Caloric restriction eliminates the aging-related decline in NMDA and AMPA receptor subunits in the rat hippocampus and induces homeostasis

Experimental Neurology

Volumn 206, Issue 1, 2007, Pages 70-79

  Shi, Lei ^a   Adams, Michelle M ^a   Linville, M Constance ^a   Newton, Isabel G ^a   Forbes, M Elizabeth ^a   Long, Ashley B ^a   Riddle, David R ^a   Brunso Bechtold, Judy K ^a  

^a WAKE FOREST UNIVERSITY HEALTH SCIENCES   (United States)

Author keywords

Dietary restriction; Electron microscopy; Fischer 344 Brown Norway rats; Glutamate receptor; Multiple spine bouton (MSB) synapses; Stratum radiatum

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; AMPA RECEPTOR; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

AGED; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; BRAIN REGION; CALORIC RESTRICTION; CONTROLLED STUDY; GROUPS BY AGE; HIPPOCAMPUS; LIFESPAN; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPSE; WESTERN BLOTTING;

AGING; ANIMALS; CALORIC RESTRICTION; COGNITION DISORDERS; DENDRITIC SPINES; DOWN-REGULATION; HIPPOCAMPUS; HOMEOSTASIS; LONGEVITY; MALE; MEMORY DISORDERS; MICROSCOPY, ELECTRON, TRANSMISSION; PROTEIN SUBUNITS; RATS; RATS, INBRED F344; RECEPTORS, AMPA; RECEPTORS, GLUTAMATE; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 34250622873     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2007.03.026     Document Type: Article

References (87)

