DOI: 10.1083/jcb.148.6.1177. Gemin4 [Penn]

Gemin4

10.1083/jcb.148.6.1177

Crossref journal-article

Rockefeller University Press

The Journal of Cell Biology (291)

Abstract

The survival of motor neurons (SMN) protein, the product of the neurodegenerative disease spinal muscular atrophy (SMA) gene, is localized both in the cytoplasm and in discrete nuclear bodies called gems. In both compartments SMN is part of a large complex that contains several proteins including Gemin2 (formerly SIP1) and the DEAD box protein Gemin3. In the cytoplasm, the SMN complex is associated with snRNP Sm core proteins and plays a critical role in spliceosomal snRNP assembly. In the nucleus, SMN is required for pre-mRNA splicing by serving in the regeneration of spliceosomes. These functions are likely impaired in cells of SMA patients because they have reduced levels of functional SMN. Here, we report the identification by nanoelectrospray mass spectrometry of a novel component of the SMN complex that we name Gemin4. Gemin4 is associated in vivo with the SMN complex through a direct interaction with Gemin3. The tight interaction of Gemin4 with Gemin3 suggests that it could serve as a cofactor of this DEAD box protein. Gemin4 also interacts directly with several of the Sm core proteins. Monoclonal antibodies against Gemin4 efficiently immunoprecipitate the spliceosomal U snRNAs U1 and U5 from Xenopus oocytes cytoplasm. Immunolocalization experiments show that Gemin4 is colocalized with SMN in the cytoplasm and in gems. Interestingly, Gemin4 is also detected in the nucleoli, suggesting that the SMN complex may also function in preribosomal RNA processing or ribosome assembly.

Bibliography

Charroux, B., Pellizzoni, L., Perkinson, R. A., Yong, J., Shevchenko, A., Mann, M., & Dreyfuss, G. (2000). Gemin4. The Journal of Cell Biology, 148(6), 1177â1186.

Authors 7

Bernard Charroux (first)
Livio Pellizzoni (additional)
Robert A. Perkinson (additional)
Jeongsik Yong (additional)
Andrej Shevchenko (additional)
Matthias Mann (additional)
Gideon Dreyfuss (additional)

