The endothelial E3 ligase HECW2 promotes endothelial cell junctions by increasing AMOTL1 protein stability via K63-linked ubiquitination

Cellular Signalling

Volumn 28, Issue 11, 2016, Pages 1642-1651

  Choi, Kyu Sung ^a   Choi, Hyun Jung ^b   Lee, Jin Kyu ^a   Im, Suhjean ^a   Zhang, Haiying ^a   Jeong, Yoonjeong ^a   Park, Jeong Ae ^a   Lee, In Kyu ^c   Kim, Young Myeong ^d   Kwon, Young Guen ^a  

^a Yonsei University   (South Korea)

^b Yonsei University College of Medicine   (South Korea)

^c Kyungpook National University School of Medicine   (South Korea)

^d Kangwon National University   (South Korea)

Author keywords

AMOTL1; EC junction; HECW2; Sprouting angiogenesis; YAP

Indexed keywords

ANGIOMOTIN LIKE 1 PROTEIN; ANGIOPOIETIN 2; CD31 ANTIGEN; PEPTIDES AND PROTEINS; UBIQUITIN PROTEIN LIGASE E3; UBIQUITIN PROTEIN LIGASE E3 HECW2; UNCLASSIFIED DRUG; YES ASSOCIATED PROTEIN; AMOTL1 PROTEIN, HUMAN; HECW2 PROTEIN, HUMAN; LYSINE; MEMBRANE PROTEIN; PHOSPHOPROTEIN; POLYUBIQUITIN; PROTEIN BINDING; SIGNAL TRANSDUCING ADAPTOR PROTEIN; UBIQUITIN PROTEIN LIGASE; YAP1 (YES-ASSOCIATED) PROTEIN, HUMAN;

AMINO ACID SUBSTITUTION; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL DIFFERENTIATION; CELL JUNCTION; CELL POLARITY; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVITY; ENZYME DEGRADATION; GENE EXPRESSION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROLINE RICH PROTEIN DOMAIN; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; UBIQUITINATION; ANGIOGENESIS; GENE DELETION; METABOLISM; PROTEIN TRANSPORT; UMBILICAL VEIN ENDOTHELIAL CELL;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANGIOPOIETIN-2; GENE DELETION; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INTERCELLULAR JUNCTIONS; LYSINE; MEMBRANE PROTEINS; NEOVASCULARIZATION, PHYSIOLOGIC; PHOSPHOPROTEINS; POLYUBIQUITIN; PROTEIN BINDING; PROTEIN STABILITY; PROTEIN TRANSPORT; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84982787957     PISSN: 08986568     EISSN: 18733913     Source Type: Journal    
DOI: 10.1016/j.cellsig.2016.07.015     Document Type: Article

References (49)

1. [1] Carmeliet, P., Jain, R.K., Molecular mechanisms and clinical applications of angiogenesis. Nature 473:7347 (2011), 298–307.
2. [2] Herbert, S.P., Stainier, D.Y., Molecular control of endothelial cell behaviour during blood vessel morphogenesis. Nat. Rev. Mol. Cell Biol. 12:9 (2011), 551–564.
3. [3] Dejana, E., Endothelial cell-cell junctions: happy together. Nat. Rev. Mol. Cell Biol. 5:4 (2004), 261–270.
4. [4] Harris, E.S., Nelson, W.J., VE-cadherin: at the front, center, and sides of endothelial cell organization and function. Curr. Opin. Cell Biol. 22:5 (2010), 651–658.
5. [5] Kamath, B.M., Spinner, N.B., Emerick, K.M., Chudley, A.E., Booth, C., Piccoli, D.A., Krantz, I.D., Vascular anomalies in Alagille syndrome: a significant cause of morbidity and mortality. Circulation 109:11 (2004), 1354–1358.
6. [6] ElAli, A., Doeppner, T.R., Zechariah, A., Hermann, D.M., Increased blood–brain barrier permeability and brain edema after focal cerebral ischemia induced by hyperlipidemia: role of lipid peroxidation and calpain-1/2, matrix metalloproteinase-2/9, and RhoA overactivation. Stroke 42:11 (2011), 3238–3244.
7. [7] Bratt, A., Birot, O., Sinha, I., Veitonmaki, N., Aase, K., Ernkvist, M., Holmgren, L., Angiomotin regulates endothelial cell-cell junctions and cell motility. J. Biol. Chem. 280:41 (2005), 34859–34869.
8. [8] Zheng, Y., Vertuani, S., Nystrom, S., Audebert, S., Meijer, I., Tegnebratt, T., Borg, J.P., Uhlen, P., Majumdar, A., Holmgren, L., Angiomotin-like protein 1 controls endothelial polarity and junction stability during sprouting angiogenesis. Circ. Res. 105:3 (2009), 260–270.
9. [9] Patrie, K.M., Identification and characterization of a novel tight junction-associated family of proteins that interacts with a WW domain of MAGI-1. Biochim. Biophys. Acta 1745:1 (2005), 131–144.
10. [10] Yi, C., Troutman, S., Fera, D., Stemmer-Rachamimov, A., Avila, J.L., Christian, N., Persson, N.L., Shimono, A., Speicher, D.W., Marmorstein, R., Holmgren, L., Kissil, J.L., A tight junction-associated Merlin-angiomotin complex mediates Merlin's regulation of mitogenic signaling and tumor suppressive functions. Cancer Cell 19:4 (2011), 527–540.
11. [11] Hultin, S., Zheng, Y., Mojallal, M., Vertuani, S., Gentili, C., Balland, M., Milloud, R., Belting, H.G., Affolter, M., Helker, C.S., Adams, R.H., Herzog, W., Uhlen, P., Majumdar, A., Holmgren, L., AmotL2 links VE-cadherin to contractile actin fibres necessary for aortic lumen expansion. Nat. Commun., 5, 2014, 3743.
12. [12] Skouloudaki, K., Walz, G., YAP1 recruits c-Abl to protect angiomotin-like 1 from Nedd4-mediated degradation. PLoS One, 7(4), 2012, e35735.
13. [13] Miyazaki, K., Ozaki, T., Kato, C., Hanamoto, T., Fujita, T., Irino, S., Watanabe, K., Nakagawa, T., Nakagawara, A., A novel HECT-type E3 ubiquitin ligase, NEDL2, stabilizes p73 and enhances its transcriptional activity. Biochem. Biophys. Res. Commun. 308:1 (2003), 106–113.
14. [14] Miyazaki, K., Fujita, T., Ozaki, T., Kato, C., Kurose, Y., Sakamoto, M., Kato, S., Goto, T., Itoyama, Y., Aoki, M., Nakagawara, A., NEDL1, a novel ubiquitin-protein isopeptide ligase for dishevelled-1, targets mutant superoxide dismutase-1. J. Biol. Chem. 279:12 (2004), 11327–11335.
15. [15] Staub, O., Dho, S., Henry, P., Correa, J., Ishikawa, T., McGlade, J., Rotin, D., WW domains of Nedd4 bind to the proline-rich PY motifs in the epithelial Na + channel deleted in Liddle's syndrome. EMBO J. 15:10 (1996), 2371–2380.
16. [16] Fotia, A.B., Ekberg, J., Adams, D.J., Cook, D.I., Poronnik, P., Kumar, S., Regulation of neuronal voltage-gated sodium channels by the ubiquitin-protein ligases Nedd4 and Nedd4-2. J. Biol. Chem. 279:28 (2004), 28930–28935.
17. [17] Qiu, L., Joazeiro, C., Fang, N., Wang, H.Y., Elly, C., Altman, Y., Fang, D., Hunter, T., Liu, Y.C., Recognition and ubiquitination of Notch by Itch, a hect-type E3 ubiquitin ligase. J. Biol. Chem. 275:46 (2000), 35734–35737.
18. [18] Asano, Y., Ihn, H., Yamane, K., Kubo, M., Tamaki, K., Impaired Smad7-Smurf-mediated negative regulation of TGF-beta signaling in scleroderma fibroblasts. J. Clin. Invest. 113:2 (2004), 253–264.
19. [19] Rotin, D., Kumar, S., Physiological functions of the HECT family of ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 10:6 (2009), 398–409.
20. [20] Broemer, M., Meier, P., Ubiquitin-mediated regulation of apoptosis. Trends Cell Biol. 19:3 (2009), 130–140.
21. [21] Zhao, X., Heng, J.I., Guardavaccaro, D., Jiang, R., Pagano, M., Guillemot, F., Iavarone, A., Lasorella, A., The HECT-domain ubiquitin ligase Huwe1 controls neural differentiation and proliferation by destabilizing the N-Myc oncoprotein. Nat. Cell Biol. 10:6 (2008), 643–653.
22. [22] Bernassola, F., Karin, M., Ciechanover, A., Melino, G., The HECT family of E3 ubiquitin ligases: multiple players in cancer development. Cancer Cell 14:1 (2008), 10–21.
23. [23] Varelas, X., The Hippo pathway effectors TAZ and YAP in development, homeostasis and disease. Development 141:8 (2014), 1614–1626.
24. [24] Choi, H.J., Zhang, H., Park, H., Choi, K.S., Lee, H.W., Agrawal, V., Kim, Y.M., Kwon, Y.G., Yes-associated protein regulates endothelial cell contact-mediated expression of angiopoietin-2. Nat. Commun., 6, 2015, 6943.
25. [25] Marin, V., Kaplanski, G., Gres, S., Farnarier, C., Bongrand, P., Endothelial cell culture: protocol to obtain and cultivate human umbilical endothelial cells. J. Immunol. Methods 254:1–2 (2001), 183–190.
26. [26] Maeng, Y.S., Choi, H.J., Kwon, J.Y., Park, Y.W., Choi, K.S., Min, J.K., Kim, Y.H., Suh, P.G., Kang, K.S., Won, M.H., Kim, Y.M., Kwon, Y.G., Endothelial progenitor cell homing: prominent role of the IGF2-IGF2R-PLCbeta2 axis. Blood 113:1 (2009), 233–243.
27. [27] Murillas, R., Simms, K.S., Hatakeyama, S., Weissman, A.M., Kuehn, M.R., Identification of developmentally expressed proteins that functionally interact with Nedd4 ubiquitin ligase. J. Biol. Chem. 277:4 (2002), 2897–2907.
28. [28] Faber, P.W., Barnes, G.T., Srinidhi, J., Chen, J., Gusella, J.F., MacDonald, M.E., Huntingtin interacts with a family of WW domain proteins. Hum. Mol. Genet. 7:9 (1998), 1463–1474.
29. [29] Bedford, M.T., Chan, D.C., Leder, P., FBP WW domains and the Abl SH3 domain bind to a specific class of proline-rich ligands. EMBO J. 16:9 (1997), 2376–2383.
30. [30] Ermekova, K.S., Zambrano, N., Linn, H., Minopoli, G., Gertler, F., Russo, T., Sudol, M., The WW domain of neural protein FE65 interacts with proline-rich motifs in Mena, the mammalian homolog of Drosophila enabled. J. Biol. Chem. 272:52 (1997), 32869–32877.
31. [31] Wang, C., An, J., Zhang, P., Xu, C., Gao, K., Wu, D., Wang, D., Yu, H., Liu, J.O., Yu, L., The Nedd4-like ubiquitin E3 ligases target angiomotin/p130 to ubiquitin-dependent degradation. Biochem. J. 444:2 (2012), 279–289.
32. [32] Lu, L., Hu, S., Wei, R., Qiu, X., Lu, K., Fu, Y., Li, H., Xing, G., Li, D., Peng, R., He, F., Zhang, L., The HECT type ubiquitin ligase NEDL2 is degraded by anaphase-promoting complex/cyclosome (APC/C)-Cdh1, and its tight regulation maintains the metaphase to anaphase transition. J. Biol. Chem. 288:50 (2013), 35637–35650.
33. [33] Wang, X., Yang, J., Han, L., Zhao, K., Wu, Q., Bao, L., Li, Z., Lv, L., Li, B., TRAF5-mediated Lys-63-linked polyubiquitination plays an essential role in positive regulation of RORgammat in promoting IL-17A expression. J. Biol. Chem. 290:48 (2015), 29086–29094.
