The Notch pathway in colorectal cancer

International Journal of Cancer

Volumn 138, Issue 8, 2016, Pages 1835-1842

  Vinson, Kaitlyn E ^a   George, Dennis C ^a   Fender, Alexander W ^a   Bertrand, Fred E ^b,c   Sigounas, George ^a  

^a EAST CAROLINA UNIVERSITY   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

colorectal cancer; EMT; Notch signaling; stemness

Indexed keywords

ANTINEOPLASTIC AGENT; NOTCH1 RECEPTOR; NOTCH RECEPTOR;

APOPTOSIS; CANCER DIAGNOSIS; CANCER MORTALITY; CANCER RESISTANCE; CANCER RISK; CANCER STEM CELL; CARCINOGENESIS; CELL PROLIFERATION; COLORECTAL CANCER; EVIDENCE BASED MEDICINE; HUMAN; METASTASIS POTENTIAL; NONHUMAN; ORGANOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEFECT; PROTEIN FUNCTION; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; COLORECTAL TUMOR; EPITHELIAL MESENCHYMAL TRANSITION; METABOLISM; PATHOLOGY; PHYSIOLOGY;

ANIMALS; COLORECTAL NEOPLASMS; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION;

EID: 84958869389     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.29800     Document Type: Review

References (91)

1. Ferlay J, Soerjomataram I, Ervik M, et al., Cancer incidence and mortality worldwide: IARC CancerBase No. 11. Lyon, France: International Agency for Research on Cancer, 2013.
2. Howlader N, Noone A, Krapcho M, et al., SEER cancer statistics review, 1975-2011. National Cancer Institute, Bethesda, MD, 2014.
3. Previs R, Coleman R, Harris A, et al., Molecular pathways: translational and therapeutic implications of the Notch signaling pathway in cancer. Clin Cancer Res 2015; 21: 955-61.
4. Medma J, Vermeulen L., Microenvironmental regulation of stem cells in intestinal homeostasis and cancer. Nature 2011; 474: 318-26.
5. Vaiopoulos A, Kostakis I, Koutsilieris M, et al., Colorectal cancer stem cells. Stem Cells 2012; 30: 363-71.
6. Bertrand F, Angus C, Partis W, et al., Developmental pathways in colon cancer: crosstalk between WNT, BMP, Hedgehog and Notch. Cell Cycle 2012; 11: 4344-51.
7. Cheng H, Leblond C., Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. Am J Anat 1974; 141: 537-62.
8. Barker N, van Es J, Kuipers J, et al., Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 2007; 449: 1003-7.
9. Kemper K, Grandela C, Medema J., Molecular identification and targeting of colorectal cancer stem cells. Oncotarget 2010; 1: 387-95.
10. Geissler K, Zach O., Pathways involved in drosophila and human cancer development: the Notch, Hedgehog, Wingless, Runt, and Trithorax pathway. Ann Hematol 2012; 91: 645-69.
11. Takebe N, Harris P, Warren R, et al., Targeting cancer stem cells by inhibiting wnt, notch, and hedgehog pathways. Nat Rev Clin Oncol 2011; 8: 97-106.
12. Burgess A, Faux M, Layton M, et al., Wnt signaling and colon tumorigenesis-a view from the periphery. Exp Cell Res 2011; 317: 2748-58.
13. Hardwick J, Kodach L, Offerhaus G, et al., Bone morphogenetic protein signaling in colorectal cancer. Nat Rev Cancer 2008; 8: 806-12.
14. Kosinski C, Li V, Chan A, et al., Gene expression patterns of human colon tops and basal crypts and BMP antagonists as intestinal stem cell niche factors. Proc Natl Acad Sci USA 2007; 104: 15418-23.
15. Brenner H, Kloor M, Pox C., Colorectal cancer. Lancet 2014; 383: 1490-502.
16. National Cancer Institute. PDQ® Genetics of Colorectal Cancer. Bethesda, MD: National Cancer Institute, 2014.
17. Fearon E, Vogelstein B., A genetic model for colorectal tumorigenesis. Cell 1990; 61: 759-67.
18. Markowitz S, Bertagnolli M., Molecular basis of colorectal cancer. N Engl J Med 2009; 361: 2449-60.
19. Hampel H, Frankel W, Martin E, et al., Screening for the lynch syndrome (hereditary nonpolyposis colorectal cancer). N Engl J Med 2005; 352: 1851-60.
20. Boland C, Shin S, Goel A., Promoter methylation in the genesis of gastrointestinal cancer. Yonsei Med J 2009; 50: 309-21.
21. Issa J-P., CpG island methylator phenotype in cancer. Nat Rev Cancer 2004; 4: 988-93.
22. Jones P, Baylin S., The fundamental role of epigenetic events in cancer. Nat Rev Genet 2002; 3: 415-28.
23. Jass J., Classification of colorectal cancer based on correlation of clinical, morphological and molecular features. Histopathology 2007; 50: 113-30.
24. Bretthauer M., Colorectal cancer screening. J Intern Med 2011; 270: 87-98.
25. Ntziachristos P, Lim JS, Sage J, et al., From fly wings to targeted cancer therapies: a centennial for notch signaling. Cancer Cell 2014; 25: 318-34.
26. Aithal M, Rajeswari N., Role of Notch signaling pathway in cancer and its association with DNA methylation. J Genet 2013; 92: 667-75.
27. Al-Hussaini H, Subramanyam D, Reedijk M, et al., Notch signaling pathway as a therapeutic target in breast cancer. Mol Cancer Ther 2011; 10: 9-15.
28. Brou C., Intracellular trafficking of notch receptors and ligands. Exp Cell Res 2009; 315: 1549-55.
29. Karamboulas C, Ailles L., Developmental signaling pathways in cancer stem cells of solid tumors. Biochim Biophys Acta 2013; 1830: 2481-95.
30. Schwanbeck R., The role of epigenetic mechanisms in Notch signaling during development. J Cell Physiol 2015;230:969-81.
31. Llagan X, Kopan R., SnapShot: notch signaling pathway. Cell 2007; 128: e1-e2.
32. Rodilla V, Villanueva A, Obrador-Hevia A, et al., Jagged1 is the pathological link between wnt and notch pathways in colorectal cancer. Proc Natl Acad Sci USA 2009; 106: 6315-20.
33. 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.
34. Wu W, Wang X, Cheng A, et al., Dysregulation and crosstalk of cellular signaling pathways in colon carcinogenesis. Crit Rev Oncol Hematol 2013; 86: 251-77.
35. Zhang Y, Li B, Ji Z-Z, et al., Notch1 regulates the growth of human colon cancers. Cancer 2010; 116: 5207-18.
36. Reedijk M, Odorcic S, Zhang H, et al., Activation of Notch signaling in human colon adenocarcinoma. Int J Oncol 2008; 33: 1223-9.
37. Chen X, Johns D, Geiman D, et al., Kruppel-like factor 4 (gut-enriched Kruppel-like factor) inhibits cell proliferation by blocking G1/S progression of the cell cycle. J Biol Chem 2001; 276: 30423-8.
38. Chu D, Zhang Z, Zhou Y, et al., Notch1 and Notch2 have opposite prognostic effects on patients with colorectal cancer. Ann Oncol 2011; 22: 2440-7.
39. Serafin V, Persano L, Moserle L, et al., Notch3 signalling promotes tumour growth in colorectal cancer. J Pathol 2011; 224: 448-60.
40. Bordonaro M, Tewari S, Atamna W, et al., The notch ligand delta-like 1 integrates inputs from TGFbeta/Activin and wnt pathways. Exp Cell Res 2011; 317: 1368-81.
41. Espinoza I, Miele L., Deadly crosstalk: Notch signaling at the intersection of EMT and cancer stem cells. Cancer Lett 2013; 341: 41-5.
42. Wang Z, Li Y, Kong D, et al., The role of Notch signaling pathway in epithelial-mesenchymal transition (EMT) during development and tumor aggressiveness. Curr Drug Targets 2010; 11: 745-51.
43. Becker K, Rosivatz E, Blechschmidt K, et al., Analysis of the E-cadherin repressor Snail in primary human cancers. Cells Tissues Organs 2007; 185: 204-12.
44. Fender AW, Nutter JM, Bertrand FE, et al., Notch-1 promotes stemness and epithelial to mesenchymal transition in colorectal cancer. J Cell Biochem 2015 Apr 25. doi: 10.1002/jcb.25196. [Epub ahead of print].
45. Roy S, Majumdar A., Signaling in colon cancer stem cells. J Mol Signal 2012; 7: 11.
46. Sikandar S, Pate K, Anderson S, et al., Notch signaling is required for formation and self-renewal of tumor-initiating cells and for repression of secretory cell differentiation in colon cancer. Cancer Res 2010; 70: 1469-78.
47. Hoey T, Yen W, Axelrod F, et al., DLL4 blockage inhibits tumor growth and reduces tumor-initiating cell frequency. Cell Stem Cell 2009; 5: 168-77.
48. Visvader J, Lindeman G., Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 2008; 8: 755-68.
49. Guo S, Liu M, Gonzalez-Perez R., Role of notch and its oncogenic signaling crosstalk in breast cancer. Biochim Biophys Acta 2011; 1815: 197-213.
50. Katoh M, Katoh M., WNT signaling pathway and stem cell signaling network. Clin Cancer Res 2007; 13: 4042-5.
51. Nakamura T, Tsuchiya K, Watanabe M., Crosstalk between wnt and notch signaling in intestinal epithelial cell fate decision. J Gastroenterol 2007; 42: 705-10.
52. Crosnier C, Stamataki D, Lewis J., Organizing cell renewal in the intestine: stem cells, signals and combinatorial control. Nat Rev Genet 2006; 7: 349-59.
53. Leow C, Romero M, Ross S, et al., Hath1, down-regulated in colon adenocarcinomas, inhibits proliferation and tumorigenesis of colon cancer cells. Cancer Res 2004; 64: 6050-7.
54. Korinek V, Barker N, Morin P, et al., Constitutive transcriptional activation by a ß-catenin-tcf complex in APC-/- colon carcinoma. Science 1997; 275: 1784-7.
55. Fre S, Pallavi S, Huyghe M, et al., Notch and wnt signals cooperatively control cell proliferation and tumorigenesis in the intestine. Proc Natl Acad Sci USA 2009; 106: 6309-14.
56. van Es J, van Gijn M, Riccio O, et al., Notch/[gamma]-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature 2005 435: 959-63.
57. Ungerback J, Elander N, Grunberg J, et al., The notch-2 gene is regulated by wnt signaling in cultured colorectal cancer cells. PLoS One 2011; 6:e17957.
58. Kim HA, Koo BK, Cho JH, et al., Notch1 counteracts WNT/[beta]-catenin signaling through chromatin modification in colorectal cancer. J Clin Invest 2012; 122: 3248-59.
59. Peignon G, Durand A, Cacheux W, et al., Complex interplay between ß-catenin signalling and notch effectors in intestinal tumorigenesis. Gut 2011; 60: 166-76.
60. Cutsem E, Kohne C, Hitre E, et al., Cetuximab and chemotherapy as initial treatment for metastatic colorectal cancer. N Engl J Med 2009; 360: 1408-17.
61. Cunningham D, Humblet Y, Siena S, et al., Cetuximab monotherapy and cetuximab plus irinotecan in irinotecan-refractory metastatic colorectal cancer. N Engl J Med 2004; 351: 337-45.
62. Lenz H, Van Cutsem E, Khambata-Ford S, et al., Multicenter phase II and translational study of cetuximab in metastatic colorectal carcinoma refractory to irinotecan, oxaliplatin, and flouropyrimidines. J Clin Oncol 2006; 24: 4914-21.
63. Goldberg R, Sargent D, Morton R, et al., A randomized controlled trial of fluorouracil plus leucovorin, irinotecan, and oxaliplatin combinations in patients with previously untreated metastatic colorectal cancer. J Clin Oncol 2004; 22: 23-30.
