Notch signaling in CD4 and CD8 T cell development

Current Opinion in Immunology

Volumn 20, Issue 2, 2008, Pages 197-202

  Laky, Karen ^a   Fowlkes, B J ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NOTCH RECEPTOR; PRESENILIN; T LYMPHOCYTE RECEPTOR;

CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL FATE; CELL LINEAGE; CELL MATURATION; CELL SELECTION; NONHUMAN; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; THYMOCYTE;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL LINEAGE; MICE; RECEPTORS, ANTIGEN, T-CELL; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; THYMUS GLAND;

EID: 44749092573     PISSN: 09527915     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.coi.2008.03.004     Document Type: Review

References (71)

1. Sundaram M.V. The love-hate relationship between Ras and Notch. Genes Dev 19 (2005) 1825-1839
2. Bray S.J. Notch signalling: a simple pathway becomes complex. Nat Rev Mol Cell Biol 7 (2006) 678-689
3. Fiuza U.M., and Arias A.M. Cell and molecular biology of Notch. J Endocrinol 194 (2007) 459-474
4. Garbe A.I., and von Boehmer H. TCR and Notch synergize in αβ versus γδ lineage choice. Transpl Immunol 28 (2007) 124-131
5. Laky K., Fleischacker C., and Fowlkes B.J. TCR and Notch signaling in CD4 and CD8 T cell development. Immunol Rev 209 (2006) 274-283. The authors further investigate CD4/CD8 T cell development in transgenic mice expressing activated Notch (NICD). In several TCR transgenic lines with NICD, development of SP thymocytes is blocked. Surprisingly, there is no evidence of Notch re-directing lineage choice as observed with the diverse TCR repertoire. DP thymocytes show increased expression of activation/maturation markers ex vivo and respond as well or better than controls to TCR stimulation in vitro. The results suggest that Notch and TCR signaling are functionally linked in developing T cells.
6. Kovall R.A. Structures of CSL, Notch and Mastermind proteins: piecing together an active transcription complex. Curr Opin Struct Biol 17 (2007) 117-127
7. Fang T.C., Yashiro-Ohtani Y., del Bianco C., Knoblock D.M., Blacklow S.C., and Pear W.S. Notch directly regulates Gata3 expression during T helper 2 cell differentiation. Immunity 27 (2007) 100-110
8. Krejci A., and Bray S. Notch activation stimulates transient and selective binding of Su(H)/CSL to target enhancers. Genes Dev 21 (2007) 1322-1327. Although CSL is thought to act as a default repressor of Notch signaling, this study shows that CSL occupancy of target enhancers is not always constitutive, and for some genes, CSL binding to DNA is induced only after Notch activation.
9. Shawber C., Nofziger D., Hsieh J.J., Lindsell C., Bogler O., Hayward D., and Weinmaster G. Notch signaling inhibits muscle cell differentiation through a CBF1-independent pathway. Development 122 (1996) 3765-3773
10. Wilson-Rawls J., Molkentin J.D., Black B.L., and Olson E.N. Activated Notch inhibits myogenic activity of the MADS-Box transcription factor myocyte enhancer factor 2C. Mol Cell Biol 19 (1999) 2853-2862
11. Sade H., Krishna S., and Sarin A. The anti-apoptotic effect of Notch-1 requires p56lck-dependent, Akt/PKB-mediated signaling in T cells. J Biol Chem 279 (2004) 2937-2944
12. Guan E., Wang J., Laborda J., Norcross M., Baeuerle P.A., and Hoffman T. T cell leukemia-associated human Notch/translocation-associated Notch homologue has I kappa B-like activity and physically interacts with nuclear factor-kappa B proteins in T cells. J Exp Med 183 (1996) 2025-2032
