Cancer-initiating cells derived from human rectal adenocarcinoma tissues carry mesenchymal phenotypes and resist drug therapies

Cell Death and Disease

Volumn 4, Issue 10, 2013, Pages

  Fan, C W ^a   Chen, T ^a   Shang, Y N ^a   Gu, Y Z ^a   Zhang, S L ^a   Lu, R ^a   OuYang, S R ^a   Zhou, X ^a   Li, Y ^a   Meng, W T ^a   Hu, J K ^a   Lu, Y ^a   Sun, X F ^b   Bu, H ^a   Zhou, Z G ^a   Mo, X M ^a  

^a SICHUAN UNIVERSITY   (China)

^b LINKÖPING UNIVERSITY   (Sweden)

Author keywords

Cancer initiating cells (CICs); CD44; CD54; Chemoresistance; Rectal adenocarcinoma

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; BIOLOGICAL MARKER; BMI1 PROTEIN; CETUXIMAB; CYTOKERATIN 20; CYTOKERATIN 7; EPIDERMAL GROWTH FACTOR RECEPTOR; EPITHELIAL CELL ADHESION MOLECULE; FLUOROURACIL; FOLINATE CALCIUM; HERMES ANTIGEN; INTERCELLULAR ADHESION MOLECULE 1; OXALIPLATIN; TRANSCRIPTION FACTOR CDX2; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; UVOMORULIN; VIMENTIN;

ADVANCED CANCER; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER CELL; CANCER INITIATING CELL; CANCER TISSUE; CELL AGGREGATION; CELL DIFFERENTIATION; CELL EXPANSION; CELL ISOLATION; CELL MIGRATION; CELL RENEWAL; CELL STRUCTURE; CELL SUBPOPULATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROGENY; RECTUM CARCINOMA; TUMOR GROWTH;

ADENOCARCINOMA; ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTIGENS, CD44; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; CARCINOGENESIS; CELL DIFFERENTIATION; CELL PROLIFERATION; CULTURE MEDIA, SERUM-FREE; DRUG RESISTANCE, NEOPLASM; EPITHELIAL-MESENCHYMAL TRANSITION; FLUOROURACIL; HUMANS; INTERCELLULAR ADHESION MOLECULE-1; LEUCOVORIN; MESODERM; MICE; NEOPLASTIC STEM CELLS; ORGANOPLATINUM COMPOUNDS; PHENOTYPE; RECTAL NEOPLASMS; SPHEROIDS, CELLULAR; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84887496386     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.337     Document Type: Article

References (48)

1. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics 2010CA Cancer J Clin 2010; 60: 277-300
2. Yamauchi M, Morikawa T, Kuchiba A, Imamura Y, Qian ZR, Nishihara R et al. Assessment of colorectal cancer molecular features along bowel subsites challenges the conception of distinct dichotomy of proximal versus distal colorectum. Gut 2012; 61: 847-854
3. Yu H, Harris RE, Gao YT, Gao R, Wynder EL. Comparative epidemiology of cancers of the colon, rectum, prostate and breast in Shanghai, China versus the United States. Int J Epidemiol 1991; 20: 76-81
4. Cunningham D, Atkin W, Lenz HJ, Lynch HT, Minsky B, Nordlinger B et al. Colorectal cancer. Lancet 2010; 375: 1030-1047
5. Ricci-Vitiani L, Fabrizi E, Palio E, De Maria R. Colon cancer stem cells. J Mol Med 2009; 87: 1097-1104
6. Todaro M, Alea MP, Di Stefano AB, Cammareri P, Vermeulen L, Lovino F et al. Colon cancer stem cells dictate tumor growth and resist cell death by production of interleukin-4. Cell Stem Cell 2007; 1: 389-402
7. Pang R, Law WL, Chu AC, Poon JT, Lam CS, Chow AK et al. A subpopulation of CD26-cancer stem cells with metastatic capacity in human colorectal cancer. Cell Stem Cell 2010; 6: 603-615
8. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T et al. Identification of human brain tumour initiating cells. Nature 2004; 432: 396-401
9. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003; 100: 3983-3988
10. Fang D, Nguyen TK, Leishear K, Finko R, Kulp AN, Hotz S et al. A tumorigenic subpopulation with stem cell properties in melanomas. Cancer Res 2005; 65: 9328-9337
11. Dembinski JL, Krauss S. Characterization and functional analysis of a slow cycling stem cell-like subpopulation in pancreas adenocarcinoma. Clin Exp Metastas 2009; 26: 611-623
12. Eramo A, Lotti F, Sette G, Pilozzi E, Biffoni M, Di Virgilio A et al. Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ 2008; 15: 504-514
13. Chen T, Yang K, Yu J, Meng W, Yuan D, Bi F et al. Identification and expansion of cancer stem cells in tumor tissues and peripheral blood derived from gastric adenocarcinoma patients. Cell Res 2012; 22: 248-258
14. O'Brien CA, Pollett A, Gallinger S, Dick JE. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 2007; 445: 106-110
15. Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C et al. Identification and expansion of human colon-cancer-initiating cells. Nature 2007; 445: 111-115
16. 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
17. Du L, Wang HY, He LY, Zhang JY, Ni BY, Wang XH et al. CD44 is of functional importance for colorectal cancer stem cells. Clin Cancer Res 2008; 14: 6751-6760
18. Fang DD, Kim YJ, Lee CN, Aggarwal S, McKinnon K, Mesmer D et al. Expansion of CD133(-) colon cancer cultures retaining stem cell properties to enable cancer stem cell target discovery. Brit J Cancer 2010; 102: 1265-1275
19. Carpentino JE, Hynes MJ, Appelman HD, Zheng T, Steindler DA, Scott EW et al. Aldehyde dehydrogenase-expressing colon stem cells contribute to tumorigenesis in the transition from colitis to cancer. Cancer Res 2009; 69: 8208-8215
20. Dylla SJ, Beviglia L, Park IK, Chartier C, Raval J, Ngan L et al. Colorectal cancer stem cells are enriched in xenogeneic tumors following chemotherapy. PLoS One 2008; 3: E2428
21. Shmelkov SV, Butler JM, Hooper AT, Hormigo A, Kushner J, Milde T et al. CD133 expression is not restricted to stem cells, and both CD133(-) and CD133(-) metastatic colon cancer cells initiate tumors. J Clin Invest 2008; 118: 2111-2120
22. Dalerba P, Dylla SJ, Park IK, Liu R, Wang X, Cho RW et al. Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci USA 2007; 104: 10158-10163
23. Chen T, Yang K, Yu J, Meng W, Yuan D, Bi F et al. Identification and expansion of cancer stem cells in tumor tissues and peripheral blood derived from gastric adenocarcinoma patients. Cell Res 2011; 22: 248-258
24. Hwang WL, Yang MH, Tsai ML, Lan HY, Su SH, Chang SC et al. SNAIL regulates interleukin-8 expression, stem cell-like activity, and tumorigenicity of human colorectal carcinoma cells. Gastroenterology 2011; 141: 279-291; 291 e271-275
25. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY et al. The epithelialmesenchymal transition generates cells with properties of stem cells. Cell 2008; 133: 704-715
