Summary
The present study demonstrates that the bovine cardiac sarcolemma possesses an NAD(P)H dehydrogenase activity which is able to oxidize both NADH and NAD(P)H in the presence of vanadate as an electron acceptor.
The NADH dehydrogenase activity was significantly higher than the NAD(P)H dehydrogenase activity and both of them were almost completely inhibited by superoxide dismutase and atebrin and markedly reduced by the addition of the protonophore 2,4-dinitrophenol. The incubation of the sarcolemma in the presence of 10−10, 10−9, 10−8 M methionine-enkephalin, a prevalent δ-opioid receptor agonist, or dynorphin A (1–17), a prevalent κ-receptor agonist, produced a dose-dependent increase in the NAD(P)H dehydrogenase activity, with 10−10 and 10−9 M dynorphin A (1–17) more effective than the corresponding doses of methionine-enkephalin. The preincubation of the sarcolemma in the presence of superoxide-dismutase, atebrin or 2,4-dinitrophenol strongly inhibited the opioid-stimulated dehydrogenase activity.
The stimulatory action elicited by 10−8 M methionine-enkephalin or dynorphin A (1–17) was completely antagonized by 10−8 M naloxone or Mr 1452, respectively, whilst 10−8 M naloxone exerted only a partially antagonistic action against the effect produced by 10−8 M dynorphin A (1–17), significantly more accentuated than the action of 10−8 M Mr 1452 versus the same dose of methionine-enkephalin.
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References
Aronson NN, Touster O (1974) Isolation of rat liver plasma membrane fragments in isotonic sucrose. In: Fleischer S, Packer L (eds) Method Enzymol. Vol 31, Academic Press, New York, pp 90–102
Bowen WD, Hellewell SB, Kelemen M, Huey R, Stewart D (1987) Affinity labeling of δ-opiate receptors using (D-Ala2, Leu5, Cys6) Enkephalin. J Biol Chem 262:13434–13439
Brain RD, Freeberg JA, Weiss CV, Briggs WR (1977) Blue-light induced absorbance changes in membrane fractions from corn and neurospora. Plant Physiol 59:948–952
Clô C, Muscari C, Tantini B, Pignatti C, Bernardi P, Ventura C (1985) Reduced mechanical activity of perfused rat heart following morphine or enkephalin peptides administration. Life Sci 37:1327–1333
Colbeau A, Nachbaur J, Vignais PM (1971) Enzymic characterization and lipid composition of rat liver subcellular membranes. Biochim Biophys Acta 249:462–492
Crane FL, Low H (1976) NADH oxidation in liver and fat cell plasma membranes. FEBS Lett 68:153–156
Crane FL, Goldenberg H, Morrè DJ, Low H (1979) Dehydrogenases of the plasma membranes. In: Roodyn DB (ed) Subcellular Biochemistry Vol 6, Plenum Press, New York, pp 345–399
Dhalla NS, McNamara DB, Anand MB (1976) Heart sarcolemma as a dynamic exictable membrane. In: Roy PE, Dhalla NS (eds) Recent advances in Studies on Cardiac Structure and Metabolism, The Sarcolemma, Vol 9, University Park Press, Baltimore, pp 1–19
Dhalla NS, Smith CI, Pierce GN, Elimban V, Makino N, Khatter JC (1986) Heart sarcolemma cation pumps and binding sites. In: Rupp H (ed) The regulation of heart function. Thieme Inc, New York, pp 121–136
Eldan M, Mayer AM (1972) Evidence for the activation of NADH-Cytochrome c reductase during germination of lettuce. Plant Physiol 26:67–72
Erdmann E, Krawietz W, Phillip G, Hackbarth I, Schmitz W, Scholz H, Crane FL (1979) Purified cardiac cell membranes with high Na+−K+ ATPase activity contain significant NADH-vanadate reductase activity. Nature 282:335–336
Erdmann E, Werdan K, Krawietz W, Lebuhn M, Christl S (1980) Significance of NADH-vanadateoxidoreductase of cardiac and erythrocyte cell membranes. Basic Res Cardiol 75:460–465
Gayda DP, Crane FL, Morrè DJ, Low H (1977) Hormone effects on NADH oxidizing enzymes of plasma membranes of rat liver. Proc Indiana Acad Sci 86:385–390
Gould JM, Cramer WA (1977) Relationship between oxygen-induced proton efflux and membrane energization in cells of escherichia coli. J Biol Chem 252:5875–5882
Guarnieri C, Ventura C, Georgountzos A, Muscari C, Budini R (1985) Involvement of superoxide radicals on adrenochrome formation stimulated by arachidonic acid in bovine heart sarcolemmal vescicles. Biochim Biophys Acta 838:355–360
Hughes J (1981) Peripheral opiate receptor mechanism. Trends in Pharmacol Sci 2:21–24
Ichikawa Y, Mason HS (1977) Distribution of cytochrome P-450 and related redox systems among hepatocyte membranes. In: King TE (ed) Oxidases and Related Redox Systems, Proceedings of the Second International Symposium, Vol 2, University Park Press, Baltimore, pp 605–625
Kuhl PW (1985) A redox cyclic model for the action of β-adrenoceptor agonists. Experientia 41:1118–1222
Lamers JMJ, Stinis JT (1981) An electrogenic Na+/Ca2+ antiporter in addition to the Ca2+ pump in cardiac sarcolemma. Biochim Biophys Acta 640:521–534
Liochev S, Fridovich I (1986) The vanadate-stimulated oxidation of NAD(P)H by biomembranes is a superoxide-initiated free radical reaction. Arch Biochem Biophys 250:139–145
Lord JAH, Waterfield AA, Hughes J, Kosterlitz HW (1977) Endogenous opioid peptides: multiple agonists and receptors. Nature 267:495–499
Low H, Crane FL (1976) Hormone regulated redox function in plasma membranes. FEBS Lett 68:157–159
Low H, Crane FL, Patrick EJ, Patten GS, Clark MG (1984) Properties and regulation of a transplasma membrane redox system of perfused rat heart. Biochim Biophys Acta 804:253–260
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin reagent. J Biol Chem 193:265–275
Marzullo G, Hine B (1960) Opiate receptor function may be modulated through an oxidation-reduction mechanism. Science 208:1171–1173
Mukerjee SP, Lynn WS (1977) Reduced nicotinamide adenine dinucleotide phosphate oxidase in adipocyte plasma membrane and its activation by insulin. Arch Biochem Biophys 184:69–76
Ostroy SE (1977) Rhodopsin and the visual process. Biochim Biophys Acta 463:91–125
Parrat JR (1986) Opioid receptors in the cardiovascular system. In: Verlag F (ed) Progress in Pharmacology, Vol 6, New York, pp 97–110
Paterson SJ, Robson LE, Kosterlitz HW (1983) Classification of opioid receptors. Br Med Bull 39:31–36
Prior TI, Patel V, Drummond GI (1985) Inactivation of the β-adrenergic receptor in cardiac muscle by dithiols. Can J Physiol Pharmacol 63:932–936
Reeves JP, Sutko JL (1980) Sodium-calcium exchange activity generates a current in cardiac membrane vesicles. Science 208:1461–1464
Sawynok J, Pinsky C, La Bella FS (1979) Minireview on the specificity of naloxone as an opiate antagonist. Life Sci 25:1621–1632
Smith JR, Simon EJ (1980) Selective protection of stereospecific enkephalin and opiate binding agonist inactivation by N-ethylmaleimide: evidence for two classes of opiate receptors. Proc Natl Acad Sci 77:281–284
Sottocasa GL, Kuylenstierna B, Ernester L, Bergstrand A (1967) An electron transport system associated with the outer membrane of liver mitochondria. J Cell Biol 32:415–437
Strauss WL, Venter JC (1985) A sulfhydryl group of the canine cardiac beta-adrenergic receptor observed in the absence of hormone. Life Sci 36:1699–1706
Ventura C, Muscari C, Spampinato S, Bernardi P, Caldarera CM (1987) Inhibitory action of opioid peptides on the ouabain-sensitive Na+−K+ and Ca2+-dependent ATPase activities in bovine cardiac sarcolemma. Peptides 8:709–713
Vijaya S, Crane FL, Ramasarma T (1984) A vanadate-stimulated NADH oxidase in erythrocyte membrane generates hydrogen peroxide. Mol Cell Biochem 62:175–185
Werdan K, Bauriedel G, Bozsik M, Krawietz W, Erdmann E (1980) Effects of vanadate in cultured rat heart muscle cells: vanadate transport, intracellular binding and vanadate-induced changes in beating and in active cation flux. Biochim Biophys Acta 597:364–383
Wright M, Drummond GI (1983) Inactivation of the β-adrenergic receptor in the skeletal muscle by dithiols. Biochem Pharmacol 32:509–515
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Ventura, C., Guarnieri, C., Bastagli, L. et al. Opioids stimulate sarcolemmal NAD(P)H-vanadate dehydrogenase activity. Basic Res Cardiol 83, 376–383 (1988). https://doi.org/10.1007/BF02005823
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DOI: https://doi.org/10.1007/BF02005823