Enhanced desumoylation in murine hearts by overexpressed SENP2 leads to congenital heart defects and cardiac dysfunction

Journal of Molecular and Cellular Cardiology

Volumn 52, Issue 3, 2012, Pages 638-649

  Kim, Eun Young ^a,b   Chen, Li ^b   Ma, Yanlin ^a   Yu, Wei ^c   Chang, Jiang ^a   Moskowitz, Ivan P ^d   Wang, Jun ^b  

^a UNIVERSITY OF TEXAS   (United States)

^b ST LUKE S EPISCOPAL HOSPITAL   (United States)

^c University of Houston   (United States)

^d UNIVERSITY OF CHICAGO   (United States)

Author keywords

Cardiomyopathy; Congenital heart defects; Nkx2.5; SENP2; SUMO

Indexed keywords

PROTEINASE; SENTRIN SPECIFIC PROTEINASE 2; SUMO 1 PROTEIN; TRANSCRIPTION FACTOR NKX2.5; UNCLASSIFIED DRUG;

AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIOMYOPATHY; CELL PROLIFERATION; CONGENITAL HEART MALFORMATION; CONTROLLED STUDY; DEATH; DESUMOYLATION; DISEASE SEVERITY; EMBRYO; GENE OVEREXPRESSION; GROWTH RETARDATION; HAPLOINSUFFICIENCY; HEART ATRIUM SEPTUM DEFECT; HEART DISEASE; HEART MUSCLE CELL; HEART VENTRICLE SEPTUM DEFECT; IN VIVO STUDY; LETHALITY; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; SUMOYLATION; TRANSGENE; WILD TYPE;

ANIMALS; CELL LINE; CELL PROLIFERATION; CYSTEINE ENDOPEPTIDASES; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC VECTORS; HEART; HEART DEFECTS, CONGENITAL; HOMEODOMAIN PROTEINS; HUMANS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MYOCARDIUM; MYOCYTES, CARDIAC; SIGNAL TRANSDUCTION; SUMO-1 PROTEIN; SUMOYLATION; TRANSCRIPTION FACTORS;

MURINAE; MUS; MUS MUSCULUS;

EID: 84857626547     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2011.11.011     Document Type: Article

References (59)

