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Release factor

Release factors are specialized proteins that recognize stop codons (UAA, UAG, and UGA) in messenger RNA during the termination phase of protein synthesis on the ribosome, thereby triggering the hydrolysis of the ester bond between the completed polypeptide chain and the peptidyl-tRNA to release the nascent protein. These factors structurally mimic transfer RNAs (tRNAs) by spanning the ribosome's decoding center and peptidyl transferase center, with a conserved GGQ motif in their catalytic domain facilitating the hydrolytic reaction. Release factors are classified into two main types: class I factors, which directly recognize stop codons and catalyze peptide release, and class II factors, which are GTPases that promote the dissociation and recycling of class I factors from the ribosome post-termination. In prokaryotes, such as , there are two class I release factors—RF1, which decodes UAA and UAG stop codons, and RF2, which decodes UAA and UGA—along with the class II factor RF3, which accelerates the release and of RF1 and RF2 without directly participating in codon . In eukaryotes, a single omnipotent class I release factor, eRF1, recognizes all three stop codons, partnering with the eRF3 to ensure efficient termination and ribosomal . Beyond canonical termination, release factors contribute to translational by promoting the dissociation of stalled or mismatched ribosomal complexes, thereby preventing the production of aberrant proteins and maintaining cellular . Structural studies, including cryo-electron , have revealed dynamic conformational changes in release factors upon ribosomal binding, transitioning from a compact to an extended state within milliseconds to align their functional domains for precise stop-codon decoding and catalysis.

Overview

Definition and Role

Release factors (RFs) are specialized proteins essential for the termination of protein synthesis in all domains of life. They recognize the stop codons—UAA (), UAG (amber), and UGA (opal)—in (mRNA) when these codons occupy the ribosomal A-site during the phase of . Upon recognition, RFs trigger the of the ester bond linking the completed polypeptide to the peptidyl-tRNA in the ribosomal , leading to the release of the nascent protein and subsequent of the ribosomal subunits from the mRNA. Structurally, RFs mimic the shape of (tRNA) molecules, allowing them to bind the ribosomal A-site without an anticodon loop, thereby ensuring precise termination without the incorporation of additional . This tRNA mimicry enables RFs to decode the stop codons directly through specific structural domains that interact with the codon and , positioning the conserved GGQ motif to facilitate peptidyl-tRNA . RFs are classified into two main types based on their functions. Class 1 RFs, such as RF1 and RF2 in prokaryotes or eRF1 in eukaryotes and , directly recognize stop codons and catalyze the reaction. In contrast, class 2 RFs, including RF3 in prokaryotes and eRF3 in eukaryotes, act as that do not recognize codons but instead promote the recycling of class 1 RFs from the after termination, enhancing the efficiency of the process. The stop codons UAA, UAG, and UGA are nearly universal signals for translation termination across bacteria, archaea, and eukaryotes, reflecting the conserved nature of the genetic code. However, exceptions occur in certain organelles, such as mitochondria and chloroplasts, where codon reassignments can alter stop codon usage—for instance, UGA encoding tryptophan instead of termination in many mitochondrial genomes.

