Amyloid-beta (Aβ1-42)-induced paralysis in Caenorhabditis elegans is inhibited by the polyphenol quercetin through activation of protein degradation pathways

Molecular Nutrition and Food Research

Volumn 58, Issue 10, 2014, Pages 1931-1940

  Regitz, Charlotte ^a   Dußling, Lisa Marie ^a   Wenzel, Uwe ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Alzheimer's disease; Amyloid peptide; Autophagy; Caenorhabditis elegans; Proteasome; Unfolded protein response

Indexed keywords

CAENORHABDITIS ELEGANS;

AMYLOID BETA PROTEIN; AMYLOID BETA-PROTEIN (1-42); ANTIOXIDANT; CAENORHABDITIS ELEGANS PROTEIN; NERVE PROTEIN; PEPTIDE FRAGMENT; PROTEASOME; QUERCETIN;

ALZHEIMER DISEASE; ANIMAL; ANTAGONISTS AND INHIBITORS; AUTOPHAGY; CAENORHABDITIS ELEGANS; CHEMICALLY INDUCED; COMPARATIVE STUDY; DIET SUPPLEMENTATION; DISEASE MODEL; ENZYMOLOGY; GENETICS; HUMAN; LYSOSOME; METABOLISM; MUSCLE; PARALYSIS; PROTEIN AGGREGATION, PATHOLOGICAL; PROTEIN DEGRADATION; RNA INTERFERENCE; TRANSGENIC ANIMAL; UNFOLDED PROTEIN RESPONSE;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTIOXIDANTS; AUTOPHAGY; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DIETARY SUPPLEMENTS; DISEASE MODELS, ANIMAL; HUMANS; LYSOSOMES; MUSCLES; NERVE TISSUE PROTEINS; PARALYSIS; PEPTIDE FRAGMENTS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN AGGREGATION, PATHOLOGICAL; PROTEOLYSIS; QUERCETIN; RNA INTERFERENCE; UNFOLDED PROTEIN RESPONSE;

EID: 84908513705     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201400014     Document Type: Article

References (58)

