Analysis of the expression, secretion and translocation of the salmonella enterica type iii secretion system effector stea

PLoS ONE

Volumn 6, Issue 10, 2011, Pages

  Cardenal Muñoz, Elena ^a   Ramos Morales, Francisco ^a  

^a UNIVERSITY OF SEVILLE   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; BACTERIAL PROTEIN; BUTYRIC ACID; STEA PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BORDETELLA PERTUSSIS; CONTROLLED STUDY; CULTURE MEDIUM; EFFECTOR CELL; EPITHELIUM CELL; HOST CELL; MACROPHAGE; NONHUMAN; OSMOLALITY; PATHOGENICITY ISLAND; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN SECRETION; SALMONELLA ENTERICA; TYPE III SECRETION SYSTEM; ANIMAL; BACTERIAL SECRETION SYSTEM; BIOSYNTHESIS; CELL CULTURE; GENETICS; GENOMIC ISLAND; HUMAN; METABOLISM; MICROBIOLOGY; MOUSE; PATHOGENICITY; PHYSIOLOGY; PROTEIN TRANSPORT; VIRULENCE;

BORDETELLA PERTUSSIS; EUKARYOTA; MURINAE; NEGIBACTERIA; SALMONELLA; SALMONELLA ENTERICA;

ANIMALS; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; CELLS, CULTURED; EPITHELIAL CELLS; GENOMIC ISLANDS; HUMANS; MACROPHAGES; MICE; PROTEIN TRANSPORT; SALMONELLA ENTERICA; VIRULENCE;

EID: 80055047524     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0026930     Document Type: Article

References (89)

1. Cornelis GR, (2006) The type III secretion injectisome. Nat Rev Microbiol 4: 811-825.
2. Ghosh P, (2004) Process of protein transport by the type III secretion system. Microbiol Mol Biol Rev 68: 771-795.
3. Ibarra JA, Steele-Mortimer O, (2009) Salmonella-the ultimate insider. Salmonella virulence factors that modulate intracellular survival. Cell Microbiol 11: 1579-1586.
4. Baumler AJ, (1997) The record of horizontal gene transfer in Salmonella. Trends Microbiol 5: 318-322.
5. Jones BD, Ghori N, Falkow S, (1994) Salmonella typhimurium initiates murine infection by penetrating and destroying the specialized epithelial M cells of the Peyer's patches. J Exp Med 180: 15-23.
6. Penheiter KL, Mathur N, Giles D, Fahlen T, Jones BD, (1997) Non-invasive Salmonella typhimurium mutants are avirulent because of an inability to enter and destroy M cells of ileal Peyer's patches. Mol Microbiol 24: 697-709.
7. Kuhle V, Hensel M, (2004) Cellular microbiology of intracellular Salmonella enterica: functions of the type III secretion system encoded by Salmonella pathogenicity island 2. Cell Mol Life Sci 61: 2812-2826.
8. Brawn LC, Hayward RD, Koronakis V, (2007) Salmonella SPI1 effector SipA persists after entry and cooperates with a SPI2 effector to regulate phagosome maturation and intracellular replication. Cell Host Microbe 1: 63-75.
9. Drecktrah D, Knodler LA, Galbraith K, Steele-Mortimer O, (2005) The Salmonella SPI1 effector SopB stimulates nitric oxide production long after invasion. Cell Microbiol 7: 105-113.
10. Hernandez LD, Hueffer K, Wenk MR, Galan JE, (2004) Salmonella modulates vesicular traffic by altering phosphoinositide metabolism. Science 304: 1805-1807.
11. Lawley TD, Chan K, Thompson LJ, Kim CC, Govoni GR, et al. (2006) Genome-wide screen for Salmonella genes required for long-term systemic infection of the mouse. PLoS Pathog 2: e11.
12. Malik-Kale P, Jolly CE, Lathrop S, Winfree S, Luterbach C, et al. (2011) Salmonella- at home in the host cell. Front Microbiol 2: 125.
13. McGhie EJ, Brawn LC, Hume PJ, Humphreys D, Koronakis V, (2009) Salmonella takes control: effector-driven manipulation of the host. Curr Opin Microbiol 12: 117-124.
14. Schmitt CK, Ikeda JS, Darnell SC, Watson PR, Bispham J, et al. (2001) Absence of all components of the flagellar export and synthesis machinery differentially alters virulence of Salmonella enterica serovar Typhimurium in models of typhoid fever, survival in macrophages, tissue culture invasiveness, and calf enterocolitis. Infect Immun 69: 5619-5625.
15. Miao EA, Andersen-Nissen E, Warren SE, Aderem A, (2007) TLR5 and Ipaf: dual sensors of bacterial flagellin in the innate immune system. Semin Immunopathol 29: 275-288.
16. Ren T, Zamboni DS, Roy CR, Dietrich WF, Vance RE, (2006) Flagellin-deficient Legionella mutants evade caspase-1- and Naip5-mediated macrophage immunity. PLoS Pathog 2: e18.
17. Sun YH, Rolan HG, Tsolis RM, (2007) Injection of flagellin into the host cell cytosol by Salmonella enterica serotype Typhimurium. J Biol Chem 282: 33897-33901.
18. Bernal-Bayard J, Cardenal-Muñoz E, Ramos-Morales F, (2010) The Salmonella type III secretion effector, Salmonella leucine-rich repeat protein (SlrP), targets the human chaperone ERdj3. J Biol Chem 285: 16360-16368.
19. Bernal-Bayard J, Ramos-Morales F, (2009) Salmonella type III secretion effector SlrP is an E3 ubiquitin ligase for mammalian thioredoxin. J Biol Chem 284: 27587-27595.
20. Tsolis RM, Townsend SM, Miao EA, Miller SI, Ficht TA, et al. (1999) Identification of a putative Salmonella enterica serotype typhimurium host range factor with homology to IpaH and YopM by signature-tagged mutagenesis. Infect Immun 67: 6385-6393.
21. Jones MA, Wood MW, Mullan PB, Watson PR, Wallis TS, et al. (1998) Secreted effector proteins of Salmonella dublin act in concert to induce enteritis. Infect Immun 66: 5799-57804.
22. Mazurkiewicz P, Thomas J, Thompson JA, Liu M, Arbibe L, et al. (2008) SpvC is a Salmonella effector with phosphothreonine lyase activity on host mitogen-activated protein kinases. Mol Microbiol 67: 1371-1383.
