Three Stages of Nascent Protein Translocation Through the Ribosome Exit Tunnel
Jazyk angličtina Země Spojené státy americké Médium print
Typ dokumentu časopisecké články, přehledy
Grantová podpora
90254
Ministerstvo Školství, Mládeže a Tělovýchovy
23-05557S
Grantová Agentura České Republiky
A1_FCH_2024_001
Vysoká Škola Chemicko-technologická v Praze
A2_FCHI_2021_34
Vysoká Škola Chemicko-technologická v Praze
PubMed
39496527
DOI
10.1002/wrna.1873
Knihovny.cz E-zdroje
- Klíčová slova
- antibiotics, cotranslational events, protein folding, ribosome, translation,
- MeSH
- lidé MeSH
- proteosyntéza * MeSH
- ribozomy * metabolismus MeSH
- transport proteinů MeSH
- Check Tag
- lidé MeSH
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
All proteins in living organisms are produced in ribosomes that facilitate the translation of genetic information into a sequence of amino acid residues. During translation, the ribosome undergoes initiation, elongation, termination, and recycling. In fact, peptide bonds are formed only during the elongation phase, which comprises periodic association of transfer RNAs and multiple auxiliary proteins with the ribosome and the addition of an amino acid to the nascent polypeptide one at a time. The protein spends a considerable amount of time attached to the ribosome. Here, we conceptually divide this portion of the protein lifetime into three stages. We define each stage on the basis of the position of the N-terminus of the nascent polypeptide within the ribosome exit tunnel and the context of the catalytic center. We argue that nascent polypeptides experience a variety of forces that determine how they translocate through the tunnel and interact with the tunnel walls. We review current knowledge about nascent polypeptide translocation and identify several white spots in our understanding of the birth of proteins.
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Adams, J. M. 1968. “On the Release of the Formyl Group From Nascent Protein.” Journal of Molecular Biology 33: 571–589.
Arenz, S., L. V. Bock, M. Graf, et al. 2016. “A Combined Cryo‐EM and Molecular Dynamics Approach Reveals the Mechanism of ErmBL‐Mediated Translation Arrest.” Nature Communications 7: 12026.
Arthur, L. L., S. Pavlovic‐Djuranovic, K. S. Koutmou, R. Green, P. Szczesny, and S. Djuranovic. 2015. “Translational Control by Lysine‐Encoding A‐Rich Sequences.” Science Advances 1: e1500154.
Balchin, D., M. Hayer‐Hartl, and F. U. Hartl. 2016. “In Vivo Aspects of Protein Folding and Quality Control.” Science 353: aac4354.
Ban, N., P. Nissen, J. Hansen, P. B. Moore, and T. A. Steitz. 2000. “The Complete Atomic Structure of the Large Ribosomal Subunit at 2.4 Å Resolution.” Science 289: 905–920.
Beckert, B., E. C. Leroy, S. Sothiselvam, et al. 2021. “Structural and Mechanistic Basis for Translation Inhibition by Macrolide and Ketolide Antibiotics.” Nature Communications 12: 4466.
Bertolini, M., K. Fenzl, I. Kats, et al. 2021. “Interactions Between Nascent Proteins Translated by Adjacent Ribosomes Drive Homomer Assembly.” Science 371: 57–64.
Bhakta, S., S. Akbar, and J. Sengupta. 2019. “Cryo‐EM Structures Reveal Relocalization of MetAP in the Presence of Other Protein Biogenesis Factors at the Ribosomal Tunnel Exit.” Journal of Molecular Biology 431: 1426–1439.
Bhuiyan, S. H. 2000. “Assembly of Archaeal Signal Recognition Particle From Recombinant Components.” Nucleic Acids Research 28: 1365–1373.
Bhushan, S., T. Hoffmann, B. Seidelt, et al. 2011. “SecM‐Stalled Ribosomes Adopt an Altered Geometry at the Peptidyl Transferase Center.” PLoS Biology 9: e1000581.
Bingel‐Erlenmeyer, R., R. Kohler, G. Kramer, et al. 2008. “A Peptide Deformylase–Ribosome Complex Reveals Mechanism of Nascent Chain Processing.” Nature 452: 108–111.
Bissonnette, L., S. Champetier, J. P. Buisson, and P. H. Roy. 1991. “Characterization of the Nonenzymatic Chloramphenicol Resistance (cmlA) Gene of the In4 Integron of Tn1696: Similarity of the Product to Transmembrane Transport Proteins.” Journal of Bacteriology 173: 4493–4502.
Bock, L. V., S. Gabrielli, M. H. Kolář, and H. Grubmüller. 2023. “Simulation of Complex Biomolecular Systems: The Ribosome Challenge.” Annual Review of Biophysics 52: 1–28.
Bornemann, T., J. Jöckel, M. V. Rodnina, and W. Wintermeyer. 2008. “Signal Sequence–Independent Membrane Targeting of Ribosomes Containing Short Nascent Peptides Within the Exit Tunnel.” Nature Structural & Molecular Biology 15: 494–499.
Bui, P. T., and T. X. Hoang. 2016. “Folding and Escape of Nascent Proteins at Ribosomal Exit Tunnel.” Journal of Chemical Physics 144: 095102.
Bui, P. T., and T. X. Hoang. 2018. “Protein Escape at the Ribosomal Exit Tunnel: Effects of Native Interactions, Tunnel Length, and Macromolecular Crowding.” Journal of Chemical Physics 149: 045102.
Bui, P. T., and T. X. Hoang. 2020. “Protein Escape at the Ribosomal Exit Tunnel: Effect of the Tunnel Shape.” Journal of Chemical Physics 153: 045105.
Bui, P. T., and T. X. Hoang. 2021. “Hydrophobic and Electrostatic Interactions Modulate Protein Escape at the Ribosomal Exit Tunnel.” Biophysical Journal 120: 4798–4808.
Bui, P. T., and T. X. Hoang. 2023. “The Protein Escape Process at the Ribosomal Exit Tunnel Has Conserved Mechanisms Across the Domains of Life.” Journal of Chemical Physics 158: 015102.
Cassaignau, A. M., L. D. Cabrita, and J. Christodoulou. 2020. “How Does the Ribosome Fold the Proteome?” Annual Review of Biochemistry 89: 389–415.
Chadani, Y., T. Kanamori, T. Niwa, et al. 2023. “Mechanistic Dissection of Premature Translation Termination Induced by Acidic Residues‐Enriched Nascent Peptide.” Cell Reports 42: 42.
Chadani, Y., T. Niwa, T. Izumi, et al. 2017. “Intrinsic Ribosome Destabilization Underlies Translation and Provides an Organism With a Strategy of Environmental Sensing.” Molecular Cell 68: 528–539.e5.
Chan, S. H. S., T. Włodarski, J. O. Streit, et al. 2022. “The Ribosome Stabilizes Partially Folded Intermediates of a Nascent Multi‐Domain Protein.” Nature Chemistry 14: 1165–1173.
Chandrasekaran, V., S. Juszkiewicz, J. Choi, et al. 2019. “Mechanism of Ribosome Stalling During Translation of a Poly(A) Tail.” Nature Structural & Molecular Biology 26: 1132–1140.
Charneski, C. A., and L. D. Hurst. 2013. “Positively Charged Residues Are the Major Determinants of Ribosomal Velocity.” PLoS Biology 11: e1001508.
Chwastyk, M., and M. Cieplak. 2021. “Nascent Folding of Proteins Across the Three Domains of Life.” Frontiers in Molecular Biosciences 8: 8.
Ciryam, P., R. I. Morimoto, M. Vendruscolo, C. M. Dobson, and E. P. O'Brien. 2013. “In Vivo Translation Rates Can Substantially Delay the Cotranslational Folding of the Escherichia coli Cytosolic Proteome.” Proceedings of the National Academy of Sciences 110: E132–E140.
Cymer, F., N. Ismail, and G. Von Heijne. 2014. “Weak Pulling Forces Exerted on Nin‐Orientated Transmembrane Segments During Co‐Translational Insertion Into the Inner Membrane of Escherichia coli.” FEBS Letters 588: 1930–1934.
Dabrowski‐Tumanski, P., M. Piejko, S. Niewieczerzal, A. Stasiak, and J. I. Sulkowska. 2018. “Protein Knotting by Active Threading of Nascent Polypeptide Chain Exiting From the Ribosome Exit Channel.” Journal of Physical Chemistry B 122: 11616–11625.
Dao Duc, K., S. S. Batra, N. Bhattacharya, J. H. D. Cate, and Y. S. Song. 2019. “Differences in the Path to Exit the Ribosome Across the Three Domains of Life.” Nucleic Acids Research 47: 4198–4210.
Das, G., and U. Varshney. 2006. “Peptidyl‐tRNA Hydrolase and Its Critical Role in Protein Biosynthesis.” Microbiology 152: 2191–2195.
Davis, A. R., D. W. Gohara, and M.‐N. F. Yap. 2014. “Sequence Selectivity of Macrolide‐Induced Translational Attenuation.” Proceedings of the National Academy of Sciences 111: 15379–15384.
Deuerling, E., M. Gamerdinger, and S. G. Kreft. 2019. “Chaperone Interactions at the Ribosome.” Cold Spring Harbor Perspectives in Biology 11: a033977.
Duc, K. D., and Y. S. Song. 2018. “The Impact of Ribosomal Interference, Codon Usage, and Exit Tunnel Interactions on Translation Elongation Rate Variation.” PLoS Genetics 14: e1007166.
Eichmann, C., S. Preissler, R. Riek, and E. Deuerling. 2010. “Cotranslational Structure Acquisition of Nascent Polypeptides Monitored by NMR Spectroscopy.” Proceedings of the National Academy of Sciences 107: 9111–9116.
Fritch, B., A. Kosolapov, P. Hudson, et al. 2018. “Origins of the Mechanochemical Coupling of Peptide Bond Formation to Protein Synthesis.” Journal of the American Chemical Society 140: 5077–5087.
Fujiwara, K., K. Ito, and S. Chiba. 2018. “MifM‐Instructed Translation Arrest Involves Nascent Chain Interactions With the Exterior as Well as the Interior of the Ribosome.” Scientific Reports 8: 10311.
Gersteuer, F., M. Morici, S. Gabrielli, et al. 2024. “The SecM Arrest Peptide Traps a Pre‐Peptide Bond Formation State of the Ribosome.” Nature Communications 15: 2431.
Giglione, C., A. Boularot, and T. Meinnel. 2004. “Protein N‐Terminal Methionine Excision.” Cellular and Molecular Life Sciences: CMLS 61: 1455–1474.
Giglione, C., and T. Meinnel. 2001a. “Organellar Peptide Deformylases: Universality of the N‐Terminal Methionine Cleavage Mechanism.” Trends in Plant Science 6: 566–572.
Giglione, C., and T. Meinnel. 2001b. “Peptide Deformylase as an Emerging Target for Antiparasitic Agents.” Emerging Therapeutic Targets 5: 41–57.
Goldman, D. H., C. M. Kaiser, A. Milin, M. Righini, I. Tinoco, and C. Bustamante. 2015. “Mechanical Force Releases Nascent Chain–Mediated Ribosome Arrest In Vitro and In Vivo.” Science 348: 457–460.
Greber, B. J., and N. Ban. 2016. “Structure and Function of the Mitochondrial Ribosome.” Annual Review of Biochemistry 85: 103–132.
Green, R., and H. F. Noller. 1997. “Ribosomes And Translation.” Annual Review of Biochemistry 66: 679–716.
Gruschke, S., and M. Ott. 2010. “The Polypeptide Tunnel Exit of the Mitochondrial Ribosome Is Tailored to Meet the Specific Requirements of the Organelle.” BioEssays 32: 1050–1057.
Gu, S.‐Q., F. Peske, H.‐J. Wieden, M. V. Rodnina, and W. Wintermeyer. 2003. “The Signal Recognition Particle Binds to Protein L23 at the Peptide Exit of the Escherichia coli Ribosome.” RNA 9: 566–573.
Guzel, P., H. Z. Yildirim, M. Yuce, and O. Kurkcuoglu. 2020. “Exploring Allosteric Signaling in the Exit Tunnel of the Bacterial Ribosome by Molecular Dynamics Simulations and Residue Network Model.” Frontiers in Molecular Biosciences 7: 7.
Herrero Del Valle, A., B. Seip, I. Cervera‐Marzal, G. Sacheau, A. C. Seefeldt, and C. A. Innis. 2020. “Ornithine Capture by a Translating Ribosome Controls Bacterial Polyamine Synthesis.” Nature Microbiology 5: 554–561.
Hoffmann, A., B. Bukau, and G. Kramer. 2010. “Structure and Function of the Molecular Chaperone Trigger Factor.” Biochimica et Biophysica Acta (BBA) ‐ Molecular Cell Research 1803: 650–661.
Holtkamp, W., G. Kokic, M. Jäger, J. Mittelstaet, A. A. Komar, and M. V. Rodnina. 2015. “Cotranslational Protein Folding on the Ribosome Monitored in Real Time.” Science 350: 1104–1107.
Ishii, E., S. Chiba, N. Hashimoto, et al. 2015. “Nascent Chain‐Monitored Remodeling of the Sec Machinery for Salinity Adaptation of Marine Bacteria.” Proceedings of the National Academy of Sciences 112: E5513–E5522.
Ismail, N., R. Hedman, N. Schiller, and G. Von Heijne. 2012. “A Biphasic Pulling Force Acts on Transmembrane Helices During Translocon‐Mediated Membrane Integration.” Nature Structural & Molecular Biology 19: 1018–1022.
Ito, K., and S. Chiba. 2013. “Arrest Peptides: Cis ‐Acting Modulators of Translation.” Annual Review of Biochemistry 82: 171–202.
Jahn, M., J. Buchner, T. Hugel, and M. Rief. 2016. “Folding and Assembly of the Large Molecular Machine Hsp90 Studied in Single‐Molecule Experiments.” Proceedings of the National Academy of Sciences 113: 1232–1237.
Janzen, D. M., L. Frolova, and A. P. Geballe. 2002. “Inhibition of Translation Termination Mediated by an Interaction of Eukaryotic Release Factor 1 With a Nascent Peptidyl‐tRNA.” Molecular and Cellular Biology 22: 8562–8570.
Koch, M., J. Willi, U. Pradère, J. Hall, and N. Polacek. 2017. “Critical 23S rRNA Interactions for Macrolide‐Dependent Ribosome Stalling on the ErmCL Nascent Peptide Chain.” Nucleic Acids Research 45: 6717–6728.
Koffer‐Gutmann, A., and H. R. V. Arnstein. 1973. “The Presence of N‐Terminal Methionine on Nascent Protein of Rat Liver and Rabbit Reticulocytes and Its Cleavage During Polypeptide‐Chain Elongation.” Biochemical Journal 134: 969–983.
Kolář, M. H., G. Nagy, J. Kunkel, S. M. Vaiana, L. V. Bock, and H. Grubmüller. 2022. “Folding of VemP Into Translation‐Arresting Secondary Structure Is Driven by the Ribosome Exit Tunnel.” Nucleic Acids Research 50: 2258–2269.
Komar, A. A. 2009. “A Pause for Thought Along the Co‐Translational Folding Pathway.” Trends in Biochemical Sciences 34: 16–24.
Kosolapov, A., and C. Deutsch. 2009. “Tertiary Interactions Within the Ribosomal Exit Tunnel.” Nature Structural & Molecular Biology 16: 405–411.
Kramer, G., D. Boehringer, N. Ban, and B. Bukau. 2009. “The Ribosome as a Platform for Co‐Translational Processing, Folding and Targeting of Newly Synthesized Proteins.” Nature Structural & Molecular Biology 16: 589–597.
Kurzchalia, T. V., M. Wiedmann, A. S. Girshovich, E. S. Bochkareva, H. Bielka, and T. A. Rapoport. 1986. “The Signal Sequence of Nascent Preprolactin Interacts With the 54K Polypeptide of the Signal Recognition Particle.” Nature 320: 634–636.
Liu, K., J. E. Rehfus, E. Mattson, and C. M. Kaiser. 2017. “The Ribosome Destabilizes Native and Non‐Native Structures in a Nascent Multidomain Protein.” Protein Science 26: 1439–1451.
Locati, M. D., J. F. B. Pagano, G. Girard, et al. 2017. “Expression of Distinct Maternal and Somatic 5.8S, 18S, and 28S rRNA Types During Zebrafish Development.” RNA 23: 1188–1199.
Lovett, P. S. 1996. “Translation Attenuation Regulation of Chloramphenicol Resistance in Bacteria — A Review.” Gene 179: 157–162.
Lu, J., and C. Deutsch. 2005. “Folding Zones Inside the Ribosomal Exit Tunnel.” Nature Structural & Molecular Biology 12: 1123–1129.
Lu, J., and C. Deutsch. 2008. “Electrostatics in the Ribosomal Tunnel Modulate Chain Elongation Rates.” Journal of Molecular Biology 384: 73–86.
Luirink, J., S. High, H. Wood, A. Giner, D. Tollervey, and B. Dobberstein. 1992. “Signal‐Sequence Recognition by an Escherichia coli Ribonucleoprotein Complex.” Nature 359: 741–743.
Malkin, L. I., and A. Rich. 1967. “Partial Resistance of Nascent Polypeptide Chains to Proteolytic Digestion Due to Ribosomal Shielding.” Journal of Molecular Biology 26: 329–346.
Matheisl, S., O. Berninghausen, T. Becker, and R. Beckmann. 2015. “Structure of a Human Translation Termination Complex.” Nucleic Acids Research 43: 8615–8626.
McGrath, H., M. Černeková, and M. H. Kolář. 2022. “Binding of the Peptide Deformylase on the Ribosome Surface Modulates the Structure and Dynamics of the Exit Tunnel Interior.” Biophysical Journal 121: 4431–4451.
Melnikov, S., A. Ben‐Shem, N. Garreau de Loubresse, L. Jenner, G. Yusupova, and M. Yusupov. 2012. “One Core, Two Shells: Bacterial and Eukaryotic Ribosomes.” Nature Structural & Molecular Biology 19: 560–567.
Menninger, J. R. 1976. “Peptidyl Transfer RNA Dissociates During Protein Synthesis From Ribosomes of Escherichia coli.” Journal of Biological Chemistry 251: 3392–3398.
Mohammad, F., R. Green, and A. R. Buskirk. 2019. “A Systematically‐Revised Ribosome Profiling Method for Bacteria Reveals Pauses at Single‐Codon Resolution.” eLife 8: e42591.
Nagao, A., Y. Nakanishi, Y. Yamaguchi, et al. 2023. “Quality Control of Protein Synthesis in the Early Elongation Stage.” Nature Communications 14: 2704.
Nakatogawa, H., and K. Ito. 2002. “The Ribosomal Exit Tunnel Functions as a Discriminating Gate.” Cell 108: 629–636.
Nilsson, O. B., R. Hedman, J. Marino, et al. 2015. “Cotranslational Protein Folding Inside the Ribosome Exit Tunnel.” Cell Reports 12: 1533–1540.
Nilsson, O. B., A. Müller‐Lucks, G. Kramer, B. Bukau, and G. Von Heijne. 2016. “Trigger Factor Reduces the Force Exerted on the Nascent Chain by a Cotranslationally Folding Protein.” Journal of Molecular Biology 428: 1356–1364.
Nissley, D. A., Q. V. Vu, F. Trovato, et al. 2020. “Electrostatic Interactions Govern Extreme Nascent Protein Ejection Times From Ribosomes and Can Delay Ribosome Recycling.” Journal of the American Chemical Society 142: 6103–6110.
Norris, K., T. Hopes, and J. L. Aspden. 2021. “Ribosome Heterogeneity and Specialization in Development.” WIREs RNA 12: e1644.
Onoue, N., Y. Yamashita, N. Nagao, D. B. Goto, H. Onouchi, and S. Naito. 2011. “S‐Adenosyl‐l‐Methionine Induces Compaction of Nascent Peptide Chain Inside the Ribosomal Exit Tunnel Upon Translation Arrest in the Arabidopsis CGS1 Gene * 169.” Journal of Biological Chemistry 286: 14903–14912.
Poirot, O., and Y. Timsit. 2016. “Neuron‐Like Networks Between Ribosomal Proteins Within the Ribosome.” Scientific Reports 6: 26485.
Ramakrishnan, V. 2002. “Ribosome Structure and the Mechanism of Translation.” Cell 108: 557–572.
Ramu, H., N. Vázquez‐Laslop, D. Klepacki, et al. 2011. “Nascent Peptide in the Ribosome Exit Tunnel Affects Functional Properties of the A‐Site of the Peptidyl Transferase Center.” Molecular Cell 41: 321–330.
Ree, R., S. Varland, and T. Arnesen. 2018. “Spotlight on Protein N‐Terminal Acetylation.” Experimental & Molecular Medicine 50: 1–13.
Reva, O., and B. Tümmler. 2008. “Think Big – Giant Genes in Bacteria.” Environmental Microbiology 10: 768–777.
Samatova, E., A. A. Komar, and M. V. Rodnina. 2024. “How the Ribosome Shapes Cotranslational Protein Folding.” Current Opinion in Structural Biology 84: 102740.
Schluenzen, F., A. Tocilj, R. Zarivach, et al. 2000. “Structure of Functionally Activated Small Ribosomal Subunit at 3.3 Å Resolution.” Cell 102: 615–623.
Shanmuganathan, V., N. Schiller, A. Magoulopoulou, et al. 2019. “Structural and Mutational Analysis of the Ribosome‐Arresting Human XBP1u.” eLife 8: e46267.
Sharma, M. R., E. C. Koc, P. P. Datta, T. M. Booth, L. L. Spremulli, and R. K. Agrawal. 2003. “Structure of the Mammalian Mitochondrial Ribosome Reveals an Expanded Functional Role for Its Component Proteins.” Cell 115: 97–108.
Shi, Z., K. Fujii, K. M. Kovary, et al. 2017. “Heterogeneous Ribosomes Preferentially Translate Distinct Subpools of mRNAs Genome‐Wide.” Molecular Cell 67: 71–83.e7.
Shiber, A., K. Döring, U. Friedrich, et al. 2018. “Cotranslational Assembly of Protein Complexes in Eukaryotes Revealed by Ribosome Profiling.” Nature 561: 268–272.
Solbiati, J., A. Chapman‐Smith, J. L. Miller, C. G. Miller, and J. E. Cronan. 1999. “Processing of the N Termini of Nascent Polypeptide Chains Requires Deformylation Prior to Methionine Removal.” Journal of Molecular Biology 290: 607–614.
Su, T., J. Cheng, D. Sohmen, et al. 2017. “The Force‐Sensing Peptide VemP Employs Extreme Compaction and Secondary Structure Formation to Induce Ribosomal Stalling.” eLife 6: e25642.
Su, T., R. Kudva, T. Becker, et al. 2021. “Structural Basis of L‐Tryptophan‐Dependent Inhibition of Release Factor 2 by the TnaC Arrest Peptide.” Nucleic Acids Research 49: 9539–9547.
Syroegin, E. A., L. Flemmich, D. Klepacki, N. Vazquez‐Laslop, R. Micura, and Y. S. Polikanov. 2022. “Structural Basis for the Context‐Specific Action of the Classic Peptidyl Transferase Inhibitor Chloramphenicol.” Nature Structural & Molecular Biology 29: 152–161.
