Differential toxic mechanisms of 2-deoxy-D-glucose versus 2-fluorodeoxy-D-glucose in hypoxic and normoxic tumor cells

Antioxidants and Redox Signaling

Volumn 9, Issue 9, 2007, Pages 1383-1390

  Kurtoglu, Metin ^a   Maher, Johnathan C ^a   Lampidis, Theodore J ^a,b  

^a UNIVERSITY OF MIAMI   (United States)

^b PAP Bldg ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ANTINEOPLASTIC AGENT; DEOXYGLUCOSE; DOCETAXEL; FLUORODEOXYGLUCOSE; GLUCOSE DERIVATIVE; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; HEXOKINASE; MANNOSE;

AEROBIC CAPACITY; ANAEROBIC CAPACITY; APOPTOSIS; CELL HYPOXIA; DRUG CYTOTOXICITY; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENCY; GLYCOLYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; REVIEW; SYSTEMATIC REVIEW; TUMOR CELL;

ANAEROBIOSIS; CELL HYPOXIA; DEOXYGLUCOSE; GLYCOLYSIS; HUMANS; MODELS, BIOLOGICAL; NEOPLASMS; OXYGEN CONSUMPTION;

EID: 34547902505     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/ars.2007.1714     Document Type: Review

References (79)

1. Ahren B and Hedner P. Mechanism for the inhibitory action of 2-deoxy-glucose on thyroid hormone secretion in the mouse. Neuroendocrinology 49: 471-475, 1989.
2. Ball HA, Wick AN, and Sanders C. Influence of glucose antimetabolites on the Walker tumor. Cancer Res 17: 235-239, 1957.
3. Breckenridge DG, Germain M, Mathai JP, Nguyen M, and Shore GC. Regulation of apoptosis by endoplasmic reticulum pathways. Oncogene 22: 8608-8618, 2003.
4. Brown J. Effects of 2-deoxyglucose on carbohydrate metabolism: review of the literature and studies in the rat. Metabolism 11: 1098-1112, 1962.
5. Carameliet P and Jain RK. Angiogenesis in cancer and other diseases. Nature 407: 249-257, 2000.
6. Cay O, Jeppsson B, Ahren B, and Bengmark S. Inhibitory effect of 2-deoxy-D-glucose on liver tumor growth in rats. Cancer Res 52: 5794-5796, 1992.
7. Chandramouli V and Carter JR. Metabolic effects of 2-deoxy-D-glucose in isolated fat cells. Biochim Biophys Acta 496: 278-291, 1977.
8. Chen J, Zhao S, Nakada K, Kuge Y, Tamaki N, Okada F, Wang J, Shindo M, Higashino F, Takeda K, Asaka M, Katoh H, Sugiyama T, Hosokawa M, and Kobayashi M. Dominant-negative hypoxia-inducible factor-1a reduces tumorigenicity of pancreatic cancer cells through the suppression of glucose metabolism. Am J Pathol 162: 1283-1291, 2003.
9. Chen W and Gueron M. The inhibition of bovine heart hexokinase by 2-deoxy-D-glucose-6-phosphate: characterization by 31P NMR and metabolic implications. Biochimie 74:867-873, 1992.
10. Cramer FB and Woodward GE. 2-deoxy-D-glucose as an antagonist of glucose in yeast fermentation. J Franklin Inst 253: 354-360, 1952.
11. Datema R, Schwarz RT, and Jankowski AW. Fluoro-glucose inhibition of protein glycosylation in vivo. Eur J Biochem 109: 331-341, 1980.
12. Datema R and Schwarz RT. Interference with glycosylation of glycoproteins. Biochem J 184: 113-123, 1979.
13. Datema R and Schwarz RT. Formation of 2-deoxyglucose-containing lipid-linked oligosaccharides. Eur J Biochem 90: 505-516, 1978.
14. Davis JA and Freeze HH. Studies of mannose metabolism and effects of long-term mannose ingestion in the mouse. Biochim Biophys Acta 1528: 116-126, 2001.
15. Dvorak HF, Brown LF, Detmar M, and Dvorak AM. Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis. Am J Pathol 146: 1029-1039, 1995.
16. Ellgaard L and Helenius A. Quality control in the endoplasmic reticulum. Nat Rev Mol Cell Biol 4: 181-191, 2003.
17. Ely JO. 2-Deoxy-D-glucose as an inhibitor of cancerous growth in animals. J Franklin Inst 258:157-160, 1954.
18. Escuin D, Simons JW, and Giannakakou P. Exploitation of the HIF axis for cancer therapy. Cancer Biol Ther 3: 608-611, 2004.
19. Flier JS, Mueckler MM, Usher P, and Lodish HF. Elevated levels of glucose transport and transporter messenger RNA are induced by ras or src oncogenes. Science 235: 1492-1495, 1987.
20. Freeze HH. Human disorders in N-glycosylation and animal models. Biochim Biophys Acta 1573: 388-393, 2002.
21. Freeze HH. Sweet solution: sugars to the rescue. J Cell Biol 158: 615-616, 2002.
22. Funasaka T, Yanagawa T, Hogan V, and Raz A. Regulation of phosphoglucose isomerase/autocrine motility factor expression by hypoxia. FASEB J 19: 1422-1430, 2005.
23. Gatenby RA and Gillies RJ. Why do cancers have high aerobic glycolysis? Nat Rev Cancer 4: 891-899, 2004.
24. Geschwind JF, Georgiades CS, Ko YH, and Pedersen PL. Recently elucidated energy catabolism pathways provide opportunities for novel treatments in hepatocellular carcinoma. Exp Rev Anticancer Ther 4: 449-547, 2004.
25. Green SL and Giaccia AJ. Tumor hypoxia and the cell cycle: implications for malignant progression and response to therapy. Cancer J Sci Am 4: 218-223, 1998.
26. Harrison L and Blackwell K. Hypoxia and anemia: factors in decreased sensitivity to radiation therapy and chemotherapy? Oncologist 9: 31-40, 2004.
27. Harrison LB, Chadha M, Hill RJ, Hu K, and Shasha D. Impact of tumor hypoxia and anemia on radiation therapy outcomes. Oncologist 7: 492-508, 2002.
28. Ibrahim NO, Hahn T, Franke C, Stiehl DP, Wirthner R, Wenger RH, and Katschinski DM. Induction of the hypoxia-inducible factor system by low levels of heat shock protein 90 inhibitors. Cancer Res 65: 11094-11100, 2005.
29. Kalns J, Krock L, and Piepmeier E Jr. The effect of hyperbaric oxygen on growth and chemosensitivity of metastatic prostate cancer. Anticancer Res 18: 363-367, 1998.
30. Kang HT and Hwang ES. 2-Deoxyglucose: an anticancer and antiviral therapeutic, but not any more a low glucose mimetic. Life Sci 78: 1392-399, 2006.
31. Karlsson S and Ahren B. Inhibition of 2-deoxy-glucose-induced glucagon secretion by muscarinic and alpha-adrenoceptor blockade in the mouse. Diabetes Res Clin Pract 3: 239-242, 1987.
32. Karlsson S, Bood M, and Ahren B. The mechanism of 2-deoxy-glucose-induced insulin secretion in the mouse. J Auton Pharmacol 7: 135-144, 1987.
33. Keenoy MY, Zahner D, and Malaisse WJ. Dissociated effects of 2-deoxy-D-glucose on D-[2-3H]glucose and D-[5-3H]glucose conversion into 3HOH in rat erythrocytes. Biochem J 288: 433-488, 1992.
34. Kelloff GJ, Hoffman JM, Johnson B, Scher HI, Siegel BA, Cheng EY, Cheson BD, O'shaughnessy J, Guyton KZ, Mankoff DA, Shankar L, Larson SM, Sigman CC, Schilsky RL, and Sullivan DC. Progress and promise of FDG-PET imaging for cancer patient management and oncologic drug development. Clin Cancer Res 11: 2785-2808, 2005.
35. Ko YH, Smith BL, Wang Y, Pomper MG, Rini DA, Torbenson MS, Hullihen J, and Pedersen PL. Advanced cancers: eradication in all cases using 3-bromopyruvate therapy to deplete ATP. Biochem Biophys Res Commun 324: 269-275, 2004.
36. Kumar P. Impact of anemia in patients with head and neck cancer. Oncologist 5: 13-18, 2000.
37. Kurtoglu M, Maher JC, Krishan A, Priebe A, and Lampidis TJ. 2-Deoxy-D-glucose kills select tumor cell types under normoxia: reversal by mannose suggests a mechanism of interference with glycosylation #2375. Presented at American Association of Cancer Research Annual Meeting: Proceeding; 2005 April 16-20. Anaheim, CA.
38. Lampidis TJ, Kurtoglu M, Maher JC, Liu H, Krishan A, Sheft V, Szymanski S, Fokt I, Rudnicki WR, Ginalski K, Lesyng B, and Priebe W. Efficacy of 2-halogen substituted D-glucose analogs in blocking glycolysis and killing "hypoxic tumor cells." Cancer Chemother Pharmacol 58: 725-734, 2006.
39. Landau BR, Laszlo J, Stengle J, and Burk D. Certain metabolic and pharmacologic effects in cancer patients given infusion of 2-deoxy-D-glucose. J Natl Cancer Inst 21: 485-494, 1958.
40. Laszlo J, Humphreys SR, and Goldin A. Effects of glucose analogues (2-deoxy-D-glucose, 2-deoxy-D-galactose) on experimental tumors. J Natl Cancer Inst 24: 267-281, 1960.
41. Liu H, Hu YP, Savaraj N, Priebe W, and Lampidis TJ. Hypoxia increases tumor cell sensitivity to glycolytic inhibitors a strategy for solid tumor therapy (model C). Biochem Pharmacol 64: 1746-1751, 2002.
42. Liu H, Hu YP, Savaraj N, Priebe W, and Lampidis TJ. Hypersensitization of tumor cells to glycolytic inhibitors. Biochemistry 40: 5542-5547, 2001.
43. Luo Y, Jiang C, Belanger AJ, Akita GY, Wadsworth SC, Gregory RJ, et al. A constitutively active hypoxia-inducible factor-1 alpha/VP16 hybrid factor activates expression of the human B-type natriuretic peptide gene. Mol Pharmacol 69: 1953-1962, 2006.
44. Maher JC, Wangpaichitr M, Savaraj N, Kurtoglu M, and Lampidis TJ. Hypoxic inducible factor-1 confers resistance to 2-deoxy-D-glucose in cell growing under hypoxia. Mol Cancer Ther 6: 732-741, 2007.
45. Maher JC, Krishan A, and 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 53: 116-122, 2004.
46. Martin DS, Bertino JR, and Koutcher JA. ATP depletion+pyrimidine depletion can markedly enhance cancer therapy: fresh insight for a new approach. Cancer Res 60: 6776-6783, 2000.
47. Maschek G, Savaraj N, Priebe W, Braunschweiger P, Hamilton K, Tidmarsh G, De Young LR, and Lampidis TJ. 2-Deoxy-D-glucose increases the efficacy of Adriamycin and paclitaxel in human osteosarcoma and non-small cell lung cancers in vivo. Cancer Res 64: 31-34, 2004.
48. Maxwell PH. The HIF pathway in cancer. Semin Cell Dev Biol 16: 523-530, 2005.
49. Maxwell PH, Pugh CW, and Ratcliffe PJ. Activation of the HIF pathway in cancer. Curr Opin Genet Dev 11: 293-299, 2001.
50. Maxwell PH, Pugh CW, and Ratcliffe PJ. Inducible operation of the erythropoietin 3′ enhancer in multiple cell lines: evidence for a widespread oxygen sensing mechanism. Proc Natl Acad Sci U S A 90: 2423-2427, 1993.
51. Mohanti BK, Rath GK, Anantha N, Kannan V, Das BS, Chandramouli BA, Banerjee AK, Das S, Jena A, Ravichandran R, Sahi UP, Kumar R, Kapoor N, Kalia VK, Dwarakanath BS, and Jain V. Improving cancer radiotherapy with 2-deoxy-D-glucose: phase I/II clinical trials on human cerebral gliomas. Int J Radiat Oncol Biol Phys 35: 103-111, 1996.
52. Niehues R, Hasilik M, Alton G, Korner C, Schiebe-Sukumar M, Koch HG, Zimmer KP, Wu R, Harms E, Reiter K, von Figura K, Freeze HH, Harms HK, and Marquardt T. Carbohydrate-deficient glycoprotein syndrome type Ib. J Clin Invest 101: 1414-1420, 1998.
53. Nirenberg MW and Hogg JF. Inhibition of anaerobic glycolysis in Ehrlich ascites tumor cells by 2-deoxy-D-glucose. Cancer Res 18: 518-521, 1958.
54. Paneerselvam K and Freeze HH. Mannose corrects altered N-glycosylation in carbohydrate-deficient glycoprotein syndrome fibroblasts. J Clin Invest 97: 1478-1487, 1996.
55. Parodi AJ. Protein glycosylation and its role in protein folding. Annu Rev Biochem 69: 69-93, 2000.
56. Pfeiffer T, Schuster S, and Bonhoeffer S. Cooperation and competition in the evolution of ATP-producing pathways. Science 292: 504-507, 2001.
57. Piret J, Mottet D, Raes M, and Michiels C. Is HIF-1α a pro- or an anti-apoptotic protein? Biochem Pharmacol 64: 889-892, 2002.
58. Pugh CW. Oxygen sensing in cancer. Ann Med 35: 380-390, 2003.
59. Rapisarda A, Shoemaker RH, and Melillo G. Targeting topoisomerase I to inhibit hypoxia inducible factor 1. Cell Cycle 3: 172-175, 2004.
60. Sakata K, Kwok TT, Murphy BJ, Laderoute KR, Gordon GR, and Sutherland RM. Hypoxia-induced drug resistance: comparison to P-glycoprotein-associated drug resistance. Br J Cancer 64: 809-814, 1991.
61. Schmidt MF, Schwarz RT, and Scholtissek C. Nucleoside-diphosphate derivatives of 2-deoxy-D-glucose in animal cells. Eur J Biochem 49: 237-247, 1974.
62. 3H] mannose in yeast and chick-embryo cells. Eur J Biochem 87: 55-68, 1978.
63. Semenza GL. Targeting HIF-1 for cancer therapy. Nat Rev Cancer 3: 721-732, 2003.
64. Semenza GL, Roth PH, Fang H, and Wang GL. Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia-inducible factor 1. J Biol Chem 269: 23757-23763, 1994.
65. Sokoloff B, Saelhof CC, McConnell B, and Simpson M. Additive effect of ascorbic acid and glucose analogs on experimental cancer and nucleic acids in tumor tissue. Growth 22: 51-61, 1958.
66. Sokoloff B, Eddy WH, Saelhof CC, and Beach J. Glucose antagonists in experimental cancer. AMA Arch Pathol 59: 729-732, 1955.
67. Sols A and Crane RK. Substrate specificity of brain hexokinase. J Biol Chem 210: 581-595, 1954.
68. Taborsky GJ Jr, Halter JB, and Porte D Jr. Morphine suppresses plasma catecholamine responses to laparotomy but not to 2-deoxyglucose. Am J Physiol 242: E317-E322, 1982.
69. Tower DB. The effects of 2-deoxy-D-glucose on metabolism of slices of cerebral cortex incubated in vitro. J Neurochem 3: 185-205, 1958.
70. Vaupel P. The role of hypoxia-induced factors in tumor progression. Oncologist 9: 10-17, 2004.
71. Vaux EC, Metzen E, Yeates KM, and Ratcliffe PJ. Regulation of hypoxia-inducible factor is preserved in the absence of a functioning mitochondrial respiratory chain. Blood 98: 296-302, 2001.
72. Waki A, Fujibayashi Y, and Yokoyama A. Recent advances in the analyses of the characteristics of tumors on FDG uptake. Nucl Med Biol 25: 589-592, 1998.
73. Wang XZ, Lawson B, Brewer JW, Zinszner H, Sanjay A, Mi LJ, Boorstein R, Kreibich G, Hendershot LM, Ron D. Signals from the stressed endoplasmic reticulum induce C/EBP-homologous protein (CHOP/GADD153). Mol Cell Biol 16: 4273-4280, 1996.
74. Wang GL, Jiang BH, Rue EA, and Semenza GL. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc Natl Acad Sci U S A 92: 5510-5514, 1995.
75. Wang GL and Semenza GL. General involvement of hypoxia-inducible factor 1 in transcriptional response to hypoxia. Proc Natl Acad Sci U S A 90: 4304-4308, 1993.
76. Warburg O. On the facultative anaerobiosis of cancer cells and its use in chemotherapy. Munch Med Wochenschr 103: 2504-2506, 1961.
77. Wick AN, Drury DR, Nakada HI, and Wolfe JB. Localization of the primary metabolic block produced by 2-deoxyglucose. J Biol Chem 224: 963-969, 1957.
78. Xu RH, Pelicano H, Zhou Y, Carew JS, Feng L, Bhalla KN, Keating MJ, and Huang P. Inhibition of glycolysis in cancer cells: a novel strategy to overcome drug resistance associated with mitochondrial respiratory defect and hypoxia. Cancer Res 65: 613-621, 2005.
79. Zu XL and Guppy M. Cancer metabolism: facts, fantasy, and fiction. Biochem Biophys Res Commun 313: 459-465, 2004.