Nenad Ban's research while affiliated with ETH Zurich and other places
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Publications (222)
Ribosomes scanning from the mRNA 5′ cap to the start codon may initiate at upstream open reading frames (uORFs), decreasing protein biosynthesis. Termination at a uORF can lead to re-initiation, where the 40S subunit resumes scanning and initiates another translation event downstream. In mammals, the noncanonical translation factors MCTS1-DENR part...
Eukaryotic ribosome assembly is an intricate process that involves four ribosomal RNAs, 80 ribosomal proteins, and over 200 biogenesis factors that take part in numerous interdependent steps. This complexity creates a large genetic space in which pathogenic mutations can occur. Dead-end ribosome intermediates that result from biogenesis errors are...
In vitro translation is an important method for studying fundamental aspects of co- and post-translational gene regulation, as well as for protein expression in the laboratory and on an industrial scale. Here, by re-examining and improving a human in vitro translation system (HITS), we were able to develop a minimal system where only four component...
Coronaviruses are a group of related RNA viruses that cause respiratory diseases in humans and animals. Understanding the mechanisms of translation regulation during coronaviral infections is critical for developing antiviral therapies and preventing viral spread. Translation of the viral single-stranded RNA genome in the host cell cytoplasm is an...
Antibiotics target key biological processes that include protein synthesis. Bacteria respond by developing resistance, which increases rapidly due to antibiotics overuse. Mupirocin, a clinically used natural antibiotic, inhibits isoleucyl-tRNA synthetase (IleRS), an enzyme that links isoleucine to its tRNAIle for protein synthesis. Two IleRSs, mupi...
DNA-encoded chemical libraries (DELs) consist of large chemical compound collections individually linked to DNA barcodes, facilitating pooled construction and screening. However, screening campaigns often fail if the molecular arrangement of the building blocks is not conducive to an efficient interaction with a protein target. Here we postulated t...
N-terminal methionine excision from newly synthesized proteins, catalyzed cotranslationally by methionine aminopeptidases (METAPs), is an essential and universally conserved process that plays a key role in cell homeostasis and protein biogenesis. However, how METAPs interact with ribosomes and how their cleavage specificity is ensured is unknown....
Nonstructural protein 1 (Nsp1) produced by coronaviruses shuts down host protein synthesis in infected cells. The C-terminal domain of SARS-CoV-2 Nsp1 was shown to bind to the small ribosomal subunit to inhibit translation, but it is not clear whether this mechanism is broadly used by coronaviruses, whether the N-terminal domain of Nsp1 binds the r...
The translocon-associated protein (TRAP) complex resides in the endoplasmic reticulum (ER) membrane and interacts with the Sec translocon and the ribosome to facilitate biogenesis of secretory and membrane proteins. TRAP plays a key role in the secretion of many hormones, including insulin. Here we reveal the molecular architecture of the mammalian...
The genetic code that specifies the identity of amino acids incorporated into proteins during protein synthesis is almost universally conserved. Mitochondrial genomes feature deviations from the standard genetic code, including the reassignment of two arginine codons to stop codons. The protein required for translation termination at these noncanon...
Antibiotics target key biological processes that include protein synthesis. Bacteria respond by developing resistance, which increases rapidly due to antibiotics overuse. Mupirocin, a clinically used natural antibiotic, inhibits isoleucyl-tRNA synthetase (IleRS), an enzyme that links isoleucine to its tRNA Ile for protein synthesis. Two IleRSs, mup...
Effective public-health measures against SARS-CoV-2 require granular knowledge of population-level immune responses. We developed a Tripartite Automated Blood Immunoassay (TRABI) to assess the IgG response against three SARS-CoV-2 proteins. We used TRABI for continuous seromonitoring of hospital patients and blood donors (n=72’250) in the canton of...
The Translocon Associated Protein (TRAP) complex resides in the endoplasmic reticulum (ER) membrane and interacts with the Sec translocon and the translating ribosome to facilitate biogenesis of secretory and membrane proteins. TRAP is essential for the secretion of many hormones, and its key role in the production of the hormone peptide insulin ha...
Isoleucyl‐tRNA synthetase (IleRS) is an essential enzyme that covalently couples isoleucine to the corresponding tRNA. Bacterial IleRSs group in two clades, ileS1 and ileS2, the latter bringing resistance to the natural antibiotic mupirocin. Generally, bacteria rely on either ileS1 or ileS2 as a standalone housekeeping gene. However, we have found...
The nascent polypeptide-associated complex (NAC) interacts with newly synthesized proteins at the ribosomal tunnel exit and competes with the signal recognition particle (SRP) to prevent mistargeting of cytosolic and mitochondrial polypeptides to the endoplasmic reticulum (ER). How NAC antagonizes SRP and how this is overcome by ER targeting signal...
Isoleucyl-tRNA synthetase (IleRS) is an essential enzyme that covalently couples isoleucine to the corresponding tRNA. Bacterial IleRSs group in two clades, ileS1 and ileS2 , the latter bringing resistance to the natural antibiotic mupirocin. Generally, bacteria rely on either ileS1 or ileS2 as a standalone housekeeping gene. However, we have found...
Significance
Mitochondria originated from ancestral bacteria and they still maintain their own reduced genome and translational apparatus that feature highly diverged mitoribosomes, specialized for the synthesis of membrane proteins. Only recently, high-resolution cryo-EM structures of the mature mitoribosomes from several species revealed their un...
Transcriptional activator PafBC is the key regulator of the mycobacterial DNA damage response and controls around 150 genes, including genes involved in the canonical SOS response, through an unknown molecular mechanism. Using a combination of biochemistry and cryo–electron microscopy, we demonstrate that PafBC in the presence of single-stranded DN...
Pupylation is the post-translational modification of lysine side chains with prokaryotic ubiquitin-like protein (Pup) that targets proteins for proteasomal degradation in mycobacteria and other members of Actinobacteria. Pup ligase PafA and depupylase Dop are the two enzymes acting in this pathway. Although they share close structural and sequence...
Co-translational protein targeting to membranes by the signal recognition particle (SRP) is a universally conserved pathway from bacteria to humans. In mammals, SRP and its receptor (SR) have many additional RNA features and protein components compared to the bacterial system, which were recently shown to play regulatory roles. Due to its complexit...
Mitochondrial ribosomes are specialized for the synthesis of membrane proteins responsible for oxidative phosphorylation. Mammalian mitoribosomes have diverged considerably from the ancestral bacterial ribosomes and feature dramatically reduced ribosomal RNAs. The structural basis of the mammalian mitochondrial ribosome assembly is currently not we...
Revolution in an RNA-packaging capsid
Artificial nucleocapsid proteins, which could be analogous to those used by viruses to package their genomes, are a promising way to protect and deliver RNAs. Using an escalating challenge by nucleases, Tetter et al. evolved a protein that forms multimeric, spherical cages into a highly efficient capsid that se...
Biogenesis of ribosomal subunits involves enzymatic modifications of rRNA that fine-tune functionally important regions. The universally conserved prokaryotic dimethyltransferase KsgA sequentially modifies two universally conserved adenosine residues in helix 45 of the small ribosomal subunit rRNA, which is in proximity of the decoding site. Here w...
Shifting frames to make more proteins
Severe acute respiratory syndrome coronavirus 2 critically depends on the ribosomal frameshifting that occurs between two large open reading frames in its genomic RNA for expression of viral replicase. Programmed frameshifting occurs during translation, when the ribosome encounters a stimulatory pseudoknot RNA...
The conserved signal recognition particle (SRP) cotranslationally delivers ~30% of the proteome to the eukaryotic endoplasmic reticulum (ER). The molecular mechanism by which eukaryotic SRP transitions from cargo recognition in the cytosol to protein translocation at the ER is not understood. Here, structural, biochemical, and single-molecule studi...
The mitochondrial translation system originates from a bacterial ancestor but has substantially diverged in the course of evolution. Here, we use single-particle cryo-electron microscopy (cryo-EM) as a screening tool to identify mitochondrial translation termination mechanisms and to describe them in molecular detail. We show how mitochondrial rele...
