Emodin inhibits invasion and migration of prostate and lung cancer cells by downregulating the expression of chemokine receptor CXCR4

Immunopharmacology and Immunotoxicology

Volumn 34, Issue 5, 2012, Pages 768-778

  Ok, Sooho ^a   Kim, Sung Moo ^a   Kim, Chulwon ^a   Nam, Dongwoo ^a   Shim, Bum Sang ^a   Kim, Sung Hoon ^a   Ahn, Kyoo Seok ^a   Choi, Seung Hoon ^a   Ahn, Kwang Seok ^a  

^a Kyung Hee University   (South Korea)

Author keywords

CXCL12; CXCR4; Emodin; Metastasis; NF B

Indexed keywords

8 HYDROCALAMENENE; 8,14 DIHYDROCALAMENENE; CHEMOKINE RECEPTOR CXCR4; EMODIN; EMODIN 6 GLYCINE; EPIDERMAL GROWTH FACTOR RECEPTOR 2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MW 218; MW 234; MW 270; MW 284; MW 432; PHYSCION; PROTEASOME; SYNAPTOTAGMIN I; UNCLASSIFIED DRUG;

ANTIANGIOGENIC ACTIVITY; APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL; CANCER INHIBITION; CANCER INVASION; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DOWN REGULATION; GENE TRANSLOCATION; HUMAN; HUMAN CELL; LUNG CANCER; LYSOSOME; METASTASIS; MOLECULAR STABILITY; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION;

CELL LINE, TUMOR; CELL MOVEMENT; CHEMOKINE CXCL12; DOWN-REGULATION; EMODIN; HUMANS; LUNG NEOPLASMS; MALE; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NF-KAPPA B; PROSTATIC NEOPLASMS; PROTEIN KINASE INHIBITORS; RECEPTOR, ERBB-2; RECEPTORS, CXCR4; TRANSCRIPTION, GENETIC;

EID: 84865175881     PISSN: 08923973     EISSN: 15322513     Source Type: Journal    
DOI: 10.3109/08923973.2012.654494     Document Type: Article

References (58)

1. Steeg, P.S. Metastasis suppressors alter the signal transduction of cancer cells. Nat Rev Cancer 2003, 3, 55-63
2. Richmond, A. Nf-kappa B, chemokine gene transcription and tumour growth. Nat Rev Immunol 2002, 2, 664-674
3. Balkwill, F. Cancer and the chemokine network. Nat Rev Cancer 2004, 4, 540-550
4. Kruizinga R.C.,Bestebroer J., Berghuis P., de Haas C.J.,Links T.P., de Vries E.G., Walenkamp, A.M. Role of chemokines and their receptors in cancer. Curr Pharm Des 2009, 15, 3396-3416
5. Lazennec, G., Richmond, A. Chemokines and chemokine receptors: New insights into cancer-related inflammation. Trends Mol Med 2010, 16, 133-144
6. Teicher, B.A., Fricker, S.P. CXCL12 (SDF-1)/CXCR4 pathway in cancer. Clin Cancer Res 2010, 16, 2927-2931
7. Kucia, M., Jankowski, K., Reca, R., Wysoczynski, M., Bandura, L., Allendorf, D.J., Zhang, J., Ratajczak, J., Ratajczak, M.Z. CXCR4-SDF-1 signalling, locomotion, chemotaxis and adhesion. J Mol Histol 2004, 35, 233-245
8. Kucia, M., Reca, R., Miekus, K., Wanzeck, J., Wojakowski, W., Janowska-Wieczorek, A., Ratajczak, J., Ratajczak, M.Z. Trafficking of normal stem cells and metastasis of cancer stem cells involve similar mechanisms: Pivotal role of the SDF-1-CXCR4 axis. Stem Cells 2005, 23, 879-894
9. Taichman, R.S., Cooper, C., Keller, E.T., Pienta, K.J., Taichman, N.S., McCauley, L.K. Use of the stromal cell-derived factor-1/CXCR4 pathway in prostate cancer metastasis to bone. Cancer Res 2002, 62, 1832-1837
10. Phillips, R.J., Burdick, M.D., Lutz, M., Belperio, J.A., Keane, M.P., Strieter, R.M. The stromal derived factor-1/CXCL12-CXC chemokine receptor 4 biological axis in non-small cell lung cancer metastases. Am J Respir Crit Care Med 2003, 167, 1676-1686
11. Andre, F., Cabioglu, N., Assi, H., Sabourin, J.C., Delaloge, S., Sahin, A., Broglio, K., Spano, J.P., Combadiere, C., Bucana, C., Soria, J.C., Cristofanilli, M. Expression of chemokine receptors predicts the site of metastatic relapse in patients with axillary node positive primary breast cancer. Ann Oncol 2006, 17, 945-951
12. Marchesi, F., Monti, P., Leone, B.E., Zerbi, A., Vecchi, A., Piemonti, L., Mantovani, A., Allavena, P. Increased survival, proliferation, and migration in metastati c human pancreatic tumor cells expressing functional CXCR4. Cancer Res 2004, 64, 8420-8427
13. Porcile, C., Bajetto, A., Barbero, S., Pirani, P., Schettini, G. CXCR4 activation induces epidermal growth factor receptor transactivation in an ovarian cancer cell line. Ann N Y Acad Sci 2004, 030, 162-169
14. Hernandez, P.A., Gorlin, R.J., Lukens, J.N., Taniuchi, S., Bohinjec, J., Francois, F., Klotman, M.E., Diaz, G.A. Mutations in the chemokine receptor gene CXCR4 are associated with WHIM syndrome, a combined immunodeficiency disease. Nat Genet 2003, 34, 70-74
15. Nagasawa, T., Hirota, S., Tachibana, K., Takakura, N., Nishikawa, S., Kitamura, Y., Yoshida, N., Kikutani, H., Kishimoto, T. Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature 1996, 382, 635-638
16. Knaut, H., Werz, C., Geisler, R., Nüsslein-Volhard, C.; Tübingen 2000 Screen Consortium. A zebrafish homologue of the chemokine receptor Cxcr4 is a germ-cell guidance receptor. Nature 2003, 421, 279-282
17. Kunwar, P.S., Lehmann, R. Developmental biology: Germ-cell attraction. Nature 2003, 421, 226-227
18. Connor, R.I., Sheridan, K.E., Ceradini, D., Choe, S., Landau, N.R. Change in coreceptor use correlates with disease progression in HIV-1-infected individuals. J Exp Med 1997, 185, 621-628
19. Scarlatti, G., Tresoldi, E., Björndal, A., Fredriksson, R., Colognesi, C., Deng, H.K., Malnati, M.S., Plebani, A., Siccardi, A.G., Littman, D.R., Fenyö, E.M., Lusso, P. In vivo evolution of HIV-1 co-receptor usage and sensitivity to chemokine-mediated suppression. Nat Med 1997, 3, 1259-1265
20. Li, Y.M., Pan, Y., Wei, Y., Cheng, X., Zhou, B.P., Tan, M., Zhou, X., Xia, W., Hortobagyi, G.N., Yu, D., Hung, M.C. Upregulation of CXCR4 is essential for HER2-mediated tumor metastasis. Cancer Cell 2004, 6, 459-469
21. Zeelenberg, I.S., Ruuls-Van Stalle, L., Roos, E. The chemokine receptor CXCR4 is required for outgrowth of colon carcinoma micrometastases. Cancer Res 2003, 63, 3833-3839
22. Proudfoot, A.E. Chemokine receptors: Multifaceted therapeutic targets. Nat Rev Immunol 2002, 2, 106-115
