In silico studies of selected multi-drug targeting against 3CLpro and nsp12 RNA-dependent RNA-polymerase proteins of SARS-CoV-2 and SARS-CoV
Inemesit A Udofia, Kofoworola O Gbayo, Oluwakemi A Oloba-Whenu, Taofeek B Ogunbayo, Chukwuemeka Isanbor
Network Modeling Analysis in Health Informatics and Bioinformatics, doi:10.1007/s13721-021-00299-2
An outbreak of a cluster of viral pneumonia cases, subsequently identified as coronavirus disease 2019 , due to a novel SARS-CoV-2 necessitates an urgent need for a vaccine to prevent infection or an approved medication for a cure. In our in silico molecular docking study, a total of 173 compounds, including FDA-approved antiviral drugs, with good ADME descriptors, and some other nucleotide analogues were screened. The results show that these compounds demonstrate strong binding affinity for the residues at the active sites of RNA-dependent RNA-polymerase (RdRp) modelled structures and Chymotrypsin-like cysteine protease (3CLpro) of the HCoV proteins. Free energies (ΔG's) of binding for SARS-CoV-2 and SARS-CoV RdRp range from -5.4 to -8.8 kcal/mol and -4.9 to -8.7 kcal/mol, respectively. Also, SARS-CoV-2 and SARS-CoV 3CLpro gave ΔG values ranging from − 5.1 to − 8.4 kcal/mol and − 5.5 to − 8.6 kcal/mol, respectively. Interesting results are obtained for ivermectin, an antiparasitic agent with broad spectrum activity, which gave the highest binding energy value (− 8.8 kcal/mol) against the 3CLpro of SARS-CoV-2 and RdRps of both SARS-CoV and SARS-CoV-2. The reason for such high binding energy values is probably due to the presence of hydroxy, methoxy and sugar moieties in its structure. The stability of the protein-ligand complexes of polymerase inhibitors considered in this investigation, such as Sofosbuvir, Remdesivir, Tenofovir, Ribavirin, Galidesivir, 5c3, 5h1 and 7a1, show strong to moderate hydrogen bonding and hydrophobic interactions (π-π stacked, π-π T-shaped, π-sigma and π-alkyl). The stability provided from such interactions translate into greater antiviral activity or inhibitory effect of the ligands. Assessment of the average free energies of binding of the FDA approved drugs are highly comparable for conformers of a particular inhibitor, indicating similar modes of binding within the pockets.
Supplementary Information The online version contains supplementary material available at https:// doi. org/ 10. 1007/ s13721-021-00299-2.
References
Bajji, Davis, Synthesis and biophysical characterization of tRNALys,3 anticodon stem-loop RNAs containing the mcm5s2U nucleoside, Org Lett,
doi:10.1021/ol006605h
Beg, Shivangi, Meena, Structural Prediction and mutational analysis of Rv3906c gene of Mycobacterium tuberculosis H 37 Rv to determine its essentiality in survival, Adv Bioinform,
doi:10.1155/2018/6152014
Ben-Zvi, Kivity, Langevitz, Shoenfeld, Hydroxychloroquine: from malaria to autoimmunity, Clin Rev Allergy Immunol
Biasini, Bienert, Waterhouse, Arnold, Studer et al., SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information, Nucleic Acids Res,
doi:10.1093/nar/gku340
Cao, Xiao, Cao, Li, Kumaki et al., Inhibition of novel reassortant avian influenza H7N9 virus infection in vitro with three antiviral drugs, oseltamivir, peramivir and favipiravir, Antiviral Chem Chemother,
doi:10.3851/IMP2672
Chaccour, Hammann, Ramón-García, Rabinovich, Ivermectin and Novel Coronavirus Disease (COVID-19): Keeping Rigor in Times of Urgency, Am J Trop Med Hygiene,
doi:10.4269/ajtmh.20-0271
Chen, Yiu, Wong, Prediction of the SARS-CoV-2 (2019-nCoV) 3C-like protease (3CL (pro)) structure: virtual screening reveals velpatasvir, ledipasvir, and other drug repurposing candidates, F1000Research,
doi:10.12688/f1000research.22457.1
Cheng, Zhang, Xie, Jiang, Arnold et al., Expression, purification, and characterization of SARS coronavirus RNA polymerase, Virology,
doi:10.1016/j.virol.2005.02.017
Erion, Bullough, Lin, Hong, HepDirect prodrugs for targeting nucleotide-based antiviral drugs to the liver, Curr Opin Investig Drugs
Fantini, Scala, Chahinian, Yahi, Structural and molecular modelling studies reveal a new mechanism of action of chloroquine and hydroxychloroquine against SARS-CoV-2 infection, Int J Antimicrob Agents,
doi:10.1016/j.ijantimicag.2020.105960
Flierl, Nero, Lim, Arthur, Yao et al., Phosphorothioate backbone modifications of nucleotide-based drugs are potent platelet activators, J Exp Med,
doi:10.1084/jem.20140391
Fox, Dixon, Guarrasi, Krubel, Treatment of primary Sjögren's syndrome with hydroxychloroquine: a retrospective, open-label study, Lupus
Fu, Li, Zhang, Strong orbital Interaction in pi-pi Stacking System
Gao, Gao, Yan, Huang, Liu et al., Structure of the RNA-dependent RNA polymerase from COVID-19 virus, Science
Gao, Tian, Yang, Breakthrough: Chloroquine phosphate has shown apparent efficacy in treatment of COVID-19 associated pneumonia in clinical studies, Biosci Trends,
