Multiple niches for Notch in cancer: Context is everything

Current Opinion in Genetics and Development

Volumn 14, Issue 1, 2004, Pages 48-54

  Weng, Andrew P ^a   Aster, Jon C ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; NOTCH RECEPTOR; ONCOPROTEIN; TUMOR SUPPRESSOR PROTEIN; VIRUS PROTEIN;

ANGIOGENESIS; CANCER INHIBITION; CARCINOGENESIS; CARCINOGENICITY; CHROMOSOME TRANSLOCATION; COMPLEX FORMATION; GENE FUNCTION; HOMEOSTASIS; HUMAN; IMMUNE RESPONSE; KERATINOCYTE; METAPLASIA; METASTASIS; NONHUMAN; ONCOGENE; ONCOVIRINAE; PANCREAS CARCINOMA; PRECANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION; STEM CELL; T LYMPHOCYTE; TISSUE REGENERATION; TRANSCRIPTION INITIATION;

ONCOVIRINAE;

EID: 0842324623     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.gde.2003.11.004     Document Type: Review

References (69)

1. Bray S. Notch signalling in Drosophila: three ways to use a pathway. Semin Cell Dev Biol. 9:1998;591-597.
2. Bessho Y., Kageyama R. Oscillations, clocks, and segmentation. Curr Opin Genet Dev. 13:2003;379-384.
3. Raya A., Koth C.M., Buscher D., Kawakami Y., Itoh T., Raya R.M., Sternik G., Tsai H.J., Rodriguez-Esteban C., Izpisua-Belmonte J.C. Activation of Notch signaling pathway precedes heart regeneration in zebrafish. Proc Natl Acad Sci USA. 100(Suppl 1):2003;11889-11895.
4. Miyamoto Y., Maitra A., Ghosh B., Zechner U., Argani P., Iacobuzio-Donahue C.A., Sriuranpong V., Iso T., Meszoely I.M., Wolfe M.S.et al. Notch mediates TGFα-induced changes in epithelial differentiation during pancreatic tumorigenesis. Cancer Cell. 3:2003;565-576 Miyamoto et al. detected evidence of altered expression of Notch signaling pathway components through expression profiling, and then showed through analysis of primary tumors and pancreatic explants that Notch lies downstream of TGF-β in a signaling network that leads to ductal metaplasia of pancreatic epithelium and expansion of nestin+ precursor cells. This paper is the best evidence to date that altered Notch signaling has a causal role in metaplasia, a common pre-neoplastic change affecting epithelial cells in many different tissues. Other examples of metaplasias that correlate with cancer risk include squamous metaplasia and lung cancer, intestinal metaplasia and gastric cancer, Barrett's esophagus and esophageal cancer, and endocervical metaplasia and cervical cancer.
5. Artavanis-Tsakonas S., Rand M.D., Lake R.J. Notch signaling: cell fate control and signal integration in development. Science. 284:1999;770-776.
6. Logeat F., Bessia C., Brou C., LeBail O., Jarriault S., Seidah N.G., Israel A. The Notch1 receptor is cleaved constitutively by a furin-like convertase. Proc Natl Acad Sci USA. 95:1998;8108-8112.
7. Rand M.D., Grimm L.M., Artavanis-Tsakonas S., Patriub V., Blacklow S.C., Sklar J., Aster J.C. Calcium depletion dissociates and activates heterodimeric notch receptors. Mol Cell Biol. 20:2000;1825-1835.
8. Brou C., Logeat F., Gupta N., Bessia C., LeBail O., Doedens J.R., Cumano A., Roux P., Black R.A., Israel A. A novel proteolytic cleavage involved in Notch signaling: the role of the disintegrin-metalloprotease TACE. Mol Cell. 5:2000;207-216.
9. Mumm J.S., Schroeter E.H., Saxena M.T., Griesemer A., Tian X., Pan D.J., Ray W.J., Kopan R. A ligand-induced extracellular cleavage regulates γ-secretase-like proteolytic activation of Notch1. Mol Cell. 5:2000;197-206.
10. De Strooper B., Annaert W., Cupers P., Saftig P., Craessaerts K., Mumm J.S., Schroeter E.H., Schrijvers V., Wolfe M.S., Ray W.J.et al. A presenilin-1-dependent gamma-secretase-like protease mediates release of Notch intracellular domain. Nature. 398:1999;518-522.
11. Struhl G., Greenwald I. Presenilin is required for activity and nuclear access of Notch in Drosophila. Nature. 398:1999;522-525.
12. Ye Y., Lukinova N., Fortini M.E. Neurogenic phenotypes and altered Notch processing in Drosophila Presenilin mutants. Nature. 398:1999;525-529.
13. Huppert S.S., Le A., Schroeter E.H., Mumm J.S., Saxena M.T., Milner L.A., Kopan R. Embryonic lethality in mice homozygous for a processing-deficient allele of Notch1. Nature. 405:2000;966-970.
