Selective dendritic susceptibility to bioenergetic, excitotoxic and redox perturbations in cortical neurons

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1853, Issue 9, 2014, Pages 2066-2076

  Hasel, Philip ^a   Mckay, Sean ^a   Qiu, Jing ^a   Hardingham, Giles E ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Antioxidant defences; Bioenergetics; Calcium signalling; Excitotoxicity; Mitochondria; Oxidative stress

Indexed keywords

ADENOSINE TRIPHOSPHATE; GLUTAREDOXIN; GLUTAREDOXIN 1; GLUTATHIONE; GREEN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN 2; HYDROGEN PEROXIDE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PYRUVATE DEHYDROGENASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; UNCLASSIFIED DRUG; CALCIUM; NICOTINAMIDE ADENINE DINUCLEOTIDE;

ANIMAL CELL; ARTICLE; BIOENERGY; BRAIN CELL; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL MEMBRANE DEPOLARIZATION; CONTROLLED STUDY; DEGENERATIVE DISEASE; DENDRITE; DEPHOSPHORYLATION; EXCITOTOXICITY; FIRING RATE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MOUSE; NERVE POTENTIAL; NERVOUS SYSTEM PARAMETERS; NEUROTOXICITY; NONHUMAN; OXIDATION; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PERIKARYON; PRIORITY JOURNAL; SOMATIC RESPONSE; SYNAPSE; SYNAPTIC TRANSMISSION; ANIMAL; BRAIN CORTEX; CELL CULTURE; CYTOLOGY; METABOLISM; PHYSIOLOGY;

ADENOSINE TRIPHOSPHATE; ANIMALS; CALCIUM; CELLS, CULTURED; CEREBRAL CORTEX; DENDRITES; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; NAD; OXIDATIVE STRESS; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 84947735900     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2014.12.021     Document Type: Article

References (91)

1. Abramov A.Y., Duchen M.R. Mechanisms underlying the loss of mitochondrial membrane potential in glutamate excitotoxicity. Biochim. Biophys. Acta 2008, 1777:953-964.
2. Al-Mubarak B., Soriano F.X., Hardingham G.E. Synaptic NMDAR activity suppresses FOXO1 expression via a cis-acting FOXO binding site: FOXO1 is a FOXO target gene. Channels (Austin) 2009, 3:233-238.
3. Andrabi S.A., Umanah G.K., Chang C., Stevens D.A., Karuppagounder S.S., Gagne J.P., Poirier G.G., Dawson V.L., Dawson T.M. Poly(ADP-ribose) polymerase-dependent energy depletion occurs through inhibition of glycolysis. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:10209-10214.
4. Ankarcrona M., Dypbukt J.M., Bonfoco E., Zhivotovsky B., Orrenius S., Lipton S.A., Nicotera P. Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 1995, 15:961-973.
5. Arundine M., Tymianski M. Molecular mechanisms of glutamate-dependent neurodegeneration in ischemia and traumatic brain injury. Cell. Mol. Life Sci. 2004, 61:657-668.
6. Bading H., Ginty D.D., Greenberg M.E. Regulation of gene expression in hippocampal neurons by distinct calcium signaling pathways. Science 1993, 260:181-186.
7. Baughman J.M., Perocchi F., Girgis H.S., Plovanich M., Belcher-Timme C.A., Sancak Y., Bao X.R., Strittmatter L., Goldberger O., Bogorad R.L., Koteliansky V., Mootha V.K. Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter. Nature 2011, 476:341-345.
8. Bell K.F., Hardingham G.E. CNS peroxiredoxins and their regulation in health and disease. Antioxid. Redox Signal. 2011, 14:1467-1477.
9. Bell K.F., Hardingham G.E. The influence of synaptic activity on neuronal health. Curr. Opin. Neurobiol. 2011, 21:299-305.
10. 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.
11. 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. U. S. A. 2011, 108:E1-E2. (author reply E3-4).
12. Bonfoco E., Krainc D., Ankarcrona M., Nicotera P., Lipton S.A. Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-d-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:7162-7166.
13. 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. 2009, 12:857-863.
14. Camacho A., Massieu L. Role of glutamate transporters in the clearance and release of glutamate during ischemia and its relation to neuronal death. Arch. Med. Res. 2006, 37:11-18.
15. Chen M., Wang Y., Hou T., Zhang H., Qu A., Wang X. Differential mitochondrial calcium responses in different cell types detected with a mitochondrial calcium fluorescent indicator, mito-GCaMP2. Acta Biochim. Biophys. Sin. (Shanghai) 2011, 43:822-830.
16. Choi D.W. Ionic dependence of glutamate neurotoxicity. J. Neurosci. 1987, 7:369-379.
17. Choi D.W. Excitotoxic cell death. J. Neurobiol. 1992, 23:1261-1276.
18. Choi D.W., Maulucci-Gedde M., Kriegstein A.R. Glutamate neurotoxicity in cortical cell culture. J. Neurosci. 1987, 7:357-368.
19. Choi D.W., Koh J.Y., Peters S. Pharmacology of glutamate neurotoxicity in cortical cell culture: attenuation by NMDA antagonists. J. Neurosci. 1988, 8:185-196.
20. Csordas G., Varnai P., Golenar T., Sheu S.S., Hajnoczky G. Calcium transport across the inner mitochondrial membrane: molecular mechanisms and pharmacology. Mol. Cell. Endocrinol. 2012, 353:109-113.
21. Dawson T.M., Zhang J., Dawson V.L., Snyder S.H. Nitric oxide: cellular regulation and neuronal injury. Prog. Brain Res. 1994, 103:365-369.
22. De Stefani D., Raffaello A., Teardo E., Szabo I., Rizzuto R. A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature 2011, 476:336-340.
23. Dickstein D.L., Kabaso D., Rocher A.B., Luebke J.I., Wearne S.L., Hof P.R. Changes in the structural complexity of the aged brain. Aging Cell 2007, 6:275-284.
24. Do K.Q., Trabesinger A.H., Kirsten-Kruger M., Lauer C.J., Dydak U., Hell D., Holsboer F., Boesiger P., Cuenod M. Schizophrenia: glutathione deficit in cerebrospinal fluid and prefrontal cortex in vivo. Eur. J. Neurosci. 2000, 12:3721-3728.
25. 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. 2013, 33:10154-10164.
26. Duan Y., Gross R.A., Sheu S.S. Ca2+-dependent generation of mitochondrial reactive oxygen species serves as a signal for poly(ADP-ribose) polymerase-1 activation during glutamate excitotoxicity. J. Physiol. 2007, 585:741-758.
27. Duchen M.R. Ca(2+)-dependent changes in the mitochondrial energetics in single dissociated mouse sensory neurons. Biochem. J. 1992, 283(Pt 1):41-50.
28. Duchen M.R. Mitochondria, calcium-dependent neuronal death and neurodegenerative disease. Pflugers Arch. 2012, 464:111-121.
29. Fan M.M., Raymond L.A. N-methyl-d-aspartate (NMDA) receptor function and excitotoxicity in Huntington's disease. Prog. Neurobiol. 2007, 81:272-293.
30. Frustaci A., Neri M., Cesario A., Adams J.B., Domenici E., Dalla Bernardina B., Bonassi S. Oxidative stress-related biomarkers in autism: systematic review and meta-analyses. Free Radic. Biol. Med. 2012, 52:2128-2141.
31. Gawryluk J.W., Wang J.F., Andreazza A.C., Shao L., Young L.T. Decreased levels of glutathione, the major brain antioxidant, in post-mortem prefrontal cortex from patients with psychiatric disorders. Int. J. Neuropsychopharmacol. 2011, 14:123-130.
32. Gellerich F.N., Gizatullina Z., Gainutdinov T., Muth K., Seppet E., Orynbayeva Z., Vielhaber S. The control of brain mitochondrial energization by cytosolic calcium: the mitochondrial gas pedal. IUBMB Life 2013, 65:180-190.
33. Ghanizadeh A., Akhondzadeh S., Hormozi M., Makarem A., Abotorabi-Zarchi M., Firoozabadi A. Glutathione-related factors and oxidative stress in autism, a review. Curr. Med. Chem. 2012, 19:4000-4005.
34. Glancy B., Balaban R.S. Role of mitochondrial Ca2+ in the regulation of cellular energetics. Biochemistry 2012, 51:2959-2973.
35. Gomez-Isla T., Spires T., De Calignon A., Hyman B.T. Neuropathology of Alzheimer's disease. Handb. Clin. Neurol. 2008, 89:233-243.
36. Greenwood S.M., Connolly C.N. Dendritic and mitochondrial changes during glutamate excitotoxicity. Neuropharmacology 2007, 53:891-898.
37. Greenwood S.M., Mizielinska S.M., Frenguelli B.G., Harvey J., Connolly C.N. Mitochondrial dysfunction and dendritic beading during neuronal toxicity. J. Biol. Chem. 2007, 282:26235-26244.
38. Grima G., Benz B., Parpura V., Cuenod M., Do K.Q. Dopamine-induced oxidative stress in neurons with glutathione deficit: implication for schizophrenia. Schizophr. Res. 2003, 62:213-224.
39. 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, 75:907-918.
40. Gupta K., Hardingham G.E., Chandran S. NMDA receptor-dependent glutamate excitotoxicity in human embryonic stem cell-derived neurons. Neurosci. Lett. 2013, 543:95-100.
41. Gupta K., Patani R., Baxter P., Serio A., Story D., Tsujita T., Hayes J.D., Pedersen R.A., Hardingham G.E., Chandran S. Human embryonic stem cell derived astrocytes mediate non-cell-autonomous neuroprotection through endogenous and drug-induced mechanisms. Cell Death Differ. 2012, 19:779-787.
42. Gutscher M., Pauleau A.L., Marty L., Brach T., Wabnitz G.H., Samstag Y., Meyer A.J., Dick T.P. Real-time imaging of the intracellular glutathione redox potential. Nat. Methods 2008, 5:553-559.
43. Gysin R., Kraftsik R., Sandell J., Bovet P., Chappuis C., Conus P., Deppen P., Preisig M., Ruiz V., Steullet P., Tosic M., Werge T., Cuenod M., Do K.Q. Impaired glutathione synthesis in schizophrenia: convergent genetic and functional evidence. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:16621-16626.
44. 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. 2012, 32:8940-8951.
45. Halliwell B. Oxidative stress and neurodegeneration: where are we now?. J. Neurochem. 2006, 97:1634-1658.
46. Hardingham G.E., Bading H. Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders. Nat. Rev. Neurosci. 2010, 11:682-696.
47. Hardingham G.E., Lipton S.A. Regulation of neuronal oxidative and nitrosative stress by endogenous protective pathways and disease processes. Antioxid. Redox Signal. 2011, 14:1421-1424.
48. Hardingham G.E., Arnold F.J., Bading H. Nuclear calcium signaling controls CREB-mediated gene expression triggered by synaptic activity. Nat. Neurosci. 2001, 4:261-267.
49. Hardingham G.E., Fukunaga Y., Bading H. Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat. Neurosci. 2002, 5:405-414.
50. Harris J.J., Jolivet R., Attwell D. Synaptic energy use and supply. Neuron 2012, 75:762-777.
51. Hung Y.P., Albeck J.G., Tantama M., Yellen G. Imaging cytosolic NADH-NAD(+) redox state with a genetically encoded fluorescent biosensor. Cell Metab. 2011, 14:545-554.
52. Imamura H., Nhat K.P., Togawa H., Saito K., Iino R., Kato-Yamada Y., Nagai T., Noji H. Visualization of ATP levels inside single living cells with fluorescence resonance energy transfer-based genetically encoded indicators. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:15651-15656.
53. Ittner L.M., Ke Y.D., Delerue F., Bi M., Gladbach A., van Eersel J., Wolfing H., Chieng B.C., Christie M.J., Napier I.A., Eckert A., Staufenbiel M., Hardeman E., Gotz J. Dendritic function of Tau mediates amyloid-beta toxicity in Alzheimer's disease mouse models. Cell 2010, 142:387-397.
54. Johnson W.M., Wilson-Delfosse A.L., Mieyal J.J. Dysregulation of glutathione homeostasis in neurodegenerative diseases. Nutrients 2012, 4:1399-1440.
55. Johri A., Beal M.F. Mitochondrial dysfunction in neurodegenerative diseases. J. Pharmacol. Exp. Ther. 2012, 342:619-630.
56. Kalia L.V., Kalia S.K., Salter M.W. NMDA receptors in clinical neurology: excitatory times ahead. Lancet Neurol. 2008, 7:742-755.
57. Keelan J., Vergun O., Duchen M.R. Excitotoxic mitochondrial depolarisation requires both calcium and nitric oxide in rat hippocampal neurons. J. Physiol. 1999, 520(Pt 3):797-813.
58. Khatri N., Man H.Y. Synaptic activity and bioenergy homeostasis: implications in brain trauma and neurodegenerative diseases. Front. Neurol. 2013, 4:199.
59. Kulak A., Steullet P., Cabungcal J.H., Werge T., Ingason A., Cuenod M., Do K.Q. Redox dysregulation in the pathophysiology of schizophrenia and bipolar disorder: insights from animal models. Antioxid. Redox Signal. 2013, 18:1428-1443.
60. Lau A., Tymianski M. Glutamate receptors, neurotoxicity and neurodegeneration. Pflugers Arch. 2010, 460:525-542.
61. Lipton S.A. Paradigm shift in neuroprotection by NMDA receptor blockade: memantine and beyond. Nat. Rev. Drug Discov. 2006, 5:160-170.
62. Lipton S.A., Rosenberg P.A. Excitatory amino acids as a final common pathway for neurologic disorders. N. Engl. J. Med. 1994, 330:613-621.
63. Llorente-Folch I., Rueda C.B., Amigo I., del Arco A., Saheki T., Pardo B., Satrustegui J. Calcium-regulation of mitochondrial respiration maintains ATP homeostasis and requires ARALAR/AGC1-malate aspartate shuttle in intact cortical neurons. J. Neurosci. 2013, 33:13957-13971. (13971a).
64. Lucas D.R., Newhouse J.P. The toxic effect of sodium l-glutamate on the inner layers of the retina. AMA Arch. Ophthalmol. 1957, 58:193-201.
65. Luebke J.I., Weaver C.M., Rocher A.B., Rodriguez A., Crimins J.L., Dickstein D.L., Wearne S.L., Hof P.R. Dendritic vulnerability in neurodegenerative disease: insights from analyses of cortical pyramidal neurons in transgenic mouse models. Brain Struct. Funct. 2010, 214:181-199.
66. Mairet-Coello G., Courchet J., Pieraut S., Courchet V., Maximov A., Polleux F. The CAMKK2-AMPK kinase pathway mediates the synaptotoxic effects of Abeta oligomers through Tau phosphorylation. Neuron 2013, 78:94-108.
67. Mao T., O'Connor D.H., Scheuss V., Nakai J., Svoboda K. Characterization and subcellular targeting of GCaMP-type genetically-encoded calcium indicators. PLoS One 2008, 3:e1796.
68. Martel M.A., Ryan T.J., Bell K.F., Fowler J.H., McMahon A., Al-Mubarak B., Komiyama N.H., Horsburgh K., Kind P.C., Grant S.G., Wyllie D.J., Hardingham G.E. The subtype of GluN2 C-terminal domain determines the response to excitotoxic insults. Neuron 2012, 74:543-556.
69. Matsuzawa D., Hashimoto K. Magnetic resonance spectroscopy study of the antioxidant defense system in schizophrenia. Antioxid. Redox Signal. 2011, 15:2057-2065.
70. Mehta A., Prabhakar M., Kumar P., Deshmukh R., Sharma P.L. Excitotoxicity: bridge to various triggers in neurodegenerative disorders. Eur. J. Pharmacol. 2013, 698:6-18.
71. Melo A., Monteiro L., Lima R.M., Oliveira D.M., Cerqueira M.D., El-Bacha R.S. Oxidative stress in neurodegenerative diseases: mechanisms and therapeutic perspectives. Oxid. Med. Cell. Longev. 2011, 2011:467180.
72. Milnerwood A., Gladding C., Pouladi M., Kaufman A., Hines R., Boyd J., Ko R., Vasuta O., Graham R., Hayden M., Murphy T., Raymond L. Early increase in extrasynaptic NMDA receptor signalling and expression contributes to phenotype onset in Huntington's disease mice. Neuron 2010, 65:178-190.
73. Mizielinska S.M., Greenwood S.M., Tummala H., Connolly C.N. Rapid dendritic and axonal responses to neuronal insults. Biochem. Soc. Trans. 2009, 37:1389-1393.
74. Nakamura T., Cho D.H., Lipton S.A. Redox regulation of protein misfolding, mitochondrial dysfunction, synaptic damage, and cell death in neurodegenerative diseases. Exp. Neurol. 2012, 238:12-21.
