The excitatory neurotransmitter glutamate stimulates DNA repair to increase neuronal resiliency

Mechanisms of Ageing and Development

Volumn 132, Issue 8-9, 2011, Pages 405-411

  Yang, Jenq Lin ^a   Sykora, Peter ^a   Wilson, David M ^a   Mattson, Mark P ^a   Bohr, Vilhelm A ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

APE1; Excitotoxicity; Glutamate; Neurodegenerative diseases; Oxidative DNA damage

Indexed keywords

AMYLOID PRECURSOR PROTEIN; CALCIUM ION; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DJ 1 PROTEIN; DNA DIRECTED DNA POLYMERASE BETA; DNA GLYCOSYLTRANSFERASE; GLUTAMIC ACID; HUNTINGTIN; PARKIN; PRESENILIN 1;

ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; APE1 GENE; ARTICLE; CALCIUM TRANSPORT; CELL DEATH; CELL PROLIFERATION; CELLULAR STRESS RESPONSE; DNA DAMAGE; DNA REPAIR; EXCISION REPAIR; EXCITOTOXICITY; GENE; GENE EXPRESSION; HUMAN; HUNTINGTON CHOREA; NERVE CELL; NERVE DEGENERATION; NEUROPROTECTION; NEUROTRANSMISSION; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; TOXICITY TESTING;

ANIMALS; CALCIUM; CALCIUM SIGNALING; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DNA REPAIR; GLUTAMIC ACID; HUMANS; MITOCHONDRIA; NEURODEGENERATIVE DISEASES; NEURONS; NEUROTRANSMITTER AGENTS; OXIDATION-REDUCTION; PROTEIN KINASE C; REACTIVE OXYGEN SPECIES;

VERTEBRATA;

EID: 80053117501     PISSN: 00476374     EISSN: 18726216     Source Type: Journal    
DOI: 10.1016/j.mad.2011.06.005     Document Type: Article

References (81)

1. Aguirre N., Beal M.F., Matson W.R., Bogdanov M.B. Increased oxidative damage to DNA in an animal model of amyotrophic lateral sclerosis. Free Radic. Res. 2005, 39:383-388.
2. Alam Z.I., Jenner A., Daniel S.E., Lees A.J., Cairns N., Marsden C.D., Jenner P., Halliwell B. Oxidative DNA damage in the parkinsonian brain: an apparent selective increase in 8-hydroxyguanine levels in substantia nigra. J. Neurochem. 1997, 69:1196-1203.
3. Ando K., Hirao S., Kabe Y., Ogura Y., Sato I., Yamaguchi Y., Wada T., Handa H. A new APE1/Ref-1-dependent pathway leading to reduction of NF-kappaB and AP-1, and activation of their DNA-binding activity. Nucleic Acids Res. 2008, 36:4327-4336.
4. Berkowitz L.A., Riabowol K.T., Gilman M.Z. Multiple sequence elements of a single functional class are required for cyclic AMP responsiveness of the mouse c-fos promoter. Mol. Cell. Biol. 1989, 9:4272-4281.
5. Bezprozvanny I., Hayden M.R. Deranged neuronal calcium signaling and Huntington disease. Biochem. Biophys. Res. Commun. 2004, 322:1310-1317.
6. Bito H., Deisseroth K., Tsien R.W. CREB phosphorylation and dephosphorylation: a Ca(2+)- and stimulus duration-dependent switch for hippocampal gene expression. Cell 1996, 87:1203-1214.
7. Bogdanov M.B., Andreassen O.A., Dedeoglu A., Ferrante R.J., Beal M.F. Increased oxidative damage to DNA in a transgenic mouse model of Huntington's disease. J. Neurochem. 2001, 79:1246-1249.
8. Bozner P., Grishko V., LeDoux S.P., Wilson G.L., Chyan Y.C., Pappolla M.A. The amyloid beta protein induces oxidative damage of mitochondrial DNA. J. Neuropathol. Exp. Neurol. 1997, 56:1356-1362.
9. Brouillet E., Conde F., Beal M.F., Hantraye P. Replicating Huntington's disease phenotype in experimental animals. Prog. Neurobiol. 1999, 59:427-468.
10. Browne S.E., Bowling A.C., MacGarvey U., Baik M.J., Berger S.C., Muqit M.M., Bird E.D., Beal M.F. Oxidative damage and metabolic dysfunction in Huntington's disease: selective vulnerability of the basal ganglia. Ann. Neurol. 1997, 41:646-653.
11. Cabelof D.C., Raffoul J.J., Yanamadala S., Guo Z., Heydari A.R. Induction of DNA polymerase beta-dependent base excision repair in response to oxidative stress in vivo. Carcinogenesis 2002, 23:1419-1425.
12. Cabelof D.C., Yanamadala S., Raffoul J.J., Guo Z., Soofi A., Heydari A.R. Caloric restriction promotes genomic stability by induction of base excision repair and reversal of its age-related decline. DNA Repair (Amst.) 2003, 2:295-307.
13. Carlezon W.A., Duman R.S., Nestler E.J. The many faces of CREB. Trends Neurosci. 2005, 28:436-445.
14. Chen K.H., Yakes F.M., Srivastava D.K., Singhal R.K., Sobol R.W., Horton J.K., Van H.B., Wilson S.H. Up-regulation of base excision repair correlates with enhanced protection against a DNA damaging agent in mouse cell lines. Nucleic Acids Res. 1998, 26:2001-2007.
15. Chinopoulos C., Tretter L., Rozsa A., dam-Vizi V. Exacerbated responses to oxidative stress by an Na(+) load in isolated nerve terminals: the role of ATP depletion and rise of [Ca(2+)](i). J. Neurosci. 2000, 20:2094-2103.
16. Choi D.W. Glutamate neurotoxicity and diseases of the nervous system. Neuron 1988, 1:623-634.
17. Choi S., Klingauf J., Tsien R.W. Postfusional regulation of cleft glutamate concentration during LTP at 'silent synapses'. Nat. Neurosci. 2000, 3:330-336.
18. Corona J.C., Romo L.B., Tapia R. Glutamate excitotoxicity and therapeutic targets for amyotrophic lateral sclerosis. Expert. Opin. Ther. Targets 2007, 11:1415-1428.
19. Culmsee C., Zhu X., Yu Q.S., Chan S.L., Camandola S., Guo Z., Greig N.H., Mattson M.P. A synthetic inhibitor of p53 protects neurons against death induced by ischemic and excitotoxic insults, and amyloid beta-peptide. J. Neurochem. 2001, 77:220-228.
20. De L.G., Russo M.T., Degan P., Tiveron C., Zijno A., Meccia E., Ventura I., Mattei E., Nakabeppu Y., Crescenzi M., Pepponi R., Pezzola A., Popoli P., Bignami M. A role for oxidized DNA precursors in Huntington's disease-like striatal neurodegeneration. PLoS Genet. 2008, 4:e1000266.
21. Dingledine R., Borges K., Bowie D., Traynelis S.F. The glutamate receptor ion channels. Pharmacol. Rev. 1999, 51:7-61.
