Type VI secretion is a major virulence determinant in Burkholderia mallei

Molecular Microbiology

Volumn 64, Issue 6, 2007, Pages 1466-1485

  Schell, Mark A ^a   Ulrich, Ricky L ^b   Ribot, Wilson J ^b   Brueggemann, Ernst E ^b   Hines, Harry B ^b   Chen, Dan ^c   Lipscomb, Lyla ^a   Kim, H Stanley ^d   Mrázek, Jan ^a   Nierman, William C ^c   DeShazer, David ^b  

^a UNIVERSITY OF GEORGIA   (United States)

^b UNITED STATES ARMY MEDICAL RESEARCH INSTITUTE OF INFECTIOUS DISEASES   (United States)

^c J CRAIG VENTER INSTITUTE   (United States)

^d Korea University College of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN FILAMENT; ARTICLE; BACTERIAL GENE; BACTERIAL MEMBRANE; BACTERIAL VIRULENCE; BURKHOLDERIA MALLEI; CONTROLLED STUDY; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENE MUTATION; GENE OVEREXPRESSION; GRAM NEGATIVE BACTERIUM; HAMSTER; MASS SPECTROMETRY; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN POLYMERIZATION; SECRETORY VESICLE; TRANSCRIPTION INITIATION;

ANIMALS; BACTERIAL PROTEINS; BURKHOLDERIA MALLEI; CELL LINE; CRICETINAE; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GLANDERS; HORSES; HUMANS; MACROPHAGES; MESOCRICETUS; MICE; MICE, INBRED BALB C; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; VIRULENCE;

BURKHOLDERIA MALLEI; CRICETINAE; EQUIDAE; MUS;

EID: 34249980077     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2007.05734.x     Document Type: Article

References (68)

