Notch3 is dispensable for thymocyte β-selection and notch1-induced T cell leukemogenesis

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Suliman, Sara ^a,b   Tan, Joanne ^a,b   Xu, Keli ^a   Kousis, Philaretos C ^a   Kowalski, Paul E ^a   Chang, Greg ^a   Egan, Sean E ^a,b   Guidos, Cynthia ^a,b  

^a HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; DELTA LIKE 4 PROTEIN; NOTCH1 RECEPTOR; NOTCH3 RECEPTOR; UNCLASSIFIED DRUG; NOTCH RECEPTOR; NOTCH3 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; BINDING AFFINITY; CELL MATURATION; CELL SELECTION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DELETION MUTANT; LEUKEMOGENESIS; LIGAND BINDING; LYMPHOID PROGENITOR CELL; MOUSE; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STEADY STATE; T CELL LEUKEMIA; T LYMPHOCYTE DEVELOPMENT; THYMOCYTE; ANIMAL; CELL DIFFERENTIATION; CYTOLOGY; FLOW CYTOMETRY; GENETICS; METABOLISM; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY; T LYMPHOCYTE;

MUS;

ANIMALS; CELL DIFFERENTIATION; FLOW CYTOMETRY; LEUKEMIA, T-CELL; MICE; MICE, MUTANT STRAINS; RECEPTOR, NOTCH1; RECEPTORS, NOTCH; T-LYMPHOCYTES; THYMOCYTES;

EID: 80052711216     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0024937     Document Type: Article

References (61)

