Addition of docosahexaenoic acid, but not arachidonic acid, activates glutathione and thioredoxin antioxidant systems in murine hippocampal HT22 cells: Potential implications in neuroprotection

Journal of Neurochemistry

Volumn 131, Issue 4, 2014, Pages 470-483

  Casañas Sánchez, Verõnica ^a   Pérez, José A ^a   Fabelo, Noemí ^a   Herrera Herrera, Antonio V ^a   Fernández, Cecilia ^a   Marín, Raquel ^a   González Montelongo, María C ^a   Díaz, Mario ^a  

^a UNIVERSIDAD DE LA LAGUNA   (Spain)

Author keywords

docosahexaenoic acid; gene expression; hippocampal cells; intron retention; neuroprotection; thioredoxin and glutathione antioxidant systems

Indexed keywords

AMYLOID BETA PROTEIN[25-35]; ARACHIDONIC ACID; DOCOSAHEXAENOIC ACID; GLUTATHIONE; GLUTATHIONE PEROXIDASE; PHOSPHOLIPID HYDROPEROXIDE GLUTATHIONE PEROXIDASE; THIOREDOXIN REDUCTASE; AMYLOID BETA PROTEIN; AMYLOID BETA-PROTEIN (1-42); AMYLOID BETA-PROTEIN (25-35); ANTIOXIDANT; GLUTAREDOXIN; PEPTIDE FRAGMENT; PEROXIREDOXIN; THIOBARBITURIC ACID REACTIVE SUBSTANCE; THIOREDOXIN;

ARTICLE; BRAIN CELL; CONTROLLED STUDY; GENE; GENE EXPRESSION; GENETIC CODE; GPX4 GENE; HIPPOCAMPUS; HT 22 CELL; INTRON; NEUROPROTECTION; PRDX3 GENE; PRIORITY JOURNAL; RNA SPLICING; SRXN1 GENE; TRXRD 1 2 GENE; TXN 1 2 GENE; UPREGULATION; ANIMAL; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECTS; METABOLISM; MOUSE; TIME; TRANSFORMED CELL LINE;

MURINAE;

AMYLOID BETA-PEPTIDES; ANIMALS; ANTIOXIDANTS; ARACHIDONIC ACID; CELL LINE, TRANSFORMED; CELL PROLIFERATION; DOCOSAHEXAENOIC ACIDS; GENE EXPRESSION; GLUTAREDOXINS; GLUTATHIONE; HIPPOCAMPUS; MICE; PEPTIDE FRAGMENTS; PEROXIREDOXINS; THIOBARBITURIC ACID REACTIVE SUBSTANCES; THIOREDOXINS; TIME FACTORS;

EID: 84922391624     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12833     Document Type: Article

References (68)

1. Arnér E. S., and, Holmgren A., (2000) Physiological functions of thioredoxin and thioredoxin reductase. Eur. J. Biochem. 267, 6102-6109.
2. Arnér E. S., Zhong L., and, Holmgren A., (1999) Preparation and assay of mammalian thioredoxin and thioredoxin reductase. Meth. Enzymol. 300, 226-239.
3. Aso E., Lomoio S., Lõpez-González I., et al,. (2012) Amyloid generation and dysfunctional immunoproteasome activation with disease progression in animal model of familial Alzheimer disease. Brain Pathol. 22, 636-653.
4. Behl C., Davis J. B., Lesley R., and, Schubert D., (1994) Hydrogen peroxide mediates amyloid beta protein toxicity. Cell 77, 817-827.
5. Björnstedt M., Hamberg M., Kumar S., Xue J., and, Holmgren A., (1995) Human thioredoxin reductase directly reduces lipid hydroperoxides by NADPH and selenocystine strongly stimulates the reaction via catalytically generated selenols. J. Biol. Chem. 270, 11761-11764.
6. Brand A., Schonfeld E., Isharel I., and, Yavin E., (2008) Docosahexaenoic acid-dependent iron accumulation in oligodendroglia cells protects from hydrogen peroxide-induced damage. J. Neurochem. 105, 1325-1335.
7. Buckley P. T., Khaladkar M., Kim J., and, Eberwine J., (2013) Cytoplasmic intron retention, function, splicing, and the sentinel RNA hypothesis. Wiley Interdiscip Rev RNA, 5, 223-230.
8. Calderon F., and, Kim H. Y., (2004) Docosahexaenoic acid promotes neurite growth in hippocampal neurons. J. Neurochem. 90, 979-988.
9. Carlberg I., and, Mannervik B., (1985) Glutathione reductase. Methods Enzymol. 113, 484-490.
10. Catalá A., (2009) Lipid peroxidation of membrane phospholipids generates hydroxy-alkenals and oxidized phospholipids active in physiological and/or pathological conditions. Chem. Phys. Lipids 157, 1-11.
11. Choi J., Zhang W., Gu X., Chen X., Hong L., Laird J. M., and, Salomon R. G., (2011) Lysophosphatidylcholine is generated by spontaneous deacylation of oxidized phospholipids. Chem. Res. Toxicol. 24, 111-118.
12. Dalfõ E., Portero-Otín M., Ayala V., Martínez A., Pamplona R., and, Ferrer I., (2005) Evidence of oxidative stress in the neocortex in incidental Lewy body disease. J. Neuropathol. Exp. Neurol. 64, 816-830.
13. Dargusch R., and, Schubert D., (2002) Specificity of resistance to oxidative stress. J. Neurochem. 81, 1394-1400.
14. Díaz M., and, Marín R., (2015) Brain polyunsaturated lipids and neurodegenerative diseases, in Nutraceuticals and Functional Foods: Natural Remedy (, Satinder K. B., Surinder K., and, Gurpreet S. D., eds), pp. 387-412. Nova Science Publishers, New York, NY.
15. Díaz M. L., Fabelo N., and, Marin R., (2012) Genotype-induced changes in biophysical properties of frontal cortex lipid raft from APP/PS1 transgenic mice. Front Physiol. 3, 1-10.
16. Dröge W., (2002) Free radicals in the physiological control of cell function. Physiol. Rev. 82, 47-95.
17. Expõsito-Rodríguez M., Borges A. A., Borges-Pérez A., and, Pérez J. A., (2011) Gene structure and spatiotemporal expression profile of tomato genes encoding YUCCA-like flavin monooxygenases: the ToFZY gene family. Plant Physiol. Biochem. 49, 782-791.
18. Fabelo N., Martín V., Santpere G., Marín R., Torrens L., Ferrer I., and, Díaz M., (2011) Severe alterations in lipid composition of frontal cortex lipid rafts from Parkinson's disease and incidental Parkinson's disease. Mol. Med. 17, 1107-1118.
19. Fabelo N., Martín V., Marín R., Santpere G., Aso E., Ferrer I., and, Díaz M., (2012) Evidence for premature lipid raft aging in APP/PS1 double-transgenic mice, a model of familial Alzheimer disease. J. Neuropathol. Exp. Neurol. 71, 868-881.
20. Fabelo N., Martín V., Marín R., Moreno D., Ferrer I., and, Díaz M., (2014) Altered lipid composition in cortical lipid rafts occurs at early stages of sporadic Alzheimer's disease and facilitates APP/BACE1 interactions. Neurobiol. Aging 35, 1801-1812.
21. Habig W. H., Pabst M. J., and, Jakoby W. B., (1974) Glutathione S-transferases-first enzymatic step in mercapturic acid formation. J. Biol. Chem. 249, 7130-7139.
22. Hashimoto M., Shahdat H. M., Yamashita S., et al,. (2008) Docosahexaenoic acid disrupts in vitro amyloid beta(1-40) fibrillation and concomitantly inhibits amyloid levels in cerebral cortex of Alzheimer's disease model rats. J. Neurochem. 107, 1634-1646.
23. Hashimoto M., Katakura M., Hossain S., Rahman A., Shimada T., and, Shido O., (2011) Docosahexaenoic acid withstands the Aβ(25-35)-induced neurotoxicity in SH-SY5Y cells. J. Nutr. Biochem. 22, 22-29.
24. Hattori F., Murayama N., Noshita T., and, Oikawa S., (2003) Mitochondrial peroxiredoxin-3 protects hippocampal neurons from excitotoxic injury in vivo. J. Neurochem. 86, 860-868.
25. Hawkes H. J., Karlenius T. C., and, Tonissen K. F., (2013) Regulation of the human thioredoxin gene promoter and its key substrates: a study of functional and putative regulatory elements. Biochim. Biophys. Acta 840, 303-314.
26. Hellemans J., Mortier G., De Paepe A., Speleman F., and, Vandesompele J., (2007) qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol. 8, R19.
27. Hissin P. J., and, Hilf R., (1976) Afluorometric method for determination of oxidized and reduced glutathione in tissues. Anal. Biochem. 74, 214-226.
28. Huang T. L., (2010) Omega-3 fatty acids, cognitive decline, and Alzheimer's disease: a critical review and evaluation of the literature. J. Alzheimers Dis. 21, 673-690.
29. Imai H., and, Nakagawa Y., (2003) Biological significance of phospholipid hydroperoxide glutathione peroxidase (PHGPx, GPx4) in mammalian cells. Free Radic. Biol. Med. 34, 145-169.
30. Ishikado A., Morino K., Nishio Y., et al,. (2013) 4-Hydroxy hexenal derived from docosahexaenoic acid protects endothelial cells via Nrf2 activation. PLoS ONE 8, e69415.
31. Jeong W., Bae S. H., Toledano M. B., and, Rhee S. G., (2012) Role of sulfiredoxin as a regulator of peroxiredoxin function and regulation of its expression. Free Radic. Bio. Med. 53, 447-456.
32. Jicha G. A., and, Markesbery W. R., (2010) Omega-3 fatty acids: potential role in the management of early Alzheimer's disease. Clin. Interv. Aging 5, 45-61.
33. Jump D. B., and, Clarke S. D., (1999) Regulation of gene expression by dietary fat. Annu. Rev. Nutr. 19, 63-90.
34. Jung K. A., and, Kwak M. K., (2010) The Nrf2 system as a potential target for the development of indirect antioxidants. Molecules 15, 7266-7291.
35. Kaduce T. L., Chen Y., Hell J. W., and, Spector A. A., (2008) Docosahexaenoic acid synthesis from n-3 fatty acid precursors in rat hippocampal neurons. J. Neurochem. 105, 1525-1535.
36. Ke N., Wang X., Xu X., and, Abassi Y. A., (2011) The xCELLigence system for real-time and label-free monitoring of cell viability. Methods Mol. Biol. 740, 33-43.
37. Khaladkar M., Buckley P. T., Lee M. T., Francis C., Eghbal M. M., Chuong T., Suresh S., Kuhn B., Eberwine J., and, Kim J., (2013) Subcellular RNA sequencing reveals broad presence of cytoplasmic intron-sequence retaining transcripts in mouse and rat neurons. PLoS ONE 8, e76194.
38. Kobayashi M., and, Yamamoto M., (2005) Molecular mechanisms activating the Nrf2-Keap1 pathway of antioxidant gene regulation. Antioxid. Redox Signal. 7, 385-394.
39. Kusunoki C., Yang L., Yoshizaki T., et al,. (2013) Omega-3 polyunsaturated fatty acid has an anti-oxidant effect via the Nrf-2/HO-1 pathway in 3T3-L1 adipocytes. Biochem. Biophys. Res. Commun. 430, 225-230.
40. Lawrence R. A., and, Burk R. F., (1976) Glutathione peroxidase activity in selenium-deficient rat liver. Biochem. Biophys. Res. Commun. 71, 952-958.
41. Marin R., Casañas V., Pérez J. A., Fabelo N., Fernandez C. E., and, Diaz M., (2013) Oestrogens as modulators of neuronal signalosomes and brain lipid homeostasis related to protection against neurodegeneration. J. Neuroendocrinol. 25, 1104-1115.
42. Marín R., Ramírez C. M., González M., González-Muñoz E., Zorzano A., Camps M., Alonso R., and, Diaz M., (2007) Voltage-dependent anion channel (VDAC) participates in amyloid beta-induced toxicity and interacts with plasma membrane estrogen receptor alpha in septal and hippocampal neurons. Mol. Membr. Biol. 24, 148-160.
43. Martín V., Almansa E., Fabelo N., and, Díaz M., (2006) Selective enrichment in polyunsaturated fatty acids in phospholipids from neuronal-derived cell lines. J. Neurosci. Methods 153, 230-238.
44. Martín V., Fabelo N., Santpere G., Puig B., Marín R., Ferrer I., and, Díaz M., (2010) Lipid alterations in lipid rafts from Alzheimer's disease human brain cortex. J. Alzheimers Dis. 19, 489-502.
45. McGee R., Jr, (1981) Membrane fatty acid modification of the neuroblastoma x glioma hybrid, NG108-15. Biochim. Biophys. Acta 663, 314-328.
46. Niemoller T. D., Stark D. T., and, Bazan N. G., (2009) Omega-3 fatty acid docosahexaenoic acid is the precursor of neuroprotectin D1 in the nervous system, in Omega-3 Fatty Acids, the Brain and Retina (, Simopoulos A. P., and, Bazan N. G., eds), pp. 46-54. World Rev Nutr Diet. Karger, Basel.
47. Niki E., Yoshida Y., Saito Y., and, Noguchi N., (2005) Lipid peroxidation: mechanisms, inhibition, and biological effects. Biochem. Biophys. Res. Commun. 338, 668-676.
48. Nolan T., Hands R. E., and, Bustin S. A., (2006) Quantification of mRNA using real-time RT-PCR. Nat. Protoc. 1, 1559-1582.
49. Ohkawa H., Ohishi N., and, Yagi K., (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 95, 351-358.
50. Okado-Matsumoto A., Matsumoto A., Fujii J., and, Taniguchi N., (2000) Peroxiredoxin IV is a secretable protein with heparin-binding properties under reduced conditions. J. Biochem. 127, 493-501.
51. Pan H. C., Kao T. K., Ou Y. C., et al,. (2009) Protective effect of docosahexaenoic acid against brain injury in ischemic rats. J. Nutr. Biochem. 20, 715-725.
52. Pfaffl M. W., Horgan G. W., and, Dempfle L., (2002) Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30, e36.
53. Rhee S. G., Chae H. Z., and, Kim K., (2005) Peroxiredoxins: a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling. Free Radic. Biol. Med. 38, 1543-1552.
54. Saito M., (2000) Dietary docosahexaenoic acid does not promote tissue lipid peroxide formation to the extent expected from the peroxidizability index of the lipids. BioFactors 13, 15-24.
55. Saito M., and, Kubo K., (2003) Relationship between tissue lipid peroxidation and peroxidizability index after alpha-linolenic, eicosapentaenoic, or docosahexaenoic acid intake in rats. Br. J. Nutr. 89, 19-28.
56. SanGiovanni J. P., and, Chew E. Y., (2005) The role of omega-3 long-chain polyunsaturated fatty acids in health and disease of the retina. Prog. Retin. Eye Res. 24, 87-138.
57. Savaskan N. E., Ufer C., Kühn H., and, Borchert A., (2007) Molecular biology of glutathione peroxidase 4: from genomic structure to developmental expression and neural function. Biol. Chem. 388, 1007-1017.
58. Scheerer P., Borchert A., Krauss N., Wessner H., Gerth C., Höhne W., and, Kuhn H., (2007) Structural basis for catalytic activity and enzyme polymerization of phospholipid hydroperoxide glutathione peroxidase-4 (GPx4). Biochemistry 46, 9041-9049.
59. Schmitz G., and, Ecker J., (2008) The opposing effects of n-3 and n-6 fatty acids. Prog. Lipid Res. 47, 147-155.
60. Singh S., Vrishni S., Singh B. K., Rahman I., and, Kakkar P., (2010) Nrf2-ARE stress response mechanism: a control point in oxidative stress-mediated dysfunctions and chronic inflammatory diseases. Free Radic. Res. 44, 1267-1288.
61. Stillwell W., and, Wassal S. R., (2003) Docosahexaenoic acid: membrane properties of a unique fatty acid. Chem. Phys. Lipids 126, 1-27.
62. Tanaka R., Sugiura Y., and, Matsushita T., (2013) Simultaneous identification of 4-hydroxy-2-hexenal and 4-hydroxy-2-nonenal in foods by pre-column fluorigenic labeling with 1,3-ciclohexanedione and reversed-phase-high-performance liquid chromatography with fluorescence detection. J. Liquid Chromatogr. Rel. Tech. 36, 881-896.
63. Tanaka R., Shigeta K., Sugiura Y., Hatate H., and, Matsushita T., (2014) Accumulation of hydroxyl lipids and 4-hydroxy-2-hexenal in live fish infected with fish diseases. Lipids 49, 385-396.
64. Valko M., Leibfritz D., Moncol J., Cronin M. T., Mazur M., and, Telser J., (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 39, 44-84.
65. Van Kuijk F. J., Holte L. L., and, Dratz E. A., (1990) 4-Hydroxyhexenal: a lipid peroxidation product derived from oxidized docosahexaenoic acid. Biochim. Biophys. Acta 1043, 116-118.
66. Yang Y. C., Lii C. K., Wei Y. L., Li C. C., Lu C. Y., Liu K. L., and, Chen H. W., (2013) Docosahexaenoic acid inhibition of inflammation is partially via cross-talk between Nrf2/hemeoxygenase 1 and IKK/NF-κB pathways. J. Nutr. Biochem. 24, 204-212.
67. Yavin E., Glozman S., and, Green P., (2001) Docosahexaenoic acid accumulation in the prenatal brain: prooxidant and antioxidant features. J. Mol. Neurosci. 16, 229-235.
68. Zhang M., An C., Gao Y., Leak R. K., Chen J., and, Zhang F., (2013) Emerging roles of Nrf2 and phase II antioxidant enzymes in neuroprotection. Prog. Neurobiol. 100, 30-47.