Home LiteratureArticle Details
PMID: 18759009 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

Molecular bases of caloric restriction regulation of neuronal synaptic plasticity.

Molecular neurobiology ·Vol. 38 ·No. 2 ·2008-10-00 ·Pages 167-77

Fontán-Lozano A, López-Lluch G, Delgado-García JM, Navas P, Carrión AM

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.

MeSH Terms
Aging/physiology Analgesia Animals Caloric Restriction Humans Learning/physiology Mitochondria/metabolism Neurodegenerative Diseases/diet therapy,physiopathology Neuronal Plasticity/physiology Neurons/physiology Synapses/metabolism
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Fontán-Lozano Angela
División de Neurociencias, Universidad Pablo de Olavide, Ctra. de Utrera Km. 1, 41013 Seville, Spain.
López-Lluch Guillermo
Delgado-García José María
Navas Placido
Carrión Angel Manuel
References (151)
151 references, click to expand
  1. Therapeutic potential of resveratrol: the in vivo evidence.
    Nat Rev Drug Discov. 2006 Jun;5(6):493-506 PMID: 16732220
  2. Prophylactic activation of neuroprotective stress response pathways by dietary and behavioral manipulations.
    NeuroRx. 2004 Jan;1(1):111-6 PMID: 15717011
  3. Cellular stress response: a novel target for chemoprevention and nutritional neuroprotection in aging, neurodegenerative disorders and longevity.
    Neurochem Res. 2008 Dec;33(12):2444-71 PMID: 18629638
  4. Dynorphin-(1-8) inhibits the release of substance P-like immunoreactivity in the spinal cord of rats following a noxious mechanical stimulus.
    Eur J Pharmacol. 1997 Apr 4;323(2-3):159-65 PMID: 9128834
  5. Glutamatergic neurotransmission in aging: a critical perspective.
    Mech Ageing Dev. 2001 Jan;122(1):1-29 PMID: 11163621
  6. Incidence of dementia and Alzheimer disease in 2 communities: Yoruba residing in Ibadan, Nigeria, and African Americans residing in Indianapolis, Indiana.
    JAMA. 2001 Feb 14;285(6):739-47 PMID: 11176911
  7. The analgesia produced by food deprivation in 4-month old, 14-month old, and 24-month old rats.
    Life Sci. 1986 Oct 27;39(17):1509-15 PMID: 3762313
  8. Dietary restriction and 2-deoxyglucose administration reduce focal ischemic brain damage and improve behavioral outcome: evidence for a preconditioning mechanism.
    J Neurosci Res. 1999 Sep 15;57(6):830-9 PMID: 10467254
  9. Protein modification by the lipid peroxidation product 4-hydroxynonenal in the spinal cords of amyotrophic lateral sclerosis patients.
    Ann Neurol. 1998 Nov;44(5):819-24 PMID: 9818940
  10. Calorie restriction induces mitochondrial biogenesis and bioenergetic efficiency.
    Proc Natl Acad Sci U S A. 2006 Feb 7;103(6):1768-73 PMID: 16446459
  11. Analgesic effects of dietary caloric restriction in adult mice.
    Pain. 2005 Apr;114(3):455-461 PMID: 15777870
  12. Modeling mitochondrial function in aging neurons.
    Trends Neurosci. 2004 Oct;27(10):601-6 PMID: 15374671
  13. Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan.
    Nature. 2003 Sep 11;425(6954):191-6 PMID: 12939617
  14. 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. 1992 Dec 1;89(23):11533-7 PMID: 1454844
  15. 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. 2004 Mar;25(3):361-75 PMID: 15123342
  16. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase.
