Abstract
Aging is associated with the decline of cognitive properties. This situation is magnified when neurodegenerative processes associated with aging appear in human patients. Neuronal synaptic plasticity events underlie cognitive properties in the central nervous system. Caloric restriction (CR; either a decrease in food intake or an intermittent fasting diet) can extend life span and increase disease resistance. Recent studies have shown that CR can have profound effects on brain function and vulnerability to injury and disease. Moreover, CR can stimulate the production of new neurons from stem cells (neurogenesis) and can enhance synaptic plasticity, which modulate pain sensation, enhance cognitive function, and may increase the ability of the brain to resist aging. The beneficial effects of CR appear to be the result of a cellular stress response stimulating the production of proteins that enhance neuronal plasticity and resistance to oxidative and metabolic insults; they include neurotrophic factors, neurotransmitter receptors, protein chaperones, and mitochondrial biosynthesis regulators. In this review, we will present and discuss the effect of CR in synaptic processes underlying analgesia and cognitive improvement in healthy, sick, and aging animals. We will also discuss the possible role of mitochondrial biogenesis induced by CR in regulation of neuronal synaptic plasticity.
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Burke SN, Barnes CA (2006) Neural plasticity in the aging brain. Nat Neurosci 7:30–40
Segovia G, Yagüe AG, García-Verdugo JM, Mora F (2006) Environmental enrichment promotes neurogenesis and changes the extracellular concentrations of glutamate and GABA in the hippocampus of aged rats. Brain Res Bull 70:8–14
Mora F, Segovia G, del Arco A (2007) Aging, plasticity and environmental enrichment: Structural changes and neurotransmitter dynamics in several areas of brain. Brain Res Rev 55:78–88
Mattson MP, Magnus T (2006) Aging and neuronal vulnerability. Nat Rev Neurosci 7:278–294
Small GW (2002) What we need to know about age related memory loss. BMJ 324:1502–1505
Rosenzweig EP, Barnes CA (2003) Impact of aging on hippocampal function: plasticity, network dynamics, and cognition. Progress Neurobiol 69:143–179
Melov S (2004) Modeling mitochondrial function in aging neurons. Trends Neurosci 27:601–606
Serrano F, Klann E (2004) Reactive oxygen species and synaptic plasticity in the aging hippocampus. Aging Res Rev 3:431–443
Segovia G, Porras A, Del Arco A, Mora F (2001) Glutamatergic neurotransmission in aging: a critical perspective. Mech Aging Dev 122:1–29
Froc DJ, Eadie B, Li AM, Wodtke K, Tse M, Christie BR (2003) Reduced synaptic plasticity in the lateral perforant path input to the dentate gyrus of aged C57BL/6 mice. J Neurophysiol 90:32–38
Watabe AM, O’Dell TJ (2003) Age-related changes in theta frequency stimulation-induced long-term potentiation. Neurobiol Aging 24:267–272
Randic M, Jiang MC, Cerne R (1993) Long-term potentiation and long-term depression of primary afferent neurotransmission in the rat spinal cord. J Neurosci 13:5228–5241
Sandkuhler J, Liu X (1998) Induction of long-term potentiation at spinal synapses by noxious stimulation or nerve injury. Eur J Neurosci 10:2476–2480
Ji RR, Kohno T, Moore KA, Woolf CJ (2003) Central sensibilization and LTP: do pain and memory share similar mechanism? Trend in Neurosci 26:696–705
Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31–39
Zhuo M (2005) Canadian association of neuroscience review: cellular and synaptic insights into physiological and pathological pain. EJLB-CIHR Michael Smith chair in neurosciences and mental health lecture. Can J Neurol Sci 32:27–36
Barger JL, Walford RL, Weindruch R (2003) The retardation of aging by caloric restriction: its significance in the transgenic era. Exp Gerontol 38:1343–1351
Ingram DK, Anson RM, de Cabo R, Mamczarz J, Zhu M, Mattison J, Lane MA, Roth GS (2004) Development of calorie restriction mimetics as a prolongevity strategy. Ann NY Acad Sci 1019:412–423
Roth GS, Mattison JA, Ottinger MA, Chachich ME, Lane MA, Ingram DK (2004) Aging in rhesus monkeys: relevance to human health interventions. Science 305:1423–1426
Anson RM, Guo Z, de Cabo R, Iyun T, Rios M, Hagepanos A, Ingram DK, Lane MA, Mattson MP (2003) Intermittent fasting dissociates beneficial effects of dietary restriction on glucose metabolism and neuronal resistance to injury from calorie intake. Proc Natl Acad Sci U S A 100:6216–6220
Mattson MP, Duan W, Guo Z (2003) Meal size and frequency affect neuronal plasticity and vulnerability to disease: cellular and molecular mechanisms. J Neurochem 84:417–431
Lane MA, Ingram DK, Roth GS (1999) Calorie restriction in nonhuman primates: effects on diabetes and cardiovascular disease risk. Toxicol Sci 52:41–48
Masoro EJ (2000) Caloric restriction and aging: an update. Exp Gerontol 35:299–305
Berrigan D, Perkins SN, Haines DC, Hursting SD (2002) Adult-onset calorie restriction and fasting delay spontaneous tumorigenesis in p53-deficient mice. Carcinogenesis 23:817–822
Hursting SD, Lavigne JA, Berrigan D, Perkins SN, Barrett JC (2003) Calorie restriction, aging, and cancer prevention: mechanisms of action and applicability to humans. Annu Rev Med 54:131–52
Mattson MP, Duan W, Lee J, Guo Z (2001) Suppression of brain aging and neurodegenerative disorder by dietary restriction and environmental enrichment: molecular mechanisms. Mech Aging Dev 122:757–778
de los Santos-Arteaga M, Sierra-Domínguez SA, Fontanella GH, Delgado-García JM, Carrión AM (2003) Analgesia induced by dietary restriction is mediated by the kappa-opioid system. J Neurosci 23:11120–11126
Weindruch R, Kayo T, Lee CK, Prolla TA (2002) Gene expression profiling of aging using DNA microarrays. Mech Aging Dev 123:177–193
Poon HF, Shepherd HM, Reed TT, Calabrese V, Stella AM, Pennisi G, Cai J, Pierce WM, Klein JB, Butterfield DA (2006) Proteomics analysis provides insight into caloric restriction mediated oxidation and expression of brain proteins associated with age-related impaired cellular processes: mitochondrial dysfunction, glutamate dysregulation and impaired protein synthesis. Neurobiol Aging 27:1020–1034
Walford RL, Harris SB, Gunion MW (1992) The calorically restricted low-fat nutrient-dense diet in biosphere 2 significantly lowers blood glucose, total leukocyte count, cholesterol, and blood pressure in humans. Proc Natl Acad Sci U S A 89:11533–11537
Walford RL, Mock D, Verdery R, MacCallum T (2002) Calorie restriction in biosphere 2: alterations in physiologic, hematologic, hormonal, and biochemical parameters in humans restricted for a 2-year period. J Gerontol A Biol Sci Med Sci 57:B211–B224
Verdery RB, Walford RL (1998) Changes in plasma lipids and lipoproteins in humans during a 2-year period of dietary restriction in Biosphere 2. Arch Intern Med 158:900–906
Heilbronn LK, Ravussin E (2003) Calorie restriction and aging: review of the literature and implications for studies in humans. Am J Clin Nutr 78:361–369
Daoudal G, Debanne D (2003) Long-term plasticity of intrinsic excitability: learning rules and mechanisms. Learn Mem 10:456–465
Gruart A, Muñoz MD, Delgado-García JM (2006) Involvement of the CA3–CA1 synapse in the acquisition of associative learning in behaving mice. J Neurosci 26:1077–1087
Woolf CJ, Salter MW (2000) Neuronal plasticity: increasing the gain in pain. Science 288:1765–1769
Ji RR, Woolf CJ (2001) Neuronal plasticity and signal transduction in nociceptive neurons: implications for the initiation and maintenance of pathological pain. Neurobiol Dis 8:1–10
Akil H, Meng F, Mansour A, Thompson R, Xie GX, Watson S (1996) Cloning and characterization of multiple opioid receptors. NIDA Res Monogr 161:27–140
Kieffer BL, Gaveriaux-Ruff C (2002) Exploring the opioid system by gene knockout. Prog Neurobiol 66:285–306
Cravatt BF, Lichtman AH (2004) The endogenous cannabinoid system and its role in nociceptive behavior. J Neurobiol 61:149–160
Vaccarino AL, Kastin AJ (2000) Endogenous opiates: 1999. Peptides 21:1975–2034
Ledent C, Valverde O, Cossu G, Pettitet F, Beslot JF, Bohme GA, Imperato A, Pedrazzini T, Roques BP, Vassart G, Fratta W, Parmentier M (1999) Unresponsiveness to cannabinoids and reduced addictive effects of opiates in CB1 receptor knockout mice. Science 283:401–404
Zimmer A, Valjent E, Konig M, Zimmer AM, Robledo P, Hahn H, Valverde O, Maldonado R (2001) Absence of delta-9-tetrahydrocannabinol dysphoric effects in dynorphin-deficient mice. J Neurosci 21:9499–9505
Davidson TL, McKenzie BR, Tujo CJ, Bish CK (1992) Development of tolerance to endogenous opiates activated by 24-h food deprivation. Appetite 19:1–13
Hamm RJ, Knisely JS (1986) The analgesia produced by food deprivation in 4-month old, 14-month old, and 24-month old rats. Life Sci 39:1509–1515
Jurcovicova J, Stancikova M, Svik K, Ondrejickova O, Krsova D, Seres J, Rokyta R (2001) Stress of chronic food restriction attenuates the development of adjuvant arthritis in male Long Evans rats. Clin Exp Rheumatol 19:371–376
Hargraves WA, Hentall ID (2005) Analgesic effect of dietary caloric restriction in adult mice. Pain 114:455–461
Sáez-Cassanelli JL, Fontanella GH, Delgado-García JM, Carrión AM (2007) Functional blockage of the cannabinoid receptor type 1 evokes a kappa-opiate-dependent analgesia. J Neurochem 103:2629–2636
Carrión AM, Mellström B, Luckman SM, Naranjo JR (1998) Stimulus-specific hierarchy of enhancer elements within the rat prodynorphin promoter. J Neurochem 70:914–921
Carrión AM, Link WA, Ledo F, Mellström B, Naranjo JR (1999) DREAM is a Ca2+-regulated transcriptional repressor. Nature 398:80–84
Naranjo JR, Mellström B, Achaval M, Sassone-Corsi P (1991) Molecular pathways of pain: Fos/Jun-mediated activation of the prodynorphin gene through a non-canonical AP-1 site. Neuron 6:607–617
Cole RL, Konradi C, Douglass J, Hyman SE (1995) Neuronal adaptation to amphetamine and dopamine: molecular mechanism of prodynorphin gene regulation in rat striatum. Neuron 14:813–823
Campos D, Jiménez-Díaz L, Naranjo JR, Carrión AM (2003) Ca2+-dependent prodynorphin transcriptional derepression in neuroblastoma cells is exerted through DREAM protein activity in a kinase-independent manner. Mol Cell Neurosci 22:135–145
Cheng HY, Pitcher GM, Laviolette SR, Whishaw IQ, Tong KI, Kockeritz LK, Wada T, Joza NA, Crackower M, Goncalves J, Sarosi I, Woodgett JR, Oliveira-dos-Santos AJ, Ikura M, van der Kooy D, Salter MW, Penninger JM (2002) DREAM is a critical transcriptional repressor for pain modulation. Cell 108:31–43
Costigan M, Woolf CJ (2002) No DREAM, no pain: closing the spinal gate. Cell 108:197–200
Randic M, Cheng G, Kojic L (1995) k-opioid receptor agonists modulate excitatory transmission in substantia gelatinosa of the rat spinal cord. J Neurosci 15:6809–6826
Zachariou V, Goldstein BD (1997) Dynorphin-(1–8) inhibits the release of substance P-like immunoreactivity in the spinal cord of rats following a nociceptive mechanical stimulus. Eur J Pharmacol 323:159–165
Dogrul A, Gardell LR, Ma S, Ossipov MH, Porreca F, Lai J (2002) Knock down of spinal CB1-receptor produces abnormal pain and elevates spinal dynorphin content in mice. Pain 100:203–209
Zecca L, Youdim MB, Riederer P, Connor JR, Crichton RR (2004) Iron, brain aging and neurodegenerative disorders. Nature Rev Neurosci 5:863–873
Ames BN (2004) Delaying the mitochondrial decay of aging. Ann NY Acad Sci 1019:406–411
Gray DA, Tsirigotis M, Woulfe J (2003) Ubiquitin, proteasomes, and the aging brain. Sci Aging Knowl Environ 2003:RE6
Trojanowski JQ, Mattson MP (2003) Overview of protein aggregation in single, double, and triple neurodegenerative brain amyloidoses. Neuromolecular Med 4:1–6
Kyng KJ, Bohr VA (2005) Gene expression and DNA repair in progeroid syndromes and human aging. Aging Res Rev 4:579–602
Lu T, Pan Y, Kao SY, Li C, Kohane I, Chan J, Yankner BA (2004) Gene regulation and DNA damage in the aging human brain. Nature 429:883–891
Mattson MP (2004) Pathways towards and away from Alzheimer’s disease. Nature 430:631–639
Sieradzan KA, Mann DM (2001) The selective vulnerability of nerve cells in Huntington’s disease. Neuropathol Appl Neurobiol 27:1–21
Jenner P (2003) Oxidative stress in Parkinson’s disease. Ann Neurol 53:S26–S36
Pedersen WA, Fu W, Keller JN, Markesbery WR, Appel S, Smith RG, Kasarskis E, Mattson MP (1998) Protein modification by the lipid peroxidation product 4-hydroxynonenal in the spinal cords of amyotrophic lateral sclerosis patients. Ann Neurol 44:819–824
Rakhit R, Crow JP, Lepock JR, Kondejewski LH, Cashman NR, Chakrabartty A (2004) Monomeric Cu,Zn-superoxide dismutase is a common misfolding intermediate in the oxidation models of sporadic and familial amyotrophic lateral sclerosis. J Biol Chem 279:15499–15504
Grondin R, Zhang Z, Yi A, Cass WA, Maswood N, Andersen AH, Elsberry DD, Klein MC, Gerhardt GA, Gash DM (2002) Chronic, controlled GDNF infusion promotes structural and functional recovery in advanced parkinsonian monkeys. Brain 125:2191–2201
Mattson MP, Duan W, Wan R, Guo Z (2004) Prophylactic activation of neuroprotective stress pathways by dietary restriction and behavioural manipulations. NeuroRx 1:111–116
Zuccato C, Tartari M, Crotti A, Goffredo D, Valenza M, Conti L, Cataudella T, Leavitt BR, Hayden MR, Timmusk T, Rigamonti D, Cattaneo E (2003) Huntingtin interacts with REST/NRSF to modulate the transcription of NRSE-controlled neuronal genes. Nature Genet 35:76–83
Kuhn HG, Dickinson-Anson H, Gage FH (1996) Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16:2027–2033
Heine VM, Maslam S, Joels M, Lucassen PJ (2004) Prominent decline of newborn cell proliferation, differentiation, and apoptosis in the aging dentate gyrus, in absence of an age-related hypothalamus-pituitary adrenal axis activation. Neurobiol Aging 25:361–375
Hofer SM, Berg S, Era P (2003) Evaluating the interdependence of aging-related changes in visual and auditory acuity, balance, and cognitive functioning. Psychol Aging 18:285–305
Idrobo F, Nandy K, Mostofsky DI, Blatt L, Nandy L (1987) Dietary restriction: effects on radial maze learning and lipofuscin pigment deposition in the hippocampus and frontal cortex. Arch Gerontol Geriatr 6:255–262
Ingram DK, Weindruch R, Spangler EL, Freeman JR, Walford RL (1987) Dietary restriction benefits learning and motor performance of aged mice. J Gerontol 42:78–81
Stewart J, Mitchell J, Kalant N (1989) The effects of life-long food restriction on spatial memory in young and aged Fischer 344 rats measured in the eight-arm radial and the Morris water mazes. Neurobiol Aging 10:669–675
Pitsikas N, Algeri S (1992) Deterioration of spatial and non-spatial reference and working memory in aged rats: protective effects of life-long caloric restriction. Neurobiol Aging 13:369–373
Pitsikas N, Garofalo P, Zanotti A, Algeri S (1992) Effect of lifelong hypocaloric diet on discrete memory of the senescent rat. Aging 3:147–152
Eckles KE, Dudek EM, Bickford PC, Browning MD (1997) Amelioration of age-related deficits in the stimulation of synapsin phosphorylation. Neurobiol Aging 18:213–217
Eckles-Smith K, Clayton D, Bickford P, Browning MD (2000) Caloric restriction prevents age-related deficits in LTP and in NMDA receptor expression. Brain Res Mol Brain Res 78:154–162
Lee CK, Weindruch R, Prolla TA (2000) Gene-expression profile of the aging brain in mice. Nat Genet 25:294–297
Park SK, Prolla TA (2005) Lessons learned from gene expression profile of aging and caloric restriction. Aging Res Rev 4:55–65
Rogers J, Webster S, Lue LF, Brachova L, Civin WH, Emmerling M, Shivers B, Walker D, McGeer P (1996) Inflammation and Alzheimer’s disease pathogenesis. Neurobiol Aging 17:681–686
Bruce-Keller AJ, Umberger G, McFall R, Mattson MP (1999) Food restriction reduces brain damage and improves behavioral outcome following excitotoxic and metabolic insults. Ann Neurol 45:8–15
Zhu H, Guo Q, Mattson MP (1999) Dietary restriction protects hippocampal neurons against the death-promoting action of a presenilin-1 mutation. Brain Res 842:224–229
Duan W, Mattson MP (1999) Dietary restriction and 2-deoxyglucose administration improve behavioral outcome and reduce degeneration of dopaminergic neurons in models of Parkinson’s disease. J Neurosci Res 57:195–192
Yu ZF, Mattson MP (1999) Dietary restriction and 2-deoxyglucose administration reduce focal ischemic brain damage and improve behavioral outcome: evidence for a preconditioning mechanism. J. Neurosci Res 57:830–839
Marder K, Tang MX, Alfaro B, Mejia H, Cote L, Louis E, Stern Y, Mayeux R (1999) Reduced risk of Alzheimer’s disease among individuals with low calorie intake. Neurology 59(Suppl.):S296–S297
Logroscino G, Marder K, Cote L, Tang MX, Shea S, Mayeux R (1996) Dietary lipids and antioxidants in Parkinson’s disease: a population-based, case-control study. Ann Neurol. 39:89–94
Hendrie HC, Ogunniyi A, Hall KS, Baiyewu O, Unverzagt FW, Gureje O, Gao S, Evans RM, Ogunseyinde AO, Adeyinka AO, Musick B, Hui SL (2001) Incidence of dementia and Alzheimer disease in 2 communities: Yoruba residing in Ibadan, Nigeria, and African Americans residing in Indianapolis, Indiana. J Am Med Assoc 285:739–747
Craik FIM, Salthouse TA (1992) The handbook of aging and cognition. Lawrence Erlbaum, Hillsdale
Babcock Q, Byrne T (2000) Student perceptions of methylphenidate abuse at a public liberal arts college. J Am College Health 49:143–145
Hall SS (2003) The quest for a smart pill. Sci Am 289:54–65
Gold PE, Cahill L, Wenk GL (2002) Ginkgo biloba: a cognitive enhancer? Psychol Sci Public Interest 3:2–11
Prolla TA, Mattson MP (2001) Molecular mechanisms of brain aging and neurodegenerative disorder: lessons from dietary restriction. Trend in Neurosci 24:S21–S31
Fontán-Lozano A, Sáez-Cassanelli JL, Inda MC, de los Santos-Arteaga M, Sierra-Domínguez SA, López-Lluch, G, Delgado-García JM, Carrión AM (2007) Caloric restriction increases learning consolidation and facilitates synaptic plasticity through mechanisms dependent on NR2B subunits of the NMDA receptor. J Neurosci 29:10185–10195
Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12:529–540
Sheng M, Cummings J, Roldan LA, Jan YN, Jan LY (1994) Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Nature 368:144–147
Dubey A, Forster MJ, Lal H, Sohal RS (1996) Effect of age and caloric intake on protein oxidation in different brain regions and on behavioral functions of the mouse. Arch Biochem Biophys 333:189–197
Finch CE, Morgan TE (1997) Food restriction and brain aging. In: Mattson MP, Geddes JW (eds) The aging brain (Advances in cell aging and gerontology). vol. 2. JAI, Greenwich, pp 279–297
Bordone L, Guarente L (2005) Calorie restriction, Sirt1 and metabolism: understanding longevity. Nat Rev Mol Cell Biol 6:298–305
Kann O, Kovács R (2007) Mitochondria and neuronal activity. Am J Physiol Cell Physiol 292:C641–C657
Pieczenik SR, Neustadt J (2007) Mitochondrial dysfunction and molecular pathways of disease. Exp Mol Pathol 83:84–92
Li Z, Okamoto K, Hayashi Y, Sheng M (2004) The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell 119:873–887
Duan W, Guo Z, Jiang H, Ware M, Mattson MP (2003) Reversal of behavioral and metabolic abnormalities, and insulin resistance syndrome, by dietary restriction in mice deficient in brain-derived neurotrophic factor. Endocrinology 144:2446–2453
Markham A, Cameron I, Franklin P, Spedding M (2004) BDNF increases rat brain mitochondrial respiratory coupling at complex I, but not complex II. Eur J Neurosci 20(5):1189–1196
Wiedemann FR, Siemen D, Mawrin C, Horn TF, Dietzmann K (2006) The neurotrophin receptor TrkB is colocalized to mitochondrial membranes. Int J Biochem Cell Biol 38:610–620
López-Lluch G, Hunt N, Jones B, Zhu M, Jamieson H, Hilmer S, Cascajo MV, Allard J, Ingram DK, Navas P, de Cabo R (2006) Calorie restriction induces mitochondrial biogenesis and bioenergetic efficiency. Proc Natl Acad Sci USA 103:1768–1773
Nisoli E, Tonello C, Cardile A, Cozzi V, Bracale R, Tedesco L, Falcone S, Valerio A, Cantoni O, Clementi E, Moncada S, Carruba MO (2005) Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science 310:314–317
Cowell RM, Blake KR, Russell JW (2007) Localization of the transcriptional coactivator PGC-1alpha to GABAergic neurons during maturation of the rat brain. J Comp Neurol 502:1–18
Lin J, Wu PH, Tarr PT, Lindenberg KS, St-Pierre J, Zhang CY, Mootha VK, Jäger S, Vianna CR, Reznick RM, Cui L, Manieri M, Donovan MX, Wu Z, Cooper MP, Fan MC, Rohas LM, Zavacki AM, Cinti S, Shulman GI, Lowell BB, Krainc D, Spiegelman BM (2004) Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1alpha null mice. Cell 119:121–135
Baker DJ, Betik AC, Krause DJ, Hepple RT (2006) No decline in skeletal muscle oxidative capacity with aging in long-term calorically restricted rats: effects are independent of mitochondrial DNA integrity. J Gerontol A Biol Sci Med Sci 61:675–684
Hepple RT, Baker DJ, McConkey M, Murynka T, Norris R (2006) Caloric restriction protects mitochondrial function with aging in skeletal and cardiac muscles. Rejuvenation Res 9:219–222
Cui L, Jeong H, Borovecki F, Parkhurst CN, Tanese N, Krainc D (2006) Transcriptional repression of PGC-1alpha by mutant huntingtin leads to mitochondrial dysfunction and neurodegeneration. Cell 127:59–69
Fride E, Ben-Or S, Allweis C (1989) Mitochondrial protein synthesis may be involved in long-term memory formation. Pharmacol Biochem Behav 32:873–878
Bennett MC, Rose GM (1992) Chronic sodium azide treatment impairs learning of the Morris water maze task. Behav Neural Biol 58:72–75
Weeber EJ, Levy M, Sampson MJ, Anflous K, Armstrong DL, Brown SE, Sweatt JD, Craigen WJ (2002) The role of mitochondrial porins and the permeability transition pore in learning and synaptic plasticity. J Biol Chem 277:18891–18897
Levy M, Faas GC, Saggau F, Craigen W, Sweatt JD (2003) Mitochondrial regulation of synaptic plasticity in the hippocampus. J Biol Chem 278:17727–17738
Tong JJ (2007) Mitochondrial delivery is essential for synaptic potentiation. Biol Bull 212:169–175
Lee J, Bruce-Keller AJ, Kruman Y, Chan SL, Mattson MP (1999) 2-deoxy-d-glucose protects hippocampal neurons against excitotoxic and oxidative injury: evidence for the involvement of stress proteins. J. Neurosci Res 57:48–61
Bodnar RJ, Merrigan KP, Wallace MM (1981) Analgesia following intraventricular administration of 2-deoxy-d-glucose. Pharmacol Biochem Behav 14:579–581
Fisher MC, Bodnar RJ (1992) 2-Deoxy-d-glucose antinociception and serotonin receptor subtype antagonist: test-specific effect in rats. Pharmacol Biochem Behav 43:1241–1246
Mukherjee K, Mathur R, Nayar U (2001) Ventromedial hypothalamic mediation of sucrose feeding induced pain modulation. Pharmacol Biochem Behav 68:43–48
Rodgers JT, Lerin C, Haas W, Gygi SP, Spiegelman BM, Puigserver P (2005) Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1. Nature 434:113–118
Brunet A, Sweeney LB, Sturgill JF, Chua KF, Greer PL, Lin Y, Tran H, Ross SE, Mostoslavsky R, Cohen HY, Hu LS, Cheng HL, Jedrychowski MP, Gygi SP, Sinclair DA, Alt FW, Greenberg ME (2004) Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 303:2011–2015
Lin SJ, Kaeberlein M, Andalis AA, Sturtz LA, Defossez PA, Culotta VC, Fink GR, Guarente L (2002) Calorie restriction extends Saccharomyces cerevisiae lifespan by increasing respiration. Nature 418:344–348
Picard F, Kurtev M, Chung N, Topark-Ngarm A, Senawong T, Machado De Oliveira R, Leid M, McBurney MW, Guarente L (2004) Sirt1 promotes fat mobilization in white adipocytes by repressing PPAR-gamma. Nature 429:771–776
Gan L, Mucke L (2008) Paths of convergence: sirtuins in aging and neurodegeneration. Neuron 58(1):10–14
Gan L (2007) Therapeutic potential of sirtuin-activating compounds in Alzheimer's disease. Drug News Perspect 20(4):233–239
Calabrese V, Cornelius C, Mancuso C, Pennisi G, Calafato S, Bellia F, Bates TE, Giuffrida Stella AM, Schapira T, Dinkova Kostova AT, Rizzarelli E (2008) Cellular stress response: a novel target for chemoprevention and nutritional neuroprotection in aging, neurodegenerative disorders and longevity. Neurochem Res doi:10.1007/s11064-008-9775-9
López-Lluch G, Irusta PM, Navas P, De Cabo R (2008) Mitochondrial biogenesis and healthy aging. Exp Gerontol doi:10.1016/j.exger.2008.06.014
Guarente L, Picard F (2005) Calorie restriction—the SIR2 connection. Cell 120(4):473–482
Kim D, Nguyen MD, Dobbin MM, Fischer A, Sananbenesi F, Rodgers JT, Delalle I, Baur JA, Sui G, Armour SM, Puigserver P, Sinclair DA, Tsai L-H (2007) SIRT1 deacetylase protects against neurodegeneration in models for Alzheimer’s disease and amyotrophic lateral sclerosis. EMBO J 26:3169–3179
Qin W, Yang T, Ho L, Zhao Z, Wang J, Chen L, Zhao W, Thiyagarajan M, MacGrogan D, Rodgers JT, Puigserver P, Sadoshima J, Deng H, Pedrini S, Gandy S, Sauve AA, Pasinetti GM (2006) Neuronal SIRT1 activation as a novel mechanism underlying the prevention of Alzheimer disease amyloid neuropathology by calorie restriction. J Biol Chem 281:21745–21754
Pallas M, Verdaguer E, Tajes M, Gutierrez-Cuesta J, Camins A (2008) Modulation of sirtuins: new targets for antiaging. Recent Patents CNS Drug Discov 3:61–69
Wood JG, Rogina B, Lavu S, Howitz K, Helfand SL, Tatar M, Sinclair D (2004) Sirtuin activators mimic caloric restriction and delay aging in metazoans. Nature 430:686–689
Baur JA, Sinclair DA (2006) Therapeutic potential of resveratrol: the in vivo evidence. Nat Rev Drug Discov 5:493–506
Howitz KT, Bitterman KJ, Cohen HY, Lamming DW, Lavu S, Wood JG, Zipkin RE, Chung P, Kisielewski A, Zhang LL, Scherer B, Sinclair DA (2003) Small molecule activators of sirtuins extend Saccharomyces cerevisiae life span. Nature 425:191–196
Baur JA, Pearson KJ, Price NL, Jamieson HA, Lerin C, Kalra A, Prabhu VV, Allard JS, Lopez-Lluch G, Lewis K, Pistell PJ, Poosala S, Becker KG, Boss O, Gwinn D, Wang M, Ramaswamy S, Fishbein KW, Spencer RG, Lakatta EG, Le Couteur D, Shaw RJ, Navas P, Puigserver P, Ingram DK, de Cabo R, Sinclair DA (2006) Resveratrol improves health and survival of mice on a high-calorie diet. Nature 444:337–342
Dasgupta B, Milbrandt J (2007) Resveratrol stimulates AMP kinase activity in neurons. Proc Natl Acad Sci U S A 104:7217–7222
Lagouge M, Argmann C, Gerhart-Hines Z, Meziane H, Lerin C, Daussin F, Messadeq N, Milne J, Lambert P, Elliott P, Geny B, Laakso M, Puigserver P, Auwerx J (2006) Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1[alpha]. Cell 127:1109–1122
Lin SJ, Defossez PA, Guarente L (2000) Requirement of NAD and SIR2 for life-span extension by calorie restriction in Saccharomyces cerevisiae. Science 289:2126–2128
Rogina B, Helfand SL (2004) Sir2 mediates longevity in the fly through a pathway related to calorie restriction. Proc Natl Acad Sci U S A 101:15998–16003
Chen D, Guarente L (2007) SIR2: a potential target for calorie restriction mimetics. TRENDS Mol Med 13:65–71
Chen J, Zhou Y, Mueller-Steiner S, Chen LF, Kwon H, Yi S, Mucke L, Gan L (2005) SIRT1 protects against microglia-dependent amyloid-b toxicity through inhibiting NF-kB signaling. J Biol Chem 280:40364–40374
Yeung F, Hoberg JE, Ramsey CS, Keller MD, Jones DR, Frye RA, Mayo MW (2004) Modulation of NF-kB-dependent transcription and cell survival by the SIRT1 deacetylase. EMBO J 23:2369–2380
Parker JA, Arango M, Abderrahmane S, Lambert E, Tourette C, Catoire H, Néri C (2005) Resveratrol rescues mutant polyglutamine cytotoxicity in nematode and mammalian neurons. Nat Genet 37:349–350
Okawara M, Katsuki H, Kurimoto E, Shibata H, Kume T, Akaike A (2007) Resveratrol protects dopaminergic neurons in midbrain slice culture from multiple insults. Biochem Pharmacol 73:550–560
Gentilli M, Mazoit JX, Bouaziz H, Fletcher D, Casper RF, Benhamou D, Savouret JF (2001) Resveratrol decreases hyperalgesia induced by carrageenan in the rat hind paw. Life Sci 68:1317–1321
Torres-López JE, Ortizc MI, Castañeda-Hernández G, Alonso-López R, Asomoza-Espinosa R, Granados-Soto V (2002) Comparison of the antinociceptive effect of celecoxib, diclofenac and resveratrol in the formalin test. Life Sci 70:1669–1676
Gupta YK, Sharma M, Briyal S (2004) Antinociceptive effect of trans-resveratrol in rats: involvement of an opiodergic mechanism. Methods Find Exp Clin Pharmacol 26:667–672
Sharma S, Kulkarni SK, Chopra K (2007) Effect of resveratrol, a polyphenolic phytoalexin, on thermal hyperalgesia in a mouse model of diabetic neuropathic pain. Fundam Clin Pharmacol 21:89–94
Acknowledgements
We thank Mr. R. Churchill for editorial assistance with the manuscript. We also thank Miss M. Cadena for technical assistance with animal handling. This work was supported by grants from the AECI, the Junta de Andalucía (BIO-122), CAMD2005, and the DGICYT (BFU2005-01024).
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Fontán-Lozano, Á., López-Lluch, G., Delgado-García, J.M. et al. Molecular Bases of Caloric Restriction Regulation of Neuronal Synaptic Plasticity. Mol Neurobiol 38, 167–177 (2008). https://doi.org/10.1007/s12035-008-8040-1
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DOI: https://doi.org/10.1007/s12035-008-8040-1