Neurons from senescence-accelerated SAMP8 mice are protected against frailty by the sirtuin 1 promoting agents melatonin and resveratrol

Journal of Pineal Research

Volumn 52, Issue 3, 2012, Pages 271-281

  Cristòfol, Rosa ^a   Porquet, David ^b   Corpas, Rubén ^a   Coto Montes, Ana ^c   Serret, Jofre ^a   Camins, Antoni ^b   Pallàs, Mercè ^b   Sanfeliu, Coral ^a  

^a INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

^c UNIVERSIDAD DE OVIEDO   (Spain)

Author keywords

aging brain; melatonin; mitochondria; resveratrol; SAMP8 mouse neuron cultures; sirtuin 1

Indexed keywords

BUTHIONINE SULFOXIMINE; MELATONIN; RESVERATROL; SIRTINOL; SIRTUIN 1;

AGING; ANIMAL EXPERIMENT; ARTICLE; BRAIN DAMAGE; BRAIN NERVE CELL; CONTROLLED STUDY; EMBRYO; LONGEVITY; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MOUSE; NERVE CELL CULTURE; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; SENESCENCE ACCELERATED MOUSE;

ANIMALS; CELLS, CULTURED; MELATONIN; MEMBRANE POTENTIALS; MICE; NEURONS; REACTIVE OXYGEN SPECIES; SIRTUIN 1; STILBENES;

EID: 84858749951     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/j.1600-079X.2011.00939.x     Document Type: Article

References (80)