    Science. 2004 Mar 26;303(5666):2011-5 PMID: 14976264
  17. 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. 1989 Nov-Dec;10(6):669-75 PMID: 2628778
  18. Meal size and frequency affect neuronal plasticity and vulnerability to disease: cellular and molecular mechanisms.
    J Neurochem. 2003 Feb;84(3):417-31 PMID: 12558961
  19. Neural plasticity in the ageing brain.
    Nat Rev Neurosci. 2006 Jan;7(1):30-40 PMID: 16371948
  20. Comparison of the antinociceptive effect of celecoxib, diclofenac and resveratrol in the formalin test.
    Life Sci. 2002 Feb 22;70(14):1669-76 PMID: 11991254
  21. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha.
    Cell. 2006 Dec 15;127(6):1109-22 PMID: 17112576
  22. Molecular mechanisms of brain aging and neurodegenerative disorders: lessons from dietary restriction.
    Trends Neurosci. 2001 Nov;24(11 Suppl):S21-31 PMID: 11881742
  23. Age-related changes in theta frequency stimulation-induced long-term potentiation.
    Neurobiol Aging. 2003 Mar-Apr;24(2):267-72 PMID: 12498960
  24. Sir2 mediates longevity in the fly through a pathway related to calorie restriction.
    Proc Natl Acad Sci U S A. 2004 Nov 9;101(45):15998-6003 PMID: 15520384
  25. Modulation of NF-kappaB-dependent transcription and cell survival by the SIRT1 deacetylase.
    EMBO J. 2004 Jun 16;23(12):2369-80 PMID: 15152190
  26. Student perceptions of methylphenidate abuse at a public liberal arts college.
    J Am Coll Health. 2000 Nov;49(3):143-5 PMID: 11125642
  27. Environmental enrichment promotes neurogenesis and changes the extracellular concentrations of glutamate and GABA in the hippocampus of aged rats.
    Brain Res Bull. 2006 Jun 15;70(1):8-14 PMID: 16750477
  28. Dietary restriction: effects on radial maze learning and lipofuscin pigment deposition in the hippocampus and frontal cortex.
    Arch Gerontol Geriatr. 1987 Dec;6(4):355-62 PMID: 3439824
  29. Calorie restriction, SIRT1 and metabolism: understanding longevity.
    Nat Rev Mol Cell Biol. 2005 Apr;6(4):298-305 PMID: 15768047
  30. Evaluating the interdependence of aging-related changes in visual and auditory acuity, balance, and cognitive functioning.
    Psychol Aging. 2003 Jun;18(2):285-305 PMID: 12825777
  31. 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. 2006 Jul;61(7):675-84 PMID: 16870628
  32. Effect of age and caloric intake on protein oxidation in different brain regions and on behavioral functions of the mouse.
    Arch Biochem Biophys. 1996 Sep 1;333(1):189-97 PMID: 8806770
  33. Molecular pathways of pain: Fos/Jun-mediated activation of a noncanonical AP-1 site in the prodynorphin gene.
    Neuron. 1991 Apr;6(4):607-17 PMID: 1901718
  34. A synaptic model of memory: long-term potentiation in the hippocampus.
    Nature. 1993 Jan 7;361(6407):31-9 PMID: 8421494
  35. Neuronal SIRT1 activation as a novel mechanism underlying the prevention of Alzheimer disease amyloid neuropathology by calorie restriction.
    J Biol Chem. 2006 Aug 4;281(31):21745-21754 PMID: 16751189
  36. kappa-opioid receptor agonists modulate excitatory transmission in substantia gelatinosa neurons of the rat spinal cord.
    J Neurosci. 1995 Oct;15(10):6809-26 PMID: 7472439
  37. Ventromedial hypothalamic mediation of sucrose feeding induced pain modulation.
    Pharmacol Biochem Behav. 2001 Jan;68(1):43-8 PMID: 11274706
  38. Paths of convergence: sirtuins in aging and neurodegeneration.
    Neuron. 2008 Apr 10;58(1):10-4 PMID: 18400158
  39. Dietary restriction protects hippocampal neurons against the death-promoting action of a presenilin-1 mutation.
    Brain Res. 1999 Sep 18;842(1):224-9 PMID: 10526115
  40. Changes in plasma lipids and lipoproteins in humans during a 2-year period of dietary restriction in Biosphere 2.
    Arch Intern Med. 1998 Apr 27;158(8):900-6 PMID: 9570177
  41. BDNF increases rat brain mitochondrial respiratory coupling at complex I, but not complex II.
    Eur J Neurosci. 2004 Sep;20(5):1189-96 PMID: 15341590
  42. Calorie restriction in nonhuman primates: effects on diabetes and cardiovascular disease risk.
    Toxicol Sci. 1999 Dec;52(2 Suppl):41-8 PMID: 10630589
  43. Calorie restriction extends Saccharomyces cerevisiae lifespan by increasing respiration.
    Nature. 2002 Jul 18;418(6895):344-8 PMID: 12124627
  44. The retardation of aging by caloric restriction: its significance in the transgenic era.
    Exp Gerontol. 2003 Nov-Dec;38(11-12):1343-51 PMID: 14698815
  45. Suppression of brain aging and neurodegenerative disorders by dietary restriction and environmental enrichment: molecular mechanisms.
    Mech Ageing Dev. 2001 May 31;122(7):757-78 PMID: 11322996
  46. Dietary restriction and 2-deoxyglucose administration improve behavioral outcome and reduce degeneration of dopaminergic neurons in models of Parkinson's disease.
    J Neurosci Res. 1999 Jul 15;57(2):195-206 PMID: 10398297
  47. Oxidative stress in Parkinson's disease.
    Ann Neurol. 2003;53 Suppl 3:S26-36; discussion S36-8 PMID: 12666096
  48. Amelioration of age-related deficits in the stimulation of synapsin phosphorylation.
    Neurobiol Aging. 1997 Mar-Apr;18(2):213-7 PMID: 9258899
  49. Requirement of NAD and SIR2 for life-span extension by calorie restriction in Saccharomyces cerevisiae.
    Science. 2000 Sep 22;289(5487):2126-8 PMID: 11000115
  50. SIR2: a potential target for calorie restriction mimetics.
    Trends Mol Med. 2007 Feb;13(2):64-71 PMID: 17207661
  51. Changing subunit composition of heteromeric NMDA receptors during development of rat cortex.
    Nature. 1994 Mar 10;368(6467):144-7 PMID: 8139656
  52. Dietary restriction benefits learning and motor performance of aged mice.
    J Gerontol. 1987 Jan;42(1):78-81 PMID: 3794202
  53. Unresponsiveness to cannabinoids and reduced addictive effects of opiates in CB1 receptor knockout mice.
    Science. 1999 Jan 15;283(5400):401-4 PMID: 9888857
  54. Ca(2+)-dependent prodynorphin transcriptional derepression in neuroblastoma cells is exerted through DREAM protein activity in a kinase-independent manner.
    Mol Cell Neurosci. 2003 Feb;22(2):135-45 PMID: 12676525
  55. Ginkgo biloba: A Cognitive Enhancer?
    Psychol Sci Public Interest. 2002 May;3(1):2-11 PMID: 26151474
  56. 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. 2005 Feb;32(1):27-36 PMID: 15825543
  57. Food restriction reduces brain damage and improves behavioral outcome following excitotoxic and metabolic insults.
    Ann Neurol. 1999 Jan;45(1):8-15 PMID: 9894871
  58. Inflammation and Alzheimer's disease pathogenesis.
    Neurobiol Aging. 1996 Sep-Oct;17(5):681-6 PMID: 8892340
  59. Neuronal adaptation to amphetamine and dopamine: molecular mechanisms of prodynorphin gene regulation in rat striatum.
    Neuron. 1995 Apr;14(4):813-23 PMID: 7718243
  60. Analgesia induced by dietary restriction is mediated by the kappa-opioid system.
    J Neurosci. 2003 Dec 3;23(35):11120-6 PMID: 14657170
  61. The role of mitochondrial porins and the permeability transition pore in learning and synaptic plasticity.
    J Biol Chem. 2002 May 24;277(21):18891-7 PMID: 11907043
  62. Aging in rhesus monkeys: relevance to human health interventions.
    Science. 2004 Sep 3;305(5689):1423-6 PMID: 15353793
  63. Effect of lifelong hypocaloric diet on discrete memory of the senescent rat.
    Aging (Milano). 1991 Jun;3(2):147-52 PMID: 1911903
  64. 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. 2006 Jul;27(7):1020-34 PMID: 15996793
  65. Chronic sodium azide treatment impairs learning of the Morris water maze task.
    Behav Neural Biol. 1992 Jul;58(1):72-5 PMID: 1417674
  66. Analgesia following intraventricular administration of 2-deoxy-D-glucose.
    Pharmacol Biochem Behav. 1981 Apr;14(4):579-81 PMID: 7232479
  67. Absence of delta -9-tetrahydrocannabinol dysphoric effects in dynorphin-deficient mice.
    J Neurosci. 2001 Dec 1;21(23):9499-505 PMID: 11717384
  68. Mitochondrial dysfunction and molecular pathways of disease.
    Exp Mol Pathol. 2007 Aug;83(1):84-92 PMID: 17239370
  69. Aging, plasticity and environmental enrichment: structural changes and neurotransmitter dynamics in several areas of the brain.
    Brain Res Rev. 2007 Aug;55(1):78-88 PMID: 17561265
  70. Stimulus-specific hierarchy of enhancer elements within the rat prodynorphin promoter.
    J Neurochem. 1998 Mar;70(3):914-21 PMID: 9489710
  71. Developmental and regional expression in the rat brain and functional properties of four NMDA receptors.
    Neuron. 1994 Mar;12(3):529-40 PMID: 7512349
  72. 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. 2002 Jun;57(6):B211-24 PMID: 12023257
  73. Impact of aging on hippocampal function: plasticity, network dynamics, and cognition.
    Prog Neurobiol. 2003 Feb;69(3):143-79 PMID: 12758108
  74. Neuronal plasticity and signal transduction in nociceptive neurons: implications for the initiation and maintenance of pathological pain.
    Neurobiol Dis. 2001 Feb;8(1):1-10 PMID: 11162235
  75. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation.
    J Neurosci. 1996 Mar 15;16(6):2027-33 PMID: 8604047
  76. Gene expression and DNA repair in progeroid syndromes and human aging.
    Ageing Res Rev. 2005 Nov;4(4):579-602 PMID: 16246641
  77. Endogenous opiates: 1999.
    Peptides. 2000 Dec;21(12):1975-2034 PMID: 11150656
  78. Long-term plasticity of intrinsic excitability: learning rules and mechanisms.
    Learn Mem. 2003 Nov-Dec;10(6):456-65 PMID: 14657257
  79. Stress of chronic food restriction attenuates the development of adjuvant arthritis in male Long Evans rats.
    Clin Exp Rheumatol. 2001 Jul-Aug;19(4):371-6 PMID: 11491491
  80. Resveratrol improves health and survival of mice on a high-calorie diet.
    Nature. 2006 Nov 16;444(7117):337-42 PMID: 17086191
  81. Ubiquitin, proteasomes, and the aging brain.
    Sci Aging Knowledge Environ. 2003 Aug 27;2003(34):RE6 PMID: 12944592
  82. Therapeutic potential of sirtuin-activating compounds in Alzheimer's disease.
    Drug News Perspect. 2007 May;20(4):233-9 PMID: 17637936
  83. Caloric restriction and aging: an update.
    Exp Gerontol. 2000 May;35(3):299-305 PMID: 10832051
  84. The quest for a smart pill.
    Sci Am. 2003 Sep;289(3):54-7, 60-5 PMID: 12951828
  85. DREAM is a Ca2+-regulated transcriptional repressor.
    Nature. 1999 Mar 4;398(6722):80-4 PMID: 10078534
  86. Overview of protein aggregation in single, double, and triple neurodegenerative brain amyloidoses.
    Neuromolecular Med. 2003;4(1-2):1-6 PMID: 14528048
  87. 'Knock-down' of spinal CB1 receptors produces abnormal pain and elevates spinal dynorphin content in mice.
