DOI: 10.1083/jcb.144.6.1097. A Conserved Biogenesis Pathway for Nucleoporins: Proteolytic Processing of a 186-Kilodalton Precursor Generates Nup98 and the Novel Nucleoporin, Nup96

A Conserved Biogenesis Pathway for Nucleoporins: Proteolytic Processing of a 186-Kilodalton Precursor Generates Nup98 and the Novel Nucleoporin, Nup96

10.1083/jcb.144.6.1097

Crossref journal-article

Rockefeller University Press

The Journal of Cell Biology (291)

Abstract

The mammalian nuclear pore complex (NPC) is comprised of ∼50 unique proteins, collectively known as nucleoporins. Through fractionation of rat liver nuclei, we have isolated &gt;30 potentially novel nucleoporins and have begun a systematic characterization of these proteins. Here, we present the characterization of Nup96, a novel nucleoporin with a predicted molecular mass of 96 kD. Nup96 is generated through an unusual biogenesis pathway that involves synthesis of a 186-kD precursor protein. Proteolytic cleavage of the precursor yields two nucleoporins: Nup98, a previously characterized GLFG-repeat containing nucleoporin, and Nup96. Mutational and functional analyses demonstrate that both the Nup98-Nup96 precursor and the previously characterized Nup98 (synthesized independently from an alternatively spliced mRNA) are proteolytically cleaved in vivo. This biogenesis pathway for Nup98 and Nup96 is evolutionarily conserved, as the putative Saccharomyces cerevisiae homologues, N-Nup145p and C-Nup145p, are also produced through proteolytic cleavage of a precursor protein. Using immunoelectron microscopy, Nup96 was localized to the nucleoplasmic side of the NPC, at or near the nucleoplasmic basket. The correct targeting of both Nup96 and Nup98 to the nucleoplasmic side of the NPC was found to be dependent on proteolytic cleavage, suggesting that the cleavage process may regulate NPC assembly. Finally, by biochemical fractionation, a complex containing Nup96, Nup107, and at least two Sec13- related proteins was identified, revealing that a major sub-complex of the NPC is conserved between yeast and mammals.

Bibliography

Fontoura, B. M. A., Blobel, G., & Matunis, M. J. (1999). A Conserved Biogenesis Pathway for Nucleoporins: Proteolytic Processing of a 186-Kilodalton Precursor Generates Nup98 and the Novel Nucleoporin, Nup96. The Journal of Cell Biology, 144(6), 1097â1112.

Authors 3

Beatriz M.A. Fontoura (first)
Günter Blobel (additional)
Michael J. Matunis (additional)

References 66 Referenced 232

10.1083/jcb.122.1.1 / J Cell Biol / Architecture of the Xenopusnuclear pore complex revealed by three-dimensional cryo-electron microscopy by Akey (1993)
10.1093/emboj/17.4.1107 / EMBO (Eur Mol Biol Organ) J / Nup116p and Nup100p are interchangeable through a conserved motif which constitutes a docking site for the mRNA transport factor Gle2p by Bailer (1998)
{'key': '2023072900404284700_B3'}
10.1083/jcb.137.5.989 / J Cell Biol / Nup84, a novel nucleoporin that is associated with CAN/Nup214 on the cytoplasmic face of the nuclear pore complex by Bastos (1997)
10.1091/mbc.9.12.3475 / Mol Biol Cell / Functional characterization of a Nup159p-containing nuclear pore subcomplex by Belgareh (1998)
10.1126/science.154.3757.1662 / Science / Nuclei from rat liver: isolation method that combines purity with high yield by Blobel (1966)
10.1038/ng0296-159 / Nat Genet / The t(7;11)(p15; p15) translocation in acute myeloid leukaemia fuses the genes for nucleoporin Nup98 and class I homeoprotein HOXA9 by Borrow (1996)
{'key': '2023072900404284700_B8', 'first-page': '193', 'article-title': 'Nuclear localization signals (NLS)', 'volume': '3', 'author': 'Boulikas', 'year': '1993', 'journal-title': 'Critical Rev Eukar Gene Expr'} / Critical Rev Eukar Gene Expr / Nuclear localization signals (NLS) by Boulikas (1993)
10.1016/S0092-8674(00)80213-5 / Cell / The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor by Brown (1997)
10.1083/jcb.136.3.515 / J Cell Biol / Identification of protein p270/Tpr as a constitutive component of the nuclear pore complex-attached intranuclear filaments by Cordes (1997)
10.1016/0092-8674(86)90784-1 / Cell / Identification and characterization of a nuclear pore complex protein by Davis (1986)
10.1128/MCB.17.2.906 / Mol Cell Biol / C-terminal truncations of the yeast nucleoporin Nup145pp produce a rapid temperature-conditional mRNA export defect and alterations to nuclear structure by Dockendorff (1997)
{'key': '2023072900404284700_B13', 'first-page': '415', 'article-title': 'Physical change in cytoplasmic messenger ribonucleoproteins in cells treated with inhibitors of mRNA transcription', 'volume': '4', 'author': 'Dreyfuss', 'year': '1984', 'journal-title': 'Mol Cell Biol'} / Mol Cell Biol / Physical change in cytoplasmic messenger ribonucleoproteins in cells treated with inhibitors of mRNA transcription by Dreyfuss (1984)
10.1083/jcb.106.3.575 / J Cell Biol / Translocation of RNA-coated gold particles through the nuclear pores of oocytes by Dworetzky (1988)
10.1083/jcb.70.3.581 / J Cell Biol / A modified procedure for the isolation of a pore complex-lamina fraction from rat liver nuclei by Dwyer (1976)
10.1242/jcs.110.7.911 / J Cell Sci / Defining the essential functional regions of the nucleoporin Nup145pp by Emtage (1997)
{'key': '2023072900404284700_B17', 'first-page': '3610', 'article-title': 'Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product', 'volume': '5', 'author': 'Evan', 'year': '1985', 'journal-title': 'Mol Cell Biol'} / Mol Cell Biol / Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product by Evan (1985)
10.1016/0092-8674(94)90297-6 / Cell / Nup145pp is required for nuclear export of mRNA and binds homopolymeric RNA in vitrovia a novel conserved motif by Fabre (1994)
10.1242/jcs.110.24.3065 / J Cell Sci / The location of the transport gate in the nuclear pore complex by Feldherr (1997)
10.1006/abio.1994.1148 / Anal Biochem / An improved procedure for enzymatic digestion of polyvinylidene difluoride-bound proteins for internal sequence analysis by Fernandez (1994)
{'key': '2023072900404284700_B21'}
10.1006/jmbi.1996.0206 / J Mol Biol / The nuclear pore complex and lamina: three-dimensional structures and interactions determined by field emission in-lens scanning electron microscopy by Goldberg (1996)
10.1091/mbc.6.11.1591 / Mol Biol Cell / Structural analysis of the p62 complex, an assembly of O-linked glycoproteins that localizes near the central gated channel of the nuclear pore complex by Guan (1995)
{'key': '2023072900404284700_B24'}
10.1016/0092-8674(92)90635-P / Cell / Architecture and design of the nuclear pore complex by Hinshaw (1992)
10.1083/jcb.134.3.589 / J Cell Biol / Molecular and functional characterization of the p62 complex, an assembly of nuclear pore proteins by Hu (1996)
10.1016/S0962-8924(97)01132-X / Trends Cell Biol / SUMO-1: ubiquitin gains weight by Johnson (1997)
10.1016/0092-8674(84)90457-4 / Cell / A short amino acid sequence able to specify nuclear location by Kalderon (1984)
10.1006/jmbi.1996.0401 / J Mol Biol / RNP export is mediated by structural reorganization of the nuclear pore basket by Kiseleva (1996)
10.1242/jcs.111.2.223 / J Cell Sci / Active nuclear pore complexes in chironomus: visualization of transporter configurations related to mRNP export by Kiseleva (1998)
10.1073/pnas.91.4.1519 / Proc Natl Acad Sci USA / The human CAN protein, a putative oncogene product associated with myeloid leukemogenesis, is a nuclear pore complex protein that faces the cytoplasm by Kraemer (1994)
{'key': '2023072900404284700_B32', 'first-page': '25', 'article-title': 'Intracellular transport of retroviral capsid components', 'volume': '214', 'author': 'Krausslich', 'year': '1996', 'journal-title': 'Curr Top Microbiol Immunol'} / Curr Top Microbiol Immunol / Intracellular transport of retroviral capsid components by Krausslich (1996)
