Effect of estrogens on base excision repair in brain and liver mitochondria of aged female rats

Biogerontology

Volumn 14, Issue 4, 2013, Pages 383-394

  Leclere R ^a   Torregrosa Munumer R ^a   Kireev, R ^a   Garcia C ^b   Vara, E ^b   Tresguerres, J A F ^a   Gredilla, R ^a  

^a SCHOOL OF MEDICINE   (Spain)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

Aging; AP endonuclease; Base excision repair; DNA; Estrogens; Mitochondria

Indexed keywords

DNA (APURINIC OR APYRIMIDINIC SITE) LYASE; ESTROGEN;

AGED; ARTICLE; BRAIN MITOCHONDRION; CONTROLLED STUDY; CYTOSOL; DEAMINATION; DEPLETION; DRUG EFFECT; ENZYME ACTIVITY; ENZYME LOCALIZATION; ESTROGEN BLOOD LEVEL; EXCISION REPAIR; FEMALE; HOMEOSTASIS; LIVER MITOCHONDRION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT;

EID: 84882244994     PISSN: 13895729     EISSN: 15736768     Source Type: Journal    
DOI: 10.1007/s10522-013-9431-x     Document Type: Article

References (66)

1. Alvarez-Delgado C, Mendoza-Rodríguez CA, Picazo O, Cerbón M (2010) Different expression of alpha and beta mitochondrial estrogen receptors in the aging rat brain: interaction with respiratory complex V. Exp Gerontol 45:580-585
2. Araneda S, Pelloux S, Radicella JP, Angulo J, Kitahama K, Gysling K, Forray MI (2005) 8-oxoguanine DNA glycosylase, but not Kin17 protein, is translocated and differentially regulated by estrogens in rat brain cells. Neuroscience 136:135-146
3. Araújo GW, Beyer C, Arnold S (2008) Oestrogen influences on mitochondrial gene expression and respiratory chain activity in cortical and mesencephalic astrocytes. J Neuroendocrinol 20:930-941
4. Arnold S, Beyer C (2009) Neuroprotection by estrogen in the brain: the mitochondrial compartment as presumed therapeutic target. J Neurochem 110:1-11
5. Arnold S, de Araújo GW, Beyer C (2008) Gender-specific regulation of mitochondrial fusion and fission gene transcription and viability of cortical astrocytes by steroid hormones. J Mol Endocrinol 41:289-300
6. Arnold S, Victor MB, Beyer C (2012) Estrogen and the regulation of mitochondrial structure and function in the brain. J Steroid Biochem Mol Biol 131:2-9
7. Azcoitia I, Perez-Martin M, Salazar V, Castillo C, Ariznavarreta C, Garcia-Segura LM, Tresguerres JAF (2005) Growth hormone prevents neuronal loss in the aged rat hippocampus. Neurobiol Aging 26:697-703
8. Baeza I, Fdez-Tresguerres J, Ariznavarreta C, De la Fuente M (2010) Effects of growth hormone, melatonin, oestrogens and phytoestrogens on the oxidized glutathione (GSSG)/reduced glutathione (GSH) ratio and lipid peroxidation in aged ovariectomized rats. Biogerontology 11:687-701
9. Bartke A, Wright JC, Mattison JA, Ingram DK, Miller RA, Roth GS (2001) Extending the lifespan of long-lived mice. Nature 414:412
10. Boesch P, Weber-Lotfi F, Ibrahim N, Tarasenko V, Cosset A, Paulus F, Lightowlers RN, Dietrich A (2011) DNA repair in organelles: pathways, organization, regulation, relevance in disease and aging. Biochim Biophys Acta 1813:186-200
11. Bohr VA (2002) Repair of oxidative DNA damage in nuclear and mitochondrial DNA, and some changes with aging in mammalian cells. Free Radic Biol Med 32:804-812
12. Bohr VA, Anson RM (1999) Mitochondrial DNA repair pathways. J Bioenerg Biomembr 31:391-398
