Protein arginine methylation modulates light-harvesting antenna translation in Chlamydomonas reinhardtii

Blifernez O, Wobbe L, Niehaus K, Kruse O (2011)
The Plant Journal 65(1): 119-130.

Download
Es wurde kein Volltext hochgeladen. Nur Publikationsnachweis!
Zeitschriftenaufsatz | Veröffentlicht | Englisch
Abstract / Bemerkung
P>Methylation of protein arginines represents an important post-translational modification mechanism, which has so far primarily been characterized in mammalian cells. In this work, we successfully identified and characterized arginine methylation as a crucial type of post-translational modification in the activity regulation of the cytosolic translation repressor protein NAB1 in the plant model organism Chlamydomonas reinhardtii. NAB1 represses the cytosolic translation of light-harvesting protein encoding mRNAs by sequestration into translationally silent messenger ribonucleoprotein complexes (mRNPs). Protein arginine methylation of NAB1 could be demonstrated by PRMT1 catalyzed methylation of recombinant NAB1 in vitro, and by immunodetection of methylated NAB1 arginines in vivo. Mass spectrometric analyses of NAB1 purified from C. reinhardtii revealed the asymmetric dimethylation of Arg90 and Arg92 within GAR motif I. Inhibition of arginine methylation by either adenosine-2'-3'-dialdehyde (AdOx) or 7,7'-carbonylbis(azanediyl)bis(4-hydroxynaphthalene-2-sulfonic acid) sodium salt hydrate (AMI-1) caused a dark-green phenotype characterized by the increased accumulation of light-harvesting complex proteins, and indicating a reduced translation repressor activity of NAB1. The extent of NAB1 arginine methylation depends on the growth conditions, with phototrophic growth causing a high methylation state and heterotrophic growth resulting in lowered methylation of the protein. In addition, we could show that NAB1 activity regulation by arginine methylation operates independently from cysteine-based redox control, which has previously been shown to control the activity of NAB1.
Erscheinungsjahr
Zeitschriftentitel
The Plant Journal
Band
65
Ausgabe
1
Seite(n)
119-130
ISSN
PUB-ID

Zitieren

Blifernez O, Wobbe L, Niehaus K, Kruse O. Protein arginine methylation modulates light-harvesting antenna translation in Chlamydomonas reinhardtii. The Plant Journal. 2011;65(1):119-130.
Blifernez, O., Wobbe, L., Niehaus, K., & Kruse, O. (2011). Protein arginine methylation modulates light-harvesting antenna translation in Chlamydomonas reinhardtii. The Plant Journal, 65(1), 119-130. doi:10.1111/j.1365-313X.2010.04406.x
Blifernez, O., Wobbe, L., Niehaus, K., and Kruse, O. (2011). Protein arginine methylation modulates light-harvesting antenna translation in Chlamydomonas reinhardtii. The Plant Journal 65, 119-130.
Blifernez, O., et al., 2011. Protein arginine methylation modulates light-harvesting antenna translation in Chlamydomonas reinhardtii. The Plant Journal, 65(1), p 119-130.
O. Blifernez, et al., “Protein arginine methylation modulates light-harvesting antenna translation in Chlamydomonas reinhardtii”, The Plant Journal, vol. 65, 2011, pp. 119-130.
Blifernez, O., Wobbe, L., Niehaus, K., Kruse, O.: Protein arginine methylation modulates light-harvesting antenna translation in Chlamydomonas reinhardtii. The Plant Journal. 65, 119-130 (2011).
Blifernez, Olga, Wobbe, Lutz, Niehaus, Karsten, and Kruse, Olaf. “Protein arginine methylation modulates light-harvesting antenna translation in Chlamydomonas reinhardtii”. The Plant Journal 65.1 (2011): 119-130.

9 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Metabolic responses to ethanol and butanol in Chlamydomonas reinhardtii.
Jiang Y, Xiao P, Shao Q, Qin H, Hu Z, Lei A, Wang J., Biotechnol Biofuels 10(), 2017
PMID: 29075323
A Light Switch Based on Protein S-Nitrosylation Fine-Tunes Photosynthetic Light Harvesting in Chlamydomonas.
Berger H, De Mia M, Morisse S, Marchand CH, Lemaire SD, Wobbe L, Kruse O., Plant Physiol 171(2), 2016
PMID: 27208221
Proteomic Analysis of a Fraction with Intact Eyespots of Chlamydomonas reinhardtii and Assignment of Protein Methylation.
Eitzinger N, Wagner V, Weisheit W, Geimer S, Boness D, Kreimer G, Mittag M., Front Plant Sci 6(), 2015
PMID: 26697039
Regulation and dynamics of the light-harvesting system.
Rochaix JD., Annu Rev Plant Biol 65(), 2014
PMID: 24471838
Integration of carbon assimilation modes with photosynthetic light capture in the green alga Chlamydomonas reinhardtii.
Berger H, Blifernez-Klassen O, Ballottari M, Bassi R, Wobbe L, Kruse O., Mol Plant 7(10), 2014
PMID: 25038233
Arginine methylation of hnRNP A2 does not directly govern its subcellular localization.
Friend LR, Landsberg MJ, Nouwens AS, Wei Y, Rothnagel JA, Smith R., PLoS One 8(9), 2013
PMID: 24098712
Cellulose degradation and assimilation by the unicellular phototrophic eukaryote Chlamydomonas reinhardtii.
Blifernez-Klassen O, Klassen V, Doebbe A, Kersting K, Grimm P, Wobbe L, Kruse O., Nat Commun 3(), 2012
PMID: 23169055
Construction and evaluation of a whole genome microarray of Chlamydomonas reinhardtii.
Toepel J, Albaum SP, Arvidsson S, Goesmann A, la Russa M, Rogge K, Kruse O., BMC Genomics 12(), 2011
PMID: 22118351

60 References

Daten bereitgestellt von Europe PubMed Central.


Atkinson, 1977
Protein arginine methylation in mammals: who, what, and why.
Bedford MT, Clarke SG., Mol. Cell 33(1), 2009
PMID: 19150423
Arginine methylation an emerging regulator of protein function.
Bedford MT, Richard S., Mol. Cell 18(3), 2005
PMID: 15866169
Arginines of the RGG box regulate FMRP association with polyribosomes and mRNA.
Blackwell E, Zhang X, Ceman S., Hum. Mol. Genet. 19(7), 2010
PMID: 20064924
Immunoprecipitation.
Bonifacino JS, Dell'Angelica EC, Springer TA., Curr Protoc Protein Sci Chapter 9(), 2001
PMID: 18429217
A mass spectrometry based method for distinguishing between symmetrically and asymmetrically dimethylated arginine residues.
Brame CJ, Moran MF, McBroom-Cerajewski LD., Rapid Commun. Mass Spectrom. 18(8), 2004
PMID: 15095356
MeMo: a web tool for prediction of protein methylation modifications.
Chen H, Xue Y, Huang N, Yao X, Sun Z., Nucleic Acids Res. 34(Web Server issue), 2006
PMID: 16845004
Small molecule regulators of protein arginine methyltransferases.
Cheng D, Yadav N, King RW, Swanson MS, Weinstein EJ, Bedford MT., J. Biol. Chem. 279(23), 2004
PMID: 15056663
Methylation regulates the intracellular protein-protein and protein-RNA interactions of FMRP.
Dolzhanskaya N, Merz G, Aletta JM, Denman RB., J. Cell. Sci. 119(Pt 9), 2006
PMID: 16636078
A major light-harvesting polypeptide of photosystem II functions in thermal dissipation.
Elrad D, Niyogi KK, Grossman AR., Plant Cell 14(8), 2002
PMID: 12172023
Protein arginine methyltransferases: guardians of the Arg?
Fackelmayer FO., Trends Biochem. Sci. 30(12), 2005
PMID: 16257219
Inhibitory study of protein arginine methyltransferase 1 using a fluorescent approach.
Feng Y, Xie N, Wu J, Yang C, Zheng YG., Biochem. Biophys. Res. Commun. 379(2), 2008
PMID: 19121292
RNA and protein interactions modulated by protein arginine methylation.
Gary JD, Clarke S., Prog. Nucleic Acid Res. Mol. Biol. 61(), 1998
PMID: 9752719
Fragmentation pathways of N(G)-methylated and unmodified arginine residues in peptides studied by ESI-MS/MS and MALDI-MS.
Gehrig PM, Hunziker PE, Zahariev S, Pongor S., J. Am. Soc. Mass Spectrom. 15(2), 2004
PMID: 14766281
Structure and functions of nucleolin.
Ginisty H, Sicard H, Roger B, Bouvet P., J. Cell. Sci. 112 ( Pt 6)(), 1999
PMID: 10036227

