Ginsenoside Rg1 promotes nonamyloidgenic cleavage of APP via estrogen receptor signaling to MAPK/ERK and PI3K/Akt

Biochimica et Biophysica Acta - General Subjects

Volumn 1820, Issue 4, 2012, Pages 453-460

  Shi, Chun ^a,b   Zheng, Dong Dan ^c   Fang, Li ^c   Wu, Fengming ^d   Kwong, Wing Hang ^b   Xu, Jie ^d  

^a GUANGZHOU MEDICAL UNIVERSITY   (China)

^b CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^c SUN YAT SEN UNIVERSITY   (China)

^d SUN YAT SEN UNIVERSITY   (China)

Author keywords

Amyloid precursor protein; Estrogen receptor; Extracellular Signal Regulated Kinase Mitogen Activated Protein Kinase; Ginsenoside Rg1

Indexed keywords

ALPHA SECRETASE; AMYLOID PRECURSOR PROTEIN; AMYLOID PRECURSOR PROTEIN ALPHA; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; GINSENOSIDE RG 1; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN KINASE C; PROTEIN PRECURSOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVITY; ESTROGEN ACTIVITY; FEMALE; HIPPOCAMPUS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LEARNING; MEMORY; NONHUMAN; POSTMENOPAUSE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN CONTENT; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; RAT; RECEPTOR AFFINITY; SIGNAL TRANSDUCTION;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; CELL LINE, TUMOR; CENTRAL NERVOUS SYSTEM AGENTS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; GINSENOSIDES; HUMANS; MAP KINASE SIGNALING SYSTEM; MEMORY; MICE; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RANDOM ALLOCATION; RATS; RATS, WISTAR; RECEPTORS, ESTROGEN; SERUM AMYLOID A PROTEIN; SIGNAL TRANSDUCTION;

PANAX GINSENG; RATTUS;

EID: 84862806592     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2011.12.005     Document Type: Article

References (64)

1. A. Paganini-Hill, and V.W. Henderson Estrogen deficiency and risk of Alzheimer's disease in women Am. J. Epidemiol. 140 1994 256 261 (Pubitemid 24231911)
2. P.P. Zandi, M.C. Carlson, B.L. Plassman, K.A. Welsh-Bohmer, L.S. Mayer, D.C. Steffens, J.C.S. Breitner, and for the Cache County Memory Study Investigators Hormone replacement therapy and incidence of Alzheimer disease in older women. The Cache County study JAMA 288 2002 2123 2129 (Pubitemid 35265379)
3. J.E. Rossouw, G.L. Anderson, R.L. Prentice, A.Z. LaCroix, C. Kooperberg, M.L. Stefanick, R.D. Jackson, S.A. Beresford, B.V. Howard, K.C. Johnson, J.M. Kotchen, J. Ockene Writing Group for the Women's Health Initiative Investigators Risks and benefits of estrogen plus progestin in healthy postmenopausal women, principal results from the Women's Health Initiative randomized controlled trial JAMA 288 2002 321 333 (Pubitemid 34761611)
4. V. Beral Million Women Study Collaborators Breast cancer and hormone-replacement therapy in the Million Women Study Lancet 362 2003 419 427 (Pubitemid 36999703)
5. Practice Committee of American Society for reproductive medicine estrogen and progestogen therapy in postmenopausal women Fertil. Steril. 90 2008 S88 S102
6. R.Y. Chan, W.F. Chen, A. Dong, D. Guo, and M.S. Wong Estrogen-like activity of ginsenoside Rg1 derived from Panax notoginseng J. Clin. Endocrinol. Metab. 87 2002 3691 3695 (Pubitemid 34879514)
7. X.Z. Lu, J.H. Wang, X. Wu, L. Zhou, L. Wang, X.W. Zhang, K.J. Cao, and J. Huang Ginsenoside Rg1 promotes bone marrow stromal cells proliferation via the activation of the estrogen receptor-mediated signaling pathway Acta Pharmacol. Sin. 29 2008 1209 1214
8. M.K. Ang-Lee, J. Moss, and C.S. Yuan Herbal medicines and perioperative care JAMA 286 2001 208 216 (Pubitemid 32640852)
9. J.G. Toplissk, A.M. Clark, E. Ernst, C.D. Hufford, G.A.R. Johnston, J.M. Rimoldi, and B.J. Weimann Natural and synthetic substances related to human health Pure Appl. Chem. 74 2002 1957 1985
10. D.W. Brann, L.B. Hendry, and V.B. Mahesh Emerging diversities in the mechanism of action of steroid hormones J. Steroid Biochem. Mol. Biol. 52 1995 113 133
11. A.S. Attele, J.A. Wu, and C.S. Yuan Ginseng pharmacology, multiple constituents and multiple actions Biochem. Pharmacol. 58 1999 1685 1693 (Pubitemid 29505408)
12. S.W. Chen, X.H. Li, K.H. Ye, Z.F. Jiang, and X.D. Ren Total saponins of Panax notoginseng protected rabbit iliac artery against balloon endothelial denudation injury Acta Pharmacol. Sin. 25 2004 1151 1156
13. F. Chen, E.A. Eckman, and C.B. Eckman Reductions in levels of the Alzheimer's amyloid β peptide after oral administration of ginsenosides FASEB J. 20 2006 1269 1271
14. R. Punnonen, and A. Lukola Oestrogen-like effect of ginseng Br. Med. J. 281 1980 1110 (Pubitemid 10021420)
15. R.B. Duda, B. Taback, B. Kessel, D.D. Dooley, H. Yang, J. Marchiori, B.M. Slomovic, and J.G. Alvarez pS2 expression induced by American ginseng in MCF-7 breast cancer cells Ann. Surg. Oncol. 3 1996 515 520 (Pubitemid 126728999)
16. J. Liu, L. Li, and W.Z. Suo HT22 hippocampal neuronal cell line possesses functional cholinergic properties Life Sci. 84 2009 267 271
17. P. Amato, S. Christophe, and P.L. Mellon Estrogenic activity of herbs commonly used as remedies for menopausal symptoms Menopause 9 2002 145 150 (Pubitemid 34194110)
18. X.M. Cui, Z.J. Chen, C.L. Wang, and J. Zeng Studies on saponin accumulative in regularities Panax notoginseng (Burk) F. H. Chen Zhongguo Zhong Yao Za Zhi 26 2001 24 25
19. Y. Lee, Y. Jin, W. Lim, S. Ji, S. Choi, S. Jang, and S. Lee A ginsenoside-Rh1, a component of ginseng saponin, activates estrogen receptor in human breast carcinoma MCF-7 cells J. Steroid Biochem. Mol. Biol. 84 2003 463 468 (Pubitemid 36555768)
20. Q.G. Gao, W.F. Chen, J.X. Xie, and M.S. Wong Ginsenoside Rg1 protects against 6-OHDA-induced neurotoxicity in neuroblastoma SK-N-SH cells via IGF-I receptor and estrogen receptor pathways J. Neurochem. 109 2009 1338 1347
21. W.S. Lau, W.F. Chen, R.Y. Chan, D.A. Guo, and M.S. Wong Mitogen-activated protein kinase (MAPK) pathway mediates the oestrogen-like activities of ginsenoside Rg1 in human breast cancer (MCF-7) cells Br. J. Pharmacol. 156 2009 1136 1146
22. Y.S. Gong, J. Chen, Q.Z. Zhang, and J.T. Zhang Effect of 17beta-oestradiol and ginsenoside on osteoporosis in ovariectomised rats J. Asian Nat. Prod. Res. 8 2006 649 656 (Pubitemid 44884805)
