The Burkholderia pseudomallei type III secretion system and BopA are required for evasion of LC3-associated phagocytosis

PLoS ONE

Volumn 6, Issue 3, 2011, Pages

  Gong, Lan ^a   Cullinane, Meabh ^a,b   Treerat, Puthayalai ^a   Ramm, Georg ^a   Prescott, Mark ^a   Adler, Ben ^a   Boyce, John D ^a   Devenish, Rodney J ^a  

^a MONASH UNIVERSITY   (Australia)

^b LA TROBE UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BIOLOGICAL MARKER; CARRIER PROTEIN; CELL MARKER; LIGHT CHAIN 3 PROTEIN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; PROTEIN BIPD; PROTEIN BOPA; UNCLASSIFIED DRUG; LAMP1 PROTEIN, MOUSE; LYSOSOME ASSOCIATED MEMBRANE PROTEIN; MAP1LC3 PROTEIN, MOUSE; MICROTUBULE ASSOCIATED PROTEIN;

ARTICLE; AUTOPHAGY; BACTERIAL GENE; BACTERIAL TRANSLOCATION; BACTERICIDAL ACTIVITY; BURKHOLDERIA PSEUDOMALLEI; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSOL; ELECTRON MICROSCOPY; HOST RESISTANCE; IMMUNE EVASION; MACROPHAGE; MELIOIDOSIS; NONHUMAN; PHAGOSOME; PROTEIN LOCALIZATION; TYPE III SECRETION SYSTEM; TYPE III SECRETION SYSTEM CLUSTER 3; ANIMAL; CELL LINE; CELL VACUOLE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; INTRACELLULAR SPACE; METABOLISM; MICROBIOLOGY; MOUSE; MUTATION; PHAGOCYTOSIS; PROTEIN TRANSPORT; SECRETION; ULTRASTRUCTURE;

BURKHOLDERIA PSEUDOMALLEI;

ANIMALS; AUTOPHAGY; BACTERIAL PROTEINS; BURKHOLDERIA PSEUDOMALLEI; CELL LINE; CYTOSOL; GENE EXPRESSION REGULATION, BACTERIAL; IMMUNE EVASION; INTRACELLULAR SPACE; LYSOSOME-ASSOCIATED MEMBRANE GLYCOPROTEINS; MICE; MICROTUBULE-ASSOCIATED PROTEINS; MUTATION; PHAGOCYTOSIS; PHAGOSOMES; PROTEIN TRANSPORT; VACUOLES;

EID: 79952613917     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0017852     Document Type: Article

References (50)

1. Lazar Adler NR, Govan B, Cullinane M, Harper M, Adler B, et al. (2009) The molecular and cellular basis of pathogenesis in melioidosis: how does Burkholderia pseudomallei cause disease? FEMS Microbiol Rev 33: 1079-1099.
2. White NJ, (2003) Melioidosis. Lancet 361: 1715-1722.
3. Cheng AC, Currie BJ, (2005) Melioidosis: epidemiology, pathophysiology, and management. Clin Microbiol Rev 18: 383-416.
4. Cheng AC, Hanna JN, Norton R, Hills SL, Davis J, et al. (2003) Melioidosis in northern Australia, 2001-02. Commun Dis Intell 27: 272-277.
5. Galyov EE, Brett PJ, DeShazer D, (2010) Molecular insights into Burkholderia pseudomallei and Burkholderia mallei pathogenesis. Annu Rev Microbiol 64: 495-517.
6. Wiersinga WJ, van der Poll T, White NJ, Day NP, Peacock SJ, (2006) Melioidosis: insights into the pathogenicity of Burkholderia pseudomallei. Nat Rev Microbiol 4: 272-282.
7. Pruksachartvuthi S, Aswapokee N, Thankerngpol K, (1990) Survival of Pseudomonas pseudomallei in human phagocytes. J Med Microbiol 31: 109-114.
8. Jones AL, Beveridge TJ, Woods DE, (1996) Intracellular survival of Burkholderia pseudomallei. Infect Immun 64: 782-790.
9. Stevens MP, Wood MW, Taylor LA, Monaghan P, Hawes P, et al. (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.
10. Kespichayawattana W, Rattanachetkul S, Wanun T, Utaisincharoen P, 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.
11. Harley VS, Dance DA, Drasar BS, Tovey G, (1998) Effects of Burkholderia pseudomallei and other Burkholderia species on eukaryotic cells in tissue culture. Microbios 96: 71-93.
12. Mehrpour M, Esclatine A, Beau I, Codogno P, (2010) Overview of macroautophagy regulation in mammalian cells. Cell Res 20: 748-762.
13. Mizushima N, (2009) Physiological functions of autophagy. Curr Top Microbiol Immunol 335: 71-84.
14. Levine B, (2005) Eating oneself and uninvited guests: autophagy-related pathways in cellular defense. Cell 120: 159-162.
15. Deretic V, (2010) Autophagy in infection. Curr Opin Cell Biol 22: 252-262.
16. Deretic V, Levine B, (2009) Autophagy, immunity, and microbial adaptations. Cell Host Microbe 5: 527-549.
17. Nakagawa I, Amano A, Mizushima N, Yamamoto A, Yamaguchi H, et al. (2004) Autophagy defends cells against invading group A Streptococcus. Science 306: 1037-1040.
18. Gutierrez MG, Master SS, Singh SB, Taylor GA, Colombo MI, et al. (2004) Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119: 753-766.
19. Yoshikawa Y, Ogawa M, Hain T, Yoshida M, Fukumatsu M, et al. (2009) Listeria monocytogenes ActA-mediated escape from autophagic recognition. Nat Cell Biol 11: 1233-1240.
20. Ogawa M, Sasakawa C, (2006) Bacterial evasion of the autophagic defense system. Curr Opin Microbiol 9: 62-68.
21. Ogawa M, Yoshimori T, Suzuki T, Sagara H, Mizushima N, et al. (2005) Escape of intracellular Shigella from autophagy. Science 307: 727-731.
22. Birmingham CL, Canadien V, Gouin E, Troy EB, Yoshimori T, et al. (2007) Listeria monocytogenes evades killing by autophagy during colonization of host cells. Autophagy 3: 442-451.
23. Dorn BR, Dunn WA Jr, Progulske-Fox A, (2002) Bacterial interactions with the autophagic pathway. Cell Microbiol 4: 1-10.
24. Lerena MC, Vazquez CL, Colombo MI, (2010) Bacterial pathogens and the autophagic response. Cell Microbiol 12: 10-18.
25. Amer AO, Swanson MS, (2005) Autophagy is an immediate macrophage response to Legionella pneumophila. Cell Microbiol 7: 765-778.
26. Celli J, de Chastellier C, Franchini DM, Pizarro-Cerda J, Moreno E, et al. (2003) Brucella evades macrophage killing via VirB-dependent sustained interactions with the endoplasmic reticulum. J Exp Med 198: 545-556.
27. Gutierrez MG, Vazquez CL, Munafo DB, Zoppino FC, Beron W, et al. (2005) Autophagy induction favours the generation and maturation of the Coxiella-replicative vacuoles. Cell Microbiol 7: 981-993.
28. Rodrigues PH, Belanger M, Dunn W Jr, Progulske-Fox A, (2008) Porphyromonas gingivalis and the autophagic pathway: an innate immune interaction? Front Biosci 13: 178-187.
