Co-receptor choice by Vα14i NKT cells is driven by Th-POK expression rather than avoidance of CD8-mediated negative selection

Journal of Experimental Medicine

Volumn 207, Issue 5, 2010, Pages 1015-1029

  Engel, Isaac ^a   Hammond, Kirsten ^a   Sullivan, Barbara A ^a   He, Xi ^b   Taniuchi, Ichiro ^c   Kappes, Dietmar ^b   Kronenberg, Mitchell ^a  

^a LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^b FOX CHASE CANCER CENTER   (United States)

^c RIKEN Center for Integrative Medical Sciences   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CD1D ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 4; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR POK; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIGEN EXPRESSION; ANTIGEN RECOGNITION; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; GENE REARRANGEMENT; HOMOZYGOSITY; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; THYMOCYTE; TRANSGENE; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, CD1; ANTIGENS, CD1D; ANTIGENS, CD4; ANTIGENS, CD8; CD8-POSITIVE T-LYMPHOCYTES; GENE REARRANGEMENT; HOMOZYGOTE; HUMANS; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; RECEPTORS, ANTIGEN, T-CELL;

EID: 77952304517     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20090557     Document Type: Article

References (56)

1. Aliahmad, P., and J. Kaye. 2008. Development of all CD4 T lineages requires nuclear factor TOX. J. Exp. Med. 205:245-256. doi:10.1084/jem.20071944
2. + T cells by CD1-expressing cortical thymocytes. J. Exp. Med. 182:2091-2096. doi:10.1084/jem.182.6.2091
3. Bendelac, A., N. Killeen, D.R. Littman, and R.H. Schwartz. 1994. A subset of CD4+ thymocytes selected by MHC class I molecules. Science. 263:1774-1778. doi:10.1126/science.7907820
4. Bendelac, A., O. Lantz, M.E. Quimby, J.W. Yewdell, J.R. Bennink, and R.R. Brutkiewicz. 1995. CD1 recognition by mouse NK1+ T lymphocytes. Science. 268:863-865. doi:10.1126/science.7538697
5. Bendelac, A., R.D. Hunziker, and O. Lantz. 1996. Increased interleukin 4 and immunoglobulin E production in transgenic mice overexpressing NK1 T cells. J. Exp. Med. 184:1285-1293. doi:10.1084/jem.184.4.1285
6. Benlagha, K., T. Kyin, A. Beavis, L. Teyton, and A. Bendelac. 2002. A thymic precursor to the NK T cell lineage. Science. 296:553-555. doi:10.1126/science.1069017
7. Benlagha, K., D.G. Wei, J. Veiga, L. Teyton, and A. Bendelac. 2005. Characterization of the early stages of thymic NKT cell development. J. Exp. Med. 202:485-492. doi:10.1084/jem.20050456
8. Berzins, S.P., A.D. Cochrane, D.G. Pellicci, M.J. Smyth, and D.I. Godfrey. 2005. Limited correlation between human thymus and blood NKT cell content revealed by an ontogeny study of paired tissue samples. Eur. J. Immunol. 35:1399-1407. doi:10.1002/eji.200425958
9. Bezbradica, J.S., T. Hill, A.K. Stanic, L. Van Kaer, and S. Joyce. 2005. Commitment toward the natural T (iNKT) cell lineage occurs at the CD4+8+ stage of thymic ontogeny. Proc. Natl. Acad. Sci. USA. 102:5114-5119. doi:10.1073/pnas.0408449102
10. Bezbradica, J.S., L.E. Gordy, A.K. Stanic, S. Dragovic, T. Hill, J. Hawiger, D. Unutmaz, L. Van Kaer, and S. Joyce. 2006. Granulocytemacrophage colony-stimulating factor regulates effector differentiation of invariant natural killer T cells during thymic ontogeny. Immunity. 25:487-497. doi:10.1016/j.immuni.2006.06.017
