RASSF tumor suppressor gene family: Biological functions and regulation

FEBS Letters

Volumn 588, Issue 16, 2014, Pages 2671-2684

  Volodko, Natalia ^a   Gordon, Marilyn ^a   Salla, Mohamed ^a   Ghazaleh, Haya Abu ^b   Baksh, Shairaz ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b AMERICAN UNIVERSITY OF THE MIDDLE EAST   (Kuwait)

Author keywords

Cancer; Epigenetics; Microtubule; NF B; RASSF; Tumor suppressor

Indexed keywords

5 METHYLCYTOSINE; ATM PROTEIN; BETA CATENIN; CYCLIN DEPENDENT KINASE 4; CYTOSINE; DAXX PROTEIN; DNA METHYLTRANSFERASE 1; INTERLEUKIN 6; MICRORNA; PROTEIN KINASE C; PROTEIN P27; RAS ASSOCIATION DOMAIN FAMILY PROTEIN; RAS ASSOCIATION DOMAIN FAMILY PROTEIN 10; RAS ASSOCIATION DOMAIN FAMILY PROTEIN 1A; RAS ASSOCIATION DOMAIN FAMILY PROTEIN 1C; RAS ASSOCIATION DOMAIN FAMILY PROTEIN 2; RAS ASSOCIATION DOMAIN FAMILY PROTEIN 3; RAS ASSOCIATION DOMAIN FAMILY PROTEIN 4; RAS ASSOCIATION DOMAIN FAMILY PROTEIN 5; RAS ASSOCIATION DOMAIN FAMILY PROTEIN 6; RAS ASSOCIATION DOMAIN FAMILY PROTEIN 7; RAS ASSOCIATION DOMAIN FAMILY PROTEIN 8; RAS ASSOCIATION DOMAIN FAMILY PROTEIN 9; RAS PROTEIN; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR PAX3; TUBULIN; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG; UNINDEXED DRUG;

CANCER INHIBITION; CARCINOGENESIS; CELL CYCLE REGULATION; CELL DEATH; CELL PROLIFERATION; CHRONIC INFLAMMATION; COLITIS; COMPLEX FORMATION; CPG ISLAND; DNA DAMAGE; DNA METHYLATION; EPIGENETICS; GENE SILENCING; GENETIC ASSOCIATION; GENETIC REGULATION; HEART VENTRICLE HYPERTROPHY; HISTONE MODIFICATION; HUMAN; INFLAMMATORY BOWEL DISEASE; MICROTUBULE; ONCOGENE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN METHYLATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN TARGETING; REGULATORY MECHANISM; REVIEW; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION;

CANCER; EPIGENETICS; MICROTUBULE; NFΚB; RASSF; TUMOR SUPPRESSOR;

ANIMALS; EPIGENESIS, GENETIC; HUMANS; MICRORNAS; PROTEIN PROCESSING, POST-TRANSLATIONAL; TUMOR SUPPRESSOR PROTEINS;

EID: 84905120617     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2014.02.041     Document Type: Review

References (191)

1. M. Gordon, and S. Baksh RASSF1A: not a prototypical Ras effector Small GTPases 2 2010 148 157
2. A.M. Richter, G.P. Pfeifer, and R.H. Dammann The RASSF proteins in cancer; from epigenetic silencing to functional characterization Biochim. Biophys. Acta 1796 2 2009 114 128 15p
3. V. Sherwood, A. Recino, A. Jeffries, A. Ward, and A.D. Chalmers The N-terminal RASSF family: a new group of Ras-association-domain-containing proteins, with emerging links to cancer formation Biochem. J. 425 2009 303 311
4. F.E. Lock, N. Underhill-Day, T. Dunwell, D. Matallanas, W. Cooper, L. Hesson, A. Recino, A. Ward, T. Pavlova, E. Zabarovsky, M.M. Grant, E.R. Maher, A.D. Chalmers, W. Kolch, and F. Latif The RASSF8 candidate tumor suppressor inhibits cell growth and regulates the Wnt and NF-kappaB signaling pathways Oncogene 29 2010 4307 4316
5. E. Estrabaud, I. Lassot, G. Blot, E. Le Rouzic, V. Tanchou, E. Quemeneur, L. Daviet, F. Margottin-Goguet, and R. Benarous RASSF1C, an isoform of the tumor suppressor RASSF1A, promotes the accumulation of {beta}-catenin by interacting with {beta}TrCP Cancer Res. 67 2007 1054 1061
6. H. Fujita, S. Fukuhara, A. Sakurai, A. Yamagishi, Y. Kamioka, Y. Nakaoka, M. Masuda, and N. Mochizuki Local activation of Rap1 contributes to directional vascular endothelial cell migration accompanied by extension of microtubules on which RAPL, a Rap1-associating molecule, localizes J. Biol. Chem. 280 2005 5022 5031
7. M.D. Vos, A. Martinez, C.A. Ellis, T. Vallecorsa, and G.J. Clark The pro-apoptotic Ras effector Nore1 may serve as a Ras-regulated tumor suppressor in the lung J. Biol. Chem. 278 2003 21938 21943
8. K. Eckfeld, L. Hesson, M.D. Vos, I. Bieche, F. Latif, and G.J. Clark RASSF4/AD037 is a potential ras effector/tumor suppressor of the RASSF family Cancer Res. 64 2004 8688 8693
9. J. Avruch, R. Xavier, N. Bardeesy, X.F. Zhang, M. Praskova, D. Zhou, and F. Xia Rassf family of tumor suppressor polypeptides J. Biol. Chem. 284 2009 11001 11005
10. M. El-Kalla, C. Onyskiw, and S. Baksh Functional importance of RASSF1A microtubule localization and polymorphisms Oncogene 29 2010 5729 5740
11. G. Hamilton, K.S. Yee, S. Scrace, and E. O'Neill ATM regulates a RASSF1A-dependent DNA damage response Curr. Biol. 19 2009 2020 2025
12. S.F. Scrace, and E. O'Neill RASSF signalling and DNA damage: monitoring the integrity of the genome? Mol. Biol. Int. 2012 2012 141732
13. 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 Nat. Genet. 25 2000 315 319
14. A. Dallol, A. Agathanggelou, S.L. Fenton, J. Ahmed-Choudhury, L. Hesson, M.D. Vos, G.J. Clark, J. Downward, E.R. Maher, and F. Latif RASSF1A interacts with microtubule-associated proteins and modulates microtubule dynamics Cancer Res. 64 2004 4112 4116
15. A. Dallol, A. Agathanggelou, S. Tommasi, G.P. Pfeifer, E.R. Maher, and F. Latif Involvement of the RASSF1A tumor suppressor gene in controlling cell migration Cancer Res. 65 2005 7653 7659
16. Y.G. Amaar, M.G. Minera, L.K. Hatran, D.D. Strong, S. Mohan, and M.E. Reeves Ras association domain family 1C protein stimulates human lung cancer cell proliferation Am. J. Physiol. Lung Cell Mol. Physiol. 291 2006 L1185 L1190
