Defective sumoylation pathway directs congenital heart disease

Birth Defects Research Part A - Clinical and Molecular Teratology

Volumn 91, Issue 6, 2011, Pages 468-476

  Wang, Jun ^a   Chen, Li ^a   Wen, Shu ^b   Zhu, Huiping ^b,c   Yu, Wei ^d   Moskowitz, Ivan P ^e   Shaw, Gary M ^f   Finnell, Richard H ^b,c   Schwartz, Robert J ^a,d  

^a TEXAS HEART INSTITUTE   (United States)

^b TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

^c UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^d University of Houston   (United States)

^e UNIVERSITY OF CHICAGO   (United States)

^f STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SUMO 1 PROTEIN; TOXIN;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; CELL PROLIFERATION; CHROMATIN; CLEFT PALATE; CONTROLLED STUDY; DNA MICROARRAY; DNA SEQUENCE; EMBRYO DEVELOPMENT; GENE MUTATION; GENETICS; HEART ATRIUM SEPTUM DEFECT; HEART DEVELOPMENT; HEART VENTRICLE SEPTUM DEFECT; HISTOPATHOLOGY; HUMAN; KNOCKOUT MOUSE; MAJOR CLINICAL STUDY; MORTALITY; MOUSE; NEWBORN; NEWBORN SCREENING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SUMOYLATION; WESTERN BLOTTING;

ANIMALS; BASE SEQUENCE; CELL PROLIFERATION; CLEFT LIP; CLEFT PALATE; HEART SEPTAL DEFECTS, ATRIAL; HEART SEPTAL DEFECTS, VENTRICULAR; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PROMOTER REGIONS, GENETIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; SUMO-1 PROTEIN; SUMOYLATION; UBIQUITIN;

MUS;

EID: 79958146174     PISSN: 15420752     EISSN: 15420760     Source Type: Journal    
DOI: 10.1002/bdra.20816     Document Type: Article

References (59)

