Peptides that activate the 20S proteasome by gate opening increased oxidized protein removal and reduced protein aggregation

Free Radical Biology and Medicine

Volumn 67, Issue , 2014, Pages 304-313

  Dal Vechio, Francisco H ^a   Cerqueira, Fernanda ^a   Augusto, Ohara ^a   Lopes, Robson ^b   Demasi, Marilene ^a  

^a INSTITUTO BUTANTAN   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

ALS; Free radicals; Proteasome; Protein aggregation; Protein oxidation; Therapeutic peptides

Indexed keywords

20S PROTEASOME; COPPER ZINC SUPEROXIDE DISMUTASE; GLUTATHIONE REDUCTASE; PEPTIDE; PROTEASOME; PROTEASOME ACTIVATING PEPTIDE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; UNCLASSIFIED DRUG; ENZYME ACTIVATOR; PROTEIN AGGREGATE; SACCHAROMYCES CEREVISIAE PROTEIN;

AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; CELL PROTECTION; CELL VIABILITY; CHEMICAL BOND; CONTROLLED STUDY; DIMERIZATION; ERYTHROCYTE; HUMAN; HUMAN CELL; IN VITRO STUDY; MOLECULAR WEIGHT; NONHUMAN; OXIDATIVE STRESS; PH; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CARBONYLATION; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN HYDROLYSIS; RABBIT; REACTION TIME; UBIQUITINATION; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; DRUG EFFECTS; ENZYME ACTIVATION; ENZYMOLOGY; METABOLISM; MOLECULAR GENETICS; NERVE CELL; OXIDATION REDUCTION REACTION; PROTEIN AGGREGATION, PATHOLOGICAL; SACCHAROMYCES CEREVISIAE; SYNTHESIS; TUMOR CELL LINE;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE, TUMOR; ENZYME ACTIVATION; ENZYME ACTIVATORS; HUMANS; MOLECULAR SEQUENCE DATA; NEURONS; OXIDATION-REDUCTION; OXIDATIVE STRESS; PEPTIDES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN AGGREGATES; PROTEIN AGGREGATION, PATHOLOGICAL; PROTEOLYSIS; RABBITS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84889998868     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2013.11.017     Document Type: Article

References (47)

