DOI QR코드

DOI QR Code

Cell Autonomous Circadian Systems and Their Relation to Inflammation

  • Annamneedi, Venkata Prakash (Convergence Research Center, Department of Pharmacy and Institute of Chronic Disease, Sahmyook University) ;
  • Park, Jun Woo (Convergence Research Center, Department of Pharmacy and Institute of Chronic Disease, Sahmyook University) ;
  • Lee, Geum Seon (Department of Counseling and Psychology, Sahmyook University) ;
  • Kang, Tae Jin (Convergence Research Center, Department of Pharmacy and Institute of Chronic Disease, Sahmyook University)
  • 투고 : 2020.11.29
  • 심사 : 2020.12.07
  • 발행 : 2021.01.01

초록

All living beings on earth have an important mechanism of 24-h periodicity, which controls their physiology, metabolism, and behavior. In humans, 24-h periodicity is regulated by the superchiasmatic nucleus (SCN) through external and environmental cues. Peripheral organs demonstrate circadian rhythms and circadian clock functions, and these are also observed in cultured cell lines. Every cell contains a CLOCK: BMAL1 loop for the generation of circadian rhythms. In this review, we focused on cell autonomous circadian rhythms in immune cells, the inflammatory diseases caused by disruption of circadian rhythms in hormones, and the role of clock genes in inflammatory diseases.

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참고문헌

  1. Arjona, A. and Sarkar, D. K. (2005) Circadian oscillations of clock genes, cytolytic factors, and cytokines in rat NK cells. J. Immunol. 174, 7618-7624. https://doi.org/10.4049/jimmunol.174.12.7618
  2. Arjona, A. and Sarkar, D. K. (2006) The circadian gene mPer2 regulates the daily rhythm of IFN-gamma. J. Interferon Cytokine Res. 26, 645-649. https://doi.org/10.1089/jir.2006.26.645
  3. Balsalobre, A., Brown, S. A., Marcacci, L., Tronche, F., Kellendonk, C., Reichardt, H. M., Schutz, G. and Schibler, U. (2000) Resetting of circadian time in peripheral tissues by glucocorticoid signaling. Science 289, 2344-2347. https://doi.org/10.1126/science.289.5488.2344
  4. Bang, J., Chang, H. W., Jung, H. R., Cho, C., Hur, J., Lee, S., Choi, T. H., Kim, S. and Ha, E. (2012) Melatonin attenuates clock gene Cryptochrome1, which may aggravate mouse anti-type II collagen antibody-induced arthritis. Rheumatol. Int. 32, 379-385. https://doi.org/10.1007/s00296-010-1641-9
  5. Barnes, P. J., Adcock, I., Spedding, M. and Vanhoutte, P. M. (1993) Anti-inflammatory actions of steroids: molecular mechanisms. Trends Pharmacol. Sci. 14, 436-441. https://doi.org/10.1016/0165-6147(93)90184-L
  6. Bergeron, C., Al-Ramli, W. and Hamid, Q. (2009) Remodeling in asthma. Proc. Am. Thorac. Soc. 6, 301-305. https://doi.org/10.1513/pats.200808-089RM
  7. Borish, L., King, M. S., Mascali, J. J., Johnson, S., Coll, B. and Rosenwasser, L. J. (1992) Transthyretin is an inhibitor of monocyte and endothelial cellinterleukin-1 production. Inflammation 16, 471-484. https://doi.org/10.1007/BF00918973
  8. Bourdoulous, S., Bensaid, A., Martinez, D., Sheikboudou, C., Trap, I., Strosberg, A. D. and Couraud, P. O. (1995) Infection of bovine brain microvessel endothelial cells with Cowdria ruminantium elicits IL-1 beta, -6, and -8 mRNA production and expression of an unusual MHC class II DQ alpha transcript. J. Immunol. 154, 4032-4038.
