The Smc5/6 complex restricts HBV when localized to ND10 without inducing an innate immune response and is counteracted by the HBV X protein shortly after infection

PLoS ONE

Volumn 12, Issue 1, 2017, Pages

  Niu, Congrong ^a   Livingston, Christine M ^a   Li, Li ^a   Beran, Rudolf K ^a   Daffis, Stephane ^a   Ramakrishnan, Dhivya ^a   Burdette, Dara ^a   Peiser, Leanne ^a   Salas, Eduardo ^a   Ramos, Hilario ^a   Yu, Mei ^a   Cheng, Guofeng ^a   Strubin, Michel ^b   Delaney, William E ^a   Fletcher, Simon P ^a  

^a GILEAD SCIENCES   (United States)

^b UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMOSOME PROTEIN; CIRCULAR DNA; COVALENTLY CLOSED CIRCULAR DNA; HEPATITIS B VIRUS X PROTEIN; NUCLEAR DOMAIN 10; NUCLEAR PROTEIN; STRUCTURAL MAINTENANCE OF CHROMOSOME 5 PROTEIN; STRUCTURAL MAINTENANCE OF CHROMOSOME 6 PROTEIN; UNCLASSIFIED DRUG; AUTOANTIGEN; CELL CYCLE PROTEIN; CELL NUCLEUS ANTIGEN; CYTOKINE; NUCLEAR DOT PROTEIN 52, HUMAN; PML PROTEIN, HUMAN; PROMYELOCYTIC LEUKEMIA PROTEIN; SMC5 PROTEIN, HUMAN; SMC6 PROTEIN, HUMAN; SP100 PROTEIN, HUMAN; TRANSACTIVATOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHRONIC HEPATITIS B; CONTROLLED STUDY; ENZYME MECHANISM; ENZYME REPRESSION; HEPATITIS B VIRUS; HUMAN; HUMAN CELL; HUMAN TISSUE; INNATE IMMUNITY; LIMIT OF QUANTITATION; LIVER CELL; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; VIRUS PATHOGENESIS; VIRUS REPLICATION; ANIMAL; CELL CULTURE; CYTOLOGY; GENETICS; HEPATITIS B; IMMUNOLOGY; METABOLISM; SCID MOUSE; VIROLOGY;

ANIMALS; ANTIGENS, NUCLEAR; AUTOANTIGENS; CELL CYCLE PROTEINS; CELLS, CULTURED; CYTOKINES; HEPATITIS B; HEPATITIS B VIRUS; HEPATOCYTES; HUMANS; IMMUNITY, INNATE; MALE; MICE; MICE, SCID; NUCLEAR PROTEINS; PROMYELOCYTIC LEUKEMIA PROTEIN; TRANS-ACTIVATORS; VIRUS REPLICATION;

EID: 85009833721     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0169648     Document Type: Article

References (66)

1. Lozano R, Naghavi M, Foreman K, Lim S, Shibuya K, Aboyans V, et al. (2012) Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 380: 2095-2128. doi: 10.1016/S0140-6736(12)61728-0 PMID: 23245604
2. Schweitzer A, Horn J, Mikolajczyk RT, Krause G, Ott JJ (2015) Estimations of worldwide prevalence of chronic hepatitis B virus infection: a systematic review of data published between 1965 and 2013. Lancet 386:1546-1555. doi: 10.1016/S0140-6736(15)61412-X PMID: 26231459
3. Kwon H, Lok AS (2011) Hepatitis B therapy. Nat Rev Gastroenterol Hepatol 8: 275-284. doi: 10.1038/nrgastro.2011.33 PMID: 21423260
4. Chen HS, Kaneko S, Girones R, Anderson RW, Hornbuckle WE, Tennant BC, et al. (1993) The wood-chuck hepatitis virus X gene is important for establishment of virus infection in woodchucks. J Virol 67: 1218-1226. PMID: 8437213
5. Zoulim F, Saputelli J, Seeger C (1994) Woodchuck hepatitis virus X protein is required for viral infection in vivo. J Virol 68: 2026-2030. PMID: 8107266
6. Tsuge M, Hiraga N, Akiyama R, Tanaka S, Matsushita M, Mitsui F, et al. (2010) HBx protein is indispensable for development of viraemia in human hepatocyte chimeric mice. J Gen Virol 91:1854-1864. doi: 10.1099/vir.0.019224-0 PMID: 20219897
7. Lucifora J, Arzberger S, Durantel D, Belloni L, Strubin M, Levrero M, et al. (2011) Hepatitis B virus X protein is essential to initiate and maintain virus replication after infection. J Hepatol 55: 996-1003. doi: 10. 1016/j.jhep.2011.02.015 PMID: 21376091
8. van Breugel PC, Robert EI, Mueller H, Decorsiere A, Zoulim F, Hantz O, et al. (2012) Hepatitis B virusX protein stimulates gene expression selectively from extrachromosomal DNA templates. Hepatology 56: 2116-2124. doi: 10.1002/hep.25928 PMID: 22744635
9. Riviere L, Gerossier L, Ducroux A, Dion S, Deng Q, Michel ML, et al. (2015) HBx relieveschromatin-mediated transcriptional repression of hepatitis B viral cccDNA involving SETDB1 histone methyltrans-ferase. J Hepatol 63:1093-1102. doi: 10.1016/j.jhep.2015.06.023 PMID: 26143443
10. Bertoletti A, Ferrari C (2012) Innate and adaptive immune responses in chronic hepatitis B virus infections: towards restoration of immune control of viral infection. Gut 61:1754-1764. doi: 10.1136/gutjnl-2011-301073 PMID: 22157327
11. Levrero M, Zucman-Rossi J (2016) Mechanisms of HBV-induced hepatocellular carcinoma. J Hepatol 64: S84-S101. doi: 10.1016/j.jhep.2016.02.021 PMID: 27084040
12. Ringelhan M, Protzer U (2015) Oncogenic potential of hepatitis B virus encoded proteins. Curr Opin Virol 14:109-115. doi: 10.1016/j.coviro.2015.08.015 PMID: 26426688
13. Decorsière A, Mueller H, van Breugel PC, Abdul F, Gerossier L, Beran RK, et al. (2016) Hepatitis B virus X protein identifies the Smc5/6 complex as a host restriction factor. Nature 531:386-389. doi: 10. 1038/nature17170 PMID: 26983541
14. Ju L, Wing J, Taylor E, Brandt R, Slijepcevic P, Horsch M, et al. (2013) SMC6 is an essential gene in mice, but a hypomorphic mutant in the ATPase domain has a mild phenotype with a range of subtle abnormalities. DNA Repair (Amst) 12: 356-366.
15. Jacome A, Gutierrez-Martinez P, Schiavoni F, Tenaglia E, Martinez P, Rodriguez-Acebes S, et al. (2015) NSMCE2 suppresses cancer and aging in mice independently of its SUMO ligase activity. EMBO J 34: 2604-2619. doi: 10.15252/embj.201591829 PMID: 26443207
16. Wu N, Yu H (2012) The Smc complexes in DNA damage response. Cell Biosci 2: 5. doi: 10.1186/2045-3701-2-5 PMID: 22369641
17. Potts PR, Yu H (2007) The SMC5/6 complex maintains telomere length in ALT cancer cells through SUMOylation of telomere-binding proteins. Nat Struct Mol Biol 14: 581-590. doi: 10.1038/nsmb1259 PMID: 17589526
18. Bernardi R, Pandolfi PP (2007) Structure, dynamics and functions of promyelocytic leukaemia nuclear bodies. Nat Rev Mol Cell Biol 8:1006-1016. doi: 10.1038/nrm2277 PMID: 17928811
19. Lallemand-Breitenbach V, de The H (2010) PML nuclear bodies. Cold Spring Harb Perspect Biol 2: a000661. doi: 10.1101/cshperspect.a000661 PMID: 20452955
20. Everett RD, Chelbi-Alix MK (2007) PML and PML nuclear bodies: implications in antiviral defence. Bio-chimie 89: 819-830. doi: 10.1016/j.biochi.2007.01.004 PMID: 17343971
21. Tavalai N, Stamminger T (2008) New insights into the role of the subnuclear structure ND10 for viral infection. Biochim Biophys Acta 1783: 2207-2221. doi: 10.1016/j.bbamcr.2008.08.004 PMID: 18775455
22. Everett RD (2013) The spatial organization of DNA virus genomes in the nucleus. PLoS Pathog 9: e1003386. doi: 10.1371/journal.ppat. 1003386 PMID: 23825941
23. Chung YL, Tsai TY (2009) Promyelocytic leukemia nuclear bodies link the DNA damage repair pathway with hepatitis B virus replication: implications for hepatitis B virus exacerbation during chemotherapy and radiotherapy. Mol Cancer Res 7:1672-1685. doi: 10.1158/1541-7786.MCR-09-0112 PMID: 19808906
24. Diner BA, Lum KK, Cristea IM (2015) The emerging role of nuclear viral DNA sensors. J Biol Chem 290: 26412-26421. doi: 10.1074/jbc.R115.652289 PMID: 26354430
25. Belloni L, Allweiss L, Guerrieri F, Pediconi N, Volz T, Pollicino T, et al. (2012) IFN-alpha inhibits HBV transcription and replication in cell culture and in humanized mice by targeting the epigenetic regulation of the nuclear cccDNA minichromosome. J Clin Invest 122: 529-537. doi: 10.1172/JCI58847 PMID: 22251702
26. Kanno T, Berta DG, Sjogren C (2015) The Smc5/6 Complex Is an ATP-Dependent Intermolecular DNA Linker. Cell Rep 12:1471-1482. doi: 10.1016/j.celrep.2015.07.048 PMID: 26299966
27. Belloni L, Pollicino T, De Nicola F, Guerrieri F, Raffa G, Fanciulli M, et al. (2009) Nuclear HBx binds the HBV minichromosome and modifies the epigenetic regulation of cccDNA function. Proc Natl Acad Sci U SA 106:19975-19979. doi: 10.1073/pnas.0908365106 PMID: 19906987
28. Gripon P, Rumin S, Urban S, Le Seyec J, Glaise D, Cannie I, et al. (2002) Infection of a human hepatoma cell line by hepatitis B virus. Proc Natl Acad Sci USA 99:15655-15660. doi: 10.1073/pnas. 232137699 PMID: 12432097
29. Yan H, Zhong G, Xu G, He W, Jing Z, Gao Z, et al. (2012) Sodium taurocholate cotransporting polypeptide is a functional receptor for human hepatitis B and D virus. Elife 1: e00049. doi: 10.7554/eLife. 00049 PMID: 23150796
30. Shlomai A, Schwartz RE, Ramanan V, Bhatta A, de Jong YP, Bhatia SN, et al. (2014) Modeling host interactions with hepatitis B virus using primary and induced pluripotent stem cell-derived hepatocellular systems. Proc Natl Acad Sci USA 111:12193-12198. doi: 10.1073/pnas.1412631111 PMID: 25092305
31. Altinel K, Hashimoto K, Wei Y, Neuveut C, Gupta I, Suzuki AM, et al. (2016) Single-nucleotide-resolu-tion mapping of HBV promoters in infected human livers and hepatocellular carcinoma. J Virol.
32. Wang J, Shen T, Huang X, Kumar GR, Chen X, Zeng Z, et al. (2016) Serum hepatitis B virus RNA is encapsidated pregenome RNA that may be associated with persistence of viral infection and rebound. J Hepatol.
33. Thomsen MK, Nandakumar R, Stadler D, Malo A, Valls RM, Wang F, et al. (2016) Lack of immunological DNA sensing in hepatocytes facilitates hepatitis B virus infection. Hepatology.
34. Bertoletti A, Maini MK, Ferrari C (2010) The host-pathogen interaction during HBV infection: immuno-logical controversies. Antivir Ther 15 Suppl 3:15-24.
35. Murphy CM, Xu Y, Li F, Nio K, Reszka-Blanco N, Li X, et al. (2016) Hepatitis B Virus X Protein Promotes Degradation of SMC5/6 to Enhance HBV Replication. Cell Rep 16: 2846-2854. doi: 10.1016/j.celrep. 2016.08.026 PMID: 27626656
36. Tavalai N, Papior P, Rechter S, Stamminger T (2008) Nuclear domain 10 components promyelocytic leukemia protein and hDaxx independently contribute to an intrinsic antiviral defense against human cytomegalovirus infection. J Virol 82:126-137. doi: 10.1128/JVI.01685-07 PMID: 17942542
37. Glass M, Everett RD (2013) Components of promyelocytic leukemia nuclear bodies (ND10) act cooperatively to repress herpesvirus infection. J Virol 87:2174-2185. doi: 10.1128/JVI.02950-12 PMID: 23221561
38. Yan N, Chen ZJ (2012) Intrinsic antiviral immunity. Nat Immunol 13: 214-222. doi: 10.1038/ni.2229 PMID: 22344284
39. Simon V, Bloch N, Landau NR (2015) Intrinsic host restrictions to HIV-1 and mechanisms of viral escape. Nat Immunol 16: 546-553. doi: 10.1038/ni.3156 PMID: 25988886
40. Kegel A, Sjogren C (2010) The Smc5/6 complex: more than repair? Cold Spring Harb Symp Quant Biol 75: 179-187. doi: 10.1101/sqb.2010.75.047 PMID: 21467147
41. Carter SD, Sjogren C (2012) The SMC complexes, DNA and chromosome topology: right or knot? Crit Rev Biochem Mol Biol 47:1-16. doi: 10.3109/10409238.2011.614593 PMID: 21923481
42. Weitzman MD, Lilley CE, Chaurushiya MS (2010) Genomes in conflict: maintaining genome integrity during virus infection. Annu Rev Microbiol 64: 61-81. doi: 10.1146/annurev.micro.112408.134016 PMID: 20690823
43. Wieland SF, Chisari FV (2005) Stealth and cunning: hepatitis B and hepatitis C viruses. J Virol 79: 9369-9380. doi: 10.1128/JVI.79.15.9369-9380.2005 PMID: 16014900
44. Durantel D, Zoulim F (2009) Innate response to hepatitis B virus infection: observations challenging the concept of a stealth virus. Hepatology 50:1692-1695. doi: 10.1002/hep.23361 PMID: 19937686
45. Wieland S, Thimme R, Purcell RH, Chisari FV (2004) Genomic analysis of the host response to hepatitis B virus infection. Proc Natl Acad Sci USA 101: 6669-6674. doi: 10.1073/pnas.0401771101 PMID: 15100412
46. Fletcher SP, Chin DJ, Cheng DT, Ravindran P, Bitter H, Gruenbaum L, et al. (2013) Identification of an intrahepatic transcriptional signature associated with self-limiting infection in the woodchuck model of hepatitis B. Hepatology 57:13-22. doi: 10.1002/hep.25954 PMID: 22806943
47. Dunn C, Peppa D, Khanna P, Nebbia G, Jones M, Brendish N, et al. (2009) Temporal analysis of early immune responses in patients with acute hepatitis B virus infection. Gastroenterology 137:1289-1300. doi: 10.1053/j.gastro.2009.06.054 PMID: 19591831
48. Sato S, Li K, Kameyama T, Hayashi T, Ishida Y, Murakami S, et al. (2015) The RNA sensor RIG-I dually functions as an innate sensor and direct antiviral factor for hepatitis B virus. Immunity 42:123-132. doi: 10.1016/j.immuni.2014.12.016 PMID: 25557055
49. Giersch K, Allweiss L, Volz T, Helbig M, Bierwolf J, Lohse AW, et al. (2015) Hepatitis Delta co-infection in humanized mice leads to pronounced induction of innate immune responses in comparison to HBV mono-infection. J Hepatol 63: 346-353. doi: 10.1016/j.jhep.2015.03.011 PMID: 25795587
50. Luangsay S, Gruffaz M, Isorce N, Testoni B, Michelet M, Faure-Dupuy S, et al. (2015) Early inhibition of hepatocyte innate responses by hepatitis B virus. J Hepatol 63:1314-1322. doi: 10.1016/j.jhep.2015. 07.014 PMID: 26216533
51. Yoneda M, Hyun J, Jakubski S, Saito S, Nakajima A, Schiff ER, et al. (2016) Hepatitis B Virus and DNA Stimulation Trigger a Rapid Innate Immune Response through NF-kappaB. J Immunol 197: 630-643. doi: 10.4049/jimmunol.1502677 PMID: 27288535
52. Hosel M, Quasdorff M, Wiegmann K, Webb D, Zedler U, Broxtermann M, et al. (2009) Not interferon, but interleukin-6 controls early gene expression in hepatitis B virus infection. Hepatology 50:1773-1782. doi: 10.1002/hep.23226 PMID: 19937696
53. Boltjes A, van Montfoort N, Biesta PJ, Op den Brouw ML, Kwekkeboom J, van der Laan LJ, et al. (2015) Kupffer cells interact with hepatitis B surface antigen in vivo and in vitro, leading to proinflammatory cytokine production and natural killer cell function. J Infect Dis 211:1268-1278. doi: 10.1093/infdis/jiu599 PMID: 25362194
54. Martin-Lluesma S, Schaeffer C, Robert EI, van Breugel PC, Leupin O, Hantz O, et al. (2008) Hepatitis B virus X protein affects S phase progression leading to chromosome segregation defects by binding to damaged DNA binding protein 1. Hepatology 48:1467-1476. doi: 10.1002/hep.22542 PMID: 18781669
55. Gallego-Paez LM, Tanaka H, Bando M, Takahashi M, Nozaki N, Nakato R, et al. (2014) Smc5/6-medi-ated regulation of replication progression contributes to chromosome assembly during mitosis in human cells. Mol Biol Cell 25: 302-317. doi: 10.1091/mbc.E13-01-0020 PMID: 24258023
56. Chisari FV, Isogawa M, Wieland SF (2010) Pathogenesis of hepatitis B virus infection. Pathol Biol (Paris) 58: 258-266.
57. Ancey PB, Testoni B, Gruffaz M, Cros MP, Durand G, Le Calvez-Kelm F, et al. (2015) Genomic responses to hepatitis B virus (HBV) infection in primary human hepatocytes. Oncotarget 6: 44877-44891. doi: 10.18632/oncotarget.6270 PMID: 26565721
58. Lamontagne J, Mell JC, Bouchard MJ (2016) Transcriptome-Wide Analysis of Hepatitis B Virus-Medi-ated Changes to Normal Hepatocyte Gene Expression. PLoS Pathog 12: e1005438. doi: 10.1371/journal.ppat.1005438 PMID: 26891448
59. Oehler N, Volz T, Bhadra OD, Kah J, Allweiss L, Giersch K, et al. (2014) Binding of hepatitis B virus to its cellular receptor alters the expression profile of genes of bile acid metabolism. Hepatology 60: 1483-1493. doi: 10.1002/hep.27159 PMID: 24711282
60. Ladner SK, Otto MJ, Barker CS, Zaifert K, Wang GH, Guo JT, et al. (1997) Inducible expression of human hepatitis B virus (HBV) in stably transfected hepatoblastoma cells: a novel system for screening potential inhibitors of HBV replication. Antimicrob Agents Chemother 41:1715-1720. PMID: 9257747
61. Cai D, Nie H, Yan R, Guo JT, Block TM, Guo H (2013) A southern blot assay for detection of hepatitis B virus covalently closed circular DNAfrom cell cultures. Methods Mol Biol 1030:151-161. doi: 10.1007/978-1-62703-484-5 13 PMID: 23821267
62. Menne S, Tumas DB, Liu KH, Thampi L, AlDeghaither D, Baldwin BH, et al. (2015) Sustained efficacy and seroconversion with the Toll-like receptor 7 agonist GS-9620 in the Woodchuck model of chronic hepatitis B. J Hepatol 62:1237-1245. doi: 10.1016/j.jhep.2014.12.026 PMID: 25559326
63. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, et al. (2013) STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29:15-21. doi: 10.1093/bioinformatics/bts635 PMID: 23104886
64. Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139-140. doi: 10.1093/bioinformatics/btp616 PMID: 19910308
65. Law CW, Chen Y, Shi W, Smyth GK (2014) voom: Precision weights unlock linear model analysis tools for RNA-seq read counts. Genome Biol 15: R29. doi: 10.1186/gb-2014-15-2-r29 PMID: 24485249
66. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Statist Soc Ser B (Methodological) 57: 289-300.