Global analysis of the eukaryotic pathways and networks regulated by Salmonella typhimurium in mouse intestinal infection in vivo

BMC Genomics

Volumn 11, Issue 1, 2010, Pages

  Liu, Xingyin ^a   Lu, Rong ^a   Xia, Yinglin ^b   Sun, Jun ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b UNIVERSITY OF ROCHESTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 1; CALGRANULIN A; CALGRANULIN B; CARBOXYLESTERASE; CASPASE; CYTOCHROME P450 2C18; CYTOCHROME P450 4B1; EPITHELIAL DERIVED NEUTROPHIL ACTIVATING FACTOR 78; GAMMA INTERFERON; GELSOLIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1; INTERLEUKIN 18 RECEPTOR; INTERLEUKIN 4; INTERLEUKIN 9; JANUS KINASE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; MUCIN 1; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN KINASE B; REPLICATION FACTOR A; SERINE PROTEINASE INHIBITOR; STAT PROTEIN; SULFOTRANSFERASE; TUMOR NECROSIS FACTOR ALPHA; VILLIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BIOINFORMATICS; CELL PROLIFERATION; COLON MUCOSA; CONTROLLED STUDY; DOWN REGULATION; ENTERITIS; FEMALE; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; HISTOPATHOLOGY; HOST RESISTANCE; IMMUNE RESPONSE; IN VIVO STUDY; INTESTINE INFECTION; MITOCHONDRION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE PHOSPHORYLATION; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; SALMONELLA TYPHIMURIUM; SIGNAL TRANSDUCTION; ANIMAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; INTESTINE; INTESTINE MUCOSA; METABOLISM; MICROBIOLOGY; PATHOLOGY; PHYSIOLOGY; REPRODUCIBILITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SALMONELLOSIS; TIME; UPREGULATION; WESTERN BLOTTING;

EUKARYOTA; MUS; SALMONELLA; SALMONELLA TYPHIMURIUM;

ANIMALS; BLOTTING, WESTERN; DOWN-REGULATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; INTESTINAL MUCOSA; INTESTINES; MICE; REPRODUCIBILITY OF RESULTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM; SIGNAL TRANSDUCTION; TIME FACTORS; UP-REGULATION;

EID: 78650286641     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-11-722     Document Type: Article

References (111)

1. Herikstad H, Motarjemi Y, Tauxe RV. Salmonella surveillance: a global survey of public health serotyping. Epidemiol Infect 2002, 129(1):1-8. 2869853, 12211575.
2. Mead PS, Slutsker L, Dietz V, McCaig LF, Bresee JS, Shapiro C, Griffin PM, Tauxe RV. Food-related illness and death in the United States. Emerg Infect Dis 1999, 5(5):607-625. 10.3201/eid0505.990502, 2627714, 10511517.
3. Darwin KH, Miller VL. Molecular basis of the interaction of Salmonella with the intestinal mucosa. Clinical microbiology reviews 1999, 12(3):405-428. 100246, 10398673.
4. Brown NF, Vallance BA, Coombes BK, Valdez Y, Coburn BA, Finlay BB. Salmonella pathogenicity island 2 is expressed prior to penetrating the intestine. PLoS Pathog 2005, 1(3):e32. 10.1371/journal.ppat.0010032, 1287911, 16304611.
5. Du F, Galan JE. Selective inhibition of type III secretion activated signaling by the Salmonella effector AvrA. PLoS Pathog 2009, 5(9):e1000595. 10.1371/journal.ppat.1000595, 2742890, 19779561.
6. Gradel KO, Nielsen HL, Schonheyder HC, Ejlertsen T, Kristensen B, Nielsen H. Increased short- and long-term risk of inflammatory bowel disease after salmonella or campylobacter gastroenteritis. Gastroenterology 2009, 137(2):495-501. 10.1053/j.gastro.2009.04.001, 19361507.
7. Kumar S. Infection as a risk factor for gallbladder cancer. J Surg Oncol 2006, 93(8):633-639. 10.1002/jso.20530, 16724347.
8. Mager DL. Bacteria and cancer: cause, coincidence or cure? A review. J Transl Med 2006, 4:14. 10.1186/1479-5876-4-14, 1479838, 16566840.
