Orphan receptor TR3 is essential for the maintenance of stem-like properties in gastric cancer cells

Cancer Letters

Volumn 329, Issue 1, 2013, Pages 37-44

  Zhan, Yan yan ^a,b   He, Jian ping ^b   Chen, Hang zi ^b   Wang, Wei jia ^b   Cai, Jian chun ^a,c  

^a THE FIRST AFFILIATED HOSPITAL OF XIAMEN UNIVERSITY   (China)

^b XIAMEN UNIVERSITY   (China)

^c FUJIAN MEDICAL UNIVERSITY   (China)

Author keywords

Gastric cancer; Nanog; Nuclear orphan receptor TR3; Stem like properties

Indexed keywords

GELATINASE B; MESSENGER RNA; NUCLEAR RECEPTOR NUR77; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR NANOG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL CULTURE; CANCER INVASION; CANCER STEM CELL; CARCINOGENICITY; CELL STRUCTURE; CONTROLLED STUDY; DOWN REGULATION; GELATINASE B GENE; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE SILENCING; GENE TARGETING; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; NUCLEAR RECEPTOR NUR77 GENE; OCTAMER TRANSCRIPTION FACTOR 4 GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATOR GENE; STOMACH CANCER; TRANSCRIPTION FACTOR NANOG GENE; TUMOR GENE;

ANIMALS; BASE SEQUENCE; CELL LINE, TUMOR; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HOMEODOMAIN PROTEINS; HUMANS; MATRIX METALLOPROTEINASE 9; MICE; MICE, INBRED BALB C; MICE, NUDE; MOLECULAR SEQUENCE DATA; NEOPLASTIC STEM CELLS; NUCLEAR RECEPTOR SUBFAMILY 4, GROUP A, MEMBER 1; OCTAMER TRANSCRIPTION FACTOR-3; PROMOTER REGIONS, GENETIC; STOMACH NEOPLASMS; TUMOR MICROENVIRONMENT; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84871720494     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2012.09.022     Document Type: Article

References (42)