References 47 Referenced 187

10.1084/jem.173.6.1407 / J. Exp. Med / Human auto antibody to a novel protein of the nuclear coiled bodyimmunological characterization and cDNA cloning of p80-coilin by Andrade (1991)
10.1038/344540a0 / Nature. / Genetic mapping of chronic childhood-onset spinal muscular atrophy to chromosome 5q11.2–13.3 by Brzustowicz (1990)
10.1086/513913 / Am. J. Hum. Genet. / When is a deletion not a deletion? When it is converted by Burghes (1997)
10.1083/jcb.147.4.715 / J. Cell Biol. / The spinal muscular atrophy disease gene product, SMNa link between snRNP biogenesis and the Cajal (coiled) body by Carvalho (1999)
10.1083/jcb.147.6.1181 / J. Cell Biol. / Gemin3, a novel DEAD box protein that interacts with SMN, the spinal muscular atrophy gene product, and is a component of gems by Charroux (1999)
10.1083/jcb.99.6.1997 / J. Cell Biol. / Monoclonal antibody characterization of the C proteins of heterogeneous nuclear ribonucleoprotein complexes in vertebrate cells by Choi (1984)
10.1093/hmg/6.8.1205 / Hum. Mol. Genet. / The survival motor neuron protein in spinal muscular atrophy by Coovert (1997)
10.1126/science.2143847 / Science / An essential signaling role for the m3G cap in the transport of U1 snRNP to the nucleus by Fischer (1990)
10.1016/S0092-8674(00)80368-2 / Cell. / The SMN-SIP1 complex has an essential role in spliceosomal snRNP biogenesis by Fischer (1997)
10.1073/pnas.95.11.6492 / Proc. Natl. Acad. Sci. USA. / Heterogeneity of subcellular localization and electrophoretic mobility of survival motor neuron (SMN) protein in mammalian neural cells and tissues by Francis (1998)
10.1002/dvg.1020160107 / Dev. Genet. / Is the sphere organelle/coiled body a universal nuclear component? by Gall (1995)
10.1038/3030 / Nat. Genet. / Differential SMN2 expression associated with SMA severity by Gavrilov (1998)
10.1006/bbrc.1995.2135 / Biochem. Biophys. Res. Commun / Survival motor neuron gene transcript analysis in muscles from spinal muscular atrophy patients by Gennarelli (1995)
10.1126/science.280.5363.547 / Science. / Structure and function in the nucleus by Lamond (1998)
10.1016/0092-8674(95)90460-3 / Cell. / Identification and characterization of a spinal muscular atrophy-determining gene by Lefebvre (1995)
10.1038/ng0797-265 / Nat. Genet. / Correlation between severity and SMN protein level in spinal muscular atrophy by Lefebvre (1997)
10.1073/pnas.76.11.5495 / Proc. Natl. Acad. Sci. USA. / Antibodies to small nuclear RNAs complexed with proteins are produced by patients with systemic lupus erythematosus by Lerner (1979)
10.1073/pnas.78.5.2737 / Proc. Natl. Acad. Sci. USA. / Monoclonal antibodies to nucleic acid-containing cellular constituentsprobes for molecular biology and autoimmune disease by Lerner (1981)
10.1002/j.1460-2075.1996.tb00725.x / EMBO (Eur. Mol. Biol. Organ.) J. / A novel nuclear structure containing the survival of motor neuron proteins by Liu (1996)
10.1016/S0092-8674(00)80367-0 / Cell. / The spinal muscular atrophy disease gene product, SMN, and its associated protein SIP1 are in a complex with spliceosomal snRNP proteins by Liu (1997)
10.1038/ng0598-63 / Nat. Genet. / SMN oligomerization defect correlates with spinal muscular atrophy severity by Lorson (1998)
10.1073/pnas.96.11.6307 / Proc. Natl. Acad. Sci. USA. / A single nucleotide in the SMN gene regulates splicing and is responsible for spinal muscular atrophy by Lorson (1999)
10.1016/0167-4781(90)90001-I / Biochim. Biophys. Acta. / Structure of spliceosomal snRNPs and their role in pre-mRNA splicing by Luhrmann (1990)
