The metabolic enhancer piracetam ameliorates the impairment of mitochondrial function and neurite outgrowth induced by ß-amyloid peptide

British Journal of Pharmacology

Volumn 160, Issue 2, 2010, Pages 246-257

  Kurz, C ^a   Ungerer, I ^a   Lipka, U ^a   Kirr, S ^a   Schutt T ^a   Eckert, A ^b   Leuner, K ^a   Muller W E ^a  

^a GOETHE UNIVERSITY   (Germany)

^b UNIVERSITY OF BASEL   (Switzerland)

Author keywords

amyloid; Alzheimer's disease; ATP production; Mitochondrial function; Neurite growth; Piracetam

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; PIRACETAM;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIOXIDANT ACTIVITY; ARTICLE; BRAIN CELL; CELL STRAIN; CELL STRAIN HEK293; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG MECHANISM; FEMALE; HUMAN; HUMAN CELL; MALE; MOUSE; NERVE FIBER GROWTH; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN SYNTHESIS;

ADENOSINE TRIPHOSPHATE; AMYLOID BETA-PROTEIN; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BRAIN; CELL LINE; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; NEURITES; NEUROPROTECTIVE AGENTS; OXIDATIVE STRESS; PC12 CELLS; PEPTIDE FRAGMENTS; PIRACETAM; RATS; TRANSFECTION;

EID: 77951669569     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2010.00656.x     Document Type: Article

References (71)

