Upregulation of CD4 Expression during MHC Class II-Specific Positive Selection Is Essential for Error-free Lineage Choice

Immunity

Volumn 31, Issue 3, 2009, Pages 480-490

  Sarafova, Sophia D ^a,c   Van Laethem, Francois ^a   Adoro, Stanley ^a   Guinter, Terry ^a   Sharrow, Susan O ^a   Feigenbaum, Lionel ^b   Singer, Alfred ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b SAIC FREDERICK INC   (United States)

^c DAVIDSON COLLEGE   (United States)

Author keywords

CELLIMMUNO; MOLIMMUNO

Indexed keywords

CD4 ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ANTIGEN EXPRESSION; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; FLOW CYTOMETRY; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; THYMOCYTE; TRANSGENIC MOUSE; UPREGULATION;

ANIMALS; ANTIGENS, CD4; CD4-POSITIVE T-LYMPHOCYTES; CELL LINEAGE; CORE BINDING FACTOR ALPHA 3 SUBUNIT; HISTOCOMPATIBILITY ANTIGENS CLASS II; LIGANDS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; THYMUS GLAND; UP-REGULATION;

EID: 70049095432     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2009.07.006     Document Type: Article

References (42)

1. Adoro S., Erman B., Sarafova S.D., Van Laethem F., Park J.H., Feigenbaum L., and Singer A. Targeting CD4 coreceptor expression to postselection thymocytes reveals that CD4/CD8 lineage choice is neither error-prone nor stochastic. J. Immunol. 181 (2008) 6975-6983
2. Aliahmad P., and Kaye J. Development of all CD4 T lineages requires nuclear factor TOX. J. Exp. Med. 205 (2008) 245-256
3. Bosselut R., Guinter T.I., Sharrow S.O., and Singer A. Unraveling a revealing paradox: Why major histocompatibility complex I-signaled thymocytes "paradoxically" appear as CD4+8lo transitional cells during positive selection of CD8+ T cells. J. Exp. Med. 197 (2003) 1709-1719
4. Brugnera E., Bhandoola A., Cibotti R., Yu Q., Guinter T.I., Yamashita Y., Sharrow S.O., and Singer A. Coreceptor reversal in the thymus: Signaled CD4+8+ thymocytes initially terminate CD8 transcription even when differentiating into CD8+ T cells. Immunity 13 (2000) 59-71
5. Cibotti R., Bhandoola A., Guinter T.I., Sharrow S.O., and Singer A. CD8 coreceptor extinction in signaled CD4(+)CD8(+) thymocytes: Coordinate roles for both transcriptional and posttranscriptional regulatory mechanisms in developing thymocytes. Mol. Cell. Biol. 20 (2000) 3852-3859
6. Dave V.P., Allman D., Keefe R., Hardy R.R., and Kappes D.J. HD mice: A novel mouse mutant with a specific defect in the generation of CD4(+) T cells. Proc. Natl. Acad. Sci. USA 95 (1998) 8187-8192
7. Davis C.B., Killeen N., Crooks M.E., Raulet D., and Littman D.R. Evidence for a stochastic mechanism in the differentiation of mature subsets of T lymphocytes. Cell 73 (1993) 237-247
8. Egawa T., Tillman R.E., Naoe Y., Taniuchi I., and Littman D.R. The role of the Runx transcription factors in thymocyte differentiation and in homeostasis of naive T cells. J. Exp. Med. 204 (2007) 1945-1957
9. Ellmeier W., Sunshine M.J., Losos K., and Littman D.R. Multiple developmental stage-specific enhancers regulate CD8 expression in developing thymocytes and in thymus-independent T cells. Immunity 9 (1998) 485-496
10. Ellmeier W., Sawada S., and Littman D.R. The regulation of CD4 and CD8 coreceptor gene expression during T cell development. Annu. Rev. Immunol. 17 (1999) 523-554
11. He X., and Kappes D.J. CD4/CD8 lineage commitment: Light at the end of the tunnel?. Curr. Opin. Immunol. 18 (2006) 135-142
12. He X., Dave V.P., Zhang Y., Hua X., Nicolas E., Xu W., Roe B.A., and Kappes D.J. The zinc finger transcription factor Th-POK regulates CD4 versus CD8 T-cell lineage commitment. Nature 433 (2005) 826-833
13. He X., Park K., Wang H., He X., Zhang Y., Hua X., Li Y., and Kappes D.J. CD4-CD8 lineage commitment is regulated by a silencer element at the ThPOK transcription-factor locus. Immunity 28 (2008) 346-358
14. Hedrick S.M. Thymus lineage commitment: A single switch. Immunity 28 (2008) 297-299
15. Hernandez-Hoyos G., Anderson M.K., Wang C., Rothenberg E.V., and Alberola-Ila J. GATA-3 expression is controlled by TCR signals and regulates CD4/CD8 differentiation. Immunity 19 (2003) 83-94
16. Huesmann M., Scott B., Kisielow P., and von Boehmer H. Kinetics and efficacy of positive selection in the thymus of normal and T cell receptor transgenic mice. Cell 66 (1991) 533-540
17. Itano A., and Robey E. Highly efficient selection of CD4 and CD8 lineage thymocytes supports an instructive model of lineage commitment. Immunity 12 (2000) 383-389
18. Itano A., Salmon P., Kioussis D., Tolaini M., Corbella P., and Robey E. The cytoplasmic domain of CD4 promotes the development of CD4 lineage T cells. J. Exp. Med. 183 (1996) 731-741
19. Kaye J., Hsu M.L., Sauron M.E., Jameson S.C., Gascoigne N.R., and Hedrick S.M. Selective development of CD4+ T cells in transgenic mice expressing a class II MHC-restricted antigen receptor. Nature 341 (1989) 746-749
