Structural Characterization of Ectodomain G Protein of Respiratory Syncytial Virus and Its Interaction with Heparan Sulfate: Multi-Spectroscopic and In Silico Studies Elucidating Host-Pathogen Interactions
Abstract
:1. Introduction
2. Results and Discussion
2.1. Structural and Conformational Stability Measurements of edG
2.1.1. Absorbance Measurements
2.1.2. Fluorescence Measurements
2.1.3. Urea and GdmCl-Induced Denaturation
2.2. Binding Interaction Studies of edG with Heparan Sulfate
2.2.1. Fluorescence Quenching Measurements
2.2.2. Absorbance Binding Measurements
2.2.3. Molecular Docking
2.2.4. MD Simulation Studies
3. Materials and Methods
3.1. Materials
3.2. Expression and Purification of edG
3.3. Sample Preparation
3.4. Absorbance Measurements
3.5. Fluorescence Measurements
3.6. ANS (8-Anilinonapthalene-1-Sulfonic Acid) Binding Measurements
3.7. Analysis of Denaturation Spectral Measurements
3.8. Fluorescence Quenching Measurements
3.9. Molecular Docking
3.10. MD Simulation Studies
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Sample Availability
References
- Coultas, J.A.; Smyth, R.; Openshaw, P.J. Respiratory syncytial virus (RSV): A scourge from infancy to old age. Thorax 2019, 74, 986–993. [Google Scholar] [CrossRef] [Green Version]
- Chatzis, O.; Darbre, S.; Pasquier, J.; Meylan, P.; Manuel, O.; Aubert, J.D.; Beck-Popovic, M.; Masouridi-Levrat, S.; Ansari, M.; Kaiser, L.; et al. Burden of severe RSV disease among immunocompromised children and adults: A 10 year retrospective study. BMC Infect. Dis. 2018, 18, 111. [Google Scholar] [CrossRef]
- Schildgen, O. The lack of protective immunity against RSV in the elderly. Epidemiol. Infect. 2009, 137, 1687–1690. [Google Scholar] [CrossRef] [PubMed]
- Stein, R.; Bont, L.J.; Zar, H.; Polack, F.P.; Park, C.; Claxton, A.; Borok, G.; Butylkova, Y.; Wegzyn, C. Respiratory syncytial virus hospitalization and mortality: Systematic review and meta-analysis. Pediatr. Pulmonol. 2016, 52, 556–569. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Resch, B. Product review on the monoclonal antibody palivizumab for prevention of respiratory syncytial virus infection. Hum. Vaccin. Immunother. 2017, 13, 2138–2149. [Google Scholar] [CrossRef] [Green Version]
- Boyoglu-Barnum, S.; Todd, S.O.; Meng, J.; Barnum, T.R.; Chirkova, T.; Haynes, L.M.; Jadhao, S.J.; Tripp, R.A.; Oomens, A.G.; Moore, M.L.; et al. Mutating the CX3C Motif in the G Protein Should Make a Live Respiratory Syncytial Virus Vaccine Safer and More Effective. J. Virol. 2017, 91, e02059. [Google Scholar] [CrossRef] [Green Version]
- Liang, B. Structures of the Mononegavirales Polymerases. J. Virol. 2020, 94. [Google Scholar] [CrossRef]
- Haynes, L.M.; Jones, L.P.; Barskey, A.; Anderson, L.J.; Tripp, R.A. Enhanced Disease and Pulmonary Eosinophilia Associated with Formalin-Inactivated Respiratory Syncytial Virus Vaccination Are Linked to G Glycoprotein CX3C-CX3CR1 Interaction and Expression of Substance P. J. Virol. 2003, 77, 9831–9844. [Google Scholar] [CrossRef] [Green Version]
- Radu, G.U.; Caidi, H.; Miao, C.; Tripp, R.A.; Anderson, L.J.; Haynes, L.M. Prophylactic Treatment with a G Glycoprotein Monoclonal Antibody Reduces Pulmonary Inflammation in Respiratory Syncytial Virus (RSV)-Challenged Naïve and Formalin-Inactivated RSV-Immunized BALB/c Mice. J. Virol. 2010, 84, 9632–9636. [Google Scholar] [CrossRef] [Green Version]
- Lee, J.; Klenow, L.; Coyle, E.M.; Golding, H.; Khurana, S. Protective antigenic sites in respiratory syncytial virus G attachment protein outside the central conserved and cysteine noose domains. PLoS Pathog. 2018, 14, e1007262. [Google Scholar] [CrossRef] [PubMed]
- Boyoglu-Barnum, S.; Chirkova, T.; Todd, S.O.; Barnum, T.R.; Gaston, K.A.; Jorquera, P.; Haynes, L.M.; Tripp, R.A.; Moore, M.L.; Anderson, L.J. Prophylaxis with a Respiratory Syncytial Virus (RSV) Anti-G Protein Monoclonal Antibody Shifts the Adaptive Immune Response to RSV rA2-line19F Infection from Th2 to Th1 in BALB/c Mice. J. Virol. 2014, 88, 10569–10583. [Google Scholar] [CrossRef] [Green Version]
- Miao, C.; Radu, G.U.; Caidi, H.; Tripp, R.; Anderson, L.J.; Haynes, L.M. Treatment with respiratory syncytial virus G glycoprotein monoclonal antibody or F(ab′)2 components mediates reduced pulmonary inflammation in mice. J. Gen. Virol. 2009, 90, 1119–1123. [Google Scholar] [CrossRef] [PubMed]
- Han, J.; Takeda, K.; Wang, M.; Zeng, W.; Jia, Y.; Shiraishi, Y.; Okamoto, M.; Dakhama, A.; Gelfand, E.W. Effects of Anti-G and Anti-F Antibodies on Airway Function after Respiratory Syncytial Virus Infection. Am. J. Respir. Cell Mol. Biol. 2014, 51, 143–154. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Caidi, H.; Miao, C.; Thornburg, N.J.; Tripp, R.A.; Anderson, L.J.; Haynes, L.M. Anti-respiratory syncytial virus (RSV) G monoclonal antibodies reduce lung inflammation and viral lung titers when delivered therapeutically in a BALB/c mouse model. Antivir. Res. 2018, 154, 149–157. [Google Scholar] [CrossRef] [PubMed]
- Kauvar, L.M.; Harcourt, J.L.; Haynes, L.M.; Tripp, R.A. Therapeutic targeting of respiratory syncytial virus G-protein. Immunother. 2010, 2, 655–661. [Google Scholar] [CrossRef] [Green Version]
- Chirkova, T.; Lin, S.; Oomens, A.G.P.; Gaston, K.A.; Boyoglu-Barnum, S.; Meng, J.; Stobart, C.C.; Cotton, C.U.; Hartert, T.V.; Moore, M.L.; et al. CX3CR1 is an important surface molecule for respiratory syncytial virus infection in human airway epithelial cells. J. Gen. Virol. 2015, 96, 2543. [Google Scholar] [CrossRef]
- Johnson, S.M.; McNally, B.A.; Ioannidis, I.; Flano, E.; Teng, M.N.; Oomens, A.G.; Walsh, E.E.; Peeples, M.E. Respiratory Syncytial Virus Uses CX3CR1 as a Receptor on Primary Human Airway Epithelial Cultures. PLoS Pathog. 2015, 11, e1005318. [Google Scholar] [CrossRef] [Green Version]
- Feldman, S.A.; Hendry, R.M.; Beeler, J.A. Identification of a Linear Heparin Binding Domain for Human Respiratory Syncytial Virus Attachment Glycoprotein G. J. Virol. 1999, 73, 6610–6617. [Google Scholar] [CrossRef] [Green Version]
- Hallak, L.K.; Spillmann, D.; Collins, P.L.; Peeples, M.E. Glycosaminoglycan Sulfation Requirements for Respiratory Syncytial Virus Infection. J. Virol. 2000, 74, 10508–10513. [Google Scholar] [CrossRef] [Green Version]
- Li, J.P.; Kusche-Gullberg, M. Heparan Sulfate: Biosynthesis, Structure, and Function. Int. Rev. Cell Mol. Biol. 2016, 325, 215–273. [Google Scholar] [CrossRef]
- Gomes, P.B.; Dietrich, C.P. Distribution of heparin and other sulfated glycosaminoglycans in vertebrates. Comp. Biochem. Physiol. Part B: Comp. Biochem. 1982, 73, 857–863. [Google Scholar] [CrossRef]
- Clausen, T.M.; Sandoval, D.R.; Spliid, C.B.; Pihl, J.; Perrett, H.R.; Painter, C.D.; Narayanan, A.; Majowicz, S.A.; Kwong, E.M.; McVicar, R.N.; et al. SARS-CoV-2 Infection Depends on Cellular Heparan Sulfate and ACE2. Cell 2020, 183, 1043–1057.e15. [Google Scholar] [CrossRef]
- Fersht, A.R. From the first protein structures to our current knowledge of protein folding: Delights and scepticisms. Nat. Rev. Mol. Cell Biol. 2008, 9, 650–654. [Google Scholar] [CrossRef]
- Hartl, F.U.; Hayer-Hartl, M. Protein folding. Molecular chaperones in the cytosol: From nascent chain to folded protein. Science 2002, 295, 1852–1858. [Google Scholar] [CrossRef] [Green Version]
- Dobson, C.M. Protein folding and misfolding. Nature 2003, 426, 884–890. [Google Scholar] [CrossRef] [PubMed]
- Street, T.O.; Bolen, D.W.; Rose, G.D. A molecular mechanism for osmolyte-induced protein stability. Proc. Natl. Acad. Sci. USA 2006, 103, 13997–14002. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Beg, I.; Minton, A.P.; Hassan, M.I.; Islam, A.; Ahmad, F. Thermal Stabilization of Proteins by Mono- and Oligosaccharides: Measurement and Analysis in the Context of an Excluded Volume Model. Biochemistry 2015, 54, 3594–3603. [Google Scholar] [CrossRef] [PubMed]
- Do, A.; Ka, D. Solvent denaturation and stabilization of globular proteins. Biochemistry 1991, 30, 5974–5985. [Google Scholar] [CrossRef]
- Lapanje, S. Random Coil Behaviour of Proteins in Concentrated Urea Solutions. Croat. Chem. Acta 1969, 41, 115–124. [Google Scholar]
- Hamza, A.; Shafat, Z.; Parray, Z.A.; Hisamuddin, M.; Khan, W.H.; Ahmed, A.; Almajhdi, F.N.; Farrag, M.A.; Mohammed, A.A.; Islam, A.; et al. Structural Characterization and Binding Studies of the Ectodomain G Protein of Respiratory Syncytial Virus Reveal the Crucial Role of pH with Possible Implications in Host–Pathogen Interactions. ACS Omega 2021, 6, 10403–10414. [Google Scholar] [CrossRef]
- Khan, P.; Parkash, A.; Islam, A.; Ahmad, F.; Hassan, M.I. Molecular basis of the structural stability of hemochromatosis factor E: A combined molecular dynamic simulation and GdmCl-induced denaturation study. Biopolymers 2016, 105, 133–142. [Google Scholar] [CrossRef] [PubMed]
- Battles, M.B.; McLellan, J.S. Respiratory syncytial virus entry and how to block it. Nat. Rev. Microbiol. 2019, 17, 233–245. [Google Scholar] [CrossRef]
