Protein oxidation and proteolysis
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Nicolle Bader
Abstract
One of the hallmarks of chronic or severe oxidative stress is the accumulation of oxidized proteins, which tend to form high-molecular-weight aggregates. The major proteolytic system responsible for the removal of oxidized cytosolic and nuclear proteins is the proteasome. This complicated proteolytic system contains a core proteasomal form (20S proteasome) and several regulators. All of these components are affected by oxidative stress to various degrees. The ATP-stimulated 26S proteasome is sensitive to oxidative stress, whereas the 20S form seems to be more resistant. The nuclear proteasome selectively degrades oxidatively damaged histones in the nuclei of mammalian cells, where it is activated and regulated by automodified PARP-1 after oxidative challenge. In this brief review we highlight the proteolysis and its regulatory effects during oxidative stress.
References
Arnold, J. and Grune, T. (2002). PARP-mediated proteasome activation: a co-ordination of DNA repair and protein degradation? Bioessays24, 1060–1065.10.1002/bies.10179Search in Google Scholar
Chondrogianni, N. and Gonos, E.S. (2005). Proteasome dysfunction in mammalian aging: steps and factors involved. Exp. Gerontol.40, 931–938.10.1016/j.exger.2005.09.004Search in Google Scholar
Ciechanover, A. (1994). The ubiquitin-proteasome proteolytic pathway. Cell79, 13–21.10.1016/0092-8674(94)90396-4Search in Google Scholar
Coux, O., Tanaka, K., and Goldberg, A.L. (1996). Structure and functions of the 20S and 26S proteasomes. Annu. Rev. Biochem.65, 801–847.10.1146/annurev.bi.65.070196.004101Search in Google Scholar
DeMartino, G.N., Proske, R.J., Moomaw, C.R., Strong, A.A., Song, X., Hisamatsu, H., and Tanaka, K. (1996). Identification, purification, and characterization of a PA700-dependent activator of the proteasome. J. Biol. Chem.271, 3112–3118.10.1074/jbc.271.6.3112Search in Google Scholar
Friguet, B. and Szweda, L.I. (1997). Inhibition of the multicatalytic proteinase (proteasome) by 4-hydroxy-2-nonenal cross-linked protein. FEBS Lett.405, 21–25.10.1016/S0014-5793(97)00148-8Search in Google Scholar
Friguet, B. (2006). Oxidized protein degradation and repair in ageing and oxidative stress. FEBS Lett.580, 2910–2916.10.1016/j.febslet.2006.03.028Search in Google Scholar PubMed
Glickman, M.H. and Ciechanover, A. (2002). The ubiquitin proteasome proteolytic pathway: destruction for the sake of construction. Physiol. Rev.82, 373–428.10.1152/physrev.00027.2001Search in Google Scholar PubMed
Griffiths, H.R. (2000). Antioxidants and protein oxidation. Free Radic. Res.33, S47–S58.Search in Google Scholar
Grune, T., Reinheckel, T., and Davies, K.J.A. (1997). Degradation of oxidized proteins in mammalian cells. FASEB J.11, 526–534.10.1096/fasebj.11.7.9212076Search in Google Scholar
Grune, T., Jung, T., Merker, K., and Davies, K.J.A. (2004). Decreased proteolysis caused by protein aggregates, inclusion bodies, plaques, lipofuscin, ceroid, and ‘aggresomes’ during oxidative stress, aging, and disease. Int. J. Biochem. Cell. Biol.36, 2519–2530.10.1016/j.biocel.2004.04.020Search in Google Scholar PubMed
Keck, S., Nitsch, R., Grune, T., and Ullrich, O. (2003). Proteasome inhibition by paired helical filament-tau in brains of patients with Alzheimer's disease. J. Neurochem.85, 115–122.10.1046/j.1471-4159.2003.01642.xSearch in Google Scholar
Keller, J.N., Hanni, K.B., and Markesbery, W.R. (2000). Impaired proteasome function in Alzheimer's disease. J. Neurochem.75, 436–439.10.1046/j.1471-4159.2000.0750436.xSearch in Google Scholar
Lasch, P., Petras, T., Ullrich, O., Backmann, J., Naumann, D., and Grune, T. (2001). Hydrogen peroxide-induced structural alterations of RNAse A. J. Biol. Chem.276, 9492–9502.10.1074/jbc.M008528200Search in Google Scholar
Luxford, C., Dean, R.T., and Davies, M.J. (2000). Radicals derived from histone hydroperoxides damage nucleobases in RNA and DNA. Chem. Res. Toxicol.13, 665–672.10.1021/tx000053uSearch in Google Scholar
Mary, J., Vougier, S., Picot, C.R., Perichon, M., Petropoulos, I., and Friguet, B. (2004). Enzymatic reactions involved in the repair of oxidized proteins. Exp. Gerontol.39, 1117–1123.10.1016/j.exger.2004.06.008Search in Google Scholar
Merker, K., Stolzing, A., and Grune, T. (2001). Proteolysis, caloric restriction and aging. Mech. Aging Dev.122, 595–615.10.1016/S0047-6374(01)00219-6Search in Google Scholar
Merker, K., Ullrich, O., Schmidt, H., Sitte, N., and Grune, T. (2003). Stability of the nuclear protein turnover during cellular senescence of human fibroblasts. FASEB J.17, 1963–1965.10.1096/fj.03-0177fjeSearch in Google Scholar PubMed
Morin, B., Davies, M.J., and Dean, R.T. (1998). The protein oxidation product 3,4-dihydroxyphenylalanine (DOPA) mediates oxidative DNA damage. Biochem. J.330, 1059–1067.10.1042/bj3301059Search in Google Scholar PubMed PubMed Central
Naskalski, J.W. and Bartosz, G. (2000). Oxidative modifications of protein structures. Adv. Clin. Chem.35, 161–253.10.1016/S0065-2423(01)35017-5Search in Google Scholar
Reinheckel, T., Sitte, N., Ullrich, O., Kuckelkorn, U., Davies, K.J.A., and Grune, T. (1998). Comparative resistance of the 20S and 26S proteasome to oxidative stress. Biochem. J.335, 637–642.10.1042/bj3350637Search in Google Scholar PubMed PubMed Central
Reinheckel, T., Ullrich, O., Sitte, N., and Grune, T. (2000). Differential impairment of 20S and 26S proteasome activities in human hematopoietic K562 cells during oxidative stress. Arch. Biochem. Biophys.377, 65–68.10.1006/abbi.2000.1717Search in Google Scholar PubMed
Rivett, A.J. (1998). Intracellular distribution of proteasomes. Curr. Opin. Immunol.10, 110–114.10.1016/S0952-7915(98)80040-XSearch in Google Scholar
Rivett, A.J. and Hearn, A.R. (2004). Proteasome function in antigen presentation: immunoproteasome complexes, peptide production, and interactions with viral proteins. Curr. Protein Pept. Sci.5, 153–161.10.2174/1389203043379774Search in Google Scholar
Rock, K.L., Gramm, C., Rothstein, L., Clark, L.K., Stein, R., Dick, L., Hwang, D., and Goldberg, A.L. (1994). Inhibitors of proteasome block the degradation of most cell proteins and the generation of peptides on MHC class I molecules. Cell78, 761–771.10.1016/S0092-8674(94)90462-6Search in Google Scholar
Shringarpure, R., Grune, T., Sitte, N., and Davies, K.J.A. (2000). 4-Hydroxynonenal-modified amyloid-beta peptide inhibits the proteasome: possible importance in Alzheimer's disease. Cell. Mol. Life Sci.57, 1802–1809.10.1007/PL00000660Search in Google Scholar
Sitte, N., Huber, M., Grune, T., Ladhoff, A., Doecke, W.-D., von Zglinicki, T., and Davies, K.J.A. (2000a). Proteasome inhibition by lipofuscin/ceroid during postmitotic aging of fibroblasts. FASEB J.14, 1490–1498.10.1096/fj.99-0843comSearch in Google Scholar
Sitte, N., Merker, K., von Zglinicki, T., and Grune, T. (2000b). Protein oxidation and degradation during proliferative senescence of human MRC-5 fibroblasts. Free Radic. Biol. Med.28, 701–708.10.1016/S0891-5849(99)00279-8Search in Google Scholar
Stadtman, E.R. (1992). Protein oxidation and aging. Science257, 1220–1224.10.1126/science.1355616Search in Google Scholar PubMed
Stadtman, E.R. (1993). Oxidation of free amino acids and amino acid residues in proteins by radiolysis and by metal-catalyzed reactions. Annu. Rev. Biochem.62, 797–821.10.1146/annurev.bi.62.070193.004053Search in Google Scholar PubMed
Stolzing, A. and Grune, T. (2001). The proteasome and its function in the ageing process. Clin. Exp. Dermatol.26, 566–572.10.1046/j.1365-2230.2001.00867.xSearch in Google Scholar PubMed
Strack, P.R., Waxman, L., and Fagan, J.M. (1996). Activation of the multicatalytic endopeptidase by oxidants. Effects on enzyme structure. Biochemistry35, 7142–7149.10.1021/bi9518048Search in Google Scholar
Tanahashi, N., Murakami, Y., Minami, Y., Shimbara, N., Hendil, K.B., and Tanaka, K. (2000). Hybrid proteasomes. Induction by interferon-γ and contribution to ATP-dependent proteolysis. J. Biol. Chem.275, 14336–14345.10.1074/jbc.275.19.14336Search in Google Scholar PubMed
Ullrich, O. and Grune, T. (2001). Proteasomal degradation of oxidatively damaged endogenous histones in K562 human leukemic cells. Free Radic. Biol. Med.31, 887–893.10.1016/S0891-5849(01)00672-4Search in Google Scholar
Ullrich, O., Reinheckel, T., Sitte, N., Hass, R., Grune, T., and Davies, K.J.A. (1999). Poly-ADP ribose polymerase activates nuclear proteasome to degrade oxidatively damaged histones. Proc. Natl. Acad. Sci. USA96, 6223–6228.10.1073/pnas.96.11.6223Search in Google Scholar PubMed PubMed Central
©2006 by Walter de Gruyter Berlin New York
Articles in the same Issue
- Highlight: Redox signaling – mechanisms and biological impact
- Paper of the Year 2005: Award to Vanessa Ferreira Merino
- Two-site substrate recognition model for the Keap1-Nrf2 system: a hinge and latch mechanism
- Hypoxia and lipid signaling
- Glutathione peroxidases and redox-regulated transcription factors
- Redox regulation of the hypoxia-inducible factor
- The l-arginine nitric oxide pathway: avenue for a multiple-level approach to assess vascular function
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- Mitochondrial signaling, TOR, and life span
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- First identification of a phosphorylcholine-substituted protein from Caenorhabditis elegans: isolation and characterization of the aspartyl protease ASP-6
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Articles in the same Issue
- Highlight: Redox signaling – mechanisms and biological impact
- Paper of the Year 2005: Award to Vanessa Ferreira Merino
- Two-site substrate recognition model for the Keap1-Nrf2 system: a hinge and latch mechanism
- Hypoxia and lipid signaling
- Glutathione peroxidases and redox-regulated transcription factors
- Redox regulation of the hypoxia-inducible factor
- The l-arginine nitric oxide pathway: avenue for a multiple-level approach to assess vascular function
- Protein oxidation and proteolysis
- Mitochondrial signaling, TOR, and life span
- Pathogenetic interplay between osmotic and oxidative stress: the hepatic encephalopathy paradigm
- Regulation of redox-sensitive exofacial protein thiols in CHO cells
- N-Ethylmaleimide-sensitive factor: a redox sensor in exocytosis
- Aspects of the biological redox chemistry of cysteine: from simple redox responses to sophisticated signalling pathways
- Singlet oxygen inactivates protein tyrosine phosphatase-1B by oxidation of the active site cysteine
- Regulatory effects of the mitochondrial energetic status on mitochondrial p66Shc
- Air pollution-associated fly ash particles induce fibrotic mechanisms in primary fibroblasts
- Incinerator fly ash provokes alteration of redox equilibrium and liberation of arachidonic acid in vitro
- Unique neuronal functions of cathepsin L and cathepsin B in secretory vesicles: biosynthesis of peptides in neurotransmission and neurodegenerative disease
- Two novel mitochondrial and chloroplastic targeting-peptide-degrading peptidasomes in A. thaliana, AtPreP1 and AtPreP2
- Switch from actin α1 to α2 expression and upregulation of biomarkers for pressure overload and cardiac hypertrophy in taurine-deficient mouse heart
- Human RBM28 protein is a specific nucleolar component of the spliceosomal snRNPs
- The β12-β13 loop is a key regulatory element for the activity and properties of the catalytic domain of protein phosphatase 1 and 2B
- DNA-binding properties of the recombinant high-mobility-group-like AT-hook-containing region from human BRG1 protein
- Papaya glutamine cyclotransferase shows a singular five-fold β-propeller architecture that suggests a novel reaction mechanism
- First identification of a phosphorylcholine-substituted protein from Caenorhabditis elegans: isolation and characterization of the aspartyl protease ASP-6
- The human cathelicidin peptide LL-37 and truncated variants induce segregation of lipids and proteins in the plasma membrane of Candida albicans
- Specificity of human cathepsin S determined by processing of peptide substrates and MHC class II-associated invariant chain
- Mast cell-dependent activation of pro matrix metalloprotease 2: a role for serglycin proteoglycan-dependent mast cell proteases
