A regulatory circuit of miR-148a/152 and DNMT1 in modulating cell transformation and tumor angiogenesis through IGF-IR and IRS1

Journal of Molecular Cell Biology

Volumn 5, Issue 1, 2013, Pages 3-13

  Xu, Qing ^a   Jiang, Yue ^b,c   Yin, Yu ^a,d   Li, Qi ^a   He, Jun ^b   Jing, Yi ^b   Qi, Yan Ting ^b   Xu, Qian ^a   Li, Wei ^a   Lu, Bo ^b   Peiper, Stephen S ^b   Jiang, Bing Hua ^a,b   Liu, Ling Zhi ^b  

^a NANJING MEDICAL UNIVERSITY   (China)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c FUJIAN NORMAL UNIVERSITY   (China)

^d ANHUI MEDICAL UNIVERSITY   (China)

Author keywords

breast cancer; DNMT1; IGF IR; IRS1; miR 148a; miR 152; tumor angiogenesis

Indexed keywords

DNA METHYLTRANSFERASE 1; INSULIN RECEPTOR SUBSTRATE 1; MICRORNA; MICRORNA 148A; MICRORNA 152; SOMATOMEDIN C RECEPTOR; UNCLASSIFIED DRUG; DNA (CYTOSINE 5) METHYLTRANSFERASE; DNA (CYTOSINE-5-)-METHYLTRANSFERASE 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INSULIN RECEPTOR SUBSTRATE; IRS1 PROTEIN, HUMAN; MIRN148 MICRORNA, HUMAN; MIRN152 MICRORNA, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; VASCULOTROPIN A;

ADULT; ANGIOGENESIS; ARTICLE; BREAST CANCER; CANCER CELL; CELL PROLIFERATION; CELL TRANSFORMATION; CLINICAL ARTICLE; COLONY FORMATION; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; DOWN REGULATION; FEMALE; GENE EXPRESSION; GENETIC REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; NEGATIVE FEEDBACK; UPREGULATION; AGED; BREAST TUMOR; CANCER GRADING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MIDDLE AGED; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; PROMOTER REGION; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ADULT; AGED; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INSULIN RECEPTOR SUBSTRATE PROTEINS; MICRORNAS; MIDDLE AGED; MITOGEN-ACTIVATED PROTEIN KINASES; NEOPLASM GRADING; NEOVASCULARIZATION, PATHOLOGIC; PHOSPHATIDYLINOSITOL 3-KINASES; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, IGF TYPE 1; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84874306245     PISSN: 16742788     EISSN: 17594685     Source Type: Journal    
DOI: 10.1093/jmcb/mjs049     Document Type: Article

References (51)