23. Goel, R.K., Das Gupta, G., Ram, S.N., Pandey, V.B. Antiulcerogenic and anti-inflammatory effects of emodin, isolated from Rhamnus triquerta wall. Indian J Exp Biol 1991, 29, 230-232
24. Kumar, A., Dhawan, S., Aggarwal, B.B. Emodin (3-methyl-1,6,8- trihydroxyanthraquinone) inhibits TNF-induced NF-kappaB activation, IkappaB degradation, and expression of cell surface adhesion proteins in human vascular endothelial cells. Oncogene 1998, 17, 913-918
25. Lin, M.L., Lu, Y.C., Chung, J.G., Li, Y.C., Wang, S.G., N.G S.H., Wu, C.Y., Su, H.L., Chen, S.S Aloe-emodin induces apoptosis of human nasopharyngeal carcinoma cells via caspase-8-mediated activation of the mitochondrial death pathway. Cancer Lett 2010, 291, 46-58
26. Ko, J.C., Su, Y.J., Lin, S.T., Jhan, J.Y., Ciou, S.C., Cheng, C.M., Lin, Y.W. Suppression of ERCC1 and Rad51 expression through ERK1/2 inactivation is essential in emodin-mediated cytotoxicity in human non-small cell lung cancer cells. Biochem Pharmacol 2010, 79, 655-664
27. Lu, G.D., Shen, H.M., Chung, M.C., Ong, C.N. Critical role of oxidative stress and sustained JNK activation in aloe-emodinmediated apoptotic cell death in human hepatoma cells. Carcinogenesis 2007, 28, 1937-1945
28. Xue, J., Ding, W., Liu, Y. Anti-diabetic effects of emodin involved in the activation of PPARgamma on high-fat diet-fed and low dose of streptozotocin-induced diabetic mice. Fitoterapia 2010, 81, 173-177
29. Lu, Y., Yang, J.H., Li, X., Hwangbo, K., Hwang, S.L., Taketomi, Y., Murakami, M., Chang, Y.C., Kim, C.H., Son, J.K., Chang, H.W. Emodin, a naturally occurring anthraquinone derivative, suppresses IgE-mediated anaphylactic reaction and mast cell activation. Biochem Pharmacol 2011, 82, 1700-1708
30. Ahn, K.S., Sethi, G., Chao, T.H., Neuteboom, S.T., Chaturvedi, M.M., Palladino, M.A., Younes, A., Aggarwal, B.B. Salinosporamide A (NPI-0052) potentiates apoptosis, suppresses osteoclastogenesis, and inhibits invasion through down-modulation of NF-kappaB regulated gene products. Blood 2007, 110, 2286-2295
31. Su, Y.T., Chang, H.L., Shyue, S.K., Hsu, S.L. Emodin induces apoptosis in human lung adenocarcinoma cells through a reactive oxygen species-dependent mitochondrial signaling pathway. Biochem Pharmacol 2005, 70, 229-241
32. Chen, R.S., Jhan, J.Y., Su, Y.J., Lee, W.T., Cheng, C.M., Ciou, S.C., Lin, S.T., Chuang, S.M., Ko, J.C., Lin, Y.W. Emodin enhances gefitinib-induced cytotoxicity via Rad51 downregulation and ERK1/2 inactivation. Exp Cell Res 2009, 315, 2658-2672
33. Su, Y.J., Tsai, M.S., Kuo, Y.H., Chiu, Y.F., Cheng, C.M., Lin, S.T., Lin, Y.W. Role of Rad51 down-regulation and extracellular signalregulated kinases 1 and 2 inactivation in emodin and mitomycin C-induced synergistic cytotoxicity in human non-small-cell lung cancer cells. Mol Pharmacol 2010, 77, 633-643
34. Fernandis, A.Z., Prasad, A., Band, H., Klösel, R., Ganju, R.K. Regulation of CXCR4-mediated chemotaxis and chemoinvasion of breast cancer cells. Oncogene 2004, 23, 157-167
35. Chinni, S.R., Yamamoto, H., Dong, Z., Sabbota, A., Bonfil, R.D., Cher, M.L. CXCL12/CXCR4 transactivates HER2 in lipid rafts of prostate cancer cells and promotes growth of metastatic deposits in bone. Mol Cancer Res 2008, 6, 446-457
36. Gangadhar, T., Nandi, S., Salgia, R. The role of chemokine receptor CXCR4 in lung cancer. Cancer Biol Ther 2010, 9, 409-416
37. Marchese, A., Benovic, J.L. Agonist-promoted ubiquitination of the G protein-coupled receptor CXCR4 mediates lysosomal sorting. J Biol Chem 2001, 276, 45509-45512
38. Bhandari, D., Trejo, J., Benovic, J.L., Marchese, A. Arrestin-2 interacts with the ubiquitin-protein isopeptide ligase atrophininteracting protein 4 and mediates endosomal sorting of the chemokine receptor CXCR4. J Biol Chem 2007, 282, 36971-36979
39. Kukreja, P., Abdel-Mageed, A.B., Mondal, D., Liu, K., Agrawal, K.C. Up-regulation of CXCR4 expression in PC-3 cells by stromalderived factor-1alpha (CXCL12) increases endothelial adhesion and transendothelial migration: Role of MEK/ERK signaling pathway-dependent NF-kappaB activation. Cancer Res 2005, 65, 9891-9898
40. Shanmugam, M.K., Rajendran, P., Li, F., Nema, T., Vali, S., Abbasi, T., Kapoor, S., Sharma, A., Kumar, A.P., Ho, P.C., Hui, K.M., Sethi, G. Ursolic acid inhibits multiple cell survival pathways leading to suppression of growth of prostate cancer xenograft in nude mice. J Mol Med 2011, 89, 713-727