doi:10.5582/bst.2020.01047
Hasan, Hossain, Analysis of COVID-19 M protein for possible clues regarding virion stability , longevity and spreading,
doi:10.31219/osf.io/e7jkc
Henderleiter, Smart, Anderson, Elian, How do organic chemistry students understand and apply hydrogen bonding?, J Chem Educ,
doi:10.1021/ed078p1126
Huang, Bosch, Li, Li, Kyoung et al., SARS coronavirus, but not human coronavirus NL63, utilizes cathepsin L to infect ACE2-expressing cells, J Biol Chem,
doi:10.1074/jbc.M508381200
Jeffrey, An introduction to hydrogen bonding
Khan, Zia, Ashraf, Uddin, Ul-Haq, Identification of chymotrypsin-like protease inhibitors of SARS-CoV-2 via integrated computational approach, J Biomol Struct Dyn,
doi:10.1080/07391102.2020.1751298
Lee, Yang, Parr, Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density, Phys Rev B,
doi:10.1103/PhysRevB.37.785
Li, Moore, Vasilieva, Sui, Wong et al., Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus, Nature,
doi:10.1038/nature02145
Lüthy, Bowie, Eisenberg, Assessment of protein models with three-dimensional profiles, Nature,
doi:10.1038/356083a0
Pamidighantam, Nakandala, Abeysinghe, Wimalasena, Yodage et al., Community science exemplars in SEAGrid science gateway: apache airavata based implementation of advanced infrastructure, Proc Comput Sci,
doi:10.1016/j.procs.2016.05.535
Pettersen, Goddard, Huang, Couch, Greenblatt et al., UCSF Chimera-a visualization system for exploratory research and analysis, J Comput Chem
Prabakaran, Xiao, Dimitrov, A model of the ACE2 structure and function as a SARS-CoV receptor, Biochem Biophys Res Commun,
doi:10.1016/j.bbrc.2003.12.081
Shi, Sivaraman, Song, Mechanism for controlling the dimermonomer switch and coupling dimerization to catalysis of the severe acute respiratory syndrome coronavirus 3C-like protease, J Virol,
doi:10.1128/JVI.02680-07
Solowiej, Thomson, Ryan, Luo, He et al., Steady-State and pre-steady-state kinetic evaluation of severe acute respiratory syndrome coronavirus (SARS-CoV) 3CLpro Cysteine protease: development of an ion-pair model for catalysis, Biochemistry,
doi:10.1021/bi702107v
Trott, Olson, AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading, J Comput Chem,
doi:10.1002/jcc.21334
Van Doremalen, Bushmaker, Morris, Holbrook, Gamble et al., Aerosol and surface stability of SARS-CoV-2 as compared with SARS-CoV-1, N Engl J Med,
doi:10.1056/NEJMc2004973
Walls, Park, Tortorici, Wall, Mcguire et al., Structure, function, and antigenicity of the SARS-CoV-2 spike glycoprotein, Cell,
doi:10.1016/j.cell.2020.02.058
Wang, Cao, Zhang, Yang, Liu et al., Remdesivir and chloroquine effectively inhibit the recently emerged novel coronavirus (2019-nCoV) in vitro, Cell Res,
doi:10.1038/s41422-020-0282-0
Wang, Lai, Wang, Further development and validation of empirical scoring functions for structure-based binding affinity 22 Page 12 of 12 prediction, J Comput Aided Mol Des,
doi:10.1023/A:1016357811882
Wang, Wang, Chen, Qin, Unique epidemiological and clinical features of the emerging 2019 novel coronavirus pneumonia (COVID-19) implicate special control measures, J Med Virol,
doi:10.1002/jmv.25748
Waterhouse, Bertoni, Bienert, Studer, Tauriello et al., SWISS-MODEL: homology modelling of protein structures and complexes, Nucleic Acids Res,
doi:10.1093/nar/gky427
Williams, Headd, Moriarty, Prisant, Videau et al., MolProbity: More and better reference data for improved all-atom structure validation, Protein Sci,
doi:10.1002/pro.3330
Yang, Roy, Zhang, Protein-ligand binding site recognition using complementary binding-specific substructure comparison and sequence profile alignment, Bioinformatics,
doi:10.1093/bioinformatics/btt447
Yang, Yang, Ding, Liu, Lou et al., The crystal structures of severe acute respiratory syndrome virus main protease and its complex with an inhibitor, Proc Natl Acad Sci
DOI record:
{
"DOI": "10.1007/s13721-021-00299-2",
"ISSN": [
"2192-6662",
"2192-6670"
],
"URL": "http://dx.doi.org/10.1007/s13721-021-00299-2",
"alternative-id": [
"299"
],
"article-number": "22",
"assertion": [
{
"group": {
"label": "Article History",
"name": "ArticleHistory"
},
"label": "Received",
"name": "received",
"order": 1,
"value": "31 October 2020"
},
{
"group": {
"label": "Article History",
"name": "ArticleHistory"
},
"label": "Revised",
"name": "revised",
"order": 2,
"value": "25 January 2021"
},
{
"group": {
"label": "Article History",
"name": "ArticleHistory"
},
"label": "Accepted",
"name": "accepted",
"order": 3,
"value": "12 March 2021"
},
{
"group": {
"label": "Article History",
"name": "ArticleHistory"
},
"label": "First Online",
"name": "first_online",
"order": 4,
"value": "25 March 2021"
},
{
"label": "Free to read",
"name": "free",
"value": "This content has been made available to all."
}
],
"author": [
{
"affiliation": [],
"family": "Udofia",
"given": "Inemesit A.",
"sequence": "first"
},
{
"affiliation": [],
"family": "Gbayo",
"given": "Kofoworola O.",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Oloba-Whenu",
"given": "Oluwakemi A.",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Ogunbayo",
"given": "Taofeek B.",
"sequence": "additional"
},
{
"ORCID": "http://orcid.org/0000-0001-6633-6066",
"affiliation": [],
"authenticated-orcid": false,
"family": "Isanbor",
"given": "Chukwuemeka",
"sequence": "additional"
}
],
"container-title": "Network Modeling Analysis in Health Informatics and Bioinformatics",
"container-title-short": "Netw Model Anal Health Inform Bioinforma",
"content-domain": {
"crossmark-restriction": false,
"domain": [
"link.springer.com"
]
},
"created": {
"date-parts": [
[
2021,
3,
25
]
],
"date-time": "2021-03-25T21:59:06Z",
"timestamp": 1616709546000
},
"deposited": {
"date-parts": [
[
2021,
12,
9
]
],
"date-time": "2021-12-09T08:21:50Z",
"timestamp": 1639038110000
},
"indexed": {
"date-parts": [
[
2023,
6,
27
]
],
"date-time": "2023-06-27T19:12:35Z",
"timestamp": 1687893155569
},
"is-referenced-by-count": 5,
"issue": "1",
"issued": {
"date-parts": [
[
2021,
3,
25
]
]
},
"journal-issue": {
"issue": "1",
"published-print": {
"date-parts": [
[
2021,
12
]
]
}
},
"language": "en",
"license": [
{
"URL": "https://www.springer.com/tdm",
"content-version": "tdm",
"delay-in-days": 0,
"start": {
"date-parts": [
[
2021,
3,
25
]
],
"date-time": "2021-03-25T00:00:00Z",
"timestamp": 1616630400000
}
},
{
"URL": "https://www.springer.com/tdm",
"content-version": "vor",
"delay-in-days": 0,
"start": {
"date-parts": [
[
2021,
3,
25
]
],
"date-time": "2021-03-25T00:00:00Z",
"timestamp": 1616630400000
}
}
],
"link": [
{
"URL": "https://link.springer.com/content/pdf/10.1007/s13721-021-00299-2.pdf",
"content-type": "application/pdf",
"content-version": "vor",
"intended-application": "text-mining"
},
{
"URL": "https://link.springer.com/article/10.1007/s13721-021-00299-2/fulltext.html",
"content-type": "text/html",
"content-version": "vor",
"intended-application": "text-mining"
},
{
"URL": "https://link.springer.com/content/pdf/10.1007/s13721-021-00299-2.pdf",
"content-type": "application/pdf",
"content-version": "vor",
"intended-application": "similarity-checking"
}
],
"member": "297",
"original-title": [],
"prefix": "10.1007",
"published": {
"date-parts": [
[
2021,
3,
25
]
]
},
"published-online": {
"date-parts": [
[
2021,
3,
25
]
]
},
"published-print": {
"date-parts": [
[
2021,
12
]
]
},
"publisher": "Springer Science and Business Media LLC",
"reference": [
{
"DOI": "10.1038/s41591-020-0820-9",
"author": "KG Andersen",
"doi-asserted-by": "publisher",
"first-page": "44",
"issue": "1",
"journal-title": "Nat Med",
"key": "299_CR1",
"unstructured": "Andersen KG, Rambaut A, Lipkin WI, Holmes EC, Garry RF (2020) The proximal origin of SARS-CoV-2. Nat Med 89(1):44–48. https://doi.org/10.1038/s41591-020-0820-9",
"volume": "89",
"year": "2020"
},
{
"DOI": "10.1021/ol006605h",
"author": "AC Bajji",
"doi-asserted-by": "publisher",
"first-page": "3865",
"issue": "24",
"journal-title": "Org Lett",
"key": "299_CR2",
"unstructured": "Bajji AC, Davis DR (2000) Synthesis and biophysical characterization of tRNALys,3 anticodon stem-loop RNAs containing the mcm5s2U nucleoside. Org Lett 2(24):3865–3868. https://doi.org/10.1021/ol006605h",
"volume": "2",
"year": "2000"
},
{
"DOI": "10.1155/2018/6152014",
"author": "MA Beg",
"doi-asserted-by": "publisher",
"journal-title": "Adv Bioinform",
"key": "299_CR3",
"unstructured": "Beg MA, Shivangi TSC, Meena LS (2018) Structural Prediction and mutational analysis of Rv3906c gene of Mycobacterium tuberculosis H37Rv to determine its essentiality in survival. Adv Bioinform. https://doi.org/10.1155/2018/6152014",
"year": "2018"
},
{
"DOI": "10.1007/s12016-010-8243-x",
"author": "I Ben-Zvi",
"doi-asserted-by": "publisher",
"first-page": "145",
"issue": "2",
"journal-title": "Clin Rev Allergy Immunol",
"key": "299_CR01",
"unstructured": "Ben-Zvi I, Kivity S, Langevitz P, Shoenfeld Y (2012) Hydroxychloroquine: from malaria to autoimmunity. Clin Rev Allergy Immunol 42(2):145–153",
"volume": "42",
"year": "2012"
},
{
"DOI": "10.1093/nar/gku340",
"author": "M Biasini",
"doi-asserted-by": "publisher",
"first-page": "W252",
"issue": "W1",
"journal-title": "Nucleic Acids Res",
"key": "299_CR4",
"unstructured": "Biasini M, Bienert S, Waterhouse A, Arnold K, Studer G, Schmidt T, Kiefer F, Cassarino TG, Bertoni M, Bordoli L, Schwede T (2014) SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res 42(W1):W252–W258. https://doi.org/10.1093/nar/gku340",
"volume": "42",
"year": "2014"
},
{
"DOI": "10.1016/j.antiviral.2020.104787",
"author": "L Caly",
"doi-asserted-by": "publisher",
