Diurnal physiology: Core principles with application to the pathogenesis, diagnosis, prevention, and treatment of myocardial hypertrophy and failure

Journal of Applied Physiology

Volumn 107, Issue 4, 2009, Pages 1318-1327

  Sole, Michael J ^a   Martino, Tami A ^b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF GUELPH   (Canada)

Author keywords

Cardiac remodeling; Cardiomyopathy; Cardiovascular; Chronobiology; Circadian; Clock

Indexed keywords

BLOOD VESSEL; CARDIOVASCULAR FUNCTION; CIRCADIAN RHYTHM; DISEASE EXACERBATION; GENE EXPRESSION; HEART; HEART DISEASE; HEART FAILURE; HEART VENTRICLE HYPERTROPHY; HUMAN; NONHUMAN; ORGAN GROWTH; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; SLEEP;

ANIMALS; BIOLOGICAL CLOCKS; CARDIOMEGALY; CARDIOVASCULAR AGENTS; CARDIOVASCULAR SYSTEM; CHRONOBIOLOGY DISORDERS; CIRCADIAN RHYTHM; DRUG CHRONOTHERAPY; GENE EXPRESSION REGULATION; HEART FAILURE; HUMANS; SLEEP; TREATMENT OUTCOME;

EID: 70350091595     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00426.2009     Document Type: Review

References (99)

1. Almon RR, Yang E, Lai W, Androulakis IP, Ghimbovschi S, Hoffman EP, Jusko WJ, Dubois DC. Relationships between circadian rhythms and modulation of gene expression by glucocorticoids in skeletal muscle. Am J Physiol Regul Integr Comp Physiol 295: R1031-R1047, 2008.
2. Andrews NP, Gralnick HR, Merryman P, Vail M, Quyyumi AA. Mechanisms underlying the morning increase in platelet aggregation: a flow cytometry study. J Am Coll Cardiol 28: 1789-1795, 1996. (Pubitemid 26426236)
3. Anea CB, Zhang M, Stepp DW, Simkins GB, Reed G, Fulton DJ, Rudic RD. Vascular disease in mice with a dysfunctional circadian clock. Circulation 119: 1510-1517, 2009.
4. Arendt J. Melatonin and human rhythms. Chronobiol Int 23: 21-37, 2006.
5. 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. (Pubitemid 30739737)
6. Bergmann O, Bhardwaj RD, Bernard S, Zdunek S, Barnabe-Heider F, Walsh S, Zupicich J, Alkass K, Buchholz BA, Druid H, Jovinge S, Frisen J. Evidence for cardiomyocyte renewal in humans. Science 324: 98-102, 2009.
7. Bjarnason GA, Jordan R. Circadian variation of cell proliferation and cell cycle protein expression in man: clinical implications. Prog Cell Cycle Res 4: 193-206, 2000.
8. Bjarnason GA, Jordan RC, Sothern RB. Circadian variation in the expression of cell-cycle proteins in human oral epithelium. Am J Pathol 154: 613-622, 1999.
9. Bjarnason GA, Jordan RC, Wood PA, Li Q, Lincoln DW, Sothern RB, Hrushesky WJ, Ben-David Y. Circadian expression of clock genes in human oral mucosa and skin: association with specific cell-cycle phases. Am J Pathol 158: 1793 - 1801, 2001.
10. Bjarnason GA, Mackenzie RG, Nabid A, Hodson ID, El-Sayed S, Grimard L, Brundage M, Wright J, Hay J, Ganguly P, Leong C, Wilson J, Jordan RC, Walker M, Tu D, Parulekar W. Comparison of toxicity associated with early morning vs. late afternoon radiotherapy in patients with head-and-neck cancer: a prospective randomized trial of the National Cancer Institute of Canada Clinical Trials Group (HN3). Int J Radiat Oncol Biol Phys 73: 166-172, 2009.
11. Boateng SY, Goldspink PH. Assembly and maintenance of the sarcomere night and day. Cardiovasc Res 77: 667-675, 2008.
12. Bradley TD, Floras JS. Obstructive sleep apnoea and its cardiovascular consequences. Lancet 373: 82-93, 2009.
13. Bradley TD, Floras JS. Sleep apnea and heart failure. I. Obstructive sleep apnea. Circulation 107: 1671-1678, 2003. (Pubitemid 36397338)
14. Bray MS, Shaw CA, Moore MW, Garcia RA, Zanquetta MM, Durgan DJ, Jeong WJ, Tsai JY, Bugger H, Zhang D, Rohrwasser A, Rennison JH, Dyck JR, Litwin SE, Hardin PE, Chow CW, Chandler MP, Abel ED, Young ME. Disruption of the circadian clock within the cardiomyocyte influences myocardial contractile function, metabolism, and gene expression. Am J Physiol Heart Circ Physiol 294: H1036-H1047, 2008. (Pubitemid 351253318)
15. Bruckschlegel G, Holmer SR, Jandeleit K, Grimm D, Muders F, Kromer EP, Riegger GA, Schunkert H. Blockade of the renin-angiotensin system in cardiac pressure-overload hypertrophy in rats. Hypertension 25: 250-259, 1995.
16. Buja LM, Vela D. Cardiomyocyte death and renewal in the normal and diseased heart. Cardiovasc Pathol 17: 349-374, 2008.
17. Bunger MK, Wilsbacher LD, Moran SM, Clendenin C, Radcliffe LA, Hogenesch JB, Simon MC, Takahashi JS, Bradfield CA. Mop3 is an essential component of the master circadian pacemaker in mammals. Cell 103: 1009-1017, 2000. (Pubitemid 32037390)
18. Chalmers JA, Lin SY, Martino TA, Arab S, Liu P, Husain M, Sole MJ, Belsham DD. Diurnal profiling of neuroendocrine genes in murine heart, and shift in proopiomelanocortin gene expression with pressure-overload cardiac hypertrophy. J Mol Endocrinol 41: 117-124, 2008.
19. 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 295: R1529-R1538, 2008.
20. Chan CT, Floras JS, Miller JA, Richardson RM, Pierratos A. Regression of left ventricular hypertrophy after conversion to nocturnal hemodialysis. Kidney Int 61: 2235-2239, 2002. (Pubitemid 34539341)
21. Charloux A, Gronfier C, Lonsdorfer-Wolf E, Piquard F, Brandenberger G. Aldosterone release during the sleep-wake cycle in humans. Am J Physiol Endocrinol Metab 276: E43-E49, 1999. (Pubitemid 29065592)
22. Couch RD. Travel, time zones, and sudden cardiac death. Emporiatric pathology. Am J Forensic Med Pathol 11: 106-111, 1990.
23. Dardente H, Cermakian N. Molecular circadian rhythms in central and peripheral clocks in mammals. Chronobiol Int 24: 195-213, 2007. (Pubitemid 46643411)
24. Davidson AJ, Sellix MT, Daniel J, Yamazaki S, Menaker M, Block GD. Chronic jet-lag increases mortality in aged mice. Curr Biol 16: R914-916, 2006. (Pubitemid 44692110)
25. De la Sierra A, Redon J, Banegas JR, Segura J, Parati G, Gorostidi M, de la Cruz JJ, Sobrino J, Llisterri JL, Alonso J, Vinyoles E, Pallares V, Sarria A, Aranda P, Ruilope LM. Prevalence and factors associated with circadian blood pressure patterns in hypertensive patients. Hypertension 53: 466-472, 2009.
26. De Luca G, Suryapranata H, Ottervanger JP, van't Hof AW, Hoorntje JC, Gosselink AT, Dambrink JH, Zijlstra F, de Boer MJ. Circadian variation in myocardial perfusion and mortality in patients with STsegment elevation myocardial infarction treated by primary angioplasty. Am Heart J 150: 1185-1189, 2005.
27. Decousus HA, Croze M, Levi FA, Jaubert JG, Perpoint BM, De Bonadona JF, Reinberg A, Queneau PM. Circadian changes in anticoagulant effect of heparin infused at a constant rate. Br Med J (Clin Res Ed) 290: 341-344, 1985. (Pubitemid 15115448)
28. Dickmeis T. Glucocorticoids and the circadian clock. J Endocrinol 200: 3-22, 2009.
29. Doi M, Hirayama J, Sassone-Corsi P. Circadian regulator CLOCK is a histone acetyltransferase. Cell 125: 497-508, 2006.
30. Drouot X, Cabello B, d'Ortho MP, Brochard L. Sleep in the intensive care unit. Sleep Med Rev 12: 391-403, 2008.
31. Gangwisch JE, Malaspina D, Boden-Albala B, Heymsfield SB. Inadequate sleep as a risk factor for obesity: analyses of the NHANES I. Sleep 28: 1289-1296, 2005. (Pubitemid 41437890)
32. Glaser R, Naidu SS, Selzer F, Jacobs AK, Laskey WK, Srinivas VS, Slater JN, Wilensky RL. Factors associated with poorer prognosis for patients undergoing primary percutaneous coronary intervention during off-hours: biology or systems failure? JACC Cardiovasc Interv 1: 681-688, 2008.
33. Gorbacheva VY, Kondratov RV, Zhang R, Cherukuri S, Gudkov AV, Takahashi JS, Antoch MP. Circadian sensitivity to the chemotherapeutic agent cyclophosphamide depends on the functional status of the CLOCK/BMAL1 transactivation complex. Proc Natl Acad Sci USA 102: 3407-3412, 2005. (Pubitemid 40328058)
34. Grimaldi B, Nakahata Y, Kaluzova M, Masubuchi S, Sassone-Corsi P. Chromatin remodeling, metabolism and circadian clocks: the interplay of CLOCK and SIRT1. Int J Biochem Cell Biol 41: 81-86, 2009.
35. Guo YF, Stein PK. Circadian rhythm in the cardiovascular system: chronocardiology. Am Heart J 145: 779-786, 2003. (Pubitemid 36570947)
36. Hardt SE, Sadoshima J. Glycogen synthase kinase-3beta: a novel regulator of cardiac hypertrophy and development. Circ Res 90: 1055-1063, 2002. (Pubitemid 34627903)
37. Haus E, Nicolau G, Lakatua DJ, Sackett-Lundeen L, Petrescu E. Circadian rhythm parameters of endocrine functions in elderly subjects during the seventh to the ninth decade of life. Chronobiologia 16: 331-352, 1989. (Pubitemid 20122854)
38. Henriques JP, Haasdijk AP, Zijlstra F. Outcome of primary angioplasty for acute myocardial infarction during routine duty hours vs. during off-hours. J Am Coll Cardiol 41: 2138-2142, 2003. (Pubitemid 36724258)
39. Hermida RC. Ambulatory blood pressure monitoring in the prediction of cardiovascular events and effects of chronotherapy: rationale and design of the MAPEC study. Chronobiol Int 24: 749-775, 2007.
40. Hermida RC, Ayala DE, Calvo C, Lopez JE, Fernandez JR, Mojon A, Dominguez MJ, Covelo M. Administration time-dependent effects of aspirin on blood pressure in untreated hypertensive patients. Hypertension 41: 1259-1267, 2003. (Pubitemid 36706075)