1. Adams M.M., Shah R.A., Janssen W.G., and Morrison J.H. Different modes of hippocampal plasticity in response to estrogen in young and aged female rats. Proc. Natl. Acad. Sci. U. S. A 98 (2001) 8071-8076
2. Adams M.M., Smith T.D., Moga D., Gallagher M., Wang Y., Wolfe B.B., Rapp P.R., and Morrison J.H. Hippocampal dependent learning ability correlates with N-methyl-d-aspartate (NMDA) receptor levels in CA3 neurons of young and aged rats. J. Comp. Neurol. 432 (2001) 230-243
3. Adams M.M., Linville M.C., Newton I.G., Long A., Forbes M.E., Riddle D.R., and Brunso-Bechtold J.K. Effect of Caloric Restriction and Age on Synaptic Proteins in Hippocampal CA3. Society for Neuroscience 35th Annual Meeting Abstract 731.13 (2005)
4. Bach M.E., Barad M., Son H., Zhuo M., Lu Y.F., Shih R., Mansuy I., Hawkins R.D., and Kandel E.R. Age-related defects in spatial memory are correlated with defects in the late phase of hippocampal long-term potentiation in vitro and are attenuated by drugs that enhance the cAMP signaling pathway. Proc. Natl. Acad. Sci. U. S. A 96 (1999) 5280-5285
5. Barnes C.A. Normal aging: regionally specific changes in hippocampal synaptic transmission. Trends Neurosci. 17 (1994) 13-18
6. Buchs P.A., and Muller D. Induction of long-term potentiation is associated with major ultrastructural changes of activated synapses. Proc. Natl. Acad. Sci. U. S. A 93 (1996) 8040-8045
7. Burke S.N., and Barnes C.A. Neural plasticity in the ageing brain. Nat. Rev., Neurosci. 7 (2006) 30-40
8. Castel-Barthe M.N., Jazat-Poindessous F., Barneoud P., Vigne E., Revah F., Mallet J., and Lamour Y. Direct intracerebral nerve growth factor gene transfer using a recombinant adenovirus: effect on basal forebrain cholinergic neurons during aging. Neurobiol. Dis. 3 (1996) 76-86
9. Clayton D.A., and Browning M.D. Deficits in the expression of the NR2B subunit in the hippocampus of aged Fisher 344 rats. Neurobiol. Aging 22 (2001) 165-168
10. Clayton D.A., Mesches M.H., Alvarez E., Bickford P.C., and Browning M.D. A hippocampal NR2B deficit can mimic age-related changes in long-term potentiation and spatial learning in the Fischer 344 rat. J. Neurosci. 22 (2002) 3628-3637
11. Demetrius L. Caloric restriction, metabolic rate, and entropy. J. Gerontol., Ser. A, Biol. Sci. Med. Sci. 59 (2004) B902-B915
12. Eckles-Smith K., Clayton D., Bickford P., and Browning M.D. Caloric restriction prevents age-related deficits in LTP and in NMDA receptor expression. Brain Res. Mol. Brain Res. 78 (2000) 154-162
13. Fischer W., Bjorklund A., Chen K., and Gage F.H. NGF improves spatial memory in aged rodents as a function of age. J. Neurosci. 11 (1991) 1889-1906
14. Fischer M., Kaech S., Wagner U., Brinkhaus H., and Matus A. Glutamate receptors regulate actin-based plasticity in dendritic spines. Nat. Neurosci. 3 (2000) 887-894
15. Foster T.C., and Norris C.M. Age-associated changes in Ca(2+)-dependent processes: relation to hippocampal synaptic plasticity. Hippocampus 7 (1997) 602-612
16. Geinisman Y., Detoledo-Morrell L., Morrell F., and Heller R.E. Hippocampal markers of age-related memory dysfunction: behavioral, electrophysiological and morphological perspectives. Prog. Neurobiol. 45 (1995) 223-252
17. Geinisman Y., Gundersen H.J., van der Zee E., and West M.J. Unbiased stereological estimation of the total number of synapses in a brain region. J. Neurocytol. 25 (1996) 805-819
18. Geinisman Y., Berry R.W., Disterhoft J.F., Power J.M., and Van der Zee E.A. Associative learning elicits the formation of multiple-synapse boutons. J. Neurosci. 21 (2001) 5568-5573
19. Geinisman Y., Ganeshina O., Yoshida R., Berry R.W., Disterhoft J.F., and Gallagher M. Aging, spatial learning, and total synapse number in the rat CA1 stratum radiatum. Neurobiol. Aging 25 (2004) 407-416
