Abstract
The acrosomal process of the sea cucumber Thyone briareus can extend 90 microm in 10 s, but an epithelial goldfish keratocyte can only glide a few microns in the same time. Both speeds reflect the rate of extension of an actin network. The difference is in the delivery of actin monomers to the polymerization region. Diffusion supplies monomers fast enough to support the observed speed of goldfish keratocytes, but previous models have indicated that the acrosomal process of Thyone extends too rapidly for diffusion to keep up. Here we reexamine the assumptions made in earlier models and present a new model, the Actin Reconcentration Model, that includes more biological detail. Salt and water fluxes during the acrosomal reaction and the nonideality of the cytoplasm are particularly significant for actin delivery. We find that the variability of the acrosomal growth curve can be explained by the salt and water fluxes, and that nonideality magnifies the effect of actin concentration changes. We calculate the speed of process growth using biologically relevant parameters from the literature and find that the predictions of the model fall among the experimental data.
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- Agre P., Preston G. M., Smith B. L., Jung J. S., Raina S., Moon C., Guggino W. B., Nielsen S. Aquaporin CHIP: the archetypal molecular water channel. Am J Physiol. 1993 Oct;265(4 Pt 2):F463–F476. doi: 10.1152/ajprenal.1993.265.4.F463. [DOI] [PubMed] [Google Scholar]
- Bray D., White J. G. Cortical flow in animal cells. Science. 1988 Feb 19;239(4842):883–888. doi: 10.1126/science.3277283. [DOI] [PubMed] [Google Scholar]
- Condeelis J. Life at the leading edge: the formation of cell protrusions. Annu Rev Cell Biol. 1993;9:411–444. doi: 10.1146/annurev.cb.09.110193.002211. [DOI] [PubMed] [Google Scholar]
- Conrad P. A., Nederlof M. A., Herman I. M., Taylor D. L. Correlated distribution of actin, myosin, and microtubules at the leading edge of migrating Swiss 3T3 fibroblasts. Cell Motil Cytoskeleton. 1989;14(4):527–543. doi: 10.1002/cm.970140410. [DOI] [PubMed] [Google Scholar]
- Cooper J. A. The role of actin polymerization in cell motility. Annu Rev Physiol. 1991;53:585–605. doi: 10.1146/annurev.ph.53.030191.003101. [DOI] [PubMed] [Google Scholar]
- Cossart P. Actin-based bacterial motility. Curr Opin Cell Biol. 1995 Feb;7(1):94–101. doi: 10.1016/0955-0674(95)80050-6. [DOI] [PubMed] [Google Scholar]
- Cudmore S., Cossart P., Griffiths G., Way M. Actin-based motility of vaccinia virus. Nature. 1995 Dec 7;378(6557):636–638. doi: 10.1038/378636a0. [DOI] [PubMed] [Google Scholar]
- DeBiasio R. L., Wang L. L., Fisher G. W., Taylor D. L. The dynamic distribution of fluorescent analogues of actin and myosin in protrusions at the leading edge of migrating Swiss 3T3 fibroblasts. J Cell Biol. 1988 Dec;107(6 Pt 2):2631–2645. doi: 10.1083/jcb.107.6.2631. [DOI] [PMC free article] [PubMed] [Google Scholar]
- DeRosier D. J., Tilney L. G. The form and function of actin. A product of its unique design. Cell Muscle Motil. 1984;5:139–169. doi: 10.1007/978-1-4684-4592-3_3. [DOI] [PubMed] [Google Scholar]
- Goldberg M. B., Theriot J. A. Shigella flexneri surface protein IcsA is sufficient to direct actin-based motility. Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6572–6576. doi: 10.1073/pnas.92.14.6572. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gros G. Concentration dependence of the self-diffusion of human and Lumbricus terrestris hemoglobin. Biophys J. 1978 Jun;22(3):453–468. doi: 10.1016/S0006-3495(78)85499-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Han J., Herzfeld J. Macromolecular diffusion in crowded solutions. Biophys J. 1993 Sep;65(3):1155–1161. doi: 10.1016/S0006-3495(93)81145-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Heinzen R. A., Hayes S. F., Peacock M. G., Hackstadt T. Directional actin polymerization associated with spotted fever group Rickettsia infection of Vero cells. Infect Immun. 1993 May;61(5):1926–1935. doi: 10.1128/iai.61.5.1926-1935.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Inoué S., Tilney L. G. Acrosomal reaction of thyone sperm. I. Changes in the sperm head visualized by high resolution video microscopy. J Cell Biol. 1982 Jun;93(3):812–819. doi: 10.1083/jcb.93.3.812. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lanni F., Taylor D. L., Ware B. R. Fluorescence photobleaching recovery in solutions of labeled actin. Biophys J. 1981 Aug;35(2):351–364. doi: 10.1016/S0006-3495(81)84794-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lanni F., Ware B. R. Detection and characterization of actin monomers, oligomers, and filaments in solution by measurement of fluorescence photobleaching recovery. Biophys J. 1984 Jul;46(1):97–110. doi: 10.1016/S0006-3495(84)84002-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lee J., Ishihara A., Theriot J. A., Jacobson K. Principles of locomotion for simple-shaped cells. Nature. 1993 Mar 11;362(6416):167–171. doi: 10.1038/362167a0. [DOI] [PubMed] [Google Scholar]
- Mitchison T. J., Cramer L. P. Actin-based cell motility and cell locomotion. Cell. 1996 Feb 9;84(3):371–379. doi: 10.1016/s0092-8674(00)81281-7. [DOI] [PubMed] [Google Scholar]
- Muramatsu N., Minton A. P. Tracer diffusion of globular proteins in concentrated protein solutions. Proc Natl Acad Sci U S A. 1988 May;85(9):2984–2988. doi: 10.1073/pnas.85.9.2984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Oster G. F., Perelson A. S. The physics of cell motility. J Cell Sci Suppl. 1987;8:35–54. doi: 10.1242/jcs.1987.supplement_8.3. [DOI] [PubMed] [Google Scholar]
- Pantaloni D., Carlier M. F. How profilin promotes actin filament assembly in the presence of thymosin beta 4. Cell. 1993 Dec 3;75(5):1007–1014. doi: 10.1016/0092-8674(93)90544-z. [DOI] [PubMed] [Google Scholar]
- Peskin C. S., Odell G. M., Oster G. F. Cellular motions and thermal fluctuations: the Brownian ratchet. Biophys J. 1993 Jul;65(1):316–324. doi: 10.1016/S0006-3495(93)81035-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pollard T. D. Rate constants for the reactions of ATP- and ADP-actin with the ends of actin filaments. J Cell Biol. 1986 Dec;103(6 Pt 2):2747–2754. doi: 10.1083/jcb.103.6.2747. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pring M., Weber A., Bubb M. R. Profilin-actin complexes directly elongate actin filaments at the barbed end. Biochemistry. 1992 Feb 18;31(6):1827–1836. doi: 10.1021/bi00121a035. [DOI] [PubMed] [Google Scholar]
- Sanger J. M., Chang R., Ashton F., Kaper J. B., Sanger J. W. Novel form of actin-based motility transports bacteria on the surfaces of infected cells. Cell Motil Cytoskeleton. 1996;34(4):279–287. doi: 10.1002/(SICI)1097-0169(1996)34:4<279::AID-CM3>3.0.CO;2-3. [DOI] [PubMed] [Google Scholar]
- Schackmann R. W., Christen R., Shapiro B. M. Membrane potential depolarization and increased intracellular pH accompany the acrosome reaction of sea urchin sperm. Proc Natl Acad Sci U S A. 1981 Oct;78(10):6066–6070. doi: 10.1073/pnas.78.10.6066. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Smith S. J. Neuronal cytomechanics: the actin-based motility of growth cones. Science. 1988 Nov 4;242(4879):708–715. doi: 10.1126/science.3055292. [DOI] [PubMed] [Google Scholar]
