The chemopreventive agent ursodeoxycholic acid inhibits proliferation of colon carcinoma cells by suppressing c-Myc expression

European Journal of Cancer Prevention

Volumn 21, Issue 5, 2012, Pages 413-422

  Peiró Jordán, Roser ^a,b   Krishna Subramanian, Santosh ^a   Hanski, Marie Luise ^a   Lüscher Firzlaff, Juliane ^c   Zeitz, Martin ^a   Hanski, Christoph ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

^c UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

Author keywords

c Myc; CDK4; CDK6; cell cycle; inhibition of proliferation; ursodeoxycholic acid

Indexed keywords

CYCLIN DEPENDENT KINASE 4; CYCLIN DEPENDENT KINASE 6; MYC PROTEIN; URSODEOXYCHOLIC ACID;

APOPTOSIS; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CARCINOMA CELL; CELL CYCLE G1 PHASE; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CELL POPULATION; CELL PROLIFERATION; COLON CANCER; COLON CARCINOMA; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SENESCENCE;

ANTINEOPLASTIC AGENTS; CARCINOMA; CELL LINE, TUMOR; CELL PROLIFERATION; COLONIC NEOPLASMS; HCT116 CELLS; HUMANS; PROTO-ONCOGENE PROTEINS C-MYC; URSODEOXYCHOLIC ACID;

EID: 84864371886     PISSN: 09598278     EISSN: 14735709     Source Type: Journal    
DOI: 10.1097/CEJ.0b013e32834ef16f     Document Type: Article

References (40)

