The Tumor Suppressor Gene, RASSF1A, Is Essential for Protection against Inflammation -Induced Injury

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Gordon, Marilyn ^a   El Kalla, Mohamed ^a   Zhao, Yuewen ^a,e   Fiteih, Yahya ^a   Law, Jennifer ^a   Volodko, Natalia ^a   Mohamed, Anwar ^a   El Kadi, Ayman O S ^a   Liu, Lei ^a   Odenbach, Jeff ^a   Thiesen, Aducio ^a   Onyskiw, Christina ^a   Ghazaleh, Haya Abu ^a,f   Park, Jikyoung ^b,g   Lee, Sean Bong ^b   Yu, Victor C ^c   Fernandez Patron, Carlos ^a   Alexander, R Todd ^a   Wine, Eytan ^a,d   Baksh, Shairaz ^a,d  

^a UNIVERSITY OF ALBERTA   (Canada)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d CROSS CANCER INSTITUTE   (Canada)

^e QUEEN S UNIVERSITY   (Canada)

^f AMERICAN UNIVERSITY OF THE MIDDLE EAST   (Kuwait)

^g Seegene Institute of Life Sciences   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN BAX; PROTEIN P53; PROTEIN P73; PROTEIN YAP; RAS ASSOCIATION DOMAIN FAMILY PROTEIN 1A; TOLL LIKE RECEPTOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; ABELSON KINASE; BAX PROTEIN, MOUSE; BENZAMIDE DERIVATIVE; DEXTRAN SULFATE; DNA BINDING PROTEIN; IMATINIB; NUCLEAR PROTEIN; PHOSPHOPROTEIN; PIPERAZINE DERIVATIVE; PYRIMIDINE DERIVATIVE; RASSF1 PROTEIN, MOUSE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TUMOR SUPPRESSOR PROTEIN; TUMOR SUPPRESSOR PROTEIN P73; YAP PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BAX GENE; CELL DAMAGE; CELL DEATH; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENTERITIS; GENE FUNCTION; GENETIC ASSOCIATION; HOMEOSTASIS; INTESTINE EPITHELIUM CELL; INTESTINE MUCOSA PERMEABILITY; MOUSE; NONHUMAN; PROTEIN PHOSPHORYLATION; RASSF1A GENE; TUMOR SUPPRESSOR GENE; UPREGULATION; ANIMAL; CHEMICALLY INDUCED; COLITIS, ULCERATIVE; COLON; DEFICIENCY; DRUG EFFECTS; EPITHELIUM CELL; GENE EXPRESSION REGULATION; GENETICS; INFLAMMATION; INTESTINE MUCOSA; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BENZAMIDES; CELL PROLIFERATION; COLITIS, ULCERATIVE; COLON; DEXTRAN SULFATE; DNA-BINDING PROTEINS; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; IMATINIB MESYLATE; INFLAMMATION; INTESTINAL MUCOSA; MICE; MICE, KNOCKOUT; NF-KAPPA B; NUCLEAR PROTEINS; PHOSPHOPROTEINS; PIPERAZINES; PROTO-ONCOGENE PROTEINS C-ABL; PYRIMIDINES; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS;

EID: 84885790623     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0075483     Document Type: Article

References (77)

1. Gordon M, Baksh S, (2010) RASSF1A: Not a prototypical Ras effector. Small Gtpases 2: 148-157.
2. Foley CJ, Freedman H, Choo SL, Onyskiw C, Fu NY, et al. (2008) Dynamics of RASSF1A/MOAP-1 association with death receptors. Mol Cell Biol 28: 4520-4535.
3. Park J, Kang SI, Lee SY, Zhang XF, Kim MS, et al. (2010) Tumor suppressor Ras-association domain family 5 (RASSF5/NORE1) mediates death receptor ligand-induced apoptosis. J Biol Chem 285: 35029-35038.
4. Tommasi S, Dammann R, Zhang Z, Wang Y, Liu L, et al. (2005) Tumor susceptibility of Rassf1a knockout mice. Cancer Res 65: 92-98.
5. van der Weyden L, Tachibana KK, Gonzalez MA, Adams DJ, Ng BL, et al. (2005) The RASSF1A isoform of RASSF1 promotes microtubule stability and suppresses tumorigenesis. Mol Cell Biol 25: 8356-8367.
6. Tommasi S, Besaratinia A, Wilczynski SP, Pfeifer GP, (2010) Loss of Rassf1a enhances p53-mediated tumor predisposition and accelerates progression to aneuploidy. Oncogene 30: 690-700.
7. Al-Sohaily S, Biankin A, Leong R, Kohonen-Corish M, Warusavitarne J, (2012) Molecular pathways in colorectal cancer. J Gastroenterol Hepatol 27: 1423-1431.
8. Stamos JL, Weis WI (2012) The beta-Catenin Destruction Complex. Cold Spring Harb Perspect Biol 5.
9. Valenta T, Hausmann G, Basler K, (2012) The many faces and functions of beta-catenin. Embo J 31: 2714-2736.
10. March HN, Rust AG, Wright NA, ten Hoeve J, de Ridder J, et al. (2012) Insertional mutagenesis identifies multiple networks of cooperating genes driving intestinal tumorigenesis. Nat Genet 43: 1202-1209.
11. van der Weyden L, Arends MJ, Dovey OM, Harrison HL, Lefebvre G, et al. (2008) Loss of Rassf1a cooperates with Apc(Min) to accelerate intestinal tumourigenesis. Oncogene 27: 4503-4508.
12. Fernandes MS, Carneiro F, Oliveira C, Seruca R, (2012) Colorectal cancer and RASSF family-A special emphasis on RASSF1A. Int J Cancer 132: 251-258.
13. Law J, Yu VC, Baksh S, (2012) Modulator of Apoptosis 1: A Highly Regulated RASSF1A-Interacting BH3-Like Protein. Mol Biol Int 2012: 536802.
14. Vos MD, Dallol A, Eckfeld K, Allen NP, Donninger H, et al. (2005) The RASSF1A tumor suppressor activates Bax via MOAP-1. J Biol Chem.
15. Wajant H, Scheurich P, (2010) TNFR1-induced activation of the classical NF-kappaB pathway. Febs J 278: 862-876.
16. Atreya I, Atreya R, Neurath MF, (2008) NF-kappaB in inflammatory bowel disease. J Intern Med 263: 591-596.
17. Rakoff-Nahoum S, Medzhitov R, (2009) Toll-like receptors and cancer. Nat Rev Cancer 9: 57-63.
18. Allen NP, Donninger H, Vos MD, Eckfeld K, Hesson L, et al. (2007) RASSF6 is a novel member of the RASSF family of tumor suppressors. Oncogene 26: 6203-6211.
19. Lock FE, Underhill-Day N, Dunwell T, Matallanas D, Cooper W, et al. (2010) The RASSF8 candidate tumor suppressor inhibits cell growth and regulates the Wnt and NF-kappaB signaling pathways. Oncogene 29: 4307-4316.
20. Song H, Kim H, Lee K, Lee DH, Kim TS, et al. (2012) Ablation of Rassf2 induces bone defects and subsequent haematopoietic anomalies in mice. Embo J 31: 1147-1159.
21. Estrabaud E, Lassot I, Blot G, Le Rouzic E, Tanchou V, et al. (2007) RASSF1C, an Isoform of the Tumor Suppressor RASSF1A, Promotes the Accumulation of {beta}-Catenin by Interacting with {beta}TrCP. Cancer Res 67: 1054-1061.
22. Abouzeid HE, Kassem AM, Abdel Wahab AH, El-mezayen HA, Sharad H, et al. (2010) Promoter hypermethylation of RASSF1A, MGMT, and HIC-1 genes in benign and malignant colorectal tumors. Tumour Biol 32: 845-852.
