Autophagy contributes to the enrichment and survival of colorectal cancer stem cells under oxaliplatin treatment

Cancer Letters

Volumn 361, Issue 1, 2015, Pages 128-136

  Yang, Hao Zheng ^a   Ma, Yi ^a   Zhou, Yan ^a   Xu, Long Mei ^a   Chen, Xiao Jing ^a   Ding, Wen Bin ^a   Zou, Han Bing ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Autophagy; Cancer stem cells; Chemoresistance; Colorectal cancer

Indexed keywords

ANTINEOPLASTIC AGENT; OXALIPLATIN; MESSENGER RNA; PLATINUM COMPLEX; TUMOR MARKER;

APOPTOSIS; ARTICLE; AUTOPHAGY; CANCER CELL; CANCER SURVIVAL; CELL COUNTING; CELL DIFFERENTIATION; COLORECTAL CANCER; CONTROLLED STUDY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING; CANCER STEM CELL; CELL PROLIFERATION; COLORECTAL NEOPLASMS; DRUG EFFECTS; DRUG RESISTANCE; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; METABOLISM; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL CULTURE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; AUTOPHAGY; BIOMARKERS, TUMOR; BLOTTING, WESTERN; CELL PROLIFERATION; COLORECTAL NEOPLASMS; DRUG RESISTANCE, NEOPLASM; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; NEOPLASTIC STEM CELLS; ORGANOPLATINUM COMPOUNDS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TUMOR CELLS, CULTURED;

EID: 84925281259     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2015.02.045     Document Type: Article

References (51)

