The role of innate immunity in the host defense against intestinal bacterial pathogens

Current Infectious Disease Reports

Volumn 14, Issue 1, 2012, Pages 15-23

  Sotolongo, John ^a   Ruiz, Jose ^a   Fukata, Masayuki ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

Antimicrobial peptide; Bacterial pathogens; Commensals; Enteropathogen; Gram negative; Host defense; Innate immunity; Macrophages; Mucosal defense; Nod like receptors; Protective immunity; Secretory IgA; Toll like receptors

Indexed keywords

ANTIBIOTIC AGENT; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; POLYPEPTIDE ANTIBIOTIC AGENT; SECRETORY IMMUNOGLOBULIN; TOLL LIKE RECEPTOR;

ANTIBIOTIC RESISTANCE; BACTERIAL COLONIZATION; BACTERIAL INFECTION; BACTERIAL VIRULENCE; BACTERICIDAL ACTIVITY; BACTERIUM CARRIER; CITROBACTER RODENTIUM; DISEASE MODEL; FOOD CONTAMINATION; HELICOBACTER HEPATICUS; HELICOBACTER INFECTION; HOST PATHOGEN INTERACTION; HOST RESISTANCE; HUMAN; IMMUNOREGULATION; IMMUNOSURVEILLANCE; INFLAMMATION; INNATE IMMUNITY; INNATE LYMPHOID CELL; INTESTINE INFECTION; INTRACELLULAR SIGNALING; LYMPHOID CELL; MOLECULAR RECOGNITION; MUCOSAL IMMUNITY; NATURAL KILLER CELL; NONHUMAN; PHAGOCYTOSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SALMONELLA TYPHIMURIUM; SALMONELLOSIS; YERSINIOSIS;

EID: 84857639945     PISSN: 15233847     EISSN: 15343146     Source Type: Journal    
DOI: 10.1007/s11908-011-0234-4     Document Type: Review

References (85)

1. M Helms P Vastrup P Gerner-Smidt K Molbak 2003 Short and long term mortality associated with foodborne bacterial gastrointestinal infections: registry based study BMJ 326 357 12586666 10.1136/bmj.326.7385.357
2. EL Yee H Palacio RL Atmar U Shah C Kilborn M Faul, et al. 2007 Widespread outbreak of norovirus gastroenteritis among evacuees of Hurricane Katrina residing in a large "megashelter" in Houston, Texas: lessons learned for prevention Clin Infect Dis 44 1032 1039 17366445 10.1086/512195 (Pubitemid 46580268)
3. DA Walton LC Ivers 2011 Responding to cholera in post-earthquake Haiti N Engl J Med 364 3 5 21142690 1:CAS:528:DC%2BC3MXisVantA%3D%3D 10.1056/NEJMp1012997
4. J Zarocostas 2011 Experts urge vaccination to try to control cholera outbreak in Haiti BMJ 342 d23 21209068 10.1136/bmj.d23
5. F Niedergang A Didierlaurent JP Kraehenbuhl JC Sirard 2004 Dendritic cells: the host Achille's heel for mucosal pathogens? Trends Microbiol 12 79 88 15036324 1:CAS:528:DC%2BD2cXpsVOisg%3D%3D 10.1016/j.tim.2003.12.011 (Pubitemid 38167342)
6. EA Miao SI Miller 1999 Bacteriophages in the evolution of pathogen-host interactions Proc Natl Acad Sci U S A 96 9452 9454 10449711 1:CAS:528: DyaK1MXlsVynu7Y%3D 10.1073/pnas.96.17.9452 (Pubitemid 29398749)
7. IE Brodsky R Medzhitov 2008 Reduced secretion of YopJ by Yersinia limits in vivo cell death but enhances bacterial virulence PLoS Pathog 4 e1000067 18483548 10.1371/journal.ppat.1000067 (Pubitemid 351811527)
8. R Arnold A Jehl T Rattei 2010 Targeting effectors: the molecular recognition of Type III secreted proteins Microbes Infect 12 346 358 20178857 1:CAS:528:DC%2BC3cXkvFKmsL4%3D 10.1016/j.micinf.2010.02.003
9. P Tyrer AR Foxwell AW Cripps MA Apicella JM Kyd 2006 Microbial pattern recognition receptors mediate M-cell uptake of a gram-negative bacterium Infect Immun 74 625 631 16369019 1:CAS:528:DC%2BD28XitlKrug%3D%3D 10.1128/IAI.74.1.625- 631.2006 (Pubitemid 43023118)