34. [34] Yang, W.L., Wu, C.Y., Wu, J., Lin, H.K., Regulation of Akt signaling activation by ubiquitination. Cell Cycle 9:3 (2010), 487–497.
35. [35] Mukhopadhyay, D., Riezman, H., Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 315:5809 (2007), 201–205.
36. [36] DeRan, M., Yang, J., Shen, C.H., Peters, E.C., Fitamant, J., Chan, P., Hsieh, M., Zhu, S., Asara, J.M., Zheng, B., Bardeesy, N., Liu, J., Wu, X., Energy stress regulates hippo-YAP signaling involving AMPK-mediated regulation of angiomotin-like 1 protein. Cell Rep. 9:2 (2014), 495–503.
37. [37] Paramasivam, M., Sarkeshik, A., Yates, J.R. 3rd, Fernandes, M.J., McCollum, D., Angiomotin family proteins are novel activators of the LATS2 kinase tumor suppressor. Mol. Biol. Cell 22:19 (2011), 3725–3733.
38. [38] Vikhanskaya, F., Bani, M.R., Borsotti, P., Ghilardi, C., Ceruti, R., Ghisleni, G., Marabese, M., Giavazzi, R., Broggini, M., Taraboletti, G., p73 overexpression increases VEGF and reduces thrombospondin-1 production: implications for tumor angiogenesis. Oncogene 20:50 (2001), 7293–7300.
39. [39] Fernandez-Alonso, R., Martin-Lopez, M., Gonzalez-Cano, L., Garcia, S., Castrillo, F., Diez-Prieto, I., Fernandez-Corona, A., Lorenzo-Marcos, M.E., Li, X., Claesson-Welsh, L., Marques, M.M., Marin, M.C., p73 is required for endothelial cell differentiation, migration and the formation of vascular networks regulating VEGF and TGFbeta signaling. Cell Death Differ. 22:8 (2015), 1287–1299.
40. [40] Dunn, C.A., Su, V., Lau, A.F., Lampe, P.D., Activation of Akt, not connexin 43 protein ubiquitination, regulates gap junction stability. J. Biol. Chem. 287:4 (2012), 2600–2607.
41. [41] Murakami, T., Frey, T., Lin, C., Antonetti, D.A., Protein kinase cbeta phosphorylates occludin regulating tight junction trafficking in vascular endothelial growth factor-induced permeability in vivo. Diabetes 61:6 (2012), 1573–1583.
42. [42] Marin, I., Animal HECT ubiquitin ligases: evolution and functional implications. BMC Evol. Biol., 10, 2010, 56.
43. [43] Traweger, A., Fang, D., Liu, Y.C., Stelzhammer, W., Krizbai, I.A., Fresser, F., Bauer, H.C., Bauer, H., The tight junction-specific protein occludin is a functional target of the E3 ubiquitin-protein ligase itch. J. Biol. Chem. 277:12 (2002), 10201–10208.
44. [44] Wang, W., Huang, J., Chen, J., Angiomotin-like proteins associate with and negatively regulate YAP1. J. Biol. Chem. 286:6 (2011), 4364–4370.
45. [45] Zhao, B., Li, L., Lu, Q., Wang, L.H., Liu, C.Y., Lei, Q., Guan, K.L., Angiomotin is a novel Hippo pathway component that inhibits YAP oncoprotein. Genes Dev. 25:1 (2011), 51–63.
46. [46] Aase, K., Ernkvist, M., Ebarasi, L., Jakobsson, L., Majumdar, A., Yi, C., Birot, O., Ming, Y., Kvanta, A., Edholm, D., Aspenstrom, P., Kissil, J., Claesson-Welsh, L., Shimono, A., Holmgren, L., Angiomotin regulates endothelial cell migration during embryonic angiogenesis. Genes Dev. 21:16 (2007), 2055–2068.
47. [47] Zhao, B., Tumaneng, K., Guan, K.L., The Hippo pathway in organ size control, tissue regeneration and stem cell self-renewal. Nat. Cell Biol. 13:8 (2011), 877–883.
48. [48] 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., Role of YAP/TAZ in mechanotransduction. Nature 474:7350 (2011), 179–183.
49. [49] Zhao, B., Wei, X., Li, W., Udan, R.S., Yang, Q., Kim, J., Xie, J., Ikenoue, T., Yu, J., Li, L., Zheng, P., Ye, K., Chinnaiyan, A., Halder, G., Lai, Z.C., Guan, K.L., Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev. 21:21 (2007), 2747–2761.