A gene-expression program reflecting the innate immune response of cultured intestinal epithelial cells to infection by Listeria monocytogenes

Genome Biology

Volumn 4, Issue 1, 2002, Pages

  Baldwin, David N ^a   Vanchinathan, Veena ^a   Brown, Patrick O ^a   Theriot, Julie A ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

Human Intestinal Epithelial Cell; Intestinal Epithelial Cell; Mutant Bacterium; Parallel Time; Transcriptional Response

Indexed keywords

ACTA PROTEIN, LISTERIA MONOCYTOGENES; BACTERIAL PROTEIN; CHEMOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MEMBRANE PROTEIN; PEPTIDE CHAIN TERMINATION RELEASE FACTOR 1; PEPTIDE CHAIN-TERMINATION RELEASE FACTOR 1; TRANSACTIVATOR PROTEIN; TRANSLATION TERMINATION FACTOR;

ARTICLE; CELL STRAIN CACO 2; DNA MICROARRAY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION PROFILING; GENETICS; HUMAN; INNATE IMMUNITY; LISTERIA MONOCYTOGENES; METABOLISM; MICROBIOLOGY; MUTATION; PATHOGENICITY; SIGNAL TRANSDUCTION; TIME; VIRULENCE;

BACTERIAL PROTEINS; CACO-2 CELLS; CHEMOKINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION PROFILING; HUMANS; IMMUNITY, NATURAL; LISTERIA MONOCYTOGENES; MEMBRANE PROTEINS; MUTATION; NF-KAPPA B; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PEPTIDE TERMINATION FACTORS; SIGNAL TRANSDUCTION; TIME FACTORS; TRANS-ACTIVATORS; VIRULENCE;

EID: 0037263735     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2002-4-1-r2     Document Type: Article

References (68)

