Abstract
We have identified an integral membrane protein of sea urchin gametes with an apparent molecular mass of 56 kD that cross-reacts with an antibody against the nucleoplasmic NH2-terminal domain of human lamin B receptor (LBR). In mature sperm, p56 is located at the tip and base of the nucleus from where it is removed by egg cytosol in vitro. In the egg, p56 is present in a subset of cytoplasmic membranes (MV2 beta) which contributes the bulk of the nuclear envelope during male pronuclear formation. p56-containing vesicles are required for nuclear envelope assembly and have a chromatin-binding capacity that is mediated by p56. Lamin B is not present in these vesicles and is imported into the nucleus from a soluble pool at a later stage of pronuclear formation. Lamin B incorporation and addition of new membranes are necessary for pronuclear swelling and nuclear envelope growth. We suggest that p56 is a sea urchin LBR homologue that targets membranes to chromatin and later anchors the membrane to the lamina.
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- 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]
- Appelbaum J., Blobel G., Georgatos S. D. In vivo phosphorylation of the lamin B receptor. Binding of lamin B to its nuclear membrane receptor is affected by phosphorylation. J Biol Chem. 1990 Mar 15;265(8):4181–4184. [PubMed] [Google Scholar]
- Bailer S. M., Eppenberger H. M., Griffiths G., Nigg E. A. Characterization of A 54-kD protein of the inner nuclear membrane: evidence for cell cycle-dependent interaction with the nuclear lamina. J Cell Biol. 1991 Aug;114(3):389–400. doi: 10.1083/jcb.114.3.389. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Burke B., Gerace L. A cell free system to study reassembly of the nuclear envelope at the end of mitosis. Cell. 1986 Feb 28;44(4):639–652. doi: 10.1016/0092-8674(86)90273-4. [DOI] [PubMed] [Google Scholar]
- Cameron L. A., Poccia D. L. In vitro development of the sea urchin male pronucleus. Dev Biol. 1994 Apr;162(2):568–578. doi: 10.1006/dbio.1994.1110. [DOI] [PubMed] [Google Scholar]
- Chaudhary N., Courvalin J. C. Stepwise reassembly of the nuclear envelope at the end of mitosis. J Cell Biol. 1993 Jul;122(2):295–306. doi: 10.1083/jcb.122.2.295. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Collas P., Pinto-Correia C., Poccia D. L. Lamin dynamics during sea urchin male pronuclear formation in vitro. Exp Cell Res. 1995 Aug;219(2):687–698. doi: 10.1006/excr.1995.1280. [DOI] [PubMed] [Google Scholar]
- Collas P., Poccia D. Distinct egg membrane vesicles differing in binding and fusion properties contribute to sea urchin male pronuclear envelopes formed in vitro. J Cell Sci. 1996 Jun;109(Pt 6):1275–1283. doi: 10.1242/jcs.109.6.1275. [DOI] [PubMed] [Google Scholar]
- Collas P., Poccia D. Lipophilic organizing structures of sperm nuclei target membrane vesicle binding and are incorporated into the nuclear envelope. Dev Biol. 1995 May;169(1):123–135. doi: 10.1006/dbio.1995.1132. [DOI] [PubMed] [Google Scholar]
- Courvalin J. C., Lassoued K., Worman H. J., Blobel G. Identification and characterization of autoantibodies against the nuclear envelope lamin B receptor from patients with primary biliary cirrhosis. J Exp Med. 1990 Sep 1;172(3):961–967. doi: 10.1084/jem.172.3.961. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Courvalin J. C., Segil N., Blobel G., Worman H. J. The lamin B receptor of the inner nuclear membrane undergoes mitosis-specific phosphorylation and is a substrate for p34cdc2-type protein kinase. J Biol Chem. 1992 Sep 25;267(27):19035–19038. [PubMed] [Google Scholar]
