Adaptive regulation of the brain's antioxidant defences by neurons and astrocytes

Free Radical Biology and Medicine

Volumn 100, Issue , 2016, Pages 147-152

  Baxter, Paul S ^a   Hardingham, Giles E ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; GLUTATHIONE; PEROXIREDOXIN; REACTIVE OXYGEN METABOLITE; THIOREDOXIN; TRANSCRIPTION FACTOR NRF2;

ANTIOXIDANT ACTIVITY; ARTICLE; ASTROCYTE; BRAIN FUNCTION; CELL ACTIVITY; CELL FUNCTION; CELL VIABILITY; FOREBRAIN; GENE CONTROL; GENE EXPRESSION; HUMAN; NERVE CELL; NERVE REGENERATION; NEUROPROTECTION; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PRIORITY JOURNAL; ANIMAL; BRAIN; METABOLISM; MITOCHONDRION; OXIDATION REDUCTION REACTION; SIGNAL TRANSDUCTION;

ANIMALS; ANTIOXIDANTS; ASTROCYTES; BRAIN; HUMANS; MITOCHONDRIA; NEURONS; NF-E2-RELATED FACTOR 2; OXIDATION-REDUCTION; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84992608899     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2016.06.027     Document Type: Review

References (77)

1. [1] Dringen, R., Pawlowski, P.G., Hirrlinger, J., Peroxide detoxification by brain cells. J. Neurosci. Res. 79 (2005), 157–165.
2. [2] Hayes, J.D., McMahon, M., Chowdhry, S., Dinkova-Kostova, A.T., Cancer chemoprevention mechanisms mediated through the Keap1-Nrf2 pathway. Antioxid. Redox Signal. 13 (2010), 1713–1748.
3. [3] Suzuki, T., Motohashi, H., Yamamoto, M., Toward clinical application of the Keap1-Nrf2 pathway. Trends Pharmacol. Sci. 34 (2013), 340–346.
4. [4] Ma, Q., Role of nrf2 in oxidative stress and toxicity. Annu. Rev. Pharmacol. Toxicol. 53 (2013), 401–426.
5. [5] Kovac, S., Angelova, P.R., Holmstrom, K.M., Zhang, Y., Dinkova-Kostova, A.T., Abramov, A.Y., Nrf2 regulates ROS production by mitochondria and NADPH oxidase. Biochim. Biophys. Acta 1850 (2015), 794–801.
6. [6] Dinkova-Kostova, A.T., Abramov, A.Y., The emerging role of Nrf2 in mitochondrial function. Free Radic. Biol. Med. 88 (2015), 179–188.
7. [7] O'Connell, M.A., Hayes, J.D., The Keap1/Nrf2 pathway in health and disease: from the bench to the clinic. Biochem. Soc. Trans. 43 (2015), 687–689.
8. [8] Itoh, K., Chiba, T., Takahashi, S., Ishii, T., Igarashi, K., Katoh, Y., Oyake, T., Hayashi, N., Satoh, K., Hatayama, I., Yamamoto, M., Nabeshima, Y., An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem. Biophys. Res. Commun. 236 (1997), 313–322.
9. [9] Itoh, K., Wakabayashi, N., Katoh, Y., Ishii, T., Igarashi, K., Engel, J.D., Yamamoto, M., Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 13 (1999), 76–86.
10. [10] Shih, A.Y., Johnson, D.A., Wong, G., Kraft, A.D., Jiang, L., Erb, H., Johnson, J.A., Murphy, T.H., Coordinate regulation of glutathione biosynthesis and release by Nrf2-expressing glia potently protects neurons from oxidative stress. J. Neurosci. 23 (2003), 3394–3406.
11. [11] Kraft, A.D., Johnson, D.A., Johnson, J.A., Nuclear factor E2-related factor 2-dependent antioxidant response element activation by tert-butylhydroquinone and sulforaphane occurring preferentially in astrocytes conditions neurons against oxidative insult. J. Neurosci. 24 (2004), 1101–1112.
12. [12] Ahlgren-Beckendorf, J.A., Reising, A.M., Schander, M.A., Herdler, J.W., Johnson, J.A., Coordinate regulation of NAD(P)H: quinone oxidoreductase and glutathione-S-transferases in primary cultures of rat neurons and glia: role of the antioxidant/electrophile responsive element. Glia 25 (1999), 131–142.
13. [13] Murphy, T.H., Yu, J., Ng, R., Johnson, D.A., Shen, H., Honey, C.R., Johnson, J.A., Preferential expression of antioxidant response element mediated gene expression in astrocytes. J. Neurochem. 76 (2001), 1670–1678.