Historical Discovery

The discovery of release factors began in the mid-1960s with studies on suppressor tRNAs, which provided early evidence that stop codons function as termination signals rather than encoding specific amino acids. In 1965, Sydney Brenner and colleagues identified amber (UAG) mutations in bacteriophage T4, where suppressor strains harboring mutated tRNAs with altered anticodons could read through these codons, inserting an amino acid and allowing protein synthesis to continue, thus demonstrating the terminatory role of UAG in wild-type cells. Similar findings for ochre (UAA) and opal (UGA) suppressors soon followed, confirming that these triplets normally halt translation without involving standard tRNAs. A pivotal advance came in 1967 when developed an protein synthesis system using extracts and demonstrated that polypeptide chain termination at stop codons required soluble protein factors, not tRNAs, as no tRNA species could bind to UAA or UAG under physiological conditions. Capecchi isolated one such release factor from the S100 supernatant fraction, showing it promoted the release of completed peptides from peptidyl-tRNA on ribosomes in a codon-dependent manner. This work established that termination is mediated by dedicated proteins, building on the elucidation recognized by the 1968 in Physiology or Medicine to Nirenberg, Khorana, and Holley, whose codon assignments included the identification of stop signals. In the late 1960s and 1970s, researchers identified and characterized the two bacterial class I release factors, RF1 and RF2. Using cell-free E. coli systems with synthetic polynucleotides containing stop codons, Edward Scolnick, Thomas Caskey, and Marshall Nirenberg separated RF activities into two distinct components in 1968: one recognizing UAA and UAG (later named RF1), and the other recognizing UAA and UGA (RF2), with both stimulating peptidyl-tRNA hydrolysis by ribosomal . Further purification and genetic studies in the 1970s, including by Charles Kurland's group on ribosome-associated termination, confirmed their essential roles and codon specificities through assays measuring formylmethionine release and cleavage. Concurrently, a third factor, RF3, was described in 1969 by Caskey and colleagues as a GTP-dependent stimulator of termination efficiency, later characterized as a that promotes dissociation of RF1 and RF2 from post-termination ribosomes. The and 1990s extended these findings to eukaryotes and . Eukaryotic release factor 1 (eRF1), the omnipotent class I factor recognizing all three stop codons, was cloned in 1990 from rabbit reticulocytes by , William Craigen, and C. Thomas Caskey, revealing sequence similarity to bacterial RFs and tryptophanyl-tRNA synthetase, and confirming its activity in mammalian systems. Eukaryotic RF3 (eRF3), a homolog of bacterial RF3, was established in the through studies showing its role in enhancing eRF1-mediated termination and recycling, with cloning in (as SUP35) in the late . Archaeal homologs of eRF1 (aRF1) were first cloned in the early , such as from Methanococcus jannaschii, displaying structural and functional similarities to eukaryotic eRF1 and underscoring conserved termination mechanisms across domains. These discoveries laid the foundation for understanding termination as a universal process, influencing subsequent structural and mechanistic studies.

Classification

Prokaryotic Release Factors

In prokaryotic systems, particularly in bacteria such as Escherichia coli, translation termination is mediated by two class 1 release factors, RF1 and RF2, which recognize specific stop codons in the mRNA and catalyze the hydrolysis of the ester bond linking the completed polypeptide to the peptidyl-tRNA in the ribosomal P site. RF1, encoded by the prfA gene, specifically recognizes the UAA and UAG stop codons, while RF2, encoded by the prfB gene, recognizes UAA and UGA. Both RF1 and RF2 share a conserved GGQ motif that is essential for their peptidyl-tRNA hydrolytic activity, with mutations in this motif severely impairing peptide release efficiency. Codon specificity in RF1 and RF2 is determined by distinct motifs that function as anticodon-like elements: (Pro-Ala-Thr) in RF1 for UAA/UAG recognition and (Ser-Pro-Phe) in RF2 for UAA/UGA recognition. These motifs enable precise decoding of the stop codons at the ribosomal A site, ensuring accurate termination without the need for an anticodon arm as in tRNAs. The class 2 release factor RF3, encoded by the prfC gene, acts as a that facilitates the dissociation of RF1 or RF2 from the after peptide release, thereby the release factors and promoting efficient termination. Bacterial systems employ only these three release factors, lacking a single universal class 1 factor capable of recognizing all stop codons, in contrast to the unified eRF1 in eukaryotes.

Eukaryotic and Archaeal Release Factors

In eukaryotes and , translation termination is mediated by two classes of release factors that differ from the prokaryotic system, which relies on codon-specific factors. Class 1 release factors, eRF1 in eukaryotes and its archaeal homolog aRF1, are omnipotent, recognizing all three stop codons (UAA, UAG, and UGA) through a flexible N-terminal mini-domain containing conserved motifs such as the YxCxxxF loop that interacts with the ribosomal decoding center. This unified recognition mechanism enhances translational fidelity by avoiding the need for multiple specialized factors, contrasting with prokaryotic RF1 and RF2 that discriminate between UAA/UAG and UAA/UGA, respectively. Class 2 release factors assist in delivering the Class 1 factor to the and stimulating termination. In eukaryotes, eRF3 is a with structural similarity to elongation factor 1 alpha (EF1α), featuring GTP-binding and ABC-like domains that facilitate interaction and GTP . The archaeal counterpart, aEF1α, serves a multifunctional role, participating in both tRNA delivery during and release factor recruitment during termination by forming a complex with aRF1. In humans, eRF1 is encoded by the ETF1 on , while eRF3 (specifically eRF3a) is encoded by GSPT1; these are homologs of the SUP45 and SUP35 genes, respectively, underscoring evolutionary . Archaeal release factors exhibit greater similarity to eukaryotic ones than to bacterial, with aRF1 sharing the three-domain architecture of eRF1 and aEF1α fulfilling the eRF3 role without a dedicated termination-specific . This universal codon recognition by a single Class 1 factor in both domains supports broader fidelity in termination, minimizing errors in protein synthesis.

Molecular Structure

Domain Architecture

Release factors (RFs) are classified into class I and class II, with class I RFs exhibiting a conserved multi-domain that enables stop codon recognition and peptidyl-tRNA hydrolysis during termination. Class I RFs across of life share a general four-domain fold, though the organization varies: 1 at the N-terminus facilitates initial codon recognition, 2 mimics the anticodon loop for precise stop codon decoding, 3 harbors the catalytic GGQ for peptidyl-tRNA , and 4 at the C-terminus mediates interactions with the . This modular allows flexibility in binding to the ribosomal A site while positioning the catalytic elements near the peptidyl transferase center. In prokaryotes, class I RFs RF1 and RF2 adopt a compact structure comprising approximately 360 amino acids, organized into the four domains connected by variable linkers that permit conformational adjustments during termination. Domain 1 (residues ~1–106) and domain 2 (~107–208) form the decoding head, with domain 2's tripeptide motif (e.g., PxT for RF1 or SPF for RF2) directly engaging the stop codon; domain 3 (~209–300) contains the GGQ loop essential for catalysis; and domain 4 (~301–360) anchors to the ribosome's 50S subunit. Prokaryotic class II RF3, a GTPase, features a three-domain architecture similar to elongation factors EF-Tu and EF-G, including a central G-domain (domain I) for GTP hydrolysis, domain II, and domain III (a C-terminal β-barrel), which aids in RF1/RF2 recycling. Recent cryo-EM studies have revealed dynamic inter-domain flexibility in RF3, enabling its translocation on the ribosome post-termination. Eukaryotic class I eRF1 displays an elongated Y-shaped architecture of about 437 in humans, divided into three primary domains plus an N-terminal mini-domain. The N-domain (residues ~1–110, including the mini-domain ~40–65) universally recognizes all three stop codons via a flexible "finger" extension; the central M-domain (~111–270) houses the conserved GGQ motif for ; and the C-domain (~271–437) mimics the E-site tRNA to stabilize binding. Eukaryotic class II eRF3 is a larger (~700 ) with two GTP-binding domains (G-domain and G'-domain, resembling eEF1A) connected to an N-terminal domain 1 and a C-terminal extension (M-domain), which collectively facilitate eRF1 delivery and recycling through GTP-dependent conformational changes. Cryo-EM reconstructions from the 2020s highlight eRF1's domain rearrangements, such as M-domain folding to position GGQ near the peptidyl transferase center. Archaeal class I RF, termed aRF1, closely resembles eRF1 but is smaller (~370–400 ), with three domains designated A (N-like, for codon recognition), B (M-like, containing GGQ), and C (for interaction), showing high structural superposition to eukaryotic counterparts despite sequence divergence. Unlike , lack a dedicated RF3 homolog and instead utilize aEF1A•GTP as a class II factor, which shares the with eRF3 but lacks the extended C-terminal domain. Recent 2023 cryo-EM structures of archaeal termination complexes underscore aRF1's domain flexibility, particularly in the A-domain, enabling stable accommodation in the ribosomal A site across diverse archaeal species.

Conserved Motifs and Binding Sites

The GGQ motif, composed of glycine-glycine- residues, is a highly located in domain 3 of class 1 release factors (RF1, RF2, and eRF1) across prokaryotes, eukaryotes, and . This motif plays a pivotal role in catalyzing the of the bond in peptidyl-tRNA by positioning the glutamine side chain to coordinate and activate a molecule, enabling its nucleophilic attack on the of the ester linkage within the center of the . Structural studies reveal that the GGQ loop packs tightly into the peptidyl transferase center upon recognition, with the glutamine residue forming hydrogen bonds that facilitate water-mediated cleavage without requiring additional catalytic residues. Mutations altering any residue in the GGQ motif, such as of the glutamine, completely abolish the hydrolysis activity while preserving codon recognition and ribosomal binding capabilities. In bacterial class 1 release factors, codon specificity is mediated by sequences that mimic tRNA anticodons. For RF1, which recognizes UAA and UAG stop codons, the conserved motif (proline-alanine-threonine) interacts with the decoding center of the subunit, forming base-specific contacts analogous to an anticodon loop. Similarly, RF2 employs the motif (serine-proline-phenylalanine) to decode UAA and UGA, with the residue serving as a universal base-pairing element and the flanking residues providing specificity to avoid misrecognition of codons like UGG. These enable precise discrimination by engaging positions 1492 and 1493 of 16S rRNA helix 44, inducing the same conformational changes as cognate tRNAs during decoding. In contrast, eukaryotic and archaeal eRF1 achieves omnipotent recognition of all three stop codons (UAA, UAG, UGA) through a more flexible arrangement in its N-terminal domain, utilizing three distinct, non-contiguous residues rather than a single . These residues, including a conserved and basic , form a discontinuous decoding site that adaptively contacts the bases and surrounding ribosomal elements, allowing broader specificity without the rigid anticodon seen in . This architectural difference supports eRF1's ability to bind any flexibly, with the residues interacting via hydrogen bonding and stacking with 18S rRNA helix 44. Class 2 release factors, such as bacterial RF3 and eukaryotic eRF3, feature GTP-binding sites characterized by the conserved G1–G4 motifs, which are hallmarks of the superfamily. The G1 (GXXXXGK[S/T]) and (DXXG) motifs coordinate the groups and magnesium in the GTP-bound state, while G2 and G4 contribute to specificity and . GTP by these motifs drives conformational rearrangements in RF3/eRF3, promoting dissociation of class 1 release factors from the post-termination and recycling the termination complex. Ribosome interaction sites in release factors ensure stable accommodation in the A site distinct from tRNA binding. In bacterial RF1 and RF2, a prominent α-helix in domain 4 extends across the intersubunit bridge, making direct contacts with helix 34 of 16S rRNA and protein S12 to anchor the factor without occupying the anticodon loop position. Similarly, in eukaryotic eRF1, domain 4's helical elements interface with helices 18, 31, and 34 of 18S rRNA, stabilizing the factor in the decoding center while the N-domain mimics tRNA positioning for codon readout. These interactions facilitate A-site occupancy solely through protein-rRNA contacts, bypassing the need for an RNA anticodon.

Mechanism of Action

Bacterial Termination Process

In , termination initiates when the ribosome's A site accommodates a (UAA, UAG, or UGA) following the completion of polypeptide elongation. Class I release factors RF1 or RF2 bind to this site with GTP-independent affinity, selected based on codon specificity: RF1 decodes UAA and UAG, while RF2 decodes UAA and UGA. Recognition occurs via an anticodon-mimicry mechanism, where conserved tripeptide motifs—PWT in RF1 and SPF in RF2—form hydrogen bonds with the stop codon bases and engage the 16S rRNA decoding center, including the 530 loop. This binding triggers minor ribosomal conformational adjustments without major domain rearrangements, positioning the release factor for subsequent . Once accommodated, the release factor's domain 3 inserts the conserved GGQ motif into the center (PTC) of the 50S subunit, where the peptidyl-tRNA resides in the . The release factor induces a conformational change in the peptidyl-tRNA, repositioning it such that the 2'-OH group of A76 adopts a C3'-endo conformation and performs an autohydrolytic nucleophilic attack on the ester bond, liberating the nascent protein. The conserved GGQ motif structurally facilitates this peptidyl-tRNA rearrangement, stabilized by interactions with 23S rRNA elements such as A2451 and A2602. This reaction proceeds without GTP involvement at this stage and ensures efficient release, typically occurring in milliseconds. Post-hydrolysis, the post-termination ribosomal complex requires disassembly to recycle components. GTP-bound RF3 binds to the , interacting with the RF1 or RF2 to induce their ejection upon GTP , which drives conformational changes in RF3 from an open to a closed state. recycling then proceeds via the ribosome recycling factor (RRF) binding to the A site, followed by G (EF-G) in its GTP form, which splits the 70S into subunits for reinitiation. This step enhances termination by preventing stalling. The bacterial termination process maintains high fidelity, achieving over 99.99% accuracy in recognition, with error rates around 10^{-5} for inappropriate of s (e.g., by near- tRNAs), which can yield aberrant extended proteins. Such precision arises from induced-fit conformational switches in the release factors upon codon binding, discriminating against near- sequences through energetic barriers. Structural insights derive from crystal structures of Thermus thermophilus 70S ribosomes with RF1 or RF2, resolved at 3.0–3.6 Å in the 2000s and 2010s, revealing RF positioning in the intersubunit space and PTC interactions. Recent cryo-EM studies post-2019, including those on and other bacterial variants, have captured RF3 dynamics at near-atomic resolution (3.3–4.0 Å), illustrating GTPase-driven rearrangements and recycling intermediates across species like Thermus and . A study further elucidated the universal autohydrolytic mechanism at atomic resolution.

