An FAK-YAP-mTOR Signaling Axis Regulates Stem Cell-Based Tissue Renewal in Mice

Cell Stem Cell

Volumn 21, Issue 1, 2017, Pages 91-106.e6

  Hu, Jimmy Kuang Hsien ^a   Du, Wei ^a,b   Shelton, Samuel J ^a,c   Oldham, Michael C ^a,c   DiPersio, C Michael ^d   Klein, Ophir D ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SICHUAN UNIVERSITY   (China)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d ALBANY MEDICAL COLLEGE   (United States)

Author keywords

adult stem cells; CDC42; epithelium; FAK; ITGA3; PP1A; TAZ; tooth; YAP

Indexed keywords

ALPHA3 INTEGRIN; FOCAL ADHESION KINASE; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHOPROTEIN PHOSPHATASE 1; PHOSPHOPROTEIN PHOSPHATASE 1A; PROTEIN; PROTEIN CDC42; PROTEIN TAZ; PROTEIN YAP; RHEB PROTEIN; UNCLASSIFIED DRUG; FOCAL ADHESION KINASE 1; MTOR PROTEIN, MOUSE; PHOSPHOPROTEIN; PTK2 PROTEIN, MOUSE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TARGET OF RAPAMYCIN KINASE; YAP PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL NUCLEUS; CELL PROLIFERATION; CELL SELF-RENEWAL; CONTROLLED STUDY; CYTOPLASM; EPITHELIUM; HYPERPLASIA; INCISOR; MODEL; MOUSE; MTOR SIGNALING; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; STEM CELL; STEM CELL EXPANSION; ANIMAL; CYTOLOGY; GENETICS; METABOLISM; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; FOCAL ADHESION KINASE 1; INCISOR; MICE; MICE, TRANSGENIC; PHOSPHOPROTEINS; SIGNAL TRANSDUCTION; STEM CELLS; TOR SERINE-THREONINE KINASES;

EID: 85018187888     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2017.03.023     Document Type: Article

References (78)

1. Aggarwal, A., Al-Rohil, R.N., Batra, A., Feustel, P.J., Jones, D.M., DiPersio, C.M., Expression of integrin α3β1 and cyclooxygenase-2 (COX2) are positively correlated in human breast cancer. BMC Cancer, 14, 2014, 459.
2. Bai, H., Zhang, N., Xu, Y., Chen, Q., Khan, M., Potter, J.J., Nayar, S.K., Cornish, T., Alpini, G., Bronk, S., et al. Yes-associated protein regulates the hepatic response after bile duct ligation. Hepatology 56 (2012), 1097–1107.
3. Baldi, P., Long, A.D., A Bayesian framework for the analysis of microarray expression data: regularized t -test and statistical inferences of gene changes. Bioinformatics 17 (2001), 509–519.
4. Beggs, H.E., Schahin-Reed, D., Zang, K., Goebbels, S., Nave, K.A., Gorski, J., Jones, K.R., Sretavan, D., Reichardt, L.F., FAK deficiency in cells contributing to the basal lamina results in cortical abnormalities resembling congenital muscular dystrophies. Neuron 40 (2003), 501–514.
5. Benjamini, Y., Hochberg, Y., Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Series B (Methodological) 57 (1995), 289–300.
6. Biehs, B., Hu, J.K., Strauli, N.B., Sangiorgi, E., Jung, H., Heber, R.P., Ho, S., Goodwin, A.F., Dasen, J.S., Capecchi, M.R., Klein, O.D., BMI1 represses Ink4a/Arf and Hox genes to regulate stem cells in the rodent incisor. Nat. Cell Biol. 15 (2013), 846–852.
7. Cai, J., Zhang, N., Zheng, Y., de Wilde, R.F., Maitra, A., Pan, D., The Hippo signaling pathway restricts the oncogenic potential of an intestinal regeneration program. Genes Dev. 24 (2010), 2383–2388.