10. A Rydstrom MJ Wick 2007 Monocyte recruitment, activation, and function in the gut-associated lymphoid tissue during oral Salmonella infection J Immunol 178 5789 5801 17442963 (Pubitemid 46674376)
11. RM Salazar-Gonzalez JH Niess DJ Zammit R Ravindran A Srinivasan JR Maxwell, et al. 2006 CCR6-mediated dendritic cell activation of pathogen-specific T cells in Peyer's patches Immunity 24 623 632 16713979 1:CAS:528:DC%2BD28XlsFWqt7c%3D 10.1016/j.immuni.2006.02.015 (Pubitemid 43744358)
12. M Rescigno M Urbano B Valzasina M Francolini G Rotta R Bonasio, et al. 2001 Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria Nat Immunol 2 361 367 11276208 1:CAS:528:DC%2BD3MXis1aktbo%3D 10.1038/86373 (Pubitemid 33706348)
13. JH Niess S Brand X Gu L Landsman S Jung BA McCormick, et al. 2005 CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance Science 307 254 258 15653504 1:CAS:528:DC%2BD2MXisVKltQ%3D%3D 10.1126/science.1102901 (Pubitemid 40116240)
14. M Chieppa M Rescigno AY Huang RN Germain 2006 Dynamic imaging of dendritic cell extension into the small bowel lumen in response to epithelial cell TLR engagement J Exp Med 203 2841 2852 17145958 1:CAS:528: DC%2BD2sXjsFaisQ%3D%3D 10.1084/jem.20061884 (Pubitemid 46026162)
15. A Vallon-Eberhard L Landsman N Yogev B Verrier S Jung 2006 Transepithelial pathogen uptake into the small intestinal lamina propria J Immunol 176 2465 2469 16456006 1:CAS:528:DC%2BD28XpvV2rtg%3D%3D (Pubitemid 43201697)
16. S Uematsu MH Jang N Chevrier Z Guo Y Kumagai M Yamamoto, et al. 2006 Detection of pathogenic intestinal bacteria by Toll-like receptor 5 on intestinal CD11c+ lamina propria cells Nat Immunol 7 868 874 16829963 1:CAS:528:DC%2BD28XntVWls7c%3D 10.1038/ni1362 (Pubitemid 44084094)
17. AJ Macpherson T Uhr 2004 Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria Science 303 1662 1665 15016999 1:CAS:528:DC%2BD2cXhvFCntr4%3D 10.1126/science.1091334 (Pubitemid 38338323)
18. S Westphal A Lugering J von Wedel C von Eiff C Maaser T Spahn, et al. 2008 Resistance of chemokine receptor 6-deficient mice to Yersinia enterocolitica infection: evidence of defective M-cell formation in vivo Am J Pathol 172 671 680 18258848 1:CAS:528:DC%2BD1cXktVKhurY%3D 10.2353/ajpath.2008. 070393 (Pubitemid 351354540)
19. S Voedisch C Koenecke S David H Herbrand R Forster M Rhen, et al. 2009 Mesenteric lymph nodes confine dendritic cell-mediated dissemination of Salmonella enterica serovar Typhimurium and limit systemic disease in mice Infect Immun 77 3170 3180 19506012 1:CAS:528:DC%2BD1MXpsFCmtbw%3D 10.1128/IAI.00272-09
20. M Fukata KS Michelsen R Eri LS Thomas B Hu K Lukasek, et al. 2005 Toll-like receptor-4 is required for intestinal response to epithelial injury and limiting bacterial translocation in a murine model of acute colitis Am J Physiol Gastrointest Liver Physiol 288 G1055 G1065 15826931 1:CAS:528: DC%2BD2MXktlSntr4%3D 10.1152/ajpgi.00328.2004 (Pubitemid 40563149)
21. B Coburn GA Grassl BB Finlay 2007 Salmonella, the host and disease: a brief review Immunol Cell Biol 85 112 118 17146467 10.1038/sj.icb.7100007 (Pubitemid 46398718)
22. S Hapfelmeier WD Hardt 2005 A mouse model for S. typhimurium-induced enterocolitis Trends Microbiol 13 497 503 16140013 1:CAS:528:DC%2BD2MXhtVWnsLvO 10.1016/j.tim.2005.08.008 (Pubitemid 41317528)
