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Abstract

Microvilli are actin-based structures found on the apical aspect of many epithelial cells. In this review, we discuss different types of microvilli, as well as comparisons with actin-based sensory stereocilia and filopodia. Much is known about the actin-bundling proteins of these structures; we summarize recent studies that focus on the components of the microvillar membrane. We pay special attention to mechanisms of membrane microfilament attachment by the ezrin/radixin/moesin family and regulation of this protein family. We also discuss the NHERF family of scaffolding proteins that are found in microvilli and their role in microvilli regulation. Microvilli on cultured cells are not static structures, and their dynamics and those of their components are discussed. Finally, we mention diseases related to microvilli and outline questions that our current knowledge will allow the field to address in the near future.

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2015-11-13
2024-06-14
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Literature Cited

  1. Ahmed S, Goh WI, Bu W. 2010. I-BAR domains, IRSp53 and filopodium formation. Semin. Cell Dev. Biol. 21:4350–56 [Google Scholar]
  2. Ahuja R, Pinyol R, Reichenbach N, Custer L, Klingensmith J. et al. 2007. Cordon-bleu is an actin nucleation factor and controls neuronal morphology. Cell 131:2337–50 [Google Scholar]
  3. Al-Momany A, Li L, Alexander RT, Ballermann BJ. 2014. Clustered PI(4,5)P2 accumulation and ezrin phosphorylation in response to CLIC5A. J. Cell Sci. 127:245164–78 [Google Scholar]
  4. Algrain M, Turunen O, Vaheri A, Louvard D, Arpin M. 1993. Ezrin contains cytoskeleton and membrane binding domains accounting for its proposed role as a membrane-cytoskeletal linker. J. Cell Biol. 120:1129–39 [Google Scholar]
  5. Antonescu CN, Aguet F, Danuser G, Schmid SL. 2011. Phosphatidylinositol-(4,5)-bisphosphate regulates clathrin-coated pit initiation, stabilization, and size. Mol. Biol. Cell 22:142588–600 [Google Scholar]
  6. Ardura JA, Friedman PA. 2011. Regulation of G protein–coupled receptor function by Na+/H+ exchange regulatory factors. Pharmacol. Rev. 63:4882–900 [Google Scholar]
  7. Argueso P, Guzman-Aranguez A, Mantelli F, Cao Z, Ricciuto J, Panjwani N. 2009. Association of cell surface mucins to galectin-3 contributes to the ocular surface epithelial barrier. J. Biol. Chem. 284:3423037–45 [Google Scholar]
  8. Balla T. 2013. Phosphoinositides: tiny lipids with giant impact on cell regulation. Physiol. Rev. 93:31019–137 [Google Scholar]
  9. Barret C, Roy C, Montcourrier P, Mangeat P, Niggli V. 2000. Mutagenesis of the phosphatidylinositol 4,5-bisphosphate (PIP2) binding site in the NH2-terminal domain of ezrin correlates with its altered cellular distribution. J. Cell Biol. 151:51067–80 [Google Scholar]
  10. Bartles JR. 1998. Small espin: a third actin-bundling protein and potential forked protein ortholog in brush border microvilli. J. Cell Biol. 143:1107–19 [Google Scholar]
  11. Bazari WL, Matsudaira P, Wallek M, Smeal T, Jakes R, Ahmed Y. 1988. Villin sequence and peptide map identify six homologous domains. PNAS 85:144986–90 [Google Scholar]
  12. Beau I, Berger A, Servin AL. 2007. Rotavirus impairs the biosynthesis of brush-border-associated dipeptidyl peptidase IV in human enterocyte-like Caco-2/TC7 cells. Cell. Microbiol. 9:3779–89 [Google Scholar]
  13. Belkina NV, Liu Y, Hao J-J, Karasuyama H, Shaw S. 2009. LOK is a major ERM kinase in resting lymphocytes and regulates cytoskeletal rearrangement through ERM phosphorylation. PNAS 106:124707–12 [Google Scholar]
  14. Ben-Aissa K, Patino-Lopez G, Belkina NV, Maniti O, Rosales T. et al. 2012. Activation of moesin, a protein that links actin cytoskeleton to the plasma membrane, occurs by phosphatidylinositol 4,5-bisphosphate (PIP2) binding sequentially to two sites and releasing an autoinhibitory linker. J. Biol. Chem. 287:2016311–23 [Google Scholar]
  15. 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 21:6970–78 [Google Scholar]
  16. Bennett V, Baines AJ. 2001. Spectrin and ankyrin-based pathways: metazoan inventions for integrating cells into tissues. Physiol. Rev. 81:31353–92 [Google Scholar]
  17. Bennett V, Lorenzo DN. 2013. Spectrin- and ankyrin-based membrane domains and the evolution of vertebrates. Curr. Top. Membr. 72:1–37 [Google Scholar]
  18. Berryman M, Bretscher A. 2000. Identification of a novel member of the chloride intracellular channel gene family (CLIC5) that associates with the actin cytoskeleton of placental microvilli. Mol. Biol. Cell 11:51509–21 [Google Scholar]
  19. Berryman M, Franck Z, Bretscher A. 1993. Ezrin is concentrated in the apical microvilli of a wide variety of epithelial cells whereas moesin is found primarily in endothelial cells. J. Cell Sci. 105:41025–43 [Google Scholar]
  20. Biemesderfer D, Mentone SA, Mooseker M, Hasson T. 2002. Expression of myosin VI within the early endocytic pathway in adult and developing proximal tubules. Am. J. Physiol. Renal Physiol. 282:5F785–94 [Google Scholar]
  21. Blazer-Yost BL, Vahle JC, Byars JM, Bacallao RL. 2004. Real-time three-dimensional imaging of lipid signal transduction: apical membrane insertion of epithelial Na+ channels. Am. J. Physiol. Cell Physiol. 287:6C1569–76 [Google Scholar]
  22. Bonilha VL, Finnemann SC, Rodriguez-Boulan E. 1999. Ezrin promotes morphogenesis of apical microvilli and basal infoldings in retinal pigment epithelium. J. Cell Biol. 147:71533–48 [Google Scholar]
  23. Bretscher A. 1983. Molecular architecture of the microvillus cytoskeleton. Ciba Found. Symp. 95:164–79 [Google Scholar]
  24. Bretscher A. 1989. Rapid phosphorylation and reorganization of ezrin and spectrin accompany morphological changes induced in A-431 cells by epidermal growth factor. J. Cell Biol. 108:3921–30 [Google Scholar]
  25. Bretscher A. 1991. Microfilament structure and function in the cortical cytoskeleton. Annu. Rev. Cell Biol. 7:337–74 [Google Scholar]
  26. Bretscher A, Chambers D, Nguyen R, Reczek D. 2000. ERM-Merlin and EBP50 protein families in plasma membrane organization and function. Annu. Rev. Cell Dev. Biol. 16:113–43 [Google Scholar]
  27. Bretscher A, Weber K. 1978. Purification of microvilli and an analysis of the protein components of the microfilament core bundle. Exp. Cell Res. 116:2397–407 [Google Scholar]
  28. Bretscher A, Weber K. 1979. Villin: the major microfilament-associated protein of the intestinal microvillus. PNAS 76:52321–25 [Google Scholar]
  29. Bretscher A, Weber K. 1980a. Fimbrin, a new microfilament-associated protein present in microvilli and other cell surface structures. J. Cell Biol. 86:1335–40 [Google Scholar]
  30. Bretscher A, Weber K. 1980b. Villin is a major protein of the microvillus cytoskeleton which binds both G and F actin in a calcium-dependent manner. Cell 20:3839–47 [Google Scholar]
  31. Brown KL, Birkenhead D, Lai JCY, Li L, Li R, Johnson P. 2005. Regulation of hyaluronan binding by F-actin and colocalization of CD44 and phosphorylated ezrin/radixin/moesin (ERM) proteins in myeloid cells. Exp. Cell Res. 303:2400–14 [Google Scholar]
  32. Brunet J-P, Cotte-Laffitte J, Linxe C, Quero A-M, Geniteau-Legendre M, Servin A. 2000. Rotavirus infection induces an increase in intracellular calcium concentration in human intestinal epithelial cells: role in microvillar actin alteration. J. Virol. 74:52323–32 [Google Scholar]
  33. Brunser O, Luft HJ. 1970. Fine structure of the apex of absorptive cell from rat small intestine. J. Ultrastruct. Res. 31:3291–311 [Google Scholar]
  34. Bryant DM, Roignot J, Datta A, Overeem AW, Kim M. et al. 2014. A molecular switch for the orientation of epithelial cell polarization. Dev. Cell 31:2171–87 [Google Scholar]
  35. Buss F, Arden SD, Lindsay M, Luzio JP, Kendrick-Jones J. 2001. Myosin VI isoform localized to clathrin-coated vesicles with a role in clathrin-mediated endocytosis. EMBO J. 20:143676–84 [Google Scholar]
  36. Canals D, Roddy P, Hannun YA. 2012. Protein phosphatase 1α mediates ceramide-induced ERM protein dephosphorylation: a novel mechanism independent of phosphatidylinositol 4, 5-biphosphate (PIP2) and myosin/ERM phosphatase. J. Biol. Chem. 287:1310145–55 [Google Scholar]
  37. Cao TT, Deacon HW, Reczek D, Bretscher A, von Zastrow M. 1999. A kinase-regulated PDZ-domain interaction controls endocytic sorting of the β2-adrenergic receptor. Nature 401:6750286–90 [Google Scholar]
  38. Carreno S, Kouranti I, Glusman ES, Fuller MT, Echard A, Payre F. 2008. Moesin and its activating kinase Slik are required for cortical stability and microtubule organization in mitotic cells. J. Cell Biol. 180:4739–46 [Google Scholar]
  39. Chen B, Li A, Wang D, Wang M, Zheng L, Bartles JR. 1999. Espin contains an additional actin-binding site in its N terminus and is a major actin-bundling protein of the Sertoli cell–spermatid ectoplasmic specialization junctional plaque. Mol. Biol. Cell 10:124327–39 [Google Scholar]
  40. Chen T, Hubbard A, Murtazina R, Price J, Yang J. et al. 2014. Myosin VI mediates the movement of NHE3 down the microvillus in intestinal epithelial cells. J. Cell Sci. 127:163535–45 [Google Scholar]
  41. Chen ZY, Hasson T, Zhang DS, Schwender BJ, Derfler BH. et al. 2001. Myosin-VIIb, a novel unconventional myosin, is a constituent of microvilli in transporting epithelia. Genomics 72:3285–96 [Google Scholar]
  42. Cheng H, Li J, Fazlieva R, Dai Z, Bu Z, Roder H. 2009. Autoinhibitory interactions between the PDZ2 and C-terminal domains in the scaffolding protein NHERF1. Structure 17:5660–69 [Google Scholar]
  43. Chishti AH, Kim AC, Marfatia SM, Lutchman M, Hanspal M. et al. 1998. The FERM domain: a unique module involved in the linkage of cytoplasmic proteins to the membrane. Trends Biochem. Sci. 23:8281–82 [Google Scholar]
  44. Chuang J-Z, Chou S-Y, Sung C-H. 2010. Chloride intracellular channel 4 is critical for the epithelial morphogenesis of RPE cells and retinal attachment. Mol. Biol. Cell 21:173017–28 [Google Scholar]
  45. Collins JH, Borysenko CW. 1984. The 110,000-dalton actin- and calmodulin-binding protein from intestinal brush border is a myosin-like ATPase. J. Biol. Chem. 259:2214128–35 [Google Scholar]
  46. Coluccio LM. 1991. Identification of the microvillar 110-kDa calmodulin complex (myosin-1) in kidney. Eur. J. Cell Biol. 56:2286–94 [Google Scholar]
  47. Coluccio LM. 1997. Myosin I. Am. J. Physiol. Cell Physiol. 273:2C347–59 [Google Scholar]
  48. Coluccio LM, Bretscher A. 1987. Calcium-regulated cooperative binding of the microvillar 110K-calmodulin complex to F-actin: formation of decorated filaments. J. Cell Biol. 105:1325–33 [Google Scholar]
  49. Coluccio LM, Bretscher A. 1988. Mapping of the microvillar 110K-calmodulin complex: calmodulin-associated or -free fragments of the 110-kD polypeptide bind F-actin and retain ATPase activity. J. Cell Biol. 106:2367–73 [Google Scholar]
  50. Coluccio LM, Bretscher A. 1989. Reassociation of microvillar core proteins: making a microvillar core in vitro. J. Cell Biol. 108:2495–502 [Google Scholar]
  51. Coluccio LM, Bretscher A. 1990. Mapping of the microvillar 110K-calmodulin complex (brush border myosin I). Identification of fragments containing the catalytic and F-actin–binding sites and demonstration of a calcium ion dependent conformational change. Biochemistry 29:5011089–94 [Google Scholar]
  52. Conzelman KA, Mooseker MS. 1987. The 110-kD protein-calmodulin complex of the intestinal microvillus is an actin-activated MgATPase. J. Cell Biol. 105:1313–24 [Google Scholar]
  53. Crawley SW, Shifrin DA, Grega-Larson NE, McConnell RE, Benesh AE. et al. 2014. Intestinal brush border assembly driven by protocadherin-based intermicrovillar adhesion. Cell 157:2433–46 [Google Scholar]
  54. Crepaldi T, Gautreau A, Comoglio PM, Louvard D, Arpin M. 1997. Ezrin is an effector of hepatocyte growth factor–mediated migration and morphogenesis in epithelial cells. J. Cell Biol. 138:2423–34 [Google Scholar]
  55. Croce A, Cassata G, Disanza A, Gagliani MC, Tacchetti C. et al. 2004. A novel actin barbed-end–capping activity in EPS-8 regulates apical morphogenesis in intestinal cells of Caenorhabditis elegans. Nat. Cell Biol. 6:121173–79 [Google Scholar]
  56. De Arruda MV, Watson S, Lin CS, Leavitt J, Matsudaira P. 1990. Fimbrin is a homologue of the cytoplasmic phosphoprotein plastin and has domains homologous with calmodulin and actin gelation proteins. J. Cell Biol. 111:31069–79 [Google Scholar]