10.1074/jbc.270.1.254 / J Biol Chem / Differential mitotic phosphorylation of proteins of the nuclear pore complex by Macaulay (1995)
10.1083/jcb.135.6.1457 / J Cell Biol / A novel ubiquitin-like modification modulates the partitioning of the Ran-GTPase-activating protein RanGAP1 between the cytosol and the nuclear pore complex by Matunis (1996)
10.1083/jcb.140.3.499 / J Cell Biol / SUMO-1 modification and its role in targeting the Ran GTPase-activating protein, RanGAP1, to the nuclear pore complex by Matunis (1998)
10.1146/annurev.biochem.67.1.265 / Annu Rev Biochem / Nucleocytoplasmic transport: the soluble phase by Mattaj (1998)
10.1016/S0962-8924(98)01252-5 / Trends Cell Biol / Two-way trafficking with ran by Melchior (1998)
10.1073/pnas.92.14.6532 / Proc Natl Acad Sci USA / Mammalian karyopherin α1β and α2β heterodimers: α1 or α2 subunit binds nuclear localization signal and β subunit interacts with peptide repeat-containing nucleoporins by Moroianu (1995)
10.1038/ng0296-154 / Nat Genet / Fusion of the nucleoporin gene Nup98 to HOXA9 by the chromosome translocation t(7;11)(p15;p15) in human myeloid leukaemia by Nakamura (1996)
10.1146/annurev.neuro.20.1.269 / Annu Rev Neurosci / RNA transport by Nakielny (1997)
10.1038/347444a0 / Nature / Identification of a receptor for protein import into mitochondria by Pain (1990)
10.1038/254109a0 / Nature / Nuclear envelope permeability by Paine (1975)
10.1016/S0955-0674(98)80016-1 / Curr Opin Cell Biol / Transport routes through the nuclear pore complex by Pemberton (1998)
10.1083/jcb.128.5.721 / J Cell Biol / Reconstituted nuclei depleted of a vertebrate GLFG containing nuclear pore protein, p97, import but are defective in nuclear growth and replication by Powers (1995)
10.1083/jcb.136.2.241 / J Cell Biol / The vertebrate nucleoporin, Nup98, is an essential component of RNA export pathways by Powers (1997)
10.1016/S0021-9258(17)32483-3 / J Biol Chem / Nup107 is a novel nuclear pore complex protein that contains a leucine zipper by Radu (1994)
10.1016/0092-8674(95)90331-3 / Cell / The peptide repeat domain of nucleoporin Nup98 functions as a docking site in transport across the nuclear pore complex by Radu (1995)
10.1083/jcb.110.4.883 / J Cell Biol / Correlation between structure and mass distribution of the nuclear pore complex and of distinct pore complex components by Reichelt (1990)
10.1016/0955-0674(92)90136-Z / Curr Biol / Novel proteases with unusual specificities by Resnick (1992)
10.1016/0092-8674(95)90181-7 / Cell / Protein import into nuclei: association and dissociation reactions involving transport substrate, transport factors, and nucleoporins by Rexach (1995)
{'key': '2023072900404284700_B51', 'first-page': '54', 'article-title': 'The 3D-structure of the nuclear pore complex as seen by high voltage electron microscopy and high resolution low voltage scanning electron microscopy', 'volume': '21', 'author': 'Ris', 'year': '1991', 'journal-title': 'EMSA Bull'} / EMSA Bull / The 3D-structure of the nuclear pore complex as seen by high voltage electron microscopy and high resolution low voltage scanning electron microscopy by Ris (1991)
10.1016/0092-8674(91)90245-T / Cell / Two interdependent basic domains in nucleoplasmin nuclear targeting sequence: identification of a class of bipartite nuclear targeting sequence by Robbins (1991)
10.1016/0962-8924(94)90085-X / Trends Cell Biol / Pores for thought: nuclear pore complex proteins by Rout (1994)
10.1002/bies.950180206 / Bioessays / The small GTPase Ran: how much does it run? by Rush (1996)
10.1038/30756 / Nature / Notch-1 signaling requires ligand-induced proteolytic release of intracellular domain by Schroeter (1998)
10.1016/S0958-1669(97)80036-5 / Curr Opin Biotech / Eukaryotic protein processing: endoproteolysis of precursor proteins by Seidah (1997)
10.1083/jcb.128.5.769 / J Cell Biol / Human SEC13Rp functions in yeast and is located on transport vesicles budding from the endoplasmic reticulum by Shaywitz (1995)
10.1016/S0092-8674(00)80981-2 / Cell / A novel complex of nucleoporins, which includes Sec13p and a Sec13p homolog, is essential for normal nuclear pores by Siniossoglou (1996)
10.1016/0092-8674(93)90047-T / Cell / A nuclear pore complex protein that contains zinc finger motifs, binds DNA and faces the nucleoplasm by Sukegawa (1993)
10.1128/MCB.17.1.256 / Mol Cell Biol / The mammalian homolog of yeast Sec13p is enriched in the intermediate compartment and is essential for protein transport from the endoplasmic reticulum to the Golgi apparatus by Tang (1997)
10.1093/emboj/16.16.5086 / EMBO (Eur Mol Biol Organ) J / Two functionally distinct domains generated by in vivo cleavage of Nup145pp: a novel biogenesis pathway for nucleoporins by Teixeira (1997)
10.1016/S0092-8674(00)80361-X / Cell / Nuclear export receptors: from importin to exportin by Ullman (1997)
10.1074/jbc.270.23.14209 / J Biol Chem / Nup358, a cytoplasmically exposed nucleoporin with peptide repeats, ran-gtp binding sites, zinc fingers, a cyclophilin a homologous domain, and a leucine-rich region by Wu (1995)
10.1016/0161-5890(95)00035-D / Mol Immunol / Differential expression of novel genes by bone marrow-derived macrophage populations by Yang (1995)
10.1016/S1097-2765(00)80023-4 / Mol Cell / Three-dimensional architecture of the isolated yeast nuclear pore complex: functional and evolutionary implications by Yang (1998)
10.1038/376184a0 / Nature / A giant nucleopore protein that binds ran/tc4 by Yokoyama (1995)

Dates

Type	When
Created	23 years, 1 month ago (July 26, 2002, 12:45 p.m.)
Deposited	2 years, 1 month ago (July 28, 2023, 8:41 p.m.)
Indexed	1 week, 6 days ago (Aug. 22, 2025, 12:45 a.m.)
Issued	26 years, 5 months ago (March 22, 1999)
Published	26 years, 5 months ago (March 22, 1999)
Published Online	26 years, 5 months ago (March 22, 1999)
Published Print	26 years, 5 months ago (March 22, 1999)

Funders 0

None

BibTeX

@article{Fontoura_1999, title={A Conserved Biogenesis Pathway for Nucleoporins: Proteolytic Processing of a 186-Kilodalton Precursor Generates Nup98 and the Novel Nucleoporin, Nup96}, volume={144}, ISSN={1540-8140}, url={http://dx.doi.org/10.1083/jcb.144.6.1097}, DOI={10.1083/jcb.144.6.1097}, number={6}, journal={The Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Fontoura, Beatriz M.A. and Blobel, Günter and Matunis, Michael J.}, year={1999}, month=mar, pages={1097–1112} }

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      "article-title": "Nup116p and Nup100p are interchangeable through a conserved motif which constitutes a docking site for the mRNA transport factor Gle2p",
      "volume": "17",
      "author": "Bailer",
      "year": "1998",
      "journal-title": "EMBO (Eur Mol Biol Organ) J"
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    {
      "key": "2023072900404284700_B4",
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      "DOI": "10.1083/jcb.137.5.989",
      "article-title": "Nup84, a novel nucleoporin that is associated with CAN/Nup214 on the cytoplasmic face of the nuclear pore complex",
      "volume": "137",
      "author": "Bastos",
      "year": "1997",
      "journal-title": "J Cell Biol"
    },
    {
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      "first-page": "3475",
      "DOI": "10.1091/mbc.9.12.3475",
      "article-title": "Functional characterization of a Nup159p-containing nuclear pore subcomplex",
      "volume": "9",
      "author": "Belgareh",
      "year": "1998",
      "journal-title": "Mol Biol Cell"
    },
    {
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      "first-page": "1662",
      "DOI": "10.1126/science.154.3757.1662",
      "article-title": "Nuclei from rat liver: isolation method that combines purity with high yield",
      "volume": "154",
      "author": "Blobel",
      "year": "1966",
      "journal-title": "Science"
    },
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      "first-page": "159",
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      "article-title": "The t(7;11)(p15; p15) translocation in acute myeloid leukaemia fuses the genes for nucleoporin Nup98 and class I homeoprotein HOXA9",
      "volume": "12",
      "author": "Borrow",
      "year": "1996",
      "journal-title": "Nat Genet"
    },
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      "first-page": "193",
      "article-title": "Nuclear localization signals (NLS)",
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      "volume": "218",
      "author": "Fernandez",
      "year": "1994",
      "journal-title": "Anal Biochem"
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      "author": "Kiseleva",
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      "author": "Kraemer",
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      "author": "Macaulay",
      "year": "1995",
      "journal-title": "J Biol Chem"
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      "volume": "135",
      "author": "Matunis",
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      "author": "Matunis",
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      "volume": "67",
      "author": "Mattaj",
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      "first-page": "175",
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      "author": "Melchior",
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      "author": "Moroianu",
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      "volume": "12",
      "author": "Nakamura",
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      "author": "Nakielny",
      "year": "1997",
      "journal-title": "Annu Rev Neurosci"
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      "first-page": "444",
      "DOI": "10.1038/347444a0",
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      "author": "Pain",
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      "author": "Pemberton",
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      "volume": "128",
      "author": "Powers",
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      "author": "Radu",
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      "author": "Reichelt",
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      "volume": "4",
      "author": "Rout",
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      "author": "Seidah",
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      "author": "Shaywitz",
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      "author": "Tang",
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