CCR5 mediates specific migration of Toxoplasma gondii-primed CD8+ lymphocytes to inflammatory intestinal epithelial cells

Gastroenterology

Volumn 125, Issue 2, 2003, Pages 491-500

  Luangsay, Souphalone ^a   Kasper, Lloyd H ^a   Rachinel, Nicolas ^a   Minns, Laurie A ^a   Mennechet, Franck J D ^a   Vandewalle, Alain ^b   Buzoni Gatel, Dominique ^c  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b INSERM   (France)

^c INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; CD8 ANTIGEN; CHEMOKINE; CHEMOKINE RECEPTOR; CHEMOKINE RECEPTOR CCR5; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INVASION; CONTROLLED STUDY; ENTERITIS; FEMALE; HOMEOSTASIS; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATORY CELL; INTESTINE CELL; INTESTINE EPITHELIUM; LYMPHOCYTE MIGRATION; MOUSE; NONHUMAN; PARASITOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMALL INTESTINE; TH1 CELL; TOXOPLASMA GONDII;

EID: 0041665003     PISSN: 00165085     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0016-5085(03)00903-X     Document Type: Article

References (36)

1. Perez de Lema G, Maier H, Nieto E, Vielhauer V, Luckow B, Mampaso F, Schlondorff D. Chemokine expression precedes inflammatory cell infiltration and chemokine receptor and cytokine expression during the initiation of murine lupus nephritis. J Am Soc Nephrol 2001;12:1369-1382.
2. Del Rio L, Bennouna S, Salinas J, Denkers EY. CXCR2 deficiency confers impaired neutrophil recruitment and increased susceptibility during Toxoplasma gondii infection. J Immunol 2001;167:6503-6509.
3. Ohtsuka Y, Lee J, Stamm DS, Sanderson IR. MIP-2 secreted by epithelial cells increases neutrophil and lymphocyte recruitment in the mouse intestine. Gut 2001;49:526-533.
4. Mackay CR. Chemokines: immunology's high impact factors. Nat Immunol 2001;2:95-101.
5. Zabel BA, Agace WW, Campbell JJ, Heath HM, Parent D, Roberts Al, Ebert EC, Kassam N, Qin S, Zovko M, LaRosa GJ, Yang L-L, Soler D, Butcher EC, Ponath PD, Parker CM, Andrew DP. Human G protein-coupled receptor GPR-9-6/CC chemokine receptor 9 is selectively expressed on intestinal homing T lymphocytes, mucosal lymphocytes, and thymocytes and is required for thymus-expressed chemokine-mediated chemotaxis. J Exp Med 1999;190:1241-1256.
6. Kunkel EJ, Campbell JJ, Haraldsen G, Pan J, Boisvert J, Roberts Al, Ebert EC, Vierra MA, Goodman SB, Genovese MC, Wardlaw AJ, Greenberg HB, Parker CM, Butcher EC, Andrew DP, Agace WW. Lymphocyte CC chemokine receptor 9 and epithelial thymus-expressed chemokine (TECK) expression distinguish the small intestinal immune compartment: epithelial expression of tissue-specific chemokines as an organizing principle in regional immunity. J Exp Med 2000;192:761-768.
7. Wurbel MA, Malissen M, Guy-Grand D, Meffre E, Nussenzweig MC, Richelme M, Carrier A, Malissen B. Mice lacking the CCR9 CC-chemokine receptor show a mild impairment of early T- and B-cell development and a reduction in T-cell receptor gamma-delta(+) gut intraepithelial lymphocytes. Blood 2001;98:2626-2632.
8. Buzoni-Gatel D, Debbabi H, Mennechet FJ, Martin V, Lepage AC, Schwartzman JD, Kasper LH. Murine ileitis after intracellular parasite infection is controlled by TGF-beta-producing intraepithelial lymphocytes. Gastroenterology 2001;120:914-924.
