Luteolin reduces the invasive potential of malignant melanoma cells by targeting β3 integrin and the epithelial-mesenchymal transition

Acta Pharmacologica Sinica

Volumn 33, Issue 10, 2012, Pages 1325-1331

  Ruan, Jun Shan ^a,c   Liu, Yu Ping ^a   Zhang, Lei ^a   Yan, Ling Geng ^a   Fan, Fang Tian ^a   Shen, Cun Si ^a   Wang, Ai Yun ^a   Zheng, Shi Zhong ^a   Wang, Shao Ming ^c   Lu, Yin ^a,b  

^a NANJING UNIVERSITY OF CHINESE MEDICINE   (China)

^b Jiangsu Key Laboratory for Pharmacology and Safety Evaluation of Chinese Materia Medica   (China)

^c FUJIAN MEDICAL UNIVERSITY   (China)

Author keywords

3 integrin FAK; E cadherin; epithelial mesenchymal transition; hypoxia; luteolin; melanoma; N cadherin

Indexed keywords

BETA3 INTEGRIN; FOCAL ADHESION KINASE; LUTEOLIN; NERVE CELL ADHESION MOLECULE; UVOMORULIN; VIMENTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER INVASION; CANCER TISSUE; CELL ADHESION; CELL INVASION; CELL MOTILITY; CELL STRUCTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME INHIBITION; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; HYPOXIA; IMMUNOHISTOCHEMISTRY; LUNG METASTASIS; LUNG PARENCHYMA; MELANOMA; MELANOMA CELL; MOUSE; NONHUMAN; PROTEIN EXPRESSION; UPREGULATION; WESTERN BLOTTING;

ANIMALS; ANTINEOPLASTIC AGENTS; BLOTTING, WESTERN; CADHERINS; CELL ADHESION; CELL CULTURE TECHNIQUES; CELL HYPOXIA; CELL LINE, TUMOR; CELL MOVEMENT; DOSE-RESPONSE RELATIONSHIP, DRUG; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; IMMUNOHISTOCHEMISTRY; INTEGRIN BETA3; LUNG NEOPLASMS; LUTEOLIN; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; NEOPLASM INVASIVENESS;

EID: 84867193837     PISSN: 16714083     EISSN: 17457254     Source Type: Journal    
DOI: 10.1038/aps.2012.93     Document Type: Article

References (37)

