The Role of YAP and TAZ in Angiogenesis and Vascular Mimicry
Abstract
1. Introduction
1.1. Angiogenesis and Its Roles in Development and Pathogenesis
1.1.1. Angiogenesis
1.1.2. Angiogenesis in Development
1.1.3. Angiogenesis in Pathogenesis
1.2. Yes-Associated Protein (YAP) and Paralog Transcription Activator with PDZ Binding Motif (TAZ)
2. Roles of YAP/TAZ in the Regulation of Endothelial Function during Angiogenesis
2.1. Angiomotin (AMOT) Family
2.2. CD44
2.3. Extracellular Matrix (ECM)
2.4. Transforming Growth Factor-β (TGFβ)/Bone Morphogenic Protein (BMP)
2.5. WNT Pathway
2.6. PROX1 Transcriptional Programing—Key Regulators of Blood Vessel and Lymphatic Endothelial Cell Trans-Differentiation
3. Roles of YAP/TAZ in Developmental Vasculogenesis and Angiogenesis
4. Roles of YAP/TAZ in Pathological Angiogenesis
5. Roles of YAP/TAZ in Tumor Angiogenesis and Vascular Mimicry
6. Conclusion and Future Directions
Funding
Acknowledgments
Conflicts of Interest
References
- Hillen, F.; Griffioen, A.W. Tumour vascularization: Sprouting angiogenesis and beyond. Cancer Metastasis Rev. 2007, 26, 489–502. [Google Scholar] [CrossRef] [PubMed]
- Djonov, V.; Baum, O.; Burri, P.H. Vascular remodeling by intussusceptive angiogenesis. Cell Tissue Res. 2003, 314, 107–117. [Google Scholar] [CrossRef] [PubMed]
- Lamalice, L.; Le Boeuf, F.; Huot, J. Endothelial cell migration during angiogenesis. Circ. Res. 2007, 100, 782–794. [Google Scholar] [CrossRef]
- Caduff, J.H.; Fischer, L.C.; Burri, P.H. Scanning electron microscope study of the developing microvasculature in the postnatal rat lung. Anat. Rec. 1986, 216, 154–164. [Google Scholar] [CrossRef] [PubMed]
- Otrock, Z.K.; Mahfouz, R.A.; Makarem, J.A.; Shamseddine, A.I. Understanding the biology of angiogenesis: Review of the most important molecular mechanisms. Blood Cellsmoleculesand Dis. 2007, 39, 212–220. [Google Scholar] [CrossRef] [PubMed]
- Deveza, L.; Choi, J.; Yang, F.J. Therapeutic angiogenesis for treating cardiovascular diseases. Theranostics 2012, 2, 801. [Google Scholar] [CrossRef]
- Couffinhal, T.; Dufourcq, P.; Daret, D.; Duplaa, C. The mechanisms of angiogenesis. Medical and therapeutic applications. La Revue de Medecine Interne 2001, 22, 1064–1082. [Google Scholar] [CrossRef]
- Muñoz-Chápuli, R. Evolution of angiogenesis. Int. J. Dev. Biol. 2011, 55, 345–351. [Google Scholar] [CrossRef]
- Breier, G. Angiogenesis in embryonic development—A review. Placenta 2000, 21, S11–S15. [Google Scholar] [CrossRef] [PubMed]
- Klagsbrun, M.; D’Amore, P.A. Vascular endothelial growth factor and its receptors. Cytokine Growth Factor Rev. 1996, 3, 259–270. [Google Scholar] [CrossRef]
- Chung, A.S.; Ferrara, N. Developmental and pathological angiogenesis. Annu. Rev. Cell Dev. Biol. 2011, 27, 563–584. [Google Scholar] [CrossRef]
- Lobov, I.; Renard, R.; Papadopoulos, N.; Gale, N.; Thurston, G.; Yancopoulos, G.; Wiegand, S.J. Delta-like ligand 4 (Dll4) is induced by VEGF as a negative regulator of angiogenic sprouting. Proc. Natl. Acad. Sci. USA 2007, 104, 3219–3224. [Google Scholar] [CrossRef] [PubMed]
- Betz, C.; Lenard, A.; Belting, H.-G.; Affolter, M. Cell behaviors and dynamics during angiogenesis. Co. Biol. 2016, 143, 2249–2260. [Google Scholar]
- Flanagan, J.G.; Vanderhaeghen, P. The ephrins and Eph receptors in neural development. Annu. Rev. Neurosci. 1998, 21, 309–345. [Google Scholar] [CrossRef]
- Creamer, D.; Sullivan, D.; Bicknell, R.; Barker, J. Angiogenesis in psoriasis. Angiogenesis 2002, 5, 231–236. [Google Scholar] [CrossRef] [PubMed]
- Tuo, J.; Wang, Y.; Cheng, R.; Li, Y.; Chen, M.; Qiu, F.; Qian, H.; Shen, D.; Penalva, R.; Xu, H. Wnt signaling in age-related macular degeneration: Human macular tissue and mouse model. J. Transl. Med. 2015, 13, 330. [Google Scholar] [CrossRef] [PubMed]
- Fallah, A.; Sadeghinia, A.; Kahroba, H.; Samadi, A.; Heidari, H.R.; Bradaran, B.; Zeinali, S.; Molavi, O. Therapeutic targeting of angiogenesis molecular pathways in angiogenesis-dependent diseases. J. Cell. Physiol. 2019, 110, 775–785. [Google Scholar] [CrossRef]
- Zetter, P.B.R. Angiogenesis and tumor metastasis. Annu. Rev. Med. 1998, 49, 407–424. [Google Scholar] [CrossRef]
- Bergers, G.; Benjamin, L.E. Tumorigenesis and the angiogenic switch. Nat. Rev. Cancer 2003, 3, 401–410. [Google Scholar] [CrossRef]
- Lawler, J. Thrombospondin-1 as an endogenous inhibitor of angiogenesis and tumor growth. J. Cell. Mol. Med. 2002, 6, 1–12. [Google Scholar] [CrossRef]