13. Chang D., Valdez P., Ho T., and Robey E. MHC recognition in thymic development: Distinct, parallel pathways for survival and lineage commitment. J Immunol 165 (2000) 6710-6715
14. Deftos M.L., Huang E., Ojala E.W., Forbush K.A., and Bevan M.J. Notch1 signaling promotes the maturation of CD4 and CD8 SP thymocytes. Immunity 13 (2000) 73-84
15. Iso T., Sartorelli V., Chung G., Shichinohe T., Kedes L., and Hamamori Y. HERP, a new primary target of Notch regulated by ligand binding. Mol Cell Biol 21 (2001) 6071-6079
16. Deftos M.L., He Y.W., Ojala E.W., and Bevan M.J. Correlating Notch signaling with thymocyte maturation. Immunity 9 (1998) 777-786
17. Campese A.F., Garbe A.I., Zhang F., Grassi F., Screpanti I., and von Boehmer H. Notch1-dependent lymphomagenesis is assisted by but does not essentially require pre-TCR signaling. Blood 108 (2006) 305-310
18. Pirot P., Grunsven L.A., Marine J.C., Huylebroeck D., and Bellefroid E.J. Direct regulation of the Nrarp gene promoter by the Notch signaling pathway. Biochem Biophys Res Comm 322 (2004) 526-534
19. Maillard I., Tu L., Sambandam A., Yashiro-Ohtani Y., Millholland J., Keeshan K., Shestova O., Xu L., Bhandoola A., and Pear W.S. The requirement for Notch signaling at the β-selection checkpoint in vivo is absolute and independent of the pre-T cell receptor. J Exp Med 203 (2006) 2239-2245. Expression of a dominant negative form of MAML (dnMAML) is conditionally induced in thymocytes using pLck-Cre. dnMAML inhibits the DN to DP stage transition, which cannot be rescued by expression of TCRβ or TCRαβ transgenes. The results reveal a requirement for Notch at the β-selection checkpoint independent of any effect on gene rearrangement/expression of the pre-TCR.
20. Amsen D., Blander J.M., Lee G.R., Tanigaki K., Honjo T., and Flavell R.A. Instruction of distinct CD4 T helper cell fates by different Notch ligands on antigen-presenting cells. Cell 117 (2004) 515-526
21. Tanaka S., Tsukada J., Suzuki W., Hayashi K., Tanigaki K., Tsuji M., Inoue H., Honjo T., and Kubo M. The Interleukin-4 enhancer CNS-2 is regulated by Notch signals and controls initial expression in NKT cells and memory-type CD4 T cells. Immunity 24 (2006) 689-701
22. Minter L.M., Turley D.M., Das P., Shin H.M., Joshi I., Lawlor R.G., Cho O.H., Palaga T., Gottipati S., Telfer J.C., et al. Inhibitors of gamma-secretase block in vivo and in vitro T helper type 1 polarization by preventing Notch upregulation of Tbx21. Nat Immunol 6 (2005) 680-688
23. Amsen D., Antov A., Jankovic D., Sher A., Radtke F., Souabni A., Busslinger M., McCright B., Gridley T., and Flavell R.A. Direct regulation of Gata3 expression determines the T helper differentiation potential of Notch. Immunity 27 (2007) 89-99
24. Koch U., Yuan J.S., Harper J.A., and Guidos C.J. Fine-tuning Notch1 activation by endocytosis and glycosylation. Semin Immunol 15 (2003) 99-106
25. McGill M.A., and McGlade C.J. Mammalian Numb proteins promote Notch1 receptor ubiquitination and degradation of the Notch1 intracellular domain. J Biol Chem 278 (2003) 23196-23203
26. Anderson A.C., Kitchens E.A., Chan S.W., Hill C.S., Jan Y.N., Zhong W.M., and Robey E.A. The Notch regulator Numb links the Notch and TCR signaling pathways. J Immunol 174 (2005) 890-897. This study demonstrates an association of Numb (a well characterized antagonist of Notch signaling) with components of TCR signal transduction in thymocytes and mature T cells. Although Numb and Notch physically associate with the TCR complex upon antigen stimulation, thymocyte development is unperturbed in the absence of Numb.
