Coilin phosphomutants disrupt Cajal body formation, reduce cell proliferation and produce a distinct coilin degradation product

PLoS ONE

Volumn 6, Issue 10, 2011, Pages

  Carrero, Zunamys I ^a   Velma, Venkatramreddy ^a   Douglas, Heather E ^a   Hebert, Michael D ^a  

^a UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO TERMINAL TELOPEPTIDE; PHOSPHOPROTEIN; PROTEIN COILIN; UNCLASSIFIED DRUG; DOXYCYCLINE; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; MUTANT PROTEIN; NUCLEAR PROTEIN; P80 COILIN; P80-COILIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL ACTIVITY; CELL CYCLE ARREST; CELL LINE; CELL PROLIFERATION; COILED BODY; CONTROLLED STUDY; GENE SILENCING; HUMAN; HUMAN CELL; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; WILD TYPE; AMINO ACID SEQUENCE; CHEMISTRY; DRUG EFFECT; FLUORESCENT ANTIBODY TECHNIQUE; GENETIC TRANSFECTION; HELA CELL; METABOLISM; MOLECULAR GENETICS; PHOSPHORYLATION;

MAMMALIA;

AMINO ACID SEQUENCE; CELL LINE; CELL PROLIFERATION; COILED BODIES; DOXYCYCLINE; FLUORESCENT ANTIBODY TECHNIQUE; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMANS; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; NUCLEAR PROTEINS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEOLYSIS; RECOMBINANT FUSION PROTEINS; TRANSFECTION;

EID: 80053457099     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0025743     Document Type: Article

References (37)

1. Morris GE, (2008) The Cajal body. Biochim Biophys Acta 1783: 2108-2115.
2. Matera AG, Izaguire-Sierra M, Praveen K, Rajendra TK, (2009) Nuclear bodies: random aggregates of sticky proteins or crucibles of macromolecular assembly? Dev Cell 17: 639-647.
3. Hebert MD, (2010) Phosphorylation and the Cajal body: modification in search of function. Arch Biochem Biophys 496: 69-76.
4. Beausoleil SA, Jedrychowski M, Schwartz D, Elias JE, Villen J, et al. (2004) Large-scale characterization of HeLa cell nuclear phosphoproteins. Proc Natl Acad Sci U S A 101: 12130-12135.
5. Dephoure N, Zhou C, Villen J, Beausoleil SA, Bakalarski CE, et al. (2008) A quantitative atlas of mitotic phosphorylation. Proc Natl Acad Sci U S A 105: 10762-10767.
6. Nousiainen M, Sillje HH, Sauer G, Nigg EA, Korner R, (2006) Phosphoproteome analysis of the human mitotic spindle. Proc Natl Acad Sci U S A 103: 5391-5396.
7. Olsen JV, Blagoev B, Gnad F, Macek B, Kumar C, et al. (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127: 635-648.
8. Olsen JV, Vermeulen M, Santamaria A, Kumar C, Miller ML, et al. (2010) Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci Signal 3: ra3.
9. Toyota CG, Davis MD, Cosman AM, Hebert MD, (2010) Coilin phosphorylation mediates interaction with SMN and SmB'. Chromosoma 119: 205-215.
10. Strzelecka M, Oates A, Neugebauer KM, (2010) Dynamic control of Cajal body number during zebrafish embyogenesis. Nucleus in press.
11. Liu JL, Wu Z, Nizami Z, Deryusheva S, Rajendra TK, et al. (2009) Coilin is essential for Cajal body organization in Drosophila melanogaster. Mol Biol Cell 20: 1661-1670.
12. Tucker KE, Berciano MT, Jacobs EY, LePage DF, Shpargel KB, et al. (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.
13. Walker MP, Tian L, Matera AG, (2009) Reduced viability, fertility and fecundity in mice lacking the cajal body marker protein, coilin. PLoS One 4: e6171.
14. Lemm I, Girard C, Kuhn AN, Watkins NJ, Schneider M, et al. (2006) Ongoing U snRNP biogenesis is required for the integrity of Cajal bodies. Mol Biol Cell 17: 3221-3231.
15. Whittom AA, Xu H, Hebert MD, (2008) Coilin levels and modifications influence artificial reporter splicing. Cell Mol Life Sci 65: 1256-1271.
16. Hearst SM, Gilder AS, Negi SS, Davis MD, George EM, et al. (2009) Cajal-body formation correlates with differential coilin phosphorylation in primary and transformed cell lines. J Cell Sci 122: 1872-1881.
17. 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.
18. Hebert MD, Matera AG, (2000) Self-association of coilin reveals a common theme in nuclear body localization. Mol Biol Cell 11: 4159-4171.
19. Shanbhag R, Kurabi A, Kwan JJ, Donaldson LW, (2010) Solution structure of the carboxy-terminal Tudor domain from human Coilin. FEBS Lett 584: 4351-4356.
20. Shababi M, Mattis VB, Lorson CL, (2010) Therapeutics that directly increase SMN expression to treat spinal muscular atrophy. Drug News Perspect 23: 475-482.
21. 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.
22. Hebert MD, Shpargel KB, Ospina JK, Tucker KE, Matera AG, (2002) Coilin methylation regulates nuclear body formation. Dev Cell 3: 329-337.
23. Boisvert FM, Cote J, Boulanger MC, Cleroux P, Bachand F, et al. (2002) Symmetrical dimethylarginine methylation is required for the localization of SMN in Cajal bodies and pre-mRNA splicing. J Cell Biol 159: 957-969.
24. Xu H, Pillai RS, Azzouz TN, Shpargel KB, Kambach C, et al. (2005) The C-terminal domain of coilin interacts with Sm proteins and U snRNPs. Chromosoma 114: 155-166.
25. Clelland AK, Kinnear NP, Oram L, Burza J, Sleeman JE, (2009) The SMN protein is a key regulator of nuclear architecture in differentiating neuroblastoma cells. Traffic 10: 1585-1598.
26. Tapia O, Bengoechea R, Berciano MT, Lafarga M, (2010) Nucleolar targeting of coilin is regulated by its hypomethylation state. Chromosoma 119: 527-540.
27. Velma V, Carrero ZI, Cosman AM, Hebert MD, (2010) Coilin interacts with Ku proteins and inhibits in vitro non-homologous DNA end joining. FEBS Lett 584: 4735-4739.
28. Gilder AS, Do PM, Carrero ZI, Cosman AM, Broome HJ, et al. (2011) Coilin participates in the suppression of RNA polymerase I in response to cisplatin-induced DNA damage. Mol Biol Cell 22: 1070-1079.
29. Morency E, Sabra M, Catez F, Texier P, Lomonte P, (2007) A novel cell response triggered by interphase centromere structural instability. J Cell Biol 177: 757-768.
30. Cioce M, Boulon S, Matera AG, Lamond AI, (2006) UV-induced fragmentation of Cajal bodies. J Cell Biol 175: 401-413.
31. Lam YW, Lyon CE, Lamond AI, (2002) Large-scale isolation of Cajal bodies from HeLa cells. Mol Biol Cell 13: 2461-2473.
32. Liu J, Hebert MD, Ye Y, Templeton DJ, Kung H, et al. (2000) Cell cycle-dependent localization of the CDK2-cyclin E complex in Cajal (coiled) bodies. J Cell Sci 113 (Pt 9): 1543-1552.
33. Lyon CE, Bohmann K, Sleeman J, Lamond AI, (1997) Inhibition of protein dephosphorylation results in the accumulation of splicing snRNPs and coiled bodies within the nucleolus. Exp Cell Res 230: 84-93.
34. Shpargel KB, Ospina JK, Tucker KE, Matera AG, Hebert MD, (2003) Control of Cajal body number is mediated by the coilin C-terminus. J Cell Sci 116: 303-312.
35. Walker MP, Rajendra TK, Saieva L, Fuentes JL, Pellizzoni L, et al. (2008) SMN complex localizes to the sarcomeric Z-disc and is a proteolytic target of calpain. Hum Mol Genet 17: 3399-3410.
36. Fuentes JL, Strayer MS, Matera AG, (2010) Molecular determinants of survival motor neuron (SMN) protein cleavage by the calcium-activated protease, calpain. PLoS One 5: e15769.
37. Sun J, Xu H, Subramony SH, Hebert MD, (2005) Interactions between Coilin and PIASy partially link Cajal bodies to PML bodies. J Cell Sci 118: 4995-5003.