Capturing host-pathogen interactions by protein microarrays: Identification of novel streptococcal proteins binding to human fibronectin, fibrinogen, and C4BP

FASEB Journal

Volumn 23, Issue 9, 2009, Pages 3100-3112

  Margarit, Immaculada ^a   Bonacci, Stefano ^a   Pietrocola, Giampiero ^b   Rindi, Simonetta ^b   Ghezzo, Claudia ^a   Bombaci, Mauro ^c   Nardi Dei, Vincenzo ^a   Grifantini, Renata ^d   Speziale, Pietro ^b   Grandi, Guido ^a  

^a NOVARTIS VACCINES AND DIAGNOSTICS   (Italy)

^b UNIVERSITY OF PAVIA   (Italy)

^c Istituto Nazionale di Genetica Molecolare   (Italy)

^d Externautics SpA   (Italy)

Author keywords

GAS; GBS; Virulence factors

Indexed keywords

COMPLEMENT COMPONENT C4 BINDING PROTEIN; FIBRINOGEN; FIBRONECTIN; MEMBRANE PROTEIN; STREPTOCOCCAL PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; ENZYME LINKED IMMUNOSORBENT ASSAY; HOST PATHOGEN INTERACTION; HUMAN; LIGAND BINDING; MOLECULAR INTERACTION; NONHUMAN; PATHOGENESIS; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN MICROARRAY; PROTEIN PROTEIN INTERACTION; STREPTOCOCCUS; STREPTOCOCCUS AGALACTIAE; STREPTOCOCCUS PYOGENES; WESTERN BLOTTING;

BACTERIAL PROTEINS; FIBRINOGEN; FIBRONECTINS; HISTOCOMPATIBILITY ANTIGENS; HOST-PATHOGEN INTERACTIONS; HUMANS; PROTEIN ARRAY ANALYSIS; PROTEIN BINDING; STREPTOCOCCUS; STREPTOCOCCUS AGALACTIAE; STREPTOCOCCUS PYOGENES;

STREPTOCOCCUS AGALACTIAE; STREPTOCOCCUS PYOGENES; STREPTOCOCCUS SP. 'GROUP B';

EID: 70349323594     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.09-131458     Document Type: Article

References (71)

1. Cunningham, M. W. (2000) Pathogenesis of group A streptococcal infections. Clin. Microbiol. Rev. 13, 470-511
2. Schuchat, A. (1999) Group B streptococcus. Lancet 353, 51-56
3. Bisno, A. L., Brito, M. O., and Collins, C. M. (2003) Molecular basis of group A streptococcal virulence. Lancet Infect. Dis. 3, 191-200
4. Doran, K. S., and Nizet, V. (2004) Molecular pathogenesis of neonatal group B streptococcal infection: no longer in its infancy. Mol. Microbiol. 54, 23-31
5. Lindahl, G., Stalhammar-Carlemalm, M., and Areschoug, T. (2005) Surface proteins of Streptococcus agalactiae and related proteins in other bacterial pathogens. Clin. Microbiol. Rev. 18, 102-127 (Pubitemid 40170663)
6. Kwinn, L. A., and Nizet, V. (2007) How group A streptococcus circumvents host phagocyte defenses. Future Microbiol. 2, 75-84
7. Westerlund, B., and Korhonen, T. K. (1993) Bacterial proteins binding to the mammalian extracellular matrix. Mol. Microbiol. 9, 687-694 (Pubitemid 23253495)
8. Lindahl, G., Sjobring, U., and Johnsson, E. (2000) Human complement regulators: a major target for pathogenic microorganisms. Curr. Opin. Immunol. 12, 44-51 (Pubitemid 30093449)
9. Rivera, J., Vannakambadi, G., Hook, M., and Speziale, P. (2007) Fibrinogen-binding proteins of Gram-positive bacteria. Thromb. Haemost. 98, 503-511
10. Talay, S. R., Valentin-Weigand, P., Jerlstrom, P. G., Timmis, K. N., and Chhatwal, G. S. (1992) Fibronectin-binding protein of Streptococcus pyogenes: sequence of the binding domain involved in adherence of streptococci to epithelial cells. Infect. Immun. 60, 3837-3844
11. Hanski, E., Jaffe, J., and Ozeri, V. (1996) Proteins F1 and F2 of Streptococcus pyogenes: properties of fibronectin binding. Adv. Exp. Med. Biol. 408, 141-150 (Pubitemid 26331062)
12. Courtney, H. S., Hasty, D. L., Li, Y., Chiang, H. C., Thacker, J. L., and Dale, J. B. (1999) Serum opacity factor is a major fibronectin-binding protein and a virulence determinant of M type 2 Streptococcus pyogenes. Mol. Microbiol. 32, 89-98 (Pubitemid 29164136)
13. Courtney, H. S., Li, Y., Dale, J. B., and Hasty, D. L. (1994) Cloning, sequencing, and expression of a fibronectin/fibrinogen-binding protein from group A streptococci. Infect. Immun. 62, 3937-3946 (Pubitemid 24264340)
14. Terao, Y., Kawabata, S., Kunitomo, E., Murakami, J., Nakagawa, I., and Hamada, S. (2001) Fba, a novel fibronectin-binding protein from Streptococcus pyogenes, promotes bacterial entry into epithelial cells, and the fba gene is positively transcribed under the Mga regulator. Mol. Microbiol. 42, 75-86 (Pubitemid 34212162)
15. Terao, Y., Kawabata, S., Nakata, M., Nakagawa, I., and Hamada, S. (2002) Molecular characterization of a novel fibronectin-binding protein of Streptococcus pyogenes strains isolated from toxic shock-like syndrome patients. J. Biol. Chem. 277, 47428-47435 (Pubitemid 36159259)
16. Beckmann, C., Waggoner, J. D., Harris, T. O., Tamura, G. S., and Rubens, C. E. (2002) Identification of novel adhesins from group B streptococci by use of phage display reveals that C5a peptidase mediates fibronectin binding. Infect. Immun. 70, 2869-2876 (Pubitemid 34564143)
17. Berggård, K., Johnsson, E., Morfeldt, E., Persson, J., Stålhammar-Carlemalm, M., and Lindahl, G. (2001) Binding of human C4BP to the hypervariable region of M protein: a molecular mechanism of phagocytosis resistance in Streptococcus pyogenes. Mol. Microbiol. 42, 539-551 (Pubitemid 32990140)
18. Pérez-Caballero, D., García-Laorden, I., Cortés, G., Wessels, M. R., de Córdoba, S. R., and Albertí, S. (2004) Interaction between complement regulators and Streptococcus pyogenes: binding of C4b-binding protein and factor H/factor H-like protein 1 to M18 strains involves two different cell surface molecules. J. Immunol. 173, 6899-6904
