Molecular insights into the interaction of apo-lactoferrin with the receptor binding domain of the SARS-CoV-2 spike protein: a molecular dynamics simulation study

References

• Abraham, M. J. (2015). GROMACS: High performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX, 1-2, 19–25. https://doi.org/10.1016/j.softx.2015.06.001
   Google Scholar
• Baker, N. A., Sept, D., Joseph, S., Holst, M. J., & McCammon, J. A. (2001). Electrostatics of nanosystems: Application to microtubules and the ribosome. Proceedings of the National Academy of Sciences of the United States of America, 98(18), 10037–10041. doi:10.1073/pnas.181342398.
   PubMed Web of Science ®Google Scholar
• Bellamy, W., Takase, M., Yamauchi, K., Wakabayashi, H., Kawase, K., & Tomita, M. (1992). Identification of the bactericidal domain of lactoferrin. Biochimica et Biophysica Acta, 1121(1-2), 130–136. https://doi.org/10.1016/0167-4838(92)90346-f
   PubMedGoogle Scholar
• Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., DiNola, A., & Haak, J. R. (1984). Molecular dynamics with coupling to an external bath. The Journal of Chemical Physics, 81(8), 3684–3690. https://doi.org/10.1063/1.448118
   Web of Science ®Google Scholar
• Bjelkmar, P., Larsson, P., Cuendet, M. A., Hess, B., & Lindahl, E. (2010). Implementation of the CHARMM force field in GROMACS: analysis of protein stability effects from correction maps, virtual interaction sites, and water models. Journal of Chemical Theory and Computation, 6(2), 459–466. doi:10.1021/ct900549r.
   PubMed Web of Science ®Google Scholar
• Campione, E., Lanna, C., Cosio, T., Rosa, L., Conte, M. P., Iacovelli, F., Romeo, A., Falconi, M., Del Vecchio, C., Franchin, E., Lia, M. S., Minieri, M., Chiaramonte, C., Ciotti, M., Nuccetelli, M., Terrinoni, A., Iannuzzi, I., Coppeda, L., Magrini, A., … Bianchi, L. (2021). Lactoferrin against SARS-CoV-2: In vitro and in silico evidences. Frontiers in Pharmacology, 12, 666600. doi:10.3389/fphar.2021.666600.
   PubMed Web of Science ®Google Scholar
• Chang, R., Ng, T. B., & Sun, W.-Z. (2020). Lactoferrin as potential preventative and adjunct treatment for COVID-19. International Journal of Antimicrobial Agents, 56(3), 106118. doi:10.1016/j.ijantimicag.2020.106118.
   PubMed Web of Science ®Google Scholar
• Chen, P.-W., Jheng, T. T., Shyu, C.-L., & Mao, F. C. (2013). Antimicrobial potential for the combination of bovine lactoferrin or its hydrolysate with lactoferrin-resistant probiotics against foodborne pathogens. Journal of Dairy Science, 96(3), 1438–1446. doi:10.3168/jds.2012-6112.
   PubMed Web of Science ®Google Scholar
• Coronaviridae Study Group of the International Committee on Taxonomy of Viruses. (2020). The species Severe acute respiratory syndrome-related coronavirus: classifying 2019-nCoV and naming it SARS-CoV-2. Nature Microbiology, 5(4), 536–544. https://doi.org/10.1038/s41564-020-0695-z
   PubMed Web of Science ®Google Scholar
• Darmawan, K. K., Karagiannis, T. C., Hughes, J. G., Small, D. M., & Hung, A. (2021). Computational design of de novo nutraceuticals: Effects of spray drying temperatures on the interaction between apo-lactoferrin whey protein complex and the peptidoglycan layer in lactic acid bacteria. LWT - Food Science and Technology, 151, 112246. https://doi.org/10.1016/j.lwt.2021.112246
   Web of Science ®Google Scholar
• Darmawan, K. K., Karagiannis, T. C., Hughes, J. G., Small, D. M., & Hung, A. (2022). Molecular modeling of lactoferrin for food and nutraceutical applications: insights from in silico techniques. Critical Reviews in Food Science and Nutrition, 1–24. https://doi.org/10.1080/10408398.2022.2067824
   Google Scholar
• Darmawan, K. K., Karagiannis, T. C., Hughes, J. G., Small, D. M., & Hung, A. (2021). In silico modelling of apo-lactoferrin under simulated gastric conditions: structural dynamics, binding with β-lactoglobulin and α-lactalbumin, and functional implications. LWT - Food Science and Technology, 148, 111726. https://doi.org/10.1016/j.lwt.2021.111726
   Web of Science ®Google Scholar
• Darmawan, K. K., Karagiannis, T. C., Hughes, J. G., Small, D. M., & Hung, A. (2020). High temperature induced structural changes of apo-lactoferrin and interactions with β-lactoglobulin and α-lactalbumin for potential encapsulation strategies. Food Hydrocolloids, 105, 105817. https://doi.org/10.1016/j.foodhyd.2020.105817
   Web of Science ®Google Scholar
• Darmawan, K. K., Karagiannis, T. C., Hughes, J. G., Small, D. M., & Hung, A. (2021). Effects of low temperatures on the conformation of apo-lactoferrin and its interactions with α-lactalbumin and β-lactoglobulin: Application of in silico approaches. Food Hydrocolloids, 121, 107055. https://doi.org/10.1016/j.foodhyd.2021.107055
   Web of Science ®Google Scholar
• Department of Health and Human Services. (2021). Similarities and differences between Flu and COVID-19. Retrieved from https://www.cdc.gov/flu/symptoms/flu-vs-covid19.htm.
   Google Scholar
• Gallo, V., Giansanti, F., Arienzo, A., & Antonini, G. (2022). Antiviral properties of whey proteins and their activity against SARS-CoV-2 infection. Journal of Functional Foods, 89, 104932. doi:10.1016/j.jff.2022.104932.
   PubMed Web of Science ®Google Scholar
• Hess, B., Kutzner, C., van der Spoel, D., & Lindahl, E. (2008). GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation. Journal of Chemical Theory and Computation, 4(3), 435–447. doi:10.1021/ct700301q.
   PubMed Web of Science ®Google Scholar
• Hou, T., Wang, J., Li, Y., & Wang, W. (2011). Assessing the performance of the MM/PBSA and MM/GBSA methods. 1. the accuracy of binding free energy calculations based on molecular dynamics simulations. Journal of Chemical Information and Modeling, 51(1), 69–82. doi:10.1021/ci100275a.
   PubMed Web of Science ®Google Scholar
• Hui, D. S., I Azhar, E., Madani, T. A., Ntoumi, F., Kock, R., Dar, O., Ippolito, G., Mchugh, T. D., Memish, Z. A., Drosten, C., Zumla, A., & Petersen, E. (2020). The continuing 2019-nCoV epidemic threat of novel coronaviruses to global health - The latest 2019 novel coronavirus outbreak in Wuhan, China. International Journal of Infectious Diseases: IJID: Official Publication of the International Society for Infectious Diseases, 91, 264–266. doi:10.1016/j.ijid.2020.01.009.
   PubMed Web of Science ®Google Scholar
• Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD-visual molecular dynamics. Journal of Molecular Graphics, 14(1), 33–38. https://doi.org/10.1016/0263-7855(96)00018-5
   PubMedGoogle Scholar
• Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., & Klein, M. L. (1983). Comparison of simple potential functions for simulating liquid water. The Journal of Chemical Physics, 79(2), 926–935. https://doi.org/10.1063/1.445869
   Web of Science ®Google Scholar
• Kaur, S. P., & Gupta, V. (2020). COVID-19 Vaccine: A comprehensive status report. Virus Research, 288, 198114. doi:10.1016/j.virusres.2020.198114.
