Phosphorylation regulates coilin activity and RNA association

Biology Open

Volumn 2, Issue 4, 2013, Pages 407-415

  Broome, Hanna J ^a   Carrero, Zunamys I ^a   Douglas, Heather E ^a   Hebert, Michael D ^a  

^a UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

Author keywords

Cajal body; SnRNA; Telomerase

Indexed keywords

EID: 84964999919     PISSN: None     EISSN: 20466390     Source Type: Journal    
DOI: 10.1242/bio.20133863     Document Type: Article

References (44)

1. Andrade, L. E. C., Chan, E. K. L., Raska, I., Peebles, C. L., Roos, G. and Tan, E. M. (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.
2. Baillat, D., Hakimi, M. A., Näär, A. M., Shilatifard, A., Cooch, N. and 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.
3. Beausoleil, S. A., Jedrychowski, M., Schwartz, D., Elias, J. E., Villén, J., Li, J., Cohn, M. A., Cantley, L. C. and Gygi, S. P. (2004). Large-scale characterization of HeLa cell nuclear phosphoproteins. Proc. Natl. Acad. Sci. USA 101, 12130-12135.
4. Broome, H. J. and Hebert, M. D. (2012). In vitro RNase and nucleic acid binding activities implicate coilin in U snRNA processing. PLoS ONE 7, e36300.
5. Broome, H. J. and Hebert, M. D. (2013). Coilin displays differential affinity for specific RNAs in vivo and is linked to telomerase RNA biogenesis. J. Mol. Biol. 425, 713-724.
6. Carmo-Fonseca, M., Pepperkok, R., Carvalho, M. T. and Lamond, A. I. (1992). Transcription-dependent colocalization of the U1, U2, U4/U6, and U5 snRNPs in coiled bodies. J. Cell Biol. 117, 1-14.
7. Carmo-Fonseca, M., Ferreira, J. and Lamond, A. I. (1993). Assembly of snRNPcontaining coiled bodies is regulated in interphase and mitosis-evidence that the coiled body is a kinetic nuclear structure. J. Cell Biol. 120, 841-852.
8. Carrero, Z. I., Velma, V., Douglas, H. E. and Hebert, M. D. (2011). Coilin phosphomutants disrupt Cajal body formation, reduce cell proliferation and produce a distinct coilin degradation product. PLoS ONE 6, e25743.
9. Collier, S., Pendle, A., Boudonck, K., van Rij, T., Dolan, L. and Shaw, P. (2006). A distant coilin homologue is required for the formation of cajal bodies in Arabidopsis. Mol. Biol. Cell 17, 2942-2951.
10. Dephoure, N., Zhou, C., Villén, J., Beausoleil, S. A., Bakalarski, C. E., Elledge, S. J. and Gygi, S. P. (2008). A quantitative atlas of mitotic phosphorylation. Proc. Natl. Acad. Sci. USA 105, 10762-10767.
11. Egloff, S., O'Reilly, D., Chapman, R. D., Taylor, A., Tanzhaus, K., Pitts, L., Eick, D. and Murphy, S. (2007). Serine-7 of the RNA polymerase II CTD is specifically required for snRNA gene expression. Science 318, 1777-1779.
12. Faustino, N. A. and Cooper, T. A. (2003). Pre-mRNA splicing and human disease. Genes Dev. 17, 419-437.
13. Frey, M. R. and Matera, A. G. (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.
14. Frey, M. R. and Matera, A. G. (2001). RNA-mediated interaction of Cajal bodies and U2 snRNA genes. J. Cell Biol. 154, 499-509.
15. Frey, M. R., Bailey, A. D., Weiner, A. M. and Matera, A. G. (1999). Association of snRNA genes with coiled bodies is mediated by nascent snRNA transcripts. Curr. Biol. 9, 126-136.
16. Gilder, A. S., Do, P. M., Carrero, Z. I., Cosman, A. M., Broome, H. J., Velma, V., Martinez, L. A. and Hebert, M. D. (2011). Coilin participates in the suppression of RNA polymerase I in response to cisplatin-induced DNA damage. Mol. Biol. Cell 22, 1070-1079.
17. Hearst, S. M., Gilder, A. S., Negi, S. S., Davis, M. D., George, E. M., Whittom, A. A., Toyota, C. G., Husedzinovic, A., Gruss, O. J. and Hebert, M. D. (2009). Cajalbody formation correlates with differential coilin phosphorylation in primary and transformed cell lines. J. Cell Sci. 122, 1872-1881.
18. Hebert, M. D. and Matera, A. G. (2000). Self-association of coilin reveals a common theme in nuclear body localization. Mol. Biol. Cell 11, 4159-4171.
19. Jády, B. E., Darzacq, X., Tucker, K. E., Matera, A. G., Bertrand, E. and 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.
20. Lam, Y. W., Lyon, C. E. and Lamond, A. I. (2002). Large-scale isolation of Cajal bodies from HeLa cells. Mol. Biol. Cell 13, 2461-2473.
21. Leeflang, E. P., Liu, W.-M., Hashimoto, C., Choudary, P. V. and Schmid, C. W. (1992). Phylogenetic evidence for multiple Alu source genes. J. Mol. Evol. 35, 7-16.
