Molecular Modeling of Protein Corona Formation and Its Interactions with Nanoparticles and Cell Membranes for Nanomedicine Applications
Abstract
:1. Introduction
2. Conformation, Binding Site and Strength of Plasma Proteins on the Nanoparticle
2.1. Gold Nanoparticles
2.2. Silver Nanoparticles
2.3. Carbon Nanomaterials
2.4. Polymer-Grafted Nanoparticles
2.5. Others
3. Competitive Adsorption and Desorption of Plasma Proteins on Nanoparticle Surfaces
4. Interactions between the Protein Corona-Particle Complex and Lipid Membrane
5. Conclusions
Funding
Institutional Review Board Statement
Informed Consent Statement
Conflicts of Interest
References
- Segura, T.; Shea, L.D. Materials for non-viral gene delivery. Annu. Rev. Mater. Res. 2001, 31, 25–46. [Google Scholar] [CrossRef]
- Ferrari, M. Cancer nanotechnology: Opportunities and challenges. Nat. Rev. Cancer 2005, 5, 161–171. [Google Scholar] [CrossRef]
- Rolland, A.P. From genes to gene medicines: Recent advances in nonviral gene delivery. Crit. Rev. Ther. Drug Carr. Syst. 1998, 15, 143–198. [Google Scholar] [CrossRef]
- Davis, M.E. Non-viral gene delivery systems. Curr. Opin. Biotechnol. 2002, 13, 128–131. [Google Scholar] [CrossRef]
- Torchilin, V.P. Micellar nanocarriers: Pharmaceutical perspectives. Pharm. Res. 2007, 24, 1–16. [Google Scholar] [CrossRef]
- Nel, A.; Xia, T.; Madler, L.; Li, N. Toxic potential of materials at the nanolevel. Science 2006, 311, 622–627. [Google Scholar] [CrossRef] [Green Version]
- Popielarski, S.R.; Pun, S.H.; Davis, M.E. A nanoparticle-based model delivery system to guide the rational design of gene delivery to the liver. 1. Synthesis and characterization. Bioconjugate Chem. 2005, 16, 1063–1070. [Google Scholar] [CrossRef]
- Luo, D.; Haverstick, K.; Belcheva, N.; Han, E.; Saltzman, W.M. Poly(ethylene glycol)-conjugated pamam dendrimer for biocompatible, high-efficiency DNA delivery. Macromolecules 2002, 35, 3456–3462. [Google Scholar] [CrossRef]
- Liu, Z.; Robinson, J.T.; Sun, X.; Dai, H. Pegylated nanographene oxide for delivery of water-insoluble cancer drugs. J. Am. Chem. Soc. 2008, 130, 10876–10877. [Google Scholar] [CrossRef] [Green Version]
- Heinz, H.; Pramanik, C.; Heinz, O.; Ding, Y.; Mishra, R.K.; Marchon, D.; Flatt, R.J.; Estrela-Lopis, I.; Llop, J.; Moya, S.; et al. Nanoparticle decoration with surfactants: Molecular interactions, assembly, and applications. Surf. Sci. Rep. 2017, 72, 1–58. [Google Scholar] [CrossRef]
- Cedervall, T.; Lynch, I.; Lindman, S.; Berggård, T.; Thulin, E.; Nilsson, H.; Dawson, K.A.; Linse, S. Understanding the nanoparticle-protein corona using methods to quntify exchange rates and affinities of proteins for nanoparticles. Proc. Natl. Acad. Sci. USA 2007, 104, 2050–2055. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ke, P.C.; Lin, S.; Parak, W.J.; Davis, T.P.; Caruso, F. A decade of the protein corona. ACS Nano 2017, 11, 11773–11776. [Google Scholar] [CrossRef] [PubMed]
- Schöttler, S.; Becker, G.; Winzen, S.; Steinbach, T.; Mohr, K.; Landfester, K.; Mailänder, V.; Wurm, F.R. Protein adsorption is required for stealth effect of poly(ethylene glycol)- and poly(phosphoester)-coated nanocarriers. Nat. Nanotechnol. 2016, 11, 372–377. [Google Scholar] [CrossRef]
- Schöttler, S.; Landfester, K.; Mailänder, V. Controlling the stealth effect of nanocarriers through understanding the protein corona. Angew. Chem. Int. Ed. 2016, 55, 8806–8815. [Google Scholar] [CrossRef]
- Nguyen, V.H.; Lee, B.J. Protein corona: A new approach for nanomedicine design. Int. J. Nanomed. 2017, 12, 3137–3151. [Google Scholar] [CrossRef] [Green Version]
- Walkey, C.D.; Chan, W.C.W. Understanding and controlling the interaction of nanomaterials with proteins in a physiological environment. Chem. Soc. Rev. 2012, 41, 2780–2799. [Google Scholar] [CrossRef]
- Hellstrand, E.; Lynch, I.; Andersson, A.; Drakenberg, T.; Dahlbäck, B.; Dawson, K.A.; Linse, S.; Cedervall, T. Complete high-density lipoproteins in nanoparticle corona. FEBS J. 2009, 276, 3372–3381. [Google Scholar] [CrossRef]
- Liu, N.; Tang, M.; Ding, J. The interaction between nanoparticles-protein corona complex and cells and its toxic effect on cells. Chemosphere 2020, 245, 125624. [Google Scholar] [CrossRef]
- Zhdanov, V.P. Formation of a protein corona around nanoparticles. Curr. Opin. Colloid Interface Sci. 2019, 41, 95–103. [Google Scholar] [CrossRef]
- Wang, L.; Li, J.; Pan, J.; Jiang, X.; Ji, Y.; Li, Y.; Qu, Y.; Zhao, Y.; Wu, X.; Chen, C. Revealing the binding structure of the protein corona on gold nanorods using synchrotron radiation-based techniques: Understanding the reduced damage in cell membranes. J. Am. Chem. Soc. 2013, 135, 17359–17368. [Google Scholar] [CrossRef]
- Ramezani, F.; Rafii-Tabar, H. An in-depth view of human serum albumin corona on gold nanoparticles. Mol. Biosyst. 2015, 11, 454–462. [Google Scholar] [CrossRef]
- Tavanti, F.; Pedone, A.; Menziani, M.C. A closer look into the ubiquitin corona on gold nanoparticles by computational studies. New J. Chem. 2015, 39, 2474–2482. [Google Scholar] [CrossRef]
- Shao, Q.; Hall, C.K. Protein adsorption on nanoparticles: Model development using computer simulation. J. Phys. Condens. Matter 2016, 28, 414019. [Google Scholar] [CrossRef] [Green Version]
- Shao, Q.; Hall, C.K. Allosteric effects of gold nanoparticles on human serum albumin. Nanoscale 2017, 9, 380–390. [Google Scholar] [CrossRef] [Green Version]
- Yang, J.; Wang, B.; You, Y.; Chang, W.J.; Tang, K.; Wang, Y.C.; Zhang, W.; Ding, F.; Gunasekaran, S. Probing the modulated formation of gold nanoparticles-beta-lactoglobulin corona complexes and their applications. Nanoscale 2017, 9, 17758–17769. [Google Scholar] [CrossRef] [PubMed]
- Tollefson, E.J.; Allen, C.R.; Chong, G.; Zhang, X.; Rozanov, N.D.; Bautista, A.; Cerda, J.J.; Pedersen, J.A.; Murphy, C.J.; Carlson, E.E.; et al. Preferential binding of cytochrome c to anionic ligand-coated gold nanoparticles: A complementary computational and experimental approach. ACS Nano 2019, 13, 6856–6866. [Google Scholar] [CrossRef] [PubMed]
- Power, D.; Rouse, I.; Poggio, S.; Brandt, E.; Lopez, H.; Lyubartsev, A.; Lobaskin, V. A multiscale model of protein adsorption on a nanoparticle surface. Model. Simul. Mater. Sci. Eng. 2019, 27, 084003. [Google Scholar] [CrossRef]
- Lu, X.; Xu, P.; Ding, H.M.; Yu, Y.S.; Huo, D.; Ma, Y.Q. Tailoring the component of protein corona via simple chemistry. Nat. Commun. 2019, 10, 4520. [Google Scholar] [CrossRef] [PubMed]
- Taha, M.; Lee, M.J. Influence of the alanine side-chain methyl group on the peptide-gold nanoparticles interactions. J. Mol. Liq. 2020, 302, 112528. [Google Scholar] [CrossRef]
