DOI QR코드

DOI QR Code

The role of extracellular biophysical cues in modulating the Hippo-YAP pathway

  • Mo, Jung-Soon (Genomic Instability Research Center (GIRC), Ajou University School of Medicine)
  • 투고 : 2016.11.23
  • 발행 : 2017.02.28

초록

The Hippo signaling pathway plays an essential role in adult-tissue homeostasis and organ-size control. In Drosophila and vertebrates, it consists of a highly conserved kinase cascade, which involves MST and Lats that negatively regulate the activity of the downstream transcription coactivators, YAP and TAZ. By interacting with TEADs and other transcription factors, they mediate both proliferative and antiapoptotic gene expression and thus regulate tissue repair and regeneration. Dysregulation or mutation of the Hippo pathway is linked to tumorigenesis and cancer development. Recent studies have uncovered multiple upstream inputs, including cell density, mechanical stress, G-protein-coupled receptor (GPCR) signaling, and nutrients, that modulate Hippo pathway activity. This review focuses on the role of the Hippo pathway as effector of these biophysical cues and its potential implications in tissue homeostasis and cancer.

키워드

참고문헌

  1. 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
  2. Harvey KF, Pfleger CM and Hariharan IK (2003) The Drosophila Mst ortholog, hippo, restricts growth and cell proliferation and promotes apoptosis. Cell 114, 457-467 https://doi.org/10.1016/S0092-8674(03)00557-9
  3. Jia J, Zhang W, Wang B, Trinko R and Jiang J (2003) The Drosophila Ste20 family kinase dMST functions as a tumor suppressor by restricting cell proliferation and promoting apoptosis. Genes Dev 17, 2514-2519 https://doi.org/10.1101/gad.1134003
  4. Justice RW, Zilian O, Woods DF, Noll M and Bryant PJ (1995) 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 9, 534-546 https://doi.org/10.1101/gad.9.5.534
  5. Pantalacci S, Tapon N and Leopold P (2003) The Salvador partner Hippo promotes apoptosis and cell-cycle exit in Drosophila. Nat Cell Biol 5, 921-927 https://doi.org/10.1038/ncb1051
  6. Xu T, Wang W, Zhang S, Stewart RA and Yu W (1995) Identifying tumor suppressors in genetic mosaics: the Drosophila lats gene encodes a putative protein kinase. Development 121, 1053-1063
  7. Udan RS, Kango-Singh M, Nolo R, Tao C and Halder G (2003) Hippo promotes proliferation arrest and apoptosis in the Salvador/Warts pathway. Nat Cell Biol 5, 914-920 https://doi.org/10.1038/ncb1050
  8. Wu S, Huang J, Dong J and Pan D (2003) Hippo encodes a Ste-20 family protein kinase that restricts cell proliferation and promotes apoptosis in conjunction with salvador and warts. Cell 114, 445-456 https://doi.org/10.1016/S0092-8674(03)00549-X
  9. Kango-Singh M, Nolo R, Tao C et al (2002) Shar-pei mediates cell proliferation arrest during imaginal disc growth in Drosophila. Development 129, 5719-5730 https://doi.org/10.1242/dev.00168
  10. Tapon N, Harvey KF, Bell DW et al (2002) Salvador promotes both cell cycle exit and apoptosis in Drosophila and is mutated in human cancer cell lines. Cell 110, 467-478 https://doi.org/10.1016/S0092-8674(02)00824-3
  11. Lai ZC, Wei X, Shimizu T et al (2005) Control of cell proliferation and apoptosis by mob as tumor suppressor, mats. Cell 120, 675-685 https://doi.org/10.1016/j.cell.2004.12.036
  12. Huang J, Wu S, Barrera J, Matthews K and Pan D (2005) The Hippo signaling pathway coordinately regulates cell proliferation and apoptosis by inactivating Yorkie, the Drosophila homolog of YAP. Cell 122, 421-434 https://doi.org/10.1016/j.cell.2005.06.007
  13. Dong J, Feldmann G, Huang J et al (2007) Elucidation of a universal size-control mechanism in Drosophila and mammals. Cell 130, 1120-1133 https://doi.org/10.1016/j.cell.2007.07.019
  14. Staley BK and Irvine KD (2012) Hippo signaling in Drosophila: recent advances and insights. Dev Dyn 241, 3-15 https://doi.org/10.1002/dvdy.22723
  15. Oh H and Irvine KD (2008) In vivo regulation of Yorkie phosphorylation and localization. Development 135, 1081-1088 https://doi.org/10.1242/dev.015255
  16. Ren F, Zhang L and Jiang J (2010) Hippo signaling regulates Yorkie nuclear localization and activity through 14-3-3 dependent and independent mechanisms. Dev Biol 337, 303-312 https://doi.org/10.1016/j.ydbio.2009.10.046
  17. Mahoney WM Jr, Hong JH, Yaffe MB and Farrance IK (2005) The transcriptional co-activator TAZ interacts differentially with transcriptional enhancer factor-1 (TEF-1) family members. Biochem J 388, 217-225 https://doi.org/10.1042/BJ20041434
  18. Vassilev A, Kaneko KJ, Shu H, Zhao Y and DePamphilis ML (2001) TEAD/TEF transcription factors utilize the activation domain of YAP65, a Src/Yes-associated protein localized in the cytoplasm. Genes Dev 15, 1229-1241 https://doi.org/10.1101/gad.888601
  19. 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
  20. Sudol M (1994) Yes-associated protein (YAP65) is a proline-rich phosphoprotein that binds to the SH3 domain of the Yes proto-oncogene product. Oncogene 9, 2145-2152
  21. Hao Y, Chun A, Cheung K, Rashidi B and Yang X (2008) Tumor suppressor LATS1 is a negative regulator of oncogene YAP. J Biol Chem 283, 5496-5509 https://doi.org/10.1074/jbc.M709037200
  22. Oka T, Mazack V and Sudol M (2008) Mst2 and Lats kinases regulate apoptotic function of Yes kinaseassociated protein (YAP). J Biol Chem 283, 27534-27546 https://doi.org/10.1074/jbc.M804380200
  23. Lei QY, Zhang H, Zhao B et al (2008) TAZ promotes cell proliferation and epithelial-mesenchymal transition and is inhibited by the Hippo pathway. Mol Cell Biol 28, 2426-2436 https://doi.org/10.1128/MCB.01874-07
  24. Kanai F, Marignani PA, Sarbassova D et al (2000) TAZ: a novel transcriptional co-activator regulated by interactions with 14-3-3 and PDZ domain proteins. EMBO J 19, 6778-6791 https://doi.org/10.1093/emboj/19.24.6778
  25. Liu CY, Zha ZY, Zhou X et al (2010) The Hippo tumor pathway promotes TAZ degradation by phosphorylating a phosphodegron and recruiting the SCF{beta}-TrCP E3 ligase. J Biol Chem 285, 37159-37169 https://doi.org/10.1074/jbc.M110.152942
  26. Zhao B, Ye X, Yu J et al (2008) TEAD mediates YAPdependent gene induction and growth control. Genes Dev 22, 1962-1971 https://doi.org/10.1101/gad.1664408
  27. Zhang H, Liu CY, Zha ZY et al (2009) TEAD transcription factors mediate the function of TAZ in cell growth and epithelial-mesenchymal transition. J Biol Chem 284, 13355-13362 https://doi.org/10.1074/jbc.M900843200
  28. Zhu C, Li L and Zhao B (2015) The regulation and function of YAP transcription co-activator. Acta Biochim Biophys Sin (Shanghai) 47, 16-28 https://doi.org/10.1093/abbs/gmu110
  29. Zanconato F, Cordenonsi M and Piccolo S (2016) YAP/TAZ at the roots of cancer. Cancer Cell 29, 783-803 https://doi.org/10.1016/j.ccell.2016.05.005
  30. Ota M and Sasaki H (2008) Mammalian Tead proteins regulate cell proliferation and contact inhibition as transcriptional mediators of Hippo signaling. Development 135, 4059-4069 https://doi.org/10.1242/dev.027151
  31. Nishioka N, Inoue K, Adachi K et al (2009) The Hippo signaling pathway components Lats and Yap pattern Tead4 activity to distinguish mouse trophectoderm from inner cell mass. Dev Cell 16, 398-410 https://doi.org/10.1016/j.devcel.2009.02.003
  32. Gumbiner BM and Kim NG (2014) The Hippo-YAP signaling pathway and contact inhibition of growth. J Cell Sci 127, 709-717 https://doi.org/10.1242/jcs.140103
  33. Yang CC, Graves HK, Moya IM et al (2015) Differential regulation of the Hippo pathway by adherens junctions and apical-basal cell polarity modules. Proc Natl Acad Sci U S A 112, 1785-1790 https://doi.org/10.1073/pnas.1420850112
