The role of notch signaling pathway in Epithelial-Mesenchymal Transition (EMT) during development and tumor aggressiveness

Current Drug Targets

Volumn 11, Issue 6, 2010, Pages 745-751

  Wang, Zhiwei ^a   Li, Yiwei ^a   Kong, Dejuan ^a   Sarkar, Fazlul H ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cancer; EMT; Notch

Indexed keywords

CURCUMIN; FIBROBLAST GROWTH FACTOR; GAMMA SECRETASE; GENISTEIN; I KAPPA B; JAGGED1; NOTCH RECEPTOR; NOTCH1 RECEPTOR; PLATELET DERIVED GROWTH FACTOR; RESVERATROL; TRANSCRIPTION FACTOR HES 1; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; TRANSFORMING GROWTH FACTOR BETA; UVOMORULIN;

APOPTOSIS; ARTICLE; BINDING AFFINITY; CANCER CELL; CANCER GROWTH; CANCER PREVENTION; CANCER THERAPY; CARCINOGENESIS; CELL DIFFERENTIATION; CELL GROWTH; CELL MATURATION; CELL PROLIFERATION; DNA BINDING; DOWN REGULATION; EPITHELIUM CELL; GENE OVEREXPRESSION; GENE REPRESSION; HOMEOSTASIS AND REGULATION; MALIGNANT NEOPLASTIC DISEASE; MESENCHYME CELL; MOLECULAR INTERACTION; MOLECULAR MECHANICS; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; SIGNAL TRANSDUCTION; TARGET CELL; TUMOR GROWTH; UPREGULATION;

ANIMALS; CELL TRANSDIFFERENTIATION; EPITHELIUM; HUMANS; MESODERM; NEOPLASMS; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION;

EID: 77953523118     PISSN: 13894501     EISSN: None     Source Type: Journal    
DOI: 10.2174/138945010791170860     Document Type: Article

References (82)

