Calpain inhibition prevents amyloid-β-induced neurodegeneration and associated behavioral dysfunction in rats

Neuropharmacology

Volumn 59, Issue 4-5, 2010, Pages 334-342

  Granic, Ivica ^a,b   Nyakas, Csaba ^a,c   Luiten, Paul G M ^a   Eisel, Ulrich L M ^a   Halmy, László G ^c   Gross, Gerhard ^d   Schoemaker, Hans ^d   Möller, Achim ^d   Nimmrich, Volker ^d  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b RADBOUD UNIVERSITY   (Netherlands)

^c INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^d ABBOTT GMBH AND CO KG   (Germany)

Author keywords

Amyloid ; Calpain; Excitotoxicity; Neurodegeneration; Nucleus basalis

Indexed keywords

A 705253; AMYLOID BETA PROTEIN; CALPASTATIN; CHOLINE ACETYLTRANSFERASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; BRAIN CORTEX; BRAIN DAMAGE; CELL ACTIVATION; CHOLINERGIC NERVE CELL; COGNITIVE DEFECT; CONTROLLED STUDY; DOSE RESPONSE; DRUG EFFICACY; EMBRYO; ENZYME ANALYSIS; EXCITOTOXICITY; FEMALE; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; MAGNOCELLULAR NUCLEUS; MALE; MICROGLIA; NERVE DEGENERATION; NERVE PROJECTION; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NONHUMAN; OLIVARY NUCLEUS; OPEN FIELD BEHAVIOR; PATTERN RECOGNITION; PRIORITY JOURNAL; RAT;

AMYLOID BETA-PEPTIDES; ANIMALS; BENZAMIDES; CALPAIN; CELLS, CULTURED; EXPLORATORY BEHAVIOR; FEMALE; GLYCOPROTEINS; MALE; MICE; MICE, INBRED C57BL; NERVE DEGENERATION; NEUROPROTECTIVE AGENTS; PEPTIDE FRAGMENTS; RATS; RATS, WISTAR;

EID: 77955925669     PISSN: 00283908     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2010.07.013     Document Type: Article

References (46)