   PubMed Web of Science ®Google Scholar
• Kell, D. B., Heyden, E. L., & Pretorius, E. (2020). The biology of lactoferrin, an iron-binding protein that can help defend against viruses and bacteria. Frontiers in Immunology, 11, 1221. (doi:10.3389/fimmu.2020.01221.
   PubMed Web of Science ®Google Scholar
• Kumari, R., Kumar, R., & Lynn, A., Open Source Drug Discovery Consortium. (2014). g_mmpbsa—A GROMACS tool for high-throughput MM-PBSA calculations. Journal of Chemical Information and Modeling, 54(7), 1951–1962. doi:10.1021/ci500020m.
   PubMed Web of Science ®Google Scholar
• Lan, J., Ge, J., Yu, J., Shan, S., Zhou, H., Fan, S., Zhang, Q., Shi, X., Wang, Q., Zhang, L., & Wang, X. (2020). Structure of the SARS-CoV-2 spike receptor-binding domain bound to the ACE2 receptor. Nature, 581(7807), 215–220. doi:10.1038/s41586-020-2180-5.
   PubMed Web of Science ®Google Scholar
• Lechowicz, J., & Krawczyk-Balska, A. (2015). An update on the transport and metabolism of iron in Listeria monocytogenes: the role of proteins involved in pathogenicity. Biometals: An International Journal on the Role of Metal Ions in Biology, Biochemistry, and Medicine, 28(4), 587–603. doi:10.1007/s10534-015-9849-5.
   PubMed Web of Science ®Google Scholar
• Liu, C., Ginn, H. M., Dejnirattisai, W., Supasa, P., Wang, B., Tuekprakhon, A., Nutalai, R., Zhou, D., Mentzer, A. J., Zhao, Y., Duyvesteyn, H. M. E., López-Camacho, C., Slon-Campos, J., Walter, T. S., Skelly, D., Johnson, S. A., Ritter, T. G., Mason, C., Costa Clemens, S. A., … Screaton, G. R. (2021). Reduced neutralization of SARS-CoV-2 B.1.617 by vaccine and convalescent serum. Cell, 184(16), 4220–4236.e13. doi:10.1016/j.cell.2021.06.020.
   PubMed Web of Science ®Google Scholar
• Madeira, F. (2022). Search and sequence analysis tools services from EMBL-EBI in 2022. Nucleic Acids Research, 50, W276. https://doi.org/10.1093/nar/gkac240
   PubMed Web of Science ®Google Scholar
• Miotto, M., Di Rienzo, L., Bò, L., Boffi, A., Ruocco, G., & Milanetti, E. (2021). Molecular mechanisms behind anti SARS-CoV-2 action of lactoferrin. Frontiers in Molecular Biosciences, 8(25), 607443. doi:10.3389/fmolb.2021.607443.
   PubMedGoogle Scholar
• Moore, S. A., Anderson, B. F., Groom, C. R., Haridas, M., & Baker, E. N. (1997). Three-dimensional structure of diferric bovine lactoferrin at 2.8 Å resolution. Journal of Molecular Biology, 274(2), 222–236. doi:10.1006/jmbi.1997.1386.
   PubMed Web of Science ®Google Scholar
• Needleman, S. B., & Wunsch, C. D. (1970). A general method applicable to the search for similarities in the amino acid sequence of two proteins. Journal of Molecular Biology, 48(3), 443–453. https://doi.org/10.1016/0022-2836(70)90057-4
   PubMed Web of Science ®Google Scholar
• Nicola, M., Alsafi, Z., Sohrabi, C., Kerwan, A., Al-Jabir, A., Iosifidis, C., Agha, M., & Agha, R. (2020). The socio-economic implications of the coronavirus pandemic (COVID-19): A review. International Journal of Surgery (London, England), 78, 185–193. doi:10.1016/j.ijsu.2020.04.018.
