Immunization with a 22-kDa outer membrane protein elicits protective immunity to multidrug-resistant Acinetobacter baumannii

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Huang, Weiwei ^a,b   Yao, Yufeng ^a,b   Wang, Shijie ^a,b   Xia, Ye ^a,b   Yang, Xu ^a,b   Long, Qiong ^a,b   Sun, Wenjia ^a,b   Liu, Cunbao ^a,b   Li, Yang ^a,b   Chu, Xiaojie ^a,b   Bai, Hongmei ^a,b   Yao, Yueting ^a,b   Ma, Yanbing ^a,b  

^a INSTITUTE OF MEDICAL BIOLOGY   (China)

^b Yunnan Engineering Research Center of Vaccine Research   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ANTIGEN; BACTERIAL VACCINE; BACTERIUM ANTIBODY; COMPLEMENT; CYTOKINE; IMMUNOGLOBULIN G; OUTER MEMBRANE PROTEIN; RECOMBINANT PROTEIN; RECOMBINANT VACCINE; SUBUNIT VACCINE;

ACINETOBACTER BAUMANNII; ACINETOBACTER INFECTIONS; ANIMAL; ANIMAL STRUCTURES; BACTERIAL LOAD; BLOOD; CHEMISTRY; CONSERVED SEQUENCE; DISEASE MODEL; FEMALE; GENETICS; IMMUNOLOGY; INSTITUTE FOR CANCER RESEARCH MOUSE; MICROBIOLOGY; MOLECULAR WEIGHT; MULTIDRUG RESISTANCE; PASSIVE IMMUNIZATION; PHAGOCYTOSIS; PRECLINICAL STUDY; SERUM; SURVIVAL ANALYSIS; VACCINATION;

ACINETOBACTER BAUMANNII; ACINETOBACTER INFECTIONS; ANIMAL STRUCTURES; ANIMALS; ANTIBODIES, BACTERIAL; ANTIGENS, BACTERIAL; BACTERIAL LOAD; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL VACCINES; BLOOD; COMPLEMENT SYSTEM PROTEINS; CONSERVED SEQUENCE; CYTOKINES; DISEASE MODELS, ANIMAL; DRUG EVALUATION, PRECLINICAL; DRUG RESISTANCE, MULTIPLE, BACTERIAL; FEMALE; IMMUNIZATION, PASSIVE; IMMUNOGLOBULIN G; MICE, INBRED ICR; MOLECULAR WEIGHT; PHAGOCYTOSIS; RECOMBINANT PROTEINS; SERUM; SURVIVAL ANALYSIS; VACCINATION; VACCINES, SUBUNIT; VACCINES, SYNTHETIC;

EID: 84957837506     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep20724     Document Type: Article

References (61)