1. Bartus R.T., Dean R.L., Beer B., Lippa A.S. The cholinergic hypothesis of geriatric memory dysfunction. Science 1982, 217:408-414.
2. Battaglia F., Trinchese F., Liu S., Walter S., Nixon R.A., Arancio O. Calpain inhibitors, a treatment for Alzheimer's disease. J. Mol. Neurosci. 2003, 20:357-362.
3. Blokland A. Acetylcholine: a neurotransmitter for learning and memory?. Brain Res. Brain Res. Rev. 1995, 21:285-300.
4. Caba E., Brown Q.B., Kawasaki B., Bahr B.A. Peptidyl alpha-keto amide inhibitor of calpain blocks excitotoxic damage without affecting signal transduction events. J. Neurosci. Res. 2002, 67:787-794.
5. Chiu K., Lam T.T., Li W.W.Y., Caprioli J., Kwong J.M.K. Calpain and N-methyl-d-aspartate (NMDA)-induced excitotoxicity in rat retinas. Brain Res. 2005, 1046:207-215.
6. Cribbs D.H., Poon W.W., Rissman R.A., Blurton-Jones M. Caspase-mediated degeneration in Alzheimer's disease. Am. J. Pathol. 2004, 165:353-355.
7. Dahlgren K.N., Manelli A.M., Stine W.B., Baker L.K., Krafft G.A., LaDu M.J. Oligomeric and fibrillar species of amyloid-beta peptides differentially affect neuronal viability. J. Biol. Chem. 2002, 277:32046-32053.
8. De Felice F.G., Velasco P.T., Lambert M.P., Viola K., Fernandez S.J., Ferreira S.T., Klein W.L. Abeta oligomers induce neuronal oxidative stress through an NMDA receptor-dependent mechanism that is blocked by the Alzheimer's drug memantine. J. Biol. Chem. 2007, 282:11590-11601.
9. Dolga A.M., Granic I., Nijholt I.M., Nyakas C., van der Zee E.A., Luiten P.G., Eisel U.L., 2009. Pretreatment with lovastatin prevents N-methyl-d-aspartate-induced neurodegeneration in the magnocellular nucleus basalis and behavioral dysfunction. J. Alzheimers Dis. (E-pub ahead of print).
10. Gaykema R.P., Nyakas C., Horvath E., Hersh L.B., Majtenyi C., Luiten P.G. Cholinergic fiber aberrations in nucleus basalis lesioned rat and Alzheimer's disease. Neurobiol. Aging 1992, 13:441-448.
11. Goll D.E., Thompson V.F., Li H., Wei W., Cong J. The calpain system. Physiol. Rev. 2003, 83:731-801.
12. Gong Y., Chang L., Viola K.L., Lacor P.N., Lambert M.P., Finch C.E., Krafft G.A., Klein W.L. Alzheimer's disease-affected brain: presence of oligomeric A beta ligands (ADDLs) suggests a molecular basis for reversible memory loss. PNAS 2003, 100:10417-10422.
13. Harkany T., Abrahám I., Timmerman W., Laskay G., Tóth B., Sasvári M., Kónya C., Sebens J.B., Korf J., Nyakas C., Zarándi M., Soós K., Penke B., Luiten P.G. β-amyloid neurotoxicity is mediated by a glutamate-triggered excitotoxic cascade in rat nucleus basalis. Eur. J. Neurosci. 2000, 12:2735-2745.
14. Harkany T., Mulder J., Horvath K.M., Keijser J., van der Meeberg E.K., Nyakas C., Luiten P.G.M. Oral post-lesion administration of 5-HT(1A) receptor agonist repinotan hydrochloride (BAY×3702) attenuates NMDA-induced delayed neuronal death in rat magnocellular nucleus basalis. Neuroscience 2001, 108:629-642.
15. Horváth K.M., Ábrahám I.M., Harkány T., Meerlo P., Bohus B.G.J., Nyakas C., Luiten P.G.M. Postnatal treatment with ACTH-(4-9) analog ORG 2766 attenuates N-methyl-d-aspartate-induced excitotoxicity in rat nucleus basalis in adulthood. Eur. J. Pharmacol. 2000, 405:33-42.
16. Hou S.T., Jiang S.X., Desbois A., Huang D., Kelly J., Tessier L., Karchewski L., Kappler J. Calpain-cleaved collapsing response mediator-protein 3 induces neuronal death after glutamate toxicity and cerebral ischemia. J. Neurosci. 2006, 26:2241-2249.
17. Huang Y., Wang K.W. The calpain family and human disease. Trends Mol. Med. 2001, 7:355-362.
18. Kelly B.L., Vassar R., Ferreira A. β-amyloid-induced dynamin 1 depletion in hippocampal neurons. J. Biol. Chem. 2005, 280:31746-31753.
19. Kelly B.L., Ferreira A. β-amyloid-induced dynamin 1 degradation is mediated by N-methyl-d-aspartate receptors in hippocampal neurons. J. Biol. Chem. 2006, 281:28079-28089.
20. Lacor P.N., Bruniel M.C., Furlow P.W., Sanz Clemente A., Velasco P.T., Wood M., Viola K.L., Klein W.L. Aβ oligomer-induced aberrations in synapse composition, shape, and density provide a molecular basis for loss of connectivity in Alzheimer's disease. J. Neurosci. 2007, 27:796-807.
21. 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., Wals P., Zhang C., Finch C.E., Krafft G.A. Diffusable, nonfibrillar ligands derived from Aβ1-42 are potent central nervous system neurotoxins. PNAS 1998, 95:6448-6453.
22. Lipton S.A., Rosenberg P.A. Excitatory amino acids as a final common pathway for neurologic disorders. N. Engl. J. Med. 1994, 330:613-622.
23. Lubisch W., Beckenbach E., Boppp S., Hofmann H.-P., Kartal A., Kästel C., Lindner T., Metz-Garrecht M., Reeb J., Regner F., Vierling M., Möller A. Benzoylalanine-derived ketoamines carrying venylbenzyl amino residues: discovery of potent water-soluble calpain inhibitors with oral bioavailability. J. Med. Chem. 2003, 46:2404-2412.
24. 2+ antagonist nimodipine, influence of aging and developmental drug treatment. Neurodegeneration 1995, 4:307-314.
25. Mattson M.P., LaFerla F.M., Chan S.L., Leissring M.A., Shepel P.N., Geiger J.D. Calcium signaling in the ER: its role in neuronal plasticity and neurodegenerative disorders. Trends Neurosci. 2000, 23:222-229.
26. Mattson M.P. Pathways towards and away from Alzheimer's disease. Nature 2004, 430:631-639.
27. Molnár Z., Soós K., Lengyel I., Penke B., Szegedi V., Budai D. Enhancement of NMDA responses by beta-amyloid peptides in the hippocampus in vivo. Neuroreport 2004, 15:1649-1652.
28. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 1983, 65:55-63.
29. Neuhof C., Götte O., Trumbeckaite S., Attenberger M., Kuzkaya N., Gellerich F., Möller A., Lubisch W., Speth M., Tillmanns H., Neuhof H. A novel water-soluble and cell-permeable calpain inhibitor protects myocardial and mitochondrial function in postischemic reperfusion. Biol. Chem. 2003, 384:1597-1603.
30. Neuhof C., Fabiunke V., Deibele K., Speth M., Möller A., Lubisch W., Fritz H., Tillmanns H., Neuhof H. Reduction of myocardial infarction by calpain inhibitors A-705239 and A-705253 in isolated perfused rabbit hearts. Biol. Chem. 2004, 385:1077-1082.
31. Nimmrich V., Szabo R., Nyakas C., Granic I., Reymann K.G., Schröder U.H., Gross G., Schoemaker H., Wicke K., Möller A., Luiten P. Inhibition of calpain prevents N-methyl-D-aspartate-induced degeneration of the nucleus basalis and associated behavioral dysfunction. J. Pharmacol. Exp. Ther. 2008, 327:343-352.
32. Nyakas C., Felszeghy K., Szabó R., Keijser J.N., Luiten P.G., Szombathelyi Z., Tihanyi K. Neuroprotective effects of vinpocetine and its major metabolite cis-apovincaminic acid on NMDA-induced neurotoxicity in a rat entorhinal cortex lesion model. CNS Neurosci. Ther. 2009, 15:89-99.
33. Pan T., Kondo S., Le W., Jankovic J. The role of autophagy-lysosome pathway in neurodegenration associated with Parkinson's disease. Brain 2008, 131:1969-1978.
34. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 1986, Academic Press, San Diego.
35. Ray S.K., Karmakar S., Nowak M.W., Banik N.L. Inhibition of calpain and caspase-3 prevented apoptosis and preserved electrophysiological properties of voltage-gated and ligand-gated ion channels in rat primary cortical neurons exposed to glutamate. Neuroscience 2006, 139:577-595.
36. Rubinsztein D.C. The roles of intracellular protein-degradation pathways in neurodegeneration. Nature 2006, 443:780-786.
37. Shankar G.M., Bloodgood B.L., Townsend M., Walsh D.M., Selkoe D.J., Sabatini B.L. Natural oligomers of the Alzheimer amyloid-beta protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signaling pathway. J. Neurosci. 2007, 27:2866-2875.
38. Saez M.E., Ramirez-Lorca R., Moron F.J., Ruiz A. The therapeutic potential of the calpain family: new aspects. Drug Discov. Today 2006, 11:917-923.
39. Selkoe D.J. Soluble oligomers of the amyloid beta-protein impair synaptic plasticity and behavior. Behav. Brain Res. 2008, 192:106-113.
40. Stine W.B., Dahlgreen K.N., Krafft G.A., Jo LaDU M. In vitro characterization of conditions for amyloid-beta peptide oligomerization and fibrillogenesis. J. Biol. Chem. 2003, 278:11612-11622.
41. Takano J., Tomioka M., Tsubuki S., Higuchi M., Iwata N., Itohara S., Maki M., Saido T.C. Calpain mediates excitotoxic DNA fragmentation via mitochondrial pathways in adult brains: evidence from calpastatin-mutant mice. J. Biol. Chem. 2005, 280:16175-16184.
42. Trommer B.L., Shah C., Yun S.H., Gamkrelidze G., Pasternak E.S., Stine W.B., Manelli A., Sullivan P., Pasternak J.F., LaDu M.J. ApoE isoform-specific effects on LTP: blockade by oligomeric amyloid-beta1-42. Neurobiol. Dis. 2005, 18:75-82.
43. Van der Zee E.A., Luiten P.G. Muscarinic acetylcholine receptors in the hippocampus, neocortex and amygdala: a review of immunocytochemical localization in relation to learning and memory. Prog. Neurobiol. 1999, 58:409-471.
44. Walsh D.M., Selkoe D.J. Aβ oligomers - a decade of discovery. J. Neurochem. 2007, 101:1172-1184.
45. Wu H.Y., Tomizawa K., Oda Y., Wei F.Y., Lu Y.F., Matsushita M., Li S.T., Moriwaki A., Matsui H. Critical role of calpain-mediated cleavage of calcineurin in excitotoxic neurodegeneration. J. Biol. Chem. 2004, 279:4929-4940.
46. Zatz M., Starling A. Calpains and disease. N. Engl. J. Med. 2005, 352:2413-2423.