Nuclear pore complexes form immobile networks and have a very low turnover in live mammalian cells

doi:10.1083/jcb.200101089

Published 9 July 2001. doi:10.1083/jcb.200101089

This Article

	Full Text
	PDF (Full Text)
	Supplemental Material Index
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JCB
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Daigle, N.
	Articles by Ellenberg, J.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Daigle, N.
	Articles by Ellenberg, J.


Related Collections

	Related Article

Social Bookmarking

	What's this?

© The Rockefeller University Press, 0021-9525/2001/7/71 $5.00
The Journal of Cell Biology, Volume 154, Number 1, July 9, 2001 71-84

Article

Nuclear pore complexes form immobile networks and have a very low turnover in live mammalian cells

Nathalie Daigle¹, Joël Beaudouin¹, Lisa Hartnell², Gabriela Imreh³, Einar Hallberg³, Jennifer Lippincott-Schwartz² and Jan Ellenberg¹

¹ European Molecular Biology Laboratory, D-69117 Heidelberg, Germany
² Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD 20892
³ Södertörns Högskola University, 141 04 Huddinge, Sweden

Address correspondence to Jan Ellenberg, Gene Expression and Cell Biology/Biophysics Programs, European Molecular Biology Laboratory, Meyerhofstrasse 1, D-69117 Heidelberg, Germany. Tel.: (49) 6221-387-328. Fax: (49) 6221-387-518. E-mail: jan.ellenberg{at}embl-heidelberg.de

The nuclear pore complex (NPC) and its relationship to the nuclearenvelope (NE) was characterized in living cells using POM121–greenfluorescent protein (GFP) and GFP-Nup153, and GFP–laminB1. No independent movement of single pore complexes was foundwithin the plane of the NE in interphase. Only large arraysof NPCs moved slowly and synchronously during global changesin nuclear shape, strongly suggesting mechanical connectionswhich form an NPC network. The nuclear lamina exhibited identicalmovements. NPC turnover measured by fluorescence recovery afterphotobleaching of POM121 was less than once per cell cycle.Nup153 association with NPCs was dynamic and turnover of thisnucleoporin was three orders of magnitude faster. Overexpressionof both nucleoporins induced the formation of annulate lamellae(AL) in the endoplasmic reticulum (ER). Turnover of AL porecomplexes was much higher than in the NE (once every 2.5 min).During mitosis, POM121 and Nup153 were completely dispersedand mobile in the ER (POM121) or cytosol (Nup153) in metaphase,and rapidly redistributed to an immobilized pool around chromatinin late anaphase. Assembly and immobilization of both nucleoporinsoccurred before detectable recruitment of lamin B1, which isthus unlikely to mediate initiation of NPC assembly at the endof mitosis.

Key Words: nuclear pore complex; nuclear envelope; confocal microscopy; FRAP; live cell imaging

Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Add to Reddit Reddit Add to Technorati Technorati What's this?

Related Article

Long live the pore: Alan W. Dove
J. Cell Biol. 2001 154: 10. [Full Text] [PDF]

This article has been cited by other articles:

Hawryluk-Gara, L. A., Platani, M., Santarella, R., Wozniak, R. W., Mattaj, I. W. (2008). Nup53 Is Required for Nuclear Envelope and Nuclear Pore Complex Assembly. Mol. Biol. Cell 19: 1753-1762 [Abstract] [Full Text]
Dultz, E., Zanin, E., Wurzenberger, C., Braun, M., Rabut, G., Sironi, L., Ellenberg, J. (2008). Systematic kinetic analysis of mitotic dis- and reassembly of the nuclear pore in living cells. J. Cell Biol. 180: 857-865 [Abstract] [Full Text]
Rothbauer, U., Zolghadr, K., Muyldermans, S., Schepers, A., Cardoso, M. C., Leonhardt, H. (2008). A Versatile Nanotrap for Biochemical and Functional Studies with Fluorescent Fusion Proteins. Mol. Cell. Proteomics 7: 282-289 [Abstract] [Full Text]
Anderson, D. J., Hetzer, M. W. (2008). Shaping the endoplasmic reticulum into the nuclear envelope. J. Cell Sci. 121: 137-142 [Abstract] [Full Text]
Liu, Q., Pante, N., Misteli, T., Elsagga, M., Crisp, M., Hodzic, D., Burke, B., Roux, K. J. (2007). Functional association of Sun1 with nuclear pore complexes. J. Cell Biol. 178: 785-798 [Abstract] [Full Text]
Fries, T., Betz, C., Sohn, K., Caesar, S., Schlenstedt, G., Bailer, S. M. (2007). A Novel Conserved Nuclear Localization Signal Is Recognized by a Group of Yeast Importins. J. Biol. Chem. 282: 19292-19301 [Abstract] [Full Text]
Ji, J. Y., Lee, R. T., Vergnes, L., Fong, L. G., Stewart, C. L., Reue, K., Young, S. G., Zhang, Q., Shanahan, C. M., Lammerding, J. (2007). Cell Nuclei Spin in the Absence of Lamin B1. J. Biol. Chem. 282: 20015-20026 [Abstract] [Full Text]
Grimaldi, M. R., Cozzolino, L., Malva, C., Graziani, F., Gigliotti, S. (2007). nup154 Genetically Interacts With cup and Plays a Cell-Type-Specific Function During Drosophila melanogaster Egg-Chamber Development. Genetics 175: 1751-1759 [Abstract] [Full Text]
Ball, J. R., Dimaano, C., Bilak, A., Kurchan, E., Zundel, M. T., Ullman, K. S. (2007). Sequence Preference in RNA Recognition by the Nucleoporin Nup153. J. Biol. Chem. 282: 8734-8740 [Abstract] [Full Text]
Ryan, K. J., Zhou, Y., Wente, S. R. (2007). The Karyopherin Kap95 Regulates Nuclear Pore Complex Assembly into Intact Nuclear Envelopes In Vivo. Mol. Biol. Cell 18: 886-898 [Abstract] [Full Text]
Maeshima, K., Yahata, K., Sasaki, Y., Nakatomi, R., Tachibana, T., Hashikawa, T., Imamoto, F., Imamoto, N. (2006). Cell-cycle-dependent dynamics of nuclear pores: pore-free islands and lamins. J. Cell Sci. 119: 4442-4451 [Abstract] [Full Text]
Lill, Y., Lill, M. A., Fahrenkrog, B., Schwarz-Herion, K., Paulillo, S., Aebi, U., Hecht, B. (2006). Single Hepatitis-B Virus Core Capsid Binding to Individual Nuclear Pore Complexes in HeLa Cells. Biophys. J 91: 3123-3130 [Abstract] [Full Text]
Yang, W., Musser, S. M. (2006). Nuclear import time and transport efficiency depend on importin {beta} concentration. J. Cell Biol. 174: 951-961 [Abstract] [Full Text]
Dahl, K. N., Scaffidi, P., Islam, M. F., Yodh, A. G., Wilson, K. L., Misteli, T. (2006). Distinct structural and mechanical properties of the nuclear lamina in Hutchinson-Gilford progeria syndrome. Proc. Natl. Acad. Sci. USA 103: 10271-10276 [Abstract] [Full Text]
Broers, J. L. V., Ramaekers, F. C. S., Bonne, G., Yaou, R. B., Hutchison, C. J. (2006). Nuclear lamins: laminopathies and their role in premature ageing.. Physiol. Rev. 86: 967-1008 [Abstract] [Full Text]