22. Dong X.X., Wang Y., Qin Z.H. Molecular mechanisms of excitotoxicity and their relevance to pathogenesis of neurodegenerative diseases. Acta Pharmacol. Sin. 2009, 30:379-387.
23. Endres M., Biniszkiewicz D., Sobol R.W., Harms C., Ahmadi M., Lipski A., Katchanov J., Mergenthaler P., Dirnagl U., Wilson S.H., Meisel A., Jaenisch R. Increased postischemic brain injury in mice deficient in uracil-DNA glycosylase. J. Clin. Invest. 2004, 113:1711-1721.
24. Enokido Y., Tamura T., Ito H., Arumughan A., Komuro A., Shiwaku H., Sone M., Foulle R., Sawada H., Ishiguro H., Ono T., Murata M., Kanazawa I., Tomilin N., Tagawa K., Wanker E.E., Okazawa H. Mutant huntingtin impairs Ku70-mediated DNA repair. J. Cell Biol. 2010, 189:425-443.
25. Facheris M., Beretta S., Ferrarese C. Peripheral markers of oxidative stress and excitotoxicity in neurodegenerative disorders: tools for diagnosis and therapy?. J. Alzheimers Dis. 2004, 6:177-184.
26. Ghosh A., Ginty D.D., Bading H., Greenberg M.E. Calcium regulation of gene expression in neuronal cells. J. Neurobiol. 1994, 25:294-303.
27. Gleichmann M., Zhang Y., Wood W.H., Becker K.G., Mughal M.R., Pazin M.J., van P.H., Kobilo T., Zonderman A.B., Troncoso J.C., Markesbery W.R., Mattson M.P. Molecular changes in brain aging and Alzheimer's disease are mirrored in experimentally silenced cortical neuron networks. Neurobiol. Aging 2010.
28. Gonsette R.E. Neurodegeneration in multiple sclerosis: the role of oxidative stress and excitotoxicity. J. Neurol. Sci. 2008, 274:48-53.
29. Gonzalez G.A., Montminy M.R. Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell 1989, 59:675-680.
30. Hardy J., Cai H., Cookson M.R., Gwinn-Hardy K., Singleton A. Genetics of Parkinson's disease and parkinsonism. Ann. Neurol. 2006, 60:389-398.
31. Hazell A.S., Butterworth R.F., Hakim A.M. Cerebral vulnerability is associated with selective increase in extracellular glutamate concentration in experimental thiamine deficiency. J. Neurochem. 1993, 61:1155-1158.
32. Hongpaisan J., Winters C.A., Andrews S.B. Calcium-dependent mitochondrial superoxide modulates nuclear CREB phosphorylation in hippocampal neurons. Mol. Cell. Neurosci. 2003, 24:1103-1115.
33. Intano G.W., Cho E.J., McMahan C.A., Walter C.A. Age-related base excision repair activity in mouse brain and liver nuclear extracts. J. Gerontol. A: Biol. Sci. Med. Sci. 2003, 58:205-211.
34. Jiang X., Zhu D., Okagaki P., Lipsky R., Wu X., Banaudha K., Mearow K., Strauss K.I., Marini A.M. N-methyl-d-aspartate and TrkB receptor activation in cerebellar granule cells: an in vitro model of preconditioning to stimulate intrinsic survival pathways in neurons. Ann. N. Y. Acad. Sci. 2003, 993:134-145.
35. Kapogiannis D., Mattson M.P. Disrupted energy metabolism and neuronal circuit dysfunction in cognitive impairment and Alzheimer's disease. Lancet Neurol. 2010.
36. Kovtun I.V., Liu Y., Bjoras M., Klungland A., Wilson S.H., McMurray C.T. OGG1 initiates age-dependent CAG trinucleotide expansion in somatic cells. Nature 2007, 447:447-452.
37. Krishna T.H., Mahipal S., Sudhakar A., Sugimoto H., Kalluri R., Rao K.S. Reduced DNA gap repair in aging rat neuronal extracts and its restoration by DNA polymerase beta and DNA-ligase. J. Neurochem. 2005, 92:818-823.
38. Kruman I.I., Culmsee C., Chan S.L., Kruman Y., Guo Z., Penix L., Mattson M.P. Homocysteine elicits a DNA damage response in neurons that promotes apoptosis and hypersensitivity to excitotoxicity. J. Neurosci. 2000, 20:6920-6926.
39. Kruman I.I., Kumaravel T.S., Lohani A., Pedersen W.A., Cutler R.G., Kruman Y., Haughey N., Lee J., Evans M., Mattson M.P. Folic acid deficiency and homocysteine impair DNA repair in hippocampal neurons and sensitize them to amyloid toxicity in experimental models of Alzheimer's disease. J. Neurosci. 2002, 22:1752-1762.
40. Kruman I.I., Pedersen W.A., Springer J.E., Mattson M.P. ALS-linked Cu/Zn-SOD mutation increases vulnerability of motor neurons to excitotoxicity by a mechanism involving increased oxidative stress and perturbed calcium homeostasis. Exp. Neurol. 1999, 160:28-39.
