DOI: 10.1083/jcb.149.2.293. The Ribosomal RNA Processing Machinery Is Recruited to the Nucleolar Domain before RNA Polymerase I during <i>Xenopus laevis</i> Development

The Ribosomal RNA Processing Machinery Is Recruited to the Nucleolar Domain before RNA Polymerase I during Xenopus laevis Development

10.1083/jcb.149.2.293

Crossref journal-article

Rockefeller University Press

The Journal of Cell Biology (291)

Abstract

Transcription and splicing of messenger RNAs are temporally and spatially coordinated through the recruitment by RNA polymerase II of processing factors. We questioned whether RNA polymerase I plays a role in the recruitment of the ribosomal RNA (rRNA) processing machinery. During Xenopus laevis embryogenesis, recruitment of the rRNA processing machinery to the nucleolar domain occurs in two steps: two types of precursor structures called prenucleolar bodies (PNBs) form independently throughout the nucleoplasm; and components of PNBs I (fibrillarin, nucleolin, and the U3 and U8 small nucleolar RNAs) fuse to the nucleolar domain before components of PNBs II (B23/NO38). This fusion process is independent of RNA polymerase I activity, as shown by actinomycin D treatment of embryos and by the lack of detectable RNA polymerase I at ribosomal gene loci during fusion. Instead, this process is concomitant with the targeting of maternally derived pre-rRNAs to the nucleolar domain. Absence of fusion was correlated with absence of these pre-rRNAs in nuclei where RNA polymerase II and III are inhibited. Therefore, during X. laevis embryogenesis, the recruitment of the rRNA processing machinery to the nucleolar domain could be dependent on the presence of pre-rRNAs, but is independent of either zygotic RNA polymerase I transcription or the presence of RNA polymerase I itself.

Bibliography

Verheggen, C., Almouzni, G., & Hernandez-Verdun, D. (2000). The Ribosomal RNA Processing Machinery Is Recruited to the Nucleolar Domain before RNA Polymerase I during Xenopus laevis Development. The Journal of Cell Biology, 149(2), 293â306.

Authors 3

Céline Verheggen (first)
Geneviève Almouzni (additional)
Danièle Hernandez-Verdun (additional)