9. Arrach N, Zhao M, Porwollik S, Hoffman RM, McClelland M. Salmonella promoters preferentially activated inside tumors. Cancer Res 2008, 68(12):4827-4832. 10.1158/0008-5472.CAN-08-0552, 18559530.
10. Zhao M, Yang M, Li XM, Jiang P, Baranov E, Li S, Xu M, Penman S, Hoffman RM. Tumor-targeting bacterial therapy with amino acid auxotrophs of GFP-expressing Salmonella typhimurium. Proceedings of the National Academy of Sciences of the United States of America 2005, 102(3):755-760. 10.1073/pnas.0408422102, 545558, 15644448.
11. Zhao M, Geller J, Ma H, Yang M, Penman S, Hoffman RM. Monotherapy with a tumor-targeting mutant of Salmonella typhimurium cures orthotopic metastatic mouse models of human prostate cancer. Proc Natl Acad Sci USA 2007, 104(24):10170-10174. 10.1073/pnas.0703867104, 1891231, 17548809.
12. Wang Y, Qu L, Uthe JJ, Bearson SM, Kuhar D, Lunney JK, Couture OP, Nettleton D, Dekkers JC, Tuggle CK. Global transcriptional response of porcine mesenteric lymph nodes to Salmonella enterica serovar Typhimurium. Genomics 2007, 90(1):72-84. 10.1016/j.ygeno.2007.03.018, 17499962.
13. 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(10):5850-5855. 10.1073/pnas.091110098, 33302, 11320214.
14. van Hemert S, Hoekman AJ, Smits MA, Rebel JM. Early host gene expression responses to a Salmonella infection in the intestine of chickens with different genetic background examined with cDNA and oligonucleotide microarrays. Comp Biochem Physiol Part D Genomics Proteomics 2006, 1(3):292-299. 10.1016/j.cbd.2006.05.001, 20483261.
15. van Hemert S, Hoekman AJ, Smits MA, Rebel JM. Gene expression responses to a Salmonella infection in the chicken intestine differ between lines. Vet Immunol Immunopathol 2006, 114(3-4):247-258. 10.1016/j.vetimm.2006.08.007, 16978708.
16. Mastroeni P, Sheppard M. Salmonella infections in the mouse model: host resistance factors and in vivo dynamics of bacterial spread and distribution in the tissues. Microbes Infect 2004, 6(4):398-405. 10.1016/j.micinf.2003.12.009, 15101397.
17. Barthel M, Hapfelmeier S, Quintanilla-Martinez L, Kremer M, Rohde M, Hogardt M, Pfeffer K, Russmann H, Hardt WD. Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infection and immunity 2003, 71(5):2839-2858. 10.1128/IAI.71.5.2839-2858.2003, 153285, 12704158.
18. Wang Y, Couture OP, Qu L, Uthe JJ, Bearson SM, Kuhar D, Lunney JK, Nettleton D, Dekkers JC, Tuggle CK. Analysis of porcine transcriptional response to Salmonella enterica serovar Choleraesuis suggests novel targets of NFkappaB are activated in the mesenteric lymph node. BMC Genomics 2008, 9:437. 10.1186/1471-2164-9-437, 2570369, 18811943.
19. Karavolos MH, Spencer H, Bulmer DM, Thompson A, Winzer K, Williams P, Hinton JC, Khan CM. Adrenaline modulates the global transcriptional profile of Salmonella revealing a role in the antimicrobial peptide and oxidative stress resistance responses. BMC Genomics 2008, 9:458. 10.1186/1471-2164-9-458, 2576261, 18837991.
20. Chiang HI, Swaggerty CL, Kogut MH, Dowd SE, Li X, Pevzner IY, Zhou H. Gene expression profiling in chicken heterophils with Salmonella enteritidis stimulation using a chicken 44 K Agilent microarray. BMC Genomics 2008, 9:526. 10.1186/1471-2164-9-526, 2588606, 18990222.
21. Abreu MT. Immunologic regulation of toll-like receptors in gut epithelium. Curr Opin Gastroenterol 2003, 19(6):559-564. 10.1097/00001574-200311000-00008, 15703605.
