Antigen-specific clonal expansion and cytolytic effector function of CD8+ T lymphocytes depend on the transcription factor Bcl11b

Journal of Experimental Medicine

Volumn 207, Issue 8, 2010, Pages 1687-1699

  Zhang, Shuning ^a   Rozell, Mike ^a   Verma, Raj K ^a   Albu, Diana I ^a   Califano, Danielle ^a   Van Valkenburgh, Jeffrey ^a   Merchant, Akeel ^a   Rangel Moreno, Javier ^b   Randall, Troy D ^b   Jenkins, Nancy A ^c   Copeland, Neal G ^c   Liu, Pentao ^d   Avram, Dorina ^a  

^a ALBANY MEDICAL COLLEGE   (United States)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^c INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^d WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GRANZYME; INTERLEUKIN 7 RECEPTOR; PERFORIN; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR BCL11B; UNCLASSIFIED DRUG; BCL11B PROTEIN, MOUSE; CD8 ANTIGEN; CD8ALPHA ANTIGEN; CD8BETA ANTIGEN; LYMPHOCYTE ANTIGEN RECEPTOR; OVA-8; OVALBUMIN; PEPTIDE FRAGMENT; PERFORIN, MOUSE; PHOSPHOLIPASE C GAMMA; PORE FORMING CYTOTOXIC PROTEIN; PROTEIN BINDING; PROTEIN KINASE ZAP 70; REPRESSOR PROTEIN; TUMOR SUPPRESSOR PROTEIN; ZAP70 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; CD8+ T LYMPHOCYTE; CELL EXPANSION; CELL PROLIFERATION; CELL SURVIVAL; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOLYSIS; GENE; GENE CONTROL; IMMUNE RESPONSE; MOUSE; NONHUMAN; PLCGAMMA1 GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; T LYMPHOCYTE; ADOPTIVE TRANSFER; ANIMAL; ANTIGEN PRESENTATION; APOPTOSIS; C57BL MOUSE; CD4+ T LYMPHOCYTE; CELL CLONE; CYTOLOGY; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY; ENHANCER REGION; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; LISTERIA MONOCYTOGENES; LISTERIOSIS; LYMPHOCYTE ACTIVATION; METABOLISM; MICROBIOLOGY; ORTHOMYXOVIRUS INFECTION; PHYSIOLOGY; SIGNAL TRANSDUCTION; T LYMPHOCYTE SUBPOPULATION; TRANSGENIC MOUSE; TRANSPLANTATION;

ADOPTIVE TRANSFER; ANIMALS; ANTIGEN PRESENTATION; ANTIGENS, CD8; APOPTOSIS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CLONE CELLS; CYTOTOXICITY, IMMUNOLOGIC; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION; GRANZYMES; LISTERIA MONOCYTOGENES; LISTERIOSIS; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; ORTHOMYXOVIRIDAE INFECTIONS; OVALBUMIN; PEPTIDE FRAGMENTS; PHOSPHOLIPASE C GAMMA; PORE FORMING CYTOTOXIC PROTEINS; PROTEIN BINDING; RECEPTORS, ANTIGEN, T-CELL; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, CYTOTOXIC; TUMOR SUPPRESSOR PROTEINS; ZAP-70 PROTEIN-TYROSINE KINASE;

EID: 77955346275     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20092136     Document Type: Article

References (48)

