Production of Anti-LPS IgM by B1a B Cells Depends on IL-1β and Is Protective against Lung Infection with Francisella tularensis LVS

PLoS Pathogens

Volumn 11, Issue 3, 2015, Pages 1-20

  del Barrio, Laura ^a   Sahoo, Manoranjan ^a   Lantier, Louis ^a   Reynolds, Joseph M ^a   Ceballos Olvera, Ivonne ^a   Re, Fabio ^a  

^a ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; IMMUNOGLOBULIN M; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 18; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; TOLL LIKE RECEPTOR 2; BACTERIUM ANTIBODY; LIPOPOLYSACCHARIDE;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY TITER; ANTIGEN ANTIBODY REACTION; ARTICLE; BACTERIAL GROWTH; BACTERIAL LOAD; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; LUNG INFECTION; LUNG LAVAGE; MOUSE; NONHUMAN; PASSIVE IMMUNIZATION; PHAGOCYTOSIS; TULAREMIA; WESTERN BLOTTING; ANIMAL; B LYMPHOCYTE; C57BL MOUSE; DISEASE MODEL; IMMUNOLOGY; KNOCKOUT MOUSE; RESPIRATORY TRACT INFECTION;

BACTERIA (MICROORGANISMS); FRANCISELLA TULARENSIS; MUS; NEGIBACTERIA;

ANIMALS; ANTIBODIES, BACTERIAL; B-LYMPHOCYTE SUBSETS; BLOTTING, WESTERN; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IMMUNOGLOBULIN M; INTERLEUKIN-1BETA; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RESPIRATORY TRACT INFECTIONS; TULAREMIA;

EID: 84926507416     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004706     Document Type: Article

References (61)