References 77 Referenced 46

10.1101/gad.13.16.2148 / Genes Dev. / The yeast exosome and human PM-Scl are related complexes of 3′-5′ exonucleases by Allmang (1999)
{'key': '2023072902063100100_Almouzni1998'}
10.1002/j.1460-2075.1995.tb07164.x / EMBO (Eur. Mol. Biol. Organ.) J. / Constraints on transcriptional activator function contribute to transcriptional quiescence during early Xenopus embryogenesis by Almouzni (1995)
10.1242/jcs.107.2.463 / J. Cell Sci. / Cell cycle redistribution of U3 snRNA and fibrillarin. Presence in the cytoplasmic nucleolus remnant and in the prenucleolar bodies at telophase by Azum-Gélade (1994)
10.1091/mbc.8.1.73 / Mol. Biol. Cell / Coiled bodies without coilin by Bauer (1997)
10.1091/mbc.5.6.633 / Mol. Biol. Cell. / In vitro assembly of coiled bodies in Xenopus egg extract by Bauer (1994)
10.1242/jcs.110.1.43 / J. Cell Sci. / Prenucleolar bodies contain coilin and are assembled in Xenopus egg extract depleted of specific nucleolar proteins and U3 RNA by Bell (1997)
10.1006/excr.1999.4411 / Exp. Cell Res. / Developmental changes in RNA polymerase I and TATA box-binding protein during early Xenopus embryogenesis by Bell (1999)
10.1083/jcb.118.6.1297 / J. Cell Biol. / In vitro assembly of prenucleolar bodies in Xenopus egg extract by Bell (1992)
10.1242/jcs.110.17.2053 / J. Cell Sci. / Association of the nucleolar transcription factor UBF with the transcriptionally inactive rRNA genes of pronuclei and early Xenopus embryos by Bell (1997)
10.1083/jcb.105.4.1483 / J. Cell Biol. / Inhibition of nucleolar reformation after microinjection of antibodies to RNA polymerase I into mitotic cells by Benavente (1987)
10.1016/S0955-0674(99)80048-9 / Curr. Opin. Cell Biol. / Coupling RNA polymerase II transcription with pre-mRNA processing by Bentley (1999)
10.1242/jcs.109.6.1241 / J. Cell Sci. / The organization of ribosomal RNA processing correlates with the distribution of nucleolar snRNAs by Beven (1996)
10.1091/mbc.10.7.2297 / Mol. Biol. Cell. / The movement of coiled bodies visualized in living plant cells by the green fluorescent protein by Boudonck (1999)
10.1074/jbc.273.21.13255 / J. Biol. Chem. / Rrp6p, the yeast homologue of the human PM-Scl 100-kDa autoantigen, is essential for efficient 5.8 S rRNA 3′ end formation by Briggs (1998)
10.1016/S0022-2836(64)80116-9 / J. Mol. Biol. / RNA synthesis during development of Xenopus laevis, the South African clawed toad by Brown (1964)
10.1016/S0968-0004(97)01125-0 / Trends Biochem. Sci. / A CTD function linking transcription to splicing by Corden (1997)
10.1093/emboj/16.2.417 / EMBO (Eur. Mol. Biol. Organ.) J. / Pop3p is essential for the activity of the RNase MRP and RNase P ribonucleoproteins in vivo by Dichtl (1997)
10.1007/BF02510477 / Chromosoma. / A class of nonribosomal nucleolar components is located in chromosome periphery and in nucleolus-derived foci during anaphase and telophase by Dundr (1997)
{'key': '2023072902063100100_Duvaletal1990', 'first-page': '4123', 'article-title': 'Stability of maternal mRNA in Xenopus embryosrole of transcription and translation', 'volume': '10', 'author': 'Duval', 'year': '1990', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Stability of maternal mRNA in Xenopus embryosrole of transcription and translation by Duval (1990)
10.1006/excr.1999.4578 / Exp. Cell Res. / Effects of anti-PM-Scl 100 (Rr6p exonuclease) antibodies on prenucleolar body dynamics at the end of mitosis by Fomproix (1999)
10.1242/jcs.111.3.359 / J. Cell Sci. / Effects of anti-fibrillarin antibodies on building of functional nucleoli at the end of mitosis by Fomproix (1998)
10.1016/S0960-9822(99)80066-9 / Curr. Biol. / Association of snRNA genes with the coiled bodies is mediated by nascent snRNA transcripts by Frey (1999)
10.1091/mbc.10.12.4385 / Mol. Biol. Cell. / Assembly of the nuclear transcription and processing machinerycajal bodies (coiled bodies) and transcriptosomes by Gall (1999)
10.1016/S0248-4900(94)80010-3 / Biol. Cell. / Fate of specific nucleolar perichromosomal proteins during mitosiscellular distribution and association with U3 snoRNA by Gautier (1994)
10.1083/jcb.60.2.502 / J. Cell Biol. / Experimental analysis of nucleolar reorganization by Giménez-Martin (1974)
10.1093/emboj/17.5.1476 / EMBO (Eur. Mol. Biol. Organ.) J. / Nucleolin functions in the first step of ribosomal RNA processing by Ginisty (1998)
{'key': '2023072902063100100_GurdonandWickens1983', 'first-page': '101:370', 'article-title': 'Use of Xenopus oocytes for the expression of cloned genes', 'volume-title': 'Methods in Enzymology', 'author': 'Gurdon', 'year': '1983'} / Methods in Enzymology / Use of Xenopus oocytes for the expression of cloned genes by Gurdon (1983)
{'key': '2023072902063100100_Hadjiolov1985'}
10.1242/jcs.104.3.843 / J. Cell Sci. / Different patterns of rDNA distribution in Pisum sativum nucleoli correlate with different levels of nucleolar activity by Highett (1993)
10.1002/(SICI)1097-4644(199608)62:2<191::AID-JCB7>3.0.CO;2-N / J. Cell Biochem. / Dynamic organization of pre-mRNA splicing factors by Huang (1996)
10.1083/jcb.133.4.719 / J. Cell Biol. / Intron-dependent recruitment of pre-mRNA splicing factors to sites of transcription by Huang (1996)
10.1016/0092-8674(93)90159-N / Cell. / In vivo evidence that transcription and splicing are coordinated by a recruiting mechanism by Jiménez-Garcia (1993)
10.1111/j.1768-322X.1989.tb00795.x / Biol. Cell. / Nucleologenesisuse of non-isotopic in situ hybridization and immunocytochemistry to compare the localization of rDNA and nucleolar proteins during mitosis by Jiménez-Garcia (1989)
10.1091/mbc.5.9.955 / Mol. Biol. Cell. / NucleologenesisU3 snRNA-containing prenucleolar bodies move to sites of active pre-rRNA transcription after mitosis by Jiménez-Garcia (1994)
10.1073/pnas.96.12.6769 / Proc. Natl. Acad. Sci. USA. / Rapid and reversible relocalization of heat shock factor 1 within seconds to nuclear stress granules by Jolly (1999)
10.1083/jcb.145.6.1133 / J. Cell Biol. / Intron-independent association of splicing factors with active genes by Jolly (1999)
10.1126/science.280.5363.547 / Science. / Structure and function in the nucleus by Lamond (1998)
10.1126/science.272.5259.268 / Science. / Accurate processing of a eukaryotic pre-rRNA by RNase MRP in vitro by Lygerou (1996)
10.1002/j.1460-2075.1996.tb00980.x / EMBO (Eur. Mol. Biol. Organ.) J. / hPop1an autoantigenic protein subunit shared by the human RNase P and RNase MRP ribonucleoproteins by Lygerou (1996)
10.1006/excr.1996.0209 / Exp. Cell Res. / Conditions favoring RNA polymerase I transcription in permeabilized cells by Masson (1996)
10.1038/385357a0 / Nature. / The C-terminal domain of RNA polymerase II couples mRNA processing to transcription by McCracken (1997)
{'key': '2023072902063100100_MebmerandDreyer1993', 'first-page': '369', 'article-title': 'Requirement for nuclear translocation and nucleolar accumulation of nucleolin of Xenopus laevis', 'volume': '61', 'author': 'Mebmer', 'year': '1993', 'journal-title': 'Eur. J. Cell. Biol.'} / Eur. J. Cell. Biol. / Requirement for nuclear translocation and nucleolar accumulation of nucleolin of Xenopus laevis by Mebmer (1993)
10.1093/nar/27.11.2271 / Nucleic Acids Res. / Evolutionarily conserved structural features in the ITS2 of mammalian pre-rRNAs and potential interactions with the snoRNA U8 detected by comparative analysis of new mouse sequences by Michot (1999)
10.1016/S0955-0674(98)80007-0 / Curr. Opin. Cell Biol. / The cellular organization of gene expression by Misteli (1998)
10.1016/S1097-2765(01)80002-2 / Mol. Cell. / RNA polymerase II targets pre-mRNA splicing factors to transcription sites in vivo by Misteli (1999)
10.1038/387523a0 / Nature. / The dynamics of a pre-mRNA splicing factor in living cells by Misteli (1997)
10.1016/S0092-8674(00)80432-8 / Cell. / The exosomea conserved eukaryotic RNA processing complex containing multiple 3′-5′ exoribonucleases by Mitchell (1997)
10.1093/hmg/4.suppl_1.1779 / Hum. Mol. Genet. / Compartmentalization of specific pre-mRNA metabolisman emerging view by Moen (1995)
10.1016/0014-4827(76)90046-X / Exp. Cell Res. / Nucleolar transcription during plant mitosis by Morcillo (1976)
10.1016/0092-8674(82)90272-0 / Cell. / A major developmental transition in early Xenopus embryos. I. Characterization and timing of cellular changes at the midblastula stage by Newport (1982)
{'key': '2023072902063100100_NieuwkoopandFaber1994', 'volume-title': 'Normal table of Xenopus laevis (Daudin)', 'author': 'Nieuwkoop', 'year': '1994'} / Normal table of Xenopus laevis (Daudin) by Nieuwkoop (1994)
10.1083/jcb.143.1.23 / J. Cell Biol. / Mutational analysis of the structure and localization of the nucleolus in the yeast Saccharomyces cerevisiae by Oakes (1998)
10.1016/0014-4827(91)90421-P / Exp. Cell Res. / Detection of fibrillarin in nucleolar remnants and the nucleolar matrix by Ochs (1991)
10.1007/BF00327463 / Chromosoma. / Nucleologenesiscomposition and fate of prenucleolar bodies by Ochs (1985)
10.1111/j.1768-322X.1985.tb00387.x / Biol. Cell. / Fibrillarina new protein of the nucleolus identified by autoimmune sera by Ochs (1985)
10.1016/0092-8674(93)90651-6 / Cell. / Disruption of U8 nucleolar snRNA inhibits 5.8S and 28S rRNA processing in the Xenopus oocyte by Peculis (1993)
10.1017/S1355838299982079 / RNA. / RNA–protein interactions in the human RNase MRP ribonucleoprotein complex by Pluk (1999)
10.1101/gad.13.12.1513 / Genes Dev. / Developmental regulation of SR protein phosphorylation and activity by Sanford (1999)
10.1242/jcs.112.12.1889 / J. Cell Sci. / The nucleolar antigen Nop 52, the human homologue of the yeast ribosomal RNA processing RRP1, is recruited at late stages of nucleologenesis by Savino (1999)
10.1093/nar/26.19.4508 / Nucleic Acids Res. / Preferential cleavage in pre-ribosomal RNA by protein B23 endoribonuclease by Savkur (1998)
10.1002/bies.950120104 / BioEssay. / Functional and dynamic aspects of the mammalian nucleolus by Scheer (1990)
10.1016/0962-8924(93)90123-I / Trends Cell Biol. / Structure, function and assembly of the nucleolus by Scheer (1993)
10.1016/0955-0674(94)90026-4 / Curr. Opin. Cell Biol. / The nucleolus by Scheer (1994)
10.1002/j.1460-2075.1987.tb02447.x / EMBO (Eur. Mol. Biol. Organ.) J. / A constitutive nucleolar protein identified as a member of the nucleoplasmin family by Schmidt-Zachmann (1987)
10.1111/j.1440-169X.1981.00579.x / Dev. Growth Differ. / Demonstration of rRNA synthesis in pre-gastrular embryos of Xenopus laevis by Shiokawa (1981)
10.1111/j.1440-169X.1981.00589.x / Dev. Growth Differ. / Non-coordinated synthesis of RNA's in pre-gastrular embryos of Xenopus laevis by Shiokawa (1981)
10.1016/S0092-8674(00)80247-0 / Cell. / Sno storm in the nucleolusnew roles for myriad small RNPs by Smith (1997)
10.1016/S0092-8674(00)80230-5 / Cell. / Pre-mRNA processing and the CTD of RNA polymerase IIthe tail that wags the dog? by Steinmetz (1997)
{'key': '2023072902063100100_ThiryandGoessens1996', 'volume-title': 'The nucleolus during the cell cycle', 'author': 'Thiry', 'year': '1996'} / The nucleolus during the cell cycle by Thiry (1996)
10.1006/excr.1996.0364 / Exp. Cell Res. / Trans-acting factors in ribosome synthesis by Tollervey (1996)
10.1083/jcb.122.4.753 / J. Cell Biol. / Nucleolus-like morphology produced during the in vitro reassociation of nucleolar components by Trimbur (1993)
10.1093/nar/27.12.2465 / Nucleic Acids Res. / hPop4a new protein subunit of the human RNase MRP and RNase P ribonucleoprotein complexes by Van Eenennaam (1999)
10.1083/jcb.142.5.1167 / J. Cell Biol. / Presence of pre-rRNAs before activation of polymerase I transcription in the building process of nucleoli during early development of Xenopus laevis by Verheggen (1998)
{'key': '2023072902063100100_Weisenbergeretal1993', 'first-page': '189', 'article-title': 'The DNA topoisomerase I inhibitor camptothecin blocks postmitotic reformation of nucleoli in mammalian cells', 'volume': '61', 'author': 'Weisenberger', 'year': '1993', 'journal-title': 'Eur. J. Cell Biol.'} / Eur. J. Cell Biol. / The DNA topoisomerase I inhibitor camptothecin blocks postmitotic reformation of nucleoli in mammalian cells by Weisenberger (1993)
10.1093/nar/23.23.4844 / Nucleic Acids Res. / Intronic U14 snoRNAs of Xenopus laevis are located in two different parent genes and can be processed from their introns during early oogenesis by Xia (1995)
10.1007/BF02510478 / Chromosoma. / Experimental induction of prenucleolar bodies (PNBs) in interphase cellsinterphase PNBs show similar characteristics as those typically observed at telophase of mitosis in untreated cells by Zatsepina (1997)

