Abstract
The heterotypic aggregation of cell mixtures or colloidal particles such as proteins occurs in a variety of settings such as thrombosis, immunology, cell separations, and diagnostics. Using the set of population balance equations (PBEs) to predict dynamic aggregate size and composition distributions is not feasible. The stochastic algorithm of Gillespie for chemical reactions (. J. Comput. Phys. 22:403-434) was reformulated to simulate the kinetic behavior of aggregating systems. The resulting Monte Carlo (MC) algorithm permits exact calculation of the decay rates of monomers and the temporally evolving distribution of sizes and compositions of the aggregates. Moreover, it permits calculation of all moments of these distributions. Using this method, we explored the heterotypic aggregation of fully activated platelets and neutrophils in a linear shear flow of shear rate G = 335 s(-1). At plasma concentrations, the half-lives of homotypically aggregating platelet and neutrophil singlets were 8.5 and 2.4 s, respectively. However, for heterotypic aggregation, the half-lives for platelets and neutrophils decreased to 2.0 and 0.11 s, respectively, demonstrating that flowing neutrophils accelerate capture of platelets and growth of aggregates. The required number of calculations per time step of the MC algorithm was typically a small fraction of Omega(1/2), where Omega is the initial number of particles in the system, making this the fastest MC method available. The speed of the algorithm makes feasible the deconvolution of kernels for general biological heterotypic aggregation processes.
Full Text
The Full Text of this article is available as a PDF (182.7 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Bednar M., Smith B., Pinto A., Mullane K. M. Neutrophil depletion suppresses 111In-labeled platelet accumulation in infarcted myocardium. J Cardiovasc Pharmacol. 1985 Sep-Oct;7(5):906–912. doi: 10.1097/00005344-198509000-00014. [DOI] [PubMed] [Google Scholar]
- Bell D. N., Spain S., Goldsmith H. L. Adenosine diphosphate-induced aggregation of human platelets in flow through tubes. I. Measurement of concentration and size of single platelets and aggregates. Biophys J. 1989 Nov;56(5):817–828. doi: 10.1016/S0006-3495(89)82728-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bell D. N., Spain S., Goldsmith H. L. Adenosine diphosphate-induced aggregation of human platelets in flow through tubes. I. Measurement of concentration and size of single platelets and aggregates. Biophys J. 1989 Nov;56(5):817–828. doi: 10.1016/S0006-3495(89)82728-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bell G. I. A theoretical model for adhesion between cells mediated by multivalent ligands. Cell Biophys. 1979 Jun;1(2):133–147. doi: 10.1007/BF02781347. [DOI] [PubMed] [Google Scholar]
- Bell G. I. Estimate of the sticking probability for cells in uniform shear flow with adhesion caused by specific bonds. Cell Biophys. 1981 Sep;3(3):289–304. doi: 10.1007/BF02782629. [DOI] [PubMed] [Google Scholar]
- Belval T. K., Hellums J. D. Analysis of shear-induced platelet aggregation with population balance mathematics. Biophys J. 1986 Sep;50(3):479–487. doi: 10.1016/S0006-3495(86)83485-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brown K. K., Henson P. M., Maclouf J., Moyle M., Ely J. A., Worthen G. S. Neutrophil-platelet adhesion: relative roles of platelet P-selectin and neutrophil beta2 (DC18) integrins. Am J Respir Cell Mol Biol. 1998 Jan;18(1):100–110. doi: 10.1165/ajrcmb.18.1.2314. [DOI] [PubMed] [Google Scholar]
- Elizalde J. I., Gómez J., Panés J., Lozano M., Casadevall M., Ramírez J., Pizcueta P., Marco F., Rojas F. D., Granger D. N. Platelet activation In mice and human Helicobacter pylori infection. J Clin Invest. 1997 Sep 1;100(5):996–1005. doi: 10.1172/JCI119650. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Evangelista V., Manarini S., Rotondo S., Martelli N., Polischuk R., McGregor J. L., de Gaetano G., Cerletti C. Platelet/polymorphonuclear leukocyte interaction in dynamic conditions: evidence of adhesion cascade and cross talk between P-selectin and the beta 2 integrin CD11b/CD18. Blood. 1996 Dec 1;88(11):4183–4194. [PubMed] [Google Scholar]
- Hamburger S. A., McEver R. P. GMP-140 mediates adhesion of stimulated platelets to neutrophils. Blood. 1990 Feb 1;75(3):550–554. [PubMed] [Google Scholar]