14. Okochi M., Steiner H., Fukumori A., Tanii H., Tomita T., Tanaka T., Iwatsubo T., Kudo T., Takeda M., Haass C. Presenilins mediate a dual intramembranous γ-secretase cleavage of Notch-1. EMBO J. 21:2002;5408-5416.
15. Schroeter E.H., Kisslinger J.A., Kopan R. Notch-1 signalling requires ligand-induced proteolytic release of intracellular domain. Nature. 393:1998;382-386.
16. Fortini M.E., Artavanis-Tsakonas S. The Suppressor of hairless protein participates in notch receptor signaling. Cell. 79:1994;273-282.
17. Jarriault S., Brou C., Logeat F., Schroeter E.H., Kopan R., Israel A. Signalling downstream of activated mammalian Notch. Nature. 377:1995;355-358.
18. Christensen S., Kodoyianni V., Bosenberg M., Friedman L., Kimble J. lag-1, a gene required for lin-12 and glp-1 signaling in Caenorhabditis elegans, is homologous to human CBF1 and Drosophila Su(H). Development. 122:1996;1373-1383.
19. Petcherski A.G., Kimble J. LAG-3 is a putative transcriptional activator in the C. elegans Notch pathway. Nature. 405:2000;364-368.
20. Wu L., Aster J.C., Blacklow S.C., Lake R., Artavanis-Tsakonas S., Griffin J.D. MAML1, a human homologue of Drosophila mastermind, is a transcriptional co-activator for NOTCH receptors. Nat Genet. 26:2000;484-489.
21. Lai E.C. Protein degradation: four E3s for the notch pathway. Curr Biol. 12:2002;R74-R78.
22. Nam Y., Weng A.P., Aster J.C., Blacklow S.C. Structural requirements for assembly of the CSL intracellular Notch1. Mastermind-like 1 transcriptional activation complex. J Biol Chem. 278:2003;21232-21239.
23. Wallberg A.E., Pedersen K., Lendahl U., Roeder R.G. p300 and PCAF act cooperatively to mediate transcriptional activation from chromatin templates by notch intracellular domains in vitro. Mol Cell Biol. 22:2002;7812-7819.
24. Fryer C.J., Lamar E., Turbachova I., Kintner C., Jones K.A. Mastermind mediates chromatin-specific transcription and turnover of the Notch enhancer complex. Genes Dev. 16:2002;1397-1411.
25. Wu L., Sun T., Kobayashi K., Gao P., Griffin J.D. Identification of a family of mastermind-like transcriptional coactivators for mammalian notch receptors. Mol Cell Biol. 22:2002;7688-7700.
26. Bush G., diSibio G., Miyamoto A., Denault J.B., Leduc R., Weinmaster G. Ligand-induced signaling in the absence of furin processing of Notch1. Dev Biol. 229:2001;494-502.
27. Martinez Arias A., Zecchini V., Brennan K. CSL-independent Notch signalling: a checkpoint in cell fate decisions during development? Curr Opin Genet Dev. 12:2002;524-533.
28. Aster J.C., Pear W.S. Notch signaling in leukemia. Curr Opin Hematol. 8:2001;237-244.
29. IC- transformed RKE cells and in a human T-cell leukemia cell line. Mol Cell Biol. 22:2002;3927-3941.
30. 1 growth arrest and apoptosis of cell lines derived from murine and human N1-associated T-ALLs. This paper suggests the ICN/CSL/MAML complex activates the expression of one or more target genes responsible for the proliferation of pre-T cells, making the Notch transcriptional activation complex a rational therapeutic target.
31. Aster J.C., Xu L., Karnell F.G., Patriub V., Pui J.C., Pear W.S. Essential roles for ankyrin repeat and transactivation domains in induction of T-cell leukemia by notch1. Mol Cell Biol. 20:2000;7505-7515.
32. Pui J.C., Allman D., Xu L., DeRocco S., Karnell F.G., Bakkour S., Lee J.Y., Kadesch T., Hardy R.R., Aster J.C.et al. Notch1 expression in early lymphopoiesis influences B versus T lineage determination. Immunity. 11:1999;299-308.
33. Radtke F., Wilson A., Stark G., Bauer M., van Meerwijk J., MacDonald H.R., Aguet M. Deficient T cell fate specification in mice with an induced inactivation of Notch1. Immunity. 10:1999;547-558.
34. Allman D., Karnell F.G., Punt J.A., Bakkour S., Xu L., Myung P., Koretzky G.A., Pui J.C., Aster J.C., Pear W.S. Separation of Notch1 promoted lineage commitment and expansion/transformation in developing T cells. J Exp Med. 194:2001;99-106.
35. Bellavia D., Campese A.F., Checquolo S., Balestri A., Biondi A., Cazzaniga G., Lendahl U., Fehling H.J., Hayday A.C., Frati L.et al. Combined expression of pTα and Notch3 in T cell leukemia identifies the requirement of preTCR for leukemogenesis. Proc Natl Acad Sci USA. 99:2002;3788-3793.
