Cell dynamics and immune response to BLV infection: A unifying model

Frontiers in Bioscience

Volumn 12, Issue 4, 2007, Pages 1520-1531

  Florins, Arnaud ^a   Gillet, Nicolas ^a   Asquith, Becca ^b   Boxus, Mathieu ^a   Burteau, Catherine ^a   Twizere, Jean Claude ^a   Urbain, Patrice ^a   Vandermeers, Fabian ^a   Debacq, Christophe ^c   Sanchez Alcaraz, Maria Teresa ^d   Schwartz Cornil, Isabelle ^e   Kerkhofs, Pierre ^f   Jean, Genèvieve ^g   Théwis, Andre ^g   Hay, Jack ^d   Mortreux, Franck ^h   Wattel, Eric ^h   Reichert, Michal ⁱ   Burny, Arsène ^a   Kettmann, Richard ^a   Bangham, Charles ^b   Willems, Luc ^a,j   more..

^a FNRS   (Belgium)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c GLAXOSMITHKLINE BIOLOGICALS   (Belgium)

^d UNIVERSITY OF TORONTO   (Canada)

^e INRA Institut National de la Recherche Agronomique   (France)

^f VETERINARY AND AGROCHEMICAL RESEARCH CENTRE   (Belgium)

^g UNIVERSITY OF LIÈGE   (Belgium)

^h CENTRE LÉON BÉRARD   (France)

ⁱ NATIONAL VETERINARY RESEARCH INSTITUTE   (Poland)

^j FUND FOR SCIENTIFIC RESEARCH   (Belgium)

more..

Author keywords

Apoptosis; BLV; Expression; Homeostasis; HTLV; Immune response; Leukemia; Silencing; Therapy; Trafficking; Virus

Indexed keywords

BOS; BOVIDAE; BOVINE LEUKEMIA VIRUS; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN T-LYMPHOTROPIC VIRUS 1; OVIS ARIES;

EID: 34249792077     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/2165     Document Type: Article

References (90)