22. Abreu MT. Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Nat Rev Immunol 10(2):131-144. 10.1038/nri2707, 20098461.
23. Becker SM, Cho KN, Guo X, Fendig K, Oosman MN, Whitehead R, Cohn SM, Houpt ER. Epithelial cell apoptosis facilitates Entamoeba histolytica infection in the gut. Am J Pathol 176(3):1316-1322. 10.2353/ajpath.2010.090740, 20093500.
24. Fu Z, Kim J, Vidrich A, Sturgill TW, Cohn SM. Intestinal Cell Kinase, a MAP Kinase-Related Kinase, Regulates Proliferation and G1 Cell Cycle Progression of Intestinal Epithelial Cells. Am J Physiol Gastrointest Liver Physiol 2009, 297(4):G632-40. 10.1152/ajpgi.00066.2009, 2763805, 19696144.
25. Keely S, Glover LE, Weissmueller T, MacManus CF, Fillon S, Fennimore B, Colgan SP. Hypoxia-inducible factor-dependent regulation of platelet-activating factor receptor as a route for gram-positive bacterial translocation across epithelia. Mol Biol Cell 2010, 21(4):538-546. 10.1091/mbc.E09-07-0573, 2820419, 20032301.
26. Jilling T, Simon D, Lu J, Meng FJ, Li D, Schy R, Thomson RB, Soliman A, Arditi M, Caplan MS. The roles of bacteria and TLR4 in rat and murine models of necrotizing enterocolitis. J Immunol 2006, 177(5):3273-3282. 2697969, 16920968.
27. Jilling T, Lu J, Jackson M, Caplan MS. Intestinal epithelial apoptosis initiates gross bowel necrosis in an experimental rat model of neonatal necrotizing enterocolitis. Pediatr Res 2004, 55(4):622-629. 10.1203/01.PDR.0000113463.70435.74, 14764921.
28. Neish AS. Molecular aspects of intestinal epithelial cell-bacterial interactions that determine the development of intestinal inflammation. Inflamm Bowel Dis 2004, 10(2):159-168. 10.1097/00054725-200403000-00015, 15168817.
29. Neish AS. Microbes in gastrointestinal health and disease. Gastroenterology 2009, 136(1):65-80. 10.1053/j.gastro.2008.10.080, 2892787, 19026645.
30. Si-Tahar M, Merlin D, Sitaraman S, Madara JL. Constitutive and regulated secretion of secretory leukocyte proteinase inhibitor by human intestinal epithelial cells. Gastroenterology 2000, 118(6):1061-1071. 10.1016/S0016-5085(00)70359-3, 10833481.
31. Kolachala V, Ruble B, Vijay-Kumar M, Wang L, Mwangi S, Figler H, Figler R, Srinivasan S, Gewirtz A, Linden J, et al. Blockade of adenosine A2B receptors ameliorates murine colitis. Br J Pharmacol 2008, 155(1):127-137. 10.1038/bjp.2008.227, 2440087, 18536750.
32. Hardt WD, Galan JE. A secreted Salmonella protein with homology to an avirulence determinant of plant pathogenic bacteria. Proc Natl Acad Sci USA 1997, 94(18):9887-9892. 10.1073/pnas.94.18.9887, 23287, 9275221.
33. Sun J, Hobert ME, Rao AS, Neish AS, Madara JL. Bacterial activation of beta-catenin signaling in human epithelia. Am J Physiol Gastrointest Liver Physiol 2004, 287(1):G220-227. 10.1152/ajpgi.00498.2003, 14764450.
34. McCormick BA, Colgan SP, Delp-Archer C, Miller SI, Madara JL. Salmonella typhimurium attachment to human intestinal epithelial monolayers: transcellular signalling to subepithelial neutrophils. J Cell Biol 1993, 123(4):895-907. 10.1083/jcb.123.4.895, 2200157, 8227148.
35. Strath J, Georgopoulos LJ, Kellam P, Blair GE. Identification of genes differentially expressed as result of adenovirus type 5- and adenovirus type 12-transformation. BMC Genomics 2009, 10:67. 10.1186/1471-2164-10-67, 2651901, 19200380.