10.1016/S0962-8924(99)01606-2 / Trends Cell Biology. / Nuclear bodiesmultifaceted subdomains of the interchromatin space by Matera (1999)
10.1086/301992 / Am. J. Hum. Genet. / Coiled bodies and gemsJanus or gemini? by Matera (1998)
10.1016/0092-8674(86)90072-3 / Cell. / Cap trimethylation of U snRNA is cytoplasmic and dependent on U snRNP protein binding by Mattaj (1986)
10.1007/978-3-642-73020-7_4 / Structure and Function of Major and Minor Small Nuclear Ribonucleoprotein Particles., M / UsnRNP assembly and transport by Mattaj (1988)
10.1016/0092-8674(85)90314-9 / Cell. / Nuclear segregation of U2 snRNA requires binding of specific snRNP proteins by Mattaj (1985)
10.1146/annurev.bi.64.070195.004341 / Annu. Rev. Biochem. / The small nucleolar RNAs by Maxwell (1995)
{'key': '2023072902014267100_Melki1999', 'first-page': '43', 'article-title': 'Molecular basis of spinal muscular atrophyrecent advances', 'volume': '14', 'author': 'Melki', 'year': '1999', 'journal-title': 'J. Child. Neurol.'} / J. Child. Neurol. / Molecular basis of spinal muscular atrophyrecent advances by Melki (1999)
10.1038/344767a0 / Nature. / Gene for chronic spinal muscular atrophies maps to chromosome 5q by Melki (1990)
10.1126/science.7910982 / Science / De novo and inherited deletions of the 5q13 region in spinal muscular atrophies by Melki (1994)
10.1128/MCB.10.7.3365 / Mol. Cell. Biol / Nucleocytoplasmic transport and processing of small nuclear RNA precursors by Neuman de Vegvar (1990)
10.1016/0014-4827(91)90421-P / Exp. Cell Res. / Detection of fibrillarin in nucleolar remnants and the nucleolar matrix by Ochs (1991)
10.1016/S0140-6736(80)90847-8 / Lancet / Classification of spinal muscular atrophies by Pearn (1980)
10.1016/S0092-8674(00)81632-3 / Cell. / A novel function for SMN, the spinal muscular atrophy disease gene product, in pre-mRNA splicing by Pellizzoni (1998)
10.1073/pnas.96.20.11167 / Proc. Natl. Acad. Sci. USA. / SMN mutants of spinal muscular atrophy patients are defective in binding to SnRNP proteins by Pellizzoni (1999)
10.1101/gad.2.2.215 / Genes Dev. / Immunopurification of heterogeneous nuclear ribonucleoprotein particles reveals an assortment of RNA-binding proteins by Pinol-Roma (1988)
10.1016/1047-8477(90)90066-L / J. Struct. Biol. / Association between the nucleolus and the coiled body by Raska (1990)
10.1007/BF02899205 / Virchows Arch. B. Cell. Pathol. Incl. Mol. Pathol. / Human autoantibodiesprobes for nucleolus structure and function by Reimer (1987)
10.1021/ac950914h / Anal. Chemistry. / Mass spectrometric sequencing of proteins from silver stained polyacrylamide gels by Shevchenko (1996)
10.1016/S0092-8674(00)80411-0 / Cell. / Compartmentalization of eukaryotic gene expressioncauses and effects by Singer (1997)
10.1016/S0960-9822(99)80475-8 / Curr. Biol. / Newly assembled snRNPs associate with coiled bodies before speckles, suggesting a nuclear snRNP maturation pathway by Sleeman (1999)
10.1016/S0092-8674(00)80247-0 / Cell. / Sno storm in the nucleolusnew roles for myriad small RNPs by Smith (1997)
10.1002/j.1460-2075.1989.tb08463.x / EMBO (Eur. Mol. Biol. Organ.) J. / U3, U8 and U13 comprise a new class of mammalian snRNPs localized in the cell nucleolus by Tyc (1989)
10.1038/379466a0 / Nature / Femtomole sequencing of proteins from polyacrylamide gels by nano electrospray mass spectrometry by Wilm (1996)
10.3109/10409239009090604 / Crit. Rev. Biochem. Mol. Biol. / Cell biology of the snRNP particles by Zieve (1990)

