Cancer and Metastasis Reviews

, Volume 31, Issue 3–4, pp 441–454 | Cite as

Diet, nutrients, phytochemicals, and cancer metastasis suppressor genes

Article

Abstract

The major factor in the morbidity and mortality of cancer patients is metastasis. There exists a relative lack of specific therapeutic approaches to control metastasis, and this is a fruitful area for investigation. A healthy diet and lifestyle not only can inhibit tumorigenesis but also can have a major impact on cancer progression and survival. Many chemicals found in edible plants are known to inhibit metastatic progression of cancer. While the mechanisms underlying antimetastatic activity of some phytochemicals are being delineated, the impact of diet, dietary components, and various phytochemicals on metastasis suppressor genes is underexplored. Epigenetic regulation of metastasis suppressor genes promises to be a potentially important mechanism by which dietary components can impact cancer metastasis since many dietary constituents are known to modulate gene expression. The review addresses this area of research as well as the current state of knowledge regarding the impact of diet, dietary components, and phytochemicals on metastasis suppressor genes.

Keywords

Cancer Dietary Nutrients Phytochemicals Metastasis suppressor Epigenetics 

Abbreviations

BRMS

Breast cancer metastasis suppressor

CTGF

Connective tissue growth factor

DHA

Docosahexaenoic acid

DLC

Deleted in colon cancer

EGCG

Epigallocatechin-3-gallate

EGF

Epidermal growth factor

EGFR

Epidermal growth factor receptor

EPA

Eicosapentaenoic acid

IFN

Interferon

KAI1

Kangai 1

MALL

Mal-like

MAPK

Mitogen activated protein kinase

MKK

Mitogen-activated protein kinase kinase

miR

Micro RNA

NDRG

N-myc downstream-regulated gene

NM23

Nonmetastatic gene 23

PDCD

Programmed cell death

PEBP

Phosphatidylethanolamine binding protein

PTEN

Phosphatase and tensin homolog

RASSF

Ras-associated domain family

RECK

Reversion-inducing-cysteine-rich protein with kazal motifs

RhoGDI2

Rho GDP-dissociation inhibitor 2

RKIP

Raf-1 kinase inhibitor protein

SNRP

Small nucleolar ribonucleoprotein

TIMP

Tissue inhibitor of metalloproteinase

TRAMP

Transgenic adenocarcinoma of the mouse prostate

Notes

Acknowledgments

This work was supported by the NIH grants R01-AA-07293 and K05-AA-017149. The author also acknowledges the helpful suggestions and editing expertise of Kathleen Smith-Meadows.

