B cell subsets are activated and produce cytokines during early phases of Francisella tularensis LVS infection

Microbial Pathogenesis

Volumn 75, Issue , 2014, Pages 49-58

  Plzakova, Lenka ^a   Kubelkova, Klara ^b   Krocova, Zuzana ^a   Zarybnicka, Lenka ^b   Sinkorova, Zuzana ^b   Macela, Ales ^a  

^a UNIVERSITY OF DEFENCE   (Czech Republic)

^b Department of Radiobiology FMHS UO   (Czech Republic)

Author keywords

Activating markers; Antigen presenting function; B cells; Cytokines; F.tularensis

Indexed keywords

B7 ANTIGEN; CD19 ANTIGEN; CD69 ANTIGEN; CD86 ANTIGEN; GAMMA INTERFERON; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 23; INTERLEUKIN 4; INTERLEUKIN 6; LIVE VACCINE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE; HLA ANTIGEN CLASS 2; LEUKOCYTE ANTIGEN;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; B LYMPHOCYTE; BACTERIAL STRAIN; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; IMMUNOREGULATION; IN VIVO STUDY; LYMPHOCYTE ACTIVATION; LYMPHOCYTE FUNCTION; MOUSE; MURINE MODEL; NONHUMAN; PERITONEUM CELL; SPLEEN CELL; TULAREMIA; ANIMAL; BAGG ALBINO MOUSE; CHEMISTRY; DISEASE MODEL; FEMALE; IMMUNOLOGY; PERITONEUM; SECRETION (PROCESS); SPLEEN; TIME;

FRANCISELLA TULARENSIS;

ANIMALS; ANTIGENS, CD; B-LYMPHOCYTE SUBSETS; CYTOKINES; DISEASE MODELS, ANIMAL; FEMALE; HISTOCOMPATIBILITY ANTIGENS CLASS II; LYMPHOCYTE ACTIVATION; MICE, INBRED BALB C; PERITONEUM; SPLEEN; TIME FACTORS; TULAREMIA;

EID: 84908661658     PISSN: 08824010     EISSN: 10961208     Source Type: Journal    
DOI: 10.1016/j.micpath.2014.08.009     Document Type: Article

References (55)

1. Foley J.E., Nieto N.C. Tularemia. Vet Microbiol 2010, 140:332-338.
2. Elkins K.L., Bosio C.M., Rhinehart-Jones T.R. Importance of B cells, but not specific antibodies, in primary and secondary protective immunity to the intracellular bacterium Francisella tularensis live vaccine strain. Infect Immun 1999, 67:6002-6007.
3. Culkin S.J., Rhinehart-Jones T., Elkins K.L. Anovel role for B cells in early protective immunity to an intracellular pathogen, Francisella tularensis strain LVS. JImmunol 1997, 158:3277-3284.
4. Elkins K.L., Rhinehart-Jones T.R., Stibitz S., Conover J.S., Klinman D.M. Bacterial DNA containing CpG motifs stimulates lymphocyte-dependent protection of mice against lethal infection with intracellular bacteria. JImmunol 1999, 162:2291-2298.
5. Dreisbach V.C., Cowley S., Elkins K.L. Purified lipopolysaccharide from Francisella tularensis live vaccine strain (LVS) induces protective immunity against LVS infection that requires B cells and gamma interferon. Infect Immun 2000, 68:1988-1996.
6. Elkins K.L., Cowley S.C., Bosio C.M. Innate and adaptive immunity to Francisella. Ann N Y Acad Sci 2007, 1105:284-324.
7. Cowley S.C., Elkins K.L. Immunity to Francisella. Front Microbiol 2011, 2:26.
8. Crane D.D., Scott D.P., Bosio C.M. Generation of a convalescent model of virulent Francisella tularensis infection for assessment of host requirements for survival of tularemia. PLoS ONE 2012, 7:e33349.
9. Vascotto F., Le Roux D., Lankar D., Faure-André G., Vargas P., Guermonprez P., et al. Antigen presentation by B lymphocytes: how receptor signaling directs membrane trafficking. Curr Opin Immunol 2007, 19:93-98.
10. Stenmark S., Lindgren H., Tärnvik A., Sjöstedt A. Specific antibodies contribute to the host protection against strains of Francisella tularensis subspecies holarctica. Microb Pathog 2003, 35:73-80.
11. Lavine C.L., Clinton S.R., Angelova-Fischer I., Marion T.N., Bina X.R., Bina J.E., et al. Immunization with heat-killed Francisella tularensis LVS elicits protective antibody-mediated immunity. Eur J Immunol 2007, 37:3007-3020.
12. Lu Z., Roche M.I., Hui J.H., Unal B., Felgner P.L., Gulati S., et al. Generation and characterization of hybridoma antibodies for immunotherapy of tularemia. Immunol Lett 2007, 112:92-103.
13. Savitt A.G., Mena-Taboada P., Monsalve G., Benach J.L. Francisella tularensis infection-derived monoclonal antibodies provide detection, protection, and therapy. Clin Vaccine Immunol 2009, 16:414-422.
14. Iglesias B.V., Bitsaktsis C., Pham G., Drake J.R., Hazlett K.R.O., Porter K., et al. Multiple mechanisms mediate enhanced immunity generated by mAb-inactivated F.tularensis immunogen. Immunol Cell Biol 2013, 91:139-148.
15. Kirimanjeswara G.S., Golden J.M., Bakshi C.S., Metzger D.W. Prophylactic and therapeutic use of antibodies for protection against respiratory infection with Francisella tularensis. JImmunol 2007, 179:532-539.
16. Furuya Y., Kirimanjeswara G.S., Roberts S., Metzger D.W. Increased susceptibility of IgA-deficient mice to pulmonary Francisella tularensis live vaccine strain infection. Infect Immun 2013, 81:3434-3441.
17. Baron S.D., Singh R., Metzger D.W. Inactivated Francisella tularensis live vaccinestrain protects against respiratory tularemia by intranasal vaccinationin an immunoglobulin A-dependent fashion. Infect Immun 2007, 75:2152-2162.
18. Jones C.L., Napier B.A., Sampson T.R., Llewellyn A.C., Schroeder M.R., Weiss D.S. Subversion of host recognition and defense systems by Francisella spp. Microbiol Mol Biol Rev 2012, 76:383-404.
19. Wilson J.E., Katkere B., Drake J.R. Francisella tularensis induces ubiquitin-dependent major histocompatibility complex class II degradation in activated macrophages. Infect Immun 2009, 77:4953-4965.
20. Hunt D., Wilson J.E., Weih K.A., Ishido S., Harton J.A., Roche P.A., et al. Francisella tularensis elicits IL-10 via a PGE[U+2082]-inducible factor, to drive macrophage MARCH1 expression and class II down-regulation. PLoS ONE 2012, 7:e37330.
21. Bosio C.M., Dow S.W. Francisella tularensis induces aberrant activation of pulmonary dendritic cells. JImmunol 2005, 175:6792-6801.
22. David J., Gates A.J., Griffiths G.D., Lukaszewski R.A. Gene expression following low dose inhalational Francisella tularensis (SchuS4) exposure in Balb/c mice and the potential role of the epithelium and cell adhesion. Microbes Infect 2012, 14:369-379.
23. Bratescu A., Mayer E.P., Teodorescu M. Binding of bacteria from the genus Brucella to human B lymphocytes. Infect Immun 1981, 31:816-821.
24. Teodorescu M., Mayer E.P. Binding of bacteria to lymphocyte subpopulations. Adv Immunol 1982, 33:307-351.
25. Lombardi G., Del Gallo F., Vismara D., Piccolella E., Colizzi V. Immunology of tuberculosis: new directions in research. Ric Clin Lab 1987, 17:1-15.
26. Bard J.A., Levitt D. Binding, ingestion, and multiplication of Chlamydia trachomatis (L2 serovar) in human leukocyte cell lines. Infect Immun 1985, 50:935-937.
27. Bard J., Levitt D. Chlamydia trachomatis stimulates human peripheral blood B lymphocytes to proliferate and secrete polyclonal immunoglobulins invitro. Infect Immun 1984, 43:84-92.
28. Fitzpatrick D.R., Wie J., Webb D., Bonfiglioli R., Gardner I.D., Mathews J.D., et al. Preferential binding of Chlamydia trachomatis to subsets of human lymphocytes and induction of interleukin-6 and interferon-gamma. Immunol Cell Biol 1991, 69(Pt 5):337-348.
29. Rosales-Reyes R., Pérez-López A., Sánchez-Gómez C., Hernández-Mote R.R., Castro-Eguiluz D., Ortiz-Navarrete V., et al. Salmonella infects B cells by macropinocytosis and formation of spacious phagosomes but does not induce pyroptosis in favor of its survival. Microb Pathog 2012, 52:367-374.
30. García-Pérez B.E., De la Cruz-López J.J., Castañeda-Sánchez J.I., Muñóz-Duarte A.R., Hernández-Pérez A.D., Villegas-Castrejón H., et al. Macropinocytosis is responsible for the uptake of pathogenic and non-pathogenic mycobacteria by B lymphocytes (Raji cells). BMC Microbiol 2012, 12:246.
31. Le Roux D., Niedergang F. New insights into antigen encounter by B cells. Immunobiology 2012, 217:1285-1291.
32. Krocova Z., Härtlova A., Souckova D., Zivna L., Kroca M., Rudolf E., et al. Interaction of B cells with intracellular pathogen Francisella tularensis. Microb Pathog 2008, 45:79-85.
33. Zivna L., Krocova Z., Härtlova A., Kubelkova K., Zakova J., Rudolf E., et al. Activation of B cell apoptotic pathways in the course of Francisella tularensis infection. Microb Pathog 2010, 49:226-236.
34. Fortier A.H., Slayter M.V., Ziemba R., Meltzer M.S., Nacy C.A. Live vaccine strain of Francisella tularensis: infection and immunity in mice. Infect Immun 1991, 59:2922-2928.
35. Baumgarth N. Innate-like B cells and their rules of engagement. Adv Exp Med Biol 2013, 785:57-66.
36. Cole L.E., Yang Y., Elkins K.L., Fernandez E.T., Qureshi N., Shlomchik M.J., et al. Antigen-specific B-1a antibodies induced by Francisella tularensis LPS provide long-term protection against F.tularensis LVS challenge. Proc Natl Acad Sci USA 2009, 106:4343-4348.
37. Crane D.D., Griffin A.J., Wehrly T.D., Bosio C.M. B1a cells enhance susceptibility to infection with virulent Francisella tularensis via modulation of NK/NKT cell responses. JImmunol 2013, 190:2756-2766.
38. Harris D.P., Haynes L., Sayles P.C., Duso D.K., Eaton S.M., Lepak N.M., et al. Reciprocal regulation of polarized cytokine production by effector B and T cells. Nat Immunol 2000, 1:475-482.
39. Mizoguchi A., Bhan A.K. Acase for regulatory B cells. JImmunol 2006, 176:705-710.
40. Aggarwal S., Ghilardi N., Xie M.-H., De Sauvage F.J., Gurney A.L. Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17. JBiol Chem 2003, 278:1910-1914.
41. Awasthi A., Kuchroo V.K. Th17 cells: from precursors to players in inflammation and infection. Int Immunol 2009, 21:489-498.
42. Mangan P.R., Harrington L.E., O'Quinn D.B., Helms W.S., Bullard D.C., Elson C.O., et al. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 2006, 441:231-234.
43. Bettelli E., Carrier Y., Gao W., Korn T., Strom T.B., Oukka M., et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006, 441:235-238.
44. Harris D.P., Goodrich S., Mohrs K., Mohrs M., Lund F.E. Cutting edge: the development of IL-4-producing B cells (B effector 2 cells) is controlled by IL-4, IL-4 receptor alpha, and Th2 cells. JImmunol 2005, 175:7103-7107.
45. Harris D.P., Goodrich S., Gerth A.J., Peng S.L., Lund F.E. Regulation of IFN-gamma production by B effector 1 cells: essential roles for T-bet and the IFN-gamma receptor. JImmunol 2005, 174:6781-6790.
46. Barr T.A., Brown S., Ryan G., Zhao J., Gray D. TLR-mediated stimulation of APC: distinct cytokine responses of B cells and dendritic cells. Eur J Immunol 2007, 37:3040-3053.
47. Lund F.E. Cytokine-producing B lymphocytes-key regulators of immunity. Curr Opin Immunol 2008, 20:332-338.
48. Shen H., Harris G., Chen W., Sjostedt A., Ryden P., Conlan W. Molecular immune responses to aerosol challenge with Francisella tularensis in mice inoculated with live vaccine candidates of varying efficacy. PLoS ONE 2010, 5:e13349.
49. Paranavitana C., Zelazowska E., DaSilva L., Pittman P.R., Nikolich M. Th17 cytokines in recall responses against Francisella tularensis in humans. JInterferon Cytokine Res 2010, 30:471-476.
50. Eneslätt K., Normark M., Björk R., Rietz C., Zingmark C., Wolfraim L.A., et al. Signatures of T cells as correlates of immunity to Francisella tularensis. PLoS ONE 2012, 7:e32367.
51. De Pascalis R., Chou A.Y., Bosio C.M., Huang C.-Y., Follmann D.A., Elkins K.L. Development of functional and molecular correlates of vaccine-induced protection for a model intracellular pathogen, F.tularensis LVS. PLoS Pathog 2012, 8:e1002494.
52. Kurtz S.L., Foreman O., Bosio C.M., Anver M.R., Elkins K.L. Interleukin-6 is essential for primary resistance to Francisella tularensis live vaccine strain infection. Infect Immun 2013, 81:585-597.
53. Lin Y., Ritchea S., Logar A., Slight S., Messmer M., Rangel-Moreno J., et al. Interleukin-17 is required for T helper 1 cell immunity and host resistance to the intracellular pathogen Francisella tularensis. Immunity 2009, 31:799-810.
54. Slight S.R., Monin L., Gopal R., Avery L., Davis M., Cleveland H., et al. IL-10 restrains IL-17 to limit lung pathology characteristics following pulmonary infection with Francisella tularensis live vaccine strain. Am J Pathol 2013, 183:1397-1404.
55. Vega-Ramos J., Alari-Pahissa E., Valle J.D., Carrasco-Marín E., Esplugues E., Borràs M., et al. CD69 limits early inflammatory diseases associated with immune response to Listeria monocytogenes infection. Immunol Cell Biol 2010, 88:707-715.