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

Molecular Biology of the Cell

Volumn 23, Issue 2, 2012, Pages 324-336

  Revenu, Céline ^a,g   Ubelmann, Florent ^a   Hurbain, Ilse ^a,b   El Marjou, Fatima ^a   Dingli, Florent ^b   Loew, Damarys ^b   Delacour, Delphine ^c   Gilet, Jules ^d   Brot Laroche, Edith ^d   Rivero, Francisco ^e,f   Louvard, Daniel ^a   Robine, Sylvie ^a  

^a CNRS   (France)

^b INSTITUT CURIE   (France)

^c INSTITUT JACQUES MONOD   (France)

^d CENTRE DE RECHERCHE DES CORDELIERS   (France)

^e UNIVERSITY OF HULL   (United Kingdom)

^f UNIVERSITY OF HULL   (United Kingdom)

^g EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; MYOSIN I; MYOSIN IA; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; KNOCKOUT MOUSE; MALE; MICROVILLUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION;

ACTINS; ANIMALS; ENTEROCYTES; MEMBRANE GLYCOPROTEINS; MICE; MICE, KNOCKOUT; MICROFILAMENT PROTEINS; MICROSCOPY, ELECTRON, TRANSMISSION; MICROVILLI; MYOSIN HEAVY CHAINS; PROTEIN STRUCTURE, TERTIARY;

MUS;

EID: 84855882479     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-09-0765     Document Type: Article

References (62)

1. Atilgan E, Wirtz D, Sun SX (2006). Mechanics and dynamics of actin-driven thin membrane protrusions. Biophys J 90, 65-76.
2. Bartles JR (2000). Parallel actin bundles and their multiple actin-bundling proteins. Curr Opin Cell Biol 12, 72-78.
3. Bathe M, Heussinger C, Claessens MM, Bausch AR, Frey E (2008). Cytoskeletal bundle mechanics. Biophys J 94, 2955-2964.
4. Benesh AE, Nambiar R, McConnell RE, Mao S, Tabb DL, Tyska MJ (2010). Differential localization and dynamics of class I myosins in the enterocyte microvillus. Mol Biol Cell 21, 970-978.
5. Boeda B et al. (2002). Myosin VIIa, harmonin and cadherin 23, three Usher I gene products that cooperate to shape the sensory hair cell bundle. EMBO J 21, 6689-6699. (Pubitemid 36014541)
6. Brawley CM, Rock RS (2009). Unconventional myosin traffic in cells reveals a selective actin cytoskeleton. Proc Natl Acad Sci USA 106, 9685-9690.
7. Brown JW, McKnight CJ (2010). Molecular model of the microvillar cytoskeleton and organization of the brush border. PLoS One 5, e9406.
8. Campellone KG, Welch MD (2010). A nucleator arms race: cellular control of actin assembly. Nat Rev Mol Cell Biol 11, 237-251.
9. Claessens MM, Bathe M, Frey E, Bausch AR (2006). Actin-binding proteins sensitively mediate F-actin bundle stiffness. Nat Mater 5, 748-753. (Pubitemid 44320328)
10. Coluccio LM, Bretscher A (1989). Reassociation of microvillar core proteins: making a microvillar core in vitro. J Cell Biol 108, 495-502.
11. Costa de Beauregard MA, Pringault E, Robine S, Louvard D (1995). Suppression of villin expression by antisense RNA impairs brush border assembly in polarized epithelial intestinal cells. EMBO J 14, 409-421.
12. Cramm-Behrens CI, Dienst M, Jacob R (2008). Apical cargo traverses endosomal compartments on the passage to the cell surface. Traffic 9, 2206-2220.
13. Croce A, Cassata G, Disanza A, Gagliani MC, Tacchetti C, Malabarba MG, Carlier MF, Scita G, Baumeister R, Di Fiore PP (2004). A novel actin barbed-end-capping activity in EPS-8 regulates apical morphogenesis in intestinal cells of Caenorhabditis elegans. Nat Cell Biol 6, 1173-1179. (Pubitemid 39625115)
14. DesMarais V, Ichetovkin I, Condeelis J, Hitchcock-DeGregori SE (2002). Spatial regulation of actin dynamics: a tropomyosin-free, actin-rich compartment at the leading edge. J Cell Sci 115, 4649-4660. (Pubitemid 36007758)
15. Disanza A et al. (2006). Regulation of cell shape by Cdc42 is mediated by the synergic actin-bundling activity of the Eps8-IRSp53 complex. Nat Cell Biol 8, 1337-1347. (Pubitemid 44835108)
16. Ferrary E et al. (1999). In vivo, villin is required for Ca2+-dependent F-actin disruption in intestinal brush borders. J Cell Biol 146, 819-830.
17. Franck Z, Footer M, Bretscher A (1990). Microinjection of villin into cultured cells induces rapid and long-lasting changes in cell morphology but does not inhibit cytokinesis, cell motility, or membrane ruffling. J Cell Biol 111, 2475-2485. (Pubitemid 120014531)
18. Friederich E, Huet C, Arpin M, Louvard D (1989). Villin induces microvilli growth and actin redistribution in transfected fibroblasts. Cell 59, 461-475. (Pubitemid 19284460)
19. Grimm-Gunter EM, Revenu C, Ramos S, Hurbain I, Smyth N, Ferrary E, Louvard D, Robine S, Rivero F (2009). Plastin 1 binds to keratin and is required for terminal web assembly in the intestinal epithelium. Mol Biol Cell 20, 2549-2562.
20. Gruneberg H, Burnett JB, Snell GD (1941). The origin of jerker, a new gene mutation of the house mouse, and linkage studies made with it. Proc Natl Acad Sci USA 27, 562-565.
21. Hansen GH, Rasmussen K, Niels-Christiansen LL, Danielsen EM (2009). Endocytic trafficking from the small intestinal brush border probed with FM dye. Am J Physiol Gastrointest Liver Physiol 297, G708-G715.
22. Hertzog M et al. (2010). Molecular basis for the dual function of Eps8 on actin dynamics: bundling and capping. PLoS Biol 8, e1000387.
23. Hirokawa N, Cheney RE, Willard M (1983). Location of a protein of the fodrin-spectrin-TW260/240 family in the mouse intestinal brush border. Cell 32, 953-965.
24. Hirokawa N, Tilney LG, Fujiwara K, Heuser JE (1982). Organization of actin, myosin, and intermediate filaments in the brush border of intestinal epithelial cells. J Cell Biol 94, 425-443. (Pubitemid 12026794)
25. Janmey PA, Lamb J, Allen PG, Matsudaira PT (1992). Phosphoinositide- binding peptides derived from the sequences of gelsolin and villin. J Biol Chem 267, 11818-11823.
26. Liu AP, Richmond DL, Maibaum L, Pronk S, Geissler PL, Fletcher DA (2008). Membrane-induced bundling of actin filaments. Nat Phys 4, 789-793.
27. Loomis PA, Zheng L, Sekerkova G, Changyaleket B, Mugnaini E, Bartles JR (2003). Espin cross-links cause the elongation of microvillus-type parallel actin bundles in vivo. J Cell Biol 163, 1045-1055. (Pubitemid 37541880)
28. Matter K, Stieger B, Klumperman J, Ginsel L, Hauri HP (1990). Endocytosis, recycling, and lysosomal delivery of brush border hydrolases in cultured human intestinal epithelial cells (Caco-2). J Biol Chem 265, 3503-3512.
29. McConnell RE, Tyska MJ (2007). Myosin-1a powers the sliding of apical membrane along microvillar actin bundles. J Cell Biol 177, 671-681. (Pubitemid 46799838)
30. Mellor H (2010). The role of formins in filopodia formation. Biochim Biophys Acta 1803, 191-200.
31. Miyata H, Nishiyama S, Akashi K, Kinosita K., Jr. (1999). Protrusive growth from giant liposomes driven by actin polymerization. Proc Natl Acad Sci USA 96, 2048-2053. (Pubitemid 29117865)
