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

Journal of Cell Biology

Volumn 144, Issue 6, 1999, Pages 1083-1096

  Gant, Tracey Michele ^a,c   Harris, Crafford A ^b   Wilson, Katherine L ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b R W JOHNSON PHARMACEUTICAL RES I   (United States)

^c CALIFORNIA PACIFIC MEDICAL CENTER   (United States)

Author keywords

Chromatin structure; Emerin; MAN; Nuclear envelope; Prereplication complex

Indexed keywords

COMPLEMENTARY DNA; EMERIN; MEMBRANE PROTEIN;

ANIMAL CELL; ARTICLE; CELL NUCLEUS MEMBRANE; CELL NUCLEUS TRANSPLANTATION; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA REPLICATION; MEMBRANE BINDING; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN EXPRESSION; TRANSMISSION ELECTRON MICROSCOPY; XENOPUS LAEVIS;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BINDING SITES; CELL NUCLEUS; CELL-FREE SYSTEM; CHROMATIN; CLONING, MOLECULAR; DNA PRIMERS; DNA REPLICATION; DNA, COMPLEMENTARY; DNA-BINDING PROTEINS; FEMALE; HUMANS; LAMINS; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON; MOLECULAR SEQUENCE DATA; NUCLEAR ENVELOPE; NUCLEAR PROTEINS; OOCYTES; PEPTIDE FRAGMENTS; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; XENOPUS LAEVIS;

ANIMALIA; STAPHYLOCOCCUS PHAGE 187; XENOPUS LAEVIS;

EID: 0033594083     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.144.6.1083     Document Type: Article

References (76)

1. Alsheimer, M., E. Fecher, and R. Benavente. 1998. Nuclear envelope remodelling during rat spermiogenesis: distribution and expression pattern of LAP2/ thymopoietins. J. Cell Sci. 111:2227-2234.
2. Bauer, D.W., C. Murphy, Z. Wu, C.H. Wu, and J.G. Gall. 1994. In vitro assembly of coiled bodies in Xenopus egg extract. Mol. Biol. Cell. 5:633-644.
3. Bell, P., M.C. Dabauvalle, and U. Scheer. 1992. In vivo assembly of prenucleolar bodies in Xenopus egg extract. J. Cell Biol. 118:1297-1304.
4. Berger, R., L. Theodor, J. Shoham, E. Gokkel, F. Brok-Simoni, K.B. Avraham, N.G. Copeland, N.A. Jenkins, G. Rechavi, and A.J. Simon. 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. Bione, S., E. Maestrini, S. Rivella, M. Mancini, S. Regis, G. Romeo, and D. Toniolo. 1994. Identification of a novel X-linked gene responsible for Emery-Dreifuss muscular dystrophy. Nature Genet. 8:323-327.
6. Blow, J.J., and J.V. Watson. 1987. Nuclei act as independent and integrated units of replication in a Xenopus cell-free DNA replication system, EMBO (Eur. Mol. Biol. Organ.) J. 6:1997-2002.
7. Boman, A.L., M.R. Delannoy, and K.L. Wilson. 1992. GTP hydrolysis is required for vesicle fusion during nuclear envelope assembly in vitro. J. Cell Biol. 116:281-294.
8. Burke, B. 1990. On the cell-free association of lamins A and C with metaphase chromosomes. Exp. Cell Res. 186:169-176.
9. Chen, H., and A. Engelman. 1998. The barrier-to-autointegration protein is a host factor for HIV type 1 integration. Proc. Natl. Acad. Sci. USA. 95:15270-15274.
10. Cox, L.S. 1992. DNA replication in cell-free extracts from Xenopus eggs is prevented by disrupting nuclear envelope function. J. Cell Sci. 101:43-53.
11. Cox, L.S., and G.H. Leno. 1990. Extracts from eggs and oocytes of Xenopus laevis differ in their capacities for nuclear assembly and DNA replication. J. Cell Sci. 97:177-184.
12. Dechat, T., J. Gotzmann, A. Stockinger, C.A. Harris, M.A. Talle, J.J. Siekierka, and R. Foisner. 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.
13. Dillin, A., and J. Rine. 1998. Roles for ORC in M phase and S phase. Science. 279:1733-1737.
14. Elgin, S.C. 1996. Heterochromatin and gene regulation in Drosophila. Curr. Opin. Genet. Dev. 6:193-202.
15. Ellis, D.J., W.G.F. Whitfield, and C.J. Hutchison. 1997. GST-lamin fusion proteins act as dominant negative mutants in Xenopus egg extracts and reveal the function of the lamina in DNA replication. J. Cell Sci. 110:2507-2518.
16. Finlay, D.R., and D.J. Forbes. 1990. Reconstitution of biochemically altered nuclear pores: transport can be eliminated and restored. Cell. 60:17-29.
17. Foisner, R., and L. Gerace. 1993. Integral membrane proteins of the nuclear envelope interact with lamins and chromosomes, and binding is modulated by mitotic phosphorylation. Cell. 73:1267-1279.
18. Fricker, M., M. Hollinshead, N. White, and D. Vaux. 1997. Interphase nuclei of many mammalian cell types contain deep, dynamic, tubular membrane-bound invaginations of the nuclear envelope. J. Cell Biol. 136:531-544.
19. Furukawa, K. 1999. LAP2 binding protein 1 (L2BP1/BAF) is a candidate mediator of LAP2-chromatin interaction. J. Cell Sci. In press.
20. Furukawa, K., N. Panté, U. Aebi, and L. Gerace. 1995. Cloning of a cDNA for lamina-associated polypeptide 2 (LAP2) and identification of regions that specify targeting to the nuclear envelope. EMBO (Eur. Mol. Biol. Organ.) J. 14:1626-1636.
21. Furukawa, K., C.E. Fritze, and L. Gerace. 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.
22. Gant, T.M., and K.L. Wilson. 1997. Nuclear assembly. Ann. Rev. Cell Dev. Biol. 13:669-695.
23. Gerace, L., and R. Foisner. 1994. Integral membrane proteins and dynamic organization of the nuclear envelope. Trends Cell Biol. 4:127-131.
24. Glass, C.A., J.R. Glass, H. Taniura, K.W. Hasel, J.M. Blevitt, and L. Gerace. 1993. The alpha-helical rod domain of human lamins A and C contains a chromatin binding site. EMBO (Eur. Mol. Biol. Organ.) J. 12:4413-4424.
25. Harris, C.A., P.J. Andryuk, S. Cline, H.K. Chan, A. Natarajan, J.J. Siekierka, and G. Goldstein. 1994. Three distinct human thymopoietins are derived from alternatively spliced mRNAs. Proc. Natl. Acad. Sci. USA. 91:6283-6287.
26. Harris, C.A., P.J. Andryuk, S.W. Cline, S. Mathew, J.J. Siekierka, and G. Goldstein. 1995. Structure and mapping of the human thymopoietin (TMPO) gene and relationship of human TMPO beta to rat lamin-associated polypeptide 2. Genomics. 28:198-205.
