Skip to main content
Log in

The Cajal body: a meeting place for spliceosomal snRNPs in the nuclear maze

  • Review
  • Published:
Chromosoma Aims and scope Submit manuscript

Abstract

Spliceosomal small nuclear ribonucleoprotein particles (snRNPs) are essential pre-mRNA splicing factors that consist of small nuclear RNAs (snRNAs) complexed with specific sets of proteins. A considerable body of evidence has established that snRNP assembly is accomplished after snRNA synthesis in the nucleus through a series of steps involving cytoplasmic and nuclear phases. Recent work indicates that snRNPs transiently localize to the Cajal body (CB), a nonmembrane-bound inclusion present in the nuclei of most cells, for the final steps in snRNP maturation, including snRNA base modification, U4/U6 snRNA annealing, and snRNA-protein assembly. Here, we review these findings that suggest a crucial role for CBs in the spliceosome cycle in which production of new snRNPs—and perhaps regenerated snRNPs after splicing—is promoted by the concentration of substrates in this previously mysterious subnuclear organelle. These insights allow us to speculate on the role of nuclear bodies in regulating the dynamics of RNP assembly to maintain a functional pool of factors available for key steps in gene expression.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abbott J, Marzluff WF, Gall JG (1999) The stem-loop binding protein (SLBP1) is present in coiled bodies of the Xenopus germinal vesicle. Mol Biol Cell 10:487–499

    PubMed  CAS  Google Scholar 

  • Achsel T, Brahms H, Kastner B, Bachi A, Wilm M, Luhrmann R (1999) A doughnut-shaped heteromer of human Sm-like proteins binds to the 3′- end of U6 snRNA, thereby facilitating U4/U6 duplex formation in vitro. EMBO J 18:5789–5802

    Article  PubMed  CAS  Google Scholar 

  • Adamson TE, Price DH (2003) Cotranscriptional processing of Drosophila histone mRNAs. Mol Cell Biol 23:4046–4055

    Article  PubMed  CAS  Google Scholar 

  • Andrade LE, Chan EK, Raska I, Peebles CL, Roos G, Tan EM (1991) Human autoantibody to a novel protein of the nuclear coiled body: immunological characterization and cDNA cloning of p80-coilin. J Exp Med 173:1407–1419

    Article  PubMed  CAS  Google Scholar 

  • Andrade LE, Tan EM, Chan EK (1993) Immunocytochemical analysis of the coiled body in the cell cycle and during cell proliferation. Proc Natl Acad Sci USA 90:1947–1951

    PubMed  CAS  Google Scholar 

  • Azzouz TN, Pillai RS, Dapp C, Chari A, Meister G, Kambach C, Fischer U, Schumperli D (2005) Toward an assembly line for U7 snRNPs: interactions of U7-specific Lsm proteins with PRMT5 and SMN complexes. J Biol Chem 280:34435–34440

    Article  PubMed  CAS  Google Scholar 

  • Baillat D, Hakimi MA, Naar AM, Shilatifard A, Cooch N, Shiekhattar R (2005) Integrator, a multiprotein mediator of small nuclear RNA processing, associates with the C-terminal repeat of RNA polymerase II. Cell 123:265–276

    Article  PubMed  CAS  Google Scholar 

  • Bauer DW, Gall JG (1997) Coiled bodies without coilin. Mol Biol Cell 8:73–82

    PubMed  CAS  Google Scholar 

  • Behrens SE, Luhrmann R (1991) Immunoaffinity purification of a [U4/U6.U5] tri-snRNP from human cells. Genes Dev 5:1439–1452

    PubMed  CAS  Google Scholar 

  • Bell M, Schreiner S, Damianov A, Reddy R, Bindereif A (2002) p110, a novel human U6 snRNP protein and U4/U6 snRNP recycling factor. EMBO J 21:2724–2735

    Article  PubMed  CAS  Google Scholar 

  • Bohmann K, Ferreira JA, Lamond AI (1995) Mutational analysis of p80 coilin indicates a functional interaction between coiled bodies and the nucleolus. J Cell Biol 131:817–831

    Article  PubMed  CAS  Google Scholar 

  • Boudonck K, Dolan L, Shaw PJ (1998) Coiled body numbers in the Arabidopsis root epidermis are regulated by cell type, developmental stage and cell cycle parameters. J Cell Sci 111:3687–3694

    PubMed  CAS  Google Scholar 

  • Boudonck K, Dolan L, Shaw PJ (1999) The movement of coiled bodies visualized in living plant cells by the green fluorescent protein. Mol Biol Cell 10:2297–2307

    PubMed  CAS  Google Scholar 

  • Boulon S, Verheggen C, Jady BE, Girard C, Pescia C, Paul C, Ospina JK, Kiss T, Matera AG, Bordonne R, Bertrand E (2004) PHAX and CRM1 are required sequentially to transport U3 snoRNA to nucleoli. Mol Cell 16:777–787

    Article  PubMed  CAS  Google Scholar 

  • Brosi R, Groning K, Behrens SE, Luhrmann R, Kramer A (1993) Interaction of mammalian splicing factor SF3a with U2 snRNP and relation of its 60-kD subunit to yeast PRP9. Science 262:102–105

    PubMed  CAS  Google Scholar 

  • Cajal RY (1903) Un sencillo metodo de coloracion seletiva del reticulo protoplasmatico y sus efectos en los diversos organos nerviosos de vertebrados e invertebrados. Trab Lab Investig Biol Univ Madr 2:129–221

    Google Scholar 

  • Callan HG, Gall JG, Murphy C (1991) Histone genes are located at the sphere loci of Xenopus lampbrush chromosomes. Chromosoma 101:245–251

    Article  PubMed  CAS  Google Scholar 

  • Carissimi C, Baccon J, Straccia M, Chiarella P, Maiolica A, Sawyer A, Rappsilber J, Pellizzoni L (2005) Unrip is a component of SMN complexes active in snRNP assembly. FEBS Lett 579:2348–2354

    Article  PubMed  CAS  Google Scholar 

  • Carmo-Fonseca M (2002) New clues to the function of the Cajal body. EMBO Rep 3:726–727

    Article  PubMed  CAS  Google Scholar 

  • Carmo-Fonseca M, Pepperkok R, Carvalho MT, Lamond AI (1992) Transcription-dependent colocalization of the U1, U2, U4/U6, and U5 snRNPs in coiled bodies. J Cell Biol 117:1–14

    Article  PubMed  CAS  Google Scholar 

  • Carmo-Fonseca M, Ferreira J, Lamond AI (1993) Assembly of snRNP-containing coiled bodies is regulated in interphase and mitosis—evidence that the coiled body is a kinetic nuclear structure. J Cell Biol 120:841–852

    Article  PubMed  CAS  Google Scholar 

  • Carmo-Fonseca M, Platani M, Swedlow JR (2002) Macromolecular mobility inside the cell nucleus. Trends Cell Biol 12:491–495

    Article  PubMed  CAS  Google Scholar 

  • Carvalho T, Almeida F, Calapez A, Lafarga M, Berciano MT, Carmo-Fonseca M (1999) The spinal muscular atrophy disease gene product, SMN: a link between snRNP biogenesis and the Cajal (coiled) body. J Cell Biol 147:715–728

    Article  PubMed  CAS  Google Scholar 

  • Chan SP, Kao DI, Tsai WY, Cheng SC (2003) The Prp19p-associated complex in spliceosome activation. Science 302:279–282

    Article  PubMed  CAS  Google Scholar 

  • Cioce M, Lamond AI (2005) Cajal bodies: a long history of discovery. Annu Rev Cell Dev Biol 21:105-131

    Article  PubMed  CAS  Google Scholar 

  • Damianov A, Schreiner S, Bindereif A (2004) Recycling of the U12-type spliceosome requires p110, a component of the U6atac snRNP. Mol Cell Biol 24:1700–1708

    Article  PubMed  CAS  Google Scholar 

  • Darzacq X, Jady BE, Verheggen C, Kiss AM, Bertrand E, Kiss T (2002) Cajal body-specific small nuclear RNAs: a novel class of 2′-O- methylation and pseudouridylation guide RNAs. EMBO J 21:2746–2756

    Article  PubMed  CAS  Google Scholar 

  • Deryusheva S, Gall JG (2004) Dynamics of coilin in Cajal bodies of the Xenopus germinal vesicle. Proc Natl Acad Sci USA 101:4810–4814

    Article  PubMed  CAS  Google Scholar 

  • Dominski Z, Yang XC, Marzluff WF (2005) The polyadenylation factor CPSF-73 is involved in histone-pre-mRNA processing. Cell 123:37–48

    Article  PubMed  CAS  Google Scholar 

  • Dundr M, Hebert MD, Karpova TS, Stanek D, Xu H, Shpargel KB, Meier UT, Neugebauer KM, Matera AG, Misteli T (2004) In vivo kinetics of Cajal body components. J Cell Biol 164:831–842

    Article  PubMed  CAS  Google Scholar 

  • Feeney RJ, Zieve GW (1990) Nuclear exchange of the U1 and U2 snRNP-specific proteins. J Cell Biol 110:871–881

    Article  PubMed  CAS  Google Scholar 

  • Fernandez R, Pena E, Navascues J, Casafont I, Lafarga M, Berciano MT (2002) cAMP-dependent reorganization of the Cajal bodies and splicing machinery in cultured Schwann cells. Glia 40:378–388

    Article  PubMed  Google Scholar 

  • Ferreira J, Carmo-Fonseca M (1995) The biogenesis of the coiled body during early mouse development. Development 121:601–612

    PubMed  CAS  Google Scholar 

  • Frey MR, Matera AG (1995) Coiled bodies contain U7 small nuclear RNA and associate with specific DNA sequences in interphase human cells. Proc Natl Acad Sci USA 92:5915–5919

    PubMed  CAS  Google Scholar 

  • Frey MR, Matera AG (2001) RNA-mediated interaction of Cajal bodies and U2 snRNA genes. J Cell Biol 154:499–509

    Article  PubMed  CAS  Google Scholar 

  • Frey MR, Bailey AD, Weiner AM, Matera AG (1999) Association of snRNA genes with coiled bodies is mediated by nascent snRNA transcripts. Curr Biol 9:126–135

    Article  PubMed  CAS  Google Scholar 

  • Friesen WJ, Massenet S, Paushkin S, Wyce A, Dreyfuss G (2001) SMN, the product of the spinal muscular atrophy gene, binds preferentially to dimethylarginine-containing protein targets. Mol Cell 7:1111–1117

    Article  PubMed  CAS  Google Scholar 

  • Gall JG (2000) Cajal bodies: the first 100 years. Annu Rev Cell Dev Biol 16:273–300

    Article  PubMed  CAS  Google Scholar 

  • Gangwani L, Flavell RA, Davis RJ (2005) ZPR1 is essential for survival and is required for localization of the survival motor neurons (SMN) protein to Cajal bodies. Mol Cell Biol 25:2744–2756

    Article  PubMed  CAS  Google Scholar 

  • Ganot P, Jady BE, Bortolin ML, Darzacq X, Kiss T (1999) Nucleolar factors direct the 2′-O-ribose methylation and pseudouridylation of U6 spliceosomal RNA. Mol Cell Biol 19:6906–6917

    PubMed  CAS  Google Scholar 

  • Gao L, Frey MR, Matera AG (1997) Human genes encoding U3 snRNA associate with coiled bodies in interphase cells and are clustered on chromosome 17p11.2 in a complex inverted repeat structure. Nucleic Acids Res 25:4740–4747

    Article  PubMed  CAS  Google Scholar 

  • Gerbi SA, Borovjagin AV, Lange TS (2003) The nucleolus: a site of ribonucleoprotein maturation. Curr Opin Cell Biol 15:318–325

    Article  PubMed  CAS  Google Scholar 

  • Grimmler M, Otter S, Peter C, Muller F, Chari A, Fischer U (2005) Unrip, a factor implicated in cap-independent translation, associates with the cytosolic SMN complex and influences its intracellular localization. Hum Mol Genet 14:3099–3111

    Article  PubMed  CAS  Google Scholar 

  • Handwerger KE, Murphy C, Gall JG (2003) Steady-state dynamics of Cajal body components in the Xenopus germinal vesicle. J Cell Biol 160:495–504

    Article  PubMed  CAS  Google Scholar 

  • Hebert MD, Matera AG (2000) Self-association of coilin reveals a common theme in nuclear body localization. Mol Biol Cell 11:4159–4171

    PubMed  CAS  Google Scholar 

  • Hebert MD, Szymczyk PW, Shpargel KB, Matera AG (2001) Coilin forms the bridge between Cajal bodies and SMN, the spinal muscular atrophy protein. Genes Dev 15:2720–2729

    Article  PubMed  CAS  Google Scholar 

  • Hebert MD, Shpargel KB, Ospina JK, Tucker KE, Matera AG (2002) Coilin methylation regulates nuclear body formation. Dev Cell 3:329–337

    Article  PubMed  CAS  Google Scholar 

  • Hoet RM, Raats JM, de Wildt R, Dumortier H, Muller S, van den Hoogen F, van Venrooij WJ (1998) Human monoclonal autoantibody fragments from combinatorial antibody libraries directed to the U1snRNP associated U1C protein; epitope mapping, immunolocalization and V-gene usage. Mol Immunol 35:1045–1055

    Article  PubMed  CAS  Google Scholar 

  • Horowitz DS, Kobayashi R, Krainer AR (1997) A new cyclophilin and the human homologues of yeast Prp3 and Prp4 form a complex associated with U4/U6 snRNPs. RNA 3:1374–1387

    PubMed  CAS  Google Scholar 

  • Jacobs EY, Frey MR, Wu W, Ingledue TC, Gebuhr TC, Gao L, Marzluff WF, Matera AG (1999) Coiled bodies preferentially associate with U4, U11, and U12 small nuclear RNA genes in interphase HeLa cells but not with U6 and U7 genes. Mol Biol Cell 10:1653–1663

    PubMed  CAS  Google Scholar 

  • Jacobs EY, Ogiwara I, Weiner AM (2004) Role of the C-terminal domain of RNA polymerase II in U2 snRNA transcription and 3′ processing. Mol Cell Biol 24:846–855

    Article  PubMed  CAS  Google Scholar 

  • Jady BE, Darzacq X, Tucker KE, Matera AG, Bertrand E, Kiss T (2003) Modification of Sm small nuclear RNAs occurs in the nucleoplasmic Cajal body following import from the cytoplasm. EMBO J 22:1878–1888

    Article  PubMed  CAS  Google Scholar 

  • Jady BE, Richard P, Bertrand E, Kiss T (2005) Cell cycle-dependent recruitment of telomerase RNA and Cajal bodies to human telomeres. Mol Biol Cell 17:944–954

    Article  PubMed  CAS  Google Scholar 

  • Jantsch MF, Gall JG (1992) Assembly and localization of the U1-specific snRNP C protein in the amphibian oocyte. J Cell Biol 119:1037–1046

    Article  PubMed  CAS  Google Scholar 

  • Jurica MS, Moore MJ (2003) Pre-mRNA splicing: awash in a sea of proteins. Mol Cell 12:5–14

    Article  PubMed  CAS  Google Scholar 

  • Jurica MS, Licklider LJ, Gygi SR, Grigorieff N, Moore MJ (2002) Purification and characterization of native spliceosomes suitable for three-dimensional structural analysis. RNA 8:426–439

    Article  PubMed  CAS  Google Scholar 

  • Kambach C, Mattaj IW (1992) Intracellular distribution of the U1A protein depends on active transport and nuclear binding to U1 snRNA. J Cell Biol 118:11–21

    Article  PubMed  CAS  Google Scholar 

  • Kambach C, Mattaj IW (1994) Nuclear transport of the U2 snRNP-specific U2B″ protein is mediated by both direct and indirect signalling mechanisms. J Cell Sci 107(Pt 7):1807–1816

    PubMed  CAS  Google Scholar 

  • Kiss T (2004) Biogenesis of small nuclear RNPs. J Cell Sci 117:5949–5951

    Article  PubMed  CAS  Google Scholar 

  • Kiss AM, Jady BE, Darzacq X, Verheggen C, Bertrand E, Kiss T (2002) A Cajal body-specific pseudouridylation guide RNA is composed of two box H/ACA snoRNA-like domains. Nucleic Acids Res 30:4643–4649

    Article  PubMed  CAS  Google Scholar 

  • Kolev NG, Steitz JA (2005) Symplekin and multiple other polyadenylation factors participate in 3′-end maturation of histone mRNAs. Genes Dev 19:2583–2592

    Article  PubMed  CAS  Google Scholar 

  • Kramer A, Gruter P, Groning K, Kastner B (1999) Combined biochemical and electron microscopic analyses reveal the architecture of the mammalian U2 snRNP. J Cell Biol 145:1355–1368

    Article  PubMed  CAS  Google Scholar 

  • Laggerbauer B, Liu S, Makarov E, Vornlocher HP, Makarova O, Ingelfinger D, Achsel T, Luhrmann R (2005) The human U5 snRNP 52K protein (CD2BP2) interacts with U5-102K (hPrp6), a U4/U6.U5 tri-snRNP bridging protein, but dissociates upon tri-snRNP formation. RNA 11:598–608

    Article  PubMed  CAS  Google Scholar 

  • Lange TS, Gerbi SA (2000) Transient nucleolar localization Of U6 small nuclear RNA in Xenopus laevis oocytes. Mol Biol Cell 11:2419–2428

    PubMed  CAS  Google Scholar 

  • Lewis JD, Tollervey D (2000) Like attracts like: getting RNA processing together in the nucleus. Science 288:1385–1389

    Article  PubMed  CAS  Google Scholar 

  • Liu JL, Murphy C, Buszczak M, Clatterbuck S, Goodman R, Gall JG (2006) The Drosophila Cajal body. J Cell Biol Vol 172 (in press)

  • Makarov EM, Makarova OV, Urlaub H, Gentzel M, Will CL, Wilm M, Luhrmann R (2002) Small nuclear ribonucleoprotein remodeling during catalytic activation of the spliceosome. Science 298:2205–2208

    Article  PubMed  CAS  Google Scholar 

  • Makarova OV, Makarov EM, Liu S, Vornlocher HP, Luhrmann R (2002) Protein 61K, encoded by a gene (PRPF31) linked to autosomal dominant retinitis pigmentosa, is required for U4/U6 center dotU5 tri-snRNP formation and pre-mRNA splicing. EMBO J 21:1148–1157

    Article  PubMed  CAS  Google Scholar 

  • Makarova OV, Makarov EM, Urlaub H, Will CL, Gentzel M, Wilm M, Luhrmann R (2004) A subset of human 35S U5 proteins, including Prp19, function prior to catalytic step 1 of splicing. EMBO J 23:2381–2391

    Article  PubMed  CAS  Google Scholar 

  • Massenet S, Pellizzoni L, Paushkin S, Mattaj IW, Dreyfuss G (2002) The SMN complex is associated with snRNPs throughout their cytoplasmic assembly pathway. Mol Cell Biol 22:6533–6541

    Article  PubMed  CAS  Google Scholar 

  • Matera AG (1998) Of coiled bodies, gems, and salmon. J Cell Biochem 70:181–192

    Article  PubMed  CAS  Google Scholar 

  • Matera AG (1999) Nuclear bodies: multifaceted subdomains of the interchromatin space. Trends Cell Biol 9:302–309

    Article  PubMed  CAS  Google Scholar 

  • Matera AG, Ward DC (1993) Nucleoplasmic organization of small nuclear ribonucleoproteins in cultured human cells. J Cell Biol 121:715–727

    Article  PubMed  CAS  Google Scholar 

  • Medenbach, Schreiner S, Liu S, Luhrmann R, Bindereif A (2004) Human U4/U6 snRNP recycling factor p110: mutational analysis reveals function of TPR domain in recycling. Mol Cell Biol 24:7392–7401

    Article  PubMed  CAS  Google Scholar 

  • Medlin JE, Uguen P, Taylor A, Bentley DL, Murphy S (2003) The C-terminal domain of pol II and a DRB-sensitive kinase are required for 3′ processing of U2 snRNA. EMBO J 22:925–934

    Article  PubMed  CAS  Google Scholar 

  • Meister G, Eggert C, Fischer U (2002) SMN-mediated assembly of RNPs: a complex story. Trends Cell Biol 12:472–478

    Article  PubMed  CAS  Google Scholar 

  • Misteli T (2001) The concept of self-organization in cellular architecture. J Cell Biol 155:181–185

    Article  PubMed  CAS  Google Scholar 

  • Molenaar C, Abdulle A, Gena A, Tanke HJ, Dirks RW (2004) Poly(A)+ RNAs roam the cell nucleus and pass through speckle domains in transcriptionally active and inactive cells. J Cell Biol 165:191–202

    Article  PubMed  CAS  Google Scholar 

  • Monneron A, Bernhard W (1969) Fine structural organization of the interphase nucleus in some mammalian cells. J Ultrastruct Res 27:266–288

    Article  PubMed  CAS  Google Scholar 

  • Narayanan U, Ospina JK, Frey MR, Hebert MD, Matera AG (2002) SMN, the spinal muscular atrophy protein, forms a pre-import snRNP complex with snurportin1 and importin beta. Hum Mol Genet 11:1785–1795

    Article  PubMed  CAS  Google Scholar 

  • Narayanan U, Achsel T, Luhrmann R, Matera AG (2004) Coupled in vitro import of U snRNPs and SMN, the spinal muscular atrophy protein. Mol Cell 16:223–234

    Article  PubMed  CAS  Google Scholar 

  • Nelissen RL, Will CL, van Venrooij WJ, Luhrmann R (1994) The association of the U1-specific 70K and C proteins with U1 snRNPs is mediated in part by common U snRNP proteins. EMBO J 13:4113–4125

    PubMed  CAS  Google Scholar 

  • Nesic D, Kramer A (2001) Domains in human splicing factors SF3a60 and SF3a66 required for binding to SF3a120, assembly of the 17S U2 snRNP, and prespliceosome formation. Mol Cell Biol 21:6406–6417

    Article  PubMed  CAS  Google Scholar 

  • Nesic D, Tanackovic G, Kramer A (2004) A role for Cajal bodies in the final steps of U2 snRNP biogenesis. J Cell Sci 117:4423–4433

    Article  PubMed  CAS  Google Scholar 

  • Neugebauer KM (2002) On the importance of being co-transcriptional. J Cell Sci 115:3865–3871

    Article  PubMed  CAS  Google Scholar 

  • Nottrott S, Urlaub H, Luhrmann R (2002) Hierarchical, clustered protein interactions with U4/U6 snRNA: a biochemical role for U4/U6 proteins. EMBO J 21:5527–5538

    Article  PubMed  CAS  Google Scholar 

  • Ogg SC, Lamond AI (2002) Cajal bodies and coilin-moving towards function. J Cell Biol 159:17–21

    Article  PubMed  CAS  Google Scholar 

  • Ohno M, Segref A, Bachi A, Wilm M, Mattaj IW (2000) PHAX, a mediator of U snRNA nuclear export whose activity is regulated by phosphorylation. Cell 101:187–198

    Article  PubMed  CAS  Google Scholar 

  • Paushkin S, Gubitz AK, Massenet S, Dreyfuss G (2002) The SMN complex, an assemblyosome of ribonucleoproteins. Curr Opin Cell Biol 14:305–312

    Article  PubMed  CAS  Google Scholar 

  • Pellizzoni L, Kataoka N, Charroux B, Dreyfuss G (1998) A novel function for SMN, the spinal muscular atrophy disease gene product, in pre-mRNA splicing. Cell 95:615–624

    Article  PubMed  CAS  Google Scholar 

  • Pillai RS, Will CL, Luhrmann R, Schumperli D, Muller B (2001) Purified U7 snRNPs lack the Sm proteins D1 and D2 but contain Lsm10, a new 14 kDa Sm D1-like protein. EMBO J 20:5470–5479

    Article  PubMed  CAS  Google Scholar 

  • Pillai RS, Grimmler M, Meister G, Will CL, Luhrmann R, Fischer U, Schumperli D (2003) Unique Sm core structure of U7 snRNPs: assembly by a specialized SMN complex and the role of a new component, Lsm11, in histone RNA processing. Genes Dev 17:2321–2333

    Article  PubMed  CAS  Google Scholar 

  • Platani M, Goldberg I, Swedlow JR, Lamond AI (2000) In vivo analysis of Cajal body movement, separation, and joining in live human cells. J Cell Biol 151:1561–1574

    Article  PubMed  CAS  Google Scholar 

  • Platani M, Goldberg I, Lamond AI, Swedlow JR (2002) Cajal body dynamics and association with chromatin are ATP-dependent. Nat Cell Biol 4:502–508

    Article  PubMed  CAS  Google Scholar 

  • Rader SD, Guthrie C (2002) A conserved Lsm-interaction motif in Prp24 required for efficient U4/U6 di-snRNP formation. RNA 8:1378–1392

    Article  PubMed  CAS  Google Scholar 

  • Raska I, Andrade LE, Ochs RL, Chan EK, Chang CM, Roos G, Tan EM (1991) Immunological and ultrastructural studies of the nuclear coiled body with autoimmune antibodies. Exp Cell Res 195:27–37

    Article  PubMed  CAS  Google Scholar 

  • Richard P, Darzacq X, Bertrand E, Jady BE, Verheggen C, Kiss T (2003) A common sequence motif determines the Cajal body-specific localization of box H/ACA scaRNAs. EMBO J 22:4283–4293

    Article  PubMed  CAS  Google Scholar 

  • Schaffert N, Hossbach M, Heintzmann R, Achsel T, Luhrmann R (2004) RNAi knockdown of hPrp31 leads to an accumulation of U4/U6 di-snRNPs in Cajal bodies. EMBO J 23:3000–3009

    Article  PubMed  CAS  Google Scholar 

  • Schneider C, Will CL, Makarova OV, Makarov EM, Luhrmann R (2002) Human U4/U6.U5 and U4atac/U6atac.U5 tri-snRNPs exhibit similar protein compositions. Mol Cell Biol 22:3219–3229

    Article  PubMed  CAS  Google Scholar 

  • Schul W, Groenhout B, Koberna K, Takagaki Y, Jenny A, Manders EM, Raska I, van Driel R, de Jong L (1996) The RNA 3′ cleavage factors CstF 64 kDa and CPSF 100 kDa are concentrated in nuclear domains closely associated with coiled bodies and newly synthesized RNA. EMBO J 15:2883–2892

    PubMed  CAS  Google Scholar 

  • Schul W, van Driel R, de Jong L (1998) Coiled bodies and U2 snRNA genes adjacent to coiled bodies are enriched in factors required for snRNA transcription. Mol Biol Cell 9:1025–1036

    PubMed  CAS  Google Scholar 

  • Schul W, Adelaar B, van Driel R, de Jong L (1999a) Coiled bodies are predisposed to a spatial association with genes that contain snoRNA sequences in their introns. J Cell Biochem 75:393–403

    Article  PubMed  CAS  Google Scholar 

  • Schul W, van Der Kraan I, Matera AG, van Driel R, de Jong L (1999b) Nuclear domains enriched in RNA 3′-processing factors associate with coiled bodies and histone genes in a cell cycle-dependent manner. Mol Biol Cell 10:3815–3824

    PubMed  CAS  Google Scholar 

  • Schumperli D, Pillai RS (2004) The special Sm core structure of the U7 snRNP: far-reaching significance of a small nuclear ribonucleoprotein. Cell Mol Life Sci 61:2560–2570

    Article  PubMed  CAS  Google Scholar 

  • Segref A, Mattaj IW, Ohno M (2001) The evolutionarily conserved region of the U snRNA export mediator PHAX is a novel RNA-binding domain that is essential for U snRNA export. RNA 7:351–360

