Flow-Dependent Endothelial YAP Regulation Contributes to Vessel Maintenance

Developmental Cell

Volumn 40, Issue 6, 2017, Pages 523-536.e6

  Nakajima, Hiroyuki ^a   Yamamoto, Kimiko ^b   Agarwala, Sobhika ^c   Terai, Kenta ^d   Fukui, Hajime ^a   Fukuhara, Shigetomo ^e   Ando, Koji ^a   Miyazaki, Takahiro ^a   Yokota, Yasuhiro ^a   Schmelzer, Etienne ^f   Belting, Heinz Georg ^f   Affolter, Markus ^f   Lecaudey, Virginie ^g   Mochizuki, Naoki ^a  

^a NATIONAL CEREBRAL AND CARDIOVASCULAR CENTER   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c UNIVERSITY OF FREIBURG   (Germany)

^d KYOTO UNIVERSITY   (Japan)

^e NIPPON MEDICAL SCHOOL   (Japan)

^f UNIVERSITY OF BASEL   (Switzerland)

^g GOETHE UNIVERSITY   (Germany)

Author keywords

fluid shear stress; Hippo pathway; mechanotransduction; vascular remodeling

Indexed keywords

ANGIOMOTIN; F ACTIN; PROTEIN; TRANSCRIPTION FACTOR YAP1; UNCLASSIFIED DRUG; ACTIN; ANGIOMOTIN PROTEIN, ZEBRAFISH; HIPPO PROTEIN, ZEBRAFISH; PHOSPHOPROTEIN; PROTEIN SERINE THREONINE KINASE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TRANSACTIVATOR PROTEIN; YAP1 (YES-ASSOCIATED) PROTEIN, HUMAN; YES-ASSOCIATED PROTEIN (YAP), ZEBRAFISH; ZEBRAFISH PROTEIN;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; BLOOD FLOW; BLOOD VESSEL; CELL NUCLEUS; CONTROLLED STUDY; EMBRYO; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; LAMINAR FLOW; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; SHEAR STRESS; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL CELL; VASCULAR ENDOTHELIUM; ZEBRA FISH; ANIMAL; BLOOD RHEOLOGY; EMBRYOLOGY; ENDOTHELIUM CELL; GENETICS; MECHANICAL STRESS; METABOLISM; PERFUSION; PROTEIN TRANSPORT; SHEAR STRENGTH; TRANSCRIPTION INITIATION; UMBILICAL VEIN ENDOTHELIAL CELL;

ACTINS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BLOOD VESSELS; CELL NUCLEUS; ENDOTHELIAL CELLS; HEMORHEOLOGY; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; PERFUSION; PHOSPHOPROTEINS; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; SHEAR STRENGTH; SIGNAL TRANSDUCTION; STRESS, MECHANICAL; TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 85016450607     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2017.02.019     Document Type: Article

References (58)

1. Agarwala, S., Duquesne, S., Liu, K., Boehm, A., Grimm, L., Link, S., Konig, S., Eimer, S., Ronneberger, O., Lecaudey, V., Amotl2a interacts with the Hippo effector Yap1 and the Wnt/beta-catenin effector Lef1 to control tissue size in zebrafish. Elife, 4, 2015, e08201.
2. Ando, J., Yamamoto, K., Flow detection and calcium signalling in vascular endothelial cells. Cardiovasc. Res. 99 (2013), 260–268.
3. Aragona, M., Panciera, T., Manfrin, A., Giulitti, S., Michielin, F., Elvassore, N., Dupont, S., Piccolo, S., A mechanical checkpoint controls multicellular growth through YAP/TAZ regulation by actin-processing factors. Cell 154 (2013), 1047–1059.
4. Asakawa, K., Suster, M.L., Mizusawa, K., Nagayoshi, S., Kotani, T., Urasaki, A., Kishimoto, Y., Hibi, M., Kawakami, K., Genetic dissection of neural circuits by Tol2 transposon-mediated Gal4 gene and enhancer trapping in zebrafish. Proc. Natl. Acad. Sci. USA 105 (2008), 1255–1260.
5. Avruch, J., Zhou, D., Fitamant, J., Bardeesy, N., Mou, F., Barrufet, L.R., Protein kinases of the Hippo pathway: regulation and substrates. Semin. Cell Dev. Biol. 23 (2012), 770–784.
6. Bao, Y., Nakagawa, K., Yang, Z., Ikeda, M., Withanage, K., Ishigami-Yuasa, M., Okuno, Y., Hata, S., Nishina, H., Hata, Y., A cell-based assay to screen stimulators of the Hippo pathway reveals the inhibitory effect of dobutamine on the YAP-dependent gene transcription. J. Biochem. 150 (2011), 199–208.
7. Benham-Pyle, B.W., Pruitt, B.L., Nelson, W.J., Cell adhesion. Mechanical strain induces E-cadherin-dependent Yap1 and beta-catenin activation to drive cell cycle entry. Science 348 (2015), 1024–1027.
8. Betz, C., Lenard, A., Belting, H.G., Affolter, M., Cell behaviors and dynamics during angiogenesis. Development 143 (2016), 2249–2260.
9. Bussmann, J., Wolfe, S.A., Siekmann, A.F., Arterial-venous network formation during brain vascularization involves hemodynamic regulation of chemokine signaling. Development 138 (2011), 1717–1726.
10. Calvo, F., Ege, N., Grande-Garcia, A., Hooper, S., Jenkins, R.P., Chaudhry, S.I., Harrington, K., Williamson, P., Moeendarbary, E., Charras, G., et al. Mechanotransduction and YAP-dependent matrix remodelling is required for the generation and maintenance of cancer-associated fibroblasts. Nat. Cell Biol. 15 (2013), 637–646.
11. Cermak, T., Doyle, E.L., Christian, M., Wang, L., Zhang, Y., Schmidt, C., Baller, J.A., Somia, N.V., Bogdanove, A.J., Voytas, D.F., Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res., 39, 2011, e82.
12. Chan, S.W., Lim, C.J., Chong, Y.F., Pobbati, A.V., Huang, C., Hong, W., Hippo pathway-independent restriction of TAZ and YAP by angiomotin. J. Biol. Chem. 286 (2011), 7018–7026.
13. Chen, C.H., Sun, Y.H., Pei, D.S., Zhu, Z.Y., Comparative expression of zebrafish lats1 and lats2 and their implication in gastrulation movements. Dev. Dyn. 238 (2009), 2850–2859.
14. Chen, Q., Jiang, L., Li, C., Hu, D., Bu, J.W., Cai, D., Du, J.L., Haemodynamics-driven developmental pruning of brain vasculature in zebrafish. PLoS Biol., 10, 2012, e1001374.
15. Cheung, A., Dantzig, J.A., Hollingworth, S., Baylor, S.M., Goldman, Y.E., Mitchison, T.J., Straight, A.F., A small-molecule inhibitor of skeletal muscle myosin II. Nat. Cell Biol. 4 (2002), 83–88.
16. Chiba, A., Watanabe-Takano, H., Terai, K., Fukui, H., Miyazaki, T., Uemura, M., Hashimoto, H., Hibi, M., Fukuhara, S., Mochizuki, N., Osteocrin, a peptide secreted from the heart and other tissues, contributes to cranial osteogenesis and chondrogenesis in zebrafish. Development 144 (2016), 334–344.
17. Chiu, J.J., Chien, S., Effects of disturbed flow on vascular endothelium: pathophysiological basis and clinical perspectives. Physiol. Rev. 91 (2011), 327–387.
18. 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.
19. Codelia, V.A., Sun, G., Irvine, K.D., Regulation of YAP by mechanical strain through Jnk and Hippo signaling. Curr. Biol. 24 (2014), 2012–2017.
