Circadian Control of Inflammatory Processes in Atherosclerosis and Its Complications

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 37, Issue 6, 2017, Pages 1022-1028

  Steffens, Sabine ^a,b   Winter, Carla ^a   Schloss, Maximilian J ^a   Hidalgo, Andres ^a,c   Weber, Christian ^a,b,d   Soehnlein, Oliver ^a,b,e  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

^c CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

^d MAASTRICHT UNIVERSITY   (Netherlands)

^e KAROLINSKA INSTITUTE   (Sweden)

Author keywords

atherosclerosis; cardiovascular disease; circadian rhythm; incidence; myocardial infarction

Indexed keywords

ATHEROSCLEROSIS; CARDIOVASCULAR FUNCTION; CIRCADIAN RHYTHM; COMPLICATION; DRESSLER SYNDROME; HEART MUSCLE INJURY; HEMATOPOIESIS; HUMAN; INFLAMMATION; METABOLISM; MOLECULAR CLOCK; NONHUMAN; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REGULATORY MECHANISM; REVIEW; TISSUE REPAIR; ANIMAL; CARDIAC MUSCLE; MYOCARDIAL INFARCTION; PATHOLOGY; PATHOPHYSIOLOGY; SIGNAL TRANSDUCTION; TIME FACTOR; WOUND HEALING;

AUTACOID; CIRCADIAN RHYTHM SIGNALING PROTEIN;

ANIMALS; ATHEROSCLEROSIS; CIRCADIAN CLOCKS; CIRCADIAN RHYTHM; CIRCADIAN RHYTHM SIGNALING PEPTIDES AND PROTEINS; HEMATOPOIESIS; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; MYOCARDIAL INFARCTION; MYOCARDIUM; SIGNAL TRANSDUCTION; TIME FACTORS; WOUND HEALING;

EID: 85019746083     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.117.309374     Document Type: Review

References (64)

