Vascular endothelial growth factors are differentially regulated by steroid hormones and antiestrogens in breast cancer cells

Molecular and Cellular Endocrinology

Volumn 149, Issue 1-2, 1999, Pages 29-40

  Ruohola, Johanna K ^a   Valve, Eeva M ^a   Karkkainen, Marika J ^b   Joukov, Vladimir ^b   Alitalo, Kari ^b   Härkönen, Pirkko L ^a  

^a UNIVERSITY OF TURKU   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Androgen; Breast cancer; Estrogen; Tamoxifen; Toremifene; Vascular endothelial growth factor

Indexed keywords

ANDROGEN; ANTIESTROGEN; CYPROTERONE ACETATE; ESTROGEN; FULVESTRANT; MESSENGER RNA; STEROID HORMONE; TAMOXIFEN; TESTOSTERONE; TOREMIFENE; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; BREAST CARCINOMA; CANCER CELL CULTURE; CANCER GROWTH; CONTROLLED STUDY; GENETIC TRANSCRIPTION; HORMONE RESPONSIVE ELEMENT; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; TUMOR VASCULARIZATION;

ANIMALS; BREAST NEOPLASMS; CYCLOHEXIMIDE; CYPROTERONE ACETATE; ENDOTHELIAL GROWTH FACTORS; ESTRADIOL; ESTROGEN ANTAGONISTS; FEMALE; HUMANS; LYMPHOKINES; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; NEOPLASMS, HORMONE-DEPENDENT; PROTEIN SYNTHESIS INHIBITORS; RNA, MESSENGER; RNA, NEOPLASM; STEROIDS; TAMOXIFEN; TESTOSTERONE; TOREMIFENE; TUMOR CELLS, CULTURED; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTORS;

EID: 0033602501     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0303-7207(99)00003-9     Document Type: Article

References (76)

1. Achen M.G., Jeltsch M., Kukk E., Mäkinen T., Vitali A., Wilks A.F., Alitalo K., Stacker S.A. Vascular endothelial growth factor D (VEGF-D) is a ligand for the tyrosine kinases VEGF receptor 2 (Flk1) and VEGF receptor 3 (Flt4). Proc. Natl. Acad. Sci. USA. 95:1998;548-553.
2. Berse B., Brown L.F., Van De Water L., Drovak H.F., Senger D.R. Vascular permeability factor (vascular endothelial growth factor) gene is expressed differentially in normal tissues, macrophages, and tumors. Mol. Biol. Cell. 3:1992;211-220.
3. Brown L.F., Berse B., Jackman R.W. et al. Expression of vascular permeability factor (vascular endothelial growth factor) and its receptors in breast cancer. Hum. Pathol. 26:1995;86-91.
4. Bubulya A., Wise S.C., Shen X-Q., Burmeister L.A., Shemshedini L. C-Jun can mediate androgen receptor-induced transactivation. J. Biol. Chem. 271:1996;24583-24589.
5. Charnock-Jones D.S., Sharkey A.M., Rajput-Williams J. et al. Identification and localization of alternately spliced mRNAs for vascular endothelial growth factor in human uterus and estrogen regulation in endometrial carcinoma cell lines. Biol. Reprod. 48:1993;1120-1128.
6. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:1987;156-159.
7. Connolly D.T., Olander J.V., Heuvelman D. et al. Human vascular permeability factor isolation from U937 cells. J. Biol. Chem. 264:1989;20017-20024.
8. Cowley E.A., Hoare S., Mosselman S., Parker M.G. Estrogen receptors α and β form heterodimers on DNA. J. Biol. Chem. 272:1997;19858-19862.
9. Cullinan-Bove K., Koos R.D. Vascular endothelial growth factor/vascular permeability factor expression in the rat uterus: rapid stimulation by estrogen correlates with estrogen-induced increases in uterine capillary permeability and growth. Endocrinology. 133:1993;829-837.
10. Darbre P.D., King R.J.B. Steroid hormone regulation of cultured breast cancer cells. Lippman M.E., Dickson R.B. Breast Cancer. Cellular and Molecular Biology. 1988;307-341 Kluwer, Boston.
11. Desmond W.J., Wolbers S.J., Sato G. Cloned mouse mammary cell lines requiring androgen for growth in culture. Cell. 8:1976;79-86.
12. Dickson R.B., Lippman M.E. Growth factors in breast cancer. Endocr. Rev. 16:1995;559-589.
13. Enholm B., Paavonen K., Ristimäki A. et al. Comparison of VEGF, VEGF-B, VEGF-C and Ang-1 mRNA regulation by serum, growth factors, oncoproteins and hypoxia. Oncogene. 14:1997;2475-2483.
14. Ferrara N., Davis-Smyth T. The biology of vascular endothelial growth factor. Endocr. Rev. 18:1997;4-25.
15. Ferrara N., Henzel W.J. Pituitary follicular cells secrete a novel heparin-binding growth factor specific for vascular endothelial cells. Biochem. Biophys. Res. Commun. 161:1989;851-858.
16. Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat. Med. 1:1995;27-31.
17. Fort P., Marty L., Piechaczyk M., El Sabrouty S., Dani C., Jeanteur P., Planchard J.M. Various rat adult tissues express only one major mRNA species from glyceraldehyde-3-phosphate-dehydrogenase multigenic family. Nucleic Acids Res. 16:1985;1431-1442.
18. Friesel R.E., Maciag T. Molecular mechanisms of angiogenesis: fibroblast growth factor signal transduction. FASEB J. 9:1995;919-925.
19. Garrido C., Saule S., Gospodarowicz D. Transcriptional regulation of vascular endothelial growth factor gene expression in ovarian bovine granulosa cells. Growth Factors. 8:1993;109-117.
20. Gasparini G., Toi M., Gion M. et al. Prognostic significance of vascular endothelial growth factor protein in node-negative breast carcinoma. J. Natl. Cancer Inst. 89:1997;139-147.
21. Gille J., Swerlick R.A., Caughman S.W. Transforming growth factor-(-induced transcriptional activation of the vascular permeability factor (VPF/VEGF) gene requires AP-2-dependent DNA binding and transactivation. EMBO J. 16:1997;750-759.
22. Goldberg M.A., Schneider T.J. Similarities between the oxygen-sensing mechanisms regulating the expression of vascular endothelial growth factor and erythropoietin. J. Biol. Chem. 269:1994;4355-4359.
23. Gospodarowicz D., Abraham J.A., Schilling J. Isolation and characterization of a vascular endothelial cell mitogen produced by pituitary-derived folliculo stellate cells. Proc. Natl. Acad. Sci. USA. 86:1989;7311-7315.
24. Grenman R., Laine K.-M., Klemi P.J., Grenman S., Hayashida D.J.S., Joensuu H. Effects of the antiestrogen toremifene on growth of the human mammary carcinoma cell line MCF-7. J. Cancer Res. Clin. Oncol. 117:1991;223-226.
25. Hanahan D., Folkman J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell. 86:1996;353-364.
26. Härkönen P.L., Laaksonen E.I.G., Valve E.M., Solic N., Darbre P.D. Temperature-sensitive mutants for steroid-sensitive growth of S115 mouse mammary tumor cells. Expt. Cell Res. 186:1990;288-298.
27. Harley C.B. Hybridisation of oligo(dT) to RNA on nitrocellulose. Gene Anal. Technol. 4:1987;17-22.