8. Camargo, F.D., Gokhale, S., Johnnidis, J.B., Fu, D., Bell, G.W., Jaenisch, R., Brummelkamp, T.R., YAP1 increases organ size and expands undifferentiated progenitor cells. Curr. Biol. 17 (2007), 2054–2060.
9. Chen, T., Heller, E., Beronja, S., Oshimori, N., Stokes, N., Fuchs, E., An RNA interference screen uncovers a new molecule in stem cell self-renewal and long-term regeneration. Nature 485 (2012), 104–108.
10. Chen, Q., Zhang, N., Gray, R.S., Li, H., Ewald, A.J., Zahnow, C.A., Pan, D., A temporal requirement for Hippo signaling in mammary gland differentiation, growth, and tumorigenesis. Genes Dev. 28 (2014), 432–437.
11. Chen, Q., Zhang, N., Xie, R., Wang, W., Cai, J., Choi, K.-S., David, K.K., Huang, B., Yabuta, N., Nojima, H., et al. Homeostatic control of Hippo signaling activity revealed by an endogenous activating mutation in YAP. Genes Dev. 29 (2015), 1285–1297.
12. Damljanović, V., Lagerholm, B.C., Jacobson, K., Bulk and micropatterned conjugation of extracellular matrix proteins to characterized polyacrylamide substrates for cell mechanotransduction assays. Biotechniques 39 (2005), 847–851.
13. Dassule, H.R., Lewis, P., Bei, M., Maas, R., McMahon, A.P., Sonic hedgehog regulates growth and morphogenesis of the tooth. Development 127 (2000), 4775–4785.
14. Dupont, S., Morsut, L., Aragona, M., Enzo, E., Giulitti, S., Cordenonsi, M., Zanconato, F., Le Digabel, J., Forcato, M., Bicciato, S., et al. Role of YAP/TAZ in mechanotransduction. Nature 474 (2011), 179–183.
15. Elbediwy, A., Vincent-Mistiaen, Z.I., Spencer-Dene, B., Stone, R.K., Boeing, S., Wculek, S.K., Cordero, J., Tan, E.H., Ridgway, R., Brunton, V.G., et al. Integrin signalling regulates YAP and TAZ to control skin homeostasis. Development 143 (2016), 1674–1687.
16. Glogauer, M., Marchal, C.C., Zhu, F., Worku, A., Clausen, B.E., Foerster, I., Marks, P., Downey, G.P., Dinauer, M., Kwiatkowski, D.J., Rac1 deletion in mouse neutrophils has selective effects on neutrophil functions. J. Immunol. 170 (2003), 5652–5657.
17. Hansen, C.G., Ng, Y.L.D., Lam, W.-L.M., Plouffe, S.W., Guan, K.-L., The Hippo pathway effectors YAP and TAZ promote cell growth by modulating amino acid signaling to mTORC1. Cell Res. 25 (2015), 1299–1313.
18. Hara, K., Maruki, Y., Long, X., Yoshino, K., Oshiro, N., Hidayat, S., Tokunaga, C., Avruch, J., Yonezawa, K., Raptor, a binding partner of target of rapamycin (TOR), mediates TOR action. Cell 110 (2002), 177–189.
19. Harada, H., Kettunen, P., Jung, H.S., Mustonen, T., Wang, Y.A., Thesleff, I., Localization of putative stem cells in dental epithelium and their association with Notch and FGF signaling. J. Cell Biol. 147 (1999), 105–120.
20. Hay, N., Sonenberg, N., Upstream and downstream of mTOR. Genes Dev. 18 (2004), 1926–1945.
21. Heallen, T., Zhang, M., Wang, J., Bonilla-Claudio, M., Klysik, E., Johnson, R.L., Martin, J.F., Hippo pathway inhibits Wnt signaling to restrain cardiomyocyte proliferation and heart size. Science 332 (2011), 458–461.
22. Hergovich, A., The Roles of NDR Protein Kinases in Hippo Signalling. Genes (Basel), 7, 2016, E21.
23. Hua, G., Lv, X., He, C., Remmenga, S.W., Rodabough, K.J., Dong, J., Yang, L., Lele, S.M., Yang, P., Zhou, J., et al. YAP induces high-grade serous carcinoma in fallopian tube secretory epithelial cells. Oncogene 35 (2016), 2247–2265.
