Site Density Functional Theory and Structural Bioinformatics Analysis of the SARS-CoV Spike Protein and hACE2 Complex

Kumawat, Nitesh; Tucs, Andrejs; Bera, Soumen; Chuev, Gennady N.; Valiev, Marat; Fedotova, Marina V.; Kruchinin, Sergey E.; Tsuda, Koji; Sljoka, Adnan; Chakraborty, Amit

doi:10.3390/molecules27030799

Site Density Functional Theory and Structural Bioinformatics Analysis of the SARS-CoV Spike Protein and hACE2 Complex

Journal Article · Wed Jan 26 00:00:00 EST 2022 · Molecules

DOI:https://doi.org/10.3390/molecules27030799· OSTI ID:2471541

^[1]; Tucs, Andrejs ^[2]; ^[3]; ^[4]; Valiev, Marat ^[5]; ^[6]; ^[6]; Tsuda, Koji ^[7]; ^[8]; Chakraborty, Amit ^[9]

Central University of Rajasthan, Ajmer (India)
University of Tokyo, Kashiwa (Japan)
University of Tennessee, Knoxville, TN (United States)
Russian Academy of Sciences (RAS), Pushchino (Russian Federation)
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Russian Academy of Sciences (RAS), Ivanovo (Russian Federation)
University of Tokyo, Kashiwa (Japan); RIKEN Center for Advanced Intelligence Project, Tokyo (Japan); National Institute for Materials Science (NIMS), Tsukuba (Japan)
RIKEN Center for Advanced Intelligence Project, Tokyo (Japan); York University, Toronto, ON (Canada)
Sikkim University, Gangtok (India)

The entry of the SARS-CoV-2, a causative agent of COVID-19, into human host cells is mediated by the SARS-CoV-2 spike (S) glycoprotein, which critically depends on the formation of complexes involving the spike protein receptor-binding domain (RBD) and the human cellular membrane receptor angiotensin-converting enzyme 2 (hACE2). Using classical site density functional theory (SDFT) and structural bioinformatics methods, we investigate binding and conformational properties of these complexes and study the overlooked role of water-mediated interactions. Analysis of the three-dimensional reference interaction site model (3DRISM) of SDFT indicates that water mediated interactions in the form of additional water bridges strongly increases the binding between SARS-CoV-2 spike protein and hACE2 compared to SARS-CoV-1-hACE2 complex. By analyzing structures of SARS-CoV-2 and SARS-CoV-1, we find that the homotrimer SARS-CoV-2 S receptor-binding domain (RBD) has expanded in size, indicating large conformational change relative to SARS-CoV-1 S protein. Protomer with the up-conformational form of RBD, which binds with hACE2, exhibits stronger intermolecular interactions at the RBD-ACE2 interface, with differential distributions and the inclusion of specific H-bonds in the CoV-2 complex. Further interface analysis has shown that interfacial water promotes and stabilizes the formation of CoV-2/hACE2 complex. This interaction causes a significant structural rigidification of the spike protein, favoring proteolytic processing of the S protein for the fusion of the viral and cellular membrane. Moreover, conformational dynamics simulations of RBD motions in SARS-CoV-2 and SARS-CoV-1 point to the role in modification of the RBD dynamics and their impact on infectivity.

View Accepted Manuscript (DOE)

Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 2471541

Journal Information:: Molecules, Journal Name: Molecules Journal Issue: 3 Vol. 27; ISSN 1420-3049

Publisher:: MDPICopyright Statement

Country of Publication:: United States

Language:: English

References (89)

Development and testing of a general amber force field Wang, Junmei; Wolf, Romain M.; Caldwell, James W. Journal of Computational Chemistry, Vol. 25, Issue 9 https://doi.org/10.1002/jcc.20035	journal	January 2004
Efficient treatment of solvation shells in 3D molecular theory of solvation Gusarov, Sergey; Pujari, Bhalchandra S.; Kovalenko, Andriy Journal of Computational Chemistry, Vol. 33, Issue 17 https://doi.org/10.1002/jcc.22974	journal	April 2012
Placevent: An algorithm for prediction of explicit solvent atom distribution-Application to HIV-1 protease and F-ATP synthase Sindhikara, Daniel J.; Yoshida, Norio; Hirata, Fumio Journal of Computational Chemistry, Vol. 33, Issue 18 https://doi.org/10.1002/jcc.22984	journal	April 2012
Extraction of site-site bridge functions and effective pair potentials from simulations of polar molecular liquids Chuev, Gennady N.; Vyalov, Ivan; Georgi, Nikolaj Journal of Computational Chemistry, Vol. 35, Issue 13 https://doi.org/10.1002/jcc.23586	journal	March 2014
MolProbity: More and better reference data for improved all-atom structure validation: PROTEIN SCIENCE.ORG Williams, Christopher J.; Headd, Jeffrey J.; Moriarty, Nigel W. Protein Science, Vol. 27, Issue 1 https://doi.org/10.1002/pro.3330	journal	November 2017
Protein flexibility predictions using graph theory Jacobs, Donald J.; Rader, A. J.; Kuhn, Leslie A. Proteins: Structure, Function, and Genetics, Vol. 44, Issue 2 https://doi.org/10.1002/prot.1081	journal	January 2001
Generating stereochemically acceptable protein pathways Farrell, Daniel W.; Speranskiy, Kirill; Thorpe, M. F. Proteins: Structure, Function, and Bioinformatics, Vol. 78, Issue 14 https://doi.org/10.1002/prot.22810	journal	September 2010
Ion-selective interactions of biologically relevant inorganic ions with alanine zwitterion: a 3D-RISM study Fedotova, Marina V.; Dmitrieva, Olga A. Amino Acids, Vol. 47, Issue 5 https://doi.org/10.1007/s00726-015-1930-4	journal	February 2015
Proline hydration at low temperatures: its role in the protection of cell from freeze-induced stress Fedotova, Marina V.; Dmitrieva, Olga A. Amino Acids, Vol. 48, Issue 7 https://doi.org/10.1007/s00726-016-2232-1	journal	April 2016
An online repository of solvation thermodynamic and structural maps of SARS-CoV-2 targets Olson, Brian; Cruz, Anthony; Chen, Lieyang Journal of Computer-Aided Molecular Design, Vol. 34, Issue 12 https://doi.org/10.1007/s10822-020-00341-x	journal	September 2020
SHIFTX2: significantly improved protein chemical shift prediction Han, Beomsoo; Liu, Yifeng; Ginzinger, Simon W. Journal of Biomolecular NMR, Vol. 50, Issue 1 https://doi.org/10.1007/s10858-011-9478-4	journal	March 2011
Applications to Soft Matter Hansen, Jean-Pierre; McDonald, Ian R. Theory of Simple Liquids, p. 511-584 https://doi.org/10.1016/B978-0-12-387032-2.00012-X	book	August 2013
Anisotropy of Fluctuation Dynamics of Proteins with an Elastic Network Model Atilgan, A. R.; Durell, S. R.; Jernigan, R. L. Biophysical Journal, Vol. 80, Issue 1 https://doi.org/10.1016/S0006-3495(01)76033-X	journal	January 2001
Ion-binding of glycine zwitterion with inorganic ions in biologically relevant aqueous electrolyte solutions Fedotova, Marina V.; Kruchinin, Sergey E. Biophysical Chemistry, Vol. 190-191 https://doi.org/10.1016/j.bpc.2014.04.001	journal	June 2014
Structure, Function, and Antigenicity of the SARS-CoV-2 Spike Glycoprotein Walls, Alexandra C.; Park, Young-Jun; Tortorici, M. Alejandra Cell, Vol. 181, Issue 2 https://doi.org/10.1016/j.cell.2020.02.058	journal	April 2020
Molecular Architecture of the SARS-CoV-2 Virus Yao, Hangping; Song, Yutong; Chen, Yong Cell, Vol. 183, Issue 3 https://doi.org/10.1016/j.cell.2020.09.018	journal	October 2020
Structural and Functional Analysis of the D614G SARS-CoV-2 Spike Protein Variant Yurkovetskiy, Leonid; Wang, Xue; Pascal, Kristen E. Cell, Vol. 183, Issue 3 https://doi.org/10.1016/j.cell.2020.09.032	journal	October 2020
Efficient classical density-functional theories of rigid-molecular fluids and a simplified free energy functional for liquid water Sundararaman, Ravishankar; Arias, T. A. Computer Physics Communications, Vol. 185, Issue 3 https://doi.org/10.1016/j.cpc.2013.11.013	journal	March 2014
Extraction of atom–atom bridge and direct correlation functions from molecular simulations: A test for ambient water Chuev, Gennady N.; Vyalov, I.; Georgi, N. Chemical Physics Letters, Vol. 561-562 https://doi.org/10.1016/j.cplett.2013.01.052	journal	March 2013
SARS Coronavirus Redux Qing, Enya; Gallagher, Tom Trends in Immunology, Vol. 41, Issue 4 https://doi.org/10.1016/j.it.2020.02.007	journal	April 2020
1D-RISM study of glycine zwitterion hydration and ion-molecular complex formation in aqueous NaCl solutions Fedotova, Marina V.; Kruchinin, Sergey E. Journal of Molecular Liquids, Vol. 169 https://doi.org/10.1016/j.molliq.2012.03.008	journal	May 2012
Hydration of para-aminobenzoic acid (PABA) and its anion—The view from statistical mechanics Fedotova, Marina V.; Kruchinin, Sergey E. Journal of Molecular Liquids, Vol. 186 https://doi.org/10.1016/j.molliq.2013.05.028	journal	October 2013
Hydration and ion-binding of glycine betaine: How they may be involved into protection of proteins under abiotic stresses Fedotova, Marina V.; Kruchinin, Sergey E. Journal of Molecular Liquids, Vol. 244 https://doi.org/10.1016/j.molliq.2017.08.117	journal	October 2017
Local ion hydration structure in aqueous imidazolium-based ionic liquids: The effects of concentration and anion nature Fedotova, Marina V.; Kruchinin, Sergey E.; Chuev, Gennady N. Journal of Molecular Liquids, Vol. 247 https://doi.org/10.1016/j.molliq.2017.09.087	journal	December 2017
Compatible osmolytes - bioprotectants: Is there a common link between their hydration and their protective action under abiotic stresses? Fedotova, Marina V. Journal of Molecular Liquids, Vol. 292 https://doi.org/10.1016/j.molliq.2019.111339	journal	October 2019
Features of local ordering of biocompatible ionic liquids: The case of choline-based amino acid ionic liquids Fedotova, Marina V.; Kruchinin, Sergey E.; Chuev, Gennady N. Journal of Molecular Liquids, Vol. 296 https://doi.org/10.1016/j.molliq.2019.112081	journal	December 2019
Hydration features of the neurotransmitter acetylcholine Fedotova, Marina V.; Kruchinin, Sergey E.; Chuev, Gennady N. Journal of Molecular Liquids, Vol. 304 https://doi.org/10.1016/j.molliq.2020.112757	journal	April 2020
Molecular insight on ion hydration and association in aqueous choline chloride solutions Fedotova, Marina V.; Kruchinin, Sergey E.; Chuev, Gennady N. Journal of Molecular Liquids, Vol. 313 https://doi.org/10.1016/j.molliq.2020.113563	journal	September 2020
Thermodynamic Characterization of Hydration Sites from Integral Equation-Derived Free Energy Densities: Application to Protein Binding Sites and Ligand Series Güssregen, Stefan; Matter, Hans; Hessler, Gerhard Journal of Chemical Information and Modeling, Vol. 57, Issue 7 https://doi.org/10.1021/acs.jcim.6b00765	journal	June 2017
Role of Solvation in Drug Design as Revealed by the Statistical Mechanics Integral Equation Theory of Liquids Yoshida, Norio Journal of Chemical Information and Modeling, Vol. 57, Issue 11 https://doi.org/10.1021/acs.jcim.7b00389	journal	October 2017
Critical Differences between the Binding Features of the Spike Proteins of SARS-CoV-2 and SARS-CoV Bai, Chen; Warshel, Arieh The Journal of Physical Chemistry B, Vol. 124, Issue 28 https://doi.org/10.1021/acs.jpcb.0c04317	journal	June 2020
Ion Pairing of the Neurotransmitters Acetylcholine and Glutamate in Aqueous Solutions Kruchinin, Sergey E.; Fedotova, Marina V. The Journal of Physical Chemistry B, Vol. 125, Issue 40 https://doi.org/10.1021/acs.jpcb.1c05117	journal	October 2021
Hydration and Ion Binding of the Osmolyte Ectoine Eiberweiser, Andreas; Nazet, Andreas; Kruchinin, Sergey E. The Journal of Physical Chemistry B, Vol. 119, Issue 49 https://doi.org/10.1021/acs.jpcb.5b09276	journal	November 2015
Molecular Theory of Hydration at Different Temperatures Sheng, Shijie; Miller, Michael; Wu, Jianzhong The Journal of Physical Chemistry B, Vol. 121, Issue 28 https://doi.org/10.1021/acs.jpcb.7b04264	journal	July 2017
Computational Insights into the Conformational Accessibility and Binding Strength of SARS-CoV-2 Spike Protein to Human Angiotensin-Converting Enzyme 2 Peng, Cheng; Zhu, Zhengdan; Shi, Yulong The Journal of Physical Chemistry Letters, Vol. 11, Issue 24 https://doi.org/10.1021/acs.jpclett.0c02958	journal	December 2020
Challenges for Density Functional Theory Cohen, Aron J.; Mori-Sánchez, Paula; Yang, Weitao Chemical Reviews, Vol. 112, Issue 1 https://doi.org/10.1021/cr200107z	journal	December 2011
A Site Density Functional Theory for Water: Application to Solvation of Amino Acid Side Chains Liu, Yu; Zhao, Shuangliang; Wu, Jianzhong Journal of Chemical Theory and Computation, Vol. 9, Issue 4 https://doi.org/10.1021/ct3010936	journal	March 2013
Integral Equation Study of the Hydrophobic Interaction between Graphene Plates Howard, Jesse J.; Perkyns, John S.; Choudhury, Niharendu Journal of Chemical Theory and Computation, Vol. 4, Issue 11 https://doi.org/10.1021/ct8002817	journal	October 2008
Three-Dimensional Molecular Theory of Solvation Coupled with Molecular Dynamics in Amber Luchko, Tyler; Gusarov, Sergey; Roe, Daniel R. Journal of Chemical Theory and Computation, Vol. 6, Issue 3 https://doi.org/10.1021/ct900460m	journal	February 2010
Liquid-state theory of hydrocarbon-water systems: application to methane, ethane, and propane Lue, Leo; Blankschtein, Daniel The Journal of Physical Chemistry, Vol. 96, Issue 21 https://doi.org/10.1021/j100200a069	journal	October 1992
First-Principle Determination of Peptide Conformations in Solvents: Combination of Monte Carlo Simulated Annealing and RISM Theory Kinoshita, Masahiro; Okamoto, Yuko; Hirata, Fumio Journal of the American Chemical Society, Vol. 120, Issue 8 https://doi.org/10.1021/ja972048r	journal	February 1998
An MM/3D-RISM Approach for Ligand Binding Affinities Genheden, Samuel; Luchko, Tyler; Gusarov, Sergey The Journal of Physical Chemistry B, Vol. 114, Issue 25 https://doi.org/10.1021/jp101461s	journal	July 2010
Classical Density-Functional Theory of Inhomogeneous Water Including Explicit Molecular Structure and Nonlinear Dielectric Response Lischner, Johannes; Arias, T. A. The Journal of Physical Chemistry B, Vol. 114, Issue 5 https://doi.org/10.1021/jp9012224	journal	February 2010
An Integral Equation To Describe the Solvation of Polar Molecules in Liquid Water Beglov, Dmitrii; Roux, Benoît The Journal of Physical Chemistry B, Vol. 101, Issue 39 https://doi.org/10.1021/jp971083h	journal	September 1997
Solvation Free Energy of Polar and Nonpolar Molecules in Water: An Extended Interaction Site Integral Equation Theory in Three Dimensions Du, Qishi; Beglov, Dmitrii; Roux, Benoît The Journal of Physical Chemistry B, Vol. 104, Issue 4 https://doi.org/10.1021/jp992712l	journal	February 2000
