The Adsorption of P2X2 Receptors Interacting with IgG Antibodies Revealed by Combined AFM Imaging and Mechanical Simulation
Abstract
:1. Introduction
2. Results
3. Discussion
4. Materials and Methods
4.1. Homology Modelling of the P2X2 Receptor
4.2. The Determination of the Initial Favorable Orientation of the Proteins on the Surface
4.3. The Formation of the P2X2 Receptor–Micelle Structure
4.4. The Mechanical Simulation of the Adsorbed Individual Proteins and Complexes via Autodesk Maya 3D
4.5. AFM Imaging of the IgG Antibody, P2X2 Receptor and Receptor–Antibody Complex
4.6. Statistical Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Kwon, K.; Lee, J.; Lee, S.; Ree, M.; Kim, H. Pneumolysin/Plasma Protein Adsorption, Bacterial Adherence, and Cell Adhesion Characteristics of a Cell-Membrane-Mimicking Polymer System. ACS Appl. Biol. Mater. 2022, 5, 2240–2252. [Google Scholar] [CrossRef] [PubMed]
- Kalasin, S.; Santore, M.M. Non-Specific Adhesion on Biomaterial Surfaces Driven by Small Amounts of Protein Adsorption. Colloids Surf. B Biointerfaces 2009, 73, 229–236. [Google Scholar] [CrossRef] [PubMed]
- Avila-Sierra, A.; Moreno, J.A.; Goode, K.; Zhu, T.; Fryer, P.J.; Taylor, A.; Zhang, Z.J. Effects of Structural and Chemical Properties of Surface Coatings on the Adsorption Characteristics of Proteins. Surf. Coat. Technol. 2023, 452, 129054. [Google Scholar] [CrossRef]
- Westphalen, H.; Kalugin, D.; Abdelrasoul, A. Structure, Function, and Adsorption of Highly Abundant Blood Proteins and Its Critical Influence on Hemodialysis Patients: A Critical Review. Biomed. Eng. Adv. 2021, 2, 100021. [Google Scholar] [CrossRef]
- Horbett, T.A.; Brash, J.L. Proteins at Interfaces II; Horbett, T.A., Brash, J.L., Eds.; ACS Symposium Series; American Chemical Society: Washington, DC, USA, 1995; Volume 602, ISBN 9780841233041. [Google Scholar]
- Culp, L.A.; Sukenik, C.N. Glass and Metal Surfaces Derivatized with Self-Assembled Monolayers: Cell Type-Specific Modulation of Fibronectin Adhesion Functions. J. Tissue Cult. Methods 1994, 16, 161–172. [Google Scholar] [CrossRef]
- Rabe, M.; Verdes, D.; Seeger, S. Understanding Protein Adsorption Phenomena at Solid Surfaces. Adv. Colloid Interface Sci. 2011, 162, 87–106. [Google Scholar] [CrossRef] [PubMed]
- Nakanishi, K.; Sakiyama, T.; Imamura, K. On the Adsorption of Proteins on Solid Surfaces, a Common but Very Complicated Phenomenon. J. Biosci. Bioeng. 2001, 91, 233–244. [Google Scholar] [CrossRef] [PubMed]
- Wei, Y.; Thyparambil, A.A.; Latour, R.A. Quantification of the Influence of Protein-Protein Interactions on Adsorbed Protein Structure and Bioactivity. Colloids Surf. B Biointerfaces 2013, 110, 363–371. [Google Scholar] [CrossRef]
- Adam, N.K. The Physics and Chemistry of Surfaces, 2nd ed.; Clarendon Press: Oxford, UK, 1938. [Google Scholar]
- Rothen, A. Films of Protein in Biological Processes. Adv. Protein Chem. 1947, 3, 123–137. [Google Scholar] [CrossRef]
- Cheesman, D.F.; Davies, J.T. Physicochemical and Biological Aspects of Proteins at Interfaces. Adv. Protein Chem. 1954, 9, 439–501. [Google Scholar] [CrossRef]
- Mathé, C.; Devineau, S.; Aude, J.-C.; Lagniel, G.; Chédin, S.; Legros, V.; Mathon, M.-H.; Renault, J.-P.; Pin, S.; Boulard, Y.; et al. Structural Determinants for Protein Adsorption/Non-Adsorption to Silica Surface. PLoS ONE 2013, 8, e81346. [Google Scholar] [CrossRef] [PubMed]
- Apte, J.S.; Gamble, L.J.; Castner, D.G.; Campbell, C.T. Kinetics of Leucine-Lysine Peptide Adsorption and Desorption at -CH3 and -COOH Terminated Alkylthiolate Monolayers. Biointerphases 2010, 5, 97–104. [Google Scholar] [CrossRef] [PubMed]
- Huber, D.L.; Manginell, R.P.; Samara, M.A.; Kim, B.I.; Bunker, B.C. Programmed Adsorption and Release of Proteins in a Microfluidic Device. Science 2003, 301, 352–354. [Google Scholar] [CrossRef] [PubMed]
- Shang, L.; Nienhaus, G.U. In Situ Characterization of Protein Adsorption onto Nanoparticles by Fluorescence Correlation Spectroscopy. Account. Chem. Res. 2017, 50, 387–395. [Google Scholar] [CrossRef]
- Scott, D.N.; Frank, M.J. Adaptive Control of Synaptic Plasticity Integrates Micro- and Macroscopic Network Function. Neuropsychopharmacology 2022, 48, 121–144. [Google Scholar] [CrossRef]
- Manzi, B.M.; Werner, M.; Ivanova, E.P.; Crawford, R.J.; Baulin, V.A. Simulations of Protein Adsorption on Nanostructured Surfaces. Sci. Rep. 2019, 9, 4694. [Google Scholar] [CrossRef]
- Kubala, P.; Batys, P.; Barbasz, J.; Weroński, P.; Cieśla, M. Random Sequential Adsorption: An Efficient Tool for Investigating the Deposition of Macromolecules and Colloidal Particles. Adv. Colloid. Interface Sci. 2022, 306, 102692. [Google Scholar] [CrossRef]
- Kubiak-Ossowska, K.; Mulheran, P.A. Multiprotein Interactions during Surface Adsorption: A Molecular Dynamics Study of Lysozyme Aggregation at a Charged Solid Surface. J. Phys. Chem. B 2011, 115, 8891–8900. [Google Scholar] [CrossRef]
- Javkhlantugs, N.; Bayar, H.; Ganzorig, C.; Ueda, K. Computational Study on the Interactions and Orientation of Monoclonal Human Immunoglobulin G on a Polystyrene Surface. Int. J. Nanomed. 2013, 8, 2487–2496. [Google Scholar] [CrossRef]
- Wei, S.; Knotts IV, T.A. A Coarse Grain Model for Protein-Surface Interactions. J. Chem. Phys. 2013, 139, 4819131. [Google Scholar] [CrossRef]
- Xu, H.; Zhao, X.; Grant, C.; Lu, J.R.; Williams, D.E.; Penfold, J. Orientation of a Monoclonal Antibody Adsorbed at the Solid/Solution Interface: A Combined Study Using Atomic Force Microscopy and Neutron Reflectivity. Langmuir 2006, 22, 6313–6320. [Google Scholar] [CrossRef] [PubMed]
- Wiseman, M.E.; Frank, C.W. Antibody Adsorption and Orientation on Hydrophobic Surfaces. Langmuir 2012, 28, 1765–1774. [Google Scholar] [CrossRef] [PubMed]
- Boshkovikj, V.; Fluke, C.J.; Crawford, R.J.; Ivanova, E.P. Three-Dimensional Visualization of Nanostructured Surfaces and Bacterial Attachment Using Autodesk® Maya®. Sci. Rep. 2014, 4, 4228. [Google Scholar] [CrossRef] [PubMed]
- Castanov, V.; Hassan, S.A.; Shakeri, S.; Vienneau, M.; Zabjek, K.; Richardson, D.; McKee, N.H.; Agur, A.M.R. Muscle Architecture of Vastus Medialis Obliquus and Longus and Its Functional Implications: A Three-dimensional Investigation. Clin. Anat. 2019, 32, 515–523. [Google Scholar] [CrossRef] [PubMed]
- Perry, J.L.; Kuehn, D.P. Three-Dimensional Computer Reconstruction of the Levator Veli Palatini Muscle in Situ Using Magnetic Resonance Imaging. Cleft Palate-Craniofacial J. 2007, 44, 421–423. [Google Scholar] [CrossRef] [PubMed]
- Ravichandiran, M.; Ravichandiran, N.; Ravichandiran, K.; Mckee, N.H.; Richardson, D.; Oliver, M.; Agur, A.M. Neuromuscular Partitioning in the Extensor Carpi Radialis Longus and Brevis Based on Intramuscular Nerve Distribution Patterns: A Three-dimensional Modeling Study. Clin. Anat. 2012, 25, 366–372. [Google Scholar] [CrossRef] [PubMed]
- Brusatori, M.A.; Van Tassel, P.R. A Kinetic Model of Protein Adsorption/Surface-Induced Transition Kinetics Evaluated by the Scaled Particle Theory. J. Colloid Interface Sci. 1999, 219, 333–338. [Google Scholar] [CrossRef]
- Baaden, M. Visualizing Biological Membrane Organization and Dynamics. J. Mol. Biol. 2019, 431, 1889–1919. [Google Scholar] [CrossRef]
- Su, Z.; Wu, Y. Computational Studies of Protein-Protein Dissociation by Statistical Potential and Coarse-Grained Simulations: A Case Study on Interactions between Colicin E9 Endonuclease and Immunity Proteins. Phys. Chem. Chem. Phys. 2019, 21, 2463. [Google Scholar] [CrossRef]
- He, Z.; Paul, F.; Roux, B. A Critical Perspective on Markov State Model Treatments of Protein–Protein Association Using Coarse-Grained Simulations. J. Chem. Phys. 2021, 154, 39144. [Google Scholar] [CrossRef]
- Dhusia, K.; Su, Z.; Wu, Y. Using Coarse-Grained Simulations to Characterize the Mechanisms of Protein–Protein Association. Biomolecules 2020, 10, 1056. [Google Scholar] [CrossRef] [PubMed]
- Oda, M.; Kozono, H.; Morii, H.; Azuma, T. Evidence of Allosteric Conformational Changes in the Antibody Constant Region upon Antigen Binding. Int. Immunol. 2003, 15, 417–426. [Google Scholar] [CrossRef] [PubMed]
- Zhou, C.; Friedt, J.-M.; Angelova, A.; Choi, K.-H.; Laureyn, W.; Frederix, F.; Francis, L.A.; Campitelli, A.; Engelborghs, Y.; Borghs, G. Human Immunoglobulin Adsorption Investigated by Means of Quartz Crystal Microbalance Dissipation, Atomic Force Microscopy, Surface Acoustic Wave, and Surface Plasmon Resonance Techniques. Langmuir 2004, 20, 5870–5878. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Z.; Marie Woys, A.; Hong, K.; Grapentin, C.; Khan, T.A.; Zarraga, I.E.; Wagner, N.J.; Liu, Y. Adsorption of Non-Ionic Surfactant and Monoclonal Antibody on Siliconized Surface Studied by Neutron Reflectometry. J. Colloid Interface Sci. 2021, 584, 429–438. [Google Scholar] [CrossRef] [PubMed]
- Song, D.; Forciniti, D. Effects of Cosolvents and PH on Protein Adsorption on Polystyrene Latex: A Dynamic Light Scattering Study. J. Colloid Interface Sci. 2000, 221, 25–37. [Google Scholar] [CrossRef] [PubMed]
- Džupponová, V.; Žoldák, G. Salt-Dependent Passive Adsorption of IgG1κ-Type Monoclonal Antibodies on Hydrophobic Microparticles. Biophys. Chem. 2021, 275, 106609. [Google Scholar] [CrossRef]
- Giacomelli, C.E.; Bremer, M.G.E.G.; Norde, W. ATR-FTIR Study of IgG Adsorbed on Different Silica Surfaces. J. Colloid Interface Sci. 1999, 220, 13–23. [Google Scholar] [CrossRef]
- Yoshimoto, K.; Nishio, M.; Sugasawa, H.; Nagasaki, Y. Direct Observation of Adsorption-Induced Inactivation of Antibody Fragments Surrounded by Mixed-PEG Layer on a Gold Surface. J. Am. Chem. Soc. 2010, 132, 7982–7989. [Google Scholar] [CrossRef]
- Xu, H.; Lu, J.R.; Williams, D.E. Effect of Surface Packing Density of Interfacially Adsorbed Monoclonal Antibody on the Binding of Hormonal Antigen Human Chorionic Gonadotrophin. J. Phys. Chem. B 2006, 110, 1907–1914. [Google Scholar] [CrossRef]
- Sun, Y.; Estevez, A.; Schlothauer, T.; Wecksler, A.T. Antigen Physiochemical Properties Allosterically Effect the IgG Fc-Region and Fc Neonatal Receptor Affinity. MAbs 2020, 12, 1802135. [Google Scholar] [CrossRef]
- Höger, K.; Mathes, J.; Frieß, W. IgG1 Adsorption to Siliconized Glass Vials—Influence of PH, Ionic Strength, and Nonionic Surfactants. J. Pharm. Sci. 2015, 104, 34–43. [Google Scholar] [CrossRef]
- Kanthe, A.; Ilott, A.; Krause, M.; Zheng, S.; Li, J.; Bu, W.; Bera, M.K.; Lin, B.; Maldarelli, C.; Tu, R.S. No Ordinary Proteins: Adsorption and Molecular Orientation of Monoclonal Antibodies. Sci. Adv. 2021, 7, abg2873. [Google Scholar] [CrossRef]
- Hu, J.; Gao, M.; Wang, Y.; Liu, M.; Wang, J.; Li, J.; Song, Z.; Chen, Y.; Wang, Z. Imaging the Substructures of Individual IgE Antibodies with Atomic Force Microscopy. Langmuir 2019, 35, 14896–14901. [Google Scholar] [CrossRef]
- Rankl, M.; Ruckstuhl, T.; Rabe, M.; Artus, G.R.J.; Walser, A.; Seeger, S. Conformational Reorientation of Immunoglobulin G during Nonspecific Interaction with Surfaces. ChemPhysChem 2006, 7, 837–846. [Google Scholar] [CrossRef]
- Coen, M.C.; Lehmann, R.; Gröning, P.; Bielmann, M.; Galli, C.; Schlapbach, L. Adsorption and Bioactivity of Protein A on Silicon Surfaces Studied by AFM and XPS. J. Colloid Interface Sci. 2001, 233, 180–189. [Google Scholar] [CrossRef]
- Barinov, N.A.; Prokhorov, V.V.; Dubrovin, E.V.; Klinov, D.V. AFM Visualization at a Single-Molecule Level of Denaturated States of Proteins on Graphite. Colloids Surf. B Biointerfaces 2016, 146, 777–784. [Google Scholar] [CrossRef]
- Liu, Y.; Yu, J. Oriented Immobilization of Proteins on Solid Supports for Use in Biosensors and Biochips: A Review. Microchim. Acta 2016, 183, 1–19. [Google Scholar] [CrossRef]
- Singh, N.K.; Pushpavanam, K.; Radhakrishna, M. Tuning Electrostatic Interactions To Control Orientation of GFP Protein Adsorption on Silica Surface. ACS Appl. Biol. Mater. 2023. [Google Scholar] [CrossRef] [PubMed]
- Susini, V.; Sanguinetti, C.; Ursino, S.; Caponi, L.; Franzini, M. Antibody-Antigen Binding Events: The Effects of Antibody Orientation and Antigen Properties on the Immunoassay Sensitivity. In Rapid Antigen Test; Anfossi, L., Ed.; IntechOpen: Rijeka, Croatia, 2023. [Google Scholar] [CrossRef]
- Šali, A.; Blundell, T.L. Comparative Protein Modelling by Satisfaction of Spatial Restraints. J. Mol. Biol. 1993, 234, 779–815. [Google Scholar] [CrossRef]
- Lovell, S.C.; Davis, I.W.; Arendall, W.B.; De Bakker, P.I.W.; Word, J.M.; Prisant, M.G.; Richardson, J.S.; Richardson, D.C. Structure Validation by Cα Geometry: ϕ,ψ and Cβ Deviation. Proteins Struct. Funct. Bioinform. 2003, 50, 437–450. [Google Scholar] [CrossRef] [PubMed]
- Wiederstein, M.; Sippl, M.J. ProSA-Web: Interactive Web Service for the Recognition of Errors in Three-Dimensional Structures of Proteins. Nucleic Acids Res. 2007, 35, 407–410. [Google Scholar] [CrossRef]
- Phillips, J.C.; Hardy, D.J.; Maia, J.D.C.; Stone, J.E.; Ribeiro, J.V.; Bernardi, R.C.; Buch, R.; Fiorin, G.; Hénin, J.; Jiang, W.; et al. Scalable Molecular Dynamics on CPU and GPU Architectures with NAMD. J. Chem. Phys. 2020, 153, 44130. [Google Scholar] [CrossRef]
- Heinz, H.; Lin, T.-J.; Mishra, R.K.; Emami, F.S. Thermodynamically Consistent Force Fields for the Assembly of Inorganic, Organic, and Biological Nanostructures: The INTERFACE Force Field. Langmuir 2013, 29, 1754–1765. [Google Scholar] [CrossRef]
