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Notch Inhibitor: a Promising Carcinoma Radiosensitizer

  • Yu, Shu-Dong (Department of Otolaryngology, Qianfoshan Hospital Affiliated to Shandong University) ;
  • Liu, Fen-Ye (Department of Traditional Chinese Medicine, Shandong Provincial Hospital Affiliated to Shandong University) ;
  • Wang, Qi-Rong (Department of Otolaryngology, Qianfoshan Hospital Affiliated to Shandong University)
  • 발행 : 2012.11.30

초록

Radiotherapy is an important part of modern cancer management for many malignancies, and enhancing the radiosensitivity of tumor cells is critical for effective cancer therapies. The Notch signaling pathway plays a key role in regulation of numerous fundamental cellular processes. Further, there is accumulating evidence that dysregulated Notch activity is involved in the genesis of many human cancers. As such, Notch inhibitors are attractive therapeutic agents, although as for other anticancer agents, they exhibit significant and potential side effects. Thus, Notch inhibitors may be best used in combination with other agents or therapy. Herein, we describe evidence supporting the use of Notch inhibitors as novel and potent radiosensitizers in cancer therapy.

키워드

참고문헌

  1. Allen TD, Rodriguez EM, Jones KD, Bishop JM (2011). Activated Notch1 induces lung adenomas in mice and cooperates with Myc in the generation of lung adenocarcinoma. Cancer Res. 71, 6010-8. https://doi.org/10.1158/0008-5472.CAN-11-0595
  2. Artavanis-Tsakonas S, Rand MD, Lake RJ (1999). Notch signaling: cell fate control and signal integration in development. Science, 284, 770-6. https://doi.org/10.1126/science.284.5415.770
  3. Bao S, Wu Q, McLendon RE, et al (2006). Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature, 444, 756-60. https://doi.org/10.1038/nature05236
  4. Bedogni B, Warneke JA, Nickoloff BJ, Giaccia AJ, Powell MB (2008). Notch1 is an effector of Akt and hypoxia in melanoma development. J Clin Invest, 118, 3660-70. https://doi.org/10.1172/JCI36157
  5. Bischoff P, Altmeyer A, Dumont F (2009). Radiosensitising agents for the radiotherapy of cancer: advances in traditional and hypoxia targeted radiosensitisers. Expert Opin Ther Pat, 19, 643-62. https://doi.org/10.1517/13543770902824172
  6. Brou C, Logeat F, Gupta N, et al (2000). A novel proteolytic cleavage involved in Notch signaling: the role of the disintegrin-metalloprotease TACE. Mol Cell, 5, 207-16. https://doi.org/10.1016/S1097-2765(00)80417-7
  7. Canman CE, Lim DS, Cimprich KA, et al (1998). Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science, 281, 1677-9. https://doi.org/10.1126/science.281.5383.1677
  8. Chen F, Pisklakova A, Li M, et al (2011). Gamma-secretase inhibitor enhances the cytotoxic effect of bortezomib in multiple myeloma. Cell Oncol (Dordr), 34, 545-51. https://doi.org/10.1007/s13402-011-0060-6
  9. Chen SM, Liu JP, Zhou JX, et al (2011). Suppression of the notch signaling pathway by gamma-secretase inhibitor GSI inhibits human nasopharyngeal carcinoma cell proliferation. Cancer Lett, 306, 76-84. https://doi.org/10.1016/j.canlet.2011.02.034
  10. Chen Y, Li D, Liu H, et al (2011). Notch-1 signaling facilitates survivin expression in human non-small cell lung cancer cells. Cancer Biol Ther, 11, 14-21. https://doi.org/10.4161/cbt.11.1.13730
  11. Chen YW, Chen KH, Huang PI, et al (2010). Cucurbitacin I suppressed stem-like property and enhanced radiationinduced apoptosis in head and neck squamous carcinoma--derived CD44(+)ALDH1(+) cells. Mol Cancer Ther, 9, 2879-92. https://doi.org/10.1158/1535-7163.MCT-10-0504
  12. Cohen-Jonathan E, Toulas C, Ader I, et al (1999). The farnesyltransferase inhibitor FTI-277 suppresses the 24-kDa FGF2-induced radioresistance in HeLa cells expressing wild-type RAS. Radiat Res, 152, 404-11. https://doi.org/10.2307/3580225
  13. Cook N, Frese KK, Bapiro TE, et al (2012). Gamma secretase inhibition promotes hypoxic necrosis in mouse pancreatic ductal adenocarcinoma. J Exp Med, 209, 437-44. https://doi.org/10.1084/jem.20111923
  14. Cooper JS, Ang KK (2005). Concomitant chemotherapy and radiation therapy certainly improves local control. Int J Radiat Oncol Biol Phys, 61, 7-9. https://doi.org/10.1016/j.ijrobp.2004.09.034
  15. Czito BG, Willett CG, Bendell JC, et al (2006). Increased toxicity with gefitinib, capecitabine, and radiation therapy in pancreatic and rectal cancer: phase I trial results. J Clin Oncol, 24, 656-62. https://doi.org/10.1200/JCO.2005.04.1749
  16. Dai L, He J, Liu Y, et al (2011). Dose-dependent proteomic analysis of glioblastoma cancer stem cells upon treatment with gamma-secretase inhibitor. Proteomics, 11, 4529-40. https://doi.org/10.1002/pmic.201000730
  17. Debeb BG, Cohen EN, Boley K, et al (2012). Pre-clinical studies of Notch signaling inhibitor RO4929097 in inflammatory breast cancer cells. Breast Cancer Res Treat, 134, 495-510. https://doi.org/10.1007/s10549-012-2075-8
  18. Deorukhkar A, Krishnan S (2010). Targeting inflammatory pathways for tumor radiosensitization. Biochem. Pharmacol, 80, 1904-14. https://doi.org/10.1016/j.bcp.2010.06.039
  19. Dextraze ME, Cecchini S, Bergeron F, et al (2009). Reaching for the other side: generating sequence-dependent interstrand cross-links with 5-bromodeoxyuridine and gamma-rays. Biochemistry, 48, 2005-11. https://doi.org/10.1021/bi801684t
  20. Diehn M, Cho RW, Lobo NA, et al (2009). Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature, 458, 780-3. https://doi.org/10.1038/nature07733
  21. Dotto GP (2008). Notch tumor suppressor function. Oncogene, 27, 5115-23. https://doi.org/10.1038/onc.2008.225
  22. Dufraine J, Funahashi Y, Kitajewski J (2008). Notch signaling regulates tumor angiogenesis by diverse mechanisms. Oncogene, 27, 5132-37. https://doi.org/10.1038/onc.2008.227
  23. Efimova EV, Liang H, Pitroda SP, et al (2009). Radioresistance of Stat1 over-expressing tumour cells is associated with suppressed apoptotic response to cytotoxic agents and increased IL6-IL8 signalling. Int J Radiat Biol, 85, 421-31. https://doi.org/10.1080/09553000902838566
  24. Ellisen LW, Bird J, West DC, et al (1991). TAN-1, the human homolog of the Drosophila notch gene, is broken by chromosomal translocations in T lymphoblastic neoplasms. Cell, 66, 649-61. https://doi.org/10.1016/0092-8674(91)90111-B
  25. Fan X, Khaki L, Zhu TS, et al (2010). NOTCH pathway blockade depletes CD133-positive glioblastoma cells and inhibits growth of tumor neurospheres and xenografts. Stem Cells, 28, 5-16.
  26. Garber K (2007). Notch emerges as new cancer drug target. J. Natl. Cancer Inst, 99, 1284-85. https://doi.org/10.1093/jnci/djm148
  27. Gil J, Stembalska A, Pesz KA, Sasiadek MM. (2008). Cancer stem cells: the theory and perspectives in cancer therapy. J Appl Genet, 49, 193-9. https://doi.org/10.1007/BF03195612
  28. Gogineni VR, Nalla AK, Gupta R, et al (2011). Chk2-mediated G2/M cell cycle arrest maintains radiation resistance in malignant meningioma cells. Cancer Lett, 313, 64-75. https://doi.org/10.1016/j.canlet.2011.08.022
  29. Guo S, Liu M, Gonzalez-Perez RR (2011). Role of Notch and its oncogenic signaling crosstalk in breast cancer. Biochim Biophys Acta, 1815, 197-213.
  30. Hajdu M, Kopper L, Sebestyen A (2010). Notch-regulation upon Dll4-stimulation of TGFb-induced apoptosis and gene expression in human B-cell non-Hodgkin lymphomas. Scand J Immunol, 71, 29-37. https://doi.org/10.1111/j.1365-3083.2009.02346.x
  31. Harrison H, Farnie G, Howell SJ, et al (2010). Regulation of breast cancer stem cell activity by signaling through the Notch4 receptor. Cancer Res, 70, 709-18. https://doi.org/10.1158/0008-5472.CAN-09-1681
  32. He Z, Subramaniam D, Ramalingam S, et al (2011). Honokiol radiosensitizes colorectal cancer cells: enhanced activity in cells with mismatch repair defects. Am J Physiol Gastrointest Liver Physiol, 301, G929-37. https://doi.org/10.1152/ajpgi.00159.2011
  33. Heidelberger C, Griesbach L, Cruz O, Schnitzer RJ, Grunberg E. (1958). Effects of 5-fluorouridine and 5-fluoro-2'-deoxyuridine on transplanted tumors. Proc Soc Exp Biol Med, 97, 470-5. https://doi.org/10.3181/00379727-97-23777
  34. Hellstrom M, Phng LK, Hofmann JJ, et al (2007). Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature, 445, 776-80. https://doi.org/10.1038/nature05571
  35. Hirose H, Ishii H, Mimori K, et al (2010). Notch pathway as candidate therapeutic target in Her2/Neu/ErbB2 receptornegative breast tumors. Oncol Rep, 23, 35-43.
  36. Hosoki A, Yonekura S, Zhao QL, et al (2012). Mitochondriatargeted superoxide dismutase (SOD2) regulates radiation resistance and radiation stress response in HeLa cells. J Radiat Res, 53, 58-71. https://doi.org/10.1269/jrr.11034
  37. Hovinga KE, Shimizu F, Wang R, et al (2010). Inhibition of notch signaling in glioblastoma targets cancer stem cells via an endothelial cell intermediate. Stem Cells, 28, 1019-29. https://doi.org/10.1002/stem.429
  38. Iliopoulos D, Hirsch HA, Wang G, Struhl K (2011). Inducible formation of breast cancer stem cells and their dynamic equilibrium with non-stem cancer cells via IL6 secretion. Proc Natl Acad Sci U S A, 108, 1397-402. https://doi.org/10.1073/pnas.1018898108
  39. Jehn BM, Bielke W, Pear WS, Osborne BA (1999). Cutting edge: protective effects of notch-1 on TCR-induced apoptosis. J Immunol, 162, 635-8.
  40. Jiang L, Wu J, Chen Q, et al (2011). Notch1 expression is upregulated in glioma and is associated with tumor progression. J Clin Neurosci, 18, 387-90. https://doi.org/10.1016/j.jocn.2010.07.131
  41. Kato Y, Yashiro M, Fuyuhiro Y, et al (2011). Effects of acute and chronic hypoxia on the radiosensitivity of gastric and esophageal cancer cells. Anticancer Res, 31, 3369-75.
