Chromium(VI) interaction with plant and animal mitochondrial bioenergetics: a comparative study.
The mechanism of Cr(VI)-induced toxicity in plants and animals has been assessed for mitochondrial bioenergetics and membrane damage in turnip root and rat liver mitochondria. By using succinate as the respiratory substrate, ADP/O and respiratory control ratio (RCR) were depressed as a function of Cr(VI) concentration. State 3 and uncoupled respiration were also depressed by Cr(VI). Rat mitochondria revealed a higher sensitivity to Cr(VI), as compared to turnip mitochondria. Rat mitochondrial state 4 respiration rate triplicated in contrast to negligible stimulation of turnip state 4 respiration. Chromium(VI) inhibited the activity of the NADH-ubiquinone oxidoreductase (complex I) from rat liver mitochondria and succinate-dehydrogenases (complex II) from plant and animal mitochondria. In rat liver mitochondria, complex I was more sensitive to Cr(VI) than complex II. The activity of cytochrome c oxidase (complex IV) was not sensitive to Cr(VI). Unique for plant mitochondria, exogenous NADH uncoupled respiration was unaffected by Cr(VI), indicating that the NADH dehydrogenase of the outer leaflet of the plant inner membrane, in addition to complexes III and IV, were insensitive to Cr(VI). The ATPase activity (complex V) was stimulated in rat liver mitochondria, but inhibited in turnip root mitochondria. In both, turnip and rat mitochondria, Cr(VI) depressed mitochondrial succinate-dependent transmembrane potential (Deltapsi) and phosphorylation efficiency, but it neither affected mitochondrial membrane permeabilization to protons (H+) nor induced membrane lipid peroxidation. However, Cr(VI) induced mitochondrial membrane permeabilization to K+, an effect that was more pronounced in turnip root than in rat liver mitochondria. In conclusion, Cr(VI)-induced perturbations of mitochondrial bioenergetics compromises energy-dependent biochemical processes and, therefore, may contribute to the basal mechanism underlying its toxic effects in plant and animal cells.
Fernandes
M A S
MA
Departamento de Zoologia, Universidade de Coimbra, 3004-517 Coimbra, Portugal. mfer@ci.uc.pt
Santos
M S
MS
Alpoim
M C
MC
Madeira
V M C
VM
Vicente
J A F
JA
D000818:Animals; D029688:Brassica napus / Q000166:cytology / Q000378:metabolism*; D002274:Carcinogens, Environmental / Q000633:toxicity*; D002463:Cell Membrane Permeability / Q000187:drug effects; D019069:Cell Respiration / Q000187:drug effects; D002857:Chromium / Q000633:toxicity*; D004305:Dose-Response Relationship, Drug; D042967:Electron Transport Complex I; D004734:Energy Metabolism / Q000187:drug effects*; D066298:In Vitro Techniques; D008297:Male; D008564:Membrane Potentials / Q000187:drug effects; D008928:Mitochondria / Q000187:drug effects* / Q000201:enzymology / Q000378:metabolism*; D008930:Mitochondria, Liver / Q000187:drug effects / Q000201:enzymology / Q000378:metabolism; D008933:Mitochondrial Swelling / Q000187:drug effects; D009247:NADH, NADPH Oxidoreductases / Q000378:metabolism; D010101:Oxygen Consumption / Q000187:drug effects; D018521:Plant Physiological Phenomena / Q000187:drug effects*; D018517:Plant Roots / Q000166:cytology / Q000378:metabolism; D051381:Rats; D017208:Rats, Wistar; D013045:Species Specificity; D013385:Succinate Dehydrogenase / Q000378:metabolism; D013997:Time Factors
D002274:Carcinogens, Environmental; D002857:Chromium; C074702:chromium hexavalent ion; D013385:Succinate Dehydrogenase; D009247:NADH, NADPH Oxidoreductases; D042967:Electron Transport Complex I