13. Borrás C, Sastre J, García-Sala D, Lloret A, Pallardó FV, Viña J (2003) Mitochondria from females exhibit higher antioxidant gene expression and lower oxidative damage than males. Free Radic Biol Med 34:546-552
14. Brown MR, Geddes JW, Sullivan PG (2004) Brain region-specific, age-related, alterations in mitochondrial responses to elevated calcium. J Bioenerg Biomembr 36:401-406
15. Busso CS, Lake MW, Izumi T (2010) Posttranslational modification of mammalian AP endonuclease (APE1). Cell Mol Life Sci 67:3609-3620
16. Caro P, Gómez J, Sanz A, Portero-Otín M, Pamplona R, Barja G (2007) Effect of graded corticosterone treatment on aging-related markers of oxidative stress in rat liver mitochondria. Biogerontology 8:1-11
17. Castillo C, Salazar V, Ariznavarreta C, Vara E, Tresguerres JA (2005) Effect of growth hormone and estrogen administration on hepatocyte alterations in old ovariectomized female wistar rats. Endocrine 26:11-18
18. Castro MR, Suarez E, Kraiselburd E, Isidro A, Paz J, Ferder L, Ayala-Torres S (2012) Aging increases mitochondrial DNA damage and oxidative stress in liver of rhesus monkeys. Exp Gerontol 47:29-37
19. Chen D, Cao G, Hastings T, Feng Y, Pei W, O'Horo C, Chen J (2002) Age-dependent decline of DNA repair activity for oxidative lesions in rat brain mitochondria. J Neurochem 81:1273-1284
20. Cline SD (2012) Mitochondrial DNA damage and its consequences for mitochondrial gene expression. Biochim Biophys Acta 1819:979-991
21. Coskun PE, Beal MF, Wallace DC (2004) Alzheimer's brains harbor somatic mtDNA control-region mutations that suppress mitochondrial transcription and replication. Proc Natl Acad Sci USA 101:10726-10731
22. Dickstein DL, Kabaso D, Rocher AB, Luebke JI, Wearne SL, Hof PR (2007) Changes in the structural complexity of the aged brain. Aging Cell 6:275-284
23. Dröge W, Schipper HM (2007) Oxidative stress and aberrant signaling in aging and cognitive decline. Aging Cell 6:361-370
24. el-Serag HB (2001) Epidemiology of hepatocellular carcinoma. Clin Liver Dis 5:87-107
25. Fantini D, Vascotto C, Marasco D, D'Ambrosio C, Romanello M, Vitagliano L, Pedone C, Poletto M, Cesaratto L, Quadrifoglio F, Scaloni A, Radicella JP, Tell G (2010) Critical lysine residues within the overlooked N-terminal domain of human APE1 regulate its biological functions. Nucleic Acids Res 38:8239-8256
26. Foster TC (2007) Calcium homeostasis and modulation of synaptic plasticity in the aged brain. Aging Cell 6:319-325
27. Furda AM, Marrangoni AM, Lokshin A, Van Houten B (2012) Oxidants and not alkylating agents induce rapid mtDNA loss and mitochondrial dysfunction. DNA Repair 11:684-692
28. Garcia-Segura LM, Balthazart J (2009) Steroids and neuroprotection: new advances. Front Neuroendocrinol 30(2):v-ix
29. Garcia-Segura LM, Diz-Chaves Y, Perez-Martin M, Darnaudéry M (2007) Estradiol, insulin-like growth factor-I and brain aging. Psychoneuroendocrinology 32:S57-S61
30. Gredilla R (2010) DNA damage and base excision repair in mitochondria and their role in aging. J Aging Res. doi: 10.4061/2011/257093
31. Gredilla R, Stevnsner T (2012) Mitochondrial base excision repair assays. Methods Mol Biol 920:289-304
32. Gredilla R, Bohr VA, Stevnsner T (2010a) Mitochondrial DNA repair and association with aging - an update. Exp Gerontol 45:478-488