41. Kruman I.I., Schwartz E., Kruman Y., Cutler R.G., Zhu X., Greig N.H., Mattson M.P. Suppression of uracil-DNA glycosylase induces neuronal apoptosis. J. Biol. Chem. 2004, 279:43952-43960.
42. Langlais P.J., Zhang S.X. Extracellular glutamate is increased in thalamus during thiamine deficiency-induced lesions and is blocked by MK-801. J. Neurochem. 1993, 61:2175-2182.
43. Lau A., Tymianski M. Glutamate receptors, neurotoxicity and neurodegeneration. Pflugers Arch. 2010, 460:525-542.
44. Liu D., Croteau D.L., Souza-Pinto N., Pitta M., Tian J., Wu C., Jiang H., Mustafa K., Keijzers G., Bohr V.A., Mattson M.P. Evidence that OGG1 glycosylase protects neurons against oxidative DNA damage and cell death under ischemic conditions. J. Cereb. Blood Flow Metab. 2010.
45. Liu Y., Prasad R., Beard W.A., Kedar P.S., Hou E.W., Shock D.D., Wilson S.H. Coordination of steps in single-nucleotide base excision repair mediated by apurinic/apyrimidinic endonuclease 1 and DNA polymerase beta. J. Biol. Chem. 2007, 282:13532-13541.
46. Marini A.M., Ueda Y., June C.H. Intracellular survival pathways against glutamate receptor agonist excitotoxicity in cultured neurons. Intracellular calcium responses. Ann. N. Y. Acad. Sci. 1999, 890:421-437.
47. Matthews R.P., Guthrie C.R., Wailes L.M., Zhao X., Means A.R., McKnight G.S. Calcium/calmodulin-dependent protein kinase types II and IV differentially regulate CREB-dependent gene expression. Mol. Cell. Biol. 1994, 14:6107-6116.
48. Mattson M.P. Glutamate and neurotrophic factors in neuronal plasticity and disease. Ann. N. Y. Acad. Sci. 2008, 1144:97-112.
49. Mattson M.P. Pathways towards and away from Alzheimer's disease. Nature 2004, 430:631-639.
50. Mattson M.P. Excitotoxic and excitoprotective mechanisms: abundant targets for the prevention and treatment of neurodegenerative disorders. Neuromolecular Med. 2003, 3:65-94.
51. Mattson M.P., Cheng B., Davis D., Bryant K., Lieberburg I., Rydel R.E. Beta-amyloid peptides destabilize calcium homeostasis and render human cortical neurons vulnerable to excitotoxicity. J. Neurosci. 1992, 12:376-389.
52. Mattson M.P., Dou P., Kater S.B. Outgrowth-regulating actions of glutamate in isolated hippocampal pyramidal neurons. J. Neurosci. 1988, 8:2087-2100.
53. Mattson M.P., Goodman Y., Luo H., Fu W., Furukawa K. Activation of NF-kappaB protects hippocampal neurons against oxidative stress-induced apoptosis: evidence for induction of manganese superoxide dismutase and suppression of peroxynitrite production and protein tyrosine nitration. J. Neurosci. Res. 1997, 49:681-697.
54. Mattson M.P., Lee R.E., Adams M.E., Guthrie P.B., Kater S.B. Interactions between entorhinal axons and target hippocampal neurons: a role for glutamate in the development of hippocampal circuitry. Neuron 1988, 1:865-876.
55. Meredith G.E., Totterdell S., Beales M., Meshul C.K. Impaired glutamate homeostasis and programmed cell death in a chronic MPTP mouse model of Parkinson's disease. Exp. Neurol. 2009, 219:334-340.
56. Polidori M.C., Mecocci P., Browne S.E., Senin U., Beal M.F. Oxidative damage to mitochondrial DNA in Huntington's disease parietal cortex. Neurosci. Lett. 1999, 272:53-56.
57. Raji N.S., Krishna T.H., Rao K.S. DNA-polymerase alpha, beta, delta and epsilon activities in isolated neuronal and astroglial cell fractions from developing and aging rat cerebral cortex. Int. J. Dev. Neurosci. 2002, 20:491-496.
58. Ramana C.V., Boldogh I., Izumi T., Mitra S. Activation of apurinic/apyrimidinic endonuclease in human cells by reactive oxygen species and its correlation with their adaptive response to genotoxicity of free radicals. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:5061-5066.
59. Rao K.S., Annapurna V.V., Raji N.S. DNA polymerase-beta may be the main player for defective DNA repair in aging rat neurons. Ann. N. Y. Acad. Sci. 2001, 928:113-120.
60. Rao-Mirotznik R., Buchsbaum G., Sterling P. Transmitter concentration at a three-dimensional synapse. J. Neurophysiol. 1998, 80:3163-3172.
61. Reynolds I.J. Mitochondrial membrane potential and the permeability transition in excitotoxicity. Ann. N. Y. Acad. Sci. 1999, 893:33-41.
62. Rolig R.L., McKinnon P.J. Linking DNA damage and neurodegeneration. Trends Neurosci. 2000, 23:417-424.
