Skip to main content
SpringerLink
Log in
Book cover

Bioenergetics of the Cell: Quantitative Aspects pp 107–121Cite as

Energetics of swelling in isolated hepatocytes: A comprehensive study

  • Chapter

  • 280 Accesses

Part of the book series: Developments in Molecular and Cellular Biochemistry ((DMCB,volume 25))

Abstract

Cell swelling is now admitted as being a new principle of metabolic control but little is known about the energetics of cell swelling. We have studied the influence of hypo- or hyperosmolarity on both isolated hepatocytes and isolated rat liver mitochondria. Cytosolic hypoosmolarity on isolated hepatocytes induces an increase in matricial volume and does not affect the myxothiazol sensitive respiratory rate while the absolute value of the overall thermodynamic driving force over the electron transport chain increases. This points to an increase in kinetic control upstream the respiratory chain when cytosolic osmolarity is decreased. On isolated rat liver mitochondria incubated in hypoosmotic potassium chloride media, energetic parameters vary as in cells and oxidative phosphorylation efficiency is not affected. Cytosolic hyperosmolarity induced by sodium co-transported amino acids, per se, does not affect either matrix volume or energetic parameters. This is not the case in isolated rat liver mitochondria incubated in sucrose hyperosmotic medium. Indeed, in this medium, adenine nucleotide carrier is inhibited as the external osmolarity increases, which lowers the state 3 respiration close to state 4 level and consequently leads to a decrease in oxidative phosphorylation efficiency. When isolated rat liver mitochondria are incubated in KC1 hyperosmotic medium, state 3 respiratory rate, matrix volume and membrane electrical potential vary as a function of time. Indeed, matrix volume is recovered in hyperosmotic KC1 medium and this recovery is dependent on Pi-Kentry. State 3 respiratory rate increases and membrane electrical potential difference decreases during the first minutes of mitochondrial incubation until the attainment of the same value as in isoosmotic medium. This shows that matrix volume, flux and force are regulated as a function of time in KC1 hyperosmotic medium. Under steady state, neither matrix volume nor energetic parameters are affected. Moreover, NaCl hyperosmotic medium allows matrix volume recovery but induces a decrease in state 3 respiratory flux. This indicates that potassium is necessary for both matrix volume and flux recovery in isolated mitochondria. We conclude that hypoosmotic medium induces an increase in kinetic control both upstream and on the respiratory chain and changes the oxidative phosphorylation response to forces. At steady state, hyperosmolarity, per se, has no effect on oxidative phosphorylation in either isolated hepatocytes or isolated mitochondria incubated in KC1 medium. Therefore, potassium plays a key role in matrix volume, flux and force regulation. (Mol Cell Biochem 184: 107–121, 1998)

This is a preview of subscription content, 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   169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   219.99
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

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Häussinger D, Lang F: Cell volume in the regulation of hepatic function: A mechanism for metabolic control. Biochim Biophys Acta 1071:331–350, 1991

    Article  PubMed  Google Scholar 

  2. Hallbrucker C, Vom Dahl S, Lang F, Häussinger D: Control of hepatic proteolysis by amino acids. The role of cell volume. Eur J Biochem 197:717–724, 1991

    Article  PubMed  CAS  Google Scholar 

  3. Bacquet A, Hue L, Meijer AJ, Van Woerkom GM, Plomb PJAM: Swelling of rat hepatocytes stimulates glycogen synthesis. J Biol Chem 265:955–959, 1990

    Google Scholar 

  4. Graf J, Haddad P, Häussinger D, Lang F: Cell volume regulation in liver. Renal Physiol Biochem 11:202–220, 1988

    PubMed  CAS  Google Scholar 

  5. Häussinger D, Stehle T, Lang F: Volume regulation in liver: Further characterization by inhibitors and ionic substitution. Hepatology 11:243–254, 1990

    Article  PubMed  Google Scholar 

  6. Lang F, Stehle T, Häussinger D: Water, K+, H+, lactate and glucose fluxes during cell volume regulation in perfused rat liver. Pflüggers Arch 413:209–216, 1989

    Article  CAS  Google Scholar 

  7. Häussinger D, Halbrucker C, Vom Dahl S, Lang F, Gerok W: Cell swelling inhibits proteolysis in perfused rat liver. Biochem. J 272:239–242, 1990

    PubMed  Google Scholar 

  8. Häussinger D, Halbrucker C, Vom Dahl S, Decker S, Schweizer V, Lang F, Gerok W: Cell volume is a major determinant of proteolysis control in liver. FEBS Lett 283:70–72, 1991

    Article  PubMed  Google Scholar 

  9. Häussinger D, Lang F J: Exposure of perfused liver to hypotonic conditions modify cellular nitrogen metabolism. Cell Biochem 43:355–361, 1990

