UBC9-Mediated Sumoylation Favorably Impacts Cardiac Function in Compromised Hearts

Circulation Research

Volumn 118, Issue 12, 2016, Pages 1894-1905

  Gupta, Manish K ^a   McLendon, Patrick M ^b   Gulick, James ^b   James, Jeanne ^b   Khalili, Kamel ^a   Robbins, Jeffrey ^b  

^a TEMPLE UNIVERSITY   (United States)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

autophagy; crystallin; heart disease; hypertrophy; transgenic mice Transgenic mice

Indexed keywords

BAFILOMYCIN A1; BECLIN 1; BETA CRYSTALLIN; COMPLEMENTARY DNA; DESMIN; MICROTUBULE ASSOCIATED PROTEIN 2; PROTEASOME; PROTEIN UBC9; SUMO 1 PROTEIN; SUMO PROTEIN; UBIQUITINATED PROTEIN; ALPHA CRYSTALLIN; CRYAB PROTEIN, MOUSE; UBIQUITIN CONJUGATING ENZYME; UBIQUITIN-CONJUGATING ENZYME UBC9;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; ECHOCARDIOGRAPHY; HEART FUNCTION; HEART MUSCLE FIBROSIS; HEART STRESS; HEART VENTRICLE HYPERTROPHY; MOUSE; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SUMOYLATION; SURVIVAL; UPREGULATION; WESTERN BLOTTING; ANIMAL; CARDIAC MUSCLE CELL; CARDIOMYOPATHY; CELL CULTURE; GENETICS; METABOLISM; RAT; SPRAGUE DAWLEY RAT;

ALPHA-CRYSTALLIN B CHAIN; ANIMALS; AUTOPHAGY; CARDIOMYOPATHIES; CELLS, CULTURED; MICE; MYOCYTES, CARDIAC; RATS; RATS, SPRAGUE-DAWLEY; SUMOYLATION; UBIQUITIN-CONJUGATING ENZYMES;

EID: 84966344031     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.115.308268     Document Type: Article

References (65)

