Table of Contents
Molecular Biology International
Volume 2012, Article ID 307628, 12 pages
http://dx.doi.org/10.1155/2012/307628
Review Article

Hippo and rassf1a Pathways: A Growing Affair

1Molecular Chemoprevention Group, Molecular Medicine Area, Regina Elena Cancer Institute, Via Elio Chianesi 53, 00143 Rome, Italy
2Translational Oncogenomic Unit, Molecular Medicine Area, Regina Elena Cancer Institute, Via Elio Chianesi 53, 00143 Rome, Italy

Received 25 March 2012; Accepted 18 May 2012

Academic Editor: Shairaz Baksh

Copyright © 2012 Francesca Fausti et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. D. Pan, “The hippo signaling pathway in development and cancer,” Developmental Cell, vol. 19, no. 4, pp. 491–505, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. B. Zhao, K. Tumaneng, and K. L. Guan, “The hippo pathway in organ size control, tissue regeneration and stem cell self-renewal,” Nature Cell Biology, vol. 13, no. 8, pp. 877–883, 2011. View at Publisher · View at Google Scholar · View at Scopus
  3. R. W. Justice, O. Zilian, D. F. Woods, M. Noll, and P. J. Bryant, “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 and Development, vol. 9, no. 5, pp. 534–546, 1995. View at Google Scholar · View at Scopus
  4. N. Tapon, K. F. Harvey, D. W. Bell et al., “salvador promotes both cell cycle exit and apoptosis in Drosophila and is mutated in human cancer cell lines,” Cell, vol. 110, no. 4, pp. 467–478, 2002. View at Publisher · View at Google Scholar · View at Scopus
  5. S. Wu, J. Huang, J. Dong, and D. Pan, “hippo encodes a Ste-20 family protein kinase that restricts cell proliferation and promotes apoptosis in conjunction with salvador and warts,” Cell, vol. 114, no. 4, pp. 445–456, 2003. View at Publisher · View at Google Scholar · View at Scopus
  6. Z. C. Lai, X. Wei, T. Shimizu et al., “Control of cell proliferation and apoptosis by mob as tumor suppressor, mats,” Cell, vol. 120, no. 5, pp. 675–685, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. M. Boedigheimer, P. Bryant, and A. Laughon, “Expanded, a negative regulator of cell proliferation in Drosophila, shows homology to the NF2 tumor suppressor,” Mechanisms of Development, vol. 44, no. 2-3, pp. 83–84, 1993. View at Google Scholar · View at Scopus
  8. D. R. LaJeunesse, B. M. McCartney, and R. G. Fehon, “Structural analysis of Drosophila Merlin reveals functional domains important for growth control and subcellular localization,” Journal of Cell Biology, vol. 141, no. 7, pp. 1589–1599, 1998. View at Publisher · View at Google Scholar · View at Scopus
  9. F. Hamaratoglu, M. Willecke, M. Kango-Singh et al., “The tumour-suppressor genes NF2/Merlin and expanded act through hippo signalling to regulate cell proliferation and apoptosis,” Nature Cell Biology, vol. 8, no. 1, pp. 27–36, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. S. Maitra, R. M. Kulikauskas, H. Gavilan, and R. G. Fehon, “The tumor suppressors Merlin and expanded function cooperatively to modulate receptor endocytosis and signaling,” Current Biology, vol. 16, no. 7, pp. 702–709, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. P. A. Mahoney, U. Weber, P. Onofrechuk, H. Biessmann, P. J. Bryant, and C. S. Goodman, “The fat tumor suppressor gene in Drosophila encodes a novel member of the cadherin gene superfamily,” Cell, vol. 67, no. 5, pp. 853–868, 1991. View at Google Scholar · View at Scopus
  12. F. C. Bennett and K. F. Harvey, “Fat cadherin modulates organ size in Drosophila via the Salvador/Warts/hippo signaling pathway,” Current Biology, vol. 16, no. 21, pp. 2101–2110, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. E. Silva, Y. Tsatskis, L. Gardano, N. Tapon, and H. McNeill, “The tumor-suppressor gene fat controls tissue growth upstream of expanded in the hippo signaling pathway,” Current Biology, vol. 16, no. 21, pp. 2081–2089, 2006. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Willecke, F. Hamaratoglu, M. Kango-Singh et al., “The fat cadherin acts through the hippo tumor-suppressor pathway to regulate tissue size,” Current Biology, vol. 16, no. 21, pp. 2090–2100, 2006. View at Publisher · View at Google Scholar · View at Scopus
  15. H. Matakatsu and S. S. Blair, “Interactions between Fat and Dachsous and the regulation of planar cell polarity in the Drosophila wing,” Development, vol. 131, no. 15, pp. 3785–3794, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. H. Matakatsu and S. S. Blair, “Separating the adhesive and signaling functions of the Fat and Dachsous protocadherins,” Development, vol. 133, no. 12, pp. 2315–2324, 2006. View at Publisher · View at Google Scholar · View at Scopus
  17. E. Cho, Y. Feng, C. Rauskolb, S. Maitra, R. Fehon, and K. D. Irvine, “Delineation of a Fat tumor suppressor pathway,” Nature Genetics, vol. 38, no. 10, pp. 1142–1150, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. Y. Feng and K. D. Irvine, “Processing and phosphorylation of the Fat receptor,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 29, pp. 11989–11994, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. R. Baumgartner, I. Poernbacher, N. Buser, E. Hafen, and H. Stocker, “The WW domain protein kibra acts upstream of hippo in Drosophila,” Developmental Cell, vol. 18, no. 2, pp. 309–316, 2010. View at Publisher · View at Google Scholar · View at Scopus
  20. A. Genevet, M. C. Wehr, R. Brain, B. J. Thompson, and N. Tapon, “Kibra is a regulator of the Salvador/Warts/hippo signaling network,” Developmental Cell, vol. 18, no. 2, pp. 300–308, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. J. Yu, Y. Zheng, J. Dong, S. Klusza, W. M. Deng, and D. Pan, “Kibra functions as a tumor suppressor protein that regulates hippo signaling in conjunction with Merlin and Expanded,” Developmental Cell, vol. 18, no. 2, pp. 288–299, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. C. L. Chen, K. M. Gajewski, F. Hamaratoglu et al., “The apical-basal cell polarity determinant Crumbs regulates hippo signaling in Drosophila,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 36, pp. 15810–15815, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. C. Ling, Y. Zheng, F. Yin et al., “The apical transmembrane protein Crumbs functions as a tumor suppressor that regulates hippo signaling by binding to expanded,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 23, pp. 10532–10537, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. B. S. Robinson, J. Huang, Y. Hong, and K. H. Moberg, “Crumbs regulates Salvador/Warts/hippo signaling in Drosophila via the FERM-domain protein expanded,” Current Biology, vol. 20, no. 7, pp. 582–590, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. J. Huang, S. Wu, J. Barrera, K. Matthews, and D. Pan, “The hippo signaling pathway coordinately regulates cell proliferation and apoptosis by inactivating Yorkie, the Drosophila homolog of YAP,” Cell, vol. 122, no. 3, pp. 421–434, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. M. Sudol, H. I. Chen, C. Bougeret, A. Einbond, and P. Bork, “Characterization of a novel protein-binding module—the WW domain,” FEBS Letters, vol. 369, no. 1, pp. 67–71, 1995. View at Publisher · View at Google Scholar · View at Scopus
  27. M. Sudol, “Newcomers to the WW domain-mediated network of the hippo tumor suppressor pathway,” Genes and Cancer, vol. 1, no. 11, pp. 1115–1118, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. M. Sudol and K. F. Harvey, “Modularity in the hippo signaling pathway,” Trends in Biochemical Sciences, vol. 35, no. 11, pp. 627–633, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. U. Tepass, C. Theres, and E. Knust, “Crumbs encodes an EGF-like protein expressed on apical membranes of Drosophila epithelial cells and required for organization of epithelia,” Cell, vol. 61, no. 5, pp. 787–799, 1990. View at Publisher · View at Google Scholar · View at Scopus
  30. C. H. Yang, J. D. Axelrod, and M. A. Simon, “Regulation of Frizzled by Fat-like cadherins during planar polarity signaling in the Drosophila compound eye,” Cell, vol. 108, no. 5, pp. 675–688, 2002. View at Publisher · View at Google Scholar · View at Scopus
  31. J. Casal, P. A. Lawrence, and G. Struhl, “Two separate molecular systems, Dachsous/Fat and Starry night/Frizzled, act independently to confer planar star polarity,” Development, vol. 133, no. 22, pp. 4561–4572, 2006. View at Publisher · View at Google Scholar · View at Scopus
  32. Y. Feng and K. D. Irvine, “Fat and expanded act in parallel to regulate growth through Warts,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 51, pp. 20362–20367, 2007. View at Publisher · View at Google Scholar · View at Scopus
  33. C. Polesello and N. Tapon, “Salvador-Warts-hippo signaling promotes Drosophila posterior follicle cell maturation downstream of notch,” Current Biology, vol. 17, no. 21, pp. 1864–1870, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. B. V. V. G. Reddy, C. Rauskolb, and K. D. Irvine, “Influence of Fat-hippo and Notch signaling on the proliferation and differentiation of Drosophila optic neuroepithelia,” Development, vol. 137, no. 14, pp. 2397–2408, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. D. Rogulja, C. Rauskolb, and K. D. Irvine, “Morphogen control of wing growth through the Fat signaling pathway,” Developmental Cell, vol. 15, no. 2, pp. 309–321, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. M. Willecke, F. Hamaratoglu, L. Sansores-Garcia, C. Tao, and G. Halder, “Boundaries of Dachsous Cadherin activity modulate the hippo signaling pathway to induce cell proliferation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 39, pp. 14897–14902, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. H. O. Ishikawa, H. Takeuchi, R. S. Haltiwanger, and K. D. Irvine, “Four-jointed is a Golgi kinase that phosphorylates a subset of cadherin domains,” Science, vol. 321, no. 5887, pp. 401–404, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. H. Matakatsu and S. S. Blair, “The DHHC palmitoyltransferase approximated regulates Fat signaling and Dachs localization and activity,” Current Biology, vol. 18, no. 18, pp. 1390–1395, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. C. Rauskolb, G. Pan, B. V. V. G. Reddy, H. Oh, and K. D. Irvine, “Zyxin links fat signaling to the hippo pathway,” PLoS Biology, vol. 9, no. 6, Article ID e1000624, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. K. Harvey and N. Tapon, “The Salvador-Warts-hippo pathway—an emerging tumour-suppressor network,” Nature Reviews Cancer, vol. 7, no. 3, pp. 182–191, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. C. Polesello, S. Huelsmann, N. Brown, and N. Tapon, “The Drosophilarassf homolog antagonizes the hippo pathway,” Current Biology, vol. 16, no. 24, pp. 2459–2465, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. P. S. Ribeiro, F. Josué, A. Wepf et al., “Combined functional genomic and proteomic approaches identify a PP2A complex as a negative regulator of hippo signaling,” Molecular Cell, vol. 39, no. 4, pp. 521–534, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. N. A. Grzeschik, L. M. Parsons, M. L. Allott, K. F. Harvey, and H. E. Richardson, “Lgl, aPKC, and Crumbs regulate the Salvador/Warts/hippo pathway through two distinct mechanisms,” Current Biology, vol. 20, no. 7, pp. 573–581, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. S. Dong, S. Kang, T. L. Gu et al., “14-3-3 Integrates prosurvival signals mediated by the AKT and MAPK pathways in ZNF198-FGFR1-transformed hematopoietic cells,” Blood, vol. 110, no. 1, pp. 360–369, 2007. View at Publisher · View at Google Scholar · View at Scopus
  45. H. Oh and K. D. Irvine, “In vivo regulation of Yorkie phosphorylation and localization,” Development, vol. 135, no. 6, pp. 1081–1088, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. M. Praskova, F. Xia, and J. Avruch, “MOBKL1A/MOBKL1B Phosphorylation by MST1 and MST2 Inhibits Cell Proliferation,” Current Biology, vol. 18, no. 5, pp. 311–321, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. B. Zhao, X. Wei, W. Li et al., “Inactivation of YAP oncoprotein by the hippo pathway is involved in cell contact inhibition and tissue growth control,” Genes and Development, vol. 21, no. 21, pp. 2747–2761, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. C. Badouel, L. Gardano, N. Amin et al., “The FERM-domain protein Expanded regulates hippo pathway activity via direct interactions with the transcriptional activator Yorkie,” Developmental Cell, vol. 16, no. 3, pp. 411–420, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. H. Oh, B. V. V. G. Reddy, and K. D. Irvine, “Phosphorylation-independent repression of Yorkie in Fat-hippo signaling,” Developmental Biology, vol. 335, no. 1, pp. 188–197, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. S. Wu, Y. Liu, Y. Zheng, J. Dong, and D. Pan, “The TEAD/TEF family protein Scalloped mediates transcriptional output of the hippo growth-regulatory pathway,” Developmental cell, vol. 14, no. 3, pp. 388–398, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. L. Zhang, F. Ren, Q. Zhang, Y. Chen, B. Wang, and J. Jiang, “The TEAD/TEF family of transcription factor Scalloped mediates hippo signaling in organ size control,” Developmental cell, vol. 14, no. 3, pp. 377–387, 2008. View at Publisher · View at Google Scholar · View at Scopus
  52. H. W. Peng, M. Slattery, and R. S. Mann, “Transcription factor choice in the hippo signaling pathway: homothorax and yorkie regulation of the microRNA bantam in the progenitor domain of the Drosophila eye imaginal disc,” Genes and Development, vol. 23, no. 19, pp. 2307–2319, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. Y. Goulev, J. D. Fauny, B. Gonzalez-Marti, D. Flagiello, J. Silber, and A. Zider, “SCALLOPED interacts with YORKIE, the nuclear effector of the hippo tumor-suppressor pathway in Drosophila,” Current Biology, vol. 18, no. 6, pp. 435–441, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. R. M. Neto-Silva, S. de Beco, and L. A. Johnston, “Evidence for a growth-stabilizing regulatory feedback mechanism between Myc and Yorkie, the Drosophila homolog of Yap,” Developmental Cell, vol. 19, no. 4, pp. 507–520, 2010. View at Publisher · View at Google Scholar · View at Scopus
  55. M. Ziosi, L. A. Baena-López, D. Grifoni et al., “dMyc functions downstream of yorkie to promote the supercompetitive behavior of hippo pathway mutant cells,” PLoS Genetics, vol. 6, no. 9, Article ID e1001140, 2010. View at Publisher · View at Google Scholar · View at Scopus
  56. C. Alarcón, A. I. Zaromytidou, Q. Xi et al., “Nuclear CDKs drive smad transcriptional activation and turnover in BMP and TGF-β pathways,” Cell, vol. 139, no. 4, pp. 757–769, 2009. View at Publisher · View at Google Scholar · View at Scopus
  57. A. Genevet, C. Polesello, K. Blight et al., “The hippo pathway regulates apical-domain size independently of its growth-control function,” Journal of Cell Science, vol. 122, pp. 2360–2370, 2009. View at Publisher · View at Google Scholar · View at Scopus
  58. A. Hergovich and B. A. Hemmings, “Mammalian NDR/LATS protein kinases in hippo tumor suppressor signaling,” BioFactors, vol. 35, no. 4, pp. 338–345, 2009. View at Publisher · View at Google Scholar · View at Scopus
  59. M. Radu and J. Chernoff, “The DeMSTification of mammalian Ste20 kinases,” Current Biology, vol. 19, no. 10, pp. R421–R425, 2009. View at Publisher · View at Google Scholar · View at Scopus
  60. Q. Y. Lei, H. Zhang, B. Zhao et al., “TAZ promotes cell proliferation and epithelial-mesenchymal transition and is inhibited by the hippo pathway,” Molecular and Cellular Biology, vol. 28, no. 7, pp. 2426–2436, 2008. View at Publisher · View at Google Scholar · View at Scopus
  61. F. D. Camargo, S. Gokhale, J. B. Johnnidis et al., “YAP1 Increases Organ Size and Expands Undifferentiated Progenitor Cells,” Current Biology, vol. 17, no. 23, pp. 2054–2060, 2007. View at Publisher · View at Google Scholar · View at Scopus
  62. J. Dong, G. Feldmann, J. Huang et al., “Elucidation of a Universal Size-Control Mechanism in Drosophila and Mammals,” Cell, vol. 130, no. 6, pp. 1120–1133, 2007. View at Publisher · View at Google Scholar · View at Scopus
  63. D. Zhou, C. Conrad, F. Xia et al., “Mst1 and Mst2 Maintain Hepatocyte Quiescence andSuppress Hepatocellular Carcinoma Development through Inactivation of the Yap1 Oncogene,” Cancer Cell, vol. 16, no. 5, pp. 425–438, 2009. View at Publisher · View at Google Scholar · View at Scopus
  64. K. P. Lee, J. H. Lee, T. S. Kim et al., “The hippo-Salvador pathway restrains hepatic oval cell proliferation, liver size, and liver tumorigenesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 18, pp. 8248–8253, 2010. View at Publisher · View at Google Scholar · View at Scopus
  65. L. Lu, Y. Li, S. M. Kim et al., “hippo signaling is a potent in vivo growth and tumor suppressor pathway in the mammalian liver,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 4, pp. 1437–1442, 2010. View at Publisher · View at Google Scholar · View at Scopus
  66. H. Song, K. K. Mak, L. Topol et al., “Mammalian Mst1 and Mst2 kinases play essential roles in organ size control and tumor suppression,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 4, pp. 1431–1436, 2010. View at Publisher · View at Google Scholar · View at Scopus
  67. M. Sudol, P. Bork, A. Einbond et al., “Characterization of the mammalian YAP (Yes-associated protein) gene and its role in defining a novel protein module, the WW domain,” Journal of Biological Chemistry, vol. 270, no. 24, pp. 14733–14741, 1995. View at Publisher · View at Google Scholar · View at Scopus
  68. E. Bertini, T. Oka, M. Sudol, S. Strano, and G. Blandino, “At the crossroad between transformation and tumor suppression,” Cell Cycle, vol. 8, no. 1, pp. 49–57, 2009. View at Google Scholar · View at Scopus
  69. A. Sawada, H. Kiyonari, K. Ukita, N. Nishioka, Y. Imuta, and H. Sasaki, “Redundant roles of Tead1 and Tead2 in notochord development and the regulation of cell proliferation and survival,” Molecular and Cellular Biology, vol. 28, no. 10, pp. 3177–3189, 2008. View at Publisher · View at Google Scholar · View at Scopus
  70. M. Ota and H. Sasaki, “Mammalian Tead proteins regulate cell proliferation and contact inhibition as transcriptional mediators of hippo signaling,” Development, vol. 135, no. 24, pp. 4059–4069, 2008. View at Publisher · View at Google Scholar · View at Scopus
  71. B. Zhao, X. Ye, J. Yu et al., “TEAD mediates YAP-dependent gene induction and growth control,” Genes and Development, vol. 22, no. 14, pp. 1962–1971, 2008. View at Publisher · View at Google Scholar · View at Scopus
  72. S. W. Chan, C. J. Lim, L. S. Loo, Y. F. Chong, C. Huang, and W. Hong, “TEADs mediate nuclear retention of TAZ to promote oncogenic transformation,” Journal of Biological Chemistry, vol. 284, no. 21, pp. 14347–14358, 2009. View at Publisher · View at Google Scholar · View at Scopus
  73. S. Dupont, L. Morsut, M. Aragona et al., “Role of YAP/TAZ in mechanotransduction,” Nature, vol. 474, no. 7350, pp. 179–183, 2011. View at Publisher · View at Google Scholar · View at Scopus
  74. M. Sudol and T. Hunter, “New wrinkles for an old domain,” Cell, vol. 103, no. 7, pp. 1001–1004, 2000. View at Publisher · View at Google Scholar · View at Scopus
  75. S. Strano, E. Munarriz, M. Rossi et al., “Physical Interaction with Yes-associated Protein Enhances p73 Transcriptional Activity,” Journal of Biological Chemistry, vol. 276, no. 18, pp. 15164–15173, 2001. View at Publisher · View at Google Scholar · View at Scopus
  76. S. Strano, O. Monti, N. Pediconi et al., “The transcriptional coactivator yes-associated protein drives p73 gene-target specificity in response to DNA damage,” Molecular Cell, vol. 18, no. 4, pp. 447–459, 2005. View at Publisher · View at Google Scholar · View at Scopus
  77. D. Matallanas, D. Romano, K. Yee et al., “rassf1a Elicits Apoptosis through an MST2 Pathway Directing Proapoptotic Transcription by the p73 Tumor Suppressor Protein,” Molecular Cell, vol. 27, no. 6, pp. 962–975, 2007. View at Publisher · View at Google Scholar · View at Scopus
  78. E. Lapi, S. Di Agostino, S. Donzelli et al., “PML, YAP, and p73 Are Components of a Proapoptotic Autoregulatory Feedback Loop,” Molecular Cell, vol. 32, no. 6, pp. 803–814, 2008. View at Publisher · View at Google Scholar · View at Scopus
  79. M. J. Boedigheimer, K. P. Nguyen, and P. J. Bryant, “expanded functions in the apical cell domain to regulate the growth rate of imaginal discs,” Developmental Genetics, vol. 20, no. 2, pp. 103–110, 1997. View at Google Scholar · View at Scopus
  80. G. A. Rouleau, P. Merel, M. Lutchman et al., “Alteration in a new gene encoding a putative membrane-organizing protein causes neuro-fibromatosis type 2,” Nature, vol. 363, no. 6429, pp. 515–521, 1993. View at Publisher · View at Google Scholar · View at Scopus
  81. Trofatter, “Erratum: A novel moesin-, ezrin-, and radixin-like gene is a candidate for the neurofibromatosis 2 tumor suppressor,” Cell, vol. 75, no. 4, pp. 791–800, 1993. View at Google Scholar · View at Scopus
  82. M. Curto, B. K. Cole, D. Lallemand, C. H. Liu, and A. I. McClatchey, “Contact-dependent inhibition of EGFR signaling by Nf2/Merlin,” Journal of Cell Biology, vol. 177, no. 5, pp. 893–903, 2007. View at Publisher · View at Google Scholar · View at Scopus
  83. N. Zhang, H. Bai, K. K. David et al., “The Merlin/NF2 Tumor Suppressor Functions through the YAP Oncoprotein to Regulate Tissue Homeostasis in Mammals,” Developmental Cell, vol. 19, no. 1, pp. 27–38, 2010. View at Publisher · View at Google Scholar · View at Scopus
  84. S. Benhamouche, M. Curto, I. Saotome et al., “Nf2/Merlin controls progenitor homeostasis and tumorigenesis in the liver,” Genes and Development, vol. 24, no. 16, pp. 1718–1730, 2010. View at Publisher · View at Google Scholar · View at Scopus
  85. Y. Lin, A. Khokhlatchev, D. Figeys, and J. Avruch, “Death-associated protein 4 binds MST1 and augments MST1-induced apoptosis,” Journal of Biological Chemistry, vol. 277, no. 50, pp. 47991–48001, 2002. View at Publisher · View at Google Scholar · View at Scopus
  86. S. Ura, H. Nishina, Y. Gotoh, and T. Katada, “Activation of the c-Jun N-terminal kinase pathway by MST1 is essential and sufficient for the induction of chromatin condensation during apoptosis,” Molecular and Cellular Biology, vol. 27, no. 15, pp. 5514–5522, 2007. View at Publisher · View at Google Scholar · View at Scopus
  87. R. Anand, A. Y. Kim, M. Brent, and R. Marmorstein, “Biochemical analysis of MST1 kinase: Elucidation of a C-terminal regulatory region,” Biochemistry, vol. 47, no. 25, pp. 6719–6726, 2008. View at Publisher · View at Google Scholar · View at Scopus
  88. E. O'Neill, L. Rushworth, M. Baccarini, and W. Kolch, “Role of the kinase MST2 in suppression of apoptosis by the proto-oncogene product Raf-1,” Science, vol. 306, no. 5705, pp. 2267–2270, 2004. View at Publisher · View at Google Scholar · View at Scopus
  89. C. Guo, X. Zhang, and G. P. Pfeifer, “The tumor suppressor rassf1a prevents dephosphorylation of the mammalian STE20-like kinases MST1 and MST2,” Journal of Biological Chemistry, vol. 286, no. 8, pp. 6253–6261, 2011. View at Publisher · View at Google Scholar · View at Scopus
  90. X. Yang, D. M. Li, W. Chen, and T. Xu, “Human homologue of Drosophila lats, LATS1, negatively regulate growth by inducing G2/M arrest or apoptosis,” Oncogene, vol. 20, no. 45, pp. 6516–6523, 2001. View at Publisher · View at Google Scholar · View at Scopus
  91. H. Xia, H. Qi, Y. Li et al., “LATS1 tumor suppressor regulates G2/M transition and apoptosis,” Oncogene, vol. 21, no. 8, pp. 1233–1241, 2002. View at Publisher · View at Google Scholar · View at Scopus
  92. N. Yabuta, N. Okada, A. Ito et al., “LATS2 is an essential mitotic regulator required for the coordination of cell division,” Journal of Biological Chemistry, vol. 282, no. 26, pp. 19259–19271, 2007. View at Publisher · View at Google Scholar · View at Scopus
  93. Y. Li, J. Pei, H. Xia, H. Ke, H. Wang, and W. Tao, “LATS2, a putative tumor suppressor, inhibits G1/S transition,” Oncogene, vol. 22, no. 28, pp. 4398–4405, 2003. View at Publisher · View at Google Scholar · View at Scopus
  94. Y. Aylon, N. Yabuta, H. Besserglick et al., “Silencing of the LATS2 tumor suppressor overrides a p53-dependent oncogenic stress checkpoint and enables mutant H-Ras-driven cell transformation,” Oncogene, vol. 28, no. 50, pp. 4469–4479, 2009. View at Publisher · View at Google Scholar · View at Scopus
  95. M. A. R. St John, W. Tao, X. Fei et al., “Mice deficient of Lats1 develop soft-tissue sarcomas, ovarian tumours and pituitary dysfunction,” Nature Genetics, vol. 21, no. 2, pp. 182–186, 1999. View at Publisher · View at Google Scholar · View at Scopus
  96. Y. Aylon, D. Michael, A. Shmueli, N. Yabuta, H. Nojima, and M. Oren, “A positive feedback loop between the p53 and LATS2 tumor suppressors prevents tetraploidization,” Genes and Development, vol. 20, no. 19, pp. 2687–2700, 2006. View at Publisher · View at Google Scholar · View at Scopus
  97. K. Zhang, E. Rodriguez-Aznar, N. Yabuta et al., “LATS2 kinase potentiates Snail1 activity by promoting nuclear retention upon phosphorylation,” EMBO Journal, vol. 31, no. 1, pp. 29–43, 2012. View at Publisher · View at Google Scholar · View at Scopus
  98. K. Tschöp, A. R. Conery, L. Litovchick et al., “A kinase shRNA screen links LATS2 and the pRB tumor suppressor,” Genes and Development, vol. 25, no. 8, pp. 814–830, 2011. View at Publisher · View at Google Scholar · View at Scopus
  99. T. Hori, A. Takaori-Kondo, Y. Kamikubo, and T. Uchiyama, “Molecular cloning of a novel human protein kinase, kpm, that is homologous to warts/lats, a Drosophila tumor suppressor,” Oncogene, vol. 19, no. 27, pp. 3101–3109, 2000. View at Google Scholar · View at Scopus
  100. L. van der Weyden and D. J. Adams, “The Ras-association domain family (RASSF) members and their role in human tumourigenesis,” Biochimica et Biophysica Acta - Reviews on Cancer, vol. 1776, no. 1, pp. 58–85, 2007. View at Publisher · View at Google Scholar · View at Scopus
  101. M. Gordon and S. Baksh, “rassf1a: Not a prototypical Ras effector,” Small GTPases, vol. 2, no. 3, pp. 148–157, 2011. View at Google Scholar · View at Scopus
  102. S. Baksh, S. Tommasi, S. Fenton et al., “The tumor suppressor rassf1a and MAP-1 link death receptor signaling to bax conformational change and cell death,” Molecular Cell, vol. 18, no. 6, pp. 637–650, 2005. View at Publisher · View at Google Scholar · View at Scopus
  103. R. Dammann, C. Li, J. H. Yoon, P. L. Chin, S. Bates, and G. P. Pfeifer, “Epigenetic inactivation of a RAS association domain family protein from the lung tumour suppressor locus 3p21.3,” Nature Genetics, vol. 25, no. 3, pp. 315–319, 2000. View at Publisher · View at Google Scholar · View at Scopus
  104. D. G. Burbee, E. Forgacs, S. Zöchbauer-Müller et al., “Epigenetic inactivation of rassf1a in lung and breast cancers and malignant phenotype suppression,” Journal of the National Cancer Institute, vol. 93, no. 9, pp. 691–699, 2001. View at Google Scholar · View at Scopus
  105. I. Kuzmin, J. W. Gillespie, A. Protopopov et al., “The rassf1a tumor suppressor gene is inactivated in prostate tumors and suppresses growth of prostate carcinoma cells,” Cancer Research, vol. 62, no. 12, pp. 3498–3502, 2002. View at Google Scholar · View at Scopus
  106. L. Shivakumar, J. Minna, T. Sakamaki, R. Pestell, and M. A. White, “The rassf1a tumor suppressor blocks cell cycle progression and inhibits cyclin D1 accumulation,” Molecular and Cellular Biology, vol. 22, no. 12, pp. 4309–4318, 2002. View at Publisher · View at Google Scholar · View at Scopus
  107. Z. G. Pan, V. I. Kashuba, X. Q. Liu et al., “High frequency somatic mutations in rassf1a in nasopharyngeal carcinoma,” Cancer Biology and Therapy, vol. 4, no. 10, pp. 1116–1122, 2005. View at Google Scholar · View at Scopus
  108. S. Tommasi, R. Dammann, Z. Zhang et al., “Tumor susceptibility of rassf1a knockout mice,” Cancer Research, vol. 65, no. 1, pp. 92–98, 2005. View at Google Scholar · View at Scopus
  109. L. van der Weyden, K. K. Tachibana, M. A. Gonzalez et al., “The rassf1a isoform of rassf1 promotes microtubule stability and suppresses tumorigenesis,” Molecular and Cellular Biology, vol. 25, no. 18, pp. 8356–8367, 2005. View at Publisher · View at Google Scholar · View at Scopus
  110. G. Hamilton, K. S. Yee, S. Scrace, and E. O'Neill, “ATM Regulates a rassf1a-Dependent DNA Damage Response,” Current Biology, vol. 19, no. 23, pp. 2020–2025, 2009. View at Publisher · View at Google Scholar · View at Scopus
  111. S. T. Kim, D. S. Lim, C. E. Canman, and M. B. Kastan, “Substrate specificities and identification of putative substrates of ATM kinase family members,” Journal of Biological Chemistry, vol. 274, no. 53, pp. 37538–37543, 1999. View at Publisher · View at Google Scholar · View at Scopus
  112. T. O'Neill, A. J. Dwyer, Y. Ziv et al., “Utilization of oriented peptide libraries to identify substrate motifs selected by ATM,” Journal of Biological Chemistry, vol. 275, no. 30, pp. 22719–22727, 2000. View at Publisher · View at Google Scholar · View at Scopus
  113. C. Guo, S. Tommasi, L. Liu, J. K. Yee, R. Dammann, and G. Pfeifer, “rassf1a Is Part of a Complex Similar to the Drosophila hippo/Salvador/Lats Tumor-Suppressor Network,” Current Biology, vol. 17, no. 8, pp. 700–705, 2007. View at Publisher · View at Google Scholar · View at Scopus
  114. H. Donninger, N. Allen, A. Henson et al., “Salvador protein is a tumor suppressor effector of rassf1a with hippo pathway-independent functions,” Journal of Biological Chemistry, vol. 286, no. 21, pp. 18483–18491, 2011. View at Publisher · View at Google Scholar · View at Scopus
  115. L. J. Saucedo and B. A. Edgar, “Filling out the hippo pathway,” Nature Reviews Molecular Cell Biology, vol. 8, no. 8, pp. 613–621, 2007. View at Publisher · View at Google Scholar · View at Scopus
  116. D. Oceandy, A. Pickard, S. Prehar et al., “Tumor suppressor ras-association domain family 1 Isoform A Is a novel regulator of cardiac hypertrophy,” Circulation, vol. 120, no. 7, pp. 607–616, 2009. View at Publisher · View at Google Scholar · View at Scopus
  117. G. W. Dorn, J. Robbins, and P. H. Sugden, “Phenotyping hypertrophy: Eschew obfuscation,” Circulation Research, vol. 92, no. 11, pp. 1171–1175, 2003. View at Publisher · View at Google Scholar · View at Scopus
  118. E. Marban and Y. Koretsune, “Cell calcium, oncogenes, and hypertrophy,” Hypertension, vol. 15, no. 6, pp. 652–658, 1990. View at Google Scholar · View at Scopus
  119. S. Rabizadeh, R. J. Xavier, K. Ishiguro et al., “The scaffold protein CNK1 interacts with the tumor suppressor rassf1a and augments rassf1a-induced cell death,” Journal of Biological Chemistry, vol. 279, no. 28, pp. 29247–29254, 2004. View at Publisher · View at Google Scholar · View at Scopus
  120. D. P. Del Re, T. Matsuda, P. Zhai et al., “Proapoptotic rassf1a/Mst1 signaling in cardiac fibroblasts is protective against pressure overload in mice,” Journal of Clinical Investigation, vol. 120, no. 10, pp. 3555–3567, 2010. View at Publisher · View at Google Scholar · View at Scopus
  121. A. von Gise, Z. Lin, K. Schlegelmilch et al., “YAP1, the nuclear target of hippo signaling, stimulates heart growth through cardiomyocyte proliferation but not hypertrophy,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 7, pp. 2394–2399, 2012. View at Publisher · View at Google Scholar · View at Scopus
  122. Y. Mao, J. Mulvaney, S. Zakaria et al., “Characterization of a Dchs1 mutant mouse reveals requirements for Dchs1-Fat4 signaling during mammalian development,” Development, vol. 138, no. 5, pp. 947–957, 2011. View at Publisher · View at Google Scholar · View at Scopus
  123. Y. Matsui, N. Nakano, D. Shao et al., “LATS2 is a negative regulator of myocyte size in the heart,” Circulation Research, vol. 103, no. 11, pp. 1309–1318, 2008. View at Publisher · View at Google Scholar · View at Scopus
  124. T. Heallen, M. Zhang, J. Wang et al., “hippo pathway inhibits wnt signaling to restrain cardiomyocyte proliferation and heart size,” Science, vol. 332, no. 6028, pp. 458–461, 2011. View at Publisher · View at Google Scholar · View at Scopus
  125. D. Vavvas, X. Li, J. Avruch, and X. F. Zhang, “Identification of Nore1 as a potential Ras effector,” Journal of Biological Chemistry, vol. 273, no. 10, pp. 5439–5442, 1998. View at Publisher · View at Google Scholar · View at Scopus
  126. A. Moshnikova, J. Frye, J. W. Shay, J. D. Minna, and A. V. Khokhlatchev, “The growth and tumor suppressor NORE1A is a cytoskeletal protein that suppresses growth by inhibition of the ERK pathway,” Journal of Biological Chemistry, vol. 281, no. 12, pp. 8143–8152, 2006. View at Publisher · View at Google Scholar · View at Scopus
  127. A. Khokhlatchev, S. Rabizadeh, R. Xavier et al., “Identification of a novel Ras-regulated proapoptotic pathway,” Current Biology, vol. 12, no. 4, pp. 253–265, 2002. View at Publisher · View at Google Scholar · View at Scopus
  128. M. Praskova, A. Khoklatchev, S. Ortiz-Vega, and J. Avruch, “Regulation of the MST1 kinase by autophosphorylation, by the growth inhibitory proteins, rassf1 and NORE1, and by Ras,” Biochemical Journal, vol. 381, pp. 453–462, 2004. View at Publisher · View at Google Scholar · View at Scopus
  129. H. J. Oh, K. K. Lee, S. J. Song et al., “Role of the tumor suppressor rassf1a in Mst1-mediated apoptosis,” Cancer Research, vol. 66, no. 5, pp. 2562–2569, 2006. View at Publisher · View at Google Scholar · View at Scopus
  130. N. P. C. Allen, H. Donninger, M. D. Vos et al., “rassf6 is a novel member of the RASSF family of tumor suppressors,” Oncogene, vol. 26, no. 42, pp. 6203–6211, 2007. View at Publisher · View at Google Scholar · View at Scopus
  131. M. Ikeda, A. Kawata, M. Nishikawa et al., “hippo pathway-dependent and-independent roles of rassf6,” Science Signaling, vol. 2, no. 90, Article ID ra59, 2009. View at Publisher · View at Google Scholar · View at Scopus