-
Články
- Časopisy
- Kurzy
- Témy
- Kongresy
- Videa
- Podcasty
Rrp12 and the Exportin Crm1 Participate in Late Assembly Events in the Nucleolus during 40S Ribosomal Subunit Biogenesis
During the synthesis of small ribosomal subunits in eukaryotes, the pre-40S particles formed in the nucleolus are rapidly transported to the cytoplasm. The mechanisms involved in the nuclear export of these particles and its coordination with other steps of the 40S synthesis pathway are mostly unknown. In this work we studied the function of Rrp12, the only major non-ribosomal factor of nuclear pre-40S particles that does not remain stably associated to them during maturation in the cytoplasm. We demonstrate that Rrp12 is required for the exit of pre-40S particles to the cytoplasm. Remarkably, we also found that Rrp12, together with the Crm1 exportin, participates in processes that occur in early pre-ribosomes in the nucleolus, including the processing of the pre-rRNA and the elimination of processing byproducts. Thus, Rrp12 and Crm1 participate in maturation steps that take place upstream of nuclear export. Our results indicate that, in the 40S subunit synthesis pathway, the completion of early pre-40S particle assembly, the initiation of byproduct degradation and the priming for nuclear export occur in an integrated manner in nucleolar pre-ribosomes.
Vyšlo v časopise: Rrp12 and the Exportin Crm1 Participate in Late Assembly Events in the Nucleolus during 40S Ribosomal Subunit Biogenesis. PLoS Genet 10(12): e32767. doi:10.1371/journal.pgen.1004836
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004836Souhrn
During the synthesis of small ribosomal subunits in eukaryotes, the pre-40S particles formed in the nucleolus are rapidly transported to the cytoplasm. The mechanisms involved in the nuclear export of these particles and its coordination with other steps of the 40S synthesis pathway are mostly unknown. In this work we studied the function of Rrp12, the only major non-ribosomal factor of nuclear pre-40S particles that does not remain stably associated to them during maturation in the cytoplasm. We demonstrate that Rrp12 is required for the exit of pre-40S particles to the cytoplasm. Remarkably, we also found that Rrp12, together with the Crm1 exportin, participates in processes that occur in early pre-ribosomes in the nucleolus, including the processing of the pre-rRNA and the elimination of processing byproducts. Thus, Rrp12 and Crm1 participate in maturation steps that take place upstream of nuclear export. Our results indicate that, in the 40S subunit synthesis pathway, the completion of early pre-40S particle assembly, the initiation of byproduct degradation and the priming for nuclear export occur in an integrated manner in nucleolar pre-ribosomes.
Zdroje
1. VenemaJ, TollerveyD (1999) Ribosome synthesis in Saccharomyces cerevisiae. Annu Rev Genet 33 : 261–311.
2. WoolfordJLJr, BasergaSJ (2013) Ribosome biogenesis in the yeast Saccharomyces cerevisiae. Genetics 195 : 643–681.
3. GrandiP, RybinV, BasslerJ, PetfalskiE, StraussD, et al. (2002) 90S pre-ribosomes include the 35S pre-rRNA, the U3 snoRNP, and 40S subunit processing factors but predominantly lack 60S synthesis factors. Mol Cell 10 : 105–115.
4. Perez-FernandezJ, RomanA, De Las RivasJ, BusteloXR, DosilM (2007) The 90S preribosome is a multimodular structure that is assembled through a hierarchical mechanism. Mol Cell Biol 27 : 5414–5429.
5. GallagherJE, DunbarDA, GrannemanS, MitchellBM, OsheimY, et al. (2004) RNA polymerase I transcription and pre-rRNA processing are linked by specific SSU processome components. Genes Dev 18 : 2506–2517.
6. Perez-FernandezJ, Martin-MarcosP, DosilM (2011) Elucidation of the assembly events required for the recruitment of Utp20, Imp4 and Bms1 onto nascent pre-ribosomes. Nucleic Acids Res 39 : 17.
7. DragonF, GallagherJE, Compagnone-PostPA, MitchellBM, PorwancherKA, et al. (2002) A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis. Nature 417 : 967–970.
8. PhippsKR, CharetteJM, BasergaSJ (2011) The SSU Processome in Ribosome Biogenesis - Progress and Prospects. WIREs RNA 2 : 1–21.
9. ThomsonE, Ferreira-CercaS, HurtE (2013) Eukaryotic ribosome biogenesis at a glance. J Cell Sci 126 : 4815–4821.
10. KresslerD, HurtE, BasslerJ (2010) Driving ribosome assembly. Biochim Biophys Acta 1803 : 673–683.
11. HenrasAK, SoudetJ, GerusM, LebaronS, Caizergues-FerrerM, et al. (2008) The post-transcriptional steps of eukaryotic ribosome biogenesis. Cell Mol Life Sci 65 : 2334–2359.
12. TschochnerH, HurtE (2003) Pre-ribosomes on the road from the nucleolus to the cytoplasm. Trends Cell Biol 13 : 255–263.
13. KarbsteinK (2011) Inside the 40S ribosome assembly machinery. Curr Opin Chem Biol 15 : 657–663.
14. LebaronS, SchneiderC, van NuesRW, SwiatkowskaA, WalshD, et al. (2012) Proofreading of pre-40S ribosome maturation by a translation initiation factor and 60S subunits. Nat Struct Mol Biol 19 : 744–753.
15. StrunkBS, NovakMN, YoungCL, KarbsteinK (2012) A translation-like cycle is a quality control checkpoint for maturing 40S ribosome subunits. Cell 150 : 111–121.
16. PertschyB, SchneiderC, GnadigM, SchaferT, TollerveyD, et al. (2009) RNA helicase Prp43 and its co-factor Pfa1 promote 20 to 18 S rRNA processing catalyzed by the endonuclease Nob1. J Biol Chem 284 : 35079–35091.
17. KarbsteinK (2013) Quality control mechanisms during ribosome maturation. Trends Cell Biol 23 : 242–250.
18. SchaferT, StraussD, PetfalskiE, TollerveyD, HurtE (2003) The path from nucleolar 90S to cytoplasmic 40S pre-ribosomes. Embo J 22 : 1370–1380.
19. MoyTI, SilverPA (2002) Requirements for the nuclear export of the small ribosomal subunit. J Cell Sci 115 : 2985–2995.
20. SchaferT, MacoB, PetfalskiE, TollerveyD, BottcherB, et al. (2006) Hrr25-dependent phosphorylation state regulates organization of the pre-40S subunit. Nature 441 : 651–655.
21. MoyTI, SilverPA (1999) Nuclear export of the small ribosomal subunit requires the ran-GTPase cycle and certain nucleoporins. Genes Dev 13 : 2118–2133.
22. OeffingerM, DlakicM, TollerveyD (2004) A pre-ribosome-associated HEAT-repeat protein is required for export of both ribosomal subunits. Genes Dev 18 : 196–209.
23. DosilM (2011) Ribosome synthesis-unrelated functions of the preribosomal factor rrp12 in cell cycle progression and the DNA damage response. Mol Cell Biol 31 : 2422–2438.
24. CombsDJ, NagelRJ, AresMJr, StevensSW (2006) Prp43p is a DEAH-box spliceosome disassembly factor essential for ribosome biogenesis. Mol Cell Biol 26 : 523–534.
25. LeedsNB, SmallEC, HileySL, HughesTR, StaleyJP (2006) The splicing factor Prp43p, a DEAH box ATPase, functions in ribosome biogenesis. Mol Cell Biol 26 : 513–522.
26. LebaronS, FromentC, Fromont-RacineM, RainJC, MonsarratB, et al. (2005) The splicing ATPase prp43p is a component of multiple preribosomal particles. Mol Cell Biol 25 : 9269–9282.
27. FazaMB, ChangY, OcchipintiL, KemmlerS, PanseVG (2012) Role of Mex67-Mtr2 in the nuclear export of 40S pre-ribosomes. PLoS Genet 8: e1002915.
28. VanrobaysE, GelugneJP, GleizesPE, Caizergues-FerrerM (2003) Late cytoplasmic maturation of the small ribosomal subunit requires RIO proteins in Saccharomyces cerevisiae. Mol Cell Biol 23 : 2083–2095.
29. VanrobaysE, GelugneJP, Caizergues-FerrerM, LafontaineDL (2004) Dim2p, a KH-domain protein required for small ribosomal subunit synthesis. Rna 10 : 645–656.
30. ChenW, BucariaJ, BandDA, SuttonA, SternglanzR (2003) Enp1, a yeast protein associated with U3 and U14 snoRNAs, is required for pre-rRNA processing and 40S subunit synthesis. Nucleic Acids Res 31 : 690–699.
31. SeiserRM, SundbergAE, WollamBJ, Zobel-ThroppP, BaldwinK, et al. (2006) Ltv1 is required for efficient nuclear export of the ribosomal small subunit in Saccharomyces cerevisiae. Genetics 174 : 679–691.
32. LafontaineD, VandenhauteJ, TollerveyD (1995) The 18S rRNA dimethylase Dim1p is required for pre-ribosomal RNA processing in yeast. Genes Dev 9 : 2470–2481.
33. DezC, DlakicM, TollerveyD (2007) Roles of the HEAT repeat proteins Utp10 and Utp20 in 40S ribosome maturation. Rna 13 : 1516–1527.
34. BillyE, WegierskiT, NasrF, FilipowiczW (2000) Rcl1p, the yeast protein similar to the RNA 3′-phosphate cyclase, associates with U3 snoRNP and is required for 18S rRNA biogenesis. Embo J 19 : 2115–2126.
35. WoollsHA, LamannaAC, KarbsteinK (2011) Roles of Dim2 in ribosome assembly. J Biol Chem 286 : 2578–2586.
36. SenapinS, Clark-WalkerGD, ChenXJ, SeraphinB, DaugeronMC (2003) RRP20, a component of the 90S preribosome, is required for pre-18S rRNA processing in Saccharomyces cerevisiae. Nucleic Acids Res 31 : 2524–2533.
37. SchneiderC, KudlaG, WlotzkaW, TuckA, TollerveyD (2012) Transcriptome-wide analysis of exosome targets. Mol Cell 48 : 422–433.
38. SchneiderC, LeungE, BrownJ, TollerveyD (2009) The N-terminal PIN domain of the exosome subunit Rrp44 harbors endonuclease activity and tethers Rrp44 to the yeast core exosome. Nucleic Acids Res 37 : 1127–1140.
39. de la CruzJ, KresslerD, TollerveyD, LinderP (1998) Dob1p (Mtr4p) is a putative ATP-dependent RNA helicase required for the 3′ end formation of 5.8S rRNA in Saccharomyces cerevisiae. Embo J 17 : 1128–1140.
40. AllmangC, MitchellP, PetfalskiE, TollerveyD (2000) Degradation of ribosomal RNA precursors by the exosome. Nucleic Acids Res 28 : 1684–1691.
41. NevilleM, RosbashM (1999) The NES-Crm1p export pathway is not a major mRNA export route in Saccharomyces cerevisiae. Embo J 18 : 3746–3756.
42. LebaronS, PapinC, CapeyrouR, ChenYL, FromentC, et al. (2009) The ATPase and helicase activities of Prp43p are stimulated by the G-patch protein Pfa1p during yeast ribosome biogenesis. Embo J 28 : 3808–3819.
43. BoulonS, VerheggenC, JadyBE, GirardC, PesciaC, et al. (2004) PHAX and CRM1 are required sequentially to transport U3 snoRNA to nucleoli. Mol Cell 16 : 777–787.
44. StrubBR, EswaraMB, PierceJB, MangrooD (2007) Utp8p is a nucleolar tRNA-binding protein that forms a complex with components of the nuclear tRNA export machinery in Saccharomyces cerevisiae. Mol Biol Cell 18 : 3845–3859.
45. WangW, BudhuA, ForguesM, WangXW (2005) Temporal and spatial control of nucleophosmin by the Ran-Crm1 complex in centrosome duplication. Nat Cell Biol 7 : 823–830.
46. Pradet-BaladeB, GirardC, BoulonS, PaulC, AzzagK, et al. (2011) CRM1 controls the composition of nucleoplasmic pre-snoRNA complexes to licence them for nucleolar transport. Embo J 30 : 2205–2218.
47. SuzukiN, NoguchiE, NakashimaN, OkiM, OhbaT, et al. (2001) The Saccharomyces cerevisiae small GTPase, Gsp1p/Ran, is involved in 3′ processing of 7S-to-5.8S rRNA and in degradation of the excised 5′-A0 fragment of 35S pre-rRNA, both of which are carried out by the exosome. Genetics 158 : 613–625.
48. TafforeauL, ZorbasC, LanghendriesJL, MullineuxST, StamatopoulouV, et al. (2013) The complexity of human ribosome biogenesis revealed by systematic nucleolar screening of Pre-rRNA processing factors. Mol Cell 51 : 539–551.
49. WildT, HorvathP, WylerE, WidmannB, BadertscherL, et al. (2010) A protein inventory of human ribosome biogenesis reveals an essential function of exportin 5 in 60S subunit export. PLoS Biol 8: e1000522.
50. Leger-SilvestreI, MilkereitP, Ferreira-CercaS, SaveanuC, RousselleJC, et al. (2004) The ribosomal protein Rps15p is required for nuclear exit of the 40S subunit precursors in yeast. Embo J 23 : 2336–2347.
51. LongtineMS, McKenzieA3rd, DemariniDJ, ShahNG, WachA, et al. (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14 : 953–961.
52. Ausubel FM, Brent R., Kingston R E., Moore D D., Seidman J G., et al.. (1994) Current Protocols in Molecular Biology. New York: John Wiley & Sons, Inc.
53. DosilM, BusteloXR (2004) Functional characterization of Pwp2, a WD family protein essential for the assembly of the 90 S pre-ribosomal particle. J Biol Chem 279 : 37385–37397.
54. GadalO, StraussD, KesslJ, TrumpowerB, TollerveyD, et al. (2001) Nuclear export of 60s ribosomal subunits depends on Xpo1p and requires a nuclear export sequence-containing factor, Nmd3p, that associates with the large subunit protein Rpl10p. Mol Cell Biol 21 : 3405–3415.
Štítky
Genetika Reprodukčná medicína
Článek Large-scale Metabolomic Profiling Identifies Novel Biomarkers for Incident Coronary Heart DiseaseČlánek Notch Signaling Mediates the Age-Associated Decrease in Adhesion of Germline Stem Cells to the NicheČlánek Phosphorylation of Mitochondrial Polyubiquitin by PINK1 Promotes Parkin Mitochondrial TetheringČlánek Natural Variation Is Associated With Genome-Wide Methylation Changes and Temperature SeasonalityČlánek Overlapping and Non-overlapping Functions of Condensins I and II in Neural Stem Cell DivisionsČlánek Unisexual Reproduction Drives Meiotic Recombination and Phenotypic and Karyotypic Plasticity inČlánek Tetraspanin (TSP-17) Protects Dopaminergic Neurons against 6-OHDA-Induced Neurodegeneration inČlánek ABA-Mediated ROS in Mitochondria Regulate Root Meristem Activity by Controlling Expression inČlánek Mutations in Global Regulators Lead to Metabolic Selection during Adaptation to Complex EnvironmentsČlánek The Evolution of Sex Ratio Distorter Suppression Affects a 25 cM Genomic Region in the Butterfly
Článok vyšiel v časopisePLOS Genetics
Najčítanejšie tento týždeň
2014 Číslo 12- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
-
Všetky články tohto čísla
- Stratification by Smoking Status Reveals an Association of Genotype with Body Mass Index in Never Smokers
- Genome Wide Meta-analysis Highlights the Role of Genetic Variation in in the Regulation of Circulating Serum Chemerin
- Occupancy of Mitochondrial Single-Stranded DNA Binding Protein Supports the Strand Displacement Mode of DNA Replication
- Distinct Genealogies for Plasmids and Chromosome
- Large-scale Metabolomic Profiling Identifies Novel Biomarkers for Incident Coronary Heart Disease
- Non-coding RNAs Prevent the Binding of the MSL-complex to Heterochromatic Regions
- Plasmid Flux in ST131 Sublineages, Analyzed by Plasmid Constellation Network (PLACNET), a New Method for Plasmid Reconstruction from Whole Genome Sequences
