Crosstalk between the Warburg effect, redox regulation and autophagy induction in tumourigenesis

• Autorzy: Gwangwa M.V. , Joubert A.M. , Visagie M.
• Języki publikacji: EN

Abstrakty

EN

Tumourigenic tissue uses modified metabolic signalling pathways in order to support hyperproliferation and survival. Cancer-associated aerobic glycolysis resulting in lactic acid production was described nearly 100 years ago. Furthermore, increased reactive oxygen species (ROS) and lactate quantities increase metabolic, survival and proliferation signalling, resulting in increased tumourigenesis. In order to maintain redox balance, the cell possesses innate antioxidant defence systems such as superoxide dismutase, catalase and glutathione. Several stimuli including cells deprived of nutrients or failure of antioxidant systems result in oxidative stress and cell death induction. Among the cell death machinery is autophagy, a compensatory mechanism whereby energy is produced from damaged and/or redundant organelles and proteins, which prevents the accumulation of waste products, thereby maintaining homeostasis. Furthermore, autophagy is maintained by several pathways including phosphoinositol 3 kinases, the mitogen-activated protein kinase family, hypoxia-inducible factor, avian myelocytomatosis viral oncogene homolog and protein kinase receptor-like endoplasmic reticulum kinase. The persistent potential of cancer metabolism, redox regulation and the crosstalk with autophagy in scientific investigation pertains to its ability to uncover essential aspects of tumourigenic transformation. This may result in clinical translational possibilities to exploit tumourigenic oxidative status and autophagy to advance our capabilities to diagnose, monitor and treat cancer.

• Wydawca: -
• Czasopismo: Cellular and Molecular Biology Letters
• Rocznik: 2018
• Tom: 23
• Opis fizyczny: p.1-19,fig.,ref.

Twórcy

autor

Gwangwa M.V.

• Department of Physiology, Faculty of Health Sciences, University of Pretoria, Private Bag X323, Arcadia 0007, South Africa

autor

Joubert A.M.

• Department of Physiology, Faculty of Health Sciences, University of Pretoria, Private Bag X323, Arcadia 0007, South Africa

autor

Visagie M.

• Department of Physiology, Faculty of Health Sciences, University of Pretoria, Private Bag X323, Arcadia 0007, South Africa

