Coilin and Cajal bodies
Language English Country United States Media print
Document type Journal Article, Review, Research Support, Non-U.S. Gov't
PubMed
37682044
PubMed Central
PMC10494742
DOI
10.1080/19491034.2023.2256036
Knihovny.cz E-resources
- Keywords
- Cajal bodies, coilin, snRNA, snRNP, snoRNA, telomerase RNA,
- MeSH
- Cell Nucleus * MeSH
- Coiled Bodies * MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Review MeSH
The nucleus of higher eukaryotes contains a number of structures that concentrate specific biomolecules and play distinct roles in nuclear metabolism. In recent years, the molecular mechanisms controlling their formation have been intensively studied. In this brief review, I focus on coilin and Cajal bodies. Coilin is a key scaffolding protein of Cajal bodies that is evolutionarily conserved in metazoans. Cajal bodies are thought to be one of the archetypal nuclear structures involved in the metabolism of several short non-coding nuclear RNAs. Yet surprisingly little is known about the structure and function of coilin, and a comprehensive model to explain the origin of Cajal bodies is also lacking. Here, I summarize recent results on Cajal bodies and coilin and discuss them in the context of the last three decades of research in this field.
See more in PubMed
Gall JG. Cajal bodies: The first 100 years. Annu Rev Cell Dev Biol. 2000;16(1):273–10. doi: 10.1146/annurev.cellbio.16.1.273 PubMed DOI
Cajal SR. Un sencillo metodo de coloracion seletiva del reticulo protoplasmatico y sus efectos en los diversos organos nerviosos de vertebrados e invertebrados. Trab Lab Invest Biol (Madrid). 1903;2:129–221.
Lafarga M, Tapia O, Romero AM, et al. Cajal bodies in neurons. RNA Biol. 2017;14(6):712–725. doi: 10.1080/15476286.2016.1231360 PubMed DOI PMC
Andrade LE, Chan EK, Raska I, et al. Human autoantibody to a novel protein of the nuclear coiled body: immunological characterization and cDNA cloning of p80-coilin. J Exp Med. 1991;173(6):1407–1419. doi: 10.1084/jem.173.6.1407 PubMed DOI PMC
Raska I, Andrade LE, Ochs RL, et al. Immunological and ultrastructural studies of the nuclear coiled body with autoimmune antibodies. Exp Cell Res. 1991;195(1):27–37. doi: 10.1016/0014-4827(91)90496-H PubMed DOI
Carmo-Fonseca M, Pepperkok R, Sproat BS, et al. In vivo detection of snRNP-rich organelles in the nuclei of mammalian cells. EMBO J. 1991;10(7):1863–1873. doi: 10.1002/j.1460-2075.1991.tb07712.x PubMed DOI PMC
Carmo-Fonseca M, Tollervey D, Pepperkok R, et al. Mammalian nuclei contain foci which are highly enriched in components of the pre-mRNA splicing machinery. EMBO J. 1991;10(1):195–206. doi: 10.1002/j.1460-2075.1991.tb07936.x PubMed DOI PMC
Carmo-Fonseca M, Pepperkok R, Carvalho MT, et al. Transcription-dependent colocalization of the U1, U2, U4/U6, and U5 snRNPs in coiled bodies. J Cell Bio. 1992;117(1):1–14. doi: 10.1083/jcb.117.1.1 PubMed DOI PMC
Frey MR, Matera AG. Coiled bodies contain U7 small nuclear RNA and associate with specific DNA sequences in interphase human cells. Proc Natl Acad Sci U S A. 1995;92(13):5915–5919. doi: 10.1073/pnas.92.13.5915 PubMed DOI PMC
Gao L, Frey MR, Matera AG. 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. 1997;25(23):4740–4747. doi: 10.1093/nar/25.23.4740 PubMed DOI PMC
