Glucose availability enhances lipopolysaccharide production and immunogenicity in the opportunistic pathogen Acinetobacter baumannii

Future Microbiology

Volumn 11, Issue 3, 2016, Pages 335-349

  Rossi, Elio ^a   Longo, Francesca ^a   Barbagallo, Marialuisa ^b   Peano, Clelia ^c   Consolandi, Clarissa ^c   Pietrelli, Alessandro ^c   Jaillon, Sebastian ^b   Garlanda, Cecilia ^b   Landini, Paolo ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^c INSTITUTE OF BIOMEDICAL TECHNOLOGIES   (Italy)

Author keywords

Acinetobacter baumannii; glucose; host pathogen interactions; innate immune response; LPS; macrophage; sepsis transcriptomics; virulence factors

Indexed keywords

CXCL1 CHEMOKINE; GLUCOSE; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; RNA; TUMOR NECROSIS FACTOR ALPHA; CULTURE MEDIUM; CYTOKINE;

ACINETOBACTER BAUMANNII; ARTICLE; BACTERIAL GROWTH; BACTERIUM ISOLATE; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; HEMOLYSIS; HUMAN; HUMAN CELL; IMMUNOGENICITY; MACROPHAGE; MACROPHAGE ACTIVATION; NONHUMAN; PRIORITY JOURNAL; REPORTER GENE; RNA SEQUENCE; SEPSIS; ACINETOBACTER INFECTION; BIOSYNTHESIS; CULTURE MEDIUM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PATHOGENICITY; TUMOR CELL LINE;

ACINETOBACTER BAUMANNII; ACINETOBACTER INFECTIONS; CELL LINE, TUMOR; CULTURE MEDIA; CYTOKINES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENES, REPORTER; GLUCOSE; HEMOLYSIS; HUMANS; LIPOPOLYSACCHARIDES; MACROPHAGES; SEPSIS;

EID: 84962467638     PISSN: 17460913     EISSN: 17460921     Source Type: Journal    
DOI: 10.2217/fmb.15.153     Document Type: Article

References (55)

