Lamin B Constitutes an Intermediate Filament Attachment Site at the Nuclear Envelope

Overview

Journal J Cell Biol

Specialty Cell Biology

Date 1987 Jul 1

PMID 3301863

Citations 63

Authors

S D Georgatos

G Blobel

Affiliations

Soon will be listed here.

Abstract

We found that urea extraction of turkey erythrocyte nuclear envelopes abolished their ability to bind exogenous 125I-vimentin, while, at the same time, it removed the nuclear lamins from the membranes. After purification of the lamins from such urea extracts, a specific binding between isolated vimentin and lamin B, or a lamin A + B hetero-oligomer, was detected by affinity chromatography. Similar analysis revealed that the 6.6-kD vimentin tail piece was involved in this interaction. By other approaches (quantitative immunoprecipitation, rate zonal sedimentation, turbidometric assays) a substoichiometric lamin B-vimentin binding was determined under in vitro conditions. It was also observed that anti-lamin B antibodies but not other sera (anti-lamin A, anti-ankyrin, preimmune) were able to block 70% of the binding of 125I-vimentin to native, vimentin-depleted, nuclear envelopes. These data, which were confirmed by using rat liver nuclear lamins, indicate that intermediate filaments may be anchored directly to the nuclear lamina, providing a continuous network connecting the plasma membrane skeleton with the karyoskeleton of eukaryotic cells.

Citing Articles

Transcriptome Analysis Reveals Vimentin-Induced Disruption of Cell-Cell Associations Augments Breast Cancer Cell Migration.

Usman S, Jamal A, Bushaala A, Waseem N, Al-Dehlawi H, Yeudall W Cells. 2022; 11(24).

PMID: 36552797 PMC: 9776984. DOI: 10.3390/cells11244035.

Desmin variants: Trigger for cardiac arrhythmias?.

Su W, van Wijk S, Brundel B Front Cell Dev Biol. 2022; 10:986718.

PMID: 36158202 PMC: 9500482. DOI: 10.3389/fcell.2022.986718.

Vimentin binds to G-quadruplex repeats found at telomeres and gene promoters.

Ceschi S, Berselli M, Cozzaglio M, Giantin M, Toppo S, Spolaore B Nucleic Acids Res. 2022; 50(3):1370-1381.

PMID: 35100428 PMC: 8860586. DOI: 10.1093/nar/gkab1274.

SOX11 promotes epithelial/mesenchymal hybrid state and alters tropism of invasive breast cancer cells.

Oliemuller E, Newman R, Tsang S, Foo S, Muirhead G, Noor F Elife. 2020; 9.

PMID: 32909943 PMC: 7518891. DOI: 10.7554/eLife.58374.

Discovery of Cell-Surface Vimentin (CSV) as a Sarcoma Target and Development of CSV-Targeted IL12 Immune Therapy.

Batth I, Li S Adv Exp Med Biol. 2020; 1257:169-178.

PMID: 32483739 DOI: 10.1007/978-3-030-43032-0_14.

References

Laemmli U . Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970; 227(5259):680-5. DOI: 10.1038/227680a0. View

Georgatos S, Blobel G . Two distinct attachment sites for vimentin along the plasma membrane and the nuclear envelope in avian erythrocytes: a basis for a vectorial assembly of intermediate filaments. J Cell Biol. 1987; 105(1):105-15. PMC: 2114891. DOI: 10.1083/jcb.105.1.105. View

Fenner C, Traut R, Mason D, Wikman-Coffelt J . Quantification of Coomassie Blue stained proteins in polyacrylamide gels based on analyses of eluted dye. Anal Biochem. 1975; 63(2):595-602. DOI: 10.1016/0003-2697(75)90386-3. View

Aaronson R, Blobel G . Isolation of nuclear pore complexes in association with a lamina. Proc Natl Acad Sci U S A. 1975; 72(3):1007-11. PMC: 432453. DOI: 10.1073/pnas.72.3.1007. View

Storti R, Coen D, Rich A . Tissue-specific forms of actin in the developing chick. Cell. 1976; 8(4):521-7. DOI: 10.1016/0092-8674(76)90220-8. View

Lehto V, Virtanen I, Kurki P . Intermediate filaments anchor the nuclei in nuclear monolayers of cultured human fibroblasts. Nature. 1978; 272(5649):175-7. DOI: 10.1038/272175a0. View

Gerace L, Blum A, Blobel G . Immunocytochemical localization of the major polypeptides of the nuclear pore complex-lamina fraction. Interphase and mitotic distribution. J Cell Biol. 1978; 79(2 Pt 1):546-66. PMC: 2110258. DOI: 10.1083/jcb.79.2.546. View

Zackroff R, Goldman R . In vitro assembly of intermediate filaments from baby hamster kidney (BHK-21) cells. Proc Natl Acad Sci U S A. 1979; 76(12):6226-30. PMC: 411836. DOI: 10.1073/pnas.76.12.6226. View

Steinert P, Idler W, Goldman R . Intermediate filaments of baby hamster kidney (BHK-21) cells and bovine epidermal keratinocytes have similar ultrastructures and subunit domain structures. Proc Natl Acad Sci U S A. 1980; 77(8):4534-8. PMC: 349878. DOI: 10.1073/pnas.77.8.4534. View

10.

Geisler N, Kaufmann E, Weber K . Proteinchemical characterization of three structurally distinct domains along the protofilament unit of desmin 10 nm filaments. Cell. 1982; 30(1):277-86. DOI: 10.1016/0092-8674(82)90033-2. View

11.

Krohne G, Debus E, Osborn M, Weber K, Franke W . A monoclonal antibody against nuclear lamina proteins reveals cell type-specificity in Xenopus laevis. Exp Cell Res. 1984; 150(1):47-59. DOI: 10.1016/0014-4827(84)90700-6. View

12.

Granger B, Lazarides E . Membrane skeletal protein 4.1 of avian erythrocytes is composed of multiple variants that exhibit tissue-specific expression. Cell. 1984; 37(2):595-607. DOI: 10.1016/0092-8674(84)90390-8. View

13.

Hogg P, Winzor D . Effects of ligand multivalency in binding studies: a general counterpart of the Scatchard analysis. Biochim Biophys Acta. 1985; 843(3):159-63. DOI: 10.1016/0304-4165(85)90134-5. View

14.

Goldman R, Goldman A, Green K, Jones J, Lieska N, Yang H . Intermediate filaments: possible functions as cytoskeletal connecting links between the nucleus and the cell surface. Ann N Y Acad Sci. 1985; 455:1-17. DOI: 10.1111/j.1749-6632.1985.tb50400.x. View

15.

McKeon F, Kirschner M, Caput D . Homologies in both primary and secondary structure between nuclear envelope and intermediate filament proteins. Nature. 1986; 319(6053):463-8. DOI: 10.1038/319463a0. View

16.

Fisher D, 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; 83(17):6450-4. PMC: 386521. DOI: 10.1073/pnas.83.17.6450. View

17.

Reeves W, Chaudhary N, Salerno A, Blobel G . Lamin B autoantibodies in sera of certain patients with systemic lupus erythematosus. J Exp Med. 1987; 165(3):750-62. PMC: 2188284. DOI: 10.1084/jem.165.3.750. View

18.

Franke W . Relationship of nuclear membranes with filaments and microtubules. Protoplasma. 1971; 73(2):263-92. DOI: 10.1007/BF01275600. View