    Article  Google Scholar 

  10. Hallbrucker C, vom Dahl S, Lang F, Haussinger D: Interactions between cell volume and hepatic nitrogen metabolism. Cont Nephrol 92:175–181, 1991

    CAS  Google Scholar 

  11. Bode B, Kilberg M: Amino acid dependent increase in hepatic system N activity is linked to cell swelling. J Biol Chem 266:7376–7381, 1991

    PubMed  CAS  Google Scholar 

  12. Häussinger D, Lang F: The mutual interaction between cell volume and cell function: A new principle of metabolic regulation. Biochem CellBio 143:1–4, 1991

    Article  Google Scholar 

  13. Meijer AJ, Bacquet A, Gustafson L, Van Woerkom GM, Hue L: Mechanism of activation of liver glycogen synthase by swelling. J Biol Chem 267:5823–5828, 1992

    PubMed  CAS  Google Scholar 

  14. Bacquet A, Gaussin V, Bollen M, Stalmaus W, Hue L: Mechanism of activation of liver acetyl-CoA carboxylase by cell swelling. Eur J Biochem 217:1083–1089, 1993

    Article  Google Scholar 

  15. Völkel H, Busch GL, Häussinger D, Lang F: Alkalinisation of acidic cellular compartments following cell swelling. FEBS Lett 338:27–30, 1994

    Article  Google Scholar 

  16. Halestrap PA: The regulation of the matrix volume of mammalian mitochondria in vivo and in vitro and its role in the control of mitochondrial metabolism. Biochim Biophys Acta 973:355–382, 1989

    Article  PubMed  CAS  Google Scholar 

  17. Halestrap PA, Davidson MA, Potter WD: Mechanisms involved in the hormonal regulation of mitochondrial function through changes in the matrix volume. Biochim Biophys Acta 1018:278–281, 1990

    Article  CAS  Google Scholar 

  18. Armston EA, Halestrap PA, Scott DR: The nature of the changes in liver mitochondrial function induced by glucagon treatment of rats. The effects of intramitochondrial volume, aging and benzyl alcohol. Biochim Biophys Acta 681:429–439, 1982

    Article  PubMed  CAS  Google Scholar 

  19. Otto AD, Ontko AJ: Structure-function relations between fatty acids oxidation and the mitochondrial inner membrane-matrix region. Eur J Biochem 129:479–485, 1982

    Article  PubMed  CAS  Google Scholar 

  20. Mathai CJ, Sauna EZ, John O, Sitaramam V: Rate limiting step in electron transport. Osmotically sensitive diffusion of quinones through voids in the bilayer. J Biol Chem 268:15442–15454, 1993

    PubMed  CAS  Google Scholar 

  21. Nicholls DG, Lindberg O: Inhibited respiration and ATPase activity of rat liver mitochondria under conditions of matrix condensation. FEBS Lett 25:61–64, 1972

    Article  PubMed  CAS  Google Scholar 

  22. Sitaramam V, Rao NM: Oxidative phosphorylation in rat liver mito chondria: Influence of physical parameters. Ind J Biochem Biophys 28:401–407, 1991

    CAS  Google Scholar 

  23. Garlid KD: Mitochondrial cation transport: A progress report. J Bioenerg Biomembr 26:537–542, 1994

    Article  PubMed  CAS  Google Scholar 

  24. Garlid KD: On the mechanism of regulation of the mitochondrial K+H+ exchanger. J Biol Chem 255:11273–11279, 1980

    PubMed  CAS  Google Scholar 

  25. Gunter TE: Transport of calcium by mitochondria. J Bioenerg Biomembr 26:465–469, 1994

    Article  PubMed  CAS  Google Scholar 

  26. Berry NM, Friend DS: High-yield preparation of isolated rat liver parenchymal cells: A biochemical and fine structural study. J Cell Biol 43:506–520, 1969

    Article  PubMed  CAS  Google Scholar 

  27. Groen AK, Sips HJ, Vervoorn RC, Tager JM: Intracellular compartmentation and control of alanine metabolism in rat liver parenchymal cells. Eur JBiochem 122:87–93, 1982

    Article  CAS  Google Scholar 

  28. Krebs HA, Heiseleit K: Urea formation in the animal body. Hoppe-Seyler’s Z Physiol Chem 210:33–66, 1932

    Article  CAS  Google Scholar 

  29. Quilan PT, Thomas AP, Armston AE, Halestrap AP: Measurement of the intramitochondrial volume in hepatocytes without cell disruption and its elevation by hormones and valinomycin. Biochem J 214:395–404, 1983

    Google Scholar 

  30. Nobes CD, Brand MD: A quantitative assessment of the use of 36C1’ distribution to measure plasma membrane potential in isolated hepatocytes. Biochim Biophys Acta 987:115–123, 1989

    Article  PubMed  CAS  Google Scholar 

  31. Nobes CD, Hay WW, Brand MD: The mechanism of stimulation of respiration by fatty acids in isolated hepatocytes. J Biol Chem 265:12910–12915, 1990

    PubMed  CAS  Google Scholar 

  32. Scott ID, Nicholls DG: Energy transduction in intact synaptosomes. BiochemJ 186:21–33, 1980

    CAS  Google Scholar 

  33. Berry MN, Gregory RB, Grivell AR, Henly DC, Nobes CD, Phillips JW, Wallace PC: Intracellular mitochondrial membrane potential as an indicator of hepatocytes energy metabolism: Further evidence for thermodynamic control of metabolism. Biochim Biophys Acta 936:294–306, 1988

    Article  PubMed  CAS  Google Scholar 

  34. Hoek JB, Nicholls DG, Williamson JR: Determination of the mitochondrial protonmotive force in isolated hepatocytes. J Biol Chem 255:1458–1464, 1980

    PubMed  CAS  Google Scholar 

  35. Murphy MP, Brand MD: The control of electron flux through cytochrome oxidase. Biochem J 243:499–505, 1987

    PubMed  CAS  Google Scholar 

  36. Zuurendonck PF, Tager JM: Rapid separation of particulate components and soluble cytoplasm of isolated rat liver cells. Biochim Biophys Acta 333:393–399, 1974

    Article  Google Scholar 

  37. Akerboom TPM, Van der Meer R, Tager JM: Techniques for the investigation of intracellular compartmentation. Tech Metab Res B 205:1–33, 1979

    Google Scholar 

  38. Krebs HA, Veech RL: In: S Papa, JM Tager, E Qualliariello, EC Slater (eds). Pyridine Nucleotide Interrelations. Adriatica Editrice, Bari, 1969, pp 329–382

    Google Scholar 

  39. Berenblum I, Chain E: Studies on the colorimetric determination of phosphate. Biochem J 32:286–294, 1938

    PubMed  CAS  Google Scholar 

  40. Henrickson RL, Meredith SC: Amino acid analysis by reverse phase high performance liquid chromatography: Precolumn derivatization with phenylisothiocyanate. Anal Biochem 136:65–74, 1984

    Article  Google Scholar 

  41. Cooper C, Lehninger AL: Oxidative phosphorylation by an enzyme complex from extracts of mitochondria. J Biol Chem 177:751–766, 1956

    Google Scholar 

  42. Gornall AG, Bardawill CJ, David MM: Determination of serum proteins by means ofthebiuret reaction. J Biol Chem 177:751–766, 1948

    CAS  Google Scholar 

  43. Rigoulet M, Devin A, Avéret N, Vandais B, Guérin B: Mechanisms of inhibition and uncoupling of respiration in isolated rat liver mito chondria by the general anesthetic 2,6-diisopropylphenol. Eur J Biochem 241:280–285, 1996

    Article  PubMed  CAS  Google Scholar 

  44. Rigoulet M, Guérin B: Phosphate transport and ATP-synthesis in yeast mitochondria: Effect of a new inhibitor: The tribenzyl phosphate. FEBS Lett 102:18–22, 1979

    Article  PubMed  CAS  Google Scholar 

  45. Rottenberg H.: The measurement of membrane potential and ApH in cells, organelles and vesicles. Meth Enzymol 55:547–569, 1979

    Article  PubMed  CAS  Google Scholar 

  46. Espié P, Guérin B, Rigoulet M: On isolated hepatocytes mitochondrial swelling induced in hypoosmotic medium does not affect the respiration rate. Biochim Biophys Acta 1230:139–146, 1995

    Article  PubMed  Google Scholar 

  47. Koretsky A, Balaban RS: Changes in pyridine nucleotides level alter oxygen consumption and extra-mitochondrial phosphate in isolated mitochondria: A31PNMR and NAD(P)H fluorescence study. Biochim Biophys Acta 893:398–408, 1987

    Article  PubMed  CAS  Google Scholar 

  48. Emaus RK, Grunwald R, Lemasters JJ: Rhodamine 123 as a probe of transmembrane potential in isolated rat liver mitochondria: Spectral and metabolic properties. Biochim Biophys Acta 850:436–448, 1986

    Article  PubMed  CAS  Google Scholar 

  49. Devin A, Guérin B, Rigoulet M: Dependence of flux size and efficiency of oxidative phosphorylation on external osmolarity in isolated rat liver mitochondria: Role of adenine nucleotide carrier. Biochim Biophys Acta 1273:13–20, 1996

