Abstract
Recently, it has been suggested that nuclear processes, such as replication, transcription, and splicing, are spatially organized and associated with a nuclear framework called the nuclear matrix, a structure of unknown molecular composition. It has been shown that chromatin is attached to the nuclear matrix via specific DNA fragments called matrix attachment regions (MARs). We have begun to dissect the plant nuclear matrix by isolating a DNA binding protein with specific affinity for MARs. Here, it is shown that MAR binding filament-like protein 1 (MFP1) is associated with specklelike structures at the nuclear periphery that are part of isolated nuclei and the nuclear matrix. A predicted N-terminal transmembrane domain is necessary for the specific targeting of MFP1 to the speckles, indicating an association with the nuclear envelope-endoplasmic reticulum continuum. In addition, it is shown that a marker protein for plant microtubule organizing centers, which has been shown to be localized on the outside of the plant nuclear envelope, is also part of the nuclear matrix. These findings indicate a close and previously undescribed connection in plants between the nuclear envelope and the internal nuclear matrix, and they suggest a function for MFP1 in attaching chromatin to specific sites at the nuclear periphery.
Full Text
The Full Text of this article is available as a PDF (344.4 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Allen G. C., Hall G. E., Jr, Childs L. C., Weissinger A. K., Spiker S., Thompson W. F. Scaffold attachment regions increase reporter gene expression in stably transformed plant cells. Plant Cell. 1993 Jun;5(6):603–613. doi: 10.1105/tpc.5.6.603. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Allen G. C., Hall G., Jr, Michalowski S., Newman W., Spiker S., Weissinger A. K., Thompson W. F. High-level transgene expression in plant cells: effects of a strong scaffold attachment region from tobacco. Plant Cell. 1996 May;8(5):899–913. doi: 10.1105/tpc.8.5.899. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Berezney R., Coffey D. S. Identification of a nuclear protein matrix. Biochem Biophys Res Commun. 1974 Oct 23;60(4):1410–1417. doi: 10.1016/0006-291x(74)90355-6. [DOI] [PubMed] [Google Scholar]
- Boevink P., Oparka K., Santa Cruz S., Martin B., Betteridge A., Hawes C. Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network. Plant J. 1998 Aug;15(3):441–447. doi: 10.1046/j.1365-313x.1998.00208.x. [DOI] [PubMed] [Google Scholar]
- Bretscher M. S., Munro S. Cholesterol and the Golgi apparatus. Science. 1993 Sep 3;261(5126):1280–1281. doi: 10.1126/science.8362242. [DOI] [PubMed] [Google Scholar]
- Chevrier V., Komesli S., Schmit A. C., Vantard M., Lambert A. M., Job D. A monoclonal antibody, raised against mammalian centrosomes and screened by recognition of plant microtubule organizing centers, identifies a pericentriolar component in different cell types. J Cell Sci. 1992 Apr;101(Pt 4):823–835. doi: 10.1242/jcs.101.4.823. [DOI] [PubMed] [Google Scholar]
- Compton D. A., Cleveland D. W. NuMA is required for the proper completion of mitosis. J Cell Biol. 1993 Feb;120(4):947–957. doi: 10.1083/jcb.120.4.947. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Davis L. I. The nuclear pore complex. Annu Rev Biochem. 1995;64:865–896. doi: 10.1146/annurev.bi.64.070195.004245. [DOI] [PubMed] [Google Scholar]
- Davis S. J., Vierstra R. D. Soluble, highly fluorescent variants of green fluorescent protein (GFP) for use in higher plants. Plant Mol Biol. 1998 Mar;36(4):521–528. doi: 10.1023/a:1005991617182. [DOI] [PubMed] [Google Scholar]
- Dickinson L. A., Joh T., Kohwi Y., Kohwi-Shigematsu T. A tissue-specific MAR/SAR DNA-binding protein with unusual binding site recognition. Cell. 1992 Aug 21;70(4):631–645. doi: 10.1016/0092-8674(92)90432-c. [DOI] [PubMed] [Google Scholar]
- Ellenberg J., Siggia E. D., Moreira J. E., Smith C. L., Presley J. F., Worman H. J., Lippincott-Schwartz J. Nuclear membrane dynamics and reassembly in living cells: targeting of an inner nuclear membrane protein in interphase and mitosis. J Cell Biol. 1997 Sep 22;138(6):1193–1206. doi: 10.1083/jcb.138.6.1193. [DOI] [PMC free article] [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]
- Galili G., Sengupta-Gopalan C., Ceriotti A. The endoplasmic reticulum of plant cells and its role in protein maturation and biogenesis of oil bodies. Plant Mol Biol. 1998 Sep;38(1-2):1–29. [PubMed] [Google Scholar]
- Grebenok R. J., Pierson E., Lambert G. M., Gong F. C., Afonso C. L., Haldeman-Cahill R., Carrington J. C., Galbraith D. W. Green-fluorescent protein fusions for efficient characterization of nuclear targeting. Plant J. 1997 Mar;11(3):573–586. doi: 10.1046/j.1365-313x.1997.11030573.x. [DOI] [PubMed] [Google Scholar]
- Göhring F., Schwab B. L., Nicotera P., Leist M., Fackelmayer F. O. The novel SAR-binding domain of scaffold attachment factor A (SAF-A) is a target in apoptotic nuclear breakdown. EMBO J. 1997 Dec 15;16(24):7361–7371. doi: 10.1093/emboj/16.24.7361. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Görlich D., Mattaj I. W. Nucleocytoplasmic transport. Science. 1996 Mar 15;271(5255):1513–1518. doi: 10.1126/science.271.5255.1513. [DOI] [PubMed] [Google Scholar]
- Hall G., Jr, Allen G. C., Loer D. S., Thompson W. F., Spiker S. Nuclear scaffolds and scaffold-attachment regions in higher plants. Proc Natl Acad Sci U S A. 1991 Oct 15;88(20):9320–9324. doi: 10.1073/pnas.88.20.9320. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Haseloff J., Siemering K. R., Prasher D. C., Hodge S. Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. Proc Natl Acad Sci U S A. 1997 Mar 18;94(6):2122–2127. doi: 10.1073/pnas.94.6.2122. [DOI] [PMC free article] [PubMed] [Google Scholar]
- He D. C., Nickerson J. A., Penman S. Core filaments of the nuclear matrix. J Cell Biol. 1990 Mar;110(3):569–580. doi: 10.1083/jcb.110.3.569. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Heese-Peck A., Raikhel N. V. The nuclear pore complex. Plant Mol Biol. 1998 Sep;38(1-2):145–162. [PubMed] [Google Scholar]
- Hicks G. R., Smith H. M., Lobreaux S., Raikhel N. V. Nuclear import in permeabilized protoplasts from higher plants has unique features. Plant Cell. 1996 Aug;8(8):1337–1352. doi: 10.1105/tpc.8.8.1337. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Knebel W., Quader H., Schnepf E. Mobile and immobile endoplasmic reticulum in onion bulb epidermis cells: short- and long-term observations with a confocal laser scanning microscope. Eur J Cell Biol. 1990 Aug;52(2):328–340. [PubMed] [Google Scholar]
- 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]
- 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]
- Lydersen B. K., Pettijohn D. E. Human-specific nuclear protein that associates with the polar region of the mitotic apparatus: distribution in a human/hamster hybrid cell. Cell. 1980 Nov;22(2 Pt 2):489–499. doi: 10.1016/0092-8674(80)90359-1. [DOI] [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]
