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WIREs Membr Transp Signal

Serotonergic signaling: multiple effectors and pleiotropic effects

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Justine Masson, Michel Boris Emerit, Michel Hamon, Michèle Darmon

Published Online: May 09 2012

DOI: 10.1002/wmts.50

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Serotonin (5‐HT) is a neurotransmitter which exerts both central and peripheral control on numerous physiological functions such as sleep/wake cycle, thermoregulation, food intake, nociception, locomotion, sexual behavior, gastrointestinal motility, blood coagulation, and cardiovascular homeostasis. These multiple effects are mediated by a family of serotonin receptors which comprises at least 13 distinct G‐protein‐coupled receptors (GPCRs) of the A type and a combination of ligand‐gated cation channel heteropentameric receptors of the conserved 5‐HT₃ Cys‐loop type. Many of these receptors are targets of pharmaceutical drugs justifying the wide interest to elucidate their functioning. Over the past decades, substantial investigations have led to the current understanding of the complex signal transduction mechanisms which these receptors initiate. The idea of a unique coupling of a receptor to a linear pathway has evolved into a multiplicity of alternative bifurcations and feedback mechanisms. The emerging signaling model includes the capacity of 5‐HT receptors GPCR superfamily to couple and initiate transduction through several G proteins depending on the tissue and/or the presence of interacting proteins. In turn, these G proteins may activate many effectors. On the other hand, the complexity increases further with the capacity of 5‐HT receptors to transduce signals through G‐protein‐independent pathways. These multiple couplings often participate in the control of gene transcription, thereby resulting in 5‐HT‐mediated long‐term (neuroplastic) adaptive functional changes. WIREs Membr Transp Signal 2012, 1:685–713. doi: 10.1002/wmts.50

Figure 1.

5‐HT_1A receptor signaling pathways. The 5‐HT_1AR is negatively coupled to AC/PKA/cAMP signaling via Gα_i/o proteins. Its activation decreases neurotransmitter release in neurons through opposite changes in K⁺ (increase) and Ca²⁺ (decrease) conductances. 5‐HT_1AR stimulation also regulates ERK phosphorylation. See Appendix for the list of abbreviations. Blue arrow, inhibition; red arrow, stimulation.

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Figure 2.

5‐HT_1B receptor signaling pathways. The 5‐HT_1BR is negatively coupled to AC/PKA/cAMP signaling via Gα_i protein. Its activation decreases neurotransmitter release in neurons through opposite changes in K⁺ and Ca²⁺ conductances. Stimulation of nuclear ERK translocation (transcription activation) following 5‐HT_1BR activation depends on kinases' cascade. See Appendix for the list of abbreviations. Blue arrow, inhibition; red arrow, stimulation.

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Figure 3.

5‐HT_2A receptor signaling pathways in muscle and vascular system. The 5‐HT_2AR stimulation induces several pathways via Gα_q protein (PLC/DAG/PKC/ Ca²⁺) and ERK phosphorylation leading to muscular contraction. See Appendix for the list of abbreviations. Blue arrow, inhibition; red arrow, stimulation.

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Figure 4.

5‐HT_2A receptor signaling pathways in neurons. 5‐HT_2AR coupling to PLC /DAG/AC/PKC‐activated pathways produces an inhibition of Ca²⁺ and Na⁺ conductances. The coupling to PLA₂ evokes the release of arachidonic acid. Several kinases' pathways are implicated in modulation of neuron morphology and plasticity via a direct interaction of the C‐terminus with interacting proteins. See Appendix for the list of abbreviations. Blue arrow, inhibition; red arrow, stimulation.

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Figure 5.

5‐HT_2A receptor signaling pathways in mesangial kidney cells. The 5‐HT_2AR is coupled to PLC and PLD via Gα_q protein and plays a role in the control of cell proliferation and fibrosis. See Appendix for the list of abbreviations. Red arrow, stimulation.

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Figure 6.

5‐HT_2B receptor signaling pathways. The 5‐HT_2BR exhibits a wide register of coupling depending on the expressing cell type. Its major coupling lies in an increase in Ca²⁺ flux via PLC/Gα_qcoupling; it may also be coupled to PLA₂. The 5‐HT_2BR activation controls cell proliferation, differentiation, or remodeling using different pathways according to the cell type such as fibroblast, lung vessel cells, or bone mesoblastic cell. See abbreviations' list. Red arrow, stimulation.

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Figure 7.

5‐HT_2C receptor signaling pathways. The 5‐HT_2CR is coupled to PLC in neurons and choroid plexus, and its activation leads to an accumulation of IP3. It inhibits K⁺ conductance in both neurons and choroid plexus and stimulates an apical Cl⁻ conductance in choroid plexus. It may also be coupled to PLD in transfected cells and choroid plexus. See Appendix for the list of abbreviations. Blue arrow, inhibition; red arrow, stimulation.

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Figure 8.

5‐HT₃ receptor signaling pathways in neurons. The 5‐HT₃R, as a member of the ligand‐gated cation channel family, mainly controls Na⁺, K⁺, and Ca²⁺ movements through its channel. Intracellular coupling depends on Ca²⁺ permeability and therefore on subunit composition of the pentamer. See Appendix for the list of abbreviations. Red arrow, stimulation.

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Figure 9.

5‐HT₄ receptor signaling pathways. The 5‐HT₄R is positively coupled to AC through Gα_s and its activation raises cAMP levels. 5‐HT₄R stimulation inhibits K⁺ channel (GIRK) conductance in neurons, but stimulates Ca²⁺ channels in cardiomyocytes resulting in an increased Ca²⁺ transient in heart. The 5‐HT₄R is also implicated in cell survival and spine growth. See Appendix for the list of abbreviations. Blue arrow, inhibition; red arrow, stimulation.

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Figure 10.

5‐HT₅ receptor signaling pathways. The 5‐HT₅R is negatively coupled to AC/PKA/cAMP signaling via Gα_i/o protein. The 5‐HT₅R may also inhibit ADP‐ribosyl cyclase in C6 glioma cells and therefore regulates Ca²⁺ levels. See Appendix for the list of abbreviations. Blue arrow, inhibition; red arrow, stimulation.

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Figure 11.

5‐HT₆ receptor signaling pathways. The 5‐HT₆ receptor is positively coupled to AC/cAMP pathway via Gα_s protein. Its stimulation inhibits K⁺ channel (GIRK) conductance in neurons and activates kinases via a direct interaction of the receptor C‐terminus with interacting proteins, which produces ERK phosphorylation or Jun translocation to the nucleus. See Appendix for the list of abbreviations. Blue arrow, inhibition; red arrow, stimulation.

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Figure 12.

5‐HT₇ receptor signaling pathways. 5‐HT₇R activation elicits Gα_s‐mediated increase in AC activity and cAMP accumulation, and neuronal depolarization by modulating K⁺ and Na⁺conductances. In hippocampal neurons, ERK phosphorylation induced by 5‐HT₇R activation depends on neuronal firing rate. In astrocytoma cells, the 5‐HT₇R stimulation enhances IL‐6 synthesis. See Appendix for the list of abbreviations. Blue arrow, inhibition; red arrow, stimulation.

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Article Title	Serotonergic signaling: multiple effectors and pleiotropic effects
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