23. J Heesemann K Gaede IB Autenrieth 1993 Experimental Yersinia enterocolitica infection in rodents: a model for human yersiniosis APMIS 101 417 429 8363822 1:STN:280:DyaK3szntFyisg%3D%3D 10.1111/j.1699-0463.1993.tb00130.x (Pubitemid 23255821)
24. R Mundy TT MacDonald G Dougan G Frankel S Wiles 2005 Citrobacter rodentium of mice and man Cell Microbiol 7 1697 1706 16309456 1:CAS:528:DC%2BD2MXht12ntLzK 10.1111/j.1462-5822.2005.00625.x (Pubitemid 41685263)
25. D Borenshtein ME McBee DB Schauer 2008 Utility of the Citrobacter rodentium infection model in laboratory mice Curr Opin Gastroenterol 24 32 37 18043230 10.1097/MOG.0b013e3282f2b0fb (Pubitemid 350190895)
26. JG Fox Z Ge MT Whary SE Erdman BH Horwitz 2011 Helicobacter hepaticus infection in mice: models for understanding lower bowel inflammation and cancer Mucosal Immunol 4 22 30 20944559 1:CAS:528:DC%2BC3cXhs1ejtb3F 10.1038/mi.2010.61
27. KJ Maloy L Salaun R Cahill G Dougan NJ Saunders F Powrie 2003 CD4+CD25+ T(R) cells suppress innate immune pathology through cytokine-dependent mechanisms J Exp Med 197 111 119 12515818 1:CAS:528:DC%2BD3sXjslWltg%3D%3D 10.1084/jem.20021345 (Pubitemid 36110262)
28. G Melmed LS Thomas N Lee SY Tesfay K Lukasek KS Michelsen, et al. 2003 Human intestinal epithelial cells are broadly unresponsive to Toll-like receptor 2-dependent bacterial ligands: implications for host-microbial interactions in the gut J Immunol 170 1406 1415 12538701 1:CAS:528:DC%2BD3sXnvVOktg%3D%3D (Pubitemid 36139508)
29. JM Otte E Cario DK Podolsky 2004 Mechanisms of cross hyporesponsiveness to Toll-like receptor bacterial ligands in intestinal epithelial cells Gastroenterology 126 1054 1070 15057745 1:CAS:528:DC%2BD2cXkt1Krtrs%3D 10.1053/j.gastro.2004.01.007 (Pubitemid 38451177)
30. LE Smythies M Sellers RH Clements M Mosteller-Barnum G Meng WH Benjamin, et al. 2005 Human intestinal macrophages display profound inflammatory anergy despite avid phagocytic and bacteriocidal activity J Clin Invest 115 66 75 15630445 1:CAS:528:DC%2BD2MXis1eksQ%3D%3D (Pubitemid 40385506)
31. DS Weiss B Raupach K Takeda S Akira A Zychlinsky 2004 Toll-like receptors are temporally involved in host defense J Immunol 172 4463 4469 15034062 1:CAS:528:DC%2BD2cXitlOqtL8%3D (Pubitemid 38375262)
32. A Vazquez-Torres BA Vallance MA Bergman BB Finlay BT Cookson J Jones-Carson, et al. 2004 Toll-like receptor 4 dependence of innate and adaptive immunity to Salmonella: importance of the Kupffer cell network J Immunol 172 6202 6208 15128808 1:CAS:528:DC%2BD2cXjs1Oju70%3D (Pubitemid 38621226)
33. A Sing N Tvardovskaia D Rost CJ Kirschning H Wagner J Heesemann 2003 Contribution of toll-like receptors 2 and 4 in an oral Yersinia enterocolitica mouse infection model Int J Med Microbiol 293 341 348 14695062 1:CAS:528:DC%2BD2cXht1aktLs%3D 10.1078/1438-4221-00277 (Pubitemid 37516675)
34. L Franchi A Amer M Body-Malapel TD Kanneganti N Ozoren R Jagirdar, et al. 2006 Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1beta in salmonella-infected macrophages Nat Immunol 7 576 582 16648852 1:CAS:528:DC%2BD28Xksleksbk%3D 10.1038/ni1346 (Pubitemid 43797338)
