An agent-based approach for modelling and simulation of glycoprotein VI receptor diffusion, localisation and dimerisation in platelet lipid rafts

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1. Lombard, J. Once upon a time the cell membranes: 175 years of cell boundary research. Biol. Direct. 9, 1–35 (2014). 2. Radhakrishnan, K., Halász, Á., Vlachos, D. & Edwards, J. S. Quantitative understanding of cell signaling: The importance of membrane organization. Curr. Opin. Biotechnol. 21, 677–682 (2010). 3. Stein, W. D. The Movement of Molecules across Cell Membranes. Academic Press, New York (1967). 4. Klammt, C. & Lillemeier, B. F. How membrane structures control T cell signaling. Front. Immunol. 3, 1–9 (2012). 5. Juliano, R. L. & Haskill, S. Signal transduction from the extracellular matrix. J. Cell Biol. 120, 577–585 (1993). 6. Goñi, F. M. The basic structure and dynamics of cell membranes: An update of the Singer-Nicolson model. Biochim. Biophys. Acta. 1838, 1467–1476 (2014). 7. Sunshine, H. & Iruela-Arispe, M. L. Membrane lipids and cell signaling. Curr. Opin. Lipidol. 28, 408–413 (2017). 8. Owen, D. M., Williamson, D., Rentero, C. & Gaus, K. Quantitative microscopy: protein dynamics and membrane organisation. Traffic 10, 962–971 (2009). 9. Trimble, W. S. & Grinstein, S. Barriers to the free diffusion of proteins and lipids in the plasma membrane. J. Cell Biol. 208, 259–271 (2015). 10. Dityatev, A., Seidenbecher, C. I. & Schachner, M. Compartmentalization from the outside: the extracellular matrix and functional microdomains in the brain. Trends Neurosci. 33, 503–512 (2010). 11. Ward, C. et al. Structural insights into ligand-induced activation of the insulin receptor. Acta Physiol. 192, 3–9 (2008). 12. Lemmon, M. A. Ligand-induced ErbB receptor dimerization. Exp. Cell Res. 315, 638–648 (2009). 13. Ardito, F., Giuliani, M., Perrone, D., Troiano, G. & Muzio, L. Lo. The crucial role of protein phosphorylation in cell signalingand its use as targeted therapy. Int. J. Mol. Med. 40, 271–280 (2017). 14. Foot, N., Henshall, T. & Kumar, S. Ubiquitination and the regulation of membrane proteins. Physiol. Rev. 97, 253–281 (2017). 15. Torres, M. et al. The implications for cells of the lipid switches driven by protein–membrane interactions and the development of membrane lipid therapy. Int. J. Mol. Sci. 21, 2377 (2020). 16. Okada, A. K. et al. Lysine acetylation regulates the interaction between proteins and membranes. Nat. Commun. 12, 1–12 (2021). 17. Sezgin, E., Levental, I., Mayor, S. & Eggeling, C. The mystery of membrane organization: Composition, regulation and roles of lipid rafts. Nat. Rev. Mol. Cell Biol. 18, 361–374 (2017). 18. Das, A. A., Darsana, T. A. & Jacob, E. Agent-based re-engineering of ErbB signaling: A modeling pipeline for integrative systems biology. Bioinformatics 33, 726–732 (2017). 19. Juliette, G., Peters, R. & Owen, D. M. An agent-based model of molecular aggregation at the cell membrane. PLoS One 15, 1–17 (2020). 20. Watson, S. Platelet activation by extracellular matrix proteins in haemostasis and thrombosis. Curr. Pharm. Des. 15, 1358–1372 (2009). 21. Mammadova-Bach, E., Nagy, M., Heemskerk, J. W., Nieswandt, B. & Braun, A. Store-operated calcium entry in thrombosis and thrombo-inflammation. Cell Calcium 77, 39–48 (2019). 22. Rayes, J., Watson, S. P. & Nieswandt, B. Functional significance of the platelet immune receptors GPVI and CLEC-2. J. Clin. Invest. 129, 12–23 (2019). 23. Horii, K., Kahn, M. L. & Herr, A. B. Structural basis for platelet collagen responses by the immune-type receptor glycoprotein VI. Blood 108, 936–942 (2006). 24. Miura, Y., Takahashi, T., Jung, S. M. & Moroi, M. Analysis of the interaction of platelet collagen receptor glycoprotein VI (GPVI) with collagen: A dimeric form of GPVI, but not the monomeric form, shows affinity to fibrous collagen. J. Biol. Chem. 277, 46197–46204 (2002). 25. Jung, S. M., Tsuji, K. & Moroi, M. Glycoprotein (GP) VI dimer as a major collagen-binding site of native platelets: direct evidence obtained with dimeric GPVI-specific Fabs. J. Thromb. Haemost. 7, 1347–1355 (2009). 26. Jung, S. M. et al. Constitutive dimerization of glycoprotein VI (GPVI) in resting platelets is essential for binding to collagen and activation in flowing blood. J. Biol. Chem. 287, 30000–30013 (2012). 27. Induruwa, I., Jung, S. M. & Warburton, E. A. Beyond antiplatelets: The role of glycoprotein VI in ischemic stroke. Int. J. Stroke 11, 618–625 (2016). 28. Dietrich, C., Yang, B., Fujiwara, T., Kusumi, A. & Jacobson, K. Relationship of lipid rafts to transient confinement zones detected by single particle tracking. Biophys. J. 82, 274–284 (2002). 29. Triantafilou, M., Morath, S., Mackie, A., Hartung, T. & Triantafilou, K. Lateral diffusion of Toll-like receptors reveals that they are transiently confined within lipid rafts on the plasma membrane. J. Cell Sci. 117, 4007–4014 (2004). 30. Bodin, S., Tronchère, H. & Payrastre, B. Lipid rafts are critical membrane domains in blood platelet activation processes. Biochim. Biophys. Acta. 1610, 247–257 (2003). 31. Bonabeau, E. Agent-based modeling: Methods and techniques for simulating human systems. Proc. Natl. Acad. Sci. U S A. 99, 7280–7287 (2002). 32. Niazi, M. & Hussain, A. Agent-based computing from multi-agent systems to agent-based models: A visual survey. Scientometrics 89, 479–499 (2011). 33. Cuevas, E. An agent-based model to evaluate the COVID-19 transmission risks in facilities. Comput. Biol. Med. 121, 103827 (2020). 34. Truszkowska A., Behring B., Hasanyan J., Zino L., Butail S., Caroppo E., Jiang Z.P., Rizzo A., P. M. High‐resolution agent‐based modeling of COVID‐19 spreading in a small town. (2021). ArXiv q-bio. doi:10.1002/adts.202000277 35. Shamil, M. S., Farheen, F., Ibtehaz, N., Khan, I. M. & Rahman, M. S. An agent-based modeling of COVID-19: validation, analysis, and recommendations. Cognit. Comput. (2021). doi:10.1007/s12559-020-09801-w 36. Wilensky, U. NetLogo. Center for Connected Learning and Computer-Based Modeling, Northwestern University, Evanston, IL. (1999). Available at: http://ccl.northwestern.edu/netlogo/. 37. Pratt, L. R., Haan, S. W., Pratt, L. R. & Haan, S. W. Effects of periodic boundary conditions on equilibrium properties of computer simulated fluids. J. Chem. Phys. 1864, (1981). 38. Michalet, X. Brownian motion in an isotropic medium. Phys. Rev. E. Interdiscip. Top. 1–13 (2010). doi:10.1103/PhysRevE.82.041914 39. Einstein, A. On the motion of small particles suspended in liquids at rest required by the molecular-kinetic theory of heat. Annu. Phys. (1905). 40. Haining, E. J. et al. Tetraspanin Tspan9 regulates platelet collagen receptor GPVI lateral diffusion and activation. Platelets 28, 629–642 (2017). 41. Dunster, J. L., Mazet, F., Fry, M. J., Gibbins, J. M. & Tindall, M. J. Regulation of early steps of GPVI signal transduction by phosphatases: a systems biology approach. PLoS Comput. Biol. 11, 1–26 (2015). 42. Frojmovic, M. M. & Milton, J. G. Human platelet size, shape, and related functions in health and disease. Physiol. Rev. 62, 185–261 (1982). 43. Prior, I. A., Muncke, C., Parton, R. G. & Hancock, J. F. Direct visualization of Ras proteins in spatially distinct cell surface microdomains. J. Cell Biol. 160, 165–170 (2003). 44. Burkhart, J. M. et al. The first comprehensive and quantitative analysis of human platelet protein composition allows the comparative analysis of structural and functional pathways. Blood 120, 73–82 (2012). 45. Honigmann, A. & Pralle, A. Compartmentalization of the cell membrane. J. Mol. Biol. 428, 4739–4748 (2016). 46. Krapf, D. Compartmentalization of the plasma membrane. Curr. Opin. Cell Biol. 53, 15–21 (2018). 47. Komatsuya, K., Kaneko, K. & Kasahara, K. Function of platelet glycosphingolipid microdomains /lipid rafts. Int. J. Mol. Sci. 21, 1–18 (2020). 48. Jooss, N. J. et al. Anti- GPVI nanobody blocks collagen- and atherosclerotic plaque– induced GPVI clustering, signaling, and thrombus formation. J. Thromb. Haemost. 20, 2617–2631 (2022). 49. Goiko, M., De Bruyn, J. R. & Heit, B. Short-lived cages restrict protein diffusion in the plasma membrane. Sci. Rep. 6, 1–13 (2016). 50. Mosqueira, A., Camino, P. A. & Barrantes, F. J. Cholesterol modulates acetylcholine receptor diffusion by tuning confinement sojourns and nanocluster stability. Sci. Rep. 8, 1–11 (2018). 51. Lee, F. A. et al. Lipid rafts facilitate the interaction of PECAM-1 with the glycoprotein VI-FcR γ-chain complex in human platelets. J. Biol. Chem. 281, 39330–39338 (2006). 52. Locke, D., Chen, H., Liu, Y., Liu, C. & Kahn, M. L. Lipid rafts orchestrate signaling by the platelet receptor glycoprotein VI. J. Biol. Chem. 277, 18801–18809 (2002). 53. Saitov, A. et al. Determinants of lipid domain size. Int. J. Mol. Sci. 1–14, 3502 (2022). 54. Rönnlund, D., Yang, Y., Blom, H., Auer, G. & Widengren, J. Fluorescence nanoscopy of platelets resolves platelet-state specific storage, release and uptake of proteins, opening up future diagnostic applications. Adv. Healthc. Mater. 1, 707–713 (2012). 55. Fujiwara, T., Ritchie, K., Murakoshi, H., Jacobson, K. & Kusumi, A. Phospholipids undergo hop diffusion in compartmentalized cell membrane. J. Cell Biol. 157, 1071–1081 (2002). 56. Best, D. et al. GPVI levels in platelets: relationship to platelet function at high shear. Blood 102, 2811–2818 (2003). 57. Barrachina, M. N. et al. GPVI surface expression and signalling pathway activation are increased in platelets from obese patients: Elucidating potential anti-atherothrombotic targets in obesity. Atherosclerosis 281, 62–70 (2019). 58. Joutsi-Korhonen, L. et al. The low-frequency allele of the platelet collagen signaling receptor glycoprotein VI is associated with reduced functional responses and expression. Blood 101, 4372–4379 (2003). 59. Veninga, A. et al. GPVI expression is linked to platelet size, age, and reactivity. Blood Adv. 6, 4162–4173 (2022). 60. Selvadurai, M. V. & Hamilton, J. R. Structure and function of the open canalicular system–the platelet’s specialized internal membrane network. Platelets 29, 319–325 (2018). 61. Emeis, J. J. et al. A guide to murine coagulation factor structure, function, assays, and genetic alterations. J. Thromb. Haemost. 5, 670–679 (2007). 62. Huang, J. et al. Assessment of a complete and classified platelet proteome from genome-wide transcripts of human platelets and megakaryocytes covering platelet functions. Sci. Rep. 11, 1–18 (2021). 63. Fachada, N., Lopes, V. V., Martins, R. C. & Rosa, A. C. Parallelization strategies for spatial agent-based models. Int. J. Parallel Program. 45, 449–481 (2017). 64. Kabiri Chimeh, M., Heywood, P., Pennisi, M., Pappalardo, F. & Richmond, P. Parallelisation strategies for agent based simulation of immune systems. BMC Bioinformatics 20, 1–14 (2019).