Oxidized proteins: Mechanisms of removal and consequences of accumulation
Abstract
Elevated levels of oxidized proteins are reported in diseased tissue from age‐related pathologies such as atherosclerosis, neurodegenerative disorders, and cataract. Unlike the precise mechanisms that exist for the repair of nucleic acids, lipids, and carbohydrates, the primary pathway for the repair of oxidized proteins is complete catabolism to their constitutive amino acids. This process can be inefficient as is evidenced by their accumulation. It is generally considered that damaged proteins are degraded by the proteasome; however, this is only true for mildly oxidized proteins, because substrates must be unfolded to enter the narrow catalytic core. Rather, evidence suggests that moderately or heavily oxidized proteins are endocytosed and enter the endosomal/lysosomal system, indicating co‐operation between the proteasomes and the lysosomes. Heavily modified substrates are incompletely degraded and accumulate within the lysosomal compartments resulting in the formation of lipofuscin‐like, autofluorescent aggregates. Accumulation eventually results in impaired turnover of large organelles such as proteasomes and mitochondria, lysosomal destablization, leakage of proteases into the cytosol and apoptosis. In this review, we summarize reports published since our last assessments of the field of oxidized protein degradation including a role for modified proteins in the induction of apoptosis. © 2009 IUBMB IUBMB Life, 61(5): 522–527, 2009
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Proteasomes can mildly degrade oxidized proteins, so protein oxidative damage can be considered temporary.
“It is well known that proteasomes (complex intracellular proteases) are able to mildly degrade oxidized proteins (Dunlop et al. 2009) and therefore protein oxidative damage can be considered temporary.”
From Reactive Oxygen Species, Toxicity, Oxidative Stress, and Antioxidants: Chronic Diseases and Aging (2023) · cites this paper as Dunlop et al. 2009
Cites
Role of oxidative stress in diabetic complications: a new perspective on an old paradigm.
Baynes, J. W., & Thorpe, S. R. (1999) · Diabetes · doi:10.2337/diabetes.48.1.1 · Cited by 2,441 · see citing works
Watts, G. D. J., Wymer, J., Kovach, M. J., Mehta, S. G., Mumm, S., Darvish, D., Pestronk, A., Whyte, M. P., & Kimonis, V. E. (2004) · Nature Genetics · doi:10.1038/ng1332 · Cited by 1,391 · see citing works
Stadtman, E. R. (2006) · Free Radical Research · doi:10.1080/10715760600918142 · Cited by 1,056 · see citing works
Misfolded proteins partition between two distinct quality control compartments
Kaganovich, D., Kopito, R., & Frydman, J. (2008) · Nature · doi:10.1038/nature07195 · Cited by 932 · see citing works
Diversity of degradation signals in the ubiquitin–proteasome system
Ravid, T., & Hochstrasser, M. (2008) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2468 · Cited by 831 · see citing works
Proteasomal function is impaired in substantia nigra in Parkinson’s disease
McNaught, K. S. P., & Jenner, P. (2001) · Neuroscience Letters · doi:10.1016/s0304-3940(00)01701-8 · Cited by 653 · see citing works
Activation of Chaperone-mediated Autophagy during Oxidative Stress
Kiffin, R., Christian, C., Knecht, E., & Cuervo, A. M. (2004) · Molecular Biology of the Cell · doi:10.1091/mbc.e04-06-0477 · Cited by 611 · see citing works
The Sizes of Peptides Generated from Protein by Mammalian 26 and 20 S Proteasomes
Kisselev, A. F., Akopian, T. N., Woo, K. M., & Goldberg, A. L. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.6.3363 · Cited by 573 · see citing works
Altered proteasomal function in sporadic Parkinson’s disease
St. P. McNaught, K., Belizaire, R., Isacson, O., Jenner, P., & Olanow, C. W. (2003) · Experimental Neurology · doi:10.1006/exnr.2002.8050 · Cited by 573 · see citing works
Zhang, C., & Cuervo, A. M. (2008) · Nature Medicine · doi:10.1038/nm.1851 · Cited by 520 · see citing works
Ubiquitin Conjugation Is Not Required for the Degradation of Oxidized Proteins by Proteasome
Shringarpure, R., Grune, T., Mehlhase, J., & Davies, K. J. A. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m206279200 · Cited by 438 · see citing works
Lipofuscin: Formation, Distribution, and Metabolic Consequences
JUNG, T., BADER, N., & GRUNE, T. (2007) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1404.008 · Cited by 415 · see citing works
Proteolysis in Cultured Liver Epithelial Cells during Oxidative Stress
Grune, T., Reinheckel, T., Joshi, M., & Davies, K. J. A. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.5.2344 · Cited by 407 · see citing works
A molecular chaperone complex at the lysosomal membrane is required for protein translocation
Agarraberes, F. A., & Dice, J. F. (2001) · Journal of Cell Science · doi:10.1242/jcs.114.13.2491 · Cited by 404 · see citing works
Droga-Mazovec, G., Bojič, L., Petelin, A., Ivanova, S., Romih, R., Repnik, U., Salvesen, G. S., Stoka, V., Turk, V., & Turk, B. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m802513200 · Cited by 399 · see citing works
Role of Oxidant Species in Aging
Stadtman, E. R. (2004) · Current Medicinal Chemistry · doi:10.2174/0929867043365341 · Cited by 368 · cited 1× · see citing works
“tionally, increased levels of oxidized proteins are observable in tissues from older animals (42), whereas caloric restriction designed to increase life-span results in a reduction in the extent of protein damage (43).”
BackgroundTanahashi, N., Murakami, Y., Minami, Y., Shimbara, N., Hendil, K. B., & Tanaka, K. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.19.14336 · Cited by 347 · see citing works
McNaught, K. S. P., Mytilineou, C., JnoBaptiste, R., Yabut, J. A., Shashidharan, P., Jenner, P. G., & Olanow, C. W. (2002) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2002.00821.x · Cited by 304 · see citing works
Lysosomes in iron metabolism, ageing and apoptosis
Kurz, T., Terman, A., Gustafsson, B., & Brunk, U. T. (2008) · Histochemistry and Cell Biology · doi:10.1007/s00418-008-0394-y · Cited by 302 · see citing works
Self-citationIFN-γ-induced immune adaptation of the proteasome system is an accelerated and transient response
Heink, S., Ludwig, D., Kloetzel, P., & Krüger, E. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0501711102 · Cited by 288 · see citing works
Tanoka, K., & Kasahara, M. (1998) · Immunological Reviews · doi:10.1111/j.1600-065x.1998.tb01195.x · Cited by 282 · see citing works
Rukhsana Sultana, A., Marzia Perluigi, A., & Butterfield, D. A. (2006) · Antioxidants and Redox Signaling · doi:10.1089/ars.2006.8.2021 · Cited by 261 · see citing works
Reits, E. A., Neijssen, J., Herberts, C. A., Benckhuijsen, W. E., Janssen, L., Drijfhout, J. W., & Neefjes, J. (2004) · Immunity · doi:10.1016/s1074-7613(04)00074-3 · Cited by 261 · see citing works
Evidence for roles of radicals in protein oxidation in advanced human atherosclerotic plaque
Fu, S., Davies, M. J., Stocker, R., & Dean, R. T. (1998) · Biochemical Journal · doi:10.1042/bj3330519 · Cited by 256 · see citing works
The calpains: modular designs and functional diversity
Croall, D. E., & Ersfeld, K. (2007) · Genome biology · doi:10.1186/gb-2007-8-6-218 · Cited by 221 · see citing works
Radical-Mediated Protein Oxidation
Davies, M. J., & Dean, R. T. (1997) · doi:10.1093/oso/9780198500971.001.0001 · Cited by 219 · see citing works
Ubiquitin-independent degradation of proteins by the proteasome
Jariel‐Encontre, I., Bossis, G., & Piechaczyk, M. (2008) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2008.05.004 · Cited by 198 · see citing works
Recognition of Misfolding Proteins by PA700, the Regulatory Subcomplex of the 26 S Proteasome
Strickland, E., Hakala, K. W., Thomas, P., & Demartino, G. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.8.5565 · Cited by 187 · see citing works
The Hydroxyl Radical in Lens Nuclear Cataractogenesis
Fu, S., Dean, R. T., Southan, M., & Truscott, R. J. W. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.44.28603 · Cited by 177 · see citing works
Medicherla, B., & Goldberg, A. L. (2008) · The Journal of Cell Biology · doi:10.1083/jcb.200803022 · Cited by 175 · see citing works
Proteasome‐dependent degradation of oxidized proteins in MRC‐5 fibroblasts
Sitte, N., Merker, K., & Grune, T. (1998) · FEBS Letters · doi:10.1016/s0014-5793(98)01495-1 · Cited by 171 · see citing works
The proteasome and its role in the degradation of oxidized proteins
Jung, T., & Grune, T. (2008) · IUBMB Life · doi:10.1002/iub.114 · Cited by 162 · see citing works
Kaushik, S., & Cuervo, A. M. (2006) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2006.08.007 · Cited by 145 · see citing works
Fagan, J. M., Waxman, L., & Goldberg, A. L. (1986) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)38440-5 · Cited by 134 · see citing works
Ryhänen, T., Hyttinen, J. M. T., Kopitz, J., Rilla, K., Kuusisto, E., Mannermaa, E., Viiri, J., Holmberg, C. I., Immonen, I., Meri, S., et al. (2009) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2008.00577.x · Cited by 131 · see citing works
Methionine Sulfoxide Reductases
Cabreiro, F., Picot, C. R., Friguet, B., & Petropoulos, I. (2006) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1354.006 · Cited by 120 · see citing works
Wihlmark, U., Wrigstad, A., Roberg, K. B., NILSSON, S. E. G., & Brunk, U. T. (1997) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(96)00555-2 · Cited by 119 · see citing works
Self-citationNucleus-Vacuole Junctions and Piecemeal Microautophagy of the Nucleus inS. cerevisiae
Kvam, E., & Goldfarb, D. S. (2007) · Autophagy · doi:10.4161/auto.3586 · Cited by 116 · see citing works
Tarcsa, E., Szymańska, G., Lecker, S. H., O’Connor, C. M., & Goldberg, A. L. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m001555200 · Cited by 111 · see citing works
Dysregulation of the Ubiquitin-Proteasome System in Human Carotid Atherosclerosis
Versari, D., Herrmann, J., Gössl, M., Mannheim, D., Sattler, K., Meyer, F. B., Lerman, L. O., & Lerman, A. (2006) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000232501.08576.73 · Cited by 111 · see citing works
Chowers, I., Wong, R., Dentchev, T., Farkas, R. H., Iacovelli, J., Gunatilaka, T. L., Medeiros, N. E., Presley, J. B., Campochiaro, P. A., Curcio, C. A., et al. (2006) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.05-1135 · Cited by 102 · see citing works
England, K., O’Driscoll, C. M., & Cotter, T. G. (2003) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4401338 · Cited by 102 · see citing works
Age-Related Macular Degeneration and Retinal Protein Modification by 4-Hydroxy-2-nonenal
Ethen, C. M., Reilly, C., Feng, X., Olsen, T. W., & Ferrington, D. A. (2007) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.06-1058 · Cited by 89 · see citing works
Recent developments in the intracellular degradation of oxidized proteins
Dunlop, R. A., Rodgers, K. J., & Dean, R. T. (2002) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(02)00958-9 · Cited by 78 · see citing works
Self-citationBiosynthetic incorporation of oxidized amino acids into proteins and their cellular proteolysis
Rodgers, K. J., Wang, H., Fu, S., & Dean, R. T. (2002) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(02)00768-2 · Cited by 71 · see citing works
Self-citationEvidence for L‐dopa incorporation into cell proteins in patients treated with levodopa
Rodgers, K. J., Hume, P. M., Morris, J. G., & Dean, R. T. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.03941.x · Cited by 43 · see citing works
Self-citationThe impact of specific oxidized amino acids on protein turnover in J774 cells
Dunlop, R. A., Dean, R. T., & Rodgers, K. J. (2008) · Biochemical Journal · doi:10.1042/bj20070161 · Cited by 43 · see citing works
Self-citationROS and protein oxidation in early stages of cytotoxic drug induced apoptosis
England, K., 'Driscoll, C. O., & Cotter, T. G. (2006) · Free Radical Research · doi:10.1080/10715760600838209 · Cited by 37 · see citing works
Human apo-lipoprotein B from normal plasma contains oxidised peptides
Bruce, D. (1999) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/s1357-2725(99)00107-7 · Cited by 19 · see citing works
Dean, R. T., Dunlop, R. A., Hume, P. M., & Rodgers, K. J. (2003) · Biochemical Society Symposia · doi:10.1042/bss0700135 · Cited by 15 · see citing works
Self-citationA pathway of lysosomal proteolysis mediated by the 73-kilodalton heat shock cognate protein.
Terlecky, S. R., Olson, T. S., & Dice, J. F. (1991) · PubMed · Cited by 6 · see citing works
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Terman, A., Kurz, T., Navratil, M., Arriaga, E. A., & Brunk, U. T. (2010) · Antioxidants & Redox Signaling · doi:10.1089/ars.2009.2598 · Cited by 490 · see citing works
Self-citationLai, R. C., Tan, S. S., Teh, B. J., Sze, S. K., Arslan, F., de Kleijn, D. P. V., Choo, A. B. H., & Lim, S. K. (2012) · International Journal of Proteomics · doi:10.1155/2012/971907 · Cited by 485 · see citing works
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Varga, Z. V., Giricz, Z., Liaudet, L., Haskó, G., Ferdinandy, P., & Pacher, P. (2014) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2014.06.030 · Cited by 288 · see citing works
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Aldini, G., Vistoli, G., Štefek, M., Chondrogianni, N., Grune, T., Sereikaitė, J., Sadowska‐Bartosz, I., & Bartosz, G. (2013) · Free Radical Research · doi:10.3109/10715762.2013.792926 · Cited by 151 · see citing works
Zhao, Y., Zhang, C., Rossiter, H., Eckhart, L., König, U., Karner, S., Mildner, M., Bochkov, V. N., Tschachler, E., & Грубер, Ф. (2013) · Journal of Investigative Dermatology · doi:10.1038/jid.2013.26 · Cited by 135 · see citing works
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Qiu, Y., Shen, X., Shyam, R., Yue, B. Y. J. T., & Ying, H. (2014) · PLoS ONE · doi:10.1371/journal.pone.0092845 · Cited by 37 · see citing works
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Chaudhary, P., Sharma, Y. K., Sharma, S., Singh, S. N., & Suryakumar, G. (2019) · Biochimie · doi:10.1016/j.biochi.2018.10.012 · Cited by 35 · see citing works
Cabet, É., Batonnet‐Pichon, S., Delort, F., Gausserès, B., Vicart, P., & Lilienbaum, A. (2015) · PLoS ONE · doi:10.1371/journal.pone.0137009 · Cited by 35 · see citing works
Davies, M. J. (2012) · Wiley eBooks · doi:10.1002/9781119953678.rad045 · Cited by 34 · see citing works
Hatasa, Y., Chikazawa, M., Furuhashi, M., Nakashima, F., Shibata, T., Kondo, T., Akagawa, M., Hamagami, H., TANAKA, H. L., Tachibana, H., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0153002 · Cited by 33 · see citing works
Marinelli, P., Navarro, S., Graña‐Montes, R., Bañó‐Polo, M., Fernández, M. R., Papaleo, E., & Ventura, S. (2017) · Redox Biology · doi:10.1016/j.redox.2017.10.022 · Cited by 33 · see citing works
Redox Proteomes in Human Physiology and Disease Mechanisms
Mannaa, A. M., & Hanisch, F. (2019) · Journal of Proteome Research · doi:10.1021/acs.jproteome.9b00586 · Cited by 34 · see citing works
Retinal Pigment Epithelium Under Oxidative Stress: Chaperoning Autophagy and Beyond
Markitantova, Y. V., & Simirskii, V. N. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26031193 · Cited by 32 · see citing works
Piyanova, A., Albayram, Ö., Rossi, C. A., Farwanah, H., Michel, K., Nicotera, P., Sandhoff, K., & Bilkei‐Gorzó, A. (2013) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2013.08.001 · Cited by 31 · see citing works
Devarajan, A., Rajasekaran, N. S., Valburg, C., Ganapathy, E., Bindra, S., & Freije, W. A. (2018) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2018.09.029 · Cited by 30 · see citing works
Jasour, M. S., Wagner, L., Sundekilde, U. K., Larsen, B. K., Rasmussen, H. T., Hjermitslev, N. H., Hammershøj, M., Dalsgaard, J., & Dalsgaard, T. K. (2018) · Aquaculture · doi:10.1016/j.aquaculture.2018.01.030 · Cited by 30 · see citing works
The microtubule-targeting agent T0070907 induces proteasomal degradation of tubulin
Harris, G., & Schaefer, K. L. (2009) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2009.08.009 · Cited by 29 · see citing works
Cathepsin D contributes to the accumulation of advanced glycation end products during photoaging
Xu, X., Zheng, Y., Huang, Y., Chen, J., Gong, Z., Li, Y., Lu, C., Lai, W., & Xu, Q. (2018) · Journal of Dermatological Science · doi:10.1016/j.jdermsci.2018.02.009 · Cited by 28 · see citing works
Proteins containing oxidized amino acids induce apoptosis in human monocytes
Dunlop, R. A., Brunk, U. T., & Rodgers, K. J. (2011) · Biochemical Journal · doi:10.1042/bj20100682 · Cited by 28 · see citing works
Self-citationAjuwon, O. R., Marnewick, J. L., & Davids, L. M. (2015) · InTech eBooks · doi:10.5772/61614 · Cited by 29 · see citing works
Fumonisin B 1 ‐induced mitochondrial toxicity and hepatoprotective potential of rooibos: An update
Abdul, N. S., & Marnewick, J. L. (2020) · Journal of Applied Toxicology · doi:10.1002/jat.4036 · Cited by 28 · see citing works
Selectivity in ROS-Induced Peptide Backbone Bond Cleavage
Stringfellow, H. M., Jones, M. R., Green, M. C., Wilson, A. K., & Francisco, J. S. (2014) · The Journal of Physical Chemistry A · doi:10.1021/jp508877m · Cited by 28 · see citing works
Hutchinson-Gilford progeria syndrome, cardiovascular disease and oxidative stress
Trigueros‐Motos, L. (2011) · Frontiers in Bioscience-Scholar · doi:10.2741/226 · Cited by 26 · see citing works
The use of Cerastoderma glaucum as a sentinel and bioindicator species: Take-home message
Velez, C., Pires, A., Sampaio, L., Cardoso, P., Moreira, A., Leandro, S. M., Figueira, E. M. D. A. P., Soares, A. M. V. M., & Freitas, R. (2015) · Ecological Indicators · doi:10.1016/j.ecolind.2015.10.051 · Cited by 26 · see citing works
Zheng, J., & Bizzozero, O. A. (2010) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2010.07062.x · Cited by 24 · see citing works
Nożyński, J. K., Zakliczynski, M., Konecka-Mrówka, D., Zakliczyńska, H., Pijet, M., Zembala‐Nożyńska, E., Lange, D., & Zembala, M. (2012) · Experimental Gerontology · doi:10.1016/j.exger.2012.09.002 · Cited by 24 · see citing works
Proteasome Biology Is Compromised in White Matter After Asphyxic Cardiac Arrest in Neonatal Piglets
Santos, P. T., O’Brien, C. E., Chen, M. W., Hopkins, C. D., Adams, S., Kulikowicz, E., Singh, R. P., Koehler, R. C., Martin, L. J., & Lee, J. K. (2018) · Journal of the American Heart Association · doi:10.1161/jaha.118.009415 · Cited by 22 · see citing works
Straub, C. P., Lau, W.-H., Preston, F. M., Headlam, M. J., Gorman, J. J., Collins, P. L., & Spann, K. M. (2011) · Virology Journal · doi:10.1186/1743-422x-8-252 · Cited by 22 · see citing works
Functional SNP in 3′-UTR MicroRNA-Binding Site ofZNF350Confers Risk for Age-Related Cataract
Gu, S., Rong, H., Zhang, G., Kang, L., Yang, M., & Guan, H. (2016) · Human Mutation · doi:10.1002/humu.23073 · Cited by 21 · see citing works
Recent information on photoaging mechanisms and the preventive role of topical sunscreen products
Pedić, L., Pondeljak, N., & Šitum, M. (2020) · Acta Dermatovenerologica Alpina Pannonica et Adriatica · doi:10.15570/actaapa.2020.40 · Cited by 22 · see citing works
Moheimani, F., Kim, C. H. J., Rahmanto, A. S., van Reyk, D. M., & Davies, M. J. (2012) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2012.04.026 · Cited by 19 · see citing works
Oxidised protein metabolism: recent insights
Samardzic, K., & Rodgers, K. J. (2017) · Biological Chemistry · doi:10.1515/hsz-2017-0124 · Cited by 18 · see citing works
Self-citationElevated Plasma Dityrosine in Patients with Hyperlipidemia Compared to Healthy Individuals
Wu, G., Cheserek, M. J., Shi, Y., Shen, L., Yu, J., & Le, G. (2014) · Annals of Nutrition and Metabolism · doi:10.1159/000365731 · Cited by 17 · see citing works
The complex modulation of lysosomal degradation pathways by cannabinoid receptors 1 and 2
Hiebel, C., & Behl, C. (2015) · Life Sciences · doi:10.1016/j.lfs.2015.03.020 · Cited by 16 · see citing works
Oxidative Stress and Cell Function
Avery, S. V. (2014) · Springer eBooks · doi:10.1007/978-3-642-30018-9_3 · Cited by 16 · see citing works
Zhang, Y., Chang, F.-M., Huang, J., Junco, J. J., Maffi, S. K., Pridgen, H. I., Catano, G., Dang, H., Ding, X. D., Yang, F., et al. (2014) · Protein & Cell · doi:10.1007/s13238-013-0018-8 · Cited by 15 · see citing works
Temporal- and Location-Specific Alterations of the GABA Recycling System in Mecp2 KO Mouse Brains
Kang, S. K., Kim, S. T., Johnston, M. V., & Kadam, S. D. (2014) · Journal of Central Nervous System Disease · doi:10.4137/jcnsd.s14012 · Cited by 13 · see citing works
Cardiac Muscle Ring Finger-1—Friend or Foe?
Willis, M. S., Zungu, M., & Patterson, C. (2010) · Trends in Cardiovascular Medicine · doi:10.1016/j.tcm.2010.03.001 · Cited by 12 · see citing works
Sadowska‐Bartosz, I., Ott, C., Grune, T., & Bartosz, G. (2014) · Free Radical Research · doi:10.3109/10715762.2014.953494 · Cited by 12 · see citing works
Artemin protects cells and proteins against oxidative and salt stress
Takalloo, Z., Sajedi, R. H., Hosseinkhani, S., & Moazzenzade, T. (2016) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2016.11.088 · Cited by 11 · see citing works
Mitochondrial damage and clearance in retinal pigment epithelial cells
Gurubaran, I. S. (2024) · Acta Ophthalmologica · doi:10.1111/aos.16661 · Cited by 10 · see citing works
Demerdash, N. E., Chen, M. W., O’Brien, C. E., Adams, S., Kulikowicz, E., Martin, L. J., & Lee, J. K. (2021) · Cells · doi:10.3390/cells10082120 · Cited by 10 · see citing works
Lee, J. K., Santos, P. T., Chen, M. W., O’Brien, C. E., Kulikowicz, E., Adams, S., Hardart, H., Koehler, R. C., & Martin, L. J. (2020) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/nlaa132 · Cited by 10 · see citing works
Santos, S. S., de Oliveira, H. A., Antônio, E. L., Teixeira, I. L. A., Mansano, B. S. D. M., Silva, F. A., de Carvalho, P. D. T. C., Tucci, P. J. F., & Serra, A. J. (2020) · Lasers in Medical Science · doi:10.1007/s10103-020-02951-1 · Cited by 9 · see citing works
Protein Stability and Unfolding Following Glycine Radical Formation
Owen, M. C., Csizmadia, I. G., Viskolcz, B., & Strodel, B. (2017) · Molecules · doi:10.3390/molecules22040655 · Cited by 8 · see citing works
Coles, N. P., Elsheikh, S., Quesnel, A., Butler, L., Achadu, O. J., Islam, M., Kalesh, K., Occhipinti, A., Angione, C., Marles‐Wright, J., et al. (2025) · Brain Communications · doi:10.1093/braincomms/fcaf133 · Cited by 8 · see citing works
Involvement of Gtr1p in the oxidative stress response in yeast Saccharomyces cerevisiae
Sekiguchi, T., Ishii, T., Kamada, Y., Funakoshi, M., Kobayashi, H., & Furuno, N. (2022) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2022.02.016 · Cited by 6 · see citing works
Nair, D., Nedungadi, D., Mishra, N., Nair, B. G., & Nair, S. S. (2021) · Biomedical Chromatography · doi:10.1002/bmc.5065 · Cited by 6 · see citing works
Pollutants and Oxidative Stress
Neto, F. F. (2014) · CRC Press eBooks · doi:10.1201/b16298-8 · Cited by 6 · see citing works
Kurepa, J., Shull, T. E., Fisher, A., Fisher, C., Ji, H., & Smalle, J. (2021) · Journal of Plant Physiology · doi:10.1016/j.jplph.2021.153429 · Cited by 4 · see citing works
EFFECTS OF NICOTINIC ACID ON PROTEIN OXIDATIVE MODIFICATIONS IN EXPERIMENTAL CHRONIC HEART FAILURE
Nizhenkovska, I. (2018) · FARMACIA · doi:10.31925/farmacia.2018.6.5 · Cited by 6 · see citing works
Hutchinson-Gilford progeria syndrome cardiovascular disease and oxidative stress
Andrés, V. (2011) · Frontiers in Bioscience-Scholar · doi:10.2741/s226 · Cited by 4 · see citing works
Stimulation of Tau Degradation
Quintanilla, R. A., Cabezas-Opazo, F., Pallo, S. P., Chesser, A. S., & Johnson, G. V. W. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-802173-6.00013-7 · Cited by 3 · see citing works
Theories and Mechanisms of Aging
Behl, C., & Ziegler, C. (2013) · SpringerBriefs in molecular medicine · doi:10.1007/978-3-642-45179-9_3 · Cited by 3 · see citing works
Phillips, C. R., Violi, J. P., Bishop, D., & Rodgers, K. J. (2026) · Amino Acids · doi:10.1007/s00726-025-03491-0 · Cited by 2 · see citing works
Self-citationCutaneous Oxidative Stress and Aging
Polefka, T. G., & Meyer, T. A. (2015) · Springer eBooks · doi:10.1007/978-3-642-27814-3_123-1 · Cited by 2 · see citing works
Cui, T., & Wang, X. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-805253-2.00003-1 · Cited by 2 · see citing works
Rojas‐Figueroa, A., Angulo, C., Granados-Amores, A., Correa-Reyes, J. G., & Saucedo, P. E. (2026) · Aquaculture · doi:10.1016/j.aquaculture.2026.743664 · Cited by 1 · see citing works
- Authors
- Dunlop, R. A., Brunk, U. T., & Rodgers, K. J.
- Affiliations
- Linköping University (SE)
- Corresponding author
- Dunlop, Rachael A.
- Brunk, Ulf T.
- Rodgers, Kenneth J.
- Venue
- IUBMB Life
- Publisher
- Wiley
- Published
- 2009-04-23
- Volume
- 61
- Issue
- 5
- Pages
- 522-527
- ISSN
- 1521-6543 (ISSN-L)
- 1521-6551
- OpenAlex
- W2008128102
- Cited by
- 124
- References
- 51
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 1 · 2023: 3 · 2022: 1 · 2021: 4 · 2020: 7 · 2019: 5 · 2018: 9 · 2017: 8 · 2016: 13 · 2015: 12 · 2014: 17 · 2013: 7 · 2012: 10
- FWCI
- 1.29
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- IUBMB Life (publishedVersion)
- PubMed (publishedVersion)
- OPUS - Open Publications of UTS Scholars (University of Technology Sydney) (submittedVersion)
- Topics
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ubiquitin and proteasome pathways
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
- Keywords
- oxidized proteins, protein degradation, proteasome, lysosomes, endocytosis, endosomal-lysosomal system, lipofuscin, protein accumulation, apoptosis, mitochondrial dysfunction, lysosomal destabilization, age-related diseases, atherosclerosis, neurodegenerative diseases, cataract
- MeSH terms
- Aging, Lysosomes, Oxidation-Reduction, Proteins, Endosomes, Apoptosis, Proteasome Endopeptidase Complex
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