Mitochondrial base excision repair in mouse synaptosomes during normal aging and in a model of Alzheimer's disease

Neurobiology of Aging

Volumn 33, Issue 4, 2012, Pages 694-707

  Gredilla, Ricardo ^a,c   Weissman, Lior ^b   Yang, Jenq Lin ^b   Bohr, Vilhelm A ^b   Stevnsner, Tinna ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b NATIONAL INSTITUTE ON AGING   (United States)

^c UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

DNA repair; Mitochondria; Neurodegeneration; Synaptic dysfunction

Indexed keywords

AMYLOID PRECURSOR PROTEIN; DNA (APURINIC OR APYRIMIDINIC SITE) LYASE; KINESIN; PRESENILIN 1; TAU PROTEIN; URACIL DNA GLYCOSIDASE;

AGING; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN MITOCHONDRION; BRAIN SYNAPTOSOME; CONTROLLED STUDY; EXCISION REPAIR; MALE; MOUSE; NERVE FIBER TRANSPORT; NONHUMAN; PRIORITY JOURNAL;

AGE FACTORS; AGING; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; DNA DAMAGE; DNA GLYCOSYLASES; DNA REPAIR; DNA, MITOCHONDRIAL; HUMANS; LAMIN TYPE A; MALE; MICE; MICE, TRANSGENIC; MICROSCOPY, ELECTRON, TRANSMISSION; MITOCHONDRIA; PRESENILIN-1; SYNAPTOSOMES; TAU PROTEINS; VOLTAGE-DEPENDENT ANION CHANNEL 1;

EID: 84856969873     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2010.06.019     Document Type: Article

References (65)

