Herpesvirus telomeric repeats facilitate genomic integration into host telomeres and mobilization of viral DNA during reactivation

Journal of Experimental Medicine

Volumn 208, Issue 3, 2011, Pages 605-615

  Kaufer, Benedikt B ^a,b   Jarosinski, Keith W ^a   Osterrieder, Nikolaus ^a,b  

^a Department of Obstetrics Gynecology   (United States)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS DNA;

ANIMAL CELL; ARTICLE; CARCINOGENESIS; CELL DIVISION; CONTROLLED STUDY; EMBRYO; INFECTION; LATENT PERIOD; LYMPHOMA; MARDIVIRUS; NONHUMAN; PRIORITY JOURNAL; TELOMERE; VIRUS CELL INTERACTION; VIRUS GENOME; VIRUS REACTIVATION;

ANIMALS; CHICKENS; DNA, VIRAL; HERPESVIRIDAE; HERPESVIRUS 2, GALLID; MAREK DISEASE; MUTATION; REPETITIVE SEQUENCES, NUCLEIC ACID; TELOMERE; VIRUS ACTIVATION; VIRUS INTEGRATION;

EID: 79952726582     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20101402     Document Type: Article

References (45)

1. Arbuckle, J.H., M.M. Medveczky, J. Luka, S.H. Hadley, A. Luegmayr, D. Ablashi, T.C. Lund, J. Tolar, K. De Meirleir, J.G. Montoya, et al. 2010. The latent human herpesvirus-6A genome specifically integrates in telomeres of human chromosomes in vivo and in vitro. Proc. Natl. Acad. Sci. USA. 107:5563-5568. doi:10.1073/pnas.0913586107
2. Blasco, M.A. 2005. Telomeres and human disease: ageing, cancer and beyond. Nat. Rev. Genet. 6:611-622. doi:10.1038/nrg1656 (Pubitemid 41044298)
3. Brown, A.C., S.J. Baigent, L.P. Smith, J.P. Chattoo, L.J. Petherbridge, P. Hawes, M.J. Allday, and V. Nair. 2006. Interaction of MEQ protein and C-terminal-binding protein is critical for induction of lymphomas by Marek's disease virus. Proc. Natl. Acad. Sci. USA. 103:1687-1692. doi:10.1073/pnas. 0507595103 (Pubitemid 43228754)
4. Calnek, B.W., K.K. Murthy, and K.A. Schat. 1978. Establishment of Marek's disease lymphoblastoid cell lines from transplantable versus primary lymphomas. Int. J. Cancer. 21:100-107. doi:10.1002/ijc.2910210117
5. Calnek, B.W., W.R. Shek, and K.A. Schat. 1981. Spontaneous and induced herpesvirus genome expression in Marek's disease tumor cell lines. Infect. Immun. 34:483-491. (Pubitemid 12117549)
6. Cesarman, E., and E.A. Mesri. 2007. Kaposi sarcoma-associated herpesvirus and other viruses in human lymphomagenesis. Curr. Top. Microbiol. Immunol. 312:263-287. doi:10.1007/978-3-540-34344-8-10 (Pubitemid 47400340)
7. Chbab, N., A. Egerer, I. Veiga, K.W. Jarosinski, and N. Osterrieder. 2010. Viral control of vTR expression is critical for efficient formation and dissemination of lymphoma induced by Marek's disease virus (MDV). Vet. Res. 41:56. doi:10.1051/vetres/2010026
8. Cohrs, R.J., and D.H. Gilden. 2001. Human herpesvirus latency. Brain Pathol. 11:465-474. doi:10.1111/j.1750-3639.2001.tb00415.x (Pubitemid 32777505)
9. Cole, R.K. 1968. Studies on genetic resistance to Marek's disease. Avian Dis. 12:9-28. doi:10.2307/1588081
10. Delany, M.E., L.M. Daniels, S.E. Swanberg, and H.A. Taylor. 2003. Telomeres in the chicken: genome stability and chromosome ends. Poult. Sci. 82:917-926. (Pubitemid 38641903)
11. Delecluse, H.J., and W. Hammerschmidt. 1993. Status of Marek's disease virus in established lymphoma cell lines: herpesvirus integration is common. J. Virol. 67:82-92. (Pubitemid 23002967)
12. Delecluse, H.J., S. Schüller, and W. Hammerschmidt. 1993. Latent Marek's disease virus can be activated from its chromosomally integrated state in herpesvirus-transformed lymphoma cells. EMBO J. 12:3277-3286. (Pubitemid 23232759)
13. Gulley, M.L., M. Raphael, C.T. Lutz, D.W. Ross, and N. Raab-Traub. 1992. Epstein-Barr virus integration in human lymphomas and lymphoid cell lines. Cancer. 70:185-191. doi:10.1002/1097-0142(19920701)70:1〈185::AID- CNCR2820700129〉3.0.CO;2-J
