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Originally published In Press as doi:10.1074/jbc.M205692200 on November 5, 2002

J. Biol. Chem., Vol. 278, Issue 4, 2701-2712, January 24, 2003
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Proximal Events in Signaling by Plasma Membrane Estrogen Receptors*

Mahnaz RazandiDagger , Ali PedramDagger , Steven T. ParkDagger , and Ellis R. LevinDagger §

From the Division of Endocrinology, Veterans Affairs Medical Center, Long Beach, Long Beach, California 90822 and the Departments of Dagger  Medicine and § Pharmacology, University of California, Irvine, California 92717

Estradiol (E2) rapidly stimulates signal transduction from plasma membrane estrogen receptors (ER) that are G protein-coupled. This is reported to occur through the transactivation of the epidermal growth factor receptor (EGFR) or insulin-like growth factor-1 receptor, similar to other G protein-coupled receptors. Here, we define the signaling events that result in EGFR and ERK activation. E2-stimulated ERK required ER in breast cancer and endothelial cells and was substantially prevented by expression of a dominant negative EGFR or by tyrphostin AG1478, a specific inhibitor for EGFR tyrosine kinase activity. Transactivation/phosphorylation of EGFR by E2 was dependent on the rapid liberation of heparin-binding EGF (HB-EGF) from cultured MCF-7 cells and was blocked by antibodies to this ligand for EGFR. Expression of dominant negative mini-genes for Galpha q and Galpha i blocked E2-induced, EGFR-dependent ERK activation, and Gbeta gamma also contributed. G protein activation led to activation of matrix metalloproteinases (MMP)-2 and -9. This resulted from Src-induced MMP activation, implicated using PP2 (Src family kinase inhibitor) or the expression of a dominant negative Src protein. Antisense oligonucleotides to MMP-2 and MMP-9 or ICI 182780 (ER antagonist) each prevented E2-induced HB-EGF liberation and ERK activation. E2 also induced AKT up-regulation in MCF-7 cells and p38beta MAP kinase activity in endothelial cells, blocked by an MMP inhibitor, GM6001, and tyrphostin AG1478. Targeting of only the E domain of ERalpha to the plasma membrane resulted in MMP activation and EGFR transactivation. Thus, specific G proteins mediate the ability of E2 to activate MMP-2 and MMP-9 via Src. This leads to HB-EGF transactivation of EGFR and signaling to multiple kinase cascades in several target cells for E2. The E domain is sufficient to enact these events, defining additional details of the important cross-talk between membrane ER and EGFR in breast cancer.

* This work was supported by a grant from the Research Service of the Department of Veteran's Affairs, a grant from the Avon Products Breast Cancer Research Foundation, Department of Defense Breast Cancer Research Program Grant BC990915, and National Institutes of Health Grant HL-59890 (to E. R. L.).The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

To whom correspondence should be addressed: Medical Service (111-I), Long Beach VA Medical Center/UC-Irvine, 5901 E. 7th St., Long Beach, CA 90822. Tel.: 562-826-5748; Fax: 562-826-5515; E-mail: ellis.levin@med.va.gov.

Copyright © 2003 by The American Society for Biochemistry and Molecular Biology, Inc.
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N. N. Bulayeva, A. L. Wozniak, L. L. Lash, and C. S. Watson
Mechanisms of membrane estrogen receptor-{alpha}-mediated rapid stimulation of Ca2+ levels and prolactin release in a pituitary cell line
Am J Physiol Endocrinol Metab, February 1, 2005; 288(2): E388 - E397.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
C. K. Osborne, J. Shou, S. Massarweh, and R. Schiff
Crosstalk between Estrogen Receptor and Growth Factor Receptor Pathways as a Cause for Endocrine Therapy Resistance in Breast Cancer
Clin. Cancer Res., January 15, 2005; 11(2): 865s - 870s.
[Abstract] [Full Text] [PDF]

