The metabolic state of cancer stem cells - A valid target for cancer therapy?

Free Radical Biology and Medicine

Volumn 79, Issue , 2015, Pages 264-268

  Vlashi, Erina ^a   Pajonk, Frank ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cancer stem cells; Free radicals; Glycolysis; Oxidative phosphorylation; Radiation

Indexed keywords

CANCER CELL METABOLISM; CANCER STEM CELL; CANCER THERAPY; CELL HETEROGENEITY; CELL METABOLISM; CELL POPULATION; CLINICAL TRIAL (TOPIC); CLONAL EVOLUTION; ENERGY YIELD; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; GLYCOLYSIS; HUMAN; MOLECULARLY TARGETED THERAPY; NONHUMAN; OUTCOME ASSESSMENT; OXIDATIVE PHOSPHORYLATION; OXYGEN THERAPY; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; REVIEW; TARGET CELL; THERAPY EFFECT; TISSUE SURVIVAL; WARBURG EFFECT; METABOLISM; NEOPLASMS; PATHOLOGY;

OXYGEN;

HUMANS; NEOPLASMS; NEOPLASTIC STEM CELLS; OXYGEN;

EID: 84923227126     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2014.10.732     Document Type: Review

References (63)

1. M. Al-Hajj, M.S. Wicha, A. Benito-Hernandez, S.J. Morrison, and M.F. Clarke Prospective identification of tumorigenic breast cancer cells Proc. Natl. Acad. Sci. USA 100 2003 3983 3988
2. S. Bao, Q. Wu, R.E. McLendon, Y. Hao, Q. Shi, A.B. Hjelmeland, M.W. Dewhirst, D.D. Bigner, and J.N. Rich Glioma stem cells promote radioresistance by preferential activation of the DNA damage response Nature 444 2006 756 760
3. J.A. Bonner, P.M. Harari, J. Giralt, N. Azarnia, D.M. Shin, R.B. Cohen, C.U. Jones, R. Sur, D. Raben, and J. Jassem Radiotherapy plus cetuximab for squamous-cell carcinoma of the head and neck N. Engl. J. Med. 354 2006 567 578
4. M. Cazzaniga, A. DeCensi, G. Pruneri, M. Puntoni, L. Bottiglieri, C. Varricchio, A. Guerrieri-Gonzaga, O.D. Gentilini, G. Pagani, and P. Dell'Orto The effect of metformin on apoptosis in a breast cancer presurgical trial Br. J. Cancer 109 2013 2792 2797
5. C.L. Chaffer, I. Brueckmann, C. Scheel, A.J. Kaestli, P.A. Wiggins, L.O. Rodrigues, M. Brooks, F. Reinhardt, Y. Su, and K. Polyak Normal and neoplastic nonstem cells can spontaneously convert to a stem-like state Proc. Natl. Acad. Sci. USA 108 2011 7950 7955
6. P.B. Chapman, A. Hauschild, C. Robert, J.B. Haanen, P. Ascierto, J. Larkin, R. Dummer, C. Garbe, A. Testori, and M. Maio Improved survival with vemurafenib in melanoma with BRAF V600E mutation N. Engl. J. Med. 364 2011 2507 2516
7. H.R. Christofk, M.G. Vander Heiden, M.H. Harris, A. Ramanathan, R.E. Gerszten, R. Wei, M.D. Fleming, S.L. Schreiber, and L.C. Cantley The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth Nature 452 2008 230 233
8. H.R. Christofk, M.G. Vander Heiden, N. Wu, J.M. Asara, and L.C. Cantley Pyruvate kinase M2 is a phosphotyrosine-binding protein Nature 452 2008 181 186
9. J. Cohnheim Congenitales, quergestreiftes Muskelsarkom der Nieren Virch. Arch. Pathol. Anat. Physiol. Klin. Med 65 1875 64 69
10. A.T. Collins, P.A. Berry, C. Hyde, M.J. Stower, and N.J. Maitland Prospective identification of tumorigenic prostate cancer stem cells Cancer Res. 65 2005 10946 10951
11. N.M. Davis, M. Sokolosky, K. Stadelman, S.L. Abrams, M. Libra, S. Candido, F. Nicoletti, J. Polesel, R. Maestro, and A. D'Assoro Deregulation of the EGFR/PI3K/PTEN/Akt/mTORC1 pathway in breast cancer: possibilities for therapeutic intervention Oncotarget 5 2014 4603 4650
