Formation of circular polyribosomes on eukaryotic mRNA without cap-structure and poly(A)-tail: A cryo electron tomography study

Nucleic Acids Research

Volumn 42, Issue 14, 2014, Pages 9461-9469

  Afonina, Zhanna A ^a   Myasnikov, Alexander G ^b   Shirokov, Vladimir A ^a   Klaholz, Bruno P ^b   Spirin, Alexander S ^a  

^a INSTITUTE OF PROTEIN RESEARCH   (Russian Federation)

^b UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; INITIATION FACTOR 4F; MESSENGER RNA; POLYADENYLIC ACID; POLYADENYLIC ACID BINDING PROTEIN;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; ELECTRON TOMOGRAPHY; EUKARYOTE; NONHUMAN; POLYADENYLATION; POLYSOME; PRIORITY JOURNAL; PROTEIN INTERACTION; RNA CAPPING; RNA STRUCTURE; RNA TRANSLATION; WHEAT GERM;

CRYOELECTRON MICROSCOPY; ELECTRON MICROSCOPE TOMOGRAPHY; POLY A; POLYRIBOSOMES; RNA CAPS; RNA, MESSENGER;

EID: 84906281181     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku599     Document Type: Article

References (44)

1. Warner, J.R., Rich, A. and Hall, C. (1962) Microscope studies of ribosomal clusters synthesizing hemoglobin. Science, 138, 1399-1403.
2. Warner, J.R., Knopf, P.M. and Rich, A. (1963) A multiple ribosomal structure in protein synthesis. Proc. Natl. Acad. Sci. U.S.A., 49, 122-129.
3. Rich, A., Warner, J.R. and Goodman, H.M. (1963) The structure and function of polyribosomes. Cold Spring Harb. Symp. Quant. Biol., 28, 269-285.
4. Gierer, A. (1963) Function of aggregated reticulocyte ribosomes in protein synthesis. J. Mol. Biol., 6, 148-157.
5. Wettstein, F.O., Staehelin, T. and Noll, H. (1963) Ribosomal aggregate engaged in protein synthesis: characterization of the ergosome. Nature, 197, 430-435.
6. Penman, S., Scherrer, K., Becker, Y. and Darnell, J. (1963) Polyribosomes in normal and poliovirus-infected HeLa cells and their relationship to messenger-RNA. Proc. Natl. Acad. Sci. U.S.A., 49, 654-662.
7. Palade, G.E. (1955) A small particular component of the cytoplasm. J. Biophys. Biochem. Cytol., 1, 59-68.
8. Mathias, A.P., Williamson, R., Huxley, H.E. and Page, S. (1964) Occurrence and function of polysomes in rabbit reticulocytes. J. Mol. Biol., 9, 154-167.
9. Shelton, E. and Kuff, E.L. (1966) Substructure and configuration of ribosomes isolated from mammalian cells. J. Mol. Biol., 22, 23-31.
10. Dallner, G., Siekevitz, P. and Palade, G.E. (1966) Biogenesis of endoplasmic reticulum membranes. I. Structural and chemical differentiation in developing rat hepatocyte. J. Cell Biol., 30, 73-96.
11. Christensen, A.K., Kahn, L.E. and Bourne, C.M. (1987) Circular polysomes predominate on the rough endoplasmic reticulum of somatotropes and mammotropes in the rat anterior pituitary. Am. J. Anat., 178, 1-10.
12. Christensen, A.K. and Bourne, C.M. (1999) Shape of large bound polysomes in cultured fibroblasts and thyroid epithelial cells. Anat. Rec., 255, 116-129.
13. Philipps, G.R. (1965) Haemoglobin synthesis and polysomes in intact reticulocytes. Nature, 205, 53-56.
14. Adamson, S.D., Howard, G.A. and Herbert, E. (1969) The ribosome cycle in a reconstituted cell-free system from reticulocytes. Cold Spring Harb. Symp. Quant. Biol., 34, 547-554.
15. Baglioni, C., Vesco, C. and Jacobs-Lorena, M. (1969) The role of ribosomal subunits in mammalian cells. Cold Spring Harb. Symp. Quant. Biol., 34, 555-565.
16. Gallie, D.R. (1991) The cap and poly(A) tail function synergistically to regulate mRNA translational efficiency. Genes Dev., 5, 2108-2116.
17. Gallie, D.R. and Tanguay, R. (1994) Poly(A) binds to initiation factors and increases cap-dependent translation in vitro. J. Biol. Chem., 269, 17166-17173.
18. Tarun, S.Z.J. and Sachs, A.B. (1996) Association of the yeast poly(A) tail binding protein with translation initiation factor eIF-4G. EMBO J., 15, 7168-7177.
19. Tarun, S.Z. Jr, Wells, S.E., Deardorff, J.A. and Sachs, A.B. (1997) Translation initiation factor eIF4G mediates in vitro poly(A) tail-dependent translation. Proc. Natl. Acad. Sci. U.S.A., 94, 9046-9051.
20. Le, H., Tanguay, R.L., Balasta, M.L., Wei, C.C., Browning, K.S., Metz, A.M., Goss, D.J. and Gallie, D.R. (1997) Translation initiation factors eIF-iso4G and eIF-4B interact with the poly(A)-binding protein and increase its RNA binding activity. J. Biol. Chem., 272, 16247-16255.
21. Wei, C.C., Balasta, M.L., Ren, J. and Goss, D.J. (1998) Wheat germ poly(A) binding protein enhances the binding affinity of eukaryotic initiation factor 4F and (iso)4F for cap analogues. Biochemistry, 17, 1910-1916.
22. Imataka, H., Gradi, A. and Sonenberg, N. (1998) 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., 17, 7480-7489.
23. Wells, S.E., Hillner, P.E., Vale, R.D. and Sachs, A.B. (1998) Circularization of mRNA by eukaryotic translation initiation factors. Mol. Cell, 2, 135-140.
24. Jacobson, A. (1996) Poly(A) metabolism and translation: the close-loop model. In: Hershey, JWB et al. Translational Control., CSHL Press, New York pp. 451-480.
25. Amrani, N., Ghosh, S., Mangus, A. and Jacobson, A. (2008) Translation factors promote formation of two states of the closed loop mRNP. Nature, 453, 1276-1280.
26. Spirin, A.S., Baranov, V.I., Ryabova, L.A., Ovodov, S.Y. and Alakhov, Y.B. (1988) A continuous cell-free translation system capable of producing polypeptides in high yield. Science, 242, 1162-1164.
27. Spirin, A.S. (2004) High-throughput cell-free systems for synthesis of functionally active proteins. Trends Biotech., 22, 538-545.
28. Shirokov, V.A., Kommer, A., Kolb, V.A. and Spirin, A.S. (2007) Continuous-exchange protein-synthesizing systems. In: Grandi, G (ed). Methods in Molecular Biology: In Vitro Transcription and Translation Protocols. 2nd edn, Vol. 375. Humana Press Inc., Totowa, NJ, 19,55.
29. Shaloiko, L.A., Granovsky, I.E., Ivashina, T.V., Ksenzenko, V.N., Shirokov, V.A. and Spirin, A.S. (2004) Effective non-viral leader for cap-independent translation in a eukaryotic cell-free system. Biotech. Bioeng., 88, 730-739.
30. Kopeina, G.S., Afonina, Z.A., Gromova, K.V., Shirokov, V.A., Vasiliev, V.D. and Spirin, A.S. (2008) Step-wise formation of eukaryotic double-row polyribosomes and circular translation of polysomal mRNA. Nucleic Acids Res. 36, 2476-2488.
31. Afonina, Zh.A., Myasnikov, A.G., Khabibullina, N.F., Belorusova, A.Yu., Ménétret, J.-F., Vasiliev, V.D., Klaholz, B. P., Shirokov, V.A. and Spirin, A.S. (2013) Topology of mRNA chain in isolated eukaryotic double-row polyribosomes. Biochemistry (Moscow) 78, 445-454.
32. Vassilenko, K.S., Alekhina, O.M., Dmitriev, S.E., Shatsky, I.N. and Spirin, A.S. (2011) Unidirectional constant rate motion of the ribosomal scanning particle during eukaryotic translation initiation. Nucleic Acids Res., 39, 5555-5567.
33. Sorzano, C.O.S., Marabini, R., Velazquez-Muriel, J., Bilbao-Castro, J. R., Scheres, S.H.W., Carazo, J.M. and Pascual-Montano, A. (2004) XMIPP: a new generation of an open-source image processing package for electron microscopy. J. Struct. Biol., 148, 194-204.
34. Halic, M., Becker, T., Frank, J., Spahn, C.M. and Beckmann, R. (2005) Localization and dynamic behavior of ribosomal protein L30e. Nat. Struct. Mol. Biol. 12, 467-468.
35. Pettersen, E.F., Goddard, T.D., Huang, C.C., Couch, G.S., Greenblatt, D.M., Meng, E.C. and Ferrin, T.E. (2004) UCSF Chimera - a visualization system for exploratory research and analysis. J. Comput. Chem., 25, 1605-1612.
36. Evstafieva, A.G., Shatsky, N., Bogdanov, A.A., Semenkov, Y.P. and Vasiliev, V.D. (1983) Localization of 5′ and 3′ ends of the ribosome-bound segment of template polynucleotides by immune electron microscopy. EMBO J., 2, 799-804.
37. Yusupova, G.Zh., Yusupov, M.M., Cate, J.H.D. and Noller, H.F. (2001) The path of messenger RNA through the ribosome. Cell, 106, 233-241.
38. Spirin, A.S. and Ajtkhozin, M.A. (1985) Informosomes and polyribosome-associated proteins in eukaryotes. TIBS, 10, 162-165.
39. Ryazanov, A.G., Ovchinnikov, L.P. and Spirin, A.S. (1987) Development of structural organization of protein-synthesizing machinery from prokaryotes to eukaryotes. Biosystems 20, 275-288.
40. Yoshida, T., Wakiyama, M., Yazaki, K. and Miura, K.-I. (1997) Transmission electron and atomic force microscopic observation of polysomes on carbon-coated grids prepared by surface spreading. J. Electron Microsc. (Tokyo), 46, 503-506.
41. Madin, K., Sawasaki, T., Kamura, N., Takai, K., Ogasawara, T., Yazaki, K., Takei, T., Miura, K.-I. and Endo, Y. (2004) Formation of circular polyribosomes in wheat germ cell-free protein synthesis system. FEBS Lett., 562, 155-159.
42. Brandt, F., Carlson, L.A., Hartl, F.U., Baumeister, W. and Grunewald, K. (2010) The three-dimensional organization of polyribosomes in intact human cells. Mol. Cell 39, 560-569.
43. Skabkin, M.A., Skabkina, O.V., Hellen, C.U.T. and Pestova, T.V. (2013) Reinitiation and other unconventional posttermination events during eukaryotic translation. Mol. Cell 51, 249-264.
44. Agalarov, S.Ch., Sakharov, P.A., Fattakhova, D.Kh., Sogorin, E.A. and Spirin, A.S. (2014) Internal translation initiation and eIF4F/ATP-independent scanning of mRNA by eukaryotic ribosomal particles. Sci. Rep., 4,4438.