23. Y. Cheng, L.H. Shen, and J.T. Zhang Anti-amnestic and anti-aging effects of ginsenoside Rg1 and Rb1 and its mechanism of action Acta Pharmacol. Sin. 26 2005 143 149 (Pubitemid 40203956)
24. S. Goodenough, M. Schäfer, and C. Behl Estrogen-induced cell signaling in a cellular model of Alzheimer's disease J. Steroid Biochem. Mol. Biol. 84 2003 301 305 (Pubitemid 36514845)
25. J.W. Fernandez, K. Rezai-Zadeh, D. Obregon, and J. Tan EGCG functions through estrogen receptor-mediated activation of ADAM10 in the promotion of non-amyloidogenic processing of APP FEBS Lett. 584 2010 4259 4267
26. L.C. Yang, Q.G. Zhang, C.F. Zhou, F. Yang, Y.D. Zhang, R.M. Wang, and D.W. Brann Extranuclear estrogen receptors mediate the neuroprotective effects of estrogen in the rat hippocampus PLoS One 5 2010 e9851
27. D. Gabuzda, J. Busciglio, and B.A. Yankner Inhibition of β-amyloid production by activation of protein kinase J. Neurochem. 61 1993 2326 2329
28. S.W. Yeon, M.W. Jung, M.J. Ha, S.U. Kim, K. Huh, M.J. Savage, E. Masliah, and I. Mook-Jung Blockade of PKC epsilon activation attenuates phorbol ester-induced increase of alpha-secretase-derived secreted form of amyloid precursor protein Biochem. Biophys. Res. Commun. 280 2001 782 787 (Pubitemid 32924498)
29. G. Zhu, D. Wang, Y.H. Lin, T. McMahon, E.H. Koo, and R.O. Messing Protein kinase C epsilon suppresses Aβ production and promotes activation of α-secretase Biochem. Biophys. Res. Commun. 285 2001 997 1006 (Pubitemid 32918036)
30. J. Desdouits-Magnen, F. Desdouits, S. Takeda, L.J. Syu, A.R. Saltiel, J.D. Buxbaum, A.J. Czernik, A.C. Nairn, and P. Greengard Regulation of secretion of Alzheimer amyloid precursor protein by the mitogen-activated protein kinase cascade J. Neurochem. 70 1998 524 530 (Pubitemid 28079341)
31. J. Mills, D. Laurent Charest, F. Lam, K. Beyreuther, N. Ida, S.L. Pelech, and P.B. Reiner Regulation of amyloid precursor protein catabolism involves the mitogen-activated protein kinase signal transduction J. Neurosci. 17 1997 9415 9422 (Pubitemid 28006386)
32. S.S. Petanceska, and S. Gandy The phosphatidylinositol 3-kinase inhibitor wortmannin alters the metabolism of the Alzheimer's amyloid precursor J. Neurochem. 73 1999 2316 2320
33. D.C. Solano, M. Sironi, C. Bonfini, S.B. Solerte, S. Govoni, and M. Racchi Insulin regulates soluble amyloid precursor protein release via phosphatidyl inositol 3 kinase-dependent pathway FASEB J. 14 2000 1015 1022 (Pubitemid 30241680)
34. W.S. Lau, R.Y. Chan, D.A. Guo, and M.S. Wong Ginsenoside Rg1 exerts estrogen-like activities via ligand-independent activation of ERalpha pathway J. Steroid Biochem. Mol. Biol. 108 2008 64 71 (Pubitemid 351173825)
35. J.A. Johnston, D.K. Ferris, J.M. Wang, D.L. Longo, J.J. Oppenheim, and D.J. Kelvin Staurosporine restores signaling and inhibits interleukin-8-induced chemotactic desensitization Eur. J. Immunol. 24 1994 2556 2562 (Pubitemid 24303107)
36. C. Shi, F. Wu, D.T. Yew, J. Xu, and Y. Zhu Bilobalide prevents apoptosis through activation of the PI3K/Akt pathway in SH-SY5Y cells Apoptosis 15 2010 715 727
37. H. Zhang, Y. Gao, Z. Dai, T. Meng, S. Tu, and Y. Yan IGF-1 reduces BACE-1 expression in PC12 cells via activation of PI3-K/Akt and MAPK/ERK1/2 signaling pathways Neurochem. Res. 36 2011 49 57
38. J. Xu, J. Zhu, C. Shi, K. Guo, and D.T. Yew Effects of genistein on hippocampal neurodegeneration of ovariectomized rats J. Mol. Neurosci. 31 2007 101 112 (Pubitemid 46742294)
39. G.M. Morris Developments of a water maze procedure for studying spatial learning in the rat J. Neurosci. Methods 11 1984 47 60
40. D. Li, J. Wang, D.T. Yew, E. Lucy Forster, and Z. Yao Age-related alterations of Nestin-immunoreactive neurons in rat basal forebrain with aged memory deficit Neurochem. Int. 53 2008 270-177
41. S. Kato, H. Endoh, Y. Masuhiro, T. Kitamoto, S. Uchiyama, H. Sasaki, S. Masushige, Y. Gotoh, E. Nishida, H. Kawashima, D. Metzger, and P. Chambon Activation of the estrogen receptor through phosphorylation by mitogen-activated protein kinase Science 270 1995 1491 1494
42. T. Sato, T. Teramoto, K. Tanaka, Y. Ohnishi, M. Irifune, and T. Nishikawa Effects of ovariectomy and calcium deficiency on learning and memory of eight-arm radial maze in middle-aged female rats Behav. Brain Res. 142 2003 207 216 (Pubitemid 36677606)