41. Lee, B.C., Lee, T.H., Avraham, S., Avraham, H.K. Involvement of the chemokine receptor CXCR4 and its ligand stromal cell-derived factor 1alpha in breast cancer cell migration through human brain microvascular endothelial cells. Mol Cancer Res 2004, 2, 327-338
42. Murphy, P.M. Chemokines and the molecular basis of cancer metastasis. N Engl J Med 2001, 345, 833-835
43. Uchida, D., Begum, N.M., Almofti, A., Nakashiro, K., Kawamata, H., Tateishi, Y., Hamakawa, H., Yoshida, H., Sato, M. Possible role of stromal-cell-derived factor-1/CXCR4 signaling on lymph node metastasis of oral squamous cell carcinoma. Exp Cell Res 2003, 290, 289-302
44. Gschwind, A., Prenzel, N., Ullrich, A. Lysophosphatidic acidinduced squamous cell carcinoma cell proliferation and motility involves epidermal growth factor receptor signal transactivation. Cancer Res 2002, 62, 6329-6336
45. Schioppa, T., Uranchimeg, B., Saccani, A., Biswas, S.K., Doni, A., Rapisarda, A., Bernasconi, S., Saccani, S., Nebuloni, M., Vago, L., Mantovani, A., Melillo, G., Sica, A. Regulation of the chemokine receptor CXCR4 by hypoxia. J Exp Med 2003, 198, 1391-1402
46. Helbig, G., Christopherson, K.W., 2nd, Bhat-Nakshatri, P., Kumar, S., Kishimoto, H., Miller, K.D., Broxmeyer, H.E., Nakshatri, H. NF-kappaB promotes breast cancer cell migration and metastasis by inducing the expression of the chemokine receptor CXCR4. J Biol Chem 2003, 278, 21631-21638
47. Bachelder, R.E., Wendt, M.A., Mercurio, A.M. Vascular endothelial growth factor promotes breast carcinoma invasion in an autocrine manner by regulating the chemokine receptor CXCR4. Cancer Res 2002, 62, 7203-7206
48. Castellone, M.D., Guarino, V., De Falco, V., Carlomagno, F., Basolo, F., Faviana, P., Kruhoffer, M., Orntoft, T., Russell, J.P., Rothstein, J.L., Fusco, A., Santoro, M., Melillo, R.M. Functional expression of the CXCR4 chemokine receptor is induced by RET/PTC oncogenes and is a common event in human papillary thyroid carcinomas. Oncogene 2004, 23, 5958-5967
49. Tomescu, O., Xia, S.J., Strezlecki, D., Bennicelli, J.L., Ginsberg, J., Pawel, B., Barr, F.G. Inducible short-term and stable long-term cell culture systems reveal that the PAX3-FKHR fusion oncoprotein regulates CXCR4, PAX3, and PAX7 expression. Lab Invest 2004, 84, 1060-1070
50. Roes, J., Choi, B.K., Cazac, B.B. Redirection of B cell responsiveness by transforming growth factor beta receptor. Proc Natl Acad Sci USA 2003, 100, 7241-7246
51. Staller, P., Sulitkova, J., Lisztwan, J., Moch, H., Oakeley, E.J., Krek, W. Chemokine receptor CXCR4 downregulated by von Hippel-Lindau tumour suppressor pVHL. Nature 2003, 425, 307-311
52. Zhou, B.P., Hu, M.C., Miller, S.A., Yu, Z., Xia, W., Lin, S.Y., Hung, M.C. HER-2/neu blocks tumor necrosis factor-induced apoptosis via the Akt/NF-kappaB pathway. J Biol Chem 2000, 275, 8027-8031
53. Huang, Q., Shen, H.M., Ong, C.N. Inhibitory effect of emodin on tumor invasion through suppression of activator protein-1 and nuclear factor-kappaB. Biochem Pharmacol 2004, 68, 361-371
54. Cabioglu, N., Sahin, A., Doucet, M., Yavuz, E., Igci, A., O Yildirim, E., Aktas, E., Bilgic, S., Kiran, B., Deniz, G., Price, J.E. Chemokine receptor CXCR4 expression in breast cancer as a potential predictive marker of isolated tumor cells in bone marrow. Clin Exp Metastasis 2005, 22, 39-46
55. Kang, H., Watkins, G., Douglas-Jones, A., Mansel, R.E., Jiang, W.G. The elevated level of CXCR4 is correlated with nodal metastasis of human breast cancer. Breast 2005, 14, 360-367
56. Jung, S.J., Kim, C.I., Park, C.H., Chang, H.S., Kim, B.H., Choi, M.S., Jung, H.R. Correlation between Chemokine Receptor CXCR4 Expression and Prognostic Factors in Patients with Prostate Cancer. Korean J Urol 2011, 52, 607-611
57. Otsuka, S., Klimowicz, A.C., Kopciuk, K., Petrillo, S.K., Konno, M., Hao, D., Muzik, H., Stolte, E., Boland, W., Morris, D., Magliocco, A.M., Bebb, D.G. CXCR4 overexpression is associated with poor outcome in females diagnosed with stage IV non-small cell lung cancer. J Thorac Oncol 2011, 6, 1169-1178
58. Chun-Guang, W., Jun-Qing, Y., Bei-Zhong, L., Dan-Ting, J., Chong, W., Liang, Z., Dan, Z., Yan, W. Anti-tumor activity of emodin against human chronic myelocytic leukemia K562 cell lines in vitro and in vivo. Eur J Pharmacol 2010, 627, 33-41