Decreased accumulation of subcellular amyloid-β with improved mitochondrial function mediates the neuroprotective effect of huperzine a

Journal of Alzheimer's Disease

Volumn 31, Issue 1, 2012, Pages 131-142

  Yang, Ling ^a   Ye, Chun Yan ^a   Huang, Xiao Tian ^a   Tang, Xi Can ^a   Zhang, Hai Yan ^a  

^a SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

Author keywords

Alzheimer's disease; amyloid peptide; huperzine A; mitochondrial dysfunction; oligomer

Indexed keywords

ACETYLCHOLINESTERASE; AMYLOID PRECURSOR PROTEIN; CYTOCHROME C OXIDASE; HUPERZINE A; OLIGOMER; SUCCINATE DEHYDROGENASE (UBIQUINONE); UBIQUINOL CYTOCHROME C REDUCTASE;

ALZHEIMER DISEASE; AMNESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME ACTIVITY; ENZYME INHIBITION; MITOCHONDRION SWELLING; MOUSE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; TRANSGENIC MOUSE;

EID: 84863918272     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-2012-120274     Document Type: Article

References (48)

1. Cruz L, Urbanc B, Buldyrev SV, Christie R, Gomez-Isla T, Havlin S, McNamara M, Stanley HE, Hyman BT (1997) Aggregation and disaggregation of senile plaques in Alzheimer disease. Proc Natl Acad Sci USA 94, 7612-7616. (Pubitemid 27345364)
2. Mattson MP (2004) Pathways towards and away from Alzheimer's disease. Nature 430, 631-639. (Pubitemid 39061671)
3. Selkoe DJ (1998) The cell biology of beta-amyloid precursor protein and presenilinin Alzheimer's disease. Trends Cell Biol 8, 447-453.
4. Kienlen-Campard P, Miolet S, Tasiaux B, Octave JN (2002) Intracellular amyloid-beta 1-42, but not extracellular soluble amyloid-beta peptides, induces neuronal apoptosis. J Biol Chem 277, 15666-15670. (Pubitemid 34967839)
5. LaFerla FM, Green KN, Oddo S (2007) Intracellular amyloid-beta in Alzheimer's disease. Nat Rev Neurosci 8, 499-509.
6. Hartmann T, Bieger SC, Bruhl B, Tienari PJ, Ida N, All-sop D, Roberts GW, Masters CL, Dotti CG, Unsicker K, Beyreuther K (1997) Distinct sites of intracellular production for Alzheimer's disease A beta40/42 amyloid peptides. Nat Med 3, 1016-1020. (Pubitemid 27391957)
7. Devi L, Prabhu BM, Galati DF, Avadhani NG, Anan-datheerthavarada HK (2006) Accumulation of amyloid precursor protein in the mitochondrial import channels of human Alzheimer's disease brainisassociated withmitochon-drial dysfunction. J Neurosci 26, 9057-9068. (Pubitemid 44319397)
8. Dragicevic N, Mamcarz M, Zhu Y, Buzzeo R, Tan J, Arendash GW, Bradshaw PC (2010) Mitochondrial amyloid-beta levels are associated with the extent of mitochondrial dysfunction in different brain regions and the degree of cognitive impairment in Alzheimer's transgenic mice. JAlzheimers Dis 20 (Suppl 2), S535-S550.
9. Nunomura A, Castellani RJ, Zhu X, Moreira PI, Perry G, Smith MA (2006) Involvement of oxidative stress in Alzheimer disease. J Neuropathol Exp Neurol 65, 631-641. (Pubitemid 44297254)
10. Du H, Guo L, Fang F, Chen D, Sosunov AA, McKhann GM, Yan Y, Wang C, Zhang H, Molkentin JD, Gunn-Moore FJ, Vonsattel JP, Arancio O, Chen JX, Yan SD (2008) Cyclophilin D deficiency attenuates mitochondrial and neuronal perturbation and ameliorates learning and memory in Alzheimer's disease. Nat Med 14, 1097-1105.
11. Lustbader JW, Cirilli M, Lin C, Xu HW, Takuma K, Wang N, Caspersen C, Chen X, Pollak S, Chaney M, Trinchese F, Liu S, Gunn-Moore F, Lue LF, Walker DG, Kuppusamy P, Zewier ZL, Arancio O, Stern D, Yan SS, Wu H (2004) ABAD directly links Abeta to mitochondrial toxicity in Alzheimer's disease. Science 304, 448-452. (Pubitemid 38495942)
12. Du H, Guo L, Yan S, Sosunov AA, McKhann GM, Yan SS (2010) Early deficits in synaptic mitochondria in an Alzheimer's disease mouse model. Proc Natl Acad Sci USA 107, 18670-18675.