- McNulty A. K., Saunders M. J. Purification and immunological detection of pea nuclear intermediate filaments: evidence for plant nuclear lamins. J Cell Sci. 1992 Oct;103(Pt 2):407–414. doi: 10.1242/jcs.103.2.407. [DOI] [PubMed] [Google Scholar]
- Meier I., Phelan T., Gruissem W., Spiker S., Schneider D. MFP1, a novel plant filament-like protein with affinity for matrix attachment region DNA. Plant Cell. 1996 Nov;8(11):2105–2115. doi: 10.1105/tpc.8.11.2105. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mewes H. W., Hani J., Pfeiffer F., Frishman D. MIPS: a database for protein sequences and complete genomes. Nucleic Acids Res. 1998 Jan 1;26(1):33–37. doi: 10.1093/nar/26.1.33. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mirkovitch J., Mirault M. E., Laemmli U. K. Organization of the higher-order chromatin loop: specific DNA attachment sites on nuclear scaffold. Cell. 1984 Nov;39(1):223–232. doi: 10.1016/0092-8674(84)90208-3. [DOI] [PubMed] [Google Scholar]
- Mlynarova L., Keizer LCP., Stiekema W. J., Nap J. P. Approaching the Lower Limits of Transgene Variability. Plant Cell. 1996 Sep;8(9):1589–1599. doi: 10.1105/tpc.8.9.1589. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mínguez A., Moreno Díaz de la Espina S. Immunological characterization of lamins in the nuclear matrix of onion cells. J Cell Sci. 1993 Sep;106(Pt 1):431–439. doi: 10.1242/jcs.106.1.431. [DOI] [PubMed] [Google Scholar]
- Nielsen H., Engelbrecht J., Brunak S., von Heijne G. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 1997 Jan;10(1):1–6. doi: 10.1093/protein/10.1.1. [DOI] [PubMed] [Google Scholar]
- Pedrazzini E., Villa A., Borgese N. A mutant cytochrome b5 with a lengthened membrane anchor escapes from the endoplasmic reticulum and reaches the plasma membrane. Proc Natl Acad Sci U S A. 1996 Apr 30;93(9):4207–4212. doi: 10.1073/pnas.93.9.4207. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Renz A., Fackelmayer F. O. Purification and molecular cloning of the scaffold attachment factor B (SAF-B), a novel human nuclear protein that specifically binds to S/MAR-DNA. Nucleic Acids Res. 1996 Mar 1;24(5):843–849. doi: 10.1093/nar/24.5.843. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Restrepo-Hartwig M. A., Ahlquist P. Brome mosaic virus helicase- and polymerase-like proteins colocalize on the endoplasmic reticulum at sites of viral RNA synthesis. J Virol. 1996 Dec;70(12):8908–8916. doi: 10.1128/jvi.70.12.8908-8916.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schaad M. C., Jensen P. E., Carrington J. C. Formation of plant RNA virus replication complexes on membranes: role of an endoplasmic reticulum-targeted viral protein. EMBO J. 1997 Jul 1;16(13):4049–4059. doi: 10.1093/emboj/16.13.4049. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schafer W. R., Rine J. Protein prenylation: genes, enzymes, targets, and functions. Annu Rev Genet. 1992;26:209–237. doi: 10.1146/annurev.ge.26.120192.001233. [DOI] [PubMed] [Google Scholar]
- Schmit A. C., Stoppin V., Chevrier V., Job D., Lambert A. M. Cell cycle dependent distribution of a centrosomal antigen at the perinuclear MTOC or at the kinetochores of higher plant cells. Chromosoma. 1994 Sep;103(5):343–351. doi: 10.1007/BF00417882. [DOI] [PubMed] [Google Scholar]