28. Hartmann K.P., Papa V., Brown E.J., Doerries U., Rosenthal S.M., Goldfine I.D. A rapid and simple one step method for isolation of poly(A)+RNA from cells in monolayer. Endocrinology. 127:1990;2038-2040.
29. Houck K.A., Ferrara N., Winer J., Cachianes G., Li B., Leung D.W. The vascular endothelial growth factor family: identification of a fourth molecular species and characterization of alternative splicing of RNA. Mol. Endocrinol. 5:1991;1806-1814.
30. Hyder S.M., Stancel G.M., Chiappetta C., Murthy L., Boettger-Tong H.L., Makela S. Uterine expression of vascular endothelial growth factor is increased by estradiol and tamoxifen. Cancer Res. 56:1996;3954-3960.
31. Hyder S.M., Murthy L., Stancel G.M. Progestin regulation of vascular endothelial growth factor in human breast cancer cells. Cancer Res. 58:1998;392-395.
32. Hyunh H.T., Pollak M. Insulin-like growth factor I gene expression in the uterus is stimulated by tamoxifen and inhibited by the pure antiestrogen ICI 182780. Cancer Res. 53:1993;5585-5588.
33. Jeltsch M., Kaipainen A., Joukov V. et al. Hyperplasia of lymphatic vessels in VEGF-C transgenic mice. Science. 276:1997;1423-1425.
34. Jordan V.C., Murphy C.S. Endocrine pharmacology of antiestrogens as antitumor agents. Endocr. Rev. 11:1990;578-610.
35. Joseph I.B.J.K., Nelson J.B., Denmeade S.R., Isaacs J.T. Androgens regulate vascular endothelial growth factor content in normal and malignant prostatic tissue. Clin. Cancer Res. 3:1997;2507-2511.
36. Joukov V., Pajusola K., Kaipainen A. et al. A novel vascular endothelial growth factor, VEGF-C, is a ligand for the Flt4 (VEGFR-3) and KDR (VEGFR-2) receptor tyrosine kinases. EMBO J. 15:1996;290-298.
37. Kallio P.J., Poukka H., Moilanen A., Jänne O.A., Palvimo J.J. Androgen receptor-mediated transcriptional regulation in the absence of direct interaction with a specific DNA element. Mol. Endocrinol. 9:1995;1017-1028.
38. Kuiper G.G.J.M., Enmark E., Pelto-Huikko M., Nilsson S., Gustafsson J.Å. Cloning of a novel estrogen receptor expressed in rat prostate and ovary. Proc. Natl. Acad. Sci. USA. 93:1996;5925-5930.
39. Laitinen M., Ristimäki A., Honkasalo M., Narko K., Paavonen K., Ritvos O. Differential hormonal regulation of vascular endothelial growth factors VEGF, VEGF-B, and VEGF-C messenger ribonucleic acid levels in cultured human granulosa-luteal cells. Endocrinology. 138:1997;4748-4756.
40. Leung D.W., Cachianes G., Kuang W.J., Goeddel D.V., Ferrara N. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science. 246:1989;1306-1309.
41. Lee J., Gray A., Yuan J., Luoh S.-M., Avraham H., Wood W.I. Vascular endothelial growth factor-related protein: a ligand and specific activator of the tyrosine kinase receptor Flt4. Proc. Natl. Acad. Sci. USA. 93:1996;1988-1992.
42. Levy A.P., Levy N.S., Wegner S., Goldberg M.A. Transcriptional regulation of the rat vascular endothelial growth factor gene by hypoxia. J. Biol. Chem. 270:1995;13333-13340.
43. Levy A.P., Levy N.S., Goldberg M.A. Post-transcriptional regulation of vascular endothelial growth factor by hypoxia. J. Biol. Chem. 271:1996;2746-2753.
44. Maglione D., Guerriero V., Viglietto G., Delli Bovi P., Persico M.G. Isolation of a human placenta cDNA coding for a protein related to the vascular permeability factor. Proc. Natl. Acad. Sci. USA. 88:1991;9267-9271.
45. Minchenco A., Bauer T., Salceda S., Caro J. Hypoxic stimulation of vascular endothelial growth factor expression in vitro and in vivo. Lab. Invest. 71:1994;374-379.
46. Mustonen T., Alitalo K. Endothelial receptor tyrosine kinases involved in angiogenesis. J. Cell Biol. 129:1995;895-898.
47. Nakamura J., Savinov A., Lu Q., Brodie A. Estrogen regulates vascular endothelial growth/ permeability factor expression in 7,12-dimethylbenz(a)anthracene-induced rat mammary tumors. Endocrinology. 137:1996;5589-5596.
48. Oh S.-J., Jeltsch M.M., Birkenhäger R. et al. VEGF and VEGF-C: specific induction of angiogenesis and lymphangiogenesis in the differentiated avian chorioallantoic membrane. Dev. Biol. 188:1997;96-109.
49. Olofsson B., Pajusola K., Kaipainen A. et al. Vascular endothelial growth factor B, a novel growth factor for endothelial cells. Proc. Natl. Acad. Sci. USA. 93:1996a;2576-2581.
50. Olofsson B., Pajusola K., von Euler G., Chilov D., Alitalo K., Eriksson U. Genomic organization of the mouse and human genes for vascular endothelial growth factor B (VEGF-B) and characterization of a second splice isoform. J. Biol. Chem. 271:1996b;19310-19317.
51. Olofsson B., Korpelainen E., Pepper M.S. et al. Vascular endothelial growth factor B (VEGF-B) binds to VEGF receptor-1 and regulates plasminogen activator activity in endothelial cells. Proc. Natl Acad. Sci. USA. 95:1998;11709-11714.
52. Orlandini M., Marconcini L., Ferruzzi R., Oliviero S. Identification of a c-fos-induced gene that is related to the platelet-derived growth factor/vascular endothelial growth factor family. Proc. Natl. Acad. Sci. USA. 93:1996;11675-11680.
53. Osborne C.K., Hobbs K., Trent J.M. Biological differences among MCF-7 human breast cancer cell lines from different laboratories. Breast Cancer Res. Treat. 9:1987;111-121.
54. Paech K., Webb P., Kuiper G.G.J.M. et al. Differential ligand activation of estrogen receptors ERα and ERβ at AP1 sites. Science. 277:1997;1508-1510.
55. Parker M.G. Structure and function of estrogen receptors. Vitam. Horm. 51:1995;267-287.
56. Philips A., Chalbos D., Rocheford H. Estradiol increases and anti-estrogens antagonize the growth factor -induced activator protein-1 activity in MCF-7 breast cancer cells without affecting c-fos and c-jun synthesis. J. Biol. Chem. 268:1993;14103-14108.
57. 145, a secreted vascular endothelial growth factor isoform that binds to extracellular matrix. J. Biol. Chem. 272:1997;7151-7158.
58. Poyet P., Labrie F. Comparison of the antiandrogenic/androgenic activities of flutamide, cyproterone acetate and megestrol acetate. Mol. Cell. Endocrinol. 42:1985;283-288.
59. Porter W., Saville B., Hoivik D., Safe S. Functional synergy between the transcription factor Sp1 and the estrogen receptor. Mol. Endocrinol. 11:1997;1569-1580.
60. Ristimäki A., Narko K., Enholm B., Joukov V., Alitalo K. Proinflammatory cytokines regulate expression of the lymphatic endothelial mitogen vascular endothelial growth factor-C. J. Biol. Chem. 273:1998;8413-8418.
61. Ruohola J.K., Valve E.M., Vainikka S., Alitalo K., Härkönen P.L. Androgen and fibroblast growth factor (FGF) regulation of FGF receptors in S115 mouse mammary tumor cells. Endocrinology. 136:1995;2179-2188.
62. Sato N., Sadar M.D., Bruchovsky N., Saatcioglu F., Rennie P.S., Lange P.H., Cleave M.E. Androgenic induction of prostate-specific antigen gene is repressed by protein-protein interaction between the androgen receptor and AP-1/c-Jun in the human prostate cancer cell line LNCaP. J. Biol. Chem. 272:1997;17485-17494.
63. Shweiki D., Itin A., Soffer D., Keshet E. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature. 359:1992;843-845.
64. Shweiki D., Itin A., Neufeld G., Gitay-Goren H., Keshet E. Patterns of expression of vascular endothelial growth factor (VEGF) and VEGF receptors in mice suggest a role in hormonally regulated angiogenesis. J. Clin. Invest. 91:1993;2235-2243.
65. Tischer E., Mitchell R., Hartman T., Silva M., Gospodarowicz D., Fiddes J.C., Abraham J.A. The human gene for vascular endothelial growth factor: multiple protein forms are encoded through alternative exon splicing. J. Biol. Chem. 266:1991;11947-11954.
66. Toi M., Hoshina S., Takayanagi T., Tominaga T. Association of vascular endothelial growth factor expression with tumor angiogenesis and with early relapse in primary breast cancer. Jpn. J. Cancer Res. 85:1994;1045-1049.
67. Toi M., Inada K., Suzuki H., Tominaga T. Tumor angiogenesis in breast cancer: Its importance as a prognostic indicator and the association with vascular endothelial growth factor expression. Breast Cancer Res. Treat. 36:1995;193-204.
68. Toi M., Kondo S., Suzuki H. et al. Quantitative analysis of vascular endothelial growth factor in primary breast cancer. Cancer. 77:1996;1101-1106.
69. Umayahara Y., Kawamori R., Watada H. et al. Estrogen regulation of the insulin-like growth factor I gene transcription involves an AP-1 enhancer. J. Biol. Chem. 269:1994;16433-16442.
70. Wakeling A.E. The future of new pure antiestrogens in clinical breast cancer. Breast Cancer Res. Treat. 25:1993;1-9.
71. Wärri A.M., Laine A.M., Majasuo K.E., Alitalo K.K., Härkönen P.L. Estrogen suppression of erbB2 expression is associated with increased growth rate of ZR-75-1 human breast cancer cells in vitro and in nude mice. Int. J. Cancer. 49:1991;616-623.
72. Wärri A.M., Huovinen R.L., Laine A.M., Martikainen P.M., Härkönen P.L. Apoptosis in toremifene-induced growth inhibition of human breast cancer cells in vivo and in vitro. J. Natl. Cancer Inst. 85:1993;1412-1418.
73. Webb P., Lopez G.N., Uht R.M., Kushner P.J. Tamoxifen activation of the estrogen receptor/AP-1 pathway: Potential origin for the cell-specific estrogen-like effects of antiestrogens. Mol. Endocrinol. 9:1995;443-456.
74. Zhang H.-T., Craft P., Scott P.A.E., Ziche M., Weich H.A., Harris A.L., Bicknell R. Enhancement of tumor growth and vascular density by transfection of vascular endothelial cell growth factor into MCF-7 human breast carcinoma cells. J. Natl. Cancer Inst. 87:1995;213-219.
75. Yoshiji H., Gomez D.E., Shibuya M., Thorgeirsson U.P. Expression of vascular endothelial growth factor, its receptor, and other angiogenic factors in human breast cancer. Cancer Res. 56:1996;2013-2016.
76. Yoshiji H., Harris S.R., Thorgeirsson U.P. Vascular endothelial growth factor is essential for initial but not continued in vivo growth of human breast carcinoma cells. Cancer Res. 57:1997;3924-3928.