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Article ; Online: Protocol for identifying physiologically relevant binding proteins of G-protein-coupled receptors.

Huang, Bill X / Kim, Hee-Yong

STAR protocols

2023 Volume 4, Issue 4, Page(s) 102691

Abstract: G-protein-coupled receptors (GPCRs) are important therapeutic targets expressed on the cell surface. Here, we present a protocol for identifying physiologically relevant binding proteins of adhesion GPCR GPR110. We describe steps for in-cell chemical ... ...

Abstract	G-protein-coupled receptors (GPCRs) are important therapeutic targets expressed on the cell surface. Here, we present a protocol for identifying physiologically relevant binding proteins of adhesion GPCR GPR110. We describe steps for in-cell chemical crosslinking, immunoprecipitation, and quantitative high-resolution mass spectrometry. Notably, we detail a label-free quantitation strategy that eliminates irrelevant interacting proteins using an inactive GPR110 mutant with impaired surface expression. Furthermore, we outline procedures for validating the identified partners. For complete details on the use and execution of this protocol, please refer to Huang et al. (2023).
MeSH term(s)	Carrier Proteins ; Receptors, G-Protein-Coupled/genetics ; Cell Membrane ; Immunoprecipitation ; Mass Spectrometry
Chemical Substances	Carrier Proteins ; Receptors, G-Protein-Coupled
Language	English
Publishing date	2023-11-04
Publishing country	United States
Document type	Journal Article
ISSN	2666-1667
ISSN (online)	2666-1667
DOI	10.1016/j.xpro.2023.102691
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Article ; Online: Protocol for identifying physiologically relevant binding proteins of G-protein-coupled receptors

Bill X. Huang / Hee-Yong Kim

STAR Protocols, Vol 4, Iss 4, Pp 102691- (2023)

2023

Abstract: Summary: G-protein-coupled receptors (GPCRs) are important therapeutic targets expressed on the cell surface. Here, we present a protocol for identifying physiologically relevant binding proteins of adhesion GPCR GPR110. We describe steps for in-cell ... ...

Abstract	Summary: G-protein-coupled receptors (GPCRs) are important therapeutic targets expressed on the cell surface. Here, we present a protocol for identifying physiologically relevant binding proteins of adhesion GPCR GPR110. We describe steps for in-cell chemical crosslinking, immunoprecipitation, and quantitative high-resolution mass spectrometry. Notably, we detail a label-free quantitation strategy that eliminates irrelevant interacting proteins using an inactive GPR110 mutant with impaired surface expression. Furthermore, we outline procedures for validating the identified partners.For complete details on the use and execution of this protocol, please refer to Huang et al. (2023).1 : Publisher’s note: Undertaking any experimental protocol requires adherence to local institutional guidelines for laboratory safety and ethics.
Keywords	Proteomics ; Protein expression and purification ; Mass Spectrometry ; Science (General) ; Q1-390
Subject code	570
Language	English
Publishing date	2023-12-01T00:00:00Z
Publisher	Elsevier
Document type	Article ; Online
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Article ; Online: Exacerbating effects of single-dose acute ethanol exposure on neuroinflammation and amelioration by GPR110 (ADGRF1) activation.

Banerjee, Sharmistha / Park, Taeyeop / Kim, Yoo Sun / Kim, Hee-Yong

Journal of neuroinflammation

2023 Volume 20, Issue 1, Page(s) 187

Abstract: Background: Neuroinflammation is a widely studied phenomenon underlying various neurodegenerative diseases. Earlier study demonstrated that pharmacological activation of GPR110 in both central and peripheral immune cells cooperatively ameliorates ... ...

