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. 1989 Jun 1;108(6):2069–2082. doi: 10.1083/jcb.108.6.2069

Lamin A, lamin B, and lamin B receptor analogues in yeast

PMCID: PMC2115584  PMID: 2544600

Abstract

Previous studies have shown that turkey erythrocyte lamin B is anchored to the nuclear envelope via a 58-kD integral membrane protein termed p58 or lamin B receptor (Worman H. J., J. Yuan, G. Blobel, and S. D. Georgatos. 1988. Proc. Natl. Acad. Sci. USA. 85:8531-8534). We now identify a p58 analogue in the yeast Saccharomyces cerevisiae. Turkey erythrocyte lamin B binds to yeast urea-extracted nuclear envelopes with high affinity, associating predominantly with a 58-kD polypeptide. This yeast polypeptide is recognized by polyclonal antibodies against turkey p58, partitions entirely with the nuclear fraction, remains membrane bound after urea extraction of the nuclear envelopes, and is structurally similar to turkey p58 by peptide mapping criteria. Using polyclonal antibodies against turkey erythrocyte lamins A and B, we also identify two yeast lamin forms. The yeast lamin B analogue has a molecular mass of 66 kD and is structurally related to erythrocyte lamin B. Moreover, the yeast lamin B analogue partitions exclusively with the nuclear envelope fraction, is quantitatively removed from the envelopes by urea extraction, and binds to turkey lamin A and vimentin. As many higher eukaryotic lamin B forms, the yeast analogue is chemically heterogeneous comprising two serologically related species with different charge characteristics. Antibodies against turkey lamin A detect a 74-kD yeast protein, slightly larger than the turkey lamin A. It is more abundant than the yeast lamin B analogue and partitions between a soluble cytoplasmic fraction and a nuclear envelope fraction. The yeast lamin A analogue can be extracted from the nuclear envelope by urea, shows structural similarity to turkey and rat lamin A, and binds to isolated turkey lamin B. These data indicate that analogues of typical nuclear lamina components (lamins A and B, as well as lamin B receptor) are present in yeast and behave as their vertebrate counterparts.

