Targeted methylation of two tumor suppressor genes is sufficient to transform mesenchymal stem cells into cancer stem/initiating cells

Cancer Research

Volumn 71, Issue 13, 2011, Pages 4653-4663

  Teng, I Wen ^a   Hou, Pei Chi ^a   Lee, Kuan Der ^b   Chu, Pei Yi ^c   Yeh, Kun Tu ^c   Jin, Victor X ^d   Tseng, Min Jen ^a   Tsai, Shaw Jenq ^e   Chang, Yu Sun ^e   Wu, Chi Sheng ^e   Sun, H Sunny ^f   Tsai, Kuen Daw ^a,g   Jeng, Long Bin ^g   Nephew, Kenneth P ^h   Huang, Tim H M ⁱ   Hsiao, Shu Huei ^a   Leu, Yu Wei ^a  

^a NATIONAL CHUNG CHENG UNIVERSITY   (Taiwan)

^b CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

^c CHANGHUA CHRISTIAN HOSPITAL   (Taiwan)

^d OHIO STATE UNIVERSITY   (United States)

^e NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^f CHANG GUNG UNIVERSITY   (Taiwan)

^g CHINA MEDICAL UNIVERSITY BEIGANG HOSPITAL   (Taiwan)

^h INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

ⁱ OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; DNA FRAGMENT; DNA METHYLTRANSFERASE INHIBITOR;

ANCHORAGE INDEPENDENT GROWTH; ANIMAL CELL; ARTICLE; CANCER STEM CELL; CARCINOGENESIS; CELL LINEAGE; CELL LOSS; COLONY FORMATION; CONTROLLED STUDY; DNA METHYLATION; DRUG ACTIVITY; DRUG RESISTANCE; GENETIC ASSOCIATION; GENETIC TRANSFECTION; GENETIC TRANSFORMATION; HETEROZYGOSITY; HIC1 GENE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; INOCULATION; MARKER GENE; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; PHENOTYPE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROMOTER REGION; RASSF1A GENE; REPORTER GENE; SOFT TISSUE SARCOMA; TUMOR SUPPRESSOR GENE; TUMOR XENOGRAFT; XENOTRANSPLANTATION;

ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; CLONING, MOLECULAR; DNA METHYLATION; GENES, TUMOR SUPPRESSOR; HUMANS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MESENCHYMAL STEM CELLS; MICE; MICE, NUDE; NEOPLASTIC STEM CELLS; PROMOTER REGIONS, GENETIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSFECTION; TRANSPLANTATION, HETEROLOGOUS; TUMOR MARKERS, BIOLOGICAL; TUMOR SUPPRESSOR PROTEINS;

EID: 79959868249     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-3418     Document Type: Article

References (44)

1. Baylin S. DNA methylation and epigenetic mechanisms of carcinogenesis. Dev Biol 2001;106:85-7.
2. Esteller M. Epigenetics in cancer. N Engl J Med 2008;358:1148-59.
3. Feinberg AP, Tycko B. The history of cancer epigenetics. Nat Rev Cancer 2004;4:143-53.
4. Balch C, Nephew KP, Huang TH, Bapat SA. Epigenetic "bivalently marked" process of cancer stem cell-driven tumorigenesis. Bioessays 2007;29:842-5.
5. Baylin SB ,Ohm JE. Epigenetic gene silencing in cancer-a mechanism for early oncogenic pathway addiction?Nat Rev Cancer 2006;6:107-16.
6. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev 2002;16:6-21.
7. Feinberg AP. Phenotypic plasticity and the epigenetics of human disease. Nature 2007;447:433-40.
8. Jones PA, Baylin SB. The epigenomics of cancer. Cell 2007;128:683-92.
9. Eden A, Gaudet F, Waghmare A, Jaenisch R. Chromosomal instability and tumors promoted by DNA hypomethylation. Science 2003;300:455.
10. Gaudet F, Hodgson JG, Eden A, Jackson-Grusby L, Dausman J, Gray JW, et al. Induction of tumors in mice by genomic hypomethylation. Science 2003;300:489-92.
11. Hsiao SH, Lee KD, Hsu CC, Tseng MJ, Jin VX, Sun WS, et al. DNA methylation of the Trip10 promoter accelerates mesenchymal stem cell lineage determination. Biochem Biophys Res Commun 2010;400:305-312.
12. Hsu CC, Li HP, Hung YH, Leu YW, Wu WH, Wang FS, et al. Targeted methylation of CMV and E1A viral promoters. Biochem Biophys Res Commun 2010;402:228-234.
13. Rosland GV, Svendsen A, Torsvik A, Sobala E, McCormack E, Immervoll H, et al. Long-term cultures of bone marrow-derived human mesenchymal stem cells frequently undergo spontaneous malignant transformation. Cancer Res 2009;69:5331-9.
14. Torsvik A, Rosland GV, Svendsen A, Molven A, Immervoll H, McCormack E, et al. Spontaneous malignant transformation of human mesenchymal stem cells reflects cross-contamination: putting the research field on track-letter. Cancer Res 2010;70:6393-6.
15. Rubio R, Garcia-Castro J, Gutierrez-Aranda I, Paramio J, Santos M, Catalina P, et al. Deficiency in p53 but not retinoblastoma induces the transformation of mesenchymal stem cells in vitro and initiates leiomyosarcoma in vivo. Cancer Res 2010;70:4185-94.
16. Chen W, Cooper TK, Zahnow CA, Overholtzer M, Zhao Z, Ladanyi M, et al. Epigenetic and genetic loss of Hic1 function accentuates the role of p53 in tumorigenesis. Cancer Cell 2004;6:387-98.
17. Chen WY, Zeng X, Carter MG, Morrell CN, Chiu Yen RW, Esteller M, et al. Heterozygous disruption of Hic1 predisposes mice to a gender-dependent spectrum of malignant tumors. Nat Genet 2003;33: 197-202.
18. Leu YW, Rahmatpanah F, Shi H, Wei SH, Liu JC, Yan PS, et al. Double RNA interference of DNMT3b and DNMT1 enhances DNA demethylation and gene reactivation. Cancer Res 2003;63:6110-5.
19. Fleuriel C, Touka M, Boulay G, Guerardel C, Rood BR, Leprince D. HIC1 (hypermethylated in cancer 1) epigenetic silencing in tumors. Int J Biochem Cell Biol 2009;41:26-33.
20. Harvey K, Tapon N. The Salvador-Warts-Hippo pathway-an emerging tumour-suppressor network. Nat Rev Cancer 2007;7:182-91.
21. Lee KD, Kuo TK, Whang-Peng J, Chung YF, Lin CT, Chou SH, et al. In vitro hepatic differentiation of human mesenchymal stem cells. Hepatology 2004;40:1275-84.
22. Yan PS, Venkataramu C, Ibrahim A, Liu JC, Shen RZ, Diaz NM, et al. Mapping geographic zones of cancer risk with epigenetic biomarkers in normal breast tissue. Clin Cancer Res 2006;12:6626-36.
23. Yan PS, Wei SH, Huang TH. Differential methylation hybridization using CpG island arrays. Methods Mol Biol 2002;200:87-100.
24. Palakurthy RK, Wajapeyee N, Santra MK, Gazin C, Lin L, Gobeil S, et al. Epigenetic silencing of the RASSF1A tumor suppressor gene through HOXB3-mediated induction of DNMT3B expression. Mol Cell 2009;36:219-30.
25. Zhang S, Balch C, Chan MW, Lai HC, Matei D, Schilder JM, et al. Identification and characterization of ovarian cancer-initiating cells from primary human tumors. Cancer Res 2008;68:4311-20.
26. Bennett FC, Harvey KF. Fat cadherin modulates organ size in Drosophila via the Salvador/Warts/Hippo signaling pathway. Curr Biol 2006;16:2101-10.
27. Meignin C, Alvarez-Garcia I, Davis I, Palacios IM. The salvador-wartshippo pathway is required for epithelial proliferation and axis specification in Drosophila. Curr Biol 2007;17:1871-8.
28. Polesello C, Tapon N. Salvador-warts-hippo signaling promotes Drosophila posterior follicle cell maturation downstream of notch. Curr Biol 2007;17:1864-70.
29. Hsiao SH, Huang TH, Leu YW. Excavating relics of DNA methylation changes during the development of neoplasia. Semin Cancer Biol 2009;19:198-208.
30. Tsuji T, Ibaragi S, Hu GF. Epithelial-mesenchymal transition and cell cooperativity in metastasis. Cancer Res 2009;69:7135-9.
31. Huber MA, Kraut N, Beug H. Molecular requirements for epithelial-mesenchymal transition during tumor progression. Curr Opin Cell Biol 2005;17:548-58.
32. Yang J, Weinberg RA. Epithelial-mesenchymal transition: at the cross-roads of development and tumor metastasis. Dev Cell 2008;14:818-29.
33. Hu M, Polyak K. Microenvironmental regulation of cancer development. Curr Opin Genet Dev 2008;18:27-34.
34. Karnoub AE, Dash AB, Vo AP, Sullivan A, Brooks MW, Bell GW, et al. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 2007;449:557-63.
35. Serakinci N, Guldberg P, Burns JS, Abdallah B, Schrodder H, Jensen T, et al. Adult human mesenchymal stem cell as a target for neoplastic transformation. Oncogene 2004;23:5095-8.
36. Teodoridis JM, Hall J, Marsh S, Kannall HD, Smyth C, Curto J, et al. CpG island methylation of DNA damage response genes in advanced ovarian cancer. Cancer Res 2005;65:8961-7.
37. AggerholmA, Holm MS, Guldberg P, Olesen LH, Hokland P. Promoter hypermethylation of p15INK4B, HIC1, CDH1, and ER is frequent in myelodysplastic syndrome and predicts poor prognosis in early-stage patients. Eur J Haematol 2006;76:23-32.
38. Kerr JF, Winterford CM, Harmon BV. Apoptosis. Its significance in cancer and cancer therapy. Cancer 1994;73:2013-26.
39. Bjerkvig R, Tysnes BB, Aboody KS, Najbauer J, Terzis AJ. Opinion: the origin of the cancer stem cell: current controversies and new insights. Nat Rev Cancer 2005;5:899-904.
40. Gupta PB, Chaffer CL, Weinberg RA. Cancer stem cells: mirage or reality? Nat Med 2009;15:1010-2.
41. Pardal R, Clarke MF, Morrison SJ. Applying the principles of stem-cell biology to cancer. Nat Rev Cancer 2003;3:895-902.
42. Wicha MS, Liu S, Dontu G. Cancer stem cells: an old idea-a paradigm shift. Cancer Res 2006;66:1883-90.
43. Ohm JE, McGarvey KM, Yu X, Cheng L, Schuebel KE, Cope L, et al. A stem cell-like chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nat Genet 2007;39:237-42.
44. van Iersel MP, Kelder T, Pico AR, Hanspers K, Coort S, Conklin BR, et al. Presenting and exploring biological pathways with PathVisio. BMC Bioinformatics 2008;9:399.