Peripheral blood B-cell death compensates for excessive proliferation in lymphoid tissues and maintains homeostasis in bovine leukemia virus-infected sheep.
[en] The size of a lymphocyte population is primarily determined by a dynamic equilibrium between cell proliferation and death. Hence, lymphocyte recirculation between the peripheral blood and lymphoid tissues is a key determinant in the maintenance of cell homeostasis. Insights into these mechanisms can be gathered from large-animal models, where lymphatic cannulation from individual lymph nodes is possible. In this study, we assessed in vivo lymphocyte trafficking in bovine leukemia virus (BLV)-infected sheep. With a carboxyfluorescein diacetate succinimidyl ester labeling technique, we demonstrate that the dynamics of lymphocyte recirculation is unaltered but that accelerated proliferation in the lymphoid tissues is compensated for by increased death in the peripheral blood cell population. Lymphocyte homeostasis is thus maintained by biphasic kinetics in two distinct tissues, emphasizing a very dynamic process during BLV infection.
Peripheral blood B-cell death compensates for excessive proliferation in lymphoid tissues and maintains homeostasis in bovine leukemia virus-infected sheep.
Publication date :
2006
Journal title :
Journal of Virology
ISSN :
0022-538X
eISSN :
1098-5514
Publisher :
American Society for Microbiology (ASM), Washington, United States - District of Columbia
Belgian Foundation against the Cancer the 6th Framework program INCA project of the European Union the Bekales Foundation the Fortis Bank Assurance F.R.S.-FNRS - Fonds de la Recherche Scientifique the Leverhulme Trust Interuniversity attraction Poles Programme
Agenes, F., M. M. Rosado, and A. A. Freitas. 2000. Considerations on B cell homeostasis. Curr. Top. Microbiol. Immunol. 252:68-75.
Asquith, B., C. Debacq, A. Florins, N. Gillet, T. Sanchez-Alcaraz, A. Mosley, and L. Willems. 2006. Quantifying lymphocyte kinetics in vivo using carboxyfluorescein diacetate succinimidyl ester (CFSE). Proc. Biol. Sci. 273:1165-1171.
Becker, H. M., M. Chen, J. B. Hay, and M. I. Cybulsky. 2004. Tracking of leukocyte recruitment into tissues of mice by in situ labeling of blood cells with the fluorescent dye CFDA SE. J. Immunol. Methods 286:69-78.
Campbell, D. J., C. H. Kim, and E. C. Butcher. 2003. Chemokines in the systemic organization of immunity. Immunol. Rev. 195:58-71.
Chevallier, N., M. Berthelemy, D. Le Rhun, V. Laine, D. Levy, and I. Schwartz-Cornil. 1998. Bovine leukemia virus-induced lymphocytosis and increased cell survival mainly involve the CD11b+ B-lymphocyte subset in sheep. J. Virol. 72:4413-4420.
Cunningham, C. P., W. G. Kimpton, J. E. Holder, and R. N. Cahill. 2001. Thymic export in aged sheep: a continuous role for the thymus throughout pre- and postnatal life. Eur. J. Immunol. 31:802-811.
Debacq, C., B. Asquith, P. Kerkhofs, D. Portetelle, A. Burny, R. Kettmann, and L. Willems. 2002. Increased cell proliferation, but not reduced cell death, induces lymphocytosis in bovine leukemia virus-infected sheep. Proc. Natl. Acad. Sci. USA 99:10048-10053.
Debacq, C., B. Asquith, M. Reichert, A. Burny, R. Kettmann, and L. Willems. 2003. Reduced cell turnover in bovine leukemia virus-infected, persistently lymphocytotic cattle. J. Virol. 77:13073-13083.
Debacq, C., J. M. Heraud, B. Asquith, C. Bangham, F. Merien, V. Moules, F. Mortreux, E. Wattel, A. Burny, R. Kettmann, M. Kazanji, and L. Willems. 2005. Reduced cell turnover in lymphocytic monkeys infected by human T-lymphotropic virus type 1. Oncogene 24:7514-7523.
Debacq, C., M. T. Sanchez Alcaraz, F. Mortreux, P. Kerkhofs, R. Kettmann, and L. Willems. 2004. Reduced proviral loads during primo-infection of sheep by bovine leukemia virus attenuated mutants. Retrovirology 1:31.
Freitas, A. A., and B. Rocha. 2000. Population biology of lymphocytes: the flight for survival. Annu. Rev. Immunol. 18:83-111.
Gaudin, E., M. Rosado, F. Agenes, A. McLean, and A. A. Freitas. 2004. B-cell homeostasis, competition, resources, and positive selection by self-antigens. Immunol. Rev. 197:102-115.
Grassmann, R., M. Aboud, and K. T. Jeang. 2005. Molecular mechanisms of cellular transformation by HTLV-1 Tax. Oncogene 24:5976-5985.
