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. 2005 Dec 10;27(2):139–146. doi: 10.1007/s11357-005-1632-z

Coenzyme Q-dependent functions of plasma membrane in the aging process

Plácido Navas 1,✉, José Manuel Villalba 2, Giorgio Lenaz 3
PMCID: PMC3458499  PMID: 23598620

Abstract

Coenzyme Q (Q) is reduced in plasma membrane and mitochondria by NAD(P)H-dependent reductases providing reducing equivalents to maintain both respiratory chain and antioxidant protection. Reactive oxygen species (ROS) are accumulated in the aging process originating mainly in mitochondria but also in other membranes, such as plasma membrane partially by the loss of electrons from the semiquinone. The reduction of Q by NAD(P)H-dependent reductases in plasma membrane is responsible for providing its antioxidant capacity, preventing both the lipid peroxidation chain and the activation of the ceramide-dependent apoptosis pathway. Both Q content and its reductases are decreased in plasma membrane of aging mammals. Calorie restriction, which extends mammal life span, increases the content of Q in the plasma membrane and also activates Q reductases in this membrane. Both lipid peroxidation and ceramide production are decreased in the plasma membrane in calorie-restricted animals. Plasma membrane is, then, an important cellular component to control the aging process through its concentration and redox state of Q.

Key words: aging, coenzyme Q, oxidative stress, plasma membrane, redox system

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References

  1. Arnold RS, Shi J, Murad E, Whalen AM, Sun CQ, Polavarapu R, et al. Hydrogen peroxide mediates the cell growth and transformation caused by the mitogenic oxidase Nox1. Proc Natl Acad Sci USA. 2001;98:5550–5555. doi: 10.1073/pnas.101505898. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Arroyo A, Navarro F, Navas P, Villalba JM. Ubiquinol regeneration by plasma membrane ubiquinone reductase. Protoplasma. 1998;205:107–113. doi: 10.1007/BF01279300. [DOI] [Google Scholar]
  3. Baker MA, Ly JD, Lawen A. Characterization of VDAC1 as a plasma membrane NADH-oxidoreductase. Biofactors. 2004;21:215–221. doi: 10.1002/biof.552210143. [DOI] [PubMed] [Google Scholar]
  4. Barja G. Aging in vertebrates, and the effect of caloric restriction: a mitochondrial free radical production–DNA damage mechanism? Biol Rev. 2004;79:235–251. doi: 10.1017/S1464793103006213. [DOI] [PubMed] [Google Scholar]
  5. Barroso MP, Gómez-Díaz C, Villalba JM, Burón MI, López-Lluch G, Navas P. Plasma membrane ubiquinone controls ceramide production and prevents cell death induced by serum withdrawal. J Bioenerg Biomembranes. 1997;29:259–267. doi: 10.1023/A:1022462111175. [DOI] [PubMed] [Google Scholar]
  6. Bassenge E, Sommer O, Schwemmer M, Bunger R. Antioxidant pyruvate inhibits cardiac formation of reactive oxygen species through changes in redox state. Am J Physiol Heart Circ Physiol. 2000;279:H2431–H2438. doi: 10.1152/ajpheart.2000.279.5.H2431. [DOI] [PubMed] [Google Scholar]
  7. Bentinger M, Turunen M, Zhang XX, Wan YJ, Dallner G. Involvement of retinoid X receptor alpha in coenzyme Q metabolism. J Mol Biol. 2003;326:795–803. doi: 10.1016/S0022-2836(02)01447-X. [DOI] [PubMed] [Google Scholar]
  8. Beyer RE, Segura-Aguilar J, Bernardo S, Cavazzoni M, Fato R, Fiorentini D, et al. The role of DT-diaphorase in the maintenance of the reduced antioxidant form of coenzyme Q in membrane systems. Proc Natl Acad Sci USA. 1996;93:2528–2532. doi: 10.1073/pnas.93.6.2528. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Brar SS, Corbin Z, Kennedy TP, Hemendinger R, Thornton L, Bommarius B, et al. NOX5 NAD(P)H oxidase regulates growth and apoptosis in DU 145 prostate cancer cells. Am J Physiol Cell Physiol. 2003;285:C353–C369. doi: 10.1152/ajpcell.00525.2002. [DOI] [PubMed] [Google Scholar]
  10. Bremer J, Davis EJ. Studies on the active transfer of reducing equivalents into mitochondria via the malate–aspartate shuttle. Biochim Biophys Acta. 1975;376:387–397. doi: 10.1016/0005-2728(75)90161-9. [DOI] [PubMed] [Google Scholar]
  11. Calabrese V, Scapagnini G, Ravagna A, Colombrita C, Spadaro F, Butterfield DA, et al. Increased expression of heat shock proteins in rat brain during aging: relationship with mitochondrial function and glutathione redox state. Mech Ageing Dev. 2004;125:325–335. doi: 10.1016/j.mad.2004.01.003. [DOI] [PubMed] [Google Scholar]
  12. Chatterjee S, Han H, Rollins S, Cleveland T. Molecular cloning, characterization, and expression of a novel human neutral sphingomyelinase. J Biol Chem. 1999;274:37407–37412. doi: 10.1074/jbc.274.52.37407. [DOI] [PubMed] [Google Scholar]
  13. Constantinescu A, Maguire JJ, Packer L. Interactions between ubiquinones and vitamins in membranes and cells. Mol Aspects Med. 1994;15:S57–S65. doi: 10.1016/0098-2997(94)90013-2. [DOI] [PubMed] [Google Scholar]
  14. Crane FL, Hatefi Y, Lester RL, Widmer C. Isolation of a quinone from beef heart mitochondria. Biochim Biophys Acta. 1957;25:220–221. doi: 10.1016/0006-3002(57)90457-2. [DOI] [PubMed] [Google Scholar]
  15. Crane FL, Sun IL, Clark MG, Grebing C, Löw H. Transplasma membrane redox systems in growth and development. Biochim Biophys Acta. 1985;811:233–264. doi: 10.1016/0304-4173(85)90013-8. [DOI] [PubMed] [Google Scholar]
  16. D'Aurelio M, Merlo Pich M, Catani L, Sgarbi G, Bovina C, Formiggini G, et al. Decreased Pasteur effect in platelets of aged individuals. Mech Ageing Dev. 2001;122:823–833. doi: 10.1016/S0047-6374(01)00239-1. [DOI] [PubMed] [Google Scholar]
  17. Dbaibo GS, El-Assaad W, Krikorian A, Liu B, Diab K, Idriss NZ, et al. Ceramide generation by two distinct pathways in tumor necrosis factor alpha-induced cell death. FEBS Lett. 2001;503:7–12. doi: 10.1016/S0014-5793(01)02625-4. [DOI] [PubMed] [Google Scholar]
  18. Cabo R, Cabello R, Rios M, López-Lluch G, Ingram DK, Lane MA, et al. The plasma membrane antioxidant system of liver is increased in aging rats by calorie restriction. Exp Gerontol. 2004;39:297–304. doi: 10.1016/j.exger.2003.12.003. [DOI] [PubMed] [Google Scholar]
  19. Grey AD. A mechanism proposed to explain the rise of oxidative stress during aging. J Anti-Aging Med. 1998;1:53–66. [Google Scholar]
  20. Grey AD. The reductive hotspot hypothesis: an update. Arch Biochem Biophys. 2000;373:295–301. doi: 10.1006/abbi.1999.1509. [DOI] [PubMed] [Google Scholar]
  21. Grey AD. The reductive hotspot hypothesis of mammalian aging: membrane metabolism magnifies mutant mitochondrial mischief. Eur J Biochem. 2002;269:2003–2009. doi: 10.1046/j.1432-1033.2002.02868.x. [DOI] [PubMed] [Google Scholar]
  22. Castillo-Olivares A, Nunez de Castro I, Medina MA. Dual role of plasma membrane electron transport systems in defense. Crit Rev Biochem Mol Biol. 2000;35:197–220. doi: 10.1080/10409230091169203. [DOI] [PubMed] [Google Scholar]
  23. Deleonardi G, Biondi A, D'Aurelio M, Pich MM, Stankov K, Falasca A, et al. Plasma membrane oxidoreductase activity in cultured cells in relation to mitochondrial function and oxidative stress. Biofactors. 2004;20:251–258. doi: 10.1002/biof.5520200408. [DOI] [PubMed] [Google Scholar]
  24. Drahota Z, Chowdhury SK, Floryk D, Mracek T, Wilhelm J, Rauchova H, et al. Glycerophospate-dependent hydrogen peroxide production by brown adipose tissue mitochondria and its activation by ferricyanide. J Bioenerg Biomembranes. 2002;34:105–113. doi: 10.1023/A:1015123908918. [DOI] [PubMed] [Google Scholar]
  25. Droge W. Free radicals in the physiological control of cell function. Physiol Rev. 2002;82:47–95. doi: 10.1152/physrev.00018.2001. [DOI] [PubMed] [Google Scholar]
  26. Droge W. Oxidative stress and aging. Adv Exp Med Biol. 2003;543:191–200. doi: 10.1007/978-1-4419-8997-0_14. [DOI] [PubMed] [Google Scholar]
  27. Echtay KS, Bienengraeber M, Klingenberg M. Role of intrahelical arginine residues in functional properties of uncoupling protein (UCP1) Biochemistry. 2001;40:5243–5248. doi: 10.1021/bi002130q. [DOI] [PubMed] [Google Scholar]
  28. Esposito LA, Kokoszka JE, Waymire KG, Cottrell B, MacGregor GR, Wallace DC. Mitochondrial oxidative stress in mice lacking the glutathione peroxidase-1 gene. Free Radic Biol Med. 2000;28:754–766. doi: 10.1016/S0891-5849(00)00161-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Fontaine E, Ichas F, Bernardi P. A ubiquinone-binding site regulates the mitochondrial permeability transition pore. J Biol Chem. 1998;273:25734–25740. doi: 10.1074/jbc.273.40.25734. [DOI] [PubMed] [Google Scholar]
  30. Gómez-Díaz C, Villalba JM, Pérez-Vicente R, Crane FL, Navas P. Ascorbate stabilization is stimulated in ρ°HL-60 cells by CoQ10 increase at the plasma membrane. Biochem Biophys Res Commun. 1997;234:79–81. doi: 10.1006/bbrc.1997.6582. [DOI] [PubMed] [Google Scholar]
  31. Hannun YA. Functions of ceramide in coordinating cellular responses to stress. Science. 1996;274:1855–1859. doi: 10.1126/science.274.5294.1855. [DOI] [PubMed] [Google Scholar]
  32. Jayadev S, Liu B, Bielawska AE, Lee JY, Nazaire F, Pushkareva MY, et al. Role for ceramide in cell cycle arrest. J Biol Chem. 1995;270:2047–2052. doi: 10.1074/jbc.270.28.16677. [DOI] [PubMed] [Google Scholar]
  33. Kagan VE, Tyurina YY. Recycling and redox cycling of phenolic antioxidants. Ann NY Acad Sci. 1998;20:425–434. doi: 10.1111/j.1749-6632.1998.tb09921.x. [DOI] [PubMed] [Google Scholar]
  34. Kagan VE, Serbinova EA, Packer L. Antioxidant effects of ubiquinones in microsomes and mitochondria are mediated by tocopherol recycling. Biochem Biophys Res Commun. 1990;169:851–857. doi: 10.1016/0006-291X(90)91971-T. [DOI] [PubMed] [Google Scholar]
  35. Kagan VE, Arroyo A, Tyurin VA, Tyurina YY, Villalba JM, Navas P. Plasma membrane NADH-coenzyme Q0 reductase generates semiquinone radicals and recycles vitamin E homologue in a superoxide-dependent reaction. FEBS Lett. 1998;428:43–46. doi: 10.1016/S0014-5793(98)00482-7. [DOI] [PubMed] [Google Scholar]
  36. Kawamukai M. Recent advance of the biosynthesis and the function of ubiquinone. Seikagaku. 1998;70:1344–1349. [PubMed] [Google Scholar]
  37. King MP, Attardi G. Human cells lacking mtDNA: repopulation with exogenous mitochondria by complementation. Science. 1989;246:500–503. doi: 10.1126/science.2814477. [DOI] [PubMed] [Google Scholar]
  38. Kishi T, Morre DM, Morre DJ. The plasma membrane NADH oxidase of HeLa cells has hydroquinone oxidase activity. Biochim Biophys Acta. 1999;1412:66–77. doi: 10.1016/S0005-2728(99)00049-3. [DOI] [PubMed] [Google Scholar]
  39. Kudin AP, Bimpong-Buta NY-B, Vielhaber S, Elger CE, Kunz WS. Characterization of superoxide-producing sites in isolated brain mitochondria. J Biol Chem. 2004;279:4127–4135. doi: 10.1074/jbc.M310341200. [DOI] [PubMed] [Google Scholar]
  40. Kushnareva Y, Murphy AN, Andreyev A. Complex I-mediated reactive oxygen species generation: modulation by cytochrome c and NAD(P)+ oxidation–reduction state. Biochem J. 2002;368:545–553. doi: 10.1042/BJ20021121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Larm JA, Vaillant F, Linnane AW, Lawen A. Up-regulation of the plasma membrane oxidoreductase as a prerequisite for the viability of human Namalwa ρ0 cells. J Biol Chem. 1994;269:30097–30100. [PubMed] [Google Scholar]
  42. Lass A, Agarwal S, Sohal RS. Mitochondrial ubiquinone homologues, superoxide radical generation, and longevity in different mammalian species. J Biol Chem. 1997;272:19199–19204. doi: 10.1074/jbc.272.31.19199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Lenaz G. Role of mitochondria in oxidative stress and ageing. Biochim Biophys Acta. 1998;1366:53–67. doi: 10.1016/S0005-2728(98)00120-0. [DOI] [PubMed] [Google Scholar]
  44. Lenaz G. The mitochondrial production of reactive oxygen species: mechanisms and implications in human pathology. IUBMB Life. 2001;52:159–164. doi: 10.1080/15216540152845957. [DOI] [PubMed] [Google Scholar]
  45. Lenaz G, Cavazzoni M, Genova ML, D'Aurelio M, Pich MM, Pallotti F, et al. Oxidative stress, antioxidant defences and aging. Biofactors. 1998;8:195–204. doi: 10.1002/biof.5520080305. [DOI] [PubMed] [Google Scholar]
  46. Lenaz G, Paolucci U, Fato R, D'Aurelio M, Parenti Castelli G, Sgarbi G, et al. Enhanced activity of the plasma membrane oxidoreductase in circulating lymphocytes from insulin-dependent diabetes mellitus patients. Biochem Biophys Res Commun. 2002;290:1589–1592. doi: 10.1006/bbrc.2002.6392. [DOI] [PubMed] [Google Scholar]
  47. Liebler DC. The role of metabolism in the antioxidant function of vitamin E. Crit Rev Toxicol. 1993;23:147–169. doi: 10.3109/10408449309117115. [DOI] [PubMed] [Google Scholar]
  48. Lightle SA, Oakley JI, Nikolova-Karakashian MN. Activation of sphingolipid turnover and chronic generation of ceramide and sphingosine in liver during aging. Mech Ageing Dev. 2000;120:111–125. doi: 10.1016/S0047-6374(00)00191-3. [DOI] [PubMed] [Google Scholar]
  49. Lind C, Cadenas E, Hochstein P, Ernster L. DT-diaphorase: purification, properties, and function. Methods Enzymol. 1990;186:287–301. doi: 10.1016/0076-6879(90)86122-c. [DOI] [PubMed] [Google Scholar]
  50. Linnane AW, Marzuki S, Ozawa T, Tanaka M. Mitochondrial DNA mutations as an important contributor to ageing and degenerative diseases. Lancet. 1989;7:642–645. doi: 10.1016/S0140-6736(89)92145-4. [DOI] [PubMed] [Google Scholar]
  51. Liu B, Obeid LM, Hannun YA. Sphingomyelinases in cell regulation. Semin Cell Dev Biol. 1997;8:311–322. doi: 10.1006/scdb.1997.0153. [DOI] [PubMed] [Google Scholar]
  52. Lopez-Lluch G, Barroso MP, Martin SF, Fernandez-Ayala DJM, Gomez-Diaz C, Villalba JM, et al. Role of plasma membrane coenzyme Q on the regulation of apoptosis. Biofactors. 1999;9:171–177. doi: 10.1002/biof.5520090212. [DOI] [PubMed] [Google Scholar]
  53. Macho A, Blázquez MV, Navas P, Muñoz E. Induction of apoptosis by vallinoid compounds is independent of Jun kinase and AP-1. Cell Growth Diff. 1998;9:277–286. [PubMed] [Google Scholar]
  54. Macho A, Calzado MA, Muñoz-Blanco J, Gómez-Díaz C, Gajate C, Mollinedo F, et al. Selective induction of apoptosis by capsaicin in transformed cells: the role of reactive oxygen species and calcium. Cell Death Differ. 1999;6:155–165. doi: 10.1038/sj.cdd.4400465. [DOI] [PubMed] [Google Scholar]
  55. Mahadev K, Motoshima H, Wu X, Ruddy JM, Arnold RS, Cheng G, et al. The NAD(P)H oxidase homolog Nox4 modulates insulin-stimulated generation of H2O2 and plays an integral role in insulin signal transduction. Mol Cell Biol. 2004;24:1844–1854. doi: 10.1128/MCB.24.5.1844-1854.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Malik SG, Vaillant F, Lawen A. Plasma membrane NADH-oxidoreductase in cells carrying mitochondrial DNA G11778A mutation and in cells devoid of mitochondrial DNA (rho0) Biofactors. 2004;20:189–198. doi: 10.1002/biof.5520200402. [DOI] [PubMed] [Google Scholar]
  57. Martín SF, Navarro F, Forthoffer N, Navas P, Villalba JM. Neutral magnesium-dependent sphingomyelinase from liver plasma membrane: purificación and inhibition by ubiquinol. J Bioenerg Biomembranes. 2001;33:143–153. doi: 10.1023/A:1010704715979. [DOI] [PubMed] [Google Scholar]
  58. Martin SF, Gomez-Diaz C, Navas P, Villalba JM. Ubiquinol inhibition of neutral sphingomyelinase in liver plasma membrane: specific inhibition of the Mg(2+)-dependent enzyme and role of isoprenoid chain. Biochem Biophys Res Commun. 2002;297:581–586. doi: 10.1016/S0006-291X(02)02222-2. [DOI] [PubMed] [Google Scholar]
  59. Martin-Romero FJ, Garcia-Martin E, Gutierrez-Merino C. Inhibition of oxidative stress produced by plasma membrane NADH oxidase delays low-potassium-induced apoptosis of cerebellar granule cells. J Neurochem. 2002;82:705–715. doi: 10.1046/j.1471-4159.2002.01023.x. [DOI] [PubMed] [Google Scholar]
  60. Masoro EJ. Dietary restriction: current status. Aging (Milano) 2001;13:261–262. doi: 10.1007/BF03353421. [DOI] [PubMed] [Google Scholar]
  61. Melov S, Coskun P, Patel M, Tuinstra R, Cottrell B, Jun AS, et al. Mitochondrial disease in superoxide dismutase 2 mutant mice. Proc Natl Acad Sci USA. 1999;96:846–851. doi: 10.1073/pnas.96.3.846. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Miquel J, Economos AC, Fleming J, Johnson JE., Jr Mitochondrial role in cell aging. Exp Gerontol. 1980;15:575–591. doi: 10.1016/0531-5565(80)90010-8. [DOI] [PubMed] [Google Scholar]
  63. Mizushima N, Koike R, Kohsaka H, Kushi Y, Handa S, Yagita H, et al. Ceramide induces apoptosis via CPP32 activation. FEBS Lett. 1996;395:267–271. doi: 10.1016/0014-5793(96)01050-2. [DOI] [PubMed] [Google Scholar]
  64. Morré DJ, Morré DM. Plasma membrane electron transport. A metabolic process deserving of renewed interest. Biofactors. 2004;20:183–187. doi: 10.1002/biof.5520200401. [DOI] [PubMed] [Google Scholar]
  65. Morré DJ, Pogue R, Morré DM. A multifunctional hydroquinone oxidase of the external cell surface and sera. Biofactors. 1999;9:179–187. doi: 10.1002/biof.5520090213. [DOI] [PubMed] [Google Scholar]
  66. Morré DM, Lenaz G, Morré DJ. Surface oxidase and oxidative stress propagation in aging. J Exp Biol. 2000;203:1513–1521. doi: 10.1242/jeb.203.10.1513. [DOI] [PubMed] [Google Scholar]
  67. Navarro F, Villalba JM, Crane FL, Mackellar WC, Navas P. A phospholipid-dependent NADH-coenzyme Q reductase from liver plasma membrane. Biochem Biophys Res Commun. 1995;212:138–143. doi: 10.1006/bbrc.1995.1947. [DOI] [PubMed] [Google Scholar]
  68. Navarro F, Navas P, Burgess JR, Bello RI, Cabo R, Arroyo A, et al. Vitamin E and selenium deficiency induces expression of the ubiquinone-dependent antioxidant system at the plasma membrane. FASEB J. 1998;12:1665–1673. doi: 10.1096/fasebj.12.15.1665. [DOI] [PubMed] [Google Scholar]
  69. Obeid LM, Linardic CM, Karolak LA, Hannun YA. Programmed cell death induced by ceramide. Science. 1993;259:1769–1771. doi: 10.1126/science.8456305. [DOI] [PubMed] [Google Scholar]
  70. Olsson U, Lundgren E, Segura-Aguilar J, Messing-Eriksson A, Andersson K, Becedas L, et al. Effects of selenium deficiency on xenobiotic-metabolizing and other enzymes in rat liver. Int J Vitam Nutr Res. 1993;63:31–37. [PubMed] [Google Scholar]
  71. Petkova DH, Momchilova-Pankova AB, Markovska TT, Koumanov KS. Age-related changes in rat liver plasma membrane sphingomyelinase activity. Exp Gerontol. 1988;23:19–24. doi: 10.1016/0531-5565(88)90016-2. [DOI] [PubMed] [Google Scholar]
  72. Prata C, Maraldi T, Zambonin L, Fiorentini D, Hakim G, Landi L. ROS production and Glut1 activity in two human megakaryocytic cell lines. Biofactors. 2004;20:223–233. doi: 10.1002/biof.5520200406. [DOI] [PubMed] [Google Scholar]
  73. Raff MC, Barres BA, Burne JF, Coles HS, Ishizaki Y, Jacobson MD. Programmed cell death and the control of the survival: lessons from the nervous system. Science. 1993;262:695–700. doi: 10.1126/science.8235590. [DOI] [PubMed] [Google Scholar]
  74. Rauchova H, Drahota Z, Lenaz G. Function of coenzyme Q in the cell: some biochemical and physiological properties. Physiol Res. 1995;44:209–216. [PubMed] [Google Scholar]
  75. Rushmore TH, Morton MR, Pickett CB. The antioxidant responsive element. Activation by oxidative stress and identification of the DNA consensus sequence required for functional activity. J Biol Chem. 1991;266:11632–11639. [PubMed] [Google Scholar]
  76. Saamhan-Arias AK, Martin-Romero FJ, Gutierrez-Merino C. Kaempferol blocks oxidative stress in cerebellar granule cells and reveals a key role for reactive oxygen species production at the plasma membrane in the commitment to apoptosis. Free Radic Biol Med. 2004;37:48–61. doi: 10.1016/j.freeradbiomed.2004.04.002. [DOI] [PubMed] [Google Scholar]
  77. Santos-Ocaña C, Villalba JM, Córdoba F, Padilla S, Crane FL, Clarke CF, et al. Genetic evidence for coenzyme Q requirement in plasma membrane electron transport. J Bioenerg Biomembranes. 1998;30:465–475. doi: 10.1023/A:1020542230308. [DOI] [PubMed] [Google Scholar]
  78. Sauer H, Gunther J, Hescheler J, Wartenberg M. Thalidomide inhibits angiogenesis in embryoid bodies by the generation of hydroxyl radicals. Am J Pathol. 2000;156:151–158. doi: 10.1016/S0002-9440(10)64714-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Sauer H, Wartenberg M, Hescheler J. Reactive oxygen species as intracellular messengers during cell growth and differentiation. Cell Physiol Biochem. 2001;11:173–186. doi: 10.1159/000047804. [DOI] [PubMed] [Google Scholar]
  80. Sharma MK, Buettner GR. Interaction of vitamin C and vitamin E during free radical stress in plasma: an ESR study. Free Radic Biol Med. 1993;14:649–653. doi: 10.1016/0891-5849(93)90146-L. [DOI] [PubMed] [Google Scholar]
  81. Shiose A, Kuroda J, Tsuruya K, Hirai M, Hirakata H, Naito S, et al. A novel superoxide-producing NAD(P)H oxidase in kidney. J Biol Chem. 2001;276:1417–1423. doi: 10.1074/jbc.M007597200. [DOI] [PubMed] [Google Scholar]
  82. Spence MW, Burgess JK. Acid and neutral sphingomyelinases of rat brain. Activity in developing brain and regional distribution in adult brain. J Neurochem. 1978;30:917–919. doi: 10.1111/j.1471-4159.1978.tb10804.x. [DOI] [PubMed] [Google Scholar]
  83. Stoyanovsky DA, Osipov AN, Quinn PJ, Kagan VE. Ubiquinone-dependent recycling of vitamin E radicals by superoxide. Arch Biochem Biophys. 1995;323:343–351. doi: 10.1006/abbi.1995.9955. [DOI] [PubMed] [Google Scholar]
  84. Sun IL, Sun EE, Crane FL, Morré DJ, Lindgren A, Löw H. Requirement for coenzyme Q in plasma membrane electron transport. Proc Natl Acad Sci USA. 1992;89:11126–11130. doi: 10.1073/pnas.89.23.11126. [DOI] [PMC free article] [PubMed] [Google Scholar]
  85. Takahashi T, Shitashige M, Okamoto T, Kishi T, Goshima K. A novel ubiquinone reductase activity in rat cytosol. FEBS Lett. 1992;314:331–334. doi: 10.1016/0014-5793(92)81499-C. [DOI] [PubMed] [Google Scholar]
  86. Takahashi T, Yamaguchi T, Shitashige M, Okamoto T, Kishi T. Reduction of ubiquinone in membrane lipids by rat liver cytosol and its involvement in the cellular defence system against lipid peroxidation. Biochem J. 1995;309:883–890. doi: 10.1042/bj3090883. [DOI] [PMC free article] [PubMed] [Google Scholar]
  87. Thannickal VJ, Day RM, Klinz SG, Bastien MC, Larios JM, Fanburg BL. Ras-dependent and -independent regulation of reactive oxygen species by mitogenic growth factors and TGF-beta1. FASEB J. 2000;14:1741–1748. doi: 10.1096/fj.99-0878com. [DOI] [PubMed] [Google Scholar]
  88. Turunen M, Olsson J, Dallner G. Metabolism and function of coenzyme Q. Biochim Biophys Acta. 2004;1660:171–199. doi: 10.1016/j.bbamem.2003.11.012. [DOI] [PubMed] [Google Scholar]
  89. Vaquero EC, Edderkaoui M, Pandol SJ, Gukovsky I, Gukovskaya AS. Reactive oxygen species produced by NAD(P)H oxidase inhibit apoptosis in pancreatic cancer cells. J Biol Chem. 2004;279:34643–34654. doi: 10.1074/jbc.M400078200. [DOI] [PubMed] [Google Scholar]
  90. Villalba JM, Navarro F, Córdoba F, Serrano A, Arroyo A, Crane FL, et al. Coenzyme Q reductase from liver plasma membrane: purification and role in trans-plasma-membrane electron transport. Proc Natl Acad Sci USA. 1995;92:4887–4891. doi: 10.1073/pnas.92.11.4887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  91. Villalba JM, Crane FL, Navas P. In: Plasma Membrane Redox Systems and Their Role in Biological Stress and Disease. Asard H, Bërczi A, Caubergs RJ, editors. Dordrecht: Kluwer; 1998. pp. 247–265. [Google Scholar]
  92. Wolvetang EJ, Larm JA, Moutsoulas P, Lawen A. Apoptosis induced by inhibitors of the plasma membrane NADH-oxidase involves Bcl-2 and calcineurin. Cell Growth Differ. 1996;7:1315–1325. [PubMed] [Google Scholar]
  93. Yang S, Madyastha P, Bingel S, Ries W, Key L. A new superoxide-generating oxidase in murine osteoclasts. J Biol Chem. 2001;276:5452–5458. doi: 10.1074/jbc.M001004200. [DOI] [PubMed] [Google Scholar]

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