Dimethyl fumarate modulates antioxidant and lipid metabolism in oligodendrocytes

Redox Biology

Volumn 5, Issue , 2015, Pages 169-175

  Huang, He ^a   Taraboletti, Alexandra ^a   Shriver, Leah P ^a  

^a UNIVERSITY OF AKRON   (United States)

Author keywords

Hydrophilic interaction liquid chromatography; Metabolomics; Neuroprotection; Oligodendrocyte; Shotgun lipidomics

Indexed keywords

ANTIOXIDANT; FATTY ACID; FUMARIC ACID DIMETHYL ESTER; KELCH LIKE ECH ASSOCIATED PROTEIN 1; MYELIN; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLINOSITOL; PHOSPHATIDYLSERINE; SPHINGOMYELIN; TRANSCRIPTION FACTOR NRF2; HYDROGEN PEROXIDE; IMMUNOSUPPRESSIVE AGENT;

AMINO ACID METABOLISM; ARTICLE; CELL METABOLISM; CELL VIABILITY; CONTROLLED STUDY; DEMYELINATION; FATTY ACID SYNTHESIS; HUMAN; HUMAN CELL; HYDROPHILIC INTERACTION CHROMATOGRAPHY; LIPID METABOLISM; LIPIDOMICS; LIPOGENESIS; METABOLOMICS; MYELIN SHEATH; OLIGODENDROGLIA; OXIDATIVE STRESS; PRIORITY JOURNAL; SIGNAL NOISE RATIO; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; UPREGULATION; CELL LINE; CHEMICAL PHENOMENA; CITRIC ACID CYCLE; CYTOLOGY; DRUG EFFECTS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; METABOLISM; METABOLOME; PRINCIPAL COMPONENT ANALYSIS;

CELL LINE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CITRIC ACID CYCLE; DIMETHYL FUMARATE; HUMANS; HYDROGEN PEROXIDE; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; IMMUNOSUPPRESSIVE AGENTS; LIPID METABOLISM; METABOLOME; OLIGODENDROGLIA; PRINCIPAL COMPONENT ANALYSIS; TANDEM MASS SPECTROMETRY;

EID: 84930937164     PISSN: 22132317     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.redox.2015.04.011     Document Type: Article

References (52)

1. Kaddurah-Daouk R., Kristal B.S., Weinshilboum R.M. Metabolomics: a global biochemical approach to Drug response and disease. Annual Review of Pharmacology and Toxicology 2008, 48(1):653-683. http://www.ncbi.nlm.nih.gov/pubmed/18184107, 10.1146/annurev.pharmtox.48.113006.094715.
2. Madsen R., Lundstedt T., Trygg J. Chemometrics in metabolomics - a review in human disease diagnosis. Analytica Chimica Acta 2010, 659(1-2):23-33. http://www.ncbi.nlm.nih.gov/pubmed/20103103, 10.1016/j.aca.2009.11.042.
3. Theodoridis G., Gika H.G., Wilson I.D. LC-MS-based methodology for global metabolite profiling in metabonomics/metabolomics. Trends in Analytical Chemistry 2008, 27(3):251-260. 10.1016/j.trac.2008.01.008.
4. Lu W., Bennett B.D., Rabinowitz J.D. Analytical strategies for LC-MS-based targeted metabolomics. Journal of Chromatography B Analytical Technologies in the Biomedical and Life Sciences 2008, 871(2):236-242. http://www.ncbi.nlm.nih.gov/pubmed/18502704, 10.1016/j.jchromb.2008.04.031.
5. Han X., Gross R.W. Shotgun lipidomics: electrospray ionization mass spectrometric analysis and quantitation of cellular lipidomes directly from crude extracts of biological samples. Mass Spectrometry Reviews 2005, 24(3):367-412. http://www.ncbi.nlm.nih.gov/pubmed/15389848, 10.1002/mas.20023.
6. Simons M., Trajkovic K. Neuron-glia communication in the control of oligodendrocyte function and myelin biogenesis. Journal of Cell Science 2006, 119(21):4381-4389. http://www.ncbi.nlm.nih.gov/pubmed/17074832, 10.1242/jcs.03242.
7. Trapp B.D., Nave K.A. Multiple sclerosis: an immune or neurodegenerative disorder?. Annual Review of Neuroscence 2008, 31:247-269. http://www.ncbi.nlm.nih.gov/pubmed/18558855, 10.1146/annurev.neuro.30.051606.094313.
8. Gilgun-Sherki Y., Melamed E., Offen D. The role of oxidative stress in the pathogenesis of multiple sclerosis: the need for effective antioxidant therapy. Journal of Neurology 2004, 251(3):261-268. http://www.ncbi.nlm.nih.gov/pubmed/15015004, 10.1007/s00415-004-0348-9.
9. LeVine S.M. The role of reactive oxygen species in the pathogenesis of multiple sclerosis. Medical Hypotheses 1992, 39(3):271-274. http://www.ncbi.nlm.nih.gov/pubmed/1335545, 10.1016/0306-9877(92)90121-R.
10. Zhang J., et al. Promoting myelin repair and return of function in multiple sclerosis. FEBS Letter 2011, 585(23):3813-3820. http://www.ncbi.nlm.nih.gov/pubmed/21864535, 10.1016/j.febslet.2011.08.017.
11. Phillips, J., Fox, R., BG-12 in Multiple Sclerosis. Seminars in Neurology, 33(01) 056-065 [doi:10.1055/s-0033-1343796].
12. Duffy S., So A., Murphy T.H. Activation of endogenous antioxidant defenses in neuronal cells prevents free radical-mediated damage. Journal of Neurochemistry 1998, 71(1):69-77. http://www.ncbi.nlm.nih.gov/pubmed/9648852, 10.1046/j.1471-4159.1998.71010069.x.
13. Lin S.X., et al. The anti-inflammatory effects of dimethyl fumarate in astrocytes involve glutathione and haem oxygenase-1. ASN NEURO 2011, 3(2). http://www.ncbi.nlm.nih.gov/pubmed/21382015, 10.1042/AN20100033.
14. Scannevin R.H., et al. Fumarates promote cytoprotection of central nervous system cells against oxidative stress via the nuclear factor (erythroid-derived 2)-like 2 pathway. Journal of Pharmacology and Experimental Therapeutics 2012, 341(1):274-284. http://www.ncbi.nlm.nih.gov/pubmed/22267202, 10.1124/jpet.111.190132.
15. Arnold D.L., et al. Magnetization transfer ratio in the delayed-release dimethyl fumarate DEFINE study. Journal of Neurology 2014, 261(12):2429-2437. 10.1007/s00415-014-7504-7.
16. Moharregh-Khiabani D., et al. Effects of fumaric acids on cuprizone induced central nervous system de- and remyelination in the mouse. PLoS One 2010, 5(7):e11769. http://www.ncbi.nlm.nih.gov/pubmed/20668697, 10.1371/journal.pone.0011769.
17. Wierinckx A., et al. Detoxication enzyme inducers modify cytokine production in rat mixed glial cells. Journal of Neuroimmunology 2005, 166(1-2):132-143. http://www.ncbi.nlm.nih.gov/pubmed/15993952, 10.1016/j.jneuroim.2005.05.013.
18. Bligh E.G., Dyer W.J. A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology 1959, 37(8):911-917. http://www.ncbi.nlm.nih.gov/pubmed/13671378, 10.1139/o59-099.
19. Smith P.K., et al. Measurement of protein using bicinchoninic acid. Analytical Biochemistry 1985, 150(1):76-85. http://www.ncbi.nlm.nih.gov/pubmed/3843705, 10.1016/0003-2697(85)90442-7.
20. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. Journal of Immunological Methods 1983, 65(1-2):55-63. http://www.ncbi.nlm.nih.gov/pubmed/6606682, 10.1016/0022-1759(83)90303-4.
21. Simons B., et al. Shotgun lipidomics by sequential precursor ION fragmentation on a hybrid quadrupole time-of-flight mass spectrometer. Metabolitess 2012, 2(1):195-213. http://www.ncbi.nlm.nih.gov/pubmed/24957374, 10.3390/metabo2010195.
22. Storey J.D., Tibshirani R. Statistical significance for genomewide studies. Proceedings of the National Academy of Sciences of the United States of America 2003, 100(16):9440-9445. http://www.ncbi.nlm.nih.gov/pubmed/12883005, 10.1073/pnas.1530509100.
23. Smith C.A., et al. METLIN: a metabolite mass spectral database. Therapeutic Drug Monitoring 2005, 27(6):747-751. http://www.ncbi.nlm.nih.gov/pubmed/16404815, 10.1097/01.ftd.0000179845.53213.39.
24. Tautenhahn R., et al. An accelerated workflow for untargeted metabolomics using the METLIN database. Nature Biotechnology 2012, 30(9):826-828. http://www.ncbi.nlm.nih.gov/pubmed/22965049, 10.1038/nbt.2348.
25. Zhu Z.J., et al. Liquid chromatography quadrupole time-of-flight mass spectrometry characterization of metabolites guided by the METLIN database. Nature Protocols 2013, 8(3):451-460. http://www.ncbi.nlm.nih.gov/pubmed/23391889, 10.1038/nprot.2013.004.
26. Wishart D.S., et al. HMDB 3.0 - the human Metabolome Database in 2013. Nucleic Acids Research 2013, 41:D801-D807. http://www.ncbi.nlm.nih.gov/pubmed/23161693, 10.1093/nar/gks1065.
27. Haider L., et al. Oxidative damage in multiple sclerosis lesions. Brain 2011, 134(7):1914-1924. http://www.ncbi.nlm.nih.gov/pubmed/21653539, 10.1093/brain/awr128.
28. van Horssen J., et al. Severe oxidative damage in multiple sclerosis lesions coincides with enhanced antioxidant enzyme expression. Free Radical Biology and Medicine 2008, 45(12):1729-1737. http://www.ncbi.nlm.nih.gov/pubmed/18930811, 10.1016/j.freeradbiomed.2008.09.023.
29. Brigelius-Flohé R., Flohé L. Basic principles and emerging concepts in the redox control of transcription factors. Antioxidants and Redox Signaling 2011, 15(8):2335-2381. http://www.ncbi.nlm.nih.gov/pubmed/21194351, 10.1089/ars.2010.3534.
30. Gerdes S., Shakery K., Mrowietz U. Dimethylfumarate inhibits nuclear binding of nuclear factor kappaB but not of nuclear factor of activated T cells and CCAAT/enhancer binding protein beta in activated human T cells. British Journal of Dermatology 2007, 156(5):838-842. http://www.ncbi.nlm.nih.gov/pubmed/17381463, 10.1111/j.1365-2133.2007.07779.x.
31. Marino G., et al. Dimethylα-ketoglutarate inhibits maladaptive autophagy in pressure overload-induced cardiomyopathy. Autophagy 2014, 10(5):930-932. 10.4161/auto.28235.
32. Zhang T.M., Sener A., Malaisse W.J. Metabolic effects and fate of succinic acid methyl esters in rat hepatocytes. Archives of Biochemistry and Biophysics 1994, 314(1):186-192. http://www.ncbi.nlm.nih.gov/pubmed/7944393, 10.1006/abbi.1994.1428.
33. Chouchani E.T., et al. Ischaemic accumulation of succinate controls reperfusion injury through mitochondrial ROS. Nature 2014, 515(7527):431-435. http://www.ncbi.nlm.nih.gov/pubmed/25383517, 10.1038/nature13909.
34. Choi I.-Y., et al. Lower levels of glutathione in the brains of secondary progressive multiple sclerosis patients measured by 1H magnetic resonance chemical shift imaging at 3T. Multiple Sclerosis 2011, 17(3):289-296. http://www.ncbi.nlm.nih.gov/pubmed/20921235, 10.1177/1352458510384010.
35. Srinivasan R., et al. MR spectroscopic imaging of glutathione in the white and gray matter at 7 T with an application to multiple sclerosis. Magnetic Resonance Imaging 2010, 28(2):163-170. http://www.ncbi.nlm.nih.gov/pubmed/19695821, 10.1016/j.mri.2009.06.008.
36. Albrecht P., et al. Effects of dimethyl fumarate on neuroprotection and immunomodulation. Journal of Neuroinflammation 2012, 9(1):163. 10.1186/1742-2094-9-163.
37. Brennan M.S., et al. Dimethyl fumarate and monoethyl fumarate exhibit differential effects on KEAP1, NRF2 activation, and glutathione depletion in vitro. PLoS One 2015, 10(3). http://www.ncbi.nlm.nih.gov/pubmed/25793262, 10.1371/journal.pone.0120254.
38. Arockia Rani P.J., Panneerselvam C. Carnitine as a free radical scavenger in aging. Experimental Gerontology 2001, 36(10):1713-1726. http://www.ncbi.nlm.nih.gov/pubmed/11672991, 10.1016/S0531-5565(01)00116-4.
39. Vamos E., et al. Neuroprotective effects of l-carnitine in a transgenic animal model of Huntington's disease. Biomedicine and Pharmacotherapy 2010, 64(4):282-286. http://www.ncbi.nlm.nih.gov/pubmed/19932584, 10.1016/j.biopha.2009.06.020.
40. May J.M. Vitamin C transport and its role in the central nervous system. Subcellular Biochemistry 2012, 56:85-103. http://www.ncbi.nlm.nih.gov/pubmed/22116696, 10.1007/978-94-007-2199-9_6.
41. Gess B., et al. Sodium-dependent vitamin C transporter 2 deficiency causes hypomyelination and extracellular matrix defects in the peripheral nervous system. Journal of Neuroscience 2011, 31(47):17180-17192. http://www.ncbi.nlm.nih.gov/pubmed/22114285, 10.1523/JNEUROSCI.3457-11.2011.
42. Buettner G.R. The pecking order of free radicals and antioxidants: lipid peroxidation, alpha-tocopherol, and ascorbate. Archives of Biochemistry and Biophysics 1993, 300(2):535-543. http://www.ncbi.nlm.nih.gov/pubmed/8434935, 10.1006/abbi.1993.1074.
43. Jing X., et al. Dimethyl fumarate attenuates 6-OHDA-induced neurotoxicity in SH-SY5Y cells and in animal model of Parkinson's disease by enhancing Nrf2 activity. Neuroscience 2015, 286:131-140. http://www.ncbi.nlm.nih.gov/pubmed/25449120, 10.1016/j.neuroscience.2014.11.047.
44. Thiessen A., Schmidt M.M., Dringen R. Fumaric acid dialkyl esters deprive cultured rat oligodendroglial cells of glutathione and upregulate the expression of heme oxygenase 1. Neuroscience Letters 2010, 475(1):56-60. http://www.ncbi.nlm.nih.gov/pubmed/20347008, 10.1016/j.neulet.2010.03.048.
45. Barateiro A., Fernandes A. Temporal oligodendrocyte lineage progression: in vitro models of proliferation, differentiation and myelination. Biochimica et Biophysica Acta 2014, 1843(9):1917-1929. http://www.ncbi.nlm.nih.gov/pubmed/24768715, 10.1016/j.bbamcr.2014.04.018.
46. Wood T.L., et al. mTOR: a link from the extracellular milieu to transcriptional regulation of oligodendrocyte development. ASN NEURO 2013, 5(1):e00108. http://www.ncbi.nlm.nih.gov/pubmed/23421405, 10.1042/AN20120092.
47. Lee Y., et al. Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature 2012, 487(7408):443-448. http://www.ncbi.nlm.nih.gov/pubmed/22801498, 10.1038/nature11314.
48. Budin I., Devaraj N.K. Membrane assembly driven by a biomimetic coupling reaction. Journal of American Chemical Society 2012, 134(2):751-753. http://www.ncbi.nlm.nih.gov/pubmed/22239722, 10.1021/ja2076873.
49. Paz Soldán M.M., Pirko I. Biogenesis and significance of central nervous system myelin. Seminars in Neurology 2012, 32(1):9-14. http://www.ncbi.nlm.nih.gov/pubmed/22422202, 10.1055/s-0032-1306381.
50. Baumann N., Pham-Dinh D. Biology of oligodendrocyte and myelin in the mammalian central nervous system. Physiological Reviews 2001, 81(2):871-927. http://www.ncbi.nlm.nih.gov/pubmed/11274346.
51. Hayes J.D., Dinkova-Kostova A.T. The Nrf2 regulatory network provides an interface between redox and intermediary metabolism. Trends in Biochemical Sciences 2014, 39(4):199-218. http://www.ncbi.nlm.nih.gov/pubmed/24647116, 10.1016/j.tibs.2014.02.002.
52. Linker R.A., et al. Fumaric acid esters exert neuroprotective effects in neuroinflammation via activation of the Nrf2 antioxidant pathway. Brain 2011, 134(3):678-692. http://www.ncbi.nlm.nih.gov/pubmed/21354971, 10.1093/brain/awq386.