1. A. Burny, Y. Cleuter, R. Kettmann, M. Mammerickx, G. Marbaix, D. Portetelle, B. A. Van den, L. Willems, and R. Thomas, Bovine leukaemia: facts and hypotheses derived from the study of an infectious cancer. Cancer Surv. 6, 139-159 (1987)
2. J. F. Ferrer, R. R. Marshak, D. A. Abt, and S. J. Kenyon, Persistent lymphocytosis in cattle: its cause, nature and relation to lymphosarcoma. Ann. Rech. Vet. 9, 851-857 (1978)
3. Z. Trainin, J. Brenner, R. Meirom, and H. Ungar-Waron, Detrimental effect of bovine leukemia virus (BLV) on the immunological state of cattle. Vet. Immunol. Immunopathol. 54, 293-302 (1996)
4. S. Bech-Nielsen, C. E. Piper, and J. F. Ferrer, Natural mode of transmission of the bovine leukemia virus: role of bloodsucking insects. Am. J. Vet. Res. 39, 1089-1092 (1978)
5. S. G. Hopkins and R. F. DiGiacomo, Natural transmission of bovine leukemia virus in dairy and beef cattle. Vet. Clin. North Am. Food Anim Pract. 13, 107-128 (1997)
6. S. Meas, J. Seto, C. Sugimoto, M. Bakhsh, M. Riaz, T. Sato, K. Naeem, K. Ohashi, and M. Onuma, Infection of bovine immunodeficiency virus and bovine leukemia virus in water buffalo and cattle populations in Pakistan. J. Vet. Med. Sci. 62, 329-331 (2000)
7. M. Mammerickx, D. Portetelle, K. de Clercq, and A. Burny, Experimental transmission of enzootic bovine leukosis to cattle, sheep and goats: infectious doses of blood and incubation period of the disease. Leuk. Res. 11, 353-358 (1987)
8. V. Altanerova, J. Ban, and C. Altaner, Induction of immune deficiency syndrome in rabbits by bovine leukaemia virus. AIDS 3, 755-758 (1989)
9. V. Altanerova, D. Porteteile, R. Kettmann, and C. Altaner, Infection of rats with bovine leukaemia virus: establishment of a virus-producing rat cell line. J. Gen. Virol. 70 (Pt 7), 1929-1932 (1989)
10. C. R. Wyatt, D. Wingett, J. S. White, C. D. Buck, D. Knowles, R. Reeves, and N. S. Magnuson, Persistent infection of rabbits with bovine leukemia virus associated with development of immune dysfunction. J. Virol. 63, 4498-4506 (1989)
11. M. Onuma, K. Tsukiyama, K. Ohya, Y. Morishima, and R. Ohno, Detection of cross-reactive antibody to BLV p24 in sera of human patients infected with HTLV. Microbiol. Immunol. 31, 131-137 (1987)
12. G. C. Buehring, S. M. Philpott, and K. Y. Choi, Humans have antibodies reactive with Bovine leukemia virus. AIDS Res. Hum. Retroviruses 19, 1105-1113 (2003)
13. R. F. DiGiacomo and S. G. Hopkins, Food animal and poultry retroviruses and human health. Vet. Clin. North Am. Food Anim Pract. 13, 177-190 (1997)
14. R. Z. Mamoun, M. Morisson, N. Rebeyrotte, B. Busetta, D. Couez, R. Kettmann, M. Hospital, and B. Guillemain, Sequence variability of bovine leukemia virus env gene and its relevance to the structure and antigenicity of the glycoproteins. J. Virol. 64, 4180-4188 (1990)
15. S. Alexandersen, S. Carpenter, J. Christensen, T. Storgaard, B. Viuff, Y. Wannemuehler, J. Belousov, and J. A. Roth, Identification of alternatively spliced mRNAs encoding potential new regulatory proteins in cattle infected with bovine leukemia virus. J. Virol. 67, 39-52 (1993)
16. D. Derse, Bovine leukemia virus transcription is controlled by a virus-encoded trans-acting factor and by cis-acting response elements. J. Virol. 61, 2462-2471 (1987)
17. D. Derse, trans-acting regulation of bovine leukemia virus mRNA processing. J. Virol. 62, 1115-1119 (1988)
18. L. Lefebvre, A. Vanderplasschen, V. Ciminale, H. Heremans, O. Dangoisse, J. C. Jauniaux, J. F. Toussaint, V. Zelnik, A. Burny, R. Kettmann, and L. Willems, Oncoviral bovine leukemia virus G4 and human T-cell leukemia virus type l p 13(II) accessory proteins interact with farnesyl pyrophosphate synthetase. J. Virol. 76, 1400-1414 (2002)
19. N. R. Rice, R. M. Stephens, D. Couez, J. Deschamps, R. Kettmann, A. Burny and R. V Gilden, The nucleotide sequence of the env gene and post-env region of bovine leukemia virus. Virology 138, 82-93 (1984)
