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. 1984 Aug 1;99(2):520–528. doi: 10.1083/jcb.99.2.520

Luminal material in microtubules of frog olfactory axons: structure and distribution

PMCID: PMC2113267  PMID: 6430914

Abstract

The substructure and distribution of luminal material in microtubules of olfactory axons were studied in the bullfrog, Rana catesbeiana. By using numerous fixation methods, with and without osmium tetroxide, the luminal component was shown not to be an artifact of fixation. The material consists of globular elements 4-5 nm in diameter loosely arranged within the lumen in a discontinuous column. Counts of microtubules showing luminal material were obtained for axons in the proximal and distal ends of the olfactory nerve, and it was found that 16-18% more of the microtubules in the distal regions showed the luminal component. This raises the possibility that the material might be translocated within the microtubule lumen and tends to accumulate as it moves distally toward the axon terminal. In contrast to those of the olfactory axons, microtubules assembled in vitro from frog brain tubulin did not show luminal material. When microtubules in olfactory axons were depolymerized in situ by cold and calcium treatment and then induced to reassemble, most of those that were formed de novo showed empty lumina. Such evidence suggests that the luminal material is not an integral component of the microtubule. The hypothesis is discussed that material may be translocated within the lumina of microtubules. Furthermore, in the case of neuronal microtubules, the possibility is raised that they may serve as conduits for their own wall subunits.

