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An essential role for γ-herpesvirus latency-associated nuclear antigen homolog in an acute lymphoproliferative disease of cattle.

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Palmeira, Leonor Sorel, Océane Van Campe, Willem Boudry, Christel Roels, Stefan Coulie, Pierre G. [UCL] Dewals, Benjamin G

Wildebeests carry asymptomatically alcelaphine herpesvirus 1 (AlHV-1), a γ-herpesvirus inducing malignant catarrhal fever (MCF) to several ruminant species (including cattle). This acute and lethal lymphoproliferative disease occurs after a prolonged asymptomatic incubation period after transmission. Our recent findings with the rabbit model indicated that AlHV-1 infection is not productive during MCF. Here, we investigated whether latency establishment could explain this apparent absence of productive infection and sought to determine its role in MCF pathogenesis. First, whole-genome cellular and viral gene expression analyses were performed in lymph nodes of MCF-developing calves. Whereas a severe disruption in cellular genes was observed, only 10% of the entire AlHV-1 genome was expressed, contrasting with the 45% observed during productive infection in vitro. In vivo, the expressed viral genes included the latency-associated nuclear antigen homolog ORF73 but none of the regions known to be essential for productive infection. Next, genomic conformation analyses revealed that AlHV-1 was essentially episomal, further suggesting that MCF might be the consequence of a latent infection rather than abortive lytic infection. This hypothesis was further supported by the high frequencies of infected CD8(+) T cells during MCF using immunodetection of ORF73 protein and single-cell RT-PCR approaches. Finally, the role of latency-associated ORF73 was addressed. A lack of ORF73 did not impair initial virus replication in vivo, but it rendered AlHV-1 unable to induce MCF and persist in vivo and conferred protection against a lethal challenge with a WT virus. Together, these findings suggest that a latent infection is essential for MCF induction.

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès restreint
Publication date 2013
Language Anglais
Journal information "Proceedings of the National academy of sciences of the United States of America" - Vol. 110, no.21, p. E1933-42 (2013)
Peer reviewed yes
Publisher National academy of sciences ((United States) [S.l.])
issn 0027-8424
e-issn 1091-6490
Publication status Publié
Affiliation UCL - SSS/DDUV - Institut de Duve
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  1. Dobson Andrew P., Borner Markus, Sinclair Anthony R. E., Hudson Peter J., Anderson T. Michael, Bigurube Gerald, Davenport Tim B. B., Deutsch James, Durant Sarah M., Estes Richard D., Estes Anna B., Fryxell John, Foley Charles, Gadd Michelle E., Haydon Dan, Holdo Ricardo, Holt Robert D., Homewood Katherine, Hopcraft J. Grant C., Hilborn Ray, Jambiya George L. K., Laurenson M. Karen, Melamari Lota, Morindat Alais Ole, Ogutu Joseph O., Schaller George, Wolanski Eric, Road will ruin Serengeti, 10.1038/467272a
  2. Holdo Ricardo M., Fryxell John M., Sinclair Anthony R. E., Dobson Andrew, Holt Robert D., Predicted Impact of Barriers to Migration on the Serengeti Wildebeest Population, 10.1371/journal.pone.0016370
