Insect capa neuropeptides impact desiccation and cold tolerance

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 112; no. 9; pp. 2882 - 2887
• Main Authors: Terhzaz, Selim, Teets, Nicholas M., Cabrero, Pablo, Henderson, Louise, Ritchie, Michael G., Nachman, Ronald J., Dow, Julian A. T., Denlinger, David L., Davies, Shireen-A.
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 03.03.2015; National Acad Sciences
• Subjects: Abiotic stress; Animals; Biological Sciences; Cold Temperature; Cold-Shock Response; Dehydration - genetics; Dehydration - metabolism; Dehydration - pathology; Drosophila melanogaster; Drosophila Proteins - biosynthesis; Drosophila Proteins - genetics; Gene Expression Regulation; Genes; Genotype & phenotype; Homeostasis; Immunohistochemistry; Insects; Malpighian Tubules - metabolism; Malpighian Tubules - pathology; Neurons - metabolism; Neurons - pathology; Neuropeptides - biosynthesis; Neuropeptides - genetics; Peptides; Signal Transduction - genetics; desiccation and cold tolerance; capa; neuropeptides; environmental stress; insects
• DOI: 10.1073/pnas.1501518112
• ISSN: 0027-8424

The success of insects is linked to their impressive tolerance to environmental stress, but little is known about how such responses are mediated by the neuroendocrine system. Here we show that the capability ( capa ) neuropeptide gene is a desiccation- and cold stress-responsive gene in diverse dipteran species. Using targeted in vivo gene silencing, physiological manipulations, stress-tolerance assays, and rationally designed neuropeptide analogs, we demonstrate that the Drosophila melanogaster capa neuropeptide gene and its encoded peptides alter desiccation and cold tolerance. Knockdown of the capa gene increases desiccation tolerance but lengthens chill coma recovery time, and injection of capa peptide analogs can reverse both phenotypes. Immunohistochemical staining suggests that capa accumulates in the capa-expressing Va neurons during desiccation and nonlethal cold stress but is not released until recovery from each stress. Our results also suggest that regulation of cellular ion and water homeostasis mediated by capa peptide signaling in the insect Malpighian (renal) tubules is a key physiological mechanism during recovery from desiccation and cold stress. This work augments our understanding of how stress tolerance is mediated by neuroendocrine signaling and illustrates the use of rationally designed peptide analogs as agents for disrupting protective stress tolerance. Significance Insects are among the most robust organisms on the planet, surviving in virtually all environments and capable of surmounting a range of environmental stresses including desiccation and cold. Although desiccation and cold tolerance share many common traits, potential mechanisms for such linked responses remain unclear. Here we show that an insect neuropeptide gene is associated with tolerance of both desiccation and cold in Drosophila melanogaster , suggesting a novel mechanism in renal tubule epithelia that enhances survival of both desiccation and cold. Also, we can reverse RNAi-induced stress tolerance phenotypes in intact flies using rationally designed peptide mimetic analogs. We thus demonstrate the power of intervention in physiological processes controlled by neuropeptides, with potential for insect pest control.