35. S Mariathasan K Newton DM Monack D Vucic DM French WP Lee, et al. 2004 Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf Nature 430 213 218 15190255 1:CAS:528:DC%2BD2cXlsVGjsrk%3D 10.1038/nature02664 (Pubitemid 38902430)
36. EA Miao CM Alpuche-Aranda M Dors AE Clark MW Bader SI Miller, et al. 2006 Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf Nat Immunol 7 569 575 16648853 1:CAS:528:DC%2BD28Xksleksbs%3D 10.1038/ni1344 (Pubitemid 43797337)
37. M Lara-Tejero FS Sutterwala Y Ogura EP Grant J Bertin AJ Coyle, et al. 2006 Role of the caspase-1 inflammasome in Salmonella typhimurium pathogenesis J Exp Med 203 1407 1412 16717117 1:CAS:528:DC%2BD28XmtVansbw%3D 10.1084/jem.20060206 (Pubitemid 43877602)
38. B Raupach SK Peuschel DM Monack A Zychlinsky 2006 Caspase-1-mediated activation of interleukin-1beta (IL-1beta) and IL-18 contributes to innate immune defenses against Salmonella enterica serovar Typhimurium infection Infect Immun 74 4922 4926 16861683 1:CAS:528:DC%2BD28XnvFWqtrs%3D 10.1128/IAI.00417-06 (Pubitemid 44157282)
39. N Arpaia J Godec L Lau KE Sivick LM McLaughlin MB Jones, et al. 2011 TLR signaling is required for Salmonella typhimurium virulence Cell. 144 675 88 21376231 1:CAS:528:DC%2BC3MXjsFeqtrY%3D 10.1016/j.cell.2011.01.031 This article nicely shows how TLR signaling forms host-pathogen interactions during S. typhimurium infection. Certain TLR signaling contributes to host effector immunity, but other TLR signaling may be used as virulence effector of the pathogen.
40. MA Khan C Ma LA Knodler Y Valdez CM Rosenberger W Deng, et al. 2006 Toll-like receptor 4 contributes to colitis development but not to host defense during Citrobacter rodentium infection in mice Infect Immun 74 2522 2536 16622187 1:CAS:528:DC%2BD28XksFagt7g%3D 10.1128/IAI.74.5.2522-2536.2006 (Pubitemid 43672959)
41. MJ Asquith O Boulard F Powrie KJ Maloy 2010 Pathogenic and protective roles of MyD88 in leukocytes and epithelial cells in mouse models of inflammatory bowel disease Gastroenterology 139 519 529 20433840 1:CAS:528:DC%2BC3cXpsVGmsr8%3D 10.1053/j.gastro.2010.04.045 This study shows distinct contributions of TLR signaling by cell type in induction of intestinal inflammation. MyD88 signaling in myeloid cells is responsible for induction of innate inflammation in the intestine.
42. ME Lamm 1997 Interaction of antigens and antibodies at mucosal surfaces Annu Rev Microbiol 51 311 340 9343353 1:CAS:528:DyaK2sXms1Shtr4%3D 10.1146/annurev.micro.51.1.311 (Pubitemid 27433052)
43. S Shimada M Kawaguchi-Miyashita A Kushiro T Sato M Nanno T Sako, et al. 1999 Generation of polymeric immunoglobulin receptor-deficient mouse with marked reduction of secretory IgA J Immunol 163 5367 5373 10553061 1:CAS:528:DyaK1MXntlKrsLk%3D
44. AJ Ouellette 2011 Paneth cell alpha-defensins in enteric innate immunity Cell Mol Life Sci 68 2215 2229 21560070 1:CAS:528:DC%2BC3MXntlajur0%3D 10.1007/s00018-011-0714-6
45. KE Shroff K Meslin JJ Cebra 1995 Commensal enteric bacteria engender a self-limiting humoral mucosal immune response while permanently colonizing the gut Infect Immun 63 3904 3913 7558298 1:CAS:528:DyaK2MXotlahsLw%3D
46. P Brandtzaeg FE Johansen 2005 Mucosal B cells: phenotypic characteristics, transcriptional regulation, and homing properties Immunol Rev 206 32 63 16048541 1:CAS:528:DC%2BD2MXhtVWjsb7E 10.1111/j.0105-2896.2005.00283.x (Pubitemid 41105162)