1. Wang J, Schwartz RJ. Sumoylation and regulation of cardiac gene expression. Circ Res. 2010;107:19-29. doi: 10.1161/CIRCRESAHA.110.220491.
2. Stastna M, Van Eyk JE. Posttranslational modifications of lysine and evolving role in heart pathologies-recent developments. Proteomics. 2015;15:1164-1180. doi: 10.1002/pmic.201400312.
3. Meluh PB, Koshland D. Evidence that the MIF2 gene of Saccharomyces cerevisiae encodes a centromere protein with homology to the mammalian centromere protein CENP-C. Mol Biol Cell. 1995;6:793-807. doi: 10.1091/mbc.6.7.793.
4. Shen Z, Pardington-Purtymun PE, Comeaux JC, Moyzis RK, Chen DJ. UBL1, a human ubiquitin-like protein associating with human RAD51/RAD52 proteins. Genomics. 1996;36:271-279. doi: 10.1006/ geno.1996.0462.
5. Geiss-Friedlander R, Melchior F. Concepts in sumoylation: a decade on. Nat Rev Mol Cell Biol. 2007;8:947-956. doi: 10.1038/nrm2293.
6. Branzei D, Foiani M. Regulation of DNA repair throughout the cell cycle. Nat Rev Mol Cell Biol. 2008;9:297-308. doi: 10.1038/nrm2351.
7. Wang J, Feng XH, Schwartz RJ. SUMO-1 modification activated GATA4-dependent cardiogenic gene activity. J Biol Chem. 2004;279:49091-49098. doi: 10.1074/jbc.M407494200.
8. Flotho A, Melchior F. Sumoylation: a regulatory protein modification in health and disease. Annu Rev Biochem. 2013;82:357-385. doi: 10.1146/ annurev-biochem-061909-093311.
9. Makhnevych T, Sydorskyy Y, Xin X, Srikumar T, Vizeacoumar FJ, Jeram SM, Li Z, Bahr S, Andrews BJ, Boone C, Raught B. Global map of SUMO function revealed by protein-protein interaction and genetic networks. Mol Cell. 2009;33:124-135. doi: 10.1016/j.molcel.2008.12.025.
10. Cubeñas-Potts C, Matunis MJ. SUMO: a multifaceted modifier of chromatin structure and function. Dev Cell. 2013;24:1-12. doi: 10.1016/j. devcel.2012.11.020.
11. Duprez E, Saurin AJ, Desterro JM, Lallemand-Breitenbach V, Howe K, Boddy MN, Solomon E, de Thé H, Hay RT, Freemont PS. SUMO-1 modification of the acute promyelocytic leukaemia protein PML: implications for nuclear localisation. J Cell Sci. 1999;112 (pt 3):381-393.
12. Su H, Wang X. The ubiquitin-proteasome system in cardiac proteinopathy: a quality control perspective. Cardiovasc Res. 2010;85:253-262. doi: 10.1093/cvr/cvp287.
13. Müller S, Hoege C, Pyrowolakis G, Jentsch S. SUMO, ubiquitin's mysterious cousin. Nat Rev Mol Cell Biol. 2001;2:202-210. doi: 10.1038/35056591.
14. Kravtsova-Ivantsiv Y, Ciechanover A. Non-canonical ubiquitin-based signals for proteasomal degradation. J Cell Sci. 2012;125:539-548. doi: 10.1242/jcs.093567.
15. Gustafsson AB, Gottlieb RA. Autophagy in ischemic heart disease. Circ Res. 2009;104:150-158. doi: 10.1161/CIRCRESAHA.108.187427.
16. Wani WY, Boyer-Guittaut M, Dodson M, Chatham J, Darley-Usmar V, Zhang J. Regulation of autophagy by protein post-translational modification. Lab Invest. 2015;95:14-25. doi: 10.1038/labinvest.2014.131.
17. Yi C, Yu L. How does acetylation regulate autophagy? Autophagy. 2012;8:1529-1530. doi: 10.4161/auto.21156.
18. Papinski D, Schuschnig M, Reiter W, et al. Early steps in autophagy depend on direct phosphorylation of Atg9 by the Atg1 kinase. Mol Cell. 2014;53:471-483. doi: 10.1016/j.molcel.2013.12.011.
19. Yang Y, Fiskus W, Yong B, Atadja P, Takahashi Y, Pandita TK, Wang HG, Bhalla KN. Acetylated hsp70 and KAP1-mediated Vps34 SUMOylation is required for autophagosome creation in autophagy. Proc Natl Acad Sci U S A. 2013;110:6841-6846. doi: 10.1073/pnas.1217692110.
20. Cajee UF, Hull R, Ntwasa M. Modification by ubiquitin-like proteins: significance in apoptosis and autophagy pathways. Int J Mol Sci. 2012;13:11804-11831. doi: 10.3390/ijms130911804.
21. Shahpasandzadeh H, Popova B, Kleinknecht A, Fraser PE, Outeiro TF, Braus GH. Interplay between sumoylation and phosphorylation for protection against α-synuclein inclusions. J Biol Chem. 2014;289:31224-31240. doi: 10.1074/jbc.M114.559237.
22. Gupta MK, Gulick J, Liu R, Wang X, Molkentin JD, Robbins J. Sumo E2 enzyme UBC9 is required for efficient protein quality control in cardiomyocytes. Circ Res. 2014;115:721-729. doi: 10.1161/CIRCRESAHA.115.304760.