1. Gaillard JL, Berche P, Frehel C, Gouin E, Cossart P: Entry of L. monocytogenes into cells is mediated by internalin, a repeat protein reminiscent of surface antigens from gram-positive cocci. Cell. 1991, 65: 1127-1141. DOI: 10.1016/0092-8674(91)90009-N
2. Mengaud J, Ohayon H, Gounon P, Mege RM, Cossart P: E-cadherin is the receptor for internalin, a surface protein required for entry of L. monocytogenes into epithelial cells. Cell. 1996, 84: 923-932. DOI: 10.1016/S0092-8674(00)81070-3
3. Braun L, Ohayon H, Cossart P: The InIB protein of Listeria monocytogenes is sufficient to promote entry into mammalian cells. Mol Microbiol. 1998, 27: 1077-1087. 10.1046/j.1365-2958.1998.00750.x. DOI: 10.1046/j.1365-2958.1998.00750.x
4. Braun L, Ghebrehiwet B, Cossart P: gC1q-R/p32, a C1q-binding protein, is a receptor for the InlB invasion protein of Listeria monocytogenes. EMBO J. 2000, 19: 1458-1466. 10.1093/emboj/19.7.1458. DOI: 10.1093/emboj/19.7.1458
5. Cossart P: Met, the HGF-SF receptor: another receptor for Listeria monocytogenes. Trends Microbiol. 2001, 9: 105-107. 10.1016/S0966-842X(00)01943-0. DOI: 10.1016/S0966-842X(00)01943-0
6. Lecuit M, Vandormael-Pournin S, Lefort J, Huerre M, Gounon P, Dupuy C, Babinet C, Cossart P: A transgenic model for listeriosis: role of internalin in crossing the intestinal barrier. Science. 2001, 292: 1722-1725. 10.1126/science.1059852. DOI: 10.1126/science.1059852
7. Cossart P: The listeriolysin O gene: a chromosomal locus crucial for the virulence of Listeria monocytogenes. Infection. 1988, 16: S157-S159. DOI: 10.1007/BF01639740
8. Goebel W, Kathariou S, Kuhn M, Sokolovic Z, Kreft J, Kohler S, Funke D, Chakraborty T, Leimeister-Wachter M: Hemolysin from Listeria - biochemistry, genetics and function in pathogenesis. Infection. 1988, 16: S149-S156. DOI: 10.1007/BF01639739
9. Gaillard JL, Berche P, Sansonetti P: Transposon mutagenesis as a tool to study the role of hemolysin in the virulence of Listeria monocytogenes. Infect Immun. 1986, 52: 50-55.
10. Gaillard JL, Berche P, Mounier J, Richard S, Sansonetti P: In vitro model of penetration and intracellular growth of Listeria monocytogenes in the human enterocyte-like cell line Caco-2. Infect Immun. 1987, 55: 2822-2829.
11. Mengaud J, Braun-Breton C, Cossart P: Identification of phosphatidylinositol-specific phospholipase C activity in Listeria monocytogenes: a novel type of virulence factor?. Mol Microbiol. 1991, 5: 367-372. DOI: 10.1111/j.1365-2958.1991.tb02118.x
12. Camilli A, Goldfine H, Portnoy DA: Listeria monocytogenes mutants lacking phosphatidylinositol-specific phospholipase C are avirulent. J Exp Med. 1991, 173: 751-754. DOI: 10.1084/jem.173.3.751
13. Smith GA, Marquis H, Jones S, Johnston NC, Portnoy DA, Goldfine H: The two distinct phospholipases C of Listeria monocytogenes have overlapping roles in escape from a vacuole and cell-to-cell spread. Infect Immun. 1995, 63: 4231-4237.
14. Kocks C, Gouin E, Tabouret M, Berche P, Ohayon H, Cossart P: L. monocytogenes-induced actin assembly requires the actA gene product, a surface protein. Cell. 1992, 68: 521-531. DOI: 10.1016/0092-8674(92)90188-I
15. Kocks C, Hellio R, Gounon P, Ohayon H, Cossart P: Polarized distribution of Listeria monocytogenes surface protein ActA at the site of directional actin assembly. J Cell Sci. 1993, 105: 699-710.
16. Tilney LG, Portnoy DA: Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J Cell Biol. 1989, 109: 1597-1608. DOI: 10.1083/jcb.109.4.1597
17. Eckmann L, Smith JR, Housley MP, Dwinell MB, Kagnoff MF: Analysis by high density cDNA arrays of altered gene expression in human intestinal epithelial cells in response to infection with the invasive enteric bacteria Salmonella. J Biol Chem. 2000, 275: 14084-14094. 10.1074/jbc.275.19.14084. DOI: 10.1074/jbc.275.19.14084
