Targeting notch to eradicate pancreatic cancer stem cells for cancer therapy

Anticancer Research

Volumn 31, Issue 4, 2011, Pages 1105-1113

  Wang, Zhiwei ^a   Ahmad, Aamir ^a   Li, Yiwei ^a   Azmi, Asfar S ^a   Miele, Lucio ^b   Sarkar, Fazlul H ^a  

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

^b UNIVERSITY OF MISSISSIPPI   (United States)

Author keywords

Cancer therapy; Drug resistance; Natural agents; Notch; Pancreatic cancer; Review; Signal pathway; Stem cells

Indexed keywords

CURCUMIN; GAMMA SECRETASE INHIBITOR; GENISTEIN; MICRORNA; NOTCH RECEPTOR; QUERCETIN; SORAFENIB; SULFORAPHANE;

ANGIOGENESIS; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; CANCER STEM CELL; CANCER THERAPY; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOTOXICITY; DRUG BIOAVAILABILITY; DRUG POTENTIATION; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; PANCREAS CANCER; PANCREAS CANCER STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR GENE;

ANTINEOPLASTIC AGENTS; HUMANS; NEOPLASTIC STEM CELLS; PANCREATIC NEOPLASMS; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION;

EID: 79956088981     PISSN: 02507005     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (86)

