Diarrhea and colitis in mice require the Salmonella pathogenicity island 2-encoded secretion function but not SifA or Spv effectors

Infection and Immunity

Volumn 80, Issue 10, 2012, Pages 3360-3370

  Fierer, Joshua ^a,b,c   Okamoto, Sharon ^c   Banerjee, Ananya ^a   Guineya, Donald G ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b Medical Service   (United States)

^c Research Service   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; MUTANT PROTEIN; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 1; SALMONELLA PATHOGENICITY ISLAND 2 PROTEIN; SIFA PROTEIN; SPV EFFECTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; CECUM; COLITIS; CONTROLLED STUDY; DIARRHEA; DISEASE SEVERITY; FECES; FEMALE; GENE LOCUS; MOUSE; NONHUMAN; OBSERVATION; PANCOLITIS; PATHOGENICITY; PRIORITY JOURNAL; SALMONELLA; SALMONELLA ENTERICA; SALMONELLOSIS; SEROTYPE; WEIGHT REDUCTION;

ADP RIBOSE TRANSFERASES; ALLELES; ANIMALS; BACTERIAL PROTEINS; CATION TRANSPORT PROTEINS; COLITIS; COLON; DIARRHEA; FECES; FEMALE; GENETIC PREDISPOSITION TO DISEASE; GLYCOPROTEINS; MACROPHAGES; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; SALMONELLA; SALMONELLA INFECTIONS, ANIMAL; SALMONELLA TYPHIMURIUM; SPECIFIC PATHOGEN-FREE ORGANISMS; VIRULENCE; VIRULENCE FACTORS;

EID: 84867617158     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00404-12     Document Type: Article

References (59)