14. [14] Bell, K.F., Al-Mubarak, B., Martel, M.A., McKay, S., Wheelan, N., Hasel, P., Markus, N.M., Baxter, P., Deighton, R.F., Serio, A., Bilican, B., Chowdhry, S., Meakin, P.J., Ashford, M.L., Wyllie, D.J., Scannevin, R.H., Chandran, S., Hayes, J.D., Hardingham, G.E., Neuronal development is promoted by weakened intrinsic antioxidant defences due to epigenetic repression of Nrf2. Nat. Commun., 6, 2015, 7066.
15. [15] Jimenez-Blasco, D., Santofimia-Castano, P., Gonzalez, A., Almeida, A., Bolanos, J.P., Astrocyte NMDA receptors’ activity sustains neuronal survival through a Cdk5-Nrf2 pathway. Cell Death Differ. 22 (2015), 1877–1889.
16. [16] Kennedy, K.A., Sandiford, S.D., Skerjanc, I.S., Li, S.S., Reactive oxygen species and the neuronal fate. Cell Mol. Life Sci. 69 (2012), 215–221.
17. [17] Vieira, H.L., Alves, P.M., Vercelli, A., Modulation of neuronal stem cell differentiation by hypoxia and reactive oxygen species. Prog. Neurobiol. 93 (2011), 444–455.
18. [18] Soriano, F.X., Leveille, F., Papadia, S., Higgins, L.G., Varley, J., Baxter, P., Hayes, J.D., Hardingham, G.E., Induction of sulfiredoxin expression and reduction of peroxiredoxin hyperoxidation by the neuroprotective Nrf2 activator 3H-1,2-dithiole-3-thione. J. Neurochem. 107 (2008), 533–543.
19. [19] Funato, Y., Michiue, T., Asashima, M., Miki, H., The thioredoxin-related redox-regulating protein nucleoredoxin inhibits Wnt-beta-catenin signalling through dishevelled. Nat. Cell Biol. 8 (2006), 501–508.
20. [20] Rharass, T., Lemcke, H., Lantow, M., Kuznetsov, S.A., Weiss, D.G., Panakova, D., Ca2+-mediated mitochondrial reactive oxygen species metabolism augments Wnt/beta-catenin pathway activation to facilitate cell differentiation. J. Biol. Chem. 289 (2014), 27937–27951.
21. [21] Yu, X., Malenka, R.C., Beta-catenin is critical for dendritic morphogenesis. Nat. Neurosci. 6 (2003), 1169–1177.
22. [22] Rosso, S.B., Sussman, D., Wynshaw-Boris, A., Salinas, P.C., Wnt signaling through Dishevelled, Rac and JNK regulates dendritic development. Nat. Neurosci. 8 (2005), 34–42.
23. [23] Yang, Y., Higashimori, H., Morel, L., Developmental maturation of astrocytes and pathogenesis of neurodevelopmental disorders. J. Neurodev. Disord., 5, 2013, 22.
24. [24] Satoh, T., Okamoto, S.I., Cui, J., Watanabe, Y., Furuta, K., Suzuki, M., Tohyama, K., Lipton, S.A., Activation of the Keap1/Nrf2 pathway for neuroprotection by electrophilic [correction of electrophillic] phase II inducers. Proc. Natl. Acad. Sci. USA 103 (2006), 768–773.
25. [25] Gonzalez-Reyes, S., Guzman-Beltran, S., Medina-Campos, O.N., Pedraza-Chaverri, J., Curcumin pretreatment induces Nrf2 and an antioxidant response and prevents hemin-induced toxicity in primary cultures of cerebellar granule neurons of rats. Oxid. Med. Cell Longev., 2013, 2013, 801418.
26. [26] Boyanapalli, S.S., Tony Kong, A.N., “Curcumin, the king of spices”: epigenetic regulatory mechanisms in the prevention of cancer, neurological, and inflammatory diseases. Curr. Pharmacol. Rep. 1 (2015), 129–139.
27. [27] Herrero-Mendez, A., Almeida, A., Fernandez, E., Maestre, C., Moncada, S., Bolanos, J.P., The bioenergetic and antioxidant status of neurons is controlled by continuous degradation of a key glycolytic enzyme by APC/C-Cdh1. Nat. Cell Biol. 11 (2009), 747–752.
28. [28] Fernandez-Fernandez, S., Almeida, A., Bolanos, J.P., Antioxidant and bioenergetic coupling between neurons and astrocytes. Biochem. J. 443 (2012), 3–11.
29. [29] Belanger, M., Allaman, I., Magistretti, P.J., Brain energy metabolism: focus on astrocyte-neuron metabolic cooperation. Cell Metab. 14 (2011), 724–738.
30. [30] Poyton, R.O., Ball, K.A., Castello, P.R., Mitochondrial generation of free radicals and hypoxic signaling. Trends Endocrinol. Metab. 20 (2009), 332–340.
31. [31] Boveris, A., Oshino, N., Chance, B., The cellular production of hydrogen peroxide. Biochem. J. 128 (1972), 617–630.
32. [32] Murphy, M.P., How mitochondria produce reactive oxygen species. Biochem. J. 417 (2009), 1–13.
33. [33] St-Pierre, J., Buckingham, J.A., Roebuck, S.J., Brand, M.D., Topology of superoxide production from different sites in the mitochondrial electron transport chain. J. Biol. Chem. 277 (2002), 44784–44790.
34. [34] Sun, J., Trumpower, B.L., Superoxide anion generation by the cytochrome bc1 complex. Arch. Biochem. Biophys. 419 (2003), 198–206.
35. 2+)-dependent changes in the mitochondrial energetics in single dissociated mouse sensory neurons. Biochem. J. 283:Pt 1 (1992), 41–50.
36. [36] Hongpaisan, J., Winters, C.A., Andrews, S.B., Calcium-dependent mitochondrial superoxide modulates nuclear CREB phosphorylation in hippocampal neurons. Mol. Cell Neurosci. 24 (2003), 1103–1115.
37. [37] Hongpaisan, J., Winters, C.A., Andrews, S.B., Strong calcium entry activates mitochondrial superoxide generation, upregulating kinase signaling in hippocampal neurons. J. Neurosci. 24 (2004), 10878–10887.
38. [38] Brennan, A.M., Suh, S.W., Won, S.J., Narasimhan, P., Kauppinen, T.M., Lee, H., Edling, Y., Chan, P.H., Swanson, R.A., NADPH oxidase is the primary source of superoxide induced by NMDA receptor activation. Nat. Neurosci. 12 (2009), 857–863.
39. [39] Dryanovski, D.I., Guzman, J.N., Xie, Z., Galteri, D.J., Volpicelli-Daley, L.A., Lee, V.M., Miller, R.J., Schumacker, P.T., Surmeier, D.J., Calcium entry and alpha-synuclein inclusions elevate dendritic mitochondrial oxidant stress in dopaminergic neurons. J. Neurosci. 33 (2013), 10154–10164.
40. [40] Reyes, R.C., Brennan, A.M., Shen, Y., Baldwin, Y., Swanson, R.A., Activation of neuronal NMDA receptors induces superoxide-mediated oxidative stress in neighboring neurons and astrocytes. J. Neurosci. 32 (2012), 12973–12978.
41. [41] Vargas, M.R., Johnson, J.A., The Nrf2-ARE cytoprotective pathway in astrocytes. Expert Rev. Mol. Med., 11, 2009, e17.
42. [42] Hirrlinger, J., Schulz, J.B., Dringen, R., Glutathione release from cultured brain cells: multidrug resistance protein 1 mediates the release of GSH from rat astroglial cells. J. Neurosci. Res. 69 (2002), 318–326.
43. [43] Dringen, R., Pfeiffer, B., Hamprecht, B., Synthesis of the antioxidant glutathione in neurons: supply by astrocytes of CysGly as precursor for neuronal glutathione. J. Neurosci. 19 (1999), 562–569.
44. [44] Gupta, K., Chandran, S., Hardingham, G.E., Human stem cell-derived astrocytes and their application to studying Nrf2-mediated neuroprotective pathways and therapeutics in neurodegeneration. Br. J. Clin. Pharmacol., 2012.
45. [45] Patani, R., Hollins, A.J., Wishart, T.M., Puddifoot, C.A., Alvarez, S., de Lera, A.R., Wyllie, D.J., Compston, D.A., Pedersen, R.A., Gillingwater, T.H., Hardingham, G.E., Allen, N.D., Chandran, S., Retinoid-independent motor neurogenesis from human embryonic stem cells reveals a medial columnar ground state. Nat. Commun., 2, 2011, 214.
