The Spectrin cytoskeleton regulates the Hippo signalling pathway

EMBO Journal

Volumn 34, Issue 7, 2015, Pages 940-954

  Fletcher, Georgina C ^a   Elbediwy, Ahmed ^a   Khanal, Ichha ^a   Ribeiro, Paulo S ^a   Tapon, Nic ^a   Thompson, Barry J ^a,b  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

cytoskeleton; Hippo signalling; Spectrin; YAP

Indexed keywords

BETA SPECTRIN; CRUMBS PROTEIN; FERM DOMAIN PROTEIN EXPANDED; FODRIN; PROTEIN; SPECTRIN; UNCLASSIFIED DRUG; YKI PROTEIN; CRUMBS PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; EXPANDED PROTEIN, DROSOPHILA; HPO PROTEIN, DROSOPHILA; MEMBRANE PROTEIN; NUCLEAR PROTEIN; PROTEIN SERINE THREONINE KINASE; SIGNAL PEPTIDE; TRANSACTIVATOR PROTEIN; YORKIE PROTEIN, DROSOPHILA;

ADULT; APICAL MEMBRANE; ARTICLE; CELL DENSITY; CONTROLLED STUDY; CYTOSKELETON; DROSOPHILA; EPITHELIUM CELL; FEMALE; GENE CONTROL; HIPPO SIGNALLING; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM; NONHUMAN; OVARY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; TISSUE GROWTH; ANIMAL; CELL LINE; CYTOLOGY; DROSOPHILA MELANOGASTER; GENETICS; MECHANOTRANSDUCTION; METABOLISM; OVARY FOLLICLE; PHYSIOLOGY;

ANIMALS; CELL LINE; CYTOSKELETON; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MECHANOTRANSDUCTION, CELLULAR; MEMBRANE PROTEINS; NUCLEAR PROTEINS; OVARIAN FOLLICLE; PROTEIN-SERINE-THREONINE KINASES; SPECTRIN; TRANS-ACTIVATORS;

EID: 84926258240     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201489642     Document Type: Article

References (71)

