XB-ART-53675
RNA
2017 Aug 01;238:1188-1199. doi: 10.1261/rna.061515.117.
Show Gene links
Show Anatomy links
Expression of distinct maternal and somatic 5.8S, 18S, and 28S rRNA types during zebrafish development.
Locati MD
,
Pagano JFB
,
Girard G
,
Ensink WA
,
van Olst M
,
van Leeuwen S
,
Nehrdich U
,
Spaink HP
,
Rauwerda H
,
Jonker MJ
,
Dekker RJ
,
Breit TM
.
???displayArticle.abstract???
There is mounting evidence that the ribosome is not a static translation machinery, but a cell-specific, adaptive system. Ribosomal variations have mostly been studied at the protein level, even though the essential transcriptional functions are primarily performed by rRNAs. At the RNA level, oocyte-specific 5S rRNAs are long known for Xenopus. Recently, we described for zebrafish a similar system in which the sole maternal-type 5S rRNA present in eggs is replaced completely during embryonic development by a somatic-type. Here, we report the discovery of an analogous system for the 45S rDNA elements: 5.8S, 18S, and 28S. The maternal-type 5.8S, 18S, and 28S rRNA sequences differ substantially from those of the somatic-type, plus the maternal-type rRNAs are also replaced by the somatic-type rRNAs during embryogenesis. We discuss the structural and functional implications of the observed sequence differences with respect to the translational functions of the 5.8S, 18S, and 28S rRNA elements. Finally, in silico evidence suggests that expansion segments (ES) in 18S rRNA, previously implicated in ribosome-mRNA interaction, may have a preference for interacting with specific mRNA genes. Taken together, our findings indicate that two distinct types of ribosomes exist in zebrafish during development, each likely conducting the translation machinery in a unique way.
???displayArticle.pubmedLink??? 28500251
???displayArticle.pmcLink??? PMC5513064
???displayArticle.link??? RNA
References [+] :
Aitken,
A mechanistic overview of translation initiation in eukaryotes.
2012, Pubmed
Aitken, A mechanistic overview of translation initiation in eukaryotes. 2012, Pubmed
Alkemar, Secondary structure of two regions in expansion segments ES3 and ES6 with the potential of forming a tertiary interaction in eukaryotic 40S ribosomal subunits. 2004, Pubmed
Allison, Differential binding of oocyte-type and somatic-type 5S rRNA to TFIIIA and ribosomal protein L5 in Xenopus oocytes: specialization for storage versus mobilization. 1995, Pubmed , Xenbase
Anger, Structures of the human and Drosophila 80S ribosome. 2013, Pubmed
Arnheim, Heterogeneity of the ribosomal genes in mice and men. 1977, Pubmed
Barendt, Broad-specificity mRNA-rRNA complementarity in efficient protein translation. 2012, Pubmed
Barna, The ribosome prophecy. 2015, Pubmed
Beringer, Modulating the activity of the peptidyl transferase center of the ribosome. 2008, Pubmed
Brown, A tribute to the Xenopus laevis oocyte and egg. 2004, Pubmed , Xenbase
BROWN, ABSENCE OF RIBOSOMAL RNA SYNTHESIS IN THE ANUCLEOLATE MUTANT OF XENOPUS LAEVIS. 1964, Pubmed , Xenbase
BROWN, Biochemistry of amphibian development. I. Ribosome and protein synthesis in early development of Rana pipiens. 1962, Pubmed
BROWN, RNA SYNTHESIS DURING THE DEVELOPMENT OF XENOPUS LAEVIS, THE SOUTH AFRICAN CLAWED TOAD. 1964, Pubmed , Xenbase
Campos, Histones: annotating chromatin. 2009, Pubmed
Cannone, The comparative RNA web (CRW) site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs. 2002, Pubmed
Chirkova, The role of the universally conserved A2450-C2063 base pair in the ribosomal peptidyl transferase center. 2010, Pubmed
Ciganda, Eukaryotic 5S rRNA biogenesis. 2011, Pubmed
Côté, Role of the ITS2-proximal stem and evidence for indirect recognition of processing sites in pre-rRNA processing in yeast. 2001, Pubmed
