The type VI secretion system encoded in salmonella pathogenicity island 19 is required for Salmonella enterica serotype gallinarum survival within infected macrophages

Infection and Immunity

Volumn 81, Issue 4, 2013, Pages 1207-1220

  Blondel, Carlos J ^a   Jiménez, Juan C ^a   Leiva, Lorenzo E ^a   Álvarez, Sergio A ^a   Pinto, Bernardo I ^a   Contreras, Francisca ^a   Pezoa, David ^a   Santiviago, Carlos A ^a   Contreras, Inés ^a  

^a UNIVERSITY OF CHILE   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; GREEN FLUORESCENT PROTEIN; HCP1 PROTEIN; HCP2 PROTEIN; PROTEIN; SPI 19 T6SS PROTEIN; UNCLASSIFIED DRUG; VGRG PROTEIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; BACTERIAL GROWTH; BACTERIAL INFECTION; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BACTERIUM CULTURE; BIRD; CELL DEATH; CONTROLLED STUDY; CYTOTOXICITY; DELETION MUTANT; HOST CELL; HOST PARASITE INTERACTION; MACROPHAGE; MOLECULAR MECHANICS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; SALMONELLA GALLINARUM; SEROTYPE;

ANIMALS; BACTERIAL SECRETION SYSTEMS; CELL LINE; CELL SURVIVAL; CHICKENS; GENE DELETION; GENOMIC ISLANDS; MACROPHAGES; MEMBRANE TRANSPORT PROTEINS; MICE; MICROBIAL VIABILITY; SALMONELLA ENTERICA; TIME FACTORS; VIRULENCE FACTORS;

EID: 84875532385     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01165-12     Document Type: Article

References (71)