    Article  PubMed  CAS  Google Scholar 

  • Shav-Tal Y, Singer RH, Darzacq X (2004) Imaging gene expression in single living cells. Nat Rev Mol Cell Biol 5:855–861

    Article  PubMed  CAS  Google Scholar 

  • Shpargel KB, Matera AG (2005) Gemin proteins are required for efficient assembly of Sm-class ribonucleoproteins. Proc Natl Acad Sci USA 102:17372–17377

    Article  PubMed  CAS  Google Scholar 

  • Singh R, Reddy R (1989) Gamma-monomethyl phosphate: a cap structure in spliceosomal U6 small nuclear RNA. Proc Natl Acad Sci USA 86:8280–8283

    PubMed  CAS  Google Scholar 

  • Sleeman JE, Lamond AI (1999) Newly assembled snRNPs associate with coiled bodies before speckles, suggesting a nuclear snRNP maturation pathway. Curr Biol 9:1065–1074

    Article  PubMed  CAS  Google Scholar 

  • Sleeman JE, Ajuh P, Lamond AI (2001) snRNP protein expression enhances the formation of Cajal bodies containing p80-coilin and SMN. J Cell Sci 114:4407–4419

    PubMed  CAS  Google Scholar 

  • Sleeman JE, Trinkle-Mulcahy L, Prescott AR, Ogg SC, Lamond AI (2003) Cajal body proteins SMN and /coilin show differential dynamic behaviour in vivo. J Cell Sci 116:2039–2050

    Article  PubMed  CAS  Google Scholar 

  • Smith KP, Lawrence JB (2000) Interactions of U2 gene loci and their nuclear transcripts with Cajal (coiled) bodies: evidence for PreU2 within Cajal bodies. Mol Biol Cell 11:2987–2998

    PubMed  CAS  Google Scholar 

  • Smith KP, Carter KC, Johnson CV, Lawrence JB (1995) U2 and U1 snRNA gene loci associate with coiled bodies. J Cell Biochem 59:473–485

    Article  PubMed  CAS  Google Scholar 

  • Staley JP, Guthrie C (1998) Mechanical devices of the spliceosome: motors, clocks, springs, and things. Cell 92:315–326

    Article  PubMed  CAS  Google Scholar 

  • Stanek D, Neugebauer KM (2004) Detection of snRNP assembly intermediates in Cajal bodies by fluorescence resonance energy transfer. J Cell Biol 166:1015–1025

    Article  PubMed  CAS  Google Scholar 

  • Stanek D, Rader SD, Klingauf M, Neugebauer KM (2003) Targeting of U4/U6 small nuclear RNP assembly factor SART3/p110 to Cajal bodies. J Cell Biol 160:505–516

    Article  PubMed  CAS  Google Scholar 

  • Teigelkamp S, Achsel T, Mundt C, Gothel SF, Cronshagen U, Lane WS, Marahiel M, Luhrmann R (1998) The 20 kD protein of human [U4/U6.U5] tri-snRNPs is a novel cyclophilin that forms a complex with the U4/U6-specific 60 kD and 90 kD proteins. RNA 4:127–141

    PubMed  CAS  Google Scholar 

  • Terns MP, Terns RM (2001) Macromolecular complexes: SMN–the master assembler. Curr Biol 11:R862–R864

    Article  PubMed  CAS  Google Scholar 

  • Tucker KE, Matera AG (2005) The Cajal body: a nuclear gathering place. In: Hemmerich P, Diekmann S (eds) Vision of the cell nucleus. American Scientific, California, USA

    Google Scholar 

  • Tucker KE, Massello LK, Gao L, Barber TJ, Hebert MD, Chan EK, Matera AG (2000) Structure and characterization of the murine p80 coilin gene, coil. J Struct Biol 129:269–277

    Article  PubMed  CAS  Google Scholar 

  • Tucker KE, Berciano MT, Jacobs EY, LePage DF, Shpargel KB, Rossire JJ, Chan EK, Lafarga M, Conlon RA, Matera AG (2001) Residual Cajal bodies in coilin knockout mice fail to recruit Sm snRNPs and SMN, the spinal muscular atrophy gene product. J Cell Biol 154:293–307

    Article  PubMed  CAS  Google Scholar 

  • Tuma RS, Roth MB (1999) Induction of coiled body-like structures in Xenopus oocytes by U7 snRNA. Chromosoma 108:337–344

    Article  PubMed  CAS  Google Scholar 

  • Tuma RS, Stolk JA, Roth MB (1993) Identification and characterization of a sphere organelle protein. J Cell Biol 122:767–773