   PubMed Web of Science ®Google Scholar
• Parrinello, M., & Rahman, A. (1980). Crystal structure and pair potentials: A molecular-dynamics study. Physical Review Letters, 45(14), 1196–1199. https://doi.org/10.1103/PhysRevLett.45.1196
   Web of Science ®Google Scholar
• Parrinello, M., & Rahman, A. (1981). Polymorphic transitions in single crystals: A new molecular dynamics method. Journal of Applied Physics, 52(12), 7182–7190. https://doi.org/10.1063/1.328693
   Web of Science ®Google Scholar
• Parrinello, M., & Rahman, A. (1982). Strain fluctuations and elastic constants. The Journal of Chemical Physics, 76(5), 2662–2666. https://doi.org/10.1063/1.443248
   Web of Science ®Google Scholar
• Pitsillou, E., Liang, J., Karagiannis, C., Ververis, K., Darmawan, K. K., Ng, K., Hung, A., & Karagiannis, T. C. (2020). Interaction of small molecules with the SARS-CoV-2 main protease in silico and in vitro validation of potential lead compounds using an enzyme-linked immunosorbent assay. Computational Biology and Chemistry, 89, 107408. doi:10.1016/j.compbiolchem.2020.107408.
   PubMed Web of Science ®Google Scholar
• Rosa, L., Tripepi, G., Naldi, E., Aimati, M., Santangeli, S., Venditto, F., Caldarelli, M., & Valenti, P. (2021). Ambulatory COVID-19 patients treated with lactoferrin as a supplementary antiviral agent: A preliminary study. Journal of Clinical Medicine, 10(18), 4276. https://doi.org/10.3390/jcm10184276
   PubMed Web of Science ®Google Scholar
• Sargsyan, K., Grauffel, C., & Lim, C. (2017). How molecular size impacts RMSD aplications in molecular dynamics simulations. Journal of Chemical Theory and Computation, 13(4), 1518–1524. doi:10.1021/acs.jctc.7b00028.
   PubMed Web of Science ®Google Scholar
• Serrano, G., Kochergina, I., Albors, A., Diaz, E., Oroval, M., Hueso, G., & Serrano, J. M. (2020). Liposomal lactoferrin as potential preventative and cure for COVID-19. International Journal of Research in Health Sciences, 8(1), 8–15. https://doi.org/10.5530/ijrhs.8.1.3
   Google Scholar
• van der Kraan, M. I. A., Groenink, J., Nazmi, K., Veerman, E. C. I., Bolscher, J. G. M., & Nieuw Amerongen, A. V. (2004). Lactoferrampin: A novel antimicrobial peptide in the N1-domain of bovine lactoferrin. Peptides, 25(2), 177–183. doi:10.1016/j.peptides.2003.12.006.
   PubMed Web of Science ®Google Scholar
• Wang, B., Timilsena, Y. P., Blanch, E., & Adhikari, B. (2019). Lactoferrin: Structure, function, denaturation and digestion. Critical Reviews in Food Science and Nutrition, 59(4), 580–596. doi:10.1080/10408398.2017.1381583.
   PubMed Web of Science ®Google Scholar
• Williams-Noonan, B. J., Todorova, N., Kulkarni, K., Aguilar, M.-I., & Yarovsky, I. (2021). An active site inhibitor induces conformational penalties for ACE2 recognition by the spike protein of SARS-CoV-2. The Journal of Physical Chemistry. B, 125(10), 2533–2550. doi:10.1021/acs.jpcb.0c11321.
   PubMed Web of Science ®Google Scholar
• Yan, Y., Tao, H., He, J., & Huang, S.-Y. (2020). The HDOCK server for integrated protein–protein docking. Nature Protocols, 15(5), 1829–1852. doi:10.1038/s41596-020-0312-x.
   PubMed Web of Science ®Google Scholar