33. Gredilla R, Garm C, Holm R, Bohr VA, Stevnsner T (2010b) Differential age-related changes in mitochondrial DNA repair activities in mouse brain regions. Neurobiol Aging 31:993-1002
34. 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
35. Hegde ML, Mantha AK, Hazra TK, Bhakat KK, Mitra S, Szczesny B (2012) Oxidative genome damage and its repair: implications in aging and neurodegenerative diseases. Mech Ageing Dev 133:157-168
36. Hota SK, Barhwal K, Singh SB, Ilavazhagan G (2007) Differential temporal response of hippocampus, cortex and cerebellum to hypobaric hypoxia: a biochemical approach. Neurochem Int 51:384-390
37. Imam SZ, Karahalil B, Hogue BA, Souza-Pinto NC, Bohr VA (2006) Mitochondrial and nuclear DNA-repair capacity of various brain regions in mouse is altered in an age-dependent manner. Neurobiol Aging 27:1129-1136
38. Jang YM, Kendaiah S, Drew B, Phillips T, Selman C, Julian D, Leeuwenburgh C (2004) Doxorubicin treatment in vivo activates caspase-12 mediated cardiac apoptosis in both male and female rats. FEBS Lett 577:483-490
39. Jeppesen DK, Bohr VA, Stevnsner T (2011) DNA repair deficiency in neurodegeneration. Prog Neurobiol 94:166-200
40. Julian D, Leeuwenburgh C (2004) Linkage between insulin and the free radical theory of aging. Am J Physiol Regul Integr Comp Physiol 286:R20-R21
41. Kireev RA, Tresguerres ACF, Castillo C, Salazar V, Ariznavarreta C, Vara E, Tresguerres JAF (2007a) Effect of exogenous administration of melatonin and growth hormone on pro-antioxidant functions of the liver in aging male rats. J Pineal Res 42:64-70
42. Kireev RA, Tresguerres AF, Vara E, Ariznavarreta C, Tresguerres JAF (2007b) Effect of chronic treatments with GH, melatonin, estrogens, and phytoestrogens on oxidative stress parameters in liver from aged female rats. Biogerontology 8:469-482
43. Kireev RA, Tresguerres ACF, Garcia C, Borras C, Ariznavarreta C, Vara E, Vina J, Tresguerres JAF (2010) Hormonal regulation of pro-inflammatory and lipid peroxidation processes in liver of old ovariectomized female rats. Biogerontology 11:229-243
44. Klinge CM (2008) Estrogenic control of mitochondrial function and biogenesis. J Cell Biochem 105:1342-1351
45. Li M, Zhong Z, Zhu J, Xiang D, Dai N, Cao X, Qing Y, Yang Z, Xie J, Li Z, Baugh L, Wang G, Wang D (2010) Identification and characterization of mitochondrial targeting sequence of human apurinic/apyrimidinic endonuclease 1. J Biol Chem 285:14871-14881
46. Li M-X, Shan J-L, Wang D, He Y, Zhou Q, Xia L, Zeng L-L, Li Z-P, Wang G, Yang Z-Z (2012) Human AP endonuclease 1 translocalizes to mitochondria after photodynamic therapy and protects cells from apoptosis. Cancer Sci 103:882-888
47. Liu P, Demple B (2010) DNA repair in mammalian mitochondria: much more than we thought? Environ Mol Mutagen 51:417-426
48. López-Torres M, Gredilla R, Sanz A, Barja G (2002) Influence of aging and long-term caloric restriction on oxygen radical generation and oxidative DNA damage in rat liver mitochondria. Free Radic Biol Med 32:882-889
49. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265-275
50. Markesbery WR, Lovell MA (2006) DNA oxidation in Alzheimer's disease. Antioxid Redox Signal 8:2039-2045
51. Marosi K, Felszeghy K, Mehra RD, Radak Z, Nyakas C (2012) Are the neuroprotective effects of estradiol and physical exercise comparable during ageing in female rats? Biogerontol 13:413-427
52. 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
53. Mora F, Segovia G, del Arco A (2007) Aging, plasticity and environmental enrichment: structural changes and neurotransmitter dynamics in several areas of the brain. Brain Res Rev 55:78-88
54. Nakabeppu Y, Tsuchimoto D, Yamaguchi H, Sakumi K (2007) Oxidative damage in nucleic acids and Parkinson's disease. J Neurosci Res 85:919-934
55. Persky AM, Green PS, Stubley L, Howell CO, Zaulyanov L, Brazeau GA, Simpkins JW (2000) Protective effect of estrogens against oxidative damage to heart and skeletal muscle in vivo and in vitro. Proc Soc Exp Biol Med 223:59-66
56. Poynard T, Ratziu V, Charlotte F, Goodman Z, McHutchison J, Albrecht J (2001) Rates and risk factors of liver fibrosis progression in patients with chronic hepatitis c. J Hepatol 34:730-739
57. Qiu G, Spangler EL, Wan R, Miller M, Mattson MP, So KF, Cabo R, de Zou S, Ingram DK (2012) Neuroprotection provided by dietary restriction in rats is further enhanced by reducing glucocortocoids. Neurobiol Aging 33:2398-2410
58. Robertson AB, Klungland A, Rognes T, Leiros I (2009) DNA repair in mammalian cells: base excision repair: the long and short of it. Cell Mol Life Sci 66:981-993
59. Smigrodzki R, Parks J, Parker WD (2004) High frequency of mitochondrial complex I mutations in Parkinson's disease and aging. Neurobiol Aging 25:1273-1281
60. Soerensen M, Dato S, Tan Q, Thinggaard M, Kleindorp R, Beekman M, Jacobsen R, Suchiman HED, de Craen AJM, Westendorp RGJ, Schreiber S, Stevnsner T, Bohr VA, Slagboom PE, Nebel A, Vaupel JW, Christensen K, McGue M, Christiansen L (2012) Human longevity and variation in GH/IGF-1/insulin signaling, DNA damage signaling and repair and pro/antioxidant pathway genes: cross sectional and longitudinal studies. Exp Gerontol 47:379-387
61. Sykora P, Wilson DM III, Bohr VA (2012) Repair of persistent strand breaks in the mitochondrial genome. Mech Ageing Dev 133:169-175
62. Tresguerres JAF, Kireev R, Tresguerres AF, Borras C, Vara E, Ariznavarreta C (2008) Molecular mechanisms involved in the hormonal prevention of aging in the rat. J Steroid Biochem Mol Biol 108:318-326
63. Vascotto C, Bisetto E, Li M, Zeef LAH, D'Ambrosio C, Domenis R, Comelli M, Delneri D, Scaloni A, Altieri F, Mavelli I, Quadrifoglio F, Kelley MR, Tell G (2011) Knock-in reconstitution studies reveal an unexpected role of Cys-65 in regulating APE1/Ref-1 subcellular trafficking and function. Mol Biol Cell 22:3887-3901
64. Viña J, Borrás C, Gambini J, Sastre J, Pallardó FV (2005) Why females live longer than males: control of longevity by sex hormones. Sci Aging Knowledge Environ 2005(23):pe17
65. Viña J, Sastre J, Pallardó FV, Gambini J, Borrás C (2006) Role of mitochondrial oxidative stress to explain the different longevity between genders: protective effect of estrogens. Free Radic Res 40:1359-1365
66. Wight E, Küng CF, Moreau P, Takase H, Bersinger NA, Lüscher TF (2000) Aging, serum estradiol levels, and pregnancy differentially affect vascular reactivity of the rat uterine artery. J Soc Gynecol Investig 7:106-113