- Prasad, S.; Mandal, I.; Singh, S.; Paul, A.; Mandal, B.; Venkatramani, R.; Swaminathan, R. Near UV-Visible electronic absorption originating from charged amino acids in a monomeric protein. Chem. Sci. 2017, 8, 5416–5433. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schmid, F.-X. Biological Macromolecules: UV-visible Spectrophotometry. Encycl. Life Sci. 2001, 1–4. [Google Scholar] [CrossRef]
- Syed, S.B.; Shahbaaz, M.; Khan, S.H.; Srivastava, S.; Islam, A.; Ahmad, F.; Hassan, I. Estimation of pH effect on the structure and stability of kinase domain of human integrin-linked kinase. J. Biomol. Struct. Dyn. 2019, 37, 156–165. [Google Scholar] [CrossRef]
- Alston, R.W.; Urbanikova, L.; Sevcik, J.; Lasagna, M.; Reinhart, G.D.; Scholtz, J.M.; Pace, C.N. Contribution of Single Tryptophan Residues to the Fluorescence and Stability of Ribonuclease Sa. Biophys. J. 2004, 87, 4036–4047. [Google Scholar] [CrossRef] [Green Version]
- Gasymov, O.K.; Abduragimov, A.R.; Glasgow, B.J. pH-Dependent Conformational Changes in Tear Lipocalin by Site-Directed Tryptophan Fluorescence. Biochemistry 2009, 49, 582–590. [Google Scholar] [CrossRef] [Green Version]
- Ptitsyn, O.; Uversky, V. The molten globule is a third thermodynamical state of protein molecules. FEBS Lett. 1994, 341, 15–18. [Google Scholar] [CrossRef] [Green Version]
- Naiyer, A.; Hassan, M.I.; Islam, A.; Sundd, M.; Ahmad, F. Structural characterization of MG and pre-MG states of proteins by MD simulations, NMR, and other techniques. J. Biomol. Struct. Dyn. 2015, 33, 2267–2284. [Google Scholar] [CrossRef]
- Slavík, J. Anilinonaphthalene sulfonate as a probe of membrane composition and function. Biochim. Biophys. Acta-Rev. Biomembr. 1982, 694, 1–25. [Google Scholar] [CrossRef]
- Gupta, P.; Khan, F.I.; Roy, S.; Anwar, S.; Dahiya, R.; Alajmi, M.F.; Hussain, A.; Rehman, M.T.; Lai, D.; Hassan, M.I. Functional implications of pH-induced conformational changes in the Sphingosine kinase 1. Spectrochim. Acta Part A Mol. Biomol. Spectrosc. 2020, 225, 117453. [Google Scholar] [CrossRef] [PubMed]
- Naseem, F.; Khan, R.H.; Haq, S.K.; Naeem, A. Characterization of molten globule state of fetuin at low pH. Biochim. Biophys. Acta-Proteins Proteom. 2003, 1649, 164–170. [Google Scholar] [CrossRef]
- Bansal, R.; Haque, M.A.; Hassan, M.I.; Ethayathulla, A.S.; Kaur, P. Structural and conformational behavior of MurE ligase from Salmonella enterica serovar Typhi at different temperature and pH conditions. Int. J. Biol. Macromol. 2020, 150, 389–399. [Google Scholar] [CrossRef]
- Haque, M.A.; Ubaid-ullah, S.; Zaidi, S.; Hassan, M.I.; Islam, A.; Batra, J.K.; Ahmad, F. Characterization of pre-molten globule state of yeast iso-1-cytochrome c and its deletants at pH 6.0 and 25 °C. Int. J. Biol. Macromol. 2015, 72, 1406–1418. [Google Scholar] [CrossRef]
- Bychkova, V.E.; Dujsekina, A.E.; Klenin, S.I.; Tiktopulo, E.I.; Uversky, A.V.N.; Ptitsyn, O.B. Molten Globule-Like State of Cytochrome c under Conditions Simulating Those Near the Membrane Surface. Biochemistry 1996, 35, 6058–6063. [Google Scholar] [CrossRef]
- Ahmad, F. Stability of acetylcholinesterase in guanidine hydrochloride solution. Can. J. Biochem. 1981, 59, 551–555. [Google Scholar] [CrossRef] [PubMed]
- Pace, C.N. [14]Determination and analysis of urea and guanidine hydrochloride denaturation curves. Methods Enzymol. 1986, 131, 266–280. [Google Scholar] [CrossRef]
- Idrees, D.; Prakash, A.; Haque, M.A.; Islam, A.; Ahmad, F.; Hassan, M.I. Spectroscopic and MD simulation studies on unfolding processes of mitochondrial carbonic anhydrase VA induced by urea. J. Biomol. Struct. Dyn. 2016, 34, 1987–1997. [Google Scholar] [CrossRef]
- Royer, C.A. Probing Protein Folding and Conformational Transitions with Fluorescence. Chem. Rev. 2006, 106, 1769–1784. [Google Scholar] [CrossRef]
- Vivian, J.T.; Callis, P.R. Mechanisms of Tryptophan Fluorescence Shifts in Proteins. Biophys. J. 2001, 80, 2093–2109. [Google Scholar] [CrossRef] [Green Version]
- Monera, O.D.; Kay, C.M.; Hodges, R.S. Protein denaturation with guanidine hydrochloride or urea provides a different estimate of stability depending on the contributions of electrostatic interactions. Protein Sci. 1994, 3, 1984–1991. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Roy, S.; Mohammad, T.; Gupta, P.; Dahiya, R.; Parveen, S.; Luqman, S.; Hasan, G.M.; Hassan, M.I. Discovery of Harmaline as a Potent Inhibitor of Sphingosine Kinase-1: A Chemopreventive Role in Lung Cancer. ACS Omega 2020, 5, 21550–21560. [Google Scholar] [CrossRef]
- Susana, S.; Mateus, N.; de Freitas, V. Interaction of Different Polyphenols with Bovine Serum Albumin (BSA) and Human Salivary α-Amylase (HSA) by Fluorescence Quenching. J. Agric. Food Chem. 2007, 55, 6726–6735. [Google Scholar] [CrossRef]
- Anwar, S.; Shamsi, A.; Shahbaaz, M.; Queen, A.; Khan, P.; Hasan, G.M.; Islam, A.; Alajmi, M.F.; Hussain, A.; Ahmad, F.; et al. Rosmarinic Acid Exhibits Anticancer Effects via MARK4 Inhibition. Sci. Rep. 2020, 10, 10300. [Google Scholar] [CrossRef]
- Rehman, M.T.; Shamsi, H.; Khan, A.U. Insight into the Binding Mechanism of Imipenem to Human Serum Albumin by Spectroscopic and Computational Approaches. Mol. Pharm. 2014, 11, 1785–1797. [Google Scholar] [CrossRef] [PubMed]
- Wang, H.-D.; Niu, C.H.; Yang, Q.; Badea, I. Study on protein conformation and adsorption behaviors in nanodiamond particle–proteincomplexes. Nanotechnology 2011, 22, 145703. [Google Scholar] [CrossRef]
- Yu, S.; Perálvarez-Marín, A.; Minelli, C.; Faraudo, J.; Roig, A.; Laromaine, A. Albumin-coated SPIONs: An experimental and theoretical evaluation of protein conformation, binding affinity and competition with serum proteins. Nanoscale 2016, 8, 14393–14405. [Google Scholar] [CrossRef] [Green Version]
- Chung, C.-S.; Hsiao, J.-C.; Chang, Y.-S.; Chang, W. A27L Protein Mediates Vaccinia Virus Interaction with Cell Surface Heparan Sulfate. J. Virol. 1998, 72, 1577–1585. [Google Scholar] [CrossRef] [Green Version]
- Shieh, M.T.; WuDunn, D.; Montgomery, R.I.; Esko, J.D.; Spear, P.G. Cell surface receptors for herpes simplex virus are heparan sulfate proteoglycans. J. Cell Biol. 1992, 116, 1273–1281. [Google Scholar] [CrossRef]
- Barth, H.; Schäfer, C.; Adah, M.I.; Zhang, F.; Linhardt, R.J.; Toyoda, H.; Kinoshita-Toyoda, A.; Toida, T.; Kuppevelt, T.H.; van Depla, E.; et al. Cellular Binding of Hepatitis C Virus Envelope Glycoprotein E2 Requires Cell Surface Heparan Sulfate. J. Biol. Chem. 2003, 278, 41003–41012. [Google Scholar] [CrossRef] [Green Version]
- Byrnes, A.P.; Griffin, D.E. Binding of Sindbis Virus to Cell Surface Heparan Sulfate. J. Virol. 1998, 72, 7349–7356. [Google Scholar] [CrossRef] [Green Version]
- Mondor, I.; Ugolini, S.; Sattentau, Q.J. Human Immunodeficiency Virus Type 1 Attachment to HeLa CD4 Cells Is CD4 Independent and gp120 Dependent and Requires Cell Surface Heparans. J. Virol. 1998, 72, 3623–3634. [Google Scholar] [CrossRef] [Green Version]
- Milewska, A.; Zarebski, M.; Nowak, P.; Stozek, K.; Potempa, J.; Pyrc, K. Human Coronavirus NL63 Utilizes Heparan Sulfate Proteoglycans for Attachment to Target Cells. J. Virol. 2014, 88, 13221–13230. [Google Scholar] [CrossRef] [Green Version]
- Kalia, M.; Chandra, V.; Rahman, S.A.; Sehgal, D.; Jameel, S. Heparan Sulfate Proteoglycans Are Required for Cellular Binding of the Hepatitis E Virus ORF2 Capsid Protein and for Viral Infection. J. Virol. 2009, 83, 12714–12724. [Google Scholar] [CrossRef] [Green Version]
- Machado, V.B.; de Sá, M.J.; Miranda Prado, A.K.; Alves de Toledo, K.; Regasini, L.O.; Pereira de Souza, F.; Caruso, Í.P.; Fossey, M.A. Biophysical and flavonoid-binding studies of the G protein ectodomain of group A human respiratory syncytial virus. Heliyon 2019, 5, e01394. [Google Scholar] [CrossRef] [Green Version]
- Shafat, Z.; Hamza, A.; Deeba, F.; Faizan, M.I.; Khan, N.; Islam, A.; Ahmed, A.; Alamery, S.F.; Parveen, S. Optimization of parameters for expression and purification of G glycoprotein ectodomain of respiratory syncytial virus. Futur. Virol. 2020, 15, 225–235. [Google Scholar] [CrossRef]
- Khan, W.H.; Srungaram, V.L.N.R.; Islam, A.; Beg, I.; Haider, M.S.H.; Ahmad, F.; Broor, S.; Parveen, S. Biophysical characterization of G protein ectodomain of group B human respiratory syncytial virus from E. coli. Prep. Biochem. Biotechnol. 2016, 46, 483–488. [Google Scholar] [CrossRef] [PubMed]
- Pace, C.N.; Vajdos, F.; Fee, L.; Grimsley, G.; Gray, T. How to measure and predict the molar absorption coefficient of a protein. Protein Sci. 1995, 4, 2411–2423. [Google Scholar] [CrossRef] [Green Version]
- Shafat, Z.; Faizan, I.; Tazeen, A.; Farooqui, A.; Deeba, F.; Aftab, S.; Hamza, A.; Parveen, S.; Islam, A.; Broor, S.; et al. In-silico analysis of ectodomain G protein of Respiratory Syncytial Virus. Indian J. Heal. Sci. Care 2017, 4, 110. [Google Scholar] [CrossRef]
- Dassault Systèmes BIOVIA. Discov. Stud. Model. Environ. 2017. San Diego. Available online: https://www.3ds.com/products-services/biovia/products/molecular-modeling-simulation/biovia-discovery-studio/ (accessed on 6 December 2021).