- Dabauvalle M. C., Schulz B., Scheer U., Peters R. Inhibition of nuclear accumulation of karyophilic proteins in living cells by microinjection of the lectin wheat germ agglutinin. Exp Cell Res. 1988 Jan;174(1):291–296. doi: 10.1016/0014-4827(88)90163-2. [DOI] [PubMed] [Google Scholar]
- Dwyer N., Blobel G. A modified procedure for the isolation of a pore complex-lamina fraction from rat liver nuclei. J Cell Biol. 1976 Sep;70(3):581–591. doi: 10.1083/jcb.70.3.581. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Finlay D. R., Newmeyer D. D., Price T. M., Forbes D. J. Inhibition of in vitro nuclear transport by a lectin that binds to nuclear pores. J Cell Biol. 1987 Feb;104(2):189–200. doi: 10.1083/jcb.104.2.189. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- 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]
- Gerace L., Blobel G. The nuclear envelope lamina is reversibly depolymerized during mitosis. Cell. 1980 Jan;19(1):277–287. doi: 10.1016/0092-8674(80)90409-2. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Harris C. A., Andryuk P. J., Cline S., Chan H. K., Natarajan A., Siekierka J. J., Goldstein G. Three distinct human thymopoietins are derived from alternatively spliced mRNAs. Proc Natl Acad Sci U S A. 1994 Jul 5;91(14):6283–6287. doi: 10.1073/pnas.91.14.6283. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hinshaw J. E., Carragher B. O., Milligan R. A. Architecture and design of the nuclear pore complex. Cell. 1992 Jun 26;69(7):1133–1141. doi: 10.1016/0092-8674(92)90635-p. [DOI] [PubMed] [Google Scholar]
- Holy J., Wessel G., Berg L., Gregg R. G., Schatten G. Molecular characterization and expression patterns of a B-type nuclear lamin during sea urchin embryogenesis. Dev Biol. 1995 Apr;168(2):464–478. doi: 10.1006/dbio.1995.1095. [DOI] [PubMed] [Google Scholar]
- Longo F. J., Anderson E. The fine structure of pronuclear development and fusion in the sea urchin, Arbacia punctulata. J Cell Biol. 1968 Nov;39(2):339–368. doi: 10.1083/jcb.39.2.339. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lourim D., Krohne G. Lamin-dependent nuclear envelope reassembly following mitosis: an argument. Trends Cell Biol. 1994 Sep;4(9):314–318. doi: 10.1016/0962-8924(94)90228-3. [DOI] [PubMed] [Google Scholar]
- Lourim D., Krohne G. Membrane-associated lamins in Xenopus egg extracts: identification of two vesicle populations. J Cell Biol. 1993 Nov;123(3):501–512. doi: 10.1083/jcb.123.3.501. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Martin L., Crimaudo C., Gerace L. cDNA cloning and characterization of lamina-associated polypeptide 1C (LAP1C), an integral protein of the inner nuclear membrane. J Biol Chem. 1995 Apr 14;270(15):8822–8828. doi: 10.1074/jbc.270.15.8822. [DOI] [PubMed] [Google Scholar]
- Matsuura S., Masuda R., Omori K., Negishi M., Tashiro Y. Distribution and induction of cytochrome P-450 in rat liver nuclear envelope. J Cell Biol. 1981 Oct;91(1):212–220. doi: 10.1083/jcb.91.1.212. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Meier J., Campbell K. H., Ford C. C., Stick R., Hutchison C. J. The role of lamin LIII in nuclear assembly and DNA replication, in cell-free extracts of Xenopus eggs. J Cell Sci. 1991 Mar;98(Pt 3):271–279. doi: 10.1242/jcs.98.3.271. [DOI] [PubMed] [Google Scholar]