36. Jickling GC, Zhan X, Ander BP, Turner RJ, Stamova B, Xu H, Tian Y, Liu D, Davis RR, Lapchak PA, et al. Genome response to tissue plasminogen activator in experimental ischemic stroke. BMC Genomics 11:254. 10.1186/1471-2164-11-254, 2875237, 20406488.
37. Storey JD, Tibshirani R. Statistical significance for genomewide studies. Proc Natl Acad Sci USA 2003, 100(16):9440-9445. 10.1073/pnas.1530509100, 170937, 12883005.
38. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 2001, 98(9):5116-5121. 10.1073/pnas.091062498, 33173, 11309499.
39. Li CJ, Li RW, Wang YH, Elsasser TH. Pathway analysis identifies perturbation of genetic networks induced by butyrate in a bovine kidney epithelial cell line. Funct Integr Genomics 2007, 7(3):193-205. 10.1007/s10142-006-0043-2, 17186197.
40. Lagoa CE, Bartels J, Baratt A, Tseng G, Clermont G, Fink MP, Billiar TR, Vodovotz Y. The role of initial trauma in the host's response to injury and hemorrhage: insights from a correlation of mathematical simulations and hepatic transcriptomic analysis. Shock 2006, 26(6):592-600. 10.1097/01.shk.0000232272.03602.0a, 17117135.
41. Calvano SE, Xiao W, Richards DR, Felciano RM, Baker HV, Cho RJ, Chen RO, Brownstein BH, Cobb JP, Tschoeke SK, et al. A network-based analysis of systemic inflammation in humans. Nature 2005, 437(7061):1032-1037. 10.1038/nature03985, 16136080.
42. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25(4):402-408. 10.1006/meth.2001.1262, 11846609.
43. Liao AP, Petrof EO, Kuppireddi S, Zhao Y, Xia Y, Claud EC, Sun J. Salmonella type III effector AvrA stabilizes cell tight junctions to inhibit inflammation in intestinal epithelial cells. PLoS ONE 2008, 3(6):e2369. 10.1371/journal.pone.0002369, 2408728, 18523661.
44. Ye Z, Petrof EO, Boone D, Claud EC, Sun J. Salmonella effector AvrA regulation of colonic epithelial cell inflammation by deubiquitination. Am J Pathol 2007, 171(3):882-892. 10.2353/ajpath.2007.070220, 1959497, 17690189.
45. Lu R, Wu S, Liu X, Xia Y, Zhang YG, Sun J. Chronic effects of a Salmonella type III secretion effector protein AvrA in vivo. PLoS ONE 5(5):e10505. 10.1371/journal.pone.0010505, 2864765, 20463922.
46. Duan Y, Liao AP, Kuppireddi S, Ye Z, Ciancio MJ, Sun J. beta-Catenin activity negatively regulates bacteria-induced inflammation. Lab Invest 2007, 87(6):613-624.
47. Wu S, Ye Z, Liu X, Zhao Y, Xia Y, Steiner A, Petrof EO, Claud EC, Sun J. Salmonella typhimurium infection increases p53 acetylation in intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 298(5):G784-794. 10.1152/ajpgi.00526.2009, 20224008.
48. Liu X, Lu R, Wu S, Sun J. Salmonella regulation of intestinal stem cells through the Wnt/beta-catenin pathway. FEBS Lett 584(5):911-916. 10.1016/j.febslet.2010.01.024, 20083111.
49. Wu S, Liao AP, Xia Y, Li YC, Li JD, Sartor RB, Sun J. Vitamin D receptor negatively regulates bacterial-stimulated NF-kappaB activity in intestine. Am J Pathol 177(2):686-697. 10.2353/ajpath.2010.090998, 20566739.
50. He W, Wang ML, Jiang HQ, Steppan CM, Shin ME, Thurnheer MC, Cebra JJ, Lazar MA, Wu GD. Bacterial colonization leads to the colonic secretion of RELMbeta/FIZZ2, a novel goblet cell-specific protein. Gastroenterology 2003, 125(5):1388-1397. 10.1016/j.gastro.2003.07.009, 14598255.
51. Young CL, Feierstein A, Southwick FS. Calcium regulation of actin filament capping and monomer binding by macrophage capping protein. J Biol Chem 1994, 269(19):13997-14002.