47. P Sundstrom SB Lundin LA Nilsson M Quiding-Jarbrink 2008 Human IgA-secreting cells induced by intestinal, but not systemic, immunization respond to CCL25 (TECK) and CCL28 (MEC) Eur J Immunol 38 3327 3338 19003934 10.1002/eji.200838506
48. M Hahne T Kataoka M Schroter K Hofmann M Irmler JL Bodmer, et al. 1998 APRIL, a new ligand of the tumor necrosis factor family, stimulates tumor cell growth J Exp Med 188 1185 1190 9743536 1:CAS:528:DyaK1cXmsVKitLg%3D 10.1084/jem.188.6.1185 (Pubitemid 28443341)
49. F Mackay P Schneider P Rennert J Browning 2003 BAFF AND APRIL: a tutorial on B cell survival Annu Rev Immunol 21 231 264 12427767 1:CAS:528: DC%2BD3sXjtF2isr0%3D 10.1146/annurev.immunol.21.120601.141152 (Pubitemid 37174532)
50. MB Litinskiy B Nardelli DM Hilbert B He A Schaffer P Casali, et al. 2002 DCs induce CD40-independent immunoglobulin class switching through BLyS and APRIL Nat Immunol 3 822 829 12154359 1:CAS:528:DC%2BD38Xms1ags7s%3D 10.1038/ni829
51. B He W Xu PA Santini AD Polydorides A Chiu J Estrella, et al. 2007 Intestinal bacteria trigger T cell-independent immunoglobulin A(2) class switching by inducing epithelial-cell secretion of the cytokine APRIL Immunity 26 812 826 17570691 1:CAS:528:DC%2BD2sXntlKnu70%3D 10.1016/j.immuni.2007.04.014 (Pubitemid 46915505)
52. JP Bouvet G Dighiero 1998 From natural polyreactive autoantibodies to a la carte monoreactive antibodies to infectious agents: is it a small world after all? Infect Immun 66 1 4 9423831 1:CAS:528:DyaK1cXnsl2k
53. AL Notkins 2004 Polyreactivity of antibody molecules Trends Immunol 25 174 179 15039043 1:CAS:528:DC%2BD2cXisVarsr0%3D 10.1016/j.it.2004.02.004 (Pubitemid 38368164)
54. L Shang M Fukata N Thirunarayanan AP Martin P Arnaboldi D Maussang, et al. 2008 Toll-like receptor signaling in small intestinal epithelium promotes B-cell recruitment and IgA production in lamina propria Gastroenterology 135 529 538 18522803 1:CAS:528:DC%2BD1cXhtVCqsLzO 10.1053/j.gastro.2008.04.020
55. ME Bruno EW Rogier AL Frantz AT Stefka SN Thompson CS Kaetzel 2010 Regulation of the polymeric immunoglobulin receptor in intestinal epithelial cells by Enterobacteriaceae: implications for mucosal homeostasis Immunol Invest 39 356 382 20450283 1:CAS:528:DC%2BC3cXlslegur0%3D 10.3109/08820131003622809
56. TA Schneeman ME Bruno H Schjerven FE Johansen L Chady CS Kaetzel 2005 Regulation of the polymeric Ig receptor by signaling through TLRs 3 and 4: linking innate and adaptive immune responses J Immunol 175 376 384 15972671 1:CAS:528:DC%2BD2MXltlynu7Y%3D (Pubitemid 40884341)
57. OL Wijburg TK Uren K Simpfendorfer FE Johansen P Brandtzaeg RA Strugnell 2006 Innate secretory antibodies protect against natural Salmonella typhimurium infection J Exp Med 203 21 26 16390940 1:CAS:528:DC%2BD28XhtVyrur8%3D 10.1084/jem.20052093 (Pubitemid 43139640)
58. T Ganz 2003 Defensins: antimicrobial peptides of innate immunity Nat Rev Immunol 3 710 720 12949495 1:CAS:528:DC%2BD3sXmvVWmtLc%3D 10.1038/nri1180 (Pubitemid 41070812)
59. CL Wilson AJ Ouellette DP Satchell T Ayabe YS Lopez-Boado JL Stratman, et al. 1999 Regulation of intestinal alpha-defensin activation by the metalloproteinase matrilysin in innate host defense Science 286 113 117 10506557 1:CAS:528:DyaK1MXmsFehurc%3D 10.1126/science.286.5437.113 (Pubitemid 29484488)
60. NH Salzman D Ghosh KM Huttner Y Paterson CL Bevins 2003 Protection against enteric salmonellosis in transgenic mice expressing a human intestinal defensin Nature 422 522 526 12660734 1:CAS:528:DC%2BD3sXisFCisrs%3D 10.1038/nature01520 (Pubitemid 36433647)
61. S Vaishnava CL Behrendt AS Ismail L Eckmann LV Hooper 2008 Paneth cells directly sense gut commensals and maintain homeostasis at the intestinal host-microbial interface Proc Natl Acad Sci U S A 105 20858 20863 19075245 1:CAS:528:DC%2BD1MXksFSntQ%3D%3D 10.1073/pnas.0808723105
62. KS Kobayashi M Chamaillard Y Ogura O Henegariu N Inohara G Nunez, et al. 2005 Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract Science 307 731 734 15692051 1:CAS:528:DC%2BD2MXpt1Wqtw%3D%3D 10.1126/science.1104911 (Pubitemid 40194644)
63. J Lee JH Mo K Katakura I Alkalay AN Rucker YT Liu, et al. 2006 Maintenance of colonic homeostasis by distinctive apical TLR9 signalling in intestinal epithelial cells Nat Cell Biol 8 1327 1336 17128265 1:CAS:528:DC%2BD28Xht1Kju7rM 10.1038/ncb1500 (Pubitemid 44835107)
64. T Hisamatsu M Suzuki HC Reinecker WJ Nadeau BA McCormick DK Podolsky 2003 CARD15/NOD2 functions as an antibacterial factor in human intestinal epithelial cells Gastroenterology 124 993 1000 12671896 1:CAS:528:DC%2BD3sXjsFOju7g%3D 10.1053/gast.2003.50153 (Pubitemid 36389802)
65. T Petnicki-Ocwieja T Hrncir YJ Liu A Biswas T Hudcovic H Tlaskalova-Hogenova, et al. 2009 Nod2 is required for the regulation of commensal microbiota in the intestine Proc Natl Acad Sci U S A 106 15813 15818 19805227 1:CAS:528:DC%2BD1MXhtFyjsLfN 10.1073/pnas.0907722106
66. A Uehara Y Fujimoto K Fukase H Takada 2007 Various human epithelial cells express functional Toll-like receptors, NOD1 and NOD2 to produce anti-microbial peptides, but not proinflammatory cytokines Mol Immunol 44 3100 3111 17403538 1:CAS:528:DC%2BD2sXksVejurk%3D 10.1016/j.molimm.2007.02.007 (Pubitemid 46610510)
67. P Vora A Youdim LS Thomas M Fukata SY Tesfay K Lukasek, et al. 2004 Beta-defensin-2 expression is regulated by TLR signaling in intestinal epithelial cells J Immunol 173 5398 5405 15494486 1:CAS:528:DC%2BD2cXos1Giur0%3D (Pubitemid 39392123)
68. JM Blander R Medzhitov 2004 Regulation of phagosome maturation by signals from toll-like receptors Science 304 1014 1018 15143282 1:CAS:528: DC%2BD2cXjvVCgsrg%3D 10.1126/science.1096158 (Pubitemid 38638100)
69. JM Blander R Medzhitov 2006 Toll-dependent selection of microbial antigens for presentation by dendritic cells Nature 440 808 812 16489357 1:CAS:528:DC%2BD28XjtFKjsLo%3D 10.1038/nature04596
70. L Kong L Sun H Zhang Q Liu Y Liu L Qin, et al. 2009 An essential role for RIG-I in toll-like receptor-stimulated phagocytosis Cell Host Microbe 6 150 161 19683681 1:CAS:528:DC%2BD1MXhtFyhsb3I 10.1016/j.chom.2009.06.008
71. CM Rosenberger BB Finlay 2003 Phagocyte sabotage: disruption of macrophage signalling by bacterial pathogens Nat Rev Mol Cell Biol 4 385 396 12728272 1:CAS:528:DC%2BD3sXjtlalt7s%3D 10.1038/nrm1104 (Pubitemid 36565570)
72. CE Wong S Sad BK Coombes 2009 Salmonella enterica serovar typhimurium exploits Toll-like receptor signaling during the host-pathogen interaction Infect Immun 77 4750 4760 19720755 1:CAS:528:DC%2BD1MXhtl2itrvP 10.1128/IAI.00545-09
73. JP Di Santo 2008 Functionally distinct NK-cell subsets: developmental origins and biological implications Eur J Immunol 38 2948 2951 18979515 10.1002/eji.200838830
74. AA Ashkar S Reid EF Verdu K Zhang BK Coombes 2009 Interleukin-15 and NK1.1+ cells provide innate protection against acute Salmonella enterica serovar Typhimurium infection in the gut and in systemic tissues Infect Immun 77 214 22 19015253 1:CAS:528:DC%2BD1MXhs1Sis74%3D 10.1128/IAI.01066-08
75. L Harrington CV Srikanth R Antony HN Shi BJ Cherayil 2007 A role for natural killer cells in intestinal inflammation caused by infection with Salmonella enterica serovar Typhimurium FEMS Immunol Med Microbiol 51 372 380 17727655 1:CAS:528:DC%2BD2sXht1aisLjM 10.1111/j.1574-695X.2007.00313.x (Pubitemid 47547511)
76. A Reynders N Yessaad TP Vu Manh M Dalod A Fenis C Aubry, et al. 2011 Identity, regulation and in vivo function of gut NKp46+RORgammat+ and NKp46+RORgammat- lymphoid cells EMBO J 30 2934 2947 21685873 1:CAS:528:DC%2BC3MXnslSmt74%3D 10.1038/emboj.2011.201
77. GF Sonnenberg LA Monticelli MM Elloso LA Fouser D Artis 2011 CD4(+) lymphoid tissue-inducer cells promote innate immunity in the gut Immunity 34 122 134 21194981 1:CAS:528:DC%2BC3MXht1Wlu7w%3D 10.1016/j.immuni.2010.12.009
78. M Cella A Fuchs W Vermi F Facchetti K Otero JK Lennerz, et al. 2009 A human natural killer cell subset provides an innate source of IL-22 for mucosal immunity Nature 457 722 725 18978771 1:CAS:528:DC%2BD1MXht1eiu7c%3D 10.1038/nature07537
79. H Mayuzumi K Inagaki-Ohara C Uyttenhove Y Okamoto G Matsuzaki 2010 Interleukin-17A is required to suppress invasion of Salmonella enterica serovar Typhimurium to enteric mucosa Immunology 131 377 385 20575990 1:CAS:528:DC%2BC3cXhtlGlsb7I 10.1111/j.1365-2567.2010.03310.x
80. M Raffatellu RL Santos DE Verhoeven MD George RP Wilson SE Winter, et al. 2008 Simian immunodeficiency virus-induced mucosal interleukin-17 deficiency promotes Salmonella dissemination from the gut Nat Med 14 421 428 18376406 1:CAS:528:DC%2BD1cXktl2isLg%3D 10.1038/nm1743 (Pubitemid 351499394)
81. Y Zheng PA Valdez DM Danilenko Y Hu SM Sa Q Gong, et al. 2008 Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens Nat Med 14 282 289 18264109 1:CAS:528:DC%2BD1cXivFOrtLw%3D 10.1038/nm1720 (Pubitemid 351347912)
82. AC Graham KD Carr AN Sieve M Indramohan TJ Break RE Berg 2011 IL-22 production is regulated by IL-23 during Listeria monocytogenes infection but is not required for bacterial clearance or tissue protection PLoS One 6 e17171 21347242 1:CAS:528:DC%2BC3MXislCnsL4%3D 10.1371/journal.pone.0017171
83. SL Lebeis KR Powell D Merlin MA Sherman D Kalman 2009 Interleukin-1 receptor signaling protects mice from lethal intestinal damage caused by the attaching and effacing pathogen Citrobacter rodentium Infect Immun 77 604 614 19075023 1:CAS:528:DC%2BD1MXhs1Shsrk%3D 10.1128/IAI.00907-08
84. B Guo G Cheng 2007 Modulation of the interferon antiviral response by the TBK1/IKKi adaptor protein TANK J Biol Chem 282 11817 11826 17327220 1:CAS:528:DC%2BD2sXktFemu7Y%3D 10.1074/jbc.M700017200 (Pubitemid 47100710)
85. M Yamamoto S Sato H Hemmi K Hoshino T Kaisho H Sanjo, et al. 2003 Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway Science 301 640 643 12855817 1:CAS:528:DC%2BD3sXlvVKnsLs%3D 10.1126/science. 1087262 (Pubitemid 36927946)