14. Hall, C.B., M.T. Caserta, K. Schnabel, L.M. Shelley, A.S. Marino, J.A. Carnahan, C. Yoo, G.K. Lofthus, and M.P. McDermott. 2008. Chromosomal integration of human herpesvirus 6 is the major mode of congenital human herpesvirus 6 infection. Pediatrics. 122:513-520. doi:10.1542/peds.2007-2838
15. Herschleb, J., G. Ananiev, and D.C. Schwartz. 2007. Pulsed-field gel electrophoresis. Nat. Protoc. 2:677-684. doi:10.1038/nprot.2007.94 (Pubitemid 47040029)
16. Jarosinski, K.W., N. Osterrieder, V.K. Nair, and K.A. Schat. 2005. Attenuation of Marek's disease virus by deletion of open reading frame RLORF4 but not RLORF5a. J. Virol. 79:11647-11659. doi:10.1128/JVI.79.18.11647-11659. 2005 (Pubitemid 41279283)
17. Jarosinski, K., L. Kattenhorn, B. Kaufer, H. Ploegh, and N. Osterrieder. 2007a. A herpesvirus ubiquitin-specific protease is critical for efficient T cell lymphoma formation. Proc. Natl. Acad. Sci. USA. 104:20025-20030. doi:10.1073/pnas.0706295104
18. Jarosinski, K.W., N.G. Margulis, J.P. Kamil, S.J. Spatz, V.K. Nair, and N. Osterrieder. 2007b. Horizontal transmission of Marek's disease virus requires US2, the UL13 protein kinase, and gC. J. Virol. 81:10575-10587. doi:10.1128/JVI.01065-07 (Pubitemid 47463331)
19. Jones, C. 1998. Alphaherpesvirus latency: its role in disease and survival of the virus in nature. Adv. Virus Res. 51:81-133. doi:10.1016/ S0065-3527(08)60784-8
20. Kaufer, B.B., B. Smejkal, and N. Osterrieder. 2010a. The varicella-zoster virus ORFS/L (ORF0) gene is required for efficient viral replication and contains an element involved in DNA cleavage. J. Virol. 84:11661-11669. doi:10.1128/JVI.00878-10
21. Kaufer, B.B., S. Trapp, K.W. Jarosinski, and N. Osterrieder. 2010b. Herpesvirus telomerase RNA(vTR)-dependent lymphoma formation does not require interaction of vTR with telomerase reverse transcriptase (TERT). PLoS Pathog. 6:e1001073. doi:10.1371/journal.ppat.1001073
22. Kishi, M., H. Harada, M. Takahashi, A. Tanaka, M. Hayashi, M. Nonoyama, S.F. Josephs, A. Buchbinder, F. Schachter, D.V. Ablashi, et al. 1988. A repeat sequence, GGGTTA, is shared by DNA of human herpesvirus 6 and Marek's disease virus. J. Virol. 62:4824-4827. (Pubitemid 19006155)
23. Li, M., M. Mizuuchi, T.R. Burke Jr., and R. Craigie. 2006. Retroviral DNA integration: reaction pathway and critical intermediates. EMBO J. 25:1295-1304. doi:10.1038/sj.emboj.7601005
24. Liu, J.L., and H.J. Kung. 2000. Marek's disease herpesvirus transforming protein MEQ: a c-Jun analogue with an alternative life style. Virus Genes. 21:51-64. doi:10.1023/A:1008132313289
25. Lupiani, B., L.F. Lee, X. Cui, I. Gimeno, A. Anderson, R.W. Morgan, R.F. Silva, R.L. Witter, H.J. Kung, and S.M. Reddy. 2004. Marek's disease virus-encoded Meq gene is involved in transformation of lymphocytes but is dispensable for replication. Proc. Natl. Acad. Sci. USA. 101:11815-11820. doi:10.1073/pnas.0404508101 (Pubitemid 39095377)
26. Luppi, M., R. Marasca, P. Barozzi, S. Ferrari, L. Ceccherini-Nelli, G. Batoni, E. Merelli, and G. Torelli. 1993. Three cases of human herpesvirus-6 latent infection: integration of viral genome in peripheral blood mononuclear cell DNA. J. Med. Virol. 40:44-52. doi:10.1002/jmv.1890400110 (Pubitemid 23142154)
27. Luppi, M., P. Barozzi, R. Marasca, and G. Torelli. 1994. Integration of human herpesvirus-6 (HHV-6) genome in chromosome 17 in two lymphoma patients. Leukemia. 8:S41-S45. (Pubitemid 24126068)
28. Mitchell, B.M., D.C. Bloom, R.J. Cohrs, D.H. Gilden, and P.G. Kennedy. 2003. Herpes simplex virus-1 and varicella-zoster virus latency in ganglia. J. Neurovirol. 9:194-204. (Pubitemid 36656453)
29. Murnane, J.P. 2006. Telomeres and chromosome instability. DNA Repair (Amst.). 5:1082-1092. doi:10.1016/j.dnarep.2006.05.030 (Pubitemid 44291621)
