Docosahexaenoic (DHA) modulates phospholipid-hydroperoxide glutathione peroxidase (Gpx4) gene expression to ensure self-protection from oxidative damage in hippocampal cells

Frontiers in Physiology

Volumn 6, Issue JUL, 2015, Pages

  Casañas Sánchez, Verónica ^a   Pérez, José A ^a   Fabelo, Noemí ^a   Quinto Alemany, David ^a   Díaz, Mario L ^a  

^a UNIVERSIDAD DE LA LAGUNA   (Spain)

Author keywords

Docosahexaenoic acid; Glutathione peroxidase 4; Hippocampal cells; Intron retention; Neuroprotection; Phospholipid hydroperoxide glutathione peroxidase; Transcriptional regulation

Indexed keywords

2 HEXENAL; 4 HYDROXY 2 HEXENAL; DOCOSAHEXAENOIC ACID; FATTY ACID BINDING PROTEIN; GLUTAREDOXIN; GLUTATHIONE; GLUTATHIONE PEROXIDASE; HYDROGEN PEROXIDE; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; PHOSPHOLIPID HYDROPEROXIDE GLUTATHIONE PEROXIDASE; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

AEROBIC METABOLISM; ALZHEIMER DISEASE; AMPLICON; ANTIOXIDANT RESPONSIVE ELEMENT; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL NUCLEUS; CEREBROSPINAL FLUID; CYTOPLASM; CYTOSOL; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; EXON; GENE; GENE DOSAGE; GENE EXPRESSION REGULATION; GENE SEQUENCE; GENE TARGETING; GENOTYPE; GLUCOSE METABOLISM; GPX4 GENE; HIPPOCAMPUS; HUMAN; IN VIVO STUDY; INTRACELLULAR SPACE; KCNMA1 GENE; LIPID PEROXIDATION; MITOCHONDRION; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; RNA TRANSLATION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; UPREGULATION;

EID: 84940026200     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2015.00203     Document Type: Article

References (65)

