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Plasma membrane redox and regulation of cell growth

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Summary

Gene expression can be activated by external oxidants which are reduced at the cell surface by plasma membrane electron transport. The signals generated in response to the plasma membrane electron transport include activation of proton release, internal calcium changes, and change in reductant/oxidant ratio in the cytosol. H2O2 generated in response to ligands which bind to plasma membrane receptors can also activate protein tyrosine kinases and gene expression. Inhibition of oxygen radical generation at the cell surface in response to the mitogen, phorbol myristate acetate by retinoic acid is consistent with a role for the plasma membrane electron transport as the source for H2O2 in Balb 3T3 cells. Agents which affect the binding of coenzyme Q to redox sites in the plasma membrane electron transport may increase formation of semiquinone radicals in the membrane which can be a source of oxygen radicals and H2O2. The generation of H2O2 by transformed cells indicates that oncogene product expression in the plasma membrane may also increase quinone-based oxygen radical generation.

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References

  • Alcain FJ, Löw H, Crane FL (1994) Ion interactions on the plasma membrane redox system. In: Abstracts of the Conference on Molecular Biology and Function of Plasma Membrane Redox, Cordoba, Spain, p 5

    Google Scholar 

  • Allen JF, Bennett J, Steinback KE, Arntzen CJ (1981) Chloroplast protein phosphorylation couples plastoquinone redox state to distribution of excitation energy between photosystems. Nature 291: 1–5

    Google Scholar 

  • Apostol I, Heinstein PF, Low PF (1989) Rapid stimulation of an oxidative burst during signal transduction. Plant Physiol 90: 109–116

    Google Scholar 

  • Bienfait HF (1988) Mechanisms in iron efficiency reactions of higher plants. J Plant Nutr 11: 605–629

    Google Scholar 

  • Boveris A (1977) Mitochondrial production of superoxide radical and hydrogen peroxide. Adv Exp Biol Med 78: 67–82

    Google Scholar 

  • Carrasco-Luna J, Calatayud A, Gonzáles-Darós F, del Valle-Tascón S (1993) Hexacyanoferrate (III) stimulation of elongation in coleoptile segments fromZea mays L. Plant Physiol 102: S 169

    Google Scholar 

  • Cerutti P, Krupitza G, Larsson R, Muehlematter D, Crawford D, Amstad P (1988) Physiological and pathological effects of oxidants in mouse cells. Ann NY Acad Sci 551: 75–81

    Google Scholar 

  • Clark MG, Partick EJ, Crane FL (1982) Properties and regulation of a trans-plasma membrane redox system in rat liver. Biochem J 204: 795–801

    Google Scholar 

  • Clark RA (1990) The human neutrophil respiratory burst oxidase. J Infect Dis 161: 1140–1147

    Google Scholar 

  • Cook SJ, McCormick F (1993) Inhibition by cAMP of ras-dependent activation ofraf. Science 262: 1069–1072

    Google Scholar 

  • Crane FL, Morré DJ, Löw H (eds) (1988) Plasma membrane oxidoreductases in control of animal and plant growth. Plenum, New York

    Google Scholar 

  • —, Löw H, Sun IL, Morré DJ, Faulk WP (1990 a) Interaction between oxidoreductase, transferrin receptor and channels in the plasma membrane. In: Sara VR, Hall K, Löw H (eds) Growth factors: from genes to clinical applications. Raven, New York, pp 129–139

    Google Scholar 

  • —, Morré DJ, Löw H (eds) (1990 b) Oxidoreduction at the plasma membrane: relation to growth and transport. CRC Press, Boca Raton

    Google Scholar 

  • —, Sun IL, Sun EE (1993) The essential functions of coenzyme Q. J Clin Invest 71: S55-S59

    Google Scholar 

  • Crowe RA, Taparowsky EJ, Crane FL (1993)Ha ras stimulates the transplasma membrane oxidoreductase of C3H 10T1/2 cells. Biochem Biophys Res Commun 196: 844–850

    Google Scholar 

  • Egan SE, Weinberg RA (1993) The pathway to signal achievement. Nature 365: 781–783

    Google Scholar 

  • Ellem KAO, Kay GF, Dunstan AJ, Stenzel DJ (1988) Redox agents which modulate the growth of melanoma cells. In: Crane FL, Morré DJ, Löw H (eds) Plasma membrane oxidoreductases in control of animal and plant growth. Plenum, New York, pp 17–26

    Google Scholar 

  • Fuhrmann GF, Fehlan R, Schneider HS, Knauf PA (1989) The effect of ferricyanide with iodoacetate in Ca-free solution on passive cation permeability in human red cells. Biochim Biophys Acta 983: 179–185

    Google Scholar 

  • Gonzalez-Reyes JA, Hidalgo A, Caler JA, Palos R, Navas P (1994) Nutrient uptake changes in ascorbate free radical-stimulated onion roots. Plant Physiol 104: 271–276

    Google Scholar 

  • Guy G, Cairns J, Ng SB, Tan YH (1993) Inactivation of a redox-sensitive protein phosphatase during the early events of tumor necrosis factor/interleukin-1 signal transduction. J Biol Chem 268: 2141–2148

    Google Scholar 

  • Harrison ML, Rathinavelu P, Arese P, Geahlen RL, Low PS (1991) Role of band 3 tyrosine phosphorylation in the regulation of erythrocyte glycolysis. J Biol Chem 266: 4106–4111

    Google Scholar 

  • Hecht D, Zink Y (1992) Inhibition of protein tyrosine phosphatase by hydrogen peroxide. Biochem Biophys Res Commun 188: 773–779

    Google Scholar 

  • Iuchi S, Lin ECC (1991) Adaption ofE. coli to respiratory conditions: regulation of gene expression. Cell 66: 5–7

    Google Scholar 

  • Kay GF, Ellem KAO (1986) Non-heme complexes of Fe III stimulate cell attachment and growth by a mechanism different from that of serum, 2-oxocarboxylates, and haemoproteins. J Gen Physiol 126: 275–282

    Google Scholar 

  • Kim C-P (1993) NADH ferricyanide reductase of rat liver and HeLa cell plasma membrane: a novel target for antitumor agents. PhD thesis, Purdue University, West Lafayette, Indiana

    Google Scholar 

  • Lesuisse E, Labbe P (1992) Iron reduction and trans-plasma membrane electron transfer in the yeastSaccharomyces cerevisiae. Plant Physiol 100: 769–777

    Google Scholar 

  • Löw H, Crane FL, Partick EJ, Clark MG (1985) α-Adrenergic stimulation of trans-sarcolemma electron efflux in perfused rat heart: possible regulation of Ca++ channels by a sarcolemma redox system. Biochim Biophys Acta 844: 142–148

    Google Scholar 

  • Luthen H, Böttger M (1993) Induction of elongation in maize coleoptile by hexachloroiridate and its interrelation with auxin and fusucoccin action. Physiol Plant 89: 77–86

    Google Scholar 

  • McCormick F (1993) How receptors turnras on. Nature 363: 15–16

    Google Scholar 

  • Meier B, Radeke HH, Selle S, Younes M, Sies H, Resch K, Hubermehl GG (1989) Human fibroblasts release reactive oxygen species in response to interleukin-1 or tumor necrosis factor α. Biochem J 263: 539–545

    Google Scholar 

  • Morré DJ, Brightman AO (1991) NADH oxidase of plasma membranes. J Bioenerg Biomembr 23: 469–489

    Google Scholar 

  • —, Davidson M, Geilen C, Lawrence J, Flesher G, Crowe R, Crane FL (1993) NADH oxidase activity of rat liver plasma membrane activated by guanine nucleotides. Biochem J 292: 647–653

    Google Scholar 

  • Navas P, Sun IL, Morré DJ, Crane FL (1986) Decrease of NADH in HeLa cells in the presence of transferrin or ferricyanide. Biochem Biophys Res Commun 135: 110–115

    Google Scholar 

  • Olsen TS, Lane MD (1989) A common mechanism for post-translational activation of plasma membrane receptors. FASEB J 3: 1618–1624

    Google Scholar 

  • Palumbo EJ, Sweatt JD, Chen S-J, Klann E (1992) Oxidation-induced persistent activation of protein kinase C in hippocampal homogenates. Biochem Biophys Res Commun 187: 1439–1445

    Google Scholar 

  • Ramasarma T, Swaroop A, MacKellar W, Crane FL (1981) Generation of hydrogen peroxide by hepatic plasma membranes. J Bioenerg Biomembr 3: 241–253

    Google Scholar 

  • Schieven GL, Kirihara JM, Burg DL, Geahlin RL, Ledbetter JA (1993) P72syk tyrosine kinase is activated by oxidizing conditions that induce lymphocyte tyrosine phosphorylation and Ca++ signals. J Biol Chem 268: 16688–16692

    Google Scholar 

  • Schreck R, Rieber P, Bauerle PA (1991) Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-KB transcription factor and HIV-1. EMBO J 10: 2247–2258

    Google Scholar 

  • Shibanuma M, Kurocki J, Nose K (1990) Stimulation by H2O2 of DNA synthesis, competence family gene expression and phosphorylation of a specific protein in quiescent Balb 3T3 cells. Oncogene 5: 1025–1032

    Google Scholar 

  • Stirpe F, Higgins T, Tazzari PL, Rozengurt E (1991) Stimulation by xanthine oxidase of 3T3 swiss fibroblasts and human lymphocytes. Exp Cell Res 192: 635–638

    Google Scholar 

  • Sun EE, Sun IL, Crane FL (1994) The mechanism of retinoic acid mediated effects on cell growth and differentiation. Proc Indiana Acad Sci 8: 133–140

    Google Scholar 

  • Sun IL, Sun EE, Crane FL, Morré DJ, Lindgren A, Löw H (1992) A requirement for coenzyme Q in plasma membrane electron transport. Proc Natl Acad Sci USA 89: 11112–11130

    Google Scholar 

  • Szatrowski TP, Nathan CF (1991) Production of large amounts of hydrogen peroxide by human tumor cells. Cancer Res 51: 794

    Google Scholar 

  • Technikova-Dubrova Z, Sardanelli AM, Stanca MR (1993) Phosphorylation of mitochondrial proteins in bovine heart. In: Abstracts of the 2nd IUBMB Conference on Biochemistry of Cell Membranes, Bari, Italy, p 74

    Google Scholar 

  • Thorstensen K, Romslo I (1990) Role of transferrin in the mechanism of cellular iron uptake. Biochem J 271: 1–10

    Google Scholar 

  • Toole-Simms W (1988) Regulation of proton release from HeLa cells by ferric reductase. PhD thesis, Purdue University, West Lafayette, Indiana

    Google Scholar 

  • —, Sun IL, Faulk WP, Löw H, Lindgren A, Crane FL, Morré DJ (1991) Inhibition of transplasma membrane electron transport by monoclonal antibodies to the transferrin receptor. Biochem Biophys Res Commun 176: 1437–1442

    Google Scholar 

  • Wenner CE, Cutry AF (1990) The stimulation of cell growth by extracellular oxidants. In: Crane FL, Morré DJ, Low H (eds) Oxidation reduction at the plasma membrane: relation to growth and transport, vol 1. CRC Press, Boca Raton, pp 131–139

    Google Scholar 

  • White S, Taetle R, Seligman PA, Rutherford M, Trowbridge IS (1990) Combinations of antitransferrin receptor monoclonal antibodies inhibit tumor cell growth in vitro and in vivo: evidence for synergistic antiproliferative effects. Cancer Res 50: 6295–6301

    Google Scholar 

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Authors and Affiliations

  1. Department of Biological Sciences, Purdue University, 47907-1392, West Lafayette, IN, USA

    F. L. Crane, I. L. Sun, E. E. Sun & R. A. Crowe

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  1. F. L. Crane
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  2. I. L. Sun
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  3. E. E. Sun
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  4. R. A. Crowe
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Crane, F.L., Sun, I.L., Sun, E.E. et al. Plasma membrane redox and regulation of cell growth. Protoplasma 184, 3–7 (1995). https://doi.org/10.1007/BF01276894

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  • DOI: https://doi.org/10.1007/BF01276894

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