30. Osterrieder, N. 1999. Sequence and initial characterization of the U(L)10 (glycoprotein M) and U(L)11 homologous genes of serotype 1 Marek's Disease Virus. Arch. Virol. 144:1853-1863. doi:10.1007/s007050050710 (Pubitemid 29490041)
31. Osterrieder, N., J.P. Kamil, D. Schumacher, B.K. Tischer, and S. Trapp. 2006. Marek's disease virus: from miasma to model. Nat. Rev. Microbiol. 4:283-294. doi:10.1038/nrmicro1382
32. Parcells, M.S., R.L. Dienglewicz, A.S. Anderson, and R.W. Morgan. 1999. Recombinant Marek's disease virus (MDV)-derived lymphoblastoid cell lines: regulation of a marker gene within the context of the MDV genome. J. Virol. 73:1362-1373. (Pubitemid 29036791)
33. Perrem, K., L.M. Colgin, A.A. Neumann, T.R. Yeager, and R.R. Reddel. 2001. Coexistence of alternative lengthening of telomeres and telomerase in hTERT-transfected GM847 cells. Mol. Cell. Biol. 21:3862-3875. doi:10.1128/MCB.21.12.3862-3875.2001 (Pubitemid 32476449)
34. Reddel, R.R. 2003. Alternative lengthening of telomeres, telomerase, and cancer. Cancer Lett. 194:155-162. doi:10.1016/S0304-3835(02)00702-4 (Pubitemid 36577326)
35. Rens, W., B. Fu, P.C. O'Brien, and M. Ferguson-Smith. 2006. Cross-species chromosome painting. Nat. Protoc. 1:783-790. doi:10.1038/nprot.2006.91
36. Sambrook, J., D.F. Fritsch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratories, Cold Spring Harbor, NY. 1659 pp.
37. Schumacher, D., B.K. Tischer, W. Fuchs, and N. Osterrieder. 2000. Reconstitution of Marek's disease virus serotype 1 (MDV-1) from DNA cloned as a bacterial artificial chromosome and characterization of a glycoprotein B-negative MDV-1 mutant. J. Virol. 74:11088-11098. doi:10.1128/JVI.74.23.11088- 11098.2000 (Pubitemid 32223974)
38. Schumacher, D., B.K. Tischer, S. Trapp, and N. Osterrieder. 2005. The protein encoded by the US3 orthologue of Marek's disease virus is required for efficient de-envelopment of perinuclear virions and involved in actin stress fiber breakdown. J. Virol. 79:3987-3997. doi:10.1128/JVI.79.7.3987-3997.2005 (Pubitemid 40388339)
39. Sears, J., M. Ujihara, S. Wong, C. Ott, J. Middeldorp, and A. Aiyar. 2004. The amino terminus of Epstein-Barr Virus (EBV) nuclear antigen 1 contains AT hooks that facilitate the replication and partitioning of latent EBV genomes by tethering them to cellular chromosomes. J. Virol. 78:11487-11505. doi:10.1128/JVI.78.21.11487-11505.2004 (Pubitemid 39390736)
40. Secchiero, P., J. Nicholas, H. Deng, T. Xiaopeng, N. van Loon, V.R. Ruvolo, Z.N. Berneman, M.S. Reitz Jr., and S. Dewhurst. 1995. Identification of human telomeric repeat motifs at the genome termini of human herpesvirus 7: structural analysis and heterogeneity. J. Virol. 69:8041-8045.
41. Sfeir, A., S. Kabir, M. van Overbeek, G.B. Celli, and T. de Lange. 2010. Loss of Rap1 induces telomere recombination in the absence of NHEJ or a DNA damage signal. Science. 327:1657-1661. doi:10.1126/science.1185100
42. Spatz, S.J., L. Petherbridge, Y. Zhao, and V. Nair. 2007. Comparative full-length sequence analysis of oncogenic and vaccine (Rispens) strains of Marek's disease virus. J. Gen. Virol. 88:1080-1096. doi:10.1099/vir.0.82600-0 (Pubitemid 46523496)
43. Stevens, J.G. 1989. Human herpesviruses: a consideration of the latent state. Microbiol. Rev. 53:318-332. (Pubitemid 19221274)
44. Tischer, B.K., J. von Einem, B. Kaufer, and N. Osterrieder. 2006. Two-step red-mediated recombination for versatile high-efficiency markerless DNA manipulation in Escherichia coli. Biotechniques. 40:191-197. (Pubitemid 46542640)
45. Trapp, S., M.S. Parcells, J.P. Kamil, D. Schumacher, B.K. Tischer, P.M. Kumar, V.K. Nair, and N. Osterrieder. 2006. A virus-encoded telomerase RNA promotes malignant T cell lymphomagenesis. J. Exp. Med. 203:1307-1317. doi:10.1084/jem.20052240 (Pubitemid 43736599)