Role of neuronal and non-neuronal acetylcholine signaling in Drosophila humoral immunity. (February 2023)

• Record Type: Journal Article
• Authors: Giordani, Giorgia; Cattabriga, Giulia; Becchimanzi, Andrea; Di Lelio, Ilaria; De Leva, Giovanna; Gigliotti, Silvia; Pennacchio, Francesco; Gargiulo, Giuseppe; Cavaliere, Valeria
• Is Part Of: Insect biochemistry and molecular biology. Volume 153(2023)
• Publication Date: 2023-02
• Subjects: Innate immunity -- Acetylcholine -- Nicotinic acetylcholine receptors -- Neuroimmunity; Insect biochemistry -- Periodicals; Insects -- Physiology -- Periodicals; Insects -- Molecular aspects -- Periodicals; Biochemistry -- Periodicals; Insectes -- Biochimie -- Périodiques; Insectes -- Composition -- Périodiques; Insectes -- Physiologie -- Périodiques; Insectes -- Aspect moléculaire -- Périodiques; Biochimie -- Périodiques; Biochemistry; Insect biochemistry; Insects -- Molecular aspects; Insects -- Physiology; Periodicals; 572.8157
• DOI: 10.1016/j.ibmb.2022.103899
• Languages: English
• ISSNs: 0965-1748

Abstract

Abstract : Acetylcholine (ACh) is one the major neurotransmitters in insects, whose role in mediating synaptic interactions between neurons in the central nervous system is well characterized. It also plays largely unexplored regulatory functions in non-neuronal tissues. Here we demonstrate that ACh signaling is involved in the modulation of the innate immune response of Drosophila melanogaster . Knockdown of ACh synthesis or ACh vesicular transport in neurons reduced the activation of drosomycin ( drs ), a gene encoding an antimicrobial peptide, in adult flies infected with a Gram-positive bacterium. drs transcription was similarly affected in Drosophila α7 nicotinic acetylcholine receptor, nAChRalpha7 (Dα7) mutants, as well as in flies expressing in the nervous system a dominant negative form (Dα7 DN ) of this specific receptor subunit. Interestingly, Dα7 DN elicited a comparable response when it was expressed in non-neuronal tissues and even when it was specifically produced in the hemocytes. Consistently, full activation of the drs gene required Dα7 expression in these cells. Moreover, knockdown of ACh synthesis in non-neuronal cells affected drs expression. Overall, these findings uncover neural and non-neural cholinergic signals that modulate insect immune defenses and shed light on the role of hemocytes in the regulation of the humoral immune response. Graphical abstract: Image 1 Highlights: Acetylcholine positively modulates Drosophila drosomycin gene expression. Nicotinic acetylcholine receptor Dα7 is involved in the immune response. Neuronal and non-neuronal cholinergic signaling modulates immunity.