Ginsenoside Rg1 attenuates amyloid-β content, regulates PKA/CREB activity, and improves cognitive performance in SAMP8 mice

Journal of Alzheimer's Disease

Volumn 19, Issue 3, 2010, Pages 977-989

  Shi, Yan Qing ^a   Huang, Tian Wen ^a,b   Chen, Li Min ^a   Pan, Xiao Dong ^a,b   Zhang, Jing ^a   Zhu, Yuan Gui ^a,b   Chen, Xiao Chun ^a,b  

^a BEIJING HOSPITAL   (China)

^b FUJIAN MEDICAL UNIVERSITY   (China)

Author keywords

Alzheimer's disease; Amyloid ; CREB; Ginsenoside Rg1; PKA; Senescence accelerated mouse prone8

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-40]; BRAIN DERIVED NEUROTROPHIC FACTOR; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE REGULATORY SUBUNIT IIALPHA; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GINSENOSIDE RG 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHEMICAL STRUCTURE; COGNITION; CONTROLLED STUDY; HIPPOCAMPUS; LEARNING DISORDER; MALE; MEMORY; MEMORY DISORDER; MOUSE; NEUROPATHOLOGY; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SENESCENCE ACCELERATED MOUSE;

EID: 77149166322     PISSN: 13872877     EISSN: None     Source Type: Journal    
DOI: 10.3233/JAD-2010-1296     Document Type: Article

References (64)

