Differential effects of the glycolysis inhibitor 2-deoxy- D -glucose on the activity of pro-apoptotic agents in metastatic melanoma cells, and induction of a cytoprotective autophagic response

International Journal of Cancer

Volumn 131, Issue 4, 2012, Pages

  Giammarioli, Anna Maria ^a   Gambardella, Lucrezia ^a   Barbati, Cristiana ^a,b   Pietraforte, Donatella ^a   Tinari, Antonella ^a   Alberton, Manuela ^a   Gnessi, Lucio ^c   Griffin, Roger J ^d   Minetti, Maurizio ^a   Malorni, Walter ^a,b  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b Istituto San Raffaele   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

2 deoxy D glucose; apoptosis; autophagy; cisplatin; melanoma; mitochondria; pyrimethamine; reactive oxygen species; temozolomide

Indexed keywords

CISPLATIN; DEOXYGLUCOSE; FREE RADICAL; PYRIMETHAMINE; STAUROSPORINE; TEMOZOLOMIDE;

APOPTOSIS; AUTOPHAGY; CELL CYCLE ARREST; CELL CYCLE CHECKPOINT; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL PROTECTION; CONTROLLED STUDY; DRUG EFFICACY; DRUG POTENTIATION; ENDOPLASMIC RETICULUM STRESS; G0 PHASE CELL CYCLE CHECKPOINT; G1 PHASE CELL CYCLE CHECKPOINT; HOMEOSTASIS; HUMAN; HUMAN CELL; MELANOMA CELL; METASTASIS POTENTIAL; MITOCHONDRION; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; REVIEW;

ADENOSINE TRIPHOSPHATE; ANTINEOPLASTIC AGENTS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; CELL CYCLE; CELL LINE, TUMOR; DEOXYGLUCOSE; GLYCOLYSIS; HUMANS; MELANOMA; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON, TRANSMISSION; MITOCHONDRIA; NEOPLASM METASTASIS; PROTO-ONCOGENE PROTEINS C-BCL-2; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN SPECIES;

EID: 84862303668     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.26420     Document Type: Review

References (41)

1. Pelicano H, Martin DS, Xu RH, Huang P,. Glycolysis inhibition for anticancer treatment. Oncogene 2006; 25: 4633-46. (Pubitemid 44187614)
2. Warburg O,. Origin of cancer cells. Science 1956; 123: 309-14.
3. Laszlo J, Humphreys S, Goldin A,. Effects of glucose analogues (2-deoxy-D-glucose, 2-deoxy-D-galactose) on experimental tumors. J Natl Cancer Inst 1960; 24: 267-80.
4. Maher JC, Krishan A, Lampidis TJ,. Greater cell cycle inhibition and cytotoxicity induced by 2-deoxy-D-glucose in tumor cells treated under hypoxic vs aerobic conditions. Cancer Chemother Pharmacol 2004; 53: 116-22. (Pubitemid 38186989)
5. Kurtoglu M, Gao N, Shang J, Maher JC, Lehrman MA, Wangpaichitr M, Savaraj N, Lane AN, Lampidis TJ,. Under normoxia, 2-deoxy-D-glucose elicits cell death in select tumor types not by inhibition of glycolysis but by interfering with N-linked glycosylation. Mol Cancer Ther 2007; 6: 3049-58. (Pubitemid 350206783)
6. Ralser M, Wamelink MM, Struys EA, Joppich C, Krobitsch S, Jakobs C, Lehrach H,. A catabolic block does not sufficiently explain how 2-deoxy-D-glucose inhibits cell growth. Proc Natl Acad Sci USA 2008; 105: 17807-11.
7. Metere A, Iorio E, Pietraforte D, Podo F, Minetti M,. Peroxynitrite signaling in human erythrocytes: synergistic role of hemoglobin oxidation and band 3 tyrosine phosphorylation. Arch Biochem Biophys 2009; 484: 173-82.
8. Halliwell B,. Oxidative stress and cancer: have we moved forward? Biochem J 2007; 401: 1-11. (Pubitemid 46115897)
9. Oberley TD,. Oxidative damage and cancer. Am J Pathol 2002; 160: 403-8. (Pubitemid 34160315)
10. Scherz-Shouval R, Shvets E, Elazar Z,. Oxidation as a post-translational modification that regulates autophagy. Autophagy 2007; 3: 371-3. (Pubitemid 46986347)
11. Giles GI,. The redox regulation of thiol dependent signaling pathways in cancer. Curr Pharm Des 2006; 12: 4427-43. (Pubitemid 44835155)
12. Matarrese P, Di Biase L, Santodonato L, Straface E, Mecchia M, Ascione B, Parmiani G, Belardelli F, Ferrantini M, Malorni W,. Type I interferon gene transfer sensitizes melanoma cells to apoptosis via a target activity on mitochondrial function. Am J Pathol 2002; 160: 1507-20. (Pubitemid 34411654)
13. Matarrese P, Nencioni L, Checconi P, Ciarlo L, Gambardella L, Ascione B, Sgarbanti R, Garaci E, Malorni W, Palamara AT,. Pepstatin A alters host cell autophagic machinery and leads to a decrease in influenza a virus production. J Cell Physiol 2011; 226: 3368-77.
14. Cossarizza A, Franceschi C, Monti D, Salvioli S, Bellesia E, Rivabene R, Biondo L, Rainaldi G, Tinari A, Malorni W,. Protective effect of N-acetylcysteine in tumor necrosis factor-alpha-induced apoptosis in U937 cells: the role of mitochondria. Exp Cell Res 1995; 220: 232-40.
15. Giammarioli AM, Maselli A, Casagrande A, Gambardella L, Gallina A, Spada M, Giovannetti A, Proietti E, Malorni W, Pierdominici M,. Pyrimethamine induces apoptosis of melanoma cells via a caspase and cathepsin double-edged mechanism. Cancer Res 2008; 68: 5291-300.
16. Chen M, Osman I, Orlow SJ,. Antifolate activity of pyrimethamine enhances temozolomide-induced cytotoxicity in melanoma cells. Mol Cancer Res 2009; 7: 703-12.
17. Zhang XD, Gillespie SK, Hersey P,. 2004 Staurosporine induces apoptosis of melanoma by both caspase-dependent and -independent apoptotic pathways. Mol Cancer Ther 2004; 3: 187-97. (Pubitemid 39193693)
18. Moreau K, Luo S, Rubinsztein DC,. Cytoprotective roles for autophagy. Curr Opin Cell Biol 2010; 22: 206-11.
19. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, Askew DS, Baba M, Baehrecke EH, Bahr BA, Ballabio A, Bamber BA, Bassham DC, et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008; 4: 151-75. (Pubitemid 351231180)
20. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, Packer M, Schneider MD, Levine B,. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 2005; 122: 927-39. (Pubitemid 41345209)
21. Hayashi-Nishino M, Fujita N, Noda T, Yamaguchi A, Yoshimori T, Yamamoto A,. A subdomain of the endoplasmic reticulum forms a cradle for autophagosome formation. Nat Cell Biol 2009; 11: 1433-7.
22. Crow JP,. Dichlorodihydrofluorescein and dihydrorhodamine 123 are sensitive indicators of peroxynitrite in vitro: implications for intracellular measurement of reactive nitrogen and oxygen species. Nitric Oxide 1997; 1: 145-57. (Pubitemid 28076555)
23. Bassenge E, Sommer O, Schwemmer M, Bunger R,. Antioxidant pyruvate inhibits cardiac formation of reactive oxygen species through changes in redox state. Am J Physiol Heart Circ Physiol 2000; 279: 2431-8.
24. Jourd'Heuil D,. Increased nitric oxide-dependent nitrosylation of 4,5-diaminofluorescein by oxidants: implications for the measurement of intracellular nitric oxide. Free Radic Biol Med 2002; 33: 676-84.
25. Tasdemir E, Maiuri MC, Tajeddine N, Vitale I, Criollo A, Vicencio JM, Hickman JA, Geneste O, Kroemer G,. Cell cycle-dependent induction of autophagy, mitophagy and reticulophagy. Cell Cycle 2007; 6: 2263-7. (Pubitemid 47547704)
26. Liu H, Hu YP, Savaraj N, Priebe W, Lampidis TJ,. Hypersensitization of tumor cells to glycolytic inhibitors. Biochemistry 2001; 40: 5542-7. (Pubitemid 32458256)
27. Simons AL, Fath MA, Mattson DM, Smith BJ, Walsh SA, Graham MM, Hichwa RD, Buatti JM, Dornfeld K, Spitz DR,. Enhanced response of human head and neck cancer xenograft tumors to cisplatin combined with 2-deoxy-D- glucose correlates with increased 18F-FDG uptake as determined by PET imaging. Int J Radiat Oncol Biol Phys 2007; 69: 1222-30. (Pubitemid 47625869)
28. Di Paola RS, Dvorzhinski D, Thalasila A, Garikapaty V, Doram D, May M, Bray K, Mathew R, Beaudoin B, Karp C, Stein M, Foran DJ, White E,. Therapeutic starvation and autophagy in prostate cancer: a new paradigm for targeting metabolism in cancer therapy. Prostate 2008; 68: 1743-52.
29. Aft RL, Zhang FW, Gius D,. Evaluation of 2-deoxy-D-glucose as a chemotherapeutic agent: mechanism of cell death. Br J Cancer 2002; 87: 805-12. (Pubitemid 35178760)
30. Matarrese P, Tinari A, Mormone E, Bianco GA, Toscano MA, Ascione B, Rabinovich GA, Malorni W,. Galectin-1 sensitizes resting human T lymphocytes to Fas (CD95)-mediated cell death via mitochondrial hyperpolarization, budding, and fission. J Biol Chem 2005; 80: 6969-85. (Pubitemid 40341253)
31. Fulda S, Galluzzi L, Kroemer G,. Targeting mitochondria for cancer therapy. Nat Rev Drug Discov 2010; 9: 447-64.
32. Zhang XD, Deslandes E, Villedieu M, Poulain L, Duval M, Gauduchon P, Schwartz L, Icard P,. Effect of 2-deoxy-D-glucose on various malignant cell lines in vitro. Anticancer Res 2006; 26: 3561-6. (Pubitemid 44701539)
33. Fath MA, Diers AR, Aykin-Burns N, Simons AL, Hua L, Spitz DR,. Mitochondrial electron transport chain blockers enhance 2-deoxy-D-glucose induced oxidative stress and cell killing in human colon carcinoma cells. Cancer Biol Ther 2009; 8: 1228-36.
34. Ben Sahra I, Laurent K, Giuliano S, Larbret F, Ponzio G, Gounon P, Le Marchand-Brustel Y, Giorgetti-Peraldi S, Cormont M, Bertolotto C, Deckert M, Auberger P, et al,. Targeting cancer cell metabolism: the combination of metformin and 2-deoxyglucose induces p53-dependent apoptosis in prostate cancer cells. Cancer Res 2010; 70: 2465-75.
35. Fimia GM, Piacentini M,. Regulation of autophagy in mammals and its interplay with apoptosis. Cell Mol Life Sci 2010; 67: 1581-8.
36. Bernales S, McDonald KL, Walter P,. Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response. PLoS Biol 2006; 4: e423.
37. Legorreta-Herrera M, Retana-Ugalde R, Ventura-Gallegos JL, Narváez, V,. Pyrimethamine induces oxidative stress in P. yoelii 17XL-infected mice: a novel immunomodulatory mechanism of action for an old antimalarial drug? Exp Parasitol 2010; 126: 381-8.
38. Gac M, Brigda J, Vahlenkamp TW,. Increased mitochondrial superoxide dismutase expression and lowered production of reactive oxygen species during rotavirus infection. Virology 2010; 404: 293-303.
39. Sinthupibulyakit C, Ittarat, W, St Clai WH, St Clair DK,. P53 Protects lung cancer cells against metabolic stress. Int J Oncol 2010; 37: 1575-81.
40. Yamauchi A, Ichimiya T, Inoue K, Taguchi Y, Matsunaga N, Koyanagi S, Fukagawa T, Aramaki H, Higuchi S, Ohdo S,. Cell-cycle-dependent pharmacology of methotrexate in HL-60. J Pharmacol Sci 2005; 99: 335-41. (Pubitemid 41813425)
41. Kurtoglu M, Maher JC, Lampidis TJ,. Differential toxic mechanisms of 2-deoxy-D-glucose versus 2-fluorodeoxy-D-glucose in hypoxic and normoxic tumor cells. Antioxid Redox Signal 2007; 9: 1383-90. (Pubitemid 47255017)