The different faces of Notch in T-helper-cell differentiation (original) (raw)
Weaver, C. T., Hatton, R. D., Mangan, P. R. & Harrington, L. E. IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu. Rev. Immunol.25, 821–852 (2007). ArticleCASPubMed Google Scholar
Abbas, A. K., Murphy, K. M. & Sher, A. Functional diversity of helper T lymphocytes. Nature383, 787–793 (1996). ArticleCASPubMed Google Scholar
Kapsenberg, M. L. Dendritic-cell control of pathogen-driven T-cell polarization. Nature Rev. Immunol.3, 984–993 (2003). ArticleCAS Google Scholar
Brombacher, F. et al. IL-12 is dispensable for innate and adaptive immunity against low doses of Listeria monocytogenes. Int. Immunol.11, 325–332 (1999). ArticleCASPubMed Google Scholar
Kaplan, M. H., Wurster, A. L. & Grusby, M. J. A signal transducer and activator of transcription (Stat)4-independent pathway for the development of T helper type 1 cells. J. Exp. Med.188, 1191–1196 (1998). ArticleCASPubMedPubMed Central Google Scholar
Magram, J. et al. IL-12-deficient mice are defective in IFNγ production and type 1 cytokine responses. Immunity4, 471–481 (1996). ArticleCASPubMed Google Scholar
Thierfelder, W. E. et al. Requirement for Stat4 in interleukin-12-mediated responses of natural killer and T cells. Nature382, 171–174 (1996). ArticleCASPubMed Google Scholar
Jankovic, D. et al. In the absence of IL-12, CD4+ T cell responses to intracellular pathogens fail to default to a Th2 pattern and are host protective in an IL-10−/− setting. Immunity16, 429–439 (2002). ArticleCASPubMed Google Scholar
Mullen, A. C. et al. Role of T-bet in commitment of TH1 cells before IL-12-dependent selection. Science292, 1907–1910 (2001). ArticleCASPubMed Google Scholar
Trembleau, S. et al. Pancreas-infiltrating Th1 cells and diabetes develop in IL-12-deficient nonobese diabetic mice. J. Immunol.163, 2960–2968 (1999). CASPubMed Google Scholar
de Wit, M. C., Horzinek, M. C., Haagmans, B. L. & Schijns, V. E. Host-dependent type 1 cytokine responses driven by inactivated viruses may fail to default in the absence of IL-12 or IFN-α/β. J. Gen. Virol.85, 795–803 (2004). ArticleCASPubMed Google Scholar
Oxenius, A., Karrer, U., Zinkernagel, R. M. & Hengartner, H. IL-12 is not required for induction of type 1 cytokine responses in viral infections. J. Immunol.162, 965–973 (1999). CASPubMed Google Scholar
Schijns, V. E. et al. Mice lacking IL-12 develop polarized Th1 cells during viral infection. J. Immunol.160, 3958–3964 (1998). References 9–14, together with reference 5, show that there are IL-12-independent pathways for the induction of TH1-cell responses CASPubMed Google Scholar
Shimoda, K. et al. Lack of IL-4-induced Th2 response and IgE class switching in mice with disrupted Stat6 gene. Nature380, 630–633 (1996). ArticleCASPubMed Google Scholar
Finkelman, F. D. et al. Stat6 regulation of in vivo IL-4 responses. J. Immunol.164, 2303–2310 (2000). ArticleCASPubMed Google Scholar
Jankovic, D. et al. Single cell analysis reveals that IL-4 receptor/Stat6 signaling is not required for the in vivo or in vitro development of CD4+ lymphocytes with a Th2 cytokine profile. J. Immunol.164, 3047–3055 (2000). ArticleCASPubMed Google Scholar
Voehringer, D., Reese, T. A., Huang, X., Shinkai, K. & Locksley, R. M. Type 2 immunity is controlled by IL-4/IL-13 expression in hematopoietic non-eosinophil cells of the innate immune system. J. Exp. Med.203, 1435–1446 (2006). ArticleCASPubMedPubMed Central Google Scholar
King, S. B., Knorn, A. M., Ohnmacht, C. & Voehringer, D. Accumulation of effector CD4 T cells during type 2 immune responses is negatively regulated by Stat6. J. Immunol.180, 754–763 (2008). References 17–20 show that IL-4-independent signals exist for the induction of TH2-cell responses. ArticleCASPubMed Google Scholar
Sporri, R. & Reis e Sousa, C. Inflammatory mediators are insufficient for full dendritic cell activation and promote expansion of CD4+ T cell populations lacking helper function. Nature Immunol.6, 163–170 (2005). ArticleCAS Google Scholar
Bray, S. J. Notch signalling: a simple pathway becomes complex. Nature Rev. Mol. Cell Biol.7, 678–689 (2006). ArticleCAS Google Scholar
Artavanis-Tsakonas, S., Rand, M. D. & Lake, R. J. Notch signaling: cell fate control and signal integration in development. Science284, 770–776 (1999). ArticleCASPubMed Google Scholar
Adler, S. H. et al. Notch signaling augments T cell responsiveness by enhancing CD25 expression. J. Immunol.171, 2896–2903 (2003). ArticleCASPubMed Google Scholar
Amsen, D. et al. Instruction of distinct CD4 T helper cell fates by different Notch ligands on antigen-presenting cells. Cell117, 515–526 (2004). This article shows that different Notch ligands elicit different outcomes in TH-cell differentiation and demonstrates that Notch directly controls the transcription ofIl4. ArticleCASPubMed Google Scholar
Kato, H. et al. Functional conservation of mouse Notch receptor family members. FEBS Lett.395, 221–224 (1996). ArticleCASPubMed Google Scholar
Ong, C. T. et al. Target selectivity of vertebrate Notch proteins. Collaboration between discrete domains and CSL-binding site architecture determines activation probability. J. Biol. Chem.281, 5106–5119 (2006). ArticleCASPubMed Google Scholar
Shimizu, K. et al. Binding of Delta1, Jagged1, and Jagged2 to Notch2 rapidly induces cleavage, nuclear translocation, and hyperphosphorylation of Notch2. Mol. Cell. Biol.20, 6913–6922 (2000). ArticleCASPubMedPubMed Central Google Scholar
Huppert, S. S., Jacobsen, T. L. & Muskavitch, M. A. Feedback regulation is central to Delta–Notch signalling required for Drosophila wing vein morphogenesis. Development124, 3283–3291 (1997). CASPubMed Google Scholar
Jaleco, A. C. et al. Differential effects of Notch ligands Delta-1 and Jagged-1 in human lymphoid differentiation. J. Exp. Med.194, 991–1002 (2001). ArticleCASPubMedPubMed Central Google Scholar
Cheng, P., Nefedova, Y., Corzo, C. A. & Gabrilovich, D. I. Regulation of dendritic-cell differentiation by bone marrow stroma via different Notch ligands. Blood109, 507–515 (2007). ArticleCASPubMedPubMed Central Google Scholar
Napolitani, G., Rinaldi, A., Bertoni, F., Sallusto, F. & Lanzavecchia, A. Selected Toll-like receptor agonist combinations synergistically trigger a T helper type 1-polarizing program in dendritic cells. Nature Immunol.6, 769–776 (2005). ArticleCAS Google Scholar
Skokos, D. & Nussenzweig, M. C. CD8− DCs induce IL-12-independent Th1 differentiation through Delta 4 Notch-like ligand in response to bacterial LPS. J. Exp. Med.204, 1525–1531 (2007). This article shows that the TH1-cell inducing role of DLLs is most prominent in IL-12-independent responses. ArticleCASPubMedPubMed Central Google Scholar
Rudd, B. D. et al. MyD88-mediated instructive signals in dendritic cells regulate pulmonary immune responses during respiratory virus infection. J. Immunol.178, 5820–5827 (2007). ArticleCASPubMed Google Scholar