- Carmeliet, P.; Jain, R.K. Angiogenesis in cancer and other diseases. Nature 2000, 407, 249–257. [Google Scholar] [CrossRef]
- Totaro, A.; Panciera, T.; Piccolo, S. YAP/TAZ upstream signals and downstream responses. Nat. Cell Biol. 2018, 20, 888–899. [Google Scholar] [CrossRef]
- Moya, I.M.; Halder, G. Hippo–YAP/TAZ signalling in organ regeneration and regenerative medicine. Nat. Rev. Mol. Cell Biol. 2018, 20, 211–226. [Google Scholar] [CrossRef]
- Maugeri-Saccà, M.; Barba, M.; Pizzuti, L.; Vici, P.; Di Lauro, L.; Dattilo, R.; Vitale, I.; Bartucci, M.; Mottolese, M.; De Maria, R. The Hippo transducers TAZ and YAP in breast cancer: Oncogenic activities and clinical implications. J. Exp. Clin. Cancer Res. 2015, 17, e14. [Google Scholar] [CrossRef]
- Hansen, C.G.; Moroishi, T.; Guan, K.-L. YAP and TAZ: A nexus for Hippo signaling and beyond. Trends Cell Biol. 2015, 25, 499–513. [Google Scholar] [CrossRef]
- Zhang, K.; Qi, H.-X.; Hu, Z.-M.; Chang, Y.-N.; Shi, Z.-M.; Han, X.-H.; Han, Y.-W.; Zhang, R.-X.; Zhang, Z.; Chen, T. YAP and TAZ take center stage in cancer. Biochemistry 2015, 54, 6555–6566. [Google Scholar] [CrossRef]
- Csibi, A.; Blenis, J. Hippo-YAP and mTOR pathways collaborate to regulate organ size. Nat. Cell Biol. 2012, 14, 1244–1245. [Google Scholar] [CrossRef]
- Tumaneng, K.; Russell, R.C.; Guan, K.-L. Organ size control by Hippo and TOR pathways. Curr. Biol. 2012, 22, R368–R379. [Google Scholar] [CrossRef]
- Hong, W.; Guan, K.-L. The YAP and TAZ transcription co-activators: Key downstream effectors of the mammalian Hippo pathway. Semin. Cell Dev. Biol. 2012, 23, 785–793. [Google Scholar] [CrossRef]
- Justice, R.W.; Zilian, O.; Woods, D.F.; Noll, M.; Bryant, P. The Drosophila tumor suppressor gene warts encodes a homolog of human myotonic dystrophy kinase and is required for the control of cell shape and proliferation. Genes Dev. 1995, 9, 534–546. [Google Scholar] [CrossRef]
- Tapon, N.; Harvey, K.F.; Bell, D.W.; Wahrer, D.C.R.; Schiripo, T.A.; Haber, D.A.; Hariharan, I.K. salvador Promotes both cell cycle exit and apoptosis in Drosophila and is mutated in human cancer cell lines. Cell 2002, 110, 467–478. [Google Scholar] [CrossRef]
- Wu, S.; Huang, J.; Dong, J.; Pan, D. hippo encodes a Ste-20 family protein kinase that restricts cell proliferation and promotes apoptosis in conjunction with salvador and warts. Cell 2003, 114, 445–456. [Google Scholar] [CrossRef]
- Lai, Z.-C.; Wei, X.; Shimizu, T.; Ramos, E.; Rohrbaugh, M.; Nikolaidis, N.; Ho, L.-L.; Li, Y. Control of cell proliferation and apoptosis by mob as tumor suppressor, mats. Cell 2005, 120, 675–685. [Google Scholar] [CrossRef]
- Pan, D. The hippo signaling pathway in development and cancer. Dev. Cell 2010, 19, 491–505. [Google Scholar] [CrossRef] [PubMed]
- Saucedo, L.J.; Edgar, B.A. Filling out the Hippo pathway. Nat. Rev. Mol. Cell Biol. 2007, 8, 613–621. [Google Scholar] [CrossRef] [PubMed]
- Zhao, B.; Wei, X.; Li, W.; Udan, R.S.; Yang, Q.; Kim, J.; Xie, J.; Ikenoue, T.; Yu, J.; Li, L. Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev. 2007, 21, 2747–2761. [Google Scholar] [CrossRef] [PubMed]
- Callus, B.A.; Verhagen, A.M.; Vaux, D.L. Association of mammalian sterile twenty kinases, Mst1 and Mst2, with hSalvador via C-terminal coiled-coil domains, leads to its stabilization and phosphorylation. Febs J. 2006, 273, 4264–4276. [Google Scholar] [CrossRef]
- Praskova, M.; Xia, F.; Avruch, J. MOBKL1A/MOBKL1B phosphorylation by MST1 and MST2 inhibits cell proliferation. Curr. Biol. 2008, 18, 311–321. [Google Scholar] [CrossRef]
- Chan, E.H.Y.; Nousiainen, M.; Chalamalasetty, R.B.; Schäfer, A.; Nigg, E.A.; Silljé, H.H.W. The Ste20-like kinase Mst2 activates the human large tumor suppressor kinase Lats1. Oncogene 2005, 24, 2076–2086. [Google Scholar] [CrossRef] [PubMed]
- Yu, F.-X.; Guan, K.-L. The Hippo pathway: Regulators and regulations. Genes Dev. 2013, 27, 355–371. [Google Scholar] [CrossRef] [PubMed]
- Hao, Y.; Chun, A.; Cheung, K.; Rashidi, B.; Yang, X. Tumor suppressor LATS1 is a negative regulator of oncogene YAP. J. Biol. Chem. 2008, 283, 5496–5509. [Google Scholar] [CrossRef] [PubMed]
- Piccolo, S.; Dupont, S.; Cordenonsi, M. The biology of YAP/TAZ: Hippo signaling and beyond. Physiol. Rev. 2014, 94, 1287–1312. [Google Scholar] [CrossRef]
- Panciera, T.; Azzolin, L.; Cordenonsi, M.; Piccolo, S. Mechanobiology of YAP and TAZ in physiology and disease. Nat. Rev. Mol. Cell Biol. 2017, 18, 758–770. [Google Scholar] [CrossRef] [PubMed]
- 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. 2011, 25, 51–63. [Google Scholar] [CrossRef] [PubMed]
- Yang, C.-C.; Graves, H.K.; Moya, I.M.; Tao, C.; Hamaratoglu, F.; Gladden, A.B.; Halder, G. Differential regulation of the Hippo pathway by adherens junctions and apical–basal cell polarity modules. Proc. Natl. Acad. Sci. USA 2015, 112, 1785–1790. [Google Scholar] [CrossRef] [PubMed]
- Yu, F.-X.; Zhao, B.; Panupinthu, N.; Jewell, J.L.; Lian, I.; Wang, L.H.; Zhao, J.; Yuan, H.; Tumaneng, K.; Li, H. Regulation of the Hippo-YAP pathway by G-protein-coupled receptor signaling. Cell 2012, 150, 780–791. [Google Scholar] [CrossRef]
- Gschwind, A.; Fischer, O.M.; Ullrich, A. The discovery of receptor tyrosine kinases: Targets for cancer therapy. Nat. Rev. Cancer 2004, 4, 361–370. [Google Scholar] [CrossRef]
- van Rensburg, H.J.J.; Lai, D.; Azad, T.; Hao, Y.; Yang, X. TAZ enhances mammary cell proliferation in 3D culture through transcriptional regulation of IRS1. Cell. Signal. 2018, 52, 12–22. [Google Scholar] [CrossRef] [PubMed]
- Fan, R.; Kim, N.-G.; Gumbiner, B.M. Regulation of Hippo pathway by mitogenic growth factors via phosphoinositide 3-kinase and phosphoinositide-dependent kinase-1. Proc. Natl. Acad. Sci. USA 2013, 110, 2569–2574. [Google Scholar] [CrossRef] [PubMed]
- Zhao, Y.; Montminy, T.; Azad, T.; Lightbody, E.; Hao, Y.; SenGupta, S.; Asselin, E.; Nicol, C.; Yang, X. PI3K Positively Regulates YAP and TAZ in Mammary Tumorigenesis Through Multiple Signaling Pathways. Mol. Cancer Res. 2018, 16, 1046–1058. [Google Scholar] [CrossRef] [PubMed]
- Glienke, J.; Schmitt, A.O.; Pilarsky, C.; Hinzmann, B.; Weiß, B.; Rosenthal, A.; Thierauch, K.H. Differential gene expression by endothelial cells in distinct angiogenic states. Eur. J. Biochem. 2000, 267, 2820–2830. [Google Scholar] [CrossRef]
- Auerbach, R.; Lewis, R.; Shinners, B.; Kubai, L.; Akhtar, N. Angiogenesis assays: A critical overview. Clin. Chem. 2003, 49, 32–40. [Google Scholar] [CrossRef]
- Auerbach, R.; Akhtar, N.; Lewis, R.L.; Shinners, B.L. Angiogenesis assays: Problems and pitfalls. Cancer Metastasis Rev. 2000, 19, 167–172. [Google Scholar] [CrossRef]
- Staton, C.A.; Lewis, C.; Bicknell, R. Angiogenesis Assays: A Critical Appraisal of Current Techniques; John Wiley & Sons: Hoboken, NJ, USA, 2007. [Google Scholar]
- Goodwin, A.M. In vitro assays of angiogenesis for assessment of angiogenic and anti-angiogenic agents. Microvasc. Res. 2007, 74, 172–183. [Google Scholar] [CrossRef]
- Cui, X.; Morales, R.-T.T.; Qian, W.; Wang, H.; Gagner, J.-P.; Dolgalev, I.; Placantonakis, D.; Zagzag, D.; Cimmino, L.; Snuderl, M. Hacking macrophage-associated immunosuppression for regulating glioblastoma angiogenesis. Biomaterials 2018, 161, 164–178. [Google Scholar] [CrossRef]
- Song, L.; Ahmed, M.F.; Li, Y.; Zeng, C.; Li, Y. Vascular Differentiation from Pluripotent Stem Cells in 3-D Auxetic Scaffolds. J. Tissue Eng. Regen. Med. 2018, 12, 1679–1689. [Google Scholar] [CrossRef]
- Aase, K.; Ernkvist, M.; Ebarasi, L.; Jakobsson, L.; Majumdar, A.; Yi, C.; Birot, O.; Ming, Y.; Kvanta, A.; Edholm, D. Angiomotin regulates endothelial cell migration during embryonic angiogenesis. Genes Dev. 2007, 21, 2055–2068. [Google Scholar] [CrossRef]
- Zheng, Y.; Vertuani, S.; Nystrom, S.; Audebert, S.; Meijer, I.; Tegnebratt, T.; Borg, J.-P.; Uhlén, P.; Majumdar, A.; Holmgren, L. Angiomotin-like protein 1 controls endothelial polarity and junction stability during sprouting angiogenesis. Circ. Res. 2009, 105, 260–270. [Google Scholar] [CrossRef]
- Skouloudaki, K.; Walz, G. YAP1 recruits c-Abl to protect angiomotin-like 1 from Nedd4-mediated degradation. PLoS ONE 2012, 7, e35735. [Google Scholar] [CrossRef]
- Dai, X.; She, P.; Chi, F.; Feng, Y.; Liu, H.; Jin, D.; Zhao, Y.; Guo, X.; Jiang, D.; Guan, K.-L.; Zhong, T.P.; Zhao, B. Phosphorylation of angiomotin by Lats1/2 kinases inhibits F-actin binding, cell migration and angiogenesis. J. Biol. Chem. 2013, 288, 34041–34051. [Google Scholar] [CrossRef]
- Hong, S.A.; Son, M.W.; Cho, J.; Jang, S.H.; Lee, H.J.; Lee, J.H.; Cho, H.D.; Oh, M.H.; Lee, M.S. Low angiomotin-p130 with concomitant high Yes-associated protein 1 expression is associated with adverse prognosis of advanced gastric cancer. Apmis 2017, 125, 996–1006. [Google Scholar] [CrossRef]
- Singleton, P.A.; Salgia, R.; Moreno-Vinasco, L.; Moitra, J.; Sammani, S.; Mirzapoiazova, T.; Garcia, J.G.N. CD44 Regulates Hepatocyte Growth Factor-mediated Vascular Integrity: ROLE OF c-Met, Tiam1/Rac1, DYNAMIN 2, AND CORTACTIN. J. Biol. Chem. 2007, 282, 30643–30657. [Google Scholar] [CrossRef] [PubMed]
- Savani, R.C.; Cao, G.; Pooler, P.M.; Zaman, A.; Zhou, Z.; DeLisser, H.M. Differential involvement of the hyaluronan (HA) receptors CD44 and receptor for HA-mediated motility in endothelial cell function and angiogenesis. J. Biol. Chem. 2001, 276, 36770–36778. [Google Scholar] [CrossRef]
- Flynn, K.M.; Michaud, M.; Canosa, S.; Madri, J.A. CD44 regulates vascular endothelial barrier integrity via a PECAM-1 dependent mechanism. Angiogenesis 2013, 16, 689–705. [Google Scholar] [CrossRef]
- Stamenkovic, I.; Yu, Q. Merlin, a “magic” linker between the extracellular cues and intracellular signaling pathways that regulate cell motility, proliferation, and survival. Curr. Protein Pept. Sci. 2010, 11, 471–484. [Google Scholar] [CrossRef]
- Badouel, C.; McNeill, H. SnapShot: The hippo signaling pathway. Cell 2011, 145, 484–484.e1. [Google Scholar] [CrossRef]
- Tsuneki, M.; Madri, J.A. Adhesion molecule-mediated hippo pathway modulates hemangioendothelioma cell behavior. Mol. Cell. Biol. 2014, 34, 4485–4499. [Google Scholar] [CrossRef]
- Tsuneki, M.; Madri, J.A. CD44 regulation of endothelial cell proliferation and apoptosis via modulation of CD31 and VE-cadherin expression. J. Biol. Chem. 2014, 289, 5357–5370. [Google Scholar] [CrossRef] [PubMed]
- Xu, Y.; Stamenkovic, I.; Yu, Q. CD44 attenuates activation of the hippo signaling pathway and is a prime therapeutic target for glioblastoma. Cancer Res. 2010, 70, 2455–2464. [Google Scholar] [CrossRef]
- Wada, K.-I.; Itoga, K.; Okano, T.; Yonemura, S.; Sasaki, H. Hippo pathway regulation by cell morphology and stress fibers. Development 2011, 138, 3907–3914. [Google Scholar] [CrossRef]
- Dupont, S.; Morsut, L.; Aragona, M.; Enzo, E.; Giulitti, S.; Cordenonsi, M.; Zanconato, F.; Le Digabel, J.; Forcato, M.; Bicciato, S. Role of YAP/TAZ in mechanotransduction. Nature 2011, 474, 179–183. [Google Scholar] [CrossRef] [PubMed]
- Nakajima, H.; Yamamoto, K.; Agarwala, S.; Terai, K.; Fukui, H.; Fukuhara, S.; Ando, K.; Miyazaki, T.; Yokota, Y.; Schmelzer, E. Flow-dependent endothelial YAP regulation contributes to vessel maintenance. Dev. Cell 2017, 40, 523–536.e6. [Google Scholar] [CrossRef] [PubMed]
- Gegenfurtner, F.A.; Jahn, B.; Wagner, H.; Ziegenhain, C.; Enard, W.; Geistlinger, L.; Rädler, J.O.; Vollmar, A.M.; Zahler, S. Micropatterning as a tool to identify regulatory triggers and kinetics of actin-mediated endothelial mechanosensing. J. Cell Sci. 2018, 131, 212886. [Google Scholar] [CrossRef]
- Dickson, M.C.; Martin, J.S.; Cousins, F.M.; Kulkarni, A.B.; Karlsson, S.; Akhurst, R.J. Defective haematopoiesis and vasculogenesis in transforming growth factor-beta 1 knock out mice. Development 1995, 121, 1845–1854. [Google Scholar]
- Oshima, M.; Oshima, H.; Taketo, M.M. TGF-β receptor type II deficiency results in defects of yolk sac hematopoiesis and vasculogenesis. Dev. Biol. 1996, 179, 297–302. [Google Scholar] [CrossRef]
- Larsson, J.; Goumans, M.J.; Sjöstrand, L.J.; van Rooijen, M.A.; Ward, D.; Levéen, P.; Xu, X.; ten Dijke, P.; Mummery, C.L.; Karlsson, S. Abnormal angiogenesis but intact hematopoietic potential in TGF-β type I receptor-deficient mice. EMBO J. 2001, 20, 1663–1673. [Google Scholar] [CrossRef] [PubMed]
- Pefani, D.E.; Pankova, D.; Abraham, A.G.; Grawenda, A.M.; Vlahov, N.; Scrace, S. TGF-β Targets the Hippo Pathway Scaffold RASSF1A to Facilitate YAP/SMAD2 Nuclear Translocation. Mol. Cell 2016, 63, 156–166. [Google Scholar] [CrossRef] [PubMed]
- Ma, B.; Cheng, H.; Gao, R.; Mu, C.; Chen, L.; Wu, S.; Chen, Q.; Zhu, Y. Zyxin-Siah2–Lats2 axis mediates cooperation between Hippo and TGF-β signalling pathways. Nat. Commun. 2016, 7, 11123. [Google Scholar] [CrossRef] [PubMed]
- Young, K.; Tweedie, E.; Conley, B.; Ames, J.; FitzSimons, M.; Brooks, P.; Liaw, L.; Vary, C.P.H. BMP9 crosstalk with the hippo pathway regulates endothelial cell matricellular and chemokine responses. PLoS ONE 2015, 10, e0122892. [Google Scholar] [CrossRef] [PubMed]
- Singh, K.K.; Matkar, P.N.; Quan, A.; Mantella, L.-E.; Teoh, H.; Al-Omran, M.; Verma, S. Investigation of TGFβ1-induced long noncoding RNAs in endothelial cells. Int. J. Vasc. Med. 2016, 2016, 2459687. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Clevers, H. Wnt/β-Catenin Signaling in Development and Disease. Cell 2006, 127, 469–480. [Google Scholar] [CrossRef] [PubMed]
- Hot, B.; Valnohova, J.; Arthofer, E.; Simon, K.; Shin, J.; Uhlén, M.; Kostenis, E.; Mulder, J.; Schulte, G. FZD10-Gα13 signalling axis points to a role of FZD10 in CNS angiogenesis. Cell. Signal. 2017, 32, 93–103. [Google Scholar] [CrossRef] [PubMed]
