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PMID: 9794805 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Comparative resistance of the 20S and 26S proteasome to oxidative stress.

The Biochemical journal ·Vol. 335 ( Pt 3) ·1998-11-01 ·Pages 637-42

Reinheckel T, Sitte N, Ullrich O, Kuckelkorn U, Davies KJ, Grune T

Abstract

Oxidatively modified ferritin is selectively recognized and degraded by the 20S proteasome. Concentrations of hydrogen peroxide (H2O2) higher than 10 micromol/mg of protein are able to prevent proteolytic degradation. Exposure of the protease to high amounts of oxidants (H2O2, peroxynitrite and hypochlorite) inhibits the enzymic activity of the 20S proteasome towards the fluorogenic peptide succinyl-leucine-leucine-valine-tyrosine-methylcoumarylamide (Suc-LLVY-MCA), as well as the proteolytic degradation of normal and oxidant-treated ferritin. Fifty per cent inhibition of the degradation of the protein substrates was achieved using 40 micromol of H2O2/mg of proteasome. No change in the composition of the enzyme was revealed by electrophoretic analysis up to concentrations of 120 micromol of H2O2/mg of proteasome. In further experiments, it was found that the 26S proteasome, the ATP- and ubiquitin-dependent form of the proteasomal system, is much more susceptible to oxidative stress. Whereas degradation of the fluorogenic peptide, Suc-LLVY-MCA, by the 20S proteasome was inhibited by 50% with 12 micromol of H2O2/mg, 3 micromol of H2O2/mg was enough to inhibit ATP-stimulated degradation by the 26S proteasome by 50%. This loss in activity could be followed by the loss of band intensity in the non-denaturing gel. Therefore we concluded that the 20S proteasome was more resistant to oxidative stress than the ATP- and ubiquitin-dependent 26S proteasome. Furthermore, we investigated the activity of both proteases in K562 cells after H2O2 treatment. Lysates from K562 cells are able to degrade oxidized ferritin at a higher rate than non-oxidized ferritin, in an ATP-independent manner. This effect could be followed even after treatment of the cells with H2O2 up to a concentration of 2mM. The lactacystin-sensitive ATP-stimulated degradation of the fluorogenic peptide Suc-LLVY-MCA declined, after treatment of the cells with 1mM H2O2, to the same level as that obtained without ATP stimulation. Therefore, we conclude that the regulation of the 20S proteasome by various regulators takes place during oxidative stress. This provides further evidence for the role of the 20S proteasome in the secondary antioxidative defences of mammalian cells.

