G protein-coupled estrogen receptor-mediated effects on cytosolic calcium and nanomechanics in brain microvascular endothelial cells

Journal of Neurochemistry

Volumn 133, Issue 5, 2015, Pages 629-639

  Altmann, Joseph B ^a   Yan, Guang ^a   Meeks, Jeffrey F ^a   Abood, Mary E ^b   Brailoiu, Eugen ^b   Cristina Brailoiu, G ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

atomic force microscopy; blood brain barrier; calcium signaling; cerebral microvasculature; GPER

Indexed keywords

APAMIN; CALCIUM ACTIVATED POTASSIUM CHANNEL; CALCIUM CHANNEL BLOCKING AGENT; CALCIUM ION; CHARIBDOTOXIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; ESTRADIOL; G PROTEIN COUPLED ESTROGEN RECEPTOR; G PROTEIN COUPLED RECEPTOR; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; TAMOXIFEN; TOXIN; UNCLASSIFIED DRUG; CALCIUM; ESTROGEN RECEPTOR;

ANIMAL CELL; ARTICLE; ATOMIC FORCE MICROSCOPY; BRAIN CAPILLARY ENDOTHELIAL CELL; CALCIUM CONDUCTANCE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ELASTICITY; ENZYME MECHANISM; HYPERPOLARIZATION; MEMBRANE POTENTIAL; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RIGIDITY; SENSITIVITY ANALYSIS; AGONISTS; ANIMAL; BIOMECHANICS; BLOOD BRAIN BARRIER; BRAIN CIRCULATION; CAPILLARY; CELL CULTURE; CYTOLOGY; CYTOSOL; ENDOTHELIUM CELL; METABOLISM; PHYSIOLOGY;

RATTUS;

ANIMALS; BIOMECHANICAL PHENOMENA; BLOOD-BRAIN BARRIER; CALCIUM; CAPILLARIES; CELLS, CULTURED; CEREBROVASCULAR CIRCULATION; CYTOSOL; ENDOTHELIAL CELLS; MEMBRANE POTENTIALS; MICROSCOPY, ATOMIC FORCE; NITRIC OXIDE; RATS; RECEPTORS, ESTROGEN; RECEPTORS, G-PROTEIN-COUPLED;

EID: 84928008470     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.13066     Document Type: Article

References (69)

1. Alexander S. P. H., Benson H. E., Faccenda E., Pawson A. J., Sharman J. L., Spedding M., Peters J. A., Harmar A. J., and CGTP Collaborators (2013) The concise guide to PHARMACOLOGY 2013/14: G protein-coupled receptors. Br. J. Pharmacol. 170, 1459-1581.
2. Arce F. T., Whitlock J. L., Birukova A. A., Birukov K. G., Arnsdorf M. F., Lal R., Garcia J. G., and, Dudek S. M., (2008) Regulation of the micromechanical properties of pulmonary endothelium by S1P and thrombin: role of cortactin. Biophys. J. 95, 886-894.
3. Arce F. T., Meckes B., Camp S. M., Garcia J. G., Dudek S. M., and, Lal R., (2013) Heterogeneous elastic response of human lung microvascular endothelial cells to barrier modulating stimuli. Nanomed. Nanotechnol. Biol. Med. 9, 875-884.
4. Ariazi E. A., Brailoiu E., Yerrum S., et al,. (2010) The G protein-coupled receptor GPR30 inhibits proliferation of estrogen receptor-positive breast cancer cells. Cancer Res. 70, 1184-1194.
5. Asl S. Z., Khaksari M., Khachki A. S., Shahrokhi N., and, Nourizade S., (2013) Contribution of estrogen receptors alpha and beta in the brain response to traumatic brain injury. J. Neurosurg. 119, 353-361.
6. Bologa C. G., Revankar C. M., Young S. M., et al,. (2006) Virtual and biomolecular screening converge on a selective agonist for GPR30. Nat. Chem. Biol. 2, 207-212.
7. Brailoiu E., Dun S. L., Brailoiu G. C., Mizuo K., Sklar L. A., Oprea T. I., Prossnitz E. R., and, Dun N. J., (2007) Distribution and characterization of estrogen receptor G protein-coupled receptor 30 in the rat central nervous system. J. Endocrinol. 193, 311-321.
8. Brailoiu G. C., Gurzu B., Gao X., et al,. (2010) Acidic NAADP-sensitive calcium stores in the endothelium: agonist-specific recruitment and role in regulating blood pressure. J. Biol. Chem. 285, 37133-37137.
9. Brailoiu G. C., Oprea T. I., Zhao P., Abood M. E., and, Brailoiu E., (2011) Intracellular cannabinoid type 1 (CB1) receptors are activated by anandamide. J. Biol. Chem. 286, 29166-29174.
10. Brailoiu G. C., Arterburn J. B., Oprea T. I., Chitravanshi V. C., and, Brailoiu E., (2013a) Bradycardic effects mediated by activation of G protein-coupled estrogen receptor in rat nucleus ambiguus. Exp. Physiol. 98, 679-691.
11. Brailoiu G. C., Benamar K., Arterburn J. B., Gao E., Rabinowitz J. E., Koch W. J., and, Brailoiu E., (2013b) Aldosterone increases cardiac vagal tone via G protein-coupled oestrogen receptor activation. J. Physiol. 591, 4223-4235.
12. Brailoiu E., Deliu E., Sporici R. A., Benamar K., and, Brailoiu G. C., (2014) HIV-1-Tat excites cardiac parasympathetic neurons of nucleus ambiguus and triggers prolonged bradycardia in conscious rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 306, R814-R822.
13. Brauner T., Hulser D. F., and, Strasser R. J., (1984) Comparative measurements of membrane potentials with microelectrodes and voltage-sensitive dyes. Biochim. Biophys. Acta 771, 208-216.
14. Broughton B. R., Miller A. A., and, Sobey C. G., (2010) Endothelium-dependent relaxation by G protein-coupled receptor 30 agonists in rat carotid arteries. Am. J. Physiol. Heart Circ. Physiol. 298, H1055-H1061.
15. Burnham M. P., Bychkov R., Feletou M., Richards G. R., Vanhoutte P. M., Weston A. H., and, Edwards G., (2002) Characterization of an apamin-sensitive small-conductance Ca(2+)-activated K(+) channel in porcine coronary artery endothelium: relevance to EDHF. Br. J. Pharmacol. 135, 1133-1143.
16. 2+-activated K+ channel in porcine coronary endothelium: relevance to EDHF. Br. J. Pharmacol. 137, 1346-1354.
17. Cardoso F. L., Brites D., and, Brito M. A., (2010) Looking at the blood-brain barrier: molecular anatomy and possible investigation approaches. Brain Res. Rev. 64, 328-363.
18. Deliu E., Brailoiu G. C., Arterburn J. B., Oprea T. I., Benamar K., Dun N. J., and, Brailoiu E., (2012) Mechanisms of G protein-coupled estrogen receptor-mediated spinal nociception. J. Pain 13, 742-754.
19. Dennis M. K., Field A. S., Burai R., et al,. (2011) Identification of a GPER/GPR30 antagonist with improved estrogen receptor counterselectivity. J. Steroid Biochem. Mol. Biol. 127, 358-366.
20. Favero G., Paganelli C., Buffoli B., Rodella L. F., and, Rezzani R., (2014) Endothelium and its alterations in cardiovascular diseases: life style intervention. Biomed Res. Int. 2014, 801896.
21. Feletou M., (2009) Calcium-activated potassium channels and endothelial dysfunction: therapeutic options? Br. J. Pharmacol. 156, 545-562.
22. Fels J., Callies C., Kusche-Vihrog K., and, Oberleithner H., (2010a) Nitric oxide release follows endothelial nanomechanics and not vice versa. Pflugers Arch. 460, 915-923.
23. Fels J., Oberleithner H., and, Kusche-Vihrog K., (2010b) Menage a trois: aldosterone, sodium and nitric oxide in vascular endothelium. Biochim. Biophys. Acta 1802, 1193-1202.
24. Fels J., Jeggle P., Liashkovich I., Peters W., and, Oberleithner H., (2014) Nanomechanics of vascular endothelium. Cell Tissue Res. 355, 727-737.
25. 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 protein-coupled receptor homolog, GPR30, and occurs via trans-activation of the epidermal growth factor receptor through release of HB-EGF. Mol. Endocrinol. 14, 1649-1660.
26. Filardo E. J., Quinn J. A., Frackelton A. R., Jr, and, Bland K. I., (2002) Estrogen action via the G protein-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.
27. Filardo E., Quinn J., Pang Y., Graeber C., Shaw S., Dong J., and, Thomas P., (2007) Activation of the novel estrogen receptor G protein-coupled receptor 30 (GPR30) at the plasma membrane. Endocrinology 148, 3236-3245.
28. Fleming I., Bauersachs J., and, Busse R., (1997) Calcium-dependent and calcium-independent activation of the endothelial NO synthase. J. Vasc. Res. 34, 165-174.
29. Florian M., Lu Y., Angle M., and, Magder S., (2004) Estrogen induced changes in Akt-dependent activation of endothelial nitric oxide synthase and vasodilation. Steroids 69, 637-645.
30. Furchgott R. F., (1999) Endothelium-derived relaxing factor: discovery, early studies, and identification as nitric oxide. Biosci. Rep. 19, 235-251.
31. Gros R., Ding Q., Sklar L. A., Prossnitz E. E., Arterburn J. B., Chorazyczewski J., and, Feldman R. D., (2011) GPR30 expression is required for the mineralocorticoid receptor-independent rapid vascular effects of aldosterone. Hypertension 57, 442-451.
32. Gros R., Ding Q., Liu B., Chorazyczewski J., and, Feldman R. D., (2013) Aldosterone mediates its rapid effects in vascular endothelial cells through GPER activation. Am. J. Physiol. Cell Physiol. 304, C532-C540.
33. 2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260, 3440-3450.
34. Haas E., Meyer M. R., Schurr U., Bhattacharya I., Minotti R., Nguyen H. H., Heigl A., Lachat M., Genoni M., and, Barton M., (2007) Differential effects of 17beta-estradiol on function and expression of estrogen receptor alpha, estrogen receptor beta, and GPR30 in arteries and veins of patients with atherosclerosis. Hypertension 49, 1358-1363.
35. Haas E., Bhattacharya I., Brailoiu E., et al,. (2009) Regulatory role of G protein-coupled estrogen receptor for vascular function and obesity. Circ. Res. 104, 288-291.
36. + exchange. Cardiovasc. Res. 69, 916-924.
37. Isensee J., Meoli L., Zazzu V., et al,. (2009) Expression pattern of G protein-coupled receptor 30 in LacZ reporter mice. Endocrinology 150, 1722-1730.
38. Kitamura N., Araya R., Kudoh M., et al,. (2009) Beneficial effects of estrogen in a mouse model of cerebrovascular insufficiency. PLoS ONE 4, e5159.
39. Kohler R., Degenhardt C., Kuhn M., Runkel N., Paul M., and, Hoyer J., (2000) Expression and function of endothelial Ca(2+)-activated K(+) channels in human mesenteric artery: a single-cell reverse transcriptase-polymerase chain reaction and electrophysiological study in situ. Circ. Res. 87, 496-503.
40. Kojima H., Nakatsubo N., Kikuchi K., Kawahara S., Kirino Y., Nagoshi H., Hirata Y., and, Nagano T., (1998) Detection and imaging of nitric oxide with novel fluorescent indicators: diaminofluoresceins. Anal. Chem. 70, 2446-2453.
41. Kubes P., and, Granger D. N., (1992) Nitric oxide modulates microvascular permeability. Am. J. Physiol. 262, H611-H615.
42. Kubes P., Suzuki M., and, Granger D. N., (1991) Nitric oxide: an endogenous modulator of leukocyte adhesion. Proc. Natl Acad. Sci. USA 88, 4651-4655.
43. Lee S. Y., Zaske A. M., Novellino T., Danila D., Ferrari M., Conyers J., and, Decuzzi P., (2011) Probing the mechanical properties of TNF-α stimulated endothelial cell with atomic force microscopy. Int. J. Nanomed. 6, 179-195.
44. Lindsey S. H., and, Chappell M. C., (2011) Evidence that the G protein-coupled membrane receptor GPR30 contributes to the cardiovascular actions of estrogen. Gend. Med. 8, 343-354.
45. Lindsey S. H., Yamaleyeva L. M., Brosnihan K. B., Gallagher P. E., and, Chappell M. C., (2011) Estrogen receptor GPR30 reduces oxidative stress and proteinuria in the salt-sensitive female mRen2.Lewis rat. Hypertension 58, 665-671.
46. Lindsey S. H., Liu L., and, Chappell M. C., (2014) Vasodilation by GPER in mesenteric arteries involves both endothelial nitric oxide and smooth muscle cAMP signaling. Steroids 81, 99-102.
47. Maggiolini M., Vivacqua A., Fasanella G., Recchia A. G., Sisci D., Pezzi V., Montanaro D., Musti A. M., Picard D., and, Andò S., (2004) The G protein-coupled receptor GPR30 mediates c-fos up-regulation by 17beta-estradiol and phytoestrogens in breast cancer cells. J. Biol. Chem. 279, 27008-27016.
48. Mathur A. B., Collinsworth A. M., Reichert W. M., Kraus W. E., and, Truskey G. A., (2001) Endothelial, cardiac muscle and skeletal muscle exhibit different viscous and elastic properties as determined by atomic force microscopy. J. Biomech. 34, 1545-1553.
49. Meyer M. R., Baretella O., Prossnitz E. R., and, Barton M., (2010) Dilation of epicardial coronary arteries by the G protein-coupled estrogen receptor agonists G-1 and ICI 182,780. Pharmacology 86, 58-64.
50. Meyer M. R., Field A. S., Kanagy N. L., Barton M., and, Prossnitz E. R., (2012) GPER regulates endothelin-dependent vascular tone and intracellular calcium. Life Sci. 91, 623-627.
51. Moccia F., Berra-Romani R., and, Tanzi F., (2012) Update on vascular endothelial Ca(2+) signalling: a tale of ion channels, pumps and transporters. World J. Biol. Chem. 3, 127-158.
52. Murata T., Dietrich H. H., Xiang C., and, Dacey R. G., Jr, (2013) G protein-coupled estrogen receptor agonist improves cerebral microvascular function after hypoxia/reoxygenation injury in male and female rats. Stroke 44, 779-785.
53. Oberleithner H., Riethmüller C., Ludwig T., Shahin V., Stock C., Schwab A., Hausberg M., Kusche K., and, Schillers H., (2006) Differential action of steroid hormones on human endothelium. J. Cell Sci. 119, 1926-1932.
54. Oberliethner H., Riethmüller C., Schillers H., MacGregor G. A., Wardener H. E., and, Hausberg M., (2007) Plasma sodium stiffens vascular endothelium and reduces nitric oxide release. Proc. Natl Acad. Sci. USA 104, 16281-16286.
55. Olde B., and, Leeb-Lundberg L. M., (2009) GPR30/GPER1: searching for a role in estrogen physiology. Trends Endocrinol. Metab. 20, 409-416.
56. Owman C., Blay P., Nilsson C., and, Lolait S. J., (1996) Cloning of human cDNA encoding a novel heptahelix receptor expressed in Burkitt's lymphoma and widely distributed in brain and peripheral tissues. Biochem. Biophys. Res. Commun. 228, 285-292.
57. Park J. H., Okayama N., Gute D., Krsmanovic A., Battarbee H., and, Alexander J. S., (1999) Hypoxia/aglycemia increases endothelial permeability: role of second messengers and cytoskeleton. Am. J. Physiol. 277, C1066-C1074.
58. Pries A. R., and, Kuebler W. M., (2006) Normal endothelium. Handb. Exp. Pharmacol. 176, 1-40.
59. Prossnitz E. R., and, Barton M., (2011) The G-protein-coupled estrogen receptor GPER in health and disease. Nat. Rev. Endocrinol. 7, 715-726.
60. Prossnitz E. R., and, Barton M., (2014) Estrogen biology: new insights into GPER function and clinical opportunities. Mol. Cell. Endocrinol. 389, 71-83.
61. Prossnitz E. R., Sklar L. A., Oprea T. I., and, Arterburn J. B., (2008) GPR30: a novel therapeutic target in estrogen-related disease. Trends Pharmacol. Sci. 29, 116-123.
62. 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.
63. Sohrabji F., and, Williams M., (2013) Stroke neuroprotection: oestrogen and insulin-like growth factor-1 interactions and the role of microglia. J. Neuroendocrinol. 25, 1173-1181.
64. Takada Y., Kato C., Kondo S., Korenaga R., and, Ando J., (1997) Cloning of cDNAs encoding G protein-coupled receptor expressed in human endothelial cells exposed to fluid shear stress. Biochem. Biophys. Res. Commun. 240, 737-741.
65. Thomas P., Pang Y., Filardo E. J., and, Dong J., (2005) Identity of an estrogen membrane receptor coupled to a G protein in human breast cancer cells. Endocrinology 146, 624-632.
66. Tica A. A., Dun E. C., Tica O. S., Gao X., Arterburn J. B., Brailoiu G. C., Oprea T. I., and, Brailoiu E., (2011) G protein-coupled estrogen receptor 1-mediated effects in the rat myometrium. Am. J. Physiol. Cell Physiol. 301, C1262-C1269.
67. 2+ signaling in the regulation of endothelial permeability. Vascul. Pharmacol. 39, 173-185.
68. 2+ channels in cerebral microvascular endothelial cells and ET-1 biosynthesis. Am. J. Physiol. Cell Physiol. 283, C1687-C1695.
69. Yu X., Li F., Klussmann E., Stallone J. N., and, Han G., (2014) G protein-coupled estrogen receptor 1 (GPER) mediates relaxation of coronary arteries via cAMP/PKA-dependent activation of MLCP. Am. J. Physiol. Endocrinol. Metab. 307, E398-E407.