1. Ahuja P, Sdek P, MacLellan WR, et al. 2007. Cardiac myocyte cell cycle control in development, disease, and regeneration. Physiol Rev 87: 521-544.
2. Alkuraya FS, Saadi I, Lund JJ, et al. 2006. SUMO1 haploinsufficiency leads to cleft lip and palate. Science 313: 1751.
3. Arnaoutov A, Azuma Y, Ribbeck K, et al. 2005. Crm1 is a mitotic effector of Ran-GTP in somatic cells. Nat Cell Biol 7: 626-632.
4. Ayaydin F, Dasso M. 2004. Distinct in vivo dynamics of vertebrate SUMO paralogues. Mol Biol Cell 15: 5208-5218.
5. Baldini A. 2005. Dissecting contiguous gene defects: TBX1. Curr Opin Genet Dev 15: 279-284.
6. Bentham J, Bhattacharya S. 2008. Genetic mechanisms controlling cardiovascular development. Ann N Y Acad Sci 1123: 10-19.
7. Biben C, Weber R, Kesteven S, et al. 2000. Cardiac septal and valvular dysmorphogenesis in mice heterozygous for mutations in the homeobox gene Nkx2-5. Circ Res 87: 888-895.
8. Bostrom P, Mann N, Wu J, et al. 2010. C/EBPbeta controls exercise-induced cardiac growth and protects against pathological cardiac remodeling. Cell 143: 1072-1083.
9. Bruneau BG, Nemer G, Schmitt JP, et al. 2001. A murine model of Holt-Oram syndrome defines roles of the T-box transcription factor Tbx5 in cardiogenesis and disease. Cell 106: 709-721.
10. Claycomb WC, Lanson NAJr, S, et al. 1998. HL-1 cells: a cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte. Proc Natl Acad Sci U S A 95: 2979-2984.
11. Dasso M. 2008. Emerging roles of the SUMO pathway in mitosis. Cell Div 3: 5.
12. David G, Neptune MA, DePinho RA, et al. 2002. SUMO-1 modification of histone deacetylase 1 (HDAC1) modulates its biological activities. J Biol Chem 277: 23658-23663.
13. Dawlaty MM, Malureanu L, Jeganathan KB, et al. 2008. Resolution of sister centromeres requires RanBP2-mediated SUMOylation of topoisomerase IIalpha. Cell 133: 103-115.
14. Evdokimov E, Sharma P, Lockett SJ, et al. 2008. 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 121: 4106-4113.
15. Fu C, Ahmed K, Ding H, et al. 2005. Stabilization of PML nuclear localization by conjugation and oligomerization of SUMO-3. Oncogene 24: 5401-5413.
16. Garg V, Kathiriya IS, Barnes R, et al. 2003. GATA4 mutations cause human congenital heart defects and reveal an interaction with TBX5. Nature 424: 443-447.
17. Golebiowski F, Szulc A, Sakowicz M, et al. 2003. Expression level of Ubc9 protein in rat tissues. Acta Biochim Pol 50: 1065-1073.
18. Hoffman JI, Kaplan S. 1900. The incidence of congenital heart disease. J Am Coll Cardiol 2002; 39: 1890-1900.
19. Huang J, Min Lu M, Cheng L, et al. 2009. Myocardin is required for cardiomyocyte survival and maintenance of heart function. Proc Natl Acad Sci U S A 106: 18734-18739.
20. Johnson ES. 2004. Protein modification by sumo. Annu Rev Biochem 73: 355-382.
21. Kagey MH, Melhuish TA, Wotton D, et al. 2003. The polycomb protein Pc2 is a SUMO E3. Cell 113: 127-137.
22. Kang X, Qi Y, Zuo Y, et al. 2010. SUMO-specific protease 2 is essential for suppression of polycomb group protein-mediated gene silencing during embryonic development. Mol Cell 38: 191-201.
23. Kirsh O, Seeler JS, Pichler A, et al. 2002. The SUMO E3 ligase RanBP2 promotes modification of the HDAC4 deacetylase. Embo J 21: 2682-2691.
24. Komatsu T, Mizusaki H, Mukai T, et al. 2004. SUMO-1 Modification of the synergy control motif of Ad4BP/SF-1 regulates synergistic transcription between Ad4BP/SF-1 and Sox9. Mol Endocrinol 18: 2451-2462.
25. Liang Q, De Windt LJ, Witt SA, et al. 2001. The transcription factors GATA4 and GATA6 regulate cardiomyocyte hypertrophy in vitro and in vivo. J Biol Chem 276: 30245-30253.
26. Ling Y, Sankpal UT, Robertson AK, et al. 2004. Modification of de novo DNA methyltransferase 3a (Dnmt3a) by SUMO-1 modulates its interaction with histone deacetylases (HDACs) and its capacity to repress transcription. Nucleic Acids Res 32: 598-610.
27. Matsuzaki K, Minami T, Tojo M, et al. 2003. Serum response factor is modulated by the SUMO-1 conjugation system. Biochem Biophys Res Commun 306: 32-38.
28. Moses KA, DeMayo F, Braun RM, et al. 2001. Embryonic expression of an Nkx2-5/Cre gene using ROSA26 reporter mice. Genesis 31: 176-180.
29. Mukhopadhyay D, Dasso M. 2007. Modification in reverse: the SUMO proteases. Trends Biochem Sci 32: 286-295.
30. Nacerddine K, Lehembre F, Bhaumik M, et al. 2005. The SUMO pathway is essential for nuclear integrity and chromosome segregation in mice. Dev Cell 9: 769-779.