1. Albu, D.I., D. Feng, D. Bhattacharya, N.A. Jenkins, N.G. Copeland, P. Liu, and D. Avram. 2007. BCL11B is required for positive selection and survival of double-positive thymocytes. J. Exp. Med. 204:3003-3015. doi:10.1084/jem. 20070863
2. lck complexes. J. Exp. Med. 194:1485-1495. doi:10.1084/jem.194.10.1485
3. Arlotta, P., B.J. Molyneaux, J. Chen, J. Inoue, R. Kominami, and J.D. Macklis. 2005. Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo. Neuron. 45:207-221. doi:10.1016/j.neuron.2004.12.036
4. Avram, D., A. Fields, K. Pretty On Top, D.J. Nevrivy, J.E. Ishmael, and M. Leid. 2000. Isolation of a novel family of C(2)H(2) zinc finger proteins implicated in transcriptional repression mediated by chicken ovalbumin upstream promoter transcription factor (COUP-TF) orphan nuclear receptors. J. Biol. Chem. 275:10315-10322. doi:10.1074/jbc.275.14.10315
5. Avram, D., A. Fields, T. Senawong, A. Topark-Ngarm, and M. Leid. 2002. COUP-TF (chicken ovalbumin upstream promoter transcription factor)-interacting protein 1 (CTIP1) is a sequence-specific DNA binding protein. Biochem. J. 368:555-563. doi:10.1042/BJ20020496 (Pubitemid 35454533)
6. Bilic, I., C. Koesters, B. Unger, M. Sekimata, A. Hertweck, R. Maschek, C.B. Wilson, and W. Ellmeier. 2006. Negative regulation of CD8 expression via Cd8 enhancer-mediated recruitment of the zinc finger protein MAZR. Nat. Immunol. 7:392-400. doi:10.1038/ni1311
7. Bonvini, E., K.E. DeBell, M.C. Verí, L. Graham, B. Stoica, J. Laborda, M.J. Aman, A. DiBaldassarre, S. Miscia, and B.L. Rellahan. 2003. On the mechanism coupling phospholipase Cgamma1 to the B- and T-cell antigen receptors. Adv. Enzyme Regul. 43:245-269. doi:10.1016/S0065-2571(02)00033-X
8. Cai, Z., and J. Sprent. 1994. Resting and activated T cells display different requirements for CD8 molecules. J. Exp. Med. 179:2005-2015. doi:10.1084/jem.179.6.2005
9. Cannarile, M.A., N.A. Lind, R. Rivera, A.D. Sheridan, K.A. Camfield, B.B. Wu, K.P. Cheung, Z. Ding, and A.W. Goldrath. 2006. Transcriptional regulator Id2 mediates CD8+ T cell immunity. Nat. Immunol. 7:1317-1325. doi:10.1038/ni1403
10. Chen, B., S.S. Wang, A.M. Hattox, H. Rayburn, S.B. Nelson, and S.K. McConnell. 2008. The Fezf2-Ctip2 genetic pathway regulates the fate choice of subcortical projection neurons in the developing cerebral cortex. Proc. Natl. Acad. Sci. USA. 105:11382-11387. doi:10.1073/pnas.0804918105
11. Cismasiu, V.B., K. Adamo, J. Gecewicz, J. Duque, Q. Lin, and D. Avram. 2005. BCL11B functionally associates with the NuRD complex in T lymphocytes to repress targeted promoter. Oncogene. 24:6753-6764. doi:10.1038/sj.onc.1208904
12. Cismasiu, V.B., S. Ghanta, J. Duque, D.I. Albu, H.M. Chen, R. Kasturi, and D. Avram. 2006. BCL11B participates in the activation of IL2 gene expression in CD4+ T lymphocytes. Blood. 108:2695-2702. doi:10.1182/blood-2006-05-021790
13. Cismasiu, V.B., E. Paskaleva, S. Suman Daya, M. Canki, K. Duus, and D. Avram. 2008. BCL11B is a general transcriptional repressor of the HIV-1 long terminal repeat in T lymphocytes through recruitment of the NuRD complex. Virology. 380:173-181. doi:10.1016/j.virol.2008.07.035
14. Cismasiu, V.B., J. Duque, E. Paskaleva, D. Califano, S. Ghanta, H.A. Young, and D. Avram. 2009. BCL11B enhances TCR/CD28-triggered NF-kappaB activation through up-regulation of Cot kinase gene expression in T-lymphocytes. Biochem. J. 417:457-466. doi:10.1042/BJ20080925
15. Crooks, M.E., and D.R. Littman. 1994. Disruption of T lymphocyte positive and negative selection in mice lacking the CD8 beta chain. Immunity. 1:277-285. doi:10.1016/1074-7613(94)90079-5 (Pubitemid 2114856)
16. Cruz-Guilloty, F., M.E. Pipkin, I.M. Djuretic, D. Levanon, J. Lotem, M.G. Lichtenheld, Y. Groner, and A. Rao. 2009. Runx3 and T-box proteins cooperate to establish the transcriptional program of effector CTLs. J. Exp. Med. 206:51-59. doi:10.1084/jem.20081242
17. D'Souza, W.N., C.F. Chang, A.M. Fischer, M. Li, and S.M. Hedrick. 2008. The Erk2 MAPK regulates CD8 T cell proliferation and survival. J. Immunol. 181:7617-7629.
18. Ellmeier, W., M.J. Sunshine, K. Losos, F. Hatam, and D.R. Littman. 1997. An enhancer that directs lineage-specific expression of CD8 in positively selected thymocytes and mature T cells. Immunity. 7:537-547. doi:10.1016/S1074-7613(00)80375-1
19. Ellmeier, W., M.J. Sunshine, K. Losos, and D.R. Littman. 1998. Multiple developmental stage-specific enhancers regulate CD8 expression in developing thymocytes and in thymus-independent T cells. Immunity. 9:485-496. doi:10.1016/S1074-7613(00)80632-9
20. Ellmeier, W., M.J. Sunshine, R. Maschek, and D.R. Littman. 2002. Combined deletion of CD8 locus cis-regulatory elements affects initiation but not maintenance of CD8 expression. Immunity. 16:623-634. doi:10.1016/S1074-7613(02) 00309-6
21. Feik, N., I. Bilic, J. Tinhofer, B. Unger, D.R. Littman, and W. Ellmeier. 2005. Functional and molecular analysis of the double-positive stage-specific CD8 enhancer E8III during thymocyte development. J. Immunol. 174:1513-1524.
22. 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:10.1016/0092-8674(91)90462-8
23. 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
24. Gil, D., A.G. Schrum, M.A. Daniels, and E. Palmer. 2008. A role for CD8 in the developmental tuning of antigen recognition and CD3 conformational change. J. Immunol. 180:3900-3909.
25. Grumont, R., P. Lock, M. Mollinari, F.M. Shannon, A. Moore, and S. Gerondakis. 2004. The mitogen-induced increase in T cell size involves PKC and NFAT activation of Rel/NF-kappaB-dependent c-myc expression. Immunity. 21:19-30. doi:10.1016/j.immuni.2004.06.004
26. Hogquist, K.A., S.C. Jameson, W.R. Heath, J.L. Howard, M.J. Bevan, and F.R. Carbone. 1994. T cell receptor antagonist peptides induce positive selection. Cell. 76:17-27. doi:10.1016/0092-8674(94)90169-4
27. Holler, P.D., and D.M. Kranz. 2003. Quantitative analysis of the contribution of TCR/pepMHC affinity and CD8 to T cell activation. Immunity. 18:255-264. doi:10.1016/S1074-7613(03)00019-0
28. Hostert, A., M. Tolaini, K. Roderick, N. Harker, T. Norton, and D. Kioussis. 1997. A region in the CD8 gene locus that directs expression to the mature CD8 T cell subset in transgenic mice. Immunity. 7:525-536. doi:10.1016/S1074-7613(00)80374-X
29. Ichii, H., A. Sakamoto, M. Hatano, S. Okada, H. Toyama, S. Taki, M. Arima, Y. Kuroda, and T. Tokuhisa. 2002. Role for Bcl-6 in the generation and maintenance of memory CD8+ T cells. Nat. Immunol. 3:558-563. doi:10.1038/ni802
30. Intlekofer, A.M., N. Takemoto, E.J. Wherry, S.A. Longworth, J.T. Northrup, V.R. Palanivel, A.C. Mullen, C.R. Gasink, S.M. Kaech, J.D. Miller, et al. 2005. Effector and memory CD8+ T cell fate coupled by T-bet and eomesodermin. Nat. Immunol. 6:1236-1244. doi:10.1038/ni1268
31. Joshi, N.S., W. Cui, A. Chandele, H.K. Lee, D.R. Urso, J. Hagman, L. Gapin, and S.M. Kaech. 2007. Inflammation directs memory precursor and short-lived effector CD8(+) T cell fates via the graded expression of T-bet transcription factor. Immunity. 27:281-295. doi:10.1016/j.immuni.2007.07.010
32. Kaech, S.M., S. Hemby, E. Kersh, and R. Ahmed. 2002. Molecular and functional profiling of memory CD8 T cell differentiation. Cell. 111:837-851. doi:10.1016/S0092-8674(02)01139-X
33. Kaech, S.M., J.T. Tan, E.J. Wherry, B.T. Konieczny, C.D. Surh, and R. Ahmed. 2003. Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat. Immunol. 4:1191-1198. doi:10.1038/ni1009