- Epigenome-Guided Analysis of the Transcriptome of Plaque Macrophages during Atherosclerosis Regression Reveals Activation of the Wnt Signaling Pathway
- The Inventiveness of Nature: An Interview with Werner Arber
- Mediation Analysis Demonstrates That -eQTLs Are Often Explained by -Mediation: A Genome-Wide Analysis among 1,800 South Asians
- Generation of Antigenic Diversity in by Structured Rearrangement of Genes During Mitosis
- A Massively Parallel Pipeline to Clone DNA Variants and Examine Molecular Phenotypes of Human Disease Mutations
- Genetic Analysis of the Cardiac Methylome at Single Nucleotide Resolution in a Model of Human Cardiovascular Disease
- Genetic Analysis of Circadian Responses to Low Frequency Electromagnetic Fields in
- The Dissection of Meiotic Chromosome Movement in Mice Using an Electroporation Technique
- Altered Chromatin Occupancy of Master Regulators Underlies Evolutionary Divergence in the Transcriptional Landscape of Erythroid Differentiation
- Syd/JIP3 and JNK Signaling Are Required for Myonuclear Positioning and Muscle Function
- Notch Signaling Mediates the Age-Associated Decrease in Adhesion of Germline Stem Cells to the Niche
- Mutation of Leads to Blurred Tonotopic Organization of Central Auditory Circuits in Mice
- The IKAROS Interaction with a Complex Including Chromatin Remodeling and Transcription Elongation Activities Is Required for Hematopoiesis
- RAN-Binding Protein 9 is Involved in Alternative Splicing and is Critical for Male Germ Cell Development and Male Fertility
- Enhanced Longevity by Ibuprofen, Conserved in Multiple Species, Occurs in Yeast through Inhibition of Tryptophan Import
- Phosphorylation of Mitochondrial Polyubiquitin by PINK1 Promotes Parkin Mitochondrial Tethering
- Recurrent Loss of Specific Introns during Angiosperm Evolution
- Natural Variation Is Associated With Genome-Wide Methylation Changes and Temperature Seasonality
- SEEDSTICK is a Master Regulator of Development and Metabolism in the Arabidopsis Seed Coat
- Overlapping and Non-overlapping Functions of Condensins I and II in Neural Stem Cell Divisions
- Unisexual Reproduction Drives Meiotic Recombination and Phenotypic and Karyotypic Plasticity in
- Tetraspanin (TSP-17) Protects Dopaminergic Neurons against 6-OHDA-Induced Neurodegeneration in
- ABA-Mediated ROS in Mitochondria Regulate Root Meristem Activity by Controlling Expression in
- Mutations in Global Regulators Lead to Metabolic Selection during Adaptation to Complex Environments
- Global Analysis of Photosynthesis Transcriptional Regulatory Networks
- Mucolipin Co-deficiency Causes Accelerated Endolysosomal Vacuolation of Enterocytes and Failure-to-Thrive from Birth to Weaning
- Controlling Pre-leukemic Thymocyte Self-Renewal
- How Malaria Parasites Avoid Running Out of Ammo
- Echoes of the Past: Hereditarianism and
- Deep Reads: Strands in the History of Molecular Genetics
- Keep on Laying Eggs Mama, RNAi My Reproductive Aging Blues Away
- Analysis of a Plant Complex Resistance Gene Locus Underlying Immune-Related Hybrid Incompatibility and Its Occurrence in Nature
- Epistatic Adaptive Evolution of Human Color Vision
- Increased and Imbalanced dNTP Pools Symmetrically Promote Both Leading and Lagging Strand Replication Infidelity
- Genetic Basis of Haloperidol Resistance in Is Complex and Dose Dependent
- Genome-Wide Analysis of DNA Methylation Dynamics during Early Human Development
- Interaction between Conjugative and Retrotransposable Elements in Horizontal Gene Transfer
- The Evolution of Sex Ratio Distorter Suppression Affects a 25 cM Genomic Region in the Butterfly
- is Required for Adult Maintenance of Dopaminergic Neurons in the Ventral Substantia Nigra
