Epigenetic silencing of RASSF1A deregulates cytoskeleton and promotes malignant behavior of adrenocortical carcinoma

Molecular Cancer

Volumn 12, Issue 1, 2013, Pages

  Korah, Reju ^a   Healy, James M ^a   Kunstman, John W ^a   Fonseca, Annabelle L ^a   Ameri, Amir H ^a   Prasad, Manju L ^a   Carling, Tobias ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Adenoma; Adrenal cortex; Carcinoma; Cytoskeleton; Epigenetic silencing; Hypermethylation; RASSF1A

Indexed keywords

MESSENGER RNA; RAS ASSOCIATION DOMAIN FAMILY PROTEIN 1A; RESTRICTION ENDONUCLEASE;

ADRENAL CORTEX ADENOMA; ADRENAL CORTEX CARCINOMA; ADRENAL CORTEX CELL; ADRENAL CORTEX TUMOR; ADULT; ARTICLE; BASEMENT MEMBRANE; CANCER CELL CULTURE; CANCER GROWTH; CANCER RECURRENCE; CELL GROWTH; CELL MOTILITY; CELL SURVIVAL; CLINICAL ARTICLE; CPG ISLAND; CYTOSKELETON; DNA METHYLATION; EPIGENETIC REPRESSION; FEMALE; GENE EXPRESSION; GENE SILENCING; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; LOSS OF FUNCTION MUTATION; MALE; MICROTUBULE; PHENOTYPE; POLYMERASE CHAIN REACTION; PROMOTER REGION; PROTEIN EXPRESSION; STABLE EXPRESSION; TRANSIENT TRANSFECTION; TUMOR SUPPRESSOR GENE; WNT SIGNALING PATHWAY;

ADRENAL CORTEX NEOPLASMS; ADRENOCORTICAL CARCINOMA; ADULT; CELL LINE, TUMOR; CPG ISLANDS; CYTOSKELETON; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; HUMANS; MALE; MICROTUBULES; MIDDLE AGED; NEOPLASM STAGING; PHENOTYPE; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; TUMOR SUPPRESSOR PROTEINS;

EID: 84881069875     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-12-87     Document Type: Article

References (55)

