Functional modulation of mitochondria by eicosapentaenoic acid provides protection against ceramide toxicity to C6 glioma cells

Journal of Agricultural and Food Chemistry

Volumn 57, Issue 24, 2009, Pages 11455-11462

  Jeng, Jaa Yeh ^a,b   Lee, Wei Hwa ^b,c   Tsai, Ya Hui ^b   Chen, Chia Yu ^b   Chao, Szu Yi ^b   Hsieh, Rong Hong ^b,d  

^a CATHAY GENERAL HOSPITAL   (Taiwan)

^b TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^d TAIPEI MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

Arachidonic acid; Ceramide; Eicosapentaenoic acid; Mitochondrial biogenesis; Mitochondrial transcription factor

Indexed keywords

ADENOSINE TRIPHOSPHATE; ARACHIDONIC ACID; CASPASE 3; CERAMIDE; DRUG DERIVATIVE; ICOSAPENTAENOIC ACID; MITOCHONDRIAL PROTEIN; N ACETYLSPHINGOSINE; N-ACETYLSPHINGOSINE; NEUROPROTECTIVE AGENT; SPHINGOSINE; TRANSCRIPTION FACTOR;

ANIMAL; ARTICLE; CELL SURVIVAL; COMPARATIVE STUDY; DRUG EFFECT; GENETICS; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; NERVE CELL; PHYSIOLOGY; RAT; TUMOR CELL LINE;

ADENOSINE TRIPHOSPHATE; ANIMALS; ARACHIDONIC ACID; CASPASE 3; CELL LINE, TUMOR; CELL SURVIVAL; CERAMIDES; EICOSAPENTAENOIC ACID; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; NEURONS; NEUROPROTECTIVE AGENTS; RATS; SPHINGOSINE; TRANSCRIPTION FACTORS;

RATTUS;

EID: 73349131068     PISSN: 00218561     EISSN: None     Source Type: Journal    
DOI: 10.1021/jf902021h     Document Type: Article

References (42)

1. Sasaki, S.; Iwata, M. Impairment of fast axonal transport in the proximal axons of anterior horn neurons in amyotrophic lateral sclerosis. Neurology 1996, 47, 535-540.
2. Mandemakers, W.; Morais, V. A.; De Strooper, B. A cell biological perspective on mitochondrial dysfunction in Parkinson disease and other neurodegenerative diseases. J. Cell. Sci. 2007, 120, 1707-1716.
3. Schon, E. A.; Manfredi, G. Neuronal degeneration and mitochondrial dysfunction. J. Clin. Invest. 2003, 111, 303-312.
4. Sarsilmaz, M.; Songur, A.; Ozyurt, H.; Kuş, I.; Ozen, O. A.; Ozyurt, B.; Söǧüt, S.; Akyol, O. Potential role of dietary omega-3 essential fatty acids on some oxidant/antioxidant parameters in rats' corpus striatum. Prostaglandins, Leukotrienes Essent. Fatty Acids 2003, 69, 253-259.
5. Grant, W. B. Dietary links to Alzheimer's disease: 1999 update. J. Alzheimer's Dis. 1999, 1, 197-201.
6. Yehuda, S.;Rabinovtz, S.;Carasso, R. L.;Mostofsky, D. I. Essential fatty acids preparation (SR-3) improves Alzheimer's patients quality of life. Int. J. Neuro Sci. 1996, 87, 141-149.
7. Lauritzen, I.; Blondeau, N; Heurteaux, C.; Widmann, C.; Romey, G.; Lazdunski, M. Polyunsaturated fatty acids are potent neuroprotectors. EMBO J. 2000, 19, 1784-1793.
8. Blondeau, N; Widmann, C.; Lazdunski, M.; Heurteaux, C. Polyunsaturated fatty acids induce ischemic and epileptic tolerance. Neuroscience 2002, 109, 231-241.
9. Lonergan, P. E.; Martin, D. S.; Horrobin, D. F.; Lynch, M. A. Neuroprotective actions of eicosapentaenoic acid on lipopolysaccharide-induced dysfunction in rat hippocampus. J. Neuro Chem. 2004, 91, 20-29.
10. Mori, T. A.; Beilin, L. J. Omega-3 fatty acids and inflammation. Curr. Atheroscler. Rep. 2004, 6, 461-467.
11. Wang, X.; Zhao, X.; Mao, Z. Y.; Wang, X. M.; Liu, Z. L. Neuroprotective effect of docosahexaenoic acid on glutamateinduced cytotoxicity in rat hippocampal cultures. Neuroreport 2003, 14, 2457-2461.
12. Taanman, J. W. The mitochondrial genome: structure, transcription, translation and replication. Biochim. Biophys. Acta 1999, 1410, 103-123.
13. Chang, D. D.; Clayton, D. A. Precise identification of individual promoters for transcription of each strand of human mitochondrial DNA. Cell 1984, 36, 635-643.
14. Fisher, R. P.; Clayton, D. A. Purification and characterization of human mitochondrial transcription factor 1. Mol. Cell. Biol. 1988, 8, 3496-3509.
15. Montoya, J.; Perez-Martos, A.; Garstka, H. L.; Wiesner, R. J. Regulation of mitochondrial transcription by mitochondrial transcription factor A. Mol. Cell. Bio Chem. 1997, 174, 227-230.
16. Larsson, N. G.; Barsh, G. S.; Clayton, D. A. Structure and chromosomal localization of the mouse mitochondrial transcription factor A gene (Tfam). Mamm. Genome 1997, 8, 139-140.
17. Jeng, J. Y.; Yeh, T. S.; Lee, J. W.; Lin, S. H.; Fong, T. H.; Hsieh, R. H. Maintenance of mitochondrial DNA copy number and expression are essential for preservation of mitochondrial function and cell growth. J. Cell. Bio Chem. 2008, 103, 347-357.
18. Rodgers, J. T.; Lerin, C.; Gerhart-Hines, Z.; Puigserver, P. Metabolic adaptations through the PGC-1 α and SIRT1 pathways. FEBS Lett. 2008, 582, 46-53.
19. Cooper, M. P.; Qu, L.; Rohas, L. M.; Lin, J.; Yang, W.; Erdjument-Bromage, H.; Tempst, P.; Spiegelman, B. M. Defects in energy homeostasis in Leigh syndrome French Canadian variant through PGC-1a/LRP130 complex. Genes Dev. 2006, 20, 2996-3009.
20. Lamantea, E.; Tiranti, V.; Bordoni, A.; Toscano, A.; Bono, F.; Servidei, S.; Apadimitriou, A.; Spelbrink, H.; Silvestri, L.; Casari, G.; Comi, G. P.; Zeviani, M. Mutations of mitochondrial DNA polymerase γA are a frequent cause of autosomal dominant or recessive progressive external ophthalmoplegia. Ann. Neurol. 2002, 52, 211-219.
21. Mancuso, M.; Salviati, L.; Sacconi, S.; Otaegui, D.; Camaño, P.; Marina, A.; Bacman, S.; Moraes, C T.; Carlo, J. R.; Garcia, M.; Garcia-Alvarez, M.; Monzon, L.; Naini, A. B.; Hirano, M.; Bonilla, E.; Taratuto, A. L.; DiMauro, S.; Vu, T. H. Mitochondrial DNA depletion: mutations in thymidine kinase gene with myopathy and SMA. Neurology 2002, 59, 1197-1202.
22. Cutler, R. G.; Kelly, J.; Storie, K.; Pedersen, W. A.; Tammara, A.; Hatanpaa, K.; Troncoso, J. C; Mattson, M. P. Involvement of oxidative stress-induced abnormalities in ceramide and cholesterol metabolism in brain aging and Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 2004, 101, 2070-2075.
23. Lee, J. T.; Xu, J.; Lee, J. M.; Ku, G.; Han, X.; Yang, D. I.; Chen, S.; Hsu, C Y. Amyloid-β peptide induces oligodendrocyte death by activating the neutral sphingomyelinase-ceramide pathway. J. Cell Biol. 2004, 164, 123-131.
24. Villena, J.; Henriquez, M.; Torres, V.; Moraga, F.; Díaz-Elizondo, J.; Arredondo, C.; Chiong, M.; Olea-Azar, C.; Stutzin, A.; Lavandero, S.; Quest, A. F. Ceramide-induced formation of ROS and ATP depletion trigger necrosis in lymphoid cells. Free Radical Biol. M Ed. 2008, 44, 1146-1160.
25. Páv, M.; Kovárů, H.; Fiserová, A.; Havrdová, E.; Lisá, V. Neurobiological aspects of depressive disorder and antidepressant treatment: role of glia. Physiol. Res. 2008, 57, 151-164.
26. Benda, P.; Lightbody, J.; Sato, G.; Levine, L.; Sweet, W. Differentiated rat glial cell strain in tissue culture. Science 1968, 161, 370-371.
27. Sullivan, N. R.; Burke, T.; Siafaka-Kapadai, A.; Javors, M.; Hensler, J. G. Effect of valproic acid on serotonin-2A receptor signaling in C6 glioma cells. J. Neuro Chem. 2004, 90, 1269-1275.
28. Benítez, J. A.; Arregui, L.; Cabrera, G.; Segovia, J. Valproic acid induces polarization, neuronal-like differentiation of a subpopulation of C6 glioma cells and selectively regulates transgene expression. Neuroscience 2008, 156, 911-920.
29. Parra, V.; Eisner, V.; Chiong, M.; Criollo, A.; Moraga, F.; Garcia, A.; Härtel, S.; Jaimovich, E.; Zorzano, A.; Hidalgo, C.; Lavandero, S. Changes in mitochondrial dynamics during ceramide-induced cardiomyocyte early apoptosis. Cardiovasc. Res. 2008, 77, 387-397.
30. German, O. L.; Miranda, G. E.; Abrahan, C. E.; Rotstein, N. P. Ceramide is a mediator of apoptosis in retina photoreceptors. Invest. Ophthalmol. Vis. Sci. 2006, 47, 1658-1668.
31. Stiban, J.; Caputo, L.; Colombini, M. Ceramide synthesis in the endoplasmic reticulum can permeabilize mitochondria to proapoptotic proteins. J. Lipid Res. 2008, 49, 625-634.
32. Miñano, A.; Caballero-Benítez, A.; Lluch, M.; Morán, J.; Rodríguez-Alvarez, J. C2-ceramide mediates cerebellar granule cells apoptosis by activation of caspases-2,-9, and-3. J. Neurosci. Res. 2008, 86, 1734-1747.
33. Stoica, B. A.; Movsesyan, V. A.; Lea, P. M.4th; Faden, A. I. Ceramide-induced neuronal apoptosis is associated with dephosphorylation of Akt, BAD, FKHR, GSK-3β, and induction of the mitochondrial-dependent intrinsic caspase pathway. Mol. Cell. Neuro Sci. 2003, 22, 365-382.
34. Buratta, M; Castigli, E.; Sciaccaluga, M.; Pellegrino, R. M.; Spinozzi, F.; Roberti, R.; Corazzi, L. Loss of cardiolipin in palmitatetreated GL15 glioblastoma cells favors cytochrome c release from mitochondria leading to apoptosis. J. Neuro Chem. 2008, 105, 1019-1031.
35. Koshkin, V.; Dai, F. F.; Robson-Doucette, C A.; Chan, C B.; Wheeler, M. B. Limited mitochondrial permeabilization is an early manifestation of palmitate-induced lipotoxicity in pancreatic β-cells. J. Biol. Chem. 2008, 283, 7936-7948.
36. Kjaer, M. A.; Vegusdal, A.; Gjoen, T.; Rustan, A. C.; Todorcević, M.; Ruyter, B. Effect of rapeseed oil and dietary n-3 fatty acids on triacylglycerol synthesis and secretion in Atlantic salmon hepatocytes. Biochim. Biophys. Acta 2008, 1781, 112-122.
37. Flachs, P.; Horakova, O.; Brauner, P.; Rossmeisl, M.; Pecina, P.; Franssen-van Hal, N.; Ruzickova, J.; Sponarova, J.; Drahota, Z.; Vlcek, C.; Keijer, J.; Houstek, J.; Kopecky, J. Polyunsaturated fatty acids of marine origin upregulate mitochondrial biogenesis and induceβ-oxidation in white fat. Diabetolona 2005, 48, 2365-2375.
38. Leonardi, F.; Attorri, L.; Di Benedetto, R.; Di Biase, A.; Sanchez, M.; Nardini, M.; Salvati, S. Effect of arachidonic, eicosapentaenoic and docosahexaenoic acids on the oxidative status of C6 glioma cells. Free Radical Res 2005, 39, 865 874
39. Kou, W.; Luchtman, D.; Song, C Eicosapentaenoic acid (EPA) increases cell viability and expression of neurotrophin receptors in retinoic acid and brain-derived neurotrophic factor differentiated SH-SY5Y cells. Eur. J. Nutr. 2008, 47, 104-113.
40. Guo, W.; Xie, W.; Lei, T.; Hamilton, J. A. Eicosapentaenoic acid, but not oleic acid, stimulates β-oxidation in adipocytes. Lipids 2005, 40, 815-821.
41. Madsen, L.; Rustan, A. C.; Vaagenes, H.; Berge, K.; Dyroy, E.; Berge, R. K. Eicosapentaenoic and docosahexaenoic acid affect mitochondrial and peroxisomal fatty acid oxidation in relation to substrate preference. Lipids 1999, 34, 951-963.
42. Bas, O.; Songur, A.; Sahin, O.; Mollaoglu, H.; Ozen, O. A.; Yaman, M.; Eser, O.; Fidan, H.; Yagmurca, M. The protective effect offish n-3 fatty acids on cerebral ischemia in rat hippocampus. Neurochem. Int. 2007, 50, 548-554.