Antiangiogenic, antimigratory and antiinflammatory effects of 2-methoxyestradiol in zebrafish larvae

Comparative Biochemistry and Physiology - C Toxicology and Pharmacology

Volumn 157, Issue 2, 2013, Pages 141-149

  Quezada, Marisol ^a   Alvarez, Marjorie ^b   Peña, Oscar A ^b   Henríquez, Soledad ^a   D'Alençon, Claudia A ^b,c   Lange, Soledad ^a   Oliva, Barbara ^a   Owen, Gareth I ^a,d   Allende, Miguel L ^b  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b UNIVERSITY OF CHILE   (Chile)

^c UNIVERSIDAD ANDRÉS BELLO   (Chile)

^d Biomedical Research Consortium (BMRC) Chile   (Chile)

Author keywords

2 methoxyestradiol; Angiogenesis; EA.hy926; Inflammation; Neutrophil migration; Primordium; Zebrafish

Indexed keywords

2 METHOXYESTRADIOL;

ANIMAL CELL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ANTIINFLAMMATORY ACTIVITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL MIGRATION; CELL SHAPE; CELL VIABILITY; CONTROLLED STUDY; DOSE RESPONSE; EMBRYO; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LARVA; MAMMAL CELL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIMORDIUM; PRIORITY JOURNAL; ZEBRA FISH;

EID: 84872869427     PISSN: 15320456     EISSN: 18781659     Source Type: Journal    
DOI: 10.1016/j.cbpc.2012.10.008     Document Type: Article

References (66)

