A miR-130a-YAP positive feedback loop promotes organ size and tumorigenesis

Cell Research

Volumn 25, Issue 9, 2015, Pages 997-1012

  Shen, Shuying ^a,b   Guo, Xiaocan ^a   Yan, Huan ^a   Lu, Yi ^d   Ji, Xinyan ^a   Li, Li ^e   Liang, Tingbo ^c   Zhou, Dawang ^f   Feng, Xin Hua ^a   Zhao, Jonathan C ^g   Yu, Jindan ^g   Gong, Xing Guo ^b   Zhang, Lei ^d   Zhao, Bin ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b ZHEJIANG UNIVERSITY   (China)

^c ZHEJIANG UNIVERSITY   (China)

^d INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^e HANGZHOU NORMAL UNIVERSITY   (China)

^f XIAMEN UNIVERSITY   (China)

^g NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Hippo; microRNA; organ size; tumorigenesis; YAP

Indexed keywords

CYR61 PROTEIN, HUMAN; CYSTEINE RICH PROTEIN 61; DROSOPHILA PROTEIN; MICRORNA; MIRN130 MICRORNA, HUMAN; PHOSPHOPROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TAZ PROTEIN, HUMAN; TRANSCRIPTION FACTOR; VGLL4 PROTEIN, HUMAN; YAP1 (YES-ASSOCIATED) PROTEIN, HUMAN;

ANIMAL; ANTAGONISTS AND INHIBITORS; CARCINOGENESIS; CELL PROLIFERATION; DROSOPHILA; GENETICS; HEP-G2 CELL LINE; HUMAN; INSTITUTE FOR CANCER RESEARCH MOUSE; MALE; METABOLISM; MOUSE; NUCLEOTIDE SEQUENCE; NUDE MOUSE; ORGAN SIZE; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; TUMOR CELL LINE; XENOGRAFT;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BASE SEQUENCE; CARCINOGENESIS; CELL LINE, TUMOR; CELL PROLIFERATION; CYSTEINE-RICH PROTEIN 61; DROSOPHILA; DROSOPHILA PROTEINS; HEP G2 CELLS; HUMANS; MALE; MICE; MICE, INBRED ICR; MICE, NUDE; MICRORNAS; ORGAN SIZE; PHOSPHOPROTEINS; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSPLANTATION, HETEROLOGOUS;

EID: 84940898894     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2015.98     Document Type: Article

References (58)

