Quantitative proteomic analysis of host-pathogen interactions: A study of Acinetobacter baumannii responses to host airways

BMC Genomics

Volumn 16, Issue 1, 2015, Pages

  Méndez, Jose Antonio ^a   Mateos, Jesús ^b   Beceiro, Alejandro ^a   Lopez, María ^a   Tomás, María ^a   Poza, Margarita ^a   Bou, Germán ^a  

^a UNIVERSITY OF A CORUÑA   (Spain)

^b Grupo de Proteomica PBR2 ProteoRed ISCIII Servicio de Reumatologia   (Spain)

Author keywords

Acinetobacter baumannii; Ex vivo; Host pathogen interaction; Proteome; Virulence

Indexed keywords

2 ISOPROPYLMALATE SYNTHASE; ACETYL COENZYME A HYDROLASE; ACONITATE HYDRATASE; ASPARTATE AMINOTRANSFERASE; ASPARTATE SEMIALDEHYDE DEHYDROGENASE; BACTERIOFERRITIN; CITRATE SYNTHASE; DNA BINDING PROTEIN; GLUCOSE DEHYDROGENASE; GLUTAMATE SYNTHASE; GLYOXALASE; INORGANIC PYROPHOSPHATASE; ISOCITRATE DEHYDROGENASE; KETOL ACID REDUCTOISOMERASE; MALATE DEHYDROGENASE; MALATE DEHYDROGENASE (DECARBOXYLATING); NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) TRANSHYDROGENASE; ORNITHINE CARBAMOYLTRANSFERASE; OXIDOREDUCTASE; OXOGLUTARATE DEHYDROGENASE; PEPTIDASE; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); PHOSPHOGLYCERATE MUTASE; PROTEOME; PYRUVATE DEHYDROGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; SUCCINATE DEHYDROGENASE; SULFURTRANSFERASE; SUPEROXIDE DISMUTASE; UNINDEXED DRUG; BACTERIAL PROTEIN; VIRULENCE FACTOR;

ACINETOBACTER BAUMANNII; AIRWAY; AMINO ACID METABOLISM; ARTICLE; BACTERIAL GROWTH; BACTERIAL PNEUMONIA; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BIOGENESIS; CARBOHYDRATE METABOLISM; CARBOHYDRATE TRANSPORT; CELL CYCLE REGULATION; CONTROLLED STUDY; ENERGY YIELD; GENE EXPRESSION PROFILING; HOST PATHOGEN INTERACTION; ION TRANSPORT; LIPID METABOLISM; LIQUID CHROMATOGRAPHY; LUNG LAVAGE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MITOSIS; MOLECULAR DYNAMICS; NEUTROPHIL; NONHUMAN; NUCLEOTIDE METABOLISM; NUCLEOTIDE TRANSPORT; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN PROCESSING; PROTEOMICS; QUANTITATIVE ANALYSIS; RESPIRATORY SYSTEM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA TRANSCRIPTION; RNA TRANSLATION; SEQUENCE HOMOLOGY; TYPE IV SECRETION SYSTEM; ANIMAL; BIOLOGICAL MODEL; BRONCHOALVEOLAR LAVAGE FLUID; CELL LINE; CELL WALL; CYTOLOGY; ENERGY METABOLISM; GENETICS; LUNG; MALE; MATRIX-ASSISTED LASER DESORPTION-IONIZATION MASS SPECTROMETRY; METABOLISM; MICROBIOLOGY; MOUSE; PATHOLOGY; PHYSIOLOGY; PNEUMONIA; RAT; VETERINARY; WISTAR RAT;

ACINETOBACTER BAUMANNII; BACTERIA (MICROORGANISMS); RATTUS;

ACINETOBACTER BAUMANNII; ANIMALS; ASPARTATE AMINOTRANSFERASES; BACTERIAL PROTEINS; BRONCHOALVEOLAR LAVAGE FLUID; CELL LINE; CELL WALL; DNA-BINDING PROTEINS; ENERGY METABOLISM; HOST-PATHOGEN INTERACTIONS; LIPID METABOLISM; LUNG; MALE; MICE; MODELS, BIOLOGICAL; PNEUMONIA; PROTEOME; PROTEOMICS; RATS; RATS, WISTAR; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; VIRULENCE FACTORS;

EID: 84930195477     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-015-1608-z     Document Type: Article

References (82)

1. Howard A, Donoghue MO, Feeney A, Sleator RD. Acinetobacter baumannii an emerging opportunistic pathogen. Virulence. 2012;3:243-50.
2. Visca P, Seifert H, Towner KJ. Acinetobacter infection-an emerging threat to human health. IUBMB Life. 2011;63:1048-54.
3. Anstey NM, Currie BJ, Hassell M, Palmer D, Dwyer B, Seifert H. Community-acquired bacteremic Acinetobacter pneumonia in tropical Australia is caused by diverse strains of Acinetobacterbaumannii with carriage in the throat in at-risk groups. J Clin Microbiol. 2002;40:685-6.
4. Leung WS, Chu CM, Tsang KY, Lo FH, Lo KF, Ho PL. Fulminant community-acquired Acinetobacter baumannii pneumonia as a distinct clinical syndrome. Chest. 2006;129:102-9.
5. Giamarellou H, Antoniadou AK, Kanellakopoulou K. Acinetobacterbaumannii: a universal threat to public health? Int J Antimicrob Agents. 2008;32:106-19.
6. Theaker C, Azadian B, Soni N. The impact of Acinetobacter baumannii in the intensive care unit. Anaesthesia. 2003;58:271-4.
7. Chen CH, Lin LC, Chang YJ, Huang CC, Liu CE, Young TG. Analysis of prognostic factors in 95 patients with Acinetobacter baumannii bacteremia. Infection. 2003;31:331-5.
8. Rodríguez-Baño J, Cisneros JM, Fernández-Cuenca F, Ribera A, Vila J, Pascual A, et al. Clinical features and epidemiology of Acinetobacter baumannii colonization and infection in Spanish hospitals. Infect Control Hosp Epidemiol. 2004;25:819-24.
9. Gayoso CM, Mateos J, Méndez JA, Fernández-Puente P, Rumbo C, Tomás M, et al. Molecular mechanisms involved in the response to desiccation stress and persistence in Acinetobacterbaumannii. J Proteome Res. 2014;13:460-76.
10. Eveillard M, Kempf M, Belmonte O, Pailhoriès H, Joly-Guillou ML. Reservoirs of Acinetobacter baumannii outside the hospital and potential involvement in emerging human community-acquired infections. Int J Infect Dis. 2013;17:e802-5.
11. Peleg AY, Seifert H, Paterson DL. Acinetobacter baumannii: emergence of a successful pathogen. Clin Microbiol. 2008;21:538-82.
12. Seifert H, Dijkshoorn L, Gerner-Smidt P, Pelzer N, Tjernberg I, Vaneechoutte M. Distribution of Acinetobacter species on human skin: comparison of phenotypic and genotypic identification methods. J Clin Microbiol. 1997;35:2819-25.
13. Chu YW, Leung CM, Houang ET, Ng KC, Leung CB, Leung HY, et al. Skin carriage of acinetobacters in Hong Kong. J Clin Microbiol. 1999;35:2962-7.
14. Fournier PE, Richet H. The epidemiology and control of Acinetobacter baumannii in health care facilities. Clin Infect Dis. 2006;42:692-9.
15. Camp C, Tatum OL. A review of Acinetobacter baumannii as a highly successful pathogen in times of war. Lab Medicine. 2010;41:649-57.
16. Hanlon GW. The emergence of multidrug resistant Acinetobacter species: a major concern in the hospital setting. Lett Appl Microbiol. 2005;41:375-8.
