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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 48 375-86 (2012)
Related entries: 4f02, 4f25

Cited: 79 times
EuropePMC logo PMID: 23041282

Abstract

Many RNA-binding proteins contain multiple single-strand nucleic acid-binding domains and assemble into large multiprotein messenger ribonucleic acid protein (mRNP) complexes. The mechanisms underlying the self-assembly of these complexes are largely unknown. In eukaryotes, the association of the translation factors polyadenylate-binding protein-1 (PABP) and eIF4G is essential for high-level expression of polyadenylated mRNAs. Here, we report the crystal structure of the ternary complex poly(A)(11)·PABP(1-190)·eIF4G(178-203) at 2.0 Å resolution. Our NMR and crystallographic data show that eIF4G interacts with the RRM2 domain of PABP. Analysis of the interaction by small-angle X-ray scattering, isothermal titration calorimetry, and electromobility shift assays reveals that this interaction is allosterically regulated by poly(A) binding to PABP. Furthermore, we have confirmed the importance of poly(A) for the endogenous PABP and eIF4G interaction in immunoprecipitation experiments using HeLa cell extracts. Our findings reveal interdomain allostery as a mechanism for cooperative assembly of RNP complexes.

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  1. The crystal structure of the Split End protein SHARP adds a new layer of complexity to proteins containing RNA recognition motifs. Arieti F, Gabus C, Tambalo M, Huet T, Round A, Thore S. Nucleic Acids Res 42 6742-6752 (2014)


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  1. How RNA-Binding Proteins Interact with RNA: Molecules and Mechanisms. Corley M, Burns MC, Yeo GW. Mol Cell 78 9-29 (2020)
  2. Mechanism and Regulation of Protein Synthesis in Saccharomyces cerevisiae. Dever TE, Kinzy TG, Pavitt GD. Genetics 203 65-107 (2016)
  3. eIF4F: a retrospective. Merrick WC. J Biol Chem 290 24091-24099 (2015)
  4. Translation initiation by cap-dependent ribosome recruitment: Recent insights and open questions. Shirokikh NE, Preiss T. Wiley Interdiscip Rev RNA 9 e1473 (2018)
  5. Mechanism, factors, and physiological role of nonsense-mediated mRNA decay. Fatscher T, Boehm V, Gehring NH. Cell Mol Life Sci 72 4523-4544 (2015)
  6. The La and related RNA-binding proteins (LARPs): structures, functions, and evolving perspectives. Maraia RJ, Mattijssen S, Cruz-Gallardo I, Conte MR. Wiley Interdiscip Rev RNA 8 (2017)
  7. The expanding universe of ribonucleoproteins: of novel RNA-binding proteins and unconventional interactions. Beckmann BM, Castello A, Medenbach J. Pflugers Arch 468 1029-1040 (2016)
  8. The "tale" of poly(A) binding protein: the MLLE domain and PAM2-containing proteins. Xie J, Kozlov G, Gehring K. Biochim Biophys Acta 1839 1062-1068 (2014)
  9. 'Black sheep' that don't leave the double-stranded RNA-binding domain fold. Gleghorn ML, Maquat LE. Trends Biochem Sci 39 328-340 (2014)
  10. mRNA length-sensing in eukaryotic translation: reconsidering the "closed loop" and its implications for translational control. Thompson MK, Gilbert WV. Curr Genet 63 613-620 (2017)
  11. The organization and regulation of mRNA-protein complexes. Rissland OS. Wiley Interdiscip Rev RNA 8 (2017)
