Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1984 Dec 1;99(6):1927–1935. doi: 10.1083/jcb.99.6.1927

Programmed expression of beta-tubulin genes during development and differentiation of the chicken

PMCID: PMC2113537  PMID: 6094589

Abstract

We have previously demonstrated that the chicken genome contains at least four different, functional beta-tubulin genes. By using gene specific probes we have now analyzed the relative levels of expression of the four encoded messenger RNA (mRNA) transcripts as a function of chicken development and differentiation. We have found that the RNA transcript from the beta 2 gene is present in large amounts in embryonic chick brain and is also preferentially expressed in spinal cord neurons, indicating that this transcript encodes the dominant neuronal beta-tubulin polypeptide. The beta 3 mRNA is present in overwhelming amounts in RNA from chicken testis suggesting that this gene encodes a flagellar or meiotic spindle tubulin. However, both of these genes are transcribed to varying, but lesser, degrees in a number of additional cell and tissue types indicating that they are not neuronal or testis specific, respectively. Beta 4' transcripts are present at moderate levels in all cell and tissue types examined, suggesting that this mRNA encodes a constitutive beta-tubulin polypeptide that is involved in an essential or housekeeping microtubule function. Transcripts from the beta 1 gene are a minor component of the beta-tubulin mRNA populations in all cells and tissues tested. Overall, we conclude that specific beta-tubulin mRNA species are expressed in markedly different ratios in different tissues in the chicken. Such developmental regulation may reflect the function(s) of the individual beta-tubulin polypeptides or, alternatively, may be required for precise control of tubulin gene expression in cells that utilize microtubules for divergent purposes.

Full Text

The Full Text of this article is available as a PDF (1.7 MB).