46. [46] Bell, K.F., Al-Mubarak, B., Fowler, J.H., Baxter, P.S., Gupta, K., Tsujita, T., Chowdhry, S., Patani, R., Chandran, S., Horsburgh, K., Hayes, J.D., Hardingham, G.E., Mild oxidative stress activates Nrf2 in astrocytes, which contributes to neuroprotective ischemic preconditioning. Proc. Natl. Acad. Sci. USA, 108, 2011 E1-2; author reply E3-4.
47. [47] Bell, K.F., Fowler, J.H., Al-Mubarak, B., Horsburgh, K., Hardingham, G.E., Activation of Nrf2-regulated glutathione pathway genes by ischemic preconditioning. Oxid. Med. Cell Longev., 2011, 2011, 689524.
48. [48] Wyllie, D.J., Livesey, M.R., Hardingham, G.E., Influence of GluN2 subunit identity on NMDA receptor function. Neuropharmacology 74 (2013), 4–17.
49. [49] Shih, A.Y., Li, P., Murphy, T.H., A small-molecule-inducible Nrf2-mediated antioxidant response provides effective prophylaxis against cerebral ischemia in vivo. J. Neurosci. 25 (2005), 10321–10335.
50. [50] Chen, P.C., Vargas, M.R., Pani, A.K., Smeyne, R.J., Johnson, D.A., Kan, Y.W., Johnson, J.A., Nrf2-mediated neuroprotection in the MPTP mouse model of Parkinson's disease: critical role for the astrocyte. Proc. Natl. Acad. Sci. USA 106 (2009), 2933–2938.
51. [51] Johnson, D.A., Johnson, J.A., Nrf2-a therapeutic target for the treatment of neurodegenerative diseases. Free Radic. Biol. Med., 2015.
52. [52] Vargas, M.R., Johnson, D.A., Sirkis, D.W., Messing, A., Johnson, J.A., Nrf2 activation in astrocytes protects against neurodegeneration in mouse models of familial amyotrophic lateral sclerosis. J. Neurosci. 28 (2008), 13574–13581.
53. [53] Calkins, M.J., Vargas, M.R., Johnson, D.A., Johnson, J.A., Astrocyte-specific overexpression of Nrf2 protects striatal neurons from mitochondrial complex II inhibition. Toxicol. Sci. 115 (2010), 557–568.
54. [54] Gan, L., Vargas, M.R., Johnson, D.A., Johnson, J.A., Astrocyte-specific overexpression of Nrf2 delays motor pathology and synuclein aggregation throughout the CNS in the alpha-synuclein mutant (A53T) mouse model. J. Neurosci. 32 (2012), 17775–17787.
55. [55] LaPash Daniels, C.M., Austin, E.V., Rockney, D.E., Jacka, E.M., Hagemann, T.L., Johnson, D.A., Johnson, J.A., Messing, A., Beneficial effects of Nrf2 overexpression in a mouse model of Alexander disease. J. Neurosci. 32 (2012), 10507–10515.
56. [56] Hardingham, G.E, Do, K.Q., Linking early-life NMDAR hypofunction and oxidative stress in schizophrenia pathogenesis. Nat. Rev. Neurosci., 2016.
57. [57] Kamat, C.D., Gadal, S., Mhatre, M., Williamson, K.S., Pye, Q.N., Hensley, K., Antioxidants in central nervous system diseases: preclinical promise and translational challenges. J. Alzheimers Dis. 15 (2008), 473–493.
58. [58] Bell, K.F., Hardingham, G.E., CNS Peroxiredoxins and Their Regulation in Health and Disease. Antioxid. Redox Signal., 2011.
59. [59] Hardingham, G.E., Lipton, S.A., Regulation of neuronal oxidative and nitrosative stress by endogenous protective pathways and disease processes. Antioxid. Redox Signal., 2011.
60. [60] Diaz-Hernandez, J.I., Almeida, A., Delgado-Esteban, M., Fernandez, E., Bolanos, J.P., Knockdown of glutamate-cysteine ligase by small hairpin RNA reveals that both catalytic and modulatory subunits are essential for the survival of primary neurons. J. Biol. Chem. 280 (2005), 38992–39001.
61. [61] Papadia, S., Soriano, F.X., Leveille, F., Martel, M.A., Dakin, K.A., Hansen, H.H., Kaindl, A., Sifringer, M., Fowler, J., Stefovska, V., McKenzie, G., Craigon, M., Corriveau, R., Ghazal, P., Horsburgh, K., Yankner, B.A., Wyllie, D.J., Ikonomidou, C., Hardingham, G.E., Synaptic NMDA receptor activity boosts intrinsic antioxidant defenses. Nat. Neurosci. 11 (2008), 476–487.