1. E. Aranda, and G.I. Owen A semi-quantitative assay to screen for angiogenic compounds and compounds with angiogenic potential using the EA.hy926 endothelial cell line Biol. Res. 42 2009 377 389
2. F. Barchiesi, E. Lucchinetti, M. Zaugg, O.O. Ogunshola, M. Wright, M. Meyer, M. Rosselli, S. Schaufelberger, D.G. Gillespie, E.K. Jackson, and R.K. Dubey Candidate genes and mechanisms for 2-methoxyestradiol-mediated vasoprotection Hypertension 56 2010 964 972
3. J. Bauer, M. Margolis, C. Schreiner, C.J. Edgell, J. Azizkhan, E. Lazarowski, and R.L. Juliano In vitro model of angiogenesis using a human endothelium-derived permanent cell line: contributions of induced gene expression, G-proteins, and integrins J. Cell. Physiol. 153 1992 437 449
4. D. Berg, R. Sonsalla, and E. Kuss Concentrations of 2 methoxyoestrogens in human serum measured by a heterologous immunoassay with an 125I-labelled ligand Acta Endocrinol. (Copenh) 103 1983 282 288
5. Y. Blum, H.G. Belting, E. Ellertsdottir, L. Herwig, F. Lüders, and M. Affolter Complex cell rearrangements during intersegmental vessel sprouting and vessel fusion in the zebrafish embryo Dev. Biol. 316 2008 312 322
6. H.J. Choi, and B.T. Zhu Critical role of cyclin B1/Cdc2 up-regulation in the induction of mitotic prometaphase arrest in human breast cancer cells treated with 2-methoxyestradiol Biochim. Biophys. Acta 1823 2012 1306 1315
7. T.K. Chourasia, and K.P. Joy Ovarian P450 aromatase activity in the catfish Heteropneustes fossilis: seasonal changes and effects of catecholestrogens Gen. Comp. Endocrinol. 156 2008 537 543
8. J.M. Chow, C.R. Liu, C.P. Lin, C.N. Lee, Y.C. Cheng, S. Lin, and H.E. Liu Downregulation of c-Myc determines sensitivity to 2-methoxyestradiol-induced apoptosis in human acute myeloid leukemia Exp. Hematol. 36 2008 140 148
9. R.J. D'Amato, C.M. Lin, E. Flynn, J. Folkman, and E. Hamel 2-Methoxyestradiol, an endogenous mammalian metabolite, inhibits tubulin polymerization by interacting at the colchicine site Proc. Natl. Acad. Sci. U. S. A. 91 1994 3964 3968
10. C. d'Alençon, O. Peña, C. Wittmann, V.E. Gallardo, R. Jones, F. Loosli, U. Liebel, C. Grabher, and M.L. Allende A high-throughput chemically induced inflammation assay in zebrafish BMC Biol. 8 2010 151
11. R.K. Dubey, and E.K. Jackson Potential vascular actions of 2-methoxyestradiol Trends Endocrinol. Metab. 20 2009 374 379
12. C.J. Edgell, C.C. McDonald, and J.B. Graham Permanent cell line expressing human factor VIII-related antigen established by hybridization Proc. Natl. Acad. Sci. U. S. A. 80 1983 3734 3737
13. C.J. Edgell, J.E. Haizlip, C.R. Bagnell, J.P. Packenham, P. Harrison, B. Wilbourn, and V.J. Madden Endothelium specific Weibel-Palade bodies in a continuous human cell line, EA.hy926 In Vitro Cell. Dev. Biol. 26 1990 1167 1172
14. J.J. Emeis, and C.J. Edgell Fibrinolytic properties of a human endothelial Irbid cell line (Ea.hy 926) Blood 71 1988 1669 1675
15. T. Fotsis, Y. Zhang, M.S. Pepper, H. Adlercreutz, R. Montesano, P.P. Nawroth, and L. Schweigerer The endogenous oestrogen metabolite 2-methoxyoestradiol inhibits angiogenesis and suppresses tumour growth Nature 368 1994 237 239
16. P. Friedl, and D. Gilmour Collective cell migration in morphogenesis, regeneration and cancer Nat. Rev. Mol. Cell Biol. 10 2009 445 457
17. V.E. Gallardo, J. Liang, M. Behra, A. Elkahloun, E.J. Villablanca, V. Russo, M.L. Allende, and S.M. Burgess Molecular dissection of the migrating posterior lateral line primordium during early development in zebrafish BMC Dev. Biol. 10 2010 120
18. G.E. Garcia, H.G. Wisniewski, M.S. Lucia, N. Arevalo, T.J. Slaga, S.L. Kraft, R. Strange, and A.P. Kumar 2-Methoxyestradiol inhibits prostate tumor development in transgenic adenocarcinoma of mouse prostate: role of tumor necrosis factor-alpha-stimulated gene 6 Clin. Cancer Res. 12 2006 980 988