13. Wang R, Yan H, Tang XC (2006) Progress in studies of huperzine A, a natural cholinesterase inhibitor from Chinese herbal medicine. Acta Pharmacol Sin 27, 1-26. (Pubitemid 43051942)
14. Zhang HY, Tang XC (2006) Neuroprotective effects of huperzine A: New therapeutic targets for neurodegenerative disease. Trends Pharmacol Sci 27, 619-625. (Pubitemid 44738090)
15. Xiao XQ, Zhang HY, Tang XC (2001) Huperzine A attenuates amyloid β-peptide fragment 25-35-induced apoptosis in rat cortical neurons via inhibiting reactive oxygen species formation and caspase-3 activation. JNeurosci Res 67, 30-36.
16. Gao X, Tang XC (2006) Huperzine A attenuates mitochondrial dysfunction in β-amyloid-treated PC12 cells by reducing oxygen free radicals accumulation and improving mitochondrial energy metabolism. J Neurosci Res 83, 1048-1057.
17. Gao X, Zheng CY, Yang L, Tang XC, Zhang HY (2009) Huperzine A protects isolated rat brain mitochondria against β-amyloid peptide. Free Radic Biol Med 46, 1454-1462.
18. Blanchard V, Moussaoui S, Czech C, Touchet N, Bonici B, Planche M, Canton T, Jedidi I, Gohin M, Wirths O, Bayer TA, Langui D, Duyckaerts C, Tremp G, Pradier L (2003) Time sequence of maturation of dystrophic neurites associated with Aβ deposits in APP/PS1 transgenic mice. Exp Neurol 184, 247-263. (Pubitemid 37444035)
19. Gureviciene I, Ikonen S, Gurevicius K, Sarkaki A, van Groen T, Pussinen R, Ylinen A, Tanila H (2004) Normal induction but accelerated decay of LTP in APP + PS1 transgenic mice. Neurobiol Dis 15, 188-195. (Pubitemid 38296749)
20. Trinchese F, Liu S, Battaglia F, Walter S, Mathews PM, Arancio O (2004) Progressive age-related development of Alzheimer-like pathology in APP/PS1 mice. Ann Neurol 55, 801-814. (Pubitemid 38702575)
21. Rosario ER, Carroll JC, Oddo S, LaFerla FM, Pike CJ (2006) Androgens regulate the development of neuropathology in a triple transgenic mouse model of Alzheimer's disease. J Neurosci 26, 13384-13389. (Pubitemid 46011649)
22. Manczak M, Anekonda TS, Henson E, Park BS, Quinn J, Reddy PH (2006) Mitochondria are a direct site of A beta accumulation in Alzheimer's disease neurons: Implications for free radical generation and oxidative damage in disease progression. Hum Mol Genet 15, 1437-1449.
23. 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.
24. Berman SB, Watkins SC, Hastings TG (2000) Quantitative biochemical and ultrastructural comparison of mitochondrial permeability transition in isolated brain and liver mitochondria: Evidence for reduced sensitivity of brain mitochondria. Exp Neurol 164, 415-425. (Pubitemid 32008986)
25. Tang XC, Han YF (1999) Pharmacological profile of huperzine A, a novel acetylcholinesterase inhibitor from Chinese herb. CNS Drug Reviews 5, 281-300. (Pubitemid 29519654)
26. Estornell E, Fato R, Pallotti F, Lenaz G (1993) Assay conditions for the mitochondrial NADH:coenzyme Q oxi-doreductase. FEBS Lett 332, 127-131. (Pubitemid 23295913)
27. King TE (1967) Preparations of succinate-cytochrome c reductase and the cytochromeb-c1 particle, and reconstitu-tion of succinate-cytochrome c reductase. Methods Enzymol 10, 216-225.
28. Wharton DC, Tzagoloff A (1967) Cytochrome oxidase from beef heart mitochondria. Methods Enzymol 10, 245-250.
29. He J, Luo H, Yan B, Yu Y, Wang H, Wei Z, Zhang Y, Xu H, Tempier A, Li X, Li XM (2009) Beneficial effects of queti-apine in a transgenic mouse model of Alzheimer's disease. Neurobiol Aging 30, 1205-1216.
30. Selkoe DJ (2002) Alzheimer's disease is a synaptic failure. Science 298, 789-791. (Pubitemid 35231524)
