Acetylation of VGLL4 Regulates Hippo-YAP Signaling and Postnatal Cardiac Growth

Developmental Cell

Volumn 39, Issue 4, 2016, Pages 466-479

  Lin, Zhiqiang ^a   Guo, Haidong ^a,b   Cao, Yuan ^a,c   Zohrabian, Sylvia ^a   Zhou, Pingzhu ^a   Ma, Qing ^a   VanDusen, Nathan ^a   Guo, Yuxuan ^a   Zhang, Jin ^a   Stevens, Sean M ^a   Liang, Feng ^d   Quan, Qimin ^d   van Gorp, Pim R ^e   Li, Amy ^f   dos Remedios, Cristobal ^f   He, Aibin ^g   Bezzerides, Vassilios J ^a   Pu, William T ^a,h  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b SHANGHAI UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

^c PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^d HARVARD UNIVERSITY   (United States)

^e LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^f UNIVERSITY OF SYDNEY   (Australia)

^g PEKING UNIVERSITY   (China)

^h HARVARD STEM CELL INSTITUTE   (United States)

Author keywords

acetylation; cardiac; cardiomyocyte; degradation; Hippo YAP pathway; necrosis; proliferation; TEAD1; VGLL4

Indexed keywords

BINDING PROTEIN; HIPPO KINASE; LYSINE; PHOSPHOTRANSFERASE; PROTEIN VGLL4; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR TEAD; TRANSCRIPTION FACTOR TEAD1; TRANSCRIPTION FACTOR YAP; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; HIPPO PROTEIN, MOUSE; PHOSPHOPROTEIN; PROTEIN BINDING; PROTEIN SERINE THREONINE KINASE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TEAD1 PROTEIN, MOUSE; VGLL4 PROTEIN, MOUSE; YAP PROTEIN, MOUSE;

ACETYLATION; ANIMAL CELL; ARTICLE; CARDIAC MUSCLE CELL; CELL DEATH; CELL PROLIFERATION; CONTROLLED STUDY; HEART DEVELOPMENT; HEART FAILURE; HEART FUNCTION; HUMAN; HUMAN TISSUE; MOUSE; NEWBORN; NONHUMAN; POSTNATAL GROWTH; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; RAT; SIGNAL TRANSDUCTION; TISSUE REGENERATION; AGING; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; GROWTH, DEVELOPMENT AND AGING; HEART; METABOLISM; PATHOLOGY; PROTEIN DOMAIN; WISTAR RAT;

ACETYLATION; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AGING; AMINO ACID SEQUENCE; ANIMALS; ANIMALS, NEWBORN; CELL PROLIFERATION; DNA-BINDING PROTEINS; HEART; HEART FAILURE; HUMANS; PHOSPHOPROTEINS; PROTEIN BINDING; PROTEIN DOMAINS; PROTEIN STABILITY; PROTEIN-SERINE-THREONINE KINASES; RATS, WISTAR; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84992143334     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2016.09.005     Document Type: Article

References (42)

1. Bai, H., Zhang, N., Xu, Y., Chen, Q., Khan, M., Potter, J.J., Nayar, S.K., Cornish, T., Alpini, G., et al. Yes-associated protein regulates the hepatic response after bile duct ligation. Hepatology 56 (2012), 1097–1107.
2. Barrett, A.J., Kembhavi, A.A., Brown, M.A., Kirschke, H., Knight, C.G., Tamai, M., Hanada, K., L-trans-Epoxysuccinyl-leucylamido(4-guanidino)butane (E-64) and its analogues as inhibitors of cysteine proteinases including cathepsins B, H and L. Biochem. J. 201 (1982), 189–198.
3. 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.
4. Chan, H.M., La Thangue, N.B., p300/CBP proteins: HATs for transcriptional bridges and scaffolds. J. Cell Sci. 114 (2001), 2363–2373.
5. Chen, H.H., Mullett, S.J., Stewart, A.F., Vgl-4, a novel member of the vestigial-like family of transcription cofactors, regulates alpha1-adrenergic activation of gene expression in cardiac myocytes. J. Biol. Chem. 279 (2004), 30800–30806.
6. de Boer, E., Rodriguez, P., Bonte, E., Krijgsveld, J., Katsantoni, E., Heck, A., Grosveld, F., Strouboulis, J., Efficient biotinylation and single-step purification of tagged transcription factors in mammalian cells and transgenic mice. Proc. Natl. Acad. Sci. USA 100 (2003), 7480–7485.
7. Del Re, D.P., Yang, Y., Nakano, N., Cho, J., Zhai, P., Yamamoto, T., Zhang, N., Yabuta, N., Nojima, H., et al. Yes-associated protein isoform 1 (Yap1) promotes cardiomyocyte survival and growth to protect against myocardial ischemic injury. J. Biol. Chem. 288 (2013), 3977–3988.
8. Dong, J., Feldmann, G., Huang, J., Wu, S., Zhang, N., Comerford, S.A., Gayyed, M.F., Anders, R.A., Maitra, A., Pan, D., Elucidation of a universal size-control mechanism in Drosophila and mammals. Cell 130 (2007), 1120–1133.
9. Dupont, S., Morsut, L., Aragona, M., Enzo, E., Giulitti, S., Cordenonsi, M., Zanconato, F., Le Digabel, J., Forcato, M., et al. Role of YAP/TAZ in mechanotransduction. Nature 474 (2011), 179–183.
10. Galli, G.G., Carrara, M., Yuan, W.-C., Valdes-Quezada, C., Gurung, B., Pepe-Mooney, B., Zhang, T., Geeven, G., Gray, N.S., et al. YAP drives growth by controlling transcriptional pause release from dynamic enhancers. Mol. Cell 60 (2015), 328–337.
11. Hata, S., Hirayama, J., Kajiho, H., Nakagawa, K., Hata, Y., Katada, T., Furutani-Seiki, M., Nishina, H., A novel acetylation cycle of transcription co-activator Yes-associated protein that is downstream of Hippo pathway is triggered in response to SN2 alkylating agents. J. Biol. Chem. 287 (2012), 22089–22098.
12. He, A., Shen, X., Ma, Q., Cao, J., von Gise, A., Zhou, P., Wang, G., Marquez, V.E., Orkin, S.H., Pu, W.T., PRC2 directly methylates GATA4 and represses its transcriptional activity. Genes Dev. 26 (2012), 37–42.
13. 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.
14. Heallen, T., Morikawa, Y., Leach, J., Tao, G., Willerson, J.T., Johnson, R.L., Martin, J.F., Hippo signaling impedes adult heart regeneration. Development 140 (2013), 4683–4690.
15. Heidenreich, P.A., Albert, N.M., Allen, L.A., Bluemke, D.A., Butler, J., Fonarow, G.C., Ikonomidis, J.S., Khavjou, O., Konstam, M.A., et al. Forecasting the impact of heart failure in the United States: a policy statement from the American Heart Association. Circ. Heart Fail. 6 (2013), 606–619.
16. Huang, J., Wu, S., Barrera, J., Matthews, K., Pan, D., The Hippo signaling pathway coordinately regulates cell proliferation and apoptosis by inactivating Yorkie, the Drosophila homolog of YAP. Cell 122 (2005), 421–434.
17. Jiao, S., Wang, H., Shi, Z., Dong, A., Zhang, W., Song, X., He, F., Wang, Y., Zhang, Z., et al. A peptide mimicking VGLL4 function acts as a YAP antagonist therapy against gastric cancer. Cancer Cell 25 (2014), 166–180.
18. Kajstura, J., Leri, A., Finato, N., Di Loreto, C., Beltrami, C.A., Anversa, P., Myocyte proliferation in end-stage cardiac failure in humans. Proc. Natl. Acad. Sci. USA 95 (1998), 8801–8805.
19. Koontz, L.M., Liu-Chittenden, Y., Yin, F., Zheng, Y., Yu, J., Huang, B., Chen, Q., Wu, S., Pan, D., The Hippo effector Yorkie controls normal tissue growth by antagonizing scalloped-mediated default repression. Dev. Cell 25 (2013), 388–401.
20. Lee, Y., Shioi, T., Kasahara, H., Jobe, S.M., Wiese, R.J., Markham, B.E., Izumo, S., The cardiac tissue-restricted homeobox protein Csx/Nkx2.5 physically associates with the zinc finger protein GATA4 and cooperatively activates atrial natriuretic factor gene expression. Mol. Cell Biol. 18 (1998), 3120–3129.