References

  1. 1.
    Aravindaram, K., & Yang, N. S. (2010). Anti-inflammatory plant natural products for cancer therapy. Planta Medica, 76(11), 1103–1117. doi:10.1055/s-0030-1249859.PubMedGoogle Scholar
  2. 2.
    Niedzwiecki, A., Roomi, M. W., Kalinovsky, T., & Rath, M. (2010). Micronutrient synergy—a new tool in effective control of metastasis and other key mechanisms of cancer. Cancer and Metastasis Reviews, 29(3), 529–542. doi:10.1007/s10555-010-9244-1.PubMedGoogle Scholar
  3. 3.
    Chahar, M. K., Sharma, N., Dobhal, M. P., & Joshi, Y. C. (2011). Flavonoids: a versatile source of anticancer drugs. Pharmacognosy Reviews, 5(9), 1–12. doi:10.4103/0973-7847.79093PRev-5-1.PubMedGoogle Scholar
  4. 4.
    Meeran, S. M., Ahmed, A., & Tollefsbol, T. O. (2010). Epigenetic targets of bioactive dietary components for cancer prevention and therapy. Clinica Epigenetics, 1(3–4), 101–116. doi:10.1007/s13148-010-0011-5.Google Scholar
  5. 5.
    Prasad, S., Phromnoi, K., Yadav, V. R., Chaturvedi, M. M., & Aggarwal, B. B. (2010). Targeting inflammatory pathways by flavonoids for prevention and treatment of cancer. Planta Medica, 76(11), 1044–1063. doi:10.1055/s-0030-1250111.PubMedGoogle Scholar
  6. 6.
    Gupta, S. C., Kim, J. H., Prasad, S., & Aggarwal, B. B. (2010). Regulation of survival, proliferation, invasion, angiogenesis, and metastasis of tumor cells through modulation of inflammatory pathways by nutraceuticals. Cancer and Metastasis Reviews, 29(3), 405–434. doi:10.1007/s10555-010-9235-2.PubMedGoogle Scholar
  7. 7.
    Bertola, A., Deveaux, V., Bonnafous, S., Rousseau, D., Anty, R., Wakkach, A., et al. (2009). Elevated expression of osteopontin may be related to adipose tissue macrophage accumulation and liver steatosis in morbid obesity. Diabetes, 58(1), 125–133. doi:10.2337/db08-0400.PubMedGoogle Scholar
  8. 8.
    Milagro, F. I., Campion, J., Cordero, P., Goyenechea, E., Gomez-Uriz, A. M., Abete, I., et al. (2011). A dual epigenomic approach for the search of obesity biomarkers: DNA methylation in relation to diet-induced weight loss. The FASEB Journal, 25(4), 1378–1389. doi:10.1096/fj.10-170365.Google Scholar
  9. 9.
    Fernandez-Twinn, D. S., Ekizoglou, S., Martin-Gronert, M. S., Tarry-Adkins, J., Wayman, A. P., Warner, M. J., et al. (2010). Poor early growth and excessive adult calorie intake independently and additively affect mitogenic signaling and increase mammary tumor susceptibility. Carcinogenesis, 31(10), 1873–1881. doi:10.1093/carcin/bgq095.PubMedGoogle Scholar
  10. 10.
    Duthie, S. J. (2011). Epigenetic modifications and human pathologies: cancer and CVD. Proceedings of the Nutrition Society, 70(1), 47–56. doi:10.1017/S0029665110003952.PubMedGoogle Scholar
  11. 11.
    Balter, K., Moller, E., & Fondell, E. (2012). The effect of dietary guidelines on cancer risk and mortality. Current Opinion in Oncology, 24(1), 90–102. doi:10.1097/CCO.0b013e32834e053100001622-201201000-00016.PubMedGoogle Scholar
  12. 12.
    Shoushtari, A. N., Szmulewitz, R. Z., & Rinker-Schaeffer, C. W. (2011). Metastasis-suppressor genes in clinical practice: lost in translation? Nature Reviews. Clinical Oncology, 8(6), 333–342. doi:10.1038/nrclinonc.2011.65.PubMedGoogle Scholar
  13. 13.
    Stafford, L. J., Vaidya, K. S., & Welch, D. R. (2008). Metastasis suppressors genes in cancer. The International Journal of Biochemistry & Cell Biology, 40(5), 874–891. doi:10.1016/j.biocel.2007.12.016.Google Scholar
  14. 14.
    Yi, Y., Nandana, S., Case, T., Nelson, C., Radmilovic, T., Matusik, R. J., et al. (2009). Candidate metastasis suppressor genes uncovered by array comparative genomic hybridization in a mouse allograft model of prostate cancer. Molecular Cytogenetics, 2, 18. doi:10.1186/1755-8166-2-18.PubMedGoogle Scholar
  15. 15.
    Bouwman, F. G., de Roos, B., Rubio-Aliaga, I., Crosley, L. K., Duthie, S. J., Mayer, C., et al. (2011). 2D-electrophoresis and multiplex immunoassay proteomic analysis of different body fluids and cellular components reveal known and novel markers for extended fasting. BMC Medical Genomics, 4, 24. doi:10.1186/1755-8794-4-24.PubMedGoogle Scholar
  16. 16.
    Yang, M. D., Lai, K. C., Lai, T. Y., Hsu, S. C., Kuo, C. L., Yu, C. S., et al. (2010). Phenethyl isothiocyanate inhibits migration and invasion of human gastric cancer AGS cells through suppressing MAPK and NF-kappaB signal pathways. Anticancer Research, 30(6), 2135–2143.PubMedGoogle Scholar
  17. 17.
    Ho, C. C., Lai, K. C., Hsu, S. C., Kuo, C. L., Ma, C. Y., Lin, M. L., et al. (2011). Benzyl isothiocyanate (BITC) inhibits migration and invasion of human gastric cancer AGS cells via suppressing ERK signal pathways. Human and Experimental Toxicology, 30(4), 296–306. doi:10.1177/0960327110371991.PubMedGoogle Scholar
  18. 18.
    Wong, A. W., Paulson, Q. X., Hong, J., Stubbins, R. E., Poh, K., Schrader, E., et al. (2011). Alcohol promotes breast cancer cell invasion by regulating the Nm23-ITGA5 pathway. Journal of Experimental & Clinical Cancer Research, 30, 75. doi:10.1186/1756-9966-30-75.Google Scholar
  19. 19.
    Kato, K., Long, N. K., Makita, H., Toida, M., Yamashita, T., Hatakeyama, D., et al. (2008). Effects of green tea polyphenol on methylation status of RECK gene and cancer cell invasion in oral squamous cell carcinoma cells. British Journal of Cancer, 99(4), 647–654. doi:10.1038/sj.bjc.6604521.PubMedGoogle Scholar
  20. 20.
    Kushiro, K., & Nunez, N. P. (2012). Ethanol inhibits B16-BL6 melanoma metastasis and cell phenotypes associated with metastasis. In Vivo, 26(1), 47–58.PubMedGoogle Scholar
  21. 21.
    Hickson, J. A., Huo, D., Vander Griend, D. J., Lin, A., Rinker-Schaeffer, C. W., & Yamada, S. D. (2006). The p38 kinases MKK4 and MKK6 suppress metastatic colonization in human ovarian carcinoma. Cancer Research, 66(4), 2264–2270. doi:10.1158/0008-5472.CAN-05-3676.PubMedGoogle Scholar
  22. 22.
    Herner, A., Sauliunaite, D., Michalski, C. W., Erkan, M., De Oliveira, T., Abiatari, I., et al. (2011). Glutamate increases pancreatic cancer cell invasion and migration via AMPA receptor activation and Kras-MAPK signaling. International Journal of Cancer, 129(10), 2349–2359. doi:10.1002/ijc.25898.Google Scholar
  23. 23.
    Barthomeuf, C. (2007). Inhibition of S1P-induced angiogenesis, metastasis and inflammation by dietary polyphenols. Free Radical Biology & Medicine, 42(2), 312–313. doi:10.1016/j.freeradbiomed.2006.11.002.Google Scholar
  24. 24.
    Chien, S. T., Lin, S. S., Wang, C. K., Lee, Y. B., Chen, K. S., Fong, Y., et al. (2011). Acacetin inhibits the invasion and migration of human non-small cell lung cancer A549 cells by suppressing the p38alpha MAPK signaling pathway. Molecular and Cellular Biochemistry, 350(1–2), 135–148. doi:10.1007/s11010-010-0692-2.PubMedGoogle Scholar
  25. 25.
    Wang, L., Kuang, L., Pan, X., Liu, J., Wang, Q., Du, B., et al. (2010). Isoalvaxanthone inhibits colon cancer cell proliferation, migration and invasion through inactivating Rac1 and AP-1. International Journal of Cancer, 127(5), 1220–1229. doi:10.1002/ijc.25119.Google Scholar
  26. 26.
    Huang, X., Chen, S., Xu, L., Liu, Y., Deb, D. K., Platanias, L. C., et al. (2005). Genistein inhibits p38 map kinase activation, matrix metalloproteinase type 2, and cell invasion in human prostate epithelial cells. Cancer Research, 65(8), 3470–3478. doi:10.1158/0008-5472.CAN-04-2807.PubMedGoogle Scholar
  27. 27.
    Fu, Y. M., & Meadows, G. G. (2007). Specific amino acid dependency regulates the cellular behavior of melanoma. Journal of Nutrition, 137(6 Suppl 1), 1591S–1596S. discussion 1597S-1598S.PubMedGoogle Scholar
  28. 28.
    Lamy, V., Bousserouel, S., Gosse, F., Minker, C., Lobstein, A., & Raul, F. (2011). Lupulone triggers p38 MAPK-controlled activation of p53 and of the TRAIL receptor apoptotic pathway in human colon cancer-derived metastatic cells. Oncology Reports, 26(1), 109–114. doi:10.3892/or.2011.1273.PubMedGoogle Scholar
  29. 29.
    Ferguson, H. J., & Bhalerao, S. (2010). Gallbladder torsion presenting as chest pain. Annals of the Royal College of Surgeons of England, 92(3), W252–W256. doi:10.1308/147870810X12659688851357.Google Scholar
  30. 30.
    Ho, Y. T., Yang, J. S., Li, T. C., Lin, J. J., Lin, J. G., Lai, K. C., et al. (2009). Berberine suppresses in vitro migration and invasion of human SCC-4 tongue squamous cancer cells through the inhibitions of FAK, IKK, NF-kappaB, u-PA and MMP-2 and -9. Cancer Letters, 279(2), 155–162. doi:10.1016/j.canlet.2009.01.033.PubMedGoogle Scholar
  31. 31.
    Senthilkumar, K., Arunkumar, R., Elumalai, P., Sharmila, G., Gunadharini, D. N., Banudevi, S., et al. (2011). Quercetin inhibits invasion, migration and signalling molecules involved in cell survival and proliferation of prostate cancer cell line (PC-3). Cell Biochemistry and Function, 29(2), 87–95. doi:10.1002/cbf.1725.PubMedGoogle Scholar
  32. 32.
    Park, K. R., Nam, D., Yun, H. M., Lee, S. G., Jang, H. J., Sethi, G., et al. (2011). beta-Caryophyllene oxide inhibits growth and induces apoptosis through the suppression of PI3K/AKT/mTOR/S6K1 pathways and ROS-mediated MAPKs activation. Cancer Letters, 312(2), 178–188. doi:10.1016/j.canlet.2011.08.001.PubMedGoogle Scholar
  33. 33.
    Xu, L., Ding, Y., Catalona, W. J., Yang, X. J., Anderson, W. F., Jovanovic, B., et al. (2009). MEK4 function, genistein treatment, and invasion of human prostate cancer cells. Journal of the National Cancer Institute, 101(16), 1141–1155. doi:10.1093/jnci/djp227.PubMedGoogle Scholar
  34. 34.
    Meadows, G. G., Zhang, H., & Ge, X. (2001). Specific amino acid deficiency alters the expression of genes in human melanoma and other tumor cell lines. Journal of Nutrition, 131, 3047S–3050S.PubMedGoogle Scholar
  35. 35.
    Meadows, G. G., Ge, X., Zhang, H., Oros, D. R., & Fu, Y.-M. (2002). Inhibition of invasion and metastasis during specific amino acid restriction associated with metastasis suppressor and other gene changes. In D. R. Welch (Ed.), Cancer metastasis—related genes (pp. 191–208, Cancer metastasis—biology and treatment, vol. 3). Dordrecht: Kluwer Academic.Google Scholar
  36. 36.
    Abdallah, R. M., Starkey, J. R., & Meadows, G. G. (1987). Dietary restriction of tyrosine and phenylalanine: inhibition of metastasis of three rodent tumors. Journal of the National Cancer Institute, 78, 759–766.PubMedGoogle Scholar
  37. 37.
    Issa, J. P. (2008). Cancer prevention: epigenetics steps up to the plate. Cancer Prevention Research (Philadelphia, Pa.), 1(4), 219–222. doi:10.1158/1940-6207.CAPR-08-0029.Google Scholar
  38. 38.
    Herceg, Z. (2007). Epigenetics and cancer: towards an evaluation of the impact of environmental and dietary factors. Mutagenesis, 22(2), 91–103. doi:10.1093/mutage/gel068.PubMedGoogle Scholar
  39. 39.
    Szyf, M. (2006). Targeting DNA methylation in cancer. Bulletin du Cancer, 93(9), 961–972.PubMedGoogle Scholar
  40. 40.
    Parasramka, M. A., Ho, E., Williams, D. E., & Dashwood, R. H. (2012). MicroRNAs, diet, and cancer: new mechanistic insights on the epigenetic actions of phytochemicals. Molecular Carcinogenesis, 51(3), 213–230. doi:10.1002/mc.20822.PubMedGoogle Scholar
  41. 41.
    Khan, S. I., Aumsuwan, P., Khan, I. A., Walker, L. A., & Dasmahapatra, A. K. (2012). Epigenetic events associated with breast cancer and their prevention by dietary components targeting the epigenome. Chemical Research in Toxicology, 25(1), 61–73. doi:10.1021/tx200378c.PubMedGoogle Scholar
  42. 42.
    Druesne-Pecollo, N., & Latino-Martel, P. (2011). Modulation of histone acetylation by garlic sulfur compounds. Anti-Cancer Agents in Medicinal Chemistry, 11(3), 254–259.PubMedGoogle Scholar
  43. 43.
    Davis, C. D., & Ross, S. A. (2007). Dietary components impact histone modifications and cancer risk. Nutrition Reviews, 65(2), 88–94.PubMedGoogle Scholar
  44. 44.
    Chimonidou, M., Strati, A., Tzitzira, A., Sotiropoulou, G., Malamos, N., Georgoulias, V., et al. (2011). DNA methylation of tumor suppressor and metastasis suppressor genes in circulating tumor cells. Clinical Chemistry, 57(8), 1169–1177. doi:10.1373/clinchem.2011.165902.PubMedGoogle Scholar
  45. 45.
    Hartsough, M. T., Clare, S. E., Mair, M., Elkahloun, A. G., Sgroi, D., Osborne, C. K., et al. (2001). Elevation of breast carcinoma Nm23-H1 metastasis suppressor gene expression and reduced motility by DNA methylation inhibition. Cancer Research, 61(5), 2320–2327.PubMedGoogle Scholar
  46. 46.
    Li, Q., & Chen, H. (2011). Epigenetic modifications of metastasis suppressor genes in colon cancer metastasis. Epigenetics, 6(7), 849–852. doi:10.4161/epi.6.7.16314.PubMedGoogle Scholar
  47. 47.
    Desrochers, T. M., Shamis, Y., Alt-Holland, A., Kudo, Y., Takata, T., Wang, G., et al. (2012). The 3D tissue microenvironment modulates DNA methylation and E-cadherin expression in squamous cell carcinoma. Epigenetics, 7(1), 34–46. doi:10.4161/epi.7.118546.PubMedGoogle Scholar
  48. 48.
    Cebrian, V., Fierro, M., Orenes-Pinero, E., Grau, L., Moya, P., Ecke, T., et al. (2011). KISS1 methylation and expression as tumor stratification biomarkers and clinical outcome prognosticators for bladder cancer patients. American Journal of Pathology, 179(2), 540–546. doi:10.1016/j.ajpath.2011.05.009.PubMedGoogle Scholar
  49. 49.
    Lou, W., Krill, D., Dhir, R., Becich, M. J., Dong, J. T., Frierson, H. F., Jr., et al. (1999). Methylation of the CD44 metastasis suppressor gene in human prostate cancer. Cancer Research, 59(10), 2329–2331.PubMedGoogle Scholar
  50. 50.
    Shi, J., Zhang, G., Yao, D., Liu, W., Wang, N., Ji, M., et al. (2012). Prognostic significance of aberrant gene methylation in gastric cancer. American Journal of Cancer Research, 2(1), 116–129.PubMedGoogle Scholar
  51. 51.
    Zhang, Z., Sun, D., Van do, N., Tang, A., Hu, L., & Huang, G. (2007). Inactivation of RASSF2A by promoter methylation correlates with lymph node metastasis in nasopharyngeal carcinoma. International Journal of Cancer, 120(1), 32–38. doi:10.1002/ijc.22185.Google Scholar
  52. 52.
    Low, J. S., Tao, Q., Ng, K. M., Goh, H. K., Shu, X. S., Woo, W. L., et al. (2011). A novel isoform of the 8p22 tumor suppressor gene DLC1 suppresses tumor growth and is frequently silenced in multiple common tumors. Oncogene, 30(16), 1923–1935. doi:10.1038/onc.2010.576.PubMedGoogle Scholar
  53. 53.
    Kaminskyy, V. O., Surova, O. V., Vaculova, A., & Zhivotovsky, B. (2011). Combined inhibition of DNA methyltransferase and histone deacetylase restores caspase-8 expression and sensitizes SCLC cells to TRAIL. Carcinogenesis, 32(10), 1450–1458. doi:10.1093/carcin/bgr135.PubMedGoogle Scholar
  54. 54.
    Noske, A., Denkert, C., Schober, H., Sers, C., Zhumabayeva, B., Weichert, W., et al. (2005). Loss of Gelsolin expression in human ovarian carcinomas. European Journal of Cancer, 41(3), 461–469. doi:10.1016/j.ejca.2004.10.025.PubMedGoogle Scholar
  55. 55.
    Kikuchi, R., Tsuda, H., Kanai, Y., Kasamatsu, T., Sengoku, K., Hirohashi, S., et al. (2007). Promoter hypermethylation contributes to frequent inactivation of a putative conditional tumor suppressor gene connective tissue growth factor in ovarian cancer. Cancer Research, 67(15), 7095–7105. doi:10.1158/0008-5472.CAN-06-4567.PubMedGoogle Scholar
  56. 56.
    Sasahara, R. M., Brochado, S. M., Takahashi, C., Oh, J., Maria-Engler, S. S., Granjeiro, J. M., et al. (2002). Transcriptional control of the RECK metastasis/angiogenesis suppressor gene. Cancer Detection and Prevention, 26(6), 435–443.PubMedGoogle Scholar
  57. 57.
    Metge, B. J., Liu, S., Riker, A. I., Fodstad, O., Samant, R. S., & Shevde, L. A. (2010). Elevated osteopontin levels in metastatic melanoma correlate with epigenetic silencing of breast cancer metastasis suppressor 1. Oncology, 78(1), 75–86. doi:10.1159/000292363.PubMedGoogle Scholar
  58. 58.
    Aghdassi, A., Sendler, M., Guenther, A., Mayerle, J., Behn, C. O., Heidecke, C. D., et al. (2012). Recruitment of histone deacetylases HDAC1 and HDAC2 by the transcriptional repressor ZEB1 downregulates E-cadherin expression in pancreatic cancer. Gut, 61(3), 439–448. doi:10.1136/gutjnl-2011-300060.PubMedGoogle Scholar
  59. 59.
    Kim, H. R., Han, R. X., Diao, Y. F., Park, C. S., & Jin, D. I. (2011). Epigenetic characterization of the PBEF and TIMP-2 genes in the developing placentae of normal mice. BMB Reports, 44(8), 535–540.PubMedGoogle Scholar
  60. 60.
    Guan, R. J., Ford, H. L., Fu, Y., Li, Y., Shaw, L. M., & Pardee, A. B. (2000). Drg-1 as a differentiation-related, putative metastatic suppressor gene in human colon cancer. Cancer Research, 60(3), 749–755.PubMedGoogle Scholar
  61. 61.
    Mielnicki, L. M., Ying, A. M., Head, K. L., Asch, H. L., & Asch, B. B. (1999). Epigenetic regulation of gelsolin expression in human breast cancer cells. Experimental Cell Research, 249(1), 161–176. doi:10.1006/excr.1999.4461.PubMedGoogle Scholar
  62. 62.
    Qin, W., Zhu, W., Shi, H., Hewett, J. E., Ruhlen, R. L., MacDonald, R. S., et al. (2009). Soy isoflavones have an antiestrogenic effect and alter mammary promoter hypermethylation in healthy premenopausal women. Nutrition and Cancer, 61(2), 238–244. doi:10.1080/01635580802404196.PubMedGoogle Scholar
  63. 63.
    Nagao, Y., Hisaoka, M., Matsuyama, A., Kanemitsu, S., Hamada, T., Fukuyama, T., et al. (2012). Association of microRNA-21 expression with its targets, PDCD4 and TIMP3, in pancreatic ductal adenocarcinoma. Modern Pathology, 25(1), 112–121. doi:10.1038/modpathol.2011.142.PubMedGoogle Scholar
  64. 64.
    Xu, Y., Zhao, F., Wang, Z., Song, Y., Luo, Y., Zhang, X., et al. (2012). MicroRNA-335 acts as a metastasis suppressor in gastric cancer by targeting Bcl-w and specificity protein 1. Oncogene, 31(11), 1398–1407. doi:10.1038/onc.2011.340.PubMedGoogle Scholar
  65. 65.
    Song, B., Wang, C., Liu, J., Wang, X., Lv, L., Wei, L., et al. (2010). MicroRNA-21 regulates breast cancer invasion partly by targeting tissue inhibitor of metalloproteinase 3 expression. Journal of Experimental & Clinical Cancer Research, 29, 29. doi:10.1186/1756-9966-29-29.Google Scholar
  66. 66.
    Fabbri, M., & Calin, G. A. (2010). Epigenetics and miRNAs in human cancer. Advances in Genetics, 70, 87–99. doi:10.1016/B978-0-12-380866-0.60004-6.PubMedGoogle Scholar
  67. 67.
    Shah, M. S., Schwartz, S. L., Zhao, C., Davidson, L. A., Zhou, B., Lupton, J. R., et al. (2011). Integrated microRNA and mRNA expression profiling in a rat colon carcinogenesis model: effect of a chemo-protective diet. Physiological Genomics, 43(10), 640–654. doi:10.1152/physiolgenomics.00213.2010.PubMedGoogle Scholar
  68. 68.
    Ernst, A., Campos, B., Meier, J., Devens, F., Liesenberg, F., Wolter, M., et al. (2010). De-repression of CTGF via the miR-17-92 cluster upon differentiation of human glioblastoma spheroid cultures. Oncogene, 29(23), 3411–3422. doi:10.1038/onc.2010.83.PubMedGoogle Scholar
  69. 69.
    Jazbutyte, V., & Thum, T. (2010). MicroRNA-21: from cancer to cardiovascular disease. Current Drug Targets, 11(8), 926–935.PubMedGoogle Scholar
  70. 70.
    Gabriely, G., Wurdinger, T., Kesari, S., Esau, C. C., Burchard, J., Linsley, P. S., et al. (2008). MicroRNA 21 promotes glioma invasion by targeting matrix metalloproteinase regulators. Molecular and Cellular Biology, 28(17), 5369–5380. doi:10.1128/MCB.00479-08MCB.00479-08.PubMedGoogle Scholar
  71. 71.