1. Bishop NA, Lu T, Yankner BA,. Neural mechanisms of ageing and cognitive decline. Nature 2010; 464: 529-535.
2. Pakkenberg B, Pelvig D, Marner L, et al., Aging and the human neocortex. Exp Gerontol 2003; 38: 95-99. (Pubitemid 36110503)
3. Castellani RJ, Lee HG, Zhu X, et al., Alzheimer disease pathology as a host response. J Neuropathol Exp Neurol 2008; 67: 523-531. (Pubitemid 351787079)
4. García-Matas S, De Vera N, Ortega-Aznar A, et al., In vitro and in vivo activation of astrocytes by amyloid β is potentiated by pro-oxidant agents. J Alzheimers Dis 2010; 20: 229-245.
5. Harman D,. Aging: a theory based on free radical and radiation chemistry. J Gerontol 1956; 1: 298-300.
6. Miquel J, Economos AC, Fleming J, Johnson Je JR,. Mitochondrial role in cell aging. Exp Gerontol 1980; 15: 575-591. (Pubitemid 11243249)
7. Viña J, Borrás C, Miquel J,. Theories of ageing. IUBMB Life 2007; 59: 249-254. (Pubitemid 46763767)
8. Navarro A, Boveris A,. The mitochondrial energy transduction system and the aging process. Am J Physiol Cell Physiol 2007; 292: C670-C686.
9. Middleton LE, Yaffe K,. Targets for the prevention of dementia. J. Alzheimers Dis 2010; 20: 915-924.
10. Smith DL Jr, Nagy TR, Allison DB,. Calorie restriction: what recent results suggest for the future of ageing research. Eur J Clin Invest 2010; 40: 440-450.
11. García-Mesa Y, López-Ramos JC, Giménez-Llort L, et al., Physical exercise protects against Alzheimer's disease in 3xTg-AD mice. J Alzheimers Dis 2011; 24: 421-454.
12. Michán S, Li Y, Chou MM, et al., SIRT1 is essential for normal cognitive function and synaptic plasticity. J Neurosci 2010; 30: 9695-9707.
13. Imai S, Armstrong CM, Kaeberlein M, Guarente L,. Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature 2000; 403: 795-800. (Pubitemid 30111843)
14. Bonda DJ, Lee H-G, Camins A, et al., The sirtuin pathway in ageing and Alzheimer disease: mechanistic and therapeutic considerations. Lancet Neurol 2011; 10: 275-279.
15. Allard JS, Perez E, Zou S, De Cabo R,. Dietary activators of Sirt1. Mol Cell Endocrinol 2009; 299: 58-63.
16. Tajes M, Gutierrez-Cuesta J, Ortuño-Sahagun D, et al., Anti-aging properties of melatonin in an in vitro murine senescence model: involvement of the sirtuin 1 pathway. J Pineal Res 2009; 47: 228-237.
17. Miller RA, Williams JB, Kiklevich JV, et al., Comparative cellular biogerontology: primer and prospectus. Ageing Res Rev 2011; 10: 181-190.
18. Pertusa M, García-Matas S, Rodríguez-Farré E, et al., Astocytes aged in vitro show a decreased neuroprotective capacity. J Neurochem 2007; 101: 794-805. (Pubitemid 46633314)
19. García-Matas S, Gutierrez-Cuesta J, Coto-Montes A, et al., Dysfunction of astrocytes in senescence-accelerated mice SAMP8 reduces their neuroprotective capacity. Aging Cell 2008; 7: 630-640.
20. Díez-Vives C, Gay M, García-Matas S, et al., Proteomic study of neuron and astrocyte cultures from senescence-accelerated mouse SAMP8 reveals degenerative changes. J Neurochem 2009; 111: 945-955.
21. Takeda T, Matsushita T, Kurozumi M, et al., Senescence-accelerated mouse (SAM): a biogerontological resource in aging research. Neurobiol Aging 1999; 20: 105-110. (Pubitemid 29488720)
22. Takeda T,. Senescence-accelerated mouse (SAM) with special references to neurodegeneration models, SAMP8 and SAMP10 mice. Neurochem Res 2009; 34: 639-659.
23. Morrison JH, Hof PR,. Life and death of neurons in the aging brain. Science 1997; 278: 412-419. (Pubitemid 27454417)
24. Galvin JE, Ginsberg SD,. Expression profiling in the aging brain: a perspective. Ageing Res Rev 2003; 4: 529-547.
25. Butterfield DA, Poon HF,. 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 2005; 40: 774-783. (Pubitemid 41416540)
26. Hardeland R, Cardinali DP, Srinivasan V, et al., Melatonin - a pleiotropic, orchestrating regulator molecule. Prog Neurobiol 2011; 93: 350-384.
27. Ungvarin Z, Sonntag WE, De Cabo R, et al., Mitochondrial protection by resveratrol. Exerc Sport Sci Rev 2011; 39: 128-312.
28. Solà C, Cristòfol R, Suñol C, Sanfeliu C,. Primary cultures for neurotoxicity testing. In: Cell Culture Techniques, Series: Neuromethods, Vol. 56, Aschner M, Suñol C, Bal-Price A, eds., Humana Press, New York, 2011; pp. 87-103.
29. Alvarez-García O, Vega-Naredo I, Sierra V, et al., Elevated oxidative stress in the brain of senescence-accelerated mice at 5 months of age. Biogerontology 2006; 7: 43-52. (Pubitemid 44026971)
30. Johnson LV, Walsh ML, Bockus BJ, Chen LB,. Monitoring of relative mitochondrial membrane potential. J Cell Biol 1981; 88: 526-535.
31. Kahlert S, Zündorf G, Reiser G,. Detection of de- and hyperpolarization of mitochondria of cultured astrocytes and neurons by the cationic fluorescent dye rhodamine 123. J Neurosci Methods 2008; 171: 87-92.
32. Kirkland JL, Peterson C,. Healthspan, translation, and new outcomes for animal studies of aging. J Gerontol A Biol Sci Med Sci 2009; 64A: 209-212.
33. Miyamoto M, Kiyota Y, Yamazaki N, et al., Age-related changes in learning and memory in the senescence-accelerated mouse (SAM). Physiol Behav 1986; 38: 399-406. (Pubitemid 17173894)
34. Miyamoto M,. Characteristics of age-related behavioral changes in senescence-accelerated mouse SAMP8 and SAMP10. Exp Gerontol 1997; 32: 139-148. (Pubitemid 27131713)
35. López-Ramos JC, Jurado-Parras MT, Sanfeliu C, et al., Learning capabilities and CA1-prefrontal synaptic plasticity in a mice model of accelerated senescence. Neurobiol Aging 2011. doi:.
36. Keuker JI, Luiten PG, Fuchs E,. Preservation of hippocampal neuron numbers in aged rhesus monkeys. Neurobiol Aging 2003; 24: 157-165. (Pubitemid 35454152)
37. Kawamata T, Akiguchi I, Yagi H, et al., Neuropathological studies on strains of senescence-accelerated mice (SAM) with age-related deficits in learning and memory. Exp Gerontol 1997; 32: 161-169. (Pubitemid 27131715)
38. Wang F, Chen H, Sun X,. Age-related spatial cognitive impairment is correlated with a decrease in ChAT in the cerebral cortex, hippocampus and forebrain of SAMP8 mice. Neurosci Lett 2009; 454: 212-217.
39. Wu Y, Zhang AQ, Wai MS, et al., Changes of apoptosis-related proteins in hippocampus of SAM mouse in development and aging. Neurobiol Aging 2006; 27: 782.e1-782.e10.
40. Caballero B, Vega-Naredo I, Sierra V, et al., Melatonin alters cell death processes in response to age-related oxidative stress in the brain of senescence-accelerated mice. J Pineal Res 2009; 46: 106-114.
41. Kawamata T, Akiguchi I, Maeda K, et al., Age-related changes in the brains of senescence-accelerated mice (SAM): association with glial and endothelial reactions. Microsc Res Tech 1998; 43: 59-67. (Pubitemid 28507014)
42. Canudas AM, Gutierrez-Cuesta J, Rodríguez MI, et al., Hyperphosphorylation of microtubule-associated protein tau in senescence-accelerated mouse (SAM). Mech Ageing Dev 2005; 126: 1300-1304. (Pubitemid 41572247)
43. Del Valle J, Duran-Vilaregut J, Manich G, et al., Early amyloid accumulation in the hippocampus of SAMP8 mice. J. Alzheimers Dis 2010; 19: 1303-1315.
44. Pallàs M, Camins A, Smith MA, et al., From aging to Alzheimer's disease: unveiling "the switch" with the senescence-accelerated mouse model (SAMP8). J Alzheimers Dis 2008; 15: 615-624.
45. Dong W, Cheng S, Huang F, et al., Mitochondrial dysfunction in long-term neuronal cultures mimics changes with aging. Med Sci Monit 2011; 17: BR91-BR96.
46. Toescu EC, Verkhratsky A,. Neuronal ageing in long-term cultures: alterations of Ca2+ homeostasis. Neuroreport 2000; 11: 3725-3729.
47. Aksenova MV, Aksenov MY, Markesbery WR, Butterfield DA,. Aging in a dish: age-dependent changes of neuronal survival, protein oxidation, and creatine kinase BB expression in long-term hippocampal cell culture. J Neurosci Res 1999; 58: 308-317. (Pubitemid 29471432)
48. Bertrand SJ, Aksenova MV, Aksenov MY, et al., Endogenous amyloidogenesis in long-term rat hippocampal cell cultures. BMC Neurosci 2011; 12: 38.
49. Xu J, Shi C, Qi Li Q, et al., Mitochondrial dysfunction in platelets and hippocampi of senescence-accelerated mice. J Bioenerg Biomembr 2007; 39: 195-202. (Pubitemid 46870549)
50. Fujibayashi Y, Yamamoto S, Waki A, et al., Increased mitochondrial DNA deletion in the brain of SAMP8, a mouse model for spontaneous oxidative stress brain. Neurosci Lett 1998; 254: 109-112. (Pubitemid 28454844)
51. Okatani Y, Wakatsuki A, Reiter RJ,. Melatonin protects hepatic mitochondrial respiratory chain activity in senescence-accelerated mice. J Pineal Res 2002; 32: 143-148. (Pubitemid 34309880)
52. Rodríguez MI, Carretero M, Escames G, et al., Chronic melatonin treatment prevents age-dependent cardiac mitochondrial dysfunction in senescence-accelerated mice. Free Radic Res 2007; 41: 15-24. (Pubitemid 44896871)
53. Nakahara H, Kanno T, Inai Y, et al., Mitochondrial dysfunction in the senescence accelerated mouse (SAM). Free Radic Biol Med 1998; 24: 85-92. (Pubitemid 28006439)
54. Kurokawa T, Asada S, Nishitani S, Hazeki O,. Age-related changes in manganese superoxide dismutase activity in the cerebral cortex of senescence-accelerated prone and resistant mouse. Neurosci Lett 2001; 298: 135-138. (Pubitemid 32037073)
55. Sureda FX, Gutierrez-Cuesta J, Romeu M, et al., Changes in oxidative stress parameters and neurodegeneration markers in the brain of the senescence-accelerated mice SAMP-8. Exp Gerontol 2006; 41: 360-367.
56. Okatani Y, Wakatsuki A, Reiter RJ, Miyahara Y,. Melatonin reduces oxidative damage of neural lipids and proteins in senescence-accelerated mouse. Neurobiol Aging 2002; 23: 639-644. (Pubitemid 34493894)
57. Rodriguez MI, Escames G, López LC, et al., Melatonin administration prevents cardiac and diaphragmatic mitochondrial oxidative damage in senescence-accelerated mice. J Endocrinol 2007; 194: 637-643. (Pubitemid 47471232)
58. García-Macia M, Vega-Naredo I, De Gonzalo-Calvo D, et al., Melatonin induces neural SOD2 expression independent of the NF-kappaB pathway and improves the mitochondrial population and function in old mice. J Pineal Res 2011; 50: 54-63.
59. Reiter RJ, Tan DX, Fuentes-Broto L,. Melatonin: a multitasking molecule. Prog Brain Res 2010; 181: 127-151.
60. Reiter RJ, Richardson BA, Johnson LY, et al., Pineal melatonin rhythm: reduction in aging Syrian hamsters. Science 1980; 210: 1372-1373. (Pubitemid 11175499)
61. Reiter RJ, Craft CM, Johnson JE Jr, et al., Age-associated reduction in nocturnal pineal melatonin levels in female rats. Endocrinology 1981; 109: 1295-1297. (Pubitemid 11008322)
62. Sack RL, Lewy AJ, Erb DL, et al., Human melatonin production decreases with age. J Pineal Res 1986; 3: 379-388. (Pubitemid 17184633)
63. Carretero M, Escames G, López LC, et al., Long-term melatonin administration protects brain mitochondria from aging. J Pineal Res 2009; 47: 192-200.
64. Okatani Y, Wakatsuki A, Reiter RJ, Miyahara Y,. Hepatic mitochondrial dysfunction in senescence-accelerated mice: correction by long-term, orally administered physiological levels of melatonin. J Pineal Res 2002; 33: 127-133.
65. Rodríguez MI, Escames G, López LC, et al., Improved mitochondrial function and increased life span after chronic melatonin treatment in senescent prone mice. Exp Gerontol 2008; 43: 749-756.
66. Galano A, Tan DX, Reiter RJ,. Melatonin as a natural ally against oxidative stress: a physicochemical examination. J Pineal Res 2011; 51: 1-16.
67. Acuña Castroviejo D, López LC, Escames G, et al., Melatonin-mitochondria interplay in health and disease. Curr Top Med Chem 2011; 11: 221-240.
68. Jou MJ, Peng TI, Reiter RJ, et al., Visualization of the antioxidative effects of melatonin at the mitochondrial level during oxidative stress-induced apoptosis of rat brain astrocytes. J Pineal Res 2004; 37: 55-70. (Pubitemid 38969021)
69. Jou MJ, Peng TI, Hsu LF, et al., Visualization of melatonin's multiple mitochondrial levels of protection against mitochondrial Ca(2+)-mediated permeability transition and beyond in rat brain astrocytes. J Pineal Res 2010; 48: 20-38.
70. Paradies G, Petrosillo G, Paradies V, et al., Melatonin, cardiolipin and mitochondrial bioenergetics in health and disease. J Pineal Res 2010; 48: 297-310.
71. Milczarek R, Hallmann A, Sokołowska E, et al., Melatonin enhances antioxidant action of alpha-tocopherol and ascorbate against NADPH- and iron-dependent lipid peroxidation in human placental mitochondria. J Pineal Res 2010; 49: 149-155.
72. Nogués MR, Giralt M, Romeu M, et al., Melatonin reduces oxidative stress in erythrocytes and plasma of senescence-accelerated mice. J Pineal Res 2006; 41: 142-149. (Pubitemid 44141749)
73. Cuesta S, Kireev R, Forman K, et al., Melatonin improves inflammation processes in liver of senescence-accelerated prone male mice (SAMP8). Exp Gerontol 2010; 45: 950-956.
74. Gutierrez-Cuesta J, Tajes M, Jiménez A, et al., Evaluation of potential pro-survival pathways regulated by melatonin in a murine senescence model. J Pineal Res 2008; 45: 497-505.
75. Dragicevic N, Copes N, O'neal-Moffitt G, et al., Melatonin treatment restores mitochondrial function in Alzheimer's mice: a mitochondrial protective role of melatonin membrane receptor signaling. J Pineal Res 2011; 51: 75-86.
76. Camins A, Pelegrí C, Vilaplana J, et al., Sirtuins and Resveratrol. In: Micronutrients and Brain Heatlh, Packer L, Sies H, Eggersdorfer M, et al. eds., CRC Press, Boca Raton, 2009; pp. 329-340.
77. Pearson KJ, Baur JA, Lewis KN, et al., Resveratrol delays age-related deterioration and mimics transcriptional aspects of dietary restriction without extending life span. Cell Metab 2008; 8: 157-168.
78. Wong YT, Gruber J, Jenner AM, et al., Chronic resveratrol intake reverses pro-inflammatory cytokine profile and oxidative DNA damage in ageing hybrid mice. Age (Dordr), 2010; 33: 229-246.
79. Ota H, Tokunaga E, Chang K, et al., Sirt1 inhibitor, Sirtinol, induces senescence-like growth arrest with attenuated Ras-MAPK signaling in human cancer cells. Oncogene 2006; 25: 176-185. (Pubitemid 43083679)
80. Pallàs M, Verdaguer E, Tajes M, Gutierrez-Cuesta J, Camins A,. Modulation of sirtuins: new targets for antiageing. Rec Pat CNS Drug Discov 2008; 3: 61-69. (Pubitemid 351223186)