The RON receptor tyrosine kinase promotes metastasis by triggering MBD4-dependent DNA methylation reprogramming

Cell Reports

Volumn 6, Issue 1, 2014, Pages 141-154

  Cunha, Stéphanie ^a   Lin, Yi Chun ^a   Goossen, ElizabethA ^a   DeVette, ChristaI ^a   Albertella, MarkR ^b   Thomson, Stuart ^b   Mulvihill, MarkJ ^b   Welm, AlanaL ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b OSI Astellas   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA GLYCOSYLTRANSFERASE; METHYL CPG BINDING PROTEIN; METHYL CPG BINDING PROTEIN 4; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN TYROSINE KINASE; RECEPTOR TYROSINE KINASE RON; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BASE MISPAIRING; BREAST METASTASIS; CANCER GROWTH; CATALYSIS; CONTROLLED STUDY; DNA METHYLATION; ENZYME ACTIVATION; EPIGENETICS; GENE EXPRESSION REGULATION; GENE LOCUS; GENETIC ASSOCIATION; LIGAND BINDING; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ANIMALS; BREAST NEOPLASMS; CARCINOGENESIS; DNA METHYLATION; ENDODEOXYRIBONUCLEASES; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HEPATOCYTE GROWTH FACTOR; HUMANS; MAMMARY NEOPLASMS, EXPERIMENTAL; MCF-7 CELLS; MICE; NEOPLASM METASTASIS; PHOSPHATIDYLINOSITOL 3-KINASES; PROGNOSIS; PROTO-ONCOGENE PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES;

EID: 84892531547     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.12.010     Document Type: Article

References (48)