- Jahan Sajib, M.S.; Sarker, P.; Wei, Y.; Tao, X.; Wei, T. Protein corona on gold nanoparticles studied with coarse-grained simulations. Langmuir 2020, 36, 13356–13363. [Google Scholar] [CrossRef] [PubMed]
- Käkinen, A.; Ding, F.; Chen, P.; Mortimer, M.; Kahru, A.; Ke, P.C. Interaction of firefly luciferase and silver nanoparticles and its impact on enzyme activity. Nanotechnology 2013, 24, 345101. [Google Scholar] [CrossRef] [PubMed]
- Ding, F.; Radic, S.; Chen, R.; Chen, P.; Geitner, N.K.; Brown, J.M.; Ke, P.C. Direct observation of a single nanoparticle-ubiquitin corona formation. Nanoscale 2013, 5, 9162–9169. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, R.; Chen, R.; Chen, P.; Wen, Y.; Ke, P.C.; Cho, S.S. Computational and experimental characterizations of silver nanoparticle-apolipoprotein biocorona. J. Phys. Chem. B 2013, 117, 13451–13456. [Google Scholar] [CrossRef] [PubMed]
- Wang, B.; Seabrook, S.A.; Nedumpully-Govindan, P.; Chen, P.; Yin, H.; Waddington, L.; Chandana Epa, V.; Winkler, D.A.; Kirby, J.K.; Ding, F.; et al. Thermostability and reversibility of silver nanoparticle-protein binding. Phys. Chem. Chem. Phys. 2015, 17, 1728–1739. [Google Scholar] [CrossRef] [PubMed]
- Nayak, P.S.; Borah, S.M.; Gogoi, H.; Asthana, S.; Bhatnagar, R.; Jha, A.N.; Jha, S. Lactoferrin adsorption onto silver nanoparticle interface: Implications of corona on protein conformation, nanoparticle cytotoxicity and the formulation adjuvanticity. Chem. Eng. J. 2019, 361, 470–484. [Google Scholar] [CrossRef]
- Ge, C.; Du, J.; Zhao, L.; Wang, L.; Liu, Y.; Li, D.; Yang, Y.; Zhou, R.; Zhao, Y.; Chai, Z.; et al. Binding of blood proteins to carbon nanotubes reduces cytotoxicity. Proc. Natl. Acad. Sci. USA 2011, 108, 16968–16973. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sengupta, B.; Gregory, W.E.; Zhu, J.; Dasetty, S.; Karakaya, M.; Brown, J.M.; Rao, A.M.; Barrows, J.K.; Sarupria, S.; Podila, R. Influence of carbon nanomaterial defects on the formation of protein corona. RSC Adv. 2015, 5, 82395–82402. [Google Scholar] [CrossRef] [Green Version]
- Lee, H. Adsorption of plasma proteins onto pegylated single-walled carbon nanotubes: The effects of protein shape, peg size and grafting density. J. Mol. Graph. Model. 2017, 75, 1–8. [Google Scholar] [CrossRef]
- Lee, H.; Larson, R.G. Adsorption of plasma proteins onto pegylated lipid bilayers: The effect of peg size and grafting density. Biomacromolecules 2016, 17, 1757–1765. [Google Scholar] [CrossRef] [Green Version]
- Settanni, G.; Zhou, J.; Suo, T.; Schöttler, S.; Landfester, K.; Schmid, F.; Mailänder, V. Protein corona composition of poly(ethylene glycol)-and poly (phosphoester)-coated nanoparticles correlates strongly with the amino acid composition of the protein surface. Nanoscale 2017, 9, 2138–2144. [Google Scholar] [CrossRef] [Green Version]
- Settanni, G.; Schäfer, T.; Muhl, C.; Barz, M.; Schmid, F. Poly-sarcosine and poly(ethylene-glycol) interactions with proteins investigated using molecular dynamics simulations. Comput. Struct. Biotechnol. J. 2018, 16, 543–550. [Google Scholar] [CrossRef] [PubMed]
- Lopez, H.; Lobaskin, V. Coarse-grained model of adsorption of blood plasma proteins onto nanoparticles. J. Chem. Phys. 2015, 143. [Google Scholar] [CrossRef] [PubMed]
- Lopez, H.; Brandt, E.G.; Mirzoev, A.; Zhurkin, D.; Lyubartsev, A.; Lobaskin, V. Multiscale Modelling of Bionano Interface. Adv. Exp. Med. Biol. 2017, 947, 173–206. [Google Scholar] [PubMed]
- Yu, G.; Zhou, J. Understanding the curvature effect of silica nanoparticles on lysozyme adsorption orientation and conformation: A mesoscopic coarse-grained simulation study. Phys. Chem. Chem. Phys. 2016, 18, 23500–23507. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wei, S.; Ahlstrom, L.S.; Brooks, C.L. Exploring protein–nanoparticle interactions with coarse-grained protein folding models. Small 2017, 13, 1603748. [Google Scholar] [CrossRef] [Green Version]
- Pilkington, E.H.; Xing, Y.; Wang, B.; Kakinen, A.; Wang, M.; Davis, T.P.; Ding, F.; Ke, P.C. Effects of protein corona on iapp amyloid aggregation, fibril remodelling, and cytotoxicity. Sci. Rep. 2017, 7, 2455. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, X.; Wang, M.; Zhang, D.; Yang, Q.; Liu, T.; Lei, R.; Zhu, S.; Zhao, Y.; Chen, C. Probing adsorption behaviors of bsa onto chiral surfaces of nanoparticles. Small 2018, 14, 1703982. [Google Scholar] [CrossRef]
- Tavakol, M.; Montazeri, A.; Naghdabadi, R.; Hajipour, M.J.; Zanganeh, S.; Caracciolo, G.; Mahmoudi, M. Disease-related metabolites affect protein-nanoparticle interactions. Nanoscale 2018, 10, 7108–7115. [Google Scholar] [CrossRef]
- Wang, B.; Sun, Y.; Davis, T.P.; Ke, P.C.; Wu, Y.; Ding, F. Understanding effects of pamam dendrimer size and surface chemistry on serum protein binding with discrete molecular dynamics simulations. ACS Sustain. Chem. Eng. 2018, 6, 11704–11715. [Google Scholar] [CrossRef]
- Fardanesh, A.; Zibaie, S.; Shariati, B.; Attar, F.; Rouhollah, F.; Akhtari, K.; Shahpasand, K.; Saboury, A.A.; Falahati, M. Amorphous aggregation of tau in the presence of titanium dioxide nanoparticles: Biophysical, computational, and cellular studies. Int. J. Nanomed. 2019, 14, 901–911. [Google Scholar] [CrossRef] [Green Version]
- Moya, C.; Escudero, R.; Malaspina, D.C.; De La Mata, M.; Hernández-Saz, J.; Faraudo, J.; Roig, A. Insights into preformed human serum albumin corona on iron oxide nanoparticles: Structure, effect of particle size, impact on mri efficiency, and metabolization. ACS Appl. Bio Mater. 2019, 2, 3084–3094. [Google Scholar] [CrossRef]
- Derakhshankhah, H.; Hosseini, A.; Taghavi, F.; Jafari, S.; Lotfabadi, A.; Ejtehadi, M.R.; Shahbazi, S.; Fattahi, A.; Ghasemi, A.; Barzegari, E.; et al. Molecular interaction of fibrinogen with zeolite nanoparticles. Sci. Rep. 2019, 9, 1–14. [Google Scholar] [CrossRef] [PubMed]
- Xu, X.; Dzubiella, J. Probing the protein corona around charged macromolecules: Interpretation of isothermal titration calorimetry by binding models and computer simulations. Colloid Polym. Sci. 2020, 298, 747–759. [Google Scholar] [CrossRef]
- Sanchez-Guzman, D.; Giraudon-Colas, G.; Marichal, L.; Boulard, Y.; Wien, F.; Degrouard, J.; Baeza-Squiban, A.; Pin, S.; Renault, J.P.; Devineau, S. In situ analysis of weakly bound proteins reveals molecular basis of soft corona formation. ACS Nano 2020, 14, 9073–9088. [Google Scholar] [CrossRef] [PubMed]
- Qi, Y.; Zhang, T.; Jing, C.; Liu, S.; Zhang, C.; Alvarez, P.J.J.; Chen, W. Nanocrystal facet modulation to enhance transferrin binding and cellular delivery. Nat. Commun. 2020, 11, 1–10. [Google Scholar] [CrossRef] [Green Version]