31. Nie X, Deng CX, Wang Q, et al. 2008. Disruption of Smad4 in neural crest cells leads to mid-gestation death with pharyngeal arch, craniofacial and cardiac defects. Dev Biol 316: 417-430.
32. Niessen K, Karsan A. 2008. Notch signaling in cardiac development. Circ Res 102: 1169-1181.
33. Niu Z, Iyer D, Conway SJ, et al. 2008. Serum response factor orchestrates nascent sarcomerogenesis and silences the biomineralization gene program in the heart. Proc Natl Acad Sci U S A 105: 17824-17829.
34. Oka T, Maillet M, Watt AJ, et al. 2006. Cardiac-specific deletion of Gata4 reveals its requirement for hypertrophy, compensation, and myocyte viability. Circ Res 98: 837-845.
35. Riising EM, Boggio R, Chiocca S, et al. 2008. The polycomb repressive complex 2 is a potential target of SUMO modifications. PLoS ONE 3: e2704.
36. Riquelme C, Barthel KK, Qin XF, et al. 2008. Ubc9 expression is essential for myotube formation in C2C12. Exp Cell Res 312: 2132-2141.
37. Rosas-Acosta G, Russell WK, Deyrieux A, et al. 2005. A universal strategy for proteomic studies of SUMO and other ubiquitin-like modifiers. Mol Cell Proteomics 4: 56-72.
38. Roy Chowdhuri S, Crum T, Woollard A, et al. 2006. The T-box factor TBX-2 and the SUMO conjugating enzyme UBC-9 are required for ABa-derived pharyngeal muscle in C. elegans. Dev Biol 295: 664-677.
39. Saitoh H, Hinchey J. 2000. Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3. J Biol Chem 275: 6252-6258.
40. Tanaka M, Chen Z, Bartunkova S, et al. 1999. The cardiac homeobox gene Csx/Nkx2.5 lies genetically upstream of multiple genes essential for heart development. Development 126: 1269-1280.
41. Tatham MH, Kim S, Jaffray E, et al. 2005. Unique binding interactions among Ubc9, SUMO and RanBP2 reveal a mechanism for SUMO paralog selection. Nat Struct Mol Biol 12: 67-74.
42. Vaughan CJ, Basson CT. 2000. Molecular determinants of atrial and ventricular septal defects and patent ductus arteriosus. Am J Med Genet 97: 304-309.
43. Vertegaal AC, Andersen JS, Ogg SC, et al. 2006. Distinct and overlapping sets of SUMO-1 and SUMO-2 target proteins revealed by quantitative proteomics. Mol Cell Proteomics 5: 2298-2310.
44. Vertegaal AC, Ogg SC, Jaffray E, et al. 2004. A proteomic study of SUMO-2 target proteins. J Biol Chem 279: 33791-33798.
45. Wang J. 2009. SUMO conjugation and cardiovascular development. Front Biosci 14: 1219-1229.
46. Wang J, Feng XH, Schwartz RJ, et al. 2004. SUMO-1 modification activated GATA4-dependent cardiogenic gene activity. J Biol Chem 279: 49091-49098.
47. Wang J, Li A, Wang Z, et al. 2007. Myocardin sumoylation transactivates cardiogenic genes in pluripotent 10T1/2 fibroblasts. Mol Cell Biol 27: 622-632.
48. Wang J, Schwartz RJ. 2010. Sumoylation and regulation of cardiac gene expression. Circ Res 107: 19-29.
49. Wang J, Zhang H, Iyer D, et al. 2008. Regulation of cardiac specific nkx2.5 gene activity by small ubiquitin-like modifier. J Biol Chem 283: 23235-23243.
50. Watanabe TK, Fujiwara T, Kawai A, et al. 1996. Cloning, expression, and mapping of UBE2I, a novel gene encoding a human homologue of yeast ubiquitin-conjugating enzymes which are critical for regulating the cell cycle. Cytogenet Cell Genet 72: 86-89.
51. Wei L, Roberts W, Wang L, et al. 2001. Rho kinases play an obligatory role in vertebrate embryonic organogenesis. Development 128: 2953-2962.
52. White SM, Constantin PE, Claycomb WC, et al. 2004. Cardiac physiology at the cellular level: use of cultured HL-1 cardiomyocytes for studies of cardiac muscle cell structure and function. Am J Physiol Heart Circ Physiol 286: H823-H829.
53. Winston JB, Erlich JM, Green CA, et al. 2010. Heterogeneity of genetic modifiers ensures normal cardiac development. Circulation 121: 1313-1321.
54. Wu JC, Child JS. 2004. Common congenital heart disorders in adults. Curr Probl Cardiol 29: 641-700.
55. Yeh ET. 2009. SUMOylation and de-SUMOylation: Wrestling with life's processes. J Biol Chem 284: 8223-8227.
56. Yeh ET, Gong L, Kamitani T, et al. 2000. Ubiquitin-like proteins: new wines in new bottles. Gene 248: 1-14.
57. Zhang FP, Mikkonen L, Toppari J, et al. 2008a. Sumo-1 function is dispensable in normal mouse development. Mol Cell Biol 28: 5381-5390.
58. Zhang XD, Goeres J, Zhang H, et al. 2008b. SUMO-2/3 modification and binding regulate the association of CENP-E with kinetochores and progression through mitosis. Mol Cell 29: 729-741.
59. Zhao R, Watt AJ, Battle MA, et al. 2008. Loss of both GATA4 and GATA6 blocks cardiac myocyte differentiation and results in acardia in mice. Dev Biol 317: 614-619.