Structural basis for type VI secretion effector recognition by a cognate immunity protein

PLoS Pathogens

Volumn 8, Issue 4, 2012, Pages

  Li, Mo ^a   Le Trong, Isolde ^a   Carl, Mike A ^a   Larson, Eric T ^b   Chou, Seemay ^a   de Leon, Justin A ^a   Dove, Simon L ^c   Stenkamp, Ronald E ^a,b   Mougous, Joseph D ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CELL PROTEIN; TOXIN ANTIBODY; TYPE VI SECRETION EXPORTED 2 PROTEIN; TYPE VI SECRETION IMMUNITY 2 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; BACTERIOSTASIS; CELL DEATH; CIRCULAR DICHROISM; CONTROLLED STUDY; CYTOPLASM; DIMERIZATION; ESCHERICHIA COLI; GENETIC SCREENING; IMMUNITY; MUTAGENESIS; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; PSEUDOMONAS AERUGINOSA; TYPE VI SECRETION SYSTEM; X RAY CRYSTALLOGRAPHY; BACTERIAL SECRETION SYSTEM; CHEMISTRY; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN MULTIMERIZATION; PROTEIN QUATERNARY STRUCTURE; PROTEIN TERTIARY STRUCTURE;

NEGIBACTERIA; PSEUDOMONAS AERUGINOSA;

BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; CRYSTALLOGRAPHY, X-RAY; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; PSEUDOMONAS AERUGINOSA;

EID: 84861170138     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002613     Document Type: Article

References (52)

1. Cascales E, (2008) The type VI secretion toolkit. EMBO Rep 9: 735-741.
2. Schwarz S, Hood RD, Mougous JD, (2010) What is type VI secretion doing in all those bugs? Trends Microbiol 18: 531-537.
3. Alvarez-Martinez CE, Christie PJ, (2009) Biological diversity of prokaryotic type IV secretion systems. Microbiol Mol Biol Rev 73: 775-808.
4. Cornelis GR, (2006) The type III secretion injectisome. Nat Rev Microbiol 4: 811-825.
5. Boyer F, Fichant G, Berthod J, Vandenbrouck Y, Attree I, (2009) Dissecting the bacterial type VI secretion system by a genome wide in silico analysis: what can be learned from available microbial genomic resources? BMC Genomics 10: 104.
6. Leiman PG, Basler M, Ramagopal UA, Bonanno JB, Sauder JM, et al. (2009) Type VI secretion apparatus and phage tail-associated protein complexes share a common evolutionary origin. Proc Natl Acad Sci U S A 106: 4154-4159.
7. Mougous JD, Cuff ME, Raunser S, Shen A, Zhou M, et al. (2006) A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312: 1526-1530.
8. Veesler D, Cambillau C, (2011) A common evolutionary origin for tailed-bacteriophage functional modules and bacterial machineries. Microbiol Mol Biol Rev 75: 423-433, first page of table of contents.
9. Kanamaru S, (2009) Structural similarity of tailed phages and pathogenic bacterial secretion systems. Proc Natl Acad Sci U S A 106: 4067-4068.
10. Bingle LE, Bailey CM, Pallen MJ, (2008) Type VI secretion: a beginner's guide. Curr Opin Microbiol 11: 3-8.
11. Aschtgen MS, Bernard CS, De Bentzmann S, Lloubes R, Cascales E, (2008) SciN is an outer membrane lipoprotein required for Type VI secretion in enteroaggregative Escherichia coli. J Bacteriol 190: 7523-7531.
12. Weber B, Hasic M, Chen C, Wai SN, Milton DL, (2009) Type VI secretion modulates quorum sensing and stress response in Vibrio anguillarum. Environ Microbiol 11: 3018-3028.
13. Hood RD, Singh P, Hsu F, Guvener T, Carl MA, et al. (2010) A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 7: 25-37.
14. Russell AB, Hood RD, Bui NK, LeRoux M, Vollmer W, et al. (2011) Type VI secretion delivers bacteriolytic effectors to target cells. Nature 475: 343-347.
15. Stebbins CE, Galan JE, (2003) Priming virulence factors for delivery into the host. Nat Rev Mol Cell Biol 4: 738-743.
16. Aoki SK, Pamma R, Hernday AD, Bickham JE, Braaten BA, et al. (2005) Contact-dependent inhibition of growth in Escherichia coli. Science 309: 1245-1248.
17. Cascales E, Buchanan SK, Duche D, Kleanthous C, Lloubes R, et al. (2007) Colicin biology. Microbiol Mol Biol Rev 71: 158-229.
18. Hayes CS, Aoki SK, Low DA, (2010) Bacterial contact-dependent delivery systems. Annu Rev Genet 44: 71-90.
19. Yamaguchi Y, Inouye M, (2011) Regulation of growth and death in Escherichia coli by toxin-antitoxin systems. Nat Rev Microbiol 9: 779-790.
20. Gerdes K, Christensen SK, Lobner-Olesen A, (2005) Prokaryotic toxin-antitoxin stress response loci. Nat Rev Microbiol 3: 371-382.
21. Maisonneuve E, Shakespeare LJ, Jorgensen MG, Gerdes K, (2011) Bacterial persistence by RNA endonucleases. Proc Natl Acad Sci U S A 108: 13206-13211.
22. Yamaguchi Y, Inouye M, (2009) mRNA interferases, sequence-specific endoribonucleases from the toxin-antitoxin systems. Prog Mol Biol Transl Sci 85: 467-500.
23. Ramage HR, Connolly LE, Cox JS, (2009) Comprehensive functional analysis of Mycobacterium tuberculosis toxin-antitoxin systems: implications for pathogenesis, stress responses, and evolution. PLoS Genet 5: e1000767.
24. Dove SL, Hochschild A, (2004) A bacterial two-hybrid system based on transcription activation. Methods Mol Biol 261: 231-246.
25. Vallet-Gely I, Donovan KE, Fang R, Joung JK, Dove SL, (2005) Repression of phase-variable cup gene expression by H-NS-like proteins in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 102: 11082-11087.
26. Parsot C, Hamiaux C, Page AL, (2003) The various and varying roles of specific chaperones in type III secretion systems. Curr Opin Microbiol 6: 7-14.
27. Aizenman E, Engelberg-Kulka H, Glaser G, (1996) An Escherichia coli chromosomal "addiction module" regulated by guanosine [corrected] 3′,5′-bispyrophosphate: a model for programmed bacterial cell death. Proc Natl Acad Sci U S A 93: 6059-6063.
28. Hendrickson WA, (1991) Determination of macromolecular structures from anomalous diffraction of synchrotron radiation. Science 254: 51-58.
29. Kleanthous C, Walker D, (2001) Immunity proteins: enzyme inhibitors that avoid the active site. Trends Biochem Sci 26: 624-631.
30. Blower TR, Salmond GP, Luisi BF, (2011) Balancing at survival's edge: the structure and adaptive benefits of prokaryotic toxin-antitoxin partners. Curr Opin Struct Biol 21: 109-118.
31. Goodman AL, Kulasekara B, Rietsch A, Boyd D, Smith RS, et al. (2004) A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa. Dev Cell 7: 745-754.
32. Wang J, Gossing M, Fang P, Zimmermann J, Li X, et al. (2011) Epsin N-terminal homology domains bind on opposite sides of two SNAREs. Proc Natl Acad Sci U S A 108: 12277-12282.
33. Silverman JM, Austin LS, Hsu F, Hicks KG, Hood RD, et al. (2011) Separate inputs modulate phosphorylation-dependent and-independent type VI secretion activation. Mol Microbiol 82: 1277-1290.
34. Hong W, (2005) SNAREs and traffic. Biochim Biophys Acta 1744: 493-517.
35. Pedersen K, Christensen SK, Gerdes K, (2002) Rapid induction and reversal of a bacteriostatic condition by controlled expression of toxins and antitoxins. Mol Microbiol 45: 501-510.
36. Kelley LA, Sternberg MJ, (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4: 363-371.
37. Kamada K, Hanaoka F, (2005) Conformational change in the catalytic site of the ribonuclease YoeB toxin by YefM antitoxin. Mol Cell 19: 497-509.
38. Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P, et al. (2000) Complete genome sequence of Pseudomonas aeruginosa PA01, an opportunistic pathogen. Nature 406: 959-964.
39. Kunkel TA, (1985) Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc Natl Acad Sci U S A 82: 488-492.
40. Rietsch A, Vallet-Gely I, Dove SL, Mekalanos JJ, (2005) ExsE, a secreted regulator of type III secretion genes in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 102: 8006-8011.
41. Vance RE, Rietsch A, Mekalanos JJ, (2005) Role of the type III secreted exoenzymes S, T, and Y in systemic spread of Pseudomonas aeruginosa PAO1 in vivo. Infect Immun 73: 1706-1713.
42. Otwinowski Z, Minor W, (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol 276: 307-329.
43. Terwilliger TC, Berendzen J, (1999) Automated MAD and MIR structure solution. Acta Crystallogr D Biol Crystallogr 55: 849-861.
44. Murshudov GN, Vagin AA, Dodson EJ, (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255.
45. Project CC, (1994) The CCP4 Suite: Programs for Protein Crystallography. Acta Crystallogr D Biol Crystallogr 50: 760-763.
46. McRee DE, (1999) XtalView/Xfit-A versatile program for manipulating atomic coordinates and electron density. J Struct Biol 125: 156-165.
47. Schrodinger LLC, (2010) The PyMOL Molecular Graphics System, Version 1.3r1.
48. Potterton E, McNicholas S, Krissinel E, Cowtan K, Noble M, (2002) The CCP4 molecular-graphics project. Acta Crystallogr D Biol Crystallogr 58: 1955-1957.
49. Davis IW, Leaver-Fay A, Chen VB, Block JN, Kapral GJ, et al. (2007) MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res 35: W375-383.
50. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, et al. (2000) The Protein Data Bank. Nucleic Acids Res 28: 235-242.
51. Dove SL, Hochschild A, (1998) Conversion of the omega subunit of Escherichia coli RNA polymerase into a transcriptional activator or an activation target. Genes Dev 12: 745-754.
52. Whiteley M, Lee KM, Greenberg EP, (1999) Identification of genes controlled by quorum sensing in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 96: 13904-13909.