Extracellular proteome of a highly invasive multidrug-resistant clinical strain of acinetobacter baumannii

Journal of Proteome Research

Volumn 11, Issue 12, 2012, Pages 5678-5694

  Mendez, Jose Antonio ^a   Soares, Nelson C ^a   Mateos, Jesús ^b   Gayoso, Carmen ^a   Rumbo, Carlos ^a   Aranda, Jesús ^a   Tomas, Maria ^a   Bou, Germán ^a  

^a HOSPITAL JUAN CANALEJO   (Spain)

^b INIBIC   (Spain)

Author keywords

2 DE; Acinetobacter baumannii; extracellular proteome; MALDI TOF TOF; outer membrane vesicles; pathogenesis; proteomics; secretome; virulence

Indexed keywords

BACTERIAL PROTEIN; FREELY SOLUBLE EXTRACELLULAR PROTEIN; HYDROGEN PEROXIDE; OUTER MEMBRANE VESICLE PROTEIN; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ACINETOBACTER BAUMANNII; ARTICLE; BACTERIAL CELL; BACTERIAL STRAIN; BACTERIAL VIRULENCE; MACROPHAGE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MULTIDRUG RESISTANCE; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ISOLATION; PROTEIN PURIFICATION; PROTEOMICS;

ACINETOBACTER BAUMANNII; ANIMALS; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL SECRETION SYSTEMS; CELL LINE, TUMOR; CELL MEMBRANE; CULTURE MEDIA; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; EXTRACELLULAR SPACE; HYDROGEN PEROXIDE; MACROPHAGES; MICE; MICROBIAL VIABILITY; OXIDATIVE STRESS; PROTEIN TRANSPORT; PROTEOME; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; VIRULENCE FACTORS;

ACINETOBACTER BAUMANNII; BACTERIA (MICROORGANISMS); OAT MOSAIC VIRUS;

EID: 84870891809     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr300496c     Document Type: Article

References (66)

