Bacterial resistance mechanism: What proteomics can elucidate

FASEB Journal

Volumn 27, Issue 4, 2013, Pages 1291-1303

  Lima, Thais Bergamin ^a   Pinto, Michelle Flaviane Soares ^a   Ribeiro, Suzana Meira ^a   Lima, Loiane Alves De ^a   Viana, Juliana Cançado ^a   Júnior, Nelson Gomes ^a   Cândido, Elizabete De Souza ^a   Dias, Simoni Campos ^a   Franco, Octávio Luiz ^a  

^a UNIVERSIDADE CATÓLICA DE BRASÍLIA   (Brazil)

Author keywords

Action mechanism; Antibiotic

Indexed keywords

AMPICILLIN; ANTIBIOTIC AGENT; BACITRACIN; BETA LACTAM; CARBAPENEM; CARBAPENEM DERIVATIVE; CASPOFUNGIN; CEPHALOSPORIN; CHLORAMPHENICOL; COTRIMOXAZOLE; DOXYCYCLINE; ERYTHROMYCIN; FOSFOMYCIN; GLUCAN; KANAMYCIN; LEVOFLOXACIN; MONOBACTAM DERIVATIVE; NALIDIXIC ACID; PENICILLIN DERIVATIVE; PIPERACILLIN PLUS TAZOBACTAM; POLYPEPTIDE ANTIBIOTIC AGENT; RIFAMPICIN; STREPTOMYCIN; SULFAMETHOXAZOLE; SULFONAMIDE; TEICOPLANIN; TETRACYCLINE; TICARCILLIN; UNINDEXED DRUG; VANCOMYCIN;

AMINO ACID SYNTHESIS; ANTIBIOTIC RESISTANCE; BACTERIAL CELL; BACTERIAL CELL WALL; BACTERIAL PHENOMENA AND FUNCTIONS; CELL MEMBRANE; CELLULAR STRESS RESPONSE; DATA BASE; DNA SYNTHESIS; ENERGY METABOLISM; HUMAN; MENINGITIS; NITROGEN METABOLISM; NONHUMAN; NUCLEOTIDE METABOLISM; PHENOTYPE; PRIORITY JOURNAL; PROTEIN SYNTHESIS INHIBITION; PROTEOMICS; Q FEVER; REVIEW; RNA SYNTHESIS; STAPHYLOCOCCUS INFECTION; STREPTOCOCCUS INFECTION; UPREGULATION;

ANTI-BACTERIAL AGENTS; BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; CELL MEMBRANE; DRUG RESISTANCE, BACTERIAL; HUMANS; PROTEOMICS;

BACTERIA (MICROORGANISMS);

EID: 84875758019     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-221127     Document Type: Review

References (102)

1. Grundmann, H., Klugman, K. P., Walsh, T., Ramon-Pardo, P., Sigauque, B., Khan, W., Laxminarayan, R., Heddini, A., and Stelling, J. (2011) A framework for global surveillance of antibiotic resistance. Drug Resist. Updat. 14, 79-87.
2. Morar, M., and Wright, G. D. (2010) The genomic enzymology of antibiotic resistance. Annu. Rev. Genet. 44, 25-51.
3. Cox, G., Thompson, G. S., Jenkins, H. T., Peske, F., Savelsbergh, A., Rodnina, M. V., Wintermeyer, W., Homans, S. W., Edwards, T. A., and O'Neill, A. J. (2012) Ribosome clearance by FusB-type proteins mediates resistance to the antibiotic fusidic acid. Proc. Natl. Acad. Sci. U. S. A. 109, 2102-2107.
4. Pinto, L., Poeta, P., Vieira, S., Caleja, C., Radhouani, H., Carvalho, C., Vieira-Pinto, M., Themudo, P., Torres, C., Vitorino, R., Domingues, P., and Igrejas, G. (2010) Genomic and proteomic evaluation of antibiotic resistance in Salmonella strains. J. Proteomics 73, 1535-1541.
