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. 1969 Oct 1;43(1):148–165. doi: 10.1083/jcb.43.1.148

STUDIES ON THE MICROTUBULES IN HELIOZOA

V. Factors Controlling the Organization of Microtubules in the Axonemal Pattern in Echinosphaerium (Actinosphaerium) nucleofilum

Lewis G Tilney 1, Breck Byers 1
PMCID: PMC2107851  PMID: 5824062

Abstract

On the assumption that the double-coiled pattern of microtubules in the axoneme of Echinosphaerium might be due to links of two sizes between adjacent microtubules, we disassembled microtubules with low temperature and then carefully analyzed the patterns of microtubules that formed upon the addition of heat (22°C) or heat and D2O. Although most of the initial clusters of microtubules that formed could not be interpreted as part of an axoneme, the spacings between these microtubules were the same as that in the axoneme, 70 and 300 A. By model building we were able to show that all clusters that form, including stages in the formation of the axoneme and its 12-fold symmetry, could be explained by links of two sizes (70 and 300 A) and the substructure of the microtubule. We could demonstrate these links with improved staining methods. We suggest that nonaxonemal assemblies of microtubules may be eliminated by the natural selection of the most energetically stable configuration of microtubules, all others undergoing disassembly under equilibrium conditions. Model building further supports this suggestion since the model axoneme possesses more links per tubule than any other cluster found.

