Involvement of PIN‐like domain nucleases in tRNA processing and translation regulation

Gobert, Anthony; Bruggeman, Mathieu; Giegé, Philippe

doi:10.1002/iub.2062

Cited by 19 publications

(19 citation statements)

References 79 publications

(104 reference statements)

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“…Alongside the RNA binding and processing functions, the PRORP family members interact in different manners with the ubiquitin system. MCPIP-1 contains a UBA domain at the N-terminus, but the presence of a similar domain in the other MCPIP members has not been experimentally validated [120][121][122]. The MCPIP proteins are also endowed with a deubiquitinating activity that targets proteins involved in the inflammatory response.…”

Section: The Prorp Family Membersmentioning

confidence: 99%

Old and New Concepts in Ubiquitin and NEDD8 Recognition

Santonico

2020

Biomolecules

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Post-translational modifications by ubiquitin and ubiquitin-like proteins (Ubls) have known roles in a myriad of cellular processes. Ubiquitin- and Ubl-binding domains transmit the information conferred by these post-translational modifications by recognizing functional surfaces and, when present, different chain structures. Numerous domains binding to ubiquitin have been characterized and their structures solved. Analogously, motifs selectively interacting with SUMO (small ubiquitin-like modifier) have been identified in several proteins and their role in SUMO-dependent processes investigated. On the other hand, proteins that specifically recognize other Ubl modifications are known only in a few cases. The high sequence identity between NEDD8 and ubiquitin has made the identification of specific NEDD8-binding domains further complicated due to the promiscuity in the recognition by several ubiquitin-binding domains. Two evolutionarily related domains, called CUBAN (cullin-binding domain associating with NEDD8) and CoCUN (cousin of CUBAN), have been recently described. The CUBAN binds monomeric NEDD8 and neddylated cullins, but it also interacts with di-ubiquitin chains. Conversely, the CoCUN domain only binds ubiquitin. CUBAN and CoCUN provide an intriguing example of how nature solved the issue of promiscuity versus selectivity in the recognition of these two highly related molecules. The structural information available to date suggests that the ancestor of CUBAN and CoCUN was a three-helix bundle domain that diversified in KHNYN (KH and NYN domain-containing) and N4BP1 (NEDD4-binding protein-1) by acquiring different features. Indeed, these domains diverged towards two recognition modes, that recall respectively the electrostatic interaction utilized by the E3-ligase RBX1/2 in the interaction with NEDD8, and the hydrophobic features described in the recognition of ubiquitin by CUE (coupling ubiquitin conjugation to ER degradation) domains. Intriguingly, CUBAN and CoCUN domains are only found in KHNYN and N4BP1, respectively, both proteins belonging to the PRORP family whose members are characterized by the combination of protein modules involved in RNA metabolism with domains mediating ubiquitin/NEDD8 recognition. This review recapitulates the current knowledge and recent findings of CUBAN and CoCUN domains and the proteins containing them.

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Section: The Prorp Family Membersmentioning

confidence: 99%

Old and New Concepts in Ubiquitin and NEDD8 Recognition

Santonico

2020

Biomolecules

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“…In all domains of life (Bacteria, Archaea and Eukarya), the mature 5′‐ends of tRNA molecules are generated by the essential endonuclease RNase P. The enzyme was originally identified to consist of a catalytic RNA and a single protein subunit in bacteria such as Escherichia coli and Bacillus subtilis . This RNA‐centric architecture was subsequently found in almost all bacterial subphyla as well as in archaea and eukarya, in the two latter phylogenetic domains in the form of a ribonucleoprotein composed of a single RNA and 4–5 (archaea) and 9–10 (eukaryotic nuclei) different protein subunits . The ribonucleoprotein type of RNase P is assumed to be the ancient form of the enzyme.…”

Section: Introductionmentioning

confidence: 99%

“…As the eukaryal PRORPs, Aq_880 is also a member of the PIN domain‐like superfamily of metallonucleases, but belonging to a different subgroup (PIN_5 cluster, VapC structural group) . In contrast to the known PRORPs (~60–65 kDa ), Aq_880 is a remarkably small protein (~23 kDa), which shows limited similarity to the metallonuclease domain of PRORPs but lacks their pentatricopeptide repeat (PPR) RNA‐binding and bipartite zinc‐binding domains . Homologs of Aq_880, termed Homologs of Aquifex RNase P (HARPs), were identified in some bacteria and many archaea (see alignment in Fig.…”