Mitochondrial ribosomes are specialized for the synthesis of membrane proteins responsible for oxidative phosphorylation. Mammalian mitoribosomes diverged considerably from the ancestral bacterial ribosomes and feature dramatically reduced ribosomal RNAs. Structural basis of the mammalian mitochondrial ribosome assembly is currently not understood....
The mitochondrial translation system originates from a bacterial ancestor but has substantially diverged in the course of evolution. Here, we use single particle cryo-EM as a screening tool to identify mitochondrial translation termination mechanisms and to describe them in molecular detail. We show how mitochondria release factor 1a releases the n...
Mitochondria are cellular organelles responsible for generation of chemical energy in the process called oxidative phosphorylation. They originate from a bacterial ancestor and maintain their own genome, which is expressed by designated, mitochondrial transcription and translation machineries that differ from those operating for nuclear gene expres...
Viruses are ubiquitous pathogens of global impact. Prompted by the hypothesis that their earliest progenitors recruited host proteins for virion formation, we have used stringent laboratory evolution to convert a bacterial enzyme lacking affinity for nucleic acids into an artificial nucleocapsid that efficiently packages and protects multiple copie...
The protein kinase mammalian target of rapamycin (mTOR) is the central regulator of cell growth. Aberrant mTOR signaling is linked to cancer, diabetes, and neurological disorders. mTOR exerts its functions in two distinct multiprotein complexes, mTORC1 and mTORC2. Here, we report a 3.2-Å resolution cryo-EM reconstruction of mTORC2. It reveals entan...
An amendment to this paper has been published and can be accessed via a link at the top of the paper.
Ribosomes have been suggested to directly control gene regulation, but regulatory roles for ribosomal RNA (rRNA) remain largely unexplored. Expansion segments (ESs) consist of multitudes of tentacle-like rRNA structures extending from the core ribosome in eukaryotes. ESs are remarkably variable in sequence and size across eukaryotic evolution with...
Programmed ribosomal frameshifting is the key event during translation of the SARS-CoV-2 RNA genome allowing synthesis of the viral RNA-dependent RNA polymerase and downstream viral proteins. Here we present the cryo-EM structure of the mammalian ribosome in the process of translating viral RNA paused in a conformation primed for frameshifting. We...
The SARS-CoV-2 non-structural protein 1 (Nsp1), also referred to as the host shutoff factor, suppresses host innate immune functions. By combining cryo-electron microscopy and biochemistry, we show that SARS-CoV-2 Nsp1 binds to the human 40S subunit in ribosomal complexes, including the 43S pre-initiation complex and the non-translating 80S ribosom...
The non-structural protein 1 (Nsp1), also referred to as the host shutoff factor, is the first viral protein that is synthesized in SARS-CoV-2 infected human cells to suppress host innate immune functions. By combining cryo-electron microscopy and biochemical experiments, we show that SARS-CoV-2 Nsp1 binds to the human 40S subunit in ribosomal comp...
In contrast to the bacterial translation machinery, mitoribosomes and mitochondrial translation factors are highly divergent in terms of composition and architecture. There is increasing evidence that the biogenesis of mitoribosomes is an intricate pathway, involving many assembly factors. To better understand this process, we investigated native a...
Mitochondria are eukaryotic organelles of bacterial origin where respiration takes place to produce cellular chemical energy. These reactions are catalyzed by the respiratory chain complexes located in the inner mitochondrial membrane. Notably, key components of the respiratory chain complexes are encoded on the mitochondrial chromosome and their e...
Serological assays can detect anti-SARS-CoV-2 (SARS2) antibodies, but their sensitivity often comes at the expense of specificity. Here we used a Ternary Automated Blood Im-munoassay (TRABI) to assess the IgG response against SARS2 in 3,815 prepandemic plasma samples and 126 virologically and/or clinically confirmed COVID-19 samples. Posterior prob...
The protein kinase mammalian target of rapamycin (mTOR) is the central regulator of cell growth. Aberrant mTOR signaling is linked to cancer, diabetes and neurological disorders. mTOR exerts its functions in two distinct multiprotein complexes, mTORC1 and mTORC2. Here we report a 3.2 Å resolution cryo-EM reconstruction of mTORC2. It reveals entangl...
