EGb 761 enhances adult hippocampal neurogenesis and phosphorylation of CREB in transgenic mouse model of Alzheimer's disease

FASEB Journal

Volumn 21, Issue 10, 2007, Pages 2400-2408

  Tchantchou, Flaubert ^a   Xu, Yanan ^a   Wu, Yanjue ^a   Christen, Yves ^c   Luo, Yuan ^a,b  

^a UNIVERSITY OF MARYLAND SCHOOL OF PHARMACY   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c IPSEN   (France)

Author keywords

AD; Dementia; Memory; Neuronal cells

Indexed keywords

AMYLOID BETA PROTEIN; BROXURIDINE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GINKGO BILOBA EXTRACT;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DOSE RESPONSE; DRUG MECHANISM; HIPPOCAMPUS; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

AGING; ALZHEIMER DISEASE; ANIMALS; CELL DIVISION; COGNITION; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DISEASE MODELS, ANIMAL; GINKGO BILOBA; HIPPOCAMPUS; HUMANS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PHOSPHORYLATION; PLANT EXTRACTS; RECOMBINANT PROTEINS;

GINKGO BILOBA; MUS; MUS MUSCULUS;

EID: 34547824397     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.06-7649com     Document Type: Article

References (58)

1. Lacor, P. N., Buniel, M. C., Chang, L., Fernandez, S. J., Gong, Y., Viola, K. L., Lambert, M. P., Velasco, P. T., Bigio, E. H., Finch, C. E., et al. (2004) Synaptic targeting by Alzheimer's-related amyloid beta oligomers. J. Neurosci. 24, 10191-10200
2. Altman, J., and Das, G. D. (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J. Comp. Neurol. 124, 319-335
3. Gould, E., Tanapat, P., Hastings, N. B., and Shors, T. J. (1999) Neurogenesis in adulthood: a possible role in learning. Trends Cogn. Sci. 3, 186-192
4. Gage, F. H. (2000) Mammalian neural stem cells. Science 287, 1433-1438
5. Gross, C. G. (2000) Neurogenesis in the adult brain: death of a dogma. Nat. Rev. Neurosci. 1, 67-73
6. Brinton, R. D., and Wang, J. M. (2006) Therapeutic potential of neurogenesis for prevention and recovery from Alzheimer's disease: allopregnanolone as a proof of concept neurogenic agent. Curr. Alzheimer. Res. 3, 185-190
7. Lledo, P. M., Alonso, M., and Grubb, M. S. (2006) Adult neurogenesis and functional plasticity in neuronal circuits. Nat. Rev. Neurosci. 7, 179-193
8. Squire, L. R. (1992) Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol. Rev. 99, 195-231
9. Dusek, J. A., and Eichenbaum, H. (1997) The hippocampus and memory for orderly stimulus relations. Proc. Natl. Acad. Sci. U. S. A. 94, 7109-7114
10. Parent, J. M., Yu, T. W., Leibowitz, R. T., Geschwind, D. H., Sloviter, R. S., and Lowenstein, D. H. (1997) Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J. Neurosci. 17, 3727-3738
11. Tanapat, P., Hastings, N. B., Reeves, A. J., and Gould, E. (1999) Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J. Neurosci. 19, 5792-5801
12. Van Praag, H., Kempermann, G., and Gage, F. H. (2000) Neural consequences of environmental enrichment. Nat. Rev. Neurosci. 1, 191-198
13. Gage, F. H. (2002) Neurogenesis in the adult brain. J. Neurosci. 22, 612-613
14. Feng, R., Rampon, C., Tang, Y. P., Shrom, D., Jin, J., Kyin, M., Sopher, B., Miller, M. W., Ware, C. B., Martin, G. M., et al. (2001) Deficient neurogenesis in forebrain-specific presenilin-1 knockout mice is associated with reduced clearance of hippocampal memory traces. Neuron 32, 911-926
