Long-term ginsenoside Rg1 supplementation improves age-related cognitive decline by promoting synaptic plasticity associated protein expression in C57BL/6J mice

Journals of Gerontology - Series A Biological Sciences and Medical Sciences

Volumn 69 A, Issue 3, 2014, Pages 282-294

  Yang, Lumeng ^a   Zhang, Jing ^a   Zheng, Kunmu ^b   Shen, Hui ^a   Chen, Xiaochun ^a  

^a FUJIAN MEDICAL UNIVERSITY   (China)

^b THE FIRST AFFILIATED HOSPITAL OF XIAMEN UNIVERSITY   (China)

Author keywords

Aging; Cognition; Ginsenoside; MTOR; Synapse

Indexed keywords

CASK KINASES; CENTRAL NERVOUS SYSTEM AGENTS; DLGH4 PROTEIN, MOUSE; GINSENOSIDE; GINSENOSIDE RG 1; GUANYLATE KINASE; HERBACEOUS AGENT; MEMBRANE PROTEIN; MTOR PROTEIN, MOUSE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; SIGNAL PEPTIDE; SYNAPTOPHYSIN; SYP PROTEIN, MOUSE; TARGET OF RAPAMYCIN KINASE;

AGING; ANIMAL; ANIMAL BEHAVIOR; ARTICLE; C57BL MOUSE; COGNITION; COMPARATIVE STUDY; DIET SUPPLEMENTATION; DRUG EFFECT; FEMALE; HIPPOCAMPUS; INBRED MOUSE STRAIN; MAZE TEST; MEMORY; MOUSE; MTOR.; NERVE CELL PLASTICITY; PANAX; RANDOMIZATION; SPATIAL BEHAVIOR; SYNAPSE; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

AGING; COGNITION; GINSENOSIDE; MTOR.; SYNAPSE;

AGING; ANIMALS; BEHAVIOR, ANIMAL; CENTRAL NERVOUS SYSTEM AGENTS; COGNITION; DIETARY SUPPLEMENTS; DRUGS, CHINESE HERBAL; FEMALE; GINSENOSIDES; GUANYLATE KINASE; HIPPOCAMPUS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MAZE LEARNING; MEMBRANE PROTEINS; MEMORY; MICE; MICE, INBRED C57BL; MICE, INBRED STRAINS; MICROSCOPY, ELECTRON, TRANSMISSION; NEURONAL PLASTICITY; PANAX; RANDOM ALLOCATION; RECEPTORS, N-METHYL-D-ASPARTATE; SPATIAL BEHAVIOR; SYNAPSES; SYNAPTOPHYSIN; TOR SERINE-THREONINE KINASES;

EID: 84896779646     PISSN: 10795006     EISSN: 1758535X     Source Type: Journal    
DOI: 10.1093/gerona/glt091     Document Type: Article

References (79)