75. Nicholls D.G. Simultaneous monitoring of ionophore- and inhibitor-mediated plasma and mitochondrial membrane potential changes in cultured neurons. J. Biol. Chem. 2006, 281:14864-14874.
76. Nicholls D.G. Mitochondrial calcium function and dysfunction in the central nervous system. Biochim. Biophys. Acta 2009, 1787:1416-1424.
77. Okamoto S., Pouladi M.A., Talantova M., Yao D., Xia P., Ehrnhoefer D.E., Zaidi R., Clemente A., Kaul M., Graham R.K., Zhang D., Vincent Chen H.S., Tong G., Hayden M.R., Lipton S.A. Balance between synaptic versus extrasynaptic NMDA receptor activity influences inclusions and neurotoxicity of mutant huntingtin. Nat. Med. 2009, 15:1407-1413.
78. Olney J.W. Brain lesions, obesity, and other disturbances in mice treated with monosodium glutamate. Science 1969, 164:719-721.
79. Papadia S., Stevenson P., Hardingham N.R., Bading H., Hardingham G.E. Nuclear Ca2+ and the cAMP response element-binding protein family mediate a late phase of activity-dependent neuroprotection. J. Neurosci. 2005, 25:4279-4287.
80. Parsons M.P., Raymond L.A. Extrasynaptic NMDA receptor involvement in central nervous system disorders. Neuron 2014, 82:279-293.
81. Puddifoot C., Martel M.A., Soriano F.X., Camacho A., Vidal-Puig A., Wyllie D.J., Hardingham G.E. PGC-1alpha negatively regulates extrasynaptic NMDAR activity and excitotoxicity. J. Neurosci. 2012, 32:6995-7000.
82. Qiu J., Tan Y.W., Hagenston A.M., Martel M.A., Kneisel N., Skehel P.A., Wyllie D.J., Bading H., Hardingham G.E. Mitochondrial calcium uniporter Mcu controls excitotoxicity and is transcriptionally repressed by neuroprotective nuclear calcium signals. Nat. Commun. 2013, 4:2034.
83. Rardin M.J., Wiley S.E., Naviaux R.K., Murphy A.N., Dixon J.E. Monitoring phosphorylation of the pyruvate dehydrogenase complex. Anal. Biochem. 2009, 389:157-164.
84. Rocher A.B., Kinson M.S., Luebke J.I. Significant structural but not physiological changes in cortical neurons of 12-month-old Tg2576 mice. Neurobiol. Dis. 2008, 32:309-318.
85. Siskova Z., Justus D., Kaneko H., Friedrichs D., Henneberg N., Beutel T., Pitsch J., Schoch S., Becker A., von der Kammer H., Remy S. Dendritic structural degeneration is functionally linked to cellular hyperexcitability in a mouse model of Alzheimer's disease. Neuron 2014, 84:1023-1033.
86. Soriano F.X., Papadia S., Hofmann F., Hardingham N.R., Bading H., Hardingham G.E. Preconditioning doses of NMDA promote neuroprotection by enhancing neuronal excitability. J. Neurosci. 2006, 26:4509-4518.
87. Spires T.L., Hyman B.T. Neuronal structure is altered by amyloid plaques. Rev. Neurosci. 2004, 15:267-278.
88. Wahl A.S., Buchthal B., Rode F., Bomholt S.F., Freitag H.E., Hardingham G.E., Ronn L.C., Bading H. Hypoxic/ischemic conditions induce expression of the putative pro-death gene Clca1 via activation of extrasynaptic N-methyl-d-aspartate receptors. Neuroscience 2009, 158:344-352.
89. Wyllie D.J., Livesey M.R., Hardingham G.E. Influence of GluN2 subunit identity on NMDA receptor function. Neuropharmacology 2013, 74:4-17.
90. Yu S.W., Wang H., Poitras M.F., Coombs C., Bowers W.J., Federoff H.J., Poirier G.G., Dawson T.M., Dawson V.L. Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science 2002, 297:259-263.
91. Zundorf G., Reiser G. Calcium dysregulation and homeostasis of neural calcium in the molecular mechanisms of neurodegenerative diseases provide multiple targets for neuroprotection. Antioxid. Redox Signal. 2011, 14:1275-1288.