A natural fast-cleaving branching ribozyme from the amoeboflagellate<i>Naegleria pringsheimi</i>

Tang, Yunjia; Nielsen, Hans Bruun; Johansen, Steinar

doi:10.4161/rna.8.6.16027

Cited by 10 publications

(10 citation statements)

References 23 publications

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“…S4). Analysis of an analogous interaction between L9 and the regulatory domain in the Naegleria LC ribozyme (17) corroborates these observations. The second tertiary interaction involves the DL2.1 and the L5 loops, which form three cis WC base pairs between residues 5′-A90UC-3′ from DL2.1 and 5′-G144AU-3′ from L5 (Figs.…”

Section: Resultssupporting

confidence: 65%

Speciation of a group I intron into a lariat capping ribozyme

Meyer

Nielsen

Oliéric

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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The lariat-capping (LC) ribozyme is a natural ribozyme isolated from eukaryotic microorganisms. Despite apparent structural similarity to group I introns, the LC ribozyme catalyzes cleavage by a 2′,5′ branching reaction, leaving the 3′ product with a 3-nt lariat cap that functionally substitutes for a conventional mRNA cap in the downstream pre-mRNA encoding a homing endonuclease. We describe the crystal structures of the precleavage and postcleavage LC ribozymes, which suggest that structural features inherited from group I ribozymes have undergone speciation due to profound changes in molecular selection pressure, ultimately giving rise to an original branching ribozyme family. The structures elucidate the role of key elements that regulate the activity of the LC ribozyme by conformational switching and suggest a mechanism by which the signal for branching is transmitted to the catalytic core. The structures also show how conserved interactions twist residues, forming the lariat to join chemical groups involved in branching.RNA structure | RNA catalysis | GIR1 | crystallography | SAXS V arious mechanisms critically regulate splicing, thus controlling the fate of host gene products. Most splicing that relies solely on autocatalytic RNA introns appears to be unregulated, but control can be achieved at the RNA level because the structural versatility of RNA allows for the fusing of functional modules that can work in concert (1). Examples of riboswitches adjoined to spliceosomal (2) or group I (3) introns illustrate this concept and suggest that uncharacterized splicing regulation mechanisms may exist.An elaborate example of RNA-regulated splicing is the group I twin-ribozyme introns found in the small subunit (SSU) ribosomal precursor in several protists (Fig. 1A). These twin-ribozyme introns are composed of a conventional group I splicing ribozyme (GIR2), into which is inserted a cassette composed of a branching ribozyme upstream from a homing endonuclease (HE) gene (4). The branching activity results in cleavage and concomitant formation of a 3-nt lariat capping the 5′ end of the HE pre-mRNA (Fig. 1B) (5), hence the name "lariat capping" (LC) ribozyme. The lariat cap appears to act as a substitute for a conventional mRNA m 7 G cap in a situation in which an mRNA is expressed from within a RNA polymerase I (polI) gene (6). The cross-talk between GIR2 and the LC ribozyme is supported by the existence of three distinct processing pathways of the rRNA precursor, depending on environmental conditions. Under favorable conditions, splicing by GIR2 takes place first, followed by branching by the LC ribozyme and further processing, and eventually translation of the HE mRNA (7,8). The transcriptional order of the ribozymes implies that the activity of the branching ribozyme is specifically repressed until splicing has taken place. Cellular stress conditions induce formation of full-length intron circles by a circularization pathway (9) that leaves the ribosomal exons unligated. Finally, starvation conditions induce bran...

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Section: Resultssupporting

confidence: 65%

Speciation of a group I intron into a lariat capping ribozyme

Meyer

Nielsen

Oliéric

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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“…These introns consist of a regular group I splicing ribozyme (GIR2) with an insertion in P2 or P6 that contains a HEG as well as a lariat capping ribozyme (LC ribozyme). Whereas GIR2 is responsible for intron forward and reverse splicing and intron RNA circularization [ 5 , 8 , 11 - 13 ], the LC ribozyme performs the 2′,5′ branching reaction at an internal intron site and is directly involved in 5′ capping of the HE mRNA, a prerequisite for intron mobility [ 14 - 17 ].…”

Section: Introductionmentioning

confidence: 99%

Molecular characterization of a new member of the lariat capping twin-ribozyme introns

et al. 2014

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BackgroundTwin-ribozyme introns represent a complex class of mobile group I introns that harbour a lariat capping (LC) ribozyme and a homing endonuclease gene embedded in a conventional self-splicing group I ribozyme (GIR2). Twin-ribozyme introns have so far been confined to nucleolar DNA in Naegleria amoeboflagellates and the myxomycete Didymium iridis.ResultsWe characterize structural organization, catalytic properties and molecular evolution of a new twin-ribozyme intron in Allovahlkampfia (Heterolobosea). The intron contains two ribozyme domains with different functions in ribosomal RNA splicing and homing endonuclease mRNA maturation. We found Allovahlkampfia GIR2 to be a typical group IC1 splicing ribozyme responsible for addition of the exogenous guanosine cofactor (exoG), exon ligation and circularization of intron RNA. The Allovahlkampfia LC ribozyme, by contrast, represents an efficient self-cleaving ribozyme that generates a small 2′,5′ lariat cap at the 5′ end of the homing endonuclease mRNA, and thus contributes to intron mobility.ConclusionsThe discovery of a twin-ribozyme intron in a member of Heterolobosea expands the distribution pattern of LC ribozymes. We identify a putative regulatory RNA element (AP2.1) in the Allovahlkampfia LC ribozyme that involves homing endonuclease mRNA coding sequences as an important structural component.

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“…GIR1 generates a 3-nucleotide lariat cap by joining the C residue at the internal processing site (IPS) and the U residue at the branch point (BP) by a 2′,5′ phosphodiester bond (Figure 5B) [68]. Similar lariat caps are generated by the Naegleria and Allovahlkampfia GIR1s [66,72]. …”

Section: Reviewmentioning

confidence: 99%

Nuclear group I introns in self-splicing and beyond

Hedberg

Johansen

2013

Mobile DNA

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Group I introns are a distinct class of RNA self-splicing introns with an ancient origin. All known group I introns present in eukaryote nuclei interrupt functional ribosomal RNA genes located in ribosomal DNA loci. The discovery of the Tetrahymena intron more than 30 years ago has been essential to our understanding of group I intron catalysis, higher-order RNA structure, and RNA folding, but other intron models have provided information about the biological role. Nuclear group I introns appear widespread among eukaryotic microorganisms, and the plasmodial slime molds (myxomycetes) contain an abundance of self-splicing introns. Here, we summarize the main conclusions from previous work on the Tetrahymena intron on RNA self-splicing catalysis as well as more recent work on myxomycete intron biology. Group I introns in myxomycetes that represent different evolutionary stages, biological roles, and functional settings are discussed.

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A natural fast-cleaving branching ribozyme from the amoeboflagellateNaegleria pringsheimi

Cited by 10 publications

References 23 publications

Speciation of a group I intron into a lariat capping ribozyme

Speciation of a group I intron into a lariat capping ribozyme

Molecular characterization of a new member of the lariat capping twin-ribozyme introns

Nuclear group I introns in self-splicing and beyond

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