    Pain. 2002 Nov;100(1-2):203-9 PMID: 12435473
  88. Development of tolerance to endogenous opiates activated by 24-h food deprivation.
    Appetite. 1992 Aug;19(1):1-13 PMID: 1416933
  89. Iron, brain ageing and neurodegenerative disorders.
    Nat Rev Neurosci. 2004 Nov;5(11):863-73 PMID: 15496864
  90. Sirt1 promotes fat mobilization in white adipocytes by repressing PPAR-gamma.
    Nature. 2004 Jun 17;429(6993):771-6 PMID: 15175761
  91. Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1alpha null mice.
    Cell. 2004 Oct 1;119(1):121-35 PMID: 15454086
  92. Exploring the opioid system by gene knockout.
    Prog Neurobiol. 2002 Apr;66(5):285-306 PMID: 12015197
  93. Chronic, controlled GDNF infusion promotes structural and functional recovery in advanced parkinsonian monkeys.
    Brain. 2002 Oct;125(Pt 10):2191-201 PMID: 12244077
  94. Neuronal plasticity: increasing the gain in pain.
    Science. 2000 Jun 9;288(5472):1765-9 PMID: 10846153
  95. Gene-expression profile of the ageing brain in mice.
    Nat Genet. 2000 Jul;25(3):294-7 PMID: 10888876
  96. Deterioration of spatial and nonspatial reference and working memory in aged rats: protective effect of life-long calorie restriction.
    Neurobiol Aging. 1992 May-Jun;13(3):369-73 PMID: 1625765
  97. Central sensitization and LTP: do pain and memory share similar mechanisms?
    Trends Neurosci. 2003 Dec;26(12):696-705 PMID: 14624855
  98. Cloning and characterization of multiple opioid receptors.
    NIDA Res Monogr. 1996;161:127-40 PMID: 8784848
  99. Mitochondrial protein synthesis may be involved in long-term memory formation.
    Pharmacol Biochem Behav. 1989 Apr;32(4):873-8 PMID: 2798536
  100. 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. 2003 May 13;100(10):6216-20 PMID: 12724520
  101. DREAM is a critical transcriptional repressor for pain modulation.
    Cell. 2002 Jan 11;108(1):31-43 PMID: 11792319
  102. Caloric restriction prevents age-related deficits in LTP and in NMDA receptor expression.
    Brain Res Mol Brain Res. 2000 May 31;78(1-2):154-62 PMID: 10891595
  103. Modulation of sirtuins: new targets for antiageing.
    Recent Pat CNS Drug Discov. 2008 Jan;3(1):61-9 PMID: 18221243
  104. Long-term potentiation and long-term depression of primary afferent neurotransmission in the rat spinal cord.
    J Neurosci. 1993 Dec;13(12):5228-41 PMID: 8254370
  105. Localization of the transcriptional coactivator PGC-1alpha to GABAergic neurons during maturation of the rat brain.
    J Comp Neurol. 2007 May 1;502(1):1-18 PMID: 17335037
  106. Development of calorie restriction mimetics as a prolongevity strategy.
    Ann N Y Acad Sci. 2004 Jun;1019:412-23 PMID: 15247056
  107. Calorie restriction, aging, and cancer prevention: mechanisms of action and applicability to humans.
    Annu Rev Med. 2003;54:131-52 PMID: 12525670
  108. Adult-onset calorie restriction and fasting delay spontaneous tumorigenesis in p53-deficient mice.
    Carcinogenesis. 2002 May;23(5):817-22 PMID: 12016155
  109. Resveratrol protects dopaminergic neurons in midbrain slice culture from multiple insults.
    Biochem Pharmacol. 2007 Feb 15;73(4):550-60 PMID: 17147953
  110. Mitochondria and neuronal activity.
    Am J Physiol Cell Physiol. 2007 Feb;292(2):C641-57 PMID: 17092996
  111. Transcriptional repression of PGC-1alpha by mutant huntingtin leads to mitochondrial dysfunction and neurodegeneration.