1. Grimont PD, Weill FX. 2007. Antigenic formulae of the Salmonella serovars, 9th ed. WHO Collaborating Centre for Reference and Research on Salmonella, Institute Pasteur, Paris, France.
2. Shivaprasad HL. 2000. Fowl typhoid and pullorum disease. Rev. Sci. Tech. 19:405-424.
3. Barrow PA, Freitas Neto OC. 2011. Pullorum disease and fowl typhoid-new thoughts on old diseases: a review. Avian Pathol. 40:1-13.
4. Haraga A, Ohlson MB, Miller SI. 2008. Salmonellae interplay with host cells. Nat. Rev. Microbiol. 6:53-66.
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 learnt from available microbial genomic resources? BMC Genomics 10:104. doi:10.1186/1471-2164-10-104.
6. Pukatzki S, McAuley SB, Miyata ST. 2009. The type VI secretion system: translocation of effectors and effector-domains. Curr. Opin. Microbiol. 12:11-17.
7. Blondel CJ, Jimenez JC, Contreras I, Santiviago CA. 2009. Comparative genomic analysis uncovers 3 novel loci encoding type six secretion systems differentially distributed in Salmonella serotypes. BMC Genomics 10:354. doi:10.1186/1471-2164-10-354.
8. Fookes M, Schroeder GN, Langridge GC, Blondel CJ, Mammina C, Connor TR, Seth-Smith H, Vernikos GS, Robinson KS, Sanders M, Petty NK, Kingsley RA, Baumler AJ, Nuccio SP, Contreras I, Santiviago CA, Maskell D, Barrow P, Humphrey T, Nastasi A, Roberts M, Frankel G, Parkhill J, Dougan G, Thomson NR. 2011. Salmonella bongori provides insights into the evolution of the salmonellae. PLoS Pathog. 7:e1002191. doi:10.1371/journal.ppat.1002191.
9. Blondel CJ, Yang HJ, Castro B, Chiang S, Toro CS, Zaldivar M, Contreras I, Andrews-Polymenis HL, Santiviago CA. 2010. Contribution of the type VI secretion system encoded in SPI-19 to chicken colonization by Salmonella enterica serotypes Gallinarum and Enteritidis. PLoS One 5:e11724. doi:10.1371/journal.pone.0011724.
10. Thomson NR, Clayton DJ, Windhorst D, Vernikos G, Davidson S, Churcher C, Quail MA, Stevens M, Jones MA, Watson M, Barron A, Layton A, Pickard D, Kingsley RA, Bignell A, Clark L, Harris B, Ormond D, Abdellah Z, Brooks K, Cherevach I, Chillingworth T, Woodward J, Norberczak H, Lord A, Arrowsmith C, Jagels K, Moule S, Mungall K, Sanders M, Whitehead S, Chabalgoity JA, Maskell D, Humphrey T, Roberts M, Barrow PA, Dougan G, Parkhill J. 2008. Comparative genome analysis of Salmonella Enteritidis PT4 and Salmonella Gallinarum 287/91 provides insights into evolutionary and host adaptation pathways. Genome Res. 18:1624-1637.
11. Barrow PA, Huggins MB, Lovell MA. 1994. Host specificity of Salmonella infection in chickens and mice is expressed in vivo primarily at the level of the reticuloendothelial system. Infect. Immun. 62:4602-4610.
12. Chappell L, Kaiser P, Barrow P, Jones MA, Johnston C, Wigley P. 2009. The immunobiology of avian systemic salmonellosis. Vet. Immunol. Immunopathol. 128:53-59.
13. Shah DH, Lee MJ, Park JH, Lee JH, Eo SK, Kwon JT, Chae JS. 2005. Identification of Salmonella gallinarum virulence genes in a chicken infection model using PCR-based signature-tagged mutagenesis. Microbiology 151:3957-3968.
14. Jones MA, Wigley P, Page KL, Hulme SD, Barrow PA. 2001. Salmonella enterica serovar Gallinarum requires the Salmonella pathogenicity island 2 type III secretion system but not the Salmonella pathogenicity island 1 type III secretion system for virulence in chickens. Infect. Immun. 69:5471-5476.
15. Jeong JH, Song M, Park SI, Cho KO, Rhee JH, Choy HE. 2008. Salmonella enterica serovar Gallinarum requires ppGpp for internalization and survival in animal cells. J. Bacteriol. 190:6340-6350.
16. Mizusaki H, Takaya A, Yamamoto T, Aizawa S. 2008. Signal pathway in salt-activated expression of the Salmonella pathogenicity island 1 type III secretion system in Salmonella enterica serovar Typhimurium. J. Bacteriol. 190:4624-4631.
17. Groisman EA, Kayser J, Soncini FC. 1997. Regulation of polymyxin resistance and adaptation to low-Mg2+ environments. J. Bacteriol. 179: 7040-7045.
18. 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.
19. Bravo D, Blondel CJ, Hoare A, Leyton L, Valvano MA, Contreras I. 2011. Type IV(B) pili are required for invasion but not for adhesion of Salmonella enterica serovar Typhi into BHK epithelial cells in a cystic fibrosis transmembrane conductance regulator-independent manner. Microb. Pathog. 51:373-377.
20. Ellermeier CD, Janakiraman A, Slauch JM. 2002. Construction of targeted single copy lac fusions using lambda Red and FLP-mediated sitespecific recombination in bacteria. Gene 290:153-161.
21. 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.
22. Gerlach RG, Holzer SU, Jackel D, Hensel M. 2007. Rapid engineering of bacterial reporter gene fusions by using Red recombination. Appl. Environ. Microbiol. 73:4234-4242.
23. Ho TD, Figueroa-Bossi N, Wang M, Uzzau S, Bossi L, Slauch JM. 2002. Identification of GtgE, a novel virulence factor encoded on the Gifsy-2 bacteriophage of Salmonella enterica serovar Typhimurium. J. Bacteriol. 184:5234-5239.
24. Schwan WR, Huang XZ, Hu L, Kopecko DJ. 2000. Differential bacterial survival, replication, and apoptosis-inducing ability of Salmonella serovars within human and murine macrophages. Infect. Immun. 68:1005-1013.
25. 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.
26. Raffatellu M, Sun YH, Wilson RP, Tran QT, Chessa D, Andrews-Polymenis HL, Lawhon SD, Figueiredo JF, Tsolis RM, Adams LG, Baumler AJ. 2005. Host restriction of Salmonella enterica serotype Typhi is not caused by functional alteration of SipA, SopB, or SopD. Infect. Immun. 73:7817-7826.
27. Hebrard M, Kroger C, Sivasankaran SK, Handler K, Hinton JC. 2011. The challenge of relating gene expression to the virulence of Salmonella enterica serovar Typhimurium. Curr. Opin. Biotechnol. 22:200-210. 28. Ellermeier JR, Slauch JM. 2007. Adaptation to the host environment: regulation of the SPI1 type III secretion system in Salmonella enterica serovar Typhimurium. Curr. Opin. Microbiol. 10:24-29.
28. Ellermeier JR, Slauch JM. 2007. Adaptation to the host environment: regulation of the SPI1 type III secretion system in Salmonella enterica serovar Typhimurium. Curr. Opin. Microbiol. 10:24-29.
29. Deiwick J, Nikolaus T, Erdogan S, Hensel M. 1999. Environmental regulation of Salmonella pathogenicity island 2 gene expression. Mol. Microbiol. 31:1759-1773.
30. Murdoch SL, Trunk K, English G, Fritsch MJ, Pourkarimi E, Coulthurst SJ. 2011. The opportunistic pathogen Serratia marcescens utilizes type VI secretion to target bacterial competitors. J. Bacteriol. 193:6057-6069.
31. MacIntyre DL, Miyata ST, Kitaoka M, Pukatzki S. 2010. The Vibrio cholerae type VI secretion system displays antimicrobial properties. Proc. Natl. Acad. Sci. U. S. A. 107:19520-19524.
32. Hood RD, Singh P, Hsu F, Guvener T, Carl MA, Trinidad RR, Silverman JM, Ohlson BB, Hicks KG, Plemel RL, Li M, Schwarz S, Wang WY, Merz AJ, Goodlett DR, Mougous JD. 2010. A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 7:25-37.
33. English G, Trunk K, Rao VA, Srikannathasan V, Hunter WN, Coulthurst SJ. 2012. New secreted toxins and immunity proteins encoded within the type VI secretion system gene cluster of Serratia marcescens. Mol. Microbiol. [Epub ahead of print.] doi:10.1111/mmi.12028.
34. 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.
35. Russell AB, Singh P, Brittnacher M, Bui NK, Hood RD, Carl MA, Agnello DM, Schwarz S, Goodlett DR, Vollmer W, Mougous JD. 2012. A widespread bacterial type VI secretion effector superfamily identified using a heuristic approach. Cell Host Microbe 11:538-549.
36. Bernard CS, Brunet YR, Gueguen E, Cascales E. 2010. Nooks and crannies in type VI secretion regulation. J. Bacteriol. 192:3850-3860.
37. 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.
38. Chakravortty D, Rohde M, Jager L, Deiwick J, Hensel M. 2005. Formation of a novel surface structure encoded by Salmonella pathogenicity island 2. EMBO J. 24:2043-2052.
39. Hoiseth SK, Stocker BA. 1981. Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291:238-239.
40. 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.
41. Suarez G, Sierra JC, Sha J, Wang S, Erova TE, Fadl AA, Foltz SM, Horneman AJ, Chopra AK. 2008. Molecular characterization of a functional type VI secretion system from a clinical isolate of Aeromonas hydrophila. Microb. Pathog. 44:344-361.
42. 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.
43. Hacker H, Furmann C, Wagner H, Hacker G. 2002. Caspase-9/-3 activation and apoptosis are induced in mouse macrophages upon ingestion and digestion of Escherichia coli bacteria. J. Immunol. 169:3172-3179. 44. Brencic A, Lory S. 2009. Determination of the regulon and identification of novelmRNAtargets of Pseudomonas aeruginosa RsmA. Mol. Microbiol. 72:612-632.
44. Brencic A, Lory S. 2009. Determination of the regulon and identification of novelmRNAtargets of Pseudomonas aeruginosa RsmA. Mol. Microbiol. 72:612-632.
45. Brencic A, McFarland KA, McManus HR, Castang S, Mogno I, Dove SL, Lory S. 2009. The GacS/GacA signal transduction system of Pseudomonas aeruginosa acts exclusively through its control over the transcription of the RsmY and RsmZ regulatory small RNAs. Mol. Microbiol. 73: 434-445.
46. Pieper R, Huang ST, Robinson JM, Clark DJ, Alami H, Parmar PP, Perry RD, Fleischmann RD, Peterson SN. 2009. Temperature and growth phase influence the outer-membrane proteome and the expres-sion of a type VI secretion system in Yersinia pestis. Microbiology 155: 498-512.
47. Wagner VE, Bushnell D, Passador L, Brooks AI, Iglewski BH. 2003. Microarray analysis of Pseudomonas aeruginosa quorum-sensing regulons: effects of growth phase and environment. J. Bacteriol. 185:2080-2095.
