Strategies for intracellular survival of Burkholderia pseudomallei

Frontiers in Microbiology

Volumn 2, Issue AUG, 2011, Pages

  Allwood, Elizabeth M ^a   Devenish, Rodney J ^a   Prescott, Mark ^a   Adler, Ben ^a   Boyce, John D ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

Adhesion; Autophagy; Burkholderia; Intracellular survival; Melioidosis; Pathogenesis; Ubiquitination

Indexed keywords

BACTERIA (MICROORGANISMS); BURKHOLDERIA; BURKHOLDERIA PSEUDOMALLEI; MAMMALIA;

EID: 84866128876     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2011.00170     Document Type: Article

References (145)

1. Aardema, H., Luijnenburg, E. M., Salm, E. F., Bijlmer, H. A., Visser, C. E., and Vant Wout, J. W. (2005). Changing epidemiology of melioidosis? A case of acute pulmonary melioidosis with fatal outcome imported from Brazil. Epidemiol. Infect. 133, 871-875.
2. Ahmed, K., Enciso, H. D., Masaki, H., Tao, M., Omori, A., Tharavichikul, P., and Nagatake, T. (1999). Attachment of Burkholderia pseudomallei to pharyngeal epithelial cells: a highly pathogenic bacteria with low attachment ability. Am. J. Trop. Med. Hyg. 60, 90-93.
3. Allwood, E. M., Logue, C. A., Hafner, G. J., Ketheesan, N., Norton, R. E., Peak, I. R., and Beacham, I. R. (2008). Evaluation of recombinant antigens for diagnosis of melioidosis. FEMS Immunol. Med. Microbiol. 54, 144-153.
4. Amann, K. J., and Pollard, T. D. (2001). Direct real-time observation of actin filament branching mediated by Arp2/3 complex using total internal reflection fluorescence microscopy. Proc. Natl. Acad. Sci. U.S.A. 98, 15009-15013.
5. Angot, A., Vergunst, A., Genin, S., and Peeters, N. (2007). Exploitation of eukaryotic ubiquitin signaling pathways by effectors translocated by bacterial type III and type IV secretion systems. PLoS Pathog. 3, e3. doi: 10.1371/journal.ppat.0030003
6. Arjcharoen, S., Wikraiphat, C., Pudla, M., Limposuwan, K., Woods, D. E., Sirisinha, S., and Utaisincharoen, P. (2007). Fate of a Burkholderia pseudomallei lipopolysaccharide mutant in the mouse macrophage cell line RAW 264.7: possible role for the O-antigenic polysaccharide moiety of lipopolysaccharide in internalization and intracellular survival. Infect. Immun. 75, 4298-4304.
7. Attree, O., and Attree, I. (2001). A second type III secretion system in Burkholderia pseudomallei: who is the real culprit? Microbiology 147, 3197-3199.
8. Bakshi, C. S., Singh, V. P., Wood, M. W., Jones, P. W., Wallis, T. S., and Galyov, E. E. (2000). Identification of SopE2, a Salmonella secreted protein which is highly homologous to SopE and involved in bacterial invasion of epithelial cells. J. Bacteriol. 182, 2341-2344.
9. Balder, R., Lipski, S., Lazarus, J. J., Grose, W., Wooten, R. M., Hogan, R. J., Woods, D. E., and Lafontaine, E. R. (2010). Identification of Burkholderia mallei and Burkholderia pseudomallei adhesins for human respiratory epithelial cells. BMC Microbiol. 10, 250. doi: 10.1186/1471-2180-10-250
10. Barth, A. L., de Abreu, E., Silva, F. A., Hoffmann,A.,Vieira,M. I.,Zavascki, A. P., Ferreira, A. G., da Cunha, L. G. J., Albano, R. M., and de Andrade Marques, E. (2007). Cystic fibrosis patient with Burkholderia pseudomallei infection acquired in Brazil. J. Clin. Microbiol. 45, 4077-4080.
11. Birmingham,C. L.,Canadien,V.,Gouin, E., Troy, E. B., Yoshimori, T., Cossart, P., Higgins, D. E., and Brumell, J. H. (2007). Listeria monocytogenes evades killing by autophagy during colonization of host cells. Autophagy 3, 442-451.
12. Boddey, J. A., Day, C. J., Flegg, C. P., Ulrich, R. L., Stephens, S. R., Beacham, I. R., Morrison, N. A., and Peak, I. R. (2007). The bacterial gene lfpA influences the potent induction of calcitonin receptor and osteoclast-related genes in Burkholderia pseudomallei-induced TRAP-positive multinucleated giant cells. Cell. Microbiol. 9, 514-531.
13. Boddey, J. A., Flegg, C. P., Day, C. J., Beacham, I. R., and Peak, I. R. (2006). Temperature-regulated microcolony formation by Burk-holderia pseudomallei requires pilA and enhances association with cultured human cells. Infect. Immun. 74, 5374-5381.
14. Boujemaa-Paterski, R., Gouin, E., Hansen, G., Samarin, S., Le Clainche, C., Didry, D., Dehoux, P., Cossart, P., Kocks, C., Carlier, M. F., and Pantaloni, D. (2001). Listeria protein ActA mimics WASP family proteins: it activates filament barbed end branching by Arp2/3 complex. Biochemistry 40, 11390-11404.
15. Breitbach, K., Rottner, K., Klocke, S., Rohde, M., Jenzora, A., Wehland, J., and Steinmetz, I. (2003). Actin-based motility of Burkholderia pseudomallei involves the Arp 2/3 complex, but not N-WASP and Ena/VASP proteins. Cell. Microbiol. 5, 385-393.
16. Brett, P. J., and Woods, D. E. (2000). Pathogenesis of and immunity to melioidosis. Acta Trop. 74, 201-210.
17. Brown, N. F., Boddey, J. A., Flegg, C. P., and Beacham, I. R. (2002). Adherence of Burkholderia pseudomallei cells to cultured human epithelial cell lines is regulated by growth temperature. Infect. Immun. 70, 974-980.
18. Burtnick, M. N., Brett, P. J., Harding, S. V., Ngugi, S. A., Ribot, W. J., Chantratita, N., Scorpio, A., Milne, T. S., Dean, R. E., Fritz, D. L., Peacock, S. J., Prior, J. L., Atkins, T. P., and Deshazer, D. (2011). The cluster 1 type VI secretion system is a major virulence determinant in Burkholderia pseudomallei. Infect. Immun. 79, 1512-1525.
19. Burtnick, M. N., Brett, P. J., Nair, V., Warawa, J. M., Woods, D. E., and Gherardini, F. C. (2008). Burkholderia pseudomallei type III secretion system mutants exhibit delayed vacuolar escape phenotypes in RAW 264.7 murine macrophages. Infect. Immun. 76, 2991-3000.
20. Burtnick, M. N., DeShazer, D., Nair, V., Gherardini, F. C., and Brett, P. J. (2010). Burkholderia mallei cluster 1 type VI secretion mutants exhibit growth and actin polymerization defects in RAW 264.7 murine macrophages. Infect. Immun. 78, 88-99.
21. Carsillo, M., Kutala, V. K., Puschel, K., Blanco, J., Kuppusamy, P., and Niewiesk, S. (2009). Nitric oxide production and nitric oxide synthase type 2 expression by cotton rat (Sigmodon hispidus) macrophages reflect the same pattern as human macrophages. Dev. Comp. Immunol. 33, 718-724.
22. Chaowagul, W., White, N. J., Dance, D. A., Wattanagoon, Y., Naigowit, P., Davis, T. M., Looareesuwan, S., and Pitakwatchara, N. (1989). Melioidosis: a major cause of community-acquired septicemia in northeastern Thailand. J. Infect. Dis. 159,890-899.
23. Chua, K. L., Chan, Y. Y., and Gan, Y. H. (2003). Flagella are virulence determinants of Burkholderia pseudomallei. Infect. Immun. 71, 1622-1629.
24. Ciborowski, P., and Gendelman, H. E. (2006). Human immunodeficiency virus-mononuclear phagocyte interactions: emerging avenues of biomarker discovery, modes of viral persistence and disease pathogenesis. Curr. HIV Res. 4, 279-291.
25. Cole, N. L., and Grose, C. (2003). Membrane fusion mediated by herpesvirus glycoproteins: the paradigm of varicella-zoster virus. Rev. Med. Virol. 13, 207-222.
26. Cossart, P. (2000). Actin-based motility of pathogens: theArp2/3 complex is a central player. Cell. Microbiol. 2, 195-205.
27. Cui, J., Yao, Q., Li, S., Ding, X., Lu, Q., Mao, H., Liu, L., Zheng, N., Chen, S., and Shao, F. (2010). Glutamine deamidation and dysfunction of ubiquitin/NEDD8 induced by a bacterial effector family. Science 329, 1215-1218.
28. Cullinane, M., Gong, L., Li, X., Lazar-Adler, N., Tra, T., Wolvetang, E., Prescott, M., Boyce, J. D., Devenish, R. J., and Adler, B. (2008). Stimulation of autophagy suppresses the intracellular survival of Burkholderia pseudomallei in mammalian cell lines. Autophagy 4, 744-753.
29. Currie, B. J., Dance, D. A., and Cheng, A. C. (2008). The global distribution of Burkholderia pseudomallei and melioidosis: an update. Trans. R. Soc. Trop. Med. Hyg. 102, S1-S4.
30. DCruze,T.,Gong,L.,Treerat,P.,Ramm, G., Boyce, J. D., Prescott, M., Adler, B., and Devenish, R. J. (2011). A role for the Burkholderia pseudomallei type three secretion system cluster 1 bpscN gene in virulence. Infect. Immun. doi: 10.1128/IAI.01351-10. [Epub ahead of print].
31. de Chastellier, C., and Thilo, L. (2006). Cholesterol depletion in Mycobacterium avium-infected macrophages overcomes the block in phagosome maturation and leads to the reversible sequestration of viable Mycobacteria in phagolysosome-derived autophagic vacuoles. Cell. Microbiol. 8, 242-256.
32. Decker, T., Stockinger, S., Karaghiosoff, M., Müller, M., and Kovarik, P. (2002). IFNs and STATs in innate immunity to microorganisms. J. Clin. Invest. 109, 1271-1277.
33. DeShazer, D., Brett, P. J., Carlyon, R., and 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.
34. Dorman, S. E., Gill,V. J., Gallin, J. I., and Holland, S. M. (1998). Burkholderia pseudomallei infection in a Puerto Rican patient with chronic granulomatous disease: case report and review of occurrences in the Americas. Clin. Infect. Dis. 26, 889-894.
35. Douglas, M. W., Lum, G., Roy, J., Fisher, D. A., Anstey, N. M., and Currie, B. J. (2004). Epidemiology of community-acquired and nosocomial bloodstream infections in tropical Australia: a 12-month prospective study. Trop. Med. Int. Health 9, 795-804.
36. Dowling, A. J., Wilkinson, P. A., Holden, M. T., Quail, M. A., Bentley, S. D., Reger, J., Waterfield, N. R., Tit-ball, R. W., and Ffrench-Constant, R. H. (2010). Genome-wide analysis reveals loci encoding anti-macrophage factors in the human pathogen Burkholderia pseudomallei K96243. PLoS ONE 5, e15693. doi: 10.1371/journal.pone.0015693
37. Dupont, N., Lacas-Gervais, S., Bertout, J., Paz, I., Freche, B., Van Nhieu, G. T., van der Goot, F. G., Sansonetti, P. J., and Lafont, F. (2009). Shigella phagocytic vacuolar membrane remnants participate in the cellular response to pathogen invasion and are regulated by autophagy. Cell Host Microbe 6, 137-149.
38. Egan, A. M., and Gordon, D. L. (1996). Burkholderia pseudomallei activates complement and is ingested but not killed by polymorphonuclear leukocytes. Infect. Immun. 64, 4952-4959
39. Egile, C., Loisel, T. P., Laurent, V., Li, R., Pantaloni, D., Sansonetti, P. J., and Carlier, M. F. (1999). Activation of the CDC42 effector N-WASP by the Shigella flexneri IcsA protein promotes actin nucleation by Arp2/3 complex and bacterial actin-based motility. J. Cell Biol. 146, 1319-1332.
40. Ekchariyawat, P., Pudla, S., Limpo-suwan, K., Arjcharoen, S., Sirisinha, S., and Utaisincharoen, P. (2005). Burkholderia pseudomallei-induced expression of suppressor of cytokine signaling 3 and cytokine-inducible src homology 2-containing protein in mouse macrophages: a possible mechanism for suppression of the response to gamma interferon stimulation. Infect. Immun. 73, 7332-7339.
41. Ekchariyawat, P., Pudla, S., Limpo-suwan, K., Arjcharoen, S., Sirisinha, S., and Utaisincharoen, P. (2007). Expression of suppressor of cytokine signaling 3 (SOCS3) and cytokine-inducible Src homology 2-containing protein (CIS) induced in Burkholderia pseudomallei-infected mouse macrophages requires bacterial internalization. Microb. Pathog. 42, 104-110.
42. Essex-Lopresti, A. E., Boddey, J. A., Thomas, R., Smith, M. P., Hartley, M. G.,Atkins,T.,Brown,N. F.,Tsang, C. H., Peak, I. R., Hill, J., Beacham, I. R., and Titball, R. W. (2005). A type IV pilin, PilA, contributes to adherence of Burkholderia pseudomallei and virulence in vivo. Infect. Immun. 73, 1260-1264.
43. Fang, F. C. (1997). Perspectives series: host/pathogen interactions. Mechanisms of nitric oxide-related antimicrobial activity. J. Clin. Invest. 99, 2818-2825.
44. Felgner, P. L., Kayala, M. A., Vigil, A., Burk, C., Nakajima-Sasaki, R., Pablo, J.,Molina,D. M.,Hirst,S.,Chew,J. S., Wang,D.,Tan,G.,Duffield,M.,Yang, R., Neel, J., Chantratita, N., Bancroft, G., Lertmemongkolchai, G., Davies, D. H., Baldi, P., Peacock, S., and Titball, R. W. (2009). A Burkholderia pseudomallei protein microarray reveals serodiagnostic and cross-reactive antigens. Proc. Natl. Acad. Sci. U.S.A. 106, 13499-13504.
45. Galyov, E. E., Brett, P. J., and DeShazer, D. (2010). Molecular insights into Burkholderia pseudomallei and Burkholderia mallei pathogenesis. Annu.Rev.Microbiol.64, 495-517.
46. Ginocchio, C. C., and Galán, J. E. (1995). Functional conservation among members of the Salmonella typhimurium InvA family of proteins. Infect. Immun. 63, 729-732.
47. Goldberg, M. B., and Theriot, J. A. (1995). Shigella flexneri surface protein IcsA is sufficient to direct actin-based motility. Proc. Natl. Acad. Sci. U.S.A. 92, 6572-6576.
48. Goley, E. D., Rodenbusch, S. E., Martin, A. C., and Welch, M. D. (2004). Critical conformational changes in the Arp2/3 complex are induced by nucleotide and nucleation promoting factor. Mol. Cell 16, 269-279.
49. Goley, E. D., and Welch, M. D. (2006). The ARP2/3 complex: an actin nucleator comes of age. Nat. Rev. Mol. Cell Biol. 7, 713-726.
50. Gong, L., Cullinane, M., Treerat, P., Ramm, G., Prescott, M., Adler, B., Boyce, J. D., and Devenish, R. J. (2011). The Burkholderia pseudomallei type III secretion system and BopA are required for evasion of LC3-associated phagocytosis. PLoS ONE 6, e17852. doi: 10.1371/journal.pone.0017852
51. Gori, A. H., Ahmed, K., Martinez, G., Masaki, H., Watanabe, K., and Nagatake, T. (1999). Mediation of attachment of Burkholderia pseudomallei to human pharyngeal epithelial cells by the asialoganglioside GM1-GM2 receptor complex. Am. J. Trop.Med.Hyg.61, 473-475.
52. Gouin, E., Egile, C., Dehoux, P., Villiers, V., Adams, J., Gertler, F., Li, R., and Cossart, P. (2004). The RickA protein of Rickettsia conorii activates the Arp2/3 complex. Nature 427, 457-461.
53. Gouin, E., Welch, M. D., and Cossart, P. (2005). Actin-based motility of intracellular pathogens. Curr. Opin. Microbiol. 8, 35-45.
54. Haase, A., Melder, A., Smith-Vaughan, H., Kemp, D., and Currie, B. (1995). RAPD analysis of isolates of Burk-holderia pseudomallei from patients with recurrent melioidosis. Epidemiol. Infect. 115, 115-121.
55. Hardt, W. D., Chen, L. M., Schuebel, K. E., Bustelo, X. R., and Galán, J. E. (1998). S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 93, 815-826.
56. Harley, V. S., Dance, D. A., Drasar, B. S., and Tovey, G. (1998a). Effects of Burkholderia pseudomallei and other Burkholderia species on eukaryotic cells in tissue culture. Microbios 96, 71-93.
57. Harley, V. S., Dance, D. A., Tovey, G., McCrossan, M. V., and Drasar, B. S. (1998b). An ultrastructural study of the phagocytosis of Burkholderia pseudomallei. Microbios 94, 35-45.
58. Harley, V. S., Dance, D. A., Tovey, G., and Drasar, B. S. (1994). Interaction of Pseudomonas pseudomallei with macrophages. Biochem. Soc. Trans. 22, 88S.
59. Hueck, C. J. (1998). Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62, 379-433.
60. Hussey, S., Travassos, L. H., and Jones, N. L. (2009). Autophagy as an emerging dimension to adaptive and innate immunity. Semin. Immunol. 21, 233-241.
61. Inglis, T. J., Robertson, T., Woods, D. E., Dutton, N., and Chang, B. J. (2003). Flagellum-mediated adhesion by Burkholderia pseudomallei precedes invasion of Acan-thamoeba astronyxis. Infect. Immun. 71, 2280-2282.
62. Jacobs, A. T., and Ignarro, L. J. (2001). Lipopolysaccharide-induced expression of interferon-beta mediates the timing of inducible nitricoxide synthase induction in RAW 264.7 macrophages. J. Biol. Chem. 276, 47950-47957.
63. Jeng, R. L., Goley, E. D., DAlessio, J. A., Chaga, O. Y., Svitkina, T. M., Borisy, G. G., Heinzen, R. A., and Welch, M. D. (2004). A Rickettsia WASP-like protein activates theArp2/3 complex and mediates actin-based motility. Cell. Microbiol. 6, 761-769.
64. Johnson, S., Roversi, P., Espina, M., Olive, A., Deane, J. E., Birket, S., Field, T., Picking, W. D., Blocker, A. J., Galyov, E. E., Picking, W. L., and Lea, S. M. (2007). Self-chaperoning of the type III secretion system needle tip proteins IpaD and BipD. J. Biol. Chem. 282, 4035-4044.
65. Jones, A. L., Beveridge, T. J., and Woods, D. E. (1996). Intracellular survival of Burkholderia pseudomallei. Infect. Immun. 64, 782-790.
66. Jones, A. L., DeShazer, D., and Woods, D. E. (1997). Identification and characterization of a two-component regulatory system involved in invasion of eukaryotic cells and heavy-metal resistance in Burkholderia pseudomallei. Infect. Immun. 65, 4972-4977.
67. Jubelin, G., Chavez, C. V., Taieb, F., Ban-field, M. J., Samba-Louaka,A., Nobe, R., Nougayrède, J. P., Zumbihl, R., Givaudan, A., Escoubas, J. M., and Oswald, E. (2009). Cycle inhibiting factors (CIFs) are a growing family of functional cyclomodulins present in invertebrate and mammal bacterial pathogens. PLoS ONE 4, e4855. doi: 10.1371/journal.pone.0004855
68. Kayath, C. A., Hussey, S., El hajjami, N., Nagra, K., Philpott, D., and Allaoui, A. (2010). Escape of intracellular Shigella from autophagy requires binding to cholesterol through the type III effector, IcsB. Microbes Infect. 12, 956-966.
69. Kespichayawattana, W., Intachote, P., Utaisincharoen, P., and Sirisinha, S. (2004). Virulent Burkholderia pseudomallei is more efficient than avirulent Burkholderia thailandensis in invasion of and adherence to cultured human epithelial cells. Microb. Pathog. 36, 287-292.
70. Kespichayawattana, W., Rattanachetkul, S.,Wanun,T.,Utaisincharoen,P.,and Sirisinha, S. (2000). Burkholderia pseudomallei induces cell fusion and actin-associated membrane protrusion: a possible mechanism for cell-to-cell spreading. Infect. Immun. 68, 5377-5384.
71. Kinzler, E. R., and Compton, T. (2005). Characterization of human cytomegalovirus glycoprotein-induced cell-cell fusion. J. Virol. 79, 7827-7837.
72. Komatsu, M., and Ichimura, Y. (2010). Selective autophagy regulates various cellular functions. Genes Cells 15, 923-933.
73. Kondo, Y., Yasui, K., Yashiro, M., Tsuge, M., Kotani, N., and Morishima, T. (2009). Multi-nucleated giant cell formation from human cord blood monocytes in vitro, in comparison with adult peripheral blood monocytes. Clin. Exp. Immunol. 158, 84-90.
74. Koponen, M. A., Zlock, D., Palmer, D. L., and Merlin, T. L. (1991). Melioidosis. Forgotten, but not gone! Arch. Intern. Med. 151, 605-608.
75. Laurent, V., Loisel, T. P., Harbeck, B., Wehman, A., Gröbe, L., Jockusch, B. M., Wehland, J., Gertler, F. B., and Carlier, M. F. (1999). Role of proteins of the Ena/VASP family in actin-based motility of Listeria monocytogenes. J. Cell Biol. 144, 1245-1258.
76. Lazar Adler, N. R., Govan, B., Cullinane, M., Harper, M., Adler, B., and Boyce, J. D. (2009). The molecular and cellular basis of pathogenesis in melioidosis: how does Burkholderia pseudomallei cause disease? FEMS Microbiol. Rev. 33, 1079-1099.
77. Le Hello, S., Currie, B. J., Godoy, D., Spratt, B. G., Mikulski, M., Lacassin, F., and Garin, B. (2005). Melioidosis in New Caledonia. Emerging Infect. Dis. 11, 1607-1609.
78. Maharjan, B., Chantratita, N., Vesaratchavest, M., Cheng, A., Wuthiekanun, V., Chierakul, W., Chaowagul, W., Day, N. P., and Peacock, S. J. (2005). Recurrent melioidosis in patients in northeast Thailand is frequently due to reinfection rather than relapse. J. Clin. Microbiol. 43, 6032-6034.
79. Makino, S., Sasakawa, C., Kamata, K., Kurata, T., and Yoshikawa, M. (1986). A genetic determinant required for continuous reinfection of adjacent cells on large plasmid in S. flexneri 2a. Cell 46, 551-555.
80. Marchès, O., Ledger, T. N., Boury, M., Ohara, M., Tu, X., Goffaux, F., Mainil, J., Rosenshine, I., Sugai, M., De Rycke, J., and Oswald, E. (2003). Enteropathogenic and enterohaemorrhagic Escherichia coli deliver a novel effector called Cif, which blocks cell cycle G2/M transition. Mol. Microbiol. 50, 1553-1567.
81. May,R. C.,Hall,M. E., Higgs,H. N., Pollard,T. D.,Chakraborty,T.,Wehland, J., Machesky, L. M., and Sechi, A. S. (1999). The Arp2/3 complex is essential for the actin-based motility of Listeria monocytogenes. Curr. Biol. 9, 759-762.
82. Monack, D. M., and Theriot, J. A. (2001). Actin-based motility is sufficient for bacterial membrane protrusion formation and host cell uptake. Cell. Microbiol. 3, 633-647.
83. Muangsombut, V., Suparak, S., Pumirat,P.,Damnin,S.,Vattanaviboon,P., Thongboonkerd,V.,and Korbsrisate, S. (2008). Inactivation of Burkholderia pseudomallei bsaQ results in decreased invasion efficiency and delayed escape of bacteria from endocytic vesicles. Arch. Microbiol. 190, 623-631.
84. Mullins, R. D., Heuser, J. A., and Pollard, T. D. (1998). The interaction of Arp2/3 complex with actin: nucleation, high affinity pointed end capping, and formation of branching networks of filaments. Proc. Natl. Acad. Sci. U.S.A. 95, 6181-6186.
85. Ngauy, V., Lemeshev, Y., Sadkowski, L., and Crawford, G. (2005). Cutaneous melioidosis in a man who was taken as a prisoner of war by the Japanese during World War II. J. Clin. Microbiol. 43, 970-972.
86. Nougayrède, J. P., Boury, M., Tasca, C., Marchès, O., Milon, A., Oswald, E., and De Rycke, J. (2001). Type III secretion-dependent cell cycle block caused in HeLa cells by enteropathogenic Escherichia coli O103. Infect. Immun. 69, 6785-6795.
87. Ogawa, M., Yoshimori, T., Suzuki, T., Sagara, H., Mizushima, N., and Sasakawa,C. (2005). Escape of intra-cellular Shigella from autophagy. Science 307, 727-731.
88. Osiriphun, Y., Wongtrakoongate, P., Sanongkiet, S., Suriyaphol, P., Thongboonkerd, V., and Tungpradabkul, S. (2009). Identification and characterization of RpoS regulon and RpoS-dependent promoters in Burkholderia pseudomallei. J. Proteome Res. 8, 3118-3131.
89. Peacock, S. J. (2006). Melioidosis. Curr. Opin. Infect. Dis. 19, 421-428.
90. Pei, J., and Grishin, N. V. (2009). The Rho GTPase inactivation domain in Vibrio cholerae MARTX toxin has a circularly permuted papain-like thiol protease fold. Proteins 77, 413-419.
91. Pelicic,V. (2008). Type IV pili: e pluribus unum? Mol. Microbiol. 68, 827-837.
92. Phewkliang,A.,Wongratanacheewin,S., and Chareonsudjai, S. (2010). Role of Burkholderia pseudomallei in the invasion, replication and induction of apoptosis in human epithelial cell lines. Southeast Asian J. Trop. Med. Public Health 41, 1164-1176.
93. Pilatz, S., Breitbach, K., Hein, N., Fehlhaber, B., Schulze, J., Brenneke, B., Eberl, L., and Steinmetz, I. (2006). Identification of Burk-holderia pseudomallei genes required for the intracellular life cycle and in vivo virulence. Infect. Immun. 74, 3576-3586.
94. Pruksachartvuthi, S., Aswapokee, N., and Thankerngpol, K. (1990). Survival of Pseudomonas pseudomallei in human phagocytes. J. Med. Microbiol. 31, 109-114.
95. Pudla,M.,Kananuruk,A.,Limposuwan, K., Sirisinha, S., and Utaisincharoen, P. (2010). Nucleotide-binding oligomerization domain-containing protein 2 regulates suppressor of cytokine signaling 3 expression in Burkholderia pseudomallei-infected mouse macrophage cell line RAW 264.7. Innate Immun. doi: 10.1177/1753425910385484. [Epub ahead of print].
96. Pukatzki, S., McAuley, S. B., and Miyata, S. T. (2009). The type VI secretion system: translocation of effectors and effector-domains. Curr. Opin. Microbiol. 12, 11-17.
97. Rainbow, L., Hart, C. A., and Winstanley, C. (2002). Distribution of type III secretion gene clusters in Burk-holderia pseudomallei, B. thailandensis and B. mallei. J. Med. Microbiol. 51, 374-384.
98. Ravikumar, B., Sarkar, S., Davies, J. E., Futter, M., Garcia-Arencibia, M., Green-Thompson, Z. W., Jimenez-Sanchez, M., Korolchuk, V. I., Lichtenberg, M., Luo, S., Massey, D. C., Menzies, F. M., Moreau, K., Narayanan, U., Renna, M., Siddiqi, F. H., Underwood, B. R., Winslow, A. R., and Rubinsztein, D. C. (2010). Regulation of mammalian autophagy in physiology and pathophysiology. Physiol. Rev. 90, 1383-1435.
99. Reckseidler, S. L., DeShazer, D., Sokol, P. A., and Woods, D. E. (2001). Detection of bacterial virulence genes by subtractive hybridization: identification of capsular polysaccharide of Burkholderia pseudomallei as a major virulence determinant. Infect. Immun. 69, 34-44.
100. Rudolph, M. G., Weise, C., Mirold, S., Hillenbrand, B., Bader, B., Witting-hofer, A., and Hardt, W. D. (1999). Biochemical analysis of SopE from Salmonella typhimurium, a highly efficient guanosine nucleotide exchange factor for RhoGTPases. J. Biol. Chem. 274, 30501-30509.
101. Samba-Louaka, A., Nougayrède, J. P., Watrin, C., Jubelin, G., Oswald, E., and Taieb, F. (2008). Bacterial cyclo-modulin Cif blocks the host cell cycle by stabilizing the cyclin-dependent kinase inhibitors p21 and p27. Cell. Microbiol. 10, 2496-2508.
102. Sanjuan, M. A., Dillon, C. P., Tait, S. W.,Moshiach,S.,Dorsey,F.,Connell, S., Komatsu, M., Tanaka, K., Cleveland, J. L., Withoff, S., and Green, D. R. (2007). Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature 450, 1253-1257.
103. Sanjuan, M. A., Milasta, S., and Green, D. R. (2009). Toll-like receptor signaling in the lysosomal pathways. Immunol. Rev. 227, 203-220.
104. Schell, M. A., Ulrich, R. L., Ribot, W. J., Brueggemann, E. E., Hines, H. B., Chen, D., Lipscomb, L., Kim, H. S., Mrazek,J.,Nierman,W. C.,and DeShazer, D. (2007). Type VI secretion is a major virulence determinant in Burkholderia mallei. Mol. Microbiol. 64, 1466-1485.
105. Schmid,D.,and Munz,C. (2007). Innate and adaptive immunity through autophagy. Immunity 27, 11-21.
106. Shabek, N., and Ciechanover, A. (2010). Degradation of ubiquitin: the fate of the cellular reaper. Cell Cycle 9, 523-530.
107. Shahnazari, S., and Brumell, J. H. (2011). Mechanisms and consequences of bacterial targeting by the autophagy pathway. Curr. Opin. Microbiol. 14, 68-75.
108. Shalom, G., Shaw, J. G., and Thomas, M. S. (2007). In vivo expression technology identifies a type VI secretion system locus in Burkholderia pseudomallei that is induced upon invasion of macrophages. Microbiology 153, 2689-2699.
109. Shanks, J., Burtnick, M. N., Brett, P. J., Waag, D. M., Spurgers, K. B., Ribot, W. J., Schell, M. A., Panchal, R. G., Gherardini, F. C., Wilkinson, K. D.,and Deshazer,D. (2009). Burk-holderia mallei tssM encodes a putative deubiquitinase that is secreted and expressed inside infected RAW 264.7 murine macrophages. Infect. Immun. 77, 1636-1648.
110. Sitthidet, C., Korbsrisate, S., Layton, A. N., Field, T. R., Stevens, M. P., and Stevens, J. M. (2011). Identification of motifs of Burkholderia pseudomallei BimA required for intracellular motility, actin binding, and actin polymerization. J. Bacteriol. 193, 1901-1910.
111. Sitthidet, C., Stevens, J. M., Chantratita, N., Currie, B. J., Peacock, S. J., Korb-srisate, S., and Stevens, M. P. (2008). Prevalence and sequence diversity of a factor required for actin-based motility in natural populations of Burkholderia species. J. Clin. Microbiol. 46, 2418-2422.
112. Stender, S., Friebel, A., Linder, S., Rohde, M., Mirold, S., and Hardt, W. D. (2000). Identification of SopE2 from Salmonella typhimurium, a conserved guanine nucleotide exchange factor for Cdc42 of the host cell. Mol. Microbiol. 36, 1206-1221.
113. Stevens, J. M., Galyov, E. E., and Stevens, M. P. (2006). Actin-dependent movement of bacterial pathogens. Nat. Rev. Microbiol. 4, 91-101.
114. Stevens, J. M., Ulrich, R. L., Taylor, L. A., Wood, M. W., Deshazer, D., Stevens, M. P., and Galyov, E. E. (2005a). Actin-binding proteins from Burk-holderia mallei and Burkholderia thailandensis can functionally compensate for the actin-based motility defect of a Burkholderia pseudomallei bimA mutant. J. Bacteriol. 187, 7857-7862.
115. Stevens, M. P., Stevens, J. M., Jeng, R. L., Taylor, L. A., Wood, M. W., Hawes, P., Monaghan, P., Welch, M. D., and Galyov, E. E. (2005b). Identification of a bacterial factor required for actin-based motility of Burkholderia pseudomallei. Mol. Microbiol. 56, 40-53.
116. Stevens,M. P.,Brown,P. J.,Wood,M. W., Wallis, T. S., and Galyov, E. E. (2001). "Cognate virulence gene clusters in Salmonella and B. pseudomallei," in Proceedings of the World Melioidosis Congress, Perth.
117. Stevens, M. P., Friebel, A., Taylor, L. A., Wood, M. W., Brown, P. J., Hardt, W. D., and Galyov, E. E. (2003). A Burkholderia pseudomallei type III secreted protein, BopE, facilitates bacterial invasion of epithelial cells and exhibits guanine nucleotide exchange factor activity. J. Bacteriol. 185, 4992-4996.
118. Stevens, M. P., and Galyov, E. E. (2004). Exploitation of host cells by Burk-holderia pseudomallei. Int. J. Med. Microbiol. 293, 549-555.
119. Stevens, M. P., Haque, A., Atkins, T., Hill, J., Wood, M. W., Easton, A., Nelson, M., Underwood-Fowler, C., Titball, R. W., Bancroft, G. J., and Galyov, E. E. (2004). Attenuated virulence and protective efficacy of a Burkholderia pseudomallei bsa type III secretion mutant in murine models of melioidosis. Microbiology 150, 2669-2676.
120. Stevens, M. P., Wood, M. W., Taylor, L. A., Monaghan, P., Hawes, P., Jones, P. W., Wallis, T. S., and Galyov, E. E. (2002). An Inv/Mxi-Spa-like type III protein secretion system in Burkholderia pseudomallei modulates intracellular behaviour of the pathogen. Mol. Microbiol. 46, 649-659.
121. Stone, R. (2007). Infectious disease. Racing to defuse a bacterial time bomb. Science 317, 1022-1024.
122. Sun, G. W., and Gan, Y. H. (2010). Unraveling type III secretion systems in the highly versatile Burkholderia pseudomallei. Trends Microbiol. 18, 561-568.
123. Sun, G. W., Lu, J., Pervaiz, S., Cao, W. P., and Gan, Y. H. (2005). Caspase-1 dependent macrophage death induced by Burkholderia pseudomallei. Cell. Microbiol. 7, 1447-1458.
124. Suparak, S., Kespichayawattana, W., Haque, A., Easton, A., Damnin, S., Lertmemongkolchai, G., Bancroft, G. J., and Korbsrisate, S. (2005). Multinucleated giant cell formation and apoptosis in infected host cells is mediated by Burk-holderia pseudomallei type III secretion protein BipB. J. Bacteriol. 187, 6556-6560.
125. Taieb, F., Nougayrède, J. P., Watrin, C., Samba-Louaka, A., and Oswald, E. (2006). Escherichia coli cyclomodulin Cif induces G2 arrest of the host cell cycle without activation of the DNA-damage checkpoint-signalling pathway. Cell. Microbiol. 8, 1910-1921.
126. Tan, K. S., Chen, Y., Lim, Y. C., Tan, G. Y., Liu, Y., Lim, Y. T., Macary, P., and Gan, Y. H. (2010). Suppression of host innate immune response by Burkholderia pseudomallei through the virulence factor TssM. J. Immunol. 184, 5160-5171.