43. Z. Feng, and J.T. Zhang Long-term melatonin or 17beta-estradiol supplementation alleviates oxidative stress in ovariectomized adult rats Free Radic. Biol. Med. 39 2005 195 204 (Pubitemid 40814545)
44. V.N. Luine, S.T. Richards, V.Y. Wu, and K.D. Beck Estradiol enhances learning and memory in a spatial memory task and effects levels of monoaminergic neurotransmitters Horm. Behav. 34 1998 149 162 (Pubitemid 28541756)
45. S.S. Petanceska, V. Nagy, D. Frail, and S. Gandy Ovariectomy and 17beta-estradiol modulate the levels of Alzheimer's amyloid beta peptides in brain Exp. Gerontol. 35 2000 1317 1325
46. J.A. Levin-Allerhand, and J.D. Smith Ovariectomy of young mutant amyloid precursor protein transgenic mice leads to increased mortality J. Mol. Neurosci. 19 2002 163 166 (Pubitemid 35013350)
47. N. Izumo, Y. Ishibashi, M. Ohba, T. Morikawa, and T. Manabe Decreased voluntary activity and amygdala levels of serotonin and dopamine in ovariectomized rats Behav. Brain Res. 227 2011 1 6
48. R.X. Song, R.J. Santen, R. Kumar, L. Adam, M.H. Jeng, S. Masamura, and W. Yue Adaptive mechanisms induced by long-term estrogen deprivation in breast cancer cells Mol. Cell. Endocrinol. 193 2002 29 42 (Pubitemid 34823605)
49. T.A. Roepke, O.K. Ronnekleiv, and M.J. Kelly Physiological consequences of membrane-initiated estrogen signaling in the brain Front. Biosci. 16 2011 1560 1573
50. L. Crews, and E. Masliah Molecular mechanisms of neurodegeneration in Alzheimer's disease Hum. Mol. Genet. 19 2010 R12 R20
51. R. Li, Y. Shen, L.B. Yang, L.F. Lue, C. Finch, and J. Rogers Estrogen enhances uptake of amyloid beta-protein by microglia derived from the human cortex J. Neurochem. 75 2000 1447 1454
52. X. Yue, M. Lu, T. Lancaster, P. Cao, S. Honda, M. Staufenbiel, N. Harada, Z. Zhong, Y. Shen, and R. Li Brain estrogen deficiency accelerates Abeta plaque formation in an Alzheimer's disease animal model Proc. Natl. Acad. Sci. U. S. A. 102 2005 19198 19203 (Pubitemid 43049589)
53. D. Morgan Learning and memory deficits in APP transgenic mouse models of amyloid deposition Neurochem. Res. 28 2003 1029 1034 (Pubitemid 36576199)
54. H. Zheng, H. Xu, S.N. Uljon, R. Gross, K. Hardy, J. Gaynor, J. LaFrancois, J. Simpkins, L.M. Refolo, S. Petanceska, R. Wang, and K. Duff Modulation of A(beta) peptides by estrogen in mouse models J. Neurochem. 80 2002 191 196 (Pubitemid 34614591)
55. J. Hardy, and D.J. Selkoe The amyloid hypothesis of Alzheimer's disease, progress and problems on the road to therapeutics Science 297 2002 353 356 (Pubitemid 34790756)
56. K. Rezai-Zadeh, D. Shytle, N. Sun, T. Mori, H. Hou, D. Jeanniton, J. Ehrhart, K. Townsend, J. Zeng, D. Morgan, J. Hardy, T. Town, and J. Tan Green tea epigallocatechin-3-gallate (EGCG) modulates amyloid precursor protein cleavage and reduces cerebral amyloidosis in Alzheimer transgenic mice J. Neurosci. 25 2005 8807 8814 (Pubitemid 41362059)
57. M.P. Mattson Cellular actions of beta-amyloid precursor protein and its soluble and fibrillogenic derivatives Physiol. Rev. 77 1997 1081-1032
58. B. De Strooper, and W. Annaert Proteolytic processing and cell biological functions of the amyloid precursor protein J. Cell Sci. 113 2000 1857 1870 (Pubitemid 30386490)
59. S. Mandel, T. Amit, L. Reznichenko, O. Weinreb, and M.B. Youdim Green tea catechins as brain-permeable, natural iron chelators-antioxidants for the treatment of neurodegenerative disorders Mol. Nutr. Food Res. 50 2006 229 234 (Pubitemid 43325663)
60. T. Odani, H. Tanizawa, and Y. Takino Studies on the absorption, distribution, excretion and metabolism of ginseng saponins. II. The absorption, distribution and excretion of ginsenoside Rg1 in the rat Chem. Pharm. Bull (Tokyo) 31 1983 292 298 (Pubitemid 13122244)
61. R. Wang, Y.N. Li, G.J. Wang, H.P. Hao, X.L. Wu, and F. Zhou Neuroprotective effects and brain transport of ginsenoside Rg1 Chin. J. Nat. Med. 7 2009 315 320
62. A.C. Wilson, L. Clemente, T. Liu, R.L. Bowen, S.V. Meethal, and C.S. Atwood Reproductive hormones regulate the selective permeability of the blood-brain barrier Biochim. Biophys. Acta 1782 2008 401 417
63. M.J. Cipolla, J.A. Godfrey, and M.J. Wiegman The effect of ovariectomy and estrogen on penetrating brain arterioles and blood-brain barrier permeability Microcirculation 9 2009 1 10
64. S. Bake, J.A. Friedman, and F. Sohrabji Reproductive age-related changes in the blood brain barrier: expression of IgG and tight junction proteins Microvasc. Res. 78 2009 413 424