Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2014, Article ID 926394, 10 pages
http://dx.doi.org/10.1155/2014/926394
Research Article

Glatiramer Acetate and Nanny Proteins Restrict Access of the Multiple Sclerosis Autoantigen Myelin Basic Protein to the 26S Proteasome

1Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, V-437, Moscow 117871, Russia
2Chemistry Department, Lomonosov Moscow State University, Moscow 119991, Russia
3Kazan Federal University, Kazan, Republic of Tatarstan 420008, Russia
4Nanotechnology Research and Education Centre RAS, St. Petersburg Academic University, St. Petersburg 194021, Russia
5Institute of Gene Biology, Russian Academy of Sciences, Moscow 117334, Russia

Received 9 May 2014; Revised 13 August 2014; Accepted 16 August 2014; Published 8 September 2014

Academic Editor: W. David Arnold

Copyright © 2014 Ekaterina Kuzina 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. R. P. Lisak and B. Zweiman, “In vitro cell-mediated immunity of cerebrospinal-fluid lymphocytes to myelin basic protein in primary demyelinating diseases,” New England Journal of Medicine, vol. 297, no. 16, pp. 850–853, 1977. View at Publisher · View at Google Scholar · View at Scopus
  2. P. R. Carnegie, B. Bencina, and G. Lamoureux, “Experimental allergic encephalomyelitis. Isolation of basic proteins and polypeptides from central nervous tissue,” Biochemical Journal, vol. 105, no. 2, pp. 559–568, 1967. View at Google Scholar · View at Scopus
  3. K. Ota, M. Matsui, E. L. Milford, G. A. Mackin, H. L. Weiner, and D. A. Hafler, “T-cell recognition of an immunodominant myelin basic protein epitope in multiple sclerosis,” Nature, vol. 346, no. 6280, pp. 183–187, 1990. View at Publisher · View at Google Scholar · View at Scopus
  4. R. Martin, M. D. Howell, D. Jaraquemada et al., “A myelin basic protein peptide is recognized by cytotoxic T cells in the context of four HLA-DR types associated with multiple sclerosis,” The Journal of Experimental Medicine, vol. 173, no. 1, pp. 19–24, 1991. View at Google Scholar
  5. A. Jurewicz, W. E. Biddison, and J. P. Antel, “MHC class I-restricted lysis of human oligodendrocytes by myelin basic protein peptide-specific CD8 T lymphocytes,” Journal of Immunology, vol. 160, no. 6, pp. 3056–3059, 1998. View at Google Scholar · View at Scopus
  6. E. S. Huseby, D. Liggitt, T. Brabb, B. Schnabel, C. Öhlén, and J. Goverman, “A pathogenic role for myelin-specific CD8+ T cells in a model for multiple sclerosis,” The Journal of Experimental Medicine, vol. 194, no. 5, pp. 669–676, 2001. View at Publisher · View at Google Scholar · View at Scopus
  7. K. L. Rock, C. Gramm, L. Rothstein et al., “Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules,” Cell, vol. 78, no. 5, pp. 761–771, 1994. View at Publisher · View at Google Scholar · View at Scopus
  8. A. Hershko, H. Heller, S. Elias, and A. Ciechanover, “Components of ubiquitin-protein ligase system. Resolution, affinity purification, and role in protein breakdown,” The Journal of Biological Chemistry, vol. 258, no. 13, pp. 8206–8214, 1983. View at Google Scholar · View at Scopus
  9. N. Tanahasi, C. Tsurumi, T. Tamura, and K. Tanaka, “Molecular structures of 20S and 26S proteasomes,” Enzyme and Protein, vol. 47, no. 4–6, pp. 241–251, 1993. View at Google Scholar · View at Scopus
  10. M. E. Matyskiela, G. C. Lander, and A. Martin, “Conformational switching of the 26S proteasome enables substrate degradation,” Nature Structural and Molecular Biology, vol. 20, no. 7, pp. 781–788, 2013. View at Publisher · View at Google Scholar · View at Scopus
  11. Y. Kravtsova-Ivantsiv, S. Cohen, and A. Ciechanover, “Modification by single ubiquitin moieties rather than polyubiquitination is sufficient for proteasomal processing of the p105 NF-kappaB precursor,” Molecular Cell, vol. 33, no. 4, pp. 496–504, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. N. Shabek, Y. Herman-Bachinsky, S. Buchsbaum et al., “The size of the proteasomal substrate determines whether its degradation will be mediated by mono- or polyubiquitylation,” Molecular Cell, vol. 48, no. 1, pp. 87–97, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. Y. Murakami, S. Matsufuji, T. Kameji et al., “Ornithine decarboxylase is degraded by the 26S proteasome without ubiquitination,” Nature, vol. 360, no. 6404, pp. 597–599, 1992. View at Publisher · View at Google Scholar · View at Scopus
