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Stochastic model of leukocyte chemosensory movement. (English) Zbl 0628.92017

The goal of the paper is to examine a unifying hypothesis for the two modes of cell migration behaviour exhibited by leukocytes: random motility - the persistent random walk behaviour of cells in uniform concentrations of chemoattractants, and chemotaxis - the biased random walk of cells observed in gradients of chemoattractants.
It is proposed that random motility is observed in macroscopically uniform concentrations because the cell perceives fluctuating gradients without a mean direction. The excepted response is an unbiased random walk characteristic of random motility. Chemotaxis is observed in macroscopic gradients because of perceived fluctuations in direction as well as magnitude around the mean gradient. The expected response is the biased random walk characteristic of chemotaxis.
The model of the cell can be formalized as a deterministic transformation (receptor - singal transduction) and response (translation with turning) of a stochastic signal not coupled to the response. The modeling equations for the particular mechanisms employed in the general model constitute a stochastic differential system in the sense of Itô.
Reviewer: Silvia Curteanu

MSC:

92Cxx Physiological, cellular and medical topics
92C05 Biophysics
Full Text: DOI

References:

[1] Allan, R. B., Wilkinson, P. C.: A visual analysis of chemotactic and chemokinetic locomotion of human neutrophil leucocytes. Exp. Cell Res. 111, 191-203 (1978) · doi:10.1016/0014-4827(78)90249-5
[2] Alt, W.: Biased random walk models for chemotaxis and related diffusion approximations. J. Math. Biol. 9, 147-177 (1980) · Zbl 0434.92001 · doi:10.1007/BF00275919
[3] Del Grosso, G., Marchetti, F.: Limit theorems in stochastic biochemical modeling. Math. Biosci. 66, 157-165 (1983) · Zbl 0532.92008 · doi:10.1016/0025-5564(83)90086-X
[4] DeLisi, C., Wiegel, F. W.: Effect of nonspecific forces and finite receptor number on rate constants of ligand-cell bound-receptor interactions. Proc. Natl. Acad. Sci. USA 78, 5569-5572 (1981) · doi:10.1073/pnas.78.9.5569
[5] Dembo, M., Harlow, F. J., Alt, W.: The biophysics of cell surface motility. In: Perelson, A., DeLisi, C., Wiegel, F. (eds.) Cell surface dynamics: concepts and models, pp. 495-543. Marcel Dekker: New York 1984
[6] Dunn, G. A.: Chemotaxis as a form of directed cell behavior: some theoretical considerations. In: Lackie, J. M., Wilkinson, P. C. (eds.) Biology of the chemotactic response, pp. 1-26. Cambridge: Cambridge University Press 1981
[7] Dunn, G. A.: Characterizing a kinesis response: time averaged measures of cell speed and directional persistence. Agents and Actions Suppl. 12, 14-33 (1983)
[8] Fisher, P. R., Grant, W. N., Dohrmann, U., Williams, K. L.: Spontaneous turning behaviour by dictyostelium discoideum slugs. J. Cell. Sci. 62, 161-170 (1983)
[9] Gail, M. H., Boone, C. W.: The locomotion of mouse fibroblasts in tissue culture. Biophys. J. 10, 980-993 (1970) · doi:10.1016/S0006-3495(70)86347-0
[10] Gardiner, C. W.: Handbook of stochastic methods for physics, chemistry and the natural sciences. New York-Heidelberg-Berlin: Springer 1983 · Zbl 0515.60002
[11] Gerisch, G., Keller, H. U.: Chemotactic reorientation of granulocytes stimulated with micropipettes containing f-met-leu-phe. J. Cell. Sci. 52, 1-10 (1981)
[12] Gihman, I. I., Skorohod, A. V.: Introduction to the theory of random processes. Philadelphia: Saunders 1969 · Zbl 0291.60019
[13] Hall, R. L.: Amoeboid movement as a correlated walk. J. Math. Biol. 4, 327-335 (1977) · Zbl 0375.92009 · doi:10.1007/BF00275081
[14] Keller, H. U., Wilkinson, P. C., Abercrombie, M., Beker, E. L., Hirsch, J. G., Miller, M. E., Ramsey, W. S., Zigmond, S. H.: A proposal for the definition of terms related to locomotion of leukocytes and other cells. Clin. Exp. Immunol. 27, 377-380 (1977)
[15] Krenner, A. J., Lobry, C.: The complexity of stochastic differential equations. Stochastics 4, 193-203 (1981) · Zbl 0452.60069
[16] Kurtz, T. G.: Approximation of population processes. Philadelphia: SIAM 1981 · Zbl 0465.60078
[17] Lackie, J. M., Burns, M. D.: Leucocyte locomotion: Comparison of random and directed paths using a modified time-lapse film analysis. J. Immunol. Meth. 62, 109-122 (1983) · doi:10.1016/0022-1759(83)90116-3
[18] Lackie, J. M., Wilkinson, P. C.: Adhesion and locomotion of neutrophil leukocytes on 2-D substrata and in 3-D matrices. In: White cell mechanics: basic science and clinical aspects, pp. 237-254. New York: Liss 1984
[19] Lauffenburger, D. A.: Influence of external concentration fluctuations on leukocyte chemotactic orientation. Cell Biophys. 4, 177-209 (1982)
[20] Lauffenburger, D. A.: Measurement of phenomenological parameters for leukocyte random motility and chemotaxis. Agents Actions Suppl. 12, 34-53 (1982)
[21] Lauffenburger, D. A.: Transport vs. reaction-limitation in receptor-ligand binding: Consequences for chemosensory cell behavior. Presented at: The 1985 Annual AIChE Meeting, Chicago, November 10-15, 1985
[22] Maher, J., Martell, J. V., Brantley, B. A., Cox, E. B., Neidel, J. E., Rosse, W. F.: The response of human neutrophils to a chemotactic tripeptide (N-formyl-methionyl-leucyl-phenylalanine) studied by microcinematography. Blood 64, 221-228 (1984)
[23] Mardia, K. V.: Statistics of directional data. New York: Academic Press 1972 · Zbl 0244.62005
[24] Mil’shtein, G. N.: Approximate integration of stochastic differential equations. Theor. Probab. 19, 557-562 (1974)
[25] Nossal, R., Zigmond, S. H.: Chemotropism indices for polymorphonuclear leukocytes. Biophys. J. 16, 1171-1182 (1976) · doi:10.1016/S0006-3495(76)85766-9
[26] Oster, G. F., Perelson, A. S.: Cell spreading and motility. J. Math. Biol. 21, 383-388 (1985) · Zbl 0558.92004 · doi:10.1007/BF00276234
[27] Pardoux, E., Talay, D.: Discretization and simulation of stochastic differential equations. Acta Applicandae Math. 3, 23-47 (1985) · Zbl 0554.60062 · doi:10.1007/BF01438265
[28] Ramsey, W. S.: Analysis of individual leukocyte behavior during chemotaxis. Exptl. Cell Res. 70, 129-139 (1972) · doi:10.1016/0014-4827(72)90190-5
[29] Rumelin, W.: Numerical treatment of stochastic differential equations. SIAM J. Numer. Anal. 19, 604-613 (1982) · Zbl 0496.65038 · doi:10.1137/0719041
[30] Shields, J. M., Haston, W. S.: Behavior of neutrophil leucocytes in uniform concentrations of chemotactic factors: contraction waves, cell polarity, and persistence. J. Cell Sci. 74, 75-93 (1985)
[31] Soong, T. T.: Random differential equations in science and engineering. New York: Academic Press 1973 · Zbl 0348.60081
[32] Sullivan, S. J., Daukas, G., Zigmond, S. H.: Asymmetric distribution of the chemotactic receptor on polymorphonuclear leukocytes. J. Cell Biol. 99, 1461-1467 (1984) · doi:10.1083/jcb.99.4.1461
[33] Sullivan, S. J., Zigmond, S. H.: Chemotactic peptide receptor modulation in polymorphonuclear leukocytes. J. Cell Biol. 85, 703-711 (1980) · doi:10.1083/jcb.85.3.703
[34] Tranquillo, R. T. Phenomenological and fundamental descriptions of leukocyte random motility and chemotaxis. Ph.D. Thesis, Department of Chemical Engineering, University of Pennsylvania 1986
[35] Tranquillo, R. T., Lauffenburger, D. A.: Consequences of chemosensory phenomena for leukocyte chemotactic orientation. Cell Biophys. 8, 1-46 (1986)
[36] Tranquillo, R. T., Lauffenburger, D. A.: Analysis of leukocyte chemosensory movement. In: Mauri, C., Rizzo, S. V., Ricevuti, G. (eds.) The biological and clinical aspects of phagocyte function. Oxford: Pergamon 1987 · Zbl 0628.92017
[37] Wright, D. J.: The digital simulation of stochastic differential equations. IEEE Trans. Auto Control 19, 75-76 (1974) · Zbl 0279.60049 · doi:10.1109/TAC.1974.1100468
[38] Zigmond, S. H.: Ability of polymorphonuclear leukocytes to orient in gradients of chemotactic factors. J. Cell Biol. 75, 606-616 (1977) · doi:10.1083/jcb.75.2.606
[39] Zigmond, S. H., Sullivan, S. J. Sensory adaptation of leukocytes to chemotactic peptides. J. Cell Biol. 82, 517-527 (1979) · doi:10.1083/jcb.82.2.517
[40] Zigmond, S. H., Klausner, R., Tranquillo, R. T., Lauffenburger, D. A.: Analysis of the requirements for time-averaging of the receptor occupancy for gradient detection by polymorphonuclear leukocytes. In: Membrane receptors and cellular regulation, pp. 347-356. New York: Liss 1985
[41] Zigmond, S. H., Levitsky, H. I., Kreel, B. J.: Cell polarity: an examination of its behavioral expression and its consequences for polymorphonuclear leukocyte chemotaxis. J. Cell Biol. 89, 585-592 (1981) · doi:10.1083/jcb.89.3.585
[42] Zigmond, S. H., Slonczewski, J. L., Wilde, M. W., Carson, M.: Calcium and the regulation of cell locomotion. In: M. Eisenbach, Balaban, M. (eds.) Sensing and response in microorganisms, pp. 195-211. Amsterdam-New York: Elsevier 1985
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