Bibliografia

• 1. Wu M, Neilson A, Swift AL, Moran R, Tamagnine J, Parsklow D, et al. Multiparameter metabolic analysis reveals a close link between attenuated mitochondrial bioenergetics function and enhanced glycolysis dependency in human tumor cells. Am J Physiol Cell Physiol. 2007;292:C125–36.
• 2. Fu X, Hu X, Li N, Zheng F, Dong X, Duan J, et al. Glutamine and glutaminolysis are required for efficient replication of infectious spleen and kidney necrosis virus in Chinese perch brain cells. Oncotarget. 2017;8(2): 2400–12.
• 3. Christofk HR, van der Heiden MG, Harris MH, Ramanathan A, Gerszten RE, Wei R, et al. The M2 splice isoform and pyruvate kinase is important for cancer metabolism and tumour growth. Nature. 2008;452:230–4.
• 4. Zhu C, Martinez AF, Martin HL, Li M, Crouch BT, Carlson DA, et al. Near-simultaneous intravital microscopy of glucose uptake and mitochondrial membrane potential, key endpoints that reflect major metabolic axes in cancer. Sci Rep. 2017;7:13722.
• 5. Koppenol WH, Bounds PL, Dang CV. Otto Warburg’s contributions to current concepts of cancer metabolism. Nat Rev Cancer. 2011;11(5):325–37.
• 6. Chung FY, Huang MY, Yeh CS, Chang HJ, Cheng TL, Yen LC, et al. GLUT1 gene is a potential hypoxic marker in colorectal cancer patients. BMC Cancer. 2009;9:241.
• 7. Wang J, Ye C, Chen C, Xiong H, Xie B, Zhou J. Glucose transporter GLUT1 expression and clinical outcome in solid tumours: a systematic review and meta-analysis. Oncotarget. 2017;8(10):16875–86.
• 8. Bravata V, Stefano A, Cammarata FP, Minafra L, Russo G, Nicolosi S, et al. Genotyping analysis and (1)(8)FDG uptake in breast cancer patients: a preliminary research. J Exp Clin Cancer Res. 2013;32:23.
• 9. Lee EE, Ma J, Sacharidou A, Mi W, Salato VK, Nguyen N, et al. A protein kinase C phosphorylation motif in Glut1 affects glucose transport and is mutated in glut 1 deficiency syndrome. Mol Cell. 2015;58(5):875–53.
• 10. Gaglio D, Metallo CM, Gameiro PA, Hiller K, Danna LS, Belestrieri C, et al. Oncogenic K-ras decouples glucose and glutamine metabolism to support cancer cell growth. Mol Syst Biol. 2011;7:523.
• 11. Keibler MA, Wasylenko TM, Kelleher JK, Iliopoulos O, van der Heiden MG, Stephanopoulos G. Metabolic requirements for cancer cell proliferation. Cancer Metab. 2016;4:16.
• 12. Schulz TJ, Thierbach R, Voigt A, Drewes G, Mietzner B, Steinberg P, et al. Induction of oxidative metabolism by mitochondrial frataxin inhibits cancer growth Otto Warburg revisited. J Biol Chem. 2005;281:977–81.
• 13. Kroemer G, Pouyssegur J. Tumor cell metabolism: cancer’s Achilles’ heel. Cancer Cell. 2008;13:472–82.
• 14. Schwartz L, Seyfried T, Alfarouk KO, Da Veiga MJ, Fais S. Out of Warburg effect: an affective cancer treatment targeting the tumour specific metabolism and dysregulated pH. Semin Cancer Biol. 2017;43:134–8.
• 15. Höckel M, Vaupel P. Tumour hypoxia: definitions and current clinical, biological, and molecular aspects. J Natl Cancer Inst. 2001;93:266–76.
• 16. Estrella V, Chen T, Lloyd M, Wojkowiak J, Cornwell HH, Ibrahim-Hashim A, et al. Acidity generated by tumor microenvironment drives local invasion. Cancer Res. 2012;73(5):1524–35.
• 17. Robertson-Tessi M, Gillies RJ, Gatenby RA, Anderson ARA. Impact of metabolic heterogeneity on tumor growth, invasion, and treatment outcomes. Cancer Res. 2015;75(8):1567–79.