11. Brossay, L., O. Naidenko, N. Burdin, J. Matsuda, T. Sakai, and M. Kronenberg. 1998a. Structural requirements for galactosylceramide recognition by CD1-restricted NK T cells. J. Immunol. 161:5124-5128. (Pubitemid 28519066)
12. Brossay, L., S. Tangri, M. Bix, S. Cardell, R. Locksley, and M. Kronenberg. 1998b. Mouse CD1-autoreactive T cells have diverse patterns of reactivity to CD1+ targets. J. Immunol. 160:3681-3688.
13. Budowle, B., and F.S. Baechtel. 1990. Modifications to improve the effectiveness of restriction fragment length polymorphism typing. Appl. Theor. Electrophor. 1:181-187.
14. Burdin, N., L. Brossay, Y. Koezuka, S.T. Smiley, M.J. Grusby, M. Gui, M. Taniguchi, K. Hayakawa, and M. Kronenberg. 1998. Selective ability of mouse CD1 to present glycolipids: alphagalactosylceramide specifically stimulates V alpha 14+ NK T lymphocytes. J. Immunol. 161:3271-3281.
15. Chun, T., M.J. Page, L. Gapin, J.L. Matsuda, H. Xu, H. Nguyen, H.S. Kang, A.K. Stanic, S. Joyce, W.A. Koltun, et al. 2003. CD1d-expressing dendritic cells but not thymic epithelial cells can mediate negative selection of NKT cells. J. Exp. Med. 197:907-918. doi:10.1084/jem.20021366
16. Dave, V.P., D. Allman, R. Keefe, R.R. Hardy, and D.J. Kappes. 1998. HD mice: a novel mouse mutant with a specific defect in the generation of CD4(+) T cells. Proc. Natl. Acad. Sci. USA. 95:8187-8192. doi:10.1073/pnas.95.14.8187
17. Egawa, T., G. Eberl, I. Taniuchi, K. Benlagha, F. Geissmann, L. Hennighausen, A. Bendelac, and D.R. Littman. 2005. Genetic evidence supporting selection of the Valpha14i NKT cell lineage from double-positive thymocyte precursors. Immunity. 22:705-716. doi:10.1016/j.immuni.2005.03.011 (Pubitemid 40814501)
18. Engel, I., and C. Murre. 1999. Ectopic expression of E47 or E12 promotes the death of E2A-deficient lymphomas. Proc. Natl. Acad. Sci. USA. 96:996-1001. doi:10.1073/pnas.96.3.996
19. Fisher, D.A., S.W. Hunt III, and L. Hood. 1985. Structure of a gene encoding a murine thymus leukemia antigen, and organization of Tla genes in the BALB/c mouse. J. Exp. Med. 162:528-545. doi:10.1084/jem.162.2.528
20. Fung-Leung, W.P., M.W. Schilham, A. Rahemtulla, T.M. Kündig, M. Vollenweider, J. Potter, W. van Ewijk, and T.W. Mak. 1991. CD8 is needed for development of cytotoxic T cells but not helper T cells. Cell. 65:443-449. doi:10.1016/00928674(91)904628
21. Garcia, K.C., C.A. Scott, A. Brunmark, F.R. Carbone, P.A. Peterson, I.A. Wilson, and L. Teyton. 1996. CD8 enhances formation of stable T-cell receptor/MHC class I molecule complexes. Nature. 384:577-581. doi:10.1038/384577a0
22. Godfrey, D.I., H.R. MacDonald, M. Kronenberg, M.J. Smyth, and L. Van Kaer. 2004. NKT cells: what's in a name? Nat. Rev. Immunol. 4:231-237. doi:10.1038/nri1309
23. Hager, E., A. Hawwari, J.L. Matsuda, M.S. Krangel, and L. Gapin. 2007. Multiple constraints at the level of TCRalpha rearrangement impact Valpha14i NKT cell development. J. Immunol. 179:2228-2234.
24. He, X., X. He, V.P. Dave, Y. Zhang, X. Hua, E. Nicolas, W. Xu, B.A. Roe, and D.J. Kappes. 2005. The zinc finger transcription factor ThPOK regulates CD4 versus CD8 T-cell lineage commitment. Nature. 433:826-833. doi:10.1038/ nature03338
25. He, X., K. Park, H. Wang, X. He, Y. Zhang, X. Hua, Y. Li, and D.J. Kappes. 2008. CD4-CD8 lineage commitment is regulated by a silencer element at the ThPOK transcription-factor locus. Immunity. 28:346-358. doi:10.1016/j. immuni.2008.02.006
26. Keefe, R., V. Dave, D. Allman, D. Wiest, and D.J. Kappes. 1999. Regulation of lineage commitment distinct from positive selection. Science. 286:1149-1153. doi:10.1126/science.286.5442.1149 (Pubitemid 29522274)
27. Kinsella, T.M., and G.P. Nolan. 1996. Episomal vectors rapidly and stably produce high-titer recombinant retrovirus. Hum. Gene Ther. 7:1405-1413. doi:10.1089/hum.1996.7.121405
28. Kjer-Nielsen, L., N.A. Borg, D.G. Pellicci, T. Beddoe, L. Kostenko, C.S. Clements, N.A. Williamson, M.J. Smyth, G.S. Besra, H.H. Reid, et al. 2006. A structural basis for selection and cross-species reactivity of the semi-invariant NKT cell receptor in CD1d/glycolipid recognition. J. Exp. Med. 203:661-673. doi:10.1084/jem.20051777
29. Kosaka, H., T. Yoshimoto, T. Yoshimoto, J. Fujimoto, and K. Nakanishi. 2008. Interferon-gamma is a therapeutic target molecule for prevention of postoperative adhesion formation. Nat. Med. 14:437-441. doi:10.1038/nm1733
30. Kovalovsky, D., O.U. Uche, S. Eladad, R.M. Hobbs, W. Yi, E. Alonzo, K. Chua, M. Eidson, H.J. Kim, J.S. Im, et al. 2008. The BTB-zinc finger transcriptional regulator PLZF controls the development of invariant natural killer T cell effector functions. Nat. Immunol. 9:1055-1064. doi:10.1038/ni.1641
31. Kronenberg, M., and I. Engel. 2007. On the road: progress in finding the unique pathway of invariant NKT cell differentiation. Curr. Opin. Immunol. 19:186-193. doi:10.1016/j.coi.2007.02.009
32. Kronenberg, M., and L. Gapin. 2002. The unconventional lifestyle of NKT cells. Nat. Rev. Immunol. 2:557-568.
33. - T cells in mice and humans. J. Exp. Med. 180:1097-1106. doi:10.1084/jem.180.3.1097
34. 2A receptor activation reduces hepatic ischemia reperfusion injury by inhibiting CD1d-dependent NKT cell activation. J. Exp. Med. 203:2639-2648. doi:10.1084/jem.20061097
35. 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 CD8alphaalpha and the nonclassical MHC class I molecule, TL. Science. 294:1936-1939. doi:10.1126/science.1063564
36. Loza, M.J., L.S. Metelitsa, and B. Perussia. 2002. NKT and T cells: coordinate regulation of NK-like phenotype and cytokine production. Eur. J. Immunol. 32:3453-3462. doi:10.1002/15214141(200212)32:12〈3453:: AIDIMMU3453〉3.0.CO;2D
37. Mancini, S.J., S.M. Candéias, J.P. Di Santo, P. Ferrier, P.N. Marche, and E. Jouvin-Marche. 2001. TCRA gene rearrangement in immature thymocytes in absence of CD3, pre-TCR, and TCR signaling. J. Immunol. 167:4485-4493.
38. Matsuda, J.L., and L. Gapin. 2005. Developmental program of mouse Valpha14i NKT cells. Curr. Opin. Immunol. 17:122-130. doi:10.1016/j.coi.2005.01. 002
39. Mendiratta, S.K., W.D. Martin, S. Hong, A. Boesteanu, S. Joyce, and L. Van Kaer. 1997. CD1d1 mutant mice are deficient in natural T cells that promptly produce IL-4. Immunity. 6:469-477. doi:10.1016/S10747613(00)802903
40. Pasqual, N., M. Gallagher, C. Aude-Garcia, M. Loiodice, F. Thuderoz, J. Demongeot, R. Ceredig, P.N. Marche, and E. Jouvin-Marche. 2002. Quantitative and qualitative changes in V-Jα rearrangements during mouse thymocytes differentiation: implication for a limited T cell receptor α chain repertoire. J. Exp. Med. 196:1163-1173. doi:10.1084/jem.20021074
41. Pear, W.S., J.P. Miller, L. Xu, J.C. Pui, B. Soffer, R.C. Quackenbush, A.M. Pendergast, R. Bronson, J.C. Aster, M.L. Scott, and D. Baltimore. 1998. Efficient and rapid induction of a chronic myelogenous leukemia-like myeloproliferative disease in mice receiving P210 bcr/abl-transduced bone marrow. Blood. 92:3780-3792.