1. Bruneau B.G., Nemer G., Schmitt J.P., Charron F., Robitaille L., Caron S., et al. A murine model of Holt-Oram syndrome defines roles of the T-box transcription factor Tbx5 in cardiogenesis and disease. Cell 2001, 106(6):709-721.
2. Niessen K., Karsan A. Notch signaling in cardiac development. Circ Res 2008, 102(10):1169-1181.
3. Nie X., Deng C.X., Wang Q., Jiao K. Disruption of Smad4 in neural crest cells leads to mid-gestation death with pharyngeal arch, craniofacial and cardiac defects. Dev Biol 2008, 316(2):417-430.
4. Tanaka M., Chen Z., Bartunkova S., Yamasaki N., Izumo S. The cardiac homeobox gene Csx/Nkx2.5 lies genetically upstream of multiple genes essential for heart development. Development 1999, 126(6):1269-1280.
5. Garg V., Kathiriya I.S., Barnes R., Schluterman M.K., King I.N., Butler C.A., et al. GATA4 mutations cause human congenital heart defects and reveal an interaction with TBX5. Nature 2003, 424(6947):443-447.
6. Baldini A. Dissecting contiguous gene defects: TBX1. Curr Opin Genet Dev 2005, 15(3):279-284.
7. Bentham J., Bhattacharya S. Genetic mechanisms controlling cardiovascular development. Ann N Y Acad Sci 2008, 1123:10-19.
8. Wang J. Cardiac function and disease: emerging role of small ubiquitin-related modifier. Wiley Interdiscip Rev Syst Biol Med 2011, 3(4):446-457. PMCID: 3110591.
9. Wang J., Schwartz R.J. Sumoylation and regulation of cardiac gene expression. Circ Res 2010, 107(1):19-29.
10. Dasso M. Emerging roles of the SUMO pathway in mitosis. Cell Div 2008, 3:5.
11. Johnson E.S., Blobel G. Cell cycle-regulated attachment of the ubiquitin-related protein SUMO to the yeast septins. J Cell Biol 1999, 147(5):981-994.
12. Poulin G., Dong Y., Fraser A.G., Hopper N.A., Ahringer J. Chromatin regulation and sumoylation in the inhibition of Ras-induced vulval development in Caenorhabditis elegans. EMBO J 2005, 24(14):2613-2623.
13. Johnson E.S. Protein modification by sumo. Annu Rev Biochem 2004, 73:355-382.
14. Rosas-Acosta G., Russell W.K., Deyrieux A., Russell D.H., Wilson V.G. A universal strategy for proteomic studies of SUMO and other ubiquitin-like modifiers. Mol Cell Proteomics 2005, 4(1):56-72.
15. Mukhopadhyay D., Dasso M. Modification in reverse: the SUMO proteases. Trends Biochem Sci 2007, 32(6):286-295.
16. Gong L., Millas S., Maul G.G., Yeh E.T. Differential regulation of sentrinized proteins by a novel sentrin-specific protease. J Biol Chem 2000, 275(5):3355-3359.
17. Hang J., Dasso M. Association of the human SUMO-1 protease SENP2 with the nuclear pore. J Biol Chem 2002, 277(22):19961-19966.
18. Mikolajczyk J., Drag M., Bekes M., Cao J.T., Ronai Z., Salvesen G.S. Small ubiquitin-related modifier (SUMO)-specific proteases: profiling the specificities and activities of human SENPs. J Biol Chem 2007, 282(36):26217-26224.
19. Yeh E.T. SUMOylation and de-SUMOylation: Wrestling with life's processes. J Biol Chem 2008, 2008.
20. Cheng J., Bawa T., Lee P., Gong L., Yeh E.T. Role of desumoylation in the development of prostate cancer. Neoplasia 2006, 8(8):667-676.
21. Gong L., Yeh E.T. Characterization of a family of nucleolar SUMO-specific proteases with preference for SUMO-2 or SUMO-3. J Biol Chem 2006, 281(23):15869-15877.
22. Di Bacco A., Ouyang J., Lee H.Y., Catic A., Ploegh H., Gill G. The SUMO-specific protease SENP5 is required for cell division. Mol Cell Biol 2006, 26(12):4489-4498.
23. Mukhopadhyay D., Ayaydin F., Kolli N., Tan S.H., Anan T., Kametaka A., et al. SUSP1 antagonizes formation of highly SUMO2/3-conjugated species. J Cell Biol 2006, 174(7):939-949.
24. Shen L.N., Geoffroy M.C., Jaffray E.G., Hay R.T. Characterization of SENP7, a SUMO-2/3-specific isopeptidase. Biochem J 2009, 421(2):223-230.
25. Cheng J., Kang X., Zhang S., Yeh E.T. SUMO-specific protease 1 is essential for stabilization of HIF1alpha during hypoxia. Cell 2007, 131(3):584-595.
26. Kang X., Qi Y., Zuo Y., Wang Q., Zou Y., Schwartz R.J., et al. SUMO-specific protease 2 is essential for suppression of polycomb group protein-mediated gene silencing during embryonic development. Mol Cell 2010, 38(2):191-201.
27. Chiu S.Y., Asai N., Costantini F., Hsu W. SUMO-specific protease 2 is essential for modulating p53-Mdm2 in development of trophoblast stem cell niches and lineages. PLoS Biol 2008, 6(12):e310.
28. Dorval V., Fraser P.E. SUMO on the road to neurodegeneration. Biochim Biophys Acta 2007, 1773(6):694-706.
29. Aribi M. Candidate genes implicated in type 1 diabetes susceptibility. Curr Diabetes Rev 2008, 4(2):110-121.
30. Wu F., Mo Y.Y. Ubiquitin-like protein modifications in prostate and breast cancer. Front Biosci 2007, 12:700-711.
31. Pauws E., Stanier P. FGF signalling and SUMO modification: new players in the aetiology of cleft lip and/or palate. Trends Genet 2007, 23(12):631-640.
32. Zhang Y.Q., Sarge K.D. Sumoylation regulates lamin A function and is lost in lamin A mutants associated with familial cardiomyopathies. J Cell Biol 2008, 182(1):35-39.
33. Wang J., Feng X.H., Schwartz R.J. SUMO-1 modification activated GATA4-dependent cardiogenic gene activity. J Biol Chem 2004, 279(47):49091-49098.
34. Wang J., Li A., Wang Z., Feng X., Olson E.N., Schwartz R.J. Myocardin sumoylation transactivates cardiogenic genes in pluripotent 10T1/2 fibroblasts. Mol Cell Biol 2007, 27(2):622-632.