MeSH Terms
Coumarins/metabolism Cysteine Endopeptidases/metabolism Erythrocytes/enzymology Ferritins/metabolism Fluorescent Dyes Humans Hydrogen Peroxide/pharmacology K562 Cells Kinetics Multienzyme Complexes/metabolism Nitrates/pharmacology Oligopeptides/metabolism Oxidants/pharmacology Oxidative Stress Peptide Hydrolases/metabolism Proteasome Endopeptidase Complex Sodium Hypochlorite/pharmacology Substrate Specificity
Chemicals
Coumarins Fluorescent Dyes Multienzyme Complexes Nitrates Oligopeptides Oxidants peroxynitric acid Ferritins succinyl-leucyl-leucyl-valyl-tyrosyl-methylcoumarinamide Hydrogen Peroxide Sodium Hypochlorite Peptide Hydrolases Cysteine Endopeptidases Proteasome Endopeptidase Complex ATP dependent 26S protease
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Reinheckel T
Clinics of Physical Medicine and Rehabilitation, Medical Faculty (Charité), Humboldt University Berlin, Schumannstr. 20/21, D-10098, Berlin, Germany.
Sitte N
Ullrich O
Kuckelkorn U
Davies K J
Grune T
References (24)
24 references, click to expand
  1. Macroxyproteinase (M.O.P.): a 670 kDa proteinase complex that degrades oxidatively denatured proteins in red blood cells.
    Free Radic Biol Med. 1989;7(5):521-36 PMID: 2558981
  2. Degradation of oxidatively denatured proteins in Escherichia coli.
    Free Radic Biol Med. 1988;5(4):215-23 PMID: 2908182
  3. The ATP-independent pathway in red blood cells that degrades oxidant-damaged hemoglobin.
    J Biol Chem. 1992 Nov 15;267(32):23015-22 PMID: 1429649
  4. The multicatalytic and 26 S proteases.
    J Biol Chem. 1993 Mar 25;268(9):6065-8 PMID: 8454582
  5. Dityrosine and tyrosine oxidation products are endogenous markers for the selective proteolysis of oxidatively modified red blood cell hemoglobin by (the 19 S) proteasome.
    J Biol Chem. 1993 Apr 25;268(12):8752-9 PMID: 8473319
  6. Potential roles of hypochlorous acid and N-chloroamines in collagen breakdown by phagocytic cells in synovitis.
    Free Radic Biol Med. 1993 Dec;15(6):637-43 PMID: 8138190
  7. Susceptibility of glucose-6-phosphate dehydrogenase modified by 4-hydroxy-2-nonenal and metal-catalyzed oxidation to proteolysis by the multicatalytic protease.
    Arch Biochem Biophys. 1994 May 15;311(1):168-73 PMID: 8185314
  8. Modification of glucose-6-phosphate dehydrogenase by 4-hydroxy-2-nonenal. Formation of cross-linked protein that inhibits the multicatalytic protease.
    J Biol Chem. 1994 Aug 26;269(34):21639-43 PMID: 8063806
  9. Proteolysis in cultured liver epithelial cells during oxidative stress. Role of the multicatalytic proteinase complex, proteasome.
    J Biol Chem. 1995 Feb 3;270(5):2344-51 PMID: 7836468
  10. Activation of the multicatalytic endopeptidase by oxidants. Effects on enzyme structure.
    Biochemistry. 1996 Jun 4;35(22):7142-9 PMID: 8679541
  11. Degradation of oxidized proteins in K562 human hematopoietic cells by proteasome.
    J Biol Chem. 1996 Jun 28;271(26):15504-9 PMID: 8663134
  12. Structure and functions of the 20S and 26S proteasomes.
    Annu Rev Biochem. 1996;65:801-47 PMID: 8811196
  13. Proteasomes: destruction as a programme.
    Trends Biochem Sci. 1996 Mar;21(3):96-102 PMID: 8882582
  14. Degradation of oxidized proteins in mammalian cells.
    FASEB J. 1997 Jun;11(7):526-34 PMID: 9212076
  15. Peroxynitrite increases the degradation of aconitase and other cellular proteins by proteasome.
    J Biol Chem. 1998 May 1;273(18):10857-62 PMID: 9556559
  16. Labeling of proteins by reductive methylation using sodium cyanoborohydride.
    J Biol Chem. 1979 Jun 10;254(11):4359-65 PMID: 571437
  17. Turnover of bacterial glutamine synthetase: oxidative inactivation precedes proteolysis.
    Proc Natl Acad Sci U S A. 1981 Apr;78(4):2120-4 PMID: 6113590
  18. Preferential degradation of the oxidatively modified form of glutamine synthetase by intracellular mammalian proteases.
    J Biol Chem. 1985 Jan 10;260(1):300-5 PMID: 2856920
  19. Purification of a liver alkaline protease which degrades oxidatively modified glutamine synthetase. Characterization as a high molecular weight cysteine proteinase.
    J Biol Chem. 1985 Oct 15;260(23):12600-6 PMID: 2864341
  20. Fragmentation of proteins by free radicals and its effect on their susceptibility to enzymic hydrolysis.
    Biochem J. 1986 Mar 1;234(2):399-403 PMID: 3718475
  21. Purification of two high molecular weight proteases from rabbit reticulocyte lysate.
    J Biol Chem. 1987 Jun 15;262(17):8303-13 PMID: 3298229
  22. Coomassie blue-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for direct visualization of polypeptides during electrophoresis.
    Anal Biochem. 1988 Aug 15;173(1):201-5 PMID: 2461119
  23. Involvement of the proteasome in various degradative processes in mammalian cells.
    Proc Natl Acad Sci U S A. 1989 Apr;86(8):2597-601 PMID: 2539595
  24. Protein degradation as an index of oxidative stress.
    Methods Enzymol. 1990;186:485-502 PMID: 2233315
Article Info
Journal
The Biochemical journal
Abbr.
Biochem J
ISSN
0264-6021
Published
1998-11-01
Pages
637-42
Language
English
Region
England
NLM ID
2984726R
PMCID
PMC1219826
Subset
IM
Grants
NIEHS NIH HHS · ES-03598 · United States
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