- Park, H.W.; Kim, Y.C.; Yu, B.; Moroishi, T.; Mo, J.-S.; Plouffe, S.W.; Meng, Z.; Lin, K.C.; Yu, F.-X.; Alexander, C.M. Alternative Wnt signaling activates YAP/TAZ. Cell 2015, 162, 780–794. [Google Scholar] [CrossRef]
- Min, J.-K.; Park, H.; Choi, H.-J.; Kim, Y.; Pyun, B.-J.; Agrawal, V.; Song, B.-W.; Jeon, J.; Maeng, Y.-S.; Rho, S.-S. The WNT antagonist Dickkopf2 promotes angiogenesis in rodent and human endothelial cells. J. Clin. Investig. 2011, 121, 1882–1893. [Google Scholar] [CrossRef] [PubMed]
- Podgrabinska, S.; Braun, P.; Velasco, P.; Kloos, B.; Pepper, M.S.; Jackson, D.G.; Skobe, M. Molecular characterization of lymphatic endothelial cells. Proc. Natl. Acad. Sci. USA 2002, 99, 16069–16074. [Google Scholar] [CrossRef] [PubMed]
- Reneman, R.S.; Arts, T.; Hoeks, A.P.G. Wall shear stress–an important determinant of endothelial cell function and structure–in the arterial system in vivo. J. Vasc. Res. 2006, 3, 251–269. [Google Scholar] [CrossRef] [PubMed]
- Lee, H.J.; Diaz, M.F.; Price, K.M.; Ozuna, J.A.; Zhang, S.; Sevick-Muraca, E.M.; Hagan, J.P.; Wenzel, P.L. Fluid shear stress activates YAP1 to promote cancer cell motility. Nat. Commun. 2017, 8, 14122. [Google Scholar] [CrossRef]
- Ivanov, K.I.; Agalarov, Y.; Valmu, L.; Samuilova, O.; Liebl, J.; Houhou, N.; Maby-El Hajjami, H.; Norrmén, C.; Jaquet, M.; Miura, N.; et al. Phosphorylation regulates FOXC2-mediated transcription in lymphatic endothelial cells. Mol. Cell. Biol. 2013, 33, 3749–3761. [Google Scholar] [CrossRef] [PubMed]
- Sabine, A.; Bovay, E.; Demir, C.S.; Kimura, W.; Jaquet, M.; Agalarov, Y.; Zangger, N.; Scallan, J.P.; Graber, W.; Gulpinar, E. FOXC2 and fluid shear stress stabilize postnatal lymphatic vasculature. J. Clin. Investig. 2015, 125, 3861–3877. [Google Scholar] [CrossRef]
- Johnson, N.C.; Dillard, M.E.; Baluk, P.; McDonald, D.M.; Harvey, N.L.; Frase, S.L.; Oliver, G. Lymphatic endothelial cell identity is reversible and its maintenance requires Prox1 activity. Genes Dev. 2008, 22, 3282–3291. [Google Scholar] [CrossRef]
- Cho, H.; Kim, J.; Ahn, J.H.; Hong, Y.-K.; Mäkinen, T.; Lim, D.-S.; Koh, G.Y. YAP and TAZ Negatively Regulate Prox1 During Developmental and Pathologic Lymphangiogenesis. Circ. Res. 2019, 124, 225–242. [Google Scholar] [CrossRef]
- Patan, S. Vasculogenesis and angiogenesis. Cancer Treat. Res. 2004, 117, 3–32. [Google Scholar]
- 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. 2006, 26, 77–87. [Google Scholar] [CrossRef]
- Nagasawa-Masuda, A.; Terai, K. Yap/Taz transcriptional activity is essential for vascular regression via Ctgf expression and actin polymerization. PLoS ONE 2017, 12, e0174633. [Google Scholar] [CrossRef]
- Brigstock, D.R. Regulation of angiogenesis and endothelial cell function by connective tissue growth factor (CTGF) and cysteine-rich 61 (CYR61). Angiogenesis 2002, 5, 153–165. [Google Scholar] [CrossRef]
- Chaqour, B.; Goppelt-Struebe, M. Mechanical regulation of the Cyr61/CCN1 and CTGF/CCN2 proteins. Fed. Eur. Biochem. Soc. J. 2006, 273, 3639–3649. [Google Scholar] [CrossRef]
- Jiang, W.G.; Watkins, G.; Fodstad, O.; Douglas-Jones, A.; Mokbel, K.; Mansel, R.E. Differential expression of the CCN family members Cyr61, CTGF and Nov in human breast cancer. Endocr. Relat. Cancer 2004, 11, 781–791. [Google Scholar] [CrossRef] [PubMed]
- Lai, D.; Ho, K.C.; Hao, Y.; Yang, X. Taxol resistance in breast cancer cells is mediated by the hippo pathway component TAZ and its downstream transcriptional targets Cyr61 and CTGF. Cancer Res. 2011, 71, 2728–2738. [Google Scholar] [CrossRef]
- Neto, F.; Klaus-Bergmann, A.; Ong, Y.T.; Alt, S.; Vion, A.-C.; Szymborska, A.; Carvalho, J.R.; Hollfinger, I.; Bartels-Klein, E.; Franco, C.A. YAP and TAZ regulate adherens junction dynamics and endothelial cell distribution during vascular development. eLife 2018, 7, e31037. [Google Scholar] [CrossRef] [PubMed]
- 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. 2015, 6, 6943. [Google Scholar] [CrossRef] [PubMed]
- Sakabe, M.; Fan, J.; Odaka, Y.; Liu, N.; Hassan, A.; Duan, X.; Stump, P.; Byerly, L.; Donaldson, M.; Hao, J. YAP/TAZ-CDC42 signaling regulates vascular tip cell migration. Proc. Natl. Acad. Sci. USA 2017, 114, 10918–10923. [Google Scholar] [CrossRef]
- Olsson, A.-K.; Dimberg, A.; Kreuger, J.; Claesson-Welsh, L. VEGF receptor signalling? In control of vascular function. Nat. Rev. Mol. Cell Biol. 2006, 7, 359. [Google Scholar] [CrossRef]
