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

Abstract

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.

Full Text

The Full Text of this article is available as a PDF (1.6 MB).

Selected References

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

  1. Aebi U., Cohn J., Buhle L., Gerace L. The nuclear lamina is a meshwork of intermediate-type filaments. Nature. 1986 Oct 9;323(6088):560–564. doi: 10.1038/323560a0. [DOI] [PubMed] [Google Scholar]
  2. Belmont A. S., Zhai Y., Thilenius A. Lamin B distribution and association with peripheral chromatin revealed by optical sectioning and electron microscopy tomography. J Cell Biol. 1993 Dec;123(6 Pt 2):1671–1685. doi: 10.1083/jcb.123.6.1671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Burke B. On the cell-free association of lamins A and C with metaphase chromosomes. Exp Cell Res. 1990 Jan;186(1):169–176. doi: 10.1016/0014-4827(90)90223-w. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Foisner R., Gerace L. Integral membrane proteins of the nuclear envelope interact with lamins and chromosomes, and binding is modulated by mitotic phosphorylation. Cell. 1993 Jul 2;73(7):1267–1279. doi: 10.1016/0092-8674(93)90355-t. [DOI] [PubMed] [Google Scholar]
  6. Furukawa K., Hotta Y. cDNA cloning of a germ cell specific lamin B3 from mouse spermatocytes and analysis of its function by ectopic expression in somatic cells. EMBO J. 1993 Jan;12(1):97–106. doi: 10.1002/j.1460-2075.1993.tb05635.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Furukawa K., Inagaki H., Hotta Y. Identification and cloning of an mRNA coding for a germ cell-specific A-type lamin in mice. Exp Cell Res. 1994 Jun;212(2):426–430. doi: 10.1006/excr.1994.1164. [DOI] [PubMed] [Google Scholar]
  8. Furukawa K., Panté N., Aebi U., Gerace L. Cloning of a cDNA for lamina-associated polypeptide 2 (LAP2) and identification of regions that specify targeting to the nuclear envelope. EMBO J. 1995 Apr 18;14(8):1626–1636. doi: 10.1002/j.1460-2075.1995.tb07151.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Georgatos S. D., Meier J., Simos G. Lamins and lamin-associated proteins. Curr Opin Cell Biol. 1994 Jun;6(3):347–353. doi: 10.1016/0955-0674(94)90025-6. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Gerace L., Foisner R. Integral membrane proteins and dynamic organization of the nuclear envelope. Trends Cell Biol. 1994 Apr;4(4):127–131. doi: 10.1016/0962-8924(94)90067-1. [DOI] [PubMed] [Google Scholar]
  12. Gerace L. Molecular trafficking across the nuclear pore complex. Curr Opin Cell Biol. 1992 Aug;4(4):637–645. doi: 10.1016/0955-0674(92)90083-o. [DOI] [PubMed] [Google Scholar]
  13. Gerace L., Ottaviano Y., Kondor-Koch C. Identification of a major polypeptide of the nuclear pore complex. J Cell Biol. 1982 Dec;95(3):826–837. doi: 10.1083/jcb.95.3.826. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gieffers C., Krohne G. In vitro reconstitution of recombinant lamin A and a lamin A mutant lacking the carboxy-terminal tail. Eur J Cell Biol. 1991 Aug;55(2):191–199. [PubMed] [Google Scholar]
  15. Glass C. A., Glass J. R., Taniura H., Hasel K. W., Blevitt J. M., Gerace L. The alpha-helical rod domain of human lamins A and C contains a chromatin binding site. EMBO J. 1993 Nov;12(11):4413–4424. doi: 10.1002/j.1460-2075.1993.tb06126.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Glass J. R., Gerace L. Lamins A and C bind and assemble at the surface of mitotic chromosomes. J Cell Biol. 1990 Sep;111(3):1047–1057. doi: 10.1083/jcb.111.3.1047. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Heins S., Aebi U. Making heads and tails of intermediate filament assembly, dynamics and networks. Curr Opin Cell Biol. 1994 Feb;6(1):25–33. doi: 10.1016/0955-0674(94)90112-0. [DOI] [PubMed] [Google Scholar]
  18. Heitlinger E., Peter M., Häner M., Lustig A., Aebi U., Nigg E. A. Expression of chicken lamin B2 in Escherichia coli: characterization of its structure, assembly, and molecular interactions. J Cell Biol. 1991 May;113(3):485–495. doi: 10.1083/jcb.113.3.485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Heitlinger E., Peter M., Lustig A., Villiger W., Nigg E. A., Aebi U. The role of the head and tail domain in lamin structure and assembly: analysis of bacterially expressed chicken lamin A and truncated B2 lamins. J Struct Biol. 1992 Jan-Feb;108(1):74–89. doi: 10.1016/1047-8477(92)90009-y. [DOI] [PubMed] [Google Scholar]
  20. Hochstrasser M., Mathog D., Gruenbaum Y., Saumweber H., Sedat J. W. Spatial organization of chromosomes in the salivary gland nuclei of Drosophila melanogaster. J Cell Biol. 1986 Jan;102(1):112–123. doi: 10.1083/jcb.102.1.112. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Hochstrasser M., Sedat J. W. Three-dimensional organization of Drosophila melanogaster interphase nuclei. I. Tissue-specific aspects of polytene nuclear architecture. J Cell Biol. 1987 Jun;104(6):1455–1470. doi: 10.1083/jcb.104.6.1455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Höger T. H., Krohne G., Franke W. W. Amino acid sequence and molecular characterization of murine lamin B as deduced from cDNA clones. Eur J Cell Biol. 1988 Dec;47(2):283–290. [PubMed] [Google Scholar]
  23. Höger T. H., Krohne G., Kleinschmidt J. A. Interaction of Xenopus lamins A and LII with chromatin in vitro mediated by a sequence element in the carboxyterminal domain. Exp Cell Res. 1991 Dec;197(2):280–289. doi: 10.1016/0014-4827(91)90434-v. [DOI] [PubMed] [Google Scholar]
  24. Höger T. H., Zatloukal K., Waizenegger I., Krohne G. Characterization of a second highly conserved B-type lamin present in cells previously thought to contain only a single B-type lamin. Chromosoma. 1990 Oct;99(6):379–390. doi: 10.1007/BF01726689. [DOI] [PubMed] [Google Scholar]
  25. Izaurralde E., Mirkovitch J., Laemmli U. K. Interaction of DNA with nuclear scaffolds in vitro. J Mol Biol. 1988 Mar 5;200(1):111–125. doi: 10.1016/0022-2836(88)90337-3. [DOI] [PubMed] [Google Scholar]
  26. Kohwi-Shigematsu T., Kohwi Y. Torsional stress stabilizes extended base unpairing in suppressor sites flanking immunoglobulin heavy chain enhancer. Biochemistry. 1990 Oct 16;29(41):9551–9560. doi: 10.1021/bi00493a009. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Ludérus M. E., de Graaf A., Mattia E., den Blaauwen J. L., Grande M. A., de Jong L., van Driel R. Binding of matrix attachment regions to lamin B1. Cell. 1992 Sep 18;70(6):949–959. doi: 10.1016/0092-8674(92)90245-8. [DOI] [PubMed] [Google Scholar]
  29. Ludérus M. E., den Blaauwen J. L., de Smit O. J., Compton D. A., van Driel R. Binding of matrix attachment regions to lamin polymers involves single-stranded regions and the minor groove. Mol Cell Biol. 1994 Sep;14(9):6297–6305. doi: 10.1128/mcb.14.9.6297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. McKeon F. Nuclear lamin proteins: domains required for nuclear targeting, assembly, and cell-cycle-regulated dynamics. Curr Opin Cell Biol. 1991 Feb;3(1):82–86. doi: 10.1016/0955-0674(91)90169-y. [DOI] [PubMed] [Google Scholar]
  32. Moir R. D., Donaldson A. D., Stewart M. Expression in Escherichia coli of human lamins A and C: influence of head and tail domains on assembly properties and paracrystal formation. J Cell Sci. 1991 Jun;99(Pt 2):363–372. doi: 10.1242/jcs.99.2.363. [DOI] [PubMed] [Google Scholar]
  33. Nachman R. L., Leung L. L. Complex formation of platelet membrane glycoproteins IIb and IIIa with fibrinogen. J Clin Invest. 1982 Feb;69(2):263–269. doi: 10.1172/JCI110448. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Nigg E. A. Assembly-disassembly of the nuclear lamina. Curr Opin Cell Biol. 1992 Feb;4(1):105–109. doi: 10.1016/0955-0674(92)90066-l. [DOI] [PubMed] [Google Scholar]
  35. Noll M., Thomas J. O., Kornberg R. D. Preparation of native chromatin and damage caused by shearing. Science. 1975 Mar 28;187(4182):1203–1206. doi: 10.1126/science.187.4182.1203. [DOI] [PubMed] [Google Scholar]
  36. Peter M., Kitten G. T., Lehner C. F., Vorburger K., Bailer S. M., Maridor G., Nigg E. A. Cloning and sequencing of cDNA clones encoding chicken lamins A and B1 and comparison of the primary structures of vertebrate A- and B-type lamins. J Mol Biol. 1989 Aug 5;208(3):393–404. doi: 10.1016/0022-2836(89)90504-4. [DOI] [PubMed] [Google Scholar]
  37. Pollard K. M., Chan E. K., Grant B. J., Sullivan K. F., Tan E. M., Glass C. A. In vitro posttranslational modification of lamin B cloned from a human T-cell line. Mol Cell Biol. 1990 May;10(5):2164–2175. doi: 10.1128/mcb.10.5.2164. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Riedel W., Werner D. Nucleotide sequence of the full-length mouse lamin C cDNA and its deduced amino-acid sequence. Biochim Biophys Acta. 1989 Jun 1;1008(1):119–122. doi: 10.1016/0167-4781(89)90179-6. [DOI] [PubMed] [Google Scholar]
  39. Rosbash M., Singer R. H. RNA travel: tracks from DNA to cytoplasm. Cell. 1993 Nov 5;75(3):399–401. doi: 10.1016/0092-8674(93)90373-x. [DOI] [PubMed] [Google Scholar]
  40. Shoeman R. L., Traub P. The in vitro DNA-binding properties of purified nuclear lamin proteins and vimentin. J Biol Chem. 1990 Jun 5;265(16):9055–9061. [PubMed] [Google Scholar]
  41. Vorburger K., Lehner C. F., Kitten G. T., Eppenberger H. M., Nigg E. A. A second higher vertebrate B-type lamin. cDNA sequence determination and in vitro processing of chicken lamin B2. J Mol Biol. 1989 Aug 5;208(3):405–415. doi: 10.1016/0022-2836(89)90505-6. [DOI] [PubMed] [Google Scholar]
  42. Yuan J., Simos G., Blobel G., Georgatos S. D. Binding of lamin A to polynucleosomes. J Biol Chem. 1991 May 15;266(14):9211–9215. [PubMed] [Google Scholar]
  43. Zentgraf H., Franke W. W. Differences of supranucleosomal organization in different kinds of chromatin: cell type-specific globular subunits containing different numbers of nucleosomes. J Cell Biol. 1984 Jul;99(1 Pt 1):272–286. doi: 10.1083/jcb.99.1.272. [DOI] [PMC free article] [PubMed] [Google Scholar]