A chromatin binding site in the tail domain of nuclear lamins that interacts with core histones

doi:10.1083/jcb.131.1.33

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A chromatin binding site in the tail domain of nuclear lamins that interacts with core histones

H Taniura, C Glass and L Gerace
Department of Cell Biology, Scripps Research Institute, La Jolla, California 92037, USA.

Interaction of chromatin with the nuclear envelope and lamina is thought to help determine higher order chromosome organization in the interphase nucleus. Previous studies have shown that nuclear lamins bind chromatin directly. Here we have localized a chromatin binding site to the carboxyl-terminal tail domains of both A- and B-type mammalian lamins, and have characterized the biochemical properties of this binding in detail. Recombinant glutathione-S-transferase fusion proteins containing the tail domains of mammalian lamins C, B1, and B2 were analyzed for their ability to associate with rat liver chromatin fragments immobilized on microtiter plate wells. We found that all three lamin tails specifically bind to chromatin with apparent KdS of 120-300 nM. By examining a series of deletion mutants, we have mapped the chromatin binding region of the lamin C tail to amino acids 396- 430, a segment immediately adjacent to the rod domain. Furthermore, by analysis of chromatin subfractions, we found that core histones constitute the principal chromatin binding component for the lamin C tail. Through cooperativity, this lamin-histone interaction could be involved in specifying the high avidity attachment of chromatin to the nuclear envelope in vivo.
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Dechat, T., Gajewski, A., Korbei, B., Gerlich, D., Daigle, N., Haraguchi, T., Furukawa, K., Ellenberg, J., Foisner, R. (2004). LAP2{alpha} and BAF transiently localize to telomeres and specific regions on chromatin during nuclear assembly. J. Cell Sci. 117: 6117-6128 [Abstract] [Full Text]
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Goldman, R. D., Gruenbaum, Y., Moir, R. D., Shumaker, D. K., Spann, T. P. (2002). Nuclear lamins: building blocks of nuclear architecture. Genes Dev. 16: 533-547 [Full Text]
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Schirmer, E. C., Guan, T., Gerace, L. (2001). Involvement of the Lamin Rod Domain in Heterotypic Lamin Interactions Important for Nuclear Organization. JCB 153: 479-490 [Abstract] [Full Text]
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Muchir, A., Bonne, G., van der Kooi, A. J., van Meegen, M., Baas, F., Bolhuis, P. A., de Visser, M., Schwartz, K. (2000). Identification of mutations in the gene encoding lamins A/C in autosomal dominant limb girdle muscular dystrophy with atrioventricular conduction disturbances (LGMD1B). Hum Mol Genet 9: 1453-1459 [Abstract] [Full Text]
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Barton, R. M., Worman, H. J. (1999). Prenylated Prelamin A Interacts with Narf, a Novel Nuclear Protein. J. Biol. Chem. 274: 30008-30018 [Abstract] [Full Text]
Gindullis, F., Peffer, N. J., Meier, I. (1999). MAF1, a Novel Plant Protein Interacting with Matrix Attachment Region Binding Protein MFP1, Is Located at the Nuclear Envelope. Plant Cell 11: 1755-1768 [Abstract] [Full Text]
Lourim, D, Krohne, G (1999). Chromatin binding and polymerization of the endogenous Xenopus egg lamins: the opposing effects of glycogen and ATP. J. Cell Sci. 111: 3675-3686 [Abstract]
Crowe, D.L., Milo, G.E., Shuler, C.E. (1999). Keratin 19 Downregulation by Oral Squamous Cell Carcinoma Lines Increases Invasive Potential. JDR 78: 1256-1263 [Abstract]
Gant, T. M., Harris, C. A., Wilson, K. L. (1999). Roles of LAP2 Proteins in Nuclear Assembly and DNA Replication: Truncated LAP2{beta} Proteins Alter Lamina Assembly, Envelope Formation, Nuclear Size, and DNA Replication Efficiency in Xenopus laevis Extracts. JCB 144: 1083-1096 [Abstract] [Full Text]
Goldberg, M., Harel, A., Brandeis, M., Rechsteiner, T., Richmond, T. J., Weiss, A. M., Gruenbaum, Y. (1999). The tail domain of lamin Dm0 binds histones H2A and H2B. Proc. Natl. Acad. Sci. USA 96: 2852-2857 [Abstract] [Full Text]
Grigoryev, S. A., Bednar, J., Woodcock, C. L. (1999). MENT, a Heterochromatin Protein That Mediates Higher Order Chromatin Folding, Is a New Serpin Family Member. J. Biol. Chem. 274: 5626-5636 [Abstract] [Full Text]
Furukawa, K (1999). LAP2 binding protein 1 (L2BP1/BAF) is a candidate mediator of LAP2-chromatin interaction. J. Cell Sci. 112: 2485-2492 [Abstract]
Goldberg, M., Lu, H., Stuurman, N., Ashery-Padan, R., Weiss, A. M., Yu, J., Bhattacharyya, D., Fisher, P. A., Gruenbaum, Y., Wolfner, M. F. (1998). Interactions among Drosophila Nuclear Envelope Proteins Lamin, Otefin, and YA. Mol. Cell. Biol. 18: 4315-4323 [Abstract] [Full Text]
Furukawa, K., Fritze, C. E., Gerace, L. (1998). The Major Nuclear Envelope Targeting Domain of LAP2 Coincides with Its Lamin Binding Region but Is Distinct from Its Chromatin Interaction Domain. J. Biol. Chem. 273: 4213-4219 [Abstract] [Full Text]
Liu, J., Wolfner, M. F. (1998). Functional Dissection of YA, an Essential, Developmentally Regulated Nuclear Lamina Protein in Drosophila melanogaster. Mol. Cell. Biol. 18: 188-197 [Abstract] [Full Text]
Rzepecki, R, Bogachev, S., Kokoza, E, Stuurman, N, Fisher, P. (1998). In vivo association of lamins with nucleic acids in Drosophila melanogaster. J. Cell Sci. 111: 121-129 [Abstract]
Ferreira, J., Paolella, G., Ramos, C., Lamond, A. I. (1997). Spatial Organization of Large-Scale Chromatin Domains in the Nucleus: A Magnified View of Single Chromosome Territories. JCB 139: 1597-1610 [Abstract] [Full Text]
Yang, L., Guan, T., Gerace, L. (1997). Lamin-binding Fragment of LAP2 Inhibits Increase in Nuclear Volume during the Cell Cycle and Progression into S Phase. JCB 139: 1077-1087 [Abstract] [Full Text]
Abney, J. R., Cutler, B., Fillbach, M. L., Axelrod, D., Scalettar, B. A. (1997). Chromatin Dynamics in Interphase Nuclei and Its Implications for Nuclear Structure. JCB 137: 1459-1468 [Abstract] [Full Text]
Yang, L., Guan, T., Gerace, L. (1997). Integral Membrane Proteins of the Nuclear Envelope Are Dispersed throughout the Endoplasmic Reticulum during Mitosis. JCB 137: 1199-1210 [Abstract] [Full Text]
Pugh, G., Coates, P., Lane, E., Raymond, Y, Quinlan, R. (1997). Distinct nuclear assembly pathways for lamins A and C lead to their increase during quiescence in Swiss 3T3 cells. J. Cell Sci. 110: 2483-2493 [Abstract]
Lopez, J., Wolfner, M. (1997). The developmentally regulated Drosophila embryonic nuclear lamina protein 'Young Arrest' (fs(1)Ya) is capable of associating with chromatin. J. Cell Sci. 110: 643-651 [Abstract]
Nakajima, T., Morita, K., Ohi, N., Arai, T., Nozaki, N., Kikuchi, A., Osaka, F., Yamao, F., Oda, K. (1996). Degradation of Topoisomerase IIalpha during Adenovirus E1A-induced Apoptosis Is Mediated by the Activation of the Ubiquitin Proteolysis System. J. Biol. Chem. 271: 24842-24849 [Abstract] [Full Text]
Machiels, B. M., Zorenc, A. H. G., Endert, J. M., Kuijpers, H. J. H., van Eys, G. J. J. M., Ramaekers, F. C. S., Broers, J. L. V. (1996). An Alternative Splicing Product of the Lamin A/C Gene Lacks Exon 10. J. Biol. Chem. 271: 9249-9253 [Abstract] [Full Text]
Lourim, D, Kempf, A, Krohne, G (1996). Characterization and quantitation of three B-type lamins in Xenopus oocytes and eggs: increase of lamin LI protein synthesis during meiotic maturation. J. Cell Sci. 109: 1775-1785 [Abstract]
Yu, J., Wolfner, M. F. (2002). The Drosophila Nuclear Lamina Protein YA Binds to DNA and Histone H2B with Four Domains. Mol. Biol. Cell 13: 558-569 [Abstract] [Full Text]