  PubMed  CAS  Google Scholar 

  80. Muller JE, Stone PH, Turi ZG, Rutherford JD, Czeisler CA, Parker C, Poole WK, Passamani E, Roberts R, Robertson T et al (1985) Circadian variation in the frequency of onset of acute myocardial infarction. N Engl J Med 313:1315–1322

    PubMed  CAS  Google Scholar 

  81. Tofler GH, Gebara OC, Mittleman MA, Taylor P, Siegel W, Venditti FJ Jr, Rasmussen CA, Muller JE (1995) Morning peak in ventricular tachyarrhythmias detected by time of implantable cardioverter/defibrillator therapy. The CPI Investigators. Circulation 92:1203–1208

    PubMed  CAS  Google Scholar 

  82. Suarez-Barrientos A, Lopez-Romero P, Vivas D, Castro-Ferreira F, Nunez-Gil I, Franco E, Ruiz-Mateos B, Garcia-Rubira JC, Fernandez-Ortiz A, Macaya C, Ibanez B (2011) Circadian variations of infarct size in acute myocardial infarction. Heart 97:970–976

    PubMed  Google Scholar 

  83. Mideo N, Reece SE, Smith AL, Metcalf CJ (2013) The Cinderella syndrome: why do malaria-infected cells burst at midnight? Trends Parasitol 29:10–16

    PubMed Central  PubMed  Google Scholar 

  84. Schernhammer ES, Kroenke CH, Laden F, Hankinson SE (2006) Night work and risk of breast cancer. Epidemiology (Cambridge, Mass) 17:108–111

    Google Scholar 

  85. Schernhammer ES, Laden F, Speizer FE, Willett WC, Hunter DJ, Kawachi I, Fuchs CS, Colditz GA (2003) Night-shift work and risk of colorectal cancer in the nurses’ health study. J Natl Cancer Inst 95:825–828

    PubMed  Google Scholar 

  86. Kubo T, Ozasa K, Mikami K, Wakai K, Fu**o Y, Watanabe Y, Miki T, Nakao M, Hayashi K, Suzuki K, Mori M, Washio M, Sakauchi F, Ito Y, Yoshimura T, Tamakoshi A (2006) Prospective cohort study of the risk of prostate cancer among rotating-shift workers: findings from the Japan Collaborative Cohort study. Am J Epidemiol 164:549–555

    PubMed  Google Scholar 

  87. Conlon M, Lightfoot N, Kreiger N (2007) Rotating shift work and risk of prostate cancer. Epidemiology 18:182–183

    PubMed  Google Scholar 

  88. Lahti TA, Partonen T, Kyyronen P, Kauppinen T, Pukkala E (2008) Night-time work predisposes to non-Hodgkin lymphoma. Int J Cancer 123:2148–2151

    PubMed  CAS  Google Scholar 

  89. Haupt CM, Alte D, Dorr M, Robinson DM, Felix SB, John U, Volzke H (2008) The relation of exposure to shift work with atherosclerosis and myocardial infarction in a general population. Atherosclerosis 201:205–211

    PubMed  CAS  Google Scholar 

  90. Tenkanen L, Sjoblom T, Harma M (1998) Joint effect of shift work and adverse life-style factors on the risk of coronary heart disease. Scand J Work Environ and Health 24:351–357

    CAS  Google Scholar 

  91. Logan RW, Zhang C, Murugan S, O’Connell S, Levitt D, Rosenwasser AM, Sarkar DK (2012) Chronic shift-lag alters the circadian clock of NK cells and promotes lung cancer growth in rats. J Immunol 188:2583–2591

    PubMed Central  PubMed  CAS  Google Scholar 

  92. Xu C, Li CY, Kong AN (2005) Induction of phase I, II and III drug metabolism/transport by xenobiotics. Arch Pharm Res 28:249–268

    PubMed  CAS  Google Scholar 

  93. Claudel T, Cretenet G, Saumet A, Gachon F (2007) Crosstalk between xenobiotics metabolism and circadian clock. FEBS Lett 581:3626–3633

    PubMed  CAS  Google Scholar 

  94. Ripperger JA, Shearman LP, Reppert SM, Schibler U (2000) CLOCK, an essential pacemaker component, controls expression of the circadian transcription factor DBP. Gen Dev 14:679–689

    CAS  Google Scholar 

  95. Ripperger JA, Schibler U (2006) Rhythmic CLOCK-BMAL1 binding to multiple E-box motifs drives circadian Dbp transcription and chromatin transitions. Nat Genet 38:369–374

    PubMed  CAS  Google Scholar 

  96. Gachon F, Olela FF, Schaad O, Descombes P, Schibler U (2006) The circadian PAR-domain basic leucine zipper transcription factors DBP, TEF, and HLF modulate basal and inducible xenobiotic detoxification. Cell Metab 4:25–36

    PubMed  CAS  Google Scholar 

  97. Murakami Y, Higashi Y, Matsunaga N, Koyanagi S, Ohdo S (2008) Circadian clock-controlled intestinal expression of the multidrug-resistance gene mdr1a in mice. Gastroenterology 135:1636–1644, e1633

    PubMed  CAS  Google Scholar 

  98. Mitsui S, Yamaguchi S, Matsuo T, Ishida Y, Okamura H (2001) Antagonistic role of E4BP4 and PAR proteins in the circadian oscillatory mechanism. Genes Dev 15:995–1006

    PubMed Central  PubMed  CAS  Google Scholar 

  99. Richardson VM, Santostefano MJ, Birnbaum LS (1998) Daily cycle of bHLH-PAS proteins, Ah receptor and Arnt, in multiple tissues of female Sprague–Dawley rats. Biochem Biophys Res Commun 252:225–231

    PubMed  CAS  Google Scholar 

  100. Ramadoss P, Marcus C, Perdew GH (2005) Role of the aryl hydrocarbon receptor in drug metabolism. Expert Opin Drug Metab Toxicol 1:9–21

    PubMed  CAS  Google Scholar 

  101. Balsalobre A, Brown SA, Marcacci L, Tronche F, Kellendonk C, Reichardt HM, Schutz G, Schibler U (2000) Resetting of circadian time in peripheral tissues by glucocorticoid signaling. Science 289:2344–2347

    PubMed  CAS  Google Scholar 

  102. Arjona A, Sarkar DK (2005) Circadian oscillations of clock genes, cytolytic factors, and cytokines in rat NK cells. J Immunol 174:7618–7624

    PubMed  CAS  Google Scholar 

  103. Vitaterna MH, King DP, Chang AM, Kornhauser JM, Lowrey PL, McDonald JD, Dove WF, Pinto LH, Turek FW, Takahashi JS (1994) Mutagenesis and map** of a mouse gene, Clock, essential for circadian behavior. Science 264:719–725

    PubMed Central  PubMed  CAS  Google Scholar 

  104. Spengler ML, Kuropatwinski KK, Comas M, Gasparian AV, Fedtsova N, Gleiberman AS, Gitlin II, Artemicheva NM, Deluca KA, Gudkov AV, Antoch MP (2012) Core circadian protein CLOCK is a positive regulator of NF-kappaB-mediated transcription. Proc Natl Acad Sci U S A 109:E2457–E2465

    PubMed Central  PubMed  CAS  Google Scholar 

  105. van der Horst GT, Muijtjens M, Kobayashi K, Takano R, Kanno S, Takao M, de Wit J, Verkerk A, Eker AP, van Leenen D, Buijs R, Bootsma D, Hoeijmakers JH, Yasui A (1999) Mammalian Cry1 and Cry2 are essential for maintenance of circadian rhythms. Nature 398:627–630

    PubMed  Google Scholar 

  106. Zheng B, Albrecht U, Kaasik K, Sage M, Lu W, Vaishnav S, Li Q, Sun ZS, Eichele G, Bradley A, Lee CC (2001) Nonredundant roles of the mPer1 and mPer2 genes in the mammalian circadian clock. Cell 105:683–694

    PubMed  CAS  Google Scholar 

  107. Logan RW, Wynne O, Levitt D, Price D, Sarkar DK (2013) Altered circadian expression of cytokines and cytolytic factors in splenic natural killer cells of Per1(−/−) mutant mice. J Interf Cytokine Res 33:108–114

    CAS  Google Scholar 

  108. Zheng B, Larkin DW, Albrecht U, Sun ZS, Sage M, Eichele G, Lee CC, Bradley A (1999) The mPer2 gene encodes a functional component of the mammalian circadian clock. Nature 400:169–173

    PubMed  CAS  Google Scholar 

  109. Cho H, Zhao X, Hatori M, Yu RT, Barish GD, Lam MT, Chong LW, DiTacchio L, Atkins AR, Glass CK, Liddle C, Auwerx J, Downes M, Panda S, Evans RM (2012) Regulation of circadian behaviour and metabolism by REV-ERB-alpha and REV-ERB-beta. Nature 485:123–127

    PubMed Central  PubMed  CAS  Google Scholar 

  110. Cutolo M (2012) Chronobiology and the treatment of rheumatoid arthritis. Curr Opin Rheumatol 24:312–318

    PubMed  CAS  Google Scholar 

  111. Reinberg A, Zagula-Mally Z, Ghata J, Halberg F (1969) Circadian reactivity rhythm of human skin to house dust, penicillin, and histamine. J Allergy 44:292–306

    PubMed  CAS  Google Scholar 

  112. Durrington HJ, Farrow SN, Loudon AS, Ray DW (2013) The circadian clock and asthma. Thorax. doi:10.1136/thoraxjnl-2013-203482

    Google Scholar 

  113. Auvil-Novak SE, Novak RD, el Sanadi N (1996) Twenty-four-hour pattern in emergency department presentation for sickle cell vaso-occlusive pain crisis. Chronobiol Int 13:449–456

    PubMed  CAS  Google Scholar 

  114. Mulcahy D, Keegan J, Cunningham D, Quyyumi A, Crean P, Park A, Wright C, Fox K (1988) Circadian variation of total ischaemic burden and its alteration with anti-anginal agents. Lancet 2:755–759

    PubMed  CAS  Google Scholar 

  115. Parker JD, Testa MA, Jimenez AH, Tofler GH, Muller JE, Parker JO, Stone PH (1994) Morning increase in ambulatory ischemia in patients with stable coronary artery disease. Importance of physical activity and increased cardiac demand. Circulation 89:604–614

    PubMed  CAS  Google Scholar 

  116. Manfredini R, Boari B, Smolensky MH, Salmi R, la Cecilia O, Maria Malagoni A, Haus E, Manfredini F (2005) Circadian variation in stroke onset: identical temporal pattern in ischemic and hemorrhagic events. Chronobiol Int 22:417–453

    PubMed  Google Scholar 

  117. Segawa K, Nakazawa S, Tsukamoto Y, Kurita Y, Goto H, Fukui A, Takano K (1987) Peptic ulcer is prevalent among shift workers. Dig Dis Sci 32:449–453

    PubMed  CAS  Google Scholar 

  118. Morikawa Y, Nakagawa H, Miura K, Soyama Y, Ishizaki M, Kido T, Naruse Y, Suwazono Y, Nogawa K (2005) Shift work and the risk of diabetes mellitus among Japanese male factory workers. Scand J Work Environ Health 31:179–183

    PubMed  Google Scholar 

  119. Pan A, Schernhammer ES, Sun Q, Hu FB (2011) Rotating night shift work and risk of type 2 diabetes: two prospective cohort studies in women. PLoS Med 8:e1001141

    PubMed Central  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the Deutsche Forschungsgemeinschaft (an Emmy-Noether grant to C.S. and a PhD fellowship (SFB 914 TP B09) to A. d. J.).

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Authors and Affiliations

  1. Walter-Brendel-Center of Experimental Medicine, Ludwig-Maximilians-Universität München, Marchioninistraße 27, 81377, Munich, Germany

    David Druzd, Alba de Juan & Christoph Scheiermann

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  1. David Druzd
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  2. Alba de Juan
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  3. Christoph Scheiermann
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Correspondence to Christoph Scheiermann.

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This article is a contribution to the special issue on New paradigms in leukocyte trafficking, lessons for therapeutics - Guest Editors: F. W. Luscinskas and B. A. Imhof

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Druzd, D., de Juan, A. & Scheiermann, C. Circadian rhythms in leukocyte trafficking. Semin Immunopathol 36, 149–162 (2014). https://doi.org/10.1007/s00281-013-0414-4

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