23. Braconi C, Huang N, Patel T, (2010) MicroRNA-dependent regulation of DNA methyltransferase-1 and tumor suppressor gene expression by interleukin-6 in human malignant cholangiocytes. Hepatology 51: 881-890.
24. Foran E, Garrity-Park MM, Mureau C, Newell J, Smyrk TC, et al. (2010) Upregulation of DNA methyltransferase-mediated gene silencing, anchorage-independent growth, and migration of colon cancer cells by interleukin-6. Mol Cancer Res 8: 471-481.
25. Madsen K, Cornish A, Soper P, McKaigney C, Jijon H, et al. (2001) Probiotic bacteria enhance murine and human intestinal epithelial barrier function. Gastroenterology 121: 580-591.
26. Baksh S, Widlund HR, Frazer-Abel AA, Du J, Fosmire S, et al. (2002) NFATc2-mediated repression of cyclin-dependent kinase 4 expression. Mol Cell 10: 1071-1081.
27. Xiao H, Gulen MF, Qin J, Yao J, Bulek K, et al. (2007) The Toll-interleukin-1 receptor member SIGIRR regulates colonic epithelial homeostasis, inflammation, and tumorigenesis. Immunity 26: 461-475.
28. Lee KK, Ohyama T, Yajima N, Tsubuki S, Yonehara S, (2001) MST, a physiological caspase substrate, highly sensitizes apoptosis both upstream and downstream of caspase activation. J Biol Chem 276: 19276-19285.
29. Stenson WF, (2010) Hyaluronic acid and intestinal inflammation. Curr Opin Gastroenterol 26: 85-87.
30. Zheng L, Riehl TE, Stenson WF, (2009) Regulation of colonic epithelial repair in mice by Toll-like receptors and hyaluronic acid. Gastroenterology 137: 2041-2051.
31. Udenigwe CC, Ramprasath VR, Aluko RE, Jones PJ, (2008) Potential of resveratrol in anticancer and anti-inflammatory therapy. Nutr Rev 66: 445-454.
32. Pringault E, Robine S, Louvard D, (1991) Structure of the human villin gene. Proc Natl Acad Sci U S A 88: 10811-10815.
33. Schulzke JD, Ploeger S, Amasheh M, Fromm A, Zeissig S, et al. (2009) Epithelial tight junctions in intestinal inflammation. Ann N Y Acad Sci 1165: 294-300.
34. Azer SA (2012) Overview of molecular pathways in inflammatory bowel disease associated with colorectal cancer development. Eur J Gastroenterol Hepatol.
35. Sturm A, Dignass AU, (2008) Epithelial restitution and wound healing in inflammatory bowel disease. World J Gastroenterol 14: 348-353.
36. Crosby LM, Waters CM, (2010) Epithelial repair mechanisms in the lung. Am J Physiol Lung Cell Mol Physiol 298: L715-731.
37. Halder G, Johnson RL, (2011) Hippo signaling: growth control and beyond. Development 138: 9-22.
38. Fausti F, Di Agostino S, Sacconi A, Strano S, Blandino G, (2012) Hippo and rassf1a Pathways: A Growing Affair. Mol Biol Int 2012: 307628.
39. Avruch J, Zhou D, Bardeesy N, (2012) YAP oncogene overexpression supercharges colon cancer proliferation. Cell Cycle 11: 1090-1096.
40. Guo C, Zhang X, Pfeifer GP, (2011) The tumor suppressor RASSF1A prevents dephosphorylation of the mammalian STE20-like kinases MST1 and MST2. J Biol Chem 286: 6253-6261.
41. Avruch J, Zhou D, Fitamant J, Bardeesy N, (2010) Mst1/2 signalling to Yap: gatekeeper for liver size and tumour development. Br J Cancer 104: 24-32.
42. Ren F, Wang B, Yue T, Yun EY, Ip YT, et al. (2010) Hippo signaling regulates Drosophila intestine stem cell proliferation through multiple pathways. Proc Natl Acad Sci U S A 107: 21064-21069.