Smith KP, Carter KC, Johnson CV, et al. U2 and U1 snRNA gene loci associate with coiled bodies. J Cell Biochem. 1995;59(4):473–485. doi: 10.1002/jcb.240590408 PubMed DOI
Schul W, Adelaar B, van Driel R, et al. Coiled bodies are predisposed to a spatial association with genes that contain snoRNA sequences in their introns. J Cell Biochem. 1999;75(3):393–403. doi: 10.1002/(SICI)1097-4644(19991201)75:3<393:AID-JCB5>3.0.CO;2-G PubMed DOI
Jacobs EY, Frey MR, Wu W, et al. 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. 1999;10(5):1653–1663. doi: 10.1091/mbc.10.5.1653 PubMed DOI PMC
Machyna M, Kehr S, Straube K, et al. The coilin interactome identifies hundreds of small noncoding RNAs that traffic through Cajal bodies. Mol Cell. 2014;56(3):389–399. doi: 10.1016/j.molcel.2014.10.004 PubMed DOI
Wang Q, Sawyer IA, Sung MH, et al. Cajal bodies are linked to genome conformation. Nat Commun. 2016;7(1):10966. doi: 10.1038/ncomms10966 PubMed DOI PMC
Frey MR, Bailey AD, Weiner AM, et al. Association of snRNA genes with coiled bodies is mediated by nascent snRNA transcripts. Curr Biol. 1999;9(3):126–135. doi: 10.1016/S0960-9822(99)80066-9 PubMed DOI
Smith KP, Lawrence JB, Gall J. Interactions of U2 gene loci and their nuclear transcripts with Cajal (coiled) bodies: evidence for PreU2 within Cajal bodies. Mol Biol Cell. 2000;11(9):2987–2998. doi: 10.1091/mbc.11.9.2987 PubMed DOI PMC
Suzuki T, Izumi H, Ohno M. Cajal body surveillance of U snRNA export complex assembly. J Cell Bio. 2010;190(4):603–612. doi: 10.1083/jcb.201004109 PubMed DOI PMC
Lardelli RM, Schaffer AE, Eggens VR, et al. Biallelic mutations in the 3´ exonuclease TOE1 cause pontocerebellar hypoplasia and uncover a role in snRNA processing. Nat Genet. 2017;49(3):457–464. doi: 10.1038/ng.3762 PubMed DOI PMC
Son A, Park JE, Kim VN. PARN and TOE1 constitute a 3´ end maturation module for nuclear non-coding RNAs. Cell Rep. 2018;23(3):888–898. doi: 10.1016/j.celrep.2018.03.089 PubMed DOI
Kiss AM, Jady BE, Darzacq X, et al. A Cajal body-specific pseudouridylation guide RNA is composed of two box H/ACA snoRNA-like domains. Nucleic Acids Res. 2002;30(21):4643–4649. doi: 10.1093/nar/gkf592 PubMed DOI PMC
Jady BE, Darzacq X, Tucker KE, et al. Modification of Sm small nuclear RNAs occurs in the nucleoplasmic Cajal body following import from the cytoplasm. EMBO J. 2003;22(8):1878–1888. doi: 10.1093/emboj/cdg187 PubMed DOI PMC
Duchemin A, O’Grady T, Hanache S, et al. DHX15-independent roles for TFIP11 in U6 snRNA modification, U4/U6.U5 tri-snRNP assembly and pre-mRNA splicing fidelity. Nat Commun. 2021;12(1):6648. doi: 10.1038/s41467-021-26932-2 PubMed DOI PMC
Narayanan A, Speckmann W, Terns R, et al. Role of the box C/D motif in localization of small nucleolar RNAs to coiled bodies and nucleoli. MBoC. 1999;10(7):2131–2147. doi: 10.1091/mbc.10.7.2131 PubMed DOI PMC
Gall JG, Bellini M, Wu Z, et al. Assembly of the nuclear transcription and processing machinery: Cajal bodies (coiled bodies) and transcriptosomes. Mol Biol Cell. 1999;10(12):4385–4402. doi: 10.1091/mbc.10.12.4385 PubMed DOI PMC
Pradet-Balade B, Girard C, Boulon S, et al. CRM1 controls the composition of nucleoplasmic pre-snoRNA complexes to licence them for nucleolar transport. EMBO J. 2011;30(11):2205–2218. doi: 10.1038/emboj.2011.128 PubMed DOI PMC
Verheggen C, Lafontaine DL, Samarsky D, et al. Mammalian and yeast U3 snoRNPs are matured in specific and related nuclear compartments. EMBO J. 2002;21(11):2736–2745. doi: 10.1093/emboj/21.11.2736 PubMed DOI PMC
Boulon S, Verheggen C, Jady BE, et al. PHAX and CRM1 are required sequentially to transport U3 snoRNA to nucleoli. Mol Cell. 2004;16(5):777–787. doi: 10.1016/j.molcel.2004.11.013 PubMed DOI
Massenet S, Bertrand E, Verheggen C. Assembly and trafficking of box C/D and H/ACA snoRNPs. RNA Biol. 2017;14(6):680–692. doi: 10.1080/15476286.2016.1243646 PubMed DOI PMC
Carmo-Fonseca M, Ferreira J, Lamond AI. Assembly of snRNP-containing coiled bodies is regulated in interphase and mitosis--evidence that the coiled body is a kinetic nuclear structure. J Cell Bio. 1993;120(4):841–852. doi: 10.1083/jcb.120.4.841 PubMed DOI PMC
Ferreira JA, Carmo-Fonseca M, Lamond AI. Differential interaction of splicing snRNPs with coiled bodies and interchromatin granules during mitosis and assembly of daughter cell nuclei. J Cell Bio. 1994;126(1):11–23. doi: 10.1083/jcb.126.1.11 PubMed DOI PMC
Haaf T, Ward DC. Inhibition of RNA polymerase II transcription causes chromatin decondensation, loss of nucleolar structure, and dispersion of chromosomal domains. Exp Cell Res. 1996;224(1):163–173. doi: 10.1006/excr.1996.0124 PubMed DOI
Pena E, Berciano MT, Fernandez R, et al. Neuronal body size correlates with the number of nucleoli and Cajal bodies, and with the organization of the splicing machinery in rat trigeminal ganglion neurons. J Comp Neurol. 2001;430(2):250–263. doi: 10.1002/1096-9861(20010205)430:2<250:AID-CNE1029>3.0.CO;2-L PubMed DOI
Tapia O, Narcis JO, Riancho J, et al. Cellular bases of the RNA metabolism dysfunction in motor neurons of a murine model of spinal muscular atrophy: role of Cajal bodies and the nucleolus. Neurobiol Dis. 2017;108:83–99. doi: 10.1016/j.nbd.2017.08.004 PubMed DOI
Lafarga M, Berciano MT, Garcia-Segura LM, et al. Acute osmotic/stress stimuli induce a transient decrease of transcriptional activity in the neurosecretory neurons of supraoptic nuclei. J Neurocytol. 1998;27(4):205–217. doi: 10.1023/A:1006937032068 PubMed DOI
Boudonck K, Dolan L, Shaw PJ. Coiled body numbers in the Arabidopsis root epidermis are regulated by cell type, developmental stage and cell cycle parameters. J Cell Sci. 1998;111(24):3687–3694. doi: 10.1242/jcs.111.24.3687 PubMed DOI
Ferreira J, Carmo-Fonseca M. The biogenesis of the coiled body during early mouse development. Development. 1995;121(2):601–612. doi: 10.1242/dev.121.2.601 PubMed DOI
Strzelecka M, Oates AC, Neugebauer KM. Dynamic control of Cajal body number during zebrafish embryogenesis. Nucleus. 2010;1(1):96–108. doi: 10.4161/nucl.1.1.10680 PubMed DOI PMC
Strzelecka M, Trowitzsch S, Weber G, et al. Coilin-dependent snRNP assembly is essential for zebrafish embryogenesis. Nat Struct Mol Biol. 2010;17(4):403–409. doi: 10.1038/nsmb.1783 PubMed DOI
Stanek D, Fox AH. Nuclear bodies: news insights into structure and function. Curr Opin Cell Biol. 2017;46:94–101. doi: 10.1016/j.ceb.2017.05.001 PubMed DOI
Shin Y, Brangwynne CP. Liquid phase condensation in cell physiology and disease. Science. 2017;357(6357). doi: 10.1126/science.aaf4382 PubMed DOI
Tucker KE, Berciano MT, Jacobs EY, et al. Residual Cajal bodies in coilin knockout mice fail to recruit Sm snRNPs and SMN, the spinal muscular atrophy gene product. J Cell Bio. 2001;154(2):293–308. doi: 10.1083/jcb.200104083 PubMed DOI PMC
