Impaired colonic B-cell responses by gastrointestinal Bacillus anthracis infection

Journal of Infectious Diseases

Volumn 210, Issue 9, 2014, Pages 1499-1507

  Sahay, Bikash ^a,b   Owen, Jennifer L ^c   Zadeh, Mojgan ^a,b   Yang, Tao ^a,b   Lightfoot, Yaíma L ^a,b   Abed, Firas ^a,b   Mohamadzadeh, Mansour ^a,b  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^c University of Florida   (United States)

Author keywords

Anthrax toxin; B 1 cells; Bacillus anthracis; Type 2 innate lymphoid cells

Indexed keywords

APRIL PROTEIN; B CELL ACTIVATING FACTOR; B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; B LYMPHOCYTE RECEPTOR; CD11B ANTIGEN; CD45 ANTIGEN; CHEMOKINE RECEPTOR CCR6; CHEMOKINE RECEPTOR CCR9; CHEMOKINE RECEPTOR CXCR5; CXCL13 CHEMOKINE; CYCLOPHILIN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G2B; INDUCIBLE T CELL COSTIMULATOR LIGAND; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 33; INTERLEUKIN 5; INTERLEUKIN 7 RECEPTOR ALPHA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; NEUTRALIZING ANTIBODY; PROGRAMMED DEATH 1 RECEPTOR; PROTEIN BCL 6; STEM CELL FACTOR RECEPTOR;

ANIMAL CELL; ANIMAL MODEL; ANTHRAX; ANTIBODY RESPONSE; ANTIGEN EXPRESSION; ARTICLE; B LYMPHOCYTE; BACILLUS ANTHRACIS; CELL DIFFERENTIATION; CELL EXPANSION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; ENZYME PHOSPHORYLATION; EPITHELIUM CELL; FLOW CYTOMETRY; GASTROINTESTINAL INFECTION; GERMINAL CENTER; HUMORAL IMMUNITY; IMMUNOGLOBULIN PRODUCTION; INNATE IMMUNITY; LYMPHOID CELL; MOUSE; NONHUMAN; PEYER PATCH; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SOMATIC HYPERMUTATION; ANIMAL; CELLULAR IMMUNITY; COLON; GASTROINTESTINAL DISEASE; IMMUNOLOGY; MICROBIOLOGY; PHYSIOLOGY;

ANIMALS; ANTHRAX; B-LYMPHOCYTES; BACILLUS ANTHRACIS; COLON; FLOW CYTOMETRY; GASTROINTESTINAL DISEASES; IMMUNITY, CELLULAR; MICE; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84924605724     PISSN: 00221899     EISSN: 15376613     Source Type: Journal    
DOI: 10.1093/infdis/jiu280     Document Type: Article

References (50)

