Reduced apurinic/apyrimidinic endonuclease 1 activity and increased DNA damage in mitochondria are related to enhanced apoptosis and inflammation in the brain of senescence- accelerated P8 mice (SAMP8)

Barja G (2004) Free radicals and aging. Trends Neurosci 27:595–600 Barja G, Herrero A (2000) Oxidative damage to mitochondrial DNA is inversely related to maximum life span in the heart and brain of mammals. FASEB J 14:312–318 Beal MF (2005) Mitochondria take center stage in aging and neurodegeneration. Ann Neurol 58:495–505 Butterfield DA, Poon HF (2005) The senescence-accelerated prone mouse (SAMP8): a model of age-related cognitive decline with relevance to alterations of the gene expression and protein abnormalities in Alzheimer’s disease. Exp Gerontol 40:774–783 Caballero B, Vega-Naredo I, Sierra V, Huidobro-Fernandez C, Soria-Valles C, De Gonzalo-Calvo D, Tolivia D, Pallas M, Camins A, Rodriguez-Colunga MJ, Coto-Montes A (2009) Melatonin alters cell death processes in response to age-related oxidative stress in the brain of senescence-accelerated mice. J Pineal Res 46:106–114 Cantuti-Castelvetri I, Lin MT, Zheng K, Keller-McGandy CE, Betensky RA, Johns DR, Beal MF, Standaert DG, Simon DK (2005) Somatic mitochondrial DNA mutations in single neurons and glia. Neurobiol Aging 26:1343–1355 Canugovi C, Shamanna RA, Croteau DL, Bohr VA (2014) Base excision DNA repair levels in mitochondrial lysates of Alzheimer’s disease. Neurobiol Aging 35:1293–1300 Cheng XR, Zhou WX, Zhang YX (2014) The behavioral, pathological and therapeutic features of the senescence-accelerated mouse prone 8 strain as an Alzheimer’s disease animal model. Ageing Res Rev 13C:13–37 Choi JY, Kim HS, Kang HK, Lee DW, Choi EM, Chung MH (1999) Thermolabile 8-hydroxyguanine DNA glycosylase with low activity in senescence-accelerated mice due to a single-base mutation. Free Radic Biol Med 27:848–854 Cuesta S, Kireev R, Forman K, Garcia C, Escames G, Ariznavarreta C, Vara E, Tresguerres JA (2010) Melatonin improves inflammation processes in liver of senescence-accelerated prone male mice (SAMP8). Exp Gerontol 45:950–956 Cuesta S, Kireev R, Garcia C, Forman K, Escames G, Vara E, Tresguerres JA (2011) Beneficial effect of melatonin treatment on inflammation, apoptosis and oxidative stress on pancreas of a senescence accelerated mice model. Mech Ageing Dev 132:573–582 Edgar D, Shabalina I, Camara Y, Wredenberg A, Calvaruso MA, Nijtmans L, Nedergaard J, Cannon B, Larsson NG, Trifunovic A (2009) Random point mutations with major effects on protein-coding genes are the driving force behind premature aging in mtDNA mutator mice. Cell Metab 10:131–138 Figueiredo-Pereira ME, Rockwell P, Schmidt-Glenewinkel T, Serrano P (2014) Neuroinflammation and J2 prostaglandins: linking impairment of the ubiquitin-proteasome pathway and mitochondria to neurodegeneration. Front Mol Neurosci 7:104 Flood JF, Morley JE (1993) Age-related changes in footshock avoidance acquisition and retention in senescence accelerated mouse (SAM). Neurobiol Aging 14:153–157 Forman K, Vara E, Garcia C, Kireev R, Cuesta S, Acuna-Castroviejo D, Tresguerres JA (2010) Beneficial effects of melatonin on cardiological alterations in a murine model of accelerated aging. J Pineal Res 49:312–320 Gabbita SP, Lovell MA, Markesbery WR (1998) Increased nuclear DNA oxidation in the brain in Alzheimer’s disease. J Neurochem 71:2034–2040 Garcia-Matas S, Paul RK, Molina-Martinez P, Palacios H, Gutierrez VM, Corpas R, Pallas M, Cristofol R, de Cabo R, Sanfeliu C (2015) In vitro caloric restriction induces protective genes and functional rejuvenation in senescent SAMP8 astrocytes. Aging Cell 14:334–344 Glass CK, Saijo K, Winner B, Marchetto MC, Gage FH (2010) Mechanisms underlying inflammation in neurodegeneration. Cell 140:918–934 Gredilla R (2010) DNA damage and base excision repair in mitochondria and their role in aging. J Aging Res 2011:257093 Gredilla R, Stevnsner T (2012) Mitochondrial base excision repair assays. Methods Mol Biol 920:289–304 Gredilla R, Garm C, Holm R, Bohr VA, Stevnsner T (2010) Differential age-related changes in mitochondrial DNA repair activities in mouse brain regions. Neurobiol Aging 31:993–1002 Gredilla R, Weissman L, Yang JL, Bohr VA, Stevnsner T (2012) Mitochondrial base excision repair in mouse synaptosomes during normal aging and in a model of Alzheimer’s disease. Neurobiol Aging 33:694–707 Griffin WS, Sheng JG, Roberts GW, Mrak RE (1995) Interleukin-1 expression in different plaque types in Alzheimer’s disease: significance in plaque evolution. J Neuropathol Exp Neurol 54:276–281 Hegde ML, Hazra TK, Mitra S (2008) Early steps in the DNA base excision/single-strand interruption repair pathway in mammalian cells. Cell Res 18:27–47 Heneka MT, Golenbock DT, Latz E (2015) Innate immunity in Alzheimer’s disease. Nat Immunol 16:229–236 Hiona A, Sanz A, Kujoth GC, Pamplona R, Seo AY, Hofer T, Someya S, Miyakawa T, Nakayama C, Samhan-Arias AK, Servais S, Barger JL, Portero-Otin M, Tanokura M, Prolla TA, Leeuwenburgh C (2010) Mitochondrial DNA mutations induce mitochondrial dysfunction, apoptosis and sarcopenia in skeletal muscle of mitochondrial DNA mutator mice. PLoS One 5:e11468 Jeppesen DK, Bohr VA, Stevnsner T (2011) DNA repair deficiency in neurodegeneration. Prog Neurobiol 94:166–200 Kujoth GC, Hiona A, Pugh TD, Someya S, Panzer K, Wohlgemuth SE, Hofer T, Seo AY, Sullivan R, Jobling WA, Morrow JD, Van Remmen H, Sedivy JM, Yamasoba T, Tanokura M, Weindruch R, Leeuwenburgh C, Prolla TA (2005) Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science 309:481–484 Kujoth GC, Bradshaw PC, Haroon S, Prolla TA (2007) The role of mitochondrial DNA mutations in mammalian aging. PLoS Genet 3:e24 Kukreja L, Kujoth GC, Prolla TA, Van Leuven F, Vassar R (2014) Increased mtDNA mutations with aging promotes amyloid accumulation and brain atrophy in the APP/Ld transgenic mouse model of Alzheimer’s disease. Mol Neurodegener 9:16 Leret ML, San Millan JA, Fabre E, Gredilla R, Barja G (2002) Deprenyl protects from MPTP-induced Parkinson-like syndrome and glutathione oxidation in rat striatum. Toxicology 170:165–171 Liu C, Cui G, Zhu M, Kang X, Guo H (2014) Neuroinflammation in Alzheimer’s disease: chemokines produced by astrocytes and chemokine receptors. Int J Clin Exp Pathol 7:8342–8355 Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275 Macchi B, Paola DR, Marino-Merlo F, Felice MR, Cuzzocrea S, Mastino A (2015) Inflammatory and Cell Death Pathways in Brain and Peripheral Blood in Parkinson’s disease. CNS Neurolog Disord Drug Targets 14:313–324 Mattson MP (2004) Pathways towards and away from Alzheimer’s disease. Nature 430:631–639 Melov S (2004) Modeling mitochondrial function in aging neurons. Trends Neurosci 27:601–606 Menardo J, Tang Y, Ladrech S, Lenoir M, Casas F, Michel C, Bourien J, Ruel J, Rebillard G, Maurice T, Puel JL, Wang J (2012) Oxidative stress, inflammation, and autophagic stress as the key mechanisms of premature age-related hearing loss in SAMP8 mouse Cochlea. Antioxid Redox Signal 16:263–274 Mitra S, Izumi T, Boldogh I, Bhakat KK, Chattopadhyay R, Szczesny B (2007) Intracellular trafficking and regulation of mammalian AP-endonuclease 1 (APE1), an essential DNA repair protein. DNA Repair (Amst) 6:461–469 Oddo S, Caccamo A, Kitazawa M, Tseng BP, LaFerla FM (2003) Amyloid deposition precedes tangle formation in a triple transgenic model of Alzheimer’s disease. Neurobiol Aging 24:1063–1070 Plesnila N, Zhu C, Culmsee C, Groger