17. Morgan DJ, Liang SY, Smith CL, Johnson JK, Harris AD, Furuno JP, et al. Frequent multidrug-resistant Acinetobacter baumannii contamination of gloves gowns and hands of healthcare workers. Infect Control Hosp Epidemiol. 2010;31:716-21.
18. Wendt C, Dietze B, Dietz E, Ruden H. Survival of Acinetobacter baumannii on dry surfaces. J Clin Microbiol. 1997;35:1394-7.
19. Rao R, Karthika R, Singh S, Shashikala P, Kanungo R, Jayachandran S, et al. Correlation between biofilm production and multiple drug resistance in imipenem resistant clinical isolates of Acinetobacter baumannii. Indian J Med Microbiol. 2008;4:333-7.
20. Gales AC, Jones RN, Sader HS. Global assessment of the antimicrobial activity of polymyxin B against 54 731 clinical isolates of Gram-negative bacilli: report from the SENTRY antimicrobial surveillance programme (2001-2004). Clin Microbiol Infect. 2006;12:315-21.
21. Ko KS, Suh JY, Kwon KT, Jung SI, Park KH, Kang CI, et al. High rates of resistance to colistin and polymyxin B in subgroups of Acinetobacter baumannii isolates from Korea. J Antimicrob Chemother. 2007;60:1163-7.
22. Barbe V, Vallenet D, Fonknechten N, Kreimeyer A, Oztas S, Labarre L, et al. Unique features revealed by the genome sequence of Acinetobacter sp ADP1 a versatile and naturally transformation competent bacterium. Nucleic Acids Res. 2004;32:5766-79.
23. Smith MG, Gianoulis TA, Pukatzki S, Mekalanos JJ, Ornston LN, Gerstein M, et al. New insights into Acinetobacter baumannii pathogenesis revealed by high-density pyrosequencing and transposon mutagenesis. Genes Dev. 2007;21:601-14.
24. Mendez JA, Soares NC, Mateos J, Gayoso C, Rumbo C, Aranda J, et al. Extracellular proteome of a highly invasive multidrug-resistant clinical strain of Acinetobacter baumannii. J Proteome Res. 2012;11:5678-94.
25. Kwon SO, Gho YS, Lee JC, Kim SI. Proteome analysis of outer membrane vesicles from a clinical Acinetobacter baumannii isolate. FEMS Microbiol Lett. 2009;297:150-6.
26. Tiwari V, Vashistt J, Kapil A, Moganty RR. Comparative proteomics of inner membrane fraction from carbapenem-resistant Acinetobacter baumannii with a reference strain. PLoS ONE. 2012;7, e39451.
27. Yun SH, Choi CW, Kwon SO, Park GW, Cho K, Kwon KH, et al. Quantitative proteomic analysis of cell wall and plasma membrane fractions from multidrug-resistant Acinetobacter baumannii. J Proteome Res. 2011;10:459-69.
28. Vashist J, Tiwari V, Kapil A, Rajeswari MR. Quantitative profiling and identification of outer membrane proteins of beta-lactam resistant strain of Acinetobacter baumannii. J Proteome Res. 2010;9:1121-8.
29. Yun SH, Choi CW, Park SH, Lee JC, Leem SH, Choi JS, et al. Proteomic analysis of outer membrane proteins from Acinetobacter baumannii DU202 in tetracycline stress condition. J Microbiol. 2008;46:720-7.
30. Soares NC, Cabral MP, Parreira JR, Gayoso C, Barba MJ, Bou G. 2-DE analysis indicates that Acinetobacter baumannii displays a robust and versatile metabolism. Proteome Sci. 2009;7:37.
31. Cabral MP, Soares NC, Aranda J, Parreira JR, Rumbo C, Poza M, et al. Proteomic and functional analyses reveal a unique lifestyle for Acinetobacter baumannii biofilms and a key role for histidine metabolism. J Proteome Res. 2011;10:3399-417.
32. Chopra S, Ramkissoon K, Anderson DC. A systematic quantitative proteomic examination of multidrug resistance in Acinetobacter baumannii. J Proteomics. 2013;12:17-39.
