The chromatin modification by SUMO-2/3 but not SUMO-1 prevents the epigenetic activation of key immune-related genes during Kaposi’s sarcoma associated herpesvirus reactivation

详细信息    查看全文

• 作者：Pei-Ching Chang (1)
  Chia-Yang Cheng (2) (3)
  Mel Campbell (4)
  Yi-Cheng Yang (1)
  Hung-Wei Hsu (1)
  Ting-Yu Chang (1)
  Chia-Han Chu (2)
  Yi-Wei Lee (1)
  Chiu-Lien Hung (5)
  Shi-Mei Lai (2)
  Clifford G Tepper (4) (6)
  Wen-Ping Hsieh (7)
  Hsei-Wei Wang (1)
  Chuan-Yi Tang (3)
  Wen-Ching Wang (2)
  Hsing-Jien Kung (4) (5) (6) (8)
  
• 刊名：BMC Genomics
• 出版年：2013
• 出版时间：December 2013
• 年：2013
• 卷：14
• 期：1
• 全文大小：1,636 KB
• 参考文献：1. Lomeli H, Vazquez M: Emerging roles of the SUMO pathway in development. / Cell Mol Life Sci 2011, 68:4045-064. CrossRef
  2. 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, 9:769-79. CrossRef
  3. Prudden J, Perry JJ, Nie M, Vashisht AA, Arvai AS, Hitomi C, Guenther G, Wohlschlegel JA, Tainer JA, Boddy MN: DNA repair and global sumoylation are regulated by distinct Ubc9 noncovalent complexes. / Mol Cell Biol 2011, 31:2299-310. CrossRef
  4. Garcia-Dominguez M, Reyes JC: SUMO association with repressor complexes, emerging routes for transcriptional control. / Biochim Biophys Acta 2009, 1789:451-59. CrossRef
  5. Wilkinson KA, Henley JM: Mechanisms, regulation and consequences of protein SUMOylation. / Biochem J 2010, 428:133-45. CrossRef
  6. Maison C, Bailly D, Roche D, Montes de Oca R, Probst AV, Vassias I, Dingli F, Lombard B, Loew D, Quivy JP, Almouzni G: SUMOylation promotes de novo targeting of HP1alpha to pericentric heterochromatin. / Nat Genet 2011, 43:220-27. CrossRef
  7. Rosonina E, Duncan SM, Manley JL: SUMO functions in constitutive transcription and during activation of inducible genes in yeast. / Genes Dev 2010, 24:1242-252. CrossRef
  8. 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, 33:124-35. CrossRef
  9. Tatham MH, Jaffray E, Vaughan OA, Desterro JM, Botting CH, Naismith JH, Hay RT: Polymeric chains of SUMO-2 and SUMO-3 are conjugated to protein substrates by SAE1/SAE2 and Ubc9. / J Biol Chem 2001, 276:35368-5374. CrossRef
  10. Matic I, van Hagen M, Schimmel J, Macek B, Ogg SC, Tatham MH, Hay RT, Lamond AI, Mann M, Vertegaal AC: In vivo identification of human small ubiquitin-like modifier polymerization sites by high accuracy mass spectrometry and an in vitro to in vivo strategy. / Mol Cell Proteomics 2008, 7:132-44. CrossRef
  11. Saitoh H, Hinchey J: Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3. / J Biol Chem 2000, 275:6252-258. CrossRef
  12. Ayaydin F, Dasso M: Distinct in vivo dynamics of vertebrate SUMO paralogues. / Mol Biol Cell 2004, 15:5208-218. CrossRef
  13. Kolli N, Mikolajczyk J, Drag M, Mukhopadhyay D, Moffatt N, Dasso M, Salvesen G, Wilkinson KD: Distribution and paralogue specificity of mammalian deSUMOylating enzymes. / Biochem J 2010, 430:335-44. CrossRef
  14. Lin DY, Huang YS, Jeng JC, Kuo HY, Chang CC, Chao TT, Ho CC, Chen YC, Lin TP, Fang HI, / et al.: Role of SUMO-interacting motif in Daxx SUMO modification, subnuclear localization, and repression of sumoylated transcription factors. / Mol Cell 2006, 24:341-54. CrossRef
  15. Namanja AT, Li YJ, Su Y, Wong S, Lu J, Colson LT, Wu C, Li SS, Chen Y: Insights into high affinity small ubiquitin-like modifier (SUMO) recognition by SUMO-interacting motifs (SIMs) revealed by a combination of NMR and peptide array analysis. / J Biol Chem 2012, 287:3231-240. CrossRef
  16. Chang PC, Izumiya Y, Wu CY, Fitzgerald LD, Campbell M, Ellison TJ, Lam KS, Luciw PA, Kung HJ: Kaposi’s sarcoma-associated herpesvirus (KSHV) encodes a SUMO E3 ligase that is SIM-dependent and SUMO-2/3-specific. / J Biol Chem 2010, 285:5266-273. CrossRef
  17. Gareau JR, Reverter D, Lima CD: Determinants of small ubiquitin-like modifier 1 (SUMO1) protein specificity, E3 ligase, and SUMO-RanGAP1 binding activities of nucleoporin RanBP2. / J Biol Chem 2012, 287:4740-751. CrossRef
  18. Tatham MH, Kim S, Jaffray E, Song J, Chen Y, Hay RT: Unique binding interactions among Ubc9, SUMO and RanBP2 reveal a mechanism for SUMO paralog selection. / Nat Struct Mol Biol 2005, 12:67-4. CrossRef
  19. Meulmeester E, Kunze M, Hsiao HH, Urlaub H, Melchior F: Mechanism and consequences for paralog-specific sumoylation of ubiquitin-specific protease 25. / Mol Cell 2008, 30:610-19. CrossRef
  20. Bailey D, O’Hare P: Herpes simplex virus 1 ICP0 co-localizes with a SUMO-specific protease. / J Gen Virol 2002, 83:2951-964.
  21. Boggio R, Chiocca S: Viruses and sumoylation: recent highlights. / Curr Opin Microbiol 2006, 9:430-36. CrossRef
  22. Boggio R, Colombo R, Hay RT, Draetta GF, Chiocca S: A mechanism for inhibiting the SUMO pathway. / Mol Cell 2004, 16:549-61. CrossRef
  23. Chang PC, Fitzgerald LD, Van Geelen A, Izumiya Y, Ellison TJ, Wang DH, Ann DK, Luciw PA, Kung HJ: Kruppel-associated box domain-associated protein-1 as a latency regulator for Kaposi’s sarcoma-associated herpesvirus and its modulation by the viral protein kinase. / Cancer Res 2009, 69:5681-689. CrossRef
  24. Chang TH, Kubota T, Matsuoka M, Jones S, Bradfute SB, Bray M, Ozato K: Ebola Zaire virus blocks type I interferon production by exploiting the host SUMO modification machinery. / PLoS Pathog 2009, 5:e1000493. CrossRef
  25. Izumiya Y, Ellison TJ, Yeh ET, Jung JU, Luciw PA, Kung HJ: Kaposi’s sarcoma-associated herpesvirus K-bZIP represses gene transcription via SUMO modification. / J Virol 2005, 79:9912-925. CrossRef
  26. Adamson AL, Kenney S: Epstein-barr virus immediate-early protein BZLF1 is SUMO-1 modified and disrupts promyelocytic leukemia bodies. / J Virol 2001, 75:2388-399. CrossRef
  27. Chang LK, Lee YH, Cheng TS, Hong YR, Lu PJ, Wang JJ, Wang WH, Kuo CW, Li SS, Liu ST: Post-translational modification of Rta of Epstein-Barr virus by SUMO-1. / J Biol Chem 2004, 279:38803-8812. CrossRef
  28. Chang LK, Liu ST, Kuo CW, Wang WH, Chuang JY, Bianchi E, Hong YR: Enhancement of transactivation activity of Rta of Epstein-Barr virus by RanBPM. / J Mol Biol 2008, 379:231-42. CrossRef
  29. Hagemeier SR, Dickerson SJ, Meng Q, Yu X, Mertz JE, Kenney SC: Sumoylation of the Epstein-Barr virus BZLF1 protein inhibits its transcriptional activity and is regulated by the virus-encoded protein kinase. / J Virol 2010, 84:4383-394. CrossRef
  30. Wimmer P, Schreiner S, Dobner T: Human pathogens and the host cell SUMOylation system. / J Virol 2012, 86:642-54. CrossRef
  31. Wen KW, Damania B: Kaposi sarcoma-associated herpesvirus (KSHV): molecular biology and oncogenesis. / Cancer Lett 2010, 289:140-50. CrossRef
  32. Moore PS, Chang Y: Why do viruses cause cancer? Highlights of the first century of human tumour virology. / Nat Rev Cancer 2010, 10:878-89. CrossRef
  33. Chang Y, Moore PS: Kaposi’s Sarcoma (KS)-associated herpesvirus and its role in KS. / Infect Agents Dis 1996, 5:215-22.
  34. Boshoff C, Schulz TF, Kennedy MM, Graham AK, Fisher C, Thomas A, McGee JO, Weiss RA, O’Leary JJ: Kaposi’s sarcoma-associated herpesvirus infects endothelial and spindle cells. / Nat Med 1995, 1:1274-278. CrossRef
  35. Coscoy L: Immune evasion by Kaposi’s sarcoma-associated herpesvirus. / Nat Rev Immunol 2007, 7:391-01. CrossRef
  36. Lee HR, Brulois K, Wong L, Jung JU: Modulation of immune system by Kaposi’s sarcoma-associated herpesvirus: lessons from viral evasion strategies. / Front Microbiol 2012, 3:44.
  37. Lefort S, Soucy-Faulkner A, Grandvaux N, Flamand L: Binding of Kaposi’s sarcoma-associated herpesvirus K-bZIP to interferon-responsive factor 3 elements modulates antiviral gene expression. / J Virol 2007, 81:10950-0960. CrossRef
  38. Yu Y, Wang SE, Hayward GS: The KSHV immediate-early transcription factor RTA encodes ubiquitin E3 ligase activity that targets IRF7 for proteosome-mediated degradation. / Immunity 2005, 22:59-0. CrossRef
  39. Lefort S, Gravel A, Flamand L: Repression of interferon-alpha stimulated genes expression by Kaposi’s sarcoma-associated herpesvirus K-bZIP protein. / Virology 2010, 408:14-0. CrossRef
  40. Bentz GL, Shackelford J, Pagano JS: Epstein-Barr virus latent membrane protein 1 regulates the function of interferon regulatory factor 7 by inducing its sumoylation. / J Virol 2012, 86:12251-2261. CrossRef
  41. Kubota T, Matsuoka M, Chang TH, Tailor P, Sasaki T, Tashiro M, Kato A, Ozato K: Virus infection triggers SUMOylation of IRF3 and IRF7, leading to the negative regulation of type I interferon gene expression. / J Biol Chem 2008, 283:25660-5670. CrossRef
  42. Richner JM, Clyde K, Pezda AC, Cheng BY, Wang T, Kumar GR, Covarrubias S, Coscoy L, Glaunsinger B: Global mRNA degradation during lytic gammaherpesvirus infection contributes to establishment of viral latency. / PLoS Pathog 2011, 7:e1002150. CrossRef
  43. Smiley JR: Herpes simplex virus virion host shutoff protein: immune evasion mediated by a viral RNase? / J Virol 2004, 78:1063-068. CrossRef
  44. Covarrubias S, Gaglia MM, Kumar GR, Wong W, Jackson AO, Glaunsinger BA: Coordinated destruction of cellular messages in translation complexes by the gammaherpesvirus host shutoff factor and the mammalian exonuclease Xrn1. / PLoS Pathog 2011, 7:e1002339. CrossRef
  45. Chang PC, Fitzgerald LD, Hsia DA, Izumiya Y, Wu CY, Hsieh WP, Lin SF, Campbell M, Lam KS, Luciw PA, / et al.: Histone demethylase JMJD2A regulates Kaposi’s sarcoma-associated herpesvirus replication and is targeted by a viral transcriptional factor. / J Virol 2011, 85:3283-293. CrossRef
  46. Liu HW, Zhang J, Heine GF, Arora M, Gulcin Ozer H, Onti-Srinivasan R, Huang K, Parvin JD: Chromatin modification by SUMO-1 stimulates the promoters of translation machinery genes. / Nucleic Acids Res 2012, 40:10172-0186. CrossRef
  47. Chang CC, Naik MT, Huang YS, Jeng JC, Liao PH, Kuo HY, Ho CC, Hsieh YL, Lin CH, Huang NJ, / et al.: Structural and functional roles of Daxx SIM phosphorylation in SUMO paralog-selective binding and apoptosis modulation. / Mol Cell 2011, 42:62-4. CrossRef
  48. Lyst MJ, Stancheva I: A role for SUMO modification in transcriptional repression and activation. / Biochem Soc Trans 2007, 35:1389-392. CrossRef
  49. Davies L, Gather U: The identification of multiple outliers. / J Am Stat Assoc 1993, 88:782-92. CrossRef
  50. Stielow B, Sapetschnig A, Kruger I, Kunert N, Brehm A, Boutros M, Suske G: Identification of SUMO-dependent chromatin-associated transcriptional repression components by a genome-wide RNAi screen. / Mol Cell 2008, 29:742-54. CrossRef
  51. Zhang XD, Goeres J, Zhang H, Yen TJ, Porter AC, Matunis MJ: SUMO-2/3 modification and binding regulate the association of CENP-E with kinetochores and progression through mitosis. / Mol Cell 2008, 29:729-41. CrossRef
  52. Liang Q, Deng H, Li X, Wu X, Tang Q, Chang TH, Peng H, Rauscher FJ 3rd, Ozato K, Zhu F: Tripartite motif-containing protein 28 is a small ubiquitin-related modifier E3 ligase and negative regulator of IFN regulatory factor 7. / J Immunol 2011, 187:4754-763. CrossRef
  53. Dunham I, Kundaje A, Aldred SF, Collins PJ, Davis CA, Doyle F, Epstein CB, Frietze S, Harrow J, Kaul R, / et al.: An integrated encyclopedia of DNA elements in the human genome. / Nature 2012, 489:57-4. CrossRef
  54. Cheng CY, Chu CH, Hsu HW, Hsu FR, Tang CY, Wang WC, Kung HJ, Chang PC: An improved ChIP-seq peak detection system for simultaneously identifying post-translational modified transcription factors by combinatorial fusion, using SUMOylation as an example. APBC2014 (Accepted)
  55. Marusic MB, Mencin N, Licen M, Banks L, Grm HS: Modification of human papillomavirus minor capsid protein L2 by sumoylation. / J Virol 2010, 84:11585-1589. CrossRef
  
