Gene expression response of the rat small intestine following oral Salmonella infection

Physiological Genomics

Volumn 30, Issue 2, 2007, Pages 123-133

  Rodenburg, Wendy ^a,b,c   Bovee Oudenhoven, Ingeborg M J ^a,b   Kramer, Evelien ^a,c   Van Der Meer, Roelof ^a,b   Keijer, Jaap ^a,c  

^a TOP INSTITUTE FOOD AND NUTRITION   (Netherlands)

^b NIZO FOOD RESEARCH   (Netherlands)

^c WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Antimicrobial defense; Detoxification; Ileal mucosa; Peyer's patches; Salmonella enteritidis

Indexed keywords

ANTIINFECTIVE AGENT; BIOLOGICAL MARKER; CALPROTECTIN; CARBOHYDRATE; CHEMOKINE; CYTOKINE; DNA; LIPOCALIN; PANCREATITIS ASSOCIATED PROTEIN; PEPTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARBOHYDRATE TRANSPORT; CELL INVASION; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DETOXIFICATION; DNA MICROARRAY; FECES ANALYSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; ILEUM MUCOSA; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; MALE; MOUTH INFECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PEYER PATCH; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RAT; REAL TIME POLYMERASE CHAIN REACTION; SALMONELLOSIS; SMALL INTESTINE; UNINDEXED SEQUENCE;

ANIMALS; DNA, COMPLEMENTARY; GENE EXPRESSION; INTESTINE, SMALL; MALE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYMERASE CHAIN REACTION; RATS; RATS, WISTAR; RNA, MESSENGER; SALMONELLA INFECTIONS;

RATTUS; RATTUS NORVEGICUS; SALMONELLA; SALMONELLA ENTERITIDIS;

EID: 34547428356     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00190.2006     Document Type: Article

References (63)