1. Burke SN, Barnes CA. Neural plasticity in the ageing brain. Nat Rev Neurosci. 2006;7:30-40.
2. Peters A, Sethares C, Luebke JI. Synapses are lost during aging in the primate prefrontal cortex. Neuroscience. 2008;152:970-981.
3. Soghomonian JJ, Sethares C, Peters A. Effects of age on axon terminals forming axosomatic and axodendritic inhibitory synapses in prefrontal cortex. Neuroscience. 2010;168:74-81.
4. Peters A, Kemper T. A review of the structural alterations in the cerebral hemispheres of the aging rhesus monkey. Neurobiol Aging. 2012;33:2357-2372.
5. Van Guilder HD, Farley JA, Yan H, et al. Hippocampal dysregulation of synaptic plasticity-associated proteins with age-related cognitive decline. Neurobiol Dis. 2011;43:201-212.
6. Squire LR, Davis HP. The pharmacology of memory: a neurobiological perspective. Annu Rev Pharmacol Toxicol. 1981;21:323-356.
7. Kelleher RJ III, Govindarajan A, Tonegawa S. Translational regulatory mechanisms in persistent forms of synaptic plasticity. Neuron. 2004;44:59-73.
8. Garelick MG, Kennedy BK. TOR on the brain. Exp Gerontol. 2011;46:155-163.
9. Schratt GM, Nigh EA, Chen WG, Hu L, Greenberg ME. BDNF regulates the translation of a select group of mRNAs by a mammalian target of rapamycin-phosphatidylinositol 3-kinase-dependent pathway during neuronal development. J Neurosci. 2004;24:7366-7377.
10. Gong R, Park CS, Abbassi NR, Tang SJ. Roles of glutamate receptors and the mammalian target of rapamycin (mTOR) signaling pathway in activity-dependent dendritic protein synthesis in hippocampal neurons. J Biol Chem. 2006;281:18802-18815.
11. Lee CC, Huang CC, Wu MY, Hsu KS. Insulin stimulates postsynaptic density-95 protein translation via the phosphoinositide 3-kinase-Akt-mammalian target of rapamycin signaling pathway. J Biol Chem. 2005;280:18543-18550.
12. Burnett PE, Barrow RK, Cohen NA, Snyder SH, Sabatini DM. RAFT1 phosphorylation of the translational regulators p70 S6 kinase and 4E-BP1. Proc Natl Acad Sci U S A. 1998;95:1432-1437.
13. Meyuhas O. Physiological roles of ribosomal protein S6: one of its kind. Int Rev Cell Mol Biol. 2008;268:1-37.
14. Ferrari S, Thomas G. S6 phosphorylation and the p70s6k/p85s6k. Crit Rev Biochem Mol Biol. 1994;29:385-413.
15. Banko JL, Poulin F, Hou L, De Maria CT, Sonenberg N, Klann E. The translation repressor 4E-BP2 is critical for eIF4F complex formation, synaptic plasticity, and memory in the hippocampus. J Neurosci. 2005;25:9581-9590.
16. Costa-Mattioli M, Sossin WS, Klann E, Sonenberg N. Translational control of long-lasting synaptic plasticity and memory. Neuron. 2009;61:10-26.
17. Hoeffer CA, Klann E. mTOR signaling: at the crossroads of plasticity, memory and disease. Trends Neurosci. 2010;33:67-75.
18. Dash PK, Orsi SA, Moore AN. Spatial memory formation and memory-enhancing effect of glucose involves activation of the tuberous sclerosis complex-Mammalian target of rapamycin pathway. J Neurosci. 2006;26:8048-8056.
19. Hoeffer CA, Tang W, Wong H, et al. Removal of FKBP12 enhances mTOR-Raptor interactions, LTP, memory, and perseverative/repetitive behavior. Neuron. 2008;60:832-845.
20. Winston D, Maimes, S. Adaptogens: Herbs for Strength, Stamina, and Stress. Rochester, VT: Healing Arts Press; 2007.
21. Liu CX, Xiao PG. Recent advances on ginseng research in China. J Ethnopharmacol. 1992;36:27-38.
22. Radad K, Gille G, Moldzio R, Saito H, Rausch WD. Ginsenosides Rb1 and Rg1 effects on mesencephalic dopaminergic cells stressed with glutamate. Brain Res. 2004;1021:41-53.
23. Zhang JT, Chui DH, Chen CF, Liu GZ. The Chemistry, Metabolism and Biological Activities of Ginseng. Beijing, China: Chemical Industry Press; 2006.
24. Tohda C, Matsumoto N, Zou K, Meselhy MR, Komatsu K. Abeta (25-35)-induced memory impairment, axonal atrophy, and synaptic loss are ameliorated by M1, A metabolite of protopanaxadiol-type saponins. Neuropsychopharmacology. 2004;29:860-868.
25. Shi YQ, Huang TW, Chen LM, et al. Ginsenoside Rg1 attenuates amyloid-beta content, regulates PKA/CREB activity, and improves cognitive performance in SAMP8 mice. J Alzheimers Dis. 2010;19:977-989.
26. Zhao H, Li Q, Zhang Z, Pei X, Wang J, Li Y. Long-term ginsenoside consumption prevents memory loss in aged SAMP8 mice by decreasing oxidative stress and up-regulating the plasticity-related proteins in hippocampus. Brain Res. 2009;1256:111-122.
27. Fang F, Chen X, Huang T, Lue LF, Luddy JS, Yan SS. Multi-faced neuroprotective effects of Ginsenoside Rg1 in an Alzheimer mouse model. Biochim Biophys Acta. 2012;1822:286-292.
28. Sievenpiper JL, Arnason JT, Leiter LA, Vuksan V. Variable effects of American ginseng: a batch of American ginseng (Panax quinquefolius L.) with a depressed ginsenoside profile does not affect postprandial glycemia. Eur J Clin Nutr. 2003;57:243-248.
29. Um JY, Chung HS, Kim MS, et al. Molecular authentication of Panax ginseng species by RAPD analysis and PCR-RFLP. Biol Pharm Bull. 2001;24:872-875.
30. Reagan-Shaw S, Nihal M, Ahmad N. Dose translation from animal to human studies revisited. FASEB J. 2008;22:659-661.
31. Ohno M, Sametsky EA, Younkin LH, et al. BACE1 deficiency rescues memory deficits and cholinergic dysfunction in a mouse model of Alzheimer's disease. Neuron. 2004;41:27-33.
32. Kimura R, Devi L, Ohno M. Partial reduction of BACE1 improves synaptic plasticity, recent and remote memories in Alzheimer's disease transgenic mice. J Neurochem. 2010;113:248-261.
33. Ma MX, Chen YM, He J, Zeng T, Wang JH. Effects of morphine and its withdrawal on Y-maze spatial recognition memory in mice. Neuroscience. 2007;147:1059-1065.
34. Zhang J, He J, Chen YM, Wang JH, Ma YY. Morphine and propranolol co-administration impair consolidation of Y-maze spatial recognition memory. Brain Res. 2008;1230:150-157.
35. Vorhees CV, Williams MT. Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat Protoc. 2006;1:848-858.
36. Quick KL, Ali SS, Arch R, Xiong C, Wozniak D, Dugan LL. A carboxyfullerene SOD mimetic improves cognition and extends the lifespan of mice. Neurobiol Aging. 2008;29:117-128.
37. Ko KM, Chiu PY, Leung HY, et al. Long-term dietary supplementation with a yang-invigorating Chinese herbal formula increases lifespan and mitigates age-associated declines in mitochondrial antioxidant status and functional ability of various tissues in male and female C57BL/6J mice. Rejuvenation Res. 2010;13:168-171.
38. Turturro A, Duffy P, Hass B, Kodell R, Hart R. Survival characteristics and age-adjusted disease incidences in C57BL/6 mice fed a commonly used cereal-based diet modulated by dietary restriction. J Gerontol A Biol Sci Med Sci. 2002;57:B379-B389.
39. Lalonde R. The neurobiological basis of spontaneous alternation. Neurosci Biobehav Rev. 2002;26:91-104.
40. Hernandez-Nicaise ML. The nervous system of ctenophores. III. Ultrastructure of synapses. J Neurocytol. 1973;2:249-263.
41. Von Strauss E, Viitanen M, De Ronchi D, Winblad B, Fratiglioni L. Aging and the occurrence of dementia: findings from a populationbased cohort with a large sample of nonagenarians. Arch Neurol. 1999;56:587-592.
