A Cocoa Peptide Protects Caenorhabditis elegans from Oxidative Stress and β-Amyloid Peptide Toxicity

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Martorell, Patricia ^a   Bataller, Esther ^a   Llopis, Silvia ^a   Gonzalez, Núria ^a   Álvarez, Beatriz ^a   Montón, Fernando ^a   Ortiz, Pepa ^a   Ramón, Daniel ^a   Genovés, Salvador ^a  

^a Food Biotechnology Department   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; ANTIOXIDANT; ASPARTYLASPARAGINYLTYROSYLASPARTYLASPARAGINYLSERYLALANYLGLYCYLLYSYLTRYPTOPHANYLTRYPTOPHANYLTRYPTOPHANYLVALYLTHREONINE; PEPTIDE DERIVATIVE; PROTEASOME; PROTEINASE; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANTIOXIDANT ACTIVITY; ARTICLE; CACAO; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DISEASE MODEL; ENZYME INHIBITION; HYDROPHOBIC INTERACTION CHROMATOGRAPHY; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PARALYSIS; PEPTIDE ANALYSIS; PROTEIN EXPRESSION; PROTEIN TARGETING; SYNAPSE; TRANSCRIPTOMICS; TRANSGENIC ORGANISM; WESTERN BLOTTING; WILD TYPE;

ALZHEIMER DISEASE; AMINO ACID SEQUENCE; AMYLOID BETA-PEPTIDES; ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTIOXIDANTS; CACAO; CAENORHABDITIS ELEGANS; DISEASE MODELS, ANIMAL; GENE EXPRESSION; HUMANS; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; OXIDATIVE STRESS; PARALYSIS; PEPTIDE FRAGMENTS; PEPTIDES;

EID: 84877648168     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0063283     Document Type: Article

References (53)

1. Dillinger TL, Barriga P, Escárcega S, Jimenez M, Salazar Lowe D, et al. (2000) Food of the gods: cure for humanity? A cultural history of the medicinal and ritual use of chocolate. J Nutr 130: 2057S-2072S.
2. Steinberg FM, Bearden MM, Keen CL, (2003) Cocoa and chocolate flavonoids: implications for cardiovascular health. J Am Diet Assoc 103: 215-223.
3. Galleano M, Oteiza PI, Fraga CG, (2009) Cocoa, chocolate, and cardiovascular disease. J Cardiovasc Pharmacol 54: 483-490.
4. Rusconi M, Conti A, (2010) Theobroma cacao L., the Food of the Gods: a scientific approach beyond myths and claims. Pharmacol Res 61: 5-13.
5. Katz DL, Doughty K, Ali A, (2011) Cocoa and chocolate in human health and disease. Antioxid Redox Signal 15: 2779-2811.
6. Preza AM, Jaramillo ME, Puebla AM, Mateos JC, Hernández R, et al. (2010) Antitumor activity against murine lymphoma L5178Y model of proteins from cacao (Theobroma cacao L.) seeds in relation with in vitro antioxidant activity. BMC Complement Altern Med 10: 61.
7. Nehlig A, (2012) The neuroprotective effects of cocoa flavanol and its influence on cognitive performance. Br J Clin Pharmacol 10doi:10.1111/j.1365-2125.2012.04378.x. [Epub ahead of print] PubMed PMID: 22775434.
8. Sarmadi BH, Ismail A, (2010) Antioxidative peptides from food proteins: a review. Peptides 31: 1949-1956.
9. Klompong V, Benjakul S, Yachai M, Visessanguan W, Shahidi F, et al. (2009) Amino acid composition and antioxidative peptides from protein hydrolysates of yellow stripe Trevally (Selaroides leptolepis). J Food Sci 74: C126-C133.
10. Kim SK, Kim YT, Byun HG, Nam KS, Joo DS, et al. (2001) Isolation and characterization of antioxidative peptides from gelatin hydrolysate of Alaska pollack skin. J Agric Food Chem 49: 1984-1989.
11. Summa C, McCourt J, Cämmerer B, Fiala A, Probst M, et al. (2008) Radical scavenging activity, anti-bacterial and mutagenic effects of cocoa bean Maillard reaction products with degree of roasting. Mol Nutr Food Res 52: 342-351.
12. Selkoe DJ, (1997) Alzheimer's disease: genotypes, phenotypes, and treatments. Science 275: 630-631.
13. Morales R, Duran-Aniotz C, Castilla J, Estrada LD, Soto C, (2011) De novo induction of amyloid-β deposition in vivo. Mol Psychiatry Oct 4. doi: 10.1038/mp.2011.120. [Epub ahead of print] PubMed PMID: 21968933.
14. Hardy J, Selkoe DJ, (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297: 353-356.
15. Sherrington R, Rogaev EI, Liang Y, Rogaeva EA, Levesque G, et al. (1995) Cloning of a gene bearing missense mutations in early-onset familial Alzheimer's disease. Nature 375: 754-760.
16. Verri M, Pastoris O, Dossena M, Aquilani R, Guerriero F, et al. (2012) Mitochondrial alterations, oxidative stress and neuroinflammation in Alzheimer's disease. Int J Immunopathol Pharmacol 25: 345-353.
17. Luo Y, (2006) Alzheimer's disease, the nematode Caenorhabditis elegans, and Ginkgo biloba leaf extract. Life Sci 78: 2066-2072.
18. Ewald CY, Li C, (2010) Understanding the molecular basis of Alzheimer's disease using a Caenorhabditis elegans model system. Brain Struct Funct 214: 263-283.
19. Calahorro F, Ruiz-Rubio M, (2011) Caenorhabditis elegans as an experimental tool for the study of complex neurological diseases: Parkinson's disease, Alzheimer's disease and autism spectrum disorder. Invert Neurosci 11: 73-83.
20. Teschendorf D, Link CD, (2009) What have worm models told us about the mechanisms of neuronal dysfunction in human neurodegenerative diseases? Mol Neurodegener 4: 38.
21. Link CD, (1995) Expression of human beta-amyloid peptide in transgenic Caenorhabditis elegans. Proc Natl Acad Sci U S A 92: 9368-9372.
22. Link CD, Johnson CJ, Fonte V, Paupard M, Hall DH, et al. (2001) Visualization of fibrillar amyloid deposits in living, transgenic Caenorhabditis elegans animals using the sensitive amyloid dye, X-34. Neurobiol Aging 22: 217-226.
23. Yoshimoto T, Walter R, Tsuru D, (1980) Proline-specific endopeptidase from Flavobacterium. J Biol Chem 10: 4786-4792.
24. Yoshimoto T, Kado K, Matsubara F, Koriyama N, Kaneto H, et al. (1987) Specific inhibitors for prolyl endopeptidase and their anti-amnesic effect. J Pharmacobiodyn 12: 730-735.
25. Martorell P, Forment JV, de Llanos R, Montón F, Llopis S, et al. (2011) Use of Saccharomyces cerevisiae and Caenorhabditis elegans as model organisms to study the effect of cocoa polyphenols in the resistance to oxidative stress. J Agric Food Chem 59: 2077-2085.
26. Martorell P, Llopis S, González N, Montón F, Ortiz P, et al. (2012) Caenorhabditis elegans as a model to study the effectiveness and metabolic targets of dietary supplements used for obesity treatment: the specific case of a conjugated linoleic acid mixture (Tonalin). J Agric Food Chem 60: 11071-11079.
27. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, et al. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264.
28. Smyth GK, (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3.
29. Benjamini Y, Hochberg Y, (1995) Controlling the False Discovery Rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B (Methodological) 57: 289-300.
30. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, et al. (2003) PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34: 267-273.
31. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, et al. (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 102: 15545-15550.
32. Sartor MA, Leikauf GD, Medvedovic M, (2009) LRpath: a logistic regression approach for identifying enriched biological groups in gene expression data. Bioinformatics 25: 211-217.
33. Montaner D, Dopazo J, (2010) Multidimensional gene set analysis of genomic data. PLoS One 5: e10348.
34. Wu Y, Wu Z, Butko P, Christen Y, Lambert MP, et al. (2006) Amyloid-beta-induced pathological behaviors are suppressed by Ginkgo biloba extract EGb 761 and ginkgolides in transgenic Caenorhabditis elegans. J Neurosci 26: 13102-13113.
35. Gutierrez-Zepeda A, Santell R, Wu Z, Brown M, Wu Y, et al. (2005) Soy isoflavone glycitein protects against beta amyloid-induced toxicity and oxidative stress in transgenic Caenorhabditis elegans. BMC Neurosci 6: 54.
36. Arya U, Dwivedi H, Subramaniam JR, (2009) Reserpine ameliorates Abeta toxicity in the Alzheimer's disease model in Caenorhabditis elegans. Exp Gerontol 44: 462-466.
37. Dostal V, Roberts CM, Link CD, (2010) Genetic mechanisms of coffee extract protection in a Caenorhabditis elegans model of β-amyloid peptide toxicity. Genetics 186: 857-866.
38. Imahori K, (2010) The biochemical study on the etiology of Alzheimer's disease. Proc Jpn Acad Ser B Phys Biol Sci 86: 54-61.
39. Bubber P, Haroutunian V, Fisch G, Blass JP, Gibson GE, (2005) Mitochondrial abnormalities in Alzheimer brain: mechanistic implications. Ann Neurol 57: 695-703.
40. Reddy PH, Beal MF, (2008) Amyloid beta, mitochondrial dysfunction and synaptic damage: implications for cognitive decline in aging and Alzheimer's disease. Trends Mol Med 14: 45-53.
41. Phelps ME, Barrio JR, (2010) Correlation of brain amyloid with "aerobic glycolysis": A question of assumptions? Proc Natl Acad Sci U S A 107: 17459-17460.
42. Chou JL, Shenoy DV, Thomas N, Choudhary PK, Laferla FM, et al. (2011) Early dysregulation of the mitochondrial proteome in a mouse model of Alzheimer's disease. J Proteomics 74: 466-479.
43. Oxenkrug GF, (2010) Metabolic syndrome, age-associated neuroendocrine disorders, and dysregulation of tryptophan-kynurenine metabolism. Ann N Y Acad Sci 1199: 1-14.
44. Hare EE, Loer CM, (2004) Function and evolution of the serotonin-synthetic bas-1 gene and other aromatic amino acid decarboxylase genes in Caenorhabditis. BMC Evol Biol 4: 24.
45. Alkema MJ, Hunter-Ensor M, Ringstad N, Horvitz HR, (2005) Tyramine Functions independently of octopamine in the Caenorhabditis elegans nervous system. Neuron 46: 247-260.
46. Brock TJ, Browse J, Watts JL, (2007) Fatty acid desaturation and the regulation of adiposity in Caenorhabditis elegans. Genetics 176: 865-875.
47. Sze JY, Victor M, Loer C, Shi Y, Ruvkun G, (2000) Food and metabolic signaling defects in a Caenorhabditis elegans serotonin-synthesis mutant. Nature 403: 560-564.
48. Glickman MH, Ciechanover A, (2002) The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 82: 373-428.
49. Alavez S, Vantipalli MC, Zucker DJ, Klang IM, Lithgow GJ, (2011) Amyloid-binding compounds maintain protein homeostasis during ageing and extend lifespan. Nature 472: 226-229.
50. Checler F, da Costa CA, Ancolio K, Chevallier N, Lopez-Perez E, et al. (2000) Role of the proteasome in Alzheimer's disease. Biochim Biophys Acta 1502: 133-138.
51. Hassan WM, Merin DA, Fonte V, Link CD, (2009) AIP-1 ameliorates beta-amyloid peptide toxicity in a Caenorhabditis elegans Alzheimer's disease model. Hum Mol Genet 18: 2739-2747.
52. Barelli H, Petit A, Hirsch E, Wilk S, De Nanteuil G, et al. (1999) S 17092-1, a highly potent, specific and cell permeant inhibitor of human proline endopeptidase. Biochem Biophys Res Commun 1999 257: 657-661.
53. Hornsten A, Lieberthal J, Fadia S, Malins R, Ha L, (2007) APL-1, a Caenorhabditis elegans protein related to the human beta-amyloid precursor protein, is essential for viability. Proc Natl Acad Sci U S A 104: 1971-1976.