12. A. Eramo, F. Lotti, G. Sette, E. Pilozzi, M. Biffoni, A. Di Virgilio, C. Conticello, L. Ruco, C. Peschle, and R. De Maria Identification and expansion of the tumorigenic lung cancer stem cell population Cell Death Differ. 15 2007 504 514
13. J.M. Evans, L.A. Donnelly, A.M. Emslie-Smith, D.R. Alessi, and A.D. Morris Metformin and reduced risk of cancer in diabetic patients BMJ 330 2005 1304 1305
14. W. Feng, A. Gentles, R.V. Nair, M. Huang, Y. Lin, C.Y. Lee, S. Cai, F.A. Scheeren, A.H. Kuo, and M. Diehn Targeting unique metabolic properties of breast tumor initiating cells Stem Cells 32 2014 1734 1745
15. C.M. Fillmore, and C. Kuperwasser Human breast cancer cell lines contain stem-like cells that self-renew, give rise to phenotypically diverse progeny and survive chemotherapy Breast Cancer Res. 10 2008 R25
16. W.A. Flavahan, Q. Wu, M. Hitomi, N. Rahim, Y. Kim, A.E. Sloan, R.J. Weil, I. Nakano, J.N. Sarkaria, and B.W. Stringer Brain tumor initiating cells adapt to restricted nutrition through preferential glucose uptake Nat. Neurosci. 16 2013 1373 1382
17. L. Ghisolfi, A.C. Keates, X. Hu, D.K. Lee, and C.J. Li Ionizing radiation induces stemness in cancer cells PLoS One 7 2012 e43628
18. C. Ginestier, M.H. Hur, E. Charafe-Jauffret, F. Monville, J. Dutcher, M. Brown, J. Jacquemier, P. Viens, C.G. Kleer, and S. Liu ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome Cell Stem Cell 1 2007 555 567
19. E. Giovannucci, D.M. Harlan, M.C. Archer, R.M. Bergenstal, S.M. Gapstur, L.A. Habel, M. Pollak, J.G. Regensteiner, and D. Yee Diabetes and cancer: a consensus report Diabetes Care 33 2010 1674 1685
20. G.G. Graham, J. Punt, M. Arora, R.O. Day, M.P. Doogue, J.K. Duong, T.J. Furlong, J.R. Greenfield, L.C. Greenup, and C.M. Kirkpatrick Clinical pharmacokinetics of metformin Clin. Pharmacokinet. 50 2011 81 98
21. P.B. Gupta, T.T. Onder, G. Jiang, K. Tao, C. Kuperwasser, R.A. Weinberg, and E.S. Lander Identification of selective inhibitors of cancer stem cells by high-throughput screening Cell 138 2009 645 659
22. H.D. Hemmati, I. Nakano, J.A. Lazareff, M. Masterman-Smith, D.H. Geschwind, M. Bronner-Fraser, and H.I. Kornblum Cancerous stem cells can arise from pediatric brain tumors Proc. Natl. Acad. Sci. USA 100 2003 15178 15183
23. C.C. Huang, Z. Liu, X. Li, S.K. Bailey, C.D. Nail, K.W. Foster, A.R. Frost, J.M. Ruppert, and S.M. Lobo-Ruppert KLF4 and PCNA identify stages of tumor initiation in a conditional model of cutaneous squamous epithelial neoplasia Cancer Biol. Ther. 4 2005 1401 1408
24. D.A. Iglesias, M.S. Yates, D. van der Hoeven, T.L. Rodkey, Q. Zhang, N.N. Co, J. Burzawa, S. Chigurupati, J. Celestino, and J. Bowser Another surprise from metformin: novel mechanism of action via K-Ras influences endometrial cancer response to therapy Mol. Cancer Ther. 12 2013 2847 2856
25. J.W. Jung, S.B. Park, S.J. Lee, M.S. Seo, J.E. Trosko, and K.S. Kang Metformin represses self-renewal of the human breast carcinoma stem cells via inhibition of estrogen receptor-mediated OCT4 expression PLoS One 6 2011 e28068
26. K. Kalinsky, K.D. Crew, S. Refice, T. Xiao, A. Wang, S.M. Feldman, B. Taback, A. Ahmad, S. Cremers, and H. Hibshoosh Presurgical trial of metformin in overweight and obese patients with newly diagnosed breast cancer Cancer Invest. 32 2014 150 157