Characterization of spike glycoprotein of SARS-CoV-2 on virus entry and its immune cross-reactivity with SARS-CoV Ou, Xiuyuan; Liu, Yan; Lei, Xiaobo Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-15562-9	journal	March 2020
The outbreak of SARS-CoV-2 pneumonia calls for viral vaccines Shang, Weilong; Yang, Yi; Rao, Yifan npj Vaccines, Vol. 5, Issue 1 https://doi.org/10.1038/s41541-020-0170-0	journal	March 2020
SARS-CoV-2 simulations go exascale to predict dramatic spike opening and cryptic pockets across the proteome Zimmerman, Maxwell I.; Porter, Justin R.; Ward, Michael D. Nature Chemistry, Vol. 13, Issue 7 https://doi.org/10.1038/s41557-021-00707-0	journal	May 2021
Structural basis of receptor recognition by SARS-CoV-2 Shang, Jian; Ye, Gang; Shi, Ke Nature, Vol. 581, Issue 7807 https://doi.org/10.1038/s41586-020-2179-y	journal	March 2020
Structure of the SARS-CoV-2 spike receptor-binding domain bound to the ACE2 receptor Lan, Jun; Ge, Jiwan; Yu, Jinfang Nature, Vol. 581, Issue 7807 https://doi.org/10.1038/s41586-020-2180-5	journal	March 2020
Stabilized coronavirus spikes are resistant to conformational changes induced by receptor recognition or proteolysis Kirchdoerfer, Robert N.; Wang, Nianshuang; Pallesen, Jesper Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-34171-7	journal	October 2018
Characterization of selective binding of biologically relevant inorganic ions with the proline zwitterion by 3D-RISM theory Fedotova, Marina V.; Dmitrieva, Olga A. New Journal of Chemistry, Vol. 39, Issue 11 https://doi.org/10.1039/C5NJ01559F	journal	January 2015
Hydration structure of osmolyte TMAO: concentration/pressure-induced response Fedotova, Marina V.; Kruchinin, Sergey E.; Chuev, Gennady N. New Journal of Chemistry, Vol. 41, Issue 3 https://doi.org/10.1039/C6NJ03296F	journal	January 2017
Interaction of organic ions with proteins Pérez-Fuentes, Leonor; Drummond, Carlos; Faraudo, Jordi Soft Matter, Vol. 13, Issue 6 https://doi.org/10.1039/C6SM02048H	journal	January 2017
Evidence for cooperative Na ⁺ and Cl ⁻ binding by strongly hydrated l -proline Dmitrieva, Olga A.; Fedotova, Marina V.; Buchner, Richard Physical Chemistry Chemical Physics, Vol. 19, Issue 31 https://doi.org/10.1039/C7CP04335J	journal	January 2017
What factors determine the stability of a weak protein–protein interaction in a charged aqueous droplet? Oh, Myong In; Consta, Styliani Physical Chemistry Chemical Physics, Vol. 19, Issue 47 https://doi.org/10.1039/C7CP05043G	journal	January 2017
Assessing the performance of the MM/PBSA and MM/GBSA methods. 10. Impacts of enhanced sampling and variable dielectric model on protein–protein Interactions Wang, Ercheng; Weng, Gaoqi; Sun, Huiyong Physical Chemistry Chemical Physics, Vol. 21, Issue 35 https://doi.org/10.1039/C9CP04096J	journal	January 2019
Hydration and dynamics of l-glutamate ion in aqueous solution Friesen, Sergej; Fedotova, Marina V.; Kruchinin, Sergey E. Physical Chemistry Chemical Physics, Vol. 23, Issue 2 https://doi.org/10.1039/D0CP05489E	journal	January 2021
Modeling the interaction of SARS-CoV-2 binding to the ACE2 receptor via molecular theory of solvation Kobryn, Alexander E.; Maruyama, Yutaka; Velázquez-Martínez, Carlos A. New Journal of Chemistry, Vol. 45, Issue 34 https://doi.org/10.1039/D1NJ02015C	journal	January 2021
Combinations of simulation and integral equation theory Kast, Stefan M. Physical Chemistry Chemical Physics, Vol. 3, Issue 23 https://doi.org/10.1039/b106075a	journal	November 2001
Optimized Cluster Expansions for Classical Fluids. II. Theory of Molecular Liquids Chandler, David; Andersen, Hans C. The Journal of Chemical Physics, Vol. 57, Issue 5 https://doi.org/10.1063/1.1678513	journal	September 1972