1. McLendon MK, Apicella MA, Allen LA, (2006) Francisella tularensis: taxonomy, genetics, and Immunopathogenesis of a potential agent of biowarfare. Annu Rev Microbiol 60: 167–185. 16704343
2. Steiner DJ, Furuya Y, Metzger DW, (2014) Host-pathogen interactions and immune evasion strategies in Francisella tularensis pathogenicity. Infect Drug Resist 7: 239–251. doi: 10.2147/IDR.S53700 25258544
3. Elkins KL, Cowley SC, Bosio CM, (2007) Innate and adaptive immunity to Francisella. Ann N Y Acad Sci 1105: 284–324. 17468235
4. Jones CL, Napier BA, Sampson TR, Llewellyn AC, Schroeder MR, et al. (2012) Subversion of host recognition and defense systems by Francisella spp. Microbiol Mol Biol Rev 76: 383–404. doi: 10.1128/MMBR.05027-11 22688817
5. Cole LE, Elkins KL, Michalek SM, Qureshi N, Eaton LJ, et al. (2006) Immunologic consequences of Francisella tularensis live vaccine strain infection: role of the innate immune response in infection and immunity. J Immunol 176: 6888–6899. 16709849
6. Hajjar AM, Harvey MD, Shaffer SA, Goodlett DR, Sjostedt A, et al. (2006) Lack of in vitro and in vivo recognition of Francisella tularensis subspecies lipopolysaccharide by Toll-like receptors. Infect Immun 74: 6730–6738. 16982824
7. Barker JH, Weiss J, Apicella MA, Nauseef WM, (2006) Basis for the failure of Francisella tularensis lipopolysaccharide to prime human polymorphonuclear leukocytes. Infect Immun 74: 3277–3284. 16714555
8. Ancuta P, Pedron T, Girard R, Sandstrom G, Chaby R, (1996) Inability of the Francisella tularensis lipopolysaccharide to mimic or to antagonize the induction of cell activation by endotoxins. Infect Immun 64: 2041–2046. 8675305
9. Dreisbach VC, Cowley S, Elkins KL, (2000) Purified lipopolysaccharide from Francisella tularensis live vaccine strain (LVS) induces protective immunity against LVS infection that requires B cells and gamma interferon. Infect Immun 68: 1988–1996. 10722593
10. Katz J, Zhang P, Martin M, Vogel SN, Michalek SM, (2006) Toll-like receptor 2 is required for inflammatory responses to Francisella tularensis LVS. Infect Immun 74: 2809–2816. 16622218
11. Malik M, Bakshi CS, Sahay B, Shah A, Lotz SA, et al. (2006) Toll-like receptor 2 is required for control of pulmonary infection with Francisella tularensis. Infect Immun 74: 3657–3662. 16714598
12. Li H, Nookala S, Bina XR, Bina JE, Re F, (2006) Innate immune response to Francisella tularensis is mediated by TLR2 and caspase-1 activation. J Leukoc Biol 80: 766–773. 16895974
13. Thakran S, Li H, Lavine CL, Miller MA, Bina JE, et al. (2008) Identification of Francisella tularensis lipoproteins that stimulate the toll-like receptor (TLR) 2/TLR1 heterodimer. J Biol Chem 283: 3751–3760. 18079113
14. Henry T, Monack DM, (2007) Activation of the inflammasome upon Francisella tularensis infection: interplay of innate immune pathways and virulence factors. Cell Microbiol 9: 2543–2551. 17662071
15. Cunha LD, Zamboni DS, (2013) Subversion of inflammasome activation and pyroptosis by pathogenic bacteria. Front Cell Infect Microbiol 3: 76. doi: 10.3389/fcimb.2013.00076 24324933
16. Atianand MK, Duffy EB, Shah A, Kar S, Malik M, et al. (2011) Francisella tularensis reveals a disparity between human and mouse NLRP3 inflammasome activation. J Biol Chem 286: 39033–39042. doi: 10.1074/jbc.M111.244079 21930705
17. Dinarello CA, (2009) Immunological and inflammatory functions of the interleukin-1 family. Annu Rev Immunol 27: 519–550. doi: 10.1146/annurev.immunol.021908.132612 19302047
18. Kingry LC, Petersen JM, (2014) Comparative review of Francisella tularensis and Francisella novicida. Front Cell Infect Microbiol 4: 35. doi: 10.3389/fcimb.2014.00035 24660164
19. Fortier AH, Slayter MV, Ziemba R, Meltzer MS, Nacy CA, (1991) Live vaccine strain of Francisella tularensis: infection and immunity in mice. Infect Immun 59: 2922–2928. 1879918
20. Elkins KL, Winegar RK, Nacy CA, Fortier AH, (1992) Introduction of Francisella tularensis at skin sites induces resistance to infection and generation of protective immunity. Microb Pathog 13: 417–421. 1297917
21. Mariathasan S, Weiss DS, Dixit VM, Monack DM, (2005) Innate immunity against Francisella tularensis is dependent on the ASC/caspase-1 axis. J Exp Med 202: 1043–1049. 16230474
22. Collazo CM, Sher A, Meierovics AI, Elkins KL, (2006) Myeloid differentiation factor-88 (MyD88) is essential for control of primary in vivo Francisella tularensis LVS infection, but not for control of intra-macrophage bacterial replication. Microbes Infect 8: 779–790. 16513388
23. Huang MT, Mortensen BL, Taxman DJ, Craven RR, Taft-Benz S, et al. (2010) Deletion of ripA alleviates suppression of the inflammasome and MAPK by Francisella tularensis. J Immunol 185: 5476–5485. doi: 10.4049/jimmunol.1002154 20921527
24. Ulland TK, Buchan BW, Ketterer MR, Fernandes-Alnemri T, Meyerholz DK, et al. (2010) Cutting edge: mutation of Francisella tularensis mviN leads to increased macrophage absent in melanoma 2 inflammasome activation and a loss of virulence. J Immunol 185: 2670–2674. doi: 10.4049/jimmunol.1001610 20679532
25. Jayakar HR, Parvathareddy J, Fitzpatrick EA, Bina XR, Bina JE, et al. (2011) A galU mutant of Francisella tularensis is attenuated for virulence in a murine pulmonary model of tularemia. BMC Microbiol 11: 179. doi: 10.1186/1471-2180-11-179 21819572
26. Peng K, Broz P, Jones J, Joubert LM, Monack D, (2011) Elevated AIM2-mediated pyroptosis triggered by hypercytotoxic Francisella mutant strains is attributed to increased intracellular bacteriolysis. Cell Microbiol 13: 1586–1600. doi: 10.1111/j.1462-5822.2011.01643.x 21883803
27. Ulland TK, Janowski AM, Buchan BW, Faron M, Cassel SL, et al. (2013) Francisella tularensis live vaccine strain folate metabolism and pseudouridine synthase gene mutants modulate macrophage caspase-1 activation. Infect Immun 81: 201–208. doi: 10.1128/IAI.00991-12 23115038
28. Puren AJ, Fantuzzi G, Gu Y, Su MS, Dinarello CA, (1998) Interleukin-18 (IFNgamma-inducing factor) induces IL-8 and IL-1beta via TNFalpha production from non-CD14+ human blood mononuclear cells. J Clin Invest 101: 711–721. 9449707
29. Okamura H, Tsutsi H, Komatsu T, Yutsudo M, Hakura A, et al. (1995) Cloning of a new cytokine that induces IFN-gamma production by T cells. Nature 378: 88–91. 7477296
30. Anthony LS, Ghadirian E, Nestel FP, Kongshavn PA, (1989) The requirement for gamma interferon in resistance of mice to experimental tularemia. Microb Pathog 7: 421–428. 2516219
31. Anthony LS, Morrissey PJ, Nano FE, (1992) Growth inhibition of Francisella tularensis live vaccine strain by IFN-gamma-activated macrophages is mediated by reactive nitrogen intermediates derived from L-arginine metabolism. J Immunol 148: 1829–1834. 1541823
32. Chen W, KuoLee R, Shen H, Conlan JW, (2004) Susceptibility of immunodeficient mice to aerosol and systemic infection with virulent strains of Francisella tularensis. Microb Pathog 36: 311–318. 15120157
33. Duckett NS, Olmos S, Durrant DM, Metzger DW, (2005) Intranasal interleukin-12 treatment for protection against respiratory infection with the Francisella tularensis live vaccine strain. Infect Immun 73: 2306–2311. 15784575
34. Horai R, Asano M, Sudo K, Kanuka H, Suzuki M, et al. (1998) Production of mice deficient in genes for interleukin (IL)-1alpha, IL-1beta, IL-1alpha/beta, and IL-1 receptor antagonist shows that IL-1beta is crucial in turpentine-induced fever development and glucocorticoid secretion. J Exp Med 187: 1463–1475. 9565638
35. Oguri S, Motegi K, Iwakura Y, Endo Y, (2002) Primary role of interleukin-1 alpha and interleukin-1 beta in lipopolysaccharide-induced hypoglycemia in mice. Clin Diagn Lab Immunol 9: 1307–1312. 12414765
36. Racine R, Winslow GM, (2009) IgM in microbial infections: taken for granted? Immunol Lett 125: 79–85. doi: 10.1016/j.imlet.2009.06.003 19539648
37. Ehrenstein MR, Notley CA, (2010) The importance of natural IgM: scavenger, protector and regulator. Nat Rev Immunol 10: 778–786. doi: 10.1038/nri2849 20948548
38. Sorokin VM, Pavlovich NV, Prozorova LA, (1996) Francisella tularensis resistance to bactericidal action of normal human serum. FEMS Immunol Med Microbiol 13: 249–252. 8861038
39. Ben Nasr A, Klimpel GR, (2008) Subversion of complement activation at the bacterial surface promotes serum resistance and opsonophagocytosis of Francisella tularensis. J Leukoc Biol 84: 77–85. doi: 10.1189/jlb.0807526 18430786
40. Schwartz JT, Barker JH, Long ME, Kaufman J, McCracken J, et al. (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. doi: 10.4049/jimmunol.1200816 22888138
41. Baumgarth N, (2011) The double life of a B-1 cell: self-reactivity selects for protective effector functions. Nat Rev Immunol 11: 34–46. doi: 10.1038/nri2901 21151033
42. Cerutti A, Cols M, Puga I, (2013) Marginal zone B cells: virtues of innate-like antibody-producing lymphocytes. Nat Rev Immunol 13: 118–132. doi: 10.1038/nri3383 23348416
43. Cole LE, Yang Y, Elkins KL, Fernandez ET, Qureshi N, et al. (2009) Antigen-specific B-1a antibodies induced by Francisella tularensis LPS provide long-term protection against F. tularensis LVS challenge. Proc Natl Acad Sci U S A 106: 4343–4348. doi: 10.1073/pnas.0813411106 19251656
44. Broz P, Monack DM, (2011) Molecular mechanisms of inflammasome activation during microbial infections. Immunol Rev 243: 174–190. doi: 10.1111/j.1600-065X.2011.01041.x 21884176
45. Cowley SC, Elkins KL, (2011) Immunity to Francisella. Front Microbiol 2: 26. doi: 10.3389/fmicb.2011.00026 21687418
46. Rhinehart-Jones TR, Fortier AH, Elkins KL, (1994) Transfer of immunity against lethal murine Francisella infection by specific antibody depends on host gamma interferon and T cells. Infect Immun 62: 3129–3137. 8039881
47. Fulop M, Mastroeni P, Green M, Titball RW, (2001) Role of antibody to lipopolysaccharide in protection against low- and high-virulence strains of Francisella tularensis. Vaccine 19: 4465–4472. 11483272
48. Kirimanjeswara GS, Golden JM, Bakshi CS, Metzger DW, (2007) Prophylactic and therapeutic use of antibodies for protection against respiratory infection with Francisella tularensis. J Immunol 179: 532–539. 17579074
49. Lavine CL, Clinton SR, Angelova-Fischer I, Marion TN, Bina XR, et al. (2007) Immunization with heat-killed Francisella tularensis LVS elicits protective antibody-mediated immunity. Eur J Immunol 37: 3007–3020. 17960662
50. Forestal CA, Malik M, Catlett SV, Savitt AG, Benach JL, et al. (2007) Francisella tularensis has a significant extracellular phase in infected mice. J Infect Dis 196: 134–137. 17538893
51. Clay CD, Soni S, Gunn JS, Schlesinger LS, (2008) Evasion of complement-mediated lysis and complement C3 deposition are regulated by Francisella tularensis lipopolysaccharide O antigen. J Immunol 181: 5568–5578. 18832715
52. Martin F, Oliver AM, Kearney JF, (2001) Marginal zone and B1 B cells unite in the early response against T-independent blood-borne particulate antigens. Immunity 14: 617–629. 11371363
53. Alugupalli KR, Gerstein RM, Chen J, Szomolanyi-Tsuda E, Woodland RT, et al. (2003) The resolution of relapsing fever borreliosis requires IgM and is concurrent with expansion of B1b lymphocytes. J Immunol 170: 3819–3827. 12646649
54. Haas KM, Poe JC, Steeber DA, Tedder TF, (2005) B-1a and B-1b cells exhibit distinct developmental requirements and have unique functional roles in innate and adaptive immunity to S. pneumoniae. Immunity 23: 7–18. 16039575
55. Cole LE, Mann BJ, Shirey KA, Richard K, Yang Y, et al. (2011) Role of TLR signaling in Francisella tularensis-LPS-induced, antibody-mediated protection against Francisella tularensis challenge. J Leukoc Biol 90: 787–797. doi: 10.1189/jlb.0111014 21750122
56. Crane DD, Griffin AJ, Wehrly TD, Bosio CM, (2013) B1a cells enhance susceptibility to infection with virulent Francisella tularensis via modulation of NK/NKT cell responses. J Immunol 190: 2756–2766. doi: 10.4049/jimmunol.1202697 23378429
57. Nakae S, Asano M, Horai R, Iwakura Y, (2001) Interleukin-1 beta, but not interleukin-1 alpha, is required for T-cell-dependent antibody production. Immunology 104: 402–409. 11899425
58. Schmitz N, Kurrer M, Bachmann MF, Kopf M, (2005) Interleukin-1 is responsible for acute lung immunopathology but increases survival of respiratory influenza virus infection. J Virol 79: 6441–6448. 15858027
59. Komai-Koma M, Gilchrist DS, McKenzie AN, Goodyear CS, Xu D, et al. (2011) IL-33 activates B1 cells and exacerbates contact sensitivity. J Immunol 186: 2584–2591. doi: 10.4049/jimmunol.1002103 21239718
60. Nurieva RI, Chung Y, Martinez GJ, Yang XO, Tanaka S, et al. (2009) Bcl6 mediates the development of T follicular helper cells. Science 325: 1001–1005. doi: 10.1126/science.1176676 19628815
61. Malkiel S, Kuhlow CJ, Mena P, Benach JL, (2009) The loss and gain of marginal zone and peritoneal B cells is different in response to relapsing fever and Lyme disease Borrelia. J Immunol 182: 498–506. 19109181