  57. DeMarco SJ, Chicka MC, Strehler EE. 2002. Plasma membrane Ca2+ ATPase isoform 2b interacts preferentially with Na+/H+ exchanger regulatory factor 2 in apical plasma membranes. J. Biol. Chem. 277:1210506–11 [Google Scholar]
  58. Di Paolo G, De Camilli P. 2006. Phosphoinositides in cell regulation and membrane dynamics. Nature 443:7112651–57 [Google Scholar]
  59. Doi Y, Itoh M, Yonemura S, Ishihara S, Takano H. et al. 1999. Normal development of mice and unimpaired cell adhesion/cell motility/actin-based cytoskeleton without compensatory up-regulation of ezrin or radixin in moesin gene knockout. J. Biol. Chem. 274:42315–21 [Google Scholar]
  60. Donowitz M, Cha B, Zachos NC, Brett CL, Sharma A. et al. 2005. NHERF family and NHE3 regulation. J. Physiol. 567:13–11 [Google Scholar]
  61. Donowitz M, Singh S, Singh P, Chakraborty M, Chen Y. et al. 2011. Alterations in the proteome of the NHERF2 knockout mouse jejunal brush border membrane vesicles. Physiol. Genomics 43:11674–84 [Google Scholar]
  62. Ezzell RM, Chafel MM, Matsudaira PT. 1989. Differential localization of villin and fimbrin during development of the mouse visceral endoderm and intestinal epithelium. Development 106:2407–19 [Google Scholar]
  63. Ferrary E, Cohen-Tannoudji M, Pehau-Arnaudet G, Lapillonne A, Athman R. et al. 1999. In vivo, villin is required for Ca2+-dependent F-actin disruption in intestinal brush borders. J. Cell Biol. 146:4819–30 [Google Scholar]
  64. Fievet BT, Gautreau A, Roy C, Del Maestro L, Mangeat P. et al. 2004. Phosphoinositide binding and phosphorylation act sequentially in the activation mechanism of ezrin. J. Cell Biol. 164:5653–59 [Google Scholar]
  65. Finnerty CM, Chambers D, Ingraffea J, Faber HR, Karplus PA, Bretscher A. 2004. The EBP50-moesin interaction involves a binding site regulated by direct masking on the FERM domain. J. Cell Sci. 117:81547–52 [Google Scholar]
  66. Flock A, Bretscher A, Weber K. 1982. Immunohistochemical localization of several cytoskeletal proteins in inner ear sensory and supporting cells. Hear. Res. 7:175–89 [Google Scholar]
  67. Fouassier L, Nichols MT, Gidey E, McWilliams RR, Robin H. et al. 2005. Protein kinase C regulates the phosphorylation and oligomerization of ERM binding phosphoprotein 50. Exp. Cell Res. 306:1264–73 [Google Scholar]
  68. Funayama N, Nagafuchi A, Sato N, Tsukita S, Tsukita S. 1991. Radixin is a novel member of the band 4.1 family. J. Cell Biol. 115:41039–48 [Google Scholar]
  69. Gandy KAO, Canals D, Adada M, Wada M, Roddy P. et al. 2013. Sphingosine 1–phosphate induces filopodia formation through S1PR2 activation of ERM proteins. Biochem. J. 449:3661–72 [Google Scholar]
  70. Garbett D, Bretscher A. 2012. PDZ interactions regulate rapid turnover of the scaffolding protein EBP50 in microvilli. J. Cell Biol. 198:2195–203 [Google Scholar]
  71. Garbett D, Bretscher A. 2014. The surprising dynamics of scaffolding proteins. Mol. Biol. Cell 25:162315–19 [Google Scholar]
  72. Garbett D, LaLonde DP, Bretscher A. 2010. The scaffolding protein EBP50 regulates microvillar assembly in a phosphorylation-dependent manner. J. Cell Biol. 191:2397–413 [Google Scholar]
  73. Garbett D, Sauvanet C, Viswanatha R, Bretscher A. 2013. The tails of apical scaffolding proteins EBP50 and E3KARP regulate their localization and dynamics. Mol. Biol. Cell 24:213381–92 [Google Scholar]
  74. Gardet A, Breton M, Fontanges P, Trugnan G, Chwetzoff S. 2006. Rotavirus spike protein VP4 binds to and remodels actin bundles of the epithelial brush border into actin bodies. J. Virol. 80:83947–56 [Google Scholar]
  75. Gary R, Bretscher A. 1993. Heterotypic and homotypic associations between ezrin and moesin, two putative membrane-cytoskeletal linking proteins. PNAS 90:2210846–50 [Google Scholar]
  76. Gary R, Bretscher A. 1995. Ezrin self-association involves binding of an N-terminal domain to a normally masked C-terminal domain that includes the F-actin binding site. Mol. Biol. Cell 6:81061–75 [Google Scholar]
  77. George SP, Chen H, Conrad JC, Khurana S. 2013. Regulation of directional cell migration by membrane-induced actin bundling. J. Cell Sci. 126:1312–26 [Google Scholar]
  78. Georgescu M-MM, Morales FC, Molina JR, Hayashi Y. 2008. Roles of NHERF1/EBP50 in cancer. Curr. Mol. Med. 8:6459–68 [Google Scholar]
  79. Gisler SM, Stagljar I, Traebert M, Bacic D, Biber J, Murer H. 2001. Interaction of the type IIa Na/Pi cotransporter with PDZ proteins. J. Biol. Chem. 276:129206–13 [Google Scholar]
  80. Glenney JR Jr, Bretscher A, Weber K. 1980. Calcium control of the intestinal microvillus cytoskeleton: its implications for the regulation of microfilament organizations. PNAS 77:116458–62 [Google Scholar]
  81. Glenney JR Jr, Kaulfus P, Weber K. 1981. F actin assembly modulated by villin: Ca++-dependent nucleation and capping of the barbed end. Cell 24:2471–80 [Google Scholar]
  82. Glenney JR Jr, Weber K. 1981. Calcium control of microfilaments: uncoupling of the F-actin–severing and -bundling activity of villin by limited proteolysis in vitro. PNAS 78:52810–14 [Google Scholar]
  83. Gloerich M, ten Klooster JP, Vliem MJ, Koorman T, Zwartkruis FJ. et al. 2012. Rap2A links intestinal cell polarity to brush border formation. Nat. Cell Biol. 14:8793–801 [Google Scholar]
  84. Glowinski C, Liu R-HS, Chen X, Darabie A, Godt D. 2014. Myosin VIIA regulates microvillus morphogenesis and interacts with cadherin Cad99C in Drosophila oogenesis. J. Cell Sci. 127:224821–32 [Google Scholar]
  85. Gorelik J, Shevchuk AI, Frolenkov GI, Diakonov IA, Lab MJ. et al. 2003. Dynamic assembly of surface structures in living cells. PNAS 100:105819–22 [Google Scholar]
  86. Gould KL, Bretscher A, Esch FS, Hunter T. 1989. cDNA cloning and sequencing of the protein-tyrosine kinase substrate, ezrin, reveals homology to band 4.1. EMBO J. 8:134133–42 [Google Scholar]
  87. Grati M, Kachar B. 2011. Myosin VIIa and sans localization at stereocilia upper tip-link density implicates these Usher syndrome proteins in mechanotransduction. PNAS 108:2811476–81 [Google Scholar]
  88. Grimm-Günter E-MS, Revenu C, Ramos S, Hurbain I, Smyth N. et al. 2009. Plastin 1 binds to keratin and is required for terminal web assembly in the intestinal epithelium. Mol. Biol. Cell 20:102549–62 [Google Scholar]
  89. Guggino WB, Stanton BA. 2006. New insights into cystic fibrosis: molecular switches that regulate CFTR. Nat. Rev. Cell Biol. 7:6426–36 [Google Scholar]
  90. Halaihel N, Liévin V, Ball JM, Estes MK, Alvarado F, Vasseur M. 2000. Direct inhibitory effect of rotavirus NSP4(114-135) peptide on the Na+-d-glucose symporter of rabbit intestinal brush border membrane. J. Virol. 74:209464–70 [Google Scholar]
  91. Hall RA, Ostedgaard LS, Premont RT, Blitzer JT, Rahman N. et al. 1998a. A C-terminal motif found in the β2-adrenergic receptor, P2Y1 receptor and cystic fibrosis transmembrane conductance regulator determines binding to the Na+/H+ exchanger regulatory factor family of PDZ proteins. PNAS 95:158496–501 [Google Scholar]
  92. Hall RA, Premont RT, Chow CW, Blitzer JT, Pitcher JA. et al. 1998b. The β2-adrenergic receptor interacts with the Na+/H+-exchanger regulatory factor to control Na+/H+ exchange. Nature 392:6676626–30 [Google Scholar]
  93. Hamada K, Shimizu T, Matsui T, Tsukita S, Hakoshima T. 2000. Structural basis of the membrane-targeting and unmasking mechanisms of the radixin FERM domain. EMBO J. 19:174449–62 [Google Scholar]
  94. Hampton CM, Liu J, Taylor DW, DeRosier DJ, Taylor KA. 2008. The 3D structure of villin as an unusual F-actin crosslinker. Structure 16:121882–91 [Google Scholar]
  95. Hannun YA, Obeid LM. 2008. Principles of bioactive lipid signalling: lessons from sphingolipids. Nat. Rev. Mol. Cell Biol. 9:2139–50 [Google Scholar]
  96. Hanono A, Garbett D, Reczek D, Chambers DN, Bretscher A. 2006. EPI64 regulates microvillar subdomains and structure. J. Cell Biol. 175:5803–13 [Google Scholar]
  97. Hanzel D, Reggio H, Bretscher A, Forte JG, Mangeat P. 1991. The secretion-stimulated 80K phosphoprotein of parietal cells is ezrin, and has properties of a membrane cytoskeletal linker in the induced apical microvilli. EMBO J. 10:92363–73 Erratum. 1991 EMBO J. 10:123978–81 [Google Scholar]
  98. Hao JJ, Liu Y, Kruhlak M, Debell KE, Rellahan BL, Shaw S. 2009. Phospholipase C–mediated hydrolysis of PIP2 releases ERM proteins from lymphocyte membrane. J. Cell Biol. 184:3451–62 [Google Scholar]
  99. Hayden SM, Wolenski JS, Mooseker MS. 1990. Binding of brush border myosin I to phospholipid vesicles. J. Cell Biol. 111:2443–51 [Google Scholar]
  100. He J, Lau AG, Yaffe MB, Hall RA. 2001. Phosphorylation and cell cycle–dependent regulation of Na+/H+ exchanger regulatory factor-1 by Cdc2 kinase. J. Biol. Chem. 276:4541559–65 [Google Scholar]
  101. Hegan PS, Giral H, Levi M, Mooseker MS. 2012. Myosin VI is required for maintenance of brush border structure, composition, and membrane trafficking functions in the intestinal epithelial cell. Cytoskeleton 69:4235–51 [Google Scholar]
  102. Heintzelman MB, Hasson T, Mooseker MS. 1994. Multiple unconventional myosin domains of the intestinal brush border cytoskeleton. J. Cell Sci. 107:13535–43 [Google Scholar]
  103. Henn A, De La Cruz EM. 2005. Vertebrate myosin VIIb is a high duty ratio motor adapted for generating and maintaining tension. J. Biol. Chem. 280:4739665–76 [Google Scholar]
  104. Hernando N, Déliot N, Gisler SM, Lederer E, Weinman EJ. et al. 2002. PDZ-domain interactions and apical expression of type IIa Na/Pi cotransporters. PNAS 99:1811957–62 [Google Scholar]
  105. Hipfner DR, Keller N, Cohen SM. 2004. Slik Sterile-20 kinase regulates Moesin activity to promote epithelial integrity during tissue growth. Genes Dev. 18:182243–48 [Google Scholar]
  106. Hirata T, Nomachi A, Tohya K, Miyasaka M, Tsukita S. et al. 2012. Moesin-deficient mice reveal a non-redundant role for moesin in lymphocyte homeostasis. Int. Immunol. 24:11705–17 [Google Scholar]
  107. Howe CL, Keller TC 3rd, Mooseker MS, Wasserman RH. 1982. Analysis of cytoskeletal proteins and Ca2+-dependent regulation of structure in intestinal brush borders from rachitic chicks. PNAS 79:41134–38 [Google Scholar]
  108. Howe CL, Mooseker MS. 1983. Characterization of the 110-kdalton actin-calmodulin-, and membrane-binding protein from microvilli of intestinal epithelial cells. J. Cell Biol. 97:4974–85 [Google Scholar]
  109. Howe CL, Mooseker MS, Graves TA. 1980. Brush-border calmodulin. A major component of the isolated microvillus core. J. Cell Biol. 85:3916–23 [Google Scholar]
  110. Hsu YH, Lin WL, Hou YT, Pu YS, Shun CT. et al. 2010. Podocalyxin EBP50 ezrin molecular complex enhances the metastatic potential of renal cell carcinoma through recruiting Rac1 guanine nucleotide exchange factor ARHGEF7. Am. J. Pathol. 176:63050–61 [Google Scholar]
  111. Hughes SC, Fehon RG. 2006. Phosphorylation and activity of the tumor suppressor Merlin and the ERM protein Moesin are coordinately regulated by the Slik kinase. J. Cell Biol. 175:2305–13 [Google Scholar]
  112. Husson C, Renault L, Didry D, Pantaloni D, Carlier M-F. 2011. Cordon-Bleu uses WH2 domains as multifunctional dynamizers of actin filament assembly. Mol. Cell 43:3464–77 [Google Scholar]
  113. Ikenouchi J, Hirata M, Yonemura S, Umeda M. 2013. Sphingomyelin clustering is essential for the formation of microvilli. J. Cell Sci. 126:163585–92 [Google Scholar]
  114. Ikenouchi J, Suzuki M, Umeda K, Ikeda K, Taguchi R. et al. 2012. Lipid polarity is maintained in absence of tight junctions. J. Biol. Chem. 287:129525–33 [Google Scholar]
  115. Ikonen E, Simons K. 1998. Protein and lipid sorting from the trans-Golgi network to the plasma membrane in polarized cells. Semin. Cell Dev. Biol. 9:5503–9 [Google Scholar]
  116. Ingraffea J, Reczek D, Bretscher A. 2002. Distinct cell type–specific expression of scaffolding proteins EBP50 and E3KARP: EBP50 is generally expressed with ezrin in specific epithelia, whereas E3KARP is not. Eur. J. Cell Biol. 81:261–68 [Google Scholar]
  117. Ito S. 1969. Structure and function of the glycocalyx. Fed. Proc. 28:112–25 [Google Scholar]
  118. Jayaraman B, Nicholson LK. 2007. Thermodynamic dissection of the Ezrin FERM/CERMAD interface. Biochemistry 46:4312174–89 [Google Scholar]