  34. 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
  35. 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
  36. 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
  37. Sun Y, Yong KM, Villa-Diaz LG et al (2014) Hippo/YAPmediated rigidity-dependent motor neuron differentiation of human pluripotent stem cells. Nat Mater 13, 599-604 https://doi.org/10.1038/nmat3945
  38. 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
  39. 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
  40. Fernandez BG, Gaspar P, Bras-Pereira C, Jezowska B, Rebelo SR 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
  41. Ikeda S, Cunningham LA, Boggess D et al (2003) Aberrant actin cytoskeleton leads to accelerated proliferation of corneal epithelial cells in mice deficient for destrin (actin depolymerizing factor). Hum Mol Genet 12, 1029-1037 https://doi.org/10.1093/hmg/ddg112
  42. 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
  43. Codelia VA, Sun G and Irvine KD (2014) Regulation of YAP by mechanical strain through Jnk and Hippo signaling. Curr Biol 24, 2012-2017 https://doi.org/10.1016/j.cub.2014.07.034
  44. Calvo F, Ege N, Grande-Garcia A et al (2013) Mechanotransduction and YAP-dependent matrix remodelling is required for the generation and maintenance of cancerassociated fibroblasts. Nat Cell Biol 15, 637-646 https://doi.org/10.1038/ncb2756
  45. Chan SW, Lim CJ, Guo K et al (2008) A role for TAZ in migration, invasion, and tumorigenesis of breast cancer cells. Cancer Res 68, 2592-2598 https://doi.org/10.1158/0008-5472.CAN-07-2696
  46. Cordenonsi M, Zanconato F, Azzolin L et al (2011) The Hippo transducer TAZ confers cancer stem cell-related traits on breast cancer cells. Cell 147, 759-772 https://doi.org/10.1016/j.cell.2011.09.048
  47. Kim KM, Choi YJ, Hwang JH et al (2014) Shear stress induced by an interstitial level of slow flow increases the osteogenic differentiation of mesenchymal stem cells through TAZ activation. PLoS One 9, e92427 https://doi.org/10.1371/journal.pone.0092427
  48. 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
  49. Sabine A, Bovay E, Demir CS et al (2015) FOXC2 and fluid shear stress stabilize postnatal lymphatic vasculature. J Clin Invest 125, 3861-3877 https://doi.org/10.1172/JCI80454
  50. 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
  51. 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
  52. Cai H and Xu Y (2013) The role of LPA and YAP signaling in long-term migration of human ovarian cancer cells. Cell Commun Signal 11, 31 https://doi.org/10.1186/1478-811X-11-31
  53. Mo JS, Yu FX, Gong R, Brown JH and Guan KL (2012) Regulation of the Hippo-YAP pathway by proteaseactivated receptors (PARs). Genes Dev 26, 2138-2143 https://doi.org/10.1101/gad.197582.112
  54. 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
  55. 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
  56. Zhu H, Cheng X, Niu X et al (2015) Proton-sensing GPCR-YAP Signalling Promotes Cell Proliferation and Survival. Int J Biol Sci 11, 1181-1189 https://doi.org/10.7150/ijbs.12500
  57. Zhu H, Guo S, Zhang Y et al (2016) Proton-sensing GPCR-YAP Signalling Promotes Cancer-associated Fibroblast Activation of Mesenchymal Stem Cells. Int J Biol Sci 12, 389-396 https://doi.org/10.7150/ijbs.13688
  58. Zhou X, Wang S, Wang Z et al (2015) Estrogen regulates Hippo signaling via GPER in breast cancer. J Clin Invest 125, 2123-2135 https://doi.org/10.1172/JCI79573
  59. Feng X, Liu P, Zhou X et al (2016) Thromboxane A2 Activates YAP/TAZ Protein to Induce Vascular Smooth Muscle Cell Proliferation and Migration. J Biol Chem 291, 18947-18958 https://doi.org/10.1074/jbc.M116.739722
  60. Wennmann DO, Vollenbroker B, Eckart AK et al (2014) The Hippo pathway is controlled by Angiotensin II signaling and its reactivation induces apoptosis in podocytes. Cell Death Dis 5, e1519 https://doi.org/10.1038/cddis.2014.476
  61. Chen D, Sun Y, Wei Y et al (2012) LIFR is a breast cancer metastasis suppressor upstream of the Hippo-YAP pathway and a prognostic marker. Nat Med 18, 1511-1517 https://doi.org/10.1038/nm.2940
  62. Fan R, Kim NG and Gumbiner BM (2013) Regulation of Hippo pathway by mitogenic growth factors via phosphoinositide 3-kinase and phosphoinositide-dependent kinase-1. Proc Natl Acad Sci U S A 110, 2569-2574 https://doi.org/10.1073/pnas.1216462110
  63. Azzolin L, Panciera T, Soligo S et al (2014) YAP/TAZ incorporation in the beta-catenin destruction complex orchestrates the Wnt response. Cell 158, 157-170 https://doi.org/10.1016/j.cell.2014.06.013
  64. Barry ER, Morikawa T, Butler BL et al (2013) Restriction of intestinal stem cell expansion and the regenerative response by YAP. Nature 493, 106-110
  65. Heallen T, Zhang M, Wang J et al (2011) Hippo pathway inhibits Wnt signaling to restrain cardiomyocyte proliferation and heart size. Science 332, 458-461 https://doi.org/10.1126/science.1199010
  66. Rosenbluh J, Nijhawan D, Cox AG et al (2012) beta-Catenin-driven cancers require a YAP1 transcriptional complex for survival and tumorigenesis. Cell 151, 1457-1473 https://doi.org/10.1016/j.cell.2012.11.026
  67. Varelas X, Miller BW, Sopko R et al (2010) The Hippo pathway regulates Wnt/beta-catenin signaling. Dev Cell 18, 579-591 https://doi.org/10.1016/j.devcel.2010.03.007
  68. 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
  69. Azzolin L, Zanconato F, Bresolin S et al (2012) Role of TAZ as mediator of Wnt signaling. Cell 151, 1443-1456 https://doi.org/10.1016/j.cell.2012.11.027
  70. Alarcon C, Zaromytidou AI, Xi Q et al (2009) Nuclear CDKs drive Smad transcriptional activation and turnover in BMP and TGF-beta pathways. Cell 139, 757-769 https://doi.org/10.1016/j.cell.2009.09.035
  71. Fujii M, Toyoda T, Nakanishi H et al (2012) TGF-beta synergizes with defects in the Hippo pathway to stimulate human malignant mesothelioma growth. J Exp Med 209, 479-494 https://doi.org/10.1084/jem.20111653
  72. Varelas X, Sakuma R, Samavarchi-Tehrani P et al (2008) TAZ controls Smad nucleocytoplasmic shuttling and regulates human embryonic stem-cell self-renewal. Nat Cell Biol 10, 837-848 https://doi.org/10.1038/ncb1748
  73. 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
  74. Liu G, Yu FX, Kim YC et al (2015) Kaposi sarcomaassociated herpesvirus promotes tumorigenesis by modulating the Hippo pathway. Oncogene 34, 3536-3546 https://doi.org/10.1038/onc.2014.281
  75. Yu FX, Luo J, Mo JS et al (2014) Mutant Gq/11 promote uveal melanoma tumorigenesis by activating YAP. Cancer Cell 25, 822-830 https://doi.org/10.1016/j.ccr.2014.04.017
  76. DeRan M, Yang J, Shen CH et al (2014) Energy stress regulates hippo-YAP signaling involving AMPK-mediated regulation of angiomotin-like 1 protein. Cell Rep 9, 495-503 https://doi.org/10.1016/j.celrep.2014.09.036
  77. Mo JS, Meng Z, Kim YC et al (2015) Cellular energy stress induces AMPK-mediated regulation of YAP and the Hippo pathway. Nat Cell Biol 17, 500-510 https://doi.org/10.1038/ncb3111
  78. Wang W, Xiao ZD, Li X et al (2015) AMPK modulates Hippo pathway activity to regulate energy homeostasis. Nat Cell Biol 17, 490-499 https://doi.org/10.1038/ncb3113
  79. Mohseni M, Sun J, Lau A et al (2014) A genetic screen identifies an LKB1-MARK signalling axis controlling the Hippo-YAP pathway. Nat Cell Biol 16, 108-117 https://doi.org/10.1038/ncb2884
  80. Nguyen HB, Babcock JT, Wells CD and Quilliam LA (2013) LKB1 tumor suppressor regulates AMP kinase/mTORindependent cell growth and proliferation via the phosphorylation of Yap. Oncogene 32, 4100-4109 https://doi.org/10.1038/onc.2012.431