15. Haughey, N. J., Nath, A., Chan, S. L., Borchard, A. C., Rao, M. S., and Mattson, M. P. (2002) Disruption of neurogenesis by amyloid beta-peptide, and perturbed neural progenitor cell homeostasis, in models of Alzheimer's disease. J. Neurochem. 83, 1509-1524
16. Jin, K., Peel, A. L., Mao, X. O., Xie, L., Cottrell, B. A., Henshall, D. C., and Greenberg, D. A. (2004) Increased hippocampal neurogenesis in Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 101, 343-347
17. Jin, K., Galvan, V., Xie, L., Mao, X. O., Gorostiza, O. F., Bredesen, D. E., and Greenberg, D. A. (2004) Enhanced neurogenesis in Alzheimer's disease transgenic (PDGF-APPSw, Ind) mice. Proc. Natl. Acad. Sci. U. S. A. 101, 13363-13367
18. Donovan, M. H., Yazdani, U., Norris, R. D., Games, D., German, D. C., and Eisch, A. J. (2006) Decreased adult hippocampal neurogenesis in the PDAPP mouse model of Alzheimer's disease. J. Comp. Neurol. 495, 70-83
19. Zhu, D. Y., Lau, L., Liu, S. H., Wei, J. S., and Lu, Y. M. (2004) Activation of cAMP-response-element-binding protein (CREB) after focal cerebral ischemia stimulates neurogenesis in the adult dentate gyrus. Proc. Natl. Acad. Sci. U. S. A. 101, 9453-9457
20. Phillips, H. S., Hains, J. M., Armanini, M., Laramee, G. R., Johnson, S. A., and Winslow, J. W. (1991) BDNF mRNA is decreased in the hippocampus of individuals with Alzheimer's disease. Neuron 7, 695-702
21. Yamamoto-Sasaki, M., Ozawa, H., Saito, T., Rosler, M., and Riederer, P. (1999) Impaired phosphorylation of cyclic AMP response element binding protein in the hippocampus of dementia of the Alzheimer type. Brain Res. 824, 300-303
22. Bender, R. A., Lauterborn, J. C., Gall, C. M., Cariaga, W., and Baram, T. Z. (2001) Enhanced CREB phosphorylation in immature dentate gyrus granule cells precedes neurotrophin expression and indicates a specific role of CREB in granule cell differentiation. Eur. J. Neurosci. 13, 679-686
23. Nakagawa, S., Kim, J. E., Lee, R., Malberg, J. E., Chen, J., Steffen, C., Zhang, Y. J., Nestler, E. J., and Duman, R. S. (2002) Regulation of neurogenesis in adult mouse hippocampus by cAMP and the cAMP response element-binding protein. J. Neurosci. 22, 3673-3682
24. Hattiangady, B., Rao, M. S., Shetty, G. A., and Shetty, A. K. (2005) Brain-derived neurotrophic factor, phosphorylated cyclic AMP response element binding protein and neuropeptide Y decline as early as middle age in the dentate gyrus and CA1 and CA3 subfields of the hippocampus. Exp. Neurol. 195, 353-371
25. Klyubin, I., Walsh, D. M., Lemere, C. A., Cullen, W. K., Shankar, G. M., Betts, V., Spooner, E. T., Jiang, L., Anwyl, R., Selkoe, D. J., and Rowan, M. J. (2005) Amyloid beta protein immunotherapy neutralizes Abeta oligomers that disrupt synaptic plasticity in vivo. Nat. Med. 11, 556-561
26. DeFeudis, F. V., and Drieu, K. (2000) Ginkgo biloba extract (EGb 761) and CNS functions: basic studies and clinical applications. Curr. Drug. Targets 1, 25-58
27. Smith, J. V., and Luo, Y. (2004) Studies on molecular mechanisms of Ginkgo biloba extract. Appl. Microbiol. Biotechnol. 64, 465-472
28. Le Bars, P. L., Katz, M. M., Berman, N., Itil, T. M., Freedman, A. M., and Schatzberg, A. F. (1997) A placebo-controlled, double-blind, randomized trial of an extract of Ginkgo biloba for dementia. North American EGb Study Group. J. Am. Med. Assoc. 278, 1327-1332
29. Oken, B. S., Storzzbach, D. M., and Kaye, J. A. (1998) The efficacy of Ginkgo biloba on cognitive function in Alzheimer disease. Arch. Neurol. 55, 1409-1415
30. Mix, J. A., and David Crews, W., Jr. (2002) A double-blind, placebo-controlled, randomized trial of Ginkgo biloba extract EGb 761(R) in a sample of cognitively intact older adults: neuropsychological findings. Hum. Psychopharmacol. 17, 267-277
31. Mazza, M., Capuano, A., Bria, P., and Mazza, S. (2006) Ginkgo biloba and donepezil: a comparison in the treatment of Alzheimer's dementia in a randomized placebo-controlled doubleblind study. Eur. J. Neurol. 13, 981-985
32. DeKosky, S. T., Fitzpatrick, A., Ives, D. G., Saxton, J., Williamson, J., Lopez, O. L., Burke, G., Fried, L., Kuller, L. H., Robbins, J., et al. (2006) The Ginkgo Evaluation of Memory (GEM) study: design and baseline data of a randomized trial of Ginkgo biloba extract in prevention of dementia. Contemp. Clin. Trials 27, 238-253
33. Bastianetto, S., Zheng, W. H., and Quirion, R. (2000) The Ginkgo biloba extract (EGb 761) protects and rescues hippocampal cells against nitric oxide-induced toxicity: involvement of its flavonoid constituents and protein kinase C. J. Neurochem. 74, 2268-2277
34. Yao, Z., Drieu, K., and Papadopoulos, V. (2001) The Ginkgo biloba extract EGb 761 rescues the PC12 neuronal cells from beta-amyloid-induced cell death by inhibiting the formation of beta-amyloid-derived diffusible neurotoxic ligands. Brain Res. 889, 181-190
35. Gohil, K., and Packer, L. (2002) Bioflavonoid-rich botanical extracts show antioxidant and gene regulatory activity. Ann. N. Y. Acad. Sci. 957, 70-77
36. Luo, Y., Smith, J. V., Paramasivam, V., Burdick, A., Curry, K. J., Buford, J. P., Khan, I., Netzer, W. J., Xu, H., and Butko, P. (2002) Inhibition of amyloid-beta aggregation and caspase-3 activation by the Ginkgo biloba extract EGb761. Proc. Natl. Acad. Sci. U. S. A. 99, 12197-12202
37. Smith, J. V., Burdick, A. J., Golik, P., Khan, I., Wallace, D., and Luo, Y. (2002) Anti-apoptotic properties of Ginkgo biloba extract EGb 761 in differentiated PC12 cells. Cell Mol. Biol. (Noisy-le-grand) 48, 699-707
38. Spencer, J. P., Rice-Evans, C., and Williams, R. J. (2003) Modulation of pro-survival Akt/protein kinase B and ERK1/2 signaling cascades by quercetin and its in vivo metabolites underlie their action on neuronal viability. J. Biol. Chem. 278, 34783-34793
39. Stackman, R. W., Eckenstein, F., Frei, B., Kulhanek, D., Nowlin, J., and Quinn, J. F. (2003) Prevention of age-related spatial memory deficits in a transgenic mouse model of Alzheimer's disease by chronic Ginkgo biloba treatment. Exp. Neurol. 184, 510-520
40. Chromy, B. A., Nowak, R. J., Lambert, M. P., Viola, K. L., Chang, L., Velasco, P. T., Jones, B. W., Fernandez, S. J., Lacor, P. N., Horowitz, P., et al. (2003) Self-assembly of Abeta(1-42) into globular neurotoxins. Biochemistry 42, 12749-12760
41. Price, D. L., and Sisodia, S. S. (1998) Mutant genes in familial Alzheimer's disease and transgenic models. Annu. Rev. Neurosci. 21, 479-505
42. Borchelt, D. R., Thinakaran, G., Eckman, C. B., Lee, M. K., Davenport, F., Ratovitsky, T., Prada, C. M., Kim, G., Seekins, S., Yager, D., et al. (1996) Familial Alzheimer's disease-linked presenilin 1 variants elevate Abeta1-42/1-40 ratio in vitro and in vivo. Neuron 17, 1005-1013
43. Vitolo, O. V., Sant'Angelo, A., Costanzo, V., Battaglia, F., Arancio, O., and 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
44. MacKenzie, S. J., and Houslay, M. D. (2000) Action of rolipram on specific PDE4 cAMP phosphodiesterase isoforms and on the phosphorylation of cAMP-response-element-binding protein (CREB) and p38 mitogen-activated protein (MAP) kinase in U937 monocytic cells. Biochem. J. 347, 571-578
45. Kayed, R., Head, E., Thompson, J. L., McIntire, T. M., Milton, S. C., Cotman, C. W., and Glabe, C. G. (2003) Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300, 486-489
46. Jiang, W., Zhang, Y., Xiao, L., Van Cleemput, J., Ji, S. P., Bai, G., and Zhang, X. (2005) Cannabinoids promote embryonic and adult hippocampus neurogenesis and produce anxiolytic-and antidepressant-like effects. J. Clin. Invest. 115, 3104-3116
47. Wu, Y., Wu, Z. X., Christen, Y., Lambert, M. P., Klein, M. L., Link, C. D., Luo, Y. (2006) Amyloid beta-induced pathological behaviors are suppressed by ginkgo biloba extract Egb 761 and ginkgolides in transgenic Caenorhabditis elegans. J. Neurosci. 26, 13102-13113
48. Lambert, M. P., Barlow, A. K., Chromy, B. A., Edwards, C., Freed, R., Liosatos, M., Morgan, T. E., Rozovsky, I., Trommer, B., Viola, K. L., et al. (1998) Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. U. S. A. 95, 6448-6453
49. Bitan, G., Kirkitadze, M. D., Lomakin, A., Vollers, S. S., Benedek, G. B., and Teplow, D. B. (2003) Amyloid beta-protein (Abeta) assembly: Abeta 40 and Abeta 42 oligomerize through distinct pathways. Proc. Natl. Acad. Sci. U. S. A. 100, 330-335
50. Beglopoulos, V., and Shen, J. (2006) Regulation of CRE-dependent transcription by presenilins: prospects for therapy of Alzheimer's disease. Trends Pharmacol. Sci. 27, 33-40
51. Colciaghi, F., Borroni, B., Zimmermann, M., Bellone, C., Longhi, A., Padovani, A., Cattabeni, F., Christen, Y., and Di Luca, M. (2004) Amyloid precursor protein metabolism is regulated toward alpha-secretase pathway by Ginkgo biloba extracts. Neurobiol. Dis. 16, 454-460
52. Ward, C. P., Redd, K., Williams, B. M., Caler, J. R., Luo, Y., and McCoy, J. G. (2002) Ginkgo biloba extract: cognitive enhancer or antistress buffer. Pharmacol. Biochem. Behav. 72, 913-922
53. Puzzo, D., Vitolo, O., Trinchese, F., Jacob, J. P., Palmeri, A., and Arancio, O. (2005) Amyloid-beta peptide inhibits activation of the nitric oxide/cGMP/cAMP-responsive element-binding protein pathway during hippocampal synaptic plasticity. J. Neurosci. 25, 6887-6897
54. Barker, N., Morin, P. J., and Clevers, H. (2000) The Yin-Yang of TCF/beta-catenin signaling. Adv. Cancer Res. 77, 1-24
55. Mattson, M. P., and Cheng, A. (2006) Neurohormetic phytochemicals: low-dose toxins that induce adaptive neuronal stress responses. Trends Neurosci. 29, 632-639
56. McCubrey, J. A., May, W. S., Duronio, V., and Mufson, A. (2000) Serine/threonine phosphorylation in cytokine signal transduction. Leukemia 14, 9-21
57. Lee, S. J., Campomanes, C. R., Sikat, P. T., Greenfield, A. T., Allen, P. B., and McEwen, B. S. (2004) Estrogen induces phosphorylation of cyclic AMP response element binding (pCREB) in primary hippocampal cells in a time-dependent manner. Neuroscience 124, 549-560
58. Shors, T. J., Miesegaes, G., Beylin, A., Zhao, M., Rydel, T., and Gould, E. (2001) Neurogenesis in the adult is involved in the formation of trace memories. Nature 410, 372-376