Emodin inhibits vascular endothelial growth factor-A-induced angiogenesis by blocking receptor-2 (KDR/Flk-1) phosphorylation

International Journal of Cancer

Volumn 118, Issue 11, 2006, Pages 2711-2720

  Kwak, Hee Jin ^a   Park, Myung Jin ^a   Park, Chang Min ^a   Moon, Sang Ik ^a   Yoo, Doo Hyun ^a   Lee, Hyung Chahn ^a   Lee, Seung Hoon ^b   Kim, Mi Suk ^b   Lee, Hyean Woo ^c   Shin, Woon Seob ^d   Park, In Chul ^a   Rhee, Chang Hun ^a   Hong, Seok Il ^a  

^a Korea Institute of Radiation and Medical Science   (South Korea)

^b National Cancer Center   (South Korea)

^c Yonsei University Wonju College of Medicine   (South Korea)

^d Kwandong University College of Medicine   (South Korea)

Author keywords

Angiogenesis; Emodin; KDR Flk 1; Tyrosine kinase inhibitor; Vascular endothelial growth factor A

Indexed keywords

CYCLIN D1; CYCLIN E; EMODIN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; FIBROBLAST GROWTH FACTOR; GELATINASE A; MATRIGEL; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN KINASE B; RETINOBLASTOMA PROTEIN; UROKINASE RECEPTOR; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ARTICLE; CELL CYCLE ARREST; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL MIGRATION; CELL PROLIFERATION; CHICK; CHORIOALLANTOIS; CONTROLLED STUDY; DOSE RESPONSE; DRUG RECEPTOR BINDING; ENDOTHELIUM CELL; ENZYME RELEASE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PLANT ROOT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RHIZOME; RHUBARB;

BIOCOMPATIBLE MATERIALS; CELL CYCLE; CELL MOVEMENT; CELL PROLIFERATION; COLLAGEN; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG COMBINATIONS; EMODIN; ENDOTHELIAL CELLS; HUMANS; LAMININ; MICE; NEOPLASM INVASIVENESS; NEOVASCULARIZATION, PATHOLOGIC; PHOSPHORYLATION; PROTEOGLYCANS; UMBILICAL CORD; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 33646337670     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.21641     Document Type: Article

References (56)

1. Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med 1971;285:1182-86.
2. Hanahan D, Folkman J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 1996;86:353-64.
3. Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1995;1:27-31.
4. Risau W. Mechanisms of angiogenesis. Nature (Lond) 1997;386:671-74.
5. Folkman S, Chesney M, Grief. Vancouver Conference Review. AIDS Care 1997;9:39-43.
6. Bussolino F, Mantovani A, Persico G. Molecular mechanisms of blood vessel formation. Trends Biochem Sci 1997;22:251-56.
7. Inser JM, Asahara T. Angiogenesis and vasculogenesis as therapeutic strategies for postnatal neovascularization. J Clin Invest 1999;103:1231-36.
8. Ferrara N. Vascular endothelial growth factor. Eur J Cancer 1996;32:2413-22.
9. Ferrara N, Davis-Smyth T. The biology of vascular endothelial growth factor. Endocr Rev 1997;18:4-25.
10. Veikkola T, Alitalo K. VEGFs, receptors and angiogenesis. Semin Cancer Biol 1999;9:211-20.
11. McMahon G. VEGF receptor signaling in tumor angiogenesis. Oncologist 2000;5:3-10.
12. Bematchez PN, Soker S, Sirois MG. Vascular endothelial growth factor effect on endothelial cell proliferation, migration, and platelet-activating factor synthesis is Flk-1-dependent. J Biol Chem 1999;274:31047-54.
13. Davis-Smyth T, Chen H, Park J, Presta LG, Ferrara N. The second immunoglobulin-like domain of the VEGF tyrosine kinase receptor Flt-1 determines ligand binding and may initiate a signal transduction cascade. EMBO J 1996;15:4919-27.
14. Pedram A, Razandi M, Levin ER. Extracellular signal-regulated protein kinase/Jun kinase cross-talk underlies vascular endothelial cell growth factor-induced endothelial cell proliferation. J Biol Chem 1998;273:26722-28.
15. Gerber HP, McMurtrey A, Kowalski J, Yan M, Keyt BA, Dixit V, Ferrara N. Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation. J Biol Chem 1998;273:30336-43.
16. Fulton D, Gratton JP, McCabe TJ, Fontana J, Fujio Y, Walsh K, Franke TF, Papapetropoulos A, Sessa WC. Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature 1999;399:597-601.
17. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM. Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 1999;399:601-5.
18. Rousseau S, Houle F, Landry J, Huot J. p38 MAP kinase activation by vascular endothelial growth factor mediates actin reorganization and cell migration in human endothelial cells. Oncogene 1997;18:2169-77.
19. Abedi H, Zachary I. Vascular endothelial growth factor stimulates tyrosine phosphorylation and recruitment to new focal adhesions of focal adhesion kinase and paxillin in endothelial cells. J Biol Chem 1997;272:15442-51.
20. Zhang L, Hung MC. Sensitization of HER-2/neu- overexpressing non-small cell lung cancer cells to chemotherapeutic drugs by tyrosine kinase inhibitor emodin. Oncogene 1996;12:571-76.
21. Zhang L, Lau YK, Xi L, Hong RL, Kim DS, Chen CF, Hortobagyi GN, Chang C, Hung MC. Tyrosine kinase inhibitors, emodin and its derivatives repress HER-2/neu-induced cellular transformation and metastasis-associated properties. Oncogene 1998;16:2855-63.
22. Zhang L, Lau YK, Xia W, Hortobagyi GN, Hung MC. Tyrosine kinase inhibitor emodin suppresses growth of HER-2/neu-overexpressing breast cancer cells in athymic mice and sensitizes these cells to the inhibitory effect of paclitaxel. Clin Cancer Res 1999;5:343-53.
23. Kumar A, Dhawan S, Aggarwal BB. Emodin (3-methyl-1,6,8-tri- hydroxyanthraquinone) inhibits TNF-induced NF-kappaB activation, IkappaB degradation, and expression of cell surface adhesion proteins in human vascular endothelial cells. Oncogene 1998;17:913-18.
24. Drabkin DS, Ausin JH. Spectrophotometric constants for common hemoglobin derivatives in human, dog, and rabbit blood. J Biol Chem 1932;98:719.
25. Kim CW, Lee HM, Lee TH, Kang C, Kleinman HK, Gho YS. Extracellular membrane vesicles from tumor cells promote angiogenesis via sphingomyelin. Cancer Res 2002;62:6312-17.
26. Sherr CJ. D-type cyclins. Trends Biochem Sci 1995;20:187-4.
27. Stetler-Stevenson WG. Matrix metalloproteinases in angiogenesis: a moving target for therapeutic intervention. J Clin Invest 1999;103:1237-41.
28. Schnaper HW, Grant DS, Stetler-Stevenson WG, Fridman R, D'Orazi G, Murphy AN, Bird RE, Hoythya M, Fuerst TR, French DL, et al. Type IV collagenase(s) and TIMPs modulate endothelial cell morphogenesis in vitro. J Cell Physiol 1993;156:235-46.
29. Pepper MS. Role of the matrix metalloproteinase and plasminogen activator-plasmin systems in angiogenesis. Arterioscler Thromb Vasc Biol 2001;21:1104-17.
30. Meyer RD, Rahimi N. Comparative structure-function analysis of VEGFR-1 and VEGFR-2: what have we learned from chimeric systems? Ann N Y Acad Sci 2003;995:200-7.
31. Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat Med 2003;9:669-76.
32. Papapetropoulos A, Garcia-Cardena G, Madri JA, Sessa WC. Nitric oxide production contributes to the angiogenic properties of vascular endothelial growth factor in human endothelial cells. J Clin Invest 1997;100:3131-39.
33. Morbidelli L, Chang CH, Douglas JG, Granger HJ, Ledda FI, Ziche M. Nitric oxide mediates mitogenic effect of VEGF on coronary venular endothelium. Am J Physiol 1996;270:H411-H415.
34. Dimmeler S, Dernbach E, Zeiher AM. Phosphorylation of the endothelial nitric oxide synthase at ser-1177 is required for VEGF-induced endothelial cell migration. FEBS Lett 2000;477:258-62.
35. Tsai TH, Chen CF. Ultraviolet spectrum identification of emodin in rabbit plasma by HPLC and its pharmacokinetics application. Asia Pac J Pharmacol 1992;7:53-6.
36. Liang JW, Hsiu SL, Huang HC, Lee-chao PD. HPLC analysis of emodin in serum, herbs and Chinese herbal prescriptions. J Food Drug Anal 1993;1:251-57.
37. Pecere T, Gazzola MV, Mucignat C, Parolin C, Vecchia FD, Cavaggioni A, Basso G, Diaspro A, Salvato B, Carli M, Palu G. Aloe-emodin is new type of anticancer agent with selective activity against neuroectodermal tumors. Cancer Res 2000;60:2800-4.
38. Wang XH, Wu SY, Zhen YS. Inhibitory effects of emodin on angiogenesis. Yao Xue Xue Bao 2004;39:254-8.
39. Risau W. Mechanisms of angiogenesis. Nature 1997;386:671-74.
40. Mukhopadhyay A, Banerjee S, Stafford LJ, Xia C, Liu M, Aggarwal BB. Curcumin-induced suppression of cell proliferation correlates with down-regulation of cyclin D1 expression and CDK4-mediated retinoblastoma protein phosphorylation. Oncogene 2002;21:8852-61.
41. Hanai J, Dhanabal M, Karumanchi SA, Albanese C, Waterman M, Chan B, Ramchandran R, Pestell R, Sukhatme VP. Endostatin causes G1 arrest of endothelial cells through inhibition of cyclin D1. J Biol Chem 2002;277:16464-69.
42. Pepper MS. Positive and negative regulation of angiogenesis: from cell biology to the clinic. Vase Med 1996;1:259-66.
43. Kahari VM, Saarialho-Kere U. Matrix metalloproteinases and their inhibitors in tumour growth and invasion. Ann Med 1999;31:34-45.
44. Mignatti P, Rifkin DB. Biology and biochemistry of proteinases in tumor invasion. Physiol Rev 1993;73:161-95.
45. Prager GW, Breuss JM, Steurer S, Mihaly J, Binder BR. Vascular endothelial growth factor (VEGF) induces rapid prourokinase (pro-uPA) activation on the surface of endothelial cells. Blood 2003;103:955-62.
46. Pepper MS, Sappino A, Stocklin R, Montesano R, Orci L, Vassalli JD. Upregulation of urokinase receptor expression on migrating endothelial cells. J Cell Biol 1993;122:673-84.
47. Min HY, Doyle LV, Vitt CR, Zandonella CL, Stratton-Thomas JR, Shuman MA, Rosenberg S. Urokinase receptor antagonists inhibit angiogenesis and primary growth in syngeneic mice. Cancer Res 1996;56:2428-33.
48. Evans CP, Elfman F, Parangi S, Conn M, Cunha G, Shuman MA. Inhibition of prostate cancer neovascularization and growth by urokinase-plasminogen activator receptor blockade. Cancer Res 1997;57:3594-99.
49. Jayasuriya H, Koonchanok NM, Geahlen RL, McLaughlin JL, Chang CJ. Emodin, a protein tyrosine kinase inhibitor from Polygonum cuspidatum. J Nat Prod 1992;55:696-8.
50. Yim H, Lee YH, Lee CH, Lee SK. Emodin, an anthraquinone derivative isolated from the rhizomes of Rheum palmatum, selectively inhibits the activity of casein kinase II as a competitive inhibitor. Planta Med 1999;65:9-13.
51. Sarno S, Moro S, Meggio F, Zagotto G, Dal Ben D, Ghisellini P, Battistutta R, Zanotti G, Pinna LA. Toward the rational design of protein kinase casein kinase-2 inhibitors. Pharmacol Ther 2002;93:159-68.
52. Zachary I, Gliki G. Signaling transduction mechanisms mediating biological actions of the vascular endothelial growth factor family. Cardiovasc Res 2001;49:568-81.
53. Tonks NK, Neel BG. Combinatorial control of the specificity of protein tyrosine phosphatases. Curr Opin Cell Biol 2001;13:182-95.
54. Huang L, Sankar S, Lin C, Kontos CD, Schroff AD, Cha EH, Feng SM, Li SF, Yu Z, Van Etten RL, Blanar MA, Peters KG. HCPTPA, a protein tyrosine phosphatase that regulates vascular endothelial growth factor receptor-mediated signal transduction and biological activity. J Biol Chem 1999;274:38183-8.
55. Seo DW, Li H, Guedez L, Wingfield PT, Diaz T, Salloum R, Wei BY, Stetler-Stevenson WG. TIMP-2 mediated inhibition of angiogenesis: an MMP-independent mechanism. Cell 2003;114:171-80.
56. Gallicchio M, Mitola S, Valdembri D, Fantozzi R, Varnum B, Avanzi GC, Bussolino F. Inhibition of vascular endothelial growth factor receptor 2-mediated endothelial cell activation by Ax1 tyrosine kinase receptor. Blood 2005;105:1970-6.