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Selected References

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  1. Bassot J. M., Martoja R. Données histologiques et ultrastructurales sur les microtubules cytoplasmiques du canal éjaculateur des insectes orthoptères. Z Zellforsch Mikrosk Anat. 1966;74(2):145–181. [PubMed] [Google Scholar]
  2. Behnke O. Incomplete microtubules observed in mammalian blood platelets during microtubule polymerization. J Cell Biol. 1967 Aug;34(2):697–701. doi: 10.1083/jcb.34.2.697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bray D., Bunge M. B. Serial analysis of microtubules in cultured rat sensory axons. J Neurocytol. 1981 Aug;10(4):589–605. doi: 10.1007/BF01262592. [DOI] [PubMed] [Google Scholar]
  4. Burton P. R., Paige J. L. Polarity of axoplasmic microtubules in the olfactory nerve of the frog. Proc Natl Acad Sci U S A. 1981 May;78(5):3269–3273. doi: 10.1073/pnas.78.5.3269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Caveney S. Muscle attachment related to cuticle architecture in Apterygota. J Cell Sci. 1969 Mar;4(2):541–559. doi: 10.1242/jcs.4.2.541. [DOI] [PubMed] [Google Scholar]
  6. Chalfie M., Thomson J. N. Organization of neuronal microtubules in the nematode Caenorhabditis elegans. J Cell Biol. 1979 Jul;82(1):278–289. doi: 10.1083/jcb.82.1.278. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dahlström A. Effect of colchicine on transport of amine storage granules in sympathetic nerves of rat. Eur J Pharmacol. 1968 Dec;5(1):111–113. doi: 10.1016/0014-2999(68)90165-9. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Griffin J. W., Fahnestock K. E., Price D. L., Hoffman P. N. Microtubule-neurofilament segregation produced by beta, beta'-iminodipropionitrile: evidence for the association of fast axonal transport with microtubules. J Neurosci. 1983 Mar;3(3):557–566. doi: 10.1523/JNEUROSCI.03-03-00557.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gupta B. L., Berridge M. J. Fine structural organization of the rectum in the blowfly, Calliphora erythrocephala (Meig.) with special reference to connective tissue, tracheae and neurosecretory innervation in the rectal papillae. J Morphol. 1966 Sep;120(1):23–81. doi: 10.1002/jmor.1051200104. [DOI] [PubMed] [Google Scholar]
  11. Hama K. The fine structure of the Schwann cell sheath of the nerve fiber in the shrimp (Penaeus japonicus). J Cell Biol. 1966 Dec;31(3):624–632. doi: 10.1083/jcb.31.3.624. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hammond G. R., Smith R. S. Inhibition of the rapid movement of optically detectable axonal particles colchicine and vinblastine. Brain Res. 1977 Jun 10;128(2):227–242. doi: 10.1016/0006-8993(77)90990-8. [DOI] [PubMed] [Google Scholar]
  13. Hardham A. R., Gunning B. E. Structure of cortical microtubule arrays in plant cells. J Cell Biol. 1978 Apr;77(1):14–34. doi: 10.1083/jcb.77.1.14. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Heslop J. P. Axonal flow and fast transport in nerves. Adv Comp Physiol Biochem. 1975;6:75–163. doi: 10.1016/b978-0-12-011506-8.50008-1. [DOI] [PubMed] [Google Scholar]
  15. Himes R. H., Burton P. R., Gaito J. M. Dimethyl sulfoxide-induced self-assembly of tubulin lacking associated proteins. J Biol Chem. 1977 Sep 10;252(17):6222–6228. [PubMed] [Google Scholar]
  16. Himes R. H., Burton P. R., Kersey R. N., Pierson G. B. Brain tubulin polymerization in the absence of "microtubule-associated proteins". Proc Natl Acad Sci U S A. 1976 Dec;73(12):4397–4399. doi: 10.1073/pnas.73.12.4397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kreutzberg G. W. Neuronal dynamics and axonal flow. IV. Blockage of intra-axonal enzyme transport by colchicine. Proc Natl Acad Sci U S A. 1969 Mar;62(3):722–728. doi: 10.1073/pnas.62.3.722. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Moran D. T., Chapman K. M., Ellis R. A. The fine structure of cockroach campaniform sensilla. J Cell Biol. 1971 Jan;48(1):155–173. doi: 10.1083/jcb.48.1.155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Papasozomenos S. C., Yoon M., Crane R., Autilio-Gambetti L., Gambetti P. Redistribution of proteins of fast axonal transport following administration of beta,beta'-iminodipropionitrile: a quantitative autoradiographic study. J Cell Biol. 1982 Nov;95(2 Pt 1):672–675. doi: 10.1083/jcb.95.2.672. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Peters A., Proskauer C. C., Kaiserman-Abramof I. R. The small pyramidal neuron of the rat cerebral cortex. The axon hillock and initial segment. J Cell Biol. 1968 Dec;39(3):604–619. doi: 10.1083/jcb.39.3.604. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Rieder C. L. Thick and thin serial sectioning for the three-dimensional reconstruction of biological ultrastructure. Methods Cell Biol. 1981;22:215–249. doi: 10.1016/s0091-679x(08)61879-8. [DOI] [PubMed] [Google Scholar]
  22. Rodríguez Echandía E. L., Piezzi R. S., Rodríguez E. M. Dense-core microtubules in neurons and gliocytes of the toad Bufo arenarum Hensel. Am J Anat. 1968 Jan;122(1):157–166. doi: 10.1002/aja.1001220110. [DOI] [PubMed] [Google Scholar]
  23. SLAUTTERBACK D. B. CYTOPLASMIC MICROTUBULES. I. HYDRA. J Cell Biol. 1963 Aug;18:367–388. doi: 10.1083/jcb.18.2.367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Sandborn E. B., LeBuis J. J., Bois P. Cytoplasmic microtubules in blood platelets. Blood. 1966 Feb;27(2):247–252. [PubMed] [Google Scholar]
  25. Shelanski M. L., Gaskin F., Cantor C. R. Microtubule assembly in the absence of added nucleotides. Proc Natl Acad Sci U S A. 1973 Mar;70(3):765–768. doi: 10.1073/pnas.70.3.765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Silver M. D., McKinstry J. E. Morphology of microtubules in rabbit platelets. Z Zellforsch Mikrosk Anat. 1967;81(1):12–17. doi: 10.1007/BF00344548. [DOI] [PubMed] [Google Scholar]
  27. Smith D. E. The location of neurofilaments and microtubules during the postnatal development of Clarke's nucleus in the kitten. Brain Res. 1973 May 30;55(1):41–53. doi: 10.1016/0006-8993(73)90487-3. [DOI] [PubMed] [Google Scholar]
  28. Smith D. S., Järlfors U., Beránek R. The organization of synaptic axcplasm in the lamprey (petromyzon marinus) central nervous system. J Cell Biol. 1970 Aug;46(2):199–219. doi: 10.1083/jcb.46.2.199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Specht S. C. Axonal transport in the optic system of neonatal and adult hamsters. Exp Neurol. 1977 Aug;56(2):252–264. doi: 10.1016/0014-4886(77)90345-4. [DOI] [PubMed] [Google Scholar]
  30. Stanley H. P., Bowman J. T., Romrell L. J., Reed S. C., Wilkinson R. F. Fine structure of normal spermatid differentiation in Drosophila melanogaster. J Ultrastruct Res. 1972 Dec;41(5):433–466. doi: 10.1016/s0022-5320(72)90049-4. [DOI] [PubMed] [Google Scholar]

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