29. Schnaith A, Kashkar H, Leggio SA, Addicks K, Kronke M, et al. (2007) Staphylococcus aureus subvert autophagy for induction of caspase-independent host cell death. J Biol Chem 282: 2695-2706.
30. Cullinane M, Gong L, Li X, Lazar-Adler N, Tra T, et al. (2008) Stimulation of autophagy suppresses the intracellular survival of Burkholderia pseudomallei in mammalian cell lines. Autophagy 4: 744-753.
31. Sanjuan MA, Dillon CP, Tait SW, Moshiach S, Dorsey F, et al. (2007) Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature 450: 1253-1257.
32. Sanjuan MA, Milasta S, Green DR, (2009) Toll-like receptor signaling in the lysosomal pathways. Immunol Rev 227: 203-220.
33. Holden MT, Titball RW, Peacock SJ, Cerdeno-Tarraga AM, Atkins T, et al. (2004) Genomic plasticity of the causative agent of melioidosis, Burkholderia pseudomallei. Proc Natl Acad Sci U S A 101: 14240-14245.
34. Milton DL, O'Toole R, Horstedt P, Wolf-Watz H, (1996) Flagellin A is essential for the virulence of Vibrio anguillarum. J Bacteriol 178: 1310-1319.
35. de Lorenzo V, Herrero M, Jakubzik U, Timmis KN, (1990) Mini-Tn5 transposon derivatives for insertion mutagenesis, promoter probing, and chromosomal insertion of cloned DNA in gram-negative eubacteria. J Bacteriol 172: 6568-6572.
36. Suzuki T, Franchi L, Toma C, Ashida H, Ogawa M, et al. (2007) Differential regulation of caspase-1 activation, pyroptosis, and autophagy via Ipaf and ASC in Shigella-infected macrophages. PLoS Pathog 3: e111.
37. Johnson S, Roversi P, Espina M, Olive A, Deane JE, et al. (2007) Self-chaperoning of the type III secretion system needle tip proteins IpaD and BipD. J Biol Chem 282: 4035-4044.
38. Stevens MP, Haque A, Atkins T, Hill J, Wood MW, et al. (2004) Attenuated virulence and protective efficacy of a Burkholderia pseudomallei bsa type III secretion mutant in murine models of melioidosis. Microbiology 150: 2669-2676.
39. Huynh KK, Eskelinen EL, Scott CC, Malevanets A, Saftig P, et al. (2007) LAMP proteins are required for fusion of lysosomes with phagosomes. EMBO J 26: 313-324.
40. Eskelinen EL, (2006) Roles of LAMP-1 and LAMP-2 in lysosome biogenesis and autophagy. Mol Aspects Med 27: 495-502.
41. Wiersinga WJ, Wieland CW, Dessing MC, Chantratita N, Cheng AC, et al. (2007) Toll-like receptor 2 impairs host defense in gram-negative sepsis caused by Burkholderia pseudomallei (Melioidosis). PLoS Med 4: e248.
42. Huang J, Canadien V, Lam GY, Steinberg BE, Dinauer MC, et al. (2009) Activation of antibacterial autophagy by NADPH oxidases. Proc Natl Acad Sci U S A 106: 6226-6231.
43. Espina M, Ausar SF, Middaugh CR, Baxter MA, Picking WD, et al. (2007) Conformational stability and differential structural analysis of LcrV, PcrV, BipD, and SipD from type III secretion systems. Protein Sci 16: 704-714.
44. Burtnick MN, Brett PJ, Nair V, Warawa JM, Woods DE, et al. (2008) Burkholderia pseudomallei type III secretion system mutants exhibit delayed vacuolar escape phenotypes in RAW 264.7 murine macrophages. Infect Immun 76: 2991-3000.
45. Pei J, Grishin NV, (2009) The Rho GTPase inactivation domain in Vibrio cholerae MARTX toxin has a circularly permuted papain-like thiol protease fold. Proteins 77: 413-419.
46. Kayath CA, Hussey S, El hajjami N, Nagra K, Philpott D, et al. (2010) Escape of intracellular Shigella from autophagy requires binding to cholesterol through the type III effector, IcsB. Microbes Infect 12: 956-966.
47. de Chastellier C, 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.
48. Yoshimori T, Amano A, (2009) Group a Streptococcus: a loser in the battle with autophagy. Curr Top Microbiol Immunol 335: 217-226.
49. Collins CA, Brown EJ, (2010) Cytosol as battleground: ubiquitin as a weapon for both host and pathogen. Trends Cell Biol 20: 205-213.
50. Tan KS, Chen Y, Lim YC, Tan GY, Liu Y, et al. (2010) Suppression of host innate immune response by Burkholderia pseudomallei through the virulence factor TssM. J Immunol 184: 5160-5171.