1. Anstey, N. M.; Currie, B. J.; Hassell, M.; Palmer, D.; Dwyer, B.; Seifert, H. Community-acquired bacteremic Acinetobacter pneumonia in tropical Australia is caused by diverse strains of Acinetobacter baumannii, with carriage in the throat in at-risk goups J. Clin. Microbiol. 2002, 40 (2) 685-686
2. Anstey, N. M.; Currie, B. J.; Withnall, K. M. Community-acquired Acinetobacter pneumonia in the northern territory of Australia Clin. Infect. Dis. 1992, 14 (1) 83-91
3. Tao, C.; Kang, M.; Chen, Z.; Xie, Y.; Fan, H.; Qin, L.; Ma, Y. Microbiologic study of the pathogens isolated from wound culture among Wenchuan earthquake survivors Diagn. Microbiol. Infect. Dis. 2009, 63 (3) 268-270
4. Charnot-Katsikas, A.; Dorafshar, A. H.; Aycock, J. K.; David, M. Z.; Weber, S. G.; Frank, K. M. Two cases of necrotizing fasciitis due to Acinetobacter baumannii J. Clin. Microbiol. 2009, 47 (1) 258-263
5. Acosta, J.; Merino, M.; Viedma, E.; Poza, M.; Sanz, F.; Otero, J. R.; Chaves, F.; Bou, G. Multidrug-Resistance Acinetobacter baummannii harbouring OXA-24 carbapenemase, Spain Emerg. Infect. Dis. 2011, 17 (6) 1064-1067
6. Russo, T. A.; Luke, N. R.; Beanan, J. M.; Olson, R.; Sauberan, S. L.; MacDonald, U.; Schultz, L. W.; Umland, T. C.; Campagnari, A. A. The K1 capsular polysaccharide of Acinetobacter baumannii Strain 307-0294 is a major virulence factor Infect. Immun. 2010, 78 (9) 3993-4000
7. Smith, M. G.; Gianoulis, T. A.; Pukatzki, S.; Mekalanos, J. J.; Ornston, L. N.; Gerstein, M.; Snyder, M. New insights into Acinetobacter baumannii pathogenesis revealed by high-density pyrosequencing and transposon mutagenesis Genes Dev. 2007, 21 (5) 601-614
8. Choi, C. H.; Lee, E. Y.; Lee, Y. C.; Park, T. I.; Kim, H. J.; Hyun, S. H.; Kim, S. A.; Lee, S.-K.; Lee, J. C. Outer membrane protein 38 of Acinetobacter baumannii localizes to the mitochondria and induces apoptosis of epithelial cells Cell Microbiol. 2005, 7 (8) 1127-1138
9. Choi, Y. W.; Park, S. A.; Lee, H. W.; Kim, D. S.; Lee, N. G. Analysis of growth phase-dependent proteome profiles reveals differential regulation of mRNA and protein in Helicobacter pylori Proteomics 2008, 8 (13) 2665-2675
10. Antunes, L. C. S.; Imperi, F.; Carattoli, A.; Visca, P. Deciphering the multifactorial nature of Acinetobacter baumannii pathogenicity PLoS ONE 2011, 6 (8) e22674
11. Stathopoulos, C.; Hendrixson, D. R.; Thanassi, D. G.; Hultgren, S. J.; St. Geme, J. W.; Curtiss, R. Secretion of virulence determinants by the general secretory pathway in Gram-negative pathogens: an evolving story Microbes Infect. 2000, 2 (9) 1061-1072
12. Pierson, T.; Matrakas, D.; Taylor, Y. U.; Manyam, G.; Morozov, V. N.; Zhou, W.; van Hoek, M. L. Proteomic characterization and functional analysis of outer membrane vesicles of Francisella novicida suggests possible role in virulence and use as a vaccine J. Proteome Res. 2010, 10 (3) 954-967
13. McConnell, M. J.; Rumbo, C.; Bou, G.; Pachón, J. Outer membrane vesicles as an cellular vaccine against Acinetobacter baumannii Vaccine 2011, 29 (34) 5705-5710
14. Kwon, S.-O.; Gho, Y. S.; Lee, J. C.; Kim, S. I. Proteome analysis of outer membrane vesicles from clinical Acinetobacter baumannii isolate FEMS Microbiol. Lett. 2009, 297, 159-156
15. Jin, J. S.; Kwon, S.-O.; Moon, D. C.; Gurung, M.; Lee, J. H.; Kim, S. I.; Lee, J. C. Acinetobacter baumannii secretes cytotoxic outer membrane protein A via outer membrane vesicles PLoS ONE 2011, 6 (2) e17027
16. Merino, M.; Acosta, J.; Poza, M.; Sanz, F.; Beceiro, A.; Chaves, F.; Bou, G. OXA-24 Carbapenemase gene flanked by XerC/XerD-Like recombination sites in different plasmids from different Acinetobacter species isolated during a nosocomial outbreak Antimicrob. Agents Chemother. 2010, 54 (6) 2724-2727