    Grunder, E., D'Ambrosio, R., Fiaschetti, G., Abela, L., Arcaro, A., Zuzak, T., et al. (2011). MicroRNA-21 suppression impedes medulloblastoma cell migration. European Journal of Cancer, 47(16), 2479–2490. doi:10.1016/j.ejca.2011.06.041.PubMedGoogle Scholar
  72. 72.
    Yang, C. H., Yue, J., Pfeffer, S. R., Handorf, C. R., & Pfeffer, L. M. (2011). MicroRNA miR-21 regulates the metastatic behavior of B16 melanoma cells. Journal of Biological Chemistry, 286(45), 39172–39178. doi:10.1074/jbc.M111.285098.PubMedGoogle Scholar
  73. 73.
    Mudduluru, G., George-William, J. N., Muppala, S., Asangani, I. A., Kumarswamy, R., Nelson, L. D., et al. (2011). Curcumin regulates miR-21 expression and inhibits invasion and metastasis in colorectal cancer. Bioscience Reports, 31(3), 185–197. doi:10.1042/BSR20100065.PubMedGoogle Scholar
  74. 74.
    Melkamu, T., Zhang, X., Tan, J., Zeng, Y., & Kassie, F. (2010). Alteration of microRNA expression in vinyl carbamate-induced mouse lung tumors and modulation by the chemopreventive agent indole-3-carbinol. Carcinogenesis, 31(2), 252–258. doi:10.1093/carcin/bgp208.PubMedGoogle Scholar
  75. 75.
    Kushiro, K., Chu, R. A., Verma, A., & Nunez, N. P. (2011). Adipocytes Promote B16BL6 Melanoma Cell Invasion and the Epithelial-to-Mesenchymal Transition. Cancer Microenvironment. doi:10.1007/s12307-011-0087-2.
  76. 76.
    Kushiro, K., & Nunez, N. P. (2011). Ob/ob serum promotes a mesenchymal cell phenotype in B16BL6 melanoma cells. Clinical & Experimental Metastasis, 28(8), 877–886. doi:10.1007/s10585-011-9418-4.Google Scholar
  77. 77.
    Jiang, W. G., Hiscox, S., Bryce, R. P., Horrobin, D. F., & Mansel, R. E. (1998). The effects of n-6 polyunsaturated fatty acids on the expression of nm-23 in human cancer cells. British Journal of Cancer, 77(5), 731–738.PubMedGoogle Scholar
  78. 78.
    Yang, Y. M., Chen, B. Q., Zheng, Y. M., Wang, X. L., Liu, J. R., Xue, Y. B., et al. (2003). The effects of conjugated linoleic acid on the expression of invasiveness and metastasis-associated gene of human gastric carcinoma cell line. Zhonghua Yu Fang Yi Xue Za Zhi, 37(1), 26–28.PubMedGoogle Scholar
  79. 79.
    Mandal, C. C., Ghosh-Choudhury, T., Yoneda, T., Choudhury, G. G., & Ghosh-Choudhury, N. (2010). Fish oil prevents breast cancer cell metastasis to bone. Biochemical and Biophysical Research Communications, 402(4), 602–607. doi:10.1016/j.bbrc.2010.10.063.PubMedGoogle Scholar
  80. 80.
    Dimri, M., Bommi, P. V., Sahasrabuddhe, A. A., Khandekar, J. D., & Dimri, G. P. (2010). Dietary omega-3 polyunsaturated fatty acids suppress expression of EZH2 in breast cancer cells. Carcinogenesis, 31(3), 489–495. doi:10.1093/carcin/bgp305.PubMedGoogle Scholar
  81. 81.
    Joseph, J., Mudduluru, G., Antony, S., Vashistha, S., Ajitkumar, P., & Somasundaram, K. (2004). Expression profiling of sodium butyrate (NaB)-treated cells: identification of regulation of genes related to cytokine signaling and cancer metastasis by NaB. Oncogene, 23(37), 6304–6315. doi:10.1038/sj.onc.12078521207852.PubMedGoogle Scholar
  82. 82.
    Butt, A. J., Hague, A., & Paraskeva, C. (1997). Butyrate- but not TGFbeta1-induced apoptosis of colorectal adenoma cells is associated with increased expression of the differentiation markers E-cadherin and alkaline phosphatase. Cell Death and Differentiation, 4(8), 725–732. doi:10.1038/sj.cdd.4400293.PubMedGoogle Scholar
  83. 83.
    Palmer, H. G., Gonzalez-Sancho, J. M., Espada, J., Berciano, M. T., Puig, I., Baulida, J., et al. (2001). Vitamin D(3) promotes the differentiation of colon carcinoma cells by the induction of E-cadherin and the inhibition of beta-catenin signaling. The Journal of Cell Biology, 154(2), 369–387.PubMedGoogle Scholar
  84. 84.
    So, J. Y., Lee, H. J., Smolarek, A. K., Paul, S., Wang, C. X., Maehr, H., et al. (2011). A novel Gemini vitamin D analog represses the expression of a stem cell marker CD44 in breast cancer. Molecular Pharmacology, 79(3), 360–367. doi:10.1124/mol.110.068403.PubMedGoogle Scholar
  85. 85.
    Liu, H. K., Wang, Q., Li, Y., Sun, W. G., Liu, J. R., Yang, Y. M., et al. (2010). Inhibitory effects of gamma-tocotrienol on invasion and metastasis of human gastric adenocarcinoma SGC-7901 cells. The Journal of Nutritional Biochemistry, 21(3), 206–213. doi:10.1016/j.jnutbio.2008.11.004.PubMedGoogle Scholar
  86. 86.
    Hellmann, J., Rommelspacher, H., & Wernicke, C. (2009). Long-term ethanol exposure impairs neuronal differentiation of human neuroblastoma cells involving neurotrophin-mediated intracellular signaling and in particular protein kinase C. Alcoholism, Clinical and Experimental Research, 33(3), 538–550. doi:10.1111/j.1530-0277.2008.00867.x.PubMedGoogle Scholar
  87. 87.