5. Bush, K. (2012) Antimicrobial agents targeting bacterial cell walls and cell membranes. Rev. Sci. Tech. 31, 43-56.
6. Kirby, A., Edwards, C., Broughton, C. M., and Williams, N. J. (2011) Glycopeptide and daptomycin resistance in communityassociated MRSA in the UK. Infection 39, 277-279.
7. Mikami, Y., Suzuki, N., Takahashi, T., Otsuka, K., and Tsuda, H. (2011) Bacitracin upregulates mbrAB transcription via mbrCD to confer bacitracin resistance in Streptococcus mutans. J. Pharmacol. Sci. 117, 204-207.
8. Barroso, D. E., Godoy, D., Castineiras, T. M., Tulenko, M. M., Rebelo, M. C., and Harrison, L. H. (2012) beta-Lactam resistance, serotype distribution, and genotypes of meningitiscausing Streptococcus pneumoniae, Rio de Janeiro, Brazil. Pediatr. Infect. Dis. J. 31, 30-36.
9. Giedraitiene, A., Vitkauskiene, A., Naginiene, R., and Pavilonis, A. (2011) Antibiotic resistance mechanisms of clinically important bacteria. Medicina (Kaunas) 47, 137-146.
10. Lee, J. H., Bae, I. K., and Lee, S. H. (2012) New definitions of extended-spectrum beta-lactamase conferring worldwide emerging antibiotic resistance. Med. Res. Rev. 32, 216-232.
11. Diaz-Mejia, J. J., Babu, M., and Emili, A. (2009) Computational and experimental approaches to chart the Escherichia coli cell-envelope-associated proteome and interactome. FEMS Microbiol. Rev. 33, 66-97.
12. Fernando, D., and Kumar, A. (2012) Growth phase-dependent expression of RND efflux pump- and outer membrane porinencoding genes in Acinetobacter baumannii ATCC 19606. J. Antimicrob. Chemother. 67, 569-572.
13. Peng, X., Xu, C., Ren, H., Lin, X., Wu, L., and Wang, S. (2005) Proteomic analysis of the sarcosine-insoluble outer membrane fraction of Pseudomonas aeruginosa responding to ampicilin, kanamycin, and tetracycline resistance. J. Proteome Res. 4, 2257- 2265.
14. Eren, E., Vijayaraghavan, J., Liu, J., Cheneke, B. R., Touw, D. S., Lepore, B. W., Indic, M., Movileanu, L., and van den Berg, B. (2012) Substrate specificity within a family of outer membrane carboxylate channels. PLoS Biol 10, e1001242.
15. Pages, J. M., James, C. E., and Winterhalter, M. (2008) The porin and the permeating antibiotic: a selective diffusion barrier in gram-negative bacteria. Nat. Rev. Microbiol. 6, 893- 903.
16. Muller, M. M., Hormann, B., Kugel, M., Syldatk, C., and Hausmann, R. (2011) Evaluation of rhamnolipid production capacity of Pseudomonas aeruginosa PAO1 in comparison to the rhamnolipid over-producer strains DSM 7108 and DSM 2874. Appl. Microbiol. Biotechnol. 89, 585-592.
17. Cavallo, J. D., Plesiat, P., Couetdic, G., Leblanc, F., and Fabre, R. (2002) Mechanisms of -lactam resistance in Pseudomonas aeruginosa: prevalence of OprM-overproducing strains in a French multicentre study (1997). J. Antimicrob. Chemother. 50, 1039-1043.
18. Li, X. Z., and Nikaido, H. (2009) Efflux-mediated drug resistance in bacteria: an update. Drugs 69, 1555-1623.
19. Dos Santos, K. V., Diniz, C. G., Veloso, L. de C., de Andrade, H. M., Giusta, M. da S., Pires, S. da F., Santos, A. V., Apolonio, A. C., de Carvalho, M. A., and Farias, L. de M. (2010) Proteomic analysis of Escherichia coli with experimentally induced resistance to piperacillin/tazobactam. Res. Microbiol. 161, 268-275.
20. Kim, H. S., and Nikaido, H. (2012) Different functions of MdtB and MdtC subunits in the heterotrimeric efflux transporter MdtB(2)C complex of Escherichia coli. Biochemistry 51, 4188- 4197.
21. Yang, L., Chen, L., Shen, L., Surette, M., and Duan, K. (2011) Inactivation of MuxABC-OpmB transporter system in Pseudomonas aeruginosa leads to increased ampicillin and carbenicillin resistance and decreased virulence. J. Microbiol. 49, 107-114.
22. Chaussee, M. A., McDowell, E. J., Rieck, L. D., Callegari, E. A., and Chaussee, M. S. (2006) Proteomic analysis of a penicillintolerant rgg mutant strain of Streptococcus pyogenes. J. Antimicrob. Chemother. 58, 752-759.
23. Monteiro, R., Vitorino, R., Domingues, P., Radhouani, H., Carvalho, C., Poeta, P., Torres, C., and Igrejas, G. (2012) Proteome of a methicillin- resistant Staphylococcus aureus clinical strain of sequence type ST398. J. Proteomics 75, 2892-2915.
24. Levine, D. P. (2006) Vancomycin: a history. Clin. Infect. Dis. 42(Suppl. 1), S5-S12.
25. Parenti, F., Beretta, G., Berti, M., and Arioli, V. (1978) Teichomycins, new antibiotics from Actinoplanes teichomyceticus Nov. Sp. I. Description of the producer strain, fermentation studies and biological properties. J. Antibiot. (Tokyo) 31, 276-283.
26. Zhanel, G. G., Trapp, S., Gin, A. S., DeCorby, M., Lagace- Wiens, P. R., Rubinstein, E., Hoban, D. J., and Karlowsky, J. A. (2008) Dalbavancin and telavancin: novel lipoglycopeptides for the treatment of gram-positive infections. Expert Rev. Anti Infect. Ther. 6, 67-81.
27. Eirich, J., Orth, R., and Sieber, S. A. (2011) Unraveling the protein targets of vancomycin in living S. aureus and E. faecalis cells. J. Am. Chem. Soc. 133, 12144-12153.
28. Kahne, D., Leimkuhler, C., Lu, W., and Walsh, C. (2005) Glycopeptide and lipoglycopeptide antibiotics. Chem. Rev. 105, 425-448.
29. Liu, C., and Chambers, H. F. (2003) Staphylococcus aureus with heterogeneous resistance to vancomycin: epidemiology, clinical significance, and critical assessment of diagnostic methods. Antimicrob. Agents Chemother. 47, 3040-3045.
30. Hong, H. J., Hutchings, M. I., and Buttner, M. J. (2008) Vancomycin resistance VanS/VanR two-component systems. Adv. Exp. Med. Biol. 631, 200-213.
31. Wang, X., He, X., Jiang, Z., Wang, J., Chen, X., Liu, D., Wang, F., Guo, Y., Zhao, J., Liu, F., Huang, L., and Yuan, J. (2010) Proteomic analysis of the Enterococcus faecalis V583 strain and clinical isolate V309 under vancomycin treatment. J. Proteome Res. 9, 1772-1785.
32. Drummelsmith, J., Winstall, E., Bergeron, M. G., Poirier, G. G., and Ouellette, M. (2007) Comparative proteomics analyses reveal a potential biomarker for the detection of vancomycinintermediate Staphylococcus aureus strains. J. Proteome. Res. 6, 4690-4702.
33. Li, H., Lin, X. M., Wang, S. Y., and Peng, X. X. (2007) Identification and antibody-therapeutic targeting of chloramphenicol- resistant outer membrane proteins in Escherichia coli. J. Proteome Res. 6, 3628-3636.
34. Xaplanteri, M. A., Andreou, A., Dinos, G. P., and Kalpaxis, D. L. (2003) Effect of polyamines on the inhibition of peptidyltransferase by antibiotics: revisiting the mechanism of chloramphenicol action. Nucleic Acids Res. 31, 5074-5083.