18. Detweiler CS, Cunanan DB, Falkow S: Host microarray analysis reveals a role for the Salmonella response regulator phoP in human macrophage cell death. Proc Natl Acad Sci USA. 2001, 98: 5850-5855. 10.1073/pnas.091110098. DOI: 10.1073/pnas.091110098
19. Cohen P, Bouaboula M, Bellis M, Baron V, Jbilo O, Poinot-Chazel C, Galiegue S, Hadibi EH, Casellas P: Monitoring cellular responses to Listeria monocytogenes with oligonucleotide arrays. J Biol Chem. 2000, 275: 11181-11190. 10.1074/jbc.275.15.11181. DOI: 10.1074/jbc.275.15.11181
20. Salama N, Guillemin K, McDaniel TK, Sherlock G, Tompkins L, Falkow S: A whole-genome microarray reveals genetic diversity among Helicobacter pylori strains. Proc Natl Acad Sci USA. 2000, 97: 14668-14673. 10.1073/pnas.97.26.14668. DOI: 10.1073/pnas.97.26.14668
21. Saban MR, Hellmich H, Nguyen NB, Winston J, Hammond TG, Saban R: Time course of LPS-induced gene expression in a mouse model of genitourinary inflammation. Physiol Genomics. 2001, 5: 147-160.
22. Hooper LV, Wong MH, Thelin A, Hansson L, Falk PG, Gordon JI: Molecular analysis of commensal host-microbial relationships in the intestine. Science. 2001, 291: 881-884. 10.1126/science.291.5505.881. DOI: 10.1126/science.291.5505.881
23. Jumarie C, Malo C: Caco-2 cells cultured in serum-free medium as a model for the study of enterocytic differentiation in vitro. J Cell Physiol. 1991, 149: 24-33. DOI: 10.1002/jcp.1041490105
24. Hilgers AR, Conradi RA, Burton PS: Caco-2 cell monolayers as a model for drug transport across the intestinal mucosa. Pharm Res. 1990, 7: 902-910. 10.1023/A:1015937605100. DOI: 10.1023/A:1015937605100
25. Ranaldi G, Islam K, Sambuy Y: Epithelial cells in culture as a model for the intestinal transport of antimicrobial agents. Antimicrob Agents Chemother. 1992, 36: 1374-1381. DOI: 10.1128/AAC.36.7.1374
26. Schuerer-Maly CC, Eckmann L, Kagnoff MF, Falco MT, Maly FE: Colonic epithelial cell lines as a source of interleukin-8: stimulation by inflammatory cytokines and bacterial lipopolysaccharide. Immunology. 1994, 81: 85-91.
27. Eckmann L, Jung HC, Schurer-Maly C, Panja A, Morzycka-Wroblewska E, Kagnoff MF: Differential cytokine expression by human intestinal epithelial cell lines: regulated expression of interleukin 8. Gastroenterology. 1993, 105: 1689-1697.
28. Yang SK, Eckmann L, Panja A, Kagnoff MF: Differential and regulated expression of C-X-C, C-C, and C-chemokines by human colon epithelial cells. Gastroenterology. 1997, 113: 1214-1223. DOI: 10.1053/gast.1997.v113.pm9322516
29. Elewaut D, DiDonato JA, Kim JM, Truong F, Eckmann L, Kagnoff MF: NF-kappa B is a central regulator of the intestinal epithelial cell innate immune response induced by infection with enteroinvasive bacteria. J Immunol. 1999, 163: 1457-1466.
30. Brundage RA, Smith GA, Camilli A, Theriot JA, Portnoy DA: Expression and phosphorylation of the Listeria monocytogenes ActA protein in mammalian cells. Proc Natl Acad Sci USA. 1993, 90: 11890-11894. DOI: 10.1073/pnas.90.24.11890
31. Chakraborty T, Leimeister-Wachter M, Domann E, Hartl M, Goebel W, Nichterlein T, Notermans S: Coordinate regulation of virulence genes in Listeria monocytogenes requires the product of the prfA gene. J Bacteriol. 1992, 174: 568-574.
32. Leimeister-Wachter M, Haffner C, Domann E, Goebel W, Chakraborty T: Identification of a gene that positively regulates expression of listeriolysin, the major virulence factor of Listeria monocytogenes. Proc Natl Acad Sci USA. 1990, 87: 8336-8340. DOI: 10.1073/pnas.87.21.8336
33. Freitag NE, Rong L, Portnoy DA: Regulation of the prfA transcriptional activator of Listeria monocytogenes: multiple promoter elements contribute to intracellular growth and cell-to-cell spread. Infect Immun. 1993, 61: 2537-2544.