22. Lemm, I., Girard, C., Kuhn, A. N., Watkins, N. J., Schneider, M., Bordonné, R. and Lührmann, R. (2006). Ongoing U snRNP biogenesis is required for the integrity of Cajal bodies. Mol. Biol. Cell 17, 3221-3231.
23. Liu, J. L., Wu, Z., Nizami, Z., Deryusheva, S., Rajendra, T. K., Beumer, K. J., Gao, H., Matera, A. G., Carroll, D. and Gall, J. G. (2009). Coilin is essential for Cajal body organization in Drosophila melanogaster. Mol. Biol. Cell 20, 1661-1670.
24. Machyna, M., Heyn, P. and Neugebauer, K. M. (2013). Cajal bodies: where form meets function. Wiley Interdiscip Rev RNA 4, 17-34.
25. Mahmoudi, S., Henriksson, S., Weibrecht, I., Smith, S., Söderberg, O., Strömblad, S., Wiman, K. G. and Farnebo, M. (2010). WRAP53 is essential for Cajal body formation and for targeting the survival of motor neuron complex to Cajal bodies. PLoS Biol. 8, e1000521.
26. Nesic, D., Tanackovic, G. and Krämer, A. (2004). A role for Cajal bodies in the final steps of U2 snRNP biogenesis. J. Cell Sci. 117, 4423-4433.
27. Nizami, Z. F. and Gall, J. G. (2012). Pearls are novel Cajal body-like structures in the Xenopus germinal vesicle that are dependent on RNA pol III transcription. Chromosome Res. 20, 953-969.
28. Otzen, D. E. and Oliveberg, M. (2001). A simple way to measure protein refolding rates in water. J. Mol. Biol. 313, 479-483.
29. Shanbhag, R., Kurabi, A., Kwan, J. J. and Donaldson, L.W. (2010). Solution structure of the carboxy-terminal Tudor domain from human Coilin. FEBS Lett. 584, 4351-4356.
30. Smith, K. P., Carter, K. C., Johnson, C. V. and Lawrence, J. B. (1995). U2 and U1 snRNA gene loci associate with coiled bodies. J. Cell. Biochem. 59, 473-485.
31. Spector, D. L., Lark, G. and Huang, S. (1992). Differences in snRNP localization between transformed and nontransformed cells. Mol. Biol. Cell 3, 555-569.
32. Stern, J. L., Zyner, K. G., Pickett, H. A., Cohen, S. B. and Bryan, T. M. (2012). Telomerase recruitment requires both TCAB1 and Cajal bodies independently. Mol. Cell. Biol. 32, 2384-2395.
33. Strzelecka, M., Oates, A. C. and Neugebauer, K. M. (2010a). Dynamic control of Cajal body number during zebrafish embryogenesis. Nucleus 1, 96-108.
34. Strzelecka, M., Trowitzsch, S., Weber, G., Lührmann, R., Oates, A. C. and Neugebauer, K. M. (2010b). Coilin-dependent snRNP assembly is essential for zebrafish embryogenesis. Nat. Struct. Mol. Biol. 17, 403-409.
35. Sun, J., Xu, H., Subramony, S. H. and Hebert, M. D. (2005). Interactions between coilin and PIASy partially link Cajal bodies to PML bodies. J. Cell Sci. 118, 4995-5003.
36. Tapia, O., Bengoechea, R., Berciano, M. T. and Lafarga, M. (2010). Nucleolar targeting of coilin is regulated by its hypomethylation state. Chromosoma 119, 527-540.
37. Theimer, C. A., Jády, B. E., Chim, N., Richard, P., Breece, K. E., Kiss, T. and Feigon, J. (2007). Structural and functional characterization of human telomerase RNA processing and cajal body localization signals. Mol. Cell 27, 869-881.
38. Toyota, C. G., Davis, M. D., Cosman, A. M. and Hebert, M. D. (2010). Coilin phosphorylationmediates interaction with SMN and SmB'. Chromosoma 119, 205-215.
39. Tucker, K. E., Berciano, M. T., Jacobs, E. Y., LePage, D. F., Shpargel, K. B., Rossire, J. J., Chan, E. K., Lafarga, M., Conlon, R. A. and Matera, A. G. (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.
40. Tycowski, K. T., Shu, M. D., Kukoyi, A. and Steitz, J. A. (2009). A conserved WD40 protein binds the Cajal body localization signal of scaRNP particles. Mol. Cell 34, 47-57.
41. Venteicher, A. S., Abreu, E. B., Meng, Z., McCann, K. E., Terns, R. M., Veenstra, T. D., Terns, M. P. and Artandi, S. E. (2009). A human telomerase holoenzyme protein required for Cajal body localization and telomere synthesis. Science 323, 644-648.
42. Walker, M. P., Tian, L. and Matera, A. G. (2009). Reduced viability, fertility and fecundity in mice lacking the cajal body marker protein, coilin. PLoS ONE 4, e6171.
43. Young, P. J., Le, T. T., thi Man, N., Burghes, A. H. M. and Morris, G. E. (2000). The relationship between SMN, the spinal muscular atrophy protein, and nuclear coiled bodies in differentiated tissues and cultured cells. Exp. Cell Res. 256, 365-374.
44. Zhu, Y., Tomlinson, R. L., Lukowiak, A. A., Terns, R. M. and Terns, M. P. (2004). Telomerase RNA accumulates in Cajal bodies in human cancer cells. Mol. Biol. Cell 15, 81-90.