- Southwick F. S., Purich D. L. Dynamic remodeling of the actin cytoskeleton: lessons learned from Listeria locomotion. Bioessays. 1994 Dec;16(12):885–891. doi: 10.1002/bies.950161206. [DOI] [PubMed] [Google Scholar]
- Tait J. F., Frieden C. Polymerization and gelation of actin studied by fluorescence photobleaching recovery. Biochemistry. 1982 Jul 20;21(15):3666–3674. doi: 10.1021/bi00258a022. [DOI] [PubMed] [Google Scholar]
- Teysseire N., Chiche-Portiche C., Raoult D. Intracellular movements of Rickettsia conorii and R. typhi based on actin polymerization. Res Microbiol. 1992 Nov-Dec;143(9):821–829. doi: 10.1016/0923-2508(92)90069-z. [DOI] [PubMed] [Google Scholar]
- Theriot J. A., Mitchison T. J. Actin microfilament dynamics in locomoting cells. Nature. 1991 Jul 11;352(6331):126–131. doi: 10.1038/352126a0. [DOI] [PubMed] [Google Scholar]
- Theriot J. A., Mitchison T. J. Comparison of actin and cell surface dynamics in motile fibroblasts. J Cell Biol. 1992 Oct;119(2):367–377. doi: 10.1083/jcb.119.2.367. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Theriot J. A., Mitchison T. J. The three faces of profilin. Cell. 1993 Dec 3;75(5):835–838. doi: 10.1016/0092-8674(93)90527-w. [DOI] [PubMed] [Google Scholar]
- Theriot J. A., Mitchison T. J., Tilney L. G., Portnoy D. A. The rate of actin-based motility of intracellular Listeria monocytogenes equals the rate of actin polymerization. Nature. 1992 May 21;357(6375):257–260. doi: 10.1038/357257a0. [DOI] [PubMed] [Google Scholar]
- Theriot J. A. The cell biology of infection by intracellular bacterial pathogens. Annu Rev Cell Dev Biol. 1995;11:213–239. doi: 10.1146/annurev.cb.11.110195.001241. [DOI] [PubMed] [Google Scholar]
- Tilney L. G. Actin, motility, and membranes. Soc Gen Physiol Ser. 1979;33:163–186. [PubMed] [Google Scholar]
- Tilney L. G., DeRosier D. J., Tilney M. S. How Listeria exploits host cell actin to form its own cytoskeleton. I. Formation of a tail and how that tail might be involved in movement. J Cell Biol. 1992 Jul;118(1):71–81. doi: 10.1083/jcb.118.1.71. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tilney L. G., DeRosier D. J., Weber A., Tilney M. S. How Listeria exploits host cell actin to form its own cytoskeleton. II. Nucleation, actin filament polarity, filament assembly, and evidence for a pointed end capper. J Cell Biol. 1992 Jul;118(1):83–93. doi: 10.1083/jcb.118.1.83. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tilney L. G., Inoué S. Acrosomal reaction of Thyone sperm. II. The kinetics and possible mechanism of acrosomal process elongation. J Cell Biol. 1982 Jun;93(3):820–827. doi: 10.1083/jcb.93.3.820. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tilney L. G., Inoué S. Acrosomal reaction of the Thyone sperm. III. The relationship between actin assembly and water influx during the extension of the acrosomal process. J Cell Biol. 1985 Apr;100(4):1273–1283. doi: 10.1083/jcb.100.4.1273. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tilney L. G., Kallenbach N. Polymerization of actin. VI. The polarity of the actin filaments in the acrosomal process and how it might be determined. J Cell Biol. 1979 Jun;81(3):608–623. doi: 10.1083/jcb.81.3.608. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tilney L. G., Kiehart D. P., Sardet C., Tilney M. Polymerization of actin. IV. Role of Ca++ and H+ in the assembly of actin and in membrane fusion in the acrosomal reaction of echinoderm sperm. J Cell Biol. 1978 May;77(2):536–550. doi: 10.1083/jcb.77.2.536. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhu C., Skalak R. A continuum model of protrusion of pseudopod in leukocytes. Biophys J. 1988 Dec;54(6):1115–1137. doi: 10.1016/S0006-3495(88)83047-9. [DOI] [PMC free article] [PubMed] [Google Scholar]