    King, M. L., & Murphy, L. L. (2007). American ginseng (Panax quinquefolius L.) extract alters mitogen-activated protein kinase cell signaling and inhibits proliferation of MCF-7 cells. Journal of Experimental Therapeutics and Oncology, 6(2), 147–155.PubMedGoogle Scholar
  88. 88.
    Shah, D. C., Jais, P., Haissaguerre, M., Takahashi, A., & Clementy, J. (1997). Negative lead I P waves during anteroseptal accessory pathway orthodromic reciprocating tachycardia. The American Journal of Cardiology, 80(2), 227–229.PubMedGoogle Scholar
  89. 89.
    Zhou, Q., Yan, B., Hu, X., Li, X. B., Zhang, J., & Fang, J. (2009). Luteolin inhibits invasion of prostate cancer PC3 cells through E-cadherin. Molecular Cancer Therapeutics, 8(6), 1684–1691. doi:10.1158/1535-7163.MCT-09-0191.PubMedGoogle Scholar
  90. 90.
    Yang, S. F., Yang, W. E., Kuo, W. H., Chang, H. R., Chu, S. C., & Hsieh, Y. S. (2008). Antimetastatic potentials of flavones on oral cancer cell via an inhibition of matrix-degrading proteases. Archives of Oral Biology, 53(3), 287–294. doi:10.1016/j.archoralbio.2007.09.001.PubMedGoogle Scholar
  91. 91.
    Kim, J. E., Kwon, J. Y., Lee, D. E., Kang, N. J., Heo, Y. S., Lee, K. W., et al. (2009). MKK4 is a novel target for the inhibition of tumor necrosis factor-alpha-induced vascular endothelial growth factor expression by myricetin. Biochemical Pharmacology, 77(3), 412–421. doi:10.1016/j.bcp.2008.10.027.PubMedGoogle Scholar
  92. 92.
    Herzog, A., Kindermann, B., Doring, F., Daniel, H., & Wenzel, U. (2004). Pleiotropic molecular effects of the pro-apoptotic dietary constituent flavone in human colon cancer cells identified by protein and mRNA expression profiling. Proteomics, 4(8), 2455–2464. doi:10.1002/pmic.200300754.PubMedGoogle Scholar
  93. 93.
    Ullmannova, V., & Popescu, N. C. (2007). Inhibition of cell proliferation, induction of apoptosis, reactivation of DLC1, and modulation of other gene expression by dietary flavone in breast cancer cell lines. Cancer Detection and Prevention, 31(2), 11011–11018. doi:10.1016/j.cdp.2007.02.005.Google Scholar
  94. 94.
    El Touny, L. H., & Banerjee, P. P. (2007). Genistein induces the metastasis suppressor kangai-1 which mediates its anti-invasive effects in TRAMP cancer cells. Biochemical and Biophysical Research Communications, 361(1), 169–175. doi:10.1016/j.bbrc.2007.07.010.PubMedGoogle Scholar
  95. 95.
    Bao, B., Wang, Z., Ali, S., Kong, D., Li, Y., Ahmad, A., et al. (2011). Notch-1 induces epithelial-mesenchymal transition consistent with cancer stem cell phenotype in pancreatic cancer cells. Cancer Letters, 307(1), 26–36. doi:10.1016/j.canlet.2011.03.012.PubMedGoogle Scholar
  96. 96.
    Deep, G., Gangar, S. C., Agarwal, C., & Agarwal, R. (2011). Role of E-cadherin in antimigratory and antiinvasive efficacy of silibinin in prostate cancer cells. Cancer Prevention Research (Philadelphia, Pa.), 4(8), 1222–1232. doi:10.1158/1940-6207.CAPR-10-0370.Google Scholar
  97. 97.
    Kim, S., Han, J., Kim, J. S., Kim, J. H., Choe, J. H., Yang, J. H., et al. (2011). Silibinin Suppresses EGFR Ligand-induced CD44 Expression through Inhibition of EGFR Activity in Breast Cancer Cells. Anticancer Research, 31(11), 3767–3773.PubMedGoogle Scholar
  98. 98.
    Chen, P. N., Hsieh, Y. S., Chiang, C. L., Chiou, H. L., Yang, S. F., & Chu, S. C. (2006). Silibinin inhibits invasion of oral cancer cells by suppressing the MAPK pathway. Journal of Dental Research, 85(3), 220–225.PubMedGoogle Scholar
  99. 99.
    Chu, S. C., Chiou, H. L., Chen, P. N., Yang, S. F., & Hsieh, Y. S. (2004). Silibinin inhibits the invasion of human lung cancer cells via decreased productions of urokinase-plasminogen activator and matrix metalloproteinase-2. Molecular Carcinogenesis, 40(3), 143–149. doi:10.1002/mc.20018.PubMedGoogle Scholar
  100. 100.
    Momeny, M., Khorramizadeh, M. R., Ghaffari, S. H., Yousefi, M., Yekaninejad, M. S., Esmaeili, R., et al. (2008). Effects of silibinin on cell growth and invasive properties of a human hepatocellular carcinoma cell line, HepG-2, through inhibition of extracellular signal-regulated kinase 1/2 phosphorylation. European Journal of Pharmacology, 591(1–3), 13–20. doi:10.1016/j.ejphar.2008.06.011.PubMedGoogle Scholar
  101. 101.
    Kwon, G. T., Cho, H. J., Chung, W. Y., Park, K. K., Moon, A., & Park, J. H. (2009). Isoliquiritigenin inhibits migration and invasion of prostate cancer cells: possible mediation by decreased JNK/AP-1 signaling. The Journal of Nutritional Biochemistry, 20(9), 663–676. doi:10.1016/j.jnutbio.2008.06.005.PubMedGoogle Scholar
  102. 102.
    Meng, Q., Qi, M., Chen, D. Z., Yuan, R., Goldberg, I. D., Rosen, E. M., et al. (2000). Suppression of breast cancer invasion and migration by indole-3-carbinol: associated with up-regulation of BRCA1 and E-cadherin/catenin complexes. Journal of Molecular Medicine (Berlin), 78(3), 155–165.Google Scholar
  103. 103.
