402
Views
11
CrossRef citations to date
0
Altmetric
Research Articles

Local structural unfolding at the edge-strands of beta sheets is the molecular basis for instability and aggregation of G85R and G93A mutants of superoxide dismutase 1

, & ORCID Icon
Pages 647-659 | Received 15 Oct 2018, Accepted 14 Feb 2019, Published online: 11 Mar 2019

References

  • Atkin, J. D., Farg, M. A., Soo, K. Y., Walker, A. K., Halloran, M., Turner, B. J., … Horne, M. K. (2014). Mutant SOD1 inhibits ER–Golgi transport in amyotrophic lateral sclerosis. Journal of Neurochemistry, 129(1), 190–204. doi:10.1111/jnc.12493
  • Banci, L., Bertini, I., Boca, M., Girotto, S., Martinelli, M., Valentine, J. S., & Vieru, M. (2008). SOD1 and amyotrophic lateral sclerosis: Mutations and oligomerization. PLoS One, 3, e1677. doi:10.1371/journal.pone.0001677
  • Banci, L., Bertini, I., Boca, M., Calderone, V., Cantini, F., Girotto, S., & Vieru, M. (2009). Structural and dynamic aspects related to oligomerization of apo SOD1 and its mutants. Proceedings of the National Academy of Sciences of the United States of America, 106(17), 6980–6985. doi:10.1073/pnas.0809845106
  • Baranyai, A., & Evans, D. J. (1989). Direct entropy calculation from computer simulation of liquids. Physical Review A, General Physics, 40(7), 3817–3822.
  • Baxa, M. C., Haddadian, E. J., Jumper, J. M., Freed, K. F., & Sosnick, T. R. (2014). Loss of conformational entropy protein folding calculated using realistic ensembles and its implications for NMR-based calculations. Proceedings of the National Academy of Sciences USA, 111 (43), 15396–15401. doi:10.1073/pnas.1407768111
  • Bunton-Stasyshyn, R. K., Saccon, R. A., Fratta, P., & Fisher, E. M. (2015). SOD1 function and its implications for amyotrophic lateral sclerosis pathology: New and renascent themes. The Neuroscientist, 21, 519–529. doi:10.1177/1073858414561795
  • Case, D. A., Cheatham, T. E., Darden, T., Gohlke, H., Luo, R., Merz, K. M., Jr., … Woods, R. J. (2005). The Amber biomolecular simulation programs. Journal of Computational Chemistry, 26(16), 1668–1688. doi:10.1002/jcc.20290
  • Cao, X., Antonyuk, S. V., Seetharaman, S. V., Whitson, L. J., Taylor, A. B., Holloway, S. P., … Tiwari, A. (2008). Structures of the G85R variant of SOD1 in familial amyotrophic lateral sclerosis. The Journal of Biological Chemistry, 283(23), 16169–16177. doi:10.1074/jbc.M801522200
  • Corson, L. B., Strain, J. J., Culotta, V. C., & Cleveland, D. W. (1998). Chaperone-facilitated copper binding is a property common to several classes of familial amyotrophic lateral sclerosis-linked superoxide dismutase mutants. Proceedings of the National Academy of Sciences of the United States of America, 95(11), 6361–6366.
  • Das, S., & Mukhopadhyay, D. (2011). Intrinsically unstructured proteins and neurodegenerative diseases: conformational promiscuity at its best. IUBMB Life, 63(7), 478–488. doi:10.1002/iub.498
  • Demeule, B., Palais, C., Machaidze, G., Gurny, R., & Arvinte, T. (2009). New methods allowing the detection of protein aggregates: A case study on trastuzumab. mABS, 1(2), 142–150.
  • De Simone, A., Kitchen, C., Kwan, A. H., Sunde, M., Dobson, C. M., & Frenkel, D. (2012). Intrinsic disorder modulates protein self-assembly and aggregation. Proceedings of the National Academy of Sciences of the United States of America, 109(18), 6951–6956. doi:10.1073/pnas.1118048109
  • Dill, K. A., Ozkan, S. B., Shell, M. S., & Weikl, T. R. (2008). The protein folding problem. Annual Review of Biophysics, 37, 289–316. doi:10.1146/annurev.biophys.37.092707.153558
  • Elam, J. S., Taylor, A. B., Strange, R., Antonyuk, S., Doucette, P. A., Rodriguez, J. A., … Yeates, T. O. (2003). Amyloid-like filaments and water-filled nanotubes formed by SOD1 mutant proteins linked to familial ALS. Nature Structural Biology, 10(6), 461–467. doi:10.1038/nsb935
  • Evans, D. J., & Holian, B. L. (1985). The Nose–Hoover thermostat. Journal of Chemical Physics., 83(8), 4069. doi:10.1063/1.449071
  • Ewald, P. (1921). Die Berechnung optischer und elektrostatischer Gitterpotentiale. Annalen Der Physik, 369(3), 253–287. doi:10.1002/andp.19213690304
  • Fink, A. L. (1998). Protein aggregation: Folding aggregates, inclusion bodies and amyloid. Folding & Design, 3(1), R9–R23. doi:10.1016/S1359-0278(98)00002-9
  • Frieden, C. (2007). Protein aggregation processes: In search of the mechanism. Protein Science: A Publication of the Protein Society, 16(11), 2334–2344. doi:10.1110/ps.073164107
  • Furukawa, Y., Anzai, I., Akiyama, S., Imai, M., Cruz, F. J., Saio, T., … Ishimori, K. (2016). Conformational disorder of the most immature Cu, Zn-superoxide dismutase leading to amyotrophic lateral sclerosis. The Journal of Biological Chemistry, 291(8), 4144–4155. doi:10.1074/jbc.M115.683763
  • Galaleldeen, A., Strange, R. W., Whitson, L. J., Antonyuk, S. V., Narayana, N., Taylor, A. B., … Hart, P. J. (2009). Structural and biophysical properties of metal-free pathogenic SOD1 mutants A4V and G93A. Archives of Biochemistry and Biophysics, 492(1-2), 40–47. doi:10.1016/j.abb.2009.09.020
  • Ghosh, D. K., Kumar, A., & Ranjan, A. (2018). Metastable states of HYPK-UBA domain's seeds drive the dynamics of its own aggregation. Biochimica et Biophysica Acta. General Subjects, 1862(12), 2846–2861. doi:10.1016/j.bbagen.2018.09.003
  • Ghosh, D. K., Roy, A., & Ranjan, A. (2018). Aggregation-prone regions in HYPK help it to form sequestration complex for toxic protein aggregates. Journal of Molecular Biology, 430(7), 963–986. doi:10.1016/j.jmb.2018.02.007
  • Ghosh, D. K., Roy, A., & Ranjan, A. (2018). Disordered nanostructure in Huntingtin interacting protein K acts as a stabilizing switch to prevent protein aggregation. Biochemistry, 57(13), 2009–2023. doi:10.1021/acs.biochem.7b00776
  • Gros-Louis, F., Gaspar, C., & Rouleau, G. A. (2006). Genetics of familial and sporadic amyotrophic lateral sclerosis. Biochimica et Biophysica Acta, 1762(11-12), 956–972. doi:10.1016/j.bbadis.2006.01.004
  • Guegan, C., & Przedborski, S. (2003). Programmed cell death in amyotrophic lateral sclerosis. The Journal of Clinical Investigation, 111(2), 153–161. doi:10.1172/JCI17610
  • Hayward, L. J., Rodriguez, J. A., Kim, J. W., Tiwari, A., Goto, J. J., Cabelli, D. E., … Brown, R. H. Jr. (2002). Decreased metallation and activity in subsets of mutant superoxide dismutases associated with familial amyotrophic lateral sclerosis. Journal of Biological Chemistry, 277(18), 15923–15931. doi:10.1074/jbc.M112087200
  • Hinsen, K. (2000). The molecular modeling toolkit: A new approach to molecular simulations. Journal of Computational Chemistry, 21(2), 79–85. doi:10.1002/(SICI)1096-987X(20000130)21:2<79::AID-JCC1>3.0.CO;2-B
  • Johnston, J. A., Dalton, M. J., Gurney, M. E., & Kopito, R. R. (2000). Formation of high molecular weight complexes of mutant Cu, Zn-superoxide dismutase in a mouse model for familial amyotrophic lateral sclerosis. Proceedings of the National Academy of Sciences USA, 97(23), 12571–12576. doi:10.1073/pnas.220417997
  • Keerthana, S. P., & Kolandaivel, P. (2015). Study of mutation and misfolding of Cu-Zn SOD1 protein. Journal of Biomolecular Structure & Dynamics, 33(1), 167–183. doi:10.1080/07391102.2013.865104
  • Klose, D. P., Wallace, B. A., & Janes, R. W. (2010). 2Struc: The secondary structure server. Bioinformatics (Oxford, England), 26(20), 2624–2625. doi:10.1093/bioinformatics/btq480
  • Kuo-Chen, C., & Hong-Bin, S. (2009). FoldRate: A web-server for predicting protein folding rates from primary sequence. The Open Bioinformatics Journal, 3(1), 31–50. doi:10.2174/1875036200903010031
  • Lashuel, H. A., Overk, C. R., Oueslati, A., & Masliah, E. (2013). The many faces of α-synuclein: From structure and toxicity to therapeutic target. Nature Reviews. Neuroscience, 14(1), 38–48. doi:10.1038/nrn3406
  • Lelie, H. L., Liba, A., Bourassa, M. W., Chattopadhyay, M., Chan, P. K., Gralla, E. B., … Whitelegge, J. P. (2011). Copper and zinc metallation status of copper–zinc superoxide dismutase from amyotrophic lateral sclerosis transgenic mice. The Journal of Biological Chemistry, 286, 2795–2806. doi:10.1074/jbc.M110.186999
  • Martyna, G. J., Tobias, D. J., & Klein, M. L. (1994). Constant pressure molecular dynamics algorithms. Journal of Chemical Physics., 101(5), 4177. doi:10.1063/1.467468
  • Matsumoto, G., Stojanovic, A., Holmberg, C. I., Kim, S., & Morimoto, R. I. (2005). Structural properties and neuronal toxicity of amyotrophic lateral sclerosis-associated Cu/Zn superoxide dismutase 1 aggregates. The Journal of Cell Biology, 171(1), 75–85. doi:10.1083/jcb.200504050
  • Mera-Adasme, R., Erdmann, H., Berezniak, T., & Ochsenfeld, C. (2016). Destabilization of the metal site as a hub for the pathogenic mechanism of five ALS-linked mutants of copper, zinc superoxide dismutase. Metallomics: Integrated Biometal Science, 8, 1141–1150. doi:10.1039/c6mt00085a
  • Parthiban, V., Gromiha, M. M., & Schomburg, D. (2006). CUPSAT: Prediction of protein stability upon point mutations. Nucleic Acids Research, 34(Web Server issue), W239–W242. doi:10.1093/nar/gkl190
  • Perry, J. J., Shin, D. S., Getzoff, E. D., & Tainer, J. A. (2010). The structural biochemistry of the superoxide dismutases. Biochimica et Biophysica Acta, 1804(2), 245–262. doi:10.1016/j.bbapap.2009.11.004
  • Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., & Ferrin, T. E. (2004). UCSF Chimera – A visualization system for exploratory research and analysis. Journal of Computational Chemistry, 25(13), 1605–1612. doi:10.1002/jcc.20084
  • Polymenidou, M., & Cleveland, D. W. (2011). The seeds of neurodegeneration: Prion-like spreading in ALS. Cell, 147(3), 498–508. doi:10.1016/j.cell.2011.10.011
  • Prakash, A., Kumar, V., Pandey, P., Bharti, D. R., Vishwakarma, P., Singh, R., … Lynn, A. M. (2018). Solvent sensitivity of protein aggregation in Cu, Zn superoxide dismutase: A molecular dynamics simulation study. Journal of Biomolecular Structure & Dynamics, 36(10), 2605–2617. doi:10.1080/07391102.2017.1364670
  • Prudencio, M., Hart, P. J., Borchelt, D. R., & Andersen, P. M. (2009). Variation in aggregation propensities among ALS-associated variants of SOD1: Correlation to human disease. Human Molecular Genetics, 18(17), 3217–3226. doi:10.1093/hmg/ddp260
  • Rakhit, R., & Chakrabartty, A. (2006). Structure, folding, and misfolding of Cu,Zn superoxide dismutase in amyotrophic lateral sclerosis. Biochimica et Biophysica Acta, 1762(11-12), 1025–1037. doi:10.1016/j.bbadis.2006.05.004
  • Ramu, M., Unni, S., Wright, G. S. A., Sruthi, U., & Padmanabhan, B. M. M. (2018). Rational discovery of a SOD1 tryptophan oxidation inhibitor with therapeutic potential for amyotrophic lateral sclerosis. Journal of Biomolecular Structure and Dynamics, 1–33. 10.1080/07391102.2018.1531787. doi:10.1080/07391102.2018.1531787
  • Rasouli, S., Abdolvahabi, A., Croom, C. M., Plewman, D. L., Shi, Y., Ayers, J. I., & Shaw, B. F. (2017). Lysine acylation in superoxide dismutase-1 electrostatically inhibits formation of fibrils with prion-like seeding. The Journal of Biological Chemistry, 292(47), 19366–19380. doi:10.1074/jbc.M117.805283
  • Richardson, J. S., & Richardson, D. C. (2002). Natural beta-sheet proteins use negative design to avoid edge-to-edge aggregation. Proceedings of the National Academy of Sciences of the United States of America, 99, 2754–2759. doi:10.1073/pnas.052706099
  • Saccon, R. A., Bunton-Stasyshyn, R. K., Fisher, E. M., & Fratta, P. (2013). Is SOD1 loss of function involved in amyotrophic lateral sclerosis?. Brain: A Journal of Neurology, 136(Pt 8), 2342–2358. doi:10.1093/brain/awt097
  • Shaw, B. F., & Valentine, J. S. (2007). How do ALS-associated mutations in superoxide dismutase 1 promote aggregation of the protein? Trends in Biochemical Sciences, 32(2), 78–85. doi:10.1016/j.tibs.2006.12.005
  • Shaw, P. J. (2005). Molecular and cellular pathways of neurodegeneration in motor neuron disease. Journal of Neurology, Neurosurgery, and Psychiatry, 76(8), 1046–1057. doi:10.1136/jnnp.2004.048652
  • Sheng, Y., Chattopadhyay, M., Whitelegge, J., & Valentine, J. S. (2012). SOD1 aggregation and ALS: Role of metallation states and disulfide status. Current Topics in Medicinal Chemistry, 12(22), 2560–2572.
  • Shi, P., Strom, A. L., Gal, J., & Zhu, H. (2010). Effects of ALS-related SOD1 mutants on dynein- and KIF5-mediated retrograde and anterograde axonal transport. Biochimica et Biophysica Acta, 1802(9), 707–716. doi:10.1016/j.bbadis.2010.05.008
  • Shi, Y., Abdolvahabi, A., & Shaw, B. F. (2014). Protein charge ladders reveal that the net charge of ALS-linked superoxide dismutase can be different in sign and magnitude from predicted values. Protein Science: A Publication of the Protein Society, 23(10), 1417–1433. doi:10.1002/pro.2526
  • Srinivasan, E., & Rajasekaran, R. (2017). Exploring the cause of aggregation and reduced Zn binding affinity by G85R mutation in SOD1 rendering amyotrophic lateral sclerosis. Proteins, 85(7), 1276–1286. doi:10.1002/prot.25288
  • Stefani, M. (2004). Protein misfolding and aggregation: New examples in medicine and biology of the dark side of the protein world. Biochimica et Biophysica Acta, 1739(1), 5–25. doi:10.1016/j.bbadis.2004.08.004
  • Tafuri, F., Ronchi, D., Magri, F., Comi, G. P., & Corti, S. (2015). SOD1 misplacing and mitochondrial dysfunction in amyotrophic lateral sclerosis pathogenesis. Frontiers in Cellular Neuroscience, 9, 336doi:10.3389/fncel.2015.00336
  • Schrödinger, LLC. (2000). The PyMOL Molecular Graphics System, Version 1.8. New York, NY: Schrödinger, LLC.
  • Tiwari, A., & Hayward, L. J. (2005). Mutant SOD1 instability: Implications for toxicity in amyotrophic lateral sclerosis. Neuro-Degenerative Diseases, 2(3-4), 115–127. doi:10.1159/000089616
  • Tompa, D. R., & Kadhirvel, S. (2017). Molecular dynamics of a far positioned SOD1 mutant V14M reveals pathogenic misfolding behavior. Journal of Biomolecular Structure and Dynamics, 36, 4085–4098. 10.1080/07391102.2017.1407675.
  • Trumbull, K. A., & Beckman, J. S. (2009). A role for copper in the toxicity of zinc-deficient superoxide dismutase to motor neurons in amyotrophic lateral sclerosis. Antioxidants & Redox Signaling, 11(7), 1627–1639. doi:10.1089/ars.2009.2574
  • Tuckerman, M. E., Berne, B. J., & Rossi, A. (1991). Molecular dynamics algorithm for multiple time scales: Systems with disparate masses. Journal of Chemical Physics, 94(2), 1465.
  • Tuckerman, M., Berne, B. J., & Martyna, G. J. (1992). Reversible multiple time scale molecular dynamics. Journal of Chemical Physics., 97(3), 1990. doi:10.1063/1.463137
  • Turner, B. J., Atkin, J. D., Farg, M. A., Zang, D. W., Rembach, A., Lopes, E. C., … Cheema, S. S. (2005). Impaired extracellular secretion of mutant superoxide dismutase 1 associates with neurotoxicity in familial amyotrophic lateral sclerosis. The Journal of Neuroscience, 25(1), 108–117. doi:10.1523/JNEUROSCI.4253-04.2005
  • Uversky, V. N. (2015). Intrinsically disordered proteins and their (disordered) proteomes in neurodegenerative disorders. Frontiers in Aging Neuroscience, 7, 18. doi:10.3389/fnagi.2015.00018
  • Valentine, J. S., & Hart, P. J. (2003). Misfolded CuZnSOD and amyotrophic lateral sclerosis. Proceedings of the National Academy of Sciences of the United States of America, 100(7), 3617–3622. doi:10.1073/pnas.0730423100
  • Valentine, J. S., Doucette, P. A., & Zittin Potter, S. (2005). Copper–zinc superoxide dismutase and amyotrophic lateral sclerosis. Annual Review of Biochemistry, 74, 563–593. doi:10.1146/annurev.biochem.72.121801.161647
  • Watanabe, S., Nagano, S., Duce, J., Kiaei, M., Li, Q. X., Tucker, S. M., … Hayward, L. J. (2007). Increased affinity for copper mediated by cysteine 111 in forms of mutant superoxide dismutase 1 linked to amyotrophic lateral sclerosis. Free Radical Biology & Medicine, 42(10), 1534–1542. doi:10.1016/j.freeradbiomed.2007.02.004
  • Wetzel, R. (1994). Mutations and off-pathway aggregation of proteins. Trends in Biotechnology, 12(5), 193–198. doi:10.1016/0167-7799(94)90082-5
  • Wilkie, A. O. (1994). The molecular basis of genetic dominance. Journal of Medical Genetics, 31(2), 89–98.
  • Zambrano, R., Jamroz, M., Szczasiuk, A., Pujols, J., Kmiecik, S., & Ventura, S. (2015). AGGRESCAN3D (A3D): Server for prediction of aggregation properties of protein structures. Nucleic Acids Research, 43(W1), W306–W313. doi:10.1093/nar/gkv359
  • Zhang, T., Faraggi, E., Li, Z., & Zhou, Y. (2013). Intrinsically semi-disordered state and its role in induced folding and protein aggregation. Cell Biochemistry and Biophysics, 67, 1193–1205. doi:10.1007/s12013-013-9638-0
  • Zhang, Z., Miteva, M. A., Wang, L., & Alexov, E. (2012). Analyzing effects of naturally occurring missense mutations. Computational and Mathematical Methods in Medicine, 2012, 805827doi:10.1155/2012/805827

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.