1. Gong Y, Chang L, Viola KL, Lacor PN, Lambert MP, Finch CE, Krafft GA, KleinWL(2003) Alzheimer's disease-affected brain: presence of oligomeric A beta ligands (ADDLs) suggests a molecular basis for reversible memory loss. Proc Natl Acad Sci U S A 100, 10417-10422.
2. Lue LF, Kuo YM, Roher AE, Brachova L, Shen Y, Sue L, Beach T, Kurth JH, Rydel RE, Rogers J (1999) Soluble amyloid beta peptide concentration as a predictor of synaptic change in Alzheimer's disease. Am J Pathol 155, 853-862.
3. McLean CA, Cherny RA, Fraser FW, Fuller SJ, Smith MJ, Beyreuther K, Bush AI, Masters CL (1999) Soluble pool of Abeta amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann Neurol 46, 860-866.
4. Selkoe DJ (2002) Alzheimer's disease is a synaptic failure. Science 298, 789-791.
5. Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, Liosatos M, Morgan TE, Rozovsky I, Trommer B, Viola KL, Wals P, Zhang C, Finch CE, Krafft GA, Klein WL (1998) Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci U S A 95, 6448-6453.
6. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, Wolfe MS, Rowan MJ, Selkoe DJ (2002) Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416, 535-539.
7. Townsend M, Shankar GM, Mehta T, Walsh DM, Selkoe DJ (2006) Effects of secreted oligomers of amyloid beta-protein on hippocampal synaptic plasticity: a potent role for trimers. J Physiol 572, 477-492.
8. Vitolo OV, Sant'Angelo A, Costanzo V, Battaglia F, Arancio O, Shelanski M(2002) Amyloid beta-peptide inhibition of the PKA/CREB pathway and long-term potentiation: reversibility by drugs that enhance cAMP signaling. Proc Natl Acad Sci U S A 99, 13217-13221.
9. Josselyn SA, Shi C, Carlezon WA, Jr., Neve RL, Nestler EJ, Davis M (2001) Long-term memory is facilitated by cAMP response element-binding protein overexpression in the amygdala. J Neurosci 21, 2404-2412.
10. Viosca J, Lopez de Armentia M, Jancic D, Barco A (2009) Enhanced CREB-dependent gene expression increases the excitability of neurons in the basal amygdala and primes the consolidation of contextual and cued fear memory. Learn Mem 16, 193-197.
11. Ou LC, Gean PW (2007) Transcriptional regulation of brainderived neurotrophic factor in the amygdala during consolidation of fear memory. Mol Pharmacol 72, 350-358.
12. Korte M, Carroll P, Wolf E, Brem G, Thoenen H, Bonhoeffer T (1995) Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc Natl Acad Sci U S A 92, 8856-8860.
13. Messaoudi E, Ying SW, Kanhema T, Croll SD, Bramham CR (2002) Brain-derived neurotrophic factor triggers transcription-dependent, late phase long-term potentiation in vivo. J Neurosci 22, 7453-7461.
14. Pang PT, Teng HK, Zaitsev E, Woo NT, Sakata K, Zhen S, Teng KK, Yung WH, Hempstead BL, Lu B (2004) Cleavage of proBDNF by tPA/plasmin is essential for long-term hippocampal plasticity. Science 306, 487-491.
15. Mizuno M,Yamada K, Olariu A, Nawa H, NabeshimaT(2000) Involvement of brain-derived neurotrophic factor in spatial memory formation and maintenance in a radial arm maze test in rats. J Neurosci 20, 7116-7121.
16. Monfils MH, Cowansage KK, LeDoux JE (2007) Brainderived neurotrophic factor: linking fear learning to memory consolidation. Mol Pharmacol 72, 235-237.
17. Lee ST, Chu K, Sim JY, Heo JH, Kim M (2008) Panax ginseng enhances cognitive performance in Alzheimer disease. Alzheimer Dis Assoc Disord 22, 222-226.
18. Zhao H, Li Q, Zhang Z, Pei X, Wang J, Li Y (2009) Longterm ginsenoside consumption prevents memory loss in aged SAMP8 mice by decreasing oxidative stress and up-regulating the plasticity-related proteins in hippocampus. Brain Res 1256, 111-122.
19. Chen XC, Chen LM, Zhu YG, Fang F, Zhou YC, Zhao CH (2003) Involvement of CDK4, pRB, and E2F1 in ginsenoside Rg1 protecting rat cortical neurons from beta-amyloidinduced apoptosis. Acta Pharmacol Sin 24, 1259-1264.
20. Flood JF, Morley JE (1993) Age-related changes in footshock avoidance acquisition and retention in senescence accelerated mouse (SAM). Neurobiol Aging 14, 153-157.
21. Ohta A, Akiguchi I, Seriu N, Ohnishi K, Yagi H, Higuchi K, Hosokawa M(2001) Deterioration in learning and memory of fear conditioning in response to context in aged SAMP8 mice. Neurobiol Aging 22, 479-484.