43. Cai J, Zhang N, Zheng Y, de Wilde RF, Maitra A, et al. (2010) The Hippo signaling pathway restricts the oncogenic potential of an intestinal regeneration program. Genes Dev 24: 2383-2388.
44. Levy D, Adamovich Y, Reuven N, Shaul Y, (2007) The Yes-associated protein 1 stabilizes p73 by preventing Itch-mediated ubiquitination of p73. Cell Death Differ 14: 743-751.
45. Zhang H, Wu S, Xing D, (2010) YAP accelerates Abeta(25-35)-induced apoptosis through upregulation of Bax expression by interaction with p73. Apoptosis 16: 808-821.
46. Tamm C, Bower N, Anneren C, (2010) Regulation of mouse embryonic stem cell self-renewal by a Yes-YAP-TEAD2 signaling pathway downstream of LIF. J Cell Sci 124: 1136-1144.
47. Levy D, Adamovich Y, Reuven N, Shaul Y, (2008) Yap1 phosphorylation by c-Abl is a critical step in selective activation of proapoptotic genes in response to DNA damage. Mol Cell 29: 350-361.
48. Colgan SP, Taylor CT, (2010) Hypoxia: an alarm signal during intestinal inflammation. Nat Rev Gastroenterol Hepatol 7: 281-287.
49. Almenier HA, Al Menshawy HH, Maher MM, Al Gamal S, (2012) Oxidative stress and inflammatory bowel disease. Front Biosci (Elite Ed) 4: 1335-1344.
50. Deininger M, Buchdunger E, Druker BJ, (2005) The development of imatinib as a therapeutic agent for chronic myeloid leukemia. Blood 105: 2640-2653.
51. Barila D, Rufini A, Condo I, Ventura N, Dorey K, et al. (2003) Caspase-dependent cleavage of c-Abl contributes to apoptosis. Mol Cell Biol 23: 2790-2799.
52. Machuy N, Rajalingam K, Rudel T, (2004) Requirement of caspase-mediated cleavage of c-Abl during stress-induced apoptosis. Cell Death Differ 11: 290-300.
53. Goldberg Z, Vogt Sionov R, Berger M, Zwang Y, Perets R, et al. (2002) Tyrosine phosphorylation of Mdm2 by c-Abl: implications for p53 regulation. EMBO J 21: 3715-3727.
54. Saleh M, Trinchieri G, (2011) Innate immune mechanisms of colitis and colitis-associated colorectal cancer. Nat Rev Immunol 11: 9-20.
55. Van Limbergen J, Philpott D, Griffiths AM (2011) Genetic profiling in inflammatory bowel disease: from association to bedside. Gastroenterology 141: 1566-1571 e1561.
56. Sudol M, Bork P, Einbond A, Kastury K, Druck T, et al. (1995) Characterization of the mammalian YAP (Yes-associated protein) gene and its role in defining a novel protein module, the WW domain. J Biol Chem 270: 14733-14741.
57. Bertini E, Oka T, Sudol M, Strano S, Blandino G, (2009) YAP: at the crossroad between transformation and tumor suppression. Cell Cycle 8: 49-57.
58. Basu S, Totty NF, Irwin MS, Sudol M, Downward J, (2003) Akt phosphorylates the Yes-associated protein, YAP, to induce interaction with 14-3-3 and attenuation of p73-mediated apoptosis. Mol Cell 11: 11-23.
59. van der Weyden L, Papaspyropoulos A, Poulogiannis G, Rust AG, Rashid M, et al. (2012) Loss of rassf1a synergizes with deregulated runx2 signaling in tumorigenesis. Cancer Res 72: 3817-3827.
60. Hodge DR, Cho E, Copeland TD, Guszczynski T, Yang E, et al. (2007) IL-6 enhances the nuclear translocation of DNA cytosine-5-methyltransferase 1 (DNMT1) via phosphorylation of the nuclear localization sequence by the AKT kinase. Cancer Genomics Proteomics 4: 387-398.
