Discovery of a splicing regulator required for cell cycle progression
In the G1 phase of the cell division cycle, eukaryotic cells prepare many of the resources necessary for a new round of growth including renewal of the transcriptional and protein synthetic capacities and building the machinery for chromosome replication. The function of G1 has an early evolutionary...
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Published in | PLoS genetics Vol. 9; no. 2; p. e1003305 |
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Main Authors | , , , , , , , , , |
Format | Journal Article |
Language | English |
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Public Library of Science
01.02.2013
Public Library of Science (PLoS) |
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Abstract | In the G1 phase of the cell division cycle, eukaryotic cells prepare many of the resources necessary for a new round of growth including renewal of the transcriptional and protein synthetic capacities and building the machinery for chromosome replication. The function of G1 has an early evolutionary origin and is preserved in single and multicellular organisms, although the regulatory mechanisms conducting G1 specific functions are only understood in a few model eukaryotes. Here we describe a new G1 mutant from an ancient family of apicomplexan protozoans. Toxoplasma gondii temperature-sensitive mutant 12-109C6 conditionally arrests in the G1 phase due to a single point mutation in a novel protein containing a single RNA-recognition-motif (TgRRM1). The resulting tyrosine to asparagine amino acid change in TgRRM1 causes severe temperature instability that generates an effective null phenotype for this protein when the mutant is shifted to the restrictive temperature. Orthologs of TgRRM1 are widely conserved in diverse eukaryote lineages, and the human counterpart (RBM42) can functionally replace the missing Toxoplasma factor. Transcriptome studies demonstrate that gene expression is downregulated in the mutant at the restrictive temperature due to a severe defect in splicing that affects both cell cycle and constitutively expressed mRNAs. The interaction of TgRRM1 with factors of the tri-SNP complex (U4/U6 & U5 snRNPs) indicate this factor may be required to assemble an active spliceosome. Thus, the TgRRM1 family of proteins is an unrecognized and evolutionarily conserved class of splicing regulators. This study demonstrates investigations into diverse unicellular eukaryotes, like the Apicomplexa, have the potential to yield new insights into important mechanisms conserved across modern eukaryotic kingdoms. |
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AbstractList | In the G1 phase of the cell division cycle, eukaryotic cells prepare many of the resources necessary for a new round of growth including renewal of the transcriptional and protein synthetic capacities and building the machinery for chromosome replication. The function of G1 has an early evolutionary origin and is preserved in single and multicellular organisms, although the regulatory mechanisms conducting G1 specific functions are only understood in a few model eukaryotes. Here we describe a new G1 mutant from an ancient family of apicomplexan protozoans. Toxoplasma gondii temperature-sensitive mutant 12-109C6 conditionally arrests in the G1 phase due to a single point mutation in a novel protein containing a single RNA-recognition-motif (TgRRM1). The resulting tyrosine to asparagine amino acid change in TgRRM1 causes severe temperature instability that generates an effective null phenotype for this protein when the mutant is shifted to the restrictive temperature. Orthologs of TgRRM1 are widely conserved in diverse eukaryote lineages, and the human counterpart (RBM42) can functionally replace the missing Toxoplasma factor. Transcriptome studies demonstrate that gene expression is downregulated in the mutant at the restrictive temperature due to a severe defect in splicing that affects both cell cycle and constitutively expressed mRNAs. The interaction of TgRRM1 with factors of the tri-SNP complex (U4/U6 & U5 snRNPs) indicate this factor may be required to assemble an active spliceosome. Thus, the TgRRM1 family of proteins is an unrecognized and evolutionarily conserved class of splicing regulators. This study demonstrates investigations into diverse unicellular eukaryotes, like the Apicomplexa, have the potential to yield new insights into important mechanisms conserved across modern eukaryotic kingdoms. In the G1 phase of the cell division cycle, eukaryotic cells prepare many of the resources necessary for a new round of growth including renewal of the transcriptional and protein synthetic capacities and building the machinery for chromosome replication. The function of G1 has an early evolutionary origin and is preserved in single and multicellular organisms, although the regulatory mechanisms conducting G1 specific functions are only understood in a few model eukaryotes. Here we describe a new G1 mutant from an ancient family of apicomplexan protozoans. Toxoplasma gondii temperature-sensitive mutant 12-109C6 conditionally arrests in the G1 phase due to a single point mutation in a novel protein containing a single RNA-recognition-motif (TgRRM1). The resulting tyrosine to asparagine amino acid change in TgRRM1 causes severe temperature instability that generates an effective null phenotype for this protein when the mutant is shifted to the restrictive temperature. Orthologs of TgRRM1 are widely conserved in diverse eukaryote lineages, and the human counterpart (RBM42) can functionally replace the missing Toxoplasma factor. Transcriptome studies demonstrate that gene expression is downregulated in the mutant at the restrictive temperature due to a severe defect in splicing that affects both cell cycle and constitutively expressed mRNAs. The interaction of TgRRM1 with factors of the tri-SNP complex (U4/U6 & U5 snRNPs) indicate this factor may be required to assemble an active spliceosome. Thus, the TgRRM1 family of proteins is an unrecognized and evolutionarily conserved class of splicing regulators. This study demonstrates investigations into diverse unicellular eukaryotes, like the Apicomplexa, have the potential to yield new insights into important mechanisms conserved across modern eukaryotic kingdoms. The study of eukaryotic cell division has overwhelmingly focused on cells from two branches of evolution, fungal and metazoan, with more distant eukaryotes rarely studied. One exception is apicomplexan pathogens where in the last two decades development of genetic models has been rapid. While not a perfect solution to fill the missing evolutionary diversity, Apicomplexans represent one of the oldest eukaryotic lineages possibly pre-dating the divergence of plant and animal kingdoms. A key to uncovering novel and conserved cell cycle mechanisms in these protists was the development of forward genetic approaches that permit unbiased discovery of essential growth factors. The apicomplexan, Toxoplasma has provided the best resource so far with ∼60,000 chemical mutants yielding a collection of 165 temperature-sensitive isolates that arrest in all phases of the parasite cell cycle. Efforts to identify the defective genes in this model are providing insights into the regulatory factors possibly active in the original eukaryote cell cycle, like the mRNA splicing factor discovered in this study. In the G1 phase of the cell division cycle, eukaryotic cells prepare many of the resources necessary for a new round of growth including renewal of the transcriptional and protein synthetic capacities and building the machinery for chromosome replication. The function of G1 has an early evolutionary origin and is preserved in single and multicellular organisms, although the regulatory mechanisms conducting G1 specific functions are only understood in a few model eukaryotes. Here we describe a new G1 mutant from an ancient family of apicomplexan protozoans. Toxoplasma gondii temperature-sensitive mutant 12-109C6 conditionally arrests in the G1 phase due to a single point mutation in a novel protein containing a single RNA-recognition-motif (TgRRM1). The resulting tyrosine to asparagine amino acid change in TgRRM1 causes severe temperature instability that generates an effective null phenotype for this protein when the mutant is shifted to the restrictive temperature. Orthologs of TgRRM1 are widely conserved in diverse eukaryote lineages, and the human counterpart (RBM42) can functionally replace the missing Toxoplasma factor. Transcriptome studies demonstrate that gene expression is downregulated in the mutant at the restrictive temperature due to a severe defect in splicing that affects both cell cycle and constitutively expressed mRNAs. The interaction of TgRRM1 with factors of the tri-SNP complex (U4/U6 & U5 snRNPs) indicate this factor may be required to assemble an active spliceosome. Thus, the TgRRM1 family of proteins is an unrecognized and evolutionarily conserved class of splicing regulators. This study demonstrates investigations into diverse unicellular eukaryotes, like the Apicomplexa, have the potential to yield new insights into important mechanisms conserved across modern eukaryotic kingdoms. |
Audience | Academic |
Author | Suvorova, Elena S Ting, Li-Min White, Michael W Balu, Bharath Markillie, Meng L Weiss, Louis M Kratzer, Stella Croken, Matthew Conde de Felipe, Magnolia Kim, Kami |
