Evidence of an oncogenic gammaherpesvirus in domestic dogs

Virology

Volumn 427, Issue 2, 2012, Pages 107-117

  Huang, Shih Hung ^a   Kozak, Philip J ^a   Kim, Jessica ^a   Habineza Ndikuyeze, Georges ^a   Meade, Charles ^a   Gaurnier Hausser, Anita ^a   Patel, Reema ^a   Robertson, Erle ^b   Mason, Nicola J ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Canine; Epstein Barr virus; Gammaherpesvirus; Large animal model; Lymphoma

Indexed keywords

IMMUNOGLOBULIN G ANTIBODY; LATENT MEMBRANE PROTEIN 1; VIRUS CAPSID ANTIGEN; VIRUS DNA; VIRUS RNA;

ANIMAL CELL; ANIMAL TISSUE; ANTIBODY TITER; ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; DOG; DOMESTIC ANIMAL; ELECTRON MICROSCOPY; ENZYME LINKED IMMUNOSORBENT ASSAY; EPSTEIN BARR VIRUS; GAMMAHERPESVIRINAE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INTERMETHOD COMPARISON; LARGE CELL LYMPHOMA; MOLECULAR PATHOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SEQUENCE ANALYSIS; SEROLOGY; VIROGENESIS; VIRUS DETECTION; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, VIRAL; ANTIBODY SPECIFICITY; ANTIGENS, VIRAL; B-LYMPHOCYTES; BASE SEQUENCE; CELLS, CULTURED; DNA, VIRAL; DOG DISEASES; DOGS; GAMMAHERPESVIRINAE; IMMUNOGLOBULIN G; IN SITU HYBRIDIZATION; LYMPHOMA, B-CELL; MOLECULAR SEQUENCE DATA; SEROLOGIC TESTS; TUMOR VIRUS INFECTIONS;

ANIMALIA; CANIS FAMILIARIS; HERPESVIRIDAE; HUMAN HERPESVIRUS 4; MIRIDAE;

EID: 84862815912     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2012.02.013     Document Type: Article

References (71)

1. Bajaj B.G., Murakami M., Robertson E.S. Molecular biology of EBV in relationship to AIDS-associated oncogenesis. Cancer Treat. Res. 2007, 133:141-162.
2. Bergman P.J., McKnight J., Novosad A., Charney S., Farrelly J., Craft D., Wulderk M., Jeffers Y., Sadelain M., Hohenhaus A.E., Segal N., Gregor P., Engelhorn M., Riviere I., Houghton A.N., Wolchok J.D. Long-term survival of dogs with advanced malignant melanoma after DNA vaccination with xenogeneic human tyrosinase: a phase I trial. Clin. Cancer Res. 2003, 9(4):1284-1290.
3. Breen M., Modiano J.F. Evolutionarily conserved cytogenetic changes in hematological malignancies of dogs and humans-man and his best friend share more than companionship. Chromosome Res. 2008, 16(1):145-154.
4. Callan M.F., Tan L., Annels N., Ogg G.S., Wilson J.D., O'Callaghan C.A., Steven N., McMichael A.J., Rickinson A.B. Direct visualization of antigen-specific CD8+ T cells during the primary immune response to Epstein-Barr virus in vivo. J. Exp. Med. 1998, 187(9):1395-1402.
5. Campbell S., Nasir L., Argyle D., Bennett D. Molecular cloning and characterization of canine metalloproteinase-9 gene promoter. Gene 2001, 273(1):81-87.
6. Chiou S.H., Chow K.C., Yang C.H., Chiang S.F., Lin C.H. Discovery of Epstein-Barr virus (EBV)-encoded RNA signal and EBV nuclear antigen leader protein DNA sequence in pet dogs. J. Gen. Virol. 2005, 86(Pt 4):899-905.
7. Chodosh J., Gan Y., Holder V.P., Sixbey J.W. Patterned entry and egress by Epstein-Barr virus in polarized CR2-positive epithelial cells. Virology 2000, 266(2):387-396.
8. Crawford D.H. Biology and disease associations of Epstein-Barr virus. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2001, 356(1408):461-473.
9. Dalla-Favera R., Bregni M., Erikson J., Patterson D., Gallo R.C., Croce C.M. Human c-myc onc gene is located on the region of chromosome 8 that is translocated in Burkitt lymphoma cells. Proc. Natl. Acad. Sci. U. S. A. 1982, 79(24):7824-7827.
10. d'Amore F., Johansen P., Houmand A., Weisenburger D., Mortensen L. Epstein-Barr virus genome in non-Hodgkin's lymphomas occurring in immunocompetent patients: highest prevalence in nonlymphoblastic T-cell lymphoma and correlation with a poor prognosis. Danish Lymphoma Study Group, LYFO. Blood 1996, 87(3):1045-1055.
11. de-The G., Geser A., Day N.E., Tukei P.M., Williams E.H., Beri D.P., Smith P.G., Dean A.G., Bronkamm G.W., Feorino P., Henle W. Epidemiological evidence for causal relationship between Epstein-Barr virus and Burkitt's lymphoma from Ugandan prospective study. Nature 1978, 274(5673):756-761.
12. Ehlers B., Spiess K., Leendertz F., Peeters M., Boesch C., Gatherer D., McGeoch D.J. Lymphocryptovirus phylogeny and the origins of Epstein-Barr virus. J. Gen. Virol. 2010, 91(Pt 3):630-642.
13. Epstein M.A., Barr Y.M. Cultivation in vitro of human lymphoblasts from Burkitt's malignant lymphoma. Lancet 1964, 1(7327):252-253.
14. Fan H., Kim S.C., Chima C.O., Israel B.F., Lawless K.M., Eagan P.A., Elmore S., Moore D.T., Schichman S.A., Swinnen L.J., Gulley M.L. Epstein-Barr viral load as a marker of lymphoma in AIDS patients. J. Med. Virol. 2005, 75(1):59-69.
15. Faumont N., Durand-Panteix S., Schlee M., Gromminger S., Schuhmacher M., Holzel M., Laux G., Mailhammer R., Rosenwald A., Staudt L.M., Bornkamm G.W., Feuillard J. c-Myc and Rel/NF-kappaB are the two master transcriptional systems activated in the latency III program of Epstein-Barr virus-immortalized B cells. J. Virol. 2009, 83(10):5014-5027.
16. Fournel-Fleury C., Magnol J.P., Bricaire P., Marchal T., Chabanne L., Delverdier A., Bryon P.A., Felman P. Cytohistological and immunological classification of canine malignant lymphomas: comparison with human non-Hodgkin's lymphomas. J. Comp. Pathol. 1997, 117(1):35-59.
17. Gallagher A., Armstrong A.A., MacKenzie J., Shield L., Khan G., Lake A., Proctor S., Taylor P., Clements G.B., Jarrett R.F. Detection of Epstein-Barr virus (EBV) genomes in the serum of patients with EBV-associated Hodgkin's disease. Int. J. Cancer 1999, 84(4):442-448.
18. Gaurnier-Hausser A., Patel R., Baldwin A., May M., Mason N.J. NEMO-binding domain peptide inhibits constitutive nf-{kappa}b activity and reduces tumor burden in a canine model of relapsed, refractory diffuse large B-cell lymphoma. Clin. Cancer Res. 2011, 17(14):4661-4671.
19. Glickman L., Glickman N., Thorpe R., 2000. The Golden Retriever Club of America National Health Survey. Available from: http://www.grca.org/healthsurvey.pdf.
20. Gulley M.L., Tang W. Laboratory assays for Epstein-Barr virus-related disease. J. Mol. Diagn. 2008, 10(4):279-292.
21. Henderson S., Rowe M., Gregory C., Croom-Carter D., Wang F., Longnecker R., Kieff E., Rickinson A. Induction of bcl-2 expression by Epstein-Barr virus latent membrane protein 1 protects infected B cells from programmed cell death. Cell 1991, 65(7):1107-1115.
22. Henle W., Henle G.E., Horwitz C.A. Epstein-Barr virus specific diagnostic tests in infectious mononucleosis. Hum. Pathol. 1974, 5(5):551-565.
23. Hinderer W., Lang D., Rothe M., Vornhagen R., Sonneborn H.H., Wolf H. Serodiagnosis of Epstein-Barr virus infection by using recombinant viral capsid antigen fragments and autologous gene fusion. J. Clin. Microbiol. 1999, 37(10):3239-3244.
24. Jiang H., Cho Y.G., Wang F. Structural, functional, and genetic comparisons of Epstein-Barr virus nuclear antigen 3A, 3B, and 3C homologues encoded by the rhesus lymphocryptovirus. J. Virol. 2000, 74(13):5921-5932.
25. Jiwa N.M., Oudejans J.J., Dukers D.F., Vos W., Horstman A., van der Valk P., Middledorp J.M., Walboomers J.M., Meijer C.J. Immunohistochemical demonstration of different latent membrane protein-1 epitopes of Epstein-Barr virus in lymphoproliferative diseases. J. Clin. Pathol. 1995, 48(5):438-442.
26. Khan G., Miyashita E.M., Yang B., Babcock G.J., Thorley-Lawson D.A. Is EBV persistence in vivo a model for B cell homeostasis?. Immunity 1996, 5(2):173-179.
27. Khan G., Lake A., Shield L., Freeland J., Andrew L., Alexander F.E., Jackson R., Taylor P.R., McCruden E.A., Jarrett R.F. Phenotype and frequency of Epstein-Barr virus-infected cells in pretreatment blood samples from patients with Hodgkin lymphoma. Br. J. Haematol. 2005, 129(4):511-519.
28. Klutts J.S., Ford B.A., Perez N.R., Gronowski A.M. Evidence-based approach for interpretation of Epstein-Barr virus serological patterns. J. Clin. Microbiol. 2009, 47(10):3204-3210.
29. Kutok J.L., Wang F. Spectrum of Epstein-Barr virus-associated diseases. Annu. Rev. Pathol. 2006, 1:375-404.
30. Lin T.Y., Bear M., Du Z., Foley K.P., Ying W., Barsoum J., London C. The novel HSP90 inhibitor STA-9090 exhibits activity against Kit-dependent and -independent malignant mast cell tumors. Exp. Hematol. 2008, 36(10):1266-1277.
31. Lindblad-Toh K., Wade C.M., Mikkelsen T.S., Karlsson E.K., Jaffe D.B., Kamal M., Clamp M., Chang J.L., Kulbokas E.J., Zody M.C., Mauceli E., Xie X., Breen M., Wayne R.K., Ostrander E.A., Ponting C.P., Galibert F., Smith D.R., DeJong P.J., Kirkness E., Alvarez P., Biagi T., Brockman W., Butler J., Chin C.W., Cook A., Cuff J., Daly M.J., DeCaprio D., Gnerre S., Grabherr M., Kellis M., Kleber M., Bardeleben C., Goodstadt L., Heger A., Hitte C., Kim L., Koepfli K.P., Parker H.G., Pollinger J.P., Searle S.M., Sutter N.B., Thomas R., Webber C., Baldwin J., Abebe A., Abouelleil A., Aftuck L., Ait-Zahra M., Aldredge T., Allen N., An P., Anderson S., Antoine C., Arachchi H., Aslam A., Ayotte L., Bachantsang P., Barry A., Bayul T., Benamara M., Berlin A., Bessette D., Blitshteyn B., Bloom T., Blye J., Boguslavskiy L., Bonnet C., Boukhgalter B., Brown A., Cahill P., Calixte N., Camarata J., Cheshatsang Y., Chu J., Citroen M., Collymore A., Cooke P., Dawoe T., Daza R., Decktor K., DeGray S., Dhargay N., Dooley K., Dorje P., Dorjee K., Dorris L., Duffey N., Dupes A., Egbiremolen O., Elong R., Falk J., Farina A., Faro S., Ferguson D., Ferreira P., Fisher S., FitzGerald M., Foley K., Foley C., Franke A., Friedrich D., Gage D., Garber M., Gearin G., Giannoukos G., Goode T., Goyette A., Graham J., Grandbois E., Gyaltsen K., Hafez N., Hagopian D., Hagos B., Hall J., Healy C., Hegarty R., Honan T., Horn A., Houde N., Hughes L., Hunnicutt L., Husby M., Jester B., Jones C., Kamat A., Kanga B., Kells C., Khazanovich D., Kieu A.C., Kisner P., Kumar M., Lance K., Landers T., Lara M., Lee W., Leger J.P., Lennon N., Leuper L., LeVine S., Liu J., Liu X., Lokyitsang Y., Lokyitsang T., Lui A., Macdonald J., Major J., Marabella R., Maru K., Matthews C., McDonough S., Mehta T., Meldrim J., Melnikov A., Meneus L., Mihalev A., Mihova T., Miller K., Mittelman R., Mlenga V., Mulrain L., Munson G., Navidi A., Naylor J., Nguyen T., Nguyen N., Nguyen C., Nicol R., Norbu N., Norbu C., Novod N., Nyima T., Olandt P., O'Neill B., O'Neill K., Osman S., Oyono L., Patti C., Perrin D., Phunkhang P., Pierre F., Priest M., Rachupka A., Raghuraman S., Rameau R., Ray V., Raymond C., Rege F., Rise C., Rogers J., Rogov P., Sahalie J., Settipalli S., Sharpe T., Shea T., Sheehan M., Sherpa N., Shi J., Shih D., Sloan J., Smith C., Sparrow T., Stalker J., Stange-Thomann N., Stavropoulos S., Stone C., Stone S., Sykes S., Tchuinga P., Tenzing P., Tesfaye S., Thoulutsang D., Thoulutsang Y., Topham K., Topping I., Tsamla T., Vassiliev H., Venkataraman V., Vo A., Wangchuk T., Wangdi T., Weiand M., Wilkinson J., Wilson A., Yadav S., Yang S., Yang X., Young G., Yu Q., Zainoun J., Zembek L., Zimmer A., Lander E.S. Genome sequence, comparative analysis and haplotype structure of the domestic dog. Nature 2005, 438(7069):803-819.
32. MacEwen E.G. Spontaneous tumors in dogs and cats: models for the study of cancer biology and treatment. Cancer Metastasis Rev. 1990, 9(2):125-136.
33. Mann K.P., Staunton D., Thorley-Lawson D.A. Epstein-Barr virus-encoded protein found in plasma membranes of transformed cells. J. Virol. 1985, 55(3):710-720.
34. Mason N.J., Coughlin C.M., Overley B., Cohen J.N., Mitchell E.L., Colligon T.A., Clifford C.A., Zurbriggen A., Sorenmo K.U., Vonderheide R.H. RNA-loaded CD40-activated B cells stimulate antigen-specific T-cell responses in dogs with spontaneous lymphoma. Gene Ther. 2008, 15(13):955-965.
35. Menezes J., Leibold W., Klein G., Clements G. Establishment and characterization of an Epstein-Barr virus (EBC)-negative lymphoblastoid B cell line (BJA-B) from an exceptional, EBV-genome-negative African Burkitt's lymphoma. Biomedicine 1975, 22(4):276-284.
36. Middeldorp J.M. Pathogenic roles for Epstein-Barr virus (EBV) gene products in EBV-associated proliferative disorders. Crit. Rev. Oncol. Hematol. 2003, 45(1):1-36.
37. Milman G., Smith K.C., Erles K. Serological detection of Epstein-Barr virus infection in dogs and cats. Vet. Microbiol. 2011, 150(1-2):15-20.
38. Moghaddam A., Koch J., Annis B., Wang F. Infection of human B lymphocytes with lymphocryptoviruses related to Epstein-Barr virus. J. Virol. 1998, 72(4):3205-3212.
39. Moon U., Park S., Oh S., Kim W., Park S., Lee S., Cho C., Kim H., Lee W., Lee S. Patients with systemic lupus erythematosus have abnormally elevated Epstein-Barr virus load in blood. Arthritis Res. Ther. 2004, 6(4):R295-R302.
40. Mueller N., Evans A., Harris N.L., Comstock G.W., Jellum E., Magnus K., Orentreich N., Polk B.F., Vogelman J. Hodgkin's disease and Epstein-Barr virus. Altered antibody pattern before diagnosis. N. Engl. J. Med. 1989, 320(11):689-695.
41. Munz C., Bickham K.L., Subklewe M., Tsang M.L., Chahroudi A., Kurilla M.G., Zhang D., O'Donnell M., Steinman R.M. Human CD4(+) T lymphocytes consistently respond to the latent Epstein-Barr virus nuclear antigen EBNA1. J. Exp. Med. 2000, 191(10):1649-1660.
42. Nemerow G.R., Cooper N.R. Early events in the infection of human B lymphocytes by Epstein-Barr virus: the internalization process. Virology 1984, 132(1):186-198.
43. Ohshima K., Kikuchi M., Eguchi F., Masuda Y., Sumiyoshi Y., Mohtai H., Takeshita M., Kimura N. Analysis of Epstein-Barr viral genomes in lymphoid malignancy using Southern blotting, polymerase chain reaction and in situ hybridization. Virchows Arch. B Cell Pathol. Incl. Mol. Pathol. 1990, 59(6):383-390.
44. Pallesen G., Hamilton-Dutoit S.J., Rowe M., Young L.S. Expression of Epstein-Barr virus latent gene products in tumour cells of Hodgkin's disease. Lancet 1991, 337(8737):320-322.
45. Paoloni M., Khanna C. Translation of new cancer treatments from pet dogs to humans. Nat. Rev. Cancer 2008, 8(2):147-156.
46. Paoloni M.C., Tandle A., Mazcko C., Hanna E., Kachala S., Leblanc A., Newman S., Vail D., Henry C., Thamm D., Sorenmo K., Hajitou A., Pasqualini R., Arap W., Khanna C., Libutti S.K. Launching a novel preclinical infrastructure: comparative oncology trials consortium directed therapeutic targeting of TNFalpha to cancer vasculature. PLoS One 2009, 4(3):e4972.
47. Pattle S.B., Farrell P.J. The role of Epstein-Barr virus in cancer. Expert Opin. Biol. Ther. 2006, 6(11):1193-1205.
48. Reischl U., Gerdes C., Motz M., Wolf H. Expression and purification of an Epstein-Barr virus encoded 23-kDa protein and characterization of its immunological properties. J. Virol. Methods 1996, 57(1):71-85.
49. Rickinson A.B., Moss D.J. Human cytotoxic T lymphocyte responses to Epstein-Barr virus infection. Annu. Rev. Immunol. 1997, 15:405-431.
50. Riddler S.A., Breinig M.C., McKnight J.L. Increased levels of circulating Epstein-Barr virus (EBV)-infected lymphocytes and decreased EBV nuclear antigen antibody responses are associated with the development of posttransplant lymphoproliferative disease in solid-organ transplant recipients. Blood 1994, 84(3):972-984.
51. Rose T.M., Strand K.B., Schultz E.R., Schaefer G., Rankin G.W., Thouless M.E., Tsai C.C., Bosch M.L. Identification of two homologs of the Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) in retroperitoneal fibromatosis of different macaque species. J. Virol. 1997, 71(5):4138-4144.
52. Rowe M. Upregulation of bcl-2 by the Epstein-Barr virus latent membrane protein LMP1: a B-cell-specific response that is delayed relative to NF-kappa B activation and to induction of cell surface markers. J. Virol. 1994, 68(9):5602-5612.
53. Rowe M. Methods in Molecular Biology. Epstein-Barr Virus Protocols 2001, 174. Humana Press, Totowa, New Jersey. J.B. Wilson (Ed.).