33. Pradet-Balade B, Boulme F, Beug H, Mullner EW, Garcia-Sanz JA. Translation control: bridging the gap between genomics and proteomics? Trends Biochem Sci. 2001;26:225-9.
34. Echenique JR, Dorsey CW, Patrito LC, Petroni A, Tolmasky ME, Actis LA. Acinetobacter baumannii has two genes encoding glutathione-dependent formaldehyde dehydrogenase: evidence for differential regulation in response to iron. Microbiology. 2001;147:2805-15.
35. Hood MI, Jacobs AC, Sayood K, Dunman PM, Skaar EP. Acinetobacter baumannii increases tolerance to antibiotics in response to monovalent cations. Antimicrob Agents Chemother. 2010;54:1029-41.
36. Brossard KA, Campagnari AA. The Acinetobacter baumannii biofilm-associated protein plays a role in adherence to human epithelial cells. Infect Immun. 2012;80:228-33.
37. Zimbler DL, Park TM, Arivett BA, Penwell WF, Greer SM, Woodruff TM, et al. Stress response and virulence functions of the Acinetobacter baumannii NfuA Fe-S scaffold protein. J Bacteriol. 2012;194:2884-93.
38. Eijkelkamp BA, Hassan KA, Paulsen IT, Brown MH. Investigation of the human pathogen Acinetobacter baumannii under iron limiting conditions. BMC Genomics. 2011;12:126.
39. Jacobs AC, Sayood K, Olmsted SB, Blanchard CE, Hinrichs S, Russell D, et al. Characterization of the Acinetobacter baumannii growth phase-dependent and serum responsive transcriptomes. FEMS Immunol Med Microbiol. 2012;64:403-12.
40. Nwugo CC, Gaddy JA, Zimbler DL, Actis LA. Deciphering the iron response in Acinetobacter baumannii: a proteomics approach. J Proteomics. 2011;74:44-58.
41. Zhang X, El-Hajj ZW, Newman E. Deficiency in L-Serine deaminase interferes with one-carbon metabolism and cell wall synthesis in Escherichia coli K-12. J Bacteriol. 2010;192:5515-25.
42. Emanuele Jr JJ, Jin H, Jacobson BL, Chang CY, Einspahr HM, Villafranca JJ. Kinetic and crystallographic studies of Escherichia coli UDP-N-acety1muramate:L-alanine ligase. Protein Sci. 1996;5:2566-74.
43. Camejo A, Buchrieser C, Couvé E, Carvalho F, Reis O, Ferreira P, et al. In vivo transcriptional profiling of listeria monocytogenes and mutagenesis identify new virulence factors involved in infection. PLoS Pathog. 2009;5:e1000449.
44. White TA, Kell DB. Comparative genomic assessment of novel broad-spectrum targets for antibacterial drugs. Comp Funct Genom. 2004;5:304-27.
45. El Zoeiby A, Sanschagrin F, Lamoureux J, Darveau A, Levesque RC. Cloning, over-expression and purification of Pseudomonas aeruginosa murC encoding uridine diphosphate N-acetylmuramate: L-alanine ligase. FEMS Microbiol Lett. 2000;183(2):281-8.
46. Zawadzke LE, Norcia M, Desbonnet CR, Wang H, Freeman-Cook K, Dougherty TJ. Identification of an inhibitor of the MurC enzyme, which catalyzes an essential step in the peptidoglycan precursor synthesis pathway. Assay Drug Dev Technol. 2008;6:95-103.
47. Hameed PS, Manjrekar P, Chinnapattu M, Humnabadkar V, Shanbhag G, Kedari C, et al. Pyrazolopyrimidines establish MurC as a vulnerable target in Pseudomonas aeruginosa and Escherichia coli. ACS Chem Biol. 2014;9(10):2274-82.
48. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403-10.
49. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25:3389-402.
