DOI QR코드

DOI QR Code

Hippo-YAP/TAZ signaling in angiogenesis

  • Park, Jeong Ae (Department of Biochemistry, College of Life Science and Biotechnology, Yonsei University) ;
  • Kwon, Young-Guen (Department of Biochemistry, College of Life Science and Biotechnology, Yonsei University)
  • Received : 2017.12.21
  • Published : 2018.03.31

Abstract

Angiogenesis is a complex, multistep process involving dynamic changes in endothelial cell (EC) shapes and behaviors, especially in specialized cell types such as tip cells (with active filopodial extensions), stalk cells (with less motility) and phalanx cells (with stable junction connections). The Hippo-Yes-associated protein (YAP)/ transcription activator with PDZ binding motif (TAZ) signaling plays a critical role in development, regeneration and organ size by regulating cell-cell contact and actin cytoskeleton dynamics. Recently, with the finding that YAP is expressed in the front edge of the developing retinal vessels, Hippo-YAP/TAZ signaling has emerged as a new pathway for blood vessel development. Intriguingly, the LATS1/2-mediated angiomotin (AMOT) family and YAP/TAZ activities contribute to EC shapes and behaviors by spatiotemporally modulating actin cytoskeleton dynamics and EC junction stability. Herein, we summarize the recent understanding of the role of Hippo-YAP/TAZ signaling in the processes of EC sprouting and junction maturation in angiogenesis.

Keywords

References

  1. Herbert SP and Stainier DY (2011) Molecular control of endothelial cell behaviour during blood vessel morphogenesis. Nat Rev Mol Cell Biol 12, 551-564
  2. Potente M, Urbich C, Sasaki K et al (2005) Involvement of Foxo transcription factors in angiogenesis and postnatal neovascularization. J Clin Invest 115, 2382-2392 https://doi.org/10.1172/JCI23126
  3. Birdsey GM, Dryden NH, Amsellem V et al (2008) Transcription factor Erg regulates angiogenesis and endothelial apoptosis through VE-cadherin. Blood 111, 3498-3506 https://doi.org/10.1182/blood-2007-08-105346
  4. Felcht M, Luck R, Schering A et al (2012) Angiopoietin-2 differentially regulates angiogenesis through TIE2 and integrin signaling. J Clin Invest 122, 1991-2005 https://doi.org/10.1172/JCI58832
  5. Nakayama M, Nakayama A, van Lessen M et al (2013) Spatial regulation of VEGF receptor endocytosis in angiogenesis. Nat Cell Biol 15, 249-260 https://doi.org/10.1038/ncb2679
  6. Kume T (2008) Foxc2 transcription factor: a newly described regulator of angiogenesis. Trends Cardiovasc Med 18, 224-228 https://doi.org/10.1016/j.tcm.2008.11.003
  7. Yu FX, Zhao B and Guan KL (2015) Hippo pathway in organ size control, tissue homeostasis, and cancer. Cell 163, 811-828 https://doi.org/10.1016/j.cell.2015.10.044
  8. Sun S and Irvine KD (2016) Cellular Organization and Cytoskeletal Regulation of the Hippo Signaling Network. Trends Cell Biol 26, 694-704 https://doi.org/10.1016/j.tcb.2016.05.003
  9. Zhao B, Li L, Tumaneng K, Wang CY and Guan KL (2010) A coordinated phosphorylation by Lats and CK1 regulates YAP stability through SCF(beta-TRCP). Genes Dev 24, 72-85 https://doi.org/10.1101/gad.1843810
  10. Hansen CG, Moroishi T and Guan KL (2015) YAP and TAZ: a nexus for Hippo signaling and beyond. Trends Cell Biol 25, 499-513 https://doi.org/10.1016/j.tcb.2015.05.002
  11. Morin-Kensicki EM, Boone BN, Howell M et al (2006) Defects in yolk sac vasculogenesis, chorioallantoic fusion, and embryonic axis elongation in mice with targeted disruption of Yap65. Mol Cell Biol 26, 77-87 https://doi.org/10.1128/MCB.26.1.77-87.2006
  12. Choi HJ, Zhang H, Park H et al (2015) Yes-associated protein regulates endothelial cell contact-mediated expression of angiopoietin-2. Nat Commun 6, 6943 https://doi.org/10.1038/ncomms7943
  13. Glienke J, Schmitt AO, Pilarsky C et al (2000) Differential gene expression by endothelial cells in distinct angiogenic states. Eur J Biochem 267, 2820-2830 https://doi.org/10.1046/j.1432-1327.2000.01325.x
  14. Min JK, Park H, Choi HJ et al (2011) The WNT antagonist Dickkopf2 promotes angiogenesis in rodent and human endothelial cells. J Clin Invest 121, 1882-1893 https://doi.org/10.1172/JCI42556
  15. Park HW, Kim YC, Yu B et al (2015) Alternative Wnt Signaling Activates YAP/TAZ. Cell 162, 780-794 https://doi.org/10.1016/j.cell.2015.07.013
  16. Bentley K, Franco CA, Philippides A et al (2014) The role of differential VE-cadherin dynamics in cell rearrangement during angiogenesis. Nat Cell Biol 16, 309-321 https://doi.org/10.1038/ncb2926
  17. Zihni C, Mills C, Matter K and Balda MS (2016) Tight junctions: from simple barriers to multifunctional molecular gates. Nat Rev Mol Cell Biol 17, 564-580 https://doi.org/10.1038/nrm.2016.80
  18. Lamalice L, Le Boeuf F and Huot J (2007) Endothelial cell migration during angiogenesis. Circ Res 100, 782-794 https://doi.org/10.1161/01.RES.0000259593.07661.1e
  19. Wang X, Freire Valls A, Schermann G et al (2017) YAP/TAZ Orchestrate VEGF Signaling during Developmental Angiogenesis. Dev Cell 42, 462-478 e467 https://doi.org/10.1016/j.devcel.2017.08.002
  20. Moleirinho S, Guerrant W and Kissil JL (2014) The Angiomotins--from discovery to function. FEBS Lett 588, 2693-2703 https://doi.org/10.1016/j.febslet.2014.02.006
  21. Aase K, Ernkvist M, Ebarasi L et al (2007) Angiomotin regulates endothelial cell migration during embryonic angiogenesis. Genes Dev 21, 2055-2068 https://doi.org/10.1101/gad.432007
  22. Zheng Y, Vertuani S, Nystrom S et al (2009) Angiomotinlike protein 1 controls endothelial polarity and junction stability during sprouting angiogenesis. Circ Res 105, 260-270 https://doi.org/10.1161/CIRCRESAHA.109.195156
  23. Kim J, Kim YH, Kim J et al (2017) YAP/TAZ regulates sprouting angiogenesis and vascular barrier maturation. J Clin Invest 127, 3441-3461 https://doi.org/10.1172/JCI93825
  24. Barry DM, Xu K, Meadows SM et al (2015) Cdc42 is required for cytoskeletal support of endothelial cell adhesion during blood vessel formation in mice. Development 142, 3058-3070 https://doi.org/10.1242/dev.125260
  25. Park H, Jung HY, Choi HJ et al (2014) Distinct roles of DKK1 and DKK2 in tumor angiogenesis. Angiogenesis 17, 221-234 https://doi.org/10.1007/s10456-013-9390-5
  26. Garnaas MK, Moodie KL, Liu ML et al (2008) Syx, a RhoA guanine exchange factor, is essential for angiogenesis in vivo. Circ Res 103, 710-716 https://doi.org/10.1161/CIRCRESAHA.108.181388