1. Yuan JS, Kousis PC, Suliman S, Visan I, Guidos CJ, (2010) Functions of notch signaling in the immune system: consensus and controversies. Annu Rev Immunol 28: 343-365.
2. Kopan R, Ilagan MX, (2009) The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 137: 216-233.
3. Radtke F, Wilson A, Stark G, Bauer M, van Meerwijk J, et al. (1999) Deficient T cell fate specification in mice with an induced inactivation of Notch1. Immunity 10: 547-558.
4. Koch U, Lacombe TA, Holland D, Bowman JL, Cohen BL, et al. (2001) Subversion of the T/B lineage decision in the thymus by lunatic fringe-mediated inhibition of Notch-1. Immunity 15: 225-236.
5. Visan I, Tan JB, Yuan JS, Harper JA, Koch U, et al. (2006) Regulation of T lymphopoiesis by Notch1 and Lunatic fringe-mediated competition for intrathymic niches. Nat Immunol 7: 634-643.
6. Koch U, Fiorini E, Benedito R, Besseyrias V, Schuster-Gossler K, et al. (2008) Delta-like 4 is the essential, nonredundant ligand for Notch1 during thymic T cell lineage commitment. J Exp Med 205: 2515-2523.
7. Hozumi K, Mailhos C, Negishi N, Hirano K, Yahata T, et al. (2008) Delta-like 4 is indispensable in thymic environment specific for T cell development. J Exp Med 205: 2507-2513.
8. Sambandam A, Maillard I, Zediak VP, Xu L, Gerstein RM, et al. (2005) Notch signaling controls the generation and differentiation of early T lineage progenitors. Nat Immunol 6: 663-670.
9. Schmitt TM, Zuniga-Pflucker JC, (2002) Induction of T cell development from hematopoietic progenitor cells by delta-like-1 in vitro. Immunity 17: 749-756.
10. Taghon TN, David ES, Zuniga-Pflucker JC, Rothenberg EV, (2005) Delayed, asynchronous, and reversible T-lineage specification induced by Notch/Delta signaling. Genes Dev 19: 965-978.
11. Tan JB, Visan I, Yuan JS, Guidos CJ, (2005) Requirement for Notch1 signals at sequential early stages of intrathymic T cell development. Nat Immunol 6: 671-679.
12. Ciofani M, Zuniga-Pflucker JC, (2005) Notch promotes survival of pre-T cells at the beta-selection checkpoint by regulating cellular metabolism. Nat Immunol 6: 881-888.
13. Hoffman ES, Passoni L, Crompton T, Leu TM, Schatz DG, et al. (1996) Productive T-cell receptor beta-chain gene rearrangement: coincident regulation of cell cycle and clonality during development in vivo. Genes Dev 10: 948-962.
14. Kelly AP, Finlay DK, Hinton HJ, Clarke RG, Fiorini E, et al. (2007) Notch-induced T cell development requires phosphoinositide-dependent kinase 1. Embo J 26: 3441-3450.
15. Taghon T, Yui MA, Pant R, Diamond RA, Rothenberg EV, (2006) Developmental and molecular characterization of emerging beta- and gammadelta-selected pre-T cells in the adult mouse thymus. Immunity 24: 53-64.
16. Yuan JS, Tan JB, Visan I, Matei IR, Urbanellis P, et al. (2011) Lunatic Fringe prolongs Delta/Notch-induced self-renewal of committed alphabeta T-cell progenitors. Blood 117: 1184-1195.
17. Ciofani M, Schmitt TM, Ciofani A, Michie AM, Cuburu N, et al. (2004) Obligatory role for cooperative signaling by pre-TCR and Notch during thymocyte differentiation. J Immunol 172: 5230-5239.
18. Huang EY, Gallegos AM, Richards SM, Lehar SM, Bevan MJ, (2003) Surface expression of Notch1 on thymocytes: correlation with the double-negative to double-positive transition. J Immunol 171: 2296-2304.
19. Guidos CJ, Weissman IL, Adkins B, (1989) Intrathymic maturation of murine T lymphocytes from CD8+ precursors. Proc Natl Acad Sci U S A 86: 7542-7546.
20. Wolfer A, Wilson A, Nemir M, MacDonald HR, Radtke F, (2002) Inactivation of Notch1 impairs VDJbeta rearrangement and allows pre-TCR-independent survival of early alpha beta Lineage Thymocytes. Immunity 16: 869-879.
21. Reizis B, Leder P, (2002) Direct induction of T lymphocyte-specific gene expression by the mammalian Notch signaling pathway. Genes Dev 16: 295-300.