1. Christiansen JJ, Rajasekaran AK. Reassessing epithelial to mesenchymal transition as a prerequisite for carcinoma invasion and metastasis. Cancer Res 2006; 66: 8319-26.
2. Klymkowsky MW, Savagner P. Epithelial-mesenchymal transition: a cancer researcher's conceptual friend and foe. Am J Pathol 2009; 174: 1588-93.
3. Min C, Eddy SF, Sherr DH, Sonenshein GE. NF-kappaB and epithelial to mesenchymal transition of cancer. J Cell Biochem 2008; 104: 733-44.
4. Moreno-Bueno G, Portillo F, Cano A. Transcriptional regulation of cell polarity in EMT and cancer. Oncogene 2008; 27: 6958-69.
5. Thiery JP, Sleeman JP. Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 2006; 7: 131-42.
6. Prindull G. Hypothesis: cell plasticity, linking embryonal stem cells to adult stem cell reservoirs and metastatic cancer cells? Exp Hematol 2005; 33: 738-46.
7. Wang Z, Li Y, Kong D, et al. Acquisition of epithelial-mesenchymal transition phenotype of gemcitabine-resistant pancreatic cancer cells is linked with activation of the notch signaling pathway. Cancer Res 2009; 69: 2400-7.
8. Fuchs BC, Fujii T, Dorfman JD, et al. Epithelial-to-mesenchymal transition and integrin-linked kinase mediate sensitivity to epidermal growth factor receptor inhibition in human hepatoma cells. Cancer Res 2008; 68: 2391-9.
9. Cheng GZ, Chan J, Wang Q, Zhang W, Sun CD, Wang LH. Twist transcriptionally up-regulates AKT2 in breast cancer cells leading to increased migration, invasion, and resistance to paclitaxel. Cancer Res 2007; 67: 1979-87.
10. Sabbah M, Emami S, Redeuilh G, et al. Molecular signature and therapeutic perspective of the epithelial-to-mesenchymal transitions in epithelial cancers. Drug Resist Updat 2008; 11: 123-51.
11. Kong D, Wang Z, Sarkar SH, et al. Platelet-derived growth factor-D overexpression contributes to epithelial-mesenchymal transition of PC3 prostate cancer cells. Stem Cells 2008; 26: 1425-35.
12. Moustakas A, Heldin CH. Signaling networks guiding epithelial-mesenchymal transitions during embryogenesis and cancer progression. Cancer Sci 2007; 98: 1512-20.
13. Zavadil J, Bottinger EP. TGF-beta and epithelial-to-mesenchymal transitions. Oncogene 2005; 24: 5764-74.
14. Gregory PA, Bracken CP, Bert AG, Goodall GJ. MicroRNAs as regulators of epithelial-mesenchymal transition. Cell Cycle 2008;7:3112-8.
15. Peter ME. Let-7 and miR-200 microRNAs: guardians against pluripotency and cancer progression. Cell Cycle 2009; 8: 843-52.
16. Cannito S, Novo E, Compagnone A, et al. Redox mechanisms switch on hypoxia-dependent epithelial-mesenchymal transition in cancer cells. Carcinogenesis 2008; 29: 2267-78.
17. Yang MH, Wu MZ, Chiou SH, et al. Direct regulation of TWIST by HIF-1alpha promotes metastasis. Nat Cell Biol 2008; 10: 295-305.
18. Niessen K, Fu Y, Chang L, Hoodless PA, McFadden D, Karsan A. Slug is a direct Notch target required for initiation of cardiac cushion cellularization. J Cell Biol 2008; 182: 315-25.
19. Sahlgren C, Gustafsson MV, Jin S, Poellinger L, Lendahl U. Notch signaling mediates hypoxia-induced tumor cell migration and invasion. Proc Natl Acad Sci U S A 2008; 105: 6392-7.
20. Timmerman LA, Grego-Bessa J, Raya A, et al. Notch promotes epithelial-mesenchymal transition during cardiac development and oncogenic transformation. Genes Dev 2004; 18: 99-115.
21. Zavadil J, Cermak L, Soto-Nieves N, Bottinger EP. Integration of TGF-beta/Smad and Jagged1/Notch signalling in epithelial-to-mesenchymal transition. EMBO J 2004; 23: 1155-65.
22. Wang Z, Li Y, Banerjee S, Sarkar FH. Emerging role of Notch in stem cells and cancer. Cancer Lett 2009; 279: 8-12.
23. Guarino M, Rubino B, Ballabio G. The role of epithelial-mesenchymal transition in cancer pathology. Pathology 2007; 39: 305-18.
24. Hugo H, Ackland ML, Blick T, et al. Epithelial--mesenchymal and mesenchymal--epithelial transitions in carcinoma progression. J Cell Physiol 2007; 213: 374-83.
25. Miele L, Osborne B. Arbiter of differentiation and death: Notch signaling meets apoptosis. J Cell Physiol 1999; 181: 393-409.
26. Miele L, Miao H, Nickoloff BJ. Notch signaling as a novel cancer therapeutic target. Curr Cancer Drug Targets 2006; 6: 313-23.
27. Miele L. Notch signaling. Clin Cancer Res 2006; 12: 1074-9.
28. Kopan R, Ilagan MX. The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 2009; 137: 216-33.
29. Dotto GP. Notch tumor suppressor function. Oncogene 2008; 27: 5115-23.
30. Dufraine J, Funahashi Y, Kitajewski J. Notch signaling regulates tumor angiogenesis by diverse mechanisms. Oncogene 2008; 27:5132-7.
31. Wang Z, Banerjee S, Li Y, Rahman KM, Zhang Y, Sarkar FH. Down-regulation of Notch-1 inhibits invasion by inactivation of nuclear factor-{kappa}B, vascular endothelial growth factor, and matrix metalloproteinase-9 in pancreatic cancer cells. Cancer Res 2006; 66: 2778-84.
32. Wang Z, Zhang Y, Banerjee S, Li Y, Sarkar FH. Inhibition of nuclear factor kappab activity by genistein is mediated via Notch-1 signaling pathway in pancreatic cancer cells. Int J Cancer 2006; 118: 1930-6.
33. Shi TP, Xu H, Wei JF, et al. Association of low expression of notch-1 and jagged-1 in human papillary bladder cancer and shorter survival. J Urol 2008; 180: 361-6.
34. Reedijk M, Pinnaduwage D, Dickson BC, et al. JAG1 expression is associated with a basal phenotype and recurrence in lymph node-negative breast cancer. Breast Cancer Res Treat 2008; 111: 439-48.
35. Dickson BC, Mulligan AM, Zhang H, et al. High-level JAG1 mRNA and protein predict poor outcome in breast cancer. Mod Pathol 2007; 20: 685-93.
36. Zhu YM, Zhao WL, Fu JF, et al. NOTCH1 mutations in T-cell acute lymphoblastic leukemia: prognostic significance and implication in multifactorial leukemogenesis. Clin Cancer Res 2006; 12: 3043-9.
37. Reedijk M, Odorcic S, Chang L, et al. High-level coexpression of JAG1 and NOTCH1 is observed in human breast cancer and is associated with poor overall survival. Cancer Res 2005; 65: 8530-7.
38. Parr C, Watkins G, Jiang WG. The possible correlation of Notch-1 and Notch-2 with clinical outcome and tumour clinicopathological parameters in human breast cancer. Int J Mol Med 2004; 14: 779-86.
39. Santagata S, Demichelis F, Riva A, et al. JAGGED1 expression is associated with prostate cancer metastasis and recurrence. Cancer Res 2004; 64: 6854-7.
40. Reedijk M, Odorcic S, Chang L, et al. High-level coexpression of JAG1 and NOTCH1 is observed in human breast cancer and is associated with poor overall survival. Cancer Res 2005; 65: 8530-7.
41. Reedijk M, Pinnaduwage D, Dickson BC, et al. JAG1 expression is associated with a basal phenotype and recurrence in lymph node-negative breast cancer. Breast Cancer Res Treat 2008; 111: 439-48.
42. Wang Z, Li Y, Banerjee S, Sarkar FH. Exploitation of the Notch signaling pathway as a novel target for cancer therapy. Anticancer Res 2008; 28: 3621-30.
43. Guo X, Wang XF. Signaling cross-talk between TGF-beta/BMP and other pathways. Cell Res 2009; 19: 71-88.
44. Poellinger L, Lendahl U. Modulating Notch signaling by pathway-intrinsic and pathway-extrinsic mechanisms. Curr Opin Genet Dev 2008; 18: 449-54.
45. Rizzo P, Osipo C, Foreman K, Golde T, Osborne B, Miele L. Rational targeting of Notch signaling in cancer. Oncogene 2008; 27: 5124-31.
46. Zardawi SJ, O'Toole SA, Sutherland RL, Musgrove EA. Dysregulation of Hedgehog, Wnt and Notch signalling pathways in breast cancer. Histol Histopathol 2009; 24: 385-98.
47. Noseda M, McLean G, Niessen K, et al. Notch activation results in phenotypic and functional changes consistent with endothelial-to-mesenchymal transformation. Circ Res 2004; 94: 910-7.
48. Becker KF, Rosivatz E, Blechschmidt K, Kremmer E, Sarbia M, Hofler H. Analysis of the E-cadherin repressor Snail in primary human cancers. Cells Tissues Organs 2007; 185: 204-12.
49. Kuphal S, Palm HG, Poser I, Bosserhoff AK. Snail-regulated genes in malignant melanoma. Melanoma Res 2005; 15: 305-13.
50. Shioiri M, Shida T, Koda K, et al. Slug expression is an independent prognostic parameter for poor survival in colorectal carcinoma patients. Br J Cancer 2006; 94: 1816-22.
51. Elloul S, Elstrand MB, Nesland JM, et al. Snail, Slug, and Smad-interacting protein 1 as novel parameters of disease aggressiveness in metastatic ovarian and breast carcinoma. Cancer 2005; 103: 1631-43.
52. Uchikado Y, Natsugoe S, Okumura H, et al. Slug Expression in the E-cadherin preserved tumors is related to prognosis in patients with esophageal squamous cell carcinoma. Clin Cancer Res 2005; 11: 1174-80.
53. Jethwa P, Naqvi M, Hardy RG, et al. Overexpression of Slug is associated with malignant progression of esophageal adenocarcinoma. World J Gastroenterol 2008; 14: 1044-52.
54. Castro AC, Rosivatz E, Schott C, et al. Slug is overexpressed in gastric carcinomas and may act synergistically with SIP1 and Snail in the down-regulation of E-cadherin. J Pathol 2007; 211: 507-15.