22. Ohta A, Akiguchi I, Seriu N, Ohnishi K, Yagi H, Higuchi K, Hosokawa M(2002) Deterioration in learning and memory of inferential tasks for evaluation of transitivity and symmetry in aged SAMP8 mice. Hippocampus 12, 803-810.
23. Takemura M, Nakamura S, Akiguchi I, Ueno M, Oka N, Ishikawa S, Shimada A, Kimura J, Takeda T (1993) Beta/A4 proteinlike immunoreactive granular structures in the brain of senescence-accelerated mouse. Am J Pathol 142, 1887-1897.
24. Yang S, Qiao H, Wen L, Zhou W, Zhang Y (2005) D-serine enhances impaired long-term potentiation in CA1 subfield of hippocampal slices from aged senescence-accelerated mouse prone/8. Neurosci Lett 379, 7-12.
25. Tomobe K, Okuma Y, Nomura Y (2007) Impairment of CREB phosphorylation in the hippocampal CA1 region of the senescence-accelerated mouse (SAM) P8. Brain Res 1141, 214-217.
26. Morley JE, Kumar VB, Bernardo AE, Farr SA, Uezu K, Tumosa N, Flood JF (2000) Beta-amyloid precursor polypeptide in SAMP8 mice affects learning and memory. Peptides 21, 1761-1767.
27. Kawarabayashi T, Younkin LH, Saido TC, Shoji M, Ashe KH, Younkin SG (2001) Age-dependent changes in brain, CSF, and plasma amyloid (beta) protein in the Tg2576 transgenic mouse model of Alzheimer's disease. J Neurosci 21, 372-381.
28. Taubenfeld SM, Wiig KA, Monti B, Dolan B, Pollonini G, Alberini CM (2001) Fornix-dependent induction of hippocampal CCAAT enhancer-binding protein [beta] and [delta] Co-localizes with phosphorylated cAMP response elementbinding protein and accompanies long-term memory consolidation. J Neurosci 21, 84-91.
29. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248-254.
30. Kato A, Fukunari A, Sakai Y, Nakajima T (1997) Prevention of amyloid-like deposition by a selective prolyl endopeptidase inhibitor, Y-29794, in senescence-accelerated mouse. J Pharmacol Exp Ther 283, 328-335.
31. Lu B (2003) BDNF and activity-dependent synaptic modulation. Learn Mem 10, 86-98.
32. Poo MM (2001) Neurotrophins as synaptic modulators. Nat Rev Neurosci 2, 24-32.
33. Pallas M, Camins A, Smith MA, Perry G, Lee HG, Casadesus G (2008) From aging to Alzheimer's disease: unveiling "the switch" with the senescence-accelerated mouse model (SAMP8). J Alzheimers Dis 15, 615-624.
34. Qi D, Zhu Y, Wen L, Liu Q, Qiao H (2009) Ginsenoside Rg1 restores the impairment of learning induced by chronic morphine administration in rats. J Psychopharmacol 23, 74-83.
35. WangXY, Chen J, Zhang JT (2001) [Effect of ginsenoside Rg1 on learning and memory impairment induced by beta-amyloid peptide(25-35) and its mechanism of action]. Yao Xue Xue Bao 36, 1-4.
36. Yamaguchi Y, Higashi M, Kobayashi H (1997) Effects of ginsenosides on maze performance and brain choline acetyltransferase activity in scopolamine-treated young rats and aged rats. Eur J Pharmacol 329, 37-41.
37. Chen F, Eckman EA, Eckman CB (2006) Reductions in levels of the Alzheimer's amyloid beta peptide after oral administration of ginsenosides. FASEB J 20, 1269-1271.
38. Wei C, Jia J, Liang P, Guan Y (2008) Ginsenoside Rg1 attenuates beta-amyloid-induced apoptosis in mutant PS1 M146L cells. Neurosci Lett 443, 145-149.
39. Lue LF, Brachova L, Civin WH, Rogers J (1996) Inflammation, A beta deposition, and neurofibrillary tangle formation as correlates of Alzheimer's disease neurodegeneration. J Neuropathol Exp Neurol 55, 1083-1088.
40. Meyer CJ, Alenghat FJ, Rim P, Fong JH, Fabry B, Ingber DE (2000) Mechanical control of cyclic AMP signalling and gene transcription through integrins. Nat Cell Biol 2, 666-668.
41. Abel T, Nguyen PV, Barad M, Deuel TA, Kandel ER, Bourtchouladze R (1997) Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based longterm memory. Cell 88, 615-626.
42. Fourcaudot E, Gambino F, Humeau Y, Casassus G, Shaban H, Poulain B, Luthi A (2008) cAMP/PKA signaling and RIM1alpha mediate presynaptic LTP in the lateral amygdala. Proc Natl Acad Sci U S A 105, 15130-15135.
43. Nayak A, Zastrow DJ, Lickteig R, Zahniser NR, Browning MD(1998) Maintenance of late-phase LTP is accompanied by PKA-dependent increase in AMPA receptor synthesis. Nature 394, 680-683.
44. Huang YY, Kandel ER, Varshavsky L, Brandon EP, Qi M, Idzerda RL, McKnight GS, Bourtchouladze R (1995) A genetic test of the effects of mutations in PKA on mossy fiber LTP and its relation to spatial and contextual learning. Cell 83, 1211-1222.
45. Goosens KA, Holt W, Maren S (2000) A role for amygdaloid PKA and PKC in the acquisition of long-term conditional fear memories in rats. Behav Brain Res 114, 145-152.
46. Michel M, Kemenes I, Muller U, Kemenes G (2008) Different phases of long-term memory require distinct temporal patterns of PKA activity after single-trial classical conditioning. Learn Mem 15, 694-702.
47. Kobierski LA,Wong AE, Srivastava S, Borsook D, Hyman SE (1999) Cyclic AMP-dependent activation of the proenkephalin gene requires phosphorylation of CREB at serine-133 and a Src-related kinase. J Neurochem 73, 129-138.
48. Gonzalez GA, Montminy MR (1989) Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell 59, 675-680.
49. Cadd G, McKnight GS (1989) Distinct patterns of cAMPdependent protein kinase gene expression in mouse brain. Neuron 3, 71-79.
50. Ventra C, Porcellini A, Feliciello A, Gallo A, Paolillo M, Mele E, Avvedimento VE, Schettini G (1996) The differential response of protein kinase A to cyclic AMP in discrete brain areas correlates with the abundance of regulatory subunit II. J Neurochem 66, 1752-1761.
51. Nomura Y, Kitamura Y, Ohnuki T, Arima T, Yamanaka Y, Sasaki K, Oomura Y (1997) Alterations in acetylcholine, NMDA, benzodiazepine receptors and protein kinase Cin the brain of the senescence-accelerated mouse: an animal model useful for studies on cognitive enhancers. Behav Brain Res 83, 51-55.
52. Hung MC, Shibasaki K, Yoshida R, Sato M, Imaizumi K (2001) Learning behaviour and cerebral protein kinase C, antioxidant status, lipid composition in senescence-accelerated mouse: influence of a phosphatidylcholine-vitamin B12 diet. Br J Nutr 86, 163-171.
53. Roberson ED, English JD, Adams JP, Selcher JC, Kondratick C, Sweatt JD (1999) The mitogen-activated protein kinase cascade couples PKA and PKC to cAMP response element binding protein phosphorylation in area CA1 of hippocampus. J Neurosci 19, 4337-4348.
54. Mayr B, MontminyM(2001) Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat Rev Mol Cell Biol 2, 599-609.
55. Lonze BE, Ginty DD (2002) Function and regulation of CREB family transcription factors in the nervous system. Neuron 35, 605-623.
56. Wang QW, Rowan MJ, Anwyl R (2009) Inhibition of LTP by beta-amyloid is prevented by activation of beta2 adrenoceptors and stimulation of the cAMP/PKA signalling pathway. Neurobiol Aging 30, 1608-1613.
57. Bekinschtein P, Cammarota M, Igaz LM, Bevilaqua LR, Izquierdo I, Medina JH (2007) Persistence of long-term memory storage requires a late protein synthesis- and BDNF- dependent phase in the hippocampus. Neuron 53, 261-277.
58. Tokuyama W, Okuno H, Hashimoto T, Xin Li Y, Miyashita Y (2000) BDNF upregulation during declarative memory formation in monkey inferior temporal cortex. Nat Neurosci 3, 1134-1142.
59. Hall J, Thomas KL, Everitt BJ (2000) Rapid and selective induction of BDNF expression in the hippocampus during contextual learning. Nat Neurosci 3, 533-535.
60. Kesslak JP, So V, Choi J, Cotman CW, Gomez-Pinilla F (1998) Learning upregulates brain-derived neurotrophic factor messenger ribonucleic acid: a mechanism to facilitate encoding and circuit maintenance? Behav Neurosci 112, 1012-1019.
61. Ou LC, Gean PW (2006) Regulation of amygdala-dependent learning by brain-derived neurotrophic factor is mediated by extracellular signal-regulated kinase and phosphatidylinositol- 3-kinase. Neuropsychopharmacology 31, 287-296.
62. Rattiner LM, Davis M, French CT, Ressler KJ (2004) Brainderived neurotrophic factor and tyrosine kinase receptor B involvement in amygdala-dependent fear conditioning. J Neurosci 24, 4796-4806.
63. Kaisho Y, Miyamoto M, Shiho O, Onoue H, Kitamura Y, Nomura S (1994) Expression of neurotrophin genes in the brain of senescence-accelerated mouse (SAM) during postnatal development. Brain Res 647, 139-144.
64. West AE, Chen WG, Dalva MB, Dolmetsch RE, Kornhauser JM, Shaywitz AJ, Takasu MA, Tao X, Greenberg ME (2001) Calcium regulation of neuronal gene expression. Proc Natl Acad Sci U S A 98, 11024-11031.