M, Moskowitz MA, Blomgren K (2004) Nuclear translocation of apoptosis-inducing factor after focal cerebral ischemia. J Cereb Blood Flow Metab 24:458–466 Riancho JA, Zarrabeitia MT, Amado JA, Olmos JM, Gonzalez-Macias J (1994) Age-related differences in cytokine secretion. Gerontology 40:8–12 Rousseaux MW, Marcogliese PC, Qu D, Hewitt SJ, Seang S, Kim RH, Slack RS, Schlossmacher MG, Lagace DC, Mak TW, Park DS (2012) Progressive dopaminergic cell loss with unilateral-to-bilateral progression in a genetic model of Parkinson disease. Proc Natl Acad Sci U S A 109:15918–15923 Sanders LH, McCoy J, Hu X, Mastroberardino PG, Dickinson BC, Chang CJ, Chu CT, Van Houten B, Greenamyre JT (2014) Mitochondrial DNA damage: molecular marker of vulnerable nigral neurons in Parkinson’s disease. Neurobiol Dis 70:214–223 Sato E, Oda N, Ozaki N, Hashimoto S, Kurokawa T, Ishibashi S (1996) Early and transient increase in oxidative stress in the cerebral cortex of senescence-accelerated mouse. Mech Ageing Dev 86:105–114 Siddiqui A, Rivera-Sanchez S, Castro Mdel R, Acevedo-Torres K, Rane A, Torres-Ramos CA, Nicholls DG, Andersen JK, Ayala-Torres S (2012) Mitochondrial DNA damage is associated with reduced mitochondrial bioenergetics in Huntington’s disease. Free Radic Biol Med 53:1478–1488 Takeda T (2009) Senescence-accelerated mouse (SAM) with special references to neurodegeneration models, SAMP8 and SAMP10 mice. Neurochem Res 34:639–659 Takeda T, Hosokawa M, Takeshita S, Irino M, Higuchi K, Matsushita T, Tomita Y, Yasuhira K, Hamamoto H, Shimizu K, Ishii M, Yamamuro T (1981) A new murine model of accelerated senescence. Mech Ageing Dev 17:183–194 Takemura M, Nakamura S, Akiguchi I, Ueno M, Oka N, Ishikawa S, Shimada A, Kimura J, Takeda T (1993) Beta/A4 proteinlike immunoreactive granular structures in the brain of senescence-accelerated mouse. Am J Pathol 142:1887–1897 Tha KK, Okuma Y, Miyazaki H, Murayama T, Uehara T, Hatakeyama R, Hayashi Y, Nomura Y (2000) Changes in expressions of proinflammatory cytokines IL-1beta, TNF-alpha and IL-6 in the brain of senescence accelerated mouse (SAM) P8. Brain Res 885:25–31 Tian F, Tong TJ, Zhang ZY, McNutt MA, Liu XW (2009) Age-dependent down-regulation of mitochondrial 8-oxoguanine DNA glycosylase in SAM-P/8 mouse brain and its effect on brain aging. Rejuvenation Res 12:209–215 Vermulst M, Bielas JH, Kujoth GC, Ladiges WC, Rabinovitch PS, Prolla TA, Loeb LA (2007) Mitochondrial point mutations do not limit the natural lifespan of mice. Nat Genet 39:540–543 Wanagat J, Cao Z, Pathare P, Aiken JM (2001) Mitochondrial DNA deletion mutations colocalize with segmental electron transport system abnormalities, muscle fiber atrophy, fiber splitting, and oxidative damage in sarcopenia. FASEB J 15:322–332 Weissman L, de Souza-Pinto NC, Stevnsner T, Bohr VA (2007a) DNA repair, mitochondria, and neurodegeneration. Neuroscience 145:1318–1329 Weissman L, Jo DG, Sorensen MM, de Souza-Pinto NC, Markesbery WR, Mattson MP, Bohr VA (2007b) Defective DNA base excision repair in brain from individuals with Alzheimer’s disease and amnestic mild cognitive impairment. Nucleic Acids Res 35:5545–5555 Yang JL, Tadokoro T, Keijzers G, Mattson MP, Bohr VA (2010) Neurons efficiently repair glutamate-induced oxidative DNA damage by a process involving CREB-mediated up-regulation of apurinic endonuclease 1. J Biol Chem 285:28191–28199 Yang JL, Lin YT, Chuang PC, Bohr VA, Mattson MP (2014) BDNF and exercise enhance neuronal DNA repair by stimulating CREB-mediated production of apurinic/apyrimidinic endonuclease 1. Neuromol Med 16:161–174 Zhu Y, Lee CC, Lam WP, Wai MS, Rudd JA, Yew DT (2007) Cell death in the Purkinje cells of the cerebellum of senescence accelerated mouse (SAMP(8)). Biogerontology 8:537–544