Distinct roles of the R3H and RRM domains in poly(A)-specific ribonuclease structural integrity and catalysis

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1834, Issue 6, 2013, Pages 1089-1098

  He, Guang Jun ^a   Zhang, Ao ^a,b   Liu, Wei Feng ^a,c   Yan, Yong Bin ^a  

^a TSINGHUA UNIVERSITY   (China)

^b LERNER RESEARCH INSTITUTE   (United States)

^c INSTITUTE OF MICROBIOLOGY   (China)

Author keywords

Enzymatic property; Poly(A) specific ribonuclease (PARN); RNA binding; Structural feature; The R3H domain; The RRM domain

Indexed keywords

MONOMER; OLIGONUCLEOTIDE; RIBONUCLEASE;

ARTICLE; BINDING AFFINITY; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVE SITE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; RNA BINDING;

BINDING SITES; CATALYSIS; EXORIBONUCLEASES; HUMANS; MUTATION; OLIGONUCLEOTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; RNA, MESSENGER; RNA-BINDING PROTEINS;

EUKARYOTA;

EID: 84878106701     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2013.01.038     Document Type: Article

References (45)

1. C.J. Wilusz, and J. Wilusz Bringing the role of mRNA decay in the control of gene expression into focus Trends Genet. 20 2004 491 497
2. N.L. Garneau, J. Wilusz, and C.J. Wilusz The highways and byways of mRNA decay Nat. Rev. Mol. Cell Biol. 8 2007 113 126
3. C.J. Wilusz, M. Wormington, and S.W. Peltz The cap-to-tail guide to mRNA turnover Nat. Rev. Mol. Cell Biol. 2 2001 237 246
4. J. Houseley, and D. Tollervey The many pathways of RNA degradation Cell 136 2009 763 776
5. A.C. Goldstrohm, and M. Wickens Multifunctional deadenylase complexes diversify mRNA control Nat. Rev. Mol. Cell Biol. 9 2008 337 344
6. X. Zhang, A. Virtanen, and F.E. Kleiman To polyadenylate or to deadenylate: That is the question Cell Cycle 9 2010 4437 4449
7. C.J. Utter, S.A. Garcia, J. Milone, and V. Bellofatto PolyA-specific ribonuclease (PARN-1) function in stage-specific mRNA turnover in Trypanosoma brucei Eukaryot. Cell 10 2011 1230 1240
8. S.V. Reverdatto, J.A. Dutko, J.A. Chekanova, D.A. Hamilton, and D.A. Belostotsky MRNA deadenylation by PARN is essential for embryogenesis in higher plants RNA 10 2004 1200 1214
9. Y. Chiba, M.A. Johnson, P. Lidder, J.T. Vogel, H. van Erp, and P.J. Green AtPARN is an essential poly(A) ribonuclease in Arabidopsis Gene 328 2004 95 102
10. C.G. Körner, M. Wormington, M. Muckenthaler, S. Schneider, E. Dehlin, and E. Wahle The deadenylating nuclease (DAN) is involved in poly(A) tail removal during the meiotic maturation of Xenopus oocytes EMBO J. 17 1998 5427 5437
11. R. Seal, R. Temperley, J. Wilusz, R.N. Lightowlers, and Z.M.A. Chrzanowska-Lightowlers Serum-deprivation stimulates cap-binding by PARN at the expense of eIF4E, consistent with the observed decrease in mRNA stability Nucleic Acids Res. 33 2005 376 387
12. N. Nishimura, N. Kitahata, M. Seki, Y. Narusaka, M. Narusaka, T. Kuromori, T. Asami, K. Shinozaki, and T. Hirayama Analysis of ABA Hypersensitive Germination2 revealed the pivotal functions of PARN in stress response in Arabidopsis Plant J. 44 2005 972 984
13. H.C. Reinhardt, P. Hasskamp, I. Schmedding, S. Morandell, M.A. van Vugt, X. Wang, R. Linding, S.E. Ong, D. Weaver, S.A. Carr, and M.B. Yaffe DNA damage activates a spatially distinct late cytoplasmic cell-cycle checkpoint network controlled by MK2-mediated RNA stabilization Mol. Cell 40 2010 34 49
14. M.A. Cevher, X. Zhang, S. Fernandez, S. Kim, J. Baquero, P. Nilsson, S. Lee, A. Virtanen, and F.E. Kleiman Nuclear deadenylation/polyadenylation factors regulate 3′ processing in response to DNA damage EMBO J. 29 2010 1674 1687
15. N. Balatsos, D. Vlachakis, V. Chatzigeorgiou, S. Manta, D. Komiotis, M. Vlassi, and C. Stathopoulos Kinetic and in silico analysis of the slow-binding inhibition of human poly(A)-specific ribonuclease (PARN) by novel nucleoside analogues Biochimie 94 2012 214 221
16. N.A.A. Balatsos, D. Vlachakis, P. Maragozidis, S. Manta, D. Anastasakis, A. Kyritsis, M. Vlassi, D. Komiotis, and C. Stathopoulos Competitive inhibition of human poly(A)-specific ribonuclease (PARN) by synthetic fluoro-pyranosyl nucleosides Biochemistry 48 2009 6044 6051
17. G.-J. He, W.-F. Liu, and Y.-B. Yan Dissimilar roles of the four conserved acidic residues in the thermal stability of poly(A)-specific ribonuclease Int. J. Mol. Sci. 12 2011 2901 2916
18. W.-F. Liu, A. Zhang, Y. Cheng, H.-M. Zhou, and Y.-B. Yan Effect of magnesium ions on the thermal stability of human poly(A)-specific ribonuclease FEBS Lett. 581 2007 1047 1052