Doris, Universal and domain-specific sequences in 23S-28S ribosomal RNA identified by computational phylogenetics. 2015, Pubmed
Gornung, 5S ribosomal RNA genes in six species of Mediterranean grey mullets: genomic organization and phylogenetic inference. 2007, Pubmed
Graifer, The central part of the 5.8 S rRNA is differently arranged in programmed and free human ribosomes. 2005, Pubmed
Gulen, Ribosomal small subunit domains radiate from a central core. 2016, Pubmed
Gunderson, Structurally distinct, stage-specific ribosomes occur in Plasmodium. 1987, Pubmed
Henras, An overview of pre-ribosomal RNA processing in eukaryotes. 2015, Pubmed
Howe, The zebrafish reference genome sequence and its relationship to the human genome. 2013, Pubmed
Ihara, Expression of variant ribosomal RNA genes in mouse oocytes and preimplantation embryos. 2011, Pubmed
Jemiolo, Point mutations in the 3' minor domain of 16S rRNA of E.coli. 1985, Pubmed
Keller, 5.8S-28S rRNA interaction and HMM-based ITS2 annotation. 2009, Pubmed
Kimmel, Stages of embryonic development of the zebrafish. 1995, Pubmed , Xenbase
Komiya, Differentiation of oocyte- and somatic-type 5S rRNAs in animals. 1986, Pubmed
Kondrashov, Ribosome-mediated specificity in Hox mRNA translation and vertebrate tissue patterning. 2011, Pubmed
Korn, Transcription of Xenopus 5S ribosomal RNA genes. 1982, Pubmed , Xenbase
Krogh, Profiling of 2'-O-Me in human rRNA reveals a subset of fractionally modified positions and provides evidence for ribosome heterogeneity. 2016, Pubmed
Kuo, Human ribosomal RNA variants from a single individual and their expression in different tissues. 1996, Pubmed
Langmead, Fast gapped-read alignment with Bowtie 2. 2012, Pubmed
Leffers, The sequence of 28S ribosomal RNA varies within and between human cell lines. 1993, Pubmed
Li, The Sequence Alignment/Map format and SAMtools. 2009, Pubmed
Locati, Linking maternal and somatic 5S rRNA types with different sequence-specific non-LTR retrotransposons. 2017, Pubmed
Long, Mutations in 23S rRNA at the peptidyl transferase center and their relationship to linezolid binding and cross-resistance. 2010, Pubmed
Long, Single 23S rRNA mutations at the ribosomal peptidyl transferase centre confer resistance to valnemulin and other antibiotics in Mycobacterium smegmatis by perturbation of the drug binding pocket. 2009, Pubmed
Martin, Ribosomal 18S rRNA base pairs with mRNA during eukaryotic translation initiation. 2016, Pubmed
Martins, Dynamics of 5S rDNA in the tilapia (Oreochromis niloticus) genome: repeat units, inverted sequences, pseudogenes and chromosome loci. 2002, Pubmed
Mauro, The ribosome filter redux. 2007, Pubmed
Mauro, The ribosome filter hypothesis. 2002, Pubmed
Mauro, Translation regulation by ribosomes: Increased complexity and expanded scope. 2016, Pubmed
McCutchan, Primary sequences of two small subunit ribosomal RNA genes from Plasmodium falciparum. 1988, Pubmed
McStay, Nucleolar organizer regions: genomic 'dark matter' requiring illumination. 2016, Pubmed
Michot, Comparisons of large subunit rRNAs reveal some eukaryote-specific elements of secondary structure. 1987, Pubmed
Moore, The involvement of RNA in ribosome function. 2002, Pubmed
Moore, The structural basis of large ribosomal subunit function. 2003, Pubmed
Newport, A major developmental transition in early Xenopus embryos: II. Control of the onset of transcription. 1982, Pubmed , Xenbase
Noller, RNA structure: reading the ribosome. 2005, Pubmed
Pánek, An evolutionary conserved pattern of 18S rRNA sequence complementarity to mRNA 5' UTRs and its implications for eukaryotic gene translation regulation. 2013, Pubmed
Peculis, The structure of the ITS2-proximal stem is required for pre-rRNA processing in yeast. 1998, Pubmed
