Indole-3-carbinol inhibits tumorigenicity of hepatocellular carcinoma cells via suppression of microRNA-21 and upregulation of phosphatase and tensin homolog

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1853, Issue 1, 2015, Pages 244-253

  Wang, Xinmei ^a   He, Hongyan ^a   Lu, Yuanzhi ^a   Ren, Wei ^b   Teng, Kun yu ^b   Chiang, Chi ling ^b   Yang, Zhaogang ^a   Yu, Bo ^a   Hsu, Shuhao ^a   Jacob, Samson T ^a,b   Ghoshal, Kalpana ^a,b   Lee, L James ^a,c  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c The Ohio State University   (United States)

Author keywords

Hepatocellular carcinoma; Indole 3 carbinol; MiR 21; MiR 221 222; PTEN

Indexed keywords

3 INDOLEMETHANOL; MICRORNA 21; MICRORNA 221; MICRORNA 222; PHOSPHATASE; PROTEIN KINASE B; TENSIN; ACTIN BINDING PROTEIN; ANTINEOPLASTIC AGENT; INDOLE DERIVATIVE; INDOLE-3-CARBINOL; MICRORNA; MIRN21 MICRORNA, HUMAN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PTEN PROTEIN, HUMAN; TENSINS;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CANCER INHIBITION; CANCER RESISTANCE; CANCER SURVIVAL; CARCINOGENICITY; CARCINOMA CELL; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; DRUG TARGETING; ENZYME REACTIVATION; FEMALE; GENE EXPRESSION; GENE REPRESSION; HEPATOCELLULAR CARCINOMA CELL LINE; HUMAN; HUMAN CELL; LIVER CELL CARCINOMA; MOUSE; NONHUMAN; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; TUMOR XENOGRAFT; UPREGULATION; WOUND HEALING; ANIMAL; ANTAGONISTS AND INHIBITORS; CARCINOMA, HEPATOCELLULAR; DRUG EFFECTS; DRUG RESISTANCE; LIVER NEOPLASMS; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANIMALS; ANTICARCINOGENIC AGENTS; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CELL PROLIFERATION; DRUG RESISTANCE, NEOPLASM; FEMALE; HUMANS; INDOLES; LIVER NEOPLASMS; MICE; MICROFILAMENT PROTEINS; MICRORNAS; PHOSPHORIC MONOESTER HYDROLASES; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; SIGNAL TRANSDUCTION;

EID: 84909992179     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2014.10.017     Document Type: Article

References (39)

1. Altekruse S.F., McGlynn K.A., Reichman M.E. Hepatocellular carcinoma incidence, mortality, and survival trends in the United States from 1975 to 2005. J. Clin. Oncol. 2009, 27:1485-1491.
2. El-Serag H.B., Rudolph K.L. Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 2007, 132:2557-2576.
3. Blum H.E. Hepatocellular carcinoma: therapy and prevention. World J. Gastroenterol. 2005, 11:7391-7400.
4. Thomas M. Molecular targeted therapy for hepatocellular carcinoma. J. Gastroenterol. 2009, 44:136-141.
5. D'Alessandro N., Poma P., Montalto G. Multifactorial nature of hepatocellular carcinoma drug resistance: could plant polyphenols be helpful?. World J. Gastroenterol. 2007, 13:2037-2043.
6. Chen K.F., Chen H.L., Tai W.T., Feng W.C., Hsu C.H., Chen P.J., Cheng A.L. Activation of phosphatidylinositol 3-kinase/Akt signaling pathway mediates acquired resistance to sorafenib in hepatocellular carcinoma cells. J. Pharmacol. Exp. Ther. 2011, 337:155-161.
7. Hu T.H., Huang C.C., Lin P.R., Chang H.W., Ger L.P., Lin Y.W., Changchien C.S., Lee C.M., Tai M.H. Expression and prognostic role of tumor suppressor gene PTEN/MMAC1/TEP1 in hepatocellular carcinoma. Cancer 2003, 97:1929-1940.
8. Nakanishi K., Sakamoto M., Yamasaki S., Todo S., Hirohashi S. Akt phosphorylation is a risk factor for early disease recurrence and poor prognosis in hepatocellular carcinoma. Cancer 2005, 103:307-312.
9. Beier R.C. Natural pesticides and bioactive components in foods. Rev. Environ. Contam. Toxicol. 1990, 113:47-137.
10. Chinni S.R., Sarkar F.H. Akt inactivation is a key event in indole-3-carbinol induced apoptosis in PC-3 cells. Clin. Cancer Res. 2002, 8:1228-1236.
11. Rahman K.M., Li Y., Sarkar F.H. Inactivation of Akt and NF-kappaB play important roles during indole-3-carbinol-induced apoptosis in breast cancer cells. Nutr. Cancer 2004, 48:84-94.
12. Weng J.R., Tsai C.H., Kulp S.K., Wang D., Lin C.H., Yang H.C., Ma Y., Sargeant A., Chiu C.F., Tsai M.H., Chen C.S. A potent indole-3-carbinol derived antitumor agent with pleiotropic effects on multiple signaling pathways in prostate cancer cells. Cancer Res. 2007, 67:7815-7824.
13. Omar H.A., Sargeant A.M., Weng J.R., Wang D., Kulp S.K., Patel T., Chen C.S. Targeting of the Akt-nuclear factor-kB signaling network by [1-(4-chloro-3-nitrobenzenesulfonyl)-1H-indol-3-yl]-methanol(OSU-A9), a novel indole-3-carbinol derivative, in a mouse model of hepatocellular carcinoma. Mol. Pharmacol. 2009, 76:957-968.
14. Takada Y., Andreeff M., Aggarwal B.B. Indole-3-carbinol suppresses NF-κB and IκBα kinase activation, causing inhibition of expression of NF-κB-regulated antiapoptotic and metastatic gene products and enhancement of apoptosis in myeloid and leukemia cells. Blood 2005, 106:2641-2649.
15. Chinni S.R., Li Y., Upadhyay S., Koppolu P.K., Sarkar F.H. Indole-3-carbinol (I3C) induced cell growth inhibition, G1 cell cycle arrest and apoptosis in prostate cancer cells. Oncogene 2001, 20:2927-2936.
16. Bell M.C., Crowley-Nowick P., Bradlow H.L., Sepkovic D.W., Schmidt-Grimminger D., Howell P., Mayeaux E.J., Tucker A., Turbat-Herrera E.A., Mathis J.M. Placebo-controlled trial of indole-3-carbinol in the treatment of CIN. Gynecol. Oncol. 2000, 78:123-129.
17. Naik R., Nixon S., Lopes A., Godfrey K., Hatem M.H., Monaghan J.M. A randomized phase II trial of indole-3-carbinol in the treatment of vulvar intraepithelial neoplasia. Int. J. Gynecol. Cancer 2006, 16:786-790.
18. Reed G.A., Peterson K.S., Smith H.J., Gray J.C., Sullivan D.K., Mayo M.S., Crowell J.A., Hurwitz A. A phase I study of indole-3-carbinol in women: tolerability and effects. Cancer Epidemiol. Biomarkers Prev. 2005, 14:1953-1960.
19. Bushati N., Cohen S.M. MicroRNA functions. Annu. Rev. Cell Dev. Biol. 2007, 23:175-205.
20. Calin G.A., Croce C.M. MicroRNA signatures in human cancer. Nat. Rev. Cancer 2006, 6:857-866.
21. Friedman J.M., Jones P.A. MicroRNAs: critical mediators of differentiation, development and disease. Swiss Med. Wkly. 2009, 139:466-472.
