Development of dilated cardiomyopathy in Bmal1-deficient mice

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 303, Issue 4, 2012, Pages

  Lefta, Mellani ^a,b   Campbell, Kenneth S ^a,b   Feng, Han Zhong ^c   Jin, Jian Ping ^c   Esser, Karyn A ^a,b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Mechanical stiffness; Myosin heavy chain; Systolic dysfunction; Titin isoforms

Indexed keywords

MYOSIN HEAVY CHAIN; PROTEIN BMAL1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONGESTIVE CARDIOMYOPATHY; DISEASE COURSE; DOWN REGULATION; EX VIVO STUDY; HEART MUSCLE CELL; HEART PERFORMANCE; HEART VENTRICLE FUNCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SARCOMERE;

AGE FACTORS; AGING; ANIMALS; ARNTL TRANSCRIPTION FACTORS; CARDIOMYOPATHY, DILATED; DISEASE PROGRESSION; GENE EXPRESSION REGULATION; HEART FAILURE; HYPERTROPHY, LEFT VENTRICULAR; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE PROTEINS; MYOCARDIAL CONTRACTION; MYOCARDIUM; MYOSIN HEAVY CHAINS; PROTEIN KINASES; RNA, MESSENGER; SARCOMERES; STROKE VOLUME; VENTRICULAR DYSFUNCTION, LEFT; VENTRICULAR FUNCTION, LEFT; VENTRICULAR PRESSURE;

EID: 84865146628     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00238.2012     Document Type: Article

References (68)

