The FMRFamide-like peptide FLP-11 regulates the production and secretion of the TGF-β-like protein DAF-7 during Caenorhabditis elegans larval development

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The FMRFamide-like peptide FLP-11 regulates the production and secretion of the TGF-β-like protein DAF-7 during Caenorhabditis elegans larval development

References

  1. Quillet, R. et al. RF-amide neuropeptides and their receptors in mammals: Pharmacological properties, drug development and main physiological functions. Pharmacol. Ther. 160, 84–132. https://doi.org/10.1016/j.pharmthera.2016.02.005 (2016).

    Google Scholar 

  2. Nagata, S. FMRFamides. In Comparative Endocrinology of Basic and Clinical Research. 432–433 (eds Ando, H., Ukena, K. & Nagata, S.) (Academic Press, 2016).

  3. Peymen, K., Watteyne, J., Frooninckx, L., Schoofs, L. & Beets, I. The FMRFamide-like peptide family in nematodes. Front. Endocrinol. (Lausanne). 5, 90. https://doi.org/10.3389/fendo.2014.00090 (2014).

    Google Scholar 

  4. Kaletta, T. & Hengartner, M. O. Finding function in novel targets: C. elegans as a model organism. Nat. Rev. Drug Discov. 5, 387–399. (2006).

  5. Chang, Y. J. et al. Modulation of locomotion and reproduction by FLP neuropeptides in the nematode Caenorhabditis elegans. PLoS One. 10, e0135164. https://doi.org/10.1371/journal.pone.0135164 (2015).

    Google Scholar 

  6. Turek, M., Besseling, J., Spies, J. P., König, S. & Bringmann, H. Sleep-active neuron specification and sleep induction require FLP-11 neuropeptides to systemically induce sleep. Elife 5, e12499. https://doi.org/10.7554/eLife.12499 (2016).

    Google Scholar 

  7. Nath, R. D., Chow, E. S., Wang, H., Schwarz, E. M. & Sternberg, P. W. C. elegans stress-induced sleep emerges from the collective action of multiple neuropeptides. Curr. Biol. 26, 2446–2455. https://doi.org/10.1016/j.cub.2016.07.048 (2016).

    Google Scholar 

  8. Lee, J. et al. (ed, S.) FMRFamide-like peptides expand the behavioral repertoire of a densely connected nervous system. Proc. Natl. Acad. Sci. U S A 114 E10726–E10735 https://doi.org/10.1073/pnas.1710374114 (2017).

    Google Scholar 

  9. Chew, Y. L. et al. An afferent neuropeptide system transmits mechanosensory signals triggering sensitization and arousal in C. elegans. Neuron 99, 1233–1246. https://doi.org/10.1016/j.neuron.2018.08.003 (2018).

    Google Scholar 

  10. Marques, F., Falquet, L., Vandewyer, E., Beets, I. & Glauser, D. A. Signaling via the FLP-14/FRPR-19 neuropeptide pathway sustains nociceptive response to repeated noxious stimuli in C. elegans. PLoS Genet. 17, e1009880. https://doi.org/10.1371/journal.pgen.1009880 (2021).

    Google Scholar 

  11. Reilly, D. K. et al. Distinct neuropeptide-receptor modules regulate a sex-specific behavioral response to a pheromone. Commun. Biol. 4, 1018. https://doi.org/10.1038/s42003-021-02547-7 (2021).

    Google Scholar 

  12. Busack, I. & Bringmann, H. A sleep-active neuron can promote survival while sleep behavior is disturbed. PLoS Genet. 19, e1010665. https://doi.org/10.1371/journal.pgen.1010665 (2023).

    Google Scholar 

  13. Nose, M. et al. Protein Research Foundation,. Regulatory mechanism of larval diapause by a C. elegans neuropeptide, FLP-3. In Peptide Science 2021 (ed. Hayashi, Y.) 91–94. (2022).

  14. Ono, M., Hori, Y., Matsunaga, Y., Iwasaki, T. & Kawano, T. Regulatory mechanism of larval diapause by a C. elegans neuropeptide, FLP-6 in the intestine. In Peptide Science 2021 (ed. Hayashi, Y.) 87–90. (Protein Research Foundation, 2022).

  15. Kageyama, N. et al. The FMRFamide-like peptide FLP-2 is involved in the modulation of larval development and adult lifespan by regulating the secretion of the insulin-like peptide INS-35 in Caenorhabditis elegans. Biosci. Biotechnol. Biochem. 86, 1231–1239. https://doi.org/10.1093/bbb/zbac108 (2022).

    Google Scholar 

  16. Une, R. et al. The FMRFamide-like peptide FLP-1 modulates larval development by regulating the production and secretion of the insulin-like peptide DAF-28 in Caenorhabditis elegans. Biosci. Biotechnol. Biochem. 87, 171–178. https://doi.org/10.1093/bbb/zbac187 (2023).

    Google Scholar 

  17. Hu, P. J. Dauer in WormBook (ed. The C. elegans Research Community). https://doi.org/10.1895/wormbook.1.144.1 (2007).

  18. Li, W., Kennedy, S. G. & Ruvkun, G. daf-28 encodes a C. elegans insulin superfamily member that is regulated by environmental cues and acts in the DAF-2 signaling pathway. Genes Dev. 17, 844–848. https://doi.org/10.1101/gad.1066503 (2003).

    Google Scholar 

  19. Kimura, K. D., Tissenbaum, H. A., Liu, Y. & Ruvkun, G. daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 277, 942–946. https://doi.org/10.1126/science (1997).

    Google Scholar 

  20. Ren, P. & et el. Control of C. elegans larval development by neuronal expression of a TGF-beta homolog. Science 274, 1389–1391. https://doi.org/10.1126/science.274.5291.1389 (1996).

    Google Scholar 

  21. Bargmann, C. I. & Horvitz, H. R. Control of larval development by chemosensory neurons in Caenorhabditis elegans. Science 251, 1243–1246. https://doi.org/10.1126/science.2006412 (1991).

    Google Scholar 

  22. Matsunaga, Y. et al. Diapause is associated with a change in the Polarity of secretion of insulin-like peptides. Nat. Commun. 7, 10573. https://doi.org/10.1038/ncomms10573 (2016).

    Google Scholar 

  23. Honda, Y. et al. Genes down-regulated in spaceflight are involved in the control of longevity in Caenorhabditis elegans. Sci. Rep. 2, 487. https://doi.org/10.1038/srep00487 (2012).

    Google Scholar 

  24. Ono, M. et al. The G protein-coupled receptor neuropeptide receptor-15 modulates larval development via the transforming growth factor-β DAF-7 protein in Caenorhabditis elegans. Biochem. Biophys. Res. Commun. 660, 28–34. https://doi.org/10.1016/j.bbrc.2023.03.080 (2023).

    Google Scholar 

  25. Fares, H. & Greenwald, I. Genetic analysis of endocytosis in Caenorhabditis elegans: coelomocyte uptake defective mutants. Genetics 159, 133–145. https://doi.org/10.1093/genetics/159.1.133 (2001).

    Google Scholar 

  26. Kao, G. et al. ASNA-1 positively regulates insulin secretion in C. elegans and mammalian cells. Cell 128, 577–587. https://doi.org/10.1016/j.cell.2006.12.031 (2007).

    Google Scholar 

  27. Gengyo-Ando, K. & Mitani, S. Characterization of mutations induced by Ethyl methanesulfonate, UV, and trimethylpsoralen in the nematode Caenorhabditis elegans. Biochem. Biophys. Res. Commun. 269, 64–69. https://doi.org/10.1006/bbrc.2000.2260 (2000).