35. Biot, F. V., Valade, E., Garnotel, E., Chevalier, J., Villard, C., Thibault, F. M., Vidal, D. R., and Pages, J. M. (2011) Involvement of the efflux pumps in chloramphenicol selected strains of Burkholderia thailandensis: proteomic and mechanistic evidence. PLoS One 6, e16892.
36. Yun, S. H., Kim, Y. H., Joo, E. J., Choi, J. S., Sohn, J. H., and Kim, S. I. (2006) Proteome analysis of cellular response of Pseudomonas putida KT2440 to tetracycline stress. Curr. Microbiol. 53, 95-101.
37. Yun, S. H., Choi, C. W., Park, S. H., Lee, J. C., Leem, S. H., Choi, J. S., Kim, S., and Kim, S. I. (2008) Proteomic analysis of outer membrane proteins from Acinetobacter baumannii DU202 in tetracycline stress condition. J. Microbiol. 46, 720-727.
38. Vranakis, I., De Bock, P. J., Papadioti, A., Tselentis, Y., Gevaert, K., Tsiotis, G., and Psaroulaki, A. (2012) Quantitative proteome profiling of C. burnetii under tetracycline stress conditions. PloS One 7, e33599.
39. Koskiniemi, S., Pranting, M., Gullberg, E., Nasvall, J., and Andersson, D. I. (2011) Activation of cryptic aminoglycoside resistance in Salmonella enterica. Mol. Microbiol. 80, 1464-1478.
40. Ozaki, M., Mizushima, S., and Nomura, M. Identification and functional characterization of the protein controlled by the streptomycin-resistant locus in E. coli. Nature 222, 333-339, 1969.
41. Okamoto, S., Tamaru, A., Nakajima, C., Nishimura, K., Tanaka, Y., Tokuyama, S., Suzuki, Y., and Ochi, K. (2007) Loss of a conserved 7-methylguanosine modification in 16S rRNA confers low-level streptomycin resistance in bacteria. Mol. Microbiol. 63, 1096-1106.
42. Sharma, P., Kumar, B., Gupta, Y., Singhal, N., Katoch, V. M., Venkatesan, K., and Bisht, D. (2010) Proteomic analysis of streptomycin resistant and sensitive clinical isolates of Mycobacterium tuberculosis. Proteome Sci. 8, 59.
43. Zhang, B., Xu, C., Zhou, S., Feng, S., Zhang, L., He, Y., and Liao, M. (2012) Comparative proteomic analysis of a Haemophilus parasuis SC096 mutant deficient in the outer membrane protein P5. Microb. Pathog. 52, 117-124.
44. Cash, P., Argo, E., Ford, L., Lawrie, L., and McKenzie, H. (1999) A proteomic analysis of erythromycin resistance in Streptococcus pneumoniae. Electrophoresis 20, 2259-2268.
45. Drlica, K., and Zhao, X. (1997) DNA gyrase, topoisomerase IV, and the 4-quinolones. Microbiol. Mol. Biol. Rev. 61, 377-392.
46. Shimada, T., Yamamoto, K., and Ishihama, A. (2009) Involvement of the leucine response transcription factor LeuO in regulation of the genes for sulfa drug efflux. J. Bacteriol. 191, 4562-4571.
47. Reeks, B. Y., Champlin, F. R., Paulsen, D. B., Scruggs, D. W., and Lawrence, M. L. (2005) Effects of sub-minimum inhibitory concentration antibiotic levels and temperature on growth kinetics and outer membrane protein expression in Mannheimia haemolytica and Haemophilus somnus. Can. J. Vet. Res. 69, 1-10.
48. Duthie, S. J., Narayanan, S., Sharp, L., Little, J., Basten, G., and Powers, H. (2004) Folate, DNA stability and colo-rectal neoplasia. Proc. Nutr. Soc. 63, 571-578.
49. Barman, S., Chatterjee, S., Chowdhury, G., Ramamurthy, T., Niyogi, S. K., Kumar, R., and Koley, H. (2010) Plasmidmediated streptomycin and sulfamethoxazole resistance in Shigella flexneri 3a. Int. J. Antimicrob. Agents. 36, 348-351.
