BMB Reports

Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
권호 표지
DOI QR코드

DOI QR Code

Regulation of Hippo signaling by actin remodeling

  • Seo, Jimyung (Graduate School of Medical Science and Engineering, KAIST) ;
  • Kim, Joon (Graduate School of Medical Science and Engineering, KAIST)
  • Received : 2017.12.21
  • Published : 2018.03.31
Download PDF
⟨ Previous Next ⟩

Abstract

The Hippo signaling pathway controls nuclear accumulation and stability of the transcriptional coregulator YAP and its paralog TAZ. The activity of Hippo-YAP signaling is influenced not only by biochemical signals, but also by cell shape and mechanical tension transmitted through cell-cell junctions and cell-matrix adhesions. Data accumulated thus far indicates that the actin cytoskeleton is a key mediator of the regulation of Hippo-YAP signaling by means of a variety of biochemical and mechanical cues. In this review, we have outlined the role of actin dynamics and actin-associated proteins in the regulation of Hippo-YAP signaling. In addition, we discuss actin-mediated regulation of YAP/TAZ activity independent of the core Hippo kinases MST and LATS. Although our understanding of the link between Hippo-YAP signaling and the actin cytoskeleton is progressing rapidly, many open questions remain.

Keywords

References

  1. Panciera T, Azzolin L, Cordenonsi M and Piccolo S (2017) Mechanobiology of YAP and TAZ in physiology and disease. Nat Rev Mol Cell Biol 18, 758-770 https://doi.org/10.1038/nrm.2017.87
  2. Yu FX and Guan KL (2013) The Hippo pathway: regulators and regulations. Genes Dev 27, 355-371 https://doi.org/10.1101/gad.210773.112
  3. Piccolo S, Dupont S and Cordenonsi M (2014) The biology of YAP/TAZ: hippo signaling and beyond. Physiol Rev 94, 1287-1312 https://doi.org/10.1152/physrev.00005.2014
  4. 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
  5. Gaspar P and Tapon N (2014) Sensing the local environment: actin architecture and Hippo signalling. Curr Opin Cell Biol 31, 74-83 https://doi.org/10.1016/j.ceb.2014.09.003
  6. Matsui Y and Lai ZC (2013) Mutual regulation between Hippo signaling and actin cytoskeleton. Protein Cell 4, 904-910 https://doi.org/10.1007/s13238-013-3084-z
  7. Murrell M, Oakes PW, Lenz M and Gardel ML (2015) Forcing cells into shape: the mechanics of actomyosin contractility. Nat Rev Mol Cell Biol 16, 486-498 https://doi.org/10.1038/nrm4012
  8. Low BC, Pan CQ, Shivashankar GV, Bershadsky A, Sudol M and Sheetz M (2014) YAP/TAZ as mechanosensors and mechanotransducers in regulating organ size and tumor growth. FEBS Lett 588, 2663-2670 https://doi.org/10.1016/j.febslet.2014.04.012
  9. Meng Z, Moroishi T, Guan KL (2016) Mechanisms of Hippo pathway regulation. Genes Dev 30, 1-17 https://doi.org/10.1101/gad.274027.115
  10. Aragona M, Panciera T, Manfrin A et al (2013) A mechanical checkpoint controls multicellular growth through YAP/TAZ regulation by actin-processing factors. Cell 154, 1047-1059 https://doi.org/10.1016/j.cell.2013.07.042
  11. Zhao B, Li L, Wang L, Wang CY, Yu J and Guan KL (2012) Cell detachment activates the Hippo pathway via cytoskeleton reorganization to induce anoikis. Genes Dev 26, 54-68 https://doi.org/10.1101/gad.173435.111
  12. 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
  13. Fischer M, Rikeit P, Knaus P and Coirault C (2016) YAP-Mediated Mechanotransduction in Skeletal Muscle. Front Physiol 7, 41
  14. Dupont S, Morsut L, Aragona M et al (2011) Role of YAP/TAZ in mechanotransduction. Nature 474, 179-183 https://doi.org/10.1038/nature10137
