The thirsty fly: Ion transport peptide (ITP) is a novel endocrine regulator of water homeostasis in Drosophila
Animals need to continuously adjust their water metabolism to the internal and external conditions. Homeostasis of body fluids thus requires tight regulation of water intake and excretion, and a balance between ingestion of water and solid food. Here, we investigated how these processes are coordina...
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Published in | PLoS genetics Vol. 14; no. 8; p. e1007618 |
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Main Authors | , , |
Format | Journal Article |
Language | English |
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01.08.2018
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Abstract | Animals need to continuously adjust their water metabolism to the internal and external conditions. Homeostasis of body fluids thus requires tight regulation of water intake and excretion, and a balance between ingestion of water and solid food. Here, we investigated how these processes are coordinated in Drosophila melanogaster. We identified the first thirst-promoting and anti-diuretic hormone of Drosophila, encoded by the gene Ion transport peptide (ITP). This endocrine regulator belongs to the CHH (crustacean hyperglycemic hormone) family of peptide hormones. Using genetic gain- and loss-of-function experiments, we show that ITP signaling acts analogous to the human vasopressin and renin-angiotensin systems; expression of ITP is elevated by dehydration of the fly, and the peptide increases thirst while repressing excretion, promoting thus conservation of water resources. ITP responds to both osmotic and desiccation stress, and dysregulation of ITP signaling compromises the fly's ability to cope with these stressors. In addition to the regulation of thirst and excretion, ITP also suppresses food intake. Altogether, our work identifies ITP as an important endocrine regulator of thirst and excretion, which integrates water homeostasis with feeding of Drosophila. |
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AbstractList | Animals need to continuously adjust their water metabolism to the internal and external conditions. Homeostasis of body fluids thus requires tight regulation of water intake and excretion, and a balance between ingestion of water and solid food. Here, we investigated how these processes are coordinated in Drosophila melanogaster. We identified the first thirst-promoting and anti-diuretic hormone of Drosophila, encoded by the gene Ion transport peptide (ITP). This endocrine regulator belongs to the CHH (crustacean hyperglycemic hormone) family of peptide hormones. Using genetic gain- and loss-of-function experiments, we show that ITP signaling acts analogous to the human vasopressin and renin-angiotensin systems; expression of ITP is elevated by dehydration of the fly, and the peptide increases thirst while repressing excretion, promoting thus conservation of water resources. ITP responds to both osmotic and desiccation stress, and dysregulation of ITP signaling compromises the fly’s ability to cope with these stressors. In addition to the regulation of thirst and excretion, ITP also suppresses food intake. Altogether, our work identifies ITP as an important endocrine regulator of thirst and excretion, which integrates water homeostasis with feeding of Drosophila. Animals need to continuously adjust their water metabolism to the internal and external conditions. Homeostasis of body fluids thus requires tight regulation of water intake and excretion, and a balance between ingestion of water and solid food. Here, we investigated how these processes are coordinated in Drosophila melanogaster . We identified the first thirst-promoting and anti-diuretic hormone of Drosophila , encoded by the gene Ion transport peptide (ITP) . This endocrine regulator belongs to the CHH (crustacean hyperglycemic hormone) family of peptide hormones. Using genetic gain- and loss-of-function experiments, we show that ITP signaling acts analogous to the human vasopressin and renin-angiotensin systems; expression of ITP is elevated by dehydration of the fly, and the peptide increases thirst while repressing excretion, promoting thus conservation of water resources. ITP responds to both osmotic and desiccation stress, and dysregulation of ITP signaling compromises the fly’s ability to cope with these stressors. In addition to the regulation of thirst and excretion, ITP also suppresses food intake. Altogether, our work identifies ITP as an important endocrine regulator of thirst and excretion, which integrates water homeostasis with feeding of Drosophila . Maintenance of energy and water balance is necessary for survival of all organisms. Even a mild dehydration triggers thirst, reduces appetite, and decreases diuresis (water excretion), thereby promoting conservation of water resources and survival under arid conditions. Homeostasis is regulated primarily by endocrine systems that utilize neuropeptides and peptide hormones. Whereas hormonal mechanisms that regulate the water balance in humans are relatively well understood, much less is known about these regulations in the fruit fly Drosophila melanogaster . Here, we describe the first thirst-promoting and anti-diuretic hormone of Drosophila , encoded by the gene Ion transport peptide (ITP) . We show that ITP increases upon dehydration, and protects the animal from loss of body water by promoting thirst and repressing excretion. ITP also suppresses feeding, and can thus be considered as a master regulator integrating water and energy balance. |
Audience | Academic |
Author | Dircksen, Heinrich Gáliková, Martina Nässel, Dick R |
AuthorAffiliation | Department of Zoology, Stockholm University, Stockholm, Sweden Washington University in Saint Louis School of Medicine, UNITED STATES |
AuthorAffiliation_xml | – name: Department of Zoology, Stockholm University, Stockholm, Sweden – name: Washington University in Saint Louis School of Medicine, UNITED STATES |
Author_xml | – sequence: 1 givenname: Martina orcidid: 0000-0001-8934-0236 surname: Gáliková fullname: Gáliková, Martina organization: Department of Zoology, Stockholm University, Stockholm, Sweden – sequence: 2 givenname: Heinrich surname: Dircksen fullname: Dircksen, Heinrich organization: Department of Zoology, Stockholm University, Stockholm, Sweden – sequence: 3 givenname: Dick R orcidid: 0000-0002-1147-7766 surname: Nässel fullname: Nässel, Dick R organization: Department of Zoology, Stockholm University, Stockholm, Sweden |
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SubjectTerms | Angiotensin Animals Antidiuretics Biology and Life Sciences Body fluids Cellular signal transduction Crustaceans Dehydration Desiccation Drosophila Drosophila melanogaster Drosophila melanogaster - genetics Drosophila Proteins - genetics Drosophila Proteins - physiology Excretion Female Food intake Gastrointestinal Tract - physiology Gene Expression Regulation Genetic aspects Homeostasis Hormones Hunger Insects Investigations Ion transport Male Medicine and Health Sciences Neurons Neuropeptides - genetics Neuropeptides - physiology Osmotic shock Peptide hormones Peptides Renin Research and Analysis Methods RNA interference Signal Transduction Stress, Physiological Thirst Thirst - physiology Vasopressin Water Water intake Water resources zoofysiologi Zoological physiology |
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Title | The thirsty fly: Ion transport peptide (ITP) is a novel endocrine regulator of water homeostasis in Drosophila |
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