  42. Keysar SB, Jimeno A (2010). More than markers: biological significance of cancer stem cell-defining molecules. Mol Cancer Ther, 9, 2450-57. https://doi.org/10.1158/1535-7163.MCT-10-0530
  43. Kotowski U, Heiduschka G, Brunner M, et al (2011). Radiosensitization of head and neck cancer cells by the phytochemical agent sulforaphane. Strahlenther Onkol, 187, 575-80. https://doi.org/10.1007/s00066-011-2218-6
  44. Krop I, Demuth T, Guthrie T, et al (2012). Phase I Pharmacologic and Pharmacodynamic Study of the Gamma Secretase (Notch) Inhibitor MK-0752 in Adult Patients With Advanced Solid Tumors. J Clin Oncol, 30, 2307-13 . https://doi.org/10.1200/JCO.2011.39.1540
  45. Kuhnert F, Kirshner JR, Thurston G (2011). Dll4-Notch signaling as a therapeutic target in tumor angiogenesis. Vasc Cell, 3, 20. https://doi.org/10.1186/2045-824X-3-20
  46. Kurrey NK, Jalgaonkar SP, Joglekar AV, et al (2009). Snail and slug mediate radioresistance and chemoresistance by antagonizing p53-mediated apoptosis and acquiring a stem-like phenotype in ovarian cancer cells. Stem Cells, 27, 2059-68. https://doi.org/10.1002/stem.154
  47. Kvols LK (2005). Radiation sensitizers: a selective review of molecules targeting DNA and non-DNA targets. J Nucl Med, 46, S187-90.
  48. Lagadec C, Vlashi E, Della DL, Dekmezian C, Pajonk F (2012). Radiation-induced reprogramming of breast cancer cells. Stem Cells, 30, 833-44. https://doi.org/10.1002/stem.1058
  49. Lai EC (2004). Notch signaling: control of cell communication and cell fate. Development, 131, 965-73. https://doi.org/10.1242/dev.01074
  50. Lee SF, Srinivasan B, Sephton CF, et al (2011). Gammasecretase-regulated proteolysis of the Notch receptor by mitochondrial intermediate peptidase. J Biol Chem, 286, 27447-53. https://doi.org/10.1074/jbc.M111.243154
  51. Li C, Zhang Y, Lu Y, et al (2011). Evidence of the cross talk between Wnt and Notch signaling pathways in non-smallcell lung cancer (NSCLC): Notch3-siRNA weakens the effect of LiCl on the cell cycle of NSCLC cell lines. J Cancer Res Clin Oncol, 137, 771-8. https://doi.org/10.1007/s00432-010-0934-4
  52. Lin H, Xiong W, Zhang X, et al (2011). Notch-1 activationdependent p53 restoration contributes to resveratrol-induced apoptosis in glioblastoma cells. Oncol Rep, 26, 925-30.
  53. Lin J, Zhang XM, Yang JC, Ye YB, Luo SQ (2010). Association of high levels of Jagged-1 and Notch-1 expression with poor prognosis in head and neck cancer. Arch Med Res, 41, 519-29. https://doi.org/10.1016/j.arcmed.2010.10.006
  54. Lin JT, Chen MK, Yeh KT, et al (2010). Association of high levels of Jagged-1 and Notch-1 expression with poor prognosis in head and neck cancer. Ann Surg Oncol, 17, 2976-83. https://doi.org/10.1245/s10434-010-1118-9
  55. Lin L, Fuchs J, Li C, et al (2011). STAT3 signaling pathway is necessary for cell survival and tumorsphere forming capacity in ALDH/CD133 stem cell-like human colon cancer cells. Biochem Biophys Res Commun, 416, 246-51. https://doi.org/10.1016/j.bbrc.2011.10.112
  56. Lino MM, Merlo A, Boulay JL (2010). Notch signaling in glioblastoma: a developmental drug target. BMC Med, 8, 72. https://doi.org/10.1186/1741-7015-8-72
  57. Liu SK, Bham SA, Fokas E, et al (2011). Delta-like ligand 4-notch blockade and tumor radiation response. J Natl Cancer Inst, 103, 1778-98. https://doi.org/10.1093/jnci/djr419
  58. Maliekal TT, Bajaj J, Giri V, Subramanyam D, Krishna S (2008). The role of Notch signaling in human cervical cancer: implications for solid tumors. Oncogene, 27, 5110-14. https://doi.org/10.1038/onc.2008.224
  59. McAllister SS, Weinberg RA (2010). Tumor-host interactions: a far-reaching relationship. J Clin Oncol, 28, 4022-8. https://doi.org/10.1200/JCO.2010.28.4257
  60. Mihatsch J, Toulany M, Bareiss PM, et al (2011). Selection of radioresistant tumor cells and presence of ALDH1 activity in vitro. Radiother Oncol, 99, 300-6. https://doi.org/10.1016/j.radonc.2011.06.003
  61. Mori M, Miyamoto T, Yakushiji H, et al (2012). Effects of N-[N-(3, 5-difluorophenacetyl-L: -alanyl)]-S-phenylglycine t-butyl ester (DAPT) on cell proliferation and apoptosis in Ishikawa endometrial cancer cells. Hum Cell, 25, 9-15. https://doi.org/10.1007/s13577-011-0038-8
  62. Morrison R, Schleicher SM, Sun Y, et al (2011). Targeting the mechanisms of resistance to chemotherapy and radiotherapy with the cancer stem cell hypothesis. J Oncol, 2011, 941876.
  63. Nam Y, Aster JC, Blacklow SC (2002). Notch signaling as a therapeutic target. Curr Opin Chem Biol, 6, 501-9. https://doi.org/10.1016/S1367-5931(02)00346-0
  64. Nickoloff BJ, Osborne BA, Miele L (2003). Notch signaling as a therapeutic target in cancer: a new approach to the development of cell fate modifying agents. Oncogene, 22, 6598-608. https://doi.org/10.1038/sj.onc.1206758
  65. Noguera-Troise I, Daly C, Papadopoulos NJ, et al (2006). Blockade of Dll4 inhibits tumour growth by promoting nonproductive angiogenesis. Nature, 444, 1032-7. https://doi.org/10.1038/nature05355
  66. Nygren P, Glimelius B (2001). The Swedish Council on Technology Assessment in Health Care (SBU) report on Cancer Chemotherapy--Project objectives, the working process, key definitions and general aspects on cancer trial methodology and interpretation. Acta Oncol, 40, 155-65. https://doi.org/10.1080/02841860151116187
  67. Ordentlich P, Lin A, Shen CP, et al (1998). Notch inhibition of E47 supports the existence of a novel signaling pathway. Mol Cell Biol, 18, 2230-39. https://doi.org/10.1128/MCB.18.4.2230
  68. Phillips TM, McBride WH, Pajonk F (2006). The response of CD24(-/low)/CD44+ breast cancer-initiating cells to radiation. J Natl Cancer Inst, 98, 1777-85. https://doi.org/10.1093/jnci/djj495
  69. Piao LS, Hur W, Kim TK, et al (2012). CD133+ liver cancer stem cells modulate radioresistance in human hepatocellular carcinoma. Cancer Lett, 315, 129-37. https://doi.org/10.1016/j.canlet.2011.10.012
  70. Purow B (2009). Notch inhibitors as a new tool in the war on cancer: a pathway to watch, Curr Pharm Biotechnol. Curr Pharm Biotechnol, 10, 154-60. https://doi.org/10.2174/138920109787315060
  71. Purow B (2012). Notch inhibition as a promising new approach to cancer therapy. Adv Exp Med Biol, 727, 305-19. https://doi.org/10.1007/978-1-4614-0899-4_23
  72. Pyo H, Choy H, Amorino GP, et al (2001). A selective cyclooxygenase-2 inhibitor, NS-398, enhances the effect of radiation in vitro and in vivo preferentially on the cells that express cyclooxygenase-2. Clin Cancer Res, 7, 2998-3005.
  73. Qi R, An H, Yu Y, et al (2003). Notch1 signaling inhibits growth of human hepatocellular carcinoma through induction of cell cycle arrest and apoptosis. Cancer Res, 63, 8323-9.
