Constitutive Activity of Serotonin Receptor 6 Regulates Human Cerebral Organoids Formation and Depression-like Behaviors

Stem Cell Reports. 2021 Jan 12;16(1):75-88. doi: 10.1016/j.stemcr.2020.11.015. Epub 2020 Dec 23.

Abstract

Serotonin receptor 6 (5-HT6R), a typical G protein-coupled receptor (GPCR) mainly expressed in the neurogenic area with constitutive activity, is of particular interest as a promising target for emotional impairment. Here, we found that 5-HT6R was highly expressed in human NSCs and activation of the receptor promoted self-renewal of human NSCs, and thus induced the expansion and folding of human cerebral organoids; dysfunction of receptor or inhibition of its constitutive activity resulted in the premature differentiation of NSCs, which ultimately depleted the NSC pool. The following mechanistic study revealed that EPAC-CREB signaling was involved in 5-HT6R regulation. Furthermore, we showed that mice with genetic deletion of 5-HT6R or knockin A268R mutant presented depression-like behaviors and impaired hippocampal neurogenesis for progressive decrease of the NSC pool. Thus, this study indicates that the modulation of 5-HT6R and its constitutive activity may provide a therapeutic alternative to alleviate depression.

Keywords: 5-HT(6)R; CRISPR-Cas9; constitutive activity; depression; human neural stem cell; iPSC; neurogenesis; organoids; self-renewal.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Brain / cytology
  • Brain / metabolism*
  • CREB-Binding Protein / metabolism
  • Cell Differentiation
  • Cell Self Renewal / drug effects
  • Depression / pathology*
  • Ethylamines / pharmacology
  • Gene Editing
  • Humans
  • Indoles / pharmacology
  • Mice
  • Mice, Transgenic
  • Mutagenesis, Site-Directed
  • Neural Stem Cells / cytology
  • Neural Stem Cells / metabolism
  • Neurogenesis
  • Organoids / cytology
  • Organoids / metabolism*
  • RNA Interference
  • RNA, Small Interfering / metabolism
  • Receptors, Serotonin / chemistry
  • Receptors, Serotonin / genetics
  • Receptors, Serotonin / metabolism*
  • Signal Transduction
  • rab1 GTP-Binding Proteins / metabolism

Substances

  • 2-(5-chloro-2-methyl-1H-indol-3-yl)-N,N-dimethylethanamine
  • Ethylamines
  • Indoles
  • RNA, Small Interfering
  • Receptors, Serotonin
  • serotonin 6 receptor
  • CREB-Binding Protein
  • CREBBP protein, human
  • rab1 GTP-Binding Proteins