β-spectrin regulates the hippo signaling pathway and modulates the basal actin network

Journal of Biological Chemistry

Volumn 290, Issue 10, 2015, Pages 6397-6407

  Wong, Kenneth Kin Lam ^a   Li, Wenyang ^b   An, Yanru ^a   Duan, Yangyang ^a   Li, Zhuoheng ^a   Kang, Yibin ^b   Yan, Yan ^a  

^a HONG KONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Hong Kong)

^b PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; CYTOLOGY; MAMMALS; PROTEINS; SIGNALING;

ACTIN CYTOSKELETON; FUNCTIONAL REGULATION; GENETIC SCREENS; MAMMALIAN CELLS; MOLECULAR MECHANISM; REPOLARIZATION; SIGNALING ACTIVITY; SIGNALING PATHWAYS;

CELL SIGNALING;

ACTIN; BETA SPECTRIN; MUTANT PROTEIN; SPECTRIN; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; HPO PROTEIN, DROSOPHILA; PROTEIN SERINE THREONINE KINASE; SIGNAL PEPTIDE;

ARTICLE; CELL POLARITY; CYTOSKELETON; DROSOPHILA; GENE SILENCING; GENETIC SCREENING; HIPPO SIGNALING PATHWAY; MAMMAL CELL; MUTATION; NONHUMAN; OOCYTE; OOCYTE DEVELOPMENT; OVARY FOLLICLE CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; REGULATORY MECHANISM; REPOLARIZATION; SIGNAL TRANSDUCTION; ANIMAL; EPITHELIUM CELL; FEMALE; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; OVARY FOLLICLE;

MAMMALIA;

ACTINS; ANIMALS; CYTOSKELETON; DROSOPHILA; DROSOPHILA PROTEINS; EPITHELIAL CELLS; FEMALE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MUTATION; OOCYTES; OOGENESIS; OVARIAN FOLLICLE; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; SPECTRIN;

EID: 84924942018     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.629493     Document Type: Article

References (75)

1. Pan, D. (2010) The hippo signaling pathway in development and cancer. Dev. Cell 19, 491-505
2. Yu, F. X., and Guan, K. L. (2013) The Hippo pathway: regulators and regulations. Genes Dev. 27, 355-371
3. Varelas, X. (2014) The Hippo pathway effectors TAZ and YAP in development, homeostasis and disease. Development 141, 1614-1626
4. Dupont, S., Morsut, L., Aragona, M., Enzo, E., Giulitti, S., Cordenonsi, M., Zanconato, F., Le Digabel, J., Forcato, M., Bicciato, S., Elvassore, N., and Piccolo, S. (2011) Role of YAP/TAZ in mechanotransduction. Nature 474, 179-183
5. Wada, K., Itoga, K., Okano, T., Yonemura, S., and Sasaki, H. (2011) Hippo pathway regulation by cell morphology and stress fibers. Development 138, 3907-3914
6. Zhao, B., Li, L., Wang, L., Wang, C. Y., Yu, J., and Guan, K. L. (2012) Cell detachment activates the Hippo pathway via cytoskeleton reorganization to induce anoikis. Genes Dev. 26, 54-68
7. Fernández, B. G., Gaspar, P., Brás-Pereira, C., Jezowska, B., Rebelo, S. R., and Janody, F. (2011) Actin-capping protein and the Hippo pathway regulate F-actin and tissue growth in Drosophila. Development 138, 2337-2346
8. Sansores-Garcia, L., Bossuyt, W., Wada, K., Yonemura, S., Tao, C., Sasaki, H., and Halder, G. (2011) Modulating F-actin organization induces organ growth by affecting the Hippo pathway. EMBO J. 30, 2325-2335
9. Aragona, M., Panciera, T., Manfrin, A., Giulitti, S., Michielin, F., Elvassore, N., Dupont, S., and Piccolo, S. (2013) A mechanical checkpoint controls multicellular growth through YAP/TAZ regulation by actin-processing factors. Cell 154, 1047-1059
10. Rauskolb, C., Sun, S., Sun, G., Pan, Y., and Irvine, K. D. (2014) Cytoskeletal tension inhibits Hippo signaling through an Ajuba-Warts complex. Cell 158, 143-156
11. Pinder, J. C., Bray, D., and Gratzer, W. B. (1975) Actin polymerisation induced by spectrin. Nature 258, 765-766
12. Tilney, L. G., and Detmers, P. (1975) Actin in erythrocyte ghosts and its association with spectrin: evidence for a nonfilamentous form of these two molecules in situ. J. Cell Biol. 66, 508-520
13. Cohen, C. M., Tyler, J. M., and Branton, D. (1980) Spectrin-actin associations studied by electron microscopy of shadowed preparations. Cell 21, 875-883
14. Marchesi, V. T., and Steers, E., Jr. (1968) Selective solubilization of a protein component of the red cell membrane. Science 159, 203-204
15. Byers, T. J., and Branton, D. (1985) Visualization of the protein associations in the erythrocyte membrane skeleton. Proc. Natl. Acad. Sci. U.S.A. 82, 6153-6157
16. Tsukita, S., Tsukita, S., and Ishikawa, H. (1980) Cytoskeletal network underlying the human erythrocyte membrane: thin-section electron microscopy. J. Cell Biol. 85, 567-576
17. Palek, J., and Lux, S. E. (1983) Red cell membrane skeletal defects in hereditary and acquired hemolytic anemias. Semin. Hematol. 20, 189-224
18. Agre, P., Casella, J. F., Zinkham, W. H., McMillan, C., and Bennett, V. (1985) Partial deficiency of erythrocyte spectrin in hereditary spherocytosis. Nature 314, 380-383
19. Agre, P., Orringer, E. P., and Bennett, V. (1982) Deficient red-cell spectrin in severe, recessively inherited spherocytosis. New Engl. J. Med. 306, 1155-1161
20. Mohandas, N., and Gallagher, P. G. (2008) Red cell membrane: past, present, and future. Blood 112, 3939-3948
21. Bennett, V., Davis, J., and Fowler, W. E. (1982) Brain spectrin, a membrane-associated protein related in structure and function to erythrocyte spectrin. Nature 299, 126-131
22. Burridge, K., Kelly, T., and Mangeat, P. (1982) Nonerythrocyte spectrins: actin-membrane attachment proteins occurring in many cell types. J. Cell Biol. 95, 478-486
23. Glenney, J. R., Jr., Glenney, P., Osborn, M., and Weber, K. (1982) An F-actin- and calmodulin-binding protein from isolated intestinal brush borders has a morphology related to spectrin. Cell 28, 843-854
24. Bennett, V., and Baines, A. J. (2001) Spectrin and ankyrin-based pathways: metazoan inventions for integrating cells into tissues. Physiol. Rev. 81, 1353-1392
25. Nelson, W. J., Shore, E. M., Wang, A. Z., and Hammerton, R. W. (1990) Identification of a membrane-cytoskeletal complex containing the cell adhesion molecule uvomorulin (E-cadherin), ankyrin, and fodrin in Madin-Darby canine kidney epithelial cells. J. Cell Biol. 110, 349-357
26. Lee, J. K., Coyne, R. S., Dubreuil, R. R., Goldstein, L. S., and Branton, D. (1993) Cell shape and interaction defects in alpha-spectrin mutants of Drosophila melanogaster. J. Cell Biol. 123, 1797-1809
27. McKeown, C., Praitis, V., and Austin, J. (1998) sma-1 encodes a βH-spectrin homolog required for Caenorhabditis elegans morphogenesis. Development 125, 2087-2098
28. Mangeat, P. H., and Burridge, K. (1984) Immunoprecipitation of nonerythrocyte spectrin within live cells following microinjection of specific antibodies: relation to cytoskeletal structures. J. Cell Biol. 98, 1363-1377
29. Hammarlund, M., Davis, W. S., and Jorgensen, E. M. (2000) Mutations in β-spectrin disrupt axon outgrowth and sarcomere structure. J. Cell Biol. 149, 931-942
30. Moorthy, S., Chen, L., and Bennett, V. (2000) Caenorhabditis elegans β-G spectrin is dispensable for establishment of epithelial polarity, but essential for muscular and neuronal function. J. Cell Biol. 149, 915-930
31. Gao, Y., Perkins, E. M., Clarkson, Y. L., Tobia, S., Lyndon, A. R., Jackson, M., and Rothstein, J. D. (2011) β-III spectrin is critical for development of Purkinje cell dendritic tree and spine morphogenesis. J. Neurosci. 31, 16581-16590
32. Featherstone, D. E., Davis, W. S., Dubreuil, R. R., and Broadie, K. (2001) Drosophila α- and β-spectrin mutations disrupt presynaptic neurotransmitter release. J. Neurosci. 21, 4215-4224
33. Pielage, J., Fetter, R. D., and Davis, G. W. (2005) Presynaptic spectrin is essential for synapse stabilization. Curr. Biol. 15, 918-928
34. Pielage, J., Fetter, R. D., and Davis, G. W. (2006) A postsynaptic spectrin scaffold defines active zone size, spacing, and efficacy at the Drosophila neuromuscular junction. J. Cell Biol. 175, 491-503
35. Xu, K., Zhong, G., and Zhuang, X. (2013) Actin, spectrin, and associated proteins form a periodic cytoskeletal structure in axons. Science 339, 452-456
36. Krieg, M., Dunn, A. R., and Goodman, M. B. (2014) Mechanical control of the sense of touch by β-spectrin. Nat. Cell Biol. 16, 224-233
37. Denef, N., Chen, Y., Weeks, S. D., Barcelo, G., and Schüpbach, T. (2008) Crag regulates epithelial architecture and polarized deposition of basement membrane proteins in Drosophila. Dev. Cell 14, 354-364
38. Clark, I., Giniger, E., Ruohola-Baker, H., Jan, L. Y., and Jan, Y. N. (1994) Transient posterior localization of a kinesin fusion protein reflects anteroposterior polarity of the Drosophila oocyte. Curr. Biol. 4, 289-300
39. Schuldt, A. J., Adams, J. H., Davidson, C. M., Micklem, D. R., Haseloff, J., St Johnston, D., and Brand, A. H. (1998) Miranda mediates asymmetric protein and RNA localization in the developing nervous system. Genes Dev. 12, 1847-1857
40. Xi, R., McGregor, J. R., and Harrison, D. A. (2003) A gradient of JAK pathway activity patterns the anterior-posterior axis of the follicular epithelium. Dev. Cell 4, 167-177
41. Pai, L. M., Barcelo, G., and Schüpbach, T. (2000) D-cbl, a negative regulator of the Egfr pathway, is required for dorsoventral patterning in Drosophila oogenesis. Cell 103, 51-61
42. Boedigheimer, M., and Laughon, A. (1993) Expanded: a gene involved in the control of cell proliferation in imaginal discs. Development 118, 1291-1301
43. Hay, B. A., Wassarman, D. A., and Rubin, G. M. (1995) Drosophila homologs of baculovirus inhibitor of apoptosis proteins function to block cell death. Cell 83, 1253-1262
44. Oda, H., and Tsukita, S. (2001) Real-time imaging of cell-cell adherens junctions reveals that Drosophila mesoderm invagination begins with two phases of apical constriction of cells. J. Cell Sci. 114, 493-501
45. Rauzi, M., Lenne, P. F., and Lecuit, T. (2010) Planar polarized actomyosin contractile flows control epithelial junction remodelling. Nature 468, 1110-1114
46. Maitra, S., Kulikauskas, R. M., Gavilan, H., and Fehon, R. G. (2006) The tumor suppressors Merlin and Expanded function cooperatively to modulate receptor endocytosis and signaling. Curr. Biol. 16, 702-709
47. McCartney, B. M., and Fehon, R. G. (1996) Distinct cellular and subcellular patterns of expression imply distinct functions for the Drosophila homologues of moesin and the neurofibromatosis 2 tumor suppressor, merlin. J. Cell Biol. 133, 843-852
48. Hülsmeier, J., Pielage, J., Rickert, C., Technau, G. M., Klämbt, C., and Stork, T. (2007) Distinct functions of α-Spectrin and β-Spectrin during axonal pathfinding. Development 134, 713-722
49. Prasad, M., Jang, A. C., Starz-Gaiano, M., Melani, M., and Montell, D. J. (2007) A protocol for culturing Drosophila melanogaster stage 9 egg chambers for live imaging. Nat. Protoc. 2, 2467-2473
50. Roth, S., and Lynch, J. A. (2009) Symmetry breaking during Drosophila oogenesis. Cold Spring Harb. Perspect. Biol. 1, a001891
51. González-Reyes, A., Elliott, H., and St Johnston, D. (1995) Polarization of both major body axes in Drosophila by gurken-torpedo signalling. Nature 375, 654-658
52. Roth, S., Neuman-Silberberg, F. S., Barcelo, G., and Schüpbach, T. (1995) cornichon and the EGF receptor signaling process are necessary for both anterior-posterior and dorsal-ventral pattern formation in Drosophila. Cell 81, 967-978
53. Deng, W. M., Althauser, C., and Ruohola-Baker, H. (2001) Notch-Delta signaling induces a transition from mitotic cell cycle to endocycle in Drosophila follicle cells. Development 128, 4737-4746
54. López-Schier, H., and St Johnston, D. (2001) Delta signaling from the germ line controls the proliferation and differentiation of the somatic follicle cells during Drosophila oogenesis. Genes Dev. 15, 1393-1405
55. Meignin, C., Alvarez-Garcia, I., Davis, I., and Palacios, I. M. (2007) The salvador-warts-hippo pathway is required for epithelial proliferation and axis specification in Drosophila. Curr. Biol. 17, 1871-1878
56. Polesello, C., and Tapon, N. (2007) Salvador-warts-hippo signaling promotes Drosophila posterior follicle cell maturation downstream of notch. Curr. Biol. 17, 1864-1870
57. Yu, J., Poulton, J., Huang, Y. C., and Deng, W. M. (2008) The hippo pathway promotes Notch signaling in regulation of cell differentiation, proliferation, and oocyte polarity. PLoS ONE 3, e1761
58. Yan, Y., Denef, N., Tang, C., and Schüpbach, T. (2011) Drosophila PI4KIIIα is required in follicle cells for oocyte polarization and Hippo signaling. Development 138, 1697-1703
59. St Johnston, D., Beuchle, D., and Nüsslein-Volhard, C. (1991) Staufen, a gene required to localize maternal RNAs in the Drosophila egg. Cell 66, 51-63
60. Byers, T. J., Dubreuil, R., Branton, D., Kiehart, D. P., and Goldstein, L. S. (1987) Drosophila spectrin: II: conserved features of the α-subunit are revealed by analysis of cDNA clones and fusion proteins. J. Cell Biol. 105, 2103-2110
61. Byers, T. J., Husain-Chishti, A., Dubreuil, R. R., Branton, D., and Goldstein, L. S. (1989) Sequence similarity of the amino-terminal domain of Drosophila β spectrin to α actinin and dystrophin. J. Cell Biol. 109, 1633-1641
62. Dubreuil, R. R., Byers, T. J., Stewart, C. T., and Kiehart, D. P. (1990) A β-spectrin isoform from Drosophila (β H) is similar in size to vertebrate dystrophin. J. Cell Biol. 111, 1849-1858
63. Lee, J. K., Brandin, E., Branton, D., and Goldstein, L. S. (1997) α-Spectrin is required for ovarian follicle monolayer integrity in Drosophila melanogaster. Development 124, 353-362
64. Sun, J., and Deng, W. M. (2005) Notch-dependent downregulation of the homeodomain gene cut is required for the mitotic cycle/endocycle switch and cell differentiation in Drosophila follicle cells. Development 132, 4299-4308
65. Hamaratoglu, F., Willecke, M., Kango-Singh, M., Nolo, R., Hyun, E., Tao, C., Jafar-Nejad, H., and 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
66. Harvey, K. F., Pfleger, C. M., and Hariharan, I. K. (2003) The Drosophila Mst ortholog, hippo, restricts growth and cell proliferation and promotes apoptosis. Cell 114, 457-467
67. Lucas, E. P., Khanal, I., Gaspar, P., Fletcher, G. C., Polesello, C., Tapon, N., and Thompson, B. J. (2013) The Hippo pathway polarizes the actin cytoskeleton during collective migration of Drosophila border cells. J. Cell Biol. 201, 875-885
68. Pesacreta, T. C., Byers, T. J., Dubreuil, R., Kiehart, D. P., and Branton, D. (1989) Drosophila spectrin: the membrane skeleton during embryogenesis. J. Cell Biol. 108, 1697-1709
69. Couzens, A. L., Knight, J. D., Kean, M. J., Teo, G., Weiss, A., Dunham, W. H., Lin, Z. Y., Bagshaw, R. D., Sicheri, F., Pawson, T., Wrana, J. L., Choi, H., and Gingras, A. C. (2013) Protein interaction network of the mammalian Hippo pathway reveals mechanisms of kinase-phosphatase interactions. Sci. Signal. 6, rs15
70. Kwon, Y., Vinayagam, A., Sun, X., Dephoure, N., Gygi, S. P., Hong, P., and Perrimon, N. (2013) The Hippo signaling pathway interactome. Science 342, 737-740
71. Machnicka, B., Grochowalska, R., Bogusławska, D. M., Sikorski, A. F., and Lecomte, M. C. (2012) Spectrin-based skeleton as an actor in cell signaling. Cell. Mol. Life Sci. 69, 191-201
72. Gutzeit, H. O. (1990) The microfilament pattern in the somatic follicle cells of mid-vitellogenic ovarian follicles of Drosophila. Eur. J. Cell Biol. 53, 349-356
73. He, L., Wang, X., Tang, H. L., and Montell, D. J. (2010) Tissue elongation requires oscillating contractions of a basal actomyosin network. Nat. Cell Biol. 12, 1133-1142
74. Delaunay, J. (2007) The molecular basis of hereditary red cell membrane disorders. Blood Rev. 21, 1-20
75. Schultz, J., Milpetz, F., Bork, P., and Ponting, C. P. (1998) SMART, a simple modular architecture research tool: identification of signaling domains. Proc. Natl. Acad. Sci. U.S.A. 95, 5857-5864