Skip to content Skip to navigation
University of Warwick
  • Study
  • |
  • Research
  • |
  • Business
  • |
  • Alumni
  • |
  • News
  • |
  • About

University of Warwick
Publications service & WRAP

Highlight your research

  • WRAP
    • Home
    • Search WRAP
    • Browse by Warwick Author
    • Browse WRAP by Year
    • Browse WRAP by Subject
    • Browse WRAP by Department
    • Browse WRAP by Funder
    • Browse Theses by Department
  • Publications Service
    • Home
    • Search Publications Service
    • Browse by Warwick Author
    • Browse Publications service by Year
    • Browse Publications service by Subject
    • Browse Publications service by Department
    • Browse Publications service by Funder
  • Statistics
  • Help & Advice
University of Warwick

The Library

  • Login

Nod1 signaling overcomes resistance of S. pneumoniae to opsonophagocytic killing

Tools
- Tools
+ Tools

Lysenko, Elena S., Clarke, Thomas B., Shchepetov, Mikhail, Ratner, Adam J., Roper, David I., Dowson, Christopher G. and Weiser, Jeffrey N.. (2007) Nod1 signaling overcomes resistance of S. pneumoniae to opsonophagocytic killing. PL o S Pathogens , Vol.3 (No.8). pp. 1073-1081. ISSN 1553-7366

[img]
Preview
PDF
WRAP_Dowson_Nod!_signaling.pdf - Requires a PDF viewer such as GSview, Xpdf or Adobe Acrobat Reader

Download (456Kb)
Official URL: http://dx.doi.org/10.1371/journal.ppat.0030118

Abstract

Airway infection by the Gram-positive pathogen Streptococcus pneumoniae (Sp) leads to recruitment of neutrophils but limited bacterial killing by these cells. Co-colonization by Sp and a Gram-negative species, Haemophilus influenzae (Hi), provides sufficient stimulus to induce neutrophil and complement-mediated clearance of Sp from the mucosal surface in a murine model. Products from Hi, but not Sp, also promote killing of Sp by ex vivo neutrophil-enriched peritoneal exudate cells. Here we identify the stimulus from Hi as its peptidoglycan. Enhancement of opsonophagocytic killing was facilitated by signaling through nucleotide-binding oligomerization domain-1 (Nod1), which is involved in recognition of γ-D-glutamyl-meso-diaminopimelic acid (meso-DAP) contained in cell walls of Hi but not Sp. Neutrophils from mice treated with Hi or compounds containing meso-DAP, including synthetic peptidoglycan fragments, showed increased Sp killing in a Nod1-dependent manner. Moreover, Nod1-/- mice showed reduced Hi-induced clearance of Sp during co-colonization. These observations offer insight into mechanisms of microbial competition and demonstrate the importance of Nod1 in neutrophil-mediated clearance of bacteria in vivo.

Item Type: Journal Article
Subjects: Q Science > QR Microbiology
Divisions: Faculty of Science > Life Sciences (2010- ) > Biological Sciences ( -2010)
Library of Congress Subject Headings (LCSH): Streptococcus pneumoniae, Neutrophils -- Immunology, Inflammation -- Immunological aspects, Haemophilus influenzae
Journal or Publication Title: PL o S Pathogens
Publisher: Public Library of Science
ISSN: 1553-7366
Date: 24 August 2007
Volume: Vol.3
Number: No.8
Page Range: pp. 1073-1081
Identification Number: 10.1371/journal.ppat.0030118
Status: Peer Reviewed
Access rights to Published version: Open Access
Funder: Biotechnology and Biological Sciences Research Council (Great Britain) (BBSRC), United States. Public Health Service (PHS), University of Pennsylvania. School of Medicine, Pediatric Infectious Diseases Society, St. Jude Children's Research Hospital
Grant number: AI44231 (PHS), AI05467 (PHS), AI38446 (PHS), AI065450 (PHS), P30 DK50306 (Penn)
References: 1. Kadioglu A, Gingles N, Grattan K, Kerr A, Mitchell T, et al. (2000) Host cellular immune response to pneumococcal lung infection in mice. Infect Immun 68: 492–501. 2. Perry F, Elson C, Greenham L, Catterall J (1993) Interference with the oxidative response of neutrophils by Streptococcus pneumoniae. Thorax 48: 364–369. 3. World Health Organization (1999) Pneumococcal vaccines. WHO position paper. Wkly Epidemiol Rec 74: 177–183. 4. Marks M, Burns T, Abadi M, Seyoum B, Thornton J, et al. (2007) The influence of neutropenia on the course of serotype 8 pneumococcal pneumonia in mice. Infect Immun 75: 1586–1597. 5. van Rossum A, Lysenko E, Weiser J (2005) Host and bacterial factors contributing to the clearance of colonization by Streptococcus pneumoniae in a murine model. Infect Immun 73: 7718–7726. 6. Lysenko E, Ratner A, Nelson A, Weiser J (2005) The role of innate immune responses in the outcome of interspecies competition for colonization of mucosal surfaces. PLoS Pathog 1: e1. doi:10.1371/journal.ppat.0010001 7. Inohara N, Chamaillard M, McDonald C, Nun˜ ez G (2005) NOD-LRR proteins: Role in host-microbial interactions and inflammatory disease. Annu Rev Biochem 74: 355–383. 8. Burroughs M, Rozdzinski E, Geelen S, Tuomanen E (1993) A structureactivity relationship for induction of meningeal inflammation by muramyl peptides. J Clin Invest 92: 297–302. 9. Girardin S, Boneca I, Carneiro L, Antignac A, Jehanno M, et al. (2003) Nod1 detects a unique muropeptide from gram-negative bacterial peptidoglycan. Science 300: 1584–1587. 10. Chamaillard M, Hashimoto M, Horie Y, Masumoto J, Qiu S, et al. (2003) An essential role for NOD1 in host recognition of bacterial peptidoglycan containing diaminopimelic acid. Nat Immunol 4: 702–707. 11. Garcia-Bustos J, Chait B, Tomasz A (1987) Structure of the peptide network of pneumococcal peptidoglycan. J Biol Chem 262: 15400–15405. 12. Girardin S, Boneca I, Viala J, Chamaillard M, Labigne A, et al. (2003) Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J Biol Chem 278: 8869–8872. 13. Hestdal K, Ruscetti F, Ihle J, Jacobsen S, Dubois C, et al. (1991) Characterization and regulation of RB6-8C5 antigen expression on murine bone marrow cells. J Immunol 147: 22–28. 14. Shuto T, Xu H, Wang B, Han J, Kai H, et al. (2001) Activation of NK-kappa B by nontypeable Haemophilus influenzae is mediated by toll-like receptor 2- TAK1-dependent NIK-IKK alpha/beta-I kappa B alpha and MKK3/6-p38 MAP kinase signaling pathways in epithelial cells. Proc Natl Acad Sci U S A 98: 8774–8779. 15. Wang X, Moser C, Louboutin J, Lysenko E, Weiner D, et al. (2002) Toll-like receptor 4 mediates innate immune responses to Haemophilus influenzae infection in mouse lung. J Immunol 168: 810–815. 16. Swords W, Ketterer M, Shao J, Campbell C, Weiser J, Apicella M (2001) Binding of the non-typeable Haemophilus influenzae lipooligosaccharide to the PAF receptor initiates host cell signalling. Cell Microbiol 3: 525–536. 17. Lysenko E, Richards J, Cox A, Stewart A, Martin A, et al. (2000) The position of phosphorylcholine on the lipopolysaccharide of Haemophilus influenzae affects binding and sensitivity to C-reactive protein mediated killing. Mol Microbiol 35: 234–245. 18. El Zoeiby A, Sanschagrin F, Havugimana P, Garnier A, Levesque R (2001) In vitro reconstruction of the biosynthetic pathway of peptidoglycan cytoplasmic precursor in Pseudomonas aeruginosa. FEMS Microbiol Lett 201: 229–235. 19. Fritz J, Ferrero R, Philpott D, Girardin S (2006) Nod-like proteins in immunity, inflammation and disease. Nat Immunol 7: 1250–1257. 20. Ratner A, Lysenko E, Paul M, Weiser J (2005) Synergistic proinflammatory responses induced by polymicrobial colonization of epithelial surfaces. Proc Natl Acad Sci U S A 102: 3429–3434. 21. Boneca I, Dussurget O, Cabanes D, Nahori M, Sousa S, et al. (2007) A critical role for peptidoglycan N-deacetylation in Listeria evasion from the host innate immune system. Proc Natl Acad Sci U S A 104: 997–1002. 22. Wolfert MA, Roychowdhury A, Boons GJ (2007) Modification of the structure of peptidoglycan is a strategy to avoid detection by nucleotidebinding oligomerization domain protein 1. Infect Immun 75: 706–713. 23. Weiser J, Nahm M (2007) Immunity to extracellular bacteria. In: Paul WE, editor. Fundamental immunology. Baltimore: Lippincott, Williams and Wilkins. In press. 24. Ratner A, Aguilar J, Shchepetov M, Lysenko E, Weiser J (2007) Nod1 mediates cytoplasmic sensing of combinations of extracellular bacteria. Cell Microbiol 9: 1343–1351. 25. Viala J, Chaput C, Boneca I, Cardona A, Girardin S, et al. (2004) Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nat Immunol 5: 1166–1174. 26. Vollmer W, Tomasz A (2002) Peptidoglycan N-acetylglucosamine deacetylase, a putative virulence factor in Streptococcus pneumoniae. Infect Immun 70: 7176–7178. 27. Crisostomo M, Vollmer W, Kharat A, Inhulsen S, Gehre F, et al. (2006) Attenuation of penicillin resistance in a peptidoglycan O-acetyl transferase mutant of Streptococcus pneumoniae. Mol Microbiol 61: 1497–1509. 28. Mine Y, Watanabe Y, Tawara S, Yokota Y, Nishida M, et al. (1983) Immunoactive peptides, FK-156 and FK-565. III. Enhancement of host defense mechanisms against infection. J Antibiot 36: 1059–1066. 29. Todd RF (1996) The continuing saga of complement receptor type 3 (CR3). J Clin Invest 98: 1–2. 30. Masumoto J, Yang K, Varambally S, Hasegawa M, Tomlins S, et al. (2006) Nod1 acts as an intracellular receptor to stimulate chemokine production and neutrophil recruitment in vivo. J Exp Med 203: 203–213. 31. Beiter K, Wartha F, Albiger B, Normark S, Zychlinsky A, et al. (2006) An endonuclease allows Streptococcus pneumoniae to escape from neutrophil extracellular traps. Curr Biol 16: 401–407. 32. Opitz B, Puschel A, Schmeck B, Hocke A, Rosseau S, et al. (2004) Nucleotide-binding oligomerization domain proteins are innate immune receptors for internalized Streptococcus pneumoniae. J Biol Chem 279: 36426– 36432. 33. Gould J, Weiser J (2002) The inhibitory effect of C-reactive protein on bacterial phosphorylcholine-platelet activating factor receptor mediated adherence is blocked by surfactant. J Infect Dis 186: 361–371. 34. McCool T, Cate T, Moy G, Weiser J (2002) The immune response to pneumococcal proteins during experimental human carriage. J Exp Med 195: 359–365. 35. Coxon A, Rieu P, Barkalow F, Askari S, Sharpe A, et al. (1996) A novel role for the beta 2 integrin CD11b/CD18 in neutrophil apoptosis: A homeostatic mechanism in inflammation. Immunity 5: 653–666. 36. Wooten RM, Ma Y, Yoder RA, Brown JP, Weis JH, et al. (2002) Toll-like receptor 2 is required for innate, but not acquired, host defense to Borrelia burgdorferi. J Immunol 168: 348–355. 37. Lubinski JM, Wang L, Soulika AM, Burger R, Wetsel RA, et al. (1998) Herpes simplex virus type 1 glycoprotein gC mediates immune evasion in vivo. J Virol 72: 8257–8263. 38. Matsumoto M, Fukuda W, Circolo A, Goellner J, Strauss-Schoenberger J, et al. (1997) Abrogation of the alternative complement pathway by targeted deletion of murine factor B. Proc Natl Acad Sci U S A 94: 8720–8725. 39. Poltorak A, He X, Smirnova I, Liu M, Van Huffel C, et al. (1998) Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: Mutations in Tlr4 gene. Science 282: 2085–2088. 40. Luo Y, Dorf M (1997) Isolation of mouse neutrophils. In: Current protocols in immunology. New York: John Wiley & Sons. p. 3.20.1. 41. Westphal O, Jann K (1965) Bacterial lipopolysaccharides: Extraction with phenol-water and further applications of the procedure. Methods Carbohydr Chem 5: 83–91. 42. Burroughs M, Chang Y, Gage D, Tuomanen E (1993) Composition of the peptidoglycan of Haemophilus influenzae. J Biol Chem 268: 11594–11598. 43. de Jonge B, Chang Y, Gage D, Tomasz A (1992) Peptidoglycan composition of a highly methicillin-resistant Staphylococcus aureus strain. The role of penicillin binding protein 2A. J Biol Chem 267: 11248–11254. 44. Sieradzki K, Tomasz A (2003) Alterations of cell wall structure and metabolism accompany reduced susceptibility to vancomycin in an isogenic series of clinical isolates of Staphylococcus aureus. J Bacteriol 185: 7103–7110. 45. Totemeyer S, Sheppard M, Lloyd A, Roper D, Dowson C, et al. (2006) IFNgamma enhances production of nitric oxide from macrophages via a mechanism that depends on nucleotide oligomerization domain-2. J Immunol 176: 4804–4810. 46. Reddy S, Waddell S, Kuo D, Wong K, Pompliano D (1999) Preparative enzymatic synthesis and characterization of the cytoplasmic intermediates of murein biosynthesis. J Am Chem Soc 121: 1175–1178. 47. Nelson AL, Roche AM, Gould JM, Chim K, Ratner AJ, Weiser JN (2007) Capsule enhances pneumococcal colonization by limiting mucus-mediated clearance. Infect Immun 75: 83–90.
URI: http://wrap.warwick.ac.uk/id/eprint/4437

Request changes to a record

Actions (login required)

View Item View Item

Document Downloads

More statistics for this item...
twitter

Email us: publications@warwick.ac.uk
Contact Details
About Us