The type VI secretion system spike protein VgrG5 mediates membrane fusion during intercellular spread by pseudomallei group Burkholderia species

Infection and Immunity

Volumn 82, Issue 4, 2014, Pages 1436-1444

  Toesca, Isabelle J ^a   French, Christopher T ^a   Miller, Jeff F ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; UNCLASSIFIED DRUG; VGRG5 SPIKE PROTEIN;

ALLELE; ARTICLE; BACTERIAL STRAIN; BURKHOLDERIA OKLAHOMENSIS; BURKHOLDERIA PSEUDOMALLEI; BURKHOLDERIA THAILANDENSIS; CELL MEMBRANE; CONTROLLED STUDY; HUMAN; HUMAN CELL; MEMBRANE FUSION; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; TYPE VI SECRETION SYSTEM;

ALLELES; BACTERIAL ADHESION; BACTERIAL SECRETION SYSTEMS; BURKHOLDERIA PSEUDOMALLEI; CELL DEATH; HEK293 CELLS; HUMANS; MEMBRANE FUSION;

EID: 84896484333     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01367-13     Document Type: Article

References (63)

1. Wiersinga WJ, Currie BJ, Peacock SJ. 2012. Melioidosis. N. Engl. J. Med. 367:1035-1044. http://dx.doi.org/10.1056/NEJMra1204699.
2. 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. http://dx.doi.org/10.1038/nrmicro1385.
3. Galyov EE, Brett PJ, DeShazer D. 2010. Molecular insights into Burkholderia pseudomallei and Burkholderia mallei pathogenesis. Annu. Rev. Microbiol. 64:495-517. http://dx.doi.org/10.1146/annurev.micro.112408.134030.
4. Nandi T, Ong C, Singh AP, Boddey J, Atkins T, Sarkar-Tyson M, Essex-Lopresti AE, Chua HH, Pearson T, Kreisberg JF, Nilsson C, Ariyaratne P, Ronning C, Losada L, Ruan Y, Sung W-K, Woods D, Titball RW, Beacham I, Peak I, Keim P, Nierman WC, Tan P. 2010. A genomic survey of positive selection in Burkholderia pseudomallei provides insights into the evolution of accidental virulence. PLoS Pathog. 6:e1000845. http://dx.doi.org/10.1371/journal.ppat.1000845.
5. Kim HS, Schell MA, Yu Y, Ulrich RL, Sarria SH, Nierman WC, 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. http://dx.doi.org/10.1186/1471-2164-6-174.
6. - Burkholderia pseudomallei isolates and development of a multiplex PCR procedure for rapid discrimination between the two biotypes. J. Clin. Microbiol. 37:1906-1912.
7. Lertpatanasuwan N, Sermsri K, Petkaseam A, Trakulsomboon S, Thamlikitkul V, Suputtamongkol Y. 1999. Arabinose-positive Burkholderia pseudomallei infection in humans: case report. Clin. Infect. Dis. 28: 927-928. http://dx.doi.org/10.1086/517252.
8. Morici LA, Heang J, Tate T, Didier PJ, Roy CJ. 2010. Differential susceptibility of inbred mouse strains to Burkholderia thailandensis aerosol infection. Microb. Pathog. 48:9-17. http://dx.doi.org/10.1016/j.micpath.2009.10.004.
9. Losada L, Ronning CM, DeShazer D, Woods D, Fedorova N, Kim HS, Shabalina SA, Pearson TR, Brinkac L, Tan P, Nandi T, Crabtree J, Badger J, Beckstrom-Sternberg S, Saqib M, Schutzer SE, Keim P, Nierman WC. 2010. Continuing evolution of Burkholderia mallei through genome reduction and large-scale rearrangements. Genome Biol. Evol. 2:102-116. http://dx.doi.org/10.1093/gbe/evq003.
10. Allwood EM, Devenish RJ, Prescott M, Adler B, Boyce JD. 2011. Strategies for intracellular survival of Burkholderia pseudomallei. Front. Microbiol. 2:170. http://dx.doi.org/10.3389/fmicb.2011.00170.
11. Stevens JM, Galyov EE, Stevens MP. 2006. Actin-dependent movement of bacterial pathogens. Nat. Rev. Microbiol. 4:91-101. http://dx.doi.org/10.1038/nrmicro1320.
12. French CT, Toesca IJ, Wu TH, Teslaa T, Beaty SM, Wong W, Liu M, Schröder I, Chiou P-Y, Teitell MA, Miller JF. 2011. Dissection of the Burkholderia intracellular life cycle using a photothermal nanoblade. Proc. Natl. Acad. Sci. U. S. A. 108:12095-12100. http://dx.doi.org/10.1073/pnas.1107183108.
13. Kespichayawattana W, Rattanachetkul S, Wanun T, Utaisincharoen P, Sirisinha S. 2000. Burkholderia pseudomallei induces cell fusion and actinassociated membrane protrusion: a possible mechanism for cell-to-cell spreading. Infect. Immun. 68:5377-5384. http://dx.doi.org/10.1128/IAI.68.9.5377-5384.2000.
14. Ray K, Marteyn B, Sansonetti PJ, Tang CM. 2009. Life on the inside: the intracellular lifestyle of cytosolic bacteria. Nat. Rev. Microbiol. 7:333-340. http://dx.doi.org/10.1038/nrmicro2112.
15. Schwarz S, West TE, Boyer F, Chiang WC, Carl MA, Hood RD, Rohmer L, Tolker-Nielsen T, Skerrett SJ, Mougous JD. 2010. Burkholderia type VI secretion systems have distinct roles in eukaryotic and bacterial cell interactions. PLoS Pathog. 6:e1001068. http://dx.doi.org/10.1371/journal.ppat.1001068.
16. Burtnick MN, Brett PJ, Harding SV, Ngugi SA, Ribot WJ, Chantratita N, Scorpio A, Milne TS, Dean RE, Fritz DL, Peacock SJ, Prior JL, Atkins TP, Deshazer D. 2011. The cluster 1 type VI secretion system is a major virulence determinant in Burkholderia pseudomallei. Infect. Immun. 79: 1512-1525. http://dx.doi.org/10.1128/IAI.01218-10.
17. Veesler D, Cambillau C. 2011. A common evolutionary origin for tailedbacteriophage functional modules and bacterial machineries. Microbiol. Mol. Biol. Rev. 75:423-433. http://dx.doi.org/10.1128/MMBR.00014-11.
18. Russell AB, Hood RD, Bui NK, Leroux M, Vollmer W, Mougous JD. 2011. Type VI secretion delivers bacteriolytic effectors to target cells. Nature 475:343-347. http://dx.doi.org/10.1038/nature10244.
19. Pukatzki S, Ma AT, Revel AT, Sturtevant D, Mekalanos JJ. 2007. Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin. Proc. Natl. Acad. Sci. U. S. A. 104:15508-15513. http://dx.doi.org/10.1073/pnas.0706532104.
20. Ma AT, McAuley S, Pukatzki S, Mekalanos JJ. 2009. Translocation of a Vibrio cholerae type VI secretion effector requires bacterial endocytosis by host cells. Cell Host Microbe 5:234-243. http://dx.doi.org/10.1016/j.chom.2009.02.005.
21. Basler M, Pilhofer M, Henderson GP, Jensen GJ, Mekalanos JJ. 2012. Type VI secretion requires a dynamic contractile phage tail-like structure. Nature 483:182-186. http://dx.doi.org/10.1038/nature10846.
22. Lossi NS, Manoli E, Forster A, Dajani R, Pape T, Freemont P, Filloux A. 2013. The HsiB1C1 (TssB-TssC) complex of the Pseudomonas aeruginosa type VI secretion system forms a bacteriophage tail sheathlike structure. J. Biol. Chem. 288:7536-7548. http://dx.doi.org/10.1074/jbc.M112.439273.
23. Schell MA, Ulrich RL, Ribot WJ, Brueggemann EE, Hines HB, Chen D, Lipscomb L, Kim HS, Mrazek J, Nierman WC, Deshazer D. 2007. Type VI secretion is a major virulence determinant in Burkholderia mallei. Mol. Microbiol. 64:1466-1485. http://dx.doi.org/10.1111/j.1365-2958.2007.05734.x.
24. Shalom G, Shaw JG, Thomas MS. 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. http://dx.doi.org/10.1099/mic.0.2007/006585-0.
25. Burtnick MN, DeShazer D, Nair V, Gherardini FC, Brett PJ. 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. http://dx.doi.org/10.1128/IAI.00985-09.
26. Bingle LE, Bailey CM, Pallen MJ. 2008. Type VI secretion: a beginner's guide. Curr. Opin. Microbiol. 11:3-8. http://dx.doi.org/10.1016/j.mib.2008.01.006.
27. Cascales E. 2008. The type VI secretion toolkit. EMBO Rep. 9:735-741. http://dx.doi.org/10.1038/embor.2008.131.
28. Mougous JD, Cuff ME, Raunser S, Shen A, Zhou M, Gifford CA, Goodman AL, Joachimiak G, Ordonez CL, Lory S, Walz T, Joachimiak A, Mekalanos JJ. 2006. A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312:1526-1530. http://dx.doi.org/10.1126/science.1128393.
29. Ballister ER, Lai AH, Zuckermann RN, Cheng Y, Mougous JD. 2008. In vitro self-assembly of tailorable nanotubes from a simple protein building block. Proc. Natl. Acad. Sci. U. S. A. 105:3733-3738. http://dx.doi.org/10.1073/pnas.0712247105.
30. Cascales E, Cambillau C. 2012. Structural biology of type VI secretion systems. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367:1102-1111. http://dx.doi.org/10.1098/rstb.2011.0209.
31. Pukatzki S, Ma AT, Sturtevant D, Krastins B, Sarracino D, Nelson WC, Heidelberg JF, Mekalanos JJ. 2006. Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc. Natl. Acad. Sci. U. S. A. 103:1528-1533. http://dx.doi.org/10.1073/pnas.0510322103.
32. Shneider MM, Buth SA, Ho BT, Basler M, Mekalanos JJ, Leiman PG. 2013. PAAR-repeat proteins sharpen and diversify the type VI secretion system spike. Nature 500:350-353. http://dx.doi.org/10.1038/nature12453.
33. Sheahan KL, Cordero CL, Satchell KJ. 2004. Identification of a domain within the multifunctional Vibrio cholerae RTX toxin that covalently cross-links actin. Proc. Natl. Acad. Sci. U. S. A. 101:9798-9803. http://dx.doi.org/10.1073/pnas.0401104101.
34. Suarez G, Sierra JC, Erova TE, Sha J, Horneman AJ, Chopra AK. 2010. A type VI secretion system effector protein, VgrG1, from Aeromonas hydrophila that induces host cell toxicity by ADP ribosylation of actin. J. Bacteriol. 192:155-168. http://dx.doi.org/10.1128/JB.01260-09.
35. Brett PJ, DeShazer D, Woods DE. 1998. Burkholderia thailandensis sp. nov., a Burkholderia pseudomallei-like species. Int. J. Syst. Bacteriol. 48(Part 1):317-320. http://dx.doi.org/10.1099/00207713-48-1-317.
36. Mima T, Schweizer HP. 2010. The BpeAB-OprB efflux pump of Burkholderia pseudomallei 1026b does not play a role in quorum sensing, virulence factor production, or extrusion of aminoglycosides but is a broadspectrum drug efflux system. Antimicrob. Agents Chemother. 54:3113-3120. http://dx.doi.org/10.1128/AAC.01803-09.
37. Barrett AR, Kang Y, Inamasu KS, Son MS, Vukovich JM, Hoang TT. 2008. Genetic tools for allelic replacement in Burkholderia species. Appl. Environ. Microbiol. 74:4498-4508. http://dx.doi.org/10.1128/AEM.00531-08.
38. Kumar A, Dalton C, Cortez-Cordova J, Schweizer HP. 2010. Mini-Tn7 vectors as genetic tools for single copy gene cloning in Acinetobacter baumannii. J. Microbiol. Methods 82:296-300. http://dx.doi.org/10.1016/j.mimet.2010.07.002.
39. Kovach ME, Elzer PH, Hill DS, Robertson GT, Farris MA, Roop RM, II, Peterson KM. 1995. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175-176. http://dx.doi.org/10.1016/0378-1119(95)00584-1.
40. Hayden HS, Lim R, Brittnacher MJ, Sims EH, Ramage ER, Fong C, Wu Z, Crist E, Chang J, Zhou Y, Radey M, Rohmer L, Haugen E, Gillett W, Wuthiekanun V, Peacock SJ, Kaul R, Miller SI, Manoil C, Jacobs MA. 2012. Evolution of Burkholderia pseudomallei in recurrent melioidosis. PLoS One 7:e36507. http://dx.doi.org/10.1371/journal.pone.0036507.
41. U'Ren JM, Hornstra H, Pearson T, Schupp JM, Leadem B, Georgia S, Sermswan RW, Keim P. 2007. Fine-scale genetic diversity among Burkholderia pseudomallei soil isolates in northeast Thailand. Appl. Environ. Microbiol. 73:6678-6681. http://dx.doi.org/10.1128/AEM.00986-07.
42. McCormick JB, Weaver RE, Hayes PS, Boyce JM, Feldman RA. 1977. Wound infection by an indigenous Pseudomonas pseudomallei-like organism isolated from the soil: case report and epidemiologic study. J. Infect. Dis. 135:103-107. http://dx.doi.org/10.1093/infdis/135.1.103.
43. Glass MB, Steigerwalt AG, Jordan JG, Wilkins PP, Gee JE. 2006. Burkholderia oklahomensis sp. nov., a Burkholderia pseudomallei-like species formerly known as the Oklahoma strain of Pseudomonas pseudomallei. Int. J. Syst. Evol. Microbiol. 56:2171-2176. http://dx.doi.org/10.1099/ijs.0.63991-0.
44. Deshazer D. 2007. Virulence of clinical and environmental isolates of Burkholderia oklahomensis and Burkholderia thailandensis in hamsters and mice. FEMS Microbiol. Lett. 277:64-69. http://dx.doi.org/10.1111/j.1574-6968.2007.00946.x.
45. Carvalho AP, Ventura GM, Pereira CB, Leao RS, Folescu TW, Higa L, Teixeira LM, Plotkowski MC, Merquior VL, Albano RM, Marques EA. 2007. Burkholderia cenocepacia, B. multivorans, B. ambifaria and B. vietnamiensis isolates from cystic fibrosis patients have different profiles of exoenzyme production. APMIS 115:311-318. http://dx.doi.org/10.1111/j.1600-0463.2007.apm_603.x.
46. Hofmann K, Stoffel W. 1993. TMBASE-a database of membrane spanning protein segments. Biol. Chem. Hoppe-Seyler 374:166.
47. Möller S, Croning MD, Apweiler R. 2001. Evaluation of methods for the prediction of membrane spanning regions. Bioinformatics 17:646-653. http://dx.doi.org/10.1093/bioinformatics/17.7.646.
48. Jones DT, Taylor WR, Thornton JM. 1994. A model recognition approach to the prediction of all-helical membrane protein structure and topology. Biochemistry 33:3038-3049. http://dx.doi.org/10.1021/bi00176a037.
49. Söding J. 2005. Protein homology detection by HMM-HMM comparison. Bioinformatics 21:951-960. http://dx.doi.org/10.1093/bioinformatics/bti125.
50. Zheng J, Ho B, Mekalanos JJ. 2011. Genetic analysis of anti-amoebae and anti-bacterial activities of the type VI secretion system in Vibrio cholerae. PLoS One 6:e23876. http://dx.doi.org/10.1371/journal.pone.0023876.
51. Zheng J, Leung KY. 2007. Dissection of a type VI secretion system in Edwardsiella tarda. Mol. Microbiol. 66:1192-1206. http://dx.doi.org/10.1111/j.1365-2958.2007.05993.x.
52. Pearson T, Giffard P, Beckstrom-Sternberg S, Auerbach R, Hornstra H, Tuanyok A, Price EP, Glass MB, Leadem B, Beckstrom-Sternberg JS, Allan GJ, Foster JT, Wagner DM, Okinaka RT, Sim SH, Pearson O, Wu Z, Chang J, Kaul R, Hoffmaster AR, Brettin TS, Robison RA, Mayo M, Gee JE, Tan P, Currie BJ, Keim P. 2009. Phylogeographic reconstruction of a bacterial species with high levels of lateral gene transfer. BMC Biol. 7:78. http://dx.doi.org/10.1186/1741-7007-7-78.
53. Wand ME, Muller CM, Titball RW, Michell SL. 2011. Macrophage and Galleria mellonella infection models reflect the virulence of naturally occurring isolates of B. pseudomallei, B. thailandensis and B. oklahomensis. BMC Microbiol. 11:11. http://dx.doi.org/10.1186/1471-2180-11-11.
54. Ooi WF, Ong C, Nandi T, Kreisberg JF, Chua HH, Sun G, Chen Y, Mueller C, Conejero L, Eshaghi M, Ang RM, Liu J, Sobral BW, Korbsrisate S, Gan YH, Titball RW, Bancroft GJ, Valade E, Tan P. 2013. The condition-dependent transcriptional landscape of Burkholderia pseudomallei. PLoS Genet. 9:e1003795. http://dx.doi.org/10.1371/journal.pgen.1003795.
55. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402. http://dx.doi.org/10.1093/nar/25.17.3389.
56. Ashkenazi A, Shai Y. 2011. Insights into the mechanism of HIV-1 envelope induced membrane fusion as revealed by its inhibitory peptides. Eur. Biophys. J. 40:349-357. http://dx.doi.org/10.1007/s00249-010-0666-z.
57. Schwarz S, Singh P, Robertson JD, Le Roux M, Skerrett SJ, Goodlett DR, West TE, Mougous JD. 2014. VgrG-5 is a Burkholderia thailandensis type VI secretion system-exported protein required for multinucleated giant cell formation and virulence. Infect. Immun. 82:1445-1452. http://dx.doi.org/10.1128/IAI.01368-13.
58. Marsden HR, Tomatsu I, Kros A. 2011. Model systems for membrane fusion. Chem. Soc. Rev. 40:1572-1585. http://dx.doi.org/10.1039/c0cs00115e.
59. Martens S, McMahon HT. 2008. Mechanisms of membrane fusion: disparate players and common principles. Nat. Rev. Mol. Cell Biol. 9:543-556. http://dx.doi.org/10.1038/nrm2417.
60. Backovic M, Jardetzky TS. 2011. Class III viral membrane fusion proteins. Adv. Exp. Med. Biol. 714:91-101. http://dx.doi.org/10.1007/978-94-007-0782-5_3.
61. Suparak S, Muangsombut V, Riyapa D, Stevens JM, Stevens MP, Lertmemongkolchai G, Korbsrisate S. 2011. Burkholderia pseudomalleiinduced cell fusion in U937 macrophages can be inhibited by monoclonal antibodies against host cell surface molecules. Microbes Infect. 13:1006-1011. http://dx.doi.org/10.1016/j.micinf.2011.06.007.
62. Jones DT, Taylor WR, Thornton JM. 1992. The rapid generation of mutation data matrices from protein sequences. Comput. Appl. Biosci. 8:275-282.
63. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28:2731-2739. http://dx.doi.org/10.1093/molbev/msr121.