1. Jemal A, Siegel R, Xu J and Ward E: Cancer statistics, 2010. CA Cancer J Clin 60: 277-300, 2010.
2. Stan SD, Singh SV and Brand RE: Chemoprevention strategies for pancreatic cancer. Nat Rev Gastroenterol Hepatol 7: 347-356, 2010.
3. Stathis A and Moore MJ: Advanced pancreatic carcinoma: current treatment and future challenges. Nat Rev Clin Oncol 7: 163-172, 2010.
4. Grover S and Syngal S: Hereditary pancreatic cancer. Gastroenterology 139: 1076-1080, 1080, 2010.
5. Hidalgo M: Pancreatic cancer. N Engl J Med 362: 1605-1617, 2010.
6. Wong HH and Lemoine NR: Biological approaches to therapy of pancreatic cancer. Pancreatology 8: 431-461, 2008.
7. Wong HH and Lemoine NR: Pancreatic cancer: molecular pathogenesis and new therapeutic targets. Nat Rev Gastroenterol Hepatol 6: 412-422, 2009.
8. Ristorcelli E and Lombardo D: Targeting Notch signaling in pancreatic cancer. Expert Opin Ther Targets 14: 541-552, 2010.
9. Miele L and Osborne B: Arbiter of differentiation and death: Notch signaling meets apoptosis. J Cell Physiol 181: 393-409, 1999. (Pubitemid 29513408)
10. Miele L: Notch signaling. Clin Cancer Res 12: 1074-1079, 2006.
11. Fortini ME: Notch signaling: the core pathway and its posttranslational regulation. Dev Cell 16: 633-647, 2009.
12. Miele L, Miao H and Nickoloff BJ: Notch signaling as a novel cancer therapeutic target. Curr Cancer Drug Targets 6: 313-323, 2006. (Pubitemid 43961866)
13. Rizzo P, Osipo C, Foreman K, Golde T, Osborne B and Miele L: Rational targeting of Notch signaling in cancer. Oncogene 27: 5124-5131, 2008.
14. Wang Z, Li Y, Banerjee S and Sarkar FH: Exploitation of the Notch signaling pathway as a novel target for cancer therapy. Anticancer Res 28: 3621-3630, 2008.
15. Dotto GP: Notch tumor suppressor function. Oncogene 27: 5115-5123, 2008.
16. Mysliwiec P and Boucher MJ: Targeting Notch signaling in pancreatic cancer patients - rationale for new therapy. Adv Med Sci 54: 1-7, 2009.
17. Wang Z, Banerjee S, Li Y, Rahman KM, Zhang Y and 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 66: 2778-2784, 2006.
18. Wang Z, Zhang Y, Li Y, Banerjee S, Liao J and Sarkar FH: Down-regulation of Notch-1 contributes to cell growth inhibition and apoptosis in pancreatic cancer cells. Mol Cancer Ther 5: 483-493, 2006.
19. Wang Z, Li Y, Banerjee S, Kong D, Ahmad A, Nogueira V, Hay N and Sarkar FH: Down-regulation of Notch-1 and Jagged-1 inhibits prostate cancer cell growth, migration and invasion, and induces apoptosis via inactivation of Akt, mTOR, and NF-kappaB signaling pathways. J Cell Biochem 109: 726-736, 2010.
20. Yin L, Velazquez OC and Liu ZJ: Notch signaling: emerging molecular targets for cancer therapy. Biochem Pharmacol 80: 690-701, 2010.
21. Buchler P, Gazdhar A, Schubert M, Giese N, Reber HA, Hines OJ, Giese T, Ceyhan GO, Muller M, Buchler MW and Friess H: The Notch signaling pathway is related to neurovascular progression of pancreatic cancer. Ann Surg 242: 791-800, 2005.
22. Miyamoto Y, Maitra A, Ghosh B, Zechner U, Argani P, Iacobuzio-Donahue CA, Sriuranpong V, Iso T, Meszoely IM, Wolfe MS, Hruban RH, Ball DW, Schmid RM and Leach SD: Notch mediates TGF alpha-induced changes in epithelial differentiation during pancreatic tumorigenesis. Cancer Cell 3: 565-576, 2003. (Pubitemid 36808651)
23. De La OJ, Emerson LL, Goodman JL, Froebe SC, Illum BE, Curtis AB and Murtaugh LC: Notch and Kras reprogram pancreatic acinar cells to ductal intraepithelial neoplasia. Proc Natl Acad Sci USA 105: 18907-18912, 2008.
24. De La OJ and Murtaugh LC: Notch and Kras in pancreatic cancer: at the crossroads of mutation, differentiation and signaling. Cell Cycle 8: 1860-1864, 2009.
25. Kimura K, Satoh K, Kanno A, Hamada S, Hirota M, Endoh M, Masamune A and Shimosegawa T: Activation of Notch signaling in tumorigenesis of experimental pancreatic cancer induced by dimethylbenzanthracene in mice. Cancer Sci 98: 155-162, 2007. (Pubitemid 44941866)
26. Mullendore ME, Koorstra JB, Li YM, Offerhaus GJ, Fan X, Henderson CM, Matsui W, Eberhart CG, Maitra A and Feldmann G: Ligand-dependent Notch signaling is involved in tumor initiation and tumor maintenance in pancreatic cancer. Clin Cancer Res 15: 2291-2301, 2009.
27. Sawey ET, Johnson JA and Crawford HC: Matrix metalloproteinase 7 controls pancreatic acinar cell transdifferentiation by activating the Notch signaling pathway. Proc Natl Acad Sci USA 104: 19327-19332, 2007.
28. Hanlon L, Avila JL, Demarest RM, Troutman S, Allen M, Ratti F, Rustgi AK, Stanger BZ, Radtke F, Adsay V, Long F, Capobianco AJ and Kissil JL: Notch1 functions as a tumor suppressor in a model of K-ras-induced pancreatic ductal adenocarcinoma. Cancer Res 70: 4280-4286, 2010.
29. Yeh JJ and Der CJ: Targeting signal transduction in pancreatic cancer treatment. Expert Opin Ther Targets 11: 673-694, 2007. (Pubitemid 46730082)
30. Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW, Guba M, Bruns CJ and Heeschen C: Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 1: 313-323, 2007. (Pubitemid 47355323)
31. Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, Adsay V, Wicha M, Clarke MF and Simeone DM: Identification of pancreatic cancer stem cells. Cancer Res 67: 1030-1037, 2007.
32. Bomken S, Fiser K, Heidenreich O and Vormoor J: Understanding the cancer stem cell. Br J Cancer 103: 439-445, 2010.
33. Eramo A, Haas TL and De MR: Lung cancer stem cells: tools and targets to fight lung cancer. Oncogene 29: 4625-4635, 2010.
34. O'Brien CA, Kreso A and Jamieson CH: Cancer stem cells and self-renewal. Clin Cancer Res 16: 3113-3120, 2010.
35. Burness ML and Sipkins DA: The stem cell niche in health and malignancy. Semin Cancer Biol 20: 107-115, 2010.
36. Liu S and Wicha MS: Targeting breast cancer stem cells. J Clin Oncol 28: 4006-4012, 2010.
37. Sell S: On the stem cell origin of cancer. Am J Pathol 176: 2584-494, 2010.
38. Todaro M, Francipane MG, Medema JP and Stassi G: Colon cancer stem cells: promise of targeted therapy. Gastroenterology 138: 2151-2162, 2010.
39. Olempska M, Eisenach PA, Ammerpohl O, Ungefroren H, Fandrich F and Kalthoff H: Detection of tumor stem cell markers in pancreatic carcinoma cell lines. Hepatobiliary Pancreat Dis Int 6: 92-97, 2007. (Pubitemid 46243168)
40. Rasheed Z, Wang Q and Matsui W: Isolation of stem cells from human pancreatic cancer xenografts. J Vis Exp 43: 2169, 2010.
41. Rasheed ZA, Yang J, Wang Q, Kowalski J, Freed I, Murter C, Hong SM, Koorstra JB, Rajeshkumar NV, He X, Goggins M, Iacobuzio-Donahue C, Berman DM, Laheru D, Jimeno A, Hidalgo M, Maitra A and Matsui W: Prognostic significance of tumorigenic cells with mesenchymal features in pancreatic adenocarcinoma. J Natl Cancer Inst 102: 340-351, 2010.
42. Phillips TM, Kim K, Vlashi E, McBride WH and Pajonk F: Effects of recombinant erythropoietin on breast cancer-initiating cells. Neoplasia 9: 1122-1129, 2007. (Pubitemid 350255350)
