BMB Reports

Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
권호 표지
DOI QR코드

DOI QR Code

Topological implications of DNA tumor viral episomes

  • Eui Tae, Kim (Department of Microbiology and Immunology, Jeju National University College of Medicine) ;
  • Kyoung-Dong, Kim (Department of Systems Biotechnology, Chung-Ang University)
  • Received : 2022.09.21
  • Accepted : 2022.11.15
  • Published : 2022.12.31
Download PDF
⟨ Previous Next ⟩

Abstract

A persistent DNA tumor virus infection transforms normal cells into cancer cells by either integrating its genome into host chromosomes or retaining it as an extrachromosomal entity called episome. Viruses have evolved mechanisms for attaching episomes to infected host cell chromatin to efficiently segregate the viral genome during mitosis. It has been reported that viral episome can affect the gene expression of the host chromosomes through interactions between viral episomes and epigenetic regulatory host factors. This mini review summarizes our current knowledge of the tethering sites of viral episomes, such as EBV, KSHV, and HBV, on host chromosomes analyzed by three-dimensional genomic tools.

Keywords

Acknowledgement

This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Ministry of Science and ICT, Republic of Korea (No. 2019R1F1A1061826, 2019R1A4A1024764, 2022R1A2C100442311 and 2021R1A2C1010 313) and the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (KHIDI) funded by the Ministry of Health & Welfare, Republic of Korea (No. HI22C1510).