1. Querfurth, H.W., LaFerla, F. M., Alzheimer's disease. N. Engl. J. Med. 2012, 362, 329-344.
2. Penke, B., Tóth, A. M., Földi, I., Szucs, M., Janáky, T., Intraneuronal β-amyloid and its interactions with proteins and subcellular organelles. Electrophoresis 2012, 33, 3608-3616.
3. Singh, B., Parsaik, A. K., Mielke, M. M., Erwin, P. J. et al., Association of Mediterranean diet with mild cognitive impairment and Alzheimer's disease: a systematic review and meta-analysis. J. Alzheimers Dis. 2014, 39, 271-382.
4. Lourida, I., Soni, M., Thompson-Coon, J., Purandare, N. et al., Mediterranean diet, cognitive function, and dementia: a systematic review. Epidemiology 2013, 24, 479-489.
5. Grossi, C., Ed Dami, T., Rigacci, S., Stefani, M. et al., Employing Alzheimer disease animal models for translational research: focus on dietary components. Neurodegener. Dis. 2014, 13, 131-134.
6. Luccarini, I., Ed Dami, T., Grossi, C., Rigacci, S. et al., Oleuropein aglycone counteracts Aβ42 toxicity in the rat brain. Neurosci. Lett. 2014, 558, 67-72.
7. Pocernich, C. B., Lange, M. L., Sultana, R., Butterfield, D. A., Nutritional approaches to modulate oxidative stress in Alzheimer's disease. Curr. Alzheimer Res. 2011, 8, 452-469.
8. Vepsäl äinen, S., Koivisto, H., Pekkarinen, E., Mäkinen, P. et al., Anthocyanin-enriched bilberry and blackcurrant extracts modulate amyloid precursor protein processing and alleviate behavioral abnormalities in the APP/PS1 mouse model of Alzheimer's disease. J. Nutr. Biochem. 2013, 24, 360-370.
9. Ossola, B., Kaariainen, T. M., Mannisto, P. T., The multiple faces of quercetin in neuroprotection. Expert. Opin. Drug Saf. 2009, 8, 397-409.
10. Ramesh, B. N., Rao, T. S., Prakasam, A., Sambamurti, K., Rao, K. S., Neuronutrition and Alzheimer's disease. J. Alzheimers Dis. 2010, 19, 1123-1139.
11. Jayasena, T., Poljak, A., Smythe, G., Braidy, N. et al., The role of polyphenols in the modulation of sirtuins and other pathways involved in Alzheimer's disease. Ageing Res. Rev. 2013, 12, 867-883.
12. Cheng, B., Gong, H., Xiao, H., Petersen, R. B. et al., Inhibiting toxic aggregation of amyloidogenic proteins: a therapeutic strategy for protein misfolding diseases. Biochim. Biophys. Acta 2013, 1830, 4860-4871.
13. O'Neill, C., Kiely, A. P., Coakley, M. F., Manning, S., Long-Smith, C. M., Insulin and IGF-1 signalling: longevity, protein homoeostasis and Alzheimer's disease.Biochem. Soc. Trans. 2012, 40, 721-727.
14. Cohen, E., Aging, protein aggregation, chaperones, and neurodegenerative disorders: mechanisms of coupling and therapeutic opportunities. Rambam Maimonides Med. J. 2012, 3, e0021.
15. Kim, Y. E., Hipp, M. S., Bracher, A., Hayer-Hartl, M., Hartl, F. U., Molecular chaperone functions in protein folding and proteostasis. Annu. Rev. Biochem. 2013, 82, 323-355.
16. Tanaka, K., Matsuda, N., Proteostasis and neurodegeneration:the roles of proteasomal degradation and autophagy. Biochim. Biophys. Acta 2014, 1843, 197-204.
17. Link, C., Expression of human β-amyloid peptide in transgenic Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 1995, 92, 9368-9372.
18. Paganga, G., Miller, N., Rice-Evans, C. A., The polyphenolic content of fruit and vegetables and their antioxidant activities. What does a serving constitute? Free Radic. Res. 1999, 30, 153-162.
19. Sato, M., Murakami, K., Uno, M., Nakagawa, Y. et al., Sitespecific inhibitory mechanism for amyloid β42 aggregation by catechol-type flavonoids targeting the Lys residues. J. Biol. Chem. 2013, 288, 23212-23224.
20. Park, S. Y., Lim, J. Y., Jeong, W., Hong, S. S. et al., Cmethylflavonoids isolated from Callistemon lanceolatus protect PC12 cells against Abeta-induced toxicity. Planta Med. 2010, 76, 863-868.
21. Ansari, M. A., Abdul, H. M., Joshi, G., Opii, W. O., Butterfield, D. A., Protective effect of quercetin in primary neurons against Abeta (1-42): relevance to Alzheimer's disease. J. Nutr. Biochem. 2009, 20, 269-275.
22. Riederer, B. M., Leuba, G., Vernay, A., Riederer, I. M., The role of the ubiquitin proteasome system in Alzheimer's disease. Exp. Biol. Med. 2011, 236, 268-276.
23. Fitzenberger, E., Boll, M., Wenzel, U., Impairment of the proteasome is crucial for glucose-induced lifespan reduction in the mev-1 mutant of Caenorhabditis elegans. Biochim. Biophys. Acta 2013, 1832, 565-573.
24. Brenner, S., The genetics of Caenorhabditis elegans. Genetics Dev. 1974, 77, 71-94.
25. Stiernagle, T., Maintenance of C. elegans. in: The C. elegans Research Community (Ed.), WormBook 2006, pp. 1-11.
26. Lehner, B., Tischler, J., Fraser, A. G., RNAi screens in Caenorhabditis elegans in a 96-well liquid format and their application to the systematic identification of genetic interactions. Nat. Protoc. 2006, 1, 1617-1620.
27. Timmons, L., Court, D. L., Fire, A., Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic in Caenorhabditis elegans. Gene 2001, 263, 103-112.
28. Pfaffl, M. W., A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 92, 2002-2007.
29. Link, C. D., Taft, A., Kapulkin, V., Duke, K. et al., Gene expression analysis in a transgenic Caenorhabditis elegans Alzheimer's disease model. Neurobiol. Aging 2003, 24, 397-413.
30. Pispa, J., Palmén, S., Holmberg, C. I., Jäntti, J. et al., C. elegans dss-1 is functionally conserved and required for oogenesis and larval growth. BMC Dev. Biol. 2008, 8, 51.
31. Iwatsubo, T., Odaka, A., Suzuki, N., Mizusawa, H. et al., Visualization of A beta 42(43) and A beta 40 in senile plaques with end-specific A beta monoclonals: evidence that an initially deposited species is A beta 42(43). Neuron 1994, 13, 45-53.
32. Vassar, R., Bennett, B. D., Babu-Khan, S., Kahn, S. et al., Beta-secretase cleavage of Alzheimer's amyloid precursor protein by transmembrane aspartic protease BACE. Science 1999, 286, 735-741.
33. Hardy, J., Selkoe, D. J., The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 2002, 297, 353-356.
34. Pereira, C., Agostinho, P., Moreira, P. I., Cardoso, S. M., Oliveira, C. R., Alzheimer's disease-associated neurotoxic mechanisms and neuroprotective strategies. Curr. Drug Targets CNS Neurol. Disord. 2005, 4, 383-403.
35. Nath, S., Agholme, L., Kurudenkandy, F. R., Granseth, B. et al., Spreading of neurodegenerative pathology via neuron-toneuron transmission of β-amyloid. J. Neurosci. 2012, 32, 8767-8777.
36. Cataldo, A. M., Hamilton, D. J., Barnett, J. L., Paskevich, P. A., Nixon, R. A., Properties of the endosomallysosomal system in the human central nervous system:disturbances mark most neurons in populations at risk to degenerate in Alzheimer's disease. J. Neurosci. 1996, 16, 186-199.
37. Devi, L., Prabhu, B. M., Galati, D. F., Avadhani, N. G., Anandatheerthavarada H. K., Accumulation of amyloid precursor protein in the mitochondrial import channels of human Alzheimer's disease brain is associated with mitochondrial dysfunction. J. Neurosci. 2006, 26, 9057-9068.
38. Viana, R. J., Nunes, A. F., Rodrigues, C. M., Endoplasmic reticulum enrollment in Alzheimer's disease. Mol. Neurobiol. 2012, 46, 522-534.
39. Virok, D. P., Simon, D., Bozsó, Z., Rajkó, R. et al., Protein array based interactome analysis of amyloid-β indicates an inhibition of protein translation. J. Proteome Res. 2011, 10, 1538-1547.
40. Arduino, D. M., Esteves, A. R., Silva, D. F., Martins-Branco, D. et al., Therapeutic intervention at cellular quality control systems in Alzheimer's and Parkinson's diseases. Curr. Pharm. Des. 2011, 17, 3446-3459.
41. Calabrese, V., Cornelius, C., Dinkova-Kostova, A. T., Calabrese, E. J., Vitagenes, cellular stress response, and acetylcarnitine:relevance to hormesis. Biofactors 2009, 35, 146-160.
42. Pallauf, K., Rimbach, G., Autophagy, polyphenols and healthy ageing. Ageing Res. Rev. 2013, 12, 237-252.
43. Ramassamy, C., Emerging role of polyphenolic compounds in the treatment of neurodegenerative diseases: a review of their intracellular targets. Eur. J. Pharmacol. 2006, 545, 51-64.
44. Rebolledo, D. L., Aldunate, R., Kohn, R., Neira, I. et al., Copper reduces Aβ oligomeric species and ameliorates neuromuscular synaptic defects in a C. elegans model of inclusion body myositis. J. Neurosci. 2011, 31, 10149-10158.
45. McColl, G., Roberts, B. R., Gunn, A. P., Perez, K. A. et al., The Caenorhabditis elegans A beta 1-42model of Alzheimer disease predominantly expresses A beta 3-42. J. Biol. Chem. 2009, 284, 22697-22702.
46. Nussbaum, J. M., Schilling, S., Cynis, H., Silva, A. et al., Prion-like behaviour and tau-dependent cytotoxicity of pyroglutamylated amyloid-β. Nature 2012, 485, 651-655.
47. Wirths, O., Breyhan, H., Cynis, H., Schilling, S. et al., Intraneuronal pyroglutamate-Abeta 3-42 triggers neurodegeneration and lethal neurological deficits in a transgenic mouse model. Acta Neuropathol. 2009, 118, 487-496.
48. Becker, A., Kohlmann, S., Alexandru, A., Jagla, W. et al., Glutaminyl cyclase-mediated toxicity of pyroglutamate-beta amyloid induces striatal neurodegeneration. BMC Neurosci. 2013, 14, 108.
49. Haynes, C. M., Petrova, K., Benedetti, C., Yang, Y., Ron, D., ClpPmediates activation of a mitochondrial unfolded protein response in C. elegans. Dev. Cell 2007, 13, 467-480.
50. Benedetti, C., Haynes, C. M., Yang, Y., Harding, H. P., Ron, D., Ubiquitin-like protein 5 positively regulates chaperone gene expression in the mitochondrial unfolded protein response. Genetics 2006, 174, 229-239.
51. Haynes, C. M., Fiorese, C. J., Lin, Y. F., Evaluating and responding to mitochondrial dysfunction: the mitochondrial unfolded-protein response and beyond. Trends Cell Biol. 2013, 23, 311-318.
52. Broadley, S. A., Hartl, F. U., Mitochondrial stress signaling: a pathway unfolds. Trends Cell Biol. 2008, 18, 1-4.
53. Taylor, R. C., Dillin, A., XBP-1 is a cell-nonautonomous regulator of stress resistance and longevity. Cell 2013, 153, 1435-1447.
54. Urano, F., Calfon, M., Yoneda, T., Yun, C. et al., A survival pathway for Caenorhabditis elegans with a blocked unfolded protein response. J. Cell Biol. 2002, 158, 639-646.
55. Pattingre, S., Espert, L., Biard-Piechaczyk, M., Codogno, P., Regulation of macroautophagy by mTOR and Beclin 1 complexes. Biochimie 2008, 90, 313-323.
56. Pietrocola, F., Mariño, G., Lissa, D., Vacchelli, E. et al., Proautophagic polyphenols reduce the acetylation of cytoplasmic proteins. Cell Cycle 2012, 11, 3851-3860.
57. Vingtdeux, V., Giliberto, L., Zhao, H., Chandakkar, P. et al., AMP-activated protein kinase signaling activation by resveratrol modulates amyloid-beta peptide metabolism. J. Biol. Chem. 2010, 285, 9100-9113.
58. Martinez-Vicente, M., Cuervo, A. M., Autophagy and neurodegeneration:when the cleaning crew goes on strike. Lancet Neurol. 2007, 6, 352-361.