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 Endocr Relat CancerHome page
A. Ring and M. Dowsett
Mechanisms of tamoxifen resistance
Endocr. Relat. Cancer, December 1, 2004; 11(4): 643 - 658.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Endocrinol.Home page
M. Razandi, A. Pedram, I. Merchenthaler, G. L. Greene, and E. R. Levin
Plasma Membrane Estrogen Receptors Exist and Functions as Dimers
Mol. Endocrinol., December 1, 2004; 18(12): 2854 - 2865.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
A.-M. Gaben, C. Saucier, M. Bedin, G. Redeuilh, and J. Mester
Mitogenic Activity of Estrogens in Human Breast Cancer Cells Does Not Rely on Direct Induction of Mitogen-Activated Protein Kinase/Extracellularly Regulated Kinase or Phosphatidylinositol 3-Kinase
Mol. Endocrinol., November 1, 2004; 18(11): 2700 - 2713.
[Abstract] [Full Text] [PDF]

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 Endocr. Rev.Home page
K.-C. Leung, G. Johannsson, G. M. Leong, and K. K. Y. Ho
Estrogen Regulation of Growth Hormone Action
Endocr. Rev., October 1, 2004; 25(5): 693 - 721.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
Q. Zhang, S. M. Thomas, S. Xi, T. E. Smithgall, J. M. Siegfried, J. Kamens, W. E. Gooding, and J. R. Grandis
Src Family Kinases Mediate Epidermal Growth Factor Receptor Ligand Cleavage, Proliferation, and Invasion of Head and Neck Cancer Cells
Cancer Res., September 1, 2004; 64(17): 6166 - 6173.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
V. V. Chaban, A. J. Lakhter, and P. Micevych
A Membrane Estrogen Receptor Mediates Intracellular Calcium Release in Astrocytes
Endocrinology, August 1, 2004; 145(8): 3788 - 3795.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
T. N. Dechow, L. Pedranzini, A. Leitch, K. Leslie, W. L. Gerald, I. Linkov, and J. F. Bromberg
Requirement of matrix metalloproteinase-9 for the transformation of human mammary epithelial cells by Stat3-C
PNAS, July 20, 2004; 101(29): 10602 - 10607.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. Biol.Home page
M. Razandi, A. Pedram, E. M. Rosen, and E. R. Levin
BRCA1 Inhibits Membrane Estrogen and Growth Factor Receptor Signaling to Cell Proliferation in Breast Cancer
Mol. Cell. Biol., July 1, 2004; 24(13): 5900 - 5913.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
M. Maggiolini, A. Vivacqua, G. Fasanella, A. G. Recchia, D. Sisci, V. Pezzi, D. Montanaro, A. M. Musti, D. Picard, and S. Ando
The G Protein-coupled Receptor GPR30 Mediates c-fos Up-regulation by 17{beta}-Estradiol and Phytoestrogens in Breast Cancer Cells
J. Biol. Chem., June 25, 2004; 279(26): 27008 - 27016.
[Abstract] [Full Text] [PDF]

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 JNCI J Natl Cancer InstHome page
J. Shou, S. Massarweh, C. K. Osborne, A. E. Wakeling, S. Ali, H. Weiss, and R. Schiff
Mechanisms of Tamoxifen Resistance: Increased Estrogen Receptor-HER2/neu Cross-Talk in ER/HER2-Positive Breast Cancer
J Natl Cancer Inst, June 16, 2004; 96(12): 926 - 935.
[Abstract] [Full Text] [PDF]

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 Endocr. Rev.Home page
S. K. Dey, H. Lim, S. K. Das, J. Reese, B. C. Paria, T. Daikoku, and H. Wang
Molecular Cues to Implantation
Endocr. Rev., June 1, 2004; 25(3): 341 - 373.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Cell Mol. Bio.Home page
W. Wu, J. M. Samet, R. Silbajoris, L. A. Dailey, D. Sheppard, P. A. Bromberg, and L. M. Graves
Heparin-Binding Epidermal Growth Factor Cleavage Mediates Zinc-Induced Epidermal Growth Factor Receptor Phosphorylation
Am. J. Respir. Cell Mol. Biol., April 1, 2004; 30(4): 540 - 547.
[Abstract] [Full Text] [PDF]