55. Leong KG, Niessen K, Kulic I, et al. Jagged1-mediated Notch activation induces epithelial-to-mesenchymal transition through Slug-induced repression of E-cadherin. J Exp Med 2007; 204: 2935-48.
56. Niimi H, Pardali K, Vanlandewijck M, Heldin CH, Moustakas A. Notch signaling is necessary for epithelial growth arrest by TGF-beta. J Cell Biol 2007; 176: 695-707.
57. Walsh DW, Roxburgh SA, McGettigan P, et al. Co-regulation of Gremlin and Notch signalling in diabetic nephropathy. Biochim Biophys Acta 2008; 1782: 10-21.
58. Katoh M, Katoh M. FGF signaling network in the gastrointestinal tract (review). Int J Oncol 2006; 29: 163-8.
59. Katoh M. Networking of WNT, FGF, Notch, BMP, and Hedgehog signaling pathways during carcinogenesis. Stem Cell Rev 2007; 3: 30-8.
60. Katoh M, Katoh M. Cross-talk of WNT and FGF signaling pathways at GSK3beta to regulate beta-catenin and SNAIL signaling cascades. Cancer Biol Ther 2006; 5: 1059-64.
61. Billottet C, Elkhatib N, Thiery JP, Jouanneau J. Targets of fibroblast growth factor 1 (FGF-1) and FGF-2 signaling involved in the invasive and tumorigenic behavior of carcinoma cells. Mol Biol Cell 2004; 15: 4725-34.
62. Billottet C, Tuefferd M, Gentien D, et al. Modulation of several waves of gene expression during FGF-1 induced epithelial-mesenchymal transition of carcinoma cells. J Cell Biochem 2008; 104: 826-39.
63. Wang Z, Kong D, Li Y, Sarkar FH. PDGF-D signaling: a novel target in cancer therapy. Curr Drug Targets 2009; 10: 38-41.
64. Li X, Eriksson U. Novel PDGF family members: PDGF-C and PDGF-D. Cytokine Growth Factor Rev 2003; 14: 91-8.
65. Fredriksson L, Li H, Eriksson U. The PDGF family: four gene products form five dimeric isoforms. Cytokine Growth Factor Rev 2004; 15: 197-204.
66. Reigstad LJ, Varhaug JE, Lillehaug JR. Structural and functional specificities of PDGF-C and PDGF-D, the novel members of the platelet-derived growth factors family. FEBS J 2005; 272: 5723-41.
67. Shih AH, Holland EC. Platelet-derived growth factor (PDGF) and glial tumorigenesis. Cancer Lett 2006; 232: 139-47.
68. Pietras K, Sjoblom T, Rubin K, Heldin CH, Ostman A. PDGF receptors as cancer drug targets. Cancer Cell 2003; 3: 439-43.
69. Yu J, Ustach C, Kim HR. Platelet-derived growth factor signaling and human cancer. J Biochem Mol Biol 2003; 36: 49-59.
70. Claxton S, Fruttiger M. Periodic Delta-like 4 expression in developing retinal arteries. Gene Expr Patterns 2004; 5: 123-7.
71. Wang Z, Kong D, Banerjee S, et al. Down-regulation of platelet-derived growth factor-D inhibits cell growth and angiogenesis through inactivation of Notch-1 and nuclear factor-kappaB signaling. Cancer Res 2007; 67: 11377-85.
72. Kong D, Li Y, Wang Z, et al. The MiR-200 Regulates PDGF-D Mediated Epithelial-Mesenchymal Transition, Adhesion and Invasion of Prostate Cancer Cells. Stem Cells 2009; 27: 1712-21.
73. Wang Z, Zhang Y, Li Y, Banerjee S, Liao J, Sarkar FH. Down-regulation of Notch-1 contributes to cell growth inhibition and apoptosis in pancreatic cancer cells. Mol Cancer Ther 2006; 5: 483-93.
74. Wang Z, Zhang Y, Banerjee S, Li Y, Sarkar FH. Notch-1 down-regulation by curcumin is associated with the inhibition of cell growth and the induction of apoptosis in pancreatic cancer cells. Cancer 2006; 106: 2503-13.
75. Shah AN, Summy JM, Zhang J, Park SI, Parikh NU, Gallick GE. Development and characterization of gemcitabine-resistant pancreatic tumor cells. Ann Surg Oncol 2007; 14: 3629-37.
76. Arumugam T, Ramachandran V, Fournier KF, et al. Epithelial to Mesenchymal Transition Contributes to Drug Resistance in Pancreatic Cancer. Cancer Res 2009; 69: 5820-8.
77. O'Neil J, Calvo J, McKenna K, et al. Activating Notch1 mutations in mouse models of T-ALL. Blood 2006; 107: 781-5.
78. Zhang Y, Wang Z, Ahmed F, Banerjee S, Li Y, Sarkar FH. Down-regulation of Jagged-1 induces cell growth inhibition and S phase arrest in prostate cancer cells. Int J Cancer 2006; 119: 2071-7.
79. Barten DM, Meredith JE, Jr., Zaczek R, Houston JG, Albright CF. Gamma-secretase inhibitors for Alzheimer's disease: balancing efficacy and toxicity. Drugs R D 2006; 7: 87-97.
80. Shih I, Wang TL. Notch signaling, gamma-secretase inhibitors, and cancer therapy. Cancer Res 2007; 67: 1879-82.
81. Cecchinato V, Chiaramonte R, Nizzardo M et al. Resveratrol-induced apoptosis in human T-cell acute lymphoblastic leukaemia MOLT-4 cells. Biochem Pharmacol 2007; 74: 1568-74.
82. Zhang Z, Wang Y, Yao R, et al. Cancer chemopreventive activity of a mixture of Chinese herbs (antitumor B) in mouse lung tumor models. Oncogene 2004; 23: 3841-50.