1. Alexander SPH, Mathie A, Peters JA (2009). Guide to Receptors and Channels (GRAC), 4th edition. Br J Pharmacol 158 (Suppl. 1 S1 S254. (Pubitemid 351415518)
2. Atamna H, Nguyen A, Schultz C, Boyle K, Newberry J, Kato H et al. (2008). Methylene blue delays cellular senescence and enhances key mitochondrial biochemical pathways. FASEB J 22 : 703 712. (Pubitemid 351348123)
3. Bachurin SA, Shevtsova EP, Kireeva EG, Oxebkrug GF, Sablin SO (2003). Mitochondria as a target for neurotoxins and neuroprotective agents. Ann N Y Acad Sci 993 : 334 344.
4. Benzi G, Pastoris O, Villa RR, Giuffrida AM (1985). Influence of aging and exogenous substances on cerebral energy metabolism in posthypoglycemic recovery. Biochem Pharmacol 34 : 1477 1483. (Pubitemid 15025785)
5. Bernales S, Wagner S, Protter AA, Hung DT (2008). Dimebon induces neurite outgrowth and mitochondrial statilizion. Program No. 543.29/S12. Neuroscience Meeting Planner.
6. Blanchard V, Moussaoui S, Czech C, Touchet N, Bonici B, Planche M et al. (2003). Time sequence of maturation of dystrophic neurites associated with Abeta deposits in APP/PS1 transgenic mice. Exp Neurol 184 : 247 263. (Pubitemid 37444035)
7. Blasko I, Kemmler G, Krampla W, Jungwirth S, Wichart I, Jellinger K et al. (2005). Plasma amyloid ß protein 42 in non-demented persons aged 75 years: effects of concomitant medication and medial temporal lobe atrophy. Neurobiol Aging 26 : 1135 1143. (Pubitemid 40726005)
8. Brandao F, Paula-Barbosa JM, Cadete-Leite A (1995). Piracetam impedes hippocampal neuronal loss during withdrawal after chronic alcohol intake. Alcohol 12 : 279 288.
9. Brandao F, Cadete-Leite A, Andrade JP, Madeira MD, Paula-Barbose MM (1996). Piracetam promotes mossy fiber synaptic reorganization in rats withdrawn from alcohol. Alcohol 13 : 239 249. (Pubitemid 26147492)
10. Callaway NL, Riha PD, Wrubel KM, Mccollum D, Gonzalez-Lima F (2002). Methylene blue restores spatial memory retention impaired by an inhibitor of cytochrome oxidase in rats. Neurosci Lett 332 : 83 86. (Pubitemid 35217846)
11. Callaway NL, Rihe PD, Bruchey AK, Munshi Z, Gonzalez-Lima F (2004). Methylene blue improves brain oxidative metabolism and memory retentions in rats. Pharmacol Biochem Behav 77 : 175 181. (Pubitemid 38076994)
12. Canevari L, Clark JB, Bates TE (1999). Beta-amyloid fragment 25-35 selectively decreases complex IV activity in isolated mitochondria. FEBS Lett 457 : 131 134. (Pubitemid 29387424)
13. Casley CS, Land JM, Sharpe MA, Clark JB, Duchen MR, Canevari L (2002). Beta-amyloid fragment 25-35 causes mitochondrial dysfunction in primary cortical neurons. Neurobiol Dis 10 : 258 267. (Pubitemid 35217579)
14. Chan SL, Furukawa K, Mattson MP (2002). Presenilins and APP in neuritic and synaptic plasticity. Neuromol Med 2 : 167 196.
15. Coq O, Xerri C (1999). Acute reorganization of the forepaw representation in the rat. SI cortex after focal cortical injury: neuroprotective effects of piracetam treatment. Eur J Neurosci 11 : 2597 2608. (Pubitemid 29364180)
16. Crouch P, Kozlowski R, Slater KJ, Fletcher J (1993). The use of ATP bioluminescence as a measure of cell proliferation and cytotoxicity. J Immunol Methods 160 : 81 88. (Pubitemid 23085118)
17. Dekosky ST, Scheff SW (1990). Synapse loss in frontal cortex biopsies in Alzheimer's disease: correlation with cognitive severity. Ann Neurol 27 (5 457 464.
18. Domanska-Janik K, Zaleska M (1977). The action of piracetam on 14C-glucose metabolism in normal and posthypoxic rat cerebral cortex slices. Pol J Pharmacol Pharm 29 : 111 116. (Pubitemid 8096076)
19. Doody RA, Gavrilova SI, Sana M, Thomas RG, Aisen PS, Bachurin SO et al. (2008). Effect of dimebon on cognition, activities of daily living, behaviour, and global function in patients with mild-to-moderate Alzheimer's disease: a randomised, double-blind, placebo-controlled study. Lancet 372 : 207 215.
20. Eckert A, Keil U, Marques CA, Bonert A, Frey C, Schüssel K et al. (2003). Mitochondrial dysfunction, apoptotic cell death, and Alzheimer's disease. Biochem Pharmacol 66 : 1627 1634. (Pubitemid 38373355)
21. Eckert A, Hauptmann S, Scherping E, Meinhardt J, Rhein V, Dröse S et al. (2008). Oligomeric and fibrillar species of ß-amyloid (Aß42) both impair mitochondrial function in P301L tau transgenic mice. J Mol Med 86 : 1255 1267.
22. Evans NA, Facci L, Owen DE, Soden PE, Burgidge SA, Prinjha RK et al. (2008). Aß1-42 reduces synapse number and inhibits neurite outgrowth in primary cortical and hippocampal neurons: a quantitive analysis. J Neurosci Methods 175 : 96 103.
23. Figueroa DJ, Morris JA, Ma L, Kandpal G, Chen E, Li YM et al. (2002). Presenilin-dependent gamma-secretase activity modulates neurite outgrowth. Neurobiol Dis 9 : 49 60. (Pubitemid 34174564)
