Table of Contents Author Guidelines Submit a Manuscript
Journal of Nucleic Acids
Volume 2018, Article ID 9581021, 14 pages
https://doi.org/10.1155/2018/9581021
Research Article

A Sequence-Dependent DNA Condensation Induced by Prion Protein

1Infectiologie Animale et Santé Publique, Institut National de la Recherche Agronomique, 37380 Nouzilly, France
2Department of Electronic Engineering and Organic Electronics Research Center, Ming-Chi University of Technology, 84 Gungjuan Rd., Taishan Dist., New Taipei City 24301, Taiwan

Correspondence should be addressed to Alakesh Bera; ude.shusu@rtc.areb.hsekala and Sajal Biring; wt.ude.tucm.liam@gnirib

Received 18 October 2017; Revised 18 December 2017; Accepted 17 January 2018; Published 20 February 2018

Academic Editor: Ben Berkhout

Copyright © 2018 Alakesh Bera and Sajal Biring. 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. A. L. Horwich and J. S. Weissman, “Deadly conformations - Protein misfolding in prion disease,” Cell, vol. 89, no. 4, pp. 499–510, 1997. View at Publisher · View at Google Scholar · View at Scopus
  2. S. B. Prusiner, “Prions,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 95, no. 23, pp. 13363–13383, 1998. View at Publisher · View at Google Scholar · View at Scopus
  3. B. Caughey, “Interactions between prion protein isoforms: The kiss of death?” Trends in Biochemical Sciences, vol. 26, no. 4, pp. 235–242, 2001. View at Publisher · View at Google Scholar · View at Scopus
  4. D. R. Brown, B. Schmidt, and H. A. Kretzschmar, “Effects of copper on survival of prion protein knockout neurons and glia,” Journal of Neurochemistry, vol. 70, no. 4, pp. 1686–1693, 1998. View at Publisher · View at Google Scholar · View at Scopus
  5. L. Westergard, H. M. Christensen, and D. A. Harris, “The cellular prion protein (PrPC): its physiological function and role in disease,” Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease, vol. 1772, no. 6, pp. 629–644, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. R. Linden, V. R. Martins, M. A. M. Prado, M. Cammarota, I. Izquierdo, and R. R. Brentani, “Physiology of the prion protein,” Physiological Reviews, vol. 88, no. 2, pp. 673–728, 2008. View at Publisher · View at Google Scholar · View at Scopus
  7. R. Linden, Y. Cordeiro, and L. M. T. R. Lima, “Allosteric function and dysfunction of the prion protein,” Cellular and Molecular Life Sciences, vol. 69, no. 7, pp. 1105–1124, 2012. View at Publisher · View at Google Scholar · View at Scopus
  8. A. Aguzzi and C. Weissmann, “Prion research: The next frontiers,” Nature, vol. 389, no. 6653, pp. 795–798, 1997. View at Publisher · View at Google Scholar · View at Scopus
  9. R. G. Rohwer, “The scrapie agent: 'A virus by any other name',” Current Topics in Microbiology and Immunology, vol. 172, pp. 195–232, 1991. View at Google Scholar · View at Scopus
  10. L. Manuelidis, T. Sklaviadis, A. Akowitz, and W. Fritch, “Viral particles are required for infection in neurodegenerative Creutzfeldt-Jakob disease,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 92, no. 11, pp. 5124–5128, 1995. View at Publisher · View at Google Scholar · View at Scopus
  11. N. R. Deleault, R. W. Lucassen, and S. Supattapone, “RNA molecules stimulate prion protein conversion,” Nature, vol. 425, no. 6959, pp. 717–720, 2003. View at Publisher · View at Google Scholar · View at Scopus
  12. K.-W. Leffers, H. Wille, J. Stöhr, E. Junger, S. B. Prusiner, and D. Riesner, “Assembly of natural and recombinant prion protein into fibrils,” biological chemistry, vol. 386, no. 6, pp. 569–580, 2005. View at Publisher · View at Google Scholar · View at Scopus
  13. G. Legname, I. V. Baskakov, H.-O. B. Nguyen et al., “Synthetic mammalian prions,” Science, vol. 305, no. 5684, pp. 673–676, 2004. View at Publisher · View at Google Scholar · View at Scopus
