Protection against Streptococcus pneumoniae serotype 1 acute infection shows a signature of Th17- and IFN-γ-mediated immunity

Immunobiology

Volumn 217, Issue 4, 2012, Pages 420-429

  Marqués, Juan M ^a   Rial, Analía ^a   Muñoz, Natalia ^a   Pellay, Francois Xavier ^b   Van Maele, Laurye ^c,d,e   Léger, Hélène ^b   Camou, Teresa ^f   Sirard, Jean Claude ^c,d,e   Benecke, Arndt ^b   Chabalgoity, José A ^a  

^a Universidad de la Republica Instituto de Higiene   (Uruguay)

^b INSTITUT DES HAUTES ÉTUDES SCIENTIFIQUES   (France)

^c INSERM   (France)

^d CNRS   (France)

^e UNIV LILLE   (France)

^f Centro Nacional de Referencia de Influenza   (Uruguay)

Author keywords

IFN ; IL 17A; Pneumonia; Protective immunity; Streptococcus pneumoniae; Th17; Transcriptome

Indexed keywords

GAMMA INTERFERON; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN M ANTIBODY; INTERLEUKIN 17; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY DETECTION; ANTIBODY RESPONSE; ARTICLE; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; FEMALE; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; HUMORAL IMMUNITY; INFECTION PREVENTION; LEUKOCYTE ACTIVATION; LOBAR PNEUMONIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SEROTYPE; STREPTOCOCCUS PNEUMONIA; STREPTOCOCCUS PNEUMONIAE; TH17 CELL; TRANSCRIPTION REGULATION;

ANIMALS; ANTIBODIES, BACTERIAL; CYTOPROTECTION; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-17; LUNG; MICE; MICE, INBRED C57BL; MICROARRAY ANALYSIS; NEUTROPHILS; PNEUMOCOCCAL INFECTIONS; POLYSACCHARIDES, BACTERIAL; STREPTOCOCCUS PNEUMONIAE; TH17 CELLS; UP-REGULATION;

EID: 84858072040     PISSN: 01712985     EISSN: 18783279     Source Type: Journal    
DOI: 10.1016/j.imbio.2011.10.012     Document Type: Article

References (56)

1. Abeyta M., Hardy G.G., Yother J. Genetic alteration of capsule type but not PspA type affects accessibility of surface-bound complement and surface antigens of Streptococcus pneumoniae. Infect. Immun. 2003, 71:218.
2. AlonsoDeVelasco E., Verheul A.F., Verhoef J., Snippe H. Streptococcus pneumoniae: virulence factors, pathogenesis, and vaccines. Microbiol. Rev. 1995, 59:591.
3. Aujla S.J., Dubin P.J., Kolls J.K. Interleukin-17 in pulmonary host defense. Exp. Lung Res. 2007, 33:507.
4. + T-cell-dependent protection against pneumococcal colonization elicited by intranasal immunization with purified pneumococcal proteins. Infect. Immun. 2007, 75:5460.
5. Brown J.S., Hussell T., Gilliland S.M., Holden D.W., Paton J.C., Ehrenstein M.R., Walport M.J., Botto M. The classical pathway is the dominant complement pathway required for innate immunity to Streptococcus pneumoniae infection in mice. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:16969.
6. Brysbaert G., Pellay F.X., Noth S., Benecke A. Quality assessment of transcriptome data using intrinsic statistical properties. Genomics Proteomics Bioinformatics 2010, 8:57.
7. Cobb B.A., Kasper D.L. Zwitterionic capsular polysaccharides: the new MHCII-dependent antigens. Cell. Microbiol. 2005, 7:1398.
8. Curtis M.M., Way S.S. Interleukin-17 in host defence against bacterial, mycobacterial and fungal pathogens. Immunology 2009, 126:177.
9. + T cells mediate abscess formation in intra-abdominal sepsis by an IL-17-dependent mechanism. J. Immunol. 2003, 170:1958.
10. Fukuyama Y., King J.D., Kataoka K., Kobayashi R., Gilbert R.S., Oishi K., Hollingshead S.K., Briles D.E., Fujihashi K. Secretory-IgA antibodies play an important role in the immunity to Streptococcus pneumoniae. J. Immunol. 2010, 185:1755.
11. + T cells promote host memory immune responses to Zwitterionic polysaccharide of Streptococcus pneumoniae. Infect. Immun. 2009, 77:3705.
12. Happel K.I., Zheng M., Young E., Quinton L.J., Lockhart E., Ramsay A.J., Shellito J.E., Schurr J.R., Bagby G.J., Nelson S., Kolls J.K. Cutting edge: roles of Toll-like receptor 4 and IL-23 in IL-17 expression in response to Klebsiella pneumoniae infection. J. Immunol. 2003, 170:4432.
13. Hortal M., Sehabiague G., Camou T., Iraola I., Estevan M., Pujadas M. Pneumococcal pneumonia in hospitalized Uruguayan children and potential prevention with different vaccine formulations. J. Pediatr. 2008, 152:850.
14. Ishigame H., Kakuta S., Nagai T., Kadoki M., Nambu A., Komiyama Y., Fujikado N., Tanahashi Y., Akitsu A., Kotaki H., Sudo K., Nakae S., Sasakawa C., Iwakura Y. Differential roles of interleukin-17A and -17F in host defense against mucoepithelial bacterial infection and allergic responses. Immunity 2009, 30:108.
15. Kadioglu A., Coward W., Colston M.J., Hewitt C.R., Andrew P.W. CD4-T-lymphocyte interactions with pneumolysin and pneumococci suggest a crucial protective role in the host response to pneumococcal infection. Infect. Immun. 2004, 72:2689.
16. Kadioglu A., Gingles N.A., Grattan K., Kerr A., Mitchell T.J., Andrew P.W. Host cellular immune response to pneumococcal lung infection in mice. Infect. Immun. 2000, 68:492.
17. Kayhty H., Auranen K., Nohynek H., Dagan R., Makela H. Nasopharyngeal colonization: a target for pneumococcal vaccination. Expert Rev. Vaccines 2006, 5:651.
18. Kolls J.K., Khader S.A. The role of Th17 cytokines in primary mucosal immunity. Cytokine Growth Factor Rev. 2010, 21:443.
19. Kolls J.K., Linden A. Interleukin-17 family members and inflammation. Immunity 2004, 21:467.
20. Ley K., Smith E., Stark M.A. IL-17A-producing neutrophil-regulatory Tn lymphocytes. Immunol. Res. 2006, 34:229.
21. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402.
22. Lu Y.J., Gross J., Bogaert D., Finn A., Bagrade L., Zhang Q., Kolls J.K., Srivastava A., Lundgren A., Forte S., Thompson C.M., Harney K.F., Anderson P.W., Lipsitch M., Malley R. Interleukin-17A mediates acquired immunity to pneumococcal colonization. PLoS Pathog. 2008, 4:e1000159.
23. Lynch J.P., Zhanel G.G. Streptococcus pneumoniae: epidemiology, risk factors, and strategies for prevention. Semin. Respir. Crit. Care Med. 2009, 30:189.
24. Malley R. Antibody and cell-mediated immunity to Streptococcus pneumoniae: implications for vaccine development. J. Mol. Med. 2010, 88:135.
25. + T cells mediate antibody-independent acquired immunity to pneumococcal colonization. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:4848.
26. McNeela E.A., Burke A., Neill D.R., Baxter C., Fernandes V.E., Ferreira D., Smeaton S., El-Rachkidy R., McLoughlin R.M., Mori A., Moran B., Fitzgerald K.A., Tschopp J., Petrilli V., Andrew P.W., Kadioglu A., Lavelle E.C. Pneumolysin activates the NLRP3 inflammasome and promotes proinflammatory cytokines independently of TLR4. PLoS Pathog. 2010, 6:e1001191.
27. Michel M.L., Keller A.C., Paget C., Fujio M., Trottein F., Savage P.B., Wong C.H., Schneider E., Dy M., Leite-de-Moraes M.C. Identification of an IL-17-producing NK1.1(neg) iNKT cell population involved in airway neutrophilia. J. Exp. Med. 2007, 204:995.
28. Mitsdoerffer M., Lee Y., Jager A., Kim H.J., Korn T., Kolls J.K., Cantor H., Bettelli E., Kuchroo V.K. Proinflammatory T helper type 17 cells are effective B-cell helpers. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:14292.
