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PMID: 24962092 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Antibody blocks acquisition of bacterial colonization through agglutination.

Mucosal immunology ·Vol. 8 ·No. 1 ·2015-01-00 ·Pages 176-85

Roche AM, Richard AL, Rahkola JT, Janoff EN, Weiser JN

Abstract

Invasive infection often begins with asymptomatic colonization of mucosal surfaces. A murine model of bacterial colonization with Streptococcus pneumoniae was used to study the mechanism for mucosal protection by immunoglobulin. In previously colonized immune mice, bacteria were rapidly sequestered within large aggregates in the nasal lumen. To further examine the role of bacterial agglutination in protection by specific antibodies, mice were passively immunized with immunoglobulin G (IgG) purified from antipneumococcal sera or pneumococcal type-specific monoclonal human IgA (hIgA1 or hIgA2). Systemically delivered IgG accessed the mucosal surface and blocked acquisition of colonization and transmission between littermates. Optimal protection by IgG was independent of Fc fragment and complement and, therefore, did not involve an opsonophagocytic mechanism. Enzymatic digestion or reduction of IgG before administration showed that protection required divalent binding that maintained its agglutinating effect. Divalent hIgA1 is cleaved by the pneumococcal member of a family of bacterial proteases that generate monovalent Fabα fragments. Thus, passive immunization with hIgA1 blocked colonization by an IgA1-protease-deficient mutant (agglutinated) but not the protease-producing wild-type parent (not agglutinated), whereas protease-resistant hIgA2 agglutinated and blocked colonization by both. Our findings highlight the importance of agglutinating antibodies in mucosal defense and reveal how successful pathogens evade this effect.

MeSH Terms
Agglutination/genetics,immunology Animals Antibodies, Monoclonal/metabolism Bacterial Proteins/genetics Cell Growth Processes/immunology Colony Count, Microbial Disease Models, Animal Humans Immune Evasion Immunoglobulin A/immunology,metabolism Immunoglobulin G/immunology,metabolism Mice Mice, Inbred C57BL Mutation/genetics Nasal Mucosa/immunology,microbiology Peptide Hydrolases/genetics Pneumococcal Infections/immunology,transmission Streptococcus pneumoniae/growth & development,physiology
Chemicals
Antibodies, Monoclonal Bacterial Proteins Immunoglobulin A Immunoglobulin G Peptide Hydrolases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Roche A M
Department of Microbiology, University of Pennsylvania, Philadelphia, Pennsylvania, USA.
Richard A L
Department of Microbiology, University of Pennsylvania, Philadelphia, Pennsylvania, USA.
Rahkola J T
1] Mucosal and Vaccine Research Program Colorado (MAVRC), Division of Infectious Disease, University of Colorado Denver, Aurora, Colorado, USA [2] Denver Veterans Affairs Medical Center, Denver, Colorado, USA.
Janoff E N
1] Mucosal and Vaccine Research Program Colorado (MAVRC), Division of Infectious Disease, University of Colorado Denver, Aurora, Colorado, USA [2] Denver Veterans Affairs Medical Center, Denver, Colorado, USA.
Weiser J N
Department of Microbiology, University of Pennsylvania, Philadelphia, Pennsylvania, USA.
References (31)
31 references, click to expand
  1. The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease.
    Nat Rev Microbiol. 2008 Apr;6(4):288-301 PMID: 18340341
  2. Decreased protective efficacy of reduced and alkylated human immune serum globulin in experimental infection with Haemophilus influenzae type b.
    Infect Immun. 1985 Jan;47(1):142-8 PMID: 3871195
  3. Antibody-enhanced pneumococcal adherence requires IgA1 protease.
    Proc Natl Acad Sci U S A. 2003 Apr 1;100(7):4215-20 PMID: 12642661
  4. 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
  5. Minimization of bacterial size allows for complement evasion and is overcome by the agglutinating effect of antibody.
    Cell Host Microbe. 2011 Nov 17;10(5):486-96 PMID: 22100164
  6. Structure and function relationships in IgA.
    Mucosal Immunol. 2011 Nov;4(6):590-7 PMID: 21937984
  7. Optimising the use of conjugate vaccines to prevent disease caused by Haemophilus influenzae type b, Neisseria meningitidis and Streptococcus pneumoniae.
    Vaccine. 2008 Aug 18;26(35):4434-45 PMID: 18617296
  8. Influenza A virus facilitates Streptococcus pneumoniae transmission and disease.
    FASEB J. 2010 Jun;24(6):1789-98 PMID: 20097876
  9. Cellular effectors mediating Th17-dependent clearance of pneumococcal colonization in mice.
    J Clin Invest. 2009 Jul;119(7):1899-909 PMID: 19509469
  10. A search for serologic correlates of immunity to Bordetella pertussis cough illnesses.
    Vaccine. 1998 Dec;16(20):1901-6 PMID: 9796041
  11. Anti-capsular polysaccharide antibody concentrations in saliva after immunization with Haemophilus influenzae type b conjugate vaccines.
    Pediatr Infect Dis J. 1995 Apr;14(4):286-94 PMID: 7603810
  12. Correlation of opsonophagocytosis and passive protection assays using human anticapsular antibodies in an infant mouse model of bacteremia for Streptococcus pneumoniae.
    J Infect Dis. 1999 Jul;180(1):133-40 PMID: 10353871
  13. Pneumococcal IgA1 protease subverts specific protection by human IgA1.
    Mucosal Immunol. 2014 Mar;7(2):249-56 PMID: 23820749
  14. Capsulation of pneumococcus with soluble cell wall-like polysaccharide. II. Nonidentity of cell wall and soluble cell wall-like polysaccharides derived from the same and from different pneumococcal strains.
    J Exp Med. 1971 Sep 1;134(3 Pt 1):600-17 PMID: 15776564
  15. Agglutinating secretory IgA preserves intestinal epithelial cell integrity during apical infection by Shigella flexneri.
    Infect Immun. 2013 Aug;81(8):3027-34 PMID: 23753631
  16. Primary antibody deficiencies.
    Nat Rev Immunol. 2013 Jul;13(7):519-33 PMID: 23765059
  17. Effect of immunoglobulin G (IgG) interchain disulfide bond cleavage on efficacy of intravenous immunoglobulin for immune thrombocytopenic purpura (ITP).
    Clin Exp Immunol. 2010 Dec;162(3):415-24 PMID: 21029072
  18. Complete genome sequence of a virulent isolate of Streptococcus pneumoniae.
    Science. 2001 Jul 20;293(5529):498-506 PMID: 11463916
  19. Changing epidemiology of invasive pneumococcal disease among older adults in the era of pediatric pneumococcal conjugate vaccine.
    JAMA. 2005 Oct 26;294(16):2043-51 PMID: 16249418
  20. Impact of the molecular form of immunoglobulin A on functional activity in defense against Streptococcus pneumoniae.
    Infect Immun. 2007 Apr;75(4):1801-10 PMID: 17261616
  21. Capsule enhances pneumococcal colonization by limiting mucus-mediated clearance.
    Infect Immun. 2007 Jan;75(1):83-90 PMID: 17088346
  22. U.S. hospitalizations for pneumonia after a decade of pneumococcal vaccination.
    N Engl J Med. 2013 Jul 11;369(2):155-63 PMID: 23841730
  23. 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
  24. Increased chain length promotes pneumococcal adherence and colonization.
    Infect Immun. 2012 Oct;80(10):3454-9 PMID: 22825449
  25. The atypical amino-terminal LPNTG-containing domain of the pneumococcal human IgA1-specific protease is required for proper enzyme localization and function.
    Mol Microbiol. 2006 Jul;61(2):526-43 PMID: 16776657
  26. Decline in invasive pneumococcal disease after the introduction of protein-polysaccharide conjugate vaccine.
    N Engl J Med. 2003 May 1;348(18):1737-46 PMID: 12724479
  27. STUDIES ON THE CHEMICAL NATURE OF THE SUBSTANCE INDUCING TRANSFORMATION OF PNEUMOCOCCAL TYPES : INDUCTION OF TRANSFORMATION BY A DESOXYRIBONUCLEIC ACID FRACTION ISOLATED FROM PNEUMOCOCCUS TYPE III.
    J Exp Med. 1944 Feb 1;79(2):137-58 PMID: 19871359
  28. The immune response to pneumococcal proteins during experimental human carriage.
    J Exp Med. 2002 Feb 4;195(3):359-65 PMID: 11828011
  29. Anti-capsular polysaccharide antibodies reduce nasopharyngeal colonization by Haemophilus influenzae type b in infant rats.
    J Infect Dis. 1993 Feb;167(2):365-71 PMID: 8421170
  30. Live attenuated Streptococcus pneumoniae strains induce serotype-independent mucosal and systemic protection in mice.
    Infect Immun. 2007 May;75(5):2469-75 PMID: 17339359
  31. Protection against infection with Pseudomonas aeruginosa by passive transfer of monoclonal antibodies to lipopolysaccharides and outer membrane proteins.
    J Infect Dis. 1984 Oct;150(4):570-6 PMID: 6436393
Article Info
Journal
Mucosal immunology
Abbr.
Mucosal Immunol
ISSN
1935-3456
Published
2015-01-00
Epub
2014-00-25
Pages
176-85
Language
English
Region
United States
NLM ID
101299742
PMCID
PMC4268183
Subset
IM
Grants
NIDDK NIH HHS · P30 DK050306 · United States
NIAID NIH HHS · R37 AI038446 · United States
NIAID NIH HHS · AI092468 · United States
NIAID NIH HHS · AI108479 · United States
NIAID NIH HHS · R01 AI105168 · United States
NIAID NIH HHS · AI05168 · United States
NIAID NIH HHS · R21 AI092468 · United States
NIDDK NIH HHS · P30-DK050306 · United States
NIAID NIH HHS · R01 AI108479 · United States
NIAID NIH HHS · AI38446 · United States
NIAID NIH HHS · R01 AI038446 · United States
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