  119. Jontes JD, Milligan RA, Pollard TD, Ostap EM. 1997. Kinetic characterization of brush border myosin-I ATPase. PNAS 94:2614332–37 [Google Scholar]
  120. Jourdan N, Brunet JP, Sapin C, Blais A, Cotte-Laffitte J. et al. 1998. Rotavirus infection reduces sucrase-isomaltase expression in human intestinal epithelial cells by perturbing protein targeting and organization of microvillar cytoskeleton. J. Virol. 72:97228–36 [Google Scholar]
  121. Karagiosis SA, Ready DF. 2004. Moesin contributes an essential structural role in Drosophila photoreceptor morphogenesis. Development 131:4725–32 [Google Scholar]
  122. Kesimer M, Ehre C, Burns KA, Davis CW, Sheehan JK, Pickles RJ. 2013. Molecular organization of the mucins and glycocalyx underlying mucus transport over mucosal surfaces of the airways. Mucosal Immunol. 6:2379–92 [Google Scholar]
  123. Khurana S, George SP. 2008. Regulation of cell structure and function by actin-binding proteins: villin's perspective. FEBS Lett. 582:142128–39 [Google Scholar]
  124. Kikuchi S, Hata M, Fukumoto K, Yamane Y, Matsui T. et al. 2002. Radixin deficiency causes conjugated hyperbilirubinemia with loss of Mrp2 from bile canalicular membranes. Nat. Genet. 31:3320–25 [Google Scholar]
  125. Kitajiri S, Fukumoto K, Hata M, Sasaki H, Katsuno T. et al. 2004. Radixin deficiency causes deafness associated with progressive degeneration of cochlear stereocilia. J. Cell Biol. 166:4559–70 [Google Scholar]
  126. Knowles BC, Roland JT, Krishnan M, Tyska MJ, Lapierre LA. et al. 2014. Myosin Vb uncoupling from RAB8A and RAB11A elicits microvillus inclusion disease. J. Clin. Investig. 124:72947–62 [Google Scholar]
  127. Kocher O, Birrane G, Tsukamoto K, Fenske S, Yesilaltay A. et al. 2010. In vitro and in vivo analysis of the binding of the C terminus of the HDL receptor scavenger receptor class B, type I (SR-BI), to the PDZ1 domain of its adaptor protein PDZK1. J. Biol. Chem. 285:4534999–10 [Google Scholar]
  128. Kocher O, Birrane G, Yesilaltay A, Shechter S, Pal R. et al. 2011. Identification of the PDZ3 domain of the adaptor protein PDZK1 as a second, physiologically functional binding site for the C terminus of the high density lipoprotein receptor scavenger receptor class B type I. J. Biol. Chem. 286:2825171–86 [Google Scholar]
  129. Kocher O, Comella N, Gilchrist A, Pal R, Tognazzi K. et al. 1999. PDZK1, a novel PDZ domain–containing protein up-regulated in carcinomas and mapped to chromosome 1q21, interacts with cMOAT (MRP2), the multidrug resistance-associated protein. Lab. Investig. 79:91161–70 [Google Scholar]
  130. Kocher O, Comella N, Tognazzi K, Brown LF. 1998. Identification and partial characterization of PDZK1: a novel protein containing PDZ interaction domains. Lab. Investig. 78:1117–25 [Google Scholar]
  131. Kocher O, Pal R, Roberts M, Cirovic C, Gilchrist A. 2003a. Targeted disruption of the PDZK1 gene by homologous recombination. Mol. Cell Biol. 23:41175–80 [Google Scholar]
  132. Kocher O, Yesilaltay A, Cirovic C, Pal R, Rigotti A, Krieger M. 2003b. Targeted disruption of the PDZK1 gene in mice causes tissue-specific depletion of the high density lipoprotein receptor scavenger receptor class B type I and altered lipoprotein metabolism. J. Biol. Chem. 278:5252820–25 [Google Scholar]
  133. Kravtsov DV, Caputo C, Collaco A, Hoekstra N, Egan ME. et al. 2012. Myosin Ia is required for CFTR brush border membrane trafficking and ion transport in the mouse small intestine. Traffic 13:81072–82 [Google Scholar]
  134. Krizek J, Coluccio LM, Bretscher A. 1987. ATPase activity of the microvillar 110 kDa polypeptide-calmodulin complex is activated in Mg2+ and inhibited in K+-EDTA by F-actin. FEBS Lett. 225:1–2269–72 [Google Scholar]
  135. Kunda P, Pelling AE, Liu T, Baum B. 2008. Moesin controls cortical rigidity, cell rounding, and spindle morphogenesis during mitosis. Curr. Biol. 18:291–101 [Google Scholar]
  136. LaLonde DP, Bretscher A. 2009. The scaffold protein PDZK1 undergoes a head-to-tail intramolecular association that negatively regulates its interaction with EBP50. Biochemistry 48:102261–71 [Google Scholar]
  137. LaLonde DP, Garbett D, Bretscher A. 2010. A regulated complex of the scaffolding proteins PDZK1 and EBP50 with ezrin contribute to microvillar organization. Mol. Biol. Cell 21:91519–29 [Google Scholar]
  138. Li J, Callaway DJ, Bu Z. 2009. Ezrin induces long-range interdomain allostery in the scaffolding protein NHERF1. J. Mol. Biol. 392:1166–80 [Google Scholar]
  139. Li JG, Chen C, Liu-Chen LY. 2002. Ezrin-radixin-moesin–binding phosphoprotein-50/Na+/H+ exchanger regulatory factor (EBP50/NHERF) blocks U50,488H-induced down-regulation of the human κ opioid receptor by enhancing its recycling rate. J. Biol. Chem. 277:3027545–52 [Google Scholar]
  140. Li Q, Nance MR, Kulikauskas R, Nyberg K, Fehon R. et al. 2007. Self-masking in an intact ERM-merlin protein: an active role for the central α-helical domain. J. Mol. Biol. 365:51446–59 [Google Scholar]
  141. Linden SK, Sutton P, Karlsson NG, Korolik V, McGuckin MA. 2008. Mucins in the mucosal barrier to infection. Mucosal Immunol. 1:3183–97 [Google Scholar]
  142. Lohi H, Lamprecht G, Markovich D, Heil A, Kujala M. et al. 2003. Isoforms of SLC26A6 mediate anion transport and have functional PDZ interaction domains. Am. J. Physiol. Cell Physiol. 284:3C769–79 [Google Scholar]
  143. Loomis PA, Kelly AE, Zheng L, Changyaleket B, Sekerková G. et al. 2006. Targeted wild-type and jerker espins reveal a novel, WH2-domain–dependent way to make actin bundles in cells. J. Cell Sci. 119:81655–65 [Google Scholar]
  144. Loomis PA, Zheng L, Sekerková 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. 163:51045–55 [Google Scholar]
  145. Mahon MJ, Donowitz M, Yun CC, Segre G V. 2002. Na+/H+ exchanger regulatory factor 2 directs parathyroid hormone 1 receptor signalling. Nature 417:6891858–61 [Google Scholar]
  146. Malmberg EK, Pelaseyed T, Petersson AC, Seidler UE, De Jonge H. et al. 2008. The C-terminus of the transmembrane mucin MUC17 binds to the scaffold protein PDZK1 that stably localizes it to the enterocyte apical membrane in the small intestine. Biochem. J. 410:2283–89 [Google Scholar]
  147. Matsudaira P, Mandelkow E, Renner W, Hesterberg LK, Weber K. 1983. Role of fimbrin and villin in determining the interfilament distances of actin bundles. Nature 301:5897209–14 [Google Scholar]
  148. Matsudaira PT, Burgess DR. 1979. Identification and organization of the components in the isolated microvillus cytoskeleton. J. Cell Biol. 83:3667–73 [Google Scholar]
  149. Maudsley S, Zamah AM, Rahman N, Blitzer JT, Luttrell LM. et al. 2000. Platelet-derived growth factor receptor association with Na+/H+ exchanger regulatory factor potentiates receptor activity. Mol. Cell. Biol. 20:228352–63 [Google Scholar]
  150. Mazerik JN, Kraft LJ, Kenworthy AK, Tyska MJ. 2014. Motor and tail homology 1 (Th1) domains antagonistically control myosin-1 dynamics. Biophys. J. 106:3649–58 [Google Scholar]
  151. Mazerik JN, Tyska MJ. 2012. Myosin-1A targets to microvilli using multiple membrane binding motifs in the tail homology 1 (TH1) domain. J. Biol. Chem. 287:1613104–15 [Google Scholar]
  152. McConnell RE, Benesh AE, Mao S, Tabb DL, Tyska MJ. 2011. Proteomic analysis of the enterocyte brush border. Am. J. Physiol. Gastrointest. Liver Physiol. 300:5G914–26 [Google Scholar]
  153. McConnell RE, Higginbotham JN, Shifrin DA, Tabb DL, Coffey RJ, Tyska MJ. 2009. The enterocyte microvillus is a vesicle-generating organelle. J. Cell Biol. 185:71285–98 [Google Scholar]
  154. McConnell RE, Tyska MJ. 2007. Myosin-1a powers the sliding of apical membrane along microvillar actin bundles. J. Cell Biol. 177:4671–81 [Google Scholar]
  155. McConnell RE, Tyska MJ. 2010. Leveraging the membrane-cytoskeleton interface with myosin-1. Trends Cell Biol. 20:7418–26 [Google Scholar]
  156. McMahon HT, Boucrot E. 2011. Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 12:8517–33 [Google Scholar]
  157. Mishra R, Grzybek M, Niki T, Hirashima M, Simons K. 2010. Galectin-9 trafficking regulates apical-basal polarity in Madin-Darby canine kidney epithelial cells. PNAS 107:4117633–38 [Google Scholar]
  158. Mooseker MS. 1985. Organization, chemistry, and assembly of the cytoskeletal apparatus of the intestinal brush border. Annu. Rev. Cell Biol. 1:209–41 [Google Scholar]
  159. Mooseker MS, Tilney LG. 1975. Organization of an actin filament–membrane complex. Filament polarity and membrane attachment in the microvilli of intestinal epithelial cells. J. Cell Biol. 67:3725–43 [Google Scholar]
  160. Morales FC, Takahashi Y, Kreimann EL, Georgescu MM. 2004. Ezrin-radixin-moesin (ERM)-binding phosphoprotein 50 organizes ERM proteins at the apical membrane of polarized epithelia. PNAS 101:5117705–10 [Google Scholar]
  161. Mori T, Kitano K, Terawaki S, Maesaki R, Fukami Y, Hakoshima T. 2008. Structural basis for CD44 recognition by ERM proteins. J. Biol. Chem. 283:4329602–12 [Google Scholar]
  162. Müller T, Hess MW, Schiefermeier N, Pfaller K, Ebner HL. et al. 2008. MYO5B mutations cause microvillus inclusion disease and disrupt epithelial cell polarity. Nat. Genet. 40:101163–65 [Google Scholar]
  163. Murthy A, Gonzalez-Agosti C, Cordero E, Pinney D, Candia C. et al. 1998. NHE-RF, a regulatory cofactor for Na+-H+ exchange, is a common interactor for merlin and ERM (MERM) proteins. J. Biol. Chem. 273:31273–76 [Google Scholar]
  164. Nakamura F, Amieva MR, Furthmayr H. 1995. Phosphorylation of threonine 558 in the carboxyl-terminal actin-binding domain of moesin by thrombin activation of human platelets. J. Biol. Chem. 270:5231377–85 [Google Scholar]
  165. Nakamura T, Shibata N, Nishimoto-Shibata T, Feng D, Ikemoto M. et al. 2005. Regulation of SR-BI protein levels by phosphorylation of its associated protein, PDZK1. PNAS 102:3813404–9 [Google Scholar]
  166. Offenhäuser N, Borgonovo A, Disanza A, Romano P, Ponzanelli I. et al. 2004. The eps8 family of proteins links growth factor stimulation to actin reorganization generating functional redundancy in the Ras/Rac pathway. Mol. Biol. Cell 15:191–98 [Google Scholar]
  167. Pearson MA, Reczek D, Bretscher A, Karplus PA. 2000. Structure of the ERM protein moesin reveals the FERM domain fold masked by an extended actin binding tail domain. Cell 101:3259–70 [Google Scholar]
  168. Pelaseyed T, Bergström JH, Gustafsson JK, Ermund A, Birchenough GMH. et al. 2014. The mucus and mucins of the goblet cells and enterocytes provide the first defense line of the gastrointestinal tract and interact with the immune system. Immunol. Rev. 260:18–20 [Google Scholar]
  169. Pelaseyed T, Gustafsson JK, Gustafsson IJ, Ermund A, Hansson GC. 2013a. Carbachol-induced MUC17 endocytosis is concomitant with NHE3 internalization and CFTR membrane recruitment in enterocytes. Am. J. Physiol. Cell Physiol. 305:4C457–67 [Google Scholar]
  170. Pelaseyed T, Hansson GC. 2011. CFTR anion channel modulates expression of human transmembrane mucin MUC3 through the PDZ protein GOPC. J. Cell Sci. 124:183074–83 [Google Scholar]
  171. Pelaseyed T, Zäch M, Petersson ÅC, Svensson F, Johansson DGA, Hansson GC. 2013b. Unfolding dynamics of the mucin SEA domain probed by force spectroscopy suggest that it acts as a cell-protective device. FEBS J. 280:61491–501 [Google Scholar]
  172. Raghuram V, Hormuth H, Foskett JK. 2003. A kinase-regulated mechanism controls CFTR channel gating by disrupting bivalent PDZ domain interactions. PNAS 100:169620–25 [Google Scholar]
  173. Rambourg A, Neutra M, Leblond CP. 1966. Presence of a “cell coat” rich in carbohydrate at the surface of cells in the rat. Anat. Rec. 154:141–71 [Google Scholar]
  174. Ramig RF. 2004. Pathogenesis of intestinal and systemic rotavirus infection. J. Virol. 78:1910213–20 [Google Scholar]
  175. Reczek D, Berryman M, Bretscher A. 1997. Identification of EBP50: a PDZ-containing phosphoprotein that associates with members of the ezrin-radixin-moesin family. J. Cell Biol. 139:1169–79 [Google Scholar]
  176. Reczek D, Bretscher A. 1998. The carboxyl-terminal region of EBP50 binds to a site in the amino-terminal domain of ezrin that is masked in the dormant molecule. J. Biol. Chem. 273:2918452–58 [Google Scholar]
  177. Reczek D, Bretscher A. 2001. Identification of EPI64, a TBC/rabGAP domain–containing microvillar protein that binds to the first PDZ domain of EBP50 and E3KARP. J. Cell Biol. 153:1191–206 [Google Scholar]