41. Hermida RC, Ayala DE, Smolensky MH, Portaluppi F. Chronotherapy in hypertensive patients: administration-time dependent effects of treatment on blood pressure regulation. Expert Rev Cardiovasc Ther 5: 463-475, 2007. (Pubitemid 46805577)
42. Hobson JA. Sleep is of the brain, by the brain and for the brain. Nature 437: 1254-1256, 2005.
43. Hu K, Ivanov P, Hilton MF, Chen Z, Ayers RT, Stanley HE, Shea SA. Endogenous circadian rhythm in an index of cardiac vulnerability independent of changes in behavior. Proc Natl Acad Sci USA 101: 18223-18227, 2004. (Pubitemid 40054101)
44. Hurd MW, Ralph MR. The significance of circadian organization for longevity in the golden hamster. J Biol Rhythms 13: 430-436, 1998. (Pubitemid 128478940)
45. Iitaka C, Miyazaki K, Akaike T, Ishida N. A role for glycogen synthase kinase-3beta in the mammalian circadian clock. J Biol Chem 280: 29397-29402, 2005. (Pubitemid 41177011)
46. Imai Y, Abe K, Munakata M, Sakuma H, Hashimoto J, Imai K, Sekino H, Yoshinaga K. Circadian blood pressure variations under different pathophysiological conditions. J Hypertens Suppl 8: S125-S132, 1990.
47. James FO, Boivin DB, Charbonneau S, Belanger V, Cermakian N. Expression of clock genes in human peripheral blood mononuclear cells throughout the sleep/wake and circadian cycles. Chronobiol Int 24: 1009-1034, 2007. (Pubitemid 350256125)
48. Jhund PS, Macintyre K, Simpson CR, Lewsey JD, Stewart S, Redpath A, Chalmers JW, Capewell S, McMurray JJ. Long-term trends in first hospitalization for heart failure and subsequent survival between 1986 and 2003: a population study of 5.1 million people. Circulation 119: 515-523, 2009.
49. Kawachi I, Colditz GA, Stampfer MJ, Willett WC, Manson JE, Speizer FE, Hennekens CH. Prospective study of shift work and risk of coronary heart disease in women. Circulation 92: 3178-3182, 1995.
50. Keaney JF Jr, Weaver DR. Vascular rhythms and adaptation: do your arteries know what time it is? Circulation 119: 1463-1466, 2009.
51. Knutsson A, Akerstedt T, Jonsson BG, Orth-Gomer K. Increased risk of ischaemic heart disease in shift workers. Lancet 2: 89-92, 1986. (Pubitemid 16097089)
52. Knutsson AB, Bøggild H. Shift work and cardiovascular disease: review of disease mechanisms. Rev Environ Health 15: 359-372, 2000. (Pubitemid 32039007)
53. Lawton G. Get up and go. New Scientist 189: 34-38, 2006.
54. Leibetseder V, Humpeler S, Svoboda M, Schmid D, Thalhammer T, Zuckermann A, Marktl W, Ekmekcioglu C. Clock genes display rhythmic expression in human hearts. Chronobiol Int 26: 621-636, 2009.
55. Maemura K, de la Monte SM, Chin MT, Layne MD, Hsieh CM, Yet SF, Perrella MA, Lee ME. CLIF, a novel cycle-like factor, regulates the circadian oscillation of plasminogen activator inhibitor-1 gene expression. J Biol Chem 275: 36847-36851, 2000. (Pubitemid 32002096)
56. Martino T, Arab S, Straume M, Belsham DD, Tata N, Cai F, Liu P, Trivieri M, Ralph M, Sole MJ. Day/night rhythms in gene expression of the normal murine heart. J Mol Med 82: 256-264, 2004. (Pubitemid 38553654)
57. Martino TA, Oudit GY, Herzenberg AM, Tata N, Koletar MM, Kabir GM, Belsham DD, Backx PH, Ralph MR, Sole MJ. Circadian rhythm disorganization produces profound cardiovascular and renal disease in hamsters. Am J Physiol Regul Integr Comp Physiol 294: R1675-R1683, 2008.
58. 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. (Pubitemid 351664310)
59. Martino TA, Tata N, Bjarnason GA, Straume M, Sole MJ. Diurnal protein expression in blood revealed by high throughput mass spectrometry proteomics and implications for translational medicine and body time of day. Am J Physiol Regul Integr Comp Physiol 293: R1430-R1437, 2007. (Pubitemid 47364642)
60. McCullough PA, Philbin EF, Spertus JA, Kaatz S, Sandberg KR, Weaver WD. Confirmation of a heart failure epidemic: findings from the Resource Utilization Among Congestive Heart Failure (REACH) study. J Am Coll Cardiol 39: 60-69, 2002. (Pubitemid 34059862)
