A new role for the architecture of microvillar actin bundles in apical retention of membrane proteins |
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Authors: | Revenu Céline Ubelmann Florent Hurbain Ilse El-Marjou Fatima Dingli Florent Loew Damarys Delacour Delphine Gilet Jules Brot-Laroche Edith Rivero Francisco Louvard Daniel Robine Sylvie |
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Affiliation: | Unité Mixte de Recherche 144, Centre National de la Recherche Scientifique, Institut Curie, 75248 Paris, Cedex 05, France. revenu@embl.de |
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Abstract: | Actin-bundling proteins are identified as key players in the morphogenesis of thin membrane protrusions. Until now, functional redundancy among the actin-bundling proteins villin, espin, and plastin-1 has prevented definitive conclusions regarding their role in intestinal microvilli. We report that triple knockout mice lacking these microvillar actin-bundling proteins suffer from growth delay but surprisingly still develop microvilli. However, the microvillar actin filaments are sparse and lack the characteristic organization of bundles. This correlates with a highly inefficient apical retention of enzymes and transporters that accumulate in subapical endocytic compartments. Myosin-1a, a motor involved in the anchorage of membrane proteins in microvilli, is also mislocalized. These findings illustrate, in vivo, a precise role for local actin filament architecture in the stabilization of apical cargoes into microvilli. Hence, the function of actin-bundling proteins is not to enable microvillar protrusion, as has been assumed, but to confer the appropriate actin organization for the apical retention of proteins essential for normal intestinal physiology. |
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