A mathematical model for ligand/receptor/G-protein dynamics and actin polymerization in human neutrophils

Journal of Theoretical Biology

Volumn 193, Issue 4, 1998, Pages 543-560

  Adams, James A ^a   Omann, Geneva M ^b   Linderman, Jennifer J ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ACTIN BINDING PROTEIN; CHEMOTACTIC PEPTIDE; FLUORESCENT DYE; GUANINE NUCLEOTIDE BINDING PROTEIN; LIGAND; RECEPTOR;

ACTIN POLYMERIZATION; ARTICLE; HUMAN; LEUKOCYTE ACTIVATION; MATHEMATICAL MODEL; MOLECULAR DYNAMICS; NEUTROPHIL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

EID: 0032555422     PISSN: 00225193     EISSN: None     Source Type: Journal    
DOI: 10.1006/jtbi.1998.0721     Document Type: Article

References (72)

1. ADAMS, K. A. (1995). The dynamics of stimulated actin polymerization in human neutrophils. Ph.D. thesis, University of Michigan.
2. ALI, H., RICHARDSON, R. M., TOMHAVE, E. D., DIDSBURY, J. R. & SNYDERMAN, R. (1993). Differences in phosphorylation of formyl peptide and C5a chemoattractant receptors correlates with differences in desensitization. J. Biol. Chem. 268, 24247-24254.
3. BENGTSSON, T., SARNDAHL, E., STENDAHL, O. & ANDERSSON, T. (1990). Involvement of GTP-binding proteins in actin polymerization in human neutrophils. PNAS 87, 2921-2925.
4. BERMAN, D. M. & GILMAN, A. G. (1998). Mammalian RGS proteins: Barbarians at the gate. J. Biol. Chem. 273, 1269-1272.
5. n. J. Cell Biol. 106, 1927-1936.
6. CAMPS, M., CAROZZI, A., SCHNABEL, P., SCHEER, A., PARKER, P. J. & GIERSCHIK, P. (1992). Isozyme-selective stimulation of phospholipase C-β2 by G protein βγ-subunits. Nature 360, 684-686.
7. CANO, M. L., LAUFFENBURGER, D. A. & ZIGMOND, S. H. (1991). Kinetic analysis of F-actin depolymerization in polymorphonuclear leukocytes indicates that chemoattractant stimulation increases actin filament number without altering the filament length distribution. J. Cell Biol. 115, 677-687.
8. CARLIER, M. F. (1991). Actin: protein structure and filament dynamics. J. Biol. Chem. 266, 1-4.
9. CARSON, M., WEBER, A. & ZIGMOND, S. H. (1986). An actin-nucleating activity in polymorphonuclear leukocytes is modulated by chemotactic peptides. J. Cell Biol. 103, 2707-2714.
10. CASSIMERIS, L., MCNEIL, H. & ZIGMOND, S. H. (1990). Chemoattractant-stimulated polymorphonuclear leukocytes contain two populations of actin filaments that differ in their spatial distributions and relative stabilities. J. Cell Biol. 110, 1067-1075.
11. 4 sequesters the majority of G-actin in resting human polymorphonuclear leukocytes. J. Cell Biol. 119, 1261-1270.
12. CIVELEKOGLU, G. & EDELSTEIN-KESHET, L. (1994). Modelling the dynamics of F-actin in the cell. Bull. Math. Biol. 56, 587-616.
13. DEVREOTES, P. N. & ZIGMOND, S. H. (1988). Chemotaxis in eukaryotic cells: a focus on leukocytes. Ann. Rev. Cell Biol. 4, 649-686.
14. DOMALEWSKI, M. D., GUYER, D. A., FREER, R. J., MUTHUKU-MARASWAMY, N. & SKLAR, L. A. (1996). Fixation traps formyl peptide receptor in high and low affinity forms that can be regulated by GTP[S] in the absence of ligand. J. Receptor, Signal Transduc. Res. 16, 59-75.
15. FAY, S. P., POSNER, R. G., SWANN, W. N. & SKLAR, L. A. (1991). Real-time analysis of the assembly of ligand, receptor, and G protein by quantitative fluorescence flow cytometry. Biochemistry 30, 5066-5075.
16. FECHHEIMER, M. & ZIGMOND, S. H. (1983). Changes in cytoskeletal proteins of polymorphonuclear leukocytes induced by chemotactic peptides. Cell Motility 3, 349-361.
17. GANTZOS, R.D. & NEUBIG, R. R. (1988). Temperature effects on α2-adrenergic receptor-Gi interactions. Biochem. Pharm. 37, 2815-2821.