19. Persson, J., Beall, B., Linse, S., and Lindahl, G. (2006) Extreme sequence divergence but conserved ligand-binding specificity in Streptococcus pyogenes M protein. PLoS Pathog. 2, e47 (Pubitemid 43794311)
20. Santi, I., Scarselli, M., Mariani, M., Pezzicoli, A., Masignani, V., Taddei, A., Grandi, G., Telford, J. L., and Soriani, M. (2007) BibA: a novel immunogenic bacterial adhesin contributing to group B Streptococcus survival in human blood. Mol. Microbiol. 63, 754-767 (Pubitemid 46105900)
21. Carlsson, F., Sandin, C., and Lindahl, G. (2005) Human fibrinogen bound to Streptococcus pyogenes M protein inhibits complement deposition via the classical pathway. Mol. Microbiol. 56, 28-39 (Pubitemid 40461485)
22. Sandin, C., Carlsson, F., and Lindahl, G. (2006) Binding of human plasma proteins to Streptococcus pyogenes M protein determines the location of opsonic and non-opsonic epitopes. Mol. Microbiol. 59, 20-30
23. Noel, G. J., Katz, S. L., and Edelson, P. J. (1991) The role of C3 in mediating binding and ingestion of group B Streptococcus serotype III by murine macrophages. Pediatr. Res. 30, 118-123
24. Schubert, A., Zakikhany, K., Schreiner, M., Frank, R., Spellerberg, B., Eikmanns, B. J., and Reinscheid, D. J. (2002) A fibrinogen receptor from group B Streptococcus interacts with fibrinogen by repetitive units with novel ligand binding sites. Mol. Microbiol. 46, 557-569 (Pubitemid 35340964)
25. MacBeath, G., and Schreiber, S. L. (2000) Printing proteins as microarrays for high-throughput function determination. Science 289, 1760-1763 (Pubitemid 30683642)
26. Zhu, H., Bilgin, M., and Snyder, M. (2003) Proteomics. Annu. Rev. Biochem. 72, 783-812
27. Korf, U., and Wiemann, S. (2005) Protein microarrays as a discovery tool for studying protein-protein interactions. Expert Rev. Proteomics 2, 13-26 (Pubitemid 40292576)
28. Bacarese-Hamilton, T., Mezzasoma, L., Ardizzoni, A., Bistoni, F., and Crisanti, A. (2004) Serodiagnosis of infectious diseases with antigen microarrays. J. Appl. Microbiol. 96, 10-17 (Pubitemid 38177900)
29. Cai, H. Y., Lu, L., Muckle, C. A., Prescott, J. F., and Chen, S. (2005) Development of a novel protein microarray method for serotyping Salmonella enterica strains. J. Clin. Microbiol. 43, 3427-3430 (Pubitemid 40981357)
30. Davies, D. H., Liang, X., Hernandez, J. E., Randall, A., Hirst, S., Mu, Y., Pablo, J., Unal, B., Nakajima-Sasaki, R., Liang, X., Crotty, S., Karem, K. L., Damon, I. K., Ahmed, R., Villarreal, L., and Felgner, P. L. (2005) Profiling the humoral immune response to infection by using proteome microarrays: high-throughput vaccine and diagnostic antigen discovery. Proc. Natl. Acad. Sci. U. S. A. 102, 547-552 (Pubitemid 40282702)
31. Li, B., Jiang, L., Song, Q., Yang, J., Chen, Z., Mu, Y., Pablo, J., Unal, B., Nakajima-Sasaki, R., Liang, X., Crotty, S., Karem, K. L., Damon, I. K., Ahmed, R., Villarreal, L., and Felgner, P. L. (2005) Protein microarray for profiling antibody responses to Yersinia pestis live vaccine. Infect. Immun. 73, 3734-3739 (Pubitemid 40745918)
32. Steller, S., Angenendt, P., Cahill, D. J., Heuberger, S., Lehrach, H., and Kreutzberger, J. (2005) Bacterial protein microarrays for identification of new potential diagnostic markers for Neisseria meningitidis infections. Proteomics 5, 2048-2055 (Pubitemid 40770569)
33. Zhu, H., Hu, S., Jona, G., Zhu, X., Kreiswirth, N., Willey, B. M., Mazzulli, T., Liu, G., Song, Q., Chen, P., Cameron, M., Tyler, A., Wang, J., Wen, J., Chen, W., Compton, S., and Snyder, M. (2006) Severe acute respiratory syndrome diagnostics using a coronavirus protein microarray. Proc. Natl. Acad. Sci. U. S. A. 103, 4011-4016