Eukaryotic and Archaeal Termination Process

In eukaryotes, termination initiates when the ternary complex of eukaryotic release factor 1 (eRF1) and eRF3 bound to GTP recognizes a in the ribosomal A site. The N-terminal domain (Domain 1) of eRF1 universally decodes all three stop codons (UAA, UAG, and UGA) through conserved motifs such as the TASNIKS and YxCxxxF regions, mimicking tRNA anticodon interactions. eRF3, functioning as a , binds to the C-terminal domain of eRF1 and enhances the affinity of the complex for the , promoting stable accommodation into the A site. This GTP-bound state positions eRF1 proximal to the center (PTC), setting the stage for . Upon recognition, GTP by eRF3 drives an allosteric conformational change in eRF1, repositioning its central domain (Domain 2) to induce peptidyl-tRNA rearrangement in the PTC, where the 2'-OH of A76 performs autohydrolysis of the ester bond, releasing the nascent polypeptide. The conserved GGQ motif structurally supports this process, with interactions between eRF1, the , and the stimulating the reaction; mutations impairing eRF3 activity, such as H348Q, reduce termination efficiency by up to 17-fold for certain contexts. The allosteric switch transitions eRF1 from a decoding to a catalytic conformation, enhancing by discriminating from near-cognate sense codons like UGG. Following , eRF3 bound to GDP dissociates from the , leaving eRF1 associated with the post-termination complex. Ribosome recycling then occurs, where the ribosome-recycling factor ABCE1, an ATP-binding cassette protein, binds to the eRF1-stalled ribosome, promoting subunit dissociation and release of eRF1, mRNA, and deacylated tRNA; this process is assisted by factors like eIF1 and eIF3 to prepare for the next round of . In , the termination process shares structural and mechanistic similarities but is simpler, relying on archaeal release factor 1 (aRF1) and the multifunctional aEF1α, which serves roles in elongation, termination, and mRNA surveillance akin to both eEF1A and eRF3. aEF1α forms a GTP-dependent complex with aRF1, facilitating recognition and peptidyl-tRNA via the universal autohydrolytic , with aRF1 providing decoding for all three stop codons. Recent cryo-EM studies of the ribosome in complex with eRF1 and eRF3 have revealed detailed interactions, including eRF1's contacts with the mRNA channel that stabilize positioning and prevent slippage, refining models of beyond earlier resolutions. These structures, achieved at near-atomic detail, highlight dynamic rearrangements during GTP hydrolysis and underscore the GTP-dependent fidelity mechanisms unique to eukaryotes and .