    Article  PubMed  Google Scholar 

  50. Groen KA, Wanders AJR, Westerhoff VH, van der Meer R, Tager MJ: Quantification of the contribution of various steps to control mito chondrial respiration. J Biol Chem 257:2754–2757, 1982

    PubMed  CAS  Google Scholar 

  51. Gellerich FN, Kunz WS, Bohnensack R: Estimation of flux control coefficient from inhibitor titration by non-linear regression. FEBS Lett 274:167–170, 1990

    Article  PubMed  CAS  Google Scholar 

  52. Groen AK: Quantification of control in studies on intermediary metabolism. Ph.D. Thesis, Amsterdam, 1984

    Google Scholar 

  53. Vignais PV, Vignais M, Defaye G: Adenosine diphosphate translocation in yeast mitochondria. Nature of the receptor site for carboxy-atractyloside. Biochemistry 12:1508–1519, 1973

    Article  PubMed  CAS  Google Scholar 

  54. Brown GC: Control of respiration and ATP synthesis in mammalians mitochondria and cells. Biochem J 284:1–13, 1992

    PubMed  CAS  Google Scholar 

  55. Quentin E, Averet N, Guerin B, Rigoulet M: Temperature dependence of the coupling efficiency of rat liver oxidative phosphorylation: role of adenine nucleotide translocator. Biophys Biochem Res Com 202:816–821, 1994

    Article  CAS  Google Scholar 

  56. Brierley GP, Baysal K, Jung DW: Cation transport systems in mitochondria: Na+ and K+ uniports and exchangers. J Bioenerg Biomembr 26:519–526, 1994

    Article  PubMed  CAS  Google Scholar 

  57. Beavis AD: On the inhibition of the mitochondrial inner membrane anion uniporter by cationic amphiphiles and others drugs. J Biol Chem 264:1508–1515, 1989

    PubMed  CAS  Google Scholar 

  58. Sturgess NC, Ashford MLJ, Cook DL, Hales CN: The sulphonylurae receptor may be an ATP sensitive potassium channel. Lancet 8453:474–475, 1985

    Article  Google Scholar 

  59. Inoue I, Nagase H, Kishi K, Higuti T: ATP-sensitive K+ channel in the mitochondrial inner membrane. Nature 352:244–247, 1991

    Article  PubMed  CAS  Google Scholar 

  60. Garlid KD, DiResta DJ, Beavis AD, Martin WH: On the mechanism by which dicyclohexylcarboxydiimide and quinine inhibits K+ transport in rat liver mitochondria. J Biol Chem 261:1529–1535, 1986

    PubMed  CAS  Google Scholar 

  61. Halestrap AP, Quilan TP, Whipps ED, Armston EA: Regulation of the mitochondrial matrix volume in vivo and in vitro. The role of calcium. Biochem J 236:779–787, 1986

    PubMed  CAS  Google Scholar 

  62. Halestrap AP, Dunlop LJ: Intramitochondrial regulation of fatty acids β-oxidation occurs between flavoproteins and ubiquinone. A role for changes in matrix volume. Biochem J 239:559–565, 1986

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut de Biochimie et Génétique Cellulaires du CNRS, Université de Bordeaux 2, 1 rue Camille Saint-Saëns, 33 077, Bordeaux cedex, France

    Anne Devin, Pascal Espié, Bernard Guérin & Michel Rigoulet

Authors
  1. Anne Devin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pascal Espié
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bernard Guérin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michel Rigoulet
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Laboratories of Bioenergetics, Institute of Chemical and Biological Physics, Tallinn, Estonia

    Valdur A. Saks

  2. Cellular and Molecular Cardiology, U 446 INSERM, Chatenay-Malabry, France

    Renée Ventura-Clapier

  3. Laboratory of Bioenergetics, Joseph Fourier University, Grenoble, France

    Valdur A. Saks , Xavier Leverve  & André Rossi ,  & 

  4. Laboratory of Bioenergetics, Institute of Biochemistry and Cellular Genetics CNRS, Bordeaux, France

    Michel Rigoulet

Rights and permissions

Reprints and permissions

Copyright information

© 1998 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Devin, A., Espié, P., Guérin, B., Rigoulet, M. (1998). Energetics of swelling in isolated hepatocytes: A comprehensive study. In: Saks, V.A., Ventura-Clapier, R., Leverve, X., Rossi, A., Rigoulet, M. (eds) Bioenergetics of the Cell: Quantitative Aspects. Developments in Molecular and Cellular Biochemistry, vol 25. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-5653-4_9

Download citation

  • DOI: https://doi.org/10.1007/978-1-4615-5653-4_9

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-7587-6

  • Online ISBN: 978-1-4615-5653-4

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation