G protein‐coupled estrogen receptor activates cell type‐specific signaling pathways in cortical cultures: relevance to the selective loss of astrocytes
Abstract
Abstract Selective activation of the G protein‐coupled estrogen receptor has been proposed to avoid some of the side effects elicited by the activation of classical estrogen receptors α and β. Although its contribution to neuroprotection triggered by estradiol in brain disorders has been explored, the results regarding ischemic stroke are contradictory, and currently, there is no consensus on the role that this receptor may play. The present study aimed to investigate the role of GPER in the ischemic insult. For that, primary cortical cultures exposed to oxygen and glucose deprivation ( OGD ) were used as a model. Our results demonstrate that neuronal survival was strongly affected by the ischemic insult and concurrent GPER activation with G1 had no further impact. In contrast, OGD had a smaller impact on astrocytes survival but G1, alone or combined with OGD , promoted their apoptosis. This effect was prevented by the GPER antagonist G15. The results also show that ischemia did not change the expression levels of GPER in neurons and astrocytes. In this study, we also demonstrate that selective activation of GPER induced astrocyte apoptosis via the phospholipase C pathway and subsequent intracellular calcium rise, whereas in neurons, this effect was notmore »
- Authors:
-
[1];
[1];
[2]
- CICS‐UBI – Health Sciences Research Centre University of Beira Interior Covilhã Portugal
- CICS‐UBI – Health Sciences Research Centre University of Beira Interior Covilhã Portugal, Faculty of Health Sciences University of Beira Interior Covilhã Portugal
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1492482
- Resource Type:
- Publisher's Accepted Manuscript
- Journal Name:
- Journal of Neurochemistry
- Additional Journal Information:
- Journal Name: Journal of Neurochemistry Journal Volume: 149 Journal Issue: 1; Journal ID: ISSN 0022-3042
- Publisher:
- Wiley-Blackwell
- Country of Publication:
- United Kingdom
- Language:
- English
Citation Formats
Roque, Cláudio, Mendes‐Oliveira, Julieta, and Baltazar, Graça. G protein‐coupled estrogen receptor activates cell type‐specific signaling pathways in cortical cultures: relevance to the selective loss of astrocytes. United Kingdom: N. p., 2019.
Web. doi:10.1111/jnc.14648.
Roque, Cláudio, Mendes‐Oliveira, Julieta, & Baltazar, Graça. G protein‐coupled estrogen receptor activates cell type‐specific signaling pathways in cortical cultures: relevance to the selective loss of astrocytes. United Kingdom. https://doi.org/10.1111/jnc.14648
Roque, Cláudio, Mendes‐Oliveira, Julieta, and Baltazar, Graça. Mon .
"G protein‐coupled estrogen receptor activates cell type‐specific signaling pathways in cortical cultures: relevance to the selective loss of astrocytes". United Kingdom. https://doi.org/10.1111/jnc.14648.
@article{osti_1492482,
title = {G protein‐coupled estrogen receptor activates cell type‐specific signaling pathways in cortical cultures: relevance to the selective loss of astrocytes},
author = {Roque, Cláudio and Mendes‐Oliveira, Julieta and Baltazar, Graça},
abstractNote = {Abstract Selective activation of the G protein‐coupled estrogen receptor has been proposed to avoid some of the side effects elicited by the activation of classical estrogen receptors α and β. Although its contribution to neuroprotection triggered by estradiol in brain disorders has been explored, the results regarding ischemic stroke are contradictory, and currently, there is no consensus on the role that this receptor may play. The present study aimed to investigate the role of GPER in the ischemic insult. For that, primary cortical cultures exposed to oxygen and glucose deprivation ( OGD ) were used as a model. Our results demonstrate that neuronal survival was strongly affected by the ischemic insult and concurrent GPER activation with G1 had no further impact. In contrast, OGD had a smaller impact on astrocytes survival but G1, alone or combined with OGD , promoted their apoptosis. This effect was prevented by the GPER antagonist G15. The results also show that ischemia did not change the expression levels of GPER in neurons and astrocytes. In this study, we also demonstrate that selective activation of GPER induced astrocyte apoptosis via the phospholipase C pathway and subsequent intracellular calcium rise, whereas in neurons, this effect was not observed. Taken together, this evidence supports a direct impact of GPER activity on the viability of astrocytes, which seems to be associated with the regulation of different signaling pathways in astrocytes and neurons. image},
doi = {10.1111/jnc.14648},
journal = {Journal of Neurochemistry},
number = 1,
volume = 149,
place = {United Kingdom},
year = {Mon Jan 28 00:00:00 EST 2019},
month = {Mon Jan 28 00:00:00 EST 2019}
}
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Works referenced in this record:
G Protein–Coupled Estrogen Receptor Agonist Improves Cerebral Microvascular Function After Hypoxia/Reoxygenation Injury in Male and Female Rats
journal, March 2013
- Murata, Takahiro; Dietrich, Hans H.; Xiang, Chuanxi
- Stroke, Vol. 44, Issue 3
Signaling, physiological functions and clinical relevance of the G protein-coupled estrogen receptor GPER
journal, September 2009
- Prossnitz, Eric R.; Barton, Matthias
- Prostaglandins & Other Lipid Mediators, Vol. 89, Issue 3-4
GPR30 estrogen receptor agonists induce mechanical hyperalgesia in the rat
journal, April 2008
- Kuhn, Julia; Dina, Olayinka A.; Goswami, Chandan
- European Journal of Neuroscience, Vol. 27, Issue 7
Beneficial role of the GPR30 agonist G-1 in an animal model of multiple sclerosis
journal, September 2009
- Blasko, Eric; Haskell, Christopher A.; Leung, Stewart
- Journal of Neuroimmunology, Vol. 214, Issue 1-2
GPER Agonist G1 Attenuates Neuroinflammation and Dopaminergic Neurodegeneration in Parkinson Disease
journal, January 2017
- Guan, Jing; Yang, Beibei; Fan, Yi
- Neuroimmunomodulation, Vol. 24, Issue 1
Selective estrogen receptor modulators decrease the production of interleukin-6 and interferon-γ-inducible protein-10 by astrocytes exposed to inflammatory challenge in vitro
journal, January 2010
- Cerciat, M.; Unkila, M.; Garcia-Segura, L. M.
- Glia, Vol. 58, Issue 1
GPR30 Regulates Glutamate Transporter GLT-1 Expression in Rat Primary Astrocytes
journal, May 2012
- Lee, Eunsook; Sidoryk-Wêgrzynowicz, Marta; Wang, Ning
- Journal of Biological Chemistry, Vol. 287, Issue 32
GPR30 co-localizes with cholinergic neurons in the basal forebrain and enhances potassium-stimulated acetylcholine release in the hippocampus
journal, February 2011
- Hammond, R.; Nelson, D.; Gibbs, R. B.
- Psychoneuroendocrinology, Vol. 36, Issue 2
Localisation of GPR30, a novel G protein-coupled oestrogen receptor, suggests multiple functions in rodent brain and peripheral tissues
journal, May 2009
- Hazell, Georgina G. J.; Yao, Song T.; Roper, James A.
- Journal of Endocrinology, Vol. 202, Issue 2
Neurotrophic and neuroprotective actions of estrogen: Basic mechanisms and clinical implications
journal, May 2007
- Brann, Darrell W.; Dhandapani, Krishnan; Wakade, Chandramohan
- Steroids, Vol. 72, Issue 5
Heart Disease and Stroke Statistics—2011 Update: A Report From the American Heart Association
journal, February 2011
- Roger, Véronique L.; Go, Alan S.; Lloyd-Jones, Donald M.
- Circulation, Vol. 123, Issue 4
Estradiol-mediated ERK phosphorylation and apoptosis in vascular smooth muscle cells requires GPR 30
journal, November 2009
- Ding, Qingming; Gros, Robert; Limbird, Lee E.
- American Journal of Physiology-Cell Physiology, Vol. 297, Issue 5
Estrogen Enhances Neurogenesis and Behavioral Recovery after Stroke
journal, July 2010
- Li, Jun; Siegel, Matt; Yuan, Mike
- Journal of Cerebral Blood Flow & Metabolism, Vol. 31, Issue 2
GPER1/GPR30 Activation Improves Neuronal Survival Following Global Cerebral Ischemia Induced by Cardiac Arrest in Mice
journal, September 2012
- Kosaka, Y.; Quillinan, N.; Bond, C. T.
