Biological role of the two overlapping poly(A)-binding protein interacting motifs 2 (PAM2) of eukaryotic releasing factor eRF3 in mRNA decay

RNA

Volumn 18, Issue 11, 2012, Pages 1957-1967

  Osawa, Masanori ^a   Hosoda, Nao ^b   Nakanishi, Tamiji ^a   Uchida, Naoyuki ^a   Kimura, Tomomi ^a   Imai, Shunsuke ^a   Machiyama, Asako ^a   Katada, Toshiaki ^a   Hoshino, Shin Ichi ^b   Shimada, Ichio ^a,c  

^a UNIVERSITY OF TOKYO   (Japan)

^b NAGOYA CITY UNIVERSITY   (Japan)

^c NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

Author keywords

Chemical exchange; eRF3; mRNA decay; PAM2; Poly(A) binding protein; Translation

Indexed keywords

EUKARYOTIC RELEASING FACTOR 3; MESSENGER RNA; POLYADENYLIC ACID BINDING PROTEIN; POLYADENYLIC ACID BINDING PROTEIN INTERACTING MOTIF 2; RELEASING FACTOR; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; BIOLOGICAL ACTIVITY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; ISOTHERMAL TITRATION CALORIMETRY; MESSENGER RNA DECAY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; RNA DEGRADATION; RNA TRANSLATION; STOICHIOMETRY;

AMINO ACID SEQUENCE; BETA-GLOBINS; BINDING SITES; CALORIMETRY; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; HALF-LIFE; HELA CELLS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDE TERMINATION FACTORS; POLY A; POLY(A)-BINDING PROTEIN I; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, QUATERNARY; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA STABILITY; RNA, MESSENGER; THERMODYNAMICS; TITRIMETRY;

EID: 84867675615     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.035311.112     Document Type: Article

References (45)

1. Albrecht M, Lengauer T. 2004. Survey on the PABC recognition motif PAM2. Biochem Biophys Res Commun 316: 129-138. (Pubitemid 38299137)
2. Bianchin C, Mauxion F, Sentis S, Seraphin B, Corbo L. 2005. Conservation of the deadenylase activity of proteins of the Caf1 family in human. RNA 11: 487-494. (Pubitemid 40397181)
3. Cavanagh J, Fairbrother WJ, Palmer AG III, Rance M, Skelton NJ. 2006. Chemical exchange effects in NMR spectroscopy. In Protein NMR spectroscopy principles and practice, 2nd ed., pp. 391-404. Elsevier Academic Press, Burlington, MA.
4. Chen J, Chiang YC, Denis CL. 2002. CCR4, a 3′-5′ poly(A) RNA and ssDNA exonuclease, is the catalytic component of the cytoplasmic deadenylase. EMBO J 21: 1414-1426. (Pubitemid 34246520)
5. Cosson B, Couturier A, Chabelskaya S, Kiktev D, Inge-Vechtomov S, Philippe M, Zhouravleva G. 2002. Poly(A)-binding protein acts in translation termination via eukaryotic release factor 3 interaction and does not influence [PSI+] propagation. Mol Cell Biol 22: 3301-3315. (Pubitemid 34453972)
6. Daugeron MC, Mauxion F, Seraphin B. 2001. The yeast POP2 gene encodes a nuclease involved in mRNA deadenylation. Nucleic Acids Res 29: 2448-2455. (Pubitemid 32600298)
7. Decker CJ, Parker R. 1993. A turnover pathway for both stable and unstable mRNAs in yeast: Evidence for a requirement for deadenylation. Genes Dev 7: 1632-1643. (Pubitemid 23234355)
8. Ezzeddine N, Chang TC, Zhu W, Yamashita A, Chen CY, Zhong Z, Yamashita Y, Zheng D, Shyu AB. 2007. Human TOB, an antiproliferative transcription factor, is a poly(A)-binding protein-dependent positive regulator of cytoplasmic mRNA deadenylation. Mol Cell Biol 27: 7791-7801. (Pubitemid 350086413)
9. Fritz DT, Bergman N, Kilpatrick WJ, Wilusz CJ, Wilusz J. 2004. Messenger RNA decay in mammalian cells: The exonuclease perspective. Cell Biochem Biophys 41: 265-278.
10. Frolova L, Le Goff X, Rasmussen HH, Cheperegin S, Drugeon G, Kress M, Arman I, Haenni AL, Celis JE, Philippe M, et al. 1994. A highly conserved eukaryotic protein family possessing properties of polypeptide chain release factor. Nature 372: 701-703.
11. Funakoshi Y, Doi Y, Hosoda N, Uchida N, Osawa M, Shimada I, Tsujimoto M, Suzuki T, Katada T, Hoshino S. 2007. Mechanism of mRNA deadenylation: Evidence for a molecular interplay between translation termination factor eRF3 and mRNA deadenylases. Genes Dev 21: 3135-3148. (Pubitemid 350223530)
12. Gorlach M, Burd CG, Dreyfuss G. 1994. The mRNA poly(A)-binding protein: Localization, abundance, and RNA-binding specificity. Exp Cell Res 211: 400-407. (Pubitemid 124002450)
13. Guntert P. 2004. Automated NMR structure calculation with CYANA. Methods Mol Biol 278: 353-378.
14. Hoshino S, Hosoda N, Araki Y, Kobayashi T, Uchida N, Funakoshi Y, Katada T. 1999a. Novel function of the eukaryotic polypeptide-chain releasing factor 3 (eRF3/GSPT) in the mRNA degradation pathway. Biochemistry (Mosc) 64: 1367-1372. (Pubitemid 129597021)
15. Hoshino S, Imai M, Kobayashi T, Uchida N, Katada T. 1999b. The eukaryotic polypeptide chain releasing factor (eRF3/GSPT) carrying the translation termination signal to the 3′-poly(A) tail of mRNA. Direct association of erf3/GSPT with polyadenylate-binding protein. J Biol Chem 274: 16677-16680.
16. Hosoda N, Kobayashi T, Uchida N, Funakoshi Y, Kikuchi Y, Hoshino S, Katada T. 2003. Translation termination factor eRF3 mediates mRNA decay through the regulation of deadenylation. J Biol Chem 278: 38287-38291. (Pubitemid 37221719)
17. Hosoda N, Funakoshi Y, Hirasawa M, Yamagishi R, Asano Y, Miyagawa R, Ogami K, Tsujimoto M, Hoshino S. 2011. Anti-proliferative protein Tob negatively regulates CPEB3 target by recruiting Caf1 deadenylase. EMBO J 30: 1311-1323.
18. Ikematsu N, Yoshida Y, Kawamura-Tsuzuku J, Ohsugi M, Onda M, Hirai M, Fujimoto J, Yamamoto T. 1999. Tob2, a novel antiproliferative Tob/BTG1 family member, associates with a component of the CCR4 transcriptional regulatory complex capable of binding cyclin-dependent kinases. Oncogene 18: 7432-7441. (Pubitemid 30035044)
19. Jee J, Guntert P. 2003. Influence of the completeness of chemical shift assignments on NMR structures obtained with automated NOE assignment. J Struct Funct Genomics 4: 179-189. (Pubitemid 37356272)
20. Jia S, Meng A. 2007. Tob genes in development and homeostasis. Dev Dyn 236: 913-921. (Pubitemid 46641333)
21. Kononenko AV, Mitkevich VA, Atkinson GC, Tenson T, Dubovaya VI, Frolova LY, Makarov AA, Hauryliuk V. 2010. GTP-dependent structural rearrangement of the eRF1:eRF3 complex and eRF3 sequence motifs essential for PABP binding. Nucleic Acids Res 38:548-558.
22. Kozlov G, Gehring K. 2010. Molecular basis of eRF3 recognition by the MLLE domain of poly(A)-binding protein. PLoS ONE 5:e10169. doi: 10.1371/journal.pone.0010169.
23. Kozlov G, Trempe JF, Khaleghpour K, Kahvejian A, Ekiel I, Gehring K. 2001. Structure and function of the C-terminal PABC domain of human poly(A)-binding protein. Proc Natl Acad Sci 98: 4409-4413. (Pubitemid 32294990)
24. Kozlov G, Siddiqui N, Coillet-Matillon S, Trempe JF, Ekiel I, Sprules T, Gehring K. 2002. Solution structure of the orphan PABC domain from Saccharomyces cerevisiae poly(A)-binding protein. J Biol Chem 277: 22822-22828. (Pubitemid 34967263)
25. Kozlov G, De Crescenzo G, Lim NS, Siddiqui N, Fantus D, Kahvejian A, Trempe JF, Elias D, Ekiel I, Sonenberg N, et al. 2004. 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 23: 272-281. (Pubitemid 38294492)
26. Kozlov G, Menade M, Rosenauer A, Nguyen L, Gehring K. 2010. Molecular determinants of PAM2 recognition by the MLLE domain of poly(A)-binding protein. J Mol Biol 397: 397-407.
27. Laskowski RA, Rullmannn JA, MacArthur MW, Kaptein R, Thornton JM. 1996. AQUA and PROCHECK-NMR: Programs for checking the quality of protein structures solved by NMR. J Biol NMR 8:477-486. (Pubitemid 126706801)
28. Mauxion F, Chen CY, Seraphin B, Shyu AB. 2009. BTG/TOB factors impact deadenylases. Trends Biochem Sci 34: 640-647.
29. Meyer S, Temme C, Wahle E. 2004. Messenger RNA turnover in eukaryotes: Pathways and enzymes. Crit Rev Biochem Mol Biol 39:197-216. (Pubitemid 39447224)
30. Nederveen AJ, Doreleijers JF, Vranken W, Miller Z, Spronk CA, Nabuurs SB, Guntert P, Livny M, Markley JL, Nilges M, et al. 2005. RECOORD: A recalculated coordinate database of 500+ proteins from the PDB using restraints from the BioMagResBank. Proteins 59: 662-672.
31. Neri D, Szyperski T, Otting G, Senn H, Wuthrich K. 1989. Stereospecific nuclear magnetic resonance assignments of the methyl groups of valine and leucine in the DNA-binding domain of the 434 repressor by biosynthetically directed fractional 13C labeling. Biochemistry 28: 7510-7516. (Pubitemid 19238098)
32. Parker R, Song H. 2004. The enzymes and control of eukaryotic mRNA turnover. Nat Struct Mol Biol 11: 121-127. (Pubitemid 38146514)
33. Prevot D, Morel AP, Voeltzel T, Rostan MC, Rimokh R, Magaud JP, Corbo L. 2001. Relationships of the antiproliferative proteins BTG1 and BTG2 with CAF1, the human homolog of a component of the yeast CCR4 transcriptional complex: Involvement in estrogen receptor α signaling pathway. J Biol Chem 276: 9640-9648.
34. Roy G, De Crescenzo G, Khaleghpour K, Kahvejian A, O'Connor-McCourt M, Sonenberg N. 2002. Paip1 interacts with poly(A) binding protein through two independent binding motifs. Mol Cell Biol 22: 3769-3782. (Pubitemid 34525219)
35. Ruan L, Osawa M, Hosoda N, Imai S, Machiyama A, Katada T, Hoshino SI, Shimada I. 2010. Quantitative characterization of Tob interactions provides the thermodynamic basis for translation termination-coupled deadenylase regulation. J Biol Chem 285:27624-27631.
36. Sachs AB, Deardorff JA. 1992. Translation initiation requires the PAB-dependent poly(A) ribonuclease in yeast. Cell 70: 961-973.
37. Siddiqui N, Mangus DA, Chang TC, Palermino JM, Shyu AB, Gehring K. 2007. Poly(A) nuclease interacts with the C-terminal domain of polyadenylate-binding protein domain from poly(A)-binding protein. J Biol Chem 282: 25067-25075. (Pubitemid 47347518)
38. TIS21/BTG2, prototype member of the PC3/BTG/TOB family: Regulator in control of cell growth, differentiation, and DNA repair? J Cell Physiol 187: 155-165.
39. Tucker M, Valencia-Sanchez MA, Staples RR, Chen J, Denis CL, Parker R. 2001. The transcription factor associated Ccr4 and Caf1 proteins are components of the major cytoplasmic mRNA deadenylase in Saccharomyces cerevisiae. Cell 104: 377-386. (Pubitemid 32206458)
40. Uchida N, Hoshino S, Imataka H, Sonenberg N, Katada T. 2002. A novel role of the mammalian GSPT/eRF3 associating with poly(A)-binding protein in Cap/poly(A)-dependent translation. J Biol Chem 277: 50286-50292. (Pubitemid 36042176)
41. Uchida N, Hoshino S, Katada T. 2004. Identification of a human cytoplasmic poly(A) nuclease complex stimulated by poly(A)-binding protein. J Biol Chem 279: 1383-1391. (Pubitemid 38082665)
42. Wiseman T, Williston S, Brandts JF, Lin LN. 1989. Rapid measurement of binding constants and heats of binding using a new titration calorimeter. Anal Biochem 179: 131-137. (Pubitemid 19149635)
43. Yamashita A, Chang TC, Yamashita Y, Zhu W, Zhong Z, Chen CY, Shyu AB. 2005. Concerted action of poly(A) nucleases and decapping enzyme in mammalian mRNA turnover. Nat Struct Mol Biol 12: 1054-1063. (Pubitemid 41746775)
44. Yoshida Y, Hosoda E, Nakamura T, Yamamoto T. 2001. Association of ANA, a member of the antiproliferative Tob family proteins, with a Caf1 component of the CCR4 transcriptional regulatory complex. Jpn J Cancer Res 92: 592-596. (Pubitemid 32633459)
45. Zhouravleva G, Frolova L, Le Goff X, Le Guellec R, Inge-Vechtomov S, Kisselev L, Philippe M. 1995. Termination of translation in eukaryotes is governed by two interacting polypeptide chain release factors, eRF1 and eRF3. EMBO J 14: 4065-4072.