1. Benz, I. Schmidt, M.A. (2001) Glycosylation with heptose residues mediated by the aah gene product is essential for adherence of the AIDA-I adhesin. Mol Microbiol 40 : 1403 1413.
2. Bladergroen, M.R., Badelt, K. Spaink, H.P. (2003) Infection-blocking genes of a symbiotic Rhizobium leguminosarum strain that are involved in temperature-dependent protein secretion. Mol Plant Microbe Interact 16 : 53 64.
3. Bossi, P., Tegnell, A., Baka, A., van Loock, F., Hendriks, J., Werner, A., et al. (2004) Bichat guidelines for the clinical management of glanders and melioidosis and bioterrorism-related glanders and melioidosis. Euro Surveill 9 : 1 6.
4. Brundage, R.A., Smith, G.A., Camilli, A., Theriot, J.A. Portnoy, D.A. (1993) Expression and phosphorylation of the Listeria monocytogenes ActA protein in mammalian cells. Proc Natl Acad Sci USA 90 : 11890 11894.
5. Cardona, S.T. Valvano, M.A. (2005) An expression vector containing a rhamnose-inducible promoter provides tightly regulated gene expression in Burkholderia cenocepacia. Plasmid 54 : 219 228.
6. Carlsson, F. Brown, E.J. (2006) Actin-based motility of intracellular bacteria, and polarized surface distribution of the bacterial effector molecules. J Cell Physiol 209 : 288 296.
7. Chain, P.S., Denef, V.J., Konstantinidis, K.T., Vergez, L.M., Agullo, L., Reyes, V.L., et al. (2006) Burkholderia xenovorans LB400 harbors a multi-replicon, 9.73-Mbp genome shaped for versatility. Proc Natl Acad Sci USA 103 : 15280 15287.
8. Currie, B.J. (2005) Burkholderia pseudomallei and Burkholderia mallei: melioidosis and glanders. In Mandell, Douglas, and Bennett's Principles and Practice of Infectious Diseases, Vol. 2. Mandell, G.L., Bennett, J.E. Dolin, R. (eds). New York : Churchill Livingstone, pp. 2622 2632.
9. Das, S. Chaudhuri, K. (2003) Identification of a unique IAHP (IcmF associated homologous proteins) cluster in Vibrio cholerae and other proteobacteria through in silico analysis. In Silico Biol 3 : 287 300.
10. Dennis, J.J. Zylstra, G.J. (1998) Plasposons: modular self-cloning minitransposon derivatives for rapid genetic analysis of Gram-negative bacterial genomes. Appl Environ Microbiol 64 : 2710 2715.
11. DeShazer, D., Brett, P.J., Carlyon, R. Woods, D.E. (1997) Mutagenesis of Burkholderia pseudomallei with Tn5-OT182: isolation of motility mutants and molecular characterization of the flagellin structural gene. J Bacteriol 179 : 2116 2125.
12. DeShazer, D., Waag, D.M., Fritz, D.L. Woods, D.E. (2001) Identification of a Burkholderia mallei polysaccharide gene cluster by subtractive hybridization and demonstration that the encoded capsule is an essential virulence determinant. Microb Pathog 30 : 253 269.
13. Desvaux, M., Parham, N.J., Scott-Tucker, A. Henderson, I.R. (2004) The general secretory pathway: a general misnomer? Trends Microbiol 12 : 306 309.
14. Dudley, E.G., Thomson, N.R., Parkhill, J., Morin, N.P. Nataro, J.P. (2006) Proteomic and microarray characterization of the AggR regulon identifies a pheU pathogenicity island in enteroaggregative Escherichia coli. Mol Microbiol 61 : 1267 1282.
15. Ferster, L.N. Kurilov, V. (1982) Characteristics of the infectious process in animals susceptible and resistant to glanders (in Russian). Arkh Patol 44 : 24 30.
16. Finn, R.D., Mistry, J., Schuster-Böckler, B., Griffiths-Jones, S., Hollich, V., Lassmann, T., et al. (2006) Pfam: clans, web tools and services. Nucleic Acids Res 34 : D247 D251.
17. Folkesson, A., Lofdahl, S. Normark, S. (2002) The Salmonella enterica subspecies I specific centisome 7 genomic island encodes novel protein families present in bacteria living in close contact with eukaryotic cells. Res Microbiol 153 : 537 545.
18. Fritz, D.L., Vogel, P., Brown, D.R. Waag, D.M. (1999) The hamster model of intraperitoneal Burkholderia mallei (glanders). Vet Pathol 36 : 276 291.
19. Harley, V.S., Dance, D.A.B., Drasar, B.S. Tovey, G. (1998) Effects of Burkholderia pseudomallei and other Burkholderia species on eukarotic cells in tissue culture. Microbios 96 : 71 93.
20. Holm, M.M., Vanlerberg, S.L., Sledjeski, D.D. Lafontaine, E.R. (2003) The Hag protein of Moraxella catarrhalis strain O35E is associated with adherence to human lung and middle ear cells. Infect Immun 71 : 4977 4984.
21. Howe, C. Miller, W.R. (1947) Human glanders: report of six cases. Ann Intern Med 26 : 93 115.
22. Hunter, D.H. (1936) Saints and martyrs. Lancet 231 : 1131 1134.
23. Karlin, S. (2001) Detecting anomalous gene clusters and pathogenicity islands in diverse bacterial genomes. Trends Microbiol 9 : 335 343.
24. Khrapova, N.P., Tikhonov, N.G. Prokhvatilova, Y.V. (1998) Detection of glycoprotein of Burkholderia pseudomallei. Emerg Infect Dis 4 : 336 337.
25. Kim, H.S., Schell, M.A., Yu, Y., Ulrich, R.L., Sarria, S.H., Nierman, W.C. DeShazer, D. (2005) Bacterial genome adaptation to niches: divergence of the potential virulence genes in three Burkholderia species of different survival strategies. BMC Genomics 6 : 174, doi: 10.1186/1471-2164-1186-1174.
26. Kohler, W. (2006) Killed in action: microbiologists and clinicians as victims of their occupation. Part 4: tick-borne relapsing fever, Malta fever, glanders, SARS. Int J Med Microbiol 296 : 1 4.
27. Lehavi, O., Aizenstien, O., Katz, L.H. Hourvitz, A. (2002) Glanders-a potential biological warfare against humans and animals. Harefuah 141 : 88 91.
28. Lin, J., Michel, L.O. Zhang, Q. (2002) CmeABC functions as a multidrug efflux system in Campylobacter jejuni. Antimicrob Agents Chemother 46 : 2124 2131.
29. Lindenthal, C. Elsinghorst, E.A. (1999) Identification of a glycoprotein produced by enterotoxigenic Escherichia coli. Infect Immun 67 : 4084 4091.
30. Lopez, J., Copps, J., Wilhelmsen, C., Moore, R., Kubay, J., St-Jacques, M., et al. (2003) Characterization of experimental equine glanders. Microbes Infect 5 : 1125 1131.
31. McFadyean, J. (1904) Glanders. J Comp Pathol 17 : 295 317.
32. Miller, W.R., Pannell, L., Cravitz, L., Tanner, W.A. Rosebury, T. (1948) Studies on certain biological characteristics of Malleomyces mallei and Malleomyces pseudomallei. II. Virulence and infectivity for animals. J Bacteriol 55 : 127 135.
33. Moore, M.M., Fernandez, D.L. Thune, R.L. (2002) Cloning and characterization of Edwardsiella ictaluri proteins expressed and recognized by the channel catfish Ictalurus punctatus immune response during infection. Dis Aquat Organ 52 : 93 107.
34. Mougous, J.D., Cuff, M.E., Raunser, S., Shen, A., Zhou, M., Gifford, C.A., et al. (2006) A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312 : 1526 1530.
35. Nano, F.E., Zhang, N., Cowley, S.C., Klose, K.E., Cheung, K.K., Roberts, M.J., et al. (2004) A Francisella tularensis pathogenicity island required for intramacrophage growth. J Bacteriol 186 : 6430 6436.
36. Nelson, M., Prior, J.L., Lever, M.S., Jones, H.E., Atkins, T.P. Titball, R.W. (2004) Evaluation of lipopolysaccharide and capsular polysaccharide as subunit vaccines against experimental melioidosis. J Med Microbiol 53 : 1177 1182.
37. Nierman, W.C., DeShazer, D., Kim, H.S., Tettelin, H., Nelson, K.E., Feldblyum, T., et al. (2004) Structural flexibility in the Burkholderia mallei genome. Proc Natl Acad Sci USA 101 : 14246 14251.
38. Orr, N., Katz, D.E., Atsmon, J., Radu, P., Yavzori, M., Halperin, T., et al. (2005) Community-based safety, immunogenicity, and transmissibility study of the Shigella sonnei WRSS1 vaccine in Israeli volunteers. Infect Immun 73 : 8027 8032.
39. Piven, N.N., Smirnova, V.I., Viktorov, D.V., Kovalenko, A.A., Farber, S.M., Yarulin, R.G. Podzolkova, G.G. (1996) Immunogenicity and heterogeneity of Pseudomonas pseudomallei surface antigen 8 (in Russian). Zh Mikrobiol Epidemiol Immunobiol 4 : 75 78.
40. Potvin, E., Lehoux, D.E., Kukavica-Ibrulj, I., Richard, K.L., Sanschagrin, F., Lau, G.W. Levesque, R.C. (2003) In vivo functional genomics of Pseudomonas aeruginosa for high-throughput screening of new virulence factors and antibacterial targets. Environ Microbiol 5 : 1294 1308.
41. Pukatzki, S., Ma, A.T., Sturtevant, D., Krastins, B., Sarracino, D., Nelson, W.C., et al. (2006) Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc Natl Acad Sci USA 103 : 1528 1533.
42. Rao, P.S., Yamada, Y., Tan, Y.P. Leung, K.Y. (2004) Use of proteomics to identify novel virulence determinants that are required for Edwardsiella tarda pathogenesis. Mol Microbiol 53 : 573 586.
43. Rhodes, E.R., Tomaras, A.P., McGillivary, G., Connerly, P.L. Actis, L.A. (2005) Genetic and functional analyses of the Actinobacillus actinomycetemcomitans AfeABCD siderophore-independent iron acquisition system. Infect Immun 73 : 3758 3763.
44. Ribot, W.J. Ulrich, R.L. (2006) The animal pathogen-like type III secretion system is required for the intracellular survival of Burkholderia mallei within J774.2 macrophages. Infect Immun 74 : 4349 4353.
45. Rotz, L.D., Khan, A.S., Lillibridge, S.R., Ostroff, S.M. Hughes, J.M. (2002) Public health assessment of potential biological terrorism agents. Emerg Infect Dis 8 : 225 230.
46. Saeed, A.I., Sharov, V., White, J., Li, J., Liang, W., Bhagabati, N., et al. (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34 : 374 378.
