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Induction and regulation of Trypanosoma brucei VSG-specific antibody responses

Published online by Cambridge University Press:  22 December 2009

S. J. BLACK ,
P. GUIRNALDA ,
D. FRENKEL ,
C. HAYNES  and
V. BOCKSTAL
S. J. BLACK*
Affiliation:
Department of Veterinary and Animal Sciences, University of Massachusetts, Amherst, Massachusetts, USA
P. GUIRNALDA
Affiliation:
Department of Veterinary and Animal Sciences, University of Massachusetts, Amherst, Massachusetts, USA
D. FRENKEL
Affiliation:
Department of Veterinary and Animal Sciences, University of Massachusetts, Amherst, Massachusetts, USA
C. HAYNES
Affiliation:
Laboratory for Cellular and Molecular Immunology, Vrije Universiteit Brussel, Pleinlaan 2, B-1050Brussels, Belgium Department of Molecular and Cellular Interactions, VIB, Brussels, Belgium
V. BOCKSTAL
Affiliation:
Laboratory for Cellular and Molecular Immunology, Vrije Universiteit Brussel, Pleinlaan 2, B-1050Brussels, Belgium Department of Molecular and Cellular Interactions, VIB, Brussels, Belgium
*
*Corresponding author: Department of Veterinary and Animal Sciences, University of Massachusetts-Amherst, MA, 01003, USA. Tel: 413 545 2573. Fax: 413 545 6326. E-mail: [email protected]
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Summary

The review addresses how infection with Trypanosoma brucei affects the development, survival and functions of B lymphocytes in mice. It discusses (1) the contributions of antibodies to trypanosome clearance from the bloodstream, (2) how B lymphocytes, the precursors of antibody producing plasma cells, interact with membrane form variable surface glycoprotein (VSG), i.e. with monovalent antigen that is free to diffuse within the lipid bilayer of the trypanosome plasma membrane and consequently can cross-link B cell antigen specific receptors by indirect processes only and (3) the extent and underlying causes of dysregulation of humoral immune responses in infected mice, focusing on the impact of wild type and GPI-PLC−/− trypanosomes on bone marrow and extramedullary B lymphopoiesis, B cell maturation and survival.

Keywords

T. bruceiantibody clearanceB cell activationB cell deletion
Type
Research Article
Information
Parasitology , Volume 137 , Special Issue 14: African trypanosomiasis: New insights for disease control , December 2010 , pp. 2041 - 2049
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Alugupalli, K. R. (2008). A distinct role for B1b lymphocytes in T cell-independent immunity. Current topics in Microbiology and Immunology 319, 105–130.Google ScholarPubMed
Black, S. J., Sendashonga, C. N., Webster, P., Koch, G. L. and Shapiro, S. Z. (1986). Regulation of parasite-specific antibody responses in resistant (C57BL/6) and susceptible (C3H/HE) mice infected with Trypanosoma (Trypanozoon) brucei brucei. Parasite Immunology 8, 425–442.CrossRefGoogle ScholarPubMed
Bolow, R., Griffiths, G., Webster, P., Stierhof, Y. D., Opperdoes, F. R. and Overath, P. (1989). Intracellular localization of the glycosyl-phosphatidylinositol-specific phospholipase C of Trypanosoma brucei. Journal of Cell Science 93, 233–240.CrossRefGoogle ScholarPubMed
Cardoso de Almeida, M. L., Allan, L. M. and Turner, M. J. (1984). Purification and properties of the membrane form of variant surface glycoproteins (VSGs) from Trypanosoma brucei. Journal of Protozoology 31, 53–60.CrossRefGoogle ScholarPubMed
Clayton, C. E., Selkirk, M. E., Corsini, C. A., Ogilvie, B. M. and Askonas, B. A. (1980). Murine trypanosomiasis: cellular proliferation and functional depletion in the blood, peritoneum, and spleen related to changes in bone marrow stem cells. Infection and Immunity 28, 824–831.CrossRefGoogle ScholarPubMed
