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Research Articles

Experiment and molecular dynamics simulations reveal proanthocyanidin B2 and B3 can inhibit prion aggregation by different mechanisms

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Pages 2424-2436 | Received 28 Dec 2022, Accepted 14 Apr 2023, Published online: 05 May 2023

References

  • Aguzzi, A. (2001). Recent developments in the pathogenesis, diagnosis, and therapy of prion diseases. Dialogues in Clinical Neuroscience, 3(1), 25–36. https://doi.org/10.31887/DCNS.2001.3.1/aaguzzi
  • Aguzzi, A., & Calella, A. M. (2009). Prions: Protein aggregation and infectious diseases. Physiological Reviews, 89(4), 1105–1152. https://doi.org/10.1152/physrev.00006.2009
  • Amadei, A., Linssen, A. B., & Berendsen, H. J. (1993). Essential dynamics of proteins. Proteins, 17(4), 412–425. https://doi.org/10.1002/prot.340170408
  • Antonyuk, S. V., Trevitt, C. R., Strange, R. W., Jackson, G. S., Sangar, D., Batchelor, M., Cooper, S., Fraser, C., Jones, S., Georgiou, T., Khalili-Shirazi, A., Clarke, A. R., Hasnain, S. S., & Collinge, J. (2009). Crystal structure of human prion protein bound to a therapeutic antibody. Proceedings of the National Academy of Sciences of the United States of America, 106(8), 2554–2558. https://doi.org/10.1073/pnas.0809170106
  • Bai, C., Lin, D., Mo, Y., Lei, J., Sun, Y., Xie, L., Yang, X., & Wei, G. (2019). Influence of fullerenol on hIAPP aggregation: Amyloid inhibition and mechanistic aspects. Physical Chemistry Chemical Physics: PCCP, 21(7), 4022–4031. https://doi.org/10.1039/c8cp07501h
  • Baral, P. K., Swayampakula, M., Rout, M. K., Kav, N. N., Spyracopoulos, L., Aguzzi, A., & James, M. N. (2014). Structural basis of prion inhibition by phenothiazine compounds. Structure (London, England: 1993), 22(2), 291–303. https://doi.org/10.1016/j.str.2013.11.009
  • Baskakov, I. V. (2004). Autocatalytic conversion of recombinant prion proteins displays a species barrier. The Journal of Biological Chemistry, 279(9), 7671–7677. https://doi.org/10.1074/jbc.M310594200
  • Baskakov, I. V., Legname, G., Prusiner, S. B., & Cohen, F. E. (2001). Folding of prion protein to its native α-helical conformation is under kinetic control. The Journal of Biological Chemistry, 276(23), 19687–19690. https://doi.org/10.1074/jbc.C100180200
  • Bayly, C. I., Cieplak, P., Cornell, W. D., & Kollman, P. A. (1993). A well-behaved electrostatic potential based method using charge restraints for deriving atomic charges: The RESP model. The Journal of Physical Chemistry, 97(40), 10269–10280. https://doi.org/10.1021/j100142a004
  • Bocharova, O. V., Breydo, L., Parfenov, A. S., Salnikov, V. V., & Baskakov, I. V. (2005). In vitro conversion of full-length mammalian prion protein produces amyloid form with physical properties of PrP(Sc). Journal of Molecular Biology, 346(2), 645–659. https://doi.org/10.1016/j.jmb.2004.11.068
  • Bonda, D. J., Manjila, S., Mehndiratta, P., Khan, F., Miller, B. R., Onwuzulike, K., Puoti, G., Cohen, M. L., Schonberger, L. B., & Cali, I. (2016). Human prion diseases: Surgical lessons learned from iatrogenic prion transmission. Neurosurgical Focus, 41(1), E10. https://doi.org/10.3171/2016.5.Focus15126
  • Bram, Y., Lampel, A., Shaltiel-Karyo, R., Ezer, A., Scherzer-Attali, R., Segal, D., & Gazit, E. (2015). Monitoring and targeting the initial dimerization stage of amyloid self-assembly. Angewandte Chemie (International ed. in English), 54(7), 2062–2067. https://doi.org/10.1002/anie.201408744
  • Calzolai, L., & Zahn, R. (2003). Influence of pH on NMR structure and stability of the human prion protein globular domain. The Journal of Biological Chemistry, 278(37), 35592–35596. https://doi.org/10.1074/jbc.M303005200
  • De Simone, A., Dodson, G. G., Verma, C. S., Zagari, A., & Fraternali, F. (2005). Prion and water: Tight and dynamical hydration sites have a key role in structural stability. Proceedings of the National Academy of Sciences of the United States of America, 102(21), 7535–7540. https://doi.org/10.1073/pnas.0501748102
