Dissecting macromolecular recognition sites in ribosome: implication to its self-assembly

References

• Ramakrishnan V. Ribosome structure and the mechanism of translation. Cell. 2002;108:557–572.
   PubMed Web of Science ®Google Scholar
• Maivali U, Remme J. Definition of bases in 23S rRNA essential for ribosomal subunit association. RNA. 2004;10:600–604.
   PubMed Web of Science ®Google Scholar
• Sharma MR, Koc EC, Datta PP, et al. Structure of the mammalian mitochondrial ribosome reveals an expanded functional role for its component proteins. Cell. 2003;115:97–108.
   PubMed Web of Science ®Google Scholar
• Ramakrishnan V. The ribosome: some hard facts about its structure and hot air about its evolution. Cold Spring Harb Symp Quant Biol. 2009;74:25–33.
   PubMedGoogle Scholar
• Schnare MN, Damberger SH, Gray MW, et al. Comprehensive comparison of structural characteristics in eukaryotic cytoplasmic large subunit (23 S-like) ribosomal RNA. J Mol Biol. 1996;256:701–719.
   PubMed Web of Science ®Google Scholar
• Wilson DN, Doudna Cate JH. The structure and function of the eukaryotic ribosome. Cold Spring Harb Perspect Biol. 2012;4:a011536.
   Web of Science ®Google Scholar
• Woolford JL Jr., Baserga SJ. Ribosome biogenesis in the yeast Saccharomyces cerevisiae. Genetics. 2013;195:643–681.
   PubMed Web of Science ®Google Scholar
• Timsit Y, Acosta Z, Allemand F, et al. The role of disordered ribosomal protein extensions in the early steps of eubacterial 50 S ribosomal subunit assembly. Int J Mol Sci. 2009;10:817–834.
   PubMed Web of Science ®Google Scholar
• Ban N, Nissen P, Hansen J, et al. The complete atomic structure of the large ribosomal subunit at 2.4 A resolution. Science. 2000;289:905–920.
   PubMed Web of Science ®Google Scholar
• Wimberly BT, Brodersen DE, Clemons WM Jr., et al. Structure of the 30S ribosomal subunit. Nature. 2000;407:327–339.
   PubMed Web of Science ®Google Scholar
• Davies C, White SW, Ramakrishnan V. The crystal structure of ribosomal protein L14 reveals an important organizational component of the translational apparatus. Structure. 1996;4:55–66.
   PubMed Web of Science ®Google Scholar
• Golden BL, Ramakrishnan V, White SW. Ribosomal protein L6: structural evidence of gene duplication from a primitive RNA binding protein. EMBO J. 1993;12:4901–4908.
   PubMed Web of Science ®Google Scholar
• Venema J, Tollervey D. Ribosome synthesis in Saccharomyces cerevisiae. Annu Rev Genet. 1999;33:261–311.
   PubMed Web of Science ®Google Scholar
• Henras AK, Soudet J, Gerus M, et al. The post-transcriptional steps of eukaryotic ribosome biogenesis. Cell Mol Life Sci. 2008;65:2334–2359.
   PubMed Web of Science ®Google Scholar
• Eichler DC, Craig N. Processing of eukaryotic ribosomal RNA. Prog Nucleic Acid Res Mol Biol. 1994;49:197–239.
   PubMedGoogle Scholar
• Burton B, Zimmermann MT, Jernigan RL, et al. A computational investigation on the connection between dynamics properties of ribosomal proteins and ribosome assembly. PLoS Comput Biol. 2012;8:e1002530.
   PubMed Web of Science ®Google Scholar
• Agalarov SC, Sridhar Prasad G, Funke PM, et al. Structure of the S15,S6,S18-rRNA complex: assembly of the 30S ribosome central domain. Science. 2000;288:107–113.
   PubMed Web of Science ®Google Scholar
• Ohmayer U, Gamalinda M, Sauert M, et al. Studies on the assembly characteristics of large subunit ribosomal proteins in S cerevisae. PLoS One. 2013;8:e68412.
   PubMed Web of Science ®Google Scholar
• Gamalinda M, Jakovljevic J, Babiano R, et al. Yeast polypeptide exit tunnel ribosomal proteins L17, L35 and L37 are necessary to recruit late-assembling factors required for 27SB pre-rRNA processing. Nucleic Acids Res. 2013;41:1965–1983.
   PubMed Web of Science ®Google Scholar
• Robledo S, Idol RA, Crimmins DL, et al. The role of human ribosomal proteins in the maturation of rRNA and ribosome production. RNA. 2008;14:1918–1929.
   PubMed Web of Science ®Google Scholar
• Ferreira-Cerca S, Poll G, Gleizes PE, et al. Roles of eukaryotic ribosomal proteins in maturation and transport of pre-18S rRNA and ribosome function. Mol Cell. 2005;20:263–275.
   PubMed Web of Science ®Google Scholar
• Kim H, Abeysirigunawarden SC, Chen K, et al. Protein-guided RNA dynamics during early ribosome assembly. Nature. 2014;506:334–338.
   PubMed Web of Science ®Google Scholar
• Held WA, Ballou B, Mizushima S, et al. Assembly mapping of 30 S ribosomal proteins from Escherichia coli Further studies. J Biol Chem. 1974;249:3103–3111.
   PubMed Web of Science ®Google Scholar
• Nierhaus KH. The assembly of prokaryotic ribosomes. Biochimie. 1991;73:739–755.
   PubMed Web of Science ®Google Scholar
• Rohl R, Nierhaus KH. Assembly map of the large subunit (50S) of Escherichia coli ribosomes. Proc Natl Acad Sci U S A. 1982;79:729–733.
   PubMed Web of Science ®Google Scholar
• Nierhaus KH, Dohme F. Total reconstitution of functionally active 50S ribosomal subunits from Escherichia coli. Proc Natl Acad Sci U S A. 1974;71:4713–4717.
   PubMed Web of Science ®Google Scholar
• Ferreira-Cerca S, Poll G, Kuhn H, et al. Analysis of the in vivo assembly pathway of eukaryotic 40S ribosomal proteins. Mol Cell. 2007;28:446–457.
   PubMed Web of Science ®Google Scholar
• Rabl J, Leibundgut M, Ataide SF, et al. Crystal structure of the eukaryotic 40S ribosomal subunit in complex with initiation factor 1. Science. 2011;331:730–736.
   PubMed Web of Science ®Google Scholar
• Karbstein K. Inside the 40S ribosome assembly machinery. Curr Opin Chem Biol. 2011;15:657–663.
   PubMed Web of Science ®Google Scholar
• Dutca LM, Culver GM. Assembly of the 5ʹ and 3ʹ minor domains of 16S ribosomal RNA as monitored by tethered probing from ribosomal protein S20. J Mol Biol. 2008;376:92–108.
   PubMed Web of Science ®Google Scholar
• Mulder AM, Yoshioka C, Beck AH, et al. Visualizing ribosome biogenesis: parallel assembly pathways for the 30S subunit. Science. 2010;330:673–677.
   PubMed Web of Science ®Google Scholar
• de la Cruz J, Karbstein K, Woolford JL Jr. Functions of ribosomal proteins in assembly of eukaryotic ribosomes in vivo. Annu Rev Biochem. 2015;84:93–129.
   PubMed Web of Science ®Google Scholar
• Ban N, Beckmann R, Cate JH, et al. A new system for naming ribosomal proteins. Curr Opin Struct Biol. 2014;24:165–169.
   PubMed Web of Science ®Google Scholar
• Brodersen DE, Clemons WM Jr., Carter AP, et al. Crystal structure of the 30 S ribosomal subunit from Thermus thermophilus: structure of the proteins and their interactions with 16 S RNA. J Mol Biol. 2002;316:725–768.
   PubMed Web of Science ®Google Scholar
• Klein DJ, Moore PB, Steitz TA. The roles of ribosomal proteins in the structure assembly, and evolution of the large ribosomal subunit. J Mol Biol. 2004;340:141–177.
   PubMed Web of Science ®Google Scholar
• Poirot O, Timsit Y. Neuron-like networks between ribosomal proteins within the ribosome. Sci Rep. 2016;6:26485.
   PubMed Web of Science ®Google Scholar
• Berman HM, Westbrook J, Feng Z, et al. The protein data bank. Nucleic Acids Res. 2000;28:235–242.
   PubMed Web of Science ®Google Scholar
• Barik A, Pilla CN, Bahadur RP SP. Molecular architecture of protein-RNA recognition sites. J Biomol Struct Dyn. 2015;33:2738–2751.
   PubMed Web of Science ®Google Scholar
• Breiman L. Random forests. Mach Learn. 2001;45:5–32.
   Web of Science ®Google Scholar
• Bahadur RP, Chakrabarti P, Rodier F, et al. A dissection of specific and non-specific protein-protein interfaces. J Mol Biol. 2004;336:943–955.
   PubMed Web of Science ®Google Scholar
• Bahadur RP, Zacharias M, Janin J. Dissecting protein-RNA recognition sites. Nucleic Acids Res. 2008;36:2705–2716.
   PubMed Web of Science ®Google Scholar
• McDonald IK, Thornton JM. Satisfying hydrogen bonding potential in proteins. J Mol Biol. 1994;238:777–793.
   PubMed Web of Science ®Google Scholar
• Barlow DJ, Thornton JM. Ion-pairs in proteins. J Mol Biol. 1983;168:867–885.
   PubMed Web of Science ®Google Scholar
• Xu D, Tsai CJ, Nussinov R. Hydrogen bonds and salt bridges across protein-protein interfaces. Protein Eng. 1997;10:999–1012.
   PubMedGoogle Scholar
• Allers J, Shamoo Y. Structure-based analysis of protein-RNA interactions using the program ENTANGLE. J Mol Biol. 2001;311:75–86.
   PubMed Web of Science ®Google Scholar
• Lawrence MC, Colman PM. Shape complementarity at protein/protein interfaces. J Mol Biol. 1993;234:946–950.
   PubMed Web of Science ®Google Scholar
• Hubbard S. NACCESS: program for calculating accessibilities. Department of biochemistry and molecular biology. London: University College of London; 1992.
   Google Scholar
• Kabsch W, Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers. 1983;22:2577–2637.
   PubMed Web of Science ®Google Scholar
• Savelsbergh A, Rodnina MV, Wintermeyer W. Distinct functions of elongation factor G in ribosome recycling and translocation. RNA. 2009;15:772–780.
   PubMed Web of Science ®Google Scholar
• Balagopal V, Parker R. Stm1 modulates translation after 80S formation in Saccharomyces cerevisiae. RNA. 2011;17:835–842.
   PubMed Web of Science ®Google Scholar
• Nadassy K, Wodak SJ, Janin J. Structural features of protein-nucleic acid recognition sites. Biochemistry. 1999;38:1999–2017.
   PubMed Web of Science ®Google Scholar
• Treger M, Westhof E. Statistical analysis of atomic contacts at RNA-protein interfaces. J Mol Recognit. 2001;14:199–214.
   PubMed Web of Science ®Google Scholar
• Ellis JJ, Broom M, Jones S. Protein-RNA interactions: structural analysis and functional classes. Proteins. 2007;66:903–911.
   PubMed Web of Science ®Google Scholar
• Hwang H, Vreven T, Janin J, et al. Protein-protein docking benchmark version 4.0. Proteins. 2010;78:3111–3114.
   PubMed Web of Science ®Google Scholar
• Bahadur RP, Chakrabarti P, Rodier F, et al. Dissecting subunit interfaces in homodimeric proteins. Proteins. 2003;53:708–719.
   PubMed Web of Science ®Google Scholar
• Guthrie C, Nomura M. Initiation of protein synthesis: a critical test of the 30S subunit model. Nature. 1968;219:232–235.
   PubMed Web of Science ®Google Scholar
• Hirokawa G, Nijman RM, Raj VS, et al. The role of ribosome recycling factor in dissociation of 70S ribosomes into subunits. RNA. 2005;11:1317–1328.
   PubMed Web of Science ®Google Scholar
• Tissieres A, Watson JD, Schlessinger D, et al. Ribonucleoprotein particles from Escherichia coli. J Mol Biol. 1959;1:221–233.
   Web of Science ®Google Scholar
• Gavrilova L, Ivanov D, Spirin A. Studies on the structure of ribosomes: III. Stepwise unfolding of the 50Sparticles without loss of ribosomal protein. J Mol Biol. 1966;16:473-489.
   PubMed Web of Science ®Google Scholar
• Nierhaus KH. Mg2+, K+, and the ribosome. J Bacteriol. 2014;196:3817–3819.
   PubMedGoogle Scholar
• Lo Conte L, Chothia C, Janin J. The atomic structure of protein-protein recognition sites. J Mol Biol. 1999;285:2177–2198.
