ALDH+ tumor-initiating cells exhibiting gain in NOTCH1 gene copy number have enhanced regrowth sensitivity to a γ-secretase inhibitor and irinotecan in colorectal cancer

Molecular Oncology

Volumn 6, Issue 3, 2012, Pages 370-381

  Arcaroli, John J ^a   Powell, Rebecca W ^a   Varella Garcia, Marileila ^a   McManus, Martine ^a   Tan, Aik Choon ^a   Quackenbush, Kevin S ^a   Pitts, Todd M ^a   Gao, Dexiang ^a   Spreafico, Anna ^a   Dasari, Arvind ^a   Touban, Basel M ^a   Messersmith, Wells A ^a  

^a UNIVERSITY OF COLORADO CANCER CENTER   (United States)

Author keywords

Cancer stem cell; Colorectal cancer; Gamma secretase inhibitor; Notch

Indexed keywords

ALDEHYDE DEHYDROGENASE; IRINOTECAN; NOTCH1 RECEPTOR; PF 3084014;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CANCER PREVENTION; CANCER RECURRENCE; COLORECTAL CANCER; CONTROLLED STUDY; DRUG EFFECT; DRUG EFFICACY; FEMALE; GENE DOSAGE; HUMAN; HUMAN CELL; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL;

EID: 84861461140     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2012.03.004     Document Type: Article

References (34)