1. Andersen A., Jones D.A. APC and DNA demethylation in cell fate specification and intestinal cancer. Adv. Exp. Med. Biol. 2013, 754:167-177.
2. Baylin S.B., Jones P.A. A decade of exploring the cancer epigenome - biological and translational implications. Nat. Rev. Cancer 2011, 11:726-734.
3. Ben-Porath I., Thomson M.W., Carey V.J., Ge R., Bell G.W., Regev A., Weinberg R.A. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat. Genet. 2008, 40:499-507.
4. Bert S.A., Robinson M.D., Strbenac D., Statham A.L., Song J.Z., Hulf T., Sutherland R.L., Coolen M.W., Stirzaker C., Clark S.J. Regional activation of the cancer genome by long-range epigenetic remodeling. Cancer Cell 2013, 23:9-22.
5. Bos P.D., Zhang X.H., Nadal C., Shu W., Gomis R.R., Nguyen D.X., Minn A.J., van de Vijver M.J., Gerald W.L., Foekens J.A., Massagué J. Genes that mediate breast cancer metastasis to the brain. Nature 2009, 459:1005-1009.
6. Chen S.S., Raval A., Johnson A.J., Hertlein E., Liu T.H., Jin V.X., Sherman M.H., Liu S.J., Dawson D.W., Williams K.E., et al. Epigenetic changes during disease progression in a murine model of human chronic lymphocytic leukemia. Proc. Natl. Acad. Sci. USA 2009, 106:13433-13438.
7. Chin K., DeVries S., Fridlyand J., Spellman P.T., Roydasgupta R., Kuo W.L., Lapuk A., Neve R.M., Qian Z., Ryder T., et al. Genomic and transcriptional aberrations linked to breast cancer pathophysiologies. Cancer Cell 2006, 10:529-541.
8. Cortellino S., Xu J., Sannai M., Moore R., Caretti E., Cigliano A., Le Coz M., Devarajan K., Wessels A., Soprano D., et al. Thymine DNA glycosylase is essential for active DNA demethylation by linked deamination-base excision repair. Cell 2011, 146:67-79.
9. Curtis C., Shah S.P., Chin S.F., Turashvili G., Rueda O.M., Dunning M.J., Speed D., Lynch A.G., Samarajiwa S., Yuan Y., et al. The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature 2012, 486:346-352. METABRIC Group.
10. DeRose Y.S., Wang G., Lin Y.C., Bernard P.S., Buys S.S., Ebbert M.T., Factor R., Matsen C., Milash B.A., Nelson E., et al. Tumor grafts derived from women with breast cancer authentically reflect tumor pathology, growth, metastasis and disease outcomes. Nat. Med. 2011, 17:1514-1520.
11. Desmedt C., Piette F., Loi S., Wang Y., Lallemand F., Haibe-Kains B., Viale G., Delorenzi M., Zhang Y., d'Assignies M.S., et al. Strong time dependence of the 76-gene prognostic signature for node-negative breast cancer patients in the TRANSBIG multicenter independent validation series. Clin. Cancer Res. 2007, 13:3207-3214. TRANSBIG Consortium.
12. Fang F., Turcan S., Rimner A., Kaufman A., Giri D., Morris L.G., Shen R., Seshan V., Mo Q., Heguy A., et al. Breast cancer methylomes establish an epigenomic foundation for metastasis. Sci. Transl. Med. 2011, 3:75ra25.
13. Feinberg A.P., Vogelstein B. Hypomethylation distinguishes genes of some human cancers from their normal counterparts. Nature 1983, 301:89-92.
14. Feng W., Orlandi R., Zhao N., Carcangiu M.L., Tagliabue E., Xu J., Bast R.C., Yu Y. Tumor suppressor genes are frequently methylated in lymph node metastases of breast cancers. BMC Cancer 2010, 10:378.
15. Gaudino G., Follenzi A., Naldini L., Collesi C., Santoro M., Gallo K.A., Godowski P.J., Comoglio P.M. RON is a heterodimeric tyrosine kinase receptor activated by the HGF homologue MSP. EMBO J. 1994, 13:3524-3532.
16. Han H.J., Russo J., Kohwi Y., Kohwi-Shigematsu T. SATB1 reprogrammes gene expression to promote breast tumour growth and metastasis. Nature 2008, 452:187-193.
17. Hansen K.D., Timp W., Bravo H.C., Sabunciyan S., Langmead B., McDonald O.G., Wen B., Wu H., Liu Y., Diep D., et al. Increased methylation variation in epigenetic domains across cancer types. Nat. Genet. 2011, 43:768-775.
18. He Y.F., Li B.Z., Li Z., Liu P., Wang Y., Tang Q., Ding J., Jia Y., Chen Z., Li L., et al. Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 2011, 333:1303-1307.
19. Heikkinen T., Greco D., Pelttari L.M., Tommiska J., Vahteristo P., Heikkilä P., Blomqvist C., Aittomäki K., Nevanlinna H. Variants on the promoter region of PTEN affect breast cancer progression and patient survival. Breast Cancer Res. 2011, 13:R130.
20. Hendrich B., Hardeland U., Ng H.H., Jiricny J., Bird A. The thymine glycosylase MBD4 can bind to the product of deamination at methylated CpG sites. Nature 1999, 401:301-304.
21. Hsu P.Y., Hsu H.K., Lan X., Juan L., Yan P.S., Labanowska J., Heerema N., Hsiao T.H., Chiu Y.C., Chen Y., et al. Amplification of distant estrogen response elements deregulates target genes associated with tamoxifen resistance in breast cancer. Cancer Cell 2013, 24:197-212.
22. Jones P.A. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat. Rev. Genet. 2012, 13:484-492.
23. Kang Y., Siegel P.M., Shu W., Drobnjak M., Kakonen S.M., Cordón-Cardo C., Guise T.A., Massagué J. A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 2003, 3:537-549.
24. Krause D.S., Van Etten R.A. Tyrosine kinases as targets for cancer therapy. N.Engl. J. Med. 2005, 353:172-187.
25. Kretschmann K.L., Eyob H., Buys S.S., Welm A.L. The macrophage stimulating protein/Ron pathway as a potential therapeutic target to impede multiple mechanisms involved in breast cancer progression. Curr. Drug Targets 2010, 11:1157-1168.