17. Desvaux, M.; Hébraud, M.; Talon, R.; Henderson, I. R. Secretion and subcellular localizations of bacterial proteins: a semantic awareness issue Trends Microbiol. 2009, 17 (4) 139-145
18. Rumbo, C.; Fernandez-Moreira, E.; Merino, M.; Poza, M.; Mendez, J. A.; Soares, N. C.; Mosquera, A.; Chaves, F.; Bou, G. Horizontal transfer of the OXA-24 carbapenemase gene via outer membrane vesicles: A new mechanism of dissemination of carbapenem resistance genes in Acinetobacter baumannii Antimicrob. Agents Chemother. 2011, 55 (7) 3084-3090
19. Deng, W.; de Hoog, C. L.; Yu, H. B.; Li, Y.; Croxen, M. A.; Thomas, N. A.; Puente, J. L.; Foster, L. J.; Finlay, B. B. A comprehensive proteomic analysis of the Type III secretome of Citrobacter rodentium J. Biol. Chem. 2010, 285 (9) 6790-6800
20. Bradford, M. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of portein-dye binding Anal. Biochem. 1976, 72, 248-54
21. Ramagli, L. Quantifying protein in 2-D PAGE solubilization buffers Methods Mol. Biol. 1999, 112, 99-103
22. Ibrahim, K. S.; Muniyandi, J.; S., K. P. Purification and characterization of manganese-dependent alkaline serina protease from Bacillus pumilus TMS55 J. Microbiol. Biotechnol. 2011, 21 (1) 20-7
23. Soares, N. C.; Cabral, M.; Parreira, J.; Gayoso, C.; Barba, M.; Bou, G. 2-DE analysis indicates that Acinetobacter baumannii displays a robust and versatile metabolism Proteome Sci. 2009, 7 (1) 37
24. Lopez-Ferrer, D.; Martínez-Bartolomé, S.; Villar, M.; Campillos, M.; Martín-Maroto, F.; Vázquez, J. Statistical model for large-scale peptide identification in databases from Tandem Mass Spectra using SEQUEST Anal. Chem. 2004, 76 (23) 6853-6860
25. Soares, N. C.; Cabral, M. P.; Gayoso, C.; Mallo, S.; Rodriguez-Velo, P.; Fernández-Moreira, E.; Bou, G. Associating growth-phase-related changes in the proteome of Acinetobacter baumannii with increased resistance to oxidative stress J. Proteome Res. 2010, 9 (4) 1951-1964
26. Gardy, J. L.; Laird, M. R.; Chen, F.; Rey, S.; Walsh, C. J.; Ester, M.; Brinkman, F. S. L. PSORTb v.2.0: Expanded prediction of bacterial protein subcellular localization and insights gained from comparative proteome analysis Bioinformatics 2005, 21 (5) 617-623
27. Juncker, A. S.; Willenbrock, H.; von Heijne, G.; Brunak, S.; Nielsen, H.; Krogh, A. Prediction of lipoprotein signal peptides in Gram-negative bacteria Protein Sci. 2003, 12 (8) 1652-1662
28. Bendtsen, J.; Nielsen, H.; Widdick, D.; Palmer, T.; Brunak, S. Prediction of twin-arginine signal peptides BMC Bioinform. 2005, 6 (1) 167
29. Rose, R. W.; Brüser, T.; Kissinger, J. C.; Pohlschröder, M. Adaptation of protein secretion to extremely high-salt conditions by extensive use of the twin-arginine translocation pathway Mol. Microbiol. 2002, 45 (4) 943-950
30. Bendtsen, J.; Kiemer, L.; Fausboll, A.; Brunak, S. Non-classical protein secretion in bacteria BMC Microbiol. 2005, 5 (1) 58
31. Aranda, J.; Bardina, C.; Beceiro, A.; Rumbo, S.; Cabral, M. P.; Barbé, J.; Bou, G. Acinetobacter baumannii RecA protein in repair of DNA damage, antimicrobial resistance, general stress response, and virulence J. Bacteriol. 2011, 193 (15) 3740-3747
32. Galka, F.; Wai, S. N.; Kusch, H.; Engelmann, S.; Hecker, M.; Schmeck, B.; Hippenstiel, S.; Uhlin, B. E.; Steinert, M. Proteomic characterization of the whole secretome of Legionella pneumophila and functional analysis of outer membrane vesicles Infect. Immun. 2008, 76 (5) 1825-1836
33. Vallejo, M. C.; Nakayasu, E. S.; Matsuo, A. L.; Sobreira, T. J. P.; Longo, L. V. G.; Ganiko, L.; Almeida, I. C.; Puccia, R. Vesicle and vesicle-free extracellular proteome of Paracoccidioides brasiliensis: Comparative analysis with other pathogenic fungi J. Proteome Res. 2012, 11 (3) 1676-1685
