DOI: 10.1083/jcb.148.2.271. Electron Tomography Reveals Posttranscriptional Binding of Pre-Mrnps to Specific Fibers in the Nucleoplasm

Electron Tomography Reveals Posttranscriptional Binding of Pre-Mrnps to Specific Fibers in the Nucleoplasm

10.1083/jcb.148.2.271

Crossref journal-article

Rockefeller University Press

The Journal of Cell Biology (291)

Abstract

Using electron tomography, we have analyzed whether the Balbiani ring (BR) pre-mRNP particles in transit from the gene to the nuclear pore complex (NPC) are bound to any structure that could impair free diffusion through the nucleoplasm. We show that one-third of the BR particles are in contact with thin connecting fibers (CFs), which in some cases merge into large fibrogranular clusters. The CFs have a specific protein composition different from that of BR particles, as shown by immuno-EM. Moreover, we have identified hrp65 as one of the protein components of the CFs. The sequencing of hrp65 cDNA reveals similarities with hnRNP proteins and splicing factors. However, hrp65 is likely to have a different function because it does not bind to nascent pre-mRNA and is not part of the pre-mRNP itself. Taken together, our observations indicate that pre-mRNPs are not always freely diffusible in the nucleoplasm but interact with fibers of specific structure and composition, which implies that some of the posttranscriptional events that the pre-mRNPs undergo before reaching the NPC occur in a bound state.

Bibliography

Miralles, F., Ãfverstedt, L.-G., Sabri, N., Aissouni, Y., Hellman, U., Skoglund, U., & Visa, N. (2000). Electron Tomography Reveals Posttranscriptional Binding of Pre-Mrnps to Specific Fibers in the Nucleoplasm. The Journal of Cell Biology, 148(2), 271â282.

Authors 7

Francesc Miralles (first)
Lars-Göran Öfverstedt (additional)
Nafiseh Sabri (additional)
Youssef Aissouni (additional)
Ulf Hellman (additional)
Ulf Skoglund (additional)
Neus Visa (additional)

