The LARP1 La-Module recognizes both ends of TOP mRNAs

References

• Bousquet-Antonelli C, Deragon JM. A comprehensive analysis of the La-motif protein superfamily. RNA. 2009;15:750–764.
   PubMed Web of Science ®Google Scholar
• 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.
   Web of Science ®Google Scholar
• 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;1799:365–378.
   PubMed Web of Science ®Google Scholar
• Dong G, Chakshusmathi G, Wolin SL, et al. Structure of the La motif: a winged helix domain mediates RNA binding via a conserved aromatic patch. EMBO J. 2004;23:1000–1007.
   PubMed Web of Science ®Google Scholar
• Alfano C, Babon J, Kelly G, et al. Resonance assignment and secondary structure of an N-terminal fragment of the human La protein. J Biomol NMR. 2003;27:93–94.
   PubMed Web of Science ®Google Scholar
• Clery A, Blatter M, Allain FH. RNA recognition motifs: boring? Not quite. Curr Opin Struct Biol. 2008;18:290–298.
   PubMed Web of Science ®Google Scholar
• Teplova M, Yuan YR, Phan AT, et al. Structural basis for recognition and sequestration of UUU(OH) 3ʹ temini of nascent RNA polymerase III transcripts by La, a rheumatic disease autoantigen. Mol Cell. 2006;21:75–85.
   PubMed Web of Science ®Google Scholar
• 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;11:323–329.
   PubMed Web of Science ®Google Scholar
• 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;43:3373–3388.
   PubMed Web of Science ®Google Scholar
• 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;43:645–660.
   PubMed Web of Science ®Google Scholar
• Isabel Cruz-Gallardo LM, Geoff Kelly R, Atkinson A, et al. LARP4A recognizes polyA RNA via a novel binding mechanism mediated by disordered regions and involving the PAM2w motif, revealing. Nucleic Acids Res. 2019;47(8):4272–4291.
   PubMed Web of Science ®Google Scholar
• Maraia RJ, Mattijssen S, Cruz-Gallardo I, et al. The La and related RNA-binding proteins (LARPs): structures, functions, and evolving perspectives. WIREs RNA. 2017;8:e1430.
   Google Scholar
• Chakshusmathi G, Kim SD, Rubinson DA, et al. A La protein requirement for efficient pre-tRNA folding. EMBO J. 2003;22:6562–6572.
   PubMed Web of Science ®Google Scholar
• Krueger BJ, Jeronimo C, Roy BB, et al. LARP7 is a stable component of the 7SK snRNP while P-TEFb, HEXIM1 and hnRNP A1 are reversibly associated. Nucleic Acids Res. 2008;36:2219–2229.
   PubMed Web of Science ®Google Scholar
• Cai L, Fritz D, Stefanovic L, et al. Binding of LARP6 to the conserved 5ʹ stem-loop regulates translation of mRNAs encoding type I collagen. J Mol Biol. 2010;395:309–326.
   PubMed Web of Science ®Google Scholar
• Stefanovic L, Longo L, Zhang Y, et al. Characterization of binding of LARP6 to the 5ʹ stem-loop of collagen mRNAs: implications for synthesis of type I collagen. RNA Biol. 2014;11:1386–1401.
   PubMed Web of Science ®Google Scholar
• Schäffler K, Schulz K, Hirmer A, et al. A stimulatory role for the La-related protein 4B in translation. RNA. 2010;16:1488–1499.
   PubMed Web of Science ®Google Scholar
• Yang R, Gaidamakov SA, Xie J, et al. La-related protein 4 binds poly(A), interacts with the poly(A)-binding protein MLLE domain via a variant PAM2w motif, and can promote mRNA stability. Mol Cell Biol. 2011;31:542–556.
   PubMed Web of Science ®Google Scholar
• Küspert M, Murakawa Y, Schäffler K, et al. LARP4B is an AU-rich sequence associated factor that promotes mRNA accumulation and translation. RNA. 2015;21:1294–1305.
   Google Scholar
• Fonseca BD, Lahr RM, Damgaard CK, et al. LARP1 on TOP of ribosome production. WIREs RNA. 2018; 9.
   Google Scholar
• Tcherkezian J, Cargnello M, Romeo Y, et al. Proteomic analysis of cap-dependent translation identifies LARP1 as a key regulator of 5ʹTOP mRNA translation. Genes Dev. 2014;28:357–371.
   PubMed Web of Science ®Google Scholar
• Sungki Hong MAF, Han T, Kamath A, et al. LARP1 functions as a molecular switch for mTORC1-mediated translation of an essential class of mRNAs. eLife. 2017;6:e25237.
   PubMed Web of Science ®Google Scholar
• Philippe L, Vasseur J, 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;46:1457–1469.
   PubMed Web of Science ®Google Scholar
• 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;290:15996–16020.
   PubMed Web of Science ®Google Scholar
• Lahr RM, Fonseca BD, Ciotti CE, et al. La-related protein 1 (LARP1) binds the mRNA cap, blocking eIF4F assembly on TOP mRNAs. eLife. 2017;6:e24146.
   PubMed Web of Science ®Google Scholar
• Aoki K, Adachi S, Homoto M, et al. LARP1 specifically recognizes the 3ʹ terminus of poly(A) mRNA. FEBS Lett. 2013;587:2173–2178.
   PubMed Web of Science ®Google Scholar
• Meyuhas O, Kahan T. The race to decipher the top secrets of TOP mRNAs. Biochim Biophys Acta. 2014;1849(7):801–811.
   PubMed Web of Science ®Google Scholar
• Thoreen CC, Chantranupong L, Keys HR, et al. A unifying model for mTORC1-mediated regulation of mRNA translation. Nature. 2012;485:109–113.
   PubMed Web of Science ®Google Scholar
• Burrows C, Abd Latip N, Lam SJ, et al. The RNA binding protein Larp1 regulates cell division, apoptosis and cell migration. Nucleic Acids Res. 2010;38:5542–5553.
   PubMed Web of Science ®Google Scholar
• Lahr RM, Mack SM, Heroux A, et al. The La-related protein 1-specific domain repurposes HEAT-like repeats to directly bind a 5ʹTOP sequence. Nucleic Acids Res. 2015;43:8077–8088.
   PubMed Web of Science ®Google Scholar
• Avni D, Shama S, Gabrizio Loreni MO. Vertebrate mRNAs with a 5ʹ-terminal pyrimidine tract are candidates for translational repression in quiescent cells: characterizationof the translational cis-regulatory element. Mol Cell Biol. 1994;14:3822–3833.
   PubMed Web of Science ®Google Scholar
• 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:e25237.
   Google Scholar
• Wells SE, Hillner PE, Vale RD, et al. Circularization of mRNA by eukaryotic translation initiation factors. Mol Cell. 1998;2:135–140.
   PubMed Web of Science ®Google Scholar
• Afonina ZA, Myasnikov AG, Shirokov VA, et al. Formation of circular polyribosomes on eukaryotic mRNA without cap-structure and poly(A)-tail: a cryo electron tomography study. Nucleic Acids Res. 2014;42:9461–9469.
   PubMed Web of Science ®Google Scholar
• Vicens Q, Kieft JS, Rissland OS. Revisiting the closed-loop model and the nature of mRNA 5′–3′ communication. Mol Cell. 2018;72:805–812.
   PubMed Web of Science ®Google Scholar
• Choe J, Lin S, Zhang W, et al. mRNA circularization by METTL3–eIF3h enhances translation and promotes oncogenesis. Nature. 2018;561:556–560.
   PubMed Web of Science ®Google Scholar
• Mura M, Hopkins TG, Michael T, et al. LARP1 post-transcriptionally regulates mTOR and contributes to cancer progression. Oncogene. 2014;34:5025–5036.
   PubMed Web of Science ®Google Scholar
• Hopkins TG, Mura M, Abd Latip N, et al. The RNA-binding protein LARP1 regulates survival and tumorigenesis in ovarian cancer. London, UK: Imperial College London; 2015.
   Google Scholar
• Nykamp K, Lee MH, Kimble J. C. elegans La-related protein, LARP-1, localizes to germline P bodies and attenuates Ras-MAPK signaling during oogenesis. RNA. 2008;14:1378–1389.
   PubMed Web of Science ®Google Scholar
• Decker CJ, Parker R. P-bodies and stress granules: possible roles in the control of translation and mRNA degradation. Cold Spring Harb Perspect Biol. 2012;4:a012286-a012286.
   PubMed Web of Science ®Google Scholar
• Wilbertz JH, Voigt F, Horvathova I, et al. Single-molecule imaging of mRNA localization and regulation during the integrated stress response. Mol Cell. 2019;73:946–958.
   PubMed Web of Science ®Google Scholar
• Cardinali B, Carissimi C, Gravina P, et al. La protein is associated with terminal oligopyrimidine mRNAs in actively translating polysomes. J Biol Chem. 2003;278:35145–35151.
   PubMed Web of Science ®Google Scholar
• Crosio C, Boyl PP, Loreni F, et al. La protein has a positive effect on the translation of TOP mRNAs in vivo. Nucleic Acids Res. 2000;28:2927–2934.
   PubMed Web of Science ®Google Scholar
• Ali N, Pruijn GJM, Kenan‖ DJ, et al. Human La antigen is required for the hepatitis C virus internal ribosome entry site-mediated translation. J Biol Chem. 2000;275:27531–27540.
   PubMed Web of Science ®Google Scholar
• Meerovitch K, Svitkin YV, Lee HS, et al. La autoantigen enhances and corrects aberrant translation of poliovirus RNA in reticulocyte lysate. J Virol. 1993;67:3798–3807.
   PubMed Web of Science ®Google Scholar
• Izumi RE, Das S, Barat B, et al. A peptide from autoantigen la blocks poliovirus and hepatitis C virus cap-independent translation and reveals a single tyrosine critical for La RNA binding and translation stimulation. J Virol. 2004;78:3763–3776.
   PubMed Web of Science ®Google Scholar
• Kim YK, Back SH, Rho J, et al. La autoantigen enhances translation of BiP mRNA. Nucleic Acids Res. 2001;29:5009–5016.
   PubMed Web of Science ®Google Scholar
• Vinayak J, Marrella SA, Hussain RH, et al. Human La binds mRNAs through contacts to the poly(A) tail. Nucleic Acids Res. 2018;4:4228–4240.
   Google Scholar
• Savitzky A, Golay MJE. Smoothing + Differentiation of Data by Simplified Least Squares Procedures. Anal Chem. 1964;36:1627–1639.
   Web of Science ®Google Scholar