34. Chen, C. S., Korobkova, E., Chen, H., Zhu, J., Jian, X., Tao, S. C., He, C., and Zhu, H. (2008) A proteome chip approach reveals new DNA damage recognition activities in Escherichia coli. Nat. Methods 5, 69-74
35. Speziale, P., Visai, L., Rindi, S., and Di Poto, A. (2008) Purification of human plasma fibronectin using immobilized gelatin and Arg affinity chromatography. Nat. Protoc. 3, 525-533
36. Borsi, L., Castellani, P., Balza, E., Siri, A., Pellecchia, C., De Scalzi, F., and Zardi, L. (1986) Large-scale procedure for the purification of fibronectin domains. Anal. Biochem. 155, 335-345 (Pubitemid 16060163)
37. Skorstengaard, K., Jensen, M. S., Petersen, T. E., and Magnusson, S. (1986) Purification and complete primary structures of the heparin-, cell-, and DNA-binding domains of bovine plasma fibronectin. Eur. J. Biochem. 154, 15-29 (Pubitemid 16077777)
38. Maione, D., Margarit, I., Rinaudo, C. D., Masignani, V., Mora, M., Scarselli, M., Tettelin, H., Brettoni, C., Iacobini, E. T., Rosini, R., D'Agostino, N., Miorin, L., Buccato, S., Mariani, M., Galli, G., Nogarotto, R., Nardi Dei, V., Vegni, F., Fraser, C., Mancuso, G., Teti, G., Madoff, L. C., Paoletti, L. C., Rappuoli, R., Kasper, D. L., Telford, J. L., and Grandi, G. (2005) Identification of a universal group B streptococcus vaccine by multiple genome screen. Science 309, 148-150 (Pubitemid 40934997)
39. Manetti, A. G., Zingaretti, C., Falugi, F., Capo, S., Bombaci, M., Gambellini, G., Bensi, G., Mora, M., Edwards, A. M., Musser, J. M., Graviss, E. A., Telford, J. L., Grandi, G., and Margarit, I. (2007) Streptococcus pyogenes pili promote pharyngeal cell adhesion and biofilm formation. Mol. Microbiol. 64, 968-983 (Pubitemid 46743959)
40. Harris, J., and Stoker, H. (1998) Maximum likelihood method. In Handbook of Mathematics and Computational Science p. 824, Springer-Verlag, New York
41. Rodríguez-Ortega, M. J., Norais, N., Bensi, G., Liberatori, S., Capo, S., Mora, M., Scarselli, M., Doro, F., Ferrari, G., Garaguso, I., Maggi, T., Neumann, A., Covre, A., Telford, J. L., and Grandi, G. (2006) Characterization and identification of vaccine candidate proteins through analysis of the group A Streptococcus surface proteome. Nat. Biotechnol. 24, 191-197 (Pubitemid 43221703)
42. Edwards, R. J., Taylor, G. W., Ferguson, M., Murray, S., Rendell, N., Wrigley, A., Bai, Z., Boyle, J., Finney, S. J., Jones, A., Russell, H. H., Turner, C., Cohen, J., Faulkner, L., and Sriskandan, S: (2005) Specific C-terminal cleavage and inactivation of interleukin-8 by invasive disease isolates of Streptococcus pyogenes. J. Infect. Dis. 192, 783-790 (Pubitemid 41193075)
43. Lauer, P., Rinaudo, C. D., Soriani, M., Margarit, I,, Maione, D., Rosini, R., Taddei, A. R., Mora, M., Rappuoli, R., Grandi, G., and Telford, J. L: (2005) Genome analysis reveals pili in group B Streptococcus. Science 309, 105 (Pubitemid 40934983)
44. Mora, M., Bensi, G., Capo, S., Falugi, F., Zingaretti, C., Manetti, A., G., Maggi, T., Taddei, A. R., Grandi, G., and Telford, J. L. (2005) Group A Streptococcus produce pilus-like structures containing protective antigens and Lancefield T antigens. Proc. Natl. Acad. Sci. U. S. A. 102, 15641-15646 (Pubitemid 41528109)
45. Rosini, R., Rinaudo, C. D., Soriani, M., Lauer, P., Mora, M., Maione, D., Taddei, A., Santi, I., Ghezzo, C., Brettoni, C., Buccato, S., Margarit. I., Grandi, G., and Telford, J. L. (2006) Identification of novel genomic islands coding for antigenic pilus-like structures in Streptococcus agalactiae. Mol. Microbiol. 61, 126-141 (Pubitemid 43911503)
