K-bZIP Mediated SUMO-2/3 Specific Modification on the KSHV Genome Negatively Regulates Lytic Gene Expression and Viral Reactivation

PLoS Pathogens

Volumn 11, Issue 7, 2015, Pages

  Yang, Wan Shan ^a   Hsu, Hung Wei ^a   Campbell, Mel ^b   Cheng, Chia Yang ^a   Chang, Pei Ching ^a,c  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; SUMO 2 PROTEIN; SUMO 3 PROTEIN; UBIQUITIN PROTEIN LIGASE E3; SUMO PROTEIN; SUMO2 PROTEIN, HUMAN; SUMO3 PROTEIN, HUMAN; UBIQUITIN; VIRAL PROTEIN;

ANIMAL CELL; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; EPIGENETICS; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; NONHUMAN; PROTEIN BINDING; PROTEIN MODIFICATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; SEQUENCE ANALYSIS; SOUTHERN BLOTTING; TRANSCRIPTION REGULATION; VIRAL GENETICS; VIRUS GENOME; VIRUS REACTIVATION; CELL LINE; GENE EXPRESSION REGULATION; GENETICS; HERPES VIRUS INFECTION; METABOLISM; PROCEDURES; VIROLOGY; VIRUS ACTIVATION; VIRUS LATENCY;

HERPESVIRIDAE; HUMAN HERPESVIRUS 8;

BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CELL LINE; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION REGULATION, VIRAL; GENOME, VIRAL; HERPESVIRIDAE INFECTIONS; HERPESVIRUS 8, HUMAN; HUMANS; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; UBIQUITINS; VIRAL PROTEINS; VIRUS ACTIVATION; VIRUS LATENCY;

EID: 84938781131     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005051     Document Type: Article

References (59)

