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PMID: 20643849 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Mucosal administration of flagellin protects mice from Streptococcus pneumoniae lung infection.

Infection and immunity ·Vol. 78 ·No. 10 ·2010-10-00 ·Pages 4226-33

Muñoz N, Van Maele L, Marqués JM, Rial A, Sirard JC, Chabalgoity JA

Abstract

Streptococcus pneumoniae is a major cause of pneumonia in infants and the elderly. Innate defenses are essential to the control of pneumococcal infections, and deficient responses can trigger disease in susceptible individuals. Here we showed that flagellin can locally activate innate immunity and thereby increase the resistance to acute pneumonia. Flagellin mucosal treatment improved S. pneumoniae clearance in the lungs and promoted increased survival of infection. In addition, lung architecture was fully restored after the treatment of infected mice, indicating that flagellin allows the reestablishment of steady-state conditions. Using a flagellin mutant that is unable to signal through Toll-like receptor 5 (TLR5), we established that TLR5 signaling is essential for protection. In the respiratory tract, flagellin induced neutrophil infiltration into airways and upregulated the expression of genes coding for interleukin 6 (IL-6), tumor necrosis factor alpha (TNF-α), CXCL1, CXCL2, and CCL20. Using depleting antibodies, we demonstrated that neutrophils are major effectors of protection. Further, we found that B- and T-cell-deficient SCID mice clear S. pneumoniae challenge to the same extent as immunocompetent animals, suggesting that these cell populations are not required for flagellin-induced protection. In conclusion, this study emphasizes that mucosal stimulation of innate immunity by a TLR not naturally engaged by S. pneumoniae can increase the potential to cure pneumococcal pneumonia.