- Hassanian, M.; Aryapour, H.; Goudarzi, A.; Javan, M.B. Are zinc oxide nanoparticles safe? A structural study on human serum albumin using in vitro and in silico methods. J. Biomol. Struct. Dyn. 2021, 39, 330–335. [Google Scholar] [CrossRef]
- Lee, H. Effects of nanoparticle electrostatics and protein–protein interactions on corona formation: Conformation and hydrodynamics. Small 2020, 16, 1906598. [Google Scholar] [CrossRef]
- Vroman, L. Effect of adsorbed proteins on the wettability of hydrophilic and hydrophobic solids. Nature 1962, 196, 476–477. [Google Scholar] [CrossRef]
- Vilaseca, P.; Dawson, K.A.; Franzese, G. Understanding and modulating the competitive surface-adsorption of proteins through coarse-grained molecular dynamics simulations. Soft Matter 2013, 9, 6978–6985. [Google Scholar] [CrossRef] [Green Version]
- Vilanova, O.; Mittag, J.J.; Kelly, P.M.; Milani, S.; Dawson, K.A.; Rädler, J.O.; Franzese, G. Understanding the kinetics of protein–nanoparticle corona formation. ACS Nano 2016, 10, 10842–10850. [Google Scholar] [CrossRef]
- Tavanti, F.; Pedone, A.; Menziani, M.C. Competitive binding of proteins to gold nanoparticles disclosed by molecular dynamics simulations. J. Phys. Chem. C 2015, 119, 22172–22180. [Google Scholar] [CrossRef]
- Tavanti, F.; Pedone, A.; Menziani, M.C. Multiscale molecular dynamics simulation of multiple protein adsorption on gold nanoparticles. Int. J. Mol. Sci. 2019, 20, 3539. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hu, G.; Jiao, B.; Shi, X.; Valle, R.P.; Fan, Q.; Zuo, Y.Y. Physicochemical properties of nanoparticles regulate translocation across pulmonary surfactant monolayer and formation of lipoprotein corona. ACS Nano 2013, 7, 10525–10533. [Google Scholar] [CrossRef] [PubMed]
- Ding, H.-M.; Ma, Y.-Q. Computer simulation of the role of protein corona in cellular delivery of nanoparticles. Biomaterials 2014, 35, 8703–8710. [Google Scholar] [CrossRef] [PubMed]
- Duan, G.; Kang, S.G.; Tian, X.; Garate, J.A.; Zhao, L.; Ge, C.; Zhou, R. Protein corona mitigates the cytotoxicity of graphene oxide by reducing its physical interaction with cell membrane. Nanoscale 2015, 7, 15214–15224. [Google Scholar] [CrossRef] [Green Version]
- Lee, H. Effect of protein corona on nanoparticle–lipid membrane binding: The binding strength and dynamics. Langmuir 2021, 37, 3751–3760. [Google Scholar] [CrossRef]
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Lee, H. Molecular Modeling of Protein Corona Formation and Its Interactions with Nanoparticles and Cell Membranes for Nanomedicine Applications. Pharmaceutics 2021, 13, 637. https://doi.org/10.3390/pharmaceutics13050637
Lee H. Molecular Modeling of Protein Corona Formation and Its Interactions with Nanoparticles and Cell Membranes for Nanomedicine Applications. Pharmaceutics. 2021; 13(5):637. https://doi.org/10.3390/pharmaceutics13050637
Chicago/Turabian StyleLee, Hwankyu. 2021. "Molecular Modeling of Protein Corona Formation and Its Interactions with Nanoparticles and Cell Membranes for Nanomedicine Applications" Pharmaceutics 13, no. 5: 637. https://doi.org/10.3390/pharmaceutics13050637
APA StyleLee, H. (2021). Molecular Modeling of Protein Corona Formation and Its Interactions with Nanoparticles and Cell Membranes for Nanomedicine Applications. Pharmaceutics, 13(5), 637. https://doi.org/10.3390/pharmaceutics13050637