Coilin, the signature protein of Cajal bodies, differentially modulates the interactions of plants with viruses in widely different taxa

References

• Trinkle-Mulcahy L, Lamond AI. Toward a high-resolution view of nuclear dynamics. Science 2007; 318:1402 - 7; http://dx.doi.org/10.1126/science.1142033; PMID: 18048679
   PubMed Web of Science ®Google Scholar
• Hiscox JA. RNA viruses: hijacking the dynamic nucleolus. Nat Rev Microbiol 2007; 5:119 - 27; http://dx.doi.org/10.1038/nrmicro1597; PMID: 17224921
   PubMed Web of Science ®Google Scholar
• Greco A. Involvement of the nucleolus in replication of human viruses. Rev Med Virol 2009; 19:201 - 14; http://dx.doi.org/10.1002/rmv.614; PMID: 19399920
   PubMed Web of Science ®Google Scholar
• Taliansky ME, Brown JWS, Rajamäki ML, Valkonen JP, Kalinina NO. Involvement of the plant nucleolus in virus and viroid infections: parallels with animal pathosystems. Adv Virus Res 2010; 77:119 - 58; http://dx.doi.org/10.1016/B978-0-12-385034-8.00005-3; PMID: 20951872
   PubMed Web of Science ®Google Scholar
• Olson MOJ. Sensing cellular stress: another new function for the nucleolus?. Sci STKE 2004; 2004:pe10; PMID: 15026578
   PubMedGoogle Scholar
• Rubbi CP, Milner J. Disruption of the nucleolus mediates stabilization of p53 in response to DNA damage and other stresses. EMBO J 2003; 22:6068 - 77; http://dx.doi.org/10.1093/emboj/cdg579; PMID: 14609953
   PubMed Web of Science ®Google Scholar
• Sirri V, Urcuqui-Inchima S, Roussel P, Hernandez-Verdun D. Nucleolus: the fascinating nuclear body. Histochem Cell Biol 2008; 129:13 - 31; http://dx.doi.org/10.1007/s00418-007-0359-6; PMID: 18046571
   PubMed Web of Science ®Google Scholar
• Boisvert F-M, van Koningsbruggen S, Navascués J, Lamond AI. The multifunctional nucleolus. Nat Rev Mol Cell Biol 2007; 8:574 - 85; http://dx.doi.org/10.1038/nrm2184; PMID: 17519961
   PubMed Web of Science ®Google Scholar
• Olson MOJ, Dundr M. The moving parts of the nucleolus. Histochem Cell Biol 2005; 123:203 - 16; http://dx.doi.org/10.1007/s00418-005-0754-9; PMID: 15742198
   PubMed Web of Science ®Google Scholar
• Kim SH, Macfarlane S, Kalinina NO, Rakitina DV, Ryabov EV, Gillespie T, Haupt S, Brown JWS, Taliansky M. Interaction of a plant virus-encoded protein with the major nucleolar protein fibrillarin is required for systemic virus infection. Proc Natl Acad Sci U S A 2007; 104:11115 - 20; http://dx.doi.org/10.1073/pnas.0704632104; PMID: 17576925
   PubMed Web of Science ®Google Scholar
• Kim SH, Ryabov EV, Kalinina NO, Rakitina DV, Gillespie T, MacFarlane S, Haupt S, Brown JWS, Taliansky M. Cajal bodies and the nucleolus are required for a plant virus systemic infection. EMBO J 2007; 26:2169 - 79; http://dx.doi.org/10.1038/sj.emboj.7601674; PMID: 17410203
   PubMed Web of Science ®Google Scholar
• Canetta E, Kim SH, Kalinina NO, Shaw J, Adya AK, Gillespie T, Brown JWS, Taliansky M. A plant virus movement protein forms ringlike complexes with the major nucleolar protein, fibrillarin, in vitro.. J Mol Biol 2008; 376:932 - 7; http://dx.doi.org/10.1016/j.jmb.2007.12.039; PMID: 18199452
   PubMed Web of Science ®Google Scholar
• Rajamäki M-L, Valkonen JPT. Control of nuclear and nucleolar localization of nuclear inclusion protein a of picorna-like Potato virus A in Nicotiana species. Plant Cell 2009; 21:2485 - 502; http://dx.doi.org/10.1105/tpc.108.064147; PMID: 19700632
   PubMed Web of Science ®Google Scholar
• Wright KM, Cowan GH, Lukhovitskaya NI, Tilsner J, Roberts AG, Savenkov EI, Torrance L. The N-terminal domain of PMTV TGB1 movement protein is required for nucleolar localization, microtubule association, and long-distance movement. Mol Plant Microbe Interact 2010; 23:1486 - 97; http://dx.doi.org/10.1094/MPMI-05-10-0105; PMID: 20923354
   PubMed Web of Science ®Google Scholar
• Torrance L, Wright KM, Crutzen F, Cowan GH, Lukhovitskaya NI, Bragard C, Savenkov EI. Unusual features of pomoviral RNA movement. Front Microbiol 2011; 2:259; http://dx.doi.org/10.3389/fmicb.2011.00259; PMID: 22203822
   PubMedGoogle Scholar
• Semashko MA, González I, Shaw J, Leonova OG, Popenko VI, Taliansky ME, Canto T, Kalinina NO. The extreme N-terminal domain of a hordeivirus TGB1 movement protein mediates its localization to the nucleolus and interaction with fibrillarin. Biochimie 2012; 94:1180 - 8; http://dx.doi.org/10.1016/j.biochi.2012.02.005; PMID: 22349738
   PubMed Web of Science ®Google Scholar
• Jiang Y, Li Z, Nagy PD. Nucleolin/Nsr1p binds to the 3′ noncoding region of the tombusvirus RNA and inhibits replication. Virology 2010; 396:10 - 20; http://dx.doi.org/10.1016/j.virol.2009.10.007; PMID: 19861225
   PubMed Web of Science ®Google Scholar
• Carmo-Fonseca M. New clues to the function of the Cajal body. EMBO Rep 2002; 3:726 - 7; http://dx.doi.org/10.1093/embo-reports/kvf154; PMID: 12151329
   PubMed Web of Science ®Google Scholar
• Cioce M, Lamond AI. Cajal bodies: a long history of discovery. Annu Rev Cell Dev Biol 2005; 21:105 - 31; http://dx.doi.org/10.1146/annurev.cellbio.20.010403.103738; PMID: 16212489
   PubMed Web of Science ®Google Scholar
• Gall JG. Cajal bodies: the first 100 years. Annu Rev Cell Dev Biol 2000; 16:273 - 300; http://dx.doi.org/10.1146/annurev.cellbio.16.1.273; PMID: 11031238
   PubMed Web of Science ®Google Scholar
• Jády BE, Bertrand E, Kiss T. Human telomerase RNA and box H/ACA scaRNAs share a common Cajal body-specific localization signal. J Cell Biol 2004; 164:647 - 52; http://dx.doi.org/10.1083/jcb.200310138; PMID: 14981093
   PubMed Web of Science ®Google Scholar
• Jády BE, Richard P, Bertrand E, Kiss T. Cell cycle-dependent recruitment of telomerase RNA and Cajal bodies to human telomeres. Mol Biol Cell 2006; 17:944 - 54; http://dx.doi.org/10.1091/mbc.E05-09-0904; PMID: 16319170
   PubMed Web of Science ®Google Scholar
• Kiss AM, Jády BE, Darzacq X, Verheggen C, Bertrand E, Kiss T. A Cajal body-specific pseudouridylation guide RNA is composed of two box H/ACA snoRNA-like domains. Nucleic Acids Res 2002; 30:4643 - 9; http://dx.doi.org/10.1093/nar/gkf592; PMID: 12409454
   PubMed Web of Science ®Google Scholar
• Kiss T. Biogenesis of small nuclear RNPs. J Cell Sci 2004; 117:5949 - 51; http://dx.doi.org/10.1242/jcs.01487; PMID: 15564372
   PubMed Web of Science ®Google Scholar
• Ogg SC, Lamond AI. Cajal bodies and coilin--moving towards function. J Cell Biol 2002; 159:17 - 21; http://dx.doi.org/10.1083/jcb.200206111; PMID: 12379800
   PubMed Web of Science ®Google Scholar
• Schümperli D, Pillai RS. The special Sm core structure of the U7 snRNP: far-reaching significance of a small nuclear ribonucleoprotein. Cell Mol Life Sci 2004; 61:2560 - 70; http://dx.doi.org/10.1007/s00018-004-4190-0; PMID: 15526162
   PubMed Web of Science ®Google Scholar
• Bassett C. Cajal bodies and plant RNA metabolism. CRC Crit Rev Plant Sci 2012; 31:258 - 70; http://dx.doi.org/10.1080/07352689.2011.645431
   Web of Science ®Google Scholar
• Andrade LE, Tan EM, Chan EK. Immunocytochemical analysis of the coiled body in the cell cycle and during cell proliferation. Proc Natl Acad Sci U S A 1993; 90:1947 - 51; http://dx.doi.org/10.1073/pnas.90.5.1947; PMID: 8446613
   PubMed Web of Science ®Google Scholar
• 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 Biol 1993; 120:841 - 52; http://dx.doi.org/10.1083/jcb.120.4.841; PMID: 7679389
   PubMed Web of Science ®Google Scholar
• Strzelecka M, Oates AC, Neugebauer KM. Dynamic control of Cajal body number during zebrafish embryogenesis. Nucleus 2010; 1:96 - 108; PMID: 21327108
   PubMed Web of Science ®Google Scholar
• Walker MP, Tian L, Matera AG. Reduced viability, fertility and fecundity in mice lacking the cajal body marker protein, coilin. PLoS One 2009; 4:e6171; http://dx.doi.org/10.1371/journal.pone.0006171; PMID: 19587784
   PubMed Web of Science ®Google Scholar
• Boulon S, Westman BJ, Hutten S, Boisvert F-M, Lamond AI. The nucleolus under stress. Mol Cell 2010; 40:216 - 27; http://dx.doi.org/10.1016/j.molcel.2010.09.024; PMID: 20965417
   PubMed Web of Science ®Google Scholar
• Collier S, Pendle A, Boudonck K, van Rij T, Dolan L, Shaw P. A distant coilin homologue is required for the formation of cajal bodies in Arabidopsis. Mol Biol Cell 2006; 17:2942 - 51; http://dx.doi.org/10.1091/mbc.E05-12-1157; PMID: 16624863
   PubMed Web of Science ®Google Scholar
• Lemm I, Girard C, Kuhn AN, Watkins NJ, Schneider M, Bordonné R, Lührmann R. Ongoing U snRNP biogenesis is required for the integrity of Cajal bodies. Mol Biol Cell 2006; 17:3221 - 31; http://dx.doi.org/10.1091/mbc.E06-03-0247; PMID: 16687569
   PubMed Web of Science ®Google Scholar
• Liu J-L, Wu Z, Nizami Z, Deryusheva S, Rajendra TK, Beumer KJ, Gao H, Matera AG, Carroll D, Gall JG. Coilin is essential for Cajal body organization in Drosophila melanogaster. Mol Biol Cell 2009; 20:1661 - 70; http://dx.doi.org/10.1091/mbc.E08-05-0525; PMID: 19158395
   PubMed Web of Science ®Google Scholar
• Strzelecka M, Trowitzsch S, Weber G, Lührmann R, Oates AC, Neugebauer KM. Coilin-dependent snRNP assembly is essential for zebrafish embryogenesis. Nat Struct Mol Biol 2010; 17:403 - 9; http://dx.doi.org/10.1038/nsmb.1783; PMID: 20357773
   PubMed Web of Science ®Google Scholar
• Tucker KE, Berciano MT, Jacobs EY, LePage DF, Shpargel KB, Rossire JJ, Chan EK, Lafarga M, Conlon RA, Matera AG. Residual Cajal bodies in coilin knockout mice fail to recruit Sm snRNPs and SMN, the spinal muscular atrophy gene product. J Cell Biol 2001; 154:293 - 307; http://dx.doi.org/10.1083/jcb.200104083; PMID: 11470819
   PubMed Web of Science ®Google Scholar
• Broome HJ, Hebert MD. In vitro RNase and nucleic acid binding activities implicate coilin in U snRNA processing. PLoS One 2012; 7:e36300; http://dx.doi.org/10.1371/journal.pone.0036300; PMID: 22558428
   PubMed Web of Science ®Google Scholar
• Broome HJ, Carrero ZI, Douglas HE, Hebert MD. Phosphorylation regulates coilin activity and RNA association. Biol Open 2013; 2:407 - 15; http://dx.doi.org/10.1242/bio.20133863; PMID: 23616925
   PubMed Web of Science ®Google Scholar
• Makarov V, Rakitina D, Protopopova A, Yaminsky I, Arutiunian A, Love AJ, Taliansky M, Kalinina N. Plant coilin: structural characteristics and RNA-binding properties. PLoS One 2013; 8:e53571; http://dx.doi.org/10.1371/journal.pone.0053571; PMID: 23320094
   PubMed Web of Science ®Google Scholar
• Lam YW, Lyon CE, Lamond AI. Large-scale isolation of Cajal bodies from HeLa cells. Mol Biol Cell 2002; 13:2461 - 73; http://dx.doi.org/10.1091/mbc.02-03-0034; PMID: 12134083