• 18. Rodríguez-Lirio A, Pérez-Yarza G, Fernández-Suárez MR, Alonso-Tejerina E, Boyano MD, Asumendi A. Metformin induces cell cycle arrest and apoptosis in drug-resistant leukemia cells. Leuk Res 2015;2015. 516460.
• 19. Chandel NS, Diebold L. Mitochondrial ROS regulation of proliferating cells. Free Radic Biol Med. 2016;100:86–93.
• 20. Poillet-Perez L, Despouy G, Delage-Mourroux R, Boyer-Guittaut M. Interplay between ROS and autophagy in cancer cells, from tumor initiation to cancer therapy. Redox Biol. 2014;4:184–92.
• 21. Turrens JF. Mitochondrial formation of reactive oxygen species. J Physiol. 2003;552:335–44.
• 22. Pérez-Carreras M, Del Hoyo P, Martin MA, Rubio JC, Martin A, Castellano G, et al. Defective heptaic mitochondrial respiratory chain in patients with nonalchoholic steatohepatitis. Hepatology. 2003;38(4):999–1007.
• 23. Schuett J, Schuett H, Oberoi R, Koch A-K, Pretzer S. Luchtefeld, et al. NADPH oxidase NOX2 mediates TLR2/6- dependent release of GM-CSF from endothelial cells. FASEB J. 2017;31(6):2612–24.
• 24. Turrens JF, Alexandre A, Lehninger AL. Ubisemiquinone is the electron acceptor for superoxide formation by complex III of heart mitochondria. Arch Biochem Biophys. 1985;237(2):408–14.
• 25. Sullivan LB, Chandel NS. Mitochondrial reactive oxygen species and cancer. Cancer Metab. 2014;2:17.
• 26. Mantzaris MD, Bellou S, Skiada V, Kitsati V, Fotsis T, Galaris D. Intracellular labile iron determines H2O2-induced apoptotic signaling via sustained activation of ASK1/JNK-p38 axis. Free Radic Biol Med. 2016;97:454–65.
• 27. Nogueira V, Hay N. Molecular pathways: reactive oxygen species homeostasis in cancer cells and implications for cancer therapy. Clin Cancer Res. 2013;19:4309–14.
• 28. Aybastier Õ, Dawbaa S, Demir C, Akgün O, Ulukaya E, Ari F. Quantification of DNA damage products by gas chromatography tandem mass spectrophotometry in lung cell lines and prevention effect of thyme antioxidants on oxidative induced DNA damage. Mutat Res. 2018;808:1–9.
• 29. Szymonik-Lesiuk S, Czechowska G, Stryjecka-Zimmer M, Słomka M, Madro A, Celiński K, et al. Catalase, superoxide dismutase, and glutathione peroxidase activities in various rat tissues after carbon tetrachloride intoxication. J Hepatobiliary Pancreat Sci. 2003; https://doi.org/10.1007/s00534-002-0824-5.
• 30. Anastasiou D, Poulogiannis G, Asara JM, Boxer MB, Jiang J-J, Shen M, et al. Inhibition of pyruvate kinase M2 by reactive oxygen species contribute to cellular antioxidant responses. Science. 2011;334(6060):1278–83.
• 31. Kung C, Hixon J, Choe S, Marks K, Gross S, Murphy E, et al. Small molecule activation of PKM2 in cancer cells induces serine auxotrophy. Chem Biol. 2012;19(9):1187–98.
• 32. Su B-Q, Han Y-Q, Fan S-S, Ming S-L, Wan B, Lu W-F, et al. PKM2 knockdown influences SREBP activation and lipid synthesis in bovine mammary-gland epithelial MAC-T cells. Biotechnol Lett. 2018:1–8.
• 33. Pamell KM, Foulks JM, Nix RN, Clifford A, Bullough J, Luo B, et al. Pharmacologic activation of PKM2 slows lung tumor xenograft growth. Mol Cancer Ther. 2013;12(8):1453–60. Gwangwa et al. Cellular & Molecular Biology Letters (2018) 23:20 Page 16 of 19
• 34. Anastasiou D, Yu Y, Israelsen WJ, Jiang JK, Boxer MB, Hong BS, et al. Pyruvate kinase M2 activators promote tetramer formation and suppress tumorigenesis. Nat Chem Biol. 2012;8:839–47.
• 35. Stortz P. Reactive oxygen species in tumor progression. Front Biosci. 2005;10:1881–96.
• 36. Wang T, Zhang X, Li JJ. The role of NF-kB in the regulation of cell stress responses. Int Immunopharmacol. 2002; 2(1):1509–20.
• 37. Chen AC-H, Arany PR, Huang Y-Y, Tomkinson EM, Sharma SK, Kharkwal GB, et al. Low-level laser therapy activates NF-kB via generation of reactive oxygen species in mouse embryonic fibroblasts. PLoS One. 2011;6(7):e22453.
• 38. Halasi M, Pandit B, Wang M, Nogueira V, Hay H, Gartel A. Combination of oxidative stress and FOXM1 inhibitors induces apoptosis in cancer cells and inhibits xenograft tumor growth. Am J Pathol. 2013;183(1):257–65.
• 39. Yin J, Duan J, Cui Z, Ren W, Li T, Yin Y. Hydrogen peroxide-induced oxidative stress activates NF-kB and NRF2/ Keap1 signals and triggers autophagy in piglets. R Soc Chem. 2015;5:15479–86.
• 40. Izumi H, Takahashi M, Uramoto H, Nakayama Y, Oyama T, Wang K-Y, et al. Monocarboxylate transporters 1 and 4 are involved in the invasion activity of human lung cancer cells. Cancer Sci. 2011;102(5):1007–13.
• 41. Xu K, Mao X, Mehta M, Cui J, Zhang C, Mao F, et al. Elucidation of how cancer cells avoid acidosis through comparative transcriptomic data analysis. PLoS One. 2013;8(8):e71177.
• 42. Semenza GL. Tumor metabolism: cancer cells give and take lactate. J Clin Invest. 2008;118(12):3835–7.
• 43. Sonveaux P, Vegran F, Schroeder T, Wergin MC, Verrax J, Rabbani ZN, et al. Targeting lactate-fueled respiration selectively kills hypoxic tumor cells in mice. J Clin Invest. 2008;118(12):3930–42.
• 44. Yoshida GJ. Metabolic reprogramming: the emerging concept and associated therapeutic strategies. J Exp Clin Cancer Res. 2015; https://doi.org/10.1186/s13046-015-0221-y.
• 45. Pertega-Gomes N, Vizcaino JR, Attig J, Jurmeister S, Lopes C, Baltazar F. A lactate shuttle system between tumour and stromal cells is associated with poor prognosis in prostate cancer. BMC Cancer. 2014;14:352.
• 46. Glick D, Barth S, Macleod KF. Autophagy: cellular and molecular mechanisms. J Pathol. 2010;221:3–12.
• 47. Ozpolat B, Benbrook DM. Targeting autophagy in cancer management – strategies and developments. Cancer Manag Res. 2015;7:291–9.
• 48. Luo M, Zhao X, Song Y, Cheng H, Zhou R. Nuclear autophagy: an evolutionary conserved mechanism of nuclear degradation in the cytoplasm. Autophagy. 2016;12:1973–83.
• 49. Kang R, Zeh HJ, Lotze MT, Tang D. The beclin 1 network regulates autophagy and apoptosis. Cell Death Differ. 2011;18:571–80.
• 50. Liang XH, Jackson S, Seaman M, Brown K, Kempkes B, Hibshoosh H, et al. Induction of autophagy and inhibition of tumorigenesis by beclin1. Nature. 1999;402:672–6.
• 51. Qin JZ, Xin H, Nickoloff BJ. Targeting glutamine metabolism sensitizes melanoma cells to TRAIL-induced death. Biochem Biophys Res Commun. 2010;398:146–52.
• 52. Ezaki J, Matsumoto N, Takeda-Ezaki M, Komatsu M, Takahashi K, Hiraoka Y. Liver autophagy contributes to the maintenance of blood glucose and amino acid levels. Autophagy. 2011;7(7):727–36.
• 53. Popelka H, Uversky VN, Klionsky DJ. Identification of Atg3 as an intrinsically disordered polypeptide yields insights into the molecular dynamics of autophagy-related proteins in yeast. Autophagy. 2014;10:103–14.
• 54. Samara C, Syntichaki P, Tavernarakis N. Autophagy is required for necrotic death in Caenorhabditis elegnas. Cell Death Differ. 2008;15:105–12.
• 55. Wallot-Hieke N, Verma N, Schlütermann D, Derleth N, Deitersen J, Böhler P. Systematic analysis of ATGF13 domain requirements for autophagy induction. Autophagy. 2017; https://doi.org/10.1080/15548627.2017.1387342.
• 56. Liu C-C, Lin Y-C, Chen Y-H, Chen C-M, Pang L-Y, Chen H-A. Cul3-KLHL20 ubiquitin ligase governs the turnover of ULK1 and VS34 complexes to control autophagy termination. Mol Cell. 2016;61:84–97.
• 57. Sengupta S, Peterson TR, Sabatini DM. Regulation of the mTOR complex 1 pathway by nutrients, growth factors, and stress. Mol Cell. 2010;40:310–22.
• 58. Kaur A, Sharmna S. Mammalian target of rapamycin (mTOR) as a potential therapeutic target in various diseases. Immunopharmacology. 2017;25:293–312.
• 59. Zou Z, Chen J, Yang J, Bai X. Targeted inhibition of rictor/mTORC2 in cancer treatment: a new era after rapamycin. Curr Cancer Drug Targets. 2016;16:288–304.
• 60. Saxton RA, Sabatini DM. mTOR signaling in growth, metabolism, and disease. Cell. 2017;168:960–76.
• 61. Durán RV, Oppliger W, Robitaille AM, Heiserich L, Skendaj R, Gottlieb E, et al. Glutaminolysis activates Rag-mTORC1 signaling. Mol Cell. 2012;47(3):649–358.
• 62. Nagelkerke A, Sweep FCGJ, Geurts-Moespot A, Bussink J, Span PN. Therapeutic targeting of autophagy in cancer. Part I: molecular pathways controlling autophagy. Semin Cancer Biol. 2014;16:26–36.
• 63. Jewell JL, Guan K-L. Differential regulation of mTORC1 by leucine and glutamine. Science. 2015;347(6218):194–8.
• 64. Shen K, Choe A, Sabatini DM. Intersubunit crosstalk in the rag GTPase heterodimer enables mTORC1 to respond rapidly to amino acid availability. Mol Cell. 2017;38(3):552–65.
• 65. Shanware NP, Bray K, Abraham RT. The PI3K, metabolic, and autophagy networks: interactive partners in cellular health and disease. Ann Rev Pharmacol Toxicol. 2013;53:89–106.
• 66. Comb WC, Hutti JE, Cogswell P, Cantley LC, Baldwin AS. P85α SH2 domain phosphorylation by IKK promotes feedback inhibition of PI3K and Akt in response to cellular starvation. Mol Cell. 2012;45:719–30.
• 67. Takeuchi H, Kondo Y, Fujiwara K, Kanzawa T, Aoki H, Mills GB, et al. Synergistic augmentation of rapamycin-induced autophagy in malignant glioma cells by phosphatidylinositol 3-kinase/protein kinase B inhibitors. Cancer Res. 2005;65(8):3336–46.
• 68. Scrima M, De Marco C, Fabiana F, Franco R, Pirrozzi G, Rocco G, et al. Signaling networks associated with AKT activation in non-small cell lung cancer (NSCLC): new insights on the role of phosphatydil-inositol-3 kinase. PLoS One. 2012;7(2):e30427.
• 69. Saiki S, Sasazawa Y, Imamichi Y, Kawajiri S, Fujimaki T, Tanida I, et al. Caffeine induces apoptosis by enhancement of autophagy via PI3K/Akt/mTOR/p70S6K inhibition. Autophagy. 2011;7:176–87.
• 70. Netland IA, Forde HE, Sleire L, Leiss L, Rahman MA, Skeie BS. Dactolisib (NVP-BEZ235) toxicity in murine brain tumour models. BMC Cancer. 2016;16:657. Gwangwa et al. Cellular & Molecular Biology Letters (2018) 23:20
• 71. Lu Y, Wang Q, Fan S, Hu B, Sun L, Xue H, et al. Effective use of PI3K inhibitor BKM120 to treat human osteosarcoma. Int J Clin Exp Med. 2017;10:6378–86.
• 72. Bohnacker T, Prota AE, Beaufils F, Burke JE, Melone A, Inglis AJ. Deconvolution of Buparlisib’s mechanism of action defines specific PI3K and tubulin inhibitors for therapeutic intervention. Nat Commun. 2017;8:14683.
• 73. Sui X, Kong N, Ye L, Han W, Zhou J, Zhang Q, et al. P38 and JNK MAPK pathways control the balance of apoptosis and autophagy in response to chemotherapeutic agents. Cancer Lett. 2014;344:174–9.
• 74. Mendoza MC, Er EE, Blenis J. The Ras-ERK and PI3K-mTOR pathways : crosstalk and compensation. Trends Biochem Sci. 2011;36:320–8.
• 75. Ray PD, Huang B-W, Tsuji Y. Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal. 2012;24:981–90.
• 76. Baregamian N, Song J, Bailey CE, Papaconstantinou J, Evers BM, Chung DH. Tumor necrosis factor-α and apoptosis signal-regulating kinase 1 control reactive oxygen species release, mitochondrial autophagy and c-Jun N-terminal kinase p38 phosphorylation during necrotizing enterocolitis. Oxidative Med Cell Longev. 2009;2:297–306.
• 77. Davies C, Tournier C. Exploring the function of the JNK ( c-Jun N-terminal kinase) signalling pathway in physiological and pathological processes to design novel therapeutic strategies. Biochem Soc Trans. 2012;40:85–96.
• 78. Houde VP, Donzelli S, Sacconi A, Galic S, Hammill JA, Bramson JL, et al. AMPK β1 reduces tumour progression and improves survival in p53-null mice. Mol Oncol. 2017;11(9):1143–55.
• 79. Zhang D, Wang L, Yan L, Miao X, Gong C, Xiao M, et al. Vacuolar protein sorting 4B regulates apoptosis of intestinal epithelial cells via p38 MAPK in Crohn’s disease. Exp Mol Pathol. 2015;98:55–64.
• 80. Li L, Chen Y, Gibson SB. Starvation-induced autophagy is regulated by mitochondrial reactive oxygen species leading to AMPK activation. Cell Signal. 2013;25:50–65.
• 81. Law BYK, Mok SWF, Chan WK, Xu SW, Wu AG, Yao XJ, et al. Hernandezine, a novel AMPK activator induces autophagic cell death in drug resistant cancers. Oncotarget. 2016;7:8090–104.
• 82. Orlotti NI, Cimino-Reale G, Borghini E, Pennati M, Sissi C, Perronne F, et al. Autophagy acts as a safeguard mechanism against G-quadruplex ligand-mediated DNA damage. Autophagy. 2012;8(8):1185–96.
• 83. Alexander A, Chai S-L, Kim J, Nanaez A, Sahin M, MacLean KH, et al. ATM signals to TSC2 in the cytoplasm to regulate mTORC1 in response to ROS. Proc Natl Acad Sci. 2010;107:4153–8.
• 84. Yoshida GJ. Therapeutic strategies of drug repositioning targeting autophagy to induce cancer cell death: from pathophysiology to treatment. J Hematol Oncol. 2017;10(1):67.
• 85. Phan LM, Yeung SC, Lee MH. Cancer metabolic reprogramming: importance, main features, and potentials for precise targeted anti-cancer therapies. Cancer Biol Med 2014;11(1):1–19.
• 86. Hardie DG. AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat Rev Mol Cell Biol. 2007;8(10):774–85.
• 87. Joungmok K, Kundu M, Viollet B, Guan K-L. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol. 2010;13:132–41.
• 88. Hardie DG, Ross FA, Hawley SA. AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat Rev Mol Cell Biol. 2012;13(4):251–62.
• 89. Egan DF, et al. Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science. 2011;331:456–61.
• 90. Rouschop KMA, Ramaekers CHMA, Schaaf MBE, Keulers TGH, Savelkouls GM, Lambin P, et al. Autophagy is required during hypoxia to lower production of reactive oxygen species. Radiother Oncol. 2009;92:411–6.
• 91. Saito S, Lin Y-C, Tsai M-H, Lin C-S, Murayama Y, Sato R, et al. Emerging roles of hypoxia-inducible factors and reactive oxygen species in cancer and pluripotent stem cells. Kaohsiung J Med Sci. 2015;31:1–8.
• 92. Semenza GL. Hif-1: upstream and downstream of cancer metabolism. Curr Opin Genet Dev. 2010;20:51–6.
• 93. Gerlinger M, Rowan AJ, Horswell S, et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med. 2012;366:883–92.
