Acinetobacter baumannii extracellular OXA-58 is primarily and selectively released via outer membrane vesicles after sec-dependent periplasmic translocation

Antimicrobial Agents and Chemotherapy

Volumn 59, Issue 12, 2015, Pages 7346-7354

  Liao, Yu Ting ^a   Kuo, Shu Chen ^a,b   Chiang, Ming Hsien ^c   Lee, Yi Tzu ^a,d   Sung, Wang Chou ^b   Chen, You Hsuan ^b   Chen, Te Li ^a,c,d   Fung, Chang Phone ^a,d  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^c NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

^d TAIPEI VETERANS GENERAL HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE PHOSPHATASE; BENZYLSULFONYL FLUORIDE; BETA LACTAMASE; BETA LACTAMASE OXA 58; CARBAPENEM; ENHANCED GREEN FLUORESCENT PROTEIN; ERYTHROSINE; IMIPENEM; KANAMYCIN; NITROCEFIN; PERIPLASMIC PROTEIN; PROTEINASE K; ROSE BENGAL; SAPONIN; SIGNAL PEPTIDE; TICARCILLIN; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATASE; BACTERIAL PROTEIN; BETA-LACTAMASE OXA-58, ACINETOBACTER BAUMANNII; CARBAPENEM DERIVATIVE; CARRIER PROTEIN; SECA PROTEIN, BACTERIA; TRANSLOCON;

ACINETOBACTER BAUMANNII; ARTICLE; BACTERIAL GROWTH; BACTERIAL OUTER MEMBRANE; BACTERIAL TRANSLOCATION; BACTERIUM CULTURE; BIOASSAY; CELL DENSITY; CELL FRACTIONATION; CELL SURFACE; COLONY FORMING UNIT; COMPUTER MODEL; CONTROLLED STUDY; CYTOLYSIS; CYTOPLASM; ENZYME DEGRADATION; ESCHERICHIA COLI; EXOSOME; EXTRACELLULAR SPACE; GENETIC VARIABILITY; HYDROLYSIS; INHIBITION ZONE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; GENETICS; METABOLISM; PERIPLASM; PROTEIN TRANSPORT; SECRETORY VESICLE;

ACINETOBACTER BAUMANNII; ADENOSINE TRIPHOSPHATASES; BACTERIAL PROTEINS; BETA-LACTAMASES; CARBAPENEMS; MEMBRANE TRANSPORT PROTEINS; PERIPLASM; PROTEIN TRANSPORT; ROSE BENGAL; SEC TRANSLOCATION CHANNELS; SECRETORY VESICLES;

EID: 84954533351     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01343-15     Document Type: Article

References (44)

1. Higgins PG, Dammhayn C, Hackel M, Seifert H. 2010. Global spread of carbapenem-resistant Acinetobacter baumannii. J Antimicrob Chemother 65:233-238. http://dx.doi.org/10.1093/jac/dkp428.
2. Lee NY, Lee HC, Ko NY, Chang CM, Shih HI, Wu CJ, Ko WC. 2007. Clinical and economic impact of multidrug resistance in nosocomial Acinetobacter baumannii bacteremia. Infect Control Hosp Epidemiol 28: 713-719. http://dx.doi.org/10.1086/517954.
3. Liao YT, Kuo SC, Lee YT, Chen CP, Lin SW, Shen LJ, Fung CP, Cho WL, Chen TL. 2014. Sheltering effect and indirect pathogenesis of carbapenem-resistant Acinetobacter baumannii in polymicrobial infection. Antimicrob Agents Chemother 58:3983-3990. http://dx.doi.org/10.1128 /AAC.02636-13.
4. Lee YT, Kuo SC, Yang SP, Lin YT, Tseng FC, Chen TL, Fung CP. 2012. Impact of appropriate antimicrobial therapy on mortality associated with Acinetobacter baumannii bacteremia: relation to severity of infection. Clin Infect Dis 55:209-215. http://dx.doi.org/10.1093/cid/cis385.
5. Lee YC, Huang YT, Tan CK, Kuo YW, Liao CH, Lee PI, Hsueh PR. 2011. Acinetobacter baumannii and Acinetobacter genospecies 13TU and 3 bacteraemia: comparison of clinical features, prognostic factors and outcomes. J Antimicrob Chemother 66:1839-1846. http://dx.doi.org /10.1093/jac/dkr200.
6. Trottier V, Namias N, Pust DG, Nuwayhid Z, Manning R, Marttos AC, Jr, Dunham MB, Schulman CI, McKenney MG. 2007. Outcomes of Acinetobacter baumannii infection in critically ill surgical patients. Surg Infect (Larchmt) 8:437-443. http://dx.doi.org/10.1089/sur.2006.029.
7. Higgins PG, Poirel L, Lehmann M, Nordmann P, Seifert H. 2009. OXA-143, a novel carbapenem-hydrolyzing class D β-lactamase in Acinetobacter baumannii. Antimicrob Agents Chemother 53:5035-5038. http: //dx.doi.org/10.1128/AAC.00856-09.
8. Chen TL, Wu RC, Shaio MF, Fung CP, Cho WL. 2008. Acquisition of a plasmid-borne blaOXA-58 gene with an upstream IS1008 insertion conferring a high level of carbapenem resistance to Acinetobacter baumannii. Antimicrob Agents Chemother 52:2573-2580. http://dx.doi.org/10.1128 /AAC.00393-08.
9. Valenzuela JK, Thomas L, Partridge SR, van der Reijden T, Dijkshoorn L, Iredell J. 2007. Horizontal gene transfer in a polyclonal outbreak of carbapenem-resistant Acinetobacter baumannii. J Clin Microbiol 45:453-460. http://dx.doi.org/10.1128/JCM.01971-06.
10. Schaar V, Nordstrom T, Morgelin M, Riesbeck K. 2011. Moraxella catarrhalis outer membrane vesicles carry β-lactamase and promote survival of Streptococcus pneumoniae and Haemophilus influenzae by inactivating amoxicillin. Antimicrob Agents Chemother 55:3845-3853. http: //dx.doi.org/10.1128/AAC.01772-10.
11. Kwon SO, Gho YS, Lee JC, Kim SI. 2009. Proteome analysis of outer membrane vesicles from a clinical Acinetobacter baumannii isolate. FEMS Microbiol Lett 297:150-156. http://dx.doi.org/10.1111/j.1574-6968.2009.01669.x.
12. Natale P, Bruser T, Driessen AJ. 2008. Sec-and Tat-mediated protein secretion across the bacterial cytoplasmic membrane-distinct translocases and mechanisms. Biochim Biophys Acta 1778:1735-1756. http://dx.doi.org/10.1016/j.bbamem.2007.07.015.
13. Pugsley AP. 1993. The complete general secretory pathway in gramnegative bacteria. Microbiol Rev 57:50-108.
14. Petersen TN, Brunak S, von Heijne G, Nielsen H. 2011. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785-786. http://dx.doi.org/10.1038/nmeth.1701.