  9. Brown, S. A., Zumbrunn, G., Fleury-Olela, F., Preitner, N. and Schibler, U. (2002) Rhythms of mammalian body temperature can sustain peripheral circadian clocks. Curr. Biol. 12, 1574-1583. https://doi.org/10.1016/S0960-9822(02)01145-4
  10. Bunger, M. K., Wilsbacher, L. D., Moran, S. M., Clendenin, C., Radcliffe, L. A., Hogenesch, J. B., Simon, M. C., Takahashi, J. S. and Bradfield, C. A. (2000) Mop3 is an essential component of the master circadian pacemaker in mammals. Cell 103, 1009-1017. https://doi.org/10.1016/S0092-8674(00)00205-1
  11. Cermakian, N., Westfall, S. and Kiessling, S. (2014) Circadian clocks and inflammation: reciprocal regulation and shared mediators. Arch. Immunol. Ther. Exp. 62, 303-318. https://doi.org/10.1007/s00005-014-0286-x
  12. Chang, Y., Chou, Y., Lee, J., Lee, P., Dai, Y., Sun, C., Lin, Y., Wang, L., Yu, H., Yang, Y., Chen, C., Wan, K. and Chiang, B. (2014) Atopic dermatitis, melatonin, and sleep disturbance. Pediatrics 134, e397-e405. https://doi.org/10.1542/peds.2014-0376
  13. Chang, Y., Lin, M., Lee, J., Lee, P., Dai, Y, Chu, K., Sun, C., Lin, Y., Wang, L., Yu, H., Yang , Y., Chen, C., Wan, K. and Chiang, B. (2016) Melatonin supplementation for children with atopic dermatitis and sleep disturbance: a randomized clinical trial. JAMA Pediatr. 170, 35-42. https://doi.org/10.1001/jamapediatrics.2015.3092
  14. Cheon, S., Park, N., Cho, S. and Kim, K. (2013) Glucocorticoid-mediated Period2 induction delays the phase of circadian rhythm. Nucleic Acids Res. 41, 6161-6174. https://doi.org/10.1093/nar/gkt307
  15. Clark, T. J. (1987) Diurnal rhythm of asthma. Chest 91, 137S-141S. https://doi.org/10.1378/chest.91.6_supplement.137s
  16. Coogan, A. N. and Wyse, C. A. (2008) Neuroimmunology of the circadian clock. Brain Res. 1232, 104-112. https://doi.org/10.1016/j.brainres.2008.07.087
  17. Curtis, A. M., Bellet, M. M., Sassone-Corsi, P. and O'Neill, L. A. (2014) Circadian clock proteins and immunity. Immunity 40, 178-186. https://doi.org/10.1016/j.immuni.2014.02.002
  18. Cutolo, M., Maestroni, G. J., Otsa, K., Villaggio, B., Capellino, S., Montagna, P., Fazzuoli, L., Veldi, T., Peets, T., Hertens, E. and Sulli, A. (2005) Circadian melatonin and cortisol levels in rheumatoid arthritis patients in winter time: a north and south Europe comparison. Ann. Rheum. Dis. 64, 212-216. https://doi.org/10.1136/ard.2004.023416
  19. Cutolo, M. and Maestroni, G. J. (2005) The melatonin-cytokine connection in rheumatoid arthritis. Ann. Rheum. Dis. 64, 1109-1111. https://doi.org/10.1136/ard.2005.038588
  20. del Gobbo, V., Libri, V., Villani, N., Calio, R. and Nistico, G. (1989) Pinealectomy inhibits interleukin-2 production and natural killer activity in mice. Int. J. Immunopharmacol. 11, 567-573. https://doi.org/10.1016/0192-0561(89)90187-2
  21. Delagrange, P. and Guardiola-Lemaitre, B. (1997) Melatonin, its receptors, and relationships with biological rhythm disorders. Clin. Neuropharmacol. 20, 482-510. https://doi.org/10.1097/00002826-199712000-00002
  22. Dimitrov, S., Lange, T., Nohroudi, K. and Born, J. (2007) Number and function of circulating human antigen presenting cells regulated by sleep. Sleep 30, 401-411. https://doi.org/10.1093/sleep/30.4.401
