Identification of an Acinetobacter baumannii Zinc Acquisition System that Facilitates Resistance to Calprotectin-mediated Zinc Sequestration

PLoS Pathogens

Volumn 8, Issue 12, 2012, Pages

  Hood, M Indriati ^a   Mortensen, Brittany L ^a   Moore, Jessica L ^a,b   Zhang, Yaofang ^a   Kehl Fie, Thomas E ^a   Sugitani, Norie ^a,b   Chazin, Walter J ^a,b   Caprioli, Richard M ^b   Skaar, Eric P ^a  

^a VANDERBILT UNIVERSITY   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALGRANULIN; IMIPENEM; KANAMYCIN; LEVOFLOXACIN; ZINC ION;

ACINETOBACTER BAUMANNII; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; CHELATION; CONTROLLED STUDY; DRUG SENSITIVITY; GEL MOBILITY SHIFT ASSAY; GROWTH INHIBITION; HISTOLOGY; LUNG INJURY; MALE; MASS SPECTROMETRY; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; PROTEIN PURIFICATION; REPORTER GENE; TRANSPOSON; ZINC METABOLISM;

ACINETOBACTER BAUMANNII; ACINETOBACTER INFECTIONS; ANIMALS; BIOLOGICAL TRANSPORT, ACTIVE; CARBAPENEMS; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, MULTIPLE, BACTERIAL; HUMANS; LEUKOCYTE L1 ANTIGEN COMPLEX; LUNG; MANGANESE; MICE; MICE, KNOCKOUT; NEUTROPHIL INFILTRATION; NEUTROPHILS; PNEUMONIA, BACTERIAL; ZINC;

ACINETOBACTER BAUMANNII; BACTERIA (MICROORGANISMS); MURINAE;

EID: 84872024018     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003068     Document Type: Article

References (63)