63. Rolseth V., Runden-Pran E., Luna L., McMurray C., Bjoras M., Ottersen O.P. Widespread distribution of DNA glycosylases removing oxidative DNA lesions in human and rodent brains. DNA Repair (Amst.) 2008, 7:1578-1588.
64. Sengpiel B., Preis E., Krieglstein J., Prehn J.H. NMDA-induced superoxide production and neurotoxicity in cultured rat hippocampal neurons: role of mitochondria. Eur. J. Neurosci. 1998, 10:1903-1910.
65. Sheng M., Thompson M.A., Greenberg M.E. CREB: a Ca(2+)-regulated transcription factor phosphorylated by calmodulin-dependent kinases. Science 1991, 252:1427-1430.
66. Stetler R.A., Gao Y., Zukin R.S., Vosler P.S., Zhang L., Zhang F., Cao G., Bennett M.V., Chen J. Apurinic/apyrimidinic endonuclease APE1 is required for PACAP-induced neuroprotection against global cerebral ischemia. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:3204-3209.
67. Sugo N., Aratani Y., Nagashima Y., Kubota Y., Koyama H. Neonatal lethality with abnormal neurogenesis in mice deficient in DNA polymerase beta. EMBO J. 2000, 19:1397-1404.
68. Sykora P., Snow E.T. Modulation of DNA polymerase beta-dependent base excision repair in cultured human cells after low dose exposure to arsenite. Toxicol. Appl. Pharmacol. 2008, 228:385-394.
69. Tell G., Damante G., Caldwell D., Kelley M.R. The intracellular localization of APE1/Ref-1: more than a passive phenomenon?. Antioxid. Redox Signal. 2005, 7:367-384.
70. Unnikrishnan A., Prychitko T.M., Patel H.V., Chowdhury M.E., Pilling A.B., Ventrella-Lucente L.F., Papakonstantinou E.V., Cabelof D.C., Heydari A.R. Folate deficiency regulates expression of DNA polymerase beta in response to oxidative stress. Free Radic. Biol. Med. 2010.
71. Vasko M.R., Guo C., Kelley M.R. The multifunctional DNA repair/redox enzyme Ape1/Ref-1 promotes survival of neurons after oxidative stress. DNA Repair (Amst.) 2005, 4:367-379.
72. Wang J., Jacob N.K., Ladner K.J., Beg A., Perko J.D., Tanner S.M., Liyanarachchi S., Fishel R., Guttridge D.C. RelA/p65 functions to maintain cellular senescence by regulating genomic stability and DNA repair. EMBO Rep. 2009, 10:1272-1278.
73. Wang W., Osenbroch P., Skinnes R., Esbensen Y., Bjoras M., Eide L. The OGG1 DNA glycosylase is essential for mitochondrial maturation during differentiation of neural stem cells. Stem Cells 2010.
74. Wang Y., Chandran J.S., Cai H., Mattson M.P. DJ-1 is essential for long-term depression at hippocampal CA1 synapses. Neuromolecular Med. 2008, 10:40-45.
75. Weissman L., Jo D.G., Sorensen M.M., de Souza-Pinto N.C., Markesbery W.R., Mattson M.P., Bohr V.A. Defective DNA base excision repair in brain from individuals with Alzheimer's disease and amnestic mild cognitive impairment. Nucleic Acids Res. 2007, 35:5545-5555.
76. Wong A.W., McCallum G.P., Jeng W., Wells P.G. Oxoguanine glycosylase 1 protects against methamphetamine-enhanced fetal brain oxidative DNA damage and neurodevelopmental deficits. J. Neurosci. 2008, 28:9047-9054.
77. Wu G.Y., Deisseroth K., Tsien R.W. Activity-dependent CREB phosphorylation: convergence of a fast, sensitive calmodulin kinase pathway and a slow, less sensitive mitogen-activated protein kinase pathway. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:2808-2813.
78. Yang J.L., Takahashi T., Keijzers G., Mattson M.P., Bohr V.A. Neurons efficiently repair glutamate-induced oxidative DNA damage by a process involving CREB-mediated Up-regulation of APE1. J. Biol. Chem. 2010.
79. Yu Z., Zhou D., Bruce-Keller A.J., Kindy M.S., Mattson M.P. Lack of the p50 subunit of nuclear factor-kappaB increases the vulnerability of hippocampal neurons to excitotoxic injury. J. Neurosci. 1999, 19:8856-8865.
80. Zhang H., Li Q., Graham R.K., Slow E., Hayden M.R., Bezprozvanny I. Full length mutant huntingtin is required for altered Ca2+ signaling and apoptosis of striatal neurons in the YAC mouse model of Huntington's disease. Neurobiol. Dis. 2008, 31:80-88.
81. Zhang J., Perry G., Smith M.A., Robertson D., Olson S.J., Graham D.G., Montine T.J. Parkinson's disease is associated with oxidative damage to cytoplasmic DNA and RNA in substantia nigra neurons. Am. J. Pathol. 1999, 154:1423-1429.