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, 10:02 p.m.)
Indexed	3 weeks, 2 days ago (Aug. 7, 2025, 4:51 a.m.)
Issued	25 years, 5 months ago (March 20, 2000)
Published	25 years, 5 months ago (March 20, 2000)
Published Online	25 years, 5 months ago (March 20, 2000)
Published Print	25 years, 5 months ago (March 20, 2000)

Funders 0

None

BibTeX

@article{Charroux_2000, title={Gemin4}, volume={148}, ISSN={1540-8140}, url={http://dx.doi.org/10.1083/jcb.148.6.1177}, DOI={10.1083/jcb.148.6.1177}, number={6}, journal={The Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Charroux, Bernard and Pellizzoni, Livio and Perkinson, Robert A. and Yong, Jeongsik and Shevchenko, Andrej and Mann, Matthias and Dreyfuss, Gideon}, year={2000}, month=mar, pages={1177–1186} }

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      "first-page": "1407",
      "DOI": "10.1084/jem.173.6.1407",
      "article-title": "Human auto antibody to a novel protein of the nuclear coiled bodyimmunological characterization and cDNA cloning of p80-coilin",
      "volume": "173",
      "author": "Andrade",
      "year": "1991",
      "journal-title": "J. Exp. Med"
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    {
      "key": "2023072902014267100_Brzustowiczetal1990",
      "doi-asserted-by": "crossref",
      "first-page": "540",
      "DOI": "10.1038/344540a0",
      "article-title": "Genetic mapping of chronic childhood-onset spinal muscular atrophy to chromosome 5q11.2\u201313.3",
      "volume": "344",
      "author": "Brzustowicz",
      "year": "1990",
      "journal-title": "Nature."
    },
    {
      "key": "2023072902014267100_Burghes1997",
      "doi-asserted-by": "crossref",
      "first-page": "9",
      "DOI": "10.1086/513913",
      "article-title": "When is a deletion not a deletion? When it is converted",
      "volume": "61",
      "author": "Burghes",
      "year": "1997",
      "journal-title": "Am. J. Hum. Genet."
    },
    {
      "key": "2023072902014267100_Carvalhoetal1999",
      "doi-asserted-by": "crossref",
      "first-page": "715",
      "DOI": "10.1083/jcb.147.4.715",
      "article-title": "The spinal muscular atrophy disease gene product, SMNa link between snRNP biogenesis and the Cajal (coiled) body",
      "volume": "147",
      "author": "Carvalho",
      "year": "1999",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072902014267100_Charrouxetal1999",
      "doi-asserted-by": "crossref",
      "first-page": "1181",
      "DOI": "10.1083/jcb.147.6.1181",
      "article-title": "Gemin3, a novel DEAD box protein that interacts with SMN, the spinal muscular atrophy gene product, and is a component of gems",
      "volume": "147",
      "author": "Charroux",
      "year": "1999",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072902014267100_ChoiandDreyfuss1984",
      "doi-asserted-by": "crossref",
      "first-page": "1997",
      "DOI": "10.1083/jcb.99.6.1997",
      "article-title": "Monoclonal antibody characterization of the C proteins of heterogeneous nuclear ribonucleoprotein complexes in vertebrate cells",
      "volume": "99",
      "author": "Choi",
      "year": "1984",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072902014267100_Coovertetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "1205",
      "DOI": "10.1093/hmg/6.8.1205",
      "article-title": "The survival motor neuron protein in spinal muscular atrophy",
      "volume": "6",
      "author": "Coovert",
      "year": "1997",
      "journal-title": "Hum. Mol. Genet."
    },
    {
      "key": "2023072902014267100_N0x29f3c00N0x29fe798",
      "doi-asserted-by": "crossref",
      "first-page": "786",
      "DOI": "10.1126/science.2143847",
      "article-title": "An essential signaling role for the m3G cap in the transport of U1 snRNP to the nucleus",
      "volume": "249",
      "author": "Fischer",
      "year": "1990",
      "journal-title": "Science"
    },
    {
      "key": "2023072902014267100_Fischeretal1997",
      "doi-asserted-by": "crossref",
      "first-page": "1023",
      "DOI": "10.1016/S0092-8674(00)80368-2",
      "article-title": "The SMN-SIP1 complex has an essential role in spliceosomal snRNP biogenesis",
      "volume": "90",
      "author": "Fischer",
      "year": "1997",
      "journal-title": "Cell."
    },
    {
      "key": "2023072902014267100_Francisetal1998",
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      "first-page": "6492",
      "DOI": "10.1073/pnas.95.11.6492",
      "article-title": "Heterogeneity of subcellular localization and electrophoretic mobility of survival motor neuron (SMN) protein in mammalian neural cells and tissues",
      "volume": "95",