  14. G. Legname, H.-O. B. Nguyen, I. V. Baskakov, F. E. Cohen, S. J. DeArmond, and S. B. Prusiner, “Strain-specified characteristics of mouse synthetic prions,” Proceedings of the National Acadamy of Sciences of the United States of America, vol. 102, no. 6, pp. 2168–2173, 2005. View at Publisher · View at Google Scholar · View at Scopus
  15. J. Castilla, P. Saá, C. Hetz, and C. Soto, “In vitro generation of infectious scrapie prions,” Cell, vol. 121, no. 2, pp. 195–206, 2005. View at Publisher · View at Google Scholar · View at Scopus
  16. J. R. Silveira, G. J. Raymond, A. G. Hughson et al., “The most infectious prion protein particles,” Nature, vol. 437, no. 7056, pp. 257–261, 2005. View at Publisher · View at Google Scholar · View at Scopus
  17. M. Enserink, “Spongiform diseases. Waiting for the final experiment.,” Science, vol. 310, no. 5755, p. 1758, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. N. Nishida, S. Katamine, and L. Manuelidis, “Medicine: Reciprocal interference between specific CJD and scrapie agents in neural cell cultures,” Science, vol. 310, no. 5747, pp. 493–496, 2005. View at Publisher · View at Google Scholar · View at Scopus
  19. J. G. Safar, K. Kellings, A. Serban et al., “Search for a prion-specific nucleic acid,” Journal of Virology, vol. 79, no. 16, pp. 10796–10806, 2005. View at Publisher · View at Google Scholar · View at Scopus
  20. A. Bera and P. K. Nandi, “Biological polyamines inhibit nucleic-acid-induced polymerisation of prion protein,” Archives of Virology, vol. 152, no. 4, pp. 655–668, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. A. Bera, A.-C. Roche, and P. K. Nandi, “Bending and unwinding of nucleic acid by prion protein,” Biochemistry, vol. 46, no. 5, pp. 1320–1328, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. A. Bera and P. K. Nandi, “Nucleic acid induced unfolding of recombinant prion protein globular fragment is pH dependent,” Protein Science, vol. 23, no. 12, pp. 1780–1788, 2014. View at Publisher · View at Google Scholar · View at Scopus
  23. P. K. Nandi and E. Leclerc, “Polymerization of murine recombinant prion protein in nucleic acid solution,” Archives of Virology, vol. 144, no. 9, pp. 1751–1763, 1999. View at Publisher · View at Google Scholar · View at Scopus
  24. Y. Cordeiro, F. Machado, L. Juliano et al., “DNA Converts Cellular Prion Protein into the β-Sheet Conformation and Inhibits Prion Peptide Aggregation,” The Journal of Biological Chemistry, vol. 276, no. 52, pp. 49400–49409, 2001. View at Publisher · View at Google Scholar · View at Scopus
  25. V. Adler, B. Zeiler, V. Kryukov, R. Kascsak, R. Rubenstein, and A. Grossman, “Small, highly structured RNAs participate in the conversion of human recombinant PrPSen to PrPRes in vitro,” Journal of Molecular Biology, vol. 332, no. 1, pp. 47–57, 2003. View at Publisher · View at Google Scholar · View at Scopus
  26. M. L. Vernon, L. Horta-Barbosa, D. A. Fuccillo, J. L. Sever, J. R. Baringer, and G. Birnbaum, “Virus-like particles and nucleoprotein-type filaments in brain tissue from two patients with Creutzfeldt-Jakob disease.,” The Lancet, vol. 1, no. 7654, pp. 964–966, 1970. View at Google Scholar · View at Scopus
  27. P. K. Nandi and J.-C. Nicole, “Nucleic acid and prion protein interaction produces spherical amyloids which can function in vivo as coats of spongiform encephalopathy agent,” Journal of Molecular Biology, vol. 344, no. 3, pp. 827–837, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. M. P. McKinley, A. Taraboulos, L. Kenaga et al., “Ultrastructural localization of scrapie prion proteins in cytoplasmic vesicles of infected cultured cells,” Laboratory Investigation, vol. 65, no. 6, pp. 622–630, 1991. View at Google Scholar · View at Scopus