1. Abrahams GL, Hensel M. Manipulating cellular transport and immune responses: dynamic interactions between intracellular Salmonella enterica and its host cells. Cell Microbiol 8: 728-737, 2006.
2. Baldwin DN, Vanchinathan V, Brown PO, Theriot JA. A gene-expression program reflecting the innate immune response of cultured intestinal epithelial cells to infection by Listeria monocytogenes. Genome Biol 4: R2, 2003.
3. Bovee-Oudenhoven IM, Lettink-Wissink ML, Van Doesburg W, Witteman BJ, Van Der Meer R. Diarrhea caused by enterotoxigenic Escherichia coli infection of humans is inhibited by dietary calcium. Gastroenterology 125: 469-476, 2003.
4. Bovee-Oudenhoven IM, ten Bruggencate SJ, Lettink-Wissink ML, van der Meer R. Dietary fructo-oligosaccharides and lactulose inhibit intestinal colonisation but stimulate translocation of salmonella in rats. Gut 52: 1572-1578, 2003.
5. Bovee-Oudenhoven IM, Termont DS, Weerkamp AH, Faassen-Peters MA, Van der Meer R. Dietary calcium inhibits the intestinal colonization and translocation of Salmonella in rats. Gastroenterology 113: 550-557, 1997.
6. Carlson M, Raab Y, Seveus L, Xu S, Hallgren R, Venge P. Human neutrophil lipocalin is a unique marker of neutrophil inflammation in ulcerative colitis and proctitis. Gut 50: 501-506, 2002.
7. Clark MA, Jepson MA. Intestinal M cells and their role in bacterial infection. Int J Med Microbiol 293: 17-39, 2003.
8. Clarke MB, Sperandio V. Events at the host-microbial interface of the gastrointestinal tract III. Cell-to-cell signaling among microbial flora, host, and pathogens: there is a whole lot of talking going on. Am J Physiol Gastrointest Liver Physiol 288: G1105-G1109, 2005.
9. Collier-Hyams LS, Sloane V, Batten BC, Neish AS. Cutting edge: bacterial modulation of epithelial signaling via changes in neddylation of cullin-1. J Immunol 175: 4194-4198, 2005.
10. Darwin KH, Miller VL. Molecular basis of the interaction of Salmonella with the intestinal mucosa. Clin Microbiol Rev 12: 405-428, 1999.
11. Desjeux A, Barthet M, Barthellemy S, Dagorn JC, Hastier P, Heresbach D, Bernard JP, Grimaud JC. Serum measurements of pancreatitis associated protein in active Crohn's disease with ileal location. Gastroenterol Clin Biol 26: 23-28, 2002.
12. Dieckgraefe BK, Crimmins DL, Landt V, Houchen C, Anant S, Porche-Sorbet R, Ladenson JH. Expression of the regenerating gene family in inflammatory bowel disease mucosa: Reg Ialpha upregulation, processing, and antiapoptotic activity. J Investig Med 50: 421-434, 2002.
13. 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 275: 14084-14094, 2000.
14. Frost AJ, Bland AP, Wallis TS. The early dynamic response of the calf ileal epithelium to Salmonella typhimurium. Vet Pathol 34: 369 - 386, 1997.
15. Havelaar AH, Garssen J, Takumi K, Koedam MA, Dufrenne JB, van Leusden FM, de La Fonteyne L, Bousema JT, Vos JG. A rat model for dose-response relationships of Salmonella Enteritidis infection. J Appl Microbiol 91: 442-452, 2001.
16. Herikstad H, Motarjemi Y, Tauxe RV. Salmonella surveillance: a global survey of public health serotyping. Epidemiol Infect 129: 1-8, 2002.
17. Hughes EA, Galan JE. Immune response to Salmonella: location, location, location? Immunity 16: 325-328, 2002.
18. Ishibashi Y, Arai T. A possible mechanism for host-specific pathogenesis of Salmonella serovars. Microb Pathog 21: 435-446, 1996.
19. Ismail AS, Hooper LV. Epithelial cells and their neighbors. IV. Bacterial contributions to intestinal epithelial barrier integrity. Am J Physiol Gastrointest Liver Physiol 289: G779-G784, 2005.
20. Jenner RG, Young RA. Insights into host responses against pathogens from transcriptional profiling. Nat Rev Microbiol 3: 281-294, 2005.
21. Jepson MA, Clark MA. The role of M cells in Salmonella infection. Microbes Infect 3: 1183-1190, 2001.
22. Jiang B, Xu S, Hou X, Pimentel DR, Brecher P, Cohen RA. Temporal control of NF-kappaB activation by ERK differentially regulates interleukin-1beta-induced gene expression. J Biol Chem 279: 1323-1329, 2004.