29. Miyamoto M., Prause O., Sjostrand M., Laan M., Lotvall J., Linden A. Endogenous IL-17 as a mediator of neutrophil recruitment caused by endotoxin exposure in mouse airways. J. Immunol. 2003, 170:4665.
30. Moffitt K.L., Gierahn T.M., Lu Y.J., Gouveia P., Alderson M., Flechtner J.B., Higgins D.E., Malley R. T(H)17-based vaccine design for prevention of Streptococcus pneumoniae colonization. Cell Host Microbe 2011, 9:158.
31. Munoz N., V.A.N.M.L., Marques J.M., Rial A., Sirard J.C., Chabalgoity J.A. Mucosal administration of flagellin protects mice from Streptococcus pneumoniae lung infection. Infect. Immun. 2010.
32. Nakae S., Komiyama Y., Nambu A., Sudo K., Iwase M., Homma I., Sekikawa K., Asano M., Iwakura Y. Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity 2002, 17:375.
33. Normark B.H., Normark S. Evolution and spread of antibiotic resistance. J. Intern. Med. 2002, 252:91.
34. Noth S., Benecke A. Avoiding inconsistencies over time and tracking difficulties in Applied Biosystems AB1700/Panther probe-to-gene annotations. BMC Bioinformatics 2005, 6:307.
35. Noth S., Brysbaert G., Benecke A. Normalization using weighted negative second order exponential error functions (NeONORM) provides robustness against asymmetries in comparative transcriptome profiles and avoids false calls. Genomics Proteomics Bioinformatics 2006, 4:90.
36. Paterson G.K., Mitchell T.J. Innate immunity and the pneumococcus. Microbiology 2006, 152:285.
37. Poolman J.T. Pneumococcal vaccine development. Expert Rev. Vaccines 2004, 3:597.
38. Rial A., Lens D., Betancor L., Benkiel H., Silva J.S., Chabalgoity J.A. Intranasal immunization with a colloid-formulated bacterial extract induces an acute inflammatory response in the lungs and elicits specific immune responses. Infect. Immun. 2004, 72:2679.
39. Richards L., Ferreira D.M., Miyaji E.N., Andrew P.W., Kadioglu A. The immunising effect of pneumococcal nasopharyngeal colonisation; protection against future colonisation and fatal invasive disease. Immunobiology 2010, 215:251.
40. Rijneveld A.W., Lauw F.N., Schultz M.J., Florquin S., Te Velde A.A., Speelman P., Van Deventer S.J., Van Der Poll T. The role of interferon-gamma in murine pneumococcal pneumonia. J. Infect. Dis. 2002, 185:91.
41. Roche A.M., King S.J., Weiser J.N. Live attenuated Streptococcus pneumoniae strains induce serotype-independent mucosal and systemic protection in mice. Infect. Immun. 2007, 75:2469.
42. Roche A.M., Weiser J.N. Identification of the targets of cross-reactive antibodies induced by Streptococcus pneumoniae colonization. Infect. Immun. 2010, 78:2231.
43. Rosseau S., Hocke A., Mollenkopf H., Schmeck B., Suttorp N., Kaufmann S.H., Zerrahn J. Comparative transcriptional profiling of the lung reveals shared and distinct features of Streptococcus pneumoniae and influenza A virus infection. Immunology 2007, 120:380.
44. Rubins J.B., Pomeroy C. Role of gamma interferon in the pathogenesis of bacteremic pneumococcal pneumonia. Infect. Immun. 1997, 65:2975.
45. Salyers A.W.D. Bacterial Pathogenesis. A Molecular Approach 2002, ASM Press. 2nd edition.
46. Trzcinski K., Thompson C., Malley R., Lipsitch M. Antibodies to conserved pneumococcal antigens correlate with, but are not required for, protection against pneumococcal colonization induced by prior exposure in a mouse model. Infect. Immun. 2005, 73:7043.
47. + T cells. Infect. Immun. 2008, 76:2678.
48. van der Poll T., Opal S.M. Pathogenesis, treatment, and prevention of pneumococcal pneumonia. Lancet 2009, 374:1543.
49. + immune cells in spleen and mucosa. J. Immunol. 2010, 185:1177.
50. Velez C.D., Lewis C.J., Kasper D.L., Cobb B.A. Type I Streptococcus pneumoniae carbohydrate utilizes a nitric oxide and MHC II-dependent pathway for antigen presentation. Immunology 2009, 127:73.
51. Wernette C.M., Frasch C.E., Madore D., Carlone G., Goldblatt D., Plikaytis B., Benjamin W., Quataert S.A., Hildreth S., Sikkema D.J., Kayhty H., Jonsdottir I., Nahm M.H. Enzyme-linked immunosorbent assay for quantitation of human antibodies to pneumococcal polysaccharides. Clin. Diagn. Lab. Immunol. 2003, 10:514.
52. WHO 23-Valent pneumococcal polysaccharide vaccine. WHO position paper. Wkly. Epidemiol. Rec. 2008, 83:373.
53. Yamamoto N., Kawakami K., Kinjo Y., Miyagi K., Kinjo T., Uezu K., Nakasone C., Nakamatsu M., Saito A. Essential role for the p40 subunit of interleukin-12 in neutrophil-mediated early host defense against pulmonary infection with Streptococcus pneumoniae: involvement of interferon-gamma. Microbes Infect. 2004, 6:1241.
54. Ye P., Garvey P.B., Zhang P., Nelson S., Bagby G., Summer W.R., Schwarzenberger P., Shellito J.E., Kolls J.K. Interleukin-17 and lung host defense against Klebsiella pneumoniae infection. Am. J. Respir. Cell Mol. Biol. 2001, 25:335.
55. Zemlickova H., Crisostomo M.I., Brandileone M.C., Camou T., Castaneda E., Corso A., Echaniz-Aviles G., Pasztor M., Tomasz A. Serotypes and clonal types of penicillin-susceptible Streptococcus pneumoniae causing invasive disease in children in five Latin American countries. Microb. Drug Resist. 2005, 11:195.
56. Zhang Z., Clarke T.B., Weiser J.N. Cellular effectors mediating Th17-dependent clearance of pneumococcal colonization in mice. J. Clin. Invest. 2009, 119:1899.