Liu JL, Wu Z, Nizami Z, et al. Coilin is essential for Cajal body organization in Drosophila melanogaster. Mol Biol Cell. 2009;20(6):1661–1670. doi: 10.1091/mbc.e08-05-0525 PubMed DOI PMC
Chen Y, Deng Z, Jiang S, et al. Human cells lacking coilin and Cajal bodies are proficient in telomerase assembly, trafficking and telomere maintenance. Nucleic Acids Res. 2015;43(1):385–395. doi: 10.1093/nar/gku1277 PubMed DOI PMC
Basello DA, Matera AG, Stanek D. A point mutation in human coilin prevents Cajal body formation. J Cell Sci. 2022;135(8). doi: 10.1242/jcs.259587 PubMed DOI PMC
Collier S, Pendle A, Boudonck K, et al. A distant coilin homologue is required for the formation of Cajal bodies in Arabidopsis. Mol Biol Cell. 2006;17(7):2942–2951. doi: 10.1091/mbc.e05-12-1157 PubMed DOI PMC
Hebert MD, Matera AG, Silver PA. Self-association of coilin reveals a common theme in nuclear body localization. Mol Biol Cell. 2000;11(12):4159–4171. doi: 10.1091/mbc.11.12.4159 PubMed DOI PMC
Courchaine E, Gelles-Watnick S, Machyna M, et al. The coilin N-terminus mediates multivalent interactions between coilin and Nopp140 to form and maintain Cajal bodies. Nat Commun. 2022;13(1):6005. doi: 10.1038/s41467-022-33434-2 PubMed DOI PMC
Stanek D, Neugebauer KM. Detection of snRNP assembly intermediates in Cajal bodies by fluorescence resonance energy transfer. J Cell Bio. 2004;166(7):1015–1025. doi: 10.1083/jcb.200405160 PubMed DOI PMC
Sleeman J, Lyon CE, Platani M, et al. Dynamic interactions between splicing snRnps, coiled bodies and nucleoli revealed using snRNP protein fusions to the green fluorescent protein. Exp Cell Res. 1998;243(2):290–304. doi: 10.1006/excr.1998.4135 PubMed DOI
Lyon CE, Bohmann K, Sleeman J, et al. Inhibition of protein dephosphorylation results in the accumulation of splicing snRNPs and coiled bodies within the nucleolus. Exp Cell Res. 1997;230(1):84–93. doi: 10.1006/excr.1996.3380 PubMed DOI
Broome HJ, Carrero ZI, Douglas HE, et al. Phosphorylation regulates coilin activity and RNA association. Biol Open. 2013;2(4):407–415. doi: 10.1242/bio.20133863 PubMed DOI PMC
Hearst SM, Gilder AS, Negi SS, et al. Cajal-body formation correlates with differential coilin phosphorylation in primary and transformed cell lines. J Cell Sci. 2009;122(11):1872–1881. doi: 10.1242/jcs.044040 PubMed DOI PMC
Carrero ZI, Velma V, Douglas HE, et al. Coilin phosphomutants disrupt Cajal body formation, reduce cell proliferation and produce a distinct coilin degradation product. PLoS One. 2011;6(10):e25743. doi: 10.1371/journal.pone.0025743 PubMed DOI PMC
Hebert MD, Poole AR. Towards an understanding of regulating Cajal body activity by protein modification. RNA Biol. 2017;14(6):761–778. doi: 10.1080/15476286.2016.1243649 PubMed DOI PMC
Berchtold D, Battich N, Pelkmans L. A systems-level study reveals regulators of membrane-less organelles in human cells. Mol Cell. 2018;72(6):1035–49 e5. doi: 10.1016/j.molcel.2018.10.036 PubMed DOI
Jonik-Nowak B, Menneteau T, Fesquet D, et al. PIP30/FAM192A is a novel regulator of the nuclear proteasome activator PA28γ. Proc Natl Acad Sci U S A. 2018;115(28):E6477–E86. doi: 10.1073/pnas.1722299115 PubMed DOI PMC
Cantarero L, Sanz-Garcia M, Vinograd-Byk H, et al. VRK1 regulates Cajal body dynamics and protects coilin from proteasomal degradation in cell cycle. Sci Rep. 2015;5(1):10543. doi: 10.1038/srep10543 PubMed DOI PMC
Niu H, Zhao M, Huang J, et al. UHMK1-dependent phosphorylation of Cajal body protein coilin alters 5-FU sensitivity in colon cancer cells. Cell Commun Signal. 2022;20(1):18. doi: 10.1186/s12964-022-00820-8 PubMed DOI PMC
Martin-Doncel E, Rojas AM, Cantarero L, et al. VRK1 functional insufficiency due to alterations in protein stability or kinase activity of human VRK1 pathogenic variants implicated in neuromotor syndromes. Sci Rep. 2019;9(1):13381. doi: 10.1038/s41598-019-49821-7 PubMed DOI PMC
Liu J, Hebert MD, Ye Y, et al. Cell cycle-dependent localization of the CDK2-cyclin E complex in Cajal (coiled) bodies. J Cell Sci. 2000;113(Pt 9):1543–1552. doi: 10.1242/jcs.113.9.1543 PubMed DOI
Bellini M, Gall JG, Blackburn EA. Coilin can form a complex with the U7 small nuclear ribonucleoprotein. Mol Biol Cell. 1998;9(10):2987–3001. doi: 10.1091/mbc.9.10.2987 PubMed DOI PMC
Makarov V, Rakitina D, Protopopova A, et al. Plant coilin: structural characteristics and RNA-binding properties. PLoS One. 2013;8(1):e53571. doi: 10.1371/journal.pone.0053571 PubMed DOI PMC
Broome HJ, Hebert MD. Coilin displays differential affinity for specific RNAs in vivo and is linked to telomerase RNA biogenesis. J Mol Biol. 2013;425(4):713–724. doi: 10.1016/j.jmb.2012.12.014 PubMed DOI PMC
Machyna M, Neugebauer KM, Stanek D. Coilin: the first 25 years. RNA Biol. 2015;12(6):590–596. doi: 10.1080/15476286.2015.1034923 PubMed DOI PMC
Hebert MD, Szymczyk PW, Shpargel KB, et al. Coilin forms the bridge between Cajal bodies and SMN, the spinal muscular atrophy protein. Genes Dev. 2001;15(20):2720–2729. doi: 10.1101/gad.908401 PubMed DOI PMC
Shanbhag R, Kurabi A, Kwan JJ, et al. Solution structure of the carboxy-terminal Tudor domain from human Coilin. FEBS Lett. 2010;584(20):4351–4356. doi: 10.1016/j.febslet.2010.09.034 PubMed DOI
Courchaine EM, Barentine AES, Straube K, et al. DMA-tudor interaction modules control the specificity of in vivo condensates. Cell. 2021;184(14):3612–3625.e17. doi: 10.1016/j.cell.2021.05.008 PubMed DOI PMC
Meister G, Eggert C, Buhler D, et al. Methylation of Sm proteins by a complex containing PRMT5 and the putative U snRNP assembly factor pICln. Curr Biol. 2001;11(24):1990–1994. doi: 10.1016/S0960-9822(01)00592-9 PubMed DOI
Meister G, Eggert C, Fischer U. SMN-mediated assembly of RNPs: a complex story. Trends Cell Biol. 2002;12(10):472–478. doi: 10.1016/S0962-8924(02)02371-1 PubMed DOI
Xu H, Pillai RS, Azzouz TN, et al. The C-terminal domain of coilin interacts with Sm proteins and U snRNPs. Chromosoma. 2005;114(3):155–166. doi: 10.1007/s00412-005-0003-y PubMed DOI PMC
Shpargel KB, Ospina JK, Tucker KE, et al. Control of Cajal body number is mediated by the coilin C-terminus. J Cell Sci. 2003;116(2):303–312. doi: 10.1242/jcs.00211 PubMed DOI
Sleeman JE, Ajuh P, Lamond AI. snRNP protein expression enhances the formation of Cajal bodies containing p80-coilin and SMN. J Cell Sci. 2001;114(24):4407–4419. doi: 10.1242/jcs.114.24.4407 PubMed DOI
Novotny I, Malinova A, Stejskalova E, et al. SART3-dependent accumulation of incomplete spliceosomal snRNPs in Cajal bodies. Cell Rep. 2015;10(3):429–440. doi: 10.1016/j.celrep.2014.12.030 PubMed DOI