23. Keilbaugh SA, Shin ME, Banchereau RF, McVay LD, Boyko N, Artis D, Cebra JJ, Wu GD. Activation of RegIIIbeta/gamma and interferon gamma expression in the intestinal tract of SCID mice: an innate response to bacterial colonisation of the gut. Gut 54: 623-629, 2005.
24. Kelly D, Campbell JI, King TP, Grant G, Jansson EA, Coutts AG, Pettersson S, Conway S. Commensal anaerobic gut bacteria attenuate inflammation by regulating nuclear-cytoplasmic shuttling of PPAR-gamma and RelA. Nat Immun 5: 104-112, 2004.
25. Kuhle V, Abrahams GL, Hensel M. Intracellular Salmonella enterica redirect exocytic transport processes in a Salmonella pathogenicity island 2-dependent manner. Traffic 7: 716-730, 2006.
26. Langmann T, Moehle C, Mauerer R, Scharl M, Liebisch G, Zahn A, Stremmel W, Schmitz G. Loss of detoxification in inflammatory bowel disease: dysregulation of pregnane X receptor target genes. Gastroenterology 127: 26-40, 2004.
27. Meyerholz DK, Stabel TJ, Ackermann MR, Carlson SA, Jones BD, Pohlenz J. Early epithelial invasion by Salmonella enterica serovar Typhimurium DT104 in the swine ileum. Vet Pathol 39: 712-720, 2002.
28. Miller SI, Pegues DA. Salmonella species, including Salmonella typhi. In: Principles and Practice of Infectious Disease, edited by Mandell GL. New York: Churchill Livingstone, 2000, p. 1700-1716.
29. Morgan ET, Li-Masters T, Cheng PY. Mechanisms of cytochrome P450 regulation by inflammatory mediators. Toxicology 181-182: 207-210, 2002.
30. Naughton PJ, Clohessy PA, Grant G, Pusztai A, Golden B. Faecal calprotectin: non-invasive marker of gastrointestinal inflammation in Salmonella infected rats. Biochem Soc Trans 24: 308S, 1996.
31. Niewold TA, Kerstens HH, van der Meulen J, Smits MA, Hulst MM. Development of a porcine small intestinal cDNA micro-array: characterization and functional analysis of the response to enterotoxigenic E. coli. Vet Immunol Immunopathol 105: 317-329, 2005.
32. Nikolsky Y, Ekins S, Nikolskaya T, Bugrim A. A novel method for generation of signature networks as biomarkers from complex high throughput data. Toxicol Lett 158: 20-29, 2005.
33. Ogawa H, Fukushima K, Naito H, Funayama Y, Unno M, Takahashi K, Kitayama T, Matsuno S, Ohtani H, Takasawa S, Okamoto H, Sasaki I. Increased expression of HIP/PAP and regenerating gene III in human inflammatory bowel disease and a murine bacterial reconstitution model. Inflamm Bowel Dis 9: 162-170, 2003.
34. Ojcius DM, Degani H, Mispelter J, Dautry-Varsat A. Enhancement of ATP levels and glucose metabolism during an infection by Chlamydia NMR studies of living cells. J Biol Chem 273: 7052-7058, 1998.
35. Olsen SJ, Bishop R, Brenner FW, Roels TH, Bean N, Tauxe RV, Slutsker L. The changing epidemiology of Salmonella: trends in serotypes isolated from humans in the United States, 1987-1997. J Infect Dis 183: 753-761, 2001.
36. Pedron T, Thibault C, Sansonetti PJ. The invasive phenotype of Shigella flexneri directs a distinct gene expression pattern in the human intestinal epithelial cell line Caco-2. J Biol Chem 278: 33878-33886, 2003.
37. Pellis L, Franssen-van Hal NL, Burema J, Keijer J. The intraclass correlation coefficient applied for evaluation of data correction, labeling methods, and rectal biopsy sampling in DNA microarray experiments. Physiol Genomics 16: 99-106, 2003.
38. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118: 229-241, 2004.
39. Reeves PG, Nielsen FH, Fahey GC Jr. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 123: 1939-1951, 1993.
40. Renton KW. Alteration of drug biotransformation and elimination during infection and inflammation. Pharmacol Ther 92: 147-163, 2001.
41. Rimoldi M, Chieppa M, Salucci V, Avogadri F, Sonzogni A, Sampietro GM, Nespoli A, Viale G, Allavena P, Rescigno M. Intestinal immune homeostasis is regulated by the crosstalk between epithelial cells and dendritic cells. Nat Immun 6: 507-514, 2005.
42. Salzman NH, Chou MM, de Jong H, Liu L, Porter EM, Paterson Y. Enteric Salmonella infection inhibits Paneth cell antimicrobial peptide expression. Infect Immun 71: 1109-1115, 2003.