127. Upadhyay, A., Wu, H. L., Williams, C., Field, T., Galyov, E. E., van den Elsen, J. M., and Bagby, S. (2008). The guanine-nucleotide-exchange factor BopE from Burkholderia pseudomallei adopts a compact version of the Salmonella SopE/SopE2 fold and undergoes a closed-to-open conformational change upon interaction with Cdc42. Biochem. J. 411, 485-493.
128. Utaisincharoen, P., Anuntagool, N., Arjcharoen, S., Limposuwan, K., Chaisuriya, P., and Sirisinha, S. (2004). Induction of iNOS expression and antimicrobial activity by interferon (IFN)-beta is distinct from IFN-gamma in Burkholderia pseudomallei-infected mouse macrophages. Clin. Exp. Immunol. 136, 277-283.
129. Utaisincharoen, P., Anuntagool, N., Limposuwan, K., Chaisuriya, P., and Sirisinha, S. (2003). Involvement of beta interferon in enhancing inducible nitric oxide synthase production and antimicrobial activity of Burkholderia pseudomallei-infected macrophages. Infect. Immun. 71, 3053-3057.
130. Utaisincharoen, P., Arjcharoen, S., Limposuwan, K., Tungprad-abkul, S., and Sirisinha, S. (2006). Burkholderia pseudomallei RpoS regulates multinucleated giant cell formation and inducible nitric oxide synthase expression in mouse macrophage cell line (RAW 264.7). Microb. Pathog. 40, 184-189.
131. Utaisincharoen, P., Tangthaworn-chaikul, N., Kespichayawattana, W., Anuntagool, N., Chaisuriya, P., and Sirisinha, S. (2000). Kinetic studies of the production of nitric oxide (NO) and tumour necrosis factor-alpha (TNF-alpha) in macrophages stimulated with Burkholderia pseudomallei endo-toxin. Clin. Exp. Immunol. 122, 324-329.
132. Utaisincharoen, P., Tangthaworn-chaikul, N., Kespichayawattana, W., Chaisuriya, P., and Sirisinha, S. (2001). Burkholderia pseudomallei interferes with inducible nitric oxide synthase (iNOS) production: a possible mechanism of evading macrophage killing. Microbiol. Immunol. 45, 307-313.
133. Utermöhlen, O., Herz, J., Schramm, M., and Krönke, M. (2008). Fusogenicity of membranes: the impact of acid sphingomyelinase on innate immune responses. Immunobiology 213, 307-314.
134. Warawa, J., and Woods, D. E. (2005). Type III secretion system cluster 3 is required for maximal virulence of Burkholderia pseudomallei in a hamster infection model. FEMS Microbiol. Lett. 242, 101-108.
135. Welch, M. D., Iwamatsu, A., and Mitchison, T. J. (1997). Actin polymerization is induced by Arp2/3 protein complex at the surface of Listeria monocytogenes. Nature 385, 265-269.
136. Welch, M. D., and Mullins, R. D. (2002). Cellular control of actin nucleation. Annu.Rev.CellDev.Biol. 18, 247-288.
137. Welch, M. D., Rosenblatt, J., Skoble, J., Portnoy, D. A., and Mitchison, T. J. (1998). Interaction of human Arp2/3 complex and the Listeria monocytogenes ActA protein in actin filament nucleation. Science 281, 105-108.
138. Whitlock, G. C., Estes, D. M., Young, G. M., Young, B., and Torres, A. G. (2008). Construction of a reporter system to study Burkholderia mallei type III secretion and identification of the BopA effector protein function in intracellular survival. Trans. R. Soc. Trop. Med. Hyg. 102, S127-S133.
139. Whitlock, G. C., Valbuena, G. A., Popov, V. L., Judy, B. M., Estes, D. M., and Torres, A. G. (2009). Burkholderia mallei cellular interactions in a respiratory cell model. J. Med. Microbiol. 58, 554-562.
140. Wiersinga, W. J., de Vos, A. F., de Beer, R., Wieland, C. W., Roelofs, J. J., Woods, D. E., and van der Poll, T. (2008). Inflammation patterns induced by different Burkholderia species in mice. Cell. Microbiol. 10, 81-87.
141. Winstanley, C., Hales, B. A., and Hart, C. A. (1999). Evidence for the presence in Burkholderia pseudomallei of a type III secretion system-associated gene cluster. J. Med. Microbiol. 48, 649-656.
142. Wong, K. T., Puthucheary, S. D., and Vadivelu, J. (1995). The histopathology of human melioidosis. Histopathology 26, 51-55.
143. Wood, M. W., Rosqvist, R., Mullan, P. B., Edwards, M. H., and Galyov, E. E. (1996). SopE, a secreted protein of Salmonella dublin, is translocated into the target eukaryotic cell via a sip-dependent mechanism and promotes bacterial entry. Mol. Microbiol. 22, 327-338.
144. Yao, Q., Cui, J., Zhu,Y., Wang, G., Hu, L., Long, C., Cao, R., Liu, X., Huang, N., Chen, S., Liu, L., and Shao, F. (2009). A bacterial type III effector family uses the papain-like hydrolytic activity to arrest the host cell cycle. Proc. Natl. Acad. Sci. U.S.A. 106, 3716-3721.
145. Zhang, L., Wang, Y., Picking, W. L., Picking, W. D., and De Guzman, R. N. (2006). Solution structure of monomeric BsaL, the type III secretion needle protein of Burkholderia pseudomallei. J. Mol. Biol. 359, 322-330.