  178. Revenu C, Ubelmann F, Hurbain I, El-Marjou F, Dingli F. et al. 2012. A new role for the architecture of microvillar actin bundles in apical retention of membrane proteins. Mol. Biol. Cell 23:2324–36 [Google Scholar]
  179. Roland JT, Bryant DM, Datta A, Itzen A, Mostov KE, Goldenring JR. 2011. Rab GTPase-Myo5B complexes control membrane recycling and epithelial polarization. PNAS 108:72789–94 [Google Scholar]
  180. Rollason R, Korolchuk V, Hamilton C, Jepson M, Banting G. 2009. A CD317/tetherin–RICH2 complex plays a critical role in the organization of the subapical actin cytoskeleton in polarized epithelial cells. J. Cell Biol. 184:5721–36 [Google Scholar]
  181. Rossmann H, Jacob P, Baisch S, Hassoun R, Meier J. et al. 2005. The CFTR associated protein CAP70 interacts with the apical Cl/HCO3 exchanger DRA in rabbit small intestinal mucosa. Biochemistry 44:114477–87 [Google Scholar]
  182. Ruemmele FM, Schmitz J, Goulet O. 2006. Microvillous inclusion disease (microvillous atrophy). Orphanet J. Rare Dis. 1:122 [Google Scholar]
  183. Rzadzinska AK, Schneider ME, Davies C, Riordan GP, Kachar B. 2004. An actin molecular treadmill and myosins maintain stereocilia functional architecture and self-renewal. J. Cell Biol. 164:6887–97 [Google Scholar]
  184. Salles FT, Andrade LR, Tanda S, Grati M, Plona KL. et al. 2014. CLIC5 stabilizes membrane-actin filament linkages at the base of hair cell stereocilia in a molecular complex with radixin, taperin, and myosin VI. Cytoskeleton 71:161–78 [Google Scholar]
  185. Saotome I, Curto M, McClatchey AI. 2004. Ezrin is essential for epithelial organization and villus morphogenesis in the developing intestine. Dev. Cell 6:6855–64 [Google Scholar]
  186. Sato N, Funayama N, Nagafuchi A, Yonemura S, Tsukita S, Tsukita S. 1992. A gene family consisting of ezrin, radixin and moesin. Its specific localization at actin filament/plasma membrane association sites. J. Cell Sci. 103:1131–43 [Google Scholar]
  187. Sato T, Mushiake S, Kato Y, Sato K, Sato M. et al. 2007. The Rab8 GTPase regulates apical protein localization in intestinal cells. Nature 448:7151366–69 [Google Scholar]
  188. Schuck S, Simons K. 2004. Polarized sorting in epithelial cells: raft clustering and the biogenesis of the apical membrane. J. Cell Sci. 117:255955–64 [Google Scholar]
  189. Sekerková G, Zheng L, Loomis PA, Mugnaini E, Bartles JR. 2006. Espins and the actin cytoskeleton of hair cell stereocilia and sensory cell microvilli. Cell. Mol. Life Sci. 63:19–202329–41 [Google Scholar]
  190. Shenolikar S, Voltz JW, Minkoff CM, Wade JB, Weinman EJ. 2002. Targeted disruption of the mouse NHERF-1 gene promotes internalization of proximal tubule sodium-phosphate cotransporter type IIa and renal phosphate wasting. PNAS 99:1711470–75 [Google Scholar]
  191. Shenolikar S, Weinman EJ. 2001. NHERF: targeting and trafficking membrane proteins. Am. J. Physiol. Renal Physiol. 280:3F389–95 [Google Scholar]
  192. Sher I, Hanemann CO, Karplus PA, Bretscher A. 2012. The tumor suppressor merlin controls growth in its open state, and phosphorylation converts it to a less-active more-closed state. Dev. Cell 22:4703–5 [Google Scholar]
  193. Shibata T, Chuma M, Kokubu A, Sakamoto M, Hirohashi S. 2003. EBP50, a β-catenin-associating protein, enhances Wnt signaling and is over-expressed in hepatocellular carcinoma. Hepatology 38:1178–86 [Google Scholar]
  194. Short DB, Trotter KW, Reczek D, Kreda SM, Bretscher A. et al. 1998. An apical PDZ protein anchors the cystic fibrosis transmembrane conductance regulator to the cytoskeleton. J. Biol. Chem. 273:3119797–801 [Google Scholar]
  195. Simons K, Van Meer G. 1988. Lipid sorting in epithelial cells. Biochemistry 27:176197–202 [Google Scholar]
  196. Sjöström B, Anniko M. 1992. Cochlear structure and function in a recessive type of genetically induced inner ear degeneration. ORL J. Otorhinolaryngol. Relat. Spec. 54:4220–28 [Google Scholar]
  197. Spence HJ, Chen YJ, Batchelor CL, Higginson JR, Suila H. et al. 2004. Ezrin-dependent regulation of the actin cytoskeleton by β-dystroglycan. Hum. Mol. Genet. 13:151657–68 [Google Scholar]
  198. Stidwill RP, Wysolmerski T, Burgess DR. 1984. The brush border cytoskeleton is not static: in vivo turnover of proteins. J. Cell Biol. 98:2641–45 [Google Scholar]
  199. Sun F, Hug MJ, Lewarchik CM, Yun C-HC, Bradbury NA, Frizzell RA. 2000. E3KARP mediates the association of ezrin and protein kinase A with the cystic fibrosis transmembrane conductance regulator in airway cells. J. Biol. Chem. 275:3829539–46 [Google Scholar]
  200. Takeuchi K, Sato N, Kasahara H, Funayama N, Nagafuchi A. et al. 1994. Perturbation of cell adhesion and microvilli formation by antisense oligonucleotides to ERM family members. J. Cell Biol. 125:61371–84 [Google Scholar]
  201. Tamura A, Kikuchi S, Hata M, Katsuno T, Matsui T. et al. 2005. Achlorhydria by ezrin knockdown: defects in the formation/expansion of apical canaliculi in gastric parietal cells. J. Cell Biol. 169:121–28 [Google Scholar]
  202. Ten Klooster JP, Jansen M, Yuan J, Oorschot V, Begthel H. et al. 2009. Mst4 and Ezrin induce brush borders downstream of the Lkb1/Strad/Mo25 polarization complex. Dev. Cell 16:4551–62 [Google Scholar]
  203. Terawaki S, Maesaki R, Hakoshima T. 2006. Structural basis for NHERF recognition by ERM proteins. Structure 14:4777–89 [Google Scholar]
  204. Thelin WR, Hodson CA, Milgram SL. 2005. Beyond the brush border: NHERF4 blazes new NHERF turf. J. Physiol. 567:113–19 [Google Scholar]
  205. Thoeni CE, Vogel GF, Tancevski I, Geley S, Lechner S. et al. 2014. Microvillus inclusion disease: loss of myosin Vb disrupts intracellular traffic and cell polarity. Traffic 15:122–42 [Google Scholar]
  206. Tilney LG. 1970. Factors controlling the reassembly of the microvillous border of the small intestine of the salamander. J. Cell Biol. 47:2408–22 [Google Scholar]
  207. Tilney LG, Derosier DJ, Mulroy MJ. 1980. The organization of actin filaments in the stereocilia of cochlear hair cells. J. Cell Biol. 86:1244–59 [Google Scholar]
  208. Tilney LG, Egelman EH, DeRosier DJ, Saunder JC. 1983. Actin filaments, stereocilia, and hair cells of the bird cochlea. II. Packing of actin filaments in the stereocilia and in the cuticular plate and what happens to the organization when the stereocilia are bent. J. Cell Biol. 96:3822–34 [Google Scholar]
  209. Tilney LG, Tilney MS, DeRosier DJ. 1992. Actin filaments, stereocilia, and hair cells: how cells count and measure. Annu. Rev. Cell Biol. 8:257–74 [Google Scholar]
  210. Tocchetti A, Soppo CBE, Zani F, Bianchi F, Gagliani MC. et al. 2010. Loss of the actin remodeler Eps8 causes intestinal defects and improved metabolic status in mice. PLOS ONE 5:3e9468 [Google Scholar]
  211. Tsukita S, Oishi K, Sato N, Sagara J, Kawai A. 1994. ERM family members as molecular linkers between the cell surface glycoprotein CD44 and actin-based cytoskeletons. J. Cell Biol. 126:2391–401 [Google Scholar]
  212. Turunen O, Wahlstrom T, Vaheri A. 1994. Ezrin has a COOH-terminal actin-binding site that is conserved in the ezrin protein family. J. Cell Biol. 126:61445–53 [Google Scholar]
  213. Tyska MJ, Mackey AT, Huang J-D, Copeland NG, Jenkins NA, Mooseker MS. 2005. Myosin-1a is critical for normal brush border structure and composition. Mol. Biol. Cell 16:52443–57 [Google Scholar]
  214. Tyska MJ, Mooseker MS. 2002. MYO1A (brush border myosin I) dynamics in the brush border of LLC-PK1-CL4 cells. Biophys. J. 82:41869–83 [Google Scholar]
  215. Ubelmann F, Chamaillard M, El-Marjou F, Simon A, Netter J. et al. 2013. Enterocyte loss of polarity and gut wound healing rely upon the F-actin–severing function of villin. PNAS 110:15E1380–89 [Google Scholar]
  216. Umeki N, Jung HS, Watanabe S, Sakai T, Li X. et al. 2009. The tail binds to the head-neck domain, inhibiting ATPase activity of myosin VIIA. PNAS 106:218483–88 [Google Scholar]
  217. Van den Bogaart G, Meyenberg K, Risselada HJ, Amin H, Willig KI. et al. 2011. Membrane protein sequestering by ionic protein-lipid interactions. Nature 479:7374552–55 [Google Scholar]
  218. Van der Post S, Hansson GC. 2014. Membrane protein profiling of human colon reveals distinct regional differences. Mol. Cell. Proteomics 13:92277–87 [Google Scholar]
  219. Viswanatha R, Ohouo PY, Smolka MB, Bretscher A. 2012. Local phosphocycling mediated by LOK/SLK restricts ezrin function to the apical aspect of epithelial cells. J. Cell Biol. 199:6969–84 [Google Scholar]
  220. Viswanatha R, Wayt J, Ohouo PY, Smolka MB, Bretscher A. 2013. Interactome analysis reveals ezrin can adopt multiple conformational states. J. Biol. Chem. 288:4935437–51 [Google Scholar]
  221. Volkmann N, DeRosier D, Matsudaira P, Hanein D. 2001. An atomic model of actin filaments cross-linked by fimbrin and its implications for bundle assembly and function. J. Cell Biol. 153:5947–56 [Google Scholar]
  222. Waharte F, Brown CM, Coscoy S, Coudrier E, Amblard F. 2005. A two-photon FRAP analysis of the cytoskeleton dynamics in the microvilli of intestinal cells. Biophys. J. 88:21467–78 [Google Scholar]
  223. Wang B, Ardura JA, Romero G, Yang Y, Hall RA, Friedman PA. 2010. Na/H exchanger regulatory factors control parathyroid hormone receptor signaling by facilitating differential activation of Gα protein subunits. J. Biol. Chem. 285:3526976–86 [Google Scholar]
  224. Wayt J, Bretscher A. 2014. Cordon Bleu serves as a platform at the basal region of microvilli where it regulates microvillar length through its WH2 domains. Mol. Biol. Cell 25:182817–27 [Google Scholar]
  225. Wegner B, Al-Momany A, Kulak SC, Kozlowski K, Obeidat M. et al. 2010. CLIC5A, a component of the ezrin-podocalyxin complex in glomeruli, is a determinant of podocyte integrity. Am. J. Physiol. Renal Physiol. 298:6F1492–503 [Google Scholar]
  226. Weinman EJ, Steplock D, Wang Y, Shenolikar S. 1995. Characterization of a protein cofactor that mediates protein kinase A regulation of the renal brush border membrane Na+-H+ exchanger. J. Clin. Investig. 95:52143–49 [Google Scholar]
  227. Wells AL, Lin AW, Chen LQ, Safer D, Cain SM. et al. 1999. Myosin VI is an actin-based motor that moves backwards. Nature 401:6752505–8 [Google Scholar]
  228. Wheeler DS, Barrick SR, Grubisha MJ, Brufsky AM, Friedman PA, Romero G. 2011. Direct interaction between NHERF1 and Frizzled regulates β-catenin signaling. Oncogene 30:132–42 [Google Scholar]
  229. Wolfrum U, Liu X, Schmitt A, Udovichenko IP, Williams DS. 1998. Myosin VIIa as a common component of cilia and microvilli. Cell Motil. Cytoskeleton 40:3261–71 [Google Scholar]
  230. Yang Y, Baboolal TG, Siththanandan V, Chen M, Walker ML. et al. 2009. A FERM domain autoregulates Drosophila myosin 7a activity. PNAS 106:114189–94 [Google Scholar]
  231. Yeung T, Ozdamar B, Paroutis P, Grinstein S. 2006. Lipid metabolism and dynamics during phagocytosis. Curr. Opin. Cell Biol. 18:4429–37 [Google Scholar]
  232. Yu CY, Chen JY, Lin YY, Shen KF, Lin WL. et al. 2007. A bipartite signal regulates the faithful delivery of apical domain marker podocalyxin/Gp135. Mol. Biol. Cell 18:51710–22 [Google Scholar]
  233. Yu FX, Guan KL. 2013. The Hippo pathway: regulators and regulations. Genes Dev. 27:4355–71 [Google Scholar]
  234. Yun CH, Lamprecht G, Forster D V, Sidor A. 1998. NHE3 kinase A regulatory protein E3KARP binds the epithelial brush border Na+/H+ exchanger NHE3 and the cytoskeletal protein ezrin. J. Biol. Chem. 273:4025856–63 [Google Scholar]
  235. Yun CH, Oh S, Zizak M, Steplock D, Tsao S. et al. 1997. cAMP-mediated inhibition of the epithelial brush border Na+/H+ exchanger, NHE3, requires an associated regulatory protein. PNAS 94:73010–15 Erratum. 1997 PNAS 94:1810006 [Google Scholar]
  236. Zeidan YH, Jenkins RW, Hannun YA. 2008. Remodeling of cellular cytoskeleton by the acid sphingomyelinase/ceramide pathway. J. Cell Biol. 181:2335–50 [Google Scholar]
  237. Zhang D-S, Piazza V, Perrin BJ, Rzadzinska AK, Poczatek JC. et al. 2012. Multi-isotope imaging mass spectrometry reveals slow protein turnover in hair-cell stereocilia. Nature 481:7382520–24 [Google Scholar]
  238. Zheng L, Sekerková 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 102:3377–85 [Google Scholar]
  239. Zwaenepoel I, Naba A, Da Cunha MML, Del Maestro L, Formstecher E. et al. 2012. Ezrin regulates microvillus morphogenesis by promoting distinct activities of Eps8 proteins. Mol. Biol. Cell 23:61080–94 [Google Scholar]
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