43. Farnie G, Clarke RB, Spence K, Pinnock N, Brennan K, Anderson NG and Bundred NJ: Novel cell culture technique for primary ductal carcinoma in situ: role of Notch and epidermal growth factor receptor signaling pathways. J Natl Cancer Inst 99: 616-627, 2007. (Pubitemid 47073543)
44. Hong SP, Wen J, Bang S, Park S and Song SY: CD44-positive cells are responsible for gemcitabine resistance in pancreatic cancer cells. Int J Cancer 125: 2323-2331, 2009.
45. Wang YH, Li F, Luo B, Wang XH, Sun HC, Liu S, Cui YQ and Xu XX: A side population of cells from a human pancreatic carcinoma cell line harbors cancer stem cell characteristics. Neoplasma 56: 371-378, 2009.
46. Ji Q, Hao X, Zhang M, Tang W, Yang M, Li L, Xiang D, Desano JT, Bommer GT, Fan D, Fearon ER, Lawrence TS and Xu L: MicroRNA miR-34 inhibits human pancreatic cancer tumor-initiating cells. PLoS One 4: e6816, 2009.
47. Wang Z, Li Y, Ahmad A, Banerjee S, Azmi AS, Kong D and Sarkar FH: Pancreatic cancer: understanding and overcoming chemoresistance. Nat Rev Gastroenterol Hepatol 8: 27-33, 2011.
48. Kong D, Banerjee S, Ahmad A, Li Y, Wang Z, Sethi S and Sarkar FH: Epithelial-to-mesenchymal transition is mechanistically linked with stem cell signatures in prostate cancer cells. PLoS One 5: e12445, 2010.
49. Li Y, Vandenboom TG, Kong D, Wang Z, Ali S, Philip PA and Sarkar FH: Up-regulation of miR-200 and let-7 by natural agents leads to the reversal of epithelial-to-mesenchymal transition in gemcitabine-resistant pancreatic cancer cells. Cancer Res 69: 6704-6712, 2009.
50. Brabletz S, Bajdak K, Meidhof S, Burk U, Niedermann G, Firat E, Wellner U, Dimmler A, Faller G, Schubert J and Brabletz T: The ZEB1/miR-200 feedback loop controls Notch signalling in cancer cells. EMBO J 30: 770-782, 2011.
51. Thiery JP, Acloque H, Huang RY and Nieto MA: Epithelial-mesenchymal transitions in development and disease. Cell 139: 871-890, 2009.
52. Thiery JP and Sleeman JP: Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 7: 131-142, 2006. (Pubitemid 43278296)
53. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, Campbell LL, Polyak K, Brisken C, Yang J and Weinberg RA: The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133: 704-715, 2008. (Pubitemid 351636299)
54. Wellner U, Schubert J, Burk UC, Schmalhofer O, Zhu F, Sonntag A, Waldvogel B, Vannier C, Darling D, zur HA, Brunton VG, Morton J, Sansom O, Schuler J, Stemmler MP, Herzberger C, Hopt U, Keck T, Brabletz S and Brabletz T: The EMT-activator ZEB1 promotes tumorigenicity by repressing sternness-inhibiting microRNAs. Nat Cell Biol 11: 1487-1495, 2009.
55. Shah AN, Summy JM, Zhang J, Park SI, Parikh NU and Gallick GE: Development and characterization of gemcitabine-resistant pancreatic tumor cells. Ann Surg Oncol 14: 3629-3637, 2007. (Pubitemid 350160137)
56. Wang Z, Li Y, Kong D, Banerjee S, Ahmad A, Azmi AS, Ali S, Abbruzzese JL, Gallick GE and Sarkar FH: Acquisition of epithelial-mesenchymal transition phenotype of gemcitabine-resistant pancreatic cancer cells is linked with activation of the notch signaling pathway. Cancer Res 69: 2400-2407, 2009.
57. Mueller MT, Hermann PC, Witthauer J, Rubio-Viqueira B, Leicht SF, Huber S, Ellwart IW, Mustafa M, Bartenstein P, D'Haese JG, Schoenberg MH, Berger F, Jauch KW, Hidalgo M and Heeschen C: Combined targeted treatment to eliminate tumorigenic cancer stem cells in human pancreatic cancer. Gastroenterology 137: 1102-1113, 2009.
58. Meng RD, Shelton CC, Li YM, Qin LX, Notterman D, Paty PB and Schwartz GK: γ-Secretase inhibitors abrogate oxaliplatin-induced activation of the Notch-1 signaling pathway in colon cancer cells resulting in enhanced chemosensitivity. Cancer Res 69: 573-582, 2009.
