Neuronal Control of Metabolism through Nutrient-Dependent Modulation of Tracheal Branching

During adaptive angiogenesis, a key process in the etiology and treatment of cancer and obesity, the vasculature changes to meet the metabolic needs of its target tissues. Although the cues governing vascular remodeling are not fully understood, target-derived signals are generally believed to under...

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Published in:Cell 2014-01, Vol.156 (1-2), p.69-83
Main Authors: Linneweber, Gerit A., Jacobson, Jake, Busch, Karl Emanuel, Hudry, Bruno, Christov, Christo P., Dormann, Dirk, Yuan, Michaela, Otani, Tomoki, Knust, Elisabeth, de Bono, Mario, Miguel-Aliaga, Irene
Format: Article
Language:English
Subjects:
Animals
Calcium - metabolism
Digestive System - blood supply
Drosophila
Drosophila melanogaster - physiology
Humans
Models, Animal
Neovascularization, Pathologic
Neovascularization, Physiologic
Neurons - metabolism
Neuropeptides - metabolism
Oxygen - metabolism
Signal Transduction
Vasoactive Intestinal Peptide - metabolism
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Summary:During adaptive angiogenesis, a key process in the etiology and treatment of cancer and obesity, the vasculature changes to meet the metabolic needs of its target tissues. Although the cues governing vascular remodeling are not fully understood, target-derived signals are generally believed to underlie this process. Here, we identify an alternative mechanism by characterizing the previously unrecognized nutrient-dependent plasticity of the Drosophila tracheal system: a network of oxygen-delivering tubules developmentally akin to mammalian blood vessels. We find that this plasticity, particularly prominent in the intestine, drives—rather than responds to—metabolic change. Mechanistically, it is regulated by distinct populations of nutrient- and oxygen-responsive neurons that, through delivery of both local and systemic insulin- and VIP-like neuropeptides, sculpt the growth of specific tracheal subsets. Thus, we describe a novel mechanism by which nutritional cues modulate neuronal activity to give rise to organ-specific, long-lasting changes in vascular architecture. [Display omitted] •The Drosophila tracheal system exhibits nutrient-dependent plasticity•Tracheal plasticity is organ specific and metabolically significant•Nutrient- and hypoxia-responsive neurons drive adaptive tracheation•Distinct insulin-like and Pdf neuropeptides control organ-specific tracheal branching Previously unrecognized nutrient-dependent plasticity of the Drosophila tracheal system drives metabolic change and is regulated by distinct populations of nutrient- and oxygen-responsive neurons.
ISSN:0092-8674
1097-4172
DOI:10.1016/j.cell.2013.12.008