1. Pan D. The hippo signaling pathway in development and cancer. Dev Cell 2010; 19:491-505.
2. Yu FX, Guan KL. The Hippo pathway: regulators and regulations. Genes Dev 2013; 27:355-371.
3. Dong J, Feldmann G, Huang J, et al. Elucidation of a universal size-control mechanism in Drosophila and mammals. Cell 2007; 130:1120-1133.
4. Xin M, Kim Y, Sutherland LB, et al. Hippo pathway effector Yap promotes cardiac regeneration. Proc Natl Acad Sci USA 2013; 110:13839-13844.
5. Cai J, Zhang N, Zheng Y, de Wilde RF, Maitra A, Pan D. The Hippo signaling pathway restricts the oncogenic potential of an intestinal regeneration program. Genes Dev 2010; 24:2383-2388.
6. Heallen T, Morikawa Y, Leach J, et al. Hippo signaling impedes adult heart regeneration. Development 2013; 140:4683-4690.
7. Chan EH, Nousiainen M, Chalamalasetty RB, Schafer A, Nigg EA, Sillje HH. The Ste20-like kinase Mst2 activates the human large tumor suppressor kinase Lats1. Oncogene 2005; 24:2076-2086.
8. Callus BA, Verhagen AM, Vaux DL. 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.
9. Hergovich A, Schmitz D, Hemmings BA. The human tumour suppressor LATS1 is activated by human MOB1 at the membrane. Biochem Biophys Res Commun 2006; 345:50-58.
10. Zhao B, Wei X, Li W, et al. Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev 2007; 21:2747-2761.
11. Zhao B, Li L, Tumaneng K, Wang CY, Guan KL. A coordinated phosphorylation by Lats and CK1 regulates YAP stability through SCF(beta-TRCP). Genes Dev 2010; 24:72-85.
12. 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.
13. Lei QY, Zhang H, Zhao B, Zha ZY, Bai F, Pei XH, et al. TAZ promotes cell proliferation and epithelial-mesenchymal transition and is inhibited by the hippo pathway. Mol Cell Biol 2008; 28:2426-2436.
14. β-TrCP E3 ligase. J Biol Chem 2010; 285:37159-37169.
15. Zhao B, Ye X, Yu J, et al. TEAD mediates YAP-dependent gene induction and growth control. Genes Dev 2008; 22:1962-1971.
16. Zhang H, Liu CY, Zha ZY, et al. TEAD transcription factors mediate the function of TAZ in cell growth and epitheli-al-mesenchymal transition. J Biol Chem 2009; 284:13355-13362.
17. Schlegelmilch K, Mohseni M, Kirak O, et al. Yap1 acts downstream of alpha-catenin to control epidermal proliferation. Cell 2011; 144:782-795.
18. Yu FX, Zhao B, Panupinthu N, et al. Regulation of the Hippo-YAP pathway by G-protein-coupled receptor signaling. Cell 2012; 150:780-791.
19. Miller E, Yang J, DeRan M, et al. Identifcation of serum-derived sphingosine-1-phosphate as a small molecule regulator of YAP. Chem Biol 2012; 19:955-962.
20. Zhao B, Li L, Wang L, Wang CY, Yu J, Guan KL. Cell detachment activates the Hippo pathway via cytoskeleton reorganization to induce anoikis. Genes Dev 2012; 26:54-68.
21. Dupont S, Morsut L, Aragona M, et al. Role of YAP/TAZ in mechanotransduction. Nature 2011; 474:179-183.
22. Wada K, Itoga K, Okano T, Yonemura S, Sasaki H. Hippo pathway regulation by cell morphology and stress fbers. Development 2011; 138:3907-3914.
23. Sansores-Garcia L, Bossuyt W, Wada K, et al. Modulating F-actin organization induces organ growth by affecting the Hippo pathway. EMBO J 2011; 30:2325-2335.
24. Leevers SJ, McNeill H. Controlling the size of organs and organisms. Curr Opin Cell Biol 2005; 17:604-609.
25. Overholtzer M, Zhang J, Smolen GA, et al. Transforming properties of YAP, a candidate oncogene on the chromosome 11q22 amplicon. Proc Natl Acad Sci USA 2006; 103:12405-12410.
26. Zhou D, Conrad C, Xia F, et al. Mst1 and Mst2 maintain he-patocyte quiescence and suppress hepatocellular carcinoma development through inactivation of the Yap1 oncogene. Cancer Cell 2009; 16:425-438.
27. Zhou D, Zhang Y, Wu H, et al. Mst1 and Mst2 protein kinases restrain intestinal stem cell proliferation and colonic tumor-igenesis by inhibition of Yes-associated protein (Yap) overabundance. Proc Natl Acad Sci USA 2011; 108:E1312-1320.
28. Zender L, Spector MS, Xue W, et al. Identifcation and validation of oncogenes in liver cancer using an integrative on-cogenomic approach. Cell 2006; 125:1253-1267.
29. Song Y, Li L, Ou Y, et al. Identifcation of genomic alterations in oesophageal squamous cell cancer. Nature 2014; 509:91-95.
30. Feng X, Degese MS, Iglesias-Bartolome R, et al. Hippo-independent activation of YAP by the GNAQ uveal melanoma oncogene through a trio-regulated rho GTPase signaling circuitry. Cancer Cell 2014; 25:831-845.