24. Huang, Z., Zhang, L., Chen, Y., Zhang, H., Zhang, Q., Li, R., Ma, J., Li, Z., Yu, C., Lai, Y., et al. Cdc42 deficiency induces podocyte apoptosis by inhibiting the Nwasp/stress fibers/YAP pathway. Cell Death Dis., 7, 2016, e2142.
25. Jackson, B., Peyrollier, K., Pedersen, E., Basse, A., Karlsson, R., Wang, Z., Lefever, T., Ochsenbein, A.M., Schmidt, G., Aktories, K., et al. RhoA is dispensable for skin development, but crucial for contraction and directed migration of keratinocytes. Mol. Biol. Cell 22 (2011), 593–605.
26. Johnson, W.E., Li, C., Rabinovic, A., Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics 8 (2007), 118–127.
27. Juuri, E., Saito, K., Ahtiainen, L., Seidel, K., Tummers, M., Hochedlinger, K., Klein, O.D., Thesleff, I., Michon, F., Sox2+ stem cells contribute to all epithelial lineages of the tooth via Sfrp5+ progenitors. Dev. Cell 23 (2012), 317–328.
28. Kaukua, N., Shahidi, M.K., Konstantinidou, C., Dyachuk, V., Kaucka, M., Furlan, A., An, Z., Wang, L., Hultman, I., Ährlund-Richter, L., et al. Glial origin of mesenchymal stem cells in a tooth model system. Nature 513 (2014), 551–554.
29. Kayala, M.A., Baldi, P., Cyber-T web server: differential analysis of high-throughput data. Nucleic Acids Res. 40 (2012), W553–559.
30. Klein, O.D., Lyons, D.B., Balooch, G., Marshall, G.W., Basson, M.A., Peterka, M., Boran, T., Peterkova, R., Martin, G.R., An FGF signaling loop sustains the generation of differentiated progeny from stem cells in mouse incisors. Development 135 (2008), 377–385.
31. Kobayashi, K., Takahashi, M., Matsushita, N., Miyazaki, J., Koike, M., Yaginuma, H., Osumi, N., Kaibuchi, K., Kobayashi, K., Survival of developing motor neurons mediated by Rho GTPase signaling pathway through Rho-kinase. J. Neurosci. 24 (2004), 3480–3488.
32. Lange, A.W., Sridharan, A., Xu, Y., Stripp, B.R., Perl, A.-K., Whitsett, J.A., Hippo/Yap signaling controls epithelial progenitor cell proliferation and differentiation in the embryonic and adult lung. J. Mol. Cell Biol. 7 (2015), 35–47.
33. Laplante, M., Sabatini, D.M., mTOR signaling at a glance. J. Cell Sci. 122 (2009), 3589–3594.
34. Levy, D., Adamovich, Y., Reuven, N., Shaul, Y., Yap1 phosphorylation by c-Abl is a critical step in selective activation of proapoptotic genes in response to DNA damage. Mol. Cell 29 (2008), 350–361.
35. Li, M., Indra, A.K., Warot, X., Brocard, J., Messaddeq, N., Kato, S., Metzger, D., Chambon, P., Skin abnormalities generated by temporally controlled RXRalpha mutations in mouse epidermis. Nature 407 (2000), 633–636.
36. Li, C.-Y., Cha, W., Luder, H.-U., Charles, R.-P., McMahon, M., Mitsiadis, T.A., Klein, O.D., E-cadherin regulates the behavior and fate of epithelial stem cells and their progeny in the mouse incisor. Dev. Biol. 366 (2012), 357–366.
37. Li, P., Silvis, M.R., Honaker, Y., Lien, W.-H., Arron, S.T., Vasioukhin, V., αE-catenin inhibits a Src-YAP1 oncogenic module that couples tyrosine kinases and the effector of Hippo signaling pathway. Genes Dev. 30 (2016), 798–811.
