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Crystal Structures of the uL3 Mutant Ribosome: Illustration of the Importance of Ribosomal Proteins for Translation Efficiency.

Mailliot J, Garreau de Loubresse N, Yusupova G, Meskauskas A, Dinman JD, Yusupov M
J Mol Biol 428 2195-202 (2016)
Cited: 15 times
EuropePMC logo PMID: 26906928

Abstract

The ribosome has been described as a ribozyme in which ribosomal RNA is responsible for peptidyl-transferase reaction catalysis. The W255C mutation of the universally conserved ribosomal protein uL3 has diverse effects on ribosome function (e.g., increased affinities for transfer RNAs, decreased rates of peptidyl-transfer), and cells harboring this mutation are resistant to peptidyl-transferase inhibitors (e.g., anisomycin). These observations beg the question of how a single amino acid mutation may have such wide ranging consequences. Here, we report the structure of the vacant yeast uL3 W255C mutant ribosome by X-ray crystallography, showing a disruption of the A-site side of the peptidyl-transferase center (PTC). An additional X-ray crystallographic structure of the anisomycin-containing mutant ribosome shows that high concentrations of this inhibitor restore a "WT-like" configuration to this region of the PTC, providing insight into the resistance mechanism of the mutant. Globally, our data demonstrate that ribosomal protein uL3 is structurally essential to ensure an optimal and catalytically efficient organization of the PTC, highlighting the importance of proteins in the RNA-centered ribosome.

Articles - 5fci mentioned but not cited (1)

  1. Crystal Structures of the uL3 Mutant Ribosome: Illustration of the Importance of Ribosomal Proteins for Translation Efficiency. Mailliot J, Garreau de Loubresse N, Yusupova G, Meskauskas A, Dinman JD, Yusupov M. J Mol Biol 428 2195-2202 (2016)


Reviews citing this publication (3)

  1. Ribosome Biogenesis and Cancer: Overview on Ribosomal Proteins. Pecoraro A, Pagano M, Russo G, Russo A. Int J Mol Sci 22 5496 (2021)
  2. Emerging Roles of Gemin5: From snRNPs Assembly to Translation Control. Martinez-Salas E, Embarc-Buh A, Francisco-Velilla R. Int J Mol Sci 21 E3868 (2020)
  3. Nervous-Like Circuits in the Ribosome Facts, Hypotheses and Perspectives. Timsit Y, Bennequin D. Int J Mol Sci 20 E2911 (2019)

Articles citing this publication (11)

  1. Structure and assembly model for the Trypanosoma cruzi 60S ribosomal subunit. Liu Z, Gutierrez-Vargas C, Wei J, Grassucci RA, Ramesh M, Espina N, Sun M, Tutuncuoglu B, Madison-Antenucci S, Woolford JL, Tong L, Frank J. Proc Natl Acad Sci U S A 113 12174-12179 (2016)
  2. The RNA-binding protein Gemin5 binds directly to the ribosome and regulates global translation. Francisco-Velilla R, Fernandez-Chamorro J, Ramajo J, Martinez-Salas E. Nucleic Acids Res 44 8335-8351 (2016)
  3. Mechanistic insights into the slow peptide bond formation with D-amino acids in the ribosomal active site. Melnikov SV, Khabibullina NF, Mairhofer E, Vargas-Rodriguez O, Reynolds NM, Micura R, Söll D, Polikanov YS. Nucleic Acids Res 47 2089-2100 (2019)
  4. Evolution of ribosomal protein network architectures. Timsit Y, Sergeant-Perthuis G, Bennequin D. Sci Rep 11 625 (2021)
  5. The Peptidyl Transferase Center: a Window to the Past. Tirumalai MR, Rivas M, Tran Q, Fox GE. Microbiol Mol Biol Rev 85 e0010421 (2021)
  6. Global translation inhibition yields condition-dependent de-repression of ribosome biogenesis mRNAs. Cheng Z, Brar GA. Nucleic Acids Res 47 5061-5073 (2019)
  7. A functional connection between translation elongation and protein folding at the ribosome exit tunnel in Saccharomyces cerevisiae. Rodríguez-Galán O, García-Gómez JJ, Rosado IV, Wei W, Méndez-Godoy A, Pillet B, Alekseenko A, Steinmetz LM, Pelechano V, Kressler D, de la Cruz J. Nucleic Acids Res 49 206-220 (2021)
  8. Rpl3l gene deletion in mice reduces heart weight over time. Grimes KM, Prasad V, Huo J, Kuwabara Y, Vanhoutte D, Baldwin TA, Bowers SLK, Johansen AKZ, Sargent MA, Lin SJ, Molkentin JD. Front Physiol 14 1054169 (2023)
  9. A Legionella toxin exhibits tRNA mimicry and glycosyl transferase activity to target the translation machinery and trigger a ribotoxic stress response. Subramanian A, Wang L, Moss T, Voorhies M, Sangwan S, Stevenson E, Pulido EH, Kwok S, Chalkley RJ, Li KH, Krogan NJ, Swaney DL, Burlingame AL, Floor SN, Sil A, Walter P, Mukherjee S. Nat Cell Biol 25 1600-1615 (2023)
  10. RPL3L-containing ribosomes determine translation elongation dynamics required for cardiac function. Shiraishi C, Matsumoto A, Ichihara K, Yamamoto T, Yokoyama T, Mizoo T, Hatano A, Matsumoto M, Tanaka Y, Matsuura-Suzuki E, Iwasaki S, Matsushima S, Tsutsui H, Nakayama KI. Nat Commun 14 2131 (2023)
  11. Concentration and time-dependent amyloidogenic characteristics of intrinsically disordered N-terminal region of Saccharomyces cerevisiae Stm1. Subbaiah S P V, Uttamrao PP, Das U, Sundaresan S, Rathinavelan T. Front Microbiol 14 1206945 (2023)


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