1. Gaynes R, Edwards JR, System NNIS, (2005) Overview of nosocomial infections caused by gram-negative bacilli. Clin Infect Dis 41: 848-854.
2. Erdem I, Ozgultekin A, Sengoz Inan A, Dincer E, Turan G, et al. (2008) Incidence, etiology, and antibiotic resistance patterns of gram-negative microorganisms isolated from patients with ventilator-associated pneumonia in a medical-surgical intensive care unit of a teaching hospital in Istanbul, Turkey (2004-2006). Jpn J Infect Dis 61: 339-342.
3. Garza-González E, Llaca-Díaz JM, Bosques-Padilla FJ, González GM, (2010) Prevalence of multidrug-resistant bacteria at a tertiary-care teaching hospital in Mexico: special focus on Acinetobacter baumannii. Chemotherapy 56: 275-279.
4. Jean S-S, Hsueh P-R, (2011) High burden of antimicrobial resistance in Asia. Int J Antimicrob Agents 37: 291-295.
5. Jean S-S, Hsueh P-R, Lee W-S, Chang H-T, Chou M-Y, et al. (2009) Nationwide surveillance of antimicrobial resistance among non-fermentative Gram-negative bacteria in Intensive Care Units in Taiwan: SMART programme data 2005. Int J Antimicrob Agents 33: 266-271.
6. Vincent J-L, Rello J, Marshall J, Silva E, Anzueto A, et al. (2009) International study of the prevalence and outcomes of infection in intensive care units. JAMA 302: 2323-2329.
7. Jawad A, Seifert H, Snelling AM, Heritage J, Hawkey PM, (1998) Survival of Acinetobacter baumannii on dry surfaces: comparison of outbreak and sporadic isolates. J Clin Microbiol 36: 1938-1941.
8. Fuangthong M, Julotok M, Chintana W, Kuhn K, Rittiroongrad S, et al. (2011) Exposure of Acinetobacter baylyi ADP1 to the biocide chlorhexidine leads to acquired resistance to the biocide itself and to oxidants. J Antimicrob Chemother 66: 319-322.
9. Kawamura-Sato K, Wachino J-i, Kondo T, Ito H, Arakawa Y, (2010) Correlation between reduced susceptibility to disinfectants and multidrug resistance among clinical isolates of Acinetobacter species. J Antimicrob Chemother 65: 1975-1983.
10. Rajamohan G, Srinivasan VB, Gebreyes WA, (2009) Biocide-tolerant multidrug-resistant Acinetobacter baumannii clinical strains are associated with higher biofilm formation. J Hosp Infect 73: 287-289.
11. Apisarnthanarak A, Mundy LM, (2009) Mortality associated with Pandrug-resistant Acinetobacter baumannii infections in Thailand. Am J Infect Control 37: 519-520.
12. Chan P-C, Huang L-M, Lin H-C, Chang L-Y, Chen M-L, et al. (2007) Control of an outbreak of pandrug-resistant Acinetobacter baumannii colonization and infection in a neonatal intensive care unit. Infect Control Hosp Epidemiol 28: 423-429.
13. Falagas ME, Bliziotis IA, (2007) Pandrug-resistant Gram-negative bacteria: the dawn of the post-antibiotic era? Int J Antimicrob Agents 29: 630-636.
14. Falagas ME, Rafailidis PI, Matthaiou DK, Virtzili S, Nikita D, et al. (2008) Pandrug-resistant Klebsiella pneumoniae, Pseudomonas aeruginosa and Acinetobacter baumannii infections: characteristics and outcome in a series of 28 patients. Int J Antimicrob Agents 32: 450-454.
15. Souli M, Galani I, Giamarellou H, (2008) Emergence of extensively drug-resistant and pandrug-resistant Gram-negative bacilli in Europe. Euro Surveill 13: pii: 19045.
16. Mortensen BL, Skaar EP, (2012) Host-microbe interactions that shape the pathogenesis of Acinetobacter baumannii infection. Cell Microbiol 14: 1336-44.
17. Hood MI, Skaar EP, Nutritional immunity: transition metals at the pathogen-host interface. Nat Rev Microbiol 10: 525-37.
18. Weinberg ED, (1975) Nutritional immunity. Host's attempt to withold iron from microbial invaders. JAMA 231: 39-41.
19. Weinberg ED, (2009) Iron availability and infection. Biochim Biophys Acta 1790: 600-605.
20. Corbin BD, Seeley EH, Raab A, Feldmann J, Miller MR, et al. (2008) Metal chelation and inhibition of bacterial growth in tissue abscesses. Science 319: 962-965.
21. Bianchi M, Niemiec MJ, Siler U, Urban CF, Reichenbach J, (2011) Restoration of anti-Aspergillus defense by neutrophil extracellular traps in human chronic granulomatous disease after gene therapy is calprotectin-dependent. J Allergy Clin Immunol 127: 1243-1252.e1247.