1. Alvarez JD, Hansen A, Ord T, Bebas P, Chappell PE, Giebultowicz JM, Williams C, Moss S, Sehgal A. The circadian clock protein BMAL1 is necessary for fertility and proper testosterone production in mice. J Biol Rhythms 23: 26-36, 2008.
2. Andrews JL, Zhang X, McCarthy JJ, McDearmon EL, Hornberger TA, Russell B, Campbell KS, Arbogast S, Reid MB, Walker JR, Hogenesch JB, Takahashi JS, Esser KA. CLOCK and BMAL1 regulate MyoD and are necessary for maintenance of skeletal muscle phenotype and function. Proc Natl Acad Sci USA 107: 19090-19095, 2010.
3. Aschoff J. Human circadian rhythms in activity, body temperature and other functions. Life Sci Space Res 5: 159-173, 1967.
4. Bell SP, Nyland L, Tischler MD, McNabb M, Granzier H, LeWinter MM. Alterations in the determinants of diastolic suction during pacing tachycardia. Circ Res 87: 235-240, 2000.
5. Boateng SY, Goldspink PH. Assembly and maintenance of the sarcomere night and day. Cardiovasc Res 77: 667-675, 2008.
6. Bunger MK, Walisser JA, Sullivan R, Manley PA, Moran SM, Kalscheur VL, Colman RJ, Bradfield CA. Progressive arthropathy in mice with a targeted disruption of the Mop3/Bmal-1 locus. Genesis 41: 122-132, 2005.
7. 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.
8. Campbell KS, Moss RL. SLControl: PC-based data acquisition and analysis for muscle mechanics. Am J Physiol Heart Circ Physiol 285: H2857-H2864, 2003.
9. Cazorla O, Freiburg A, Helmes M, Centner T, McNabb M, Wu Y, Trombitas K, Labeit S, Granzier H. Differential expression of cardiac titin isoforms and modulation of cellular stiffness. Circ Res 86: 59-67, 2000.
10. Collins TJ. ImageJ for microscopy. Biotechniques 43: 25-30, 2007.
11. Coughlin SS, Tefft MC, Rice JC, Gerone JL, Baughman KL. Epidemiology of idiopathic dilated cardiomyopathy in the elderly: pooled results from two case-control studies. Am J Epidemiol 143: 881-888, 1996.
12. Curtis AM, Cheng Y, Kapoor S, Reilly D, Price TS, Fitzgerald GA. Circadian variation of blood pressure and the vascular response to asynchronous stress. Proc Natl Acad Sci USA 104: 3450-3455, 2007.
13. Durgan DJ, Tsai JY, Grenett MH, Pat BM, Ratcliffe WF, Villegas-Montoya C, Garvey ME, Nagendran J, Dyck JR, Bray MS, Gamble KL, Gimble JM, Young ME. Evidence suggesting that the cardiomyocyte circadian clock modulates responsiveness of the heart to hypertrophic stimuli in mice. Chronobiol Int 28: 187-203, 2011.
14. Eisenberg BR. Adaptability of ultrastructure in the mammalian muscle. J Exp Biol 115: 55-68, 1985.
15. Feldman MD, Alderman JD, Aroesty JM, Royal HD, Ferguson JJ, Owen RM, Grossman W, McKay RG. Depression of systolic and diastolic myocardial reserve during atrial pacing tachycardia in patients with dilated cardiomyopathy. J Clin Invest 82: 1661-1669, 1988.
16. Feng HZ, Biesiadecki BJ, Yu ZB, Hossain MM, Jin JP. Restricted N-terminal truncation of cardiac troponin T: a novel mechanism for functional adaptation to energetic crisis. J Physiol 586: 3537-3550, 2008.
17. Ferreira LF, Moylan JS, Stasko S, Smith JD, Campbell KS, Reid MB. Sphingomyelinase depresses force and calcium sensitivity of the contractile apparatus in mouse diaphragm muscle fibers. J Appl Physiol 112: 1538-1545, 2012.
18. Frank D, Kuhn C, Katus HA, Frey N. The sarcomeric Z-disc: a nodal point in signalling and disease. J Mol Med 84: 446-468, 2006.
19. Fukuda N, Wu Y, Nair P, Granzier HL. Phosphorylation of titin modulates passive stiffness of cardiac muscle in a titin isoform-dependent manner. J Gen Physiol 125: 257-271, 2005.
20. Fuller GA, Bicer S, Hamlin RL, Yamaguchi M, Reiser PJ. Increased myosin heavy chain-beta with atrial expression of ventricular light chain-2 in canine cardiomyopathy. J Card Fail 13: 680-686, 2007.
21. Gekakis N, Staknis D, Nguyen HB, Davis FC, Wilsbacher LD, King DP, Takahashi JS, Weitz CJ. Role of the CLOCK protein in the mammalian circadian mechanism. Science 280: 1564-1569, 1998.
22. Gentry-Smetana S, Redford D, Moore D, Larson DF. Direct effects of volatile anesthetics on cardiac function. Perfusion 23: 43-47, 2008.
23. Granzier H, Wu Y, Siegfried L, LeWinter M. Titin: physiological function and role in cardiomyopathy and failure. Heart Fail Rev 10: 211-223, 2005.
