1lj2 › Citations

Recognition of eIF4G by rotavirus NSP3 reveals a basis for mRNA circularization.

Groft CM, Burley SK
Mol Cell 9 1273-83 (2002)
Cited: 84 times
EuropePMC logo PMID: 12086624

Abstract

Rotaviruses, segmented double-stranded RNA viruses, co-opt the eukaryotic translation machinery with the aid of nonstructural protein 3 (NSP3), a rotaviral functional homolog of the cellular poly(A) binding protein (PABP). NSP3 binds to viral mRNA 3' consensus sequences and circularizes mRNA via interactions with eIF4G. Here, we present the X-ray structure of the C-terminal domain of NSP3 (NSP3-C) recognizing a fragment of eIF4GI. Homodimerization of NSP3-C yields a symmetric, elongated, largely alpha-helical structure with two hydrophobic eIF4G binding pockets at the dimer interface. Site-directed mutagenesis and isothermal titration calorimetry documented that NSP3 and PABP use analogous eIF4G recognition strategies, despite marked differences in tertiary structure.

Reviews - 1lj2 mentioned but not cited (1)

  1. Rotavirus non-structural proteins: structure and function. Hu L, Crawford SE, Hyser JM, Estes MK, Prasad BV. Curr Opin Virol 2 380-388 (2012)

Articles - 1lj2 mentioned but not cited (2)

  1. Distinguishing the genotype 1 genes and proteins of human Wa-like rotaviruses vs. porcine rotaviruses. Silva FD, Gregori F, McDonald SM. Infect Genet Evol 43 6-14 (2016)
  2. A novel computational strategy for defining the minimal protein molecular surface representation. Grassmann G, Miotto M, Di Rienzo L, Gosti G, Ruocco G, Milanetti E. PLoS One 17 e0266004 (2022)


Reviews citing this publication (28)