34. Sibelius U, Schulz EC, Rose F, Hattar K, Jacobs T, Weiss S, Chakraborty T, Seeger W, Grimminger F: Role of Listeria monocytogenes exotoxins listeriolysin and phosphatidylinositol-specific phospholipase C in activation of human neutrophils. Infect Immun. 1999, 67: 1125-1130.
35. Rose F, Zeller SA, Chakraborty T, Domann E, Machleidt T, Kronke M, Seeger W, Grimminger F, Sibelius U: Human endothelial cell activation and mediator release in response to Listeria monocytogenes virulence factors. Infect Immun. 2001, 69: 897-905. 10.1128/IAI.69.2.897-905.2001. DOI: 10.1128/IAI.69.2.897-905.2001
36. Vazquez MA, Sicher SC, Wright WJ, Proctor ML, Schmalzried SR, Stallworth KR, Crowley JC, Lu CY: Differential regulation of TNF-alpha production by listeriolysin-producing versus non-producing strains of Listeria monocytogenes. J Leukocyte Biol. 1995, 58: 556-562.
37. Vazquez MA, Sicher SC, Proctor ML, Crowley JC, Lu CY: Differential regulation of Ia expression and antigen presentation by listeriolysin-producing versus non-producing strains of Listeria monocytogenes. J Leukocyte Biol. 1996, 59: 683-690.
38. Drevets DA: Listeria monocytogenes virulence factors that stimulate endothelial cells. Infect Immun. 1998, 66: 232-238.
39. Kayal S, Lilienbaum A, Poyart C, Memet S, Israel A, Berche P: Listeriolysin O-dependent activation of endothelial cells during infection with Listeria monocytogenes: activation of NF-kappa B and upregulation of adhesion molecules and chemokines. Mol Microbiol. 1999, 31: 1709-1722. 10.1046/j.1365-2958.1999.01305.x. DOI: 10.1046/j.1365-2958.1999.01305.x
40. Lashkari DA, DeRisi JL, McCusker JH, Namath AF, Gentile C, Hwang SY, Brown PO, Davis RW: Yeast microarrays for genome wide parallel genetic and gene expression analysis. Proc Natl Acad Sci USA. 1997, 94: 13057-13062. 10.1073/pnas.94.24.13057. DOI: 10.1073/pnas.94.24.13057
41. Alizadeh AA, Eisen MB, Davis RE, Ma C, Lossos IS, Rosenwald A, Boldrick JC, Sabet H, Tran T, Yu X, et al: Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature. 2000, 403: 503-511. 10.1038/35000501. DOI: 10.1038/35000501
42. Iyer VR, Eisen MB, Ross DT, Schuler G, Moore T, Lee JCF, Trent JM, Staudt LM, Hudson J, Boguski MS, et al: The transcriptional program in the response of human fibroblasts to serum. Science. 1999, 283: 83-87. 10.1126/science.283.5398.83. DOI: 10.1126/science.283.5398.83
43. Pollack JR, Perou CM, Alizadeh AA, Eisen MB, Pergamenschikov A, Williams CF, Jeffrey SS, Botstein D, Brown PO: Genome-wide analysis of DNA copy-number changes using cDNA microarrays. Nat Genet. 1999, 23: 41-46. 10.1038/14385. DOI: 10.1038/14385
44. Tusher VG, Tibshirani R, Chu G: Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA. 2001, 98: 5116-5121. 10.1073/pnas.091062498. DOI: 10.1073/pnas.091062498
45. Cameron LA, Giardini PA, Soo FS, Theriot JA: Secrets of actin-based motility revealed by a bacterial pathogen. Nat Rev Mol Cell Biol. 2000, 1: 110-119. 10.1038/35040061. DOI: 10.1038/35040061
46. Sheehan B, Klarsfeld A, Msadek T, Cossart P: Differential activation of virulence gene expression by PrfA, the Listeria monocytogenes virulence regulator. J Bacteriol. 1995, 177: 6469-6476.
47. Anisowicz A, Messineo M, Lee SW, Sager R: An NF-kappa B-like transcription factor mediates IL-1/TNF-alpha induction of gro in human fibroblasts. J Immunol. 1991, 147: 520-527.
48. Boldrick JC, Alizadeh AA, Diehn M, Dudoit S, Liu CL, Belcher CE, Botstein D, Staudt LM, Brown PO, Relman DA: Stereotyped and specific gene expression programs in human innate immune responses to bacteria. Proc Natl Acad Sci USA. 2002, 99: 972-977. 10.1073/pnas.231625398. DOI: 10.1073/pnas.231625398
