The hippo pathway member Yap plays a key role in influencing fate decisions in muscle satellite cells

Journal of Cell Science

Volumn 125, Issue 24, 2012, Pages 6009-6019

  Judson, Robert N ^a   Tremblay, Annie M ^b,c,d   Knopp, Paul ^e   White, Robert B ^e,f   Urcia, Roby ^a   De Bari, Cosimo ^a   Zammit, Peter S ^e   Camargo, Fernando D ^b,c,d   Wackerhage, Henning ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c Harvard University   (United States)

^d HARVARD STEM CELL INSTITUTE   (United States)

^e KING'S COLLEGE LONDON   (United Kingdom)

^f EDITH COWAN UNIVERSITY   (Australia)

Author keywords

Hippo pathway; Satellite cells; Skeletal muscle; Yes associated protein (Yap)

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; CD34 ANTIGEN; MYOD PROTEIN; REGULATOR PROTEIN; TRANSCRIPTION FACTOR PAX7; UNCLASSIFIED DRUG; YES ASSOCIATED PROTEIN; HIPPO PROTEIN, MOUSE; PHOSPHOPROTEIN; PROTEIN SERINE THREONINE KINASE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; YAP PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CELL ACTIVATION; CELL DIFFERENTIATION; CELL FATE; CELL PROLIFERATION; CELL RENEWAL; CONTROLLED STUDY; GENE SILENCING; MOUSE; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SKELETAL MUSCLE SATELLITE CELL; ANIMAL; CELL GROWTH; CELL NUCLEUS; CHICK EMBRYO; CYTOLOGY; GENETIC TRANSFECTION; GENETICS; HORSE; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL GROWTH PROCESSES; CELL NUCLEUS; CHICK EMBRYO; HORSES; MICE; PHOSPHOPROTEINS; PROTEIN-SERINE-THREONINE KINASES; SATELLITE CELLS, SKELETAL MUSCLE; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 84871907591     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.109546     Document Type: Article

References (72)