1. Akbari M., Visnes T., Krokan H.E., Otterlei M. Mitochondrial base excision repair of uracil and AP sites take place by single-nucleotide insertion and long-patch DNA synthesis. DNA Repair 2008, 7:605-616.
2. Barja G. The quantitative measurement of H2O2 generation in isolated mitochondria. J. Bioenerg. Biomembr. 2002, 34:227-233.
3. Barja G. Free radicals and aging. Trends Neurosci. 2004, 27:595-600.
4. Beal M.F. Mitochondria take center stage in aging and neurodegeneration. Ann. Neurol. 2005, 58:495-505.
5. Bohr V.A. Repair of oxidative DNA damage in nuclear and mitochondrial DNA, and some changes with aging in mammalian cells. Free Radic. Biol. Med. 2002, 32:804-812.
6. Borrás C., Sastre J., García-Sala D., Lloret A., Pallardó F.V., Viña J. Mitochondria from females exhibit higher antioxidant gene expression and lower oxidative damage than males. Free Radic. Biol. Med. 2003, 34:546-552.
7. Bota D.A., Davies K.J.A. Protein degradation in mitochondria: implications for oxidative stress, aging and disease, a novel etiological classification of mitochondrial proteolytic disorders. Mitochondrion 2001, 1:33-49.
8. Brown M.R., Sullivan P.G., Geddes J.W. Synaptic mitochondria are more susceptible to Ca2+ overload than nonsynaptic mitochondria. J. Biol. Chem. 2006, 281:11658-11668.
9. Cantuti-Castelvetri I., Lin M.T., Zheng K., Keller-McGandy C.E., Betensky R.A., Jonhs D.R., Flint Beal M., Standaert D.G., Simon D.K. Somatic mitochondrial DNA mutations in single neurons and glia. Neurobiol. Aging 2005, 26:1343-1355.
10. Chatterjee A., Singh K.K. Uracil-DNA glycosylase-deficient yeast exhibit a mitochondrial mutator phenotype. Nucleic Acids Res. 2001, 29:4935-4940.
11. Chen D.X., Minami M., Henshall D.C., Meller R., Kisby G., Simon R.P. Upregulation of mitochondrial base-excision repair capability within rat brain after brief ischemia. J. Cereb. Blood Flow Metab. 2003, 23:88-98.
12. Chen D., Cao G., Hastings T., Feng Y., Pei W., O'Horo C., Chen J. Age-related decline of DNA repair activity for oxidative lesions in rat brain mitochondria. J. Neurochem. 2002, 81:1273-1284.
13. Clayton D.A., Doda J.M., Friedberg E.C. The absence of a pyrimidine dimer repair mechanism in mammalian mitochondria. Proc. Natl. Acad. Sci. U. S. A. 1974, 71:2777-2781.
14. Cortina M.S., Gordon W.C., Lukiw W.J., Bazan N.G. Oxidative stress-induced retinal damage up-regulates DNA polymerase gamma and 8-oxoguanine-DNA-glycosylase in photoreceptor synaptic mitochondria. Exp. Eye Res. 2005, 81:742-750.
15. Cross D.J., Flexman J.A., Anzai Y., Maravilla K.R., Minoshima S. Age-related decrease in axonal transport measured by MR imaging in vivo. Neuroimage 2008, 39:915-926.
16. 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.
17. Dröge W., Schipper H.M. Oxidative stress and aberrant signaling in aging and cognitive decline. Aging Cell 2007, 6:361-370.
18. Fontán-Lozano A., López-Llunch G., Delgado-García J.M., Navas P., Carrión A.M. Molecular bases of caloric restriction regulation of neuronal synaptic plasticity. Mol. Neurobiol. 2008, 38:167-177.
19. Foster T.C. Calcium homeostasis and modulation of synaptic plasticity in the aged brain. Aging Cell 2007, 6:319-325.
20. Gabbita S.P., Lovell M.A., Markesbery W.R. Increased nuclear DNA oxidation in the brain in Alzheimer's disease. J. Neurochem 1998, 71:2034-2040.
21. Gredilla R., Garm C., Holm R., Bohr V.A., Stevnsner T. Differential age-related changes in mitochondrial DNA repair activities in mouse brain regions. Neurobiol. Aging 2010, 31:993-1002.
22. Hagen L., Kavli B., Sousa M.M., Torseth K., Liabakk N.B., Sundheim O., Peña-Diaz J., Otterlei M., Hørning O., Jensen O.N., Krokan H.E., Slupphaug G. Cell cycle-specific UNG2 phosphorylations regulate protein turnover, activity and association with RPA. EMBO J 2008, 27:51-61.
23. Hollenbeck P.J. Products of endocytosis and autophagy are retrieved from axons by regulated retrograde organelle transport. J. Cell Biol. 1993, 121:305-315.
24. Hollenbeck P.J., Saxton W.M. The axonal transport of mitochondria. J. Cell Sci. 2005, 118:5411-5419.
25. Huang C., Miyamoto H., Huang R.H. The mouse cerebellum from 1 to 34 months: Parallel fibers. Neurobiol. Aging 2006, 27:1715-1718.
26. Hübscher U., Kuenzle C.C., Spadari S. Identity of DNA polymerase γ from synaptosomal mitochondria and rat-brain nuclei. Eur. J. Biochem. 1977, 81:249-258.
27. Hübscher U., Kuenzle C.C., Spadari S. Functional roles of DNA polymerases β and γ. Proc. Natl. Acad. Sci. U. S. A. 1979, 76:2316-2320.
28. Imam S., Karahalil B., Hogue B., Souza-Pinto N., Bohr V. Mitochondrial and nuclear DNA-repair capacity of various brain regions in mouse is altered in an age-dependent manner. Neurobiol. Aging 2006, 27:1129-1136.
29. Jernigan T.L., Archibald S.L., Fennema-Notestine C., Gamst A.C., Stout J.C., Bonner J., Hesselink J.R. Effects of age on tissues and regions of the cerebrum and cerebellum. Neurobiol. Aging 2001, 22:581-594.
30. Kilbride S.N., Telford J.E., Davey G.P. Age-related changes in H2O2 production and bioenergetics in rat brain synaptosomes. Biochim. Biophys. Acta 2008, 1777:783-788.
31. Kimura N., Imamura O., Ono F., Terao K. Aging attenuates dynactin-dynein interaction: down-regulation of dynein causes accumulation of endogenous Tau and Amyloid precursor protein in human neuroblastoma cells. J. Neurosci. Res 2007, 85:2909-2916.
32. Kimura N., Inoue M., Okabayashi S., Ono F., Negishi T. Dynein dysfunction induces endocytic pathology accompanied by an increase in rab GTPases. J. Biol. Chem. 2009, 284:31291-31301.
33. Knobloch M., Mansuy I.M. Dendritic spine loss and synaptic alterations in Alzheimer's disease. Mol. Neurobiol. 2008, 37:73-82.
34. Kristian T., Hopkins I.B., McKenna M.C., Fiskum G. Isolation of mitochondria with high respiratory control from primary cultures of neurons and astrocytes using nitrogen cavitation. J. Neurosci. Methods 2006, 152:136-143.
35. Kujoth G.C., Bradshaw P.C., Haroon S., Prolla T.A. The role of mitochondrial DNA mutations in mammalian aging. PLoS Genet. 2007, 3:e24.
36. Lai J.C.K., Clark J.B. Preparation of synaptic and nonsynaptic mitochondria from mammalian brain. Methods Enzymol. 1979, 55:51-60.
37. Lai J.C.K., Walsh J.M., Dennis S.C., Clark J.B. Synaptic and non-synaptic mitochondria from rat brain: isolation and characterization. J. Neurochem. 1977, 28:625-631.
38. Liu P., Qian L., Sung J., deSouza-Pinto N., Zheng L., Bogenhagen D.F., Bohr V.A., Wilson D.M., Shen B., Demple B. Removal of oxidative DNA damage via FEN1-dependent long-patch base excision repair in human cell mitochondria. Mol. Cell. Biol. 2008, 28:4975-4987.
39. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 1951, 193:265-275.
40. Ly C.V., Verstreken P. Mitochondria at the synapse. Neuroscientist 2006, 12:291-299.
41. Martinez B., Rodrigues T.B., Gine E., Kaninda J.P., Perez-Castillo A., Santos A. Hypothyroidism decreases the biogenesis in free mitochondria and neuronal oxygen consumption in the cerebral cortez of developing rats. Endocrinology 2009, 150:3953-3959.
42. Mattson M.P. Pathways towards and away from Alzheimer's disease. Nature 2004, 430:631-639.
43. Mattson M.P., Partin J., Begley J.G. Amyloid beta-peptide induces apoptosis-related events in synapses and dendrites. Brain Res. 1998, 807:759-766.
44. Melov S. Modeling mitochondrial function in aging neurons. Trends Neurosci. 2004, 27:601-606.
45. Mora F., Segovia G., del Arco A. Aging, plasticity and environmental enrichment: structural changes and neurotransmitter dynamics in several areas of the brain. Brain Res. Rev. 2007, 55:78-88.
46. Morocz M., Kalman J., Juhasz A., Sinko I., McGlynn A.P., Downes C.S., Janka Z., Rasko I. Elevated levels of oxidative DNA damage in lymphocytes from patients with Alzheimer's disease. Neurobiol. Aging 2002, 23:47-53.
47. Morrison J.H., Hof P.R. Selective vulneravility of corticocortical and hippocampal circuits in aging and Alzheimer's disease. Prog. Brain Res. 2002, 136:467-486.
48. Nyaga S.G., Bohr V.A. Characterization of specialized mtDNA glycosylases. Mitochondrial DNA: Methods and Protocols 2002, 227-244. Humana Press, Totowa, NJ. W.C. Copeland (Ed.).
49. Oddo S., Caccamo A., Kitazawa M., Tseng B.P., Laferla F.M. Amyloid deposition precedes tangle formation in a triple transgenic model of Alzheimer's disease. Neurobiol. Aging 2003, 24:1063-1070.
50. Oddo S., Caccamo A., Sheperd J.D., Murphy M.P., Golde T.E., Kayed R., Metherate R., Mattson M.P., Akbari Y., Laferla F.M. Triple-transgenic model of Alzheimer's disease with plaques and tangles, intracellular Abeta and synaptic dysfunction. Neuron 2003, 39:409-421.
51. Ogihara M., Tanno M., Izumiyama N., Nakamura H., Taguchi T. Increase in DNA polymerase γ in the hearts of adriamycin-administered rats. Exp. Mol. Pathol 2002, 73:234-241.
52. Rendon A., Masmoudi A. Purification of non-synaptic and synaptic mitochondria and plasma membranes from rat brain by rapid Percoll gradient procedure. J. Neurosci. Methods 1985, 14:41-51.
53. Reddy P.H. Mitochondrial dysfunction in aging and Alzheimer's disease: strategies to protect neurons. Antioxid. Redox Signal. 2007, 9:1647-1658.
54. Schrimpf S.P., Meskenaite V., Brunner E., Rutishauser D., Walther P., Eng J., Aebersold R., Sonderegger P. Proteomic analysis of synaptosomes using isotope-coded affinity tags and mass spectrometry. Proteomics 2005, 5:2531-2541.
55. Selkoe D.J. Alzheimer's disease is a synaptic failure. Science 2002, 298:789-791.
56. Shi P., Gal J., Kwinter D.M., Liu X., Zhu H. Mitochondrial dysfunction in amyotrophic lateral sclerosis. Biochim. Biophys. Acta 2010, 1802:45-51.
57. Souza-Pinto N.C., Croteau D.L., Hudson E.K., Hansford R.G., Bohr V.A. Ageassociated increase in 8-oxo-deoxyguanosine glycosylase/AP lyase activity increases in mitochondrial but not in nuclear extracts. Nucleic Acids Res 1999, 27:1935-1942.
58. Stokin G.B., Goldstein L.S.B. Axonal transport and Alzheimer's disease. Annu. Rev. Biochem 2006, 75:607-627.
59. Stuart J.A., Karahalil B., Hogue B.A., Souza-Pinto N., Bohr V.A. Mitochondrial and nuclear DNA base excision repair are affected differently by caloric restriction. FASEB J. 2004, 18:595-597.
60. Tatsua T., Langer T. Quality control of mitochondria: protection against neurodegeneration and ageing. EMBO J 2008, 27:306-314.
61. Vermulst M., Bielas J.H., Kujoth G.C., Ladiges W.C., Rabinovitch P.S., Prolla T.A., Loeb L.A. Mitochondrial point mutations do not limit the natural lifespan of mice. Nat. Genet. 2007, 39:540-543. mitochondria, and neurodegeneration. Neuroscience 145, 1318-1329.
62. Weissman L., Jo D., Sørensen M.M., Souza-Pinto N., Markersbery 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.
63. Weissman L., Souza-Pinto N., Mattson M.P., Bohr V.A. DNA base excision repair activities in mouse models of Alzheimer's disease. Neurobiol. Aging 2009, 30:2080-2081.
64. West M.J., Coleman P.D., Flood D.G., Troncoso J.C. Differences in the pattern of hippocampal neuronal loss in normal ageing and Alzheimer's disease. Lancet 1994, 344:769-772.
65. West M.J., Kawas C.H., Stewart W.F., Rudow G.L., Troncoso J.C. Hippocampal neurons in pre-clinical Alzheimer's disease. Neurobiol. Aging 2004, 25:1205-1212.