34. Kioussis, D., and W. Ellmeier. 2002. Chromatin and CD4, CD8A and CD8B gene expression during thymic differentiation. Nat. Rev. Immunol. 2:909-919. doi:10.1038/nri952 (Pubitemid 37323212)
35. Manders, P.M., P.J. Hunter, A.I. Telaranta, J.M. Carr, J.L. Marshall, M. Carrasco, Y. Murakami, M.J. Palmowski, V. Cerundolo, S.M. Kaech, et al. 2005. BCL6b mediates the enhanced magnitude of the secondary response of memory CD8+ T lymphocytes. Proc. Natl. Acad. Sci. USA. 102:7418-7425. doi:10.1073/pnas. 0501585102
36. Pearce, E.L., A.C. Mullen, G.A. Martins, C.M. Krawczyk, A.S. Hutchins, V.P. Zediak, M. Banica, C.B. DiCioccio, D.A. Gross, C.A. Mao, et al. 2003. Control of effector CD8+ T cell function by the transcription factor Eomesodermin. Science. 302:1041-1043. doi:10.1126/science.1090148
37. Pipkin, M.E., B. Ljutic, F. Cruz-Guilloty, M. Nouzova, A. Rao, J.C. Zúñiga-Pflücker, and M.G. Lichtenheld. 2007. Chromosome transfer activates and delineates a locus control region for perforin. Immunity. 26:29-41. doi:10.1016/j.immuni.2006.11.009
38. Sato, T., S. Ohno, T. Hayashi, C. Sato, K. Kohu, M. Satake, and S. Habu. 2005. Dual functions of Runx proteins for reactivating CD8 and silencing CD4 at the commitment process into CD8 thymocytes. Immunity. 22:317-328. doi:10.1016/j.immuni.2005.01.012
39. Shen, H., M.K. Slifka, M. Matloubian, E.R. Jensen, R. Ahmed, and J.F. Miller. 1995. Recombinant Listeria monocytogenes as a live vaccine vehicle for the induction of protective anti-viral cell-mediated immunity. Proc. Natl. Acad. Sci. USA. 92:3987-3991. doi:10.1073/pnas.92.9.3987
40. Szabo, S.J., B.M. Sullivan, C. Stemmann, A.R. Satoskar, B.P. Sleckman, and L.H. Glimcher. 2002. Distinct effects of T-bet in TH1 lineage commitment and IFN-gamma production in CD4 and CD8 T cells. Science. 295:338-342. doi:10.1126/science.1065543
41. Takemoto, N., A.M. Intlekofer, J.T. Northrup, E.J. Wherry, and S.L. Reiner. 2006. Cutting Edge: IL-12 inversely regulates T-bet and eomesodermin expression during pathogen-induced CD8+ T cell differentiation. J. Immunol. 177:7515-7519.
42. van Stipdonk, M.J., E.E. Lemmens, and S.P. Schoenberger. 2001. Naïve CTLs require a single brief period of antigenic stimulation for clonal expansion and differentiation. Nat. Immunol. 2:423-429.
43. Veillette, A., J.C. Zúñiga-Pflücker, J.B. Bolen, and A.M. Kruisbeek. 1989. Engagement of CD4 and CD8 expressed on immature thymocytes induces activation of intracellular tyrosine phosphorylation pathways. J. Exp. Med. 170:1671-1680. doi:10.1084/jem.170.5.1671 (Pubitemid 19284565)
44. Voskoboinik, I., M.J. Smyth, and J.A. Trapani. 2006. Perforin-mediated target-cell death and immune homeostasis. Nat. Rev. Immunol. 6:940-952. doi:10.1038/nri1983
45. Wakabayashi, Y., J. Inoue, Y. Takahashi, A. Matsuki, H. Kosugi-Okano, T. Shinbo, Y. Mishima, O. Niwa, and R. Kominami. 2003. Homozygous deletions and point mutations of the Rit1/Bcl11b gene in gamma-ray induced mouse thymic lymphomas. Biochem. Biophys. Res. Commun. 301:598-603. doi:10.1016/S0006- 291X(02)03069-3
46. Wilde, J.I., and S.P. Watson. 2001. Regulation of phospholipase C gamma isoforms in haematopoietic cells: why one, not the other? Cell. Signal. 13:691-701. doi:10.1016/S0898-6568(01)00191-7
47. Wildin, R.S., H.U. Wang, K.A. Forbush, and R.M. Perlmutter. 1995. Functional dissection of the murine lck distal promoter. J. Immunol. 155:1286-1295.
48. Zhang, D.J., Q. Wang, J. Wei, G. Baimukanova, F. Buchholz, A.F. Stewart, X. Mao, and N. Killeen. 2005. Selective expression of the Cre recombinase in late-stage thymocytes using the distal promoter of the Lck gene. J. Immunol. 174:6725-6731.