  1. Poly(A)-binding proteins: multifunctional scaffolds for the post-transcriptional control of gene expression. Mangus DA, Evans MC, Jacobson A. Genome Biol 4 223 (2003)
  2. Eukaryotic translation initiation factors and regulators. Sonenberg N, Dever TE. Curr Opin Struct Biol 13 56-63 (2003)
  3. Tinkering with translation: protein synthesis in virus-infected cells. Walsh D, Mathews MB, Mohr I. Cold Spring Harb Perspect Biol 5 a012351 (2013)
  4. Coiled coils: attractive protein folding motifs for the fabrication of self-assembled, responsive and bioactive materials. Apostolovic B, Danial M, Klok HA. Chem Soc Rev 39 3541-3575 (2010)
  5. 'Ribozoomin'--translation initiation from the perspective of the ribosome-bound eukaryotic initiation factors (eIFs). Valásek LS. Curr Protein Pept Sci 13 305-330 (2012)
  6. Assortment and packaging of the segmented rotavirus genome. McDonald SM, Patton JT. Trends Microbiol 19 136-144 (2011)
  7. Circular RNA, the Key for Translation. Prats AC, David F, Diallo LH, Roussel E, Tatin F, Garmy-Susini B, Lacazette E. Int J Mol Sci 21 E8591 (2020)
  8. Translation initiation: variations in the mechanism can be anticipated. Malys N, McCarthy JE. Cell Mol Life Sci 68 991-1003 (2011)
  9. Emerging themes in rotavirus cell entry, genome organization, transcription and replication. Jayaram H, Estes MK, Prasad BV. Virus Res 101 67-81 (2004)
  10. RNA-binding proteins in early development. Colegrove-Otero LJ, Minshall N, Standart N. Crit Rev Biochem Mol Biol 40 21-73 (2005)
  11. Non-canonical Translation in Plant RNA Viruses. Miras M, Miller WA, Truniger V, Aranda MA. Front Plant Sci 8 494 (2017)
  12. Poly(A)-binding protein (PABP): a common viral target. Smith RW, Gray NK. Biochem J 426 1-12 (2010)
  13. Harnessing self-assembled peptide nanoparticles in epitope vaccine design. Negahdaripour M, Golkar N, Hajighahramani N, Kianpour S, Nezafat N, Ghasemi Y. Biotechnol Adv 35 575-596 (2017)
  14. CBP80-promoted mRNP rearrangements during the pioneer round of translation, nonsense-mediated mRNA decay, and thereafter. Maquat LE, Hwang J, Sato H, Tang Y. Cold Spring Harb Symp Quant Biol 75 127-134 (2010)
  15. The organization and regulation of mRNA-protein complexes. Rissland OS. Wiley Interdiscip Rev RNA 8 (2017)
  16. How strong is the case for regulation of the initiation step of translation by elements at the 3' end of eukaryotic mRNAs? Kozak M. Gene 343 41-54 (2004)
  17. A survey of the year 2002 literature on applications of isothermal titration calorimetry. Cliff MJ, Ladbury JE. J Mol Recognit 16 383-391 (2003)
  18. Translation initiation of viral mRNAs. López-Lastra M, Ramdohr P, Letelier A, Vallejos M, Vera-Otarola J, Valiente-Echeverría F. Rev Med Virol 20 177-195 (2010)
  19. 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)
  20. Quantitative studies of mRNA recruitment to the eukaryotic ribosome. Fraser CS. Biochimie 114 58-71 (2015)
  21. The Role of the RNA-RNA Interactome in the Hepatitis C Virus Life Cycle. Romero-López C, Berzal-Herranz A. Int J Mol Sci 21 E1479 (2020)
  22. Stress Response and Translation Control in Rotavirus Infection. López S, Oceguera A, Sandoval-Jaime C. Viruses 8 E162 (2016)
  23. Recent advances in rotavirus reverse genetics and its utilization in basic research and vaccine development. Uprety T, Wang D, Li F. Arch Virol 166 2369-2386 (2021)
  24. Re-Examining Rotavirus Innate Immune Evasion: Potential Applications of the Reverse Genetics System. Antia A, Pinski AN, Ding S. mBio 13 e0130822 (2022)
  25. Treading a HOSTile path: Mapping the dynamic landscape of host cell-rotavirus interactions to explore novel host-directed curative dimensions. Patra U, Mukhopadhyay U, Mukherjee A, Dutta S, Chawla-Sarkar M. Virulence 12 1022-1062 (2021)
  26. Linking Α to Ω: diverse and dynamic RNA-based mechanisms to regulate gene expression by 5'-to-3' communication. Filbin ME, Kieft JS. F1000Res 5 F1000 Faculty Rev-2037 (2016)
  27. The Paradoxes of Viral mRNA Translation during Mammalian Orthoreovirus Infection. Guo Y, Parker JSL. Viruses 13 275 (2021)
  28. Single-molecule visualization of mRNA circularization during translation. Kim B, Seol J, Kim YK, Lee JB. Exp Mol Med 55 283-289 (2023)

Articles citing this publication (53)