  12. Applications of isothermal titration calorimetry - the research and technical developments from 2011 to 2015. Falconer RJ. J Mol Recognit 29 504-515 (2016)
  13. Quantitative studies of mRNA recruitment to the eukaryotic ribosome. Fraser CS. Biochimie 114 58-71 (2015)
  14. LARP1 and LARP4: up close with PABP for mRNA 3' poly(A) protection and stabilization. Mattijssen S, Kozlov G, Fonseca BD, Gehring K, Maraia RJ. RNA Biol 18 259-274 (2021)
  15. RNA and Proteins: Mutual Respect. Hall KB. F1000Res 6 345 (2017)
  16. Targeting IRES-dependent translation as a novel approach for treating Duchenne muscular dystrophy. Péladeau C, Jasmin BJ. RNA Biol 18 1238-1251 (2021)
  17. Structure and function of molecular machines involved in deadenylation-dependent 5'-3' mRNA degradation. Zhao Q, Pavanello L, Bartlam M, Winkler GS. Front Genet 14 1233842 (2023)
  18. The molecular basis of translation initiation and its regulation in eukaryotes. Brito Querido J, Díaz-López I, Ramakrishnan V. Nat Rev Mol Cell Biol (2023)

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  1. Comprehensive Identification of RNA-Binding Domains in Human Cells. Castello A, Fischer B, Frese CK, Horos R, Alleaume AM, Foehr S, Curk T, Krijgsveld J, Hentze MW. Mol Cell 63 696-710 (2016)
  2. Deep mutational scanning of an RRM domain of the Saccharomyces cerevisiae poly(A)-binding protein. Melamed D, Young DL, Gamble CE, Miller CR, Fields S. RNA 19 1537-1551 (2013)
  3. Translation of yes-associated protein (YAP) was antagonized by its circular RNA via suppressing the assembly of the translation initiation machinery. Wu N, Yuan Z, Du KY, Fang L, Lyu J, Zhang C, He A, Eshaghi E, Zeng K, Ma J, Du WW, Yang BB. Cell Death Differ 26 2758-2773 (2019)
  4. Inferring protein 3D structure from deep mutation scans. Rollins NJ, Brock KP, Poelwijk FJ, Stiffler MA, Gauthier NP, Sander C, Marks DS. Nat Genet 51 1170-1176 (2019)
  5. A fly trap mechanism provides sequence-specific RNA recognition by CPEB proteins. Afroz T, Skrisovska L, Belloc E, Guillén-Boixet J, Méndez R, Allain FH. Genes Dev 28 1498-1514 (2014)
  6. The interaction of cytoplasmic poly(A)-binding protein with eukaryotic initiation factor 4G suppresses nonsense-mediated mRNA decay. Fatscher T, Boehm V, Weiche B, Gehring NH. RNA 20 1579-1592 (2014)
  7. Approaching rational epitope vaccine design for hepatitis C virus with meta-server and multivalent scaffolding. He L, Cheng Y, Kong L, Azadnia P, Giang E, Kim J, Wood MR, Wilson IA, Law M, Zhu J. Sci Rep 5 12501 (2015)
  8. Poly(A) tail length regulates PABPC1 expression to tune translation in the heart. Chorghade S, Seimetz J, Emmons R, Yang J, Bresson SM, Lisio M, Parise G, Conrad NK, Kalsotra A. Elife 6 e24139 (2017)
  9. Solution structure of the two RNA recognition motifs of hnRNP A1 using segmental isotope labeling: how the relative orientation between RRMs influences the nucleic acid binding topology. Barraud P, Allain FH. J Biomol NMR 55 119-138 (2013)
  10. BTG2 bridges PABPC1 RNA-binding domains and CAF1 deadenylase to control cell proliferation. Stupfler B, Birck C, Séraphin B, Mauxion F. Nat Commun 7 10811 (2016)
  11. Control of translation and miRNA-dependent repression by a novel poly(A) binding protein, hnRNP-Q. Svitkin YV, Yanagiya A, Karetnikov AE, Alain T, Fabian MR, Khoutorsky A, Perreault S, Topisirovic I, Sonenberg N. PLoS Biol 11 e1001564 (2013)