1. Bain CC, Mowat AM. 2011. Intestinal macrophages-specialised adaptation to a unique environment. Eur. J. Immunol. 41:2494-2498.
2. Barthel M, et al. 2003. Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect. Immun. 71:2839-2858.
3. Bertelsen LS, Paesold G, Eckmann L, Barrett KE. 2003. Salmonella infection induces a hypersecretory phenotype in human intestinal xenografts by inducing cyclooxygenase 2. Infect. Immun. 71:2102-2109.
4. Beuzón CR, et al. 2000. Salmonella maintains the integrity of its intracellular vacuole through the action of SifA. EMBO J. 19:3235-3249.
5. Beuzon CR, Salcedo SP, Holden DW. 2002. Growth and killing of a Salmonella enterica serovar Typhimurium sifA mutant strain in the cytosol of different host cell lines. Microbiology 148:2705-2715.
6. Bohnhoff M, Drake BL, Miller CP. 1954. Effect of streptomycin on susceptibility of intestinal tract to experimental Salmonella infection. Proc. Soc. Exp. Biol. Med. 86:132-137.
7. Boucrot E, Beuzón CR, Holden DW, Gorvel J-P, Meresse S. 2003. Salmonella typhimurium SifA effector protein requires its membraneanchoring C-terminal hexapeptide for its biological function. J. Biol. Chem. 278:14196-14202.
8. Brawn LC, Hayward RD, Koronaksi 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. Browne SH, Hasegawa P, Okamoto S, Fierer J, Guiney DG. 2008. Identification of Salmonella SPI-2 secretion system components required for SpvB-mediated cytotoxicity in macrophages and virulence in mice. FEMS Immunol. Med. Microbiol. 52:194-201.
10. Brumell JH, Tang P, Zaharik ML, Finlay BB. 2002. Disruption of the Salmonella-containing vacuole leads to increased replication of Salmonella enterica serovar Typhimurium in the cytosol of epithelial cells. Infect. Immun. 70:3264-3270.
11. 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.
12. 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.
13. Coombes BK, 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.
14. Fields PI, Swanson RV, Haidaris CG, Heffron F. 1986. Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc. Natl. Acad. Sci. U. S. A. 83:5189-5193.
15. Fierer J, Guiney DG. 2001. Diverse virulence traits underlying different clinical outcomes of Salmonella infection. J. Clin. Invest. 107:775-780.
16. Fierer J, Krause M, Tauxe R, Guiney DG. 1992. Salmonella typhimurium bacteremia: association with the virulence plasmid. J. Infect. Dis. 166:639-642.
17. Geddes K, et al. 2010. Nod1 and Nod2 regulation of inflammation in the Salmonella colitis model. Infect. Immun. 78:5107-5115.
18. Govoni G, et al. 1996. The bcg/ity/lsh locus: genetic transfer of resistance to infections in C57BL/6J mice transgenic for the Nramp1Gly169 allele. Infect. Immun. 64:2923-2929.
19. Guiney DG, Fierer J. 2011. The role of the spv genes in Salmonella pathogenesis. Front. Microbiol. 2:129.
20. Guiney DG, Lesnick M. 2005. Targeting of the actin cytoskeleton during infection by Salmonella strains. Clin. Immunol. 114:248-255.
21. Guttman JA, et al. 2006. Attaching and effacing pathogen-induced tight junction disruption in vivo. Cell. Microbiol. 8:634-645.
22. Haneda T, et al. 2012. Salmonella type III effector SpvC, a phosphothreonine lyase, contributes to reduction in inflammatory response during intestinal phase of infection. Cell. Microbiol. 14:485- 499.
23. Hapfelmeier S, et al. 2004. Role of the Salmonella pathogenicity island 1 effector proteins SipA, SopB, SopE, and SopE2 in Salmonella enterica subspecies 1 serovar Typhimurium colitis in streptomycin-pretreated mice. Infect. Immun. 72:795- 809.
24. Hapfelmeier S, Hardt W-D. 2005. A mouse model for S. typhimuriuminduced enterocolitis. Trends Microbiol. 13:497-503.
25. Hapfelmeier S, et al. 2008. Microbe sampling by mucosal dendritic cells is a discrete, MyD88-independent step in delta invG S. typhimurium colitis. J. Exp. Med. 205:437- 450.
26. Hapfelmeier S, et al. 2005. The Salmonella pathogenicity island (SPI)-2 and SPI-1 type III secretion systems allow Salmonella serovar typhimurium to trigger colitis via MyD88-dependent and MyD88-independent mechanisms. J. Immunol. 174:1675-1685.
27. Hu Q, et al. 2008. Salmonella enterica serovar Senftenberg human clinical isolates lacking SPI-1. J. Clin. Microbiol. 46:1330-1336.
28. Ibarra JA, Steele-Mortimer O. 2009. Salmonella-the ultimate insider. Salmonella virulence factors that modulate intracellular survival. Cell. Microbiol. 11:1579-1586.
29. 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.
30. Käppeli R, Kaiser P, Stecher B, Hardt W-D. 2011. Roles of spvB and spvC in S. Typhimurium colitis via the alternative pathway. Int. J. Med. Microbiol. 301:117-124.
31. Kayagaki N, et al. 2011. Non-canonical inflammasome activation targets caspase-11. Nature 479:117-122.