1. Alfaro, L. A., Dick, S. A., Siegel, A. L., Anonuevo, A. S., McNagny, K. M., Megeney, L. A., Cornelison, D. D. and Rossi, F. M. (2011). CD34 promotes satellite cell motility and entry into proliferation to facilitate efficient skeletal muscle regeneration. Stem Cells 29, 2030-2041.
2. Angus, L., Moleirinho, S., Herron, L., Sinha, A., Zhang, X., Niestrata, M., Dholakia, K., Prystowsky, M. B., Harvey, K. F., Reynolds, P. A. et al. (2012). Willin/FRMD6 expression activates the Hippo signaling pathway kinases in mammals and antagonizes oncogenic YAP. Oncogene 31, 238-250.
3. Beauchamp, J. R., Heslop, L., Yu, D. S., Tajbakhsh, S., Kelly, R. G., Wernig, A., Buckingham, M. E., Partridge, T. A. and Zammit, P. S. (2000). Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells. J. Cell Biol. 151, 1221-1234.
4. Benhaddou, A., Keime, C., Ye, T., Morlon, A., Michel, I., Jost, B., Mengus, G. and Davidson, I. (2012). Transcription factor TEAD4 regulates expression of myogenin and the unfolded protein response genes during C2C12 cell differentiation. Cell Death Differ. 19, 220-231.
5. Camargo, F. D., Gokhale, S., Johnnidis, J. B., Fu, D., Bell, G. W., Jaenisch, R. and Brummelkamp, T. R. (2007). YAP1 increases organ size and expands undifferentiated progenitor cells. Curr. Biol. 17, 2054-2060.
6. Cao, X., Pfaff, S. L. and Gage, F. H. (2008). YAP regulates neural progenitor cell number via the TEA domain transcription factor. Genes Dev. 22, 3320-3334.
7. Cao, Y., Yao, Z., Sarkar, D., Lawrence, M., Sanchez, G. J., Parker, M. H., MacQuarrie, K. L., Davison, J., Morgan, M. T., Ruzzo, W. L. et al. (2010). Genome-wide MyoD binding in skeletal muscle cells: a potential for broad cellular reprogramming. Dev. Cell 18, 662-674.
8. Cash, J. N., Angerman, E. B., Kattamuri, C., Nolan, K., Zhao, H., Sidis, Y., Keutmann, H. T. and Thompson, T. B. (2012). Structure of myostatin?follistatinlike 3: N-terminal domains of follistatin-type molecules exhibit alternate modes of binding. J. Biol. Chem. 287, 1043-1053.
9. Cerletti, M., Jurga, S., Witczak, C. A., Hirshman, M. F., Shadrach, J. L., Goodyear, L. J. and Wagers, A. J. (2008). Highly efficient, functional engraftment of skeletal muscle stem cells in dystrophic muscles. Cell 134, 37-47.
10. Chan, S. W., Lim, C. J., Chong, Y. F., Pobbati, A. V., Huang, C. and Hong, W. (2011). Hippo pathway-independent restriction of TAZ and YAP by angiomotin. J. Biol. Chem. 286, 7018-7026.
11. Collins, C. A. and Zammit, P. S. (2009). Isolation and grafting of single muscle fibres. Methods Mol. Biol. 482, 319-330.
12. Collins, C. A., Olsen, I., Zammit, P. S., Heslop, L., Petrie, A., Partridge, T. A. and Morgan, J. E. (2005). Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell 122, 289-301.
13. Das Thakur, M., Feng, Y., Jagannathan, R., Seppa, M. J., Skeath, J. B. and Longmore, G. D. (2010). Ajuba LIM proteins are negative regulators of the Hippo signaling pathway. Curr. Biol. 20, 657-662.
14. Dong, J., Feldmann, G., Huang, J., Wu, S., Zhang, N., Comerford, S. A., Gayyed, M. F., Anders, R. A., Maitra, A. and Pan, D. (2007). Elucidation of a universal sizecontrol mechanism in Drosophila and mammals. Cell 130, 1120-1133.
15. Dupont, S., Morsut, L., Aragona, M., Enzo, E., Giulitti, S., Cordenonsi, M., Zanconato, F., Le Digabel, J., Forcato, M., Bicciato, S. et al. (2011). Role of YAP/ TAZ in mechanotransduction. Nature 474, 179-183.
16. Foletta, V. C., Prior, M. J., Stupka, N., Carey, K., Segal, D. H., Jones, S., Swinton, C., Martin, S., Cameron-Smith, D. and Walder, K. R. (2009). NDRG2, a novel regulator of myoblast proliferation, is regulated by anabolic and catabolic factors. J. Physiol. 587, 1619-1634.
