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Molecular and Cellular Biology, December 2001, p. 8289-8300, Vol. 21, No. 24
0270-7306/01/$04.00+0 DOI: 10.1128/MCB.21.24.8289-8300.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
The Methylosome, a 20S Complex Containing JBP1 and
pICln, Produces Dimethylarginine-Modified Sm Proteins
Westley J.
Friesen,1
Sergey
Paushkin,1
Anastasia
Wyce,1
Severine
Massenet,1
G. Scott
Pesiridis,1
Gregory
Van
Duyne,1
Juri
Rappsilber,2
Matthias
Mann,2 and
Gideon
Dreyfuss1,*
Howard Hughes Medical Institute and
Department of Biochemistry and Biophysics, University of Pennsylvania
School of Medicine, Philadelphia, Pennsylvania
19104-6148,1 and Protein Interaction
Laboratory, CEBI, and Department of Biochemistry and Molecular
Biology, University of Southern Denmark, DK-5230 Odense M,
Denmark2
Received 24 July 2001/Returned for modification 10 September
2001/Accepted 13 September 2001
snRNPs, integral components of the pre-mRNA splicing machinery,
consist of seven Sm proteins which assemble in the cytoplasm as a ring
structure on the snRNAs U1, U2, U4, and U5. The survival motor
neuron (SMN) protein, the spinal muscular atrophy disease gene product,
is crucial for snRNP core particle assembly in vivo. SMN binds
preferentially and directly to the symmetrical dimethylarginine (sDMA)-modified arginine- and glycine-rich (RG-rich) domains of SmD1
and SmD3. We found that the unmodified, but not the sDMA-modified, RG
domains of SmD1 and SmD3 associate with a 20S methyltransferase complex, termed the methylosome, that contains the methyltransferase JBP1 and a JBP1-interacting protein, pICln. JBP1 binds SmD1 and SmD3
via their RG domains, while pICln binds the Sm domains. JBP1 produces
sDMAs in the RG domain-containing Sm proteins. We further demonstrate
the existence of a 6S complex that contains pICln, SmD1, and SmD3 but
not JBP1. SmD3 from the methylosome, but not that from the 6S complex,
can be transferred to the SMN complex in vitro. Together with previous
results, these data indicate that methylation of Sm proteins by the
methylosome directs Sm proteins to the SMN complex for assembly into
snRNP core particles and suggest that the methylosome can regulate
snRNP assembly.
*
Corresponding author. Mailing address: Howard Hughes
Medical Institute and Department of Biochemistry & Biophysics,
University of Pennsylvania School of Medicine, Philadelphia, PA
19104-6148. Phone: (215) 898-0398. Fax: (215) 573-2000. E-mail:
gdreyfuss{at}hhmi.upenn.edu.
Molecular and Cellular Biology, December 2001, p. 8289-8300, Vol. 21, No. 24
0270-7306/01/$04.00+0 DOI: 10.1128/MCB.21.24.8289-8300.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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-
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-
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[Full Text]
-
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[Abstract]
[Full Text]
-
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(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
[Abstract]
[Full Text]
-
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[Abstract]
[Full Text]
-
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[Abstract]
[Full Text]
-
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(2003). Epstein-Barr Virus Nuclear Antigen 2 Binds via Its Methylated Arginine-Glycine Repeat to the Survival Motor Neuron Protein. J. Virol.
77: 5008-5013
[Abstract]
[Full Text]
-
Cote, J., Boisvert, F.-M., Boulanger, M.-C., Bedford, M. T., Richard, S.
(2003). Sam68 RNA Binding Protein Is an In Vivo Substrate for Protein Arginine N-Methyltransferase 1. Mol. Biol. Cell
14: 274-287
[Abstract]
[Full Text]
-
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[Abstract]
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-
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(2002). ICP27 Interacts with the RNA Export Factor Aly/REF To Direct Herpes Simplex Virus Type 1 Intronless mRNAs to the TAP Export Pathway. J. Virol.
76: 12877-12889
[Abstract]
[Full Text]
-
Whitehead, S. E., Jones, K. W., Zhang, X., Cheng, X., Terns, R. M., Terns, M. P.
(2002). Determinants of the Interaction of the Spinal Muscular Atrophy Disease Protein SMN with the Dimethylarginine-modified Box H/ACA Small Nucleolar Ribonucleoprotein GAR1. J. Biol. Chem.
277: 48087-48093
[Abstract]
[Full Text]
-
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(2002). Essential Role for the SMN Complex in the Specificity of snRNP Assembly. Science
298: 1775-1779
[Abstract]
[Full Text]
-
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(2002). Lipopolysaccharide-induced Methylation of HuR, an mRNA-stabilizing Protein, by CARM1. J. Biol. Chem.
277: 44623-44630
[Abstract]
[Full Text]
-
Wang, Z., Moran, M. F.
(2002). Phospholipase C-{gamma}1: A Phospholipase and Guanine Nucleotide Exchange Factor. Mol. Interv.
2: 352-355
[Abstract]
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-
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(2002). The SMN Complex Is Associated with snRNPs throughout Their Cytoplasmic Assembly Pathway. Mol. Cell. Biol.
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-
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-
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-
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