Roithova A, Klimesova K, Panek J, et al. The Sm-core mediates the retention of partially-assembled spliceosomal snRnps in Cajal bodies until their full maturation. Nucleic Acids Res. 2018;46(7):3774–3790. doi: 10.1093/nar/gky070 PubMed DOI PMC
Kaiser TE, Intine RV, Dundr M. De Novo formation of a subnuclear body. Science. 2008;322(5908):1713–1717. doi: 10.1126/science.1165216 PubMed DOI
Takata H, Nishijima H, Maeshima K, et al. The Integrator complex is required for integrity of Cajal bodies. J Cell Sci. 2012;125(1):166–175. doi: 10.1242/jcs.090837 PubMed DOI
Albrecht TR, Shevtsov SP, Wu Y, et al. Integrator subunit 4 is a ‘symplekin-like’ scaffold that associates with INTS9/11 to form the integrator cleavage module. Nucleic Acids Res. 2018;46(8):4241–4255. doi: 10.1093/nar/gky100 PubMed DOI PMC
Lemm I, Girard C, Kuhn AN, et al. Ongoing U snRNP biogenesis is required for the integrity of Cajal bodies. Mol Biol Cell. 2006;17(7):3221–3231. doi: 10.1091/mbc.e06-03-0247 PubMed DOI PMC
Moreno-Castro C, Prieto-Sanchez S, Sanchez-Hernandez N, et al. Role for the splicing factor TCERG1 in Cajal body integrity and snRNP assembly. J Cell Sci. 2019;132. doi: 10.1242/jcs.232728 PubMed DOI
Cihlarova Z, Kubovciak J, Sobol M, et al. BRAT1 links integrator and defective RNA processing with neurodegeneration. Nat Commun. 2022;13(1):5026. doi: 10.1038/s41467-022-32763-6 PubMed DOI PMC
Girard C, Neel H, Bertrand E, et al. Depletion of SMN by RNA interference in HeLa cells induces defects in Cajal body formation. Nucleic Acids Res. 2006;34(10):2925–2932. doi: 10.1093/nar/gkl374 PubMed DOI PMC
Mahmoudi S, Henriksson S, Weibrecht I, et al. WRAP53 is essential for Cajal body formation and for targeting the survival of motor neuron complex to Cajal bodies. PLoS Biol. 2010;8(11):e1000521. doi: 10.1371/journal.pbio.1000521 PubMed DOI PMC
Shpargel KB, aG M. Gemin proteins are required for efficient assembly of Sm-class ribonucleoproteins. Proc Natl Acad Sci U S A. 2005;102(48):17372–17377. doi: 10.1073/pnas.0508947102 PubMed DOI PMC
Zhai F, Wang J, Luo X, et al. Roles of NOLC1 in cancers and viral infection. J Cancer Res Clin Oncol. 2023;149(12):10593–10608. doi: 10.1007/s00432-023-04934-5 PubMed DOI PMC
Meier UT, Blobel G. NAP57, a mammalian nucleolar protein with a putative homolog in yeast and bacteria. J Cell Bio. 1994;127(6):1505–1514. doi: 10.1083/jcb.127.6.1505 PubMed DOI PMC
Yang Y, Isaac C, Wang C, et al. Conserved composition of mammalian box H/ACA and box C/D small nucleolar ribonucleoprotein particles and their interaction with the common factor Nopp140. Mol Biol Cell. 2000;11(2):567–577. doi: 10.1091/mbc.11.2.567 PubMed DOI PMC
Wang C, Query CC, Meier UT. Immunopurified small nucleolar ribonucleoprotein particles pseudouridylate rRNA independently of their association with phosphorylated Nopp140. Mol Cell Biol. 2002;22(24):8457–8466. doi: 10.1128/MCB.22.24.8457-8466.2002 PubMed DOI PMC
Isaac C, Yang Y, Meier UT. Nopp140 functions as a molecular link between the nucleolus and the coiled bodies. J Cell Bio. 1998;142(2):319–329. doi: 10.1083/jcb.142.2.319 PubMed DOI PMC
Bizarro J, Deryusheva S, Wacheul L, et al. Nopp140-chaperoned 2´-O-methylation of small nuclear RNAs in Cajal bodies ensures splicing fidelity. Genes Dev. 2021;35(15–16):1123–1141. doi: 10.1101/gad.348660.121 PubMed DOI PMC