26. Singh A, Settleman J. EMT, cancer stem cells and drug resistance: An emerging axis of evil in the war on cancer. Oncogene 2010; 29: 4741-4751
27. Jhawer M, Goel S, Wilson AJ, Montagna C, Ling YH, Byun DS et al. PIK3CA mutation/ PTEN expression status predicts response of colon cancer cells to the epidermal growth factor receptor inhibitor cetuximab. Cancer Res 2008; 68: 1953-1961
28. Todaro M, Alea MP, Scopelliti A, Medema JP, Stassi G. IL-4-mediated drug resistance in colon cancer stem cells. Cell Cycle 2008; 7: 309-313
29. Minoo P, Zlobec I, Peterson M, Terracciano L, Lugli A. Characterization of rectal, proximal and distal colon cancers based on clinicopathological, molecular and protein profiles. Int J Oncol 2010; 37: 707-718
30. van Engeland M, Derks S, Smits KM, Meijer GA, Herman JG. Colorectal cancer epigenetics: Complex simplicity. J Clin Oncol 2011; 29: 1382-1391
31. Sadanandam A, Lyssiotis CA, Homicsko K, Collisson EA, Gibb WJ, Wullschleger S et al. A colorectal cancer classification system that associates cellular phenotype and responses to therapy. Nat Med 2013; 19: 619-625
32. De Sousa EMF, Wang X, Jansen M, Fessler E, Trinh A. Poor-prognosis colon cancer is defined by a molecularly distinct subtype and develops from serrated precursor lesions. Nat Med 2013; 19: 614-618
33. Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T. Opinion: Migrating cancer stem cells-An integrated concept of malignant tumour progression. Nat Rev Cancer 2005; 5: 744-749
34. Brabletz T, Jung A, Reu S, Porzner M, Hlubek F, Kunz-Schughart LA et al. Variable beta-catenin expression in colorectal cancers indicates tumor progression driven by the tumor environment. Proc Natl Acad Sci USA 2001; 98: 10356-10361
35. Cui L, Ohuchida K, Mizumoto K, Moriyama T, Onimaru M, Nakata K et al. Prospectively isolated cancer-Associated CD10(-) fibroblasts have stronger interactions with CD133(-) colon cancer cells than with CD133(-) cancer cells. PLoS One 2010; 5: E12121
36. Christ B, Stock P, Dollinger MM. CD13: Waving the flag for a novel cancer stem cell target. Hepatology 2011; 53: 1388-1390
37. Harrington M. Blocking CD47 to stop tumor growth. Lab Anim 2012; 41: 111
38. Yeung TM, Gandhi SC, Wilding JL, Muschel R, Bodmer WF. Cancer stem cells from colorectal cancer-derived cell lines. Proc Natl Acad Sci USA 2010; 107: 3722-3727
39. Kanwar SS, Yu Y, Nautiyal J, Patel BB, Majumdar AP. The Wnt/beta-catenin pathway regulates growth and maintenance of colonospheres. Mol Cancer 2010; 9: 212
40. Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CH, Jones DL et al. Cancer stem cells-perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res 2006; 66: 9339-9344
41. Crea F, Danesi R, Farrar WL. Cancer stem cell epigenetics and chemoresistance. Epigenomics-UK 2009; 1: 63-79
42. Croker AK, Goodale D, Chu J, Postenka C, Hedley BD, Hess DA et al. High aldehyde dehydrogenase and expression of cancer stem cell markers selects for breast cancer cells with enhanced malignant and metastatic ability. J Cell Mol Med 2009; 13: 2236-2252
43. Chen YC, Chen YW, Hsu HS, Tseng LM, Huang PI, Lu KH et al. Aldehyde dehydrogenase 1 is a putative marker for cancer stem cells in head and neck squamous cancer. Biochem Biophys Res Commun 2009; 385: 307-313
44. Bednar F, Simeone DM. Pancreatic cancer stem cells and relevance to cancer treatments. J Cell Biochem 2009; 107: 40-45
45. Fabrizi E, di Martino S, Pelacchi F, Ricci-Vitiani L. Therapeutic implications of colon cancer stem cells. World J Gastroenterol 2010; 16: 3871-3877
46. Bokemeyer C, Bondarenko I, Makhson A, Hartmann JT, Aparicio J, de Braud F et al. Fluorouracil, leucovorin, and oxaliplatin with and without cetuximab in the first-line treatment of metastatic colorectal cancer. J Clin Oncol 2009; 27: 663-671
47. Tveit KM, Guren T, Glimelius B, Pfeiffer P, Sorbye H, Pyrhonen S et al. Phase III trial of cetuximab with continuous or intermittent fluorouracil, leucovorin, and oxaliplatin (Nordic FLOX) versus FLOX alone in first-line treatment of metastatic colorectal cancer: The NORDIC-VII study. J Clin Oncol 2012; 30: 1755-1762
48. Brabletz S, Schmalhofer O, Brabletz T. Gastrointestinal stem cells in development and cancer. J Pathol 2009; 217: 307-317