42. Robey, E.A., B.J. Fowlkes, J.W. Gordon, D. Kioussis, H. von Boehmer, F. Ramsdell, and R. Axel. 1991. Thymic selection in CD8 transgenic mice supports an instructive model for commitment to a CD4 or CD8 lineage. Cell. 64:99-107. doi:10.1016/00928674(91)90212H
43. Savage, A.K., M.G. Constantinides, J. Han, D. Picard, E. Martin, B. Li, O. Lantz, and A. Bendelac. 2008. The transcription factor PLZF directs the effector program of the NKT cell lineage. Immunity. 29:391-403. doi:10.1016/j.immuni.2008.07.011
44. Schümann, J., M.P. Mycko, P. Dellabona, G. Casorati, and H.R. MacDonald. 2006. Cutting edge: influence of the TCR Vbeta domain on the selection of semi-invariant NKT cells by endogenous ligands. J. Immunol. 176:2064-2068.
45. Setoguchi, R., M. Tachibana, Y. Naoe, S. Muroi, K. Akiyama, C. Tezuka, T. Okuda, and I. Taniuchi. 2008. Repression of the transcription factor ThPOK by Runx complexes in cytotoxic T cell development. Science. 319:822-825. doi:10.1126/science.1151844 (Pubitemid 351225874)
46. Sidobre, S., O.V. Naidenko, B.C. Sim, N.R. Gascoigne, K.C. Garcia, and M. Kronenberg. 2002. The V alpha 14 NKT cell TCR exhibits high-affinity binding to a glycolipid/CD1d complex. J. Immunol. 169:1340-1348.
47. Singer, A., S. Adoro, and J.H. Park. 2008. Lineage fate and intense debate: myths, models and mechanisms of CD4- versus CD8- lineage choice. Nat. Rev. Immunol. 8:788-801. doi:10.1038/nri2416
48. Stetson, D.B., M. Mohrs, R.L. Reinhardt, J.L. Baron, Z.E. Wang, L. Gapin, M. Kronenberg, and R.M. Locksley. 2003. Constitutive cytokine mRNAs mark natural killer (NK) and NK T cells poised for rapid effector function. J. Exp. Med. 198:1069-1076. doi:10.1084/jem.20030630
49. Sun, G., X. Liu, P. Mercado, S.R. Jenkinson, M. Kypriotou, L. Feigenbaum, P. Galéra, and R. Bosselut. 2005. The zinc finger protein cKrox directs CD4 lineage differentiation during intrathymic T cell positive selection. Nat. Immunol. 6:373-381. doi:10.1038/ni1183
50. Teitell, M., H.R. Holcombe, L. Brossay, A. Hagenbaugh, M.J. Jackson, L. Pond, S.P. Balk, C. Terhorst, P.A. Peterson, and M. Kronenberg. 1997. Nonclassical behavior of the mouse CD1 class I-like molecule. J. Immunol. 158:2143-2149.
51. Tupin, E., Y. Kinjo, and M. Kronenberg. 2007. The unique role of natural killer T cells in the response to microorganisms. Nat. Rev. Microbiol. 5:405-417. doi:10.1038/nrmicro1657 (Pubitemid 46780078)
52. b-/- deficient mice possess functional CD8+ T cells and natural killer cells. Proc. Natl. Acad. Sci. USA. 95:12492-12497. doi:10.1073/pnas.95.21.12492
53. Wack, A., M. Coles, T. Norton, A. Hostert, and D. Kioussis. 2000. Early onset of CD8 transgene expression inhibits the transition from DN3 to DP thymocytes. J. Immunol. 165:1236-1242.
54. Wang, L., K.F. Wildt, E. Castro, Y. Xiong, L. Feigenbaum, L. Tessarollo, and R. Bosselut. 2008. The zinc finger transcription factor Zbtb7b represses CD8-lineage gene expression in peripheral CD4+ T cells. Immunity. 29:876-887. doi:10.1016/j.immuni.2008.09.019
55. Wei, D.G., S.A. Curran, P.B. Savage, L. Teyton, and A. Bendelac. 2006. Mechanisms imposing the Vβ bias of Vα14 natural killer T cells and consequences for microbial glycolipid recognition. J. Exp. Med. 203:1197-1207. doi:10.1084/jem.20060418
56. Yannoutsos, N., P. Wilson, W. Yu, H.T. Chen, A. Nussenzweig, H. Petrie, and M.C. Nussenzweig. 2001. The role of recombination activating gene (RAG) reinduction in thymocyte development in vivo. J. Exp. Med. 194:471-480. doi:10.1084/jem.194.4.471