  15. Wrighton KH (2011) Mechanotransduction: YAP and TAZ feel the force. Nat Rev Mol Cell Biol 12, 404
  16. Zhao B, Wei X, Li W et al (2007) Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev 21, 2747-2761 https://doi.org/10.1101/gad.1602907
  17. Kaneko K, Ito M, Naoe Y, Lacy-Hulbert A and Ikeda K (2014) Integrin alphav in the mechanical response of osteoblast lineage cells. Biochem Biophys Res Commun 447, 352-357 https://doi.org/10.1016/j.bbrc.2014.04.006
  18. Wang KC, Yeh YT, Nguyen P et al (2016) Flow-dependent YAP/TAZ activities regulate endothelial phenotypes and atherosclerosis. Proc Natl Acad Sci U S A 113, 11525-11530 https://doi.org/10.1073/pnas.1613121113
  19. Clark K, Langeslag M, Figdor CG and van Leeuwen FN (2007) Myosin II and mechanotransduction: a balancing act. Trends Cell Biol 17, 178-186 https://doi.org/10.1016/j.tcb.2007.02.002
  20. Sansores-Garcia L, Bossuyt W, Wada K et al (2011) Modulating F-actin organization induces organ growth by affecting the Hippo pathway. EMBO J 30, 2325-2335 https://doi.org/10.1038/emboj.2011.157
  21. Elosegui-Artola A, Oria R, Chen Y et al (2016) Mechanical regulation of a molecular clutch defines force transmission and transduction in response to matrix rigidity. Nat Cell Biol 18, 540-548 https://doi.org/10.1038/ncb3336
  22. Kuroda M, Wada H, Kimura Y, Ueda K and Kioka N (2017) Vinculin promotes nuclear localization of TAZ to inhibit ECM stiffness-dependent differentiation into adipocytes. J Cell Sci 130, 989-1002 https://doi.org/10.1242/jcs.194779
  23. Engler AJ, Sen S, Sweeney HL and Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126, 677-689 https://doi.org/10.1016/j.cell.2006.06.044
  24. Levental KR, Yu H, Kass L et al (2009) Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139, 891-906 https://doi.org/10.1016/j.cell.2009.10.027
  25. Butcher DT, Alliston T and Weaver VM (2009) A tense situation: forcing tumour progression. Nat Rev Cancer 9, 108-122 https://doi.org/10.1038/nrc2544
  26. Harvey KF, Zhang X and Thomas DM (2013) The Hippo pathway and human cancer. Nat Rev Cancer 13, 246-257 https://doi.org/10.1038/nrc3458
  27. Schroeder MC and Halder G (2012) Regulation of the Hippo pathway by cell architecture and mechanical signals. Semin Cell Dev Biol 23, 803-811 https://doi.org/10.1016/j.semcdb.2012.06.001
  28. Benham-Pyle BW, Pruitt BL and Nelson WJ (2015) Cell adhesion. Mechanical strain induces E-cadherin-dependent Yap1 and beta-catenin activation to drive cell cycle entry. Science 348, 1024-1027 https://doi.org/10.1126/science.aaa4559
  29. Furukawa KT, Yamashita K, Sakurai N and Ohno S (2017) The Epithelial Circumferential Actin Belt Regulates YAP/TAZ through Nucleocytoplasmic Shuttling of Merlin. Cell Rep 20, 1435-1447 https://doi.org/10.1016/j.celrep.2017.07.032
  30. Driscoll TP, Cosgrove BD, Heo SJ, Shurden ZE and Mauck RL (2015) Cytoskeletal to Nuclear Strain Transfer Regulates YAP Signaling in Mesenchymal Stem Cells. Biophys J 108, 2783-2793 https://doi.org/10.1016/j.bpj.2015.05.010
  31. Aureille J, Belaadi N and Guilluy C (2017) Mechanotransduction via the nuclear envelope: a distant reflection of the cell surface. Curr Opin Cell Biol 44, 59-67 https://doi.org/10.1016/j.ceb.2016.10.003
  32. Strambio-De-Castillia C, Niepel M and Rout MP (2010) The nuclear pore complex: bridging nuclear transport and gene regulation. Nat Rev Mol Cell Biol 11, 490-501
  33. Elosegui-Artola A, Andreu I, Beedle AEM et al (2017) Force Triggers YAP Nuclear Entry by Regulating Transport across Nuclear Pores. Cell 171, 1397-1410 e14 https://doi.org/10.1016/j.cell.2017.10.008
