Dynamic actin remodeling during epithelial-mesenchymal transition depends on increased moesin expression

Molecular Biology of the Cell

Volumn 22, Issue 24, 2011, Pages 4750-4764

  Haynes, Jennifer ^a   Srivastava, Jyoti ^a   Madson, Nikki ^a   Wittmann, Torsten ^a   Barber, Diane L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ALPHA SMOOTH MUSCLE ACTIN; BETA ACTIN; EZRIN; FOCAL ADHESION KINASE; GREEN FLUORESCENT PROTEIN; HERMES ANTIGEN; MOESIN; MYOSIN LIGHT CHAIN; NERVE CELL ADHESION MOLECULE; PHALLOIDIN; RADIXIN; SHORT HAIRPIN RNA; TRANSFORMING GROWTH FACTOR BETA; UVOMORULIN;

ACTIN FILAMENT; AGED; ANIMAL CELL; ARTICLE; ATTENUATION; AUTOPHOSPHORYLATION; BREAST EPITHELIUM; CELL ADHESION; CELL ELONGATION; CELL INVASION; CELL MIGRATION; CELL STRUCTURE; CELL TRANSDIFFERENTIATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; CYTOSKELETON; ELECTROKYMOGRAPHY; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; MOLECULAR IMAGING; MOLECULAR MODEL; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; WOUND HEALING;

ACTIN CYTOSKELETON; ACTINS; ANIMALS; ANTIGENS, CD44; CELL LINE; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; FOCAL ADHESION PROTEIN-TYROSINE KINASES; GENE EXPRESSION REGULATION; HUMANS; MICE; MICROFILAMENT PROTEINS; MYOSIN LIGHT CHAINS; PHOSPHORYLATION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84055176150     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-02-0119     Document Type: Article

References (53)

