Protein Binding Leads to Reduced Stability and Solvated Disorder in the Polystyrene Nanoparticle Corona
Radha P. Somarathne
Department of Chemistry, Mississippi State University, Mississippi State, MS, 39762 USA
Search for more papers by this authorDhanush L. Amarasekara
Department of Chemistry, Mississippi State University, Mississippi State, MS, 39762 USA
Search for more papers by this authorChathuri S. Kariyawasam
Department of Chemistry, Mississippi State University, Mississippi State, MS, 39762 USA
Search for more papers by this authorHarley A. Robertson
Department of Chemistry, Mississippi State University, Mississippi State, MS, 39762 USA
Search for more papers by this authorRailey Mayatt
Department of Chemistry, Mississippi State University, Mississippi State, MS, 39762 USA
Search for more papers by this authorSteven R. Gwaltney
Department of Chemistry, Mississippi State University, Mississippi State, MS, 39762 USA
Search for more papers by this authorCorresponding Author
Nicholas C. Fitzkee
Department of Chemistry, Mississippi State University, Mississippi State, MS, 39762 USA
E-mail: [email protected]
Search for more papers by this authorRadha P. Somarathne
Department of Chemistry, Mississippi State University, Mississippi State, MS, 39762 USA
Search for more papers by this authorDhanush L. Amarasekara
Department of Chemistry, Mississippi State University, Mississippi State, MS, 39762 USA
Search for more papers by this authorChathuri S. Kariyawasam
Department of Chemistry, Mississippi State University, Mississippi State, MS, 39762 USA
Search for more papers by this authorHarley A. Robertson
Department of Chemistry, Mississippi State University, Mississippi State, MS, 39762 USA
Search for more papers by this authorRailey Mayatt
Department of Chemistry, Mississippi State University, Mississippi State, MS, 39762 USA
Search for more papers by this authorSteven R. Gwaltney
Department of Chemistry, Mississippi State University, Mississippi State, MS, 39762 USA
Search for more papers by this authorCorresponding Author
Nicholas C. Fitzkee
Department of Chemistry, Mississippi State University, Mississippi State, MS, 39762 USA
E-mail: [email protected]
Search for more papers by this authorAbstract
Understanding the conformation of proteins in the nanoparticle corona has important implications in how organisms respond to nanoparticle-based drugs. These proteins coat the nanoparticle surface, and their properties will influence the nanoparticle's interaction with cell targets and the immune system. While some coronas are thought to be disordered, two key unanswered questions are the degree of disorder and solvent accessibility. Here, a model is developed for protein corona disorder in polystyrene nanoparticles of varying size. For two different proteins, it is found that binding affinity decreases as nanoparticle size increases. The stoichiometry of binding, along with changes in the hydrodynamic size, supports a highly solvated, disordered protein corona anchored at a small number of attachment sites. The scaling of the stoichiometry versus nanoparticle size is consistent with disordered polymer dimensions. Moreover, it is found that proteins are destabilized less in the presence of larger nanoparticles, and hydrophobic exposure decreases at lower curvatures. The observations hold for proteins on flat polystyrene surfaces, which have the lowest hydrophobic exposure. The model provides an explanation for previous observations of increased amyloid fibrillation rates in the presence of larger nanoparticles, and it may rationalize how cell receptors can recognize protein disorder in therapeutic nanoparticles.
Conflict of Interest
The authors declare no conflict of interest.
Open Research
Data Availability Statement
The data that support the findings of this study are openly available in Zenodo at https://doi.org/10.5281/zenodo.8105819, reference number 8105819.
Supporting Information
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References
- 1J. Zhu, Z. Zhao, H. Chen, X. Chen, J. Liu, Nanoscale 2022, 14, 8818.
- 2F. Cheng, W. Gu, H. Zhang, C. Song, Y. Zhu, F. Ge, K. Qu, H. Xu, X.-J. Wu, L. Wang, Nanoscale 2022, 14, 8825.
- 3P. Hivare, A. Gangrade, G. Swarup, K. Bhavsar, A. Singh, R. Gupta, P. Thareja, S. Gupta, D. Bhatia, Nanoscale 2022, 14, 8611.