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, 10:07 p.m.)
Indexed	2 months, 2 weeks ago (June 20, 2025, 12:05 a.m.)
Issued	25 years, 4 months ago (April 17, 2000)
Published	25 years, 4 months ago (April 17, 2000)
Published Online	25 years, 4 months ago (April 17, 2000)
Published Print	25 years, 4 months ago (April 17, 2000)

Funders 0

None

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        6,
        20
      ]
    ],
    "date-time": "2025-06-20T04:05:27Z",
    "timestamp": 1750392327856
  },
  "reference-count": 77,
  "publisher": "Rockefeller University Press",
  "issue": "2",
  "content-domain": {
    "domain": [
      "rupress.org"
    ],
    "crossmark-restriction": true
  },
  "published-print": {
    "date-parts": [
      [
        2000,
        4,
        17
      ]
    ]
  },
  "abstract": "<jats:p>Transcription and splicing of messenger RNAs are temporally and spatially coordinated through the recruitment by RNA polymerase II of processing factors. We questioned whether RNA polymerase I plays a role in the recruitment of the ribosomal RNA (rRNA) processing machinery. During Xenopus laevis embryogenesis, recruitment of the rRNA processing machinery to the nucleolar domain occurs in two steps: two types of precursor structures called prenucleolar bodies (PNBs) form independently throughout the nucleoplasm; and components of PNBs I (fibrillarin, nucleolin, and the U3 and U8 small nucleolar RNAs) fuse to the nucleolar domain before components of PNBs II (B23/NO38). This fusion process is independent of RNA polymerase I activity, as shown by actinomycin D treatment of embryos and by the lack of detectable RNA polymerase I at ribosomal gene loci during fusion. Instead, this process is concomitant with the targeting of maternally derived pre-rRNAs to the nucleolar domain. Absence of fusion was correlated with absence of these pre-rRNAs in nuclei where RNA polymerase II and III are inhibited. Therefore, during X. laevis embryogenesis, the recruitment of the rRNA processing machinery to the nucleolar domain could be dependent on the presence of pre-rRNAs, but is independent of either zygotic RNA polymerase I transcription or the presence of RNA polymerase I itself.</jats:p>",
  "DOI": "10.1083/jcb.149.2.293",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2002,
        7,
        26
      ]
    ],
    "date-time": "2002-07-26T16:45:41Z",
    "timestamp": 1027701941000
  },
  "page": "293-306",
  "update-policy": "http://dx.doi.org/10.1083/jcb.crossmarkpolicy",
  "source": "Crossref",
  "is-referenced-by-count": 46,
  "title": "The Ribosomal RNA Processing Machinery Is Recruited to the Nucleolar Domain before RNA Polymerase I during <i>Xenopus laevis</i> Development",
  "prefix": "10.1083",
  "volume": "149",
  "author": [
    {
      "given": "C\u00e9line",
      "family": "Verheggen",
      "sequence": "first",
      "affiliation": [
        {
          "name": "aInstitut Jacques Monod, UMR 7592, 75251 Paris, France"
        },
        {
          "name": "bInstitut Curie, Section de Recherche, UMR 144, 75248 Paris, France"
        }
      ]
    },
    {
      "given": "Genevi\u00e8ve",
      "family": "Almouzni",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "bInstitut Curie, Section de Recherche, UMR 144, 75248 Paris, France"
        }
      ]
    },
    {
      "given": "Dani\u00e8le",
      "family": "Hernandez-Verdun",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "aInstitut Jacques Monod, UMR 7592, 75251 Paris, France"
        }
      ]
    }
  ],
  "member": "291",
  "published-online": {
    "date-parts": [
      [
        2000,
        4,
        17
      ]
    ]
  },
  "reference": [
    {
      "key": "2023072902063100100_Allmangetal1999",
      "doi-asserted-by": "crossref",
      "first-page": "2148",
      "DOI": "10.1101/gad.13.16.2148",
      "article-title": "The yeast exosome and human PM-Scl are related complexes of 3\u2032-5\u2032 exonucleases",
      "volume": "13",
      "author": "Allmang",
      "year": "1999",
      "journal-title": "Genes Dev."
    },
    {
      "key": "2023072902063100100_Almouzni1998"
    },
    {
      "key": "2023072902063100100_AlmouzniandWolffe1995",
      "doi-asserted-by": "crossref",
      "first-page": "1752",
      "DOI": "10.1002/j.1460-2075.1995.tb07164.x",
      "article-title": "Constraints on transcriptional activator function contribute to transcriptional quiescence during early Xenopus embryogenesis",
      "volume": "14",
      "author": "Almouzni",
      "year": "1995",
      "journal-title": "EMBO (Eur. Mol. Biol. Organ.) J."
    },
    {
      "key": "2023072902063100100_N0x28047b0N0x3530a00",
      "doi-asserted-by": "crossref",
      "first-page": "463",
      "DOI": "10.1242/jcs.107.2.463",
      "article-title": "Cell cycle redistribution of U3 snRNA and fibrillarin. Presence in the cytoplasmic nucleolus remnant and in the prenucleolar bodies at telophase",
      "volume": "107",
      "author": "Azum-G\u00e9lade",
      "year": "1994",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "2023072902063100100_BauerandGall1997",
      "doi-asserted-by": "crossref",
      "first-page": "73",
      "DOI": "10.1091/mbc.8.1.73",
      "article-title": "Coiled bodies without coilin",
      "volume": "8",
      "author": "Bauer",
      "year": "1997",
      "journal-title": "Mol. Biol. Cell"
    },
    {
      "key": "2023072902063100100_Baueretal1994",
      "doi-asserted-by": "crossref",
      "first-page": "633",
      "DOI": "10.1091/mbc.5.6.633",
      "article-title": "In vitro assembly of coiled bodies in Xenopus egg extract",
      "volume": "5",
      "author": "Bauer",
      "year": "1994",
      "journal-title": "Mol. Biol. Cell."
    },
    {
      "key": "2023072902063100100_BellandScheer1997",
      "doi-asserted-by": "crossref",
      "first-page": "43",
      "DOI": "10.1242/jcs.110.1.43",
      "article-title": "Prenucleolar bodies contain coilin and are assembled in Xenopus egg extract depleted of specific nucleolar proteins and U3 RNA",
      "volume": "110",
      "author": "Bell",
      "year": "1997",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "2023072902063100100_BellandScheer1999",
      "doi-asserted-by": "crossref",
      "first-page": "122",
      "DOI": "10.1006/excr.1999.4411",
      "article-title": "Developmental changes in RNA polymerase I and TATA box-binding protein during early Xenopus embryogenesis",
      "volume": "248",
      "author": "Bell",
      "year": "1999",
      "journal-title": "Exp. Cell Res."
    },
    {
      "key": "2023072902063100100_Belletal1992",
      "doi-asserted-by": "crossref",
      "first-page": "1297",
      "DOI": "10.1083/jcb.118.6.1297",
      "article-title": "In vitro assembly of prenucleolar bodies in Xenopus egg extract",
      "volume": "118",
      "author": "Bell",
      "year": "1992",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072902063100100_Belletal1997",
      "doi-asserted-by": "crossref",
      "first-page": "2053",
      "DOI": "10.1242/jcs.110.17.2053",
      "article-title": "Association of the nucleolar transcription factor UBF with the transcriptionally inactive rRNA genes of pronuclei and early Xenopus embryos",
      "volume": "110",
      "author": "Bell",
      "year": "1997",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "2023072902063100100_Benaventeetal1987",
      "doi-asserted-by": "crossref",
      "first-page": "1483",
      "DOI": "10.1083/jcb.105.4.1483",
      "article-title": "Inhibition of nucleolar reformation after microinjection of antibodies to RNA polymerase I into mitotic cells",
      "volume": "105",
      "author": "Benavente",
      "year": "1987",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072902063100100_Bentley1999",
      "doi-asserted-by": "crossref",
      "first-page": "347",
      "DOI": "10.1016/S0955-0674(99)80048-9",
      "article-title": "Coupling RNA polymerase II transcription with pre-mRNA processing",
      "volume": "11",
      "author": "Bentley",
      "year": "1999",
      "journal-title": "Curr. Opin. Cell Biol."
    },
    {
      "key": "2023072902063100100_Bevenetal1996",
      "doi-asserted-by": "crossref",
      "first-page": "1241",
      "DOI": "10.1242/jcs.109.6.1241",
      "article-title": "The organization of ribosomal RNA processing correlates with the distribution of nucleolar snRNAs",
      "volume": "109",
      "author": "Beven",
      "year": "1996",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "2023072902063100100_Boudoncketal1999",
      "doi-asserted-by": "crossref",
      "first-page": "2297",
      "DOI": "10.1091/mbc.10.7.2297",
      "article-title": "The movement of coiled bodies visualized in living plant cells by the green fluorescent protein",
      "volume": "10",
      "author": "Boudonck",
      "year": "1999",
      "journal-title": "Mol. Biol. Cell."
    },
    {
      "key": "2023072902063100100_Briggsetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "13255",
      "DOI": "10.1074/jbc.273.21.13255",
      "article-title": "Rrp6p, the yeast homologue of the human PM-Scl 100-kDa autoantigen, is essential for efficient 5.8 S rRNA 3\u2032 end formation",
      "volume": "273",
      "author": "Briggs",
      "year": "1998",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072902063100100_BrownandLittna1964",
      "doi-asserted-by": "crossref",
      "first-page": "669",
      "DOI": "10.1016/S0022-2836(64)80116-9",
      "article-title": "RNA synthesis during development of Xenopus laevis, the South African clawed toad",
      "volume": "8",
      "author": "Brown",
      "year": "1964",
      "journal-title": "J. Mol. Biol."
    },
    {
      "key": "2023072902063100100_CordenandPatturajan1997",
      "doi-asserted-by": "crossref",
      "first-page": "413",
      "DOI": "10.1016/S0968-0004(97)01125-0",
      "article-title": "A CTD function linking transcription to splicing",
      "volume": "22",
      "author": "Corden",
      "year": "1997",
      "journal-title": "Trends Biochem. Sci."
    },
    {
      "key": "2023072902063100100_DichtlandTollervey1997",
      "doi-asserted-by": "crossref",
      "first-page": "417",
      "DOI": "10.1093/emboj/16.2.417",
      "article-title": "Pop3p is essential for the activity of the RNase MRP and RNase P ribonucleoproteins in vivo",
      "volume": "16",
      "author": "Dichtl",
      "year": "1997",
      "journal-title": "EMBO (Eur. Mol. Biol. Organ.) J."
    },
    {
      "key": "2023072902063100100_Dundretal1997",
      "doi-asserted-by": "crossref",
      "first-page": "407",
      "DOI": "10.1007/BF02510477",
      "article-title": "A class of nonribosomal nucleolar components is located in chromosome periphery and in nucleolus-derived foci during anaphase and telophase",
      "volume": "105",
      "author": "Dundr",
      "year": "1997",
      "journal-title": "Chromosoma."
    },
    {
      "key": "2023072902063100100_Duvaletal1990",
      "first-page": "4123",
      "article-title": "Stability of maternal mRNA in Xenopus embryosrole of transcription and translation",
      "volume": "10",
      "author": "Duval",
      "year": "1990",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2023072902063100100_FomproixandHernandez-Verdun1999",
      "doi-asserted-by": "crossref",
      "first-page": "452",
      "DOI": "10.1006/excr.1999.4578",
      "article-title": "Effects of anti-PM-Scl 100 (Rr6p exonuclease) antibodies on prenucleolar body dynamics at the end of mitosis",
      "volume": "251",
      "author": "Fomproix",
      "year": "1999",
      "journal-title": "Exp. Cell Res."
    },
    {
      "key": "2023072902063100100_Fomproixetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "359",
      "DOI": "10.1242/jcs.111.3.359",
      "article-title": "Effects of anti-fibrillarin antibodies on building of functional nucleoli at the end of mitosis",
      "volume": "111",
      "author": "Fomproix",
      "year": "1998",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "2023072902063100100_Freyetal1999",
      "doi-asserted-by": "crossref",
      "first-page": "126",
      "DOI": "10.1016/S0960-9822(99)80066-9",
      "article-title": "Association of snRNA genes with the coiled bodies is mediated by nascent snRNA transcripts",
      "volume": "9",
      "author": "Frey",
      "year": "1999",
      "journal-title": "Curr. Biol."
    },
    {
      "key": "2023072902063100100_Galletal1999",
      "doi-asserted-by": "crossref",
      "first-page": "4385",
      "DOI": "10.1091/mbc.10.12.4385",
      "article-title": "Assembly of the nuclear transcription and processing machinerycajal bodies (coiled bodies) and transcriptosomes",
      "volume": "10",
      "author": "Gall",
      "year": "1999",
      "journal-title": "Mol. Biol. Cell."
    },
    {
      "key": "2023072902063100100_Gautieretal1994",
      "doi-asserted-by": "crossref",
      "first-page": "81",
      "DOI": "10.1016/S0248-4900(94)80010-3",
      "article-title": "Fate of specific nucleolar perichromosomal proteins during mitosiscellular distribution and association with U3 snoRNA",
      "volume": "82",
      "author": "Gautier",
      "year": "1994",
      "journal-title": "Biol. Cell."
    },
    {
      "key": "2023072902063100100_N0x28047b0N0x3531240",
      "doi-asserted-by": "crossref",
      "first-page": "502",
      "DOI": "10.1083/jcb.60.2.502",
      "article-title": "Experimental analysis of nucleolar reorganization",
      "volume": "60",
      "author": "Gim\u00e9nez-Martin",
      "year": "1974",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072902063100100_Ginistyetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "1476",
      "DOI": "10.1093/emboj/17.5.1476",
      "article-title": "Nucleolin functions in the first step of ribosomal RNA processing",
      "volume": "17",
      "author": "Ginisty",
      "year": "1998",
      "journal-title": "EMBO (Eur. Mol. Biol. Organ.) J."
    },
    {
      "key": "2023072902063100100_GurdonandWickens1983",
      "first-page": "101:370",
      "article-title": "Use of Xenopus oocytes for the expression of cloned genes",
      "volume-title": "Methods in Enzymology",
      "author": "Gurdon",
      "year": "1983"
    },
    {
      "key": "2023072902063100100_Hadjiolov1985"
    },
    {
      "key": "2023072902063100100_Highettetal1993",
      "doi-asserted-by": "crossref",
      "first-page": "843",
      "DOI": "10.1242/jcs.104.3.843",
      "article-title": "Different patterns of rDNA distribution in Pisum sativum nucleoli correlate with different levels of nucleolar activity",
      "volume": "104",
      "author": "Highett",
      "year": "1993",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "2023072902063100100_HuangandSpector1996a",
      "doi-asserted-by": "crossref",
      "first-page": "191",
      "DOI": "10.1002/(SICI)1097-4644(199608)62:2<191::AID-JCB7>3.0.CO;2-N",
      "article-title": "Dynamic organization of pre-mRNA splicing factors",
      "volume": "62",
      "author": "Huang",
      "year": "1996",
      "journal-title": "J. Cell Biochem."
    },
    {
      "key": "2023072902063100100_HuangandSpector1996b",
      "doi-asserted-by": "crossref",
      "first-page": "719",
      "DOI": "10.1083/jcb.133.4.719",
      "article-title": "Intron-dependent recruitment of pre-mRNA splicing factors to sites of transcription",
      "volume": "133",
      "author": "Huang",
      "year": "1996",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072902063100100_N0x28047b0N0x35314e0",
      "doi-asserted-by": "crossref",
      "first-page": "47",
      "DOI": "10.1016/0092-8674(93)90159-N",
      "article-title": "In vivo evidence that transcription and splicing are coordinated by a recruiting mechanism",
      "volume": "73",
      "author": "Jim\u00e9nez-Garcia",
      "year": "1993",
      "journal-title": "Cell."
    },
    {
      "key": "2023072902063100100_N0x28047b0N0x3531540",
      "doi-asserted-by": "crossref",
      "first-page": "239",
      "DOI": "10.1111/j.1768-322X.1989.tb00795.x",
      "article-title": "Nucleologenesisuse of non-isotopic in situ hybridization and immunocytochemistry to compare the localization of rDNA and nucleolar proteins during mitosis",
      "volume": "65",
      "author": "Jim\u00e9nez-Garcia",
      "year": "1989",
      "journal-title": "Biol. Cell."
    },
    {
      "key": "2023072902063100100_N0x28047b0N0x35315a0",
      "doi-asserted-by": "crossref",
      "first-page": "955",
      "DOI": "10.1091/mbc.5.9.955",
      "article-title": "NucleologenesisU3 snRNA-containing prenucleolar bodies move to sites of active pre-rRNA transcription after mitosis",
      "volume": "5",
      "author": "Jim\u00e9nez-Garcia",
      "year": "1994",
      "journal-title": "Mol. Biol. Cell."
    },
    {
      "key": "2023072902063100100_Jollyetal1999a",
      "doi-asserted-by": "crossref",
      "first-page": "6769",
      "DOI": "10.1073/pnas.96.12.6769",
      "article-title": "Rapid and reversible relocalization of heat shock factor 1 within seconds to nuclear stress granules",
      "volume": "96",
      "author": "Jolly",
      "year": "1999",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072902063100100_Jollyetal1999b",
      "doi-asserted-by": "crossref",
      "first-page": "1133",
      "DOI": "10.1083/jcb.145.6.1133",
      "article-title": "Intron-independent association of splicing factors with active genes",
      "volume": "145",
      "author": "Jolly",
      "year": "1999",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072902063100100_LamondandEarnshaw1998",
      "doi-asserted-by": "crossref",
      "first-page": "547",
      "DOI": "10.1126/science.280.5363.547",
      "article-title": "Structure and function in the nucleus",
      "volume": "280",
      "author": "Lamond",
      "year": "1998",
      "journal-title": "Science."
    },
    {
      "key": "2023072902063100100_Lygerouetal1996a",
      "doi-asserted-by": "crossref",
      "first-page": "268",
      "DOI": "10.1126/science.272.5259.268",
      "article-title": "Accurate processing of a eukaryotic pre-rRNA by RNase MRP in vitro",
      "volume": "272",
      "author": "Lygerou",
      "year": "1996",
      "journal-title": "Science."
    },
    {
      "key": "2023072902063100100_Lygerouetal1996b",
      "doi-asserted-by": "crossref",
      "first-page": "5936",
      "DOI": "10.1002/j.1460-2075.1996.tb00980.x",
      "article-title": "hPop1an autoantigenic protein subunit shared by the human RNase P and RNase MRP ribonucleoproteins",
      "volume": "15",
      "author": "Lygerou",
      "year": "1996",
      "journal-title": "EMBO (Eur. Mol. Biol. Organ.) J."
    },
    {
      "key": "2023072902063100100_Massonetal1996",
      "doi-asserted-by": "crossref",
      "first-page": "114",
      "DOI": "10.1006/excr.1996.0209",
      "article-title": "Conditions favoring RNA polymerase I transcription in permeabilized cells",
      "volume": "226",
      "author": "Masson",
      "year": "1996",
      "journal-title": "Exp. Cell Res."
    },
    {
      "key": "2023072902063100100_McCrackenetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "357",
      "DOI": "10.1038/385357a0",
      "article-title": "The C-terminal domain of RNA polymerase II couples mRNA processing to transcription",
      "volume": "385",
      "author": "McCracken",
      "year": "1997",
      "journal-title": "Nature."
    },
    {
      "key": "2023072902063100100_MebmerandDreyer1993",
      "first-page": "369",
      "article-title": "Requirement for nuclear translocation and nucleolar accumulation of nucleolin of Xenopus laevis",
      "volume": "61",
      "author": "Mebmer",
      "year": "1993",