1. Bergogne-Berezin, E. & Towner, K. J. Acinetobacter spp. as nosocomial pathogens: microbiological, clinical, and epidemiological features. Clin Microbiol Rev. 9, 148-165 (1996).
2. Talbot, G. H. et al. Bad bugs need drugs: an update on the development pipeline from the Antimicrobial Availability Task Force of the Infectious Diseases Society of America. Clin Infect Dis. 42, 657-668 (2006).
3. Roca, I., Espinal, P., Vila-Farres, X. & Vila, J. The Acinetobacter baumannii Oxymoron: Commensal Hospital Dweller Turned Pan-Drug-Resistant Menace. Front Microbiol. 3, 148 (2012).
4. Fishbain, J. & Peleg, A. Y. Treatment of Acinetobacter infections. Clin Infect Dis. 51, 79-84 (2010).
5. Magiorakos, A. P. et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 18, 268-281 (2012).
6. Howard, A., O'Donoghue, M., Feeney, A. & Sleator, R. D. Acinetobacter baumannii: an emerging opportunistic pathogen. Virulence. 3, 243-250 (2012).
7. Garcia-Quintanilla, M., Pulido, M. R., Lopez-Rojas, R., Pachon, J. & McConnell, M. J. Emerging therapies for multidrug resistant Acinetobacter baumannii. Trends Microbiol. 21, 157-163 (2013).
8. Goel, V. K. & Kapil, A. Monoclonal antibodies against the iron regulated outer membrane Proteins of Acinetobacter baumannii are bactericidal. BMC Microbiol. 1, 16 (2001).
9. McConnell, M. J. & Pachón, J. Active and passive immunization against Acinetobacter baumannii using an inactivated whole cell vaccine. Vaccine. 29, 1-5 (2010).
10. McConnell, M. J. et al. Vaccination with Outer Membrane Complexes Elicits Rapid Protective Immunity to Multidrug-Resistant Acinetobacter baumannii. Infect Immun. 79, 518-526 (2010).
11. McConnell, M. J., Rumbo, C., Bou, G. & Pachón, J. Outer membrane vesicles as an acellular vaccine against Acinetobacter baumannii. Vaccine. 29, 5705-5710 (2011).
12. Huang, W. et al. Immunization against Multidrug-Resistant Acinetobacter baumannii Effectively Protects Mice in both Pneumonia and Sepsis Models. PLoS ONE. 9, e100727 (2014).
13. Fattahian, Y. et al. Protection against Acinetobacter baumannii infection via its functional deprivation of biofilm associated protein (Bap). Microb Pathog. 51, 402-406 (2011).
14. Bentancor, L. V., O'Malley, J. M., Bozkurt-Guzel, C., Pier, G. B. & Maira-Litran, T. Poly-N-Acetyl-(1-6)-Glucosamine Is a Target for Protective Immunity against Acinetobacter baumannii Infections. Infect Immun. 80, 651-656 (2011).
15. Bentancor, L. V. et al. Evaluation of the Trimeric Autotransporter Ata as a Vaccine Candidate against Acinetobacter baumannii Infections. Infect Immun. 80, 3381-3388 (2012).
16. Russo, T. A. et al. The K1 Capsular Polysaccharide from Acinetobacter baumannii Is a Potential Therapeutic Target via Passive Immunization. Infect Immun. 81, 915-922 (2013).
17. Luo, G. et al. Active and passive immunization protects against lethal, extreme drug resistant-Acinetobacter baumannii infection. PLoS One. 7, e29446 (2012).
18. Choi, C. H. et al. Acinetobacter baumannii outer membrane protein A targets the nucleus and induces cytotoxicity. Cell Microbiol. 10, 309-319 (2008).
19. Jin, J. S. et al. Acinetobacter baumannii secretes cytotoxic outer membrane protein A via outer membrane vesicles. PLoS One. 6, e17027 (2011).
20. McConnell, M. J. & Pachón, J. Expression, purification, and refolding of biologically active Acinetobacter baumannii OmpA from Escherichia coli inclusion bodies. Protein Expr Purif. 77, 98-103 (2011).
21. Smith, S. G., Mahon, V., Lambert, M. A. & Fagan, R. P. A molecular Swiss army knife: OmpA structure, function and expression. FEMS Microbiol Lett. 273, 1-11 (2007).