- 4A. Wang, K. Vangala, T. Vo, D. Zhang, N. C. Fitzkee, J. Phys. Chem. C 2014, 118, 8134.
- 5T. Cedervall, I. Lynch, S. Lindman, T. Berggård, E. Thulin, H. Nilsson, K. A. Dawson, S. Linse, Proc. Natl. Acad. Sci. USA 2007, 104, 2050.
- 6M. P. Monopoli, C. Åberg, A. Salvati, K. A. Dawson, Nat. Nanotechnol. 2012, 7, 779.
- 7S. Milani, F. Baldelli Bombelli, A. S. Pitek, K. A. Dawson, J. Rädler, ACS Nano 2012, 6, 2532.
- 8Y.-H. Cheng, C. He, J. E. Riviere, N. A. Monteiro-Riviere, Z. Lin, ACS Nano 2020, 14, 3075.
- 9M. Kurylowicz, H. Paulin, J. Mogyoros, M. Giuliani, J. R. Dutcher, J. R. Soc., Interface 2014, 11, 20130818.
- 10H. Gao, Q. He, Expert Opin. Drug Deliv. 2014, 11, 409.
- 11F. S. M. Tekie, M. Hajiramezanali, P. Geramifar, M. Raoufi, R. Dinarvand, M. Soleimani, F. Atyabi, Sci. Rep. 2020, 10, 9664.
- 12F. Chen, G. Wang, J. I. Griffin, B. Brenneman, N. K. Banda, V. M. Holers, D. S. Backos, L. Wu, S. M. Moghimi, D. Simberg, Nat. Nanotechnol. 2017, 12, 387.
- 13A. Lesniak, F. Fenaroli, M. P. Monopoli, C. Åberg, K. A. Dawson, A. Salvati, ACS Nano 2012, 6, 5845.
- 14D. J. O'Connell, F. B. Bombelli, A. S. Pitek, M. P. Monopoli, D. J. Cahill, K. A. Dawson, Nanoscale 2015, 7, 15268.
- 15J. X. Xu, N. C. Fitzkee, Front. Physiol. 2021, 12, 715419.
- 16O. Vilanova, J. J. Mittag, P. M. Kelly, S. Milani, K. A. Dawson, J. O. Rädler, G. Franzese, ACS Nano 2016, 10, 10842.
- 17J. Ashby, S. Schachermeyer, S. Pan, W. Zhong, Anal. Chem. 2013, 85, 7494.
- 18J. X. Xu, M.d. S. Alom, N. C. Fitzkee, Anal. Chem. 2021, 93, 11982.
- 19Y. Zhang, J. L. Y. Wu, J. Lazarovits, W. C. W. Chan, J. Am. Chem. Soc. 2020, 142, 8827.
- 20J. X. Xu, M.d. S. Alom, R. Yadav, N. C. Fitzkee, Nat. Commun. 2022, 13, 7313.
- 21K. Siriwardana, A. Lacour, D. Zhang, J. Phys. Chem. C 2016, 120, 6900.
- 22S. Sheibani, K. Basu, A. Farnudi, A. Ashkarran, M. Ichikawa, J. F. Presley, K. H. Bui, M. R. Ejtehadi, H. Vali, M. Mahmoudi, Nat. Commun. 2021, 12, 573.
- 23A. A. Shemetov, I. Nabiev, A. Sukhanova, ACS Nano 2012, 6, 4585.
- 24J. E. Gagner, M. D. Lopez, J. S. Dordick, R. W. Siegel, Biomaterials 2011, 32, 7241.
- 25P. Roach, D. Farrar, C. C. Perry, J. Am. Chem. Soc. 2006, 128, 3939.
- 26D.-H. Tsai, F. W. Delrio, A. M. Keene, K. M. Tyner, R. I. Maccuspie, T. J. Cho, M. R. Zachariah, V. A. Hackley, Langmuir 2011, 27, 2464.
- 27M. Lundqvist, I. Sethson, B.-H. Jonsson, Biochemistry 2005, 44, 10093.
- 28P. Sabatino, L. Casella, A. Granata, M. Iafisco, I. G. Lesci, E. Monzani, N. Roveri, J. Colloid Interface Sci. 2007, 314, 389.