27. C. Lagadec, E. Vlashi, S. Bhuta, C. Lai, P. Mischel, M. Werner, M. Henke, and F. Pajonk Tumor cells with low proteasome subunit expression predict overall survival in head and neck cancer patients BMC Cancer 14 2014 152
28. C. Lagadec, E. Vlashi, L. Della Donna, C. Dekmezian, and F. Pajonk Radiation-induced reprogramming of breast cancer cells Stem Cells 30 2012 833 844
29. C. Lagadec, E. Vlashi, L. Della Donna, and F. Pajonk The response of breast cancer initiating cells to fractionated radiation Cancer Res. 69 2009 587S (-587S)
30. E.D. Lagadinou, A. Sach, K. Callahan, R.M. Rossi, S.J. Neering, M. Minhajuddin, J.M. Ashton, S. Pei, V. Grose, and K.M. O'Dwyer BCL-2 inhibition targets oxidative phosphorylation and selectively eradicates quiescent human leukemia stem cells Cell Stem Cell 12 2013 329 341
31. T. Lapidot, C. Sirard, J. Vormoor, B. Murdoch, T. Hoang, J. Caceres-Cortes, M. Minden, B. Paterson, M.A. Caligiuri, and J.E. Dick A cell initiating human acute myeloid leukaemia after transplantation into SCID mice Nature 367 1994 645 648
32. P.P. Liu, J. Liao, Z.J. Tang, W.J. Wu, J. Yang, Z.L. Zeng, Y. Hu, P. Wang, H.Q. Ju, and R.H. Xu Metabolic regulation of cancer cell side population by glucose through activation of the Akt pathway Cell Death Differ. 21 2014 124 135
33. S. Liu, Y. Cong, D. Wang, Y. Sun, L. Deng, Y. Liu, R. Martin-Trevino, L. Shang, S.P. McDermott, and M.D. Landis Breast cancer stem cells transition between epithelial and mesenchymal states reflective of their normal counterparts Stem Cell Rep 2 2014 78 91
34. P.C. Nowell The clonal evolution of tumor cell populations Science 194 1976 23 28
35. C. Oliveras-Ferraros, A. Vazquez-Martin, and J.A. Menendez Pharmacological mimicking of caloric restriction elicits epigenetic reprogramming of differentiated cells to stem-like self-renewal states Rejuvenation Res 13 2010 519 526
36. R. Palorini, G. Votta, C. Balestrieri, A. Monestiroli, S. Olivieri, R. Vento, and F. Chiaradonna Energy metabolism characterization of a novel cancer stem cell-like line 3AB-OS J. Cell. Biochem. 115 2014 368 379
37. A.Y. Pandya, L.I. Talley, A.R. Frost, T.J. Fitzgerald, V. Trivedi, M. Chakravarthy, D.C. Chhieng, W.E. Grizzle, J.A. Engler, H. Krontiras Nuclear localization of KLF4 is associated with an aggressive phenotype in early-stage breast cancer Clin. Cancer Res. 10 2004 2709 2719
38. T.M. Phillips, W.H. McBride, and F. Pajonk The response of CD24(-/low)/CD44+ breast cancer-initiating cells to radiation J. Natl. Cancer Inst. 98 2006 1777 1785
39. D. Ponti, A. Costa, N. Zaffaroni, G. Pratesi, G. Petrangolini, D. Coradini, S. Pilotti, M.A. Pierotti, and M.G. Daidone Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties Cancer Res. 65 2005 5506 5511
40. M.E. Prince Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma Proc. Natl. Acad. Sci. USA 104 2007 973 978
41. E. Quintana, M. Shackleton, M.S. Sabel, D.R. Fullen, T.M. Johnson, and S.J. Morrison Efficient tumour formation by single human melanoma cells Nature 456 2008 593 598
42. E. Racker, and M. Spector Warburg effect revisited: merger of biochemistry and molecular biology Science 213 1981 303 307
43. T. Reya, S.J. Morrison, M.F. Clarke, and I.L. Weissman Stem cells, cancer, and cancer stem cells Nature 414 2001 105 111
44. L. Ricci-Vitiani, D.G. Lombardi, E. Pilozzi, M. Biffoni, M. Todaro, C. Peschle, and R. De Maria Identification and expansion of human colon-cancer-initiating cells Nature 445 2007 111 115
45. K. Salmina, E. Jankevics, A. Huna, D. Perminov, I. Radovica, T. Klymenko, A. Ivanov, E. Jascenko, H. Scherthan, and M. Cragg Up-regulation of the embryonic self-renewal network through reversible polyploidy in irradiated p53-mutant tumour cells Exp. Cell Res. 316 2010 2099 2112
46. T. Schatton, G.F. Murphy, N.Y. Frank, K. Yamaura, A.M. Waaga-Gasser, M. Gasser, Q. Zhan, S. Jordan, L.M. Duncan, and C. Weishaupt Identification of cells initiating human melanomas Nature 451 2008 345 349
47. A.J. Scheen Clinical pharmacokinetics of metformin Clin. Pharmacokinet. 30 1996 359 371
48. S.K. Singh, I.D. Clarke, M. Terasaki, V.E. Bonn, C. Hawkins, J. Squire, and P.B. Dirks Identification of a cancer stem cell in human brain tumors Cancer Res. 63 2003 5821 5828
49. M.M. Ter-Pogossian, M.E. Phelps, E.J. Hoffman, and N.A. Mullani A positron-emission transaxial tomograph for nuclear imaging (PETT) Radiology 114 1975 89 98
50. K.K. Tsilidis, D. Capothanassi, N.E. Allen, E.C. Rizos, D.S. Lopez, K. van Veldhoven, C. Sacerdote, D. Ashby, P. Vineis, and I. Tzoulaki Metformin does not affect cancer risk: a cohort study in the U.K. clinical practice research datalink analyzed like an intention-to-treat trial Diabetes Care 37 2014 2522 2532
51. M.G. Vander Heiden, L.C. Cantley, and C.B. Thompson Understanding the Warburg effect: the metabolic requirements of cell proliferation Science 324 2009 1029 1033
52. R. Virchow Cellular-Pathologie Arch. Pathol. Anat. Physiol. Klin. Med 8 1855 3 39
53. E. Vlashi, K. Kim, C. Lagadec, L.D. Donna, J.T. McDonald, M. Eghbali, J.W. Sayre, E. Stefani, W. McBride, and F. Pajonk In vivo imaging, tracking, and targeting of cancer stem cells J. Natl. Cancer Inst. 101 2009 350 359
54. E. Vlashi, C. Lagadec, M. Chan, P. Frohnen, A.J. McDonald, and F. Pajonk Targeted elimination of breast cancer cells with low proteasome activity is sufficient for tumor regression Breast Cancer Res. Treat. 141 2013 197 203
55. E. Vlashi, C. Lagadec, L. Vergnes, T. Matsutani, K. Masui, M. Poulou, R. Popescu, L. Della Donna, P. Evers, and C. Dekmezian Metabolic state of glioma stem cells and nontumorigenic cells Proc. Natl. Acad. Sci. USA 108 2011 16062 16067
56. E. Vlashi, C. Lagadec, L. Vergnes, K. Reue, P. Frohnen, M. Chan, Y. Alhiyari, M.B. Dratver, and F. Pajonk Metabolic differences in breast cancer stem cells and differentiated progeny Breast Cancer Res. Treat. 146 2014 525 534
57. O. Warburg Tests on surviving carcinoma cultures Biochem. Z. 142 1923 317 333
58. O. Warburg On the formation of lactic acid with growth Biochem. Z. 160 1925 307 311
59. O. Warburg, K. Posener, and E. Negelein Ueber den Stoffwechsel der Tumoren Biochem. Z. 152 1924 319 344
60. O. Warburg, F. Wind, and E. Negelein The metabolism of tumors in the body J. Gen. Physiol. 8 1927 519 530
61. S. Weinhouse On respiratory impairment in cancer cells Science 124 1956 267 269
62. W.A. Woodward, M.S. Chen, F. Behbod, M.P. Alfaro, T.A. Buchholz, and J.M. Rosen WNT/beta-catenin mediates radiation resistance of mouse mammary progenitor cells Proc. Natl. Acad. Sci. USA 104 2007 618 623
63. X.L. Zu, and M. Guppy Cancer metabolism: facts, fantasy, and fiction Biochem. Biophys. Res. Commun. 313 2004 459 465