   PubMed Web of Science ®Google Scholar
• Bahadur RP, Rodier F, Janin J. A dissection of the protein-protein interfaces in icosahedral virus capsids. J Mol Biol. 2007;367:574–590.
   PubMed Web of Science ®Google Scholar
• Iwakiri J, Tateishi H, Chakraborty A, et al. Dissecting the protein-RNA interface: the role of protein surface shapes and RNA secondary structures in protein-RNA recognition. Nucleic Acids Res. 2012;40:3299–3306.
   PubMed Web of Science ®Google Scholar
• Costantini S, Colonna G, Facchiano AM. ESBRI: a web server for evaluating salt bridges in proteins. Bioinformation. 2008;3:137–138.
   PubMedGoogle Scholar
• Neves MA, Yeager M, Abagyan R. Unusual arginine formations in protein function and assembly: rings, strings, and stacks. J Phys Chem B. 2012;116:7006–7013.
   PubMed Web of Science ®Google Scholar
• Wilson KA, Kellie JL, Wetmore SD. DNA-protein pi-interactions in nature: abundance, structure, composition and strength of contacts between aromatic amino acids and DNA nucleobases or deoxyribose sugar. Nucleic Acids Res. 2014;42:6726–6741.
   PubMed Web of Science ®Google Scholar
• Chen R, Weng Z. A novel shape complementarity scoring function for protein-protein docking. Proteins. 2003;51:397–408.
   PubMed Web of Science ®Google Scholar
• Shajani Z, Sykes MT, Williamson JR. Assembly of bacterial ribosomes. Annu Rev Biochem. 2011;80:501–526.
   PubMed Web of Science ®Google Scholar
• Levy ED, Boeri Erba E, Robinson CV, et al. Assembly reflects evolution of protein complexes. Nature. 2008;453:1262–1265.
   PubMed Web of Science ®Google Scholar
• Bahadur RP, Janin J. Residue conservation in viral capsid assembly. Proteins. 2008;71:407–414.
   PubMed Web of Science ®Google Scholar
• Yanshina DD, Bulygin KN, Malygin AA, et al. Hydroxylated histidine of human ribosomal protein uL2 is involved in maintaining the local structure of 28S rRNA in the ribosomal peptidyl transferase center. FEBS J. 2015;282:1554–1566.
   PubMed Web of Science ®Google Scholar
• Diedrich G, Spahn CM, Stelzl U, et al. Ribosomal protein L2 is involved in the association of the ribosomal subunits, tRNA binding to A and P sites and peptidyl transfer. EMBO J. 2000;19:5241–5250.
   PubMed Web of Science ®Google Scholar
• Lee B, Richards FM. The interpretation of protein structures: estimation of static accessibility. J Mol Biol. 1971;55:379–400.
   PubMed Web of Science ®Google Scholar
• Barik A, Mishra A, Bahadur RP. PRince: a web server for structural and physicochemical analysis of protein-RNA interface. Nucleic Acids Res. 2012;40:W440–4.
   PubMed Web of Science ®Google Scholar
• Mizushima S, Nomura M. Assembly mapping of 30S ribosomal proteins from E. coli. Nature. 1970;226:1214.
   PubMed Web of Science ®Google Scholar
• Xu Z, Culver GM. Differential assembly of 16S rRNA domains during 30S subunit formation. RNA. 2010;16:1990–2001.
   PubMed Web of Science ®Google Scholar
• Talkington MW, Siuzdak G, Williamson JR. An assembly landscape for the 30S ribosomal subunit. Nature. 2005;438:628–632.
   PubMed Web of Science ®Google Scholar
• Ramaswamy P, Woodson SA. S16 throws a conformational switch during assembly of 30S 5ʹ domain. Nat Struct Mol Biol. 2009;16:438–445.
   PubMed Web of Science ®Google Scholar
• Kruiswijk T, Planta RJ, Krop JM. The course of the assembly of ribosomal subunits in yeast. Biochim Biophys Acta. 1978;517:378–389.
   PubMedGoogle Scholar
• Gamalinda M, Ohmayer U, Jakovljevic J, et al. A hierarchical model for assembly of eukaryotic 60S ribosomal subunit domains. Genes Dev. 2014;28:198–210.
   PubMed Web of Science ®Google Scholar
• Pedregosa F, Varoquaux G, Gramfort A, et al. Scikit-learn: machine learning in python. J Mach Learn Res. 2011;12:2825–2830.
   Web of Science ®Google Scholar