- 29J. Wang, X. Chen, M. L. Clarke, Z. Chen, J. Phys. Chem. B 2006, 110, 5017.
- 30H. Pan, M. Qin, W. Meng, Y. Cao, W. Wang, Langmuir 2012, 28, 12779.
- 31X. Wang, R. Lei, L. Li, X. Fei, R. Ju, X. Sun, H. Cao, Q. Zhang, C. Chen, X. Wang, Nanoscale 2021, 13, 20425.
- 32S. Winzen, S. Schoettler, G. Baier, C. Rosenauer, V. Mailaender, K. Landfester, K. Mohr, Nanoscale 2015, 7, 2992.
- 33G. Baier, C. Costa, A. Zeller, D. Baumann, C. Sayer, P. H. H. Araujo, V. Mailänder, A. Musyanovych, K. Landfester, Macromol. Biosci. 2011, 11, 628.
- 34R. P. Somarathne, E. R. Chappell, Y. R. Perera, R. Yadav, J. Y. Park, N. C. Fitzkee, Front. Microbiol. 2021, 12, 658373.
- 35K. E. Woods, Y. R. Perera, M. B. Davidson, C. A. Wilks, D. K. Yadav, N. C. Fitzkee, J. Phys. Chem. C 2016, 120, 27944.
- 36J. X. Xu, M. S. Alom, R. Yadav, N. C. Fitzkee, Nat. Commun. 2022, 13, 7313.
- 37J. X. Xu, M. S. Alom, N. C. Fitzkee, Anal. Chem. 2021, 93, 11982.
- 38S. Zoll, M. Schlag, A. V. Shkumatov, M. Rautenberg, D. I. Svergun, F. Götz, T. Stehle, J. Bacteriol. 2012, 194, 3789.
- 39S. Zoll, B. Pätzold, M. Schlag, F. Götz, H. Kalbacher, T. Stehle, PLoS Pathog. 2010, 6, 1000807.
- 40M. Lundqvist, J. Stigler, G. Elia, I. Lynch, T. Cedervall, K. A. Dawson, Proc. Natl. Acad. Sci. USA 2008, 105, 14265.
- 41J. E. Kohn, I. S. Millett, J. Jacob, B. Zagrovic, T. M. Dillon, N. Cingel, R. S. Dothager, S. Seifert, P. Thiyagarajan, T. R. Sosnick, M. Z. Hasan, V. S. Pande, I. Ruczinski, S. Doniach, K. W. Plaxco, Proc. Natl. Acad. Sci. USA 2004, 101, 12491.
- 42M. K. Frank, F. Dyda, A. Dobrodumov, A. M. Gronenborn, Nat. Struct. Mol. Biol. 2002, 9, 877.
- 43A. L. Becker, N. Welsch, C. Schneider, M. Ballauff, Biomacromolecules 2011, 12, 3936.
- 44C. Yigit, N. Welsch, M. Ballauff, J. Dzubiella, Langmuir 2012, 28, 14373.
- 45S. Winzen, J. C. Schwabacher, J. Müller, K. Landfester, K. Mohr, Biomacromolecules 2016, 17, 3845.
- 46A. Velazquez-Campoy, G. Goñi, J. R. Peregrina, M. Medina, Biophys. J. 2006, 91, 1887.
- 47R. Huang, B. L. T. Lau, Biochim. Biophys. Acta 2016, 1860, 945.
- 48S. P. Boulos, T. A. Davis, J. A. Yang, S. E. Lohse, A. M. Alkilany, L. A. Holland, C. J. Murphy, Langmuir 2013, 29, 14984.
- 49A. Wang, Y. R. Perera, M. B. Davidson, N. C. Fitzkee, J. Phys. Chem. C: Nanomater Interfaces 2016, 120, 24231.
- 50X. Cao, Y. Han, F. Li, Z. Li, D. J. Mcclements, L. He, E. A. Decker, B. Xing, H. Xiao, NanoImpact 2019, 13, 37.
- 51C. F. Quinn, M. C. Carpenter, M. L. Croteau, D. E. Wilcox, in Methods in Enzymology (Ed: A. L. Feig), Academic Press, Cambridge, MA, 2016, pp. 3–21.
- 52D. Sahu, M. Bastidas, C. W. Lawrence, W. G. Noid, S. A. Showalter, in Methods in Enzymology (Ed: A. L. Feig), Academic Press, Cambridge, MA, 2016, pp. 23–45.
- 53S. Link, M. A. El-Sayed, J. Phys. Chem. B 1999, 103, 4212.
- 54N. C. Fitzkee, G. D. Rose, Proc. Natl. Acad. Sci. USA 2004, 101, 12497.
- 55D. K. Wilkins, S. B. Grimshaw, V. Receveur, C. M. Dobson, J. A. Jones, L. J. Smith, Biochemistry 1999, 38, 16424.
- 56B. Hammouda, in Polymer Characteristics, Springer, Berlin, Heidelberg, 1993, pp. 87.
10.1007/BFb0025862 Google Scholar
- 57H. Hofmann, A. Soranno, A. Borgia, K. Gast, D. Nettels, B. Schuler, Proc. Natl. Acad. Sci. USA 2012, 109, 16155.
- 58C. N. Pace, K. L. Shaw, Proteins 2000, 4, 1.
- 59W. Shang, J. H. Nuffer, J. S. Dordick, R. W. Siegel, Nano Lett. 2007, 7, 1991.
- 60J. K. Myers, C. Nick Pace, J. Martin Scholtz, Protein Sci. 1995, 4, 2138.
- 61W. C. Johnson, Proteins: Struct., Funct., Bioinf. 1990, 7, 205.
- 62N. J. Greenfield, Nat. Protoc. 2006, 1, 2876.
- 63C. C. Fleischer, C. K. Payne, J. Phys. Chem. B 2014, 118, 14017.
- 64L. Treuel, M. Malissek, J. S. Gebauer, R. Zellner, ChemPhysChem 2010, 11, 3093.
- 65A. J. Guliyeva, O. K. Gasymov, Biochem. Biophys. Rep. 2020, 24, 100843.
- 66Y. R. Perera, J. X. Xu, D. L. Amarasekara, A. C. Hughes, I. Abbood, N. C. Fitzkee, Molecules 2021, 26, 5788.
- 67Y. Hunashal, C. Cantarutti, S. Giorgetti, L. Marchese, F. Fogolari, G. Esposito, Molecules 2020, 25, 5187.
- 68M. D'onofrio, F. Munari, M. Assfalg, Molecules 2020, 25, 5625.
- 69F. Cañaveras, R. Madueño, J. M. Sevilla, M. Blázquez, T. Pineda, J. Phys. Chem. C 2012, 116, 10430.
- 70T. Sen, S. Mandal, S. Haldar, K. Chattopadhyay, A. Patra, J. Phys. Chem. C 2011, 115, 24037.
- 71C. Loos, T. Syrovets, A. Musyanovych, V. Mailänder, K. Landfester, G. U. Nienhaus, T. Simmet, Beilstein J. Nanotechnol. 2014, 5, 2403.
- 72L. Suresh, J. Y. Walz, J. Colloid Interface Sci. 1997, 196, 177.
- 73A. Morrone, R. Giri, R. D. Toofanny, C. Travaglini-Allocatelli, M. Brunori, V. Daggett, S. Gianni, Biophys. J. 2011, 101, 2053.
- 74M. Miriani, I. Eberini, S. Iametti, P. Ferranti, C. Sensi, F. Bonomi, Proteins: Struct., Funct., Bioinf. 2014, 82, 1272.
- 75H. Xiao, B. Huang, G. Yao, W. Kang, S. Gong, H. Pan, Y.i Cao, J. Wang, J. Zhang, W. Wang, Sci. China Phys. Mech. Astron. 2018, 61, 038711.
10.1007/s11433-017-9124-3 Google Scholar
- 76R. L. Baldwin, G. D. Rose, Curr. Opin. Struct. Biol. 2013, 23, 4.
- 77Y. Zhang, L. B. Casabianca, J. Phys. Chem. Lett. 2018, 9, 6921.
- 78H. Xu, L. B. Casabianca, Sci. Rep. 2020, 10, 12351.
- 79M. Xie, A. L. Hansen, J. Yuan, R. Brüschweiler, J. Phys. Chem. C 2016, 120, 24463.
- 80M. Xie, D.-W. Li, J. Yuan, A. L. Hansen, R. Brüschweiler, Chem. – Eur. J. 2018, 24, 16997.
- 81T. Dos Santos, J. Varela, I. Lynch, A. Salvati, K. A. Dawson, PLoS One 2011, 6, 24438.
- 82O. Lunov, T. Syrovets, C. Loos, J. Beil, M. Delacher, K. Tron, G. U. Nienhaus, A. Musyanovych, V. Mailänder, K. Landfester, T. Simmet, ACS Nano 2011, 5, 1657.
- 83C. Cabaleiro-Lago, O. Szczepankiewicz, S. Linse, Langmuir 2012, 28, 1852.
- 84M. Mahmoudi, H. R. Kalhor, S. Laurent, I. Lynch, Nanoscale 2013, 5, 2570.
- 85J. Luo, S. K. T. S. Wärmländer, C.-H. Yu, K. Muhammad, A. Gräslund, J. Pieter Abrahams, Nanoscale 2014, 6, 6720.
- 86Q. Ma, G. Wei, X. Yang, Nanoscale 2013, 5, 10397.
- 87H. Yang, M. Wang, Y. Zhang, X. Liu, S. Yu, Y. Guo, S. Yang, L. Yang, Int. J. Biol. Macromol. 2019, 135, 1114.
- 88C. Cabaleiro-Lago, F. Quinlan-Pluck, I. Lynch, K. A. Dawson, S. Linse, ACS Chem. Neurosci. 2010, 1, 279.
- 89Y. Chen, Q. Liu, F. Yang, H. Yu, Y. Xie, W. Yao, Colloids Surf., B 2022, 218, 112736.
- 90J. X. Xu, M. S. Alom, R. Yadav, N. C. Fitzkee, 2022, 2022.
- 91T. H. Scheuermann, C. A. Brautigam, Methods 2015, 76, 87.
- 92V. H. Le, R. Buscaglia, J. B. Chaires, E. A. Lewis, Anal. Biochem. 2013, 434, 233.
- 93G. R. Grimsley, B. M. P. Huyghues-Despointes, C. N. Pace, J. M. Scholtz, CSH Protoc 2006, 2006, prot4241.
- 94S. Jo, T. Kim, V. G. Iyer, W. Im, J. Comput. Chem. 2008, 29, 1859.
- 95Y. K. Choi, S.-J. Park, S. Park, S. Kim, N. R. Kern, J. Lee, W. Im, J. Chem. Theory Comput. 2021, 17, 2431.
- 96J. C. Gordon, J. B. Myers, T. Folta, V. Shoja, L. S. Heath, A. Onufriev, Nucleic Acids Res. 2005, 33, W368.
- 97D. A. Case, H. M. Aktulga, K. Belfon, I. Y. Ben-Shalom, S. R. Brozell, D. S. Cerutti, T. E. Cheatham III, G. A. Cisneros, V. W. D. Cruzeiro, T. A. Darden, R. E. Duke, G. Giambasu, M. K. Gilson, H. Gohlke, A. W. Goetz, R. Harris, S. Izadi, S. A. Izmailov, C. Jin, K. Kasavajhala, M. C. Kaymak, E. King, A. Kovalenko, T. Kurtzman, T. S. Lee, S. LeGrand, P. Li, C. Lin, J. Liu, T. Luchko, et al., 2021.
- 98C. Tian, K. Kasavajhala, K. A. A. Belfon, L. Raguette, H. Huang, A. N. Migues, J. Bickel, Y. Wang, J. Pincay, Q. Wu, C. Simmerling, J. Chem. Theory Comput. 2020, 16, 528.
- 99X. He, V. H. Man, W. Yang, T.-S. Lee, J. Wang, J. Chem. Phys. 2020, 153, 114502.
- 100W. L. Jorgensen, J. Chandrasekhar, J. D. Madura, R. W. Impey, M. L. Klein, J. Chem. Phys. 1983, 79, 926.
- 101W. Humphrey, A. Dalke, K. Schulten, J. Mol. Graphics 1996, 14, 33.