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 Mol Cancer ResHome page
K. Sengupta, S. Banerjee, N. K. Saxena, and S. K. Banerjee
Thombospondin-1 Disrupts Estrogen-Induced Endothelial Cell Proliferation and Migration and Its Expression Is Suppressed by Estradiol
Mol. Cancer Res., March 1, 2004; 2(3): 150 - 158.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
N. Yamanaka, T. Morisaki, H. Nakashima, A. Tasaki, M. Kubo, H. Kuga, C. Nakahara, K. Nakamura, H. Noshiro, T. Yao, et al.
Interleukin 1{beta} Enhances Invasive Ability of Gastric Carcinoma through Nuclear Factor-{kappa}B Activation
Clin. Cancer Res., March 1, 2004; 10(5): 1853 - 1859.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
R. X. Song, C. J. Barnes, Z. Zhang, Y. Bao, R. Kumar, and R. J. Santen
The role of Shc and insulin-like growth factor 1 receptor in mediating the translocation of estrogen receptor {alpha} to the plasma membrane
PNAS, February 17, 2004; 101(7): 2076 - 2081.
[Abstract] [Full Text] [PDF]

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 Circ. Res.Home page
A. Huang, D. Sun, Z. Wu, C. Yan, M. A. Carroll, H. Jiang, J. R. Falck, and G. Kaley
Estrogen Elicits Cytochrome P450--Mediated Flow-Induced Dilation of Arterioles in NO Deficiency: Role of PI3K-Akt Phosphorylation in Genomic Regulation
Circ. Res., February 6, 2004; 94(2): 245 - 252.
[Abstract] [Full Text] [PDF]

Home page
 Circ. Res.Home page
L. Hao, M. Du, A. Lopez-Campistrous, and C. Fernandez-Patron
Agonist-Induced Activation of Matrix Metalloproteinase-7 Promotes Vasoconstriction Through the Epidermal Growth Factor-Receptor Pathway
Circ. Res., January 9, 2004; 94(1): 68 - 76.
[Abstract] [Full Text] [PDF]

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 FASEB J.Home page
A. M. FOWLER, N. SOLODIN, M. T. PREISLER-MASHEK, P. ZHANG, A. V. LEE, and E. T. ALARID
Increases in estrogen receptor-{alpha} concentration in breast cancer cells promote serine 118/104/106-independent AF-1 transactivation and growth in the absence of estrogen
FASEB J, January 1, 2004; 18(1): 81 - 93.
[Abstract] [Full Text] [PDF]

Home page
 Clin. Cancer Res.Home page
R. Schiff, S. A. Massarweh, J. Shou, L. Bharwani, S. K. Mohsin, and C. K. Osborne
Cross-Talk between Estrogen Receptor and Growth Factor Pathways as a Molecular Target for Overcoming Endocrine Resistance
Clin. Cancer Res., January 1, 2004; 10(1): 331S - 336S.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
O. S. Gardner, B. J. Dewar, H. S. Earp, J. M. Samet, and L. M. Graves
Dependence of Peroxisome Proliferator-activated Receptor Ligand-induced Mitogen-activated Protein Kinase Signaling on Epidermal Growth Factor Receptor Transactivation
J. Biol. Chem., November 21, 2003; 278(47): 46261 - 46269.
[Abstract] [Full Text] [PDF]

Home page
 JAMAHome page
P. N. Hopkins and E. A. Brinton
Estrogen Receptor 1 Variants and Coronary Artery Disease: Shedding Light Into a Murky Pool
JAMA, November 5, 2003; 290(17): 2317 - 2319.
[Full Text] [PDF]

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 J. Biol. Chem.Home page
M. Sun, L. Yang, R. I. Feldman, X.-m. Sun, K. N. Bhalla, R. Jove, S. V. Nicosia, and J. Q. Cheng
Activation of Phosphatidylinositol 3-Kinase/Akt Pathway by Androgen through Interaction of p85{alpha}, Androgen Receptor, and Src
J. Biol. Chem., October 31, 2003; 278(44): 42992 - 43000.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Endocrinol.Home page
O. A. Sukocheva, L. Wang, N. Albanese, S. M. Pitson, M. A. Vadas, and P. Xia
Sphingosine Kinase Transmits Estrogen Signaling in Human Breast Cancer Cells
Mol. Endocrinol., October 1, 2003; 17(10): 2002 - 2012.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Endocrinol.Home page
E. R. Levin
Bidirectional Signaling between the Estrogen Receptor and the Epidermal Growth Factor Receptor
Mol. Endocrinol., March 1, 2003; 17(3): 309 - 317.
[Abstract] [Full Text] [PDF]


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