18. GOLDSCHMIDT-CLERMONT, P. J., FURMAN, M. I., WACHSSTOCK, D., SAFER, D., NACHIMIAS, V. T. & POLLARD, T. D. (1992). The control of actin nucleotide exchange by thymosin beta 4 and profilin. A potential regulatory mechanism for actin polymerization in cells. Mol. Biol. Cell 3, 1015-1024.
19. 4 in human blood cells and serum. J. Chromatography 397, 279-285.
20. HOFFMAN, J. F., LINDERMAN, J.J. & OMANN, G. M. (1996a). Receptor upregulation, internalization, and interconverting receptor states: critical components of a quantitative description of N-formyl peptide-receptor dynamics in the neutrophil. J. Biol. Chem. 271, 18394-18404.
21. HOFFMAN, J. F., OMANN, G. M. & LINDERMAN, J.J. (1996b). Interconverting receptor states at 4°C for the neutrophil N-formyl peptide receptor. Biochemistry 35, 13047-13055.
22. HOWARD, T., CHAPONNIER, C., YIN, H. & STOSSEL, T. (1990). Gelsolin-actin interaction and actin polymerization in human neutrophils. J. Cell Biol. 110, 1983-1991.
23. HOWARD, T. H. & MEYER, W. H. (1984). Chemotactic peptide modulation of actin assembly and locomotion in neutrophils. J. Cell Biol. 98, 1265-1271.
24. HOWARD, T. H. & ORESAJO, C. O. (1985a). The kinetics of chemotactic peptide-induced change in F-actin content, F-actin distribution, and the shape of neutrophils. J. Cell Biol. 101, 1078-1085.
25. HOWARD, T. H. & ORESAJO, C. O. (1985b). A method for quantifying F-actin in chemotactic peptide activated neutrophils: study of the effect of tBOC peptide. Cell Motility 5, 545-557.
26. JESAITIS, A. J. & ALLEN, R. A. (1988). Activation of the neutrophil respiratory burst by chemoattractants: regulation of the N-formyl peptide receptor in the plasma membrane. J. Bioenergetics Biomem. 20, 679-707.
27. JESAITIS, A. J., TOLLEY, J. O. & ALLEN, R. A. (1986). Receptor-cytoskeleton interactions and membrane traffic may regulate chemoattractant-induced superoxide production in human granulocytes. J. Biol. Chem. 261, 13662-13669.
28. JESAITIS, A. J., BOKOCH, G. M., TOLLEY, J. O. & ALLEN, R. A. (1988). Lateral segregation of neutrophil chemotactic receptors into actin-and fodrin-rich plasma membrane microdomains depleted in guanyl nucleotide regulatory proteins. J. Cell Biol. 107, 921-928.
29. JESAITIS, A. J., TOLLEY, J. O., BOKOCH, G. M. & ALLEN, R. A. (1989). Regulation of chemoattractant receptor interaction with transducing proteins by organizational control in the plasma membrane of human neutrophils. J. Cell Biol. 109, 2783-2790.
30. KATZ, A., WU, D. & SIMON, M. I. (1992). Subunits of βγ of heterotrimeric G protein activate β2 isoform of phospholipase C. Nature 360, 686-689.
31. LAUFFENBURGER, D. A. & LINDERMAN, J. J. (1993). Receptors: Models for Binding, Trafficking, and Signaling. New York, Oxford University Press.
32. MARASCO, W. A., FANTONE, J. C., FREER, R. J. & WARD, P. A. (1983). Characterization of the rat neutrophil formyl peptide chemotaxis receptor. Am. J. Pathol. 111, 273-281.
33. MCLEISH, K. R., GIERSCHIK, P. & JACOBS, K. H. (1989). Desensitization uncouples the formyl peptide receptor-guanine nucleotide binding protein interaction in HL60 cells. Mol. Pharm. 36, 384-390.
34. NEUBIG, R. R. & SKLAR, L. A. (1993). Subsecond modulation of formyl peptide-linked guanine nucleotide-binding proteins by guanosine 5′-o-(3-thio)triphosphate in permeabilized neutrophils. Mol. Pharm. 43, 734-740.
35. NEUBIG, R. R., GANTZOS, R. D. & THOMSEN, W. J. (1988). Mechanism of agonist and antagonist binding to α2 adrenergic receptors: evidence for a precoupled receptor-guanine nucleotide protein complex. Biochemistry 27, 2374-2384.