38. Livak, K.J., Schmittgen, T.D., Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25 (2001), 402–408.
39. Lu, L., Li, Y., Kim, S.M., Bossuyt, W., Liu, P., Qiu, Q., Wang, Y., Halder, G., Finegold, M.J., Lee, J.-S., Johnson, R.L., Hippo signaling is a potent in vivo growth and tumor suppressor pathway in the mammalian liver. Proc. Natl. Acad. Sci. USA 107 (2010), 1437–1442.
40. Makita, R., Uchijima, Y., Nishiyama, K., Amano, T., Chen, Q., Takeuchi, T., Mitani, A., Nagase, T., Yatomi, Y., Aburatani, H., et al. Multiple renal cysts, urinary concentration defects, and pulmonary emphysematous changes in mice lacking TAZ. Am. J. Physiol. Renal Physiol. 294 (2008), F542–F553.
41. McLean, G.W., Carragher, N.O., Avizienyte, E., Evans, J., Brunton, V.G., Frame, M.C., The role of focal-adhesion kinase in cancer - a new therapeutic opportunity. Nat. Rev. Cancer 5 (2005), 505–515.
42. Meng, Z., Moroishi, T., Mottier-Pavie, V., Plouffe, S.W., Hansen, C.G., Hong, A.W., Park, H.W., Mo, J.-S., Lu, W., Lu, S., et al. MAP4K family kinases act in parallel to MST1/2 to activate LATS1/2 in the Hippo pathway. Nat. Commun., 6, 2015, 8357.
43. Mitchell, K., Szekeres, C., Milano, V., Svenson, K.B., Nilsen-Hamilton, M., Kreidberg, J.A., DiPersio, C.M., Alpha3beta1 integrin in epidermis promotes wound angiogenesis and keratinocyte-to-endothelial-cell crosstalk through the induction of MRP3. J. Cell Sci. 122 (2009), 1778–1787.
44. Mo, J.-S., Meng, Z., Kim, Y.C., Park, H.W., Hansen, C.G., Kim, S., Lim, D.-S., Guan, K.-L., Cellular energy stress induces AMPK-mediated regulation of YAP and the Hippo pathway. Nat. Cell Biol. 17 (2015), 500–510.
45. Moroishi, T., Park, H.W., Qin, B., Chen, Q., Meng, Z., Plouffe, S.W., Taniguchi, K., Yu, F.-X., Karin, M., Pan, D., Guan, K.L., A YAP/TAZ-induced feedback mechanism regulates Hippo pathway homeostasis. Genes Dev. 29 (2015), 1271–1284.
46. Muzumdar, M.D., Tasic, B., Miyamichi, K., Li, L., Luo, L., A global double-fluorescent Cre reporter mouse. Genesis 45 (2007), 593–605.
47. Oldham, M.C., Langfelder, P., Horvath, S., Network methods for describing sample relationships in genomic datasets: application to Huntington's disease. BMC Syst. Biol., 6, 2012, 63.
48. Parsa, S., Kuremoto, K., Seidel, K., Tabatabai, R., Mackenzie, B., Yamaza, T., Akiyama, K., Branch, J., Koh, C.J., Al Alam, D., et al. Signaling by FGFR2b controls the regenerative capacity of adult mouse incisors. Development 137 (2010), 3743–3752.
49. Porazinski, S., Wang, H., Asaoka, Y., Behrndt, M., Miyamoto, T., Morita, H., Hata, S., Sasaki, T., Krens, S.F.G., Osada, Y., et al. YAP is essential for tissue tension to ensure vertebrate 3D body shape. Nature 521 (2015), 217–221.
50. Prowse, A.B.J., Chong, F., Gray, P.P., Munro, T.P., Stem cell integrins: implications for ex-vivo culture and cellular therapies. Stem Cell Res. (Amst.) 6 (2011), 1–12.
51. Qi, Q., Li, D.Y., Luo, H.R., Guan, K.-L., Ye, K., Netrin-1 exerts oncogenic activities through enhancing Yes-associated protein stability. Proc. Natl. Acad. Sci. USA 112 (2015), 7255–7260.
52. Raghavan, S., Bauer, C., Mundschau, G., Li, Q., Fuchs, E., Conditional ablation of beta1 integrin in skin. Severe defects in epidermal proliferation, basement membrane formation, and hair follicle invagination. J. Cell Biol. 150 (2000), 1149–1160.
53. Reginensi, A., Scott, R.P., Gregorieff, A., Bagherie-Lachidan, M., Chung, C., Lim, D.-S., Pawson, T., Wrana, J., McNeill, H., Yap- and Cdc42-dependent nephrogenesis and morphogenesis during mouse kidney development. PLoS Genet., 9, 2013, e1003380.
54. Sachs, N., Secades, P., van Hulst, L., Kreft, M., Song, J.-Y., Sonnenberg, A., Loss of integrin α3 prevents skin tumor formation by promoting epidermal turnover and depletion of slow-cycling cells. Proc. Natl. Acad. Sci. USA 109 (2012), 21468–21473.
55. Schlegelmilch, K., Mohseni, M., Kirak, O., Pruszak, J., Rodriguez, J.R., Zhou, D., Kreger, B.T., Vasioukhin, V., Avruch, J., Brummelkamp, T.R., Camargo, F.D., Yap1 acts downstream of α-catenin to control epidermal proliferation. Cell 144 (2011), 782–795.
56. Seguin, L., Desgrosellier, J.S., Weis, S.M., Cheresh, D.A., Integrins and cancer: regulators of cancer stemness, metastasis, and drug resistance. Trends Cell Biol. 25 (2015), 234–240.
57. Seidel, K., Ahn, C.P., Lyons, D., Nee, A., Ting, K., Brownell, I., Cao, T., Carano, R.A.D., Curran, T., Schober, M., et al. Hedgehog signaling regulates the generation of ameloblast progenitors in the continuously growing mouse incisor. Development 137 (2010), 3753–3761.
58. Sengupta, S., Peterson, T.R., Laplante, M., Oh, S., Sabatini, D.M., mTORC1 controls fasting-induced ketogenesis and its modulation by ageing. Nature 468 (2010), 1100–1104.
59. Suomalainen, M., Thesleff, I., Patterns of Wnt pathway activity in the mouse incisor indicate absence of Wnt/beta-catenin signaling in the epithelial stem cells. Dev. Dyn. 239 (2010), 364–372.
60. Szymaniak, A.D., Mahoney, J.E., Cardoso, W.V., Varelas, X., Crumbs3-Mediated Polarity Directs Airway Epithelial Cell Fate through the Hippo Pathway Effector Yap. Dev. Cell 34 (2015), 283–296.
61. Tang, Y., Rowe, R.G., Botvinick, E.L., Kurup, A., Putnam, A.J., Seiki, M., Weaver, V.M., Keller, E.T., Goldstein, S., Dai, J., et al. MT1-MMP-dependent control of skeletal stem cell commitment via a β1-integrin/YAP/TAZ signaling axis. Dev. Cell 25 (2013), 402–416.
62. Tumaneng, K., Schlegelmilch, K., Russell, R.C., Yimlamai, D., Basnet, H., Mahadevan, N., Fitamant, J., Bardeesy, N., Camargo, F.D., Guan, K.-L., YAP mediates crosstalk between the Hippo and PI(3)K–TOR pathways by suppressing PTEN via miR-29. Nat. Cell Biol. 14 (2012), 1322–1329.
63. Varelas, X., Miller, B.W., Sopko, R., Song, S., Gregorieff, A., Fellouse, F.A., Sakuma, R., Pawson, T., Hunziker, W., McNeill, H., et al. The Hippo pathway regulates Wnt/β-catenin signaling. Dev. Cell 18 (2010), 579–591.
64. Wabik, A., Jones, P.H., Switching roles: the functional plasticity of adult tissue stem cells. EMBO J. 34 (2015), 1164–1179.
