CD3-NK1.1+ cells aid in the early induction of a Th1 response to an attaching and effacing enteric pathogen

European Journal of Immunology

Volumn 43, Issue 10, 2013, Pages 2638-2649

  Reid Yu, Sarah A ^a,b   Small, Cherrie Lee N ^a,b   Coombes, Brian K ^a,b  

^a MCMASTER UNIVERSITY   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

Author keywords

Attaching and effacing pathogen; Citrobacter rodentium; Colitis; Natural killer (NK) cells; T helper cell 1 (Th1) response

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 12; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL LOAD; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CITROBACTER RODENTIUM; CLOSTRIDIUM INFECTION; COLITIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; IMMUNOPATHOGENESIS; INTESTINE CRYPT; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; TH1 CELL;

ATTACHING AND EFFACING PATHOGEN; CITROBACTER RODENTIUM; COLITIS; NATURAL KILLER (NK) CELLS; T HELPER CELL 1 (TH1) RESPONSE;

ANIMALS; ANTIBODIES, BACTERIAL; ANTIGENS, CD3; ANTIGENS, LY; BACTERIAL LOAD; CELL MOVEMENT; CITROBACTER RODENTIUM; COLON; ENTEROBACTERIACEAE INFECTIONS; ESCHERICHIA COLI; FEMALE; HYPERPLASIA; INTERFERON-GAMMA; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; LYMPHOCYTE DEPLETION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY B; TH1 CELLS;

EID: 84885766419     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201343435     Document Type: Article

References (42)

1. Nataro, J. P. and Kaper, J. B., Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 1998. 11: 142-201.
2. Frankel, G., Phillips, A. D., Rosenshine, I., Dougan, G., Kaper, J. B. and Knutton, S., Enteropathogenic and enterohaemorrhagic Escherichia coli: more subversive elements. Mol. Microbiol. 1998. 30: 911-921.
3. Frankel, G., Philips, A. D., Novakova, M., Batchelor, M., Hicks, S. and Dougan, G., Generation of Escherichia coli intimin derivatives with differing biological activities using site-directed mutagenesis of the intimin C-terminus domain. Mol. Microbiol. 1998. 29: 559-570.
4. Clarke, S. C., Haigh, R. D., Freestone, P. P. and Williams, P. H., Virulence of enteropathogenic Escherichia coli, a global pathogen. Clin. Microbiol. Rev. 2003. 16: 365-378.
5. McDaniel, T. K., Jarvis, K. G., Donnenberg, M. S. and Kaper, J. B., A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc. Natl. Acad. Sci. USA 1995. 92: 1664-1668.
6. Petty, N. K., Bulgin, R., Crepin, V. F., Cerdeno-Tarraga, A. M., Schroeder, G. N., Quail, M. A., Lennard, N. et al., The Citrobacter rodentium genome sequence reveals convergent evolution with human pathogenic Escherichia coli. J. Bacteriol. 2010. 192: 525-538.
7. Khan, M. A., Bouzari, S., Ma, C., Rosenberger, C. M., Bergstrom, K. S., Gibson, D. L., Steiner, T. S. and Vallance, B. A., Flagellin-dependent and -independent inflammatory responses following infection by enteropathogenic Escherichia coli and Citrobacter rodentium. Infect. Immun. 2008. 76: 1410-1422.
8. Frankel, G., Lider, O., Hershkoviz, R., Mould, A. P., Kachalsky, S. G., Candy, D. C., Cahalon, L. et al., The cell-binding domain of intimin from enteropathogenic Escherichia coli binds to beta1 integrins. J. Biol. Chem. 1996. 271: 20359-20364.
9. Luperchio, S. A. and Schauer, D. B., Molecular pathogenesis of Citrobacter rodentium and transmissible murine colonic hyperplasia. Microbes Infect. 2001. 3: 333-340.
10. Vallance, B. A., Deng, W., Knodler, L. A. and Finlay, B. B., Mice lacking T and B lymphocytes develop transient colitis and crypt hyperplasia yet suffer impaired bacterial clearance during Citrobacter rodentium infection. Infect. Immun. 2002. 70: 2070-2081.
11. Maaser, C., Housley, M. P., Iimura, M., Smith, J. R., Vallance, B. A., Finlay, B. B., Schreiber, J. R. et al., Clearance of Citrobacter rodentium requires B cells but not secretory immunoglobulin A (IgA) or IgM antibodies. Infect. Immun. 2004. 72: 3315-3324.
12. Simmons, C. P., Clare, S., Ghaem-Maghami, M., Uren, T. K., Rankin, J., Huett, A., Goldin, R. et al., Central role for B lymphocytes and CD4+ T cells in immunity to infection by the attaching and effacing pathogen Citrobacter rodentium. Infect. Immun. 2003. 71: 5077-5086.
13. Lebeis, S. L., Bommarius, B., Parkos, C. A., Sherman, M. A. and Kalman, D., TLR signaling mediated by MyD88 is required for a protective innate immune response by neutrophils to Citrobacter rodentium. J. Immunol. 2007. 179: 566-577.
14. Wei, O. L., Hilliard, A., Kalman, D. and Sherman, M., Mast cells limit systemic bacterial dissemination but not colitis in response to Citrobacter rodentium. Infect. Immun. 2005. 73: 1978-1985.
15. Bry, L. and Brenner, M. B., Critical role of T cell-dependent serum antibody, but not the gut-associated lymphoid tissue, for surviving acute mucosal infection with Citrobacter rodentium, an attaching and effacing pathogen. J. Immunol. 2004. 172: 433-441.
16. Simmons, C. P., Goncalves, N. S., Ghaem-Maghami, M., Bajaj-Elliott, M., Clare, S., Neves, B., Frankel, G. et al., Impaired resistance and enhanced pathology during infection with a noninvasive, attaching-effacing enteric bacterial pathogen, Citrobacter rodentium, in mice lacking IL-12 or IFN-gamma. J. Immunol. 2002. 168: 1804-1812.
17. Satoh-Takayama, N., Dumoutier, L., Lesjean-Pottier, S., Ribeiro, V. S. G., Mandelboim, O., Renauld, J. C., Vosshenrich, C. A. J. et al., The natural cytotoxicity receptor NKp46 is dispensable for IL-22-mediated innate intestinal immune defense against Citrobacter rodentium. J. Immunol. 2009. 183: 6579-6587.
18. Ishigame, H., Kakuta, S., Nagai, T., Kadoki, M., Nambu, A., Komiyama, Y., Fujikado, N. et al., Differential roles of interleukin-17A and-17F in host defense against mucoepithelial bacterial infection and allergic responses. Immunity 2009. 30: 108-119.
19. Shiomi, H., Masuda, A., Nishiumi, S., Nishida, M., Takagawa, T., Shiomi, Y., Kutsumi, H. et al., Gamma interferon produced by antigen-specific CD4+ T cells regulates the mucosal immune responses to Citrobacter rodentium infection. Infect. Immun. 2010. 78: 2653-2666.
20. Martin-Fontecha, A., Thomsen, L. L., Brett, S., Gerard, C., Lipp, M., Lanzavecchia, A. and Sallusto, F., Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nat. Immunol. 2004. 5: 1260-1265.
21. Sanabria, M. X., Vargas-Inchaustegui, D. A., Xin, L. and Soong, L., Role of natural killer cells in modulating dendritic cell responses to Leishmania amazonensis infection. Infect. Immun. 2008. 76: 5100-5109.
22. Zuerner, R. L., Alt, D. P., Palmer, M. V., Thacker, T. C. and Olsen, S. C., A Leptospira borgpetersenii Serovar Hardjo vaccine induces a Th1 response, activates NK cells, and reduces renal colonization. Clin. Vaccine Immunol. 2011. 18: 684-691.
23. Ing, R. and Stevenson, M. M., Dendritic cell and NK cell reciprocal cross talk promotes gamma interferon-dependent immunity to blood-stage Plasmodium chabaudi AS infection in mice. Infect. Immun. 2009. 77: 770-782.
24. Jiao, L., Gao, X., Joyee, A. G., Zhao, L., Qiu, H., Yang, M., Fan, Y. et al., NK cells promote type 1 T cell immunity through modulating the function of dendritic cells during intracellular bacterial infection. J. Immunol. 2011. 187: 401-411.
25. Orange, J. S. and Biron, C. A., Characterization of early IL-12, IFN-alphabeta, and TNF effects on antiviral state and NK cell responses during murine cytomegalovirus infection. J. Immunol. 1996. 156: 4746-4756.
26. Hall, L. J., Murphy, C. T., Hurley, G., Quinlan, A., Shanahan, F., Nally, K. and Melgar, S., Natural killer cells protect against mucosal and systemic infection with the enteric pathogen Citrobacter rodentium. Infect. Immun. 2013. 81: 460-469.
27. Fehniger, T. A., Cooper, M. A., Nuovo, G. J., Cella, M., Facchetti, F., Colonna, M. and Caligiuri, M. A., CD56bright natural killer cells are present in human lymph nodes and are activated by T cell-derived IL-2: a potential new link between adaptive and innate immunity. Blood 2003. 101: 3052-3057.
28. Vonarbourg, C., Mortha, A., Bui, V. L., Hernandez, P. P., Kiss, E. A., Hoyler, T., Flach, M. et al., Regulated expression of nuclear receptor RORgammat confers distinct functional fates to NK cell receptor-expressing RORgammat(+) innate lymphocytes. Immunity 2010. 33: 736-751.
29. Reschner, A., Hubert, P., Delvenne, P., Boniver, J. and Jacobs, N., Innate lymphocyte and dendritic cell cross-talk: a key factor in the regulation of the immune response. Clin. Exp. Immunol. 2008. 152: 219-226.
30. Rot, A. and von Andrian, U. H., Chemokines in innate and adaptive host defense: basic chemokinese grammar for immune cells. Annu. Rev. Immunol. 2004. 22: 891-928.
31. Cole, A. M., Ganz, T., Liese, A. M., Burdick, M. D., Liu, L. and Strieter, R. M., Cutting edge: IFN-inducible ELR- CXC chemokines display defensin-like antimicrobial activity. J. Immunol. 2001. 167: 623-627.
32. Higgins, L. M., Frankel, G., Connerton, I., Goncalves, N. S., Dougan, G. and MacDonald, T. T., Role of bacterial intimin in colonic hyperplasia and inflammation. Science 1999. 285: 588-591.
33. Wiltrout, R. H., Santoni, A., Peterson, E. S., Knott, D. C., Overton, W. R., Herberman, R. B. and Holden, H. T., Reactivity of anti-asialo GM1 serum with tumoricidal and non-tumoricidal mouse macrophages. J. Leukoc. Biol. 1985. 37: 597-614.
34. Klose, C. S., Kiss, E. A., Schwierzeck, V., Ebert, K., Hoyler, T., d'Hargues, Y., Goppert, N. et al., A T-bet gradient controls the fate and function of CCR6-RORgammat+ innate lymphoid cells. Nature 2013. 494: 261-265.
35. Rhee, S. J., Walker, W. A. and Cherayil, B. J., Developmentally regulated intestinal expression of IFN-gamma and its target genes and the age-specific response to enteric Salmonella infection. J. Immunol. 2005. 175: 1127-1136.
36. Hirata, Y., Egea, L., Dann, S. M., Eckmann, L. and Kagnoff, M. F., GM-CSF-facilitated dendritic cell recruitment and survival govern the intestinal mucosal response to a mouse enteric bacterial pathogen. Cell Host Microbe. 2010. 7: 151-163.
37. Satoskar, A. R., Stamm, L. M., Zhang, X., Satoskar, A. A., Okano, M., Terhorst, C., David, J. R. and Wang, B., Mice lacking NK cells develop an efficient Th1 response and control cutaneous Leishmania major infection. J. Immunol. 1999. 162: 6747-6754.
38. Wakil, A. E., Wang, Z. E., Ryan, J. C., Fowell, D. J. and Locksley, R. M., Interferon gamma derived from CD4(+) T cells is sufficient to mediate T helper cell type 1 development. J. Exp. Med. 1998. 188: 1651-1656.
39. Lanzavecchia, A. and Sallusto, F., Dynamics of T lymphocyte responses: intermediates, effectors, and memory cells. Science 2000. 290: 92-97.
40. Coburn, B., Li, Y., Owen, D., Vallance, B. A. and Finlay, B. B., Salmonella enterica serovar Typhimurium pathogenicity island 2 is necessary for complete virulence in a mouse model of infectious enterocolitis. Infect. Immun. 2005. 73: 3219-3227.
41. Saverymuttu, S. H., Camilleri, M., Rees, H., Lavender, J. P., Hodgson, H. J. and Chadwick, V. S., Indium 111-granulocyte scanning in the assessment of disease extent and disease activity in inflammatory bowel disease. A comparison with colonoscopy, histology, and fecal indium 111-granulocyte excretion. Gastroenterology 1986. 90: 1121-1128.
42. Barthel, M., Hapfelmeier, S., Quintanilla-Martinez, L., Kremer, M., Rohde, M., Hogardt, M., Pfeffer, K. et al., Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect. Immun. 2003. 71: 2839-2858.