1. Aegerter-Wilmsen T, Aegerter CM, Hafen E, Basler K, (2007) Model for the regulation of size in the wing imaginal disc of Drosophila. Mech Dev 124: 318-326
2. Aragona M, Panciera T, Manfrin A, Giulitti S, Michielin F, Elvassore N, Dupont S, Piccolo S, (2013) A mechanical checkpoint controls multicellular growth through YAP/TAZ regulation by actin-processing factors. Cell 154: 1047-1059
3. Baumgartner R, Poernbacher I, Buser N, Hafen E, Stocker H, (2010) The WW domain protein Kibra acts upstream of Hippo in Drosophila. Dev Cell 18: 309-316
4. Bennett V, Baines AJ, (2001) Spectrin and ankyrin-based pathways: metazoan inventions for integrating cells into tissues. Physiol Rev 81: 1353-1392
5. Bennett V, Healy J, (2009) Membrane domains based on ankyrin and spectrin associated with cell-cell interactions. Cold Spring Harb Perspect Biol 1: a003012
6. Byers TJ, Branton D, (1985) Visualization of the protein associations in the erythrocyte membrane skeleton. Proc Natl Acad Sci USA 82: 6153-6157
7. Cai J, Zhang N, Zheng Y, de Wilde RF, Maitra A, Pan D, (2010) The Hippo signaling pathway restricts the oncogenic potential of an intestinal regeneration program. Genes Dev 24: 2383-2388
8. Camargo FD, Gokhale S, Johnnidis JB, Fu D, Bell GW, Jaenisch R, Brummelkamp TR, (2007) YAP1 increases organ size and expands undifferentiated progenitor cells. Curr Biol 17: 2054-2060
9. Chen CL, Gajewski KM, Hamaratoglu F, Bossuyt W, Sansores-Garcia L, Tao C, Halder G, (2010) The apical-basal cell polarity determinant Crumbs regulates Hippo signaling in Drosophila. Proc Natl Acad Sci USA 107: 15810-15815
10. Codelia VA, Sun G, Irvine KD, (2014) Regulation of YAP by mechanical strain through Jnk and Hippo signaling. Curr Biol 24: 2012-2017
11. Cordenonsi M, Zanconato F, Azzolin L, Forcato M, Rosato A, Frasson C, Inui M, Montagner M, Parenti AR, Poletti A, Daidone MG, Dupont S, Basso G, Bicciato S, Piccolo S, (2011) The Hippo transducer TAZ confers cancer stem cell-related traits on breast cancer cells. Cell 147: 759-772
12. Das Thakur M, Feng Y, Jagannathan R, Seppa MJ, Skeath JB, Longmore GD, (2010) Ajuba LIM proteins are negative regulators of the Hippo signaling pathway. Curr Biol 20: 657-662
13. Dupont S, Morsut L, Aragona M, Enzo E, Giulitti S, Cordenonsi M, Zanconato F, Le Digabel J, Forcato M, Bicciato S, Elvassore N, Piccolo S, (2011) Role of YAP/TAZ in mechanotransduction. Nature 474: 179-183
14. Fletcher GC, Lucas EP, Brain R, Tournier A, Thompson BJ, (2012) Positive feedback and mutual antagonism combine to polarize Crumbs in the Drosophila follicle cell epithelium. Curr Biol 22: 1116-1122
15. Gaspar P, Tapon N, (2014) Sensing the local environment: actin architecture and Hippo signalling. Curr Opin Cell Biol 31C: 74-83
16. Genevet A, Wehr MC, Brain R, Thompson BJ, Tapon N, (2010) Kibra is a regulator of the Salvador/Warts/Hippo signaling network. Dev Cell 18: 300-308
17. Halder G, Johnson RL, (2011) Hippo signaling: growth control and beyond. Development 138: 9-22
18. Hamaratoglu F, Willecke M, Kango-Singh M, Nolo R, Hyun E, Tao C, Jafar-Nejad H, Halder G, (2006) The tumour-suppressor genes NF2/Merlin and Expanded act through Hippo signalling to regulate cell proliferation and apoptosis. Nat Cell Biol 8: 27-36
19. Harvey KF, Pfleger CM, Hariharan IK, (2003) The Drosophila Mst ortholog, hippo, restricts growth and cell proliferation and promotes apoptosis. Cell 114: 457-467
20. 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
21. Huang J, Wu S, Barrera J, Matthews K, Pan D, (2005) The Hippo signaling pathway coordinately regulates cell proliferation and apoptosis by inactivating Yorkie, the Drosophila Homolog of YAP. Cell 122: 421-434
22. Huang J, Kalderon D, (2014) Coupling of Hedgehog and Hippo pathways promotes stem cell maintenance by stimulating proliferation. J Cell Biol 205: 325-338
23. Irvine KD, (2012) Integration of intercellular signaling through the Hippo pathway. Semin Cell Dev Biol 23: 812-817
24. Johnson CP, Tang HY, Carag C, Speicher DW, Discher DE, (2007) Forced unfolding of proteins within cells. Science 317: 663-666
25. Karpowicz P, Perez J, Perrimon N, (2010) The Hippo tumor suppressor pathway regulates intestinal stem cell regeneration. Development 137: 4135-4145
26. Kim NG, Koh E, Chen X, Gumbiner BM, (2011) E-cadherin mediates contact inhibition of proliferation through Hippo signaling-pathway components. Proc Natl Acad Sci USA 108: 11930-11935
27. Koontz LM, Liu-Chittenden Y, Yin F, Zheng Y, Yu J, Huang B, Chen Q, Wu S, Pan D, (2013) The Hippo effector Yorkie controls normal tissue growth by antagonizing scalloped-mediated default repression. Dev Cell 25: 388-401
28. Krieg M, Dunn AR, Goodman MB, (2014) Mechanical control of the sense of touch by beta-spectrin. Nat Cell Biol 16: 224-233
29. Lee JK, Brandin E, Branton D, Goldstein LS, (1997) alpha-Spectrin is required for ovarian follicle monolayer integrity in Drosophila melanogaster. Development 124: 353-362
30. Legoff L, Rouault H, Lecuit T, (2013) A global pattern of mechanical stress polarizes cell divisions and cell shape in the growing Drosophila wing disc. Development 140: 4051-4059
31. Ling C, Zheng Y, Yin F, Yu J, Huang J, Hong Y, Wu S, Pan D, (2010) The apical transmembrane protein Crumbs functions as a tumor suppressor that regulates Hippo signaling by binding to Expanded. Proc Natl Acad Sci USA 107: 10532-10537
32. Lucas EP, Khanal I, Gaspar P, Fletcher GC, Polesello C, Tapon N, Thompson BJ, (2013) The Hippo pathway polarizes the actin cytoskeleton during collective migration of Drosophila border cells. J Cell Biol 201: 875-885
33. Mao Y, Tournier AL, Bates PA, Gale JE, Tapon N, Thompson BJ, (2011) Planar polarization of the atypical myosin Dachs orients cell divisions in Drosophila. Genes Dev 25: 131-136
34. Mao Y, Tournier AL, Hoppe A, Kester L, Thompson BJ, Tapon N, (2013) Differential proliferation rates generate patterns of mechanical tension that orient tissue growth. EMBO J 32: 2790-2803
35. Medina E, Williams J, Klipfell E, Zarnescu D, Thomas G, Le Bivic A, (2002) Crumbs interacts with moesin and beta(Heavy)-spectrin in the apical membrane skeleton of Drosophila. J Cell Biol 158: 941-951
36. Meignin C, Alvarez-Garcia I, Davis I, Palacios IM, (2007) The salvador-warts-hippo pathway is required for epithelial proliferation and axis specification in Drosophila. Curr Biol 17: 1871-1878
37. Meng F, Sachs F, (2012) Orientation-based FRET sensor for real-time imaging of cellular forces. J Cell Sci 125: 743-750
38. Pan D, (2010) The hippo signaling pathway in development and cancer. Dev Cell 19: 491-505
39. Pellikka M, Tanentzapf G, Pinto M, Smith C, McGlade CJ, Ready DF, Tepass U, (2002) Crumbs, the Drosophila homologue of human CRB1/RP12, is essential for photoreceptor morphogenesis. Nature 416: 143-149
40. Polesello C, Tapon N, (2007) Salvador-warts-hippo signaling promotes Drosophila posterior follicle cell maturation downstream of notch. Curr Biol 17: 1864-1870
41. Rauskolb C, Sun S, Sun G, Pan Y, Irvine KD, (2014) Cytoskeletal tension inhibits hippo signaling through an Ajuba-Warts complex. Cell 158: 143-156
42. Robinson BS, Huang J, Hong Y, Moberg KH, (2010) Crumbs regulates Salvador/Warts/Hippo signaling in Drosophila via the FERM-domain protein Expanded. Curr Biol 20: 582-590
43. Rosse C, Formstecher E, Boeckeler K, Zhao Y, Kremerskothen J, White MD, Camonis JH, Parker PJ, (2009) An aPKC-exocyst complex controls paxillin phosphorylation and migration through localised JNK1 activation. PLoS Biol 7: e1000235
44. Sansores-Garcia L, Bossuyt W, Wada K, Yonemura S, Tao C, Sasaki H, Halder G, (2011) Modulating F-actin organization induces organ growth by affecting the Hippo pathway. EMBO J 30: 2325-2335
45. Sansores-Garcia L, Atkins M, Moya IM, Shahmoradgoli M, Tao C, Mills GB, Halder G, (2013) Mask is required for the activity of the Hippo pathway effector Yki/YAP. Curr Biol 23: 229-235
46. Schlegelmilch K, Mohseni M, Kirak O, Pruszak J, Rodriguez JR, Zhou D, Kreger BT, Vasioukhin V, Avruch J, Brummelkamp TR, Camargo FD, (2011) Yap1 acts downstream of alpha-catenin to control epidermal proliferation. Cell 144: 782-795
47. Schluck T, Nienhaus U, Aegerter-Wilmsen T, Aegerter CM, (2013) Mechanical control of organ size in the development of the Drosophila wing disc. PLoS One 8: e76171
48. Shaw RL, Kohlmaier A, Polesello C, Veelken C, Edgar BA, Tapon N, (2010) The Hippo pathway regulates intestinal stem cell proliferation during Drosophila adult midgut regeneration. Development 137: 4147-4158
49. Sidor CM, Brain R, Thompson BJ, (2013) Mask proteins are cofactors of Yorkie/YAP in the Hippo pathway. Curr Biol 23: 223-228
50. Silvis MR, Kreger BT, Lien WH, Klezovitch O, Rudakova GM, Camargo FD, Lantz DM, Seykora JT, Vasioukhin V, (2011) Alpha-catenin is a tumor suppressor that controls cell accumulation by regulating the localization and activity of the transcriptional coactivator Yap1. Sci Signal 4: ra33
51. Stabach PR, Simonovic I, Ranieri MA, Aboodi MS, Steitz TA, Simonovic M, Morrow JS, (2009) The structure of the ankyrin-binding site of beta-spectrin reveals how tandem spectrin-repeats generate unique ligand-binding properties. Blood 113: 5377-5384
52. Staley BK, Irvine KD, (2010) Warts and Yorkie mediate intestinal regeneration by influencing stem cell proliferation. Curr Biol 20: 1580-1587
53. Stokke BT, Mikkelsen A, Elgsaeter A, (1986) Spectrin, human erythrocyte shapes, and mechanochemical properties. Biophys J 49: 319-327
54. Tapon N, Harvey KF, (2012) The Hippo pathway-from top to bottom and everything in between. Semin Cell Dev Biol 23: 768-769
55. Thomas GH, Kiehart DP, (1994) Beta heavy-spectrin has a restricted tissue and subcellular distribution during Drosophila embryogenesis. Development 120: 2039-2050
56. Thomas GH, Zarnescu DC, Juedes AE, Bales MA, Londergan A, Korte CC, Kiehart DP, (1998) Drosophila betaHeavy-spectrin is essential for development and contributes to specific cell fates in the eye. Development 125: 2125-2134
57. Thomas GH, Williams JA, (1999) Dynamic rearrangement of the spectrin membrane skeleton during the generation of epithelial polarity in Drosophila. J Cell Sci 112 (Pt 17): 2843-2852
58. Thompson BJ, Pichaud F, Roper K, (2013) Sticking together the Crumbs-an unexpected function for an old friend. Nat Rev Mol Cell Biol 14: 307-314
59. Udan RS, Kango-Singh M, Nolo R, Tao C, Halder G, (2003) Hippo promotes proliferation arrest and apoptosis in the Salvador/Warts pathway. Nat Cell Biol 5: 914-920
60. Ursitti JA, Pumplin DW, Wade JB, Bloch RJ, (1991) Ultrastructure of the human erythrocyte cytoskeleton and its attachment to the membrane. Cell Motil Cytoskelet 19: 227-243
61. Varelas X, Samavarchi-Tehrani P, Narimatsu M, Weiss A, Cockburn K, Larsen BG, Rossant J, Wrana JL, (2010) The Crumbs complex couples cell density sensing to Hippo-dependent control of the TGF-beta-SMAD pathway. Dev Cell 19: 831-844
62. Wang Y, Riechmann V, (2007) The role of the actomyosin cytoskeleton in coordination of tissue growth during Drosophila oogenesis. Curr Biol 17: 1349-1355
63. Wu S, Huang J, Dong J, Pan D, (2003) hippo encodes a Ste-20 family protein kinase that restricts cell proliferation and promotes apoptosis in conjunction with salvador and warts. Cell 114: 445-456
64. Wu S, Liu Y, Zheng Y, Dong J, Pan D, (2008) The TEAD/TEF family protein Scalloped mediates transcriptional output of the Hippo growth-regulatory pathway. Dev Cell 14: 388-398
65. Yin F, Yu J, Zheng Y, Chen Q, Zhang N, Pan D, (2013) Spatial organization of Hippo signaling at the plasma membrane mediated by the tumor suppressor Merlin/NF2. Cell 154: 1342-1355
66. Yu J, Zheng Y, Dong J, Klusza S, Deng WM, Pan D, (2010) Kibra functions as a tumor suppressor protein that regulates Hippo signaling in conjunction with Merlin and Expanded. Dev Cell 18: 288-299
67. Zarnescu DC, Thomas GH, (1999) Apical spectrin is essential for epithelial morphogenesis but not apicobasal polarity in Drosophila. J Cell Biol 146: 1075-1086
68. Zhang N, Bai H, David KK, Dong J, Zheng Y, Cai J, Giovannini M, Liu P, Anders RA, Pan D, (2010) The Merlin/NF2 tumor suppressor functions through the YAP oncoprotein to regulate tissue homeostasis in mammals. Dev Cell 19: 27-38
69. Zhang H, Pasolli HA, Fuchs E, (2011) Yes-associated protein (YAP) transcriptional coactivator functions in balancing growth and differentiation in skin. Proc Natl Acad Sci USA 108: 2270-2275
70. Zhao B, Wei X, Li W, Udan RS, Yang Q, Kim J, Xie J, Ikenoue T, Yu J, Li L, Zheng P, Ye K, Chinnaiyan A, Halder G, Lai ZC, Guan KL, (2007) Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev 21: 2747-2761
71. Zhao B, Li L, Lu Q, Wang LH, Liu CY, Lei Q, Guan KL, (2011) Angiomotin is a novel Hippo pathway component that inhibits YAP oncoprotein. Genes Dev 25: 51-63