  74. Ramakrishnan V, Ansell S, Haug J, et al (2012). MRK003, a gamma-secretase inhibitor exhibits promising in vitro preclinical activity in multiple myeloma and non-Hodgkin's lymphoma. Leukemia, 26, 340-8. https://doi.org/10.1038/leu.2011.192
  75. Rasul S, Balasubramanian R, Filipovic A, et al (2009). Inhibition of gamma-secretase induces G2/M arrest and triggers apoptosis in breast cancer cells. Br J Cancer, 100, 1879-88. https://doi.org/10.1038/sj.bjc.6605034
  76. Reichert S, Rodel C, Mirsch J, et al (2011). Survivin inhibition and DNA double-strand break repair: a molecular mechanism to overcome radioresistance in glioblastoma. Radiother Oncol, 101, 51-8. https://doi.org/10.1016/j.radonc.2011.06.037
  77. Searfoss GH, Jordan WH, Calligaro DO, et al (2003). Adipsin, a biomarker of gastrointestinal toxicity mediated by a functional gamma-secretase inhibitor. J Biol Chem, 278, 46107-16. https://doi.org/10.1074/jbc.M307757200
  78. Sethi N, Dai X, Winter CG, Kang Y (2011). Tumor-derived JAGGED1 promotes osteolytic bone metastasis of breast cancer by engaging notch signaling in bone cells. Cancer Cell, 19, 192-205. https://doi.org/10.1016/j.ccr.2010.12.022
  79. Sikandar SS, Pate KT, Anderson S, et al (2010). 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, 70, 1469-78. https://doi.org/10.1158/0008-5472.CAN-09-2557
  80. Spalding AC, Lawrence TS (2006). New and emerging radiosensitizers and radioprotectors. Cancer Invest, 24, 444-56. https://doi.org/10.1080/07357900600705706
  81. Squatrito M, Brennan CW, Helmy K, et al (2010). Loss of ATM/Chk2/p53 pathway components accelerates tumor development and contributes to radiation resistance in gliomas. Cancer Cell, 18, 619-29. https://doi.org/10.1016/j.ccr.2010.10.034
  82. Sriuranpong V, Borges MW, Ravi RK, et al (2001). Notch signaling induces cell cycle arrest in small cell lung cancer cells. Cancer Res, 61, 3200-5.
  83. Strosberg JR, Yeatman T, Weber J, et al (2012). A phase II study of RO4929097 in metastatic colorectal cancer. Eur J Cancer, 48, 997-1003. https://doi.org/10.1016/j.ejca.2012.02.056
  84. Suwanjunee S, Wongchana W, Palaga T (2008). Inhibition of gamma-secretase affects proliferation of leukemia and hepatoma cell lines through Notch signaling. Anticancer Drugs, 19, 477-86. https://doi.org/10.1097/CAD.0b013e3282fc6cdd
  85. Szumiel I (2008). Intrinsic radiation sensitivity: cellular signaling is the key. Radiat Res, 169, 249-58. https://doi.org/10.1667/RR1239.1
  86. Teimourian S, Jalal R, Sohrabpour M, Goliaei B (2006). Downregulation of Hsp27 radiosensitizes human prostate cancer cells. Int J Urol, 13, 1221-5. https://doi.org/10.1111/j.1442-2042.2006.01483.x
  87. Tien AC, Rajan A, Bellen HJ (2009). A Notch updated. J Cell Biol, 184, 621-9. https://doi.org/10.1083/jcb.200811141
  88. Tsuyada A, Chow A, Wu J, et al (2012). CCL2 mediates crosstalk between cancer cells and stromal fibroblasts that regulates breast cancer stem cells. Cancer Res, 72, 2768-79 . https://doi.org/10.1158/0008-5472.CAN-11-3567
  89. Wang J, Wakeman TP, Lathia JD, et al (2010). Notch promotes radioresistance of glioma stem cells. Stem Cells, 28, 17-28.
  90. Wang M, Li JT, Zeng YX, Hou JH, Lin QQ. (2005). Expression and Significance of Notch1, P21WAF1 and involucrin in nasopharyngeal carcinoma. Ai Zheng, 24, 1230-4.
  91. Wang Z, Li Y, Banerjee S, Sarkar FH (2008). Anticancer Res. Exploitation of the Notch signaling pathway as a novel target for cancer therapy. Anticancer Res, 28, 3621-30.
  92. Wang Z, Li Y, Banerjee S, Sarkar FH (2009). Emerging role of Notch in stem cells and cancer. Cancer Lett, 279, 8-12. https://doi.org/10.1016/j.canlet.2008.09.030
  93. Wei P, Walls M, Qiu M, et al (2010). Evaluation of selective gamma-secretase inhibitor PF-03084014 for its antitumor efficacy and gastrointestinal safety to guide optimal clinical trial design. Mol Cancer Ther, 9, 1618-28. https://doi.org/10.1158/1535-7163.MCT-10-0034
  94. Whitehead J, Thygesen H, Jaki T, et al (2012). A novel Phase I/ IIa design for early phase oncology studies and its application in the evaluation of MK-0752 in pancreatic cancer. Stat Med, 31, 1931-43 . https://doi.org/10.1002/sim.5331
  95. Woodward WA, Chen MS, Behbod F, et al (2007). WNT/betacatenin mediates radiation resistance of mouse mammary progenitor cells. Proc Natl Acad Sci U S A, 104, 618-23. https://doi.org/10.1073/pnas.0606599104
  96. Wu Y, Cain-Hom C, Choy L, et al (2010). Therapeutic antibody targeting of individual Notch receptors. Nature, 464, 1052-7. https://doi.org/10.1038/nature08878
  97. Xu X, Zhao Y, Xu M, et al (2011). Activation of Notch signal pathway is associated with a poorer prognosis in acute myeloid leukemia. Med Oncol, 28, S483-9. https://doi.org/10.1007/s12032-010-9667-0
  98. Yeung TM, Gandhi SC, Bodmer WF (2011). Hypoxia and lineage specification of cell line-derived colorectal cancer stem cells. Proc Natl Acad Sci U S A, 108, 4382-7. https://doi.org/10.1073/pnas.1014519107
  99. Yu J, Liu F, Sun M, Sun Z, Sun S (2011). Enhancement of radiosensitivity and the potential mechanism on human esophageal carcinoma cells by tetrandrine. Cancer Biother Radiopharm, 26, 437-42. https://doi.org/10.1089/cbr.2011.0964
  100. Yu S, Zhang R, Liu F, et al (2011). Down-regulation of Notch signaling by a gamma-secretase inhibitor enhances the radiosensitivity of nasopharyngeal carcinoma cells. Oncol Rep, 26, 1323-8.
  101. Zaidi S, McLaughlin M, Bhide SA, et al (2012). The HSP90 Inhibitor NVP-AUY922 Radiosensitizes by Abrogation of Homologous Recombination Resulting in Mitotic Entry with Unresolved DNA Damage. PLoS One, 7, e35436. https://doi.org/10.1371/journal.pone.0035436
  102. Zhang AL, Russell PJ, Knittel T, Milross C (2007). Paclitaxel enhanced radiation sensitization for the suppression of human prostate cancer tumor growth via a p53 independent pathway. Prostate, 67, 1630-40. https://doi.org/10.1002/pros.20638
  103. Zhang X, Komaki R, Wang L, Fang B, Chang JY (2008). Treatment of radioresistant stem-like esophageal cancer cells by an apoptotic gene-armed, telomerase-specific oncolytic adenovirus. Clin Cancer Res, 14, 2813-23. https://doi.org/10.1158/1078-0432.CCR-07-1528
  104. Zhang XP, Zheng G, Zou L, et al (2008). Notch activation promotes cell proliferation and the formation of neural stem cell-like colonies in human glioma cells. Mol. Cell. Biochem. 307, 101-8.
  105. Zhang Y, Li B, Ji ZZ Zheng PS. (2010). Notch1 regulates the growth of human colon cancers. Cancer. 116, 5207-18. https://doi.org/10.1002/cncr.25449
  106. Zhang Y, Peng J, Zhang H, et al. (2010). Notch1 signaling is activated in cells expressing embryonic stem cell proteins in human primary nasopharyngeal carcinoma. J Otolaryngol Head Neck Surg, 39, 157-66.
  107. Zhen Y, Zhao S, Li Q, Li Y, Kawamoto K (2010). Arsenic trioxide-mediated Notch pathway inhibition depletes the cancer stem-like cell population in gliomas. Cancer Lett, 292, 64-72. https://doi.org/10.1016/j.canlet.2009.11.005

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