27. Hozak, P., D.A. Jackson, and P.R. Cook. 1994. Replication factories and nuclear bodies: the ultrastructural characterization of replication sites during the cell cycle. J. Cell Sci. 107:2191-2202.
28. Hua, X.H., and J. Newport. 1998. Identification of a preinitiation step in DNA replication that is independent of origin recognition complex and cdc6, but dependent on cdk2. J. Cell Biol. 140:271-281.
29. Hua, X.H., H. Yan, and J. Newport. 1997. A role for cdk2 kinase in negatively regulating DNA replication during S phase of the cell cycle. J. Cell Biol. 137: 183-192.
30. Hutchison, C.J., J.M. Bridger, L.S. Cox, and I.R. Kill. 1994. Weaving a pattern from disparate threads: lamin function in nuclear assembly and DNA replication. J. Cell Sci. 107:3259-3269.
31. Ikegami, S., T. Taguchi, M. Ohashi, M. Oguro, H. Nagano, and Y. Mano. 1978. Aphidicolin prevents mitotic cell division by interfering with the activity of DNA polymerase-α. Nature. 275:458-460.
32. Ishijima, Y., T. Toda, H. Matsushita, M. Yoshida, and N. Kimura. 1996. Expression of thymopoietin beta/lamina-associated polypeptide 2 (TP beta/LAP2) and its family proteins as revealed by specific antibody induced against recombinant human thymopoietin. Biochem. Biophys. Res. Commun. 226: 431-438.
33. Jallepali, P.V., and T.J. Kelly. 1997. Cyclin-dependent kinase and initiation at eukaryotic origins: a replication switch? Curr. Opin. Cell Biol. 9:358-363.
34. Jenkins, H., T. Holman, C. Lyon, B. Lane, R. Stick, and C. Hutchison. 1993. Nuclei that lack a lamina accumulate karyophilic proteins and assemble a nuclear matrix. J. Cell Sci. 106:275-285.
35. Lamond, A.I., and W.C. Earnshaw. 1998. Structure and function in the nucleus. Science. 280:547-553.
36. Lawlis, S.J., S.M. Keezer, J.-R. Wu, and D.M. Gilbert. 1996. Chromosome architecture can dictate site-specific initiation of DNA replication in Xenopus egg extracts. J. Cell Biol. 135:1207-1218.
37. Lee, M.S., and R. Craigie. 1998. A previously unidentified host protein protects retroviral DNA from autointegration. Proc. Natl. Acad Sci. USA. 95:1528-1533.
38. Leno, G.H., and R.A. Laskey. 1991. DNA replication in cell-free extracts from Xenopus laevis. Methods Cell Biol. 36:561-579.
39. Lohka, M.J., and Y. Masui. 1983. The germinal vesicle material required for sperm pronuclear formation is located in the soluble fraction of egg cytoplasm. Exp. Cell Res. 148:481-491.
40. Lorka, T., F.H. Cruzalegui, D. Fesquet, J.-C. Cavadore, J. Méry, A. Means, and M. Dorée. 1993. Calmodulin-dependent protein kinase 11 mediates inactivation of MPF and CSF upon fertilization of Xenopus eggs. Nature. 366:270-273.
41. Lourim, D., and G. Krohne. 1993. Membrane-associated lamins in Xenopus egg extracts: identification of two vesicle populations. J. Cell Biol. 123:501-512.
42. Lourim, D., A. Kempf, and G. Krohne. 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.
43. Maison, C., A. Pyrpasopoulou, P.A. Theodoropoulos, and S.D. Georgatos. 1997. The inner nuclear membrane protein LAP1 forms a native complex with B-type lamins and partitions with spindle-associated mitotic vesicles. EMBO (Eur. Mol. Biol. Org.) J. 16:4839-4850.
44. Manilal, S., N.T. Man, C.A. Sewry, and G.E. Morris. 1996. The Emery-Dreifuss muscular dystrophy protein, emerin, is a nuclear membrane protein. Hum. Mol. Genet. 5:801-808.
45. Martin, L., C. Crimaudo, and L. Gerace. 1995. cDNA cloning and characterization of lamina-associated polypeptide 1C (LAP1C), an integral protein of the inner nuclear membrane. J. Biol. Chem. 270:8822-8828.
46. Masui, Y. 1996. A quest for cytoplasmic factors that control the cell cycle. Prog. Cell Cycle Res. 2:1-13.
47. Meier, J., K.H. Campbell, C.C. Ford, R. Stick, and C.J. Hutchison. 1991. The role of lamin LIII in nuclear assembly and DNA replication, in cell-free extracts of Xenopus eggs. J. Cell Sci. 98:271-279.
48. Mills, A.D., J.J. Blow, J.G. White, W.B. Amos, D. Wilcock, and R.A. Laskey. 1989. Replication occurs at discrete foci spaced throughout nuclei replicating in vitro. J. Cell Sci. 94:471-477.
49. Moir, R.D., M. Montag-Lowy, and R.D. Goldman. 1994. Dynamic properties of nuclear lamins: lamin B is associated with sites of DNA replication. J. Cell Biol. 125:1201-1212.
50. Nagano, A., R. Koga, M. Ogawa, Y. Kurano, J. Kawada, R. Okada, Y.K. Hayashi, T. Tsukahara, and K. Arahata. 1996. Emerin deficiency at the nuclear membrane in patients with Emery-Dreifuss muscular dystrophy. Nat. Genet. 12:254-259.
51. Newmeyer, D.D., and K.L. Wilson. 1991. Egg extracts for nuclear import and nuclear assembly reactions. Methods Cell Biol. 36:607-634.
52. Newmeyer, D.D., D.R. Finlay, and D.J. Forbes. 1986. In vitro transport of a fluorescent nuclear protein and exclusion of non-nuclear proteins. J. Cell Biol. 103:2091-2102.
53. Newport, J., and W. Dunphy. 1992. Characterization of the membrane binding and fusion events during nuclear envelope assembly using purified components. J. Cell Biol. 116:295-306.
54. Newport, J.W., K.L. Wilson, and W.G. Dunphy. 1990. A lamin-independent pathway for nuclear envelope assembly. J. Cell Biol. 111:2247-2259.
55. Nikolakaki, E., G. Simos, S.D. Georgatos, and T. Giannakouros. 1996. A nuclear envelope-associated kinase phosphorylates arginine-serine motifs and modulates interactions between the lamin B receptor and other nuclear proteins. J. Biol. Chem. 271:8365-8372.
56. Ohno, M., M. Fornerod, and I.W. Mattaj. 1998. Nucleocytoplasmic transport: the last 200 nanometers. Cell. 92:327-336.
57. Pak, D.T.S., M. Pflumm, I. Chesnokov, D.W. Huang, R. Kellum, J. Marr, P. Romanowski, and M.R. Botchan. 1997. Association of the origin replication complex with heterochromatin and HP1 in higher eukaryotes. Cell. 91:311-323.
58. Paulin-Levasseur, M., D.L. Blake, M. Julien, and L. Rouleau. 1996. The MAN antigens are non-lamin constituents of the nuclear lamina in vertebrate cells. Chromosoma. 104:367-379.
59. Powers, M.A., C. Macaulay, F.R. Masiarz, and D.J. Forbes. 1995. Reconstituted nuclei depleted of a vertebrate GLFG nuclear pore protein, p97, import but are defective in nuclear growth and replication. J. Cell Biol. 128:721-736.
60. Pyrpasopoulou, A., J. Meier, C. Maison, G. Simos, and S.D. Georgatos. 1996. The lamin B receptor (LBR) provides essential chromatin docking sites at the nuclear envelope. EMBO (Eur. Mol. Biol. Org.) J. 15:7108-7119.
61. Schmidt, M., M. Tschodrich-Rotter, R. Peters, and G. Krohne. 1994. Properties of fluorescently labeled Xenopus lamin A in vivo. Eur. J. Cell Biol. 65:70-81.
62. Simos, G., and S.D. Georgatos. 1992. The inner nuclear membrane protein p58 associates in vivo with a p58 kinase and the nuclear lamins. EMBO (Eur. Mol. Biol. Org.) J. 11:4027-4036.
63. Spann, T.P., R.D. Moir, A.E. Goldman, R. Stick, and R.D. Goldman. 1997. Disruption of nuclear lamin organization alters the distribution of replication factors and inhibits DNA synthesis. J. Cell Biol. 136:1201-1212.
64. Stillman, B. 1996. Cell cycle control of DNA replication. Science. 274:1659-1664.
65. Taniura, H., C. Glass, and L. Gerace. 1995. A chromatin binding site in the tail domain of nuclear lamins that interacts with core histones. J. Cell Biol. 131: 33-44.
66. Walter, J., L. Sun, and J. Newport. 1998. Regulated chromosomal DNA replication in the absence of a nucleus. Molec. Cell 1:519-529.
67. Weast, R.C. 1967. Handbook of Chemistry and Physics. 48th edition. Chemical Rubber Publishing Co. Cleveland, OH. D-144. D-149.
68. Wiese, C., M.W. Goldberg, T.D. Allen, and K.L. Wilson. 1997. Nuclear envelope assembly in Xenopus extracts visualized by scanning EM reveals a transport-dependent "envelope smoothing" event. J. Cell Sci. 110:1489-1502.
69. Wilson, K.L., and J. Newport. 1988. A trypsin-sensitive receptor on membrane vesicles is required for nuclear envelope formation in vitro. J. Cell Biol. 107: 57-68.
70. Wilson, K.L., and C. Wiese. 1996. Reconstituting the nuclear envelope and endoplasmic reticulum in vitro. Sem. Cell Dev. Biol. 7:487-496.
71. Worman, H.J., J. Yuan, G. Blobel, and S.D. Georgatos. 1988. A lamin B receptor in the nuclear envelope. Proc. Natl. Acad. Sci. USA. 85:8531-8534.
72. Worman, H.J., C.D. Evans, and G. Blobel. 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.
73. Yang, L., T. Guan, and L. Gerace. 1997. 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.
74. Ye, Q., and H.J. Worman. 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.
75. Ye, Q., and H.J. Worman. 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.
76. Ye, Q., I. Callebaut, A. Pezhman, J.C. Courvalin, and H.J. Worman. 1997. Domain-specific interactions of human HP1-type chromodomain proteins and inner nuclear membrane protein LBR. J. Biol. Chem. 272:14983-14989.