  3. PLOWRIGHT W., FERRIS R. D., SCOTT G. R., Blue Wildebeest and the Ætiological Agent of Bovine Malignant Catarrhal Fever, 10.1038/1881167a0
  4. Plowright, Research in veterinary science, 6, 56 (1965)
  5. Plowright, Research in veterinary science, 6, 69 (1965)
  6. Russell George C., Stewart James P., Haig David M., Malignant catarrhal fever: A review, 10.1016/j.tvjl.2007.11.007
  7. Schock A., Reid H.W., Characterisation of the lymphoproliferation in rabbits experimentally affected with malignant catarrhal fever, 10.1016/s0378-1135(96)01239-4
  8. Swa S., Wright H., Thomson J., Reid H., Haig D., Constitutive activation of Lck and Fyn tyrosine kinases in large granular lymphocytes infected with the gamma-herpesvirus agents of malignant catarrhal fever, 10.1046/j.1365-2567.2001.01154.x
  9. Bridgen Anne, Munro R., Reid H.W., The detection of alcelaphine herpesvirus-1 DNA by in situ hybridization of tissues from rabbits affected with malignant catarrhal fever, 10.1016/0021-9975(92)90021-l
  10. Patel J. R., Edington N., The Detection of the Herpesvirus of Bovine Malignant Catarrhal Fever in Rabbit Lymphocytes in vivo and in vitro, 10.1099/0022-1317-48-2-437
  11. Dewals Benjamin, Boudry Christel, Farnir Frédéric, Drion Pierre-Vincent, Vanderplasschen Alain, Malignant Catarrhal Fever Induced by Alcelaphine herpesvirus 1 Is Associated with Proliferation of CD8+ T Cells Supporting a Latent Infection, 10.1371/journal.pone.0001627
  12. Dewals B., Myster F., Palmeira L., Gillet L., Ackermann M., Vanderplasschen A., Ex Vivo Bioluminescence Detection of Alcelaphine Herpesvirus 1 Infection during Malignant Catarrhal Fever, 10.1128/jvi.00286-11
  13. Buxton D., Reid H., Transmission of malignant catarrhal fever to rabbits, 10.1136/vr.106.11.243
  14. Dewals Benjamin G, Vanderplasschen Alain, Malignant catarrhal fever induced by Alcelaphine herpesvirus 1 is characterized by an expansion of activated CD3+CD8+CD4- T cells expressing a cytotoxic phenotype in both lymphoid and non-lymphoid tissues, 10.1186/1297-9716-42-95
  15. Blake N., Immune evasion by gammaherpesvirus genome maintenance proteins, 10.1099/vir.0.018242-0
  16. Thonur Leenadevi, Russell George C., Stewart James P., Haig David M., Differential Transcription of Ovine Herpesvirus 2 Genes in Lymphocytes from Reservoir and Susceptible Species, 10.1007/s11262-005-5842-3
  17. Ensser, Journal of Virology, 71, 6517 (1997)
  18. Budt M., Hristozova T., Hille G., Berger K., Brune W., Construction of a Lytically Replicating Kaposi's Sarcoma-Associated Herpesvirus, 10.1128/jvi.05071-11
  19. Fowler P., ORF73 of murine herpesvirus-68 is critical for the establishment and maintenance of latency, 10.1099/vir.0.19594-0
  20. Moorman N. J., Willer D. O., Speck S. H., The Gammaherpesvirus 68 Latency-Associated Nuclear Antigen Homolog Is Critical for the Establishment of Splenic Latency, 10.1128/jvi.77.19.10295-10303.2003
  21. Thirion M., Machiels B., Farnir F., Donofrio G., Gillet L., Dewals B., Vanderplasschen A., Bovine herpesvirus 4 ORF73 is dispensable for virus growth in vitro, but is essential for virus persistence in vivo, 10.1099/vir.0.023192-0
  22. Forrest J. C., Paden C. R., Allen R. D., Collins J., Speck S. H., ORF73-Null Murine Gammaherpesvirus 68 Reveals Roles for mLANA and p53 in Virus Replication, 10.1128/jvi.00111-07