24. Granzier HL, Irving TC. Passive tension in cardiac muscle: contribution of collagen, titin, microtubules, and intermediate filaments. Biophys J 68: 1027-1044, 1995.
25. Gregorio CC, Granzier H, Sorimachi H, Labeit S. Muscle assembly: a titanic achievement? Curr Opin Cell Biol 11: 18-25, 1999.
26. Grundschober C, Delaunay F, Puhlhofer A, Triqueneaux G, Laudet V, Bartfai T, Nef P. Circadian regulation of diverse gene products revealed by mRNA expression profiling of synchronized fibroblasts. J Biol Chem 276: 46751-46758, 2001.
27. Ha M, Park J. Shiftwork and metabolic risk factors of cardiovascular disease. J Occup Health 47: 89-95, 2005.
28. Haddad F, Qin AX, Bodell PW, Zhang LY, Guo H, Giger JM, Baldwin KM. Regulation of antisense RNA expression during cardiac MHC gene switching in response to pressure overload. Am J Physiol Heart Circ Physiol 290: H2351-H2361, 2006.
29. Harding P, Yang XP, Yang J, Shesely E, He Q, LaPointe MC. Gene expression profiling of dilated cardiomyopathy in older male EP4 knockout mice. Am J Physiol Heart Circ Physiol 298: H623-H632, 2010.
30. Hasenfuss G, Mulieri LA, Leavitt BJ, Allen PD, Haeberle JR, Alpert NR. Alteration of contractile function and excitation-contraction coupling in dilated cardiomyopathy. Circ Res 70: 1225-1232, 1992.
31. James J, Martin L, Krenz M, Quatman C, Jones F, Klevitsky R, Gulick J, Robbins J. Forced expression of alpha-myosin heavy chain in the rabbit ventricle results in cardioprotection under cardiomyopathic conditions. Circulation 111: 2339-2346, 2005.
32. Knutsson A. Health disorders of shift workers. Occup Med (Lond) 53: 103-108, 2003.
33. Koller M. Health risks related to shift work. An example of timecontingent effects of long-term stress. Int Arch Occup Environ Health 53: 59-75, 1983.
34. Kondratov RV, Kondratova AA, Gorbacheva VY, Vykhovanets OV, Antoch MP. Early aging and age-related pathologies in mice deficient in BMAL1, the core component of the circadian clock. Genes Dev 20: 1868-1873, 2006.
35. Kruger M, Kotter S, Grutzner A, Lang P, Andresen C, Redfield MM, Butt E, dos Remedios CG, Linke WA. Protein kinase G modulates human myocardial passive stiffness by phosphorylation of the titin springs. Circ Res 104: 87-94, 2009.
36. Kruger M, Linke WA. Protein kinase-A phosphorylates titin in human heart muscle and reduces myofibrillar passive tension. J Muscle Res Cell Motil 27: 435-444, 2006.
37. Laposky A, Easton A, Dugovic C, Walisser J, Bradfield C, Turek F. Deletion of the mammalian circadian clock gene BMAL1/Mop3 alters baseline sleep architecture and the response to sleep deprivation. Sleep 28: 395-409, 2005.
38. Lefta M, Wolff G, Esser KA. Circadian rhythms, the molecular clock, and skeletal muscle. Curr Top Dev Biol 96: 231-271, 2011.
39. McCarthy JJ, Andrews JL, McDearmon EL, Campbell KS, Barber BK, Miller BH, Walker JR, Hogenesch JB, Takahashi JS, Esser KA. Identification of the circadian transcriptome in adult mouse skeletal muscle. Physiol Genomics 31: 86-95, 2007.
40. McConnell BK, Jones KA, Fatkin D, Arroyo LH, Lee RT, Aristizabal O, Turnbull DH, Georgakopoulos D, Kass D, Bond M, Niimura H, Schoen FJ, Conner D, Fischman DA, Seidman CE, Seidman JG. Dilated cardiomyopathy in homozygous myosin-binding protein-C mutant mice. J Clin Invest 104: 1235-1244, 1999.
41. Meyer M, Trost SU, Bluhm WF, Knot HJ, Swanson E, Dillmann WH. Impaired sarcoplasmic reticulum function leads to contractile dysfunction and cardiac hypertrophy. Am J Physiol Heart Circ Physiol 280: H2046-H2052, 2001.
42. Mosendane T, Raal FJ. Shift work and its effects on the cardiovascular system. Cardiovasc J Afr 19: 210-215, 2008.
43. Motulsky H. Fitting Models to Biological Data Using Linear and Non-Linear Regression. A Practical Guide to Curve Fitting. Oxford, UK: Oxford University Press, 2004.
44. Nagueh SF, Shah G, Wu Y, Torre-Amione G, King NM, Lahmers S, Witt CC, Becker K, Labeit S, Granzier HL. Altered titin expression, myocardial stiffness, and left ventricular function in patients with dilated cardiomyopathy. Circulation 110: 155-162, 2004.
