Gambogic acid inhibits tumor cell adhesion by suppressing integrin β1 and membrane lipid rafts-associated integrin signaling pathway

Biochemical Pharmacology

Volumn 82, Issue 12, 2011, Pages 1873-1883

  Li, Chenglin ^a   Lu, Na ^a   Qi, Qi ^b   Li, Fanni ^a   Ling, Yun ^a   Chen, Yan ^a   Qin, Yansu ^a   Li, Zhiyu ^a   Zhang, Haiwei ^a   You, Qidong ^a   Guo, Qinglong ^a,c  

^a CHINA PHARMACEUTICAL UNIVERSITY   (China)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c China Pharmaceutical University   (China)

Author keywords

Adhesion; Cholesterol; Gambogic acid; Integrin 1; Lipid raft

Indexed keywords

ACETYL COENZYME A ACETYLTRANSFERASE; BETA1 INTEGRIN; CHOLESTEROL; FIBRONECTIN; GAMBOGIC ACID; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; MESSENGER RNA; STEROL REGULATORY ELEMENT BINDING PROTEIN 2;

ANTINEOPLASTIC ACTIVITY; ARTICLE; AUTOPHOSPHORYLATION; BREAST CARCINOMA; CANCER CELL; CELL ADHESION; COMPETITIVE INHIBITION; CONTROLLED STUDY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IN VITRO STUDY; LIPID RAFT; LIVER CELL CARCINOMA; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

ANTIGENS, CD29; ANTINEOPLASTIC AGENTS; CELL ADHESION; CELL LINE, TUMOR; CHOLESTEROL; FIBRONECTINS; FOCAL ADHESIONS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MEMBRANE MICRODOMAINS; MOLECULAR STRUCTURE; SIGNAL TRANSDUCTION; XANTHONES;

EID: 80555131105     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2011.09.013     Document Type: Article

References (59)

1. T. Bogenrieder, and M. Herlyn Axis of evil: molecular mechanisms of cancer metastasis Oncogene 22 2003 6524 6536 (Pubitemid 37372332)
2. V. Ellenrieder, G. Adler, and T.M. Gress Invasion and metastasis in pancreatic cancer Ann Oncol 10 Suppl. 4 1999 46 50
3. C. Zhang, Y. Liu, Y. Gao, J. Shen, S. Zheng, and M. Wei Modified heparins inhibit integrin alpha(IIb)beta(3) mediated adhesion of melanoma cells to platelets in vitro and in vivo Int J Cancer 125 2009 2058 2065
4. G.V. Glinsky Anti-adhesion cancer therapy Cancer Metastasis Rev 17 1998 177 185 (Pubitemid 28391952)
5. J.A. Posey, M.B. Khazaeli, A. DelGrosso, M.N. Saleh, C.Y. Lin, and W. Huse A pilot trial of Vitaxin, a humanized anti-vitronectin receptor (anti alpha v beta 3) antibody in patients with metastatic cancer Cancer Biother Radiopharm 16 2001 125 132 (Pubitemid 34121636)
6. Y. Rikitake, and Y. Takai Interactions of the cell adhesion molecule nectin with transmembrane and peripheral membrane proteins for pleiotropic functions Cell Mol Life Sci 65 2008 253 263 (Pubitemid 351161481)
7. J.D. Humphries, A. Byron, and M.J. Humphries Integrin ligands at a glance J Cell Sci 119 2006 3901 3903 (Pubitemid 44650863)
8. C. Selhuber-Unkel, M. Lopez-Garcia, H. Kessler, and J.P. Spatz Cooperativity in adhesion cluster formation during initial cell adhesion Biophys J 95 2008 5424 5431
9. F.G. Giancotti, and E. Ruoslahti Integrin signaling Science 285 1999 1028 1032
10. M.A. Wozniak, K. Modzelewska, L. Kwong, and P.J. Keely Focal adhesion regulation of cell behavior Biochim Biophys Acta 1692 2004 103 119 (Pubitemid 38891769)
11. C. Wang, Y. Yoo, H. Fan, E. Kim, K.L. Guan, and J.L. Guan Regulation of Integrin beta 1 recycling to lipid rafts by Rab1a to promote cell migration J Biol Chem 285 2010 29398 29405
12. D. Lingwood, and K. Simons Lipid rafts as a membrane-organizing principle Science 327 2010 46 50
13. S. Staubach, and F.G. Hanisch Lipid rafts: signaling and sorting platforms of cells and their roles in cancer Expert Rev Proteomics 8 2011 263 277
14. K. Tsuda, N. Furuta, H. Inaba, S. Kawai, K. Hanada, and T. Yoshimori Functional analysis of alpha5beta1 integrin and lipid rafts in invasion of epithelial cells by Porphyromonas gingivalis using fluorescent beads coated with bacterial membrane vesicles Cell Struct Funct 33 2008 123 132
15. B. Leitinger, and N. Hogg The involvement of lipid rafts in the regulation of integrin function J Cell Sci 115 2002 963 972 (Pubitemid 34257381)
16. S. Kasibhatla, K.A. Jessen, S. Maliartchouk, J.Y. Wang, N.M. English, and J. Drewe A role for transferrin receptor in triggering apoptosis when targeted with gambogic acid Proc Natl Acad Sci USA 102 2005 12095 12100 (Pubitemid 41291134)
17. M.K. Pandey, B. Sung, K.S. Ahn, A.B. Kunnumakkara, M.M. Chaturvedi, and B.B. Aggarwal Gambogic acid, a novel ligand for transferrin receptor, potentiates TNF-induced apoptosis through modulation of the nuclear factor-kappaB signaling pathway Blood 110 2007 3517 3525 (Pubitemid 350159615)
18. T. Yi, Z. Yi, S.G. Cho, J. Luo, M.K. Pandey, and B.B. Aggarwal Gambogic acid inhibits angiogenesis and prostate tumor growth by suppressing vascular endothelial growth factor receptor 2 signaling Cancer Res 68 2008 1843 1850 (Pubitemid 351416570)
19. Q. Qi, H. Gu, Y. Yang, N. Lu, J. Zhao, and W. Liu Involvement of matrix metalloproteinase 2 and 9 in gambogic acid induced suppression of MDA-MB-435 human breast carcinoma cell lung metastasis J Mol Med 86 2008 1367 1377
20. Q. Qi, N. Lu, X.T. Wang, H.Y. Gu, Y. Yang, and W. Liu Anti-invasive effect of gambogic acid in MDA-MB-231 human breast carcinoma cells Biochem Cell Biol 86 2008 386 395
21. J. Zhao, Q. Qi, Y. Yang, H.Y. Gu, N. Lu, and W. Liu Inhibition of alpha(4) integrin mediated adhesion was involved in the reduction of B16-F10 melanoma cells lung colonization in C57BL/6 mice treated with gambogic acid Eur J Pharmacol 589 2008 127 131
22. H.Z. Zhang, S. Kasibhatla, Y. Wang, J. Herich, J. Guastella, and B. Tseng Discovery, characterization and SAR of gambogic acid as a potent apoptosis inducer by a HTS assay Bioorg Med Chem 12 2004 309 317 (Pubitemid 38064204)
23. Q. Huang, H.M. Shen, G. Shui, M.R. Wenk, and C.N. Ong Emodin inhibits tumor cell adhesion through disruption of the membrane lipid Raft-associated integrin signaling pathway Cancer Res 66 2006 5807 5815 (Pubitemid 43927135)
24. T. Isaji, J. Gu, R. Nishiuchi, Y. Zhao, M. Takahashi, and E. Miyoshi Introduction of bisecting GlcNAc into integrin alpha5beta1 reduces ligand binding and down-regulates cell adhesion and cell migration J Biol Chem 279 2004 19747 19754 (Pubitemid 38623413)
25. C. Lee Coimmunoprecipitation assay Methods Mol Biol 362 2007 401 406 (Pubitemid 350183185)
26. K. Gaus, S. Le Lay, N. Balasubramanian, and M.A. Schwartz Integrin-mediated adhesion regulates membrane order J Cell Biol 174 2006 725 734 (Pubitemid 44306728)
27. Y.T. Tai, K. Podar, L. Catley, Y.H. Tseng, M. Akiyama, and R. Shringarpure Insulin-like growth factor-1 induces adhesion and migration in human multiple myeloma cells via activation of beta1-integrin and phosphatidylinositol 3′-kinase/AKT signaling Cancer Res 63 2003 5850 5858 (Pubitemid 37187484)
28. E.G. Bligh, and W.J. Dyer A rapid method of total lipid extraction and purification Can J Biochem Physiol 37 1959 911 917
29. J. Acimovic, A. Lovgren-Sandblom, K. Monostory, D. Rozman, M. Golicnik, and D. Lutjohann Combined gas chromatographic/mass spectrometric analysis of cholesterol precursors and plant sterols in cultured cells J Chromatogr B: Analyt Technol Biomed Life Sci 877 2009 2081 2086
30. K.E. Michael, D.W. Dumbauld, K.L. Burns, S.K. Hanks, and A.J. Garcia Focal adhesion kinase modulates cell adhesion strengthening via integrin activation Mol Biol Cell 20 2009 2508 2519
31. C.C. Kumar Signaling by integrin receptors Oncogene 17 1998 1365 1373
32. V.G. Brunton, E. Avizienyte, V.J. Fincham, B. Serrels, C.A. Metcalf 3rd, and T.K. Sawyer Identification of Src-specific phosphorylation site on focal adhesion kinase: dissection of the role of Src SH2 and catalytic functions and their consequences for tumor cell behavior Cancer Res 65 2005 1335 1342 (Pubitemid 40270160)
33. C.E. Turner, J.R. Glenney Jr., and K. Burridge Paxillin: a new vinculin-binding protein present in focal adhesions J Cell Biol 111 1990 1059 1068
34. J.B. Helms, and C. Zurzolo Lipids as targeting signals: lipid rafts and intracellular trafficking Traffic 5 2004 247 254 (Pubitemid 38455748)
35. E.V. Vassilieva, K. Gerner-Smidt, A.I. Ivanov, and A. Nusrat Lipid rafts mediate internalization of beta1-integrin in migrating intestinal epithelial cells Am J Physiol Gastrointest Liver Physiol 295 2008 G965 G976
36. E.P. Kilsdonk, P.G. Yancey, G.W. Stoudt, F.W. Bangerter, W.J. Johnson, and M.C. Phillips Cellular cholesterol efflux mediated by cyclodextrins J Biol Chem 270 1995 17250 17256
37. R.A. Lacalle, E. Mira, C. Gomez-Mouton, S. Jimenez-Baranda, A.C. Martinez, and S. Manes Specific SHP-2 partitioning in raft domains triggers integrin-mediated signaling via Rho activation J Cell Biol 157 2002 277 289 (Pubitemid 34839824)
38. J. Wollam, and A. Antebi Sterol regulation of metabolism, homeostasis, and development Annu Rev Biochem 80 2011 885 916
39. C. Robichon, and I. Dugail De novo cholesterol synthesis at the crossroads of adaptive response to extracellular stress through SREBP Biochimie 89 2007 260 264 (Pubitemid 46161953)
