The Journal of Nutritional Biochemistry
Volume 20, Issue 9 , Pages 663-676 , September 2009

Isoliquiritigenin inhibits migration and invasion of prostate cancer cells: possible mediation by decreased JNK/AP-1 signaling

  • Gyoo Taik Kwon

      Affiliations

    • Department of Food Science and Nutrition, Hallym University, Chuncheon, 200-702, South Korea
    • The first two authors contributed equally to this work.
  • ,
  • Han Jin Cho

      Affiliations

    • Department of Food Science and Nutrition, Hallym University, Chuncheon, 200-702, South Korea
    • The first two authors contributed equally to this work.
  • ,
  • Won-Yoon Chung

      Affiliations

    • Department of Oral Biology, College of Dentistry, Yonsei University, Seoul, 120-752, South Korea
  • ,
  • Kwang-Kyun Park

      Affiliations

    • Department of Oral Biology, College of Dentistry, Yonsei University, Seoul, 120-752, South Korea
  • ,
  • Aree Moon

      Affiliations

    • College of Pharmacy, Duksung Women's University, Seoul, 132-714, South Korea
  • ,
  • Jung Han Yoon Park

      Affiliations

    • Department of Food Science and Nutrition, Hallym University, Chuncheon, 200-702, South Korea
    • Corresponding Author InformationCorresponding author. Tel.: +82 33 248 2134; fax: +82 33 256 0199.

Received 29 January 2008 ,Revised 24 May 2008 ,Accepted 9 June 2008.

