Skip to main content
SpringerLink
Log in

Control of mitochondrial membrane potential and ROS formation by reversible phosphorylation of cytochrome c oxidase

  • Chapter
Oxygen/Nitrogen Radicals: Cell Injury and Disease

Part of the book series: Developments in Molecular and Cellular Biochemistry ((DMCB,volume 37))

Abstract

Phosphorylation of isolated cytochrome c oxidase from bovine kidney and heart, and of the reconstituted heart enzyme, with protein kinase A, cAMP and ATP turns on the allosteric ATP-inhibition at high ATP/ADP ratios. Also incubation of isolated bovine liver mitochondria only with cAMP and ATP turns on, and subsequent incubation with Ca2+ turns off the allosteric ATP-inhibition of cytochrome c oxidase. In the bovine heart enzyme occur only three consensus sequences for cAMP-dependent phosphorylation (in subunits I, III and Vb). The evolutionary conservation of RRYS441at the cytosolic side of subunit I, together with the above results, suggest that phosphorylation of Ser441turns on the allosteric ATP-inhibition of cytochrome c oxidase. The results support the `molecular-physiological hypothesis’ [29], which proposes a low mitochondrial membrane potential through the allosteric ATP-inhibition. A hormone-or agonist-stimulated increase of cellular [Ca2+] is suggested to activate a mitochondrial protein phosphatase which dephosphorylates cytochrome c oxidase, turns off the allosteric ATP-inhibition and results in increase of mitochondrial membrane potential and ROS formation. (Mol Cell Biochem 234/235: 63–70, 2002)

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Chance B, Sies H, Boveris A: Hydroperoxide metabolism in mammalian organs. Physiol Rev 59: 527–605, 1979

    PubMed  CAS  Google Scholar 

  2. Boveris A: Determination of the production of superoxide radicals and hydrogen peroxide in mitochondria. Meth Enzymol 105: 429–435, 1984

    Article  PubMed  CAS  Google Scholar 

  3. Turrens JF: Superoxide production by the mitochondrial respiratory chain. Biosci Rep 17: 3–8, 1997

    Article  PubMed  CAS  Google Scholar 

  4. McLennan HR, Degli Eposti M: The contribution of mitochondrial respiratory complexes to the production of reactive oxygen species. J Bioenerg Biomembr 32: 153–162, 2000

    Article  PubMed  CAS  Google Scholar 

  5. Hansford RG, Hogue BA, Mildaziene V: Dependence of H2O2formation by rat heart mitochondria on substrate availability and donor age. J Bioenerg Biomembr 29: 89–95, 1997

    Article  PubMed  CAS  Google Scholar 

  6. Négre-Salvayre A, Hirtz C, Carrera G, Cazenave R, Troly M, Salvayre R, Penicoud L, Casteilla L: A role for uncoupling protein-2 as a regulator of mitochondrial hydrogen peroxide generation. FASEB J 11: 809–815, 1997

    PubMed  Google Scholar 

  7. Liu SS: Generating, partitioning, targeting and functioning of superoxide in mitochondria. Biosci Rep 17: 259–272, 1997

    Article  PubMed  CAS  Google Scholar 

  8. Liu SS: Cooperation of a ‘reactive oxygen cycle’ with the Q cycle and the proton cycle in the respiratory chain - superoxide generating and cycling mechanism in mitochondria. J Bioenerg Biomembr 31: 367–376, 1999

    Article  PubMed  CAS  Google Scholar 

  9. Korshunov SS, Skulachev VP, StarkovAA: High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett 416: 15–18, 1997

    Article  PubMed  CAS  Google Scholar 

  10. Papa S, Guerrieri F, Capitanio, N: A possible role of slips in cytochrome c oxidase in the antioxygen defense system of the cell. Biosci Rep 17: 23–31, 1997

    Article  PubMed  CAS  Google Scholar 

  11. Skulachev VP: Uncoupling: New approaches to an old problem of bioenergetics. Biochim Biophys Acta 1363: 100–124, 1998

    Article  PubMed  CAS  Google Scholar 

  12. Dugan LL, Sensi SL, Canzoniero LM, Handran SM, Lin TS, Goldberg MP, Choi DW: Mitochondrial production of reactive oxygen species in corticol neurons following exposure to N-methyl-D-aspartate. J Neurosci 15: 6377–6388, 1995

    PubMed  CAS  Google Scholar 

  13. Reynolds IJ, Hastings TG: Glutamate induces the production of reactive oxygen species in cultured forebrain neurons following NMDA receptor activation. J Neurosci 15: 3318–3327, 1995

    PubMed  CAS  Google Scholar 

  14. Bindokas VP, Jordan J, Lee CC, Miller RJ: Superoxide production in rat hippocampal neurons: Selective imaging with hydroethidine. J Neurosci 16: 1324–1336, 1996

    PubMed  CAS  Google Scholar 

  15. Velazquez JLP, Frantseva MV, Carlen PL:In vitroischemia promotes glutamate-mediated free radical generation and intracellular calcium accumulation in hippocampal pyramidal neurons. J Neurosci 17: 9085–9094, 1997

    CAS  Google Scholar 

  16. Castilho RF, Hansson O, Ward MW, Budd SL, Nicholls DG: Mitochondrial control of acute glutamate excitotoxicity in cultured cerebellar granule cells. J Neurosci 18: 10277–10286, 1998

    PubMed  CAS  Google Scholar 

  17. Sengpiel B, Preis E, Krieglstein J, Prehn JH: NMDA-induced superoxide production and neurotoxicity in cultured rat hippocampal neurons: Role of mitochondria. Eur J Neurosci 10: 1903–1910, 1998

    Article  PubMed  CAS  Google Scholar 

  18. Boldyrev AA, Carpenter DO, Huentelman MJ, Peters, CM, Johnson P: Sources of reactive oxygen species production in excitotoxin-stimu-lated cerebellar granule cells. Biochem Biophys Res Commun 256: 320–324, 1999

    Article  PubMed  CAS  Google Scholar 

  19. Khodorov BI, Pinelis V, Vergun O, Storozhevykh T, Vinskaya N: Mitochondrial deenergization underlies neuronal calcium overload following a prolonged glutamate challenge. FEBS Lett 397: 230–234, 1996

    Article  PubMed  CAS  Google Scholar 

  20. Isaev NK, Zorov DB, Stelmashook EV, Uzbekov RE, Kozhemyakin MB, Victorov IV: Neurotoxic glutamate treatment of cultured cerebellar granule cells induces Ca“-dependent collapse of mitochondrial membrane potential and ultrastructural alterations of mitochondria. FEBS Lett 392: 143–147, 1996

    Article  PubMed  CAS  Google Scholar 

  21. Robb-Gaspers LD, Burnett P, Rutter GA, Denton RM, Rizzuto R, Thomas AP: Integrating cytosolic calcium signals into mitochondria] metabolic responses. EMBO J 17: 4987–5000, 1998

    Article  PubMed  CAS  Google Scholar 

  22. Robb-Gaspers LD, Rutter GA, Burnett P, Hajnoczky G, Denton RM, Thomas AP: Coupling between cytosolic and mitochondrial calcium oscillations: Role in the regulation of hepatic metabolism. Biochim Biophys Acta 1366: 17–32, 1998

    Article  PubMed  CAS  Google Scholar 

  23. Krohn AJ, Wahlbrink T, Prehn JHM: Mitochondrial depolarization is not required for neuronal apoptosis. J Neurosci 19: 7394–7404, 1999

    PubMed  CAS  Google Scholar 

  24. Nicholls DG, Budd SL: Mitochondria and neuronal excitotoxicity. Biochim Biophys Acta 1366: 97–112, 1998

    Article  PubMed  CAS  Google Scholar 

  25. Castilho RF, Ward MW, Nicholls DG: Oxidative stress, mitochondrial function, and acute glutamate excitotoxicity in cultured cerebellar granule cells. J Neurochem 72: 1394–1401, 1999

    Article  PubMed  CAS  Google Scholar 

  26. Nicholls DG, Ward MW: Mitochondrial membrane potential and neuronal glutamate excitotoxicity: Mortality and millivolts. Trends Neurosci 23: 166–174, 2000

    Article  PubMed  CAS  Google Scholar 

  27. Kadenbach B, Bender E, Reith A, Becker A, Hammerschmidt S, Lee I, Arnold S, Hüttemann M: Possible influence of metabolic activity on aging. J Anti-Aging Med 2: 255–264, 1999

    Article  CAS  Google Scholar 

  28. Kadenbach B, Hüttemann M, Arnold S, Lee I, Mühlenbein N, Bender E: Mitochondrial energy metabolism is regulated via nuclear-coded subunits of cytochrome c oxidase. Free Radic Biol Med 29: 211–221, 2000

    Article  PubMed  CAS  Google Scholar 

  29. Ludwig B, Kadenbach B, Bender E, Arnold S, Hüttemann M, Lee I, Kadenbach B: Cytochrome c oxidase and the regulation of oxidative phosphorylation. Chem Biol Chem 2: 392–403, 2000

    Google Scholar 

  30. Tsukihara T, Aoyama H, Yamashita E, Tomizaki T, Yamaguchi H, Shinzawa-Itoh K, Nakashima R, Yaono R, Yoshikawa S: The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 A. Science 272: 1136–1144, 1996

    Article  PubMed  CAS  Google Scholar 

  31. Iwata S, Ostermeier C, Ludwig B, Michel H: Structure at 2.8 A resolution of cytochrome c oxidase fromParacoccus denitrificans.Nature 376: 660–669, 1995

    Article  PubMed  CAS  Google Scholar 

  32. Arnold S, Kadenbach B: Cell respiration is controlled by ATP, an allosteric inhibitor of cytochrome c oxidase. Eur J Biochem 249: 350–354, 1997

    Article  PubMed  CAS  Google Scholar 

  33. Arnold S, Kadenbach B: Intramitochondrial ATP/ADP-ratios control cytochrome c oxidase activity allosterically. FEBS Lett 443: 105–108, 1999

    Article  PubMed  CAS  Google Scholar 

  34. Kadenbach B, Arnold S: Minireview. A second mechanism of respiratory control. FEBS Lett 447: 131–134, 1999

    Article  PubMed  CAS  Google Scholar 

  35. Nicholls DG, Ferguson SJ: In: Bioenergetics 2. Academic Press Limited, London, San Diego, 1992, pp 82–87

    Google Scholar 

  36. Bender E, Kadenbach B: The allosteric ATP-inhibition of cytochrome c oxidase is reversibly switched on by cAMP-dependent phosphorylation. FEBS Lett 466: 130–134, 2000

    Article  PubMed  CAS  Google Scholar 

  37. Lee I, Bender E, Arnold S, Kadenbach B: New control of mitochondrial membrane potential and ROS formation. Biol Chem 382: 1629–1633, 2001

    Article  PubMed  CAS  Google Scholar 

  38. Kaim G, Dimroth P: ATP synthesis by F-type ATP synthase is obligatorily dependent on the transmembrane voltage. EMBO J 18: 4118–4127, 1999

    Article  PubMed  CAS  Google Scholar 

  39. Yoshikawa S, Choc MG, O’Toole MC, Caughey WS: An infrared study of CO binding to heart cytochrome c oxidase and hemoglobin A. J Biol Chem 252: 5498–5508, 1977

    PubMed  CAS  Google Scholar 

  40. Yoshikawa S, Tera T, Takahashi Y, Tsukihara T: Crystalline cytochrome c oxidase of bovine heart mitochondrial membrane: Composition and x-ray diffraction studies. Proc Natl Acad Sci USA 85: 1354–1358, 1988

    Article  PubMed  CAS  Google Scholar 

  41. Kadenbach B, Stroh A, Ungibauer M, Kuhn-Nentwig L, Bilge U, Jarausch J: Isozymes of cytochrome c oxidase: Characterization and isolation from different tissues. Meth Enzymol 126: 32–45, 1986

    Article  PubMed  CAS  Google Scholar 

  42. Napiwotzki J, Shinzawa-Itoh K, Yoshikawa S, Kadenbach B: ATP and ADP bind to cytochrome c oxidase and regulate its activity. Biol Chem 378: 1013–1021, 1997

    Article  PubMed  CAS  Google Scholar 

  43. Napiwotzki J, Kadenbach B: Extramitochondrial ATP/ADP-ratios regulate cytochrome c oxidase activity via binding to the cytosolic domain of subunit IV. Biol Chem 379: 335–339, 1998

    Article  PubMed  CAS  Google Scholar 

  44. Anthony G, Reimann A, Kadenbach B: Tissue-specific regulation of bovine heart cytochrome c oxidase by ADP via interaction with subunit VIa. Proc Natl Acad Sci USA 90: 1652–1656, 1993

    Article  PubMed  CAS  Google Scholar 

  45. Kennaway NG, Carrero-Valenzuela RD, Ewart G, Balan VK, Lightowlers R, Zhang Y-Z, Powell BR, Capaldi RA, Buist NRM: Isoforms of mammalian cytochrome c oxidase: Correlation with human cytochrome c oxidase deficiency. Pediatr Res 28: 529–535, 1990

    Article  PubMed  CAS  Google Scholar 

  46. Pearson RB, Kemp BE: Protein kinase phosphorylation site sequences and consensus specificity motifs: Tabulations. Meth Enzymol 200: 62–81, 1991

    Article  PubMed  CAS  Google Scholar 

  47. Wan B, Doumen C, Duszynski J, Salama G, Vary TC, Lalloue KF: Effects of cardiac work on electrical potential gradient across mitochondrial membrane in perfused rat hearts. Am J Physiol 265: H453–H460, 1993

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Fachbereich Chemie, Philipps-University, Marburg, Germany

    Icksoo Lee, Elisabeth Bender & Bernhard Kadenbach

Authors
  1. Icksoo Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elisabeth Bender
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bernhard Kadenbach
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Pathology and Physiology Research Branch, National Institute for Occupational Safety and Health, 1095 Willowdale Road Mall Stop B167, Morgantown, WV, 26505, USA

    Val Vallyathan , Xianglin Shi Ph.D.  & Vince Castranova ,  & 

Rights and permissions

Reprints and permissions

Copyright information

© 2002 Springer Science+Business Media New York

About this chapter

Cite this chapter

Lee, I., Bender, E., Kadenbach, B. (2002). Control of mitochondrial membrane potential and ROS formation by reversible phosphorylation of cytochrome c oxidase. In: Vallyathan, V., Shi, X., Castranova, V. (eds) Oxygen/Nitrogen Radicals: Cell Injury and Disease. Developments in Molecular and Cellular Biochemistry, vol 37. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-1087-1_7

Download citation

  • DOI: https://doi.org/10.1007/978-1-4615-1087-1_7

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-5388-1

  • Online ISBN: 978-1-4615-1087-1

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation