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PMID: 19509469 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Cellular effectors mediating Th17-dependent clearance of pneumococcal colonization in mice.

The Journal of clinical investigation ·Vol. 119 ·No. 7 ·2009-07-00 ·Pages 1899-909

Zhang Z, Clarke TB, Weiser JN

Abstract

Microbial colonization of mucosal surfaces may be an initial event in the progression to disease, and it is often a transient process. For the extracellular pathogen Streptococcus pneumoniae studied in a mouse model, nasopharyngeal carriage is eliminated over a period of weeks and requires cellular rather than humoral immunity. Here, we demonstrate that primary infection led to TLR2-dependent recruitment of monocyte/macrophages into the upper airway lumen, where they engulfed pneumococci. Pharmacologic depletion of luminal monocyte/macrophages by intranasal instillation of liposomal clodronate diminished pneumococcal clearance. Efficient clearance of colonization required TLR2 signaling to generate a population of pneumococcal-specific IL-17-expressing CD4+ T cells. Depletion of either IL-17A or CD4+ T cells was sufficient to block the recruitment of monocyte/macrophages that allowed for effective late pneumococcal clearance. In contrast with naive mice, previously colonized mice showed enhanced early clearance that correlated with a more robust influx of luminal neutrophils. As for primary colonization, these cellular responses required Th17 immunity. Our findings demonstrate that monocyte/macrophages and neutrophils recruited to the mucosal surface are key effectors in clearing primary and secondary bacterial colonization, respectively.

MeSH Terms
Animals CD4-Positive T-Lymphocytes/immunology Clodronic Acid/administration & dosage Interleukin-17/physiology Liposomes Macrophages/physiology Mice Mice, Inbred C57BL Monocytes/physiology Pneumococcal Infections/immunology Toll-Like Receptor 2/physiology
Chemicals
Interleukin-17 Liposomes Tlr2 protein, mouse Toll-Like Receptor 2 Clodronic Acid
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Zhang Zhe
Department of Microbiology, University of Pennsylvania School of Medicine, Philadelphia, PA 19104-6076, USA.
Clarke Thomas B
Weiser Jeffrey N
References (53)
53 references, click to expand
  1. Are anticapsular antibodies the primary mechanism of protection against invasive pneumococcal disease?
    PLoS Med. 2005 Jan;2(1):e15 PMID: 15696204
  2. 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
  3. Limited role of antibody in clearance of Streptococcus pneumoniae in a murine model of colonization.
    Infect Immun. 2004 Oct;72(10):5807-13 PMID: 15385481
  4. Protection against nasopharyngeal colonization by Streptococcus pneumoniae is mediated by antigen-specific CD4+ T cells.
    Infect Immun. 2008 Jun;76(6):2678-84 PMID: 18391006
  5. Host and bacterial factors contributing to the clearance of colonization by Streptococcus pneumoniae in a murine model.
    Infect Immun. 2005 Nov;73(11):7718-26 PMID: 16239576
  6. Multiserotype protection of mice against pneumococcal colonization of the nasopharynx and middle ear by killed nonencapsulated cells given intranasally with a nontoxic adjuvant.
    Infect Immun. 2004 Jul;72(7):4290-2 PMID: 15213177
  7. Recognition of pneumolysin by Toll-like receptor 4 confers resistance to pneumococcal infection.
    Proc Natl Acad Sci U S A. 2003 Feb 18;100(4):1966-71 PMID: 12569171
  8. Expression of C-reactive protein in the human respiratory tract.
    Infect Immun. 2001 Mar;69(3):1747-54 PMID: 11179352
  9. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages.
    Nat Immunol. 2005 Nov;6(11):1123-32 PMID: 16200070
  10. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells.
    Nature. 2006 May 11;441(7090):235-8 PMID: 16648838
  11. PREVENTION OF PNEUMOCOCCAL PNEUMONIA BY IMMUNIZATION WITH SPECIFIC CAPSULAR POLYSACCHARIDES.
    J Exp Med. 1945 Nov 30;82(6):445-65 PMID: 19871511
  12. Expression and function of Toll-like receptors in T lymphocytes.
    Curr Opin Immunol. 2007 Feb;19(1):39-45 PMID: 17129718
  13. A novel method for isolation of neutrophils from murine blood using negative immunomagnetic separation.
    Am J Pathol. 2001 Aug;159(2):473-81 PMID: 11485906
  14. 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
  15. Streptococcus pneumoniae colonisation: the key to pneumococcal disease.
    Lancet Infect Dis. 2004 Mar;4(3):144-54 PMID: 14998500
  16. The scavenger receptor MARCO is required for lung defense against pneumococcal pneumonia and inhaled particles.
    J Exp Med. 2004 Jul 19;200(2):267-72 PMID: 15263032
  17. Antibody-independent, interleukin-17A-mediated, cross-serotype immunity to pneumococci in mice immunized intranasally with the cell wall polysaccharide.
    Infect Immun. 2006 Apr;74(4):2187-95 PMID: 16552049
  18. Human C-reactive protein is protective against fatal Streptococcus pneumoniae infection in transgenic mice.
    J Immunol. 1995 Sep 1;155(5):2557-63 PMID: 7650385
  19. Interleukin-17 as a recruitment and survival factor for airway macrophages in allergic airway inflammation.
    Am J Respir Cell Mol Biol. 2005 Sep;33(3):248-53 PMID: 15901616
  20. The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease.
    Nat Rev Microbiol. 2008 Apr;6(4):288-301 PMID: 18340341
  21. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17.
    Nat Immunol. 2005 Nov;6(11):1133-41 PMID: 16200068
  22. Immunogenicity and impact on nasopharyngeal carriage of a nonavalent pneumococcal conjugate vaccine.
    J Infect Dis. 1999 Oct;180(4):1171-6 PMID: 10479145
  23. Cytokine kinetics and other host factors in response to pneumococcal pulmonary infection in mice.
    Infect Immun. 1998 Mar;66(3):912-22 PMID: 9488375
  24. Some aspects of the pneumococcal carrier state.
    J Antimicrob Chemother. 1986 Jul;18 Suppl A:35-45 PMID: 3745031
  25. Interaction of SIGNR1 expressed by marginal zone macrophages with marginal zone B cells is essential to early IgM responses against Streptococcus pneumoniae.
    Mol Immunol. 2008 May;45(10):2881-7 PMID: 18343501
  26. A recombinant Listeria monocytogenes vaccine expressing a model tumour antigen protects mice against lethal tumour cell challenge and causes regression of established tumours.
    Nat Med. 1995 May;1(5):471-7 PMID: 7585097
  27. Antibody-independent, CD4+ T-cell-dependent protection against pneumococcal colonization elicited by intranasal immunization with purified pneumococcal proteins.
    Infect Immun. 2007 Nov;75(11):5460-4 PMID: 17698570