    Huang, C. S., Shih, M. K., Chuang, C. H., & Hu, M. L. (2005). Lycopene inhibits cell migration and invasion and upregulates Nm23-H1 in a highly invasive hepatocarcinoma, SK-Hep-1 cells. Journal of Nutrition, 135(9), 2119–2123.PubMedGoogle Scholar
  104. 104.
    Choo, E. J., Rhee, Y. H., Jeong, S. J., Lee, H. J., Kim, H. S., Ko, H. S., et al. (2011). Anethole exerts antimetatstaic activity via inhibition of matrix metalloproteinase 2/9 and AKT/mitogen-activated kinase/nuclear factor kappa B signaling pathways. Biological and Pharmaceutical Bulletin, 34(1), 41–46.PubMedGoogle Scholar
  105. 105.
    Farabegoli, F., Papi, A., & Orlandi, M. (2011). (-)-Epigallocatechin-3-gallate down-regulates EGFR, MMP-2, MMP-9 and EMMPRIN and inhibits the invasion of MCF-7 tamoxifen-resistant cells. Bioscience Reports, 31(2), 99–108. doi:10.1042/BSR20090143.PubMedGoogle Scholar
  106. 106.
    Hsu, Y. C., & Liou, Y. M. (2011). The anti-cancer effects of (-)-epigallocatechin-3-gallate on the signaling pathways associated with membrane receptors in MCF-7 cells. Journal of Cellular Physiology, 226(10), 2721–2730. doi:10.1002/jcp.22623.PubMedGoogle Scholar
  107. 107.
    O'Connell, M. A., & Rushworth, S. A. (2008). Curcumin: potential for hepatic fibrosis therapy? British Journal of Pharmacology, 153(3), 403–405. doi:10.1038/sj.bjp.0707580.PubMedGoogle Scholar
  108. 108.
    Ray, S., Chattopadhyay, N., Mitra, A., Siddiqi, M., & Chatterjee, A. (2003). Curcumin exhibits antimetastatic properties by modulating integrin receptors, collagenase activity, and expression of Nm23 and E-cadherin. Journal of Environmental Pathology, Toxicology and Oncology, 22(1), 49–58.PubMedGoogle Scholar
  109. 109.
    Yan, C., Jamaluddin, M. S., Aggarwal, B., Myers, J., & Boyd, D. D. (2005). Gene expression profiling identifies activating transcription factor 3 as a novel contributor to the proapoptotic effect of curcumin. Molecular Cancer Therapeutics, 4(2), 233–241.PubMedGoogle Scholar
  110. 110.
    Lin, H. J., Su, C. C., Lu, H. F., Yang, J. S., Hsu, S. C., Ip, S. W., et al. (2010). Curcumin blocks migration and invasion of mouse-rat hybrid retina ganglion cells (N18) through the inhibition of MMP-2, -9, FAK, Rho A and Rock-1 gene expression. Oncology Reports, 23(3), 665–670.PubMedGoogle Scholar
  111. 111.
    Wang, L., Alcon, A., Yuan, H., Ho, J., Li, Q. J., & Martins-Green, M. (2011). Cellular and molecular mechanisms of pomegranate juice-induced anti-metastatic effect on prostate cancer cells. Integrated Biology (Camb), 3(7), 742–754. doi:10.1039/c0ib00122h.Google Scholar
  112. 112.
    Huijzer, J. C., McFarland, M., Niles, R. M., & Meadows, G. G. (1996). Phorbol 12-myristate 13-acetate enhances nm23 gene expression in murine melanocytes but not in syngeneic B16-BL6 melanoma variants. Journal of Cellular Physiology, 166(3), 487–494. doi:10.1002/(SICI)1097-4652(199603)166:3<487::AID-JCP3>3.0.CO;2-L.PubMedGoogle Scholar
  113. 113.
    Krahenbuhl, S., & Reichen, J. (1992). Adaptation of mitochondrial metabolism in liver cirrhosis. Different strategies to maintain a vital function. Scandinavian Journal of Gastroenterology – Supplement, 193, 90–96.PubMedGoogle Scholar
  114. 114.
    Nagothu, K. K., Jaszewski, R., Moragoda, L., Rishi, A. K., Finkenauer, R., Tobi, M., et al. (2003). Folic acid mediated attenuation of loss of heterozygosity of DCC tumor suppressor gene in the colonic mucosa of patients with colorectal adenomas. Cancer Detection and Prevention, 27(4), 297–304.PubMedGoogle Scholar
  115. 115.
    Wang, J., Betancourt, A. M., Mobley, J. A., & Lamartiniere, C. A. (2011). Proteomic discovery of genistein action in the rat mammary gland. Journal of Proteome Research, 10(4), 1621–1631. doi:10.1021/pr100974w.PubMedGoogle Scholar
  116. 116.
    Singh, R. P., Raina, K., Sharma, G., & Agarwal, R. (2008). Silibinin inhibits established prostate tumor growth, progression, invasion, and metastasis and suppresses tumor angiogenesis and epithelial-mesenchymal transition in transgenic adenocarcinoma of the mouse prostate model mice. Clinical Cancer Research, 14(23), 7773–7780. doi:10.1158/1078-0432.CCR-08-1309.PubMedGoogle Scholar
  117. 117.
    Kim, E. J., Shin, M., Park, H., Hong, J. E., Shin, H. K., Kim, J., et al. (2009). Oral administration of 3,3′-diindolylmethane inhibits lung metastasis of 4 T1 murine mammary carcinoma cells in BALB/c mice. Journal of Nutrition, 139(12), 2373–2379. doi:10.3945/jn.109.111864.PubMedGoogle Scholar
  118. 118.
    Huang, C. S., Liao, J. W., & Hu, M. L. (2008). Lycopene inhibits experimental metastasis of human hepatoma SK-Hep-1 cells in athymic nude mice. Journal of Nutrition, 138(3), 538–543.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC (outside the USA) 2012

Authors and Affiliations

  1. 1.Department of Pharmaceutical Sciences, College of PharmacyWashington State UniversityPullmanUSA

Personalised recommendations