  29. L. Fioriti, S. Dossena, L. R. Stewart et al., “Cytosolic prion protein (PrP) is not toxic in N2a cells and primary neurons expressing pathogenic PrP mutations,” The Journal of Biological Chemistry, vol. 280, no. 12, pp. 11320–11328, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. K. S. Lee, A. C. Magalhães, S. M. Zanata, R. R. Brentani, V. R. Martins, and M. A. M. Prado, “Internalization of mammalian fluorescent cellular prion protein and N-terminal deletion mutants in living cells,” Journal of Neurochemistry, vol. 79, no. 1, pp. 79–87, 2001. View at Publisher · View at Google Scholar · View at Scopus
  31. J. Ma, R. Wollmann, and S. Lindquist, “Neurotoxicity and neurodegeneration when PrP accumulates in the cytosol,” Science, vol. 298, no. 5599, pp. 1781–1785, 2002. View at Publisher · View at Google Scholar · View at Scopus
  32. Y. Cordeiro and J. L. Silva, “The hypothesis of the catalytic action of nucleic acid on the conversion of prion protein,” Protein and Peptide Letters, vol. 12, no. 3, pp. 251–255, 2005. View at Publisher · View at Google Scholar · View at Scopus
  33. D. K. Chattoraj, L. C. Gosule, and J. A. Schellman, “DNA condensation with polyamines. II. Electron microscopic studies,” Journal of Molecular Biology, vol. 121, no. 3, pp. 327–337, 1978. View at Publisher · View at Google Scholar · View at Scopus
  34. J. C. Sitko, E. M. Mateescu, and H. G. Hansma, “Sequence-dependent DNA condensation and the electrostatic zipper,” Biophysical Journal, vol. 84, no. 1, pp. 419–431, 2003. View at Publisher · View at Google Scholar · View at Scopus
  35. J. Dekker, “GC- and AT-rich chromatin domains differ in conformation and histone modification status and are differentially modulated by Rpd3p,” Genome Biology, vol. 8, no. 6, article no. R116, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. B. Macedo, T. A. Millen, C. A. C. A. Braga et al., “Nonspecific prion protein-nucleic acid interactions lead to different aggregates and cytotoxic species,” Biochemistry, vol. 51, no. 27, pp. 5402–5413, 2012. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Bera, E. M. Perkins, J. Zhu, H. Zhu, and P. Desai, “DNA binding and condensation properties of the herpes simplex virus type 1 triplex protein VP19C,” PLoS ONE, vol. 9, no. 8, Article ID e104640, 2014. View at Publisher · View at Google Scholar · View at Scopus
  38. B. Berkhout, N. L. Vastenhouw, B. I. F. Klasens, and H. Huthoff, “Structural features in the HIV-1 repeat region facilitate strand transfer during reverse transcription,” RNA, vol. 7, no. 8, pp. 1097–1114, 2001. View at Publisher · View at Google Scholar · View at Scopus
  39. E. Tuite, S. K. Kim, B. Norden, and M. Takahashi, “Effects of intercalators on complexation of RecA with duplex DNA,” Biochemistry, vol. 34, no. 50, pp. 16365–16374, 1995. View at Publisher · View at Google Scholar · View at Scopus
  40. G. Krishnamoorthy, G. Duportail, and Y. Mély, “Structure and dynamics of condensed DNA probed by 1,1-(4,4,8,8-tetramethyl-4,8-diazaundecamethylene)bis[4-[[3-methylbenz-1,3-oxazol-2-y1]methylidine]-1,4-dihydroquinolinium] tetraiodide fluorescence,” Biochemistry, vol. 41, no. 51, pp. 15277–15287, 2002. View at Publisher · View at Google Scholar · View at Scopus
  41. G. Krishnamoorthy, B. Roques, J.-L. Darlix, and Y. Mély, “DNA condensation by the nucleocapsid protein of HIV-1: A mechnism ensuring DNA protection,” Nucleic Acids Research, vol. 31, no. 18, pp. 5425–5432, 2003. View at Publisher · View at Google Scholar · View at Scopus
  42. V. A. Bloomfield, “Condensation of DNA by multivalent cations: Considerations on mechanism,” Biopolymers, vol. 31, no. 13, pp. 1471–1481, 1991. View at Publisher · View at Google Scholar · View at Scopus
  43. H. Rezaei, D. Marc, Y. Choiset et al., “High yield purification and physico-chemical properties of full-length recombinant allelic variants of sheep prion protein linked to scrapie susceptibility,” European Journal of Biochemistry, vol. 267, no. 10, pp. 2833–2839, 2000. View at Publisher · View at Google Scholar · View at Scopus
  44. M. A. Wells, G. S. Jackson, S. Jones et al., “A reassessment of copper(II) binding in the full-length prion protein,” Biochemical Journal, vol. 399, no. 3, pp. 435–444, 2006. View at Publisher · View at Google Scholar · View at Scopus
  45. S. Liemann and R. Glockshuber, “Influence of amino acid substitutions related to inherited human prion diseases on the thermodynamic stability of the cellular prion protein,” Biochemistry, vol. 38, no. 11, pp. 3258–3267, 1999. View at Publisher · View at Google Scholar · View at Scopus
  46. D. Sagi, N. Friedman, C. Vorgias, A. B. Oppenheim, and J. Stavans, “Modulation of DNA conformations through the formation of alternative high-order HU-DNA complexes,” Journal of Molecular Biology, vol. 341, no. 2, pp. 419–428, 2004. View at Publisher · View at Google Scholar · View at Scopus
  47. P. K. Nandi and P.-Y. Sizaret, “Murine recombinant prion protein induces ordered aggregation of linear nucleic acids to condensed globular structures,” Archives of Virology, vol. 146, no. 2, pp. 327–345, 2001. View at Publisher · View at Google Scholar · View at Scopus
  48. J. Widom and R. L. Baldwin, “Cation-induced toroidal condensation of DNA. Studies with Co3+(NH3)6,” Journal of Molecular Biology, vol. 144, no. 4, pp. 431–453, 1980. View at Publisher · View at Google Scholar · View at Scopus
  49. K. H. Abramo, J. B. Pitner, and L. B. McGown, “Spectroscopic studies of single-stranded DNA ligands and oxazole yellow dyes,” Biospectroscopy, vol. 4, no. 1, pp. 27–35, 1998. View at Publisher · View at Google Scholar · View at Scopus
  50. M. H. Kombrabail and G. Krishnamoorthy, “Fluorescence dynamics of DNA condensed by the molecular crowding agent poly(ethylene glycol),” Journal of Fluorescence, vol. 15, no. 5, pp. 741–747, 2005. View at Publisher · View at Google Scholar · View at Scopus
  51. T. Kral, M. Hof, and M. Langner, “The effect of spermine on plasmid condensation and dye release observed by fluorescence correlation spectroscopy,” biological chemistry, vol. 383, no. 2, pp. 331–335, 2002. View at Publisher · View at Google Scholar · View at Scopus
  52. C. Gabus, E. Derrington, P. Leblanc et al., “The Prion Protein Has RNA Binding and Chaperoning Properties Characteristic of Nucleocapsid Protein NCp7 of HIV-1,” The Journal of Biological Chemistry, vol. 276, no. 22, pp. 19301–19309, 2001. View at Publisher · View at Google Scholar · View at Scopus
  53. A. Küffer, A. K. K. Lakkaraju, A. Mogha et al., “The prion protein is an agonistic ligand of the G protein-coupled receptor Adgrg6,” Nature, vol. 536, no. 7617, pp. 464–468, 2016. View at Publisher · View at Google Scholar · View at Scopus
  54. C. Ma, L. Sun, and V. A. Bloomfield, “Condensation of plasmids enhanced by Z-DNA conformation of d(CG)n inserts,” Biochemistry, vol. 34, pp. 3521–3528, 1995. View at Google Scholar
  55. T. J. Thomas, U. B. Gunnia, and T. Thomas, “Polyamine-induced B-DNA to Z-DNA conformational transition of a plasmid DNA with (dG-dC)n insert,” The Journal of Biological Chemistry, vol. 266, no. 10, pp. 6137–6141, 1991. View at Google Scholar · View at Scopus
  56. R. Hasan, M. K. Alam, and R. Ali, “Polyamine induced Z-conformation of native calf thymus DNA,” FEBS Letters, vol. 368, no. 1, pp. 27–30, 1995. View at Publisher · View at Google Scholar · View at Scopus
  57. J. Ruiz-Chica, M. A. Medina, F. Sánchez-Jiménez, and F. J. Ramírez, “Raman study of the interaction between polyamines and a GC oligonucleotide,” Biochemical and Biophysical Research Communications, vol. 285, no. 2, pp. 437–446, 2001. View at Publisher · View at Google Scholar · View at Scopus
  58. S. Harteis and S. Schneider, “Making the bend: DNA tertiary structure and protein-DNA interactions,” International Journal of Molecular Sciences, vol. 15, no. 7, pp. 12335–12363, 2014. View at Publisher · View at Google Scholar · View at Scopus
  59. F. Bailly, C. Bailly, P. Colson, C. Houssier, and J.-P. Hénichart, “A tandem repeat of the SPKK peptide motif induces Ψ-type DNA structures at alternating AT sequences,” FEBS Letters, vol. 324, no. 2, pp. 181–184, 1993. View at Publisher · View at Google Scholar · View at Scopus
  60. C. Gabus, S. Auxilien, C. Péchoux et al., “The prion protein has DNA strand transfer properties similar to retroviral nucleocapsid protein,” Journal of Molecular Biology, vol. 307, no. 4, pp. 1011–1021, 2001. View at Publisher · View at Google Scholar · View at Scopus
  61. P. K. Nandi, E. Leclerc, and D. Marc, “Unusual property of prion protein unfolding in neutral salt solution,” Biochemistry, vol. 41, no. 36, pp. 11017–11024, 2002. View at Publisher · View at Google Scholar · View at Scopus
  62. P. K. Nandi, A. Bera, and P.-Y. Sizaret, “Osmolyte Trimethylamine N-Oxide Converts Recombinant α-Helical Prion Protein to its Soluble β-Structured Form at High Temperature,” Journal of Molecular Biology, vol. 362, no. 4, pp. 810–820, 2006. View at Publisher · View at Google Scholar · View at Scopus
  63. J. L. Silva, L. M. T. R. Lima, D. Foguel, and Y. Cordeiro, “Intriguing nucleic-acid-binding features of mammalian prion protein,” Trends in Biochemical Sciences, vol. 33, no. 3, pp. 132–140, 2008. View at Publisher · View at Google Scholar · View at Scopus
  64. J. L. Silva and Y. Cordeiro, “The "Jekyll and Hyde" actions of nucleic acids on the prion-like aggregation of proteins,” The Journal of Biological Chemistry, vol. 291, no. 30, pp. 15482–15490, 2016. View at Publisher · View at Google Scholar · View at Scopus
  65. J. Yoo, H. Kim, A. Aksimentiev, and T. Ha, “Direct evidence for sequence-dependent attraction between double-stranded DNA controlled by methylation,” Nature Communications, vol. 7, Article ID 11045, 2016. View at Publisher · View at Google Scholar · View at Scopus
  66. N. S. Hachiya, K. Watanabe, Y. Sakasegawa, and K. Kaneko, “Microtubules-associated intracellular localization of the NH 2-terminal cellular prion protein fragment,” Biochemical and Biophysical Research Communications, vol. 313, no. 3, pp. 818–823, 2004. View at Publisher · View at Google Scholar · View at Scopus
  67. K. Qin, L. Zhao, Y. Tang, S. Bhatta, J. M. Simard, and R. Y. Zhao, “Doppel-induced apoptosis and counteraction by cellular prion protein in neuroblastoma and astrocytes,” Neuroscience, vol. 141, no. 3, pp. 1375–1388, 2006. View at Publisher · View at Google Scholar · View at Scopus
  68. E. H. Blackburn, “Telomere states and cell fates,” Nature, vol. 408, no. 6808, pp. 53–56, 2000. View at Publisher · View at Google Scholar · View at Scopus
  69. A. E. Vinogradov, “DNA helix: The importance of being GC-rich,” Nucleic Acids Research, vol. 31, no. 7, pp. 1838–1844, 2003. View at Publisher · View at Google Scholar · View at Scopus
  70. K. Pfeifer, M. Bachmann, H. C. Schröder, J. Forrest, and W. E. G. Müller, “Kinetics of expression of prion protein in uninfected and scrapie‐infected N2a mouse neuroblastoma cells,” Cell Biochemistry & Function, vol. 11, no. 1, pp. 1–11, 1993. View at Publisher · View at Google Scholar · View at Scopus
  71. A. Mangé, C. Crozet, L. Sylvain, and F. Béranger, “Scrapie-like prion protein is translocated to the nuclei of infected cells independently of proteasome inhibition and interacts with chromatin,” Journal of Cell Science, vol. 117, no. 11, pp. 2411–2416, 2004. View at Publisher · View at Google Scholar · View at Scopus
  72. S. M. Fullerton, A. B. Carvalho, and A. G. Clark, “Local rates of recombination are positively correlated with GC content in the human genome,” Molecular Biology and Evolution, vol. 18, no. 6, pp. 1139–1142, 2001. View at Publisher · View at Google Scholar · View at Scopus