50. Koser, C. U., Summers, D. K., and Archer, J. A. (2010) Role of the dihydrofolate reductase DfrA (Rv2763c) in trimethoprimsulfamethoxazole (co-trimoxazole) resistance in Mycobacterium tuberculosis. Antimicrob. Agents Chemother. 54, 4951-4952; author reply 4952.
51. Hu, L. F., Chang, X., Ye, Y., Wang, Z. X., Shao, Y. B., Shi, W., Li, X., and Li, J. B. (2011) Stenotrophomonas maltophilia resistance to trimethoprim/sulfamethoxazole mediated by acquisition of sul and dfrA genes in a plasmid-mediated class 1 integron. Int. J. Antimicrob. Agents 37, 230-234.
52. Fenollar, F., Rolain, J. M., Alric, L., Papo, T., Chauveheid, M. P., van de Beek, D., and Raoult, D. (2009) Resistance to trimethoprim sulfamethoxazole and Tropheryma whipplei. Int. J. Antimicrob. Agents. 34, 255-259.
53. Ho, P. L., Chow, K. H., Lo, P. Y., Lee, K. F., and Lai, E. L. (2009) Changes in the epidemiology of methicillin-resistant Staphylococcus aureus associated with spread of the ST45 lineage in Hong Kong. Diagn. Microbiol. Infect. Dis. 64, 131-137.
54. Dueger, E. L., Asturias, E. J., Matheu, J., Gordillo, R., Torres, O., and Halsey, N. (2008) Increasing penicillin and trimethoprim- sulfamethoxazole resistance in nasopharyngeal Streptococcus pneumoniae isolates from Guatemalan children, 2001- 2006. Int. J. Infect. Dis. 12, 289-297.
55. Silva, L. V., Araujo, M. T., Santos, K. R., and Nunes, A. P. (2011) Evaluation of the synergistic potential of vancomycin combined with other antimicrobial agents against methicillinresistant Staphylococcus aureus and coagulase-negative Staphylococcus spp strains. Mem. Inst. Oswaldo Cruz 106, 44-50.
56. Yekutiel, A., Shalit, I., Shadkchan, Y., and Osherov, N. (2004) In vitro activity of caspofungin combined with sulfamethoxa-zole against clinical isolates of Aspergillus spp. Antimicrob. Agents Chemother. 48, 3279-3283.
57. Nanduri, B., Lawrence, M. L., Vanguri, S., Pechan, T., and Burgess, S. C. (2005) Proteomic analysis using an unfinished bacterial genome: the effects of subminimum inhibitory concentrations of antibiotics on Mannheimia haemolytica virulence factor expression. Proteomics 5, 4852-4863.
58. Vranakis, I., Sandalakis, V., Chochlakis, D., Tselentis, Y., and Psaroulaki, A. (2010) DNA gyrase and topoisomerase IV mutations in an in vitro fluoroquinolone-resistant Coxiella burnetii strain. Microb. Drug Resist. 16, 111-117.
59. Yamade, M., Sugimoto, M., Uotani, T., Nishino, M., Kodaira, C., and Furuta, T. (2011) Resistance of Helicobacter pylori to quinolones and clarithromycin assessed by genetic testing in Japan. J. Gastroenterol. Hepatol. 26, 1457-1461.
60. Del Castillo, E., Montes-Bayon, M., Anon, E., and Sanz-Medel, A. (2011) Quantitative targeted biomarker assay for glycated haemoglobin by multidimensional LC using mass spectrometric detection. J. Proteomics 74, 35-43.
61. He, G. X., Thorpe, C., Walsh, D., Crow, R., Chen, H., Kumar, S., and Varela, M. F. (2011) EmmdR, a new member of the MATE family of multidrug transporters, extrudes quinolones from Enterobacter cloacae. Arch. Microbiol. 193, 759-765.
62. Vranakis, I., De Bock, P. J., Papadioti, A., Tselentis, Y., Gevaert, K., Tsiotis, G., and Psaroulaki, A. (2011) Identification of potentially involved proteins in levofloxacin resistance mechanisms in Coxiella burnetii. J. Proteome Res. 10, 756-762.
