Identification of a novel plasmin(ogen)-binding motif in surface displayed α-enolase of Streptococcus pneumoniae

Molecular Microbiology

Volumn 49, Issue 2, 2003, Pages 411-423

  Bergmann, Simone ^a,b   Wild, Daniela ^a   Diekmann, Oliver ^a   Frank, Ronald ^a   Bracht, Dagmar ^a   Chhatwal, Gursharan S ^a   Hammerschmidt, Sven ^a  

^a HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ENOLASE; BACTERIAL PROTEIN; ENOLASE; EPITOPE; LYSINE; MUTANT PROTEIN; PEPTIDE; PHENYALALANYLTYROSYLASPARTYLLYSYLGLUTAMYLARGINYLLYSYLVALYLTYROSYLASPARTIC ACID; PLASMIN; PLASMINOGEN; SERINE PROTEINASE; SYNTHETIC PEPTIDE; TISSUE PLASMINOGEN ACTIVATOR; UNCLASSIFIED DRUG; UROKINASE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL VIRULENCE; BACTERIUM MUTANT; BINDING AFFINITY; BINDING ASSAY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; COMPETITIVE INHIBITION; COMPLEX FORMATION; CONTROLLED STUDY; ISOTOPE LABELING; KRINGLE DOMAIN; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; STREPTOCOCCUS INFECTION; STREPTOCOCCUS PNEUMONIAE; SURFACE PLASMON RESONANCE;

AMINO ACID MOTIFS; ANIMALS; BACTERIAL PROTEINS; BINDING SITES; HUMANS; MICE; MICE, INBRED BALB C; MUTAGENESIS, SITE-DIRECTED; PEPTIDES; PHOSPHOPYRUVATE HYDRATASE; PLASMIN; PLASMINOGEN; PROTEIN BINDING; STREPTOCOCCUS PNEUMONIAE; SURFACE PLASMON RESONANCE; VIRULENCE;

ANIMALIA; BACTERIA (MICROORGANISMS); POSIBACTERIA; STREPTOCOCCUS; STREPTOCOCCUS PNEUMONIAE;

EID: 0038501069     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2003.03557.x     Document Type: Article

References (50)

1. Andronicos, N.M., Baker, M.S., Lackmann, M., and Ranson, M. (2000) Deconstructing the interaction of gtu-plasminogen with its receptor α-enolase. Fibrinolysis Proteolysis 14: 327-336.
2. Austrian, R. (1986) Some aspects of the pneumococcal carrier state. J Antimicrob Chemotherapy 18: 35-45.
3. 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.
4. Brooks-Walter, A., Briles, D.E., and Hollingshead, S.K. (1999) The pspC gene of Streptococcus pneumoniae encodes a polymorphic protein, PspC, which elicits cross-reactive antibodies to PspA and provides immunity to pneumococcal bacteremia. Infect Immun 67: 6533-6542.
5. Calvin, N.M., and Hanawalt, P.C. (1988) High-efficiency transformation of bacterial cells by electroporation. J Bacteriol 170: 2796-2801.
6. Chhatwal, G.S., Preissner, K.T., Muller Berghaus, G., and Blobel, H. (1987) Specific binding of the human S protein (vitronectin) to streptococci, Staphylococcus aureus and Escherichia coli. Infect Immun 55: 1878-1883.
7. Christensen, U. (1984) The AH-site of plasminogen and two C-terminal fragments. A weak lysine-binding site preferring ligands not carrying a free carboxylate function. Biochem J 223: 413-421.
8. Cundell, D.R., Gerard, N.P., Gerard, C., Idanpaan-Heikkila, I., and Tuomanen, E.I. (1995) Streptococcus pneumoniae anchor to activated human cells by the receptor for platelet-activating factor. Nature 377: 435-438.
9. Duval-Jobe, C., and Parmely, M.J. (1994) Regulation of plasminogen activation by human U937 promonocytic cells. J Biol Chem 269: 21353-21357.
10. Eberhard, T., Kronvall, G., and Ullberg, M. (1999) Plasminogen binding promotes migration through reconstituted basement membranes. Microb Pathog 26: 175-181.
11. Emini, E.A., Hughes, J.V., Perlow, D.S., and Boger, J. (1985) Induction of hepatitis A virus neutralizing antibody by virus-specific synthetic peptide. J Virol 55: 836-839.
12. Frank, R., and Overwin (1996) SPOT-synthesis: epitope analysis with arrays of synthetic peptides prepared on cellulose membranes. In Methods in Molecular Biology, 66: Epitope Mapping Protocols Morris, G.E.(ed.), Totowa, USA: The Humana Press Inc., 149-169.
13. Garnier, J., Osguthorpe, D.J., and Robson, B. (1978) Analysis of the accuracy and implications of simple methods for predicting the secondary structure of globular proteins. J Mol Biol 120: 97-120.
14. Glaser, P., Rusniok, C., Chevalier, F., Buchrieser, C., Frangeul, L., Zouine, M., et al. (2002) Genome sequence of Streptococcus agalactiae, a pathogen causing invasive neonatal diseases. Mol Microbiol 45: 1499-1513.
15. Gonzales-Gronow, M., Stack, S., and Pizzo, S.V. (1991) Plasmin-binding to plasminogen receptor enhances catalytic efficiency and activates the receptor for subsequent ligand binding. Arch Biochem Biophys 286: 625-628.
16. 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.
17. Hammerschmidt, S., Tillig, M., 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.
18. Håvarstein, L.S., Coomaraswamy, G., and Morrison, D.A. (1995) An unmodified heptadecapeptide pheromone induces competence for genetic transformation in Streptococcus pneumoniae. Proc Natl Acad Sci USA 92: 11140-11144.
19. 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.
20. Hughes, M.J., Moore, J.C., Lane, J.D., Wilson, R., Pribul, P.K., Younes, Z.N., et al. (2002) Identification of major outer surface proteins of Streptococcus agalactiae. Infect Immun 70: 1254-1259.
21. Janin, J., and Wodak, S. (1978) Conformation of amino acid side chains in proteins. J Mol Biol 125: 357-386.
22. Lottenberg, R. (1997) A novel approach to explore the role of plasminogen in bacterial pathogenesis. Trends Microbiol 5: 466-468.
23. Lottenberg, R., Broder, C.C., and Boyle, M.D. (1987) Identification of a specific receptor for plasmin on a group A streptococcus. Infect Immun 55: 1914-1928.
24. Lottenberg, R., Broder, C.C., Boyle, M.D.P., Kain, S.J., Schroeder, B.L., and Curtiss, R., III (1992) Cloning, sequence analysis and expression in Escherichia coli of a streptococal plasmin receptor. J Bacteriol 174: 5204-5210.
25. Lottenberg, R., Minning-Wenz, D., and Boyle, M.D. (1994) Capturing host plasmin (ogen) a common mechanism for invasive pathogens? Trends Microbiol 2: 20-24.
26. Matsuka, Y.V., Novokhatny, V.V., and Kudinov, S.A. (1990) Fluorescence spectroscopic analysis of ligand binding to kringle 1+2+3 and kringle 1 fragments from human plasminogen. Eur J Biochem 190: 93-97.
27. Miles, L.A., Dahlberg, C.M., and Plow, E.F. (1988) The cell binding domains of plasminogen and their function in plasma. J Biol Chem 263: 11928-11934.
28. Miles, L.A., Dahlberg, C.M., Plescia, J., Felez, J., Kato, K., and Plow, E.F. (1991) Role of cell-surface lysines in plasminogen binding to cells: identification of α-enolases as a candidate plasminogen receptor. Biochemistry 30: 1682-1691.
29. Miyashita, C., Wenzel, E., and Heiden, M. (1988) Plasminogen: a brief introduction into its biochemistry and function. Haemostasis 18: 7-13.
30. Morrison, D.A., Trombe, M.C., Hayden, M.K., Waszak, G.A., and Chen, J.D. (1984) Isolation of transformation-deficient Streptococcus pneumoniae mutants defective in control of competence, using insertion-duplication mutagenesis with the erythromycin resistance determinant of pAMβ1. J Bacteriol 159: 870-876.
31. Musher, D.M. (1992) Infections caused by Streptococcus pneumoniae: clinical spectrum, pathogenesis, immunity, and treatment. Clin Infect Dis 14; 801-809.
32. Nice, E.C., Mcinerney, T.L., and Jackson, D.C. (1996) Analysis of the interaction between a synthetic peptide of influenza virus hemagglutinin and monoclonal antibody using an optical biosensor. Mol Immunol 33: 659-670.
33. Novokhatny, V.V., Matsuka, Y.V., and Kudinov, S.A. (1989) Analysis of ligand binding to kringles 4 and 5 fragments from human plasminogen. Thromb Res 53: 243-253.
34. Pancholi, V. (2001) Multifunctional-enolase: its role in diseases. Cell Mol Life Sci 58: 902-920.
35. Pancholi, V., and Fischetti, V.A. (1992) A major surface protein on group A streptococci is a glyceraldehyde-3-phosphate dehydrogenase with multiple binding activity. J Exp Med 176: 415-426.
36. Pancholi, V., and Fischetti, V.A. (1998) α-enolase, a novel strong plasmin(ogen) binding protein on the surface of pathogenic streptococci. J Biol Chem 273: 14503-14515.
37. Plow, E.F., Felez, J., and Miles, L.A. (1991) Cellular regulation of fibrinolysis. Thromb Haemostasis 66: 32-36.
38. Plow, E.F., Herren, T., Redlitz, A., Miles, L.A., and Hoover-Plow, J.L. (1995) The cell biology of the plasminogen system. FASEB J 9: 939-945.
39. Pollanen, J., Stephens, R.W., and Vaheri, A. (1991) Directed plasminogen activation at the surface of normal and malignant cells. Adv Cancer Ress 57: 273-328.
40. Redlitz, A., Fowler, B.J., Plow, E.F., and Miles, L.A. (1995) The role of an enolase-related molecule in plasminogen binding to cells. Eur J Biochem 227: 407-415.
41. Saksela, O., and Rifkin, D.B. (1988) Cell-associated plasminogen activation: regulation and physiological functions. Annu Rev Cell Biol 4: 93-126.
42. 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.
43. Tettelin, H., Masignani, V., Cieslewicz, M.J., Eisen, J.A., Peterson, S., Wessels, M.R., et al. (2002) Complete genome sequence and comparative genomic analysis of an emerging human pathogen, serotype V Streptococcus agalactiae. Proc Natl Acad Sci USA 99: 12391-12396.
44. Tiraby, G., and Fox, M.S. (1973) Marker discrimination in transformation and mutation of pneumococcus. Proc Natl Acad Sci USA 70: 3541-3545.
45. Voskuilen, M., Vermond, A., Veeneman, G.H., van Boom, J.H., Klasen, E.A., Zegers, N.D., and Nieuwenhuizen, W. (1987) Fibrinogen lysine residue A alpha 157 plays a crucial role in the fibrin-induced acceleration of plasminogen activation, catalyzed by tissue-type plasminogen activator. J Biol Chem 262: 5944-5946.
46. Winram, S.B., and Lottenberg, R. (1998) Site-directed mutagenesis of streptococcal plasmin receptor protein (Plr) identifies the C-terminal Lys334 as essential for plasmin binding, but mutation of plr gene does not reduce plasmin binding to group A streptococci. Microbiology 144: 2025-2035.
47. Wistedt, A.C., Ringdahl, U., Müller-Esterl, W., and Sjöbring, U. (1995) Identification of a plasminogen-binding motif in PAM, a bacterial surface protein. Mol Microbiol 18: 569-578.
48. Wistedt, A.C., Kotarsky, H., Marti, D., Ringdahl, U., Castillino, F.J., Schaller, J., and Sjöbring, U. (1998) Kringle 2 mediates high affinity binding of plasminogen to an internal sequence in streptococcal surface protein PAM. J Biol Chem 38: 24420-24424.
49. Wong, A.P., Cortez, S.L., and Baricos, W.H. (1992) Role of plasmin and gelatinase in extracellular matrix degradation by cultured rat mesangial cells. Am J Physiol 263: 1112-1118.
50. 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.