- PRL1, an RNA-Binding Protein, Positively Regulates the Accumulation of miRNAs and siRNAs in Arabidopsis
- Genetic Control of Contagious Asexuality in the Pea Aphid
- Early Mesozoic Coexistence of Amniotes and Hepadnaviridae
- Local and Systemic Regulation of Plant Root System Architecture and Symbiotic Nodulation by a Receptor-Like Kinase
- Gene Pathways That Delay Reproductive Senescence
- The Evolution of Fungal Metabolic Pathways
- Maf1 Is a Novel Target of PTEN and PI3K Signaling That Negatively Regulates Oncogenesis and Lipid Metabolism
- Formation of Linear Amplicons with Inverted Duplications in Requires the MRE11 Nuclease
- Identification of Rare Causal Variants in Sequence-Based Studies: Methods and Applications to , a Gene Involved in Cohen Syndrome and Autism
- Rrp12 and the Exportin Crm1 Participate in Late Assembly Events in the Nucleolus during 40S Ribosomal Subunit Biogenesis
- The Mutations in the ATP-Binding Groove of the Rad3/XPD Helicase Lead to -Cockayne Syndrome-Like Phenotypes
- Topoisomerase I Plays a Critical Role in Suppressing Genome Instability at a Highly Transcribed G-Quadruplex-Forming Sequence
- A Cbx8-Containing Polycomb Complex Facilitates the Transition to Gene Activation during ES Cell Differentiation
- Transcriptional Frameshifting Rescues Type VI Secretion by the Production of Two Length Variants from the Prematurely Interrupted Gene
- Association Mapping across Numerous Traits Reveals Patterns of Functional Variation in Maize
- Genome-Wide Analysis of -Regulated and Phased Small RNAs Underscores the Importance of the ta-siRNA Pathway to Maize Development
- Dissemination of Cephalosporin Resistance Genes between Strains from Farm Animals and Humans by Specific Plasmid Lineages
- The Tau Tubulin Kinases TTBK1/2 Promote Accumulation of Pathological TDP-43
- Germline Signals Deploy NHR-49 to Modulate Fatty-Acid β-Oxidation and Desaturation in Somatic Tissues of
- Microevolution of in Macrophages Restores Filamentation in a Nonfilamentous Mutant
- Vangl2-Regulated Polarisation of Second Heart Field-Derived Cells Is Required for Outflow Tract Lengthening during Cardiac Development
- Chondrocytes Transdifferentiate into Osteoblasts in Endochondral Bone during Development, Postnatal Growth and Fracture Healing in Mice
- A ABC Transporter Regulates Lifespan
- RA and FGF Signalling Are Required in the Zebrafish Otic Vesicle to Pattern and Maintain Ventral Otic Identities
- , and Reprogram Thymocytes into Self-Renewing Cells
- The miR9863 Family Regulates Distinct Alleles in Barley to Attenuate NLR Receptor-Triggered Disease Resistance and Cell-Death Signaling
- Detection of Pleiotropy through a Phenome-Wide Association Study (PheWAS) of Epidemiologic Data as Part of the Environmental Architecture for Genes Linked to Environment (EAGLE) Study
- Extensive Copy-Number Variation of Young Genes across Stickleback Populations
- The and Genetic Modules Interact to Regulate Ciliogenesis and Ciliary Microtubule Patterning in
- Analysis of the Genome, Transcriptome and Secretome Provides Insight into Its Pioneer Colonization Strategies of Wood
- PLOS Genetics
- Archív čísel
- Aktuálne číslo
- Informácie o časopise
Najčítanejšie v tomto čísle- Tetraspanin (TSP-17) Protects Dopaminergic Neurons against 6-OHDA-Induced Neurodegeneration in
- Maf1 Is a Novel Target of PTEN and PI3K Signaling That Negatively Regulates Oncogenesis and Lipid Metabolism
- The IKAROS Interaction with a Complex Including Chromatin Remodeling and Transcription Elongation Activities Is Required for Hematopoiesis
- Echoes of the Past: Hereditarianism and
Prihlásenie#ADS_BOTTOM_SCRIPTS#Zabudnuté hesloZadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.
- Časopisy