281
Views
3
CrossRef citations to date
0
Altmetric
Research Articles

Conformational changes associated with L16P and T118M mutations in the membrane-embedded PMP22 protein, consequential in CMT-1A

, , &
Pages 2880-2894 | Received 29 May 2016, Accepted 01 Sep 2016, Published online: 05 Oct 2016

References

  • Adlkofer, K., Naef, R., & Suter, U. (1997). Analysis of compound heterozygous mice reveals that the Trembler mutation can behave as a gain-of-function allele. Journal of Neuroscience Research, 49, 671–680.10.1002/(ISSN)1097-4547
  • Amadei, A., Linssen, A. B., & Berendsen, H. J. (1993). Essential dynamics of protein. Proteins, 17, 412–425.10.1002/(ISSN)1097-0134
  • Bello, M., Campos-Rodriguez, R., Rojas-Hernandez, S., Contis-Montes de Oca, A., & Correa-Basurto, J. (2015). Predicting peptide vaccine candidates against H1N1 influenza virus through theoretical approaches. Immunologic Research, 62, 3–15.10.1007/s12026-015-8629-1
  • Bello, M., & Correa-Basurto, J. (2013). Molecular dynamics simulations to provide insights into epitopes coupled to the soluble and membrane-bound MHC-II complexes. PLoS ONE, 8, e72575.10.1371/journal.pone.0072575
  • Berendsen, H. J. C., van der Spoel, D., & van Drunen, R. (1995). GROMACS. A message-passing parallel molecular dynamics implementation. Computer Physics Communications, 91, 43–56.10.1016/0010-4655(95)00042-E
  • Case, D. A., Cheatham, T. E., Darden, T., Gohlke, H., Luo, R., Merz, K. M., … Woods, R. J. (2005). The Amber biomolecular simulation programs. Journal of Computational Chemistry, 26, 1668–1688.10.1002/(ISSN)1096-987X
  • Chen, V. B., Arendall III, W. B., Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., … Richardson, D. C. (2010). MolProbity: All-atom structure validation for macromolecular crystallography. Acta Crystallographica, D66, 12–21.
  • Colby, J., Nicholson, R., Dickson, K. M., Orfali, W., Naef, R., Suter, U., … Snipes, G. J. (2000). PMP22 carrying the trembler or trembler-J mutation is intracellularly retained in myelinating schwann cells. Neurobiology of Disease, 7, 561–573.10.1006/nbdi.2000.0323
  • Comeau, S. R., Gatchell, D. W., Vajda, S., & Camacho, C. J. (2004). ClusPro: An automated docking and discrimination method for the prediction of protein complexes. Bioinformatics, 20, 45–50.10.1093/bioinformatics/btg371
  • Darden, T., York, D., & Pedersen, L. (1993). Particle Mesh Ewald-an N.Log(N) method for Ewald sums in large systems. Journal of Chemical Physics, 98, 10089–10092.10.1063/1.464397
  • DeLano, W. L. (2002). The PyMOL molecular graphics system. San Carlos, CA: DeLano Scientific. Retrieved from http://www.pymol.org
  • D’Urso, D., Prior, R., Greiner-Petter, R., Gabreels-Festen, A. A., & Muller, H. W. (1998). Overloaded endoplasmic reticulum-Golgi compartments, a possible pathomechanism of peripheral neuropathies caused by mutations of the peripheral myelin protein PMP22. Journal of Neuroscience, 18, 731–740.
  • Fledrich, R., Stassart, R. M., Klink, A., Rasch, L. M., Prukop, T., Haag, L., … Sereda, M. W. (2014). Soluble neuregulin-1 modulates disease pathogenesis in rodent models of Charcot-Marie-Tooth disease 1A. Nature Medicine, 20, 1055–1061.10.1038/nm.3664
  • Gohlke, H., & Case, D. A. (2004). Converging free energy estimates: MMPB(GB)SA studies on the protein-protein complex Ras-Raf. Journal of Computational Chemistry, 25, 238–250.10.1002/(ISSN)1096-987X
  • Götz, A. W., Williamson, M. J., Xu, D., Poole, D., Le Grand, S., & Walker, R. C. (2012). Routine microsecond molecular dynamics simulations with AMBER-Part I: Generalized Born. Journal of Chemical Theory and Computation, 8, 1542–1555.10.1021/ct200909j
  • Hara, T., Hashimoto, Y., Akuzawa, T., Hirai, R., Kobayashi, H., & Sato, K. (2014). Rer1 and calnexin regulate endoplasmic reticulum retention of a peripheral myelin protein 22 mutant that causes type 1A Charcot-Marie-Tooth disease. Scientific Reports, 4, 6992.10.1038/srep06992
  • Hawkins, G. D., Cramer, C. J., & Truhlar, D. G. (1996). Parametrized models of aqueous free energies of solvation based on pairwise descreening of solute atomic charges from a dielectric medium. Journal of Physical Chemistry, 100, 19824–19839.10.1021/jp961710n
  • Hoogendijk, J. E., Janssen, E. A., Gabreëls-Festen, A. A., Hensels, G. W., Joosten, E. M., Gabreëls, F. J., … Ongerboer de Visser, B. W. (1993). Allelic heterogeneity in hereditary motor and sensory neuropathy type Ia (Charcot-Marie-Tooth disease type 1a). Neurology, 43, 1010–1015.10.1212/WNL.43.5.1010
  • Houlden, H., & Reilly, M. M. (2006). Molecular genetics of autosomal-dominant demyelinating Charcot-Marie-Tooth disease. NeuroMolecular Medicine, 8, 43–62.10.1385/NMM:8:1-2:43
  • Ionasescu, V. V., Ionasescu, R., Searby, C., & Neahring, R. (1995). Dejerine-Sottas disease with de novo dominant point mutation of the PMP22 gene. Neurology, 45, 1766–1767.10.1212/WNL.45.9.1766
  • Jo, S., Lim, J. B., Klauda, J. B., & Im, W. (2009). CHARMM-GUI membrane builder for mixed bilayers and its application to yeast membranes. Biophysical Journal, 97, 50–58.10.1016/j.bpj.2009.04.013
  • Jo, S. T., Kim, & Im, W. (2007). Automated builder and database of protein/membrane complexes for molecular dynamics simulations. PLoS ONE, 2, e880.10.1371/journal.pone.0000880
  • Kollman, P. A., Massova, I., Reyes, C., Kuhn, B., Huo, S., Chong, L., … Cheatham 3rd, T. E. (2000). Calculating structures and free energies of complex molecules: Combining molecular mechanics and continuum models. Accounts of Chemical Research, 33, 889–897.10.1021/ar000033j
  • Kozakov, D., Hall, D. R., Beglov, D., Brenke, R., Comeau, S. R., Shen, Y., & … Vajda, S. (2010). Achieving reliability and high accuracy in automated protein docking: Cluspro, PIPER, SDU, and stability analysis in CAPRI rounds 13-19. Proteins, 78, 3124–3130.10.1002/prot.v78:15
  • Kumar, C. V., Swetha, R, G., Anbarasu, A., & Ramaiah, S. (2014). Computational analysis reveals the association of threonine 118 methionine mutation in PMP22 resulting in CMT-1A. Advances in Bioinformatics, 2014, 502618.
  • Li, J., Parker, B., Martyn, C., Natarajan, C., & Guo, J. (2013). The PMP22 gene and its related diseases. Molecular Neurobiology, 47, 673–698.10.1007/s12035-012-8370-x
  • Lindahl, E., Hess, B., & van der Spoel, D. (2001). GROMACS 3.0: A package for molecular simulation and trajectory analysis. Journal of Molecular Modeling, 7, 306–317.
  • Lomize, M. A., Lomize, A. L., Pogozheva, I. D., & Mosberg, H. I. (2006). OPM: Orientations of proteins in membranes database. Bioinformatics, 22, 623–625.10.1093/bioinformatics/btk023
  • Lupski, J. R., & Chance, P. F. (2005). Hereditary motor and sensory neuropathies involving altered dosage or mutations of PMP22: The CMT1A duplication and HNPP deletion. In P. J. Dyck & P. K. Thomas (Eds.), Peripheral Neuropathy (4th ed., pp. 1659–1680). Philadelphia, PA: Elsevier Saunders.10.1016/B978-0-7216-9491-7.50073-9
  • Lupski, J. R., de Oca-Luna, R. M., Slaugenhaupt, S., Pentao, L., Guzzetta, V., Trask, B. J., … Patel, P. I. (1991). DNA duplication associated with Charcot-Marie-Tooth disease type 1A. Cell, 66, 219–232.10.1016/0092-8674(91)90613-4
  • Lupski, J. R., & Garcia, C. A. (2001). Charcot-Marie-Tooth peripheral neuropathies and related disorders. In C. R. Scriver, A. L. Beaudet, & W. S. Sly (Eds.), The metabolic and molecular bases of inherited disorders (8th ed., pp. 5759–5788). New York, NY: McGraw-Hill.
  • Marques Jr. W., Thomas, P. K., Sweeney, M. G., Carr, L., & Wood, N. W. (1998). Dejerine-Sottas neuropathy and PMP22 point mutations: A new base pair substitution and a possible “hot spot” on Ser72. Annals of Neurology, 43, 680–683.10.1002/(ISSN)1531-8249
  • Matsunami, N., Smith, B., Ballard, L., Lensch, M. W., Robertson, M., Albertsen, H., & … Chance, P. F. (1992). Peripheral myelin protein-22 gene maps in the duplication in chromosome 17p11.2 associated with Charcot-Marie-Tooth 1A. Nature Genetics, 1, 176–179.10.1038/ng0692-176
  • Meekins, G. D., Emery, M. J., & Weiss, M. D. (2004). Nerve conduction abnormalities in the trembler-j mouse: A model for Charcot-Marie-Tooth disease type 1A? Journal of the Peripheral Nervous System, 9, 177–182.10.1111/j.1085-9489.2004.09310.x
  • Miller, B. R., McGee, T. D., Swails, J. M., Homeyer, N., Gohlke, H., & Roitberg, A. E. (2012). MMPBSA.py: An efficient program for end-state free energy calculations. Journal of Chemical Theory and Computation, 8, 3314–3321.10.1021/ct300418h
  • Mittendorf, K. F., Kroncke, B. M., Meiler, J., & Sanders, C. R. (2014). The homology model of PMP22 suggests mutations resulting in peripheralneuropathy disrupt transmembrane helix packing. Biochemistry, 53, 6139–6141.10.1021/bi500809t
  • Naef, R., & Suter, U. (1999). Impaired intracellular trafficking is a common disease mechanism of PMP22 point mutations in peripheral neuropathies. Neurobiology of Disease, 6, 1–14.10.1006/nbdi.1998.0227
  • Nakatsukasa, K., & Brodsky, J. L. (2008). The recognition and retrotranslocation of misfolded proteins from the endoplasmic reticulum. Traffic, 9, 861–870.10.1111/j.1600-0854.2008.00729.x
  • Nelis, E., Timmerman, V., De Jonghe, P., & Van Broeckhoven, C. (1994). Identification of a 5_ splice site mutation in the PMP-22 gene in autosomal dominant Charcot-Marie-Tooth disease type 1. Human Molecular Genetics, 3, 515–516.10.1093/hmg/3.3.515
  • Nicholson, G. A., Valentijn, L. J., Cherryson, A. K., Kennerson, M. L., Bragg, T. L., DeKroon, R. M., & … Bolhuis, P. A. (1994). A frame shift mutation in the PMP22 gene in hereditary neuropathy with liability to pressure palsies. Nature Genetics, 6, 263–266.10.1038/ng0394-263
  • Numakura, C., Lin, C., Oka, N., Akiguchi, I., & Hayasaka, K. (2000). Hemizygous mutation of the peripheral myelin protein 22 gene associated with Charcot-Marie-Tooth disease type 1. Annals of Neurology, 47, 101–103.10.1002/(ISSN)1531-8249
  • Nygaard, R., Zou, Y., Dror, R. O., Mildorf, T. J., Arlow, D. H., Manglik, A., … Kobilka, B. K. (2013). The dynamic process of β(2) adrenergic receptor activation. Cell, 152, 532–542.10.1016/j.cell.2013.01.008
  • Parman, Y., Planté-Bordeneuve, V., Guiochon-Mantel, A., Eraksoy, M., & Said, G. (1999). Recessive inheritance of a new point mutation of the PMP22 gene in Dejerine-Sottas disease. Annals of Neurology, 45, 518–522.10.1002/(ISSN)1531-8249
  • Patel, P. I., Roa, B. B., Welcher, A. A., Schoener-Scott, R., Trask, B. J., Pentao, L., … Suter, U. (1992). The gene for the peripheral myelin protein PMP-22 is a candidate for Charcot-Marie-Tooth disease type 1A. Nature Genetics, 1, 159–165.10.1038/ng0692-159
  • Patzkó, A., & Shy, M. E. (2011). Update on Charcot-Marie-Tooth disease. Current Neurology and Neuroscience Reports, 11, 78–88.10.1007/s11910-010-0158-7
  • Raeymaekers, P., Timmerman, V., Nelis, E., De Jonghe, P., Hoogendijk, J. E., Baas, F., … Bolhuis, P. A. (1991). Duplication in chromosome 17p11.2 in Charcot-Marie-Tooth neuropathy type 1a (CMT 1a). The HMSN Collaborative Research Group. Neuromuscular Disorder, 1, 93–97.10.1016/0960-8966(91)90055-W
  • Roa, B. B., Dyck, P. J., Marks, H. G., Chance, P. F., & Lupski, J. R. (1993). Dejerine-Sottas syndrome associated with point mutation in the peripheral myelin protein 22 (PMP22) gene. Nature Genetics, 5, 269–273.10.1038/ng1193-269
  • Roa, B. B., Garcia, C. A., Pentao, L., Killian, J. M., Trask, B. J., Suter, U., … Lupski, J. R. (1993). Evidence for a recessive PMP22 point mutation in Charcot-Marie-Tooth disease type 1A. Nature Genetics, 5, 189–194.10.1038/ng1093-189
  • Roa, B. B., Garcia, C. A., Suter, U., Kulpa, D. A., Wise, C. A., Mueller, J., … Lupski, J. R. (1993). Charcot-Marie-Tooth Disease type 1A. Association with a spontaneous point mutation in the PMP22 gene. New England Journal of Medicine, 329, 96–101.10.1056/NEJM199307083290205
  • Roy, A., Kucukural, A., & Zhang, Y. (2010). I-TASSER: A unified platform for automated protein structure and function prediction. Nature Protocols, 5, 725–738.10.1038/nprot.2010.5
  • Salomon-Ferrer, R., Götz, A. W., Poole, D., Le Grand, S., & Walker, R. C. (2013). Routine microsecond molecular dynamics simulations with AMBER-Part II: Particle Mesh Ewald. Journal of Chemical Theory and Computation, 9, 3878–3888.10.1021/ct400314y
  • Schlebach, J. P., Narayan, M., Alford, C., Mittendorf, K. F., Carter, B. D., Li, J., … Sanders, C, R. (2015). Conformational stability and pathogenic misfolding of the integral membrane protein PMP22. Journal of American Chemical Society, 137, 8758–8768.10.1021/jacs.5b03743
  • Skjevik, A. A., Madej, B. D., Walker, R. C., & Teigen, K. (2012). LIPID11: A modular framework for lipid simulations using amber. Journal of Physical Chemistry B, 116, 11124–11136.10.1021/jp3059992
  • Snipes, G. J., Suter, U., Welcher, A. A., & Shooter, E. M. (1992). Characterization of a novel peripheral nervous system myelin protein (PMP-22/SR13). Journal of Cell Biology, 117, 225–238.10.1083/jcb.117.1.225
  • Srinivasan, J., Miller, J., Kollman, P. A., & Case, D. A. (1998). Continuum solvent studies of the stability of RNA hairpin loops and helices. Journal of Biomolecular Structure and Dynamics, 16, 671–682.10.1080/07391102.1998.10508279
  • Timmerman, V., Nelis, E., Van Hul, W., Nieuwenhuijsen, B. W., Chen, K. L., Wang, S., … Van Broeckhoven, C. (1992). The peripheral myelin protein gene PMP-22 is contained within the Charcot-Marie-Tooth disease type 1A duplication. Nature Genetics, 1, 171–175.10.1038/ng0692-171
  • Tobler, A. R., Liu, N., Mueller, L., & Shooter, E. M. (2002). Differential aggregation of the Trembler and Trembler Jmutants of peripheral myelin protein 22. Proceedings of the National Academy of Science USA, 99, 483–488.10.1073/pnas.012593399
  • Tobler, A. R., Notterpek, L., Naef, R., Taylor, V., Suter, U., & Shooter, E. M. (1999). Transport of Trembler-J mutant peripheral myelin protein 22 is blocked in the intermediate compartment and affects the transport of the wildtype protein by direct interaction. Journal of Neuroscience, 19, 2027–2036.
  • Valentijn, L. J., Bolhuis, P. A., Zorn, I., Hoogendijk, J. E., van den Bosch, N., Hensels, G. W., … Baas, F. (1992). The peripheral myelin gene PMP-22/GAS-3 is duplicated in Charcot- Marie-Tooth disease type 1A. Nature Genetics, 1, 166–170.10.1038/ng0692-166
  • Van Der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A. E., & Berendsen, H. J. (2005). GROMACS. Fast, flexible, and free. Journal Computational Chemistry, 26, 1701–1718.10.1002/(ISSN)1096-987X
  • Van Gunsteren, W. F., & Berendsen, H. J. C. (1997). Algorithms for macromolecular dynamics and constraint dynamics. Molecular Physics, 34, 1311–1327.
  • Wallace, A. C., Laskowski, R. A., & Thornton, J. M. (1995). LIGPLOT: A program to generate schematic diagrams of protein-ligand interactions. Protein Engineering Design & Selection, 8, 127–134.10.1093/protein/8.2.127
  • Wang, J., Hou, T., & Xu, X. (2006). Recent advances in free energy calculations with a combination of molecular mechanics and continuum models. Current Computational-Aided Drug Design, 2, 287–306.10.2174/157340906778226454
  • Wang, J., Wolf, R. M., Caldwell, J. W., Kollman, P. A., & Case, D. A. (2004). Development and testing of a general amber force field. Journal of Computational Chemistry, 25, 1157–1174.10.1002/(ISSN)1096-987X
  • Wolf, M. G., Hoefling, M., Aponte-Santamaría, C., Grubmüller, H., & Groenhof, G. (2010). g_membed. Efficient insertion of a membrane protein into an equilibrated lipid bilayer with minimal perturbation. Journal of Computational Chemistry, 31, 2169–2174.10.1002/jcc.v31:11
  • Woolf, T. B. & Roux, B. (1994). Molecular dynamics simulation of the gramicidin channel in a phospholipid bilayer. Proceedings of the National Academy of Science USA, 91, 11631–11635.10.1073/pnas.91.24.11631
  • Woolf, T. B., & Roux, B. (1996). Structure, energetics, and dynamics of lipid–protein interactions: A molecular dynamics study of the gramicidin A channel in a DMPC bilayer. Proteins, 24, 92–114.10.1002/(ISSN)1097-0134
  • Xu, D., & Yang, Z. (2011). Improving the physical realism and structural accuracy of protein models by a two-step atomic-level energy minimization. Biophysical Journal, 101, 2525–2534.10.1016/j.bpj.2011.10.024
  • Yang, J., Yan, R., Roy, A., Xu, D., Poisson, J., & Zhang, Y. (2015). The I-TASSER Suite: Protein structure and function prediction. Nature Methods, 12, 7–8.
  • Zhang, Y. (2008). I-TASSER server for protein 3D structure prediction. BMC Bioinformatics, 9, 40. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/1821531610.1186/1471-2105-9-40

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.