Estrogen enhances linkage in the vascular endothelial calmodulin network via a feedforward mechanism at the G protein-coupled estrogen receptor 1

Journal of Biological Chemistry

Volumn 291, Issue 20, 2016, Pages 10805-10823

  Tran, Quang Kim ^a   Firkins, Rachel ^a   Giles, Jennifer ^a   Francis, Sarah ^a   Matnishian, Vahe ^a   Tran, Phuong ^a   VerMeer, Mark ^a   Jasurda, Jake ^a   Burgard, Michelle Ann ^a   Gebert Oberle, Briana ^a  

^a Des Moines University College of Osteopathic Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CAMS; CELL MEMBRANES; ENDOTHELIAL CELLS; ENZYME ACTIVITY; GENE EXPRESSION; NITRIC OXIDE; PHOSPHORYLATION;

CARDIOVASCULAR TISSUES; ENDOTHELIAL FUNCTION; ENDOTHELIAL NITRIC-OXIDE SYNTHASE (ENOS); ESTROGEN RECEPTOR; FEEDFORWARD LOOPS; RECEPTOR EXPRESSION; TYROSINE PHOSPHORYLATION; VASCULAR ENDOTHELIUM;

CALMODULIN;

ADENOSINE TRIPHOSPHATASE (CALCIUM); CALCIUM ION; CALMODULIN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; EPIDERMAL GROWTH FACTOR RECEPTOR; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR ALPHA; G PROTEIN COUPLED RECEPTOR 30; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; SERINE; PLASMA MEMBRANE CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL MEMBRANE; CELL SPECIFICITY; EMBRYO; ENDOTHELIUM CELL; ENZYME ACTIVITY; FETUS; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; MUTATIONAL ANALYSIS; NEWBORN; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; TRANSACTIVATION; UPREGULATION; VASCULAR ENDOTHELIUM; ANIMAL; CELL CULTURE; CYTOLOGY; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PIG;

ANIMALS; CALCIUM SIGNALING; CALMODULIN; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGENS; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHORYLATION; PLASMA MEMBRANE CALCIUM-TRANSPORTING ATPASES; SWINE;

EID: 84969277689     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.697334     Document Type: Article

References (64)

1. Chakrabarti, S., Morton, J. S., and Davidge, S. T. (2014) Mechanisms of estrogen effects on the endothelium: an overview. Can. J. Cardiol. 30, 705-712
2. Nilsson, S., Mäkelä, S., Treuter, E., Tujague, M., Thomsen, J., Andersson, G., Enmark, E., Pettersson, K., Warner, M., and Gustafsson, J. A. (2001) Mechanisms of estrogen action. Physiol. Rev. 81, 1535-1565
3. Filardo, E. J., and Thomas, P. (2012) Minireview: G protein-coupled estrogen receptor-1, GPER-1: its mechanism of action and role in female reproductive cancer, renal and vascular physiology. Endocrinology 153, 2953-2962
4. Prossnitz, E. R., and Arterburn, J. B. (2015) International Union of Basic and Clinical Pharmacology. XCVII. G protein-coupled estrogen receptor and its pharmacologic modulators. Pharmacol. Rev. 67, 505-540
5. Vivacqua, A., Bonofiglio, D., Recchia, A. G., Musti, A. M., Picard, D., Andò, S., and Maggiolini, M. (2006) The G protein-coupled receptor GPR30 mediates the proliferative effects induced by 17β-estradiol and hydroxytamoxifen in endometrial cancer cells. Mol. Endocrinol. 20, 631-646
6. Vivacqua, A., Bonofiglio, D., Albanito, L., Madeo, A., Rago, V., Carpino, A., Musti, A. M., Picard, D., Andò, S., and Maggiolini, M. (2006) 17β-Estradiol, genistein, and 4-hydroxytamoxifen induce the proliferation of thyroid cancer cells through the G protein-coupled receptor GPR30. Mol. Pharmacol. 70, 1414-1423
7. Albanito, L., Madeo, A., Lappano, R., Vivacqua, A., Rago, V., Carpino, A., Oprea, T. I., Prossnitz, E. R., Musti, A. M., Andò, S., and Maggiolini, M. (2007) G protein-coupled receptor 30 (GPR30) mediates gene expression changes and growth response to 17β-estradiol and selective GPR30 ligand G-1 in ovarian cancer cells. Cancer Res. 67, 1859-1866
8. Santolla, M. F., Lappano, R., De Marco, P., Pupo, M., Vivacqua, A., Sisci, D., Abonante, S., Iacopetta, D., Cappello, A. R., Dolce, V., and Maggiolini, M. (2012) G protein-coupled estrogen receptor mediates the up-regulation of fatty acid synthase induced by 17β-estradiol in cancer cells and cancer-associated fibroblasts. J. Biol. Chem. 287, 43234-43245
9. Filardo, E. J., Quinn, J. A., Bland, K. I., and Frackelton, A. R., Jr. (2000) Estrogen-induced activation of Erk-1 and Erk-2 requires the G proteincoupled receptor homolog, GPR30, and occurs via trans-activation of the epidermal growth factor receptor through release of HB-EGF. Mol. Endocrinol. 14, 1649-1660
10. Revankar, C. M., Cimino, D. F., Sklar, L. A., Arterburn, J. B., and Prossnitz, E. R. (2005) A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science 307, 1625-1630
11. Levitan, I. B. (1999) It is calmodulin after all! Mediator of the calcium modulation of multiple ion channels. Neuron 22, 645-648
12. Jurado, L. A., Chockalingam, P. S., and Jarrett, H. W. (1999) Apocalmodulin. Physiol. Rev. 79, 661-682
13. Shen, X., Valencia, C. A., Szostak, J., Dong, B., and Liu, R. (2005) Scanning the human proteome for calmodulin-binding proteins. Proc. Natl. Acad. Sci. U.S.A. 102, 5969-5974
14. Persechini, A., and Stemmer, P. M. (2002) Calmodulin is a limiting factor in the cell. Trends Cardiovasc. Med. 12, 32-37
15. Kakiuchi, S., Yasuda, S., Yamazaki, R., Teshima, Y., Kanda, K., Kakiuchi, R., and Sobue, K. (1982) Quantitative determinations of calmodulin in the supernatant and particulate fractions of mammalian tissues. J. Biochem. 92, 1041-1048
16. Luby-Phelps, K., Hori, M., Phelps, J. M., and Won, D. (1995) Ca2+-regulated dynamic compartmentalization of calmodulin in living smooth muscle cells. J. Biol. Chem. 270, 21532-21538