      "author": "Francis",
      "year": "1998",
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      "key": "2023072902014267100_Galletal1995",
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      "first-page": "25",
      "DOI": "10.1002/dvg.1020160107",
      "article-title": "Is the sphere organelle/coiled body a universal nuclear component?",
      "volume": "16",
      "author": "Gall",
      "year": "1995",
      "journal-title": "Dev. Genet."
    },
    {
      "key": "2023072902014267100_Gavrilovetal1998",
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      "first-page": "230",
      "DOI": "10.1038/3030",
      "article-title": "Differential SMN2 expression associated with SMA severity",
      "volume": "20",
      "author": "Gavrilov",
      "year": "1998",
      "journal-title": "Nat. Genet."
    },
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      "author": "Gennarelli",
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      "author": "Lamond",
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    },
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      "key": "2023072902014267100_Lefebvreetal1995",
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      "first-page": "155",
      "DOI": "10.1016/0092-8674(95)90460-3",
      "article-title": "Identification and characterization of a spinal muscular atrophy-determining gene",
      "volume": "89",
      "author": "Lefebvre",
      "year": "1995",
      "journal-title": "Cell."
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    {
      "key": "2023072902014267100_Lefebvreetal1997",
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      "first-page": "265",
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      "volume": "16",
      "author": "Lefebvre",
      "year": "1997",
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    },
    {
      "key": "2023072902014267100_LernerandSteitz1979",
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      "first-page": "5495",
      "DOI": "10.1073/pnas.76.11.5495",
      "article-title": "Antibodies to small nuclear RNAs complexed with proteins are produced by patients with systemic lupus erythematosus",
      "volume": "76",
      "author": "Lerner",
      "year": "1979",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
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      "key": "2023072902014267100_Lerneretal1981",
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      "article-title": "Monoclonal antibodies to nucleic acid-containing cellular constituentsprobes for molecular biology and autoimmune disease",
      "volume": "78",
      "author": "Lerner",
      "year": "1981",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072902014267100_LiuandDreyfuss1996",
      "doi-asserted-by": "crossref",
      "first-page": "3555",
      "DOI": "10.1002/j.1460-2075.1996.tb00725.x",
      "article-title": "A novel nuclear structure containing the survival of motor neuron proteins",
      "volume": "15",
      "author": "Liu",
      "year": "1996",
      "journal-title": "EMBO (Eur. Mol. Biol. Organ.) J."
    },
    {
      "key": "2023072902014267100_Liuetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "1013",
      "DOI": "10.1016/S0092-8674(00)80367-0",
      "article-title": "The spinal muscular atrophy disease gene product, SMN, and its associated protein SIP1 are in a complex with spliceosomal snRNP proteins",
      "volume": "90",
      "author": "Liu",
      "year": "1997",
      "journal-title": "Cell."
    },
    {
      "key": "2023072902014267100_Lorsonetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "63",
      "DOI": "10.1038/ng0598-63",
      "article-title": "SMN oligomerization defect correlates with spinal muscular atrophy severity",
      "volume": "19",
      "author": "Lorson",
      "year": "1998",
      "journal-title": "Nat. Genet."
    },
    {
      "key": "2023072902014267100_Lorsonetal1999",
      "doi-asserted-by": "crossref",
      "first-page": "6307",
      "DOI": "10.1073/pnas.96.11.6307",
      "article-title": "A single nucleotide in the SMN gene regulates splicing and is responsible for spinal muscular atrophy",
      "volume": "96",
      "author": "Lorson",
      "year": "1999",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072902014267100_Luhrmannetal1990",
      "doi-asserted-by": "crossref",
      "first-page": "265",
      "DOI": "10.1016/0167-4781(90)90001-I",
      "article-title": "Structure of spliceosomal snRNPs and their role in pre-mRNA splicing",
      "volume": "1087",
      "author": "Luhrmann",
      "year": "1990",
      "journal-title": "Biochim. Biophys. Acta."
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      "key": "2023072902014267100_Matera1999",
      "doi-asserted-by": "crossref",
      "first-page": "302",
      "DOI": "10.1016/S0962-8924(99)01606-2",
      "article-title": "Nuclear bodiesmultifaceted subdomains of the interchromatin space",
      "volume": "9",
      "author": "Matera",
      "year": "1999",
      "journal-title": "Trends Cell Biology."
    },
    {
      "key": "2023072902014267100_MateraandFrey1998",
      "doi-asserted-by": "crossref",
      "first-page": "317",
      "DOI": "10.1086/301992",
      "article-title": "Coiled bodies and gemsJanus or gemini?",
      "volume": "63",
      "author": "Matera",
      "year": "1998",
      "journal-title": "Am. J. Hum. Genet."
    },
    {
      "key": "2023072902014267100_Mattaj1986",
      "doi-asserted-by": "crossref",
      "first-page": "905",
      "DOI": "10.1016/0092-8674(86)90072-3",
      "article-title": "Cap trimethylation of U snRNA is cytoplasmic and dependent on U snRNP protein binding",
      "volume": "46",
      "author": "Mattaj",
      "year": "1986",
      "journal-title": "Cell."
    },
    {
      "key": "2023072902014267100_Mattaj1988",
      "doi-asserted-by": "crossref",
      "first-page": "100",
      "DOI": "10.1007/978-3-642-73020-7_4",
      "article-title": "UsnRNP assembly and transport",
      "volume-title": "Structure and Function of Major and Minor Small Nuclear Ribonucleoprotein Particles., M",
      "author": "Mattaj",
      "year": "1988"
    },
    {
      "key": "2023072902014267100_MattajandDeRobertis1985",
      "doi-asserted-by": "crossref",
      "first-page": "111",
      "DOI": "10.1016/0092-8674(85)90314-9",
      "article-title": "Nuclear segregation of U2 snRNA requires binding of specific snRNP proteins",
      "volume": "40",
      "author": "Mattaj",
      "year": "1985",
      "journal-title": "Cell."
    },
    {
      "key": "2023072902014267100_MaxwellandFournier1995",
      "doi-asserted-by": "crossref",
      "first-page": "897",
      "DOI": "10.1146/annurev.bi.64.070195.004341",
      "article-title": "The small nucleolar RNAs",
      "volume": "35",
      "author": "Maxwell",
      "year": "1995",
      "journal-title": "Annu. Rev. Biochem."
    },
    {
      "key": "2023072902014267100_Melki1999",
      "first-page": "43",
      "article-title": "Molecular basis of spinal muscular atrophyrecent advances",
      "volume": "14",
      "author": "Melki",
      "year": "1999",
      "journal-title": "J. Child. Neurol."
    },
    {
      "key": "2023072902014267100_Melkietal1990",
      "doi-asserted-by": "crossref",
      "first-page": "767",
      "DOI": "10.1038/344767a0",
      "article-title": "Gene for chronic spinal muscular atrophies maps to chromosome 5q",
      "volume": "344",
      "author": "Melki",
      "year": "1990",
      "journal-title": "Nature."
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    {
      "key": "2023072902014267100_Melkietal1994",
      "doi-asserted-by": "crossref",
      "first-page": "1474",
      "DOI": "10.1126/science.7910982",
      "article-title": "De novo and inherited deletions of the 5q13 region in spinal muscular atrophies",
      "volume": "264",
      "author": "Melki",
      "year": "1994",
      "journal-title": "Science"
    },
    {
      "key": "2023072902014267100_NeumandeVegvarandDahlberg1990",
      "doi-asserted-by": "crossref",
      "first-page": "3365",
      "DOI": "10.1128/MCB.10.7.3365",
      "article-title": "Nucleocytoplasmic transport and processing of small nuclear RNA precursors",
      "volume": "10",
      "author": "Neuman de Vegvar",
      "year": "1990",
      "journal-title": "Mol. Cell. Biol"
    },
    {
      "key": "2023072902014267100_OchsandSmetana1991",
      "doi-asserted-by": "crossref",
      "first-page": "183",
      "DOI": "10.1016/0014-4827(91)90421-P",
      "article-title": "Detection of fibrillarin in nucleolar remnants and the nucleolar matrix",
      "volume": "197",
      "author": "Ochs",
      "year": "1991",
      "journal-title": "Exp. Cell Res."
    },
    {
      "key": "2023072902014267100_Pearn1980",
      "doi-asserted-by": "crossref",
      "first-page": "919",
      "DOI": "10.1016/S0140-6736(80)90847-8",
      "article-title": "Classification of spinal muscular atrophies",
      "volume": "1",
      "author": "Pearn",
      "year": "1980",
      "journal-title": "Lancet"
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    {
      "key": "2023072902014267100_Pellizzonietal1998",
      "doi-asserted-by": "crossref",
      "first-page": "615",
      "DOI": "10.1016/S0092-8674(00)81632-3",