• 94. Yoshida GJ, Saya H. Therapeutic strategies targeting cancer stem cells. Cancer Sci. 2016;107(1):5–11.
• 95. Yoshida GJ, Saya H. EpCAM expression in the prostate cancer makes the difference in the response to growth factors. Biochem Biophys Res Commun. 2014;443(1):239–45.
• 96. Klein CA, Blankenstein TJF, Schmidt-Kittler O, Petronio M, Polzer B, Stoecklein NH, et al. Genetic heterogeneity of single disseminated tumour cells in minimal residual cancer. Lancet. 2002;360(9334):683–9.
• 97. Bischof J, Westhoff MA, Wagner JE, Halatsch M-E, Trentmann S, Knippschild U, et al. Cancer stem cells: the potential role of autophagy, proteolysis, and cathepsins in glioblastoma stem cells. Tumour Biol. 2017:1–13.
• 98. Nguyen LV, Vanner R, Dirks P, Eaves CJ. Cancer stem cells: an evolving concept. Nat Rev Cancer. 2012;12:133–43.
• 99. Jiang X, Gwye Y, Russell D, Cao C, Douglas D, Hung L, et al. CD133 expression in chemo-resistant Ewing sarcoma cells. BMC Cancer. 2010;10:116.
• 100. Fan F, Bellister S, Lu J, Ye X, Boulbes DR, Tozzi F, et al. The requirement for freshly isolated colorectal cancer (CRC) cells in isolating CRC stem cells. Br J Cancer. 2015;112:539–46.
• 101. Peiris-Pagè M, Martinez-Outschoorn UE, Pestell RG, Sotgia F, Lisanti MP. Cancer stem cell metabolism. Breast Cancer Res. 2016;18:55.
• 102. De Luca A, Fiorillo M, Peiris-Pages M, Ozsvari B, Smith DL, Sanchez-Alvarez R, et al. Mitochondrial biogenesis is required for the anchorage-independent survival and propagation of stem-like cancer cells. Oncotarget. 2015; 6(17):14777–95.
• 103. Lamb R, Bonuccelli G, Ozsvari B, Peiris-Pages M, Fiorillo M, Smith DL, et al. Mitochondrial mass, a new metabolic biomarker for stem-like cancer cells: understanding WNT/FGF-driven anabolic signaling. Oncotarget. 2015;6(31):30453–71.
• 104. Vlashi E, Lagadec C, Vergnes L, Reue K, Frohnen P, Chan M, et al. Metabolic differences in breast cancer stem cells and differentiated progeny. Breast Cancer Res Treat. 2014;146(3):525–34.
• 105. Farnie G, Sotgia F, Lisanti MP. High mitochondrial mass identifies a sub-population of stem-like cancer cells that are chemo-resistant. Oncotarget. 2015;6(31):30472–86.
• 106. Liu P-P, Liao J, Tang Z-J, Wu W-J, Yang J, Zeng ZL. Metabolic regulation of cancer cell side population by glucose through activation of the AKT pathway. Cell Death Differ. 2014;21:124–35.
• 107. Cipolleschi MG, Marzi I, Santini R, Fredducci D, Vinci MC, D’Amico M, et al. Hypoxia-resistant profile implies vulnerability of cancer stem cells to physiological agents, which suggests new therapeutic targets. Cell Cycle. 2014;13(2):268–78.
• 108. Mizuno T, Suzuki N, Makino H, Furui T, Morii E, Aoki H, et al. Cancer stem-like cells of ovarian clear cell carcinoma are enriched in the ALDH-high population associated with an accelerated scavenging system in reactive oxygen species. Gynecol Oncol. 2015;137:299–305.
• 109. Kim HM, Haraguchi N, Ishii H, Ohkuma M, Okano M, Mimori K, et al. Increased CD13 expression reduces reactive oxygen species, promoting survival of liver cancer stem cells via an epithelial–mesenchymal transition-like phenomenon. Ann Surg Oncol. 2012;19:539–48.
• 110. Yoshida GJ, Saya H. Inversed relationship between CD44 variant and c-Myc due to oxidative stress-induced canonical Wnt activation. Biochem Biophys Res Commun. 2014;443:622–7.