1. McConnell MJ, Actis L, Pachón J. Acinetobacter baumannii: human infections, factors contributing to pathogenesis and animal models. FEMS Microbiol. Rev. 37, 130-155 (2013).
2. Valencia R, Arroyo LA, Conde M et al. Nosocomial outbreak of infection with pan-drug-resistant Acinetobacter baumannii in a tertiary care university hospital. Infect. Control Hosp. Epidemiol. 30, 257-263 (2009).
3. Vila J, Pachón J. Therapeutic options for Acinetobacter baumannii infections: an update. Expert. Opin. Pharmacother. 13, 2319-2336 (2012).
4. Dexter C, Murray GL, Paulsen IT, Peleg AY. Community-acquired Acinetobacter baumannii: clinical characteristics, epidemiology and pathogenesis. Expert. Rev. Anti Infect. Ther. 13, 567-573 (2015).
5. Choi CH, Lee EY, Lee YC 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).
6. Jin JS, Kwon SO, Moon DC et al. Acinetobacter baumannii secretes cytotoxic outer membrane protein A via outer membrane vesicles. PLoS ONE 6, e17027 (2011).
7. Luke NR, Sauberan SL, Russo TA et al. Identification and characterization of a glycosyltransferase involved in Acinetobacter baumannii lipopolysaccharide core biosynthesis. Infect. Immun. 78, 2017-2023 (2010).
8. Jawad A, Seifert H, Snelling AM, Heritage J, Hawkey PM. Survival of Acinetobacter baumannii on dry surfaces: comparison of outbreak and sporadic isolates. J. Clin. Microbiol. 36, 1938-1941 (1998).
9. Fiester SE, Actis LA. Stress responses in the opportunistic pathogen Acinetobacter baumannii. Future Microbiol. 8, 353-365 (2013).
10. Villegas MV, Hartstein AI. Acinetobacter outbreaks, 1977-2000. Infect. Control Hosp. Epidemiol. 24, 284-295 (2003).
11. Gaddy JA, Actis LA. Regulation of Acinetobacter baumannii biofilm formation. Future Microbiol. 4, 273-278 (2009).
12. Lee HW, Koh YM, Kim J et al. Capacity of multidrug-resistant clinical isolates of Acinetobacter baumannii to form biofilm and adhere to epithelial cell surfaces. Clin. Microbiol. Infect. 14, 49-54 (2008).
13. Choi AH, Slamti L, Avci FY, Pier GB, Maira-Litrán T. The pgaABCD locus of Acinetobacter baumannii encodes the production of poly-beta-1-6-Nacetylglucosamine, which is critical for biofilm formation. J. Bacteriol. 191, 5953-5963 (2009).
14. Tomaras AP, Dorsey CW, Edelmann RE, Actis LA. Attachment to and biofilm formation on abiotic surfaces by Acinetobacter baumannii: involvement of a novel chaperoneusher pili assembly system. Microbiology 149, 3473-3484 (2003).
15. Loehfelm TW, Luke NR, Campagnari AA. Identification and characterization of an Acinetobacter baumannii biofilm-associated protein. J. Bacteriol. 190, 1036-1044 (2008).
16. Russo TA, Luke NR, Beanan JM et al. The K1 capsular polysaccharide of Acinetobacter baumannii strain 307-0294 is a major virulence factor. Infect. Immun. 78, 3993-4000 (2010).
17. Marti S, Nait Chabane Y, Alexandre S et al. Growth of Acinetobacter baumannii in pellicle enhanced the expression of potential virulence factors. PLoS ONE 6, e26030 (2011).
18. Freckmann G, Hagenlocher S, Baumstark A et al. Continuous glucose profiles in healthy subjects under everyday life conditions and after different meals. J. Diabetes Sci. Technol. 1, 695-703 (2007).
19. Thennadil SN, Rennert JL, Wenzel BJ, Hazen KH, Ruchti TL, Block MB. Comparison of glucose concentration in interstitial fluid, and capillary and venous blood during rapid changes in blood glucose levels. Diabetes Technol. Ther. 3, 357-365 (2001).
20. Daddaoua A, Molina-Santiago C, de la Torre J, Krell T, Ramos JL. GtrS and GltR form a two-component system: the central role of 2- ketogluconate in the expression of exotoxin A and glucose catabolic enzymes in Pseudomonas aeruginosa. Nucleic Acids Res. 42, 7654-7663 (2014).
21. Munson GP. Virulence regulons of enterotoxigenic Escherichia coli. Immunol. Res. 57, 229-236 (2013).
22. Zarrilli R, Giannouli M, Rocco F et al. Genome sequences of three Acinetobacter baumannii strains assigned to the multilocus sequence typing genotypes ST2, ST25, and ST78. J. Bacteriol. 193, 2359-2360 (2011).
23. Dorel C, Vidal O, Prigent-Combaret C, Vallet I, Lejeune P. Involvement of the Cpx signal transduction pathway of E. coli in biofilm formation. FEMS Microbiol. Lett. 178, 169-175 (1999).
24. Nucleo E, Steffanoni L, Fugazza G et al. Growth in glucose-based medium and exposure to subinhibitory concentrations of imipenem induce biofilm formation in a multidrug-resistant clinical isolate of Acinetobacter baumannii. BMC Microbiol. 22, 9-270 (2009).
25. Spaink HP, Okker RJH, Wijffelman CA, Pees E, Lugtenberg BJJ. Promoters in the nodulation region of the Rhizobium leguminosarum Sym plasmid pRL1J1. Plant. Mol. Biol. 9, 27-39 (1987).
26. Peano C, Chiaramonte F, Motta S et al. Gene and protein expression in response to different growth temperatures and oxygen availability in Burkholderia thailandensis. PLoS ONE 9, e93009 (2014).
27. Goldberg JB, Ohman DE. Cloning and expression in Pseudomonas aeruginosa of a gene involved in the production of alginate. J. Bacteriol. 158, 1115-1121 (1984).