17. M.E. Reeves, S.W. Baldwin, M.L. Baldwin, S.T. Chen, J.M. Moretz, R.J. Aragon, X. Li, D.D. Strong, S. Mohan, and Y.G. Amaar Ras-association domain family 1C protein promotes breast cancer cell migration and attenuates apoptosis BMC Cancer 10 2010 562
18. Y.G. Amaar, D.J. Baylink, and S. Mohan Ras-association domain family 1 protein, RASSF1C, is an IGFBP-5 binding partner and a potential regulator of osteoblast cell proliferation J. Bone Miner. Res. 20 2005 1430 1439
19. M.D. Vos, A. Martinez, C. Elam, A. Dallol, B.J. Taylor, F. Latif, and G.J. Clark A role for the RASSF1A tumor suppressor in the regulation of tubulin polymerization and genomic stability Cancer Res. 64 2004 4244 4250
20. L. Liu, S. Tommasi, D.H. Lee, R. Dammann, and G.P. Pfeifer Control of microtubule stability by the RASSF1A tumor suppressor Oncogene 22 2003 8125 8136
21. R. Rong, W. Jin, J. Zhang, M.S. Sheikh, and Y. Huang Tumor suppressor RASSF1A is a microtubule-binding protein that stabilizes microtubules and induces G2/M arrest Oncogene 23 2004 8216 8230
22. A. Dallol, L.B. Hesson, D. Matallanas, W.N. Cooper, E. O'Neill, E.R. Maher, W. Kolch, and F. Latif RAN GTPase is a RASSF1A effector involved in controlling microtubule organization Curr. Biol. 19 2009 1227 1232
23. H.Y. Jung, J.S. Jung, Y.M. Whang, and Y.H. Kim RASSF1A suppresses cell migration through inactivation of HDAC6 and increase of acetylated alpha-tubulin Cancer Res. Treat. 45 2013 134 144
24. R. Korah, J.M. Healy, J.W. Kunstman, A.L. Fonseca, A.H. Ameri, M.L. Prasad, and T. Carling Epigenetic silencing of RASSF1A deregulates cytoskeleton and promotes malignant behavior of adrenocortical carcinoma Mol. Cancer 12 2013 87
25. M.S. Song, J.S. Chang, S.J. Song, T.H. Yang, H. Lee, and D.S. Lim The centrosomal protein RAS association domain family protein 1A (RASSF1A)-binding protein 1 regulates mitotic progression by recruiting RASSF1A to spindle poles J. Biol. Chem. 280 2005 3920 3927
26. L. Liu, K. Baier, R. Dammann, and G.P. Pfeifer The tumor suppressor RASSF1A does not interact with Cdc20, an activator of the anaphase-promoting complex Cell Cycle 6 2007 1663 1665
27. M.S. Song, and D.S. Lim Control of APC-Cdc20 by the tumor suppressor RASSF1A Cell Cycle 3 2004 574 576
28. M.S. Song, S.J. Song, N.G. Ayad, J.S. Chang, J.H. Lee, H.K. Hong, H. Lee, N. Choi, J. Kim, H. Kim, J.W. Kim, E.J. Choi, M.W. Kirschner, and D.S. Lim The tumour suppressor RASSF1A regulates mitosis by inhibiting the APC-Cdc20 complex Nat. Cell Biol. 6 2004 129 137
29. S.J. Song, M.S. Song, S.J. Kim, S.Y. Kim, S.H. Kwon, J.G. Kim, D.F. Calvisi, D. Kang, and D.S. Lim Aurora A regulates prometaphase progression by inhibiting the ability of RASSF1A to suppress APC-Cdc20 activity Cancer Res. 69 2009 2314 2323
30. R. Xie, S. Nguyen, K. McKeehan, F. Wang, W.L. McKeehan, and L. Liu Microtubule-associated protein 1s (MAP1S) bridges autophagic components with microtubules and mitochondria to affect autophagosomal biogenesis and degradation J. Biol. Chem. 286 12 2011 10367 10377
31. 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 Mol. Cell. Biol. 22 2002 4309 4318
32. Y.M. Whang, Y.H. Kim, J.S. Kim, and Y.D. Yoo RASSF1A suppresses the c-Jun-NH2-kinase pathway and inhibits cell cycle progression Cancer Res. 65 2005 3682 3690
33. S.L. Fenton, A. Dallol, A. Agathanggelou, L. Hesson, J. Ahmed-Choudhury, S. Baksh, C. Sardet, R. Dammann, J.D. Minna, J. Downward, E.R. Maher, and F. Latif Identification of the E1A-regulated transcription factor p120 E4F as an interacting partner of the RASSF1A candidate tumor suppressor gene Cancer Res. 64 2004 102 107
34. J. Ahmed-Choudhury, A. Agathanggelou, S.L. Fenton, C. Ricketts, G.J. Clark, E.R. Maher, and F. Latif Transcriptional regulation of cyclin A2 by RASSF1A through the enhanced binding of p120E4F to the cyclin A2 promoter Cancer Res. 65 2005 2690 2697
35. S. Thaler, P.S. Hahnel, A. Schad, R. Dammann, and M. Schuler RASSF1A mediates p21Cip1/Waf1-dependent cell cycle arrest and senescence through modulation of the Raf-MEK-ERK pathway and inhibition of Akt Cancer Res. 69 2009 1748 1757
36. M.S. Song, S.J. Song, S.Y. Kim, H.J. Oh, and D.S. Lim The tumour suppressor RASSF1A promotes MDM2 self-ubiquitination by disrupting the MDM2-DAXX-HAUSP complex EMBO J. 27 2008 1863 1874
37. L.K. Su, K.W. Kinzler, B. Vogelstein, A.C. Preisinger, A.R. Moser, C. Luongo, K.A. Gould, and W.F. Dove Multiple intestinal neoplasia caused by a mutation in the murine homolog of the APC gene Science 256 1992 668 670
38. A.M. Carothers, K.A. Melstrom Jr.; J.D. Mueller, M.J. Weyant, and M.M. Bertagnolli Progressive changes in adherens junction structure during intestinal adenoma formation in Apc mutant mice J. Biol. Chem. 276 2001 39094 39102
39. L. van der Weyden, M.J. Arends, O.M. Dovey, H.L. Harrison, G. Lefebvre, N. Conte, F.V. Gergely, A. Bradley, and D.J. Adams Loss of Rassf1a cooperates with Apc(Min) to accelerate intestinal tumourigenesis Oncogene 27 2008 4503 4508
40. S. Baksh, S. Tommasi, S. Fenton, V.C. Yu, L.M. Martins, G.P. Pfeifer, F. Latif, J. Downward, and B.G. Neel The tumor suppressor RASSF1A and MAP-1 link death receptor signaling to Bax conformational change and cell death Mol. Cell 18 2005 637 650
41. C.J. Foley, H. Freedman, S.L. Choo, C. Onyskiw, N.Y. Fu, V.C. Yu, J. Tuszynski, J.C. Pratt, and S. Baksh Dynamics of RASSF1A/MOAP-1 association with death receptors Mol. Cell. Biol. 28 2008 4520 4535
42. H.J. Oh, K.K. Lee, S.J. Song, M.S. Jin, M.S. Song, J.H. Lee, C.R. Im, J.O. Lee, S. Yonehara, and D.S. Lim Role of the tumor suppressor RASSF1A in Mst1-mediated apoptosis Cancer Res. 66 2006 2562 2569
