Table of Contents Author Guidelines Submit a Manuscript
Journal of Nucleic Acids
Volume 2017, Article ID 6067345, 8 pages
https://doi.org/10.1155/2017/6067345
Research Article

The 2D Structure of the T. brucei Preedited RPS12 mRNA Is Not Affected by Macromolecular Crowding

Department of Molecular Genetics, Darmstadt University of Technology, Darmstadt, Germany

Correspondence should be addressed to H. Ulrich Göringer; ed.tdatsmrad-ut.oib@regnirog

Received 3 February 2017; Accepted 4 April 2017; Published 18 June 2017

Academic Editor: Luis A. Marky

Copyright © 2017 W.-Matthias Leeder et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. A. Doudna and T. R. Cech, “The chemical repertoire of natural ribozymes,” Nature, vol. 418, no. 6894, pp. 222–228, 2002. View at Publisher · View at Google Scholar · View at Scopus
  2. D. E. Draper, D. Grilley, and A. M. Soto, “Ions and RNA folding,” Annual Review of Biophysics and Biomolecular Structure, vol. 34, pp. 221–243, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. A. M. Soto, V. Misra, and D. E. Draper, “Tertiary structure of an RNA pseudoknot is stabilized by ‘diffuse’ Mg2+ ions,” Biochemistry, vol. 46, no. 11, pp. 2973–2983, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. D. Leipply and D. E. Draper, “Dependence of RNA tertiary structural stability on Mg2+ concentration: interpretation of the hill equation and coefficient,” Biochemistry, vol. 49, no. 9, pp. 1843–1853, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. J. Tyrrell, J. L. McGinnis, K. M. Weeks, and G. J. Pielak, “The cellular environment stabilizes adenine riboswitch RNA structure,” Biochemistry, vol. 52, no. 48, pp. 8777–8785, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. G. S. Manning, “The molecular theory of polyelectrolyte solutions with applications to the electrostatic properties of polynucleotides,” Quarterly Reviews of Biophysics, vol. 11, no. 2, pp. 179–246, 1978. View at Publisher · View at Google Scholar · View at Scopus
  7. V. K. Misra and D. E. Draper, “Mg2+ binding to tRNA revisited: the nonlinear Poisson-Boltzmann model,” Journal of Molecular Biology, vol. 299, no. 3, pp. 813–825, 2000. View at Publisher · View at Google Scholar · View at Scopus
  8. D. Lambert, D. Leipply, R. Shiman, and D. E. Draper, “The influence of monovalent cation size on the stability of RNA tertiary structures,” Journal of Molecular Biology, vol. 390, no. 4, pp. 791–804, 2009. View at Publisher · View at Google Scholar · View at Scopus
  9. S. Miyamoto, K. Kashiwagi, K. Ito, S. Watanabe, and K. Igarashi, “Estimation of polyamine distribution and polyamine stimulation of protein synthesis in Escherichia coli,” Archives of Biochemistry and Biophysics, vol. 300, no. 1, pp. 63–68, 1993. View at Publisher · View at Google Scholar · View at Scopus
  10. D. Lambert and D. E. Draper, “Effects of Osmolytes on RNA secondary and tertiary structure stabilities and RNA-Mg2+ interactions,” Journal of Molecular Biology, vol. 370, no. 5, pp. 993–1005, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. B. D. Bennett, E. H. Kimball, M. Gao, R. Osterhout, S. J. Van Dien, and J. D. Rabinowitz, “Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli,” Nature Chemical Biology, vol. 5, no. 8, pp. 593–599, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. D. Lambert, D. Leipply, and D. E. Draper, “The Osmolyte TMAO stabilizes native RNA tertiary structures in the absence of Mg2+: evidence for a large barrier to folding from phosphate dehydration,” Journal of Molecular Biology, vol. 404, no. 1, pp. 138–157, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. R. J. Trachman and D. E. Draper, “Comparison of interactions of diamine and Mg2+ with RNA tertiary structures: similar versus differential effects on the stabilities of diverse RNA folds,” Biochemistry, vol. 52, no. 34, pp. 5911–5919, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. S. B. Zimmerman and S. O. Trach, “Estimation of macromolecule concentrations and excluded volume effects for the cytoplasm of Escherichia coli,” Journal of Molecular Biology, vol. 222, no. 3, pp. 599–620, 1991. View at Publisher · View at Google Scholar · View at Scopus
  15. R. J. Ellis, “Macromolecular crowding: obvious but underappreciated,” Trends in Biochemical Sciences, vol. 26, no. 10, pp. 597–604, 2001. View at Publisher · View at Google Scholar · View at Scopus
  16. D. Thirumalai, D. K. Klimov, and G. H. Lorimer, “Caging helps proteins fold,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 20, pp. 11195–11197, 2003. View at Publisher · View at Google Scholar · View at Scopus
  17. D. Kilburn, J. H. Roh, L. Guo, R. M. Briber, and S. A. Woodson, “Molecular crowding stabilizes folded RNA structure by the excluded volume effect,” Journal of the American Chemical Society, vol. 132, no. 25, pp. 8690–8696, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. D. Kilburn, J. H. Roh, R. Behrouzi, R. M. Briber, and S. A. Woodson, “Crowders perturb the entropy of RNA energy landscapes to favor folding,” Journal of the American Chemical Society, vol. 135, no. 27, pp. 10055–10063, 2013. View at Publisher · View at Google Scholar · View at Scopus
  19. H. U. Göringer, “‘Gestalt’, composition and function of the Trypanosoma brucei editosome,” Annual Review of Microbiology, vol. 66, pp. 65–82, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. P. A. Srere, “The infrastructure of the mitochondrial matrix,” Trends in Biochemical Sciences, vol. 5, no. 5, pp. 120-121, 1980. View at Publisher · View at Google Scholar · View at Scopus
  21. K. S. Harve, R. Lareu, R. Rajagopalan, and M. Raghunath, “Understanding how the crowded interior of cells stabilizes DNA/DNA and DNA/RNA hybrids-in silico predictions and in vitro evidence,” Nucleic Acids Research, vol. 38, no. 1, pp. 172–181, 2009. View at Publisher · View at Google Scholar · View at Scopus
  22. W.-M. Leeder, C. Voigt, M. Brecht, and H. U. Göringer, “The RNA chaperone activity of the Trypanosoma brucei editosome raises the dynamic of bound pre-mRNAs,” Scientific Reports, vol. 6, Article ID 19309, 2016. View at Publisher · View at Google Scholar · View at Scopus
  23. W.-M. Leeder, N. F. C. Hummel, and H. U. Göringer, “Multiple G-quartet structures in pre-edited mRNAs suggest evolutionary driving force for RNA editing in trypanosomes,” Scientific Reports, vol. 6, Article ID 29810, 2016. View at Publisher · View at Google Scholar · View at Scopus
  24. V. S. Katari, L. Van Esdonk, and H. U. Göringer, “Molecular crowding inhibits U-insertion/deletion RNA editing in vitro: consequences for the in vivo reaction,” PLoS ONE, vol. 8, no. 12, Article ID e83796, 2013. View at Publisher · View at Google Scholar · View at Scopus
  25. G. A. Cross, “Identification, purification and properties of clone-specific glycoprotein antigens constituting the surface coat of Trypanosoma brucei,” Parasitology, vol. 71, no. 3, pp. 393–417, 1975. View at Publisher · View at Google Scholar · View at Scopus
  26. R. Turner, K. Shefer, and M. Ares Jr., “Safer one-pot synthesis of the ‘SHAPE’ reagent 1-methyl-7-nitroisatoic anhydride (1m7),” RNA, vol. 19, no. 12, pp. 1857–1863, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. S. M. Vasa, N. Guex, K. A. Wilkinson, K. M. Weeks, and M. C. Giddings, “ShapeFinder: a software system for high-throughput quantitative analysis of nucleic acid reactivity information resolved by capillary electrophoresis,” RNA, vol. 14, no. 10, pp. 1979–1990, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. C. E. Hajdin, S. Bellaousov, W. Huggins, C. W. Leonard, D. H. Mathews, and K. M. Weeks, “Accurate SHAPE-directed RNA secondary structure modeling, including pseudoknots,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 14, pp. 5498–5503, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. J. S. Reuter and D. H. Mathews, “RNAstructure: software for RNA secondary structure prediction and analysis,” BMC Bioinformatics, vol. 11, article no. 129, 2010. View at Publisher · View at Google Scholar · View at Scopus
  30. R. C. Spitale, P. Crisalli, R. A. Flynn, E. A. Torre, E. T. Kool, and H. Y. Chang, “RNA SHAPE analysis in living cells,” Nature Chemical Biology, vol. 9, no. 1, pp. 18–20, 2013. View at Publisher · View at Google Scholar · View at Scopus
  31. Y. Ding, Y. Tang, C. K. Kwok, Y. Zhang, P. C. Bevilacqua, and S. M. Assmann, “In vivo genome-wide profiling of RNA secondary structure reveals novel regulatory features,” Nature, vol. 505, no. 7485, pp. 696–700, 2014. View at Publisher · View at Google Scholar · View at Scopus
  32. S. Rouskin, M. Zubradt, S. Washietl, M. Kellis, and J. S. Weissman, “Genome-wide probing of RNA structure reveals active unfolding of mRNA structures in vivo,” Nature, vol. 505, no. 7485, pp. 701–705, 2014. View at Publisher · View at Google Scholar · View at Scopus
  33. J. L. McGinnis, Q. Liu, C. A. Lavender et al., “In-cell SHAPE reveals that free 30S ribosome subunits,” Proceedings of the National Academy of Sciences of the United States of America, vol. 112, no. 8, pp. 2425–2430, 2015. View at Publisher · View at Google Scholar · View at Scopus
  34. A. P. Minton, “The influence of macromolecular crowding and macromolecular confinement on biochemical reactions in physiological media,” The Journal of Biological Chemistry, vol. 276, no. 14, pp. 10577–10580, 2001. View at Publisher · View at Google Scholar · View at Scopus
  35. N. A. Chebotareva, B. I. Kurganov, and N. B. Livanova, “Biochemical effects of molecular crowding,” Biochemistry (Moscow), vol. 69, no. 11, pp. 1239–1251, 2004. View at Publisher · View at Google Scholar · View at Scopus
  36. P.-G. de Gennes, Scaling Concepts in Polymer Physics, Cornell University Press, Ithaca, NY, USA, 1979. View at Publisher · View at Google Scholar
  37. N. Kozer and G. Schreiber, “Effect of crowding on protein-protein association rates: fundamental differences between low and high mass crowding agents,” Journal of Molecular Biology, vol. 336, no. 3, pp. 763–774, 2004. View at Publisher · View at Google Scholar · View at Scopus
  38. N. Kozer, Y. Y. Kuttner, G. Haran, and G. Schreiber, “Protein-protein association in polymer solutions: from dilute to semidilute to concentrated,” Biophysical Journal, vol. 92, no. 6, pp. 2139–2149, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. E. J. Merino, K. A. Wilkinson, J. L. Coughlan, and K. M. Weeks, “RNA structure analysis at single nucleotide resolution by Selective 2′-Hydroxyl Acylation and Primer Extension (SHAPE),” Journal of the American Chemical Society, vol. 127, no. 12, pp. 4223–4231, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. J. Tyrrell, K. M. Weeks, and G. J. Pielak, “Challenge of mimicking the influences of the cellular environment on RNA structure by PEG-induced macromolecular crowding,” Biochemistry, vol. 54, no. 42, pp. 6447–6453, 2015. View at Publisher · View at Google Scholar · View at Scopus
  41. S. L. Heilman-Miller, J. Pan, D. Thirumalai, and S. A. Woodson, “Role of counterion condensation in folding of the Tetrahymena ribozyme II. Counterion-dependence of folding kinetics,” Journal of Molecular Biology, vol. 309, no. 1, pp. 57–68, 2001. View at Publisher · View at Google Scholar · View at Scopus
  42. S. L. Heilman-Miller, D. Thirumalai, and S. A. Woodson, “Role of counterion condensation in folding of the Tetrahymena ribozyme. I. Equilibrium stabilization by cations,” Journal of Molecular Biology, vol. 306, no. 5, pp. 1157–1166, 2001. View at Publisher · View at Google Scholar · View at Scopus
  43. D. Thirumalai, N. Lee, S. A. Woodson, and D. K. Klimov, “Early events in RNA folding,” Annual Review of Physical Chemistry, vol. 52, pp. 751–762, 2001. View at Publisher · View at Google Scholar · View at Scopus
  44. D. Grilley, A. M. Soto, and D. E. Draper, “Mg2+-RNA interaction free energies and their relationship to the folding of RNA tertiary structures,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 38, pp. 14003–14008, 2006. View at Publisher · View at Google Scholar · View at Scopus
  45. D. Leipply and D. E. Draper, “Evidence for a thermodynamically distinct Mg2+ ion associated with formation of an RNA tertiary structure,” Journal of the American Chemical Society, vol. 133, no. 34, pp. 13397–13405, 2011. View at Publisher · View at Google Scholar · View at Scopus
  46. S.-I. Nakano, H. T. Karimata, Y. Kitagawa, and N. Sugimoto, “Facilitation of RNA enzyme activity in the molecular crowding media of cosolutes,” Journal of the American Chemical Society, vol. 131, no. 46, pp. 16881–16888, 2009. View at Publisher · View at Google Scholar · View at Scopus
  47. C. A. Strulson, J. A. Boyer, E. E. Whitman, and P. C. Bevilacqua, “Molecular crowders and cosolutes promote folding cooperativity of RNA under physiological ionic conditions,” RNA, vol. 20, no. 3, pp. 331–347, 2014. View at Publisher · View at Google Scholar · View at Scopus
  48. H. Zhou, G. Rivas, and A. P. Minton, “Macromolecular crowding and confinement: biochemical, biophysical, and potential physiological consequences,” Annual Review of Biophysics, vol. 37, pp. 375–397, 2008. View at Publisher · View at Google Scholar · View at Scopus