34. Huang, D.; Ou, B.; R.L., P. Chemistry behind antioxidant capacity assays J. Agric. Food Chem. 2005, 53, 1841-1856
35. Cosgrove, K.; Coutts, G.; Jonsson, I.-M.; Tarkowski, A.; Kokai-Kun, J. F.; Mond, J. J.; Foster, S. J. Catalase (KatA) and alkyl hydroperoxide reductase (AhpC) have compensatory roles in peroxide stress resistance and are required for survival, persistence, and nasal colonization in Staphylococcus aureus J. Bacteriol. 2007, 189 (3) 1025-1035
36. Hampton, M. B.; Kettle, A. J.; Winterbourn, C. C. Involvement of superoxide and myeloperoxidase in oxygen-dependent killing of Staphylococcus aureus by neutrophils Infect. Immun. 1996, 64 (9) 3512-3517
37. Nunoshiba, T.; DeRojas-Walker, T.; Tannenbaum, S. R.; Demple, B. Roles of nitric oxide in inducible resistance of Escherichia coli to activated murine macrophages Infect. Immun. 1995, 63 (3) 794-798
38. Nunoshiba, T.; deRojas-Walker, T.; Wishnok, J. S.; Tannenbaum, S. R.; Demple, B. Activation by nitric oxide of an oxidative-stress response that defends Escherichia coli against activated macrophages Proc. Natl. Acad. Sci. 1993, 90 (21) 9993-9997
39. West, A. P.; Brodsky, I. E.; Rahner, C.; Woo, D. K.; Erdjument-Bromage, H.; Tempst, P.; Walsh, M. C.; Choi, Y.; Shadel, G. S.; Ghosh, S. TLR signalling augments macrophage bactericidal activity through mitochondrial ROS Nature 2011, 472 (7344) 476-480
40. Berlanda Scorza, F.; Doro, F.; Rodríguez-Ortega, M. J.; Stella, M.; Liberatori, S.; Taddei, A. R.; Serino, L.; Gomes Moriel, D.; Nesta, B.; Fontana, M. R.; Spagnuolo, A.; Pizza, M.; Norais, N.; Grandi, G. Proteomics characterization of outer membrane vesicles from the extraintestinal pathogenic Escherichia coli ΔtolR IHE3034 mutant Mol. Cell. Proteomics 2008, 7 (3) 473-485
41. Niemann, G. S.; Brown, R. N.; Gustin, J. K.; Stufkens, A.; Shaikh-Kidwai, A. S.; Li, J.; McDermott, J. E.; Brewer, H. M.; Schepmoes, A.; Smith, R. D.; Adkins, J. N.; Heffron, F. Discovery of novel secreted virulence factors from Salmonella enterica Serovar Typhimurium by proteomic analysis of culture supernatants Infect. Immun. 2011, 79 (1) 33-43
42. Braunstein, M.; Espinosa, B. J.; Chan, J.; Belisle, J. T.; R. Jacobs, W. SecA2 functions in the secretion of superoxide dismutase A and in the virulence of Mycobacterium tuberculosis Mol. Microbiol. 2003, 48 (2) 453-464
43. Song, C.; Kumar, A.; Saleh, M. Bioinformatic comparison of bacterial secretomes Genomics, Proteomics Bioinform. 2009, 7 (1-2) 37-46
44. Bomberger, J. M.; MacEachran, D. P.; Coutermarsh, B. A.; Ye, S.; O'Toole, G. A.; Stanton, B. A. Long-Distance Delivery of bacterial virulence factors by Pseudomonas aeruginosa outer membrane vesicles PLoS Pathog. 2009, 5 (4) e1000382
45. Hal Jones, C.; Danese, P. N.; Pinkner, J. S.; Silhavy, T. J.; Hultgren, S. J. The chaperone-assisted membrane release and folding pathway is sensed by two signal transduction systems EMBO J. 1997, 16 (21) 6394-6406
46. Puorger, C.; Vetsch, M.; Wider, G.; Glockshuber, R. Structure, folding and stability of FimA, themain structural subunit of Type 1 Pili from uropathogenic Escherichia coli strains J. Mol. Biol. 2011, 412 (3) 520-535
47. Altschul, S. F.; Gish, W.; Miller, W.; Myers, E. W.; Lipman, D. J. Basic local alignment search tool J. Mol. Biol. 1990, 215 (3) 403-410
48. Altschul, S. F.; Madden, T. L.; Schäffer, A. A.; Zhang, J.; Zhang, Z.; Miller, W.; Lipman, D. J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Nucleic Acids Res. 1997, 25 (17) 3389-3402
49. Yeo, H.-J.; Yokoyama, T.; Walkiewicz, K.; Kim, Y.; Grass, S.; Geme, J. W. S. The structure of the Haemophilus influenzae HMW1 Pro-piece reveals a structural domain essential for bacterial two-partner secretion J. Biol. Chem. 2007, 282 (42) 31076-31084