19. A. Ghysen, and C. Dambly-Chaudière The lateral line microcosmos Genes Dev. 17 2007 2118 2130
20. X. Guo, Q. Mei, Y. Xing, L. Ye, H. Zhang, X. Shi, and Z. Zhang Preparation and cytotoxicity of poly (dl-lactide-co-glycolide) microspheres encapsulating 2-methoxyestradiol Drug Deliv. 19 2012 143 148
21. P. Haas, and D. Gilmour Chemokine signaling mediates self-organizing tissue migration in the zebrafish lateral line Dev. Cell 10 2006 673 680
22. P. Haffter, M. Granato, M. Brand, M.C. Mullins, M. Hammerschmidt, D.A. Kane, J. Odenthal, F.J. van Eeden, Y.J. Jiang, C.P. Heisenberg, R.N. Kelsh, M. Furutani-Seiki, E. Vogelsang, D. Beuchle, U. Schach, C. Fabian, and C. Nüsslein-Volhard The identification of genes with unique and essential functions in the development of the zebrafish, Danio rerio Development 123 1996 1 36
23. C. Hall, M.V. Flores, T. Storm, K. Crosier, and P. Crosier The zebrafish lysozyme C promoter drives myeloid-specific expression in transgenic fish BMC Dev. Biol. 7 2007 42
24. D. Hassel, P. Cheng, M.P. White, K.N. Ivey, J. Kroll, H.G. Augustin, H.A. Katus, D.Y. Stainier, and D. Srivastava MicroRNA-10 Regulates the Angiogenic Behavior of Zebrafish and Human Endothelial Cells by Promoting Vascular Endothelial Growth Factor Signaling Circ Res. 111 2012 1421 1433
25. M.R. Harrison, N.M. Hahn, R. Pili, W.K. Oh, H. Hammers, C. Sweeney, K. Kim, S. Perlman, J. Arnott, C. Sidor, G. Wilding, and G. Liu A phase II study of 2-methoxyestradiol (2ME2) NanoCrystal® dispersion (NCD) in patients with taxane-refractory, metastatic castrate-resistant prostate cancer (CRPC) Invest. New Drugs 29 2011 1465 1474
26. M.W. Hung, Z.J. Zhang, S. Li, B. Lei, S. Yuan, G.Z. Cui, P. Man Hoi, K. Chan, and S.M. Lee From omics to drug metabolism and high content screen of natural product in zebrafish: a new model for discovery of neuroactive compound Evid. Based Complement Alternat. Med. 2012 2012 605303
27. J.S. Isenberg, Y. Jia, L. Field, L.A. Ridnour, A. Sparatore, P. Del Soldato, A.L. Sowers, G.C. Yeh, T.W. Moody, D.A. Wink, R. Ramchandran, and D.D. Roberts Modulation of angiogenesis by dithiolethione-modified NSAIDs and valproic acid Br. J. Pharmacol. 151 2007 63 72
28. A.C. Issekutz, and K. Sapru Modulation of adjuvant arthritis in the rat by 2-methoxyestradiol: an effect independent of an anti-angiogenic action Int. Immunopharmacol. 8 2008 708 716
29. M. Kalén, E. Wallgard, N. Asker, A. Nasevicius, E. Athley, E. Billgren, J.D. Larson, S.A. Wadman, E. Norseng, K.J. Clark, L. He, L. Karlsson-Lindahl, A.K. Häger, H. Weber, H. Augustin, T. Samuelsson, C.K. Kemmet, C.M. Utesch, J.J. Essner, P.B. Hackett, and M. Hellström Combination of reverse and chemical genetic screens reveals angiogenesis inhibitors and targets Chem. Biol. 16 2009 432 441
30. K. Kamath, T. Okouneva, G. Larson, D. Panda, L. Wilson, and M.A. Jordan 2-Methoxyestradiol suppresses microtubule dynamics and arrests mitosis without depolymerizing microtubules Mol. Cancer Ther. 5 2006 2225 2233
31. S. Kato, A. Sadarangani, S. Lange, A.M. Delpiano, M. Vargas, J. Brañes, J. Carvajal, S. Lipkowitz, G.I. Owen, and M.A. Cuello 2-methoxyestradiol mediates apoptosis through caspase-dependent and independent mechanisms in ovarian cancer cells but not in normal counterparts Reprod. Sci. 15 2008 878 894
32. M. Konantz, T.B. Balci, U.F. Hartwig, G. Dellaire, M.C. André, J.N. Berman, and C. Lengerke Zebrafish xenografts as a tool for in vivo studies on human cancer Ann N Y Acad Sci. 1266 2012 124 137