22. Maillard I, Tu L, Sambandam A, Yashiro-Ohtani Y, Millholland J, et al. (2006) The requirement for Notch signaling at the beta-selection checkpoint in vivo is absolute and independent of the pre-T cell receptor. J Exp Med 203: 2239-2245.
23. Garbe AI, Krueger A, Gounari F, Zuniga-Pflucker JC, von Boehmer H, (2006) Differential synergy of Notch and T cell receptor signaling determines alphabeta versus gammadelta lineage fate. J Exp Med 203: 1579-1590.
24. Deftos ML, Huang E, Ojala EW, Forbush KA, Bevan MJ, (2000) Notch1 signaling promotes the maturation of CD4 and CD8 SP thymocytes. Immunity 13: 73-84.
25. Fowlkes BJ, Robey EA, (2002) A reassessment of the effect of activated Notch1 on CD4 and CD8 T cell development. J Immunol 169: 1817-1821.
26. Aster JC, Blacklow SC, Pear WS, (2011) Notch signalling in T-cell lymphoblastic leukaemia/lymphoma and other haematological malignancies. The Journal of pathology 223: 262-273.
27. Hamada Y, Kadokawa Y, Okabe M, Ikawa M, Coleman JR, et al. (1999) Mutation in ankyrin repeats of the mouse Notch2 gene induces early embryonic lethality. Development 126: 3415-3424.
28. Witt CM, Hurez V, Swindle CS, Hamada Y, Klug CA, (2003) Activated Notch2 potentiates CD8 lineage maturation and promotes the selective development of B1 B cells. Molecular and cellular biology 23: 8637-8650.
29. Besseyrias V, Fiorini E, Strobl LJ, Zimber-Strobl U, Dumortier A, et al. (2007) Hierarchy of Notch-Delta interactions promoting T cell lineage commitment and maturation. J Exp Med 204: 331-343.
30. Bellavia D, Campese AF, Alesse E, Vacca A, Felli MP, et al. (2000) Constitutive activation of NF-kappaB and T-cell leukemia/lymphoma in Notch3 transgenic mice. EMBO J 19: 3337-3348.
31. Bellavia D, Campese AF, Checquolo S, Balestri A, Biondi A, et al. (2002) Combined expression of pTalpha and Notch3 in T cell leukemia identifies the requirement of preTCR for leukemogenesis. Proc Natl Acad Sci U S A 99: 3788-3793.
32. Bellavia D, Mecarozzi M, Campese AF, Grazioli P, Talora C, et al. (2007) Notch3 and the Notch3-upregulated RNA-binding protein HuD regulate Ikaros alternative splicing. EMBO J 26: 1670-1680.
33. Qiu X, Lim CH, Ho SH, Lee KH, Jiang YJ, (2009) Temporal Notch activation through Notch1a and Notch3 is required for maintaining zebrafish rhombomere boundaries. Dev Genes Evol 219: 339-351.
34. Ohashi S, Natsuizaka M, Yashiro-Ohtani Y, Kalman RA, Nakagawa M, et al. (2010) NOTCH1 and NOTCH3 coordinate esophageal squamous differentiation through a CSL-dependent transcriptional network. Gastroenterology 139: 2113-2123.
35. Palomero T, Lim WK, Odom DT, Sulis ML, Real PJ, et al. (2006) NOTCH1 directly regulates c-MYC and activates a feed-forward-loop transcriptional network promoting leukemic cell growth. Proc Natl Acad Sci U S A 103: 18261-18266.
36. Weng AP, Millholland JM, Yashiro-Ohtani Y, Arcangeli ML, Lau A, et al. (2006) c-Myc is an important direct target of Notch1 in T-cell acute lymphoblastic leukemia/lymphoma. Genes Dev 20: 2096-2109.
37. Xu K, Nieuwenhuis E, Cohen BL, Wang W, Canty AJ, et al. (2010) Lunatic Fringe-mediated Notch signaling is required for lung alveogenesis. Am J Physiol Lung Cell Mol Physiol 298: L45-56.
38. Murtaugh LC, Stanger BZ, Kwan KM, Melton DA, (2003) Notch signaling controls multiple steps of pancreatic differentiation. Proc Natl Acad Sci U S A 100: 14920-14925.
39. Mitchell KJ, Pinson KI, Kelly OG, Brennan J, Zupicich J, et al. (2001) Functional analysis of secreted and transmembrane proteins critical to mouse development. Nature Genetics 28: 241-249.
40. Arboleda-Velasquez JF, Zhou Z, Shin HK, Louvi A, Kim HH, et al. (2008) Linking Notch signaling to ischemic stroke. Proc Natl Acad Sci U S A 105: 4856-4861.
41. Yui MA, Feng N, Rothenberg EV, (2010) Fine-scale staging of T cell lineage commitment in adult mouse thymus. J Immunol 185: 284-293.