  12. Molecular Basis for poly(A) RNP Architecture and Recognition by the Pan2-Pan3 Deadenylase. Schäfer IB, Yamashita M, Schuller JM, Schüssler S, Reichelt P, Strauss M, Conti E. Cell 177 1619-1631.e21 (2019)
  13. Dynamic recognition of the mRNA cap by Saccharomyces cerevisiae eIF4E. O'Leary SE, Petrov A, Chen J, Puglisi JD. Structure 21 2197-2207 (2013)
  14. The influence of microRNAs and poly(A) tail length on endogenous mRNA-protein complexes. Rissland OS, Subtelny AO, Wang M, Lugowski A, Nicholson B, Laver JD, Sidhu SS, Smibert CA, Lipshitz HD, Bartel DP. Genome Biol 18 211 (2017)
  15. Structure of the parallel duplex of poly(A) RNA: evaluation of a 50 year-old prediction. Safaee N, Noronha AM, Rodionov D, Kozlov G, Wilds CJ, Sheldrick GM, Gehring K. Angew Chem Int Ed Engl 52 10370-10373 (2013)
  16. A versatile assay for RNA-binding proteins in living cells. Strein C, Alleaume AM, Rothbauer U, Hentze MW, Castello A. RNA 20 721-731 (2014)
  17. Combining natural sequence variation with high throughput mutational data to reveal protein interaction sites. Melamed D, Young DL, Miller CR, Fields S. PLoS Genet 11 e1004918 (2015)
  18. PABPC1 exerts carcinogenesis in gastric carcinoma by targeting miR-34c. Zhu J, Ding H, Wang X, Lu Q. Int J Clin Exp Pathol 8 3794-3802 (2015)
  19. Cytoplasmic poly(A)-binding protein 1 (PABPC1) interacts with the RNA-binding protein hnRNPLL and thereby regulates immunoglobulin secretion in plasma cells. Peng Y, Yuan J, Zhang Z, Chang X. J Biol Chem 292 12285-12295 (2017)
  20. A network of RNA-binding proteins controls translation efficiency to activate anaerobic metabolism. Ho JJD, Balukoff NC, Theodoridis PR, Wang M, Krieger JR, Schatz JH, Lee S. Nat Commun 11 2677 (2020)
  21. Structural study of the Fox-1 RRM protein hydration reveals a role for key water molecules in RRM-RNA recognition. Krepl M, Blatter M, Cléry A, Damberger FF, Allain FHT, Sponer J. Nucleic Acids Res 45 8046-8063 (2017)
  22. The Jigsaw Puzzle of mRNA Translation Initiation in Eukaryotes: A Decade of Structures Unraveling the Mechanics of the Process. Hashem Y, Frank J. Annu Rev Biophys 47 125-151 (2018)
  23. The mRNA repressor TRIM71 cooperates with Nonsense-Mediated Decay factors to destabilize the mRNA of CDKN1A/p21. Torres-Fernández LA, Jux B, Bille M, Port Y, Schneider K, Geyer M, Mayer G, Kolanus W. Nucleic Acids Res 47 11861-11879 (2019)
  24. Phosphodiester modifications in mRNA poly(A) tail prevent deadenylation without compromising protein expression. Strzelecka D, Smietanski M, Sikorski PJ, Warminski M, Kowalska J, Jemielity J. RNA 26 1815-1837 (2020)
  25. Aromatic side-chain conformational switch on the surface of the RNA Recognition Motif enables RNA discrimination. Diarra Dit Konté N, Krepl M, Damberger FF, Ripin N, Duss O, Šponer J, Allain FH. Nat Commun 8 654 (2017)
  26. Characterization of the multimeric structure of poly(A)-binding protein on a poly(A) tail. Sawazaki R, Imai S, Yokogawa M, Hosoda N, Hoshino SI, Mio M, Mio K, Shimada I, Osawa M. Sci Rep 8 1455 (2018)
  27. Linkage and allostery in snRNP protein/RNA complexes. Williams SG, Hall KB. Biochemistry 53 3529-3539 (2014)
  28. Sbp1 modulates the translation of Pab1 mRNA in a poly(A)- and RGG-dependent manner. Brandariz-Núñez A, Zeng F, Lam QN, Jin H. RNA 24 43-55 (2018)
  29. Structural basis of nucleic acid binding by Nicotiana tabacum glycine-rich RNA-binding protein: implications for its RNA chaperone function. Khan F, Daniëls MA, Folkers GE, Boelens R, Saqlan Naqvi SM, van Ingen H. Nucleic Acids Res 42 8705-8718 (2014)
  30. Dynamic interaction of poly(A)-binding protein with the ribosome. Machida K, Shigeta T, Yamamoto Y, Ito T, Svitkin Y, Sonenberg N, Imataka H. Sci Rep 8 17435 (2018)
  31. Functional Segments on Intrinsically Disordered Regions in Disease-Related Proteins. Anbo H, Sato M, Okoshi A, Fukuchi S. Biomolecules 9 E88 (2019)
  32. Effect of PFOA on DNA Methylation and Alternative Splicing in Mouse Liver. Wen Y, Chen J, Li J, Arif W, Kalsotra A, Irudayaraj J. Toxicol Lett 329 38-46 (2020)
  33. Evolutionary history exposes radical diversification among classes of interaction partners of the MLLE domain of plant poly(A)-binding proteins. Jiménez-López D, Bravo J, Guzmán P. BMC Evol Biol 15 195 (2015)
  34. 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)
  35. Structural and biochemical analysis of the Hordeum vulgare L. HvGR-RBP1 protein, a glycine-rich RNA-binding protein involved in the regulation of barley plant development and stress response. Tripet BP, Mason KE, Eilers BJ, Burns J, Powell P, Fischer AM, Copié V. Biochemistry 53 7945-7960 (2014)
  36. The Leishmania PABP1-eIF4E4 interface: a novel 5'-3' interaction architecture for trans-spliced mRNAs. Dos Santos Rodrigues FH, Firczuk H, Breeze AL, Cameron AD, Walko M, Wilson AJ, Zanchin NIT, McCarthy JEG. Nucleic Acids Res 47 1493-1504 (2019)
  37. Prevalent RNA recognition motif duplication in the human genome. Tsai YS, Gomez SM, Wang Z. RNA 20 702-712 (2014)
  38. Recognition of Poly(A) RNA through Its Intrinsic Helical Structure. Tang TTL, Passmore LA. Cold Spring Harb Symp Quant Biol 84 21-30 (2019)
  39. Structure and Mechanism of Dimer-Monomer Transition of a Plant Poly(A)-Binding Protein upon RNA Interaction: Insights into Its Poly(A) Tail Assembly. Domingues MN, Sforça ML, Soprano AS, Lee J, de Souza TACB, Cassago A, Portugal RV, de Mattos Zeri AC, Murakami MT, Sadanandom A, de Oliveira PSL, Benedetti CE. J Mol Biol 427 2491-2506 (2015)
  40. The bent conformation of poly(A)-binding protein induced by RNA-binding is required for its translational activation function. Hong KY, Lee SH, Gu S, Kim E, An S, Kwon J, Lee JB, Jang SK. RNA Biol 14 370-377 (2017)
  41. Harnessing short poly(A)-binding protein-interacting peptides for the suppression of nonsense-mediated mRNA decay. Fatscher T, Gehring NH. Sci Rep 6 37311 (2016)
  42. Molecular Determinants and Specificity of mRNA with Alternatively-Spliced UPF1 Isoforms, Influenced by an Insertion in the 'Regulatory Loop'. Padariya M, Fahraeus R, Hupp T, Kalathiya U. Int J Mol Sci 22 12744 (2021)
  43. PABP prevents the untimely decay of select mRNA populations in human cells. Kajjo S, Sharma S, Chen S, Brothers WR, Cott M, Hasaj B, Jovanovic P, Larsson O, Fabian MR. EMBO J 41 e108650 (2022)
  44. Domain-functional analyses of PIWIL1 and PABPC1 indicate their synergistic roles in protein translation via 3'-UTRs of meiotic mRNAs. Wu Y, Xu K, Qi H. Biol Reprod 99 773-788 (2018)
  45. MicroRNP-mediated translational activation of nonadenylated mRNAs in a mammalian cell-free system. Wakiyama M, Ogami K, Iwaoka R, Aoki K, Hoshino SI. Genes Cells 23 332-344 (2018)
  46. Nuclear, Cytosolic, and Surface-Localized Poly(A)-Binding Proteins of Plasmodium yoelii. Minns AM, Hart KJ, Subramanian S, Hafenstein S, Lindner SE. mSphere 3 e00435-17 (2018)
  47. PABP1 Drives the Selective Translation of Influenza A Virus mRNA. de Rozières CM, Pequeno A, Shahabi S, Lucas TM, Godula K, Ghosh G, Joseph S. J Mol Biol 434 167460 (2022)
  48. The flip-flop configuration of the PABP-dimer leads to switching of the translation function. Gu S, Jeon HM, Nam SW, Hong KY, Rahman MS, Lee JB, Kim Y, Jang SK. Nucleic Acids Res 50 306-321 (2022)
  49. Interaction of HuDA and PABP at 5'UTR of mouse insulin2 regulates insulin biosynthesis. Pandey PR, Sarwade RD, Khalique A, Seshadri V. PLoS One 13 e0194482 (2018)
  50. Transcriptome analysis reveals the encystment-related lncRNA expression profile and coexpressed mRNAs in Pseudourostyla cristata. Pan N, Bhatti MZ, Zhang W, Ni B, Fan X, Chen J. Sci Rep 11 8274 (2021)
  51. Chemically Modified Poly(A) Analogs Targeting PABP: Structure Activity Relationship and Translation Inhibitory Properties. Perzanowska O, Smietanski M, Jemielity J, Kowalska J. Chemistry 28 e202201115 (2022)
  52. Paip2A inhibits translation by competitively binding to the RNA recognition motifs of PABPC1 and promoting its dissociation from the poly(A) tail. Sagae T, Yokogawa M, Sawazaki R, Ishii Y, Hosoda N, Hoshino SI, Imai S, Shimada I, Osawa M. J Biol Chem 298 101844 (2022)
  53. Analysis of domain organization and functional signatures of trypanosomatid keIF4Gs. Das S. Mol Cell Biochem 477 2415-2431 (2022)
  54. Mip6 binds directly to the Mex67 UBA domain to maintain low levels of Msn2/4 stress-dependent mRNAs. Martín-Expósito M, Gas ME, Mohamad N, Nuño-Cabanes C, Tejada-Colón A, Pascual-García P, de la Fuente L, Chaves-Arquero B, Merran J, Corden J, Conesa A, Pérez-Cañadillas JM, Bravo J, Rodríguez-Navarro S. EMBO Rep 20 e47964 (2019)
  55. Overexpressing CrePAPS Polyadenylate Activity Enhances Protein Translation and Accumulation in Chlamydomonas reinhardtii. Wang Q, Zhuang J, Ni S, Luo H, Zheng K, Li X, Lan C, Zhao D, Bai Y, Jia B, Hu Z. Mar Drugs 20 276 (2022)
  56. Pab1 acetylation at K131 decreases stress granule formation in Saccharomyces cerevisiae. Sivananthan S, Gosse JT, Huard S, Baetz K. J Biol Chem 299 102834 (2023)
  57. The Binding Specificity of PAB1 with Poly(A) mRNA, Regulated by Its Structural Folding. Padariya M, Kalathiya U. Biomedicines 10 2981 (2022)
  58. Uncovering a mammalian neural-specific poly(A) binding protein with unique properties. Sharma S, Kajjo S, Harra Z, Hasaj B, Delisle V, Ray D, Gutierrez RL, Carrier I, Kleinman C, Morris Q, Hughes TR, McInnes R, Fabian MR. Genes Dev 37 760-777 (2023)
  59. Upstream of N-Ras C-terminal cold shock domains mediate poly(A) specificity in a novel RNA recognition mode and bind poly(A) binding protein. Hollmann NM, Jagtap PKA, Linse JB, Ullmann P, Payr M, Murciano B, Simon B, Hub JS, Hennig J. Nucleic Acids Res 51 1895-1913 (2023)
  60. eIF4G1 N-terminal intrinsically disordered domain is a multi-docking station for RNA, Pab1, Pub1, and self-assembly. Chaves-Arquero B, Martínez-Lumbreras S, Sibille N, Camero S, Bernadó P, Jiménez MÁ, Zorrilla S, Pérez-Cañadillas JM. Front Mol Biosci 9 986121 (2022)


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