Huperzine a alleviates synaptic deficits and modulates amyloidogenic and nonamyloidogenic pathways in APPswe/PS1dE9 transgenic mice

Journal of Neuroscience Research

Volumn 90, Issue 2, 2012, Pages 508-517

  Wang, Ying ^a   Tang, Xi Can ^a   Zhang, Hai Yan ^a  

^a SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

Author keywords

amyloid; Adam10; Alzheimer's disease; Bace1; Huperzine a

Indexed keywords

ADAM10 ENDOPEPTIDASE; AMYLOID PRECURSOR PROTEIN; BETA ACTIN; BETA SECRETASE 1; HUPERZINE A; MEMBRANE METALLOENDOPEPTIDASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; OLIGOMER; PRESENILIN 1; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOPHYSIN; SYNAPTOTAGMIN;

ANIMAL EXPERIMENT; ARTICLE; BRAIN CORTEX; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; DENDRITIC SPINE; DENSITY; DRUG MECHANISM; DRUG POTENCY; ENZYME PHOSPHORYLATION; FRONTAL CORTEX; FRONTAL LOBE; HIPPOCAMPUS; HUMAN; HUMAN CELL; IN VIVO STUDY; MOUSE; NEUROMODULATION; NEUROPROTECTION; NONHUMAN; PARIETAL CORTEX; PARIETAL LOBE; PRIORITY JOURNAL; PROTEIN METABOLISM; PROTEIN PROCESSING; REGULATORY MECHANISM; SENILE PLAQUE; SYNAPSE; TRANSGENIC MOUSE;

ALKALOIDS; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; DENDRITIC SPINES; HEK293 CELLS; HUMANS; MICE; MICE, TRANSGENIC; NEUROPROTECTIVE AGENTS; PLAQUE, AMYLOID; PRESENILIN-1; SESQUITERPENES; SIGNAL TRANSDUCTION; SYNAPSES;

EID: 83155180349     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22775     Document Type: Article

References (61)

1. Bandyopadhyay S, Hartley DM, Cahill CM, Lahiri DK, Chattopadhyay N, Rogers JT. 2006. Interleukin-1alpha stimulates non-amyloidogenic pathway by alpha-secretase (ADAM-10 and ADAM-17) cleavage of APP in human astrocytic cells involving p38 MAP kinase. J Neurosci Res 84: 106-118.
2. Bittner T, Fuhrmann M, Burgold S, Ochs SM, Hoffmann N, Mitteregger G, Kretzschmar H, LaFerla FM, Herms J. 2010. Multiple events lead to dendritic spine loss in triple transgenic Alzheimer's disease mice. PLoS One 5: e15477.
3. Brose N, Petrenko AG, Sudhof TC, Jahn R. 1992. Synaptotagmin: a calcium sensor on the synaptic vesicle surface. Science 256: 1021-1025.
4. Calabrese B, Wilson MS, Halpain S. 2006. Development and regulation of dendritic spine synapses. Physiology 21: 38-47.
5. Camden JM, Schrader AM, Camden RE, Gonzalez FA, Erb L, Seye CI, Weisman GA. 2005. P2Y2 nucleotide receptors enhance alpha-secretase-dependent amyloid precursor protein processing. J Biol Chem 280: 18696-18702.
6. Canet-Aviles RM, Anderton M, Hooper NM, Turner AJ, Vaughan PF. 2002. Muscarine enhances soluble amyloid precursor protein secretion in human neuroblastoma SH-SY5Y by a pathway dependent on protein kinase C(alpha), src-tyrosine kinase and extracellular signal-regulated kinase but not phospholipase C. Brain Res Mol Brain Res 102: 62-72.
7. Chen Y, Rex CS, Rice CJ, Dube CM, Gall CM, Lynch G, Baram TZ. 2010. Correlated memory defects and hippocampal dendritic spine loss after acute stress involve corticotropin-releasing hormone signaling. Proc Natl Acad Sci U S A 107: 13123-13128.
8. Cheung EC, Slack RS. 2004. Emerging role for ERK as a key regulator of neuronal apoptosis. Sci STKE 2004: PE45.
9. Chiba T, Yamada M, Sasabe J, Terashita K, Shimoda M, Matsuoka M, Aiso S. 2009. Amyloid-beta causes memory impairment by disturbing the JAK2/STAT3 axis in hippocampal neurons. Mol Psychiatry 14: 206-222.
10. Counts SE, Nadeem M, Lad SP, Wuu J, Mufson EJ. 2006. Differential expression of synaptic proteins in the frontal and temporal cortex of elderly subjects with mild cognitive impairment. J Neuropathol Exp Neurol 65: 592-601.
11. Desdouits-Magnen J, Desdouits F, Takeda S, Syu LJ, Saltiel AR, Buxbaum JD, Czernik AJ, Nairn AC, Greengard P. 1998. Regulation of secretion of Alzheimer amyloid precursor protein by the mitogen-activated protein kinase cascade. J Neurochem 70: 524-530.
12. Dong H, Martin MV, Chambers S, Csernansky JG. 2007. Spatial relationship between synapse loss and beta-amyloid deposition in Tg2576 mice. J Comp Neurol 500: 311-321.
13. Esch FS, Keim PS, Beattie EC, Blacher RW, Culwell AR, Oltersdorf T, McClure D, Ward PJ. 1990. Cleavage of amyloid beta peptide during constitutive processing of its precursor. Science 248: 1122-1124.
14. Garcia-Alloza M, Robbins EM, Zhang-Nunes SX, Purcell SM, Betensky RA, Raju S, Prada C, Greenberg SM, Bacskai BJ, Frosch MP. 2006. Characterization of amyloid deposition in the APPswe/PS1dE9 mouse model of Alzheimer disease. Neurobiol Dis 24: 516-524.
15. Glavan G, Schliebs R, Zivin M. 2009. Synaptotagmins in neurodegeneration. Anat Rec 292: 1849-1862.
16. Haass C, Selkoe DJ. 2007. Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide. Nat Rev Mol Cell Biol 8: 101-112.
17. Hardy J, Selkoe DJ. 2002. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297: 353-356.
18. Haring R, Fisher A, Marciano D, Pittel Z, Kloog Y, Zuckerman A, Eshhar N, Heldman E. 1998. Mitogen-activated protein kinase-dependent and protein kinase C-dependent pathways link the m1 muscarinic receptor to beta-amyloid precursor protein secretion. J Neurochem 71: 2094-2103.
19. Hedberg MM, Clos MV, Ratia M, Gonzalez D, Lithner CU, Camps P, Munoz-Torrero D, Badia A, Gimenez-Llort L, Nordberg A. 2010. Effect of huprine X on beta-amyloid, synaptophysin and alpha7 neuronal nicotinic acetylcholine receptors in the brain of 3× Tg-AD and APPswe transgenic mice. Neurodegener Dis 7: 379-388.
20. Hersh LB, Rodgers DW. 2008. Neprilysin and amyloid beta peptide degradation. Curr Alzheimer Res 5: 225-231.
21. Holcomb L, Gordon MN, McGowan E, Yu X, Benkovic S, Jantzen P, Wright K, Saad I, Mueller R, Morgan D, Sanders S, Zehr C, O'Campo K, Hardy J, Prada CM, Eckman C, Younkin S, Hsiao K, Duff K. 1998. Accelerated Alzheimer-type phenotype in transgenic mice carrying both mutant amyloid precursor protein and presenilin 1 transgenes. Nat Med 4: 97-100.