61. Mendoza J. Circadian clocks: setting time by food. J Neuroendocrinol 19: 127-137, 2007. (Pubitemid 46043835)
62. Mistlberger RE, Skene DJ. Social influences on mammalian circadian rhythms: animal and human studies. Biol Rev Camb Philos Soc 79: 533-556, 2004.
63. Mohri T, Emoto N, Nonaka H, Fukuya H, Yagita K, Okamura H, Yokoyama M. Alterations of circadian expressions of clock genes in Dahl salt-sensitive rats fed a high-salt diet. Hypertension 42: 189-194, 2003. (Pubitemid 36944595)
64. Morgan TO, Aubert JF, Wang Q. Sodium, angiotensin II, blood pressure, and cardiac hypertrophy. Kidney Int Suppl 67: S213-S215, 1998. (Pubitemid 28405721)
65. Morgan TO, Brunner HR, Aubert JF, Wang Q, Griffiths C, Delbridge L. Cardiac hypertrophy depends upon sleep blood pressure: a study in rats. J Hypertens 18: 445-451, 2000. (Pubitemid 30209727)
66. Mukamal KJ, Muller JE, Maclure M, Sherwood JB, Mittleman MA. Increased risk of congestive heart failure among infarctions with nighttime onset. Am Heart J 140: 438-442, 2000. (Pubitemid 30695920)
67. Muller JE, Tofler GH, Stone PH. Circadian variation and triggers of onset of acute cardiovascular disease. Circulation 79: 733-743, 1989.
68. Naito Y, Tsujino T, Fujioka Y, Ohyanagi M, Iwasaki T. Augmented diurnal variations of the cardiac renin-angiotensin system in hypertensive rats. Hypertension 40: 827-833, 2002. (Pubitemid 35434902)
69. Nonaka H, Emoto N, Ikeda K, Fukuya H, Rohman MS, Raharjo SB, Yagita K, Okamura H, Yokoyama M. Angiotensin II induces circadian gene expression of clock genes in cultured vascular smooth muscle cells. Circulation 104: 1746-1748, 2001. (Pubitemid 32963335)
70. Nozue K, Covington MF, Duek PD, Lorrain S, Fankhauser C, Harmer SL, Maloof JN. Rhythmic growth explained by coincidence between internal and external cues. Nature 448: 358-361, 2007. (Pubitemid 47080338)
71. Osiel S, Golombek DA, Ralph MR. Conservation of locomotor behavior in the golden hamster: effects of light cycle and a circadian period mutation. Physiol Behav 65: 123-131, 1998. (Pubitemid 28511424)
72. Otto ME, Svatikova A, Barretto RB, Santos S, Hoffmann M, Khandheria B, Somers V. Early morning attenuation of endothelial function in healthy humans. Circulation 109: 2507-2510, 2004. (Pubitemid 38720548)
73. Pando MP, Sassone-Corsi P. Signaling to the mammalian circadian clocks: in pursuit of the primary mammalian circadian photoreceptor. Sci STKE 2001: RE16, 2001.
74. Papageorgopoulos C, Caldwell K, Schweingrubber H, Neese RA, Shackleton CH, Hellerstein M. Measuring synthesis rates of muscle creatine kinase and myosin with stable isotopes and mass spectrometry. Anal Biochem 309: 1-10, 2002. (Pubitemid 35305783)
75. Paul T, Lemmer B. Disturbance of circadian rhythms in analgosedated intensive care unit patients with and without craniocerebral injury. Chronobiol Int 24: 45-61, 2007. (Pubitemid 46279992)
76. Penev PD, Kolker DE, Zee PC, Turek FW. Chronic circadian desynchronization decreases the survival of animals with cardiomyopathic heart disease. Am J Physiol Heart Circ Physiol 275: H2334-H2337, 1998. (Pubitemid 128731919)
77. Qi L, Boateng SY. The circadian protein Clock localizes to the sarcomeric Z-disk and is a sensor of myofilament cross-bridge activity in cardiac myocytes. Biochem Biophys Res Commun 351: 1054-1059, 2006. (Pubitemid 44715891)
78. Ralph MR, Menaker M. A mutation of the circadian system in golden hamsters. Science 241: 1225-1227, 1988. (Pubitemid 18216005)
79. 3H]leucine in myocardium of the rat. Recent Adv Stud Card Struct Metab 7: 105-110, 1975.
80. Roenneberg T, Merrow M. Timeline: Circadian clocks-the fall and rise of physiology. Nat Rev Mol Cell Biol 6: 965-971, 2005. (Pubitemid 41778715)
81. 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 112: 2716-2724, 2005. (Pubitemid 41532610)