22. Asangani I.A., Rasheed S.A., Nikolova D.A., Leupold J.H., Colburn N.H., Post S., Allgayer H. MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene 2008, 27:2128-2136.
23. Garofalo M., Di Leva G., Romano G., Nuovo G., Suh S.S., Ngankeu A., Taccioli C., Pichiorri F., Alder H., Secchiero P., Gasparini P., Gonelli A., Costinean S., Acunzo M., Condorelli G., Croce C.M. miR-221&222 regulate TRAIL resistance and enhance tumorigenicity through PTEN and TIMP3 downregulation. Cancer Cell 2009, 16:498-509.
24. Kano M., Seki N., Kikkawa N., Fujimura L., Hoshino I., Akutsu Y., Chiyomaru T., Enokida H., Nakagawa M., Matsubara H. miR-145, miR-133a and miR-133b: tumor-suppressive miRNAs target FSCN1 in esophageal squamous cell carcinoma. Int. J. Cancer 2010, 127:2804-2814.
25. Wang B., Hsu S.H., Majumder S., Kutay H., Huang W., Jacob S.T., Ghoshal K. TGFbeta-mediated upregulation of hepatic miR-181b promotes hepatocarcinogenesis by targeting TIMP3. Oncogene 2010, 29:1787-1797.
26. Melkamu T., Zhang X., Tan J., Zeng Y., Kassie F. Alteration of microRNA expression in vinyl carbamate-induced mouse lung tumors and modulation by the chemopreventive agent indole-3-carbinol. Carcinogenesis 2010, 31:252-258.
27. Li Y., VandenBoom T.G., Kong D., Wang Z., Ali S., Philip P.A., Sarkar F.H. Up-regulation of miR-200 and let-7 by natural agents leads to the reversal of epithelial-to-mesenchymal transition in gemcitabine-resistant pancreatic cancer cells. Cancer Res. 2009, 69:6704-6712.
28. Li Y., Kong D., Ahmad A., Bao B., Dyson G., Sarkar F.H. Epigenetic deregulation of miR-29a and miR-1256 by isoflavone contributes to the inhibition of prostate cancer cell growth and invasion. Epigenetics 2012, 7:940-949.
29. Sun M., Estrov Z., Ji Y., Coombes K.R., Harris D.H., Kurzrock R. Curcumin (diferuloylmethane) alters the expression profiles of microRNAs in human pancreatic cancer cells. Mol. Cancer Ther. 2008, 7:464-473.
30. Tili E., Michaille J.J., Adair B., Alder H., Limagne E., Taccioli C., Ferracin M., Delmas D., Latruffe N., Croce C.M. Resveratrol decreases the levels of miR-155 by upregulating miR-663, a microRNA targeting JunB and JunD. Carcinogenesis 2010, 31:1561-1566.
31. Wang X., Yu B., Wu Y., Lee R.J., Lee L.J. Efficient down-regulation of CDK4 by novel lipid nanoparticle-mediated siRNA delivery. Anticancer Res. 2011, 31:1619-1626.
32. Sargeant A.M., Rengel R.C., Kulp S.K., Klein R.D., Clinton S.K., Wang Y.C., Chen C.S. OSU-HDAC42, a histone deacetylase inhibitor, blocks prostate tumor progression in the transgenic adenocarcinoma of the mouse prostate model. Cancer Res. 2008, 68:3999-4009.
33. Manning B.D., Cantley L.C. AKT/PKB signaling: navigating downstream. Cell 2007, 129:1261-1274.
34. Meng F., Henson R., Wehbe-Janek H., Ghoshal K., Jacob S.T., Patel T. MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer. Gastroenterology 2007, 133:647-658.
35. Park J.K., Kogure T., Nuovo G.J., Jiang J., He L., Kim J.H., Phelps M.A., Papenfuss T.L., Croce C.M., Patel T., Schmittgen T.D. miR-221 silencing blocks hepatocellular carcinoma and promotes survival. Cancer Res. 2011, 71:7608-7616.
36. Bai S., Nasser M.W., Wang B., Hsu S.H., Datta J., Kutay H., Yadav A., Nuovo G., Kumar P., Ghoshal K. MicroRNA-122 inhibits tumorigenic properties of hepatocellular carcinoma cells and sensitizes these cells to sorafenib. J. Biol. Chem. 2009, 284:32015-32027.
37. Kota J., Chivukula R.R., O'Donnell K.A., Wentzel E.A., Montgomery C.L., Hwang H.W., Chang T.C., Vivekanandan P., Torbenson M., Clark K.R., Mendell J.R., Mendell J.T. Therapeutic microRNA delivery suppresses tumorigenesis in a murine liver cancer model. Cell 2009, 137:1005-1017.
38. Wang B., Majumder S., Nuovo G., Kutay H., Volinia S., Patel T., Schmittgen T.D., Croce C., Ghoshal K., Jacob S.T. Role of microRNA-155 at early stages of hepatocarcinogenesis induced by choline-deficient and amino acid-defined diet in C57BL/6 mice. Hepatology 2009, 50:1152-1161.
39. Jin Y. 3,3'-Diindolylmethane inhibits breast cancer cell growth via miR-21-mediated Cdc25A degradation. Mol. Cell. Biochem. 2011, 358:345-354.