MeSH Terms
Administration, Intranasal Animals B-Lymphocytes Bacterial Vaccines/administration & dosage,immunology Bronchoalveolar Lavage Female Flagellin/genetics,immunology Immunity, Innate Lung/cytology,microbiology,pathology Mice Mice, Inbred BALB C Mice, Inbred C57BL Mice, SCID Mutation Nasal Mucosa/immunology Neutrophils/physiology Pneumonia, Pneumococcal/immunology,prevention & control Signal Transduction Streptococcus pneumoniae/genetics,immunology T-Lymphocytes Toll-Like Receptor 5/physiology
Chemicals
Bacterial Vaccines Toll-Like Receptor 5 Flagellin
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Muñoz Natalia
Department of Biotechnology, Instituto de Higiene, Facultad de Medicina, Universidad de la República, Montevideo, Uruguay.
Van Maele Laurye
Marqués Juan M
Rial Analía
Sirard Jean-Claude
Chabalgoity José A
References (43)
43 references, click to expand
  1. The role of innate immune responses in the outcome of interspecies competition for colonization of mucosal surfaces.
    PLoS Pathog. 2005 Sep;1(1):e1 PMID: 16201010
  2. Stimulation of lung innate immunity protects against lethal pneumococcal pneumonia in mice.
    Am J Respir Crit Care Med. 2008 Jun 15;177(12):1322-30 PMID: 18388354
  3. Cutting edge: Tlr5-/- mice are more susceptible to Escherichia coli urinary tract infection.
    J Immunol. 2007 Apr 15;178(8):4717-20 PMID: 17404249
  4. Vaccination with the pneumococcal 7-valent conjugate: a successful experiment but the species is adapting.
    Expert Rev Vaccines. 2007 Jun;6(3):297-300 PMID: 17542743
  5. Administration of a synthetic TLR4 agonist protects mice from pneumonic tularemia.
    J Immunol. 2008 Jun 1;180(11):7574-81 PMID: 18490759
  6. Nucleotide-binding oligomerization domain proteins are innate immune receptors for internalized Streptococcus pneumoniae.
    J Biol Chem. 2004 Aug 27;279(35):36426-32 PMID: 15215247
  7. Flagellar activation of epithelial signaling.
    Am J Respir Cell Mol Biol. 2006 May;34(5):548-51 PMID: 16439803
  8. Involvement of Toll-like receptor 5 in the recognition of flagellated bacteria.
    Proc Natl Acad Sci U S A. 2006 Aug 15;103(33):12487-92 PMID: 16891416
  9. Nasopharyngeal colonization: a target for pneumococcal vaccination.
    Expert Rev Vaccines. 2006 Oct;5(5):651-67 PMID: 17181439
  10. Flagellin stimulation of intestinal epithelial cells triggers CCL20-mediated migration of dendritic cells.
    Proc Natl Acad Sci U S A. 2001 Nov 20;98(24):13722-7 PMID: 11717433
  11. Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf.
    Nat Immunol. 2006 Jun;7(6):569-75 PMID: 16648853
  12. Complexities of targeting innate immunity to treat infection.
    Trends Immunol. 2007 Jun;28(6):260-6 PMID: 17468048
  13. Activation of airway epithelial cells by toll-like receptor agonists.
    Am J Respir Cell Mol Biol. 2004 Sep;31(3):358-64 PMID: 15191912
  14. Dynamics of intrapulmonary bacterial growth in a murine model of repeated microaspiration.
    Am J Respir Cell Mol Biol. 2005 Nov;33(5):476-82 PMID: 16014897
  15. B-1a and B-1b cells exhibit distinct developmental requirements and have unique functional roles in innate and adaptive immunity to S. pneumoniae.
    Immunity. 2005 Jul;23(1):7-18 PMID: 16039575
  16. CD4-T-lymphocyte interactions with pneumolysin and pneumococci suggest a crucial protective role in the host response to pneumococcal infection.
    Infect Immun. 2004 May;72(5):2689-97 PMID: 15102777
  17. Nod1 signaling overcomes resistance of S. pneumoniae to opsonophagocytic killing.
    PLoS Pathog. 2007 Aug 24;3(8):e118 PMID: 17722978
  18. Coactivation of Syk kinase and MyD88 adaptor protein pathways by bacteria promotes regulatory properties of neutrophils.
    Immunity. 2009 Nov 20;31(5):761-71 PMID: 19913447
  19. Radioresistant cells expressing TLR5 control the respiratory epithelium's innate immune responses to flagellin.
    Eur J Immunol. 2009 Jun;39(6):1587-96 PMID: 19424969
  20. Pyogenic bacterial infections in humans with MyD88 deficiency.
    Science. 2008 Aug 1;321(5889):691-6 PMID: 18669862
  21. Deletion of flagellin's hypervariable region abrogates antibody-mediated neutralization and systemic activation of TLR5-dependent immunity.
    J Immunol. 2008 Aug 1;181(3):2036-43 PMID: 18641341
  22. Myeloid differentiation factor 88-dependent signalling controls bacterial growth during colonization and systemic pneumococcal disease in mice.
    Cell Microbiol. 2005 Nov;7(11):1603-15 PMID: 16207247
  23. Influence of neutropenia on the course of serotype 8 pneumococcal pneumonia in mice.
    Infect Immun. 2007 Apr;75(4):1586-97 PMID: 17296760
  24. Toll-like receptors stimulate human neutrophil function.
    Blood. 2003 Oct 1;102(7):2660-9 PMID: 12829592
  25. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5.
    Nature. 2001 Apr 26;410(6832):1099-103 PMID: 11323673
  26. Gene expression of Toll-like receptors and associated molecules induced by inflammatory stimuli in the primary alveolar macrophage.
    Biochem Biophys Res Commun. 2003 Jun 6;305(3):649-55 PMID: 12763043
  27. The role of flagellin versus motility in acute lung disease caused by Pseudomonas aeruginosa.
    J Infect Dis. 2007 Jul 15;196(2):289-96 PMID: 17570117
  28. Pathogenesis, treatment, and prevention of pneumococcal pneumonia.
    Lancet. 2009 Oct 31;374(9700):1543-56 PMID: 19880020
  29. Neutrophil recruitment to the lungs during bacterial pneumonia.
    Infect Immun. 2009 Feb;77(2):568-75 PMID: 19015252
  30. Multidrug-resistant Streptococcus pneumoniae infections: current and future therapeutic options.
    Drugs. 2007;67(16):2355-82 PMID: 17983256
  31. Molecular epidemiologic characterization of penicillin-resistant Streptococcus pneumoniae invasive pediatric isolates recovered in six Latin-American countries: an overview. PAHO/Rockefeller University Workshop. Pan American Health Organization.
    Microb Drug Resist. 1998 Fall;4(3):195-207 PMID: 9818971
  32. Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome.
    Proc Natl Acad Sci U S A. 2010 Feb 16;107(7):3076-80 PMID: 20133635
  33. Mucosal administration of flagellin induces innate immunity in the mouse lung.
    Infect Immun. 2004 Nov;72(11):6676-9 PMID: 15501801
  34. Bacterial flagellins: mediators of pathogenicity and host immune responses in mucosa.
    Trends Microbiol. 2004 Nov;12(11):509-17 PMID: 15488392
  35. Evolution and spread of antibiotic resistance.
    J Intern Med. 2002 Aug;252(2):91-106 PMID: 12190884
  36. Current and future drugs targeting one class of innate immunity receptors: the Toll-like receptors.
    Drug Discov Today. 2007 Jan;12(1-2):80-7 PMID: 17198976
  37. Host cellular immune response to pneumococcal lung infection in mice.
    Infect Immun. 2000 Feb;68(2):492-501 PMID: 10639409
  38. Both innate immunity and type 1 humoral immunity to Streptococcus pneumoniae are mediated by MyD88 but differ in their relative levels of dependence on toll-like receptor 2.
    Infect Immun. 2005 Jan;73(1):298-307 PMID: 15618166
  39. Exogenous heat-killed Escherichia coli improves alveolar macrophage activity and reduces Pneumocystis carinii lung burden in infant mice.
    Infect Immun. 2007 Jul;75(7):3382-93 PMID: 17485459
  40. Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1beta in salmonella-infected macrophages.
    Nat Immunol. 2006 Jun;7(6):576-82 PMID: 16648852
  41. Pneumococcal conjugate vaccine for childhood immunization--WHO position paper.
    Wkly Epidemiol Rec. 2007 Mar 23;82(12):93-104 PMID: 17380597
  42. Characterisation of an oxidative response inhibitor produced by Streptococcus pneumoniae.
    Thorax. 1994 Jul;49(7):676-83 PMID: 8066562
  43. Intranasal immunization with a colloid-formulated bacterial extract induces an acute inflammatory response in the lungs and elicits specific immune responses.
    Infect Immun. 2004 May;72(5):2679-88 PMID: 15102776
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
1098-5522
Published
2010-10-00
Epub
2010-00-19
Pages
4226-33
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC2950348
Subset
IM
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