  14. R. J. Sheaff, J. D. Singer, J. Swanger, M. Smitherman, J. M. Roberts, and B. E. Clurman, “Proteasomal turnover of p21Cip1 does not require p21Cip1 ubiquitination,” Molecular Cell, vol. 5, no. 2, pp. 403–410, 2000. View at Publisher · View at Google Scholar · View at Scopus
  15. A. Ciechanover and A. Stanhill, “The complexity of recognition of ubiquitinated substrates by the 26S proteasome,” Biochimica et Biophysica Acta—Molecular Cell Research, vol. 1843, no. 1, pp. 86–96, 2014. View at Publisher · View at Google Scholar · View at Scopus
  16. G. K. Tofaris, R. Layfield, and M. G. Spillantini, “α-Synuclein metabolism and aggregation is linked to ubiquitin-independent degradation by the proteasome,” FEBS Letters, vol. 509, no. 1, pp. 22–26, 2001. View at Publisher · View at Google Scholar · View at Scopus
  17. P. Tsvetkov, N. Reuven, C. Prives, and Y. Shaul, “Susceptibility of p53 unstructured N terminus to 20 S proteasomal degradation programs the stress response,” Journal of Biological Chemistry, vol. 284, no. 39, pp. 26234–26242, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. A. Jr. Belogurov, A. Kudriaeva, E. Kuzina et al., “Multiple sclerosis autoantigen myelin basic protein escapes control by ubiquitination during proteasomal degradation,” Journal of Biological Chemistry, vol. 289, no. 25, pp. 17758–17766, 2014. View at Google Scholar
  19. A. A. Belogurov Jr., N. A. Ponomarenko, V. M. Govorun, A. G. Gabibov, and A. V. Bacheva, “Site-specific degradation of myelin basic protein by the proteasome,” Doklady Biochemistry and Biophysics, vol. 425, no. 1, pp. 68–72, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. E. S. Kuzina, E. L. Chernolovskaya, A. A. Kudriaeva et al., “Immunoproteasome enhances intracellular proteolysis of myelin basic protein,” Doklady Biochemistry and Biophysics, vol. 453, no. 1, pp. 300–303, 2013. View at Google Scholar
  21. G. Harauz, N. Ishiyama, C. M. D. Hill, I. R. Bates, D. S. Libich, and C. Farès, “Myelin basic protein—diverse conformational states of an intrinsically unstructured protein and its roles in myelin assembly and multiple sclerosis,” Micron, vol. 35, no. 7, pp. 503–542, 2004. View at Publisher · View at Google Scholar · View at Scopus
  22. J. M. Boggs, L. Homchaudhuri, G. Ranagaraj, Y. Liu, G. S. Smith, and G. Harauz, “Interaction of myelin basic protein with cytoskeletal and signaling proteins in cultured primary oligodendrocytes and N19 oligodendroglial cells,” BMC Research Notes, vol. 7, article 387, 2014. View at Publisher · View at Google Scholar
  23. C. M. D. Hill and G. Harauz, “Charge effects modulate actin assembly by classic myelin basic protein isoforms,” Biochemical and Biophysical Research Communications, vol. 329, no. 1, pp. 362–369, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. D. S. Libich, C. Hill, I. R. Bates et al., “Interaction of the 18.5-kD isoform of myelin basic protein with Ca2+-calmodulin: effects of deimination assessed by intrinsic Trp fluorescence spectroscopy, dynamic light scattering, and circular dichroism,” Protein Science, vol. 12, no. 7, pp. 1507–1521, 2003. View at Publisher · View at Google Scholar · View at Scopus
  25. V. Majava, C. Wang, M. Myllykoski et al., “Structural analysis of the complex between calmodulin and full-length myelin basic protein, an intrinsically disordered molecule,” Amino Acids, vol. 39, no. 1, pp. 59–71, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. G. S. T. Smith, M. De Avila, P. M. Paez et al., “Proline substitutions and threonine pseudophosphorylation of the SH3 ligand of 18.5-kDa myelin basic protein decrease its affinity for the Fyn-SH3 domain and alter process development and protein localization in oligodendrocytes,” Journal of Neuroscience Research, vol. 90, no. 1, pp. 28–47, 2012. View at Publisher · View at Google Scholar · View at Scopus
  27. L. Homchaudhuri, E. Polverini, W. Gao, G. Harauz, and J. M. Boggs, “Influence of membrane surface charge and post-translational modifications to myelin basic protein on its ability to tether the Fyn-SH3 domain to a membrane in vitro,” Biochemistry, vol. 48, no. 11, pp. 2385–2393, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. S. D. Miller, W. J. Karpus, and T. S. Davidson, “Experimental autoimmune encephalomyelitis in the mouse,” Current Protocols in Immunology, chapter 15, unit 151, 2010. View at Google Scholar