Sun, J., Krawczyk, C. J. & Pearce, E. J. Suppression of Th2 cell development by Notch ligands Delta1 and Delta4. J. Immunol.180, 1655–1661 (2008). This article shows that DLLs may inhibit TH2-cell responses rather than actively promote TH1-cell responses. ArticleCASPubMed Google Scholar
Debarry, J. et al. Acinetobacter lwoffii and Lactococcus lactis strains isolated from farm cowsheds possess strong allergy-protective properties. J. Allergy Clin. Immunol.119, 1514–1521 (2007). ArticlePubMed Google Scholar
Maekawa, Y. et al. Delta1–Notch3 interactions bias the functional differentiation of activated CD4+ T cells. Immunity19, 549–559 (2003). This study is the first demonstration of a link between Notch and TH1-cell differentiation. ArticleCASPubMed Google Scholar
Elyaman, W. et al. JAGGED1 and Delta1 differentially regulate the outcome of experimental autoimmune encephalomyelitis. J. Immunol.179, 5990–5998 (2007). ArticleCASPubMed Google Scholar
Okamoto, M. et al. Essential role of Notch signaling in effector memory CD8+ T cell-mediated airway hyperresponsiveness and inflammation. J. Exp. Med.205, 1087–1097 (2008). ArticleCASPubMedPubMed Central Google Scholar
Minter, L. M. et al. Inhibitors of γ-secretase block in vivo and in vitro T helper type 1 polarization by preventing Notch upregulation of Tbx21. Nature Immunol.6, 680–688 (2005). ArticleCAS Google Scholar
Amsen, D. et al. Direct regulation of Gata3 expression determines the T helper differentiation potential of Notch. Immunity27, 89–99 (2007). ArticleCASPubMedPubMed Central Google Scholar
Ong, C. T., Sedy, J. R., Murphy, K. M. & Kopan, R. Notch and presenilin regulate cellular expansion and cytokine secretion but cannot instruct Th1/Th2 fate acquisition. PLoS ONE3, e2823 (2008). ArticleCASPubMedPubMed Central Google Scholar
Wolfe, M. S. & Kopan, R. Intramembrane proteolysis: theme and variations. Science305, 1119–1123 (2004). ArticleCASPubMed Google Scholar
Fang, T. C. et al. Notch directly regulates Gata3 expression during T helper 2 cell differentiation. Immunity27, 100–110 (2007). Together with reference 42, this report shows direct regulation ofGATA3transcription by Notch. ArticleCASPubMedPubMed Central Google Scholar
Osipo, C., Golde, T. E., Osborne, B. A. & Miele, L. A. Off the beaten pathway: the complex cross talk between Notch and NF-κB. Lab. Invest.88, 11–17 (2008). ArticleCASPubMed Google Scholar
Oswald, F., Liptay, S., Adler, G. & Schmid, R. M. NF-κB2 is a putative target gene of activated Notch-1 via RBP-Jκ. Mol. Cell. Biol.18, 2077–2088 (1998). ArticleCASPubMedPubMed Central Google Scholar
Cheng, P. et al. Notch-1 regulates NF-κB activity in hemopoietic progenitor cells. J. Immunol.167, 4458–4467 (2001). ArticleCASPubMed Google Scholar
Song, L. L. et al. Notch-1 associates with IKKα and regulates IKK activity in cervical cancer cells. Oncogene27, 5833–5844 (2008). ArticleCASPubMed Google Scholar
Vilimas, T. et al. Targeting the NF-κB signaling pathway in Notch1-induced T-cell leukemia. Nature Med.13, 70–77 (2007). ArticleCASPubMed Google Scholar
Vacca, A. et al. Notch3 and pre-TCR interaction unveils distinct NF-κB pathways in T-cell development and leukemia. EMBO J.25, 1000–1008 (2006). ArticleCASPubMedPubMed Central Google Scholar
Shin, H. M. et al. Notch1 augments NF-κB activity by facilitating its nuclear retention. EMBO J.25, 129–138 (2006). ArticleCASPubMed Google Scholar
Boothby, M. Specificity of sn50 for NF-κB? Nature Immunol.2, 471–472 (2001). ArticleCAS Google Scholar
