RNA chaperone activity of translation initiation factor IF1

Croitoru, Victor; Semrad, Katharina; Prenninger, Silvia; Rajkowitsch, Lukas; Vejen, Max; Laursen, Brian Søgaard; Sperling‐Petersen, Hans Uffe; Isaksson, Leif A.

doi:10.1016/j.biochi.2006.06.017

Cited by 31 publications

(29 citation statements)

References 28 publications

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“…Our observation that IF1 is an RNA chaperone is consistent with a previous report which showed that IF1 alters the structures of various oligonucleotides and disrupts nucleic acid interactions in vitro (33). During the preparation of this article, an interesting report by Croitoru et al was published (6). The authors showed that IF1 activates splicing of the group I intron of the thymidylate synthase gene from phage T4 and suggested that this activity requires the RNA chaperoning activity of IF1.…”

Section: Discussionsupporting

confidence: 79%

Transcription Antitermination by Translation Initiation Factor IF1

et al. 2007

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Bacterial translation initiation factor IF1 is an S1 domain protein that belongs to the oligomer binding (OB) fold proteins. Cold shock domain (CSD)-containing proteins such as CspA (the major cold shock protein of Escherichia coli) and its homologues also belong to the OB fold protein family. The striking structural similarity between IF1 and CspA homologues suggests a functional overlap between these proteins. Certain members of the CspA family of cold shock proteins act as nucleic acid chaperones: they melt secondary structures in nucleic acids and act as transcription antiterminators. This activity may help the cell to acclimatize to low temperatures, since cold-induced stabilization of secondary structures in nascent RNA can impede transcription elongation. Here we show that the E. coli translation initiation factor, IF1, also has RNA chaperone activity and acts as a transcription antiterminator in vivo and in vitro. We further show that the RNA chaperone activity of IF1, although critical for transcription antitermination, is not essential for its role in supporting cell growth, which presumably functions in translation. The results thus indicate that IF1 may participate in transcription regulation and that cross talk and/or functional overlap may exist between the Csp family proteins, known to be involved in transcription regulation at cold shock, and S1 domain proteins, known to function in translation.Shifting exponentially growing Escherichia coli cells from 37°C to 15°C elicits a cold shock response, during which the synthesis of most cellular proteins is strongly decreased while the synthesis of several cold shock proteins is strongly increased. The most highly produced cold shock protein is the CspA protein. E. coli has nine CspA homologues, only some of which are cold shock inducible. CspA and its homologues destabilize secondary structures in both RNA and DNA and are therefore referred to as nucleic acid chaperones (13). In our previous studies, we showed that CspA and its homologues CspC and CspE act as transcription antiterminators (1). Stabilization of secondary structures in RNA upon a temperature downshift affects transcription elongation by RNA polymerase. Therefore, the RNA chaperoning activity of CspA and its cold-inducible homologues might facilitate transcription at low temperatures. Indeed, the nucleic acid melting activity of CspA family proteins is essential both for transcription antitermination and for cold acclimation of cells (27).X-ray and nuclear magnetic resonance structures of E. coli CspA and Bacillus subtilis CspB reveal a barrel of five antiparallel ␤-strands with a surface-exposed patch of several aromatic amino acids (8,23,31,32,34). These amino acids are involved in nucleic acid binding activity (11,35), and some are essential for nucleic acid chaperoning activity (27,29).The common fold of CspA homologues has been named the cold shock domain (CSD). The structure of the CSD is very similar to the S1 domain structure. On the basis of this similarity, the CSD and S1 domain...

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Section: Discussionsupporting

confidence: 79%

Transcription Antitermination by Translation Initiation Factor IF1

et al. 2007

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“…IF1 is active in trans-splicing, it rescues the splicing of a misfolded intron in vivo, and it resolves a terminator stem in vitro and in vivo. 29,69 CspA has further striking similarity (43% sequence identity) to the cold shock domain of the Y-box factors, which are eukaryotic nucleic acid binding proteins involved in transcriptional and translational regulation. 70 One well-studied member is the major messenger ribonucleoprotein particle protein p50, also known as YB-1, which is a general regulator of translation by modulating mRNA structural rearrangements and packaging.…”

Section: Classification Of Proteins With Rna Chaperone Activitymentioning

confidence: 98%

“…In vitro annealing of short, unstructured RNAs occurs by itself, but this reaction can be accelerated by annealingactive proteins up to the diffusion limit. 29,30 Molecular crowding might be one of the mechanisms proteins with RNA annealing activity (RNA annealers) employ, which results in an increase in the local RNA concentration and thereby enhances the probability of RNA annealing. This can be achieved by simultaneous binding of both RNAs.…”

Section: Proteins That Assist Rnas In Foldingmentioning

confidence: 99%

RNA Chaperones, RNA Annealers and RNA Helicases

Rajkowitsch¹,

Chen²,

Stampfl³

et al. 2007

RNA Biology

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RNA molecules face difficulties when folding into their native structures. In the cell, proteins can assist RNAs in reaching their functionally active states by binding and stabilizing a specific structure or, in a quite opposite way, by interacting in a non-specific manner. These proteins can either facilitate RNA-RNA interactions in a reaction termed RNA annealing, or they can resolve non-functional inhibitory structures. The latter is defined as "RNA chaperone activity" and is the main topic of this review. Here we define RNA chaperone activity in a stringent way and we review those proteins for which RNA chaperone activity has been clearly demonstrated. These proteins belong to quite diverse families such as hnRNPs, histone-like proteins, ribosomal proteins, cold shock domain proteins and viral nucleocapsid proteins. DExD/H-box containing RNA helicases are discussed as a special family of enzymes that restructure RNA or RNPs in an ATP-dependent manner. We further address the different mechanisms RNA chaperones might use to promote folding including the recently proposed theory of protein disorder as a key element in triggering RNA-protein interactions. Finally, we present a new website for proteins with RNA chaperone activity which compiles all the information on these proteins with the perspective to promote the understanding of their activity.

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“…IF1, one of the three factors essential to initiate protein synthesis in bacteria is a β-barrel RNA binding protein (Gualerzi et al, 2001;Boelens and Gualerzi, 2002;Laursen et al, 2005) with RNA chaperone activity (Croitoru et al, 2006) which binds to the 30S ribosomal subunit (Celano et al, 1988;Carter et al, 2001) induces a conformational change of the subunit mainly involving helix 44 of 16S rRNA (Carter et al, 2001) and stimulates, together with IF2 and IF3, the formation of both 30S and 70S initiation complexes (30SIC and 70SIC) (Wintermeyer and Gualerzi, 1983;Pon and Gualerzi, 1984). Furthermore, IF1 cooperates with IF3 to maintain a sufficient pool of free subunits (Godefroy-Colburn et al, 1975;Giangrossi et al, 2007) and to ensure initiation fidelity by discriminating against non-canonical 30S initiation complexes (Milon et al, 2008).…”

Section: Introductionmentioning

confidence: 96%