- Schrodinger, L. The PyMOL Molecular Graphics System. Version 1. 2010. Available online: https://sourceforge.net/projects/pymol/files/latest/download (accessed on 6 December 2021).
- Pronk, S.; Páll, S.; Schulz, R.; Larsson, P.; Bjelkmar, P.; Apostolov, R.; Shirts, M.R.; Smith, J.C.; Kasson, P.M.; van der Spoel, D.; et al. GROMACS 4.5: A high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics 2013, 29, 845–854. [Google Scholar] [CrossRef] [PubMed]
- Oostenbrink, C.; Villa, A.; Mark, A.E.; Gunsteren, W.F. Van A biomolecular force field based on the free enthalpy of hydration and solvation: The GROMOS force-field parameter sets 53A5 and 53A6. J. Comput. Chem. 2004, 25, 1656–1676. [Google Scholar] [CrossRef] [PubMed]
- Schüttelkopf, A.W.; Van Aalten, D.M.F. PRODRG: A tool for high-throughput crystallography of protein–ligand complexes. Acta Crystallogr. Sect. D Biol. Crystallogr. 2004, 60, 1355–1363. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zielkiewicz, J. Structural properties of water: Comparison of the SPC, SPCE, TIP4P, and TIP5P models of water. J. Chem. Phys. 2005, 123, 104501. [Google Scholar] [CrossRef] [PubMed]
Probes | Denaturants | Transition | ΔG0D, kcal mol−1 | m, kcal mol−1 M−1 | Cm, M |
---|---|---|---|---|---|
F344 | Urea | N↔D | 3.76 ± 0.34 | 0.85 ± 0.08 | 4.42 ± 0.16 |
GdmCl | N↔D | 2.53 ± 0.20 | 1.66 ± 0.09 | 1.52 ± 0.07 |
Ksv (104 M−1) | Kq (1013 M−1 s−1) | K (106 M−1) | n | R2 |
---|---|---|---|---|
4.96 | 1.73 | 3.98 | 1.44 | 0.98 |
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Hamza, A.; Samad, A.; Imam, M.A.; Faizan, M.I.; Ahmed, A.; Almajhdi, F.N.; Hussain, T.; Islam, A.; Parveen, S. Structural Characterization of Ectodomain G Protein of Respiratory Syncytial Virus and Its Interaction with Heparan Sulfate: Multi-Spectroscopic and In Silico Studies Elucidating Host-Pathogen Interactions. Molecules 2021, 26, 7398. https://doi.org/10.3390/molecules26237398
Hamza A, Samad A, Imam MA, Faizan MI, Ahmed A, Almajhdi FN, Hussain T, Islam A, Parveen S. Structural Characterization of Ectodomain G Protein of Respiratory Syncytial Virus and Its Interaction with Heparan Sulfate: Multi-Spectroscopic and In Silico Studies Elucidating Host-Pathogen Interactions. Molecules. 2021; 26(23):7398. https://doi.org/10.3390/molecules26237398
Chicago/Turabian StyleHamza, Abu, Abdus Samad, Md. Ali Imam, Md. Imam Faizan, Anwar Ahmed, Fahad N. Almajhdi, Tajamul Hussain, Asimul Islam, and Shama Parveen. 2021. "Structural Characterization of Ectodomain G Protein of Respiratory Syncytial Virus and Its Interaction with Heparan Sulfate: Multi-Spectroscopic and In Silico Studies Elucidating Host-Pathogen Interactions" Molecules 26, no. 23: 7398. https://doi.org/10.3390/molecules26237398