Muscle-specific RING finger 1 negatively regulates pathological cardiac hypertrophy through downregulation of calcineurin A

Circulation: Heart Failure

Volumn 7, Issue 3, 2014, Pages 479-490

  Maejima, Yasuhiro ^a   Usui, Soichiro ^a,b   Zhai, Peiyong ^a   Takamura, Masayuki ^b   Kaneko, Shuichi ^b   Zablocki, Daniela ^a   Yokota, Mitsuhiro ^c,d   Isobe, Mitsuaki ^d   Sadoshima, Junichi ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^b KANAZAWA UNIVERSITY GRADUATE SCHOOL OF MEDICAL SCIENCE   (Japan)

^c AICHI GAKUIN UNIVERSITY   (Japan)

^d TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

Author keywords

Calcineurin; Cardiomegaly; Muscular atrophy; Ubiquitin protein ligases; Ubiquitination

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; ATRIAL NATRIURETIC FACTOR; CALCINEURIN; CALCINEURIN A; MESSENGER RNA; MUSCLE RING FINGER 1 PROTEIN; TRANSCRIPTION FACTOR NFAT; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; AORTA CONSTRICTION; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; FIBROSIS; HEART LEFT VENTRICLE FAILURE; HEART LEFT VENTRICLE MASS; HEART LEFT VENTRICLE OVERLOAD; HEART MUSCLE CELL; HEART VENTRICLE HYPERTROPHY; HISTOPATHOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; UBIQUITINATION; UPREGULATION;

CALCINEURIN; CARDIOMEGALY; MUSCULAR ATROPHY; UBIQUITIN PROTEIN LIGASES; UBIQUITINATION;

ANIMALS; AORTA; CALCINEURIN; CARDIOMEGALY; DISEASE MODELS, ANIMAL; DOWN-REGULATION; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MUSCLE PROTEINS; MYOCARDIUM; MYOCYTES, CARDIAC; NFATC TRANSCRIPTION FACTORS; SIGNAL TRANSDUCTION; UBIQUITIN-PROTEIN LIGASES;

EID: 84902512348     PISSN: 19413289     EISSN: 19413297     Source Type: Journal    
DOI: 10.1161/CIRCHEARTFAILURE.113.000713     Document Type: Article

References (32)