50. Deng WL, Lin YC, Lin RH, Wei CF, Huang YC, Peng HL, et al. Effects of galU Mutation on Pseudomonas syringae-plant interactions. Mol Plant-Microbe Interact. 2010;23:1184-96.
51. Jayakar HR, Parvathareddy J, Fitzpatrick EA, Bina XR, Bina JE, Re F, et al. A galU mutant of francisella tularensis is attenuated for virulence in a murine pulmonary model of tularemia. BMC Microbiol. 2011;179:1471-2180.
52. Jiang SS, Lin TY, Wang WB, Liu MC, Hsueh PR, Liaw SJ. Characterization of UDP-glucose dehydrogenase and UDP-glucose pyrophosphorylase mutants of Proteus mirabilis: defectiveness in polymyxin B resistance swarming and virulence. Antimicrob Agents Chemother. 2010;54:2000-9.
53. Mollerach M, López R, García E. Characterization of the galU gene of Streptococcus pneumoniae encoding a uridine diphosphoglucose pyrophosphorylase: a gene essential for capsular polysaccharide biosynthesis. J Exp Med. 1998;188:2047-56.
54. Priebe GP, Dean CR, Zaidi T, Meluleni GJ, Coleman FT, Coutinho YS, et al. The galU Gene of Pseudomonas aeruginosa is required for corneal infection and efficient systemic spread following pneumonia but not for infection confined to the lung. Infect Immun. 2004;72:4224-32.
55. Crosa JH, Mey AR, Payne SM. Iron Transport in Bacteria. Washington, DC: ASM Press; 2004.
56. Skaar EP. The battle for iron between bacterial pathogens and their vertebrate hosts. PLoS Pathog. 2010;6, e1000949.
57. Dittrich AM, Meyer HA, Hamelmann E. The role of lipocalins in airway disease. Clin Exp Allergy. 2013;43:503-11.
58. Välimäki E, Miettinen JJ, Lietzén N, Matikainen S, Nyman TA. Monosodium urate activates Src/Pyk2/PI3 Kinase and Cathepsin dependent unconventional protein secretion from human primary macrophages. Mol Cell Proteomics. 2013;12:749-63.
59. Miethke M, Marahiel MA. Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev. 2007;71:413-51.
60. Raffatellu M, George MD, Akiyama Y, Hornsby MJ, Nuccio SP, Paixao TA. Lipocalin-2 resistance confers an advantage to Salmonella enterica serotype Typhimurium for growth and survival in the inflamed intestine. Cell Host Microbe. 2009;5:476-86.
61. Proschak A, Lubuta P, Grün P, Löhr F, Wilharm G, Berardinis VD, et al. Structure and Biosynthesis of Fimsbactins A-F, Siderophores from Acinetobacter baumannii and Acinetobacter baylyi. ChemBioChem. 2013;14:633-8.
62. Wen ZT, Suntharaligham P, Cvitkovitch DG, Burne RA. Trigger factor in Streptococcus mutans is involved in stress tolerance competence development and biofilm formation. Infect Immun. 2005;73:219-25.
63. Ullers RS, Schwager DAF, Georgopoulos C, Genevaux P. Trigger factor can antagonize both SecB and DnaK/DnaJ chaperone functions in Escherichia coli. PNAS. 2007;104:3101-6.
64. Bigot A, Botton E, Dubail I, Charbit A. A homolog of Bacillus subtilis trigger factor in Listeria monocytogenes is involved in stress tolerance and bacterial virulence. Appl Environ Microbiol. 2006;72:6623-31.
65. Henard CA, Bourret TJ, Song M, Vázquez-Torres A. Control of redox balance by the stringent response regulatory protein promotes antioxidant defenses of Salmonella. J Biol Chem. 2010;285:36785-93.
66. Frees D, Chastanet A, Qazi S, Sørensen K, Hill P, Msadek T, et al. Clp ATPases are required for stress tolerance intracellular replication and biofilm formation in Staphylococcus aureus. Mol Microbiol. 2004;54:1445-62.
