RUNX3 directly interacts with intracellular domain of Notch1 and suppresses Notch signaling in hepatocellular carcinoma cells

Experimental Cell Research

Volumn 316, Issue 2, 2010, Pages 149-157

  Gao, Juan ^a   Chen, Yu ^b   Wu, Kai Chun ^b   Liu, Jie ^b   Zhao, Yan Qiu ^b   Pan, Yang Lin ^b   Du, Rui ^b   Zheng, Guo Rong ^a   Xiong, Yi Min ^a   Xu, Hua Lin ^a   Fan, Dai Ming ^b  

^a WUHAN GENERAL HOSPITAL OF GUANGZHOU COMMAND   (China)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

HCC; HES 1; Notch1; RBP J; RUNX3

Indexed keywords

IMMUNOGLOBULIN J RECOMBINATION SIGNAL SEQUENCE BINDING PROTEIN; NOTCH1 RECEPTOR; TRANSCRIPTION FACTOR HES 1; TRANSCRIPTION FACTOR RUNX3;

ARTICLE; CANCER CELL CULTURE; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; LIVER CELL CARCINOMA; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

EID: 70450255162     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2009.09.025     Document Type: Article

References (46)

1. Kania M.A., Bonner A.S., Duffy J.B., and Gergen J.P. The Drosophila segmentation gene runt encodes a novel nuclear regulatory protein that is also expressed in the developing nervous system. Genes Dev. 4 (1990) 1701-1713
2. Coffman J.A. Runx transcription factors and the developmental balance between cell proliferation and differentiation. Cell Biol. Int. 27 (2003) 315-324
3. Wang Q., Stacy T., Binder M., Marin-Padilla M., Sharpe A.H., and Speck N.A. Disruption of the Cbfa2 gene causes necrosis and hemorrhaging in the central nervous systems and blocks definitive hematopoiesis. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 3444-3449
4. Otto F., Thornell A.P., Crompton T., Denzel A., Gilmour K.C., Rosewell I.R., Stamp G.W., Beddington R.S., Mundlos S., Olsen B.R., Selby P.B., and Owen M.J. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell 89 (1997) 765-771
5. Levanon D., Bettoun D., Harris-Cerruti C., Woolf E., Negreanu V., Eilam R., Bernstein Y., Goldenberg D., Xiao C., Fliegauf M., Kremer E., Otto F., Brenner O., Lev-Tov A., and Groner Y. The Runx3 transcription factor regulates development and survival of TrkC dorsal root ganglia neurons. EMBO J. 21 (2002) 3454-3463
6. Speck N.A., and Gilliland D.G. Core-binding factors in haematopoiesis and leukaemia. Nat. Rev., Cancer 2 (2002) 502-513
7. Pratap J., Lian J.B., Javed A., Barnes G.L., van Wijnen A.J., Stein J.L., and Stein G.S. Regulatory roles of Runx2 in metastatic tumor and cancer cell interactions with bone. Cancer Metastasis Rev. 25 (2006) 589-600
8. Dhillon V.S., Shahid M., and Husain S.A. CpG methylation of the FHIT, FANCF, cyclin-D2, BRCA2 and RUNX3 genes in Granulosa cell tumors (GCTs) of ovarian origin. Mol. Cancer 3 (2004) 33
9. Chi X.Z., Yang J.O., Lee K.Y., Ito K., Sakakura C., Li Q.L., Kim H.R., Cha E.J., Lee Y.H., Kaneda A., Ushijima T., Kim W.J., Ito Y., and Bae S.C. RUNX3 suppresses gastric epithelial cell growth by inducing p21 (WAF1/Cip1) expression in cooperation with transforming growth factor {beta}-activated SMAD. Mol. Cell. Biol. 25 (2005) 8097-8107
10. Li Q.L., Kim H.R., Kim W.J., Choi J.K., Lee Y.H., Kim H.M., Li L.S., Kim H., Chang J., Ito Y., Lee K.Y., and Bae S.C. Transcriptional silencing of the RUNX3 gene by CpG hypermethylation is associated with lung cancer. Biochem. Biophys. Res. Commun. 314 (2004) 223-228
11. Takahashi T., Shivapurkar N., Riquelme E., Shigematsu H., Reddy J., Suzuki M., Miyajima K., Zhou X., Bekele B.N., Gazdar A.F., and Wistuba I.I. Aberrant promoter hypermethylation of multiple genes in gall bladder carcinoma and chrocholecystitis. Clin. Cancer Res. 10 (2004) 6126-6133
12. Li Q.L., Ito K., Sakakura C., Fukamachi H., Inoue K., Chi X.Z., Lee K.Y., Nomura S., Lee C.W., Han S.B., Kim H.M., Kim W.J., Yamamoto H., Yamashita N., Yano T., Ikeda T., Itohara S., Inazawa J., Abe T., Hagiwara A., Yamagishi H., Ooe A., Kaneda A., Sugimura T., Ushijima T., Bae S.C., and Ito Y. Causal relationship between the loss of RUNX3 expression and gastric cancer. Cell 109 (2002) 113-124