"journal-title": "Antivir Res",
"key": "299_CR5",
"unstructured": "Caly L, Druce JD, Catton MG, Jans DA, Wagstaff KM (2020) The FDA-approved Drug Ivermectin inhibits the replication of SARS-CoV-2 in vitro. Antivir Res. https://doi.org/10.1016/j.antiviral.2020.104787",
"year": "2020"
},
{
"DOI": "10.3851/IMP2672",
"author": "R-Y Cao",
"doi-asserted-by": "publisher",
"first-page": "237",
"issue": "6",
"journal-title": "Antiviral Chem Chemother",
"key": "299_CR6",
"unstructured": "Cao R-Y, Xiao J-H, Cao B, Li S, Kumaki Y, Zhong W (2014) Inhibition of novel reassortant avian influenza H7N9 virus infection in vitro with three antiviral drugs, oseltamivir, peramivir and favipiravir. Antiviral Chem Chemother 23(6):237–240. https://doi.org/10.3851/IMP2672",
"volume": "23",
"year": "2014"
},
{
"DOI": "10.4269/ajtmh.20-0271",
"author": "C Chaccour",
"doi-asserted-by": "publisher",
"journal-title": "Am J Trop Med Hygiene",
"key": "299_CR7",
"unstructured": "Chaccour C, Hammann F, Ramón-García S, Rabinovich NR (2020) Ivermectin and Novel Coronavirus Disease (COVID-19): Keeping Rigor in Times of Urgency. Am J Trop Med Hygiene. https://doi.org/10.4269/ajtmh.20-0271",
"year": "2020"
},
{
"DOI": "10.3978/j.issn.2072-1439.2013.06.19",
"author": "PKS Chan",
"doi-asserted-by": "publisher",
"first-page": "S118",
"issue": "Suppl 2",
"journal-title": "J Thorac Dis",
"key": "299_CR8",
"unstructured": "Chan PKS, Chan MCW (2013) Tracing the SARS-coronavirus. J Thorac Dis 5 Suppl 2(Suppl 2):S118–S121. https://doi.org/10.3978/j.issn.2072-1439.2013.06.19",
"volume": "5 Suppl 2",
"year": "2013"
},
{
"DOI": "10.12688/f1000research.22457.1",
"author": "YW Chen",
"doi-asserted-by": "publisher",
"first-page": "129",
"journal-title": "F1000Research",
"key": "299_CR9",
"unstructured": "Chen YW, Yiu C-PB, Wong K-Y (2020) Prediction of the SARS-CoV-2 (2019-nCoV) 3C-like protease (3CL (pro)) structure: virtual screening reveals velpatasvir, ledipasvir, and other drug repurposing candidates. F1000Research 9:129. https://doi.org/10.12688/f1000research.22457.1",
"volume": "9",
"year": "2020"
},
{
"DOI": "10.1016/j.virol.2005.02.017",
"author": "A Cheng",
"doi-asserted-by": "publisher",
"first-page": "165",
"issue": "2",
"journal-title": "Virology",
"key": "299_CR10",
"unstructured": "Cheng A, Zhang W, Xie Y, Jiang W, Arnold E, Sarafianos SG, Ding J (2005) Expression, purification, and characterization of SARS coronavirus RNA polymerase. Virology 335(2):165–176. https://doi.org/10.1016/j.virol.2005.02.017",
"volume": "335",
"year": "2005"
},
{
"DOI": "10.1016/j.ijantimicag.2020.105932",
"author": "P Colson",
"doi-asserted-by": "publisher",
"journal-title": "Int J Antimicrob Agents",
"key": "299_CR11",
"unstructured": "Colson P, Rolain JM, Lagier JC, Brouqui P, Raoult D (2020) Chloroquine and hydroxychloroquine as available weapons to fight COVID-19. Int J Antimicrob Agents. https://doi.org/10.1016/j.ijantimicag.2020.105932",
"year": "2020"
},
{
"DOI": "10.1016/bs.aivir.2018.01.001",
"doi-asserted-by": "publisher",
"key": "299_CR12",
"unstructured": "Corman VM, Muth D, Niemeyer D, Drosten C (2018) Hosts and sources of endemic human coronaviruses. In: Advances in virus research, vol. 100. Elsevier Inc., pp 163–188. https://doi.org/10.1016/bs.aivir.2018.01.001"
},
{
"DOI": "10.1007/978-1-4939-2269-7_19",
"author": "S Dallakyan",
"doi-asserted-by": "publisher",
"first-page": "243",
"key": "299_CR13",
"unstructured": "Dallakyan S, Olson AJ (2015) Small-molecule library screening by docking with PyRx BT—chemical biology: methods and protocols. In: Hempel JE, Williams CH, Hong CC (eds) Chemical biology. Springer New York, pp 243–250. https://doi.org/10.1007/978-1-4939-2269-7_19",
"volume-title": "Chemical biology",
"year": "2015"
},
{
"key": "299_CR14",
"unstructured": "Erion MD, Bullough DA, Lin C-C, Hong Z (2006). HepDirect prodrugs for targeting nucleotide-based antiviral drugs to the liver. Curr Opin Investig Drugs (London, England : 2000) 7(2): 109–117. http://europepmc.org/abstract/MED/16499280. Accessed 23 Apr 2020"
},
{
"DOI": "10.1016/j.ijantimicag.2020.105960",
"author": "J Fantini",
"doi-asserted-by": "publisher",
"journal-title": "Int J Antimicrob Agents",
"key": "299_CR15",
"unstructured": "Fantini J, Di Scala C, Chahinian H, Yahi N (2020) Structural and molecular modelling studies reveal a new mechanism of action of chloroquine and hydroxychloroquine against SARS-CoV-2 infection. Int J Antimicrob Agents. https://doi.org/10.1016/j.ijantimicag.2020.105960",
"year": "2020"
},
{
"DOI": "10.1084/jem.20140391",
"author": "U Flierl",
"doi-asserted-by": "publisher",
"first-page": "129",
"issue": "2",
"journal-title": "J Exp Med",
"key": "299_CR16",
"unstructured": "Flierl U, Nero TL, Lim B, Arthur JF, Yao Y, Jung SM, Gitz E, Pollitt AY, Zaldivia MTK, Jandrot-Perrus M, Schäfer A, Nieswandt B, Andrews RK, Parker MW, Gardiner EE, Peter K (2015) Phosphorothioate backbone modifications of nucleotide-based drugs are potent platelet activators. J Exp Med 212(2):129–137. https://doi.org/10.1084/jem.20140391",
"volume": "212",
"year": "2015"
},
{
"DOI": "10.1177/0961203396005001081",
"author": "RI Fox",
"doi-asserted-by": "publisher",
"first-page": "31",
"issue": "1_suppl",
"journal-title": "Lupus",
"key": "299_CR02",
"unstructured": "Fox RI, Dixon R, Guarrasi V, Krubel S (1996) Treatment of primary Sjögren's syndrome with hydroxychloroquine: a retrospective, open-label study. Lupus 5(1_suppl):31–36",
"volume": "5",
"year": "1996"
},
{
"key": "299_CR17",
"unstructured": "Fu X-X, Li J-F, Zhang R-Q (2016) Strong orbital Interaction in pi-pi Stacking System. In: arXiv e-prints arXiv:1601.01150. https://ui.adsabs.harvard.edu/abs/2016arXiv160101150F. Accessed 23 Apr 2020"
},
{
"DOI": "10.5582/bst.2020.01047",
"author": "J Gao",
"doi-asserted-by": "publisher",
"first-page": "72",
"issue": "1",
"journal-title": "Biosci Trends",
"key": "299_CR18",
"unstructured": "Gao J, Tian Z, Yang X (2020a) Breakthrough: Chloroquine phosphate has shown apparent efficacy in treatment of COVID-19 associated pneumonia in clinical studies. Biosci Trends 14(1):72–73. https://doi.org/10.5582/bst.2020.01047",
"volume": "14",
"year": "2020"
},
{
"DOI": "10.1126/science.abb7498",
"author": "Y Gao",
"doi-asserted-by": "publisher",
"first-page": "779",
"issue": "6492",
"journal-title": "Science",
"key": "299_CR19",
"unstructured": "Gao Y, Gao Y, Yan L, Huang Y, Liu F, Zhao Y, Cao L, Wang T, Sun Q, Ming Z, Zhang L, Ge J, Zheng L, Zhang Y, Wang H, Zhu Y, Zhu C, Wang Q, Lou Z, Rao Z (2020b) Structure of the RNA-dependent RNA polymerase from COVID-19 virus. Science 368(6492):779–782",
"volume": "368",
"year": "2020"
},
{
"DOI": "10.31219/osf.io/e7jkc",
"doi-asserted-by": "publisher",
"key": "299_CR20",
"unstructured": "Hasan S, Hossain MM (2020) Analysis of COVID-19 M protein for possible clues regarding virion stability , longevity and spreading. https://doi.org/10.31219/osf.io/e7jkc"
},
{
"DOI": "10.1021/ed078p1126",
"author": "J Henderleiter",
"doi-asserted-by": "publisher",
"first-page": "1126",
"issue": "8",
"journal-title": "J Chem Educ",
"key": "299_CR21",
"unstructured": "Henderleiter J, Smart R, Anderson J, Elian O (2001) How do organic chemistry students understand and apply hydrogen bonding? J Chem Educ 78(8):1126. https://doi.org/10.1021/ed078p1126",
"volume": "78",
"year": "2001"
},
{
"DOI": "10.1074/jbc.M508381200",
"author": "IC Huang",
"doi-asserted-by": "publisher",
"first-page": "3198",
"issue": "6",
"journal-title": "J Biol Chem",
"key": "299_CR22",
"unstructured": "Huang IC, Bosch BJ, Li F, Li W, Kyoung HL, Ghiran S, Vasilieva N, Dermody TS, Harrison SC, Dormitzer PR, Farzan M, Rottier PJM, Choe H (2006) SARS coronavirus, but not human coronavirus NL63, utilizes cathepsin L to infect ACE2-expressing cells. J Biol Chem 281(6):3198–3203. https://doi.org/10.1074/jbc.M508381200",
"volume": "281",
"year": "2006"
},
{
"key": "299_CR23",
"unstructured": "Jeffrey GA (1997) An introduction to hydrogen bonding (12th ed.). Oxford University Press. https://books.google.fr/books?id=ZRAFifo37QsC. Accessed 23 Apr 2020"
},
{
"DOI": "10.1038/s41586-020-2223-y",
"author": "Z Jin",
"doi-asserted-by": "publisher",
"first-page": "289",
"issue": "7811",
"journal-title": "Nature",
"key": "299_CR24",
"unstructured": "Jin Z, Du X, Xu Y, Deng Y, Liu M, Zhao Y, Zhang B, Li X, Zhang L, Peng C, Duan Y, Yu J, Wang L, Yang K, Liu F, Jiang R, Yang X, You T, Liu X, Yang H (2020) Structure of Mpro from SARS-CoV-2 and discovery of its inhibitors. Nature 582(7811):289–293. https://doi.org/10.1038/s41586-020-2223-y",
"volume": "582",
"year": "2020"
},
{
"DOI": "10.1101/2020.01.30.927574",
"author": "J Ju",
"doi-asserted-by": "publisher",
"journal-title": "BioRxiv",
"key": "299_CR25",
"unstructured": "Ju J, Kumar S, Li X, Jockusch S, Russo JJ (2020a) Nucleotide analogues as inhibitors of viral polymerases. BioRxiv. https://doi.org/10.1101/2020.01.30.927574",
"year": "2020"
},
{
"DOI": "10.1101/2020.03.12.989186",
"author": "J Ju",
"doi-asserted-by": "publisher",
"journal-title": "BioRxiv",
"key": "299_CR26",
"unstructured": "Ju J, Li X, Kumar S, Jockusch S, Chien M, Tao C, Morozova I, Kalachikov S, Kirchdoerfer RN, Russo JJ (2020b) Nucleotide Analogues as Inhibitors of SARS-CoV Polymerase. BioRxiv. https://doi.org/10.1101/2020.03.12.989186",
"year": "2020"
},
{
"DOI": "10.1080/07391102.2020.1751298",
"author": "SA Khan",
"doi-asserted-by": "publisher",
"first-page": "1",
"issue": "1",
"journal-title": "J Biomol Struct Dyn",
"key": "299_CR27",
"unstructured": "Khan SA, Zia K, Ashraf S, Uddin R, Ul-Haq Z (2020) Identification of chymotrypsin-like protease inhibitors of SARS-CoV-2 via integrated computational approach. J Biomol Struct Dyn 9(1):1–10. https://doi.org/10.1080/07391102.2020.1751298",
"volume": "9",
"year": "2020"
},
{
"DOI": "10.1038/s41467-019-10280-3",
"author": "RN Kirchdoerfer",
"doi-asserted-by": "publisher",
"first-page": "1",
"issue": "1",
"journal-title": "Nat Commun",
"key": "299_CR28",
"unstructured": "Kirchdoerfer RN, Ward AB (2019) Structure of the SARS-CoV nsp12 polymerase bound to nsp7 and nsp8 co-factors. Nat Commun 10(1):1–9. https://doi.org/10.1038/s41467-019-10280-3",
"volume": "10",
"year": "2019"
},
{
"DOI": "10.1103/PhysRevB.37.785",
"author": "C Lee",
"doi-asserted-by": "publisher",
"first-page": "785",
"issue": "2",
"journal-title": "Phys Rev B",
"key": "299_CR29",
"unstructured": "Lee C, Yang W, Parr RG (1988) Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density. Phys Rev B 37(2):785–789. https://doi.org/10.1103/PhysRevB.37.785",
"volume": "37",
"year": "1988"
},
{
"DOI": "10.1038/d41573-020-00016-0",
"author": "G Li",
"doi-asserted-by": "publisher",
"first-page": "149",
"issue": "3",
"journal-title": "Nat Rev Drug Discov",
"key": "299_CR30",
"unstructured": "Li G, De Clercq E (2020) Therapeutic options for the 2019 novel coronavirus (2019-nCoV). Nat Rev Drug Discov 19(3):149–150. https://doi.org/10.1038/d41573-020-00016-0",
"volume": "19",
"year": "2020"
},
{
"DOI": "10.1038/nature02145",
"author": "W Li",
"doi-asserted-by": "publisher",
"first-page": "450",
"issue": "6965",
"journal-title": "Nature",
"key": "299_CR31",
"unstructured": "Li W, Moore MJ, Vasilieva N, Sui J, Wong SK, Berne MA, Somasundaran M, Sullivan JL, Luzuriaga K, Greenough TC, Choe H, Farzan M (2003) Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 426(6965):450–454. https://doi.org/10.1038/nature02145",
"volume": "426",
"year": "2003"
},
{
"DOI": "10.1038/356083a0",
"author": "R Lüthy",
"doi-asserted-by": "publisher",
"first-page": "83",
"issue": "6364",
"journal-title": "Nature",
"key": "299_CR32",
"unstructured": "Lüthy R, Bowie JU, Eisenberg D (1992) Assessment of protein models with three-dimensional profiles. Nature 356(6364):83–85. https://doi.org/10.1038/356083a0",
"volume": "356",
"year": "1992"
},
{
"DOI": "10.1016/j.antiviral.2017.02.004",
"author": "B Martin",
"doi-asserted-by": "publisher",
"first-page": "48",
"journal-title": "Antivir Res",
"key": "299_CR33",
"unstructured": "Martin B, Canard B, Decroly E (2017) Filovirus proteins for antiviral drug discovery: Structure/function bases of the replication cycle. Antivir Res 141:48–61. https://doi.org/10.1016/j.antiviral.2017.02.004",
"volume": "141",
"year": "2017"
},
{
"DOI": "10.1039/C2SC20045G",
"author": "CR Martinez",
"doi-asserted-by": "publisher",
"first-page": "2191",
"issue": "7",
"journal-title": "Chem Sci",
"key": "299_CR34",
"unstructured": "Martinez CR, Iverson BL (2012) Rethinking the term “pi-stacking.” Chem Sci 3(7):2191–2201. https://doi.org/10.1039/C2SC20045G",
"volume": "3",
"year": "2012"
},
{
"DOI": "10.1016/S0065-3527(06)66005-3",
"author": "PS Masters",
"doi-asserted-by": "publisher",
"first-page": "193",
"issue": "06",
"journal-title": "Adv Virus Res",
"key": "299_CR35",
"unstructured": "Masters PS (2006) The molecular biology of coronaviruses. Adv Virus Res 65(06):193–292. https://doi.org/10.1016/S0065-3527(06)66005-3",
"volume": "65",
"year": "2006"
},
{
"DOI": "10.1016/j.procs.2016.05.535",
"author": "S Pamidighantam",
"doi-asserted-by": "publisher",
"first-page": "1927",
"journal-title": "Proc Comput Sci",
"key": "299_CR36",
"unstructured": "Pamidighantam S, Nakandala S, Abeysinghe E, Wimalasena C, Yodage SR, Marru S, Pierce M (2016) Community science exemplars in SEAGrid science gateway: apache airavata based implementation of advanced infrastructure. Proc Comput Sci 80:1927–1939. https://doi.org/10.1016/j.procs.2016.05.535",
"volume": "80",
"year": "2016"
},
{
"DOI": "10.1007/s00726-007-0015-4",
"author": "SK Panigrahi",
"doi-asserted-by": "publisher",
"first-page": "617",
"issue": "4",
"journal-title": "Amino Acids",
"key": "299_CR37",
"unstructured": "Panigrahi SK (2008) Strong and weak hydrogen bonds in protein-ligand complexes of kinases: a comparative study. Amino Acids 34(4):617–633. https://doi.org/10.1007/s00726-007-0015-4",
"volume": "34",
"year": "2008"
},
{
"DOI": "10.1016/B978-0-12-815422-9.00014-0",
"author": "VM Patil",
"doi-asserted-by": "publisher",
"first-page": "387",
"key": "299_CR38",
"unstructured": "Patil VM, Balasubramanian K, Masand N (2019) Chapter 14—dengue virus polymerase: a crucial target for antiviral drug discovery. In: Gupta SPBT-VP (ed) Viral polymerases. Academic Press, pp 387–428. https://doi.org/10.1016/B978-0-12-815422-9.00014-0",
"volume-title": "Viral polymerases",
"year": "2019"
},
{
"DOI": "10.1385/0-89603-246-9:307",
"author": "WR Pearson",
"doi-asserted-by": "publisher",
"first-page": "307",
"key": "299_CR39",
"unstructured": "Pearson WR (1994) Using the FASTA program to search protein and DNA sequence databases. In: Griffin AM, Griffin HG (eds) Computer analysis of sequence data. Humana Press, pp 307–331. https://doi.org/10.1385/0-89603-246-9:307",
"volume-title": "Computer analysis of sequence data",
"year": "1994"
},
{
"DOI": "10.1002/jcc.20084",
"author": "EF Pettersen",
"doi-asserted-by": "publisher",
"first-page": "1605",
"journal-title": "J Comput Chem",
"key": "299_CR40",
"unstructured": "Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE (2004) UCSF Chimera—a visualization system for exploratory research and analysis. J Comput Chem 25:1605",
"volume": "25",
"year": "2004"
},
{
"DOI": "10.1016/j.bbrc.2003.12.081",
"author": "P Prabakaran",
"doi-asserted-by": "publisher",
"first-page": "235",
"issue": "1",
"journal-title": "Biochem Biophys Res Commun",
"key": "299_CR41",
"unstructured": "Prabakaran P, Xiao X, Dimitrov DS (2004) A model of the ACE2 structure and function as a SARS-CoV receptor. Biochem Biophys Res Commun 314(1):235–241. https://doi.org/10.1016/j.bbrc.2003.12.081",
"volume": "314",
"year": "2004"
},
{
"DOI": "10.1016/S1574-1400(05)01009-1",
"doi-asserted-by": "publisher",
"key": "299_CR42",
"unstructured": "Raha K, Merz KMBT-ARC C (2005) Chapter 9 Calculating binding free energy in protein–ligand interaction. In: Annual reports in computational chemistry, vol. 1. Elsevier, pp. 113–130. https://doi.org/10.1016/S1574-1400(05)01009-1"
},
{
"DOI": "10.1128/JVI.02680-07",
"author": "J Shi",
"doi-asserted-by": "publisher",
"first-page": "4620LP",
"issue": "9",
"journal-title": "J Virol",
"key": "299_CR43",
"unstructured": "Shi J, Sivaraman J, Song J (2008) Mechanism for controlling the dimer-monomer switch and coupling dimerization to catalysis of the severe acute respiratory syndrome coronavirus 3C-like protease. J Virol 82(9):4620LP – 4629. https://doi.org/10.1128/JVI.02680-07",
"volume": "82",
"year": "2008"
},
{
"DOI": "10.1021/bi702107v",
"author": "J Solowiej",
"doi-asserted-by": "publisher",
"first-page": "2617",
"issue": "8",
"journal-title": "Biochemistry",
"key": "299_CR44",
"unstructured": "Solowiej J, Thomson JA, Ryan K, Luo C, He M, Lou J, Murray BW (2008) Steady-State and pre-steady-state kinetic evaluation of severe acute respiratory syndrome coronavirus (SARS-CoV) 3CLpro Cysteine protease: development of an ion-pair model for catalysis. Biochemistry 47(8):2617–2630. https://doi.org/10.1021/bi702107v",
"volume": "47",
"year": "2008"
},
{
"DOI": "10.1099/0022-1317-69-12-2939",
"author": "W Spaan",
"doi-asserted-by": "publisher",
"first-page": "2939",
"issue": "12",
"journal-title": "J Gen Virol",
"key": "299_CR45",
"unstructured": "Spaan W, Cavanagh D, Horzinek MC (1988) Coronaviruses: structure and genome expression. J Gen Virol 69(12):2939–2952. https://doi.org/10.1099/0022-1317-69-12-2939",
"volume": "69",
"year": "1988"
},
{
"DOI": "10.3390/molecules22071038",
"author": "V Spiwok",
"doi-asserted-by": "publisher",
"journal-title": "Molecules",
"key": "299_CR46",
"unstructured": "Spiwok V (2017) CH/π Interactions in Carbohydrate Recognition. Molecules. https://doi.org/10.3390/molecules22071038",
"year": "2017"
},
{
"DOI": "10.1016/B978-0-12-815422-9.00003-6",
"author": "S Tomar",
"doi-asserted-by": "publisher",
"first-page": "69",
"key": "299_CR47",
"unstructured": "Tomar S, Mudgal R, Pareek A (2019) Chapter 3—RNA-dependent RNA polymerase of alphaviruses: a potential target for the design of drugs against alphaviruses. In: Gupta SPBT-VP (ed) Viral polymerases. Academic Press, pp 69–94. https://doi.org/10.1016/B978-0-12-815422-9.00003-6",
"volume-title": "Viral polymerases",
"year": "2019"
},
{
"DOI": "10.1016/j.antiviral.2020.104762",
"author": "F Touret",
"doi-asserted-by": "publisher",
"first-page": "104762",
"journal-title": "Antivir Res",
"key": "299_CR48",
"unstructured": "Touret F, de Lamballerie X (2020) Of chloroquine and COVID-19. Antivir Res 177:104762. https://doi.org/10.1016/j.antiviral.2020.104762",
"volume": "177",
"year": "2020"
},
{
"DOI": "10.1002/jcc.21334",
"author": "O Trott",
"doi-asserted-by": "publisher",
"first-page": "455",
"issue": "2",
"journal-title": "J Comput Chem",
"key": "299_CR49",
"unstructured": "Trott O, Olson AJ (2010) AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J Comput Chem 31(2):455–461. https://doi.org/10.1002/jcc.21334",
"volume": "31",
"year": "2010"
},
{
"DOI": "10.1056/NEJMc2004973",
"author": "N van Doremalen",
"doi-asserted-by": "publisher",
"first-page": "1564",
"issue": "16",
"journal-title": "N Engl J Med",
"key": "299_CR50",
"unstructured": "van Doremalen N, Bushmaker T, Morris DH, Holbrook MG, Gamble A, Williamson BN, Tamin A, Harcourt JL, Thornburg NJ, Gerber SI, Lloyd-Smith JO, de Wit E, Munster VJ (2020) Aerosol and surface stability of SARS-CoV-2 as compared with SARS-CoV-1. N Engl J Med 382(16):1564–1567. https://doi.org/10.1056/NEJMc2004973",
"volume": "382",
"year": "2020"
},
{
"DOI": "10.1016/j.cell.2020.02.058",
"author": "AC Walls",
"doi-asserted-by": "publisher",
"first-page": "1",
"journal-title": "Cell",
"key": "299_CR51",
"unstructured": "Walls AC, Park Y-J, Tortorici MA, Wall A, McGuire AT, Veesler D (2020) Structure, function, and antigenicity of the SARS-CoV-2 spike glycoprotein. Cell 180:1–12. https://doi.org/10.1016/j.cell.2020.02.058",
"volume": "180",
"year": "2020"
},
{
"DOI": "10.1023/A:1016357811882",
"author": "R Wang",
"doi-asserted-by": "publisher",
"first-page": "11",
"issue": "1",
"journal-title": "J Comput Aided Mol Des",
"key": "299_CR53",
"unstructured": "Wang R, Lai L, Wang S (2002) Further development and validation of empirical scoring functions for structure-based binding affinity prediction. J Comput Aided Mol Des 16(1):11–26. https://doi.org/10.1023/A:1016357811882",
"volume": "16",
"year": "2002"
},
{
"DOI": "10.1038/s41422-020-0282-0",
"author": "M Wang",
"doi-asserted-by": "publisher",
"first-page": "269",
"issue": "3",
"journal-title": "Cell Res",
"key": "299_CR52",
"unstructured": "Wang M, Cao R, Zhang L, Yang X, Liu J, Xu M, Shi Z, Hu Z, Zhong W, Xiao G (2020a) Remdesivir and chloroquine effectively inhibit the recently emerged novel coronavirus (2019-nCoV) in vitro. Cell Res 30(3):269–271. https://doi.org/10.1038/s41422-020-0282-0",
"volume": "30",
"year": "2020"
},
{
"DOI": "10.1002/jmv.25748",
"author": "Y Wang",
"doi-asserted-by": "publisher",
"journal-title": "J Med Virol",
"key": "299_CR54",
"unstructured": "Wang Y, Wang Y, Chen Y, Qin Q (2020b) Unique epidemiological and clinical features of the emerging 2019 novel coronavirus pneumonia (COVID-19) implicate special control measures. J Med Virol. https://doi.org/10.1002/jmv.25748",
"year": "2020"
},
{
"DOI": "10.1093/nar/gky427",
"author": "A Waterhouse",
"doi-asserted-by": "publisher",
"first-page": "296",
"issue": "1",
"journal-title": "Nucleic Acids Res",
"key": "299_CR55",
"unstructured": "Waterhouse A, Bertoni M, Bienert S, Studer G, Tauriello G, Gumienny R, Heer FT, de Beer TAP, Rempfer C, Bordoli L, Lepore R, Schwede T (2018) SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res 46(1):296-W303. https://doi.org/10.1093/nar/gky427",
"volume": "46",
"year": "2018"
},
{
"DOI": "10.1093/nar/gkz966",
"doi-asserted-by": "publisher",
"key": "299_CR56",
"unstructured": "WHO (2020) Coronavirus disease (COVID-2019) situation reports 318. https://doi.org/10.1093/nar/gkz966"
},
{
"DOI": "10.1002/pro.3330",
"author": "CJ Williams",
"doi-asserted-by": "publisher",
"first-page": "293",
"issue": "1",
"journal-title": "Protein Sci",
"key": "299_CR57",
"unstructured": "Williams CJ, Headd JJ, Moriarty NW, Prisant MG, Videau LL, Deis LN, Verma V, Keedy DA, Hintze BJ, Chen VB, Jain S, Lewis SM, Arendall WB III, Snoeyink J, Adams PD, Lovell SC, Richardson JS, Richardson DC (2018) MolProbity: More and better reference data for improved all-atom structure validation. Protein Sci 27(1):293–315. https://doi.org/10.1002/pro.3330",
"volume": "27",
"year": "2018"
},
{
"DOI": "10.1073/pnas.1835675100",
"author": "H Yang",
"doi-asserted-by": "publisher",
"first-page": "13190",
"issue": "23",
"journal-title": "Proc Natl Acad Sci USA",
"key": "299_CR58",
"unstructured": "Yang H, Yang M, Ding Y, Liu Y, Lou Z, Zhou Z, Sun L, Mo L, Ye S, Pang H, Gao GF, Anand K, Bartlam M, Hilgenfeld R, Rao Z (2003) The crystal structures of severe acute respiratory syndrome virus main protease and its complex with an inhibitor. Proc Natl Acad Sci USA 100(23):13190–13195",
"volume": "100",
"year": "2003"
},
{
"DOI": "10.1093/bioinformatics/btt447",
"author": "J Yang",
"doi-asserted-by": "publisher",
"first-page": "2588",
"issue": "20",
"journal-title": "Bioinformatics",
"key": "299_CR59",
"unstructured": "Yang J, Roy A, Zhang Y (2013) Protein–ligand binding site recognition using complementary binding-specific substructure comparison and sequence profile alignment. Bioinformatics 29(20):2588–2595. https://doi.org/10.1093/bioinformatics/btt447",
"volume": "29",
"year": "2013"
}
],
"reference-count": 61,
"references-count": 61,
"relation": {},
"resource": {
"primary": {
"URL": "https://link.springer.com/10.1007/s13721-021-00299-2"
}
},
"score": 1,
"short-title": [],
"source": "Crossref",
"subject": [],
"subtitle": [],
"title": "In silico studies of selected multi-drug targeting against 3CLpro and nsp12 RNA-dependent RNA-polymerase proteins of SARS-CoV-2 and SARS-CoV",
"type": "journal-article",
"update-policy": "http://dx.doi.org/10.1007/springer_crossmark_policy",
"volume": "10"
}