Fibrillarin Ribonuclease Activity is Dependent on the GAR Domain and Modulated by Phospholipids

Fibrillarin is a highly conserved nucleolar methyltransferase responsible for ribosomal RNA methylation across evolution from Archaea to humans. It has been reported that fibrillarin is involved in the methylation of histone H2A in nucleoli and other processes, including viral progression, cellular...

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Main Authors: Francisco Guillen-Chable, Ulises Rodríguez Corona, Alejandro Pereira-Santana, Andrea Bayona, Luis Carlos Rodríguez-Zapata, Cecilia Aquino, Lenka Šebestová, Nicolas Vitale, Pavel Hozak, Enrique Castano
Format: Article
Language:English
Published: MDPI AG 2020-05-01
Series:Cells
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Online Access:https://www.mdpi.com/2073-4409/9/5/1143
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author Francisco Guillen-Chable
Ulises Rodríguez Corona
Alejandro Pereira-Santana
Andrea Bayona
Luis Carlos Rodríguez-Zapata
Cecilia Aquino
Lenka Šebestová
Nicolas Vitale
Pavel Hozak
Enrique Castano
author_facet Francisco Guillen-Chable
Ulises Rodríguez Corona
Alejandro Pereira-Santana
Andrea Bayona
Luis Carlos Rodríguez-Zapata
Cecilia Aquino
Lenka Šebestová
Nicolas Vitale
Pavel Hozak
Enrique Castano
author_sort Francisco Guillen-Chable
collection DOAJ
description Fibrillarin is a highly conserved nucleolar methyltransferase responsible for ribosomal RNA methylation across evolution from Archaea to humans. It has been reported that fibrillarin is involved in the methylation of histone H2A in nucleoli and other processes, including viral progression, cellular stress, nuclear shape, and cell cycle progression. We show that fibrillarin has an additional activity as a ribonuclease. The activity is affected by phosphoinositides and phosphatidic acid and insensitive to ribonuclease inhibitors. Furthermore, the presence of phosphatidic acid releases the fibrillarin-U3 snoRNA complex. We show that the ribonuclease activity localizes to the GAR (glycine/arginine-rich) domain conserved in a small group of RNA interacting proteins. The introduction of the GAR domain occurred in evolution in the transition from archaea to eukaryotic cells. The interaction of this domain with phospholipids may allow a phase separation of this protein in nucleoli.
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spelling doaj.art-dd24a231afec44fc982564ad426cb6072023-11-19T23:36:07ZengMDPI AGCells2073-44092020-05-0195114310.3390/cells9051143Fibrillarin Ribonuclease Activity is Dependent on the GAR Domain and Modulated by PhospholipidsFrancisco Guillen-Chable0Ulises Rodríguez Corona1Alejandro Pereira-Santana2Andrea Bayona3Luis Carlos Rodríguez-Zapata4Cecilia Aquino5Lenka Šebestová6Nicolas Vitale7Pavel Hozak8Enrique Castano9Biochemistry and Molecular Plant Biology Department, Centro de Investigación Científica de Yucatán, A.C. Calle 43 No. 130, Colonia Chuburná de Hidalgo, Mérida C.P. 97200, Yucatán, MexicoBiochemistry and Molecular Plant Biology Department, Centro de Investigación Científica de Yucatán, A.C. Calle 43 No. 130, Colonia Chuburná de Hidalgo, Mérida C.P. 97200, Yucatán, MexicoIndustrial Biotechnology Department, Centro de Investigación y Asistencia en Tecnología y Diseño del Estado de Jalisco, A.C., Camino Arenero 1227, el Bajio, Zapopan C.P. 45019, Jalisco, MexicoBiochemistry and Molecular Plant Biology Department, Centro de Investigación Científica de Yucatán, A.C. Calle 43 No. 130, Colonia Chuburná de Hidalgo, Mérida C.P. 97200, Yucatán, MexicoBiotechnology Department, Centro de Investigación Científica de Yucatán, A.C. Calle 43 No. 130, Colonia Chuburná de Hidalgo, Mérida C.P. 97200, Yucatan, MexicoBiochemistry and Molecular Plant Biology Department, Centro de Investigación Científica de Yucatán, A.C. Calle 43 No. 130, Colonia Chuburná de Hidalgo, Mérida C.P. 97200, Yucatán, MexicoDepartment of Biology of the Cell Nucleus, Institute of Molecular Genetics of the CAS, v.v.i., Videnska 1083, 142 20 Prague, Czech RepublicInstitute of Celullar and Integrative Neuroscience (INCI), UPR-3212 The French National Centre for Scientific Research & University of Strasbourg, 67000 Strasbourg, FranceDepartment of Biology of the Cell Nucleus, Institute of Molecular Genetics of the CAS, v.v.i., Videnska 1083, 142 20 Prague, Czech RepublicBiochemistry and Molecular Plant Biology Department, Centro de Investigación Científica de Yucatán, A.C. Calle 43 No. 130, Colonia Chuburná de Hidalgo, Mérida C.P. 97200, Yucatán, MexicoFibrillarin is a highly conserved nucleolar methyltransferase responsible for ribosomal RNA methylation across evolution from Archaea to humans. It has been reported that fibrillarin is involved in the methylation of histone H2A in nucleoli and other processes, including viral progression, cellular stress, nuclear shape, and cell cycle progression. We show that fibrillarin has an additional activity as a ribonuclease. The activity is affected by phosphoinositides and phosphatidic acid and insensitive to ribonuclease inhibitors. Furthermore, the presence of phosphatidic acid releases the fibrillarin-U3 snoRNA complex. We show that the ribonuclease activity localizes to the GAR (glycine/arginine-rich) domain conserved in a small group of RNA interacting proteins. The introduction of the GAR domain occurred in evolution in the transition from archaea to eukaryotic cells. The interaction of this domain with phospholipids may allow a phase separation of this protein in nucleoli.https://www.mdpi.com/2073-4409/9/5/1143nucleolusribonucleolar particlerRNAfibrillarinphosphoinositidesviral progression
spellingShingle Francisco Guillen-Chable
Ulises Rodríguez Corona
Alejandro Pereira-Santana
Andrea Bayona
Luis Carlos Rodríguez-Zapata
Cecilia Aquino
Lenka Šebestová
Nicolas Vitale
Pavel Hozak
Enrique Castano
Fibrillarin Ribonuclease Activity is Dependent on the GAR Domain and Modulated by Phospholipids
Cells
nucleolus
ribonucleolar particle
rRNA
fibrillarin
phosphoinositides
viral progression
title Fibrillarin Ribonuclease Activity is Dependent on the GAR Domain and Modulated by Phospholipids
title_full Fibrillarin Ribonuclease Activity is Dependent on the GAR Domain and Modulated by Phospholipids
title_fullStr Fibrillarin Ribonuclease Activity is Dependent on the GAR Domain and Modulated by Phospholipids
title_full_unstemmed Fibrillarin Ribonuclease Activity is Dependent on the GAR Domain and Modulated by Phospholipids
title_short Fibrillarin Ribonuclease Activity is Dependent on the GAR Domain and Modulated by Phospholipids
title_sort fibrillarin ribonuclease activity is dependent on the gar domain and modulated by phospholipids
topic nucleolus
ribonucleolar particle
rRNA
fibrillarin
phosphoinositides
viral progression
url https://www.mdpi.com/2073-4409/9/5/1143
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