50. Jacob-Dubuisson, F.; Locht, C.; Antoine, R. Two-partner secretion in Gram-negative bacteria: a thrifty, specific pathway for large virulence proteins Mol. Microbiol. 2001, 40 (2) 306-313
51. Hayes, C. S.; Aoki, S. K.; Low, D. A. Bacterial contact-dependent delivery systems Annu. Rev. Genet. 2010, 44 (1) 71-90
52. Wu, J.-W.; Chen, X.-L. Extracellular metalloproteases from bacteria Appl. Microbiol. Biotechnol. 2011, 92 (2) 253-262
53. Chung, M. C.; Popova, T. G.; Millis, B. A.; Mukherjee, D. V.; Zhou, W.; Liotta, L. A.; Petricoin, E. F.; Chandhoke, V.; Bailey, C.; Popov, S. G. Secreted neutral metalloproteases of Bacillus anthracis as candidate pathogenic factors J. Biol. Chem. 2006, 281 (42) 31408-31418
54. Smith, H.; Stanley, J. L. Purification of the third factor of Anthrax toxin J. Gen. Microbiol. 1962, 29, 517-521
55. Thwaite, J. E.; Hibbs, S.; Titball, R. W.; Atkins, T. P. Proteolytic degradation of human antimicrobial peptide LL-37 by Bacillus anthracis may contribute to virulence Antimicrob. Agents Chemother. 2006, 50 (50) 2316-2322
56. Hube, B.; Stehr, F.; Bossenz, M.; Mazur, A.; Kretschmar, M.; Schäfer, W. Secreted lipases of Candida albicans;: cloning, characterisation and expression analysis of a new gene family with at least ten members Arch. Microbiol. 2000, 174 (5) 362-374
57. Choi, C. H.; Hyun, S. H.; Lee, J. Y.; Lee, J. S.; Lee, Y. S.; Kim, S. A.; Chae, J.-P.; Yoo, S. M.; Lee, J. C. Acinetobacter baumannii outer membrane protein A targets the nucleus and induces cytotoxicity Cell Microbiol. 2008, 10 (2) 309-319
58. Tullius, M. V.; Harth, G.; Horwitz, M. A. High extracellular levels of Mycobacterium tuberculosis glutamine synthetase and superoxide dismutase in actively growing cultures are due to high expression and extracellular stability rather than to a protein-specific export mechanism Infect. Immun. 2001, 69 (10) 6348-6363
59. Harth, G.; Horwitz, M. A. Export of recombinant Mycobacterium tuberculosis superoxide dismutase is dependent upon both information in the protein and mycobacterial export machinery J. Biol. Chem. 1999, 274 (7) 4281-4292
60. De Groote, M. A.; Ochsner, U. A.; Shiloh, M. U.; Nathan, C.; McCord, J. M.; Dinauer, M. C.; Libby, S. J.; Vazquez-Torres, A. s.; Xu, Y.; Fang, F. C. Periplasmic superoxide dismutase protects Salmonella from products of phagocyte NADPH-oxidase and nitric oxide synthase Proc. Natl. Acad. Sci. 1997, 94 (25) 13997-14001
61. Wilks, K. E.; Dunn, K. L. R.; Farrant, J. L.; Reddin, K. M.; Gorringe, A. R.; Langford, P. R.; Kroll, J. S. Periplasmic superoxide dismutase in Meningococcal Pathogenicity Infect. Immun. 1998, 66 (1) 213-217
62. San Mateo, L. R.; Toffer, K. L.; Orndorff, P. E.; Kawula, T. H. Neutropenia restores virulence to an attenuated Cu,Zn Superoxide dismutase-deficient Haemophilus ducreyi strain in the swine model of chancroid Infect. Immun. 1999, 67 (10) 5345-5351
63. Moro, A.; Ruiz-Cabello, F.; Fernandez-Cano, A.; Stock, R. P. A, G., Secretion by trypanosoma cruzi of a peptidyl-prolpyl cis-trans isomerase involved in cell infection EMBO J. 1995, 14 (11) 2483-2490
64. Moulder, J. W. Comparative Biology of intracellular parasitism Microbiol. Rev. 1985, 49 (3) 298-337
65. Hermans, P. W. M.; Adrian, P. V.; Albert, C.; Estevao, S.; Hoogenboezem, T.; Luijendijk, I. H. T.; Kamphausen, T.; Hammerschmidt, S. The Streptococcal lipoprotein rotamase A (SlrA) Is a functional peptidyl-prolyl isomerase involved in pneumococcal colonization J. Biol. Chem. 2006, 281 (2) 968-976
66. Inatsuka, C. S.; Julio, S. M.; Cotter, P. A. Bordetella filamentous hemagglutinin plays a critical role in immunomodulation, suggesting a mechanism for host specificity Proc. Natl. Acad. Sci. 2005, 102 (51) 18578-18583