28. Miller JH. Experiments In Molecular Genetics. Cold Spring Harbor Laboratory Press, NY, USA (1972).
29. Antunes LC, Imperi F, Carattoli A, Visca P. Deciphering the multifactorial nature of Acinetobacter baumannii pathogenicity. PLoS ONE 6, e22674 (2011).
30. Blocker A, Gounon P, Larquet E et al. The tripartite type III secreton of Shigella flexneri inserts IpaB and IpaC into host membranes. J. Cell. Biol. 147, 683-693 (1999).
31. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F. Colorimetric method for determination of sugars and related substances. Anal. Chem. 28, 350-356 (1956).
32. Marolda CL, Lahiry P, Vinés E, Saldías S, Valvano MA. Micromethods for the characterization of lipid A-core and O-antigen lipopolysaccharide. Methods Mol. Biol. 347, 237-252 (2006).
33. Maskell JP. The resolution of bacteroides lipopolysaccharides by polyacrylamide gel electrophoresis. J. Med. Microbiol. 34, 253-257 (1991).
34. Reuhs BL, Carlson RW, Kim JS. Rhizobium fredii and Rhizobium meliloti produce 3-deoxy-d-manno-2-octulosonic acidcontaining polysaccharides that are structurally analogous to group II K antigens (capsular polysaccharides) found in Escherichia coli. J. Bacteriol. 175, 3570-3580 (1993).
35. Moalli F, Doni A, Deban L et al. Role of complement and Fc{gamma} receptors in the protective activity of the long pentraxin PTX3 against Aspergillus fumigatus. Blood 116, 5170-5180 (2010).
36. R Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria (2015). www.R-project.org
37. Muller LM, Gorter KJ, Hak E et al. Increased risk of common infections in patients with Type 1 and Type 2 diabetes mellitus. Clin. Infect. Dis. 41, 281-288 (2005).
38. Patric. www.patricbrc.org
39. Cox RA. Quantitative relationships for specific growth rates and macromolecular compositions of Mycobacterium tuberculosis, Streptomyces coelicolor A3 (2) and Escherichia coli B/r: an integrative theoretical approach. Microbiology 150, 1413-1426 (2004).
40. Cabral MP, Soares NC, Aranda J et al. Proteomic and functional analyses reveal a unique lifestyle for Acinetobacter baumannii biofilms and a key role for histidine metabolism. J. Proteome Res. 10, 3399-3417 (2011).
41. Tayabali AF, Nguyen KC, Shwed PS, Crosthwait J, Coleman G, Seligy VL. Comparison of the virulence potential of Acinetobacter strains from clinical and environmental sources. PLoS ONE 7, e37024 (2012).
42. Villa F, Remelli W, Forlani F, Gambino M, Landini P, Cappitelli F. Effects of chronic sub-lethal oxidative stress on biofilm formation by Azotobacter vinelandii. Biofouling 28, 823-833 (2012).
43. Fregolino E, Gargiulo V, Lanzetta R, Parrilli M, Holst O, Castro CD. Identification and structural determination of the capsular polysaccharides from two Acinetobacter baumannii clinical isolates, MG1 and SMAL. Carbohydr. Res. 346(7), 973-977 (2011).
44. Kenyon JJ, Holt KE, Pickard D, Dougan G, Hall RM. Insertions in the OCL1 locus of Acinetobacter baumannii lead to shortened lipooligosaccharides. Res. Microbiol. 165(6), 472-475 (2014).
45. Kenyon JJ, Nigro SJ, Hall RM. Variation in the OC Locus of Acinetobacter baumannii genomes predicts extensive structural diversity in the Lipooligosaccharide. PLoS ONE 9(9), e107833 (2014).
46. Mattsby-Baltzer I, Lindgren K, Lindholm B, Edebo L. Endotoxin shedding by enterobacteria: free and cell-bound endotoxin differ in Limulus activity. Infect. Immun. 59, 689-695 (1991).
47. Beveridge TJ. Structures of Gram-negative cell walls and their derived membrane vesicles. J. Bacteriol. 181, 4725-4733 (1999).
48. Li ZT, Zhang RL, Bi XG et al. Outer membrane vesicles isolated from two clinical Acinetobacter baumannii strains exhibit different toxicity and proteome characteristics. Microb. Pathog. 81, 46-52 (2015).
49. Jun SH, Lee JH, Kim BR et al. Acinetobacter baumannii outer membrane vesicles elicit a potent innate immune response via membrane proteins. PLoS ONE 8, e71751 (2013).
50. Bleumink-Pluym NM, van Alphen LB, Bouwman LI, Wösten MM, van Putten JP. Identification of a functional type VI secretion system in Campylobacter jejuni conferring capsule polysaccharide sensitive cytotoxicity. PLoS Pathog. 9, e1003393 (2013).
51. Weber BS, Miyata ST, Iwashkiw JA et al. Genomic and functional analysis of the type VI secretion system in Acinetobacter. PLoS ONE 8, e55142 (2013).
52. Carruthers MD, Nicholson PA, Tracy EN, Munson RS Jr. Acinetobacter baumannii utilizes a type VI secretion system for bacterial competition. PLoS ONE 8, e59388 (2013).
53. Ciznár I, Shands JW Jr. Effect of alkalitreated lipopolysaccharide on erythrocyte membrane stability. Infect. Immun. 4, 362-367 (1971).
54. Carr C Jr, Morrison DC. Mechanism of polymyxin B-mediated lysis of lipopolysaccharide-treated erythrocytes. Infect. Immun. 49, 84-89 (1985).
55. Poole K, Braun V. Influence of growth temperature and lipopolysaccharide on hemolytic activity of Serratia marcescens. J. Bacteriol. 170, 5146-5152 (1988).