Rare variants in genes encoding MuRF1 and MuRF2 are modifiers of hypertrophic cardiomyopathy

International Journal of Molecular Sciences

Volumn 15, Issue 6, 2014, Pages 9302-9313

  Su, Ming ^a   Wang, Jizheng ^a   Kang, Lianming ^a   Wang, Yilu ^b   Zou, Yubao ^a   Feng, Xinxing ^a   Wang, Dong ^a   Ahmad, Ferhaan ^c   Zhou, Xianliang ^a   Hui, Rutai ^a   Song, Lei ^a  

^a FUWAI HOSPITAL   (China)

^b Emergency Department   (China)

^c UNIVERSITY OF IOWA   (United States)

Author keywords

Hypertrophic cardiomyopathy; Modifier; Muscle ring finger protein; Rare variant

Indexed keywords

ADULT; ARTICLE; CAPILLARY SANGER SEQUENCING; CONTROLLED STUDY; DNA SEQUENCE; FEMALE; GENE; GENETIC ASSOCIATION; GENETIC VARIABILITY; HEART VENTRICLE HYPERTROPHY; HUMAN; HYPERTROPHIC CARDIOMYOPATHY; MAJOR CLINICAL STUDY; MALE; MISSENSE MUTATION; MUSCLE RING FINGER 1 GENE; MUSCLE RING FINGER 2 GENE; NONSENSE MUTATION; NUCLEOTIDE SEQUENCE; PREVALENCE; PROTEIN DEGRADATION; SARCOMERE; SINGLE NUCLEOTIDE POLYMORPHISM; GENETICS; HEART MUSCLE; METABOLISM; MIDDLE AGED; MUTATION; PATHOLOGY;

MUSCLE PROTEIN; TRIM63 PROTEIN, HUMAN; UBIQUITIN PROTEIN LIGASE;

ADULT; CARDIOMYOPATHY, HYPERTROPHIC; FEMALE; GENETIC VARIATION; HUMANS; MALE; MIDDLE AGED; MUSCLE PROTEINS; MUTATION; MYOCARDIUM; UBIQUITIN-PROTEIN LIGASES;

EID: 84901400963     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms15069302     Document Type: Article

References (35)

1. Gersh, B.J.; Maron, B.J.; Bonow, R.O.; Dearani, J.A.; Fifer, M.A.; Link, M.S.; Naidu, S.S.; Nishimura, R.A.; Ommen, S.R.; Rakowski, H.; et al. 2011 ACCF/AHA guideline for the diagnosis and treatment of hypertrophic cardiomyopathy. Circulation 2011, 124, 2761-2796.
2. Maron, B.J.; Gardin, J.M.; Flack, J.M.; Gidding, S.S.; Kurosaki, T.T.; Bild, D.E. Prevalence of hypertrophic cardiomyopathy in a general population of young adults. Echocardiographic analysis of 4111 subjects in the CARDIA Study. Coronary artery risk development in (young) adults. Circulation 1995, 92, 785-789.
3. Zou, Y.; Song, L.; Wang, Z.; Ma, A.; Liu, T.; Gu, H.; Lu, S.; Wu, P.; Zhang, Y.; Shen, L.; et al. Prevalence of idiopathic hypertrophic cardiomyopathy in China: A population-based echocardiographic analysis of 8080 adults. Am. J. Med. 2004, 116, 14-18.
4. Maron, B.J.; Maron, M.S.; Semsarian, C. Genetics of hypertrophic cardiomyopathy after 20 years: Clinical perspectives. J. Am. Coll. Cardiol. 2012, 60, 705-715.
5. Maron, B.J.; Maron, M.S. Hypertrophic cardiomyopathy. Lancet 2013, 381, 242-255.
6. Seidman, C.E.; Seidman, J.G. Identifying sarcomere gene mutations in hypertrophic cardiomyopathy: A personal history. Circ. Res. 2011, 108, 743-750.
7. Maron, B.J. Hypertrophic cardiomyopathy: A systematic review. JAMA 2002, 287, 1308-1320.
8. Page, S.P.; Kounas, S.; Syrris, P.; Christiansen, M.; Frank-Hansen, R.; Andersen, P.S.; Elliott, P.M.; McKenna, W.J. Cardiac myosin binding protein-C mutations in families with hypertrophic cardiomyopathy: Disease expression in relation to age, gender, and long term outcome. Circulation 2012, 5, 156-166.
9. Pagan, J.; Seto, T.; Pagano, M.; Cittadini, A. Role of the ubiquitin proteasome system in the heart. Circ. Res. 2013, 112, 1046-1058.
10. Calise, J.; Powell, S.R. The ubiquitin proteasome system and myocardial ischemia. Am. J. Physiol. 2013, 304, H337-H349.
11. Schlossarek, S.; Englmann, D.R.; Sultan, K.R.; Sauer, M.; Eschenhagen, T.; Carrier, L. Defective proteolytic systems in Mybpc3-targeted mice with cardiac hypertrophy. Basic Res. Cardiol. 2012, 107, 235.
12. Schlossarek, S.; Schuermann, F.; Geertz, B.; Mearini, G.; Eschenhagen, T.; Carrier, L. Adrenergic stress reveals septal hypertrophy and proteasome impairment in heterozygous Mybpc3-targeted knock-in mice. J. Muscle Res. Cell Motil. 2012, 33, 5-15.
13. Bahrudin, U.; Morikawa, K.; Takeuchi, A.; Kurata, Y.; Miake, J.; Mizuta, E.; Adachi, K.; Higaki, K.; Yamamoto, Y.; Shirayoshi, Y.; et al. Impairment of ubiquitin-proteasome system by E334K cMyBPC modifies channel proteins, leading to electrophysiological dysfunction. J. Mol. Biol. 2011, 413, 857-878.
14. Glass, D.J. Signalling pathways that mediate skeletal muscle hypertrophy and atrophy. Nat. Cell Biol. 2003, 5, 87-90.
15. Spencer, J.A.; Eliazer, S.; Ilaria, R.L., Jr.; Richardson, J.A.; Olson, E.N. Regulation of microtubule dynamics and myogenic differentiation by MURF, a striated muscle RING-finger protein. J. Cell Biol. 2000, 150, 771-784.
16. Arya, R.; Kedar, V.; Hwang, J.R.; McDonough, H.; Li, H.H.; Taylor, J.; Patterson, C. Muscle ring finger protein-1 inhibits PKC activation and prevents cardiomyocyte hypertrophy. J. Cell Biol. 2004, 167, 1147-1159.
17. Kedar, V.; McDonough, H.; Arya, R.; Li, H.H.; Rockman, H.A.; Patterson, C. Muscle-specific ring finger 1 is a bona fide ubiquitin ligase that degrades cardiac troponin I. Proc. Natl. Acad. Sci. USA 2004, 101, 18135-18140.
18. Witt, S.H.; Granzier, H.; Witt, C.C.; Labeit, S. MURF-1 and MURF-2 target a specific subset of myofibrillar proteins redundantly: Towards understanding MURF-dependent muscle ubiquitination. J. Mol. Biol. 2005, 350, 713-722.
19. Willis, M.S.; Ike, C.; Li, L.; Wang, D.Z.; Glass, D.J.; Patterson, C. Muscle ring finger 1, but not muscle RING finger 2, regulates cardiac hypertrophy in vivo. Circ. Res. 2007, 100, 456-459.
