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Vol. 53, Issue 1, 25-72, March 2001

Cellular and Molecular Pharmacology of Antiestrogen Action and Resistance

Robert Clarke1, Fabio Leonessa, James N. Welch and Todd C. Skaar

Vincent T. Lombardi Cancer Center, Georgetown University School of Medicine, Washington, DC

I. Introduction
    A. Role of Estrogens in Affecting Breast Cancer Risk and Progression
    B. Antiestrogens: Partial Agonists and Antagonists
    C. Response Rates to Tamoxifen and Expression of Steroid Hormone Receptors
    D. Overview of Antiestrogen Resistance Mechanisms
II. Endogenous and Exogenous Estrogens in Antiestrogen Resistance
    A. Origins of Intratumor Estrogens
    B. Intratumor Estrogen Concentrations
    C. Does the Pituitary-Ovarian Axis Affect Response to Tamoxifen in Premenopausal Women?
    D. Can Endogenous Estrogens or Hormone Replacement Therapies Produce Antiestrogen Resistance?
III. Pharmacokinetics in Resistance to Tamoxifen
    A. Basic Pharmacology of Tamoxifen
    B. Intracellular Antiestrogen Binding Sites
    C. Binding to Plasma Membranes
    D. Altered Drug Accumulation/Transport and P-glycoprotein (mdr1)
    E. Metabolism and Resistance
    F. Comments
IV. Cell Culture Models of Antiestrogen Responsiveness and Resistance
    A. R27 and LY2
    B. MCF-7RR
    C. The LCC Series
    D. ZR-75-9a1
    E. Resistance Phenotypes Implied by Cell Culture Models
V. Tamoxifen-Stimulated Proliferation as a Resistance Mechanism
    A. In Vivo Selection against Tamoxifen or ICI 182,780
    B. MCF-WES and MCF/TOT
    C. Fibroblast Growth Factor-Transfected MCF-7 Variants and Their Role(s) in Antiestrogen Resistance
    D. Angiogenesis and Tamoxifen Resistance
    E. Tamoxifen Stimulation as a Resistance Phenotype in Patients and Tamoxifen Flare
VI. Estrogen Receptors, Mutant Receptors, Coregulators, and Gene Networks
    A. Wild-Type and Mutant Estrogen Receptor-alpha and Estrogen Receptor-beta
    B. Coregulators of Estrogen Receptor Action
    C. Estrogenic and Antiestrogenic Regulation of Mitogen-Activated Protein Kinase
    D. Regulation of Gene Networks by Receptor Cross-Talk: Mitogen-Activated Protein Kinase Activation and Estrogen Receptor Function
    E. Mitogen-Activated Protein Kinases in Mediating the Effects of Estrogens and Conferring Antiestrogen Resistance
    F. Estrogen Receptor Signaling through AP-1 and Antiestrogen Resistance
    G. Signaling to Mitogenesis or Apoptosis in Antiestrogen Resistance
VII. Growth Factors as Mediators of Antiestrogen Resistance
    A. Gene Networks: Growth Factors, Their Receptors, and Cellular Signaling
    B. Epidermal Growth Factor, Transforming Growth Factor-alpha , and Other Family Members
    C. Epidermal Growth Factor-Receptor and c-erb-B2
    D. Tranforming Growth Factor-beta Family
    E. Insulin-Like Growth Factors, Their Receptors, and Binding Proteins
VIII. Estrogen Receptor-Independent Targets for Mediating Antiestrogen Action and Resistance
    A. Oxidative Stress
    B. Perturbations in Membrane Structure/Function
    C. Protein Kinase C
    D. Calmodulin
    E. Comments on the Possible Role of Nongenomic Effects
IX. Immunologic Mechanisms of Tamoxifen Resistance
    A. Cell-Mediated Immunity
    B. Natural Killer Cells
    C. Macrophages
    D. Lymphokine-Activated Killer Cells, Cytotoxic T Cells, and Other Cell-Mediated Immunity Effector Cells
    E. Humoral Immunity
X. Conclusions and Future Prospects
Acknowledgments
References

Antiestrogen therapy remains one of the most widely used and effective treatments for the management of endocrine responsive breast cancers. This reflects the ability of antiestrogens to compete with estrogens for binding to estrogen receptors. Whereas response rates of up to 70% are reported in patients with tumors expressing estrogen and progesterone receptors, most responsive tumors will eventually acquire resistance. The most important factor in de novo resistance is lack of expression of these receptors. However, the mechanisms driving resistance in tumors that express estrogen and/or progesterone receptors are unclear. A tamoxifen-stimulated phenotype has been described, but seems to occur only in a minority of patients. Most tumors (>80%) may become resistant through other, less well defined, resistance mechanisms. These may be multifactorial, including changes in immunity, host endocrinology, and drug pharmacokinetics. Significant changes within the tumor cells may also occur, including alterations in the ratio of the estrogen receptor alpha :beta forms and/or other changes in estrogen receptor-driven transcription complex function. These may lead to perturbations in the gene network signaling downstream of estrogen receptors. Cells may also alter paracrine and autocrine growth factor interactions, potentially producing a ligand-independent activation of estrogen receptors by mitogen-activated protein kinases. Antiestrogens can affect the function of intracellular proteins and signaling that may, or may not, involve estrogen receptor-mediated events. These include changes in oxidative stress responses, specific protein kinase C isoform activation, calmodulin function, and cell membrane structure/function.

1 Address for correspondence: Robert Clarke, Ph.D., D.Sc., W405A Research Building, Vincent T. Lombardi Cancer Center, Georgetown University School of Medicine, 3970 Reservoir Rd., NW, Washington, DC 20007. E-mail: clarker{at}gunet.georgetown.edu

0031-6997/01/5301-0025$03.00/0
PHARMACOLOGICAL REVIEWS
Copyright © 2001 by The American Society for Pharmacology and Experimental Therapeutics


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J. M. Garcia Pedrero, B. del Rio, C. Martinez-Campa, M. Muramatsu, P. S. Lazo, and S. Ramos
Calmodulin Is a Selective Modulator of Estrogen Receptors
Mol. Endocrinol., May 1, 2002; 16(5): 947 - 960.
[Abstract] [Full Text] [PDF]