SVCT2, a potential therapeutic target, protects against oxidative stress during ethanol-induced neurotoxicity via JNK/p38 MAPKs, NF-κB and miRNA125a-5p

Free Radical Biology and Medicine

Volumn 96, Issue , 2016, Pages 362-373

  Tian, Hua ^a,b   Ye, Xiaoxia ^a   Hou, Xiaojie ^a   Yang, Xiaowei ^a   Yang, Jingyu ^a   Wu, Chunfu ^a  

^a SHENYANG PHARMACEUTICAL UNIVERSITY   (China)

^b QIQIHAR MEDICAL UNIVERSITY   (China)

Author keywords

Ascorbic acid; Ethanol; MIR 125a 5p; Neurodegeneration; Oxidativestress; SVCT2

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; 4 HYDROXYNONENAL; ALCOHOL; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; GLUTATHIONE; GLUTATHIONE DISULFIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MICRORNA; MICRORNA 125A 5P; MITOGEN ACTIVATED PROTEIN KINASE P38; NEUROPROTECTIVE AGENT; PROTEIN; PYRROLIDINE DITHIOCARBAMATE; SMALL INTERFERING RNA; SODIUM ASCORBIC ACID COTRANSPORTER; SODIUM VITAMIN C TRANSPORTER 2; STRESS ACTIVATED PROTEIN KINASE; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG; 4-HYDROXY-2-NONENAL; ALDEHYDE; ANTIOXIDANT; ASCORBIC ACID; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; SLC23A2 PROTEIN, RAT;

ADULT; ALCOHOL INTOXICATION; ALCOHOL WITHDRAWAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BINGE DRINKING; BRAIN CELL; CEREBROSPINAL FLUID; CONTROLLED STUDY; CORRELATIONAL STUDY; DEGENERATIVE DISEASE; DENDRITE; DOWN REGULATION; DRUG TARGETING; EXPERIMENTAL BRAIN INJURY; FETUS; GENE OVEREXPRESSION; IN VITRO STUDY; MALE; NERVE CELL LESION; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PREFRONTAL CORTEX; PRIMARY CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RNAI THERAPEUTICS; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; CHEMICALLY INDUCED; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; NERVE CELL; NERVE DEGENERATION; PATHOLOGY;

ALDEHYDES; ANIMALS; ANTIOXIDANTS; ASCORBIC ACID; BINGE DRINKING; DENDRITES; ETHANOL; GENE EXPRESSION REGULATION; HUMANS; MAP KINASE KINASE 4; MICRORNAS; NERVE DEGENERATION; NEURONS; NF-KAPPA B; OXIDATIVE STRESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PREFRONTAL CORTEX; RATS; RNA, SMALL INTERFERING; SODIUM-COUPLED VITAMIN C TRANSPORTERS;

EID: 84968754925     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2016.03.039     Document Type: Article

References (78)

1. J.M. May Vitamin C transport and its role in the central nervous system Sub-cell. Biochem. 56 2012 85 103
2. M.E. Meredith, F.E. Harrison, and J.M. May Differential regulation of the ascorbic acid transporter SVCT2 during development and in response to ascorbic acid depletion Biochem. Biophys. Res. Commun. 414 2011 737 742
3. M. Burzle, Y. Suzuki, D. Ackermann, H. Miyazaki, N. Maeda, B. Clemencon, R. Burrier, and M.A. Hediger The sodium-dependent ascorbic acid transporter family SLC23 Mol. Asp. Med. 34 2013 436 454
4. S. Qiu, L. Li, E.J. Weeber, and J.M. May Ascorbate transport by primary cultured neurons and its role in neuronal function and protection against excitotoxicity J. Neurosci. Res. 85 2007 1046 1056
5. B. Gess, S. Sevimli, J.K. Strecker, P. Young, and W.R. Schabitz Sodium-dependent vitamin C transporter 2 (SVCT2) expression and activity in brain capillary endothelial cells after transient ischemia in mice PLoS One 6 2011 e17139
6. F.E. Harrison, S.M. Dawes, M.E. Meredith, V.R. Babaev, L. Li, and J.M. May Low vitamin C and increased oxidative stress and cell death in mice that lack the sodium-dependent vitamin C transporter SVCT2 Free Radic. Biol. Med. 49 2010 821 829
7. M.A. Collins, T.D. Corso, and E.J. Neafsey Neuronal degeneration in rat cerebrocortical and olfactory regions during subchronic "binge" intoxication with ethanol: possible explanation for olfactory deficits in alcoholics Alcohol. Clin. Exp. Res. 20 1996 284 292
8. J.A. Obernier, T.W. Bouldin, and F.T. Crews Binge ethanol exposure in adult rats causes necrotic cell death Alcohol. Clin. Exp. Res. 26 2002 547 557
9. S.A Shah, G.H. Yoon, and M.O. Kim Protection of the developing brain with anthocyanins against ethanol-induced oxidative stress and neurodegeneration Mol. Neurobiol. 2014
10. S.K. Das, K.R. Hiran, S. Mukherjee, and D.M. Vasudevan Oxidative stress is the primary event: effects of ethanol consumption in brain Indian J. Clin. Biochem. 22 2007 99 104
11. M.I. Naseer, H.Y. Lee, and M.O. Kim Neuroprotective effect of vitamin C against the ethanol and nicotine modulation of GABA(B) receptor and PKA-alpha expression in prenatal rat brain Synapse 64 2010 467 477
12. Y. Peng, K.H. Kwok, P.H. Yang, S.S. Ng, J. Liu, O.G. Wong, M.L. He, H.F. Kung, and M.C. Lin Ascorbic acid inhibits ROS production, NF-kappa B activation and prevents ethanol-induced growth retardation and microencephaly Neuropharmacology 48 2005 426 434
13. Y. Hou, C. Wu, J. Yang, X. He, and T. Guo Ethanol inducing ascorbic acid release in the prefrontal cortex and striatum of freely moving mice Yakugaku Zasshi: J. Pharm. Soc. Jpn. 126 2006 671 675
14. Pei Gang Yan, C.F. Wu, Mei Huang, and Wen Liu Role of nitric oxide in ethanol-induced ascorbic acid release in striatum of freely moving mice Toxicol. Lett. 145 2003 69 78
15. P.F. Gu, J.Y. Yang, C.F. Wu, W. Li, and Y. Shang Frontal decortication eliminates drug-induced ascorbic acid release in the striatum but not the nucleus accumbens of freely moving rats Brain Res. 1033 2005 194 201
16. +-dependent l-ascorbic acid transporters Nature 399 1999 70 75
17. W.J. Liang, D. Johnson, L.S. Ma, S.M. Jarvis, and L. Wei-Jun Regulation of the human vitamin C transporters expressed in COS-1 cells by protein kinase C [corrected] Am. J. Physiol. Cell Physiol. 283 2002 C1696 C1704
18. C.C. Portugal, T.G. da Encarnacao, R. Socodato, S.R. Moreira, D. Brudzewsky, A.F. Ambrosio, and R. Paes-de-Carvalho Nitric oxide modulates sodium vitamin C transporter 2 (SVCT-2) protein expression via protein kinase G (PKG) and nuclear factor-kappaB (NF-kappaB) J. Biol. Chem. 287 2012 3860 3872
19. J.X. Wilson, E.M. Jaworski, A. Kulaga, and S.J. Dixon Substrate regulation of ascorbate transport activity in astrocytes Neurochem. Res. 15 1990 1037 1043
20. T. Seno, N. Inoue, K. Matsui, J. Ejiri, K. Hirata, S. Kawashima, and M. Yokoyama Functional expression of sodium-dependent vitamin C transporter 2 in human endothelial cells J. Vasc. Res. 41 2004 345 351
21. B.A. Ballif, and J. Blenis Molecular mechanisms mediating mammalian mitogen-activated protein kinase (MAPK) kinase (MEK)-MAPK cell survival signals Cell Growth Differ.: Mol. Biol. J. Am. Assoc. Cancer Res. 12 2001 397 408
22. G. Rathnasamy, V. Sivakumar, P. Rangarajan, W.S. Foulds, E.A. Ling, and C. Kaur NF-kappaB-mediated nitric oxide production and activation of caspase-3 cause retinal ganglion cell death in the hypoxic neonatal retina Investig. Ophthalmol. Vis. Sci. 55 2014 5878 5889
23. R. Perez-Rodriguez, A.M. Olivan, C. Roncero, J. Moron-Oset, M.P. Gonzalez, and M.J. Oset-Gasque Glutamate triggers neurosecretion and apoptosis in bovine chromaffin cells through a mechanism involving NO production by neuronal NO synthase activation Free Radic. Biol. Med. 69 2014 390 402
24. B.M. Ku, Y.K. Lee, J.Y. Jeong, J. Mun, J.Y. Han, G.S. Roh, H.J. Kim, G.J. Cho, W.S. Choi, G.S. Yi, and S.S. Kang Ethanol-induced oxidative stress is mediated by p38 MAPK pathway in mouse hippocampal cells Neurosci. Lett. 419 2007 64 67
25. Y. Zhang, G. Wei, Z. Di, and Q. Zhao miR-339-5p inhibits alcohol-induced brain inflammation through regulating NF-kappaB pathway Biochem. Biophys. Res. Commun. 452 2014 450 456
26. X. Chen, J. Liu, W.K. Feng, X. Wu, and S.Y. Chen MiR-125b protects against ethanol-induced apoptosis in neural crest cells and mouse embryos by targeting Bak 1 and PUMA Exp. Neurol. 271 2015 104 111
27. R.C. Miranda MicroRNAs and Fetal Brain Development: Implications for Ethanol Teratology during the Second Trimester Period of Neurogenesis Front. Genet. 3 2012 77
28. A.S. Flynt, and E.C. Lai Biological principles of microRNA-mediated regulation: shared themes amid diversity Nat. Rev. Genet. 9 2008 831 842
29. R.J. Wang, Y.H. Zheng, P. Wang, and J.Z. Zhang Serum miR-125a-5p, miR-145 and miR-146a as diagnostic biomarkers in non-small cell lung cancer Int. J. Clin. Exp. Pathol. 8 2015 765 771
30. S. Banerjee, H. Cui, N. Xie, Z. Tan, S. Yang, M. Icyuz, V.J. Thannickal, E. Abraham, and G. Liu miR-125a-5p regulates differential activation of macrophages and inflammation J. Biol. Chem. 288 2013 35428 35436
31. M.L. Ufkin, S. Peterson, X. Yang, H. Driscoll, C. Duarte, and P. Sathyanarayana miR-125a regulates cell cycle, proliferation, and apoptosis by targeting the ErbB pathway in acute myeloid leukemia Leuk. Res. 38 2014 402 410
32. F. Lamarche, C. Carcenac, B. Gonthier, C. Cottet-Rousselle, C. Chauvin, L. Barret, X. Leverve, M. Savasta, and E. Fontaine Mitochondrial permeability transition pore inhibitors prevent ethanol-induced neuronal death in mice Chem. Res. Toxicol. 26 2013 78 88
33. C. Xie, W.R. Markesbery, and M.A. Lovell Survival of hippocampal and cortical neurons in a mixture of MEM+ and B27-supplemented neurobasal medium Free Radic. Biol. Med. 28 2000 665 672
34. E. Majchrowicz Induction of physical dependence upon ethanol and the associated behavioral changes in rats Psychopharmacologia 43 1975 245 254
35. K. Nixon, and F.T. Crews Temporally specific burst in cell proliferation increases hippocampal neurogenesis in protracted abstinence from alcohol J. Neurosci: Off. J. Soc. Neurosci. 24 2004 9714 9722
36. W.A. Hunt Are binge drinkers more at risk of developing brain damage? Alcohol 10 1993 559 561
37. D.M. Hayes, M.A. Deeny, C.A. Shaner, and K. Nixon Determining the threshold for alcohol-induced brain damage: new evidence with gliosis markers Alcohol. Clin. Exp. Res. 37 2013 425 434
38. D.J. Knapp, and F.T. Crews Induction of cyclooxygenase-2 in brain during acute and chronic ethanol treatment and ethanol withdrawal Alcoholism, Clin. Exp. Res. 23 1999 633 643
39. L.C. Schmued, K.J. Hopkins, and B. Fluoro-Jade A high affinity fluorescent marker for the localization of neuronal degeneration Brain Res. 874 2000 123 130
40. Y.N. Zhao, F. Wang, Y.X. Fan, G.F. Ping, J.Y. Yang, and C.F. Wu Activated microglia are implicated in cognitive deficits, neuronal death, and successful recovery following intermittent ethanol exposure Behav. Brain Res. 236 2013 270 282
41. R. Nirogi, V. Kandikere, K. Mudigonda, G. Bhyrapuneni, N. Muddana, R. Saralaya, and V. Benade A simple and rapid method to collect the cerebrospinal fluid of rats and its application for the assessment of drug penetration into the central nervous system J. Neurosci. Methods 178 2009 116 119
42. M.E. Meredith, and J.M. May Regulation of embryonic neurotransmitter and tyrosine hydroxylase protein levels by ascorbic acid Brain Res. 1539 2013 7 14
43. L.A. Pachla, and P.T. Kissinger Analysis of ascorbic acid by liquid chromatography with amperometric detection Methods Enzymol. 62 1979 15 24
44. J.M. May, and Z.C. Qu Nitric oxide mediates tightening of the endothelial barrier by ascorbic acid Biochem. Biophys. Res. Commun. 404 2011 701 705
45. M.I. Naseer, N. Ullah, I. Ullah, P.O. Koh, H.Y. Lee, M.S. Park, and M.O. Kim Vitamin C protects against ethanol and PTZ-induced apoptotic neurodegeneration in prenatal rat hippocampal neurons Synapse 65 2011 562 571
46. R. Roivainen, B. Hundle, and R.O. Messing Ethanol enhances growth factor activation of mitogen-activated protein kinases by a protein kinase C-dependent mechanism Proc. Natl. Acad. Sci. USA 92 1995 1891 1895
47. C.C. Portugal, V.S. Miya, C. Calaza Kda, R.A. Santos, and R. Paes-de-Carvalho Glutamate receptors modulate sodium-dependent and calcium-independent vitamin C bidirectional transport in cultured avian retinal cells J. Neurochem. 108 2009 507 520
48. S.A. Prins, M.M. Przybycien-Szymanska, Y.S. Rao, and T.R. Pak Long-term effects of peripubertal binge EtOH exposure on hippocampal microRNA expression in the rat PLoS One 9 2014 e83166
