Fibronectin receptor exhibits high lateral mobility in embryonic locomoting cells but is immobile in focal contacts and fibrillar streaks in stationary cells

doi:10.1083/jcb.107.4.1385

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Fibronectin receptor exhibits high lateral mobility in embryonic locomoting cells but is immobile in focal contacts and fibrillar streaks in stationary cells

JL Duband, GH Nuckolls, A Ishihara, T Hasegawa, KM Yamada, JP Thiery and K Jacobson
Centre National de la Recherche Scientifique, Ecole Normale Superieure, Paris, France.

The dynamic process of embryonic cell motility was investigated by analyzing the lateral mobility of the fibronectin receptor in various locomotory or stationary avian embryonic cells, using the technique of fluorescence recovery after photobleaching. The lateral mobility of fibronectin receptors, labeled by a monoclonal antibody, was defined by the diffusion coefficient and mobile fraction of these receptors. Even though the lateral diffusion coefficient did not vary appreciably (2 X 10(-10) cm2/S less than or equal to D less than or equal to 4 X 10(-10) cm2/S) with the locomotory state and the cell type, the mobile fraction was highly dependent on the degree of cell motility. In locomoting cells, the population of fibronectin receptors, which was uniformly distributed on the cell surface, displayed a high mobile fraction of 66 +/- 19% at 25 degrees C (82 +/- 14% at 37 degrees C). In contrast, in nonmotile cells, the population of receptors was concentrated in focal contacts and fibrillar streaks associated with microfilament bundles and, in these sites, the mobile fraction was small (16 +/- 8%). When cells were in a stage intermediate between highly motile and stationary, the population of fibronectin receptors was distributed both in focal contacts with a small mobile fraction and in a diffuse pattern with a reduced mobile fraction (33 +/- 9%) relative to the diffuse population in highly locomotory cells. The mobile fraction of the fibronectin receptor was found to be temperature dependent in locomoting but not in stationary cells. The mobile fraction could be modulated by affecting the interaction between the receptor and the substratum. The strength of this interaction could be increased by growing cells on a substratum coated with polyclonal antibodies to the receptor. This caused the mobile fraction to decrease. The interaction could be decreased by using a probe, monoclonal antibodies to the receptor known to perturb the adhesion of certain cell types which caused the mobile fraction to increase. From these results, we conclude that in locomoting embryonic cells, most fibronectin receptors can readily diffuse in the plane of the membrane. This degree of lateral mobility may be correlated to the labile adhesions to the substratum presumably required for high motility. In contrast, fibronectin receptors in stationary cells are immobilized in focal contacts and fibrillar streaks which are in close association with both extracellular and cytoskeletal structures; these stable complexes appear to provide firm anchorage to the substratum.
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Appeddu, P., Shur, B. (1994). Control of stable lamellipodia formation by expression of cell surface beta 1,4-galactosyltransferase cytoplasmic domains. J. Cell Sci. 107: 2535-2545 [Abstract]
Clyman, R., Tannenbaum, J, Chen, Y., Cooper, D, Yurchenco, P., Kramer, R., Waleh, N. (1994). Ductus arteriosus smooth muscle cell migration on collagen: dependence on laminin and its receptors. J. Cell Sci. 107: 1007-1018 [Abstract]
Tranqui, L, Usson, Y, Marie, C, Block, M. (1993). Adhesion of CHO cells to fibronectin is mediated by functionally and structurally distinct adhesion plaques. J. Cell Sci. 106: 377-387 [Abstract]
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Delannet, M, Duband, J. (1992). Transforming growth factor-beta control of cell-substratum adhesion during avian neural crest cell emigration in vitro. Development 116: 275-287 [Abstract]
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Rodriguez-Boulan, E, Nelson, W. (1989). Morphogenesis of the polarized epithelial cell phenotype. Science 245: 718-725 [Abstract]
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