32. Leone P, Meresse S. 2011. Kinesin regulation by Salmonella. Virulence 2:63- 66.
33. Lesnick ML, Reiner NE, Fierer J, Guiney DG. 2001. The Salmonella spvB virulence gene encodes an enzyme that ADP-ribosylates actin and destabilizes the cytoskeleton of eukaryotic cells. Mol. Microbiol. 39:1464-1470.
34. Libby SJ, et al. 1997. The spv genes on the Salmonella dublin virulence plasmid are required for severe enteritis and systemic infection in the natural host. Infect. Immun. 65:1786-1792.
35. Mahon BE, et al. 1997. An international outbreak of Salmonella infections caused by alfalfa sprouts grown from contaminated seeds. J. Infect. Dis. 175:876-882.
36. Marcus SL, Brumell JH, Pfeifer CG, Finlay BB. 2000. Salmonella pathogenicity islands: big virulence in small packages. Microbes Infect. 2:145- 156.
37. Miao EA, Miller SI. 2000. A conserved amino acid sequence directing intracellular type III secretion by Salmonella typhimurium. Proc. Natl. Acad. Sci. U. S. A. 97:7539-7544.
38. Mohle-Boetani JC, et al. 1999. An outbreak of Salmonella serogroup Saphra due to cantaloupes from Mexico. J. Infect. Dis. 180:1361-1364.
39. Mueller AJ, et al. 2012. Salmonella gut invasion involves TTSS-2-dependent epithelial traversal, basolateral exit, and uptake by epitheliumsampling lamina propria phagocytes. Cell Host Microbe 11:19-32.
40. Obonyo M, et al. 2007. Deficiencies of myeloid differentiation factor 88, Toll-like receptor 2 (TLR2), or TLR4 produce specific defects in macrophage cytokine secretion induced by Helicobacter pylori. Infect. Immun. 75:2408-2414.
41. Ohlson MB, et al. 2008. Structure and function of Salmonella SifA indicate that its interactions with SKIP, SseJ, and RhoA family GTPases induce endosomal tubulation. Cell Host Microbe 4:434-446.
42. Potter M, et al. 1983. A BALB/c congenic strain of mice that carries a genetic locus (Ity) controlling resistance to intracellular parasites. Infect. Immun. 40:1234-1235.
43. Roudier C, Fierer J, Guiney DG. 1992. Characterization of translation termination mutations in the spv operon of the Salmonella virulence plasmid pSDL2. J. Bacteriol. 174:6418-6423.
44. Sanders E, Brachman PS, Friedman EA, Goldsby J, McCall CE. 1965. Salmonellosis in the United States. Results of nationwide surveillance. Am. J. Epidemiol. 81:370-384.
45. Sheth AN, et al. 2011. A national outbreak of Salmonella serotype Tennessee infections from contaminated peanut butter: a new food vehicle for salmonellosis in the United States. Clin. Infect. Dis. 53:356-362.
46. Smythies LE, et al. 2005. Human intestinal macrophages display profound inflammatory anergy despite avid phagocytic and bacteriocidal activity. J. Clin. Invest. 115:66-75.
47. Stecher B, et al. 2004. Flagella and chemotaxis are required for efficient induction of Salmonella enterica serovar Typhimurium colitis in streptomycin-pretreated mice. Infect. Immun. 72:4138-4150.
48. + mice. Infect. Immun. 74:5047-5057.
49. Stein MA, Leung KY, Zwick M, Garcia-del Portillo F, Finlay BB. 1996. Identification of a Salmonella virulence gene required for formation of filamentous structures containing lysosomal membrane glycoproteins within epithelial cells. Mol. Microbiol. 20:151-164.
50. Suar M, et al. 2009. Accelerated type III secretion system 2 dependent enteropathogenesis by a Salmonella enterica serovar Enteritidis PT4/6 strain. Infect. Immun. 77:3569-3577.
51. Tsolis RM, Adams LG, Ficht TA, Bäumler AJ. 1999. Contribution of Salmonella typhimurium virulence factors to diarrheal disease in calves. Infect. Immun. 67:4879-4885.
52. Valdez Y, et al. 2009. Nramp1 drives an accelerated inflammatory response during Salmonella-induced colitis in mice. Cell. Microbiol. 11: 351-362.
53. Van Beneden CA, et al. 1999. Multinational outbreak of Salmonella enterica serotype Newport infections due to contaminated alfalfa sprouts. JAMA 281:158-162.
54. Vazquez-Torres A, et al. 1999. Extraintestinal dissemination of Salmonella by CD18-expressing phagocytes. Nature 401:804-808.
55. Vijay-Kumar M, et al. 2006. Flagellin suppresses epithelial apoptosis and limits disease during enteric infection. Am. J. Pathol. 169:1686-1700.
56. Woo H, Okamoto S, Guiney DG, Gunn JS, Fierer J. 2008. A model of Salmonella colitis with features of diarrhea in SLC11A1 wild-type mice. PLoS One 3:e1603. doi:10.1371/journal.pone.0001603.
57. Woodward MJ, McLaren I, Wray C. 1989. Distribution of virulence plasmids within salmonellae. J. Gen. Microbiol. 135:503-511.
58. Wray C, Sojka WJ. 1981. Salmonella dublin infection of calves: use of small doses to simulate natural infection on the farm. J. Hyg. (Lond.) 87:501-509.
59. Zhang S, et al. 2002. The Salmonella enterica serotype Typhimurium effector proteins SipA, SopA, SopB, SopD, and SopE2 act in concert to induce diarrhea in calves. Infect. Immun. 70:3843-3855.