CD133-positive cancer stem cells from colo205 human colon adenocarcinoma cell line show resistance to chemotherapy and display a specific metabolomic profile

Genes and Cancer

Volumn 5, Issue 7-8, 2014, Pages 250-260

  Vincent, Zangiacomi ^a   Urakami, Kenichi ^a   Maruyama, Koji ^a   Yamaguchi, Ken ^a   Kusuhara, Masatoshi ^a  

^a SHIZUOKA CANCER CENTER   (Japan)

Author keywords

Adenocarcinoma; Cancer stem cells; CD133; CE TOF MS; Metabolomics

Indexed keywords

CD133 ANTIGEN; CISPLATIN; FLUOROURACIL;

ARTICLE; CANCER CHEMOTHERAPY; CANCER STEM CELL; CANCER SURVIVAL; CAPILLARY ELECTROPHORESIS; CARCINOGENESIS; CELL INVASION; CELL ISOLATION; COLON ADENOCARCINOMA; COLONY FORMATION; CONTROLLED STUDY; DOWN REGULATION; DRUG SENSITIVITY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; METASTASIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR GROWTH; TUMOR INVASION; TUMOR RECURRENCE; UPREGULATION;

EID: 84919638312     PISSN: 19476019     EISSN: 19476027     Source Type: Journal    
DOI: None     Document Type: Article

References (50)

