Hippo signaling pathway and organ size control

Fly

Volumn 3, Issue 1, 2009, Pages 68-73

  Zhang, Lei ^a   Yue, Tao ^b   Jiang, Jin ^b  

^a INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^b UNIVERSITY OF TEXAS AT DALLAS   (United States)

Author keywords

Fat; Hippo; Lats; Merlin; MST; NF2; TEAD; Wts; Yap; Yki

Indexed keywords

EID: 69249117040     PISSN: 19336934     EISSN: 19336942     Source Type: Journal    
DOI: 10.4161/fly.3.1.7788     Document Type: Review

References (85)

1. Conlon I, Raff M. Size control in animal development. Cell 1999; 96: 235-44.
2. Hariharan IK, Bilder D. Regulation of imaginal disc growth by tumor-suppressor genes in Drosophila. Ann Rev Gen 2006; 40: 335-61.
3. Bryant PJ, Simpson P. Intrinsic and extrinsic control of growth in developing organs. Q Rev Biol 1984; 59: 387-415.
4. Bryant PJ, Levinson P. Intrinsic growth control in the imaginal primordia of Drosophila, and the autonomous action of a lethal mutation causing overgrowth. Dev Biol 1985; 107: 355-63.
5. Bryant PJ, Huettner B, Held LJ, Ryerse J, Szidonya J. Mutations at the fat locus interfere with cell proliferation control and epithelial morphogenesis in Drosophila. Dev Biol 1988; 129: 541-54.
6. Watson KL, Justice RW, Bryant PJ. Drosophila in cancer research: the first fifty tumor suppressor genes. J Cell Sci 1994; 18: 19-33.
7. Justice RW, Zilian O, Woods DF, Noll M, Bryant PJ. 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: 534-46.
8. Xu T, Wang W, Zhang S, Stewart RA, Yu W. Identifying tumor suppressors in genetic mosaics: the Drosophila lats gene encodes a putative protein kinase. Development 1995; 121: 1053-63.
9. Tapon N, Harvey KF, Bell DW, Wahrer DCR, Schiripo TA, Haber DA, Hariharan IK. salvador promotes both cell cycle exit and apoptosis in Drosophila and is mutated in human cancer cell lines. Cell 2002; 110: 467-78
10. Jia J, Zhang W, Wang B, Trinko R, Jiang J. The Drosophila Ste20 family kinase dMST functions as a tumor suppressor by restricting cell proliferation and promoting apoptosis. Genes Dev 2003; 17: 2514-9.
11. Wu S, Huang J, Dong J, Pan D. hippo Encodes a Ste-20 family protein kinase that restricts cell proliferation and promotes spoptosis in vonjunction with salvador and warts. Cell 2003; 114: 445-56.
12. Harvey KF, Pfleger CM, Hariharan IK. The Drosophila Mst ortholog, hippo, restricts growth and cell proliferation and promotes apoptosis. Cell 2003; 114: 457-67.
13. Pantalacci S, Tapon N, Leopold P. The Salvador partner Hippo promotes apoptosis and cell cycle exit in Drosophila. Nat Cell Biol 2003; 5: 921.
14. Udan RS, Kango-Singh M, Nolo R, Chunyao T, Halder G. Hippo promotes proliferation arrest and apoptosis in the Salvador/Warts pathway. Nat Cell Biol 2003; 5: 914.
15. 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: 675-85.
16. Wei X, Shimizu T, Lai ZC. Mob as tumor suppressor is activated by Hippo kinase for growth inhibition in Drosophila. Embo J 2007; 26: 1772-81.
17. Praskova M, Xia F, Avruch J. MOBKL1A/MOBKL1B phosphorylation by MST1 and MST2 inhibits cell proliferation. Curr Biol 2008; 18: 311-21.
18. Harvey K, Tapon N. The Salvador-Warts-Hippo pathway-an emerging tumour-suppressor network. Nat Rev Cancer 2007; 7: 182-91.
19. Thompson BJ, Cohen SM. The Hippo pathway regulates the bantam microRNA to control cell proliferation and apoptosis in Drosophila. Cell 2006; 126: 767-74.
20. Wu X, Yamada-Mabuchi M, Morris EJ, Tanwar PS, Dobens L, Gluderer S, Khan S, Cao J, Stocker H, Hafen E, Dyson NJ, Raftery LA. The Drosophila homolog of human tumor suppressor TSC-22 promotes cellular growth, proliferation and survival. Proc Natl Acad Sci 2008; 105: 5414-9. (Pubitemid 351753877)