1. Grothey A. Reintroduction of oxaliplatin: a viable approach to the long-term management of metastatic colorectal cancer. Oncology 2010, 79:389-399.
2. Ricci-Vitiani L., Fabrizi E., Palio E., De Maria R. Colon cancer stem cells. J. Mol. Med 2009, 87:1097-1104.
3. Siegel R., Naishadham D., Jemal A. Cancer statistics, 2013. CA Cancer J. Clin 2013, 63:11-30.
4. Punt C.J., Tol J. More is less - combining targeted therapies in metastatic colorectal cancer. Nat. Rev. Clin. Oncol 2009, 6:731-733.
5. 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.
6. Dave B., Chang J. Treatment resistance in stem cells and breast cancer. J. Mammary Gland Biol. Neoplasia 2009, 14:79-82.
7. Chu P., Clanton D.J., Snipas T.S., Lee J., Mitchell E., Nguyen M.L., et al. Characterization of a subpopulation of colon cancer cells with stem cell-like properties. Int. J. Cancer 2009, 124:1312-1321.
8. Cammareri P., Scopelliti A., Todaro M., Eterno V., Francescangeli F., Moyer M.P., et al. Aurora-a is essential for the tumorigenic capacity and chemoresistance of colorectal cancer stem cells. Cancer Res 2010, 70:4655-4665.
9. Fan C.W., Chen T., Shang Y.N., Gu Y.Z., Zhang S.L., Lu R., et al. Cancer-initiating cells derived from human rectal adenocarcinoma tissues carry mesenchymal phenotypes and resist drug therapies. Cell Death Dis 2013, 4:e828.
10. Lara-Padilla E., Caceres-Cortes J.R. On the nature of the tumor-initiating cell. Curr. Stem Cell Res. Ther 2012, 7:26-35.
11. Warr M.R., Binnewies M., Flach J., Reynaud D., Garg T., Malhotra R., et al. FOXO3A directs a protective autophagy program in haematopoietic stem cells. Nature 2013, 494:323-327.
12. Chaachouay H., Ohneseit P., Toulany M., Kehlbach R., Multhoff G., Rodemann H.P. Autophagy contributes to resistance of tumor cells to ionizing radiation. Radiother. Oncol 2011, 99:287-292.
13. Mizushima N., Yoshimori T., Levine B. Methods in mammalian autophagy research. Cell 2010, 140:313-326.
14. Yang Z., Klionsky D.J. An overview of the molecular mechanism of autophagy. Curr. Top. Microbiol. Immunol 2009, 335:1-32.
15. Pan H., Cai N., Li M., Liu G.H., Izpisua Belmonte J.C. Autophagic control of cell 'stemness'. EMBO Mol. Med 2013, 5:327-331.
16. Singh B.N., Kumar D., Shankar S., Srivastava R.K. Rottlerin induces autophagy which leads to apoptotic cell death through inhibition of PI3K/Akt/mTOR pathway in human pancreatic cancer stem cells. Biochem. Pharmacol 2012, 84:1154-1163.
17. Gong C., Bauvy C., Tonelli G., Yue W., Delomenie C., Nicolas V., et al. Beclin 1 and autophagy are required for the tumorigenicity of breast cancer stem-like/progenitor cells. Oncogene 2013, 32:2261-2272. 2272e.1-11.
18. Gong C., Song E., Codogno P., Mehrpour M. The roles of BECN1 and autophagy in cancer are context dependent. Autophagy 2012, 8:1853-1855.
19. Rausch V., Liu L., Apel A., Rettig T., Gladkich J., Labsch S., et al. Autophagy mediates survival of pancreatic tumour-initiating cells in a hypoxic microenvironment. J. Pathol 2012, 227:325-335.
20. Palmeira dos Santos C., Pereira G.J., Barbosa C.M., Jurkiewicz A., Smaili S.S., Bincoletto C. Comparative study of autophagy inhibition by 3MA and CQ on cytarabine induced death of leukaemia cells. J. Cancer Res. Clin. Oncol 2014, 140:909-920.
21. Mousavi S.A., Brech A., Berg T., Kjeken R. Phosphoinositide 3-kinase regulates maturation of lysosomes in rat hepatocytes. Biochem. J. 2003, 372:861-869.
22. Klionsky D.J., Abeliovich H., Agostinis P., Agrawal D.K., Aliev G., Askew D.S., et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008, 4:151-175.
23. Schmeisser H., Fey S.B., Horowitz J., Fischer E.R., Balinsky C.A., Miyake K., et al. Type I interferons induce autophagy in certain human cancer cell lines. Autophagy 2013, 9:683-696.
24. Song Y.J., Zhang S.S., Guo X.L., Sun K., Han Z.P., Li R., et al. Autophagy contributes to the survival of CD133+ liver cancer stem cells in the hypoxic and nutrient-deprived tumor microenvironment. Cancer Lett 2013, 339:70-81.
25. Ma Y., Kang X.N., Ding W.B., Yang H.Z., Wang Y., Zhang J., et al. Renal tissue thawed for 30 minutes is still suitable for gene expression analysis. PLoS ONE 2014, 9:e93175.
26. Ma Y., Yang H.Z., Dong B.J., Zou H.B., Zhou Y., Kong X.M., et al. Biphasic regulation of autophagy by miR-96 in prostate cancer cells under hypoxia. Oncotarget 2014, 5:9169-9182.
27. Ertmer A., Huber V., Gilch S., Yoshimori T., Erfle V., Duyster J., et al. The anticancer drug imatinib induces cellular autophagy. Leukemia 2007, 21:936-942.