Peterson, Characterization of two xenopus somatic 5S DNAs and one minor oocyte-specific 5S DNA. 1980, Pubmed , Xenbase
Petrov, Secondary structure and domain architecture of the 23S and 5S rRNAs. 2013, Pubmed
Petrov, Secondary structures of rRNAs from all three domains of life. 2014, Pubmed
Polacek, The ribosomal peptidyl transferase center: structure, function, evolution, inhibition. 2005, Pubmed
Preiss, All Ribosomes Are Created Equal. Really? 2016, Pubmed
Qi, Regulation of Plasmodium yoelii oocyst development by strain- and stage-specific small-subunit rRNA. 2015, Pubmed
Ramesh, Eukaryote-specific rRNA expansion segments function in ribosome biogenesis. 2016, Pubmed
Rauwerda, Mother-Specific Signature in the Maternal Transcriptome Composition of Mature, Unfertilized Zebrafish Eggs. 2016, Pubmed
Rochaix, Ribosomal RNA gene amplification by rolling circles. 1974, Pubmed , Xenbase
Rogers, Structural features of the large subunit rRNA expressed in Plasmodium falciparum sporozoites that distinguish it from the asexually expressed subunit rRNA. 1996, Pubmed
Sakai, Human ribosomal RNA gene cluster: identification of the proximal end containing a novel tandem repeat sequence. 1995, Pubmed
Schluenzen, Structure of functionally activated small ribosomal subunit at 3.3 angstroms resolution. 2000, Pubmed
Shi, Translating the genome in time and space: specialized ribosomes, RNA regulons, and RNA-binding proteins. 2015, Pubmed
Shi, Functional role of the sarcin-ricin loop of the 23S rRNA in the elongation cycle of protein synthesis. 2012, Pubmed
Stoykova, Different rates of synthesis and turnover of ribosomal RNA in rat brain and liver. 1983, Pubmed
Szewczak, The conformation of the sarcin/ricin loop from 28S ribosomal RNA. 1993, Pubmed
Thomas, Persistence of oocyte amplified rDNA during early development of Xenopus laevis eggs. 1977, Pubmed , Xenbase
Tranque, rRNA complementarity within mRNAs: a possible basis for mRNA-ribosome interactions and translational control. 1998, Pubmed
Treangen, Repetitive DNA and next-generation sequencing: computational challenges and solutions. 2011, Pubmed
Uchiumi, A functional site of the GTPase-associated center within 28S ribosomal RNA probed with an anti-RNA autoantibody. 1994, Pubmed
Uchiumi, Direct evidence for interaction of the conserved GTPase domain within 28 S RNA with mammalian ribosomal acidic phosphoproteins and L12. 1992, Pubmed
van Spaendonk, Functional equivalence of structurally distinct ribosomes in the malaria parasite, Plasmodium berghei. 2001, Pubmed
Venema, Ribosome synthesis in Saccharomyces cerevisiae. 1999, Pubmed
Verrier, Complementarity between the mRNA 5' untranslated region and 18S ribosomal RNA can inhibit translation. 2000, Pubmed
Voorhees, Structural basis of the translational elongation cycle. 2013, Pubmed
Waters, Developmental regulation of stage-specific ribosome populations in Plasmodium. 1989, Pubmed
Wegnez, Sequence heterogeneity of 5 S RNA in Xenopus laevis. 1972, Pubmed , Xenbase
Wellauer, Arrangement of length heterogeneity in repeating units of amplified and chromosomal ribosomal DNA from Xenopus laevis. 1976, Pubmed , Xenbase
Wilson, The structure and function of the eukaryotic ribosome. 2012, Pubmed
Wormington, Onset of 5 S RNA gene regulation during Xenopus embryogenesis. 1983, Pubmed , Xenbase
Xu, Mutations in the GTPase center of Escherichia coli 23S rRNA indicate release factor 2-interactive sites. 2002, Pubmed
Xue, Specialized ribosomes: a new frontier in gene regulation and organismal biology. 2012, Pubmed
Yadav, The Modular Adaptive Ribosome. 2016, Pubmed
Yang, 23S rRNA nucleotides in the peptidyl transferase center are essential for tryptophanase operon induction. 2009, Pubmed