Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1982 Nov 1;95(2):672–675. doi: 10.1083/jcb.95.2.672

Redistribution of proteins of fast axonal transport following administration of beta,beta'-iminodipropionitrile: a quantitative autoradiographic study

PMCID: PMC2112962  PMID: 6183280

Abstract

Beta,beta'-iminodipropionitrile (IDPN) produces a rearrangement of axoplasmic organelles with displacement of microtubules, smooth endoplasmic reticulum, and mitochondria toward the center and of neurofilaments toward the periphery of the axon, whereas the rate of the fast component of axonal transport is unchanged. Separation of microtubules and neurofilaments makes the IDPN axons an excellent model for study of the role of these two organelles in axonal transport. The cross-sectional distribution of [3H]-labeled proteins moving with the front of the fast transport was analyzed by quantitative electron microscopic autoradiography in sciatic nerves of IDPN-treated and control rats, 6 h after injection of a 1:1 mixture of [3H]-proline and [3H]-lysine into lumbar ventral horns. In IDPN axons most of the transported [3H] proteins were located in the central region with microtubules, smooth endoplasmic reticulum and mitochondria, whereas few or none were in the periphery with neurofilaments. In control axons the [3H]-labeled proteins were uniformly distributed within the axoplasm. It is concluded that in fast axonal transport: (a) neurofilaments play no primary role; (b) the normal architecture of the axonal cytoskeleton and the normal cross-sectional distribution of transported materials are not indispensable for the maintenance of a normal rate of transport. The present findings are consistent with the models of fast transport that envision microtubules as the key organelles in providing directionality and propulsive force to the fast component of axonal transport.

Full Text

The Full Text of this article is available as a PDF (1.1 MB).

Selected References

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

  1. Ball E. H., Singer S. J. Mitochondria are associated with microtubules and not with intermediate filaments in cultured fibroblasts. Proc Natl Acad Sci U S A. 1982 Jan;79(1):123–126. doi: 10.1073/pnas.79.1.123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Brady S. T., Crothers S. D., Nosal C., McClure W. O. Fast axonal transport in the presence of high Ca2+: evidence that microtubules are not required. Proc Natl Acad Sci U S A. 1980 Oct;77(10):5909–5913. doi: 10.1073/pnas.77.10.5909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brady S. T., Lasek R. J. Nerve-specific enolase and creatine phosphokinase in axonal transport: soluble proteins and the axoplasmic matrix. Cell. 1981 Feb;23(2):515–523. doi: 10.1016/0092-8674(81)90147-1. [DOI] [PubMed] [Google Scholar]
  4. Brimijoin S. Microtubules and the capacity of the system for rapid axonal transport. Fed Proc. 1982 May;41(7):2312–2316. [PubMed] [Google Scholar]
  5. Byers M. R. Structural correlates of rapid axonal transport: evidence that microtubules may not be directly involved. Brain Res. 1974 Jul 19;75(1):97–113. doi: 10.1016/0006-8993(74)90773-2. [DOI] [PubMed] [Google Scholar]
  6. Chretien M., Patey G., Souyri F., Droz B. 'Acrylamide-induced' neuropathy and impairment of axonal transport of proteins. II. Abnormal accumulations of smooth endoplasmic reticulum as sites of focal retention of fast transported proteins. Electron microscope radioautographic study. Brain Res. 1981 Jan 26;205(1):15–28. doi: 10.1016/0006-8993(81)90716-2. [DOI] [PubMed] [Google Scholar]
  7. Eckert B. S., Koons S. J., Schantz A. W., Zobel C. R. Association of creatine phosphokinase with the cytoskeleton of cultured mammalian cells. J Cell Biol. 1980 Jul;86(1):1–5. doi: 10.1083/jcb.86.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Ellisman M. H., Porter K. R. Microtrabecular structure of the axoplasmic matrix: visualization of cross-linking structures and their distribution. J Cell Biol. 1980 Nov;87(2 Pt 1):464–479. doi: 10.1083/jcb.87.2.464. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gambetti P., Autilio-Gambetti L. A., Gonatas N. K., Shafer B. Protein synthesis in synaptosomal fractions. Ultrastructural radioautographic study. J Cell Biol. 1972 Mar;52(3):526–535. doi: 10.1083/jcb.52.3.526. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Grafstein B., Forman D. S. Intracellular transport in neurons. Physiol Rev. 1980 Oct;60(4):1167–1283. doi: 10.1152/physrev.1980.60.4.1167. [DOI] [PubMed] [Google Scholar]
  11. Gross G. W. The microstream concept of axoplasmic and dendritic transport. Adv Neurol. 1975;12:283–296. [PubMed] [Google Scholar]
  12. Lasek R. J. Axoplasmic transport of labeled proteins in rat ventral motoneurons. Exp Neurol. 1968 May;21(1):41–51. doi: 10.1016/0014-4886(68)90032-0. [DOI] [PubMed] [Google Scholar]
  13. Ochs S. Calcium and the mechanism of axoplasmic transport. Fed Proc. 1982 May;41(7):2301–2306. [PubMed] [Google Scholar]
  14. Papasozomenos S. C., Autilio-Gambetti L., Gambetti P. Reorganization of axoplasmic organelles following beta, beta'-iminodipropionitrile administration. J Cell Biol. 1981 Dec;91(3 Pt 1):866–871. doi: 10.1083/jcb.91.3.866. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Pollard T. D. Which organelles are necessary for fast neuronal transport? Neurosci Res Program Bull. 1981 Oct;20(1):92–97. [PubMed] [Google Scholar]
  16. Rambourg A., Droz B. Smooth endoplasmic reticulum and axonal transport. J Neurochem. 1980 Jul;35(1):16–25. doi: 10.1111/j.1471-4159.1980.tb12484.x. [DOI] [PubMed] [Google Scholar]
  17. Salpeter M. M., Bachmann L., Salpeter E. E. Resolution in electron microscope radioautography. J Cell Biol. 1969 Apr;41(1):1–32. doi: 10.1083/jcb.41.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Schwartz J. H. Axonal transport: components, mechanisms, and specificity. Annu Rev Neurosci. 1979;2:467–504. doi: 10.1146/annurev.ne.02.030179.002343. [DOI] [PubMed] [Google Scholar]
  19. Souyri F., Chretien M., Droz B. 'Acrylamide-induced' neuropathy and impairment of axonal transport of proteins. I. Multifocal retention of fast transported proteins at the periphery of axons as revealed by light microscope radioautography. Brain Res. 1981 Jan 26;205(1):1–13. doi: 10.1016/0006-8993(81)90715-0. [DOI] [PubMed] [Google Scholar]
  20. Stearns M. E. High voltage electron microscopy studies of axoplasmic transport in neurons: a possible regulatory role for divalent cations. J Cell Biol. 1982 Mar;92(3):765–776. doi: 10.1083/jcb.92.3.765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Tessler A., Autilio-Gambetti A., Gambetti P. Axonal growth during regeneration: a quantitative autoradiographic study. J Cell Biol. 1980 Oct;87(1):197–203. doi: 10.1083/jcb.87.1.197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. The role of fast transport in the nervous system. Neurosci Res Program Bull. 1981 Oct;20(1):1–138. [PubMed] [Google Scholar]
  23. Tytell M., Black M. M., Garner J. A., Lasek R. J. Axonal transport: each major rate component reflects the movement of distinct macromolecular complexes. Science. 1981 Oct 9;214(4517):179–181. doi: 10.1126/science.6169148. [DOI] [PubMed] [Google Scholar]
  24. Willard M., Simon C. Antibody decoration of neurofilaments. J Cell Biol. 1981 May;89(2):198–205. doi: 10.1083/jcb.89.2.198. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Wolosewick J. J., Porter K. R. Microtrabecular lattice of the cytoplasmic ground substance. Artifact or reality. J Cell Biol. 1979 Jul;82(1):114–139. doi: 10.1083/jcb.82.1.114. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Wolosewick J. J., Porter K. R. Stereo high-voltage electron microscopy of whole cells of the human diploid line, WI-38. Am J Anat. 1976 Nov;147(3):303–323. doi: 10.1002/aja.1001470305. [DOI] [PubMed] [Google Scholar]

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

RESOURCES