43. A. Khokhlatchev, S. Rabizadeh, R. Xavier, M. Nedwidek, T. Chen, X.F. Zhang, B. Seed, and J. Avruch Identification of a novel Ras-regulated proapoptotic pathway Curr. Biol. 12 2002 253 265
44. 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 Biochem. J. 381 2004 453 462
45. D. Matallanas, D. Romano, K. Yee, K. Meissl, L. Kucerova, D. Piazzolla, M. Baccarini, J.K. Vass, W. Kolch, and E. O'Neill RASSF1A elicits apoptosis through an MST2 pathway directing proapoptotic transcription by the p73 tumor suppressor protein Mol. Cell 27 2007 962 975
46. M. Gordon, M. El-Kalla, Y. Zhao, Y. Fiteih, J. Law, N. Volodko, A. Mohamed, A.O. El-Kadi, L. Liu, J. Odenbach, A. Thiesen, C. Onyskiw, H.A. Ghazaleh, J. Park, S.B. Lee, V.C. Yu, C. Fernandez-Patron, R.T. Alexander, E. Wine, and S. Baksh The tumor suppressor gene, RASSF1A, is essential for protection against inflammation-induced injury PLoS One 8 2013 e75483
47. S. Tommasi, R. Dammann, Z. Zhang, Y. Wang, L. Liu, W.M. Tsark, S.P. Wilczynski, J. Li, M. You, and G.P. Pfeifer Tumor susceptibility of Rassf1a knockout mice Cancer Res. 65 2005 92 98
48. L. van der Weyden, K.K. Tachibana, M.A. Gonzalez, D.J. Adams, B.L. Ng, R. Petty, A.R. Venkitaraman, M.J. Arends, and A. Bradley The RASSF1A isoform of RASSF1 promotes microtubule stability and suppresses tumorigenesis Mol. Cell. Biol. 25 2005 8356 8367
49. D. Oceandy, A. Pickard, S. Prehar, M. Zi, T.M. Mohamed, P.J. Stanley, F. Baudoin-Stanley, R. Nadif, S. Tommasi, G.P. Pfeifer, A.L. Armesilla, E.J. Cartwright, and L. Neyses Tumor suppressor Ras-association domain family 1 isoform A is a novel regulator of cardiac hypertrophy Circulation 120 2009 607 616
50. D.P. Del Re, T. Matsuda, P. Zhai, S. Gao, G.J. Clark, L. Van Der Weyden, and J. Sadoshima Proapoptotic Rassf1A/Mst1 signaling in cardiac fibroblasts is protective against pressure overload in mice J. Clin. Invest. 120 2010 3555 3567
51. C. Duan, M. Liu, J. Zhang, and R. Ma RASSF1A: a potential novel therapeutic target against cardiac hypertrophy Prog. Biophys. Mol. Biol. 113 2013 284 288
52. L. van der Weyden, L. Happerfield, M.J. Arends, and D.J. Adams Megaoesophagus in Rassf1a-null mice Int. J. Exp. Pathol. 90 2009 101 108
53. X. Zhou, T.T. Li, X. Feng, E. Hsiang, Y. Xiong, K.L. Guan, and Q.Y. Lei Targeted polyubiquitylation of RASSF1C by the Mule and SCFbeta-TrCP ligases in response to DNA damage Biochem. J. 441 2010 227 236
54. D. Kitagawa, H. Kajiho, T. Negishi, S. Ura, T. Watanabe, T. Wada, H. Ichijo, T. Katada, and H. Nishina Release of RASSF1C from the nucleus by Daxx degradation links DNA damage and SAPK/JNK activation EMBO J. 25 2006 3286 3297
55. E. Escobar-Cabrera, D.K. Lau, S. Giovinazzi, A.M. Ishov, and L.P. McIntosh Structural characterization of the DAXX N-terminal helical bundle domain and its complex with Rassf1C Structure 18 2010 1642 1653
56. X. Chen, Z. Li, J. Zhang, Z. Mao, D. Ma, and H. Wang Tissue factor pathway inhibitor-2 may interact with nuclear protein RASSF1C Acta Biochim. Biophys. Sin. 44 2012 183 185
57. W.N. Cooper, R.E. Dickinson, A. Dallol, E.V. Grigorieva, T.V. Pavlova, L.B. Hesson, I. Bieche, M. Broggini, E.R. Maher, E.R. Zabarovsky, G.J. Clark, and F. Latif Epigenetic regulation of the ras effector/tumour suppressor RASSF2 in breast and lung cancer Oncogene 27 2008 1805 1811
58. K. Akino, M. Toyota, H. Suzuki, H. Mita, Y. Sasaki, M. Ohe-Toyota, J.P. Issa, Y. Hinoda, K. Imai, and T. Tokino The Ras effector RASSF2 is a novel tumor-suppressor gene in human colorectal cancer Gastroenterology 129 2005 156 169
59. L.B. Hesson, R. Wilson, D. Morton, C. Adams, M. Walker, E.R. Maher, and F. Latif CpG island promoter hypermethylation of a novel Ras-effector gene RASSF2A is an early event in colon carcinogenesis and correlates inversely with K-ras mutations Oncogene 24 2005 3987 3994
60. Z. Zhang, D. Sun, N. Van do, A. Tang, L. Hu, and G. Huang Inactivation of RASSF2A by promoter methylation correlates with lymph node metastasis in nasopharyngeal carcinoma Int. J. Cancer 120 2007 32 38
61. H.W. Park, H.C. Kang, I.J. Kim, S.G. Jang, K. Kim, H.J. Yoon, S.Y. Jeong, and J.G. Park Correlation between hypermethylation of the RASSF2A promoter and K-ras/BRAF mutations in microsatellite-stable colorectal cancers Int. J. Cancer 120 2007 7 12
62. M.D. Vos, C.A. Ellis, C. Elam, A.S. Ulku, B.J. Taylor, and G.J. Clark RASSF2 is a novel K-Ras-specific effector and potential tumor suppressor J. Biol. Chem. 278 2003 28045 28051
63. G. Kumari, and S. Mahalingam Extracellular signal-regulated kinase 2 (ERK-2) mediated phosphorylation regulates nucleo-cytoplasmic shuttling and cell growth control of Ras-associated tumor suppressor protein, RASSF2 Exp. Cell Res. 315 2009 2775 2790
64. H. Donninger, L. Hesson, M. Vos, K. Beebe, L. Gordon, D. Sidransky, J.W. Liu, T. Schlegel, S. Payne, A. Hartmann, F. Latif, and G.J. Clark The Ras effector RASSF2 controls the PAR-4 tumor suppressor Mol. Cell. Biol. 30 2010 2608 2620
65. N. El-Guendy, Y. Zhao, S. Gurumurthy, R. Burikhanov, and V.M. Rangnekar Identification of a unique core domain of par-4 sufficient for selective apoptosis induction in cancer cells Mol. Cell. Biol. 23 2003 5516 5525
66. H. Song, S. Oh, H.J. Oh, and D.S. Lim Role of the tumor suppressor RASSF2 in regulation of MST1 kinase activity Biochem. Biophys. Res. Commun. 391 2010 969 973