24. Fordyce DE, Clark VJ, Paylor R, Wehner JM (1995). Enhancement of hippocampally-mediated learning and protein kinase C activity by oxiracetam in learning-impaired DBA/2 mice. Brain Res 672 : 170 176.
25. Fukui H, Moraes CT (2008). The mitochondrial impairment, oxidative stress and neurodegeneration connection: reality or just an attractive hypothesis? Trends Neurosci 31 : 252 256.
26. Giurgea CE (1982). The nootropic concept and its prospective implications. Drug Dev Res 2 : 441 446. (Pubitemid 13191544)
27. Guglielmotto M, Aragno M, Auteooi R, Giliberto L, Novo E, Colombatto S et al. (2009). The up-regulation of BACE1 mediated by hypoxia and ischemic injury: role of ocidative stress and HIF1α. J Neurochem 198 : 1045 1056.
28. Gura T (2008). Hope in Alzheimer's fight emerges from unexpected places. Nature Med 14 : 894.
29. Hauptmann S, Scherping I, Dröse S, Brandt U, Schulz KL, Jendrach J et al. (2009). Mitochondrial dysfunction: an early event in Alzheimer pathology accumulates with age in AD transgenic mice. Neurobiol Aging 30 (10 1574 1586.
30. He Z, Liao Y, Zheng M, Zeng FD, Guo LJ (2008). Piracetam improves cognitive deficits caused by chronic cerebral hypoperfusion in rats. Cell Mol Neurobiol 28 : 613 627. (Pubitemid 351624502)
31. Heiss WD, Hebold I, Klinkhammer PL, Ziffling P, Szelies B, Pawlik G et al. (1988). Effect of piracetam on cerebral glucose metabolism in Alzneimer's disease as measured by positron emission tomography. J Cereb Blood Flow Metab 8 : 613 617.
32. Hirata K, Yamaguchi H, Takaura Y, Takagi A, Fukushime T, Iwakami N et al. (2005). A novel neurotropic agent, T-817MA [1-{3-[2-(1-benzothiophen-5-yl) Ethoxy] propyl}-2-azetidinol maleate], attenuates amyloid-ß-induced neurotoxicity and promotes neurite outgrowth in rat cultured central nervous system neurons. J Pharmacol Exp Ther 314 : 252 259. (Pubitemid 41058262)
33. Hlinak Z, Krejci E (2002). Oxiracetam prevented the scopolamine but not the diazepam induced memory deficits in mice. Behav Res 133 : 395 399.
34. Holinski S, Claus B, Alaaraj N, Dohmen PM, Kirilova K, Neumann K et al. (2008). Cerebroprotective effect of piracetam in patients undergoing coronary bypass surgery. Med Sci Monit 14 : 1 5.
35. 1-42- induced neurite outgrowth reduction in rat primary cortical neurons: neuroprotective effects of α7 neuronal nicotinic acetylcholine receptor ligands. Brain Res 1151 : 227 235. (Pubitemid 46709875)
36. Jin SM, Cho HJ, Jung ES, Shim MY, Mook-Jung I (2008). DNA damage-inducing agents elicit gamma-secretase activation mediated by oxidative stress. Cell Death Differ 15 : 1375 1384.
37. Keil U, Bonert A, Marques CA, Scherping I, Weyermann J, Strosznajder JB et al. (2004). Amyloid beta-induced changes in nitric oxide production and mitochondrial activity lead to apoptosis. J Biol Chem 279 : 50310 50320. (Pubitemid 39577847)
38. Keil U, Scherping I, Hauptmann S, Schuessel K, Eckert A, Müller WE (2006). Piracetam improves mitochondrial dysfunction following oxidative stress. Br J Pharmacol 147 : 199 208. (Pubitemid 43151568)
39. Kuboyama T, Tohda C, Komatsu K (2005). Neuritic regeneration and synaptic reconstruction induced by withanolide A. Br J Pharmacol 144 : 961 971. (Pubitemid 40593022)
40. Lacor PN, Buniel MC, Furlow PW, Sanzclemente A, Velasco PT, Wood M et al. (2007). Aß oligomer-induced aberrations in synapse composition, shape, and density provide a molecular basis for loss of connectivity in Alzheimer's disease. J Neurosci 27 (4 796 807. (Pubitemid 46174498)
41. Leuner K, Hauptmann S, Abdel-Kader R, Scherping I, Keil U, Strosznajder JB et al. (2007). Mitochondrial dysfunction: the first domino in brain aging and Alzheimer's disease? Antioxid Redox Signal 9 : 1659 1675. (Pubitemid 47462969)
42. Leutz S, Steiner B, Marques CA, Haass C, Müller WE, Eckert A (2002). Reduction of tropic support enhances apoptosis in PC12 cells expressing Alzheimer's App mutation and sensitizes cells to staurosporine-induced cell death. J Mol Neurosci 18 : 189 201. (Pubitemid 34569409)
43. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951). Protein measurement with the folin phenol reagent. J Biol Chem 193 : 265 275.
44. Marques A, Keil U, Bonert A, Steiner B, Haass C, Müller WE et al. (2003). Neurotoxic mechanisms caused by the Alzheimer's disease-linked Swedisch amyloid precursor protein mutation: oxidative stress, caspases, and the JNK pathway. J Biol Chem 278 : 28294 28302. (Pubitemid 36900031)
45. Mattson MP (2007). Mitochondrial regulation of neuronal plasticity. Neurochem Res 32 : 707 715.
46. Mattson MP, Magnus T (2006). Ageing and neuronal vulnerability. Nature 7 : 278 294.