  29. M. H. Glickman, D. M. Rubin, V. A. Fried, and D. Finley, “The regulatory particle of the Saccharomyces cerevisiae proteasome,” Molecular and Cellular Biology, vol. 18, no. 6, pp. 3149–3162, 1998. View at Google Scholar · View at Scopus
  30. V. V. Bamm, M. A. M. Ahmed, and G. Harauz, “Interaction of myelin basic protein with actin in the presence of dodecylphosphocholine micelles,” Biochemistry, vol. 49, no. 32, pp. 6903–6915, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. V. Majava, M. V. Petoukhov, N. Hayashi, P. Pirilä, D. I. Svergun, and P. Kursula, “Interaction between the C-terminal region of human myelin basic protein and calmodulin: analysis of complex formation and solution structure,” BMC Structural Biology, vol. 8, article 10, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. D. Teitelbaum, R. Aharoni, M. Sela, and R. Arnon, “Cross-reactions and specificities of monoclonal antibodies against myelin basic protein and against the synthetic copolymer 1,” Proceedings of the National Academy of Sciences of the United States of America, vol. 88, no. 21, pp. 9528–9532, 1991. View at Publisher · View at Google Scholar · View at Scopus
  33. L. A. Munishkina, A. L. Fink, and V. N. Uversky, “Conformational prerequisites for formation of amyloid fibrils from histones,” Journal of Molecular Biology, vol. 342, no. 4, pp. 1305–1324, 2004. View at Publisher · View at Google Scholar · View at Scopus
  34. Q. Deveraux, V. Ustrell, C. Pickart, and M. Rechsteiner, “A 26 S protease subunit that binds ubiquitin conjugates,” Journal of Biological Chemistry, vol. 269, no. 10, pp. 7059–7061, 1994. View at Google Scholar · View at Scopus
  35. K. Husnjak, S. Elsasser, N. Zhang et al., “Proteasome subunit Rpn13 is a novel ubiquitin receptor,” Nature, vol. 453, no. 7194, pp. 481–488, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. C. Wang, U. Neugebauer, J. Bürck et al., “Charge isomers of myelin basic protein: structure and interactions with membranes, nucleotide analogues, and calmodulin,” PLoS ONE, vol. 6, no. 5, Article ID e19915, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. M. A. Ahmed, V. V. Bamm, L. Shi et al., “Induced secondary structure and polymorphism in an intrinsically disordered structural linker of the CNS: solid-state NMR and FTIR spectroscopy of myelin basic protein bound to actin,” Biophysical Journal, vol. 96, no. 1, pp. 180–191, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. C. G. Pack, H. Yukii, A. Toh-e et al., “Quantitative live-cell imaging reveals spatio-temporal dynamics and cytoplasmic assembly of the 26S proteasome,” Nature Communications, vol. 5, p. 3396, 2014. View at Google Scholar
  39. D. J. Black, Q.-K. Tran, and A. Persechini, “Monitoring the total available calmodulin concentration in intact cells over the physiological range in free Ca2+,” Cell Calcium, vol. 35, no. 5, pp. 415–425, 2004. View at Publisher · View at Google Scholar · View at Scopus
  40. A. Persechini and B. Cronk, “The relationship between the free concentrations of Ca2+ and Ca2+- calmodulin in intact cells,” The Journal of Biological Chemistry, vol. 274, no. 11, pp. 6827–6830, 1999. View at Publisher · View at Google Scholar · View at Scopus
  41. T. D. Pollard, L. Blanchoin, and R. D. Mullins, “Molecular mechanisms controlling actin filament dynamics in nonmuscle cells,” Annual Review of Biophysics and Biomolecular Structure, vol. 29, pp. 545–576, 2000. View at Publisher · View at Google Scholar · View at Scopus
  42. T. Kiuchi, T. Nagai, K. Ohashi, and K. Mizuno, “Measurements of spatiotemporal changes in G-actin concentration reveal its effect on stimulus-induced actin assembly and lamellipodium extension,” Journal of Cell Biology, vol. 193, no. 2, pp. 365–380, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. P. Tsvetkov, N. Reuven, and Y. Shaul, “The nanny model for IDPs,” Nature Chemical Biology, vol. 5, no. 11, pp. 778–781, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. M. K. Tewari, G. Sinnathamby, D. Rajagopal, and L. C. Eisenlohr, “A cytosolic pathway for MHC class II-restricted antigen processing that is proteasome and TAP dependent,” Nature Immunology, vol. 6, no. 3, pp. 287–294, 2005. View at Publisher · View at Google Scholar · View at Scopus