1. Aleksic T., Feller S.M. Gamma-secretase inhibition combined with platinum compounds enhances cell death in a large subset of colorectal cancer cells. Cell Commun. Signal. 2008, 6:8.
2. Carpentino J.E., Hynes M.J., Appelman H.D., Zheng T., Steindler D.A., Scott E.W., Huang E.H. Aldehyde dehydrogenase-expressing colon stem cells contribute to tumorigenesis in the transition from colitis to cancer. Cancer Res. 2009, 69:8208-8215.
3. Chu D., Wang W., Xie H., Li Y., Dong G., Xu C., Chen D., Zheng J., Li M., Lu Z., Ji G. Notch1 expression in colorectal carcinoma determines tumor differentiation status. J. Gastrointest. Surg. 2009, 13:253-260.
4. Chu D., Li Y., Wang W., Zhao Q., Li J., Lu Y., Li M., Dong G., Zhang H., Xie H., Ji G. High level of Notch1 protein is associated with poor overall survival in colorectal cancer. Ann. Surg. Oncol. 2010, 17:1337-1342.
5. Curry C.L., Reed L.L., Golde T.E., Miele L., Nickoloff B.J., Foreman K.E. Gamma secretase inhibitor blocks Notch activation and induces apoptosis in Kaposi's sarcoma tumor cells. Oncogene 2005, 24:6333-6344.
6. Dangles-Marie V., Pocard M., Richon S., Weiswald L.B., Assayag F., Saulnier P., Judde J.G., Janneau J.L., Auger N., Validire P., Dutrillaux B., Praz F., Bellet D., Poupon M.F. Establishment of human colon cancer cell lines from fresh tumors versus xenografts: comparison of success rate and cell line features. Cancer Res. 2007, 67:398-407.
7. Emmink B.L., Van Houdt W., Vries R.G., Hoogwater F.J., Jimenez C.R., Clevers H., Borel Rinkes I.H., Kranenburg O. Differentiated human colorectal cancer cells protect tumor-initiating cells from irinotecan. Gastroenterology 2011, 141:269-278. Abstract: AACR: Colorectal Cancer: Biology to Therapy.
8. Fan X., Mikolaenko I., Elhassan I., Ni X., Wang Y., Ball D., Brat D.J., Perry A., Eberhart C.G. Notch1 and notch2 have opposite effects on embryonal brain tumor growth. Cancer Res. 2004, 64:7787-7793.
9. Hoey T., Yen W.C., Axelrod F., Basi J., Donigian L., Dylla S., Fitch-Bruhns M., Lazetic S., Park I.K., Sato A., Satyal S., Wang X., Clarke M.F., Lewicki J., Gurney A. DLL4 blockade inhibits tumor growth and reduces tumor-initiating cell frequency. Cell Stem Cell 2009, 5:168-177.
10. Hopfer O., Zwahlen D., Fey M.F., Aebi S. The Notch pathway in ovarian carcinomas and adenomas. Br. J. Cancer 2005, 93:709-718.
11. Huang E.H., Hynes M.J., Zhang T., Ginestier C., Dontu G., Appelman H., Fields J.Z., Wicha M.S., Boman B.M. Aldehyde dehydrogenase 1 is a marker for normal and malignant human colonic stem cells (SC) and tracks SC overpopulation during colon tumorigenesis. Cancer Res. 2009, 69:3382-3389.
12. Jemal A., Siegel R., Ward E., Hao Y., Xu J., Thun M.J. Cancer statistics, 2009. CA Cancer J. Clin. 2009, 59:225-249.
13. Kanehisa M., Araki M., Goto S., Hattori M., Hirakawa M., Itoh M., Katayama T., Kawashima S., Okuda S., Tokimatsu T., Yamanishi Y. KEGG for linking genomes to life and the environment. Nucleic Acids Res. 2008, 36:D480-D484.
14. Lee S.F., Shah S., Yu C., Wigley W.C., Li H., Lim M., Pedersen K., Han W., Thomas P., Lundkvist J., Hao Y.H., Yu G. A conserved GXXXG motif in APH-1 is critical for assembly and activity of the gamma-secretase complex. J. Biol. Chem. 2004, 279:4144-4152.
15. Li C., Heidt D.G., Dalerba P., Burant C.F., Zhang L., Adsay V., Wicha M., Clarke M.F., Simeone D.M. Identification of pancreatic cancer stem cells. Cancer Res. 2007, 67:1030-1037.
16. Meng R.D., Shelton C.C., Li Y.M., Qin L.X., Notterman D., Paty P.B., Schwartz G.K. Gamma-secretase inhibitors abrogate oxaliplatin-induced activation of the Notch-1 signaling pathway in colon cancer cells resulting in enhanced chemosensitivity. Cancer Res. 2009, 69:573-582.
17. Messersmith W., LoRusso P., Cleary J.M., Dasari A., Zhang X., et al. A phase I dose-escalation study of the novel gamma secretase inhibitor PF-03084014 in patients (pts) with advanced solid tumors. J. Clin. Oncol. 2011, 29. suppl; abstr 3100.
18. Murata K., Hattori M., Hirai N., Shinozuka Y., Hirata H., Kageyama R., Sakai T., Minato N. Hes1 directly controls cell proliferation through the transcriptional repression of p27Kip1. Mol. Cell Biol. 2005, 25:4262-4271.
19. Noguera-Troise I., Daly C., Papadopoulos N.J., Coetzee S., Boland P., Gale N.W., Lin H.C., Yancopoulos G.D., Thurston G. Blockade of Dll4 inhibits tumour growth by promoting non-productive angiogenesis. Nature 2006, 444:1032-1037.
20. O'Brien C.A., Pollett A., Gallinger S., Dick J.E. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 2007, 445:106-110.
21. Oswald F., Liptay S., Adler G., Schmid R.M. NF-kappaB2 is a putative target gene of activated Notch-1 via RBP-Jkappa. Mol. Cell Biol. 1998, 18:2077-2088.
22. Pannuti A., Foreman K., Rizzo P., Osipo C., Golde T., Osborne B., Miele L. Targeting Notch to target cancer stem cells. Clin. Cancer Res. 2010, 16:3141-3152.
23. Reedijk M., Odorcic S., Chang L., Zhang H., Miller N., McCready D.R., Lockwood G., Egan S.E. High-level coexpression of JAG1 and NOTCH1 is observed in human breast cancer and is associated with poor overall survival. Cancer Res. 2005, 65:8530-8537.
24. Ricci-Vitiani L., Lombardi D.G., Pilozzi E., Biffoni M., Todaro M., Peschle C., De Maria R. Identification and expansion of human colon-cancer-initiating cells. Nature 2007, 445:111-115.
25. Rubio-Viqueira B., Jimeno A., Cusatis G., Zhang X., Iacobuzio-Donahue C., Karikari C., Shi C., Danenberg K., Danenberg P.V., Kuramochi H., Tanaka K., Singh S., Salimi-Moosavi H., Bouraoud N., Amador M.L., Altiok S., Kulesza P., Yeo C., Messersmith W., Eshleman J., Hruban R.H., Maitra A., Hidalgo M. An in vivo platform for translational drug development in pancreatic cancer. Clin. Cancer Res. 2006, 12:4652-4661.
26. Santagata S., Demichelis F., Riva A., Varambally S., Hofer M.D., Kutok J.L., Kim R., Tang J., Montie J.E., Chinnaiyan A.M., Rubin M.A., Aster J.C. JAGGED1 expression is associated with prostate cancer metastasis and recurrence. Cancer Res. 2004, 64:6854-6857.
27. Schatton T., Murphy G.F., Frank N.Y., Yamaura K., Waaga-Gasser A.M., Gasser M., Zhan Q., Jordan S., Duncan L.M., Weishaupt C., Fuhlbrigge R.C., Kupper T.S., Sayegh M.H., Frank M.H. Identification of cells initiating human melanomas. Nature 2008, 451:345-349.
28. Sikandar S.S., Pate K.T., Anderson S., Dizon D., Edwards R.A., Waterman M.L., Lipkin S.M. 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, 70:1469-1478.
29. Singh S.K., Hawkins C., Clarke I.D., Squire J.A., Bayani J., Hide T., Henkelman R.M., Cusimano M.D., Dirks P.B. Identification of human brain tumour initiating cells. Nature 2004, 432:396-401.
30. Subramanian A., Tamayo P., Mootha V.K., Mukherjee S., Ebert B.L., Gillette M.A., Paulovich A., Pomeroy S.L., Golub T.R., Lander E.S., Mesirov J.P. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:15545-15550.
31. van Es J.H., van Gijn M.E., Riccio O., van den Born M., Vooijs M., Begthel H., Cozijnsen M., Robine S., Winton D.J., Radtke F., Clevers H. Notch/gamma-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature 2005, 435:959-963.
32. Vasiliou V., Pappa A., Estey T. Role of human aldehyde dehydrogenases in endobiotic and xenobiotic metabolism. Drug Metab. Rev. 2004, 36:279-299.
33. Zhang Y., Li B., Ji Z.Z., Zheng P.S. Notch1 regulates the growth of human colon cancers. Cancer 2010, 116:5207-5218.
34. Zhou B.B., Zhang H., Damelin M., Geles K.G., Grindley J.C., Dirks P.B. Tumour-initiating cells: challenges and opportunities for anticancer drug discovery. Nat. Rev. Drug Discov. 2009, 8:806-823.