67. H. Song, H. Kim, K. Lee, D.H. Lee, T.S. Kim, J.Y. Song, D. Lee, D. Choi, C.Y. Ko, H.S. Kim, H.I. Shin, J. Choi, H. Park, C. Park, D. Jeong, and D.S. Lim Ablation of Rassf2 induces bone defects and subsequent haematopoietic anomalies in mice EMBO J. 31 2012 1147 1159
68. S. Tommasi, R. Dammann, S.G. Jin, X.F. Zhang, J. Avruch, and G.P. Pfeifer RASSF3 and NORE1: identification and cloning of two human homologues of the putative tumor suppressor gene RASSF1 Oncogene 21 2002 2713 2720
69. H. Peng, H. Liu, S. Zhao, J. Wu, J. Fan, and J. Liao Silencing of RASSF3 by DNA hypermethylation is associated with tumorigenesis in somatotroph adenomas PLoS One 8 2013 e59024
70. A. Fukatsu, F. Ishiguro, I. Tanaka, T. Kudo, K. Nakagawa, K. Shinjo, Y. Kondo, M. Fujii, Y. Hasegawa, K. Tomizawa, T. Mitsudomi, H. Osada, Y. Hata, and Y. Sekido RASSF3 downregulation increases malignant phenotypes of non-small cell lung cancer Lung Cancer 83 1 2014 23 39
71. I.C. Jacquemart, A.E. Springs, and W.Y. Chen Rassf3 is responsible in part for resistance to mammary tumor development in neu transgenic mice Int. J. Oncol. 34 2009 517 528
72. T. Kudo, M. Ikeda, M. Nishikawa, Z. Yang, K. Ohno, K. Nakagawa, and Y. Hata The RASSF3 candidate tumor suppressor induces apoptosis and G1-S cell-cycle arrest via p53 Cancer Res. 72 2012 2901 2911
73. K. Steinmann, A. Sandner, U. Schagdarsurengin, and R.H. Dammann Frequent promoter hypermethylation of tumor-related genes in head and neck squamous cell carcinoma Oncol. Rep. 22 2009 1519 1526
74. L.S. Chow, K.W. Lo, J. Kwong, A.Y. Wong, and D.P. Huang Aberrant methylation of RASSF4/AD037 in nasopharyngeal carcinoma Oncol. Rep. 12 2004 781 787
75. L.E. Crose, K.A. Galindo, J.G. Kephart, C. Chen, J. Fitamant, N. Bardeesy, R.C. Bentley, R.L. Galindo, J.T. Ashley Chi, and C.M. Linardic Alveolar rhabdomyosarcoma-associated PAX3-FOXO1 promotes tumorigenesis via Hippo pathway suppression J. Clin. Invest. 124 2014 285 296
76. P.H. Sorensen, J.C. Lynch, S.J. Qualman, R. Tirabosco, J.F. Lim, H.M. Maurer, J.A. Bridge, W.M. Crist, T.J. Triche, and F.G. Barr PAX3-FKHR and PAX7-FKHR gene fusions are prognostic indicators in alveolar rhabdomyosarcoma: a report from the children's oncology group J. Clin. Oncol. 20 2002 2672 2679
77. Y. Michifuri, Y. Hirohashi, T. Torigoe, A. Miyazaki, J. Fujino, Y. Tamura, T. Tsukahara, T. Kanaseki, J. Kobayashi, T. Sasaki, A. Takahashi, K. Nakamori, A. Yamaguchi, H. Hiratsuka, and N. Sato Small proline-rich protein-1B is overexpressed in human oral squamous cell cancer stem-like cells and is related to their growth through activation of MAP kinase signal Biochem. Biophys. Res. Commun. 439 2013 96 102
78. D. Vavvas, X. Li, J. Avruch, and X.F. Zhang Identification of Nore1 as a potential Ras effector J. Biol. Chem. 273 1998 5439 5442
79. 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 The Journal of biological chemistry. 281 2006 8143 8152
80. J. Park, S.I. Kang, S.Y. Lee, X.F. Zhang, M.S. Kim, L.F. Beers, D.S. Lim, J. Avruch, H.S. Kim, and S.B. Lee Tumor suppressor Ras-association domain family 5 (RASSF5/NORE1) mediates death receptor ligand-induced apoptosis The Journal of biological chemistry. 285 2010 35029 35038
81. S. Ortiz-Vega, A. Khokhlatchev, M. Nedwidek, X.F. Zhang, R. Dammann, G.P. Pfeifer, and J. Avruch The putative tumor suppressor RASSF1A homodimerizes and heterodimerizes with the Ras-GTP binding protein Nore1 Oncogene 21 2002 1381 1390
82. Y. Aoyama, J. Avruch, and X.F. Zhang Nore1 inhibits tumor cell growth independent of Ras or the MST1/2 kinases Oncogene 23 2004 3426 3433
83. T. Nakamura, S. Yasuda, H. Nagai, S. Koinuma, S. Morishita, A. Goto, T. Kinashi, and N. Wada Longest neurite-specific activation of Rap1B in hippocampal neurons contributes to polarity formation through RalA and Nore1A in addition to PI3-kinase Genes to cells: devoted to molecular & cellular mechanisms. 18 2013 1020 1031
84. K. Katagiri, A. Maeda, M. Shimonaka, and T. Kinashi RAPL, a Rap1-binding molecule that mediates Rap1-induced adhesion through spatial regulation of LFA-1 Nat. Immunol. 4 2003 741 748
85. K. Katagiri, Y. Ueda, T. Tomiyama, K. Yasuda, Y. Toda, S. Ikehara, K.I. Nakayama, and T. Kinashi Deficiency of Rap1-binding protein RAPL causes lymphoproliferative disorders through mislocalization of p27kip1 Immunity 34 2011 24 38
86. K. Katagiri, N. Ohnishi, K. Kabashima, T. Iyoda, N. Takeda, Y. Shinkai, K. Inaba, and T. Kinashi Crucial functions of the Rap1 effector molecule RAPL in lymphocyte and dendritic cell trafficking Nat. Immunol. 5 2004 1045 1051
87. N.P. Allen, H. Donninger, M.D. Vos, K. Eckfeld, L. Hesson, L. Gordon, M.J. Birrer, F. Latif, and G.J. Clark RASSF6 is a novel member of the RASSF family of tumor suppressors Oncogene 26 2007 6203 6211
88. J. Hull, K. Rowlands, E. Lockhart, M. Sharland, C. Moore, N. Hanchard, and D.P. Kwiatkowski Haplotype mapping of the bronchiolitis susceptibility locus near IL8 Hum. Genet. 114 2004 272 279
89. L. van der Weyden, and D.J. Adams The Ras-association domain family (RASSF) members and their role in human tumourigenesis Biochim. Biophys. Acta 1776 2007 58 85
90. A. Djos, T. Martinsson, P. Kogner, and H. Caren The RASSF gene family members RASSF5, RASSF6 and RASSF7 show frequent DNA methylation in neuroblastoma Mol. Cancer 11 2012 40
91. L.B. Hesson, T.L. Dunwell, W.N. Cooper, D. Catchpoole, A.T. Brini, R. Chiaramonte, M. Griffiths, A.D. Chalmers, E.R. Maher, and F. Latif The novel RASSF6 and RASSF10 candidate tumour suppressor genes are frequently epigenetically inactivated in childhood leukaemias Mol. Cancer 8 2009 42
92. M. Ikeda, S. Hirabayashi, N. Fujiwara, H. Mori, A. Kawata, J. Iida, Y. Bao, Y. Sato, T. Iida, H. Sugimura, and Y. Hata Ras-association domain family protein 6 induces apoptosis via both caspase-dependent and caspase-independent pathways Exp. Cell Res. 313 7 2007 1484 1495 12p
93. M. Ikeda, A. Kawata, M. Nishikawa, Y. Tateishi, M. Yamaguchi, K. Nakagawa, S. Hirabayashi, Y. Bao, S. Hidaka, Y. Hirata, and Y. Hata Hippo pathway-dependent and -independent roles of RASSF6 Sci. Signal. 2 2009 ra59
94. H. Iwasa, T. Kudo, S. Maimaiti, M. Ikeda, J. Maruyama, K. Nakagawa, and Y. Hata The RASSF6 tumor suppressor protein regulates apoptosis and the cell cycle via MDM2 protein and p53 protein J. Biol. Chem. 288 2013 30320 30329
95. J.N. Weitzel, and J. Patel A single P1 clone bearing three genes from human chromosome 11p15.5: HRC1, HRAS1, and RNH Genet. Anal. Tech. Appl. 11 1994 165 170
96. A.W. Lowe, M. Olsen, Y. Hao, S.P. Lee, K. Taek Lee, X. Chen, M. van de Rijn, and P.O. Brown Gene expression patterns in pancreatic tumors, cells and tissues PLoS One 2 2007 e323
97. R. Brandt, R. Grutzmann, A. Bauer, R. Jesnowski, J. Ringel, M. Lohr, C. Pilarsky, and J.D. Hoheisel DNA microarray analysis of pancreatic malignancies, Pancreatology: official journal of the International Association of Pancreatology 4 2004 587 597
98. H. Friess, J. Ding, J. Kleeff, L. Fenkell, J.A. Rosinski, A. Guweidhi, J.F. Reidhaar-Olson, M. Korc, J. Hammer, and M.W. Buchler Microarray-based identification of differentially expressed growth- and metastasis-associated genes in pancreatic cancer Cell. Mol. Life Sci. 60 2003 1180 1199
99. C.D. Logsdon, D.M. Simeone, C. Binkley, T. Arumugam, J.K. Greenson, T.J. Giordano, D.E. Misek, R. Kuick, and S. Hanash Molecular profiling of pancreatic adenocarcinoma and chronic pancreatitis identifies multiple genes differentially regulated in pancreatic cancer Cancer Res. 63 2003 2649 2657
100. G.L. Mutter, J.P. Baak, J.T. Fitzgerald, R. Gray, D. Neuberg, G.A. Kust, R. Gentleman, S.R. Gullans, L.J. Wei, and M. Wilcox Global expression changes of constitutive and hormonally regulated genes during endometrial neoplastic transformation Gynecol. Oncol. 83 2001 177 185
101. D.S. Tan, M.B. Lambros, S. Rayter, R. Natrajan, R. Vatcheva, Q. Gao, C. Marchio, F.C. Geyer, K. Savage, S. Parry, K. Fenwick, N. Tamber, A. Mackay, T. Dexter, C. Jameson, W.G. McCluggage, A. Williams, A. Graham, D. Faratian, M. El-Bahrawy, A.J. Paige, H. Gabra, M.E. Gore, M. Zvelebil, C.J. Lord, S.B. Kaye, A. Ashworth, and J.S. Reis-Filho PPM1D is a potential therapeutic target in ovarian clear cell carcinomas Clin. Cancer Res. 15 2009 2269 2280
102. A. Recino, V. Sherwood, A. Flaxman, W.N. Cooper, F. Latif, A. Ward, and A.D. Chalmers Human RASSF7 regulates the microtubule cytoskeleton and is required for spindle formation, Aurora B activation and chromosomal congression during mitosis Biochem. J. 430 2010 207 213
103. V. Sherwood, R. Manbodh, C. Sheppard, and A.D. Chalmers RASSF7 is a member of a new family of RAS association domain-containing proteins and is required for completing mitosis Mol. Biol. Cell 19 4 2008 1772 1782
104. S. Takahashi, A. Ebihara, H. Kajiho, K. Kontani, H. Nishina, and T. Katada RASSF7 negatively regulates pro-apoptotic JNK signaling by inhibiting the activity of phosphorylated-MKK7 Cell Death Differ. 18 2011 645 655
105. F.S. Falvella, G. Manenti, M. Spinola, C. Pignatiello, B. Conti, U. Pastorino, and T.A. Dragani Identification of RASSF8 as a candidate lung tumor suppressor gene Oncogene 25 2006 3934 3938
106. E.I. Rykova, T.E. Skvortsova, A.L. Hoffmann, S.N. Tamkovich, A.V. Starikov, O.E. Bryzgunova, V.I. Permiakova, J.M. Warnecke, G. Sczakiel, V.V. Vlasov, and P.P. Laktionov Breast cancer diagnostics based on extracellular DNA and RNA circulating in blood Biomed. Khim. 54 2008 94 103
107. J. Jin, F.D. Smith, C. Stark, C.D. Wells, J.P. Fawcett, S. Kulkarni, P. Metalnikov, P. O'Donnell, P. Taylor, L. Taylor, A. Zougman, J.R. Woodgett, L.K. Langeberg, J.D. Scott, and T. Pawson Proteomic, functional, and domain-based analysis of in vivo 14-3-3 binding proteins involved in cytoskeletal regulation and cellular organization Curr. Biol. 14 2004 1436 1450
108. M.J. van Hemert, H.Y. Steensma, and G.P. van Heusden 14-3-3 Proteins: key regulators of cell division, signalling and apoptosis Bioessays 23 2001 936 946
109. H.A. Ghazaleh, R.S. Chow, S.L. Choo, D. Pham, J.D. Olesen, R.X. Wong, C. Onyskiw, and S. Baksh 14-3-3 Mediated regulation of the tumor suppressor protein, RASSF1A Apoptosis 15 2010 117 127
110. L. Chen, R.C. Johnson, and S.L. Milgram P-CIP1, a novel protein that interacts with the cytosolic domain of peptidylglycine alpha-amidating monooxygenase, is associated with endosomes J. Biol. Chem. 273 1998 33524 33532
111. M.R. Alam, B.D. Caldwell, R.C. Johnson, D.N. Darlington, R.E. Mains, and B.A. Eipper Novel proteins that interact with the COOH-terminal cytosolic routing determinants of an integral membrane peptide-processing enzyme J. Biol. Chem. 271 1996 28636 28640
112. C.M. Lee, P. Yang, L.C. Chen, C.C. Chen, S.C. Wu, H.Y. Cheng, and Y.S. Chang A novel role of RASSF9 in maintaining epidermal homeostasis PLoS One 6 2011 e17867