Cronin, C. N., Nolan, D. P. and Voorheis, H. P. (1989). The enzymes of the classical pentose phosphate pathway display differential activities in procyclic and bloodstream forms of Trypanosoma brucei. FEBS Letters 244, 26–30.CrossRefGoogle ScholarPubMed
Dempsey, W. L. and Mansfield, J. M. (1983). Lymphocyte function in experimental African trypanosomiasis. V. Role of antibody and the mononuclear phagocyte system in variant-specific immunity. Journal of Immunology 130, 405–411.CrossRefGoogle ScholarPubMed
Depoil, D., Fleire, S., Treanor, B. L., Weber, M., Harwood, N. E., Marchbank, K. L., Tybulewicz, V. L. and Batista, F. D. (2008). CD19 is essential for B cell activation by promoting B cell receptor-antigen microcluster formation in response to membrane-bound ligand. Nature Immunology 9, 63–72.CrossRefGoogle ScholarPubMed
Dubois, M. E., Demick, K. P. and Mansfield, J. M. (2005). Trypanosomes expressing a mosaic variant surface glycoprotein coat escape early detection by the immune system. Infection and Immunity 73, 2690–2697.CrossRefGoogle ScholarPubMed
Duleu, S., Vincendeau, P., Courtois, P., Semballa, S., Lagroye, I., Daulouede, S., Boucher, J. L., Wilson, K. T., Veyret, B. and Gobert, A. P. (2004). Mouse strain susceptibility to trypanosome infection: an arginase-dependent effect. Journal of Immunology 172, 6298–6303.CrossRefGoogle ScholarPubMed
Engstler, M., Pfohl, T., Herminghaus, S., Boshart, M., Wiegertjes, G., Heddergott, N. and Overath, P. (2007). Hydrodynamic flow-mediated protein sorting on the cell surface of trypanosomes. Cell 131, 505–515.CrossRefGoogle ScholarPubMed
Guirnalda, P., Murphy, N. B., Nolan, D. and Black, S. J. (2007). Anti-Trypanosoma brucei activity in Cape buffalo serum during the cryptic phase of parasitemia is mediated by antibodies. International Journal for Parasitology 37, 1391–1399.CrossRefGoogle ScholarPubMed
Hanrahan, O., Webb, H., O'Byrne, R., Brabazon, E., Treumann, A., Sunter, J. D., Carrington, M. and Voorheis, H. P. (2009). The glycosylphosphatidylinositol-PLC in Trypanosoma brucei forms a linear array on the exterior of the flagellar membrane before and after activation. PLoS Pathogens 5, e1000468.CrossRefGoogle ScholarPubMed
Karpusas, M., Lucci, J., Ferrant, J., Benjamin, C., Taylor, F. R., Strauch, K., Garber, E. and Hsu, Y. M. (2001). Structure of CD40 ligand in complex with the Fab fragment of a neutralizing humanized antibody. Structure 9, 321–329.CrossRefGoogle ScholarPubMed
Kaushik, R. S., Uzonna, J. E., Gordon, J. R. and Tabel, H. (1999). Innate resistance to Trypanosoma congolense infections: differential production of nitric oxide by macrophages from susceptible BALB/c and resistant C57Bl/6 mice. Experimental Parasitology 92, 131–143.CrossRefGoogle ScholarPubMed
Kitani, H., Black, S. J., Nakamura, Y., Naessens, J., Murphy, N. B., Yokomizo, Y., Gibson, J. and Iraqi, F. (2002). Recombinant tumor necrosis factor alpha does not inhibit the growth of African trypanosomes in axenic cultures. Infection and Immunity 70, 2210–2214.CrossRefGoogle Scholar
Kraal, G. and Mebius, R. (2006). New insights into the cell biology of the marginal zone of the spleen. International Reviews of Cytology 250, 175–215.CrossRefGoogle ScholarPubMed
Lok, S. M., Kostyuchenko, V., Nybakken, G. E., Holdaway, H. A., Battisti, A. J., Sukupolvi-Petty, S., Sedlak, D., Fremont, D. H., Chipman, P. R., Roehrig, J. T., Diamond, M. S., Kuhn, R. J. and Rossmann, M. G. (2008). Binding of a neutralizing antibody to dengue virus alters the arrangement of surface glycoproteins. Nature Structural and Molecular Biology 15, 312–317.CrossRefGoogle ScholarPubMed
Lopes-Carvalho, T. and Kearney, J. F. (2004). Development and selection of marginal zone B cells. Immunological Reviews 197, 192–205.CrossRefGoogle ScholarPubMed
