A specific interaction between SecA2 and a region of the preprotein adjacent to the signal peptide occurs during transport via the accessory Sec system

Journal of Biological Chemistry

Volumn 287, Issue 29, 2012, Pages 24438-24447

  Bensing, Barbara A ^a   Yen, Yihfen T ^a   Seepersaud, Ravin ^a   Sullam, Paul M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL CELL SURFACE; E. COLI; IN-VIVO; N-TERMINALS; PHOTOCROSS-LINKING; PREPROTEINS; SIGNAL PEPTIDE; SITE-SPECIFIC; SPECIFIC INTERACTION; STREPTOCOCCUS GORDONII;

AMINO ACIDS; CELL MEMBRANES; ESCHERICHIA COLI; GLYCOPROTEINS; PROTEINS;

ACCESSORIES;

ACCESSORY SEC SYSTEM; ASP1 PROTEIN; ASP2 PROTEIN; ASP3 PROTEIN; CARRIER PROTEIN; GLYCOPROTEIN; GSPB PROTEIN; PROTEIN PRECURSOR; PROTEIN SECA; SECA2 PROTEIN; SIGNAL PEPTIDE; UNCLASSIFIED DRUG;

ACCESSORY SEC TRANSPORT DOMAIN; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; STREPTOCOCCUS GORDONII;

ADENOSINE TRIPHOSPHATASES; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; ESCHERICHIA COLI; PROTEIN BINDING; PROTEIN SORTING SIGNALS; STREPTOCOCCUS GORDONII;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; STAPHYLOCOCCUS; STREPTOCOCCUS GORDONII;

EID: 84863793927     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.378059     Document Type: Article

References (42)

1. Froeliger, E. H., and Fives-Taylor, P. (2001) Streptococcus parasanguis fimbria-associated adhesin Fap1 is required for biofilm formation. Infect. Immun. 69, 2512-2519 (Pubitemid 32239724)
2. Handley, P. S., Correia, F. F., Russell, K., Rosan, B., and DiRienzo, J. M. (2005) Association of a novel high molecular weight, serine-rich protein (SrpA) with fibril-mediated adhesion of the oral biofilm bacterium Streptococcus cristatus. Oral. Microbiol. Immunol. 20, 131-140 (Pubitemid 40559424)
3. Mistou, M. Y., Dramsi, S., Brega, S., Poyart, C., and Trieu-Cuot, P. (2009) Molecular dissection of the secA2 locus of group B streptococcus reveals that glycosylation of the Srr1 LPXTG protein is required for full virulence. J. Bacteriol 191, 4195-4206
4. Obert, C., Sublett, J., Kaushal, D., Hinojosa, E., Barton, T., Tuomanen, E. I., and Orihuela, C. J. (2006) Identification of a candidate Streptococcus pneumoniae core genome and regions of diversity correlated with invasive pneumococcal disease. Infect. Immun. 74, 4766-4777 (Pubitemid 44157264)
5. 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
6. Seifert, K. N., Adderson, E. E., Whiting, A. A., Bohnsack, J. F., Crowley, P. J., and Brady, L. J. (2006)Aunique serine-rich repeat protein (Srr-2) and novel surface antigen (epsilon) associated with a virulent lineage of serotype III Streptococcus agalactiae. Microbiology 152, 1029-1040
7. Siboo, I. R., Chambers, H. F., and Sullam, P. M. (2005) Role of SraP, a serine-rich surface protein of Staphylococcus aureus, in binding to human platelets. Infect. Immun. 73, 2273-2280 (Pubitemid 40470828)
8. Takahashi, Y., Takashima, E., Shimazu, K., Yagishita, H., Aoba, T., and Konishi, K. (2006) Contribution of sialic acid-binding adhesin to pathogenesis of experimental endocarditis caused by Streptococcus gordonii DL1. Infect. Immun. 74, 740-743 (Pubitemid 43023131)
9. van Sorge, N. M., Quach, D., Gurney, M. A., Sullam, P. M., Nizet, V., and Doran, K. S. (2009) The group B streptococcal serine-rich repeat 1 glyco-protein mediates penetration of the blood-brain barrier. J. Infect. Dis. 199, 1479-1487
10. Xiong, Y. Q., Bensing, B. A., Bayer, A. S., Chambers, H. F., and Sullam, P. M. (2008) Role of the serine-rich surface glycoprotein GspB of Streptococcus gordonii in the pathogenesis of infective endocarditis. Microb. Pathog. 45, 297-301
11. Takamatsu, D., Bensing, B. A., Cheng, H., Jarvis, G. A., Siboo, I. R., López, J. A., Griffiss, J. M., and Sullam, P. M. (2005) Binding of the Streptococcus gordonii surface glycoproteins GspB and Hsa to specific carbohydrate structures on platelet membrane glycoprotein Ibα. Mol. Microbiol. 58, 380-392 (Pubitemid 41476156)
12. Takahashi, Y., Sandberg, A. L., Ruhl, S., Muller, J., and Cisar, J. O. (1997) A specific cell surface antigen of Streptococcus gordonii is associated with bacterial hemagglutination and adhesion to α2-3-linked sialic acid-containing receptors. Infect. Immun. 65, 5042-5051 (Pubitemid 27513548)
13. 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
14. Samen, U., Eikmanns, B. J., Reinscheid, D. J., and Borges, F. (2007) The surface protein Srr-1 of Streptococcus agalactiae binds human keratin 4 and promotes adherence to epithelial HEp-2 cells. Infect. Immun. 75, 5405-5414 (Pubitemid 350033629)
15. Plummer, C., Wu, H., Kerrigan, S. W., Meade, G., Cox, D., and Ian Douglas, C. W. (2005) A serine-rich glycoprotein of Streptococcus sanguis mediates adhesion to platelets via GPIb. Br. J. Haematol. 129, 101-109 (Pubitemid 40524058)
16. Siboo, I. R., Chaffin, D. O., Rubens, C. E., and Sullam, P. M. (2008) Characterization of the accessory Sec system of Staphylococcus aureus. J. Bacteriol 190, 6188-6196
17. Bensing, B. A., and Sullam, P. M. (2002) An accessory sec locus of Streptococcus gordonii is required for export of the surface protein GspB and for normal levels of binding to human platelets. Mol. Microbiol. 44, 1081-1094 (Pubitemid 34535542)
18. Chen, Q., Wu, H., and Fives-Taylor, P. M. (2004) Investigating the role of secA2 in secretion and glycosylation of a fimbrial adhesin in Streptococcus parasanguis FW213. Mol. Microbiol. 53, 843-856 (Pubitemid 39036964)
19. Bensing, B. A., and Sullam, P. M. (2009) Characterization of Streptococcus gordonii SecA2 as a paralogue of SecA. J. Bacteriol. 191, 3482-3491
20. Bensing, B. A., and Sullam, P. M. (2010) Transport of preproteins by the accessory Sec system requires a specific domain adjacent to the signal peptide. J. Bacteriol. 192, 4223-4232
21. Takamatsu, D., Bensing, B. A., and Sullam, P. M. (2005) Two additional components of the accessory Sec system mediating export of the Streptococcus gordonii platelet-binding protein GspB. J. Bacteriol. 187, 3878-3883 (Pubitemid 40705596)
22. Takamatsu, D., Bensing, B. A., and Sullam, P. M. (2004) Genes in the accessory sec locus of Streptococcus gordonii have three functionally distinct effects on the expression of the platelet-binding protein GspB. Mol. Microbiol. 52, 189-203 (Pubitemid 38519631)
23. Seepersaud, R., Bensing, B. A., Yen, Y. T., and Sullam, P. M. (2010) Asp3 mediates multiple protein-protein interactions within the accessory Sec system of Streptococcus gordonii. Mol. Microbiol. 78, 490-505
24. Zhou, M., Zhang, H., Zhu, F., and Wu, H. (2011) Canonical SecA associates with an accessory secretory protein complex involved in biogenesis of a streptococcal serine-rich repeat glycoprotein. J. Bacteriol. 193, 6560-6566
25. Yen, Y. T., Seepersaud, R., Bensing, B. A., and Sullam, P. M. (2011) Asp2 and Asp3 interact directly with GspB, the export substrate of the Streptococcus gordonii accessory Sec System. J. Bacteriol. 193, 3165-3174
26. Bensing, B. A., Takamatsu, D., and Sullam, P. M. (2005) Determinants of the streptococcal surface glycoprotein GspB that facilitate export by the accessory Sec system. Mol. Microbiol. 58, 1468-1481 (Pubitemid 41705423)
27. Bensing, B. A., Siboo, I. R., and Sullam, P. M. (2007) Glycine residues in the hydrophobic core of the GspB signal sequence route export toward the accessory Sec pathway. J. Bacteriol 189, 3846-3854 (Pubitemid 46740182)
28. Mori, H., and Ito, K. (2006) Different modes of SecY-SecA interactions revealed by site-directed in vivo photo-cross-linking. Proc. Natl. Acad. Sci. U.S.A. 103, 16159-16164 (Pubitemid 44715167)
29. Ieva, R., and Bernstein, H. D. (2009) Interaction of an autotransporter passenger domain with BamA during its translocation across the bacterial outer membrane. Proc. Natl. Acad. Sci. U.S.A. 106, 19120-19125
30. Das, S., and Oliver, D. B. (2011) Mapping of the SecA, SecY and SecA. SecG interfaces by site-directed in vivo photocross-linking. J. Biol. Chem. 286, 12371-12380
31. Young, T. S., and Schultz, P. G. (2010) Beyond the canonical 20 amino acids: expanding the genetic lexicon. J. Biol. Chem. 285, 11039-11044
32. Liu, C. C., and Schultz, P. G. (2010) Adding new chemistries to the genetic code. Annu. Rev. Biochem. 79, 413-444
33. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A., and Struhl, K. (1997) Current Protocols in Molecular Biology, John Wiley & Sons, Inc.
34. Takamatsu, D., Bensing, B. A., and Sullam, P. M. (2004) Four proteins encoded in the gspB-secY2A2 operon of Streptococcus gordonii mediate the intracellular glycosylation of the platelet-binding protein GspB. J. Bacteriol. 186, 7100-7111 (Pubitemid 39383094)
35. Macrina, F. L., Evans, R. P., Tobian, J. A., Hartley, D. L., Clewell, D. B., and Jones, K. R. (1983) Novel shuttle plasmid vehicles for Escherichia-Streptococcus transgeneric cloning. Gene 25, 145-150 (Pubitemid 14241215)
36. Pyburn, T. M., Bensing, B. A., Xiong, Y. Q., Melancon, B. J., Tomasiak, T. M., Ward, N. J., Yankovskaya, V., Oliver, K. M., Cecchini, G., Sulikowski, G. A., Tyska, M. J., Sullam, P. M., and Iverson, T. M. (2011) A structural model for binding of the serine-rich repeat adhesin GspB to host carbohydrate receptors. PLoS Pathog. 7, e1002112
37. Bryan, E. M., Bae, T., Kleerebezem, M., and Dunny, G. M. (2000) Improved vectors for nisin-controlled expression in gram-positive bacteria. Plasmid 44, 183-190
38. Auclair, S. M., Moses, J. P., Musial-Siwek, M., Kendall, D. A., Oliver, D. B., and Mukerji, I. (2010) Mapping of the signal peptide-binding domain of Escherichia coli SecA using Forster resonance energy transfer. Biochemistry 49, 782-792
39. Gelis, I., Bonvin, A. M., Keramisanou, D., Koukaki, M., Gouridis, G., Karamanou, S., Economou, A., and Kalodimos, C. G. (2007) Structural basis for signal-sequence recognition by the translocase motor SecA as determined by NMR. Cell 131, 756-769 (Pubitemid 350087200)
40. Zimmer, J., and Rapoport, T. A. (2009) Conformational flexibility and peptide interaction of the translocation ATPase SecA. J. Mol. Biol. 394, 606-612
41. Gouridis, G., Karamanou, S., Gelis, I., Kalodimos, C. G., and Economou, A. (2009) Signal peptides are allosteric activators of the protein translocase. Nature 462, 363-367
42. Zimmer, J., Nam, Y., and Rapoport, T. A. (2008) Structure of a complex of the ATPase SecA and the protein-translocation channel. Nature 455, 936-943