27. Wilson A., Ardiet D.L., Saner C., Vilain N., Beermann F., Aguet M., MacDonald H.R., and Zilian O. Normal hemopoiesis and lymphopoiesis in the combined absence of Numb and Numblike. J Immunol 178 (2007) 6746-6751. Although Numb-deficiency has no adverse affect on T cell development, it was possible that Numblike, a Numb homologue, functionally compensated for Numb. This paper demonstrates that hematopoiesis and T cell development proceed normally in the absence of both Numb and Numblike.
28. Izon D.J., Aster J.C., He Y.P., Weng A., Karnell F.G., Patriub V., Xu L.W., Bakkour S., Rodriguez C., Allman D., et al. Deltex1 redirects lymphoid progenitors to the B cell lineage by antagonizing Notch1. Immunity 16 (2002) 231-243
29. Matsuno K, Diederich R.J., Go MJ, Blaumueller CM, Artavanis-Tsakonas S: Deltex acts as a positive regulator of Notch signaling through interactions with the Notch Ankrin repeats. Development 1995, 121:2633-2644.
30. Lehar S.M., and Bevan M.J. T cells develop normally in the absence of both Deltex1 and Deltex2. Mol Cell Biol 26 (2006) 7358-7371. Germline deletion of both Deltex1 and Deltex2 genes has no impact on thymocyte development. Nevertheless, the authors conclude from experiments in which expression of all Deltex forms are reduced that Deltex can negatively regulate Notch signaling in thymocyte progenitors.
31. Onoyama I., Tsunematsu R., Matsumoto A., Kimura T., de Alboran I.M., Nakayama K., and Nakayama K.I. Conditional inactivation of Fbxw7 impairs cell-cycle exit during T cell differentiation and results in lymphomatogenesis. J Exp Med 204 (2007) 2875-2888
32. Kitamoto T., Takahashi K., Takimoto H., Tomizuka K., Hayasaka M., Tabira T., and Hanaoka K. Functional redundancy of the Notch gene family during mouse embryogenesis: Analysis of Notch gene expression in Notch3-deficient mice. Biochem Biophys Res Comm 331 (2005) 1154-1162
33. Vercauteren S.M., and Sutherland H.J. Constitutively active Notch4 promotes early human hematopoietic progenitor cell maintenance while inhibiting differentiation and causes lymphoid abnormalities in vivo. Blood 104 (2004) 2315-2322
34. Krebs L.T., Xue Y., Norton C.R., Shutter J.R., Maguire M., Sundberg J.P., Gallahan D., Closson V., Kitajewski J., Callahan R., et al. Notch signaling is essential for vascular morphogenesis in mice. Genes Dev 14 (2000) 1343-1352
35. Wolfer A., Bakker T., Wilson A., Nicolas M., Ioannidis V., Littman D.R., Wilson C.B., Held W., MacDonald H.R., and Radtke F. Inactivation of Notch I in immature thymocytes does not perturb CD4 or CD8T cell development. Nature 2 (2001) 235-241
36. Tanigaki K., Tsuji M., Yamamoto N., Han H., Tsukada J., Inoue H., Kubo M., and Honjo T. Regulation of αβ/γδT cell lineage commitment and peripheral T cell responses by Notch/RBP-J signaling. Immunity 20 (2004) 611-622
37. Tu L., Fang T.C., Artis D., Shestova O., Pross S.E., Maillard I., and Pear W.S. Notch signaling is an important regulator of type 2 immunity. J Exp Med 202 (2005) 1037-1042. Expression of dnMAML is conditionally induced in thymocytes using Cd4-Cre. Thymocyte development and T cell activation are normal, but IL-4 production and protective Th2 responses to helminth infection are impaired.
38. Laky K., and Fowlkes B.J. Presenilins regulate αβ T cell development by modulating TCR signaling. J Exp Med 204 (2007) 2115-2129. Notch signaling is inhibited in thymocytes by germline deletion of the Presenilin2 gene and conditional deletion of Presenilin1 gene mediated by Cd4-Cre. Impaired positive selection and maturation of SP thymocytes correlates with attenuated TCR signal transduction in DP thymocytes. The authors conclude that Notch potentiates TCR signaling in the positive selection and development of αβ T cells but plays no role in CD4/CD8 T lineage commitment.