    Google Scholar 

  28. Georgi, L. L., Albert, P. S. & Riddle, D. L. daf-1, a C. elegans gene controlling Dauer larva development, encodes a novel receptor protein kinase. Cell 61, 635–645. https://doi.org/10.1016/0092-8674(90)90475-t (1990).

    Google Scholar 

  29. Patterson, G. I., Koweek, A., Wong, A., Liu, Y. & Ruvkun, G. The DAF-3 Smad protein antagonizes TGF-beta-related receptor signaling in the Caenorhabditis elegans Dauer pathway. Genes Dev. 11, 2679–2690. https://doi.org/10.1101/gad.11.20.2679 (1997).

    Google Scholar 

  30. Lin, K., Dorman, J. B., Rodan, A. & Kenyon, C. daf-16: an HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science 278, 1319–1322. https://doi.org/10.1126/science.278.5341.1319 (1997).

    Google Scholar 

  31. Ogg, S. et al. The fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature 389, 994–999. https://doi.org/10.1038/40194 (1997).

    Google Scholar 

  32. Butcher, R. A. et al. Biosynthesis of the caenorhabditis elegans Dauer pheromone. Proc. Natl. Acad. Sci. U S A. 106, 1875–1879. https://doi.org/10.1073/pnas.0810338106 (2009).

    Google Scholar 

  33. Kawano, T. et al. Lifespan extending activity of substances secreted by the nematode Caenorhabditis elegans that include the dauer-inducing pheromone. Biosci. Biotechnol. Biochem. 69, 2479–2481. https://doi.org/10.1271/bbb.69.2479.2005 (2005).

    Google Scholar 

  34. Beets, I. et al. System-wide mapping of peptide-GPCR interactions in C. elegans. Cell. Rep. 42, 113058. https://doi.org/10.1016/j.celrep.2023.113058 (2023).

    Google Scholar 

  35. Hilbert, Z. A. & Kim, D. H. PDF-1 neuropeptide signaling regulates sexually dimorphic gene expression in shared sensory neurons of C. elegans. eLife 7, e36547. https://doi.org/10.7554/eLife.36547 (2018).

  36. Rossi, L. et al. The neuropeptide FLP-11 induces and self-inhibits sleep through the receptor DMSR-1 in Caenorhabiditis elegans. Curr. Biol. 35, 2183–2194. https://doi.org/10.1016/j.cub.2025.03.039 (2025).

    Google Scholar 

  37. Tan, C. M. J. et al. The role of neuropeptide Y in cardiovascular health and disease. Front. Physiol. 9, 1281. https://doi.org/10.3389/fphys.2018.01281 (2018).

    Google Scholar 

  38. Brenner, S. The genetics of Caenorhabditis elegans. Genetics 77, 71–94. https://doi.org/10.1093/genetics/77.1.71 (1974).

    Google Scholar 

  39. Zhang, M. G. & Sternberg, P. W. Both entry to and exit from diapause arrest in Caenorhabditis elegans are regulated by a steroid hormone pathway. Development 149, dev200173. https://doi.org/10.1242/dev.200173 (2022).

    Google Scholar 

  40. Mariol, M. C., Walter, L., Bellemin, S. & Gieseler, K. A rapid protocol for integrating extrachromosomal arrays with high transmission rate into the C. elegans genome. J. Vis. Exp. 82, e50773. https://doi.org/10.3791/50773 (2013).

    Google Scholar 

  41. Shiraishi, A. et al. Repertoires of G protein-coupled receptors for Ciona-specific neuropeptides. Proc. Natl. Acad. Sci. U S A. 116, 7847–7856. https://doi.org/10.1073/pnas.1816640116 (2019).

    Google Scholar 

  42. Li, C. & Kim, K. Family of FLP peptides in caenorhabditis elegans and related nematodes. Front. Endocrinol. 5, 150. 0.3389/fendo.2014.00150 (2014).

    Google Scholar 

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