In mycobacteria, transcriptional activator PafBC is responsible for upregulating the majority of genes induced by DNA damage. Understanding the mechanism of PafBC activation is impeded by a lack of structural information on this transcription factor that contains a widespread, but poorly understood WYL domain frequently encountered in bacterial tra...
Cotranslational protein targeting is a conserved process for membrane protein biogenesis. In Escherichia coli, the essential ATPase SecA was found to cotranslationally target a subset of nascent membrane proteins to the SecYEG translocase at the plasma membrane. The molecular mechanism of this pathway remains unclear. Here we use biochemical and cr...
Assembly pathway for mitoribosome
The biogenesis of ribosomes is a multistep process facilitated by assembly factors. Saurer et al. provided structural information on the maturation process of the mitochondrial ribosome, or mitoribosome, in the parasitic protozoan Trypanosoma brucei (see the Perspective by Karbstein). Cells evolved a dedicated mach...
Although the basic aspects of protein synthesis are preserved in all kingdoms of life, there are many important structural and functional differences between bacterial and the more complex eukaryotic ribosomes. High-resolution cryo-electron microscopy (cryo-EM) and X-ray crystallography structures of eukaryotic ribosomes have revealed the complex a...
Cotranslational processing of newly synthesized proteins is fundamental for correct protein maturation. Protein biogenesis factors are thought to bind nascent polypeptides not before they exit the ribosomal tunnel. Here, we identify a nascent chain recognition mechanism deep inside the ribosomal tunnel by an essential eukaryotic cytosolic chaperone...
In mycobacteria, transcriptional activator PafBC is responsible for upregulating the majority of genes induced by DNA damage. Understanding the mechanism of PafBC activation is impeded by a lack of structural information on this transcription factor that contains a widespread, but poorly understood WYL domain frequently encountered in bacterial tra...
Structure of the largest, most complex ribosome
Ribosomes are two-subunit ribonucleoprotein assemblies that catalyze the translation of messenger RNA into protein. Ribosomal RNAs (rRNAs) play key structural and functional roles. Ramrath et al. report the high-resolution structure of mitochondrial ribosomes from the unicellular parasite Trypanosoma...
Mitochondria maintain their own specialized protein synthesis machinery, which in mammals is used exclusively for the synthesis of the membrane proteins responsible for oxidative phosphorylation1,2. The initiation of protein synthesis in mitochondria differs substantially from bacterial or cytosolic translation systems. Mitochondrial translation in...
Biomolecular mass spectrometry has matured strongly over the past decades and has now reached a stage where it can provide deep insights into the structure and composition of large cellular assemblies. Here, we describe a three-tiered hybrid mass spectrometry approach that enables the dissection of macromolecular complexes in order to complement st...
First steps of translocation elucidated
Ribosomes synthesizing membrane or secretory proteins are targeted to the endoplasmic reticulum (ER) in eukaryotic cells by the signal recognition particle (SRP). Upon reaching the ER, the SRP interacts with its receptor to promote transfer of the signal sequence to the protein-conducting channel or transloco...
Final maturation of eukaryotic ribosomes occurs in the cytoplasm and requires the sequential removal of associated assembly factors and processing of the immature 20S pre-RNA Using cryo-electron microscopy (cryo-EM), we have determined the structure of a yeast cytoplasmic pre-40S particle in complex with Enp1, Ltv1, Rio2, Tsr1, and Pno1 assembly fa...
ELife digest
To grow and multiply, a living cell must take a variety of factors into account, such as its own energy levels and the availability of nutrients. A protein called mTOR sits at the core of a signaling pathway that integrates these and other sources information. Problems with the mTOR pathway contribute to several diseases including diab...
Mitochondrial ribosomes (mitoribosomes) almost exclusively synthesize essential components of the oxidative phosphorylation machinery. Dysfunction of mitochondrial protein biosynthesis leads to human diseases and plays an important role in the altered metabolism of cancer cells. Recent developments in cryo-electron microscopy enabled the structural...
Final maturation of eukaryotic ribosomes occurs in the cytoplasm and requires the sequential removal of associated assembly factors and processing of the immature 20S pre-RNA. Using cryo-electron microscopy (cryo-EM), we have determined the structure of a cytoplasmic pre-40S particle poised to initiate final maturation at a resolution of 3.4 Å. The...
The ribosome carries out the synthesis of proteins in every living cell. It consequently represents a frontline target in anti-microbial therapy. Tuberculosis ranks among the leading causes of death worldwide, due in large part to the combination of difficult-to-treat latency and antibiotic resistance. Here, we present the 3.3-Å cryo-EM structure o...
After having translated short upstream open reading frames, ribosomes can re-initiate translation on the same mRNA. This process, referred to as re-initiation, controls the translation of a large fraction of mammalian cellular mRNAs, many of which are important in cancer. Key ribosomal binding proteins involved in re-initiation are the eukaryotic t...
Close-up of the proposed fit of the SecYEG translocon bound via the SR to the quaternary complex. The depicted view is a cut through the DDM detergent micelle.
Close-up of the activated SRP-SR NG heterodimer bound to the distal site of the SRP RNA and to the surface of the ribosome.
Overview of the SRP, SR, SecYEG complex bound to the translating ribosome. The 3D map was filtered to 8 Å resolution. Coloring scheme is identical to the one used in the main figures.
Morphing of the SRP core region in the closed and the activated states. In the activated state, the signal sequence extends outward beyond the M-domain binding groove by 15Å.
Close-up of the M-domain (cyan) of the SRP protein bound to the signal sequence (magenta) in the activated sta te.
Supplementary Figures, Supplementary Tables and Supplementary References
During co-translational protein targeting, the signal recognition particle (SRP) binds to the translating ribosome displaying the signal sequence to deliver it to the SRP receptor (SR) on the membrane, where the signal peptide is transferred to the translocon. Using electron cryo-microscopy, we have determined the structure of a quaternary complex...
In all organisms, mRNA-directed protein synthesis is catalysed by ribosomes. Although the basic aspects of translation are preserved in all kingdoms of life, important differences are found in the process of translation initiation, which is rate-limiting and the most important step for translation regulation. While great strides had been taken towa...
Morph movie between trimer of pentamers from AaLS-wt and AaLS-13 around the 3-fold rotational symmetry axes. The mutated residues for AaLS-13 are colored as in Supplementary movie 2.
Morph movie between trimer of pentamers of AaLS-wt and AaLS-neg around 3-fold rotational symmetry axes. The mutated residues for AaLS-neg are colored as in Supplementary movie 1.
Morph movie between the AaLS-wt pentamer and the AaLS-13 pentamer. The mutated residues for AaLS-13 are shown as spheres, and the introduced negative charges from site-directed mutagenesis (R83E, T86E, T120E, and Q123E) and directed evolution (V115D, A118D, and K131E) are indicated in red and magenta, respectively. The other mutations from directed...
Morph movie of the 2-fold contact between AaLS-wt and AaLS-13, showing the hinge motion. The 2-fold contact exits at the pentamer-pentamer interface of each structure
Supplementary Figures and Supplementary Tables.
Proteins that self-assemble into regular shell-like polyhedra are useful, both in nature and in the laboratory, as molecular containers. Here we describe cryo-electron microscopy (EM) structures of two versatile encapsulation systems that exploit engineered electrostatic interactions for cargo loading. We show that increasing the number of negative...
Morph movie between the AaLS-wt pentamer and the AaLS-neg pentamer. The mutated residues for AaLS-neg are shown as spheres, and the introduced negative charges (R83E, T86E, T120E, and Q123E) are indicated in red.
Expanded View Figures PDF
Analogous to eukaryotic ubiquitination, proteins in actinobacteria can be post-translationally modified in a process referred to as pupylation, the covalent attachment of prokaryotic ubiquitin-like protein Pup to lysine side chains of the target protein via an isopeptide bond. Like in eukaryotes, an opposing activity counteracts the modification by...
Originally published, uncorrected article.
(PDF)
[This corrects the article DOI: 10.1371/journal.pbio.1002557.].
Citations
... RNA viruses, including SARS-CoV-2 have evolved impressive mechanisms to inhibit host cell translation and promote viral protein synthesis [5][6][7]. When SARS-CoV-2 infects a host cell, the 30 kb-long single-stranded capped and polyadenylated viral RNA genome is translated to produce non-structural proteins (Nsps) (Figure 1) [8]. ...