References

  1. Lieberman PM (2013) Keeping it quiet: chromatin control of gammaherpesvirus latency. Nat Rev Microbiol 11, 863-875 https://doi.org/10.1038/nrmicro3135
  2. Lieberman PM (2016) Epigenetics and genetics of viral latency. Cell Host Microbe 19, 619-628 https://doi.org/10.1016/j.chom.2016.04.008
  3. Crosbie EJ, Einstein MH, Franceschi S and Kitchener HC (2013) Human papillomavirus and cervical cancer. Lancet 382, 889-899 https://doi.org/10.1016/S0140-6736(13)60022-7
  4. Goncalves PH, Ziegelbauer J, Uldrick TS and Yarchoan R (2017) Kaposi sarcoma herpesvirus-associated cancers and related diseases. Curr Opin HIV AIDS 12, 47-56 https://doi.org/10.1097/COH.0000000000000330
  5. Matsukura T, Koi S and Sugase M (1989) Both episomal and integrated forms of human papillomavirus type 16 are involved in invasive cervical cancers. Virology 172, 63-72 https://doi.org/10.1016/0042-6822(89)90107-4
  6. Okabe A, Huang KK, Matsusaka K et al (2020) Cross-species chromatin interactions drive transcriptional rewiring in Epstein-Barr virus-positive gastric adenocarcinoma. Nat Genet 52, 919-930 https://doi.org/10.1038/s41588-020-0665-7
  7. Chakravorty A, Sugden B and Johannsen EC (2019) An epigenetic journey: Epstein-Barr virus transcribes chromatinized and subsequently unchromatinized templates during its lytic cycle. J Virol 93, e02247-18 https://doi.org/10.1128/jvi.masthead.93-19
  8. Mrozek-Gorska P, Buschle A, Pich D et al (2019) Epstein-Barr virus reprograms human B lymphocytes immediately in the prelatent phase of infection. Proc Natl Acad Sci U S A 116, 16046-16055 https://doi.org/10.1073/pnas.1901314116
  9. Chang Y, Cesarman E, Pessin MS et al (1994) Identification of herpesvirus-like DNA sequences in AIDSassociated Kaposi's sarcoma. Science 266, 1865-1869 https://doi.org/10.1126/science.7997879
  10. Purushothaman P, Dabral P, Gupta N, Sarkar R and Verma SC (2016) KSHV genome replication and maintenance. Front Microbiol 7, 54
  11. Ueda K, Sakakibara S, Ohsaki E and Yada K (2006) Lack of a mechanism for faithful partition and maintenance of the KSHV genome. Virus Res 122, 85-94 https://doi.org/10.1016/j.virusres.2006.07.002
  12. Lu F, Day L, Gao SJ and Lieberman PM (2006) Acetylation of the latency-associated nuclear antigen regulates repression of Kaposi's sarcoma-associated herpesvirus lytic transcription. J Virol 80, 5273-5282 https://doi.org/10.1128/JVI.02541-05
  13. Zhu FX, Cusano T and Yuan Y (1999) Identification of the immediate-early transcripts of Kaposi's sarcoma-associated herpesvirus. J Virol 73, 5556-5567 https://doi.org/10.1128/jvi.73.7.5556-5567.1999
  14. Jenner RG, Alba MM, Boshoff C and Kellam P (2001) Kaposi's sarcoma-associated herpesvirus latent and lytic gene expression as revealed by DNA arrays. J Virol 75, 891-902 https://doi.org/10.1128/JVI.75.2.891-902.2001
  15. Toth Z, Brulois K, Lee HR et al (2013) Biphasic euchromatin-to-heterochromatin transition on the KSHV genome following de novo infection. PLoS Pathog 9, e1003813
  16. Tu T, Budzinska MA, Vondran FWR, Shackel NA and Urban S (2018) Hepatitis B virus DNA integration occurs early in the viral life cycle in an in vitro infection model via sodium taurocholate cotransporting polypeptide-dependent uptake of enveloped virus particles. J Virol 92, e02007-17
  17. Tuttleman JS, Pourcel C and Summers J (1986) Formation of the pool of covalently closed circular viral DNA in hepadnavirus-infected cells. Cell 47, 451-460 https://doi.org/10.1016/0092-8674(86)90602-1
  18. Allweiss L, Volz T, Giersch K et al (2018) Proliferation of primary human hepatocytes and prevention of hepatitis B virus reinfection efficiently deplete nuclear cccDNA in vivo. Gut 67, 542-552 https://doi.org/10.1136/gutjnl-2016-312162
  19. Pyeon D, Pearce SM, Lank SM, Ahlquist P and Lambert PF (2009) Establishment of human papillomavirus infection requires cell cycle progression. PLoS Pathog 5, e1000318
  20. Lieberman PM (2014) Virology. Epstein-Barr virus turns 50. Science 343, 1323-1325 https://doi.org/10.1126/science.1252786
  21. Jones CH, Hayward SD and Rawlins DR (1989) Interaction of the lymphocyte-derived Epstein-Barr virus nuclear antigen EBNA-1 with its DNA-binding sites. J Virol 63, 101-110 https://doi.org/10.1128/jvi.63.1.101-110.1989
  22. Rawlins DR, Milman G, Hayward SD and Hayward GS (1985) Sequence-specific DNA binding of the Epstein-Barr virus nuclear antigen (EBNA-1) to clustered sites in the plasmid maintenance region. Cell 42, 859-868 https://doi.org/10.1016/0092-8674(85)90282-x
  23. Ambinder RF, Shah WA, Rawlins DR, Hayward GS and Hayward SD (1990) Definition of the sequence requirements for binding of the EBNA-1 protein to its palindromic target sites in Epstein-Barr virus DNA. J Virol 64, 2369-2379 https://doi.org/10.1128/jvi.64.5.2369-2379.1990
  24. Morgan SM, Tanizawa H, Caruso LB et al (2022) The three-dimensional structure of Epstein-Barr virus genome varies by latency type and is regulated by PARP1 enzymatic activity. Nat Commun 13, 187
  25. Jourdan N, Jobart-Malfait A, Dos Reis G et al (2012) Live-cell imaging reveals multiple interactions between Epstein-Barr virus nuclear antigen 1 and cellular chromatin during interphase and mitosis. J Virol 86, 5314-5329 https://doi.org/10.1128/JVI.06303-11
  26. Deschamps T, Bazot Q, Leske DM et al (2017) Epstein-Barr virus nuclear antigen 1 interacts with regulator of chromosome condensation 1 dynamically throughout the cell cycle. J Gen Virol 98, 251-265 https://doi.org/10.1099/jgv.0.000681
  27. Lin A, Wang S, Nguyen T, Shire K and Frappier L (2008) The EBNA1 protein of Epstein-Barr virus functionally interacts with Brd4. J Virol 82, 12009-12019 https://doi.org/10.1128/JVI.01680-08
  28. Shire K, Ceccarelli DF, Avolio-Hunter TM and Frappier L (1999) EBP2, a human protein that interacts with sequences of the Epstein-Barr virus nuclear antigen 1 important for plasmid maintenance. J Virol 73, 2587-2595 https://doi.org/10.1128/jvi.73.4.2587-2595.1999
  29. Cotter MA, 2nd and Robertson ES (1999) The latency-associated nuclear antigen tethers the Kaposi's sarcoma-associated herpesvirus genome to host chromosomes in body cavity-based lymphoma cells. Virology 264, 254-264 https://doi.org/10.1006/viro.1999.9999
  30. Barbera AJ, Chodaparambil JV, Kelley-Clarke B et al (2006) The nucleosomal surface as a docking station for Kaposi's sarcoma herpesvirus LANA. Science 311, 856-861 https://doi.org/10.1126/science.1120541
  31. Lim C, Choi C and Choe J (2004) Mitotic chromosome-binding activity of latency-associated nuclear antigen 1 is required for DNA replication from terminal repeat sequence of Kaposi's sarcoma-associated herpesvirus. J Virol 78, 7248-7256 https://doi.org/10.1128/JVI.78.13.7248-7256.2004
  32. Barbera AJ, Ballestas ME and Kaye KM (2004) The Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen 1 N terminus is essential for chromosome association, DNA replication, and episome persistence. J Virol 78, 294-301 https://doi.org/10.1128/JVI.78.1.294-301.2004
  33. Kumar A, Lyu Y, Yanagihashi Y et al (2022) KSHV episome tethering sites on host chromosomes and regulation of latency-lytic switch by CHD4. Cell Rep 39, 110788
  34. Ohsaki E, Ueda K, Sakakibara S, Do E, Yada K and Yamanishi K (2004) Poly(ADP-ribose) polymerase 1 binds to Kaposi's sarcoma-associated herpesvirus (KSHV) terminal repeat sequence and modulates KSHV replication in latency. J Virol 78, 9936-9946 https://doi.org/10.1128/JVI.78.18.9936-9946.2004
  35. Si H, Verma SC, Lampson MA, Cai Q and Robertson ES (2008) Kaposi's sarcoma-associated herpesvirus-encoded LANA can interact with the nuclear mitotic apparatus protein to regulate genome maintenance and segregation. J Virol 82, 6734-6746 https://doi.org/10.1128/JVI.00342-08
  36. Krithivas A, Fujimuro M, Weidner M, Young DB and Hayward SD (2002) Protein interactions targeting the latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus to cell chromosomes. J Virol 76, 11596-11604 https://doi.org/10.1128/JVI.76.22.11596-11604.2002
  37. Xiao B, Verma SC, Cai Q et al (2010) Bub1 and CENP-F can contribute to Kaposi's sarcoma-associated herpesvirus genome persistence by targeting LANA to kinetochores. J Virol 84, 9718-9732 https://doi.org/10.1128/JVI.00713-10
  38. Belloni L, Pollicino T, De Nicola F et al (2009) Nuclear HBx binds the HBV minichromosome and modifies the epigenetic regulation of cccDNA function. Proc Natl Acad Sci U S A 106, 19975-19979 https://doi.org/10.1073/pnas.0908365106
  39. Piirsoo M, Ustav E, Mandel T, Stenlund A and Ustav M (1996) Cis and trans requirements for stable episomal maintenance of the BPV-1 replicator. EMBO J 15, 1-11 https://doi.org/10.1002/j.1460-2075.1996.tb00328.x
  40. Bastien N and McBride AA (2000) Interaction of the papillomavirus E2 protein with mitotic chromosomes. Virology 270, 124-134 https://doi.org/10.1006/viro.2000.0265
  41. Ilves I, Kivi S and Ustav M (1999) Long-term episomal maintenance of bovine papillomavirus type 1 plasmids is determined by attachment to host chromosomes, which Is mediated by the viral E2 protein and its binding sites. J Virol 73, 4404-4412 https://doi.org/10.1128/JVI.73.5.4404-4412.1999
  42. Sullivan CS and Pipas JM (2002) T antigens of simian virus 40: molecular chaperones for viral replication and tumorigenesis. Microbiol Mol Biol Rev 66, 179-202 https://doi.org/10.1128/MMBR.66.2.179-202.2002
  43. Calattini S, Sereti I, Scheinberg P, Kimura H, Childs RW and Cohen JI (2010) Detection of EBV genomes in plasmablasts/plasma cells and non-B cells in the blood of most patients with EBV lymphoproliferative disorders by using Immuno-FISH. Blood 116, 4546-4559
  44. Kim KD, Tanizawa H, De Leo A et al (2020) Epigenetic specifications of host chromosome docking sites for latent Epstein-Barr virus. Nat Commun 11, 877
  45. Kempfer R and Pombo A (2020) Methods for mapping 3D chromosome architecture. Nat Rev Genet 21, 207-226 https://doi.org/10.1038/s41576-019-0195-2
  46. Zhao Z, Tavoosidana G, Sjolinder M et al (2006) Circular chromosome conformation capture (4C) uncovers extensive networks of epigenetically regulated intra- and interchromosomal interactions. Nat Genet 38, 1341-1347 https://doi.org/10.1038/ng1891
  47. Lieberman-Aiden E, van Berkum NL, Williams L et al (2009) Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326, 289-293 https://doi.org/10.1126/science.1181369
  48. van de Werken HJ, Landan G, Holwerda SJ et al (2012) Robust 4C-seq data analysis to screen for regulatory DNA interactions. Nat Methods 9, 969-972 https://doi.org/10.1038/nmeth.2173
  49. van de Werken HJ, de Vree PJ, Splinter E et al (2012) 4C technology: protocols and data analysis. Methods Enzymol 513, 89-112 https://doi.org/10.1016/B978-0-12-391938-0.00004-5
  50. Mifsud B, Tavares-Cadete F, Young AN et al (2015) Mapping long-range promoter contacts in human cells with high-resolution capture Hi-C. Nat Genet 47, 598-606 https://doi.org/10.1038/ng.3286
  51. Yang B, Li B, Jia L et al (2020) 3D landscape of Hepatitis B virus interactions with human chromatins. Cell Discov 6, 95
  52. Moquin SA, Thomas S, Whalen S et al (2018) The Epstein-Barr virus episome maneuvers between nuclear chromatin compartments during reactivation. J Virol 92, e01413-17
  53. Wang L, Laing J, Yan B et al (2020) Epstein-Barr virus episome physically interacts with active regions of the host genome in lymphoblastoid cells. J Virol 94, e01390-20
  54. Tang D, Zhao H, Wu Y et al (2021) Transcriptionally inactive hepatitis B virus episome DNA preferentially resides in the vicinity of chromosome 19 in 3D host genome upon infection. Cell Rep 35, 109288
  55. Hensel KO, Cantner F, Bangert F, Wirth S and Postberg J (2018) Episomal HBV persistence within transcribed host nuclear chromatin compartments involves HBx. Epigenetics Chromatin 11, 34
  56. Moreau P, Cournac A, Palumbo GA et al (2018) Tridimensional infiltration of DNA viruses into the host genome shows preferential contact with active chromatin. Nat Commun 9, 4268
  57. Heslop HE (2020) Sensitizing Burkitt lymphoma to EBVCTLs. Blood 135, 1822-1823 https://doi.org/10.1182/blood.2020005492
  58. Toth Z, Papp B, Brulois K, Choi YJ, Gao SJ and Jung JU (2016) LANA-mediated recruitment of host polycomb repressive complexes onto the KSHV genome during de novo infection. PLoS Pathog 12, e1005878
  59. Benhenda S, Cougot D, Buendia MA and Neuveut C (2009) Hepatitis B virus X protein molecular functions and its role in virus life cycle and pathogenesis. Adv Cancer Res 103, 75-109 https://doi.org/10.1016/S0065-230X(09)03004-8
  60. Leupin O, Bontron S, Schaeffer C and Strubin M (2005) Hepatitis B virus X protein stimulates viral genome replication via a DDB1-dependent pathway distinct from that leading to cell death. J Virol 79, 4238-4245 https://doi.org/10.1128/JVI.79.7.4238-4245.2005
  61. Dowen JM, Fan ZP, Hnisz D et al (2014) Control of cell identity genes occurs in insulated neighborhoods in mammalian chromosomes. Cell 159, 374-387 https://doi.org/10.1016/j.cell.2014.09.030
  62. Risca VI and Greenleaf WJ (2015) Unraveling the 3D genome: genomics tools for multiscale exploration. Trends Genet 31, 357-372
  63. Nagano T, Lubling Y, Stevens TJ et al (2013) Single-cell Hi-C reveals cell-to-cell variability in chromosome structure. Nature 502, 59-64 https://doi.org/10.1038/nature12593
  64. Nagano T, Lubling Y, Varnai C et al (2017) Cell-cycle dynamics of chromosomal organization at single-cell resolution. Nature 547, 61-67 https://doi.org/10.1038/nature23001
  65. Tempera I, Wiedmer A, Dheekollu J and Lieberman PM (2010) CTCF prevents the epigenetic drift of EBV latency promoter Qp. PLoS Pathog 6, e1001048
  66. Pentland I and Parish JL (2015) Targeting CTCF to control virus gene expression: a common theme amongst diverse DNA viruses. Viruses 7, 3574-3585 https://doi.org/10.3390/v7072791
  67. Bloom DC, Giordani NV and Kwiatkowski DL (2010) Epigenetic regulation of latent HSV-1 gene expression. Biochim Biophys Acta 1799, 246-256 https://doi.org/10.1016/j.bbagrm.2009.12.001
  68. Decorsiere A, Mueller H, van Breugel PC et al (2016) Hepatitis B virus X protein identifies the Smc5/6 complex as a host restriction factor. Nature 531, 386-389 https://doi.org/10.1038/nature17170