Macaskill, J. A., Holmes, P. H., Whitelaw, D. D., McConnell, I., Jennings, F. W. and Urquhart, G. M. (1980). Immunological clearance of 75Se-labelled Trypanosoma brucei in mice. II. Mechanisms in immune animals. Immunology 40, 629–635.Google ScholarPubMed
Magez, S., Radwanska, M., Drennan, M., Fick, L., Baral, T. N., Brombacher, F. and De Baetselier, P. (2006). Interferon-gamma and nitric oxide in combination with antibodies are key protective host immune factors during Trypanosoma congolense Tc13 Infections. Journal of Infectious Diseases 193, 1575–1583.CrossRefGoogle ScholarPubMed
Magez, S., Radwanska, M., Stijlemans, B., Xong, H. V., Pays, E. and De Baetselier, P. (2001). A conserved flagellar pocket exposed high mannose moiety is used by African trypanosomes as a host cytokine binding molecule. Journal of Biological Chemistry 276, 33458–33464.CrossRefGoogle ScholarPubMed
Magez, S., Stijlemans, B., Radwanska, M., Pays, E., Ferguson, M. A. and De Baetselier, P. (1998). The glycosyl-inositol-phosphate and dimyristoylglycerol moieties of the glycosylphosphatidylinositol anchor of the trypanosome variant-specific surface glycoprotein are distinct macrophage-activating factors. Journal of Immunology 160, 1949–1956.CrossRefGoogle ScholarPubMed
Mansfield, J. M. and Paulnock, D. M. (2008). Genetic manipulation of African trypanosomes as a tool to dissect the immunobiology of infection. Parasite Immunology 30, 245–253.CrossRefGoogle ScholarPubMed
Marcello, L. and Barry, J. D. (2007). Analysis of the VSG gene silent archive in Trypanosoma brucei reveals that mosaic gene expression is prominent in antigenic variation and is favored by archive substructure. Genome Research 17, 1344–1352.CrossRefGoogle ScholarPubMed
McLintock, L. M., Turner, C. M. and Vickerman, K. (1993). Comparison of the effects of immune killing mechanisms on Trypanosoma brucei parasites of slender and stumpy morphology. Parasite Immunology 15, 475–480.CrossRefGoogle ScholarPubMed
Mehlert, A., Bond, C. S. and Ferguson, M. A. (2002). The glycoforms of a Trypanosoma brucei variant surface glycoprotein and molecular modeling of a glycosylated surface coat. Glycobiology 12, 607–612.CrossRefGoogle ScholarPubMed
Muranjan, M., Wang, Q., Li, Y. L., Hamilton, E., Otieno-Omondi, F. P., Wang, J., Van Praagh, A., Grootenhuis, J. G. and Black, S. J. (1997). The trypanocidal Cape buffalo serum protein is xanthine oxidase. Infection and Immunity 65, 3806–3814.CrossRefGoogle ScholarPubMed
Namangala, B., De Baetselier, P., Noel, W., Brys, L. and Beschin, A. (2001). Alternative versus classical macrophage activation during experimental African trypanosomosis. Journal of Leukocyte Biology 69, 387–396.CrossRefGoogle ScholarPubMed
Natesan, S. K., Peacock, L., Matthews, K., Gibson, W. and Field, M. C. (2007). Activation of endocytosis as an adaptation to the mammalian host by trypanosomes. Eukaryotic Cell 6, 2029–2037.CrossRefGoogle Scholar
Newson, J., Mahan, S. M. and Black, S. J. (1990). Synthesis and secretion of immunoglobulin by spleen cells from resistant and susceptible mice infected with Trypanosoma brucei brucei GUTat 3.1. Parasite Immunology 12, 125–139.CrossRefGoogle ScholarPubMed
O'Beirne, C., Lowry, C. M. and Voorheis, H. P. (1998). Both IgM and IgG anti-VSG antibodies initiate a cycle of aggregation-disaggregation of bloodstream forms of Trypanosoma brucei without damage to the parasite. Molecular and Biochemical Parasitology 91, 165–193.CrossRefGoogle ScholarPubMed
Pan, W., Ogunremi, O., Wei, G., Shi, M. and Tabel, H. (2006). CR3 (CD11b/CD18) is the major macrophage receptor for IgM antibody-mediated phagocytosis of African trypanosomes: diverse effect on subsequent synthesis of tumor necrosis factor alpha and nitric oxide. Microbes and Infection 8, 1209–1218.CrossRefGoogle ScholarPubMed