1. Charafe-Jauffret E, Ginestier C, Bertucci F, Cabaud O, Wicinski J, Finetti P, Josselin E, Adelaide J, Nguyen TT, Monville F, Jacquemier J, Thomassin-Piana J, Pinna G, et al. ALDH1-positive cancer stem cells predict engraftment of primary breast tumors and are governed by a common stem cell program. Cancer Res. 2013; 73(24): 7290-7300.
2. Yin S, Li J, Hu C, Chen X, Yao M, Yan M, Jiang G, Ge C, Xie H, Wan D, Yang S, Zheng S, Gu J. CD133 positive hepatocellular carcinoma cells possess high capacity for tumorigenicity. Int J Cancer. 2007; 120(7): 1444-1450.
3. 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(7123): 106-110.
4. Yae T, Tsuchihashi K, Ishimoto T, Motohara T, Yoshikawa M, Yoshida GJ, Wada T, Masuko T, Mogushi K, Tanaka H, Osawa T, Kanki Y, Minami T, et al. Alternative splicing of CD44 mRNA by ESRP1 enhances lung colonization of metastatic cancer cell. Nat Commun. 2012; 3: 883.
5. Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C, De Maria R. Identification and expansion of human colon-cancer-initiating cells. Nature. 2007; 445(7123): 111-115.
6. Qiang L, Yang Y, Ma YJ, Chen FH, Zhang LB, Liu W, Qi Q, Lu N, Tao L, Wang XT, You QD, Guo QL. Isolation and characterization of cancer stem like cells in human glioblastoma cell lines. Cancer Lett. 2009; 279(1): 13-21.
7. Liu H, Patel MR, Prescher JA, Patsialou A, Qian D, Lin J, Wen S, Chang YF, Bachmann MH, Shimono Y, Dalerba P, Adorno M, Lobo N, et al. Cancer stem cells from human breast tumors are involved in spontaneous metastases in orthotopic mouse models. Proc Natl Acad Sci USA. 2010; 107(42): 18115-18120.
8. Christ O, Lucke K, Imren S, Leung K, Hamilton M, Eaves A, Smith C, Eaves C. Improved purification of hematopoietic stem cells based on their elevated aldehyde dehydrogenase activity. Haematologica. 2007; 92(9): 1165-1172.
9. Bensimon J, Altmeyer-Morel S, Benjelloun H, Chevillard S, Lebeau J. CD24(-/low) stem-like breast cancer marker defines the radiation-resistant cells involved in memorization and transmission of radiation-induced genomic instability. Oncogene. 2013; 32(2): 251-258.
10. Huang EH, Hynes MJ, Zhang T, Ginestier C, Dontu G, Appelman H, Fields JZ, Wicha MS, Boman BM. 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(8): 3382-3389.
11. Jung P, Sato T, Merlos-Suárez A, Barriga FM, Iglesias M, Rossell D, Auer H, Gallardo M, Blasco MA, Sancho E, Clevers H, Batlle E. Isolation and in vitro expansion of human colonic stem cells. Nat Med. 2011; 17(10): 1225-1227.
12. Boegl M, Prinz C. CD133 expression in different stages of gastric adenocarcinoma. Br J Cancer. 2009; 100(8): 1365-1366.
13. Li CY, Li BX, Liang Y, Peng RQ, Ding Y, Xu DZ, Zhang X, Pan ZZ, Wan DS, Zeng YX, Zhu XF, Zhang XS. Higher percentage of CD133+ cells is associated with poor prognosis in colon carcinoma patients with stage IIIB. J Transl Med. 2009; 7: 56.
14. Zhang Q, Shi S, Yen Y, Brown J, Ta JQ, Le AD. A subpopulation of CD133(+) cancer stem-like cells characterized in human oral squamous cell carcinoma confer resistance to chemotherapy. Cancer Lett. 2010; 289(2): 151-160.
15. Carpentino JE, Hynes MJ, Appelman HD, Zheng T, Steindler DA, Scott EW, Huang EH. Aldehyde dehydrogenase-expressing colon stem cells contribute to tumorigenesis in the transition from colitis to cancer. Cancer Res. 2009; 69(20): 8208-8215.
16. Armstrong L, Stojkovic M, Dimmick I, Ahmad S, Stojkovic P, Hole N, Lako M. Phenotypic characterization of murine primitive hematopoietic progenitor cells isolated on basis of aldehyde dehydrogenase activity. Stem Cells. 2004; 22(7): 1142-1151.
17. Shmelkov SV, Meeus S, Moussazadeh N, Kermani P, Rashbaum WK, Rabbany SY, Hanson MA, Lane WJ, St Clair R, Walsh KA, Dias S, Jacobson JT, Hempstead BL, 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(6): 2111-2120.
18. Charafe-Jauffret E, Ginestier C, Birnbaum D. Breast cancer stem cells: tools and models to rely on. BMC Cancer. 2009; 9: 202.
19. Ma Y, Liu W, Peng J, Huang L, Zhang P, Zhao X, Cheng Y, Qin H. A pilot study of gas chromatograph/mass spectrometry-based serum metabolic profiling of colorectal cancer after operation. Mol Biol Rep. 2010; 37(3): 1403-1411.
20. Zhao Y, Butler EB, Tan M. Targeting cellular metabolism to improve cancer therapeutics. Cell Death Dis. 2013; 4: 532.
21. McGraw TE, Mittal V. Stem cells: Metabolism regulates differentiation. Nat Chem Biol. 2010; 6(3): 176-177.
22. Qiu Y, Cai G, Su M, Chen T, Zheng X, Xu Y, Ni Y, Zhao A, Xu LX, Cai S, Jia W. Serum metabolite profiling of human colorectal cancer using GC-TOFMS and UPLC-QTOFMS. J Proteome Res. 2009; 8(10): 4844-4850.
23. Zenobi R. Single-cell metabolomics: analytical and biological perspectives. Science. 2013; 342(6163): 1243259.
24. Zhang LZ, Zhang CQ, Yan ZY, Yang QC, Jiang Y, Zeng BF. Tumor-initiating cells and tumor vascularization. Pediatr Blood Cancer. 2011; 56(3): 335-340.
25. Sun Y, Campisi J, Higano C, Beer TM, Porter P, Coleman I, True L, Nelson PS. Treatment-induced damage to the tumor microenvironment promotes prostate cancer therapy resistance through WNT16B. Nat Med. 2012; 18(9): 1359-1368.