52. Hayward RD, Koronakis V. Direct nucleation and bundling of actin by the SipC protein of invasive Salmonella. EMBO J 1999, 18(18):4926-4934. 10.1093/emboj/18.18.4926, 1171564, 10487745.
53. Zhou D, Mooseker MS, Galan JE. Role of the S. typhimurium actin-binding protein SipA in bacterial internalization. Science 1999, 283(5410):2092-2095. 10.1126/science.283.5410.2092, 10092234.
54. Scherer CA, Cooper E, Miller SI. The Salmonella type III secretion translocon protein SspC is inserted into the epithelial cell plasma membrane upon infection. Mol Microbiol 2000, 37(5):1133-1145. 10.1046/j.1365-2958.2000.02066.x, 10972831.
55. Unsal-Kacmaz K, Chastain PD, Qu PP, Minoo P, Cordeiro-Stone M, Sancar A, Kaufmann WK. The human Tim/Tipin complex coordinates an Intra-S checkpoint response to UV that slows replication fork displacement. Mol Cell Biol 2007, 27(8):3131-3142. 10.1128/MCB.02190-06, 1899931, 17296725.
56. Errico A, Costanzo V, Hunt T. Tipin is required for stalled replication forks to resume DNA replication after removal of aphidicolin in Xenopus egg extracts. Proc Natl Acad Sci USA 2007, 104(38):14929-14934. 10.1073/pnas.0706347104, 1975688, 17846426.
57. Wu S, Ye Z, Liu X, Zhao Y, Xia Y, Steiner A, Petrof EO, Claud EC, Sun J. Salmonella typhimurium infection increases p53 acetylation in intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 2010, 298(5):G784-794. 10.1152/ajpgi.00526.2009, 20224008.
58. Rodenburg W, Keijer J, Kramer E, Roosing S, Vink C, Katan MB, van der Meer R, Bovee-Oudenhoven IM. Salmonella induces prominent gene expression in the rat colon. BMC Microbiol 2007, 7:84. 10.1186/1471-2180-7-84, 2048963, 17850650.
59. Lewin MJ. The somatostatin receptor in the GI tract. Annu Rev Physiol 1992, 54:455-468. 10.1146/annurev.ph.54.030192.002323, 1348612.
60. Rossowski WJ, Gu ZF, Akarca US, Jensen RT, Coy DH. Characterization of somatostatin receptor subtypes controlling rat gastric acid and pancreatic amylase release. Peptides 1994, 15(8):1421-1424. 10.1016/0196-9781(94)90118-X, 7535424.
61. Bousquet C, Puente E, Buscail L, Vaysse N, Susini C. Antiproliferative effect of somatostatin and analogs. Chemotherapy 2001, 47(Suppl 2):30-39. 10.1159/000049159, 11275700.
62. van Hemert S, Hoekman AJ, Smits MA, Rebel JM. Immunological and gene expression responses to a Salmonella infection in the chicken intestine. Vet Res 2007, 38(1):51-63. 10.1051/vetres:2006048, 17156737.
63. Vreugdenhil GR, Wijnands PG, Netea MG, van der Meer JW, Melchers WJ, Galama JM. Enterovirus-induced production of pro-inflammatory and T-helper cytokines by human leukocytes. Cytokine 2000, 12(12):1793-1796. 10.1006/cyto.2000.0786, 11097750.
64. Bertilsson PM, Olsson P, Magnusson KE. Cytokines influence mRNA expression of cytochrome P450 3A4 and MDRI in intestinal cells. J Pharm Sci 2001, 90(5):638-646. 10.1002/1520-6017(200105)90:5<638::AID-JPS1020>3.0.CO;2-L, 11288108.
65. Gewirtz AT, Rao AS, Simon PO, Merlin D, Carnes D, Madara JL, Neish AS. Salmonella typhimurium induces epithelial IL-8 expression via Ca(2+)-mediated activation of the NF-kappaB pathway. J Clin Invest 2000, 105(1):79-92. 10.1172/JCI8066, 382586, 10619864.
66. Hobbie S, Chen LM, Davis RJ, Galan JE. Involvement of mitogen-activated protein kinase pathways in the nuclear responses and cytokine production induced by Salmonella typhimurium in cultured intestinal epithelial cells. J Immunol 1997, 159(11):5550-5559.
67. Neish AS, Gewirtz AT, Zeng H, Young AN, Hobert ME, Karmali V, Rao AS, Madara JL. Prokaryotic regulation of epithelial responses by inhibition of IkappaB-alpha ubiquitination. Science 2000, 289(5484):1560-1563. 10.1126/science.289.5484.1560, 10968793.
68. Barnes PJ, Adcock IM. Glucocorticoid resistance in inflammatory diseases. Lancet 2009, 373(9678):1905-1917. 10.1016/S0140-6736(09)60326-3, 19482216.
69. McAuley JL, Linden SK, Png CW, King RM, Pennington HL, Gendler SJ, Florin TH, Hill GR, Korolik V, McGuckin MA. MUC1 cell surface mucin is a critical element of the mucosal barrier to infection. J Clin Invest 2007, 117(8):2313-2324. 10.1172/JCI26705, 1913485, 17641781.
70. Ray P, Krishnamoorthy N, Ray A. Emerging functions of c-kit and its ligand stem cell factor in dendritic cells: regulators of T cell differentiation. Cell Cycle 2008, 7(18):2826-2832.
71. Ali S. Role of c-kit/SCF in cause and treatment of gastrointestinal stromal tumors (GIST). Gene 2007, 401(1-2):38-45. 10.1016/j.gene.2007.06.017, 17659849.
72. Restuccia DF, Hemmings BA. Cell signaling. Blocking Akt-ivity. Science 2009, 325(5944):1083-1084. 10.1126/science.1179972, 19713516.
73. 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(10):1815-1823. 10.1172/JCI2466, 509131, 9819367.
74. Jones RM, Wu H, Wentworth C, Luo L, Collier-Hyams L, Neish AS. Salmonella AvrA Coordinates Suppression of Host Immune and Apoptotic Defenses via JNK Pathway Blockade. Cell Host Microbe 2008, 3(4):233-244. 10.1016/j.chom.2008.02.016, 18407067.
75. Steele-Mortimer O, Knodler LA, Marcus SL, Scheid MP, Goh B, Pfeifer CG, Duronio V, Finlay BB. Activation of Akt/protein kinase B in epithelial cells by the Salmonella typhimurium effector sigD. J Biol Chem 2000, 275(48):37718-37724. 10.1074/jbc.M008187200, 10978351.
76. Knodler LA, Finlay BB, Steele-Mortimer O. The Salmonella effector protein SopB protects epithelial cells from apoptosis by sustained activation of Akt. J Biol Chem 2005, 280(10):9058-9064. 10.1074/jbc.M412588200, 15642738.
77. Galan JE, Pace J, Hayman MJ. Involvement of the epidermal growth factor receptor in the invasion of cultured mammalian cells by Salmonella typhimurium. Nature 1992, 357(6379):588-589. 10.1038/357588a0, 1608468.
78. Oda K, Matsuoka Y, Funahashi A, Kitano H. A comprehensive pathway map of epidermal growth factor receptor signaling. Mol Syst Biol 2005, 1. 2005 0010, 10.1038/msb4100014, 1681468, 16729045.
79. Bertelsen LS, Paesold G, Marcus SL, Finlay BB, Eckmann L, Barrett KE. Modulation of chloride secretory responses and barrier function of intestinal epithelial cells by the Salmonella effector protein SigD. Am J Physiol Cell Physiol 2004, 287(4):C939-948. 10.1152/ajpcell.00413.2003, 15175224.
80. Nilsson R, Bajic VB, Suzuki H, di Bernardo D, Bjorkegren J, Katayama S, Reid JF, Sweet MJ, Gariboldi M, Carninci P, et al. Transcriptional network dynamics in macrophage activation. Genomics 2006, 88(2):133-142. 10.1016/j.ygeno.2006.03.022, 16698233.
81. Takaya A, Tomoyasu T, Matsui H, Yamamoto T. The DnaK/DnaJ chaperone machinery of Salmonella enterica serovar Typhimurium is essential for invasion of epithelial cells and survival within macrophages, leading to systemic infection. Infect Immun 2004, 72(3):1364-1373. 10.1128/IAI.72.3.1364-1373.2004, 356005, 14977940.
