Notch1 is an effector of Akt and hypoxia in melanoma development

Journal of Clinical Investigation

Volumn 118, Issue 11, 2008, Pages 3660-3670

  Bedogni, Barbara ^a   Warneke, James A ^b   Nickoloff, Brian J ^c   Giaccia, Amato J ^a   Powell, Marianne Broome ^a,d  

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c LOYOLA UNIVERSITY MEDICAL CENTER   (United States)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NOTCH1 RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL PROLIFERATION; CONTROLLED STUDY; GENE ACTIVATION; GENE INTERACTION; HUMAN; HUMAN CELL; HYPOXIA; MALE; MELANOCYTE; MELANOMA; MOUSE; NONHUMAN; ONCOGENE; ONCOGENE AKT; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TUMOR GROWTH; TUMOR SUPPRESSOR GENE; XENOGRAFT;

ANIMALS; ANOXIA; CELL LINE, TUMOR; GENES, REPORTER; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LUCIFERASES; MALE; MELANOCYTES; MELANOMA; MICE; MICE, SCID; NF-KAPPA B; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, NOTCH1; RNA, MESSENGER; SIGNAL TRANSDUCTION; UP-REGULATION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 55849139852     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI36157     Document Type: Article

References (66)

1. Demunter, A., Stas, M., Degreef, H., De Wolf-Peeters, C., and van den Oord, J.J. 2001. Analysis of N- and K-ras mutations in the distinctive tumor progression phases of melanoma. J. Invest. Dermatol. 117:1483- 1489.
2. Davies, H., et al. 2002. Mutations of the BRAF gene in human cancer. Nature. 417:949-954.
3. Stahl, J.M., et al. 2004. Deregulated Akt3 activity promotes development of malignant melanoma. Cancer Res. 64:7002-7010.
4. Cannon-Albright, L.A., Kamb, A., and Skolnick, M. 1996. A review of inherited predisposition to melanoma. Semin. Oncol. 23:667-672.
5. Artavanis-Tsakonas, S., Rand, M.D., and Lake, R.J. 1999. Notch signaling: cell fate control and signal integration in development. Science. 284:770-776.
6. Kadesch, T. 2004. Notch signaling: the demise of elegant simplicity. Curr. Opin. Genet. Dev. 14:506-512.
7. Ellisen, L.W., et al. 1991. TAN-1, the human homolog of the Drosophila notch gene, is broken by chromosomal translocations in T lymphoblastic neoplasms. Cell. 66:649-661.
8. Grabher, C., von Boehmer, H., and Look, A.T. 2006. Notch 1 activation in the molecular pathogenesis of T-cell acute lymphoblastic leukaemia. Nat. Rev. Cancer. 6:347-359.
9. O'Neil, J., et al. 2007. FBW7 mutations in leukemic cells mediate NOTCH pathway activation and resistance to gamma-secretase inhibitors. J. Exp. Med. 204:1813-1824.
10. Song, J.H., Schnittke, N., Zaat, A., Walsh, C.S., and Miller, C.W. 2008. FBXW7 mutation in adult T-cell and B-cell acute lymphocytic leukemias. Leuk. Res. 32:1751-1755.
11. Konishi, J., et al. 2007. Gamma-secretase inhibitor prevents Notch3 activation and reduces proliferation in human lung cancers. Cancer Res. 67:8051-8057.
12. Pahlman, S., Stockhausen, M.T., Fredlund, E., and Axelson, H. 2004. Notch signaling in neuroblastoma. Semin. Cancer Biol. 14:365-373.
13. Rangarajan, A., et al. 2001. Activated Notch1 signaling cooperates with papillomavirus oncogenes in transformation and generates resistance to apoptosis on matrix withdrawal through PKB/Akt. Virology. 286:23-30.
14. Santagata, S., et al. 2004. JAGGED1 expression is associated with prostate cancer metastasis and recurrence. Cancer Res. 64:6854-6857.
15. Sjolund, J., et al. 2008. Suppression of renal cell carcinoma growth by inhibition of Notch signaling in vitro and in vivo. J. Clin. Invest. 118:217-228.
16. Nicolas, M., et al. 2003. Notch1 functions as a tumor suppressor in mouse skin. Nat. Genet. 33:416-421.
17. Xia, X., et al. 2001. Loss of presenilin 1 is associated with enhanced beta-catenin signaling and skin tumorigenesis. Proc. Natl. Acad. Sci. U. S. A. 98:10863-10868.
18. Hoek, K., et al. 2004. Expression profiling reveals novel pathways in the transformation of melanocytes to melanomas. Cancer Res. 64:5270-5282.
19. Qin, J.Z., et al. 2004. p53-independent NOXA induction overcomes apoptotic resistance of malignant melanomas. Mol. Cancer Ther. 3:895-902.
20. Balint, K., et al. 2005. Activation of Notch1 signaling is required for beta-catenin-mediated human primary melanoma progression. J. Clin. Invest. 115:3166-3176.
21. Liu, Z.J., et al. 2006. Notch1 signaling promotes primary melanoma progression by activating mitogen-activated protein kinase/phosphatidylinositol 3-kinase-Akt pathways and up-regulating N-cadherin expression. Cancer Res. 66:4182-4190.
22. Weijzen, S., et al. 2002. Activation of Notch-1 signaling maintains the neoplastic phenotype in human Ras-transformed cells. Nat. Med. 8:979-986.
23. Lamont, R.E., and Childs, S. 2006. MAPping out arteries and veins. Sci. STKE. 2006:pe39.
24. Calzavara, E., et al. 2008. Reciprocal regulation of Notch and PI3K/Akt signalling in T-ALL cells in vitro. J. Cell. Biochem. 103:1405-1412.
25. Palomero, T., et al. 2007. Mutational loss of PTEN induces resistance to NOTCH1 inhibition in T-cell leukemia. Nat. Med. 13:1203-1210.
26. Gustafsson, M.V., et al. 2005. Hypoxia requires notch signaling to maintain the undifferentiated cell state. Dev. Cell. 9:617-628.
27. Bedogni, B., et al. 2005. The hypoxic microenvironment of the skin contributes to Akt mediated melanocyte transformation. Cancer Cell. 8:443-454.
28. Evans, S.M., Schrlau, A.E., Chalian, A.A., Zhang, P., and Koch, C.J. 2006. Oxygen levels in normal and previously irradiated human skin as assessed by EF5 binding. J. Invest. Dermatol. 126:2596-2606.
29. Miele, L., Miao, H., and Nickoloff, B.J. 2006. NOTCH signaling as a novel cancer therapeutic target. Curr. Cancer Drug Targets. 6:313-323.
30. Rhodes, D.R., et al. 2004. ONCOMINE: a cancer microarray database and integrated data-mining platform. Neoplasia. 6:1-6.
31. Miele, L. 2006. Notch signaling. Clin. Cancer Res. 12:1074-1079.
32. Haluska, F.G., et al. 2006. Genetic alterations in signaling pathways in melanoma. Clin. Cancer Res. 12:2301s-2307s.
33. Bedogni, B., et al. 2004. Topical treatment with inhibitors of the phosphatidylinositol 3′-kinase/Akt and Raf/mitogen-activated protein kinase kinase/extracellular signal-regulated kinase pathways reduces melanoma development in severe combined immunodeficient mice. Cancer Res. 64:2552-2560.
34. Dhawan, P., Singh, A.B., Ellis, D.L., and Richmond, A. 2002. Constitutive activation of Akt/protein kinase B in melanoma leads to up-regulation of nuclear factor-kappaB and tumor progression. Cancer Res. 62:7335-7342.
35. Amiri, K.I., and Richmond, A. 2005. Role of nuclear factor-kappa B in melanoma. Cancer Metastasis Rev. 24:301-313.
36. Osipo, C., Golde, T.E., Osborne, B.A., and Miele, L.A. 2008. Off the beaten pathway: the complex cross talk between Notch and NF-kappaB. Lab. Invest. 88:11-17.
37. Dajee, M., Tarutani, M., Deng, H., Cai, T., and Khavari, P.A. 2002. Epidermal Ras blockade demonstrates spatially localized Ras promotion of proliferation and inhibition of differentiation. Oncogene. 21:1527-1538.
38. Vaupel, P., and Mayer, A. 2007. Hypoxia in cancer: significance and impact on clinical outcome. Cancer Metastasis Rev. 26:225-239.
39. Michaylira, C.Z., and Nakagawa, H. 2006. Hypoxic microenvironment as a cradle for melanoma development and progression. Cancer Biol. Ther. 5:476-479.
40. Chen, Y., et al. 2007. Oxygen concentration determines the biological effects of NOTCH-1 signaling in adenocarcinoma of the lung. Cancer Res. 67:7954-7959.
41. Koch, C.J. 2002. Measurement of absolute oxygen levels in cells and tissues using oxygen sensors and 2-nitroimidazole EF5. Methods Enzymol. 352:3-31.
42. Ronchini, C., and Capobianco, A.J. 2001. Induction of cyclin D1 transcription and CDK2 activity by Notch(ic): implication for cell cycle disruption in transformation by Notch(ic). Mol. Cell. Biol. 21:5925-5934.