1. Akare S, Jean-Louis S, Chen W, Wood DJ, Powell AA, Martinez JD (2006). Ursodeoxycholic acid modulates histone acetylation and induces differentiation and senescence. Int J Cancer 119:2958-2969. (Pubitemid 44846251)
2. Alberts DS, Martinez ME, Hess LM, Einspahr JG, Green SB, Bhattacharyya AK, et al. (2005). Phase III trial of ursodeoxycholic acid to prevent colorectal adenoma recurrence. J Natl Cancer Inst 97:846-853. (Pubitemid 40909127)
3. Brabletz T, Herrmann K, Jung A, Faller G, Kirchner T (2000). Expression of nuclear beta-catenin and c-myc is correlated with tumor size but not with proliferative activity of colorectal adenomas. Am J Pathol 156:865-870. (Pubitemid 30626945)
4. Claassen GF, Hann SR (2000). A role for transcriptional repression of p21CIP1 by c-Myc in overcoming transforming growth factor beta-induced cell-cycle arrest. Proc Natl Acad Sci USA 97:9498-9503. (Pubitemid 30650804)
5. D'Orazio D, Muller PY, Heinimann K, Albrecht C, Bendik I, Herzog U, et al. (2002). Overexpression of Wnt target genes in adenomas of familial adenomatous polyposis patients. Anticancer Res 22:3409-3414. (Pubitemid 36070122)
6. Feldman R, Martinez JD (2009). Growth suppression by ursodeoxycholic acid involves caveolin-1 enhanced degradation of EGFR. Biochim Biophys Acta 1793:1387-1394.
7. Gartel AL, Ye X, Goufman E, Shianov P, Hay N, Najmabadi F, Tyner AL (2001). Myc represses the p21(WAF1/CIP1) promoter and interacts with Sp1/Sp3. Proc Natl Acad Sci USA 98:4510-4515. (Pubitemid 32295007)
8. Geltinger C, Hortnagel K, Polack A (1996). TATA box and Sp1 sites mediate the activation of c-myc promoter P1 by immunoglobulin kappa enhancers. Gene Expr 6:113-127.
9. Grandori C, Cowley SM, James LP, Eisenman RN (2000). The Myc/Max/Mad network and the transcriptional control of cell behavior. Annu Rev Cell Dev Biol 16:653-699. (Pubitemid 32037520)
10. Hermeking H, Rago C, Schuhmacher M, Li Q, Barrett JF, Obaya AJ, et al. (2000). Identification of CDK4 as a target of c-MYC. Proc Natl Acad Sci USA 97:2229-2234. (Pubitemid 30134051)
11. Hirose Y, Berger MS, Pieper RO (2001). p53 effects both the duration of G2/M arrest and the fate of temozolomide-treated human glioblastoma cells. Cancer Res 61:1957-1963. (Pubitemid 32692013)
12. Ifandi V, Al-Rubeai M (2003). Stable transfection of CHO cells with the c-myc gene results in increased proliferation rates, reduces serum dependency, and induces anchorage independence. Cytotechnology 41:1-10. (Pubitemid 36875117)
13. Im E, Martinez JD (2004). Ursodeoxycholic acid (UDCA) can inhibit deoxycholic acid (DCA)-induced apoptosis via modulation of EGFR/Raf-1/ERK signaling in human colon cancer cells. J Nutr 134:483-486. (Pubitemid 38141837)
14. Jeong JH, Kang SS, Park KK, Chang HW, Magae J, Chang YC (2010). p53-independent induction of G1 arrest and p21WAF1/CIP1 expression by ascofuranone, an isoprenoid antibiotic, through downregulation of c-Myc. Mol Cancer Ther 9:2102-2113.
15. Kamemura K, Hayes BK, Comer FI, Hart GW (2002). Dynamic interplay between O-glycosylation and O-phosphorylation of nucleocytoplasmic proteins: alternative glycosylation/phosphorylation of THR-58, a known mutational hot spot of c-Myc in lymphomas, is regulated by mitogens. J Biol Chem 277:19229-19235. (Pubitemid 34952491)
16. Kohno H, Suzuki R, Yasui Y, Miyamoto S, Wakabayashi K, Tanaka T (2007). Ursodeoxycholic acid versus sulfasalazine in colitis-related colon carcinogen-esis in mice. Clin Cancer Res 13:2519-2525. (Pubitemid 46698605)
17. Krishna-Subramanian S, Hanski ML, Loddenkemper C, Choudhary B, Pages G, Zeitz M, Hanski C. UDCA slows down intestinal cell proliferation by inducing high and sustained ERK phosphorylation. Int J Cancer, published online 2011.
18. Lee SH, Hu LL, Gonzalez-Navajas J, Seo GS, Shen C, Brick J, et al. (2010). ERK activation drives intestinal tumorigenesis in Apc(min/+) mice. Nat Med 16:665-670.
19. Loddenkemper C, Keller S, Hanski ML, Cao M, Jahreis G, Stein H, et al. (2006). Prevention of colitis-associated carcinogenesis in a mouse model by diet supplementation with ursodeoxycholic acid. Int J Cancer 118:2750-2757. (Pubitemid 43673353)
20. Miura T, Ouchida R, Yoshikawa N, Okamoto K, Makino Y, Nakamura T, et al. (2001). Functional modulation of the glucocorticoid receptor and suppression of NF-kappaB-dependent transcription by ursodeoxycholic acid. J Biol Chem 276:47371-47378.
21. Mori H, Yamada Y, Hirose Y, Kuno T, Katayama M, Sakata K, et al. (2002). Chemoprevention of large bowel carcinogenesis; the role of control of cell proliferation and significance of beta-catenin-accumulated crypts as a new biomarker. Eur J Cancer Prev 11 (Suppl 2):S71-S75. (Pubitemid 35265866)
22. Mukherjee S, Conrad SE (2005). c-Myc suppresses p21WAF1/CIP1 expression during estrogen signaling and antiestrogen resistance in human breast cancer cells. J Biol Chem 280:17617-17625. (Pubitemid 41388996)
23. Navarro F, Gutman D, Meire E, Caceres M, Rigoutsos I, Bentwich Z, Lieberman J (2009). miR-34a contributes to megakaryocytic differentiation of K562 cells independently of p53. Blood 114:2181-2192.
24. Orian A, van Steensel B, Delrow J, Bussemaker HJ, Li L, Sawado T, et al. (2003). Genomic binding by the Drosophila Myc, Max, Mad/Mnt transcription factor network. Genes Dev 17:1101-1114. (Pubitemid 36534985)
25. Pardi DS, Loftus EV Jr, Kremers WK, Keach J, Lindor KD (2003). Ursodeoxycholic acid as a chemopreventive agent in patients with ulcerative colitis and primary sclerosing cholangitis. Gastroenterology 124:889-893. (Pubitemid 36389790)
26. Rivadeneira DB, Mayhew CN, Thangavel C, Sotillo E, Reed CA, Grana X, Knudsen ES (2010). Proliferative suppression by CDK4/6 inhibition: complex function of the retinoblastoma pathway in liver tissue and hepatoma cells. Gastroenterology 138:1920-1930.
27. Sato S, Fujita N, Tsuruo T (2002). Interference with PDK1-Akt survival signaling pathway by UCN-01 (7-hydroxystaurosporine). Oncogene 21:1727-1738. (Pubitemid 34259036)
28. Sears RC (2004). The life cycle of C-myc: from synthesis to degradation. Cell Cycle 3:1133-1137. (Pubitemid 40268631)
29. Seoane J, Le HV, Massague J (2002). Myc suppression of the p21(Cip1) Cdk inhibitor influences the outcome of the p53 response to DNA damage. Nature 419:729-734. (Pubitemid 35177959)
30. Serfaty L, De Leusse A, Rosmorduc O, Desaint B, Flejou JF, Chazouilleres O, et al. (2003). Ursodeoxycholic acid therapy and the risk of colorectal adenoma in patients with primary biliary cirrhosis: an observational study. Hepatology 38:203-209. (Pubitemid 36775812)
31. Shah SA, Volkov Y, Arfin Q, Abdel-Latif MM, Kelleher D (2006). Ursodeoxycholic acid inhibits interleukin 1 beta corrected and deoxycholic acid-induced activation of NF-kappaB and AP-1 in human colon cancer cells. Int J Cancer 118:532-539. (Pubitemid 43076000)
32. Sherr CJ, Roberts JM (1999). CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev 13:1501-1512. (Pubitemid 29297917)
33. Shiraki K, Ito T, Sugimoto K, Fuke H, Inoue T, Miyashita K, et al. (2005). Different effects of bile acids, ursodeoxycholic acid and deoxycholic acid, on cell growth and cell death in human colonic adenocarcinoma cells. Int J Mol Med 16:729-733.
34. Sjoqvist U, Tribukait B, Ost A, Einarsson C, Oxelmark L, Lofberg R (2004). Ursodeoxycholic acid treatment in IBD-patients with colorectal dysplasia and/or DNA-aneuploidy: a prospective, double-blind, randomized controlled pilot study. Anticancer Res 24:3121-3127. (Pubitemid 39390961)
35. Tetsu O, McCormick F (2003). Proliferation of cancer cells despite CDK2 inhibition. Cancer Cell 3:233-245. (Pubitemid 37443879)
36. Tung BY, Emond MJ, Haggitt RC, Bronner MP, Kimmey MB, Kowdley KV, Brentnall TA (2001). Ursodiol use is associated with lower prevalence of colonic neoplasia in patients with ulcerative colitis and primary sclerosing cholangitis. Ann Intern Med 134:89-95. (Pubitemid 32096335)
37. Wali RK, Khare S, Tretiakova M, Cohen G, Nguyen L, Hart J, et al. (2002a). Ursodeoxycholic acid and F(6)-D(3) inhibit aberrant crypt proliferation in the rat azoxymethane model of colon cancer: roles of cyclin D1 and E-cadherin. Cancer Epidemiol Biomarkers Prev 11:1653-1662. (Pubitemid 36020020)
38. Wali RK, Stoiber D, Nguyen L, Hart J, Sitrin MD, Brasitus T, Bissonnette M (2002b). Ursodeoxycholic acid inhibits the initiation and postinitiation phases of azoxymethane-induced colonic tumor development. Cancer Epidemiol Biomarkers Prev 11:1316-1321. (Pubitemid 35340366)
39. Wang H, Mannava S, Grachtchouk V, Zhuang D, Soengas MS, Gudkov AV, et al. (2008). c-Myc depletion inhibits proliferation of human tumor cells at various stages of the cell cycle. Oncogene 27:1905-1915. (Pubitemid 351430817)
40. Wu CH, van Riggelen J, Yetil A, Fan AC, Bachireddy P, Felsher DW (2007). Cellular senescence is an important mechanism of tumor regression upon c-Myc inactivation. Proc Natl Acad Sci USA 104:13028-13033. (Pubitemid 351737587)