36. NORGAUER, J., EBERLE, M., FAY, S. P., LEMKE, H. D. & SKLAR, L. A. (1991). Kinetics of N-formyl peptide receptor up-regulation during stimulation in human neutrophils. J. Immun. 146, 975-980.
37. OMANN, G. M. (1998). Actin polymerization in human neutrophils. In: Phagocytic Function: A Guide for Research and Clinical Evaluation (Robinson, J. P. & Babrock, G. F., eds) p. 155. New York: Wiley-Liss.
38. OMANN, G. M. & SKLAR, L. A. (1988). Response of neutrophils to stimulus infusion: differential sensitivity of cytoskeletal activation and oxidant production. J. Cell Biol. 107, 951-958.
39. OMANN, G. M., ALLEN, R. A., BOKOCH, G. M., PAINTER, R. G., TRAYNOR, A. E. & SKLAR, L. A. (1987a). Signal transduction and cytoskeletal activation on the neutrophil. Physiol. Rev. 67, 285-322.
40. OMANN, G. M., TRAYNOR, A. E., HARRIS, A. & SKLAR, L. A. (1987b). LTB4-induced activation signals and responses in neutrophils are short-lived compared with formyl peptide. J. Immunol. 138, 2626-2632.
41. OMANN, G. M., HARTER, J. M., HASSAN, N., MANSFIELD, P. J., SUCHARD, S. J. & NEUBIG, R. R. (1992). A threshold level of coupled G-proteins is required to transduce neutrophil responses. J. Immunol. 149, 2172-2178.
42. OMANN, G. M., RENGAN, R., HOFFMAN, J. F. & LINDERMAN, J. J. (1995). Rapid oscillations of actin polymerization/depolymerization in polymorphonuclear leukocytes stimulated by leukotriene B4 and platelet activating factor. J. Immunol. 155, 5375-5381.
43. POLLARD, T. D. (1986). Rate constants for the reactions of ATP-and ADP-actin with the ends of actin filaments. J. Cell Biol. 103, 2747-2754.
44. POSNER, R. G., FAY, S. P., DOMALEWSKI, M. D. & SKLAR, L. A. (1994). Continuous spectrofluorometric analysis of formyl peptide receptor ternary complex interactions. Mol. Pharm. 45, 65-73.
45. PROSSNITZ, E. R., KIM, C. M., BENOVIC, J. L. & YE, R. D. (1995). Phosphorylation of the N-formyl peptide receptor carboxyl terminus by the G protein-coupled receptor kinase, GRK2. J. Biol. Chem. 270, 1130-1137.
46. SHEA, L. (1997). Kinetics of ligand, G-protein, and receptor interaction for signal transduction: a modeling study. Ph.D. thesis, University of Michigan.
47. SHEA, L. & LINDERMAN, J. J. (1997). Mechanistic model of G-protein signal transduction: determinants of efficacy and the effect of precoupled receptors. Biochem. Pharm. 53, 519-530.
48. SHEFCYK, J., YASSIN, R., VOLPI, M., MOLSKI, T. F. P., NACCACHE, P. H., MUNOZ, J. J., BECKER, E. L., FEINSTEIN, M. B. & SHA'AFI, R. I. (1985). Pertussis but not cholera toxin inhibits the stimulated increase in actin association with the cytoskeleton in rabbit neutrophils: role of the "G proteins" in stimulus-response coupling. Biochem. Biophys. Res. Commun. 126, 1174-1181.
49. SKLAR, L. A. (1986). Ligand-receptor dynamics and signal amplification in the neutrophil. Adv. Immunol. 39, 95-143.
50. SKLAR, L. A. (1987). Real-time spectroscopic analysis of ligand-receptor dynamics. Ann. Rev. Biophys. Biophys. Chem. 16, 479-506.
51. SKLAR, L. A. & OMANN, G. M. (1990). Kinetics of excitation and adaptation in polymorphonuclear leukocytes. Seminars Cell Biol. 1, 115-123.
52. SKLAR, L. A., FINNEY, D. A., OADES, Z. G., JESAITIS, A. J., PAINTER, R. G. & COCHRANE, C. G. (1984). The dynamics of ligand-receptor interactions. Real-time analyses of association, dissociation, and internalization of an N-formyl peptide and its receptors on the human neutrophil. J. Biol. Chem. 259, 5661-5669.
53. SKLAR, L. A., HYSLOP, P. A., OADES, Z. G., OMANN, G. M., JESAITIS, A. J., PAINTER, R. G. & COCHRANE, C. G. (1985a). Signal transduction and ligand-receptor dynamics in the human neutrophil. Transient responses and occupancy-response relations at the formyl peptide receptor. J. Biol. Chem. 260, 11461-11467.
54. ++. J. Cell Biol. 101, 1161-1166.
55. SKLAR, L. A., SAYRE, J., MCNEIL, V. M. & FINNEY, D. A. (1985c). Competitive binding kinetics in ligand-receptor-competitor system. Rate parameters for unlabeled ligands for the formyl peptide receptor. Mol. Pharm. 28, 323-330.
56. SKLAR, L. A., MUELLER, H., OMANN, G. & OADES, Z. (1989a). Three states for the formyl peptide receptor on intact cells. J. Biol. Chem. 264, 8483-8486.
57. SKLAR, L. A., MUELLER, H., SWANN, W. N., COMSTOCK, C., OMANN, G. M. & BOKOCH, G. M. (1989b). Dynamics of interaction among ligand, receptor, and G protein. In: ACS Symposium Series 383, Luminescence Applications in Biological, Chemical, Environmental, and Hydrological Sciences (Goldberg, M. C. ed.), Chap. 4, pp. 52-69. Washington D.C.: American Chemical Society.
58. SOUTHWICK, F. S. & YOUNG, C. L. (1990). The actin released from profilin-actin complexes is insufficient to account for the increase in F-Actin in chemoattractant-stimulated polymorphonuclear leukocytes. J. Cell Biol. 110, 1965-1973.
59. SOUTHWICK, F. S., DABIRI, G. A., PASCHETTO, M. & ZIGMOND, S. H. (1989). Polymorphonuclear leukocyte adherence induces actin polymerization by a transduction pathway which differs from that used by chemoattractants. J. Cell Biol. 109, 1561-1569.
60. TARDIF, M., MERY, L., BROUCHON, L. & BOULAY, F. (1993). Agonist-dependent phosphorylation of N-formyl peptide and activation peptide from the fifth complement component of C (C5a) chemoattractant receptors in differentiated HL60 cells. J. Immunol. 150, 3534-3545.
61. TARDIF, M., HUANG, S., REDMOND, T., SAFER, D., PRING, M. & ZIGMOND, S. H. (1995). Actin polymerization induced by GTP gamma S in permeabilized neutrophils is induced and maintained by free barbed ends. J. Biol. Chem. 270, 28075-28083.
62. TAYLOR, C. W. (1990). The role of G proteins in transmembrane signalling. Biochem. J. 272, 1-13.
63. THELEN, M., DEWALD, B. & BAGGIOLINI, M. (1993). Neutrophil signal transduction and activation of the respiratory burst. Physiol. Rev. 73 797-821.
64. THERRIEN, S. & NACCACHE, P. H. (1989). Guanine nucleotide-induced polymerization of actin in electropermeabilized human neutrophils. J. Cell Biol. 109, 1125-1132.
65. THOMPSEN, W. J. & NEUBIG, R. R. (1989). Rapid kinetics of α2-adrenergic inhibition of adenylate cyclase. Evidence for a distal rate-limiting step. Biochemistry 28, 8778-8786.
66. WALLACE, P. J., WERSTO, R. P., PACKMAN, C. H. & LICHTMAN, M. A. (1984). Chemotactic peptide-induced changes in neutrophil actin conformation. J. Cell Biol. 99, 1060-1065.
67. WANG, D., BERRY, K. & HOWARD, T. H. (1990). Kinetic analysis of chemotactic peptide-induced actin polymerization in neutrophils. Cell Mot. Cytoskeleton 16, 80-87.
68. WATTS, R. G. & HOWARD, T. H. (1993). Mechanisms for actin reorganization in chemotactic factor-activated polymorphonuclear leukocytes. Blood 81, 2750-2757.
69. 4 with muscle and platelet actin: implications for actin sequestration in resting platelets. Biochemistry 31, 6179-6185.
70. WEGNER, A. & ENGEL, J. (1975). Kinetics of the cooperative association of actin to actin filaments. Biophys. Chem. 3, 215-225.
71. WHITE, J. R., NACCACHE, P. H. & SHA'AFI, R. I. (1983). Stimulation by chemotactic factor of actin association with the cytoskeleton in rabbit neutrophils: effect of calcium and cytochalsin B. J. Biol. Chem. 258, 14041-14047.
72. ZIGMOND, S. H., SULLIVAN, S. J. & LAUFFENBURGER, D. A. (1982). Kinetic analysis of chemotactic peptide receptor modulation. J. Cell Biol. 92, 34-43.