20. Cui, Y., Hameed, F.M., Yang, B., Lee, K., Pan, C.Q., Park, S., Sheetz, M., Cyclic stretching of soft substrates induces spreading and growth. Nat. Commun., 6, 2015, 6333.
21. Dupont, S., Morsut, L., Aragona, M., Enzo, E., Giulitti, S., Cordenonsi, M., Zanconato, F., Le, D.J., Forcato, M., Bicciato, S., et al. Role of YAP/TAZ in mechanotransduction. Nature 474 (2011), 179–183.
22. Eilken, H.M., Adams, R.H., Dynamics of endothelial cell behavior in sprouting angiogenesis. Curr. Opin. Cell Biol. 22 (2010), 617–625.
23. Ernkvist, M., Aase, K., Ukomadu, C., Wohlschlegel, J., Blackman, R., Veitonmaki, N., Bratt, A., Dutta, A., Holmgren, L., p130-angiomotin associates to actin and controls endothelial cell shape. FEBS J. 273 (2006), 2000–2011.
24. Feng, X., Degese, M.S., Iglesias-Bartolome, R., Vaque, J.P., Molinolo, A.A., Rodrigues, M., Zaidi, M.R., Ksander, B.R., Merlino, G., Sodhi, A., et al. Hippo-independent activation of YAP by the GNAQ uveal melanoma oncogene through a trio-regulated rho GTPase signaling circuitry. Cancer Cell 25 (2014), 831–845.
25. Franco, C.A., Jones, M.L., Bernabeu, M.O., Geudens, I., Mathivet, T., Rosa, A., Lopes, F.M., Lima, A.P., Ragab, A., Collins, R.T., et al. Dynamic endothelial cell rearrangements drive developmental vessel regression. PLoS Biol., 13, 2015, e1002125.
26. Freund, J.B., Goetz, J.G., Hill, K.L., Vermot, J., Fluid flows and forces in development: functions, features and biophysical principles. Development 139 (2012), 1229–1245.
27. Fukui, H., Terai, K., Nakajima, H., Chiba, A., Fukuhara, S., Mochizuki, N., S1P-Yap1 signaling regulates endoderm formation required for cardiac precursor cell migration in zebrafish. Dev. Cell 31 (2014), 128–136.
28. Geudens, I., Gerhardt, H., Coordinating cell behaviour during blood vessel formation. Development 138 (2011), 4569–4583.
29. Hahn, C., Schwartz, M.A., Mechanotransduction in vascular physiology and atherogenesis. Nat. Rev. Mol. Cell Biol. 10 (2009), 53–62.
30. Herbert, S.P., Stainier, D.Y., Molecular control of endothelial cell behaviour during blood vessel morphogenesis. Nat. Rev. Mol. Cell Biol. 12 (2011), 551–564.
31. Herwig, L., Blum, Y., Krudewig, A., Ellertsdottir, E., Lenard, A., Belting, H.G., Affolter, M., Distinct cellular mechanisms of blood vessel fusion in the zebrafish embryo. Curr. Biol. 21 (2011), 1942–1948.
32. Kok, F.O., Shin, M., Ni, C.W., Gupta, A., Grosse, A.S., van Impel, A., Kirchmaier, B.C., Peterson-Maduro, J., Kourkoulis, G., Male, I., et al. Reverse genetic screening reveals poor correlation between morpholino-induced and mutant phenotypes in zebrafish. Dev. Cell 32 (2015), 97–108.
33. Kwon, H.B., Fukuhara, S., Asakawa, K., Ando, K., Kashiwada, T., Kawakami, K., Hibi, M., Kwon, Y.G., Kim, K.W., Alitalo, K., et al. The parallel growth of motoneuron axons with the dorsal aorta depends on Vegfc/Vegfr3 signaling in zebrafish. Development 140 (2013), 4081–4090.
34. Langheinrich, U., Vacun, G., Wagner, T., Zebrafish embryos express an orthologue of HERG and are sensitive toward a range of QT-prolonging drugs inducing severe arrhythmia. Toxicol. Appl. Pharmacol. 193 (2003), 370–382.
35. Lawson, N.D., Weinstein, B.M., In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev. Biol. 248 (2002), 307–318.
36. Lucitti, J.L., Jones, E.A., Huang, C., Chen, J., Fraser, S.E., Dickinson, M.E., Vascular remodeling of the mouse yolk sac requires hemodynamic force. Development 134 (2007), 3317–3326.
37. Mana-Capelli, S., Paramasivam, M., Dutta, S., McCollum, D., Angiomotins link F-actin architecture to Hippo pathway signaling. Mol. Biol. Cell 25 (2014), 1676–1685.
38. Meeson, A., Palmer, M., Calfon, M., Lang, R., A relationship between apoptosis and flow during programmed capillary regression is revealed by vital analysis. Development 122 (1996), 3929–3938.