1. Hill JA, Olson EN. Cardiac plasticity. N Engl J Med. 2008;358:1370-1380.
2. Molkentin JD, Lu JR, Antos CL, Markham B, Richardson J, Robbins J, Grant SR, Olson EN. A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell. 1998;93:215-228.
3. Heineke J, Molkentin JD. Regulation of cardiac hypertrophy by intracellular signalling pathways. Nat Rev Mol Cell Biol. 2006;7:589-600.
4. Oka T, Dai YS, Molkentin JD. Regulation of calcineurin through transcriptional induction of the calcineurin A beta promoter in vitro and in vivo. Mol Cell Biol. 2005;25:6649-6659.
5. Rothermel BA, McKinsey TA, Vega RB, Nicol RL, Mammen P, Yang J, Antos CL, Shelton JM, Bassel-Duby R, Olson EN, Williams RS. Myocyte-enriched calcineurin-interacting protein, MCIP1, inhibits cardiac hypertrophy in vivo. Proc Natl Acad Sci U S A. 2001;98:3328-3333.
6. Heineke J, Auger-Messier M, Correll RN, Xu J, Benard MJ, Yuan W, Drexler H, Parise LV, Molkentin JD. CIB1 is a regulator of pathological cardiac hypertrophy. Nat Med. 2010;16:872-879.
7. Centner T, Yano J, Kimura E, McElhinny AS, Pelin K, Witt CC, Bang ML, Trombitas K, Granzier H, Gregorio CC, Sorimachi H, Labeit S. Identification of muscle specific ring finger proteins as potential regulators of the titin kinase domain. J Mol Biol. 2001;306:717-726.
8. Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, Clarke BA, Poueymirou WT, Panaro FJ, Na E, Dharmarajan K, Pan ZQ, Valenzuela DM, DeChiara TM, Stitt TN, Yancopoulos GD, Glass DJ. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science. 2001;294:1704-1708.
9. Spencer JA, Eliazer S, Ilaria RL Jr, Richardson JA, Olson EN. Regulation of microtubule dynamics and myogenic differentiation by MURF, a striated muscle RING-finger protein. J Cell Biol. 2000;150:771-784.
10. Willis MS, Ike C, Li L, Wang DZ, Glass DJ, Patterson C. Muscle ring finger 1, but not muscle ring finger 2, regulates cardiac hypertrophy in vivo. Circ Res. 2007;100:456-459.
11. Willis MS, Schisler JC, Li L, Rodríguez JE, Hilliard EG, Charles PC, Patterson C. Cardiac muscle ring finger-1 increases susceptibility to heart failure in vivo. Circ Res. 2009;105:80-88.
12. Chen SN, Czernuszewicz G, Tan Y, Lombardi R, Jin J, Willerson JT, Marian AJ. Human molecular genetic and functional studies identify TRIM63, encoding Muscle RING Finger Protein 1, as a novel gene for human hypertrophic cardiomyopathy. Circ Res. 2012;111:907-919.
13. Gelpi RJ, Gao S, Zhai P, Yan L, Hong C, Danridge LM, Ge H, Maejima Y, Donato M, Yokota M, Molkentin JD, Vatner DE, Vatner SF, Sadoshima J. Genetic inhibition of calcineurin induces diastolic dysfunction in mice with chronic pressure overload. Am J Physiol Heart Circ Physiol. 2009;297:H1814-H1819.
14. Jiang J, Ballinger CA, Wu Y, Dai Q, Cyr DM, Höhfeld J, Patterson C. CHIP is a U-box-dependent E3 ubiquitin ligase: identification of Hsc70 as a target for ubiquitylation. J Biol Chem. 2001;276:42938-42944.
15. Christie D. Resampling with Excel. Teaching Statistics. 2004; 26:9-14.
16. Arya R, Kedar V, Hwang JR, McDonough H, Li HH, Taylor J, Patterson C. Muscle ring finger protein-1 inhibits PKC{epsilon} activation and prevents cardiomyocyte hypertrophy. J Cell Biol. 2004;167:1147-1159.
17. Ago T, Liu T, Zhai P, Chen W, Li H, Molkentin JD, Vatner SF, Sadoshima J. A redox-dependent pathway for regulating class II HDACs and cardiac hypertrophy. Cell. 2008;133:978-993.
18. Adams V, Linke A, Wisloff U, Döring C, Erbs S, Kränkel N, Witt CC, Labeit S, Müller-Werdan U, Schuler G, Hambrecht R. Myocardial expression of Murf-1 and MAFbx after induction of chronic heart failure: Effect on myocardial contractility. Cardiovasc Res. 2007;73:120-129.
19. Donaldson C, Eder S, Baker C, Aronovitz MJ, Weiss AD, Hall-Porter M, Wang F, Ackerman A, Karas RH, Molkentin JD, Patten RD. Estrogen attenuates left ventricular and cardiomyocyte hypertrophy by an estrogen receptor-dependent pathway that increases calcineurin degradation. Circ Res. 2009;104:265-275.
20. Cai D, Frantz JD, Tawa NE Jr, Melendez PA, Oh BC, Lidov HG, Hasselgren PO, Frontera WR, Lee J, Glass DJ, Shoelson SE. IKKbeta/ NF-kappaB activation causes severe muscle wasting in mice. Cell. 2004;119:285-298.
21. Sandri M, Lin J, Handschin C, Yang W, Arany ZP, Lecker SH, Goldberg AL, Spiegelman BM. PGC-1alpha protects skeletal muscle from atrophy by suppressing FoxO3 action and atrophy-specific gene transcription. Proc Natl Acad Sci U S A. 2006;103:16260-16265.
22. Li HH, Willis MS, Lockyer P, Miller N, McDonough H, Glass DJ, Patterson C. Atrogin-1 inhibits Akt-dependent cardiac hypertrophy in mice via ubiquitin-dependent coactivation of Forkhead proteins. J Clin Invest. 2007;117:3211-3223.
23. Wilkins BJ, Dai YS, Bueno OF, Parsons SA, Xu J, Plank DM, Jones F, Kimball TR, Molkentin JD. Calcineurin/NFAT coupling participates in pathological, but not physiological, cardiac hypertrophy. Circ Res. 2004;94:110-118.
24. Kingsbury TJ, Cunningham KW. A conserved family of calcineurin regulators. Genes Dev. 2000;14:1595-1604.
25. Li HH, Kedar V, Zhang C, McDonough H, Arya R, Wang DZ, Patterson C. Atrogin-1/muscle atrophy F-box inhibits calcineurin-dependent cardiac hypertrophy by participating in an SCF ubiquitin ligase complex. J Clin Invest. 2004;114:1058-1071.
26. Usui S, Maejima Y, Pain J, Hong C, Cho J, Park JY, Zablocki D, Tian B, Glass DJ, Sadoshima J. Endogenous muscle atrophy F-box mediates pressure overload-induced cardiac hypertrophy through regulation of nuclear factor-kappaB. Circ Res. 2011;109:161-171.
27. Frey N, McKinsey TA, Olson EN. Decoding calcium signals involved in cardiac growth and function. Nat Med. 2000;6:1221-1227.
28. Moriscot AS, Baptista IL, Bogomolovas J, Witt C, Hirner S, Granzier H, Labeit S. MuRF1 is a muscle fiber-type II associated factor and together with MuRF2 regulates type-II fiber trophicity and maintenance. J Struct Biol. 2010;170:344-353.
29. McElhinny AS, Kakinuma K, Sorimachi H, Labeit S, Gregorio CC. Muscle-specific RING finger-1 interacts with titin to regulate sarcomeric M-line and thick filament structure and may have nuclear functions via its interaction with glucocorticoid modulatory element binding protein- 1. J Cell Biol. 2002;157:125-136.
30. Clarke BA, Drujan D, Willis MS, Murphy LO, Corpina RA, Burova E, Rakhilin SV, Stitt TN, Patterson C, Latres E, Glass DJ. The E3 Ligase MuRF1 degrades myosin heavy chain protein in dexamethasone-treated skeletal muscle. Cell Metab. 2007;6:376-385.
31. Kedar V, McDonough H, Arya R, Li HH, Rockman HA, Patterson C. Muscle-specific RING finger 1 is a bona fide ubiquitin ligase that degrades cardiac troponin I. Proc Natl Acad Sci U S A. 2004;101:18135-18140.
32. Mearini G, Gedicke C, Schlossarek S, Witt CC, Krämer E, Cao P, Gomes MD, Lecker SH, Labeit S, Willis MS, Eschenhagen T, Carrier L. Atrogin-1 and MuRF1 regulate cardiac MyBP-C levels via different mechanisms. Cardiovasc Res. 2010;85:357-366.