1. Garcia-Dominguez M, Reyes JC, (2009) SUMO association with repressor complexes, emerging routes for transcriptional control. Biochim Biophys Acta 1789: 451–459. doi: 10.1016/j.bbagrm.2009.07.001 19616654
2. Gill G, (2010) SUMO weighs in on polycomb-dependent gene repression. Mol Cell 38: 157–159. doi: 10.1016/j.molcel.2010.04.006 20417594
3. Maison C, Bailly D, Roche D, Montes de Oca R, Probst AV, et al. (2011) SUMOylation promotes de novo targeting of HP1alpha to pericentric heterochromatin. Nat Genet 43: 220–227. doi: 10.1038/ng.765 21317888
4. Cubenas-Potts C, Matunis MJ, (2013) SUMO: a multifaceted modifier of chromatin structure and function. Dev Cell 24: 1–12. doi: 10.1016/j.devcel.2012.11.020 23328396
5. Rosonina E, Duncan SM, Manley JL, (2010) SUMO functions in constitutive transcription and during activation of inducible genes in yeast. Genes Dev 24: 1242–1252. doi: 10.1101/gad.1917910 20504900
6. Tatham MH, Jaffray E, Vaughan OA, Desterro JM, Botting CH, et al. (2001) Polymeric chains of SUMO-2 and SUMO-3 are conjugated to protein substrates by SAE1/SAE2 and Ubc9. J Biol Chem 276: 35368–35374. 11451954
7. Matic I, van Hagen M, Schimmel J, Macek B, Ogg SC, et al. (2008) 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 7: 132–144. 17938407
8. Ayaydin F, Dasso M, (2004) Distinct in vivo dynamics of vertebrate SUMO paralogues. Mol Biol Cell 15: 5208–5218. 15456902
9. 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. 10692421
10. Chang PC, Cheng CY, Campbell M, Yang YC, Hsu HW, et al. (2013) 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. BMC Genomics 14: 824. doi: 10.1186/1471-2164-14-824 24267727
11. Liu HW, Zhang J, Heine GF, Arora M, Gulcin Ozer H, et al. (2012) Chromatin modification by SUMO-1 stimulates the promoters of translation machinery genes. Nucleic Acids Res 40: 10172–10186. doi: 10.1093/nar/gks819 22941651
12. Neyret-Kahn H, Benhamed M, Ye T, Le Gras S, Cossec JC, et al. (2013) Sumoylation at chromatin governs coordinated repression of a transcriptional program essential for cell growth and proliferation. Genome Res 23: 1563–1579. doi: 10.1101/gr.154872.113 23893515
13. Wen KW, Damania B, (2010) Kaposi sarcoma-associated herpesvirus (KSHV): molecular biology and oncogenesis. Cancer Lett 289: 140–150. doi: 10.1016/j.canlet.2009.07.004 19651473
14. Staskus KA, Zhong W, Gebhard K, Herndier B, Wang H, et al. (1997) Kaposi's sarcoma-associated herpesvirus gene expression in endothelial (spindle) tumor cells. J Virol 71: 715–719. 8985403
15. Chang Y, Moore PS, (1996) Kaposi's Sarcoma (KS)-associated herpesvirus and its role in KS. Infect Agents Dis 5: 215–222. 8884366
16. Whitby D, Howard MR, Tenant-Flowers M, Brink NS, Copas A, et al. (1995) Detection of Kaposi sarcoma associated herpesvirus in peripheral blood of HIV-infected individuals and progression to Kaposi's sarcoma. Lancet 346: 799–802. 7674745
17. Chang PC, Fitzgerald LD, Hsia DA, Izumiya Y, Wu CY, et al. (2011) Histone demethylase JMJD2A regulates Kaposi's sarcoma-associated herpesvirus replication and is targeted by a viral transcriptional factor. J Virol 85: 3283–3293. doi: 10.1128/JVI.02485-10 21228229
18. Gunther T, Grundhoff A, (2010) The epigenetic landscape of latent Kaposi sarcoma-associated herpesvirus genomes. PLoS Pathog 6: e1000935. doi: 10.1371/journal.ppat.1000935 20532208
19. Toth Z, Brulois K, Lee HR, Izumiya Y, Tepper C, et al. (2013) Biphasic euchromatin-to-heterochromatin transition on the KSHV genome following de novo infection. PLoS Pathog 9: e1003813. doi: 10.1371/journal.ppat.1003813 24367262
20. Toth Z, Maglinte DT, Lee SH, Lee HR, Wong LY, et al. (2010) Epigenetic analysis of KSHV latent and lytic genomes. PLoS Pathog 6: e1001013. doi: 10.1371/journal.ppat.1001013 20661424
21. Gareau JR, Reverter D, Lima CD, (2012) Determinants of Small Ubiquitin-like Modifier 1 (SUMO1) Protein Specificity, E3 Ligase, and SUMO-RanGAP1 Binding Activities of Nucleoporin RanBP2. J Biol Chem 287: 4740–4751. doi: 10.1074/jbc.M111.321141 22194619
22. Tatham MH, Kim S, Jaffray E, Song J, Chen Y, 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. 15608651
23. Namanja AT, Li YJ, Su Y, Wong S, Lu J, et al. (2012) 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 287: 3231–3240. doi: 10.1074/jbc.M111.293118 22147707
24. Everett RD, Boutell C, Hale BG, (2013) Interplay between viruses and host sumoylation pathways. Nat Rev Microbiol 11: 400–411. doi: 10.1038/nrmicro3015 23624814
25. Wimmer P, Schreiner S, Dobner T, (2012) Human pathogens and the host cell SUMOylation system. J Virol 86: 642–654. doi: 10.1128/JVI.06227-11 22072786
26. Mattoscio D, Segre CV, Chiocca S, (2013) Viral manipulation of cellular protein conjugation pathways: The SUMO lesson. World J Virol 2: 79–90. doi: 10.5501/wjv.v2.i2.79 24175232
27. Chang PC, Izumiya Y, Wu CY, Fitzgerald LD, Campbell M, et al. (2010) Kaposi's sarcoma-associated herpesvirus (KSHV) encodes a SUMO E3 ligase that is SIM-dependent and SUMO-2/3-specific. J Biol Chem 285: 5266–5273. doi: 10.1074/jbc.M109.088088 20034935
28. Krishnan HH, Sharma-Walia N, Zeng L, Gao SJ, Chandran B, (2005) Envelope glycoprotein gB of Kaposi's sarcoma-associated herpesvirus is essential for egress from infected cells. J Virol 79: 10952–10967. 16103147
29. Krishnan HH, Naranatt PP, Smith MS, Zeng L, Bloomer C, et al. (2004) Concurrent expression of latent and a limited number of lytic genes with immune modulation and antiapoptotic function by Kaposi's sarcoma-associated herpesvirus early during infection of primary endothelial and fibroblast cells and subsequent decline of lytic gene expression. J Virol 78: 3601–3620. 15016882
30. Myoung J, Ganem D, (2011) Generation of a doxycycline-inducible KSHV producer cell line of endothelial origin: maintenance of tight latency with efficient reactivation upon induction. J Virol Methods 174: 12–21. doi: 10.1016/j.jviromet.2011.03.012 21419799
31. Nakamura H, Lu M, Gwack Y, Souvlis J, Zeichner SL, et al. (2003) Global changes in Kaposi's sarcoma-associated virus gene expression patterns following expression of a tetracycline-inducible Rta transactivator. J Virol 77: 4205–4220. 12634378
32. Ellison TJ, Izumiya Y, Izumiya C, Luciw PA, Kung HJ, (2009) A comprehensive analysis of recruitment and transactivation potential of K-Rta and K-bZIP during reactivation of Kaposi's sarcoma-associated herpesvirus. Virology 387: 76–88. doi: 10.1016/j.virol.2009.02.016 19269659
33. Brulois KF, Chang H, Lee AS, Ensser A, Wong LY, et al. (2012) Construction and manipulation of a new Kaposi's sarcoma-associated herpesvirus bacterial artificial chromosome clone. J Virol 86: 9708–9720. doi: 10.1128/JVI.01019-12 22740391
34. Martinez FP, Tang Q, (2012) Leucine zipper domain is required for Kaposi sarcoma-associated herpesvirus (KSHV) K-bZIP protein to interact with histone deacetylase and is important for KSHV replication. J Biol Chem 287: 15622–15634. doi: 10.1074/jbc.M111.315861 22416134
35. Lefort S, Flamand L, (2009) Kaposi's sarcoma-associated herpesvirus K-bZIP protein is necessary for lytic viral gene expression, DNA replication, and virion production in primary effusion lymphoma cell lines. J Virol 83: 5869–5880. doi: 10.1128/JVI.01821-08 19321621
36. Wang Y, Sathish N, Hollow C, Yuan Y, (2011) Functional characterization of Kaposi's sarcoma-associated herpesvirus open reading frame K8 by bacterial artificial chromosome-based mutagenesis. J Virol 85: 1943–1957. doi: 10.1128/JVI.02060-10 21159864
37. Gangappa S, Kapadia SB, Speck SH, Virgin HWt, (2002) Antibody to a lytic cycle viral protein decreases gammaherpesvirus latency in B-cell-deficient mice. J Virol 76: 11460–11468. 12388707
38. Moser JM, Farrell ML, Krug LT, Upton JW, Speck SH, (2006) A gammaherpesvirus 68 gene 50 null mutant establishes long-term latency in the lung but fails to vaccinate against a wild-type virus challenge. J Virol 80: 1592–1598. 16415035
39. Ganem D, (2010) KSHV and the pathogenesis of Kaposi sarcoma: listening to human biology and medicine. J Clin Invest 120: 939–949. doi: 10.1172/JCI40567 20364091
40. Mesri EA, Cesarman E, Boshoff C, (2010) Kaposi's sarcoma and its associated herpesvirus. Nat Rev Cancer 10: 707–719. doi: 10.1038/nrc2888 20865011
41. Palmeri D, Spadavecchia S, Carroll KD, Lukac DM, (2007) Promoter- and cell-specific transcriptional transactivation by the Kaposi's sarcoma-associated herpesvirus ORF57/Mta protein. J Virol 81: 13299–13314. 17913801