82. Scheer FA, Hilton MF, Mantzoros CS, Shea SA. Adverse metabolic and cardiovascular consequences of circadian misalignment. Proc Natl Acad Sci USA 106: 4453-4458, 2009.
83. Somers VK, White DP, Amin R, Abraham WT, Costa F, Culebras A, Daniels S, Floras JS, Hunt CE, Olson LJ, Pickering TG, Russell R, Woo M, Young T. Sleep apnea and cardiovascular disease: an American Heart Association/American College of Cardiology Foundation Scientific Statement from the American Heart Association Council for High Blood Pressure Research Professional Education Committee, Council on Clinical Cardiology, Stroke Council, and Council on Cardiovascular Nursing. J Am Coll Cardiol 52: 686-717, 2008.
84. Spiegel K, Leproult R, Van Cauter E. Impact of sleep debt on metabolic and endocrine function. Lancet 354: 1435-1439, 1999. (Pubitemid 29494756)
85. Storch KF, Lipan O, Leykin I, Viswanathan N, Davis FC, Wong WH, Weitz CJ. Extensive and divergent circadian gene expression in liver and heart. Nature 417: 78-83, 2002. (Pubitemid 34498819)
86. Stratmann M, Schibler U. Properties, entrainment, and physiological functions of mammalian peripheral oscillators. J Biol Rhythms 21: 494-506, 2006. (Pubitemid 44706830)
87. Su W, Guo Z, Randall DC, Cassis L, Brown DR, Gong MC. Hypertension and disrupted blood pressure circadian rhythm in type 2 diabetic db/db mice. Am J Physiol Heart Circ Physiol 295: H1634-H1641, 2008.
88. Tanaka K, Ashizawa N, Kawano H, Sato O, Seto S, Nishihara E, Terazono H, Isomoto S, Shinohara K, Yano K. Aldosterone induces circadian gene expression of clock genes in H9c2 cardiomyoblasts. Heart Vessels 22: 254-260, 2007. (Pubitemid 47163375)
89. Tata N, Martino T, Vanderlaan R, Dawood F, Khaper N, Liu PP, Husain M, Backx PH, Sole MJ. Chronotherapy: diurnal efficacy of captopril (Abstract). J Cardiac Fail 11: S99, 2005.
90. Verdecchia P, Schillaci G, Guerrieri M, Gatteschi C, Benemio G, Boldrini F, Porcellati C. Circadian blood pressure changes and left ventricular hypertrophy in essential hypertension. Circulation 81: 528-536, 1990. (Pubitemid 20055961)
91. Waldrop RD, Saydjari R, Arnold JR, Ford P, Rubin NH, Poston GJ, Lawrence J, Rayford PL, Townsend CM Jr, Thompson JC. Twenty-four-hour variations in ornithine decarboxylase and acid phosphatase in mice. Proc Soc Exp Biol Med 191: 420-424, 1989. (Pubitemid 19253907)
92. Weinberg EO, Schoen FJ, George D, Kagaya Y, Douglas PS, Litwin SE, Schunkert H, Benedict CR, Lorell BH. Angiotensin-converting enzyme inhibition prolongs survival and modifies the transition to heart failure in rats with pressure overload hypertrophy due to ascending aortic stenosis. Circulation 90: 1410-1422, 1994. (Pubitemid 24284463)
93. Willich SN, Levy D, Rocco MB, Tofler GH, Stone PH, Muller JE. Circadian variation in the incidence of sudden cardiac death in the Framingham Heart Study population. Am J Cardiol 60: 801-806, 1987. (Pubitemid 17163439)
94. Yin L, Wang J, Klein PS, Lazar MA. Nuclear receptor Rev-erbalpha is a critical lithium-sensitive component of the circadian clock. Science 311: 1002-1005, 2006. (Pubitemid 43271727)
95. Young ME. The circadian clock within the heart: potential influence on myocardial gene expression, metabolism, and function. Am J Physiol Heart Circ Physiol 290: H1-H16, 2006.
96. Young ME, Bray MS. Potential role for peripheral circadian clock dyssynchrony in the pathogenesis of cardiovascular dysfunction. Sleep Med 8: 656-667, 2007. (Pubitemid 47181211)
97. Young ME, Razeghi P, Cedars AM, Guthrie PH, Taegtmeyer H. Intrinsic diurnal variations in cardiac metabolism and contractile function. Circ Res 89: 1199-1208, 2001. (Pubitemid 34627879)
98. Young ME, Razeghi P, Taegtmeyer H. Clock genes in the heart: characterization and attenuation with hypertrophy. Circ Res 88: 1142-1150, 2001. (Pubitemid 34132514)
99. Young ME, Wilson CR, Razeghi P, Guthrie PH, Taegtmeyer H. Alterations of the circadian clock in the heart by streptozotocin-induced diabetes. J Mol Cell Cardiol 34: 223-231, 2002. (Pubitemid 35222831)