Abstract	Background: Neuroinflammation is a widely studied phenomenon underlying various neurodegenerative diseases. Earlier study demonstrated that pharmacological activation of GPR110 in both central and peripheral immune cells cooperatively ameliorates neuroinflammation caused by systemic lipopolysaccharide (LPS) administration. Ethanol consumption has been associated with exacerbation of neurodegenerative and systemic inflammatory conditions. The goal of this study is to determine the effects of single-dose acute ethanol exposure and GPR110 activation on the neuro-inflammation mechanisms. Methods: For in vivo studies, GPR110 wild type (WT) and knockout (KO) mice at 10-12 weeks of age were given an oral gavage of ethanol (3 g/kg) or maltose (5.4 g/kg) at 1-4 h prior to the injection of LPS (1 mg/kg, i.p.) followed by the GPR110 ligand, synaptamide (5 mg/kg). After 2-24 h, brains were collected for the analysis of gene expression by RT-PCR or protein expression by western blotting and enzyme-linked immunosorbent assay (ELISA). Microglial activation was assessed by western blotting and immunohistochemistry. For in vitro studies, microglia and peritoneal macrophages were isolated from adult WT mice and treated with 25 mM ethanol for 4 h and then with LPS (100 ng/ml) followed by 10 nM synaptamide for 2 h for gene expression and 12 h for protein analysis. Results: Single-dose exposure to ethanol by gavage before LPS injection upregulated pro-inflammatory cytokine expression in the brain and plasma. The LPS-induced Iba-1 expression in the brain was significantly higher after ethanol pretreatment in both WT and GPR110KO mice. GPR110 ligand decreased the mRNA and/or protein expression of these cytokines and Iba-1 in the WT but not in GPR110KO mice. In the isolated microglia and peritoneal macrophages, ethanol also exacerbated the LPS-induced expression of pro-inflammatory cytokines which was mitigated at least partially by synaptamide. The expression of an inflammasome marker NLRP3 upregulated by LPS was further elevated with prior exposure to ethanol, especially in the brains of GPR110KO mice. Both ethanol and LPS reduced adenylate cyclase 8 mRNA expression which was reversed by the activation of GPR110. PDE4B expression at both mRNA and protein level in the brain increased after ethanol and LPS treatment while synaptamide suppressed its expression in a GPR110-dependent manner. Conclusion: Single-dose ethanol exposure exacerbated LPS-induced inflammatory responses. The GPR110 ligand synaptamide ameliorated this effect of ethanol by counteracting on the cAMP system, the common target for synaptamide and ethanol, and by regulating NLRP3 inflammasome.
MeSH term(s)	Animals ; Mice ; Cytokines/metabolism ; Ethanol/toxicity ; Inflammasomes/metabolism ; Ligands ; Lipopolysaccharides/toxicity ; Mice, Inbred C57BL ; Mice, Knockout ; Microglia/metabolism ; Neuroinflammatory Diseases ; NLR Family, Pyrin Domain-Containing 3 Protein/metabolism ; Receptors, G-Protein-Coupled/genetics ; Receptors, G-Protein-Coupled/metabolism ; RNA, Messenger/metabolism
Chemical Substances	Cytokines ; Ethanol (3K9958V90M) ; Inflammasomes ; Ligands ; Lipopolysaccharides ; NLR Family, Pyrin Domain-Containing 3 Protein ; Receptors, G-Protein-Coupled ; RNA, Messenger ; synaptamide ; ADGRF1 protein, mouse
Language	English
Publishing date	2023-08-14
Publishing country	England
Document type	Journal Article
ZDB-ID	2156455-3
ISSN	1742-2094 ; 1742-2094
ISSN (online)	1742-2094
ISSN	1742-2094
DOI	10.1186/s12974-023-02868-w
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Article ; Online: Molecular and Signaling Mechanisms for Docosahexaenoic Acid-Derived Neurodevelopment and Neuroprotection.

Kim, Hee-Yong / Huang, Bill X / Spector, Arthur A

International journal of molecular sciences

2022 Volume 23, Issue 9

Abstract: The neurodevelopmental and neuroprotective actions of docosahexaenoic acid (DHA) are mediated by mechanisms involving membrane- and metabolite-related signal transduction. A key characteristic in the membrane-mediated action of DHA results from the ... ...

Abstract	The neurodevelopmental and neuroprotective actions of docosahexaenoic acid (DHA) are mediated by mechanisms involving membrane- and metabolite-related signal transduction. A key characteristic in the membrane-mediated action of DHA results from the stimulated synthesis of neuronal phosphatidylserine (PS). The resulting DHA-PS-rich membrane domains facilitate the translocation and activation of kinases such as Raf-1, protein kinase C (PKC), and Akt. The activation of these signaling pathways promotes neuronal development and survival. DHA is also metabolized in neural tissues to bioactive mediators. Neuroprotectin D1, a docosatriene synthesized by the lipoxygenase activity, has an anti-inflammatory property, and elovanoids formed from DHA elongation products exhibit antioxidant effects in the retina. Synaptamide, an endocannabinoid-like lipid mediator synthesized from DHA in the brain, promotes neurogenesis and synaptogenesis and exerts anti-inflammatory effects. It binds to the GAIN domain of the GPR110 (ADGRF1) receptor, triggers the cAMP/protein kinase A (PKA) signaling pathway, and activates the cAMP-response element binding protein (CREB). The DHA status in the brain influences not only the PS-dependent signal transduction but also the metabolite formation and expression of pre- and post-synaptic proteins that are downstream of the CREB and affect neurotransmission. The combined actions of these processes contribute to the neurodevelopmental and neuroprotective effects of DHA.
MeSH term(s)	Anti-Inflammatory Agents/pharmacology ; Cyclic AMP Response Element-Binding Protein/metabolism ; Docosahexaenoic Acids/metabolism ; Docosahexaenoic Acids/pharmacology ; Endocannabinoids/metabolism ; Neuroprotection ; Signal Transduction
Chemical Substances	Anti-Inflammatory Agents ; Cyclic AMP Response Element-Binding Protein ; Endocannabinoids ; Docosahexaenoic Acids (25167-62-8)
Language	English
Publishing date	2022-04-22
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2019364-6
ISSN	1422-0067 ; 1422-0067 ; 1661-6596
ISSN (online)	1422-0067
ISSN	1422-0067 ; 1661-6596
DOI	10.3390/ijms23094635
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Article ; Online: Molecular and Signaling Mechanisms for Docosahexaenoic Acid-Derived Neurodevelopment and Neuroprotection

Hee-Yong Kim / Bill X. Huang / Arthur A. Spector

International Journal of Molecular Sciences, Vol 23, Iss 4635, p

2022 Volume 4635

Abstract	The neurodevelopmental and neuroprotective actions of docosahexaenoic acid (DHA) are mediated by mechanisms involving membrane- and metabolite-related signal transduction. A key characteristic in the membrane-mediated action of DHA results from the stimulated synthesis of neuronal phosphatidylserine (PS). The resulting DHA-PS-rich membrane domains facilitate the translocation and activation of kinases such as Raf-1, protein kinase C (PKC), and Akt. The activation of these signaling pathways promotes neuronal development and survival. DHA is also metabolized in neural tissues to bioactive mediators. Neuroprotectin D1, a docosatriene synthesized by the lipoxygenase activity, has an anti-inflammatory property, and elovanoids formed from DHA elongation products exhibit antioxidant effects in the retina. Synaptamide, an endocannabinoid-like lipid mediator synthesized from DHA in the brain, promotes neurogenesis and synaptogenesis and exerts anti-inflammatory effects. It binds to the GAIN domain of the GPR110 (ADGRF1) receptor, triggers the cAMP/protein kinase A (PKA) signaling pathway, and activates the cAMP-response element binding protein (CREB). The DHA status in the brain influences not only the PS-dependent signal transduction but also the metabolite formation and expression of pre- and post-synaptic proteins that are downstream of the CREB and affect neurotransmission. The combined actions of these processes contribute to the neurodevelopmental and neuroprotective effects of DHA.
Keywords	docosahexaenoic acid ; phosphatidylserine ; N -docosahexaenoylphosphatidylethanolamine ; N -docosahexaenoylethanolamine ; synaptamide ; synaptic membrane proteins ; Biology (General) ; QH301-705.5 ; Chemistry ; QD1-999
Subject code	571
Language	English
Publishing date	2022-04-01T00:00:00Z
Publisher	MDPI AG
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Phospholipids: a neuroinflammation emerging target.

Kim, Hee-Yong

Nature chemical biology

2015 Volume 11, Issue 2, Page(s) 99–100

MeSH term(s)	Animals ; Humans ; Immunologic Factors/metabolism ; Lysophospholipids/metabolism ; Male ; Monoacylglycerol Lipases/genetics ; Phospholipases/genetics
Chemical Substances	Immunologic Factors ; Lysophospholipids ; lysophosphatidylserine ; Phospholipases (EC 3.1.-) ; ABHD16A protein, mouse (EC 3.1.1.23) ; Abhd12 protein, mouse (EC 3.1.1.23) ; Monoacylglycerol Lipases (EC 3.1.1.23)
Language	English
Publishing date	2015-01-05
Publishing country	United States
Document type	Journal Article ; Comment
ZDB-ID	2202962-X
ISSN	1552-4469 ; 1552-4450
ISSN (online)	1552-4469
ISSN	1552-4450
DOI	10.1038/nchembio.1740
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Article ; Online: Neuroprotection by docosahexaenoic acid in brain injury.

Kim, Hee-Yong

Military medicine

2014 Volume 179, Issue 11 Suppl, Page(s) 106–111

Abstract: Docosahexaenoic acid (DHA, 22:6 n-3) is an omega-3 polyunsaturated fatty acid highly enriched in the brain and is recognized as an essential nutrient for proper development of brain function. Common brain injuries often cause lifelong neurological and ... ...

Abstract	Docosahexaenoic acid (DHA, 22:6 n-3) is an omega-3 polyunsaturated fatty acid highly enriched in the brain and is recognized as an essential nutrient for proper development of brain function. Common brain injuries often cause lifelong neurological and cognitive impairments, especially in learning and memory. Optimizing the nutritional DHA status in neural tissues may allow significantly improved resilience for the central nervous system to injury and optimized recovery. This article discusses neuroprotective effects of DHA, which are potentially important for improving injury outcome, thus reducing the risk of lifelong neurological impairment associated with brain injury.
MeSH term(s)	Brain Injuries/drug therapy ; Cognition Disorders/prevention & control ; Docosahexaenoic Acids/therapeutic use ; Humans ; Learning Disorders/prevention & control ; Memory Disorders/prevention & control ; Neuroprotective Agents/therapeutic use ; Recovery of Function/drug effects
Chemical Substances	Neuroprotective Agents ; Docosahexaenoic Acids (25167-62-8)
Language	English
Publishing date	2014-11
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Intramural ; Review
ZDB-ID	391061-1
ISSN	1930-613X ; 0026-4075
ISSN (online)	1930-613X
ISSN	0026-4075
DOI	10.7205/MILMED-D-14-00162
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Article ; Online: Interaction between GPR110 (ADGRF1) and tight junction protein occludin implicated in blood-brain barrier permeability

Bill X. Huang / Huazhen Chen / Yuyoung Joo / Heung-Sun Kwon / Cheng Fu / Arthur A. Spector / Hee-Yong Kim

iScience, Vol 26, Iss 4, Pp 106550- (2023)

2023

Abstract: Summary: Activation of adhesion receptor GPR110 by the endogenous ligand synaptamide promotes neurogenesis, neurite growth, and synaptogenesis in developing brains through cAMP signal transduction. However, interacting partners of GPR110 and their ... ...

Abstract	Summary: Activation of adhesion receptor GPR110 by the endogenous ligand synaptamide promotes neurogenesis, neurite growth, and synaptogenesis in developing brains through cAMP signal transduction. However, interacting partners of GPR110 and their involvement in cellular function remain unclear. Here, we demonstrate using chemical crosslinking, affinity purification, and quantitative mass spectrometry that GPR110 interacts with the tight junction adhesion protein occludin. By removing non-specific partners by comparing the binding proteins of GPR110 WT and an inactive mutant exhibiting impaired surface expression, occludin was distinguished as a true binding partner which was further confirmed by reciprocal co-immunoprecipitation assay. Deletion of GPR110 in mice led to the disruption of blood-brain barrier (BBB) and reduced occludin phosphorylation at Y285 in the brain. The Y285 phosphorylation increased upon the ligand-induced activation of GPR110. These data suggest an important role of GPR110-occludin interaction in BBB function and association of previously unknown GPR110-dependent occludin phosphorylation at Y285 with BBB integrity.
Keywords	Biochemistry ; Biomolecules ; Biochemical mechanism ; Science ; Q
Language	English
Publishing date	2023-04-01T00:00:00Z
Publisher	Elsevier
Document type	Article ; Online
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Article ; Online: Ligand-Induced Activation of GPR110 (ADGRF1) to Improve Visual Function Impaired by Optic Nerve Injury

Heung-Sun Kwon / Karl Kevala / Haohua Qian / Mones Abu-Asab / Samarjit Patnaik / Juan Marugan / Hee-Yong Kim

International Journal of Molecular Sciences, Vol 24, Iss 5340, p

2023 Volume 5340

Abstract: It is extremely difficult to achieve functional recovery after axonal injury in the adult central nervous system. The activation of G-protein coupled receptor 110 (GPR110, ADGRF1) has been shown to stimulate neurite extension in developing neurons and ... ...

Abstract	It is extremely difficult to achieve functional recovery after axonal injury in the adult central nervous system. The activation of G-protein coupled receptor 110 (GPR110, ADGRF1) has been shown to stimulate neurite extension in developing neurons and after axonal injury in adult mice. Here, we demonstrate that GPR110 activation partially restores visual function impaired by optic nerve injury in adult mice. Intravitreal injection of GPR110 ligands, synaptamide and its stable analogue dimethylsynaptamide (A8) after optic nerve crush significantly reduced axonal degeneration and improved axonal integrity and visual function in wild-type but not gpr110 knockout mice. The retina obtained from the injured mice treated with GPR110 ligands also showed a significant reduction in the crush-induced loss of retinal ganglion cells. Our data suggest that targeting GPR110 may be a viable strategy for functional recovery after optic nerve injury.
Keywords	synaptamide ; A8 ; axonal degeneration ; retinal ganglion cells ; neuronal survival ; optic nerve crush ; Biology (General) ; QH301-705.5 ; Chemistry ; QD1-999
Language	English
Publishing date	2023-03-01T00:00:00Z
Publisher	MDPI AG
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Emergence of omega-3 fatty acids in biomedical research.

Spector, Arthur A / Kim, Hee-Yong

Prostaglandins, leukotrienes, and essential fatty acids

2018 Volume 140, Page(s) 47–50

Abstract: Shortly after the discovery that linoleic acid was an essential fatty acid in 1930, α-linolenic acid also was reported to prevent the fatty acid deficiency syndrome in animals. However, several prominent laboratories could not confirm the findings with α- ...

Abstract	Shortly after the discovery that linoleic acid was an essential fatty acid in 1930, α-linolenic acid also was reported to prevent the fatty acid deficiency syndrome in animals. However, several prominent laboratories could not confirm the findings with α-linolenic acid, and as a result there was a loss of interest in omega-3 fatty acids in lipid research. Even the findings that a prostaglandin can be synthesized from eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) is necessary for optimum retinal function generated only limited interest in omega-3 fatty acids. The breakthrough came in the 1970s when Dyerberg and Bang reported that the low incidence of atherosclerotic coronary disease in Greenland Eskimos was due to the high marine lipid content of their diet. They subsequently found that EPA, which was increased in Eskimo plasma, inhibited platelet aggregation, and they concluded that the low incidence of coronary artery disease was due to the anti-thrombotic effect of EPA. This stimulated widespread interest and research in EPA and DHA, leading to the present view that, like their omega-6 counterparts, omega-3 fatty acids have important physiological functions and are essential fatty acids.
MeSH term(s)	Animals ; Arachidonic Acid/physiology ; Biomedical Research ; Coronary Artery Disease/blood ; Coronary Thrombosis/blood ; Diet ; Fatty Acids, Omega-3/pharmacology ; Fatty Acids, Omega-3/physiology ; Fibrinolytic Agents/pharmacology ; Humans ; Inuit ; Linoleic Acid/physiology ; Platelet Aggregation/drug effects ; Platelet Aggregation/physiology ; Rats
Chemical Substances	Fatty Acids, Omega-3 ; Fibrinolytic Agents ; Arachidonic Acid (27YG812J1I) ; Linoleic Acid (9KJL21T0QJ)
Language	English
Publishing date	2018-12-03
Publishing country	Scotland
Document type	Journal Article ; Review
ZDB-ID	286714-x
ISSN	1532-2823 ; 0952-3278
ISSN (online)	1532-2823
ISSN	0952-3278
DOI	10.1016/j.plefa.2018.11.017
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