    Article  PubMed  CAS  Google Scholar 

  • Tycowski KT, You ZH, Graham PJ, Steitz JA (1998) Modification of U6 spliceosomal RNA is guided by other small RNAs. Mol Cell 2:629–638

    Article  PubMed  CAS  Google Scholar 

  • Uguen P, Murphy S (2003) The 3′ ends of human pre-snRNAs are produced by RNA polymerase II CTD-dependent RNA processing. EMBO J 22:4544–4554

    Article  PubMed  CAS  Google Scholar 

  • Watkins NJ, Segault V, Charpentier B, Nottrott S, Fabrizio P, Bachi A, Wilm M, Rosbash M, Branlant C, Luhrmann R (2000) A common core RNP structure shared between the small nucleoar box C/D RNPs and the spliceosomal U4 snRNP. Cell 103:457–466

    Article  PubMed  CAS  Google Scholar 

  • Watkins NJ, Lemm I, Ingelfinger D, Schneider C, Hossbach M, Urlaub H, Luhrmann R (2004) Assembly and maturation of the U3 snoRNP in the nucleoplasm in a large dynamic multiprotein complex. Mol Cell 16:789–798

    Article  PubMed  CAS  Google Scholar 

  • Will CL, Luhrmann R (2005) Splicing of a rare class of introns by the U12-dependent spliceosome. Biol Chem 386:713–724

    Article  PubMed  CAS  Google Scholar 

  • Will CL, Urlaub H, Achsel T, Gentzel M, Wilm M, Luhrmann R (2002) Characterization of novel SF3b and 17S U2 snRNP proteins, including a human Prp5p homologue and an SF3b DEAD-box protein. EMBO J 21:4978–4988

    Article  PubMed  CAS  Google Scholar 

  • Will CL, Schneider C, Hossbach M, Urlaub H, Rauhut R, Elbashir S, Tuschl T, Luhrmann R (2004) The human 18S U11/U12 snRNP contains a set of novel proteins not found in the U2-dependent spliceosome. RNA 10:929–941

    Article  PubMed  CAS  Google Scholar 

  • Wu CH, Gall JG (1993) U7 small nuclear RNA in C snurposomes of the Xenopus germinal vesicle. Proc Natl Acad Sci USA 90:6257–6259

    PubMed  CAS  Google Scholar 

  • Wu CH, Murphy C, Gall JG (1996) The Sm binding site targets U7 snRNA to coiled bodies (spheres) of amphibian oocytes. RNA 2:811–823

    PubMed  CAS  Google Scholar 

  • Xu H, Pillai RS, Azzouz TN, Shpargel KB, Kambach C, Hebert MD, Schumperli D, Matera AG (2005) The C-terminal domain of coilin interacts with Sm proteins and U snRNPs. Chromosoma 114:155–166

    Article  PubMed  CAS  Google Scholar 

  • Yan D, Perriman R, Igel H, Howe KJ, Neville M, Ares M, Jr. (1998) CUS2, a yeast homolog of human Tat-SF1, rescues function of misfolded U2 through an unusual RNA recognition motif. Mol Cell Biol 18:5000–5009

    PubMed  CAS  Google Scholar 

  • Yu YT, Shu MD, Steitz JA (1998) Modifications of U2 snRNA are required for snRNP assembly and pre-mRNA splicing. EMBO J 17:5783–5795

    Article  PubMed  CAS  Google Scholar 

  • Zaric B, Chami M, Remigy H, Engel A, Ballmer-Hofer K, Winkler FK, Kambach C (2005) Reconstitution of two recombinant LSm protein complexes reveals aspects of their architecture, assembly, and function. J Biol Chem 280:16066–16075

    Article  PubMed  CAS  Google Scholar 

  • Zhao X, Yu YT (2004) Pseudouridines in and near the branch site recognition region of U2 snRNA are required for snRNP biogenesis and pre-mRNA splicing in Xenopus oocytes. RNA 10:681–690

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

Work in our laboratories is supported by the Max Planck Society, a grant (to KMN) from the Deutsche Forschung Gemeinschaft (NE909/1-1), and grants (to DS) from Granting Agency of the Czech Republic (301/05/0601) and the Czech Ministry of Education (1K05009, MSM0021620806, AV0Z50110509 and LC535). We thank Christine Panagiotidis for help with graphics and Mirko Klingauf, Magda Strzelecka, and Arnold Kiss for helpful discussions and comments on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to David Staněk.

Additional information

Communicated by G. Matera

Rights and permissions

Reprints and permissions

About this article

Cite this article

Staněk, D., Neugebauer, K.M. The Cajal body: a meeting place for spliceosomal snRNPs in the nuclear maze. Chromosoma 115, 343–354 (2006). https://doi.org/10.1007/s00412-006-0056-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00412-006-0056-6

Keywords

Navigation