- Huang P. Y., Hellums J. D. Aggregation and disaggregation kinetics of human blood platelets: Part I. Development and validation of a population balance method. Biophys J. 1993 Jul;65(1):334–343. doi: 10.1016/S0006-3495(93)81078-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Huang P. Y., Hellums J. D. Aggregation and disaggregation kinetics of human blood platelets: Part II. Shear-induced platelet aggregation. Biophys J. 1993 Jul;65(1):344–353. doi: 10.1016/S0006-3495(93)81079-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Huang P. Y., Hellums J. D. Aggregation and disaggregation kinetics of human blood platelets: Part III. The disaggregation under shear stress of platelet aggregates. Biophys J. 1993 Jul;65(1):354–361. doi: 10.1016/S0006-3495(93)81080-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Konstantopoulos K., Neelamegham S., Burns A. R., Hentzen E., Kansas G. S., Snapp K. R., Berg E. L., Hellums J. D., Smith C. W., McIntire L. V. Venous levels of shear support neutrophil-platelet adhesion and neutrophil aggregation in blood via P-selectin and beta2-integrin. Circulation. 1998 Sep 1;98(9):873–882. doi: 10.1161/01.cir.98.9.873. [DOI] [PubMed] [Google Scholar]
- Long M., Goldsmith H. L., Tees D. F., Zhu C. Probabilistic modeling of shear-induced formation and breakage of doublets cross-linked by receptor-ligand bonds. Biophys J. 1999 Feb;76(2):1112–1128. doi: 10.1016/S0006-3495(99)77276-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Macken C. A., Perelson A. S. Aggregation of cell surface receptors by multivalent ligands. J Math Biol. 1982;14(3):365–370. doi: 10.1007/BF00275399. [DOI] [PubMed] [Google Scholar]
- Minamino T., Kitakaze M., Asanuma H., Tomiyama Y., Shiraga M., Sato H., Ueda Y., Funaya H., Kuzuya T., Matsuzawa Y. Endogenous adenosine inhibits P-selectin-dependent formation of coronary thromboemboli during hypoperfusion in dogs. J Clin Invest. 1998 Apr 15;101(8):1643–1653. doi: 10.1172/JCI635. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Neelamegham S., Taylor A. D., Hellums J. D., Dembo M., Smith C. W., Simon S. I. Modeling the reversible kinetics of neutrophil aggregation under hydrodynamic shear. Biophys J. 1997 Apr;72(4):1527–1540. doi: 10.1016/S0006-3495(97)78801-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Neelamegham S., Zygourakis K. A quantitative assay for intercellular aggregation. Ann Biomed Eng. 1997 Jan-Feb;25(1):180–189. doi: 10.1007/BF02738549. [DOI] [PubMed] [Google Scholar]
- Neumann F. J., Marx N., Gawaz M., Brand K., Ott I., Rokitta C., Sticherling C., Meinl C., May A., Schömig A. Induction of cytokine expression in leukocytes by binding of thrombin-stimulated platelets. Circulation. 1997 May 20;95(10):2387–2394. doi: 10.1161/01.cir.95.10.2387. [DOI] [PubMed] [Google Scholar]
- Ott I., Neumann F. J., Gawaz M., Schmitt M., Schömig A. Increased neutrophil-platelet adhesion in patients with unstable angina. Circulation. 1996 Sep 15;94(6):1239–1246. doi: 10.1161/01.cir.94.6.1239. [DOI] [PubMed] [Google Scholar]
- Palabrica T., Lobb R., Furie B. C., Aronovitz M., Benjamin C., Hsu Y. M., Sajer S. A., Furie B. Leukocyte accumulation promoting fibrin deposition is mediated in vivo by P-selectin on adherent platelets. Nature. 1992 Oct 29;359(6398):848–851. doi: 10.1038/359848a0. [DOI] [PubMed] [Google Scholar]
- Perelson A. S., Wiegel F. W. The equilibrium size distribution of rouleaux. Biophys J. 1982 Feb;37(2):515–522. doi: 10.1016/S0006-3495(82)84697-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Plescia J., Altieri D. C. Activation of Mac-1 (CD11b/CD18)-bound factor X by released cathepsin G defines an alternative pathway of leucocyte initiation of coagulation. Biochem J. 1996 Nov 1;319(Pt 3):873–879. doi: 10.1042/bj3190873. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rinder C. S., Bonan J. L., Rinder H. M., Mathew J., Hines R., Smith B. R. Cardiopulmonary bypass induces leukocyte-platelet adhesion. Blood. 1992 Mar 1;79(5):1201–1205. [PubMed] [Google Scholar]
- Rinder H. M., Bonan J. L., Rinder C. S., Ault K. A., Smith B. R. Activated and unactivated platelet adhesion to monocytes and neutrophils. Blood. 1991 Oct 1;78(7):1760–1769. [PubMed] [Google Scholar]
- Samsel R. W., Perelson A. S. Kinetics of rouleau formation. I. A mass action approach with geometric features. Biophys J. 1982 Feb;37(2):493–514. doi: 10.1016/S0006-3495(82)84696-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tandon P., Diamond S. L. Hydrodynamic effects and receptor interactions of platelets and their aggregates in linear shear flow. Biophys J. 1997 Nov;73(5):2819–2835. doi: 10.1016/S0006-3495(97)78311-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tandon P., Diamond S. L. Kinetics of beta2-integrin and L-selectin bonding during neutrophil aggregation in shear flow. Biophys J. 1998 Dec;75(6):3163–3178. doi: 10.1016/S0006-3495(98)77758-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Taylor A. D., Neelamegham S., Hellums J. D., Smith C. W., Simon S. I. Molecular dynamics of the transition from L-selectin- to beta 2-integrin-dependent neutrophil adhesion under defined hydrodynamic shear. Biophys J. 1996 Dec;71(6):3488–3500. doi: 10.1016/S0006-3495(96)79544-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