9. Mennechet FJ, Kasper LH, Rachinel N, Li W, Vandewalle A, Buzoni-Gatel D. Lamina propria CD4+ T lymphocytes synergize with murine intestinal epithelial cells to enhance proinflammatory response against an intracellular pathogen. J Immunol 2002;168:2988-2996.
10. Chardes T, Buzoni-Gatel D, Lepage A, Bernard F, Bout D. Toxoplasma gondii oral infection induces specific cytotoxic CD8 alpha/beta+ Thy-1+ gut intraepithelial lymphocytes, lytic for parasite-infected enterocytes. J Immunol 1994;153:4596-4603.
11. Buzoni-Gatel D, Lepage AC, Dimier-Poisson IH, Bout DT, Kasper LH. Adoptive transfer of gut intraepithelial lymphocytes protects against murine infection with Toxoplasma gondii. J Immunol 1997;158:5883-5889.
12. Buzoni-Gatel D, Debbabi H, Moretto M, Dimier-Poisson IH, Lepage AC, Bout DT, Kasper LH. Intraepithelial lymphocytes traffic to the intestine and enhance resistance to Toxoplasma gondii oral infection. J Immunol 1999;162:5846-5852.
13. Gao JL, Wynn TA, Chang Y, Lee EJ, Broxmeyer HE, Cooper S, Tiffany HL, Westphal H, Kwon-Chung J, Murphy PM. Impaired host defense, hematopoiesis, granulomatous inflammation and type 1-type 2 cytokine balance in mice lacking CC chemokine receptor 1. J Exp Med 1997;185:1959-1968.
14. Bens M, Bogdanova A, Cluzeaud F, Miquerol L, Kerneis S, Kraehenbuhl JP, Kahn A, Pringault E, Vandewalle A. Transimmortalized mouse intestinal cells (m-ICc12) that maintain a crypt phenotype. Am J Physiol 1996;270:C1666-C1674.
15. Bouma G, Kaushiva A, Strober W. Experimental murine colitis is regulated by two genetic loci, including one on chromosome 11 that regulates IL-12 responses. Gastroenterology 2002;123:554-565.
16. Burg JL, Grover CM, Pouletty P, Boothroyd JC. Direct and sensitive detection of a pathogenic protozoan, Toxoplasma gondii, by polymerase chain reaction. J Clin Microbiol 1989;27:1787-1792.
17. Kirisits MJ, Mui E, McLeod R. Measurement of the efficacy of vaccines and antimicrobial therapy against infection with Toxoplasma gondii. Int J Parasitol 2000;30:149-155.
18. Liesenfeld O. Oral infection of C57BL/6 mice with Toxoplasma gondii: a new model of inflammatory bowel disease? J Infect Dis 2002;185(Suppl 1):S96-S101.
19. Khan IA, Schwartzman JD, Matsuura T, Kasper LH. A dichotomous role for nitric oxide during acute Toxoplasma gondii infection in mice. Proc Natl Acad Sci U S A 1997;94:13955-13960.
20. Uehara S, Grinberg A, Farber JM, Love PE. A role for CCR9 in T lymphocyte development and migration. J Immunol 2002;168:2811-2819.
21. Agace WW, Roberts AI, Wu L, Greineder C, Ebert EC, Parker CM. Human intestinal lamina propria and intraepithelial lymphocytes express receptors specific for chemokines induced by inflammation. Eur J Immunol 2000;30:819-826.
22. Bonecchi R, Bianchi G, Bordignon PP, D'Ambrosio D, Lang R, Borsatti A, Sozzani S, Allavena P, Gray PA, Mantovani A, Sinigaglia F. Differential expression of chemokine receptors and chemotactic responsiveness of type 1 T helper cells (Th1s) and Th2s. J Exp Med 1998;187:129-134.
23. Loetscher P, Uguccioni M, Bordoli L, Baggiolini M, Moser B, Chizzolini C, Dayer JM. CCR5 is characteristic of Th1 lymphocytes. Nature 1998;391:344-345.
24. Uekusa Y, Yu WG, Mukai T, Gao P, Yamaguchi N, Murai M, Matsushima K, Obika S, Imanishi T, Higashibata Y, Nomura S, Kitamura Y, Fujiwara H, Hamaoka T. A pivotal role for CC chemokine receptor 5 in T-cell migration to tumor sites induced by interleukin 12 treatment in tumor-bearing mice. Cancer Res 2002;62:3751-3758.
25. Scheerens H, Hessel E, de Waal-Malefyt R, Leach MW, Rennick D. Characterization of chemokines and chemokine receptors in two murine models of inflammatory bowel disease: IL-10-/- mice and Rag-2-/- mice reconstituted with CD4+CD45RBhigh T cells. Eur J Immunol 2001;31:1465-1474.
26. Nitcheu J, Bonduelle O, Combadiere C, Tefit M, Seilhean D, Mazier D, Combadiere B. Perforin-dependent brain-infiltrating cytotoxic CD8+ T lymphocytes mediate experimental cerebral malaria pathogenesis. J Immunol 2003;170:2221-2228.
27. Huffnagle GB, McNeil LK, McDonald RA, Murphy JW, Toews GB, Maeda N, Kuziel WA. Cutting edge: role of C-C chemokine receptor 5 in organ-specific and innate immunity to Cryptococcus neoformans. J Immunol 1999;163:4642-4646.
28. Dawson TC, Beck MA, Kuziel WA, Henderson F, Maeda N. Contrasting effects of CCR5 and CCR2 deficiency in the pulmonary inflammatory response to influenza A virus. Am J Pathol 2000;156:1951-1959.
29. Glass WG, Lane TE. Functional expression of chemokine receptor CCR5 on CD4(+) T cells during virus-induced central nervous system disease. J Virol 2003;77:191-198.
30. Aliberti J, Reis e Sousa C, Schito M, Hieny S, Wells T, Huffnagle GB, Sher A. CCR5 provides a signal for microbial induced production of IL-12 by CD8 alpha+ dendritic cells. Nat Immunol 2000;1:83-87.
31. Denkers EY, Kim L, Butcher BA. In the belly of the beast: subversion of macrophage proinflammatory signalling cascades during Toxoplasma gondii infection. Cell Microbiol 2003;5:75-83.
32. Andres PG, Beck PL, Mizoguchi E, Mizoguchi A, Bhan AK, Dawson T, Kuziel WA, Maeda N, MacDermott RP, Podolsky DK, Reinecker H-C. Mice with a selective deletion of the CC chemokine receptors 5 or 2 are protected from dextran sodium sulfate-mediated colitis: lack of CC chemokine receptor 5 expression results in a NK1.1+ lymphocyte-associated Th2-type immune response in the intestine. J Immunol 2000;164:6303-6312.
33. Peng KC, Cluzeaud F, Bens M, Van Huyen JP, Wioland MA, Lacave R, Vandewalle A. Tissue and cell distribution of the multidrug resistance-associated protein (MRP) in mouse intestine and kidney. J Histochem Cytochem 1999;47:757-768.
34. Hornef MW, Frisan T, Vandewalle A, Normark S, Richter-Dahlfors A. Toll-like receptor 4 resides in the Golgi apparatus and colocalizes with internalized lipopolysaccharide in intestinal epithelial cells. J Exp Med 2002;195:559-570.
35. Luo Y, Berman MA, Zhai Q, Fischer FR, Abromson-Leeman SR, Zhang Y, Kuziel WA, Gerard C, Dorf ME. RANTES stimulates inflammatory cascades and receptor modulation in murine astrocytes. Glia 2002;39:19-30.
36. Khan IA, MacLean JA, Lee FS, Casciotti L, DeHaan E, Schwartzman JD, Luster AD. IP-10 is critical for effector T cell trafficking and host survival in Toxoplasma gondii infection. Immunity 2000;12:483-494.