Differences in mitochondrial function and antioxidant systems between regions of human glioma

Cellular Physiology and Biochemistry

Volumn 22, Issue 5-6, 2008, Pages 757-768

  Santandreu, Francisca M ^a,b,c   Brell, Marta ^d   Gene, Alexandra H ^d   Guevara, Rocío ^a,b,c   Oliver, Jordi ^a,b,c   Couce, Marta E ^d,e   Roca, Pilar ^a,b  

^a Departament de Biologia Fonamental I Ciències de la Salut

^b UNIVERSITAT DE LES ILLES BALEARS   (Spain)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

^d HOSPITAL UNIVERSITARIO SON ESPASES   (Spain)

^e HUSD   (Spain)

Author keywords

Fresh tissue; Human glioma; Intratumoral regions; Isolated mitochondria; Manganese superoxide dismutase; Oxidative metabolism; Reactive oxygen species; Redox behaviour

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ANTIOXIDANT; BIOLOGICAL MARKER; CYTOCHROME C OXIDASE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; HYDROGEN PEROXIDE; MANGANESE SUPEROXIDE DISMUTASE; MITOCHONDRIAL PROTEIN;

AEROBIC METABOLISM; ANTIOXIDANT ACTIVITY; ARTICLE; BRAIN MITOCHONDRION; CANCER CELL; CANCER CHEMOTHERAPY; CANCER RADIOTHERAPY; CANCER RESISTANCE; CELL DAMAGE; CELL METABOLISM; CELL POPULATION; ENZYME ACTIVITY; GLIOMA; HUMAN; HUMAN CELL CULTURE; HUMAN TISSUE; LIPID PEROXIDATION; MITOCHONDRIAL RESPIRATION; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PRIORITY JOURNAL;

EID: 57649229829     PISSN: 10158987     EISSN: None     Source Type: Journal    
DOI: 10.1159/000185559     Document Type: Article

References (70)

1. Warburg O: On the origin of cancer cells. Science 1956;123:309-314.
2. Thompson CB: Apoptosis in the pathogenesis and treatment of disease. Science 1995;267:1456-1462.
3. Carew JS, Huang P: Mitochondrial defects in cancer. Mol Cancer 2002;1:9.
4. Oudard S, Boitier E, Miccoli L, Rousset S, Dutrillaux B, Poupon MF: Gliomas are driven by glycolysis: putative roles of hexokinase, oxidative phosphorylation and mitochondrial ultrastructure. Anticancer Res 1997;17:1903-1911.
5. Eng C, Kiuru M, Fernandez MJ, Aaltonen LA: A role for mitochondrial enzymes in inherited neoplasia and beyond. Nat Rev Cancer 2003;3:193-202.
6. Rustin P: Mitochondria, from cell death to proliferation. Nat Genet 2002;30:352-353.
7. Cuezva JM, Krajewska M, de Heredia ML, Krajewski S, Santamaria G, Kim H, Zapata JM, Marusawa H, Chamorro M, Reed JC: The bioenergetic signature of cancer: a marker of tumor progression. Cancer Res 2002;62:6674-6681.
8. Dang CV, Semenza GL: Oncogenic alterations of metabolism. Trends Biochem Sci 1999;24:68-72.
9. Lyons SA, Chung WJ, Weaver AK, Ogunrinu T, Sontheimer H: Autocrine glutamate signaling promotes glioma cell invasion. Cancer Res 2007;67:9463-9471.
10. Bru A, Albertos S, Luis Subiza J, Garcia-Asenjo JL, Bru I: The universal dynamics of tumor growth. Biophys J 2003;85:2948-2961.
11. Poli G, Leonarduzzi G, Biasi F, Chiarpotto E: Oxidative stress and cell signalling. Curr Med Chem 2004;11:1163-1182.
12. Lee HC, Wei YH: Mitochondrial biogenesis and mitochondrial DNA maintenance of mammalian cells under oxidative stress. Int J Biochem Cell Biol 2005;37:822-834.
13. Laerum OD, Bjerkvig R, Steinsvag SK, de Ridder L: Invasiveness of primary brain tumors. Cancer Metastasis Rev 1984;3:223-236.
14. Kaba SE, Kyritsis AP: Recognition and management of gliomas. Drugs 1997;53:235-244.
15. Hentschel SJ, Sawaya R: Optimizing outcomes with maximal surgical resection of malignant gliomas. Cancer Control 2003;10:109-114.
16. Deponte M, Urig S, Arscott LD, Fritz-Wolf K, Reau R, Herold-Mende C, Koncarevic S, Meyer M, Davioud-Charvet E, Ballou DP, Williams CH, Jr., Becker K: Mechanistic studies on a novel, highly potent gold-phosphole inhibitor of human glutathione reductase. J Biol Chem 2005;280:20628-20637.
17. Bradford M: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248-254.
18. Vassault A (ed): Lactate Dehydrogenase. Verlag Chemie, Weinheim, Basel, 1984.
19. Nakano K, Tarashima M, Tachikawa E, Noda N, Nakayama T, Sasaki K, Mizoguchi E, Matsuzaki M, Osawa M: Platelet mitochondrial evaluation during cytochrome c and dichloroacetate treatments of MELAS. Mitochondrion 2005;5:426-433.
20. Chrzanowska-Lightowlers ZM, Turnbull DM, Lightowlers RN: A microtiter plate assay for cytochrome c oxidase in permeabilized whole cells. Anal Biochem 1993;214:45-49.
21. Ragan CI, Wilson MT, Darley-Usmar VM, Lowe PN (eds): Subfractionation of mitochondria and isolation of the proteins of oxidative phosphorylation. Oxford, 1987.
22. Quick KL, Hardt JI, Dugan LL: Rapid microplate assay for superoxide scavenging efficiency. J Neurosci Methods 2000;97:139-144.
23. Smith AD, Morris VC, Levander OA: Rapid determination of glutathione peroxidase and thioredoxin reductase activities using a 96-well microplate format: comparison to standard cuvette-based assays. Int J Vitam Nutr Res 2001;71:87-92.
24. Wen JJ, Vyatkina G, Garg N: Oxidative damage during chagasic cardiomyopathy development: role of mitochondrial oxidant release and inefficient antioxidant defense. Free Radic Biol Med 2004;37:1821-1833.
25. Lopez-Torres M, Gredilla R, Sanz A, Barja G: Influence of aging and long-term caloric restriction on oxygen radical generation and oxidative DNA damage in rat liver mitochondria. Free Radic Biol Med 2002;32:882-889.
26. Valle A, Guevara R, Garcia-Palmer FJ, Roca P, Oliver J: Sexual dimorphism in liver mitochondrial oxidative capacity is conserved under caloric restriction conditions. Am J Physiol Cell Physiol 2007;293:C1302-1308.
27. Tietze F: Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal Biochem 1969;27:502-522.
28. Koekemoer TC, Oelofsen W: Properties of porcine white adipose tissue and liver mitochondrial subpopulations. Int J Biochem Cell Biol 2001;33:889-901.
29. Justo R, Oliver J, Gianotti M: Brown adipose tissue mitochondrial subpopulations show different morphological and thermogenic characteristics. Mitochondrion 2005;5:45-53.
30. Mambo E, Gao X, Cohen Y, Guo Z, Talalay P, Sidransky D: Electrophile and oxidant damage of mitochondrial DNA leading to rapid evolution of homoplasmic mutations. Proc Natl Acad Sci U S A 2003;100:1838-1843.
31. Milano J, Day BJ: A catalytic antioxidant metalloporphyrin blocks hydrogen peroxide-induced mitochondrial DNA damage. Nucleic Acids Res 2000;28:968-973.
32. Yakes FM, Van Houten B: Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress. Proc Natl Acad Sci U S A 1997;94:514-519.
33. Melov S, Hinerfeld D, Esposito L, Wallace DC: Multi-organ characterization of mitochondrial genomic rearrangements in ad libitum and caloric restricted mice show striking somatic mitochondrial DNA rearrangements with age. Nucleic Acids Res 1997;25:974-982.
34. Buege JA, Aust SD: Microsomal lipid peroxidation. Methods Enzymol 1978;52:302-310.
35. Levine RL, Williams JA, Stadtman ER, Shacter E: Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol 1994;233:346-357.
36. Reznick AZ, Parcker L: Oxidative damage to proteins: spectrophotometric method for carbonyl assay. Methods Enzymol 1994;233:357-363.
37. Kudin AP, Bimpong-Buta NY, Vielhaber S, Elger CE, Kunz WS: Characterization of superoxide-producing sites in isolated brain mitochondria. J Biol Chem 2004;279:4127-4135.
38. Song C, Al-Mehdi AB, Fisher AB: An immediate endothelial cell signaling response to lung ischemia. Am J Physiol Lung Cell Mol Physiol 2001;281:L993-1000.
39. Maragos WF, Korde AS: Mitochondrial uncoupling as a potential therapeutic target in acute central nervous system injury. J Neurochem 2004;91:257-262.
40. Rousset S, Alves-Guerra MC, Mozo J, Miroux B, Cassard-Doulcier AM, Bouillaud F, Ricquier D: The biology of mitochondrial uncoupling proteins. Diabetes 2004;53 Suppl 1:S130-135.
41. Lee YW, Ha MS, Kim YK: Role of reactive oxygen species and glutathione in inorganic mercury-induced injury in human glioma cells. Neurochem Res 2001;26:1187-1193.
42. Shapiro JR, Shapiro WR: The subpopulations and isolated cell types of freshly resected high grade human gliomas: their influence on the tumor's evolution in vivo and behavior and therapy in vitro. Cancer Metastasis Rev 1985;4:107-124.
43. Leaver HA, Williams JR, Smith C, Whittle IR: Intracellular oxidation by human glioma cell populations: effect of arachidonic acid. Prostaglandins Leukot Essent Fatty Acids 2004;70:449-453.
44. Kato K, Ogura T, Kishimoto A, Minegishi Y, Nakajima N, Miyazaki M, Esumi H: Critical roles of AMP-activated protein kinase in constitutive tolerance of cancer cells to nutrient deprivation and tumor formation. Oncogene 2002;21:6082-6090.
45. Peoc'h M, Le Duc G, Trayaud A, Farion R, Le Bas JF, Pasquier B, Remy C: Quantification and distribution of neovascularization following microinjection of C6 glioma cells in rat brain. Anticancer Res 1999;19:3025-3030.
46. Le Duc G, Peoc'h M, Remy C, Charpy O, Muller RN, Le Bas JF, Decorps M: Use of T(2)-weighted susceptibility contrast MRI for mapping the blood volume in the glioma-bearing rat brain. Magn Reson Med 1999;42:754-761.
47. Seyfried TN, Mukherjee P: Targeting energy metabolism in brain cancer: review and hypothesis. Nutr Metab (Lond) 2005;2:30.
48. Maurer I, Zierz S, Moller H: Evidence for a mitochondrial oxidative phosphorylation defect in brains from patients with schizophrenia. Schizophr Res 2001;48:125-136.
49. Djouadi F, Bastin J, Gilbert T, Rotig A, Rustin P, Merlet-Benichou C: Mitochondrial biogenesis and development of respiratory chain enzymes in kidney cells: role of glucocorticoids. Am J Physiol 1994;267:C245-254.
50. Paradies G, Ruggiero FM, Petrosillo G, Quagliariello E: Peroxidative damage to cardiac mitochondria: cytochrome oxidase and cardiolipin alterations. FEBS Lett 1998;424:155-158.
51. Prabu SK, Anandatheerthavarada HK, Raza H, Srinivasan S, Spear JF, Avadhani NG: Protein kinase A-mediated phosphorylation modulates cytochrome c oxidase function and augments hypoxia and myocardial ischemia-related injury. J Biol Chem 2006;281:2061-2070.
52. Kiebish MA, Seyfried TN: Absence of pathogenic mitochondrial DNA mutations in mouse brain tumors. BMC Cancer 2005;5:102.
53. Nicholls DG: Mitochondrial membrane potential and aging. Aging Cell 2004;3:35-40.
54. Harper ME, Bevilacqua L, Hagopian K, Weindruch R, Ramsey JJ: Ageing, oxidative stress, and mitochondrial uncoupling. Acta Physiol Scand 2004;182:321-331.
55. Lee I, Bender E, Kadenbach B: Control of mitochondrial membrane potential and ROS formation by reversible phosphorylation of cytochrome c oxidase. Mol Cell Biochem 2002;234-235:63-70.
56. Herrero A, Barja G: ADP-regulation of mitochondrial free radical production is different with complex I- or complex II-linked substrates: implications for the exercise paradox and brain hypermetabolism. J Bioenerg Biomembr 1997;29:241-249.
57. Yokomizo A, Ono M, Nanri H, Makino Y, Ohga T, Wada M, Okamoto T, Yodoi J, Kuwano M, Kohno K: Cellular levels of thioredoxin associated with drug sensitivity to cisplatin, mitomycin C, doxorubicin, and etoposide. Cancer Res 1995;55:4293-4296.
58. Lazo JS, Kuo SM, Woo ES, Pitt BR: The protein thiol metallothionein as an antioxidant and protectant against antineoplastic drugs. Chem Biol Interact 1998;111-112:255-262.
59. Portakal O, Ozkaya O, Erden Inal M, Bozan B, Kosan M, Sayek I: Coenzyme Q10 concentrations and antioxidant status in tissues of breast cancer patients. Clin Biochem 2000;33:279-284.
60. Brown NS, Bicknell R: Hypoxia and oxidative stress in breast cancer. Oxidative stress: its effects on the growth, metastatic potential and response to therapy of breast cancer. Breast Cancer Res 2001;3:323-327.
61. Zhong W, Oberley LW, Oberley TD, Yan T, Domann FE, St Clair DK: Inhibition of cell growth and sensitization to oxidative damage by overexpression of manganese superoxide dismutase in rat glioma cells. Cell Growth Differ 1996;7:1175-1186.
62. Li S, Yan T, Yang JQ, Oberley TD, Oberley LW: The role of cellular glutathione peroxidase redox regulation in the suppression of tumor cell growth by manganese superoxide dismutase. Cancer Res 2000;60:3927-3939.
63. Lee HC, Kim DW, Jung KY, Park IC, Park MJ, Kim MS, Woo SH, Rhee CH, Yoo H, Lee SH, Hong SI: Increased expression of antioxidant enzymes in radioresistant variant from U251 human glioblastoma cell line. Int J Mol Med 2004;13:883-887.
64. Wang W, Ballatori N: Endogenous glutathione conjugates:occurrence and biological functions. Pharmacol Rev 1998;50:335-356.
65. Grandjean F, Bremaud L, Robert J, Ratinaud MH: Alterations in the expression of cytochrome c oxidase subunits in doxorubicin-resistant leukemia K562 cells. Biochem Pharmacol 2002;63:823-831.
66. Harper ME, Antoniou A, Villalobos-Menuey E, Russo A, Trauger R, Vendemelio M, George A, Bartholomew R, Carlo D, Shaikh A, Kupperman J, Newell EW, Bespalov IA, Wallace SS, Liu Y, Rogers JR, Gibbs GL, Leahy JL, Camley RE, Melamede R, MK. N: Characterization of a novel metabolic strategy used by drug-resistant tumor cells. FASEB J 2002;16:1550-1557
67. Seyfried TN: Perspectives on brain tumor formation involving macrophages, glia, and neural stem cells. Perspect Biol Med 2001;44:263-282.
68. Sonnenschein C, Soto AM: The Society of Cells: Cancer and the Control of Cell Proliferation. New York: Springer-Verlag 1999.
69. Mehta MP, Rodrigus P, Terhaard CH, Rao A, Suh J, Roa W, Souhami L, Bezjak A, Leibenhaut M, Komaki R, Schultz C, Timmerman R, Curran W, Smith J, Phan SC, Miller RA, Renschler MF: Survival and neurologic outcomes in a randomized trial of motexafin gadolinium and wholebrain radiation therapy in brain metastases. J Clin Oncol 2003;21:2529-2536.
70. Nebeling LC, Miraldi F, Shurin SB, Lerner E: Effects of a ketogenic diet on tumor metabolism and nutritional status in pediatric oncology patients: two case reports. J Am Coll Nutr 1995;14:202-208.