Pin1 and WWP2 regulate GluR2 Q/R site RNA editing by ADAR2 with opposing effects

EMBO Journal

Volumn 30, Issue 20, 2011, Pages 4211-4222

  Marcucci, Roberto ^a   Brindle, James ^a   Paro, Simona ^a   Casadio, Angela ^a   Hempel, Sophie ^a   Morrice, Nicholas ^b   Bisso, Andrea ^c,d   Keegan, Liam P ^a   Del Sal, Giannino ^c,d   O'Connell, Mary A ^a  

^a WESTERN GENERAL HOSPITAL   (United Kingdom)

^b BEATSON INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

^c Laboratorio Nazionale CIB   (Italy)

^d UNIVERSITY OF TRIESTE   (Italy)

Author keywords

ADAR2; GluR2; Pin1; RNA editing; WWP2

Indexed keywords

ADENOSINE DEAMINASE; CELL PROTEIN; PEPTIDYLPROLYL ISOMERASE PIN1; RNA; UBIQUITIN PROTEIN LIGASE E3;

ARTICLE; CYTOPLASM; EMBRYO DEVELOPMENT; FIBROBLAST; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY;

ADENOSINE DEAMINASE; ANIMALS; CELL LINE; FIBROBLASTS; MICE; PEPTIDYLPROLYL ISOMERASE; RECEPTORS, AMPA; RNA EDITING; RNA POLYMERASE II; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 80054895180     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.303     Document Type: Article

References (47)