21. Huang J, Wu S, Barrera J, Matthews K, Pan D. The Hippo signaling pathway coordinately regulates cell proliferation and apoptosis by inactivating Yorkie, the Drosophila homolog of YAP. Cell 2005; 122: 421-34.
22. Wu S, Liu Y, Zheng Y, Dong J, Pan D. The TEAD/TEF family protein scalloped mediates transcriptional output of the Hippo growth-regulatory pathway. Dev Cell 2008; 14: 388-98.
23. Zhang L, Ren F, Zhang Q, Chen Y, Wang B, Jiang J. The TEAD/TEF family of transcription factor scalloped mediates Hippo signaling in organ size control. Dev Cell 2008; 14: 377-87.
24. Goulev Y, Fauny JD, Gonzalez-Marti B, Flagiello D, Silber J, Zider A. SCALLOPED interacts with YORKIE, the nuclear effector of the Hippo tumor-suppressor pathway in Drosophila. Curr Biol 2008; 18: 435-41.
25. Dong J, Feldmann G, Huang J, Wu S, Zhang N, Comerford SA, Gayyed MF, Anders RA, Maitra A, Pan D. Elucidation of a universal size-control mechanism in Drosophila and mammals. Cell 2007; 130: 1120-33.
26. Oh H, Irvine KD. In vivo regulation of Yorkie phosphorylation and localization. Development 2008; 135: 1081-8.
27. Barolo S, Posakony JW. Three habits of highly effective signaling pathways: principles of transcriptional control by developmental cell signaling. Genes Dev 2002; 16: 1167-81.
28. Bennett FC, Harvey KF. Fat cadherin modulates organ size in Drosophila via the Salvador/Warts/Hippo signaling pathway. Curr Biol 2006; 16: 2101-10.
29. Cho E, Feng Y, Rauskolb C, Maitra S, Fehon R, Irvine KD. Delineation of a Fat tumor suppressor pathway. Nat Genet 2006; 38: 1142-50.
30. Silva E, Tsatskis Y, Gardano L, Tapon N, McNeill H. The tumor-suppressor gene fat controls tissue growth upstream of expanded in the hippo signaling pathway. Curr Biol 2006; 16: 2081-9.
31. Willecke M, Hamaratoglu F, Kango-Singh M, Udan R, Chen CL, Tao C, Zhang X, Halder G. The fat cadherin acts through the hippo tumor-suppressor pathway to regulate tissue size. Curr Biol 2006; 16: 2090-100.
32. Mahoney PA, Weber U, Onofrechuk P, Biessmann H, Bryant PJ, Goodman CS. The fat tumor suppressor gene in Drosophila encodes a novel member of the cadherin gene superfamily. Cell 1991; 67: 853-68.
33. Matakatsu H, Blair SS. Separating the adhesive and signaling functions of the Fat and Dachsous protocadherins. Development 2006; 133: 2315-24.
34. Feng Y, Irvine KD. Fat and expanded act in parallel to regulate growth through warts. Proc Natl Acad Sci USA 2007; 104: 20362-7.
35. Hamaratoglu F, Willecke M, Kango-Singh M, Nolo R, Hyun E, Tao C, Jafar-Nejad H, Halder G. The tumour-suppressor genes NF2/Merlin and Expanded act through Hippo signalling to regulate cell proliferation and apoptosis. Nat Cell Biol 2006; 8: 27-36.
36. McClatchey AI, Giovannini M. Membrane organization and tumorigenesis-the NF2 tumor suppressor, Merlin. Genes Dev 2005; 19: 2265-77.
37. Mao Y, Rauskolb C, Cho E, Hu WL, Hayter H, Minihan G, Katz FN, Irvine KD. Dachs: an unconventional myosin that functions downstream of Fat to regulate growth, affinity and gene expression in Drosophila. Development 2006; 133: 2539-51.
38. Matakatsu H, Blair SS. The DHHC palmitoyltransferase approximated regulates Fat signaling and Dachs localization and activity. Curr Biol 2008; 18: 1390-5.
39. Zilian O, Frei E, Burke R, Brentrup D, Gutjahr T, Bryant PJ, Noll M. double-time is identical to discs overgrown, which is required for cell survival, proliferation and growth arrest in Drosophila imaginal discs. Development (UK) 1999; 126: 5409-20.
40. Lawrence PA, Struhl G, Casal J. Planar cell polarity: one or two pathways? Nat Rev Genet 2007; 8: 555-63.
41. Clark HF, Brentrup D, Schneitz K, Bieber A, Goodman C, Noll M. Dachsous encodes a member of the cadherin superfamily that controls imaginal disc morphogenesis in Drosophila. Genes Dev 1995; 9: 1530-42.
