Endomorphin-2, an endogenous tetrapeptide, protects against Aβ1-42 in vitro and in vivo

FASEB Journal

Volumn 20, Issue 8, 2006, Pages

  Szegedi, Viktor ^a   Juhá, Gábor ^a   Rózsa, Éva ^a   Juhász Vedres, Gabriella ^a   Datki, Zsolt ^a   Fülöp, Lívia ^a   Bozsó, Zsolt ^a   Lakatos, Andrea ^a   Laczkó, Ilona ^b   Farkas, Tamás ^a   Kis, Zsolt ^a   Tóth, Géza ^b   Soós, Katalin ^a   Zarándi, Márta ^a   Budai, Dénes ^a   Toldi, József ^a   Penke, Botond ^a  

^a UNIVERSITY OF SZEGED   (Hungary)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

Alzheimer's disease; Circular dichroism; Fibrillogenesis; Rat; Single unit; Transmission electronmicroscopy

Indexed keywords

3 (4,5 DIMETHYLTHIAZOLYL 2) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; AMYLOID BETA PROTEIN[1-42]; BROMINE DERIVATIVE; ENDOMORPHIN 2; ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; N METHYL DEXTRO ASPARTIC ACID; TETRAPEPTIDE; TRITIUM; AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN (1 42); AMYLOID BETA-PROTEIN (1-42); N METHYLASPARTIC ACID; NEUROPROTECTIVE AGENT; OLIGOPEPTIDE; PEPTIDE FRAGMENT;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING ASSAY; CIRCULAR DICHROISM; CONCENTRATION RESPONSE; CONTROLLED STUDY; ELECTRON MICROSCOPY; ELECTROPHYSIOLOGY; EVOKED RESPONSE; IN VITRO STUDY; IN VIVO STUDY; LIGHT SCATTERING; NEUROMODULATION; NONHUMAN; OXIDATION REDUCTION REACTION; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; RAT; ANIMAL; CELL CULTURE; CELL SURVIVAL; CHEMISTRY; DRUG ANTAGONISM; DRUG EFFECT; EXCITATORY POSTSYNAPTIC POTENTIAL; IONTOPHORESIS; LIGHT; METABOLISM; NERVE CELL; PHYSIOLOGY; RADIATION SCATTERING; RADIOASSAY; TRANSMISSION ELECTRON MICROSCOPY; TUMOR CELL LINE; ULTRASTRUCTURE; WISTAR RAT;

AMYLOID BETA-PROTEIN; ANIMALS; CELL LINE, TUMOR; CELL SURVIVAL; CELLS, CULTURED; CIRCULAR DICHROISM; ENKEPHALIN, ALA(2)-MEPHE(4)-GLY(5)-; EVOKED POTENTIALS; EXCITATORY POSTSYNAPTIC POTENTIALS; IONTOPHORESIS; LIGHT; MICROSCOPY, ELECTRON, TRANSMISSION; N-METHYLASPARTATE; NEURONS; NEUROPROTECTIVE AGENTS; OLIGOPEPTIDES; PEPTIDE FRAGMENTS; RADIOLIGAND ASSAY; RATS; RATS, WISTAR; SCATTERING, RADIATION;

EID: 33845614389     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.05-4891fje     Document Type: Article

References (57)

1. Lahiri, D. K., Farlow, M. R., Sambamurti, K., Greig, N. H., Giacobini, E., and Schneider, L. S. (2003) A critical analysis of new molecular targets and strategies for drug developments in Alzheimer's disease. Curr. Drug Targets 4, 97-112
2. Selkoe, D. J. (2001) Alzheimer's disease: genes, proteins, and therapy. Physiol. Rev. 81, 741-766
3. Rocchi, A., Pellegrini, S., Siciliano, G., and Murri, L. (2003) Causative and susceptibility genes for Alzheimer's disease: a review. Brain Res. Bull. 61, 1-24
4. Phinney, A. L., Horne, P., Yang, J., Janus, C., Bergeron, C., and Westaway, D. (2003) Mouse models of Alzheimer's disease: the long and filamentous road. Neurol. Res. 25, 590-600
5. Hardy, J., and Allsop, D. (1991) Amyloid deposition as the central event in the aetiology of Alzheimer's disease. Trends Pharmacol. Sci. 12, 383-388
6. Lambert, M. P., Stevens, G., Sabo, S., Barber, K., Wang, G., Wade, W., Krafft, G., Snyder, S., Holzman, T. F., and Klein, W. L. (1994) Beta/A4-evoked degeneration of differentiated SH-SY5Y human neuroblastoma cells. J. Neurosci. Res. 39, 377-385
7. Datki, Z., Juhasz, A., Galfi, M., Soos, K., Papp, R., Zadori, D., and Penke, B. (2003) Method for measuring neurotoxicity of aggregating polypeptides with the MTT assay on differentiated neuroblastoma cells. Brain Res. Bull. 62, 223-229
8. Harkany, T., Abraham, I., Timmerman, W., Laskay, G., Toth, B., Sasvari, M., Konya, C., Sebens, J. B., Korf, J., Nyakas, C., et al. (2000) beta-amyloid neurotoxicity is mediated by a glutamate-triggered excitotoxic cascade in rat nucleus basalis. Eur. J. Neurosci. 12, 2735-2745
9. Nitta, A., Fukuta, T., Hasegawa, T., and Nabeshima, T. (1997) Continuous infusion of beta-amyloid protein into the rat cerebral ventricle induces learning impairment and neuronal and morphological degeneration. Jpn. J. Pharmacol. 73, 51-57
10. Yu, S. P., Farhangrazi, Z. S., Ying, H. S., Yeh, C. H., and Choi, D. W. (1998) Enhancement of outward potassium current may participate in beta-amyloid peptide-induced cortical neuronal death. Neurobiol. Dis. 5, 81-88
11. Bores, G. M., Smith, C. P., Wirtz-Brugger, F., and Giovanni, A. (1998) Amyloid beta-peptides inhibit Na+/K+-ATPase: tissue slices versus primary cultures. Brain Res. Bull. 46, 423-427
12. Palotas, A., Kalman, J., Palotas, M., Juhasz, A., Janka, Z., and Penke, B. (2002) Beta-amyloid-induced increase in the resting intracellular calcium concentration gives support to tell Alzheimer lymphocytes from control ones. Brain Res. Bull. 58, 203-205
13. Fukuyama, R., Wadhwani, K. C., Galdzicki, Z., Rapoport, S. I., and Ehrenstein, G. (1994) beta-Amyloid polypeptide increases calcium-uptake in PC12 cells: a possible mechanism for its cellular toxicity in Alzheimer's disease. Brain Res. 667, 269-272
14. Ito, E., Oka, K., Etcheberrigaray, R., Nelson, T. J., McPhie, D. L., Tofel-Grehl, B., Gibson, G. E., and Alkon, D. L. (1994) Internal Ca2+ mobilization is altered in fibroblasts from patients with Alzheimer disease. Proc. Natl. Acad. Sci. U. S. A. 91, 534-538
15. Trommer, B. L., Shah, C., Yun, S. H., Gamkrelidze, G., Pasternak, E. S., Blaine Stine, W., Manelli, A., Sullivan, P., Pasternak, J. F., and LaDu, M. J. (2005) ApoE isoform-specific effects on LTP: blockade by oligomeric amyloid-beta1- 42. Neurobiol. Dis. 18, 75-82
16. Molnar, Z., Soos, K., Lengyel, I., Penke, B., Szegedi, V., and Budai, D. (2004) Enhancement of NMDA responses by betaamyloid peptides in the hippocampus in vivo. Neuroreport. 15, 1649-1652
17. Szegedi, V., Fulop, L., Farkas, T., Rozsa, E., Robotka, H., Kis, Z., Penke, Z., Horvath, S., Molnar, Z., Datki, Z., et al. (2005) Pentapeptides derived from Abeta 1-42 protect neurons from the modulatory effect of Abeta fibrils-an in vitro and in vivo electrophysiological study. Neurobiol. Dis. 18, 499-508
18. Stephan, A., Laroche, S., and Davis, S. (2001) Generation of aggregated beta-amyloid in the rat hippocampus impairs synaptic transmission and plasticity and causes memory deficits. J. Neurosci. 21, 5703-5714
19. Chen, Q. S., Kagan, B. L., Hirakura, Y., and Xie, C. W. (2000) Impairment of hippocampal long-term potentiation by Alzheimer amyloid beta-peptides. J. Neurosci. Res. 60, 65-72
20. Pike, C. J., Burdick, D., Walencewicz, A. J., Glabe, C. G., and Cotman, C. W.(1993) Neurodegeneration induced by betaamyloid peptides in vitro: the role of peptide assembly state. J. Neurosci. 13, 1676-1687
21. Soto, C. (1999) Plaque busters: strategies to inhibit amyloid formation in Alzheimer's disease. Mol. Med. Today 5, 343-350
22. Tjernberg, L. O., Naslund, J., Lindqvist, F., Johansson, J., Karlstrom, A. R., Thyberg, J., Terenius, L., and Nordstedt, C. (1996) Arrest of beta-amyloid fibril formation by a pentapeptide ligand. J. Biol. Chem. 271, 8545-8548
23. Soto, C., Kindy, M. S., Baumann, M., and Frangione, B. (1996) Inhibition of Alzheimer's amyloidosis by peptides that prevent beta-sheet conformation. Biochem. Biophys. Res. Commun. 226, 672-680
24. Pappolla, M., Bozner, P., Soto, C., Shao, H., Robakis, N. K., Zagorski, M., Frangione, B., and Ghiso, J. (1998) Inhibition of Alzheimer beta-fibrillogenesis by melatonin. J. Biol. Chem. 273, 7185-7188
25. Permanne, B., Adessi, C., Saborio, G. P., Fraga, S., Frossard, M. J., Van Dorpe, J., Dewachter, I., Banks, W. A., Van Leuven, F., and Soto, C. (2002) Reduction of amyloid load and cerebral damage in a transgenic mouse model of Alzheimer's disease by treatment with a beta-sheet breaker peptide. FASEB J. 16, 860-862
26. Zadina, J. E., Hackler, L., Ge, L. J., and Kastin, A. J. (1997) A potent and selective endogenous agonist for the mu-opiate receptor. Nature 386, 499-502
27. Martin-Schild, S., Gerall, A. A., Kastin, A. J., and Zadina, J. E. (1999) Differential distribution of endomorphin 1- and endomorphin 2-like immunoreactivities in the CNS of the rodent. J. Comp. Neurol. 405, 450-471
28. Zadina, J. E., Martin-Schild, S., Gerall, A. A., Kastin, A. J., Hackler, L., Ge, L. J., and Zhang, X. (1999) Endomorphins: novel endogenous mu-opiate receptor agonists in regions of high mu-opiate receptor density. Ann. N. Y. Acad. Sci. 897, 136-144
29. Joachim, C., Games, D., Morris, J., Ward, P., Frenkel, D., and Selkoe, D. (1991) Antibodies to non-beta regions of the betaamyloid precursor protein detect a subset of senile plaques. Am. J. Pathol. 138, 373-384
30. Games, D., Adams, D., Alessandrini, R., Barbour, R., Berthelette, P., Blackwell, C., Carr, T., Clemens, J., Donaldson, T., Gillespie, F., et al. (1995) Alzheimer-type neuropathology in transgenic mice overexpressing V717F beta-amyloid precursor protein. Nature 373, 523-527
31. Hsiao, K., Chapman, P., Nilsen, S., Eckman, C., Harigaya, Y., Younkin, S., Yang, F., and Cole, G. (1996) Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 274, 99-102
32. Lin, X., Yang, D. J., Cai, W. Q., Zhao, Q. Y., Gao, Y. F., Chen, Q., and Wang, R. (2003) Endomorphins, endogenous opioid peptides, provide antioxidant defense in the brain against free radical-induced damage. Biochim. Biophys. Acta 1639, 195-202
33. Liao, S. L., Chen, W. Y., Raung, S. L., and Chen, C. J. (2003) Neuroprotection of naloxone against ischemic injury in rats: role of mu receptor antagonism. Neurosci. Lett. 345, 169-172
34. Iglesias, M., Segura, M. F., Comella, J. X., and Olmos, G. (2003) Mu-opioid receptor activation prevents apoptosis following serum withdrawal in differentiated SH-SY5Y cells and cortical neurons via phosphatidylinositol 3-kinase. Neuropharmacology 44, 482-492
35. Budai, D. (2004) Ultralow-noise headstage and main amplifiers for extracellular spike recording. Acta Biol. Szeged 48, 13-17
36. Vass, E., Hollosi, M., Besson, F., and Buchet, R. (2003) Vibrational spectroscopic detection of beta- and gamma-turns in synthetic and natural peptides and proteins. Chem. Rev. 103, 1917-1954
37. Datki, Z., Papp, R., Zadori, D., Soos, K., Fulop, L., Juhasz, A., Laskay, G., Hetenyi, C., Mihalik, E., Zarandi, M., and Penke, B. (2004) In vitro model of neurotoxicity of Abeta 1-42 and neuroprotection by a pentapeptide: irreversible events during the first hour. Neurobiol. Dis. 17, 507-515
38. Wogulis, M., Wright, S., Cunningham, D., Chilcote, T., Powell, K., and Rydel, R. E. (2005) Nucleation-dependent polymerization is an essential component of amyloid-mediated neuronal cell death. J. Neurosci. 25, 1071-1080
39. Shearman, M. S., Ragan, C. I., and Iversen, L. L. (1994) Inhibition of PC12 cell redox activity is a specific, early indicator of the mechanism of beta-amyloid-mediated cell death. Proc. Natl. Acad. Sci. U. S. A. 91, 1470-1474
40. Yao, P. J., Zhu, M., Pyun, E. I., Brooks, A. I., Therianos, S., Meyers, V. E., and Coleman, P. D. (2003) Defects in expression of genes related to synaptic vesicle trafficking in frontal cortex of Alzheimer's disease. Neurobiol. Dis. 12, 97-109
41. Selkoe, D. J. (2004) Cell biology of protein misfolding: the examples of Alzheimer's and Parkinson's diseases. Nat. Cell Biol. 6, 1054-1061
42. Szegedi, V., Juhasz, G., Budai, D., and Penke, B. (2005) Divergent effects of Abeta1-42 on ionotropic glutamate receptor-mediated responses in CA1 neurons in vivo. Brain Res. 1062, 120-126
43. Hertel, C., Hauser, N., Schubenel, R., Seilheimer, B., and Kemp, J. A. (1996) Beta-amyloid-induced cell toxicity: enhancement of 3-(4,5- dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide-dependent cell death. J. Neurochem. 67, 272-276
44. Liu, Y., and Schubert, D. (1997) Cytotoxic amyloid peptides inhibit cellular 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) reduction by enhancing MTT formazan exocytosis. J. Neurochem. 69, 2285-2293
45. Chacon, M. A., Barria, M. I., Soto, C., and Inestrosa, N. C. (2004) Beta-sheet breaker peptide prevents Abeta-induced spatial memory impairments with partial reduction of amyloid deposits. Mol. Psychiatry 9, 953-961
46. Klein, W. L., Krafft, G. A., and Finch, C. E. (2001) Targeting small Abeta oligomers: the solution to an Alzheimer's disease conundrum? Trends Neurosci. 24, 219-224
47. Walsh, D. M., and Selkoe, D. J. (2004) Deciphering the molecular basis of memory failure in Alzheimer's disease. Neuron 44, 181-193
48. El Khoury, J., Hickman, S. E., Thomas, C. A., Cao, L., Silverstein, S. C., and Loike, J. D. (1996) Scavenger receptor-mediated adhesion of microglia to beta-amyloid fibrils. Nature 382, 716-719
49. Muehlhauser, F., Liebl, U., Kuehl, S., Walter, S., Bertsch, T., and Fassbender, K. (2001) Aggregation-Dependent interaction of the Alzheimer's beta-amyloid and microglia. Clin. Chem. Lab. Med. 39, 313-316
50. Luhrs, T., Ritter, C., Adrian, M., Riek-Loher, D., Bohrmann, B., Dobeli, H., Schubert, D., and Riek, R. (2005) 3D structure of Alzheimer's amyloid-{beta}(1-42) fibrils. Proc. Natl. Acad. Sci. U. S. A. 102, 17342-17347
51. Barghorn, S., Nimmrich, V., Striebinger, A., Krantz, C., Keller, P., Janson, B., Bahr, M., Schmidt, M., Bitner, R. S., Harlan, J., Barlow, E., Ebert, U., and Hillen, H. (2005) Globular amyloid beta-peptide oligomer - a homogenous and stable neuropathological protein in Alzheimer's disease. J. Neurochem. 95, 834-847
52. Malmo, C., Vilasi, S., Iannuzzi, C., Tacchi, S., Cametti, C., Irace, G., and Sirangelo, I. (2005) Tetracycline inhibits W7FW14F apomyoglobin fibril extension and keeps the amyloid protein in a prefibrillar, highly cytotoxic state. FASEB J. 20, 346-347
53. Louzada, P. R., Lima, A. C., Mendonca-Silva, D. L., Noel, F., De Mello, F. G., and Ferreira, S. T. (2004) Taurine prevents the neurotoxicity of beta-amyloid and glutamate receptor agonists: activation of GABA receptors and possible implications for Alzheimer's disease and other neurological disorders. FASEB J. 18, 511-518
54. Savvateeva, E. V., Popov, A. V., Kamyshev, N. G., Iliadi, K. G., Bragina, J. V., Heisenberg, M., Kornhuber, J., and Riederer, P. (1999) Age-dependent changes in memory and mushroom bodies in the Drosophila mutant vermilion deficient in the kynurenine pathway of tryptophan metabolism. Rosss Fiziols Zhs Ims IM Sechenova 85, 167-183
55. Drake, C. T., and Milner, T. A. (2002) Mu opioid receptors are in discrete hippocampal interneuron subpopulations. Hippocampus 12, 119-136
56. Drake, C. T., and Milner, T. A. (1999) Mu opioid receptors are in somatodendritic and axonal compartments of GABAergic neurons in rat hippocampal formation. Brain Res. 849, 203-215
57. McQuiston, A. R., and Saggau, P. (2003) Mu-opioid receptors facilitate the propagation of excitatory activity in rat hippocampal area CA1 by disinhibition of all anatomical layers. J. Neurophysiol. 90, 1936-1948