39. Bray S. A Notch affair. Cell 93 (1998) 499-503
40. Ciofani M., Schmitt T.M., Ciofani A., Michie A.M., Cuburu N., Aublin A., Maryanski J.L., and Zuniga-Pflucker J.C. Obligatory role for cooperative signaling by pre-TCR and notch during thymocyte differentiation. J Immunol 172 (2004) 5230-5239
41. L. TCR activation was not investigated.
42. Oyama T., Harigaya K., Muradil A., Hozumi K., Habu S., Oguro H., Iwama A., Matsuno K., Sakamoto R., Sato M., et al. Mastermind-1 is required for Notch signal-dependent steps in lymphocyte development in vivo. Proc Natl Acad Sci U S A 104 (2007) 9764-9769. Germline deletion of the MAML1 gene causes growth retardation and early death. Marginal zone B cell development is abrogated, and there is a partial block at the DN to DP stage of thymocyte development.
43. Prevorovsky M., Puta F., and Folk P. Fungal CSL transcription factors. BMC Genomics 8 (2007) 233
44. Beres T.M., Masui T., Swift G.H., Shi L., Henke R.M., and MacDonald R.J. PTF1 Is an organ-specific and Notch-independent basic helix-loop-helix complex containing the mammalian suppressor of hairless (RBP-J) or its paralogue, RBP-L. Mol Cell Biol 26 (2006) 117-130
45. Bray S., and Furriols M. Notch pathway: Making sense of suppressor of hairless. Curr Biol 11 (2001) R217-R221
46. Shen H., McElhinny A.S., Cao Y., Gao P., Liu J., Bronson R., Griffin J.D., and Wu L. The Notch coactivator, MAML1, functions as a novel coactivator for MEF2C-mediated transcription and is required for normal myogenesis. Genes Dev 20 (2006) 675-688
47. Zhao Y., Katzman R.B., Delmolino L.M., Bhat I., Zhang Y., Gurumurthy C.B., Germaniuk-Kurowska A., Reddi H.V., Solomon A., Zeng M.S., et al. The Notch Regulator MAML1 Interacts with p53 and functions as a coactivator. J Biol Chem 282 (2007) 11969-11981
48. Selkoe D.J., and Wolfe M.S. Presenilin: Running with scissors in the membrane. Cell 131 (2007) 215-221
49. Doroquez D.B., and Rebay I. Signal integration during development: Mechanisms of EGFR and Notch pathway function and cross-talk. Crit Rev Biochem Mol Biol 41 (2006) 339-385
50. Osborne B.A., and Minter L.M. Notch signaling during peripheral T-cell activation and differentiation. Nat Rev Immunol 7 (2007) 64-75
51. Benson R.A., Adamson K., Corsin-Jimenez M., Marley J.V., Wahl K., Lamb J.R., and Howie S.E.M. Notch1 co-localizes with CD4 on activated T cells and Notch signaling is required for IL-10 production. Eur J Immunol 35 (2005) 859-869
52. Huang Y.H., Li D., Winoto A., and Robey E.A. Distinct transcriptional programs in thymocytes responding to T cell receptor, Notch, and positive selection signals. Proc Natl Acad Sci U S A 101 (2004) 4936-4941
53. + thymocytes by modulating TCR signal strength. Immunity 14 (2001) 253-264
54. van den Brandt J., Kwon S.H., Hunig T., McPherson K.G., and Reichardt H.M. Sustained pre-TCR expression in Notch1IC-transgenic rats impairs T cell maturation and selection. J Immunol 174 (2005) 7845-7852. Development of SP thymocytes is compromised in rats expressing a NICD transgene driven by the pLck promoter. The authors propose that defective development is because of prolonged expression of the pre-TCR in DP thymocytes, resulting in alterations in RAG and TCRαβ expression.