Gupta, V. K., I. McConnell, R. G. Dalziel, and J. Hopkins. 1998. Two B cell subpopulations have distinct recirculation characteristics. Eur. J. Immunol. 28:1597-1603.
Hall, J. G., and B. Morris. 1963. The lymph-borne cells of the immune response. Q. J. Exp. Physiol. Cogn. Med. Sci. 48:235-247.
Hein, W. R., and P. J. Griebel. 2003. A road less travelled: large animal models in immunological research. Nat. Rev. Immunol. 3:79-84.
Jeang, K. T., C. Z. Giam, F. Majone, and M. Aboud. 2004. Life, death, and tax: role of HTLV-I oncoprotein in genetic instability and cellular transformation. J. Biol. Chem. 279:31991-31994.
Lagarias, D. M., and K. Radke. 1989. Transcriptional activation of bovine leukemia virus in blood cells from experimentally infected, asymptomatic sheep with latent infections. J. Virol. 63:2099-2107.
Moritoyo, T., S. Izumo, H. Moritoyo, Y. Tanaka, Y. Kiyomatsu, M. Nagai, K. Usuku, M. Sorimachi, and M. Osame. 1999. Detection of human T-lymphotropic virus type I p40tax protein in cerebrospinal fluid cells from patients with human T-lymphotropic virus type I-associated myelopathy/tropical spastic paraparesis. J. Neurovirol. 5:241-248.
Mortreux, F., I. Leclercq, A. S. Gabet, A. Leroy, E. Westhof, A. Gessain, S. Wain-Hobson, and E. Wattel. 2001. Somatic mutation in human T-cell leukemia virus type 1 provirus and flanking cellular sequences during clonal expansion in vivo. J. Natl. Cancer Inst. 93:367-377.
Moules, V., C. Pomier, D. Sibon, A. S. Gabet, M. Reichert, P. Kerkhofs, L. Willems, F. Mortreux, and E. Wattel. 2005. Fate of premalignant clones during the asymptomatic phase preceding lymphoid malignancy. Cancer Res. 65:1234-1243.
Murakami, K., K. Okada, Y. Ikawa, and Y. Aida. 1994. Bovine leukemia virus induces CD5- B cell lymphoma in sheep despite temporarily increasing CD5+ B cells in asymptomatic stage. Virology 202:458-465.
Naessens, J. 1997. Surface Ig on B lymphocytes from cattle and sheep. Int. Immunol. 9:349-354.
Nicot, C., R. L. Harrod, V. Ciminale, and G. Franchini. 2005. Human T-cell leukemia/lymphoma virus type 1 nonstructural genes and their functions. Oncogene 24:6026-6034.
Porteteile, D., M. Mammerickx, and A. Burny. 1989. 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.
Ratner, L. 2005. Pathogenesis and treatment of human T-cell leukemia virus infection. Immunol. Res. 32:217-224.
Ristevski, B., A. J. Young, L. Dudler, R. N. Cahill, W. Kimpton, E. Washington, and J. B. Hay. 2003. Tracking dendritic cells: use of an in situ method to label all blood leukocytes. Int. Immunol. 15:159-165.
Schenkel, A. R., H. Uno, and C. D. Pauza. 1999. Asymptomatic simian immunodeficiency virus infection decreases blood CD4+ T cells by accumulating recirculating lymphocytes in the lymphoid tissues. J. Virol. 73:601-607.
Wang, L., J. J. Chen, B. B. Gelman, R. Konig, and M. W. Cloyd. 1999. A novel mechanism of CD4 lymphocyte depletion involves effects of HIV on resting lymphocytes: induction of lymph node homing and apoptosis upon secondary signaling through homing receptors. J. Immunol. 162:268-276.
Willems, L., 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. 2000. Genetic determinants of bovine leukemia virus pathogenesis. AIDS Res. Hum. Retrovir. 16:1787-1795.
Willems, L., R. Kettmann, F. Dequiedt, D. Portetelle, V. Voneche, I. Cornil, P. Kerkhofs, A. Burny, and M. Mammerickx. 1993. In vivo infection of sheep by bovine leukemia virus mutants. J. Virol. 67:4078-4085.
Yoshida, M. 2005. Discovery of HTLV-1, the first human retrovirus, its unique regulatory mechanisms, and insights into pathogenesis. Oncogene 24:5931-5937.
Young, A. J. 1999. The physiology of lymphocyte migration through the single lymph node in vivo. Semin. Immunol. 11:73-83.
Young, A. J., and J. B. Hay. 1995. Rapid turnover of the recirculating lymphocyte pool in vivo. Int. Immunol. 7:1607-1615.
Young, A. J., W. L. Marston, M. Dessing, L. Dudler, and W. R. Hein. 1997. Distinct recirculating and non-recirculating B-lymphocyte pools in the peripheral blood are defined by coordinated expression of CD21 and L-selectin. Blood 90:4865-4875.