B1a cells enhance susceptibility to infection with virulent francisella tularensis via modulation of NK/NKT cell responses

Journal of Immunology

Volumn 190, Issue 6, 2013, Pages 2756-2766

  Crane, Deborah D ^a   Griffin, Amanda J ^a   Wehrly, Tara D ^a   Bosio, Catharine M ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12;

ADOPTIVE TRANSFER; ANIMAL CELL; ANTIBODY RESPONSE; ARTICLE; B LYMPHOCYTE; BACTERIAL STRAIN; CONTROLLED STUDY; FRANCISELLA TULARENSIS; IMMUNE RESPONSE; INFECTION SENSITIVITY; LUNG ALVEOLUS CELL; LUNG ALVEOLUS MACROPHAGE; LUNG INFECTION; MACROPHAGE; MODULATION; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; SPLEEN CELL; TH1 CELL; WILD TYPE;

ANIMALS; ANTIBODIES, BACTERIAL; B-LYMPHOCYTE SUBSETS; CELL COMMUNICATION; CELLS, CULTURED; EXUDATES AND TRANSUDATES; FRANCISELLA TULARENSIS; GENETIC PREDISPOSITION TO DISEASE; KILLER CELLS, NATURAL; MICE; MICE, INBRED CBA; MICE, MUTANT STRAINS; NATURAL KILLER T-CELLS; PERITONEUM; PROTEIN-TYROSINE KINASES; SURVIVAL ANALYSIS; TH1 CELLS; TULAREMIA; VIRULENCE;

EID: 84874845541     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1202697     Document Type: Article

References (63)

1. Swanson, C. L., R. Pelanda, and R. M. Torres. 2013. Division of labor during primary humoral immunity. Immunol. Res. 55: 277-286
2. Lund, F. E., and T. D. Randall. 2010. Effector and regulatory B cells: modulators of CD4(+) T cell immunity. Nat. Rev. Immunol. 10: 236-247
3. Clemens, D. L., B. Y. Lee, and M. A. Horwitz. 2009. Francisella tularensis phagosomal escape does not require acidification of the phagosome. Infect. Immun. 77: 1757-1773
4. Fortier, A. H., D. A. Leiby, R. B. Narayanan, E. Asafoadjei, R. M. Crawford, C. A. Nacy, and M. S. Meltzer. 1995. Growth of Francisella tularensis LVS in macrophages: the acidic intracellular compartment provides essential iron required for growth. Infect. Immun. 63: 1478-1483
5. McCRUMB, F. R., Jr., M. J. Snyder, and T. E. Woodward. 1957. Studies on human infection with Pasteurella tularensis; comparison of streptomycin and chloramphenicol in the prophylaxis of clinical disease. Trans. Assoc. Am. Physicians 70: 74-79, discussion 79-80
6. Risi, G. F., and D. J. Pombo. 1995. Relapse of tularemia after aminoglycoside therapy: case report and discussion of therapeutic options. Clin. Infect. Dis. 20: 174-175
7. Harris, S. 1992. Japanese biological warfare research on humans: a case study of microbiology and ethics. Ann. N. Y. Acad. Sci. 666: 21-52
8. Elkins, K. L., A. T. MacIntyre, and T. R. Rhinehart-Jones. 1998. Nonspecific early protective immunity in Francisella and Listeria infections can be dependent on lymphocytes. Infect. Immun. 66: 3467-3469
9. Crane, D. D., D. P. Scott, and C. M. Bosio. 2012. Generation of a convalescent model of virulent Francisella tularensis infection for assessment of host requirements for survival of tularemia. PLoS ONE 7: e33349
10. Drabick, J. J., R. B. Narayanan, J. C. Williams, J. W. Leduc, and C. A. Nacy. 1994. Passive protection of mice against lethal Francisella tularensis (live tularemia vaccine strain) infection by the sera of human recipients of the live tularemia vaccine. Am. J. Med. Sci. 308: 83-87
11. Hickey, A. J., K. R. Hazlett, G. S. Kirimanjeswara, and D. W. Metzger. 2011. Identification of Francisella tularensis outer membrane protein A (FopA) as a protective antigen for tularemia. Vaccine 29: 6941-6947
12. Kirimanjeswara, G. S., J. M. Golden, C. S. Bakshi, and D. W. Metzger. 2007. Prophylactic and therapeutic use of antibodies for protection against respiratory infection with Francisella tularensis. J. Immunol. 179: 532-539
13. Lavine, C. L., S. R. Clinton, I. Angelova-Fischer, T. N. Marion, X. R. Bina, J. E. Bina, M. A. Whitt, and M. A. Miller. 2007. Immunization with heat-killed Francisella tularensis LVS elicits protective antibody-mediated immunity. Eur. J. Immunol. 37: 3007-3020
14. Mara-Koosham, G., J. A. Hutt, C. R. Lyons, and T. H. Wu. 2011. Antibodies contribute to effective vaccination against respiratory infection by type A Francisella tularensis strains. Infect. Immun. 79: 1770-1778
15. Pammit, M. A., E. K. Raulie, C. M. Lauriano, K. E. Klose, and B. P. Arulanandam. 2006. Intranasal vaccination with a defined attenuated Francisella novicida strain induces gamma interferon-dependent antibodymediated protection against tularemia. Infect. Immun. 74: 2063-2071
16. Savitt, A. G., P. Mena-Taboada, G. Monsalve, and J. L. Benach. 2009. Francisella tularensis infection-derived monoclonal antibodies provide detection, protection, and therapy. Clin. Vaccine Immunol. 16: 414-422
17. Stenmark, S., H. Lindgren, A. Tärnvik, and A. Sjöstedt. 2003. Specific antibodies contribute to the host protection against strains of Francisella tularensis subspecies holarctica. Microb. Pathog. 35: 73-80
18. Lu, Z., G. Madico, M. I. Roche, Q. Wang, J. H. Hui, H. M. Perkins, J. Zaia, C. E. Costello, and J. Sharon. 2012. Protective B-cell epitopes of Francisella tularensis O-polysaccharide in a mouse model of respiratory tularaemia. Immunology 136: 352-360
19. Lu, Z., M. I. Roche, J. H. Hui, B. Unal, P. L. Felgner, S. Gulati, G. Madico, and J. Sharon. 2007. Generation and characterization of hybridoma antibodies for immunotherapy of tularemia. Immunol. Lett. 112: 92-103
20. Foshay, L. 1940. Tularemia: A summary of certain aspects of the disease including methods for early diagnosis and the results of serum treatment in 600 patients. Medicine 19: 1-83
21. Cole, L. E., Y. Yang, K. L. Elkins, E. T. Fernandez, N. Qureshi, M. J. Shlomchik, L. A. Herzenberg, L. A. Herzenberg, and S. N. Vogel. 2009. Antigen-specific B- 1a antibodies induced by Francisella tularensis LPS provide long-term protection against F. tularensis LVS challenge. Proc. Natl. Acad. Sci. USA 106: 4343-4348
22. Bosio, C. M., and K. L. Elkins. 2001. Susceptibility to secondary Francisella tularensis live vaccine strain infection in B-cell-deficient mice is associated with neutrophilia but not with defects in specific T-cell-mediated immunity. Infect. Immun. 69: 194-203
23. Elkins, K. L., T. R. Rhinehart-Jones, S. J. Culkin, D. Yee, and R. K. Winegar. 1996. Minimal requirements for murine resistance to infection with Francisella tularensis LVS. Infect. Immun. 64: 3288-3293
24. Bosio, C. M., H. Bielefeldt-Ohmann, and J. T. Belisle. 2007. Active suppression of the pulmonary immune response by Francisella tularensis Schu4. J. Immunol. 178: 4538-4547
25. Guth, A. M., W. J. Janssen, C. M. Bosio, E. C. Crouch, P. M. Henson, and S. W. Dow. 2009. Lung environment determines unique phenotype of alveolar macrophages. Am. J. Physiol. Lung Cell. Mol. Physiol. 296: L936-L946
26. Warfield, K. L., J. G. Perkins, D. L. Swenson, E. M. Deal, C. M. Bosio, M. J. Aman, W. M. Yokoyama, H. A. Young, and S. Bavari. 2004. Role of natural killer cells in innate protection against lethal ebola virus infection. J. Exp. Med. 200: 169-179
27. Chase, J. C., and C. M. Bosio. 2010. The presence of CD14 overcomes evasion of innate immune responses by virulent Francisella tularensis in human dendritic cells in vitro and pulmonary cells in vivo. Infect. Immun. 78: 154-167
28. Anderson, R. V., D. D. Crane, and C. M. Bosio. 2010. Long lived protection against pneumonic tularemia is correlated with cellular immunity in peripheral, not pulmonary, organs. Vaccine 28: 6562-6572
29. Perlmutter, R. M., M. Nahm, K. E. Stein, J. Slack, I. Zitron, W. E. Paul, and J. M. Davie. 1979. Immunoglobulin subclass-specific immunodeficiency in mice with an X-linked B-lymphocyte defect. J. Exp. Med. 149: 993-998
30. Pinschewer, D. D., A. F. Ochsenbein, A. B. Satterthwaite, O. N. Witte, H. Hengartner, and R. M. Zinkernagel. 1999. A Btk transgene restores the antiviral TI-2 antibody responses of xid mice in a dose-dependent fashion. Eur. J. Immunol. 29: 2981-2987
31. Reale, M. A., C. A. Bona, and J. L. Schulman. 1985. Isotype profiles of antiinfluenza antibodies in mice bearing the xid defect. J. Virol. 53: 425-429
32. de Weers, M., M. C. Verschuren, M. E. Kraakman, R. G. Mensink, R. K. Schuurman, J. J. van Dongen, and R. W. Hendriks. 1993. The Bruton's tyrosine kinase gene is expressed throughout B cell differentiation, from early precursor B cell stages preceding immunoglobulin gene rearrangement up to mature B cell stages. Eur. J. Immunol. 23: 3109-3114
33. Honda, F., H. Kano, H. Kanegane, S. Nonoyama, E. S. Kim, S. K. Lee, M. Takagi, S. Mizutani, and T. Morio. 2012. The kinase Btk negatively regulates the production of reactive oxygen species and stimulation-induced apoptosis in human neutrophils. Nat. Immunol. 13: 369-378
34. Jefferies, C. A., S. Doyle, C. Brunner, A. Dunne, E. Brint, C. Wietek, E. Walch, T. Wirth, and L. A. O'Neill. 2003. Bruton's tyrosine kinase is a Toll/interleukin- 1 receptor domain-binding protein that participates in nuclear factor kappaB activation by Toll-like receptor 4. J. Biol. Chem. 278: 26258-26264
35. Mangla, A., A. Khare, V. Vineeth, N. N. Panday, A. Mukhopadhyay B. Ravindran, V. Bal, A. George, and S. Rath. 2004. Pleiotropic consequences of Bruton tyrosine kinase deficiency in myeloid lineages lead to poor inflammatory responses. Blood 104: 1191-1197
36. Crane, D. D., S. L. Warner, and C. M. Bosio. 2009. A novel role for plasminmediated degradation of opsonizing antibody in the evasion of host immunity by virulent, but not attenuated, Francisella tularensis. J. Immunol. 183: 4593-4600
37. Ireland, R., N. Olivares-Zavaleta, J. M. Warawa, F. C. Gherardini, C. Jarrett, B. J. Hinnebusch, J. T. Belisle, J. Fairman, and C. M. Bosio. 2010. Effective, broad spectrum control of virulent bacterial infections using cationic DNA liposome complexes combined with bacterial antigens. PLoS Pathog. 6: e1000921
38. Telepnev, M., I. Golovliov, T. Grundström, A. Tärnvik, and A. Sjöstedt. 2003. Francisella tularensis inhibits Toll-like receptor-mediated activation of intracellular signalling and secretion of TNF-alpha and IL-1 from murine macrophages. Cell. Microbiol. 5: 41-51
39. Butchar, J. P., T. J. Cremer, C. D. Clay, M. A. Gavrilin, M. D. Wewers, C. B. Marsh, L. S. Schlesinger, and S. Tridandapani. 2008. Microarray analysis of human monocytes infected with Francisella tularensis identifies new targets of host response subversion. PLoS ONE 3: e2924
40. Parsa, K. V., L. P. Ganesan, M. V. Rajaram, M. A. Gavrilin, A. Balagopal, N. P. Mohapatra, M. D. Wewers, L. S. Schlesinger, J. S. Gunn, and S. Tridandapani. 2006. Macrophage pro-inflammatory response to Francisella novicida infection is regulated by SHIP. PLoS Pathog. 2: e71
41. Sjöstedt, A., J. W. Conlan, and R. J. North. 1994. Neutrophils are critical for host defense against primary infection with the facultative intracellular bacterium Francisella tularensis in mice and participate in defense against reinfection. Infect. Immun. 62: 2779-2783
42. O'Garra, A., R. Chang, N. Go, R. Hastings, G. Haughton, and M. Howard. 1992. Ly-1 B (B-1) cells are the main source of B cell-derived interleukin 10. Eur. J. Immunol. 22: 711-717
43. Saraiva, M., and A. O'Garra. 2010. The regulation of IL-10 production by immune cells. Nat. Rev. Immunol. 10: 170-181
44. Forrester, L. M., J. D. Ansell, and H. S. Micklem. 1987. Development of B lymphocytes in mice heterozygous for the X-linked immunodeficiency (xid) mutation. xid inhibits development of all splenic and lymph node B cells at a stage subsequent to their initial formation in bone marrow. J. Exp. Med. 165: 949-958
45. Duckett, N. S., S. Olmos, D. M. Durrant, and D. W. Metzger. 2005. Intranasal interleukin-12 treatment for protection against respiratory infection with the Francisella tularensis live vaccine strain. Infect. Immun. 73: 2306-2311
46. Al-Qaoud, K. M., B. Fleischer, and A. Hoerauf. 1998. The Xid defect imparts susceptibility to experimental murine filariosis-association with a lack of antibody and IL-10 production by B cells in response to phosphorylcholine. Int. Immunol. 10: 17-25
47. Eguchi, M., and Y. Kikuchi. 2010. Binding of Salmonella-specific antibody facilitates specific T cell responses via augmentation of bacterial uptake and induction of apoptosis in macrophages. J. Infect. Dis. 201: 62-70
48. Kadioglu, A., and P. W. Andrew. 2005. Susceptibility and resistance to pneumococcal disease in mice. Brief. Funct. Genomics Proteomics 4: 241-247
49. Lim, P. L., W. F. Choy, S. T. Chan, D. T. Leung, and S. S. Ng. 1994. Transgeneencoded antiphosphorylcholine (T15+) antibodies protect CBA/N (xid) mice against infection with Streptococcus pneumoniae but not Trichinella spiralis. Infect. Immun. 62: 1658-1661
50. McSorley, S. J., and M. K. Jenkins. 2000. Antibody is required for protection against virulent but not attenuated Salmonella enterica serovar typhimurium. Infect. Immun. 68: 3344-3348
51. Hayakawa, K., R. R. Hardy, and L. A. Herzenberg. 1986. Peritoneal Ly-1 B cells: genetic control, autoantibody production, increased lambda light chain expression. Eur. J. Immunol. 16: 450-456
52. Martin, F., A. M. Oliver, and J. F. Kearney. 2001. Marginal zone and B1 B cells unite in the early response against T-independent blood-borne particulate antigens. Immunity 14: 617-629
53. Schwartz, J. T., J. H. Barker, M. E. Long, J. Kaufman, J. McCracken, and L. A. Allen. 2012. Natural IgM mediates complement-dependent uptake of Francisella tularensis by human neutrophils via complement receptors 1 and 3 in nonimmune serum. J. Immunol. 189: 3064-3077
54. Conlan, J. W., R. KuoLee, H. Shen, and A. Webb. 2002. Different host defences are required to protect mice from primary systemic vs pulmonary infection with the facultative intracellular bacterial pathogen, Francisella tularensis LVS. Microb. Pathog. 32: 127-134
55. López, M. C., N. S. Duckett, S. D. Baron, and D. W. Metzger. 2004. Early activation of NK cells after lung infection with the intracellular bacterium, Francisella tularensis LVS. Cell. Immunol. 232: 75-85
56. Hoerauf, A., W. Solbach, M. Lohoff, and M. Röllinghoff. 1994. The Xid defect determines an improved clinical course of murine leishmaniasis in susceptible mice. Int. Immunol. 6: 1117-1124
57. Santos-Lima, E. C., R. Vasconcellos, B. Reina-San-Martín, C. Fesel, A. Cordeiro-Da-Silva, A. Berneman, A. Cosson, A. Coutinho, and P. Minoprio. 2001. Significant association between the skewed natural antibody repertoire of Xid mice and resistance to Trypanosoma cruzi infection. Eur. J. Immunol. 31: 634-645
58. Zhao, Y. X., A. Abdelnour, R. Holmdahl, and A. Tarkowski. 1995. Mice with the xid B cell defect are less susceptible to developing Staphylococcus aureus-induced arthritis. J. Immunol. 155: 2067-2076
59. Andersson, H., B. Hartmanová, R. Kuolee, P. Rydén, W. Conlan, W. Chen, and A. Sjöstedt. 2006. Transcriptional profiling of host responses in mouse lungs following aerosol infection with type A Francisella tularensis. J. Med. Microbiol. 55: 263-271
60. Conlan, J. W., X. Zhao, G. Harris, H. Shen, M. Bolanowski, C. Rietz, A. Sjostedt, and W. Chen. 2008. Molecular immunology of experimental primary tularemia in mice infected by respiratory or intradermal routes with type A Francisella tularensis. Mol. Immunol. 45: 2962-2969
61. Mares, C. A., S. S. Ojeda, E. G. Morris, Q. Li, and J. M. Teale. 2008. Initial delay in the immune response to Francisella tularensis is followed by hypercytokinemia characteristic of severe sepsis and correlating with upregulation and release of damage-associated molecular patterns. Infect. Immun. 76: 3001-3010
62. Bauler, T. J., J. C. Chase, and C. M. Bosio. 2011. IFN-β mediates suppression of IL-12p40 in human dendritic cells following infection with virulent Francisella tularensis. J. Immunol. 187: 1845-1855
63. Chase, J. C., J. Celli, and C. M. Bosio. 2009. Direct and indirect impairment of human dendritic cell function by virulent Francisella tularensis Schu S4. Infect. Immun. 77: 180-195