1. Wajchenberg BL, Albergaria Pereira MA, Medonca BB, Latronico AC, Campos Carneiro P, Alves VA, et al. Adrenocortical carcinoma: clinical and laboratory observations. Cancer 2000, 88:711-36. 10.1002/(SICI)1097-0142(20000215)88:4<711::AID-CNCR1>3.0.CO;2-W, 10679640.
2. Lehmann T, Wrzesinski T. The molecular basis of adrenocortical cancer. Cancer Genet 2012, 205:131-7. 10.1016/j.cancergen.2012.02.009, 22559973.
3. Fassnacht M, Terzolo M, Allolio B, Baudin E, Haak H, Berruti A, et al. Combination chemotherapy in advanced adrenocortical carcinoma. N Engl J Med 2012, 366:2189-97. 10.1056/NEJMoa1200966, 22551107.
4. Berthon A, Martinez A, Bertherat J, Val P. Wnt/beta-catenin signalling in adrenal physiology and tumour development. Mol Cell Endocrinol 2012, 351:87-95. 10.1016/j.mce.2011.09.009, 21930188.
5. Dackiw AP, Lee JE, Gagel RF, Evans DB. Adrenal cortical carcinoma. World J Surg 2001, 25:914-26. 10.1007/s00268-001-0030-7, 11572033.
6. Ng L, Libertino JM. Adrenocortical carcinoma: diagnosis, evaluation and treatment. J Urol 2003, 169:5-11.
7. Ohgaki H, Kleihues P, Heitz PU. p53 mutations in sporadic adrenocortical tumors. Int j cancer J int du cancer 1993, 54:408-10.
8. Reincke M, Karl M, Travis WH, Mastorakos G, Allolio B, Linehan HM, et al. p53 mutations in human adrenocortical neoplasms: immunohistochemical and molecular studies. J clin endocrinol metab 1994, 78:790-4. 10.1210/jc.78.3.790, 8126158.
9. Wagner J, Portwine C, Rabin K, Leclerc JM, Narod SA, Malkin D. High frequency of germline p53 mutations in childhood adrenocortical cancer. J Natl Cancer Inst 1994, 86:1707-10. 10.1093/jnci/86.22.1707, 7966399.
10. Libe R, Groussin L, Tissier F, Elie C, Rene-Corail F, Fratticci A, et al. Somatic TP53 mutations are relatively rare among adrenocortical cancers with the frequent 17p13 loss of heterozygosity. Clin cancer res off j Am Assoc Cancer Res 2007, 13:844-50.
11. Soon PS, McDonald KL, Robinson BG, Sidhu SB. Molecular markers and the pathogenesis of adrenocortical cancer. Oncologist 2008, 13:548-61. 10.1634/theoncologist.2007-0243, 18515740.
12. Tissier F, Cavard C, Groussin L, Perlemoine K, Fumey G, Hagnere AM, et al. Mutations of beta-catenin in adrenocortical tumors: activation of the Wnt signaling pathway is a frequent event in both benign and malignant adrenocortical tumors. Cancer res 2005, 65:7622-7.
13. Bertherat J, Groussin L, Sandrini F, Matyakhina L, Bei T, Stergiopoulos S, et al. Molecular and functional analysis of PRKAR1A and its locus (17q22-24) in sporadic adrenocortical tumors: 17q losses, somatic mutations, and protein kinase A expression and activity. Cancer res 2003, 63:5308-19.
14. Heaton JH, Wood MA, Kim AC, Lima LO, Barlaskar FM, et al. Progression to adrenocortical tumorigenesis in mice and humans through insulin-like growth factor 2 and b-catenin. Am J Pathol 2012, 181(3):1017-33. 10.1016/j.ajpath.2012.05.026, 22800756.
15. Donninger H, Vos MD, Clark GJ. The RASSF1A tumor suppressor. J Cell Sci 2007, 120:3163-72. 10.1242/jcs.010389, 17878233.
16. Avruch J, Xavier R, Bardeesy N, Zhang XF, Praskova M, Zhou D, et al. Rassf family of tumor suppressor polypeptides. J Biol Chem 2009, 284:11001-5. 2670104, 19091744.
17. Fausti F, Di Agostino S, Sacconi A, Strano S, Blandino G. Hippo and rassf1a Pathways: A Growing Affair. Mol biol int 2012, 2012:307628. 3399428, 22830020.
18. Agathanggelou A, Cooper WN, Latif F. Role of the Ras-association domain family 1 tumor suppressor gene in human cancers. Cancer Res 2005, 65:3497-3508. 10.1158/0008-5472.CAN-04-4088, 15867337.
19. Richter AM, Pfeifer GP, Dammann RH. The RASSF proteins in cancer; from epigenetic silencing to functional characterization. Biochim Biophys Acta 2009, 1796:114-28.
20. Dumitrescu RG. Epigenetic markers of early tumor development. Methods Mol Biol 2012, 863:3-14. 10.1007/978-1-61779-612-8_1, 22359284.
21. Pylayeva-Gupta Y, Grabocka E, Bar-Sagi D. RAS oncogenes: weaving a tumorigenic web. Nature rev Cancer 2011, 11:761-74.
22. Song MS, Song SJ, Ayad NG, Chang JS, Lee JH, Hong HK, et al. The tumour suppressor RASSF1A regulates mitosis by inhibiting the APC-Cdc20 complex. Nat Cell Biol 2004, 6:129-37. 10.1038/ncb1091, 14743218.
23. Liu L, Tommasi S, Lee DH, Dammann R, Pfeifer GP. Control of microtubule stability by the RASSF1A tumor suppressor. Oncogene 2003, 22:8125-36. 10.1038/sj.onc.1206984, 14603253.
24. Dallol A, Agathanggelou A, Fenton SL, Ahmed-Choudhury J, Hesson L, Vos MD, et al. RASSF1A interacts with microtubule-associated proteins and modulates microtubule dynamics. Cancer Res 2004, 64:4112-6. 10.1158/0008-5472.CAN-04-0267, 15205320.
25. Vos MD, Ellis CA, Bell A, Birrer MJ, Clark GJ. Ras uses the novel tumor suppressor RASSF1 as an effector to mediate apoptosis. J Biol Chem 2000, 275:35669-72. 10.1074/jbc.C000463200, 10998413.
26. Fernandes MS, Carneiro F, Oliveira C, Seruca R. Colorectal cancer and RASSF family-A special emphasis on RASSF1A. Int J Cancer 2012, 132(2):251-8.
27. Baksh S, Tommasi S, Fenton S, Yu VC, Martins LM, Pfeifer GP, et al. The tumor suppressor RASSF1A and MAP-1 link death receptor signaling to Bax conformational change and cell death. Mol Cell 2005, 18:637-50. 10.1016/j.molcel.2005.05.010, 15949439.
28. Dallol A, Agathanggelou A, Tommasi S, Pfeifer GP, Maher ER, Latif F. Involvement of the RASSF1A tumor suppressor gene in controlling cell migration. Cancer Res 2005, 65:7653-9.
29. Burbee DG, Forgacs E, Zochbauer-Muller S, Shivakumar L, Fong K, Gao B, et al. Epigenetic inactivation of RASSF1A in lung and breast cancers and malignant phenotype suppression. J Natl Cancer Inst 2001, 93:691-9. 10.1093/jnci/93.9.691, 11333291.
30. Tommasi S, Dammann R, Zhang Z, Wang Y, Liu L, Tsark WM, et al. Tumor susceptibility of Rassf1a knockout mice. Cancer Res 2005, 65:92-8.
31. Schagdarsurengin U, Gimm O, Hoang-Vu C, Dralle H, Pfeifer GP, Dammann R. Frequent epigenetic silencing of the CpG island promoter of RASSF1A in thyroid carcinoma. Cancer Res 2002, 62:3698-701.
32. Xing M, Cohen Y, Mambo E, Tallini G, Udelsman R, Ladenson PW, et al. Early occurrence of RASSF1A hypermethylation and its mutual exclusion with BRAF mutation in thyroid tumorigenesis. Cancer Res 2004, 64:1664-8. 10.1158/0008-5472.CAN-03-3242, 14996725.
33. Lee SJ, Lee MH, Kim DW, Lee S, Huang SM, Ryu MJ, et al. Cross-Regulation between Oncogenic BRAF(V600E) Kinase and the MST1 Pathway in Papillary Thyroid Carcinoma. Plos One 2011, 6(1):e16180. 10.1371/journal.pone.0016180, 3020965, 21249150.
34. Catalano MG, Fortunati N, Boccuzzi G. Epigenetics modifications and therapeutic prospects in human thyroid cancer. Front Endocrinol (Lausanne) 2012, 3:40.
35. Fonseca AL, Kugelberg J, Starker LF, Scholl U, Choi M, Hellman P, et al. Comprehensive DNA methylation analysis of benign and malignant adrenocortical tumors. Genes Chromosomes Cancer 2012, 51:949-60. 10.1002/gcc.21978, 22733721.
36. Jain M, Rechache N, Kebebew E. Molecular markers of adrenocortical tumors. J Surg Oncol 2012, 106:549-56. 10.1002/jso.23119, 22504887.
37. Rechache NS, Wang Y, Stevenson HS, Killian JK, Edelman DC, Merino M, et al. DNA methylation profiling identifies global methylation differences and markers of adrenocortical tumors. J Clin Endocrinol Metab 2012, 97:E1004-13. 10.1210/jc.2011-3298, 3387424, 22472567.
38. Barreau O, Assie G, Wilmot Roussel H, Ragazzon B, Baudry C, Perlemoine K, et al. Identification of a CpG Island Methylator Phenotype in Adrenocortical Carcinomas. J Clin Endocrinol Metab 2013, 98(1):E174-E184. 10.1210/jc.2012-2993, 23093492.