82. Bernal-Bayard J, Cardenal-Munoz E, Ramos-Morales F. The Salmonella type III secretion effector, salmonella leucine-rich repeat protein (SlrP), targets the human chaperone ERdj3. J Biol Chem 285(21):16360-16368. 10.1074/jbc.M110.100669, 20335166.
83. Sun SC, Ganchi PA, Ballard DW, Greene WC. NF-kappa B controls expression of inhibitor I kappa B alpha: evidence for an inducible autoregulatory pathway. Science 1993, 259(5103):1912-1915. 10.1126/science.8096091, 8096091.
84. Totzke G, Essmann F, Pohlmann S, Lindenblatt C, Janicke RU, Schulze-Osthoff K. A novel member of the IkappaB family, human IkappaB-zeta, inhibits transactivation of p65 and its DNA binding. J Biol Chem 2006, 281(18):12645-12654. 10.1074/jbc.M511956200, 16513645.
85. Khan S, Malik F, Suri KA, Singh J. Molecular insight into the immune up-regulatory properties of the leaf extract of Ashwagandha and identification of Th1 immunostimulatory chemical entity. Vaccine 2009, 27(43):6080-6087. 10.1016/j.vaccine.2009.07.011, 19628058.
86. Bao S, Beagley KW, France MP, Shen J, Husband AJ. Interferon-gamma plays a critical role in intestinal immunity against Salmonella typhimurium infection. Immunology 2000, 99(3):464-472. 10.1046/j.1365-2567.2000.00955.x, 2327174, 10712678.
87. Singh SR, Liu W, Hou SX. The adult Drosophila malpighian tubules are maintained by multipotent stem cells. Cell Stem Cell 2007, 1(2):191-203. 10.1016/j.stem.2007.07.003, 2040309, 18371350.
88. Rodenburg W, Bovee-Oudenhoven IM, Kramer E, van der Meer R, Keijer J. Gene expression response of the rat small intestine following oral Salmonella infection. Physiol Genomics 2007, 30(2):123-133. 10.1152/physiolgenomics.00190.2006, 17374845.
89. Uthaiah RC, Praefcke GJ, Howard JC, Herrmann C. IIGP1, an interferon-gamma-inducible 47-kDa GTPase of the mouse, showing cooperative enzymatic activity and GTP-dependent multimerization. J Biol Chem 2003, 278(31):29336-29343. 10.1074/jbc.M211973200, 12732635.
90. Locksley RM, Killeen N, Lenardo MJ. The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell 2001, 104(4):487-501. 10.1016/S0092-8674(01)00237-9, 11239407.
91. Gaur U, Aggarwal BB. Regulation of proliferation, survival and apoptosis by members of the TNF superfamily. Biochem Pharmacol 2003, 66(8):1403-1408. 10.1016/S0006-2952(03)00490-8, 14555214.
92. Degrandi D, Konermann C, Beuter-Gunia C, Kresse A, Wurthner J, Kurig S, Beer S, Pfeffer K. Extensive characterization of IFN-induced GTPases mGBP1 to mGBP10 involved in host defense. J Immunol 2007, 179(11):7729-7740.
93. Clare S, Goldin R, Hale C, Aspinall R, Simmons C, Mastroeni P, Dougan G. Intracellular adhesion molecule 1 plays a key role in acquired immunity to salmonellosis. Infect Immun 2003, 71(10):5881-5891. 10.1128/IAI.71.10.5881-5891.2003, 201057, 14500509.
94. Arnold JW, Niesel DW, Annable CR, Hess CB, Asuncion M, Cho YJ, Peterson JW, Klimpel GR. Tumor necrosis factor-alpha mediates the early pathology in Salmonella infection of the gastrointestinal tract. Microb Pathog 1993, 14(3):217-227. 10.1006/mpat.1993.1021, 8321123.
95. Demoulin JB, Renauld JC. Interleukin 9 and its receptor: an overview of structure and function. Int Rev Immunol 1998, 16(3-4):345-364. 10.3109/08830189809043001, 9505195.