    Cell. 2006 Oct 6;127(1):59-69 PMID: 17018277
  112. SIRT1 deacetylase protects against neurodegeneration in models for Alzheimer's disease and amyotrophic lateral sclerosis.
    EMBO J. 2007 Jul 11;26(13):3169-79 PMID: 17581637
  113. Lessons learned from gene expression profile studies of aging and caloric restriction.
    Ageing Res Rev. 2005 Jan;4(1):55-65 PMID: 15619470
  114. Resveratrol decreases hyperalgesia induced by carrageenan in the rat hind paw.
    Life Sci. 2001 Feb 2;68(11):1317-21 PMID: 11233998
  115. Mitochondrial regulation of synaptic plasticity in the hippocampus.
    J Biol Chem. 2003 May 16;278(20):17727-34 PMID: 12604600
  116. The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses.
    Cell. 2004 Dec 17;119(6):873-87 PMID: 15607982
  117. Functional blockage of the cannabinoid receptor type 1 evokes a kappa-opiate-dependent analgesia.
    J Neurochem. 2007 Dec;103(6):2629-39 PMID: 17953671
  118. Antinociceptive effect of trans-resveratrol in rats: Involvement of an opioidergic mechanism.
    Methods Find Exp Clin Pharmacol. 2004 Nov;26(9):667-72 PMID: 15632951
  119. Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1.
    Nature. 2005 Mar 3;434(7029):113-8 PMID: 15744310
  120. Gene regulation and DNA damage in the ageing human brain.
    Nature. 2004 Jun 24;429(6994):883-91 PMID: 15190254
  121. Sirtuin activators mimic caloric restriction and delay ageing in metazoans.
    Nature. 2004 Aug 5;430(7000):686-9 PMID: 15254550
  122. The endogenous cannabinoid system and its role in nociceptive behavior.
    J Neurobiol. 2004 Oct;61(1):149-60 PMID: 15362158
  123. No DREAM, No pain. Closing the spinal gate.
    Cell. 2002 Feb 8;108(3):297-300 PMID: 11853663
  124. Ageing and neuronal vulnerability.
    Nat Rev Neurosci. 2006 Apr;7(4):278-94 PMID: 16552414
  125. 2-Deoxy-D-glucose antinociception and serotonin receptor subtype antagonists: test-specific effects in rats.
    Pharmacol Biochem Behav. 1992 Dec;43(4):1241-6 PMID: 1475308
  126. Involvement of the CA3-CA1 synapse in the acquisition of associative learning in behaving mice.
    J Neurosci. 2006 Jan 25;26(4):1077-87 PMID: 16436593
  127. Monomeric Cu,Zn-superoxide dismutase is a common misfolding intermediate in the oxidation models of sporadic and familial amyotrophic lateral sclerosis.
    J Biol Chem. 2004 Apr 9;279(15):15499-504 PMID: 14734542
  128. Dietary lipids and antioxidants in Parkinson's disease: a population-based, case-control study.
    Ann Neurol. 1996 Jan;39(1):89-94 PMID: 8572672
  129. Calorie restriction--the SIR2 connection.
    Cell. 2005 Feb 25;120(4):473-82 PMID: 15734680
  130. Delaying the mitochondrial decay of aging.
    Ann N Y Acad Sci. 2004 Jun;1019:406-11 PMID: 15247055
  131. 2-Deoxy-D-glucose protects hippocampal neurons against excitotoxic and oxidative injury: evidence for the involvement of stress proteins.