23. Miao EA, Scherer CA, Tsolis RM, Kingsley RA, Adams LG, et al. (1999) Salmonella typhimurium leucine-rich repeat proteins are targeted to the SPI1 and SPI2 type III secretion systems. Mol Microbiol 34: 850-864.
24. Geddes K, Worley M, Niemann G, Heffron F, (2005) Identification of new secreted effectors in Salmonella enterica serovar Typhimurium. Infect Immun 73: 6260-6271.
25. Niemann GS, Brown RN, Gustin JK, Stufkens A, Shaikh-Kidwai AS, et al. (2011) Discovery of novel secreted virulence factors from Salmonella enterica serovar Typhimurium by proteomic analysis of culture supernatants. Infect Immun 79: 33-43.
26. Fink SL, Cookson BT, (2007) Pyroptosis and host cell death responses during Salmonella infection. Cell Microbiol 9: 2562-2570.
27. Hautefort I, Thompson A, Eriksson-Ygberg S, Parker ML, Lucchini S, et al. (2008) During infection of epithelial cells Salmonella enterica serovar Typhimurium undergoes a time-dependent transcriptional adaptation that results in simultaneous expression of three type 3 secretion systems. Cell Microbiol 10: 958-984.
28. Sory MP, Cornelis GR, (1994) Translocation of a hybrid YopE-adenylate cyclase from Yersinia enterocolitica into HeLa cells. Mol Microbiol 14: 583-594.
29. García-Calderón CB, Casadesús J, Ramos-Morales F, (2007) Rcs and PhoPQ regulatory overlap in the control of Salmonella enterica virulence. J Bacteriol 189: 6635-6644.
30. Lee CA, Falkow S, (1990) The ability of Salmonella to enter mammalian cells is affected by bacterial growth state. Proc Natl Acad Sci U S A 87: 4304-4308.
31. Deiwick J, Nikolaus T, Shea JE, Gleeson C, Holden DW, et al. (1998) Mutations in Salmonella pathogenicity island 2 (SPI2) genes affecting transcription of SPI1 genes and resistance to antimicrobial agents. J Bacteriol 180: 4775-4780.
32. Yu XJ, McGourty K, Liu M, Unsworth KE, Holden DW, (2010) pH sensing by intracellular Salmonella induces effector translocation. Science 328: 1040-1043.
33. Van Engelenburg SB, Palmer AE, (2010) Imaging type-III secretion reveals dynamics and spatial segregation of Salmonella effectors. Nat Methods 7: 325-330.
34. Coombes BK, Brown NF, Valdez Y, Brumell JH, Finlay BB, (2004) Expression and secretion of Salmonella pathogenicity island-2 virulence genes in response to acidification exhibit differential requirements of a functional type III secretion apparatus and SsaL. J Biol Chem 279: 49804-49815.
35. Bajaj V, Lucas RL, Hwang C, Lee CA, (1996) Co-ordinate regulation of Salmonella typhimurium invasion genes by environmental and regulatory factors is mediated by control of hilA expression. Mol Microbiol 22: 703-714.
36. Darwin KH, Miller VL, (2000) The putative invasion protein chaperone SicA acts together with InvF to activate the expression of Salmonella typhimurium virulence genes. Mol Microbiol 35: 949-960.
37. Darwin KH, Miller VL, (2001) Type III secretion chaperone-dependent regulation: activation of virulence genes by SicA and InvF in Salmonella typhimurium. EMBO J 20: 1850-1862.
38. Le Gall T, Mavris M, Martino MC, Bernardini ML, Denamur E, et al. (2005) Analysis of virulence plasmid gene expression defines three classes of effectors in the type III secretion system of Shigella flexneri. Microbiology 151: 951-962.
39. Mavris M, Page AL, Tournebize R, Demers B, Sansonetti P, et al. (2002) Regulation of transcription by the activity of the Shigella flexneri type III secretion apparatus. Mol Microbiol 43: 1543-1553.
40. Mavris M, Sansonetti PJ, Parsot C, (2002) Identification of the cis-acting site involved in activation of promoters regulated by activity of the type III secretion apparatus in Shigella flexneri. J Bacteriol 184: 6751-6759.
41. Walker KA, Miller VL, (2009) Synchronous gene expression of the Yersinia enterocolitica Ysa type III secretion system and its effectors. J Bacteriol 191: 1816-1826.
42. Cummings JH, Pomare EW, Branch WJ, Naylor CP, Macfarlane GT, (1987) Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut 28: 1221-1227.
43. Van Immerseel F, De Buck J, De Smet I, Pasmans F, Haesebrouck F, et al. (2004) Interactions of butyric acid- and acetic acid-treated Salmonella with chicken primary cecal epithelial cells in vitro. Avian Dis 48: 384-391.
44. Van Immerseel F, Fievez V, de Buck J, Pasmans F, Martel A, et al. (2004) Microencapsulated short-chain fatty acids in feed modify colonization and invasion early after infection with Salmonella enteritidis in young chickens. Poult Sci 83: 69-74.
45. Gantois I, Ducatelle R, Pasmans F, Haesebrouck F, Hautefort I, et al. (2006) Butyrate specifically down-regulates Salmonella pathogenicity island 1 gene expression. Appl Environ Microbiol 72: 946-949.
46. Gong H, Su J, Bai Y, Miao L, Kim K, et al. (2009) Characterization of the expression of Salmonella Type III secretion system factor PrgI, SipA, SipB, SopE2, SpaO, and SptP in cultures and in mice. BMC Microbiol 9: 73.
47. Bispham J, Tripathi BN, Watson PR, Wallis TS, (2001) Salmonella pathogenicity island 2 influences both systemic salmonellosis and Salmonella-induced enteritis in calves. Infect Immun 69: 367-377.
48. Brown NF, Vallance BA, Coombes BK, Valdez Y, Coburn BA, et al. (2005) Salmonella pathogenicity island 2 is expressed prior to penetrating the intestine. PLoS Pathog 1: e32.
49. Coburn B, Li Y, Owen D, Vallance BA, Finlay BB, (2005) Salmonella enterica serovar Typhimurium pathogenicity island 2 is necessary for complete virulence in a mouse model of infectious enterocolitis. Infect Immun 73: 3219-3227.
50. Coombes BK, Coburn BA, Potter AA, Gomis S, Mirakhur K, et al. (2005) Analysis of the contribution of Salmonella pathogenicity islands 1 and 2 to enteric disease progression using a novel bovine ileal loop model and a murine model of infectious enterocolitis. Infect Immun 73: 7161-7169.
51. Osborne SE, Coombes BK, (2011) Transcriptional priming of Salmonella pathogenicity island-2 precedes cellular invasion. PLoS One 6: e21648.
52. Collazo CM, Galan JE, (1996) Requirement for exported proteins in secretion through the invasion-associated type III system of Salmonella typhimurium. Infect Immun 64: 3524-3531.
53. Deane JE, Abrusci P, Johnson S, Lea SM, (2010) Timing is everything: the regulation of type III secretion. Cell Mol Life Sci 67: 1065-1075.
54. Edqvist PJ, Olsson J, Lavander M, Sundberg L, Forsberg A, et al. (2003) YscP and YscU regulate substrate specificity of the Yersinia type III secretion system. J Bacteriol 185: 2259-2266.
55. Kubori T, Galan JE, (2002) Salmonella type III secretion-associated protein InvE controls translocation of effector proteins into host cells. J Bacteriol 184: 4699-4708.
56. Lara-Tejero M, Galan JE, (2009) Salmonella enterica serovar Typhimurium pathogenicity island 1-encoded type III secretion system translocases mediate intimate attachment to nonphagocytic cells. Infect Immun 77: 2635-2642.
57. Riordan KE, Sorg JA, Berube BJ, Schneewind O, (2008) Impassable YscP substrates and their impact on the Yersinia enterocolitica type III secretion pathway. J Bacteriol 190: 6204-6216.
58. Sorg JA, Blaylock B, Schneewind O, (2006) Secretion signal recognition by YscN, the Yersinia type III secretion ATPase. Proc Natl Acad Sci U S A 103: 16490-16495.
59. Wang D, Roe AJ, McAteer S, Shipston MJ, Gally DL, (2008) Hierarchal type III secretion of translocators and effectors from Escherichia coli O157:H7 requires the carboxy terminus of SepL that binds to Tir. Mol Microbiol 69: 1499-1512.
60. Lara-Tejero M, Kato J, Wagner S, Liu X, Galan JE, (2011) A sorting platform determines the order of protein secretion in bacterial type III systems. Science 331: 1188-1191.
61. Misselwitz B, Kreibich SK, Rout S, Stecher B, Periaswamy B, et al. (2011) Salmonella enterica serovar Typhimurium binds to HeLa cells via Fim-mediated reversible adhesion and irreversible type three secretion system 1-mediated docking. Infect Immun 79: 330-341.
62. Arnold R, Brandmaier S, Kleine F, Tischler P, Heinz E, et al. (2009) Sequence-based prediction of type III secreted proteins. PLoS Pathog 5: e1000376.
63. Lower M, Schneider G, (2009) Prediction of type III secretion signals in genomes of gram-negative bacteria. PLoS One 4: e5917.
64. Samudrala R, Heffron F, McDermott JE, (2009) Accurate prediction of secreted substrates and identification of a conserved putative secretion signal for type III secretion systems. PLoS Pathog 5: e1000375.