  23. Drazen, D. L., Bilu, D., Bilbo, S. D. and Nelson, R. J. (2001) Melatonin enhancement of splenocyte proliferation is attenuated by luzindole, a melatonin receptor antagonist. Am. J. Physiol. Regul. Integr. Comp. Physiol. 280, R1476-R1482. https://doi.org/10.1152/ajpregu.2001.280.5.R1476
  24. Duguay, D. and Cermakian, N. (2009) The crosstalk between physiology and circadian clock proteins. Chronobiol. Int. 26, 1479-1513. https://doi.org/10.3109/07420520903497575
  25. Durrington, H. J., Farrow, S. N., Loudon, A. S. and Ray, D. W. (2014) The circadian clock and asthma. Thorax 69, 90-92. https://doi.org/10.1136/thoraxjnl-2013-203482
  26. Ehlers, A., Xie, W., Agapov, E., Brown, S., Steinberg, D., Tidwell R., Sajol, G., Schutz, R., Weaver, R., Yu, H., Castro, M., Bacharier, L. B., Wang, X., Holtzman, M. J. and Haspel, J. A. (2018) BMAL1 links the circadian clock to viral airway pathology and asthma phenotypes. Mucosal Immunol. 11, 97-111. https://doi.org/10.1038/mi.2017.24
  27. Esquifino, A. I., Selgas, L., Arce, A., Maggiore, V. D. and Cardinali, D. P. (1996) Twenty-four-hour rhythms in immune responses in rat submaxillary lymph nodes and spleen: effect of cyclosporine. Brain Behav. Immun. 10, 92-102. https://doi.org/10.1006/brbi.1996.0010
  28. Fabry, Z., Fitzsimmons, K. M., Herlein, J. A., Moninger, T. O., Dobbs, M. B. and Hart, M. N. (1993) Production of the cytokines interleukin 1 and 6 by murine brain microvessel endothelium and smooth muscle pericytes. J. Neuroimmunol. 47, 23-34. https://doi.org/10.1016/0165-5728(93)90281-3
  29. Fernandes, G., Halberg, F., Yunis, E. J. and Good, R. A. (1976) Circadian rhythmic plaque-forming cell response of spleens from mice immunized with Srbc. J. Immunol. 117, 962-966.
  30. Fukuoka, Y., Burioka N., Takata, M., Ohso, S., Miyata, M., Endo, M. and Shimizu, E. (2005) Glucocorticoid administration increases hPer1 mRNA levels in human peripheral blood mononuclear cells in vitro or in vivo. J. Biol. Rhythms 20, 550-553. https://doi.org/10.1177/0748730405279866
  31. Gibbs, J. E., Beesley, S., Plumb, J., Singh, D., Farrow, S., Ray, D. W. and Loudon, A. S. I. (2009) Circadian timing in the lung; a specific role for bronchiolar epithelial cells. Endocrinology 150, 268-276. https://doi.org/10.1210/en.2008-0638
  32. Gibbs, J., Ince, L., Matthews, L., Mei, J., Bell, T., Yang, N., Saer, B., Begley, N., Poolman, T., Pariollaud, M., Farrow, S., Francesco, D., Hussel, T., Worthen, G. S., Ray, D. and Loudon, A. (2014) An epithelial circadian clock controls pulmonary inflammation and glucocorticoid action. Nat. Med. 20, 919-926. https://doi.org/10.1038/nm.3599
  33. Gibbs, J. E., Blaikley, J., Beesley, S., Matthews, L., Simpson, K. D., Boyce, S. H., Farrow, S. N., Else, K. J., Singh, D., Ray, D. W. and Loudon, A. S. I. (2012) The nuclear receptor REV-ERBα mediates circadian regulation of innate immunity through selective regulation of inflammatory cytokines. Proc. Natl. Acad. Sci. U.S.A. 109, 582-587. https://doi.org/10.1073/pnas.1106750109
  34. Guo, H., Brewer, J. M., Lehman, M. N. and Bittman, E. L. (2006) Suprachiasmatic regulation of circadian rhythms of gene expression in hamster peripheral organs: effects of transplanting the pacemaker. J. Neurosci. 26, 6406-6412. https://doi.org/10.1523/JNEUROSCI.4676-05.2006
  35. Hadden, H., Soldin, S. J. and Massaro, D. (2012) Circadian disruption alters mouse lung clock gene expression and lung mechanics. J. Appl. Physiol. 113, 385-392. https://doi.org/10.1152/japplphysiol.00244.2012
