Lysine methyltransferase Smyd2 regulates Hsp90-mediated protection of the sarcomeric titin springs and cardiac function

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 4, 2013, Pages 812-822

  Voelkel, Tobias ^a   Andresen, Christian ^a,b   Unger, Andreas ^a   Just, Steffen ^c   Rottbauer, Wolfgang ^c   Linke, Wolfgang A ^a,d  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b UNIVERSITY HOSPITAL DÜSSELDORF   (Germany)

^c UNIVERSITY HOSPITAL ULM   (Germany)

^d UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

Author keywords

Hsp90; Protein methylation; Protein quality control; Sarcomere; Titin

Indexed keywords

CONNECTIN; HEAT SHOCK PROTEIN 90; HISTONE LYSINE METHYLTRANSFERASE; SMYD2 PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CYTOPLASM; HEART FUNCTION; HEART MUSCLE CELL; HEART PERFORMANCE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT;

ACTININ; ANIMALS; ANIMALS, NEWBORN; CELL NUCLEUS; CHICK EMBRYO; CYTOPLASM; DNA-BINDING PROTEINS; HISTONE-LYSINE N-METHYLTRANSFERASE; HSP90 HEAT-SHOCK PROTEINS; LYSINE; MICE; MODELS, MOLECULAR; MUSCLE PROTEINS; MYOCARDIUM; MYOCYTES, CARDIAC; PROTEIN BINDING; PROTEIN KINASES; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; RATS; SARCOMERES; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

DANIO RERIO;

EID: 84875071253     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2012.09.012     Document Type: Article

References (52)

1. Portbury A.L., Willis M.S., Patterson C. Tearin' up my heart: proteolysis in the cardiac sarcomere. J. Biol. Chem. 2011, 286:9929-9934.
2. Hartl F.U., Bracher A., Hayer-Hartl M. Molecular chaperones in protein folding and proteostasis. Nature 2011, 475:324-332.
3. Willis M.S., Schisler J.C., Portbury A.L., Patterson C. Build it up-tear it down: protein quality control in the cardiac sarcomere. Cardiovasc. Res. 2009, 81:439-448.
4. Christians E.S., Benjamin I.J. Proteostasis and REDOX state in the heart. Am. J. Physiol. Heart Circ. Physiol. 2012, 302:H24-H37.
5. Krüger M., Linke W.A. The giant protein titin: a regulatory node that integrates myocyte signaling pathways. J. Biol. Chem. 2011, 286:9905-9912.
6. Barral J.M., Hutagalung A.H., Brinker A., Hartl F.U., Epstein H.F. Role of the myosin assembly protein UNC-45 as a molecular chaperone for myosin. Science 2012, 295:669-671.
7. Srikakulam R., Liu L., Winkelmann D.A. Unc45b forms a cytosolic complex with Hsp90 and targets the unfolded myosin motor domain. PLoS One 2008, 3:e2137.
8. Bernick E.P., Zhang P.J., Du S. Knockdown and overexpression of Unc-45b result in defective myofibril organization in skeletal muscles of zebrafish embryos. BMC Cell Biol. 2010, 11:70.
9. Etard C., Roostalu U., Strähle U. Shuttling of the chaperones Unc45b and Hsp90a between the A band and the Z line of the myofibril. J. Cell Biol. 2008, 180:1163-1175.
10. Wohlgemuth S.L., Crawford B.D., Pilgrim D.B. The myosin co-chaperone UNC-45 is required for skeletal and cardiac muscle function in zebrafish. Dev. Biol. 2007, 303:483-492.
11. Donlin L.T., Andresen C., Just S., Rudensky E., Pappas C.T., Kruger M., Jacobs E.Y., Unger A., Zieseniss A., Dobenecker M.W., Voelkel T., Chait B.T., Gregorio C.C., Rottbauer W., Tarakhovsky A., Linke W.A. Smyd2 controls cytoplasmic lysine methylation of Hsp90 and myofilament organization. Genes Dev. 2012, 26:114-119.
12. Abu-Farha M., Lanouette S., Elisma F., Tremblay V., Butson J., Figeys D., Couture J.F. Proteomic analyses of the SMYD family interactomes identify HSP90 as a novel target for SMYD2. J. Mol. Cell Biol. 2011, 3:301-308.
13. Sirinupong N., Brunzelle J., Ye J., Pirzada A., Nico L., Yang Z. Crystal structure of cardiac-specific histone methyltransferase SmyD1 reveals unusual active site architecture. J. Biol. Chem. 2010, 285:40635-40644.
14. Wang L., Li L., Zhang H., Luo X., Dai J., Zhou S., Gu J., Zhu J., Atadja P., Lu C., Li E., Zhao K. Structure of human SMYD2 protein reveals the basis of p53 tumor suppressor methylation. J. Biol. Chem. 2011, 286:38725-38737.
15. Ferguson A.D., Larsen N.A., Howard T., Pollard H., Green I., Grande C., Cheung T., Garcia-Arenas R., Cowen S., Wu J., Godin R., Chen H., Keen N. Structural basis of substrate methylation and inhibition of SMYD2. Structure 2011, 19:1262-1273.
16. Jiang Y., Sirinupong N., Brunzelle J., Yang Z. Crystal structures of histone and p53 methyltransferase SmyD2 reveal a conformational flexibility of the autoinhibitory C-terminal domain. PLoS One 2011, 6:e21640.
17. Xu S., Zhong C., Zhang T., Ding J. Structure of human lysine methyltransferase Smyd2 reveals insights into the substrate divergence in Smyd proteins. J. Mol. Cell Biol. 2011, 3:293-300.
18. Sirinupong N., Brunzelle J., Doko E., Yang Z. Structural insights into the autoinhibition and posttranslational activation of histone methyltransferase SmyD3. J. Mol. Biol. 2011, 406:149-159.
19. Foreman K.W., Brown M., Park F., Emtage S., Harriss J., Das C., Zhu L., Crew A., Arnold L., Shaaban S., Tucker P. Structural and functional profiling of the human histone methyltransferase SMYD3. PLoS One 2011, 6:e22290.
20. Xu S., Wu J., Sun B., Zhong C., Ding J. Structural and biochemical studies of human lysine methyltransferase Smyd3 reveal the important functional roles of its post-SET and TPR domains and the regulation of its activity by DNA binding. Nucleic Acids Res. 2011, 39:4438-4449.
21. Gottlieb P.D., Pierce S.A., Sims R.J., Yamagishi H., Weihe E.K., Harriss J.V., Maika S.D., Kuziel W.A., King H.L., Olson E.N., Nakagawa O., Srivastava D. Bop encodes a muscle-restricted protein containing MYND and SET domains and is essential for cardiac differentiation and morphogenesis. Nat. Genet. 2002, 31:25-32.
22. Li D., Niu Z., Yu W., Qian Y., Wang Q., Li Q., Yi Z., Luo J., Wu X., Wang Y., Schwartz R.J., Liu M. SMYD1, the myogenic activator, is a direct target of serum response factor and myogenin. Nucleic Acids Res. 2009, 37:7059-7071.
23. Tan X., Rotllant J., Li H., De Deyne P., Du S.J. SmyD1, a histone methyltransferase, is required for myofibril organization and muscle contraction in zebrafish embryos. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:2713-2718.
24. Just S., Meder B., Berger I.M., Etard C., Trano N., Patzel E., Hassel D., Marquart S., Dahme T., Vogel B., Fishman M.C., Katus H.A., Strähle U., Rottbauer W. The myosin-interacting protein SMYD1 is essential for sarcomere organization. J. Cell Sci. 2011, 124:3127-3136.
25. Li H., Xu J., Bian Y.H., Rotllant P., Shen T., Chu W., Zhang J., Schneider M., Du S.J. Smyd1b_tv1, a key regulator of sarcomere assembly, is localized on the M-line of skeletal muscle fibers. PLoS One 2011, 6:e28524.
26. Hamamoto R., Furukawa Y., Morita M., Iimura Y., Silva F.P., Li M., Yagyu R., Nakamura Y. SMYD3 encodes a histone methyltransferase involved in the proliferation of cancer cells. Nat. Cell Biol. 2004, 6:731-740.
27. Medjkane S., Cock-Rada A., Weitzman J.B. Role of the SMYD3 histone methyltransferase in tumorigenesis: local or global effects?. Cell Cycle 2012, 11:1865.