43. Klinakis, A., et al. 2006. Myc is a Notch1 transcriptional target and a requisite for Notch1-induced mammary tumorigenesis in mice. Proc. Natl. Acad. Sci. U. S. A. 103:9262-9267.
44. Wang, Z., et al. 2006. Down-regulation of notch-1 inhibits invasion by inactivation of nuclear factor-kappaB, vascular endothelial growth factor, and matrix metalloproteinase-9 in pancreatic cancer cells. Cancer Res. 66:2778-2784.
45. Flaherty, K.T. 2006. Chemotherapy and targeted therapy combinations in advanced melanoma. Clin. Cancer Res. 12:2366s-2370s.
46. Sosman, J.A., and Puzanov, I. 2006. Molecular targets in melanoma from angiogenesis to apoptosis. Clin. Cancer Res. 12:2376s-2383s.
47. Bash, J., et al. 1999. Rel/NF-kappaB can trigger the Notch signaling pathway by inducing the expression of Jagged1, a ligand for Notch receptors. EMBO J. 18:2803-2811.
48. Merlino, G., and Noonan, F.P. 2003. Modeling gene-environment interactions in malignant melanoma. Trends Mol. Med. 9:102-108.
49. Zheng, X., et al. 2008. Interaction with factor inhibiting HIF-1 defines an additional mode of cross-coupling between the Notch and hypoxia signaling pathways. Proc. Natl. Acad. Sci. U. S. A. 105:3368-3373.
50. Govindarajan, B., et al. 2007. Overexpression of Akt converts radial growth melanoma to vertical growth melanoma. J. Clin. Invest. 117:719-729.
51. Fried, L., and Arbiser, J.L. 2008. The reactive oxygen-driven tumor: relevance to melanoma. Pigment Cell Melanoma Res. 21:117-122.
52. Klimova, T., and Chandel, N.S. 2008. Mitochondrial complex III regulates hypoxic activation of HIF. Cell Death Differ. 15:660-666.
53. Wang, Z., et al. 2006. Down-regulation of Notch-1 contributes to cell growth inhibition and apoptosis in pancreatic cancer cells. Mol. Cancer Ther. 5:483-493.
54. Nefedova, Y., Sullivan, D.M., Bolick, S.C., Dalton, W.S., and Gabrilovich, D.I. 2008. Inhibition of Notch signaling induces apoptosis of myeloma cells and enhances sensitivity to chemotherapy. Blood. 111:2220-2229.
55. Bedogni, B., and Powell, M.B. 2006. Skin hypoxia: a promoting environmental factor in melanomagenesis. Cell Cycle. 5:1258-1261.
56. Alaluf, S., Muir-Howie, H., Hu, H.L., Evans, A., and Green, M.R. 2000. Atmospheric oxygen accelerates the induction of a post-mitotic phenotype in human dermal fibroblasts: the key protective role of glutathione. Differentiation. 66:147-155.
57. Balin, A.K., and Pratt, L. 2002. Oxygen modulates the growth of skin fibroblasts. In Vitro Cell Dev. Biol. Anim. 38:305-310.
58. Parrinello, S., et al. 2003. Oxygen sensitivity severely limits the replicative lifespan of murine fibroblasts. Nat. Cell Biol. 5:741-747.
59. Harris, A.L. 2002. Hypoxia - a key regulatory factor in tumour growth. Nat. Rev. Cancer. 2:38-47.
60. Gross, A., McDonnell, J.M., and Korsmeyer, S.J. 1999. BCL-2 family members and the mitochondria in apoptosis. Genes Dev. 13:1899-1911.
61. Bheeshmachar, G., et al. 2006. Evidence for a role for notch signaling in the cytokine-dependent survival of activated T cells. J. Immunol. 177:5041-5050.
62. Polsky, D., and Cordon-Cardo, C. 2003. Oncogenes in melanoma. Oncogene. 22:3087-3091.
63. Rosenwald, I.B. 2004. The role of translation in neoplastic transformation from a pathologist's point of view. Oncogene. 23:3230-3247.
64. Rankin, E.B., Tomaszewski, J.E., and Haase, V.H. 2006. Renal cyst development in mice with conditional inactivation of the von Hippel-Lindau tumor suppressor. Cancer Res. 66:2576-2583.
65. Koch, C.J., Evans, S.M., and Lord, E.M. 1995. Oxygen dependence of cellular uptake of EF5 [2-(2-nitro-1H-imidazol-1-yl)-N-(2,2,3,3,3- pentafluoropropyl)a cet amide]: analysis of drug adducts by fluorescent antibodies vs bound radioactivity. Br. J. Cancer. 72:869-874.
66. Arbiser, J.L., et al. 1997. Oncogenic H-ras stimulates tumor angiogenesis by two distinct pathways. Proc. Natl. Acad. Sci. U. S. A. 94:861-866.