Das, J. et al. A critical role for NF-κB in GATA3 expression and TH2 differentiation in allergic airway inflammation. Nature Immunol.2, 45–50 (2001). ArticleCAS Google Scholar
Tanigaki, K. et al. Regulation of αβ/γδ T cell lineage commitment and peripheral T cell responses by Notch/RBP-J signaling. Immunity20, 611–622 (2004). Together with references 25, 42 and 45, this article provides strong genetic evidence that the Notch signalling pathway is required for TH2-cell responses. ArticleCASPubMed Google Scholar
Barolo, S. et al. A Notch-independent activity of suppressor of hairless is required for normal mechanoreceptor physiology. Cell103, 957–969 (2000). ArticleCASPubMed Google Scholar
McElhinny, A. S., Li, J. L. & Wu, L. Mastermind-like transcriptional co-activators: emerging roles in regulating cross talk among multiple signaling pathways. Oncogene27, 5138–5147 (2008). ArticleCASPubMed Google Scholar
Krawczyk, C. M., Sun, J. & Pearce, E. J. Th2 differentiation is unaffected by Jagged2 expression on dendritic cells. J. Immunol.180, 7931–7937 (2008). ArticleCASPubMed Google Scholar
Krishnamoorthy, N. et al. Activation of c-Kit in dendritic cells regulates T helper cell differentiation and allergic asthma. Nature Med.14, 565–573 (2008). ArticleCASPubMed Google Scholar
Liotta, F. et al. Human immature myeloid dendritic cells trigger a TH2-polarizing program via Jagged-1/Notch interaction. J. Allergy Clin. Immunol.121, 1000–1005 (2008). ArticleCASPubMed Google Scholar
Kaisho, T. et al. Endotoxin can induce MyD88-deficient dendritic cells to support Th2 cell differentiation. Int. Immunol.14, 695–700 (2002). ArticleCASPubMed Google Scholar
Schnare, M. et al. Toll-like receptors control activation of adaptive immune responses. Nature Immunol.2, 947–950 (2001). ArticleCAS Google Scholar
Worsley, A. G. et al. Dendritic cell expression of the Notch ligand Jagged2 is not essential for Th2 response induction in vivo. Eur. J. Immunol.38, 1043–1049 (2008). ArticleCASPubMed Google Scholar
Cui, X. Y. et al. NB-3/Notch1 pathway via Deltex1 promotes neural progenitor cell differentiation into oligodendrocytes. J. Biol. Chem.279, 25858–25865 (2004). ArticleCASPubMed Google Scholar
Hu, Q. D. et al. F3/contactin acts as a functional ligand for Notch during oligodendrocyte maturation. Cell115, 163–175 (2003). ArticleCASPubMed Google Scholar
Tanaka, S. et al. The interleukin-4 enhancer CNS-2 is regulated by Notch signals and controls initial expression in NKT cells and memory-type CD4 T cells. Immunity24, 689–701 (2006). ArticleCASPubMed Google Scholar
Ouyang, W. et al. Stat6-independent GATA-3 autoactivation directs IL-4-independent Th2 development and commitment. Immunity12, 27–37 (2000). ArticleCASPubMed Google Scholar
Asnagli, H., Afkarian, M. & Murphy, K. M. Cutting Edge: identification of an alternative GATA-3 promoter directing tissue-specific gene expression in mouse and human. J. Immunol.168, 4268–4271 (2002). ArticleCASPubMed Google Scholar
Solymar, D. C., Agarwal, S., Bassing, C. H., Alt, F. W. & Rao, A. A 3′ enhancer in the IL-4 gene regulates cytokine production by Th2 cells and mast cells. Immunity17, 41–50 (2002). ArticleCASPubMed Google Scholar
Anastasi, E. et al. Expression of activated Notch3 in transgenic mice enhances generation of T regulatory cells and protects against experimental autoimmune diabetes. J. Immunol.171, 4504–4511 (2003). ArticleCASPubMed Google Scholar