Tahirov, T. H., H. Oki, T. Tsukihara, et al. 1998. “Crystal Structure of Methionine Aminopeptidase From Hyperthermophile, Pyrococcus Furiosus.” Journal of Molecular Biology 284: 101–124.
Thommen, M., W. Holtkamp, and M. V. Rodnina. 2017. “Co‐Translational Protein Folding: Progress and Methods.” Current Opinion in Structural Biology 42: 83–89.
Tsai, A., G. Kornberg, M. Johansson, J. Chen, and J. D. Puglisi. 2014. “The Dynamics of SecM‐Induced Translational Stalling.” Cell Reports 7: 1521–1533.
Tu, L., P. Khanna, and C. Deutsch. 2014. “Transmembrane Segments Form Tertiary Hairpins in the Folding Vestibule of the Ribosome.” Journal of Molecular Biology 426: 185–198.
Tuller, T., I. Veksler‐Lublinsky, N. Gazit, M. Kupiec, E. Ruppin, and M. Ziv‐Ukelson. 2011. “Composite Effects of Gene Determinants on the Translation Speed and Density of Ribosomes.” Genome Biology 12: R110.
Van Der Stel, A.‐X., E. R. Gordon, A. Sengupta, et al. 2021. “Structural Basis for the Tryptophan Sensitivity of TnaC‐Mediated Ribosome Stalling.” Nature Communications 12: 5340.
Voss, N. R., M. Gerstein, T. A. Steitz, and P. B. Moore. 2006. “The Geometry of the Ribosomal Polypeptide Exit Tunnel.” Journal of Molecular Biology 360: 893–906.
Walter, P., and G. Blobel. 1982. “Signal Recognition Particle Contains a 7S RNA Essential for Protein Translocation Across the Endoplasmic Reticulum.” Nature 299: 691–698.
Weisblum, B. 1995. “Erythromycin Resistance by Ribosome Modification.” Antimicrobial Agents and Chemotherapy 39: 577–585.
Wells, J. N., L. T. Bergendahl, and J. A. Marsh. 2016. “Operon Gene Order Is Optimized for Ordered Protein Complex Assembly.” Cell Reports 14: 679–685.
Williams, N. K., and B. Dichtl. 2018. “Co‐Translational Control of Protein Complex Formation: A Fundamental Pathway of Cellular Organization?” Biochemical Society Transactions 46: 197–206.
Wilson, D. N. 2014. “Ribosome‐Targeting Antibiotics and Mechanisms of Bacterial Resistance.” Nature Reviews Microbiology 12: 35–48.
Wilson, D. N., S. Arenz, and R. Beckmann. 2016. “Translation Regulation via Nascent Polypeptide‐Mediated Ribosome Stalling.” Current Opinion in Structural Biology 37: 123–133.
Wimberly, B. T., D. E. Brodersen, W. M. Clemons Jr., et al. 2000. “Structure of the 30S Ribosomal Subunit.” Nature 407: 327–339.
Worthan, S. B., E. A. Franklin, C. Pham, M.‐N. F. Yap, and L. R. Cruz‐Vera. 2022. “The Identity of the Constriction Region of the Ribosomal Exit Tunnel Is Important to Maintain Gene Expression in Escherichia coli.” Microbiology Spectrum 10: e0226121.
Yang, C.‐I., H.‐H. Hsieh, and S.‐o. Shan. 2019. “Timing and Specificity of Cotranslational Nascent Protein Modification in Bacteria.” Proceedings of the National Academy of Sciences 116: 23050–23060.
Youngman, E. M., M. E. McDonald, and R. Green. 2008. “Peptide Release on the Ribosome: Mechanism and Implications for Translational Control.” Annual Review of Microbiology 62: 353–373.
Yu, S., S. Srebnik, and K. Dao Duc. 2023. “Geometric Differences in the Ribosome Exit Tunnel Impact the Escape of Small Nascent Proteins.” Biophysical Journal 122: 20–29.
Zhang, J. 2000. “Protein‐Length Distributions for the Three Domains of Life.” Trends in Genetics 16: 107–109.