Cytoplasmic poly(A) binding protein-1 binds to genomically encoded sequences within mammalian mRNAs

RNA

Volumn 22, Issue 1, 2016, Pages 61-74

  Kini, Hemant K ^a   Silverman, Ian M ^b   Ji, Xinjun ^a   Gregory, Brian D ^b   Liebhaber, Stephen A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

CLIP seq; Poly(A) binding protein; Polyadenylation signal; Translational control

Indexed keywords

CYTOPLASMIC POLY(A) BINDING PROTEIN 1; MESSENGER RNA; PANCREATIC RIBONUCLEASE; POLYADENYLIC ACID BINDING PROTEIN; TRANSCRIPTOME; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; POLYADENYLIC ACID;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL GENETICS; ARTICLE; BINDING SITE; CELL FUNCTION; CODON; GENE CONTROL; GENETIC ANALYSIS; GENETIC CODE; GENOME; MOUSE; NONHUMAN; OPEN READING FRAME; POLYADENYLATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN SYNTHESIS; RNA CLEAVAGE; RNA PROCESSING; RNA REPLICATION; RNA SEQUENCE; TRANSLATION INITIATION; 3T3 CELL LINE; ANIMAL; CELL CULTURE; CYTOPLASM; MAMMAL; METABOLISM;

3' UNTRANSLATED REGIONS; 5' UNTRANSLATED REGIONS; ANIMALS; CELLS, CULTURED; CYTOPLASM; MAMMALS; MICE; NIH 3T3 CELLS; POLY A; POLY(A)-BINDING PROTEIN I; RNA, MESSENGER; TRANSCRIPTOME;

EID: 85009754220     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.053447.115     Document Type: Article

References (60)

1. Adam SA, Nakagawa T, Swanson MS, Woodruff TK, Dreyfuss G. 1986. mRNA polyadenylate-binding protein: gene isolation and sequencing and identification of a ribonucleoprotein consensus sequence. Mol Cell Biol 6:2932-2943.
2. Althammer S, González-Vallinas J, Ballaré C, Beato M, Eyras E. 2011. Pyicos: a versatile toolkit for the analysis of high-throughput sequencing data. Bioinformatics 27:3333-3340.
3. Anders S, Pyl PT, Huber W. 2015. HTSeq-a Python framework to work with high-throughput sequencing data. Bioinformatics 31:166-169.
4. Baejen C, Torkler P, Gressel S, Essig K, Söding J, Cramer P. 2014. Transcriptome maps of mRNP biogenesis factors define pre-mRNA recognition. Mol Cell 55:745-757.
5. Bag J, Wu J. 1996. Translational control of poly (A)-binding protein expression. Eur J Biochem 237:143-152.
6. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS. 2009. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37(Web Server issue):W202-W208.
7. Bembom O, Keles S, van der Laan MJ. 2007. Supervised detection of conserved motifs in DNA sequences with cosmo. Stat Appl Genet Mol Biol 6: Article8.
8. Blobel G. 1973. A protein of molecular weight 78, 000 bound to the poly-adenylate region of eukaryotic messenger RNAs. Proc Natl Acad Sci 70:924-928.
9. Burd CG, Dreyfuss G. 1994. Conserved structures and diversity of functions of RNA-binding proteins. Science 265:615-621.
10. Chi SW, Zang JB, Mele A, Darnell RB. 2009. Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature 460:479-486.
11. de Melo Neto OP, Standart N, Martins de Sa C. 1995. Autoregulation of poly (A)-binding protein synthesis in vitro. Nucleic Acids Res 23:2198-2205.
12. de Melo Neto OP, Walker JA, Martins de Sa CM, Standart N. 2000. Levels of free PABP are limited by newly polyadenylated mRNA in early Spisula embryogenesis. Nucleic Acids Res 28:3346-3353.
13. de Moor CH, Meijer H, Lissenden S. 2005. Mechanisms of translational control by the 3' UTR in development and differentiation. Semin Cell Dev Biol 16:49-58.
14. Elliott R, Li F, Dragomir I, Chua MM, Gregory BD, Weiss SR. 2013. Analysis of the host transcriptome from demyelinating spinal cord of murine coronavirus-infected mice. PLoS One 8:e75346.
15. Gebauer F, Preiss T, Hentze MW. 2012. From cis-regulatory elements to complex RNPs and back. Cold Spring Harb Perspect Biol 4:a012245.
16. Good PJ, Abler L, Herring D, Sheets MD. 2004. Xenopus embryonic poly (A) binding protein 2 (ePABP2) defines a new family of cytoplasmic poly (A) binding proteins expressed during the early stages of vertebrate development. Genesis 38:166-175.
17. Gorgoni B, Richardson WA, Burgess HM, Anderson RC, Wilkie GS, Gautier P, Martins JP, Brook M, Sheets MD, Gray NK. 2011. Poly (A)-binding proteins are functionally distinct and have essential roles during vertebrate development. Proc Natl Acad Sci 108:7844-7849.
18. Goss DJ, Kleiman FE. 2013. Poly (A) binding proteins: are they all created equal? Wiley Interdiscip Rev RNA 4:167-179.
19. Guo Z, Sherman F. 1995. 3'-end-forming signals of yeast mRNA. Mol Cell Biol 15:5983-5990.
20. Hornstein E, Git A, Braunstein I, Avni D, Meyuhas O. 1999. The expression of poly (A)-binding protein gene is translationally regulated in a growth-dependent fashion through a 5'-terminal oligopyrimidine tract motif. J Biol Chem 274:1708-1714.
21. Huang da W, Sherman BT, Lempicki RA. 2009. Systematic and integra-tive analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4:44-57.
22. Ingolia NT, Lareau LF, Weissman JS. 2011. Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell 147:789-802.
23. Ingolia NT, Brar GA, Rouskin S, McGeachy AM, Weissman JS. 2012. The ribosome profiling strategy for monitoring translation in vivo by deep sequencing of ribosome-protected mRNA fragments. Nat Protoc 7:1534-1550.
24. Kahvejian A, Svitkin YV, Sukarieh R, M'Boutchou MN, Sonenberg N. 2005. Mammalian poly (A)-binding protein is a eukaryotic translation initiation factor, which acts via multiple mechanisms. Genes Dev 19:104-113.
25. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. 2013. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14:R36.
26. Kini HK, Kong J, Liebhaber SA. 2014. Cytoplasmic poly (A) binding protein C4 serves a critical role in erythroid differentiation. Mol Cell Biol 34:1300-1309.
27. Kleene KC, Wang MY, Cutler M, Hall C, Shih D. 1994. Developmental expression of poly (A) binding protein mRNAs during spermatogen-esis in the mouse. Mol Reprod Dev 39:355-364.
28. Mangus DA, Evans MC, Jacobson A. 2003. Poly (A)-binding proteins: multifunctional scaffolds for the post-transcriptional control of gene expression. Genome Biol 4:223.
29. Martin M. 2011. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17:10-12.
30. Melo EO, de Melo Neto OP, Martins de Sá C. 2003a. Adenosine-rich elements present in the 5'-untranslated region of PABP mRNA can selectively reduce the abundance and translation of CAT mRNAs in vivo. FEBS Lett 546:329-334.
31. Melo EO, Dhalia R, Martins de Sa C, Standart N, de Melo Neto OP. 2003b. 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 278:46357-46368.
32. Moore MJ, Zhang C, Gantman EC, Mele A, Darnell JC, Darnell RB. 2014. Mapping Argonaute and conventional RNA-binding protein interactions with RNA at single-nucleotide resolution using HITS-CLIP and CIMS analysis. Nat Protoc 9:263-293.
33. Nayler O, Stratling W, Bourquin JP, Stagljar I, Lindemann L, Jasper H, Hartmann AM, Fackelmayer FO, Ullrich A, Stamm S. 1998. SAF-B protein couples transcription and pre-mRNA splicing to SAR/MAR elements. Nucleic Acids Res 26:3542-3549.
34. Paasinen-Sohns A, Kaariainen E, Yin M, Járvinen K, Nummela P, Hölttá E. 2011. Chaotic neovascularization induced by aggressive fi-brosarcoma cells overexpressing S-adenosylmethionine decarboxy-lase. Int J Biochem Cell Biol 43:441-454.
35. Peixeiro I, Inácio Â, Barbosa C, Silva AL, Liebhaber SA, Romão L. 2012. Interaction of PABPC1 with the translation initiation complex is critical to the NMD resistance of AUG-proximal nonsense mutations. Nucleic Acids Res 40:1160-1173.
36. Pesole G, Liuni S, Grillo G, Saccone C. 1997. Structural and compositional features of untranslated regions of eukaryotic mRNAs. Gene 205:95-102.
37. Quinlan AR, Hall IM. 2010. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26:841-842.
38. Richter JD. 2007. CPEB: a life in translation. Trends Biochem Sci 32:279-285.
39. Sachs AB, Davis RW, Kornberg RD. 1987. A single domain of yeast poly (A)-binding protein is necessary and sufficient for RNA binding and cell viability. Mol Cell Biol 7:3268-3276.
40. Sigrist SJ, Thiel PR, Reiff DF, Lachance PE, Lasko P, Schuster CM. 2000. Postsynaptic translation affects the efficacy and morphology of neu-romuscular junctions. Nature 405:1062-1065.
41. Sladic RT, Lagnado CA, Bagley CJ, Goodall GJ. 2004. Human PABP binds AU-rich RNA via RNA-binding domains 3 and 4. Eur J Biochem 271:450-457.
42. Smith RW, Blee TK, Gray NK. 2014. Poly (A)-binding proteins are required for diverse biological processes in metazoans. Biochem Soc Trans 42:1229-1237.
43. Sugimoto Y, König J, Hussain S, Zupan B, Curk T, Frye M, Ule J. 2012. Analysis of CLIP and iCLIP methods for nucleotide-resolution studies of protein-RNA interactions. Genome Biol 13:R67.
44. Tabassum R, Jaiswal A, Chauhan G, Dwivedi OP, Ghosh S, Marwaha RK, Tandon N, Bharadwaj D. 2012. Genetic variant of AMD1 is associated with obesity in urban Indian children. PLoS One 7:e33162.
45. Tarun SZ Jr, Sachs AB. 1995. A common function for mRNA 5' and 3' ends in translation initiation in yeast. Genes Dev 9:2997-3007.
46. Theis M, Si K, Kandel ER. 2003. Two previously undescribed members of the mouse CPEB family of genes and their inducible expression in the principal cell layers of the hippocampus. Proc Natl Acad Sci 100:9602-9607.
47. Tian B, Hu J, Zhang H, Lutz CS. 2005. A large-scale analysis of mRNA polyadenylation of human and mouse genes. Nucleic Acids Res 33:201-212.
48. Trapnell C, Pachter L, Salzberg SL. 2009. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25:1105-1111.
49. Tuck AC, Tollervey D. 2013. A transcriptome-wide atlas of RNP composition reveals diverse classes of mRNAs and lncRNAs. Cell 154:996-1009.
50. Uchida N, Hoshino S, Imataka H, Sonenberg N, Katada T. 2002. A novel role of the mammalian GSPT/eRF3 associating with poly (A)-bind-ing protein in cap/poly (A)-dependent translation. J Biol Chem 277:50286-50292.
51. Ule J, Jensen K, Mele A, Darnell RB. 2005. CLIP: a method for identifying protein-RNA interaction sites in living cells. Methods 37:376-386.
52. Verlaet M, Deregowski V, Denis G, Humblet C, Stalmans MT, Bours V, Castronovo V, Boniver J, Defresne MP. 2001. Genetic imbalances in preleukemic thymuses. Biochem Biophys Res Commun 283:12-18.
53. Wahle E. 1991. A novel poly (A)-binding protein acts as a specificity factor in the second phase of messenger RNA polyadenylation. Cell 66:759-768.
54. Wang Z, Kiledjian M. 2000. The poly (A)-binding protein and an mRNA stability protein jointly regulate an endoribonuclease activity. Mol Cell Biol 20:6334-6341.
55. Wells SE, Hillner PE, Vale RD, Sachs AB. 1998. Circularization of mRNA by eukaryotic translation initiation factors. Mol Cell 2:135-140.
56. Williams KR, Konigsberg WH. 1991. Identification of amino acid residues at interface of protein-nucleic acid complexes by photochemical cross-linking. Methods Enzymol 208:516-539.
57. Wilusz CJ, Gao M, Jones CL, Wilusz J, Peltz SW. 2001. Poly (A)-binding proteins regulate both mRNA deadenylation and decapping in yeast cytoplasmic extracts. RNA 7:1416-1424.
58. Wormington M, Searfoss AM, Hurney CA. 1996. Overexpression of poly (A) binding protein prevents maturation-specific deadenylation and translational inactivation in Xenopus oocytes. EMBO J 15:900-909.
59. Yanagiya A, Delbes G, Svitkin YV, Robaire B, Sonenberg N. 2010. The poly (A)-binding protein partner Paip2a controls translation during late spermiogenesis in mice. J Clin Invest 120:3389-3400.
60. Zhang C, Darnell RB. 2011. Mapping in vivo protein-RNA interactions at single-nucleotide resolution from HITS-CLIP data. Nat Biotechnol 29:607-614.