145
Views
0
CrossRef citations to date
0
Altmetric
Research paper

Enhanced binding of guanylated poly(A) RNA by the LaM domain of LARP1

, , , , & ORCID Icon
Pages 7-16 | Accepted 08 Jul 2024, Published online: 17 Jul 2024

References

  • Bayfield MA, Yang R, Maraia RJ. Conserved and divergent features of the structure and function of La and La-related proteins (LARPs). Biochim Biophys Acta. 2010;1799(5–6):365–378. doi: 10.1016/j.bbagrm.2010.01.011
  • Mattijssen S, Kozlov G, Fonseca BD, et al. LARP1 and LARP4: up close with PABP for mRNA 3’ poly(A) protection and stabilization. RNA Biol. 2021;18(2):259–274. doi: 10.1080/15476286.2020.1868753
  • Bousquet-Antonelli C, Deragon JM. A comprehensive analysis of the La-motif protein superfamily. RNA. 2009;15(5):750–764. doi: 10.1261/rna.1478709
  • Deragon JM. Distribution, organization an evolutionary history of La and LARPs in eukaryotes. RNA Biol. 2021;18(2):159–167. doi: 10.1080/15476286.2020.1739930
  • Merret R, Martino L, Bousquet-Antonelli C, et al. The association of a La module with the PABP-interacting motif PAM2 is a recurrent evolutionary process that led to the neofunctionalization of La-related proteins. RNA. 2013;19(1):36–50. doi: 10.1261/rna.035469.112
  • Maraia RJ, Mattijssen S, Cruz-Gallardo I, et al. The La and related RNA-binding proteins (LARPs): structures, functions, and evolving perspectives. Wiley Interdiscip Rev RNA. 2017:8(6. doi: 10.1002/wrna.1430
  • Kozlov G, Mattijssen S, Jiang J, et al. Structural basis of 3’-end poly(A) RNA recognition by LARP1. Nucleic Acids Res. 2022;50(16):9534–9547. doi: 10.1093/nar/gkac696
  • Lahr RM, Fonseca BD, Ciotti GE, et al. La-related protein 1 (LARP1) binds the mRNA cap, blocking eIF4F assembly on TOP mRNAs. Elife. 2017;6. doi: 10.7554/eLife.24146
  • Schneider C, Erhard F, Binotti B, et al. An unusual mode of baseline translation adjusts cellular protein synthesis capacity to metabolic needs. Cell Rep. 2022;41(2):111467. doi: 10.1016/j.celrep.2022.111467
  • Fuentes P, Pelletier J, Martinez-Herraez C, et al. The 40S-LARP1 complex reprograms the cellular translatome upon mTOR inhibition to preserve the protein synthetic capacity. Sci Adv. 2021. 7(48):eabg9275.
  • Philippe L, van den Elzen AMG, Watson MJ, et al. Global analysis of LARP1 translation targets reveals tunable and dynamic features of 5’ TOP motifs. Proc Natl Acad Sci USA. 2020;117(10):5319–5328. doi: 10.1073/pnas.1912864117
  • Goering R, Arora A, Pockalny MC, et al. RNA localization mechanisms transcend cell morphology. Elife. 2023;12:12. doi: 10.7554/eLife.80040
  • Fonseca BD, Zakaria C, Jia JJ, et al. La-related protein 1 (LARP1) represses terminal oligopyrimidine (TOP) mRNA translation downstream of mTOR complex 1 (mTORC1). J Biol Chem. 2015;290(26):15996–16020. doi: 10.1074/jbc.M114.621730
  • Berman AJ, Thoreen CC, Dedeic Z, et al. Controversies around the function of LARP1. RNA Biol. 2021;18(2):207–217. doi: 10.1080/15476286.2020.1733787
  • Al-Ashtal HA, Rubottom CM, Leeper TC, et al. The LARP1 La-module recognizes both ends of TOP mRNAs. RNA Biol. 2021;18(2):248–258. doi: 10.1080/15476286.2019.1669404
  • Philippe L, Vasseur JJ, Debart F, et al. La-related protein 1 (LARP1) repression of TOP mRNA translation is mediated through its cap-binding domain and controlled by an adjacent regulatory region. Nucleic Acids Res. 2018;46(3):1457–1469. doi: 10.1093/nar/gkx1237
  • Jia JJ, Lahr RM, Solgaard MT, et al. mTORC1 promotes TOP mRNA translation through site-specific phosphorylation of LARP1. Nucleic Acids Res. 2021;49(6):3461–3489. doi: 10.1093/nar/gkaa1239
  • Mura M, Hopkins TG, Michael T, et al. LARP1 post-transcriptionally regulates mTOR and contributes to cancer progression. Oncogene. 2015;34(39):5025–5036. doi: 10.1038/onc.2014.428
  • Hopkins TG, Mura M, Al-Ashtal HA, et al. The RNA-binding protein LARP1 is a post-transcriptional regulator of survival and tumorigenesis in ovarian cancer. Nucleic Acids Res. 2016;44(3):1227–1246. doi: 10.1093/nar/gkv1515
  • Hong S, Freeberg MA, Han T, et al. LARP1 functions as a molecular switch for mTORC1-mediated translation of an essential class of mRNAs. Elife. 2017;6. doi: 10.7554/eLife.25237
  • Smith EM, Benbahouche NEH, Morris K, et al. The mTOR regulated RNA-binding protein LARP1 requires PABPC1 for guided mRNA interaction. Nucleic Acids Res. 2021;49(1):458–478. doi: 10.1093/nar/gkaa1189
  • To TL, Cuadros AM, Shah H, et al. A compendium of genetic modifiers of mitochondrial dysfunction reveals intra-organelle buffering. Cell. 2019;179(5):1222–1238 e17. doi: 10.1016/j.cell.2019.10.032
  • Haneke K, Schott J, Lindner D, et al. CDK1 couples proliferation with protein synthesis. J Cell Biol. 2020;219(3). doi: 10.1083/jcb.201906147
  • Alfano C, Sanfelice D, Babon J, et al. Structural analysis of cooperative RNA binding by the La motif and central RRM domain of human La protein. Nat Struct Mol Biol. 2004;11(4):323–329. doi: 10.1038/nsmb747
  • Teplova M, Yuan YR, Phan AT, et al. Structural basis for recognition and sequestration of UUU(OH) 3’ temini of nascent RNA polymerase III transcripts by La, a rheumatic disease autoantigen. Mol Cell. 2006;21(1):75–85. doi: 10.1016/j.molcel.2005.10.027
  • Kotik-Kogan O, Valentine ER, Sanfelice D, et al. Structural analysis reveals conformational plasticity in the recognition of RNA 3’ ends by the human La protein. Structure. 2008;16(6):852–862. doi: 10.1016/j.str.2008.02.021
  • Martino L, Pennell S, Kelly G, et al. Synergic interplay of the La motif, RRM1 and the interdomain linker of LARP6 in the recognition of collagen mRNA expands the RNA binding repertoire of the La module. Nucleic Acids Res. 2015;43(1):645–660. doi: 10.1093/nar/gku1287
  • Eichhorn CD, Chug R, Feigon J. hLARP7 C-terminal domain contains an xRRM that binds the 3’ hairpin of 7SK RNA. Nucleic Acids Res. 2016;44(20):9977–9989. doi: 10.1093/nar/gkw833
  • Eichhorn CD, Yang Y, Repeta L, et al. Structural basis for recognition of human 7SK long noncoding RNA by the La-related protein Larp7. Proc Natl Acad Sci USA. 2018;115(28):E6457–E6466. doi: 10.1073/pnas.1806276115
  • Cruz-Gallardo I, Martino L, Kelly G, et al. LARP4A recognizes polyA RNA via a novel binding mechanism mediated by disordered regions and involving the PAM2w motif, revealing interplay between PABP, LARP4A and mRNA. Nucleic Acids Res. 2019;47(8):4272–4291. doi: 10.1093/nar/gkz144
  • Yang Y, Liu S, Egloff S, et al. Structural basis of RNA conformational switching in the transcriptional regulator 7SK RNP. Mol Cell. 2022;82(9):1724–1736 e7. doi: 10.1016/j.molcel.2022.03.001
  • Uchikawa E, Natchiar KS, Han X, et al. Structural insight into the mechanism of stabilization of the 7SK small nuclear RNA by LARP7. Nucleic Acids Res. 2015;43(6):3373–3388. doi: 10.1093/nar/gkv173
  • Lizarrondo J, Dock-Bregeon AC, Martino L, et al. Structural dynamics in the La-module of La-related proteins. RNA Biol. 2021;18(2):194–206. doi: 10.1080/15476286.2020.1733799
  • Ogami K, Oishi Y, Sakamoto K, et al. mTOR- and LARP1-dependent regulation of TOP mRNA poly(A) tail and ribosome loading. Cell Rep. 2022;41(4):111548. doi: 10.1016/j.celrep.2022.111548
  • Park J, Kim M, Yi H, et al. Short poly(A) tails are protected from deadenylation by the LARP1-PABP complex. Nat Struct Mol Biol. 2023;30(3):330–338. doi: 10.1038/s41594-023-00930-y
  • Aoki K, Adachi S, Homoto M, et al. LARP1 specifically recognizes the 3’ terminus of poly(A) mRNA. FEBS Lett. 2013;587(14):2173–2178. doi: 10.1016/j.febslet.2013.05.035
  • Mattijssen S, Kozlov G, Gaidamakov S, et al. The isolated La-module of LARP1 mediates 3’ poly(A) protection and mRNA stabilization, dependent on its intrinsic PAM2 binding to PABPC1. RNA Biol. 2021;18(2):275–289. doi: 10.1080/15476286.2020.1860376
  • Rhodes D, Lipps HJ. G-quadruplexes and their regulatory roles in biology. Nucleic Acids Res. 2015;43(18):8627–8637. doi: 10.1093/nar/gkv862
  • Zhang Z, Vogele J, Mrazikova K, et al. Phosphorothioate substitutions in RNA structure studied by molecular dynamics simulations, QM/MM calculations, and NMR experiments. J Phys Chem B. 2021;125(3):825–840. doi: 10.1021/acs.jpcb.0c10192
  • Kerkhofs K, Garg J, Fafard-Couture E, et al. Altered tRNA processing is linked to a distinct and unusual La protein in Tetrahymena thermophila. Nat Commun. 2022;13(1):7332. doi: 10.1038/s41467-022-34796-3
  • Cassidy KC, Lahr RM, Kaminsky JC, et al. Capturing the mechanism underlying TOP mRNA binding to LARP1. Structure. 2019;27(12):1771–1781 e5. doi: 10.1016/j.str.2019.10.006
  • Gentilella A, Moron-Duran FD, Fuentes P, et al. Autogenous control of 5‘TOP mRNA stability by 40S ribosomes. Mol Cell. 2017;67(1):55–70 e4. doi: 10.1016/j.molcel.2017.06.005
  • Chang H, Lim J, Ha M, et al. TAIL-seq: genome-wide determination of poly(A) tail length and 3’ end modifications. Mol Cell. 2014;53(6):1044–1052. doi: 10.1016/j.molcel.2014.02.007
  • Lim J, Kim D, Lee YS, et al. Mixed tailing by TENT4A and TENT4B shields mRNA from rapid deadenylation. Science. 2018;361(6403):701–704. doi: 10.1126/science.aam5794
  • Yoo CJ, Wolin SL. The yeast La protein is required for the 3’ endonucleolytic cleavage that matures tRNA precursors. Cell. 1997;89(3):393–402. doi: 10.1016/S0092-8674(00)80220-2
  • Chakshusmathi G, Kim SD, Rubinson DA, et al. A La protein requirement for efficient pre-tRNA folding. Embo J. 2003;22(24):6562–6572. doi: 10.1093/emboj/cdg625
  • Jahns H, Taneja N, Willoughby JLS, et al. Chirality matters: stereo-defined phosphorothioate linkages at the termini of small interfering RNAs improve pharmacology in vivo. Nucleic Acids Res. 2022;50(3):1221–1240. doi: 10.1093/nar/gkab544
  • Crooke ST, Seth PP, Vickers TA, et al. The interaction of phosphorothioate-containing RNA targeted drugs with proteins is a critical determinant of the therapeutic effects of these agents. J Am Chem Soc. 2020;142(35):14754–14771. doi: 10.1021/jacs.0c04928
  • Copp W, Denisov AY, Xie J, et al. Influence of nucleotide modifications at the C2’ position on the Hoogsteen base-paired parallel-stranded duplex of poly(A) RNA. Nucleic Acids Res. 2017;45(17):10321–10331. doi: 10.1093/nar/gkx713
  • Delaglio F, Grzesiek S, Vuister GW, et al. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR. 1995;6(3):277–293. doi: 10.1007/BF00197809
  • Goddard TD, Kneller DG. SPARKY 3. San Francisco: University of California; 2008.
  • Otwinowski Z, Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 1997;276:307–326.
  • McCoy AJ, Grosse-Kunstleve RW, Adams PD, et al. Phaser crystallographic software. J Appl Crystallogr. 2007;40(Pt 4):658–674. doi: 10.1107/S0021889807021206
  • Emsley P, Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr. 2004;60(Pt 12 Pt 1):2126–2132. doi: 10.1107/S0907444904019158
  • Adams PD, Afonine PV, Bunkoczi G, et al. The Phenix software for automated determination of macromolecular structures. Methods. 2011;55(1):94–106. doi: 10.1016/j.ymeth.2011.07.005
  • Winn MD, Murshudov GN, Papiz MZ. Macromolecular TLS refinement in REFMAC at moderate resolutions. Macromol Crystallogr. 2003;374:300–321.