Jurynczyk, M., Jurewicz, A., Raine, C. S. & Selmaj, K. Notch3 inhibition in myelin-reactive T cells down-regulates protein kinase C θ and attenuates experimental autoimmune encephalomyelitis. J. Immunol.180, 2634–2640 (2008). ArticleCASPubMed Google Scholar
Veldhoen, M. et al. Transforming growth factor-β 'reprograms' the differentiation of T helper 2 cells and promotes an interleukin 9-producing subset. Nature Immunol.9, 1341–1346 (2008). ArticleCAS Google Scholar
Dardalhon, V. et al. IL-4 inhibits TGF-β-induced Foxp3+ T cells and, together with TGF-β, generates IL-9+ IL-10+ Foxp3− effector T cells. Nature Immunol.9, 1347–1355 (2008). ArticleCAS Google Scholar
King, C., Tangye, S. G. & Mackay, C. R. T follicular helper (TFH) cells in normal and dysregulated immune responses. Annu. Rev. Immunol.26, 741–766 (2008). ArticleCASPubMed Google Scholar
Vigouroux, S. et al. Induction of antigen-specific regulatory T cells following overexpression of a Notch ligand by human B lymphocytes. J. Virol.77, 10872–10880 (2003). ArticleCASPubMedPubMed Central Google Scholar
Yvon, E. S. et al. Overexpression of the Notch ligand, Jagged-1, induces alloantigen-specific human regulatory T cells. Blood102, 3815–3821 (2003). ArticleCASPubMed Google Scholar
Hoyne, G. F. et al. Serrate1-induced Notch signalling regulates the decision between immunity and tolerance made by peripheral CD4+ T cells. Int. Immunol.12, 177–185 (2000). ArticleCASPubMed Google Scholar
Kared, H. et al. Jagged2-expressing hematopoietic progenitors promote regulatory T cell expansion in the periphery through Notch signaling. Immunity25, 823–834 (2006). ArticleCASPubMed Google Scholar
Jankovic, D. et al. Conventional T-bet+Foxp3− Th1 cells are the major source of host-protective regulatory IL-10 during intracellular protozoan infection. J. Exp. Med.204, 273–283 (2007). ArticleCASPubMedPubMed Central Google Scholar
Anderson, C. F., Oukka, M., Kuchroo, V. J. & Sacks, D. CD4+CD25−Foxp3− Th1 cells are the source of IL-10-mediated immune suppression in chronic cutaneous leishmaniasis. J. Exp. Med.204, 285–297 (2007). ArticleCASPubMedPubMed Central Google Scholar
Eagar, T. N. et al. Notch 1 signaling regulates peripheral T cell activation. Immunity20, 407–415 (2004). ArticleCASPubMed Google Scholar
Ostroukhova, M. et al. Treg-mediated immunosuppression involves activation of the Notch–HES1 axis by membrane-bound TGF-β. J. Clin. Invest.116, 996–1004 (2006). ArticleCASPubMedPubMed Central Google Scholar
Palaga, T., Miele, L., Golde, T. E. & Osborne, B. A. TCR-mediated Notch signaling regulates proliferation and IFN-γ production in peripheral T cells. J. Immunol.171, 3019–3024 (2003). ArticleCASPubMed Google Scholar
Kluppel, M. & Wrana, J. L. Turning it up a Notch: cross-talk between TGFβ and Notch signaling. Bioessays27, 115–118 (2005). ArticleCASPubMed Google Scholar
Samon, J. B. et al. Notch1 and TGFβ1 cooperatively regulate Foxp3 expression and the maintenance of peripheral regulatory T cells. Blood112, 1813–1821 (2008). ArticleCASPubMedPubMed Central Google Scholar
Tournoy, J. et al. Partial loss of presenilins causes seborrheic keratosis and autoimmune disease in mice. Hum. Mol. Genet.13, 1321–1331 (2004). ArticleCASPubMed Google Scholar
Schaller, M. A. et al. Notch ligand Delta-like 4 regulates disease pathogenesis during respiratory viral infections by modulating Th2 cytokines. J. Exp. Med.204, 2925–2934 (2007). ArticleCASPubMedPubMed Central Google Scholar