26. Krzywinski M., Schein J., Birol I., Connors J., Gascoyne R., Horsman D., Jones S.J., Marra M.A. Circos: an information aesthetic for comparative genomics. Genome Res. 2009, 19:1639-1645.
27. Li B.Q., Wang M.H., Kung H.F., Ronsin C., Breathnach R., Leonard E.J., Kamata T. Macrophage-stimulating protein activates Ras by both activation and translocation of SOS nucleotide exchange factor. Biochem. Biophys. Res. Commun. 1995, 216:110-118.
28. Liu X., Zhao L., Derose Y.S., Lin Y.C., Bieniasz M., Eyob H., Buys S.S., Neumayer L., Welm A.L. Short-form Ron promotes spontaneous breast cancer metastasis through interaction with phosphoinositide 3-kinase. Genes Cancer 2011, 2:753-762.
29. Miller L.D., Smeds J., George J., Vega V.B., Vergara L., Ploner A., Pawitan Y., Hall P., Klaar S., Liu E.T., Bergh J. An expression signature for p53 status in human breast cancer predicts mutation status, transcriptional effects, and patient survival. Proc. Natl. Acad. Sci. USA 2005, 102:13550-13555.
30. Minn A.J., Gupta G.P., Siegel P.M., Bos P.D., Shu W., Giri D.D., Viale A., Olshen A.B., Gerald W.L., Massagué J. Genes that mediate breast cancer metastasis to lung. Nature 2005, 436:518-524.
31. Nix D.A., Di Sera T.L., Dalley B.K., Milash B.A., Cundick R.M., Quinn K.S., Courdy S.J. Next generation tools for genomic data generation, distribution, and visualization. BMC Bioinformatics 2010, 11:455.
32. Petronzelli F., Riccio A., Markham G.D., Seeholzer S.H., Stoerker J., Genuardi M., Yeung A.T., Matsumoto Y., Bellacosa A. Biphasic kinetics of the human DNA repair protein MED1 (MBD4), a mismatch-specific DNA N-glycosylase. J.Biol. Chem. 2000, 275:32422-32429.
33. Rai K., Huggins I.J., James S.R., Karpf A.R., Jones D.A., Cairns B.R. DNA demethylation in zebrafish involves the coupling of a deaminase, a glycosylase, and gadd45. Cell 2008, 135:1201-1212.
34. Rai K., Sarkar S., Broadbent T.J., Voas M., Grossmann K.F., Nadauld L.D., Dehghanizadeh S., Hagos F.T., Li Y., Toth R.K., et al. DNA demethylase activity maintains intestinal cells in an undifferentiated state following loss of APC. Cell 2010, 142:930-942.
35. Rodenhiser D.I., Andrews J., Kennette W., Sadikovic B., Mendlowitz A., Tuck A.B., Chambers A.F. Epigenetic mapping and functional analysis in a breast cancer metastasis model using whole-genome promoter tiling microarrays. Breast Cancer Res. 2008, 10:R62.
36. Ronsin C., Muscatelli F., Mattei M.G., Breathnach R. A novel putative receptor protein tyrosine kinase of the met family. Oncogene 1993, 8:1195-1202.
37. Santoro M.M., Collesi C., Grisendi S., Gaudino G., Comoglio P.M. Constitutive activation of the RON gene promotes invasive growth but not transformation. Mol. Cell. Biol. 1996, 16:7072-7083.
38. Segal E., Friedman N., Koller D., Regev A. A module map showing conditional activity of expression modules in cancer. Nat. Genet. 2004, 36:1090-1098.
39. Sørlie T., Perou C.M., Tibshirani R., Aas T., Geisler S., Johnsen H., Hastie T., Eisen M.B., van de Rijn M., Jeffrey S.S., et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc. Natl. Acad. Sci. USA 2001, 98:10869-10874.
40. Steinig A.G., Li A.H., Wang J., Chen X., Dong H., Ferraro C., Jin M., Kadalbajoo M., Kleinberg A., Stolz K.M., et al. Novel 6-aminofuro[3,2-c]pyridines as potent, orally efficacious inhibitors of cMET and RON kinases. Bioorg. Med. Chem. Lett. 2013, 23:4381-4387.
41. Stephens P.J., Tarpey P.S., Davies H., Van Loo P., Greenman C., Wedge D.C., Nik-Zainal S., Martin S., Varela I., Bignell G.R., et al. The landscape of cancer genes and mutational processes in breast cancer. Nature 2012, 486:400-404. Oslo Breast Cancer Consortium (OSBREAC).
42. Suvà M.L., Riggi N., Bernstein B.E. Epigenetic reprogramming in cancer. Science 2013, 339:1567-1570.
43. van de Vijver M.J., He Y.D., van't Veer L.J., Dai H., Hart A.A., Voskuil D.W., Schreiber G.J., Peterse J.L., Roberts C., Marton M.J., et al. A gene-expression signature as a predictor of survival in breast cancer. N.Engl. J. Med. 2002, 347:1999-2009.
44. van 't Veer L.J., Dai H., van de Vijver M.J., He Y.D., Hart A.A., Mao M., Peterse H.L., van der Kooy K., Marton M.J., Witteveen A.T., et al. Gene expression profiling predicts clinical outcome of breast cancer. Nature 2002, 415:530-536.
45. Wang M.H., Ronsin C., Gesnel M.C., Coupey L., Skeel A., Leonard E.J., Breathnach R. Identification of the ron gene product as the receptor for the human macrophage stimulating protein. Science 1994, 266:117-119.
46. Wang M.H., Montero-Julian F.A., Dauny I., Leonard E.J. Requirement of phosphatidylinositol-3 kinase for epithelial cell migration activated by human macrophage stimulating protein. Oncogene 1996, 13:2167-2175.
47. Wang M.H., Padhye S.S., Guin S., Ma Q., Zhou Y.Q. Potential therapeutics specific to c-MET/RON receptor tyrosine kinases for molecular targeting in cancer therapy. Acta Pharmacol. Sin. 2010, 31:1181-1188.
48. Welm A.L., Sneddon J.B., Taylor C., Nuyten D.S., van de Vijver M.J., Hasegawa B.H., Bishop J.M. The macrophage-stimulating protein pathway promotes metastasis in a mouse model for breast cancer and predicts poor prognosis in humans. Proc. Natl. Acad. Sci. USA 2007, 104:7570-7575.