42. Matakatsu H, Blair SS. Interactions between Fat and Dachsous and the regulation of planar cell polarity in the Drosophila wing. Development 2004; 131: 3785-94.
43. Cho E, Irvine KD. Action of fat, four-jointed, dachsous and dachs in distal-to-proximal wing signaling. Development 2004; 131: 4489-500.
44. Ishikawa HO, Takeuchi H, Haltiwanger RS, Irvine KD. Four-jointed is a Golgi kinase that phosphorylates a subset of cadherin domains. Science 2008; 321: 401-4.
45. Villano JL, Katz FN. four-jointed is required for intermediate growth in the proximal-distal axis in Drosophila. Development 1995; 121: 2767-77.
46. Rogulja D, Rauskolb C, Irvine KD. Morphogen control of wing growth through the Fat signaling pathway. Dev Cell 2008; 15: 309-21.
47. Willecke M, Hamaratoglu F, Sansores-Garcia L, Tao C, Halder G. Boundaries of Dachsous cadherin activity modulate the Hippo signaling pathway to induce cell proliferation. Proc Natl Acad Sci USA 2008; 105: 14897-902.
48. Rogulja D, Irvine KD. Regulation of cell proliferation by a morphogen gradient. Cell 2005; 123: 449-61.
49. Schwank G, Restrepo S, Basler K. Growth regulation by Dpp: an essential role for Brinker and a non-essential role for graded signaling levels. Development 2008; 135: 4003-13.
50. Hufnagel L, Teleman AA, Rouault H, Cohen SM, Shraiman BI. On the mechanism of wing size determination in fly development. Proc Natl Acad Sci USA 2007; 104: 3835-40.
51. Pan D. Hippo signaling in organ size control. Genes Dev 2007; 21: 886-97.
52. Zeng Q, Hong W. The emerging role of the Hippo pathway in cell contact inhibition, organ size control and cancer development in mammals. Cancer Cell 2008; 13: 188-92.
53. Reddy BV, Irvine KD. The Fat and Warts signaling pathways: new insights into their regulation, mechanism and conservation. Development 2008; 135: 2827-38.
54. Tao W, Zhang S, Turenchalk GS, Stewart RA, St. John MA, Chen W, Xu T. Human homologue of the Drosophila melanogaster lats tumour suppressor modulates CDC2 activity. Nat Genet 1999; 21: 177-81.
55. Dong J, Feldmann G, Huang J, Wu S, Zhang N, Comerford SA, Gayyed MF, Anders RA, Maitra A, Pan D. Elucidation of a universal size-control mechanism in Drosophila and mammals. Cell 2007; 130: 1120-33.
56. Baker NE, Li W. Cell competition and its possible relation to cancer. Cancer Res 2008; 68: 5505-7.
57. Zender L, Spector MS, Xue W, Flemming P, Cordon-Cardo C, Silke J, Fan S-T, Luk JM, Wigler M, Hannon GJ. Identification and validation of oncogenes in liver cancer using an integrative oncogenomic approach. Cell 2006; 125: 1253-67.
58. Zhao B, Wei X, Li W, Udan RS, Yang Q, Kim J, Xie J, Ikenoue T, Yu J, Li L, Zheng P, Ye K, Chinnaiyan A, Halder G, Lai Z-C, Guan K-L. Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev 2007; 21: 2747-61.
59. Camargo FD, Gokhale S, Johnnidis JB, Fu D, Bell GW, Jaenisch R, Brummelkamp TR. YAP1 increases organ size and expands undifferentiated progenitor cells. Curr Biol 2007; 17: 2054-60.
60. Steinhardt AA, Gayyed MF, Klein AP, Dong J, Maitra A, Pan D, Montgomery EA, Anders RA. Expression of Yes-associated protein in common solid tumors. Hum Pathol 2008.
61. St. John MA, Tao W, Fei X, Fukumoto R, Carcangiu ML, Brownstein DG, Parlow AF, McGrath J, Xu T. Mice deficient of Lats1 develop soft-tissue sarcomas, ovarian tumours and pituitary dysfunction. Nat Genet 1999; 21: 182-6.
62. McPherson JP, Tamblyn L, Elia A, Migon E, Shehabeldin A, Matysiak-Zablocki E, Lemmers B, Salmena L, Hakem A, Fish J, Kassam F, Squire J, Bruneau BG, Hande MP, Hakem R. Lats2/Kpm is required for embryonic development, proliferation control and genomic integrity. Embo J 2004; 23: 3677-88.
63. Yabuta N, Okada N, Ito A, Hosomi T, Nishihara S, Sasayama Y, Fujimori A, Okuzaki D, Zhao H, Ikawa M, Okabe M, Nojima H. Lats2 is an essential mitotic regulator required for the coordination of cell division. J Biol Chem 2007; 282: 19259-71.