47. Müller WE, Koch S, Scheuer D, Rostock A, Bartsch R (1997). Effects of piracetam on membrane fluidity in the aged mouse, rat, and human brain. Biochem Pharmacol 53 : 135 140. (Pubitemid 27013468)
48. Müller WE, Eckert GP, Eckert A (1999). Piracetam: novelty in a unique mode of action. Pharmacopsychiatry 32 (Suppl. 1 2 9.
49. Naftalin RJ, Cunningham P, Afzal-Ahmed I (2004). Piracetam and TRH analogues antagonise inhibition by barbiturates, diazepam, melatonin and galanin of human erythrocyte D-glucose transport. Br J Pharmacol 142 : 594 608. (Pubitemid 38869874)
50. Pereira C, Santos MS, Oliveira C (1999). Involvement of oxidative stress on the impairment of energy metabolism induced by A beta peptides on PC12 cells: protection by antioxidants. Neurobiol Dis 6 : 209 219. (Pubitemid 29297822)
51. Peters I, Igbavboa U, Schütt T, Haidari S, Hartig U, Böttner S et al. (2009). The interaction of beta-amyloid protein with cellular membranes stimulates its own production. Biochim Biophys Acta 1788 : 964 972.
52. Petratos A, Li XQ, George AJ, Hou X, Kerr LM, Unabia SE et al. (2008). The ß-amyloid protein of Alzheimer's disease increases neuronal CRMP-2 phosphorylation by a Rho-GTP mechanism. Brain 131 : 90 108.
53. Reddy PH, Beal IMF (2008). Amyloid beta, mitochondrial dysfunction and synaptic damage: implications for cognitive decline in aging and Alzheimer's disease. Trends Mol Med 14 : 45 53.
54. Riha PD, Bruchex AK, Echevarria DJ, Gonzalez-Lima F (2005). Memory facilitation by methylene blue: dose-dependent effect on behaviour and brain oxygen consumption. Eur J Pharmacol 511 : 151 158. (Pubitemid 40417721)
55. Saletu G, Hitzenberger G, Grunberger J, Anderer P, Zyhlarz G, Linzmayer L et al. (1995). Double-blind, placebo-controlled, pharmacokinetic and-dynamic studies with 2 new formulations of piracetam (infusion and sirup) under hypoxia in man. Int J Clin Pharmacol Ther 33 : 249 262.
56. Sastre J, Pallardo FV, Vina J (2003). The role of mitochondrial oxidative stress in aging. Free Radic Biol Med 35 : 1 8. (Pubitemid 36782332)
57. Scheuer K, Rostock A, Bartsch R, Müller WE (1999). Piracetam improves cognitive performance by restoring neurochemical deficits of the aged rat brain. Pharmacopsychiatry 32 (Suppl. 1 10 16.
58. Schon EA, Manfredi G (2003). Neuronal degeneration and mitochondrial dysfunction. J Clin Invest 111 : 303 312. (Pubitemid 36182203)
59. Selkoe DJ (2002). Alzheimer's disease is a synaptic failure. Science 278 : 789 791.
60. Shankar GM, Ki S, Mehta TH, Garcia-Munoz A, Shepardson NE, Smith I et al. (2008). Amyloid-ß protein dimers isolated directly from Alzheimers's brains impairs synaptic plasticity and memory. Nature Med 14 : 837 842.
61. Smith Am, Wehner JM (2002). Aniracetam improves contextual fear conditioning and increases hippocampal γ-PKC activation. Hippocampus 12 : 76 85. (Pubitemid 34211249)
62. Stine WB, Dahlgren KN, Krafft GA, Ladu MJ (2003). In vitro characterization conditions for amyloid-beta peptide oligomerization and fibrillogenesis. J Biol Chem 278 : 11612 11622.
63. Stoll L, Schubert T, Müller WE (1992). Age-related deficits of central muscarinic cholinergic receptor function in the mouse: partial restoration by chronic piracetam treatment. Neurobiol Aging 1 : 39 44.
64. Szelies G, Mielke R, Kessler J, Heiss WD (2001). Restitution of alpha-topography by piracetam in post-stroke aphasie. Int J Clin Pharmacol Ther 39 : 152 157. (Pubitemid 32280139)
65. Terry RD, Masliah E, Salmon DP, Butters N, Deteresa R, Hill R et al. (1991). Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann Neuro 30 (4 572 580.
66. Uebelhack R, Vohs D, Zytowski M, Schewe HJ, Koch C, Konertz W (2003). Effects of piracetam on cognitive performance in patients undergoing bypass surgery. Pharmacopsychiatry 36 : 89 93. (Pubitemid 36791782)
67. Valzelli L, Bernasconi S, Sala A (1980). Piracetam activity may differ according to the age of the recipient mouse. Int Pharmacopsychiatry 15 : 150 156. (Pubitemid 11145006)
68. Villard V, Espallergues J, Keller E, Alkam T, Nitta A, Yamada K et al. (2009). Anitamnesic and neuroprotective effects of the aminotetrahydrofuran derivative ANAVEXI-41 against amyloid Aß(25-35)-induced toxicity in mice. Neuropsychopharmacology 34 : 1552 1566.
69. Waegemans T, Wilsher CR, Danniau A, Ferris SH, Kurz A, Winblad B (2002). Clinical efficacy of piracetam in cognitive impairment: a meta-analysis. Dement Geriatr Cogn Disord 13 : 217 224. (Pubitemid 34507607)
70. Walsh DM, Selkoe DJ (2007). Aß oligomers - a decade of discovery. J Neurochem 101 : 1172 1184.
71. Xerri C, Zennou-Azogui Y (2003). Influence of the postlesion environment and chronic piracetam treatment on the organization of the somatotopic map in the rat primary somatosensory cortex after focal cortical injury. Neuroscience 118 : 161 177. (Pubitemid 36369540)