Home LiteratureArticle Details
PMID: 10200323 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Estrogen-induced activation of mitogen-activated protein kinase requires mobilization of intracellular calcium.

Improta-Brears T, Whorton AR, Codazzi F, York JD, Meyer T, McDonnell DP

Abstract

Estrogens and growth factors such as epidermal growth factor (EGF) act as mitogens promoting cellular proliferation in the breast and in the reproductive tract. Although it was considered originally that these agents manifested their mitogenic actions through separate pathways, there is a growing body of evidence suggesting that the EGF and estrogen-mediated signaling pathways are intertwined. Indeed, it has been demonstrated recently that 17beta-estradiol (E2) can induce a rapid activation of mitogen-activated protein kinase (MAPK) in mammalian cells, an event that is independent of both transcription and protein synthesis. In this study, we have used a pharmacological approach to dissect this novel pathway in MCF-7 breast cancer cells and have determined that in the presence of endogenous estrogen receptor, activation of MAPK by E2 is preceded by a rapid increase in cytosolic calcium. The involvement of intracellular calcium in this process was supported by the finding that the presence of EGTA and Ca2+-free medium did not affect the activation of MAPK by E2 and, additionally, that this response was blocked by the addition of the intracellular calcium chelator 1,2-bis(2-aminophenoxy)ethane-N,N,N',N'-tetraacetate. Cumulatively, these data indicate that the estrogen receptor, in addition to functioning as a transcription factor, is also involved, through a nongenomic mechanism, in the regulation of both intracellular calcium homeostasis and MAPK-signaling pathways. Although nongenomic actions of estrogens have been suggested by numerous studies in the past, the ability to link estradiol and the estrogen receptor to a well defined signaling pathway strongly supports a physiological role for this activity.

MeSH Terms
Breast Neoplasms Calcimycin/pharmacology Calcium/metabolism Calcium-Calmodulin-Dependent Protein Kinases/metabolism Cell Nucleus/enzymology Cytoplasm/enzymology Egtazic Acid/pharmacology Enzyme Activation/drug effects Epidermal Growth Factor/pharmacology Estradiol/analogs & derivatives,pharmacology,physiology Estrogen Antagonists/pharmacology Female Fulvestrant HeLa Cells Humans Mitogen-Activated Protein Kinase 1/metabolism Mitogen-Activated Protein Kinase 3 Mitogen-Activated Protein Kinases Recombinant Proteins/pharmacology Tumor Cells, Cultured
Chemicals
Estrogen Antagonists Recombinant Proteins Fulvestrant Calcimycin Estradiol Egtazic Acid Epidermal Growth Factor Calcium-Calmodulin-Dependent Protein Kinases Mitogen-Activated Protein Kinase 1 Mitogen-Activated Protein Kinase 3 Mitogen-Activated Protein Kinases Calcium
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Improta-Brears T
Department of Pharmacology and Cancer Biology, Duke University Medical Center, Durham, NC 27710, USA.
Whorton A R
Codazzi F
York J D
Meyer T
McDonnell D P
References (46)
46 references, click to expand
  1. Differential expression of epidermal growth factor receptor (EGF-R) gene and regulation of EGF-R bioactivity by progesterone and estrogen in the adult mouse uterus.
    Endocrinology. 1994 Feb;134(2):971-81 PMID: 7507841
  2. Ras-dependent mitogen-activated protein kinase activation by G protein-coupled receptors. Convergence of Gi- and Gq-mediated pathways on calcium/calmodulin, Pyk2, and Src kinase.
    J Biol Chem. 1997 Aug 1;272(31):19125-32 PMID: 9235901
  3. A single autophosphorylation site confers oncogenicity to the Neu/ErbB-2 receptor and enables coupling to the MAP kinase pathway.
    EMBO J. 1994 Jul 15;13(14):3302-11 PMID: 7913890
  4. Estrogen action via the cAMP signaling pathway: stimulation of adenylate cyclase and cAMP-regulated gene transcription.
    Proc Natl Acad Sci U S A. 1994 Aug 30;91(18):8517-21 PMID: 8078914
  5. An alternative ligand-independent pathway for activation of steroid receptors.
    Recent Prog Horm Res. 1995;50:333-47 PMID: 7740165
  6. Protein tyrosine kinase PYK2 involved in Ca(2+)-induced regulation of ion channel and MAP kinase functions.
    Nature. 1995 Aug 31;376(6543):737-45 PMID: 7544443
  7. Release of Ca2+ from a nonmitochondrial intracellular store in pancreatic acinar cells by inositol-1,4,5-trisphosphate.
    Nature. 1983 Nov 3-9;306(5938):67-9 PMID: 6605482
  8. The second messenger linking receptor activation to internal Ca release in liver.
    Nature. 1984 May 3-9;309(5963):63-6 PMID: 6325926
  9. Activation of the estrogen receptor through phosphorylation by mitogen-activated protein kinase.
    Science. 1995 Dec 1;270(5241):1491-4 PMID: 7491495
  10. Tyrosine kinase/p21ras/MAP-kinase pathway activation by estradiol-receptor complex in MCF-7 cells.
    EMBO J. 1996 Mar 15;15(6):1292-300 PMID: 8635462
  11. Activation of the unliganded estrogen receptor by EGF involves the MAP kinase pathway and direct phosphorylation.
    EMBO J. 1996 May 1;15(9):2174-83 PMID: 8641283
  12. Calcium influx via the NMDA receptor induces immediate early gene transcription by a MAP kinase/ERK-dependent mechanism.
    J Neurosci. 1996 Sep 1;16(17):5425-36 PMID: 8757255
  13. Activation of mitogen-activated protein (MAP) kinase pathway by pervanadate, a potent inhibitor of tyrosine phosphatases.
    J Biol Chem. 1996 Sep 6;271(36):22251-5 PMID: 8703041
  14. Sequential modification of serines 621 and 624 in the Raf-1 carboxyl terminus produces alterations in its electrophoretic mobility.
    J Biol Chem. 1997 Jan 24;272(4):2136-42 PMID: 8999914
  15. Intracellular calcium-release channels: regulators of cell life and death.
    Am J Physiol. 1997 Feb;272(2 Pt 2):H597-605 PMID: 9124414
  16. Elementary and global aspects of calcium signalling.
    J Physiol. 1997 Mar 1;499 ( Pt 2):291-306 PMID: 9080360
  17. Differential activation of transcription factors induced by Ca2+ response amplitude and duration.
    Nature. 1997 Apr 24;386(6627):855-8 PMID: 9126747
  18. Phospholipase C beta and membrane action of calcitriol and estradiol.
    J Biol Chem. 1997 May 2;272(18):11902-7 PMID: 9115251
  19. Rapid activation of MAP kinase by estrogen in the bone cell line.
    Biochem Biophys Res Commun. 1997 Jun 9;235(1):99-102 PMID: 9196043
  20. Inositol trisphosphate and diacylglycerol as second messengers.
    Biochem J. 1984 Jun 1;220(2):345-60 PMID: 6146314
  21. Regulation of epidermal growth factor receptor by estrogen.
    J Biol Chem. 1985 Aug 15;260(17):9820-4 PMID: 2991264
  22. Effect of estrogen and progesterone treatment on calcium uptake by the myometrium and smooth muscle of the lower urinary tract.
    Eur J Pharmacol. 1986 Aug 7;127(1-2):37-42 PMID: 3758176
  23. Mitogen-stimulated release of inositol phosphates in human fibroblasts.
    Arch Biochem Biophys. 1987 Feb 1;252(2):478-86 PMID: 3028268
  24. Influence of estrogens on mouse uterine epidermal growth factor precursor protein and messenger ribonucleic acid.
    Endocrinology. 1988 Jun;122(6):2355-63 PMID: 3286224
  25. Activation of calcium entry by the tumor promoter thapsigargin in parotid acinar cells. Evidence that an intracellular calcium pool and not an inositol phosphate regulates calcium fluxes at the plasma membrane.
    J Biol Chem. 1989 Jul 25;264(21):12266-71 PMID: 2663854
  26. Inositol polyphosphates and intracellular calcium release.
    Arch Biochem Biophys. 1989 Aug 15;273(1):1-15 PMID: 2667466
  27. Inositol phosphates and cell signalling.
    Nature. 1989 Sep 21;341(6239):197-205 PMID: 2550825
  28. Thapsigargin, a tumor promoter, discharges intracellular Ca2+ stores by specific inhibition of the endoplasmic reticulum Ca2(+)-ATPase.
    Proc Natl Acad Sci U S A. 1990 Apr;87(7):2466-70 PMID: 2138778
  29. Epidermal growth factor replaces estrogen in the stimulation of female genital-tract growth and differentiation.
    Proc Natl Acad Sci U S A. 1991 Jan 1;88(1):21-5 PMID: 1986369
  30. Molecular mechanism of action of a steroid hormone receptor.
    Recent Prog Horm Res. 1991;47:1-24; discussion 24-6 PMID: 1745818
  31. Nuclear localization and regulation of erk- and rsk-encoded protein kinases.
    Mol Cell Biol. 1992 Mar;12(3):915-27 PMID: 1545823
  32. A new, nongenomic estrogen action: the rapid release of intracellular calcium.
    Endocrinology. 1992 Sep;131(3):1305-12 PMID: 1505465
  33. Human T-cell mitogen-activated protein kinase kinases are related to yeast signal transduction kinases.
    J Biol Chem. 1992 Dec 25;267(36):25628-31 PMID: 1281467
  34. Regulation and properties of extracellular signal-regulated protein kinases 1 and 2 in vitro.
    J Biol Chem. 1993 Mar 5;268(7):5097-106 PMID: 8444886
  35. The MAP kinase cascade is essential for diverse signal transduction pathways.
    Trends Biochem Sci. 1993 Apr;18(4):128-31 PMID: 8388132
  36. Signal transduction via the MAP kinases: proceed at your own RSK.
    Proc Natl Acad Sci U S A. 1993 Jul 1;90(13):5889-92 PMID: 8392180
  37. Growth factors induce nuclear translocation of MAP kinases (p42mapk and p44mapk) but not of their activator MAP kinase kinase (p45mapkk) in fibroblasts.
    J Cell Biol. 1993 Sep;122(5):1079-88 PMID: 8394845
  38. Serum-induced translocation of mitogen-activated protein kinase to the cell surface ruffling membrane and the nucleus.
    J Cell Biol. 1993 Sep;122(5):1089-101 PMID: 8394846
  39. Stimulation of estrogen receptor-mediated transcription and alteration in the phosphorylation state of the rat uterine estrogen receptor by estrogen, cyclic adenosine monophosphate, and insulin-like growth factor-I.
    Mol Endocrinol. 1993 Jun;7(6):743-52 PMID: 7689695
  40. The pathway to signal achievement.
    Nature. 1993 Oct 28;365(6449):781-3 PMID: 8413661
  41. Peptide growth factors elicit estrogen receptor-dependent transcriptional activation of an estrogen-responsive element.
    Mol Endocrinol. 1993 Aug;7(8):992-8 PMID: 8232319
  42. 17 beta-estradiol mimics ligand activity of the c-erbB2 protooncogene product.
    Proc Natl Acad Sci U S A. 1993 Nov 15;90(22):10803-7 PMID: 7902571
  43. Cell signaling and estrogens in female rat osteoblasts: a possible involvement of unconventional nonnuclear receptors.
    J Bone Miner Res. 1993 Nov;8(11):1365-76 PMID: 8266828
  44. Susceptibility to virus infection is determined by a Stat-mediated response to the autocrine effect of virus-induced type I interferon.
    Cytokine. 1997 Jun;9(6):383-93 PMID: 9199872
  45. Estrogen: nontranscriptional signaling pathway.
    Recent Prog Horm Res. 1997;52:33-68; discussion 68-9 PMID: 9238847
  46. Ras-dependent activation of MAP kinase pathway mediated by G-protein beta gamma subunits.
    Nature. 1994 Jun 2;369(6479):418-20 PMID: 8196770
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1999-04-13
Pages
4686-91
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC16393
Subset
IM
Grants
NIDDK NIH HHS · R01 DK048807 · United States
NIDDK NIH HHS · R37 DK048807 · United States
NIDDK NIH HHS · DK48807 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com