Riback JA, Zhu L, Ferrolino MC, et al. Composition-dependent thermodynamics of intracellular phase separation. Nature. 2020;581(7807):209–214. doi: 10.1038/s41586-020-2256-2 PubMed DOI PMC
Klingauf M, Stanek D, Neugebauer KM, et al. Enhancement of U4/U6 small nuclear ribonucleoprotein particle association in Cajal bodies predicted by mathematical modeling. Mol Biol Cell. 2006;17(12):4972–4981. doi: 10.1091/mbc.e06-06-0513 PubMed DOI PMC
Stanek D, Pridalova-Hnilicova J, Novotny I, et al. Spliceosomal small nuclear ribonucleoprotein particles repeatedly cycle through Cajal bodies. Mol Biol Cell. 2008;19(6):2534–2543. doi: 10.1091/mbc.e07-12-1259 PubMed DOI PMC
Novotny I, Blazikova M, Stanek D, et al. In vivo kinetics of U4/U6·U5 tri-snRNP formation in Cajal bodies. Mol Biol Cell. 2011;22(4):513–523. doi: 10.1091/mbc.e10-07-0560 PubMed DOI PMC
Schaffert N, Hossbach M, Heintzmann R, et al. RNAi knockdown of hPrp31 leads to an accumulation of U4/U6 di-snRnps in Cajal bodies. EMBO J. 2004;23(15):3000–3009. doi: 10.1038/sj.emboj.7600296 PubMed DOI PMC
Walker MP, Tian L, Matera AG, et al. Reduced viability, fertility and fecundity in mice lacking the Cajal body marker protein, coilin. PLoS One. 2009;4(7):e6171. doi: 10.1371/journal.pone.0006171 PubMed DOI PMC
Abulfaraj AA, Alhoraibi HM, Mariappan K, et al. Analysis of the Arabidopsis coilin mutant reveals a positive role of AtCOILIN in plant immunity. Plant Physiol. 2022;190(1):745–761. doi: 10.1093/plphys/kiac280 PubMed DOI PMC
Deryusheva S, Gall JG, Matera AG. Small Cajal body–specific RNAs of Drosophila function in the absence of Cajal bodies. Mol Biol Cell. 2009;20(24):5250–5259. doi: 10.1091/mbc.e09-09-0777 PubMed DOI PMC
Bizarro J, Dodre M, Huttin A, et al. NUFIP and the HSP90/R2TP chaperone bind the SMN complex and facilitate assembly of U4-specific proteins. Nucleic Acids Res. 2015;43(18):8973–8989. doi: 10.1093/nar/gkv809 PubMed DOI PMC
Nesic D, Tanackovic G, Kramer A. A role for Cajal bodies in the final steps of U2 snRNP biogenesis. J Cell Sci. 2004;117(19):4423–4433. doi: 10.1242/jcs.01308 PubMed DOI
Tanackovic G, Kramer A. Human splicing factor SF3a, but not SF1, is essential for pre-mRNA splicing in vivo. Mol Biol Cell. 2005;16(3):1366–1377. doi: 10.1091/mbc.e04-11-1034 PubMed DOI PMC
Malinova A, Cvackova Z, Mateju D, et al. Assembly of the U5 snRNP component PRPF8 is controlled by the HSP90/R2TP chaperones. J Cell Bio. 2017;216(6):1579–1596. doi: 10.1083/jcb.201701165 PubMed DOI PMC
Klimesova K, Vojackova J, Radivojevic N, et al. TSSC4 is a component of U5 snRNP that promotes tri-snRNP formation. Nat Commun. 2021;12(1):3646. doi: 10.1038/s41467-021-23934-y PubMed DOI PMC
Klimesova K, Petrzilkova H, Barinka C, et al. SART3 associates with a post-splicing complex. J Cell Sci. 2023;136(2). doi: 10.1242/jcs.260380 PubMed DOI
Zhu Y, Tomlinson RL, Lukowiak AA, et al. Telomerase RNA accumulates in Cajal bodies in human cancer cells. Mol Biol Cell. 2004;15(1):81–90. doi: 10.1091/mbc.e03-07-0525 PubMed DOI PMC
Jady BE, Bertrand E, Kiss T. Human telomerase RNA and box H/ACA scaRnas share a common Cajal body–specific localization signal. J Cell Bio. 2004;164(5):647–652. doi: 10.1083/jcb.200310138 PubMed DOI PMC
Venteicher AS, Abreu EB, Meng Z, et al. A human telomerase holoenzyme protein required for Cajal body localization and telomere synthesis. Science. 2009;323(5914):644–648. doi: 10.1126/science.1165357 PubMed DOI PMC