1. Hutchinson L. Skin cancer: Novel resistance mechanism revealed. Nat Rev Clin Oncol 2012; 9: 5.
2. Berk DR, LaBuz E, Dadras SS, Johnson DL, Swetter SM. Melanoma and melanocytic tumors of uncertain malignant potential in children, adolescents and young adults-the Stanford experience 1995-2008. Pediatr Dermatol 2010; 27: 244-54.
3. Virgili G, Gatta G, Ciccolallo L, Capocaccia R, Biggeri A, Crocetti E, et al. Incidence of uveal melanoma in Europe. Ophthalmology 2007; 114: 2309-15.
4. Weir HK, Marrett LD, Cokkinides V, Barnholtz-Sloan J, Patel P, Tai E, et al. Melanoma in adolescents and young adults (ages 15-39 years): United States, 1999-2006. J Am Acad Dermatol 2011; 65: S38-49.
5. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008; 133: 704-15.
6. Dave B, Mittal V, Tan NM, Chang JC. Epithelial-mesenchymal transition, cancer stem cells and treatment resistance. Breast Cancer Res 2012; 14: 202.
7. Kushiro K, Chu RA, Verma A, Nunez NP. Adipocytes promote B16BL6 melanoma cell invasion and the epithelial-to-mesenchymal transition. Cancer Microenviron 2012; 5: 73-82.
8. Sun H, Hu K, Wu M, Xiong J, Yuan L, Tang Y, et al. Contact by melanoma cells causes malignant transformation of human epitheliallike stem cells via alpha V integrin activation of transforming growth factor beta1 signaling. Exp Biol Med (Maywood) 2011; 236: 352-65.
9. Toh B, Wang X, Keeble J, Sim WJ, Khoo K, Wong WC, et al. Mesenchymal transition and dissemination of cancer cells is driven by myeloid-derived suppressor cells infiltrating the primary tumor. PLoS Biol 2011; 9: e1001162.
10. Lin K, Baritaki S, Militello L, Malaponte G, Bevelacqua Y, Bonavida B. The role of B-RAF mutations in melanoma and the induction of EMT via dysregulation of the NF-kappaB/Snail/RKIP/PTEN circuit. Genes Cancer 2010; 1: 409-20.
11. Alonso SR, Tracey L, Ortiz P, Perez-Gomez B, Palacios J, Pollan M, et al. A high-throughput study in melanoma identifies epithelialmesenchymal transition as a major determinant of metastasis. Cancer Res 2007; 67: 3450-60.
12. Lin Y, Shi R, Wang X, Shen HM. Luteolin, a flavonoid with potential for cancer prevention and therapy. Curr Cancer Drug Targets 2008; 8: 634-46.
13. Zhou Q, Yan B, Hu X, Li XB, Zhang J, Fang J. Luteolin inhibits invasion of prostate cancer PC3 cells through E-cadherin. Mol Cancer Ther 2009; 8: 1684-91.
14. Jo M, Lester RD, Montel V, Eastman B, Takimoto S, Gonias SL. Reversibility of epithelial-mesenchymal transition (EMT) induced in breast cancer cells by activation of urokinase receptor-dependent cell signaling. J Biol Chem 2009; 284: 22825-33.
15. Chen L, Lu Y, Wu JM, Xu B, Zhang LJ, Gao M, et al. Ligustrazine inhibits B16F10 melanoma metastasis and suppresses angiogenesis induced by vascular endothelial growth factor. Biochem Biophys Res Commun 2009; 386: 374-9.
16. Chen W, Lu Y, Wu J, Gao M, Wang A, Xu B. Beta-elemene inhibits melanoma growth and metastasis via suppressing vascular endothelial growth factor-mediated angiogenesis. Cancer Chemother Pharmacol 2011; 67: 799-808.
17. Zhang LJ, Chen L, Lu Y, Wu JM, Xu B, Sun ZG, et al. Danshensu has anti-tumor activity in B16F10 melanoma by inhibiting angiogenesis and tumor cell invasion. Eur J Pharmacol 2010; 643: 195-201.
18. Jiang J, Tang YL, Liang XH. EMT: a new vision of hypoxia promoting cancer progression. Cancer Biol Ther 2011; 11: 714-23.
19. Jing Y, Han Z, Zhang S, Liu Y, Wei L. Epithelial-mesenchymal transition in tumor microenvironment. Cell Biosci 2011; 1: 29.
20. Hakomori SI. Glycosynaptic microdomains controlling tumor cell phenotype through alteration of cell growth, adhesion, and motility. FEBS Lett 2010; 584: 1901-6.
21. Rhim AD, Mirek ET, Aiello NM, Maitra A, Bailey JM, McAllister F, et al. EMT and dissemination precede pancreatic tumor formation. Cell 2012; 148: 349-61.
22. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008; 133: 704-15.
23. Nakashima S, Matsuda H, Oda Y, Nakamura S, Xu F, Yoshikawa M. Melanogenesis inhibitors from the desert plant Anastatica hierochuntica in B16 melanoma cells. Bioorg Med Chem 2010; 18: 2337-45.
24. Selvendiran K, Koga H, Ueno T, Yoshida T, Maeyama M, Torimura T, et al. Luteolin promotes degradation in signal transducer and activator of transcription 3 in human hepatoma cells: an implication for the antitumor potential of flavonoids. Cancer Res 2006; 66: 4826-34.
25. Byun S, Lee KW, Jung SK, Lee EJ, Hwang MK, Lim SH, et al. Luteolin inhibits protein kinase C(epsilon) and c-Src activities and UVB-induced skin cancer. Cancer Res 2010; 70: 2415-23.
26. Tang X, Wang H, Fan L, Wu X, Xin A, Ren H, et al. Luteolin inhibits Nrf2 leading to negative regulation of the Nrf2/ARE pathway and sensitization of human lung carcinoma A549 cells to therapeutic drugs. Free Radic Biol Med 2011; 50: 1599-609.
27. Zhou Q, Yan B, Hu X, Li XB, Zhang J, Fang J. Luteolin inhibits invasion of prostate cancer PC3 cells through E-cadherin. Mol Cancer Ther 2009; 8: 1684-91.
28. Lin YS, Tsai PH, Kandaswami CC, Cheng CH, Ke FC, Lee PP, et al. Effects of dietary flavonoids, luteolin, and quercetin on the reversal of epithelial-mesenchymal transition in A431 epidermal cancer cells. Cancer Sci 2011; 102: 1829-39.
29. Zeng R, Yao Y, Han M, Zhao X, Liu XC, Wei J, et al. Biliverdin reductase mediates hypoxia-induced EMT via PI3-kinase and Akt. J Am Soc Nephrol 2008; 19: 380-7.
30. Sumual S, Saad S, Tang O, Yong R, McGinn S, Chen XM, et al. Differential regulation of Snail by hypoxia and hyperglycemia in human proximal tubule cells. Int J Biochem Cell Biol 2010; 42: 1689-97.
31. van MH, Verslype C, Windmolders P, van ER, Nevens F, van PJ. Characterization of a cell culture model for clinically aggressive hepatocellular carcinoma induced by chronic hypoxia. Cancer Lett 2012; 315: 178-88.
32. Theys J, Jutten B, Habets R, Paesmans K, Groot AJ, Lambin P, et al. E-cadherin loss associated with EMT promotes radioresistance in human tumor cells. Radiother Oncol 2011; 99: 392-7.
33. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell 2009; 139: 871-90.
34. Rhim AD, Mirek ET, Aiello NM, Maitra A, Bailey JM, McAllister F, et al. EMT and dissemination precede pancreatic tumor formation. Cell 2012; 148: 349-61.
35. Goetz JG, Minguet S, Navarro-Lerida I, Lazcano JJ, Samaniego R, Calvo E, et al. Biomechanical remodeling of the microenvironment by stromal caveolin-1 favors tumor invasion and metastasis. Cell 2011; 146: 148-63.
36. Qian F, Vaux DL, Weissman IL. Expression of the integrin alpha 4 beta 1 on melanoma cells can inhibit the invasive stage of metastasis formation. Cell 1994; 77: 335-47.
37. Selivanova G, Ivaska J. Integrins and mutant p53 on the road to metastasis. Cell 2009; 139: 1220-2.