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. 1981 Jun 1;89(3):579–584. doi: 10.1083/jcb.89.3.579

Axonal transport of the mitochondria-specific lipid, diphosphatidylglycerol, in the rat visual system

PMCID: PMC2111787  PMID: 6166617

Abstract

Rats 24 d old were injected intraocularly with [2-3H]glycerol and [35S]methionine and killed 1 h-60 d later. 35S label in protein and 3H label in total phospholipid and a mitochondria-specific lipid, diphosphatidylglycerol(DPG), were determined in optic pathway structures (retinas, optic nerves, optic tracts, lateral geniculate bodies, and superior colliculi). Incorporation of label into retinal protein and phospholipid was nearly maximal 1 h postinjection, after which the label appeared in successive optic pathway structures. Based on the time difference between the arrival of label in the optic tract and superior colliculus, it was calculated that protein and phospholipid were transported at a rate of about 400 mm/d, and DPG at about half this rate. Transported labeled phospholipid and DPG, which initially comprised 3-5% of the lipid label, continued to accumulate in the visual structures for 6-8 d postinjection. The distribution of transported material among the optic pathway structures as a function of time differed markedly for different labeled macromolecules. Rapidly transported proteins distributed preferentially to the nerve endings (superior colliculus and lateral geniculate). Total phospholipid quickly established a pattern of comparable labeling of axon (optic nerve and tract) and nerve endings. In contrast, the distribution of transported labeled DPG gradually shifted toward the nerve ending and stabilized by 2-4 d. A model is proposed in which apparent "transport" of mitochondria is actually the result of random bidirectional saltatory movements of individual mitochondria which equilibrate them among cell body, axon, and nerve ending pools.

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Selected References

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  1. Banks P., Mangnall D., Mayor D. The re-distribution of cytochrome oxidase, noradrenaline and adenosine triphosphate in adrenergic nerves constricted at two points. J Physiol. 1969 Feb;200(3):745–762. doi: 10.1113/jphysiol.1969.sp008720. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Blaker W. D., Toews A. D., Morell P. Cholesterol is a component of the rapid phase of axonal transport. J Neurobiol. 1980 May;11(3):243–250. doi: 10.1002/neu.480110303. [DOI] [PubMed] [Google Scholar]
  3. Breckenridge W. C., Gombos G., Morgan I. G. The lipid composition of adult rat brain synaptosomal plasma membranes. Biochim Biophys Acta. 1972 Jun 20;266(3):695–707. doi: 10.1016/0006-3002(72)90012-1. [DOI] [PubMed] [Google Scholar]
  4. Breckenridge W. C., Morgan I. G., Zanetta J. P., Vincendon G. Adult rat brain synaptic vesicles. II. Lipid composition. Biochim Biophys Acta. 1973 Oct 5;320(3):681–686. doi: 10.1016/0304-4165(73)90148-7. [DOI] [PubMed] [Google Scholar]
  5. Breuer A. C., Christian C. N., Henkart M., Nelson P. G. Computer analysis of organelle translocation in primary neuronal cultures and continuous cell lines. J Cell Biol. 1975 Jun;65(3):562–576. doi: 10.1083/jcb.65.3.562. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cancalon P., Beidler L. M. Distribution along the axon and into various subcellular fractions of molecules labeled with (3H)leucine and rapidly transported in the garfish olfactory nerve. Brain Res. 1975 May 23;89(2):225–244. doi: 10.1016/0006-8993(75)90715-5. [DOI] [PubMed] [Google Scholar]
  7. Cancalon P. Subcellular and polypeptide distributions of slowly transported proteins in the garfish olfactory nerve. Brain Res. 1979 Jan 26;161(1):115–130. doi: 10.1016/0006-8993(79)90199-9. [DOI] [PubMed] [Google Scholar]
  8. Cooper P. D., Smith R. S. The movement of optically detectable organelles in myelinated axons of Xenopus laevis. J Physiol. 1974 Oct;242(1):77–97. doi: 10.1113/jphysiol.1974.sp010695. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cuénod M., Schonbach J. Synaptic proteins and axonal flow in the pigeon visual pathway. J Neurochem. 1971 Jun;18(6):809–816. doi: 10.1111/j.1471-4159.1971.tb12010.x. [DOI] [PubMed] [Google Scholar]
  10. Davidson J. B., Stanacev N. Z. Biosynthesis of cardiolipin in mitochondria. Can J Biochem. 1971 Oct;49(10):1117–1124. doi: 10.1139/o71-161. [DOI] [PubMed] [Google Scholar]
  11. Droz B., Koenig H. L., Biamberardino L. D., Di Giamberardino L. Axonal migration of protein and glycoprotein to nerve endings. I. Radioautographic analysis of the renewal of protein in nerve endings of chicken ciliary ganglion after intracerebral injection of (3H)lysine. Brain Res. 1973 Sep 28;60(1):93–127. doi: 10.1016/0006-8993(73)90852-4. [DOI] [PubMed] [Google Scholar]
  12. Eichberg J., Whittaker V. P., Dawson R. M. Distribution of lipids in subcellular particles of guinea-pig brain. Biochem J. 1964 Jul;92(1):91–100. doi: 10.1042/bj0920091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Forman D. S., Padjen A. L., Siggins G. R. Axonal transport of organelles visualized by light microscopy: cinemicrographic and computer analysis. Brain Res. 1977 Nov 11;136(2):197–213. doi: 10.1016/0006-8993(77)90798-3. [DOI] [PubMed] [Google Scholar]
  14. Getz G. S., Bartley W., Lurie D., Notton B. M. The phospholipids of various sheep organs, rat liver and of their subcellular fractions. Biochim Biophys Acta. 1968 Mar 4;152(2):325–339. doi: 10.1016/0005-2760(68)90040-4. [DOI] [PubMed] [Google Scholar]
  15. Goodrum J. F., Toews A. D., Morell P. Axonal transport and metabolism of [3H]fucose- and [35S]-sulfate-labeled macromolecules in the rat visual system. Brain Res. 1979 Nov 2;176(2):255–272. doi: 10.1016/0006-8993(79)90982-x. [DOI] [PubMed] [Google Scholar]
  16. Haley J. E., Ledeen R. W. Incorporation of axonally transported substances into myelin lipids. J Neurochem. 1979 Mar;32(3):735–742. doi: 10.1111/j.1471-4159.1979.tb04556.x. [DOI] [PubMed] [Google Scholar]
  17. Hostetler K. Y., van den Bosch H. Subcellular and submitochondrial localization of the biosynthesis of cardiolipin and related phospholipids in rat liver. Biochim Biophys Acta. 1972 Mar 23;260(3):380–386. doi: 10.1016/0005-2760(72)90052-5. [DOI] [PubMed] [Google Scholar]
  18. Jeffrey P. L., James K. A., Kidman A. D., Richards A. M., Austin L. The flow of mitochondria in chicken sciatic nerve. J Neurobiol. 1972;3(3):199–208. doi: 10.1002/neu.480030303. [DOI] [PubMed] [Google Scholar]
  19. Karlsson J. O., Sjöstrand J. Synthesis, migration and turnover of protein in retinal ganglion cells. J Neurochem. 1971 May;18(5):749–767. doi: 10.1111/j.1471-4159.1971.tb12005.x. [DOI] [PubMed] [Google Scholar]
  20. Khan M. A., Ochs S. Slow axoplasmic transport of mitochondria (MAO) and lactic dehydrogenase in mammalian nerve fibers. Brain Res. 1975 Oct 17;96(2):267–277. doi: 10.1016/0006-8993(75)90735-0. [DOI] [PubMed] [Google Scholar]
  21. Kirkpatrick J. B., Bray J. J., Palmer S. M. Visualization of axoplasmic flow in vitro by Nomarski microscopy. Comparison to rapid flow of radioactive proteins. Brain Res. 1972 Aug 11;43(1):1–10. doi: 10.1016/0006-8993(72)90270-3. [DOI] [PubMed] [Google Scholar]
  22. Leestma J. E., Freeman S. S. Computer-assisted analysis of particulate axoplasmic flow in organized CNS tissue cultures. J Neurobiol. 1977 Sep;8(5):453–467. doi: 10.1002/neu.480080506. [DOI] [PubMed] [Google Scholar]
  23. Lorenz T., Willard M. Subcellular fractionation of intra-axonally transport polypeptides in the rabbit visual system. Proc Natl Acad Sci U S A. 1978 Jan;75(1):505–509. doi: 10.1073/pnas.75.1.505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. McMurray W. C., Dawson R. M. Phospholipid exchange reactions within the liver cell. Biochem J. 1969 Mar;112(1):91–108. doi: 10.1042/bj1120091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Miller E. K., Dawson R. M. Can mitochondria and synaptosomes of guinea-pig brain synthesize phospholipids? Biochem J. 1972 Feb;126(4):805–821. doi: 10.1042/bj1260805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Miller E. K., Dawson R. M. Exchange of phospholipids between brain membranes in vitro. Biochem J. 1972 Feb;126(4):823–835. doi: 10.1042/bj1260823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Miller S. L., Benjamins J. A., Morell P. Metabolism of glycerophospholipids of myelin and microsomes in rat brain. Reutilization of precursors. J Biol Chem. 1977 Jun 25;252(12):4025–4037. [PubMed] [Google Scholar]
  28. Ochs S. Retention and redistribution of proteins in mammalian nerve fibres by axoplasmic transport. J Physiol. 1975 Dec;253(2):459–475. doi: 10.1113/jphysiol.1975.sp011200. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Ochs S. Trophic functions of the neuron. 3. Mechanisms of neurotrophic interactions. Systems of material transport in nerve fibers (axoplasmic transport) related to nerve function and trophic control. Ann N Y Acad Sci. 1974 Mar 22;228(0):202–223. doi: 10.1111/j.1749-6632.1974.tb20511.x. [DOI] [PubMed] [Google Scholar]
  30. Partlow L. M., Ross C. D., Motwani R., McDougal D. B., Jr Transport of axonal enzymes in surviving segments of frog sciatic nerve. J Gen Physiol. 1972 Oct;60(4):388–405. doi: 10.1085/jgp.60.4.388. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Paulson J. C., McClure W. O. Microtubules and axoplasmic transport. Brain Res. 1974 Jun 20;73(2):333–337. doi: 10.1016/0006-8993(74)91053-1. [DOI] [PubMed] [Google Scholar]
  32. Schlichter D. J., McClure W. O. Dynamics of axoplasmic transport in the optic system of the rat. Exp Brain Res. 1974;21(1):83–95. doi: 10.1007/BF00234259. [DOI] [PubMed] [Google Scholar]
  33. Schonbach J., Schonbach C., Cuénod M. Distribution of transported proteins in the slow phase of axoplasmic flow. An electron microscopical autoradiographic study. J Comp Neurol. 1973 Nov 1;152(1):1–16. doi: 10.1002/cne.901520102. [DOI] [PubMed] [Google Scholar]
  34. Schonbach J., Schonbach C., Cuénoid M. Rapid phase of axoplasmic flow and synaptic proteins: an electron microscopical autoradiographic study. J Comp Neurol. 1971 Apr;141(4):485–497. doi: 10.1002/cne.901410406. [DOI] [PubMed] [Google Scholar]
  35. Smith R. S. Detection of organelles in myelinated nerve fibers by dark-field microscopy. Can J Physiol Pharmacol. 1972 May;50(5):467–469. doi: 10.1139/y72-071. [DOI] [PubMed] [Google Scholar]
  36. Stoffel W., Schiefer H. G. Biosynthesis and composition of phosphatides in outer and inner mitochondrial membranes. Hoppe Seylers Z Physiol Chem. 1968 Aug;349(8):1017–1026. doi: 10.1515/bchm2.1968.349.2.1017. [DOI] [PubMed] [Google Scholar]
  37. Tamai Y., Araki S. M., Katsuta K., Satake M. Molecular composition of the submicrosomal membrane lipid of rat brain. J Cell Biol. 1974 Dec;63(3):749–758. doi: 10.1083/jcb.63.3.749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Tamir H., Rapport M. M., Roizin L., Huang Y. L., Liu J. C. Preparation of synaptosomes and vesicles with sodium diatrizoate. J Neurochem. 1974 Nov;23(5):943–949. doi: 10.1111/j.1471-4159.1974.tb10746.x. [DOI] [PubMed] [Google Scholar]
  39. Wiggins R. C., Miller S. L., Benjamins J. A., Krigman M. R., Morell P. Myelin synthesis during postnatal nutritional deprivation and subsequent rehabilitation. Brain Res. 1976 May 7;107(2):257–273. doi: 10.1016/0006-8993(76)90225-0. [DOI] [PubMed] [Google Scholar]
  40. Willard M., Cowan W. M., Vagelos P. R. The polypeptide composition of intra-axonally transported proteins: evidence for four transport velocities. Proc Natl Acad Sci U S A. 1974 Jun;71(6):2183–2187. doi: 10.1073/pnas.71.6.2183. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Wuthier R. E. Two-dimensional chromatography on silica gel-loaded paper for the microanalysis of polar lipids. J Lipid Res. 1966 Jul;7(4):544–550. [PubMed] [Google Scholar]

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