33. A. Kurokawa, K. Azuma, T. Mita, Y. Toyofuku, Y. Fujitani, T. Hirose, K. Iwabuchi, H. Ogawa, S. Takeda, R. Kawamori, and H. Watada 2-Methoxyestradiol reduces monocyte adhesion to aortic endothelial cells in ovariectomized rats Endocr. J. 54 2007 1027 1031
34. N.D. Lawson, and B.M. Weinstein In vivo imaging of embryonic vascular development using transgenic zebrafish Dev. Biol. 248 2002 307 318
35. V. Lecaudey, G. Cakan-Akdogan, W.H. Norton, and D. Gilmour Dynamic Fgf signaling couples morphogenesis and migration in the zebrafish lateral line primordium Development 135 2008 2695 2705
36. A. Letamendia, C. Quevedo, I. Ibarbia, J.M. Virto, O. Holgado, M. Diez, J.C. Izpisua-Belmonte, and C. Callol-Massot Development and validation of an automated high-throughput system for zebrafish in vivo screenings PLoS One 7 2012 e36690
37. E.Y. Ma, and D.W. Raible Signaling pathways regulating zebrafish lateral line development Curr. Biol. 19 2009 R381 R386
38. N.J. Mabjeesh, D. Escuin, T.M. LaVallee, V.S. Pribluda, G.M. Swartz, M.S. Johnson, M.T. Willard, H. Zhong, J.W. Simons, and P. Giannakakou 2ME2 inhibits tumor growth and angiogenesis by disrupting microtubules and dysregulating HIF Cancer Cell 3 2003 363 375
39. F. Machado-Linde, P. Pelegrin, M.L. Sanchez-Ferrer, J. Leon, P. Cascales, and J.J. Parrilla 2-methoxyestradiol in the pathophysiology of endometriosis: focus on angiogenesis and therapeutic potential Reprod. Sci. 19 2012 1018 1029
40. D. Matei, J. Schilder, G. Sutton, S. Perkins, T. Breen, C. Quon, and C. Sidor Activity of 2 methoxyestradiol (Panzem NCD) in advanced, platinum-resistant ovarian cancer and primary peritoneal carcinomatosis: a Hoosier Oncology Group trial Gynecol. Oncol. 115 2009 90 96
41. M.C. McKinney, and B.M. Weinstein Using the zebrafish to study vessel formation Methods Enzymol. 444 2008 65 97
42. S. Mooberry Mechanism of action of 2-methoxyestradiol: new developments Drug Resist. Updat. 6 2003 355 361
43. A.O. Mueck, and H. Seeger 2-Methoxyestradiol-biology and mechanism of action Steroids 75 2010 625 631
44. V.S. Pribluda, E.R. Gubish Jr., T.M. Lavallee, A. Treston, G.M. Swartz, and S.J. Green 2-Methoxyestradiol: an endogenous antiangiogenic and antiproliferative drug candidate Cancer Metastasis Rev. 19 2000 173 179
45. M. Quezada, J. Diaz, S. Henriquez, M.L. Bravo, E. Aranda, B. Oliva, M. Villalon, S. Kato, M.A. Cuello, J.J. Brosens, C.A. Lange, and G.I. Owen 2-Methoxyestradiol inhibits progesterone-dependent tissue factor expression and activity in breast cancer cells Horm. Cancer 1 2010 117 126
46. M.J. Redd, G. Kelly, G. Dunn, M. Way, and P. Martin Imaging macrophage chemotaxis in vivo: studies of microtubule function in zebrafish wound inflammation Cell Motil. Cytoskeleton 63 2006 415 422
47. S.A. Renshaw, C.A. Loynes, D.M. Trushell, S. Elworthy, P.W. Ingham, and M.K. Whyte A transgenic zebrafish model of neutrophilic inflammation Blood 108 2006 3976 3978
48. S.A. Salama, M.W. Kamel, S. Botting, S.M. Salih, M.A. Borahay, A.A. Hamed, G.S. Kilic, M. Saeed, M.Y. Williams, and C.R. Diaz-Arrastia Catechol-o-methyltransferase expression and 2-methoxyestradiol affect microtubule dynamics and modify steroid receptor signaling in leiomyoma cells PLoS One 4 2009 e7356
49. S.A. Salama, C.R. Diaz-Arrastia, G.S. Kilic, and M.W. Kamel 2-Methoxyestradiol causes functional repression of transforming growth factor β3 signaling by ameliorating Smad and non-Smad signaling pathways in immortalized uterine fibroid cells Fertil Steril. 98 2012 178 184
50. M. Sattler, L.R. Quinnan, Y.B. Pride, J.L. Gramlich, S.C. Chu, G.C. Even, S.K. Kraeft, L.B. Chen, and R. Salgia 2-methoxyestradiol alters cell motility, migration, and adhesion Blood 102 2003 289 296