17. Gharaibeh, B., Lu, A., Tebbets, J., Zheng, B., Feduska, J., Crisan, M., Péault, B., Cummins, J. and Huard, J. (2008). Isolation of a slowly adhering cell fraction containing stem cells from murine skeletal muscle by the preplate technique. Nat. Protoc. 3, 1501-1509.
18. Gnocchi, V. F., White, R. B., Ono, Y., Ellis, J. A. and Zammit, P. S. (2009). Further characterisation of the molecular signature of quiescent and activated mouse muscle satellite cells. PLoS ONE 4, e5205.
19. Halder, G., Polaczyk, P., Kraus, M. E., Hudson, A., Kim, J., Laughon, A. and Carroll, S. (1998). The Vestigial and Scalloped proteins act together to directly regulate wing-specific gene expression in Drosophila. Genes Dev. 12, 3900-3909.
20. Harvey, K. and Tapon, N. (2007). The Salvador-Warts-Hippo pathway - an emerging tumour-suppressor network. Nat. Rev. Cancer 7, 182-191.
21. Heallen, T., Zhang, M., Wang, J., Bonilla-Claudio, M., Klysik, E., Johnson, R. L. and Martin, J. F. (2011). Hippo pathway inhibits Wnt signaling to restrain cardiomyocyte proliferation and heart size. Science 332, 458-461.
22. Heintzman, N. D., Hon, G. C., Hawkins, R. D., Kheradpour, P., Stark, A., Harp, L. F., Ye, Z., Lee, L. K., Stuart, R. K., Ching, C. W. et al. (2009). Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459, 108-112.
23. Iovino, S., Oriente, F., Botta, G., Cabaro, S., Iovane, V., Paciello, O., Viggiano, D., Perruolo, G., Formisano, P. and Beguinot, F. (2012). PED/PEA-15 induces autophagy and mediates TGF-beta1 effect on muscle cell differentiation. Cell Death Differ. 19, 1127-1138.
24. Johnston, A. P., Baker, J., Bellamy, L. M., McKay, B. R., De Lisio, M. and Parise, G. (2010). Regulation of muscle satellite cell activation and chemotaxis by angiotensin II. PLoS ONE 5, e15212.
25. Kassar-Duchossoy, L., Gayraud-Morel, B., Gomes, D., Rocancourt, D., Buckingham, M., Shinin, V. and Tajbakhsh, S. (2004). Mrf4 determines skeletal muscle identity in Myf5:Myod double-mutant mice. Nature 431, 466-471.
26. Lavasani, M., Lu, A., Peng, H., Cummins, J. and Huard, J. (2006). Nerve growth factor improves the muscle regeneration capacity of muscle stem cells in dystrophic muscle. Hum. Gene Ther. 17, 180-192.
27. Lee, K. P., Lee, J. H., Kim, T. S., Kim, T. H., Park, H. D., Byun, J. S., Kim, M. C., Jeong, W. I., Calvisi, D. F., Kim, J. M. et al. (2010). The Hippo-Salvador pathway restrains hepatic oval cell proliferation, liver size, and liver tumorigenesis. Proc. Natl. Acad. Sci. USA 107, 8248-8253.
28. Lee, K. S., Smith, K., Amieux, P. S. and Wang, E. H. (2008). MBNL3/CHCR prevents myogenic differentiation by inhibiting MyoD-dependent gene transcription. Differentiation 76, 299-309.
29. Lempiäinen, H. and Shore, D. (2009). Growth control and ribosome biogenesis. Curr. Opin. Cell Biol. 21, 855-863.
30. Lepper, C., Partridge, T. A. and Fan, C. M. (2011). An absolute requirement for Pax7- positive satellite cells in acute injury-induced skeletal muscle regeneration. Development 138, 3639-3646.
31. Lian, I., Kim, J., Okazawa, H., Zhao, J., Zhao, B., Yu, J., Chinnaiyan, A., Israel, M. A., Goldstein, L. S., Abujarour, R. et al. (2010). The role of YAP transcription coactivator in regulating stem cell self-renewal and differentiation. Genes Dev. 24, 1106-1118.
32. Mahoney, W. M., Jr, Hong, J. H., Yaffe, M. B. and Farrance, I. K. (2005). The transcriptional co-activator TAZ interacts differentially with transcriptional enhancer factor-1 (TEF-1) family members. Biochem. J. 388, 217-225.
33. Mauro, A. (1961). Satellite cell of skeletal muscle fibers. J. Biophys. Biochem. Cytol. 9, 493-495.
34. Maeda, T., Chapman, D. L. and Stewart, A. F. (2002). Mammalian vestigial-like 2, a cofactor of TEF-1 and MEF2 transcription factors that promotes skeletal muscle differentiation. J. Biol. Chem. 277, 48889-48898.
35. McCarthy, J. J., Mula, J., Miyazaki, M., Erfani, R., Garrison, K., Farooqui, A. B., Srikuea, R., Lawson, B. A., Grimes, B., Keller, C. et al. (2011). Effective fiber hypertrophy in satellite cell-depleted skeletal muscle. Development 138, 3657-3666.
36. McCroskery, S., Thomas, M., Maxwell, L., Sharma, M. and Kambadur, R. (2003). Myostatin negatively regulates satellite cell activation and self-renewal. J. Cell Biol. 162, 1135-1147.
37. Mielcarek, M., Günther, S., Krüger, M. and Braun, T. (2002). VITO-1, a novel vestigial related protein is predominantly expressed in the skeletal muscle lineage. Mech. Dev. 119 Suppl. 1:, S269-S274.
38. Mizuno, T., Murakami, H., Fujii, M., Ishiguro, F., Tanaka, I., Kondo, Y., Akatsuka, S., Toyokuni, S., Yokoi, K., Osada, H. et al. (2012). YAP induces malignant mesothelioma cell proliferation by upregulating transcription of cell cycle-promoting genes. Oncogene 31, 5117-5122.
39. Mourikis, P., Sambasivan, R., Castel, D., Rocheteau, P., Bizzarro, V. and Tajbakhsh, S. (2012). A critical requirement for notch signaling in maintenance of the quiescent skeletal muscle stem cell state. Stem Cells 30, 243-252.
40. Oka, T., Schmitt, A. P. and Sudol, M. (2012). Opposing roles of angiomotin-like-1 and zona occludens-2 on pro-apoptotic function of YAP. Oncogene 31, 128-134.
41. Ono, Y., Calhabeu, F., Morgan, J. E., Katagiri, T., Amthor, H. and Zammit, P. S. (2011). BMP signalling permits population expansion by preventing premature myogenic differentiation in muscle satellite cells. Cell Death Differ. 18, 222-234.
42. Otto, A., Schmidt, C., Luke, G., Allen, S., Valasek, P., Muntoni, F., Lawrence-Watt, D. and Patel, K. (2008). Canonical Wnt signalling induces satellite-cell proliferation during adult skeletal muscle regeneration. J. Cell Sci. 121, 2939-2950.
43. Pallafacchina, G., François, S., Regnault, B., Czarny, B., Dive, V., Cumano, A., Montarras, D. and Buckingham, M. (2010). An adult tissue-specific stem cell in its niche: a gene profiling analysis of in vivo quiescent and activated muscle satellite cells. Stem Cell Res. 4, 77-91.
44. Pan, D. (2010). The hippo signaling pathway in development and cancer. Dev. Cell 19, 491-505.
45. Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45.
46. Pobbati, A. V., Chan, S. W., Lee, I., Song, H. and Hong, W. (2012). Structural and functional similarity between the Vgll1-TEAD and the YAP-TEAD complexes. Structure 20, 1135-1140.
47. Qiu, H., Wang, F., Liu, C., Xu, X. and Liu, B. (2011). TEAD1-dependent expression of the FoxO3a gene in mouse skeletal muscle. BMC Mol. Biol. 12, 1.
48. Ramalho-Santos, M., Yoon, S., Matsuzaki, Y., Mulligan, R. C. and Melton, D. A. (2002). "Stemness": transcriptional profiling of embryonic and adult stem cells. Science 298, 597-600.
49. Relaix, F. and Zammit, P. S. (2012). Satellite cells are essential for skeletal muscle regeneration: the cell on the edge returns centre stage. Development 139, 2845-2856.
50. Ribas, R., Moncaut, N., Siligan, C., Taylor, K., Cross, J. W., Rigby, P. W. and Carvajal, J. J. (2011). Members of the TEAD family of transcription factors regulate the expression of Myf5 in ventral somitic compartments. Dev. Biol. 355, 372-380.
51. Sacco, A., Doyonnas, R., Kraft, P., Vitorovic, S. and Blau, H. M. (2008). Self-renewal and expansion of single transplanted muscle stem cells. Nature 456, 502-506.
52. Sandri, M., Sandri, C., Gilbert, A., Skurk, C., Calabria, E., Picard, A., Walsh, K., Schiaffino, S., Lecker, S. H. and Goldberg, A. L. (2004). Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117, 399-412.
53. Saucedo, L. J. and Edgar, B. A. (2007). Filling out the Hippo pathway. Nat. Rev. Mol. Cell Biol. 8, 613-621.
54. Scharner, J. and Zammit, P. S. (2011). The muscle satellite cell at 50: the formative years. Skelet. Muscle 1, 28.
55. Schlegelmilch, K., Mohseni, M., Kirak, O., Pruszak, J., Rodriguez, J. R., Zhou, D., Kreger, B. T., Vasioukhin, V., Avruch, J., Brummelkamp, T. R. et al. (2011). Yap1 acts downstream of a-catenin to control epidermal proliferation. Cell 144, 782-795.
56. Sudol, M. and Harvey, K. F. (2010). Modularity in the Hippo signaling pathway. Trends Biochem. Sci. 35, 627-633.
57. Sun, G., Haginoya, K., Wu, Y., Chiba, Y., Nakanishi, T., Onuma, A., Sato, Y., Takigawa, M., Iinuma, K. and Tsuchiya, S. (2008). Connective tissue growth factor is overexpressed in muscles of human muscular dystrophy. J. Neurol. Sci. 267, 48-56.
58. Tatsumi, R., Anderson, J. E., Nevoret, C. J., Halevy, O. and Allen, R. E. (1998). HGF/SF is present in normal adult skeletal muscle and is capable of activating satellite cells. Dev. Biol. 194, 114-128.
59. Tintignac, L. A., Lagirand, J., Batonnet, S., Sirri, V., Leibovitch, M. P. and Leibovitch, S. A. (2005). Degradation of MyoD mediated by the SCF (MAFbx) ubiquitin ligase. J. Biol. Chem. 280, 2847-2856.
60. Tomczak, K. K., Marinescu, V. D., Ramoni, M. F., Sanoudou, D., Montanaro, F., Han, M., Kunkel, L. M., Kohane, I. S. and Beggs, A. H. (2004). Expression profiling and identification of novel genes involved in myogenic differentiation. FASEB J. 18, 403-405.
61. Vassilev, A., Kaneko, K. J., Shu, H., Zhao, Y. and DePamphilis, M. L. (2001). TEAD/TEF transcription factors utilize the activation domain of YAP65, a Src/Yesassociated protein localized in the cytoplasm. Genes Dev. 15, 1229-1241.
62. Watt, K. I., Judson, R., Medlow, P., Reid, K., Kurth, T. B., Burniston, J. G., Ratkevicius, A., De Bari, C. and Wackerhage, H. (2010). Yap is a novel regulator of C2C12 myogenesis. Biochem. Biophys. Res. Commun. 393, 619-624.
63. Yamada, M., Tatsumi, R., Yamanouchi, K., Hosoyama, T., Shiratsuchi, S., Sato, A., Mizunoya, W., Ikeuchi, Y., Furuse, M. and Allen, R. E. (2010). High concentrations of HGF inhibit skeletal muscle satellite cell proliferation in vitro by inducing expression of myostatin: a possible mechanism for reestablishing satellite cell quiescence in vivo. Am. J. Physiol. Cell Physiol. 298, C465-C476.
64. Yoshida, T. (2008). MCAT elements and the TEF-1 family of transcription factors in muscle development and disease. Arterioscler. Thromb. Vasc. Biol. 28, 8-17.
65. Yoshihama, Y., Chida, K. and Ohno, S. (2012). The KIBRA-aPKC connection: A potential regulator of membrane trafficking and cell polarity. Commun. Integr. Biol. 5, 146-151.
66. Yu, F. X., Zhao, B., Panupinthu, N., Jewell, J. L., Lian, I., Wang, L. H., Zhao, J., Yuan, H., Tumaneng, K., Li, H. et al. (2012). Regulation of the Hippo-YAP pathway by G-protein-coupled receptor signaling. Cell 150, 780-791.
67. Zammit, P. S., Golding, J. P., Nagata, Y., Hudon, V., Partridge, T. A. and Beauchamp, J. R. (2004). Muscle satellite cells adopt divergent fates: a mechanism for self-renewal? J. Cell Biol. 166, 347-357.
68. Zammit, P. S., Relaix, F., Nagata, Y., Ruiz, A. P., Collins, C. A., Partridge, T. A. and Beauchamp, J. R. (2006). Pax7 and myogenic progression in skeletal muscle satellite cells. J. Cell Sci. 119, 1824-1832.
69. Zhang, H., Deo, M., Thompson, R. C., Uhler, M. D. and Turner, D. L. (2012). Negative regulation of Yap during neuronal differentiation. Dev. Biol. 361, 103-115.
70. Zhao, B., Ye, X., Yu, J., Li, L., Li, W., Li, S., Yu, J., Lin, J. D., Wang, C. Y., Chinnaiyan, A. M. et al. (2008). TEAD mediates YAP-dependent gene induction and growth control. Genes Dev. 22, 1962-1971.
71. Zhao, B., Li, L., Tumaneng, K., Wang, C. Y. and Guan, K. L. (2010). A coordinated phosphorylation by Lats and CK1 regulates YAP stability through SCF(beta-TRCP). Genes Dev. 24, 72-85.
72. Zhao, B., Li, L., Lu, Q., Wang, L. H., Liu, C. Y., Lei, Q. and Guan, K. L. (2011). Angiomotin is a novel Hippo pathway component that inhibits YAP oncoprotein. Genes Dev. 25, 51-63.