49. J.Y. Yang, X. Xue, H. Tian, X.X. Wang, Y.X. Dong, F. Wang, Y.N. Zhao, X.C. Yao, W. Cui, and C.F. Wu Role of microglia in ethanol-induced neurodegenerative disease: pathological and behavioral dysfunction at different developmental stages Pharmacol. Ther. 2014
50. N. Tajuddin, K.H. Moon, S.A. Marshall, K. Nixon, E.J. Neafsey, H.Y. Kim, and M.A. Collins Neuroinflammation and neurodegeneration in adult rat brain from binge ethanol exposure: abrogation by docosahexaenoic acid PLoS One 9 2014 e101223
51. M.A. Collins, and E.J. Neafsey Neuroinflammatory pathways in binge alcohol-induced neuronal degeneration: oxidative stress cascade involving aquaporin, brain edema, and phospholipase A2 activation Neurotox. Res. 21 2012 70 78
52. C.F. Wu, J. Liu, S. Consolo, and W. Liu 5-HT1A receptors mediate inhibition of ethanol-induced ascorbic acid release in rat striatum studied by microdialysis Neurosci. Lett. 250 1998 95 98
53. Yue Hou, C. Wu, Jingyu Yang, Xiang He, and Tao Guo Ethanol similarly inducres ascorbic acid release in the prefrontal cortex and striatum of freely moving mice Pharm. Soc. Jpn. 126 2006 671 675
54. M. Huang, W. Liu, Q. Li, and C.F. Wu Endogenous released ascorbic acid suppresses ethanol-induced hydroxyl radical production in rat striatum Brain Res. 944 2002 90 96
55. S. Sotiriou, S. Gispert, J. Cheng, Y. Wang, A. Chen, S. Hoogstraten-Miller, G.F. Miller, O. Kwon, M. Levine, S.H. Guttentag, and R.L. Nussbaum Ascorbic-acid transporter Slc23a1 is essential for vitamin C transport into the brain and for perinatal survival Nat. Med. 8 2002 514 517
56. J.M. May, L. Li, and Z.C. Qu Oxidized LDL up-regulates the ascorbic acid transporter SVCT2 in endothelial cells Mol. Cell. Biochem. 343 2010 217 222
57. H. Rouach, P. Houze, M. Park, and R. Nordmann Changes in cerebellar iron metabolism and their prevention by allopurinol in oxidative stress related to acute ethanol administration in rats C. R. des Seances Soc. Biol. Fil. 183 1989 40 47
58. F. Nualart, L. Mack, A. Garcia, P. Cisternas, E.R. Bongarzone, M. Heitzer, N. Jara, F. Martinez, L. Ferrada, F. Espinoza, V. Baeza, and K. Salazar Vitamin C transporters, recycling and the bystander effect in the nervous system: SVCT2 versus gluts J. Stem Cell Res. Ther. 4 2014 209
59. V. Ulloa, M. Garcia-Robles, F. Martinez, K. Salazar, K. Reinicke, F. Perez, D.F. Godoy, A.S. Godoy, and F. Nualart Human choroid plexus papilloma cells efficiently transport glucose and vitamin C J. Neurochem. 127 2013 403 414
60. S. Angelow, M. Haselbach, and H.J. Galla Functional characterisation of the active ascorbic acid transport into cerebrospinal fluid using primary cultured choroid plexus cells Brain Res. 988 2003 105 113
61. 2+ mobilization and increases GFAP content in rat hippocampal astrocytes Brain Res. 1178 2007 28 37
62. J. Barabas, E. Nagy, and I. Degrell Ascorbic acid in cerebrospinal fluid - a possible protection against free radicals in the brain Arch. Gerontol. Geriatr. 21 1995 43 48
63. S.B. Aylett, V. Neergheen, I.P. Hargreaves, S. Eaton, J.M. Land, S. Rahman, and S.J. Heales Levels of 5-methyltetrahydrofolate and ascorbic acid in cerebrospinal fluid are correlated: implications for the accelerated degradation of folate by reactive oxygen species Neurochem. Int. 63 2013 750 755
