Insights into the role of oxidative stress in the pathology of friedreich ataxia using peroxidation resistant polyunsaturated fatty acids

Redox Biology

Volumn 1, Issue 1, 2013, Pages 398-404

  Cotticelli, M Grazia ^a   Crabbe, Andrew M ^a   Wilson, Robert B ^a   Shchepinov, Mikhail S ^b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b Retrotope Inc   (United States)

Author keywords

Deuterated PUFAs; Friedreich ataxia; Linoleic acid; Linolenic acid; Oxidative stress

Indexed keywords

HYDROGEN; IDEBENONE; LINOLEIC ACID; LINOLENIC ACID; POLYUNSATURATED FATTY ACID; REACTIVE OXYGEN METABOLITE; UNSATURATED FATTY ACID;

ANIMAL CELL; ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; FIBROBLAST; FRIEDREICH ATAXIA; HUMAN; HUMAN CELL; LIPID PEROXIDATION; MOUSE; NEUROPATHOLOGY; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; YEAST CELL; ANIMAL; METABOLISM; PATHOLOGY;

ANIMALS; FATTY ACIDS, UNSATURATED; FRIEDREICH ATAXIA; HUMANS; LIPID PEROXIDATION; MICE; OXIDATIVE STRESS;

EID: 84883021878     PISSN: 22132317     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.redox.2013.06.004     Document Type: Article

References (59)

1. Schmucker S., Puccio H. Understanding the molecular mechanisms of Friedreich's ataxia to develop therapeutic approaches. Human Molecular Genetics 2010, 19(R1):R103-R110.
2. Santos R., Lefevre S., Sliwa D., Seguin A., Camadro J.M., Lesuisse E. Friedreich ataxia: molecular mechanisms, redox considerations, and therapeutic opportunities. Antioxidants and Redox Signaling 2010, 13(5):651-690.
3. Stemmler T.L., Lesuisse E., Pain D., Dancis A. Frataxin and mitochondrial FeS cluster biogenesis. Journal of Biological Chemistry 2010, 285(35):26737-26743.
4. Marmolino D. Friedreich's ataxia: past, present and future. Brain Research Reviews 2011, 67(1-2):311-330.
5. Koeppen A.H. Friedreich's ataxia: pathology, pathogenesis, and molecular genetics. Journal of the Neurological Sciences 2011, 303(1-2):1-12.
6. Muhlenhoff U., Richhardt N., Ristow M., Kispal G., Lill R. The yeast frataxin homolog Yfh1p plays a specific role in the maturation of cellular Fe/S proteins. Human Molecular Genetics 2002, 11:2025-2036.
7. Muhlenhoff U., Gerber J., Richhardt N., Lill R. Components involved in assembly and dislocation of iron-sulfur clusters on the scaffold protein Isu1p. EMBO Journal 2003, 22(18):4815-4825.
8. Babcock M., de Silva D., Oaks R., Davis-Kaplan S., Jiralerspong S., Montermini L., et al. Regulation of mitochondrial iron accumulation by Yfh1p, a putative homolog of Frataxin. Science 1997, 276:1709-1712.
9. Wilson R.B., Roof D.M. Respiratory deficiency due to loss of mitochondrial DNA in yeast lacking the frataxin homologue. Nature Genetics 1997, 16:352-357.
10. Foury F., Cazzalini O. Deletion of the yeast homologue of the human gene associated with Friedreich's ataxia elicits iron accumulation in mitochondria. FEBS Letters 1997, 411:373-377.
11. Radisky D.C., Babcock M.C., Kaplan J.K. The yeast frataxin homologue mediates mitochondrial iron efflux: evidence for a mitochondrial iron cycle. Journal of Biological Chemistry 1999, 274:4497-4499.
12. Foury F. Low iron concentration and aconitase deficiency in a yeast frataxin homologue deficient strain. FEBS Letters 1999, 456(2):281-284.
13. Rotig A., de Lonlay P., Chretien D., Foury F., Koenig M., Sidi D., et al. Aconitase and mitochondrial iron-sulphur protein deficiency in Friedreich's ataxia. Nature Genetics 1997, 17:215-217.
14. Bradley J.L., Blake J.C., Chamberlain S., Thomas P.K., Cooper J.M., Schapira A.H. Clinical biochemical and molecular genetic correlations in Friedreich's ataxia. Human Molecular Genetics 2000, 9(2):275-282.
15. Lodi R., Cooper J.M., Bradley J.L., Manners D., Styles P., Taylor D.J., et al. Deficit of in vivo mitochondrial ATP production in patients with Friedreich ataxia'. Proceedings of the National Academy of Sciences of the United States of America 1999, 96:11492-11495.
16. Lodi R., Hart P.E., Rajagopalan B., Taylor D.J., Crilley J.G., Bradley J.L., et al. Antioxidant treatment improves in vivo cardiac and skeletal muscle bioenergetics in patients with Friedreich's ataxia. Annals of Neurology 2001, 49:590-596.
17. Puccio H., Simon D., Cossee M., Criqui-Filipe P., Tiziano F., Melki J., et al. Mouse models for Friedreich ataxia exhibit cardiomyopathy, sensory nerve defect and Fe-S enzyme deficiency followed by intramitochondrial iron deposits. Nature Genetics 2001, 27(2):181-186.
18. Lynch D.R., Lech G., Farmer J.M., Balcer L.J., Bank W., Chance B., et al. Near-infrared muscle spectroscopy in patients with Friedreich's ataxia. Muscle and Nerve 2002, 25(5):664-673.
19. Schulz J.B., Dehmer T., Schols L., Mende H., Hardt C., Vorgerd M., et al. Oxidative stress in patients with Friedreich ataxia. [see comments]. Neurology 2000, 55(11):1719-1721.
20. Emond M., Lepage G., Vanasse M., Pandolfo M. Increased levels of plasma malondialdehyde in Friedreich ataxia. [see comments]. Neurology 2000, 55(11):1752-1753.
21. Li K., Besse E.K., Ha D., Kovtunovych G., Rouault T.A. Iron-dependent regulation of frataxin expression: implications for treatment of Friedreich ataxia. Human Molecular Genetics 2008, 17(15):2265-2273.
22. Kakhlon O., Manning H., Breuer W., Melamed-Book N., Lu C., Cortopassi G., et al. Cell functions impaired by frataxin deficiency are restored by drug-mediated iron relocation. Blood 2008, 112(13):5219-5227.
23. Armstrong J.S., Khdour O., Hecht S.M. Does oxidative stress contribute to the pathology of Friedreich's ataxia? A radical question. FASEB Journal 2010, 24(7):2152-2163.
24. Horton A.A., Fairhurst S. Lipid peroxidation and mechanisms of toxicity. Critical Reviews in Toxicology 1987, 18(1):27-79.
25. Bucher J.R., Tien M., Aust S.D. The requirement for ferric in the initiation of lipid peroxidation by chelated ferrous iron. Biochemical and Biophysical Research Communications 1983, 111(3):777-784.
26. Braughler J.M., Duncan L.A., Chase R.L. The involvement of iron in lipid peroxidation. Importance of ferric to ferrous ratios in initiation. Journal of Biological Chemistry 1986, 261(22):10282-10289.
27. Reed T.T. Lipid peroxidation and neurodegenerative disease. Free Radical Biology and Medicine 2011, 51(7):1302-1319.
28. Bowry V.W., Stocker R. Tocopherol-mediated peroxidation. The prooxidant effect of vitamin E on the radical-initiated oxidation of human low-density lipoprotein. Journal of the American Chemical Society 1993, 115:6029-6044.
29. Rustin P., von Kleist-Retzow J.C., Chantrel-Groussard K., Sidi D., Munnich A., Rotig A. Effect of idebenone on cardiomyopathy in Friedreich's ataxia: a preliminary study. Lancet 1999, 354(9177):477-479.
30. Hausse A.O., Aggoun Y., Bonnet D., Sidi D., Munnich A., Rotig A., et al. Idebenone and reduced cardiac hypertrophy in Friedreich's ataxia. [see comments.]. Heart 2002, 87:346-349.
31. Mariotti C., Solari A., Torta D., Marano L., Fiorentini C., Di Donato S. Idebenone treatment in Friedreich patients: one-year-long randomized placebo-controlled trial. Neurology 2003, 60(10):1676-1679.
32. Buyse G., Mertens L., Di Salvo G., Matthijs I., Weidemann F., Eyskens B., et al. Idebenone treatment in Friedreich's ataxia: neurological, cardiac, and biochemical monitoring. Neurology 2003, 60(10):1679-1681.
33. Barnham K.J., Masters C.L., Bush A.I. Neurodegenerative diseases and oxidative stress. Nature Reviews Drug Discovery 2004, 3(3):205-214.
34. Di Prospero N.A., Sumner C.J., Penzak S.R., Ravina B., Fischbeck K.H., Taylor J.P. Safety, tolerability, and pharmacokinetics of high-dose idebenone in patients with Friedreich ataxia. Archives of Neurology 2007, 64(6):803-808.
35. Zimniak P. Detoxification reactions: relevance to aging. Ageing Research Reviews 2008, 7(4):281-300.
36. Niki E. Lipid peroxidation: physiological levels and dual biological effects. Free Radical Biology and Medicine 2009, 47(5):469-484.
37. Sugiyama Y., Fujita T., Matsumoto M., Okamoto K., Imada I. Effects of idebenone (CV-2619) and its metabolites on respiratory activity and lipid peroxidation in brain mitochondria from rats and dogs. Journal of Pharmacobiodynamics 1985, 8(12):1006-1017.
38. Lynch D.R., Perlman S.L., Meier T. A phase 3, double-blind, placebo-controlled trial of idebenone in friedreich ataxia. Archives of Neurology 2010, 67(8):941-947.
39. Meier T., Perlman S.L., Rummey C., Coppard N.J., Lynch D.R. Assessment of neurological efficacy of idebenone in pediatric patients with Friedreich's ataxia: data from a 6-month controlled study followed by a 12-month open-label extension study. Journal of Neurology 2011, 22.
40. Lagedrost S.J., Sutton M.S., Cohen M.S., Satou G.M., Kaufman B.D., Perlman S.L., et al. Idebenone in Friedreich ataxia cardiomyopathy-results from a 6-month phase III study (IONIA). American Heart Journal 2011, 161(3). (639-45.e1).
41. Cunnane S.C. Problems with essential fatty acids: time for a new paradigm?. Progress in Lipid Research 2003, 42(6):544-568.
42. Brenner R.R. The oxidative desaturation of unsaturated fatty acids in animals. Molecular and Cellular Biochemistry 1974, 3(1):41-52.
43. Innis S.M. Fatty acids and early human development. Early Human Development 2007, 83(12):761-766.
44. Alessandri J.M., Guesnet P., Vancassel S., Astorg P., Denis I., Langelier B., et al. Polyunsaturated fatty acids in the central nervous system: evolution of concepts and nutritional implications throughout life. Reproduction Nutrition Development 2004, 44(6):509-538.
45. Kagan V.E., Tyurin V.A., Jiang J., Tyurina Y.Y., Ritov V.B., Amoscato A.A., et al. Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors. Nature Chemical Biology 2005, 1(4):223-232.
46. Yin H., Xu L., Porter N.A. Free radical lipid peroxidation: mechanisms and analysis. Chemical Reviews 2011, 111(10):5944-5972.
47. Dobretsov G.E., Borschevskaya T.A., Petrov V.A., Vladimirov Y.A. The increase of phospholipid bilayer rigidity after lipid peroxidation. FEBS Letters 1977, 84(1):125-128.
48. Halliwell B., Chirico S. Lipid peroxidation: its mechanism, measurement, and significance. American Journal of Clinical Nutrition 1993, 57(5 Suppl.):715S-724S. (discussion 24S-25S).
49. Hill S., Hirano K., Shmanai V.V., Marbois B.N., Vidovic D., Bekish A.V., et al. Isotope-reinforced polyunsaturated fatty acids protect yeast cells from oxidative stress. Free Radical Biology and Medicine 2011, 50(1):130-138.
50. Shchepinov M.S., Chou V.P., Pollock E., Langston J.W., Cantor C.R., Molinari R.J., et al. Isotopic reinforcement of essential polyunsaturated fatty acids diminishes nigrostriatal degeneration in a mouse model of Parkinson's disease. Toxicology Letters 2011, 207(2):97-103.
51. Hill S., Lamberson C.R., Xu L., To R., Tsui H.S., Shmanai V.V., et al. Small amounts of isotope-reinforced polyunsaturated fatty acids suppress lipid autoxidation. Free Radical Biology and Medicine 2012.
52. Foulks J.M., Weyrich A.S., Zimmerman G.A., McIntyre T.M. A yeast PAF acetylhydrolase ortholog suppresses oxidative death. Free Radical Biology and Medicine 2008, 45(4):434-442.
53. Hill S., Lamberson C.R., Xu L., To R., Tsui H.S., Shmanai V.V., et al. Small amounts of isotope-reinforced polyunsaturated fatty acids suppress lipid autoxidation. Free Radical Biology and Medicine 2012, 53(4):893-906.
54. Calmels N., Schmucker S., Wattenhofer-Donze M., Martelli A., Vaucamps N., Reutenauer L., et al. The first cellular models based on frataxin missense mutations that reproduce spontaneously the defects associated with Friedreich ataxia. PLoS One 2009, 4(7):e6379.
55. Cotticelli M.G., Rasmussen L., Kushner N.L., McKellip S., Sosa M.I., Manouvakhova A., et al. Primary and secondary drug screening assays for Friedreich ataxia. Journal of Biomolecular Screening 2012, 17(3):303-313.
56. Lynch D.R., Willi S.M., Wilson R.B., Cotticelli M.G., Brigatti K.W., Deutsch E.C., et al. A0001 in Friedreich ataxia: biochemical characterization and effects in a clinical trial. Movement Disorders 2012, 27(8):1026-1033.
57. Drummen G.P., van Liebergen L.C., Op den Kamp J.A., Post J.A. C11-BODIPY(581/591), an oxidation-sensitive fluorescent lipid peroxidation probe: (micro)spectroscopic characterization and validation of methodology. Free Radical Biology and Medicine 2002, 33(4):473-490.
58. MacDonald M.L., Murray I.V., Axelsen P.H. Mass spectrometric analysis demonstrates that BODIPY 581/591 C11 overestimates and inhibits oxidative lipid damage. Free Radical Biology and Medicine 2007, 42(9):1392-1397.
59. Shchepinov M.S. Reactive oxygen species, isotope effect, essential nutrients, and enhanced longevity. Rejuvenation Research 2007, 10(1):47-59.