42. Corrada MM, Brookmeyer R, Berlau D, Paganini-Hill A, Kawas CH. Prevalence of dementia after age 90: results from the 90+ study. Neurology. 2008;71:337-343.
43. Yuan Y, Chen YP, Boyd-Kirkup J, Khaitovich P, Somel M. Accelerated aging-related transcriptome changes in the female prefrontal cortex. Aging Cell. 2012;11:894-901.
44. Benice TS, Rizk A, Kohama S, Pfankuch T, Raber J. Sex-differences in age-related cognitive decline in C57BL/6J mice associated with increased brain microtubule-associated protein 2 and synaptophysin immunoreactivity. Neuroscience. 2006;137:413-423.
45. Yu YF, Zhai F, Dai CF, Hu JJ. The relationship between age-related hearing loss and synaptic changes in the hippocampus of C57BL/6J mice. Exp Gerontol. 2011;46:716-722.
46. Adams MM, Shi L, Linville MC, et al. Caloric restriction and age affect synaptic proteins in hippocampal CA3 and spatial learning ability. Exp Neurol. 2008;211:141-149.
47. Fuentes-Santamaría V, Alvarado JC, Henkel CK, Brunso-Bechtold JK. Cochlear ablation in adult ferrets results in changes in insulin-like growth factor-1 and synaptophysin immunostaining in the cochlear nucleus. Neuroscience. 2007;148:1033-1047.
48. Südhof TC. The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature. 1995;375:645-653.
49. Lau GC, Saha S, Faris R, Russek SJ. Up-regulation of NMDAR1 subunit gene expression in cortical neurons via a PKA-dependent pathway. J Neurochem. 2004;88:564-575.
50. Béïque JC, Lin DT, Kang MG, Aizawa H, Takamiya K, Huganir RL. Synapse-specific regulation of AMPA receptor function by PSD-95. Proc Natl Acad Sci U S A. 2006;103:19535-19540.
51. Vickers CA, Stephens B, Bowen J, Arbuthnott GW, Grant SG, Ingham CA. Neurone specific regulation of dendritic spines in vivo by post synaptic density 95 protein (PSD-95). Brain Res. 2006;1090:89-98.
52. Migaud M, Charlesworth P, Dempster M, et al. Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature. 1998;396:433-439.
53. Tao-Cheng JH, Dosemeci A, Winters CA, Reese TS. Changes in the distribution of calcium calmodulin-dependent protein kinase II at the presynaptic bouton after depolarization. Brain Cell Biol. 2006;35:117-124.
54. Nielander HB, Onofri F, Valtorta F, et al. Phosphorylation of VAMP/synaptobrevin in synaptic vesicles by endogenous protein kinases. J Neurochem. 1995;65:1712-1720.
55. Park CS, Elgersma Y, Grant SG, Morrison JH. alpha-Isoform of calciumcalmodulin-dependent protein kinase II and postsynaptic density protein 95 differentially regulate synaptic expression of NR2A- and NR2B-containing N-methyl-d-aspartate receptors in hippocampus. Neuroscience. 2008;151:43-55.
56. Elgersma Y, Sweatt JD, Giese KP. Mouse genetic approaches to investigating calcium/calmodulin-dependent protein kinase II function in plasticity and cognition. J Neurosci. 2004;24:8410-8415.
57. Miller S, Yasuda M, Coats JK, Jones Y, Martone ME, Mayford M. Disruption of dendritic translation of CaMKIIalpha impairs stabilization of synaptic plasticity and memory consolidation. Neuron. 2002;36:507-519.
58. Klann E, Dever TE. Biochemical mechanisms for translational regulation in synaptic plasticity. Nat Rev Neurosci. 2004;5:931-942.
59. Guertin DA, Sabatini DM. An expanding role for mTOR in cancer. Trends Mol Med. 2005;11:353-361.
60. Tischmeyer W, Schicknick H, Kraus M, et al. Rapamycin-sensitive signalling in long-term consolidation of auditory cortex-dependent memory. Eur J Neurosci. 2003;18:942-950.
61. Parsons RG, Gafford GM, Helmstetter FJ. Translational control via the mammalian target of rapamycin pathway is critical for the formation and stability of long-term fear memory in amygdala neurons. J Neurosci. 2006;26:12977-12983.