AuthorAffiliation | 6 Fundamental and Computational Sciences, Pacific Northwest National Laboratory, Richland, Washington, United States of America 4 Department of Animal Pathology, University of Las Palmas de Gran Canaria, Arucas, Las Palmas de Gran Canaria, Spain 5 Tropical Disease Research Program, Center for Infectious Disease and Biodefense Research, SRI International, Harrisonburg, Virginia, United States of America Centre National de la Recherche Scientifique, France 1 Departments of Molecular Medicine and Global Health and the Florida Center for Drug Discovery and Innovation, University of South Florida, Tampa, Florida, United States of America 2 Department of Medicine, Albert Einstein College of Medicine, Bronx, New York, United States of America 3 Department of Microbiology and Immunology, Albert Einstein College of Medicine, Bronx, New York, United States of America |
AuthorAffiliation_xml | – name: 6 Fundamental and Computational Sciences, Pacific Northwest National Laboratory, Richland, Washington, United States of America – name: 1 Departments of Molecular Medicine and Global Health and the Florida Center for Drug Discovery and Innovation, University of South Florida, Tampa, Florida, United States of America – name: 4 Department of Animal Pathology, University of Las Palmas de Gran Canaria, Arucas, Las Palmas de Gran Canaria, Spain – name: Centre National de la Recherche Scientifique, France – name: 2 Department of Medicine, Albert Einstein College of Medicine, Bronx, New York, United States of America – name: 3 Department of Microbiology and Immunology, Albert Einstein College of Medicine, Bronx, New York, United States of America – name: 5 Tropical Disease Research Program, Center for Infectious Disease and Biodefense Research, SRI International, Harrisonburg, Virginia, United States of America |
Author_xml | – sequence: 1 givenname: Elena S surname: Suvorova fullname: Suvorova, Elena S organization: Departments of Molecular Medicine and Global Health and the Florida Center for Drug Discovery and Innovation, University of South Florida, Tampa, Florida, United States of America – sequence: 2 givenname: Matthew surname: Croken fullname: Croken, Matthew – sequence: 3 givenname: Stella surname: Kratzer fullname: Kratzer, Stella – sequence: 4 givenname: Li-Min surname: Ting fullname: Ting, Li-Min – sequence: 5 givenname: Magnolia surname: Conde de Felipe fullname: Conde de Felipe, Magnolia – sequence: 6 givenname: Bharath surname: Balu fullname: Balu, Bharath – sequence: 7 givenname: Meng L surname: Markillie fullname: Markillie, Meng L – sequence: 8 givenname: Louis M surname: Weiss fullname: Weiss, Louis M – sequence: 9 givenname: Kami surname: Kim fullname: Kim, Kami – sequence: 10 givenname: Michael W surname: White fullname: White, Michael W |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/23437009$$D View this record in MEDLINE/PubMed |
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Copyright | COPYRIGHT 2013 Public Library of Science 2013 Suvorova et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Suvorova ES, Croken M, Kratzer S, Ting L-M, de Felipe MC, et al. (2013) Discovery of a Splicing Regulator Required for Cell Cycle Progression. PLoS Genet 9(2): e1003305. doi:10.1371/journal.pgen.1003305 2013 Suvorova et al 2013 Suvorova et al |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Conceived and designed the experiments: ESS MC MCdF LMW KK MWW. Performed the experiments: ESS MC SK MCdF BB L-MT MLM. Analyzed the data: ESS MC BB LMW KK MWW. Wrote the paper: ESS MC KK MWW. The authors have declared that no competing interests exist. |
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Snippet | In the G1 phase of the cell division cycle, eukaryotic cells prepare many of the resources necessary for a new round of growth including renewal of the... In the G1 phase of the cell division cycle, eukaryotic cells prepare many of the resources necessary for a new round of growth including renewal of the... |
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SubjectTerms | Alternative Splicing - genetics Biology Cell cycle Cell Cycle - genetics Chromosomes Colleges & universities Conserved Sequence - genetics Eukaryotes G1 Phase - genetics Gene Expression Regulation Genetic aspects Genetic engineering Genetics Humans Medicine Mutation Nucleotide Motifs - genetics Parasites Physiological aspects Proteins RNA, Messenger - genetics RNA, Messenger - metabolism RNA-Binding Proteins - genetics RNA-Binding Proteins - metabolism Sequence Homology, Amino Acid Temperature Toxoplasma Toxoplasma - genetics Toxoplasma - metabolism |
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Title | Discovery of a splicing regulator required for cell cycle progression |
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