      "journal-title": "Eur. J. Cell. Biol."
    },
    {
      "key": "2023072902063100100_Michotetal1999",
      "doi-asserted-by": "crossref",
      "first-page": "2271",
      "DOI": "10.1093/nar/27.11.2271",
      "article-title": "Evolutionarily conserved structural features in the ITS2 of mammalian pre-rRNAs and potential interactions with the snoRNA U8 detected by comparative analysis of new mouse sequences",
      "volume": "27",
      "author": "Michot",
      "year": "1999",
      "journal-title": "Nucleic Acids Res."
    },
    {
      "key": "2023072902063100100_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": "2023072902063100100_MisteliandSpector1999",
      "doi-asserted-by": "crossref",
      "first-page": "697",
      "DOI": "10.1016/S1097-2765(01)80002-2",
      "article-title": "RNA polymerase II targets pre-mRNA splicing factors to transcription sites in vivo",
      "volume": "3",
      "author": "Misteli",
      "year": "1999",
      "journal-title": "Mol. Cell."
    },
    {
      "key": "2023072902063100100_Mistelietal1997",
      "doi-asserted-by": "crossref",
      "first-page": "523",
      "DOI": "10.1038/387523a0",
      "article-title": "The dynamics of a pre-mRNA splicing factor in living cells",
      "volume": "387",
      "author": "Misteli",
      "year": "1997",
      "journal-title": "Nature."
    },
    {
      "key": "2023072902063100100_Mitchelletal1997",
      "doi-asserted-by": "crossref",
      "first-page": "457",
      "DOI": "10.1016/S0092-8674(00)80432-8",
      "article-title": "The exosomea conserved eukaryotic RNA processing complex containing multiple 3\u2032-5\u2032 exoribonucleases",
      "volume": "91",
      "author": "Mitchell",
      "year": "1997",
      "journal-title": "Cell."
    },
    {
      "key": "2023072902063100100_Moenetal1995",
      "doi-asserted-by": "crossref",
      "first-page": "1779",
      "DOI": "10.1093/hmg/4.suppl_1.1779",
      "article-title": "Compartmentalization of specific pre-mRNA metabolisman emerging view",
      "volume": "4",
      "author": "Moen",
      "year": "1995",
      "journal-title": "Hum. Mol. Genet."
    },
    {
      "key": "2023072902063100100_Morcilloetal1976",
      "doi-asserted-by": "crossref",
      "first-page": "311",
      "DOI": "10.1016/0014-4827(76)90046-X",
      "article-title": "Nucleolar transcription during plant mitosis",
      "volume": "102",
      "author": "Morcillo",
      "year": "1976",
      "journal-title": "Exp. Cell Res."
    },
    {
      "key": "2023072902063100100_NewportandKirschner1982",
      "doi-asserted-by": "crossref",
      "first-page": "675",
      "DOI": "10.1016/0092-8674(82)90272-0",
      "article-title": "A major developmental transition in early Xenopus embryos. I. Characterization and timing of cellular changes at the midblastula stage",
      "volume": "30",
      "author": "Newport",
      "year": "1982",
      "journal-title": "Cell."
    },
    {
      "key": "2023072902063100100_NieuwkoopandFaber1994",
      "volume-title": "Normal table of Xenopus laevis (Daudin)",
      "author": "Nieuwkoop",
      "year": "1994"
    },
    {
      "key": "2023072902063100100_Oakesetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "23",
      "DOI": "10.1083/jcb.143.1.23",
      "article-title": "Mutational analysis of the structure and localization of the nucleolus in the yeast Saccharomyces cerevisiae",
      "volume": "143",
      "author": "Oakes",
      "year": "1998",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072902063100100_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": "2023072902063100100_Ochsetal1985a",
      "doi-asserted-by": "crossref",
      "first-page": "330",
      "DOI": "10.1007/BF00327463",
      "article-title": "Nucleologenesiscomposition and fate of prenucleolar bodies",
      "volume": "92",
      "author": "Ochs",
      "year": "1985",
      "journal-title": "Chromosoma."
    },
    {
      "key": "2023072902063100100_Ochsetal1985b",
      "doi-asserted-by": "crossref",
      "first-page": "123",
      "DOI": "10.1111/j.1768-322X.1985.tb00387.x",
      "article-title": "Fibrillarina new protein of the nucleolus identified by autoimmune sera",
      "volume": "54",
      "author": "Ochs",
      "year": "1985",
      "journal-title": "Biol. Cell."
    },
    {
      "key": "2023072902063100100_PeculisandSteitz1993",
      "doi-asserted-by": "crossref",
      "first-page": "1233",
      "DOI": "10.1016/0092-8674(93)90651-6",
      "article-title": "Disruption of U8 nucleolar snRNA inhibits 5.8S and 28S rRNA processing in the Xenopus oocyte",
      "volume": "73",
      "author": "Peculis",
      "year": "1993",
      "journal-title": "Cell."
    },
    {
      "key": "2023072902063100100_Pluketal1999",
      "doi-asserted-by": "crossref",
      "first-page": "512",
      "DOI": "10.1017/S1355838299982079",
      "article-title": "RNA\u2013protein interactions in the human RNase MRP ribonucleoprotein complex",
      "volume": "5",
      "author": "Pluk",
      "year": "1999",
      "journal-title": "RNA."
    },
    {
      "key": "2023072902063100100_SanfordandBruzik1999",
      "doi-asserted-by": "crossref",
      "first-page": "1513",
      "DOI": "10.1101/gad.13.12.1513",
      "article-title": "Developmental regulation of SR protein phosphorylation and activity",
      "volume": "13",
      "author": "Sanford",
      "year": "1999",
      "journal-title": "Genes Dev."
    },
    {
      "key": "2023072902063100100_Savinoetal1999",
      "doi-asserted-by": "crossref",
      "first-page": "1889",
      "DOI": "10.1242/jcs.112.12.1889",
      "article-title": "The nucleolar antigen Nop 52, the human homologue of the yeast ribosomal RNA processing RRP1, is recruited at late stages of nucleologenesis",
      "volume": "112",
      "author": "Savino",
      "year": "1999",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "2023072902063100100_SavkurandOlson1998",
      "doi-asserted-by": "crossref",
      "first-page": "4508",
      "DOI": "10.1093/nar/26.19.4508",
      "article-title": "Preferential cleavage in pre-ribosomal RNA by protein B23 endoribonuclease",
      "volume": "26",
      "author": "Savkur",
      "year": "1998",
      "journal-title": "Nucleic Acids Res."
    },
    {
      "key": "2023072902063100100_ScheerandBenavente1990",
      "doi-asserted-by": "crossref",
      "first-page": "14",
      "DOI": "10.1002/bies.950120104",
      "article-title": "Functional and dynamic aspects of the mammalian nucleolus",
      "volume": "12",
      "author": "Scheer",
      "year": "1990",