  23. Wen K. W., Dittmer D. P., Damania B., Disruption of LANA in Rhesus Rhadinovirus Generates a Highly Lytic Recombinant Virus, 10.1128/jvi.00704-09
  24. Cheng Benson Yee Hin, Zhi Jizu, Santana Alexis, Khan Sohail, Salinas Eduardo, Forrest J. Craig, Zheng Yueting, Jaggi Shirin, Leatherwood Janet, Krug Laurie T., Tiled Microarray Identification of Novel Viral Transcript Structures and Distinct Transcriptional Profiles during Two Modes of Productive Murine Gammaherpesvirus 68 Infection, 10.1128/jvi.05892-11
  25. Gatherer D., Seirafian S., Cunningham C., Holton M., Dargan D. J., Baluchova K., Hector R. D., Galbraith J., Herzyk P., Wilkinson G. W. G., Davison A. J., High-resolution human cytomegalovirus transcriptome, 10.1073/pnas.1115861108
  26. Johnson L. Steven, Willert Erin K., Virgin Herbert W., Redefining the Genetics of Murine Gammaherpesvirus 68 via Transcriptome-Based Annotation, 10.1016/j.chom.2010.05.005
  27. Chandriani S., Xu Y., Ganem D., The Lytic Transcriptome of Kaposi's Sarcoma-Associated Herpesvirus Reveals Extensive Transcription of Noncoding Regions, Including Regions Antisense to Important Genes, 10.1128/jvi.00645-10
  28. Meier-Trummer Claudia S., Rehrauer Hubert, Franchini Marco, Patrignani Andrea, Wagner Ulrich, Ackermann Mathias, Malignant Catarrhal Fever of Cattle Is Associated with Low Abundance of IL-2 Transcript and a Predominantly Latent Profile of Ovine Herpesvirus 2 Gene Expression, 10.1371/journal.pone.0006265
  29. Mesri Enrique A., Cesarman Ethel, Boshoff Chris, Kaposi's sarcoma and its associated herpesvirus, 10.1038/nrc2888
  30. Saha A., Robertson E. S., Epstein-Barr Virus-Associated B-cell Lymphomas: Pathogenesis and Clinical Outcomes, 10.1158/1078-0432.ccr-10-2578
  31. Jia Q., Freeman M. L., Yager E. J., McHardy I., Tong L., Martinez-Guzman D., Rickabaugh T., Hwang S., Blackman M. A., Sun R., Wu T.-T., Induction of Protective Immunity against Murine Gammaherpesvirus 68 Infection in the Absence of Viral Latency, 10.1128/jvi.01543-09
  32. Jia Q., Chernishof V., Bortz E., Mchardy I., Wu T.-T., Liao H.-I, Sun R., Murine Gammaherpesvirus 68 Open Reading Frame 45 Plays an Essential Role during the Immediate-Early Phase of Viral Replication, 10.1128/jvi.79.8.5129-5141.2005
  33. PLOWRIGHT W., MACADAM R. F., ARMSTRONG J. A., Growth and Characterization of the Virus of Bovine Malignant Catarrhal Fever in East Africa, 10.1099/00221287-39-2-253
  34. Dry I., Haig D. M., Inglis N. F., Imrie L., Stewart J. P., Russell G. C., Proteomic Analysis of Pathogenic and Attenuated Alcelaphine Herpesvirus 1, 10.1128/jvi.00094-08
  35. Wright H., Stewart J.P., Ireri R.G., Campbell I., Pow I., Reid H.W., Haig D.M., Genome re-arrangements associated with loss of pathogenicity of the γ-herpesvirus alcelaphine herpesvirus-1, 10.1016/s0034-5288(03)00043-2
  36. Ballestas M. E., Efficient Persistence of Extrachromosomal KSHV DNA Mediated by Latency-Associated Nuclear Antigen, 10.1126/science.284.5414.641
  37. Friborg, Nature; Physical Science (London), 402, 889 (1999)
  38. Si H., Robertson E. S., Kaposi's Sarcoma-Associated Herpesvirus-Encoded Latency-Associated Nuclear Antigen Induces Chromosomal Instability through Inhibition of p53 Function, 10.1128/jvi.80.2.697-709.2006
  39. Boshoff Chris, Radkov Stoyan A., Kellam Paul, 10.1038/80459
  40. Di Bartolo D. L., Cannon M., Liu Y.-F., Renne R., Chadburn A., Boshoff C., Cesarman E., KSHV LANA inhibits TGF-  signaling through epigenetic silencing of the TGF-  type II receptor, 10.1182/blood-2007-09-110544