An interaction site model integral equation study of molecular fluids explicitly considering the molecular orientation Sumi, Tomonari; Sekino, Hideo The Journal of Chemical Physics, Vol. 125, Issue 3 https://doi.org/10.1063/1.2215603	journal	July 2006
Reference interaction site model study of self-aggregating cyanine dyes Chuev, Gennady N.; Fedorov, Maxim V. The Journal of Chemical Physics, Vol. 131, Issue 7 https://doi.org/10.1063/1.3211948	journal	August 2009
Protein solvation from theory and simulation: Exact treatment of Coulomb interactions in three-dimensional theories Perkyns, John S.; Lynch, Gillian C.; Howard, Jesse J. The Journal of Chemical Physics, Vol. 132, Issue 6 https://doi.org/10.1063/1.3299277	journal	February 2010
Towards a more accurate reference interaction site model integral equation theory for molecular liquids Kežić, Bernarda; Perera, Aurélien The Journal of Chemical Physics, Vol. 135, Issue 23 https://doi.org/10.1063/1.3666006	journal	December 2011
Application of efficient algorithm for solving six-dimensional molecular Ornstein-Zernike equation Ishizuka, R.; Yoshida, N. The Journal of Chemical Physics, Vol. 136, Issue 11 https://doi.org/10.1063/1.3693623	journal	March 2012
Density functional theory of nonuniform polyatomic systems. I. General formulation Chandler, David; McCoy, John D.; Singer, Sherwin J. The Journal of Chemical Physics, Vol. 85, Issue 10 https://doi.org/10.1063/1.451510	journal	November 1986
Density functional theory of nonuniform polyatomic systems. II. Rational closures for integral equations Chandler, David; McCoy, John D.; Singer, Sherwin J. The Journal of Chemical Physics, Vol. 85, Issue 10 https://doi.org/10.1063/1.451511	journal	November 1986
Aqueous interaction site integral-equation theory that exactly takes into account intramolecular correlations Chong, Song-Ho; Ham, Sihyun The Journal of Chemical Physics, Vol. 137, Issue 15 https://doi.org/10.1063/1.4758072	journal	October 2012
Nucleation in n-alkanes: A density-functional approach Seok, Chaok; Oxtoby, David W. The Journal of Chemical Physics, Vol. 109, Issue 18 https://doi.org/10.1063/1.477445	journal	November 1998
Efficient molecular density functional theory using generalized spherical harmonics expansions Ding, Lu; Levesque, Maximilien; Borgis, Daniel The Journal of Chemical Physics, Vol. 147, Issue 9 https://doi.org/10.1063/1.4994281	journal	September 2017
Chemical bond effects in classical site density functional theory of inhomogeneous molecular liquids Chuev, Gennady N.; Fedotova, Marina V.; Valiev, Marat The Journal of Chemical Physics, Vol. 152, Issue 4 https://doi.org/10.1063/1.5139619	journal	January 2020
Renormalized site density functional theory for models of ion hydration Chuev, Gennady N.; Fedotova, Marina V.; Valiev, Marat The Journal of Chemical Physics, Vol. 155, Issue 6 https://doi.org/10.1063/5.0060249	journal	August 2021
Cell entry mechanisms of SARS-CoV-2 Shang, Jian; Wan, Yushun; Luo, Chuming Proceedings of the National Academy of Sciences, Vol. 117, Issue 21 https://doi.org/10.1073/pnas.2003138117	journal	May 2020
Site density models of inhomogeneous classical molecular liquids Valiev, Marat; Chuev, Gennady N. Journal of Statistical Mechanics: Theory and Experiment, Vol. 2018, Issue 9 https://doi.org/10.1088/1742-5468/aad6bf	journal	August 2018
Renormalized site density functional theory Chuev, Gennady N.; Fedotova, Marina V.; Valiev, Marat Journal of Statistical Mechanics: Theory and Experiment, Vol. 2021, Issue 3 https://doi.org/10.1088/1742-5468/abdeb3	journal	March 2021
PRODIGY: a web server for predicting the binding affinity of protein–protein complexes Xue, Li C.; Rodrigues, João Pglm; Kastritis, Panagiotis L. Bioinformatics https://doi.org/10.1093/bioinformatics/btw514	journal	August 2016
iMODS: internal coordinates normal mode analysis server López-Blanco, José Ramón; Aliaga, José I.; Quintana-Ortí, Enrique S. Nucleic Acids Research, Vol. 42, Issue W1 https://doi.org/10.1093/nar/gku339	journal	April 2014
Kohn-Sham-Like Approach toward a Classical Density-Functional Theory of Inhomogeneous Polar Molecular Liquids: An Application to Liquid Hydrogen Chloride Lischner, Johannes; Arias, T. A. Physical Review Letters, Vol. 101, Issue 21 https://doi.org/10.1103/PhysRevLett.101.216401	journal	November 2008
Density functional theory: Its origins, rise to prominence, and future Jones, R. O. Reviews of Modern Physics, Vol. 87, Issue 3 https://doi.org/10.1103/RevModPhys.87.897	journal	August 2015
Effect of ambient temperature on respiratory tract cells exposed to SARS-CoV-2 viral mimicking nanospheres—An experimental study Kumar, Sachin; Paul, Alexandra; Chatterjee, Sayantan Biointerphases, Vol. 16, Issue 1 https://doi.org/10.1116/6.0000743	journal	January 2021
Structure of SARS Coronavirus Spike Receptor-Binding Domain Complexed with Receptor Li, F. Science, Vol. 309, Issue 5742 https://doi.org/10.1126/science.1116480	journal	September 2005
Cryo-EM structure of the 2019-nCoV spike in the prefusion conformation Wrapp, Daniel; Wang, Nianshuang; Corbett, Kizzmekia S. Science, Vol. 367, Issue 6483 https://doi.org/10.1126/science.abb2507	journal	February 2020
Structural basis for the recognition of SARS-CoV-2 by full-length human ACE2 Yan, Renhong; Zhang, Yuanyuan; Li, Yaning Science, Vol. 367, Issue 6485 https://doi.org/10.1126/science.abb2762	journal	March 2020
Structure, Function, and Evolution of Coronavirus Spike Proteins Li, Fang Annual Review of Virology, Vol. 3, Issue 1 https://doi.org/10.1146/annurev-virology-110615-042301	journal	September 2016
The Effects of Temperature and Relative Humidity on the Viability of the SARS Coronavirus Chan, K. H.; Peiris, J. S. Malik; Lam, S. Y. Advances in Virology, Vol. 2011 https://doi.org/10.1155/2011/734690	journal	January 2011
Hyperphosphorylation of Intrinsically Disordered Tau Protein Induces an Amyloidogenic Shift in Its Conformational Ensemble Zhu, Shaolong; Shala, Agnesa; Bezginov, Alexandr PLOS ONE, Vol. 10, Issue 3 https://doi.org/10.1371/journal.pone.0120416	journal	March 2015
Virtual Screening Strategies in Drug Discovery: A Critical Review Lavecchia, A.; Giovanni, C. Current Medicinal Chemistry, Vol. 20, Issue 23 https://doi.org/10.2174/09298673113209990001	journal	June 2013
In Silico Screening of Bioactive and Biomimetic Solutes Using Molecular Integral Equation Theory S. Palmer, David; N. Chuev, Gennady; L. Ratkova, Ekaterina Current Pharmaceutical Design, Vol. 17, Issue 17 https://doi.org/10.2174/138161211796355065	journal	June 2011

Similar Records

Structural Insights into Immune Recognition of the Severe Acute Respiratory Syndrome Coronavirus S Protein Receptor Binding Domain

Journal Article · Wed Dec 31 23:00:00 EST 2008 · Journal of Molecular Biology · OSTI ID:980526

Enhanced Binding of SARS-CoV-2 Spike Protein to Receptor by Distal Polybasic Cleavage Sites

Journal Article · Sat Aug 01 20:00:00 EDT 2020 · ACS Nano · OSTI ID:1800585

Related Subjects

3DRISM
60 APPLIED LIFE SCIENCES
Biochemistry & Molecular Biology
Chemistry
conformational dynamics
coronavirus
normal mode analysis
site density functional theory
spike protein binding to human receptor
structural rigidity

Site Density Functional Theory and Structural Bioinformatics Analysis of the SARS-CoV Spike Protein and hACE2 Complex

Citation Formats

References (89)

Similar Records

Related Subjects