64. Modulation of fluorouracil by leucovorin in patients with advanced colorectal cancer: evidence in terms of response rate. Advanced colorectal cancer meta-analysis project. J Clin Oncol 1992; 10: 896-903.
65. Hsiang Y, Hertzberg R, Hecht S, et al., Camptothecin induces protein-linked DNA breaks via mammalian DNA topoisomerase I. J Biol Chem 1985; 260: 14873-8.
66. Saltz L, Cox J, Blanke C, et al, Irinotecan study group irinotecan plus fluorouracil and leucovorin for metastatic colorectal cancer. Irinotecan Study Group. N Engl J Med 2000; 343: 905-14.
67. Douillard J, Cunningham D, Roth A, et al., Irinotecan combined with fluorouracil compared with fluorouracil alone as first-line treatment for metastatic colorectal cancer: a multicenter randomised trial. Lancet 2000; 355: 1041-7.
68. De Gramont A, Figer A, Seymour M, et al., Leucovorin and fluorouracil with or without oxaliplatin as first-line treatment in advanced colorectal cancer. J Clin Oncol 2000; 18: 2938-47.
69. Aste-Amezaga M, Zhang N, Lineberger J, et al., Characterization of Notch1 antibodies that inhibit signaling of both normal and mutated Notch1 receptors. PLoS One 2010; 5:e9094.
70. Li K, Li Y, Wu W, et al., Modulation of notch signaling by antibodies specific for the extracellular negative regulatory region of NOTCH3. J Biol Chem 2008; 283: 8046-54.
71. Wu Y, Cain-Hom C, Choy L, et al., Therapeutic antibody targeting of individual notch receptors. Nature 2010; 464: 1052-7.
72. Ridgway J, Zhang G, Wu Y, et al., Inhibition of Dll4 signaling inhibits tumour growth by deregulating angiogenesis. Nature 2006; 444: 1083-7.
73. Noguera-Troise I, Daly C, Papadopoulos N, et al., Blockade of Dll4 inhibits tumour growth by promoting non-productive angiogenesis. Nature 2006; 444: 1032-7.
74. Scehent J, Jiang W, Kumar S, et al., Inhibition of Dll4-mediated signaling induces proliferation of immature vessels and results in poor tissue perfusion. Blood 2007; 109: 4753-60.
75. Reynolds N, Lukacs N, Long N, et al., Delta-like ligand 4 regulates central nervous system T cell accumulation during experimental autoimmune encephalomyelitis. J Immunol 2011; 187: 2803-13.
76. Espinoza I, Miele L., Notch inhibitors for cancer treatment. Pharmacol Ther 2013; 139: 95-110.
77. Funahashi Y, Hernandez S, Das I, et al., A notch1 ectodomain construct inhibits endothelial notch signaling, tumor growth, and angiogenesis. Cancer Res 2008; 68: 4727-35.
78. Varnum-Finney B, Wu L, Yu M, et al., Immobilization of Notch ligand, Delta-1, is required for induction of notch signaling. J Cell Sci 2000; 113: 4313 -1 8.
79. Aster J, Pear W, Blacklow S., Notch signaling in leukemia. Annu Rev Pathol 2008; 3: 587-613.
80. Tammam J, Ware C, Efferson C, et al., Down-regulation of the Notch pathway mediated by a gamma-secretase inhibitor induces anti-tumour effects in mouse models of T-cell leukaemia. Br J Pharmacol 2009; 158: 1183-95.
81. Wei P, Walls M, Qiu M, et al., Evaluation of selective gamma-secretase inhibitor PF-03084014 for its antitumor efficacy and gastrointestinal safety to guide optimal clinical trial design. Mol Cancer Ther 2010; 9: 1618-28.
82. Fouladi M, Stewart C, Olson K, et al., Phase I trial of MK-0752 in children with refractory CNS malignancies: a pediatric brain tumor consortium study. J Clin Oncol 2011; 29: 3529-34.
83. Pandya K, Meeke K, Clementz A, et al., Targeting both Notch and ErB-2 signaling pathways is required for prevention of ErB-2-positive breast tumour recurrence. Br J Cancer 2011; 105: 796-806.
84. Moellering R, Cornejo M, Davis T, et al., Direct inhibition of the NOTCH transcription factor complex. Nature 2009; 462: 182-8.
85. Wang Z, Zhang Y, Banerjee S, et al., 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.
86. Wang Z, Zhang Y, Banerjee S, et al., 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.
87. Wang H, Zou J, Zhao B, et al., Genome-wide analysis reveals conserved and divergent features of Notch1/RBPJ binding in human and murine T-lymphoblastic leukemia cells. Proc Natl Acad Sci USA 2011; 108: 14908-13.
88. Kawahara T, Kawaguchi-Ihara N, Okuhashi Y, et al., Cyclopamine and quercetin suppress the growth of leukemia and lymphoma cells. Anticancer Res 2009; 29: 4629-32.
89. Kallifatidis G, Labsch S, Rausch V, et al., Sulforaphane increases drug-mediated cytotoxicity toward cancer stem-like cells of pancreas and prostate. Mol Ther 2011; 19: 188-95.
90. Zhou W, Kallifatidis G, Baumann B, et al., Dietary polyphenol quercetin targets pancreatic cancer stem cells. Int J Oncol 2010; 37: 551-61.
91. Liao S, Xia J, Chen Z, et al., Inhibitory effect of curumin on oral carcinoma CAL-27 cells via suppression of Notch-1 and NF-kappaB signaling pathways. J Cell Biochem 2011; 112: 1055-65.