  41. Lu J., Verma S. C., Murakami M., Cai Q., Kumar P., Xiao B., Robertson E. S., Latency-Associated Nuclear Antigen of Kaposi's Sarcoma-Associated Herpesvirus (KSHV) Upregulates Survivin Expression in KSHV-Associated B-Lymphoma Cells and Contributes to Their Proliferation, 10.1128/jvi.00397-09
  42. Coulter L.J., Wright H., Reid H.W., Molecular Genomic Characterization of the Viruses of Malignant Catarrhal Fever, 10.1053/jcpa.2000.0524
  43. Walz N., Christalla T., Tessmer U., Grundhoff A., A Global Analysis of Evolutionary Conservation among Known and Predicted Gammaherpesvirus MicroRNAs, 10.1128/jvi.01302-09
  44. Pearce M., Matsumura S., Wilson A. C., Transcripts Encoding K12, v-FLIP, v-Cyclin, and the MicroRNA Cluster of Kaposi's Sarcoma-Associated Herpesvirus Originate from a Common Promoter, 10.1128/jvi.79.22.14457-14464.2005
  45. Haig David M., Grant Dawn, Deane David, Campbell Iris, Thomson Jackie, Jepson Catherine, Buxton David, Russell George C., An immunisation strategy for the protection of cattle against alcelaphine herpesvirus-1-induced malignant catarrhal fever, 10.1016/j.vaccine.2008.06.056
  46. Plowright, Research in veterinary science, 19, 159 (1975)
  47. Rossiter P.B., Gumm I.D., Mirangi P.K., Immunological relationships between malignant catarrhal fever virus (Alcelaphine herpesvirus 1) and Bovine cytomegalovirus (Bovine herpesvirus 3), 10.1016/0378-1135(88)90025-9
  48. Fowler P., Vaccine potential of a murine gammaherpesvirus-68 mutant deficient for ORF73, 10.1099/vir.0.19760-0
  49. Warming S., Simple and highly efficient BAC recombineering using galK selection, 10.1093/nar/gni035
  50. Gentleman Robert C, Carey Vincent J, Bates Douglas M, Bolstad Ben, Dettling Marcel, Dudoit Sandrine, Ellis Byron, Gautier Laurent, Ge Yongchao, Gentry Jeff, Hornik Kurt, Hothorn Torsten, Huber Wolfgang, Iacus Stefano, Irizarry Rafael, Leisch Friedrich, Li Cheng, Maechler Martin, Rossini Anthony J, Sawitzki Gunther, Smith Colin, Smyth Gordon, Tierney Luke, Yang Jean YH, Zhang Jianhua, 10.1186/gb-2004-5-10-r80
  51. Smyth Gordon K, Speed Terry, Normalization of cDNA microarray data, 10.1016/s1046-2023(03)00155-5
  52. McGeoch Duncan J., Cook Simon, Dolan Aidan, Jamieson Fiona E., Telford Elizabeth A.R., Molecular Phylogeny and Evolutionary Timescale for the Family of Mammalian Herpesviruses, 10.1006/jmbi.1995.0152
  53. Dewals B., Myster F., Palmeira L., Gillet L., Ackermann M., Vanderplasschen A., Ex Vivo Bioluminescence Detection of Alcelaphine Herpesvirus 1 Infection during Malignant Catarrhal Fever, 10.1128/jvi.00286-11
  54. Dewals Benjamin G, Vanderplasschen Alain, Malignant catarrhal fever induced by Alcelaphine herpesvirus 1 is characterized by an expansion of activated CD3+CD8+CD4- T cells expressing a cytotoxic phenotype in both lymphoid and non-lymphoid tissues, 10.1186/1297-9716-42-95
Bibliographic reference Palmeira, Leonor ; Sorel, Océane ; Van Campe, Willem ; Boudry, Christel ; Roels, Stefan ; et. al. An essential role for γ-herpesvirus latency-associated nuclear antigen homolog in an acute lymphoproliferative disease of cattle.. In: Proceedings of the National academy of sciences of the United States of America, Vol. 110, no.21, p. E1933-42 (2013)
Permanent URL http://hdl.handle.net/2078.1/130012