42. Guito J, Lukac DM, (2012) KSHV Rta Promoter Specification and Viral Reactivation. Front Microbiol 3: 30. doi: 10.3389/fmicb.2012.00030 22347875
43. Feng WH, Hong G, Delecluse HJ, Kenney SC, (2004) Lytic induction therapy for Epstein-Barr virus-positive B-cell lymphomas. J Virol 78: 1893–1902. 14747554
44. Fu DX, Tanhehco Y, Chen J, Foss CA, Fox JJ, et al. (2008) Bortezomib-induced enzyme-targeted radiation therapy in herpesvirus-associated tumors. Nat Med 14: 1118–1122. doi: 10.1038/nm.1864 18776891
45. Dillon PJ, Gregory SM, Tamburro K, Sanders MK, Johnson GL, et al. (2013) Tousled-like kinases modulate reactivation of gammaherpesviruses from latency. Cell Host Microbe 13: 204–214. doi: 10.1016/j.chom.2012.12.005 23414760
46. Archin NM, Margolis DM, (2014) Emerging strategies to deplete the HIV reservoir. Curr Opin Infect Dis 27: 29–35. doi: 10.1097/QCO.0000000000000026 24296585
47. Chen J, Ueda K, Sakakibara S, Okuno T, Parravicini C, et al. (2001) Activation of latent Kaposi's sarcoma-associated herpesvirus by demethylation of the promoter of the lytic transactivator. Proc Natl Acad Sci U S A 98: 4119–4124. 11274437
48. Lu F, Zhou J, Wiedmer A, Madden K, Yuan Y, et al. (2003) Chromatin remodeling of the Kaposi's sarcoma-associated herpesvirus ORF50 promoter correlates with reactivation from latency. J Virol 77: 11425–11435. 14557628
49. Yu Y, Black JB, Goldsmith CS, Browning PJ, Bhalla K, et al. (1999) Induction of human herpesvirus-8 DNA replication and transcription by butyrate and TPA in BCBL-1 cells. J Gen Virol 80 (Pt 1): 83–90. 9934688
50. Cai Q, Cai S, Zhu C, Verma SC, Choi JY, et al. (2013) A unique SUMO-2-interacting motif within LANA is essential for KSHV latency. PLoS Pathog 9: e1003750. doi: 10.1371/journal.ppat.1003750 24278015
51. Izumiya Y, Ellison TJ, Yeh ET, Jung JU, Luciw PA, et al. (2005) Kaposi's sarcoma-associated herpesvirus K-bZIP represses gene transcription via SUMO modification. J Virol 79: 9912–9925. 16014952
52. Lefort S, Soucy-Faulkner A, Grandvaux N, Flamand L, (2007) Binding of Kaposi's sarcoma-associated herpesvirus K-bZIP to interferon-responsive factor 3 elements modulates antiviral gene expression. J Virol 81: 10950–10960. 17652396
53. Kim ET, Kim YE, Huh YH, Ahn JH, (2010) Role of noncovalent SUMO binding by the human cytomegalovirus IE2 transactivator in lytic growth. J Virol 84: 8111–8123. doi: 10.1128/JVI.00459-10 20519406
54. Rossetto C, Yamboliev I, Pari GS, (2009) Kaposi's sarcoma-associated herpesvirus/human herpesvirus 8 K-bZIP modulates latency-associated nuclear protein-mediated suppression of lytic origin-dependent DNA synthesis. J Virol 83: 8492–8501. doi: 10.1128/JVI.00922-09 19553319
55. Lin CL, Li H, Wang Y, Zhu FX, Kudchodkar S, et al. (2003) Kaposi's sarcoma-associated herpesvirus lytic origin (ori-Lyt)-dependent DNA replication: identification of the ori-Lyt and association of K8 bZip protein with the origin. J Virol 77: 5578–5588. 12719550
56. Wang Y, Li H, Chan MY, Zhu FX, Lukac DM, et al. (2004) Kaposi's sarcoma-associated herpesvirus ori-Lyt-dependent DNA replication: cis-acting requirements for replication and ori-Lyt-associated RNA transcription. J Virol 78: 8615–8629. 15280471
57. AuCoin DP, Colletti KS, Cei SA, Papouskova I, Tarrant M, et al. (2004) Amplification of the Kaposi's sarcoma-associated herpesvirus/human herpesvirus 8 lytic origin of DNA replication is dependent upon a cis-acting AT-rich region and an ORF50 response element and the trans-acting factors ORF50 (K-Rta) and K8 (K-bZIP). Virology 318: 542–555. 14972523
58. Kato-Noah T, Xu Y, Rossetto CC, Colletti K, Papouskova I, et al. (2007) Overexpression of the kaposi's sarcoma-associated herpesvirus transactivator K-Rta can complement a K-bZIP deletion BACmid and yields an enhanced growth phenotype. J Virol 81: 13519–13532. 17913803
59. Izumiya Y, Kobayashi K, Kim KY, Pochampalli M, Izumiya C, et al. (2013) Kaposi's sarcoma-associated herpesvirus K-Rta exhibits SUMO-targeting ubiquitin ligase (STUbL) like activity and is essential for viral reactivation. PLoS Pathog 9: e1003506. doi: 10.1371/journal.ppat.1003506 23990779