62. Blundell J, Kouser M, Powell CM. Systemic inhibition of mammalian target of rapamycin inhibits fear memory reconsolidation. Neurobiol Learn Mem. 2008;90:28-35.
63. Schicknick H, Schott BH, Budinger E, et al. Dopaminergic modulation of auditory cortex-dependent memory consolidation through mTOR. Cereb Cortex. 2008;18:2646-2658.
64. Banko JL, Merhav M, Stern E, Sonenberg N, Rosenblum K, Klann E. Behavioral alterations in mice lacking the translation repressor 4E-BP2. Neurobiol Learn Mem. 2007;87:248-256.
65. Antion MD, Merhav M, Hoeffer CA, et al. Removal of S6K1 and S6K2 leads to divergent alterations in learning, memory, and synaptic plasticity. Learn Mem. 2008;15:29-38.
66. Stoica L, Zhu PJ, Huang W, Zhou H, Kozma SC, Costa-Mattioli M. Selective pharmacogenetic inhibition of mammalian target of Rapamycin complex I (mTORC1) blocks long-term synaptic plasticity and memory storage. Proc Natl Acad Sci U S A. 2011;108:3791-3796.
67. Fortress AM, Fan L, Orr PT, Zhao Z, Frick KM. Estradiol-induced object recognition memory consolidation is dependent on activation of mTOR signaling in the dorsal hippocampus. Learn Mem. 2013;20:147-155.
68. Orr PT, Rubin AJ, Fan L, Kent BA, Frick KM. The progesteroneinduced enhancement of object recognition memory consolidation involves activation of the extracellular signal-regulated kinase (ERK) and mammalian target of rapamycin (mTOR) pathways in the dorsal hippocampus. Horm Behav. 2012;61:487-495.
69. Toescu EC. Normal brain ageing: models and mechanisms. Philos Trans R Soc Lond B Biol Sci. 2005;360:2347-2354.
70. Deak F, Sonntag WE. Aging, synaptic dysfunction, and insulin-like growth factor (IGF)-1. J Gerontol A Biol Sci Med Sci. 2012;67:611-625.
71. Deli A, Schipany K, Rosner M, et al. Blocking mTORC1 activity by rapamycin leads to impairment of spatial memory retrieval but not acquisition in C57BL/6J mice. Behav Brain Res. 2012;229:320-324.
72. Ma T, Hoeffer CA, Capetillo-Zarate E, et al. Dysregulation of the mTOR pathway mediates impairment of synaptic plasticity in a mouse model of Alzheimer's disease. PLoS One. 2010;5:e12845.
73. Caccamo A, Majumder S, Richardson A, Strong R, Oddo S. Molecular interplay between mammalian target of rapamycin (mTOR), amyloidbeta, and Tau: effects on cognitive impairments. J Biol Chem. 2010;285:13107-13120.
74. Spilman P, Podlutskaya N, Hart MJ, et al. Inhibition of mTOR by rapamycin abolishes cognitive deficits and reduces amyloid-beta levels in a mouse model of Alzheimer's disease. PLoS One. 2010;5:e9979.
75. Webb JL, Ravikumar B, Atkins J, Skepper JN, Rubinsztein DC. Alpha-Synuclein is degraded by both autophagy and the proteasome. J Biol Chem. 2003;278:25009-25013.
76. Pan T, Rawal P, Wu Y, et al. Rapamycin protects against rotenoneinduced apoptosis through autophagy induction. Neuroscience. 2009;164:541-551.
77. Majumder S, Caccamo A, Medina DX, et al. Lifelong rapamycin administration ameliorates age-dependent cognitive deficits by reducing IL-1β and enhancing NMDA signaling. Aging Cell. 2012;11:326-335.
78. Halloran J, Hussong SA, Burbank R, et al. Chronic inhibition of mammalian target of rapamycin by rapamycin modulates cognitive and non-cognitive components of behavior throughout lifespan in mice. Neuroscience. 2012;223:102-113.
79. Kim DH, Sarbassov DD, Ali SM, et al. mTOR interacts with raptor to form a nutrient-sensitive complex that signals to the cell growth machinery. Cell. 2002;110:163-175.