26. Ong CW, Kim LG, Kong HH, Low LY, Iacopetta B, Soong R, Salto-Tellez M. CD133 expression predicts for nonresponse to chemotherapy in colorectal cancer. Mod Pathol. 2010; 23(3): 450-457.
27. Ishimoto T, Nagano O, Yae T, Tamada M, Motohara T, Oshima H, Oshima M, Ikeda T, Asaba R, Yagi H, Masuko T, Shimizu T, Ishikawa T, et al. CD44 variant regulates redox status in cancer cells by stabilizing the xCT subunit of system xc(-) and thereby promotes tumor growth. Cancer Cell. 2011; 19(3): 387-400.
28. Urakami K, Zangiacomi V, Yamaguchi K, Kusuhara M. Quantitative metabolome profiling of Illicium anisatum by capillary electrophoresis time-of-flight mass spectrometry. Biomed Res. 2010; 31(2): 161-163.
29. Chen J, Li Y, Yu TS, McKay RM, Burns DK, Kernie SG, Parada LF. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature. 2012; 488(7412): 522-526.
30. Vander Heiden MG, Locasale JW, Swanson KD, Sharfi H, Heffron GJ, Amador-Noguez D, Christofk HR, Wagner G, Rabinowitz JD, Asara JM, Cantley LC. Evidence for an alternative glycolytic pathway in rapidly proliferating cells. Science. 2010; 329(5998): 1492-1499.
31. Ishimoto T, Oshima H, Oshima M, Kai K, Torii R, Masuko T, Baba H, Saya H, Nagano O. CD44+ slow-cycling tumor cell expansion is triggered by cooperative actions of Wnt and prostaglandin E2 in gastric tumorigenesis. Cancer Sci. 2010; 101(3): 673-678.
32. Chen HH, Kuo MT. Role of glutathione in the regulation of cisplatin resistance in cancer chemotherapy. Met Based Drugs. 2010; 2010.
33. Walker JE. The ATP synthase: the understood, the uncertain and the unknown. Biochem Soc Trans. 2013; 41(1): 1-16.
34. Maldonado EN, Lemasters JJ. Warburg revisited: regulation of mitochondrial metabolism by voltage-dependent anion channels in cancer cells. J Pharmacol Exp Ther. 2012; 342(3): 637-641.
35. Johnston PG, Geoffrey F, Drake J, Voeller D, Grem JL, Allegra CJ. The cellular interaction of 5-fluorouracil and cisplatin in a human colon carcinoma cell line. Eur J Cancer. 1996; 32A(12): 2148-2154.
36. Kreso A, van Galen P, Pedley NM, Lima-Fernandes E, Frelin C, Davis T, Cao L, Baiazitov R, Du W, Sydorenko N, Moon YC, Gibson L, Wang Y, et al. Self-renewal as a therapeutic target in human colorectal cancer. Nat Med. 2014; 20(1): 29-36.
37. Paldino E, Tesori V, Casalbore P, Gasbarrini A, Puglisi MA. Tumor initiating cells and chemoresistance: which is the best strategy to target colon cancer stem cells? Biomed Res Int. 2014; 2014: 859871.
38. Hitosugi T, Kang S, Vander Heiden MG, Chung TW, Elf S, Lythgoe K, Dong S, Lonial S, Wang X, Chen GZ, Xie J, Gu TL, Polakiewicz RD, et al. Tyrosine phosphorylation inhibits PKM2 to promote the Warburg effect and tumor growth. Sci Signal. 2009; 2(97): 73.
39. Kee HJ, Cheong JH. Tumor bioenergetics: an emerging avenue for cancer metabolism targeted therapy. BMB Rep. 2014; 47(3): 158-166.
40. Liu Y, Han ZP, Zhang SS, Jing YY, Bu XX, Wang CY, Sun K, Jiang GC, Zhao X, Li R, Gao L, Zhao QD, Wu MC, et al. Effects of inflammatory factors on mesenchymal stem cells and their role in the promotion of tumor angiogenesis in colon cancer. J Biol Chem. 2011; 286(28): 25007-25015.
41. Kincade PW. Plasticity of supporting cells in a stem cell factory. Immunity. 2010; 33(3): 291-293.
42. Hirayama A, Kami K, Sugimoto M, Sugawara M, Toki N, Onozuka H, Kinoshita T, Saito N, Ochiai A, Tomita M, Esumi H, Soga T. Quantitative metabolome profiling of colon and stomach cancer microenvironment by capillary electrophoresis time-of-flight mass spectrometry. Cancer Res. 2009; 69(11): 4918-4925.
43. Hartmann M, Zimmermann D, Nolte J. Changes of the metabolism of the colon cancer cell line SW-480 under serum-free and serum-reduced growth conditions. In Vitro Cell Dev Biol Anim. 2008; 44(10): 458-463.
44. Magee JA, Piskounova E, Morrison SJ. Cancer stem cells: impact, heterogeneity, and uncertainty. Cancer Cell. 2012; 21(3): 283-296.
45. Sugihara E, Saya H. Complexity of cancer stem cells. Int J Cancer. 2013; 132(6): 1249-1259.
46. Yu JW, Zhang P, Wu JG, Wu SH, Li XQ, Wang ST, Lu RQ, Ni XC, Jiang BJ. Expressions and clinical significances of CD133 protein and CD133 mRNA in primary lesion of gastric adenocarcinoma. J Exp Clin Cancer Res. 2010; 29: 141.
47. Kemper K, Sprick MR, de Bree M, Scopelliti A, Vermeulen L, Hoek M, Zeilstra J, Pals ST, Mehmet H, Stassi G, Medema JP. The AC133 epitope, but not the CD133 protein, is lost upon cancer stem cell differentiation. Cancer Res. 2010; 70(2): 719-729.
48. Zangiacomi V, Balon N, Maddens S, Lapierre V, Tiberghien P, Schlichter R, Versaux-Botteri C, Deschaseaux F. Cord blood-derived neurons are originated from CD133+/CD34 stem/progenitor cells in a cell-to-cell contact dependent manner. Stem Cells Dev. 2008; 17(5): 1005-1016.
49. Beier CP, Beier D. CD133 negative cancer stem cells in glioblastoma. Front Biosci. 2011; 3: 701-710.
50. Sampetrean O, Saya H. Characteristics of glioma stem cells. Brain Tumor Pathol. 2013; 30(4): 209-214.