  34. Sit ST and Manser E (2011) Rho GTPases and their role in organizing the actin cytoskeleton. J Cell Sci 124, 679-683 https://doi.org/10.1242/jcs.064964
  35. Amano M, Nakayama M and Kaibuchi K (2010) Rho-kinase/ROCK: A key regulator of the cytoskeleton and cell polarity. Cytoskeleton (Hoboken) 67, 545-554 https://doi.org/10.1002/cm.20472
  36. Steinestel K, Wardelmann E, Hartmann W and Grunewald I (2015) Regulators of Actin Dynamics in Gastrointestinal Tract Tumors. Gastroenterol Res Pract 2015, 930157
  37. Fernandez BG, Gaspar P, Bras-Pereira C, Jezowska B, Rebelo S R and Janody F (2011) Actin-Capping Protein and the Hippo pathway regulate F-actin and tissue growth in Drosophila. Development 138, 2337-2346 https://doi.org/10.1242/dev.063545
  38. Lappano R and Maggiolini M (2011) G protein-coupled receptors: novel targets for drug discovery in cancer. Nat Rev Drug Discov 10, 47-60 https://doi.org/10.1038/nrd3320
  39. Miller E, Yang J, DeRan M et al (2012) Identification of serum-derived sphingosine-1-phosphate as a small molecule regulator of YAP. Chem Biol 19, 955-962 https://doi.org/10.1016/j.chembiol.2012.07.005
  40. Yu FX, Zhang Y, Park HW et al (2013) Protein kinase A activates the Hippo pathway to modulate cell proliferation and differentiation. Genes Dev 27, 1223-1232 https://doi.org/10.1101/gad.219402.113
  41. Feng X, Degese MS, Iglesias-Bartolome R et al (2014) Hippo-independent activation of YAP by the GNAQ uveal melanoma oncogene through a trio-regulated rho GTPase signaling circuitry. Cancer cell 25, 831-845 https://doi.org/10.1016/j.ccr.2014.04.016
  42. Trofatter JA, MacCollin MM, Rutter JL et al (1993) A novel moesin-, ezrin-, radixin-like gene is a candidate for the neurofibromatosis 2 tumor suppressor. Cell 75, 826 https://doi.org/10.1016/0092-8674(93)90501-G
  43. McClatchey AI and Giovannini M (2005) Membrane organization and tumorigenesis--the NF2 tumor suppressor, Merlin. Genes Dev 19, 2265-2277 https://doi.org/10.1101/gad.1335605
  44. Yin F, Yu J, Zheng Y, Chen Q, Zhang N and Pan D (2013) Spatial organization of Hippo signaling at the plasma membrane mediated by the tumor suppressor Merlin/NF2. Cell 154, 1342-1355 https://doi.org/10.1016/j.cell.2013.08.025
  45. Zhao B, Li L, Lu Q et al (2011) Angiomotin is a novel Hippo pathway component that inhibits YAP oncoprotein. Genes Dev 25, 51-63 https://doi.org/10.1101/gad.2000111
  46. Chan SW, Lim CJ, Chong YF, Pobbati AV, Huang C and Hong W (2011) Hippo pathway-independent restriction of TAZ and YAP by angiomotin. J Biol Chem 286, 7018-7026 https://doi.org/10.1074/jbc.C110.212621
  47. Wang W, Huang J and Chen J (2011) Angiomotin-like proteins associate with and negatively regulate YAP1. J Biol Chem 286, 4364-4370 https://doi.org/10.1074/jbc.C110.205401
  48. 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
  49. Lucas EP, Khanal I, Gaspar P et al (2013) The Hippo pathway polarizes the actin cytoskeleton during collective migration of Drosophila border cells. J Cell Biol 201, 875-885 https://doi.org/10.1083/jcb.201210073
  50. Nardone G, Oliver-De La Cruz J et al (2017) YAP regulates cell mechanics by controlling focal adhesion assembly. Nat Commun 8, 15321 https://doi.org/10.1038/ncomms15321

Cited by

  1. RHOA activity in expanding blastocysts is essential to regulate HIPPO-YAP signaling and to maintain the trophectoderm-specific gene expression program in a ROCK/actin filament-independent manner vol.25, pp.2, 2019, https://doi.org/10.1093/molehr/gay048