31. Yu FX, Luo J, Mo JS, et al. Mutant Gq/11 promote uveal melanoma tumorigenesis by activating YAP. Cancer Cell 2014; 25:822-830.
32. Zhang N, Bai H, David KK, et al. The Merlin/NF2 tumor suppressor functions through the YAP oncoprotein to regulate tissue homeostasis in mammals. Dev Cell 2010; 19:27-38.
33. Jiao S, Wang H, Shi Z, et al. A peptide mimicking VGLL4 function acts as a YAP antagonist therapy against gastric cancer. Cancer Cell 2014; 25:166-180.
34. Koontz LM, Liu-Chittenden Y, Yin F, et al. The hippo effector yorkie controls normal tissue growth by antagonizing scal-loped-mediated default repression. Dev Cell 2013; 25:388-401.
35. Zhang W, Gao Y, Li P, et al. VGLL4 functions as a new tumor suppressor in lung cancer by negatively regulating the YAP-TEAD transcriptional complex. Cell Res 2014; 24:331-343.
36. Thompson BJ, Cohen SM. The Hippo pathway regulates the bantam microRNA to control cell proliferation and apoptosis in Drosophila. Cell 2006; 126:767-774.
37. Nolo R, Morrison CM, Tao C, Zhang X, Halder G. The bantam microRNA is a target of the hippo tumor-suppressor pathway. Curr Biol 2006; 16:1895-1904.
38. Huang H, Li J, Hu L, et al. Bantam is essential for Drosophila intestinal stem cell proliferation in response to Hippo signaling. Dev Biol 2014; 385:211-219.
39. Song H, Mak KK, Topol L, et al. Mammalian Mst1 and Mst2 kinases play essential roles in organ size control and tumor suppression. Proc Natl Acad Sci USA 2010; 107:1431-1436.
40. Lu L, Li Y, Kim SM, et al. Hippo signaling is a potent in vivo growth and tumor suppressor pathway in the mammalian liver. Proc Natl Acad Sci USA 2010; 107:1437-1442.
41. McClatchey AI, Saotome I, Mercer K, et al. Mice heterozygous for a mutation at the Nf2 tumor suppressor locus develop a range of highly metastatic tumors. Genes Dev 1998; 12:1121-1133.
42. Lee KP, Lee JH, Kim TS, et al. The Hippo-Salvador pathway restrains hepatic oval cell proliferation, liver size, and liver tumorigenesis. Proc Natl Acad Sci USA 2010; 107:8248-8253.
43. Tao J, Calvisi DF, Ranganathan S, et al. Activation of be-ta-catenin and Yap1 in human hepatoblastoma and induction of hepatocarcinogenesis in mice. Gastroenterology 2014; 147:690-701.
44. Guo T, Lu Y, Li P, et al. A novel partner of Scalloped regulates Hippo signaling via antagonizing Scalloped-Yorkie activity. Cell Res 2013; 23:1201-1214.
45. Brennecke J, Hipfner DR, Stark A, Russell RB, Cohen SM. Bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila. Cell 2003; 113:25-36.
46. Zhao B, Li L, Lei Q, Guan KL. The Hippo-YAP pathway in organ size control and tumorigenesis: an updated version. Genes Dev 2010; 24:862-874.
47. Liu-Chittenden Y, Huang B, Shim JS, et al. Genetic and pharmacological disruption of the TEAD-YAP complex suppresses the oncogenic activity of YAP. Genes Dev 2012; 26:1300-1305.
48. Tumaneng K, Schlegelmilch K, Russell RC, et al. YAP mediates crosstalk between the Hippo and PI(3)K-TOR pathways by suppressing PTEN via miR-29. Nat Cell Biol 2012; 14:1322-1329.
49. Ebert MS, Sharp PA. Roles for microRNAs in conferring robustness to biological processes. Cell 2012; 149:515-524.
50. Vidigal JA, Ventura A. The biological functions of miRNAs: lessons from in vivo studies. Trends Cell Biol 2015; 25:137-147.
51. Moroishi T, Hansen CG, Guan KL. The emerging roles of YAP and TAZ in cancer. Nat Rev Cancer 2015; 15:73-79.
52. Kapoor A, Yao W, Ying H, et al. Yap1 activation enables bypass of oncogenic Kras addiction in pancreatic cancer. Cell 2014; 158:185-197.
53. Shao DD, Xue W, Krall EB, et al. KRAS and YAP1 converge to regulate EMT and tumor survival. Cell 2014; 158:171-184.
54. Rosenbluh J, Nijhawan D, Cox AG, et al. β-Catenin-driven cancers require a YAP1 transcriptional complex for survival and tumorigenesis. Cell 2012; 151:1457-1473.
55. Chan SW, Lim CJ, Guo K, et al. A role for TAZ in migration, invasion, and tumorigenesis of breast cancer cells. Cancer Res 2008; 68:2592-2598.
56. Cordenonsi M, Zanconato F, Azzolin L, et al. The Hippo transducer TAZ confers cancer stem cell-related traits on breast cancer cells. Cell 2011; 147:759-772.
57. Chen Y, Gao DY, Huang L. In vivo delivery of miRNAs for cancer therapy: challenges and strategies. Adv Drug Deliv Rev 2015; 81:128-141.
58. Cheng CJ, Bahal R, Babar IA, et al. MicroRNA silencing for cancer therapy targeted to the tumour microenvironment. Nature 2015; 518:107-110.