Selected References

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

  1. Bond J. F., Farmer S. R. Regulation of tubulin and actin mRNA production in rat brain: expression of a new beta-tubulin mRNA with development. Mol Cell Biol. 1983 Aug;3(8):1333–1342. doi: 10.1128/mcb.3.8.1333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Brunke K. J., Collis P. S., Weeks D. P. Post-translational modification of tubulin dependent on organelle assembly. Nature. 1982 Jun 10;297(5866):516–518. doi: 10.1038/297516a0. [DOI] [PubMed] [Google Scholar]
  3. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  4. Cleveland D. W., Lopata M. A., MacDonald R. J., Cowan N. J., Rutter W. J., Kirschner M. W. Number and evolutionary conservation of alpha- and beta-tubulin and cytoplasmic beta- and gamma-actin genes using specific cloned cDNA probes. Cell. 1980 May;20(1):95–105. doi: 10.1016/0092-8674(80)90238-x. [DOI] [PubMed] [Google Scholar]
  5. Cleveland D. W. The tubulins: from DNA to RNA to protein and back again. Cell. 1983 Sep;34(2):330–332. doi: 10.1016/0092-8674(83)90366-5. [DOI] [PubMed] [Google Scholar]
  6. Gozes I., Littauer U. Z. Tubulin microheterogeneity increases with rat brain maturation. Nature. 1978 Nov 23;276(5686):411–413. doi: 10.1038/276411a0. [DOI] [PubMed] [Google Scholar]
  7. Hall J. L., Dudley L., Dobner P. R., Lewis S. A., Cowan N. J. Identification of two human beta-tubulin isotypes. Mol Cell Biol. 1983 May;3(5):854–862. doi: 10.1128/mcb.3.5.854. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Kalfayan L., Wensink P. C. Developmental regulation of Drosophila alpha-tubulin genes. Cell. 1982 May;29(1):91–98. doi: 10.1016/0092-8674(82)90093-9. [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. Kost T. A., Theodorakis N., Hughes S. H. The nucleotide sequence of the chick cytoplasmic beta-actin gene. Nucleic Acids Res. 1983 Dec 10;11(23):8287–8301. doi: 10.1093/nar/11.23.8287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. L'Hernault S. W., Rosenbaum J. L. Chlamydomonas alpha-tubulin is posttranslationally modified in the flagella during flagellar assembly. J Cell Biol. 1983 Jul;97(1):258–263. doi: 10.1083/jcb.97.1.258. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Lee M. G., Lewis S. A., Wilde C. D., Cowan N. J. Evolutionary history of a multigene family: an expressed human beta-tubulin gene and three processed pseudogenes. Cell. 1983 Jun;33(2):477–487. doi: 10.1016/0092-8674(83)90429-4. [DOI] [PubMed] [Google Scholar]
  13. Lopata M. A., Havercroft J. C., Chow L. T., Cleveland D. W. Four unique genes required for beta tubulin expression in vertebrates. Cell. 1983 Mar;32(3):713–724. doi: 10.1016/0092-8674(83)90057-0. [DOI] [PubMed] [Google Scholar]
  14. McKeithan T. W., Lefebvre P. A., Silflow C. D., Rosenbaum J. L. Multiple forms of tubulin in Polytomella and Chlamydomonas: evidence for a precursor of flagellar alpha-tubulin. J Cell Biol. 1983 Apr;96(4):1056–1063. doi: 10.1083/jcb.96.4.1056. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Murphy D. B., Wallis K. T. Brain and erythrocyte microtubules from chicken contain different beta-tubulin polypeptides. J Biol Chem. 1983 Jun 25;258(12):7870–7875. [PubMed] [Google Scholar]
  16. Murphy D. B., Wallis K. T. Isolation of microtubule protein from chicken erythrocytes and determination of the critical concentration for tubulin polymerization in vitro and in vivo. J Biol Chem. 1983 Jul 10;258(13):8357–8364. [PubMed] [Google Scholar]
  17. Natzle J. E., McCarthy B. J. Regulation of Drosophila alpha- and beta-tubulin genes during development. Dev Biol. 1984 Jul;104(1):187–198. doi: 10.1016/0012-1606(84)90047-2. [DOI] [PubMed] [Google Scholar]
  18. Nelles L. P., Bamburg J. R. Comparative peptide mapping and isoelectric focusing of isolated subunits from chick embryo brain tubulin. J Neurochem. 1979 Feb;32(2):477–489. doi: 10.1111/j.1471-4159.1979.tb00374.x. [DOI] [PubMed] [Google Scholar]
  19. Shank P. R., Hughes S. H., Kung H. J., Majors J. E., Quintrell N., Guntaka R. V., Bishop J. M., Varmus H. E. Mapping unintegrated avian sarcoma virus DNA: termini of linear DNA bear 300 nucleotides present once or twice in two species of circular DNA. Cell. 1978 Dec;15(4):1383–1395. doi: 10.1016/0092-8674(78)90063-6. [DOI] [PubMed] [Google Scholar]
  20. Sullivan K. F., Wilson L. Developmental and biochemical analysis of chick brain tubulin heterogeneity. J Neurochem. 1984 May;42(5):1363–1371. doi: 10.1111/j.1471-4159.1984.tb02796.x. [DOI] [PubMed] [Google Scholar]
  21. Tarlow D. M., Watkins P. A., Reed R. E., Miller R. S., Zwergel E. E., Lane M. D. Lipogenesis and the synthesis and secretion of very low density lipoprotein by avian liver cells in nonproliferating monolayer culture. Hormonal effects. J Cell Biol. 1977 May;73(2):332–353. doi: 10.1083/jcb.73.2.332. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Valenzuela P., Quiroga M., Zaldivar J., Rutter W. J., Kirschner M. W., Cleveland D. W. Nucleotide and corresponding amino acid sequences encoded by alpha and beta tubulin mRNAs. Nature. 1981 Feb 19;289(5799):650–655. doi: 10.1038/289650a0. [DOI] [PubMed] [Google Scholar]
  24. Wilde C. D., Crowther C. E., Cripe T. P., Gwo-Shu Lee M., Cowan N. J. Evidence that a human beta-tubulin pseudogene is derived from its corresponding mRNA. Nature. 1982 May 6;297(5861):83–84. doi: 10.1038/297083a0. [DOI] [PubMed] [Google Scholar]

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

RESOURCES