1. Aizawa H, Sawada J, Hideyama T, Yamashita T, Katayama T, Hasebe N, Kimura T, Yahara O, Kwak S (2010) TDP-43 pathology in sporadic ALS occurs in motor neurons lacking the RNA editing enzyme ADAR2. Acta Neuropathol 120: 75-84
2. Ayala YM, Misteli T, Baralle FE (2008) TDP-43 regulates retinoblas-toma protein phosphorylation through the repression of cyclin-dependent kinase 6 expression. Proc Natl Acad Sci USA 105: 3785-3789 (Pubitemid 351723476)
3. Beullens M, Vancauwenbergh S, Morrice N, Derua R, Ceulemans H, Waelkens E, Bollen M (2005) Substrate specificity and activity regulation of protein kinase MELK. J Biol Chem 280: 40003-40011 (Pubitemid 41779134)
4. Buratti E, Baralle FE (2001) Characterization and functional implications of the RNA binding properties of nuclear factor TDP-43, a novel splicing regulator of CFTR exon 9. J Biol Chem 276: 36337-36343
5. Davis FM, Tsao TY, Fowler SK, Rao PN (1983) Monoclonal antibodies to mitotic cells. Proc Natl Acad Sci USA 80: 2926-2930
6. Dephoure N, Zhou C, Villen J, Beausoleil SA, Bakalarski CE, Elledge SJ, Gygi SP (2008) A quantitative atlas of mitotic phosphoryla-tion. Proc Natl Acad Sci USA 105: 10762-10767
7. Desterro JM, Keegan LP, Lafarga M, Berciano MT, O'Connell M, Carmo-Fonseca M (2003) Dynamic association of RNA-editing enzymes with the nucleolus. J Cell Sci 116: 1805-1818 (Pubitemid 36582167)
8. Fujimori F, Takahashi K, Uchida C, Uchida T (1999) Mice lacking Pin1 develop normally, but are defective in entering cell cycle from G(0) arrest. Biochem Biophys Res Commun 265: 658-663
9. Gallo A, Keegan LP, Ring GM, O'Connell MA (2003) An ADAR that edits transcripts encoding ion channel subunits functions as a dimer. EMBO J 22: 3421-3430 (Pubitemid 36834872)
10. Greger IH, Khatri L, Kong X, Ziff EB (2003) AMPA receptor tetra-merization is mediated by q/r editing. Neuron 40: 763-774 (Pubitemid 37431036)
11. Heale BS, Keegan LP, McGurk L, Michlewski G, Brindle J, Stanton CM, Caceres JF, O'Connell MA (2009) Editing independent effects of ADARs on the miRNA/siRNA pathways. EMBO J 28: 3145-3156
12. Higuchi M, Maas S, Single FN, Hartner J, Rozov A, Burnashev N, Feldmeyer D, Sprengel R, Seeburg PH (2000) Point mutation in an AMPA receptor gene rescues lethality in mice deficient in the RNA-editing enzyme ADAR2. Nature 406: 78-81 (Pubitemid 30460214)
13. Higuchi M, Single FN, Kohler M, Sommer B, Sprengel R, Seeburg PH (1993) RNA editing of AMPA receptor subunit GluR-B: a base-paired intron-exon structure determines position and efficiency. Cell 75: 1361-1370 (Pubitemid 24021910)
14. Hollmann M, Hartley M, Heinemann S (1991) Ca2+ permeability of KA-AMPA-gated glutamate receptor channels depends on sub-unit composition. Science 252: 851-853 (Pubitemid 121000528)
15. Kask K, Zamanillo D, Rozov A, Burnashev N, Sprengel R, Seeburg PH (1998) The AMPA receptor subunit GluR-B in its Q/R site-unedited form is not essential for brain development and function. Proc Natl Acad Sci USA 95: 13777-13782 (Pubitemid 28523049)
16. Kawahara Y, Ito K, Sun H, Aizawa H, Kanazawa I, Kwak S (2004) Glutamate receptors: RNA editing and death of motor neurons. Nature 427: 801
17. Lai F, Chen CX, Lee VM, Nishikura K (1997) Dramatic increase of the RNA editing for glutamate receptor subunits during terminal differentiation of clonal human neurons. J Neurochem 69: 43-52 (Pubitemid 27274154)
18. Lee TH, Chen CH, Suizu F, Huang P, Schiene-Fischer C, Daum S, Zhang YJ, Goate A, Chen RH, Zhou XZ, Lu KP (2011) Death-associated protein kinase 1 phosphorylates Pin1 and inhibits its prolyl isomerase activity and cellular function. Mol Cell 42: 147-159
19. Li H, Zhang Z, Wang B, Zhang J, Zhao Y, Jin Y (2007) Wwp2-mediated ubiquitination of the RNA polymerase II large subunit in mouse embryonic pluripotent stem cells. Mol Cell Biol 27: 5296-5305 (Pubitemid 47124385)
20. Liu S, Lau L, Wei J, Zhu D, Zou S, Sun HS, Fu Y, Liu F, Lu Y (2004) Expression of Ca(2+)-permeable AMPA receptor channels primes cell death in transient forebrain ischemia. Neuron 43: 43-55 (Pubitemid 38952818)
21. Liu SJ, Zukin RS (2007) Ca2+-permeable AMPA receptors in synaptic plasticity and neuronal death. Trends Neurosci 30: 126-134 (Pubitemid 46283597)
22. Lu KP, Zhou XZ (2007) The prolyl isomerase PIN1: a pivotal new twist in phosphorylation signalling and disease. Nat Rev Mol Cell Biol 8: 904-916 (Pubitemid 47622559)
23. Lu PJ, Zhou XZ, Liou YC, Noel JP, Lu KP (2002) Critical role of WW domain phosphorylation in regulating phosphoserine binding activity and Pin1 function. J Biol Chem 277: 2381-2384 (Pubitemid 34953258)
24. Lu PJ, Zhou XZ, Shen M, Lu KP (1999) Function of WW domains as phosphoserine-or phosphothreonine-binding modules. Science 283: 1325-1328
25. Macbeth MR, Lingam AT, Bass BL (2004) Evidence for auto-inhibition by the N terminus of hADAR2 and activation by dsRNA binding. RNA 10: 1563-1571 (Pubitemid 39288191)
26. Macbeth MR, Schubert HL, Vandemark AP, Lingam AT, Hill CP, Bass BL (2005) Inositol hexakisphosphate is bound in the ADAR2 core and required for RNA editing. Science 309: 1534-1539 (Pubitemid 41266474)
27. O'Connell MA, Gerber A, Keller W (1997) Purification of human double-stranded RNA-specific editase 1 (hRED1) involved in editing of brain glutamate receptor B pre-mRNA. J Biol Chem 272: 473-478 (Pubitemid 27021182)
28. Parrinello S, Samper E, Krtolica A, Goldstein J, Melov S, Campisi J (2003) Oxygen sensitivity severely limits the replicative lifespan of murine fibroblasts. Nat Cell Biol 5: 741-747 (Pubitemid 36986782)
29. Peng PL, Zhong X, Tu W, Soundarapandian MM, Molner P, Zhu D, Lau L, Liu S, Liu F, Lu Y (2006) ADAR2-dependent RNA editing of AMPA receptor subunit GluR2 determines vulnerability of neurons in forebrain ischemia. Neuron 49: 719-733 (Pubitemid 43290131)
30. Pirozzi G, McConnell SJ, Uveges AJ, Carter JM, Sparks AB, Kay BK, Fowlkes DM (1997) Identification of novel human WW domain-containing proteins by cloning of ligand targets. J Biol Chem 272: 14611-14616 (Pubitemid 27251722)
31. Poulsen H, Jorgensen R, Heding A, Nielsen FC, Bonven B, Egebjerg J (2006) Dimerization of ADAR2 is mediated by the double-stranded RNA binding domain. RNA 12: 1350-1360 (Pubitemid 43990559)
32. Ranganathan R, Lu KP, Hunter T, Noel JP (1997) Structural and functional analysis of the mitotic rotamase Pin1 suggests substrate recognition is phosphorylation dependent. Cell 89: 875-886 (Pubitemid 27513514)
33. Ring GM, O'Connell MA, Keegan LP (2004) Purification and assay of recombinant ADAR proteins expressed in the yeast Pichia pastoris or in Escherichia coli. Methods Mol Biol 265: 219-238
34. Rodriguez MS, Desterro JM, Lain S, Midgley CA, Lane DP, Hay RT (1999) SUMO-1 modification activates the transcriptional response of p53. EMBO J 18: 6455-6461 (Pubitemid 29533249)
35. Rustighi A, Tiberi L, Soldano A, Napoli M, Nuciforo P, Rosato A, Kaplan F, Capobianco A, Pece S, Di Fiore PP, Del Sal G (2009) The prolyl-isomerase Pin1 is a Notch1 target that enhances Notch1 activation in cancer. Nat Cell Biol 11: 133-142
36. Ryo A, Nakamura M, Wulf G, Liou YC, Lu KP (2001) Pin1 regulates turnover and subcellular localization of beta-catenin by inhibiting its interaction with APC. Nat Cell Biol 3: 793-801 (Pubitemid 32842684)
37. Ryo A, Suizu F, Yoshida Y, Perrem K, Liou YC, Wulf G, Rottapel R, Yamaoka S, Lu KP (2003) Regulation of NF-kappaB signaling by Pin1-dependent prolyl isomerization and ubiquitin-mediated proteolysis of p65/RelA. Mol Cell 12: 1413-1426 (Pubitemid 38037011)
38. Sansam CL, Wells KS, Emeson RB (2003) Modulation of RNA editing by functional nucleolar sequestration of ADAR2. Proc Natl Acad Sci USA 100: 14018-14023 (Pubitemid 37499183)
39. Sommer B, Kohler M, Sprengel R, Seeburg PH (1991) RNA editing in brain controls a determinant of ion flow in glutamate-gated channels. Cell 67: 11-19 (Pubitemid 121001421)
40. Valente L, Nishikura K (2007) RNA binding-independent dimerization of adenosine deaminases acting on RNA and dominant negative effects of nonfunctional subunits on dimer functions. J Biol Chem 282: 16054-16061 (Pubitemid 47100344)
41. Verdoorn TA, Burnashev N, Monyer H, Seeburg PH, Sakmann B (1991) Structural determinants of ion flow through recombinant glutamate receptor channels. Science 252: 1715-1718 (Pubitemid 21917095)
42. Wong SK, Sato S, Lazinski DW (2003) Elevated activity of the large form of ADAR1 in vivo: very efficient RNA editing occurs in the cytoplasm. RNA 9: 586-598 (Pubitemid 36505456)
43. Wu X, Chang A, Sudol M, Hanes SD (2001) Genetic interactions between the ESS1 prolyl-isomerase and the RSP5 ubiquitin ligase reveal opposing effects on RNA polymerase II function. Curr Genet 40: 234-242 (Pubitemid 34036856)
44. Xu YX, Manley JL (2007) Pin1 modulates RNA polymerase II activity during the transcription cycle. Genes Dev 21: 2950-2962 (Pubitemid 350133442)
45. Yaffe MB, Schutkowski M, Shen M, Zhou XZ, Stukenberg PT, Rahfeld JU, Xu J, Kuang J, Kirschner MW, Fischer G, Cantley LC, Lu KP (1997) Sequence-specific and phosphorylation-depen-dent proline isomerization: a potential mitotic regulatory mechanism. Science 278: 1957-1960 (Pubitemid 28013239)
46. Zacchi P, Gostissa M, Uchida T, Salvagno C, Avolio F, Volinia S, Ronai Z, Blandino G, Schneider C, Del Sal G (2002) The prolyl isomerase Pin1 reveals a mechanism to control p53 functions after genotoxic insults. Nature 419: 853-857 (Pubitemid 35238573)
47. Zheng H, You H, Zhou XZ, Murray SA, Uchida T, Wulf G, Gu L, Tang X, Lu KP, Xiao ZX (2002) The prolyl isomerase Pin1 is a regulator of p53 in genotoxic response. Nature 419: 849-853 (Pubitemid 35238572)