1. O. Coux, K. Tanaka, and A.F. Goldberg Structure and functions of the 20S and 26S proteasomes Annu. Rev. Biochem. 65 1996 801 847 (Pubitemid 26255262)
2. M.H. Glickman, and A. Ciechanover The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction Physiol. Rev. 82 2002 373 428 (Pubitemid 34654457)
3. K.J. Davies Degradation of oxidized proteins by the 20S proteasome Biochimie 83 2001 301 310 (Pubitemid 32293650)
4. R. Shringapure, T. Grune, J. Mehlhase, and K.J. Davies Ubiquitin conjugation is not required for the degradation of oxidized proteins by proteasome J. Biol. Chem. 278 2003 311 318 (Pubitemid 36043578)
5. T. Jung, B. Catalgol, and T. Grune The proteasomal system Mol. Aspects Med. 30 2009 191 296
6. N. Tanahashi, Y. Murakami, Y. Minami, N. Shimbara, K.B. Hendil, and K. Tanaka Hybrid proteasomes: induction by interferon-gamma and contribution to ATP-dependent proteolysis J. Biol. Chem. 275 2000 14336 14345 (Pubitemid 30339716)
7. S.E. Babbitt, A. Kiss, A.E. Deffenbaugh, Y.H. Chang, E. Bailly, H. Erdjument-Bromage, P. Tempst, T. Buranda, L.A. Sklar, J. Baumler, E. Gogol, and D. Skowyra ATP hydrolysis-dependent disassembly of the 26S proteasome is part of the catalytic cycle Cell 121 2005 553 565 (Pubitemid 40720009)
8. G. Fenteany, and S.L. Schreiber Lactacystin, proteasome function, and cell fate J. Biol. Chem. 273 1998 8545 8548 (Pubitemid 28176125)
9. L. Huang, and C.H. Chen Proteasome regulators: activators and inhibitors Curr. Med. Chem. 16 2009 931 939
10. M.K. Kwak, J.M. Cho, B. Huang, S. Shin, and T.W. Kensler Role of increased expression of the proteasome in the protective effects of sulphoraphane against hydrogen peroxide-mediated cytotoxicity in murine neuroblastoma cells Free Radic. Biol. Med. 43 2007 809 817 (Pubitemid 47103310)
11. N. Chondrogianni, and E.S. Gonos Proteasome activation as a novel antiaging strategy IUBMB Life 60 2008 651 655
12. N. Chondrogianni, C. Tzavelas, A.J. Pemberton, I.P. Nezis, A.J. Rivett, and E.S. Gonos Overexpression of proteasome beta 5 subunit increases the amount of assembled proteasome and confers ameliorated response to oxidative stress and higher survival rates J. Biol. Chem. 280 2005 11840 11850 (Pubitemid 40418498)
13. U. Kruegel, B. Robison, T. Dange, G. Kahlert, J.R. Delaney, S. Kotireddy, M. Tsuchiya, S. Tsuchiyama, C.J. Murakami, J. Schleit, G. Sutphin, D. Carr, K. Tar, G. Dittmar, M. Kaeberlein, B.K. Kennedy, and M. Schmidt Elevated proteasome capacity extends replicative lifespan in Saccharomyces cerevisiae PLoS Genet. 7 2011 e1002253
14. A.F. Kisselev, D. Kaganovich, and A.L. Goldberg Binding of hydrophobic peptides to several non-catalytic sites promotes peptide hydrolysis by all active sites of 20S proteasomes: evidence for peptide-induced channel opening in the alpharings J. Biol. Chem. 277 2002 22260 22270 (Pubitemid 34967192)
15. A.L. Bulteau, M. Moreau, A. Saunois, C. Nizard, and B. Friguet Algae extract-mediated stimulation and protection of proteasome activity within human keratinocytes exposed to UVA and UVB irradiation Antioxid. Redox Signaling 8 2006 136 143 (Pubitemid 43324540)
16. M. Katsiki, N. Chondrogianni, I. Chinou, A.J. Rivett, and E.S. Gonos The olive constituent oleuropein exhibits proteasome stimulatory properties in vitro and confers life span extension of human embryonic fibroblasts Rejuvenation Res. 10 2007 157 172 (Pubitemid 46944984)
17. E. Atherton, and R.C. Sheppard Solid Phase Peptide Synthesis - a Practical Approach 1989 Oxford Univ. Press New York
18. D. Yamashiro, D.B. Hope, and V. Du Vigneaud Isomeric dimers of oxytocin J. Am. Chem. Soc. 90 1968 3857 3860
19. R. Verma, S. Chen, R. Feldman, D. Schieltz, J. Yates, J. Dohmen, and R.J. Deshaies Proteasomal proteomics: identification of nucleotide-sensitive proteasome-interacting proteins by mass spectrometric analysis of affinity-purified proteasomes Mol. Biol. Cell 11 2000 3425 3439
20. M. Bajorek, D. Finley, and M.H. Glickman Proteasome disassembly and downregulation is correlated with viability during stationary phase Curr. Biol. 13 2003 1140 1144 (Pubitemid 36815263)
21. M. Demasi, R. Shringarpure, and K.J. Davies Glutathiolation of the proteasome is enhanced by proteolytic inhibitors Arch. Biochem. Biophys. 389 2001 254 263 (Pubitemid 32881951)
22. S.S. Twining Fluorescein isothiocyanate-labeled casein assay for proteolytic enzymes Anal. Biochem. 143 1984 30 34 (Pubitemid 15157534)
23. 2+ concentration in transfected neuroblastoma SH-SY5Y cells FEBS Lett. 414 1997 358 365
24. E. Shacter, J.A. Williams, M. Lim, and R.L. Levine Differential susceptibility of plasma proteins to oxidative modification: examination by western blot immunoassay Free Radic. Biol. Med. 17 1994 429 437 (Pubitemid 24320292)
25. D.B. Medinas, F.C. Gozzo, L.F.A. Santos, A.H. Iglesias, and O. Augusto A ditryptophan cross-link is responsible for the covalent dimerization of human superoxide dismutase 1 during its bicarbonate-dependent peroxidase activity Free Radic. Biol. Med. 49 2010 1046 1053
26. G.M. Silva, L.E. Netto, V. Simões, L.F. Santos, F.C. Gozzo, M.A. Demasi, C.L. Oliveira, R.N. Bicev, C.F. Klitzke, M.C. Sogayar, and M. Demasi Redox control of 20S proteasome gating Antioxid. Redox Signaling 16 2012 1183 1194
27. Derwent Innovations Index. International Publication No. WO2008/009085A1. New York: Thomson Reuters.
28. R. Banerjee Redox outside the box: linking extracellular redox remodeling with intracellular redox J. Biol. Chem. 287 2012 4397 4402
29. C.G. Goetz Amyotrophic lateral sclerosis: early contributions of Jean-Martin Charcot Muscle Nerve 23 2000 336 343 (Pubitemid 30126978)
30. D.R. Rosen, P. Sapp, J. O'Regan, D. McKenna-Yasek, K.S. Schlumpf, J.L. Haines, J.F. Gusella, H.R. Horvitz, and R.H. Brown Jr. Genetic linkage analysis of familial amyotrophic lateral sclerosis using human chromosome 21 microsatellite DNA markers Am. J. Med. Genet. 51 1994 61 69 (Pubitemid 24142622)
31. P.M. Andersen, P. Nilsson, V. Ala-Hurula, M.L. Keränen, I. Tarvainen, T. Haltia, L. Nilsson, M. Binzer, L. Forsgren, and S.L. Marklund Amyotrophic lateral sclerosis associated with homozygosity for an Asp90Ala mutation in CuZn-superoxide dismutase Nat. Genet. 10 1995 61 66
32. A. Al-Chalabi, A. Jones, C. Troakes, A. King, S. Al-Sarraj, and L.H. van den Berg The genetics and neuropathology of amyotrophic lateral sclerosis Acta Neuropathol. 124 2012 339 352
33. J.A. Johnston, M.J. Dalton, M.E. Gurney, and R.R. Kopito Formation of high molecular weight complexes of mutant Cu, Zn-superoxide dismutase in a mouse model for familial amyotrophic lateral sclerosis Proc. Natl. Acad. Sci. USA 97 2000 12571 12576
34. M.J. Lindberg, R. Bystrom, N. Boknas, P.M. Andersen, and M. Oliveberg Systematically perturbed folding patterns of amyotrophic lateral sclerosis (ALS)-associated SOD1 mutants Proc. Natl. Acad. Sci. USA 102 2005 9754 9759 (Pubitemid 40993641)
35. R. Rakhit, J.P. Crow, J.R. Lepock, L.H. Kondejewski, N.R. Cashman, and A. Chakrabartty Monomeric Cu,Zn-superoxide dismutase is a common misfolding intermediate in the oxidation models of sporadic and familial amyotrophic lateral sclerosis J. Biol. Chem. 279 2004 15499 15504 (Pubitemid 38618950)
36. L. Di Noto, L.J. Whitson, X. Cao, P.J. Hart, and R.L. Levine Proteasomal degradation of mutant superoxide dismutases linked to amyotrophic lateral sclerosis J. Biol. Chem. 280 2005 39907 39913 (Pubitemid 41779125)
37. E.R. Stadtman, and R.L. Levine Free radical-mediated oxidation of free amino acids and amino acid residues in proteins Amino Acids 25 2003 207 218 (Pubitemid 38043943)
38. Q. Chen, J. Thorpe, J.R. Dohmen, F. Li, and J.N. Keller Ump1 extends yeast lifespan and enhances viability during oxidative stress: central role for the proteasome? Free Radic. Biol. Med. 40 2006 120 126 (Pubitemid 41759409)
39. Q. Huang, and M.E. Figueiredo-Pereira Ubiquitin/proteasome pathway impairment in neurodegeneration: therapeutic implications Apoptosis 15 2010 1292 1311
40. Y. Hong, W. Yan, S. Chen, C.R. Sun, and J.M. Zhang The role of Nrf2 signaling in the regulation of antioxidants and detoxifying enzymes after traumatic brain injury in rats and mice Acta Pharmacol. Sin 31 2010 1421 1430
41. N. Rogers, S. Paine, L. Bedford, and R. Layfield The ubiquitin-proteasome system: contributions to cell death or survival in neurodegeneration Neuropathol. Appl. Neurobiol. 36 2010 113 124
42. D.A. Nijholt, L. De Kimpe, H.L. Elfrink, J.J. Hoozemans, and W. Scheper Removing protein aggregates: the role of proteolysis in neurodegeneration Curr. Med. Chem. 18 2011 2459 2476
43. C. Bendotti, M. Marino, C. Cheroni, E. Fontana, V. Crippa, A. Poletti, and S. De Biasi Dysfunction of constitutive and inducible ubiquitin-proteasome system in amyotrophic lateral sclerosis: implication for protein aggregation and immune response Prog. Neurobiol. 97 2012 1101 1126
44. E. Kabashi, J.N. Agar, M.J. Strong, and H.D. Durham Impaired proteasome function in sporadic amyotrophic lateral sclerosis Amyotrophic Lateral Scler 13 2012 367 371
45. E. Kabashi, J.N. Agar, Y. Hong, D.M. Taylor, S. Minotti, D.A. Figlewicz, and H.D.J. Durham Proteasomes remain intact, but show early focal alteration in their composition in a mouse model of amyotrophic lateral sclerosis Neurochemistry 105 2008 2353 2366 (Pubitemid 351782260)
46. T. Grune, B. Catalgol, A. Licht, G. Ermak, A.M. Pickering, J.K. Ngo, and K.J. Davies HSP70 mediates dissociation and reassociation of the 26S proteasome during adaptation to oxidative stress Free Radic. Biol. Med. 51 2011 1355 1364
47. A.M. Pickering, L. Vojtovich, J. Tower, and K.J. Davies Oxidative stress adaptation with acute, chronic, and repeated stress Free Radic. Biol. Med. 55C 2012 109 118