59. Tammam J, Ware C, Efferson C, O'Neil J, Rao S, Qu X, Gorenstein J, Angagaw M, Kim H, Kenific C, Kunii K, Leach KJ, Nikov G, Zhao J, Dai X, Hardwick J, Scott M, Winter C, Bristow L, Elbi C, Reilly JF, Look T, Draetta G, Van der PL, Kohl NE, Strack PR and Majumder PK: Down-regulation of the Notch pathway mediated by a gamma-secretase inhibitor induces antitumour effects in mouse models of T-cell leukaemia. Br J Pharmacol 158: 1183-1195, 2009.
60. Watters JW, Cheng C, Majumder PK, Wang R, Yalavarthi S, Meeske C, Kong L, Sun W, Lin J, Heyer J, Ware C, Winter C, Reilly JF, Demuth T, Clark S, Chiu MI, Robinson MO, Kohl N and Kannan K: De novo discovery of a gamma-secretase inhibitor response signature using a novel in vivo breast tumor model. Cancer Res 69: 8949-8957, 2009.
61. Fan X, Khaki L, Zhu TS, Soules ME, Talsma CE, Gul N, Koh C, Zhang J, Li YM, Maciaczyk J, Nikkhah G, Dimeco F, Piccirillo S, Vescovi AL and Eberhart CG: NOTCH pathway blockade depletes CD133-positive glioblastoma cells and inhibits growth of tumor neurospheres and xenografts. Stem Cells 28: 5-16, 2010.
62. Efferson CL, Winkelmann CT, Ware C, Sullivan T, Giampaoli S, Tammam J, Patel S, Mesiti G, Reilly JF, Gibson RE, Buser C, Yeatman T, Coppola D, Winter C, Clark EA, Draetta GF, Strack PR and Majumder PK: Down-regulation of Notch pathway by a gamma-secretase inhibitor attenuates AKT/mammalian target of rapamycin signaling and glucose uptake in an ERBB2 transgenic breast cancer model. Cancer Res 70: 2476-2484, 2010.
63. Gilbert CA, Daou MC, Moser RP and Ross AH: Gamma-secretase inhibitors enhance temozolomide treatment of human gliomas by inhibiting neurosphere repopulation and xenograft recurrence. Cancer Res 70: 6870-6879, 2010.
64. Plentz R, Park JS, Rhim AD, Abravanel D, Hezel AF, Sharma SV, Gurumurthy S, Deshpande V, Kenific C, Settleman J, Majumder PK, Stanger BZ and Bardeesy N: Inhibition of gamma-secretase activity inhibits tumor progression in a mouse model of pancreatic ductal adenocarcinoma. Gastroenterology 136: 1741-1749, 2009.
65. Fan X, Matsui W, Khaki L, Stearns D, Chun J, Li YM and Eberhart CG: Notch pathway inhibition depletes stem-like cells and blocks engraftment in embryonal brain tumors. Cancer Res 66: 7445-7452, 2006. (Pubitemid 44289197)
66. Ulasov IV, Nandi S, Dey M, Sonabend AM and Lesniak MS: Inhibition of Sonic hedgehog and Notch pathways enhances sensitivity of CD133(+) glioma stem cells to temozolomide therapy. Mol Med 17: 103-112, 2011.
67. Pannuti A, Foreman K, Rizzo P, Osipo C, Golde T, Osborne B and Miele L: Targeting Notch to target cancer stem cells. Clin Cancer Res 16: 3141-3152, 2010.
68. Li Y, Zhang T, Korkaya H, Liu S, Lee HF, Newman B, Yu Y, Clouthier SG, Schwartz SJ, Wicha MS and Sun D: Sulforaphane, a dietary component of broccoli/broccoli sprouts, inhibits breast cancer stem cells. Clin Cancer Res 16: 2580-2590, 2010.
69. Kallifatidis G, Rausch V, Baumann B, Apel A, Beckermann BM, Groth A, Mattern J, Li Z, Kolb A, Moldenhauer G, Altevogt P, Wirth T, Werner J, Schemmer P, Buchler MW, Salnikov AV and Herr I: Sulforaphane targets pancreatic tumour-initiating cells by NF-kappaB-induced antiapoptotic signalling. Gut 58: 949-963, 2009.
70. Rausch V, Liu L, Kallifatidis G, Baumann B, Mattern J, Gladkich J, Wirth T, Schemmer P, Buchler MW, Zoller M, Salnikov AV and Herr I: Synergistic activity of sorafenib and sulforaphane abolishes pancreatic cancer stem cell characteristics. Cancer Res 70: 5004-5013, 2010.