20. N. R. Rice, R. M. Stephens, A. Burny, and R. V. Gilden, The gag and pol genes of bovine leukemia virus: nucleotide sequence and analysis. Virology 142, 357-377 (1985)
21. N. Sagata, T. Yasunaga, K. Ohishi, J. Tsuzuku-Kawamura, M. Onuma, and Y. Ikawa, Comparison of the entire genomes of bovine leukemia virus and human T-cell leukemia virus and characterization of their unidentified open reading frames. EMBO J. 3, 3231 -3237 ( 1984)
22. L. Willems, A. Gegonne, G. Chen, A. Burny, R. Kettmann, and J. Ghysdael, The bovine leukemia virus p34 is a transactivator protein. EMBOJ. 6, 3385-3389 (1987)
23. P. Kerkhofs, H. Heremans, A. Burny, R. Kettmann, and L. Willems, In vitro and in vivo oncogenic potential of bovine leukemia virus G4 protein. J. Virol. 72, 2554-2559 (1998)
24. J. C. Twizere, P. Kerkhofs, A. Burny, D. Portetelle, R. Kettmann, and L. Willems, Discordance between bovine leukemia virus tax immortalization in vitro and oncogenicity in vivo. J. Virol. 74, 9895-9902 (2000)
25. L. Willems, P. Kerkhofs, F. Dequiedt, D. Portetelle, M. Mammerickx, A. Burny, and R. Kettmann, Attenuation of bovine leukemia virus by deletion of R3 and G4 open reading frames. Proc. Natl. Acad. Sci. U. S A 91, 11532-11536 (1994)
26. L. Willems, A. Burny, D. Collete, O. Dangoisse, F. Dequiedt, J. S. Gatot, P. Kerkhofs, L. Lefebvre, C. Merezak, T. Peremans, D. Portetelle, J. C. Twizere, and R. Kettmann, Genetic determinants of bovine leukemia virus pathogenesis. AIDS Res. Hum. Retroviruses 16, 1787-1795 (2000)
27. L. Willems, A. Burny, O. Dangoisse, D. Collete, F. Dequiedt, J. S. Gatot, P. Kerkhofs, L. Lefebvre, C. Merezak, D. Portetelle, J. C. Twizere, and R. Kettmann. Bovine leukemia virus as a model for human T-cell leukemia virus. Current Topics in Virology 1, 139-167. (1999)
28. M. Mammerickx, D. Portetelle, and A. Bumy, Experimental cross-transmissions of bovine leukemia virus (BLV) between several animal species. Zentralbl. Veterinarmed. B 28, 69-81 (1981)
29. A. Bumy, F. Bex, C. Brück, Y. Cleuter, D. Dekegel, J. Ghysdael, R. Kettmann, M. Leclercq, M. Mammerickx, and D. Portetelle, Biochemical and epidemiological studies on bovine leukemia virus (BLV) Haematol. Blood Transfus. 23, 445-452 (1979)
30. V. Moules, C. Pomier, D. Sibon, A. S. Gabet, N. Reichert, P. Kerkhofs, L. Willems, F. Mortreux, and E. Wattel, Fate of premalignant clones during the asymptomatic phase preceding lymphoid malignancy. Cancer Research 65, 1234-1243 (2005)
31. F. Dequiedt, R. Kettmann, A. Burny, and L. Willems, Mutations in the p53 tumor-suppressor gene are frequently associated with bovine leukemia virus-induced leukemogenesis in cattle but not in sheep. Virology 209, 676-683 (1995)
32. W. Zhuang, S. Tajima, K. Okada, Y. Ikawa, and Y. Aida, Point mutation of p53 tumor suppressor gene in bovine leukemia virus-induced lymphosarcoma. Leukemia 11 Suppl 3, 344-346 (1997)
33. S. Tajima, W. Z. Zhuang, M. V. Kato, K. Okada, Y. Ikawa, and Y. Aida, Function and conformation of wild-type p53 protein are influenced by mutations in bovine leukemia virus-induced B-cell lymphosarcoma. Virology 243, 735-746 (1998)
34. G. G. Dimijian, Evolving together: the biology of symbiosis, part 1. Proc. (Bayl. Univ Med. Cent. ) 13, 217-226 (2000)
35. M. A. Gilchrist and D. Coombs, Evolution of virulence: Interdependence, constraints, and selection using nested models. Theor. Popul. Biol. 69, 145-153 (2006)
36. K. Radke, D. Grossman, and L. C. Kidd, Humoral immune response of experimentally infected sheep defines two early periods of bovine leukemia virus replication. Microb. Pathog. 9, 159-171 (1990)
37. D. Portetelle, M. Mammerickx, and A. Burny, Use of two monoclonal antibodies in an ELISA test for the detection of antibodies to bovine leukaemia virus envelope protein gp51. J. Virol. Methods 23, 211-222 (1989)
38. D. Portetelle, C. Bruck, A. Burny, D. Dekegel, M. Mammerickx, and J. Urbain, Detection of complement-dependent lytic antibodies in sera from bovine leukemia virus-infected animals. Ann. Rech. Vet. 9, 667-674 (1978)
39. A. D. Hislop, M. F. Good, L. Mateo, J. Gardner, M. H. Gatei, R. C. Daniel, B. V. Meyers, M. F. Lavin, and A. Suhrbier, Vaccine-induced cytotoxic T lymphocytes protect against retroviral challenge. Nat. Med. 4, 1193-1196 (1998)
40. H. Kabeya, K. Ohashi, and M. Onuma, Host immune responses in the course of bovine leukemia virus infection. J. Vet. Med. Sci. 63, 703-708 (2001)
41. P. Lundberg and G. A. Splitter, gammadelta(+) T-Lp6phocyte cytotoxicity against envelope-expressing target cells is unique to the alymphocytic state of bovine leukemia virus infection in the natural host. J. Virol. 74, 8299-8306 (2000)
42. I. Callebaut, V. Voneche, A. Mager, O. Furniere, V. Krchnak, M. Merza, J. Zavada, M. Mammerickx, A. Burny, and D. Portetelle, Mapping of B-neutralizing and T-helper cell epitopes on the bovine leukemia virus external glycoprotein gp51. J. Virol. 61, 5321-5327 (1993)
43. H. Kabeya, K. Ohashi, C. Sugimoto, and M. Onuma, Characterization of immune responses caused by bovine leukemia virus envelope peptides in sheep. J. Vet. Med. Sci. 61, 475-480 (1999)
44. D. M. Stone, L. K. Norton, J. C. Chambers, and W. J. Meek, CD4 T lymphocyte activation in BLV-induced persistent B lymphocytosis in cattle. Clin. Immunol. 96, 280-288 (2000)
45. H. A. Lewin, G. C. Russell, and E. J. Glass, Comparative organization and function of the major histocompatibility complex of domesticated cattle. Immunol. Rev. 167, 145-158 (1999)
46. Y. Nagaoka, H. Kabeya, M. Onuma, N. Kasai, K. Okada, and Y. Aida, Ovine MHC class II DRB1 alleles associated with resistance or susceptibility to development of bovine leukemia virus-induced ovine lymphoma. Cancer Res. 59, 975-981 (1999)
47. R. Meirom, S. Moss, J. Brenner, D. Heller, and Z. Trainin, Levels and role of cytokines in bovine leukemia virus (BLV) infection. Leukemia 11 Suppl 3, 219-220 (1997)
48. H. Kabeya, A. Fukuda, K. Ohashi, C. Sugimoto, and M. Onuma, Tumor necrosis factor alpha and its receptors in experimentally bovine leukemia virus-infected sheep. Vet. Immunol. Immunopathol. 81, 129-139 (2001)
49. J. C. Twizere, V. Kruys, L. Lefebvre, A. Vanderplasschen, D. Collete, C. Debacq, W. S. Lai, J. C. Jauniaux, L. R. Bernstein, O. J. Semmes, A. Burny, P. J. Blackshear, R. Kettmann, and L. Willems, Interaction of retroviral Tax oncoproteins with tristetraprolin and regulation of tumor necrosis factor-alpha expression. J. Natl. Cancer Inst. 95, 1846-1859 (2003)
50. S. Konnai, T. Usui, K. Ohashi, and M. Onuma, The rapid quantitative analysis of bovine cytokine genes by real-time RT-PCR. Vet. Microbiol. 94, 283-294 (2003)
51. R. G. Keefe, Y. Choi, D. A. Ferrick, and J. L. Stott, Bovine cytokine expression during different phases of bovine leukemia virus infection. Vet. Immunol. Immunopathol. 56, 39-51 (1997)
52. D. Pyeon and G. A. Splitter, Regulation of bovine leukemia virus tax and pol mRNA levels by interleukin-2 and -10. J. Virol. 73, 8427-8434 (1999)
53. B. Yakobson, J. Brenner, H. Ungar-Waron, and Z. Trainin, Cellular immune response cytokine expression during the initial stage of bovine leukemia virus (BLV) infection determines the disease progression to persistent lymphocytosis. Comp Immunol. Microbiol. Infect. Dis. 23, 197-208 (2000)
54. M. Amills, V. Ramiya, J. Norimine, C. A. Olmstead, and H. A. Lewin, Reduced IL-2 and IL-4 mRNA expression in CD4+ T cells from bovine leukemia virusinfected cows with persistent lymphocytosis. Virology 304, 1-9 (2002)