22. Kehl-Fie TE, Chitayat S, Hood MI, Damo S, Restrepo N, et al. (2011) Nutrient metal sequestration by calprotectin inhibits bacterial superoxide defense, enhancing neutrophil killing of Staphylococcus aureus. Cell Host Microbe 10: 158-164.
23. Liu JZ, Jellbauer S, Poe A, Ton V, Pesciaroli M, et al. (2012) Zinc sequestration by the neutrophil protein calprotectin enhances Salmonella growth in the inflamed gut. Cell Host Microbe 11: 227-239.
24. Urban CF, Ermert D, Schmid M, Abu-Abed U, Goosmann C, et al. (2009) Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Path 5: e1000639.
25. Actis LA, Tolmasky ME, Crosa LM, Crosa JH, (1993) Effect of iron-limiting conditions on growth of clinical isolates of Acinetobacter baumannii. J Clin Microbiol 31: 2812-2815.
26. Dorsey CW, Beglin MS, Actis LA, (2003) Detection and analysis of iron uptake components expressed by Acinetobacter baumannii clinical isolates. J Clin Microbiol 41: 4188-4193.
27. Dorsey CW, Tolmasky ME, Crosa JH, Actis LA, (2003) Genetic organization of an Acinetobacter baumannii chromosomal region harbouring genes related to siderophore biosynthesis and transport. Microbiology 149: 1227-1238.
28. Dorsey CW, Tomaras AP, Connerly PL, Tolmasky ME, Crosa JH, et al. (2004) The siderophore-mediated iron acquisition systems of Acinetobacter baumannii ATCC 19606 and Vibrio anguillarum 775 are structurally and functionally related. Microbiology 150: 3657-3667.
29. Echenique JR, Arienti H, Tolmasky ME, Read RR, Staneloni RJ, et al. (1992) Characterization of a high-affinity iron transport system in Acinetobacter baumannii. J Bacteriol 174: 7670-7679.
30. Zimbler DL, Penwell WF, Gaddy JA, Menke SM, Tomaras AP, et al. (2009) Iron acquisition functions expressed by the human pathogen Acinetobacter baumannii. Biometals 22: 23-32.
31. Hsu K, Champaiboon C, Guenther BD, Sorenson BS, Khammanivong A, et al. (2009) Anti-infective protective properties of S100 calgranulins. Antiinflamm Antiallergy Agents Med Chem 8: 290-305.
32. McCormick A, Heesemann L, Wagener J, Marcos V, Hartl D, et al. (2010) NETs formed by human neutrophils inhibit growth of the pathogenic mold Aspergillus fumigatus. Microb Infect 12: 928-936.
33. Terrin G, Passariello A, Manguso F, Salvia G, Rapacciuolo L, et al. (2011) Serum calprotectin: an antimicrobial peptide as a new marker for the diagnosis of sepsis in very low birth weight newborns. Clin Dev Immunol 2011: 291085.
34. Brandtzaeg P, Gabrielsen TO, Dale I, Müller F, Steinbakk M, et al. (1995) The leucocyte protein L1 (calprotectin): a putative nonspecific defence factor at epithelial surfaces. Adv Exp Med Biol 371A: 201-206.
35. Qiu H, KuoLee R, Harris G, Chen W, (2009) Role of NADPH phagocyte oxidase in host defense against acute respiratory Acinetobacter baumannii infection in mice. Infect Immun 77: 1015-1021.
36. van Faassen H, KuoLee R, Harris G, Zhao X, Conlan JW, et al. (2007) Neutrophils play an important role in host resistance to respiratory infection with Acinetobacter baumannii in mice. Infect Immun 75: 5597-5608.
37. Attia AS, Schroeder KA, Seeley EH, Wilson KJ, Hammer ND, et al. (2012) Monitoring the inflammatory response to infection through the integration of MALDI IMS and MRI. Cell Host Microbe 11: 664-673.
38. Manitz M-P, Horst B, Seeliger S, Strey A, Skryabin BV, et al. (2003) Loss of S100A9 (MRP14) results in reduced interleukin-8-induced CD11b surface expression, a polarized microfilament system, and diminished responsiveness to chemoattractants in vitro. Mol Cell Biol 23: 1034-1043.
39. Rahman SMJ, Gonzalez AL, Li M, Seeley EH, Zimmerman LJ, et al. (2011) Lung cancer diagnosis from proteomic analysis of preinvasive lesions. Cancer Res 71: 3009-3017.
40. Ammendola S, Pasquali P, Pistoia C, Petrucci P, Petrarca P, et al. (2007) High-affinity Zn2+ uptake system ZnuABC is required for bacterial zinc homeostasis in intracellular environments and contributes to the virulence of Salmonella enterica. Infect Immun 75: 5867-5876.
41. Campoy S, Jara M, Busquets N, Pérez de Rozas AM, Badiola I, et al. (2002) Role of the high-affinity zinc uptake znuABC system in Salmonella enterica serovar Typhimurium virulence. Infect Immun 70: 4721-4725.