15. Bendtsen JD, Nielsen H, Widdick D, Palmer T, Brunak S. 2005. Prediction of twin-arginine signal peptides. BMC Bioinformatics 6:167. http: //dx.doi.org/10.1186/1471-2105-6-167.
16. Koshland D, Botstein D. 1980. Secretion of β-lactamase requires the carboxy end of the protein. Cell 20:749-760. http://dx.doi.org/10.1016 /0092-8674(80)90321-9.
17. Kostakioti M, Newman CL, Thanassi DG, Stathopoulos C. 2005. Mechanisms of protein export across the bacterial outer membrane. J Bacteriol 187:4306-4314. http://dx.doi.org/10.1128/JB.187.13.4306-4314.2005.
18. Dalbey RE, Kuhn A. 2012. Protein traffic in gram-negative bacteria-how exported and secreted proteins find their way. FEMS Microbiol Rev 36: 1023-1045. http://dx.doi.org/10.1111/j.1574-6976.2012.00327.x.
19. Bonnington KE, Kuehn MJ. 2014. Protein selection and export via outer membrane vesicles. Biochim Biophys Acta 1843:1612-1619. http://dx.doi.org/10.1016/j.bbamcr.2013.12.011.
20. Lu X, Zhu H. 2005. Tube-gel digestion: a novel proteomic approach for high-throughput analysis of membrane proteins. Mol Cell Proteomics 4:1948-1958. http://dx.doi.org/10.1074/mcp.M500138-MCP200.
21. Chen JH, Chang YW, Yao CW, Chiueh TS, Huang SC, Chien KY, Chen A, Chang FY, Wong CH, Chen YJ. 2004. Plasma proteome of severe acute respiratory syndrome analyzed by two-dimensional gel electrophoresis and mass spectrometry. Proc Natl Acad Sci U S A 101:17039-17044. http://dx.doi.org/10.1073/pnas.0407992101.
22. Segers K, Anne J. 2011. Traffic jam at the bacterial sec translocase: targeting the SecA nanomotor by small-molecule inhibitors. Chem Biol 18: 685-698. http://dx.doi.org/10.1016/j.chembiol.2011.04.007.
23. Tse YM, Yu M, Tsang JS. 2009. Topological analysis of a haloacid permease of a Burkholderia sp. bacterium with a PhoA-LacZ reporter. BMC Microbiol 9:233. http://dx.doi.org/10.1186/1471-2180-9-233.
24. Lee EY, Choi DS, Kim KP, Gho YS. 2008. Proteomics in gram-negative bacterial outer membrane vesicles. Mass Spectrom Rev 27:535-555. http: //dx.doi.org/10.1002/mas.20175.
25. Koning RI, de Breij A, Oostergetel GT, Nibbering PH, Koster AJ, Dijkshoorn L. 2013. Cryo-electron tomography analysis of membrane vesicles from Acinetobacter baumannii ATCC 19606T. Res Microbiol 164: 397-405. http://dx.doi.org/10.1016/j.resmic.2013.02.007.
26. Dallo SF, Zhang B, Denno J, Hong S, Tsai A, Haskins W, Ye JY, Weitao T. 2012. Association of Acinetobacter baumannii EF-Tu with cell surface, outer membrane vesicles, and fibronectin. ScientificWorldJournal 2012: 128705. http://dx.doi.org/10.1100/2012/128705.
27. McBroom AJ, Kuehn MJ. 2007. Release of outer membrane vesicles by gram-negative bacteria is a novel envelope stress response. Mol Microbiol 63:545-558. http://dx.doi.org/10.1111/j.1365-2958.2006.05522.x.
28. Yoon H, Ansong C, Adkins JN, Heffron F. 2011. Discovery of Salmonella virulence factors translocated via outer membrane vesicles to murine macrophages. Infect Immun 79:2182-2192. http://dx.doi.org/10.1128/IAI.01277-10.
29. Stentz R, Horn N, Cross K, Salt L, Brearley C, Livermore DM, Carding SR. 2015. Cephalosporinases associated with outer membrane vesicles released by Bacteroides spp. protect gut pathogens and commensals against β-lactam antibiotics. J Antimicrob Chemother 70:701-709. http: //dx.doi.org/10.1093/jac/dku466.
30. Deatherage BL, Lara JC, Bergsbaken T, Rassoulian Barrett SL, Lara S, Cookson BT. 2009. Biogenesis of bacterial membrane vesicles. Mol Microbiol 72:1395-1407. http://dx.doi.org/10.1111/j.1365-2958.2009.06731.x.
31. McBroom AJ, Johnson AP, Vemulapalli S, Kuehn MJ. 2006. Outer membrane vesicle production by Escherichia coli is independent of membrane instability. J Bacteriol 188:5385-5392. http://dx.doi.org/10.1128/JB.00498-06.
32. Bielaszewska M, Ruter C, Kunsmann L, Greune L, Bauwens A, Zhang W, Kuczius T, Kim KS, Mellmann A, Schmidt MA, Karch H. 2013. Enterohemorrhagic Escherichia coli hemolysin employs outer membrane vesicles to target mitochondria and cause endothelial and epithelial apoptosis. PLoS Pathog 9:e1003797. http://dx.doi.org/10.1371/journal.ppat.1003797.
33. Wai SN, Lindmark B, Soderblom T, Takade A, Westermark M, Oscarsson J, Jass J, Richter-Dahlfors A, Mizunoe Y, Uhlin BE. 2003. Vesicle-mediated export and assembly of pore-forming oligomers of the enterobacterial ClyA cytotoxin. Cell 115:25-35. http://dx.doi.org/10.1016 /S0092-8674(03)00754-2.
34. Ciofu O, Beveridge TJ, Kadurugamuwa J, Walther-Rasmussen J, Hoiby N. 2000. Chromosomal β-lactamase is packaged into membrane vesicles and secreted from Pseudomonas aeruginosa. J Antimicrob Chemother 45: 9-13. http://dx.doi.org/10.1093/jac/45.1.9.
35. Bauman SJ, Kuehn MJ. 2006. Purification of outer membrane vesicles from Pseudomonas aeruginosa and their activation of an IL-8 response. Microbes Infect 8:2400-2408. http://dx.doi.org/10.1016/j.micinf.2006.05.001.
36. Thompson SS, Naidu YM, Pestka JJ. 1985. Ultrastructural localization of an extracellular protease in Pseudomonas fragi by using the peroxidaseantiperoxidase reaction. Appl Environ Microbiol 50:1038-1042.
37. Vasilyeva NV, Tsfasman IM, Suzina NE, Stepnaya OA, Kulaev IS. 2008. Secretion of bacteriolytic endopeptidase L5 of Lysobacter sp. XL1 into the medium by means of outer membrane vesicles. FEBS J 275:3827-3835. http://dx.doi.org/10.1111/j.1742-4658.2008.06530.x.
38. Elhenawy W, Debelyy MO, Feldman MF. 2014. Preferential packing of acidic glycosidases and proteases into Bacteroides outer membrane vesicles. mBio 5:e00909-14. http://dx.doi.org/10.1128/mBio.00909-14.
39. Haurat MF, Elhenawy W, Feldman MF. 2015. Prokaryotic membrane vesicles: new insights on biogenesis and biological roles. Biol Chem 396: 95-109. http://dx.doi.org/10.1515/hsz-2014-0183.
40. Pradel N, Delmas J, Wu LF, Santini CL, Bonnet R. 2009. Sec-and Tat-dependent translocation of β-lactamases across the Escherichia coli inner membrane. Antimicrob Agents Chemother 53:242-248. http://dx.doi.org/10.1128/AAC.00642-08.
41. Papanikou E, Karamanou S, Economou A. 2007. Bacterial protein secretion through the translocase nanomachine. Nat Rev Microbiol 5:839-851. http://dx.doi.org/10.1038/nrmicro1771.
42. Kusters I, Driessen AJ. 2011. SecA, a remarkable nanomachine. Cell Mol Life Sci 68:2053-2066. http://dx.doi.org/10.1007/s00018-011-0681-y.
43. Hajduk PJ, Huth JR, Tse C. 2005. Predicting protein druggability. Drug Discov Today 10:1675-1682. http://dx.doi.org/10.1016/S1359-6446(05)03624-X.
44. Huang YJ, Wang H, Gao FB, Li M, Yang H, Wang B, Tai PC. 2012. Fluorescein analogues inhibit SecA ATPase: the first sub-micromolar inhibitor of bacterial protein translocation. ChemMedChem 7:571-577. http://dx.doi.org/10.1002/cmdc.201100594.