Characterization of the secretion pathway of the collagen adhesin EmaA of Aggregatibacter actinomycetemcomitans

Molecular Oral Microbiology

Volumn 27, Issue 5, 2012, Pages 382-396

  Jiang, X ^a   Ruiz, T ^b   Mintz, K P ^a  

^a UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF VERMONT   (United States)

Author keywords

Chaperones; DnaK; SecB; Signal peptide; Trimeric autotransporter

Indexed keywords

ADHESIN; AMINO ACID; CHAPERONE; CHLORAMPHENICOL; COLLAGEN; DNA FRAGMENT; EXTRACELLULAR MATRIX PROTEIN ADHESIN A; GENOMIC DNA; MONOMER; PROTEIN DNAK; SIGNAL PEPTIDE; UNCLASSIFIED DRUG;

AGGREGATIBACTER ACTINOMYCETEMCOMITANS; AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL MEMBRANE; BACTERIUM MUTANT; CONTROLLED STUDY; DNA SEQUENCE; ESCHERICHIA COLI; EXTRACELLULAR MATRIX; GENE DELETION; GRAM NEGATIVE BACTERIUM; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PERIODONTITIS; PLASMID; POLYMERASE CHAIN REACTION; PROTEIN SECRETION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; SECB GENE; TRANSMISSION ELECTRON MICROSCOPY;

ACTINOBACILLUS ACTINOMYCETEMCOMITANS; ADENINE; ADENOSINE TRIPHOSPHATASES; ADHESINS, BACTERIAL; BACTERIAL PROTEINS; CELL MEMBRANE; CHROMOSOME DELETION; COLLAGEN; ESCHERICHIA COLI; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; HEAT-SHOCK RESPONSE; HUMANS; MOLECULAR CHAPERONES; MUTAGENESIS, INSERTIONAL; PLASMIDS; PROTEIN SORTING SIGNALS; SIGNAL RECOGNITION PARTICLE; THYMINE; TRANSFORMATION, BACTERIAL;

EID: 84866168766     PISSN: 20411006     EISSN: 20411014     Source Type: Journal    
DOI: 10.1111/j.2041-1014.2012.00652.x     Document Type: Article

References (61)

1. Baars, L., Ytterberg, A.J., Drew, D. et al. (2006) Defining the role of the Escherichia coli chaperone SecB using comparative proteomics. J Biol Chem281: 10024-10034.
2. Batey, R.T., Rambo, R.P., Lucast, L., Rha, B. and Doudna, J.A. (2000) Crystal structure of the ribonucleoprotein core of the signal recognition particle. Science287: 1232-1239.
3. Bernstein, H.D., Poritz, M.A., Strub, K., Hoben, P.J., Brenner, S. and Walter, P. (1989) Model for signal sequence recognition from amino-acid sequence of 54K subunit of signal recognition particle. Nature340: 482-486.
4. Carlile, J.R., Beckman, E.N. and Arensman, R.M. (1984) Actinobacillus actinomycetemcomitans pneumonia. Clin Pediatr (Phila)23: 578-580.
5. Christersson, L.A. (1993) Actinobacillus actinomycetemcomitans and localized juvenile periodontitis. Clinical, microbiologic and histologic studies. Swed Dent J Suppl90: 1-46.
6. Crane, J.M., Suo, Y., Lilly, A.A., Mao, C., Hubbell, W.L. and Randall, L.L. (2006) Sites of interaction of a precursor polypeptide on the export chaperone SecB mapped by site-directed spin labeling. J Mol Biol363: 63-74.
7. Dennis, J.J. and Zylstra, G.J. (1998) Improved antibiotic-resistance cassettes through restriction site elimination using Pfu DNA polymerase PCR. Biotechniques25: 772-774, 776.
8. Desvaux, M., Scott-Tucker, A., Turner, S.M. et al. (2007) A conserved extended signal peptide region directs posttranslational protein translocation via a novel mechanism. Microbiology153: 59-70.
9. Driessen, A.J. and Nouwen, N. (2008) Protein translocation across the bacterial cytoplasmic membrane. Annu Rev Biochem77: 643-667.
10. Fives-Taylor, P.M., Meyer, D.H., Mintz, K.P. and Brissette, C. (1999) Virulence factors of Actinobacillus actinomycetemcomitans. Periodontol 200020: 136-167.
11. Froderberg, L., Houben, E.N., Baars, L., Luirink, J. and de Gier, J.W. (2004) Targeting and translocation of two lipoproteins in Escherichia coli via the SRP/Sec/YidC pathway. J Biol Chem279: 31026-31032.
12. Gallant, C.V., Sedic, M., Chicoine, E.A., Ruiz, T. and Mintz, K.P. (2008) Membrane morphology and leukotoxin secretion are associated with a novel membrane protein of Aggregatibacter actinomycetemcomitans. J Bacteriol190: 5972-5980.
13. Goulhen, F., Grenier, D. and Mayrand, D. (2003) Oral microbial heat-shock proteins and their potential contributions to infections. Crit Rev Oral Biol Med14: 399-412.
14. Grant, S.G., Jessee, J., Bloom, F.R. and Hanahan, D. (1990) Differential plasmid rescue from transgenic mouse DNAs into Escherichia coli methylation-restriction mutants. Proc Natl Acad Sci U S A87: 4645-4649.
15. Hardy, S.J. and Randall, L.L. (1991) A kinetic partitioning model of selective binding of nonnative proteins by the bacterial chaperone SecB. Science251: 439-443.
16. Hartl, F.U., Lecker, S., Schiebel, E., Hendrick, J.P. and Wickner, W. (1990) The binding cascade of SecB to SecA to SecY/E mediates preprotein targeting to the E. coli plasma membrane. Cell63: 269-279.
17. von Heijne, G. (1990) The signal peptide. J Membr Biol115: 195-201.
18. Janakiraman, A., Fixen, K.R., Gray, A.N., Niki, H. and Goldberg, M.B. (2009) A genome-scale proteomic screen identifies a role for DnaK in chaperoning of polar autotransporters in Shigella. J Bacteriol191: 6300-6311.
19. Jiang, X., Ruiz, T. and Mintz, K.P. (2011) The extended signal peptide of the trimeric autotransporter EmaA of Aggregatibacter actinomycetemcomitans modulates secretion. J Bacteriol193: 6983-6994.
20. Kachlany, S.C. (2010) Aggregatibacter actinomycetemcomitans leukotoxin: from threat to therapy. J Dent Res89: 561-570.
21. Kamath-Loeb, A.S., Lu, C.Z., Suh, W.C., Lonetto, M.A. and Gross, C.A. (1995) Analysis of three DnaK mutant proteins suggests that progression through the ATPase cycle requires conformational changes. J Biol Chem270: 30051-30059.
22. Kerner, M.J., Naylor, D.J., Ishihama, Y. et al. (2005) Proteome-wide analysis of chaperonin-dependent protein folding in Escherichia coli. Cell122: 209-220.
23. Kusukawa, N., Yura, T., Ueguchi, C., Akiyama, Y. and Ito, K. (1989) Effects of mutations in heat-shock genes groES and groEL on protein export in Escherichia coli. EMBO J8: 3517-3521.
24. Luirink, J., High, S., Wood, H., Giner, A., Tollervey, D. and Dobberstein, B. (1992) Signal-sequence recognition by an Escherichia coli ribonucleoprotein complex. Nature359: 741-743.
25. Luirink, J., von Heijne, G., Houben, E. and de Gier, J.W. (2005) Biogenesis of inner membrane proteins in Escherichia coli. Annu Rev Microbiol59: 329-355.
26. Mauff, A.C., Miller, S., Kuhnle, V. and Carmichael, M. (1983) Infections due to Actinobacillus actinomycetemcomitans. A report of 3 cases. S Afr Med J63: 580-581.
27. Miller, A., Wang, L. and Kendall, D.A. (2002) SecB modulates the nucleotide-bound state of SecA and stimulates ATPase activity. Biochemistry41: 5325-5332.
28. Mintz, K.P. (2004) Identification of an extracellular matrix protein adhesin, EmaA, which mediates the adhesion of Actinobacillus actinomycetemcomitans to collagen. Microbiology150: 2677-2688.
29. Mintz, K.P. and Fives-Taylor, P.M. (1999) Binding of the periodontal pathogen Actinobacillus actinomycetemcomitans to extracellular matrix proteins. Oral Microbiol Immunol14: 109-116.
30. Mintz, K.P., Brissette, C. and Fives-Taylor, P.M. (2002) A recombinase A-deficient strain of Actinobacillus actinomycetemcomitans constructed by insertional mutagenesis using a mobilizable plasmid. FEMS Microbiol Lett206: 87-92.
31. Muhle, I., Rau, J. and Ruskin, J. (1979) Vertebral osteomyelitis due to Actinobacillus actinomycetemcomitans. JAMA241: 1824-1825.
32. Neidhardt, F.C., VanBogelen, R.A. and Vaughn, V. (1984) The genetics and regulation of heat-shock proteins. Annu Rev Genet18: 295-329.
33. + but not ATP hydrolysis. Nature365: 664-666.
34. Peterson, J.H., Woolhead, C.A. and Bernstein, H.D. (2003) Basic amino acids in a distinct subset of signal peptides promote interaction with the signal recognition particle. J Biol Chem278: 46155-46162.
35. Peterson, J.H., Szabady, R.L. and Bernstein, H.D. (2006) An unusual signal peptide extension inhibits the binding of bacterial presecretory proteins to the signal recognition particle, trigger factor, and the SecYEG complex. J Biol Chem281: 9038-9048.
36. Poritz, M.A., Bernstein, H.D., Strub, K., Zopf, D., Wilhelm, H. and Walter, P. (1990) An E. coli ribonucleoprotein containing 4.5S RNA resembles mammalian signal recognition particle. Science250: 1111-1117.
37. Priefer, U.B., Simon, R. and Puhler, A. (1985) Extension of the host range of Escherichia coli vectors by incorporation of RSF1010 replication and mobilization functions. J Bacteriol163: 324-330.
38. Qi, H.Y., Hyndman, J.B. and Bernstein, H.D. (2002) DnaK promotes the selective export of outer membrane protein precursors in SecA-deficient Escherichia coli. J Biol Chem277: 51077-51083.
39. Randall, L.L. and Hardy, S.J. (1995) High selectivity with low specificity: how SecB has solved the paradox of chaperone binding. Trends Biochem Sci20: 65-69.
40. Reider, J. and Wheat, J. (1979) Endocarditis caused by Actinobacillus actinomycetemcomitans. South Med J72: 1219-1220.
41. Rudiger, S., Germeroth, L., Schneider-Mergener, J. and Bukau, B. (1997) Substrate specificity of the DnaK chaperone determined by screening cellulose-bound peptide libraries. EMBO J16: 1501-1507.
42. Ruiz, T., Lenox, C., Radermacher, M. and Mintz, K.P. (2006) Novel surface structures are associated with the adhesion of Actinobacillus actinomycetemcomitans to collagen. Infect Immun74: 6163-6170.
43. Schmid, D., Baici, A., Gehring, H. and Christen, P. (1994) Kinetics of molecular chaperone action. Science263: 971-973.
44. Sijbrandi, R., Urbanus, M.L., ten Hagen-Jongman, C.M. et al. (2003) Signal recognition particle (SRP)-mediated targeting and Sec-dependent translocation of an extracellular Escherichia coli protein. J Biol Chem278: 4654-4659.
45. Slots, J., Reynolds, H.S. and Genco, R.J. (1980) Actinobacillus actinomycetemcomitans in human periodontal disease: a cross-sectional microbiological investigation. Infect Immun29: 1013-1020.
46. van der Sluis, E.O. and Driessen, A.J. (2006) Stepwise evolution of the Sec machinery in Proteobacteria. Trends Microbiol14: 105-108.
47. Sreenivasan, P.K., LeBlanc, D.J., Lee, L.N. and Fives-Taylor, P. (1991) Transformation of Actinobacillus actinomycetemcomitans by electroporation, utilizing constructed shuttle plasmids. Infect Immun59: 4621-4627.
48. Tang, G., Kitten, T., Munro, C.L., Wellman, G.C. and Mintz, K.P. (2008) EmaA, a potential virulence determinant of Aggregatibacter actinomycetemcomitans in infective endocarditis. Infect Immun76: 2316-2324.
49. Thanabalu, T., Koronakis, E., Hughes, C. and Koronakis, V. (1998) Substrate-induced assembly of a contiguous channel for protein export from E. coli: reversible bridging of an inner-membrane translocase to an outer membrane exit pore. EMBO J17: 6487-6496.
50. Tian, H. and Beckwith, J. (2002) Genetic screen yields mutations in genes encoding all known components of the Escherichia coli signal recognition particle pathway. J Bacteriol184: 111-118.
51. Tomilo, M., Wilkinson, K.S. and Ryan, P. (1994) Can a signal sequence become too hydrophobic?J Biol Chem269: 32016-32021.
52. Valent, Q.A., Kendall, D.A., High, S., Kusters, R., Oudega, B. and Luirink, J. (1995) Early events in preprotein recognition in E. coli: interaction of SRP and trigger factor with nascent polypeptides. EMBO J14: 5494-5505.
53. Van Durme, J., Maurer-Stroh, S., Gallardo, R., Wilkinson, H., Rousseau, F. and Schymkowitz, J. (2009) Accurate prediction of DnaK-peptide binding via homology modeling and experimental data. PLoS Comput Biol5: e1000475.
54. Walter, P. and Johnson, A.E. (1994) Signal sequence recognition and protein targeting to the endoplasmic reticulum membrane. Annu Rev Cell Biol10: 87-119.
55. Watanabe, M. and Blobel, G. (1989) SecB functions as a cytosolic signal recognition factor for protein export in E. coli. Cell58: 695-705.
56. Wild, J., Altman, E., Yura, T. and Gross, C.A. (1992a) DnaK and DnaJ heat shock proteins participate in protein export in Escherichia coli. Genes Dev6: 1165-1172.
57. Wild, J., Kamath-Loeb, A., Ziegelhoffer, E., Lonetto, M., Kawasaki, Y. and Gross, C.A. (1992b) Partial loss of function mutations in DnaK, the Escherichia coli homologue of the 70-kDa heat shock proteins, affect highly conserved amino acids implicated in ATP binding and hydrolysis. Proc Natl Acad Sci U S A89: 7139-7143.
58. Wild, J., Rossmeissl, P., Walter, W.A. and Gross, C.A. (1996) Involvement of the DnaK-DnaJ-GrpE chaperone team in protein secretion in Escherichia coli. J Bacteriol178: 3608-3613.
59. Yu, C., Ruiz, T., Lenox, C. and Mintz, K.P. (2008) Functional mapping of an oligomeric autotransporter adhesin of Aggregatibacter actinomycetemcomitans. J Bacteriol190: 3098-3109.
60. Zambon, J.J. (1985) Actinobacillus actinomycetemcomitans in human periodontal disease. J Clin Periodontol12: 1-20.
61. Zhu, X., Zhao, X., Burkholder, W.F. et al. (1996) Structural analysis of substrate binding by the molecular chaperone DnaK. Science272: 1606-1614.