1. Bakin AV, Tomlinson AK, Bhowmick NA, Moses HL, Arteaga CL (2000). Phosphatidylinositol 3-kinase function is required for transforming growth factor beta-mediated epithelial to mesenchymal transition and cell migration. J Biol Chem 275, 36803-36810. (Pubitemid 32002090)
2. Bhowmick NA, Ghiassi M, Bakin A, Aakre M, Lundquist CA, Engel ME, Arteaga CL, Moses HL (2001). Transforming growth factor-beta1 mediates epithelial to mesenchymal transdifferentiation through a RhoA-dependent mechanism. Mol Biol Cell 12, 27-36. (Pubitemid 32060576)
3. Brown KA, Aakre ME, Gorska AE, Price JO, Eltom SE, Pietenpol JA, Moses HL (2004). Induction by transforming growth factor-beta1 of epithelial to mesenchymal transition is a rare event in vitro. Breast Cancer Res 6, R215-R231.
4. Buckley ST, Medina C, Kasper M, Ehrhardt C (2011). Interplay between RAGE, CD44, and focal adhesion molecules in epithelial-mesenchymal transition of alveolar epithelial cells. Am J Physiol Lung Cell Mol Physiol 300, L548-L559.
5. Cho HJ, Yoo J (2007). Rho activation is required for transforming growth factor-beta-induced epithelial-mesenchymal transition in lens epithelial cells. Cell Biol Int 31, 1225-1230. (Pubitemid 47030990)
6. Doi Y, Itoh M, Yonemura S, Ishihara S, Takano H, Noda T, Tsukita S (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, 2315-2321.
7. Edlund S, Landstrom M, Heldin CH, Aspenstrom P (2002). Transforming growth factor-beta-induced mobilization of actin cytoskeleton requires signaling by small GTPases Cdc42 and RhoA. Mol Biol Cell 13, 902-914. (Pubitemid 34250354)
8. Estecha A, Sanchez-Martin L, Puig-Kroger A, Bartolome RA, Teixido J, Samaniego R, Sanchez-Mateos P (2009). Moesin orchestrates cortical polarity of melanoma tumour cells to initiate 3D invasion. J Cell Sci 122, 3492-3501.
9. Faure S, Salazar-Fontana LI, Semichon M, Tybulewicz VL, Bismuth G, Trautmann A, Germain RN, Delon J (2004). ERM proteins regulate cytoskeleton relaxation promoting T cell-APC conjugation. Nat Immunol 5, 272-279. (Pubitemid 38332124)
10. Fehon RG, McClatchey AI, Bretscher A (2010). Organizing the cell cortex: the role of ERM proteins. Nat Rev Mol Cell Biol 11, 276-287.
11. Fievet B, Louvard D, Arpin M (2007). ERM proteins in epithelial cell organization and functions. Biochim Biophys Acta 1773, 653-660. (Pubitemid 46660175)
12. Gautreau A, Louvard D, Arpin M (2000). Morphogenic effects of ezrin require a phosphorylation-induced transition from oligomers to monomers at the plasma membrane. J Cell Biol 150, 193-203. (Pubitemid 30480237)
13. Godar S et al. (2008). Growth-inhibitory and tumor-suppressive functions of p53 depend on its repression of CD44 expression. Cell 134, 62-73. (Pubitemid 351905743)
14. Halder SK, Beauchamp RD, Datta PK (2005). A specific inhibitor of TGF-beta receptor kinase, SB-431542, as a potent antitumor agent for human cancers. Neoplasia 7, 509-521. (Pubitemid 40791869)
15. Hutchison N, Hendry BM, Sharpe CC (2009). Rho isoforms have distinct and specific functions in the process of epithelial to mesenchymal transition in renal proximal tubular cells. Cell Signal 21, 1522-1531.
16. Ilani T, Khanna C, Zhou M, Veenstra TD, Bretscher A (2007). Immune synapse formation requires ZAP-70 recruitment by ezrin and CD43 removal by moesin. J Cell Biol 179, 733-746. (Pubitemid 350146258)
17. Kasai H, Allen JT, Mason RM, Kamimura T, Zhang Z (2005). TGF-beta1 induces human alveolar epithelial to mesenchymal cell transition (EMT). Respir Res 6, 56.
18. Keshamouni VG et al. (2006). Differential protein expression profiling by iTRAQ-2DLC-MS/MS of lung cancer cells undergoing epithelial-mesenchymal transition reveals a migratory/invasive phenotype. J Proteome Res 5, 1143-1154. (Pubitemid 43727792)
19. Kikuchi S et al. (2002). Radixin deficiency causes conjugated hyperbilirubinemia with loss of Mrp2 from bile canalicular membranes. Nat Genet 31, 320-325.
20. Kitajiri S, Fukumoto K, Hata M, Sasaki H, Katsuno T, Nakagawa T, Ito J, Tsukita S, Tsukita S (2004). Radixin deficiency causes deafness associated with progressive degeneration of cochlear stereocilia. J Cell Biol 166, 559-570. (Pubitemid 39097175)
21. Lamouille S, Derynck R (2007). Cell size and invasion in TGF-beta-induced epithelial to mesenchymal transition is regulated by activation of the mTOR pathway. J Cell Biol 178, 437-451. (Pubitemid 47196152)
22. Lee JH, Katakai T, Hara T, Gonda H, Sugai M, Shimizu A (2004). Roles of p-ERM and Rho-ROCK signaling in lymphocyte polarity and uropod formation. J Cell Biol 167, 327-337. (Pubitemid 39435075)
23. Lenferink AE, Cantin C, Nantel A, Wang E, Durocher Y, Banville M, Paul-Roc B, Marcil A, Wilson MR, O'Connor-McCourt MD (2010). Transcriptome profiling of a TGF-beta-induced epithelial-to-mesenchymal transition reveals extracellular clusterin as a target for therapeutic antibodies. Oncogene 29, 831-844.
24. Mackay DJ, Esch F, Furthmayr H, Hall A (1997). Rho- and rac-dependent assembly of focal adhesion complexes and actin filaments in permeabilized fibroblasts: an essential role for ezrin/radixin/moesin proteins. J Cell Biol 138, 927-938. (Pubitemid 27365053)
25. Maeda M, Johnson KR, Wheelock MJ (2005). Cadherin switching: essential for behavioral but not morphological changes during an epithelium-to-mesenchyme transition. J Cell Sci 118, 873-887. (Pubitemid 40484880)
26. Mani SA et al. (2008). The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133, 704-715. (Pubitemid 351636299)
27. Martin-Villar E, Megias D, Castel S, Yurrita MM, Vilaro S, Quintanilla M (2006). Podoplanin binds ERM proteins to activate RhoA and promote epithelial-mesenchymal transition. J Cell Sci 119, 4541-4553. (Pubitemid 44830653)