13. Kang S., Kim J.W., Kang G.H., Park N.H., Song Y.S., Kang S.B., and Lee H.P. Polymorphism in folate- and methionine-metabolizing enzyme and aberrant CpG island hypermethylation in uterine cervical cancer. Gynecol. Oncol. 96 (2005) 173-180
14. Guo C., Ding J., Yao L., Sun L., Lin T., Song Y., Sun L., and Fan D.M. Tumor suppressor gene Runx3 sensitizes gastric cancer cells to chemotherapeutic drugs by down-regulating Bcl-2, MDR-1 and MRP-1. Int. J. Cancer 116 (2005) 155-160
15. Wei D., Gong W., Oh S.C., Li Q., Kim W.D., Wang L., Le X., Yao J., Wu T.T., Huang S., and Xie K. Loss of RUNX3 expression significantly affects the clinical outcome of gastric cancer patients and its restoration causes drastic suppression of tumor growth and metastasis. Cancer Res. 65 (2005) 4809-4816
16. Yamamura Y., Lee W.L., Inoue K., Ida H., and Ito Y. RUNX3 cooperates with FoxO3a to induce apoptosis in gastric cancer cells. J. Biol. Chem. 281 (2006) 5267-5276
17. Miyagawa K., Sakakura C., Nakashima S., Yoshikawa T., Kin S., Nakase Y., Ito K., Yamagishi H., Ida H., Yazumi S., Chiba T., Ito Y., and Hagiwara A. Down-regulation of RUNX1, RUNX3 and CBFbeta in hepatocellular carcinomas in an early stage of hepatocarcinogenesis. Anticancer Res. 26 (2006) 3633-3643
18. Park W.S., Cho Y.G., Kim C.J., Song J.H., Lee Y.S., Kim S.Y., Nam S.W., Lee S.H., Yoo N.J., and Lee J.Y. Hypermethylation of the RUNX3 gene in hepatocellular carcinoma. Exp. Mol. Med. 37 (2005) 276-281
19. Mori T., Nomoto S., Koshikawa K., Fujii T., Sakai M., Nishikawa Y., Inoue S., Takeda S., Kaneko T., and Nakao A. Decreased expression and frequent allelic inactivation of the RUNX3 gene at 1p36 in human hepatocellular carcinoma. Liver Int. 25 (2005) 380-388
20. Davis R.L., and Turner D.L. Vertebrate hairy and Enhancer of split related proteins: transcriptional repressors regulating cellular differentiation and embryo patterning. Oncogene 20 (2001) 8342-8357
21. Tun T., Hamaguchi Y., Matsunami N., Furukawa T., and Honjo T. Recognition sequence of a highly conserved DNA binding protein RBP-Jk. Nucleic Acids Res. 22 (1994) 965-971
22. Ellisen L.W., Bird J., West D.C., Soreng A.L., Reynolds T.C., Smith S.D., and Sklar J. TAN-1, the human homolog of the Drosophila notch gene, is broken by chromosomal translocations in T lymphoblastic neoplasms. Cell 66 (1991) 649-661
23. Gallahan D., and Callahan R. The mouse mammary tumor associated gene INT-3 is a unique member of the NOTCH gene family (NOTCH4). Oncogene 14 (1997) 1883-1890
24. Balint K., Xiao M., Pinnix C.C., A Soma I., Veres I., Juhasz E.J., Brown A.J., Herlyn M., and Liu Z.J. Activation of Notch1 signaling is required for β-catenin-mediated human primary melanoma progression. J. Clin. Invest. 115 (2005) 3166-3176
25. Wang Z., Banerjee S., Li Y., Rahman K.M.W., Zhang Y., and Sarkar F.H. Down-regulation of Notch-1 inhibits invasion by inactivation of nuclear factor-KB, vascular endothelial growth factor, and matrix metalloproteinase-9 in pancreatic cancer cells. Cancer Res. 66 (2006) 2778-2784
26. Wang Z., Zhang Y., Li Y., Banerjee S., Liao J., and Sarkar F.H. Down-regulation of Notch-1 contributes to cell growth inhibition and apoptosis in pancreatic cancer cells. Mol. Cancer Ther. 5 (2006) 483-493
27. Jensen C.H., Jauho E.I., Santoni-Rugiu E., Holmskov U., Teisner B., Tygstrup N., and Bisgaard H.C. Transit-amplifying ductular (oval) cells and their hepatocytic progeny are characterized by a novel and distinctive expression of Delta-like protein/preadipocyte factor1/fetal antigen1. Am. J. Pathol. 164 (2004) 1347-1359
28. Kohler C., Bell A.W., Bowen W.C., Monga S.P., Fleig W., and Michalopoulos G.K. Expression of Notch-1 and its ligand Jagged-1 in rat liver during liver regeneration. Hepatology 39 (2004) 1056-1065
29. Cantarini M.C., de la Monte S.M., Pang M., Tong M., D'Errico A., Trevisani F., and Wands J.R. Aspartyl-asparagyl β hydroxylase over-expression in hum an hepatoma is linked to activation of insulin-like growth factor and Notch signaling mechanisms. Hepatology 44 (2006) 46-457
30. Gao J., Chen C., Hong L., Wang J., Du Y., Song J., Shao X., Zhang J., Han H., Liu J., and Fan D. Expression of Jagged1 and its association with hepatitis B virus X protein in hepatocellular carcinoma. Biochem. Biophys. Res. Commun. 356 (2007) 341-347
31. Gao J., Song Z., Chen Y., Xia L., Wang J., Fan R., Du R., Zhang F., Hong L., Song J., Zou X., Xu H., Zheng G., Liu J., and Fan D. Deregulated expression of Notch receptors in human hepatocellular carcinoma. Dig. Liver Dis. 40 (2008) 114-121
32. Spender L.C., Whiteman H.J., Karstegl C.E., and Farrell P.J. Transcriptional cross-regulation of RUNX1 by RUNX3 in human B cells. Oncogene 24 (2005) 1873-1881
33. Ross D.A., and Kadesch T. The Notch intracellular domain can function as a coactivator for LEF-1. Mol. Cell. Biol. 21 (2001) 537-7544
34. Qin H., Wang J., Liang Y., Taniguchi Y., Tanigaki K., and Han H. RING1 inhibits transactivation of RBP-J by Notch through interaction with LIM protein KyoT2. Nucleic Acids Res. 32 (2004) 1492-1501
35. Kato H., Taniguchi Y., Kurooka H., Minoguchi S., Sakai T., Nomura-Okazaki S., Tamura K., and Honjo T. Involvement of RBP-J in biological functions of mouse Notch1 and its derivatives. Development 124 (1997) 4133-4141
36. Li J., Li J., Yang X., Qin H., Zhou P., Liang Y., and Han H. The C terminus of MINT forms homodimers and abrogates MINT-mediated transcriptional repression. Biochim. Biophys. Acta 1729 (2005) 50-56
37. Liang Y., Chang J., Lynch S.J., Lukac D.M., and Ganem D. The lytic switch protein of KSHV activates gene expression via functional interaction with RBP-Jκ (CSL), the target of the Notch signaling pathway. Gene Dev. 16 (2002) 1977-1989
38. McLarren K.W., Theriault F.M., and Stifani S. Association with the nuclear matrix and interaction with Groucho and RUNX proteins regulate the transcription repression activity of the basic helix loop helix factor Hes1. J. Biol. Chem. 276 (2001) 1578-1584
39. Burns C.E., Traver D., Mayhall E., Shepard J.L., and Zon L.I. Hematopoietic stem cell fate is established by the Notch-Runx pathway. Genes Dev 19 (2005) 2331-2342
40. Tsai C., and Gergen P. Pair-rule expression of the Drosophila fushi tarazu gene: a nuclear receptor response element mediates the opposing regulatory effects of runtand hairy. Development 121 (1995) 453-462
41. Garg V., Muth A.N., Ransom J.F., Schluterman M.K., Barnes R., King I.N., Grossfeld P.D., and Srivastava D. Mutations in NOTCH1 cause aortic valve disease. Nature 437 (2005) 270-274
42. Durst K.L., and Hiebert S.W. Role of RUNX family members in transcriptional repression and gene silencing. Oncogene 23 (2004) 4220-4224
43. Hanai J., Chen L.F., Kanno T., Ohtani-Fujita N., Kim W.Y., Guo W.H., Imamura T., Ishidou Y., Fukuchi M., Shi M.J., Stavnezer J., Kawabata M., Miyazono K., and Ito Y. Interaction and functional cooperation of PEBP2/CBF with Smads. Synergistic induction of the immunoglobulin germline Calpha promoter. J. Biol. Chem. 274 (1999) 31577-31582
44. Waltzer L., Ferjoux G., Bataille L., and Haenlin M., Cooperation between the GATA and RUNX factors Serpent and Lozenge during Drosophila hematopoiesis. EMBO J. 24 (2003) 6516-6525
45. Kao H.Y., Ordentlich P., Koyano-Nakagawa N., Tang Z., Downes M., Kintner C.R., Evans R.M., and Kadesch T. A histone deacetylase corepressor complex regulates the Notch signal transduction pathway. Genes Dev. 12 (1998) 2269-2277
46. Hsieh J.J., Zhou S., Chen L., Young D.B., and Hayward S.D. CIR, a corepressor linking the DNA binding factor CBF1 to the histone deacetylase complex. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 23-28