23. Subramaniam A, Jones WK, Gulick J, Wert S, Neumann J, Robbins J. Tissue-specific regulation of the alpha-myosin heavy chain gene promoter in transgenic mice. J Biol Chem. 1991;266:24613-24620.
24. Sanbe A, Osinska H, Saffitz JE, Glabe CG, Kayed R, Maloyan A, Robbins J. Desmin-related cardiomyopathy in transgenic mice: a cardiac amyloidosis. Proc Natl Acad Sci U S A. 2004;101:10132-10136. doi: 10.1073/ pnas.0401900101.
25. Haq S, Choukroun G, Kang ZB, et al. Glycogen synthase kinase-3beta is a negative regulator of cardiomyocyte hypertrophy. J Cell Biol. 2000;151:117-130. doi: 10.1083/jcb.151.1.117.
26. Luo J, Deng ZL, Luo X, Tang N, Song WX, Chen J, Sharff KA, Luu HH, Haydon RC, Kinzler KW, Vogelstein B, He TC. A protocol for rapid generation of recombinant adenoviruses using the AdEasy system. Nat Protoc. 2007;2:1236-1247. doi: 10.1038/nprot.2007.135.
27. Liu ZQ, Mahmood T, Yang PC. Western blot: technique, theory and trouble shooting. N Am J Med Sci. 2014;6:160. doi: 10.4103/1947-2714.128482.
28. Mizushima N, Yamamoto A, Matsui M, Yoshimori T, Ohsumi Y. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell. 2004;15:1101-1111. doi: 10.1091/mbc.E03-09-0704.
29. Su H, Li F, Ranek MJ, Wei N, Wang X. COP9 signalosome regulates autophagosome maturation. Circulation. 2011;124:2117-2128. doi: 10.1161/CIRCULATIONAHA.111.048934.
30. Bhuiyan MS, Pattison JS, Osinska H, James J, Gulick J, McLendon PM, Hill JA, Sadoshima J, Robbins J. Enhanced autophagy ameliorates cardiac proteinopathy. J Clin Invest. 2013;123:5284-5297. doi: 10.1172/JCI70877.
31. Pistner A, Belmonte S, Coulthard T, Blaxall B. Murine echocardiography and ultrasound imaging. J Vis Exp. 2010;42:2100. doi: 10.3791/2100.
32. Sadayappan S, Gulick J, Osinska H, Martin LA, Hahn HS, Dorn GW 2nd, Klevitsky R, Seidman CE, Seidman JG, Robbins J. Cardiac myosin-binding protein-C phosphorylation and cardiac function. Circ Res. 2005;97:1156-1163. doi: 10.1161/01.RES.0000190605.79013.4d.
33. Sengupta A, Molkentin JD, Yutzey KE. FoxO transcription factors promote autophagy in cardiomyocytes. J Biol Chem. 2009;284:28319-28331. doi: 10.1074/jbc.M109.024406.
34. Matsui Y, Takagi H, Qu X, Abdellatif M, Sakoda H, Asano T, Levine B, Sadoshima J. Distinct roles of autophagy in the heart during ischemia and reperfusion: roles of AMP-activated protein kinase and Beclin 1 in mediating autophagy. Circ Res. 2007;100:914-922. doi: 10.1161/01. RES.0000261924.76669.36.
35. Pattison JS, Osinska H, Robbins J. Atg7 induces basal autophagy and rescues autophagic deficiency in CryABR120G cardiomyocytes. Circ Res. 2011;109:151-160. doi: 10.1161/CIRCRESAHA.110.237339.
36. Kang R, Zeh HJ, Lotze MT, Tang D. The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ. 2011;18:571-580. doi: 10.1038/ cdd.2010.191.
37. Cui Z, Scruggs SB, Gilda JE, Ping P, Gomes AV. Regulation of cardiac proteasomes by ubiquitination, SUMOylation, and beyond. J Mol Cell Cardiol. 2014;71:32-42. doi: 10.1016/j.yjmcc.2013.10.008.
38. Popelka H, Klionsky DJ. Post-translationally-modified structures in the autophagy machinery: an integrative perspective. FEBS J. 2015;282:3474-3488. doi: 10.1111/febs.13356.
39. van der Veen AG, Ploegh HL. Ubiquitin-like proteins. Annu Rev Biochem. 2012;81:323-357. doi: 10.1146/annurev-biochem-093010-153308.
40. Zhu H, Tannous P, Johnstone JL, Kong Y, Shelton JM, Richardson JA, Le V, Levine B, Rothermel BA, Hill JA. Cardiac autophagy is a maladaptive response to hemodynamic stress. J Clin Invest. 2007;117:1782-1793. doi: 10.1172/JCI27523.
41. Vicart P, Caron A, Guicheney P, Li Z, Prévost MC, Faure A, Chateau D, Chapon F, Tomé F, Dupret JM, Paulin D, Fardeau M. A missense mutation in the alphaB-crystallin chaperone gene causes a desmin-related myopathy. Nat Genet. 1998;20:92-95. doi: 10.1038/1765.
42. Wang X, Osinska H, Dorn GW 2nd, Nieman M, Lorenz JN, Gerdes AM, Witt S, Kimball T, Gulick J, Robbins J. Mouse model of desmin-related cardiomyopathy. Circulation. 2001;103:2402-2407.
43. Wang X, Osinska H, Klevitsky R, Gerdes AM, Nieman M, Lorenz J, Hewett T, Robbins J. Expression of R120G-alphaB-crystallin causes aberrant desmin and alphaB-crystallin aggregation and cardiomyopathy in mice. Circ Res. 2001;89:84-91.