Puffer, E. B., Pontrello, J. K., Hollenbeck, J. J., Kink, J. A. and Kiessling, L. L. (2007). Activating B cell signaling with defined multivalent ligands. ACS Chemical Biology 2, 252–262.CrossRefGoogle ScholarPubMed
Radwanska, M., Guirnalda, P., De Trez, C., Ryffel, B., Black, S. and Magez, S. (2008). Trypanosomiasis-induced B cell apoptosis results in loss of protective anti-parasite antibody responses and abolishment of vaccine-induced memory responses. PLoS Pathogens 4, e1000078.CrossRefGoogle ScholarPubMed
Rolin, S., Hancocq-Quertier, J., Paturiaux-Hanocq, F., Nolan, D. P. and Pays, E. (1998). Mild acid stress as a differentiation trigger in Trypanosoma brucei. Molecular and Biochemical Parasitology 93, 251–262.CrossRefGoogle ScholarPubMed
Roux, K. H., Strelets, L., Brekke, O. H., Sandlie, I. and Michaelsen, T. E. (1998). Comparisons of the ability of human IgG3 hinge mutants, IgM, IgE, and IgA2, to form small immune complexes: a role for flexibility and geometry. Journal of Immunology 161, 4083–4090.CrossRefGoogle ScholarPubMed
Sacco, R. E., Hagen, M., Donelson, J. E. and Lynch, R. G. (1994). B lymphocytes of mice display an aberrant activation phenotype and are cell cycle arrested in G0/G1A during acute infection with Trypanosoma brucei. Journal of Immunology 153, 1714–1723.CrossRefGoogle ScholarPubMed
Sendashonga, C. N. and Black, S. J. (1982). Humoral responses against Trypanosoma brucei variable surface antigen are induced by degenerating parasites. Parasite Immunology 4, 245–257.CrossRefGoogle ScholarPubMed
Sendashonga, C. N. and Black, S. J. (1986). Analysis of B cell and T cell proliferative responses induced by monomorphic and pleomorphic Trypanosoma brucei parasites in mice. Parasite Immunology 8, 443–453.CrossRefGoogle Scholar
Sohn, H. W., Tolar, P. and Pierce, S. K. (2008). Membrane heterogeneities in the formation of B cell receptor-Lyn kinase microclusters and the immune synapse. Journal of Cell Biology 182, 367–379.CrossRefGoogle ScholarPubMed
Subramanya, S. and Mensa-Wilmot, K. (2006). Regulated cleavage of intracellular glycosylphosphatidylinositol in a trypanosome. Peroxisome-to-endoplasmic reticulum translocation of a phospholipase C. FEBS Journal 273, 2110–2126.CrossRefGoogle Scholar
Tachado, S. D. and Schofield, L. (1994). Glycosylphosphatidylinositol toxin of Trypanosoma brucei regulates IL-1 alpha and TNF-alpha expression in macrophages by protein tyrosine kinase mediated signal transduction. Biochemical and Biophysical Research Communications 205, 984–991.CrossRefGoogle ScholarPubMed
Takahashi, Y., Miyamoto, H., Fukuma, T., Nishiyama, T., Araki, T. and Shinka, S. (1987). In vivo interaction between Trypanosoma gambiense and leucocytes in mice. Zentralblat für Bakteriologie, Mikrobiologie und Hygiene A 264, 399–406.Google ScholarPubMed
Tolar, P., Hanna, J., Krueger, P. D. and Pierce, S. K. (2009). The constant region of the membrane immunoglobulin mediates B cell-receptor clustering and signaling in response to membrane antigens. Immunity 30, 44–55.CrossRefGoogle ScholarPubMed
Tung, J. W. and Herzenberg, L. A. (2007). Unraveling B-1 progenitors. Current Opinions in Immunology 19, 150–155.CrossRefGoogle ScholarPubMed
Wang, J., Van Praagh, A., Hamilton, E., Wang, Q., Zou, B., Muranjan, M., Murphy, N. B. and Black, S. J. (2002). Serum xanthine oxidase: origin, regulation, and contribution to control of trypanosome parasitemia. Antioxidants and Redox Signaling 4, 161–178.CrossRefGoogle ScholarPubMed
Webb, H., Carnall, N., Vanhamme, L., Rolin, S., Van Den Abbeele, J., Welburn, S., Pays, E. and Carrington, M. (1997). The GPI-phospholipase C of Trypanosoma brucei is nonessential but influences parasitemia in mice. Journal of Cell Biology 139, 103–114.CrossRefGoogle ScholarPubMed