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HCV IRES Captures an Actively Translating 80S Ribosome.

Yokoyama T, Machida K, Iwasaki W, Shigeta T, Nishimoto M, Takahashi M, Sakamoto A, Yonemochi M, Harada Y, Shigematsu H, Shirouzu M, Tadakuma H, Imataka H, Ito T
Mol Cell 74 1205-1214.e8 (2019)
Related entries: 6ip5, 6ip8

Cited: 26 times
EuropePMC logo PMID: 31080011

Abstract

Translation initiation of hepatitis C virus (HCV) genomic RNA is induced by an internal ribosome entry site (IRES). Our cryoelectron microscopy (cryo-EM) analysis revealed that the HCV IRES binds to the solvent side of the 40S platform of the cap-dependently translating 80S ribosome. Furthermore, we obtained the cryo-EM structures of the HCV IRES capturing the 40S subunit of the IRES-dependently translating 80S ribosome. In the elucidated structures, the HCV IRES "body," consisting of domain III except for subdomain IIIb, binds to the 40S subunit, while the "long arm," consisting of domain II, remains flexible and does not impede the ongoing translation. Biochemical experiments revealed that the cap-dependently translating ribosome becomes a better substrate for the HCV IRES than the free ribosome. Therefore, the HCV IRES is likely to efficiently induce the translation initiation of its downstream mRNA with the captured translating ribosome as soon as the ongoing translation terminates.

Reviews citing this publication (13)

  1. Hallmarks of ribosomopathies. Kampen KR, Sulima SO, Vereecke S, De Keersmaecker K. Nucleic Acids Res 48 1013-1028 (2020)
  2. Hepatitis C Virus Translation Regulation. Niepmann M, Gerresheim GK. Int J Mol Sci 21 (2020)
  3. So close, no matter how far: multiple paths connecting transcription to mRNA translation in eukaryotes. Slobodin B, Dikstein R. EMBO Rep 21 e50799 (2020)
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  5. Delayed by Design: Role of Suboptimal Signal Peptidase Processing of Viral Structural Protein Precursors in Flaviviridae Virus Assembly. Alzahrani N, Wu MJ, Shanmugam S, Yi M. Viruses 12 (2020)
  6. Evaluating RNA Structural Flexibility: Viruses Lead the Way. Fairman CW, Lever AML, Kenyon JC. Viruses 13 2130 (2021)
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  8. Minding the message: tactics controlling RNA decay, modification, and translation in virus-infected cells. Burgess HM, Vink EI, Mohr I. Genes Dev 36 108-132 (2022)
  9. Non-Canonical Translation Initiation Mechanisms Employed by Eukaryotic Viral mRNAs. Sorokin II, Vassilenko KS, Terenin IM, Kalinina NO, Agol VI, Dmitriev SE. Biochemistry (Mosc) 86 1060-1094 (2021)
  10. RNA-Binding Proteins as Regulators of Internal Initiation of Viral mRNA Translation. López-Ulloa B, Fuentes Y, Pizarro-Ortega MS, López-Lastra M. Viruses 14 188 (2022)
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  12. The Diverse Genomic Landscape of Diamond-Blackfan Anemia: Two Novel Variants and a Mini-Review. Pelagiadis I, Kyriakidis I, Katzilakis N, Kosmeri C, Veltra D, Sofocleous C, Glentis S, Kattamis A, Makis A, Stiakaki E. Children (Basel) 10 1812 (2023)
  13. The tale of two flaviviruses: subversion of host pathways by RNA shapes in dengue and hepatitis C viral RNA genomes. Shivaprasad S, Sarnow P. Curr Opin Microbiol 59 79-85 (2021)

Articles citing this publication (13)

  1. The viral protein NSP1 acts as a ribosome gatekeeper for shutting down host translation and fostering SARS-CoV-2 translation. Tidu A, Janvier A, Schaeffer L, Sosnowski P, Kuhn L, Hammann P, Westhof E, Eriani G, Martin F. RNA rna.078121.120 (2020)
  2. Synthetic Antibody Binding to a Preorganized RNA Domain of Hepatitis C Virus Internal Ribosome Entry Site Inhibits Translation. Koirala D, Lewicka A, Koldobskaya Y, Huang H, Piccirilli JA. ACS Chem Biol 15 205-216 (2020)
  3. A complex IRES at the 5'-UTR of a viral mRNA assembles a functional 48S complex via an uAUG intermediate. Neupane R, Pisareva VP, Rodriguez CF, Pisarev AV, Fernández IS. Elife 9 (2020)
  4. Molecular architecture of 40S translation initiation complexes on the hepatitis C virus IRES. Brown ZP, Abaeva IS, De S, Hellen CUT, Pestova TV, Frank J. EMBO J 41 e110581 (2022)
  5. A parasitic fungus employs mutated eIF4A to survive on rocaglate-synthesizing Aglaia plants. Chen M, Kumakura N, Saito H, Muller R, Nishimoto M, Mito M, Gan P, Ingolia NT, Shirasu K, Ito T, Shichino Y, Iwasaki S. Elife 12 e81302 (2023)
  6. Dynamic interplay between RPL3- and RPL3L-containing ribosomes modulates mitochondrial activity in the mammalian heart. Milenkovic I, Santos Vieira HG, Lucas MC, Ruiz-Orera J, Patone G, Kesteven S, Wu J, Feneley M, Espadas G, Sabidó E, Hübner N, van Heesch S, Völkers M, Novoa EM. Nucleic Acids Res 51 5301-5324 (2023)
  7. METTL18-mediated histidine methylation of RPL3 modulates translation elongation for proteostasis maintenance. Matsuura-Suzuki E, Shimazu T, Takahashi M, Kotoshiba K, Suzuki T, Kashiwagi K, Sohtome Y, Akakabe M, Sodeoka M, Dohmae N, Ito T, Shinkai Y, Iwasaki S. Elife 11 e72780 (2022)
  8. RNA-responsive elements for eukaryotic translational control. Zhao EM, Mao AS, de Puig H, Zhang K, Tippens ND, Tan X, Ran FA, Han I, Nguyen PQ, Chory EJ, Hua TY, Ramesh P, Thompson DB, Oh CY, Zigon ES, English MA, Collins JJ. Nat Biotechnol 40 539-545 (2022)
  9. Cap-independent translation and a precisely located RNA sequence enable SARS-CoV-2 to control host translation and escape anti-viral response. Slobodin B, Sehrawat U, Lev A, Hayat D, Zuckerman B, Fraticelli D, Ogran A, Ben-Shmuel A, Bar-David E, Levy H, Ulitsky I, Dikstein R. Nucleic Acids Res 50 8080-8092 (2022)
  10. Human-rabbit Hybrid Translation System to Explore the Function of Modified Ribosomes. Matsuura-Suzuki E, Toh H, Iwasaki S. Bio Protoc 13 e4714 (2023)
  11. 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)
  12. Systematic detection of tertiary structural modules in large RNAs and RNP interfaces by Tb-seq. Patel S, Sexton AN, Strine MS, Wilen CB, Simon MD, Pyle AM. Nat Commun 14 3426 (2023)
  13. Various miRNAs compensate the role of miR-122 on HCV replication. Ono C, Fukuhara T, Li S, Wang J, Sato A, Izumi T, Fauzyah Y, Yamamoto T, Morioka Y, Dokholyan NV, Standley DM, Matsuura Y. PLoS Pathog 16 e1008308 (2020)


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