      "journal-title": "BioEssay."
    },
    {
      "key": "2023072902063100100_Scheeretal1993",
      "doi-asserted-by": "crossref",
      "first-page": "236",
      "DOI": "10.1016/0962-8924(93)90123-I",
      "article-title": "Structure, function and assembly of the nucleolus",
      "volume": "3",
      "author": "Scheer",
      "year": "1993",
      "journal-title": "Trends Cell Biol."
    },
    {
      "key": "2023072902063100100_ScheerandWeisenberger1994",
      "doi-asserted-by": "crossref",
      "first-page": "354",
      "DOI": "10.1016/0955-0674(94)90026-4",
      "article-title": "The nucleolus",
      "volume": "6",
      "author": "Scheer",
      "year": "1994",
      "journal-title": "Curr. Opin. Cell Biol."
    },
    {
      "key": "2023072902063100100_Schmidt-Zachmannetal1987",
      "doi-asserted-by": "crossref",
      "first-page": "1881",
      "DOI": "10.1002/j.1460-2075.1987.tb02447.x",
      "article-title": "A constitutive nucleolar protein identified as a member of the nucleoplasmin family",
      "volume": "6",
      "author": "Schmidt-Zachmann",
      "year": "1987",
      "journal-title": "EMBO (Eur. Mol. Biol. Organ.) J."
    },
    {
      "key": "2023072902063100100_Shiokawaetal1981a",
      "doi-asserted-by": "crossref",
      "first-page": "579",
      "DOI": "10.1111/j.1440-169X.1981.00579.x",
      "article-title": "Demonstration of rRNA synthesis in pre-gastrular embryos of Xenopus laevis",
      "volume": "23",
      "author": "Shiokawa",
      "year": "1981",
      "journal-title": "Dev. Growth Differ."
    },
    {
      "key": "2023072902063100100_Shiokawaetal1981b",
      "doi-asserted-by": "crossref",
      "first-page": "589",
      "DOI": "10.1111/j.1440-169X.1981.00589.x",
      "article-title": "Non-coordinated synthesis of RNA's in pre-gastrular embryos of Xenopus laevis",
      "volume": "23",
      "author": "Shiokawa",
      "year": "1981",
      "journal-title": "Dev. Growth Differ."
    },
    {
      "key": "2023072902063100100_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."
    },
    {
      "key": "2023072902063100100_Steinmetz1997",
      "doi-asserted-by": "crossref",
      "first-page": "491",
      "DOI": "10.1016/S0092-8674(00)80230-5",
      "article-title": "Pre-mRNA processing and the CTD of RNA polymerase IIthe tail that wags the dog?",
      "volume": "89",
      "author": "Steinmetz",
      "year": "1997",
      "journal-title": "Cell."
    },
    {
      "key": "2023072902063100100_ThiryandGoessens1996",
      "volume-title": "The nucleolus during the cell cycle",
      "author": "Thiry",
      "year": "1996"
    },
    {
      "key": "2023072902063100100_Tollervey1996",
      "doi-asserted-by": "crossref",
      "first-page": "226",
      "DOI": "10.1006/excr.1996.0364",
      "article-title": "Trans-acting factors in ribosome synthesis",
      "volume": "229",
      "author": "Tollervey",
      "year": "1996",
      "journal-title": "Exp. Cell Res."
    },
    {
      "key": "2023072902063100100_TrimburandWalsh1993",
      "doi-asserted-by": "crossref",
      "first-page": "753",
      "DOI": "10.1083/jcb.122.4.753",
      "article-title": "Nucleolus-like morphology produced during the in vitro reassociation of nucleolar components",
      "volume": "122",
      "author": "Trimbur",
      "year": "1993",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072902063100100_VanEenennaametal1999",
      "doi-asserted-by": "crossref",
      "first-page": "2465",
      "DOI": "10.1093/nar/27.12.2465",
      "article-title": "hPop4a new protein subunit of the human RNase MRP and RNase P ribonucleoprotein complexes",
      "volume": "27",
      "author": "Van Eenennaam",
      "year": "1999",
      "journal-title": "Nucleic Acids Res."
    },
    {
      "key": "2023072902063100100_Verheggenetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "1167",
      "DOI": "10.1083/jcb.142.5.1167",
      "article-title": "Presence of pre-rRNAs before activation of polymerase I transcription in the building process of nucleoli during early development of Xenopus laevis",
      "volume": "142",
      "author": "Verheggen",
      "year": "1998",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072902063100100_Weisenbergeretal1993",
      "first-page": "189",
      "article-title": "The DNA topoisomerase I inhibitor camptothecin blocks postmitotic reformation of nucleoli in mammalian cells",
      "volume": "61",
      "author": "Weisenberger",
      "year": "1993",
      "journal-title": "Eur. J. Cell Biol."
    },
    {
      "key": "2023072902063100100_Xiaetal1995",
      "doi-asserted-by": "crossref",
      "first-page": "4844",
      "DOI": "10.1093/nar/23.23.4844",
      "article-title": "Intronic U14 snoRNAs of Xenopus laevis are located in two different parent genes and can be processed from their introns during early oogenesis",
      "volume": "23",
      "author": "Xia",
      "year": "1995",
      "journal-title": "Nucleic Acids Res."
    },
    {
      "key": "2023072902063100100_Zatsepinaetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "418",
      "DOI": "10.1007/BF02510478",
      "article-title": "Experimental induction of prenucleolar bodies (PNBs) in interphase cellsinterphase PNBs show similar characteristics as those typically observed at telophase of mitosis in untreated cells",
      "volume": "105",
      "author": "Zatsepina",
      "year": "1997",
      "journal-title": "Chromosoma."
    }
  ],
  "container-title": "The Journal of Cell Biology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://rupress.org/jcb/article-pdf/149/2/293/1857651/9909078.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "syndication"
    },
    {
      "URL": "https://rupress.org/jcb/article-pdf/149/2/293/1857651/9909078.pdf",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        7,
        29
      ]
    ],
    "date-time": "2023-07-29T02:07:41Z",
    "timestamp": 1690596461000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://rupress.org/jcb/article/149/2/293/32090/The-Ribosomal-RNA-Processing-Machinery-Is"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2000,
        4,
        17
      ]
    ]
  },
  "references-count": 77,
  "journal-issue": {
    "issue": "2",
    "published-print": {
      "date-parts": [
        [
          2000,
          4,
          17
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1083/jcb.149.2.293",
  "relation": {},
  "ISSN": [
    "0021-9525",
    "1540-8140"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        2000,
        4,
        17
      ]
    ]
  }
}