96. Levitt RC, McLane MP, MacDonald D, Ferrante V, Weiss C, Zhou T, Holroyd KJ, Nicolaides NC. IL-9 pathway in asthma: new therapeutic targets for allergic inflammatory disorders. J Allergy Clin Immunol 1999, 103(5 Pt 2):S485-491. 10.1016/S0091-6749(99)70165-X, 10329852.
97. Nelms K, Keegan AD, Zamorano J, Ryan JJ, Paul WE. The IL-4 receptor: signaling mechanisms and biologic functions. Annu Rev Immunol 1999, 17:701-738. 10.1146/annurev.immunol.17.1.701, 10358772.
98. Polinska B, Matowicka-Karna J, Kemona H. [The cytokines in inflammatory bowel disease]. Postepy Hig Med Dosw (Online) 2009, 63:389-394.
99. Sanchez-Munoz F, Dominguez-Lopez A, Yamamoto-Furusho JK. Role of cytokines in inflammatory bowel disease. World J Gastroenterol 2008, 14(27):4280-4288. 10.3748/wjg.14.4280, 2731177, 18666314.
100. Giallourakis C, Kashiwada M, Pan PY, Danial N, Jiang H, Cambier J, Coggeshall KM, Rothman P. Positive regulation of interleukin-4-mediated proliferation by the SH2-containing inositol-5'-phosphatase. J Biol Chem 2000, 275(38):29275-29282. 10.1074/jbc.M002853200, 10875931.
101. Jiang H, Harris MB, Rothman P. IL-4/IL-13 signaling beyond JAK/STAT. J Allergy Clin Immunol 2000, 105(6 Pt 1):1063-1070. 10.1067/mai.2000.107604, 10856136.
102. Knoops L, Renauld JC. IL-9 and its receptor: from signal transduction to tumorigenesis. Growth Factors 2004, 22(4):207-215. 10.1080/08977190410001720879, 15621723.
103. Gingras S, Cote S, Simard J. Multiple signal transduction pathways mediate interleukin-4-induced 3beta-hydroxysteroid dehydrogenase/Delta5-Delta4 isomerase in normal and tumoral target tissues. J Steroid Biochem Mol Biol 2001, 76(1-5):213-225. 10.1016/S0960-0760(00)00148-5, 11384880.
104. Wurster AL, Withers DJ, Uchida T, White MF, Grusby MJ. Stat6 and IRS-2 cooperate in interleukin 4 (IL-4)-induced proliferation and differentiation but are dispensable for IL-4-dependent rescue from apoptosis. Mol Cell Biol 2002, 22(1):117-126. 10.1128/MCB.22.1.117-126.2002, 134231, 11739727.
105. Kroeger KM, Sullivan BM, Locksley RM. IL-18 and IL-33 elicit Th2 cytokines from basophils via a MyD88- and p38alpha-dependent pathway. J Leukoc Biol 2009, 86(4):769-778. 10.1189/jlb.0708452, 2752018, 19451398.
106. Coffman RL. Immunology. The origin of TH2 responses. Science 328(5982):1116-1117. 10.1126/science.1192009, 20508120.
107. Paul WE, Zhu J. How are T(H)2-type immune responses initiated and amplified?. Nat Rev Immunol 10(4):225-235. 10.1038/nri2735, 20336151.
108. Agaisse H, Perrimon N. The roles of JAK/STAT signaling in Drosophila immune responses. Immunol Rev 2004, 198:72-82. 10.1111/j.0105-2896.2004.0133.x, 15199955.
109. Galiana-Arnoux D, Deddouche S, Imler JL. [Antiviral immunity in drosophila]. J Soc Biol 2007, 201(4):359-365. 10.1051/jbio:2007906, 18533096.
110. Cronin SJ, Nehme NT, Limmer S, Liegeois S, Pospisilik JA, Schramek D, Leibbrandt A, Simoes Rde M, Gruber S, Puc U, et al. Genome-wide RNAi screen identifies genes involved in intestinal pathogenic bacterial infection. Science 2009, 325(5938):340-343. 10.1126/science.1173164, 2975362, 19520911.
111. Mudter J, Neurath MF. The role of signal transducers and activators of transcription in T inflammatory bowel diseases. Inflamm Bowel Dis 2003, 9(5):332-337. 10.1097/00054725-200309000-00008, 14555918.