63. Beck, M., Malmstrom, J. A., Lange, V., Schmidt, A., Deutsch, E. W., and Aebersold, R. (2009) Visual proteomics of the human pathogen Leptospira interrogans. Nat. Methods 6, 817-823.
64. Varhimo, E., Savijoki, K., Jefremoff, H., Jalava, J., Sukura, A., and Varmanen, P. (2008) Ciprofloxacin induces mutagenesis to antibiotic resistance independent of UmuC in Streptococcus uberis. Environ. Microbiol. 10, 2179-2183.
65. Poutanen, M., Varhimo, E., Kalkkinen, N., Sukura, A., Varmanen, P., and Savijoki, K. (2009) Two-dimensional difference gel electrophoresis analysis of Streptococcus uberis in response to mutagenesis-inducing ciprofloxacin challenge. J. Proteome Res. 8, 246-255.
66. Coldham, N. G., Randall, L. P., Piddock, L. J., and Woodward, M. J. (2006) Effect of fluoroquinolone exposure on the proteome of Salmonella enterica serovar Typhimurium. J. Antimicrob. Chemother. 58, 1145-1153.
67. Gliniewicz, K., Plant, K. P., LaPatra, S. E., LaFrentz, B. R., Cain, K., Snekvik, K. R., and Call, D. R. (2012) Comparative proteomic analysis of virulent and rifampicin-attenuated Flavobacterium psychrophilum. J. Fish Dis. 35, 529-539.
68. Neri, A., Mignogna, G., Fazio, C., Giorgi, A., Schinina, M. E., and Stefanelli, P. (2010) Neisseria meningitidis rifampicin-resistant strains: analysis of protein differentially expressed. BMC Microbiol. 10, 246.
69. Sandalakis, V., Psaroulaki, A., De Bock, P. J., Christidou, A., Gevaert, K., Tsiotis, G., and Tselentis, Y. (2012) Investigation of rifampicin resistance mechanisms in Brucella abortus using MS-driven comparative proteomics. J. Proteome Res. 11, 2374- 2385.
70. Jung, D., Powers, J. P., Straus, S. K., and Hancock, R. E. (2008) Lipid-specific binding of the calcium-dependent antibiotic daptomycin leads to changes in lipid polymorphism of model membranes. Chem. Physics Lipids 154, 120-128.
71. Rubinchik, E., Schneider, T., Elliott, M., Scott, W. R., Pan, J., Anklin, C., Yang, H., Dugourd, D., Muller, A., Gries, K., Straus, S. K., Sahl, H. G., and Hancock, R. E. (2011) Mechanism of action and limited cross-resistance of new lipopeptide MX- 2401. Antimicrob. Agents Chemother. 55, 2743-2754.
72. van Hal, S. J., Paterson, D. L., and Gosbell, I. B. (2011) Emergence of daptomycin resistance following vancomycinunresponsive Staphylococcus aureus bacteraemia in a daptomycin- naive patient a review of the literature. Eur. J. Clin. Microbiol. Infect. Dis. 30, 603-610.
73. Wecke, T., Zuhlke, D., Mader, U., Jordan, S., Voigt, B., Pelzer, S., Labischinski, H., Homuth, G., Hecker, M., and Mascher, T. (2009) Daptomycin versus Friulimicin B: in-depth profiling of Bacillus subtilis cell envelope stress responses. Antimicrob. Agents Chemother. 53, 1619-1623.
74. Hachmann, A. B., Angert, E. R., and Helmann, J. D. (2009) Genetic analysis of factors affecting susceptibility of Bacillus subtilis to daptomycin. Antimicrob. Agents Chemother. 53, 1598- 1609.
75. Fischer, A., Yang, S.-J., Bayer, A. S., Vaezzadeh, A. R., Herzig, S., Stenz, L., Girard, M., Sakoulas, G., Scherl, A., Yeaman, M. R., Proctor, R. A., Schrenzel, J., and François, P. (2011) Daptomycin resistance mechanisms in clinically derived Staphylococcus aureus strains assessed by a combined transcriptomics and proteomics approach. J. Antimicrob. Chemother. 66, 1696 -1711.
76. Candido, E. S., Pinto, M. F., Pelegrini, P. B., Lima, T. B., Silva, O. N., Pogue, R., Grossi-de-Sa, M. F., and Franco, O. L. (2011) Plant storage proteins with antimicrobial activity: novel insights into plant defense mechanisms. FASEB J. 25, 3290 -3305.
77. Saar-Dover, R., Bitler, A., Nezer, R., Shmuel-Galia, L., Firon, A., Shimoni, E., Trieu-Cuot, P., and Shai, Y. (2012) D-alanylation of lipoteichoic acids confers resistance to cationic peptides in group B streptococcus by increasing the cell wall density. PLoS Pathog. 8, e1002891.
78. Fernandez, L., Alvarez-Ortega, C., Wiegand, I., Olivares, J., Kocincová, D., Lam, J. S., Martínez, J. L., and Hancock, R. E. (2012) Characterization of the polymyxin B resistome of Pseudomonas aeruginosa. [E-pub ahead of print] Antimicrob. Agents Chemother. doi: 10.1128/AAC.01583-12.
79. Rosales-Reyes, R., Saldias, M. S., Aubert, D. F., El-Halfawy, O. M., and Valvano, M. A. (2012) The suhB gene of Burkholderia cenocepacia is required for protein secretion, biofilm formation, motility and polymyxin B resistance. Microbiology 158, 2315-2324.
80. Gan, H. M., Lean, S. S., Suhaili, Z., Thong, K. L., and Yeo, C. C. (2012) Genome sequence of Acinetobacter baumannii AC12, a polymyxin-resistant strain isolated from Terengganu, Malaysia. J. Bacteriol. 194, 5979-5980.
81. Maria-Neto, S., Candido, E. de S., Rodrigues, D. R., de Sousa, D. A., da Silva, E. M., de Moraes, L. M., Otero-Gonzalez, A. de J., Magalhaes, B. S., Dias, S. C., and Franco, O. L. (2012) Deciphering the magainin resistance process of Escherichia coli strains in light of the cytosolic proteome. Antimicrob. Agents Chemother. 56, 1714-1724.
82. Loutet, S. A., and Valvano, M. A. (2011) Extreme antimicrobial Peptide and polymyxin B resistance in the genus Burkholderia. Front. Microbiol. 2, 159.
83. Beceiro, A., Llobet, E., Aranda, J., Bengoechea, J. A., Doumith, M., Hornsey, M., Dhanji, H., Chart, H., Bou, G., Livermore, D. M., and Woodford, N. (2011) Phosphoethanolamine modification of lipid A in colistin-resistant variants of Acinetobacter baumannii mediated by the pmrAB two-component regulatory system. Antimicrob. Agents Chemother. 55, 3370-3379.
84. Zucca, M., Scutera, S., and Savoia, D. (2011) New antimicrobial frontiers. Mini Rev. Med. Chem. 11, 888-900.
85. Fehri, L. F., Sirand-Pugnet, P., Gourgues, G., Jan, G., Wroblewski, H., and Blanchard, A. (2005) Resistance to antimicrobial peptides and stress response in Mycoplasma pulmonis. Antimicrob. Agents Chemother. 49, 4154-4165.
86. Chiu, Y., Kuo, T. Y., Lin, C. C., and Chen, W. J. (2010) Proteomic analysis reveals responsive proteins of Vibrio parahaemolyticus on exposure to cationic antimicrobial peptides. J. Appl. Microbiol. 110, 80-89.
87. Fernandez-Reyes, M., Rodriguez-Falcon, M., Chiva, C., Pachon, J., Andreu, D., and Rivas, L. (2009) The cost of resistance to colistin in Acinetobacter baumannii: a proteomic perspective. Proteomics 9, 1632-1645.
88. Oh, J. T., Cajal, Y., Dhurjati, P. S., Van Dyk, T. K., and Jain, M. K. (1998) Cecropins induce the hyperosmotic stress response in Escherichia coli. Biochim. Biophys. Acta 1415, 235-245.