1. Mikesell P, Ivins BE, Ristroph JD, Dreier TM. Evidence for plasmidmediated toxin production in Bacillus anthracis. Infect Immun 1983;39:371-6.
2. Tonello F, Zornetta I. Bacillus anthracis factors for phagosomal escape. Toxins (Basel) 2012; 4:536-53.
3. Makino S, Watarai M, Cheun HI, Shirahata T, Uchida I. Effect of the lower molecular capsule released from the cell surface of Bacillus anthracis on the pathogenesis of anthrax. J Infect Dis 2002; 186:227-33.
4. Lee YK, Mazmanian SK. Has the microbiota played a critical role in the evolution of the adaptive immune system? Science 2010; 330:1768-73.
5. Fagarasan S. Intestinal IgA synthesis: a primitive form of adaptive immunity that regulates microbial communities in the gut. Curr Top Microbiol Immunol 2006; 308:137-53.
6. Shulzhenko N, Morgun A, Hsiao W, et al. Crosstalk between B lymphocytes, microbiota and the intestinal epithelium governs immunity versus metabolism in the gut. Nat Med 2011; 17:1585-93.
7. Wang H, Shin DM, Abbasi S, et al. Expression of plasma cell alloantigen 1 defines layered development of B-1a B-cell subsets with distinct innate-like functions. Proc Natl Acad Sci U S A 2012; 109:20077-82.
8. Hayakawa K, Hardy RR, Parks DR, Herzenberg LA. The "Ly-1 B" cell subpopulation in normal immunodefective, and autoimmune mice. J Exp Med 1983; 157:202-18.
9. Fagarasan S, Honjo T. T-independent immune response: new aspects of B cell biology. Science 2000; 290:89-92.
10. Macpherson AJ, Gatto D, Sainsbury E, Harriman GR, Hengartner H, Zinkernagel RM. A primitive T cell-independent mechanism of intestinal mucosal IgA responses to commensal vacteria. Science 2000;288:2222-6.
11. Hong HA, Khaneja R, Tam NM, et al. Bacillus subtilis isolated from the human gastrointestinal tract. Res Microbiol 2009; 160:134-43.
12. Moro K, Yamada T, Tanabe M, et al. Innate production of T(H)2 cytokines by adipose tissue-associated c-Kit(+)Sca-1(+) lymphoid cells. Nature 2010; 463:540-4.
13. Welkos SL, Keener TJ, Gibbs PH. Differences in susceptibility of inbred mice to Bacillus anthracis. Infect Immun 1986; 51:795-800.
14. Kathania M, Zadeh M, Lightfoot YL, et al. Colonic immune stimulation by targeted oral vaccine. PLoS One 2013; 8:e55143.
15. Mohamadzadeh M, Durmaz E, Zadeh M, et al. Targeted expression of anthrax protective antigen by Lactobacillus gasseri as an anthrax vaccine. Future Microbiol 2010; 5:1289-96.
16. Goossens PL. Animal models of human anthrax: the Quest for the Holy Grail. Mol Aspects Med 2009; 30:467-80.
17. Bachmann M, Dragoi C, Poleganov MA, Pfeilschifter J, Mühl H. Interleu-kin-directly activates T-bet expression and function via p38 mitogenactivated protein kinase and nuclear factor-kB in acute myeloid leukemiaderived predendritic KG-1 cells. Mol Cancer Ther 2007; 6:723-31.
18. Kao C, Oestreich KJ, Paley MA, et al. Transcription factor T-bet represses expression of the inhibitory receptor PD-1 and sustains virus-specific CD8+ T cell responses during chronic infection. Nat Immunol 2011;12:663-71.
19. Okazaki T, Maeda A, Nishimura H, Kurosaki T, Honjo T. PD-1 immunoreceptor inhibits B cell receptor-mediated signaling by recruiting src homology 2-domain-containing tyrosine phosphatase 2 to phosphotyrosine. Proc Natl Acad Sci U S A 2001; 98:13866-71.
20. Haas KM. Programmed cell death 1 suppresses B-1b cell expansion and long-lived IgG production in response to T cell-independent type 2 antigens. J Immunol 2011; 187:5183-95.
21. Castigli E, Wilson SA, Scott S, et al. TACI and BAFF-R mediate isotype switching in B cells. J Exp Med 2005; 201:35-9.
22. Vasanwala FH, Kusam S, Toney LM, Dent AL. Repression of AP-1 function: a mechanism for the regulation of Blimp-1 expression and B lymphocyte differentiation by the B cell lymphoma-6 protooncogene. J Immunol 2002; 169:1922-9.
23. Spencer SP, Wilhelm C, Yang Q, et al. Adaptation of innate lymphoid cells to a micronutrient deficiency promotes type 2 barrier immunity. Science 2014; 343:432-7.
24. Brenneman KE, Doganay M, Akmal A, et al. The early humoral immune response to Bacillus anthracis toxins in patients infected with cutaneous anthrax. FEMS Immunol Med Microbiol 2011; 62:164-72.
25. Spits H, Cupedo T. Innate lymphoidcells: emerging insights indevelopment, lineage relationships, and function. Annu Rev Immunol 2012; 30:647-75.
26. Licona-Limon P, Kim LK, Palm NW, Flavell RA. TH2, allergy and group 2 innate lymphoid cells. Nat Immunol 2013; 14:536-42.
27. Bulek K, Swaidani S, Aronica M, Li X. Epithelium: the interplay between innate and Th2 immunity. Immunol Cell Biol 2010; 88:257-68.
28. Sahay B, Owen JL, Yang T, et al. Activation of B cells by a dendritic cell-targeted oral vaccine. Curr Pharmaceut Biotechnol 2014; 14:867-77.
29. Comerford I, McColl SR. Mini-review series: focus on chemokines. Immunol Cell Biol 2011; 89:183-4.
30. Ansel KM, Harris RB, Cyster JG. CXCL13 is required for B1 cell homing, natural antibody production, and body cavity immunity. Immunity 2002; 16:67-76.
31. Oscherwitz J, Yu F, Jacobs JL, Cease KB. Recombinant vaccine displaying the loop-neutralizing determinant from protective antigen completely protects rabbits from experimental inhalation anthrax. Clin Vaccine Immunol 2013; 20:341-9.
32. Takada M, Koizumi T, Bachiller D, Ruther U, Tokuhisa T. Deregulated c-fos modulates IgG2b production of B cells mediated by lipopolysaccharide. Immunobiology 1993; 188:233-41.
33. Wang Y, Prywes R. Activation of the c-fos enhancer by the erk MAP kinase pathway through two sequence elements: the c-fos AP-1 and p62TCF sites. Oncogene 2000; 19:1379-85.
34. Tanos T, Marinissen MJ, Leskow FC, et al. Phosphorylation of c-Fos by members of the p38 MAPK family. Role in the AP-1 response to UV light. J Biol Chem 2005; 280:18842-52.
35. Xie T, Sun C, Uslu K, et al. A new murine model for gastrointestinal anthrax infection. PLoS One 2013; 8:e66943.
36. Swartz MN. Recognition and management of anthrax - an update. N Engl J Med 2001; 345:1621-6.
37. Brodsky IE, Medzhitov R. Targeting of immune signalling networks by bacterial pathogens. Nat Cell Biol 2009; 11:521-6.
38. Roy CR, Mocarski ES. Pathogen subversion of cell-intrinsic innate immunity. Nat Immunol 2007; 8:1179-87.
39. Mohamadzadeh M, Chen L, Schmaljohn AL. How Ebola and Marburg viruses battle the immune system. Nat Rev Immunol 2007; 7:556-67.
40. Ebrahimi CM, Sheen TR, Renken CW, Gottlieb RA, Doran KS. Contribution of lethal toxin and edema toxin to the pathogenesis of anthrax meningitis. Infect Immun 2011; 79:2510-8.
41. Young JA, Collier RJ. Anthrax toxin: receptor binding, internalization, pore formation, and translocation. Annu Rev Biochem 2007; 76:243-65.
42. Hu H, Leppla SH. Anthrax toxin uptake by primary immune cells as determined with a lethal factor-beta-lactamase fusion protein. PLoS One 2009; 4:e7946.
43. Rayamajhi M, Delgado C, Condon TV, Riches DW, Lenz LL. Lung B cells promote early pathogen dissemination and hasten death from inhalation anthrax. Mucosal Immunol 2012; 5:444-54.
44. Oliva CR, Swiecki MK, Griguer CE, et al. The integrin Mac-1 (CR3) mediates internalization and directs Bacillus anthracis spores into professional phagocytes. Proc Natl Acad Sci U S A 2008; 105:1261-6.
45. Arthur JS, Ley SC. Mitogen-activated protein kinases in innate immunity. Nat Rev Immunol 2013; 13:679-92.
46. Palmer G, Gabay C. Interleukin-33 biology with potential insights into human diseases. Nat Rev Rheumatol 2011; 7:321-9.
47. Baldari CT, Tonello F, Paccani SR, Montecucco C. Anthrax toxins: A paradigm of bacterial immune suppression. Trends Immunol 2006; 27:434-40.
48. Quinn CP, Dull PM, Semenova V, et al. Immune responses to Bacillus anthracis protective antigen in patients with bioterrorism-related cutaneous or inhalation anthrax. J Infect Dis 2004; 190:1228-36.
49. Fang H, Xu L, Chen TY, Cyr JM, Frucht DM. Anthrax lethal toxin has direct and potent inhibitory effects on B cell proliferation and immunoglobulin production. J Immunol 2006; 176:6155-61.
50. Hadler JL. Learning from the 2001 anthrax attacks: immunological characteristics. J Infect Dis 2007; 195:163-4.