31. Bernardi P, Broekemeier KM, Pfeiffer DR (1994) Recent progress on regulation of the mitochondrial permeability transition pore; a cyclosporin-sensitive pore in the inner mitochondrial membrane. J Bioenerg Biomembr 26, 509-517. (Pubitemid 24378753)
32. De Felice FG, Wu D, Lambert MP, Fernandez SJ, Velasco PT, Lacor PN, Bigio EH, Jerecic J, Acton PJ, Shughrue PJ, Chen-Dodson E, Kinney GG, Klein WL (2008) Alzheimer's disease-type neuronal tau hyperphosphorylation induced by A beta oligomers. Neurobiol Aging 29, 1334-1347. (Pubitemid 351970596)
33. Fernandez A, Llacuna L, Fernandez-Checa JC, Colell A (2009) Mitochondrial cholesterol loading exacerbates amyloid-β peptide-induced inflammation and neurotoxicity. J Neurosci 29, 6394-6405.
34. 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 USA 95, 6448-6453.
35. Tang KH, Blankenship RE (2010) Both forward and reverse TCA cycles operate in green sulfur bacteria. JBiol Chem 285, 35848-35854.
36. Yao J, Irwin RW, Zhao L, Nilsen J, Hamilton RT, Brinton RD (2009) Mitochondrial bioenergetic deficit precedes Alzheimer's pathology in female mouse model of Alzheimer's disease. Proc Natl Acad Sci USA 106, 14670-14675.
37. Pan X, Gong N, Zhao J, Yu Z, Gu F, Chen J, Sun X, Zhao L, Yu M, Xu Z, Dong W, Qin Y, Fei G, Zhong C, Xu TL (2010) Powerful beneficial effects of benfotiamine on cognitive impairment and beta-amyloid deposition in amyloid precursor protein/presenilin-1 transgenic mice. Brain 133, 1342-1351.
38. Wang H, Tang XC (1998) Anticholinesterase effects of huperzine A, E2020, and tacrine in rats. Zhongguo Yao Li Xue Bao 19, 27-30. (Pubitemid 28073943)
39. Fu H, Li W, Lao Y, Luo J, Lee NT, Kan KK, Tsang HW, Tsim KW, Pang Y, Li Z, Chang DC, Li M, Han Y (2006) Bis (7)-tacrine attenuates beta amyloid-induced neuronal apoptosis by regulating L-type calcium channels. J Neurochem 98, 1400-1410. (Pubitemid 44200432)
40. Liu X, Xu K, Yan M, Wang Y, Zheng X (2010) Protective effects of galantamine against Abeta-induced PC12 cell apoptosis by preventing mitochondrial dysfunction and endo-plasmic reticulum stress. Neurochem Int 57, 588-599.
41. Noh MY, Koh SH, Kim Y, Kim HY, Cho GW, Kim SH (2009) Neuroprotective effects of donepezil through inhibition of GSK-3 activity in amyloid-beta-induced neuronal cell death. J Neurochem 108, 1116-1125.
42. 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 nonamyloido-genic pathway in an Alzheimer transgenic mouse model. Neuropsychopharmacol 36, 1073-1089.
43. Wang Y, Tang XC, Zhang HY (2012) Huperzine a alleviates synaptic deficits and modulates amyloidogenic and nonamy-loidogenic pathways in APPswe/PS1dE9 transgenic mice. J Neurosci Res 90, 508-517.
44. Anderson MF, Sims NR (2000) Improved recovery of highly enriched mitochondrial fractions from small brain tissue samples. Brain Res 5, 95-101. (Pubitemid 30136070)
45. Sims NR, Anderson MF (2008) Isolation of mitochondria from rat brain using Percoll density gradient centrifugation. Nat Protoc 3, 1228-1239.
46. Tillement L, Lecanu L, Yao W, Greeson J, Papadopoulos V (2006) The spirostenol (22R, 25R)-20alpha-spirost-5-en-3beta-yl hexanoate blocks mitochondrial uptake of Abeta in neuronal cells and prevents Abeta-induced impairment of mitochondrial function. Steroids 71, 725-735. (Pubitemid 43994018)
47. Hansson Petersen CA, Alikhani N, Behbahani H, Wiehager B, Pavlov PF, Alafuzoff I, Leinonen V, Ito A, Winblad B, Glaser E, Ankarcrona M (2008) The amyloid beta-peptide is imported into mitochondria via the TOM import machinery and localized to mitochondrial cristae. Proc Natl Acad Sci USA 105, 13145-13150.
48. Tillement L, Lecanu L, Papadopoulos V (2011) Further evidence on mitochondrial targeting of beta-amyloid and specificity of beta-amyloid-induced mitotoxicity in neurons. Neurodegener Dis 8, 331-344.