44. Zee BM, Levin RS, Dimaggio PA, Garcia BA. Global turnover of histone post-translational modifications and variants in human cells. Epigenetics Chromatin. 2010;3:22. doi: 10.1186/1756-8935-3-22.
45. Liddy KA, White MY, Cordwell SJ. Functional decorations: post-translational modifications and heart disease delineated by targeted proteomics. Genome Med. 2013;5:20. doi: 10.1186/gm424.
46. Sadayappan S, Osinska H, Klevitsky R, Lorenz JN, Sargent M, Molkentin JD, Seidman CE, Seidman JG, Robbins J. Cardiac myosin binding protein C phosphorylation is cardioprotective. Proc Natl Acad Sci U S A. 2006;103:16918-16923. doi: 10.1073/pnas.0607069103.
47. Montpetit ML, Stocker PJ, Schwetz TA, et al. Regulated and aberrant glycosylation modulate cardiac electrical signaling. Proc Natl Acad Sci U S A. 2009;106:16517-16522.
48. Herrmann J, Lerman LO, Lerman A. Ubiquitin and ubiquitin-like proteins in protein regulation. Circ Res. 2007;100:1276-1291. doi: 10.1161/01. RES.0000264500.11888.f0.
49. Kho C, Lee A, Jeong D, Oh JG, Chaanine AH, Kizana E, Park WJ, Hajjar RJ. SUMO1-dependent modulation of SERCA2a in heart failure. Nature. 2011;477:601-605. doi: 10.1038/nature10407.
50. Zhao J. Sumoylation regulates diverse biological processes. Cell Mol Life Sci. 2007;64:3017-3033. doi: 10.1007/s00018-007-7137-4.
51. Wang J. Cardiac function and disease: emerging role of small ubiquitinrelated modifier. Wiley Interdiscip Rev Syst Biol Med. 2011;3:446-457. doi: 10.1002/wsbm.130.
52. Bellail AC, Olson JJ, Hao C. SUMO1 modification stabilizes CDK6 protein and drives the cell cycle and glioblastoma progression. Nat Commun. 2014;5:4234. doi: 10.1038/ncomms5234.
53. Tatham MH, Matic I, Mann M, Hay RT. Comparative proteomic analysis identifies a role for SUMO in protein quality control. Sci Signal. 2011;4:rs4. doi: 10.1126/scisignal.2001484.
54. Guzzo CM, Matunis MJ. Expanding SUMO and ubiquitin-mediated signaling through hybrid SUMO-ubiquitin chains and their receptors. Cell Cycle. 2013;12:1015-1017. doi: 10.4161/cc.24332.
55. Praefcke GJ, Hofmann K, Dohmen RJ. SUMO playing tag with ubiquitin. Trends Biochem Sci. 2012;37:23-31. doi: 10.1016/j.tibs.2011.09.002.
56. Wei W, Yang P, Pang J, Zhang S, Wang Y, Wang MH, Dong Z, She JX, Wang CY. A stress-dependent SUMO4 sumoylation of its substrate proteins. Biochem Biophys Res Commun. 2008;375:454-459. doi: 10.1016/j. bbrc.2008.08.028.
57. Nacerddine K, Lehembre F, Bhaumik M, Artus J, Cohen-Tannoudji M, Babinet C, Pandolfi PP, Dejean A. The SUMO pathway is essential for nuclear integrity and chromosome segregation in mice. Dev Cell. 2005;9:769-779. doi: 10.1016/j.devcel.2005.10.007.
58. Lim Y, Lee D, Kalichamy K, Hong SE, Michalak M, Ahnn J, Kim do H, Lee SK. Sumoylation regulates ER stress response by modulating calreticulin gene expression in XBP-1-dependent mode in Caenorhabditis elegans. Int J Biochem Cell Biol. 2014;53:399-408. doi: 10.1016/j.biocel.2014.06.005.
59. Krumova P, Meulmeester E, Garrido M, et al. Sumoylation inhibits alphasynuclein aggregation and toxicity. J Cell Biol. 2011;194:49-60.
60. Saito T, Sadoshima J. Molecular mechanisms of mitochondrial autophagy/ mitophagy in the heart. Circ Res. 2015;116:1477-1490. doi: 10.1161/ CIRCRESAHA.116.303790.
61. Mizushima N, Klionsky DJ. Protein turnover via autophagy: implications for metabolism. Annu Rev Nutr. 2007;27:19-40. doi: 10.1146/annurev. nutr.27.061406.093749.
62. Maloyan A, Robbins J. Autophagy in desmin-related cardiomyopathy: thoughts at the halfway point. Autophagy. 2010;6:665-666. doi: 10.1161/ CIRCRESAHA.109.212639.
63. Kim J, Kundu M, Viollet B, Guan KL. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol. 2011;13:132-141. doi: 10.1038/ncb2152.
64. Vekrellis K, Xilouri M, Emmanouilidou E, Rideout HJ, Stefanis L. Pathological roles of α-synuclein in neurological disorders. Lancet Neurol. 2011;10:1015-1025. doi: 10.1016/S1474-4422(11)70213-7.
65. Breydo L, Wu JW, Uversky VN. α-synuclein misfolding and Parkinson's disease. Biochim Biophys Acta. 2012;1822:261-285. doi: 10.1016/j. bbadis.2011.10.002.