36. Huang E.Y., Gallegos A.M., Richards S.M., Lehar S.M., Bevan M.J. Surface expression of Notch1 on thymocytes: correlation with the double-negative to double-positive transition. J Immunol. 171:2003;2296-2304.
37. Rohn J.L., Lauring A.S., Linenberger M.L., Overbaugh J. Transduction of Notch2 in feline leukemia virus-induced thymic lymphoma. J Virol. 70:1996;8071-8080.
38. Kawamata S., Du C., Li K., Lavau C. Overexpression of the Notch target genes Hes in vivo induces lymphoid and myeloid alterations. Oncogene. 21:2002;3855-3863.
39. IC-induced T cell leukemogenesis. Cancer Cell. 3:2003;551-564 An important issue in understanding the context-dependent effects of Notch is how upstream factors regulate access of the ICN/CSL/MAML complex to potential target genes. In this paper, Beverly and Capobianco show one type of proviral insertion affecting N-mediated leukemognesis alters expression of Ikaros, a transcriptional regulator of early stages of hematolymphoid development that binds DNA at sequences resembling those recognized by CSL. Although Ikaros is an attractive candidate to modify the consequences of Notch signaling in normal progenitors by altering CSL access to particular promoters, additional work will be needed to prove the proposed promoter competition model is physiologically relevant.
40. Callahan R., Raafat A. Notch signaling in mammary gland tumorigenesis. J Mammary Gland Biol Neoplasia. 6:2001;23-36.
41. Fitzgerald K., Harrington A., Leder P. Ras pathway signals are required for notch-mediated oncogenesis. Oncogene. 19:2000;4191-4198.
42. Rangarajan A., Talora C., Okuyama R., Nicolas M., Mammucari C., Oh H., Aster J.C., Krishna S., Metzger D., Chambon P.et al. Notch signaling is a direct determinant of keratinocyte growth arrest and entry into differentiation. EMBO J. 20:2001;3427-3436.
43. Nicolas M., Wolfer A., Raj K., Kummer J.A., Mill P., van Noort M., Hui C.C., Clevers H., Dotto G.P., Radtke F. Notch1 functions as a tumor suppressor in mouse skin. Nat Genet. 33:2003;416-421 This paper shows unequivocally that loss of N1 function in keratinocytes is oncogenic, meaning N1 functions as a tumor suppressor and an oncogene in different cellular contexts. N1 loss of function resulted in basal-cell-like carcinomas or squamous cell carcinomas (in the presence of an activated ras allele), and also enhanced the development of carcinogen-induced skin cancers. These results drive home the fact that the pathophysiologic effects of altered Notch signals, just like their normal functions, differ dramatically depending on cellular context.
44. Shou J., Ross S., Koeppen H., de Sauvage F.J., Gao W.Q. Dynamics of notch expression during murine prostate development and tumorigenesis. Cancer Res. 61:2001;7291-7297.
45. Hofelmayr H., Strobl L.J., Marschall G., Bornkamm G.W., Zimber-Strobl U. Activated Notch1 can transiently substitute for EBNA2 in the maintenance of proliferation of LMP1-expressing immortalized B cells. J Virol. 75:2001;2033-2040.
46. Lee J.M., Lee K.H., Weidner M., Osborne B.A., Hayward S.D. Epstein-Barr virus EBNA2 blocks Nur77-mediated apoptosis. Proc Natl Acad Sci USA. 99:2002;11878-11883.
47. Johansen L.M., Deppmann C.D., Erickson K.D., Coffin W.F. III, Thornton T.M., Humphrey S.E., Martin J.M., Taparowsky E.J. EBNA2 and activated Notch induce expression of BATF. J Virol. 77:2003;6029-6040.
48. Harada S., Kieff E. Epstein-Barr virus nuclear protein LP stimulates EBNA-2 acidic domain-mediated transcriptional activation. J Virol. 71:1997;6611-6618.
49. Kusano S., Raab-Traub N. An Epstein-Barr virus protein interacts with Notch. J Virol. 75:2001;384-395.
50. IC. J Virol. 75:2001;2946-2956.
51. Morimura T., Goitsuka R., Zhang Y., Saito I., Reth M., Kitamura D. Cell cycle arrest and apoptosis induced by Notch1 in B cells. J Biol Chem. 275:2000;36523-36531.
