Polyribosomes are molecular 3D nanoprinters that orchestrate the assembly of vault particles

ACS Nano

Volumn 8, Issue 11, 2014, Pages 11552-11559

  Mrazek, Jan ^a   Toso, Daniel ^b   Ryazantsev, Sergey ^a,b   Zhang, Xing ^b   Zhou, Z Hong ^b   Fernandez, Beatriz Campo ^b   Kickhoefer, Valerie A ^a   Rome, Leonard H ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cryo electron tomography; Nanoprinting; Polyribosome function; Structure based mutagenesis; Vault particle

Indexed keywords

ELECTRIC IMPEDANCE TOMOGRAPHY; GENES; MUTAGENESIS; PROTEINS;

CELLULAR ENVIRONMENT; CRYO-ELECTRON TOMOGRAPHY; GENETIC INFORMATION; MOLECULAR MACHINES; NANOPRINTING; PROTEIN STRUCTURES; RIBONUCLEOPROTEIN COMPLEX; STRUCTURE-BASED;

BIOSYNTHESIS;

AMINO ACID SEQUENCE; ANIMAL; CELL LINE; COMPUTER ASSISTED TOMOGRAPHY; MOLECULAR GENETICS; POLYSOME; SEQUENCE HOMOLOGY; SPODOPTERA; THREE DIMENSIONAL PRINTING;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; MOLECULAR SEQUENCE DATA; POLYRIBOSOMES; PRINTING, THREE-DIMENSIONAL; SEQUENCE HOMOLOGY, AMINO ACID; SPODOPTERA; TOMOGRAPHY, X-RAY COMPUTED;

EID: 84912571664     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn504778h     Document Type: Article

References (24)

1. Warner, J. R.; Knopf, P. M.; Rich, A. A Multiple Ribosomal Structure in Protein Synthesis. Proc. Natl. Acad. Sci. U.S.A. 1963, 49, 122-9.
2. Warner, J. R.; Rich, A.; Hall, C. E. Electron Microscope Studies of Ribosomal Clusters Synthesizing Hemoglobin. Science 1962, 138, 1399-403.
3. Martin, K.A.; Miller, O. L., Jr. Polysome Structure in SeaUrchin Eggs and Embryos: An Electron Microscopic Analysis. Dev. Biol. 1983, 98, 338-48.
4. Christensen, A. K.; Bourne, C. M. Shape of Large Bound Polysomes in Cultured Fibroblasts and Thyroid Epithelial Cells. Anat. Rec. 1999, 255, 116-29.
5. 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, 2476-88.
6. 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, 261-71.
7. Brandt, F.; Carlson, L. A.; Hartl, F. U.; Baumeister, W.; Grunewald, K. The Three-Dimensional Organization of Polyribosomes in Intact Human Cells. Mol. Cell 2010, 39, 560-9.
8. Kedersha, N. L.; Rome, L. H. Isolation and Characterization of a Novel Ribonucleoprotein Particle: Large Structures Contain a Single Species of Small Rna. J. Cell Biol. 1986, 103, 699-709.
9. Berger, W.; Steiner, E.; Grusch, M.; Elbling, L.; Micksche, M. Vaults and the Major Vault Protein: Novel Roles in Signal Pathway Regulation and Immunity. Cell. Mol. Life Sci. 2009, 66, 43-61.
10. Tanaka, H.; Kato, K.; Yamashita, E.; Sumizawa, T.; Zhou, Y.; Yao, M.; Iwasaki, K.; Yoshimura, M.; Tsukihara, T. The Structure of Rat Liver Vault at 3.5 Angstrom Resolution. Science 2009, 323, 384-8.
11. Mikyas, Y.; Makabi, M.; Raval-Fernandes, S.; Harrington, L.; Kickhoefer, V. A.; Rome, L. H.; Stewart, P. L. Cryoelectron Microscopy Imaging of Recombinant and Tissue Derived Vaults: Localization of the MVP N Termini and VPARP. J. Mol. Biol. 2004, 344, 91-105.
12. Anderson, D. H.; Kickhoefer, V. A.; Sievers, S. A.; Rome, L. H.; Eisenberg, D. Draft Crystal Structure of the Vault Shell at 9-A˚ Resolution. PLoS Biol. 2007, 5, e318.
13. Rome, L. H.; Kickhoefer, V. A. Development of the Vault Particle as a Platform Technology. ACS Nano 2013, 7, 889-902.
14. Han, M.; Kickhoefer, V. A.; Nemerow, G. R.; Rome, L. H. Targeted Vault Nanoparticles Engineered with an Endosomolytic Peptide Deliver Biomolecules to the Cytoplasm. ACS Nano 2011, 5, 6128-37.
15. Buehler, D. C.; Marsden, M. D.; Shen, S.; Toso, D. B.; Wu, X.; Loo, J. A.; Zhou, Z. H.; Kickhoefer, V. A.; Wender, P. A.; Zack, J. A.; Rome, L. H. Bioengineered Vaults: Self-Assembling Protein Shell-Lipophilic Core Nanoparticles for Drug Delivery. ACS Nano 2014, 8, 7723-32.
16. Pettersen, E. F.; Goddard, T. D.; Huang, C. C.; Couch, G. S.; Greenblatt, D. M.; Meng, E. C.; Ferrin, T. E. UCSF Chimera - A Visualization System for Exploratory Research and Analysis. J. Comput. Chem. 2004, 25, 1605-12.
17. 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 A˚ Resolution. Structure 2008, 16, 535-48.
18. Pfeffer, S.; Brandt, F.; Hrabe, T.; Lang, S.; Eibauer, M.; Zimmermann, R.; Forster, F. Structure and 3D Arrangement of Endoplasmic Reticulum Membrane-Associated Ribosomes. Structure 2012, 20, 1508-18.
19. Nicholls, C. D.; McLure, K. G.; Shields, M. A.; Lee, P. W. Biogenesis of P53 Involves Cotranslational Dimerization of Monomers and Posttranslational Dimerization of Dimers. Implications on the Dominant Negative Effect. J. Biol. Chem. 2002, 277, 12937-45.
20. Lin, L.; DeMartino, G. N.; Greene, W. C. Cotranslational Dimerization of the Rel Homology Domain of Nf-κb1 Generates P50-P105 Heterodimers and Is Required for Effective P50 Production. EMBO J. 2000, 19, 4712-22.
21. Fulton, A. B.; L'Ecuyer, T. Cotranslational Assembly of Some Cytoskeletal Proteins: Implications and Prospects. J. Cell Sci. 1993, 105, 867-71.
22. Duncan, C. D.; Mata, J. Widespread Cotranslational Formation of Protein Complexes. PLoS Gen. 2011, 7, e1002398.
23. Stephen, A. G.; Raval-Fernandes, S.; Huynh, T.; Torres, M.; Kickhoefer, V. A.; Rome, L. H. Assembly of Vault-like Particles in Insect Cells Expressing Only the Major Vault Protein. J. Biol. Chem. 2001, 276, 23217-20.
24. Poderycki, M. J.; Kickhoefer, V. A.; Kaddis, C. S.; Raval-Fernandes, S.; Johansson, E.; Zink, J. I.; Loo, J. A.; Rome, L. H. The Vault Exterior Shell Is a Dynamic Structure That Allows Incorporation of Vault-Associated Proteins into Its Interior. Biochemistry 2006, 45, 12184-93.