28. Masszi A, Di Ciano C, Sirokmany G, Arthur WT, Rotstein OD, Wang J, McCulloch CA, Rosivall L, Mucsi I, Kapus A (2003). Central role for Rho in TGF-beta1-induced alpha-smooth muscle actin expression during epithelial-mesenchymal transition. Am J Physiol Renal Physiol 284, F911-F924. (Pubitemid 36443575)
29. Matsui T, Maeda M, Doi Y, Yonemura S, Amano M, Kaibuchi K, Tsukita S, Tsukita S (1998). Rho-kinase phosphorylates COOH-terminal threonines of ezrin/radixin/moesin (ERM) proteins and regulates their head-to-tail association. J Cell Biol 140, 647-657. (Pubitemid 28134067)
30. Miettinen PJ, Ebner R, Lopez AR, Derynck R (1994). TGF-beta induced transdifferentiation of mammary epithelial cells to mesenchymal cells: involvement of type I receptors. J Cell Biol 127, 2021-2036.
31. Mori M et al. (2009). Zyxin mediates actin fiber reorganization in epithelial-mesenchymal transition and contributes to endocardial morphogenesis. Mol Biol Cell 20, 3115-3124.
32. Moustakas A, Heldin CH (2007). Signaling networks guiding epithelial-mesenchymal transitions during embryogenesis and cancer progression. Cancer Sci 98, 1512-1520. (Pubitemid 47308444)
33. Nakamura K, Yano H, Schaefer E, Sabe H (2001). Different modes and qualities of tyrosine phosphorylation of Fak and Pyk2 during epithelial-mesenchymal transdifferentiation and cell migration: analysis of specific phosphorylation events using site-directed antibodies. Oncogene 20, 2626-2635. (Pubitemid 32525293)
34. Okayama T et al. (2008). Attenuated response to liver injury in moesin-deficient mice: impaired stellate cell migration and decreased fibrosis. Biochim Biophys Acta 1782 542-548.
35. Oshiro N, Fukata Y, Kaibuchi K (1998). Phosphorylation of moesin by rho-associated kinase (Rho-kinase) plays a crucial role in the formation of microvilli-like structures. J Biol Chem 273, 34663-34666. (Pubitemid 29028150)
36. Ostapkowicz A, Inai K, Smith L, Kreda S, Spychala J (2006). Lipid rafts remodeling in estrogen receptor-negative breast cancer is reversed by histone deacetylase inhibitor. Mol Cancer Ther 5, 238-245.
37. Riedl J et al. (2008). LifeAct: a versatile marker to visualize F-actin. Nat Methods 5, 605-607. (Pubitemid 351911864)
38. Rowe RG et al. (2009). Mesenchymal cells reactivate Snail1 expression to drive three-dimensional invasion programs. J Cell Biol 184, 399-408.
39. Safina AF, Varga AE, Bianchi A, Zheng Q, Kunnev D, Liang P, Bakin AV (2009). Ras alters epithelial-mesenchymal transition in response to TGFbeta by reducing actin fibers and cell-matrix adhesion. Cell Cycle 8, 284-298.
40. 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)
41. Shaw RJ, Henry M, Solomon F, Jacks T (1998). RhoA-dependent phosphorylation and relocalization of ERM proteins into apical membrane/actin protrusions in fibroblasts. Mol Biol Cell 9, 403-419. (Pubitemid 28084134)
42. Shi-Wen X et al. (2004). Endothelin-1 promotes myofibroblast induction through the ETA receptor via a rac/phosphoinositide 3-kinase/Akt-dependent pathway and is essential for the enhanced contractile phenotype of fibrotic fibroblasts. Mol Biol Cell 15, 2707-2719. (Pubitemid 38691860)
43. Speck O, Hughes SC, Noren NK, Kulikauskas RM, Fehon RG (2003). Moesin functions antagonistically to the Rho pathway to maintain epithelial integrity. Nature 421, 83-87. (Pubitemid 36077089)
44. Takahashi E et al. (2010). Tumor necrosis factor-alpha regulates transforming growth factor-beta-dependent epithelial-mesenchymal transition by promoting hyaluronan-CD44-moesin interaction. J Biol Chem 285, 4060-4073.
45. Takahashi K, Sasaki T, Mammoto A, Takaishi K, Kameyama T, Tsukita S, Takai Y (1997). Direct interaction of the Rho GDP dissociation inhibitor with ezrin/radixin/moesin initiates the activation of the Rho small G protein. J Biol Chem 272, 23371-23375. (Pubitemid 27392478)
46. Tamura A, Kikuchi S, Hata M, Katsuno T, Matsui T, Hayashi H, Suzuki Y, Noda T, Tsukita S, Tsukita S (2005). Achlorhydria by ezrin knockdown: defects in the formation/expansion of apical canaliculi in gastric parietal cells. J Cell Biol 169, 21-28. (Pubitemid 40562910)
47. Tavares AL, Mercado-Pimentel ME, Runyan RB, Kitten GT (2006). TGF beta-mediated RhoA expression is necessary for epithelial-mesenchymal transition in the embryonic chick heart. Dev Dyn 235, 1589-1598. (Pubitemid 43787961)
48. Valcourt U, Kowanetz M, Niimi H, Heldin CH, Moustakas A (2005). TGF-beta and the Smad signaling pathway support transcriptomic reprogramming during epithelial-mesenchymal cell transition. Mol Biol Cell 16, 1987-2002. (Pubitemid 40471965)
49. Vargha R, Endemann M, Kratochwill K, Riesenhuber A, Wick N, Krachler AM, Malaga-Dieguez L, Aufricht C (2006). Ex vivo reversal of in vivo transdifferentiation in mesothelial cells grown from peritoneal dialysate effluents. Nephrol Dial Transplant 21, 2943-2947. (Pubitemid 44542254)
50. Xie L, Law BK, Aakre ME, Edgerton M, Shyr Y, Bhowmick NA, Moses HL (2003). Transforming growth factor beta-regulated gene expression in a mouse mammary gland epithelial cell line. Breast Cancer Res 5, R187-198.
51. Xu J, Lamouille S, Derynck R (2009). TGF-beta-induced epithelial to mesenchymal transition. Cell Res 19, 156-172.
52. Yilmaz M, Christofori G (2009). EMT, the cytoskeleton, and cancer cell invasion. Cancer Metastasis Rev 28, 15-33.
53. Zavadil J, Bitzer M, Liang D, Yang YC, Massimi A, Kneitz S, Piek E, Bottinger EP (2001). Genetic programs of epithelial cell plasticity directed by transforming growth factor-beta. Proc Natl Acad Sci USA 98, 6686-6691. (Pubitemid 32538277)