39. Miesfeld, J.B., Gestri, G., Clark, B.S., Flinn, M.A., Poole, R.J., Bader, J.R., Besharse, J.C., Wilson, S.W., Link, B.A., Yap and Taz regulate retinal pigment epithelial cell fate. Development 142 (2015), 3021–3032.
40. Montero-Balaguer, M., Swirsding, K., Orsenigo, F., Cotelli, F., Mione, M., Dejana, E., Stable vascular connections and remodeling require full expression of VE-cadherin in zebrafish embryos. PLoS One, 4, 2009, e5772.
41. Morin-Kensicki, E.M., Boone, B.N., Howell, M., Stonebraker, J.R., Teed, J., Alb, J.G., Magnuson, T.R., O'Neal, W., Milgram, S.L., Defects in yolk sac vasculogenesis, chorioallantoic fusion, and embryonic axis elongation in mice with targeted disruption of Yap65. Mol. Cell. Biol. 26 (2006), 77–87.
42. Ota, M., Sasaki, H., Mammalian Tead proteins regulate cell proliferation and contact inhibition as transcriptional mediators of Hippo signaling. Development 135 (2008), 4059–4069.
43. Piccolo, S., Dupont, S., Cordenonsi, M., The biology of YAP/TAZ: hippo signaling and beyond. Physiol. Rev. 94 (2014), 1287–1312.
44. Porazinski, S., Wang, H., Asaoka, Y., Behrndt, M., Miyamoto, T., Morita, H., Hata, S., Sasaki, T., Krens, S.F., Osada, Y., et al. YAP is essential for tissue tension to ensure vertebrate 3D body shape. Nature 521 (2015), 217–221.
45. Rossi, A., Kontarakis, Z., Gerri, C., Nolte, H., Holper, S., Kruger, M., Stainier, D.Y., Genetic compensation induced by deleterious mutations but not gene knockdowns. Nature 524 (2015), 230–233.
46. Sabine, A., Bovay, E., Demir, C.S., Kimura, W., Jaquet, M., Agalarov, Y., Zangger, N., Scallan, J.P., Graber, W., Gulpinar, E., et al. FOXC2 and fluid shear stress stabilize postnatal lymphatic vasculature. J. Clin. Invest. 125 (2015), 3861–3877.
47. Sakurai, A., Fukuhara, S., Yamagishi, A., Sako, K., Kamioka, Y., Masuda, M., Nakaoka, Y., Mochizuki, N., MAGI-1 is required for Rap1 activation upon cell-cell contact and for enhancement of vascular endothelial cadherin-mediated cell adhesion. Mol. Biol. Cell 17 (2006), 966–976.
48. Serluca, F.C., Drummond, I.A., Fishman, M.C., Endothelial signaling in kidney morphogenesis: a role for hemodynamic forces. Curr. Biol. 12 (2002), 492–497.
49. Uemura, M., Nagasawa, A., Terai, K., Yap/Taz transcriptional activity in endothelial cells promotes intramembranous ossification via the BMP pathway. Sci. Rep., 6, 2016, 27473.
50. Wada, K., Itoga, K., Okano, T., Yonemura, S., Sasaki, H., Hippo pathway regulation by cell morphology and stress fibers. Development 138 (2011), 3907–3914.
51. Wang, Y., Kaiser, M.S., Larson, J.D., Nasevicius, A., Clark, K.J., Wadman, S.A., Roberg-Perez, S.E., Ekker, S.C., Hackett, P.B., McGrail, M., et al. Moesin1 and Ve-cadherin are required in endothelial cells during in vivo tubulogenesis. Development 137 (2010), 3119–3128.
52. Wang, W., Huang, J., Chen, J., Angiomotin-like proteins associate with and negatively regulate YAP1. J. Biol. Chem. 286 (2011), 4364–4370.
53. Wang, K.C., Yeh, Y.T., Nguyen, P., Limqueco, E., Lopez, J., Thorossian, S., Guan, K.L., Li, Y.J., Chien, S., Flow-dependent YAP/TAZ activities regulate endothelial phenotypes and atherosclerosis. Proc. Natl. Acad. Sci. USA 113 (2016), 11525–11530.
54. Yamamoto, K., Shimizu, N., Obi, S., Kumagaya, S., Taketani, Y., Kamiya, A., Ando, J., Involvement of cell surface ATP synthase in flow-induced ATP release by vascular endothelial cells. Am. J. Physiol. Heart Circ. Physiol. 293 (2007), H1646–H1653.
55. 2+ oscillations reflect VEGFR signaling-regulated angiogenic capacity in vivo. Elife, 4, 2015, e08817.
56. Yu, F.X., Guan, K.L., The Hippo pathway: regulators and regulations. Genes Dev. 27 (2013), 355–371.
57. 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 (2011), 51–63.
58. Zygmunt, T., Gay, C.M., Blondelle, J., Singh, M.K., Flaherty, K.M., Means, P.C., Herwig, L., Krudewig, A., Belting, H.G., Affolter, M., et al. Semaphorin-PlexinD1 signaling limits angiogenic potential via the VEGF decoy receptor sFlt1. Dev. Cell 21 (2011), 301–314.