   PubMed Web of Science ®Google Scholar
• Platani M, Goldberg I, Swedlow JR, Lamond AI. In vivo analysis of Cajal body movement, separation, and joining in live human cells. J Cell Biol 2000; 151:1561 - 74; http://dx.doi.org/10.1083/jcb.151.7.1561; PMID: 11134083
   PubMed Web of Science ®Google Scholar
• Velma V, Carrero ZI, Cosman AM, Hebert MD. Coilin interacts with Ku proteins and inhibits in vitro non-homologous DNA end joining. FEBS Lett 2010; 584:4735 - 9; http://dx.doi.org/10.1016/j.febslet.2010.11.004; PMID: 21070772
   PubMed Web of Science ®Google Scholar
• James NJ, Howell GJ, Walker JH, Blair GE. The role of Cajal bodies in the expression of late phase adenovirus proteins. Virology 2010; 399:299 - 311; http://dx.doi.org/10.1016/j.virol.2010.01.013; PMID: 20137801
   PubMed Web of Science ®Google Scholar
• Ghazala W, Waltermann A, Pilot R, Winter S, Varrelmann M. Functional characterization and subcellular localization of the 16K cysteine-rich suppressor of gene silencing protein of tobacco rattle virus. J Gen Virol 2008; 89:1748 - 58; http://dx.doi.org/10.1099/vir.0.83503-0; PMID: 18559946
   PubMed Web of Science ®Google Scholar
• Sharma P, Ikegami M. Characterization of signals that dictate nuclear/nucleolar and cytoplasmic shuttling of the capsid protein of Tomato leaf curl Java virus associated with DNA β satellite. Virus Res 2009; 144:145 - 53; http://dx.doi.org/10.1016/j.virusres.2009.04.019; PMID: 19409945
   PubMed Web of Science ®Google Scholar
• Levy A, Zheng JY, Lazarowitz SG. The tobamovirus Turnip Vein Clearing Virus 30-kilodalton movement protein localizes to novel nuclear filaments to enhance virus infection. J Virol 2013; 87:6428 - 40; http://dx.doi.org/10.1128/JVI.03390-12; PMID: 23536678
   PubMed Web of Science ®Google Scholar
• Xu P, Zhang Y, Kang L, Roossinck MJ, Mysore KS. Computational estimation and experimental verification of off-target silencing during posttranscriptional gene silencing in plants. Plant Physiol 2006; 142:429 - 40; http://dx.doi.org/10.1104/pp.106.083295; PMID: 16920874
   PubMed Web of Science ®Google Scholar
• Bombarely A, Rosli HG, Vrebalov J, Moffett P, Mueller LA, Martin GB. A draft genome sequence of Nicotiana benthamiana to enhance molecular plant-microbe biology research. Mol Plant Microbe Interact 2012; 25:1523 - 30; http://dx.doi.org/10.1094/MPMI-06-12-0148-TA; PMID: 22876960
   PubMed Web of Science ®Google Scholar
• Ratcliff F, Harrison BD, Baulcombe DC. A similarity between viral defense and gene silencing in plants. Science 1997; 276:1558 - 60; http://dx.doi.org/10.1126/science.276.5318.1558; PMID: 18610513
   PubMed Web of Science ®Google Scholar
• Ratcliff FG, MacFarlane SA, Baulcombe DC. Gene silencing without DNA. rna-mediated cross-protection between viruses. Plant Cell 1999; 11:1207 - 16; PMID: 10402423
   PubMed Web of Science ®Google Scholar
• MacFarlane SA, Popovich AH. Efficient expression of foreign proteins in roots from tobravirus vectors. Virology 2000; 267:29 - 35; http://dx.doi.org/10.1006/viro.1999.0098; PMID: 10648180
   PubMed Web of Science ®Google Scholar
• Lawrence DM, Jackson AO. Requirements for cell-to-cell movement of Barley stripe mosaic virus in monocot and dicot hosts. Mol Plant Pathol 2001; 2:65 - 75; http://dx.doi.org/10.1046/j.1364-3703.2001.00052.x; PMID: 20572993
   PubMed Web of Science ®Google Scholar
• Hull R. Matthews’ Plant Virology. London: Academic Press: 2002 .