54. Rutgen B.C., Hammer S.E., Gerner W., Christian M., de Arespacochaga A.G., Willmann M., Kleiter M., Schwendenwein I., Saalmuller A. Establishment and characterization of a novel canine B-cell line derived from a spontaneously occurring diffuse large cell lymphoma. Leuk Res 2010, 34(7):932-938.
55. Sample J.T. Epstein-Barr virus types 1 and 2 differ in their EBNA-3A, EBNA-3B, and EBNA-3C genes. J. Virol. 1990, 64(9):4084-4092.
56. Sampson B. The Dog and Its Genome 2006, 44. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. K.L.-T.E.A. Ostrander, U. Giger (Eds.).
57. Sivachandran Epstein-Barr virus nuclear antigen 1 Hijacks the host kinase CK2 to disrupt PML nuclear bodies. J. Virol. 2010, 84(21):11113-11123.
58. Taub R., Kirsch I., Morton C., Lenoir G., Swan D., Tronick S., Aaronson S., Leder P. Translocation of the c-myc gene into the immunoglobulin heavy chain locus in human Burkitt lymphoma and murine plasmacytoma cells. Proc. Natl. Acad. Sci. U. S. A. 1982, 79(24):7837-7841.
59. Thomas R., Smith K.C., Ostrander E.A., Galibert F., Breen M. Chromosome aberrations in canine multicentric lymphomas detected with comparative genomic hybridisation and a panel of single locus probes. Br. J. Cancer 2003, 89(8):1530-1537.
60. Thorley-Lawson D.A., Allday M.J. The curious case of the tumour virus: 50 years of Burkitt's lymphoma. Nat. Rev. Microbiol. 2008, 6(12):913-924.
61. Vail D.M., MacEwen E.G. Spontaneously occurring tumors of companion animals as models for human cancer. Cancer Invest. 2000, 18(8):781-792.
62. van Grunsven W.M., Nabbe A., Middeldorp J.M. Identification and molecular characterization of two diagnostically relevant marker proteins of the Epstein-Barr virus capsid antigen complex. J. Med. Virol. 1993, 40(2):161-169.
63. van Grunsven W.M., van Heerde E.C., de Haard H.J., Spaan W.J., Middeldorp J.M. Gene mapping and expression of two immunodominant Epstein-Barr virus capsid proteins. J. Virol. 1993, 67(7):3908-3916.
64. van Grunsven W.M., Spaan W.J., Middeldorp J.M. Localization and diagnostic application of immunodominant domains of the BFRF3-encoded Epstein-Barr virus capsid protein. J. Infect. Dis. 1994, 170(1):13-19.
65. Vila C., Savolainen P., Maldonado J.E., Amorim I.R., Rice J.E., Honeycutt R.L., Crandall K.A., Lundeberg J., Wayne R.K. Multiple and ancient origins of the domestic dog. Science 1997, 276(5319):1687-1689.
66. Weiss L.M., Chen Y.Y., Liu X.F., Shibata D. Epstein-Barr virus and Hodgkin's disease. A correlative in situ hybridization and polymerase chain reaction study. Am. J. Pathol. 1991, 139(6):1259-1265.
67. Wu T.C., Mann R.B., Charache P., Hayward S.D., Staal S., Lambe B.C., Ambinder R.F. Detection of EBV gene expression in Reed-Sternberg cells of Hodgkin's disease. Int. J. Cancer 1990, 46(5):801-804.
68. Yang L., Maruo S., Takada K. CD21-mediated entry and stable infection by Epstein-Barr virus in canine and rat cells. J. Virol. 2000, 74(22):10745-10751.
69. Yates J.L., Warren N., Sugden B. Stable replication of plasmids derived from Epstein-Barr virus in various mammalian cells. Nature 1985, 313(6005):812-815.
70. Young L.S., Murray P.G. Epstein-Barr virus and oncogenesis: from latent genes to tumours. Oncogene 2003, 22(33):5108-5121.
71. Young L.S., Rickinson A.B. Epstein-Barr virus: 40 years on. Nat. Rev. Cancer 2004, 4(10):757-768.