89. Vaara, M. (1993) Outer membrane permeability barrier to azithromycin, clarithromycin, and roxithromycin in gramnegative enteric bacteria. Antimicrob. Agents Chemother. 37, 354 -356.
90. Fernandez, L., Gooderham, W. J., Bains, M., McPhee, J. B., Wiegand, I., and Hancock, R. E. (2010) Adaptive resistance to the "last hope" antibiotics polymyxin B and colistin in Pseudomonas aeruginosa is mediated by the novel two-component regulatory system ParR-ParS. Antimicrob. Agents Chemother. 54, 3372-3382.
91. Catel-Ferreira, M., Coadou, G., Molle, V., Mugnier, P., Nordmann, P., Siroy, A., Jouenne, T., and De, E. (2011) Structurefunction relationships of CarO, the carbapenem resistanceassociated outer membrane protein of Acinetobacter baumannii. J. Antimicrob. Chemother. 66, 2053-2056.
92. Moore, R. A., and Hancock, R. E. (1986) Involvement of outer membrane of Pseudomonas cepacia in aminoglycoside and polymyxin resistance. Antimicrob. Agents Chemother. 30, 923-926.
93. Bishop, R. E. (2005) The lipid A palmitoyltransferase PagP: molecular mechanisms and role in bacterial pathogenesis. Mol. Microbiol. 57, 900-912.
94. Monsieurs, P., De Keersmaecker, S., Navarre, W. W., Bader, M. W., De Smet, F., McClelland, M., Fang, F. C., De Moor, B., Vanderleyden, J., and Marchal, K. (2005) Comparison of the PhoPQ regulon in Escherichia coli and Salmonella typhimurium. J. Mol. Evol. 60, 462-474.
95. Cajal, Y., Ghanta, J., Easwaran, K., Surolia, A., and Jain, M. K. (1996) Specificity for the exchange of phospholipids through polymyxin B mediated intermembrane molecular contacts. Biochemistry 35, 5684-5695.
96. Vijayakumar, S. R., Kirchhof, M. G., Patten, C. L., and Schellhorn, H. E. (2004) RpoS-regulated genes of Escherichia coli identified by random lacZ fusion mutagenesis. J. Bacteriol. 186, 8499-8507.
97. Raynaud, C., and Charbit, A. (2005) Regulation of expression of type I signal peptidases in Listeria monocytogenes. Microbiology 151, 3769-3776.
98. Otero-Gonzalez, A. J., Magalhaes, B. S., Garcia-Villarino, M., Lopez-Abarrategui, C., Sousa, D. A., Dias, S. C., and Franco, O. L. (2010) Antimicrobial peptides from marine invertebrates as a new frontier for microbial infection control. FASEB J. 24, 1320-1334.
99. Xiong, X. P., Wang, C., Ye, M. Z., Yang, T. C., Peng, X. X., and Li, H. (2010) Differentially expressed outer membrane proteins of Vibrio alginolyticus in response to six types of antibiotics. Mar. Biotechnol. (NY) 12, 686-695.
100. Hornsey, M., Loman, N., Wareham, D. W., Ellington, M. J., Pallen, M. J., Turton, J. F., Underwood, A., Gaulton, T., Thomas, C. P., Doumith, M., Livermore, D. M., and Woodford, N. (2011) Whole-genome comparison of two Acinetobacter baumannii isolates from a single patient, where resistance developed during tigecycline therapy. J. Antimicrob. Chemother. 66, 1499-1503.
101. Amini, S., and Tavazoie, S. (2011) Antibiotics and the postgenome revolution. Curr. Opin. Microbiol. 14, 513-518.
102. Sparbier, K., Schubert, S., Weller, U., Boogen, C., and Kostrzewa, M. (2012) Matrix-assisted laser desorption ionizationtime of flight mass spectrometry-based functional assay for rapid detection of resistance against beta-lactam antibiotics. J. Clin. Microbiol. 50, 927-937.