  • Essmann, U., Perera, L., Berkowitz, M. L., Darden, T., Lee, H., & Pedersen, L. G. (1995). A smooth particle mesh Ewald method. Journal of Chemical Physics. 103(19), 8577–8593. https://doi.org/10.1063/1.470117
  • Feig, M., Karanicolas, J., & Brooks, C. L. 3rd (2004). MMTSB Tool Set: Enhanced sampling and multiscale modeling methods for applications in structural biology. Journal of Molecular Graphics & Modelling, 22(5), 377–395. https://doi.org/10.1016/j.jmgm.2003.12.005
  • Frid, P., Anisimov, S. V., & Popovic, N. (2007). Congo red and protein aggregation in neurodegenerative diseases. Brain Research Reviews, 53(1), 135–160. https://doi.org/10.1016/j.brainresrev.2006.08.001
  • Frishman, D., & Argos, P. (1995). Knowledge-based protein secondary structure assignment. Proteins, 23(4), 566–579. https://doi.org/10.1002/prot.340230412
  • Gambetti, P., Cali, I., Notari, S., Kong, Q., Zou, W. Q., & Surewicz, W. K. (2011). Molecular biology and pathology of prion strains in sporadic human prion diseases. Acta Neuropathologica, 121(1), 79–90. https://doi.org/10.1007/s00401-010-0761-3
  • Hornak, V., Abel, R., Okur, A., Strockbine, B., Roitberg, A., & Simmerling, C. (2006). Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins, 65(3), 712–725. https://doi.org/10.1002/prot.21123
  • Hosokawa-Muto, J., Kamatari, Y. O., Nakamura, H. K., & Kuwata, K. (2009). Variety of antiprion compounds discovered through an in silico screen based on cellular-form prion protein structure: Correlation between antiprion activity and binding affinity. Antimicrobial Agents and Chemotherapy, 53(2), 765–771. https://doi.org/10.1128/aac.01112-08
  • Hou, T., Wang, J., Li, Y., & Wang, W. (2011). Assessing the performance of the MM/PBSA and MM/GBSA methods. 1. The accuracy of binding free energy calculations based on molecular dynamics simulations. Journal of Chemical Information and Modeling, 51(1), 69–82. https://doi.org/10.1021/ci100275a
  • Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD: Visual molecular dynamics. Journal of Molecular Graphics, 14(1), 33–38. https://doi.org/10.1016/0263-7855(96)00018-5
  • Hyeon, J. W., Choi, J., Kim, S. Y., Govindaraj, R. G., Jam Hwang, K., Lee, Y. S., An, S. S., Lee, M. K., Joung, J. Y., No, K. T., & Lee, J. (2015). Discovery of novel anti-prion compounds using in silico and in vitro approaches. Scientific Reports, 5, 14944. https://doi.org/10.1038/srep14944
  • Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., & Klein, M. L. (1983). Comparison of simple potential functions for simulating liquid water. Journal of Chemical Physics. 79(2), 926–935. https://doi.org/10.1063/1.445869
  • Knaus, K. J., Morillas, M., Swietnicki, W., Malone, M., Surewicz, W. K., & Yee, V. C. (2001). Crystal structure of the human prion protein reveals a mechanism for oligomerization. Nature Structural Biology, 8(9), 770–774. https://doi.org/10.1038/nsb0901-770
  • Kuwata, K., Nishida, N., Matsumoto, T., Kamatari, Y. O., Hosokawa-Muto, J., Kodama, K., Nakamura, H. K., Kimura, K., Kawasaki, M., Takakura, Y., Shirabe, S., Takata, J., Kataoka, Y., & Katamine, S. (2007). Hot spots in prion protein for pathogenic conversion. Proceedings of the National Academy of Sciences of the United States of America, 104(29), 11921–11926. https://doi.org/10.1073/pnas.0702671104
  • Lee, J., & Chang, I. (2019). Structural insight into conformational change in prion protein by breakage of electrostatic network around H187 due to its protonation. Scientific Reports, 9(1), 19305. https://doi.org/10.1038/s41598-019-55808-1
  • Li, L., Zhu, Y., Zhou, S., An, X., Zhang, Y., Bai, Q., He, Y. X., Liu, H., & Yao, X. (2017). Experimental and theoretical insights into the inhibition mechanism of prion fibrillation by resveratrol and its derivatives. ACS Chemical Neuroscience, 8(12), 2698–2707. https://doi.org/10.1021/acschemneuro.7b00240
  • Liu, T., & Bitan, G. (2012). Modulating self-assembly of amyloidogenic proteins as a therapeutic approach for neurodegenerative diseases: Strategies and mechanisms. ChemMedChem. 7(3), 359–374. https://doi.org/10.1002/cmdc.201100585
  • Lou, Z., Wang, B., Guo, C., Wang, K., Zhang, H., & Xu, B. (2015). Molecular-level insights of early-stage prion protein aggregation on mica and gold surface determined by AFM imaging and molecular simulation. Colloids and Surfaces. B, Biointerfaces, 135, 371–378. https://doi.org/10.1016/j.colsurfb.2015.07.053
  • Mizuno, M., Mori, K., Misawa, T., Takaki, T., Demizu, Y., Shibanuma, M., & Fukuhara, K. (2019). Inhibition of β-amyloid-induced neurotoxicity by planar analogues of procyanidin B3. Bioorganic & Medicinal Chemistry Letters, 29(18), 2659–2663. https://doi.org/10.1016/j.bmcl.2019.07.038
  • Ning, L., Guo, J., Jin, N., Liu, H., & Yao, X. (2014). The role of Cys179-Cys214 disulfide bond in the stability and folding of prion protein: Insights from molecular dynamics simulations. Journal of Molecular Modeling, 20(2), 2106. https://doi.org/10.1007/s00894-014-2106-y
  • Pagadala, N. S., Syed, K., & Bhat, R. (2017). In silico strategies on prion pathogenic conversion and inhibition from PrP(C) -PrP(Sc). Expert Opinion on Drug Discovery, 12(3), 241–248. https://doi.org/10.1080/17460441.2017.1287171
  • Pan, K. M., Baldwin, M., Nguyen, J., Gasset, M., Serban, A., Groth, D., Mehlhorn, I., Huang, Z., Fletterick, R. J., & Cohen, F. E. &. (1993). Conversion of alpha-helices into beta-sheets features in the formation of the scrapie prion proteins. Proceedings of the National Academy of Sciences of the United States of America, 90(23), 10962–10966. https://doi.org/10.1073/pnas.90.23.10962
  • Puoti, G., Bizzi, A., Forloni, G., Safar, J. G., Tagliavini, F., & Gambetti, P. (2012). Sporadic human prion diseases: Molecular insights and diagnosis. The Lancet. Neurology, 11(7), 618–628. https://doi.org/10.1016/s1474-4422(12)70063-7
  • Ryckaert, J. P., Ciccotti, G., & Berendsen, H. J. C. (1977). Numerical integration of the Cartesian equations of motion of a system with constraints: Molecular dynamics of n-alkanes. Journal of Computational Physics, 23(3), 327–341. https://doi.org/10.1016/0021-9991(77)90098-5
  • Sabareesan, A. T., & Udgaonkar, J. B. (2016). Pathogenic Mutations within the Disordered Palindromic Region of the Prion Protein Induce Structure Therein and Accelerate the Formation of Misfolded Oligomers. Journal of Molecular Biology, 428(20), 3935–3947. https://doi.org/10.1016/j.jmb.2016.08.015
  • Smeriglio, A., Barreca, D., Bellocco, E., & Trombetta, D. (2017). Proanthocyanidins and hydrolysable tannins: Occurrence, dietary intake and pharmacological effects. British Journal of Pharmacology, 174(11), 1244–1262. https://doi.org/10.1111/bph.13630
  • Snow, A. D., Castillo, G. M., Nguyen, B. P., Choi, P. Y., Cummings, J. A., Cam, J., Hu, Q., Lake, T., Pan, W., Kastin, A. J., Kirschner, D. A., Wood, S. G., Rockenstein, E., Masliah, E., Lorimer, S., Tanzi, R. E., & Larsen, L. (2019). The Amazon rain forest plant Uncaria tomentosa (cat’s claw) and its specific proanthocyanidin constituents are potent inhibitors and reducers of both brain plaques and tangles. Scientific Reports, 9(1), 561. https://doi.org/10.1038/s41598-019-38645-0
  • Sun, J., Ma, X., Sun, L., Zhang, Y., Hao, C., & Wang, W. (2023). Inhibitory effects and mechanisms of proanthocyanidins against enterovirus 71 infection. Virus Research, 329, 199098. https://doi.org/10.1016/j.virusres.2023.199098
  • Tompa, P., Tusnády, G. E., Friedrich, P., & Simon, I. (2002). The role of dimerization in prion replication. Biophysical Journal, 82(4), 1711–1718. https://doi.org/10.1016/s0006-3495(02)75523-9
  • 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(9), 1157–1174. https://doi.org/10.1002/jcc.20035
  • Zhou, S., Liu, X., An, X., Yao, X., & Liu, H. (2017). Molecular dynamics simulation study on the binding and stabilization mechanism of antiprion compounds to the "Hot Spot" region of PrP(C). ACS Chemical Neuroscience, 8(11), 2446–2456. https://doi.org/10.1021/acschemneuro.7b00214
  • Zhou, S., Shi, D., Liu, X., Liu, H., & Yao, X. (2016). Protective V127 prion variant prevents prion disease by interrupting the formation of dimer and fibril from molecular dynamics simulations. Scientific Reports, 6, 21804. https://doi.org/10.1038/srep21804

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