71. Kallifatidis G, Labsch S, Rausch V, Mattern J, Gladkich J, Moldenhauer G, Buchler MW, Salnikov AV and Herr I: Sulforaphane increases drug-mediated cytotoxicity toward cancer stem-like cells of pancreas and prostate. Mol Ther 19: 188-195, 2011.
72. Kawahara T, Kawaguchi-Ihara N, Okuhashi Y, Itoh M, Nara N and Tohda S: Cyclopamine and quercetin suppress the growth of leukemia and lymphoma cells. Anticancer Res 29: 4629-4632, 2009.
73. Tang SN, Singh C, Nall D, Meeker D, Shankar S and Srivastava RK: The dietary bioflavonoid quercetin synergizes with epigallocathechin gallate (EGCG) to inhibit prostate cancer stem cell characteristics, invasion, migration and epithelial-mesenchymal transition. J Mol Signal 5: 14, 2010.
74. Zhou W, Kallifatidis G, Baumann B, Rausch V, Mattern J, Gladkich J, Giese N, Moldenhauer G, Wirth T, Buchler MW, Salnikov AV and Herr I: Dietary polyphenol quercetin targets pancreatic cancer stem cells. Int J Oncol 37: 551-561, 2010.
75. Aggarwal BB: Targeting inflammation-induced obesity and metabolic diseases by curcumin and other nutraceuticals. Annu Rev Nutr 30: 173-199, 2010.
76. Wang Z, Zhang Y, Banerjee S, Li Y and 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 106: 2503-2513, 2006. (Pubitemid 43787677)
77. Ali S, Ahmad A, Banerjee S, Padhye S, Dominiak K, Schaffert JM, Wang Z, Philip PA and Sarkar FH: Gemcitabine sensitivity can be induced in pancreatic cancer cells through modulation of miR-200 and miR-21 expression by curcumin or its analogue CDF. Cancer Res 70: 3606-3617, 2010.
78. Fong D, Yeh A, Naftalovich R, Choi TH and Chan MM: Curcumin inhibits the side population (SP) phenotype of the rat C6 glioma cell line: towards targeting of cancer stem cells with phytochemicals. Cancer Lett 293: 65-72, 2010.
79. Yu Y, Kanwar SS, Patel BB, Nautiyal J, Sarkar FH and Majumdar AP: Elimination of colon cancer stem-Like cells by the combination of curcumin and FOLFOX. Transl Oncol 2: 321-328, 2009.
80. Kakarala M, Brenner DE, Korkaya H, Cheng C, Tazi K, Ginestier C, Liu S, Dontu G and Wicha MS: Targeting breast stem cells with the cancer preventive compounds curcumin and pipeline. Breast Cancer Res Treat 122: 777-785, 2010.
81. Bao B and Sarkar F: Anti-tumor activity of a novel compound-CDF is mediated by regulating miR-21, miR-200, PTEN, and Wnt/β-catenin signaling in pancreatic cancer. PLoS One 6 (3): e17850, 2011.
82. Sarkar FH, Li Y, Wang Z and Kong D: The role of nutraceuticals in the regulation of Wnt and Hedgehog signaling in cancer. Cancer Metastasis Rev 29: 383-394, 2010.
83. Wang Z, Zhang Y, Banerjee S, Li Y and Sarkar FH: Inhibition of nuclear factor kappab activity by genistein is mediated via Notch-1 signaling pathway in pancreatic cancer cells. Int J Cancer 118: 1930-1936, 2006.
84. Slusarz A, Shenouda NS, Sakla MS, Drenkhahn SK, Narula AS, MacDonald RS, Besch-Williford CL and Lubahn DB: Common botanical compounds inhibit the hedgehog signaling pathway in prostate cancer. Cancer Res 70: 3382-3390, 2010.
85. Regenbrecht CR, Jung M, Lehrach H and Adjaye J: The molecular basis of genistein-induced mitotic arrest and exit of self-renewal in embryonal carcinoma and primary cancer cell lines. BMC Med Genomics 1: 49, 2008.
86. Rao A, Woodruff RD, Wade WN, Kute TE and Cramer SD: Genistein and vitamin D synergistically inhibit human prostatic epithelial cell growth. J Nutr 132: 3191-3194, 2002.