References 

  1. Surh YJ. Cancer chemoprevention with dietary phytochemicals. Nat Rev Cancer. 2003;3:768–780
  2. Sporn MB, Suh N. Chemoprevention of cancer. Carcinogenesis. 2000;21:525–530
  3. Lippman SM, Hong WK. Cancer prevention science and practice. Cancer Res. 2002;62:5119–5125
  4. Clinton SK, Giovannucci E. Diet, nutrition, and prostate cancer. Annu Rev Nutr. 1998;18:413–440
  5. Kelloff GJ. Perspectives on cancer chemoprevention research and drug development. Adv Cancer Res. 2000;78:199–334
  6. Jemal A, Siegel R, Ward E, Murray T, Xu J, Thun MJ. Cancer statistics, 2007. CA Cancer J Clin. 2007;57:43–66
  7. Sporn MB. The war on cancer. Lancet. 1996;347:1377–1381
  8. Kelloff GJ, Lieberman R, Steele VE, Boone CW, Lubet RA, Kopelovitch L, et al. Chemoprevention of prostate cancer: concepts and strategies. Eur Urol. 1999;35:342–350
  9. Kim EJ, Park SY, Shin HK, Kwon DY, Surh YJ, Park JH. Activation of caspase-8 contributes to 3,3¢-diindolylmethane-induced apoptosis in colon cancer cells. J Nutr. 2007;137:31–36
  10. Singh RP, Agarwal R. Prostate cancer chemoprevention by silibinin: bench to bedside. Mol Carcinog. 2006;45:436–442
  11. Yamamoto S, Aizu E, Jiang H, Nakadate T, Kiyoto I, Wang JC, et al. The potent anti-tumor-promoting agent isoliquiritigenin. Carcinogenesis. 1991;12:317–323
  12. Baba M, Asano R, Takigami I, Takahashi T, Ohmura M, Okada Y, et al. Studies on cancer chemoprevention by traditional folk medicines: XXV. Inhibitory effect of isoliquiritigenin on azoxymethane-induced murine colon aberrant crypt focus formation and carcinogenesis. Biol Pharm Bull. 2002;25:247–250
  13. Yamazaki S, Morita T, Endo H, Hamamoto T, Baba M, Joichi Y, et al. Isoliquiritigenin suppresses pulmonary metastasis of mouse renal cell carcinoma. Cancer Lett. 2002;183:23–30
  14. Jung JI, Lim SS, Choi HJ, Cho HJ, Shin HK, Kim EJ, et al. Isoliquiritigenin induces apoptosis by depolarizing mitochondrial membranes in prostate cancer cells. J Nutr Biochem. 2006;17:689–696
  15. Kanazawa M, Satomi Y, Mizutani Y, Ukimura O, Kawauchi A, Sakai T, et al. Isoliquiritigenin inhibits the growth of prostate cancer. Eur Urol. 2003;43:580–586
  16. Jung JI, Chung E, Seon MR, Shin HK, Kim EJ, Lim SS, et al. Isoliquiritigenin (ISL) inhibits ErbB3 signaling in prostate cancer cells. Biofactors. 2006;28:159–168
  17. Bennett BL, Sasaki DT, Murray BW, O'Leary EC, Sakata ST, Xu W, et al. SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc Natl Acad Sci U S A. 2001;98:13681–13686
  18. Kim EJ, Holthuizen PE, Park HS, Ha YL, Jung KC, Park JHY. Trans-10,cis-12 conjugated linoleic acid inhibits Caco-2 colon cancer cell growth. Am J Physiol Gastrointest Liver Physiol. 2002;283:G357–G367
  19. Cho HJ, Kim WK, Kim EJ, Jung KC, Park S, Lee HS, et al. Conjugated linoleic acid inhibits cell proliferation and ErbB3 signaling in HT-29 human colon cell line. Am J Physiol Gastrointest Liver Physiol. 2003;284:G996–G1005
  20. Kim EJ, Kang IJ, Cho HJ, Kim WK, Ha YL, Park JH. Conjugated linoleic acid downregulates insulin-like growth factor-I receptor levels in HT-29 human colon cancer cells. J Nutr. 2003;133:2675–2681
  21. Lim DY, Tyner AL, Park JB, Lee JY, Choi YH, Park JH. Inhibition of colon cancer cell proliferation by the dietary compound conjugated linoleic acid is mediated by the CDK inhibitor p21(CIP1/WAF1). J Cell Physiol. 2005;205:107–113
  22. Culig Z, Hobisch A, Cronauer MV, Radmayr C, Trapman J, Hittmair A, et al. Androgen receptor activation in prostatic tumor cell lines by insulin-like growth factor-I, keratinocyte growth factor, and epidermal growth factor. Cancer Res. 1994;54:5474–5478
  23. Cha HJ, Bae SK, Lee HY, Lee OH, Sato H, Seiki M, et al. Anti-invasive activity of ursolic acid correlates with the reduced expression of matrix metalloproteinase-9 (MMP-9) in HT1080 human fibrosarcoma cells. Cancer Res. 1996;56:2281–2284
  24. Strongin AY, Marmer BL, Grant GA, Goldberg GI. Plasma membrane-dependent activation of the 72-kDa type IV collagenase is prevented by complex formation with TIMP-2. J Biol Chem. 1993;268:14033–14039
  25. Hackel PO, Zwick E, Prenzel N, Ullrich A. Epidermal growth factor receptors: critical mediators of multiple receptor pathways. Curr Opin Cell Biol. 1999;11:184–189
  26. Iwashita K, Kobori M, Yamaki K, Tsushida T. Flavonoids inhibit cell growth and induce apoptosis in B16 melanoma 4A5 cells. Biosci Biotechnol Biochem. 2000;64:1813–1820
  27. Maggiolini M, Statti G, Vivacqua A, Gabriele S, Rago V, Loizzo M, et al. Estrogenic and antiproliferative activities of isoliquiritigenin in MCF7 breast cancer cells. J Steroid Biochem Mol Biol. 2002;82:315–322
  28. Ma J, Fu NY, Pang DB, Wu WY, Xu AL. Apoptosis induced by isoliquiritigenin in human gastric cancer MGC-803 cells. Planta Med. 2001;67:754–757
  29. Wells A. Tumor invasion: role of growth factor-induced cell motility. Adv Cancer Res. 2000;78:31–101
  30. Kim HG, Kassis J, Souto JC, Turner T, Wells A. EGF receptor signaling in prostate morphogenesis and tumorigenesis. Histol Histopathol. 1999;14:1175–1182
  31. Di Lorenzo G, Tortora G, D'Armiento FP, De Rosa G, Staibano S, Autorino R, et al. Expression of epidermal growth factor receptor correlates with disease relapse and progression to androgen-independence in human prostate cancer. Clin Cancer Res. 2002;8:3438–3444
  32. Hegeman RB, Liu G, Wilding G, McNeel DG. Newer therapies in advanced prostate cancer. Clin Prostate Cancer. 2004;3:150–156
  33. Hernes E, Fossa SD, Berner A, Otnes B, Nesland JM. Expression of the epidermal growth factor receptor family in prostate carcinoma before and during androgen-independence. Br J Cancer. 2004;90:449–454
  34. Zellweger T, Ninck C, Bloch M, Mirlacher M, Koivisto PA, Helin HJ, et al. Expression patterns of potential therapeutic targets in prostate cancer. Int J Cancer. 2005;113:619–628
  35. Rajan R, Vanderslice R, Kapur S, Lynch J, Thompson R, Djakiew D. Epidermal growth factor (EGF) promotes chemomigration of a human prostate tumor cell line, and EGF immunoreactive proteins are present at sites of metastasis in the stroma of lymph nodes and medullary bone. Prostate. 1996;28:1–9
  36. Freeman MR, Paul S, Kaefer M, Ishikawa M, Adam RM, Renshaw AA, et al. Heparin-binding EGF-like growth factor in the human prostate: synthesis predominantly by interstitial and vascular smooth muscle cells and action as a carcinoma cell mitogen. J Cell Biochem. 1998;68:328–338
  37. Gmyrek GA, Walburg M, Webb CP, Yu HM, You X, Vaughan ED, et al. Normal and malignant prostate epithelial cells differ in their response to hepatocyte growth factor/scatter factor. Am J Pathol. 2001;159:579–590
  38. Fujiuchi Y, Nagakawa O, Murakami K, Fuse H, Saiki I. Effect of hepatocyte growth factor on invasion of prostate cancer cell lines. Oncol Rep. 2003;10:1001–1006
  39. Hurle RA, Davies G, Parr C, Mason MD, Jenkins SA, Kynaston HG, et al. Hepatocyte growth factor/scatter factor and prostate cancer: a review. Histol Histopathol. 2005;20:1339–1349
  40. Knudsen BS, Edlund M. Prostate cancer and the met hepatocyte growth factor receptor. Adv Cancer Res. 2004;91:31–67
  41. Coussens LM, Werb Z. Matrix metalloproteinases and the development of cancer. Chem Biol. 1996;3:895–904
  42. Liotta LA, Stetler-Stevenson WG. Tumor invasion and metastasis: an imbalance of positive and negative regulation. Cancer Res. 1991;51:5054s–5059s
  43. Zhang L, Shi J, Feng J, Klocker H, Lee C, Zhang J. Type IV collagenase (matrix metalloproteinase-2 and -9) in prostate cancer. Prostate Cancer Prostatic Dis. 2004;7:327–332
  44. Castellino FJ, Ploplis VA. Structure and function of the plasminogen/plasmin system. Thromb Haemost. 2005;93:647–654
  45. Kwaan HC. The plasminogen–plasmin system in malignancy. Cancer Metastasis Rev. 1992;11:291–311