1. Chen L, Yang G, Recent advances in circadian rhythms in cardiovascular system. Front Pharmacol 2015 6 71. doi: 10.3389/fphar.2015.00071.
2. Feng D, Lazar MA, Clocks, metabolism, and the epigenome. Mol Cell 2012 47 158 167. doi: 10.1016/j.molcel.2012.06.026.
3. Green CB, Takahashi JS, Bass J, The meter of metabolism. Cell 2008 134 728 742. doi: 10.1016/j.cell.2008.08.022.
4. Panda S, Antoch MP, Miller BH, Su AI, Schook AB, Straume M, Schultz PG, Kay SA, Takahashi JS, Hogenesch JB, Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 2002 109 307 320
5. Zhang R, Lahens NF, Ballance HI, Hughes ME, Hogenesch JB, A circadian gene expression atlas in mammals: implications for biology and medicine. Proc Natl Acad Sci USA 2014 111 16219 16224. doi: 10.1073/pnas.1408886111.
6. Scheiermann C, Kunisaki Y, Frenette PS, Circadian control of the immune system. Nat Rev Immunol 2013 13 190 198. doi: 10.1038/nri3386.
7. Scheiermann C, Kunisaki Y, Lucas D, Chow A, Jang JE, Zhang D, Hashimoto D, Merad M, Frenette PS, Adrenergic nerves govern circadian leukocyte recruitment to tissues. Immunity 2012 37 290 301. doi: 10.1016/j.immuni.2012.05.021.
8. Schloss MJ, Horckmans M, Nitz K, Duchene J, Drechsler M, Bidzhekov K, Scheiermann C, Weber C, Soehnlein O, Steffens S, The time-of-day of myocardial infarction onset affects healing through oscillations in cardiac neutrophil recruitment. EMBO Mol Med 2016 8 937 948. doi: 10.15252/emmm.201506083.
9. Swirski FK, Libby P, Aikawa E, Alcaide P, Luscinskas FW, Weissleder R, Pittet MJ, Ly-6Chi monocytes dominate hypercholesterolemia-associated monocytosis and give rise to macrophages in atheromata. J Clin Invest 2007 117 195 205. doi: 10.1172/JCI29950.
10. Nguyen KD, Fentress SJ, Qiu Y, Yun K, Cox JS, Chawla A, Circadian gene Bmal1 regulates diurnal oscillations of Ly6C(hi) inflammatory monocytes. Science 2013 341 1483 1488. doi: 10.1126/science.1240636.
11. Libby P, Ridker PM, Hansson GK, Progress and challenges in translating the biology of atherosclerosis. Nature 2011 473 317 325. doi: 10.1038/nature10146.
12. Husse J, Eichele G, Oster H, Synchronization of the mammalian circadian timing system: Light can control peripheral clocks independently of the SCN clock: alternate routes of entrainment optimize the alignment of the body's circadian clock network with external time. Bioessays 2015 37 1119 1128. doi: 10.1002/bies.201500026.
13. Golombek DA, Rosenstein RE, Physiology of circadian entrainment. Physiol Rev 2010 90 1063 1102. doi: 10.1152/physrev.00009.2009.
14. 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 2005 2 297 307. doi: 10.1016/j.cmet.2005.09.009.
15. Balsalobre A, Brown SA, Marcacci L, Tronche F, Kellendonk C, Reichardt HM, Schütz G, Schibler U, Resetting of circadian time in peripheral tissues by glucocorticoid signaling. Science 2000 289 2344 2347
16. Shearman LP, Sriram S, Weaver DR, Maywood ES, Chaves I, Zheng B, Kume K, Lee CC, van der Horst GT, Hastings MH, Reppert SM, Interacting molecular loops in the mammalian circadian clock. Science 2000 288 1013 1019
17. Preitner N, Damiola F, Lopez-Molina L, Zakany J, Duboule D, Albrecht U, Schibler U, The orphan nuclear receptor REV-ERBalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell 2002 110 251 260
18. Takeda Y, Jothi R, Birault V, Jetten AM, RORγ directly regulates the circadian expression of clock genes and downstream targets in vivo. Nucleic Acids Res 2012 40 8519 8535. doi: 10.1093/nar/gks630.
19. Silver AC, Arjona A, Walker WE, Fikrig E, The circadian clock controls toll-like receptor 9-mediated innate and adaptive immunity. Immunity 2012 36 251 261. doi: 10.1016/j.immuni.2011.12.017.
20. Tofler GH, Brezinski D, Schafer AI, Czeisler CA, Rutherford JD, Willich SN, Gleason RE, Williams GH, Muller JE, Concurrent morning increase in platelet aggregability and the risk of myocardial infarction and sudden cardiac death. N Engl J Med 1987 316 1514 1518. doi: 10.1056/NEJM198706113162405.
21. Millar-Craig MW, Bishop CN, Raftery EB, Circadian variation of blood-pressure. Lancet 1978 1 795 797
22. Muller JE, Ludmer PL, Willich SN, Tofler GH, Aylmer G, Klangos I, Stone PH, Circadian variation in the frequency of sudden cardiac death. Circulation 1987 75 131 138
23. Muller JE, Tofler GH, Willich SN, Stone PH, Circadian variation of cardiovascular disease and sympathetic activity. J Cardiovasc Pharmacol 1987 10 suppl 2 S104-S109. discussion S110-101
24. Goldberg RJ, Brady P, Muller JE, Chen ZY, de Groot M, Zonneveld P, Dalen JE, Time of onset of symptoms of acute myocardial infarction. Am J Cardiol 1990 66 140 144
25. Carson PA, O'Connor CM, Miller AB, Anderson S, Belkin R, Neuberg GW, Wertheimer JH, Frid D, Cropp A, Packer M, Circadian rhythm and sudden death in heart failure: results from Prospective Randomized Amlodipine Survival Trial. J Am Coll Cardiol 2000 36 541 546
26. Tsementzis SA, Gill JS, Hitchcock ER, Gill SK, Beevers DG, Diurnal variation of and activity during the onset of stroke. Neurosurgery 1985 17 901 904
27. Knutsson A, Akerstedt T, Jonsson BG, Orth-Gomer K, Increased risk of ischaemic heart disease in shift workers. Lancet 1986 2 89 92
28. Boden G, Ruiz J, Urbain JL, Chen X, Evidence for a circadian rhythm of insulin secretion. Am J Physiol 1996 271 2 pt 1 E246 E252
29. Sennels HP, Jørgensen HL, Fahrenkrug J, Diurnal changes of biochemical metabolic markers in healthy young males-the Bispebjerg study of diurnal variations. Scand J Clin Lab Invest 2015 75 686 692. doi: 10.3109/00365513.2015.1080385.
30. Sennels HP, Jørgensen HL, Hansen AL, Goetze JP, Fahrenkrug J, Diurnal variation of hematology parameters in healthy young males: the Bispebjerg study of diurnal variations. Scand J Clin Lab Invest 2011 71 532 541. doi: 10.3109/00365513.2011.602422.
31. Man K, Loudon A, Chawla A, Immunity around the clock. Science 2016 354 999 1003. doi: 10.1126/science.aah4966.
32. Mercier FE, Ragu C, Scadden DT, The bone marrow at the crossroads of blood and immunity. Nat Rev Immunol 2011 12 49 60. doi: 10.1038/nri3132.
33. Smaaland R, Sothern RB, Laerum OD, Abrahamsen JF, Rhythms in human bone marrow and blood cells. Chronobiol Int 2002 19 101 127
34. Lucas D, Battista M, Shi PA, Isola L, Frenette PS, Mobilized hematopoietic stem cell yield depends on species-specific circadian timing. Cell Stem Cell 2008 3 364 366. doi: 10.1016/j.stem.2008.09.004.
35. Méndez-Ferrer S, Lucas D, Battista M, Frenette PS, Haematopoietic stem cell release is regulated by circadian oscillations. Nature 2008 452 442 447. doi: 10.1038/nature06685.
36. Katayama Y, Battista M, Kao WM, Hidalgo A, Peired AJ, Thomas SA, Frenette PS, Signals from the sympathetic nervous system regulate hematopoietic stem cell egress from bone marrow. Cell 2006 124 407 421. doi: 10.1016/j.cell.2005.10.041.
37. Méndez-Ferrer S, Michurina TV, Ferraro F, Mazloom AR, Macarthur BD, Lira SA, Scadden DT, Ma'ayan A, Enikolopov GN, Frenette PS, Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 2010 466 829 834. doi: 10.1038/nature09262.
38. Dutta P, Courties G, Wei Y, Myocardial infarction accelerates atherosclerosis. Nature 2012 487 325 329. doi: 10.1038/nature11260.
39. Soehnlein O, Steffens S, Hidalgo A, Weber C, Neutrophils as protagonists and targets in chronic inflammation. Nat Rev Immunol 2017 17 248 261. doi: 10.1038/nri.2017.10.
40. Casanova-Acebes M, Pitaval C, Weiss LA, Nombela-Arrieta C, Chèvre R, A-González N, Kunisaki Y, Zhang D, van Rooijen N, Silberstein LE, Weber C, Nagasawa T, Frenette PS, Castrillo A, Hidalgo A, Rhythmic modulation of the hematopoietic niche through neutrophil clearance. Cell 2013 153 1025 1035. doi: 10.1016/j.cell.2013.04.040.
41. Rudic RD, McNamara P, Reilly D, Grosser T, Curtis AM, Price TS, Panda S, Hogenesch JB, FitzGerald GA, Bioinformatic analysis of circadian gene oscillation in mouse aorta. Circulation 2005 112 2716 2724. doi: 10.1161/CIRCULATIONAHA.105.568626.
42. Lin C, Tang X, Zhu Z, Liao X, Zhao R, Fu W, Chen B, Jiang J, Qian R, Guo D, The rhythmic expression of clock genes attenuated in human plaque-derived vascular smooth muscle cells. Lipids Health Dis 2014 13 14. doi: 10.1186/1476-511X-13-14.
43. Xu C, Lu C, Hua L, Jin H, Yin L, Chen S, Qian R, Rhythm changes of clock genes, apoptosis-related genes and atherosclerosis-related genes in apolipoprotein E knockout mice. Can J Cardiol 2009 25 473 479
44. Yang L, Chu Y, Wang L, Wang Y, Zhao X, He W, Zhang P, Yang X, Liu X, Tian L, Li B, Dong S, Gao C, Overexpression of CRY1 protects against the development of atherosclerosis via the TLR/NF-κB pathway. Int Immunopharmacol 2015 28 525 530. doi: 10.1016/j.intimp.2015.07.001.
45. Ma H, Zhong W, Jiang Y, Fontaine C, Li S, Fu J, Olkkonen VM, Staels B, Yan D, Increased atherosclerotic lesions in LDL receptor deficient mice with hematopoietic nuclear receptor Rev-erbα knock-down. J Am Heart Assoc 2013 2 e000235. doi: 10.1161/JAHA.113.000235.
46. Sitaula S, Billon C, Kamenecka TM, Solt LA, Burris TP, Suppression of atherosclerosis by synthetic REV-ERB agonist. Biochem Biophys Res Commun 2015 460 566 571. doi: 10.1016/j.bbrc.2015.03.070.
47. Yang G, Chen L, Grant GR, Paschos G, Song WL, Musiek ES, Lee V, McLoughlin SC, Grosser T, Cotsarelis G, FitzGerald GA, Timing of expression of the core clock gene bmal1 influences its effects on aging and survival. Sci Transl Med 2016 8 324ra316. doi: 10.1126/scitranslmed.aad3305.
48. Sládek M, Sumová A, Kováciková Z, Bendová Z, Laurinová K, Illnerová H, Insight into molecular core clock mechanism of embryonic and early postnatal rat suprachiasmatic nucleus. Proc Natl Acad Sci USA 2004 101 6231 6236. doi: 10.1073/pnas.0401149101.
49. Huo M, Huang Y, Qu D, Zhang H, Wong WT, Chawla A, Huang Y, Tian XY, Myeloid Bmal1 deletion increases monocyte recruitment and worsens atherosclerosis. FASEB J 2017 31 1097 1106. doi: 10.1096/fj.201601030R.
50. Boring L, Gosling J, Cleary M, Charo IF, Decreased lesion formation in CCR2-/-mice reveals a role for chemokines in the initiation of atherosclerosis. Nature 1998 394 894 897. doi: 10.1038/29788.
51. Gu L, Okada Y, Clinton SK, Gerard C, Sukhova GK, Libby P, Rollins BJ, Absence of monocyte chemoattractant protein-1 reduces atherosclerosis in low density lipoprotein receptor-deficient mice. Mol Cell 1998 2 275 281
52. Soehnlein O, Drechsler M, Döring Y, Distinct functions of chemokine receptor axes in the atherogenic mobilization and recruitment of classical monocytes. EMBO Mol Med 2013 5 471 481. doi: 10.1002/emmm.201201717.
53. 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 2007 115 2188 2195. doi: 10.1161/CIRCULATIONAHA.106.653303.
54. Yang Z, Ming XF, Recent advances in understanding endothelial dysfunction in atherosclerosis. Clin Med Res 2006 4 53 65
55. 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 2011 108 17147 17152. doi: 10.1073/pnas.1112998108.
56. Somanath PR, Podrez EA, Chen J, Ma Y, Marchant K, Antoch M, Byzova TV, Deficiency in core circadian protein Bmal1 is associated with a prothrombotic and vascular phenotype. J Cell Physiol 2011 226 132 140. doi: 10.1002/jcp.22314.
57. Keller M, Mazuch J, Abraham U, Eom GD, Herzog ED, Volk HD, Kramer A, Maier B, A circadian clock in macrophages controls inflammatory immune responses. Proc Natl Acad Sci USA 2009 106 21407 21412
58. Chalmers JA, Martino TA, Tata N, Ralph MR, Sole MJ, Belsham DD, Vascular circadian rhythms in a mouse vascular smooth muscle cell line (Movas-1). Am J Physiol Regul Integr Comp Physiol 2008 295 R1529 R1538. doi: 10.1152/ajpregu.90572.2008.
59. Suárez-Barrientos A, López-Romero P, Vivas D, Castro-Ferreira F, Núñez-Gil I, Franco E, Ruiz-Mateos B, García-Rubira JC, Fernández-Ortiz A, Macaya C, Ibanez B, Circadian variations of infarct size in acute myocardial infarction. Heart 2011 97 970 976. doi: 10.1136/hrt.2010.212621.
60. Fournier S, Eeckhout E, Mangiacapra F, Trana C, Lauriers N, Beggah AT, Monney P, Cook S, Bardy D, Vogt P, Muller O, Circadian variations of ischemic burden among patients with myocardial infarction undergoing primary percutaneous coronary intervention. Am Heart J 2012 163 208 213. doi: 10.1016/j.ahj.2011.11.006.
61. Reiter R, Swingen C, Moore L, Henry TD, Traverse JH, Circadian dependence of infarct size and left ventricular function after ST elevation myocardial infarction. Circ Res 2012 110 105 110. doi: 10.1161/CIRCRESAHA.111.254284.
62. Durgan DJ, Pulinilkunnil T, Villegas-Montoya C, Garvey ME, Frangogiannis NG, Michael LH, Chow CW, Dyck JR, Young ME, Short communication: ischemia/reperfusion tolerance is time-of-day-dependent: mediation by the cardiomyocyte circadian clock. Circ Res 2010 106 546 550. doi: 10.1161/CIRCRESAHA.109.209346.
63. Virag JA, Dries JL, Easton PR, Friesland AM, DeAntonio JH, Chintalgattu V, Cozzi E, Lehmann BD, Ding JM, Lust RM, Attenuation of myocardial injury in mice with functional deletion of the circadian rhythm gene mPer2. Am J Physiol Heart Circ Physiol 2010 298 H1088 H1095. doi: 10.1152/ajpheart.01280.2008.
64. Alibhai FJ, Tsimakouridze EV, Chinnappareddy N, Wright DC, Billia F, O'Sullivan ML, Pyle WG, Sole MJ, Martino TA, Short-term disruption of diurnal rhythms after murine myocardial infarction adversely affects long-term myocardial structure and function. Circ Res 2014 114 1713 1722. doi: 10.1161/CIRCRESAHA.114.302995.