- Meier J., Georgatos S. D. Type B lamins remain associated with the integral nuclear envelope protein p58 during mitosis: implications for nuclear reassembly. EMBO J. 1994 Apr 15;13(8):1888–1898. doi: 10.1002/j.1460-2075.1994.tb06458.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Newport J. W., Wilson K. L., Dunphy W. G. A lamin-independent pathway for nuclear envelope assembly. J Cell Biol. 1990 Dec;111(6 Pt 1):2247–2259. doi: 10.1083/jcb.111.6.2247. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nikolakaki E., Simos G., Georgatos S. D., Giannakouros T. A nuclear envelope-associated kinase phosphorylates arginine-serine motifs and modulates interactions between the lamin B receptor and other nuclear proteins. J Biol Chem. 1996 Apr 5;271(14):8365–8372. doi: 10.1074/jbc.271.14.8365. [DOI] [PubMed] [Google Scholar]
- Poccia D. L., Green G. R. Nuclei and chromosomal proteins. Methods Cell Biol. 1986;27:153–174. doi: 10.1016/s0091-679x(08)60347-7. [DOI] [PubMed] [Google Scholar]
- Schuler E., Lin F., Worman H. J. Characterization of the human gene encoding LBR, an integral protein of the nuclear envelope inner membrane. J Biol Chem. 1994 Apr 15;269(15):11312–11317. [PubMed] [Google Scholar]
- Sheehan M. A., Mills A. D., Sleeman A. M., Laskey R. A., Blow J. J. Steps in the assembly of replication-competent nuclei in a cell-free system from Xenopus eggs. J Cell Biol. 1988 Jan;106(1):1–12. doi: 10.1083/jcb.106.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Simos G., Georgatos S. D. The inner nuclear membrane protein p58 associates in vivo with a p58 kinase and the nuclear lamins. EMBO J. 1992 Nov;11(11):4027–4036. doi: 10.1002/j.1460-2075.1992.tb05496.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Smith S., Blobel G. Colocalization of vertebrate lamin B and lamin B receptor (LBR) in nuclear envelopes and in LBR-induced membrane stacks of the yeast Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1994 Oct 11;91(21):10124–10128. doi: 10.1073/pnas.91.21.10124. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Soullam B., Worman H. J. Signals and structural features involved in integral membrane protein targeting to the inner nuclear membrane. J Cell Biol. 1995 Jul;130(1):15–27. doi: 10.1083/jcb.130.1.15. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Soullam B., Worman H. J. The amino-terminal domain of the lamin B receptor is a nuclear envelope targeting signal. J Cell Biol. 1993 Mar;120(5):1093–1100. doi: 10.1083/jcb.120.5.1093. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ulitzur N., Harel A., Feinstein N., Gruenbaum Y. Lamin activity is essential for nuclear envelope assembly in a Drosophila embryo cell-free extract. J Cell Biol. 1992 Oct;119(1):17–25. doi: 10.1083/jcb.119.1.17. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vigers G. P., Lohka M. J. A distinct vesicle population targets membranes and pore complexes to the nuclear envelope in Xenopus eggs. J Cell Biol. 1991 Feb;112(4):545–556. doi: 10.1083/jcb.112.4.545. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wilson K. L., Newport J. A trypsin-sensitive receptor on membrane vesicles is required for nuclear envelope formation in vitro. J Cell Biol. 1988 Jul;107(1):57–68. doi: 10.1083/jcb.107.1.57. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Worman H. J., Yuan J., Blobel G., Georgatos S. D. A lamin B receptor in the nuclear envelope. Proc Natl Acad Sci U S A. 1988 Nov;85(22):8531–8534. doi: 10.1073/pnas.85.22.8531. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ye Q., Worman H. J. Interaction between an integral protein of the nuclear envelope inner membrane and human chromodomain proteins homologous to Drosophila HP1. J Biol Chem. 1996 Jun 21;271(25):14653–14656. doi: 10.1074/jbc.271.25.14653. [DOI] [PubMed] [Google Scholar]
- Ye Q., Worman H. J. Primary structure analysis and lamin B and DNA binding of human LBR, an integral protein of the nuclear envelope inner membrane. J Biol Chem. 1994 Apr 15;269(15):11306–11311. [PubMed] [Google Scholar]