Proteoglycans involved in bidirectional communication between mast cells and hippocampal neurons
Abstract Background Mast cells (MCs) in the brain can respond to environmental cues and relay signals to neurons that may directly influence neuronal electrical activity, calcium signaling, and neurotransmission. MCs also express receptors for neurotransmitters and consequently can be activated by t...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2019-05-01
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| Series: | Journal of Neuroinflammation |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s12974-019-1504-6 |
| _version_ | 1818554979632283648 |
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| author | Juan Antonio Flores María Pilar Ramírez-Ponce María Ángeles Montes Santiago Balseiro-Gómez Jorge Acosta Guillermo Álvarez de Toledo Eva Alés |
| author_facet | Juan Antonio Flores María Pilar Ramírez-Ponce María Ángeles Montes Santiago Balseiro-Gómez Jorge Acosta Guillermo Álvarez de Toledo Eva Alés |
| author_sort | Juan Antonio Flores |
| collection | DOAJ |
| description | Abstract Background Mast cells (MCs) in the brain can respond to environmental cues and relay signals to neurons that may directly influence neuronal electrical activity, calcium signaling, and neurotransmission. MCs also express receptors for neurotransmitters and consequently can be activated by them. Here, we developed a coculture model of peritoneal MCs, incubated together with dissociated hippocampal neurons for the study of cellular mechanisms involved in the mast cell-neuron interactions. Methods Calcium imaging was used to simultaneously record changes in intracellular calcium [Ca2+]i in neurons and MCs. To provide insight into the contribution of MCs on neurotransmitter release in rat hippocampal neurons, we used analysis of FM dye release, evoked by a cocktail of mediators from MCs stimulated by heat. Results Bidirectional communication is set up between MCs and hippocampal neurons. Neuronal depolarization caused intracellular calcium [Ca2+]i oscillations in MCs that produced a quick response in neurons. Furthermore, activation of MCs with antigen or the secretagogue compound 48/80 also resulted in a neuronal [Ca2+]i response. Moreover, local application onto neurons of the MC mediator cocktail elicited Ca2+ transients and a synaptic release associated with FM dye destaining. Neuronal response was partially blocked by D-APV, a N-methyl-D-aspartate receptor (NMDAR) antagonist, and was inhibited when the cocktail was pre-digested with chondroitinase ABC, which induces enzymatic removal of proteoglycans of chondroitin sulfate (CS). Conclusions MC-hippocampal neuron interaction affects neuronal [Ca2+]i and exocytosis signaling through a NMDAR-dependent mechanism. |
| first_indexed | 2024-12-12T09:47:13Z |
| format | Article |
| id | doaj.art-0c1407c252134a37b6521c505c5e0cf2 |
| institution | Directory Open Access Journal |
| issn | 1742-2094 |
| language | English |
| last_indexed | 2024-12-12T09:47:13Z |
| publishDate | 2019-05-01 |
| publisher | BMC |
| record_format | Article |
| series | Journal of Neuroinflammation |
| spelling | doaj.art-0c1407c252134a37b6521c505c5e0cf22022-12-22T00:28:22ZengBMCJournal of Neuroinflammation1742-20942019-05-0116111310.1186/s12974-019-1504-6Proteoglycans involved in bidirectional communication between mast cells and hippocampal neuronsJuan Antonio Flores0María Pilar Ramírez-Ponce1María Ángeles Montes2Santiago Balseiro-Gómez3Jorge Acosta4Guillermo Álvarez de Toledo5Eva Alés6Dpto. de Fisiología Médica y Biofísica, Facultad de Medicina, Universidad de SevillaDpto. de Fisiología Médica y Biofísica, Facultad de Medicina, Universidad de SevillaDpto. de Fisiología Médica y Biofísica, Facultad de Medicina, Universidad de SevillaDpto. de Fisiología Médica y Biofísica, Facultad de Medicina, Universidad de SevillaDpto. de Fisiología Médica y Biofísica, Facultad de Medicina, Universidad de SevillaDpto. de Fisiología Médica y Biofísica, Facultad de Medicina, Universidad de SevillaDpto. de Fisiología Médica y Biofísica, Facultad de Medicina, Universidad de SevillaAbstract Background Mast cells (MCs) in the brain can respond to environmental cues and relay signals to neurons that may directly influence neuronal electrical activity, calcium signaling, and neurotransmission. MCs also express receptors for neurotransmitters and consequently can be activated by them. Here, we developed a coculture model of peritoneal MCs, incubated together with dissociated hippocampal neurons for the study of cellular mechanisms involved in the mast cell-neuron interactions. Methods Calcium imaging was used to simultaneously record changes in intracellular calcium [Ca2+]i in neurons and MCs. To provide insight into the contribution of MCs on neurotransmitter release in rat hippocampal neurons, we used analysis of FM dye release, evoked by a cocktail of mediators from MCs stimulated by heat. Results Bidirectional communication is set up between MCs and hippocampal neurons. Neuronal depolarization caused intracellular calcium [Ca2+]i oscillations in MCs that produced a quick response in neurons. Furthermore, activation of MCs with antigen or the secretagogue compound 48/80 also resulted in a neuronal [Ca2+]i response. Moreover, local application onto neurons of the MC mediator cocktail elicited Ca2+ transients and a synaptic release associated with FM dye destaining. Neuronal response was partially blocked by D-APV, a N-methyl-D-aspartate receptor (NMDAR) antagonist, and was inhibited when the cocktail was pre-digested with chondroitinase ABC, which induces enzymatic removal of proteoglycans of chondroitin sulfate (CS). Conclusions MC-hippocampal neuron interaction affects neuronal [Ca2+]i and exocytosis signaling through a NMDAR-dependent mechanism.http://link.springer.com/article/10.1186/s12974-019-1504-6Ca2+ imagingneuro-immunehippocampal neurotransmissionNMDA receptorsproteoglycansexocytosis |
| spellingShingle | Juan Antonio Flores María Pilar Ramírez-Ponce María Ángeles Montes Santiago Balseiro-Gómez Jorge Acosta Guillermo Álvarez de Toledo Eva Alés Proteoglycans involved in bidirectional communication between mast cells and hippocampal neurons Journal of Neuroinflammation Ca2+ imaging neuro-immune hippocampal neurotransmission NMDA receptors proteoglycans exocytosis |
| title | Proteoglycans involved in bidirectional communication between mast cells and hippocampal neurons |
| title_full | Proteoglycans involved in bidirectional communication between mast cells and hippocampal neurons |
| title_fullStr | Proteoglycans involved in bidirectional communication between mast cells and hippocampal neurons |
| title_full_unstemmed | Proteoglycans involved in bidirectional communication between mast cells and hippocampal neurons |
| title_short | Proteoglycans involved in bidirectional communication between mast cells and hippocampal neurons |
| title_sort | proteoglycans involved in bidirectional communication between mast cells and hippocampal neurons |
| topic | Ca2+ imaging neuro-immune hippocampal neurotransmission NMDA receptors proteoglycans exocytosis |
| url | http://link.springer.com/article/10.1186/s12974-019-1504-6 |
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