Section: Introductionmentioning

confidence: 99%

Homologs of aquifex aeolicus protein‐only RNase P are not the major RNase P activities in the archaea haloferax volcanii and methanosarcina mazei

et al. 2019

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The mature 5′‐ends of tRNAs are generated by RNase P in all domains of life. The ancient form of the enzyme is a ribonucleoprotein consisting of a catalytic RNA and one or more protein subunits. However, in the hyperthermophilic bacterium Aquifex aeolicus and close relatives, RNase P is a protein‐only enzyme consisting of a single type of polypeptide (Aq_880, ~23 kDa). In many archaea, homologs of Aq_880 were identified (termed HARPs for Homologs of Aquifex RNase P) in addition to the RNA‐based RNase P, raising the question about the functions of HARP and the classical RNase P in these archaea. Here we investigated HARPs from two euryarchaeotes, Haloferax volcanii and Methanosarcina mazei. Archaeal strains with HARP gene knockouts showed no growth phenotypes under standard conditions, temperature and salt stress (H. volcanii) or nitrogen deficiency (M. mazei). Recombinant H. volcanii and M. mazei HARPs were basically able to catalyse specific tRNA 5′‐end maturation in vitro. Furthermore, M. mazei HARP was able to rescue growth of an Escherichia coli RNase P depletion strain with comparable efficiency as Aq_880, while H. volcanii HARP was unable to do so. In conclusion, both archaeal HARPs showed the capacity (in at least one functional assay) to act as RNases P. However, the ease to obtain knockouts of the singular HARP genes and the lack of growth phenotypes upon HARP gene deletion contrasts with the findings that the canonical RNase P RNA gene cannot be deleted in H. volcanii, and a knockdown of RNase P RNA in H. volcanii results in severe tRNA processing defects. We conclude that archaeal HARPs do not make a major contribution to global tRNA 5′‐end maturation in archaea, but may well exert a specialised, yet unknown function in (t)RNA metabolism. © 2019 IUBMB Life, 2019 © 2019 IUBMB Life, 71(8):1109–1116, 2019

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“…HARPs belong to the PIN domain-like superfamily of metallonucleases. They were assigned to the PIN_5 cluster, VapC structural group, whereas eukaryal PRORPs belong to a different subgroup of this superfamily (Matelska, Steczkiewicz, and Ginalski 2017;Gobert, Bruggeman, and Giegé 2019). HARPs oligomerize and Aq880 was originally observed to elute as a large homo-oligomeric complex of ~420-kDa in gel filtration experiments (Nickel et al 2017).…”

Section: Introductionmentioning

confidence: 99%

“…The findings suggest that HARP is neither essential nor represents the housekeeping RNase P function in archaea, explaining its sporadic loss in archaea. HARPs are evolutionarily linked to toxin-antitoxin systems ( Daniels et al, 2019 ; Schwarz et al, 2019 ; Gobert et al, 2019 ). Frequently, the toxin proteins are endoribonucleases that cleave mRNA, rRNA, tmRNA, or tRNA to inhibit protein biosynthesis in response to certain stresses ( Masuda and Inouye, 2017 ).…”

Section: Introductionmentioning

confidence: 99%

Structure and mechanistic features of the prokaryotic minimal RNase P

Feyh

Waeber

Prinz

et al. 2021

eLife

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Endonucleolytic removal of 5'-leader sequences from tRNA precursor transcripts (pre-tRNAs) by RNase P is essential for protein synthesis. Beyond RNA-based RNase P enzymes, protein-only versions of the enzyme exert this function in various Eukarya (there termed PRORPs) and in some bacteria (Aquifex aeolicus and close relatives); both enzyme types belong to distinct subgroups of the PIN domain metallonuclease superfamily. Homologs of Aquifex RNase P (HARPs) are also expressed in some other bacteria and many archaea, where they coexist with RNA-based RNase P and do not represent the main RNase P activity. Here we solved the structure of the bacterial HARP from Halorhodospira halophila by cryo-EM revealing a novel screw-like dodecameric assembly. Biochemical experiments demonstrate that oligomerization is required for RNase P activity of HARPs. We propose that the tRNA substrate binds to an extended spike-helix (SH) domain that protrudes from the screw-like assembly to position the 5'-end in close proximity to the active site of the neighboring dimer. The structure suggests that eukaryotic PRORPs and prokaryotic HARPs recognize the same structural elements of pre-tRNAs (tRNA elbow region and cleavage site). Our analysis thus delivers the structural and mechanistic basis for pre-tRNA processing by the prokaryotic HARP system.

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Involvement of PIN‐like domain nucleases in tRNA processing and translation regulation

Cited by 19 publications

References 79 publications

Old and New Concepts in Ubiquitin and NEDD8 Recognition

Old and New Concepts in Ubiquitin and NEDD8 Recognition

Homologs of aquifex aeolicus protein‐only RNase P are not the major RNase P activities in the archaea haloferax volcanii and methanosarcina mazei

Structure and mechanistic features of the prokaryotic minimal RNase P

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