Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1994 Mar 15;91(6):2100–2104. doi: 10.1073/pnas.91.6.2100

Cytoplasmic dynein is involved in nuclear migration in Aspergillus nidulans.

X Xiang 1, S M Beckwith 1, N R Morris 1
PMCID: PMC43317  PMID: 8134356

Abstract

Nuclear migration plays an important role in the growth and development of many organisms including the multinuclear fungus Aspergillus nidulans. We have identified four genes, nudA, nudC, nudF, and nudG, in which temperature-sensitive mutations affect nuclear distribution. In this report, we describe the cloning of the nudA gene by complementation of the mutant phenotype by using a chromosome VIII-specific cosmid library. A genomic fragment of nudA hybridized to an mRNA of approximately 14 kb. Sequencing analysis of nudA revealed four ATP-binding sites that are characteristic of the cytoplasmic dynein heavy chain. The amino acid sequence of the nudA gene product shows 52% overall identity with the rat brain cytoplasmic dynein heavy chain. Our study provides in vivo evidence that dynein, a microtubule motor molecule, plays a role in the nuclear migration process.

Full text

PDF
2103

Images in this article

2101Image
on p.2101
2101Image
on p.2101
2101Image
on p.2101

Selected References

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

  1. Brody H., Griffith J., Cuticchia A. J., Arnold J., Timberlake W. E. Chromosome-specific recombinant DNA libraries from the fungus Aspergillus nidulans. Nucleic Acids Res. 1991 Jun 11;19(11):3105–3109. doi: 10.1093/nar/19.11.3105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Englander L. L., Rubin L. L. Acetylcholine receptor clustering and nuclear movement in muscle fibers in culture. J Cell Biol. 1987 Jan;104(1):87–95. doi: 10.1083/jcb.104.1.87. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Enos A. P., Morris N. R. Mutation of a gene that encodes a kinesin-like protein blocks nuclear division in A. nidulans. Cell. 1990 Mar 23;60(6):1019–1027. doi: 10.1016/0092-8674(90)90350-n. [DOI] [PubMed] [Google Scholar]
  5. Eshel D., Urrestarazu L. A., Vissers S., Jauniaux J. C., van Vliet-Reedijk J. C., Planta R. J., Gibbons I. R. Cytoplasmic dynein is required for normal nuclear segregation in yeast. Proc Natl Acad Sci U S A. 1993 Dec 1;90(23):11172–11176. doi: 10.1073/pnas.90.23.11172. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Gibbons I. R., Gibbons B. H., Mocz G., Asai D. J. Multiple nucleotide-binding sites in the sequence of dynein beta heavy chain. Nature. 1991 Aug 15;352(6336):640–643. doi: 10.1038/352640a0. [DOI] [PubMed] [Google Scholar]
  7. Hirokawa N., Sato-Yoshitake R., Yoshida T., Kawashima T. Brain dynein (MAP1C) localizes on both anterogradely and retrogradely transported membranous organelles in vivo. J Cell Biol. 1990 Sep;111(3):1027–1037. doi: 10.1083/jcb.111.3.1027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Koonce M. P., Grissom P. M., McIntosh J. R. Dynein from Dictyostelium: primary structure comparisons between a cytoplasmic motor enzyme and flagellar dynein. J Cell Biol. 1992 Dec;119(6):1597–1604. doi: 10.1083/jcb.119.6.1597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Li Y. Y., Yeh E., Hays T., Bloom K. Disruption of mitotic spindle orientation in a yeast dynein mutant. Proc Natl Acad Sci U S A. 1993 Nov 1;90(21):10096–10100. doi: 10.1073/pnas.90.21.10096. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. McIntosh J. R., Pfarr C. M. Mitotic motors. J Cell Biol. 1991 Nov;115(3):577–585. doi: 10.1083/jcb.115.3.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Meluh P. B., Rose M. D. KAR3, a kinesin-related gene required for yeast nuclear fusion. Cell. 1990 Mar 23;60(6):1029–1041. doi: 10.1016/0092-8674(90)90351-e. [DOI] [PubMed] [Google Scholar]
  12. Mikami A., Paschal B. M., Mazumdar M., Vallee R. B. Molecular cloning of the retrograde transport motor cytoplasmic dynein (MAP 1C). Neuron. 1993 May;10(5):787–796. doi: 10.1016/0896-6273(93)90195-w. [DOI] [PubMed] [Google Scholar]
  13. Morris N. R. Mitotic mutants of Aspergillus nidulans. Genet Res. 1975 Dec;26(3):237–254. doi: 10.1017/s0016672300016049. [DOI] [PubMed] [Google Scholar]
