359
Views
13
CrossRef citations to date
0
Altmetric
Research Articles

Structural heterogeneity in RNA recognition motif 2 (RRM2) of TAR DNA-binding protein 43 (TDP-43): clue to amyotrophic lateral sclerosis

ORCID Icon, ORCID Icon, , &
Pages 357-367 | Received 13 Sep 2019, Accepted 23 Dec 2019, Published online: 22 Jan 2020

References

  • Abraham, M. J., Murtola, T., Schulz, R., Páll, S., Smith, J. C., Hess, B., & Lindahl, E. (2015). GROMACS: High performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX, 1–2, 19–25. doi:10.1016/j.softx.2015.06.001
  • Arai, T., Hasegawa, M., Akiyama, H., Ikeda, K., Nonaka, T., Mori, H., … Oda, T. (2006). TDP-43 is a component of ubiquitin-positive tau-negative inclusions in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Biochemical and Biophysical Research Communications, 351(3), 602–611. piii:S0006-291X(06)02318-7. doi:10.1016/j.bbrc.2006.10.093
  • Austin, J. A., Wright, G. S., Watanabe, S., Grossmann, J. G., Antonyuk, S. V., Yamanaka, K., & Hasnain, S. S. (2014). Disease causing mutants of TDP-43 nucleic acid binding domains are resistant to aggregation and have increased stability and half-life. Proceedings of the National Academy of Sciences, 111(11), 4309–4314. doi:10.1073/pnas.1317317111
  • Berendsen, H. J. C., Grigera, J. R., & Straatsma, T. P. (1987). The missing term in effective pair potentials. The Journal of Physical Chemistry, 91(24), 6269–6271. doi:10.1021/j100308a038
  • Best, R. B., Hummer, G., & Eaton, W. A. (2013). Native contacts determine protein folding mechanisms in atomistic simulations. Proceedings of the National Academy of Sciences, 110(44), 17874–17879. doi:10.1073/pnas.1311599110
  • Camilloni, C., Rocco, A. G., Eberini, I., Gianazza, E., Broglia, R. A., & Tiana, G. (2008). Urea and guanidinium chloride denature protein L in different ways in molecular dynamics simulations. Biophysical Journal, 94(12), 4654–4661. doi:10.1529/biophysj.107.125799
  • Camilloni, C., & Vendruscolo, M. (2014). Statistical mechanics of the denatured state of a protein using replica-averaged metadynamics. Journal of the American Chemical Society, 136(25), 8982–8991. doi:10.1021/ja5027584
  • Darden, T., York, D., & Pedersen, L. (1993). Particle mesh Ewald: An N⋅log(N) method for Ewald sums in large systems. The Journal of Chemical Physics, 98(12), 10089–10092. doi:10.1063/1.464397
  • Day, R., Paschek, D., & Garcia, A. E. (2010). Microsecond simulations of the folding/unfolding thermodynamics of the Trp-cage miniprotein. Proteins: Structure, Function, and Bioinformatics, 78(8), 1889–1899. doi:10.1002/prot.22702
  • Guenther, E. L., Ge, P., Trinh, H., Sawaya, M. R., Cascio, D., Boyer, D. R., … Eisenberg, D. S. (2018). Atomic-level evidence for packing and positional amyloid polymorphism by segment from TDP-43 RRM2. Nature Structural & Molecular Biology, 25(4), 311–319.
  • Hess, B., Bekker, H., Berendsen, H. J., & Fraaije, J. G. (1997). LINCS: A linear constraint solver for molecular simulations. Journal of Computational Chemistry, 18(12), 1463–1472. doi:10.1002/(SICI)1096-987X(199709)18:12<1463::AID-JCC4>3.0.CO;2-H
  • Heyda, J., KožÍšEk, M., Bednárova, L., Thompson, G., Konvalinka, J., VondrášEk, JÍ., & Jungwirth, P., (2011). Urea and guanidinium induced denaturation of a Trp-cage miniprotein. The Journal of Physical Chemistry B, 115((28), 8910–8924. doi:10.1021/jp200790h
  • Igaz, L. M., Kwong, L. K., Chen-Plotkin, A., Winton, M. J., Unger, T. L., Xu, Y., … Lee, V. M-Y. (2009). Expression of TDP-43 C-terminal fragments in vitro recapitulates pathological features of TDP-43 proteinopathies. Journal of Biological Chemistry, 284(13), 8516–8524. doi:10.1074/jbc.M809462200
  • Igaz, L. M., Kwong, L. K., Xu, Y., Truax, A. C., Uryu, K., Neumann, M., … Lee, V. M-Y. (2008). Enrichment of C-terminal fragments in TAR DNA-binding protein-43 cytoplasmic inclusions in brain but not in spinal cord of frontotemporal lobar degeneration and amyotrophic lateral sclerosis. The American Journal of Pathology, 173(1), 182–194. doi:10.2353/ajpath.2008.080003
  • Johnson, B. S., McCaffery, J. M., Lindquist, S., & Gitler, A. D. (2008). A yeast TDP-43 proteinopathy model: Exploring the molecular determinants of TDP-43 aggregation and cellular toxicity. Proceedings of the National Academy of Sciences, 105(17), 6439–6444. doi:10.1073/pnas.0802082105
  • Kabsch, W., & Sander, C. (1983). Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features. Biopolymers, 22(12), 2577–2637. doi:10.1002/bip.360221211
  • Khan, S. H., Prakash, A., Pandey, P., Lynn, A. M., Islam, A., Hassan, M. I., & Ahmad, F. (2019). Protein folding: Molecular dynamics simulations and in vitro studies for probing mechanism of urea- and guanidinium chloride-induced unfolding of horse cytochrome-c. International Journal of Biological Macromolecules, 122, 695–704. pii:S0141-8130(18)34827-X. doi:10.1016/j.ijbiomac.2018.10.186
  • Kiernan, M. C., Vucic, S., Cheah, B. C., Turner, M. R., Eisen, A., Hardiman, O., … Zoing, M. C. (2011). Amyotrophic lateral sclerosis. The Lancet, 377(9769), 942–955. doi:10.1016/S0140-6736(10)61156-7
  • Kumar, V., Islam, A., Hassan, M. I., & Ahmad, F. (2016). Therapeutic progress in amyotrophic lateral sclerosis-beginning to learning. European Journal of Medicinal Chemistry, 121, 903–917. doi:10.1016/j.ejmech.2016.06.017
  • Kumar, V., Pandey, P., Idrees, D., Prakash, A., & Lynn, A. M. (2019). Delineating the effect of mutations on the conformational dynamics of N-terminal domain of TDP-43. Biophysical Chemistry, 250, 106–174. pii:S0301-4622(18)30417-4. doi:10.1016/j.bpc.2019.106174
  • Kumar, V., Prakash, A., & Lynn, A. M. (2018). Alterations in local stability and dynamics of A4V SOD1 in the presence of trifluoroethanol. Biopolymers, 109(3), e23102. doi:10.1002/bip.23102
  • Kumar, V., Prakash, A., Pandey, P., Lynn, A. M., & Hassan, M. I. (2018). TFE-induced local unfolding and fibrillation of SOD1: Bridging the experiment and simulation studies. Biochemical Journal, 475, 1701–1719. doi:10.1042/BCJ20180085
  • Kumar, V., Prakash, A., Tomar, A. K., Srivastava, A., Kundu, B., … Hassan, M. I. (2019). Exploring the aggregation-prone regions from structural domains of human TDP-43. Biochimica Biophysica Acta Proteins and Proteomics, 1867(3), 286–296. pii:S1570-9639(18)30177-8. doi:10.1016/j.bbapap.2018.10.008
  • Le Marchand, T., de Rosa, M., Salvi, N., Sala, B. M., Andreas, L. B., Barbet-Massin, E., … Ricagno, S. (2018). Conformational dynamics in crystals reveal the molecular bases for D76N beta-2 microglobulin aggregation propensity. Nature Communications, 9(1), 1658. doi:10.1038/s41467-018-04078-y
  • Li, Q., Yokoshi, M., Okada, H., & Kawahara, Y. (2015). The cleavage pattern of TDP-43 determines its rate of clearance and cytotoxicity. Nature Communications, 6 (1), 6183. doi:10.1038/ncomms7183
  • Mackness, B. C., Tran, M. T., McClain, S. P., Matthews, C. R., & Zitzewitz, J. A. (2014). Folding of the RNA recognition motif (RRM) domains of the amyotrophic lateral sclerosis (ALS)-linked protein TDP-43 reveals an intermediate state. Journal of Biological Chemistry, 289(12), 8264–8276. doi:10.1074/jbc.M113.542779
  • McGibbon, R. T., Beauchamp, K. A., Harrigan, M. P., Klein, C., Swails, J. M., Hernández, C. X., … Pande, V. S. (2015). MDTraj: A modern open library for the analysis of molecular dynamics trajectories. Biophysical Journal, 109(8), 1528–1532. doi:10.1016/j.bpj.2015.08.015
  • Morgan, B. R., Zitzewitz, J. A., & Massi, F. (2017). Structural rearrangement upon fragmentation of the stability core of the ALS-linked protein TDP-43. Biophysical Journal, 113(3), 540–549. doi:S0006-3495(17)30699-9
  • Neudecker, P., Robustelli, P., Cavalli, A., Walsh, P., Lundstrom, P., Zarrine-Afsar, A., … Kay, L. E. (2012). Structure of an intermediate state in protein folding and aggregation. Science, 336(6079), 362–366. doi:10.1126/science.1214203
  • Neumann, M., Sampathu, D. M., Kwong, L. K., Truax, A. C., Micsenyi, M. C., Chou, T. T., … Lee, V. M.-Y. (2006). Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science, 314(5796), 130–133. pii:314/5796/130. doi:10.1126/science.1134108
  • Pandey, P., Meena, N. K., Prakash, A., Kumar, V., Lynn, A. M., & Ahmad, F. (2019). Characterization of heterogeneous intermediate ensembles on the guanidinium chloride-induced unfolding pathway of beta-lactoglobulin. Journal of Biomolecular Structure and Dynamics, 18, 1–12. doi:10.1080/07391102.2019.1593245
  • Parakh, S., & Atkin, J. D. (2016). Protein folding alterations in amyotrophic lateral sclerosis. Brain Research, 1648(B), 633–649. pii:S0006-8993(16)30203-7. doi:10.1016/j.brainres.2016.04.010
  • Parrinello, M., & Rahman, A. (1980). Crystal structure and pair potentials: A molecular-dynamics study. Physical Review Letters, 45(14), 1196–1199. doi:10.1103/PhysRevLett.45.1196
  • Pasinelli, P., & Brown, R. H. (2006). Molecular biology of amyotrophic lateral sclerosis: Insights from genetics. Nature Reviews Neuroscience, 7(9), 710–723. pii:nrn1971. doi:10.1038/nrn1971
  • Pillai, M., & Jha, S. K. (2019). The folding and aggregation energy landscapes of tethered RRM domains of human TDP-43 are coupled via a metastable molten globule-like oligomer. Biochemistry, 58(6), 608–620. doi:10.1021/acs.biochem.8b01013
  • 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., Idrees, D., Haque, M. A., Islam, A., Ahmad, F., & Hassan, M. I. (2017). GdmCl-induced unfolding studies of human carbonic anhydrase IX: A combined spectroscopic and MD simulation approach. Journal of Biomolecular Structure and Dynamics, 35(6), 1295–1306. doi:10.1080/07391102.2016.1179596
  • Prakash, A., Kumar, V., Meena, N. K., Hassan, M. I., & Lynn, A. M. (2018). Comparative analysis of thermal unfolding simulations of RNA recognition motifs (RRMs) of TAR DNA-binding protein 43 (TDP-43). Journal of Biomolecular Structure and Dynamics, 37(1), 1–17. doi:10.1080/07391102.2017.1422026
  • Prakash, A., Kumar, V., Meena, N. K., & Lynn, A. M. (2018). Elucidation of the structural stability and dynamics of heterogeneous intermediate ensembles in unfolding pathway of the N-terminal domain of TDP-43. RSC Advances, 8(35), 19835–19845. doi:10.1039/C8RA03368D
  • Prakash, A., Kumar, V., Pandey, P., Bharti, D. R., Vishwakarma, P., Singh, R., … Lynn, A. M. (2017). Solvent sensitivity of protein aggregation in Cu, Zn superoxide dismutase: A molecular dynamics simulation study. Journal of Biomolecular Structure and Dynamics, 36(10), 1–39. doi:10.1080/07391102.2017.1364670
  • Tavella, D., Zitzewitz, J. A., & Massi, F. (2018). Characterization of TDP-43 RRM2 partially folded states and their significance to ALS pathogenesis. Biophysical Journal, 115(9), 1673–1680. pii:S0006-3495(18)31063-4. doi:10.1016/j.bpj.2018.09.011
  • Wang, Y-T., Kuo, P-H., Chiang, C-H., Liang, J-R., Chen, Y-R., Wang, S., … Yuan, H. S. (2013). The truncated C-terminal RNA recognition motif of TDP-43 protein plays a key role in forming proteinaceous aggregates. Journal of Biological Chemistry, 288(13), 9049–9057. doi:10.1074/jbc.M112.438564
  • Zacco, E., Martin, S. R., Thorogate, R., & Pastore, A. (2018). The RNA-recognition motifs of TAR DNA-binding protein 43 may play a role in the aberrant self-assembly of the protein. Frontiers in Molecular Neuroscience, 11, 372. doi:10.3389/fnmol.2018.00372.
  • Zhang, Y.-J., Xu, Y.-F., Cook, C., Gendron, T. F., Roettges, P., Link, C. D., … Petrucelli, L. (2009). Aberrant cleavage of TDP-43 enhances aggregation and cellular toxicity. Proceedings of the National Academy of Sciences, 106(18), 7607–7612. doi:10.1073/pnas.0900688106
  • Zhou, R. (2003). Trp-cage: Folding free energy landscape in explicit water. Proceedings of the National Academy of Sciences, 100(23), 13280–13285. doi:10.1073/pnas.2233312100

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.