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. 1987 Nov 1;105(5):2167–2177. doi: 10.1083/jcb.105.5.2167

Posttranslational modification and microtubule stability

PMCID: PMC2114866  PMID: 3316248

Abstract

We have probed the relationship between tubulin posttranslational modification and microtubule stability, using a variation of the antibody-blocking technique. In human retinoblastoma cells we find that acetylated and detyrosinated microtubules represent congruent subsets of the cells' total microtubules. We also find that stable microtubules defined as those that had not undergone polymerization within 1 h after injection of biotin-tubulin were all posttranslationally modified; furthermore dynamic microtubules were all unmodified. We therefore conclude that in these cells the stable, acetylated, and detyrosinated microtubules represent the same subset of the cells' total network. Posttranslational modification, however, is not a prerequisite for microtubule stability and vice versa. Potorous tridactylis kidney cells have no detectable acetylated microtubules but do have a sizable subset of stable ones, and chick embryo fibroblast cells are extensively modified but have few stable microtubules. We conclude that different cell types can create specific microtubule subsets by modulating the relative rates of posttranslational modification and microtubule turnover.

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Selected References

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  1. Binder L. I., Frankfurter A., Rebhun L. I. Differential localization of MAP-2 and tau in mammalian neurons in situ. Ann N Y Acad Sci. 1986;466:145–166. doi: 10.1111/j.1749-6632.1986.tb38392.x. [DOI] [PubMed] [Google Scholar]
  2. Blose S. H., Meltzer D. I., Feramisco J. R. 10-nm filaments are induced to collapse in living cells microinjected with monoclonal and polyclonal antibodies against tubulin. J Cell Biol. 1984 Mar;98(3):847–858. doi: 10.1083/jcb.98.3.847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bluestein H. G. Neurocytotoxic antibodies in serum of patients with systemic lupus erythematosus. Proc Natl Acad Sci U S A. 1978 Aug;75(8):3965–3969. doi: 10.1073/pnas.75.8.3965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1006/abio.1976.9999. [DOI] [PubMed] [Google Scholar]
  5. Geuens G., Gundersen G. G., Nuydens R., Cornelissen F., Bulinski J. C., DeBrabander M. Ultrastructural colocalization of tyrosinated and detyrosinated alpha-tubulin in interphase and mitotic cells. J Cell Biol. 1986 Nov;103(5):1883–1893. doi: 10.1083/jcb.103.5.1883. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Graessmann A., Graessmann M., Mueller C. Microinjection of early SV40 DNA fragments and T antigen. Methods Enzymol. 1980;65(1):816–825. doi: 10.1016/s0076-6879(80)65076-9. [DOI] [PubMed] [Google Scholar]
  7. Graessmann M., Graessman A. "Early" simian-virus-40-specific RNA contains information for tumor antigen formation and chromatin replication. Proc Natl Acad Sci U S A. 1976 Feb;73(2):366–370. doi: 10.1073/pnas.73.2.366. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gundersen G. G., Kalnoski M. H., Bulinski J. C. Distinct populations of microtubules: tyrosinated and nontyrosinated alpha tubulin are distributed differently in vivo. Cell. 1984 Oct;38(3):779–789. doi: 10.1016/0092-8674(84)90273-3. [DOI] [PubMed] [Google Scholar]
  9. Kemphues K. J., Kaufman T. C., Raff R. A., Raff E. C. The testis-specific beta-tubulin subunit in Drosophila melanogaster has multiple functions in spermatogenesis. Cell. 1982 Dec;31(3 Pt 2):655–670. doi: 10.1016/0092-8674(82)90321-x. [DOI] [PubMed] [Google Scholar]
  10. Kirschner M., Mitchison T. Beyond self-assembly: from microtubules to morphogenesis. Cell. 1986 May 9;45(3):329–342. doi: 10.1016/0092-8674(86)90318-1. [DOI] [PubMed] [Google Scholar]
  11. Kirschner M., Schulze E. Morphogenesis and the control of microtubule dynamics in cells. J Cell Sci Suppl. 1986;5:293–310. doi: 10.1242/jcs.1986.supplement_5.19. [DOI] [PubMed] [Google Scholar]
  12. Kristofferson D., Mitchison T., Kirschner M. Direct observation of steady-state microtubule dynamics. J Cell Biol. 1986 Mar;102(3):1007–1019. doi: 10.1083/jcb.102.3.1007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Maruta H., Greer K., Rosenbaum J. L. The acetylation of alpha-tubulin and its relationship to the assembly and disassembly of microtubules. J Cell Biol. 1986 Aug;103(2):571–579. doi: 10.1083/jcb.103.2.571. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Matus A., Bernhardt R., Bodmer R., Alaimo D. Microtubule-associated protein 2 and tubulin are differently distributed in the dendrites of developing neurons. Neuroscience. 1986 Feb;17(2):371–389. doi: 10.1016/0306-4522(86)90253-8. [DOI] [PubMed] [Google Scholar]
  15. Mitchison T. J., Kirschner M. W. Properties of the kinetochore in vitro. II. Microtubule capture and ATP-dependent translocation. J Cell Biol. 1985 Sep;101(3):766–777. doi: 10.1083/jcb.101.3.766. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Mitchison T., Kirschner M. Microtubule assembly nucleated by isolated centrosomes. Nature. 1984 Nov 15;312(5991):232–237. doi: 10.1038/312232a0. [DOI] [PubMed] [Google Scholar]
  17. Piperno G., Fuller M. T. Monoclonal antibodies specific for an acetylated form of alpha-tubulin recognize the antigen in cilia and flagella from a variety of organisms. J Cell Biol. 1985 Dec;101(6):2085–2094. doi: 10.1083/jcb.101.6.2085. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Piperno G., LeDizet M., Chang X. J. Microtubules containing acetylated alpha-tubulin in mammalian cells in culture. J Cell Biol. 1987 Feb;104(2):289–302. doi: 10.1083/jcb.104.2.289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Raybin D., Flavin M. Modification of tubulin by tyrosylation in cells and extracts and its effect on assembly in vitro. J Cell Biol. 1977 May;73(2):492–504. doi: 10.1083/jcb.73.2.492. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Saxton W. M., Stemple D. L., Leslie R. J., Salmon E. D., Zavortink M., McIntosh J. R. Tubulin dynamics in cultured mammalian cells. J Cell Biol. 1984 Dec;99(6):2175–2186. doi: 10.1083/jcb.99.6.2175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Schulze E., Kirschner M. Dynamic and stable populations of microtubules in cells. J Cell Biol. 1987 Feb;104(2):277–288. doi: 10.1083/jcb.104.2.277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Schulze E., Kirschner M. Microtubule dynamics in interphase cells. J Cell Biol. 1986 Mar;102(3):1020–1031. doi: 10.1083/jcb.102.3.1020. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Suprenant K. A., Marsh J. C. Temperature and pH govern the self-assembly of microtubules from unfertilized sea-urchin egg extracts. J Cell Sci. 1987 Feb;87(Pt 1):71–84. doi: 10.1242/jcs.87.1.71. [DOI] [PubMed] [Google Scholar]
  24. Thompson W. C., Asai D. J., Carney D. H. Heterogeneity among microtubules of the cytoplasmic microtubule complex detected by a monoclonal antibody to alpha tubulin. J Cell Biol. 1984 Mar;98(3):1017–1025. doi: 10.1083/jcb.98.3.1017. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Weingarten M. D., Lockwood A. H., Hwo S. Y., Kirschner M. W. A protein factor essential for microtubule assembly. Proc Natl Acad Sci U S A. 1975 May;72(5):1858–1862. doi: 10.1073/pnas.72.5.1858. [DOI] [PMC free article] [PubMed] [Google Scholar]

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