22. Weiser, J. N. & Gotschlich, E. C. Outer membrane protein A (OmpA) contributes to serum resistance and pathogenicity of Escherichia coli K-1. Infect Immun. 59, 2252-2258 (1991).
23. Torres, A. G. & Kaper, J. B. Multiple elements controlling adherence of enterohemorrhagic Escherichia coli O157:H7 to HeLa cells. Infect Immun. 71, 4985-4995 (2003).
24. Prasadarao, N. V. et al. Outer membrane protein A of Escherichia coli contributes to invasion of brain microvascular endothelial cells. Infect Immun. 64, 146-153 (1996).
25. Prasadarao, N. V., Blom, A. M., Villoutreix, B. O. & Linsangan, L. C. A novel interaction of outer membrane protein A with C4b binding protein mediates serum resistance of Escherichia coli K1. J Immunol. 169, 6352-6360 (2002).
26. Bou, G., Cervero, G., Dominguez, M. A., Quereda, C. & Martinez-Beltran, J. Characterization of a nosocomial outbreak caused by a multiresistant Acinetobacter baumannii strain with a carbapenem-hydrolyzing enzyme: high-level carbapenem resistance in A. baumannii is not due solely to the presence of beta-lactamases. J Clin Microbiol. 38, 3299-3305 (2000).
27. Fernandez-Cuenca, F. et al. Relationship between beta-lactamase production, outer membrane protein and penicillin-binding protein profiles on the activity of carbapenems against clinical isolates of Acinetobacter baumannii. J Antimicrob Chemother. 51, 565-574 (2003).
28. Mussi, M. A., Limansky, A. S. & Viale, A. M. Acquisition of Resistance to Carbapenems in Multidrug-Resistant Clinical Strains of Acinetobacter baumannii: Natural Insertional Inactivation of a Gene Encoding a Member of a Novel Family of -Barrel Outer Membrane Proteins. Antimicrob Agents Chemother. 49, 1432-1440 (2005).
29. Tomas, M. d. M. et al. Cloning and Functional Analysis of the Gene Encoding the 33- to 36-Kilodalton Outer Membrane Protein Associated with Carbapenem Resistance in Acinetobacter baumannii. Antimicrob Agents Chemother. 49, 5172-5175 (2005).
30. Siroy, A. et al. Channel Formation by CarO, the Carbapenem Resistance-Associated Outer Membrane Protein of Acinetobacter baumannii. Antimicrob Agents Chemother. 49, 4876-4883 (2005).
31. Dupont, M., Pages, J. M., Lafitte, D., Siroy, A. & Bollet, C. Identification of an OprD homologue in Acinetobacter baumannii. J Proteome Res. 4, 2386-2390 (2005).
32. Alcántar-Curiel, M. D. et al. Molecular Mechanisms Associated with Nosocomial Carbapenem-resistant Acinetobacter baumannii in Mexico. Arch Med Res. 45, 553-560 (2014).
33. Peleg, A. Y., Seifert, H. & Paterson, D. L. Acinetobacter baumannii: Emergence of a Successful Pathogen. Clin Microbiol Rev. 21, 538-582 (2008).
34. Yun, S.-H. et al. Proteomic analysis of outer membrane proteins from Acinetobacter baumannii DU202 in tetracycline stress condition. J Microbiol. 46, 720-727 (2008).
35. LaVallie, E. R. et al. A thioredoxin gene fusion expression system that circumvents inclusion body formation in the E. coli cytoplasm. Biotechnology (N Y). 11, 187-193 (1993).
36. Wichterman, K. A., Baue, A. E. & Chaudry, I. H. Sepsis and septic shock-a review of laboratory models and a proposal. J Surg Res. 29, 189-201 (1980).
37. Fink, M. P. & Heard, S. O. Laboratory models of sepsis and septic shock. J Surg Res. 49, 186-196 (1990).
38. Deitch, E. A. Animal models of sepsis and shock: a review and lessons learned. Shock. 9, 1-11 (1998).
39. Cross, A. S., Opal, S. M., Sadoff, J. C. & Gemski, P. Choice of bacteria in animal models of sepsis. Infect Immun. 61, 2741-2747 (1993).
40. Buras, J. A., Holzmann, B. & Sitkovsky, M. Animal models of sepsis: setting the stage. Nat Rev Drug Discov. 4, 854-865 (2005).