  1. Mammalian poly(A)-binding protein is a eukaryotic translation initiation factor, which acts via multiple mechanisms. Kahvejian A, Svitkin YV, Sukarieh R, M'Boutchou MN, Sonenberg N. Genes Dev 19 104-113 (2005)
  2. Mammalian miRNA RISC recruits CAF1 and PABP to affect PABP-dependent deadenylation. Fabian MR, Mathonnet G, Sundermeier T, Mathys H, Zipprich JT, Svitkin YV, Rivas F, Jinek M, Wohlschlegel J, Doudna JA, Chen CY, Shyu AB, Yates JR, Hannon GJ, Filipowicz W, Duchaine TF, Sonenberg N. Mol Cell 35 868-880 (2009)
  3. The stem-loop binding protein is required for efficient translation of histone mRNA in vivo and in vitro. Sànchez R, Marzluff WF. Mol Cell Biol 22 7093-7104 (2002)
  4. Gene expression in peripheral blood mononuclear cells from patients with chronic fatigue syndrome. Kaushik N, Fear D, Richards SC, McDermott CR, Nuwaysir EF, Kellam P, Harrison TJ, Wilkinson RJ, Tyrrell DA, Holgate ST, Kerr JR. J Clin Pathol 58 826-832 (2005)
  5. Interdomain allostery promotes assembly of the poly(A) mRNA complex with PABP and eIF4G. Safaee N, Kozlov G, Noronha AM, Xie J, Wilds CJ, Gehring K. Mol Cell 48 375-386 (2012)
  6. Nuclear import of cytoplasmic poly(A) binding protein restricts gene expression via hyperadenylation and nuclear retention of mRNA. Kumar GR, Glaunsinger BA. Mol Cell Biol 30 4996-5008 (2010)
  7. Nuclear localization of cytoplasmic poly(A)-binding protein upon rotavirus infection involves the interaction of NSP3 with eIF4G and RoXaN. Harb M, Becker MM, Vitour D, Baron CH, Vende P, Brown SC, Bolte S, Arold ST, Poncet D. J Virol 82 11283-11293 (2008)
  8. Multiple elements in the eIF4G1 N-terminus promote assembly of eIF4G1•PABP mRNPs in vivo. Park EH, Walker SE, Lee JM, Rothenburg S, Lorsch JR, Hinnebusch AG. EMBO J 30 302-316 (2011)
  9. Rotavirus Nonstructural Protein NSP3 is not required for viral protein synthesis. Montero H, Arias CF, Lopez S. J Virol 80 9031-9038 (2006)
  10. Virus-mediated compartmentalization of the host translational machinery. Desmet EA, Anguish LJ, Parker JS. mBio 5 e01463-14 (2014)
  11. Expansion of family Reoviridae to include nine-segmented dsRNA viruses: isolation and characterization of a new virus designated Aedes pseudoscutellaris reovirus assigned to a proposed genus (Dinovernavirus). Attoui H, Mohd Jaafar F, Belhouchet M, Biagini P, Cantaloube JF, de Micco P, de Lamballerie X. Virology 343 212-223 (2005)
  12. Rotavirus viroplasm fusion and perinuclear localization are dynamic processes requiring stabilized microtubules. Eichwald C, Arnoldi F, Laimbacher AS, Schraner EM, Fraefel C, Wild P, Burrone OR, Ackermann M. PLoS One 7 e47947 (2012)
  13. Rotavirus infection induces the unfolded protein response of the cell and controls it through the nonstructural protein NSP3. Trujillo-Alonso V, Maruri-Avidal L, Arias CF, López S. J Virol 85 12594-12604 (2011)
  14. Dual mechanism for the translation of subgenomic mRNA from Sindbis virus in infected and uninfected cells. Sanz MA, Castelló A, Ventoso I, Berlanga JJ, Carrasco L. PLoS One 4 e4772 (2009)
  15. The molecular basis of coupling between poly(A)-tail length and translational efficiency. Xiang K, Bartel DP. Elife 10 e66493 (2021)
  16. Rotavirus NSP3 Is a Translational Surrogate of the Poly(A) Binding Protein-Poly(A) Complex. Gratia M, Sarot E, Vende P, Charpilienne A, Baron CH, Duarte M, Pyronnet S, Poncet D. J Virol 89 8773-8782 (2015)
  17. Cloning and sequence analysis of dsRNA segments 5, 6 and 7 of a novel non-group A, B, C adult rotavirus that caused an outbreak of gastroenteritis in China. Yang H, Makeyev EV, Kang Z, Ji S, Bamford DH, van Dijk AA. Virus Res 106 15-26 (2004)
  18. Circularization of the HIV-1 RNA genome. Ooms M, Abbink TE, Pham C, Berkhout B. Nucleic Acids Res 35 5253-5261 (2007)
  19. Eukaryotic initiation factor 4G suppresses nonsense-mediated mRNA decay by two genetically separable mechanisms. Joncourt R, Eberle AB, Rufener SC, Mühlemann O. PLoS One 9 e104391 (2014)
  20. Generation of Recombinant Rotavirus Expressing NSP3-UnaG Fusion Protein by a Simplified Reverse Genetics System. Philip AA, Perry JL, Eaton HE, Shmulevitz M, Hyser JM, Patton JT. J Virol 93 e01616-19 (2019)
  21. Rotavirus prevents the expression of host responses by blocking the nucleocytoplasmic transport of polyadenylated mRNAs. Rubio RM, Mora SI, Romero P, Arias CF, López S. J Virol 87 6336-6345 (2013)
  22. Rotavirus disrupts cytoplasmic P bodies during infection. Bhowmick R, Mukherjee A, Patra U, Chawla-Sarkar M. Virus Res 210 344-354 (2015)
  23. Rotavirus variant replicates efficiently although encoding an aberrant NSP3 that fails to induce nuclear localization of poly(A)-binding protein. Arnold MM, Brownback CS, Taraporewala ZF, Patton JT. J Gen Virol 93 1483-1494 (2012)
  24. Recruitment of host translation initiation factor eIF4G by the Vaccinia Virus ssDNA-binding protein I3. Zaborowska I, Kellner K, Henry M, Meleady P, Walsh D. Virology 425 11-22 (2012)
  25. Tyrosine phosphorylation modulates mitochondrial chaperonin Hsp60 and delays rotavirus NSP4-mediated apoptotic signaling in host cells. Chattopadhyay S, Mukherjee A, Patra U, Bhowmick R, Basak T, Sengupta S, Chawla-Sarkar M. Cell Microbiol 19 (2017)
  26. Active participation of cellular chaperone Hsp90 in regulating the function of rotavirus nonstructural protein 3 (NSP3). Dutta D, Chattopadhyay S, Bagchi P, Halder UC, Nandi S, Mukherjee A, Kobayashi N, Taniguchi K, Chawla-Sarkar M. J Biol Chem 286 20065-20077 (2011)
  27. Functional Cyclization of Eukaryotic mRNAs. Alekhina OM, Terenin IM, Dmitriev SE, Vassilenko KS. Int J Mol Sci 21 E1677 (2020)
  28. Structures required for poly(A) tail-independent translation overlap with, but are distinct from, cap-independent translation and RNA replication signals at the 3' end of Tobacco necrosis virus RNA. Shen R, Miller WA. Virology 358 448-458 (2007)
  29. Atomic structure of the translation regulatory protein NS1 of bluetongue virus. Kerviel A, Ge P, Lai M, Jih J, Boyce M, Zhang X, Zhou ZH, Roy P. Nat Microbiol 4 837-845 (2019)
  30. Experimental pathways towards developing a rotavirus reverse genetics system: synthetic full length rotavirus ssRNAs are neither infectious nor translated in permissive cells. Richards JE, Desselberger U, Lever AM. PLoS One 8 e74328 (2013)
  31. Rotavirus Strategies Against the Innate Antiviral System. López S, Sánchez-Tacuba L, Moreno J, Arias CF. Annu Rev Virol 3 591-609 (2016)
  32. Understanding the penetrance of intrinsic protein disorder in rotavirus proteome. Kumar D, Singh A, Kumar P, Uversky VN, Rao CD, Giri R. Int J Biol Macromol 144 892-908 (2020)
  33. Cell-line-induced mutation of the rotavirus genome alters expression of an IRF3-interacting protein. Kearney K, Chen D, Taraporewala ZF, Vende P, Hoshino Y, Tortorici MA, Barro M, Patton JT. EMBO J 23 4072-4081 (2004)
  34. Rotavirus replication is correlated with S/G2 interphase arrest of the host cell cycle. Glück S, Buttafuoco A, Meier AF, Arnoldi F, Vogt B, Schraner EM, Ackermann M, Eichwald C. PLoS One 12 e0179607 (2017)
  35. The molecular choreography of protein synthesis: translational control, regulation, and pathways. Chen J, Choi J, O'Leary SE, Prabhakar A, Petrov A, Grosely R, Puglisi EV, Puglisi JD. Q Rev Biophys 49 e11 (2016)
  36. Your personalized protein structure: Andrei N. Lupas fused to GCN4 adaptors. Deiss S, Hernandez Alvarez B, Bär K, Ewers CP, Coles M, Albrecht R, Hartmann MD. J Struct Biol 186 380-385 (2014)
  37. Challenging the Roles of NSP3 and Untranslated Regions in Rotavirus mRNA Translation. Gratia M, Vende P, Charpilienne A, Baron HC, Laroche C, Sarot E, Pyronnet S, Duarte M, Poncet D. PLoS One 11 e0145998 (2016)
  38. Functional Segments on Intrinsically Disordered Regions in Disease-Related Proteins. Anbo H, Sato M, Okoshi A, Fukuchi S. Biomolecules 9 E88 (2019)
  39. Nonstructural Protein σ1s Is Required for Optimal Reovirus Protein Expression. Phillips MB, Stuart JD, Simon EJ, Boehme KW. J Virol 92 e02259-17 (2018)
  40. Progressive Rotavirus Infection Downregulates Redox-Sensitive Transcription Factor Nrf2 and Nrf2-Driven Transcription Units. Patra U, Mukhopadhyay U, Mukherjee A, Sarkar R, Chawla-Sarkar M. Oxid Med Cell Longev 2020 7289120 (2020)
  41. Pub1p C-terminal RRM domain interacts with Tif4631p through a conserved region neighbouring the Pab1p binding site. Santiveri CM, Mirassou Y, Rico-Lastres P, Martínez-Lumbreras S, Pérez-Cañadillas JM. PLoS One 6 e24481 (2011)
  42. The rotaviral NSP3 protein stimulates translation of polyadenylated target mRNAs independently of its RNA-binding domain. Keryer-Bibens C, Legagneux V, Namanda-Vanderbeken A, Cosson B, Paillard L, Poncet D, Osborne HB. Biochem Biophys Res Commun 390 302-306 (2009)
  43. Rotavirus Infection Alters Splicing of the Stress-Related Transcription Factor XBP1. Duarte M, Vende P, Charpilienne A, Gratia M, Laroche C, Poncet D. J Virol 93 e01739-18 (2019)
  44. Translation of SARS-CoV-2 gRNA Is Extremely Efficient and Competitive despite a High Degree of Secondary Structures and the Presence of an uORF. Condé L, Allatif O, Ohlmann T, de Breyne S. Viruses 14 1505 (2022)
  45. Regulation of gene expression by the NSP1 and NSP3 non-structural proteins of rotavirus. Chung KT, McCrae MA. Arch Virol 156 2197-2203 (2011)
  46. Viperin, an IFN-Stimulated Protein, Delays Rotavirus Release by Inhibiting Non-Structural Protein 4 (NSP4)-Induced Intrinsic Apoptosis. Sarkar R, Nandi S, Lo M, Gope A, Chawla-Sarkar M. Viruses 13 1324 (2021)
  47. NIa-Pro of Papaya ringspot virus interacts with Carica papaya eukaryotic translation initiation factor 3 subunit G (CpeIF3G). Gao L, Tuo D, Shen W, Yan P, Li X, Zhou P. Virus Genes 50 97-103 (2015)
  48. Species A rotavirus NSP3 acquires its translation inhibitory function prior to stable dimer formation. Contreras-Treviño HI, Reyna-Rosas E, León-Rodríguez R, Ruiz-Ordaz BH, Dinkova TD, Cevallos AM, Padilla-Noriega L. PLoS One 12 e0181871 (2017)
  49. The viral nucleocapsid protein and the human RNA-binding protein Mex3A promote translation of the Andes orthohantavirus small mRNA. Vera-Otarola J, Castillo-Vargas E, Angulo J, Barriga FM, Batlle E, Lopez-Lastra M. PLoS Pathog 17 e1009931 (2021)
  50. Identification of mutations in the genome of rotavirus SA11 temperature-sensitive mutants D, H, I and J by whole genome sequences analysis and assignment of tsI to gene 7 encoding NSP3. Vende P, Gratia M, Duarte MD, Charpilienne A, Saguy M, Poncet D. Virus Res 176 144-154 (2013)
  51. Rotavirus Spike Protein VP4 Mediates Viroplasm Assembly by Association to Actin Filaments. Vetter J, Papa G, Seyffert M, Gunasekera K, De Lorenzo G, Wiesendanger M, Reymond JL, Fraefel C, Burrone OR, Eichwald C. J Virol 96 e0107422 (2022)
  52. Sequestering the 5'-cap for viral RNA packaging. Ding P, Summers MF. Bioessays 44 e2200104 (2022)
  53. Silver and gold in the Protein Data Bank. Carugo O. J Inorg Biochem 175 244-247 (2017)


Quick links