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Selected References

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

  1. Allen R. D. Fine structure, reconstruction and possible functions of components of the cortex of Tetrahymena pyriformis. J Protozool. 1967 Nov;14(4):553–565. doi: 10.1111/j.1550-7408.1967.tb02042.x. [DOI] [PubMed] [Google Scholar]
  2. Anderson E., Dumont J. N. A comparative study of the concrement vacuole of certain endocommensal ciliates--a so-called mechanoreceptor. J Ultrastruct Res. 1966 Jun;15(3):414–450. doi: 10.1016/s0022-5320(66)80117-x. [DOI] [PubMed] [Google Scholar]
  3. BYERS B., PORTER K. R. ORIENTED MICROTUBULES IN ELONGATING CELLS OF THE DEVELOPING LENS RUDIMENT AFTER INDUCTION. Proc Natl Acad Sci U S A. 1964 Oct;52:1091–1099. doi: 10.1073/pnas.52.4.1091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. GIBBONS I. R. The relationship between the fine structure and direction of beat in gill cilia of a lamellibranch mollusc. J Biophys Biochem Cytol. 1961 Oct;11:179–205. doi: 10.1083/jcb.11.1.179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. GRIMSTONE A. V., CLEVELAND L. R. THE FINE STRUCTURE AND FUNCTION OF THE CONTRACTILE AXOSTYLES OF CERTAIN FLAGELLATES. J Cell Biol. 1965 Mar;24:387–400. doi: 10.1083/jcb.24.3.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Gall J. G. Microtubule fine structure. J Cell Biol. 1966 Dec;31(3):639–643. doi: 10.1083/jcb.31.3.639. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gibbins J. R., Tilney L. G., Porter K. R. Microtubules in the formation and development of the primary mesenchyme in Arbacia punctulata. I. The distribution of microtubules. J Cell Biol. 1969 Apr;41(1):201–226. doi: 10.1083/jcb.41.1.201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Grim J. N. Ultrastructure of pellicular and ciliary structures of Euplotes eurystomus. J Protozool. 1967 Nov;14(4):625–633. doi: 10.1111/j.1550-7408.1967.tb02052.x. [DOI] [PubMed] [Google Scholar]
  9. Grimstone A. V., Klug A. Observations on the substructure of flagellar fibres. J Cell Sci. 1966 Sep;1(3):351–362. doi: 10.1242/jcs.1.3.351. [DOI] [PubMed] [Google Scholar]
  10. Inoué S., Sato H. Cell motility by labile association of molecules. The nature of mitotic spindle fibers and their role in chromosome movement. J Gen Physiol. 1967 Jul;50(6 Suppl):259–292. [PMC free article] [PubMed] [Google Scholar]
  11. Kessel R. G. The association between microtubules and nuclei during spermiogenesis in the dragonfly. J Ultrastruct Res. 1966 Oct;16(3):293–304. doi: 10.1016/s0022-5320(66)80064-3. [DOI] [PubMed] [Google Scholar]
  12. Kiefer B., Sakai H., Solari A. J., Mazia D. The molecular unit of the microtubules of the mitotic apparatus. J Mol Biol. 1966 Sep;20(1):75–79. doi: 10.1016/0022-2836(66)90118-5. [DOI] [PubMed] [Google Scholar]
  13. Ledbetter M. C., Porter K. R. Morphology of Microtubules of Plant Cell. Science. 1964 May 15;144(3620):872–874. doi: 10.1126/science.144.3620.872. [DOI] [PubMed] [Google Scholar]
  14. McIntosh J. R., Porter K. R. Microtubules in the spermatids of the domestic fowl. J Cell Biol. 1967 Oct;35(1):153–173. doi: 10.1083/jcb.35.1.153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. PEASE D. C. THE ULTRASTRUCTURE OF FLAGELLAR FIBRILS. J Cell Biol. 1963 Aug;18:313–326. doi: 10.1083/jcb.18.2.313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Palay S. L., Sotelo C., Peters A., Orkand P. M. The axon hillock and the initial segment. J Cell Biol. 1968 Jul;38(1):193–201. doi: 10.1083/jcb.38.1.193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. ROTH L. E., SHIGENAKA Y. THE STRUCTURE AND FORMATION OF CILIA AND FILAMENTS IN RUMEN PROTOZOA. J Cell Biol. 1964 Feb;20:249–270. doi: 10.1083/jcb.20.2.249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Rudzinska M. A. The fine structure and function of the tentacle in Tokophrya infusionum. J Cell Biol. 1965 Jun;25(3):459–477. doi: 10.1083/jcb.25.3.459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. SOMMER J. R., BLUM J. J. PELLICULAR CHANGES DURING DIVISION IN ASTASIA LONGA. Exp Cell Res. 1964 Jul;35:423–425. doi: 10.1016/0014-4827(64)90110-7. [DOI] [PubMed] [Google Scholar]
  20. Tilney L. G., Hiramoto Y., Marsland D. Studies on the microtubules in heliozoa. 3. A pressure analysis of the role of these structures in the formation and maintenance of the axopodia of Actinosphaerium nucleofilum (Barrett). J Cell Biol. 1966 Apr;29(1):77–95. doi: 10.1083/jcb.29.1.77. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Tilney L. G., Porter K. R. Studies on microtubules in Heliozoa. I. The fine structure of Actinosphaerium nucleofilum (Barrett), with particular reference to the axial rod structure. Protoplasma. 1965;60(4):317–344. doi: 10.1007/BF01247886. [DOI] [PubMed] [Google Scholar]
  22. Tilney L. G., Porter K. R. Studies on the microtubules in heliozoa. II. The effect of low temperature on these structures in the formation and maintenance of the axopodia. J Cell Biol. 1967 Jul;34(1):327–343. doi: 10.1083/jcb.34.1.327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Tilney L. G. Studies on the microtubules in heliozoa. IV. The effect of colchicine on the formation and maintenance of the axopodia and the redevelopment of pattern in Actinosphaerium nucleofilum (Barrett). J Cell Sci. 1968 Dec;3(4):549–562. doi: 10.1242/jcs.3.4.549. [DOI] [PubMed] [Google Scholar]
  24. Tucker J. B. Fine structure and function of the cytopharyngeal basket in the ciliate Nassula. J Cell Sci. 1968 Dec;3(4):493–514. doi: 10.1242/jcs.3.4.493. [DOI] [PubMed] [Google Scholar]
  25. Watters C. Studies on the motility of the Heliozoa. I. The locomotion of Actinosphaerium eichhorni and Actinophrys sp. J Cell Sci. 1968 Jun;3(2):231–244. doi: 10.1242/jcs.3.2.231. [DOI] [PubMed] [Google Scholar]

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