Computational Interrogation of The Human Norovirus-Host Cell Interactions Facilitated by A-Type Antigen

Year 2019, , 1056 - 1065, 01.12.2019

Abdulkadir Kocak , Muslum Yildiz

https://doi.org/10.16984/saufenbilder.525430

Abstract

Norovirus infectivity, which causes norovirus-induced gastroenteritis,
depends on the interaction between capsid protein VP1 of the virus and host
cell HGBA receptors that tailor the cell membrane surface. The interaction
results in VP1-HGBA complex formation prior to infection. The details of this
interaction have been provided by x-ray structures of HGBA-VP1 complexes, but
the dynamic nature of this interaction is not fully uncovered. Therefore, the
dynamics that drive the formation of VP1-HGBA complex, which is crucial for
developing new therapeutic approaches to find a cure for gastroenteritis
disease, need to be elucidated. Here, we computationally analyzed the wild type
VP1 capsid protein in complex with A-type HGBA antigen to unravel interactions
that are important for virus to enter inside the host cell during infection. We
have found that the ligand binding causes a fluctuation in a distant loop which
resides in the interface of capsid building blocks, VP proteins. This
fluctuation leads an instability in capsid particle that may be an indication
for virus uncoating mechanism during the cell penetration.

Keywords

Norovirus, therapeutic antibody, HBGA blockage, molecular dynamics

References

• A. Z. Kapikian, R. G. Wyatt, R. Dolin, T. S. Thornhill, A. R. Kalica, and R. M. Chanock, "Visualization by Immune Electron-Microscopy of a 27-Nm Particle Associated with Acute Infectious Nonbacterial Gastroenteritis," Journal of Virology, vol. 10, pp. 1075-1081, 1972.
• K. L. Kotloff, J. P. Nataro, W. C. Blackwelder, D. Nasrin, T. H. Farag, S. Panchalingam, et al., "Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study," Lancet, vol. 382, pp. 209-22, Jul 20 2013.
• G. Belliot, B. A. Lopman, K. Ambert-Balay, and P. Pothier, "The burden of norovirus gastroenteritis: an important foodborne and healthcare-related infection," Clin Microbiol Infect, vol. 20, pp. 724-30, Aug 2014.
• A. Kambhampati, M. Koopmans, and B. A. Lopman, "Burden of norovirus in healthcare facilities and strategies for outbreak control," J Hosp Infect, vol. 89, pp. 296-301, Apr 2015.
• T. N. Hoa Tran, E. Trainor, T. Nakagomi, N. A. Cunliffe, and O. Nakagomi, "Molecular epidemiology of noroviruses associated with acute sporadic gastroenteritis in children: global distribution of genogroups, genotypes and GII.4 variants," J Clin Virol, vol. 56, pp. 185-93, Mar 2013.
• S. M. Karst, C. E. Wobus, I. G. Goodfellow, K. Y. Green, and H. W. Virgin, "Advances in norovirus biology," Cell Host Microbe, vol. 15, pp. 668-80, Jun 11 2014.
• J. Rocha-Pereira, J. Neyts, and D. Jochmans, "Norovirus: targets and tools in antiviral drug discovery," Biochem Pharmacol, vol. 91, pp. 1-11, Sep 1 2014.
• M. Tan and X. Jiang, "Vaccine against norovirus," Hum Vaccin Immunother, vol. 10, pp. 1449-56, 2014.
• N. Aliabadi, B. A. Lopman, U. D. Parashar, and A. J. Hall, "Progress toward norovirus vaccines: considerations for further development and implementation in potential target populations," Expert Rev Vaccines, vol. 14, pp. 1241-53, 2015.
• E. Robilotti, S. Deresinski, and B. A. Pinsky, "Norovirus," Clin Microbiol Rev, vol. 28, pp. 134-64, Jan 2015.
• S. M. Karst, S. Zhu, and I. G. Goodfellow, "The molecular pathology of noroviruses," J Pathol, vol. 235, pp. 206-16, Jan 2015.
• P. A. White, "Evolution of norovirus," Clin Microbiol Infect, vol. 20, pp. 741-5, Aug 2014.
• M. M. Patel, A. J. Hall, J. Vinje, and U. D. Parashar, "Noroviruses: a comprehensive review," J Clin Virol, vol. 44, pp. 1-8, Jan 2009.
• S. Caddy, A. Breiman, J. le Pendu, and I. Goodfellow, "Genogroup IV and VI canine noroviruses interact with histo-blood group antigens," J Virol, vol. 88, pp. 10377-91, Sep 2014.
• M. de Graaf, J. van Beek, and M. P. Koopmans, "Human norovirus transmission and evolution in a changing world," Nat Rev Microbiol, vol. 14, pp. 421-33, Jul 2016.
• S. Shanker, R. Czako, B. Sankaran, R. L. Atmar, M. K. Estes, and B. V. Prasad, "Structural analysis of determinants of histo-blood group antigen binding specificity in genogroup I noroviruses," J Virol, vol. 88, pp. 6168-80, Jun 2014.
• G. Sapparapu, R. Czako, G. Alvarado, S. Shanker, B. V. Prasad, R. L. Atmar, et al., "Frequent Use of the IgA Isotype in Human B Cells Encoding Potent Norovirus-Specific Monoclonal Antibodies That Block HBGA Binding," PLoS Pathog, vol. 12, p. e1005719, Jun 2016.
• K. Tamminen, M. Malm, T. Vesikari, and V. Blazevic, "Mucosal Antibodies Induced by Intranasal but Not Intramuscular Immunization Block Norovirus GII.4 Virus-Like Particle Receptor Binding," Viral Immunol, vol. 29, pp. 315-9, Jun 2016.
• L. Garaicoechea, A. Aguilar, G. I. Parra, M. Bok, S. V. Sosnovtsev, G. Canziani, et al., "Llama nanoantibodies with therapeutic potential against human norovirus diarrhea," PLoS One, vol. 10, p. e0133665, 2015.
• V. P. Lochridge, K. L. Jutila, J. W. Graff, and M. E. Hardy, "Epitopes in the P2 domain of norovirus VP1 recognized by monoclonal antibodies that block cell interactions," J Gen Virol, vol. 86, pp. 2799-806, Oct 2005.
• B. V. V. Prasad, M. E. Hardy, T. Dokland, J. Bella, M. G. Rossmann, and M. K. Estes, "X-ray crystallographic structure of the Norwalk virus capsid," Science, vol. 286, pp. 287-290, Oct 8 1999.
• J. M. Choi, A. M. Hutson, M. K. Estes, and B. V. V. Prasad, "Atomic resolution structural characterization of recognition of histo-blood group antigens by Norwalk virus," Proceedings of the National Academy of Sciences of the United States of America, vol. 105, pp. 9175-9180, Jul 8 2008.
• T. Kubota, A. Kumagai, H. Ito, S. Furukawa, Y. Someya, N. Takeda, et al., "Structural basis for the recognition of Lewis antigens by genogroup I norovirus," J Virol, vol. 86, pp. 11138-50, Oct 2012.
• A. Kocak and M. Yildiz, "Molecular dynamics studies of the norovirus-host cell interaction mediated by h-type 1 antigen," Trakya University Journal of Natural Sciences, vol. ASAP, 2019.
• L. Schrödinger, "Maestro," in Schrödinger Release 2015-2, ed. New York, NY: Schrödinger, LLC, 2015.
• M. H. Olsson, C. R. Sondergaard, M. Rostkowski, and J. H. Jensen, "PROPKA3: Consistent Treatment of Internal and Surface Residues in Empirical pKa Predictions," J Chem Theory Comput, vol. 7, pp. 525-37, Feb 8 2011.
• K. Lindorff-Larsen, S. Piana, K. Palmo, P. Maragakis, J. L. Klepeis, R. O. Dror, et al., "Improved side-chain torsion potentials for the Amber ff99SB protein force field," Proteins, vol. 78, pp. 1950-1958, 2010.
• J. Wang, W. Wang, P. A. Kollman, and D. A. Case, "Automatic atom type and bond type perception in molecular mechanical calculations," Journal of Molecular Graphics and Modelling, vol. 25, pp. 247-260, 2006/10/01/ 2006.
• J. Wang, R. M. Wolf, J. W. Caldwell, P. A. Kollman, and D. A. Case, "Development and testing of a general amber force field," Journal of Computational Chemistry, vol. 25, pp. 1157-1174, 2004.
• M. J. Abraham, T. Murtola, R. Schulz, S. Páll, J. C. Smith, B. Hess, et al., "GROMACS: High performance molecular simulations through multi-level parallelism from laptops to supercomputers," SoftwareX, vol. 1-2, pp. 19-25, 2015.
• K. Toukan and A. Rahman, "Molecular-dynamics study of atomic motions in water," Phys Rev B Condens Matter, vol. 31, pp. 2643-2648, Mar 1 1985.
• A. Kocak, I. Erol, M. Yildiz, and H. Can, "Computational insights into the protonation states of catalytic dyad in BACE1-acyl guanidine based inhibitor complex," J Mol Graph Model, vol. 70, pp. 226-235, Nov 2016.
• A. Kocak and M. Yildiz, "Docking, molecular dynamics and free energy studies on aspartoacylase mutations involved in Canavan disease," J Mol Graph Model, vol. 74, pp. 44-53, Jun 2017.