47. Samygin, V.M., Khrapova, N.P., Spiridonov, V.A. Stepin, A.A. (2001) Antigen 8 biosynthesis during cultivation of Burkholderia pseudomallei and B. mallei (in Russian). Zh Mikrobiol Epidemiol Immunobiol 4 : 50 52.
48. Schlieker, C., Zentgraf, H., Dersch, P. Mogk, A. (2005) ClpV, a unique Hsp100/Clp member of pathogenic proteobacteria. Biol Chem 386 : 1115 1127.
49. Scholz, H.C., Joseph, M., Tomaso, H., Al Dahouk, S., Witte, A., Kinne, J., et al. (2006) Detection of the reemerging agent Burkholderia mallei in a recent outbreak of glanders in the United Arab Emirates by a newly developed fliP-based polymerase chain reaction assay. Diagn Microbiol Infect Dis 54 : 241 247.
50. Schweizer, H.P., Klassen, T. Hoang, T. (1996) Improved methods for gene analysis and expression in Pseudomonas spp. In Molecular Biology of Pseudomonads Nakazawa, T., Furukawa, K., Haas, D. Silver, S. (eds). Washington, D.C American Society for Microbiology, pp. 229 237.
51. Simon, R., Priefer, U. Puhler, A. (1983) A broad host range mobilization system for in vivo genetic engineering: tranposon mutagenesis in gram negative bacteria. Bio/Technology 1 : 784 791.
52. Snel, B., Lehmann, G., Bork, P. Huynen, M.A. (2000) STRING: a web-server to retrieve and display the repeatedly occurring neighbourhood of a gene. Nucleic Acids Res 28 : 3442 3444.
53. Srinivasan, A., Kraus, C.N., DeShazer, D., Becker, P.M., Dick, J.D., Spacek, L., et al. (2001) Glanders in a military microbiologist. N Engl J Med 354 : 256 258.
54. Stevens, J.M., Ulrich, R.L., Taylor, L.A., Wood, M.W., DeShazer, D., Stevens, M.P. Galyov, E.E. (2005a) Actin-binding proteins from Burkholderia mallei and Burkholderia thailandensis can functionally compensate for the actin-based motility defect of a Burkholderia pseudomallei bimA mutant. J Bacteriol 187 : 7857 7862.
55. Stevens, M.P., Stevens, J.M., Jeng, R.L., Taylor, L.A., Wood, M.W., Hawes, P., et al. (2005b) Identification of a bacterial factor required for actin-based motility of Burkholderia pseudomallei. Mol Microbiol 56 : 40 53.
56. Stewart, J.C. (1904) Pyaemic glanders in the human subject. Ann Surg 40 : 109 113.
57. Tatusov, R.L., Fedorova, N.D., Jackson, J.D., Jacobs, A.R., Kiryutin, B., Koonin, E.V., et al. (2003) The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4 : 41.
58. Tuanyok, A., Kim, H.S., Nierman, W.C., Yu, Y., Dunbar, J., Moore, R.A., Baker, P., Tom, M., Ling, J.M. Woods, D.E. (2005) Genome-wide expression analysis of iron regulation in Burkholderia pseudomallei and Burkholderia mallei using DNA microarrays. FEMS Microbiol Lett 252 : 327 335.
59. Tusher, V.G., Tibshirani, R. Chu, G. (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98 : 5116 5121.
60. Ulrich, R.L. DeShazer, D. (2004) Type III secretion: a virulence factor delivery system essential for the pathogenicity of Burkholderia mallei. Infect Immun 72 : 1150 1154.
61. Ulrich, R.L., DeShazer, D., Hines, H.B. Jeddeloh, J.A. (2004) Quorum sensing: a transcriptional regulatory system involved in the pathogenicity of Burkholderia mallei. Infect Immun 72 : 6589 6596.
62. Ulrich, R.L., Amemiya, K., Waag, D.M., Roy, C.J. DeShazer, D. (2005) Aerogenic vaccination with a Burkholderia mallei auxotroph protects against aerosol-initiated glanders in mice. Vaccine 23 : 1986 1992.
63. Voskuhl, G.W., Cornea, P., Bronze, M.S. Greenfield, R.A. (2003) Other bacterial diseases as a potential consequence of bioterrorism: Q fever, brucellosis, glanders, and melioidosis. J Okla State Med Assoc 96 : 214 217.
64. Waag, D.M. DeShazer, D. (2004) Glanders: new insights into an old disease. In Biological Weapons Defense: Infectious Diseases and Counterbioterrorism. Lindler, L.E., Lebeda, F.J. Korch, G.W. (eds). Totowa, NJ : Humana Press, pp. 209 237.
65. Wang, J.S. Maldonado, M.A. (2006) The ubiquitin-proteasome system and its role in inflammatory and autoimmune diseases. Cell Mol Immunol 3 : 255 261.
66. Williams, S.G., Varcoe, L.T., Attridge, S.R. Manning, P.A. (1996) Vibrio cholerae Hcp, a secreted protein coregulated with HlyA. Infect Immun 64 : 283 289.
67. Wilson, K. (1987) Preparation of genomic DNA from bacteria. In Current Protocols in Molecular Biology. Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A. Struhl, K. (eds). New York : John Wiley & Sons, pp. 2.4.1 2. 4.5.
68. Zheng, J., Tung, S.L. Leung, K.Y. (2005) Regulation of a type III and a putative secretion system in Edwardsiella tarda by EsrC is under the control of a two-component system, EsrA-EsrB. Infect Immun 73 : 4127 4137.