- Ferrara, N.; Gerber, H.-P.; LeCouter, J. The biology of VEGF and its receptors. Nat. Med. 2003, 9, 669. [Google Scholar] [CrossRef]
- Azad, T.; Nouri, K.; van Rensburg Janse, H.J.; Hao, Y.; Yang, X. Monitoring Hippo Signaling Pathway Activity Using a Luciferase-based Large Tumor Suppressor (LATS) Biosensor. J. Vis. Exp. 2018, E58416. [Google Scholar] [CrossRef]
- Azad, T.; van Rensburg, H.J.J.; Lightbody, E.D.; Neveu, B.; Champagne, A.; Ghaffari, A.; Kay, V.R.; Hao, Y.; Shen, H.; Yeung, B. A LATS biosensor screen identifies VEGFR as a regulator of the Hippo pathway in angiogenesis. Nat. Commun. 2018, 9, 1061. [Google Scholar] [CrossRef]
- Wang, X.; Valls, A.F.; Schermann, G.; Shen, Y.; Moya, I.M.; Castro, L.; Urban, S.; Solecki, G.M.; Winkler, F.; Riedemann, L. YAP/TAZ orchestrate VEGF signaling during developmental angiogenesis. Dev. Cell 2017, 42, 462–478.e7. [Google Scholar] [CrossRef]
- He, J.; Bao, Q.; Zhang, Y.; Liu, M.; Lv, H.; Liu, Y.; Yao, L.; Li, B.; Zhang, C.; He, S. Yes-associated protein promotes angiogenesis via signal transducer and activator of transcription 3 in endothelial cells. Circ. Res. 2018, 122, 591–605. [Google Scholar] [CrossRef]
- Bergers, G.; Song, S. The role of pericytes in blood-vessel formation and maintenance. Neuro Oncol. 2005, 7, 452–464. [Google Scholar] [CrossRef]
- Paiva, A.E.; Lousado, L.; Guerra, D.A.; Azevedo, P.O.; Sena, I.F.; Andreotti, J.P.; Santos, G.S.; Gonçalves, R.; Mintz, A.; Birbrair, A. Pericytes in the premetastatic niche. Cancer Res. 2018, 78, 2779–2786. [Google Scholar] [CrossRef]
- Kato, K.; Diéguez-Hurtado, R.; Hong, S.P.; Kato-Azuma, S.; Adams, S.; Stehling, M.; Trappmann, B.; Wrana, J.L.; Koh, G.Y.; Adams, R.H. Pulmonary pericytes regulate lung morphogenesis. Nat. Commun. 2018, 9, 2448. [Google Scholar] [CrossRef]
- Tímár, J.; Döme, B.; Fazekas, K.; Janovics, Á.; Paku, S. Angiogenesis-dependent diseases and angiogenesis therapy. Pathol. Oncol. Res. 2001, 7, 85–94. [Google Scholar] [CrossRef] [PubMed]
- Barreto, S.; Gonzalez-Vazquez, A.; Cameron, A.R.; Cavanagh, B.; Murray, D.J.; O’Brien, F.J. Identification of the mechanisms by which age alters the mechanosensitivity of mesenchymal stromal cells on substrates of differing stiffness: Implications for osteogenesis and angiogenesis. Acta Biomater. 2017, 53, 59–69. [Google Scholar] [CrossRef] [PubMed]
- Goetzl, E.J.; Schwartz, J.B.; Mustapic, M.; Lobach, I.V.; Daneman, R.; Abner, E.L.; Jicha, G.A. Altered cargo proteins of human plasma endothelial cell–derived exosomes in atherosclerotic cerebrovascular disease. FASEB J. 2017, 31, 3689–3694. [Google Scholar] [CrossRef] [PubMed]
- Lin, M.; Yuan, W.; Su, Z.; Lin, C.; Huang, T.; Chen, Y.; Wang, J. Yes-associated protein mediates angiotensin II-induced vascular smooth muscle cell phenotypic modulation and hypertensive vascular remodelling. Cell Prolif. 2018, 51, e12517. [Google Scholar] [CrossRef]
- Bharadwaj, A.S.; Appukuttan, B.; Wilmarth, P.A.; Pan, Y.; Stempel, A.J.; Chipps, T.J.; Benedetti, E.E.; Zamora, D.O.; Choi, D.; David, L.L. Role of the retinal vascular endothelial cell in ocular disease. Prog. Retin. Eye Res. 2013, 32, 102–180. [Google Scholar] [CrossRef] [PubMed]
- Yan, Z.; Shi, H.; Zhu, R.; Li, L.; Qin, B.; Kang, L.; Chen, H.; Guan, H. Inhibition of YAP ameliorates choroidal neovascularization via inhibiting endothelial cell proliferation. Mol. Vis. 2018, 24, 83–93. [Google Scholar]
- Kim, J.; Kim, Y.H.; Kim, J.; Bae, H.; Lee, D.-H.; Kim, K.H.; Hong, S.P.; Jang, S.P.; Kubota, Y.; Kwon, Y.-G. YAP/TAZ regulates sprouting angiogenesis and vascular barrier maturation. J. Clin. Investig. 2017, 127, 3441–3461. [Google Scholar] [CrossRef]
- Zhu, M.; Liu, X.; Wang, Y.; Chen, L.; Wang, L.; Qin, X.; Xu, J.; Li, L.; Tu, Y.; Zhou, T. YAP via interacting with STAT3 regulates VEGF-induced angiogenesis in human retinal microvascular endothelial cells. Exp. Cell Res. 2018, 373, 155–163. [Google Scholar] [CrossRef]
- Hao, G.-M.; Lv, T.-T.; Wu, Y.; Wang, H.-L.; Xing, W.; Wang, Y.; Li, C.; Zhang, Z.-J.; Wang, Z.-L.; Wang, W. The Hippo signaling pathway: A potential therapeutic target is reversed by a Chinese patent drug in rats with diabetic retinopathy. BMC Complementary Altern. Med. 2017, 17, 187. [Google Scholar] [CrossRef]
- Um, J.; Yu, J.; Park, K.S. Substance P accelerates wound healing in type 2 diabetic mice through endothelial progenitor cell mobilization and Yes-associated protein activation. Mol. Med. Rep. 2017, 15, 3035–3040. [Google Scholar] [CrossRef]
