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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.

Yang R, Gaidamakov SA, Xie J, Lee J, Martino L, Kozlov G, Crawford AK, Russo AN, Conte MR, Gehring K, Maraia RJ
Mol Cell Biol 31 542-56 (2011)
Cited: 64 times
EuropePMC logo PMID: 21098120

Abstract

The conserved RNA binding protein La recognizes UUU-3'OH on its small nuclear RNA ligands and stabilizes them against 3'-end-mediated decay. We report that newly described La-related protein 4 (LARP4) is a factor that can bind poly(A) RNA and interact with poly(A) binding protein (PABP). Yeast two-hybrid analysis and reciprocal immunoprecipitations (IPs) from HeLa cells revealed that LARP4 interacts with RACK1, a 40S ribosome- and mRNA-associated protein. LARP4 cosediments with 40S ribosome subunits and polyribosomes, and its knockdown decreases translation. Mutagenesis of the RNA binding or PABP interaction motifs decrease LARP4 association with polysomes. Several translation and mRNA metabolism-related proteins use a PAM2 sequence containing a critical invariant phenylalanine to make direct contact with the MLLE domain of PABP, and their competition for the MLLE is thought to regulate mRNA homeostasis. Unlike all ∼150 previously analyzed PAM2 sequences, LARP4 contains a variant PAM2 (PAM2w) with tryptophan in place of the phenylalanine. Binding and nuclear magnetic resonance (NMR) studies have shown that a peptide representing LARP4 PAM2w interacts with the MLLE of PABP within the affinity range measured for other PAM2 motif peptides. A cocrystal of PABC bound to LARP4 PAM2w shows tryptophan in the pocket in PABC-MLLE otherwise occupied by phenylalanine. We present evidence that LARP4 expression stimulates luciferase reporter activity by promoting mRNA stability, as shown by mRNA decay analysis of luciferase and cellular mRNAs. We propose that LARP4 activity is integrated with other PAM2 protein activities by PABP as part of mRNA homeostasis.

Reviews - 3pkn mentioned but not cited (2)

  1. 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)
  2. The La-related proteins: structures and interactions of a versatile superfamily of RNA-binding proteins. Dock-Bregeon AC, Lewis KA, Conte MR. RNA Biol 18 178-193 (2021)

Articles - 3pkn mentioned but not cited (3)

  1. 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. Yang R, Gaidamakov SA, Xie J, Lee J, Martino L, Kozlov G, Crawford AK, Russo AN, Conte MR, Gehring K, Maraia RJ. Mol Cell Biol 31 542-556 (2011)
  2. Crystal Structure of a Variant PAM2 Motif of LARP4B Bound to the MLLE Domain of PABPC1. Grimm C, Pelz JP, Schneider C, Schäffler K, Fischer U. Biomolecules 10 E872 (2020)
  3. Interactome-Based Machine Learning Predicts Potential Therapeutics for COVID-19. Ghosh N, Saha I, Gambin A. ACS Omega 8 13840-13854 (2023)


Reviews citing this publication (10)

  1. Handshakes and Fights: The Regulatory Interplay of RNA-Binding Proteins. Dassi E. Front Mol Biosci 4 67 (2017)
  2. The La-Related Proteins, a Family with Connections to Cancer. Stavraka C, Blagden S. Biomolecules 5 2701-2722 (2015)
  3. 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)
  4. Poly(A) RNA-binding proteins and polyadenosine RNA: new members and novel functions. Wigington CP, Williams KR, Meers MP, Bassell GJ, Corbett AH. Wiley Interdiscip Rev RNA 5 601-622 (2014)
  5. 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)
  6. Controversies around the function of LARP1. Berman AJ, Thoreen CC, Dedeic Z, Chettle J, Roux PP, Blagden SP. RNA Biol 18 207-217 (2021)
  7. Nonsense-mediated RNA decay: an emerging modulator of malignancy. Tan K, Stupack DG, Wilkinson MF. Nat Rev Cancer 22 437-451 (2022)
  8. Stabilize and connect: the role of LARP7 in nuclear non-coding RNA metabolism. Hasler D, Meister G, Fischer U. RNA Biol 18 290-303 (2021)
  9. La proteins couple use of sequence-specific and non-specific binding modes to engage RNA substrates. Bayfield MA, Vinayak J, Kerkhofs K, Mansouri-Noori F. RNA Biol 18 168-177 (2021)
  10. Nonsense-Mediated mRNA Decay as a Mediator of Tumorigenesis. Nagar P, Islam MR, Rahman MA. Genes (Basel) 14 357 (2023)

Articles citing this publication (49)

  1. La-related Protein 1 (LARP1) Represses Terminal Oligopyrimidine (TOP) mRNA Translation Downstream of mTOR Complex 1 (mTORC1). Fonseca BD, Zakaria C, Jia JJ, Graber TE, Svitkin Y, Tahmasebi S, Healy D, Hoang HD, Jensen JM, Diao IT, Lussier A, Dajadian C, Padmanabhan N, Wang W, Matta-Camacho E, Hearnden J, Smith EM, Tsukumo Y, Yanagiya A, Morita M, Petroulakis E, González JL, Hernández G, Alain T, Damgaard CK. J Biol Chem 290 15996-16020 (2015)
  2. The RNA-binding protein LARP1 is a post-transcriptional regulator of survival and tumorigenesis in ovarian cancer. Hopkins TG, Mura M, Al-Ashtal HA, Lahr RM, Abd-Latip N, Sweeney K, Lu H, Weir J, El-Bahrawy M, Steel JH, Ghaem-Maghami S, Aboagye EO, Berman AJ, Blagden SP. Nucleic Acids Res 44 1227-1246 (2016)
  3. Systematic Discovery of RNA Binding Proteins that Regulate MicroRNA Levels. Nussbacher JK, Yeo GW. Mol Cell 69 1005-1016.e7 (2018)
  4. Lack of tRNA modification isopentenyl-A37 alters mRNA decoding and causes metabolic deficiencies in fission yeast. Lamichhane TN, Blewett NH, Crawford AK, Cherkasova VA, Iben JR, Begley TJ, Farabaugh PJ, Maraia RJ. Mol Cell Biol 33 2918-2929 (2013)
  5. Changes in mRNA abundance drive shuttling of RNA binding proteins, linking cytoplasmic RNA degradation to transcription. Gilbertson S, Federspiel JD, Hartenian E, Cristea IM, Glaunsinger B. Elife 7 e37663 (2018)
  6. Widespread Translational Control of Fibrosis in the Human Heart by RNA-Binding Proteins. Chothani S, Schäfer S, Adami E, Viswanathan S, Widjaja AA, Langley SR, Tan J, Wang M, Quaife NM, Jian Pua C, D'Agostino G, Guna Shekeran S, George BL, Lim S, Yiqun Cao E, van Heesch S, Witte F, Felkin LE, Christodoulou EG, Dong J, Blachut S, Patone G, Barton PJR, Hubner N, Cook SA, Rackham OJL. Circulation 140 937-951 (2019)
  7. Structural insight into the mechanism of stabilization of the 7SK small nuclear RNA by LARP7. Uchikawa E, Natchiar KS, Han X, Proux F, Roblin P, Zhang E, Durand A, Klaholz BP, Dock-Bregeon AC. Nucleic Acids Res 43 3373-3388 (2015)
  8. 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. Martino L, Pennell S, Kelly G, Busi B, Brown P, Atkinson RA, Salisbury NJ, Ooi ZH, See KW, Smerdon SJ, Alfano C, Bui TT, Conte MR. Nucleic Acids Res 43 645-660 (2015)
  9. 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. Merret R, Martino L, Bousquet-Antonelli C, Fneich S, Descombin J, Billey E, Conte MR, Deragon JM. RNA 19 36-50 (2013)
  10. Systematic Discovery of Endogenous Human Ribonucleoprotein Complexes. Mallam AL, Sae-Lee W, Schaub JM, Tu F, Battenhouse A, Jang YJ, Kim J, Wallingford JB, Finkelstein IJ, Marcotte EM, Drew K. Cell Rep 29 1351-1368.e5 (2019)
  11. The RNA-binding protein LARP4 regulates cancer cell migration and invasion. Seetharaman S, Flemyng E, Shen J, Conte MR, Ridley AJ. Cytoskeleton (Hoboken) 73 680-690 (2016)
  12. Up-regulation of circ_LARP4 suppresses cell proliferation and migration in ovarian cancer by regulating miR-513b-5p/LARP4 axis. Lin W, Ye H, You K, Chen L. Cancer Cell Int 20 5 (2020)
  13. An atlas of alternative polyadenylation quantitative trait loci contributing to complex trait and disease heritability. Li L, Huang KL, Gao Y, Cui Y, Wang G, Elrod ND, Li Y, Chen YE, Ji P, Peng F, Russell WK, Wagner EJ, Li W. Nat Genet 53 994-1005 (2021)
  14. LARP4 mRNA codon-tRNA match contributes to LARP4 activity for ribosomal protein mRNA poly(A) tail length protection. Mattijssen S, Arimbasseri AG, Iben JR, Gaidamakov S, Lee J, Hafner M, Maraia RJ. Elife 6 e28889 (2017)
  15. LARP4B is an AU-rich sequence associated factor that promotes mRNA accumulation and translation. Küspert M, Murakawa Y, Schäffler K, Vanselow JT, Wolf E, Juranek S, Schlosser A, Landthaler M, Fischer U. RNA 21 1294-1305 (2015)
  16. Conservation of RNA chaperone activity of the human La-related proteins 4, 6 and 7. Hussain RH, Zawawi M, Bayfield MA. Nucleic Acids Res 41 8715-8725 (2013)
  17. The yeast La related protein Slf1p is a key activator of translation during the oxidative stress response. Kershaw CJ, Costello JL, Castelli LM, Talavera D, Rowe W, Sims PF, Ashe MP, Hubbard SJ, Pavitt GD, Grant CM. PLoS Genet 11 e1004903 (2015)
  18. mTORC1 promotes TOP mRNA translation through site-specific phosphorylation of LARP1. Jia JJ, Lahr RM, Solgaard MT, Moraes BJ, Pointet R, Yang AD, Celucci G, Graber TE, Hoang HD, Niklaus MR, Pena IA, Hollensen AK, Smith EM, Chaker-Margot M, Anton L, Dajadian C, Livingstone M, Hearnden J, Wang XD, Yu Y, Maier T, Damgaard CK, Berman AJ, Alain T, Fonseca BD. Nucleic Acids Res 49 3461-3489 (2021)
  19. 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. Cruz-Gallardo I, Martino L, Kelly G, Atkinson RA, Trotta R, De Tito S, Coleman P, Ahdash Z, Gu Y, Bui TTT, Conte MR. Nucleic Acids Res 47 4272-4291 (2019)
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  21. The LARP1 La-Module recognizes both ends of TOP mRNAs. Al-Ashtal HA, Rubottom CM, Leeper TC, Berman AJ. RNA Biol 18 248-258 (2021)
  22. hsa_circ_0003222 accelerates stemness and progression of non-small cell lung cancer by sponging miR-527. Li C, Zhang J, Yang X, Hu C, Chu T, Zhong R, Shen Y, Hu F, Pan F, Xu J, Lu J, Zheng X, Zhang H, Nie W, Han B, Zhang X. Cell Death Dis 12 807 (2021)
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  25. Human La binds mRNAs through contacts to the poly(A) tail. Vinayak J, Marrella SA, Hussain RH, Rozenfeld L, Solomon K, Bayfield MA. Nucleic Acids Res 46 4228-4240 (2018)
  26. The RNA-binding protein SERBP1 interacts selectively with the signaling protein RACK1. Bolger GB. Cell Signal 35 256-263 (2017)
  27. Community structure analysis of transcriptional networks reveals distinct molecular pathways for early- and late-onset temporal lobe epilepsy with childhood febrile seizures. Moreira-Filho CA, Bando SY, Bertonha FB, Iamashita P, Silva FN, Costa Lda F, Silva AV, Castro LH, Wen HT. PLoS One 10 e0128174 (2015)
  28. Gene expression changes in spinal motoneurons of the SOD1(G93A) transgenic model for ALS after treatment with G-CSF. Henriques A, Kastner S, Chatzikonstantinou E, Pitzer C, Plaas C, Kirsch F, Wafzig O, Krüger C, Spoelgen R, Gonzalez De Aguilar JL, Gretz N, Schneider A. Front Cell Neurosci 8 464 (2014)
  29. Single molecule poly(A) tail-seq shows LARP4 opposes deadenylation throughout mRNA lifespan with most impact on short tails. Mattijssen S, Iben JR, Li T, Coon SL, Maraia RJ. Elife 9 e59186 (2020)
  30. LARP4 Is Regulated by Tumor Necrosis Factor Alpha in a Tristetraprolin-Dependent Manner. Mattijssen S, Maraia RJ. Mol Cell Biol 36 574-584 (2016)
  31. The isolated La-module of LARP1 mediates 3' poly(A) protection and mRNA stabilization, dependent on its intrinsic PAM2 binding to PABPC1. Mattijssen S, Kozlov G, Gaidamakov S, Ranjan A, Fonseca BD, Gehring K, Maraia RJ. RNA Biol 18 275-289 (2021)
  32. Transcriptome-wide stability analysis uncovers LARP4-mediated NFκB1 mRNA stabilization during T cell activation. Tian Y, Zeng Z, Li X, Wang Y, Chen R, Mattijssen S, Gaidamakov S, Wu Y, Maraia RJ, Peng W, Zhu J. Nucleic Acids Res 48 8724-8739 (2020)
  33. 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)
  34. Recombinant expression and purification of the RNA-binding LARP6 proteins from fish genetic model organisms. Castro JM, Horn DA, Pu X, Lewis KA. Protein Expr Purif 134 147-153 (2017)
  35. Resonance assignment of human LARP4A La module. Cruz-Gallardo I, Martino L, Trotta R, De Tito S, Kelly G, Atkinson RA, Randazzo A, Conte MR. Biomol NMR Assign 13 169-172 (2019)
  36. Structural dynamics in the La-module of La-related proteins. Lizarrondo J, Dock-Bregeon AC, Martino L, Conte MR. RNA Biol 18 194-206 (2021)
  37. Buffy Coat Transcriptomic Analysis Reveals Alterations in Host Cell Protein Synthesis and Cell Cycle in Severe COVID-19 Patients. Cavalcante LTF, da Fonseca GC, Amado Leon LA, Salvio AL, Brustolini OJ, Gerber AL, Guimarães APC, Marques CAB, Fernandes RA, Ramos Filho CHF, Kader RL, Pimentel Amaro M, da Costa Gonçalves JP, Vieira Alves-Leon S, Vasconcelos ATR. Int J Mol Sci 23 13588 (2022)
  38. Fyn Regulates Binding Partners of Cyclic-AMP Dependent Protein Kinase A. Schmoker AM, Barritt SA, Weir ME, Mann JE, Hogan TC, Ballif BA, Deming PB. Proteomes 6 37 (2018)
  39. UBR5 promotes tumor immune evasion through enhancing IFN-γ-induced PDL1 transcription in triple negative breast cancer. Wu B, Song M, Dong Q, Xiang G, Li J, Ma X, Wei F. Theranostics 12 5086-5102 (2022)
  40. MetastaSite: Predicting metastasis to different sites using deep learning with gene expression data. Albaradei S, Albaradei A, Alsaedi A, Uludag M, Thafar MA, Gojobori T, Essack M, Gao X. Front Mol Biosci 9 913602 (2022)
  41. Complementary analysis of proteome-wide proteomics reveals changes in RNA binding protein-profiles during prostate cancer progression. Aikio E, Koivukoski S, Kallio E, Sadeesh N, Niskanen EA, Latonen L. Cancer Rep (Hoboken) 6 e1886 (2023)
  42. Serum peptidome: diagnostic window into pathogenic processes following occupational exposure to carbon nanomaterials. Mostovenko E, Dahm MM, Schubauer-Berigan MK, Eye T, Erdely A, Young TL, Campen MJ, Ottens AK. Part Fibre Toxicol 18 39 (2021)
  43. A MademoiseLLE domain binding platform links the key RNA transporter to endosomes. Devan SK, Schott-Verdugo S, Müntjes K, Bismar L, Reiners J, Hachani E, Schmitt L, Höppner A, Smits SH, Gohlke H, Feldbrügge M. PLoS Genet 18 e1010269 (2022)
  44. Interaction of LARP4 to filamin A mechanosensing domain regulates cell migrations. Mao Z, Nakamura F. Front Cell Dev Biol 11 1152109 (2023)
  45. La-related protein 4 is enriched in vaccinia virus factories and is required for efficient viral replication in primary human fibroblasts. Dhungel P, Brahim Belhaouari D, Yang Z. Microbiol Spectr e0139023 (2023)
  46. RNA-Protein Interactome at the Hepatitis E Virus Internal Ribosome Entry Site. Kumar S, Verma R, Saha S, Agrahari AK, Shukla S, Singh ON, Berry U, Anurag, Maiti TK, Asthana S, Ranjith-Kumar CT, Surjit M. Microbiol Spectr 11 e0282722 (2023)
  47. Short poly(A) tails are protected from deadenylation by the LARP1-PABP complex. Park J, Kim M, Yi H, Baeg K, Choi Y, Lee YS, Lim J, Kim VN. Nat Struct Mol Biol 30 330-338 (2023)
  48. Structural basis of 3'-end poly(A) RNA recognition by LARP1. Kozlov G, Mattijssen S, Jiang J, Nyandwi S, Sprules T, Iben JR, Coon SL, Gaidamakov S, Noronha AM, Wilds CJ, Maraia RJ, Gehring K. Nucleic Acids Res 50 9534-9547 (2022)
  49. The MYC-Regulated RNA-Binding Proteins hnRNPC and LARP1 Are Drivers of Multiple Myeloma Cell Growth and Disease Progression and Negatively Predict Patient Survival. Seibert M, Koschade SE, Stolp V, Häupl B, Wempe F, Serve H, Kurrle N, Schnütgen F, von Metzler I. Cancers (Basel) 15 5508 (2023)


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