32. Mogilner A, Rubinstein B (2005). The physics of filopodial protrusion. Biophys J 89, 782-795. (Pubitemid 41098966)
33. Nagy S, Ricca BL, Norstrom MF, Courson DS, Brawley CM, Smithback PA, Rock RS (2008). A myosin motor that selects bundled actin for motility. Proc Natl Acad Sci USA 105, 9616-9620. (Pubitemid 352031349)
34. Nagy S, Rock RS (2010). Structured post-IQ domain governs selectivity of myosin X for fascin-actin bundles. J Biol Chem 285, 26608-26617.
35. Naoz M, Manor U, Sakaguchi H, Kachar B, Gov NS (2008). Protein localization by actin treadmilling and molecular motors regulates stereocilia shape and treadmilling rate. Biophys J 95, 5706-5718.
36. +)ATPase and implications for the organization of membrane domains in polarized cells. Nature 328, 533-536.
37. Pellegrin S, Mellor H (2005). The Rho family GTPase Rif induces filopodia through mDia2. Curr Biol 15, 129-133.
38. Peskin CS, Odell GM, Oster GF (1993). Cellular motions and thermal fluctuations: the Brownian ratchet. Biophys J 65, 316-324. (Pubitemid 23206064)
39. Pinson KI, Dunbar L, Samuelson L, Gumucio DL (1998). Targeted disruption of the mouse villin gene does not impair the morphogenesis of microvilli. Dev Dyn 211, 109-121. (Pubitemid 28035816)
40. Prost J, Barbetta C, Joanny JF (2007). Dynamical control of the shape and size of stereocilia and microvilli. Biophys J 93, 1124-1133. (Pubitemid 47330893)
41. Revenu C, Athman R, Robine S, Louvard D (2004). The co-workers of actin filaments: from cell structures to signals. Nat Rev Mol Cell Biol 5, 635-646. (Pubitemid 39025064)
42. Ricca BL, Rock RS (2010). The stepping pattern of myosin X is adapted for processive motility on bundled actin. Biophys J 99, 1818-1826.
43. Rodriguez-Boulan E, Kreitzer G, Musch A (2005). Organization of vesicular trafficking in epithelia. Nat Rev Mol Cell Biol 6, 233-247. (Pubitemid 40314924)
44. Rzadzinska AK, Nevalainen EM, Prosser HM, Lappalainen P, Steel KP (2009). MyosinVIIa interacts with Twinfilin-2 at the tips of mechanosensory stereocilia in the inner ear. PLoS One 4, e7097.
45. Saotome I, Curto M, McClatchey AI (2004). Ezrin is essential for epithelial organization and villus morphogenesis in the developing intestine. Dev Cell 6, 855-864. (Pubitemid 38745419)
46. Sato T et al. (2007). The Rab8 GTPase regulates apical protein localization in intestinal cells. Nature 448, 366-369. (Pubitemid 47080335)
47. Tang N, Ostap EM (2001). Motor domain-dependent localization of myo1b (myr-1). Curr Biol 11, 1131-1135. (Pubitemid 32675767)
48. Temm-Grove CJ, Jockusch BM, Weinberger RP, Schevzov G, Helfman DM (1998). Distinct localizations of tropomyosin isoforms in LLC-PK1 epithelial cells suggests specialized function at cell-cell adhesions. Cell Motil Cytoskeleton 40, 393-407. (Pubitemid 28364159)
49. Tilney LG, Connelly PS, Ruggiero L, Vranich KA, Guild GM (2003). Actin filament turnover regulated by cross-linking accounts for the size, shape, location, and number of actin bundles in Drosophila bristles. Mol Biol Cell 14, 3953-3966. (Pubitemid 37186300)
50. Tilney LG, Connelly PS, Vranich KA, Shaw MK, Guild GM (1998). Why are two different cross-linkers necessary for actin bundle formation in vivo and what does each cross-link contribute? J Cell Biol 143, 121-133. (Pubitemid 28480522)
51. Tilney LG, Tilney MS (1988). The actin filament content of hair cells of the bird cochlea is nearly constant even though the length, width, and number of stereocilia vary depending on the hair cell location. J Cell Biol 107, 2563-2574.
52. Tilney LG, Tilney MS, Guild GM (1995). F actin bundles in Drosophila bristles. I. Two filament cross-links are involved in bundling. J Cell Biol 130, 629-638.
53. Tocchetti A et al. (2010). Loss of the actin remodeler Eps8 causes intestinal defects and improved metabolic status in mice. PLoS One 5, e9468.
54. Tokuo H, Ikebe M (2004). Myosin X transports Mena/VASP to the tip of filopodia. Biochem Biophys Res Commun 319, 214-220. (Pubitemid 38670182)
55. Tyska MJ, Mackey AT, Huang JD, Copeland NG, Jenkins NA, Mooseker MS (2005). Myosin-1a is critical for normal brush border structure and composition. Mol Biol Cell 16, 2443-2457. (Pubitemid 40632225)
56. Tyska MJ, Mooseker MS (2004). A role for myosin-1A in the localization of a brush border disaccharidase. J Cell Biol 165, 395-405. (Pubitemid 38649914)
57. Verpy E et al. (2000). A defect in harmonin, a PDZ domain-containing protein expressed in the inner ear sensory hair cells, underlies Usher syndrome type 1C. Nat Genet 26, 51-55.
58. Vignjevic D, Kojima S, Aratyn Y, Danciu O, Svitkina T, Borisy GG (2006). Role of fascin in filopodial protrusion. J Cell Biol 174, 863-875. (Pubitemid 44373735)
59. Weisz OA, Rodriguez-Boulan E (2009). Apical trafficking in epithelial cells: signals, clusters and motors. J Cell Sci 122, 4253-4266.
60. Yamashiro S, Yamakita Y, Ono S, Matsumura F (1998). Fascin, an actin-bundling protein, induces membrane protrusions and increases cell motility of epithelial cells. Mol Biol Cell 9, 993-1006. (Pubitemid 28457295)
61. Zheng L, Sekerkova G, Vranich K, Tilney LG, Mugnaini E, Bartles JR (2000). The deaf jerker mouse has a mutation in the gene encoding the espin actin-bundling proteins of hair cell stereocilia and lacks espins. Cell 102, 377-385.
62. Zigmond SH, Furukawa R, Fechheimer M (1992). Inhibition of actin filament depolymerization by the Dictyostelium 30,000-D actin-bundling protein. J Cell Biol 119, 559-567.