  81. Gailite I, Aerne BL and Tapon N (2015) Differential control of Yorkie activity by LKB1/AMPK and the Hippo/Warts cascade in the central nervous system. Proc Natl Acad Sci U S A 112, E5169-5178 https://doi.org/10.1073/pnas.1505512112
  82. Park YY, Sohn BH, Johnson RL et al (2016) Yes-associated protein 1 and transcriptional coactivator with PDZbinding motif activate the mammalian target of rapamycin complex 1 pathway by regulating amino acid transporters in hepatocellular carcinoma. Hepatology 63, 159-172 https://doi.org/10.1002/hep.28223
  83. Hansen CG, Ng YL, Lam WL, Plouffe SW and Guan KL (2015) The Hippo pathway effectors YAP and TAZ promote cell growth by modulating amino acid signaling to mTORC1. Cell Res 25, 1299-1313 https://doi.org/10.1038/cr.2015.140
  84. Artinian N, Cloninger C, Holmes B, Benavides-Serrato A, Bashir T and Gera J (2015) Phosphorylation of the Hippo Pathway Component AMOTL2 by the mTORC2 Kinase Promotes YAP Signaling, Resulting in Enhanced Glioblastoma Growth and Invasiveness. J Biol Chem 290, 19387-19401 https://doi.org/10.1074/jbc.M115.656587
  85. Sciarretta S, Zhai P, Maejima Y et al (2015) mTORC2 regulates cardiac response to stress by inhibiting MST1. Cell Rep 11, 125-136 https://doi.org/10.1016/j.celrep.2015.03.010
  86. Liang N, Zhang C, Dill P et al (2014) Regulation of YAP by mTOR and autophagy reveals a therapeutic target of tuberous sclerosis complex. J Exp Med 211, 2249-2263 https://doi.org/10.1084/jem.20140341
  87. Parker J and Struhl G (2015) Scaling the Drosophila Wing: TOR-Dependent Target Gene Access by the Hippo Pathway Transducer Yorkie. PLoS Biol 13, e1002274 https://doi.org/10.1371/journal.pbio.1002274
  88. Tumaneng K, Schlegelmilch K, Russell RC et al (2012) YAP mediates crosstalk between the Hippo and PI(3)KTOR pathways by suppressing PTEN via miR-29. Nat Cell Biol 14, 1322-1329 https://doi.org/10.1038/ncb2615
  89. Cinar B, Collak FK, Lopez D et al (2011) MST1 is a multifunctional caspase-independent inhibitor of androgenic signaling. Cancer Res 71, 4303-4313 https://doi.org/10.1158/0008-5472.CAN-10-4532
  90. Collak FK, Yagiz K, Luthringer DJ, Erkaya B and Cinar B (2012) Threonine-120 phosphorylation regulated by phosphoinositide-3-kinase/Akt and mammalian target of rapamycin pathway signaling limits the antitumor activity of mammalian sterile 20-like kinase 1. J Biol Chem 287, 23698-23709 https://doi.org/10.1074/jbc.M112.358713
  91. Garcia-Martinez JM and Alessi DR (2008) mTOR complex 2 (mTORC2) controls hydrophobic motif phosphorylation and activation of serum- and glucocorticoid-induced protein kinase 1 (SGK1). Biochem J 416, 375-385 https://doi.org/10.1042/BJ20081668
  92. Ikenoue T, Inoki K, Yang Q, Zhou X and Guan KL (2008) Essential function of TORC2 in PKC and Akt turn motif phosphorylation, maturation and signalling. EMBO J 27, 1919-1931 https://doi.org/10.1038/emboj.2008.119
  93. Facchinetti V, Ouyang W, Wei H et al (2008) The mammalian target of rapamycin complex 2 controls folding and stability of Akt and protein kinase C. EMBO J 27, 1932-1943 https://doi.org/10.1038/emboj.2008.120
  94. Sorrentino G, Ruggeri N, Specchia V et al (2014) Metabolic control of YAP and TAZ by the mevalonate pathway. Nat Cell Biol 16, 357-366 https://doi.org/10.1038/ncb2936
  95. Wehr MC, Holder MV, Gailite I et al (2013) Salt-inducible kinases regulate growth through the Hippo signalling pathway in Drosophila. Nat Cell Biol 15, 61-71 https://doi.org/10.1038/ncb2658

피인용 문헌

  1. AMOT130 linking F-actin to YAP is involved in intervertebral disc degeneration pp.09607722, 2018, https://doi.org/10.1111/cpr.12492
  2. The history and regulatory mechanism of the Hippo pathway vol.51, pp.3, 2018, https://doi.org/10.5483/BMBRep.2018.51.3.022