61. Liao X, Siu MK, Chan KY, Wong ES, Ngan HY, et al. (2008) Hypermethylation of RAS effector related genes and DNA methyltransferase 1 expression in endometrial carcinogenesis. Int J Cancer 123: 296-302.
62. Deng X, Gao F, Flagg T, Anderson J, May WS, (2006) Bcl2's flexible loop domain regulates p53 binding and survival. Mol Cell Biol 26: 4421-4434.
63. Zhou D, Zhang Y, Wu H, Barry E, Yin Y, et al. (2011) Mst1 and Mst2 protein kinases restrain intestinal stem cell proliferation and colonic tumorigenesis by inhibition of Yes-associated protein (Yap) overabundance. Proc Natl Acad Sci U S A 108: E1312-1320.
64. Matallanas D, Romano D, Yee K, Meissl K, Kucerova L, et al. (2007) RASSF1A elicits apoptosis through an MST2 pathway directing proapoptotic transcription by the p73 tumor suppressor protein. Mol Cell 27: 962-975.
65. Schlegelmilch K, Mohseni M, Kirak O, Pruszak J, Rodriguez JR, et al. (2011) Yap1 acts downstream of alpha-catenin to control epidermal proliferation. Cell 144: 782-795.
66. Goretsky T, Dirisina R, Sinh P, Mittal N, Managlia E, et al. (2012) p53 mediates TNF-induced epithelial cell apoptosis in IBD. Am J Pathol 181: 1306-1315.
67. Dirisina R, Katzman RB, Goretsky T, Managlia E, Mittal N, et al. (2011) p53 and PUMA independently regulate apoptosis of intestinal epithelial cells in patients and mice with colitis. Gastroenterology 141: 1036-1045.
68. Kjellev S, (2009) The trefoil factor family- small peptides with multiple functionalities. Cell Mol Life Sci 66: 1350-1369.
69. Loncar MB, Al-azzeh ED, Sommer PS, Marinovic M, Schmehl K, et al. (2003) Tumour necrosis factor alpha and nuclear factor kappaB inhibit transcription of human TFF3 encoding a gastrointestinal healing peptide. Gut 52: 1297-1303.
70. Scrace SF, O'Neill E, (2012) RASSF Signalling and DNA Damage: Monitoring the Integrity of the Genome? Mol Biol Int 2012: 141732.
71. Biasi F, Leonarduzzi G, Oteiza PI, Poli G (2013) Inflammatory Bowel Disease: Mechanisms, Redox Considerations and Therapeutic Targets. Antioxid Redox Signal 2013.
72. Roessner A, Kuester D, Malfertheiner P, Schneider-Stock R, (2008) Oxidative stress in ulcerative colitis-associated carcinogenesis. Pathol Res Pract 204: 511-524.
73. Anwar A, Keating AK, Joung D, Sather S, Kim GK, et al. (2009) Mer tyrosine kinase (MerTK) promotes macrophage survival following exposure to oxidative stress. J Leukoc Biol 86: 73-79.
74. Lin Q, Wang J, Childress C, Yang W, (2012) The activation mechanism of ACK1 (activated Cdc42-associated tyrosine kinase 1). Biochem J 445: 255-264.
75. Mahajan NP, Liu Y, Majumder S, Warren MR, Parker CE, et al. (2007) Activated Cdc42-associated kinase Ack1 promotes prostate cancer progression via androgen receptor tyrosine phosphorylation. Proc Natl Acad Sci U S A 104: 8438-8443.
76. Baksh S, Burns K, Busaan J, Michalak M, (1992) Expression and purification of recombinant and native calreticulin. Protein Expr Purif 3: 322-331.
77. Zhang H, He J, Li J, Tian D, Gu L, et al. (2013) Methylation of RASSF1A gene promoter is regulated by p53 and DAXX. FASEB J 27: 232-242.