References 50 Referenced 49

{'key': '2023072901313361200_Agutter1995', 'first-page': '183', 'article-title': 'Intracellular structure and nucleocytoplasmic transport', 'volume': '162B', 'author': 'Agutter', 'year': '1995', 'journal-title': 'Int. Rev. Cytol.'} / Int. Rev. Cytol. / Intracellular structure and nucleocytoplasmic transport by Agutter (1995)
10.1101/gad.10.22.2881 / Genes Dev. / A protein of the SR family of splicing factors binds extensively to exonic Balbiani ring pre-mRNA and accompanies the RNA from the gene to the nuclear pore by Alzhanova-Ericsson (1996)
10.1093/nar/21.13.3093 / Nucleic Acids Res. / The SWISS-PROT protein sequence data bank, recent developments by Bairoch (1993)
10.1128/MCB.17.2.677 / Mol. Cel. Biol. / The intracisternal A–particle proximal enhancer-binding protein activates transcription and is identical to the RNA- and DNA-binding protein p54nrb/NonO by Basu (1997)
10.1016/0092-8674(94)90182-1 / Cell. / Splicing of Balbiani ring 1 gene pre-mRNA occurs simultaneously with transcription by Baurén (1994)
10.1101/gad.12.17.2759 / Genes Dev. / Transcriptional termination in the Balbiani ring 1 gene is closely coupled to 3′-end formation and excision of the 3′-terminal intron by Baurén (1998)
10.1083/jcb.135.2.303 / J. Cell Biol. / Spliced exons of adenovirus late RNAs colocalize with snRNP in a specific nuclear domain by Bridge (1996)
10.1126/science.8036511 / Science. / Conserved structures and diversity of functions of RNA-binding proteins by Burd (1994)
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)
10.1093/emboj/18.10.2855 / EMBO (Eur. Mol. Biol. Organ.) J. / Inefficient processing impairs release of RNA from the site of transcription by Custódio (1999)
10.1016/S0960-9822(99)80256-5 / Curr. Biol. / Pre-mRNP particlesfrom gene to nuclear pore by Daneholt (1999)
10.1093/nar/21.17.4085 / Nucleic Acids Res. / Purification and cDNA cloning of HeLa cell p54nrb, a nuclear protein with two RNA recognition motifs and extensive homology to human splicing factor PSF and Drosophila NONA/BJ6 by Dong (1993)
10.1101/SQB.1978.042.01.089 / Cold Spring Harbor Symp. Quant. Biol. / Fate of Balbiani-ring RNA in vivo by Edström (1978)
10.1083/jcb.102.5.1654 / J. Cell Biol. / The nonchromatin substructures of the nucleusthe ribonucleoprotein (RNP)-containing and RNP-depleted matrices analyzed by sequential fractionation and resinless section electron microscopy by Fey (1986)
10.1007/978-3-642-59219-5_8 / Protein Structure Analysis. Preparation, characterization, and microsequencing / Isolation of peptides for microsequencing by in-gel proteolytic digestion by Hellman (1997)
10.1083/jcb.137.1.27 / J. Cell Biol. / A role for the M9 transport signal of hnRNP A1 in mRNA nuclear export by Izaurralde (1997)
10.1016/0896-6273(90)90197-N / Neuron. / Molecular analysis of no-on-transient A, a gene required for normal vision in Drosophila by Jones (1990)
10.1016/0092-8674(86)90762-2 / Cell. / Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes by Kozak (1986)
10.1016/S0955-0674(99)80051-9 / Curr. Opin. Cell Biol. / HnRNP complexescomposition, structure, and function by Krecic (1999)
10.1016/0092-8674(89)90127-X / Cell. / Some cis- and trans-acting mutants for splicing target pre-mRNA to the cytoplasm by Legrain (1989)
10.1007/BF00327356 / Chromosoma. / Heat shock phenomena in Chironomus tentans. IIn vivo effects of heat, overheat, and quenching on salivary chromosome puffing by Lezzi (1981)
10.1016/0014-4827(92)90437-D / Exp. Cell. Res. / Demonstration of a 7-nm RNP fiber as the basic structural element in a premessenger RNP particle by Lönnroth (1992)
10.1146/annurev.biochem.67.1.265 / Annu. Rev. Biochem. / Nucleocytoplasmic transportthe soluble phase by Mattaj (1998)
10.1016/0092-8674(95)90119-1 / Cell. / A nuclear export signal in hnRNP A1a signal-mediated, temperature-dependent nuclear protein export pathway by Michael (1995)
10.1016/S0955-0674(98)80007-0 / Curr. Opin. Cell Biol. / The cellular organization of gene expression by Misteli (1998)
10.1083/jcb.134.6.1365 / J. Cell Biol. / The hnRNP C proteins contain a nuclear retention sequence that can override nuclear export signals by Nakielny (1996)
10.1101/gad.7.3.393 / Genes Dev. / Cloning and characterization of PSF, a novel pre-mRNA splicing factor by Patton (1993)
10.1006/jmbi.1997.1618 / J. Mol. Biol. / Thinking about a nuclear matrix by Pederson (1998)
10.1073/pnas.95.11.6043 / Proc. Natl. Acad. Sci. USA. / Intranuclear diffusion and hybridization state of oligonucleotides measured by fluorescence correlation spectroscopy in living cells by Politz (1998)
10.1006/excr.1996.0363 / Exp. Cell Res. / Ultrastructure of the nucleus in relation to transcription and splicingroles of perichromatin fibrils and interchromatin granules by Puvion (1996)
{'key': '2023072901313361200_Puvion-Dutilleuletal1997', 'first-page': '315', 'article-title': 'Identification of transcription factories in nuclei of HeLa cells transiently expressing the Us11 gene of herpes simplex virus type 1', 'volume': '6', 'author': 'Puvion-Dutilleul', 'year': '1997', 'journal-title': 'Gene Expr.'} / Gene Expr. / Identification of transcription factories in nuclei of HeLa cells transiently expressing the Us11 gene of herpes simplex virus type 1 by Puvion-Dutilleul (1997)
10.1523/JNEUROSCI.12-02-00390.1992 / J. Neurosci. / The dissonance mutation at the no-on-transient-A locus of D. melanogastergenetic control of courtship song and visual behaviors by a protein with putative RNA-binding motifs by Rendahl (1992)
10.1006/excr.1999.4490 / Exp. Cell. Res. / The intranuclear movement of Balbiani ring pre-messenger ribonucleoprotein particles by Singh (1999)
10.1016/0092-8674(83)90542-1 / Cell. / Visualization of the formation and transport of a specific hnRNP particle by Skoglund (1983)
10.1038/319560a0 / Nature. / Three-dimensional structure of a specific pre-messenger RNP particle established by electron microscope tomography by Skoglund (1986)
10.1006/jsbi.1996.0081 / J. Struct. Biol / Maximum-entropy three-dimensional reconstruction with deconvolution of the contrast transfer functiona test application with adenovirus by Skoglund (1996)
10.1007/978-3-642-80356-7_4 / RNP Particles, Splicing and Autoimmune Diseases / Procedures for three-dimensional reconstruction from thin sections with electron tomography by Skoglund (1998)
10.1083/jcb.144.5.839 / J. Cell Biol. / Proteins connecting the nuclear pore complex with the nuclear interior by Strambio-de-Castillia (1999)
10.1101/gad.12.21.3303 / Genes Dev. / Nuclear RNA export by Stutz (1998)
10.1083/jcb.142.5.1181 / J. Cell Biol. / The hrp23 protein in the balbiani ring pre-mRNP particles is released just before or at the binding of the particles to the nuclear pore complex by Sun (1998)
10.1083/jcb.133.1.5 / J. Cell Biol. / A nuclear cap-binding complex binds Balbiani ring pre-mRNA cotranscriptionally and accompanies the ribonucleoprotein particle during nuclear export by Visa (1996)
10.1016/S0092-8674(00)80980-0 / Cell. / A pre-mRNA-binding protein accompanies the RNA from the gene through the nuclear pores and into polysomes by Visa (1996)
10.1007/BF00337601 / Chromosoma. / The puff-specific Drosophila protein Bj6, encoded by the gene no-on transient A, shows homology to RNA-binding proteins by von Besser (1990)
10.1073/pnas.88.16.7391 / Proc. Natl. Acad. Sci. USA. / Localization of pre-messenger RNA at discrete nuclear sites by Wang (1991)
10.1016/S0079-6603(08)60858-2 / Prog. Nucleic Acid Res. Mol. Biol. / The Balbiani ring multigene familycoding repetitive sequences and evolution of a tissue-specific cell function by Wieslander (1994)
10.1128/MCB.16.4.1425 / Mol. Cel. Biol. / Identification of two RNA-binding proteins in Balbiani ring premessenger ribonucleoprotein granules and presence of these proteins in specific subsets of heterogeneous nuclear ribonucleoprotein particles by Wurtz (1996)
10.1016/0014-4827(82)90255-5 / Exp. Cell Res. / Chironomus tentans epithelial cell lines sensitive to ecdysteroids, juvenile hormone, insulin and heat shock by Wyss (1982)
10.1083/jcb.131.6.1635 / J. Cell Biol. / Nonrandom gene organizationstructural arrangements of specific pre-mRNA transcription and splicing with SC-35 domains by Xing (1995)
10.1083/jcb.121.4.729 / J. Cell Biol. / Evidence for channeled diffusion of pre-mRNAs during nuclear RNA transport in metazoans by Zachar (1993)
10.1242/jcs.110.8.927 / J. Cell Sci. / A Drosophila Tpr homolog is localized both in the extrachromosomal channel network and to nuclear pore complexes by Zimowska (1997)

Dates

Type	When
Created	23 years ago (July 26, 2002, 12:45 p.m.)
Deposited	2 years ago (July 28, 2023, 9:32 p.m.)
Indexed	1 year ago (Aug. 12, 2024, 9:11 a.m.)
Issued	25 years, 7 months ago (Jan. 24, 2000)
Published	25 years, 7 months ago (Jan. 24, 2000)
Published Online	25 years, 7 months ago (Jan. 24, 2000)
Published Print	25 years, 7 months ago (Jan. 24, 2000)

Funders 0

None

BibTeX

@article{Miralles_2000, title={Electron Tomography Reveals Posttranscriptional Binding of Pre-Mrnps to Specific Fibers in the Nucleoplasm}, volume={148}, ISSN={1540-8140}, url={http://dx.doi.org/10.1083/jcb.148.2.271}, DOI={10.1083/jcb.148.2.271}, number={2}, journal={The Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Miralles, Francesc and Öfverstedt, Lars-Göran and Sabri, Nafiseh and Aissouni, Youssef and Hellman, Ulf and Skoglund, Ulf and Visa, Neus}, year={2000}, month=jan, pages={271–282} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2024,
        8,
        12
      ]
    ],
    "date-time": "2024-08-12T13:11:53Z",
    "timestamp": 1723468313036
  },
  "reference-count": 50,
  "publisher": "Rockefeller University Press",
  "issue": "2",
  "content-domain": {
    "domain": [
      "rupress.org"
    ],
    "crossmark-restriction": true
  },
  "published-print": {
    "date-parts": [
      [
        2000,
        1,
        24
      ]
    ]
  },
  "abstract": "<jats:p>Using electron tomography, we have analyzed whether the Balbiani ring (BR) pre-mRNP particles in transit from the gene to the nuclear pore complex (NPC) are bound to any structure that could impair free diffusion through the nucleoplasm. We show that one-third of the BR particles are in contact with thin connecting fibers (CFs), which in some cases merge into large fibrogranular clusters. The CFs have a specific protein composition different from that of BR particles, as shown by immuno-EM. Moreover, we have identified hrp65 as one of the protein components of the CFs. The sequencing of hrp65 cDNA reveals similarities with hnRNP proteins and splicing factors. However, hrp65 is likely to have a different function because it does not bind to nascent pre-mRNA and is not part of the pre-mRNP itself. Taken together, our observations indicate that pre-mRNPs are not always freely diffusible in the nucleoplasm but interact with fibers of specific structure and composition, which implies that some of the posttranscriptional events that the pre-mRNPs undergo before reaching the NPC occur in a bound state.</jats:p>",
  "DOI": "10.1083/jcb.148.2.271",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2002,
        7,
        26
      ]
    ],
    "date-time": "2002-07-26T16:45:41Z",
    "timestamp": 1027701941000
  },
  "page": "271-282",
  "update-policy": "http://dx.doi.org/10.1083/jcb.crossmarkpolicy",
  "source": "Crossref",
  "is-referenced-by-count": 49,
  "title": "Electron Tomography Reveals Posttranscriptional Binding of Pre-Mrnps to Specific Fibers in the Nucleoplasm",
  "prefix": "10.1083",
  "volume": "148",
  "author": [
    {
      "given": "Francesc",
      "family": "Miralles",
      "sequence": "first",
      "affiliation": [
        {
          "name": "aDepartment of Molecular Genome Research, Stockholm University, SE-106 91 Stockholm, Sweden"
        }
      ]
    },
    {
      "given": "Lars-G\u00f6ran",
      "family": "\u00d6fverstedt",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "bDepartment of Cell and Molecular Biology, Karolinska Institute, SE-171 77 Stockholm, Sweden"
        }
      ]
    },
    {
      "given": "Nafiseh",
      "family": "Sabri",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "aDepartment of Molecular Genome Research, Stockholm University, SE-106 91 Stockholm, Sweden"
        }
      ]
    },
    {
      "given": "Youssef",
      "family": "Aissouni",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "cInstitut Paoli Calmettes, INSERM-U119, Canc\u00e9rologie Exp\u00e9rimentale, F-13009 Marseille, France"
        }
      ]
    },
    {
      "given": "Ulf",
      "family": "Hellman",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "dLudwig Institute for Cancer Research, SE-751 24 Uppsala, Sweden"
        }
      ]
    },
    {
      "given": "Ulf",
      "family": "Skoglund",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "bDepartment of Cell and Molecular Biology, Karolinska Institute, SE-171 77 Stockholm, Sweden"
        }
      ]
    },
    {
      "given": "Neus",
      "family": "Visa",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "aDepartment of Molecular Genome Research, Stockholm University, SE-106 91 Stockholm, Sweden"
        }
      ]
    }
  ],
  "member": "291",
  "published-online": {
    "date-parts": [
      [
        2000,
        1,
        24
      ]
    ]
  },
  "reference": [
    {
      "key": "2023072901313361200_Agutter1995",
      "first-page": "183",
      "article-title": "Intracellular structure and nucleocytoplasmic transport",
      "volume": "162B",
      "author": "Agutter",
      "year": "1995",
      "journal-title": "Int. Rev. Cytol."
    },
    {
      "key": "2023072901313361200_Alzhanova-Ericssonetal1996",
      "doi-asserted-by": "crossref",
      "first-page": "2881",
      "DOI": "10.1101/gad.10.22.2881",
      "article-title": "A protein of the SR family of splicing factors binds extensively to exonic Balbiani ring pre-mRNA and accompanies the RNA from the gene to the nuclear pore",
      "volume": "10",
      "author": "Alzhanova-Ericsson",
      "year": "1996",
      "journal-title": "Genes Dev."
    },
    {
      "key": "2023072901313361200_BairochandBoeckmann1993",
      "doi-asserted-by": "crossref",
      "first-page": "3093",
      "DOI": "10.1093/nar/21.13.3093",
      "article-title": "The SWISS-PROT protein sequence data bank, recent developments",
      "volume": "21",
      "author": "Bairoch",
      "year": "1993",
      "journal-title": "Nucleic Acids Res."
    },
    {
      "key": "2023072901313361200_Basuetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "677",
      "DOI": "10.1128/MCB.17.2.677",
      "article-title": "The intracisternal A\u2013particle proximal enhancer-binding protein activates transcription and is identical to the RNA- and DNA-binding protein p54nrb/NonO",
      "volume": "17",
      "author": "Basu",
      "year": "1997",
      "journal-title": "Mol. Cel. Biol."
    },
    {
      "key": "2023072901313361200_N0x2966390N0x3593ee0",
      "doi-asserted-by": "crossref",
      "first-page": "183",
      "DOI": "10.1016/0092-8674(94)90182-1",
      "article-title": "Splicing of Balbiani ring 1 gene pre-mRNA occurs simultaneously with transcription",
      "volume": "76",
      "author": "Baur\u00e9n",
      "year": "1994",
      "journal-title": "Cell."
    },
    {
      "key": "2023072901313361200_N0x2966390N0x3593f40",
      "doi-asserted-by": "crossref",
      "first-page": "2759",
      "DOI": "10.1101/gad.12.17.2759",
      "article-title": "Transcriptional termination in the Balbiani ring 1 gene is closely coupled to 3\u2032-end formation and excision of the 3\u2032-terminal intron",
      "volume": "12",
      "author": "Baur\u00e9n",
      "year": "1998",
      "journal-title": "Genes Dev."
    },
    {
      "key": "2023072901313361200_Bridgeetal1996",
      "doi-asserted-by": "crossref",
      "first-page": "303",
      "DOI": "10.1083/jcb.135.2.303",
      "article-title": "Spliced exons of adenovirus late RNAs colocalize with snRNP in a specific nuclear domain",
      "volume": "135",
      "author": "Bridge",
      "year": "1996",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072901313361200_BurdandDreyfuss1994",
      "doi-asserted-by": "crossref",
      "first-page": "615",
      "DOI": "10.1126/science.8036511",
      "article-title": "Conserved structures and diversity of functions of RNA-binding proteins",
      "volume": "265",
      "author": "Burd",
      "year": "1994",
      "journal-title": "Science."
    },
    {
      "key": "2023072901313361200_Cordesetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "515",
      "DOI": "10.1083/jcb.136.3.515",
      "article-title": "Identification of protein p270/Tpr as a constitutive component of the nuclear pore complex-attached intranuclear filaments",
      "volume": "136",
      "author": "Cordes",
      "year": "1997",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072901313361200_N0x2966390N0x35940c0",
      "doi-asserted-by": "crossref",
      "first-page": "2855",
      "DOI": "10.1093/emboj/18.10.2855",
      "article-title": "Inefficient processing impairs release of RNA from the site of transcription",
      "volume": "18",
      "author": "Cust\u00f3dio",
      "year": "1999",
      "journal-title": "EMBO (Eur. Mol. Biol. Organ.) J."
    },
    {
      "key": "2023072901313361200_Daneholt1999",
      "doi-asserted-by": "crossref",
      "first-page": "412",
      "DOI": "10.1016/S0960-9822(99)80256-5",
      "article-title": "Pre-mRNP particlesfrom gene to nuclear pore",
      "volume": "9",
      "author": "Daneholt",
      "year": "1999",
      "journal-title": "Curr. Biol."
    },
    {
      "key": "2023072901313361200_Dongetal1993",
      "doi-asserted-by": "crossref",
      "first-page": "4085",
      "DOI": "10.1093/nar/21.17.4085",
      "article-title": "Purification and cDNA cloning of HeLa cell p54nrb, a nuclear protein with two RNA recognition motifs and extensive homology to human splicing factor PSF and Drosophila NONA/BJ6",
      "volume": "21",
      "author": "Dong",
      "year": "1993",
      "journal-title": "Nucleic Acids Res."
    },
    {
      "key": "2023072901313361200_N0x2966390N0x35941e0",
      "doi-asserted-by": "crossref",
      "first-page": "877",
      "DOI": "10.1101/SQB.1978.042.01.089",
      "article-title": "Fate of Balbiani-ring RNA in vivo",
      "volume": "42",
      "author": "Edstr\u00f6m",
      "year": "1978",
      "journal-title": "Cold Spring Harbor Symp. Quant. Biol."
    },
    {
      "key": "2023072901313361200_Feyetal1986",
      "doi-asserted-by": "crossref",
      "first-page": "1654",
      "DOI": "10.1083/jcb.102.5.1654",
      "article-title": "The nonchromatin substructures of the nucleusthe ribonucleoprotein (RNP)-containing and RNP-depleted matrices analyzed by sequential fractionation and resinless section electron microscopy",
      "volume": "102",
      "author": "Fey",
      "year": "1986",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072901313361200_Hellman1997",
      "doi-asserted-by": "crossref",
      "first-page": "97",
      "DOI": "10.1007/978-3-642-59219-5_8",
      "article-title": "Isolation of peptides for microsequencing by in-gel proteolytic digestion",
      "volume-title": "Protein Structure Analysis. Preparation, characterization, and microsequencing",
      "author": "Hellman",
      "year": "1997"
    },
    {
      "key": "2023072901313361200_Izaurraldeetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "27",
      "DOI": "10.1083/jcb.137.1.27",
      "article-title": "A role for the M9 transport signal of hnRNP A1 in mRNA nuclear export",
      "volume": "137",
      "author": "Izaurralde",
      "year": "1997",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072901313361200_JonesandRubin1990",
      "doi-asserted-by": "crossref",
      "first-page": "711",
      "DOI": "10.1016/0896-6273(90)90197-N",
      "article-title": "Molecular analysis of no-on-transient A, a gene required for normal vision in Drosophila",
      "volume": "4",
      "author": "Jones",
      "year": "1990",
      "journal-title": "Neuron."
    },
    {
      "key": "2023072901313361200_Kozak1986",
      "doi-asserted-by": "crossref",
      "first-page": "283",
      "DOI": "10.1016/0092-8674(86)90762-2",
      "article-title": "Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes",
      "volume": "44",
      "author": "Kozak",
      "year": "1986",
      "journal-title": "Cell."
    },
    {
      "key": "2023072901313361200_KrecicandSwanson1999",
      "doi-asserted-by": "crossref",
      "first-page": "363",
      "DOI": "10.1016/S0955-0674(99)80051-9",
      "article-title": "HnRNP complexescomposition, structure, and function",
      "volume": "11",
      "author": "Krecic",
      "year": "1999",
      "journal-title": "Curr. Opin. Cell Biol."
    },
    {
      "key": "2023072901313361200_LegrainandRosbash1989",
      "doi-asserted-by": "crossref",
      "first-page": "573",
      "DOI": "10.1016/0092-8674(89)90127-X",
      "article-title": "Some cis- and trans-acting mutants for splicing target pre-mRNA to the cytoplasm",
      "volume": "57",
      "author": "Legrain",
      "year": "1989",
      "journal-title": "Cell."
    },
    {
      "key": "2023072901313361200_Lezzietal1981",
      "doi-asserted-by": "crossref",
      "first-page": "327",
      "DOI": "10.1007/BF00327356",
      "article-title": "Heat shock phenomena in Chironomus tentans. IIn vivo effects of heat, overheat, and quenching on salivary chromosome puffing",
      "volume": "83",
      "author": "Lezzi",
      "year": "1981",
      "journal-title": "Chromosoma."
    },
    {
      "key": "2023072901313361200_N0x2966390N0x3594540",
      "doi-asserted-by": "crossref",
      "first-page": "292",
      "DOI": "10.1016/0014-4827(92)90437-D",
      "article-title": "Demonstration of a 7-nm RNP fiber as the basic structural element in a premessenger RNP particle",
      "volume": "199",
      "author": "L\u00f6nnroth",
      "year": "1992",
      "journal-title": "Exp. Cell. Res."
    },
    {
      "key": "2023072901313361200_MattajandEnglmeier1998",
      "doi-asserted-by": "crossref",
      "first-page": "265",
      "DOI": "10.1146/annurev.biochem.67.1.265",
      "article-title": "Nucleocytoplasmic transportthe soluble phase",
      "volume": "67",
      "author": "Mattaj",
      "year": "1998",
      "journal-title": "Annu. Rev. Biochem."
    },
    {
      "key": "2023072901313361200_Michaeletal1995",
      "doi-asserted-by": "crossref",
      "first-page": "415",
      "DOI": "10.1016/0092-8674(95)90119-1",
      "article-title": "A nuclear export signal in hnRNP A1a signal-mediated, temperature-dependent nuclear protein export pathway",
      "volume": "83",
      "author": "Michael",
      "year": "1995",
      "journal-title": "Cell."
    },
    {
      "key": "2023072901313361200_MisteliandSpector1998",
      "doi-asserted-by": "crossref",
      "first-page": "323",
      "DOI": "10.1016/S0955-0674(98)80007-0",
      "article-title": "The cellular organization of gene expression",
      "volume": "10",
      "author": "Misteli",
      "year": "1998",
      "journal-title": "Curr. Opin. Cell Biol."
    },
    {
      "key": "2023072901313361200_NakielnyandDreyfuss1996",
      "doi-asserted-by": "crossref",
      "first-page": "1365",
      "DOI": "10.1083/jcb.134.6.1365",
      "article-title": "The hnRNP C proteins contain a nuclear retention sequence that can override nuclear export signals",
      "volume": "134",
      "author": "Nakielny",
      "year": "1996",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072901313361200_Pattonetal1993",
      "doi-asserted-by": "crossref",
      "first-page": "393",
      "DOI": "10.1101/gad.7.3.393",
      "article-title": "Cloning and characterization of PSF, a novel pre-mRNA splicing factor",
      "volume": "7",
      "author": "Patton",
      "year": "1993",
      "journal-title": "Genes Dev."
    },
    {
      "key": "2023072901313361200_Pederson1998",
      "doi-asserted-by": "crossref",
      "first-page": "147",
      "DOI": "10.1006/jmbi.1997.1618",
      "article-title": "Thinking about a nuclear matrix",
      "volume": "277",
      "author": "Pederson",
      "year": "1998",
      "journal-title": "J. Mol. Biol."
    },
    {
      "key": "2023072901313361200_Politzetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "6043",
      "DOI": "10.1073/pnas.95.11.6043",
      "article-title": "Intranuclear diffusion and hybridization state of oligonucleotides measured by fluorescence correlation spectroscopy in living cells",
      "volume": "95",
      "author": "Politz",
      "year": "1998",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072901313361200_PuvionandPuvion-Dutilleul1996",
      "doi-asserted-by": "crossref",
      "first-page": "217",
      "DOI": "10.1006/excr.1996.0363",
      "article-title": "Ultrastructure of the nucleus in relation to transcription and splicingroles of perichromatin fibrils and interchromatin granules",
      "volume": "229",
      "author": "Puvion",
      "year": "1996",
      "journal-title": "Exp. Cell Res."
    },
    {
      "key": "2023072901313361200_Puvion-Dutilleuletal1997",
      "first-page": "315",
      "article-title": "Identification of transcription factories in nuclei of HeLa cells transiently expressing the Us11 gene of herpes simplex virus type 1",
      "volume": "6",
      "author": "Puvion-Dutilleul",
      "year": "1997",
      "journal-title": "Gene Expr."
    },
    {
      "key": "2023072901313361200_Rendahletal1992",
      "doi-asserted-by": "crossref",
      "first-page": "390",
      "DOI": "10.1523/JNEUROSCI.12-02-00390.1992",
      "article-title": "The dissonance mutation at the no-on-transient-A locus of D. melanogastergenetic control of courtship song and visual behaviors by a protein with putative RNA-binding motifs",
      "volume": "12",
      "author": "Rendahl",
      "year": "1992",
      "journal-title": "J. Neurosci."
    },
    {
      "key": "2023072901313361200_Singhetal1999",
      "doi-asserted-by": "crossref",
      "first-page": "135",
      "DOI": "10.1006/excr.1999.4490",
      "article-title": "The intranuclear movement of Balbiani ring pre-messenger ribonucleoprotein particles",
      "volume": "251",
      "author": "Singh",
      "year": "1999",
      "journal-title": "Exp. Cell. Res."
    },
    {
      "key": "2023072901313361200_Skoglundetal1983",
      "doi-asserted-by": "crossref",
      "first-page": "847",
      "DOI": "10.1016/0092-8674(83)90542-1",
      "article-title": "Visualization of the formation and transport of a specific hnRNP particle",
      "volume": "34",
      "author": "Skoglund",
      "year": "1983",
      "journal-title": "Cell."
    },
    {
      "key": "2023072901313361200_Skoglundetal1986",
      "doi-asserted-by": "crossref",
      "first-page": "560",
      "DOI": "10.1038/319560a0",
      "article-title": "Three-dimensional structure of a specific pre-messenger RNP particle established by electron microscope tomography",
      "volume": "319",
      "author": "Skoglund",
      "year": "1986",
      "journal-title": "Nature."
    },
    {
      "key": "2023072901313361200_Skoglundetal1996",
      "doi-asserted-by": "crossref",
      "first-page": "173",
      "DOI": "10.1006/jsbi.1996.0081",
      "article-title": "Maximum-entropy three-dimensional reconstruction with deconvolution of the contrast transfer functiona test application with adenovirus",
      "volume": "117",
      "author": "Skoglund",
      "year": "1996",
      "journal-title": "J. Struct. Biol"
    },
    {
      "key": "2023072901313361200_Skoglundetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "72",
      "DOI": "10.1007/978-3-642-80356-7_4",
      "article-title": "Procedures for three-dimensional reconstruction from thin sections with electron tomography",
      "volume-title": "RNP Particles, Splicing and Autoimmune Diseases",
      "author": "Skoglund",
      "year": "1998"
    },
    {
      "key": "2023072901313361200_Strambio-de-Castilliaetal1999",
      "doi-asserted-by": "crossref",
      "first-page": "839",
      "DOI": "10.1083/jcb.144.5.839",
      "article-title": "Proteins connecting the nuclear pore complex with the nuclear interior",
      "volume": "144",
      "author": "Strambio-de-Castillia",
      "year": "1999",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072901313361200_StutzandRosbash1998",
      "doi-asserted-by": "crossref",
      "first-page": "3303",
      "DOI": "10.1101/gad.12.21.3303",
      "article-title": "Nuclear RNA export",
      "volume": "12",
      "author": "Stutz",
      "year": "1998",
      "journal-title": "Genes Dev."
    },
    {
      "key": "2023072901313361200_Sunetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "1181",
      "DOI": "10.1083/jcb.142.5.1181",
      "article-title": "The hrp23 protein in the balbiani ring pre-mRNP particles is released just before or at the binding of the particles to the nuclear pore complex",
      "volume": "142",
      "author": "Sun",
      "year": "1998",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072901313361200_Visaetal1996a",
      "doi-asserted-by": "crossref",
      "first-page": "5",
      "DOI": "10.1083/jcb.133.1.5",
      "article-title": "A nuclear cap-binding complex binds Balbiani ring pre-mRNA cotranscriptionally and accompanies the ribonucleoprotein particle during nuclear export",
      "volume": "133",
      "author": "Visa",
      "year": "1996",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072901313361200_Visaetal1996b",
      "doi-asserted-by": "crossref",
      "first-page": "253",
      "DOI": "10.1016/S0092-8674(00)80980-0",
      "article-title": "A pre-mRNA-binding protein accompanies the RNA from the gene through the nuclear pores and into polysomes",
      "volume": "84",
      "author": "Visa",
      "year": "1996",
      "journal-title": "Cell."
    },
    {
      "key": "2023072901313361200_vonBesseretal1990",
      "doi-asserted-by": "crossref",
      "first-page": "37",
      "DOI": "10.1007/BF00337601",
      "article-title": "The puff-specific Drosophila protein Bj6, encoded by the gene no-on transient A, shows homology to RNA-binding proteins",
      "volume": "100",
      "author": "von Besser",
      "year": "1990",
      "journal-title": "Chromosoma."
    },
    {
      "key": "2023072901313361200_Wangetal1991",
      "doi-asserted-by": "crossref",
      "first-page": "7391",
      "DOI": "10.1073/pnas.88.16.7391",
      "article-title": "Localization of pre-messenger RNA at discrete nuclear sites",
      "volume": "88",
      "author": "Wang",
      "year": "1991",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072901313361200_Wieslander1994",
      "doi-asserted-by": "crossref",
      "first-page": "275",
      "DOI": "10.1016/S0079-6603(08)60858-2",
      "article-title": "The Balbiani ring multigene familycoding repetitive sequences and evolution of a tissue-specific cell function",
      "volume": "48",
      "author": "Wieslander",
      "year": "1994",
      "journal-title": "Prog. Nucleic Acid Res. Mol. Biol."
    },
    {
      "key": "2023072901313361200_Wurtzetal1996",
      "doi-asserted-by": "crossref",
      "first-page": "1425",
      "DOI": "10.1128/MCB.16.4.1425",
      "article-title": "Identification of two RNA-binding proteins in Balbiani ring premessenger ribonucleoprotein granules and presence of these proteins in specific subsets of heterogeneous nuclear ribonucleoprotein particles",
      "volume": "16",
      "author": "Wurtz",
      "year": "1996",
      "journal-title": "Mol. Cel. Biol."
    },
    {
      "key": "2023072901313361200_Wyss1982",
      "doi-asserted-by": "crossref",
      "first-page": "309",
      "DOI": "10.1016/0014-4827(82)90255-5",
      "article-title": "Chironomus tentans epithelial cell lines sensitive to ecdysteroids, juvenile hormone, insulin and heat shock",
      "volume": "139",
      "author": "Wyss",
      "year": "1982",
      "journal-title": "Exp. Cell Res."
    },
    {
      "key": "2023072901313361200_Xingetal1995",
      "doi-asserted-by": "crossref",
      "first-page": "1635",
      "DOI": "10.1083/jcb.131.6.1635",
      "article-title": "Nonrandom gene organizationstructural arrangements of specific pre-mRNA transcription and splicing with SC-35 domains",
      "volume": "131",
      "author": "Xing",
      "year": "1995",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072901313361200_Zacharetal1993",
      "doi-asserted-by": "crossref",
      "first-page": "729",
      "DOI": "10.1083/jcb.121.4.729",
      "article-title": "Evidence for channeled diffusion of pre-mRNAs during nuclear RNA transport in metazoans",
      "volume": "121",
      "author": "Zachar",
      "year": "1993",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072901313361200_Zimowskaetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "927",
      "DOI": "10.1242/jcs.110.8.927",
      "article-title": "A Drosophila Tpr homolog is localized both in the extrachromosomal channel network and to nuclear pore complexes",
      "volume": "110",
      "author": "Zimowska",
      "year": "1997",
      "journal-title": "J. Cell Sci."
    }
  ],
  "container-title": "The Journal of Cell Biology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://rupress.org/jcb/article-pdf/148/2/271/1854546/9910047.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "syndication"
    },
    {
      "URL": "https://rupress.org/jcb/article-pdf/148/2/271/1854546/9910047.pdf",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        7,
        29
      ]
    ],
    "date-time": "2023-07-29T01:32:25Z",
    "timestamp": 1690594345000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://rupress.org/jcb/article/148/2/271/20442/Electron-Tomography-Reveals-Posttranscriptional"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2000,
        1,
        24
      ]
    ]
  },
  "references-count": 50,
  "journal-issue": {
    "issue": "2",
    "published-print": {
      "date-parts": [
        [
          2000,
          1,
          24
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1083/jcb.148.2.271",
  "relation": {},
  "ISSN": [
    "0021-9525",
    "1540-8140"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        2000,
        1,
        24
      ]
    ]
  }
}