45. Neagoe C, Opitz CA, Makarenko I, Linke WA. Gigantic variety: expression patterns of titin isoforms in striated muscles and consequences for myofibrillar passive stiffness. J Muscle Res Cell Motil 24: 175-189, 2003.
46. O'Connell TD, Rodrigo MC, Simpson PC. Isolation and culture of adult mouse cardiac myocytes. Methods Mol Biol 357: 271-296, 2007.
47. Oparil S, Bishop SP, Clubb FJ Jr. Myocardial cell hypertrophy or hyperplasia. Hypertension 6: III38-III43, 1984.
48. Opitz CA, Linke WA. Plasticity of cardiac titin/connectin in heart development. J Muscle Res Cell Motil 26: 333-342, 2005.
49. 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 109: 307-320, 2002.
50. Reiser PJ, Kline WO. Electrophoretic separation and quantitation of cardiac myosin heavy chain isoforms in eight mammalian species. Am J Physiol Heart Circ Physiol 274: H1048-H1053, 1998.
51. Roth DM, Swaney JS, Dalton ND, Gilpin EA, Ross J Jr. Impact of anesthesia on cardiac function during echocardiography in mice. Am J Physiol Heart Circ Physiol 282: H2134-H2140, 2002.
52. Rudic RD, McNamara P, Curtis AM, Boston RC, Panda S, Hogenesch JB, Fitzgerald GA. BMAL1 and CLOCK, two essential components of the circadian clock, are involved in glucose homeostasis. PLoS Biol 2: e377, 2004.
53. Schonberger J, Seidman CE. Many roads lead to a broken heart: the genetics of dilated cardiomyopathy. Am J Hum Genet 69: 249-260, 2001.
54. Seidman JG, Seidman C. The genetic basis for cardiomyopathy: from mutation identification to mechanistic paradigms. Cell 104: 557-567, 2001.
55. 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.
56. Sun Y, Yang Z, Niu Z, Wang W, Peng J, Li Q, Ma MY, Zhao Y. The mortality of MOP3 deficient mice with a systemic functional failure. J Biomed Sci 13: 845-851, 2006.
57. Swinnen M, Vanhoutte D, Van Almen GC, Hamdani N, Schellings MW, D'Hooge J, Van der Velden J, Weaver MS, Sage EH, Bornstein P, Verheyen FK, VandenDriessche T, Chuah MK, Westermann D, Paulus WJ, Van de Werf F, Schroen B, Carmeliet P, Pinto YM, Heymans S. Absence of thrombospondin-2 causes age-related dilated cardiomyopathy. Circulation 120: 1585-1597, 2009.
58. Talmadge RJ, Roy RR. Electrophoretic separation of rat skeletal muscle myosin heavy-chain isoforms. J Appl Physiol 75: 2337-2340, 1993.
59. Tardiff JC, Hewett TE, Factor SM, Vikstrom KL, Robbins J, Leinwand LA. Expression of the beta (slow)-isoform of MHC in the adult mouse heart causes dominant-negative functional effects. Am J Physiol Heart Circ Physiol 278: H412-H419, 2000.
60. Towbin JA, Bowles NE. The failing heart. Nature 415: 227-233, 2002.
61. Vitaterna MH, King DP, Chang AM, Kornhauser JM, Lowrey PL, McDonald JD, Dove WF, Pinto LH, Turek FW, Takahashi JS. Mutagenesis and mapping of a mouse gene, Clock, essential for circadian behavior. Science 264: 719-725, 1994.
62. Warren CM, Krzesinski PR, Campbell KS, Moss RL, Greaser ML. Titin isoform changes in rat myocardium during development. Mech Dev 121: 1301-1312, 2004.
63. Warren CM, Krzesinski PR, Greaser ML. Vertical agarose gel electrophoresis and electroblotting of high-molecular-weight proteins. Electrophoresis 24: 1695-1702, 2003.
64. Wu J, Bu L, Gong H, Jiang G, Li L, Ma H, Zhou N, Lin L, Chen Z, Ye Y, Niu Y, Sun A, Ge J, Zou Y. Effects of heart rate and anesthetic timing on high-resolution echocardiographic assessment under isoflurane anesthesia in mice. J Ultrasound Med 29: 1771-1778, 2010.
65. Wu Y, Bell SP, Trombitas K, Witt CC, Labeit S, LeWinter MM, Granzier H. Changes in titin isoform expression in pacing-induced cardiac failure give rise to increased passive muscle stiffness. Circulation 106: 1384-1389, 2002.
66. Zakhary DR, Moravec CS, Stewart RW, Bond M. Protein kinase A (PKA)-dependent troponin-I phosphorylation and PKA regulatory subunits are decreased in human dilated cardiomyopathy. Circulation 99: 505-510, 1999.
67. Zhang EE, Kay SA. Clocks not winding down: unravelling circadian networks. Nat Rev Mol Cell Biol 11: 764-776, 2010.
68. Zhou YY, Wang SQ, Zhu WZ, Chruscinski A, Kobilka BK, Ziman B, Wang S, Lakatta EG, Cheng H, Xiao RP. Culture and adenoviral infection of adult mouse cardiac myocytes: methods for cellular genetic physiology. Am J Physiol Heart Circ Physiol 279: H429-H436, 2000.