... Because eukaryotic mRNA translation relies on recruiting the 40S ribosomal subunit to the template mRNA [2], Nsp1 suppresses the global translation of the host with direct consequences on viral propagation because the host cell translation machinery is employed to promote the production of viral proteins [20,22]. This strategy is shared among different Betacoronaviruses, as shown by structural and biochemical studies using Nsp1 from MERS [29,30] and the Bat-Hp-CoV_Zhejiang2013, referred to as Bat-Hp Coronavirus [30]. In all cases, the C-terminal end anchors Nsp1 with high affinity to the mRNA entry channel in a conformation that clashes with the translated mRNA. ...
... This antigen is abundantly expressed in the salivary glands and kidneys (by immunouorescence studies), 31 and this molecular event may be responsible for the accumulation of biocidal radiation in healthy structures. Despite documented efforts to identify ligands specic to PSMA over GCPIII, 33,34 PSMA-targeted RLTs which show high tumor-to-salivary gland and tumor-to-kidney ratios have not yet been reported. ...
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... surface. The zinc-finger motive containing N-terminus of mammalian MAP1 is recognized by the nascent polypeptide associated complex (NAC), which administers MAP1 recruitment to the PTE 11 . In contrast, our recent structures of MAP2 reveal a (which was not certified by peer review) is the author/funder. ...
... To judge how common uL22 engagement is, we re-examined publicly available RTC maps for previously overlooked uL22 density. We found clear uL22 CTH density in maps from several recent studies (Figure 4-figure supplement 1; Gemmer et al., 2023b;Jaskolowski et al., 2023;Pauwels et al., 2023). Most importantly, it is present in subtomogram averages of RTCs transporting diverse endogenous nascent chains through intact microsomal membranes (Gemmer et al., 2023b), and the uL22 CTH density in those maps is just as strong as in the present dataset (~40% occupancy; Figure 4figure supplement 1A). ...
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... Two start codons were observed within these two mitogenomes: GTG and the standard codon ATG, which are also relatively common start codons in vertebrates [46][47][48][49]. There are multiple types of stop codons, including AGG, TAA, TAG, and an incomplete codon T. AGG serves as a codon for encoding arginine, but in mitochondria, owing to the absence of cognate tRNAs, this codon is reassigned to function as a stop codon [50] and terminates translation by interacting with mitochondrial release factor 1 [51,52]. The incomplete T stop codon could be completed by means of posttranscriptional polyadenylation [20]. ...
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... Since the official recognition of SARS-CoV-2 in January 2020 [1], a significant number of studies have been published, elucidating the characteristics, diagnosis methods, possible mechanisms, and severity of the disease, as well as immune responses to SARS-CoV-2 in people suffering from COVID-19 and information on the virus itself [4][5][6][7][8][9][10][11]. However, these studies largely focused on COVID-19 s ability to cause deadly disease in humans. ...
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... For cotranslational ER-targeting, NAC acts as a gatekeeper to shield nascent chains, which are not substrates for SRP, while facilitating recruitment of SRP to the ribosome. Another study shows that the Translocon Associated Protein (TRAP) may help recruiting ribosomes to the ER and subsequently aids in stabilizing the RNC-Sec61 complex and contributes to membrane protein biogenesis [57]. ...
... In some cases, they even reach millimolar levels 17 , which we term here hyper-resistance. IleRS1 and IleRS2 generally occur individually in bacteria, but there is a small group of Bacillaceae that carry both genes in the genome 21 . IleRS2 plays an important role in providing mupirocin resistance to bacteria in hospital environments, since mupirocin-resistant Staphylococcus aureus isolates acquired the ileS2 gene on a plasmid 22 . ...
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... Its large surface provided by the four charged and extended protein termini might have far-reaching implications on other RAFs that associate to the tunnel exit during translation. Work on NAC has already highlighted its importance in SRP regulation [22][23][24][25] , protein folding and proteostasis 26 as well as MAP1 coordination 11,27 . Its omnipresence in this early stage of co-translational protein maturation strongly implies an additional role in the regulation of acetylation. ...
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