Evolution and Variations

Evolutionary Origins

Release factors involved in translation termination exhibit distinct evolutionary trajectories across the domains of , reflecting independent origins for the bacterial and archaeo-eukaryotic lineages. In , RF1 and RF2 evolved from a common ancestor distinct from that of the archaeal and eukaryotic eRF1 (also known as aRF1 in archaea), with bacterial factors adopting an RNase H-like fold while eRF1 features a unique α/β architecture. This underscores the separate of class I release factors following the split between and the archaeo-eukaryotic lineage. Recent phylogenomic analyses reinforce the unity of archaeal and eukaryotic eRF1, grouping them into a coherent distinct from bacterial counterparts, consistent with broader evidence for an archaeal origin of eukaryotic translation machinery. The () likely possessed a proto-release factor, possibly a tRNA-like , that catalyzed peptidyl-tRNA via a conserved essential for release. This ancestral system predates the major domain divergence, estimated at approximately 3.5 billion years ago, when bacterial and archaeo-eukaryotic lineages separated, leading to lineage-specific elaborations of termination mechanisms. The itself remains universally conserved across all release factors, highlighting its ancient role in ribosomal center interactions. A striking example of is observed in the anticodon employed by release factors to recognize stop codons, where both bacterial and archaeo-eukaryotic factors emulate tRNA anticodon loops but through structurally dissimilar means. Bacterial RF1 and RF2 utilize compact motifs within their variable regions for codon-specific recognition (e.g., a motif in RF1 for UAA/UAG), enabling precise decoding in the ribosomal A site. In contrast, eRF1 employs dispersed, non-contiguous residues across its N-terminal domain to achieve analogous tRNA-like positioning and discrimination, demonstrating functional despite independent origins. Class II release factors also arose through events from ancestral elongation . In , RF3 emerged as a paralog of the EF-G , adapting translocation functions for RF1/RF2 recycling post-termination. Similarly, the eukaryotic eRF3 (and archaeal homologs) duplicated from the EF-Tu/EF1α lineage, evolving to stimulate eRF1 activity and facilitate dissociation from the . In certain eukaryotes, such as , eRF3 acquired an additional N-terminal prion-like domain (as in Sup35p), which is non-conserved and enables formation but is absent in archaeal and most eukaryotic orthologs, representing a later innovation rather than an ancestral feature.

Organellar Release Factors

Organellar release factors operate within mitochondria and chloroplasts, s that inherited bacterial-like systems from their endosymbiotic ancestors. These factors facilitate termination adapted to the unique genetic codes and environmental constraints of each , with genes often transferred to the genome over evolutionary time. In human mitochondria, termination relies on a simplified set of bacterial-type class I release factors, lacking an RF2 homolog. The primary factor, mtRF1a (encoded by MTRF1A), recognizes UAA and UAG stop codons, promoting peptidyl-tRNA via its conserved GGQ motif. A related factor, mtRF1 (encoded by MTRF1), specializes in terminating at the COX1 gene's non-canonical AGA/AGG stops, preventing ribosomal stalling and triggering pathways. For UGA codons, which code for rather than serving as stops in most mitochondrial s, termination and rescue occur through ICT1 (also known as mL62 or MRPL58), an integral mitoribosomal protein that cleaves stalled peptidyl-tRNAs during non-stop events or at reassigned stops. Another rescue factor, mtRF-R (encoded by MTRFR or C12orf65), assists in resolving stalled ribosomes, particularly under stress conditions. Mutations in these factors, such as in MTRFR, are associated with mitochondrial encephalomyopathies, spastic paraparesis, and neurodegeneration, highlighting their role in maintaining organellar ; for instance, MTRFR variants lead to impaired and . Post-2019 studies have expanded on this diversity, revealing how GGQ motif disruptions in ICT1 or mtRF1a compromise cell viability and exacerbate oxidative damage in disease models, linking release factor dysfunction to broader neuropathologies like . Chloroplasts in plants retain a more canonical bacterial termination system, employing a single class I release factor, cpRF1 (e.g., AtcpRF1 in Arabidopsis thaliana or ZmcpRF1 in maize), which recognizes all three stop codons (UAA, UAG, UGA) without codon reassignment. Encoded by nuclear genes following endosymbiotic gene transfer, cpRF1 is essential for chloroplast biogenesis and development; its absence results in albino seedlings and arrested embryogenesis due to defective protein synthesis. Mutations in cpRF1 homologs disrupt thylakoid formation and photosynthesis, underscoring its conserved bacterial-like function in organellar translation. Ribosome recycling in organelles differs from cytosolic systems, avoiding reliance on eukaryotic eRF3. In mitochondria, post-termination dissociation involves the recycling factor (mtRRF) and the GTPase mtEF-G1, which split the ribosomal subunits for reuse, with ICT1 occasionally aiding in this process during rescue. Chloroplasts employ analogous bacterial-style recycling via cpRRF and chloroplast-specific EF-G homologs, ensuring efficient translation cycles within the environment.