67. Eijkelkamp BA, Stroeher UH, Hassan KA, Papadimitrious MS, Paulsen IT, Brown MH. Adherence and motility characteristics of clinical Acinetobacter baumannii isolates. FEMS Microbiol Lett. 2011;323:44-51.
68. Choi CH, Lee EY, Lee YC, Park TI, Kim HJ, Hyun SH, et al. Outer membrane protein 38 of Acinetobacter baumannii localizes to the mitochondria and induces apoptosis of epithelial cells. Cell Microbiol. 2005;7:1127-38.
69. Gaddy JA, Tomaras AP, Actis LA. The Acinetobacter baumannii 19606 OmpA protein plays a role in biofilm formation on abiotic surfaces and in the interaction of this pathogen with eukaryotic cells. Infect Immun. 2009;77:3150-60.
70. Law RJ, Hamlin JN, Sivro A, McCorrister SJ, Cardama GA, Cardona ST. A functional phenylacetic acid catabolic pathway is required for full pathogenicity of Burkholderia cenocepacia in the Caenorhabditis elegans host model. J Bacteriol. 2008;190:7209-18.
71. Wu JW, Chen XL. Extracellular metalloproteases from bacteria. Appl Microbiol Biotechnol. 2011;92:253-62.
72. Moro A, Ruiz-Cabello F, Fernandez-Cano A, Stock RP, González A. Secretion by trypanosoma cruzi of a peptidyl-prolpyl cis-trans isomerase involved in cell infection. EMBO J. 1995;14:2483-90.
73. Moulder JW. Comparative biology of intracellular parasitism. Microbiol Rev. 1985;49:298-337.
74. Hermans PWM, Adrian PV, Albert C, Estevao S, Hoogenboezem T, Luijendijk IHT, et al. The Streptococcal lipoprotein rotamase A (SlrA) is a functional peptidyl-prolyl isomerase involved in pneumococcal colonization. J Biol Chem. 2006;281:968-76.
75. Xia Q, Wang T, Taub F, Park Y, Capestany CA, Lamont RJ, et al. Quantitative proteomics of intracellular Porphyromonas gingivalis. Proteomics. 2007;7:4323-37.
76. Dieppedale J, Sobral D, Dupuis M, Dubail I, Klimentova J, Stulik J, et al. Charbit: a identification of a putative chaperone involved in stress resistance and virulence in Francisella tularensis. Infect Immun. 2011;79:1428-39.
77. Umland TC, Schultz LW, MacDonald U, Beanan JM, Olson R, Russo TA. In vivo-validated essential genes identified in acinetobacter baumanniiby using human ascites overlap poorly with essential genes detected on laboratory media. mBio. 2012;3:e00113-12.
78. Merino M, Alvarez-Fraga L, Gómez MJ, Aransay AM, Lavín JL, Chaves F, et al. Complete genome sequence of the multiresistant Acinetobacter baumannii strain AbH12O-A2, isolated during a large outbreak in Spain. Genome Announc. 2014;2(6):e01182-14.
79. Fernández-Puente P, Mateos J, Fernández-Costa C, Oreiro N, Fernández-López C, Ruiz-Romero C, et al. Identification of a panel of novel serum osteoarthritis biomarkers. J Proteome Res. 2011;10:5095-101.
80. Wu J, Kobayashi M, Sousa EA, Liu W, Cai J, Goldman SJ, et al. Differential proteomic analysis of bronchoalveolar lavage fluid in asthmatics following segmental antigen challenge. Mol Cell Proteomics. 2005;4:1251-64.
81. Crowther JE, Kutala VK, Kuppusamy P, Ferguson JS, Beharka AA, Zweier JL, et al. Pulmonary surfactant protein a inhibits macrophage reactive oxygen intermediate production in response to stimuli by reducing NADPH oxidase activity. J Immunol. 2004;172:6866-74.
82. Polati R, Castagna A, Bossi A, Campostrini N, Zaninotto F, Timperio AM, et al. High resolution preparation of monocyte-derived macrophages (MDM) protein fractions for clinical proteomics. Proteome Sci. 2009;7:4.