43. Santos RL, Zhang S, Tsolis RM, Baumler AJ, Adams LG. Morphologic and molecular characterization of Salmonella typhimurium infection in neonatal calves. Vet Pathol 39: 200-215, 2002.
44. Santos RL, Zhang S, Tsolis RM, Kingsley RA, Adams LG, Baumler AJ. Animal models of Salmonella infections: enteritis versus typhoid fever. Microbes Infect 3: 1335-1344, 2001.
45. Sass W, Dreyer HP, Seifert J. Rapid insorption of small particles in the gut. Am J Gastroenterol 85: 255-260, 1990.
46. Schwan WR, Huang XZ, Hu L, Kopecko DJ. Differential bacterial survival, replication, and apoptosis-inducing ability of Salmonella serovars within human and murine macrophages. Infect Immun 68: 1005-1013, 2000.
47. Sorbara LR, Maldarelli F, Chamoun G, Schilling B, Chokekijcahi S, Staudt L, Mitsuya H, Simpson IA, Zeichner SL. Human immunodefi-ciency virus type 1 infection of H9 cells induces increased glucose transporter expression. J Virol 70: 7275-7279, 1996.
48. Stecher B, Macpherson AJ, Hapfelmeier S, Kremer M, Stallmach T, Hardt WD. Comparison of Salmonella enterica serovar Typhimurium colitis in germfree mice and mice pretreated with streptomycin. Infect Immun 73: 3228-3241, 2005.
49. Stokes NR, Zhou X, Meltzer SJ, Kaper JB. Transcriptional responses of intestinal epithelial cells to infection with Vibrio cholerae. Infect Immun 72: 4240-4248, 2004.
50. Ten Bruggencate SJ, Bovee-Oudenhoven IM, Lettink-Wissink ML, Katan MB, Van Der Meer R. Dietary fructo-oligosaccharides and inulin decrease resistance of rats to Salmonella: protective role of calcium. Gut 53: 530-535, 2004.
51. Ten Bruggencate SJ, Bovee-Oudenhoven IM, Lettink-Wissink ML, Van der Meer R. Dietary fructo-oligosaccharides dose-dependently increase translocation of Salmonella in rats. J Nutr 133: 2313-2318, 2003.
52. Tian B, Nowak DE, Jamaluddin M, Wang S, Brasier AR. Identification of direct genomic targets downstream of the nuclear factor-kappaB transcription factor mediating tumor necrosis factor signaling. J Biol Chem 280: 17435-17448, 2005.
53. van Asten AJ, Koninkx JF, van Dijk JE. Salmonella entry: M cells versus absorptive enterocytes. Vet Microbiol 108: 149-152, 2005.
54. van Hal NL, Vorst O, van Houwelingen AM, Kok EJ, Peijnenburg A, Aharoni A, van Tunen AJ, Keijer J. The application of DNA microarrays in gene expression analysis. J Biotechnol 78: 271-280, 2000.
55. Vladoianu IR, Chang HR, Pechere JC. Expression of host resistance to Salmonella typhi and Salmonella typhimurium: bacterial survival within macrophages of murine and human origin. Microb Pathog 8: 83-90, 1990.
56. Wallis TS, Galyov EE. Molecular basis of Salmonella-induced enteritis. Mol Microbiol 36: 997-1005, 2000.
57. Wallis TS, Starkey WG, Stephen J, Haddon SJ, Osborne MP, Candy DC. The nature and role of mucosal damage in relation to Salmonella typhimurium-induced fluid secretion in the rabbit ileum. J Med Microbiol 22: 39-49, 1986.
58. Wassell J, Dolwani S, Metzner M, Losty H, Hawthorne A. Faecal calprotectin: a new marker for Crohn's disease? Ann Clin Biochem 41: 230-232, 2004.
59. White P, Liebhaber SA, Cooke NE. 129X1/SvJ mouse strain has a novel defect in inflammatory cell recruitment. J Immunol 168: 869-874, 2002.
60. Wick MJ. Living in the danger zone: innate immunity to Salmonella. Curr Opin Microbiol 7: 51-57, 2004.
61. Xu C, Li CY, Kong AN. Induction of phase I, II and III drug metabolism/ transport by xenobiotics. Arch Pharmacol Res (Seoul) 28: 249-268, 2005.
62. Zeng H, Wu H, Sloane V, Jones R, Yu Y, Lin P, Gewirtz AT, Neish AS. Flagellin/TLR5 responses in epithelia reveal intertwined activation of inflammatory and apoptotic pathways. Am J Physiol Gastrointest Liver Physiol 290: G96-G108, 2006.
63. Zhang S, Adams LG, Nunes J, Khare S, Tsolis RM, Baumler AJ. Secreted effector proteins of Salmonella enterica serotype typhimurium elicit host-specific chemokine profiles in animal models of typhoid fever and enterocolitis. Infect Immun 71: 4795-4803, 2003.