21. Li, J., Gao, E., Vite, A., Yi, R., Gomez, L., Goossens, S., van Roy, F., Radice, G., Alpha-catenins control cardiomyocyte proliferation by regulating yap activity. Circ. Res. 116 (2014), 70–79.
22. Lin, Z., Pu, W.T., Strategies for cardiac regeneration and repair. Sci. Transl. Med., 6, 2014, 239rv1.
23. Lin, Z., Pu, W.T., Releasing YAP from an α-catenin trap increases cardiomyocyte proliferation. Circ. Res. 116 (2015), 9–11.
24. Lin, Z., von Gise, A., Zhou, P., Gu, F., Ma, Q., Jiang, J., Yau, A.L., Buck, J.N., Gouin, K.A., et al. Cardiac-specific YAP activation improves cardiac function and survival in an experimental murine MI model. Circ. Res. 115 (2014), 354–363.
25. 2+- and mitochondrial-dependent cardiomyocyte necrosis as a primary mediator of heart failure. J. Clin. Invest. 117 (2007), 2431–2444.
26. Oudhoff, M.J., Freeman, S.A., Couzens, A.L., Antignano, F., Kuznetsova, E., Min, P.H., Northrop, J.P., Lehnertz, B., Barsyte-Lovejoy, D., et al. Control of the hippo pathway by Set7-dependent methylation of Yap. Dev. Cell 26 (2013), 188–194.
27. Pan, D., The hippo signaling pathway in development and cancer. Dev. Cell 19 (2010), 491–505.
28. Prasad, K.-M.R., Xu, Y., Yang, Z., Acton, T., French, A., Robust cardiomyocyte-specific gene expression following systemic injection of AAV: in vivo gene delivery follows a Poisson distribution. Gene Ther. 18 (2011), 43–52.
29. Schlegelmilch, K., Mohseni, M., Kirak, O., Pruszak, J., Rodriguez, J.R., Zhou, D., Kreger, B.T., Vasioukhin, V., Avruch, J., et al. Yap1 acts downstream of alpha-catenin to control epidermal proliferation. Cell 144 (2011), 782–795.
30. Snippert, H.J., van der Flier, L.G., Sato, T., van Es, J.H., van den Born, M., Kroon-Veenboer, C., Barker, N., Klein, A.M., van Rheenen, J., et al. Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 143 (2010), 134–144.
31. Söderberg, O., Gullberg, M., Jarvius, M., Ridderstråle, K., Leuchowius, K.-J., Jarvius, J., Wester, K., Hydbring, P., Bahram, F., et al. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat. Methods, 3, 2006, 995.
32. Umezawa, H., Structures and activities of protease inhibitors of microbial origin. Methods Enzymol. 45 (1976), 678–695.
33. Varelas, X., Miller, B.W., Sopko, R., Song, S., Gregorieff, A., Fellouse, F.A., Sakuma, R., Pawson, T., Hunziker, W., et al. The Hippo pathway regulates Wnt/beta-catenin signaling. Dev. Cell 18 (2010), 579–591.
34. von Gise, A., Lin, Z., Schlegelmilch, K., Honor, L.B., Pan, G.M., Buck, J.N., Ma, Q., Ishiwata, T., Zhou, B., et al. YAP1, the nuclear target of Hippo signaling, stimulates heart growth through cardiomyocyte proliferation but not hypertrophy. Proc. Natl. Acad. Sci. USA 109 (2012), 2394–2399.
35. Walsh, S., Ponten, A., Fleischmann, B.K., Jovinge, S., Cardiomyocyte cell cycle control and growth estimation in vivo—an analysis based on cardiomyocyte nuclei. Cardiovasc. Res. 86 (2010), 365–373.
36. 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.
37. Xin, M., Kim, Y., Sutherland, L.B., Murakami, M., Qi, X., McAnally, J., Porrello, E.R., Mahmoud, A.I., Tan, W., et al. Hippo pathway effector Yap promotes cardiac regeneration. Proc. Natl. Acad. Sci. USA 110 (2013), 13839–13844.
38. Yang, D., Kita, S., Liang, F., Wang, C., Tian, H., Ji, Y., Lončar, M., Quan, Q., High sensitivity and high Q-factor nanoslotted parallel quadrabeam photonic crystal cavity for real-time and label-free sensing. Appl. Phys. Lett., 105, 2014, 063118.
39. Yoshida, T., MCAT elements and the TEF-1 family of transcription factors in muscle development and disease. Arterioscler. Thromb. Vasc. Biol. 28 (2008), 8–17.
40. Zanconato, F., Forcato, M., Battilana, G., Azzolin, L., Quaranta, E., Bodega, B., Rosato, A., Bicciato, S., Cordenonsi, M., Piccolo, S., Genome-wide association between YAP/TAZ/TEAD and AP-1 at enhancers drives oncogenic growth. Nat. Cell Biol. 17 (2015), 1218–1227.
41. Zhang, Z.D., Paccanaro, A., Fu, Y., Weissman, S., Weng, Z., Chang, J., Snyder, M., Gerstein, M.B., Statistical analysis of the genomic distribution and correlation of regulatory elements in the ENCODE regions. Genome Res. 17 (2007), 787–797.
42. Zhang, H., von Gise, A., Liu, Q., Hu, T., Tian, X., He, L., Pu, W., Huang, X., He, L., Cai, C.L., et al. Yap1 is required for endothelial to mesenchymal transition of the atrioventricular cushion. J. Biol. Chem. 289 (2014), 18681–18692.