113. V.K. Hill, N. Underhill-Day, D. Krex, K. Robel, C.B. Sangan, H.R. Summersgill, M. Morris, D. Gentle, A.D. Chalmers, E.R. Maher, and F. Latif Epigenetic inactivation of the RASSF10 candidate tumor suppressor gene is a frequent and an early event in gliomagenesis Oncogene 30 2011 978 989
114. U. Schagdarsurengin, A.M. Richter, C. Wohler, and R.H. Dammann Frequent epigenetic inactivation of RASSF10 in thyroid cancer Epigenetics 4 2009 571 576
115. T. Dansranjavin, F. Wagenlehner, S. Gattenloehner, K. Steger, W. Weidner, R. Dammann, and U. Schagdarsurengin Epigenetic down regulation of RASSF10 and its possible clinical implication in prostate carcinoma Prostate 72 2012 1550 1558
116. Z. Wei, X. Chen, J. Chen, W. Wang, X. Xu, and Q. Cai RASSF10 is epigenetically silenced and functions as a tumor suppressor in gastric cancer Biochem. Biophys. Res. Commun. 432 2013 632 637
117. S. Hu, J. Wan, Y. Su, Q. Song, Y. Zeng, H.N. Nguyen, J. Shin, E. Cox, H.S. Rho, C. Woodard, S. Xia, S. Liu, H. Lyu, G.L. Ming, H. Wade, H. Song, J. Qian, and H. Zhu DNA methylation presents distinct binding sites for human transcription factors eLife 2 2013 e00726
118. K.N. Harikrishnan, M.Z. Chow, E.K. Baker, S. Pal, S. Bassal, D. Brasacchio, L. Wang, J.M. Craig, P.L. Jones, S. Sif, and A. El-Osta Brahma links the SWI/SNF chromatin-remodeling complex with MeCP2-dependent transcriptional silencing Nat. Genet. 37 2005 254 264
119. J.K. Christman 5-Azacytidine and 5-aza-2′-deoxycytidine as inhibitors of DNA methylation: mechanistic studies and their implications for cancer therapy Oncogene 21 2002 5483 5495
120. J. Klajic, T. Fleischer, E. Dejeux, H. Edvardsen, F. Warnberg, I. Bukholm, P.E. Lonning, H. Solvang, A.L. Borresen-Dale, J. Tost, and V.N. Kristensen Quantitative DNA methylation analyses reveal stage dependent DNA methylation and association to clinico-pathological factors in breast tumors BMC Cancer 13 2013 456
121. L. Du, Z. Xie, L.C. Wu, M. Chiu, J. Lin, K.K. Chan, S. Liu, and Z. Liu Reactivation of RASSF1A in breast cancer cells by curcumin Nutr. Cancer 64 2012 1228 1235
122. S. Kang, H.S. Kim, S.S. Seo, S.Y. Park, D. Sidransky, and S.M. Dong Inverse correlation between RASSF1A hypermethylation, KRAS and BRAF mutations in cervical adenocarcinoma Gynecol. Oncol. 105 2007 662 666
123. M. Brait, M. Loyo, E. Rosenbaum, K.L. Ostrow, A. Markova, S. Papagerakis, M. Zahurak, S.M. Goodman, M. Zeiger, D. Sidransky, C.B. Umbricht, and M.O. Hoque Correlation between BRAF mutation and promoter methylation of TIMP3, RARbeta2 and RASSF1A in thyroid cancer Epigenetics 7 2012 710 719
124. N. Nakamura, J.A. Carney, L. Jin, S. Kajita, J. Pallares, H. Zhang, X. Qian, T.J. Sebo, L.A. Erickson, and R.V. Lloyd RASSF1A and NORE1A methylation and BRAFV600E mutations in thyroid tumors Lab. Invest. 85 2005 1065 1075
125. M. Xing, Y. Cohen, E. Mambo, G. Tallini, R. Udelsman, P.W. Ladenson, and D. Sidransky Early occurrence of RASSF1A hypermethylation and its mutual exclusion with BRAF mutation in thyroid tumorigenesis Cancer Res. 64 2004 1664 1668
126. M. Haruta, Y. Matsumoto, H. Izumi, N. Watanabe, M. Fukuzawa, S. Matsuura, and Y. Kaneko Combined BubR1 protein down-regulation and RASSF1A hypermethylation in Wilms tumors with diverse cytogenetic changes Mol. Carcinog. 47 2008 660 666
127. H. Donninger, M.D. Vos, and G.J. Clark The RASSF1A tumor suppressor J. Cell Sci. 120 2007 3163 3172
128. D. Zare-Abdollahi, S. Safari, A. Movafagh, M. Ghadiani, S. Riazi-Isfahani, and M.D. Omrani Intact expression status of RASSF1A in acute myeloid leukemia Med. Oncol. 31 2014 770
129. G. Malpeli, E. Amato, M. Dandrea, C. Fumagalli, V. Debattisti, L. Boninsegna, G. Pelosi, M. Falconi, and A. Scarpa Methylation-associated down-regulation of RASSF1A and up-regulation of RASSF1C in pancreatic endocrine tumors BMC Cancer 11 2010 351
130. P.S. Yan, H. Shi, F. Rahmatpanah, T.H. Hsiau, A.H. Hsiau, Y.W. Leu, J.C. Liu, and T.H. Huang Differential distribution of DNA methylation within the RASSF1A CpG island in breast cancer Cancer Res. 63 2003 6178 6186
131. H.E. Abouzeid, A.M. Kassem, A.H. Abdel Wahab, H.A. El-mezayen, H. Sharad, and S. Abdel Rahman Promoter hypermethylation of RASSF1A, MGMT, and HIC-1 genes in benign and malignant colorectal tumors Tumour Biol. 32 2010 845 852
132. L. de Ridder, M.A. Benninga, J.A. Taminiau, D.W. Hommes, and S.J. van Deventer Infliximab use in children and adolescents with inflammatory bowel disease J. Pediatr. Gastroenterol. Nutr. 45 2007 3 14
133. D.C. Baumgart, and S.R. Carding Inflammatory bowel disease: cause and immunobiology Lancet 369 2007 1627 1640
134. C. Xiao, and S. Ghosh NF-kappaB, an evolutionarily conserved mediator of immune and inflammatory responses Adv. Exp. Med. Biol. 560 2005 41 45
135. C. Braconi, N. Huang, and T. Patel MicroRNA-dependent regulation of DNA methyltransferase-1 and tumor suppressor gene expression by interleukin-6 in human malignant cholangiocytes Hepatology 51 2010 881 890
136. E. Foran, M.M. Garrity-Park, C. Mureau, J. Newell, T.C. Smyrk, P.J. Limburg, and L.J. Egan Upregulation of DNA methyltransferase-mediated gene silencing, anchorage-independent growth, and migration of colon cancer cells by interleukin-6 Mol. Cancer Res. 8 2010 471 481
137. R. Dammann, U. Schagdarsurengin, L. Liu, N. Otto, O. Gimm, H. Dralle, B.O. Boehm, G.P. Pfeifer, and C. Hoang-Vu Frequent RASSF1A promoter hypermethylation and K-ras mutations in pancreatic carcinoma Oncogene 22 2003 3806 3812
138. E. Dimitriadis, T. Kalogeropoulos, S. Velaeti, S. Sotiriou, E. Vassiliou, L. Fasoulis, V. Klapsas, M. Synesiou, A. Apostolaki, T. Trangas, and N. Pandis Study of genetic and epigenetic alterations in urine samples as diagnostic markers for prostate cancer Anticancer Res. 33 2013 191 197
139. H. Ahmed Promoter methylation in prostate cancer and its application for the early detection of prostate cancer using serum and urine samples Biomarkers Cancer 2010 2010 17 33
140. J. Yu, T. Zhu, Z. Wang, H. Zhang, Z. Qian, H. Xu, B. Gao, W. Wang, L. Gu, J. Meng, J. Wang, X. Feng, Y. Li, X. Yao, and J. Zhu A novel set of DNA methylation markers in urine sediments for sensitive/specific detection of bladder cancer Clin. Cancer Res. 13 2007 7296 7304
141. R. Krassenstein, E. Sauter, E. Dulaimi, C. Battagli, H. Ehya, A. Klein-Szanto, and P. Cairns Detection of breast cancer in nipple aspirate fluid by CpG island hypermethylation Clin. Cancer Res. 10 2004 28 32
142. A.T. Martins, P. Monteiro, J. Ramalho-Carvalho, V.L. Costa, M. Dinis-Ribeiro, C. Leal, R. Henrique, and C. Jeronimo High RASSF1A promoter methylation levels are predictive of poor prognosis in fine-needle aspirate washings of breast cancer lesions Breast Cancer Res. Treat. 129 2011 1 9
143. S. Honorio, A. Agathanggelou, M. Schuermann, W. Pankow, P. Viacava, E.R. Maher, and F. Latif Detection of RASSF1A aberrant promoter hypermethylation in sputum from chronic smokers and ductal carcinoma in situ from breast cancer patients Oncogene 22 2003 147 150
144. P. Yi, N. Yin, Y. Zheng, H. Jiang, X. Yu, Y. Yan, Q. Liu, F. Xiao, and L. Li Elevated plasma levels of hypermethylated RASSF1A Gene sequences in pregnant women with intrahepatic cholestasis Cell Biochem. Biophys. 67 2013 977 981
145. U. Schagdarsurengin, A.M. Richter, J. Hornung, C. Lange, K. Steinmann,
146. D. Guerrero-Setas, N. Perez-Janices, L. Blanco-Fernandez, A. Ojer, K. Cambra, M. Berdasco, M. Esteller, S. Maria-Ruiz, N. Torrea, and R. Guarch RASSF2 hypermethylation is present and related to shorter survival in squamous cervical cancer Mod. Pathol. 26 2013 1111 1122
147. H. Guo, H. Liu, J. Wei, Y. Li, H. Yu, X. Guan, E.W. Li, G. Li, E.M. Sturgis, Q. Wei, and Z. Liu Functional single nucleotide polymorphisms of the RASSF3 gene and susceptibility to squamous cell carcinoma of the head and neck Eur. J. Cancer 3 2013 e3997
148. S. Kuznetsov, and A.V. Khokhlatchev The growth and tumor suppressors NORE1A and RASSF1A are targets for calpain-mediated proteolysis PLoS One 3 2008 e3997
149. Y. Sanada, T. Kumoto, H. Suehiro, F. Nishimura, N. Kato, Y. Hata, A. Sorisky, and N. Yanaka RASSF6 expression in adipocytes is down-regulated by interaction with macrophages PLoS One 8 2013 e61931
150. P. Helmbold, A.M. Richter, S. Walesch, A. Skorokhod, W. Marsch, A. Enk, and R.H. Dammann RASSF10 promoter hypermethylation is frequent in malignant melanoma of the skin but uncommon in nevus cell nevi J. Invest. Dermatol. 132 2012 687 694
151. H. Zhang, J. He, J. Li, D. Tian, L. Gu, and M. Zhou Methylation of RASSF1A gene promoter is regulated by p53 and DAXX FASEB J. 27 2012 232 242
152. R.K. Palakurthy, N. Wajapeyee, M.K. Santra, C. Gazin, L. Lin, S. Gobeil, and M.R. Green Epigenetic silencing of the RASSF1A tumor suppressor gene through HOXB3-mediated induction of DNMT3B expression Mol. Cell 36 2009 219 230
153. Q. Li, F. Zhu, and P. Chen MiR-7 and miR-218 epigenetically control tumor suppressor genes RASSF1A and Claudin-6 by targeting HoxB3 in breast cancer Biochem. Biophys. Res. Commun. 424 2012 28 33
154. F.C. Beckedorff, A.C. Ayupe, R. Crocci-Souza, M.S. Amaral, H.I. Nakaya, D.T. Soltys, C.F. Menck, E.M. Reis, and S. Verjovski-Almeida The intronic long noncoding RNA ANRASSF1 recruits PRC2 to the RASSF1A promoter, reducing the expression of RASSF1A and increasing cell proliferation PLoS Genet. 9 2013 e1003705
155. M. Gordon, M. El-Kalla, and S. Baksh RASSF1 polymorphisms in cancer Mol. Biol. Int. 2012 2012 365213
156. R.C. Friedman, K.K. Farh, C.B. Burge, and D.P. Bartel Most mammalian mRNAs are conserved targets of microRNAs Genome Res. 19 2009 92 105
157. A. Esquela-Kerscher, and F.J. Slack Oncomirs - microRNAs with a role in cancer Nat. Rev. Cancer 6 2006 259 269
158. H. Osada, and T. Takahashi MicroRNAs in biological processes and carcinogenesis Carcinogenesis 28 2007 2 12
159. A. Kozomara, and S. Griffiths-Jones MiRBase: integrating microRNA annotation and deep-sequencing data Nucleic Acids Res. 39 2011 D152 D157
160. L. Yang, Z. Ma, D. Wang, W. Zhao, L. Chen, and G. Wang MicroRNA-602 regulating tumor suppressive gene RASSF1A is overexpressed in hepatitis B virus-infected liver and hepatocellular carcinoma Cancer Biol. Ther. 9 2010 803 808
161. H. Wang, J. Wu, X. Meng, X. Ying, Y. Zuo, R. Liu, Z. Pan, T. Kang, and W. Huang MicroRNA-342 inhibits colorectal cancer cell proliferation and invasion by directly targeting DNA methyltransferase 1 Carcinogenesis 32 2010 1033 1042
162. Y. Chen, J. Luo, R. Tian, H. Sun, and S. Zou MiR-373 negatively regulates methyl-CpG-binding domain protein 2 (MBD2) in hilar cholangiocarcinoma Dig. Dis. Sci. 56 2011 1693 1701
163. Y. Chen, W. Gao, J. Luo, R. Tian, H. Sun, and S. Zou Methyl-CpG binding protein MBD2 is implicated in methylation-mediated suppression of miR-373 in hilar cholangiocarcinoma Oncol. Rep. 25 2011 443 451
164. F. Sato, S. Tsuchiya, S.J. Meltzer, and K. Shimizu MicroRNAs and epigenetics FEBS J. 278 2011 1598 1609