• 作者单位：Pei-Ching Chang (1)
  Chia-Yang Cheng (2) (3)
  Mel Campbell (4)
  Yi-Cheng Yang (1)
  Hung-Wei Hsu (1)
  Ting-Yu Chang (1)
  Chia-Han Chu (2)
  Yi-Wei Lee (1)
  Chiu-Lien Hung (5)
  Shi-Mei Lai (2)
  Clifford G Tepper (4) (6)
  Wen-Ping Hsieh (7)
  Hsei-Wei Wang (1)
  Chuan-Yi Tang (3)
  Wen-Ching Wang (2)
  Hsing-Jien Kung (4) (5) (6) (8)
  
  1. Institute of Microbiology and Immunology, National Yang-Ming University, Taipei, 11221, Taiwan
  2. Institute of Molecular and Cellular Biology and Department of Life Science, National Tsing Hua University, Hsinchu, 300, Taiwan
  3. Department of Computer Science, National Tsing Hua University, Hsinchu, 300, Taiwan
  4. UC Davis Cancer Center, University of California, Davis, CA, 95616, USA
  5. Division of Molecular and Genomic Medicine, National Health Research Institutes, 35 Keyan Road, Zhunan, Miaoli County, 35053, Taiwan
  6. Department of Biochemistry and Molecular Medicine, University of California, Davis, CA, 95616, USA
  7. Institute of Statistics, National Tsing Hua University, Hsinchu, 300, Taiwan
  8. Institute for Translational Medicine, College of Medical Science and Technology, Taipei Medical University, 250 Wu-Xin Street, Taipei City, Taiwan
  
• ISSN：1471-2164

文摘

Background SUMOylation, as part of the epigenetic regulation of transcription, has been intensively studied in lower eukaryotes that contain only a single SUMO protein; however, the functions of SUMOylation during mammalian epigenetic transcriptional regulation are largely uncharacterized. Mammals express three major SUMO paralogues: SUMO-1, SUMO-2, and SUMO-3 (normally referred to as SUMO-1 and SUMO-2/3). Herpesviruses, including Kaposi’s sarcoma associated herpesvirus (KSHV), seem to have evolved mechanisms that directly or indirectly modulate the SUMO machinery in order to evade host immune surveillance, thus advancing their survival. Interestingly, KSHV encodes a SUMO E3 ligase, K-bZIP, with specificity toward SUMO-2/3 and is an excellent model for investigating the global functional differences between SUMO paralogues. Results We investigated the effect of experimental herpesvirus reactivation in a KSHV infected B lymphoma cell line on genomic SUMO-1 and SUMO-2/3 binding profiles together with the potential role of chromatin SUMOylation in transcription regulation. This was carried out via high-throughput sequencing analysis. Interestingly, chromatin immunoprecipitation sequencing (ChIP-seq) experiments showed that KSHV reactivation is accompanied by a significant increase in SUMO-2/3 modification around promoter regions, but SUMO-1 enrichment was absent. Expression profiling revealed that the SUMO-2/3 targeted genes are primarily highly transcribed genes that show no expression changes during viral reactivation. Gene ontology analysis further showed that these genes are involved in cellular immune responses and cytokine signaling. High-throughput annotation of SUMO occupancy of transcription factor binding sites (TFBS) pinpointed the presence of three master regulators of immune responses, IRF-1, IRF-2, and IRF-7, as potential SUMO-2/3 targeted transcriptional factors after KSHV reactivation. Conclusion Our study is the first to identify differential genome-wide SUMO modifications between SUMO paralogues during herpesvirus reactivation. Our findings indicate that SUMO-2/3 modification near protein-coding gene promoters occurs in order to maintain host immune-related gene unaltered during viral reactivation.