Analysis of interactions of salmonella type three secretion mutants with 3-D intestinal epithelial cells

PLoS ONE

Volumn 5, Issue 12, 2010, Pages

  Radtke, Andrea L ^a   Wilson, James W ^a,b   Sarker, Shameema ^a   Nickerson, Cheryl A ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

^b VILLANOVA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM ISOLATION; BACTERIUM MUTANT; CELL AGGREGATION; CELL INTERACTION; CELL TYPE; CONTROLLED STUDY; GASTROINTESTINAL INFECTION; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM CELL; MICROBIAL ACTIVITY; NONHUMAN; PANETH CELL; PATHOGENICITY ISLAND; SALMONELLA ENTERICA; TYPE III SECRETION SYSTEM; TYPHOID FEVER; WILD TYPE; ANIMAL; CELL CULTURE; CELL LINE; CONFOCAL MICROSCOPY; CYTOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; INTESTINE MUCOSA; METABOLISM; METHODOLOGY; MICROBIOLOGY; MOUSE; MOUSE MUTANT; MUTATION; SALMONELLOSIS; THREE DIMENSIONAL IMAGING;

ANIMALIA; BACTERIA (MICROORGANISMS); SALMONELLA; SALMONELLA ENTERICA;

ANIMALS; CELL LINE; CELLS, CULTURED; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; IMAGING, THREE-DIMENSIONAL; INTESTINAL MUCOSA; MICE; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; MUTATION; SALMONELLA ENTERICA; SALMONELLA INFECTIONS;

EID: 78650804659     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0015750     Document Type: Article

References (85)

1. Mead PS, Slutsker L, Dietz V, McCaig LF, Bresee JS, et al. (1999) Food-related illness and death in the United States. Emerg Infect Dis 5: 607-625.
2. Galan JE, Collmer A (1999) Type III secretion machines: bacterial devices for protein delivery into host cells. Science 284: 1322-1328.
3. Galan JE, Zhou D (2000) Striking a balance: modulation of the actin cytoskeleton by Salmonella. Proc Natl Acad Sci U S A 97: 8754-8761.
4. Hueck CJ (1998) Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev 62: 379-433.
5. Macnab RM (1999) The bacterial flagellum: reversible rotary propellor and type III export apparatus. J Bacteriol 181: 7149-7153.
6. Galan JE (2001) Salmonella interactions with host cells: type III secretion at work. Annu Rev Cell Dev Biol 17: 53-86.
7. Sukhan A, Kubori T, Wilson J, Galan JE (2001) Genetic analysis of assembly of the Salmonella enterica serovar Typhimurium type III secretion-associated needle complex. J Bacteriol 183: 1159-1167.
8. Francis CL, Ryan TA, Jones BD, Smith SJ, Falkow S (1993) Ruffles induced by Salmonella and other stimuli direct macropinocytosis of bacteria. Nature 364: 639-642.
9. Garcia del Portillo F, Finlay BB (1994) Salmonella invasion of nonphagocytic cells induces formation of macropinosomes in the host cell. Infect Immun 62: 4641-4645.
10. 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.
11. Waterman SR, Holden DW (2003) Functions and effectors of the Salmonella pathogenicity island 2 type III secretion system. Cell Microbiol 5: 501-511.
12. Frye J, Karlinsey JE, Felise HR, Marzolf B, Dowidar N, et al. (2006) Identification of new flagellar genes of Salmonella enterica serovar Typhimurium. J Bacteriol 188: 2233-2243.
13. Yanagihara S, Iyoda S, Ohnishi K, Iino T, Kutsukake K (1999) Structure and transcriptional control of the flagellar master operon of Salmonella typhimurium. Genes Genet Syst 74: 105-111.
14. Kutsukake K (1997) Autogenous and global control of the flagellar master operon, flhD, in Salmonella typhimurium. Mol Gen Genet 254: 440-448.
15. Claret L, Miquel S, Vieille N, Ryjenkov DA, Gomelsky M, et al. (2007) The flagellar sigma factor FliA regulates adhesion and invasion of Crohn diseaseassociated Escherichia coli via a cyclic dimeric GMP-dependent pathway. J Biol Chem 282: 33275-33283.
16. Carter PB, Collins FM (1974) The route of enteric infection in normal mice. J Exp Med 139: 1189-1203.
17. Pullinger GD, Paulin SM, Charleston B, Watson PR, Bowen AJ, et al. (2007) Systemic translocation of Salmonella enterica serovar Dublin in cattle occurs predominantly via efferent lymphatics in a cell-free niche and requires type III secretion system 1 (T3SS-1) but not T3SS-2. Infect Immun 75: 5191-5199.
18. Raffatellu M, Wilson RP, Chessa D, Andrews-Polymenis H, Tran QT, et al. (2005) SipA, SopA, SopB, SopD, and SopE2 contribute to Salmonella enterica serotype typhimurium invasion of epithelial cells. Infect Immun 73: 146-154.
19. Baumler AJ, Tsolis RM, Valentine PJ, Ficht TA, Heffron F (1997) Synergistic effect of mutations in invA and lpfC on the ability of Salmonella typhimurium to cause murine typhoid. Infect Immun 65: 2254-2259.
20. Bueno SM, Wozniak A, Leiva ED, Riquelme SA, Carreno LJ, et al. Salmonella pathogenicity island 1 differentially modulates bacterial entry to dendritic and non-phagocytic cells. Immunology 130: 273-287.
21. Morgan E, Campbell JD, Rowe SC, Bispham J, Stevens MP, et al. (2004) Identification of host-specific colonization factors of Salmonella enterica serovar Typhimurium. Mol Microbiol 54: 994-1010.
22. Watson PR, Paulin SM, Bland AP, Jones PW, Wallis TS (1995) Characterization of intestinal invasion by Salmonella typhimurium and Salmonella dublin and effect of a mutation in the invH gene. Infect Immun 63: 2743-2754.