- Translational Stroke Research, Vol. 3, Issue 4
Sphingosine induces apoptosis in hippocampal neurons and astrocytes by activating caspase-3/-9 via a mitochondrial pathway linked to SDK/14-3-3 protein/Bax/cytochrome c
journal, June 2011
- Kanno, Takeshi; Nishizaki, Tomoyuki
- Journal of Cellular Physiology, Vol. 226, Issue 9
Estrogen Signaling through the Transmembrane G Protein–Coupled Receptor GPR30
journal, March 2008
- Prossnitz, Eric R.; Arterburn, Jeffrey B.; Smith, Harriet O.
- Annual Review of Physiology, Vol. 70, Issue 1
Vasodilation in Response to the GPR30 Agonist G-1 is Not Different From Estradiol in the mRen2.Lewis Female Rat
journal, January 2011
- Lindsey, Sarah H.; Carver, Kyle A.; Prossnitz, Eric R.
- Journal of Cardiovascular Pharmacology, Vol. 57, Issue 5
The membrane-type estrogen receptor G-protein-coupled estrogen receptor suppresses lipopolysaccharide-induced interleukin 6 via inhibition of nuclear factor-kappa B pathway in murine macrophage cells
journal, July 2017
- Okamoto, Mariko; Suzuki, Takuto; Mizukami, Yoichi
- Animal Science Journal, Vol. 88, Issue 11
GPER expressed on microglia mediates the anti-inflammatory effect of estradiol in ischemic stroke
journal, March 2016
- Zhao, Tian-Zhi; Ding, Qian; Hu, Jun
- Brain and Behavior, Vol. 6, Issue 4
17β-Estradiol activates GPER- and ESR1-dependent pathways inducing apoptosis in GC-2 cells, a mouse spermatocyte-derived cell line
journal, May 2012
- Chimento, Adele; Sirianni, Rosa; Casaburi, Ivan
- Molecular and Cellular Endocrinology, Vol. 355, Issue 1
Estrogen destabilizes microtubules through an ion-conductivity-independent TRPV1 pathway: TRPV1-C-terminus regulates microtubule stability
journal, May 2011
- Goswami, Chandan; Kuhn, Julia; Dina, Olayinka A.
- Journal of Neurochemistry, Vol. 117, Issue 6
Cloning of Human cDNA Encoding a Novel Heptahelix Receptor Expressed in Burkitt's Lymphoma and Widely Distributed in Brain and Peripheral Tissues
journal, November 1996
- Owman, Christer; Blay, Pilar; Nilsson, Christer
- Biochemical and Biophysical Research Communications, Vol. 228, Issue 2
Identification of a Gene (GPR30) with Homology to the G-Protein-Coupled Receptor Superfamily Associated with Estrogen Receptor Expression in Breast Cancer
journal, November 1997
- Carmeci, Charles; Thompson, Devon A.; Ring, Huijun Z.
- Genomics, Vol. 45, Issue 3
Timing of estrogen therapy after ovariectomy dictates the efficacy of its neuroprotective and antiinflammatory actions
journal, March 2007
- Suzuki, S.; Brown, C. M.; Dela Cruz, C. D.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 14
G protein-coupled estrogen receptor 1-mediated effects in the rat myometrium
journal, November 2011
- Tica, Andrei A.; Dun, Erica C.; Tica, Oana S.
- American Journal of Physiology-Cell Physiology, Vol. 301, Issue 5
GPER: A new tool to protect dopaminergic neurons?
journal, October 2015
- Bessa, Agustina; Campos, Filipa Lopes; Videira, Rita Alexandra
- Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease, Vol. 1852, Issue 10
Estrogen receptors mediate rapid activation of phospholipase C pathway in the rat endometrium
journal, December 2011
- Konigame, Vivian C.; Siu, Erica R.; Royer, Carine
- Steroids, Vol. 76, Issue 14
The Role of Calcium in the Regulation of Apoptosis
journal, October 1997
- McConkey, David J.; Orrenius, Sten
- Biochemical and Biophysical Research Communications, Vol. 239, Issue 2
Membrane Estrogen Receptor Regulates Experimental Autoimmune Encephalomyelitis through Up-regulation of Programmed Death 1
journal, February 2009
- Wang, Chunhe; Dehghani, Babak; Li, Yuexin
- The Journal of Immunology, Vol. 182, Issue 5
Stroke Increases G Protein-Coupled Estrogen Receptor Expression in the Brain of Male but Not Female Mice
journal, January 2013
- Broughton, Brad R. S.; Brait, Vanessa H.; Guida, Elizabeth
- Neurosignals, Vol. 21, Issue 3-4
Activation of G protein-coupled estrogen receptor 1 (GPER-1) ameliorates blood-brain barrier permeability after global cerebral ischemia in ovariectomized rats
journal, August 2016
- Lu, Dan; Qu, Yan; Shi, Fei
- Biochemical and Biophysical Research Communications, Vol. 477, Issue 2
NAD Induces Astrocyte Calcium Flux and Cell Death by ART2 and P2X7 Pathway
journal, September 2012
- Wang, Jianbiao; Yang, Junhua; Liu, Puqing
- The American Journal of Pathology, Vol. 181, Issue 3
Estrogen Replacement Therapy for Stroke
journal, January 2014
- Pabon, Mibel; Tamboli, Cyrus; Tamboli, Sarosh
- Cell Medicine, Vol. 6, Issue 3
Synthetic Estrogen Derivatives Demonstrate the Functionality of Intracellular GPR30
journal, July 2007
- Revankar, Chetana M.; Mitchell, Hugh D.; Field, Angela S.
- ACS Chemical Biology, Vol. 2, Issue 8
GPER activation is effective in protecting against inflammation-induced nigral dopaminergic loss and motor function impairment
journal, August 2017
- Mendes-Oliveira, Julieta; Lopes Campos, Filipa; Videira, Rita Alexandra
- Brain, Behavior, and Immunity, Vol. 64
Estrogens and Experimental Ischemic Stroke: A Systematic Review
journal, January 2006
- Gibson, Claire L.; Gray, Laura J.; Murphy, Sean P.
- Journal of Cerebral Blood Flow & Metabolism, Vol. 26, Issue 9
Insights into Rapid Modulation of Neuroplasticity by Brain Estrogens
journal, August 2013
- Srivastava, Deepak P.; Woolfrey, Kevin M.; Penzes, Peter
- Pharmacological Reviews, Vol. 65, Issue 4
Distribution and characterization of estrogen receptor G protein-coupled receptor 30 in the rat central nervous system
journal, May 2007
- Brailoiu, E.; Dun, S. L.; Brailoiu, G. C.
- Journal of Endocrinology, Vol. 193, Issue 2
Ameliorative effect of membrane-associated estrogen receptor G protein coupled receptor 30 activation on object recognition memory in mouse models of Alzheimer's disease
journal, July 2016
- Kubota, Takashi; Matsumoto, Hiroshi; Kirino, Yutaka
- Journal of Pharmacological Sciences, Vol. 131, Issue 3
Estrogen neuroprotection and the critical period hypothesis
journal, January 2012
- Scott, Erin; Zhang, Quan-guang; Wang, Ruimin
- Frontiers in Neuroendocrinology, Vol. 33, Issue 1
Oestrogen and Nigrostriatal Dopaminergic Neurodegeneration: Animal Models and Clinical Reports of Parkinson'S Disease
journal, July 2007
- Liu, Bin; Dluzen, Dean E.
- Clinical and Experimental Pharmacology and Physiology, Vol. 34, Issue 7
A novel method for culturing stellate astrocytes reveals spatially distinct Ca 2+ signaling and vesicle recycling in astrocytic processes
journal, December 2016
- Wolfes, Anne C.; Ahmed, Saheeb; Awasthi, Ankit
- The Journal of General Physiology, Vol. 149, Issue 1
17β-Estradiol Inhibits Oxidative Stress-Induced Apoptosis in Keratinocytes by Promoting Bcl-2 Expression
journal, December 2003
- Kanda, Naoko; Watanabe, Shinichi
- Journal of Investigative Dermatology, Vol. 121, Issue 6
G Protein-Coupled Estrogen Receptor-Selective Ligands Modulate Endometrial Tumor Growth
journal, January 2013
- Petrie, Whitney K.; Dennis, Megan K.; Hu, Chelin
- Obstetrics and Gynecology International, Vol. 2013
Anti-inflammatory effect of selective estrogen receptor modulators (SERMs) in microglial cells
journal, May 2005
- Suuronen, T.; Nuutinen, T.; Huuskonen, J.
- Inflammation Research, Vol. 54, Issue 5
In vivo effects of a GPR30 antagonist
journal, May 2009
- Dennis, Megan K.; Burai, Ritwik; Ramesh, Chinnasamy
- Nature Chemical Biology, Vol. 5, Issue 6
Antidepressants, sertraline and paroxetine, increase calcium influx and induce mitochondrial damage-mediated apoptosis of astrocytes
journal, December 2017
- Then, Chee-Kin; Liu, Kao-Hui; Liao, Ming-Hsuan
- Oncotarget, Vol. 8, Issue 70
Extra-nuclear estrogen receptor GPR30 regulates serotonin function in rat hypothalamus
journal, February 2009
- Xu, H.; Qin, S.; Carrasco, G. A.
- Neuroscience, Vol. 158, Issue 4
A Transmembrane Intracellular Estrogen Receptor Mediates Rapid Cell Signaling
journal, March 2005
- Revankar, C. M.
- Science, Vol. 307, Issue 5715
Estrogen biology: New insights into GPER function and clinical opportunities
journal, May 2014
- Prossnitz, Eric R.; Barton, Matthias
- Molecular and Cellular Endocrinology, Vol. 389, Issue 1-2
Binding and activation of the seven-transmembrane estrogen receptor GPR30 by environmental estrogens: A potential novel mechanism of endocrine disruption
journal, December 2006
- Thomas, Peter; Dong, Jing
- The Journal of Steroid Biochemistry and Molecular Biology, Vol. 102, Issue 1-5
Estrogen and non-genomic upregulation of voltage-gated Na+ channel activity in MDA-MB-231 human breast cancer cells: Role in adhesion
journal, April 2010
- Fraser, Scott P.; Ozerlat-Gunduz, Iley; Onkal, Rustem
- Journal of Cellular Physiology, Vol. 224, Issue 2
Virtual and biomolecular screening converge on a selective agonist for GPR30
journal, March 2006
- Bologa, Cristian G.; Revankar, Chetana M.; Young, Susan M.
- Nature Chemical Biology, Vol. 2, Issue 4
A novel putative G-protein-coupled receptor expressed in lung, heart and lymphoid tissue
journal, April 1997
- Kvingedal, Ane M.; Smeland, Erlend B.
- FEBS Letters, Vol. 407, Issue 1
Protein Kinase C δ Activates the MEK-ERK Pathway in a Manner Independent of Ras and Dependent on Raf
journal, September 1996
- Ueda, Yoshihiko; Hirai, Syu-ichi; Osada, Shin-ichi
- Journal of Biological Chemistry, Vol. 271, Issue 38
Acute Administration of Non-Classical Estrogen Receptor Agonists Attenuates Ischemia-Induced Hippocampal Neuron Loss in Middle-Aged Female Rats
journal, January 2010
- Lebesgue, Diane; Traub, Michael; De Butte-Smith, Maxine
- PLoS ONE, Vol. 5, Issue 1
GPR30 activation is neither necessary nor sufficient for acute neuroprotection by 17β-estradiol after an ischemic injury in organotypic hippocampal slice cultures
journal, May 2014
- Lamprecht, Michael R.; Morrison, Barclay
- Brain Research, Vol. 1563
Expression and intracellular distribution of the G protein-coupled receptor 30 in rat hippocampal formation
journal, August 2008
- Matsuda, KenIchi; Sakamoto, Hirotaka; Mori, Hiroko
- Neuroscience Letters, Vol. 441, Issue 1
The G-protein-coupled estrogen receptor GPER in health and disease
journal, August 2011
- Prossnitz, Eric R.; Barton, Matthias
- Nature Reviews Endocrinology, Vol. 7, Issue 12
Astrocyte apoptosis: implications for neuroprotection
journal, February 2004
- Takuma, Kazuhiro; Baba, Akemichi; Matsuda, Toshio
- Progress in Neurobiology, Vol. 72, Issue 2
Apoptotic effect of ethanol is potentiated by caffeine-induced calcium release in rat astrocytes
journal, January 2006
- Hirata, Hanako; Machado, Lucas S.; Okuno, Clayton S.
- Neuroscience Letters, Vol. 393, Issue 2-3
Primary culture of cellular subtypes from postnatal mouse for in vitro studies of oxygen glucose deprivation
journal, August 2011
- Jones, Susan M.; Novak, Alicia E.; Elliott, J. Paul
- Journal of Neuroscience Methods, Vol. 199, Issue 2
Impact of Astrocytes on the Injury Induced by In Vitro Ischemia
journal, March 2017
- Roque, Cláudio; Baltazar, Graça
- Cellular and Molecular Neurobiology, Vol. 37, Issue 8
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
journal, January 2002
- Filardo, Edward J.; Quinn, Jeffrey A.; Frackelton, A. Raymond
- Molecular Endocrinology, Vol. 16, Issue 1
Activation of the Novel Estrogen Receptor G Protein-Coupled Receptor 30 (GPR30) at the Plasma Membrane
journal, July 2007
- Filardo, E.; Quinn, J.; Pang, Y.
- Endocrinology, Vol. 148, Issue 7
Estrogen Actions in the Brain and the Basis for Differential Action in Men and Women: A Case for Sex-Specific Medicines
journal, April 2010
- Gillies, Glenda E.; McArthur, Simon
- Pharmacological Reviews, Vol. 62, Issue 2
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
journal, October 2000
- Filardo, Edward J.; Quinn, Jeffrey A.; Bland, Kirby I.
- Molecular Endocrinology, Vol. 14, Issue 10
Expression of estrogen receptor GPR30 in the rat spinal cord and in autonomic and sensory ganglia
journal, May 2009
- Dun, Siok L.; Brailoiu, G. Cristina; Gao, Xin
- Journal of Neuroscience Research, Vol. 87, Issue 7
JNK1 regulates histone acetylation in trigeminal neurons following chemical stimulation
journal, November 2008
- Wu, Jing; Zhang, Xuan; Nauta, Haring J.
- Biochemical and Biophysical Research Communications, Vol. 376, Issue 4
Involvement of Na + -Ca 2+ Exchanger in Reperfusion-induced Delayed Cell Death of Cultured Rat Astrocytes
journal, May 1996
- Matsuda, Toshio; Takuma, Kazuhiro; Nishiguchi, Emi
- European Journal of Neuroscience, Vol. 8, Issue 5
Neuroprotective effects of estrogens following ischemic stroke
journal, July 2009
- Suzuki, Shotaro; Brown, Candice M.; Wise, Phyllis M.
- Frontiers in Neuroendocrinology, Vol. 30, Issue 2
17β-Estradiol Stimulates the Growth of Human Keratinocytes by Inducing Cyclin D2 Expression
journal, August 2004
- Kanda, Naoko; Watanabe, Shinichi
- Journal of Investigative Dermatology, Vol. 123, Issue 2
Apoptosis in Ca 2 + reperfusion injury of cultured astrocytes: roles of reactive oxygen species and NF-κB activation : Astrocyte apoptosis by reactive oxygen species
journal, December 1999
- Takuma, Kazuhiro; Lee, Eibai; Kidawara, Miyuki
- European Journal of Neuroscience, Vol. 11, Issue 12
Discovery of Three Novel G-Protein-Coupled Receptor Genes
journal, January 1998
- O'Dowd, Brian F.; Nguyen, Tuan; Marchese, Adriano
- Genomics, Vol. 47, Issue 2
Sex-Dependent Effects of G Protein–Coupled Estrogen Receptor Activity on Outcome After Ischemic Stroke
journal, March 2014
- Broughton, Brad R. S.; Brait, Vanessa H.; Kim, Hyun Ah
- Stroke, Vol. 45, Issue 3
Cloning of cDNAs Encoding G Protein-Coupled Receptor Expressed in Human Endothelial Cells Exposed to Fluid Shear Stress
journal, November 1997
- Takada, Yoshio; Kato, Chihiro; Kondo, Shuhei
- Biochemical and Biophysical Research Communications, Vol. 240, Issue 3
Reprint of ”GPR30 mediates estrogen rapid signaling and neuroprotection”
journal, May 2014
- Tang, Hui; Zhang, Quanguang; Yang, Licai
- Molecular and Cellular Endocrinology, Vol. 389, Issue 1-2
What Is the Role of Astrocyte Calcium in Neurophysiology?
journal, September 2008
- Agulhon, Cendra; Petravicz, Jeremy; McMullen, Allison B.
- Neuron, Vol. 59, Issue 6