51. G. Schumacher, and P. Neuhaus The physiological estrogen metabolite 2-methoxyestradiol reduces tumor growth and induces apoptosis in human solid tumors J. Cancer Res. Clin. Oncol. 127 2001 405 410
52. H. Seeger, D. Wallwiener, and A.O. Mueck Different effects of estradiol and various antiestrogens on TNF-alpha-induced changes of biochemical markers for growth and invasion of human breast cancer cells Life Sci. 78 2006 1464 1468
53. F.H. Shand, S.Y. Langenbach, C.R. Keenan, S.P. Ma, B.J. Wheaton, M.J. Schuliga, J. Ziogas, and A.G. Stewart In vitro and in vivo evidence for anti-inflammatory properties of 2-methoxyestradiol J. Pharmacol. Exp. Ther. 336 2011 962 972
54. C.A. Staton, W.R. Malcolm, and N.J. Brown A critical analysis of current in vitro and in vivo angiogenesis assays Int. J. Exp. Pathol. 90 2009 195 221
55. W.L. Seng, K. Eng, J. Lee, and P. McGrath Use of a monoclonal antibody specific for activated endothelial cells to quantitate angiogenesis in vivo in zebrafish after drug treatment Angiogenesis 7 2004 243 253
56. A. Stubelius, E. Andréasson, A. Karlsson, C. Ohlsson, A. Tivesten, U. Islander, and H. Carlsten Role of 2-methoxyestradiol as inhibitor of arthritis and osteoporosis in a model of postmenopausal rheumatoid arthritis Clin. Immunol. 140 2011 37 46
57. A.J. Tevaarwerk, K.D. Holen, D.B. Alberti, C. Sidor, J. Arnott, C. Quon, G. Wilding, and G. Liu Phase I trial of 2-methoxyestradiol nanocrystal dispersion in advanced solid malignancies Clin. Cancer Res. 15 2009 1460 1465
58. E.Y. Tong, G.C. Collins, A.E. Greene-Colozzi, J.L. Chen, P.D. Manos, K.M. Judkins, J.A. Lee, M.J. Ophir, F.M. Laliberte, and T.J. Levesque Motion-based angiogenesis analysis: a simple method to quantify blood vessel growth Zebrafish 6 2009 239 243
59. T.C. Tran, B. Sneed, J. Haider, D. Blavo, A. White, T. Aiyejorun, T.C. Baranowski, A.L. Rubinstein, T.N. Doan, R. Dingledine, and E.M. Sandberg Automated, quantitative screening assay for antiangiogenic compounds using transgenic zebrafish Cancer Res. 67 2007 11386 11392
60. E.J. Villablanca, D. Zhou, B. Valentinis, A. Negro, L. Raccosta, L. Mauri, A. Prinetti, S. Sonnino, C. Bordignon, C. Traversari, and V. Russo Selected natural and synthetic retinoids impair CCR7- and CXCR4-dependent cell migration in vitro and in vivo J. Leukoc. Biol. 84 2008 871 879
61. A. Vogt, A. Cholewinski, X. Shen, S.G. Nelson, J. Lazo, J. Tsang, and N. Hukreide Automated image-based phenotypic analysis in zebrafish embryos Dev. Dyn. 238 2009 656 663
62. C. Wang, W. Tao, Y. Wang, J. Bikow, B. Lu, A. Keating, S. Verma, T.G. Parker, R. Han, and X.Y. Wen Rosuvastatin, identified from a zebrafish chemical genetic screen for antiangiogenic compounds, suppresses the growth of prostate cancer Eur. Urol. 58 2010 418 426
63. T. Xiao, T. Roeser, W. Staub, and H. Baier A GFP-based genetic screen reveals mutations that disrupt the architecture of the zebrafish retinotectal projection Development 132 13 2005 2955 2967
64. H. Yin, Y. Gui, and X.L. Zheng 2-Methoxyestradiol inhibits atorvastatin-induced rounding of human vascular smooth muscle cells J. Cell. Physiol. 222 2010 556 564
65. T.L. Yue, X. Wang, C.S. Louden, S. Gupta, K. Pillarisetti, J.L. Gu, T.K. Hart, P.G. Lysko, and G.Z. Feuerstein 2-Methoxyestradiol, an endogenous estrogen metabolite, induces apoptosis in endothelial cells and inhibits angiogenesis: possible role for stress-activated protein kinase signaling pathway and Fas expression Mol. Pharmacol. 51 1997 951 962
66. J. Zhang, M. Sattler, G. Tonon, C. Grabher, S. Lababidi, A. Zimmerhackl, M.S. Raab, S. Vallet, Y. Zhou, M.A. Cartron, T. Hideshima, Y.T. Tai, D. Chauhan, K.C. Anderson, and K. Podar Targeting angiogenesis via a c-Myc/hypoxia- inducible factor-1alpha-dependent pathway in multiple myeloma Cancer Res. 69 2009 5082 5090