20. Fielitz, J.; van Rooij, E.; Spencer, J.A.; Shelton, J.M.; Latif, S.; van der Nagel, R.; Bezprozvannaya, S.; de Windt, L.; Richardson, J.A.; Bassel-Duby, R.; et al. Loss of muscle-specific RING-finger 3 predisposes the heart to cardiac rupture after myocardial infarction. Proc. Natl. Acad. Sci. USA 2007, 104, 4377-4382.
21. Fielitz, J.; Kim, M.S.; Shelton, J.M.; Latif, S.; Spencer, J.A.; Glass, D.J.; Richardson, J.A.; Bassel-Duby, R.; Olson, E.N. Myosin accumulation and striated muscle myopathy result from the loss of muscle RING finger 1 and 3. J. Clin. Investig. 2007, 117, 2486-2495.
22. Willis, M.S.; Schisler, J.C.; Li, L.; Rodriguez, J.E.; Hilliard, E.G.; Charles, P.C.; Patterson, C. Cardiac muscle RING finger-1 increases susceptibility to heart failure in vivo. Circ. Res. 2009, 105, 80-88.
23. Li, H.H.; Du, J.; Fan, Y.N.; Zhang, M.L.; Liu, D.P.; Li, L.; Lockyer, P.; Kang, E.Y.; Patterson, C.; Willis, M.S. The ubiquitin ligase MuRF1 protects against cardiac ischemia/reperfusion injury by its proteasome-dependent degradation of phospho-c-Jun. Am. J. Pathol. 2011, 178, 1043-1058.
24. Chen, S.N.; Czernuszewicz, G.; Tan, Y.; Lombardi, R.; Jin, J.; Willerson, J.T.; Marian, A.J. 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.
25. Yang, J.; Zhao, Y.; Hao, P.; Meng, X.; Dong, M.; Wang, Y.; Zhang, Y.; Zhang, C. Impact of angiotensin I converting enzyme insertion/deletion polymorphisms on dilated cardiomyopathy and hypertrophic cardiomyopathy risk. PLoS One 2013, 8, e63309.
26. Kolder, I.C.; Michels, M.; Christiaans, I.; Ten Cate, F.J.; Majoor-Krakauer, D.; Danser, A.H.; Lekanne Deprez, R.H.; Tanck, M.; Wilde, A.A.; Bezzina, C.R.; et al. The role of renin-angiotensin-aldosterone system polymorphisms in phenotypic expression of MYBPC3-related hypertrophic cardiomyopathy. Eur. J. Hum. Genet. 2012, 20, 1071-1077.
27. Friedrich, F.W.; Bausero, P.; Sun, Y.; Treszl, A.; Kramer, E.; Juhr, D.; Richard, P.; Wegscheider, K.; Schwartz, K.; Brito, D.; et al. A new polymorphism in human calmodulin III gene promoter is a potential modifier gene for familial hypertrophic cardiomyopathy. Eur. Heart J. 2009, 30, 1648-1655.
28. Predmore, J.M.; Wang, P.; Davis, F.; Bartolone, S.; Westfall, M.V.; Dyke, D.B.; Pagani, F.; Powell, S.R.; Day, S.M. Ubiquitin proteasome dysfunction in human hypertrophic and dilated cardiomyopathies. Circulation 2010, 121, 997-1004.
29. Bahrudin, U.; Morisaki, H.; Morisaki, T.; Ninomiya, H.; Higaki, K.; Nanba, E.; Igawa, O.; Takashima, S.; Mizuta, E.; Miake, J.; et al. Ubiquitin-proteasome system impairment caused by a missense cardiac myosin-binding protein C mutation and associated with cardiac dysfunction in hypertrophic cardiomyopathy. J. Mol. Biol. 2008, 384, 896-907.
30. Vignier, N.; Schlossarek, S.; Fraysse, B.; Mearini, G.; Kramer, E.; Pointu, H.; Mougenot, N.; Guiard, J.; Reimer, R.; Hohenberg, H.; et al. Nonsense-mediated mRNA decay and ubiquitin-proteasome system regulate cardiac myosin-binding protein C mutant levels in cardiomyopathic mice. Circ. Res. 2009, 105, 239-248.
31. Willis, M.S.; Wadosky, K.M.; Rodriguez, J.E.; Schisler, J.C.; Lockyer, P.; Hilliard, E.G.; Glass, D.J.; Patterson, C. Muscle RING finger 1 and muscle ring finger 2 are necessary but functionally redundant during developmental cardiac growth and regulate E2F1-mediated gene expression in vivo. Cell Biochem. Funct. 2014, 32, 39-50.
32. Witt, C.C.; Witt, S.H.; Lerche, S.; Labeit, D.; Back, W.; Labeit, S. Cooperative control of striated muscle mass and metabolism by MuRF1 and MuRF2. EMBO J. 2008, 27, 350-360.
33. Ploski, R.; Pollak, A.; Muller, S.; Franaszczyk, M.; Michalak, E.; Kosinska, J.; Stawinski, P.; Spiewak, M.; Seggewiss, H.; Bilinska, Z.T. Does p. Q247X in TRIM63 cause human hypertrophic cardiomyopathy? Circ. Res. 2014, 114, e2-e5.
34. Adzhubei, I.A.; Schmidt, S.; Peshkin, L.; Ramensky, V.E.; Gerasimova, A.; Bork, P.; Kondrashov, A.S.; Sunyaev, S.R. A method and server for predicting damaging missense mutations. Nat. Methods 2010, 7, 248-249.
35. Kumar, P.; Henikoff, S.; Ng, P.C. Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat. Protoc. 2009, 4, 1073-1081.