28. Van Aller G.S., Reynoird N., Barbash O., Huddleston M., Liu S., Zmoos A.F., McDevitt P., Sinnamon R., Le B., Mas G., Annan R., Sage J., Garcia B.A., Tummino P.J., Gozani O., Kruger R.G. Smyd3 regulates cancer cell phenotypes and catalyzes histone H4 lysine 5 methylation. Epigenetics 2012, 7:340-343.
29. Kunizaki M., Hamamoto R., Silva F.P., Yamaguchi K., Nagayasu T., Shibuya M., Nakamura Y., Furukawa Y. The lysine 831 of vascular endothelial growth factor receptor 1 is a novel target of methylation by SMYD3. Cancer Res. 2007, 67:10759-10765.
30. Brown M.A., Sims R.J., Gottlieb P.D., Tucker P.W. Identification and characterization of Smyd2: a split SET/MYND domain-containing histone H3 lysine 36-specific methyltransferase that interacts with the Sin3 histone deacetylase complex. Mol. Cancer 2006, 5:26.
31. Fujii T., Tsunesumi S., Yamaguchi K., Watanabe S., Furukawa Y. Smyd3 is required for the development of cardiac and skeletal muscle in zebrafish. PLoS One 2011, 6:e23491.
32. Hu L., Zhu Y.T., Qi C., Zhu Y.J. Identification of Smyd4 as a potential tumor suppressor gene involved in breast cancer development. Cancer Res. 2009, 69:4067-4072.
33. Thompson E.C., Travers A.A. A Drosophila Smyd4 homologue is a muscle-specific transcriptional modulator involved in development. PLoS One 2008, 3:e3008.
34. Stender J.D., Pascual G., Liu W., Kaikkonen M.U., Do K., Spann N.J., Boutros M., Perrimon N., Rosenfeld M.G., Glass C.K. Control of proinflammatory gene programs by regulated trimethylation and demethylation of histone H4K20. Mol. Cell 2012, 48:28-38.
35. Abu-Farha M., Lambert J.P., Al-Madhoun A.S., Elisma F., Skerjanc I.S., Figeys D. The tale of two domains: proteomics and genomics analysis of SMYD2, a new histone methyltransferase. Mol. Cell. Proteomics 2008, 7:560-572.
36. Diehl F., Brown M.A., van Amerongen M.J., Novoyatleva T., Wietelmann A., Harriss J., Ferrazzi F., Böttger T., Harvey R.P., Tucker P.W., Engel F.B. Cardiac deletion of Smyd2 is dispensable for mouse heart development. PLoS One 2010, 5:e9748.
37. Huang J., Perez-Burgos L., Placek B.J., Sengupta R., Richter M., Dorsey J.A., Kubicek S., Opravil S., Jenuwein T., Berger S.L. Repression of p53 activity by Smyd2-mediated methylation. Nature 2006, 444:629-632.
38. Wu J., Cheung T., Grande C., Ferguson A.D., Zhu X., Theriault K., Code E., Birr C., Keen N., Chen H. Biochemical characterization of human SET and MYND domain-containing protein 2 methyltransferase. Biochemistry 2011, 50:6488-6497.
39. Saddic L.A., West L.E., Aslanian A., Yates J.R., Rubin S.M., Gozani O., Sage J. Methylation of the retinoblastoma tumor suppressor by SMYD2. J. Biol. Chem. 2010, 285:37733-37740.
40. Krüger M., Sachse C., Zimmermann W.H., Eschenhagen T., Klede S., Linke W.A. Thyroid hormone regulates developmental titin isoform transitions via the phosphatidylinositol-3-kinase/AKT pathway. Circ. Res. 2008, 102:439-447.
41. Gregorio C.C., Fowler V.M. Mechanisms of thin filament assembly in embryonic chick cardiac myocytes: tropomodulin requires tropomyosin for assembly. J. Cell Biol. 1995, 129:683-695.
42. Neagoe C., Kulke M., del Monte F., Gwathmey J.K., de Tombe P.P., Hajjar R.J., Linke W.A. Titin isoform switch in ischemic human heart disease. Circulation 2002, 106:1333-1341.
43. Nave R., Fürst D.O., Weber K. Visualization of the polarity of isolated titin molecules: a single globular head on a long thin rod as the M band anchoring domain?. J. Cell Biol. 1989, 109:2177-2187.
44. Rottbauer W., Just S., Wessels G., Trano N., Most P., Katus H.A., Fishman M.C. VEGF-PLCgamma1 pathway controls cardiac contractility in the embryonic heart. Genes Dev. 2005, 19:1624-1634.
45. Sims R.J., Weihe E.K., Zhu L., O'Malley S., Harriss J.V., Gottlieb P.D. m-Bop, a repressor protein essential for cardiogenesis, interacts with skNAC, a heart- and muscle-specific transcription factor. J. Biol. Chem. 2002, 277:26524-26529.
46. Miller M.K., Bang M.L., Witt C.C., Labeit D., Trombitas C., Watanabe K., Granzier H., McElhinny A.S., Gregorio C.C., Labeit S. The muscle ankyrin repeat proteins: CARP, ankrd2/Arpp and DARP as a family of titin filament-based stress response molecules. J. Mol. Biol. 2003, 333:951-964.
47. Sun X.J., Xu P.F., Zhou T., Hu M., Fu C.T., Zhang Y., Jin Y., Chen Y., Chen S.J., Huang Q.H., Liu T.X., Chen Z. Genome-wide survey and developmental expression mapping of zebrafish SET domain-containing genes. PLoS One 2008, 3:e1499.
48. Kawamura S., Yoshigai E., Kuhara S., Tashiro K. Smyd1 and smyd2 are expressed in muscle tissue in Xenopus laevis. Cytotechnology 2008, 57:161-168.
49. Hawkins T.A., Haramis A.P., Etard C., Prodromou C., Vaughan C.K., Ashworth R., Ray S., Behra M., Holder N., Talbot W.S., Pearl L.H., Strähle U., Wilson S.W. The ATPase-dependent chaperoning activity of Hsp90a regulates thick filament formation and integration during skeletal muscle myofibrillogenesis. Development 2008, 135:1147-1156.
50. Du S.J., Li H., Bian Y., Zhong Y. Heat-shock protein 90alpha1 is required for organized myofibril assembly in skeletal muscles of zebrafish embryos. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:554-559.
51. Codina M., Li J., Gutiérrez J., Kao J.P., Du S.J. Loss of Smyhc1 or Hsp90alpha1 function results in different effects on myofibril organization in skeletal muscles of zebrafish embryos. PLoS One 2010, 5:e8416.
52. Abaci N., Güleç C., Bayrak F., Kömürcü Bayrak E., Kahveci G., Erginel Unaltuna N. The variations of BOP gene in hypertrophic cardiomyopathy. Anadolu Kardiyol. Derg. 2010, 10:303-309.