• 111. Funato Y, Michiue T, Asashima M, Miki H. The thioredoxin-related redox-regulating protein nucleoredoxin inhibits Wnt-beta-catenin signalling through dishevelled. Nat Cell Biol. 2006;8:501–8.
• 112. Ishimoto T, Nagano O, Yae T, Tamada M, Motohara T, Oshima H, 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;19:387–400.
• 113. Lei Y, Zhang D, Yu J, Dong H, Zhang J, Yang S. Targeting autophagy in cancer stem cells as an anticancer therapy. Cancer Lett. 2017;393:33–9. https://doi.org/10.1016/j.canlet.2017.02.012.
• 114. Yoshida GJ, Saya H, Zouboulis CC. Three-dimensional culture of sebaceous gland cells revealing the role of prostaglandin E2-induced activation of canonical Wnt signaling. Biochem Biophys Res Commun. 2013;438:640–6.
• 115. Yae T, Tsuchihashi K, Ishimoto T, Motohara T, Yoshikawa M, Yoshida GJ, et al. Alternative splicing of CD44 mRNA by ESRP1 enhances lung colonization of metastatic cancer cell. Nat Commun. 2012;3:883.
• 116. Yoshida GJ, Fuchimoto Y, Osumi T, Shimada H, Hosaka S, Morioka H, et al. Li-Fraumeni syndrome with simultaneous osteosarcoma and liver cancer: increased expression of a CD44 variant isoform after chemotherapy. BMC Cancer. 2012;12:444.
• 117. Korswagen HC. Regulation of the Wnt/beta-catenin pathway by redox signaling. Dev Cell. 2006;10(6):687–8.
• 118. Yoshida GJ. The heterogeneity of cancer stem-like cells at the invasive front. Cancer Cell Int. 2017;17:23.
• 119. Kajla S, Mondol AS, Nagasawa A, Zhang Y, Kato M, Matsuno K, et al. A crucial role for nox1 in redox-dependent regulation of Wnt-β-catenin signaling. FASEB J. 2012;26(5):2049–59.
• 120. Pietras A, Katz AM, Ekström EJ, Wee B, Halliday JJ, Pitter KL, et al. Osteopontin-CD44 signaling in the glioma perivascular niche enhances cancer stem cell phenotypes and promotes aggressive tumor growth. Cell Stem Cell. 2014;14:357–69.
• 121. Konopleva M, Tabe Y, Zeng Z, Andreeff M. Therapeutic targeting of microenvironmental interactions in leukemia: mechanisms and approaches. Drug Resist Updat. 2009;12(4–5):103–13.
• 122. Lee K, Qian DZ, Rey R, Wei H, Liu JO, Semenza GL. Anthracycline chemotherapy inhibits HIF-1 transcriptional activity and tumor-induced mobilization of circulating angiogenic cells. Proc Natl Acad Sci U S A. 2009;106:2353–8.
• 123. Lei Y, Zhang D, Yu J, Dong H, Zang J, Yang S. Targeting autophagy in cancer stem cells as an anticancer therapy. Cancer Lett. 2017;393:33–9.
• 124. Zhang D, Zhao Q, Sun H, Yin L, Wu J, Xu J, et al. Defective autophagy leads to the suppression of stem-like features of CD271+ osteosarcoma cells. J Biomed Sci. 2016;23:82.
• 125. Zhang L, Xu L, Zhang F, Vlashi E. Doxycycline inhibits the cancer stem cell phenotype and epithelial-tomesenchymal transition in breast cancer. Cell Cycle. 2016;16(8):737–45.
• 126. Gozuacik D, Kimchi A. Autophagy as a cell death and tumour suppressor mechanism. Oncogene. 2004;23:2891–906.
• 127. Kongara S, Karantza V. The interplay between autophagy and ROS in tumorigenesis. Front Oncol. 2012;21:1–13.
• 128. DeBerardinis RJ, Sayed N, Ditsworth D, Thompson CB. Brick by brick: metabolism and tumor cell growth. Curr Opin Genet Dev. 2008;18:54–61.
• 129. Kroemer G, Mariño G, Levine B. Autophagy and the integrated stress response. Mol Cell. 2010;40:280–93.
• 130. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144:646–74.
• 131. Tong L, Chuang C-C, Wu S. Reactive oxygen species in redox cancer therapy. Cancer Lett. 2015;367:18–25.

Identyfikatory

DOI

10.1186/s11658-018-0088-y