65. Wang Y, Zhang Q, Sun MA, Guo D, (2011) High-accuracy prediction of bacterial type III secreted effectors based on position-specific amino acid composition profiles. Bioinformatics 27: 777-784.
66. Yang Y, Zhao J, Morgan RL, Ma W, Jiang T, (2010) Computational prediction of type III secreted proteins from gram-negative bacteria. BMC Bioinformatics 11 (Suppl 1): S47.
67. Crawford JA, Kaper JB, (2002) The N-terminus of enteropathogenic Escherichia coli (EPEC) Tir mediates transport across bacterial and eukaryotic cell membranes. Mol Microbiol 46: 855-868.
68. Karavolos MH, Roe AJ, Wilson M, Henderson J, Lee JJ, et al. (2005) Type III secretion of the Salmonella effector protein SopE is mediated via an N-terminal amino acid signal and not an mRNA sequence. J Bacteriol 187: 1559-1567.
69. Lloyd SA, Norman M, Rosqvist R, Wolf-Watz H, (2001) Yersinia YopE is targeted for type III secretion by N-terminal, not mRNA, signals. Mol Microbiol 39: 520-531.
70. Lloyd SA, Sjostrom M, Andersson S, Wolf-Watz H, (2002) Molecular characterization of type III secretion signals via analysis of synthetic N-terminal amino acid sequences. Mol Microbiol 43: 51-59.
71. Schechter LM, Roberts KA, Jamir Y, Alfano JR, Collmer A, (2004) Pseudomonas syringae type III secretion system targeting signals and novel effectors studied with a Cya translocation reporter. J Bacteriol 186: 543-555.
72. Kim BH, Kim HG, Kim JS, Jang JI, Park YK, (2007) Analysis of functional domains present in the N-terminus of the SipB protein. Microbiology 153: 2998-3008.
73. Russmann H, Kubori T, Sauer J, Galan JE, (2002) Molecular and functional analysis of the type III secretion signal of the Salmonella enterica InvJ protein. Mol Microbiol 46: 769-779.
74. Fields KA, Hackstadt T, (2000) Evidence for the secretion of Chlamydia trachomatis CopN by a type III secretion mechanism. Mol Microbiol 38: 1048-1060.
75. Subtil A, Delevoye C, Balana ME, Tastevin L, Perrinet S, et al. (2005) A directed screen for chlamydial proteins secreted by a type III mechanism identifies a translocated protein and numerous other new candidates. Mol Microbiol 56: 1636-1647.
76. Subtil A, Parsot C, Dautry-Varsat A, (2001) Secretion of predicted Inc proteins of Chlamydia pneumoniae by a heterologous type III machinery. Mol Microbiol 39: 792-800.
77. Lee SH, Galan JE, (2004) Salmonella type III secretion-associated chaperones confer secretion-pathway specificity. Mol Microbiol 51: 483-495.
78. Schmieger H, (1972) Phage P22-mutants with increased or decreased transduction abilities. Mol Gen Genet 119: 75-88.
79. Maloy SR, (1990) Experimental techniques in bacterial genetics Boston, MA Jones & Barlett.
80. Chan RK, Botstein D, Watanabe T, Ogata Y, (1972) Specialized transduction of tetracycline resistance by phage P22 in Salmonella typhimurium. II. Properties of a high-frequency-transducing lysate. Virology 50: 883-898.
81. Valinsky L, Nisan I, Tu X, Nisan G, Rosenshine I, et al. (2002) A host-specific virulence protein of Erwinia herbicola pv. gypsophilae is translocated into human epithelial cells by the Type III secretion system of enteropathogenic Escherichia coli. Mol Plant Pathol 3: 97-101.
82. Glaser P, Danchin A, Ladant D, Barzu O, Ullmann A, (1988) Bordetella pertussis adenylate cyclase: the gene and the protein. Tokai J Exp Clin Med 13 (Suppl): 239-252.
83. Datsenko KA, Wanner BL, (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97: 6640-6645.
84. Ellermeier CD, Janakiraman A, Slauch JM, (2002) Construction of targeted single copy lac fusions using lambda Red and FLP-mediated site-specific recombination in bacteria. Gene 290: 153-161.
85. Uzzau S, Figueroa-Bossi N, Rubino S, Bossi L, (2001) Epitope tagging of chromosomal genes in Salmonella. Proc Natl Acad Sci U S A 98: 15264-15269.
86. Miller JH, (1972) Experiments in molecular genetics Cold Spring Harbor, NY Cold Spring Harbor Laboratory Press.
87. Hanahan D, (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166: 557-580.
88. Hedegaard L, Danchin A, (1985) The cya gene region of Erwinia chrysanthemi B374: organisation and gene products. Mol Gen Genet 201: 38-42.
89. Cherepanov PP, Wackernagel W, (1995) Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158: 9-14.