  27. Ernkvist M, Luna Persson N, Audebert S et al (2009) The Amot/Patj/Syx signaling complex spatially controls RhoA GTPase activity in migrating endothelial cells. Blood 113, 244-253 https://doi.org/10.1182/blood-2008-04-153874
  28. Iruela-Arispe ML and Davis GE (2009) Cellular and molecular mechanisms of vascular lumen formation. Dev Cell 16, 222-231 https://doi.org/10.1016/j.devcel.2009.01.013
  29. Iden S, Rehder D, August B et al (2006) A distinct PAR complex associates physically with VE-cadherin in vertebrate endothelial cells. EMBO Rep 7, 1239-1246 https://doi.org/10.1038/sj.embor.7400819
  30. Koh W, Mahan RD and Davis GE (2008) Cdc42- and Rac1-mediated endothelial lumen formation requires Pak2, Pak4 and Par3, and PKC-dependent signaling. J Cell Sci 121, 989-1001 https://doi.org/10.1242/jcs.020693
  31. Xu K, Sacharidou A, Fu S et al (2011) Blood vessel tubulogenesis requires Rasip1 regulation of GTPase signaling. Dev Cell 20, 526-539 https://doi.org/10.1016/j.devcel.2011.02.010
  32. Hultin S, Subramani A, Hildebrand S, Zheng Y, Majumdar A and Holmgren L (2017) AmotL2 integrates polarity and junctional cues to modulate cell shape. Sci Rep 7, 7548 https://doi.org/10.1038/s41598-017-07968-1
  33. Hultin S, Zheng Y, Mojallal M et al (2014) AmotL2 links VE-cadherin to contractile actin fibres necessary for aortic lumen expansion. Nat Commun 5, 3743
  34. Wang Y, Li Z, Xu P et al (2011) Angiomotin-like2 gene (amotl2) is required for migration and proliferation of endothelial cells during angiogenesis. J Biol Chem 286, 41095-41104 https://doi.org/10.1074/jbc.M111.296806
  35. Kouklis P, Konstantoulaki M, Vogel S, Broman M and Malik AB (2004) Cdc42 regulates the restoration of endothelial barrier function. Circ Res 94, 159-166 https://doi.org/10.1161/01.RES.0000110418.38500.31
  36. Komarova YA, Kruse K, Mehta D and Malik AB (2017) Protein Interactions at Endothelial Junctions and Signaling Mechanisms Regulating Endothelial Permeability. Circ Res 120, 179-206 https://doi.org/10.1161/CIRCRESAHA.116.306534
  37. Wada K, Itoga K, Okano T, Yonemura S and Sasaki H (2011) Hippo pathway regulation by cell morphology and stress fibers. Development 138, 3907-3914 https://doi.org/10.1242/dev.070987
  38. Choi KS, Choi HJ, Lee JK et al (2016) The endothelial E3 ligase HECW2 promotes endothelial cell junctions by increasing AMOTL1 protein stability via K63-linked ubiquitination. Cell Signal 28, 1642-1651 https://doi.org/10.1016/j.cellsig.2016.07.015
  39. Skouloudaki K and Walz G (2012) YAP1 recruits c-Abl to protect angiomotin-like 1 from Nedd4-mediated degradation. PLoS One 7, e35735 https://doi.org/10.1371/journal.pone.0035735
  40. Sakabe M, Fan J, Odaka Y et al (2017) YAP/TAZ-CDC42 signaling regulates vascular tip cell migration. Proc Natl Acad Sci U S A 114, 10918-10923
  41. Napione L, Pavan S, Veglio A et al (2012) Unraveling the influence of endothelial cell density on VEGF-A signaling. Blood 119, 5599-5607 https://doi.org/10.1182/blood-2011-11-390666
  42. Chen J, Somanath PR, Razorenova O et al (2005) Akt1 regulates pathological angiogenesis, vascular maturation and permeability in vivo. Nat Med 11, 1188-1196 https://doi.org/10.1038/nm1307
  43. Bernascone I and Martin-Belmonte F (2013) Crossroads of Wnt and Hippo in epithelial tissues. Trends Cell Biol 23, 380-389 https://doi.org/10.1016/j.tcb.2013.03.007
  44. Basu S, Totty NF, Irwin MS, Sudol M and Downward J (2003) Akt phosphorylates the Yes-associated protein, YAP, to induce interaction with 14-3-3 and attenuation of p73-mediated apoptosis. Mol Cell 11, 11-23 https://doi.org/10.1016/S1097-2765(02)00776-1
  45. Giampietro C, Disanza A, Bravi L et al (2015) The actin-binding protein EPS8 binds VE-cadherin and modulates YAP localization and signaling. J Cell Biol 211, 1177-1192 https://doi.org/10.1083/jcb.201501089
  46. Nakajima H, Yamamoto K, Agarwala S et al (2017) Flow-Dependent Endothelial YAP Regulation Contributes to Vessel Maintenance. Dev Cell 40, 523-536 e526 https://doi.org/10.1016/j.devcel.2017.02.019
  47. Young K, Tweedie E, Conley B et al (2015) BMP9 Crosstalk with the Hippo Pathway Regulates Endothelial Cell Matricellular and Chemokine Responses. PLoS One 10, e0122892 https://doi.org/10.1371/journal.pone.0122892
  48. Yu FX, Zhao B, Panupinthu N et al (2012) Regulation of the Hippo-YAP pathway by G-protein-coupled receptor signaling. Cell 150, 780-791 https://doi.org/10.1016/j.cell.2012.06.037
  49. Kim W, Khan SK, Gvozdenovic-Jeremic J et al (2017) Hippo signaling interactions with Wnt/beta-catenin and Notch signaling repress liver tumorigenesis. J Clin Invest 127, 137-152

Cited by

  1. Cardiac Progenitor Cell–Derived Extracellular Vesicles Reduce Infarct Size and Associate with Increased Cardiovascular Cell Proliferation pp.1937-5395, 2018, https://doi.org/10.1007/s12265-018-9842-9
  2. Convergence of VEGF and YAP/TAZ signaling: Implications for angiogenesis and cancer biology vol.11, pp.552, 2018, https://doi.org/10.1126/scisignal.aau1165
  3. Putting VE-cadherin into JAIL for junction remodeling vol.132, pp.1, 2019, https://doi.org/10.1242/jcs.222893