20
Views
17
CrossRef citations to date
0
Altmetric
Article

RASSF1A Inactivation Unleashes a Tumor Suppressor/Oncogene Cascade with Context-Dependent Consequences on Cell Cycle Progression

, , , , &
Pages 2350-2358 | Received 15 Nov 2013, Accepted 07 Apr 2014, Published online: 20 Mar 2023

REFERENCES

  • Donninger H, Vos MD, Clark GJ. 2007. The RASSF1A tumor suppressor. J. Cell Sci. 120:3163–3172. http://dx.doi.org/10.1242/jcs.010389.
  • Pan ZG, Kashuba VI, Liu XQ, Shao JY, Zhang RH, Jiang JH, Guo C, Zabarovsky E, Ernberg I, Zeng YX. 2005. High frequency somatic mutations in RASSF1A in nasopharyngeal carcinoma. Cancer Biol. Ther. 4:1116–1122. http://dx.doi.org/10.4161/cbt.4.10.2023.
  • Agathanggelou A, Cooper WN, Latif F. 2005. Role of the Ras-association domain family 1 tumor suppressor gene in human cancers. Cancer Res. 65:3497–3508. http://dx.doi.org/10.1158/0008-5472.CAN-04-4088.
  • Chan MW, Chan LW, Tang NL, Lo KW, Tong JH, Chan AW, Cheung HY, Wong WS, Chan PS, Lai FM, To KF. 2003. Frequent hypermethylation of promoter region of RASSF1A in tumor tissues and voided urine of urinary bladder cancer patients. Int. J. Cancer 104:611–616. http://dx.doi.org/10.1002/ijc.10971.
  • Tomizawa Y, Kohno T, Kondo H, Otsuka A, Nishioka M, Niki T, Yamada T, Maeshima A, Yoshimura K, Saito R, Minna JD, Yokota J. 2002. Clinicopathological significance of epigenetic inactivation of RASSF1A at 3p21.3 in stage I lung adenocarcinoma. Clin. Cancer Res. 8:2362–2368.
  • Yu MY, Tong JH, Chan PK, Lee TL, Chan MW, Chan AW, Lo KW, To KF. 2003. Hypermethylation of the tumor suppressor gene RASSFIA and frequent concomitant loss of heterozygosity at 3p21 in cervical cancers. Int. J. Cancer 105:204–209. http://dx.doi.org/10.1002/ijc.11051.
  • Burbee DG, Forgacs E, Zochbauer-Muller S, Shivakumar L, Fong K, Gao B, Randle D, Kondo M, Virmani A, Bader S, Sekido Y, Latif F, Milchgrub S, Toyooka S, Gazdar AF, Lerman MI, Zabarovsky E, White M, Minna JD. 2001. Epigenetic inactivation of RASSF1A in lung and breast cancers and malignant phenotype suppression. J. Natl. Cancer Inst. 93:691–699. http://dx.doi.org/10.1093/jnci/93.9.691.
  • Tommasi S, Dammann R, Zhang Z, Wang Y, Liu L, Tsark WM, Wilczynski SP, Li J, You M, Pfeifer GP. 2005. Tumor susceptibility of Rassf1a knockout mice. Cancer Res. 65:92–98.
  • van der Weyden L, Tachibana KK, Gonzalez MA, Adams DJ, Ng BL, Petty R, Venkitaraman AR, Arends MJ, Bradley A. 2005. The RASSF1A isoform of RASSF1 promotes microtubule stability and suppresses tumorigenesis. Mol. Cell. Biol. 25:8356–8367. http://dx.doi.org/10.1128/MCB.25.18.8356-8367.2005.
  • Dammann R, Li C, Yoon JH, Chin PL, Bates S, Pfeifer GP. 2000. Epigenetic inactivation of a RAS association domain family protein from the lung tumour suppressor locus 3p21.3. Nat. Genet. 25:315–319. http://dx.doi.org/10.1038/77083.
  • Dreijerink K, Braga E, Kuzmin I, Geil L, Duh FM, Angeloni D, Zbar B, Lerman MI, Stanbridge EJ, Minna JD, Protopopov A, Li J, Kashuba V, Klein G, Zabarovsky ER. 2001. The candidate tumor suppressor gene, RASSF1A, from human chromosome 3p21.3 is involved in kidney tumorigenesis. Proc. Natl. Acad. Sci. U. S. A. 98:7504–7509. http://dx.doi.org/10.1073/pnas.131216298.
  • Kuzmin I, Gillespie JW, Protopopov A, Geil L, Dreijerink K, Yang Y, Vocke CD, Duh FM, Zabarovsky E, Minna JD, Rhim JS, Emmert-Buck MR, Linehan WM, Lerman MI. 2002. The RASSF1A tumor suppressor gene is inactivated in prostate tumors and suppresses growth of prostate carcinoma cells. Cancer Res. 62:3498–3502.
  • Richter AM, Pfeifer GP, Dammann RH. 2009. The RASSF proteins in cancer; from epigenetic silencing to functional characterization. Biochim. Biophys. Acta 1796:114–128. http://dx.doi.org/10.1016/j.bbcan.2009.03.004.