52. •,53]. Given the context-dependency of Notch effects, it seems quite plausible that results in cell lines may not reflect in vivo effects. It is also notable that MAML1, a component of the ICN/CSL/MAML1 complex, was originally identified as an E6-binding protein. It will be of interest to determine if the effects of E6 on MAML1 function are analogous to its antagonistic effects on p53 function.
53. Weijzen S., Zlobin A., Braid M., Miele L., Kast W.M. HPV16 E6 and E7 oncoproteins regulate Notch-1 expression and cooperate to induce transformation. J Cell Physiol. 194:2003;356-362.
54. Nair P., Somasundaram K., Krishna S. Activated Notch1 inhibits p53-induced apoptosis and sustains transformation by human papillomavirus type 16 E6 and E7 oncogenes through a PI3K-PKB/Akt-dependent pathway. J Virol. 77:2003;7106-7112.
55. Zagouras P., Stifani S., Blaumueller C.M., Carcangiu M.L., Artavanis-Tsakonas S. Alterations in Notch signaling in neoplastic lesions of the human cervix. Proc Natl Acad Sci USA. 92:1995;6414-6418.
56. Tonon G., Modi S., Wu L., Kubo A., Coxon A.B., Komiya T., O'Neil K., Stover K., El-Naggar A., Griffin J.D.et al. t(11;19)(q21;p13) translocation in mucoepidermoid carcinoma creates a novel fusion product that disrupts a Notch signaling pathway. Nat Genet. 33:2003;208-213 This paper demonstrates a high percentage of human mucoepidermoid carcinomas, tumors usually arising in the salivary glands or upper aerodigestive tract that exhibit both glandular and squamous differentiation, contain a (11;19) chromosomal translocation involving the MAML2 and MECT1 genes. The position of the t(11;19) breakpoints are such that the 5′ promoter and exon sequences of MAML2 are replaced by the analogous sequences of the MECT1. The resultant MECT1/MAML2 fusion gene encodes a protein in which the ICN1-binding region of MAML2 is replaced with a non-homologous sequence derived from MECT1. Although MECT1/MAML2 polypeptide lacks the ability to bind ICN1, it is not yet clear whether the fusion protein has dominant loss or gain of function activities.
57. Rossant J., Hirashima M. Vascular development and patterning: making the right choices. Curr Opin Genet Dev. 13:2003;408-412.
58. Sullivan D.C., Bicknell R. New molecular pathways in angiogenesis. Br J Cancer. 89:2003;228-231.
59. Cheng P, Nefedova Y, Miele L, Osborne BA, Gabrilovich D: Notch signaling is necessary but not sufficient for differentiation of dendritic cells. Blood 2003, in press.
60. Yvon ES, Vigouroux S, Rousseau RF, Biagi E, Amrolia P, Dotti G, Wagner HJ, Brenner MK: Overexpression of the Notch ligand, Jagged-1, induces alloantigen-specific human regulatory T cells. Blood 2003.
61. Ohishi K., Katayama N., Shiku H., Varnum-Finney B., Bernstein I.D. Notch signalling in hematopoiesis. Semin Cell Dev Biol. 14:2003;143-150.
62. Reizis B., Leder P. Direct induction of T lymphocyte-specific gene expression by the mammalian Notch signaling pathway. Genes Dev. 16:2002;295-300.
63. Nam Y., Aster J.C., Blacklow S.C. Notch signaling as a therapeutic target. Curr Opin Chem Biol. 6:2002;501-509.
64. IC-ER chimeras display hormone-dependent transformation, nuclear accumulation, phosphorylation and CBF1 activation. Oncogene. 19:2000;3914-3924.
65. Jundt F., Anagnostopoulos I., Forster R., Mathas S., Stein H., Dorken B. Activated Notch1 signaling promotes tumor cell proliferation and survival in Hodgkin and anaplastic large cell lymphoma. Blood. 99:2002;3398-3403.
66. Bocchetta M., Miele L., Pass H.I., Carbone M. Notch-1 induction, a novel activity of SV40 required for growth of SV40-transformed human mesothelial cells. Oncogene. 22:2003;81-89.
67. Yan X.Q., Sarmiento U., Sun Y., Huang G., Guo J., Juan T., Van G., Qi M.Y., Scully S., Senaldi G.et al. A novel Notch ligand, Dll4, induces T-cell leukemia/lymphoma when overexpressed in mice by retroviral-mediated gene transfer. Blood. 98:2001;3793-3799.
68. Brumby A.M., Richardson H.E. scribble mutants cooperate with oncogenic Ras or Notch to cause neoplastic overgrowth in Drosophila. EMBO J. 22:2003;5769-5779.
69. Tsuji H., Ishii-Ohba H., Ukai H., Katsube T., Ogiu T. Radiation-induced deletions in the 5′ end region of Notch1 lead to the formation of truncated proteins and are involved in the development of mouse thymic lymphomas. Carcinogenesis. 24:2003;1257-1268.