   Google Scholar
• Baulcombe D. RNA silencing. Trends Biochem Sci 2005; 30:290 - 3; http://dx.doi.org/10.1016/j.tibs.2005.04.012; PMID: 15950871
   PubMed Web of Science ®Google Scholar
• Voinnet O. Induction and suppression of RNA silencing: insights from viral infections. Nat Rev Genet 2005; 6:206 - 20; http://dx.doi.org/10.1038/nrg1555; PMID: 15703763
   PubMed Web of Science ®Google Scholar
• Burgyán J, Havelda Z. Viral suppressors of RNA silencing. Trends Plant Sci 2011; 16:265 - 72; http://dx.doi.org/10.1016/j.tplants.2011.02.010; PMID: 21439890
   PubMed Web of Science ®Google Scholar
• Deleris A, Gallego-Bartolome J, Bao J, Kasschau KD, Carrington JC, Voinnet O. Hierarchical action and inhibition of plant Dicer-like proteins in antiviral defense. Science 2006; 313:68 - 71; http://dx.doi.org/10.1126/science.1128214; PMID: 16741077
   PubMed Web of Science ®Google Scholar
• Martín-Hernández AM, Baulcombe DC. Tobacco rattle virus 16-kilodalton protein encodes a suppressor of RNA silencing that allows transient viral entry in meristems. J Virol 2008; 82:4064 - 71; http://dx.doi.org/10.1128/JVI.02438-07; PMID: 18272576
   PubMed Web of Science ®Google Scholar
• Yelina NE, Savenkov EI, Solovyev AG, Morozov SY, Valkonen JP. Long-distance movement, virulence, and RNA silencing suppression controlled by a single protein in hordei- and potyviruses: complementary functions between virus families. J Virol 2002; 76:12981 - 91; http://dx.doi.org/10.1128/JVI.76.24.12981-12991.2002; PMID: 12438624
   PubMed Web of Science ®Google Scholar
• Voinnet O. Non-cell autonomous RNA silencing. FEBS Lett 2005; 579:5858 - 71; http://dx.doi.org/10.1016/j.febslet.2005.09.039; PMID: 16242131
   PubMed Web of Science ®Google Scholar
• Baumberger N, Baulcombe DC. Arabidopsis ARGONAUTE1 is an RNA Slicer that selectively recruits microRNAs and short interfering RNAs. Proc Natl Acad Sci U S A 2005; 102:11928 - 33; http://dx.doi.org/10.1073/pnas.0505461102; PMID: 16081530
   PubMed Web of Science ®Google Scholar
• Anandalakshmi R, Pruss GJ, Ge X, Marathe R, Mallory AC, Smith TH, Vance VB. A viral suppressor of gene silencing in plants. Proc Natl Acad Sci U S A 1998; 95:13079 - 84; http://dx.doi.org/10.1073/pnas.95.22.13079; PMID: 9789044
   PubMed Web of Science ®Google Scholar
• Semashko MA, Rakitina DV, González I, Canto T, Kalinina NO, Taliansky ME. Movement protein of hordeivirus interacts in vitro and in vivo with coilin, a major structural protein of Cajal bodies. Dokl Biochem Biophys 2012; 442:57 - 60; http://dx.doi.org/10.1134/S1607672912010164; PMID: 22419098
   PubMed Web of Science ®Google Scholar
• Taliansky M, Kim SH, Mayo MA, Kalinina NO, Fraser G, McGeachy KD, Barker H. Escape of a plant virus from amplicon-mediated RNA silencing is associated with biotic or abiotic stress. Plant J 2004; 39:194 - 205; http://dx.doi.org/10.1111/j.1365-313X.2004.02120.x; PMID: 15225285
   PubMed Web of Science ®Google Scholar
• Gushchin VA, Lukhovitskaya NI, Andreev DE, Wright KM, Taliansky ME, Solovyev AG, Morozov SY, MacFarlane SA. Dynamic localization of two tobamovirus ORF6 proteins involves distinct organellar compartments. J Gen Virol 2013; 94:230 - 40; http://dx.doi.org/10.1099/vir.0.045278-0; PMID: 23052393
   PubMed Web of Science ®Google Scholar
• Ryabov EV, Robinson DJ, Taliansky ME. A plant virus-encoded protein facilitates long-distance movement of heterologous viral RNA. Proc Natl Acad Sci U S A 1999; 96:1212 - 7; http://dx.doi.org/10.1073/pnas.96.4.1212; PMID: 9990003
   PubMed Web of Science ®Google Scholar
• Ascencio-Ibañez JT, Settlage SB. DNA abrasion onto plants is an effective method for geminivirus infection and virus-induced gene silencing. J Virol Methods 2007; 142:198 - 203; http://dx.doi.org/10.1016/j.jviromet.2007.01.031; PMID: 17337069
   PubMed Web of Science ®Google Scholar
• Taliansky M, Aranda M, Garcia-Arenal F. Differential invasion by tobamoviruses of Nicotiana megalosiphon following the hypersensitive response. Phytopathology 1994; 84:812 - 5; http://dx.doi.org/10.1094/Phyto-84-812
   Web of Science ®Google Scholar