Stavru, F., Nautrup-Pedersen, G., Cordes, V. C., Gorlich, D. (2006). Nuclear pore complex assembly and maintenance in POM121- and gp210-deficient cells. J. Cell Biol. 173: 477-483 [Abstract] [Full Text]
D'Angelo, M. A., Anderson, D. J., Richard, E., Hetzer, M. W. (2006). Nuclear pores form de novo from both sides of the nuclear envelope.. Science 312: 440-443 [Abstract] [Full Text]
Delbarre, E., Tramier, M., Coppey-Moisan, M., Gaillard, C., Courvalin, J.-C., Buendia, B. (2006). The truncated prelamin A in Hutchinson-Gilford progeria syndrome alters segregation of A-type and B-type lamin homopolymers. Hum Mol Genet 15: 1113-1122 [Abstract] [Full Text]
Soop, T., Ivarsson, B., Bjorkroth, B., Fomproix, N., Masich, S., Cordes, V. C., Daneholt, B. (2005). Nup153 Affects Entry of Messenger and Ribosomal Ribonucleoproteins into the Nuclear Basket during Export. Mol. Biol. Cell 16: 5610-5620 [Abstract] [Full Text]
Onischenko, E. A., Gubanova, N. V., Kiseleva, E. V., Hallberg, E. (2005). Cdk1 and Okadaic Acid-sensitive Phosphatases Control Assembly of Nuclear Pore Complexes in Drosophila Embryos. Mol. Biol. Cell 16: 5152-5162 [Abstract] [Full Text]
Kano, F., Kondo, H., Yamamoto, A., Tanaka, A. R., Hosokawa, N., Nagata, K., Murata, M. (2005). The maintenance of the endoplasmic reticulum network is regulated by p47, a cofactor of p97, through phosphorylation by cdc2 kinase. GENES CELLS 10: 333-344 [Abstract] [Full Text]
Varadarajan, P., Mahalingam, S., Liu, P., Ng, S. B. H., Gandotra, S., Dorairajoo, D. S. K., Balasundaram, D. (2005). The Functionally Conserved Nucleoporins Nup124p from Fission Yeast and the Human Nup153 Mediate Nuclear Import and Activity of the Tf1 Retrotransposon and HIV-1 Vpr. Mol. Biol. Cell 16: 1823-1838 [Abstract] [Full Text]
Goodchild, R. E., Dauer, W. T. (2005). The AAA+ protein torsinA interacts with a conserved domain present in LAP1 and a novel ER protein. J. Cell Biol. 168: 855-862 [Abstract] [Full Text]
Ferreri-Jacobia, M., Mak, D.-O. D., Foskett, J. K. (2005). Translational Mobility of the Type 3 Inositol 1,4,5-Trisphosphate Receptor Ca2+ Release Channel in Endoplasmic Reticulum Membrane. J. Biol. Chem. 280: 3824-3831 [Abstract] [Full Text]
Lehotzky, A., Tirian, L., Tokesi, N., Lenart, P., Szabo, B., Kovacs, J., Ovadi, J. (2004). Dynamic targeting of microtubules by TPPP/p25 affects cell survival. J. Cell Sci. 117: 6249-6259 [Abstract] [Full Text]
Dechat, T., Gajewski, A., Korbei, B., Gerlich, D., Daigle, N., Haraguchi, T., Furukawa, K., Ellenberg, J., Foisner, R. (2004). LAP2{alpha} and BAF transiently localize to telomeres and specific regions on chromatin during nuclear assembly. J. Cell Sci. 117: 6117-6128 [Abstract] [Full Text]
Maroto, B., Valle, N., Saffrich, R., Almendral, J. M. (2004). Nuclear Export of the Nonenveloped Parvovirus Virion Is Directed by an Unordered Protein Signal Exposed on the Capsid Surface. J. Virol. 78: 10685-10694 [Abstract] [Full Text]
Krull, S., Thyberg, J., Bjorkroth, B., Rackwitz, H.-R., Cordes, V. C. (2004). Nucleoporins as Components of the Nuclear Pore Complex Core Structure and Tpr as the Architectural Element of the Nuclear Basket. Mol. Biol. Cell 15: 4261-4277 [Abstract] [Full Text]
Yang, W., Gelles, J., Musser, S. M. (2004). Imaging of single-molecule translocation through nuclear pore complexes. Proc. Natl. Acad. Sci. USA 101: 12887-12892 [Abstract] [Full Text]
Giannone, G., Ronde, P., Gaire, M., Beaudouin, J., Haiech, J., Ellenberg, J., Takeda, K. (2004). Calcium Rises Locally Trigger Focal Adhesion Disassembly and Enhance Residency of Focal Adhesion Kinase at Focal Adhesions. J. Biol. Chem. 279: 28715-28723 [Abstract] [Full Text]
Loiodice, I., Alves, A., Rabut, G., van Overbeek, M., Ellenberg, J., Sibarita, J.-B., Doye, V. (2004). The Entire Nup107-160 Complex, Including Three New Members, Is Targeted as One Entity to Kinetochores in Mitosis. Mol. Biol. Cell 15: 3333-3344 [Abstract] [Full Text]
Hoyt, C. C., Bouchard, R. J., Tyler, K. L. (2004). Novel Nuclear Herniations Induced by Nuclear Localization of a Viral Protein. J. Virol. 78: 6360-6369 [Abstract] [Full Text]
Kiseleva, E., Drummond, S. P., Goldberg, M. W., Rutherford, S. A., Allen, T. D., Wilson, K. L. (2004). Actin- and protein-4.1-containing filaments link nuclear pore complexes to subnuclear organelles in Xenopus oocyte nuclei. J. Cell Sci. 117: 2481-2490 [Abstract] [Full Text]
Mearini, G., Nielsen, P. E., Fackelmayer, F. O. (2004). Localization and dynamics of small circular DNA in live mammalian nuclei. Nucleic Acids Res 32: 2642-2651 [Abstract] [Full Text]
Dimaano, C., Ullman, K. S. (2004). Nucleocytoplasmic Transport: Integrating mRNA Production and Turnover with Export through the Nuclear Pore. Mol. Cell. Biol. 24: 3069-3076 [Full Text]
Griffis, E. R., Craige, B., Dimaano, C., Ullman, K. S., Powers, M. A. (2004). Distinct Functional Domains within Nucleoporins Nup153 and Nup98 Mediate Transcription-dependent Mobility. Mol. Biol. Cell 15: 1991-2002 [Abstract] [Full Text]
Favreau, C., Higuet, D., Courvalin, J.-C., Buendia, B. (2004). Expression of a Mutant Lamin A That Causes Emery-Dreifuss Muscular Dystrophy Inhibits In Vitro Differentiation of C2C12 Myoblasts. Mol. Cell. Biol. 24: 1481-1492 [Abstract] [Full Text]
Forler, D., Rabut, G., Ciccarelli, F. D., Herold, A., Kocher, T., Niggeweg, R., Bork, P., Ellenberg, J., Izaurralde, E. (2004). RanBP2/Nup358 Provides a Major Binding Site for NXF1-p15 Dimers at the Nuclear Pore Complex and Functions in Nuclear mRNA Export. Mol. Cell. Biol. 24: 1155-1167 [Abstract] [Full Text]
Harel, A., Chan, R. C., Lachish-Zalait, A., Zimmerman, E., Elbaum, M., Forbes, D. J. (2003). Importin {beta} Negatively Regulates Nuclear Membrane Fusion and Nuclear Pore Complex Assembly. Mol. Biol. Cell 14: 4387-4396 [Abstract] [Full Text]
Enninga, J., Levay, A., Fontoura, B. M. A. (2003). Sec13 Shuttles between the Nucleus and the Cytoplasm and Stably Interacts with Nup96 at the Nuclear Pore Complex. Mol. Cell. Biol. 23: 7271-7284 [Abstract] [Full Text]
Cronshaw, J. M., Matunis, M. J. (2003). The nuclear pore complex protein ALADIN is mislocalized in triple A syndrome. Proc. Natl. Acad. Sci. USA 100: 5823-5827 [Abstract] [Full Text]
Arabi, A., Rustum, C., Hallberg, E., Wright, A. P. H. (2003). Accumulation of c-Myc and proteasomes at the nucleoli of cells containing elevated c-Myc protein levels. J. Cell Sci. 116: 1707-1717 [Abstract] [Full Text]
Hase, M. E., Cordes, V. C. (2003). Direct Interaction with Nup153 Mediates Binding of Tpr to the Periphery of the Nuclear Pore Complex. Mol. Biol. Cell 14: 1923-1940 [Abstract] [Full Text]
Lenart, P., Rabut, G., Daigle, N., Hand, A. R., Terasaki, M., Ellenberg, J. (2003). Nuclear envelope breakdown in starfish oocytes proceeds by partial NPC disassembly followed by a rapidly spreading fenestration of nuclear membranes. J. Cell Biol. 160: 1055-1068 [Abstract] [Full Text]
Kendirgi, F., Barry, D. M., Griffis, E. R., Powers, M. A., Wente, S. R. (2003). An essential role for hGle1 nucleocytoplasmic shuttling in mRNA export. J. Cell Biol. 160: 1029-1040 [Abstract] [Full Text]
Griffis, E. R., Xu, S., Powers, M. A. (2003). Nup98 Localizes to Both Nuclear and Cytoplasmic Sides of the Nuclear Pore and Binds to Two Distinct Nucleoporin Subcomplexes. Mol. Biol. Cell 14: 600-610 [Abstract] [Full Text]
Shulga, N., Goldfarb, D. S. (2003). Binding Dynamics of Structural Nucleoporins Govern Nuclear Pore Complex Permeability and May Mediate Channel Gating. Mol. Cell. Biol. 23: 534-542 [Abstract] [Full Text]
Kruse, C., Jaedicke, A., Beaudouin, J., Bohl, F., Ferring, D., Guttler, T., Ellenberg, J., Jansen, R.-P. (2002). Ribonucleoprotein-dependent localization of the yeast class V myosin Myo4p. J. Cell Biol. 159: 971-982 [Abstract] [Full Text]
Lusk, C. P., Makhnevych, T., Marelli, M., Aitchison, J. D., Wozniak, R. W. (2002). Karyopherins in nuclear pore biogenesis: a role for Kap121p in the assembly of Nup53p into nuclear pore complexes. J. Cell Biol. 159: 267-278 [Abstract] [Full Text]
Drummond, S. P., Wilson, K. L. (2002). Interference with the cytoplasmic tail of gp210 disrupts "close apposition" of nuclear membranes and blocks nuclear pore dilation. J. Cell Biol. 158: 53-62 [Abstract] [Full Text]
Lombardo, E., Ramirez, J. C., Garcia, J., Almendral, J. M. (2002). Complementary Roles of Multiple Nuclear Targeting Signals in the Capsid Proteins of the Parvovirus Minute Virus of Mice during Assembly and Onset of Infection. J. Virol. 76: 7049-7059 [Abstract] [Full Text]
Windoffer, R., Borchert-Stuhltrager, M., Leube, R. E. (2002). Desmosomes: interconnected calcium-dependent structures of remarkable stability with significant integral membrane protein turnover. J. Cell Sci. 115: 1717-1732 [Abstract] [Full Text]
Kihlmark, M., Imreh, G., Hallberg, E. (2002). Sequential degradation of proteins from the nuclear envelope during apoptosis. J. Cell Sci. 114: 3643-3653 [Abstract] [Full Text]
Goldman, R. D., Gruenbaum, Y., Moir, R. D., Shumaker, D. K., Spann, T. P. (2002). Nuclear lamins: building blocks of nuclear architecture. Genes Dev. 16: 533-547 [Full Text]
Wu, W., Lin, F., Worman, H. J. (2002). Intracellular trafficking of MAN1, an integral protein of the nuclear envelope inner membrane. J. Cell Sci. 115: 1361-1371 [Abstract] [Full Text]
Vasu, S., Shah, S., Orjalo, A., Park, M., Fischer, W. H., Forbes, D. J. (2001). Novel vertebrate nucleoporins Nup133 and Nup160 play a role in mRNA export. J. Cell Biol. 155: 339-354 [Abstract] [Full Text]
Lyman, S. K., Gerace, L. (2001). Nuclear pore complexes: dynamics in unexpected places. J. Cell Biol. 154: 17-20 [Abstract] [Full Text]
Dimaano, C., Ball, J. R., Prunuske, A. J., Ullman, K. S. (2001). RNA Association Defines a Functionally Conserved Domain in the Nuclear Pore Protein Nup153. J. Biol. Chem. 276: 45349-45357 [Abstract] [Full Text]
Griffis, E. R., Altan, N., Lippincott-Schwartz, J., Powers, M. A. (2002). Nup98 Is a Mobile Nucleoporin with Transcription-dependent Dynamics. Mol. Biol. Cell 13: 1282-1297 [Abstract] [Full Text]