- Xu, X.-M.; Xu, T.-M.; Wei, Y.-B.; Gao, X.-X.; Sun, J.-C.; Wang, Y.; Kong, Q.-J.; Shi, J.-G. Low-Intensity Pulsed Ultrasound Treatment Accelerates Angiogenesis by Activating YAP/TAZ in Human Umbilical Vein Endothelial Cells. Ultrasound Med. Biol. 2018, 44, 2655–2661. [Google Scholar] [CrossRef] [PubMed]
- Yuan, L.; Mao, Y.; Luo, W.; Wu, W.; Xu, H.; Wang, X.L.; Shen, Y.H. Palmitic acid dysregulates the Hippo-YAP pathway and inhibits angiogenesis by inducing mitochondrial damage and activating the cytosolic DNA sensor cGAS-STING-IRF3 signaling. J. Biol. Chem. 2017, 292, 15002–15015. [Google Scholar] [CrossRef]
- Mammoto, A.; Muyleart, M.; Kadlec, A.; Gutterman, D.; Mammoto, T. YAP1-TEAD1 signaling controls angiogenesis and mitochondrial biogenesis through PGC1α. Microvasc. Res. 2018, 119, 73–83. [Google Scholar] [CrossRef]
- Hanahan, D.; Weinberg, R.A. Hallmarks of cancer: The next generation. Cell 2011, 144, 646–674. [Google Scholar] [CrossRef] [PubMed]
- Xu, C.; Mao, L.; Xiong, J.; Wen, J.; Wang, Y.; Geng, D.; Liu, Y. TAZ Expression on Endothelial Cells Is Closely Related to Blood Vascular Density and VEGFR2 Expression in Astrocytomas. J. Neuropathol. Exp. Neurol. 2019, 78, 172–180. [Google Scholar] [CrossRef] [PubMed]
- Venkataramani, V.; Küffer, S.; Cheung, K.C.P.; Jiang, X.; Trümper, L.; Wulf, G.G.; Ströbel, P. CD31 expression determines redox status and chemoresistance in human angiosarcomas. Clin. Cancer Res. 2018, 24, 460–473. [Google Scholar] [CrossRef]
- Marti, P.; Stein, C.; Blumer, T.; Abraham, Y.; Dill, M.T.; Pikiolek, M.; Orsini, V.; Jurisic, G.; Megel, P.; Makowska, Z. YAP promotes proliferation, chemoresistance, and angiogenesis in human cholangiocarcinoma through TEAD transcription factors. Hepatology 2015, 62, 1497–1510. [Google Scholar] [CrossRef] [PubMed]
- Pan, Z.; Tian, Y.; Zhang, B.; Zhang, X.; Shi, H.; Liang, Z.; Wu, P.; Li, R.; You, B.; Yang, L. YAP signaling in gastric cancer-derived mesenchymal stem cells is critical for its promoting role in cancer progression. Int. J. Oncol. 2017, 51, 1055–1066. [Google Scholar] [CrossRef]
- Maniotis, A.J.; Folberg, R.; Hess, A.; Seftor, E.A.; Gardner, L.M.; Pe’er, J.; Trent, J.M.; Meltzer, P.S.; Hendrix, M.J. Vascular channel formation by human melanoma cells in vivo and in vitro: Vasculogenic mimicry. Am. J. Pathol. 1999, 155, 739–752. [Google Scholar] [CrossRef]
- Delgado-Bellido, D.; Serrano-Saenz, S.; Fernández-Cortés, M.; Oliver, F.J. Vasculogenic mimicry signaling revisited: Focus on non-vascular VE-cadherin. Mol. Cancer 2017, 16, 65. [Google Scholar] [CrossRef]
- Hendrix, M.J.; Seftor, E.A.; Seftor, R.E.; Chao, J.T.; Chien, D.S.; Chu, Y.W. Tumor cell vascular mimicry: Novel targeting opportunity in melanoma. Pharmacol. Ther. 2016, 159, 83–92. [Google Scholar] [CrossRef] [PubMed]
- Hendrix, M.J.; Seftor, E.A.; Hess, A.R.; Seftor, R.E. Vasculogenic mimicry and tumour-cell plasticity: Lessons from melanoma. Nat. Rev. Cancer 2003, 3, 411. [Google Scholar] [CrossRef]
- Shirakawa, K.; Kobayashi, H.; Heike, Y.; Kawamoto, S.; Brechbiel, M.W.; Kasumi, F.; Iwanaga, T.; Konishi, F.; Terada, M.; Wakasugi, H. Hemodynamics in vasculogenic mimicry and angiogenesis of inflammatory breast cancer xenograft. Cancer Res. 2002, 62, 560–566. [Google Scholar]
- Williamson, S.C.; Metcalf, R.L.; Trapani, F.; Mohan, S.; Antonello, J.; Abbott, B.; Leong, H.S.; Chester, C.P.; Simms, N.; Polanski, R. Vasculogenic mimicry in small cell lung cancer. Nat. Commun. 2016, 7, 13322. [Google Scholar] [CrossRef]
- Sood, A.K.; Seftor, E.A.; Fletcher, M.S.; Gardner, L.M.; Heidger, P.M.; Buller, R.E.; Seftor, R.E.; Hendrix, M.J. Molecular determinants of ovarian cancer plasticity. Am. J. Pathol. 2001, 158, 1279–1288. [Google Scholar] [CrossRef]
- Cai, X.S.; Jia, Y.W.; Mei, J.; Tang, R.Y. Tumor blood vessels formation in osteosarcoma: Vasculogenesis mimicry. Chin. Med. J. 2004, 117, 94–98. [Google Scholar]
- Li, M.; Gu, Y.; Zhang, Z.; Zhang, S.; Zhang, D.; Saleem, A.F.; Zhao, X.; Sun, B. Vasculogenic mimicry: A new prognostic sign of gastric adenocarcinoma. Pathol. Oncol. Res. 2010, 16, 259–266. [Google Scholar] [CrossRef] [PubMed]
- Streeter, E.H.; Harris, A.L. Angiogenesis in bladder cancer—Prognostic marker and target for future therapy. Surg. Oncol. 2002, 11, 85–100. [Google Scholar] [CrossRef]
- Sun, T.; Sun, B.C.; Zhao, X.L.; Zhao, N.; Dong, X.Y.; Che, N.; Yao, Z.; Ma, Y.M.; Gu, Q.; Zong, W.K. Promotion of tumor cell metastasis and vasculogenic mimicry by way of transcription coactivation by Bcl-2 and Twist1: A study of hepatocellular carcinoma. Hepatology 2011, 54, 1690–1706. [Google Scholar] [CrossRef] [PubMed]
- Baeten, C.I.; Hillen, F.; Pauwels, P.; de Bruine, A.P.; Baeten, C.G. Prognostic role of vasculogenic mimicry in colorectal cancer. Dis. Colon Rectum 2009, 52, 2028–2035. [Google Scholar] [CrossRef] [PubMed]
- Bora-Singhal, N.; Nguyen, J.; Schaal, C.; Perumal, D.; Singh, S.; Coppola, D.; Chellappan, S. YAP1 regulates OCT4 activity and SOX2 expression to facilitate self-renewal and vascular mimicry of stem-like cells. Stem Cells 2015, 33, 1705–1718. [Google Scholar] [CrossRef]
- Wei, H.; Wang, F.; Wang, Y.; Li, T.; Xiu, P.; Zhong, J.; Sun, X.; Li, J. Verteporfin suppresses cell survival, angiogenesis and vasculogenic mimicry of pancreatic ductal adenocarcinoma via disrupting the YAP-TEAD complex. Cancer Sci. 2017, 108, 478–487. [Google Scholar] [CrossRef]
- van Rensburg, H.J.J.; Azad, T.; Ling, M.; Hao, Y.; Snetsinger, B.; Khanal, P.; Minassian, L.M.; Graham, C.H.; Rauh, M.J.; Yang, X. The Hippo pathway component TAZ promotes immune evasion in human cancer through PD-L1. Cancer Res. 2018, 78, 1457–1470. [Google Scholar] [CrossRef]
- Cross, M.J.; Claesson-Welsh, L. FGF and VEGF function in angiogenesis: Signalling pathways, biological responses and therapeutic inhibition. Trends Pharmacol. Sci. 2001, 22, 201–207. [Google Scholar] [CrossRef]
- Zhao, Y.; Adjei, A.A. Targeting angiogenesis in cancer therapy: Moving beyond vascular endothelial growth factor. Oncologist 2015, 20, 660–673. [Google Scholar] [CrossRef]
Main Finding | Ref. |
---|---|
Angiomotin is a negative regulator of YAP | [44] |
Angiomotin-like 1 degradation by Nedd4 is regulated by YAP through c-ABL | [60] |
YAP/TAZ are the main mediators of mechanotransduction in endothelial cells | [72] |
BMP9 crosstalk with the Hippo pathway regulates endothelial cell matricellular response | [80] |
mRNAs upregulated in ECs in response to TGFβ1 treatment are involved in hippo signaling | [81] |
Flow-dependent endothelial YAP regulation contributes to vessel maintenance | [73] |
YAP/TAZ negatively regulate prox1 during developmental and pathologic lymphangiogenesis | [92] |
YAP disruption in mice causes defects in yolk sac vasculogenesis and chorioallantoic fusion | [94] |
YAP/TAZ activity is essential for vascular regression via Ctgf and actin polymerization | [95] |
Adherens junction and endothelial cell distribution in angiogenesis is regulated by YAP/TAZ | [100] |
YAP regulates angiopoietin-2 expression in ECs | [101] |
Vascular tip cell migration is regulated by YAP/TAZ-CDC42 signaling pathway | [102] |
VEGFR is a regulator of YAP/TAZ in the Hippo pathway in angiogenesis through PI3K/MAPK pathways | [106] |
VEGF activates YAP/TAZ via its effects on actin cytoskeleton | [107] |
YAP promotes angiogenesis via Stat3 | [108] |
YAP mediates angiotensin II-induced vascular smooth muscle cell phenotypic modulation and hypertensive vascular remodelling | [115] |
YAP inhibition ameliorates choroidal neovascularization | [117] |
YAP/TAZ regulates vascular barrier maturation | [118] |
YAP via interacting with STAT3 regulates VEGF-induced angiogenesis in retina | [119] |
Substance P accelerates wound healing in type 2 diabetic mice through YAP activation | [121] |
Ultrasound treatment accelerates angiogenesis by activating YAP/TAZ | [122] |
Palmitic acid inhibits angiogenesis through YAP suppression | [123] |
YAP1-TEAD1 controls angiogenesis and mitochondrial biogenesis through PGC1α. | [124] |
Blood vascular density and VEGFR2 expression in astrocytomas is regulated by TAZ | [126] |
Cell proliferation, chemoresistance, and angiogenesis in human cholangiocarcinoma is regulated by YAP | [128] |
YAP regulates OCT4 activity and SOX2 expression to facilitate vascular mimicry | [142] |
Verteporfin suppresses vasculogenic mimicry of pancreatic ductal adenocarcinoma | [143] |
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Azad, T.; Ghahremani, M.; Yang, X. The Role of YAP and TAZ in Angiogenesis and Vascular Mimicry. Cells 2019, 8, 407. https://doi.org/10.3390/cells8050407
Azad T, Ghahremani M, Yang X. The Role of YAP and TAZ in Angiogenesis and Vascular Mimicry. Cells. 2019; 8(5):407. https://doi.org/10.3390/cells8050407
Chicago/Turabian StyleAzad, Taha, Mina Ghahremani, and Xiaolong Yang. 2019. "The Role of YAP and TAZ in Angiogenesis and Vascular Mimicry" Cells 8, no. 5: 407. https://doi.org/10.3390/cells8050407
APA StyleAzad, T., Ghahremani, M., & Yang, X. (2019). The Role of YAP and TAZ in Angiogenesis and Vascular Mimicry. Cells, 8(5), 407. https://doi.org/10.3390/cells8050407