  36. Haeck, I. M., Timmer-de Mik, L., Lentjes, E. G., Buskens, E., Hijnen, D. J., Guikers, C., Bruijnzeel-Koomen, C. A. F. M. and de Bruin-Weller, M. S. (2007) Low basal serum cortisol in patients with severe atopic dermatitis: potent topical corticosteroids wrongfully accused. Br. J. Dermatol. 156, 979-985. https://doi.org/10.1111/j.1365-2133.2007.07753.x
  37. Halberg, F., Johnson, E. A., Brown, B. W. and Bittner, J. J. (1960) Susceptibility rhythm to E. coli endotoxin and bioassay. Proc. Soc. Exp. Biol. Med. 103, 142-144. https://doi.org/10.3181/00379727-103-25439
  38. Haldar, C. and Ahmad, R. (2010) Photoimmunomodulation and melatonin. J. Photochem. Photobiol. B Biol. 98, 107-117. https://doi.org/10.1016/j.jphotobiol.2009.11.014
  39. Hara-Chikuma, M. and Verkman, A. S. (2008) Roles of aquaporin-3 in the epidermis. J. Invest. Dermatol. 128, 2145-2151. https://doi.org/10.1038/jid.2008.70
  40. Hastings, M., O'Neill, J. S. and Maywood, E. S. (2007) Circadian clocks: regulators of endocrine and metabolic rhythms. J. Endocrinol. 195, 187-198. https://doi.org/10.1677/JOE-07-0378
  41. Haus, E. (2007) Chronobiology in the endocrine system. Adv. Drug Deliv. Rev. 59, 985-1014. https://doi.org/10.1016/j.addr.2007.01.001
  42. Hayashi, M., Shimba, S. and Tezuka, M. (2007) Characterization of the molecular clock in mouse peritoneal macrophages. Biol. Pharm. Bull. 30, 621-626. https://doi.org/10.1248/bpb.30.621
  43. Hrushesky, W. J., Langevin, T., Kim, Y. J. and Wood, P. A. (1994) Circadian dynamics of tumor necrosis factor alpha (cachectin) lethality. J. Exp. Med. 180, 1059-1065. https://doi.org/10.1084/jem.180.3.1059
  44. Hwang, J. W., Sundar, I. K., Yao, H., Sellix, M. T. and Rahman, I. (2014) Circadian clock function is disrupted by environmental tobacco/cigarette smoke, leading to lung inflammation and injury via a SIRT1-BMAL1 pathway. FASEB J. 28, 176-194. https://doi.org/10.1096/fj.13-232629
  45. Inouye, S. T. and Kawamura, H. (1979) Persistence of circadian rhythmicity in a mammalian hypothalamic "island" containing the suprachiasmatic nucleus. Proc. Natl. Acad. Sci. U.S.A. 76, 5962-5966. https://doi.org/10.1073/pnas.76.11.5962
  46. Kawate, T., Abo, T., Hinuma, S. and Kumagai, K. (1981) Studies of the bioperiodicity of the immune response. II. Co-variations of murine T and B cells and a role of corticosteroid. J. Immunol. 126, 1364-1367.
  47. Keller, M., Mazuch, J., Abraham, U., Eom, G. D., Herzog, E. D., Volk, H., Kramer, A. and Maier, B. (2009) A circadian clock in macrophages controls inflammatory immune responses. Proc. Natl. Acad. Sci. U.S.A. 106, 21407-21412. https://doi.org/10.1073/pnas.0906361106
  48. Kelly, E. A., Houtman, J. J. and Jarjour, N. N. (2004) Inflammatory changes associated with circadian variation in pulmonary function in subjects with mild asthma. Clin. Exp. Allergy 34, 227-233. https://doi.org/10.1111/j.1365-2222.2004.01866.x
  49. Kiessling, S., Eichele, G. and Oster, H. (2010) Adrenal glucocorticoids have a key role in circadian resynchronization in a mouse model of jet lag. J. Clin. Invest. 120, 2600-2609. https://doi.org/10.1172/JCI41192
  50. Kim, T. H., Jung, J. A., Kim, G. D., Jang, A. H., Ahn, H. J., Park, Y. S. and Park, C. S. (2009) Melatonin inhibits the development of 2,4-dinitrofluorobenzene-induced atopic dermatitis-like skin lesions in NC/Nga mice. J. Pineal Res. 47, 324-329. https://doi.org/10.1111/j.1600-079X.2009.00718.x
  51. Kobayashi, E. H., Suzuki, T., Funayama, R., Nagashima, T., Hayashi, M., Sekine, H., Tanaka, N., Moriguchi, T., Motohashi, H., Nakayama, K. and Yamamoto, M. (2016) Nrf2 suppresses macrophage inflammatory response by blocking proinflammatory cytokine transcription. Nat. Commun. 7, 11624. https://doi.org/10.1038/ncomms11624
  52. Kondratov, R. V., Vykhovanets, O., Kondratova, A. A. and Antoch, M. P. (2009) Antioxidant N-acetyl-L-cysteine ameliorates symptoms of premature aging associated with the deficiency of the circadian protein BMAL1. Aging (Albany N.Y.) 1, 979-987. https://doi.org/10.18632/aging.100113
  53. Kondratov, R. V., Kondratova, A. A., Gorbacheva, V. Y., Vykhovanets, O. V. and Antoch, M. P. (2006) Early aging and age-related pathologies in mice deficient in BMAL1, the core component of the circadian clock. Genes Dev. 20, 1868-1873. https://doi.org/10.1101/gad.1432206
  54. Krieger, D. T. (1975) Rhythms of ACTH and corticosteroid secretion in health and disease, and their experimental modification. J. Steroid Biochem. 6, 785-791. https://doi.org/10.1016/0022-4731(75)90068-0
  55. Kwak, Y., Lundkvist, G. B., Brask, J., Davidson, A., Menaker, M., Kritensoon, K. and Block, G. D. (2008) Interferon-gamma alters electrical activity and clock gene expression in suprachiasmatic nucleus neurons. J. Biol. Rhythms 23, 150-159. https://doi.org/10.1177/0748730407313355
  56. Lakatos, P., Blumsohn, A., Eastell, R., Tarjan, G., Shinoda, H. and Sterm. P. H. (1995) Circadian rhythm of in vitro bone-resorbing activity in human serum. J. Clin. Endocrinol. Metab. 80, 3185-3190. https://doi.org/10.1210/jcem.80.11.7593424
  57. Lamia, K. A., Storch, K. F. and Weitz, C. J. (2008) Physiological significance of a peripheral tissue circadian clock. Proc. Natl. Acad. Sci. U.S.A. 105, 15172-15177. https://doi.org/10.1073/pnas.0806717105
  58. Lange, T., Dimitrov, S., Fehm, H. L. and Born, J. (2006) Sleep-like concentrations of growth hormone and cortisol modulate type 1 and type2 in-vitro cytokine production in human T cells. Int. Immunopharmacol. 6, 216-225. https://doi.org/10.1016/j.intimp.2005.08.006
  59. Lange, T., Dimitrov, S. and Born, J. (2010) Effects of sleep and circadian rhythm on the human immune system. Ann. N. Y. Acad. Sci. 1193, 48-59. https://doi.org/10.1111/j.1749-6632.2009.05300.x
  60. Le Fur, I., Reinberg, A., Lopez, S., Morizot, F., Mechkouri, M. and Tschachler, E. (2001) Analysis of circadian and ultradian rhythms of skin surface properties of face and forearm of healthy women. J. Invest. Dermatol. 117, 718-724. https://doi.org/10.1046/j.0022-202x.2001.01433.x
  61. Lee, H., Chen, R., Lee, Y., Yoo, S. and Lee, C. (2009) Essential roles of CKIδ and CKIε in the mammalian circadian clock. Proc. Natl. Acad. Sci. U.S.A. 106, 21359-21366. https://doi.org/10.1073/pnas.0906651106
  62. Lee, J., Moulik, M., Fang, Z., Saha, P., Zou, F., Xu, Y., Nelson, D. L., Ma, K., Moore, D. D. and Yechoor, V. K. (2013) Bmal1 and β-cell clock are required for adaptation to circadian disruption, and their loss of function leads to oxidative stress-induced β-cell failure in mice. Mol. Cell. Biol. 33, 2327-2338. https://doi.org/10.1128/MCB.01421-12
  63. Lincoln, G. A., Clarke, I. J., Hut, R. A. and Hazlerigg, D. G. (2006) Characterizing a mammalian circannual pacemaker. Science 314, 1941-1944. https://doi.org/10.1126/science.1132009
  64. Litinski, M., Scheer, F. A. and Shea, S. A. (2009) Influence of the circadian system on disease severity. Sleep Med. Clin. 4, 143-163. https://doi.org/10.1016/j.jsmc.2009.02.005
  65. Liu, J., Mankani, G., Shi, A., Meyer, M., Cunningham-Runddles, S., Ma, X. and Sun, Z. S. (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. https://doi.org/10.1128/IAI.00287-06
  66. Majde, J. A. and Krueger, J. M. (2005) Links between the innate immune system and sleep. J. Allergy Clin. Immunol. 116, 1188-1198. https://doi.org/10.1016/j.jaci.2005.08.005
  67. Maronde, E. and Stehle, J. H. (2007) The mammalian pineal gland: known facts, unknown facets. Trends Endocrinol. Metab. 18, 142-149. https://doi.org/10.1016/j.tem.2007.03.001
  68. Marpegan, L., Bekinschtein, T. A., Costas, M. A. and Golombek, D. A. (2005) Circadian responses to endotoxin treatment in mice. J. Neuroimmunol. 160, 102-109. https://doi.org/10.1016/j.jneuroim.2004.11.003
  69. Mauriz, J. L., Collado, P. S., Veneroso, C., Reiter, R. J. and GonzalesGallego, J. (2013) A review of the molecular aspects of melatonin's anti-inflammatory actions: recent insights and new perspectives. J. Pineal Res. 54, 1-14. https://doi.org/10.1111/j.1600-079X.2012.01014.x
  70. Meyer-Bernstein, E. L., Jetton, A. E., Matsumoto, S. I., Markuns, J. F., Lehman, M. N. and Bittman, E. L. (1999) Effects of suprachiasmatic transplants on circadian rhythms of neuroendocrine function in golden hamsters. Endocrinology 140, 207-218. https://doi.org/10.1210/endo.140.1.6428
  71. Mittal, M., Siddiqui, M. R., Tran, K., Reddy, S. P. and Malik, A. B. (2014) Reactive oxygen species in inflammation and tissue injury. Antioxid. Redox Signal. 20, 1126-1167. https://doi.org/10.1089/ars.2012.5149
  72. Munoz-Hoyos, A., Espin-Quirantes, C., Molina-Carballo, A., Uberos, J., Contreras-Chova, F., Narbona-Lopez, E. and Gutierrez-Salmeron, M. J. (2007) Neuroendocrine and circadian aspects (melatonin and beta-endorphin) of atopic dermatitis in the child. Pediatr. Allergy Immunol. 18, 679-686. https://doi.org/10.1111/j.1399-3038.2007.00574.x
  73. Musiek, E. S., Lim, M. M., Yang, G., Bauer, A. Q., Qi, L., Lee, Y., Roh, J. H., Ortiz-Gonzalez, X., Dearborn, J. T., Culver, J. P., Herzog, E. D., Hogenesch, J. B., Wozniak, D. F., Dikranian, K., Giasson, B. I., Weaver, D. R., Holtzman, D. M. and Fitzgerald, G. A (2013) Circadian clock proteins regulate neuronal redox homeostasis and neurodegeneration. J. Clin. Invest. 123, 5389-5400. https://doi.org/10.1172/JCI70317
  74. Nagoshi, E., Saini, C., Bauer, C., Laroche, T., Naf, F. and Schibler, U. (2004) Circadian gene expression in individual fibroblasts: cellautonomous and self-sustained oscillators pass time to daughter cells. Cell 119, 693-705. https://doi.org/10.1016/j.cell.2004.11.015
  75. Nakagawa, H. and Okumura, N. (2010) Coordinated regulation of circadian rhythms and homeostasis by the suprachiasmatic nucleus. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 86, 391-409. https://doi.org/10.2183/pjab.86.391
  76. Neeck, G., Federlin, K., Graef, V., Rusch, D. and Schmidt, K. L. (1990) Adrenal secretion of cortisol in patients with rheumatoid arthritis. J. Rheumatol. 17, 24-29.
  77. Nguyen, K. D., Fentress, S. J., Qiu, Y., Yun, K., Cox, J. S. and Chawla, A. (2013) Circadian gene Bmal1 regulates diurnal oscillations of Ly6C(hi) inflammatory monocytes. Science 341, 1483-1488. https://doi.org/10.1126/science.1240636
  78. Oishi, Y., Hayashi, S., Isagawa, T., Oshima, M., Iwama, A., Shimba, S., Okamura, H. and Manabe, I. (2017) Bmal1 regulates inflammatory responses in macrophages by modulating enhancer RNA transcription. Sci. Rep. 7, 7086. https://doi.org/10.1038/s41598-017-07100-3
  79. Patel, T., Ishiuji, Y. and Yosipovitch, G. (2007) Nocturnal itch: why do we itch at night? Acta Derm. Venereol. 87, 295-298. https://doi.org/10.2340/00015555-0280
  80. Pekovic-Vaughan, V., Gibbs, J., Yoshitane, H., Yang, N., Pathiranage, D., Guo, B., Sagami, A., Taguchi, K., Bechtole, D., Loudon, A., Yamamoto, M., Chan, J., van der Horst, G. T., Fukada, Y. and Meng, Q. (2014) The circadian clock regulates rhythmic activation of the NRF2/glutathione-mediated antioxidant defense pathway to modulate pulmonary fibrosis. Genes Dev. 28, 548-560. https://doi.org/10.1101/gad.237081.113
  81. Ralph, M. R., Foster, R. G., Davis, F. C. and Menaker, M. (1990) Transplanted suprachiasmatic nucleus determines circadian period. Science 247, 975-978. https://doi.org/10.1126/science.2305266
  82. Robinson, I. and Reddy, A. B. (2014) Molecular mechanisms of the circadian clockwork in mammals. FEBS Lett. 588, 2477-2483. https://doi.org/10.1016/j.febslet.2014.06.005
  83. Rosenwasser, A. M. (2009) Functional neuroanatomy of sleep and circadian rhythms. Brain Res. Rev. 61, 281-306. https://doi.org/10.1016/j.brainresrev.2009.08.001
  84. Schibler, U. (2006) Circadian time keeping: the daily ups and downs of genes, cells, and organisms. Prog. Brain Res. 153, 271-282. https://doi.org/10.1016/S0079-6123(06)53016-X
  85. Schibler, U. (2007) The daily timing of gene expression and physiology in mammals. Dialogues Clin. Neurosci. 9, 257-272. https://doi.org/10.31887/DCNS.2007.9.3/uschibler
  86. Schmidt, R., Parish, E. J., Dionisius, V., Cathelineau, C., Michel, S., Shroot, B., Rolland, A., Brzokewicz, A. and Reichert, U. (1991) Modulation of cellular cholesterol and its effect on cornified envelope formation in cultured human epidermal keratinocytes. J. Invest. Dermatol. 97, 771-775. https://doi.org/10.1111/1523-1747.ep12486720
  87. Schwarz, W., Birau, N., Hornstein, O. P., Heubeck, B., Schonberger, A., Meyer, C. and Gottschalk, J. (1988) Alterations of melatonin secretion in atopic eczema. Acta Derm. Venereol. 68, 224-229.
  88. Segall, L. A. and Amir, S. (2010) Glucocorticoid regulation of clock gene expression in the mammalian limbic forebrain. J. Mol. Neurosci. 42, 168-175. https://doi.org/10.1007/s12031-010-9341-1
  89. Silver, A. C., Arjona, A., Walker, W. E. and Fikrig, E. (2012) The circadian clock controls toll-like receptor 9-mediated innate and adaptive immunity. Immunity 36, 251-261. https://doi.org/10.1016/j.immuni.2011.12.017
  90. So, A. Y., Bernal, T. U., Pillsbury, M. L., Yamamoto, K. R. and Feldman, B. J. (2009) Glucocorticoid regulation of the circadian clock modulates glucose homeostasis. Proc .Natl. Acad. Sci. U.S.A. 106, 17582-17587. https://doi.org/10.1073/pnas.0909733106
  91. Son, G. H., Chung, S. and Kim, K. (2011) The adrenal peripheral clock: glucocorticoid and the circadian timing system. Front. Neuroendocrinol. 32, 451-465. https://doi.org/10.1016/j.yfrne.2011.07.003
  92. Sporl, F., Schellenberg, K., Blatt, T., Wenck, H., Wittern, K., Schrader, A. and Kramer, A. (2011) A circadian clock in HaCaT keratinocytes. J. Invest. Dermatol. 131, 338-348. https://doi.org/10.1038/jid.2010.315
  93. Storch, K. F., Paz, C., Signorovitch, J., Raviola, E., Pawlyk, B., Li, T. and Weitz, C. J. (2007) Intrinsic circadian clock of the mammalian retina: importance for retinal processing of visual information. Cell 130, 730-741. https://doi.org/10.1016/j.cell.2007.06.045
  94. Sulli, A., Maestroni, G. J., Villaggio, B., Hertens, E., Craviotto, C., Pizzorni, C., Briata, M., Seriolo, B. and Cutolo, M. (2002) Melatonin serum levels in rheumatoid arthritis. Ann. N. Y. Acad. Sci. 966, 276-283. https://doi.org/10.1111/j.1749-6632.2002.tb04227.x
  95. Takahashi, J. S., Hong, H. K., Ko, C. H. and McDearmon, E. L. (2008) The genetics of mammalian circadian order and disorder: implications for physiology and disease. Nat. Rev. Genet. 9, 764-775. https://doi.org/10.1038/nrg2430
  96. Vaughn, A. R., Clark, A. K., Sivamani, R. K. and Shi, V. Y. (2018) Circadian rhythm in atopic dermatitis-pathophysiology and implications for chronotherapy. Pediatr. Dermatol. 35, 152-157. https://doi.org/10.1111/pde.13364
  97. Verschoore, M., Poncet, M., Krebs, B. and Ortonne, J. P. (1993) Circadian variations in the number of actively secreting sebaceous follicles and androgen circadian rhythms. Chronobiol. Int. 10, 349-359. https://doi.org/10.3109/07420529309064489
  98. Webster, J. I., Tonelli, L. and Sternberg, E. M. (2002) Neuroendocrine regulation of immunity. Annu. Rev. Immunol. 20, 125-163. https://doi.org/10.1146/annurev.immunol.20.082401.104914
  99. Welsh, D. K., Yoo, S. H., Liu, A. C., Takahashi, J. S. and Kay, S. A. (2004) Bioluminescence imaging of individual fibroblasts reveals persistent, independently phased circadian rhythms of clock gene expression. Curr. Biol. 14, 2289-2295. https://doi.org/10.1016/j.cub.2004.11.057
  100. Yamazaki, S., Numano, R., Abe, M., Hida, A., Takahashi, R., Ueda, M., Block, G. D., Sakaki, Y., Menaker, M. and Tei, H. (2000) Resetting central and peripheral circadian oscillators in transgenic rats. Science 288, 682-685. https://doi.org/10.1126/science.288.5466.682
  101. Yosipovitch, G., Xiong, G. L., Haus, E., Sackett-Lundeen, L., Ashkenazi, I. and Maibach, H. I. (1998) Time-dependent variations of the skin barrier function in humans: transepidermal water loss, stratum corneum hydration, skin surface pH, and skin temperature. J. Invest. Dermatol. 110, 20-23. https://doi.org/10.1046/j.1523-1747.1998.00069.x
  102. Yosipovitch, G., Goon, A. T., Wee, J., Chan, Y. H., Zucker, I. and Goh, C. L. (2002) Itch characteristics in Chinese patients with atopic dermatitis using a new questionnaire for the assessment of pruritus. Int. J. Dermatol. 41, 212-216. https://doi.org/10.1046/j.1365-4362.2002.01460.x
  103. Yosipovitch, G., Sackett-Lundeen, L., Goon, A., Huak, C. Y., Goh, C. L. and Haus, E. (2004) Circadian and ultradian (12 h) variations of skin blood flow and barrier function in non-irritated and irritated skin-effect of topical corticosteroids. J. Invest. Dermatol. 122, 824-829. https://doi.org/10.1111/j.0022-202X.2004.22313.x
  104. Young, M. R., Matthews, J. P., Kanabrocki, E. L., Sothern, R. B., Roitman-Johnson, B. and Scheving, L. E. (1995) Circadian rhythmometry of serum interleukin-2, interleukin-10, tumor necrosis factoralpha, and granulocyte-macrophage colony-stimulating factor in men. Chronobiol. Int. 12, 19-27. https://doi.org/10.3109/07420529509064496
  105. Zheng, B., Larkin, D. W., Albrecht, U., Sun, Z. S., Sage, M., Eichele, G., Lee, C. C. and Bradley, A. (1999) The mPer2 gene encodes a functional componentof the mammalian circadian clock. Nature 400, 169-173. https://doi.org/10.1038/22118