- Spiker S., Thompson W. F. Nuclear Matrix Attachment Regions and Transgene Expression in Plants. Plant Physiol. 1996 Jan;110(1):15–21. doi: 10.1104/pp.110.1.15. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Staehelin L. A. The plant ER: a dynamic organelle composed of a large number of discrete functional domains. Plant J. 1997 Jun;11(6):1151–1165. doi: 10.1046/j.1365-313x.1997.11061151.x. [DOI] [PubMed] [Google Scholar]
- Stoppin V., Lambert A. M., Vantard M. Plant microtubule-associated proteins (MAPs) affect microtubule nucleation and growth at plant nuclei and mammalian centrosomes. Eur J Cell Biol. 1996 Jan;69(1):11–23. [PubMed] [Google Scholar]
- Stoppin V., Vantard M., Schmit A. C., Lambert A. M. Isolated Plant Nuclei Nucleate Microtubule Assembly: The Nuclear Surface in Higher Plants Has Centrosome-like Activity. Plant Cell. 1994 Aug;6(8):1099–1106. doi: 10.1105/tpc.6.8.1099. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sukegawa J., Blobel G. A nuclear pore complex protein that contains zinc finger motifs, binds DNA, and faces the nucleoplasm. Cell. 1993 Jan 15;72(1):29–38. doi: 10.1016/0092-8674(93)90047-t. [DOI] [PubMed] [Google Scholar]
- Verheijen R., van Venrooij W., Ramaekers F. The nuclear matrix: structure and composition. J Cell Sci. 1988 May;90(Pt 1):11–36. doi: 10.1242/jcs.90.1.11. [DOI] [PubMed] [Google Scholar]
- Wei X., Samarabandu J., Devdhar R. S., Siegel A. J., Acharya R., Berezney R. Segregation of transcription and replication sites into higher order domains. Science. 1998 Sep 4;281(5382):1502–1506. doi: 10.1126/science.281.5382.1502. [DOI] [PubMed] [Google Scholar]
- Whitmarsh A. J., Cavanagh J., Tournier C., Yasuda J., Davis R. J. A mammalian scaffold complex that selectively mediates MAP kinase activation. Science. 1998 Sep 11;281(5383):1671–1674. doi: 10.1126/science.281.5383.1671. [DOI] [PubMed] [Google Scholar]
- Yang C. H., Snyder M. The nuclear-mitotic apparatus protein is important in the establishment and maintenance of the bipolar mitotic spindle apparatus. Mol Biol Cell. 1992 Nov;3(11):1259–1267. doi: 10.1091/mbc.3.11.1259. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yang M., Ellenberg J., Bonifacino J. S., Weissman A. M. The transmembrane domain of a carboxyl-terminal anchored protein determines localization to the endoplasmic reticulum. J Biol Chem. 1997 Jan 17;272(3):1970–1975. doi: 10.1074/jbc.272.3.1970. [DOI] [PubMed] [Google Scholar]
- Zhao K., Harel A., Stuurman N., Guedalia D., Gruenbaum Y. Binding of matrix attachment regions to nuclear lamin is mediated by the rod domain and depends on the lamin polymerization state. FEBS Lett. 1996 Feb 12;380(1-2):161–164. doi: 10.1016/0014-5793(96)00034-8. [DOI] [PubMed] [Google Scholar]
- von Arnim A. G., Deng X. W., Stacey M. G. Cloning vectors for the expression of green fluorescent protein fusion proteins in transgenic plants. Gene. 1998 Oct 9;221(1):35–43. doi: 10.1016/s0378-1119(98)00433-8. [DOI] [PubMed] [Google Scholar]
- von Heijne G. Membrane protein structure prediction. Hydrophobicity analysis and the positive-inside rule. J Mol Biol. 1992 May 20;225(2):487–494. doi: 10.1016/0022-2836(92)90934-c. [DOI] [PubMed] [Google Scholar]
- von Kries J. P., Buhrmester H., Strätling W. H. A matrix/scaffold attachment region binding protein: identification, purification, and mode of binding. Cell. 1991 Jan 11;64(1):123–135. doi: 10.1016/0092-8674(91)90214-j. [DOI] [PubMed] [Google Scholar]