46. Ferretti, J. J., McShan, W. M., Ajdic, D., Savic, D. J., Savic, G., Lyon, K., Primeaux, C., Sezate, S., Suvorov, A. N., Kenton, S., Lai, H. S., Lin, S. P., Qian, Y., Jia, H. G., Najar, F. Z., Ren, Q., Zhu, H., Song, L., White, J., Yuan, X., Clifton, S. W., Roe, B. A., and McLaughlin, R. (2001) Complete genome sequence of an M1 strain of Streptococcus pyogenes. Proc. Natl. Acad. Sci. U. S. A. 98, 4658-4663 (Pubitemid 32295032)
47. Tettelin, H., Masignani, V., Cieslewicz, M. J., Eisen, J. A., Peterson, S., Wessels, M. R., Paulsen, I. T., Nelson, K. E., Margarit, I., Read, T. D., Madoff, L. C., Wolf, A. M., Beanan, M. J., Brinkac, L. M., Daugherty, S. C., DeBoy, R. T., Durkin, A. S., Kolonay, J. F., Madupu, R., Lewis, M. R., Radune, D., Fedorova, N. B., Scanlan, D., Khouri, H., Mulligan, S., Carty, H. A., Cline, R. T., Van Aken, S. E., Gill, J., Scarselli, M., Mora, M., Iacobini, E. T., Brettoni, C., Galli, G., Mariani, M., Vegni, F., Maione, D., Rinaudo, D., Rappuoli, R., Telford, J. L., Kasper, D. L., Grandi, G., and Fraser, C. M. (2002) Complete genome sequence and comparative genomic analysis of an emerging human pathogen, serotype V Streptococcus agalactiae. Proc. Natl. Acad. Sci. U. S. A. 99, 12391-12396
48. Tettelin, H., Masignani, V., Cieslewicz, M. J., Donati, C., Medini, D., Ward, N. L., Angiuoli, S. V., Crabtree, J., Jones, A. L., Durkin, A. S., Deboy, R. T., Davidsen, T. M., Mora, M., Scarselli, M., Margarit y Ros, I., Peterson, J. D., Hauser, C. R., Sundaram, J. P., Nelson, W. C., Madupu, R., Brinkac, L. M., Dodson, R. J., Rosovitz, M. J., Sullivan, S. A., Daugherty, S. C., Haft, D. H., Selengut, J., Gwinn, M. L., Zhou, L., Zafar, N., Khouri, H., Radune, D., Dimitrov, G., Watkins, K., O'Connor, K. J., Smith, S., Utterback, T. R., White, O., Rubens, C. E., Grandi, G., Madoff, L. C., Kasper, D. L., Telford, J. L., Wessels, M. R., Rappuoli, R., and Fraser, C. M: (2005) Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial "pan-genome." Proc. Natl. Acad. Sci. U. S. A. 102, 13950-13955
49. Hanski, E., and Caparon, M. (1992) Protein F, a fibronectin-binding protein, is an adhesin of the group A streptococcus Streptococcus pyogenes. Proc. Natl. Acad. Sci. U. S. A. 89, 6172-6176
50. Katerov, V., Andreev, A., Schalen, C., and Totolian, A. A. (1998) Protein F, a fibronectin-binding protein of Streptococcus pyogenes, also binds human fibrinogen: isolation of the protein and mapping of the binding region. Microbiology 144 (Pt 1), 119-126 (Pubitemid 28045219)
51. Cue, D., Lam, H., and Cleary, P. P. (2001) Genetic dissection of the Streptococcus pyogenes M1 protein: regions involved in fibronectin binding and intracellular invasion. Microb. Pathog. 31, 231-242 (Pubitemid 33096068)
52. Cheng, Q., Stafslien, D., Purushothaman, S. S., and Cleary, P. (2002) The group B streptococcal C5a peptidase is both a specific protease and an invasin. Infect. Immun. 70, 2408-2413 (Pubitemid 34408382)
53. Schmidt, K. H., Mann, K., Cooney, J., and Kohler, W. (1993) Multiple binding of type 3 streptococcal M protein to human fibrinogen, albumin and fibronectin. FEMS Immunol. Med. Microbiol. 7, 135-143 (Pubitemid 23255973)
54. Akesson, P., Schmidt, K. H., Cooney, J., and Bjorck, L. (1994) M1 protein and protein H: IgGFc- and albumin-binding streptococcal surface proteins encoded by adjacent genes. Biochem. J. 300 (Pt 3), 877-886 (Pubitemid 24180607)
55. Gutekunst, H., Eikmanns, B. J., and Reinscheid, D. J. (2004) The novel fibrinogen-binding protein FbsB promotes Streptococcus agalactiae invasion into epithelial cells. Infect. Immun. 72, 3495-3504 (Pubitemid 38697776)
56. Brochet, M., Couve, E., Zouine, M., Vallaeys, T., Rusniok, C., Lamy, M. C., Buchrieser, C., Trieu-Cuot, P., Kunst, F., Poyart, C., and Glaser, P: (2006) Genomic diversity and evolution within the species Streptococcus agalactiae. Microbes Infect. 8, 1227-1243 (Pubitemid 43831687)
57. Meenan, N. A., Visai, L., Valtulina, V., Schwarz-Linek, U., Norris, N. C., Gurusiddappa, S., Höök, M., Speziale, P., and Potts, J. R. (2007) The tandem -zipper model defines high affinity fibronectin-binding repeats within Staphylococcus aureus FnBPA. J. Biol. Chem. 282, 25893-25902 (Pubitemid 47372812)
58. Rubens, C. E., Smith, S., Hulse, M., Chi, E. Y., and van Belle, G. (1992) Respiratory epithelial cell invasion by group B streptococci. Infect. Immun. 60, 5157-5163
59. Cue, D., Dombek, P. E., Lam, H., and Cleary, P. P. (1998) Streptococcus pyogenes serotype M1 encodes multiple pathways for entry into human epithelial cells. Infect. Immun. 66, 4593-4601 (Pubitemid 28453058)
60. Marraffini, L. A., Dedent, A. C., and Schneewind, O. (2006) Sortases and the art of anchoring proteins to the envelopes of gram-positive bacteria. Microbiol. Mol. Biol. Rev. 70, 192-221
61. Johri, A. K., Paoletti, L. C., Glaser, P., Dua, M., Sharma, P. K., Grandi, G., and Rappuoli, R. (2006) Group B Streptococcus: global incidence and vaccine development. Nat. Rev. Microbiol. 4, 932-942 (Pubitemid 44768255)
62. Dale, J. B. (2008) Current status of group A streptococcal vaccine development. Adv. Exp. Med. Biol. 609, 53-63
63. Joh, D., Wann, E. R., Kreikemeyer, B., Speziale, P., and Hook, M. (1999) Role of fibronectin-binding MSCRAMMs in bacterial adherence and entry into mammalian cells. Matrix Biol. 18, 211-223 (Pubitemid 29324737)
64. Williams, M. J., Phan, I., Harvey, T. S., Rostagno, A., Gold, L. I., and Campbell, I. D. (1994) Solution structure of a pair of fibronectin type 1 modules with fibrin binding activity. J. Mol. Biol. 235, 1302-1311 (Pubitemid 24148932)
65. Schwarz-Linek, U., Werner, J. M., Pickford, A. R., Gurusiddappa, S., Kim, J. H., Pilka, E. S., Briggs, J. A., Gough, T. S., Höök, M., Campbell, I. D., and Potts, J. R. (2003) Pathogenic bacteria attach to human fibronectin through a tandem -zipper. Nature 423, 177-181 (Pubitemid 36569541)
66. Johri, A. K., Margarit, I., Broenstrup, M., Brettoni, C., Hua, L., Gygi, S. P., Telford, J. L., Grandi, G., Paoletti, L. C. (2007) Transcriptional and proteomic profiles of group B Streptococcus type V reveal potential adherence proteins associated with high-level invasion. Infect. Immun. 75, 1473-1483 (Pubitemid 46385841)
67. Panizzi, P., Friedrich, R., Fuentes-Prior, P., Richter, K., Bock, P. E., and Bode, W. (2006) Fibrinogen substrate recognition by staphylocoagulase • (pro)thrombin complexes. J. Biol. Chem. 281, 1179-1187
68. Lee, L. Y., Liang, X., Hook, M., and Brown, E. L. (2004) Identification and characterization of the C3 binding domain of the Staphylococcus aureus extracellular fibrinogen-binding protein (Efb). J. Biol. Chem. 279, 50710-50716 (Pubitemid 40017808)
69. Chavakis, T., Wiechmann, K., Preissner, K. T., and Herrmann, M. (2005) Staphylococcus aureus interactions with the endothelium: the role of bacterial "secretable expanded repertoire adhesive molecules" (SERAM) in disturbing host defense systems. Thromb. Haemost. 94, 278-285
70. Sobke, A. C., Selimovic, D., Orlova, V., Hassan, M., Chavakis, T., Athanasopoulos, A. N., Schubert, U., Hussain, M., Thiel, G., Preissner, K.T., and Herrmann, M. (2006) The extracellular adherence protein from Staphylococcus aureus abrogates angiogenic responses of endothelial cells by blocking Ras activation. FASEB J. 20, 2621-2623 (Pubitemid 44953800)
71. Lidèn, A., van Wieringen, T., Lannergård, J., Kassner, A., Heinegård, D., Reed, R. K., Guss, B., and Rubin, K. (2008) A secreted collagen- and fibronectin-binding streptococcal protein modulates cell-mediated collagen gel contraction and interstitial fluid pressure. J. Biol. Chem. 283, 1234-1242