Abstract
Plant mitochondria produce reactive oxygen species (ROS) as an unavoidable side product of aerobic metabolism, but they have mechanisms for regulating this production such as the alternative oxidase. Once produced, ROS can be removed by several different enzyme systems. Finally, should the first two strategies fail, the ROS produced can act as a signal to the rest of the cell and/or cause damage to DNA, lipids and proteins. Proteins are modified in a variety of ways by ROS, some direct, others indirect e.g. by conjugation with breakdown products of fatty acid peroxidation. Reversible oxidation of cysteine and methionine side chains is an important mechanism for regulating enzyme activity. Mitochondria from both mammalian and plant tissues contain a number of oxidised proteins, but the relative abundance of these post-translationally modified forms is as yet unknown, as are the consequences of the modification for the properties and turnover time of the proteins. Specific proteins appear to be particularly vulnerable to oxidative carbonylation in the matrix of plant mitochondria; these include several enzymes of the Krebs cycle, glycine decarboxylase, superoxide dismutase and heat shock proteins. Plant mitochondria contain a number of different proteases, but their role in removing oxidatively damaged proteins is, as yet, unclear.
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Abbreviations
- AOX:
-
alternative oxidase
- CCO:
-
cytochrome c oxidase
- DPI:
-
diphenylene iodonium
- DNP:
-
dinitrophenylhydrazone
- DNPH:
-
dinitrophenylhydrazine
- ETC:
-
electron transport chain
- FDH:
-
formate dehydrogenase
- LC-MS:
-
liquid chromatography mass spectrometry
- PCD:
-
programmed cell death
- PUFA:
-
polyunsaturated fatty acids
- ROS:
-
reactive oxygen species
- SOD:
-
superoxide dismutase
References
F. Corpas, J. Barroso and L. A. del Rio Peroxisomes as a source of reactive oxygen species and nitric oxide signal molecules in plant cells Trends Plant Sci. 2003 6 145–150
C. H. Foyer and G. Noctor. Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria Physiol. Plant. 2003 119 355–364
D. P. Maxwell, Y. Wang and L., McIntosh, The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells Proc. Natl. Acad. Sci. U. S. A. 1999 96 8271–8276
F. A. Hoeberichts and E. J., Woltering, Multiple mediators of plant programmed cell death: interplay of conserved cell death mechanisms and plant-specific regulators Bioessays 2003 25 47–57
H. Düssmann, D. Kogel, M. Rehm and J. H. M., Prehn, Mitochondrial membrane permeabilization and superoxide production during apoptosis - A single-cell analysis J. Biol. Chem. 2003 278 12645–12649
M. Kim, J.-W. Ahn, U.-H. Jin, D. Choi, K.-H. Paek and H.-S. Pai Activation of the programmed cell death pathway by inhibition of proteasome function in plants J. Biol. Chem. 2003 278 19406–19415
I. M. Møller Plant mitochondria and oxidative stress: Electron transport, NADPH turnover, and metabolism of reactive oxygen species Annu. Rev. Plant Physiol. Plant Mol. Biol. 2001 52 561–591
V. Casolo, E. Braidot, E. Chiandussi, F. Macri and A., Vianello, The role of mild uncoupling and non-coupled respiration in the regulation of hydrogen peroxide generation by plant mitochondria FEBS Lett. 2000 474 53–57
M. Brandalise, I. G. Maia, J. Borecky, A. E. Vercesi and P., Arruda, Overexpression of plant uncoupling mitochondrial protein in transgenic tobacco increases tolerance to oxidative stress J. Bioenerg. Biomembr. 2003 35 203–209
J. Fang and D. S., Beattie, Rotenone-insensitive NADH dehydrogenase is a potential source of superoxide in procyclic Trypanosoma brucei mitochondria Mol. Biochem. Parasitol. 2002 123 135–142
J. F. Turrens and A., Boveris, Generation of superoxide anion by the NADH dehydrogenase of bovine heart-mitochondria Biochem. J. 1980 191 421–427
V. O’Donnell, G. Smith and O., Jones, Involvement of phenyl radicals in Iodonium compound inhibition of flavoenzymes Mol. Pharmacol. 2003 48 778–785
A. Majander, M. Finel and M. Wikström Diphenyleneiodonium inhibits reduction of iron-sulfur clusters in the mitochondrial NADH-ubiquinone oxidoreductase (Complex I) J. Biol. Chem. 1994 269 21037–21042
A. M. P. Melo, T. H. Roberts and I. M. Møller Evidence for the presence of two rotenone-insensitive NAD(P)H dehydrogenases on the inner surface of the inner membrane of potato tuber mitochondria Biochim. Biophys. Acta-Bioenerg. 1996 1276 133–139
S. C. Agius, N. V. Bykova, A. U. Igamberdiev and I. M. Møller The internal rotenone-insensitive NADPH dehydrogenase contributes to malate oxidation by potato tuber and pea leaf mitochondria Physiol. Plant. 1998 104 329–336
T. H. Roberts, K. M. Fredlund and I. M. Møller Direct evidence for the presence of 2 external NAD(P)H dehydrogenases coupled to the electron-transport chain in plant mitochondria FEBS Lett. 1995 373 307–309
M. Sabar, R. de Paepe and Y. de Kouchkovsky Complex I impairment, respiratory compensations, and photosynthetic decrease in nuclear and mitochondrial male sterile mutants of Nicotiana sylvestris Plant Physiol. 2000 124 1239–1249
C. Dutilleul, M. Garmier, G. Noctor, C. Mathieu, P. Chetrit, C. H. Foyer and R. de Paepe Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation Plant Cell 2003 15 1212–1226
T. Yagi, B. Seo, S. Di Bernardo, E. Nakamaru-Ogiso, M.-C. Kao and A. Matsuno-Yagi NADH dehydrogenases: From basic science to biomedicine J. Bioenerg. Biomembr. 2001 33 233–242
G. K. Agrawal, R. Rakwal, M. Yonekura, A. Kubo and H., Saji, Proteome analysis of differentially displayed proteins as a tool for investigating ozone stress in rice (Oryza sativa L.) seedlings Proteomics 2002 2 947–959
R. Rakwal, G. K. Agrawal, A. Kubo, M. Yonekura, S. Tamogami, H. Saji and H., Iwahashi, Defense/stress responses elicited in rice seedlings exposed to the gaseous air pollutant sulfur dioxide Environ. Exp. Bot. 2003 49 223–235
C. Bowler, L. Slooten, S. Vandenbranden, R. Derycke, J. Botterman, C. Sybesma, M. Vanmontagu and D., Inze, Manganese superoxide-dismutase can reduce cellular-damage mediated by oxygen radicals in transgenic plants EMBO J. 1991 10 1723–1732
W. Vancamp, H. Willekens, C. Bowler, H. Vanmontagu, D. Inze, P. Reupoldpopp, H. Sandermann and C., Langebartels, Elevated levels of superoxide-dismutase protect transgenic plants against ozone damage Bio-Technol. 1994 12 165–168
S. Pasqualini, C. Piccioni, L. Reale, L. Ederli, G. D. Torre and F., Ferranti, Ozone-induced cell death in Tobacco cultivar Bel W3 okabts, The role of programmed cell death in lesion formation Plant Physiol. 2003 133 1122–1134
K. Takubo, T. Morikawa, Y. Nonaka, M. Mizutani, S. Takenaka, K. Takabe, M. Takahaski and D., Ohta, Identification and molecular characterization of mitochondrial ferredoxins and ferredoxin reductase from Arabidopsis Plant Mol. Biol. 2003 52 817–830 The Prosthetic Groups and Metal Ions in Protein Active Sites Database, version 2.0, http://metallo.scripps.edu/PROMISE/MAIN.html
B. Halliwell and J. M. C. Gutteridge, Free Radicals in Biology and Medicine, Oxford University Press, Oxford, 3rd edn., 1998, pp. 1-936
V. N. Luzikov Mitochondrial Biog. Breakdown 19841–362
H. Bakala, E. Delaval, M. Hamelin, J. Bismuth, C. Borot-Laloi, B. Corman and B., Friguet, Changes in rat liver mitochondria with aging - Lon protease-like activity and N-epsiloncarboxymethyllysine accumulation in the matrix Eur. J. Biochem. 2003 270 2295–2302
D. Lloyd, K. A. Lemar, L. E. J. Salgado, T. M. Gould and D. B., Murray, Respiratory oscillations in yeast: mitochondrial reactive oxygen species, apoptosis and time; a hypothesis FEMS Yeast Res. 2003 3 333–339
H. Aguilaniu, L. Gustafsson, M. Rigoulet and T., Nystrom, Asymmetric inheritance of oxidatively damaged proteins during cytokinesis Science 2003 299 1751–1753
D. A. Bota and H. Van Remmen and K. J. A., Davies, Modulation of Lon protease activity and aconitase turnover during aging and oxidative stress FEBS Lett. 2002 532 103–106
R. T. Dean, S. L. Fu, R. Stocker and M. J., Davies, Biochemistry and pathology of radical-mediated protein oxidation Biochem. J. 1997 324 1–18
R. Rakhit, P. Cunningham, A. Furtos-Matei, S. Dahan, X. F. Qi, J. P. Crow, N. R. Cashman, L. H. Kondejewski and A., Chakrabartty, Oxidation-induced misfolding and aggregation of superoxide dismutase and its implications for amyotrophic lateral sclerosis J. Biol. Chem. 2002 277 47551–47556
E., Shacter, Quantification and significance of protein oxidation in biological samples Drug Metab. Rev. 2000 32 307–326 E. Shacter, http://www.medicine.uiowa.edu/FRRB/VirtualSchool/Virtual.html
P. Ghezzi and V., Bonetto, Redox proteomics: Identification of oxidatively, modified proteins Proteomics 2003 3 1145–1153
A. Konrad, M. Banze and F., Follmann, Mitochondria of plant leaves contain two thioredoxins. Completion of the thioredoxin profile of higher plants J. Plant Physiol. 1996 149 317–321
M. Banze and H., Follmann, Organelle-specific NADPH thioredoxin reductase in plant mitochondria J. Plant Physiol. 2000 156 126–129
V. Bunik, A. Shoubnikova, S. Loeffelhardt, H. Bisswanger, H. O. Borbe and H., Follmann, Using Lipoate enantiomers and thioredoxin to study the mechanism of the 2-oxoacid-dependent dihydrolipoate production by the 2-oxoacid dehydrogenase complexes FEBS Lett. 1995 371 167–170
N. Gustavsson, B. P. Kokke, U. Härndahl, M. Silow, U. Bechtold, Z. Poghosyan, D. Murphy, W. C. Boelens and C., Sundby, A peptide methionine sulfoxide reductase highly expressed in photosynthetic tissue in Arabidopsis thaliana can protect the chaperone-like activity of a chloroplast-localized small heat shock protein Plant J. 2002 29 545–553
B. S. Berlett and E. R., Stadtman, Protein oxidation in aging, disease, and oxidative stress J. Biol. Chem. 1997 272 20313–20316
R. Levine, J. Williams, E. R. Stadtman and E., Shacter, Carbonyl assays for determination of oxidatively modified proteins Methods Enzymol. 1994 233 346–357
S. W. Taylor, E. Fahy, J. Murray, R. A. Capaldi and S. S., Ghosh, Oxidative post-translational modification of tryptophan residues in cardiac mitochondrial proteins J. Biol. Chem. 2003 278 19587–19590
B. K. Kristensen, P. Askerlund, N. Bykova, H. Egsgaard, and I. M. Møller, Identification of oxidised mitochondrial proteins by immunoprecipitation and two-dimensional liquid chromatography-tandem mass spectrometry [MS submitted for publication]. 2004
O. V. Karpova, E. V. Kuzmin, T. E. Elthon and K. J., Newton, Differential expression of alternative oxidase genes in maize mitochondrial mutants Plant Cell 2002 14 3271–3284
L. J. Sweetlove, J. L. Heazlewood, V. Herald, R. Holtzapffel, D. A. Day, C. J. Leaver and A. H., Millar, The impact of oxidative stress on Arabidopsis mitochondria Plant J. 2002 32 891–904
J. Sakai, H. Ishikawa, S. Kojima, H. Satoh, S. Yamamoto and M., Kanaoka, Proteomic analysis of rat heart in ischemia and ischemia-reperfusion using fluorescence two-dimensional difference gel electrophoresis Proteomics 2003 3 1318–1324
F. Courtois-Verniquet and R., Douce, Lack of aconitase in glyoxysomes and peroxisomes Biochem. J. 1993 294 103–107
T. Kurahashi, A. Miyazaki, S. Suwan and M., Isobe, Extensive investigations on oxidized amino acid residues in H2O2-treated Cu,Zn-SOD protein with LC-ESI-Q-TOF-MS, MS/MS for the determination of the copper-binding site J. Am. Chem. Soc. 2001 123 9268–9278
M. Whittaker and J., Whittaker, A glutamate bridge is essential for dimer stability and metal selectivity in manganese superoxide dismutase J. Biol. Chem. 1998 273 22188–22193
F. Yamakura, H. Taka, T. Fujimura and K., Murayama, Inactivation of human manganese-superoxide dismutase by peroxynitrite is caused by exclusive nitration of tyrosine 34 to 3-nitrotyrosine J. Biol. Chem. 1998 273 14085–14089
J. R. Cherry, M. H. Lamsa, P. Schneider, J. Vind, A. Svendsen, A. Jones and A. H., Pedersen, Directed evolution of a fungal peroxidase Nature Biotechnol. 1999 17 379–384
G., Daum, Lipids of mitochondria Biochim. Biophys. Acta 1985 822 1–42
R. Bligny and R., Douce, Precise localization of cardiolipin in plant cells Biochim. Biophys. Acta 1980 617 254–263
O. Caiveau, D. Fortune, C. Cantrel, A. Zachowski and F., Moreau, Consequences of omega-6-oleate desaturase deficiency on lipid dynamics and functional properties of mitochondrial membranes of Arabidopsis thaliana J. Biol. Chem. 2001 276 5788–5794
G. Paradies, F. M. Ruggiero, G. Petrosillo and E., Quagliariello, Peroxidative damage to cardiac mitochondria: cytochrome oxidase and cardiolipin alterations FEBS Lett. 1998 424 155–158
F. Goglia and V. P., Skulachev, A function for novel uncoupling proteins: antioxidant defense of mitochondrial matrix by translocating fatty acid peroxides from the inner to the outer membrane leaflet FASEB J. 2003 17 1585–1591
J. F. Hare and R., Hodges, Turnover of mitochondrial matrix polypeptides in hepatoma monolayer cultures J. Biol. Chem. 1982 257 2950–2953
J. F. Hare and R., Hodges, Turnover of mitochondrial inner membrane-proteins in hepatoma monolayer-cultures J. Biol. Chem. 1982 257 3575–3580
M. Rep and L. A., Grivell, The role of protein degradation in mitochondrial function and biogenesis Curr. Genet. 1996 30 367–380
W. Huth, S. Rolle and I., Wunderlich, Turnover of matrix proteins in mammalian mitochondria Biochem. J. 2002 364 275–284
K. Röttgers, N. Zufall, B. Guiard and W., Voos, The ClpB homolog Hsp78 is required for the efficient degradation of proteins in the mitochondrial matrix J. Biol. Chem. 2002 277 45829–45837
Z. Adam, I. Adamska, K. Nakabayashi, O. Ostersetzer, K. Haussuhl, A. Manuell, B. Zheng, O. Vallon, S. R. Rodermel, K. Shinozaki and A. K., Clarke, Chloroplast and mitochondrial proteases in Arabidopsis. A proposed nomenclature Plant Physiol. 2001 125 1912–1918
T. Halperin, B. Zheng, H. Itzhaki, A. Clarke and Z., Adam, Plant mitochondria contain proteolytic and regulatory subunits of the ATP-dependent Clp protease Plant Mol. Biol. 2001 45 461–468
R. Sarria, A. Lyznik, C. Vallejos and S., Mackenzie, A cytoplasmic male sterility-associated mitochondrial peptide in common bean is post-translationally regulated Plant Cell 2003 10 1217–1228
M. Lindahl, C. Spetea, T. Hundal, A. Oppenheim, Z. Adam and B., Andersson, The thylakoid FtsH protease plays a role in the light-induced turnover of the photosystem II D1 protein Plant Cell 2000 12 419–431
O. Ostersetzer and Z., Adam, Light-stimulated degradation of an unassembled Rieske FeS protein by a thylakoid-bound protease: The possible role of the FstH protease Plant Cell 2003 9 957–965
I. Arnold and T., Langer, Membrane protein degradation by AAA proteases in mitochondria Biochim. Biophys. Acta-Mol. Cell Res. 2002 1592 89–96
P. Moberg Mol. Stud. Mitochondrial Targeting Pept. 2003 1–54
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Møller, I.M., Kristensen, B.K. Protein oxidation in plant mitochondria as a stress indicator. Photochem Photobiol Sci 3, 730–735 (2004). https://doi.org/10.1039/b315561g
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DOI: https://doi.org/10.1039/b315561g