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Selected References

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  1. Adams A. E., Pringle J. R. Relationship of actin and tubulin distribution to bud growth in wild-type and morphogenetic-mutant Saccharomyces cerevisiae. J Cell Biol. 1984 Mar;98(3):934–945. doi: 10.1083/jcb.98.3.934. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aris J. P., Blobel G. Identification and characterization of a yeast nucleolar protein that is similar to a rat liver nucleolar protein. J Cell Biol. 1988 Jul;107(1):17–31. doi: 10.1083/jcb.107.1.17. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Burke B., Gerace L. A cell free system to study reassembly of the nuclear envelope at the end of mitosis. Cell. 1986 Feb 28;44(4):639–652. doi: 10.1016/0092-8674(86)90273-4. [DOI] [PubMed] [Google Scholar]
  4. Byers B., Goetsch L. A highly ordered ring of membrane-associated filaments in budding yeast. J Cell Biol. 1976 Jun;69(3):717–721. doi: 10.1083/jcb.69.3.717. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Byers B., Goetsch L. Duplication of spindle plaques and integration of the yeast cell cycle. Cold Spring Harb Symp Quant Biol. 1974;38:123–131. doi: 10.1101/sqb.1974.038.01.016. [DOI] [PubMed] [Google Scholar]
  6. Carter B. L. The yeast nucleus. Adv Microb Physiol. 1978;17:243–302. doi: 10.1016/s0065-2911(08)60059-4. [DOI] [PubMed] [Google Scholar]
  7. Fisher D. Z., Chaudhary N., Blobel G. cDNA sequencing of nuclear lamins A and C reveals primary and secondary structural homology to intermediate filament proteins. Proc Natl Acad Sci U S A. 1986 Sep;83(17):6450–6454. doi: 10.1073/pnas.83.17.6450. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Georgatos S. D., Blobel G. Lamin B constitutes an intermediate filament attachment site at the nuclear envelope. J Cell Biol. 1987 Jul;105(1):117–125. doi: 10.1083/jcb.105.1.117. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Georgatos S. D., Stournaras C., Blobel G. Heterotypic and homotypic associations between the nuclear lamins: site-specificity and control by phosphorylation. Proc Natl Acad Sci U S A. 1988 Jun;85(12):4325–4329. doi: 10.1073/pnas.85.12.4325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Georgatos S. D., Weaver D. C., Marchesi V. T. Site specificity in vimentin-membrane interactions: intermediate filament subunits associate with the plasma membrane via their head domains. J Cell Biol. 1985 Jun;100(6):1962–1967. doi: 10.1083/jcb.100.6.1962. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Georgatos S. D., Weber K., Geisler N., Blobel G. Binding of two desmin derivatives to the plasma membrane and the nuclear envelope of avian erythrocytes: evidence for a conserved site-specificity in intermediate filament-membrane interactions. Proc Natl Acad Sci U S A. 1987 Oct;84(19):6780–6784. doi: 10.1073/pnas.84.19.6780. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gerace L., Blobel G. The nuclear envelope lamina is reversibly depolymerized during mitosis. Cell. 1980 Jan;19(1):277–287. doi: 10.1016/0092-8674(80)90409-2. [DOI] [PubMed] [Google Scholar]
  13. Gerace L., Burke B. Functional organization of the nuclear envelope. Annu Rev Cell Biol. 1988;4:335–374. doi: 10.1146/annurev.cb.04.110188.002003. [DOI] [PubMed] [Google Scholar]
  14. Gerace L., Comeau C., Benson M. Organization and modulation of nuclear lamina structure. J Cell Sci Suppl. 1984;1:137–160. doi: 10.1242/jcs.1984.supplement_1.10. [DOI] [PubMed] [Google Scholar]
  15. Greer C., Schekman R. Actin from Saccharomyces cerevisiae. Mol Cell Biol. 1982 Oct;2(10):1270–1278. doi: 10.1128/mcb.2.10.1270. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Jacobs C. W., Adams A. E., Szaniszlo P. J., Pringle J. R. Functions of microtubules in the Saccharomyces cerevisiae cell cycle. J Cell Biol. 1988 Oct;107(4):1409–1426. doi: 10.1083/jcb.107.4.1409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kilmartin J. V., Adams A. E. Structural rearrangements of tubulin and actin during the cell cycle of the yeast Saccharomyces. J Cell Biol. 1984 Mar;98(3):922–933. doi: 10.1083/jcb.98.3.922. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kilmartin J. V. Purification of yeast tubulin by self-assembly in vitro. Biochemistry. 1981 Jun 9;20(12):3629–3633. doi: 10.1021/bi00515a050. [DOI] [PubMed] [Google Scholar]
  19. Koteliansky V. E., Glukhova M. A., Bejanian M. V., Surguchov A. P., Smirnov V. N. Isolation and characterization of actin-like protein from yeast Saccharomyces cerevisiae. FEBS Lett. 1979 Jun 1;102(1):55–58. doi: 10.1016/0014-5793(79)80927-8. [DOI] [PubMed] [Google Scholar]
  20. Krohne G., Wolin S. L., McKeon F. D., Franke W. W., Kirschner M. W. Nuclear lamin LI of Xenopus laevis: cDNA cloning, amino acid sequence and binding specificity of a member of the lamin B subfamily. EMBO J. 1987 Dec 1;6(12):3801–3808. doi: 10.1002/j.1460-2075.1987.tb02716.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  22. Lehner C. F., Stick R., Eppenberger H. M., Nigg E. A. Differential expression of nuclear lamin proteins during chicken development. J Cell Biol. 1987 Jul;105(1):577–587. doi: 10.1083/jcb.105.1.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Magdolen V., Oechsner U., Müller G., Bandlow W. The intron-containing gene for yeast profilin (PFY) encodes a vital function. Mol Cell Biol. 1988 Dec;8(12):5108–5115. doi: 10.1128/mcb.8.12.5108. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. McKeon F. D., Kirschner M. W., Caput D. Homologies in both primary and secondary structure between nuclear envelope and intermediate filament proteins. Nature. 1986 Feb 6;319(6053):463–468. doi: 10.1038/319463a0. [DOI] [PubMed] [Google Scholar]
  25. Newport J. Nuclear reconstitution in vitro: stages of assembly around protein-free DNA. Cell. 1987 Jan 30;48(2):205–217. doi: 10.1016/0092-8674(87)90424-7. [DOI] [PubMed] [Google Scholar]
  26. O'Farrell P. Z., Goodman H. M., O'Farrell P. H. High resolution two-dimensional electrophoresis of basic as well as acidic proteins. Cell. 1977 Dec;12(4):1133–1141. doi: 10.1016/0092-8674(77)90176-3. [DOI] [PubMed] [Google Scholar]
  27. Peterson J. B., Ris H. Electron-microscopic study of the spindle and chromosome movement in the yeast Saccharomyces cerevisiae. J Cell Sci. 1976 Nov;22(2):219–242. doi: 10.1242/jcs.22.2.219. [DOI] [PubMed] [Google Scholar]
  28. Water R. D., Pringle J. R., Kleinsmith L. J. Identification of an actin-like protein and of its messenger ribonucleic acid in Saccharomyces cerevisiae. J Bacteriol. 1980 Dec;144(3):1143–1151. doi: 10.1128/jb.144.3.1143-1151.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Watts F. Z., Miller D. M., Orr E. Identification of myosin heavy chain in Saccharomyces cerevisiae. Nature. 1985 Jul 4;316(6023):83–85. doi: 10.1038/316083a0. [DOI] [PubMed] [Google Scholar]
  30. Wolin S. L., Krohne G., Kirschner M. W. A new lamin in Xenopus somatic tissues displays strong homology to human lamin A. EMBO J. 1987 Dec 1;6(12):3809–3818. doi: 10.1002/j.1460-2075.1987.tb02717.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Worman H. J., Lazaridis I., Georgatos S. D. Nuclear lamina heterogeneity in mammalian cells. Differential expression of the major lamins and variations in lamin B phosphorylation. J Biol Chem. 1988 Aug 25;263(24):12135–12141. [PubMed] [Google Scholar]
  32. Worman H. J., Yuan J., Blobel G., Georgatos S. D. A lamin B receptor in the nuclear envelope. Proc Natl Acad Sci U S A. 1988 Nov;85(22):8531–8534. doi: 10.1073/pnas.85.22.8531. [DOI] [PMC free article] [PubMed] [Google Scholar]

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