20. Guo Z.H., and Mattson M.P. Neurotrophic factors protect cortical synaptic terminals against amyloid and oxidative stress-induced impairment of glucose transport, glutamate transport and mitochondrial function. Cereb. Cortex 10 (2000) 50-57
21. Hayashi Y., Shi S.H., Esteban J.A., Piccini A., Poncer J.C., and Malinow R. Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287 (2000) 2262-2267
22. Hering H., and Sheng M. Dendritic spines: structure, dynamics and regulation. Nat. Rev., Neurosci. 2 (2001) 880-888
23. Hollmann M., and Heinemann S. Cloned glutamate receptors. Annu. Rev. Neurosci. 17 (1994) 31-108
24. Ingram D.K., Weindruch R., Spangler E.L., Freeman J.R., and Walford R.L. Dietary restriction benefits learning and motor performance of aged mice. J. Gerontol. 42 (1987) 78-81
25. Izquierdo I., and Medina J.H. Memory formation: the sequence of biochemical events in the hippocampus and its connection to activity in other brain structures. Neurobiol. Learn. Mem. 68 (1997) 285-316
26. Jevtovic-Todorovic V., and Carter L.B. The anesthetics nitrous oxide and ketamine are more neurotoxic to old than to young rat brain. Neurobiol. Aging 26 (2005) 947-956
27. Jones T.A. Multiple synapse formation in the motor cortex opposite unilateral sensorimotor cortex lesions in adult rats. J. Comp. Neurol. 414 (1999) 57-66
28. Jones T.A., Klintsova A.Y., Kilman V.L., Sirevaag A.M., and Greenough W.T. Induction of multiple synapses by experience in the visual cortex of adult rats. Neurobiol. Learn. Mem. 68 (1997) 13-20
29. Jones T.A., Chu C.J., Grande L.A., and Gregory A.D. Motor skills training enhances lesion-induced structural plasticity in the motor cortex of adult rats. J. Neurosci. 19 (1999) 10153-10163
30. Kalani R., Judge S., Carter C., Pahor M., and Leeuwenburgh C. Effects of caloric restriction and exercise on age-related, chronic inflammation assessed by C-reactive protein and interleukin-6. J. Gerontol., Ser. A, Biol. Sci. Med. Sci. 61 (2006) 211-217
31. Kirkwood T.B., and Shanley D.P. Food restriction, evolution and ageing. Mech. Ageing Dev. 126 (2005) 1011-1016
32. Koubova J., and Guarente L. How does calorie restriction work?. Genes Dev. 17 (2003) 313-321
33. Luscher C., Nicoll R.A., Malenka R.C., and Muller D. Synaptic plasticity and dynamic modulation of the postsynaptic membrane. Nat. Neurosci. 3 (2000) 545-550
34. Magnusson K.R. Influence of diet restriction on NMDA receptor subunits and learning during aging. Neurobiol. Aging 22 (2001) 613-627
35. Magnusson K.R., and Cotman C.W. Age-related changes in excitatory amino acid receptors in two mouse strains. Neurobiol. Aging 14 (1993) 197-206
36. Magnusson K.R., Nelson S.E., and Young A.B. Age-related changes in the protein expression of subunits of the NMDA receptor. Brain Res. Mol. Brain Res. 99 (2002) 40-45
37. Major D.E., Kesslak J.P., Cotman C.W., Finch C.E., and Day J.R. Life-long dietary restriction attenuates age-related increases in hippocampal glial fibrillary acidic protein mRNA. Neurobiol. Aging 18 (1997) 523-526
38. Malinow R., and Malenka R.C. AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 25 (2002) 103-126
39. Markowska A.L., and Savonenko A. Retardation of cognitive aging by life-long diet restriction: implications for genetic variance. Neurobiol. Aging 23 (2002) 75-86
40. Markowska A.L., Mooney M., and Sonntag W.E. Insulin-like growth factor-1 ameliorates age-related behavioral deficits. Neuroscience 87 (1998) 559-569
41. Martin S.J., Grimwood P.D., and Morris R.G. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu. Rev. Neurosci. 23 (2000) 649-711
42. McCarter R.J., and McGee J.R. Transient reduction of metabolic rate by food restriction. Am. J. Physiol. 257 (1989) E175-E179
43. McHugh T.J., Blum K.I., Tsien J.Z., Tonegawa S., and Wilson M.A. Impaired hippocampal representation of space in CA1-specific NMDAR1 knockout mice. Cell 87 (1996) 1339-1349
44. Mesches M.H., Gemma C., Veng L.M., Allgeier C., Young D.A., Browning M.D., and Bickford P.C. Sulindac improves memory and increases NMDA receptor subunits in aged Fischer 344 rats. Neurobiol. Aging 25 (2004) 315-324
45. Monti B., Virgili M., and Contestabile A. Alterations of markers related to synaptic function in aging rat brain, in normal conditions or under conditions of long-term dietary manipulation. Neurochem. Int. 44 (2004) 579-584
46. Morrison J.H., and Hof P.R. Life and death of neurons in the aging brain. Science 278 (1997) 412-419
47. Moser M.B., and Moser E.I. Functional differentiation in the hippocampus. Hippocampus 8 (1998) 608-619
48. Moser M.B., Moser E.I., Forrest E., Andersen P., and Morris R.G. Spatial learning with a minislab in the dorsal hippocampus. Proc. Natl. Acad. Sci. U. S. A 92 (1995) 9697-9701
49. Mouton P.R. Principles and Practices of Unbiased Stereology (2002)
50. Nakazawa K., Quirk M.C., Chitwood R.A., Watanabe M., Yeckel M.F., Sun L.D., Kato A., Carr C.A., Johnston D., Wilson M.A., and Tonegawa S. Requirement for hippocampal CA3 NMDA receptors in associative memory recall. Science 297 (2002) 211-218
51. Newcomer J.W., and Krystal J.H. NMDA receptor regulation of memory and behavior in humans. Hippocampus 11 (2001) 529-542
52. Newton I.G., Forbes M.E., Legault C., Johnson J.E., Brunso-Bechtold J.K., and Riddle D.R. Caloric restriction does not reverse aging-related changes in hippocampal BDNF. Neurobiol. Aging 26 (2005) 683-688
53. Newton, I.G., Forbes, M.E., Linville, M.C., Pang, H., Tucker, E.W., Riddle, D.R., Brunso-Bechtold, J.K., in press. Effects of aging and caloric restriction on dentate gyrus synapses and glutamate receptor subunits. Neurobiol. Aging. [Epub ahead of print].
54. Nicholson D.A., Yoshida R., Berry R.W., Gallagher M., and Geinisman Y. Reduction in size of perforated postsynaptic densities in hippocampal axospinous synapses and age-related spatial learning impairments. J. Neurosci. 24 (2004) 7648-7653
55. Nikonenko I., Jourdain P., Alberi S., Toni N., and Muller D. Activity-induced changes of spine morphology. Hippocampus 12 (2002) 585-591
56. Oh M.M., Kuo A.G., Wu W.W., Sametsky E.A., and Disterhoft J.F. Watermaze learning enhances excitability of CA1 pyramidal neurons. J. Neurophysiol. 90 (2003) 2171-2179
57. Okada M., Nakanishi H., Amamoto T., Urae R., Ando S., Yazawa K., and Fujiwara M. How does prolonged caloric restriction ameliorate age-related impairment of long-term potentiation in the hippocampus?. Brain Res. Mol. Brain Res. 111 (2003) 175-181
58. Otani S., and Ben Ari Y. Biochemical correlates of long-term potentiation in hippocampal synapses. Int. Rev. Neurobiol. 35 (1993) 1-41
59. Paxinos, G., Watson, C., 1986. The rat brain in stereotaxic coordinates, 1st Edition. Academic Press, San Diego, CA.
60. Rapp P.R., and Gallagher M. Preserved neuron number in the hippocampus of aged rats with spatial learning deficits. Proc. Natl. Acad. Sci. U. S. A 93 (1996) 9926-9930
61. Riedel G., Platt B., and Micheau J. Glutamate receptor function in learning and memory. Behav. Brain Res. 140 (2003) 1-47
62. Rosenzweig E.S., and Barnes C.A. Impact of aging on hippocampal function: plasticity, network dynamics, and cognition. Prog. Neurobiol. 69 (2003) 143-179
63. Rosenzweig E.S., Rao G., McNaughton B.L., and Barnes C.A. Role of temporal summation in age-related long-term potentiation-induction deficits. Hippocampus 7 (1997) 549-558
64. Roth G.S., Ingram D.K., and Lane M.A. Slowing ageing by caloric restriction. Nat. Med. 1 (1995) 414-415
65. Shi L., Linville M.C., Tucker E.W., Sonntag W.E., and Brunso-Bechtold J.K. Differential effects of aging and insulin-like growth factor-1 on synapses in CA1 of rat hippocampus. Cereb. Cortex 15 (2005) 571-577
66. Smith T.D., Adams M.M., Gallagher M., Morrison J.H., and Rapp P.R. Circuit-specific alterations in hippocampal synaptophysin immunoreactivity predict spatial learning impairment in aged rats. J. Neurosci. 20 (2000) 6587-6593
67. Sohal R.S., and Weindruch R. Oxidative stress, caloric restriction, and aging. Science 273 (1996) 59-63
68. Sonntag W.E., Bennett S.A., Khan A.S., Thornton P.L., Xu X., Ingram R.L., and Brunso-Bechtold J.K. Age and insulin-like growth factor-1 modulate N-methyl-d-aspartate receptor subtype expression in rats. Brain Res. Bull. 51 (2000) 331-338
69. Sonntag W.E., Lynch C.D., Cefalu W.T., Ingram R.L., Bennett S.A., Thornton P.L., and Khan A.S. Pleiotropic effects of growth hormone and insulin-like growth factor (IGF)-1 on biological aging: inferences from moderate caloric-restricted animals. J. Gerontol., Ser. A, Biol. Sci. Med. Sci. 54 (1999) B521-B538
70. Sorra K.E., Fiala J.C., and Harris K.M. Critical assessment of the involvement of perforations, spinules, and spine branching in hippocampal synapse formation. J. Comp. Neurol. 398 (1998) 225-240
71. Sterio D.C. The unbiased estimation of number and sizes of arbitrary particles using the dissector. J. Microsc. 134 Pt 2 (1984) 127-136
72. Tacconi M.T., Lligona L., Salmona M., Pitsikas N., and Algeri S. Aging and food restriction: effect on lipids of cerebral cortex. Neurobiol. Aging 12 (1991) 55-59
73. Tamaru M., Yoneda Y., Ogita K., Shimizu J., and Nagata Y. Age-related decreases of the N-methyl-d-aspartate receptor complex in the rat cerebral cortex and hippocampus. Brain Res. 542 (1991) 83-90
74. Tata D.A., Marciano V.A., and Anderson B.J. Synapse loss from chronically elevated glucocorticoids: relationship to neuropil volume and cell number in hippocampal area CA3. J. Comp. Neurol. 498 (2006) 363-374
75. Tombaugh G.C., Rowe W.B., Chow A.R., Michael T.H., and Rose G.M. Theta-frequency synaptic potentiation in CA1 in vitro distinguishes cognitively impaired from unimpaired aged Fischer 344 rats. J. Neurosci. 22 (2002) 9932-9940
76. Toni N., Buchs P.A., Nikonenko I., Bron C.R., and Muller D. LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature 402 (1999) 421-425
77. Toni N., Buchs P.A., Nikonenko I., Povilaitite P., Parisi L., and Muller D. Remodeling of synaptic membranes after induction of long-term potentiation. J. Neurosci. 21 (2001) 6245-6251
78. Tovar K.R., and Westbrook G.L. Mobile NMDA receptors at hippocampal synapses. Neuron 34 (2002) 255-264
79. Tsien J.Z., Huerta P.T., and Tonegawa S. The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory. Cell 87 (1996) 1327-1338
80. Weeks A.C., Ivanco T.L., Leboutillier J.C., Marrone D.F., Racine R.J., and Petit T.L. Unique changes in synaptic morphology following tetanization under pharmacological blockade. Synapse 47 (2003) 77-86
81. Weindruch R., Naylor P.H., Goldstein A.L., and Walford R.L. Influences of aging and dietary restriction on serum thymosin alpha 1 levels in mice. J. Gerontol. 43 (1988) B40-B42
82. Wenk G.L., and Barnes C.A. Regional changes in the hippocampal density of AMPA and NMDA receptors across the lifespan of the rat. Brain Res. 885 (2000) 1-5
83. Wenk G.L., Walker L.C., Price D.L., and Cork L.C. Loss of NMDA, but not GABA-A, binding in the brains of aged rats and monkeys. Neurobiol. Aging 12 (1991) 93-98
84. West M.J., Slomianka L., and Gundersen H.J. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat. Rec. 231 (1991) 482-497
85. Yu B.P., and Chung H.Y. Stress resistance by caloric restriction for longevity. Ann. N. Y. Acad. Sci. 928 (2001) 39-47
86. Yu B.P., Masoro E.J., and McMahan C.A. Nutritional influences on aging of Fischer 344 rats: I. Physical, metabolic, and longevity characteristics. J. Gerontol. 40 (1985) 657-670
87. Ziff E.B. Enlightening the postsynaptic density. Neuron 19 (1997) 1163-1174