17. Tran, Q. K., Black, D. J., and Persechini, A. (2003) Intracellular coupling via limiting calmodulin. J. Biol. Chem. 278, 24247-24250
18. Tran, Q. K., Black, D. J., Persechini, A. (2005) Dominant affectors in the calmodulin network shape the time courses of target responses in the cell. Cell Calcium 37, 541-553
19. Kim, S. A., Heinze, K. G., Waxham, M. N., and Schwille, P. (2004) Intracellular calmodulin availability accessed with two-photon cross-correlation. Proc. Natl. Acad. Sci. U.S.A. 101, 105-110
20. Song, Q., Saucerman, J. J., Bossuyt, J., and Bers, D. M. (2008) Differential integration of Ca2+-calmodulin signal in intact ventricular myocytes at low and high affinity Ca2+-calmodulin targets. J. Biol. Chem. 283, 31531-31540
21. Wu, X., and Bers, D. M. (2007) Free and bound intracellular calmodulin measurements in cardiac myocytes. Cell Calcium 41, 353-364
22. Rakhilin, S. V., Olson, P. A., Nishi, A., Starkova, N. N., Fienberg, A. A., Nairn, A. C., Surmeier, D. J., and Greengard, P. (2004) A network of control mediated by regulator of calcium/calmodulin-dependent signaling. Science 306, 698-701
23. Tran, Q. K., VerMeer, M., Burgard, M. A., Hassan, A. B., and Giles, J. (2015) Hetero-oligomeric complex between the G protein-coupled estrogen receptor 1 and the plasma membrane Ca2+-ATPase 4b. J. Biol. Chem. 290, 13293-13307
24. Watanabe, H., Takahashi, R., Zhang, X. X., Kakizawa, H., Hayashi, H., and Ohno, R. (1996) Inhibition of agonist-induced Ca2+ entry in endothelial cells by myosin light-chain kinase inhibitor. Biochem. Biophys. Res. Commun. 225, 777-784
25. Watanabe, H., Tran, Q. K., Takeuchi, K., Fukao, M., Liu, M. Y., Kanno, M., Hayashi, T., Iguchi, A., Seto, M., and Ohashi, K. (2001) Myosin light-chain kinase regulates endothelial calcium entry and endothelium-dependent vasodilation. FASEB J. 15, 282-284
26. Watanabe, H., Kuhne, W., Spahr, R., Schwartz, P., and Piper, H. M. (1991) Macromolecule permeability of coronary and aortic endothelial monolayers under energy depletion. Am. J. Physiol. 260, H1344-H1352
27. Tran, Q. K., Vermeer, M. (2014) Biosensor-based approach identifies four distinct calmodulin-binding domains in the G Protein-Coupled Estrogen Receptor 1. PLoS One 9, e89669
28. Pfaffl, M. W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45
29. Romoser, V. A., Hinkle, P. M., and Persechini, A. (1997) Detection in living cells of Ca2+-dependent changes in the fluorescence emission of an indicator composed of two green fluorescent protein variants linked by a calmodulin-binding sequence: a new class of fluorescent indicators. J. Biol. Chem. 272, 13270-13274
30. Persechini, A., and Cronk, B. (1999) The relationship between the free concentrations of Ca2+ and Ca2+-calmodulin in intact cells. J. Biol. Chem. 274, 6827-6830
31. Isotani, E., Zhi, G., Lau, K. S., Huang, J., Mizuno, Y., Persechini, A., Geguchadze, R., Kamm, K. E., and Stull, J. T. (2004) Real-time evaluation of myosin light chain kinase activation in smooth muscle tissues from a transgenic calmodulin-biosensor mouse. Proc. Natl. Acad. Sci. U.S.A. 101, 6279-6284
32. Spahr, R., Piper, H. M. (1990) in Cell Culture Techniques in Heart and Vessel Research (Piper, H. M., ed) pp. 220-229, Springer-Verlag, Heidelberg
33. Kuhne, W., Besselmann, M., Noll, T., Muhs, A., Watanabe, H., and Piper, H. M. (1993) Disintegration of cytoskeletal structure of actin filaments in energy-depleted endothelial cells. Am. J. Physiol. 264, H1599-H1608
34. McConnell, E. J., White, G. W., Brokaw, J. J., and Raess, B. U. (2000) Pharmacological and immunohistochemical characterization of calmodulin-stimulated (Ca2+ + Mg2+)-ATPase in cultured porcine aortic endothelial cells. Circ. Res. 86, 191-197
35. Fleming, I., Fisslthaler, B., Dimmeler, S., Kemp, B. E., and Busse, R. (2001) Phosphorylation of Thr495 regulates Ca2+/calmodulin-dependent endothelial nitric oxide synthase activity. Circ. Res. 88, E68-E75
36. Vladusic, E. A., Hornby, A. E., Guerra-Vladusic, F. K., Lakins, J., and Lupu, R. (2000) Expression and regulation of estrogen receptor β in human breast tumors and cell lines. Oncol. Rep. 7, 157-167
37. Filardo, E. J., Quinn, J. A., Frackelton, A. R., Jr., and Bland, K. I. (2002) Estrogen action via theGprotein-coupled receptor, GPR30: stimulation of adenylyl cyclase and cAMP-mediated attenuation of the epidermal growth factor receptor-to-MAPK signaling axis. Mol. Endocrinol. 16, 70-84
38. Filardo, E. J., Quinn, J. A., and Sabo, E. (2008) Association of the membrane estrogen receptor, GPR30, with breast tumor metastasis and transactivation of the epidermal growth factor receptor. Steroids 73, 870-873
39. Castoria, G., Migliaccio, A., Nola, E., and Auricchio, F. (1988) In vitro interaction of estradiol receptor with Ca2+-calmodulin. Mol. Endocrinol. 2, 167-174
40. Li, Z., Joyal, J. L., and Sacks, D. B. (2001) Calmodulin enhances the stability of the estrogen receptor. J. Biol. Chem. 276, 17354-17360
41. Li, L., Li, Z., and Sacks, D. B. (2005) The transcriptional activity of estrogen receptor-α is dependent on Ca2+/calmodulin. J. Biol. Chem. 280, 13097-13104
42. Zhang, Y., Li, Z., Sacks, D. B., and Ames, J. B. (2012) Structural basis for Ca2+-induced activation and dimerization of estrogen receptor α by calmodulin. J. Biol. Chem. 287, 9336-9344
43. Li, L., Li, Z., and Sacks, D. B. (2003) Calmodulin regulates the transcriptional activity of estrogen receptors: selective inhibition of calmodulin function in subcellular compartments. J. Biol. Chem. 278, 1195-1200
44. Li, L., and Sacks, D. B. (2007) Functional interactions between calmodulin and estrogen receptor-α. Cell. Signal. 19, 439-443
45. Ding, Q., Gros, R., Limbird, L. E., Chorazyczewski, J., and Feldman, R. D. (2009) Estradiol-mediated ERK phosphorylation and apoptosis in vascular smooth muscle cells requires GPR 30. Am. J. Physiol. Cell Physiol. 297, C1178-C1187
46. Caride, A. J., Elwess, N. L., Verma, A. K., Filoteo, A. G., Enyedi, A., Bajzer, Z., and Penniston, J. T. (1999) The rate of activation by calmodulin of isoform 4 of the plasma membrane Ca2+ pump is slow and is changed by alternative splicing. J. Biol. Chem. 274, 35227-35232
47. Di Leva, F., Domi, T., Fedrizzi, L., Lim, D., and Carafoli, E. (2008) The plasma membrane Ca2+ ATPase of animal cells: structure, function and regulation. Arch. Biochem. Biophys. 476, 65-74
48. Wang, X., Reznick, S., Li, P., Liang, W., and van Breemen, C. (2002) Ca2+ removal mechanisms in freshly isolated rabbit aortic endothelial cells. Cell Calcium 31, 265-277
49. Dean, W. L., Chen, D., Brandt, P. C., and Vanaman, T. C. (1997) Regulation of platelet plasma membrane Ca2+-ATPase by cAMP-dependent and tyrosine phosphorylation. J. Biol. Chem. 272, 15113-15119
50. Bredt, D. S., and Snyder, S. H. (1990) Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. Proc. Natl. Acad. Sci. U.S.A. 87, 682-685
51. Mount, P. F., Kemp, B. E., and Power, D. A. (2007) Regulation of endothelial and myocardial NO synthesis by multi-site eNOS phosphorylation. J. Mol. Cell Cardiol. 42, 271-279