55. Adler S.H., Chiffoleau E., Xu L., Dalton N.M., Burg J.M., Wells A.D., Wolfe M.S., Turka L.A., and Pear W.S. Notch signaling augments T cell responsiveness by enhancing CD25 expression. J Immunol 171 (2003) 2896-2903
56. Palaga T., Miele L., Golde T.E., and Osborne B.A. TCR-mediated Notch signaling regulates proliferation and IFNγ production in peripheral T cells. J Immunol 171 (2003) 3019-3024
57. Rottinger E., Croce J., Lhomond G., Besnardeau L., Gache C., and Lepage T. Nemo-like kinase (NLK) acts downstream of Notch/Delta signalling to downregulate TCF during mesoderm induction in the sea urchin embryo. Development 133 (2006) 4341-4353
58. Kondoh K., Sunadome K., and Nishida E. Notch signaling suppresses p38 MAPK activity via induction of MKP-1 in myogenesis. J Biol Chem 282 (2007) 3058-3065
59. Liu Z.J., Xiao M., Balint K., Soma A., Pinnix C.C., Capobianco A.J., Velazquez O.C., and Herlyn M. Inhibition of endothelial cell proliferation by Notch1 signaling is mediated by repressing MAPK and PI3K/Akt pathways and requires MAML1. FASEB J 20 (2006) 1009-1011
60. Whelan J., Forbes S.L., and Bertrand F.E. CBF-1 (RBP-Jk) binds to the PTEN promoter and regulates PTEN gene expression. Cell Cycle 6 (2007) 80-84
61. McKenzie G., Ward G., Stallwood Y., Briend E., Papadia S., Lennard A., Turner M., Champion B., and Hardingham G.E. Cellular Notch resonsiveness is defined by pohosphoinositide 3-kinase dependent signals. BMC Cell Biol 7 (2006) 10
62. Kelly A., Finlay D., Hinton H.J., Clarke R.G., Fiorini E., Radtke F., and Cantrell D.A. Notch-induced T cell development requires phosphoinositide-dependent kinase 1. EMBO J 26 (2007) 3441-3450
63. Mammucari C., di Vignano A.T., Sharov A.A., Neilson J., Havrda M.C., Roop D.R., Botchkarev V.A., Crabtree G.R., and Dotto G.P. Integration of Notch 1 and calcineurin/NFAT signaling pathways in keratinocyte growth and differentiation control. Dev Cell 8 (2005) 665-676
64. Moran S.T., Cariappa A., Liu H., Muir B., Sgroi D., Boboila C., and Pillai S. Synergism between NF-κB1/p50 and Notch2 during the development of marginal zone B lymphocytes. J Immunol 179 (2007) 195-200
65. Shin H.M., Minter H.M., Cho O.H., Gottipati S., Fauq A.H., Golde T.E., Sonenshein G.E., and Osborne B.A. Notch1 augments NF-kB activity by facilitating its nuclear retention. EMBO J 25 (2006) 129-138
66. Wang T., Holt C.M., Xu C., Ridley C., Jones P.O., Baron M., and Trump D. Notch3 activation modulates cell growth behaviour and cross-talk to Wnt/TCF signalling pathway. Cell Signal 19 (2007) 2458-2467
67. Fowlkes B.J., and Robey E.A. A reassessment of the effect of activated Notch1 on CD4 and CD8 T cell development. J Immunol 169 (2002) 1817-1821
68. Robey E, Chang D, Itano A, Cado D, Alexander H, Lans D, Weinmaster G, Salmon P: An activated form of Notch influences the choice between CD4 and CD8 T cell lineages. Cell 1996, 87:483-492.
69. Doerfler P., Shearman M.S., and Perlmutter R.M. Presenilin-dependent γ-secretase activity modulates thymocyte development. Proc Natl Acad Sci U S A 98 (2001) 9312-9317
70. Hadland B.K., Manley N.R., Su D., Longmore G.D., Moore C.L., Wolfe M.S., Schroeter E.H., and Kopan R. γ-Secretase inhibitors repress thymocyte development. Proc Natl Acad Sci U S A 98 (2001) 7487-7491
71. Kopan R. All good things must come to an end: How is Notch signaling turned off?. Sci STKE 9 (1999) PE1