A new role for the architecture of microvillar actin bundles in apical retention of membrane proteins

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

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. © 2012 Revenu et al.

Citation

Revenu, C., Ubelmann, F., Hurbain, I., El-Marjou, F., Dingli, F., Loew, D., Delacour, D., Gilet, J., Brot-Laroche, E., Rivero, F., Louvard, D., & Robine, S. (2012). A new role for the architecture of microvillar actin bundles in apical retention of membrane proteins. Molecular Biology of the Cell, 23(2), 324-336. https://doi.org/10.1091/mbc.E11-09-0765

• Journal Article Type: Article
• Acceptance Date: Nov 16, 2011
• Online Publication Date: Nov 23, 2011
• Publication Date: Jan 15, 2012
• Deposit Date: Apr 1, 2022
• Publicly Available Date: Apr 20, 2022
• Journal: Molecular Biology of the Cell
• Print ISSN: 1059-1524
• Publisher: American Society for Cell Biology
• Peer Reviewed: Peer Reviewed
• Volume: 23
• Issue: 2
• Pages: 324-336
• DOI: https://doi.org/10.1091/mbc.E11-09-0765
• Public URL: https://hull-repository.worktribe.com/output/540974