Skip to main content
Biochemical Journal logoLink to Biochemical Journal
. 1972 Feb;126(3):689–700. doi: 10.1042/bj1260689

The effect of the coupled oxidation of substrate on the permeability of blowfly flight-muscle mitochondria to potassium and other cations

Richard G Hansford 1,*, Albert L Lehninger 1
PMCID: PMC1178428  PMID: 5075274

Abstract

1. Blowfly flight-muscle mitochondria respiring in the absence of phosphate acceptor (i.e. in state 4) take up greater amounts of K+, Na+, choline, phosphate and Cl (but less NH4+) than non-respiring control mitochondria. 2. Uptake of cations is accompanied by an increase in the volume of the mitochondrial matrix, determined with the use of [14C]-sucrose and 3H2O. The osmolarity of the salt solution taken up was approximately that of the suspending medium. 3. The [14C]sucrose-inaccessible space decreased with increasing osmolarity of potassium chloride in the suspending medium, confirming that the blowfly mitochondrion behaves as an osmometer. 4. Light-scattering studies showed that both respiratory substrate and a permeant anion such as phosphate or acetate are required for rapid and massive entry of K+, which occurs in an electrophoretic process rather than in exchange for H+. The increase in permeability to K+ and other cations is probably the result of a large increase in the exposed area of inner membrane surface in these mitochondria, with no intrinsic increase in the permeability per unit area. 5. No increase in permeability to K+ and other cations occurs during phosphorylation of ADP in state 3 respiration.

Full text

PDF
689

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. AMOORE J. E., BARTLEY W. The permeability of isolated rat-liver mitochondria to sucrose, sodium chloride and potassium chloride at 0 degrees. Biochem J. 1958 Jun;69(2):223–236. doi: 10.1042/bj0690223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. AMOORE J. E. Exchange of potassium ions across a concentration difference by isolated rat-liver mitochondria. Biochem J. 1960 Sep;76:438–444. doi: 10.1042/bj0760438. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Azzi A., Azzone G. F. Swelling and shrinkage phenomena in liver mitochondria. IV. Reversible swelling changes linked to transport of monovalent cations stimulated by valinomycin. Biochim Biophys Acta. 1966 Mar 7;113(3):445–456. doi: 10.1016/s0926-6593(66)80003-6. [DOI] [PubMed] [Google Scholar]
  4. Azzi A., Azzone G. F. Swelling and shrinkage phenomena in liver mitochondria. VI. Metabolism-independent swelling coupled to ion movement. Biochim Biophys Acta. 1967 May 9;131(3):468–478. doi: 10.1016/0005-2728(67)90006-0. [DOI] [PubMed] [Google Scholar]
  5. BARTLEY W., DAVIES R. E. Active transport of ions by sub-cellular particles. Biochem J. 1954 May;57(1):37–49. doi: 10.1042/bj0570037. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. BARTLEY W. Solute movemetns during volume changes in rat-liver mitochondria. Biochem J. 1961 Jul;80:46–57. doi: 10.1042/bj0800046. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Berenblum I., Chain E. An improved method for the colorimetric determination of phosphate. Biochem J. 1938 Feb;32(2):295–298. doi: 10.1042/bj0320295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Blondin G. A., Green D. E. Mechanism of mitochondrial swelling. 3. Two forms of energized swelling. Arch Biochem Biophys. 1969 Jul;132(2):509–523. doi: 10.1016/0003-9861(69)90395-6. [DOI] [PubMed] [Google Scholar]
  9. Brierley G. P. Energy-linked alteration of the permeability of heart mitochondria to chloride and other anions. Biochemistry. 1970 Feb 17;9(4):697–707. doi: 10.1021/bi00806a001. [DOI] [PubMed] [Google Scholar]
  10. Brierley G. P., Settlemire C. T., Knight V. A. Ion transport by heart mitochondria. XI. The spontaneous and induced permeability of heart mitochondria to cations. Arch Biochem Biophys. 1968 Jul;126(1):276–288. doi: 10.1016/0003-9861(68)90584-5. [DOI] [PubMed] [Google Scholar]
  11. CHANCE B., WILLIAMS G. R. Respiratory enzymes in oxidative phosphorylation. III. The steady state. J Biol Chem. 1955 Nov;217(1):409–427. [PubMed] [Google Scholar]
  12. CHAPPELL J. B., CROFTS A. R. GRAMICIDIN AND ION TRANSPORT IN ISOLATED LIVER MITOCHONDRIA. Biochem J. 1965 May;95:393–402. doi: 10.1042/bj0950393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. CHRISTIE G. S., AHMED K., MCLEAN A. E., JUDAH D. ACTIVE TRANSPORT OF POTASSIUM BY MITOCHONDRIA. I. EXCHANGE OF K+ AND H+. Biochim Biophys Acta. 1965 Mar 29;94:432–440. doi: 10.1016/0926-6585(65)90051-8. [DOI] [PubMed] [Google Scholar]
  14. Carafoli E., Hansford R. G., Sackton B., Lehninger A. L. Interaction of Ca2+ with blowfly flight muscle mitochondria. J Biol Chem. 1971 Feb 25;246(4):964–972. [PubMed] [Google Scholar]
  15. Childress C. C., Sacktor B. Pyruvate oxidation and the permeability of mitochondria from blowfly flight muscle. Science. 1966 Oct 14;154(3746):268–270. doi: 10.1126/science.154.3746.268. [DOI] [PubMed] [Google Scholar]
  16. Cockrell R. S., Harris E. J., Pressman B. C. Energetics of potassium transport in mitochondria induced by valinomycin. Biochemistry. 1966 Jul;5(7):2326–2335. doi: 10.1021/bi00871a022. [DOI] [PubMed] [Google Scholar]
  17. GAMBLE J. L., Jr Potassium binding and oxidative phosphorylation in mitochondria and mitochondrial fragments. J Biol Chem. 1957 Oct;228(2):955–971. [PubMed] [Google Scholar]
  18. Hackenbrock C. R. Ultrastructural bases for metabolically linked mechanical activity in mitochondria. I. Reversible ultrastructural changes with change in metabolic steady state in isolated liver mitochondria. J Cell Biol. 1966 Aug;30(2):269–297. doi: 10.1083/jcb.30.2.269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hackenbrock C. R. Ultrastructural bases for metabolically linked mechanical activity in mitochondria. II. Electron transport-linked ultrastructural transformations in mitochondria. J Cell Biol. 1968 May;37(2):345–369. doi: 10.1083/jcb.37.2.345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Harris E. J., Catlin G., Pressman B. C. Effect of transport-inducing antibiotics and other agents on potassium flux in mitochondria. Biochemistry. 1967 May;6(5):1360–1369. doi: 10.1021/bi00857a019. [DOI] [PubMed] [Google Scholar]
  21. Harris E. J., Cockrell R., Pressman B. C. Induced and spontaneous movements of potassium ions into mitochondria. Biochem J. 1966 Apr;99(1):200–213. doi: 10.1042/bj0990200. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Harris E. J., van Dam K. Changes of total water and sucrose space accompanying induced ion uptake or phosphate swelling of rat liver mitochondria. Biochem J. 1968 Feb;106(3):759–766. doi: 10.1042/bj1060759. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hunter G. R., Brierley G. P. Ion transport by heart mitochondria. XIV. The mannitol-impermeable compartment of the mitochondrion and its relation to ion uptake. Biochim Biophys Acta. 1969 May;180(1):68–80. doi: 10.1016/0005-2728(69)90195-9. [DOI] [PubMed] [Google Scholar]
  24. Klingenberg M. Localization of the glycerol-phosphate dehydrogenase in the outer phase of the mitochondrial inner membrane. Eur J Biochem. 1970 Apr;13(2):247–252. doi: 10.1111/j.1432-1033.1970.tb00924.x. [DOI] [PubMed] [Google Scholar]
  25. Massari S., Azzone G. F. The mechanism of ion translocation in mitochondria. 2. Active transport and proton pump. Eur J Biochem. 1970 Feb;12(2):310–318. doi: 10.1111/j.1432-1033.1970.tb00852.x. [DOI] [PubMed] [Google Scholar]
  26. Mitchell P., Moyle J. Respiration-driven proton translocation in rat liver mitochondria. Biochem J. 1967 Dec;105(3):1147–1162. doi: 10.1042/bj1051147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Mitchell P., Moyle J. Translocation of some anions cations and acids in rat liver mitochondria. Eur J Biochem. 1969 Jun;9(2):149–155. doi: 10.1111/j.1432-1033.1969.tb00588.x. [DOI] [PubMed] [Google Scholar]
  28. Mitchell P. Translocations through natural membranes. Adv Enzymol Relat Areas Mol Biol. 1967;29:33–87. doi: 10.1002/9780470122747.ch2. [DOI] [PubMed] [Google Scholar]
  29. PRICE G. M., LEWIS S. E. Distribution of phosphorus compounds in blowfly thoracic muscle. Biochem J. 1959 Jan;71(1):176–185. doi: 10.1042/bj0710176. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Pfaff E., Klingenberg M., Ritt E., Vogell W. Korrelation des unspezifisch permeablen mitochondrialen Raumes mit dem "Intermembran-Raum". Eur J Biochem. 1968 Jul;5(2):222–232. doi: 10.1111/j.1432-1033.1968.tb00361.x. [DOI] [PubMed] [Google Scholar]
  31. Pressman B. C. Induced active transport of ions in mitochondria. Proc Natl Acad Sci U S A. 1965 May;53(5):1076–1083. doi: 10.1073/pnas.53.5.1076. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. ROSEN H. A modified ninhydrin colorimetric analysis for amino acids. Arch Biochem Biophys. 1957 Mar;67(1):10–15. doi: 10.1016/0003-9861(57)90241-2. [DOI] [PubMed] [Google Scholar]
  33. ROTTENBERG H., SOLOMON A. K. ENERGY LINKED K UPTAKE IN MITOCHONDRIA. Biochem Biophys Res Commun. 1965 Jun 18;20:85–92. [PubMed] [Google Scholar]
  34. Rasmussen H., Chance B., Ogata E. A mechanism for the reactions of calcium with mitochondria. Proc Natl Acad Sci U S A. 1965 May;53(5):1069–1076. doi: 10.1073/pnas.53.5.1069. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. SLATER E. C. Mechanism of phosphorylation in the respiratory chain. Nature. 1953 Nov 28;172(4387):975–978. doi: 10.1038/172975a0. [DOI] [PubMed] [Google Scholar]
  36. SPECTOR W. G. Electrolyte flux in isolated mitochondria. Proc R Soc Lond B Biol Sci. 1953 Apr 17;141(903):268–279. doi: 10.1098/rspb.1953.0041. [DOI] [PubMed] [Google Scholar]
  37. TEDESCHI H. Osmotic reversal of mitochondrial swelling. Biochim Biophys Acta. 1961 Jan 1;46:159–169. doi: 10.1016/0006-3002(61)90659-x. [DOI] [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES