The cell envelope proteome of Aggregatibacter actinomycetemcomitans

Molecular Oral Microbiology

Volumn 30, Issue 2, 2015, Pages 97-110

  Smith, K P ^a   Fields, J G ^b   Voogt, R D ^a   Deng, B ^b   Lam, Y W ^b   Mintz, K P ^a  

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

^b UNIVERSITY OF VERMONT   (United States)

Author keywords

Bioinformatics; Membrane proteins; Periodontal disease; Secretion systems

Indexed keywords

ADHESIN; AMINO ACID; BACTERIAL PROTEIN; CELL ENVELOPE PROTEIN; CHAPERONE; CYTOPLASM PROTEIN; ENVELOPE PROTEIN; IRON; LIPOPROTEIN; PERIPLASMIC PROTEIN; PORIN; PROTEOME; SUGAR; UNCLASSIFIED DRUG; UREA; BACTERIAL SECRETION SYSTEM; OUTER MEMBRANE PROTEIN;

AGGREGATIBACTER ACTINOMYCETEMCOMITANS; ARTICLE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL MEMBRANE; BACTERIAL STRAIN; BIOINFORMATICS; MASS SPECTROMETRY; NONHUMAN; OPEN READING FRAME; PREDICTION; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; PROTEOMICS; SURFACE PROPERTY; TYPE I SECRETION SYSTEM; TYPE II SECRETION SYSTEM; TYPE V SECRETION SYSTEM; BACTERIAL SECRETION SYSTEM; BIOLOGY; CELL MEMBRANE; CELL WALL; GENETICS; METABOLISM; PERIPLASM;

AGGREGATIBACTER ACTINOMYCETEMCOMITANS; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL SECRETION SYSTEMS; CELL MEMBRANE; CELL WALL; COMPUTATIONAL BIOLOGY; GENOME, BACTERIAL; PERIPLASM; PROTEOME;

EID: 84924407635     PISSN: 20411006     EISSN: 20411014     Source Type: Journal    
DOI: 10.1111/omi.12074     Document Type: Article

References (74)

1. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. and Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
2. Asakawa, R., Komatsuzawa, H., Kawai, T. et al. (2003) Outer membrane protein 100, a versatile virulence factor of Actinobacillus actinomycetemcomitans. Mol Microbiol 50: 1125-1139.
3. Ashburner, M., Ball, C.A., Blake, J.A. et al. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25: 25-29.
4. Bendtsen, J.D., Nielsen, H., Widdick, D., Palmer, T. and Brunak, S. (2005) Prediction of twin-arginine signal peptides. BMC Bioinformatics 6: 167.
5. Berven, F.S., Flikka, K., Jensen, H.B. and Eidhammer, I. (2004) BOMP: a program to predict integral beta-barrel outer membrane proteins encoded within genomes of Gram-negative bacteria. Nucleic Acids Res 32: W394-W399.
6. Berven, F.S., Karlsen, O.A., Straume, A.H. et al. (2006) Analysing the outer membrane subproteome of Methylococcus capsulatus (Bath) using proteomics and novel biocomputing tools. Arch Microbiol 184: 362-377.
7. Boersema, P.J., Raijmakers, R., Lemeer, S., Mohammed, S. and Heck, A.J. (2009) Multiplex peptide stable isotope dimethyl labeling for quantitative proteomics. Nat Protoc 4: 484-494.
8. Braun, R.J., Kinkl, N., Beer, M. and Ueffing, M. (2007) Two-dimensional electrophoresis of membrane proteins. Anal Bioanal Chem 389: 1033-1045.
9. Brown, S.A. and Whiteley, M. (2007) A novel exclusion mechanism for carbon resource partitioning in Aggregatibacter actinomycetemcomitans. J Bacteriol 189: 6407-6414.
10. Chen, T., Yu, W.H., Izard, J., Baranova, O.V., Lakshmanan, A. and Dewhirst, F.E. (2010) The Human Oral Microbiome Database: a web accessible resource for investigating oral microbe taxonomic and genomic information. Database (Oxford) 2010: baq013.
11. Conesa, A., Gotz, S., Garcia-Gomez, J.M., Terol, J., Talon, M. and Robles, M. (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674-3676.
12. Darveau, R.P. (2010) Periodontitis: a polymicrobial disruption of host homeostasis. Nat Rev Microbiol 8: 481-490.
13. Davidson, A.L. and Chen, J. (2004) ATP-binding cassette transporters in bacteria. Annu Rev Biochem 73: 241-268.
14. Dephoure, N. and Gygi, S.P. (2011) A solid phase extraction-based platform for rapid phosphoproteomic analysis. Methods 54: 379-386.
15. Di Bonaventura, M.P., DeSalle, R., Pop, M. et al. (2009) Complete genome sequence of Aggregatibacter (Haemophilus) aphrophilus NJ8700. J Bacteriol 191: 4693-4694.
16. Emanuelsson, O., Brunak, S., von Heijne, G. and Nielsen, H. (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2: 953-971.
17. Finn, R.D., Clements, J. and Eddy, S.R. (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39: W29-W37.
18. Fives-Taylor, P.M., Meyer, D.H., Mintz, K.P. and Brissette, C. (1999) Virulence factors of Actinobacillus actinomycetemcomitans. Periodontol 2000 20: 136-167.
19. Gardy, J.L. and Brinkman, F.S. (2006) Methods for predicting bacterial protein subcellular localization. Nat Rev Microbiol 4: 741-751.
20. Garg, A. and Gupta, D. (2008) VirulentPred: a SVM based prediction method for virulent proteins in bacterial pathogens. BMC Bioinformatics 9: 62.
21. Gygi, S.P., Corthals, G.L., Zhang, Y., Rochon, Y. and Aebersold, R. (2000) Evaluation of two-dimensional gel electrophoresis-based proteome analysis technology. Proc Natl Acad Sci USA 97: 9390-9395.
22. Herskovits, A.A. and Bibi, E. (2000) Association of Escherichia coli ribosomes with the inner membrane requires the signal recognition particle receptor but is independent of the signal recognition particle. Proc Natl Acad Sci USA 97: 4621-4626.
23. Hsu, J.L., Huang, S.Y., Chow, N.H. and Chen, S.H. (2003) Stable-isotope dimethyl labeling for quantitative proteomics. Anal Chem 75: 6843-6852.
24. Huang, C.Z., Lin, X.M., Wu, L.N. et al. (2006) Systematic identification of the subproteome of Escherichia coli cell envelope reveals the interaction network of membrane proteins and membrane-associated peripheral proteins. J Proteome Res 5: 3268-3276.
25. Jain, E., Bairoch, A., Duvaud, S. et al. (2009) Infrastructure for the life sciences: design and implementation of the UniProt website. BMC Bioinformatics 10: 136.
26. Jorth, P. and Whiteley, M. (2010) Characterization of a novel riboswitch-regulated lysine transporter in Aggregatibacter actinomycetemcomitans. J Bacteriol 192: 6240-6250.
27. Jorth, P., Trivedi, U., Rumbaugh, K. and Whiteley, M. (2013) Probing bacterial metabolism during infection using high-resolution transcriptomics. J Bacteriol 195: 4991-4998.
28. Juncker, A.S., Willenbrock, H., Von Heijne, G., Brunak, S., Nielsen, H. and Krogh, A. (2003) Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci 12: 1652-1662.
29. Kaplan, A.H., Weber, D.J., Oddone, E.Z. and Perfect, J.R. (1989) Infection due to Actinobacillus actinomycetemcomitans: 15 cases and review. Rev Infect Dis 11: 46-63.
30. Koebnik, R., Locher, K.P. and Van Gelder, P. (2000) Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol Microbiol 37: 239-253.
31. Komatsuzawa, H., Asakawa, R., Kawai, T. et al. (2002) Identification of six major outer membrane proteins from Actinobacillus actinomycetemcomitans. Gene 288: 195-201.
32. Kram, K.E., Hovel-Miner, G.A., Tomich, M. and Figurski, D.H. (2008) Transcriptional regulation of the tad locus in Aggregatibacter actinomycetemcomitans: a termination cascade. J Bacteriol 190: 3859-3868.
33. Krogh, A., Larsson, B., von Heijne, G. and Sonnhammer, E.L. (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305: 567-580.
34. Lally, E.T., Golub, E.E., Kieba, I.R. et al. (1989) Analysis of the Actinobacillus actinomycetemcomitans leukotoxin gene. Delineation of unique features and comparison to homologous toxins. J Biol Chem 264: 15451-15456.
35. Lee, P.A., Tullman-Ercek, D. and Georgiou, G. (2006) The bacterial twin-arginine translocation pathway. Annu Rev Microbiol 60: 373-395.
36. Libby, E.A., Roggiani, M. and Goulian, M. (2012) Membrane protein expression triggers chromosomal locus repositioning in bacteria. Proc Natl Acad Sci USA 109: 7445-7450.
37. Liu, H., Lin, D. and Yates, J.R. 3rd (2002) Multidimensional separations for protein/peptide analysis in the post-genomic era. Biotechniques 32: 898, 900, 902 passim.
38. Marti, S., Sanchez-Cespedes, J., Oliveira, E., Bellido, D., Giralt, E. and Vila, J. (2006) Proteomic analysis of a fraction enriched in cell envelope proteins of Acinetobacter baumannii. Proteomics 6(Suppl 1): S82-S87.
39. Mayer, M.P., Bueno, L.C., Hansen, E.J. and DiRienzo, J.M. (1999) Identification of a cytolethal distending toxin gene locus and features of a virulence-associated region in Actinobacillus actinomycetemcomitans. Infect Immun 67: 1227-1237.
40. Mintz, K.P. (2004) Identification of an extracellular matrix protein adhesin, EmaA, which mediates the adhesion of Actinobacillus actinomycetemcomitans to collagen. Microbiology 150: 2677-2688.
41. Mintz, K.P. and Fives-Taylor, P.M. (1994) Adhesion of Actinobacillus actinomycetemcomitans to a human oral cell line. Infect Immun 62: 3672-3678.
42. Olsen, I., Shah, H.N. and Gharbia, S.E. (1999) Taxonomy and biochemical characteristics of Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis. Periodontol 2000 20: 14-52.
43. Pao, S.S., Paulsen, I.T. and Saier, M.H. Jr (1998) Major facilitator superfamily. Microbiol Mol Biol Rev 62: 1-34.
44. Paturel, L., Casalta, J.P., Habib, G., Nezri, M. and Raoult, D. (2004) Actinobacillus actinomycetemcomitans endocarditis. Clin Microbiol Infect 10: 98-118.
45. Petersen, T.N., Brunak, S., von Heijne, G. and Nielsen, H. (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8: 785-786.
46. Postma, P.W., Lengeler, J.W. and Jacobson, G.R. (1993) Phosphoenolpyruvate:carbohydrate phosphotransferase systems of bacteria. Microbiol Rev 57: 543-594.
47. Punta, M., Coggill, P.C., Eberhardt, R.Y. et al. (2012) The Pfam protein families database. Nucleic Acids Res 40: D290-D301.
48. Rabilloud, T. (2009) Membrane proteins and proteomics: love is possible, but so difficult. Electrophoresis 30(Suppl 1): S174-S180.
49. Rahamat-Langendoen, J.C., van Vonderen, M.G., Engstrom, L.J., Manson, W.L., van Winkelhoff, A.J. and Mooi-Kokenberg, E.A. (2011) Brain abscess associated with Aggregatibacter actinomycetemcomitans: case report and review of literature. J Clin Periodontol 38: 702-706.
50. Rigel, N.W. and Silhavy, T.J. (2012) Making a beta-barrel: assembly of outer membrane proteins in Gram-negative bacteria. Curr Opin Microbiol 15: 189-193.
51. Rose, J.E., Meyer, D.H. and Fives-Taylor, P.M. (2003) Aae, an autotransporter involved in adhesion of Actinobacillus actinomycetemcomitans to epithelial cells. Infect Immun 71: 2384-2393.
52. Rylev, M., Abduljabar, A.B., Reinholdt, J. et al. (2011) Proteomic and immunoproteomic analysis of Aggregatibacter actinomycetemcomitans JP2 clone strain HK1651. J Proteomics 74: 2972-2985.
53. Ryter, A. (1968) Association of the nucleus and the membrane of bacteria: a morphological study. Bacteriol Rev 32: 39-54.
54. Saier, M.H. Jr (2000) Families of transmembrane transporters selective for amino acids and their derivatives. Microbiology 146(Pt 8): 1775-1795.
55. Saier, M.H. Jr, Yen, M.R., Noto, K., Tamang, D.G. and Elkan, C. (2009) The Transporter Classification Database: recent advances. Nucleic Acids Res 37: D274-D278.
56. Scannapieco, F.A. (1999) Role of oral bacteria in respiratory infection. J Periodontol 70: 793-802.
57. Silhavy, T.J., Kahne, D. and Walker, S. (2010) The bacterial cell envelope. Cold Spring Harb Perspect Biol 2: a000414.
58. Solis, N. and Cordwell, S.J. (2011) Current methodologies for proteomics of bacterial surface-exposed and cell envelope proteins. Proteomics 11: 3169-3189.
59. Sreenivasan, P.K., Meyer, D.H. and Fives-Taylor, P.M. (1993) Factors influencing the growth and viability of Actinobacillus actinomycetemcomitans. Oral Microbiol Immunol 8: 361-369.
60. Syrjanen, S.M., Alakuijala, L., Alakuijala, P., Markkanen, S.O. and Markkanen, H. (1990) Free amino acid levels in oral fluids of normal subjects and patients with periodontal disease. Arch Oral Biol 35: 189-193.
61. 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 Immun 76: 2316-2324.
62. Tang, G., Kawai, T., Komatsuzawa, H. and Mintz, K.P. (2012) Lipopolysaccharides mediate leukotoxin secretion in Aggregatibacter actinomycetemcomitans. Mol Oral Microbiol 27: 70-82.
63. Tatusov, R.L., Koonin, E.V. and Lipman, D.J. (1997) A genomic perspective on protein families. Science 278: 631-637.
64. Tokuda, H. and Matsuyama, S. (2004) Sorting of lipoproteins to the outer membrane in E. coli. Biochim Biophys Acta 1693: 5-13.
65. Tomich, M., Planet, P.J. and Figurski, D.H. (2007) The tad locus: postcards from the widespread colonization island. Nat Rev Microbiol 5: 363-375.
66. Tseng, T.T., Tyler, B.M. and Setubal, J.C. (2009) Protein secretion systems in bacterial-host associations, and their description in the Gene Ontology. BMC Microbiol 9(Suppl 1): S2.
67. Wang, Y., Liu, A. and Chen, C. (2005) Genetic basis for conversion of rough-to-smooth colony morphology in Actinobacillus actinomycetemcomitans. Infect Immun 73: 3749-3753.
68. Washburn, M.P. (2004) Utilisation of proteomics datasets generated via multidimensional protein identification technology (MudPIT). Brief Funct Genomic Proteomic 3: 280-286.
69. Wu, S., Zhu, Z., Fu, L., Niu, B. and Li, W. (2011) WebMGA: a customizable web server for fast metagenomic sequence analysis. BMC Genomics 12: 444.
70. Yu, C.S., Lin, C.J. and Hwang, J.K. (2004) Predicting subcellular localization of proteins for Gram-negative bacteria by support vector machines based on n-peptide compositions. Protein Sci 13: 1402-1406.
71. Yu, N.Y., Wagner, J.R., Laird, M.R. et al. (2010) PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes. Bioinformatics 26: 1608-1615.
72. Zambon, J.J., Slots, J. and Genco, R.J. (1983) Serology of oral Actinobacillus actinomycetemcomitans and serotype distribution in human periodontal disease. Infect Immun 41: 19-27.
73. Zhou, J. and Rudd, K.E. (2013) EcoGene 3.0. Nucleic Acids Res 41: D613-D624.
74. Zijnge, V., Kieselbach, T. and Oscarsson, J. (2012) Proteomics of protein secretion by Aggregatibacter actinomycetemcomitans. PLoS ONE 7: e41662.