28. Li X., Fan Z. The epidermal growth factor receptor antibody cetuximab induces autophagy in cancer cells by downregulating HIF-1alpha and Bcl-2 and activating the beclin 1/hVps34 complex. Cancer Res 2010, 70:5942-5952.
29. Zhu K., Dunner K., McConkey D.J. Proteasome inhibitors activate autophagy as a cytoprotective response in human prostate cancer cells. Oncogene 2010, 29:451-462.
30. Bjorkoy G., Lamark T., Pankiv S., Overvatn A., Brech A., Johansen T. Monitoring autophagic degradation of p62/SQSTM1. Methods Enzymol 2009, 452:181-197.
31. Mizushima N., Yamamoto A., Hatano M., Kobayashi Y., Kabeya Y., Suzuki K., et al. Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J. Cell Biol 2001, 152:657-668.
32. Komatsu M., Waguri S., Ueno T., Iwata J., Murata S., Tanida I., et al. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J. Cell Biol 2005, 169:425-434.
33. Colak S., Zimberlin C.D., Fessler E., Hogdal L., Prasetyanti P.R., Grandela C.M., et al. Decreased mitochondrial priming determines chemoresistance of colon cancer stem cells. Cell Death Differ 2014, 21:1170-1177.
34. Visvader J.E., Lindeman G.J. Cancer stem cells: current status and evolving complexities. Cell Stem Cell 2012, 10:717-728.
35. Magee J.A., Piskounova E., Morrison S.J. Cancer stem cells: impact, heterogeneity, and uncertainty. Cancer Cell 2012, 21:283-296.
36. Du L., Wang H., He L., Zhang J., Ni B., Wang X., et al. CD44 is of functional importance for colorectal cancer stem cells. Clin. Cancer Res 2008, 14:6751-6760.
37. Ohata H., Ishiguro T., Aihara Y., Sato A., Sakai H., Sekine S., et al. Induction of the stem-like cell regulator CD44 by Rho kinase inhibition contributes to the maintenance of colon cancer-initiating cells. Cancer Res 2012, 72:5101-5110.
38. Kantara C., O'Connell M., Sarkar S., Moya S., Ullrich R., Singh P. Curcumin promotes autophagic survival of a subset of colon cancer stem cells, which are ablated by DCLK1-siRNA. Cancer Res 2014, 74:2487-2498.
39. Haraguchi N., Ohkuma M., Sakashita H., Matsuzaki S., Tanaka F., Mimori K., et al. CD133+CD44+ population efficiently enriches colon cancer initiating cells. Ann. Surg. Oncol 2008, 15:2927-2933.
40. Ju S.Y., Chiou S.H., Su Y. Maintenance of the stemness in CD44(+) HCT-15 and HCT-116 human colon cancer cells requires miR-203 suppression. Stem Cell Res 2014, 12:86-100.
41. Goldberg R.M., Sargent D.J., Morton R.F., Fuchs C.S., Ramanathan R.K., Williamson S.K., et al. Randomized controlled trial of reduced-dose bolus fluorouracil plus leucovorin and irinotecan or infused fluorouracil plus leucovorin and oxaliplatin in patients with previously untreated metastatic colorectal cancer: a North American Intergroup Trial. J. Clin. Oncol 2006, 24:3347-3353.
42. Degenhardt K., Mathew R., Beaudoin B., Bray K., Anderson D., Chen G., et al. Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 2006, 10:51-64.
43. Mathew R., Karp C.M., Beaudoin B., Vuong N., Chen G., Chen H.Y., et al. Autophagy suppresses tumorigenesis through elimination of p62. Cell 2009, 137:1062-1075.
44. Qadir M.A., Kwok B., Dragowska W.H., To K.H., Le D., Bally M.B., et al. Macroautophagy inhibition sensitizes tamoxifen-resistant breast cancer cells and enhances mitochondrial depolarization. Breast Cancer Res. Treat 2008, 112:389-403.
45. O'Donovan T.R., O'Sullivan G.C., McKenna S.L. Induction of autophagy by drug-resistant esophageal cancer cells promotes their survival and recovery following treatment with chemotherapeutics. Autophagy 2011, 7:509-524.
46. Apel A., Herr I., Schwarz H., Rodemann H.P., Mayer A. Blocked autophagy sensitizes resistant carcinoma cells to radiation therapy. Cancer Res 2008, 68:1485-1494.
47. Mathew R., Karantza-Wadsworth V., White E. Role of autophagy in cancer. Nat. Rev. Cancer 2007, 7:961-967.
48. Amaravadi R.K., Yu D., Lum J.J., Bui T., Christophorou M.A., Evan G.I., et al. Autophagy inhibition enhances therapy-induced apoptosis in a Myc-induced model of lymphoma. J. Clin. Invest 2007, 117:326-336.
49. Dubrovska A., Kim S., Salamone R.J., Walker J.R., Maira S.M., Garcia-Echeverria C., et al. The role of PTEN/Akt/PI3K signaling in the maintenance and viability of prostate cancer stem-like cell populations. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:268-273.
50. Zhou J., Wulfkuhle J., Zhang H., Gu P., Yang Y., Deng J., et al. Activation of the PTEN/mTOR/STAT3 pathway in breast cancer stem-like cells is required for viability and maintenance. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:16158-16163.
51. Keniry M., Parsons R. The role of PTEN signaling perturbations in cancer and in targeted therapy. Oncogene 2008, 27:5477-5485.