23. Wallis TS, Galyov EE (2000) Molecular basis of Salmonella-induced enteritis. Mol Microbiol 36: 997-1005.
24. Frost AJ, Bland AP, Wallis TS (1997) The early dynamic response of the calf ileal epithelium to Salmonella typhimurium. Vet Pathol 34: 369-386.
25. Galyov EE, Wood MW, Rosqvist R, Mullan PB, Watson PR, et al. (1997) A secreted effector protein of Salmonella dublin is translocated into eukaryotic cells and mediates inflammation and fluid secretion in infected ileal mucosa. Mol Microbiol 25: 903-912.
26. Tenor JL, McCormick BA, Ausubel FM, Aballay A (2004) Caenorhabditis elegans-based screen identifies Salmonella virulence factors required for conserved host-pathogen interactions. Curr Biol 14: 1018-1024.
27. Santos RL, Zhang S, Tsolis RM, Kingsley RA, Adams LG, et al. (2001) Animal models of Salmonella infections: enteritis versus typhoid fever. Microbes Infect 3: 1335-1344.
28. Hu Q, Coburn B, Deng W, Li Y, Shi X, et al. (2008) Salmonella enterica serovar Senftenberg human clinical isolates lacking SPI-1. J Clin Microbiol 46: 1330-1336.
29. Hurley BP, McCormick BA (2003) Translating tissue culture results into animal models: the case of Salmonella typhimurium. Trends Microbiol 11: 562-569.
30. LaMarca HL, Ott CM, Honer Zu Bentrup K, Leblanc CL, Pierson DL, et al. (2005) Three-dimensional growth of extravillous cytotrophoblasts promotes differentiation and invasion. Placenta 26: 709-720.
31. Nickerson CA, Goodwin TJ, Terlonge J, Ott CM, Buchanan KL, et al. (2001) Three-dimensional tissue assemblies: novel models for the study of Salmonella enterica serovar Typhimurium pathogenesis. Infect Immun 69: 7106-7120.
32. Honer zu Bentrup K, Ramamurthy R, Ott CM, Emami K, Nelman-Gonzalez M, et al. (2006) Three-dimensional organotypic models of human colonic epithelium to study the early stages of enteric salmonellosis. Microbes Infect 8: 1813-1825.
33. Carterson AJ, Honer zu Bentrup K, Ott CM, Clarke MS, Pierson DL, et al. (2005) A549 lung epithelial cells grown as three-dimensional aggregates: alternative tissue culture model for Pseudomonas aeruginosa pathogenesis. Infect Immun 73: 1129-1140.
34. Straub TM, Honer zu Bentrup K, Orosz-Coghlan P, Dohnalkova A, Mayer BK, et al. (2007) In vitro cell culture infectivity assay for human noroviruses. Emerg Infect Dis 13: 396-403.
35. Hjelm BE, Berta AN, Nickerson CA, Arntzen CJ, Herbst-Kralovetz MM. Development and characterization of a three-dimensional organotypic human vaginal epithelial cell model. Biol Reprod 82: 617-627.
36. Barrila J, Radtke AL, Crabbe A, Sarker S, Herbst-Kralovetz MM, et al. (2010) 3D cell culture models: Innovative platforms for studying host-pathogen interactions. Nature Reviews Microbiology 8: 791-801.
37. Darwin KH, Miller VL (1999) Molecular basis of the interaction of Salmonella with the intestinal mucosa. Clin Microbiol Rev 12: 405-428.
38. MacBeth KJ, Lee CA (1993) Prolonged inhibition of bacterial protein synthesis abolishes Salmonella invasion. Infect Immun 61: 1544-1546.
39. Martinez-Argudo I, Jepson MA (2008) Salmonella translocates across an in vitro M cell model independently of SPI-1 and SPI-2. Microbiology 154: 3887-3894.
40. Lim JS, Na HS, Lee HC, Choy HE, Park SC, et al. (2009) Caveolae-mediated entry of Salmonella typhimurium in a human M-cell model. Biochem Biophys Res Commun 390: 1322-1327.
41. Jepson MA, Clark MA (2001) The role of M cells in Salmonella infection. Microbes Infect 3: 1183-1190.
42. Hase K, Kawano K, Nochi T, Pontes GS, Fukuda S, et al. (2009) Uptake through glycoprotein 2 of FimH(+) bacteria by M cells initiates mucosal immune response. Nature 462: 226-230.
43. Galan JE, Curtiss R 3rd (1989) Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. Proc Natl Acad Sci U S A 86: 6383-6387.
44. Galan JE, Ginocchio C, Costeas P (1992) Molecular and functional characterization of the Salmonella invasion gene invA: homology of InvA to members of a new protein family. J Bacteriol 174: 4338-4349.
45. Heesemann J, Laufs R (1985) Double immunofluorescence microscopic technique for accurate differentiation of extracellularly and intracellularly located bacteria in cell culture. J Clin Microbiol 22: 168-175.
46. Bishop A, House D, Perkins T, Baker S, Kingsley RA, et al. (2008) Interaction of Salmonella enterica serovar Typhi with cultured epithelial cells: roles of surface structures in adhesion and invasion. Microbiology 154: 1914-1926.
47. Macnab RM (2004) Type III flagellar protein export and flagellar assembly. Biochim Biophys Acta 1694: 207-217.
48. Fraser GM, Hirano T, Ferris HU, Devgan LL, Kihara M, et al. (2003) Substrate specificity of type III flagellar protein export in Salmonella is controlled by subdomain interactions in FlhB. Mol Microbiol 48: 1043-1057.
49. Murray RA, Lee CA (2000) Invasion genes are not required for Salmonella enterica serovar typhimurium to breach the intestinal epithelium: evidence that salmonella pathogenicity island 1 has alternative functions during infection. Infect Immun 68: 5050-5055.
50. Brayden DJ, Jepson MA, Baird AW (2005) Keynote review: intestinal Peyer's patch M cells and oral vaccine targeting. Drug Discov Today 10: 1145-1157.
51. Clark MA, Jepson MA, Simmons NL, Hirst BH (1994) Preferential interaction of Salmonella typhimurium with mouse Peyer's patch M cells. Res Microbiol 145: 543-552.
52. Clark MA, Hirst BH, Jepson MA (1998) Inoculum composition and Salmonella pathogenicity island 1 regulate M-cell invasion and epithelial destruction by Salmonella typhimurium. Infect Immun 66: 724-731.
53. 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.
54. Kraehenbuhl JP, Neutra MR (2000) Epithelial M cells: differentiation and function. Annu Rev Cell Dev Biol 16: 301-332.
55. Giannasca PJ, Giannasca KT, Leichtner AM, Neutra MR (1999) Human intestinal M cells display the sialyl Lewis A antigen. Infect Immun 67: 946-953.
56. Steele-Mortimer O, Meresse S, Gorvel JP, Toh BH, Finlay BB (1999) Biogenesis of Salmonella typhimurium-containing vacuoles in epithelial cells involves interactions with the early endocytic pathway. Cell Microbiol 1: 33-49.
57. Misselwitz B, Kreibich SK, Rout S, Stecher B, Periaswamy B, et al. (2010) Salmonella Typhimurium binds to HeLa cells via Fim-mediated reversible adhesion and irreversible TTSS-1 mediated docking. Infect Immun [Epub ahead of print].
58. Schenk M, Mueller C (2008) The mucosal immune system at the gastrointestinal barrier. Best Pract Res Clin Gastroenterol 22: 391-409.
59. Ho SY, Storch J (2001) Common mechanisms of monoacylglycerol and fatty acid uptake by human intestinal Caco-2 cells. Am J Physiol Cell Physiol 281: C1106-1117.
60. Westphal V, Murch S, Kim S, Srikrishna G, Winchester B, et al. (2000) Reduced heparan sulfate accumulation in enterocytes contributes to protein-losing enteropathy in a congenital disorder of glycosylation. Am J Pathol 157: 1917-1925.
61. Henry-Stanley MJ, Zhang B, Erlandsen SL, Wells CL (2006) Synergistic effect of tumor necrosis factor-alpha and interferon-gamma on enterocyte shedding of syndecan-1 and associated decreases in internalization of Listeria monocytogenes and Staphylococcus aureus. Cytokine 34: 252-259.
62. Bevins CL (2004) The Paneth cell and the innate immune response. Curr Opin Gastroenterol 20: 572-580.
63. Ayabe T, Satchell DP, Wilson CL, Parks WC, Selsted ME, et al. (2000) Secretion of microbicidal alpha-defensins by intestinal Paneth cells in response to bacteria. Nat Immunol 1: 113-118.
64. Keshav S (2006) Paneth cells: leukocyte-like mediators of innate immunity in the intestine. J Leukoc Biol 80: 500-508.
65. Mastroianni JR, Ouellette AJ (2009) Alpha-defensins in enteric innate immunity: functional Paneth cell alpha-defensins in mouse colonic lumen. J Biol Chem 284: 27848-27856.
66. Nevalainen TJ, Shah VI, de Peralta-Venturina M, Amin MB (2001) Absence of group II phospholipase A2, a Paneth cell marker, from the epididymis. APMIS 109: 295-298.
67. Gersemann M, Becker S, Kubler I, Koslowski M, Wang G, et al. (2009) Differences in goblet cell differentiation between Crohn's disease and ulcerative colitis. Differentiation 77: 84-94.
68. Steele-Mortimer O, Brumell JH, Knodler LA, Meresse S, Lopez A, et al. (2002) The invasion-associated type III secretion system of Salmonella enterica serovar Typhimurium is necessary for intracellular proliferation and vacuole biogenesis in epithelial cells. Cell Microbiol 4: 43-54.
69. 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.
70. Desin TS, Lam PK, Koch B, Mickael C, Berberov E, et al. (2009) Salmonella enterica serovar enteritidis pathogenicity island 1 is not essential for but facilitates rapid systemic spread in chickens. Infect Immun 77: 2866-2875.
71. Jeong JH, Song M, Park SI, Cho KO, Rhee JH, et al. (2008) Salmonella enterica serovar gallinarum requires ppGpp for internalization and survival in animal cells. J Bacteriol 190: 6340-6350.
72. Hensel M (2004) Evolution of pathogenicity islands of Salmonella enterica. Int J Med Microbiol 294: 95-102.
73. Horiuchi S, Inagaki Y, Okamura N, Nakaya R, Yamamoto N (1992) Type 1 pili enhance the invasion of Salmonella braenderup and Salmonella typhimurium to HeLa cells. Microbiol Immunol 36: 593-602.
74. Lee FK, Morris C, Hackett J (2006) The Salmonella enterica serovar Typhi Vi capsule and self-association pili share controls on expression. FEMS Microbiol Lett 261: 41-46.
75. Folkesson A, Lofdahl S, Normark S (2002) The Salmonella enterica subspecies I specific centisome 7 genomic island encodes novel protein families present in bacteria living in close contact with eukaryotic cells. Res Microbiol 153: 537-545.
76. Folkesson A, Advani A, Sukupolvi S, Pfeifer JD, Normark S, et al. (1999) Multiple insertions of fimbrial operons correlate with the evolution of Salmonella serovars responsible for human disease. Mol Microbiol 33: 612-622.
77. Townsend SM, Kramer NE, Edwards R, Baker S, Hamlin N, et al. (2001) Salmonella enterica serovar Typhi possesses a unique repertoire of fimbrial gene sequences. Infect Immun 69: 2894-2901.
78. Edwards RA, Schifferli DM, Maloy SR (2000) A role for Salmonella fimbriae in intraperitoneal infections. Proc Natl Acad Sci U S A 97: 1258-1262.
79. Humphries AD, Townsend SM, Kingsley RA, Nicholson TL, Tsolis RM, et al. (2001) Role of fimbriae as antigens and intestinal colonization factors of Salmonella serovars. FEMS Microbiol Lett 201: 121-125.
80. Baumler AJ, Gilde AJ, Tsolis RM, van der Velden AW, Ahmer BM, et al. (1997) Contribution of horizontal gene transfer and deletion events to development of distinctive patterns of fimbrial operons during evolution of Salmonella serotypes. J Bacteriol 179: 317-322.
81. Gerlach RG, Jackel D, Stecher B, Wagner C, Lupas A, et al. (2007) Salmonella Pathogenicity Island 4 encodes a giant non-fimbrial adhesin and the cognate type 1 secretion system. Cell Microbiol 9: 1834-1850.
82. Lennox ES (1955) Transduction of linked genetic characters of the host by bacteriophage P1. Virology 1: 190-206.
83. Henle G, Deinhardt F (1957) The establishment of strains of human cells in tissue culture. J Immunol 79: 54-59.
84. Chen TR, Drabkowski D, Hay RJ, Macy M, Peterson W, Jr. (1987) WiDr is a derivative of another colon adenocarcinoma cell line, HT-29. Cancer Genet Cytogenet 27: 125-134.
85. Goodwin TJ, Schroeder WF, Wolf DA, Moyer MP (1993) Rotating-wall vessel coculture of small intestine as a prelude to tissue modeling: aspects of simulated microgravity. Proc Soc Exp Biol Med 202: 181-192.