22. Holsinger RM, McLean CA, Beyreuther K, Masters CL, Evin G. 2002. Increased expression of the amyloid precursor beta-secretase in Alzheimer's disease. Ann Neurol 51: 783-786.
23. Jacobsen JS, Wu CC, Redwine JM, Comery TA, Arias R, Bowlby M, Martone R, Morrison JH, Pangalos MN, Reinhart PH, Bloom FE. 2006. Early-onset behavioral and synaptic deficits in a mouse model of Alzheimer's disease. Proc Natl Acad Sci U S A 103: 5161-5166.
24. Jahn R, Sudhof TC. 1993. Synaptic vesicle traffic: rush hour in the nerve terminal. J Neurochem 61: 12-21.
25. Kanemitsu H, Tomiyama T, Mori H. 2003. Human neprilysin is capable of degrading amyloid beta peptide not only in the monomeric form but also the pathological oligomeric form. Neurosci Lett 350: 113-116.
26. Knobloch M, Farinelli M, Konietzko U, Nitsch RM, Mansuy IM. 2007. Abeta oligomer-mediated long-term potentiation impairment involves protein phosphatase 1-dependent mechanisms. J Neurosci 27: 7648-7653.
27. Koffie RM, Meyer-Luehmann M, Hashimoto T, Adams KW, Mielke ML, Garcia-Alloza M, Micheva KD, Smith SJ, Kim ML, Lee VM, Hyman BT, Spires-Jones TL. 2009. Oligomeric amyloid beta associates with postsynaptic densities and correlates with excitatory synapse loss near senile plaques. Proc Natl Acad Sci U S A 106: 4012-4017.
28. Kojro E, Postina R, Buro C, Meiringer C, Gehrig-Burger K, Fahrenholz F. 2006. The neuropeptide PACAP promotes the alpha-secretase pathway for processing the Alzheimer amyloid precursor protein. FASEB J 20: 512-514.
29. 2 receptor. J Neurochem 109: 1300-1310.
30. Kuhn PH, Wang H, Dislich B, Colombo A, Zeitschel U, Ellwart JW, Kremmer E, Rossner S, Lichtenthaler SF. 2010. ADAM10 is the physiologically relevant, constitutive alpha-secretase of the amyloid precursor protein in primary neurons. EMBO J 29: 3020-3032.
31. Lanz TA, Carter DB, Merchant KM. 2003. Dendritic spine loss in the hippocampus of young PDAPP and Tg2576 mice and its prevention by the ApoE2 genotype. Neurobiol Dis 13: 246-253.
32. 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.
33. Magga J, Puli L, Pihlaja R, Kanninen K, Neulamaa S, Malm T, Hartig W, Grosche J, Goldsteins G, Tanila H, Koistinaho J, Koistinaho M. 2010. Human intravenous immunoglobulin provides protection against Abeta toxicity by multiple mechanisms in a mouse model of Alzheimer's disease. J Neuroinflammation 7: 90.
34. 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.
35. Mills J, Reiner PB. 1999. Regulation of amyloid precursor protein cleavage. J Neurochem 72: 443-460.
36. Mills J, Laurent Charest D, Lam F, Beyreuther K, Ida N, Pelech SL, Reiner PB. 1997. Regulation of amyloid precursor protein catabolism involves the mitogen-activated protein kinase signal transduction pathway. J Neurosci 17: 9415-9422.
37. Moolman DL, Vitolo OV, Vonsattel JP, Shelanski ML. 2004. Dendrite and dendritic spine alterations in Alzheimer models. J Neurocytol 33: 377-387.
38. Nitsch RM, Slack BE, Wurtman RJ, Growdon JH. 1992. Release of Alzheimer amyloid precursor derivatives stimulated by activation of muscarinic acetylcholine receptors. Science 258: 304-307.
39. Ono K, Condron MM, Teplow DB. 2009. Structure-neurotoxicity relationships of amyloid beta-protein oligomers. Proc Natl Acad Sci U S A 106: 14745-14750.
40. Peng Y, Lee DY, Jiang L, Ma Z, Schachter SC, Lemere CA. 2007. Huperzine A regulates amyloid precursor protein processing via protein kinase C and mitogen-activated protein kinase pathways in neuroblastoma SK-N-SH cells over-expressing wild type human amyloid precursor protein 695. Neuroscience 150: 386-395.
41. Peng Y, Hu Y, Xu S, Feng N, Wang L, Wang X. 2011. L-3-n-butylphthalide regulates amyloid precursor protein processing by PKC and MAPK pathways in SK-N-SH cells over-expressing wild type human APP695. Neurosci Lett 487: 211-216.
42. Reddy PH, Mani G, Park BS, Jacques J, Murdoch G, Whetsell WJr, Kaye J, Manczak M. 2005. Differential loss of synaptic proteins in Alzheimer's disease: implications for synaptic dysfunction. J Alzheimers Dis 7: 103-117; discussion173-180.
43. Reiserer RS, Harrison FE, Syverud DC, McDonald MP. 2007. Impaired spatial learning in the APPSwe + PSEN1DeltaE9 bigenic mouse model of Alzheimer's disease. Genes Brain Behav 6: 54-65.
44. Rutten BP, Van der Kolk NM, Schafer S, van Zandvoort MA, Bayer TA, Steinbusch HW, Schmitz C. 2005. Age-related loss of synaptophysin immunoreactive presynaptic boutons within the hippocampus of APP751SL, PS1M146L, and APP751SL/PS1M146L transgenic mice. Am J Pathol 167: 161-173.
45. Savage MJ, Lin YG, Ciallella JR, Flood DG, Scott RW. 2002. Activation of c-Jun N-terminal kinase and p38 in an Alzheimer's disease model is associated with amyloid deposition. J Neurosci 22: 3376-3385.
46. Shankar GM, Li S, Mehta TH, Garcia-Munoz A, Shepardson NE, Smith I, Brett FM, Farrell MA, Rowan MJ, Lemere CA, Regan CM, Walsh DM, Sabatini BL, Selkoe DJ. 2008. Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 14: 837-842.
47. Smith TD, Adams MM, Gallagher M, Morrison JH, Rapp PR. 2000. Circuit-specific alterations in hippocampal synaptophysin immunoreactivity predict spatial learning impairment in aged rats. J Neurosci 20: 6587-6593.
48. Spires TL, Meyer-Luehmann M, Stern EA, McLean PJ, Skoch J, Nguyen PT, Bacskai BJ, Hyman BT. 2005. Dendritic spine abnormalities in amyloid precursor protein transgenic mice demonstrated by gene transfer and intravital multiphoton microscopy. J Neurosci 25: 7278-7287.
49. Spires-Jones TL, Meyer-Luehmann M, Osetek JD, Jones PB, Stern EA, Bacskai BJ, Hyman BT. 2007. Impaired spine stability underlies plaque-related spine loss in an Alzheimer's disease mouse model. Am J Pathol 171: 1304-1311.
50. Tang LL, Wang R, Tang XC. 2005. Effects of huperzine A on secretion of nerve growth factor in cultured rat cortical astrocytes and neurite outgrowth in rat PC12 cells. Acta Pharmacol Sin 26: 673-678.
51. Tsai J, Grutzendler J, Duff K, Gan WB. 2004. Fibrillar amyloid deposition leads to local synaptic abnormalities and breakage of neuronal branches. Nat Neurosci 7: 1181-1183.
52. Wang CY, Zheng W, Wang T, Xie JW, Wang SL, Zhao BL, Teng WP, Wang ZY. 2011. Huperzine A activates Wnt/beta-catenin signaling and enhances the nonamyloidogenic pathway in an Alzheimer transgenic mouse model. Neuropsychopharmacology 36: 1073-1089.
53. Wang J, Dickson DW, Trojanowski JQ, Lee VM. 1999. The levels of soluble versus insoluble brain Abeta distinguish Alzheimer's disease from normal and pathologic aging. Exp Neurol 158: 328-337.
54. Wiley JC, Pettan-Brewer C, Ladiges WC. 2011. Phenylbutyric acid reduces amyloid plaques and rescues cognitive behavior in AD transgenic mice. Aging Cell 10: 418-428.
55. Woodard-Grice AV, McBrayer AC, Wakefield JK, Zhuo Y, Bellis SL. 2008. Proteolytic shedding of ST6Gal-I by BACE1 regulates the glycosylation and function of alpha4beta1 integrins. J Biol Chem 283: 26364-26373.
56. Wu HY, Hudry E, Hashimoto T, Kuchibhotla K, Rozkalne A, Fan Z, Spires-Jones T, Xie H, Arbel-Ornath M, Grosskreutz CL, Bacskai BJ, Hyman BT. 2010. Amyloid beta induces the morphological neurodegenerative triad of spine loss, dendritic simplification, and neuritic dystrophies through calcineurin activation. J Neurosci 30: 2636-2649.
57. Yan H, Zhang HY, Tang XC. 2007. Involvement of M1-muscarinic acetylcholine receptors, protein kinase C and mitogen-activated protein kinase in the effect of huperzine A on secretory amyloid precursor protein-alpha. Neuroreport 18: 689-692.
58. Yang F, Lim GP, Begum AN, Ubeda OJ, Simmons MR, Ambegaokar SS, Chen PP, Kayed R, Glabe CG, Frautschy SA, Cole GM. 2005. Curcumin inhibits formation of amyloid beta oligomers and fibrils, binds plaques, and reduces amyloid in vivo. J Biol Chem 280: 5892-5901.
59. Yoon IS, Chen E, Busse T, Repetto E, Lakshmana MK, Koo EH, Kang DE. 2007. Low-density lipoprotein receptor-related protein promotes amyloid precursor protein trafficking to lipid rafts in the endocytic pathway. FASEB J 21: 2742-2752.
60. Yue P, Tao T, Zhao Y, Ren J, Chai X. 2007. Huperzine A in rat plasma and CSF following intranasal administration. Int J Pharmacol 337: 127-132.
61. Zhang HY, Yan H, Tang XC. 2004. Huperzine A enhances the level of secretory amyloid precursor protein and protein kinase C-alpha in intracerebroventricular beta-amyloid-(1-40) infused rats and human embryonic kidney 293 Swedish mutant cells. Neurosci Lett 360: 21-24.