62. [62] Baxter, P.S., Bell, K.F., Hasel, P., Kaindl, A.M., Fricker, M., Thomson, D., Cregan, S.P., Gillingwater, T.H., Hardingham, G.E., Synaptic NMDA receptor activity is coupled to the transcriptional control of the glutathione system. Nat. Commun., 6, 2015, 6761.
63. [63] Lewerenz, J., Baxter, P., Kassubek, R., Albrecht, P., Van Liefferinge, J., Westhoff, M.A., Halatsch, M.E., Karpel-Massler, G., Meakin, P.J., Hayes, J.D., Aronica, E., Smolders, I., Ludolph, A.C., Methner, A., Conrad, M., Massie, A., Hardingham, G.E., Maher, P., Phosphoinositide 3-kinases upregulate system xc(-) via eukaryotic initiation factor 2alpha and activating transcription factor 4 - A pathway active in glioblastomas and epilepsy. Antioxid. Redox Signal. 20 (2014), 2907–2922.
64. [64] Hall, C.N., Klein-Flugge, M.C., Howarth, C., Attwell, D., Oxidative phosphorylation, not glycolysis, powers presynaptic and postsynaptic mechanisms underlying brain information processing. J. Neurosci. 32 (2012), 8940–8951.
65. [65] Harris, J.J., Jolivet, R., Attwell, D., Synaptic energy use and supply. Neuron 75 (2012), 762–777.
66. [66] Hasel, P., McKay, S., Qiu, J., Hardingham, G.E., Selective dendritic susceptibility to bioenergetic, excitotoxic and redox perturbations in cortical neurons. Biochim. Biophys. Acta 1853 (2015), 2066–2076.
67. [67] Deighton, R.F., Markus, N.M., Al-Mubarak, B., Bell, K.F., Papadia, S., Meakin, P.J., Chowdhry, S., Hayes, J.D., Hardingham, G.E., Nrf2 target genes can be controlled by neuronal activity in the absence of Nrf2 and astrocytes. Proc. Natl. Acad. Sci. USA 111 (2014), E1818–1820.
68. [68] Soriano, F.X., Baxter, P., Murray, L.M., Sporn, M.B., Gillingwater, T.H., Hardingham, G.E., Transcriptional regulation of the AP-1 and Nrf2 target gene sulfiredoxin. Mol. Cells 27 (2009), 279–282.
69. [69] Nguyen, T., Yang, C.S., Pickett, C.B., The pathways and molecular mechanisms regulating Nrf2 activation in response to chemical stress. Free Radic. Biol. Med. 37 (2004), 433–441.
70. [70] Turrigiano, G., Homeostatic synaptic plasticity: local and global mechanisms for stabilizing neuronal function. Cold Spring Harb. Perspect. Biol., 4, 2012, a005736.
71. [71] Hardingham, N.R., Hardingham, G.E., Fox, K.D., Jack, J.J., Presynaptic efficacy directs normalization of synaptic strength in layer 2/3 rat neocortex after paired activity. J. Neurophysiol. 97 (2007), 2965–2975.
72. [72] Yin, J., Yuan, Q., Structural homeostasis in the nervous system: a balancing act for wiring plasticity and stability. Front. Cell Neurosci., 8, 2014, 439.
73. [73] Habas, A., Hahn, J., Wang, X., Margeta, M., Neuronal activity regulates astrocytic Nrf2 signaling. Proc. Natl. Acad. Sci. USA 110 (2013), 18291–18296.
74. [74] West, A.E., Greenberg, M.E., Neuronal activity-regulated gene transcription in synapse development and cognitive function. Cold Spring Harb. Perspect. Biol., 3, 2011.
75. [75] Bell, K.F., Hardingham, G.E., The influence of synaptic activity on neuronal health. Curr. Opin. Neurobiol. 21 (2011), 299–305.
76. [76] Swanson, R.A., Liu, J., Miller, J.W., Rothstein, J.D., Farrell, K., Stein, B.A., Longuemare, M.C., Neuronal regulation of glutamate transporter subtype expression in astrocytes. J. Neurosci. 17 (1997), 932–940.
77. [77] Cahoy, J.D., Emery, B., Kaushal, A., Foo, L.C., Zamanian, J.L., Christopherson, K.S., Xing, Y., Lubischer, J.L., Krieg, P.A., Krupenko, S.A., Thompson, W.J., Barres, B.A., A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J. Neurosci. 28 (2008), 264–278.