40. I.J. Fidler, and M.L. Kripke Metastasis results from preexisting variant cells within a malignant tumor Science 197 1977 893 895 (Pubitemid 8168759)
41. L. Dolle, H.T. Depypere, and M.E. Bracke Anti-invasive/anti-metastasis strategies: new roads, new tools and new hopes Curr Cancer Drug Targets 6 2006 729 751 (Pubitemid 44875965)
42. M. Pignatelli, and G. Stamp Integrins in tumour development and spread Cancer Surv 24 1995 113 127
43. X. Wang, N. Lu, Q. Yang, D. Gong, C. Lin, and S. Zhang Studies on chemical modification and biology of a natural product, gambogic acid (III): determination of the essential pharmacophore for biological activity Eur J Med Chem 46 2011 1280 1290
44. Y. Kawai, M. Kaidoh, and T. Ohhashi MDA-MB-231 produces ATP-mediated ICAM-1-dependent facilitation of the attachment of carcinoma cells to human lymphatic endothelial cells Am J Physiol Cell Physiol 295 2008 C1123 C1132
45. I.L. Botchkina, R.A. Rowehl, D.E. Rivadeneira, M.S. Karpeh Jr., H. Crawford, and A. Dufour Phenotypic subpopulations of metastatic colon cancer stem cells: genomic analysis Cancer Genomics Proteomics 6 2009 19 29
46. Y. Zhang, M.Y. Hu, W.Z. Wu, Z.J. Wang, K. Zhou, and X.L. Zha The membrane-cytoskeleton organizer ezrin is necessary for hepatocellular carcinoma cell growth and invasiveness J Cancer Res Clin Oncol 132 2006 685 697 (Pubitemid 44337929)
47. A.J. Garcia, and D. Boettiger Integrin-fibronectin interactions at the cell-material interface: initial integrin binding and signaling Biomaterials 20 1999 2427 2433
48. S.M. Kim, and J.H. Hahn CD98 activation increases surface expression and clustering of beta1 integrins in MCF-7 cells through FAK/Src- and cytoskeleton-independent mechanisms Exp Mol Med 40 2008 261 270
49. G. Morozevich, N. Kozlova, I. Cheglakov, N. Ushakova, and A. Berman Integrin alpha5beta1 controls invasion of human breast carcinoma cells by direct and indirect modulation of MMP-2 collagenase activity Cell Cycle 8 2009 2219 2225
50. B. Hu, M.J. Jarzynka, P. Guo, Y. Imanishi, D.D. Schlaepfer, and S.Y. Cheng Angiopoietin 2 induces glioma cell invasion by stimulating matrix metalloprotease 2 expression through the alphavbeta1 integrin and focal adhesion kinase signaling pathway Cancer Res 66 2006 775 783 (Pubitemid 43165942)
51. S. Runz, C.T. Mierke, S. Joumaa, J. Behrens, B. Fabry, and P. Altevogt CD24 induces localization of beta1 integrin to lipid raft domains Biochem Biophys Res Commun 365 2008 35 41 (Pubitemid 350110573)
52. S. Schuck, and K. Simons Polarized sorting in epithelial cells: raft clustering and the biogenesis of the apical membrane J Cell Sci 117 2004 5955 5964 (Pubitemid 40123962)
53. C. Radel, M. Carlile-Klusacek, and V. Rizzo Participation of caveolae in beta1 integrin-mediated mechanotransduction Biochem Biophys Res Commun 358 2007 626 631 (Pubitemid 46755750)
54. G. Pande The role of membrane lipids in regulation of integrin functions Curr Opin Cell Biol 12 2000 569 574
55. R. Xavier, T. Brennan, Q. Li, C. McCormack, and B. Seed Membrane compartmentation is required for efficient T cell activation Immunity 8 1998 723 732 (Pubitemid 28294519)
56. E.J. Jacobs, and S.M. Gapstur Cholesterol and cancer: answers and new questions Cancer Epidemiol Biomarkers Prev 18 2009 2805 2806
57. D.W. Russell Cholesterol biosynthesis and metabolism Cardiovasc Drugs Ther 6 1992 103 110
58. R.E. Soccio, and J.L. Breslow Intracellular cholesterol transport Arterioscler Thromb Vasc Biol 24 2004 1150 1160 (Pubitemid 38880002)
59. A. Miyazaki, and T. Watanabe Acyl-coenzyme A: cholesterol acyltransferase (ACAT) Nippon Rinsho 62 Suppl. 12 2004 89 91