    J Neurosci Res. 1999 Jul 1;57(1):48-61 PMID: 10397635
  132. Resveratrol stimulates AMP kinase activity in neurons.
    Proc Natl Acad Sci U S A. 2007 Apr 24;104(17):7217-22 PMID: 17438283
  133. Huntingtin interacts with REST/NRSF to modulate the transcription of NRSE-controlled neuronal genes.
    Nat Genet. 2003 Sep;35(1):76-83 PMID: 12881722
  134. Caloric restriction protects mitochondrial function with aging in skeletal and cardiac muscles.
    Rejuvenation Res. 2006 Summer;9(2):219-22 PMID: 16706647
  135. Reversal of behavioral and metabolic abnormalities, and insulin resistance syndrome, by dietary restriction in mice deficient in brain-derived neurotrophic factor.
    Endocrinology. 2003 Jun;144(6):2446-53 PMID: 12746306
  136. Induction of long-term potentiation at spinal synapses by noxious stimulation or nerve injury.
    Eur J Neurosci. 1998 Jul;10(7):2476-80 PMID: 9749775
  137. What we need to know about age related memory loss.
    BMJ. 2002 Jun 22;324(7352):1502-5 PMID: 12077041
  138. Reduced synaptic plasticity in the lateral perforant path input to the dentate gyrus of aged C57BL/6 mice.
    J Neurophysiol. 2003 Jul;90(1):32-8 PMID: 12634277
  139. Mitochondrial biogenesis and healthy aging.
    Exp Gerontol. 2008 Sep;43(9):813-9 PMID: 18662766
  140. Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS.
    Science. 2005 Oct 14;310(5746):314-7 PMID: 16224023
  141. Caloric restriction increases learning consolidation and facilitates synaptic plasticity through mechanisms dependent on NR2B subunits of the NMDA receptor.
    J Neurosci. 2007 Sep 19;27(38):10185-95 PMID: 17881524
  142. Effect of resveratrol, a polyphenolic phytoalexin, on thermal hyperalgesia in a mouse model of diabetic neuropathic pain.
    Fundam Clin Pharmacol. 2007 Feb;21(1):89-94 PMID: 17227449
  143. Mitochondrial delivery is essential for synaptic potentiation.
    Biol Bull. 2007 Apr;212(2):169-75 PMID: 17438209
  144. Gene expression profiling of aging using DNA microarrays.
    Mech Ageing Dev. 2002 Jan;123(2-3):177-93 PMID: 11718811
  145. Calorie restriction and aging: review of the literature and implications for studies in humans.
    Am J Clin Nutr. 2003 Sep;78(3):361-9 PMID: 12936916
  146. Pathways towards and away from Alzheimer's disease.
    Nature. 2004 Aug 5;430(7000):631-9 PMID: 15295589
  147. SIRT1 protects against microglia-dependent amyloid-beta toxicity through inhibiting NF-kappaB signaling.
    J Biol Chem. 2005 Dec 2;280(48):40364-74 PMID: 16183991
  148. The neurotrophin receptor TrkB is colocalized to mitochondrial membranes.
    Int J Biochem Cell Biol. 2006;38(4):610-20 PMID: 16343976
  149. The selective vulnerability of nerve cells in Huntington's disease.
    Neuropathol Appl Neurobiol. 2001 Feb;27(1):1-21 PMID: 11298997
  150. Resveratrol rescues mutant polyglutamine cytotoxicity in nematode and mammalian neurons.
    Nat Genet. 2005 Apr;37(4):349-50 PMID: 15793589
  151. Reactive oxygen species and synaptic plasticity in the aging hippocampus.
    Ageing Res Rev. 2004 Nov;3(4):431-43 PMID: 15541710
Article Info
Journal
Molecular neurobiology
Abbr.
Mol Neurobiol
ISSN
0893-7648
DOI
10.1007/s12035-008-8040-1
Published
2008-10-00
Epub
2008-00-30
Pages
167-77
Language
English
Region
United States
NLM ID
8900963
Subset
IM
External Links
PubMed source DOI: 10.1007/s12035-008-8040-1 View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2