64. 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: 2076-86.
65. Lee JH, Kim TS, Yang TH, Koo BK, Oh SP, Lee KP, Oh HJ, Lee SH, Kong YY, Kim JM, Lim DS. A crucial role of WW45 in developing epithelial tissues in the mouse. Embo J 2008; 27: 1231-42.
66. Overholtzer M, Zhang J, Smolen GA, Muir B, Li W, Sgroi DC, Deng C-X, Brugge JS, Haber DA. Transforming properties of YAP, a candidate oncogene on the chromosome 11q22 amplicon. Proc Natl Acad Sci 2006; 0605579103.
67. 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: 5496-509.
68. Zhao B, Ye X, Yu J, Li L, Li W, Li S, Yu J, Lin JD, Wang CY, Chinnaiyan AM, Lai ZC, Guan KL. TEAD mediates YAP-dependent gene induction and growth control. Genes Dev 2008; 22: 1962-71.
69. Cao X, Pfaff SL, Gage FH. YAP regulates neural progenitor cell number via the TEA domain transcription factor. Genes Dev 2008.
70. Ota M, Sasaki H. Mammalian Tead proteins regulate cell proliferation and contact inhibition as transcriptional mediators of Hippo signaling. Development 2008; 135: 4059-69.
71. McClatchey AI. Neurofibromatosis. Annu Rev Pathol 2007; 2: 191-216.
72. Girard N. Imaging features of neurofibromatosis type 2. J Neuroradiol 2005; 32: 198-203.
73. Goutagny S, Bouccara D, Bozorg-Grayeli A, Sterkers O, Kalamarides M. Neurofibromatosis type 2. Rev Neurol 2007; 163: 765-77.
74. Striedinger K, VandenBerg SR, Baia GS, McDermott MW, Gutmann DH, Lal A. The neurofibromatosis 2 tumor suppressor gene product, merlin, regulates human meningioma cell growth by signaling through YAP. Neoplasia 2008; 10: 1204-12.
75. Saburi S, Hester I, Fischer E, Pontoglio M, Eremina V, Gessler M, Quaggin SE, Harrison R, Mount R, McNeill H. Loss of Fat4 disrupts PCP signaling and oriented cell division and leads to cystic kidney disease. Nat Genet 2008; 40: 1010-5.
76. Qi C, Zhu YT, Hu L, Zhu YJ. Identification of Fat4 as a candidate tumor suppressor gene in breast cancers. Intl J Cancer 2009; 124: 793-8.
77. Kawahara M, Hori T, Chonabayashi K, Oka T, Sudol M, Uchiyama T. Kpm/Lats2 is linked to chemo-sensitivity of leukemic cells through the stabilization of p73. Blood 2008; blood-2007-09-111773.
78. Strano S, Monti O, Pediconi N, Baccarini A, Fontemaggi G, Lapi E, Mantovani F, Damalas A, Citro G, Sacchi A, Del Sal G, Levrero M, Blandino G. The transcriptional coactivator Yes-associated protein drives p73 gene-target specificity in response to DNA damage. Mol Cell 2005; 18: 447-59.
79. Mikeladze-Dvali T, Wernet MF, Pistillo D, Mazzoni EO, Teleman AA, Chen Y-W, Cohen S, Desplan C. The growth regulators warts/lats and melted interact in a bistable loop to specify opposite fates in Drosophila R8 photoreceptors. Cell 2005; 122: 775-87.
80. Emoto K, Parrish JZ, Jan LY, Jan YN. The tumour suppressor Hippo acts with the NDR kinases in dendritic tiling and maintenance. Nature 2006; 443: 210-3.
81. Parrish JZ, Emoto K, Jan LY, Jan YN. Polycomb genes interact with the tumor suppressor genes hippo and warts in the maintenance of Drosophila sensory neuron dendrites. Genes Dev 2007; 21: 956-72.
82. Polesello C, Tapon N. Salvador-warts-hippo signaling promotes Drosophila posterior follicle cell maturation downstream of notch. Curr Biol 2007; 17: 1864-70.
83. Meignin C, Alvarez-Garcia I, Davis I, Palacios IM. The salvador-warts-hippo pathway is required for epithelial proliferation and axis specification in Drosophila. Curr Biol 2007; 17: 1871-8.
84. Yu J, Poulton J, Huang YC, Deng WM. The hippo pathway promotes Notch signaling in regulation of cell differentiation, proliferation and oocyte polarity. PLoS ONE 2008; 3: 1761.
85. Dutta S, Baehrecke EH. Warts is required for PI3K-regulated growth arrest, Autophagy and autophagic cell death in Drosophila. Curr Biol 2008; 18: 1466-75.