Streptococcus pneumoniae Endopeptidase O (PepO) is a multifunctional plasminogen-and fibronectin-binding protein, facilitating evasion of innate immunity and invasion of host cells

Journal of Biological Chemistry

Volumn 288, Issue 10, 2013, Pages 6849-6863

  Agarwal, Vaibhav ^a,b   Kuchipudi, Arunakar ^a,b   Fulde, Marcus ^b,c   Riesbeck, Kristian ^a,d   Bergmann, Simone ^a,e   Blom, Anna M ^a,b  

^a Department of Medicine   (Sweden)

^b Medical Protein Chemistry   (Sweden)

^c LUND UNIVERSITY   (Sweden)

^d HANNOVER MEDICAL SCHOOL   (Germany)

^e TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRONECTIN BINDINGS; FIBRONECTIN-BINDING PROTEIN; HOST CELLS; HOST PROTEINS; HOST-CELL INVASION; INNATE IMMUNITY; MULTIPLE STRATEGY; STREPTOCOCCUS PNEUMONIAE;

PROTEINS;

IMMUNE SYSTEM;

BACTERIAL PROTEIN; COMPLEMENT COMPONENT C3B; ENDOPEPTIDASE O; FIBRONECTIN; LYSINE; PLASMINOGEN; UNCLASSIFIED DRUG; UROKINASE;

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM ISOLATE; BINDING AFFINITY; BINDING ASSAY; BINDING SITE; CELL ADHESION; CELL INVASION; CONTROLLED STUDY; ENDOPEPTIDASE O GENE; ENDOTHELIUM CELL; FLOW CYTOMETRY; GENE FUNCTION; HOST CELL; HUMAN; HUMAN CELL; INNATE IMMUNITY; IONIC STRENGTH; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; RESIDUE ANALYSIS; SEQUENCE ANALYSIS; STREPTOCOCCUS PNEUMONIAE;

BACTERIAL ADHESION; BACTERIAL PROTEINS; BLOTTING, WESTERN; CELL LINE, TUMOR; CELLS, CULTURED; COMPLEMENT C3B; ENDOPEPTIDASES; EPITHELIAL CELLS; FIBRINOLYSIN; FIBRONECTINS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; IMMUNE EVASION; IMMUNITY, INNATE; MICROSCOPY, CONFOCAL; MUTATION; PLASMINOGEN; PROTEIN BINDING; STREPTOCOCCUS PNEUMONIAE; UROKINASE-TYPE PLASMINOGEN ACTIVATOR;

EID: 84874911012     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.405530     Document Type: Article

References (52)

1. Cartwright, K. (2002) Pneumococcal disease in Western Europe. Burden of disease, antibiotic resistance and management. Eur. J. Pediatr. 161, 188-195 (Pubitemid 34253335)
2. File, T. M. (2003) Community-acquired pneumonia. Lancet 362, 1991-2001
3. O'Brien, K. L., Wolfson, L. J., Watt, J. P., Henkle, E., Deloria-Knoll, M., McCall, N., Lee, E., Mulholland, K., Levine, O. S., and Cherian, T. (2009) Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years. Global estimates. Lancet 374, 893-902
4. Bergmann, S., and Hammerschmidt, S. (2006) Versatility of pneumococcal surface proteins. Microbiology 152, 295-303 (Pubitemid 43210660)
5. Kadioglu, A., Weiser, J. N., Paton, J. C., and Andrew, P. W. (2008) The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Nat. Rev. Microbiol. 6, 288-301 (Pubitemid 351404773)
6. Mitchell, A. M., and Mitchell, T. J. (2010) Streptococcus pneumoniae. Virulence factors and variation. Clin. Microbiol. Infect. 16, 411-418
7. Frolet, C., Beniazza, M., Roux, L., Gallet, B., Noirclerc-Savoye, M., Vernet, T., and Di Guilmi, A. M. (2010) New adhesin functions of surface-exposed pneumococcal proteins. BMC Microbiol. 10, 190
8. Hammerschmidt, S. (2006) Adherence molecules of pathogenic pneumococci. Curr. Opin. Microbiol. 9, 12-20 (Pubitemid 43184332)
9. Löfling, J., Vimberg, V., Battig, P., and Henriques-Normark, B. (2011) Cellular interactions by LPxTG-anchored pneumococcal adhesins and their streptococcal homologues. Cell Microbiol. 13, 186-197
10. Elm, C., Braathen, R., Bergmann, S., Frank, R., Vaerman, J. P., Kaetzel, C. S., Chhatwal, G. S., Johansen, F. E., and Hammerschmidt, S. (2004) Ectodomains 3 and 4 of human polymeric Immunoglobulin receptor (hpIgR) mediate invasion of Streptococcus pneumoniae into the epithelium. J. Biol. Chem. 279, 6296-6304 (Pubitemid 38248762)
11. Hammerschmidt, S., Talay, S. R., Brandtzaeg, P., and Chhatwal, G. S. (1997) SpsA, a novel pneumococcal surface protein with specific binding to secretory immunoglobulin A and secretory component. Mol. Microbiol. 25, 1113-1124 (Pubitemid 27410190)
12. Zhang, J. R., Mostov, K. E., Lamm, M. E., Nanno, M., Shimida, S., Ohwaki, M., and Tuomanen, E. (2000) The polymeric immunoglobulin receptor translocates pneumococci across human nasopharyngeal epithelial cells. Cell 102, 827-837
13. Anderton, J. M., Rajam, G., Romero-Steiner, S., Summer, S., Kowalczyk, A. P., Carlone, G. M., Sampson, J. S., and Ades, E. W. (2007) E-cadherin is a receptor for the common protein pneumococcal surface adhesin A (PsaA) of Streptococcus pneumoniae. Microb. Pathog. 42, 225-236 (Pubitemid 46661895)
14. Rose, L., Shivshankar, P., Hinojosa, E., Rodriguez, A., Sanchez, C. J., and Orihuela, C. J. (2008) Antibodies against PsrP, a novel Streptococcus pneumoniae adhesin, block adhesion and protect mice against pneumococcal challenge. J. Infect. Dis. 198, 375-383
15. Shivshankar, P., Sanchez, C., Rose, L. F., and Orihuela, C. J. (2009) The Streptococcus pneumoniae adhesin PsrP binds to Keratin 10 on lung cells. Mol. Microbiol. 73, 663-679
16. Bagnoli, F., Moschioni, M., Donati, C., Dimitrovska, V., Ferlenghi, I., Facciotti, C., Muzzi, A., Giusti, F., Emolo, C., Sinisi, A., Hilleringmann, M., Pansegrau, W., Censini, S., Rappuoli, R., Covacci, A., Masignani, V., and Barocchi, M. A. (2008)Asecond pilus type in Streptococcus pneumoniae is prevalent in emerging serotypes and mediates adhesion to host cells. J. Bacteriol. 190, 5480-5492
17. Barocchi, M. A., Ries, J., Zogaj, X., Hemsley, C., Albiger, B., Kanth, A., Dahlberg, S., Fernebro, J., Moschioni, M., Masignani, V., Hultenby, K., Taddei, A. R., Beiter, K., Wartha, F., von Euler, A., Covacci, A., Holden, D. W., Normark, S., Rappuoli, R., and Henriques-Normark, B. (2006) A pneumococcal pilus influences virulence and host inflammatory responses. Proc. Natl. Acad. Sci. U.S.A. 103, 2857-2862
18. Lähteenmäki, K., Kuusela, P., and Korhonen, T. K. (2001) Bacterial plasminogen activators and receptors. FEMS Microbiol. Rev. 25, 531-552 (Pubitemid 34019193)
19. Talay, S. R. (2005) Gram-positive adhesins. Contrib. Microbiol. 12, 90-113
20. Holmes, A. R., McNab, R., Millsap, K. W., Rohde, M., Hammerschmidt, S., Mawdsley, J. L., and Jenkinson, H. F. (2001) The pavA gene of Streptococcus pneumoniae encodes a fibronectin-binding protein that is essential for virulence. Mol. Microbiol. 41, 1395-1408 (Pubitemid 32939510)
21. Jensch, I., Gámez, G., Rothe, M., Ebert, S., Fulde, M., Somplatzki, D., Bergmann, S., Petruschka, L., Rohde, M., Nau, R., and Hammerschmidt, S. (2010) PavB is a surface-exposed adhesin of Streptococcus pneumoniae contributing to nasopharyngeal colonization and airways infections. Mol. Microbiol. 77, 22-43
22. Papasergi, S., Garibaldi, M., Tuscano, G., Signorino, G., Ricci, S., Peppoloni, S., Pernice, I., Lo Passo, C., Teti, G., Felici, F., and Beninati, C. (2010) Plasminogen-and fibronectin-binding protein B is involved in the adherence of Streptococcus pneumoniae to human epithelial cells. J. Biol. Chem. 285, 7517-7524
23. Pracht, D., Elm, C., Gerber, J., Bergmann, S., Rohde, M., Seiler, M., Kim, K. S., Jenkinson, H. F., Nau, R., and Hammerschmidt, S. (2005) PavA of Streptococcus pneumoniae modulates adherence, invasion, and meningeal inflammation. Infect. Immun. 73, 2680-2689 (Pubitemid 40570332)
24. Yamaguchi, M., Terao, Y., Mori, Y., Hamada, S., and Kawabata, S. (2008) PfbA, a novel plasmin-and fibronectin-binding protein of Streptococcus pneumoniae, contributes to fibronectin-dependent adhesion and antiphagocytosis. J. Biol. Chem. 283, 36272-36279
25. Singh, P., Carraher, C., and Schwarzbauer, J. E. (2010) Assembly of fibronectin extracellular matrix. Annu. Rev. Cell Dev. Biol. 26, 397-419
26. Schwarz-Linek, U., Höök, M., and Potts, J. R. (2004) The molecular basis of fibronectin-mediated bacterial adherence to host cells. Mol. Microbiol. 52, 631-641 (Pubitemid 38621735)
27. Collen, D., and Verstraete, M. (1975) Molecular biology of human plasminogen. II. Metabolism in physiological and some pathological conditions in man. Thromb. Diath. Haemorrh. 34, 403-408
28. Saksela, O., and Rifkin, D. B. (1988) Cell-associated plasminogen activation. Regulation and physiological functions. Annu. Rev. Cell Biol. 4, 93-126 (Pubitemid 19139253)
29. Vassalli, J. D., Sappino, A. P., and Belin, D. (1991) The plasminogen activator/ plasmin system. J. Clin. Invest. 88, 1067-1072
30. Bergmann, S., Rohde, M., Chhatwal, G. S., and Hammerschmidt, S. (2001) α-Enolase of Streptococcus pneumoniae is a plasmin(ogen)-binding protein displayed on the bacterial cell surface. Mol. Microbiol. 40, 1273-1287 (Pubitemid 32635298)
31. Bergmann, S., Rohde, M., and Hammerschmidt, S. (2004) Glyceraldehyde-3-phosphate dehydrogenase of Streptococcus pneumoniae is a surface-displayed plasminogen-binding protein. Infect. Immun. 72, 2416-2419 (Pubitemid 38419963)
32. Agarwal, V., Asmat, T. M., Luo, S., Jensch, I., Zipfel, P. F., and Hammerschmidt, S. (2010) Complement regulator Factor H mediates a two-step uptake of Streptococcus pneumoniae by human cells. J. Biol. Chem. 285, 23486-23495
33. Bergmann, S., Lang, A., Rohde, M., Agarwal, V., Rennemeier, C., Grashoff, C., Preissner, K. T., and Hammerschmidt, S. (2009) Integrin-linked kinase is required for vitronectin-mediated internalization of Streptococcus pneumoniae by host cells. J. Cell Sci. 122, 256-267
34. Hammerschmidt, S., Agarwal, V., Kunert, A., Haelbich, S., Skerka, C., and Zipfel, P. F. (2007) The host immune regulator factor H interacts via two contact sites with the PspC protein of Streptococcus pneumoniae and mediates adhesion to host epithelial cells. J. Immunol. 178, 5848-5858 (Pubitemid 46674382)
35. Rennemeier, C., Hammerschmidt, S., Niemann, S., Inamura, S., Zähringer, U., and Kehrel, B. E. (2007) Thrombospondin-1 promotes cellular adherence of Gram-positive pathogens via recognition of peptidoglycan. FASEB J. 21, 3118-3132 (Pubitemid 47565532)
36. Agarwal, V., and Hammerschmidt, S. (2009) Cdc42 and the phosphatidylinositol 3-kinase-Akt pathway are essential for PspC-mediated internalization of pneumococci by respiratory epithelial cells. J. Biol. Chem. 284, 19427-19436
37. Hammerschmidt, S., Tillig, M. P., Wolff, S., Vaerman, J. P., and Chhatwal, G. S. (2000) Species-specific binding of human secretory component to SpsA protein of Streptococcus pneumoniae via a hexapeptide motif. Mol. Microbiol. 36, 726-736 (Pubitemid 30258855)
38. Barthel, D., Schindler, S., and Zipfel, P. F. (2012) Plasminogen is a complement inhibitor. J. Biol. Chem. 287, 18831-18842
39. Barthel, D., Singh, B., Riesbeck, K., and Zipfel, P. F. (2012) Haemophilus influenzae uses the surface protein E to acquire human plasminogen and to evade innate immunity. J. Immunol. 188, 379-385
40. Bernardo-García, N., Bartual, S. G., Fulde, M., Bergmann, S., and Hermoso, J. A. (2011) Crystallization and preliminary x-ray diffraction analysis of phosphoglycerate kinase from Streptococcus pneumoniae. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 67, 1285-1289
41. Bland, N. D., Pinney, J. W., Thomas, J. E., Turner, A. J., and Isaac, R. E. (2008) Bioinformatic analysis of the neprilysin (M13) family of peptidases reveals complex evolutionary and functional relationships. BMC Evol. Biol. 8, 16
42. Rawlings, N. D., and Barrett, A. J. (1993) Evolutionary families of peptidases. Biochem. J. 290, 205-218 (Pubitemid 23081221)
43. Turner, A. J., Isaac, R. E., and Coates, D. (2001) The neprilysin (NEP) family of zinc metalloendopeptidases. Genomics and function. Bioessays 23, 261-269 (Pubitemid 32192145)
44. Turner, A. J., Brown, C. D., Carson, J. A., and Barnes, K. (2000) The neprilysin family in health and disease. Adv. Exp. Med. Biol. 477, 229-240 (Pubitemid 32174009)
45. Rosenow, C., Ryan, P., Weiser, J. N., Johnson, S., Fontan, P., Ortqvist, A., and Masure, H. R. (1997) Contribution of novel choline-binding proteins to adherence, colonization and immunogenicity of Streptococcus pneumoniae. Mol. Microbiol. 25, 819-829 (Pubitemid 27397511)
46. Bergmann, S., Rohde, M., Preissner, K. T., and Hammerschmidt, S. (2005) The nine residue plasminogen-binding motif of the pneumococcal enolase is the major cofactor of plasmin-mediated degradation of extracellular matrix, dissolution of fibrin and transmigration. Thromb. Haemost. 94, 304-311 (Pubitemid 41122484)
47. Hallström, T., Haupt, K., Kraiczy, P., Hortschansky, P., Wallich, R., Skerka, C., and Zipfel, P. F. (2010) Complement regulator-acquiring surface protein 1 of Borrelia burgdorferi binds to human bone morphogenic protein 2, several extracellular matrix proteins, and plasminogen. J. Infect. Dis. 202, 490-498
48. Kunert, A., Losse, J., Gruszin, C., Hühn, M., Kaendler, K., Mikkat, S., Volke, D., Hoffmann, R., Jokiranta, T. S., Seeberger, H., Moellmann, U., Hellwage, J., and Zipfel, P. F. (2007) Immune evasion of the human pathogen Pseudomonas aeruginosa. Elongation factor Tuf is a factor H and plasminogen binding protein. J. Immunol. 179, 2979-2988
49. Luo, S., Poltermann, S., Kunert, A., Rupp, S., and Zipfel, P. F. (2009) Immune evasion of the human pathogenic yeast Candida albicans. Pra1 is a Factor H, FHL-1 and plasminogen binding surface protein. Mol. Immunol. 47, 541-550
50. Poltermann, S., Kunert, A., von der Heide, M., Eck, R., Hartmann, A., and Zipfel, P. F. (2007) Gpm1p is a factor H-, FHL-1-, and plasminogen-binding surface protein of Candida albicans. J. Biol. Chem. 282, 37537-37544
51. Wiles, K. G., Panizzi, P., Kroh, H. K., and Bock, P. E. (2010) Skizzle is a novel plasminogen-and plasmin-binding protein from Streptococcus agalactiae that targets proteins of human fibrinolysis to promote plasmin generation. J. Biol. Chem. 285, 21153-21164
52. Ansai, T., Yu, W., Urnowey, S., Barik, S., and Takehara, T. (2003) Construction of a pepO gene-deficient mutant of Porphyromonas gingivalis. Potential role of endopeptidase O in the invasion of host cells. Oral Microbiol. Immunol. 18, 398-400 (Pubitemid 37372902)