19. M.S. Wu, M. Reuter, H. Lilie, Y.Y. Liu, E. Wahle, and H.W. Song Structural insight into poly(A) binding and catalytic mechanism of human PARN EMBO J. 24 2005 4082 4093
20. Y.-G. Ren, L.A. Kirsebom, and A. Virtanen Coordination of divalent metal ions in the active site of poly(A)-specific ribonuclease J. Biol. Chem. 279 2004 48702 48706
21. 2 +-mediated cleavage J. Biol. Chem. 277 2002 5982 5987
22. J. Åström, A. Åström, and A. Virtanen Properties of a HeLa cell 3′ exonuclease specific for degrading poly(A) tails of mammalian mRNA J. Biol. Chem. 267 1992 18154 18159
23. E. Dehlin, M. Wormington, C.G. Korner, and E. Wahle Cap-dependent deadenylation of mRNA EMBO J. 19 2000 1079 1086
24. M. Gao, D.T. Fritz, L.P. Ford, and J. Wilusz Interaction between a poly(A)-specific ribonuclease and the 5′ Cap influences mRNA deadenylation rates in vitro Mol. Cell 5 2000 479 488
25. J. Martînez, Y.G. Ren, P. Nilsson, M. Ehrenberg, and A. Virtanen The mRNA cap structure stimulates rate of poly(A) removal and amplifies processivity of degradation J. Biol. Chem. 276 2001 27923 27929
26. A. Niedzwiecka, M. Lekka, P. Nilsson, and A. Virtanen Global architecture of human poly(A)-specific ribonuclease by atomic force microscopy in liquid and dynamic light scattering Biophys. Chem. 158 2011 141 149
27. G.-J. He, A. Zhang, W.-F. Liu, Y. Cheng, and Y.-B. Yan Conformational stability and multistate unfolding of poly(A)-specific ribonuclease FEBS J. 276 2009 2849 2860
28. P.R. Copeland, and M. Wormington The mechanism and regulation of deadenylation: Identification and characterization of Xenopus PARN RNA 7 2001 875 886
29. 7GpppG binding to poly(A)-specific ribonuclease Structure 17 2009 276 286
30. W.-F. Liu, A. Zhang, G.-J. He, and Y.-B. Yan The R3H domain stabilizes poly(A)-specific ribonuclease by stabilizing the RRM domain Biochem. Biophys. Res. Commun. 360 2007 846 851
31. P. Nilsson, N. Henriksson, A. Niedzwiecka, N.A.A. Balatsos, K. Kokkoris, J. Eriksson, and A. Virtanen A multifunctional RNA recognition motif in poly(A)-specific ribonuclease with cap and poly(A) binding properties J. Biol. Chem. 282 2007 32902 32911
32. N. Henriksson, P. Nilsson, M. Wu, H. Song, and A. Virtanen Recognition of adenosine residues by the active site of poly(A)-specific ribonuclease J. Biol. Chem. 285 2010 163 170
33. T. Nagata, S. Suzuki, R. Endo, M. Shirouzu, T. Terada, M. Inoue, T. Kigawa, N. Kobayashi, P. Guntert, A. Tanaka, Y. Hayashizaki, Y. Muto, and S. Yokoyama The RRM domain of poly(A)-specific ribonuclease has a noncanonical binding site for mRNA cap analog recognition Nucleic Acids Res. 36 2008 4754 4767
34. 7G-cap-binding mode J. Mol. Biol. 382 2008 827 834
35. A. Zhang, W.-F. Liu, and Y.-B. Yan Role of the RRM domain in the activity, structure and stability of poly(A)-specific ribonuclease Arch. Biochem. Biophys. 461 2007 255 262
36. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72 1976 248 254
37. L. Stryer The interaction of a naphthalene dye with apomyoglobin and apohemoglobin. A fluorescent probe of non-polar binding sites J. Mol. Biol. 13 1965 482 495
38. G.-J. He, and Y.-B. Yan A deadenylase assay by size-exclusion chromatography PLoS One 7 2012 e33700
39. T.M. Lohman, and D.P. Mascotti Nonspecific ligand-DNA equilibrium binding parameters determined by fluorescence methods Methods Enzymol. 212 1992 424 458
40. S. Wang, W.-F. Liu, Y.-Z. He, A. Zhang, L. Huang, Z.-Y. Dong, and Y.-B. Yan Multistate folding of a hyperthermostable Fe-superoxide dismutase (TcSOD) in guanidinium hydrochloride: The importance of the quaternary structure Biochim. Biophys. Acta Proteins Proteomics 1784 2008 445 454
41. W.-F. Liu, A. Zhang, Y. Cheng, H.-M. Zhou, and Y.-B. Yan Allosteric regulation of human poly(A)-specific ribonuclease by cap and potassium ions Biochem. Biophys. Res. Commun. 379 2009 341 345
42. W.-F. Liu, and Y.-B. Yan Biophysical and biochemical characterization of recombinant human Pop2 deadenylase Protein Expr. Purif. 60 2008 46 52
43. J. Martìnez, Y.G. Ren, A.C. Thuresson, U. Hellma, J. Åström, and A. Virtanen A 54-kDa fragment of the poly(A)-specific ribonuclease is an oligomeric, processive, and cap-interacting poly(A)-specific 3′ exonuclease J. Biol. Chem. 275 2000 24222 24230
44. C.G. Körner, and E. Wahle Poly(A) tail shortening by a mammalian poly(A)-specific 3′-exoribonuclease J. Biol. Chem. 272 1997 10448 10456
45. C. Maris, C. Dominguez, and F.H.-T. Allain The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression FEBS J. 272 2005 2118 2131