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. 1983 Apr;80(8):2243–2247. doi: 10.1073/pnas.80.8.2243

Structural and functional evidence for multiple channel complexes in the outer membrane of Neurospora crassa mitochondria.

C A Mannella, M Colombini, J Frank
PMCID: PMC393795  PMID: 6300902

Abstract

The outer membrane of mitochondria contains proteins that form channels called VDAC (voltage-dependent anion-selective channels). Two independent lines of evidence suggest that these channels occur in specific complexes in the outer membrane of Neurospora mitochondria. Electron microscopic images of these outer membranes reveal polymorphic crystalline arrays of putative pores. These arrays can be shown to be interrelated by movement in the membrane plane of a particular rigid channel triplet or of regular aggregates of this triplet. Detergent extracts of the same outer membranes induce single- and multiple-step conductances in planar phospholipid membranes, with a marked preference for the insertion of triplets and multiples of triplets. The tendency of the mitochondrial channels to occur as extended arrays, apparently built up from triplets, may have important functional and evolutionary implications.

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Selected References

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

  1. Colombini M. A candidate for the permeability pathway of the outer mitochondrial membrane. Nature. 1979 Jun 14;279(5714):643–645. doi: 10.1038/279643a0. [DOI] [PubMed] [Google Scholar]
  2. Colombini M. Structure and mode of action of a voltage dependent anion-selective channel (VDAC) located in the outer mitochondrial membrane. Ann N Y Acad Sci. 1980;341:552–563. doi: 10.1111/j.1749-6632.1980.tb47198.x. [DOI] [PubMed] [Google Scholar]
  3. Felgner P. L., Messer J. L., Wilson J. E. Purification of a hexokinase-binding protein from the outer mitochondrial membrane. J Biol Chem. 1979 Jun 25;254(12):4946–4949. [PubMed] [Google Scholar]
  4. Fiek C., Benz R., Roos N., Brdiczka D. Evidence for identity between the hexokinase-binding protein and the mitochondrial porin in the outer membrane of rat liver mitochondria. Biochim Biophys Acta. 1982 Jun 14;688(2):429–440. doi: 10.1016/0005-2736(82)90354-6. [DOI] [PubMed] [Google Scholar]
  5. Freitag H., Neupert W., Benz R. Purification and characterisation of a pore protein of the outer mitochondrial membrane from Neurospora crassa. Eur J Biochem. 1982 Apr;123(3):629–636. doi: 10.1111/j.1432-1033.1982.tb06578.x. [DOI] [PubMed] [Google Scholar]
  6. Lindén M., Gellerfors P., Nelson B. D. Pore protein and the hexokinase-binding protein from the outer membrane of rat liver mitochondria are identical. FEBS Lett. 1982 May 17;141(2):189–192. doi: 10.1016/0014-5793(82)80044-6. [DOI] [PubMed] [Google Scholar]
  7. Makowski L., Caspar D. L., Goodenough D. A., Phillips W. C. Gap Junction Structures: III. The Effect of Variations in the Isolation Procedure. Biophys J. 1982 Jan;37(1):189–191. doi: 10.1016/S0006-3495(82)84663-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Mannella C. A., Bonner W. D., Jr X-ray diffraction from oriented outer mitochondrial membranes. Detection of in-plane subunit structure. Biochim Biophys Acta. 1975 Dec 1;413(2):226–233. doi: 10.1016/0005-2736(75)90106-6. [DOI] [PubMed] [Google Scholar]
  9. Mannella C. A., Frank J. Effects of divalent metal ions and chelators on the structure of outer mitochondrial membranes from neurospora crassa. Biophys J. 1982 Jan;37(1):3–4. doi: 10.1016/S0006-3495(82)84569-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Mannella C. A. Structure of the outer mitochondrial membrane: ordered arrays of porelike subunits in outer-membrane fractions from Neurospora crassa mitochondria. J Cell Biol. 1982 Sep;94(3):680–687. doi: 10.1083/jcb.94.3.680. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Montal M., Mueller P. Formation of bimolecular membranes from lipid monolayers and a study of their electrical properties. Proc Natl Acad Sci U S A. 1972 Dec;69(12):3561–3566. doi: 10.1073/pnas.69.12.3561. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. O'Brien R. L., Brierley G. Compartmentation of heart mitochondria. I. Permeability characteristics of isolated beef heart mitochondria. J Biol Chem. 1965 Nov;240(11):4527–4531. [PubMed] [Google Scholar]
  13. Parsons D. F., Williams G. R., Chance B. Characteristics of isolated and purified preparations of the outer and inner membranes of mitochondria. Ann N Y Acad Sci. 1966 Jul 14;137(2):643–666. doi: 10.1111/j.1749-6632.1966.tb50188.x. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Rose I. A., Warms J. V. Mitochondrial hexokinase. Release, rebinding, and location. J Biol Chem. 1967 Apr 10;242(7):1635–1645. [PubMed] [Google Scholar]
  16. Schein S. J., Colombini M., Finkelstein A. Reconstitution in planar lipid bilayers of a voltage-dependent anion-selective channel obtained from paramecium mitochondria. J Membr Biol. 1976 Dec 28;30(2):99–120. doi: 10.1007/BF01869662. [DOI] [PubMed] [Google Scholar]
  17. Schindler H., Rosenbusch J. P. Matrix protein from Escherichia coli outer membranes forms voltage-controlled channels in lipid bilayers. Proc Natl Acad Sci U S A. 1978 Aug;75(8):3751–3755. doi: 10.1073/pnas.75.8.3751. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Steven A. C., Heggeler B., Müller R., Kistler J., Rosenbusch J. P. Ultrastructure of a periodic protein layer in the outer membrane of Escherichia coli. J Cell Biol. 1977 Feb;72(2):292–301. doi: 10.1083/jcb.72.2.292. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Unwin P. N., Zampighi G. Structure of the junction between communicating cells. Nature. 1980 Feb 7;283(5747):545–549. doi: 10.1038/283545a0. [DOI] [PubMed] [Google Scholar]
  20. WERKHEISER W. C., BARTLEY W. The study of steady-state concentrations of internal solutes of mitochondria by rapid centrifugal transfer to a fixation medium. Biochem J. 1957 May;66(1):79–91. doi: 10.1042/bj0660079. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Zalman L. S., Nikaido H., Kagawa Y. Mitochondrial outer membrane contains a protein producing nonspecific diffusion channels. J Biol Chem. 1980 Mar 10;255(5):1771–1774. [PubMed] [Google Scholar]
  22. Zampighi G., Unwin P. N. Two forms of isolated gap junctions. J Mol Biol. 1979 Dec 5;135(2):451–464. doi: 10.1016/0022-2836(79)90446-7. [DOI] [PubMed] [Google Scholar]

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