52. Haynes, M. P., Sinha, D., Russell, K. S., Collinge, M., Fulton, D., Morales-Ruiz, M., Sessa, W. C., and Bender, J. R. (2000) Membrane estrogen receptor engagement activates endothelial nitric oxide synthase via the PI3-kinase-Akt pathway in human endothelial cells. Circ. Res. 87, 677-682
53. Michell, B. J., Harris, M. B., Chen, Z. P., Ju, H., Venema, V. J., Blackstone, M. A., Huang, W., Venema, R. C., and Kemp, B. E. (2002) Identification of regulatory sites of phosphorylation of the bovine endothelial nitric-oxide synthase at serine 617 and serine 635. J. Biol. Chem. 277, 42344-42351
54. Tran, Q. K., Leonard, J., Black, D. J., Nadeau, O. W., Boulatnikov, I. G., and Persechini, A. (2009) Effects of combined phosphorylation at Ser-617 and Ser-1179 in endothelial nitric-oxide synthase on EC50(Ca2+) values for calmodulin binding and enzyme activation. J. Biol. Chem. 284, 11892-11899
55. Tran, Q. K., Leonard, J., Black, D. J., and Persechini, A. (2008) Phosphorylation within an autoinhibitory domain in endothelial nitric oxide synthase reduces the Ca2+ concentrations required for calmodulin to bind and activate the enzyme. Biochemistry 47, 7557-7566
56. Pollock, J. S., Förstermann, U., Mitchell, J. A., Warner, T. D., Schmidt, H. H., Nakane, M., and Murad, F. (1991) Purification and characterization of particulate endothelium-derived relaxing factor synthase from cultured and native bovine aortic endothelial cells. Proc. Natl. Acad. Sci. U.S.A. 88, 10480-10484
57. Das, S. K., Tan, J., Raja, S., Halder, J., Paria, B. C., and Dey, S. K. (2000) Estrogen targets genes involved in protein processing, calcium homeostasis, and Wnt signaling in the mouse uterus independent of estrogen receptor-α and-β. J. Biol. Chem. 275, 28834-28842
58. Albanito, L., Lappano, R., Madeo, A., Chimento, A., Prossnitz, E. R., Cappello, A. R., Dolce, V., Abonante, S., Pezzi, V., and Maggiolini, M. (2015) Effects of atrazine on estrogen receptor α-and G protein-coupled receptor 30-mediated signaling and proliferation in cancer cells and cancerassociated fibroblasts. Environ. Health Perspect. 123, 493-499
59. Pandey, D. P., Lappano, R., Albanito, L., Madeo, A., Maggiolini, M., and Picard, D. (2009) Estrogenic GPR30 signalling induces proliferation and migration of breast cancer cells through CTGF. EMBO J. 28, 523-532
60. Lin, B. C., Suzawa, M., Blind, R. D., Tobias, S. C., Bulun, S. E., Scanlan, T. S., and Ingraham, H. A. (2009) Stimulating the GPR30 estrogen receptor with a novel tamoxifen analogue activates SF-1 and promotes endometrial cell proliferation. Cancer Res. 69, 5415-5423
61. O'Connor, V., El Far, O., Bofill-Cardona, E., Nanoff, C., Freissmuth, M., Karschin, A., Airas, J. M., Betz, H., and Boehm, S. (1999) Calmodulin dependence of presynaptic metabotropic glutamate receptor signaling. Science 286, 1180-1184
62. El-Beialy, W., Galal, N., Deyama, Y., Yoshimura, Y., Suzuki, K., Tei, K., and Totsuka, Y. (2010) Effects of estrogen on PMCA 2 and 4 in human fibroblast-like synovial cells and mouse macrophage-like cells. Endocr. J. 57, 93-97
63. Zhang, R., Liu, Z., Qu, Y., Xu, Y., and Yang, Q. (2013) Two distinct calmodulin binding sites in the third intracellular loop and carboxyl tail of angiotensin II (AT1A) receptor. PLoS One 8, e65266
64. Strehler, E. E., and Zacharias, D. A. (2001) Role of alternative splicing in generating isoform diversity among plasma membrane calcium pumps. Physiol. Rev. 81, 21-50