1. Ahluwalia, A., Hurteau, J.A., Bigsby, R.M., et al. (2001). DNA methylation in ovarian cancer. II. Expression of DNA methyltransferases in ovarian cancer cell lines and normal ovarian epithelial cells. Gynecol. Oncol. 82, 299-304. (Pubitemid 32730607)
2. Balaguer, F., Link, A., Lozano, J.J., et al. (2010). Epigenetic silencing of miR-137 is an early event in colorectal carcinogenesis. Cancer Res. 70, 6609-6618.
3. Bartel, D.P. (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297.
4. Bernardino, J., Roux, C., Almeida, A., et al. (1997). DNA hypomethylation in breast cancer: an independent parameter of tumor progression? Cancer Genet. Cytogenet. 97, 83-89. (Pubitemid 27362497)
5. Berns, K., Horlings, H.M., Hennessy, B.T., et al. (2007). A functional genetic approach identifies the PI3K pathway as a major determinant of trastuzumab resistance in breast cancer. Cancer Cell 12, 395-402. (Pubitemid 47539306)
6. Bestor, T.H. (2000). The DNA methyltransferases of mammals. Hum. Mol. Genet. 9, 2395-2402.
7. Birgisdottir, V., Stefansson, O.A., Bodvarsdottir, S.K., et al. (2006). Epigenetic silencing and deletion of the BRCA1 gene in sporadic breast cancer. Breast Cancer Res. 8, R38.
8. Brooks, P.C., Silletti, S., von Schalscha, T.L., et al. (1998). Disruption of angiogenesis by PEX, a noncatalytic metalloproteinase fragment with integrin binding activity. Cell 92, 391-400. (Pubitemid 28093016)
9. Brooks, J., Cairns, P., and Zeleniuch-Jacquotte, A. (2009). Promoter methylation and the detection of breast cancer. Cancer Causes Control 20, 1539-1550.
10. Calin, G.A., Ferracin, M., Cimmino, A., et al. (2005). A MicroRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N. Engl. J. Med. 353, 1793-1801. (Pubitemid 41549891)
11. Campan, M., Weisenberger, D.J., and Laird, P.W. (2006). DNA methylation profiles of female steroid hormone-driven human malignancies. Curr. Top. Microbiol. Immunol. 310, 141-178. (Pubitemid 47400289)
12. Chang, Q., Li, Y., White, M.F., et al. (2002). Constitutive activation of insulin receptor substrate 1 is a frequent event in human tumors: therapeutic implications. Cancer Res. 62, 6035-6038. (Pubitemid 35244449)
13. Chen, Y., Song, Y., Wang, Z., et al. (2010). Altered expression of MiR-148a and MiR-152 in gastrointestinal cancers and its clinical significance. J. Gastrointest. Surg. 14, 1170-1179.
14. Chen, P.S., Su, J.L., Cha, S.T., et al. (2011). miR-107 promotes tumor progression by targeting the let-7 microRNA in mice and humans. J. Clin. Invest. 121, 3442-3455.
15. De Meyts, P., and Whittaker, J. (2002). Structural biology of insulin and IGF1 receptors: implications for drug design. Nat. Rev. Drug Discov. 1, 769-783. (Pubitemid 37361561)
16. Dearth, R.K., Cui, X., Kim, H.J., et al. (2006). Mammary tumorigenesis and metastasis caused by overexpression of insulin receptor substrate 1 (IRS-1) or IRS-2. Mol. Cell. Biol. 26, 9302-9314. (Pubitemid 44904425)
17. del Rincon, S.V., Guo, Q., Morelli, C., et al. (2004). Retinoic acid mediates degradation of IRS-1 by the ubiquitin-proteasome pathway, via a PKC-dependant mechanism. Oncogene 23, 9269-9279. (Pubitemid 40069697)
18. Egger, G., Liang, G., Aparicio, A., et al. (2004). Epigenetics in human disease and prospects for epigenetic therapy. Nature 429, 457-463. (Pubitemid 38715140)
19. Hanoun, N., Delpu, Y., Suriawinata, A.A., et al. (2010). The silencing of microRNA 148a production by DNA hypermethylation is an early event in pancreatic carcinogenesis. Clin. Chem. 56, 1107-1118.
20. Hennessy, B.T., Smith, D.L., Ram, P.T., et al. (2005). Exploiting the PI3K/AKT pathway for cancer drug discovery. Nat. Rev. Drug Discov. 4, 988-1004.
21. Hildebrandt, M.A., Gu, J., Lin, J., et al. (2010). Hsa-miR-9 methylation status is associated with cancer development and metastatic recurrence in patients with clear cell renal cell carcinoma. Oncogene 29, 5724-5728.
22. Huang, J., Wang, Y., Guo, Y., et al. (2010). Down-regulated microRNA-152 induces aberrant DNA methylation in hepatitis B virus-related hepatocellular carcinoma by targeting DNA methyltransferase 1. Hepatology 52, 60-70.
23. Iorio, M.V., Ferracin, M., Liu, C.G., et al. (2005). MicroRNA gene expression deregulation in human breast cancer. Cancer Res. 65, 7065-7070. (Pubitemid 41161233)
24. Jiang, B.H., Zheng, J.Z., Aoki, M., et al. (2000). Phosphatidylinositol 3-kinase signaling mediates angiogenesis and expression of vascular endothelial growth factor in endothelial cells. Proc. Natl Acad. Sci. USA 97, 1749-1753. (Pubitemid 30118514)
25. Jin, Z., Tamura, G., Tsuchiya, T., et al. (2001). Adenomatous polyposis coli (APC) gene promoter hypermethylation in primary breast cancers. Br. J. Cancer 85, 69-73. (Pubitemid 32695718)
