Specificity factors in cytoplasmic polyadenylation

Abstract

Poly(A) tail elongation after export of an messenger RNA ( mRNA ) to the cytoplasm is called cytoplasmic polyadenylation. It was first discovered in oocytes and embryos, where it has roles in meiosis and development. In recent years, however, has been implicated in many other processes, including synaptic plasticity and mitosis. This review aims to introduce cytoplasmic polyadenylation with an emphasis on the factors and elements mediating this process for different mRNAs and in different animal species. We will discuss the RNA sequence elements mediating cytoplasmic polyadenylation in the 3′ untranslated regions of mRNAs , including the CPE , MBE , TCS , eCPE , and C‐ CPE . In addition to describing the role of general polyadenylation factors, we discuss the specific RNA binding protein families associated with cytoplasmic polyadenylation elements, including CPEB ( CPEB1 , CPEB2 , CPEB3 , and CPEB4 ), Pumilio ( PUM2 ), Musashi ( MSI1 , MSI2 ), zygote arrest ( ZAR2 ), ELAV like proteins ( ELAVL1 , HuR ), poly(C) binding proteins ( PCBP2 , αCP2 , hnRNP‐E2 ), and Bicaudal C ( BICC1 ). Some emerging themes in cytoplasmic polyadenylation will be highlighted. To facilitate understanding for those working in different organisms and fields, particularly those who are analyzing high throughput data, HUGO gene nomenclature for the human orthologs is used throughout. Where human orthologs have not been clearly identified, reference is made to protein families identified in man. WIREs RNA 2013, 4:437–461. doi: 10.1002/wrna.1171 This article is categorized under: RNA Interactions with Proteins and Other Molecules > Protein–RNA Interactions: Functional Implications Translation > Translation Regulation RNA Processing > 3' End Processing

Shown for reading. Its publisher allows quoting it, not republishing it.

References 312

1. 1.

   Proudfoot NJ. Ending the message: poly(A) signals then and now. Genes Dev. 2011;25:1770-1782.

   Not in our library10.1101/gad.17268411

2. 2.

   Nagaike T, Manley JL. Transcriptional activators enhance polyadenylation of mRNA precursors. RNA Biol. 2011;8:964-967.

   Not in our library10.4161/rna.8.6.17210

3. 3.

   Martinson HG. An active role for splicing in 3′-end formation. Wiley Interdiscip Rev RNA. 2011;2:459-470.

   Not in our library10.1002/wrna.68

4. 4.

   Kuehner JN, Pearson EL, Moore C. Unravelling the means to an end: RNA polymerase II transcription termination. Nat Rev Mol Cell Biol. 2011;12:283-294.

   Not in our library10.1038/nrm3098

5. 5.

   Tian B, Graber JH. Signals for pre-mRNA cleavage and polyadenylation. Wiley Interdiscip Rev RNA. 2011;3:385-396.

   Not in our library10.1002/wrna.116

6. 6.

   Yang Q, Doublie S. Structural biology of poly(A) site definition. Wiley Interdiscip Rev RNA. 2011;2:732-747.

   Not in our library10.1002/wrna.88

7. 7.

   Millevoi S, Vagner S. Molecular mechanisms of eukaryotic pre-mRNA 3′ end processing regulation. Nucleic Acids Res. 2009;38:2757-2774.

   Not in our library10.1093/nar/gkp1176

8. 8.

   Chan S, Choi EA, Shi Y. Pre-mRNA 3′-end processing complex assembly and function. Wiley Interdiscip Rev RNA. 2011;2:321-335.

   Not in our library10.1002/wrna.54

9. 9.

   Mandel CR, Kaneko S, Zhang H, Gebauer D, Vethantham V, Manley JL, Tong L. Polyadenylation factor CPSF-73 is the pre-mRNA 3′-end-processing endonuclease. Nature. 2006;444:953-956.

   Not in our library10.1038/nature05363

10. 10.

    Kaufmann I, Martin G, Friedlein A, Langen H, Keller W. Human Fip1 is a subunit of CPSF that binds to U-rich RNA elements and stimulates poly(A) polymerase. EMBO J. 2004;23:616-626.

    Not in our library10.1038/sj.emboj.7600070

11. 11.

    Preker PJ, Lingner J, Minvielle-Sebastia L, Keller W. The FIP1 gene encodes a component of a yeast pre-mRNA polyadenylation factor that directly interacts with poly(A) polymerase. Cell. 1995;81:379-389.

    Not in our library10.1016/0092-8674(95)90391-7

12. 12.

    Takagaki Y, Manley JL. Complex protein interactions within the human polyadenylation machinery identify a novel component. Mol Cell Biol. 2000;20:1515-1525.

    Not in our library10.1128/mcb.20.5.1515-1525.2000

13. 13.

    Kolev NG, Yario TA, Benson E, Steitz JA. Conserved motifs in both CPSF73 and CPSF100 are required to assemble the active endonuclease for histone mRNA 3′-end maturation. EMBO Rep. 2008;9:1013-1018.

    Not in our library10.1038/embor.2008.146

14. 14.

    Yang Q, Gilmartin GM, Doublie S. The structure of human cleavage factor Im hints at functions beyond UGUA-specific RNA binding: A role in alternative polyadenylation and a potential link to 5′ capping and splicing. RNA Biol. 2011;8:748-753.

    Not in our library10.4161/rna.8.5.16040

15. 15.

    Lutz CS, Moreira A. Alternative mRNA polyadenylation in eukaryotes: an effective regulator of gene expression. Wiley Interdiscip Rev RNA. 2011;2:22-31.

    Not in our library10.1002/wrna.47

16. 16.

    Di Giammartino DC, Nishida K, Manley JL. Mechanisms and consequences of alternative polyadenylation. Mol Cell. 2011;43:853-866.

    Not in our library10.1016/j.molcel.2011.08.017

17. 17.

    Dettwiler S, Aringhieri C, Cardinale S, Keller W, Barabino SM. Distinct sequence motifs within the 68-kDa subunit of cleavage factor Im mediate RNA binding, protein-protein interactions, and subcellular localization. J Biol Chem. 2004;279:35788-35797.

    Not in our library10.1074/jbc.m403927200

18. 18.

    Kuhn U, Gundel M, Knoth A, Kerwitz Y, Rudel S, Wahle E. Poly(A) tail length is controlled by the nuclear poly(A)-binding protein regulating the interaction between poly(A) polymerase and the cleavage and polyadenylation specificity factor. J Biol Chem. 2009;284:22803-22814.

    Not in our library10.1074/jbc.m109.018226

19. 19.

    Kerwitz Y, Kuhn U, Lilie H, Knoth A, Scheuermann T, Friedrich H, Schwarz E, Wahle E. Stimulation of poly(A) polymerase through a direct interaction with the nuclear poly(A) binding protein allosterically regulated by RNA. EMBO J. 2003;22:3705-3714.

    Not in our library10.1093/emboj/cdg347

20. 20.

    Bardwell VJ, Zarkower D, Edmonds M, Wickens M. The enzyme that adds poly(A) to mRNAs is a classical poly(A) polymerase. Mol Cell Biol. 1990;10:846-849.

    Not in our library10.1128/mcb.10.2.846-849.1990

21. 21.

    Topalian SL, Kaneko S, Gonzales MI, Bond GL, Ward Y, Manley JL. Identification and functional characterization of neo-poly(A) polymerase, an RNA processing enzyme overexpressed in human tumors. Mol Cell Biol. 2001;21:5614-5623.

    Not in our library10.1128/mcb.21.16.5614-5623.2001

22. 22.

    Shi Y, Di Giammartino DC, Taylor D, Sarkeshik A, Rice WJ, Yates JR, Frank J, Manley JL. Molecular architecture of the human pre-mRNA 3′ processing complex. Mol Cell. 2009;33:365-376.

    Not in our library10.1016/j.molcel.2008.12.028

23. 23.

    Gonzales ML, Mellman DL, Anderson RA. CKIα is associated with and phosphorylates star-PAP and is also required for expression of select star-PAP target messenger RNAs. J Biol Chem. 2008;283:12665-12673.

    Not in our library10.1074/jbc.m800656200

24. 24.

    Laishram RS, Barlow CA, Anderson RA. CKI isoforms {α} and {varepsilon} regulate Star-PAP target messages by controlling Star-PAP poly(A) polymerase activity and phosphoinositide stimulation. Nucleic Acids Res. 2011;39:7961-7973.

    Not in our library10.1093/nar/gkr549

25. 25.

    Laishram RS, Anderson RA. The poly A polymerase Star-PAP controls 3′-end cleavage by promoting CPSF interaction and specificity toward the pre-mRNA. EMBO J. 2010;29:4132-4145.

    Not in our library10.1038/emboj.2010.287

26. 26.

    Li W, Laishram RS, Ji Z, Barlow CA, Tian B, Anderson RA. Star-PAP control of BIK expression and apoptosis is regulated by nuclear PIPKIα and PKCdelta signaling. Mol Cell. 2012;45:25-37.

    Not in our library10.1016/j.molcel.2011.11.017

27. 27.

    Mellman DL, Anderson RA. A novel gene expression pathway regulated by nuclear phosphoinositides. Adv Enzyme Regul. 2009;49:11-28.

    Not in our library10.1016/j.advenzreg.2009.01.007

28. 28.

    Mellman DL, Gonzales ML, Song C, Barlow CA, Wang P, Kendziorski C, Anderson RA. A PtdIns4,5P2-regulated nuclear poly(A) polymerase controls expression of select mRNAs. Nature. 2008;451:1013-1017.

    Not in our library10.1038/nature06666

29. 29.

    Soucek S, Corbett AH, Fasken MB. The long and the short of it: The role of the zinc finger polyadenosine RNA binding protein, Nab2, in control of poly(A) tail length. Biochim Biophys Acta. 1819;2012:546-554.

    Not in our library10.1016/j.bbagrm.2012.03.006

30. 30.

    Sagawa F, Ibrahim H, Morrison AL, Wilusz CJ, Wilusz J. Nucleophosmin deposition during mRNA 3′ end processing influences poly(A) tail length. EMBO J. 2011;30:3994-4005.

    Not in our library10.1038/emboj.2011.272

31. 31.

    Kuehn U, Guendel M, Knoth A, Kerwitz Y, Ruedel S, Wahle E. Poly(A) tail length is controlled by the nuclear poly(A) binding protein regulating the interaction between poly(A) polymerase and the cleavage and polyadenylation specificity factor. J Biol Chem. 2009;284:22803-22814.

    Not in our library10.1074/jbc.m109.018226

32. 32.

    Johnson SA, Kim H, Erickson B, Bentley DL. The export factor Yra1 modulates mRNA 3′ end processing. Nat Struct Mol Biol. 2011;18:1164-1171.

    Not in our library10.1038/nsmb.2126

33. 33.

    Qu X, Lykke-Andersen S, Nasser T, Saguez C, Bertrand E, Jensen TH, Moore C. Assembly of an export-competent mRNP is needed for efficient release of the 3′ end processing complex after polyadenylation. Mol Cell Biol. 2009;29:5327-5338.

    Not in our library10.1128/mcb.00468-09

34. 34.

    Brook M, Gray NK. The role of mammalian poly(A)-binding proteins in co-ordinating mRNA turnover. Biochem Soc Trans. 2012;40:856-864.

    Not in our library10.1042/bst20120100

35. 35.

    Burgess HM, Gray NK. mRNA-specific regulation of translation by poly(A)-binding proteins. Biochem Soc Trans. 2010;38:1517-1522.

    Not in our library10.1042/bst0381517

36. 36.

    Burgess HM, Gray NK. An integrated model for the nucleo-cytoplasmic transport of cytoplasmic poly(A)-binding proteins. Commun Integr Biol. 2012;5:243-247.

    Not in our library10.4161/cib.19347

37. 37.

    Afonina E, Stauber R, Pavlakis GN. The human poly(A)-binding protein 1 shuttles between the nucleus and the cytoplasm. J Biol Chem. 1998;273:13015-13021.

    Not in our library10.1074/jbc.273.21.13015

38. 38.

    Hosoda N, Lejeune F, Maquat LE. Evidence that poly(A) binding protein C1 binds nuclear pre-mRNA poly(A) tails. Mol Cell Biol. 2006;26:3085-3097.

    Not in our library10.1128/mcb.26.8.3085-3097.2006

39. 39.

    Craig AWB, Haghighat A, Yu AT, Sonenberg N. Interaction of polyadenylate-binding protein with the eIF4G homologue PAIP enhances translation. Nature. 1998;392:520-523.

    Not in our library10.1038/33198

40. 40.

    Derry MC, Yanagiya A, Martineau Y, Sonenberg N. Regulation of poly(A)-binding protein through PABP-interacting proteins. Cold Spring Harb Symp Quant Biol. 2006;71:537-543.

    Not in our library10.1101/sqb.2006.71.061

Cited by papers we hold 2

• Cataloguing and Selection of mRNAs Localized to Dendrites in Neurons and Regulated by RNA-Binding Proteins in RNA Granules · 2020
  Not checked
• The non-canonical poly(A) polymerase FAM46C acts as an onco-suppressor in multiple myeloma · 2017
  Not checked

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.