41. Joly-Guillou, M. L., Wolff, M., Pocidalo, J. J. & Walker, F. & Carbon, C. Use of a new mouse model of Acinetobacter baumannii pneumonia to evaluate the postantibiotic effect of imipenem. Antimicrob Agents Chemother. 41, 345-351 (1997).
42. van Faassen, H. et al. Neutrophils play an important role in host resistance to respiratory infection with Acinetobacter baumannii in mice. Infect Immun. 75, 5597-5608 (2007).
43. Song, J. Y., Cheong, H. J., Lee, J., Sung, A. K. & Kim, W. J. Efficacy of monotherapy and combined antibiotic therapy for carbapenemresistant Acinetobacter baumannii pneumonia in an immunosuppressed mouse model. Int J Antimicrob Agents. 33, 33-39 (2009).
44. KuoLee, R. et al. Intranasal immunization protects against Acinetobacter baumannii-associated pneumonia in mice. Vaccine. 33, 260-267 (2015).
45. Choi, C. H. et al. Outer membrane protein 38 of Acinetobacter baumannii localizes to the mitochondria and induces apoptosis of epithelial cells. Cell Microbiol. 7, 1127-1138 (2005).
46. Galdiero, S. et al. Microbe-host interactions: structure and role of Gram-negative bacterial porins. Curr Protein Pept Sci. 13, 843-854 (2012).
47. Tachikawa, T. & Kato, J.-i. Suppression of the Temperature-Sensitive Mutation of the bamDGene Required for the Assembly of Outer Membrane Proteins by Multicopy of theyiaDGene in Escherichia coli. Biosci Biotechnol Biochem. 75, 162-164 (2014).
48. Deatherage, B. L. et al. Biogenesis of bacterial membrane vesicles. Mol Microbiol. 72, 1395-1407 (2009).
49. Moon, D. C. et al. Acinetobacter baumannii outer membrane protein a modulates the biogenesis of outer membrane vesicles. J Microbiol. 50, 155-160 (2012).
50. O'Hagan, D. T. & Valiante, N. M. Recent advances in the discovery and delivery of vaccine adjuvants. Nat Rev Drug Discov. 2, 727-735 (2003).
51. Wu, Y. et al. Sustained high-titer antibody responses induced by conjugating a malarial vaccine candidate to outer-membrane protein complex. Proc Natl Acad Sci USA 103, 18243-18248 (2006).
52. Koser, M. L. et al. Rabies virus nucleoprotein as a carrier for foreign antigens. Proc Natl Acad Sci USA. 101, 9405-9410 (2004).
53. Bai, X., Findlow, J. & Borrow, R. Recombinant protein meningococcal serogroup B vaccine combined with outer membrane vesicles. Expert Opin Biol Ther. 11, 969-985 (2011).
54. Madico, G. et al. The meningococcal vaccine candidate GNA1870 binds the complement regulatory protein factor H and enhances serum resistance. J Immunol. 177, 501-510 (2006).
55. Fletcher, L. D. et al. Vaccine Potential of the Neisseria meningitidis 2086 Lipoprotein. Infect Immun. 72, 2088-2100 (2004).
56. Arnold, K., Bordoli, L., Kopp, J. & Schwede, T. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics. 22, 195-201 (2006).
57. Schwede, T., Kopp, J., Guex, N. & Peitsch, M. C. SWISS-MODEL: An automated protein homology-modeling server. Nucleic Acids Res. 31, 3381-3385 (2003).
58. Guex, N. & Peitsch, M. C. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis. 18, 2714-2723 (1997).
59. Lin, L. et al. Acinetobacter baumannii rOmpA vaccine dose alters immune polarization and immunodominant epitopes. Vaccine. 31, 313-318 (2013).
60. Ausubel, F. M. et al. Long-Distance Delivery of Bacterial Virulence Factors by Pseudomonas aeruginosa Outer Membrane Vesicles. PLoS Pathog. 5, e1000382 (2009).
61. Kaufmann, G. F., García-Quintanilla, M., Pulido, M. R., Pachón, J. & McConnell, M. J. Immunization with Lipopolysaccharide-Deficient Whole Cells Provides Protective Immunity in an Experimental Mouse Model of Acinetobacter baumannii Infection. PLoS ONE. 9, e114410 (2014).