48. Ishikawa T, Rompikuntal PK, Lindmark B, Milton DL, Wai SN. 2009. Quorum sensing regulation of the two hcp alleles in Vibrio cholerae O1 strains. PLoS One 4:e6734. doi:10.1371/journal.pone.0006734.
49. Khajanchi BK, Sha J, Kozlova EV, Erova TE, Suarez G, Sierra JC, Popov VL, Horneman AJ, Chopra AK. 2009. N-acylhomoserine lactones involved in quorum sensing control the type VI secretion system, biofilm formation, protease production, and in vivo virulence in a clinical isolate of Aeromonas hydrophila. Microbiology 155:3518-3531.
50. Lesic B, Starkey M, He J, Hazan R, Rahme LG. 2009. Quorum sensing differentially regulates Pseudomonas aeruginosa type VI secretion locus I and homologous loci II and III, which are required for pathogenesis. Microbiology 155:2845-2855.
51. Mougous JD, Gifford CA, Ramsdell TL, Mekalanos JJ. 2007. Threonine phosphorylation post-translationally regulates protein secretion in Pseudomonas aeruginosa. Nat. Cell Biol. 9:797-803.
52. 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.
53. Valdivia RH, Falkow S. 1997. Fluorescence-based isolation of bacterial genes expressed within host cells. Science 277:2007-2011.
54. Cirillo DM, Valdivia RH, Monack DM, Falkow S. 1998. Macrophagedependent induction of the Salmonella pathogenicity island 2 type III secretion system and its role in intracellular survival. Mol. Microbiol. 30: 175-188.
55. Lim S, Kim B, Choi HS, Lee Y, Ryu S. 2006. Fis is required for proper regulation of ssaG expression in Salmonella enterica serovar Typhimurium. Microb. Pathog. 41:33-42.
56. Bradley MD, Beach MB, de Koning AP, Pratt TS, Osuna R. 2007. Effects of Fis on Escherichia coli gene expression during different growth stages. Microbiology 153:2922-2940.
57. Xu J, Johnson RC. 1995. Identification of genes negatively regulated by Fis: Fis and RpoS comodulate growth-phase-dependent gene expression in Escherichia coli. J. Bacteriol. 177:938-947.
58. 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.
59. Steele-Mortimer O. 2008. The Salmonella-containing vacuole: moving with the times. Curr. Opin. Microbiol. 11:38-45.
60. Brumell JH, Grinstein S. 2004. Salmonella redirects phagosomal maturation. Curr. Opin. Microbiol. 7:78-84.
61. Bakowski MA, Braun V, Brumell JH. 2008. Salmonella-containing vacuoles: directing traffic and nesting to grow. Traffic 9:2022-2031.
62. Thompson JA, Liu M, Helaine S, Holden DW. 2011. Contribution of the PhoP/Q regulon to survival and replication of Salmonella enterica serovar Typhimurium in macrophages. Microbiology 157:2084-2093.
63. Setta AM, Barrow PA, Kaiser P, Jones MA. 2012. Early immune dynamics following infection with Salmonella enterica serovars Enteritidis, Infantis, Pullorum and Gallinarum: cytokine and chemokine gene expression profile and cellular changes of chicken cecal tonsils. Comp. Immunol. Microbiol. Infect. Dis. 35:397-410.
64. Setta A, Barrow PA, Kaiser P, Jones MA. 2012. Immune dynamics following infection of avian macrophages and epithelial cells with typhoidal and non-typhoidal Salmonella enterica serovars; bacterial invasion and persistence, nitric oxide and oxygen production, differential host gene expression, NF-kappaB signalling and cell cytotoxicity. Vet. Immunol. Immunopathol. 146:212-224.
65. Libby SJ, Brehm MA, Greiner DL, Shultz LD, McClelland M, Smith KD, Cookson BT, Karlinsey JE, Kinkel TL, Porwollik S, Canals R, Cummings LA, Fang FC. 2010. Humanized nonobese diabetic-scid IL2rgamma null mice are susceptible to lethal Salmonella Typhi infection. Proc. Natl. Acad. Sci. U. S. A. 107:15589-15594.
66. Wang M, Luo Z, Du H, Xu S, Ni B, Zhang H, Sheng X, Xu H, Huang X. 2011. Molecular characterization of a functional type VI secretion system in Salmonella enterica serovar Typhi. Curr. Microbiol. 63:22-31.
67. Liu J, Guo JT, Li YG, Johnston RN, Liu GR, Liu SL. 2012. The type VI secretion system gene cluster of Salmonella typhimurium: required for full virulence in mice. J. Basic Microbiol. [Epub ahead of print.] doi:10.1002 /jobm.201200047.
68. Mulder DT, Cooper CA, Coombes BK. 2012. Type VI secretion systemassociated gene clusters contribute to pathogenesis of Salmonella enterica serovar Typhimurium. Infect. Immun. 80:1996-2007.
69. 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.
70. Santiviago CA, Blondel CJ, Quezada CP, Silva CA, Tobar PM, Porwollik S, McClelland M, Andrews-Polymenis HL, Toro CS, Zaldivar M, Contreras I. 2010. Spontaneous excision of the Salmonella enterica serovar Enteritidis-specific defective prophage-like element SE14. J. Bacteriol. 192:2246-2254.
71. Santiviago CA, Reynolds MM, Porwollik S, Choi SH, Long F, Andrews-Polymenis HL, McClelland M. 2009. Analysis of pools of targeted Salmonella deletion mutants identifies novel genes affecting fitness during competitive infection in mice. PLoS Pathog. 5:e1000477. doi:10.1371 /journal.ppat.1000477.