  • Eskiocak U, Kim SB, Ly P, Roig AI, Biglione S, Komurov K, Cornelius C, Wright WE, White MA, Shay JW. 2011. Functional parsing of driver mutations in the colorectal cancer genome reveals numerous suppressors of anchorage-independent growth. Cancer Res. 71:4359–4365. http://dx.doi.org/10.1158/0008-5472.CAN-11-0794.
  • Shivakumar L, Minna J, Sakamaki T, Pestell R, White MA. 2002. The RASSF1A tumor suppressor blocks cell cycle progression and inhibits cyclin D1 accumulation. Mol. Cell. Biol. 22:4309–4318. http://dx.doi.org/10.1128/MCB.22.12.4309-4318.2002.
  • Estrabaud E, Lassot I, Blot G, Le Rouzic E, Tanchou V, Quemeneur E, Daviet L, Margottin-Goguet F, Benarous R. 2007. RASSF1C, an isoform of the tumor suppressor RASSF1A, promotes the accumulation of beta-catenin by interacting with betaTrCP. Cancer Res. 67:1054–1061. http://dx.doi.org/10.1158/0008-5472.CAN-06-2530.
  • Singh SK, Kagalwala MN, Parker-Thornburg J, Adams H, Majumder S. 2008. REST maintains self-renewal and pluripotency of embryonic stem cells. Nature 453:223–227. http://dx.doi.org/10.1038/nature06863.
  • Ou YH, Torres M, Ram R, Formstecher E, Roland C, Cheng T, Brekken R, Wurz R, Tasker A, Polverino T, Tan SL, White MA. 2011. TBK1 directly engages Akt/PKB survival signaling to support oncogenic transformation. Mol. Cell 41:458–470. http://dx.doi.org/10.1016/j.molcel.2011.01.019.
  • Whitehurst AW, Ram R, Shivakumar L, Gao B, Minna JD, White MA. 2008. The RASSF1A tumor suppressor restrains anaphase-promoting complex/cyclosome activity during the G1/S phase transition to promote cell cycle progression in human epithelial cells. Mol. Cell. Biol. 28:3190–3197. http://dx.doi.org/10.1128/MCB.02291-07.
  • Frescas D, Pagano M. 2008. Deregulated proteolysis by the F-box proteins SKP2 and beta-TrCP: tipping the scales of cancer. Nat. Rev. Cancer 8:438–449. http://dx.doi.org/10.1038/nrc2396.
  • Westbrook TF, Martin ES, Schlabach MR, Leng Y, Liang AC, Feng B, Zhao JJ, Roberts TM, Mandel G, Hannon GJ, Depinho RA, Chin L, Elledge SJ. 2005. A genetic screen for candidate tumor suppressors identifies REST. Cell 121:837–848. http://dx.doi.org/10.1016/j.cell.2005.03.033.
  • Westbrook TF, Hu G, Ang XL, Mulligan P, Pavlova NN, Liang A, Leng Y, Maehr R, Shi Y, Harper JW, Elledge SJ. 2008. SCFbeta-TRCP controls oncogenic transformation and neural differentiation through REST degradation. Nature 452:370–374. http://dx.doi.org/10.1038/nature06780.
  • Kreisler A, Strissel PL, Strick R, Neumann SB, Schumacher U, Becker CM. 2010. Regulation of the NRSF/REST gene by methylation and CREB affects the cellular phenotype of small-cell lung cancer. Oncogene 29:5828–5838. http://dx.doi.org/10.1038/onc.2010.321.
  • Calipel A, Abonnet V, Nicole O, Mascarelli F, Coupland SE, Damato B, Mouriaux F. 2011. Status of RASSF1A in uveal melanocytes and melanoma cells. Mol. Cancer Res. 9:1187–1198. http://dx.doi.org/10.1158/1541-7786.MCR-10-0437.
  • Hatley ME, Patrick DM, Garcia MR, Richardson JA, Bassel-Duby R, van Rooij E, Olson EN. 2010. Modulation of K-Ras-dependent lung tumorigenesis by microRNA-21. Cancer Cell 18:282–293. http://dx.doi.org/10.1016/j.ccr.2010.08.013.
  • O'Neill E, Rushworth L, Baccarini M, Kolch W. 2004. Role of the kinase MST2 in suppression of apoptosis by the proto-oncogene product Raf-1. Science 306:2267–2270. http://dx.doi.org/10.1126/science.1103233.
  • Kilili GK, Kyriakis JM. 2010. Mammalian Ste20-like kinase (Mst2) indirectly supports Raf-1/ERK pathway activity via maintenance of protein phosphatase-2A catalytic subunit levels and consequent suppression of inhibitory Raf-1 phosphorylation. J. Biol. Chem. 285:15076–15087. http://dx.doi.org/10.1074/jbc.M109.078915.
  • Matallanas D, Romano D, Yee K, Meissl K, Kucerova L, Piazzolla D, Baccarini M, Vass JK, Kolch W, O'Neill E. 2007. RASSF1A elicits apoptosis through an MST2 pathway directing proapoptotic transcription by the p73 tumor suppressor protein. Mol. Cell 27:962–975. http://dx.doi.org/10.1016/j.molcel.2007.08.008.
  • Becker KA, Ghule PN, Therrien JA, Lian JB, Stein JL, van Wijnen AJ, Stein GS. 2006. Self-renewal of human embryonic stem cells is supported by a shortened G1 cell cycle phase. J. Cell Physiol. 209:883–893. http://dx.doi.org/10.1002/jcp.20776.
  • Hong Y, Stambrook PJ. 2004. Restoration of an absent G1 arrest and protection from apoptosis in embryonic stem cells after ionizing radiation. Proc. Natl. Acad. Sci. U. S. A. 101:14443–14448. http://dx.doi.org/10.1073/pnas.0401346101.
  • Roig AI, Eskiocak U, Hight SK, Kim SB, Delgado O, Souza RF, Spechler SJ, Wright WE, Shay JW. 2010. Immortalized epithelial cells derived from human colon biopsies express stem cell markers and differentiate in vitro. Gastroenterology 138:1012–1021. http://dx.doi.org/10.1053/j.gastro.2009.11.052.
  • Peters I, Rehmet K, Wilke N, Kuczyk MA, Hennenlotter J, Eilers T, Machtens S, Jonas U, Serth J. 2007. RASSF1A promoter methylation and expression analysis in normal and neoplastic kidney indicates a role in early tumorigenesis. Mol. Cancer 6:49. http://dx.doi.org/10.1186/1476-4598-6-49.
  • Yeo W, Wong WL, Wong N, Law BK, Tse GM, Zhong S. 2005. High frequency of promoter hypermethylation of RASSF1A in tumorous and non-tumourous tissue of breast cancer. Pathology 37:125–130. http://dx.doi.org/10.1080/00313020500058623.
  • Honorio S, Agathanggelou A, Wernert N, Rothe M, Maher ER, Latif F. 2003. Frequent epigenetic inactivation of the RASSF1A tumour suppressor gene in testicular tumours and distinct methylation profiles of seminoma and nonseminoma testicular germ cell tumours. Oncogene 22:461–466. http://dx.doi.org/10.1038/sj.onc.1206119.
  • Vicent S, Chen R, Sayles LC, Lin C, Walker RG, Gillespie AK, Subramanian A, Hinkle G, Yang X, Saif S, Root DE, Huff V, Hahn WC, Sweet-Cordero EA. 2010. Wilms tumor 1 (WT1) regulates KRAS-driven oncogenesis and senescence in mouse and human models. J. Clin. Invest. 120:3940–3952. http://dx.doi.org/10.1172/JCI44165.
  • Young AP, Schlisio S, Minamishima YA, Zhang Q, Li L, Grisanzio C, Signoretti S, Kaelin WGJr. 2008. VHL loss actuates a HIF-independent senescence programme mediated by Rb and p400. Nat. Cell Biol. 10:361–369. http://dx.doi.org/10.1038/ncb1699.
  • Chen Z, Trotman LC, Shaffer D, Lin HK, Dotan ZA, Niki M, Koutcher JA, Scher HI, Ludwig T, Gerald W, Cordon-Cardo C, Pandolfi PP. 2005. Crucial role of p53-dependent cellular senescence in suppression of Pten-deficient tumorigenesis. Nature 436:725–730. http://dx.doi.org/10.1038/nature03918.
  • Lin HK, Chen Z, Wang G, Nardella C, Lee SW, Chan CH, Yang WL, Wang J, Egia A, Nakayama KI, Cordon-Cardo C, Teruya-Feldstein J, Pandolfi PP. 2010. Skp2 targeting suppresses tumorigenesis by Arf-p53-independent cellular senescence. Nature 464:374–379. http://dx.doi.org/10.1038/nature08815.
  • Pan X, Wang ZX, Wang R. 2010. MicroRNA-21: a novel therapeutic target in human cancer. Cancer Biol. Ther. 10:1224–1232. http://dx.doi.org/10.4161/cbt.10.12.14252.
  • Selcuklu SD, Donoghue MT, Spillane C. 2009. miR-21 as a key regulator of oncogenic processes. Biochem. Soc. Trans. 37:918–925. http://dx.doi.org/10.1042/BST0370918.
  • Wu L, Grigoryan AV, Li Y, Hao B, Pagano M, Cardozo TJ. 2012. Specific small molecule inhibitors of Skp2-mediated p27 degradation. Chem. Biol. 19:1515–1524. http://dx.doi.org/10.1016/j.chembiol.2012.09.015.
  • Chan CH, Morrow JK, Li CF, Gao Y, Jin G, Moten A, Stagg LJ, Ladbury JE, Cai Z, Xu D, Logothetis CJ, Hung MC, Zhang S, Lin HK. 2013. Pharmacological inactivation of Skp2 SCF ubiquitin ligase restricts cancer stem cell traits and cancer progression. Cell 154:556–568. http://dx.doi.org/10.1016/j.cell.2013.06.048.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.