Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1968 May 1;37(2):345–369. doi: 10.1083/jcb.37.2.345

ULTRASTRUCTURAL BASES FOR METABOLICALLY LINKED MECHANICAL ACTIVITY IN MITOCHONDRIA

II. Electron Transport-Linked Ultrastructural Transformations in Mitochondria

Charles R Hackenbrock 1
PMCID: PMC2107416  PMID: 5656397

Abstract

Isolated mitochondria are capable of undergoing dramatic reversible ultrastructural transformations between a condensed and an orthodox conformation. These two conformations are the extremes in ultrastructural organization between which structually and functionally intact mitochondria transform during reversible respiratory cycles. It has been found that electron transport is required for the condensed-to-orthodox ultrastructural transformation which occurs in mitochondria under State IV conditions, i.e., under conditions in which exogenous substrate is present and ADP is deficient. Inhibition of State IV electron transport at the cyanide-, antimycin A-, or Amytal-sensitive sites in the respiratory chain results in inhibition of this transformation. Resumption of electron transport in initially inhibited mitochondrial systems, initiated by channeling electrons through pathways which bypass the inhibited sites, results in resumption of the ultrastructural transformation. The condensed-to-orthodox transformation is DNP insensitive and, therefore, does not require participation of the coupling enzymes of the energy-transfer pathway. It is concluded that this ultrastructural transformation is manifest by the conversion of the chemical energy of electron transport directly into mechanical work. The reversed ultrastructural transformation, i.e., orthodox-to-condensed, which occurs during ADP-activated State III electron transport, is inhibited by DNP and parallels suppression of acceptor control and oxidative phosphorylation. Mechanochemical ultrastructural transformation as a basis for energy transfer in mitochondria is considered with respect to the results presented.

Full Text

The Full Text of this article is available as a PDF (3.0 MB).

Selected References

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

  1. 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]
  2. BERGER M. Studies on the distribution of potassium in the rat liver cell and the mechanism of potassium accumulation. Biochim Biophys Acta. 1957 Mar;23(3):504–509. doi: 10.1016/0006-3002(57)90369-4. [DOI] [PubMed] [Google Scholar]
  3. Brierley G. P., Bhattacharyya R. N. Activation of Mg++ accumulation in isolated heart mitochondria by Zn++ and by p-chloromercuribenzene sulfonate. Biochem Biophys Res Commun. 1966 Jun 13;23(5):647–651. doi: 10.1016/0006-291x(66)90448-7. [DOI] [PubMed] [Google Scholar]
  4. CARAFOLI E., ROSSI C. S., LEHNINGER A. L. CATION AND ANION BALANCE DURING ACTIVE ACCUMULATION OF CA++ AND MG++ BY ISOLATED MITOCHONDRIA. J Biol Chem. 1964 Sep;239:3055–3061. [PubMed] [Google Scholar]
  5. CHANCE B. Spectra and reaction kinetics of respiratory pigments of homogenized and intact cells. Nature. 1952 Feb 9;169(4293):215–221. doi: 10.1038/169215a0. [DOI] [PubMed] [Google Scholar]
  6. CHANCE B. THE ENERGY-LINKED REACTION OF CALCIUM WITH MITOCHONDRIA. J Biol Chem. 1965 Jun;240:2729–2748. [PubMed] [Google Scholar]
  7. 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]
  8. CHANCE B., WILLIAMS G. R. The respiratory chain and oxidative phosphorylation. Adv Enzymol Relat Subj Biochem. 1956;17:65–134. doi: 10.1002/9780470122624.ch2. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. CHAPPELL J. B., GREVILLE G. D. Mitochondrial swelling and electron transport. I. Swelling supported by ferricyanide. Biochim Biophys Acta. 1960 Mar 11;38:483–494. doi: 10.1016/0006-3002(60)91283-x. [DOI] [PubMed] [Google Scholar]
  11. CHAPPELL J. B., GREVILLE G. D. Mitochondrial swelling and electron transport. I. Swelling supported by ferricyanide. Biochim Biophys Acta. 1960 Mar 11;38:483–494. doi: 10.1016/0006-3002(60)91283-x. [DOI] [PubMed] [Google Scholar]
  12. CLARK L. C., Jr, WOLF R., GRANGER D., TAYLOR Z. Continuous recording of blood oxygen tensions by polarography. J Appl Physiol. 1953 Sep;6(3):189–193. doi: 10.1152/jappl.1953.6.3.189. [DOI] [PubMed] [Google Scholar]
  13. CONNELLY J. L., LARDY H. A. ANTIBIOTICS AS TOOLS FOR METABOLIC STUDIES. 3. EFFECTS OF OLIGOMYCIN AND AUROVERTIN ON THE SWELLING AND CONTRACTION PROCESSES OF MITOCHONDRIA. Biochemistry. 1964 Dec;3:1969–1973. doi: 10.1021/bi00900a031. [DOI] [PubMed] [Google Scholar]
  14. Carafoli E., Rossi C. S., Lehninger A. L. Energy-coupling in mitochondria during resting or state 4 respiration. Biochem Biophys Res Commun. 1965 May 18;19(5):609–614. doi: 10.1016/0006-291x(65)90383-9. [DOI] [PubMed] [Google Scholar]
  15. Chalkley H. W., Cornfield J., Park H. A Method for Estimating Volume-Surface Ratios. Science. 1949 Sep 23;110(2856):295–297. doi: 10.1126/science.110.2856.295. [DOI] [PubMed] [Google Scholar]
  16. Chance B., Lee C. P., Mela L. Control and conservation of energy in the cytochrome chain. Fed Proc. 1967 Sep;26(5):1341–1354. [PubMed] [Google Scholar]
  17. 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]
  18. EMMELOT P. Abolition by 2:4-dinitrophenol of the protective effect of succinate and adenine nucletides on the onset of the thvroxine-induced swelling of liver mitochondria. Nature. 1960 Dec 31;188:1197–1199. doi: 10.1038/1881197a0. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Gamble J. L., Jr, Hess R. C., Jr Mitochondrial electrolytes. Am J Physiol. 1966 Apr;210(4):765–770. doi: 10.1152/ajplegacy.1966.210.4.765. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. 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]
  23. KARNOVSKY M. J. Simple methods for "staining with lead" at high pH in electron microscopy. J Biophys Biochem Cytol. 1961 Dec;11:729–732. doi: 10.1083/jcb.11.3.729. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. LARDY H. A., CONNELLY J. L., JOHNSON D. ANTIBIOTIC STUDIES. II. INHIBITION OF PHOSPHORYL TRANSFER IN MITOCHONDRIA BY OLIGOMYCIN AND AUROVERTIN. Biochemistry. 1964 Dec;3:1961–1968. doi: 10.1021/bi00900a030. [DOI] [PubMed] [Google Scholar]
  25. LARDY H. A., WELLMAN H. Oxidative phosphorylations; rôle of inorganic phosphate and acceptor systems in control of metabolic rates. J Biol Chem. 1952 Mar;195(1):215–224. [PubMed] [Google Scholar]
  26. LEHNINGER A. L. Oxidative phosphorylation. Harvey Lect. 1953;49:176–215. [PubMed] [Google Scholar]
  27. Lehninger A. L., Carafoli E., Rossi C. S. Energy-linked ion movements in mitochondrial systems. Adv Enzymol Relat Areas Mol Biol. 1967;29:259–320. doi: 10.1002/9780470122747.ch6. [DOI] [PubMed] [Google Scholar]
  28. MITCHELL P. Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature. 1961 Jul 8;191:144–148. doi: 10.1038/191144a0. [DOI] [PubMed] [Google Scholar]
  29. Mintz H. A., Yawn D. H., Safer B., Bresnick E., Liebelt A. G., Blailock Z. R., Rabin E. R., Schwartz A. Morphological and biochemical studies of isolated mitochondria from fetal, neonatal, and adult liver and from neoplastic tissues. J Cell Biol. 1967 Aug;34(2):513–523. doi: 10.1083/jcb.34.2.513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. PRESSMAN B. C., PARK J. K. Competition between magnesium and guanidine for mitochondrial binding sites. Biochem Biophys Res Commun. 1963 May 3;11:182–186. doi: 10.1016/0006-291x(63)90331-0. [DOI] [PubMed] [Google Scholar]
  31. Packer L., Mustafa M. G. Pathways of electron flow established by tetramethylphenylenediamine in mitochondria and ascites tumor cells. Biochim Biophys Acta. 1966 Jan 11;113(1):1–12. doi: 10.1016/s0926-6593(66)80115-7. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Rasmussen H., Ogata E. Parathyroid hormone and the reactions of mitochondria to cations. Biochemistry. 1966 Feb;5(2):733–745. doi: 10.1021/bi00866a047. [DOI] [PubMed] [Google Scholar]
  34. SIEKEVITZ P., LOW H., ERNSTER L., LINDBERG O. On a possible mechanism of the adenosinetriphosphatase of liver mitochondria. Biochim Biophys Acta. 1958 Aug;29(2):378–391. doi: 10.1016/0006-3002(58)90197-5. [DOI] [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. TEDESCHI H., HARRIS D. L. The osmotic behavior and permeability to non-electrolytes of mitochondria. Arch Biochem Biophys. 1955 Sep;58(1):52–67. doi: 10.1016/0003-9861(55)90092-8. [DOI] [PubMed] [Google Scholar]
  37. Weibel E. R., Kistler G. S., Scherle W. F. Practical stereological methods for morphometric cytology. J Cell Biol. 1966 Jul;30(1):23–38. doi: 10.1083/jcb.30.1.23. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Weinbach E. C., Garbus J., Sheffield H. G. Morphology of mitochondria in the coupled, uncoupled and recoupled states. Exp Cell Res. 1967 Apr;46(1):129–143. doi: 10.1016/0014-4827(67)90415-6. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES