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Research Paper

Phosphorylation and interactions associated with the control of the Leishmania Poly-A Binding Protein 1 (PABP1) function during translation initiation

, , , , , , , , , & show all
Pages 739-755 | Received 31 Jul 2017, Accepted 13 Feb 2018, Published online: 23 Mar 2018

References

  • Ouellette M, Papadopoulou B. Coordinated gene expression by post-transcriptional regulons in African trypanosomes. J Biol. 2009;8:100. doi:10.1186/jbiol203
  • Fernandez-Moya SM, Estevez AM. Posttranscriptional control and the role of RNA-binding proteins in gene regulation in trypanosomatid protozoan parasites. Wiley Interdiscip Rev RNA. 2010;1:34–46. doi:10.1002/wrna.6
  • De Gaudenzi JG, Noe G, Campo VA, Frasch AC, et al. Gene expression regulation in trypanosomatids. Essays Biochem. 2011;51:31–46. doi:10.1042/bse0510031
  • Schwede A, Kramer S, Carrington M. How do trypanosomes change gene expression in response to the environment? Protoplasma. 2012;249:223–38. doi:10.1007/s00709-011-0282-5
  • Kramer S. Developmental regulation of gene expression in the absence of transcriptional control: the case of kinetoplastids. Mol Biochem Parasitol. 2012;181:61–72. doi:10.1016/j.molbiopara.2011.10.002
  • Clayton CE. Networks of gene expression regulation in Trypanosoma brucei. Mol Biochem Parasitol. 2014;195:96–106. doi:10.1016/j.molbiopara.2014.06.005
  • Clayton CE. Gene expression in Kinetoplastids. Curr Opin Microbiol. 2016;32:46–51. doi:10.1016/j.mib.2016.04.018
  • van der Kelen K, Beyaert R, Inzé D, et al. Translational control of eukaryotic gene expression Crit Rev Biochem Mol Biol. 2009;44:143–68. doi:10.1080/10409230902882090
  • Gingras AC, Raught B, Sonenberg N. eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu Rev Biochem. 1999;68:913–63. doi:10.1146/annurev.biochem.68.1.913
  • Gallie DR. The role of the poly (A) binding protein in the assembly of the cap-binding complex during translation initiation in plants. Translation. 2014;731:1–14
  • Merrick WC. eIF4F: A Retrospective. J Biol Chem. 2015;290:24091–9. doi:10.1074/jbc.R115.675280
  • Aylett CHS, Ban N. Eukaryotic aspects of translation initiation brought into focus. Philos Trans R Soc London B Biol Sci. 2017;372: doi:10.1098/rstb.2016.0186
  • Kühn U, Wahle E. Structure and function of poly(A) binding proteins. Biochim Biophys Acta. 2004;1678:67–84. doi:10.1016/j.bbaexp.2004.03.008
  • Gorgoni B, Gray NK. The roles of cytoplasmic poly(A)-binding proteins in regulating gene expression: a developmental perspective. Brief Funct Genomic Proteomic. 2004;3:125–41. doi:10.1093/bfgp/3.2.125
  • Lemay J-F, Lemieux C, St-André O, et al. Crossing the borders: Poly(A)-binding proteins working on both sides of the fence. RNA Biol. 2010;7:291–5. doi:10.4161/rna.7.3.11649
  • Eliseeva IA, Lyabin DN, Ovchinnikov LP. Poly(A)-binding proteins: structure, domain organization, and activity regulation. Biochem. 2013;78:1377–91
  • Smith RWP, Blee TKP, Gray NK. Poly(A)-binding proteins are required for diverse biological processes in metazoans. Biochem Soc Trans. 2014;42:1229–37. doi:10.1042/BST20140111
  • Wigington CP, Williams KR, Meers MP, et al. Poly(A) RNA-binding proteins and polyadenosine RNA: new members and novel functions. Wiley Interdiscip Rev RNA. 2014;13:601–22. doi:10.1002/wrna.1233
  • Gray NK, Hrabálková L, Scanlon JP, et al. Poly(A)-binding proteins and mRNA localization: who rules the roost? Biochem Soc Trans. 2015;43:1277–84. doi:10.1042/BST20150171
  • Goss DJ, Kleiman FE. Poly(A) binding proteins: are they all created equal? Wiley Interdiscip Rev RNA. 2013;4:167–79. doi:10.1002/wrna.1151
  • Burd CG, Dreyfuss G. Conserved structures and diversity of functions of RNA-binding proteins. Science. 1994;265:615–21. doi:10.1126/science.8036511
  • Deo RC, Bonanno JB, Sonenberg N, et al. Recognition of polyadenylate RNA by the poly(A)-binding protein. Cell. 1999;98:835–45. doi:10.1016/S0092-8674(00)81517-2
  • Kuhn U, Pieler T, Kühn U, et al. Xenopus poly(A) binding protein: functional domains in RNA binding and protein-protein interaction. J Mol Biol. 1996;256:20–30. doi:10.1006/jmbi.1996.0065
  • Kessler SH, Sachs AB. RNA recognition motif 2 of yeast Pab1p is required for its functional interaction with eukaryotic translation initiation factor 4G. Mol Cell Biol. 1998;18:51–7. doi:10.1128/MCB.18.1.51
  • Imataka H, Gradi A, Sonenberg N. A newly identified N-terminal amino acid sequence of human eIF4G binds poly(A)-binding protein and functions in poly(A)-dependent translation. EMBO J. 1998;17:7480–9. doi:10.1093/emboj/17.24.7480
  • Cheng S, Gallie DR. eIF4G, eIFiso4G, and eIF4B bind the poly(A)-binding protein through overlapping sites within the RNA recognition motif domains. J Biol Chem. 2007;282:25247–58. doi:10.1074/jbc.M702193200
  • Khanam T, Muddashetty RS, Kahvejian A, et al. Poly(A)-binding protein binds to A-rich sequences via RNA-binding domains 1+2 and 3+4. RNA Biol. 2006;3:170–7. doi:10.4161/rna.3.4.4075
  • Sladic RT, Lagnado CA, Bagley CJ, et al. Human PABP binds AU-rich RNA via RNA-binding domains 3 and 4. Eur J Biochem. 2004;271:450–7. doi:10.1046/j.1432-1033.2003.03945.x
  • Khacho M, Mekhail K, Pilon-Larose K, et al. eEF1A Is a Novel Component of the Mammalian Nuclear Protein Export Machinery. Mol Biol Cell. 2008;19:5296–308. doi:10.1091/mbc.E08-06-0562
  • Melo EO, Dhalia R, Martins de SC, et al. Identification of a C-terminal poly(A)-binding protein (PABP)-PABP interaction domain: role in cooperative binding to poly (A) and efficient cap distal translational repression. J Biol Chem. 2003;278:46357–68. doi:10.1074/jbc.M307624200
  • Lin J, Fabian M, Sonenberg N, et al. Nanopore detachment kinetics of poly(A) binding proteins from RNA molecules reveals the critical role of C-terminus interactions. Biophys J. 2012;102:1427–34. doi:10.1016/j.bpj.2012.02.025
  • Khaleghpour K, Kahvejian A, De CG, Roy G, et al. Dual interactions of the translational repressor Paip2 with poly(A) binding protein. Mol Cell Biol. 2001;21:5200–13. doi:10.1128/MCB.21.15.5200-5213.2001
  • Albrecht M, Lengauer T. Survey on the PABC recognition motif PAM2. Biochem Biophys Res Commun. 2004;316:129–38. doi:10.1016/j.bbrc.2004.02.024
  • Jiménez-López D, Bravo J, Guzmán P. Evolutionary history exposes radical diversification among classes of interaction partners of the MLLE domain of plant poly(A)-binding proteins. BMC Evol Biol. 2015;15:195. doi:10.1186/s12862-015-0475-1
  • da Costa Lima TD, Moura DMN, Reis CRS, et al. Functional characterization of three leishmania poly(a) binding protein homologues with distinct binding properties to RNA and protein partners. Eukaryot Cell. 2010;9:1484–94. doi:10.1128/EC.00148-10
  • Kramer S, Bannerman-Chukualim B, Ellis L, et al. Differential localization of the two T. brucei poly(A) binding proteins to the nucleus and RNP granules suggests binding to distinct mRNA pools. PLoS One. 2013;8:e54004. doi:10.1371/journal.pone.0054004
  • Pitula J, Ruyechan WT, Williams N. Trypanosoma brucei: identification and purification of a poly(A)-binding protein. Exp Parasitol. 1998;88:157–60. doi:10.1006/expr.1998.4211
  • Guerra N, Vega-Sendino M, Pérez-Morgado MI, et al. Identification and functional characterization of a poly(A)-binding protein from Leishmania infantum (LiPABP). FEBS Lett. 2011;585:193–8. doi:10.1016/j.febslet.2010.11.042
  • Erben ED, Fadda A, Lueong S, et al. A genome-wide tethering screen reveals novel potential post-transcriptional regulators in Trypanosoma brucei. PLoS Pathog. 2014;10:e1004178. doi:10.1371/journal.ppat.1004178
  • Lueong S, Merce C, Fischer B, et al. Gene expression regulatory networks in Trypanosoma brucei: Insights into the role of the mRNA-binding proteome. Mol Microbiol. 2016;100:457–71. doi:10.1111/mmi.13328
  • Klein C, Terrao M, Inchaustegui GD, et al. Polysomes of Trypanosoma brucei: Association with Initiation Factors and RNA-Binding Proteins. PLoS One. 2015;10:e0135973. doi:10.1371/journal.pone.0135973
  • Dhalia R, Reis CR, Freire ER, et al. Translation initiation in Leishmania major: characterisation of multiple eIF4F subunit homologues. Mol Biochem Parasitol. 2005;140:23–41. doi:10.1016/j.molbiopara.2004.12.001
  • Jagus R, Bachvaroff TR, Joshi B, et al. Diversity of eukaryotic translational initiation factor eIF4E in protists. Comp Funct Genomics. 2012;2012:134839. doi:10.1155/2012/134839
  • de Melo Neto OP, Reis CR, Moura DM, Freire ER, et al. Unique and conserved features of the protein synthesis apparatus in trypanosomatid (Trypanosoma and Leishmania) species. In: Hernandez G, Jagus R, editors. Evolution of the protein synthesis machinery and its regulation. Springer International Publishing; 2016. p. page 435–75
  • Zinoviev A, Shapira M. Evolutionary conservation and diversification of the translation initiation apparatus in trypanosomatids. Comp Funct Genomics. 2012;2012:813718. doi:10.1155/2012/813718
  • Freire E, Sturm N, Campbell D, et al. The role of cytoplasmic mRNA cap-binding protein complexes in Trypanosoma brucei and other trypanosomatids. Pathogens. 2017;6:55. doi:10.3390/pathogens6040055
  • Yoffe Y, Leger M, Zinoviev A, et al. Evolutionary changes in the Leishmania eIF4F complex involve variations in the eIF4E-eIF4G interactions. Nucleic Acids Res. 2009;37:3243–53. doi:10.1093/nar/gkp190
  • Freire ER, Dhalia R, Moura DMN, et al. The four trypanosomatid eIF4E homologues fall into two separate groups, with distinct features in primary sequence and biological properties. Mol Biochem Parasitol. 2011;176:25–36. doi:10.1016/j.molbiopara.2010.11.011
  • Zinoviev A, Leger M, Wagner G, et al. A novel 4E-interacting protein in Leishmania is involved in stage-specific translation pathways. Nucleic Acids Res. 2011;39:8404–15. doi:10.1093/nar/gkr555
  • Zinoviev A, Manor S, Shapira M. Nutritional stress affects an atypical cap-binding protein in Leishmania. RNA Biol. 2012;9:1450–60. doi:10.4161/rna.22709
  • Moura DMN, Reis CRS, Xavier CC, et al. Two related trypanosomatid eIF4G homologues have functional differences compatible with distinct roles during translation initiation. RNA Biol. 2015;12:305–19. doi:10.1080/15476286.2015.1017233
  • de Melo Neto OP, da Costa Lima TDC, Xavier CC, et al. The unique Leishmania EIF4E4 N-terminus is a target for multiple phosphorylation events and participates in critical interactions required for translation initiation. RNA Biol. 2015;12:1209–21. doi:10.1080/15476286.2015.1086865
  • Bates EJ, Knuepfer E, Smith DF. Poly(A)-binding protein I of Leishmania: functional analysis and localisation in trypanosomatid parasites. Nucleic Acids Res. 2000;28:1211–20. doi:10.1093/nar/28.5.1211
  • Urbaniak MD, Martin DM, Ferguson MA. Global quantitative SILAC phosphoproteomics reveals differential phosphorylation is widespread between the procyclic and bloodstream form lifecycle stages of Trypanosoma brucei. J Proteome Res. 2013;12:2233–44. doi:10.1021/pr400086y
  • Pereira MMC, Malvezzi AM, Nascimento LM, et al. The eIF4E subunits of two distinct trypanosomatid eIF4F complexes are subjected to differential post-translational modifications associated to distinct growth phases in culture. Mol Biochem Parasitol. 2013;190:82–6. doi:10.1016/j.molbiopara.2013.06.008
  • Pyronnet S, Imataka H, Gingras AC, et al. Human eukaryotic translation initiation factor 4G (eIF4G) recruits mnk1 to phosphorylate eIF4E. EMBO J. 1999;18:270–9. doi:10.1093/emboj/18.1.270
  • Kozlov G, Ménade M, Rosenauer A, et al. Molecular determinants of PAM2 recognition by the MLLE domain of poly(A)-binding protein. J Mol Biol. 2010;397:397–407. doi:10.1016/j.jmb.2010.01.032
  • Kozlov G, De CG, Lim NS, Siddiqui N, et al. Structural basis of ligand recognition by PABC, a highly specific peptide-binding domain found in poly(A)-binding protein and a HECT ubiquitin ligase. EMBO J. 2004;23:272–81. doi:10.1038/sj.emboj.7600048
  • Kozlov G, Gehring K. Molecular basis of eRF3 recognition by the MLLE domain of poly(A)-binding protein. PLoS One. 2010;5:e10169. doi:10.1371/journal.pone.0010169
  • Hu H, Gourguechon S, Wang CC, et al. The G1 cyclin-dependent kinase CRK1 in Trypanosoma brucei regulates anterograde protein transport by phosphorylating the COPII subunit Sec31. J Biol Chem. 2016;291:15527–39. doi:10.1074/jbc.M116.715185
  • Naula C, Parsons M, Mottram JC. Protein kinases as drug targets in trypanosomes and Leishmania. Biochim Biophys Acta. 2005;1754:151–9. doi:10.1016/j.bbapap.2005.08.018
  • Le H, Browning KS, Gallie DR. The phosphorylation state of poly(A)-binding protein specifies its binding to poly(A) RNA and its interaction with eukaryotic initiation factor (eIF) 4F, eIFiso4F, and eIF4B. J Biol Chem. 2000;275:17452–62. doi:10.1074/jbc.M001186200
  • Friend K, Brook M, Bezirci FB, et al. Embryonic poly(A)-binding protein (ePAB) phosphorylation is required for Xenopus oocyte maturation. Biochem J. 2012;445:93–100. doi:10.1042/BJ20120304
  • Ma S, Musa T, Bag J. Reduced stability of mitogen-activated protein kinase kinase-2 mRNA and phosphorylation of Poly(A)-binding Protein (PABP) in cells overexpressing PABP. J Biol Chem. 2006;281:3145–56. doi:10.1074/jbc.M508937200
  • Brook M, McCracken L, Reddington JP, et al. The multifunctional poly(A)-binding protein (PABP) 1 is subject to extensive dynamic post-translational modification, which molecular modelling suggests plays an important role in co-ordinating its activities. Biochem J. 2012;441:803–12. doi:10.1042/BJ20111474
  • Siddiqui N, Kozlov G, D'Orso I, et al. Solution structure of the C-terminal domain from poly(A)-binding protein in Trypanosoma cruzi: a vegetal PABC domain. Protein Sci. 2003;12:1925–33. doi:10.1110/ps.0390103
  • Huang K-L, Chadee AB, Chen C-Y a, et al. Phosphorylation at intrinsically disordered regions of PAM2 motif-containing proteins modulates their interactions with PABPC1 and influences mRNA fate. RNA. 2013;19:295–305. doi:10.1261/rna.037317.112
  • Huntzinger E, Braun JE, Heimstädt S, et al. Two PABPC1-binding sites in GW182 proteins promote miRNA-mediated gene silencing. EMBO J. 2010;29:4146–60. doi:10.1038/emboj.2010.274
  • Kononenko A V., Mitkevich VA, Atkinson GC, et al. GTP-dependent structural rearrangement of the eRF1:eRF3 complex and eRF3 sequence motifs essential for PABP binding. Nucleic Acids Res. 2010;38:548–58. doi:10.1093/nar/gkp908
  • Gallie DR, Liu R. Phylogenetic analysis reveals dynamic evolution of the poly(A)-binding protein gene family in plants. BMC Evol Biol. 2014;14:238. doi:10.1186/s12862-014-0238-4
  • Derry MC, Yanagiya A, Martineau Y, et al. Regulation of poly(A)-binding protein through PABP-interacting proteins. Cold Spring Harb Symp Quant Biol. 2006;71:537–43. doi:10.1101/sqb.2006.71.061
  • Minia I, Clayton C. Regulating a post-transcriptional regulator: protein phosphorylation, degradation and translational blockage in control of the trypanosome stress-response RNA-Binding Protein ZC3H11. PLoS Pathog. 2016;12:1–31. doi:10.1371/journal.ppat.1005514
  • Papadopoulou B, Roy G, Ouellette M. A novel antifolate resistance gene on the amplified H circle of Leishmania. EMBO J. 1992;11:3601–8
  • McNicoll F, Muller M, Cloutier S, et al. Distinct 3′-untranslated region elements regulate stage-specific mRNA accumulation and translation in Leishmania. J Biol Chem. 2005;280:35238–46. doi:10.1074/jbc.M507511200
  • Cloutier S, Laverdière M, Chou MN, et al. Translational control through eIF2alpha phosphorylation during the Leishmania differentiation process. PLoS One. 2012;7:e35085. doi:10.1371/journal.pone.0035085
  • Sali A, Blundell TL. Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol. 1993;234:779–815. doi:10.1006/jmbi.1993.1626
  • Leaver-Fay A, Tyka M, Lewis SM, et al. ROSETTA3: An object-oriented software suite for the simulation and design of macromolecules. Methods Enzimol. 2011;487:545–74. doi:10.1016/B978-0-12-381270-4.00019-6
  • Laskowski RA, MacArthur MW, Moss DS, et al. PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr. 1993;26:283–91. doi:10.1107/S0021889892009944
  • Padmanabhan PK, Samant M, Cloutier S, et al. Apoptosis-like programmed cell death induces antisense ribosomal RNA (rRNA) fragmentation and rRNA degradation in Leishmania. Cell Death Differ. 2012;19:1972–82. doi:10.1038/cdd.2012.85
  • Mureev S, Kovtun O, Nguyen UTT, et al. Species-independent translational leaders facilitate cell-free expression. Nat Biotechnol. 2009;27:747–52. doi:10.1038/nbt.1556
  • Rezende AM, Assis LA, Nunes EC, et al. The translation initiation complex eIF3 in trypanosomatids and other pathogenic excavates–identification of conserved and divergent features based on orthologue analysis. BMC Genomics. 2014;15:1175. doi:10.1186/1471-2164-15-1175

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