1. Han M.E., Lee Y.S., Baek S.Y., Kim B.S., Kim J.B., Oh S.O. Hedgehog signaling regulates the survival of gastric cancer cells by regulating the expression of Bcl-2. Int. J. Mol. Sci. 2009, 10:3033-3043.
2. Jemal A., Siegel R., Ward E., Hao Y., Xu J., Murray T., Thun M.J. Cancer statistics 2008. CA Cancer J. Clin. 2008, 58:71-96.
3. Jordan C.T., Guzman M.L., Noble M. Cancer stem cells. N. Engl. J. Med. 2006, 355:1253-1261.
4. Clarke M.F., Dick J.E., Dirks P.B., Eaves C.J., Jamieson C.H., Jones D.L., Visvader J., Weissman I.L., Wahl G.M. Cancer stem cells - perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res. 2006, 66:9339-9344.
5. Farnie G., Clarke R.B. Mammary stem cells and breast cancer - role of Notch signalling. Stem Cell Rev. 2007, 3:169-175.
6. Al-Hajj M., Wicha M.S., Ito-Hernandez A., Morrison S.J., Clarke M.F. Prospective identification of tumorigenic breast cancer cells. Proc. Natl. Acad. Sci. USA 2003, 100:3983-3988.
7. A. Kreso and C.A. O'Brien, Colon cancer stem cells, Curr. Protoc. Stem Cell Biol. (2008) Unit (Chapter 3).
8. O'Brien C.A., Pollett A., Gallinger S., Dick J.E. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 2007, 445:106-110.
9. Yang Z.F., Ho D.W., Ng M.N., Lau C.K., Yu W.C., Ngai P., Chu P.W., Lam C.T., Poon R.T., Fan S.T. Significance of CD90+ cancer stem cells in human liver cancer. Cancer Cell 2008, 13:153-166.
10. Cao L., Zhou Y., Zhai B., Liao J., Xu W., Zhang R., Li J., Zhang Y., Chen L., Qian H., Wu M., Yin Z. Sphere-forming cell subpopulations with cancer stem cell properties in human hepatoma cell lines. BMC Gastroenterol. 2011, 11:71.
11. Matsui W., Huff C.A., Wang Q., Malehorn M.T., Barber J., Tanhehco Y., Smith B.D., Civin C.I., Jones R.J. Characterization of clonogenic multiple myeloma cells. Blood 2004, 103:2332-2336.
12. Takaishi S., Okumura T., Tu S., Wang S.S., Shibata W., Vigneshwaran R., Gordon S.A., Shimada Y., Wang T.C. Identification of gastric cancer stem cells using the cell surface marker CD44. Stem Cells 2009, 27:1006-1020.
13. Jiang J., Zhang Y., Chuai S., Wang Z., Zheng D., Xu F., Zhang Y., Li C., Liang Y., Chen Z. Trastuzumab (herceptin) targets gastric cancer stem cells characterized by CD90 phenotype. Oncogene 2012, 31:671-682.
14. Zhang C., Li C., He F., Cai Y., Yang H. Identification of CD44+CD24+ gastric cancer stem cells. J. Cancer Res. Clin. Oncol. 2011, 137:1679-1686.
15. Han M.E., Jeon T.Y., Hwang S.H., Lee Y.S., Kim H.J., Shim H.E., Yoon S., Baek S.Y., Kim B.S., Kang C.D., Oh S.O. Cancer spheres from gastric cancer patients provide an ideal model system for cancer stem cell research. Cell. Mol. Life Sci. 2011, 68:3589-3605.
16. Nishii T., Yashiro M., Shinto O., Sawada T., Ohira M., Hirakawa K. Cancer stem cell-like SP cells have a high adhesion ability to the peritoneum in gastric carcinoma. Cancer Sci. 2009, 100:1397-1402.
17. Yang L., Ping Y.F., Yu X., Qian F., Guo Z.J., Qian C., Cui Y.H., Bian X.W. Gastric cancer stem-like cells possess higher capability of invasion and metastasis in association with a mesenchymal transition phenotype. Cancer Lett. 2011, 310:46-52.
18. Li H., Kolluri S.K., Gu J., Dawson M.I., Cao X., Hobbs P.D., Lin B., Chen G., Lu J., Lin F., Xie Z., Fontana J.A., Reed J.C., Zhang X. Cytochrome c release and apoptosis induced by mitochondrial targeting of nuclear orphan receptor TR3. Science 2000, 289:1159-1164.
19. Pei L., Waki H., Vaitheesvaran B., Wilpitz D.C., Kurland I.J., Tontonoz P. NR4A orphan nuclear receptors are transcriptional regulators of hepatic glucose metabolism. Nat. Med. 2006, 12:1048-1055.
20. Zhan Y., Du X., Chen H., Liu J., Zhao B., Huang D., Li G., Xu Q., Zhang M., Weimer B.C., Chen D., Cheng Z., Zhang L., Li Q., Li S., Zheng Z., Song S., Huang Y., Ye Z., Su W., Lin S.C., Shen Y., Wu Q. Cytosporone B is an agonist for nuclear orphan receptor Nur77. Nat. Chem. Biol. 2008, 4:548-556.
21. Chen H.Z., Liu Q.F., Li L., Wang W.J., Yao L.M., Yang M., Liu B., Chen W., Zhan Y.Y., Zhang M.Q., Cai J.C., Zheng Z.H., Lin S.C., Li B.A., Wu Q. The orphan receptor TR3 suppresses intestinal tumorigenesis in mice by downregulating Wnt signalling. Gut 2012, 61:714-724.
22. Liu J.J., Zeng H.N., Zhang L.R., Zhan Y.Y., Chen Y., Wang Y., Wang J., Xiang S.H., Liu W.J., Wang W.J., Chen H.Z., Shen Y.M., Su W.J., Huang P.Q., Zhang H.K., Wu Q. A unique pharmacophore for activation of the nuclear orphan receptor Nur77 in vivo and in vitro. Cancer Res. 2010, 70:3628-3637.
23. Philips A., Lesage S., Gingras R., Maira M.H., Gauthier Y., Hugo P., Drouin J. Novel dimeric Nur77 signaling mechanism in endocrine and lymphoid cells. Mol. Cell. Biol. 1997, 17:5946-5951.
24. Kolluri S.K., Bruey-Sedano N., Cao X., Lin B., Lin F., Han Y.H., Dawson M.I., Zhang X.K. Mitogenic effect of orphan receptor TR3 and its regulation by MEKK1 in lung cancer cells. Mol. Cell. Biol. 2003, 23:8651-8667.
25. Lin B., Kolluri S.K., Lin F., Liu W., Han Y.H., Cao X., Dawson M.I., Reed J.C., Zhang X.K. Conversion of Bcl-2 from protector to killer by interaction with nuclear orphan receptor Nur77/TR3. Cell 2004, 116:527-540.
26. Alexopoulou A.N., Leao M., Caballero O.L., Da S.L., Reid L., Lakhani S.R., Simpson A.J., Marshall J.F., Neville A.M., Jat P.S. Dissecting the transcriptional networks underlying breast cancer: NR4A1 reduces the migration of normal and breast cancer cell lines. Breast Cancer Res. 2010, 12:R51.
27. Thurber A.E., Douglas G., Sturm E.C., Zabierowski S.E., Smit D.J., Ramakrishnan S.N., Hacker E., Leonard J.H., Herlyn M., Sturm R.A. Inverse expression states of the BRN2 and MITF transcription factors in melanoma spheres and tumour xenografts regulate the NOTCH pathway. Oncogene 2011, 30:3036-3048.
28. Smalley K.S., Haass N.K., Brafford P.A., Lioni M., Flaherty K.T., Herlyn M. Multiple signaling pathways must be targeted to overcome drug resistance in cell lines derived from melanoma metastases. Mol. Cancer Ther. 2006, 5:1136-1144.
29. Han M., Wang Y., Liu M., Bi X., Bao J., Zeng N., Zhu Z., Mo Z., Wu C., Chen X. MiR-21 regulates epithelial-mesenchymal transition phenotype and hypoxia-inducible factor-1alpha expression in third-sphere forming breast cancer stem cell-like cells. Cancer Sci. 2012, 103:1058-1064.
30. Fillmore C.M., Kuperwasser C. Human breast cancer cell lines contain stem-like cells that self-renew, give rise to phenotypically diverse progeny and survive chemotherapy. Breast Cancer Res. 2008, 10:R25.
31. Pan G.J., Chang Z.Y., Scholer H.R., Pei D. Stem cell pluripotency and transcription factor Oct4. Cell Res. 2002, 12:321-329.
32. Chambers I., Colby D., Robertson M., Nichols J., Lee S., Tweedie S., Smith A. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 2003, 113:643-655.
33. Chiou S.H., Wang M.L., Chou Y.T., Chen C.J., Hong C.F., Hsieh W.J., Chang H.T., Chen Y.S., Lin T.W., Hsu H.S., Wu C.W. Coexpression of Oct4 and Nanog enhances malignancy in lung adenocarcinoma by inducing cancer stem cell-like properties and epithelial-mesenchymal transdifferentiation. Cancer Res. 2010, 70:10433-10444.
34. Woessner J.F. Matrix metalloproteinases and their inhibitors in connective tissue remodeling. FASEB J. 1991, 5:2145-2154.
35. Wu H., Lin Y., Li W., Sun Z., Gao W., Zhang H., Xie L., Jiang F., Qin B., Yan T., Chen L., Zhao Y., Cao X., Wu Y., Lin B., Zhou H., Wong A.S., Zhang X.K., Zeng J.Z. Regulation of Nur77 expression by beta-catenin and its mitogenic effect in colon cancer cells. FASEB J. 2011, 25:192-205.
36. Lee S.O., Abdelrahim M., Yoon K., Chintharlapalli S., Papineni S., Kim K., Wang H., Safe S. Inactivation of the orphan nuclear receptor TR3/Nur77 inhibits pancreatic cancer cell and tumor growth. Cancer Res. 2010, 70:6824-6836.
37. Bras A., Albar J.P., Leonardo E., de Buitrago G.G., Martinez A. Ceramide-induced cell death is independent of the Fas/Fas ligand pathway and is prevented by Nur77 overexpression in A20 B cells. Cell Death Differ. 2000, 7:262-271.
38. Mullican S.E., Zhang S., Konopleva M., Ruvolo V., Andreeff M., Milbrandt J., Conneely O.M. Abrogation of nuclear receptors Nr4a3 and Nr4a1 leads to development of acute myeloid leukemia. Nat. Med. 2007, 13:730-735.
39. Thiery J.P., Acloque H., Huang R.Y., Nieto M.A. Epithelial-mesenchymal transitions in development and disease. Cell 2009, 139:871-890.
40. Yang W.H., Lan H.Y., Huang C.H., Tai S.K., Tzeng C.H., Kao S.Y., Wu K.J., Hung M.C., Yang M.H. RAC1 activation mediates Twist1-induced cancer cell migration. Nat. Cell Biol. 2012, 14:366-374.
41. Siu M.K., Wong E.S., Chan H.Y., Ngan H.Y., Chan K.Y., Cheung A.N. Overexpression of NANOG in gestational trophoblastic diseases: effect on apoptosis, cell invasion, and clinical outcome. Am. J. Pathol. 2008, 173:1165-1172.
42. Pan G., Li J., Zhou Y., Zheng H., Pei D. A negative feedback loop of transcription factors that controls stem cell pluripotency and self-renewal. FASEB J. 2006, 20:1730-1732.