26. Karpf, A.R., and Matsui, S. (2005). Genetic disruption of cytosine DNA methyltransferase enzymes induces chromosomal instability in human cancer cells. Cancer Res. 65, 8635-8639. (Pubitemid 41377349)
27. Kozaki, K., Imoto, I., Mogi, S., et al. (2008). Exploration of tumor-suppressive microRNAs silenced by DNA hypermethylation in oral cancer. Cancer Res. 68, 2094-2105. (Pubitemid 351521781)
28. La Rocca, G., Shi, B., Badin, M., et al. (2009). Growth inhibition by microRNAs that target the insulin receptor substrate-1. Cell Cycle 8, 2255-2259.
29. Lehmann, U., Hasemeier, B., Christgen, M., et al. (2008). Epigenetic inactivation of microRNA gene hsa-mir-9-1 in human breast cancer. J. Pathol. 214, 17-24.
30. Liu, X., Zhan, Z., Xu, L., et al. (2010). MicroRNA-148/152 impair innate response and antigen presentation of TLR-triggered dendritic cells by targeting CaMKIIalpha. J. Immunol. 185, 7244-7251.
31. Mirza, S., Sharma, G., Prasad, C.P., et al. (2007). Promoter hypermethylation of TMS1, BRCA1, ERalpha and PRB in serum and tumor DNA of invasive ductal breast carcinoma patients. Life Sci. 81, 280-287. (Pubitemid 47030571)
32. Mizuno, S., Chijiwa, T., Okamura, T., et al. (2001). Expression of DNA methyltransferases DNMT1, 3A, and 3B in normal hematopoiesis and in acute and chronic myelogenous leukemia. Blood 97, 1172-1179. (Pubitemid 32183737)
33. Pan, W., Zhu, S., Yuan, M., et al. (2010). MicroRNA-21 and microRNA-148a contribute to DNA hypomethylation in lupus CD4+ T cells by directly and indirectly targeting DNA methyltransferase 1. J. Immunol. 184, 6773-6781.
34. Park, B.H., and Davidson, N.E. (2007). PI3 kinase activation and response to Trastuzumab Therapy: what's neu with herceptin resistance? Cancer Cell 12, 297-299. (Pubitemid 47539315)
35. Robertson, K.D., Uzvolgyi, E., Liang, G., et al. (1999). The human DNA methyltransferases (DNMTs) 1, 3a and 3b: coordinate mRNA expression in normal tissues and overexpression in tumors. Nucleic Acids Res. 27, 2291-2298. (Pubitemid 29245646)
36. Roll, J.D., Rivenbark, A.G., Jones, W.D., et al. (2008). DNMT3b overexpression contributes to a hypermethylator phenotype in human breast cancer cell lines. Mol. Cancer 7, 15.
37. Sehat, B., Tofigh, A., Lin, Y., et al. (2010). SUMOylation mediates the nuclear translocation and signaling of the IGF-1 receptor. Sci. Signal. 3, ra10.
38. Semenza, G.L. (2011). Oxygen sensing, homeostasis, and disease. N. Engl. J. Med. 365, 537-547.
39. Soares, J., Pinto, A.E., Cunha, C.V., et al. (1999). Global DNA hypomethylation in breast carcinoma: correlation with prognostic factors and tumor progression. Cancer 85, 112-118. (Pubitemid 29031364)
40. Stumpel, D.J., Schotte, D., Lange-Turenhout, E.A., et al. (2011). Hypermethylation of specific microRNA genes in MLL-rearranged infant acute lymphoblastic leukemia: major matters at a micro scale. Leukemia 25, 429-439.
41. Sui, M., Huang, Y., Park, B.H., et al. (2007). Estrogen receptor alpha mediates breast cancer cell resistance to paclitaxel through inhibition of apoptotic cell death. Cancer Res. 67, 5337-5344. (Pubitemid 46997273)
42. Sun, X.J., Rothenberg, P., Kahn, C.R., et al. (1991). Structure of the insulin receptor substrate IRS-1 defines a unique signal transduction protein. Nature 352, 73-77. (Pubitemid 21896701)
43. Tamimi, R.M., Colditz, G.A., Wang, Y., et al. (2011). Expression of IGF1R in normal breast tissue and subsequent risk of breast cancer. Breast Cancer Res. Treat. 128, 243-250.
44. Toyota, M., Suzuki, H., Sasaki, Y., et al. (2008). Epigenetic silencing of microRNA-34b/c and B-cell translocation gene 4 is associated with CpG island methylation in colorectal cancer. Cancer Res. 68, 4123-4132.
45. Visvanathan, K., Sukumar, S., and Davidson, N.E. (2006). Epigenetic biomarkers and breast cancer: cause for optimism. Clin. Cancer Res. 12, 6591-6593. (Pubitemid 44876824)
46. Vivanco, I., and Sawyers, C.L. (2002). The phosphatidylinositol 3-kinase AKT pathway in human cancer. Nat. Rev. Cancer 2, 489-501. (Pubitemid 37328931)
47. Wilson, A.S., Power, B.E., and Molloy, P.L. (2007). DNA hypomethylation and human diseases. Biochim. Biophys. Acta 1775, 138-162. (Pubitemid 44881198)
48. Wolffe, A.P., and Matzke, M.A. (1999). Epigenetics: regulation through repression. Science 286, 481-486.
49. Xia, C., Meng, Q., Liu, L.Z., et al. (2007). Reactive oxygen species regulate angiogenesis and tumor growth through vascular endothelial growth factor. Cancer Res. 67, 10823-10830. (Pubitemid 350145911)
50. Xu, Q., Liu, L.Z., Qian, X., et al. (2012). MiR-145 directly targets p70S6K1 in cancer cells to inhibit tumor growth and angiogenesis. Nucleic Acids Res. 40, 761-774.
51. Zheng, B., Liang, L., Wang, C., et al. (2011). MicroRNA-148a suppresses tumor cell invasion and metastasis by downregulating ROCK1 in gastric cancer. Clin. Cancer Res. 17, 7574-7583.