  46. Brew K, Dinakarpandian D, Nagase H. Tissue inhibitors of metalloproteinases: evolution, structure and function. Biochim Biophys Acta. 2000;1477:267–283
  47. Wilhelm SM, Collier IE, Marmer BL, Eisen AZ, Grant GA, Goldberg GI. SV40-transformed human lung fibroblasts secrete a 92-kDa type IV collagenase which is identical to that secreted by normal human macrophages. J Biol Chem. 1989;264:17213–17221
  48. Stetler-Stevenson WG, Krutzsch HC, Liotta LA. Tissue inhibitor of metalloproteinase (TIMP-2). A new member of the metalloproteinase inhibitor family. J Biol Chem. 1989;264:17374–17378
  49. Chirco R, Liu XW, Jung KK, Kim HR. Novel functions of TIMPs in cell signaling. Cancer Metastasis Rev. 2006;25:99–113
  50. Soula-Rothhut M, Coissard C, Sartelet H, Boudot C, Bellon G, Martiny L, et al. The tumor suppressor PTEN inhibits EGF-induced TSP-1 and TIMP-1 expression in FTC-133 thyroid carcinoma cells. Exp Cell Res. 2005;304:187–201
  51. Joo YE, Seo KS, Kim HS, Rew JS, Park CS, Kim SJ. Expression of tissue inhibitors of metalloproteinases (TIMPs) in gastric cancer. Dig Dis Sci. 2000;45:114–121
  52. Zeng ZS, Cohen AM, Zhang ZF, Stetler-Stevenson W, Guillem JG. Elevated tissue inhibitor of metalloproteinase 1 RNA in colorectal cancer stroma correlates with lymph node and distant metastases. Clin Cancer Res. 1995;1:899–906
  53. Wu ZS, Wu Q, Yang JH, Wang HQ, Ding XD, Yang F, et al. Prognostic significance of MMP-9 and TIMP-1 serum and tissue expression in breast cancer. Int J Cancer. 2008;122:2050–2056
  54. Folkman J. Role of angiogenesis in tumor growth and metastasis. Semin Oncol. 2002;29:15–18
  55. Ferrara N, Kerbel RS. Angiogenesis as a therapeutic target. Nature. 2005;438:967–974
  56. Chevalier S, Defoy I, Lacoste J, Hamel L, Guy L, Begin LR, et al. Vascular endothelial growth factor and signaling in the prostate: more than angiogenesis. Mol Cell Endocrinol. 2002;189:169–179
  57. Eccles SA. Parallels in invasion and angiogenesis provide pivotal points for therapeutic intervention. Int J Dev Biol. 2004;48:583–598
  58. Finkenzeller G, Technau A, Marme D. Hypoxia-induced transcription of the vascular endothelial growth factor gene is independent of functional AP-1 transcription factor. Biochem Biophys Res Commun. 1995;208:432–439
  59. Cho HJ, Kang JH, Kwak JY, Lee TS, Lee IS, Park NG, et al. Ascofuranone suppresses PMA-mediated matrix metalloproteinase-9 gene activation through the Ras/Raf/MEK/ERK- and Ap1-dependent mechanisms. Carcinogenesis. 2007;28:1104–1110
  60. De Cesare D, Vallone D, Caracciolo A, Sassone-Corsi P, Nerlov C, Verde P. Heterodimerization of c-Jun with ATF-2 and c-Fos is required for positive and negative regulation of the human urokinase enhancer. Oncogene. 1995;11:365–376
  61. Zutter MM, Santoro SA, Painter AS, Tsung YL, Gafford A. The human alpha 2 integrin gene promoter. Identification of positive and negative regulatory elements important for cell-type and developmentally restricted gene expression. J Biol Chem. 1994;269:463–469
  62. Tsou TC, Yeh SC, Tsai FY, Chen JW, Chiang HC. Glutathione regulation of redox-sensitive signals in tumor necrosis factor-alpha-induced vascular endothelial dysfunction. Toxicol Appl Pharmacol. 2007;221:168–178
  63. Lee CK, Son SH, Park KK, Park JH, Lim SS, Chung WY. Isoliquiritigenin inhibits tumor growth and protects the kidney and liver against chemotherapy-induced toxicity in a mouse xenograft model of colon carcinoma. J Pharmacol Sci. 2008;106:444–451

 This work was supported by Basic Research Program of the Korea Science and Engineering Foundation (R01-2004-000-10177-0) and a grant (code number: 20070301034039) from BioGreen 21 Program, Rural Development Administration, Republic of Korea.

PII: S0955-2863(08)00138-1

doi: 10.1016/j.jnutbio.2008.06.005

The Journal of Nutritional Biochemistry
Volume 20, Issue 9 , Pages 663-676 , September 2009