165. R. Rong, L.Y. Jiang, M.S. Sheikh, and Y. Huang Mitotic kinase Aurora-A phosphorylates RASSF1A and modulates RASSF1A-mediated microtubule interaction and M-phase cell cycle regulation Oncogene 26 2007 7700 7708
166. M.S. Song, S.J. Song, S.J. Kim, K. Nakayama, K.I. Nakayama, and D.S. Lim Skp2 regulates the antiproliferative function of the tumor suppressor RASSF1A via ubiquitin-mediated degradation at the G1-S transition Oncogene 27 2008 3176 3185
167. S.K. Verma, T.S. Ganesan, and P.J. Parker The tumour suppressor RASSF1A is a novel substrate of PKC FEBS Lett. 582 2008 2270 2276
168. A. Vichalkovski, E. Gresko, H. Cornils, A. Hergovich, D. Schmitz, and B.A. Hemmings NDR kinase is activated by RASSF1A/MST1 in response to Fas receptor stimulation and promotes apoptosis Curr. Biol. 18 2008 1889 1895
169. S.J. Song, S.J. Kim, M.S. Song, and D.S. Lim Aurora B-mediated phosphorylation of RASSF1A maintains proper cytokinesis by recruiting Syntaxin16 to the midzone and midbody Cancer Res. 69 2009 8540 8544
170. L. Jiang, R. Rong, M.S. Sheikh, and Y. Huang Mitotic Arrest by Tumor Suppressor RASSF1A is Regulated via Chk1 Phosphorylation Mol. Cancer Res. 12 1 2014 119 129
171. L.K. Teixeira, and S.I. Reed Ubiquitin ligases and cell cycle control Annu. Rev. Biochem. 82 2013 387 414
172. L. Jiang, R. Rong, M.S. Sheikh, and Y. Huang Cullin-4A.DNA damage-binding protein 1 E3 ligase complex targets tumor suppressor RASSF1A for degradation during mitosis J. Biol. Chem. 286 2010 6971 6978
173. D.F. Calvisi, S. Ladu, F. Pinna, M. Frau, M.L. Tomasi, M. Sini, M.M. Simile, P. Bonelli, M.R. Muroni, M.A. Seddaiu, D.S. Lim, F. Feo, and R.M. Pascale SKP2 and CKS1 promote degradation of cell cycle regulators and are associated with hepatocellular carcinoma prognosis Gastroenterology 137 2009 (1816-26 e1-10)
174. Y. Tian, Y. Hou, X. Zhou, H. Cheng, and R. Zhou Tumor suppressor RASSF1A promoter: p53 binding and methylation PLoS One 6 2011 e17017
175. M.D. Vos, A. Dallol, K. Eckfeld, N.P. Allen, H. Donninger, L.B. Hesson, D. Calvisi, F. Latif, and G.J. Clark The RASSF1A tumor suppressor activates Bax via MOAP-1 J. Biol. Chem. 281 8 2006 4557 4563
176. A. Dallol, W. Kolch, and F. Latif When RASSF1A RAN into tumor suppression: Ran GTPase is a RASSF1A effector involved in controlling microtubule organization Cell Cycle 8 2009 3796 3797
177. J.J. Chan, D. Flatters, F. Rodrigues-Lima, J. Yan, K. Thalassinos, and M. Katan Comparative analysis of interactions of RASSF1-10 Adv. Biol. Regul. 53 2013 190 201
178. S.K. Verma, T.S. Ganesan, U. Kishore, and P.J. Parker The tumor suppressor RASSF1A is a novel effector of small G protein Rap1A Protein Cell 2 2011 237 249
179. D.F. Calvisi, S. Ladu, A. Gorden, M. Farina, E.A. Conner, J.S. Lee, V.M. Factor, and S.S. Thorgeirsson Ubiquitous activation of Ras and Jak/Stat pathways in human HCC Gastroenterology 130 2006 1117 1128
180. A. Lorenzato, C. Martino, N. Dani, Y. Oligschlager, A.M. Ferrero, N. Biglia, R. Calogero, M. Olivero, and M.F. Di Renzo The cellular apoptosis susceptibility CAS/CSE1L gene protects ovarian cancer cells from death by suppressing RASSF1C FASEB J. 26 2012 2446 2456
181. J. Clark, J. Freeman, and H. Donninger Loss of RASSF2 Enhances Tumorigencity of Lung Cancer Cells and Confers Resistance to Chemotherapy Mol. Biol. Int. 2012 2012 705948
182. C. Bee, A. Moshnikova, C.D. Mellor, J.E. Molloy, Y. Koryakina, B. Stieglitz, A. Khokhlatchev, and C. Herrmann Growth and tumor suppressor NORE1A is a regulatory node between Ras signaling and microtubule nucleation J. Biol. Chem. 285 2010 16258 16266
183. D. Lee, S.J. Park, K.S. Sung, J. Park, S.B. Lee, S.Y. Park, H.J. Lee, J.W. Ahn, S.J. Choi, S.G. Lee, S.H. Kim, D.H. Kim, J. Kim, Y. Kim, and C.Y. Choi Mdm2 associates with Ras effector NORE1 to induce the degradation of oncoprotein HIPK1 EMBO Rep. 13 2012 163 169
184. K. Ishiguro, J. Avruch, A. Landry, S. Qin, T. Ando, H. Goto, and R. Xavier Nore1B regulates TCR signaling via Ras and Carma1 Cell. Signal. 18 2006 1647 1654
185. R. Suryaraja, M. Anitha, K. Anbarasu, G. Kumari, and S. Mahalingam The E3 ubiquitin ligase Itch regulates tumor suppressor protein RASSF5/NORE1 stability in an acetylation-dependent manner Cell Death Dis. 4 2013 e565
186. M. Miertzschke, P. Stanley, T.D. Bunney, F. Rodrigues-Lima, N. Hogg, and M. Katan Characterization of interactions of adapter protein RAPL/Nore1B with RAP GTPases and their role in T cell migration J. Biol. Chem. 282 2007 30629 30642
187. J.H. Kim, W.S. Kim, and C. Park Epstein-Barr virus latent membrane protein 1 increases genomic instability through Egr-1-mediated up-regulation of activation-induced cytidine deaminase in B-cell lymphoma Leukemia Lymphoma 54 2013 2035 2040
188. P. Rodriguez-Viciana, C. Sabatier, and F. McCormick Signaling specificity by Ras family GTPases is determined by the full spectrum of effectors they regulate Mol. Cell. Biol. 24 2004 4943 4954
189. Hill, V. K.; Underhill-Day, N.; Krex, D.; Robel, K.; Sangan, C. B.; Summersgill, H. R.; Morris, M.; Gentle, D.; Chalmers, A. D.; Maher, E. R. & Latif, F. (2010) Epigenetic inactivation of the RASSF10 candidate tumor suppressor gene is a frequent and an early event in gliomagenesis, Oncogene.
190. A.M. Richter, S.K. Walesch, P. Wurl, H. Taubert, and R.H. Dammann The tumor suppressor RASSF10 is upregulated upon contact inhibition and frequently epigenetically silenced in cancer Oncogenesis 1 2012 e18
191. T. Tsunoda, and T. Takagi Estimating transcription factor bindability on DNA Bioinformatics 15 1999 622 630