64. A. Melo, L. Monteiro, R.M. Lima, D.M. Oliveira, M.D. Cerqueira, and R.S. El-Bacha Oxidative stress in neurodegenerative diseases: mechanisms and therapeutic perspectives Oxid. Med. Cell. Longev. 2011 2011 467180
65. U. Mutlu-Turkoglu, S. Dogru-Abbasoglu, G. Aykac-Toker, H. Mirsal, M. Beyazyurek, and M. Uysal Increased lipid and protein oxidation and DNA damage in patients with chronic alcoholism J. Lab. Clin. Med. 136 2000 287 291
66. J. Haorah, S.H. Ramirez, N. Floreani, S. Gorantla, B. Morsey, and Y. Persidsky Mechanism of alcohol-induced oxidative stress and neuronal injury Free Radic. Biol. Med. 45 2008 1542 1550
67. V. Ramachandran, L.T. Watts, S.K. Maffi, J. Chen, S. Schenker, and G. Henderson Ethanol-induced oxidative stress precedes mitochondrially mediated apoptotic death of cultured fetal cortical neurons J. Neurosci. Res. 74 2003 577 588
68. L.T. Watts, M.L. Rathinam, S. Schenker, and G.I. Henderson Astrocytes protect neurons from ethanol-induced oxidative stress and apoptotic death J. Neurosci. Res. 80 2005 655 666
69. D.W. Lee, Y.K. Nam, T.K. Kim, J.H. Kim, S.Y. Kim, J.W. Min, J.H. Lee, H.Y. Kim, D.J. Kim, and B.Y. Choe Dose-dependent influence of short-term intermittent ethanol intoxication on cerebral neurochemical changes in rats detected by ex vivo proton nuclear magnetic resonance spectroscopy Neuroscience 262 2014 107 117
70. U.V. Berger, X.-C.M. Lu, W. Liu, Z. Tang, B.S. Slusher, and M.A. Hediger Effect of middle cerebral artery occlusion on mRNA expression for the sodium-coupled vitamin C transporter SVCT2 in rat brain J. Neurochem. 86 2003 896 906
71. M. Castro, T. Caprile, A. Astuya, C. Millan, K. Reinicke, J.C. Vera, O. Vasquez, L.G. Aguayo, and F. Nualart High-affinity sodium-vitamin C co-transporters (SVCT) expression in embryonic mouse neurons J. Neurochem. 78 2001 815 823
72. H. Do, H.J. Park, E.H. Sohn, B.O. Kim, S.H. Um, J.H. Kwak, E.Y. Moon, D.K. Rhee, and S. Pyo Ethanol induces cell cycle arrest and triggers apoptosis via Sp1-dependent p75NTR expression in human neuroblastoma cells Cell Biol. Toxicol. 29 2013 365 380
73. H.S. Kalluri, and M.K. Ticku Regulation of ERK phosphorylation by ethanol in fetal cortical neurons Neurochem. Res. 28 2003 765 769
74. H.S. Kalluri, and M.K. Ticku Ethanol-mediated inhibition of mitogen-activated protein kinase phosphorylation in mouse brain Eur. J. Pharmacol. 439 2002 53 58
75. R.C. Miranda, A.Z. Pietrzykowski, Y. Tang, P. Sathyan, D. Mayfield, A. Keshavarzian, W. Sampson, and D. Hereld MicroRNAs: master regulators of ethanol abuse and toxicity? Alcohol. Clin. Exp. Res. 34 2010 575 587
76. R.C. Miranda MicroRNAs and ethanol toxicity Int. Rev. Neurobiol. 115 2014 245 284
77. R.S. Muddashetty, V.C. Nalavadi, C. Gross, X. Yao, L. Xing, O. Laur, S.T. Warren, and G.J. Bassell Reversible inhibition of PSD-95 mRNA translation by miR-125a, FMRP phosphorylation, and mGluR signaling Mol. Cell 42 2011 673 688
78. S.W. Kim, K. Ramasamy, H. Bouamar, A.P. Lin, D. Jiang, and R.C. Aguiar MicroRNAs miR-125a and miR-125b constitutively activate the NF-kappaB pathway by targeting the tumor necrosis factor alpha-induced protein 3 (TNFAIP3, A20) Proc. Natl. Acad. Sci. USA 109 2012 7865 7870