55. M. Amills, J. Norimine, C. A. Olmstead, and H. A. Lewin, Cytokine mRNA expression in B cells from bovine leukemia virus-infected cattle with persistent lymphocytosis. Cytokine 28, 25-28 (2004)
56. M. B. A. Oldstone, Viral persistence: Parameters, mechanisms and future predictions. Virology 344, 111-118 (2006)
57. E. M. Gaynor, M. L. Mirsky, and H. A. Lewin, Use of flow cytometry and RT-PCR for detecting gene expression by single cells. Biotechniques 2l, 286-291 (1996)
58. W. A. Jensen, J. Rovnak, and G. L. Cockerell, In vivo transcription of the bovine leukemia virus tax/rex region in normal and neoplastic lymphocytes of cattle and sheep. J. Virol. 65, 2484-2490 (1991)
59. D. M. Lagarias and K. Radke, Transcriptional activation of bovine leukemia virus in blood cells from experimentally infected, asymptomatic sheep with latent infections. J. Virol. 63, 2099-2107 (1989)
60. K. Radke, T. J. Sigala, and D. Grossman, Transcription of bovine leukemia virus in peripheral blood cells obtained during early infection in vivo. Microb. Pathog. 12, 319-331 (1992)
61. P. Gupta, S. V. Kashmiri, and J. F. Ferrer, Transcriptional control of the bovine leukemia virus genome: role and characterization of a nonimmunoglobulin plasma protein from bovine leukemia virus-infected cattle. J. Virol. 50, 267-270 (1984)
62. M. J. van den Heuvel, B. J. Jefferson, and R. M. Jacobs, Isolation of a bovine plasma fibronectin-containing complex which inhibits the expression of bovine leukemia virus p24. J. Virol. 79, 8164-8170 (2005)
63. S. Tajima and Y. Aida, Induction of expression of bovine leukemia virus (BLV) in blood taken from BLV-infected cows without removal of plasma. Microbes Infect. 7, 1211-1216 (2005)
64. E. Wattel, M. Cavrois, A. Gessain, and S. WainHobson, Clonal expansion of infected cells: A way of life for HTLV-I. Journal of Acquired Immune Deficiency Syndromes and Human Retrovirology 13, S92-S99 (1996)
65. S. Tajima, M. Takahashi, S. N. Takeshima, S. Konnai, S. A. Yin, S. Watarai, Y. Tanaka, M. Onuma, K. Okada, and Y. Aida, A mutant form of the tax protein of bovine leukemia virus (BLV), with enhanced transactivation activity, increases expression and propagation of BLV in vitro but not in vivo. J. Virol. 77, 1894-1903 (2003)
66. L. Willems, H. Heremans, G. Chen, D. Porteteile, A. Billiau, A. Burny, and R. Kettmann, Cooperation between bovine leukaemia virus transactivator protein and Ha-ras oncogene product in cellular transformation. EMBOJ. 9,1577-1581 (1990)
67. L. Willems, C. Grimonpont, P. Kerkhofs, C. Capiau, D. Gheysen, K. Conrath, R. Roussef, R. Mamoun, D. Portetelle, A. Burny, E. Adam, L. Lefebvre, J. C. Twizere, H. Heremans, and R. Kettmann, Phosphorylation of bovine leukemia virus Tax protein is required for in vitro transformation but not for transactivation. Oncogene 16, 2165-2176 (1998)
68. M. L. Yeung, Y. Bennasser, S. Y. Le, and K. T. Jeang, siRNA, miRNA and HTV: promises and challenges. Cell Research 15, 935-946 (2005)
69. F. Dequiedt, E. Hanon, P. Kerkhofs, P. P. Pastoret, D. Portetelle, A. Burny, R. Kettmann, and L. Willems, Both wild-type and strongly attenuated bovine leukemia viruses protect peripheral blood mononuclear cells from apoptosis. J. Virol. 71, 630-639 (1997)
70. I. Schwartz-Cornil, N. Chevallier, C. Belloc, D. Le Rhun, V. Laine, M. Berthelemy, A. Mateo, and D. Levy, Bovine leukaemia virus-induced lymphocytosis in sheep is associated with reduction of spontaneous B cell apoptosis. J. Gen. Virol. 78 (Pt 1), 153-162 (1997)
71. C. Debacq, B. Asquith, P. Kerkhofs, D. Portetelle, A. Burny, R. Kettmann, and L. Willems, Increased cell proliferation, but not reduced cell death, induces lymphocytosis in bovine leukemia virus-infected sheep. Proc. Natl. Acad. Sci. U. SA 99, 10048-10053 (2002)
72. A. Jacobs, Myelodysplastic syndromes: pathogenesis, functional abnormalities, and clinical implications. J. Clin. Pathol. 38, 1201-1217 (1985)