65. Waikel, R.L., Kawachi, Y., Waikel, P.A., Wang, X.-J., Roop, D.R., Deregulated expression of c-Myc depletes epidermal stem cells. Nat. Genet. 28 (2001), 165–168.
66. Wang, J., Xiao, Y., Hsu, C.-W., Martinez-Traverso, I.M., Zhang, M., Bai, Y., Ishii, M., Maxson, R.E., Olson, E.N., Dickinson, M.E., et al. Yap and Taz play a crucial role in neural crest-derived craniofacial development. Development 143 (2016), 504–515.
67. White, A.C., Khuu, J.K., Dang, C.Y., Hu, J., Tran, K.V., Liu, A., Gomez, S., Zhang, Z., Yi, R., Scumpia, P., et al. Stem cell quiescence acts as a tumour suppressor in squamous tumours. Nat. Cell Biol. 16 (2014), 99–107.
68. Wu, X., Quondamatteo, F., Lefever, T., Czuchra, A., Meyer, H., Chrostek, A., Paus, R., Langbein, L., Brakebusch, C., Cdc42 controls progenitor cell differentiation and beta-catenin turnover in skin. Genes Dev. 20 (2006), 571–585.
69. Xin, M., Kim, Y., Sutherland, L.B., Qi, X., McAnally, J., Schwartz, R.J., Richardson, J.A., Bassel-Duby, R., Olson, E.N., Regulation of insulin-like growth factor signaling by Yap governs cardiomyocyte proliferation and embryonic heart size. Sci. Signal., 4, 2011, ra70.
70. Xin, M., Kim, Y., Sutherland, L.B., Murakami, M., Qi, X., McAnally, J., Porrello, E.R., Mahmoud, A.I., Tan, W., Shelton, J.M., et al. Hippo pathway effector Yap promotes cardiac regeneration. Proc. Natl. Acad. Sci. USA 110 (2013), 13839–13844.
71. Yilmaz, O.H., Valdez, R., Theisen, B.K., Guo, W., Ferguson, D.O., Wu, H., Morrison, S.J., Pten dependence distinguishes haematopoietic stem cells from leukaemia-initiating cells. Nature 441 (2006), 475–482.
72. 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. Regulation of the Hippo-YAP pathway by G-protein-coupled receptor signaling. Cell 150 (2012), 780–791.
73. Yu, F.-X., Zhao, B., Guan, K.-L., Hippo Pathway in Organ Size Control, Tissue Homeostasis, and Cancer. Cell 163 (2015), 811–828.
74. Zhang, H., Wang, Z., Zhang, Z., PP1α, PP1β and Wip-1 regulate H4S47 phosphorylation and deposition of histone H3 variant H3.3. Nucleic Acids Res. 41 (2013), 8085–8093.
75. Zhao, B., Wei, X., Li, W., Udan, R.S., Yang, Q., Kim, J., Xie, J., Ikenoue, T., Yu, J., Li, L., et al. Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev. 21 (2007), 2747–2761.
76. Zhao, B., Li, L., Tumaneng, K., Wang, C.-Y., Guan, K.-L., A coordinated phosphorylation by Lats and CK1 regulates YAP stability through SCF(beta-TRCP). Genes Dev. 24 (2010), 72–85.
77. Zheng, Y., Wang, W., Liu, B., Deng, H., Uster, E., Pan, D., Identification of Happyhour/MAP4K as Alternative Hpo/Mst-like Kinases in the Hippo Kinase Cascade. Dev. Cell 34 (2015), 642–655.
78. Zhou, D., Zhang, Y., Wu, H., Barry, E., Yin, Y., Lawrence, E., Dawson, D., Willis, J.E., Markowitz, S.D., Camargo, F.D., Avruch, J., Mst1 and Mst2 protein kinases restrain intestinal stem cell proliferation and colonic tumorigenesis by inhibition of Yes-associated protein (Yap) overabundance. Proc. Natl. Acad. Sci. USA 108 (2011), E1312–E1320.