39. Gao ZH, Suppola S, Liu J, Heikkila P, Janne J, Voutilainen R. Association of H19 promoter methylation with the expression of H19 and IGF-II genes in adrenocortical tumors. J Clin Endocrinol Metab 2002, 87:1170-6. 10.1210/jc.87.3.1170, 11889182.
40. Byun DS, Lee MG, Chae KS, Ryu BG, Chi SG. Frequent epigenetic inactivation of RASSF1A by aberrant promoter hypermethylation in human gastric adenocarcinoma. Cancer Res 2001, 61:7034-8.
41. Maruyama R, Toyooka S, Toyooka KO, Virmani AK, Zochbauer-Muller S, Farinas AJ, et al. Aberrant promoter methylation profile of prostate cancers and its relationship to clinicopathological features. Clin Cancer Res 2002, 8:514-9.
42. Pfeifer GP, Yoon JH, Liu L, Tommasi S, Wilczynski SP, Dammann R. Methylation of the RASSF1A gene in human cancers. Biol Chem 2002, 383:907-14.
43. Yu J, Ni M, Xu J, Zhang HY, Gao BM, Gu JR, et al. Methylation profiling of twenty promoter-CpG islands of genes which may contribute to hepatocellular carcinogenesis. Bmc Cancer 2002, 2. doi:10.1186/1471-2407-2-29.
44. van Engeland M, Roemen GM, Brink M, Pachen MM, Weijenberg MP, de Bruine AP, et al. K-ras mutations and RASSF1A promoter methylation in colorectal cancer. Oncogene 2002, 21:3792-5. 10.1038/sj.onc.1205466, 12032847.
45. Yu MY, Tong JHM, Chan PKS, Lee TL, Chan MWY, Chan AWH, et al. Hypermethylation of the tumor suppressor gene Rassfia and frequent concomitant loss of heterozygosity at 3p21 in cervical cancers. Int J Cancer 2003, 105:204-9. 10.1002/ijc.11051, 12673680.
46. Astuti D, Agathanggelou A, Honorio S, Dallol A, Martinsson T, Kogner P, et al. RASSF1A promoter region CpG island hypermethylation in phaeochromocytomas and neuroblastoma tumours. Oncogene 2001, 20:7573-7. 10.1038/sj.onc.1204968, 11709729.
47. Malpeli G, Amato E, Dandrea M, Fumagalli C, Debattisti V, Boninsegna L, et al. Methylation-associated down-regulation of RASSF1A and up-regulation of RASSF1C in pancreatic endocrine tumors. BMC Cancer 2011, 11:351. 10.1186/1471-2407-11-351, 3170651, 21838870.
48. Gao BN, Xie XJ, Huang CX, Shames DS, Chen TTL, Lewis CM, et al. RASSF1A polymorphism A133S is associated with early onset breast cancer in BRCA1/2 mutation carriers. Cancer Res 2008, 68:22-5. 10.1158/0008-5472.CAN-07-5183, 2833356, 18172292.
49. Geli J, Kiss N, Lanner F, Foukakis T, Natalishvili N, Larsson O, et al. The Ras effectors NORE1A and RASSF1A are frequently inactivated in pheochromocytoma and abdominal paraganglioma. Endocr Relat Cancer 2007, 14:125-34. 10.1677/ERC-06-0031, 17395981.
50. Geli J, Kiss N, Karimi M, Lee JJ, Backdahl M, Ekstrom TJ, et al. Global and regional CpG methylation in pheochromocytomas and abdominal paragangliomas: association to malignant behavior. Clin Cancer Res 2008, 14:2551-9. 10.1158/1078-0432.CCR-07-1867, 18451216.
51. Rong R, Jin W, Zhang J, Sheikh MS, Huang Y. Tumor suppressor RASSF1A is a microtubule-binding protein that stabilizes microtubules and induces G2/M arrest. Oncogene 2004, 23:8216-30. 10.1038/sj.onc.1207901, 15378022.
52. Vos MD, Martinez A, Elam C, Dallol A, Taylor BJ, Latif F, et al. A role for the RASSF1A tumor suppressor in the regulation of tubulin polymerization and genomic stability. Cancer Res 2004, 64:4244-50. 10.1158/0008-5472.CAN-04-0339, 15205337.
53. El-Kalla M, Onyskiw C, Baksh S. Functional importance of RASSF1A microtubule localization and polymorphisms. Oncogene 2010, 29:5729-40. 10.1038/onc.2010.316, 20697344.
54. Agathanggelou A, Honorio S, Macartney DP, Martinez A, Dallol A, Rader J, et al. Methylation associated inactivation of RASSF1A from region 3p21.3 in lung, breast and ovarian tumours. Oncogene 2001, 20:1509-18. 10.1038/sj.onc.1204175, 11313894.
55. Korah R, Choi L, Barrios J, Wieder R. Expression of FGF-2 alters focal adhesion dynamics in migration-restricted MDA-MB-231 breast cancer cells. Breast Cancer Res Treat 2004, 88(1):17-28. 10.1007/s10459-004-6006-2, 15538042.