73. C. Debacq, B. Asquith, M. Reichert, A. Burny, R. Kettmann, and L. Willems, Reduced cell turnover in bovine leukemia virus-infected, persistently lymphocytotic cattle. J. Virol. 77, 13073-13083 (2003)
74. B. Ristevski, A. J. Young, L. Dudler, R. N. P. Cahill, W. Kimpton, E. Washington, and J. B. Hay, Tracking dendritic cells: use of an in situ method to label all blood leukocytes. International Immunology 15, 159-165 (2003)
75. J. B. Hay and W. N. Andrade, Lymphocyte recirculation, exercise, and immune responses. Can. J. Physiol Pharmacol. 76, 490-496 (1998)
76. W. R. Hein and P. J. Griebel, A road less travelled: large animal models in immunological research. Nat. Rev. Immunol. 3, 79-84 (2003)
77. A. J. Young, J. B. Hay, and C. R. Mackay, Lymphocyte recirculation and life span in vivo. Curr. Top. Microbiol. Immunol 184, 161-173 (1993)
78. B. Asquith, C. Debacq, A. Florins, N. Gillet, M. T. Sanchez Alcaraz, A. Mosley, and L. Willems. Quantifying lymphocyte kinetics in vivo using CFSE. Proceedings of the Royal Society of London in press. 2006.
79. C. Yoo and P. Jones. Epigenetic therapy of cancer: past, present and future. Nature reviews 5, 37-50. 2006.
80. R. A. Blaheta, H. Nau, M. Michaelis, and J. Cinatl, Valproate and valproate-analogues: Potent tools to fight against cancer. Current Medicinal Chemistry 9, 1417-1433 (2002)
81. A. Achachi, A. Florins, N. Gillet, C. Debacq, P. Urbain, G. M. Foutsop, F. Vandermeers, A. Jasik, M. Reichert, P. Kerkhofs, L. Lagneaux, A. Burny, R. Kettmann, and L. Willems, Valproate activates bovine leukemia virus gene expression, triggers apoptosis, and induces leukemia/lymphoma regression in vivo. Proc. Natl. Acad. Sci. U. SA 102, 10309-10314 (2005)
82. D. C. Drummond, C. O. Noble, D. B. Kirpotin, Z. X. Guo, G. K. Scott, and C. C. Benz, Clinical development of histone deacetylase inhibitors as anticancer agents. Annual Review of Pharmacology and Toxicology 45, 495-528 (2005)
83. A. Insinga, S. Monestiroli, S. Ronzoni, V. Gelmetti, F. Marchesi, A. Viale, L. Altucci, C. Nervi, S. Minucci, and P. G. Pelicci, Inhibitors of histone deacetylases induce tumorselective apoptosis through activation of the death receptor pathway. Nature Medicine 11, 71-76 (2005)
84. A. Nebbioso, N. Clarke, E. Voltz, E. Germain, C. Ambrosino, P. Bontempo, R. Alvarez, E. M. Schiavone, F. Ferrara, F. Bresciani, A. Weisz, A. R. de Lera, H. Gronemeyer, and L. Altucci, Tumor-selective action of HDAC inhibitors involves TRAIL induction in acute myeloid leukemia cells. Nature Medicine 11, 77-84 (2005)
85. C. R. M. Bangham and M. Osame, Cellular immune response to HTLV-1. Oncogene 24, 6035-6046 (2005)
86. C. Merezak, C. Pierreux, E. Adam, F. Lemaigre, G. G. Rousseau, C. Calomme, C. Van Lint, D. Christophe, P. Kerkhofs, A. Bumy, R. Kettmann, and L. Willems, Suboptimal enhancer sequences are required for efficient bovine leukemia virus propagation in vivo: implications for viral latency. J. Virol. 75, 6977-6988 (2001)
87. C. Debacq, M. T. Sanchez Alcaraz, F. Mortreux, P. Kerkhofs, R. Kettmann, and L. Willems, Reduced proviral loads during primo-infection of sheep by Bovine Leukemia virus attenuated mutants. Retrovirology 1, 31 (2004)
88. M. A. Powers and K. Radke, Activation of bovine leukemia virus transcription in lymphocytes from infected sheep: rapid transition through early to late gene expression. J. Virol. 66, 4769-4777 (1992)
89. L. Willems, R. Kettmann, F. Dequiedt, D. Portetelle, V. Voneche, I. Cornil, P. Kerkhofs, A. Burny, and M. Mammerickx, In vivo infection of sheep by bovine leukemia virus mutants. J. Virol. 67, 4078-4085 (1993)
90. V. Ciminale, G. N. Pavlakis, D. Derse, C. P. Cunningham, and B. K. Felber, Complex splicing in the human T-cell leukemia virus (HTLV) family of retroviruses: novel mRNAs and proteins produced by HTLV type I. J. Virol. 66, 1737-1745 (1992)