The Three-Dimensional Organization of Polyribosomes in Intact Human Cells

Molecular Cell

Volumn 39, Issue 4, 2010, Pages 560-569

  Brandt, Florian ^a   Carlson, Lars Anders ^a,b   Hartl, F Ulrich ^a   Baumeister, Wolfgang ^a   Grünewald, Kay ^a,c  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^c Division of Structural Biology   (United Kingdom)

Author keywords

Cellbio; RNA

Indexed keywords

ELONGATION FACTOR; TRANSFER RNA; PROTEIN SYNTHESIS INHIBITOR; PUROMYCIN;

ARTICLE; CONTROLLED STUDY; ELECTRON TOMOGRAPHY; HUMAN; HUMAN CELL; POLYSOME; PROTEIN FOLDING; PROTEIN PROCESSING; PROTEIN TARGETING; RIBOSOME; BINDING SITE; BRAIN TUMOR; CHEMICAL STRUCTURE; DRUG EFFECTS; GLIOBLASTOMA; METABOLISM; PROTEIN CONFORMATION; PROTEIN SYNTHESIS; STRUCTURE ACTIVITY RELATION; THREE DIMENSIONAL IMAGING; TUMOR CELL LINE; ULTRASTRUCTURE;

BINDING SITES; BRAIN NEOPLASMS; CELL LINE, TUMOR; ELECTRON MICROSCOPE TOMOGRAPHY; GLIOBLASTOMA; HUMANS; IMAGING, THREE-DIMENSIONAL; MODELS, MOLECULAR; POLYRIBOSOMES; PROTEIN BIOSYNTHESIS; PROTEIN CONFORMATION; PROTEIN SYNTHESIS INHIBITORS; PUROMYCIN; STRUCTURE-ACTIVITY RELATIONSHIP;

BACTERIA (MICROORGANISMS);

EID: 77956006893     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2010.08.003     Document Type: Article

References (46)

1. Ban N., Nissen P., Hansen J., Moore P.B., Steitz T.A. The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution. Science 2000, 289:905-920.
2. Baram D., Pyetan E., Sittner A., Auerbach-Nevo T., Bashan A., Yonath A. Structure of trigger factor binding domain in biologically homologous complex with eubacterial ribosome reveals its chaperone action. Proc. Natl. Acad. Sci. USA 2005, 102:12017-12022.
3. Bartesaghi A., Sprechmann P., Liu J., Randall G., Sapiro G., Subramaniam S. Classification and 3D averaging with missing wedge correction in biological electron tomography. J. Struct. Biol. 2008, 162:436-450.
4. Beckmann R., Spahn C.M., Eswar N., Helmers J., Penczek P.A., Sali A., Frank J., Blobel G. Architecture of the protein-conducting channel associated with the translating 80S ribosome. Cell 2001, 107:361-372.
5. Best C., Nickell S., Baumeister W. Localization of protein complexes by pattern recognition. Methods Cell Biol. 2007, 79:615-638.
6. Blobel G., Dobberstein B. Transfer of proteins across membranes. I. Presence of proteolytically processed and unprocessed nascent immunoglobulin light chains on membrane-bound ribosomes of murine myeloma. J. Cell Biol. 1975, 67:835-851.
7. Böhm J., Frangakis A.S., Hegerl R., Nickell S., Typke D., Baumeister W. Toward detecting and identifying macromolecules in a cellular context: template matching applied to electron tomograms. Proc. Natl. Acad. Sci. USA 2000, 97:14245-14250.
8. Brandt F., Etchells S.A., Ortiz J.O., Elcock A.H., Hartl F.U., Baumeister W. The native 3D organization of bacterial polysomes. Cell 2009, 136:261-271.
9. Buchan J.R., Parker R. Eukaryotic stress granules: the ins and outs of translation. Mol. Cell 2009, 36:932-941.
10. Buchan J.R., Stansfield I. Halting a cellular production line: responses to ribosomal pausing during translation. Biol. Cell 2007, 99:475-487.
11. Chandramouli P., Topf M., Menetret J.F., Eswar N., Cannone J.J., Gutell R.R., Sali A., Akey C.W. Structure of the mammalian 80S ribosome at 8.7 Å resolution. Structure 2008, 16:535-548.
12. Ferbitz L., Maier T., Patzelt H., Bukau B., Deuerling E., Ban N. Trigger factor in complex with the ribosome forms a molecular cradle for nascent proteins. Nature 2004, 431:590-596.
13. Fernandez J.J., Li S., Crowther R.A. CTF determination and correction in electron cryotomography. Ultramicroscopy 2006, 106:587-596.
14. Förster F., Pruggnaller S., Seybert A., Frangakis A.S. Classification of cryo-electron sub-tomograms using constrained correlation. J. Struct. Biol. 2008, 161:276-286.
15. Frangakis A.S., Bohm J., Forster F., Nickell S., Nicastro D., Typke D., Hegerl R., Baumeister W. Identification of macromolecular complexes in cryoelectron tomograms of phantom cells. Proc. Natl. Acad. Sci. USA 2002, 99:14153-14158.
16. Grünewald K., Medalia O., Gross A., Steven A.C., Baumeister W. Prospects of electron cryotomography to visualize macromolecular complexes inside cellular compartments: implications of crowding. Biophys. Chem. 2003, 100:577-591.
17. Halic M., Becker T., Frank J., Spahn C.M., Beckmann R. Localization and dynamic behavior of ribosomal protein L30e. Nat. Struct. Mol. Biol. 2005, 12:467-468.
18. Halic M., Gartmann M., Schlenker O., Mielke T., Pool M.R., Sinning I., Beckmann R. Signal recognition particle receptor exposes the ribosomal translocon binding site. Science 2006, 312:745-747.
19. Hartl F.U., Hayer-Hartl M. Converging concepts of protein folding in vitro and in vivo. Nat. Struct. Mol. Biol. 2009, 16:574-581.
20. Hendrickson D.G., Hogan D.J., McCullough H.L., Myers J.W., Herschlag D., Ferrell J.E., Brown P.O. Concordant regulation of translation and mRNA abundance for hundreds of targets of a human microRNA. PLoS Biol. 2009, 7:e1000238. 10.1371/journal.pbio.1000238.
21. Hundley H.A., Walter W., Bairstow S., Craig E.A. Human Mpp11 J protein: ribosome-tethered molecular chaperones are ubiquitous. Science 2005, 308:1032-1034.
22. Ingolia N.T., Ghaemmaghami S., Newman J.R., Weissman J.S. Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 2009, 324:218-223.
23. Kopeina G.S., Afonina Z.A., Gromova K.V., Shirokov V.A., Vasiliev V.D., Spirin A.S. Step-wise formation of eukaryotic double-row polyribosomes and circular translation of polysomal mRNA. Nucleic Acids Res. 2008, 36:2476-2488.
24. Kramer G., Boehringer D., Ban N., Bukau B. The ribosome as a platform for co-translational processing, folding and targeting of newly synthesized proteins. Nat. Struct. Mol. Biol. 2009, 16:589-597.
25. Lecompte O., Ripp R., Thierry J.C., Moras D., Poch O. Comparative analysis of ribosomal proteins in complete genomes: an example of reductive evolution at the domain scale. Nucleic Acids Res. 2002, 30:5382-5390.
26. Lucic V., Förster F., Baumeister W. Structural studies by electron tomography: from cells to molecules. Annu. Rev. Biochem. 2005, 74:833-865.
27. Madin K., Sawasaki T., Kamura N., Takai K., Ogasawara T., Yazaki K., Takei T., Miura K., Endo Y. Formation of circular polyribosomes in wheat germ cell-free protein synthesis system. FEBS Lett. 2004, 562:155-159.
28. Maiolica A., Cittaro D., Borsotti D., Sennels L., Ciferri C., Tarricone C., Musacchio A., Rappsilber J. Structural analysis of multiprotein complexes by cross-linking, mass spectrometry, and database searching. Mol. Cell. Proteomics 2007, 6:2200-2211.
29. Medalia O., Weber I., Frangakis A.S., Nicastro D., Gerisch G., Baumeister W. Macromolecular architecture in eukaryotic cells visualized by cryoelectron tomography. Science 2002, 298:1209-1213.
30. Menetret J.F., Hegde R.S., Aguiar M., Gygi S.P., Park E., Rapoport T.A., Akey C.W. Single copies of Sec61 and TRAP associate with a nontranslating mammalian ribosome. Structure 2008, 16:1126-1137.
31. Nickell S., Förster F., Linaroudis A., Net W.D., Beck F., Hegerl R., Baumeister W., Plitzko J.M. TOM software toolbox: acquisition and analysis for electron tomography. J. Struct. Biol. 2005, 149:227-234.
32. Ortiz J.O., Förster F., Kurner J., Linaroudis A.A., Baumeister W. Mapping 70S ribosomes in intact cells by cryoelectron tomography and pattern recognition. J. Struct. Biol. 2006, 156:334-341.
33. Pisarev A.V., Hellen C.U., Pestova T.V. Recycling of eukaryotic posttermination ribosomal complexes. Cell 2007, 131:286-299.
34. Schuwirth B.S., Borovinskaya M.A., Hau C.W., Zhang W., Vila-Sanjurjo A., Holton J.M., Cate J.H. Structures of the bacterial ribosome at 3.5 Å resolution. Science 2005, 310:827-834.
35. Sivan G., Kedersha N., Elroy-Stein O. Ribosomal slowdown mediates translational arrest during cellular division. Mol. Cell. Biol. 2007, 27:6639-6646.
36. Slayter H.S., Warner J.R., Rich A., Hall C.E. The visualization of polyribosomal structure. J. Mol. Biol. 1963, 17:652-657.
37. Spahn C.M., Gomez-Lorenzo M.G., Grassucci R.A., Jorgensen R., Andersen G.R., Beckmann R., Penczek P.A., Ballesta J.P., Frank J. Domain movements of elongation factor eEF2 and the eukaryotic 80S ribosome facilitate tRNA translocation. EMBO J. 2004, 23:1008-1019.
38. Spahn C.M., Jan E., Mulder A., Grassucci R.A., Sarnow P., Frank J. Cryo-EM visualization of a viral internal ribosome entry site bound to human ribosomes: the IRES functions as an RNA-based translation factor. Cell 2004, 118:465-475.
39. 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.
40. Trabuco L.G., Villa E., Mitra K., Frank J., Schulten K. Flexible fitting of atomic structures into electron microscopy maps using molecular dynamics. Structure 2008, 16:673-683.
41. Warner J.R., Rich A., Hall C.E. Electron microscope studies of ribosomal clusters synthesizing hemoglobin. Science 1962, 138:1399-1403.
42. Wegrzyn R.D., Hofmann D., Merz F., Nikolay R., Rauch T., Graf C., Deuerling E. A conserved motif is prerequisite for the interaction of NAC with ribosomal protein L23 and nascent chains. J. Biol. Chem. 2006, 281:2847-2857.
43. 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.
44. Wimberly B.T., Brodersen D.E., Clemons W.M., Morgan-Warren R.J., Carter A.P., Vonrhein C., Hartsch T., Ramakrishnan V. Structure of the 30S ribosomal subunit. Nature 2000, 407:327-339.
45. Wolin S.L., Walter P. Ribosome pausing and stacking during translation of a eukaryotic mRNA. EMBO J. 1988, 7:3559-3569.
46. Zanetti G., Riches J.D., Fuller S.D., Briggs J.A. Contrast transfer function correction applied to cryo-electron tomography and sub-tomogram averaging. J. Struct. Biol. 2009, 168:305-312.