Involvement of Neuronal Tachykinin-like Receptor at 86C in Disc Repair Via Regulation of Kynurenine Metabolism

Overview

Journal iScience

Publisher Cell Press

Date 2023 Aug 28

PMID 37636053

Authors

Soshiro Kashio

Shu Masuda

Masayuki Miura

Affiliations

Soon will be listed here.

Abstract

Neurons contribute to the regeneration of projected tissues; however, it remains unclear whether they are involved in the non-innervated tissue regeneration. Herein, we showed that a neuronal tachykinin-like receptor at 86C (TkR86C) is required for the repair of non-innervated wing discs in . Using a genetic tissue repair system in larvae, we performed genetic screening for G protein-coupled receptors to search for signal mediatory systems for remote tissue repair. An evolutionarily conserved neuroinflammatory receptor, TkR86C, was identified as the candidate receptor. Neuron-specific knockdown of impaired disc repair without affecting normal development. We investigated the humoral metabolites of the kynurenine (Kyn) pathway regulated in the fat body because of their role as tissue repair-mediating factors. Neuronal knockdown of hampered injury-dependent changes in the expression of in the fat body and humoral Kyn metabolites. Our data indicate the involvement of TkR86C neurons upstream of Kyn metabolism in non-autonomous tissue regeneration.

References

Poels J, Birse R, Nachman R, Fichna J, Janecka A, Broeck J . Characterization and distribution of NKD, a receptor for Drosophila tachykinin-related peptide 6. Peptides. 2008; 30(3):545-56. DOI: 10.1016/j.peptides.2008.10.012. View

Deng B, Li Q, Liu X, Cao Y, Li B, Qian Y . Chemoconnectomics: Mapping Chemical Transmission in Drosophila. Neuron. 2019; 101(5):876-893.e4. DOI: 10.1016/j.neuron.2019.01.045. View

Jan Y, Ghysen A, CHRISTOPH I, Barbel S, Jan L . Formation of neuronal pathways in the imaginal discs of Drosophila melanogaster. J Neurosci. 1985; 5(9):2453-64. PMC: 6565306. View

Torosyan R, Huang S, Bommi P, Tiwari R, An S, Schonfeld M . Hypoxic preconditioning protects against ischemic kidney injury through the IDO1/kynurenine pathway. Cell Rep. 2021; 36(7):109547. PMC: 8487442. DOI: 10.1016/j.celrep.2021.109547. View

Makanae A, Hirata A, Honjo Y, Mitogawa K, Satoh A . Nerve independent limb induction in axolotls. Dev Biol. 2013; 381(1):213-26. DOI: 10.1016/j.ydbio.2013.05.010. View

Izumi T, Imai J, Yamamoto J, Kawana Y, Endo A, Sugawara H . Vagus-macrophage-hepatocyte link promotes post-injury liver regeneration and whole-body survival through hepatic FoxM1 activation. Nat Commun. 2018; 9(1):5300. PMC: 6294142. DOI: 10.1038/s41467-018-07747-0. View

Kashio S, Miura M . Kynurenine Metabolism in the Fat Body Non-autonomously Regulates Imaginal Disc Repair in . iScience. 2020; 23(12):101738. PMC: 7756137. DOI: 10.1016/j.isci.2020.101738. View

Nassel D, Zandawala M, Kawada T, Satake H . Tachykinins: Neuropeptides That Are Ancient, Diverse, Widespread and Functionally Pleiotropic. Front Neurosci. 2019; 13:1262. PMC: 6880623. DOI: 10.3389/fnins.2019.01262. View

Garelli A, Heredia F, Casimiro A, Macedo A, Nunes C, Garcez M . Dilp8 requires the neuronal relaxin receptor Lgr3 to couple growth to developmental timing. Nat Commun. 2015; 6:8732. PMC: 4640092. DOI: 10.1038/ncomms9732. View

10.

Inoue A, Raimondi F, Ngako Kadji F, Singh G, Kishi T, Uwamizu A . Illuminating G-Protein-Coupling Selectivity of GPCRs. Cell. 2019; 177(7):1933-1947.e25. PMC: 6773469. DOI: 10.1016/j.cell.2019.04.044. View

11.

Satoh A, Graham G, Bryant S, Gardiner D . Neurotrophic regulation of epidermal dedifferentiation during wound healing and limb regeneration in the axolotl (Ambystoma mexicanum). Dev Biol. 2008; 319(2):321-35. DOI: 10.1016/j.ydbio.2008.04.030. View

12.

Sugiura T, Wang H, Barsacchi R, Simon A, Tanaka E . MARCKS-like protein is an initiating molecule in axolotl appendage regeneration. Nature. 2016; 531(7593):237-40. PMC: 4795554. DOI: 10.1038/nature16974. View

13.

Lee W, Miura M . Mechanisms of systemic wound response in Drosophila. Curr Top Dev Biol. 2014; 108:153-83. DOI: 10.1016/B978-0-12-391498-9.00001-2. View

14.

Kennerdell J, Carthew R . Heritable gene silencing in Drosophila using double-stranded RNA. Nat Biotechnol. 2000; 18(8):896-8. DOI: 10.1038/78531. View

15.

Lee S, Cho E, Yoon S, Kim Y, Kim E . Metabolic control of daily locomotor activity mediated by tachykinin in Drosophila. Commun Biol. 2021; 4(1):693. PMC: 8184744. DOI: 10.1038/s42003-021-02219-6. View

16.

Jiang H, Lkhagva A, Daubnerova I, Chae H, Simo L, Jung S . Natalisin, a tachykinin-like signaling system, regulates sexual activity and fecundity in insects. Proc Natl Acad Sci U S A. 2013; 110(37):E3526-34. PMC: 3773796. DOI: 10.1073/pnas.1310676110. View

17.

Garay E, Schuth N, Barbanente A, Tejeda-Guzman C, Vitone D, Osorio B . Tryptophan regulates zinc stores. Proc Natl Acad Sci U S A. 2022; 119(16):e2117807119. PMC: 9169789. DOI: 10.1073/pnas.2117807119. View

18.

Li F, Huang Q, Chen J, Peng Y, Roop D, Bedford J . Apoptotic cells activate the "phoenix rising" pathway to promote wound healing and tissue regeneration. Sci Signal. 2010; 3(110):ra13. PMC: 2905599. DOI: 10.1126/scisignal.2000634. View

19.

Koto A, Motoyama N, Tahara H, McGregor S, Moriyama M, Okabe T . Oxytocin/vasopressin-like peptide inotocin regulates cuticular hydrocarbon synthesis and water balancing in ants. Proc Natl Acad Sci U S A. 2019; 116(12):5597-5606. PMC: 6431230. DOI: 10.1073/pnas.1817788116. View

20.

Agudelo L, Femenia T, Orhan F, Porsmyr-Palmertz M, Goiny M, Martinez-Redondo V . Skeletal muscle PGC-1α1 modulates kynurenine metabolism and mediates resilience to stress-induced depression. Cell. 2014; 159(1):33-45. DOI: 10.1016/j.cell.2014.07.051. View