- Martinez, L.; Andrade, R.; Birgin, E.G.; Martínez, J.M. PACKMOL: A Package for Building Initial Configurations for Molecular Dynamics Simulations. J. Comput. Chem. 2009, 30, 2157–2164. [Google Scholar] [CrossRef]
- Morgner, N.; Montenegro, F.; Barrera, N.P.; Robinson, C.V. Mass Spectrometry—From Peripheral Proteins to Membrane Motors. J. Mol. Biol. 2012, 423, 1–13. [Google Scholar] [CrossRef]
- Barrera, N.P.; Ormond, S.J.; Henderson, R.M.; Murrell-Lagnado, R.D.; Edwardson, J.M. Atomic Force Microscopy Imaging Demonstrates That P2X2 Receptors Are Trimers but That P2X6 Receptor Subunits Do Not Oligomerize. J. Biol. Chem. 2005, 280, 10759–10765. [Google Scholar] [CrossRef] [PubMed]
- Carnally, S.M.; Edwardson, J.M.; Barrera, N.P. Imaging the Spatial Orientation of Subunits within Membrane Receptors by Atomic Force Microscopy. Methods Mol. Biol. 2011, 736, 47–60. [Google Scholar] [CrossRef] [PubMed]
Model | Favorable Residues | Unfavorable Residues | Affinity |
---|---|---|---|
IgG Antibody | 14 | 7 | 7 |
P2X2 Receptor | 10 | 3 | 7 |
Complex complete extended (IgG extended/P2X2 extended) | 24 | 10 | 14 |
Complex partially extended (IgG extended/P2X2 Up) | 14 | 9 | 5 |
Simulation | Regression Parameters | |||||||
---|---|---|---|---|---|---|---|---|
Protein | Condition | Orientation | y0 | a | b | c | d | R sqr |
Antibody | Individual | Down | 0.0914 | 0.5378 | 0.3951 | 0.1381 | 0.0500 | 0.9993 |
Up | 0.1288 | 0.5086 | 0.6070 | 0.0967 | 0.0500 | 0.9989 | ||
Extended | 0.0656 | 0.1937 | 0.6112 | 0.1485 | 0.0500 | 0.9971 | ||
Complex | IgG Extended/P2X2 Up | 0.1041 | 0.1283 | 0.5769 | 0.1406 | 0.0300 | 0.9917 | |
IgG Extended/P2X2 Extended | 0.0618 | 0.1426 | 0.8480 | 0.1867 | 0.0300 | 0.9810 | ||
Receptor | Individual | Down | 0.2591 | 1.1087 | 0.2213 | 5.498e−13 | 0.0270 | 0.9948 |
Up | 0.2383 | 1.1296 | 0.2312 | 0.0050 | 0.0270 | 0.9967 | ||
Extended | 0.0796 | 0.3111 | 0.2208 | 0.3538 | 0.0270 | 0.9998 | ||
Complex | P2X2 Up/IgG Extended | 0.1112 | 1.2584 | 0.0501 | 7.442e−13 | 0.0350 | 0.9963 | |
P2X2 Extended/IgG Extended | 0.0991 | 0.2684 | 0.1939 | 0.3168 | 0.0350 | 0.9920 |
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Santander, E.A.; Bravo, G.; Chang-Halabi, Y.; Olguín-Orellana, G.J.; Naulin, P.A.; Barrera, M.J.; Montenegro, F.A.; Barrera, N.P. The Adsorption of P2X2 Receptors Interacting with IgG Antibodies Revealed by Combined AFM Imaging and Mechanical Simulation. Int. J. Mol. Sci. 2024, 25, 336. https://doi.org/10.3390/ijms25010336
Santander EA, Bravo G, Chang-Halabi Y, Olguín-Orellana GJ, Naulin PA, Barrera MJ, Montenegro FA, Barrera NP. The Adsorption of P2X2 Receptors Interacting with IgG Antibodies Revealed by Combined AFM Imaging and Mechanical Simulation. International Journal of Molecular Sciences. 2024; 25(1):336. https://doi.org/10.3390/ijms25010336
Chicago/Turabian StyleSantander, Eduardo A., Graciela Bravo, Yuan Chang-Halabi, Gabriel J. Olguín-Orellana, Pamela A. Naulin, Mario J. Barrera, Felipe A. Montenegro, and Nelson P. Barrera. 2024. "The Adsorption of P2X2 Receptors Interacting with IgG Antibodies Revealed by Combined AFM Imaging and Mechanical Simulation" International Journal of Molecular Sciences 25, no. 1: 336. https://doi.org/10.3390/ijms25010336