Identification of an atypical zinc metalloproteinase, ZmpC, from an epidemic conjunctivitis-causing strain of Streptococcus pneumoniae

Microbial Pathogenesis

Volumn 56, Issue , 2013, Pages 40-46

  Menon, Balaraj B ^a   Govindarajan, Bharathi ^a  

^a SCHEPENS EYE RESEARCH INSTITUTE   (United States)

Author keywords

Bacterial conjunctivitis; Mucins; Streptococcus pneumoniae; Zinc metalloproteinases

Indexed keywords

ALANINE; BACTERIAL DNA; MEMBRANE PROTEIN; METALLOPROTEINASE; MUCIN; MUCIN 16; RECOMBINANT ENZYME; UNCLASSIFIED DRUG; ZINC METALLOPROTEINASE;

5' UNTRANSLATED REGION; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CONJUNCTIVITIS; CONTROLLED STUDY; CORNEA EPITHELIUM; ENZYME ANALYSIS; EPITHELIUM CELL; GENE DELETION; GLYCOCALYX; GRAM POSITIVE BACTERIUM; HUMAN; HUMAN CELL; IN VITRO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PERMEABILITY BARRIER; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN STRUCTURE; SEQUENCE ANALYSIS; SEROTYPE; STREPTOCOCCUS PNEUMONIAE; ZMPC GENE;

CA-125 ANTIGEN; CONJUNCTIVITIS; DNA, BACTERIAL; EPIDEMICS; HYDROLYSIS; MEMBRANE PROTEINS; METALLOENDOPEPTIDASES; MOLECULAR SEQUENCE DATA; PNEUMOCOCCAL INFECTIONS; SEQUENCE ANALYSIS, DNA; SEQUENCE DELETION; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); POSIBACTERIA; STREPTOCOCCUS PNEUMONIAE;

EID: 84873744690     PISSN: 08824010     EISSN: 10961208     Source Type: Journal    
DOI: 10.1016/j.micpath.2012.11.006     Document Type: Article

References (39)

1. AlonsoDeVelasco E., Verheul A.F., Verhoef J., Snippe H. Streptococcus pneumoniae: virulence factors, pathogenesis, and vaccines. Microbiological Reviews 1995, 59:591-603.
2. Kadioglu A., Weiser J.N., Paton J.C., Andrew P.W. The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Nature Reviews Microbiology 2008, 6:288-301.
3. Mitchell A.M., Mitchell T.J. Streptococcus pneumoniae: virulence factors and variation. Clinical Microbiology and Infection 2010, 16:411-418.
4. Martin M., Turco J.H., Zegans M.E., Facklam R.R., Sodha S., Elliott J.A., et al. An outbreak of conjunctivitis due to atypical Streptococcus pneumoniae. New England Journal of Medicine 2003, 348:1112-1121.
5. Barker J.H., Musher D.M., Silberman R., Phan H.M., Watson D.A. Genetic relatedness among nontypeable pneumococci implicated in sporadic cases of conjunctivitis. Journal of Clinical Microbiology 1999, 37:4039-4041.
6. Talbot U.M., Paton A.W., Paton J.C. Uptake of Streptococcus pneumoniae by respiratory epithelial cells. Infection and Immunity 1996, 64:3772-3777.
7. Williamson Y.M., Gowrisankar R., Longo D.L., Facklam R., Gipson I.K., Ades E.P., et al. Adherence of nontypeable Streptococcus pneumoniae to human conjunctival epithelial cells. Microbial Pathogenesis 2008, 44:175-185.
8. Zhang J.-R., Mostov K.E., Lamm M.E., Nanno M., Shimida S.-I., Ohwaki M., et al. The polymeric immunoglobulin receptor translocates pneumococci across human nasopharyngeal epithelial cells. Cell 2000, 102:827-837.
9. Rosenow C., Ryan P., Weiser J.N., Johnson S., Fontan P., Ortqvist A., et al. Contribution of novel choline-binding proteins to adherence, colonization and immunogenicity of Streptococcus pneumoniae. Molecular Microbiology 1997, 25:819-829.
10. King S.J., Hippe K.R., Weiser J.N. Deglycosylation of human glycoconjugates by the sequential activities of exoglycosidases expressed by Streptococcus pneumoniae. Molecular Microbiology 2006, 59:961-974.
11. Bergmann S., Hammerschmidt S. Versatility of pneumococcal surface proteins. Microbiology 2006, 152:295-303.
12. Pracht D., Elm C., Gerber J., Bergmann S., Rohde M., Seiler M., et al. PavA of Streptococcus pneumoniae modulates adherence, invasion, and meningeal inflammation. Infection and Immunity 2005, 73:2680-2689.
13. Bergmann S., Rohde M., Chhatwal G.S., Hammerschmidt S. α-Enolase of Streptococcus pneumoniae is a plasmin(ogen)-binding protein displayed on the bacterial cell surface. Molecular Microbiology 2001, 40:1273-1287.
14. Barocchi M.A., Ries J., Zogaj X., Hemsley C., Albiger B., Kanth A., et al. A pneumococcal pilus influences virulence and host inflammatory responses. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:2857-2862.
15. Bagnoli F., Moschioni M., Donati C., Dimitrovska V., Ferlenghi I., Facciotti C., et al. A second pilus type in Streptococcus pneumoniae is prevalent in emerging serotypes and mediates adhesion to host cells. Journal of Bacteriology 2008, 190:5480-5492.
16. Hilleringmann M., Giusti F., Baudner B.C., Masignani V., Covacci A., Rappuoli R., et al. Pneumococcal Pili are composed of protofilaments exposing adhesive clusters of Rrg A. PLoS Pathogens 2008, 4:e1000026.
17. Linden S.K., Sutton P., Karlsson N.G., Korolik V., McGuckin M.A. Mucins in the mucosal barrier to infection. Mucosal Immunology 2008, 1:183-197.
18. DeSouza M.M., Gulnar A.S., Roger E.P., JoAnne J., Rachele K., Xinhui Z., et al. MUC1/episialin: a critical barrier in the female reproductive tract. Journal of Reproductive Immunology 2000, 45:127-158.
19. McGuckin M.A., Every A.L., Skene C.D., Linden S.K., Chionh Y.T., Swierczak A., et al. Muc1 mucin limits both Helicobacter pylori colonization of the murine gastric mucosa and associated gastritis. Gastroenterology 2007, 133:1210-1218.
20. McAuley J.L., Linden S.K., Png C.W., King R.M., Pennington H.L., Gendler S.J., et al. MUC1 cell surface mucin is a critical element of the mucosal barrier to infection. Journal of Clinical Investigation 2007, 117:2313-2324.
21. Blalock T.D., Spurr-Michaud S.J., Tisdale A.S., Heimer S.R., Gilmore M.S., Ramesh V., et al. Functions of MUC16 in corneal epithelial cells. Investigative Ophthalmology & Visual Science 2007, 48:4509-4518.
22. Govindarajan B., Menon B.B., Spurr-Michaud S., Rastogi K., Gilmore M.S., Argüeso P., et al. A metalloproteinase secreted by Streptococcus pneumoniae removes membrane mucin MUC16 from the epithelial glycocalyx barrier. PLoS One 2012, 7:e32418.
23. Gipson I.K., Spurr-Michaud S., Argueso P., Tisdale A., Ng T.F., Russo C.L. Mucin gene expression in immortalized human corneal-limbal and conjunctival epithelial cell lines. Investigative Ophthalmology & Visual Science 2003, 44:2496-2506.
24. Blalock T.D., Spurr-Michaud S.J., Tisdale A.S., Gipson I.K. Release of membrane-associated mucins from ocular surface epithelia. Investigative Ophthalmology & Visual Science 2008, 49:1864-1871.
25. Nustad K., Bast R.C., Brien T.J., Nilsson O., Seguin P., Suresh M.R., et al. Specificity and affinity of 26 monoclonal antibodies against the CA 125 antigen: first report from the ISOBM TD-1 workshop. international society for oncodevelopmental biology and medicine. Tumour Biology 1996, 17:196-219.
26. Oggioni M.R., Memmi G., Maggi T., Chiavolini D., Iannelli F., Pozzi G. Pneumococcal zinc metalloproteinase ZmpC cleaves human matrix metalloproteinase 9 and is a virulence factor in experimental pneumonia. Molecular Microbiology 2003, 49:795-805.
27. Chen Y., Hayashida A., Bennett A.E., Hollingshead S.K., Park P.W. Streptococcus pneumoniae sheds syndecan-1 ectodomains through ZmpC, a metalloproteinase virulence factor. Journal of Biological Chemistry 2007, 282:159-167.
28. Camilli R., Pettini E., Grosso M.D., Pozzi G., Pantosti A., Oggioni M.R. Zinc metalloproteinase genes in clinical isolates of Streptococcus pneumoniae: association of the full array with a clonal cluster comprising serotypes 8 and 11A. Microbiology 2006, 152:313-321.
29. Poulsen K., Reinholdt J., Kilian M. Characterization of the Streptococcus pneumoniae immunoglobulin A1 protease gene (iga) and its translation product. Infection and Immunity 1996, 64:3957-3966.
30. Weiser J., Bae D., Fasching C., Scamurra R., Ratner A., Janoff E. Antibody-enhanced pneumococcal adherence requires IgA1 protease. Proceedings of the National Academy of Sciences USA 2003, 100:4215-4220.
31. Blue C.E., Paterson G.K., Kerr A.R., Bergé M., Claverys J.P., Mitchell T.J. ZmpB, a novel virulence factor of Streptococcus pneumoniae that induces tumor necrosis factor alpha production in the respiratory tract. Infection and Immunity 2003, 71:4925-4935.
32. Hsieh Y.-C., Tsao P.-N., Chen C.-L., Lin T.-L., Lee W.-S., Shao P.-L., et al. Establishment of a young mouse model and identification of an allelic variation of zmpB in complicated pneumonia caused by Streptococcus pneumoniae. Critical Care Medicine 2008, 36:1248-1255.
33. Bergé M., García P., Iannelli F., Prère M.F., Granadel C., Polissi A., et al. The puzzle of zmpB and extensive chain formation, autolysis defect and non-translocation of choline-binding proteins in Streptococcus pneumoniae. Molecular Microbiology 2001, 39:1651-1660.
34. Chiavolini D., Memmi G., Maggi T., Iannelli F., Pozzi G., Oggioni M. The three extra-cellular zinc metalloproteinases of Streptococcus pneumoniae have a different impact on virulence in mice. BMC Microbiology 2003, 3:14.
35. Camilli R., Bonnal R., Del Grosso M., Iacono M., Corti G., Rizzi E., et al. Complete genome sequence of a serotype 11A, ST62 Streptococcus pneumoniae invasive isolate. BMC Microbiology 2011, 11:25.
36. Novick R.P. Sortase: the surface protein anchoring transpeptidase and the LPXTG motif. Trends in Microbiology 2000, 8:148-151.
37. Ton-That H., Liu G., Mazmanian S.K., Faull K.F., Schneewind O. Purification and characterization of sortase, the transpeptidase that cleaves surface proteins of Staphylococcus aureus at the LPXTG motif. Proceedings of the National Academy of Sciences 1999, 96:12424-12429.
38. Bender M.H., Weiser J.N. The atypical amino-terminal LPNTG-containing domain of the pneumococcal human IgA1-specific protease is required for proper enzyme localization and function. Molecular Microbiology 2006, 61:526-543.
39. Reinholdt J., Kilian M. Comparative analysis of immunoglobulin A1 protease activity among bacteria representing different genera, species, and strains. Infection and Immunity 1997, 65:4452-4459.