42. Davis LM, Kakuda T, DiRita VJ, (2009) A Campylobacter jejuni znuA orthologue is essential for growth in low-zinc environments and chick colonization. J Bacteriol 191: 1631-1640.
43. Desrosiers DC, Bearden SW, Mier I, Abney J, Paulley JT, et al. (2010) Znu is the predominant zinc importer in Yersinia pestis during in vitro growth but is not essential for virulence. Infect Immun 78: 5163-5177.
44. Shin J-H, Jung HJ, An YJ, Cho Y-B, Cha S-S, et al. (2011) Graded expression of zinc-responsive genes through two regulatory zinc-binding sites in Zur. Proc Natl Acad Sci U S A 108: 5045-5050.
45. Gaballa A, Helmann JD, (1998) Identification of a zinc-specific metalloregulatory protein, Zur, controlling zinc transport operons in Bacillus subtilis. J Bacteriol 180: 5815-5821.
46. Huang D-L, Tang D-J, Liao Q, Li H-C, Chen Q, et al. (2008) The Zur of Xanthomonas campestris functions as a repressor and an activator of putative zinc homeostasis genes via recognizing two distinct sequences within its target promoters. Nucleic Acids Res 36: 4295-4309.
47. Li Y, Qiu Y, Gao H, Guo Z, Han Y, et al. (2009) Characterization of Zur-dependent genes and direct Zur targets in Yersinia pestis. BMC Microbiol 9: 128.
48. Panina EM, Mironov AA, Gelfand MS, (2003) Comparative genomics of bacterial zinc regulons: enhanced ion transport, pathogenesis, and rearrangement of ribosomal proteins. Proc Natl Acad Sci U S A 100: 9912-9917.
49. Kallifidas D, Pascoe B, Owen GA, Strain-Damerell CM, Hong H-J, et al. (2010) The zinc-responsive regulator Zur controls expression of the coelibactin gene cluster in Streptomyces coelicolor. J Bacteriol 192: 608-611.
50. Maciag A, Dainese E, Rodriguez GM, Milano A, Provvedi R, et al. (2007) Global analysis of the Mycobacterium tuberculosis Zur (FurB) regulon. J Bacteriol 189: 730-740.
51. Stork M, Bos MP, Jongerius I, de Kok N, Schilders I, et al. (2010) An outer membrane receptor of Neisseria meningitidis involved in zinc acquisition with vaccine potential. PLoS Path 6: e1000969.
52. Kumar P, Sannigrahi S, Tzeng Y-L, (2012) The Neisseria meningitidis ZnuD zinc receptor contributes to interactions with epithelial cells and supports heme utilization when expressed in Escherichia coli. Infect Immun 80: 657-667.
53. Eijkelkamp B, Hassan K, Paulsen I, Brown M, (2011) Investigation of the human pathogen Acinetobacter baumannii under iron limiting. BMC Genomics 12: 126.
54. Esterly JS, Griffith M, Qi C, Malczynski M, Postelnick MJ, et al. (2011) Impact of carbapenem resistance and receipt of active antimicrobial therapy on clinical outcomes of Acinetobacter baumannii bloodstream infections. Antimicrob Agents Chemother 55: 4844-4849.
55. Queenan AM, Pillar CM, Deane J, Sahm DF, Lynch AS, et al. (2012) Multidrug resistance among Acinetobacter spp. in the USA and activity profile of key agents: results from CAPITAL Surveillance 2010. Diagn Microbiol Infect Dis 73: 267-270.
56. Sowmiya M, Umashankar V, Muthukumaran S, Madhavan H, Malathi J, (2012) Studies on New Delhi Metallo-Beta-Lactamse-1 producing Acinetobacter baumannii isolated from donor swab in a tertiary eye care centre, India and structural analysis of its antibiotic binding interactions. Bioinformation 8: 445-452.
57. Nordmann P, Poirel L, Walsh TR, Livermore DM, (2011) The emerging NDM carbapenemases. Trends Microbiol 19: 588-595.
58. Adams MD, Goglin K, Molyneaux N, Hujer KM, Lavender H, et al. (2008) Comparative genome sequence analysis of multidrug-resistant Acinetobacter baumannii. J Bacteriol 190: 8053-8064.
59. Kehl-Fie TE, Skaar EP, (2010) Nutritional immunity beyond iron: a role for manganese and zinc. Curr Opin Chem Biol 14: 218-224.
60. Jacobs AC, Hood I, Boyd KL, Olson PD, Morrison J, et al. (2010) Inactivation of Phospholipase D diminishes Acinetobacter baumannii pathogenesis. Infect Immun 78: 1952-1962.
61. Aranda J, Poza M, Pardo B, Rumbo S, Rumbo C, et al. (2012) A rapid and simple method for constructing stable mutants of Acinetobacter. BMC Microbiol 10: 279.
62. Bailey TL, Williams N, Misleh C, Li WW, (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 34: W369-W373.
63. Crooks GE, Hon G, Chandonia JM, Brenner SE, (2004) WebLogo: a sequence logo generator. Genome Res 14: 1188-1190.