Cristofari G, Adolf E, Reichenbach P, et al. Human telomerase RNA accumulation in Cajal bodies facilitates telomerase recruitment to telomeres and telomere elongation. Mol Cell. 2007;27(6):882–889. doi: 10.1016/j.molcel.2007.07.020 PubMed DOI
Zhong F, Savage SA, Shkreli M, et al. Disruption of telomerase trafficking by TCAB1 mutation causes dyskeratosis congenita. Genes Dev. 2011;25(1):11–16. doi: 10.1101/gad.2006411 PubMed DOI PMC
Stern JL, Zyner KG, Pickett HA, et al. Telomerase recruitment requires both TCAB1 and Cajal bodies independently. Mol Cell Biol. 2012;32(13):2384–2395. doi: 10.1128/MCB.00379-12 PubMed DOI PMC
Tomlinson RL, Li J, Culp BR, et al. A Cajal body-independent pathway for telomerase trafficking in mice. Exp Cell Res. 2010;316(17):2797–2809. doi: 10.1016/j.yexcr.2010.07.001 PubMed DOI PMC
Vogan JM, Zhang X, Youmans DT, et al. Minimized human telomerase maintains telomeres and resolves endogenous roles of H/ACA proteins, TCAB1, and Cajal bodies. Elife. 2016;5. doi: 10.7554/eLife.18221 PubMed DOI PMC
Buemi V, Schillaci O, Santorsola M, et al. TGS1 mediates 2,2,7-trimethyl guanosine capping of the human telomerase RNA to direct telomerase dependent telomere maintenance. Nat Commun. 2022;13(1):2302. doi: 10.1038/s41467-022-29907-z PubMed DOI PMC
Chen L, Roake CM, Galati A, et al. Loss of human TGS1 hypermethylase promotes increased telomerase RNA and telomere elongation. Cell Rep. 2020;30(5):1358–72 e5. doi: 10.1016/j.celrep.2020.01.004 PubMed DOI PMC
Kim NK, Theimer CA, Mitchell JR, et al. Effect of pseudouridylation on the structure and activity of the catalytically essential P6.1 hairpin in human telomerase RNA. Nucleic Acids Res. 2010;38(19):6746–6756. doi: 10.1093/nar/gkq525 PubMed DOI PMC
Rudzka M, Wroblewska-Ankiewicz P, Majewska K, et al. Functional nuclear retention of pre-mRNA involving Cajal bodies during meiotic prophase in European larch (Larix decidua). Plant Cell. 2022;34(6):2404–2423. doi: 10.1093/plcell/koac091 PubMed DOI PMC
Shaw J, Love AJ, Makarova SS, et al. Coilin, the signature protein of Cajal bodies, differentially modulates the interactions of plants with viruses in widely different taxa. Nucleus. 2014;5(1):85–94. doi: 10.4161/nucl.28315 PubMed DOI PMC
Love AJ, Yu C, Petukhova NV, et al. Cajal bodies and their role in plant stress and disease responses. RNA Biol. 2017;14(6):779–790. doi: 10.1080/15476286.2016.1243650 PubMed DOI PMC
Kotova E, Jarnik M, Tulin AV, et al. Poly (ADP-ribose) polymerase 1 is required for protein localization to Cajal body. PLoS Genet. 2009;5(2):e1000387. doi: 10.1371/journal.pgen.1000387 PubMed DOI PMC
Spechenkova N, Samarskaya VO, Kalinina NO, et al. Plant Poly(ADP-Ribose) polymerase 1 is a potential mediator of cross-talk between the Cajal body protein coilin and salicylic acid-mediated antiviral defence. Viruses. 2023;15(6):15. doi: 10.3390/v15061282 PubMed DOI PMC
Shaw J, Yu C, Makhotenko AV, et al. Interaction of a plant virus protein with the signature Cajal body protein coilin facilitates salicylic acid-mediated plant defence responses. New Phytol. 2019;224(1):439–453. doi: 10.1111/nph.15994 PubMed DOI
Petrovska B, Sebela M, Dolezel J. Inside a plant nucleus: discovering the proteins. J Exp Bot. 2015;66(6):1627–1640. doi: 10.1093/jxb/erv041 PubMed DOI