Harris, 2009
Protein-RNA interactions: a structural analysis.
Jones S, Daley DT, Luscombe NM, Berman HM, Thornton JM., Nucleic Acids Res. 29(4), 2001
PMID: 11160927
Isolation of state transition mutants of Chlamydomonas reinhardtii by fuorescence video imaging
Kruse, Photosynth. Res. 61(), 1999
In vivo and in vitro arginine methylation of RNA-binding proteins.
Liu Q, Dreyfuss G., Mol. Cell. Biol. 15(5), 1995
PMID: 7739561
RNA-binding strategies common to cold-shock domain- and RNA recognition motif-containing proteins.
Manival X, Ghisolfi-Nieto L, Joseph G, Bouvet P, Erard M., Nucleic Acids Res. 29(11), 2001
PMID: 11376140
Amino acid sequence of UP1, an hnRNP-derived single-stranded nucleic acid binding protein from calf thymus.
Merrill BM, Lopresti MB, Stone KL, Williams KR., Int. J. Pept. Protein Res. 29(1), 1987
PMID: 3032834
Redox-sensitive GFP in Arabidopsis thaliana is a quantitative biosensor for the redox potential of the cellular glutathione redox buffer.
Meyer AJ, Brach T, Marty L, Kreye S, Rouhier N, Jacquot JP, Hell R., Plant J. 52(5), 2007
PMID: 17892447
Nab1, an RNA-binding protein involved in the light-regulated differential expression of the light-harvesting antenna of Chlamydomonas reinhardtii
Mussgnug, Plant Cell 173(), 2005
The mRNA-binding protein YB-1 (p50) prevents association of the eukaryotic initiation factor eIF4G with mRNA and inhibits protein synthesis at the initiation stage.
Nekrasov MP, Ivshina MP, Chernov KG, Kovrigina EA, Evdokimova VM, Thomas AA, Hershey JW, Ovchinnikov LP., J. Biol. Chem. 278(16), 2003
PMID: 12582179
Regulation of flowering time by the protein arginine methyltransferase AtPRMT10.
Niu L, Lu F, Pei Y, Liu C, Cao X., EMBO Rep. 8(12), 2007
PMID: 18007657
Identifying and quantifying in vivo methylation sites by heavy methyl SILAC.
Ong SE, Mittler G, Mann M., Nat. Methods 1(2), 2004
PMID: 15782174
Monitoring disulfide bond formation in the eukaryotic cytosol.
Ostergaard H, Tachibana C, Winther JR., J. Cell Biol. 166(3), 2004
PMID: 15277542
Protein arginine methylation: Cellular functions and methods of analysis.
Pahlich S, Zakaryan RP, Gehring H., Biochim. Biophys. Acta 1764(12), 2006
PMID: 17010682
PRMT11: a new Arabidopsis MBD7 protein partner with arginine methyltransferase activity.
Scebba F, De Bastiani M, Bernacchia G, Andreucci A, Galli A, Pitto L., Plant J. 52(2), 2007
PMID: 17711414
A protein methylation pathway in Chlamydomonas flagella is active during flagellar resorption.
Schneider MJ, Ulland M, Sloboda RD., Mol. Biol. Cell 19(10), 2008
PMID: 18701702
Protein methylation in full length Chlamydomonas flagella.
Sloboda RD, Howard L., Cell Motil. Cytoskeleton 66(8), 2009
PMID: 19472373
Proteomics of Chlamydomonas reinhardtii light-harvesting proteins.
Stauber EJ, Fink A, Markert C, Kruse O, Johanningmeier U, Hippler M., Eukaryotic Cell 2(5), 2003
PMID: 14555480
Identification and characterization of the methyl arginines in the fragile X mental retardation protein Fmrp.
Stetler A, Winograd C, Sayegh J, Cheever A, Patton E, Zhang X, Clarke S, Ceman S., Hum. Mol. Genet. 15(1), 2005
PMID: 16319129
PRMT1 is the predominant type I protein arginine methyltransferase in mammalian cells.
Tang J, Frankel A, Cook RJ, Kim S, Paik WK, Williams KR, Clarke S, Herschman HR., J. Biol. Chem. 275(11), 2000
PMID: 10713084
Environmentally modulated phosphoproteome of photosynthetic membranes in the green alga Chlamydomonas reinhardtii.
Turkina MV, Kargul J, Blanco-Rivero A, Villarejo A, Barber J, Vener AV., Mol. Cell Proteomics 5(8), 2006
PMID: 16670252
SKB1-mediated symmetric dimethylation of histone H4R3 controls flowering time in Arabidopsis.
Wang X, Zhang Y, Ma Q, Zhang Z, Xue Y, Bao S, Chong K., EMBO J. 26(7), 2007
PMID: 17363895
High-throughput mass spectrometric discovery of protein post-translational modifications.
Wilkins MR, Gasteiger E, Gooley AA, Herbert BR, Molloy MP, Binz PA, Ou K, Sanchez JC, Bairoch A, Williams KL, Hochstrasser DF., J. Mol. Biol. 289(3), 1999
PMID: 10356335
Cysteine modification of a specific repressor protein controls the translational status of nucleus-encoded LHCII mRNAs in Chlamydomonas.
Wobbe L, Blifernez O, Schwarz C, Mussgnug JH, Nickelsen J, Kruse O., Proc. Natl. Acad. Sci. U.S.A. 106(32), 2009
PMID: 19666611
I-TASSER server for protein 3D structure prediction.
Zhang Y., BMC Bioinformatics 9(), 2008
PMID: 18215316

Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®

Quellen

PMID: 21175895
PubMed | Europe PMC

Suchen in

Google Scholar