  28. Pulmonary surfactant protein A augments the phagocytosis of Streptococcus pneumoniae by alveolar macrophages through a casein kinase 2-dependent increase of cell surface localization of scavenger receptor A.
    J Biol Chem. 2004 May 14;279(20):21421-30 PMID: 14993215
  29. The liposome-mediated macrophage 'suicide' technique.
    J Immunol Methods. 1989 Nov 13;124(1):1-6 PMID: 2530286
  30. CD4+ T cells mediate antibody-independent acquired immunity to pneumococcal colonization.
    Proc Natl Acad Sci U S A. 2005 Mar 29;102(13):4848-53 PMID: 15781870
  31. The inhibitory effect of C-reactive protein on bacterial phosphorylcholine platelet-activating factor receptor-mediated adherence is blocked by surfactant.
    J Infect Dis. 2002 Aug 1;186(3):361-71 PMID: 12134232
  32. Early clearance of pneumococci from the lungs of decomplemented rats.
    Infect Immun. 1982 Apr;36(1):24-9 PMID: 7076296
  33. Antibody responses to nasopharyngeal carriage of Streptococcus pneumoniae in adults: a longitudinal household study.
    J Infect Dis. 2005 Aug 1;192(3):387-93 PMID: 15995951
  34. Neutrophil-toxin interactions promote antigen delivery and mucosal clearance of Streptococcus pneumoniae.
    J Immunol. 2008 May 1;180(9):6246-54 PMID: 18424747
  35. Macrophage Turnover Kinetics in the Lungs of Mice Infected with Streptococcus pneumoniae.
    Am J Respir Cell Mol Biol. 2008 Jan;38(1):105-13 PMID: 17690327
  36. Efficacy of nine-valent pneumococcal conjugate vaccine against pneumonia and invasive pneumococcal disease in The Gambia: randomised, double-blind, placebo-controlled trial.
    Lancet. 2005 Mar 26-Apr 1;365(9465):1139-46 PMID: 15794968
  37. Macrophage complement receptors and pathogen clearance.
    Cell Microbiol. 2007 Sep;9(9):2095-102 PMID: 17590164
  38. Serum serotype-specific pneumococcal anticapsular immunoglobulin g concentrations after immunization with a 9-valent conjugate pneumococcal vaccine correlate with nasopharyngeal acquisition of pneumococcus.
    J Infect Dis. 2005 Aug 1;192(3):367-76 PMID: 15995949
  39. Phase variation in pneumococcal opacity: relationship between colonial morphology and nasopharyngeal colonization.
    Infect Immun. 1994 Jun;62(6):2582-9 PMID: 8188381
  40. Monocytes recruited into the alveolar air space of mice show a monocytic phenotype but upregulate CD14.
    Am J Physiol Lung Cell Mol Physiol. 2001 Jan;280(1):L58-68 PMID: 11133495
  41. Interleukin-17A mediates acquired immunity to pneumococcal colonization.
    PLoS Pathog. 2008 Sep 19;4(9):e1000159 PMID: 18802458
  42. Long-term effect of pneumococcal conjugate vaccine on nasopharyngeal colonization by Streptococcus pneumoniae--and associated interactions with Staphylococcus aureus and Haemophilus influenzae colonization--in HIV-Infected and HIV-uninfected children.
    J Infect Dis. 2007 Dec 1;196(11):1662-6 PMID: 18008250
  43. Interleukin-17 family members and inflammation.
    Immunity. 2004 Oct;21(4):467-76 PMID: 15485625
  44. TLR signaling.
    Curr Top Microbiol Immunol. 2006;311:1-16 PMID: 17048703
  45. Endogenous IL-17 as a mediator of neutrophil recruitment caused by endotoxin exposure in mouse airways.
    J Immunol. 2003 May 1;170(9):4665-72 PMID: 12707345
  46. Th17 cells and mucosal host defense.
    Semin Immunol. 2007 Dec;19(6):377-82 PMID: 18054248
  47. Nasopharyngeal carriage of Streptococcus pneumoniae in Finnish children younger than 2 years old.
    J Infect Dis. 2001 Aug 15;184(4):451-9 PMID: 11471103
  48. The immune response to pneumococcal proteins during experimental human carriage.
    J Exp Med. 2002 Feb 4;195(3):359-65 PMID: 11828011
  49. Early bacterial colonization induces toll-like receptor-dependent transforming growth factor beta signaling in the epithelium.
    Infect Immun. 2009 May;77(5):2212-20 PMID: 19255194
  50. Live attenuated Streptococcus pneumoniae strains induce serotype-independent mucosal and systemic protection in mice.
    Infect Immun. 2007 May;75(5):2469-75 PMID: 17339359
  51. Differential roles of TLR2 and TLR4 in recognition of gram-negative and gram-positive bacterial cell wall components.
    Immunity. 1999 Oct;11(4):443-51 PMID: 10549626
  52. Inhibition of pulmonary antibacterial defense by interferon-gamma during recovery from influenza infection.
    Nat Med. 2008 May;14(5):558-64 PMID: 18438414
  53. Blockade of antimicrobial proteins S100A8 and S100A9 inhibits phagocyte migration to the alveoli in streptococcal pneumonia.
    J Immunol. 2008 Mar 1;180(5):3366-74 PMID: 18292562
Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
1558-8238
Published
2009-07-00
Epub
2009-00-08
Pages
1899-909
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC2701860
Subset
IM
Grants
NIAID NIH HHS · R01 AI044231 · United States
NIDDK NIH HHS · P30 DK050306 · United States
NIAID NIH HHS · R21 AI044231 · United States
NIAID NIH HHS · AI44231 · United States
NIDDK NIH HHS · P30 DK50306 · United States
NIAID NIH HHS · AI38446 · United States
NIAID NIH HHS · R01 AI038446 · United States
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