Interdomain Allostery Promotes Assembly of the Poly(A) mRNA Complex with PABP and eIF4G

Molecular Cell

Volumn 48, Issue 3, 2012, Pages 375-386

  Safaee, Nozhat ^a   Kozlov, Guennadi ^a   Noronha, Anne M ^a,b   Xie, Jingwei ^a   Wilds, Christopher J ^a,b   Gehring, Kalle ^a  

^a MCGILL UNIVERSITY   (Canada)

^b Gina Cody School of Engineering and Computer Science   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CELL EXTRACT; INITIATION FACTOR 4G; MULTIPROTEIN COMPLEX; POLYADENYLATED RNA; POLYADENYLIC ACID BINDING PROTEIN; RIBONUCLEOPROTEIN;

ALLOSTERISM; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; GEL MOBILITY SHIFT ASSAY; HELA CELL; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; ISOTHERMAL TITRATION CALORIMETRY; NUCLEAR MAGNETIC RESONANCE; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; RADIATION SCATTERING; RNA BINDING; RNA STRUCTURE;

AMINO ACID SEQUENCE; BINDING SITES; CALORIMETRY; CRYSTALLOGRAPHY, X-RAY; ELECTROPHORETIC MOBILITY SHIFT ASSAY; EUKARYOTIC INITIATION FACTOR-4G; HELA CELLS; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; NUCLEIC ACID CONFORMATION; POLY A; POLY(A)-BINDING PROTEIN I; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RIBONUCLEOPROTEINS; RNA, MESSENGER; SCATTERING, SMALL ANGLE; SEQUENCE HOMOLOGY, AMINO ACID; X-RAY DIFFRACTION;

EUKARYOTA;

EID: 84869085954     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2012.09.001     Document Type: Article

References (48)

1. Amrani N., Ghosh S., Mangus D.A., Jacobson A. Translation factors promote the formation of two states of the closed-loop mRNP. Nature 2008, 453:1276-1280.
2. Belsham G. Picornavirus RNA translation: roles for cellular proteins. Trends Microbiol. 2000, 8:330-335.
3. Borman A.M. Free poly(A) stimulates capped mRNA translation in vitro through the eIF4G-poly(A)-binding Protein interaction. J. Biol. Chem. 2002, 277:36818-36824.
4. Braunstein S., Karpisheva K., Pola C., Goldberg J., Hochman T., Yee H., Cangiarella J., Arju R., Formenti S.C., Schneider R.J. A hypoxia-controlled cap-dependent to cap-independent translation switch in breast cancer. Mol. Cell 2007, 28:501-512.
5. Burgess H.M., Gray N.K. mRNA-specific regulation of translation by poly(A)-binding proteins. Biochem. Soc. Trans. 2010, 38:1517-1522.
6. Clemens M.J., Bushell M., Jeffrey I.W., Pain V.M., Morley S.J. Translation initiation factor modifications and the regulation of protein synthesis in apoptotic cells. Cell Death Differ. 2000, 7:603-615.
7. Cléry A., Blatter M., Allain F.H.-T. RNA recognition motifs: boring? Not quite. Curr. Opin. Struct. Biol. 2008, 18:290-298.
8. Craig A.W., Haghighat A., Yu A.T., Sonenberg N. Interaction of polyadenylate-binding protein with the eIF4G homologue PAIP enhances translation. Nature 1998, 392:520-523.
9. Deo R.C., Bonanno J.B., Sonenberg N., Burley S.K. Recognition of polyadenylate RNA by the poly(A)-binding protein. Cell 1999, 98:835-845.
10. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 2004, 60:2126-2132.
11. Fabian M.R., Mathonnet G., Sundermeier T., Mathys H., Zipprich J.T., Svitkin Y.V., Rivas F., Jinek M., Wohlschlegel J., Doudna J.A., et al. Mammalian miRNA RISC recruits CAF1 and PABP to affect PABP-dependent deadenylation. Mol. Cell 2009, 35:1-13.
12. Franke D., Svergun D.I. DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering. J. Appl. Cryst. 2009, 42:342-346.
13. Fukuchi-Shimogori T., Ishii I., Kashiwagi K., Mashiba H., Ekimoto H., Igarashi K. Malignant transformation by overproduction of translation initiation factor eIF4G. Cancer Res. 1997, 57:5041-5044.
14. Garcia M.A., Gil J., Ventoso I., Guerra S., Domingo E., Rivas C., Esteban M. Impact of protein kinase PKR in cell biology: from antiviral to antiproliferative action. Microbiol. Mol. Biol. Rev. 2006, 70:1032-1060.
15. Görlach M., Burd C.G., Dreyfuss G. The mRNA poly(A)-binding protein: localization, abundance, and RNA-binding specificity. Exp. Cell Res. 1994, 211:400-407.
16. Groft C.M., Burley S.K. Recognition of eIF4G by rotavirus NSP3 reveals a basis for mRNA circularization. Mol. Cell 2002, 9:1273-1283.
17. Gross J., Moerke N., von der Haar T., Lugovskoy A., Sachs A.B., McCarthy J., Wagner G. Ribosome loading onto the mRNA cap is driven by conformational coupling between eIF4G and eIF4E. Cell 2003, 115:739-750.
18. Hinton T.M., Coldwell M.J., Carpenter G.A., Morley S.J., Pain V.M. Functional analysis of individual binding activities of the scaffold protein eIF4G. J. Biol. Chem. 2007, 282:1695-1708.
19. Imataka H., Gradi A., Sonenberg N. A newly identified N-terminal amino acid sequence of human eIF4G binds poly(A)-binding protein and functions in poly(A)-dependent translation. EMBO J. 1998, 17:7480-7489.
20. Kahvejian A. Mammalian poly(A)-binding protein is a eukaryotic translation initiation factor, which acts via multiple mechanisms. Genes Dev. 2005, 19:104-113.
21. Khaleghpour K., Kahvejian A., De Crescenzo G., Roy G., Svitkin Y.V., Imataka H., O'Connor-McCourt M., Sonenberg N. Dual interactions of the translational repressor Paip2 with poly (A) binding protein. Mol. Cell. Biol. 2001, 21:5200-5213.
22. Khaleghpour K., Svitkin Y.V., Craig A.W., DeMaria C.T., Deo R.C., Burley S.K., Sonenberg N. Translational repression by a novel partner of human poly(A) binding protein, Paip2. Mol. Cell 2001, 7:205-216.
23. Korneeva N.L. Mutually cooperative binding of eukaryotic translation initiation factor (eIF) 3 and eIF4A to human eIF4G-1. J. Biol. Chem. 2000, 275:41369-41376.
24. Kozin M.B., Svergun D.I. Automated matching of high- and low-resolution structural models. J. Appl. Cryst. 2001, 34:33-41.
25. Kozlov G., Trempe J.F., Khaleghpour K., Kahvejian A., Ekiel I., Gehring K. Structure and function of the C-terminal PABC domain of human poly(A)-binding protein. Proc. Natl. Acad. Sci. USA 2001, 98:4409-4413.
26. Kozlov G., Safaee N., Rosenauer A., Gehring K. Structural basis of binding of P-body-associated proteins GW182 and ataxin-2 by the Mlle domain of poly(A)-binding protein. J. Biol. Chem. 2010, 285:13599-13606.
27. LeFebvre A.K., Korneeva N.L., Trutschl M., Cvek U., Duzan R.D., Bradley C.A., Hershey J.W.B., Rhoads R.E. Translation initiation factor eIF4G-1 binds to eIF3 through the eIF3e subunit. J. Biol. Chem. 2006, 281:22917-22932.
28. Mackereth C. Dynamics in multi-domain protein recognition of RNA. Curr. Opin. Struct. Biol. 2012, 22:1-10.
29. Marintchev A., Edmonds K.A., Marintcheva B., Hendrickson E., Oberer M., Suzuki C., Herdy B., Sonenberg N., Wagner G. Topology and regulation of the human eIF4A/4G/4H helicase complex in translation initiation. Cell 2009, 136:447-460.
30. Michel Y.M., Poncet D., Piron M., Kean K.M., Borman A.M. Cap-Poly(A) synergy in mammalian cell-free extracts. Investigation of the requirements for poly(A)-mediated stimulation of translation initiation. J. Biol. Chem. 2000, 275:32268-32276.
31. Murshudov G.N., Vagin A.A., Lebedev A., Wilson K.S., Dodson E.J. Efficient anisotropic refinement of macromolecular structures using FFT. Acta Crystallogr. D Biol. Crystallogr. 1999, 55:247-255.
32. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 1997, 276:307-326.
33. Piron M., Vende P., Cohen J., Poncet D. Rotavirus RNA-binding protein NSP3 interacts with eIF4GI and evicts the poly(A) binding protein from eIF4F. EMBO J. 1998, 17:5811-5821.
34. Ramirez-Valle F., Braunstein S., Zavadil J., Formenti S.C., Schneider R.J. eIF4GI links nutrient sensing by mTOR to cell proliferation and inhibition of autophagy. J. Cell Biol. 2008, 181:293-307.
35. Read R.J. Pushing the boundaries of molecular replacement with maximum likelihood. Acta Crystallogr. D Biol. Crystallogr. 2001, 57:1373-1382.
36. Sachs A.B., Sarnow P., Hentze M.W. Starting at the beginning, middle, and end: translation initiation in eukaryotes. Cell 1997, 89:831-838.
37. Smith R.W.P., Gray N.K. Poly(A)-binding protein (PABP): a common viral target. Biochem. J. 2010, 426:1-12.
38. Sonenberg N., Hinnebusch A.G. New modes of translational control in development, behavior, and disease. Mol. Cell 2007, 28:721-729.
39. Sonenberg N., Hinnebusch A.G. Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 2009, 136:731-745.
40. Svergun D.I. Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Cryst. 1992, 25:495-503.
41. Svitkin Y.V., Imataka H., Khaleghpour K., Kahvejian A., Liebig H.D., Sonenberg N. Poly(A)-binding protein interaction with elF4G stimulates picornavirus IRES-dependent translation. RNA 2001, 7:1743-1752.
42. Tarun S.Z., Sachs A.B. A common function for mRNA " 5 and 3" ends in translation initiation in yeast. Genes Dev. 1995, 9:2997-3007.
43. Tarun S.Z., Sachs A.B. Association of the yeast poly (A) tail binding protein with translation initiation factor eIF-4G. EMBO J. 1996, 15:7168-7177.
44. Tarun S.Z., Wells S.E., Deardorff J.A., Sachs A.B. Translation initiation factor eIF4G mediates in vitro poly(A) tail-dependent translation. Proc. Natl. Acad. Sci. USA 1997, 94:9046-9051.
45. Volkov V.V., Svergun D.I. Uniqueness of ab initio shape determination in small-angle scattering. J. Appl. Cryst. 2003, 36:860-864.
46. Wells S.E., Hillner P.E., Vale R.D., Sachs A.B. Circularization of mRNA by eukaryotic translation initiation factors. Mol. Cell 1998, 2:135-140.
47. Winn M.D., Murshudov G.N., Papiz M.Z. Macromolecular TLS refinement in REFMAC at moderate resolutions. Methods Enzymol. 2003, 374:300-321.
48. Zekri L., Huntzinger E., Heimstadt S., Izaurralde E. The silencing domain of GW182 interacts with PABPC1 to promote translational repression and degradation of microRNA targets and is required for target release. Mol. Cell. Biol. 2009, 29:6220-6231.