Functional diversity of LAP2α and LAP2β in postmitotic chromosome association is caused by an α-specific nuclear targeting domain

EMBO Journal

Volumn 18, Issue 22, 1999, Pages 6370-6384

  Vlcek, Sylvia ^a   Just, Herwig ^a   Dechat, Thomas ^a   Foisner, Roland ^a  

^a UNIVERSITY OF VIENNA   (Austria)

Author keywords

Chromesome; Lamina associated polypeptide; Mitosis; Nuclear lamina; Nuclear matrix

Indexed keywords

POLYPEPTIDE; RECOMBINANT PROTEIN; DNA BINDING PROTEIN; ISOPROTEIN; LAMINA ASSOCIATED POLYPEPTIDE 2; LAMINA-ASSOCIATED POLYPEPTIDE 2; MEMBRANE PROTEIN; NUCLEAR PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHROMATIN; CHROMOSOME; CONTROLLED STUDY; HUMAN; HUMAN CELL; INTERPHASE; MITOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DOMAIN; ANIMAL; BINDING SITE; CELL CYCLE; CELL LINE; CELL NUCLEUS; CHEMISTRY; CHO CELL; GENE DELETION; GENETIC TRANSFECTION; GENETICS; HAMSTER; HELA CELL; METABOLISM; METAPHASE; MUTAGENESIS; PHYSIOLOGY; RAT;

ANIMALS; BINDING SITES; CELL CYCLE; CELL LINE; CELL NUCLEUS; CHO CELLS; CHROMOSOMES; CRICETINAE; DNA-BINDING PROTEINS; HELA CELLS; HUMANS; INTERPHASE; MEMBRANE PROTEINS; METAPHASE; MITOSIS; MUTAGENESIS; NUCLEAR PROTEINS; PROTEIN ISOFORMS; RATS; RECOMBINANT PROTEINS; SEQUENCE DELETION; TRANSFECTION;

EID: 0033570904     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.22.6370     Document Type: Article

References (45)

1. Alsheimer, M., Fecher, E. and Benavente, R. (1998) Nuclear envelope remodelling during rat spermiogenesis: distribution and expression pattern of LAP2/thymopoietins. J. Cell Sci., 111, 2227-2234.
2. Ashery-Padan, R., Weiss, A.M., Feinstein, N. and Gruenbaum, Y. (1997) Distinct regions specify the targeting of otefin to the nucleoplasmic side of the nuclear envelope. J. Biol. Chem., 272. 2493-2499.
3. Baricheva, E.A., Berrios, M., Bogachev, S.S., Borisevich, I.V., Lapik, E.R., Sharakhov, I.V, Stuurman, N. and Fisher, P.A. (1996) DNA from Drosophila melanogaster β-heterochromatin binds specifically to nuclear lamins in vitro and the nuclear envelope in situ. Gene, 171, 171-176.
4. Berger, R. et al. (1996) The characterization and localization of the mouse thymopoietin/lamina-associated polypeptide 2 gene and its alternatively spliced products. Genome Res., 6, 361-370.
5. 1 nuclei of human dermal fibroblasts. J. Cell Sci., 104, 297-306.
6. Burke, B. and Gerace, L. (1986) A cell free system to study reassembly of the nuclear envelope at the end of mitosis. Cell, 44, 639-652.
7. Dechat, T., Gotzmann, J., Stockinger, A., Harris, C.A., Talle, M.A., Siekierka, J.J. and Foisner, R. (1998) Detergent-salt resistance of LAP2α in interphase nuclei and phosphorylation-dependent association with chromosomes early in nuclear assembly implies functions in nuclear structure dynamics. EMBO J., 17, 4887-4902.
8. Foisner, R. and Gerace, L. (1993) Integral membrane proteins of the nuclear envelope interact with lamins and chromosomes and binding is modulated by mitotic phosphorylation. Cell, 73, 1267-1279.
9. Furukawa, K. (1999) LAP2 binding protein 1 (L2BP1/BAF) is a candidate mediator of LAP2-chromatin interaction. J. Cell Sci., 112, 2485-2492.
10. Furukawa, K., Pante, N., Aebi, U. and Gerace, L. (1995) Cloning of a cDNA for lamina-associated polypeptide 2 (LAP2) and identification of regions that specify targeting to the nuclear envelope. EMBO J., 14, 1626-1636.
11. Furukawa, K., Glass, C. and Kondo, T. (1997) Characterization of the chromatin binding activity of lamina-associated polypeptide (LAP) 2. Biochem. Biophys. Res. Commun., 238, 240-246.
12. Furukawa, K., Fritze, C.E. and 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.
13. Gant, T.M., Harris, C.A. and Wilson, K.L. (1999) Roles of LAP2 proteins in nuclear assembly and DNA replication: truncated LAP2β proteins alter lamina assembly, envelope formation, nuclear size and DNA replication efficiency in Xenopus laevis extracts. J. Cell Biol., 144, 1083-1096.
14. Glass, C.A., Glass, J.R., Taniura, H., Hasel, K.W., Blevitt, J.M. and Gerace, L. (1993) The α-helical rod domain of human lamins A and C contains a chromatin binding site. EMBO J., 12. 4413-4424.
15. Glass, J.R. and Gerace, L. (1990) Lamins A and C bind and assemble at the surface of mitotic chromosomes. J. Cell Biol., 111, 1047-1057.
16. Gossen, M. and Bujard, H. (1995) Efficacy of tetracycline-controlled gene expression is influenced by cell type: commentary. Biotechniques, 19, 213-216 (discussion 216-217).
17. Gossen, M., Freundlieb, S., Bender, G., Muller, G., Hillen, W. and Bujard, H. (1995) Transcriptional activation by tetracyclines in mammalian cells. Science, 268, 1766-1769.
18. Harris, C.A., Andryuk, P.J., Cline, S., Chan, H.K., Natarajan, A., Siekierka, J.J. and Goldstein, G. (1994) Three distinct human thymopoietins are derived from alternatively spliced mRNAs. Proc. Natl Acad. Sci. USA, 91, 6283-6287.
19. Harris, C.A., Andryuk, P.J., Cline, S.W., Mathew, S., Siekierka, J.J. and Goldstein, G. (1995) Structure and mapping of the human thymopoietin (TMPO) gene and relationship of human TMPO β to rat lamin-associated polypeptide 2. Genomics, 28, 198-205.
20. Hoger, T.H., Krohne, G. and Kleinschmidt, J.A. (1991) Interaction of Xenopus lamins A and LII with chromatin in vitro mediated by a sequence element in the carboxyterminal domain. Exp. Cell Res., 197, 280-289.
21. Hozak, P., Sasseville, A.M., Raymond, Y. and Cook, P.R. (1995) Lamin proteins form an internal nucleoskeleton as well as a peripheral lamina in human cells. J. Cell Sci., 108, 635-644.
22. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
23. Lamond, A.I. and Earnshaw, W.C. (1998) Structure and function in the nucleus. Science, 280, 547-553.
24. Loewinger, L. and McKeon, F. (1988) Mutations in the nuclear lamin proteins resulting in their aberrant assembly in the cytoplasm. EMBO J., 7, 2301-2309.
25. Luderus, M.E., de Graaf, A., Mattia, E., den Blaauwen, J.L., Grande, M.A., de Jong, L. and van Driel, R. (1992) Binding of matrix attachment regions to lamin B1. Cell, 70, 949-959.
26. Meier, J. and Georgatos, S.D. (1994) Type B lamins remain associated with the integral nuclear envelope protein p58 during mitosis: implications for nuclear reassembly. EMBO J., 13, 1888-1898.
27. Moir, R.D., Montag-Lowy, M. and Goldman, R.D. (1994) Dynamic properties of nuclear lamins: lamin B is associated with sites of DNA replication. J. Cell Biol., 125, 1201-1212.
28. Moir, R.D., Spann, T.P. and Goldman, R.D. (1995) The dynamic properties and possible functions of nuclear lamins. Int. Rev. Cytol, 162B, 141-182.
29. Neri, L.M., Raymond, Y., Giordano, A., Capitani, S. and Martelli, A.M. (1999) Lamin A is part of the internal nucleoskeleton of human erythroleukemia cells. J. Cell Physiol., 178, 284-295.
30. Nigg, E.A. (1997) Nucleocytoplasmic transport: signals, mechanisms and regulation. Nature, 386, 779-787.
31. Ohno, M., Fornerod, M. and Mattaj, I.W. (1998) Nucleocytoplasmic transport: the last 200 nanometers. Cell, 92, 327-336.
32. Pyrpasopoulou, A., Meier, J., Maison, C., Simos, G. and Georgatos, S.D. (1996) The lamin B receptor (LBR) provides essential chromatin docking sites at the nuclear envelope. EMBO J., 15, 7108-7119.
33. Rzepecki, R., Bogachev, S.S., Kokoza, E., Stuurman, N. and Fisher, P.A. (1998) In vivo association of lamins with nucleic acids in Drosophila melanogaster. J. Cell Sci., 111, 121-129.
34. Simos, G. and Georgatos, S.D. (1992) The inner nuclear membrane protein p58 associates in vivo with a p58 kinase and the nuclear lamins. EMBO J., 11, 4027-4036.
35. Soullam, B. and Worman, H.J. (1993) The amino-terminal domain of the lamin B receptor is a nuclear envelope targeting signal. J. Cell Biol., 120, 1093-1100.
36. Spann, T.P., Moir, R.D., Goldman, A.E., Stick, R. and Goldman, R.D. (1997) Disruption of nuclear lamin organization alters the distribution of replication factors and inhibits DNA synthesis. J. Cell Biol., 136, 1201-1212.
37. Taniura, H., Glass, C. and Gerace, L. (1995) A chromatin binding site in the tail domain of nuclear lamins that interacts with core histones. J. Cell Biol., 131, 33-44.
38. Worman, H.J., Evans, C.D. and Blobel,G. (1990) The lamin B receptor of the nuclear envelope inner membrane: a polytopic protein with eight potential transmembrane domains. J. Cell Biol., 111, 1535-1542.
39. Yang, L., Guan, T. and Gerace, L. (1997a) Integral membrane proteins of the nuclear envelope are dispersed throughout the endoplasmic reticulum during mitosis. J. Cell Biol., 137, 1199-1210.
40. Yang, L., Guan, T. and Gerace, L. (1997b) Lamin-binding fragment of LAP2 inhibits increase in nuclear volume during the cell cycle and progression into S phase. J. Cell Biol., 139, 1077-1087.
41. Ye, Q. and Worman, H.J. (1994) Primary structure analysis and lamin B and DNA binding of human LBR, an integral protein of the nuclear envelope inner membrane. J. Biol. Chem., 269, 11306-11311.
42. Ye, Q. and Worman, H.J. (1996) Interaction between an integral protein of the nuclear envelope inner membrane and human chromodomain proteins homologous to Drosophila HP1. J. Biol. Chem., 271, 14653-14656.
43. Ye, Q., Callebaut, I., Pezhman, A., Courvalin, J.C. and Worman, H.J. (1997) Domain-specific interactions of human HP1-type chromodomain proteins and inner nuclear membrane protein LBR. J. Biol. Chem., 272, 14983-14989.
44. Yuan, J., Simos, G., Blobel, G. and Georgatos, S.D. (1991) Binding of lamin A to polynucleosomes. J. Biol. Chem., 266, 9211-9215.
45. Zhao, K., Harel, A., Stuurman, N., Guedalia, D. and Gruenbaum, Y. (1996) Binding of matrix attachment regions to nuclear lamin is mediated by the rod domain and depends on the lamin polymerization state. FEBS Lett., 380, 161-164.