Infection-induced expansion of a MHC class Ib-dependent intestinal intraepithelial γδ T cell subset

Journal of Immunology

Volumn 172, Issue 11, 2004, Pages 6828-6837

  Davies, Adrian ^a,d   Lopez Briones, Sergio ^a   Ong, Helena ^a   O'Neil Marshall, Cynthia ^a   Lemonnier, François A ^b   Nagaraju, Kanneboyina ^a   Metcalf, Eleanor S ^c   Soloski, Mark J ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INSTITUT PASTEUR   (France)

^c Uniformed Services University of the Health Sciences and the Walter Reed National Military Medical Center   (United States)

^d MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; CD94 ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1B; T LYMPHOCYTE RECEPTOR DELTA CHAIN; T LYMPHOCYTE RECEPTOR GAMMA CHAIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL INFECTION; BACTERIAL VIRULENCE; CONTROLLED STUDY; IMMUNE RESPONSE; IMMUNE SYSTEM; INTESTINE EPITHELIUM; MOUSE; NONHUMAN; PRIORITY JOURNAL; SALMONELLA; T LYMPHOCYTE;

EID: 2442656559     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.172.11.6828     Document Type: Article

References (99)

1. Jones, B. D., N. Ghori, and S. Falkow. 1994. Salmonella typhimurium initiates murine infection by penetrating and destroying the specialized epithelial M cells of the Peyers patches. J. Exp. Med. 180:15.
2. Clark, M. A., M. A. Jepson, N. L. Simmons, and B. H. Hirst. 1994. Preferential interaction of Salmonella typhimurium with mouse Peyer's patch M cells. Res. Microbiol. 145:543.
3. Jepson, M. A., and M. A. Clark. 2001. The role of M cells in Salmonella infection. Microbes Infect. 3:1183.
4. Sansonetti, P. J., and A. Phalipon. 1999. M cells as ports of entry for enteroinvasive pathogens: mechanisms of interaction, consequences for the disease process. Semin. Immunol. 11:193.
5. Carter, P. B., and F. M. Collins. 1974. The route of enteric infection in normal mice. J. Exp. Med. 139:1189.
6. Jones, B. D., and S. Falkow. 1996. Salmonellosis: host immune responses and bacterial virulence determinants. Annu. Rev. Immunol. 14:533.
7. Makela, P. H., and C. E. Hormaeche. 1997. Immunity to Salmonella. In Host Response to Intracellular Pathogens, S. H. E. Kaufman, ed. R. G. Landes, Austin, TX, p. 143.
8. Mittrucker, H. W., and S. H. Kaufmann. 2000. Immune response to infection with Salmonella typhimurium in mice. J. Leukocyte Biol. 67:457.
9. Weintraub, B. C., L. Eckmann, S. Okamoto, M. Hense, S. M. Hedrick, and J. Fierer. 1997. Role of αβ and γδ T cells in the host response to Salmonella infection as demonstrated in T-cell-receptor-deficient mice of defined Ity genotypes. Infect. Immun. 65:2306.
10. Sinha, K., P. Mastroeni, J. Harrison, R. D. de Hormaeche, and C. E. Hormaeche. 1997. Salmonella typhimurium aroA, htrA, and aroD htrA mutants cause progressive infections in athymic (nu/nu) BALB/c mice. Infect. Immun. 65:1566.
11. O'Brien, A. D., and E. S. Metcalf. 1982. Control of early Salmonella typhimurium growth in innately Salmonella-resistant mice does not require functional T lymphocytes. J. Immunol. 129:1349.
12. Portillo, F. G.-D., and B. B. Finlay. 1994. Salmonella invasion of nonphagocytic cells induce formation of macropinosome in the host cell. Infect. Immun. 62:4641.
13. Galan, J. E. 1996. Molecular genetic basis of Salmonella entry into host cells. Mol. Microbiol. 20:263.
14. Richterdahlfors, A., A. M. J. Buchan, and B. B. Finlay. 1997. Murine salmonellosis studied by confocal microscopy: Salmonella typhimurium resides intracellularly inside macrophages and exerts a cytotoxic effect on phagocytes in vivo. J. Exp. Med. 186:569.
15. Pfeifer, J. D., M. J. Wick, R. L. Roberts, K. Findlay, S. J. Normark, and C. V. Harding. 1993. Phagocytic processing of bacterial antigens for class I MHC presentation to T cells. Nature 361:359.
16. Mastroeni, P., R. B. Villarreal, and C. E. Hormaeche. 1992. Role of T cells, TNF-α and IFN-γ, in recall of immunity to oral challenge with virulent salmonellae in mice vaccinated with live attenuated aro-Salmonella vaccines. Microb. Pathog. 13:477.
17. + T cells and T-independent mechanisms in acquired resistance to Salmonella typhimurium infection. J. Immunol. 145:1265.
18. + TCR-αβ cells and IFN-γ in bacterial clearance independent of intracellular location. J. Immunol. 156:3321.
19. + T cell responses during natural infection with Salmonella typhimurium. J. Immunol. 164:986.
20. + T cells in acquired immunity and granuloma formation. Microb. Pathog. 14:45-55. 14:45.
21. + T cells in immunity to Salmonella infection and the involvement of MHC class Ib molecules. J. Immunol. 162:5398.
22. + intraepithelial lymphocytes. Nature 333:855.
23. + intraepithelial lymphocytes. Science 243:1716.
24. + lymphocyte populations with different T cell receptors: a role for the gut epithelium in T cell differentiation. J. Exp. Med. 173:471.
25. Rocha, B., P. Vassalli, and D. Guy-Grand. 1994. Thymic and extrathymic origins of gut intraepithelial lymphocyte populations in mice. J. Exp. Med. 180:681.
26. Arstila, T., T. P. Arstila, S. Calbo, F. Selz, M. Malassis-Seris, P. Vassalli, P. Kourilsky, and D. Guy-Grand. 2000. Identical T cell clones are located within the mouse gut epithelium and lamina propia and circulate in the thoracic duct lymph. J. Exp. Med. 191:823.
27. Das, G., and C. A. Janeway, Jr. 1999. Development of CD8α/α and CD8α/β T cells in major histocompatibility, complex class I-deficient mice. J. Exp. Med. 190:881.
28. + T cells and natural killer cells. Proc. Natl. Acad. Sci. USA 95:12492.
29. + T cells. Cell 71:1205.
30. + lympho-hemopoietic progenitors develop. J. Exp. Med. 184:1449.
31. 2-microglobulin- and/or TAP1-deficient mice. J. Immunol. 156:2710.
32. + intestinal intraepithelial lymphocytes. J. Immunol. 156:4209.
33. 2-microglobulin. Eur. J. Immunol. 25:2332.
34. Park, S. H., D. Guy-Grand, F. A. Lemonnier, C. R. Wang, A. Bendelac, and B. Jabri. 1999. Selection and expansion of CD8α/α T cell receptor α/β intestinal intraepithelial lymphocytes in the absence of both classical major histocompatibility complex class I and nonclassical CD1 molecules. J. Exp. Med. 190:885.
35. + T cells are found in intestinal intraepithelial lymphocytes of mice that lack classical MHC class I molecules. J. Immunol. 163:4100.
36. + cells in murine intestinal intraepithelial lymphocytes. J. Exp. Med. 192:1521.
37. Lefrancois, L. 1991. Phenotypic complexity of intraepithelial lymphocytes of the small intestine. J. Immunol. 147:1746.
38. 2-microglobulin-deficient mice. Proc. Natl. Acad. Sci. USA 89:653.
39. Schild, H., N. Mavaddat, C. Litzenberger, E. W. Ehrich, M. M. Davis, J. A. Bluestone, L. Matis, R. K. Draper, and Y. H. Chien. 1994. The nature of major histocompatibility complex recognition by γδ T cells. Cell 76:29.
40. Ito, K., L. Van Kaer, M. Bonneville, S. Hsu, D. B. Murphy, and S. Tonegawa. 1990. Recognition of the product of a novel MHC TL region gene (27b) by a mouse γδ T cell receptor. Cell 62:549.
41. Crowley, M. P., A. M. Fahrer, N. Baumgarth, J. Hampl, I. Gutgemann, L. Teyton, and Y. Chien. 2000. A population of murine γδ T cells that recognize an inducible MHC class Ib molecule. Science 287:314.
42. Leishman, A. J., O. V. Naidenko, A. Attinger, F. Koning, C. J. Lena, Y. Xiong, H. C. Chang, E. Reinherz, M. Kronenberg, and H. Cheroutre. 2001. T cell responses modulated through interaction between CD8αα and the nonclassical MHC class I molecule, TL. Science 294:1936.
43. Jamieson, A. M., A. Diefenbach, C. W. McMahon, N. Xiong, J. R. Carlyle, and D. H. Raulet. 2002. The role of the NKG2D immunoreceptor in immune cell activation and natural killing. Immunity 17:19.
44. Bleicher, P. A., S. P. Balk, S. J. Hagen, R. S. Blumberg, T. J. Flotte, and C. Terhorst. 1990. Expression of murine CD1 on gastrointestinal epithelium. Science 250:679.
45. Hershberg, R., P. Eghtesady, B. Sydora, K. Brorson, H. Cheroutre, R. Modlin, and M. Kronenberg. 1990. Expression of the thymus leukemia antigen in mouse intestinal epithelium. Proc. Natl. Acad. Sci. USA 87:9727.
46. Eghtesady, P., K. A. Brorson, H. Cheroutre, R. E. Tigelaar, L. Hood, and M. Kronenberg. 1992. Expression of mouse Tla region class I genes in tissues enriched for γδ cells. [Published erratum appears in 1993 Immunogenetics 38: 80.] Immunogenetics 36:377.
47. Eghtesady, P., K. A. Brorson, H. Cheroutre, R. E. Tigelaar, L. Hood, and M. Kronenberg. 1992. Expression of mouse Tla region class I genes in tissues enriched for γδ cells. [Published erratum appears in 1993 Immunogenetics 38: 80.] Immunogenetics 36:377.
48. + T cells. Science 248:1227.
49. Tanchot, C., F. A. Lemonnier, B. Perarnau, A. A. Freitas, and B. Rocha. 1997. Differential requirements for survival and proliferation of CD8 naive or memory T cells. Science 276:2057.
50. + T cell repertoire and anti-lymphocytic choriomeningitis virus cytolytic responses. Eur. J. Immunol. 29:1243.
51. Guy-Grand, D., C. Griscelli, and P. Vassalli. 1978. The mouse gut T lymphocyte, a novel type of T cell: nature, origin, and traffic in mice in normal and graft-versus-host conditions. J. Exp. Med. 148:1661.
52. Aldrich, C. J., A. DeCloux, A. S. Woods, R. J. Cotter, M. J. Soloski, and J. Forman. 1994. Identification of a Tap-dependent leader peptide recognized by alloreactive T cells specific for a class Ib antigen. Cell 79:649.
53. Mage, M. G., L. Lee, R. K. Ribaudo, M. Corr, S. Kozlowski, L. McHugh, and D. H. Margulies. 1992. A recombinant, soluble, single-chain class I major histocompatibility complex molecule with biological activity. Proc. Natl. Acad. Sci. USA 89:10658.
54. 2m knockout mice. FASEB J. 12:1779.
55. d interact with NK and TCR. J. Immunol. 163:3699.
56. 2-Microglobulin gene mutations: a study of established colorectal cell lines and fresh tumors. Proc. Natl. Acad. Sci. USA 91:4751.
57. Dexter, D. L., J. A. Barbosa, and P. Calabresi. 1979. N,N-Dimethylfomamide-induced alteration of cell culture characteristics and loss of tumorigenicity in cultured human colon carcinoma cells. Cancer Res. 39:1020.
58. del Senno, L., D. Anzanel, R. Barbieri, D. Buzzoni, P. Rossi, R. Piva, and R. Gambari. 1986. Cell Biol. Int. Rep. 10:195.
59. Wingren, C., M. P. Crowley, M. Degano, Y. Chien, and I. A. Wilson. 2000. Crystal structure of a γδ T cell receptor ligand T22: a truncated MHC-like fold. Science 287:310.
60. Steele, C. R., D. E. Oppenheim, and A. C. Hayday. 2000. γ(δ) T cells: non-classical ligands for non-classical cells. Curr. Biol. 10:R282.
61. Vidovic, D., M. Roglic, K. McKune, S. Guerder, C. MacKay, and Z. Dembic. 1989. Qa-1 restricted recognition of foreign antigen by a γδ T-cell hybridoma. Nature 340:646.
62. Tsujimura, K., T. Takahashi, A. Morita, H. Hasegawa-Nishiwaki, S. Iwase, and Y. Obata. 1996. Positive selection of γδ CTL by TL antigen expressed in the thymus. J. Exp. Med. 184:2175.
63. Braud, V. M., D. S. Allan, C. A. O'Callaghan, K. Soderstrom, A. D'Andrea, G. S. Ogg, S. Lazetic, N. T. Young, J. I. Bell, J. H. Phillips, et al. 1998. HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature 391:795.
64. Borrego, F., M. Ulbrecht, E. H. Weiss, J. E. Coligan, and A. G. Brooks. 1998. Recognition of human histocompatibility leukocyte antigen HLA-E complexed with HLA class I signal sequence-derived peptides by CD94/NKG2 confers protection from natural killer cell-mediated lysis. J. Exp. Med. 187:813.
65. Lee, N., M. Llano, M. Carretero, A. Ishitani, F. Navarro, M. Lopez-Botet, and D. E. Geraghty. 1998. HLA-E is a major ligand for the natural killer inhibitory receptor CD94/NKG2A. Proc. Natl. Acad. Sci. USA 95:5199.
66. b. J. Exp. Med. 188:1841.
67. Lowen, L. C., C. J. Aldrich, and J. Forman. 1993. Analysis of T cell receptors specific for recognition of class IB antigens. J. Immunol. 151:6155.
68. b. J. Exp. Med. 188:961.
69. Chun, T., C. J. Aldrich, M. E. Baldeon, L. V. Kawczynski, M. J. Soloski, and H. R. Gaskins. 1998. Constitutive and regulated expression of the class IB molecule Qa-1 in pancreatic β cells. Immunology 94:64.
70. + T cells expressing Vβ8 TCR: a role of the Qa-1 molecule. Immunity 2:185.
71. Bouwer, H. G. A., M. S. Seaman, J. Forman, and D. J. Hinrichs. 1997. MHC class Ib-restricted cells contribute to antilisterial immunity: evidence for Qa-Ib as a key restricting element for Listeria-specific CTLs. J. Immunol. 159:2795.
72. + pulmonary T cells regulate αβ T cell-independent airway responsiveness. Proc. Natl. Acad. Sci. USA 99:8850.
73. Born, W., L. Hall, A. Dallas, J. Boymel, T. Shinnick, D. Young, P. Brennan, and R. O'Brien. 1990. Recognition of a peptide antigen by heat shock-reactive γδ T lymphocytes. Science 249:67.
74. Imani, F., and M. J. Soloski. 1991. Heat shock proteins can regulate expression of the Tla region-encoded class Ib molecule Qa-1. Proc. Natl. Acad. Sci. USA 88:10475.
75. O'Brien, R. L., Y. X. Fu, R. Cranfill, A. Dallas, C. Ellis, C. Reardon, J. Lang, S. R. Carding, R. Kubo, and W. Born. 1992. Heat shock protein Hsp60-reactive γδ cells: a large, diversified T-lymphocyte subset with highly focused specificity. Proc. Natl. Acad. Sci. USA 89:4348.
76. Lo, W.-F., A. Woods, R. Cotter, A. DeCloux, E. S. Metcalf, and M. J. Soloski. 2000. Molecular mimicry mediated by MHC class Ib molecules following infection with Gram-negative pathogens. Nat. Med. 6:215.
77. - cells: a possible mechanism of tolerance during NK cell development. J. Immunol. 162:6976.
78. Davies, A., S. Kalb, B. Liang, C. J. Aldrich, F. A. Lemonnier, H. Jiang, R. Cotter, and M. J. Soloski. 2003. A peptide from heat shock protein 60 is the dominant peptide bound to Qa-1 in the absence of the MHC class Ia leader sequence peptide Qdm. J. Immunol. 170:5027.
79. Starr, T. K., S. C. Jameson, and K. A. Hogquist. 2003. Positive and negative selection of T cells. Annu. Rev. Immunol. 21:139.
80. Goldrath, A. W., and M. J. Bevan. 1999. Selecting and maintaining a diverse T-cell repertoire. Nature 402:255.
81. Hayday, A., and R. Tigelaar. 2003. Immunoregulation in the tissues by γδT cells. Nat. Rev. Immunol. 3:233.
82. Hayday, A., E. Theodoridis, E. Ramsburg, and J. Shires. 2001. Intraepithelial lymphocytes: exploring the Third Way in immunology. Nat. Immunol. 2:997.
83. Carding, S. R., and P. J. Egan. 2002. γδ T cells: functional plasticity and heterogeneity. Nat. Rev. Immunol. 2:336.
84. Findly, R. C., S. J. Roberts, and A. C. Hayday. 1993. Dynamic response of murine gut intraepithelial T cells after infection by the coccidian parasite Eimeria. Eur. J. Immunol. 23:2557.
85. +-deficient mice display abnormal but distinct phenotypes toward a natural, widespread infection of the intestinal epithelium. Proc. Natl. Acad. Sci. USA 93:11774.
86. Havran, W. L. 2000. A role for epithelial γδ T cells in tissue repair. Immunol. Res. 21:63.
87. Chen, Y., K. Chou, E. Fuchs, W. L. Havran, and R. Boismenu. 2002. Protection of the intestinal mucosa by intraepithelial γδ T cells. Proc. Natl. Acad. Sci. USA 99:14338.
88. Jameson, J., K. Ugarte, N. Chen, P. Yachi, E. Fuchs, R. Boismenu, and W. L. Havran. 2002. A role for skin γδ T cells in wound repair. Science 296:747.
89. Mombaerts, P., J. Arnoldi, F. Russ, S. Tonegawa, and S. H. Kaufmann. 1993. Different roles of αβ and γδ T cells in immunity against an intracellular bacterial pathogen. Nature 365:53.
90. Fu, Y. X., C. E. Roark, K. Kelly, D. Drevets, P. Campbell, R. O'Brien, and W. Born. 1994. Immune protection and control of inflammatory tissue necrosis by γδ T cells. J. Immunol. 153:3101.
91. Monack, D. M., B. Raupach, A. E. Hromockyj, and S. Falkow. 1996. Salmonella typhimurium invasion induces apoptosis in infected macrophages. Proc. Natl. Acad. Sci. USA 93:9833.
92. Takeuchi, A. 1967. Electron microscopic studies of experimental Salmonella infection: penetration into the intestinal epithelium by Salmonella typhimurium. Am. J. Pathol. 50:109.
93. Mixter, P. F., V. Camerini, B. J. Stone, V. L. Miller, and M. Kronenberg. 1994. Mouse T lymphocytes that express a γδ T-cell antigen receptor contribute to resistance to Salmonella infection in vivo. Infect. Immun. 62:4618.
94. Cerwenka, A., A. B. Bakker, T. McClanahan, J. Wagner, J. Wu, J. H. Phillips, and L. L. Lanier. 2000. Retinoic acid early inducible genes define a ligand family for the activating NKG2D receptor in mice. Immunity 12:721.
95. Diefenbach, A., A. M. Jamieson, S. D. Liu, N. Shastri, and D. H. Raulet. 2000. Ligands for the murine NKG2D receptor: expression by tumor cells and activation of NK cells and macrophages. Nat. Immunol. 1:119.
96. Girardi, M., D. E. Oppenheim, C. R. Steele, J. M. Lewis, E. Glusac, R. Filler, P. Hobby, B. Sutton, R. E. Tigelaar, and A. C. Hayday. 2001. Regulation of cutaneous malignancy by γδ T cells. Science 294:605.
97. Imani, F., T. Shinneck, and M. Soloski. 1995. Class Ib molecules: a role in the presentation of heat-shock proteins in the immune system? In Stress Proteins in Medicine. W. van Eden and D. Young, eds. Dekker, New York, p. 547.
98. Groh, V., A. Steinle, S. Bauer, and T. Spies. 1998. Recognition of stress-induced MHC molecules by intestinal epithelial γδ T cells. Science 279:1737.
99. Jabri, B., N. P. de Serre, C. Cellier, K. Evans, C. Gache, C. Carvalho, J. F. Mougenot, M. Allez, R. Jian, P. Desreumaux, et al. 2000. Selective expansion of intraepithelial lymphocytes expressing the HLA-E-specific natural killer receptor CD94 in celiac disease. Gastroenterology 118:867.