42. Raafat A, Goldhar AS, Klauzinska M, Xu K, Amirjazil I, et al. (2011) Expression of Notch receptors, ligands, and target genes during development of the mouse mammary gland. Journal of cellular physiology 226: 1940-1952.
43. Kitamoto T, Takahashi K, Takimoto H, Tomizuka K, Hayasaka M, et al. (2005) Functional redundancy of the Notch gene family during mouse embryogenesis: analysis of Notch gene expression in Notch3-deficient mice. Biochem Biophys Res Commun 331: 1154-1162.
44. Visan I, Yuan JS, Liu Y, Stanley P, Guidos CJ, (2010) Lunatic fringe enhances competition for delta-like Notch ligands but does not overcome defective pre-TCR signaling during thymocyte beta-selection in vivo. Journal of immunology 185: 4609-4617.
45. Guidos CJ, Weissman IL, Adkins B, (1989) Developmental potential of CD4-8- thymocytes. Peripheral progeny include mature CD4-8- T cells bearing alpha beta T cell receptor. J Immunol 142: 3773-3780.
46. Krebs LT, Xue Y, Norton CR, Shutter JR, Maguire M, et al. (2000) Notch signaling is essential for vascular morphogenesis in mice. Genes Dev 14: 1343-1352.
47. Yuan JS, Tan JB, Visan I, Matei IR, Urbanellis P, et al. (2010) Lunatic Fringe prolongs Delta/Notch-induced self-renewal of committed alphabeta T-cell progenitors. Blood 117: 1184-1195.
48. Jeannet R, Mastio J, Macias-Garcia A, Oravecz A, Ashworth T, et al. (2010) Oncogenic activation of the Notch1 gene in Ikaros-deficient T-ALL by deletion of its promoter. Blood prepublished online: September 9, 2010.
49. Krebs LT, Xue Y, Norton CR, Sundberg JP, Beatus P, et al. (2003) Characterization of Notch3-deficient mice: normal embryonic development and absence of genetic interactions with a Notch1 mutation. Genesis 37: 139-143.
50. Domenga V, Fardoux P, Lacombe P, Monet M, Maciazek J, et al. (2004) Notch3 is required for arterial identity and maturation of vascular smooth muscle cells. Genes & development 18: 2730-2735.
51. Joutel A, Corpechot C, Ducros A, Vahedi K, Chabriat H, et al. (1996) Notch3 mutations in CADASIL, a hereditary adult-onset condition causing stroke and dementia. Nature 383: 707-710.
52. Boulos N, Helle F, Dussaule JC, Placier S, Milliez P, et al. (2011) Notch3 is essential for regulation of the renal vascular tone. Hypertension 57: 1176-1182.
53. Li X, Zhang X, Leathers R, Makino A, Huang C, et al. (2009) Notch3 signaling promotes the development of pulmonary arterial hypertension. Nature medicine 15: 1289-1297.
54. Lin L, Mernaugh R, Yi F, Blum D, Carbone DP, et al. (2010) Targeting specific regions of the Notch3 ligand-binding domain induces apoptosis and inhibits tumor growth in lung cancer. Cancer research 70: 632-638.
55. Park JT, Li M, Nakayama K, Mao TL, Davidson B, et al. (2006) Notch3 gene amplification in ovarian cancer. Cancer research 66: 6312-6318.
56. Li K, Li Y, Wu W, Gordon WR, Chang DW, et al. (2008) Modulation of Notch signaling by antibodies specific for the extracellular negative regulatory region of NOTCH3. The Journal of biological chemistry 283: 8046-8054.
57. Shimizu K, Chiba S, Saito T, Kumano K, Hamada Y, et al. (2002) Functional diversity among Notch1, Notch2, and Notch3 receptors. Biochem Biophys Res Commun 291: 775-779.
58. Chadwick N, Zeef L, Portillo V, Fennessy C, Warrander F, et al. (2009) Identification of novel Notch target genes in T cell leukaemia. Mol Cancer 8: 35.
59. Ong CT, Cheng HT, Chang LW, Ohtsuka T, Kageyama R, et al. (2006) Target selectivity of vertebrate notch proteins. Collaboration between discrete domains and CSL-binding site architecture determines activation probability. J Biol Chem 281: 5106-5119.
60. Nam Y, Sliz P, Pear WS, Aster JC, Blacklow SC, (2007) Cooperative assembly of higher-order Notch complexes functions as a switch to induce transcription. Proc Natl Acad Sci U S A 104: 2103-2108.
61. Liu H, Chi AW, Arnett KL, Chiang MY, Xu L, et al. (2010) Notch dimerization is required for leukemogenesis and T-cell development. Genes Dev 24: 2395-2407.