1. Alessandri, J. M., Guesnet, P., Vancassel, S., Astorg, P., Denis, I., Langelier, B., et al. (2004). Polyunsaturated fatty acids in the central nervous system: evolution of concepts and nutritional implications throughout life. Reprod. Nutr. Dev. 44, 509-538. doi: 10.1051/rnd:2004063.
2. Arnér, E. S. J., and Holmgren, A. (2000). Physiological functions of thioredoxin and thioredoxin reductase. Eur. J. Biochem. 267, 6102-6109. doi: 10.1046/j.1432-1327.2000.01701.x.
3. Aso, E., Lomoio, S., López-Gonzalez, I., Joda, L., Carmona, M., Fernández-Yagüe, N., et al. (2012). Amyloid generation and dysfunctional immunoproteasome activation with disease progression in animal model of familial Alzheimer disease. Brain Pathol. 22, 636-653. doi: 10.1111/j.1750-3639.2011.00560.x.
4. Bazinet, R. P., and Layé, S. (2014). Polyunsaturated fatty acids and their metabolites in brain function and disease. Nat. Rev. Neurosci. 15, 771-785. doi: 10.1038/nrn3820.
5. Behl, C., Davis, J. B., Lesley, R., and Schubert, D. (1994). Hydrogen peroxide mediates amyloid beta protein toxicity. Cell 77, 817-827. doi: 10.1016/0092-8674(94)90131-7.
6. Bell, T. J., Miyashiro, K. Y., Sul, J. Y., Buckley, P. T., Lee, M. T., McCullough, R., et al. (2010). Intron retention facilitates splice variant diversity in calcium-activated big potassium channel populations. Proc. Natl. Acad. Sci. U.S.A. 107, 21152-21157. doi: 10.1073/pnas.1015264107.
7. Bell, T. J., Miyashiro, K. Y., Sul, J. Y., McCullough, R., Buckley, P. T., Jochems, J., et al. (2008). Cytoplasmic BK(Ca) channel intron-containing mRNAs contribute to the intrinsic excitability of hippocampal neurons. Proc. Natl. Acad. Sci. U.S.A. 105, 1901-1906. doi: 10.1073/pnas.0711796105.
8. 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. doi: 10.1074/jbc.270.20.11761.
9. Brigelius-Flohé, R., and Maiorino, M. (2013). Glutathione peroxidases. Biochim. Biophys. Acta. 1830, 3289-3303. doi: 10.1016/j.bbagen.2012.11.020.
10. Buckley, P. T., Khaladkar, M., Kim, J., and Eberwine, J. (2014). Cytoplasmic intron retention, function, splicing, and the sentinel RNA hypothesis. Wiley Interdiscip. Rev. RNA 5, 223-230. doi: 10.1002/wrna.1203.
11. Buckley, P. T., Lee, M. T., Sul, J. Y., Miyashiro, K. Y., Bell, T. J., Fisher, S. A., et al. (2011). Cytoplasmic intron sequence-retaining transcripts can be dendritically targeted via ID element retrotransposons. Neuron 69, 877-884. doi: 10.1016/j.neuron.2011.02.028.
12. Calderon, F., and Kim, H. Y. (2004). Docosahexaenoic acid promotes neurite growth in hippocampal neurons. J. Neurochem. 90, 979-988. doi: 10.1111/j.1471-4159.2004.02520.x.
13. Cao, D., Kevala, K., Kim, J., Moon, H. S., Jun, S. B., Lovinger, D., et al. (2009). Docosahexaenoic acid promotes hippocampal neuronal development and synaptic function. J. Neurochem. 111, 510-521. doi: 10.1111/j.1471-4159.2009.06335.x.
14. Casañas-Sánchez, V., Pérez, J. A., Fabelo, N., Herrera-Herrera, A. V., Fernández, C., Marín, R., et al. (2014). Addition of docosahexaenoic acid, but not arachidonic acid, activates glutathione and thioredoxin antioxidant systems in murine hippocampal HT22 cells: potential implications in neuroprotection. J. Neurochem. 131, 470-483. doi: 10.1111/jnc.12833.
15. 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. doi: 10.1016/j.chemphyslip.2008.09.004.
16. Chen, Y., Tian, Z., Liang, Z., Sun, S., Dai, C., Ling, Lee, M. H., et al. (2012). Brain gene expression of a sporadic (icv-STZ Mouse) and a familial mouse model (3xTg-AD mouse) of Alzheimer's disease. PLoS ONE 7:e51432. doi: 10.1371/journal.pone.0051432.
17. Crawford, M. A., Bloom, M., Broadhurst, C. L., Schmidt, W. F., Cunnane, S. C., Galli, C., et al. (1999). Evidence for the unique function of docosahexaenoic acid during the evolution of the modern hominid brain. Lipids 34, S39-S47. doi: 10.1007/BF02562227.
18. Crawford, M. A., Broadhurst, C. L., Guest, M., Nagar, A., Wang, Y., Ghebremeskel, K., et al. (2013). A quantum theory for the irreplaceable role of docosahexaenoic acid in neural cell signalling throughout evolution. Prostagl. Leukot. Essent. Fatty Acids 88, 5-13. doi: 10.1016/j.plefa.2012.08.005.
19. Díaz, M., Fabelo, N., and Marin, R. (2012). Genotype-induced changes in biophysical properties of frontal cortex lipid raft from APP/PS1 transgenic mice. Front. Physiol. 3:454. doi: 10.3389/fphys.2012.00454.
20. Díaz, M., Fabelo, N., Martín, V., Ferrer, I., Gómez, T., and Marín, R. (2015). Biophysical alterations in lipid rafts from human cerebral cortex associate with increased BACE1/Aβ PP interaction in early stages of Alzheimer's disease. J. Alzheimers Dis. 43, 1185-1198. doi: 10.3233/JAD-141146.
21. Díaz, M., and Marín, R. (2013). "Brain polyunsaturated lipids and neurodegenerative diseases," in Nutraceuticals and Functional Foods: Natural Remedy, eds S. K. Brar, S. Kaur, and G. S. Dhillon (Hauppage, NY: Nova Science Publishers), 387-412.
22. Dröge, W. (2002). Free radicals in the physiological control of cell function. Physiol. Rev. 82, 47-95. doi: 10.1152/physrev.00018.2001.
23. Expósito-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. doi: 10.1016/j.plaphy.2011.02.022.
24. Fabelo, N., Martín, V., Marín, R., Santpere, G., Aso, E., Ferrer, I., et al. (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. doi: 10.1097/NEN.0b013e31826be03c.
25. Farooqui, A. A., Horrocks, L. A., and Farooqui, T. (2000). Deacylation and reacylation of neural membrane glycerophospholipids. J. Mol. Neurosci. 14, 123-135. doi: 10.1385/JMN:14:3:123.
26. Fritz, K. S., and Petersen, D. R. (2013). An overview of the chemistry and biology of reactive aldehydes. Free Radicals Biol. Med. 59, 85-91. doi: 10.1016/j.freeradbiomed.2012.06.025.
27. Godeas, C., Tramer, F., Micali, F., Soranzo, M., Sandri, G., and Panfili, E. (1997). Distribution and possible novel role of phospholipid hydroperoxide glutathione peroxidase in rat epididymal spermatozoa. Biol. Reprod. 57, 1502-1508. doi: 10.1095/biolreprod57.6.1502.
28. Gwon, A. R., Park, J. S., Arumugam, T. V., Kwon, Y. K., Chan, S. L., Kim, S. H., et al. (2012). Oxidative lipid modification of nicastrin enhances amyloidogenic γ-secretase activity in Alzheimer's disease. Aging Cell 11, 559-568. doi: 10.1111/j.1474-9726.2012.00817.x.
29. 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. doi: 10.3233/JAD-2010-090934.
30. Imai, H., Hirao, F., Sakamoto, T., Sekine, K., Mizukura, Y., Saito, M., et al. (2003). Early embryonic lethality caused by targeted disruption of the mouse PHGPx gene. Biochem. Biophys. Res. Commun. 305, 278-286. doi: 10.1016/S0006-291X(03)00734-4.
31. 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. doi: 10.1016/S0891-5849(02)01197-8.
32. Innis, S. M. (2007). Dietary (n-3) fatty acids and brain development. J. Nutr. 137, 855-859. doi: 10.1016/j.brainres.2008.08.078.
33. Ishikado, A., Morino, K., Nishio, Y., Nakagawa, F., Mukose, A., Sono, Y., et al. (2013). 4-Hydroxy hexenal derived from docosahexaenoic acid protects endothelial cells via Nrf2 activation. PLoS ONE 8:e69415. doi: 10.1371/journal.pone.0069415.
34. Khaladkar, M., Buckley, P. T., Lee, M. T., Francis, C., Eghbal, M. M., Chuong, T., et al. (2013). Subcellular RNA sequencing reveals broad presence of cytoplasmic intron-sequence retaining transcripts in mouse and rat neurons. PLoS ONE 8:e76194. doi: 10.1371/journal.pone.0076194.
35. Kobayashi, M., and Yamamoto, M. (2005). Molecular mechanisms activating the Nrf2-Keap1 pathway of antioxidant gene regulation. Antioxid. Redox. Signal. 7, 385-394. doi: 10.1089/ars.2005.7.385.
36. Kusunoki, C., Yang, L., Yoshizaki, T., Nakagawa, F., Ishikado, A., Kondo, M., 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. doi: 10.1016/j.bbrc.2012.10.115.
37. Marcus, D. L., Thomas, C., Rodriguez, C., Simberkoff, K., Tsai, J. S., Strafaci, J. A., et al. (1998). Increased peroxidation and reduced antioxidant enzyme activity in Alzheimer's disease. Exp. Neurol. 150, 40-44. doi: 10.1006/exnr.1997.6750.
38. Markesbery, W. R., and Lovell, M. A. (1998). Four-hydroxynonenal, a product of lipid peroxidation, is increased in the brain in Alzheimer's disease. Neurobiol. Aging 19, 33-36. doi: 10.1016/S0197-4580(98)00009-8.
39. 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. Meth. 153, 230-238. doi: 10.1016/j.jneumeth.2005.10.019.
40. Moriguchi, T., Harauma, A., and Salem, N. (2013). Plasticity of mouse brain docosahexaenoic acid: modulation by diet and age. Lipids 48, 343-355. doi: 10.1007/s11745-013-3775-5.
41. Naudí, A., Jové, M., Ayala, V., Portero-Otín, M., Barja, G., and Pamplona, R. (2013). Membrane lipid unsaturation as physiological adaptation to animal longevity. Front. Physiol. 4:372. doi: 10.3389/fphys.2013.00372.
42. Nauser, T., Dockheer, S., Kissner, R., and Koppenol, W. H. (2006). Catalysis of electron transfer by selenocysteine. Biochemistry 16, 6038-6043. doi: 10.1021/bi0602260.
43. Niki, E., Yoshida, Y., Saito, Y., and Noguchi, N. (2005). Lipid peroxidation: mechanisms, inhibition, and biological effects. Biochem. Biophys. Res. Commun. 338, 668-676. doi: 10.1016/j.bbrc.2005.08.072.
44. Oster, T., and Pillot, T. (2010). Docosahexaenoic acid and synaptic protection in Alzheimer's disease mice. Biochim. Biophys. Acta 1801, 791-798. doi: 10.1016/j.bbalip.2010.02.011.
45. Pamplona, R., Dalfó, E., Ayala, V., Bellmunt, J., Prat, J., Ferrer, I., et al. (2005). Proteins in human brain cortex are modified by oxidation, glycoxidation, and lipoxidation: effects of Alzheimer disease and identification of lipoxidation targets. J. Biol. Chem. 280, 21522-21530. doi: 10.1074/jbc.M502255200.
46. Pfeifer, H., Conrad, M., Roethlein, D., Kyriakopoulos, A., Brielmeier, M., Bornkamm, G. W., et al. (2001). Identification of a specific sperm nuclei selenoenzyme necessary for protamine thiol cross-linking during sperm maturation. FASEB J. 15, 1236-1238. doi: 10.1096/fj.00-0655fje.
47. Plourde, M., and Cunnane, S. C. (2007). Extremely limited synthesis of long chain polyunsaturates in adults: implications for their dietary essentiality and use as supplements. Appl. Physiol. Nutr. Metab. 32, 619-634. doi: 10.1139/H07-034.
48. Porter, N. A., Caldwell, S. E., and Mills, K. A. (1995). Mechanisms of free radical oxidation of unsaturated lipids. Lipids 30, 277-290. doi: 10.1007/BF02536034.
49. Praticò, D., M. Y., Lee, V., Trojanowski, J. Q., Rokach, J., and Fitzgerald, G. A. (1998). Increased F2-isoprostanes in Alzheimer's disease: evidence for enhanced lipid peroxidation in vivo. FASEB J. 12, 1777-1783.
50. 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. doi: 10.1515/BC.2007.126.
51. Scheerer, P., Borchert, A., Krauss, N., Wessner, H., Gerth, C., Hohne, W., et al. (2007). Structural basis for catalytic activity and enzyme polymerization of phospholipid hydroperoxide glutathione peroxidase-4 (GPx4). Biochemistry 46, 9041-9049. doi: 10.1021/bi700840d.
52. Simopoulos, A. P. (2011). Evolutionary aspects of diet: the Omega-6/Omega-3 Ratio and the brain. Mol. Neurobiol. 44, 203-215. doi: 10.1007/s12035-010-8162-0.
53. Singh, M., Dang, T. N., Arseneault, M., and Ramassamy, C. (2010). Role of by-products of lipid oxidation in Alzheimer's disease brain: a focus on acrolein. J. Alzheimers. Dis. 21, 741-756. doi: 10.3233/JAD-2010-100405.
54. Solfrizzi, V., D'Introno, A., Colacicco, A. M., Capurso, C., Todarello, O., Pellicani, V., et al. (2006). Circulating biomarkers of cognitive decline and dementia. Clin. Chim. Acta 364, 91-112. doi: 10.1016/j.cca.2005.06.015.
55. Stillwell, W., and Wassal, S. R. (2003). Docosahexaenoic acid: membrane properties of a unique fatty acid. Chem. Phys. Lipids 126, 1-27. doi: 10.1016/S0009-3084(03)00101-4.
56. Uauy, R., Hoffman, D. R., Peirano, P., Birch, D. G., and Birch, E. E. (2001). Essential fatty acids in visual and brain development. Lipids 36, 885-895. doi: 10.1007/s11745-001-0798-1.
57. Ufer, C., and Wang, C. C. (2011). The roles of glutathione peroxidases during embryo development. Front. Mol. Neurosci. 4:12. doi: 10.3389/fnmol.2011.00012.
58. Unger, T., Korade, Z., Lazarov, O., Terrano, D., Schor, N. F., Sisodia, S. S., et al. (2005). Transcriptome differences between the frontal cortex and hippocampus of wild-type and humanized presenilin-1 transgenic mice. Am. J. Geriatr. Psychiatry 13, 1041-1051. doi: 10.1097/00019442-200512000-00003.
59. 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. doi: 10.1016/j.biocel.2006.07.001.
60. 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. doi: 10.1016/0005-2760(90)90118-H.
61. Wu, K. C., Cui, J. Y., and Klaassen, C. D. (2011). Beneficial role of Nrf2 in regulating NADPH generation and consumption. Toxicol. Sci. 123, 590-600. doi: 10.1093/toxsci/kfr183.
62. Yang, Y. C., Lii, C. K., Wei, Y. L., Li, C. C., Lu, C. Y., Liu, K. L., et al. (2013). Docosahexaenoic acid inhibition of inflammation is partially via cross-talk between Nrf2/heme oxygenase 1 and IKK/NF-κB pathways. J. Nutr. Biochem. 24, 204-212. doi: 10.1016/j.jnutbio.2012.05.003.
63. Yant, L. J., Ran, Q., Rao, L., Van Remmen, H., Shibatani, T., Belter, J. G., et al. (2003). The selenoprotein GPX4 is essential for mouse development and protects from radiation and oxidative damage insults. Free Radic. Biol. Med. 34, 496-502. doi: 10.1016/S0891-5849(02)01360-6.
64. 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. doi: 10.1016/j.pneurobio.2012.09.003.
65. Zhong, X., Liu, J. R., Kyle, J. W., Hanck, D. A., and Agnew, W. S. (2006). A profile of alternative RNA splicing and transcript variation of CACNA1H, a human T-channel gene candidate for idiopathic generalized epilepsies. Hum. Mol. Genet. 15, 1497-1512. doi: 10.1093/hmg/ddl068.