35. Wang J., Zhang H., Iyer D., Feng X.H., Schwartz R.J. Regulation of cardiac specific Nkx2.5 gene activity by sumo modificaiton. J Biol Chem 2008.
36. Wang J., Chen L., Wen S., Zhu H., Yu W., Moskowitz I.P., et al. Defective sumoylation pathway directs congenital heart disease. Birth Defects Res A Clin Mol Teratol 2011, 91(6):468-476.
37. Chen C.Y., Croissant J., Majesky M., Topouzis S., McQuinn T., Frankovsky M.J., et al. Activation of the cardiac alpha-actin promoter depends upon serum response factor, Tinman homologue, Nkx-2.5, and intact serum response elements. Dev Genet 1996, 19(2):119-130.
38. Wang J., Zhang H., Iyer D., Feng X.H., Schwartz R.J. Regulation of cardiac specific nkx2.5 gene activity by small ubiquitin-like modifier. J Biol Chem 2008, 283(34):23235-23243. PMCID: 2516993.
39. Kim E.Y., Chen L., Ma Y., Yu W., Chang J., Moskowitz I.P., et al. Expression of sumoylation deficient nkx2.5 mutant in nkx2.5 haploinsufficient mice leads to congenital heart defects. PLoS One 2011, 6(6):e20803. PMCID: 3108998.
40. Moses K.A., DeMayo F., Braun R.M., Reecy J.L., Schwartz R.J. Embryonic expression of an Nkx2-5/Cre gene using ROSA26 reporter mice. Genesis 2001, 31(4):176-180.
41. Evdokimov E., Sharma P., Lockett S.J., Lualdi M., Kuehn M.R. Loss of SUMO1 in mice affects RanGAP1 localization and formation of PML nuclear bodies, but is not lethal as it can be compensated by SUMO2 or SUMO3. J Cell Sci 2008, 121(Pt 24):4106-4113.
42. Monzen K., Shiojima I., Hiroi Y., Kudoh S., Oka T., Takimoto E., et al. Bone morphogenetic proteins induce cardiomyocyte differentiation through the mitogen-activated protein kinase kinase kinase TAK1 and cardiac transcription factors Csx/Nkx-2.5 and GATA-4. Mol Cell Biol 1999, 19(10):7096-7105.
43. Fujikura J., Yamato E., Yonemura S., Hosoda K., Masui S., Nakao K., et al. Differentiation of embryonic stem cells is induced by GATA factors. Genes Dev 2002, 16(7):784-789. PMCID: 186328.
44. Manabe I., Owens G.K. Recruitment of serum response factor and hyperacetylation of histones at smooth muscle-specific regulatory regions during differentiation of a novel P19-derived in vitro smooth muscle differentiation system. Circ Res 2001, 88(11):1127-1134.
45. Schoenfeld J.R., Vasser M., Jhurani P., Ng P., Hunter J.J., Ross J., et al. Distinct molecular phenotypes in murine cardiac muscle development, growth, and hypertrophy. J Mol Cell Cardiol 1998, 30(11):2269-2280.
46. Makino S., Fukuda K., Miyoshi S., Konishi F., Kodama H., Pan J., et al. Cardiomyocytes can be generated from marrow stromal cells in vitro. J Clin Invest 1999, 103(5):697-705. PMCID: 408125.
47. Zhang H., Saitoh H., Matunis M.J. Enzymes of the SUMO modification pathway localize to filaments of the nuclear pore complex. Mol Cell Biol 2002, 22(18):6498-6508. PMCID: 135644.
48. Kasahara H., Lee B., Schott J.J., Benson D.W., Seidman J.G., Seidman C.E., et al. Loss of function and inhibitory effects of human CSX/NKX2.5 homeoprotein mutations associated with congenital heart disease. J Clin Invest 2000, 106(2):299-308.
49. Tanaka M., Berul C.I., Ishii M., Jay P.Y., Wakimoto H., Douglas P., et al. A mouse model of congenital heart disease: cardiac arrhythmias and atrial septal defect caused by haploinsufficiency of the cardiac transcription factor Csx/Nkx2.5. Cold Spring Harb Symp Quant Biol 2002, 67:317-325.
50. Terada R., Warren S., Lu J.T., Chien K.R., Wessels A., Kasahara H. Ablation of Nkx2-5 at mid-embryonic stage results in premature lethality and cardiac malformation. Cardiovasc Res 2011, 91(2):289-299. PMCID: 3125071.
51. Alkuraya F.S., Saadi I., Lund J.J., Turbe-Doan A., Morton C.C., Maas R.L. SUMO1 haploinsufficiency leads to cleft lip and palate. Science 2006, 313(5794):1751.
52. Song T., Li G., Jing G., Jiao X., Shi J., Zhang B., et al. SUMO1 polymorphisms are associated with non-syndromic cleft lip with or without cleft palate. Biochem Biophys Res Commun 2008, 377(4):1265-1268.
53. Joseph J., Tan S.H., Karpova T.S., McNally J.G., Dasso M. SUMO-1 targets RanGAP1 to kinetochores and mitotic spindles. J Cell Biol 2002, 156(4):595-602.
54. Dawlaty M.M., Malureanu L., Jeganathan K.B., Kao E., Sustmann C., Tahk S., et al. Resolution of sister centromeres requires RanBP2-mediated SUMOylation of topoisomerase IIalpha. Cell 2008, 133(1):103-115.
55. Azuma Y., Arnaoutov A., Anan T., Dasso M. PIASy mediates SUMO-2 conjugation of Topoisomerase-II on mitotic chromosomes. EMBO J 2005, 24(12):2172-2182.
56. Argao E.A., Kern M.J., Branford W.W., Scott W.J., Potter S.S. Malformations of the heart, kidney, palate, and skeleton in alpha-MHC-Hoxb-7 transgenic mice. Mech Dev 1995, 52(2-3):291-303.
57. Moskowitz I.P., Kim J.B., Moore M.L., Wolf C.M., Peterson M.A., Shendure J., et al. A molecular pathway including Id2, Tbx5, and Nkx2-5 required for cardiac conduction system development. Cell 2007, 129(7):1365-1376.
58. Thakar K., Niedenthal R., Okaz E., Franken S., Jakobs A., Gupta S., et al. SUMOylation of the hepatoma-derived growth factor negatively influences its binding to chromatin. FEBS J 2008, 275(7):1411-1426.
59. Melchior F., Schergaut M., Pichler A. SUMO: ligases, isopeptidases and nuclear pores. Trends Biochem Sci 2003, 28(11):612-618.