  14. O'Connell M. J., Meluh P. B., Rose M. D., Morris N. R. Suppression of the bimC4 mitotic spindle defect by deletion of klpA, a gene encoding a KAR3-related kinesin-like protein in Aspergillus nidulans. J Cell Biol. 1993 Jan;120(1):153–162. doi: 10.1083/jcb.120.1.153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. O'Connell M. J., Osmani A. H., Morris N. R., Osmani S. A. An extra copy of nimEcyclinB elevates pre-MPF levels and partially suppresses mutation of nimTcdc25 in Aspergillus nidulans. EMBO J. 1992 Jun;11(6):2139–2149. doi: 10.1002/j.1460-2075.1992.tb05273.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Oakley B. R., Morris N. R. A beta-tubulin mutation in Aspergillus nidulans that blocks microtubule function without blocking assembly. Cell. 1981 Jun;24(3):837–845. doi: 10.1016/0092-8674(81)90109-4. [DOI] [PubMed] [Google Scholar]
  17. Oakley B. R., Morris N. R. Nuclear movement is beta--tubulin-dependent in Aspergillus nidulans. Cell. 1980 Jan;19(1):255–262. doi: 10.1016/0092-8674(80)90407-9. [DOI] [PubMed] [Google Scholar]
  18. Ogawa K. Four ATP-binding sites in the midregion of the beta heavy chain of dynein. Nature. 1991 Aug 15;352(6336):643–645. doi: 10.1038/352643a0. [DOI] [PubMed] [Google Scholar]
  19. Osmani A. H., Osmani S. A., Morris N. R. The molecular cloning and identification of a gene product specifically required for nuclear movement in Aspergillus nidulans. J Cell Biol. 1990 Aug;111(2):543–551. doi: 10.1083/jcb.111.2.543. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Osmani S. A., May G. S., Morris N. R. Regulation of the mRNA levels of nimA, a gene required for the G2-M transition in Aspergillus nidulans. J Cell Biol. 1987 Jun;104(6):1495–1504. doi: 10.1083/jcb.104.6.1495. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. PONTECORVO G., ROPER J. A., HEMMONS L. M., MACDONALD K. D., BUFTON A. W. J. The genetics of Aspergillus nidulans. Adv Genet. 1953;5:141–238. doi: 10.1016/s0065-2660(08)60408-3. [DOI] [PubMed] [Google Scholar]
  22. Reeve W. J., Kelly F. P. Nuclear position in the cells of the mouse early embryo. J Embryol Exp Morphol. 1983 Jun;75:117–139. [PubMed] [Google Scholar]
  23. Saunders W. S., Hoyt M. A. Kinesin-related proteins required for structural integrity of the mitotic spindle. Cell. 1992 Aug 7;70(3):451–458. doi: 10.1016/0092-8674(92)90169-d. [DOI] [PubMed] [Google Scholar]
  24. Schatten G. Motility during fertilization. Int Rev Cytol. 1982;79:59–163. doi: 10.1016/s0074-7696(08)61673-3. [DOI] [PubMed] [Google Scholar]
  25. Schroer T. A., Sheetz M. P. Functions of microtubule-based motors. Annu Rev Physiol. 1991;53:629–652. doi: 10.1146/annurev.ph.53.030191.003213. [DOI] [PubMed] [Google Scholar]
  26. Smith J. L., Schoenwolf G. C. Role of cell-cycle in regulating neuroepithelial cell shape during bending of the chick neural plate. Cell Tissue Res. 1988 Jun;252(3):491–500. doi: 10.1007/BF00216636. [DOI] [PubMed] [Google Scholar]
  27. Vaisberg E. A., Koonce M. P., McIntosh J. R. Cytoplasmic dynein plays a role in mammalian mitotic spindle formation. J Cell Biol. 1993 Nov;123(4):849–858. doi: 10.1083/jcb.123.4.849. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Vallee R. B., Shpetner H. S. Motor proteins of cytoplasmic microtubules. Annu Rev Biochem. 1990;59:909–932. doi: 10.1146/annurev.bi.59.070190.004401. [DOI] [PubMed] [Google Scholar]
  29. Vallee R. Molecular analysis of the microtubule motor dynein. Proc Natl Acad Sci U S A. 1993 Oct 1;90(19):8769–8772. doi: 10.1073/pnas.90.19.8769. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Walker R. A., Sheetz M. P. Cytoplasmic microtubule-associated motors. Annu Rev Biochem. 1993;62:429–451. doi: 10.1146/annurev.bi.62.070193.002241. [DOI] [PubMed] [Google Scholar]
  31. Wang E., Cross R. K., Choppin P. W. Involvement of microtubules and 10-nm filaments in the movement and positioning of nuclei in syncytia. J Cell Biol. 1979 Nov;83(2 Pt 1):320–337. doi: 10.1083/jcb.83.2.320. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Zhang Z., Tanaka Y., Nonaka S., Aizawa H., Kawasaki H., Nakata T., Hirokawa N. The primary structure of rat brain (cytoplasmic) dynein heavy chain, a cytoplasmic motor enzyme. Proc Natl Acad Sci U S A. 1993 Sep 1;90(17):7928–7932. doi: 10.1073/pnas.90.17.7928. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES