Summary
We have considered the regulatory interrelationship of the plasma membrane oxidoreductase (PMOR) system and the mitochondrial respiratory capacity of human Namalwa (lymphoblastoid) cells. To this end, we made use of mitchondrially respiratory competent (ϱ+) cells and ϱ0 cells, which lack mitochondrial DNA (mtDNA) and consequently mitochondrial respiratory activity. NADH-fer-ricyanide reductase activity of the PMOR system is increased 3-fold in ϱ0 Namalwa cells compared to ϱ+ cells. It is also shown for the first time that addition of coenzyme Q10 and coenzyme Q10-ana-logues, which can rescue ϱ0 Namalwa cells in the absence of pyravate, gives rise to a further 2–3-fold increase in plasma membrane NADH-ferricyanide reductase activity. These systems were examined to determine if there exists a correlation between the regulation of the PMOR system and extracellular Superoxide radical formation as measured with the fluorescence probe L-012. No correlation was found between NADH-ferricyanide reductase activity and extracellular Superoxide radical production. PMOR function in cellular proliferation appears therefore not to involve extracellular Superoxide radical production.
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Abbreviations
- CoQ10 :
-
coenzyme Q10
- EtBr:
-
ethidium bromide
- HCO-60:
-
polyoxyethylated hydrogenated castor oil
- HEPES:
-
4-(2-hydroxyethyl)-1-piperazineethanesulfonic acid
- mtDNA:
-
mitochondrial DNA
- L-012:
-
8-amino-5-chloro-7-phenylpyrido(3,4-d)pyridazine-1,4(2H,3H)dione
- SOD:
-
Superoxide dismutase
References
Asard H, Caubergs R, Anders D, DeGreef JA (1987) Duroquinone-stimulated NADH oxidase andb type cytochromes in the plasma membrane of cauliflower and mung beans. Plant Sci 53: 109–119
Askerlund P, Larsson C (1991) NAD(P)H oxidase and peroxidase activities in purified plasma membranes from cauliflower inflorescences. Physiol Plant 71: 9–19
Bellavite P (1988) The superoxide-forming enzymatic systems of phagocytes. In: Halliwell B, Gutteridge JMC (eds) Free radicals in biology and medicine, vol 4. Pergamon, New York, pp 225–261
Brightman AO, Wang J, Miu RK, Sun IL, Barr R, Crane FL, Morré DJ (1992) A growth factor and hormone-stimulated NADH oxidase from rat liver plasma membrane. Biochim Biophys Acta 1105: 109–117
Chen JJ, Jones ME (1976) The cellular location of dihydroorotate dehydrogenase: relation to de novo biosynthesis of pyrimidines. Arch Biochem Biophys 176: 82–90
Clark MG, Partick EJ, Patten GS, Crane FL, Löw H, Grebing C (1981) Evidence for the extracellular reduction of ferricyanide by rat liver. Biochem J 200: 565–572
Crane FL, Roberts H, Linnane AW (1982) Transmembrane ferricyanide reduction by cells of the yeastSaccharomyces cerevisiae. J Bioenerg Biomembr 14: 191–205
—, Sun IL, Clark MG, Grebing C, Löw H (1985) Plasma membrane redox systems in growth and development. Biochim Biophys Acta 811: 233–264
— —, Barr R, Löw H (1991) Electron and proton transport across the plasma membrane. J Bioenerg Biomembr 23: 773–803
Desjardins P, Frost E, Morais R (1985) Ethidium bromide-induced loss of mitochondrial DNA from primary chicken embryo fibroblasts. Mol Cell Biol 5: 1163–1169
Dorseuil O, Vazquez A, Lang P, Bertoglio J, Gacon G, Leca G (1992) Inhibition of Superoxide production in B lymphocytes by Rac antisense oligonucleotides. J Biol Chem 267: 20540–20542
Goldenberg H, Crane FL, Morré DJ (1979) NADH oxidoreductase of mouse liver plasma membranes. J Biol Chem 254: 2491–2498
Hertzberg NH, Zwart R, Wolterman RA, Ruiter JPN, Wanders RJA, Bolhuis PA, van den Bogert C (1993) Differentiation and proliferation of respiration-deficient human myoblasts. Biochim Biophys Acta 1181: 63–67
King MP, Attardi G (1989) Human cells lacking mtDNA: repopulation with exogenous mitochondria by complementation. Science 246: 500–504
Lawen A, Martinus RD, McMullen GL, Nagley P, Vaillant F, Wolvetang EJ, Linnane AW (1995) The universality of bioenergetic disease: the role of mitochondrial mutation and the putative inter-relationship between mitochondria and plasma membrane NADH oxidoreductase. Mol Aspects Med (in press)
Linnane AW, Baumer A, Maxwell RJ, Preston H, Zhang C, Marzuki S (1990) Mitochondrial gene mutation: the aging process and degenerative diseases. Biochem Int 22: 1067–1076
—, Zhang C, Baumer A, Nagley P (1992) Mitochondrial DNA mutation and the aging process: bioenergy and pharmacological intervention. Mutation Res 275: 195–208
May JM, deHaen C (1979) Insulin-stimulated hydrogen peroxide formation in rat epididymal fat cells. J Biol Chem 254: 2214–2220
Martinus RD, Linnane AW, Nagley P (1993) Growth of p0 human Namalwa cells lacking oxidative phosphorylation can be sustained by redox compounds potassium ferricyanide or coenzyme q10 putatively acting through the plasma membrane oxidase. Biochem Mol Biol Int 31: 997–1005
Marzuki S, Noer AS, Lertrit P, Uttahanaphol P, Thyagarajan D, Kapsa R, Sudoyo H, Byrne E (1991) Molecular pathology of mitochondrial respiratory disorders: normal nucleotide variants of human mitochondrial genome and mtDNA lesion in MERRF encephalomyopathy. In: Sato T, DiMauro S (eds) Progress in neuropathology, vol 7. Raven, New York, pp 181–193
Møller I, Bérczi A (1986) Salicylhydroxamic acid-stimulated NADH oxidation by purified plasmalemma vesicles from wheat roots. Physiol Plant 68: 67–74
Morais R, Gregoire M, Jeanette L, Gravel D (1989) Chick embryo cells rendered respiration-deficient by chloramphenicol and ethidium bromide are auxotrophic for pyrimidines. Biochem Biophys Res Commun 94: 71–77
Morré DJ, Brightman AO (1991) NADH oxidase of plasma membranes. J Bioenerg Biomembr 23: 469–489
Nishinaka Y, Aramaki Y, Yoshida H, Masuya H, Sugawara T, Ichimori Y (1993) A sensitive chemiluminescence probe, L-012, for measuring the production of Superoxide anions by cells. Biochem Biophys Res Commun 193: 554–559
Nyormoi O, Klein RE, Adams A, Dombos L (1973) Sensitivity to EBV superinfection and IUdR inducibility of hybrid cells formed between a sensitive and a relatively resistant Burkitt lymphoma cell line. In J Cancer 12: 396–405
O'Brien PJ (1991) Molecular mechanisms of quinone cytotoxicity. Chem Biol Interact 80: 1–41
Ramasarma T, Swaroop A, MacKellar W, Crane FL (1981) Generation of hydrogen peroxide on oxidation of NADH by hepatic plasma membranes. J Bioenerg Biomembr 13: 241–253
Segal AW, Abo A (1993) The biochemical basis of the NADPH oxidase of phagocytes. Trends Biochem Sci 18: 43–47
Shibanuma M, Kuroki T, Nose K (1990) Stimulation by hydrogen peroxide of DNA synthesis, competence family gene expression and phosphorylation of a specific protein in quiescent Balb/3T3 cells. Oncogene 5: 1025–1032
Thor H, Smith MT, Hartzell P, Bellomo G, Jewell SA, Orrenius S (1982) The metabolism of menadione (2-methyl-1,4-naphtho-quinone) in isolated hepatocytes. J Biol Chem 257: 12419–12425
Vaillant F, Loveland BE, Nagley P, Linnane AW (1991) Some biochemical properties of human lymphoblastoid Namalwa cells grown anaerobically. Biochem Int 23: 571–580
Vianello A, Macri F (1990) Generation of Superoxide anion and hydrogen peroxide at the surface of plant cells. J Bioenerg Biomembr 23: 409–423
—, Zancani M, Macri F (1990) Hydrogen peroxide formation and iron ion oxidoreduction linked to NADH oxidation in radish plasmalemma vesicles. Biochim Biophys Acta 1023: 19–24
Wolvetang EJ, Johnson K, Krauer K, Ralph SJ, Linnane AW (1994) Mitochondrial respiratory chain inhibitors induce apoptosis. FEBS Lett 339: 40–44
Zhang C, Baumer A, Maxwell RJ, Linnane AW, Nagley P (1992) Multiple mitochondrial DNA deletions in an elderly human individual. FEBS Lett 297: 34–38
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Larm, J.A., Wolvetang, E.J., Vaillant, F. et al. Increase of plasma membrane oxidoreductase activity is not correlated with the production of extracellular Superoxide radicals in human Namalwa cells. Protoplasma 184, 173–180 (1995). https://doi.org/10.1007/BF01276917
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DOI: https://doi.org/10.1007/BF01276917