      "article-title": "A novel function for SMN, the spinal muscular atrophy disease gene product, in pre-mRNA splicing",
      "volume": "95",
      "author": "Pellizzoni",
      "year": "1998",
      "journal-title": "Cell."
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    {
      "key": "2023072902014267100_Pellizzonietal1999",
      "doi-asserted-by": "crossref",
      "first-page": "11167",
      "DOI": "10.1073/pnas.96.20.11167",
      "article-title": "SMN mutants of spinal muscular atrophy patients are defective in binding to SnRNP proteins",
      "volume": "96",
      "author": "Pellizzoni",
      "year": "1999",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072902014267100_Pinol-Romaetal1988",
      "doi-asserted-by": "crossref",
      "first-page": "215",
      "DOI": "10.1101/gad.2.2.215",
      "article-title": "Immunopurification of heterogeneous nuclear ribonucleoprotein particles reveals an assortment of RNA-binding proteins",
      "volume": "2",
      "author": "Pinol-Roma",
      "year": "1988",
      "journal-title": "Genes Dev."
    },
    {
      "key": "2023072902014267100_Raskaetal1990",
      "doi-asserted-by": "crossref",
      "first-page": "120",
      "DOI": "10.1016/1047-8477(90)90066-L",
      "article-title": "Association between the nucleolus and the coiled body",
      "volume": "10",
      "author": "Raska",
      "year": "1990",
      "journal-title": "J. Struct. Biol."
    },
    {
      "key": "2023072902014267100_Reimeretal1987",
      "doi-asserted-by": "crossref",
      "first-page": "131",
      "DOI": "10.1007/BF02899205",
      "article-title": "Human autoantibodiesprobes for nucleolus structure and function",
      "volume": "54",
      "author": "Reimer",
      "year": "1987",
      "journal-title": "Virchows Arch. B. Cell. Pathol. Incl. Mol. Pathol."
    },
    {
      "key": "2023072902014267100_Shevchenkoetal1996",
      "doi-asserted-by": "crossref",
      "first-page": "850",
      "DOI": "10.1021/ac950914h",
      "article-title": "Mass spectrometric sequencing of proteins from silver stained polyacrylamide gels",
      "volume": "68",
      "author": "Shevchenko",
      "year": "1996",
      "journal-title": "Anal. Chemistry."
    },
    {
      "key": "2023072902014267100_SingerandGreen1997",
      "doi-asserted-by": "crossref",
      "first-page": "291",
      "DOI": "10.1016/S0092-8674(00)80411-0",
      "article-title": "Compartmentalization of eukaryotic gene expressioncauses and effects",
      "volume": "91",
      "author": "Singer",
      "year": "1997",
      "journal-title": "Cell."
    },
    {
      "key": "2023072902014267100_SleemanandLamond1999",
      "doi-asserted-by": "crossref",
      "first-page": "1065",
      "DOI": "10.1016/S0960-9822(99)80475-8",
      "article-title": "Newly assembled snRNPs associate with coiled bodies before speckles, suggesting a nuclear snRNP maturation pathway",
      "volume": "9",
      "author": "Sleeman",
      "year": "1999",
      "journal-title": "Curr. Biol."
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    {
      "key": "2023072902014267100_SmithandSteitz1997",
      "doi-asserted-by": "crossref",
      "first-page": "669",
      "DOI": "10.1016/S0092-8674(00)80247-0",
      "article-title": "Sno storm in the nucleolusnew roles for myriad small RNPs",
      "volume": "89",
      "author": "Smith",
      "year": "1997",
      "journal-title": "Cell."
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    {
      "key": "2023072902014267100_TycandSteitz1989",
      "doi-asserted-by": "crossref",
      "first-page": "3113",
      "DOI": "10.1002/j.1460-2075.1989.tb08463.x",
      "article-title": "U3, U8 and U13 comprise a new class of mammalian snRNPs localized in the cell nucleolus",
      "volume": "8",
      "author": "Tyc",
      "year": "1989",
      "journal-title": "EMBO (Eur. Mol. Biol. Organ.) J."
    },
    {
      "key": "2023072902014267100_Wilmetal1996",
      "doi-asserted-by": "crossref",
      "first-page": "466",
      "DOI": "10.1038/379466a0",
      "article-title": "Femtomole sequencing of proteins from polyacrylamide gels by nano electrospray mass spectrometry",
      "volume": "379",
      "author": "Wilm",
      "year": "1996",
      "journal-title": "Nature"
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    {
      "key": "2023072902014267100_ZieveandSauterer1990",
      "doi-asserted-by": "crossref",
      "first-page": "1",
      "DOI": "10.3109/10409239009090604",
      "article-title": "Cell biology of the snRNP particles",
      "volume": "25",
      "author": "Zieve",
      "year": "1990",
      "journal-title": "Crit. Rev. Biochem. Mol. Biol."
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