49. Medzhitov R, Janeway C: The Toll receptor family and microbial recognition. Trends Microbiol. 2000, 8: 452-456. 10.1016/S0966-842X(00)01845-X. DOI: 10.1016/S0966-842X(00)01845-X
50. Meister M, Lemaitre B, Hoffmann JA: Antimicrobial peptide defense in Drosophila. BioEssays. 1997, 19: 1019-1026. DOI: 10.1002/bies.950191112
51. Imler JL, Hoffmann JA: Toll receptors in innate immunity. Trends Cell Biol. 2001, 11: 304-311. 10.1016/S0962-8924(01)02004-9. DOI: 10.1016/S0962-8924(01)02004-9
52. Cario E, Podolsky DK: Differential alteration in intestinal epithelial cell expression of toll-like receptor 3 (TLR3) and TLR4 in inflammatory bowel disease. Infect Immun. 2000, 68: 7010-7017. 10.1128/IAI.68.12.7010-7017.2000. DOI: 10.1128/IAI.68.12.7010-7017.2000
53. Cario E, Rosenberg IM, Brandwein SL, Beck PL, Reinecker HC, Podolsky DK: Lipopolysaccharide activates distinct signaling pathways in intestinal epithelial cell lines expressing Toll-like receptors. J Immunol. 2000, 164: 966-972. DOI: 10.4049/jimmunol.164.2.966
54. Fusunyan RD, Nanthakumar NN, Baldeon ME, Walker WA: Evidence for an innate immune response in the immature human intestine: Toll-like receptors on fetal enterocytes. Pediatr Res. 2001, 49: 589-593. DOI: 10.1203/00006450-200104000-00023
55. Hayashi F, Smith KD, Ozinsky A, Hawn TR, Yi EC, Goodlett DR, Eng JK, Akira S, Underhill DM, Aderem A: The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature. 2001, 410: 1099-1103. 10.1038/35074106. DOI: 10.1038/35074106
56. Kim JM, Eckmann L, Savidge TC, Lowe DC, Witthoft T, Kagnoff MF: Apoptosis of human intestinal epithelial cells after bacterial invasion. J Clin Invest. 1998, 102: 1815-1823. DOI: 10.1172/JCI2466
57. Conlan JW: Neutrophils and tumour necrosis factor-alpha are important for controlling early gastrointestinal stages of experimental murine listeriosis. J Med Microbiol. 1997, 46: 239-250. DOI: 10.1099/00222615-46-3-239
58. Lopez S, Marco AJ, Prats N, Czuprynski CJ: Critical role of neutrophils in eliminating Listeria monocytogenes from the central nervous system during experimental murine listeriosis. Infect Immun. 2000, 68: 4789-4791. 10.1128/IAI.68.8.4789-4791.2000. DOI: 10.1128/IAI.68.8.4789-4791.2000
59. Eckmann L, Kagnoff MF, Fierer J: Epithelial cells secrete the chemokine interleukin-8 in response to bacterial entry. Infect Immun. 1993, 61: 4569-4574.
60. Jung HC, Eckmann L, Yang SK, Panja A, Fierer J, Morzycka-Wroblewska E, Kagnoff MF: A distinct array of proinflammatory cytokines is expressed in human colon epithelial cells in response to bacterial invasion. J Clin Invest. 1995, 95: 55-65. DOI: 10.1172/JCI117676
61. Adams AE, Pringle JR: Staining of actin with fluorochrome-conjugated phalloidin. Methods Enzymol. 1991, 194: 729-731. DOI: 10.1016/0076-6879(91)94054-G
62. Brown Lab: experimental protocols. [http://cmgm.stanford.edu/pbrown/protocols/index.html]
63. A gene-expression program reflecting the innate immune response of cultured intestinal epithelial cells to infection by Listeria monocytogenes - supplementary information. [http://genome-www.stanford.edu/listeria/gut]
64. Stanford: functional genomics facility. [http://www.microarray.org]
65. Stanford Microarray Database. [http://genome-www5.stanford.edu/MicroArray/SMD/]
66. Sherlock G, Hernandez-Boussard T, Kasarskis A, Binkley G, Matese JC, Dwight SS, Kaloper M, Weng S, Jin H, Ball CA, et al: The Stanford Microarray Database. Nucleic Acids Res. 2001, 29: 152-155. 10.1093/nar/29.1.152. DOI: 10.1093/nar/29.1.152
67. SAM: significance analysis of microarrays. [http://www-stat.stanford.edu/~tibs/SAM/index.html]
68. Eisen MB, Spellman PT, Brown PO, Botstein D: Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA. 1998, 95: 14863-14868. 10.1073/pnas.95.25.14863. DOI: 10.1073/pnas.95.25.14863