20. Kioussis D., and Ellmeier W. Chromatin and CD4, CD8A and CD8B gene expression during thymic differentiation. Nat. Rev. Immunol. 2 (2002) 909-919
21. Lee N.A., Loh D.Y., and Lacy E. CD8 surface levels alter the fate of alpha/beta T cell receptor-expressing thymocytes in transgenic mice. J. Exp. Med. 175 (1992) 1013-1025
22. Leung R.K., Thomson K., Gallimore A., Jones E., Van den Broek M., Sierro S., Alsheikhly A.R., McMichael A., and Rahemtulla A. Deletion of the CD4 silencer element supports a stochastic mechanism of thymocyte lineage commitment. Nat. Immunol. 2 (2001) 1167-1173
23. Lucas B., and Germain R.N. Unexpectedly complex regulation of CD4/CD8 coreceptor expression supports a revised model for CD4+CD8+ thymocyte differentiation. Immunity 5 (1996) 461-477
24. Matechak E.O., Killeen N., Hedrick S.M., and Fowlkes B.J. MHC class II-specific T cells can develop in the CD8 lineage when CD4 is absent. Immunity 4 (1996) 337-347
25. Sant'Angelo D.B., Lucas B., Waterbury P.G., Cohen B., Brabb T., Goverman J., Germain R.N., and Janeway Jr. C.A. A molecular map of T cell development. Immunity 9 (1998) 179-186
26. Sarafova S.D., Erman B., Yu Q., Van Laethem F., Guinter T., Sharrow S.O., Feigenbaum L., Wildt K.F., Ellmeier W., and Singer A. Modulation of coreceptor transcription during positive selection dictates lineage fate independently of TCR/coreceptor specificity. Immunity 23 (2005) 75-87
27. Sato T., Ohno S., Hayashi T., Sato C., Kohu K., Satake M., and Habu S. Dual functions of Runx proteins for reactivating CD8 and silencing CD4 at the commitment process into CD8 thymocytes. Immunity 22 (2005) 317-328
28. Sawada S., Scarborough J.D., Killeen N., and Littman D.R. A lineage-specific transcriptional silencer regulates CD4 gene expression during T lymphocyte development. Cell 77 (1994) 917-929
29. Setoguchi R., Tachibana M., Naoe Y., Muroi S., Akiyama K., Tezuka C., Okuda T., and Taniuchi I. Repression of the transcription factor Th-POK by Runx complexes in cytotoxic T cell development. Science 319 (2008) 822-825
30. Singer A. New perspectives on a developmental dilemma: The kinetic signaling model and the importance of signal duration for the CD4/CD8 lineage decision. Curr. Opin. Immunol. 14 (2002) 207-215
31. Singer A., and Bosselut R. CD4/CD8 coreceptors in thymocyte development, selection, and lineage commitment: Analysis of the CD4/CD8 lineage decision. Adv. Immunol. 83 (2004) 91-131
32. Singer A., Adoro S., and Park J.H. Lineage fate and intense debate: Myths, models and mechanisms of CD4- versus CD8-lineage choice. Nat. Rev. Immunol. 8 (2008) 788-801
33. Starr T.K., Jameson S.C., and Hogquist K.A. Positive and negative selection of T cells. Annu. Rev. Immunol. 21 (2003) 139-176
34. Sun G., Liu X., Mercado P., Jenkinson S.R., Kypriotou M., Feigenbaum L., Galera P., and Bosselut R. The zinc finger protein cKrox directs CD4 lineage differentiation during intrathymic T cell positive selection. Nat. Immunol. 6 (2005) 373-381
35. Taniuchi I., Osato M., Egawa T., Sunshine M.J., Bae S.C., Komori T., Ito Y., and Littman D.R. Differential requirements for Runx proteins in CD4 repression and epigenetic silencing during T lymphocyte development. Cell 111 (2002) 621-633
36. Taniuchi I., Ellmeier W., and Littman D.R. The CD4/CD8 lineage choice: New insights into epigenetic regulation during T cell development. Adv. Immunol. 83 (2004) 55-89
37. Tyznik A.J., Sun J.C., and Bevan M.J. The CD8 population in CD4-deficient mice is heavily contaminated with MHC class II-restricted T cells. J. Exp. Med. 199 (2004) 559-565
38. Van Laethem F., Sarafova S.D., Park J.H., Tai X., Pobezinsky L., Guinter T.I., Adoro S., Adams A., Sharrow S.O., Feigenbaum L., and Singer A. Deletion of CD4 and CD8 coreceptors permits generation of alphabetaT cells that recognize antigens independently of the MHC. Immunity 27 (2007) 735-750
39. Wang L., Wildt K.F., Zhu J., Zhang X., Feigenbaum L., Tessarollo L., Paul W.E., Fowlkes B.J., and Bosselut R. Distinct functions for the transcription factors GATA-3 and ThPOK during intrathymic differentiation of CD4(+) T cells. Nat. Immunol. 9 (2008) 1122-1130
40. Wilkinson B., Chen J.Y., Han P., Rufner K.M., Goularte O.D., and Kaye J. TOX: An HMG box protein implicated in the regulation of thymocyte selection. Nat. Immunol. 3 (2002) 272-280
41. Wong P., Goldrath A.W., and Rudensky A.Y. Competition for specific intrathymic ligands limits positive selection in a TCR transgenic model of CD4+ T cell development. J. Immunol. 164 (2000) 6252-6259
42. Yasutomo K., Doyle C., Miele L., Fuchs C., and Germain R.N. The duration of antigen receptor signalling determines CD4+ versus CD8+ T-cell lineage fate. Nature 404 (2000) 506-510