Abstract
The ability to maintain metabolic homeostasis is a key capability critical for the survival and well-being of animals living in constantly changing environments. Metabolic homeostasis depends on neuromodulators, such as biogenic amines, neuropeptides, and hormones, to signal changes in animals’ internal metabolic status and to orchestrate their behaviors accordingly. An important example is the regulation of feeding behavior by conserved molecular and cellular mechanisms across the animal kingdom. Its relatively simple brain coupled with well-characterized genetics and behavioral paradigms makes the fruit fly Drosophila melanogaster an excellent model for investigating the neuromodulatory regulation of feeding behavior. In this review we discuss the neuromodulators and neural circuits that integrate the internal physiological status with external sensory cues and modulate feeding behavior in adult fruit flies. Studies show that various specific aspects of feeding behavior are subjected to unique neuromodulatory regulation, which permits fruit flies to maintain metabolic homeostasis effectively.
概要
现代社会很多人受到肥胖、代谢紊乱和饮食不调的困扰,我们迫切地需要解决这些严重影响人类生活的问题,但直接在人类中开展研究的方式进展比较缓慢。幸运的是人类的进食和代谢过程与其它高等动物甚至昆虫相似,都具有极高的保守性。因此,我们可以利用相对容易操作的低等生物作为研究对象,加快解决问题的进程。果蝇便是一种非常好的实验对象,它是一种神经系统比较简单的模式生物。本文对果蝇成虫的进食行为进行了详细阐述,强调了果蝇的神经系统能实时监控机体的代谢状态,并能将其与外界环境的食物信号精准整合,从而调节它们进食的每个步骤。通过对果蝇进食和代谢相关的神经调节的研究能拓宽我们对人类相应疾病研究的视野。
Similar content being viewed by others
References
Ahn JE, Chen Y, Amrein H, 2017. Molecular basis of fatty acid taste in Drosophila. eLife, 6:e30115. https://doi.org/10.7554/eLife.30115
Al-Anzi B, Armand E, Nagamei P, et al., 2010. The leucokinin pathway and its neurons regulate meal size in Drosophila. Curr Biol, 20(11):969–978. https://doi.org/10.1016/j.cub.2010.04.039
Bharucha KN, Tarr P, Zipursky SL, 2008. A glucagon-like endocrine pathway in Drosophila modulates both lipid and carbohydrate homeostasis. J Exp Biol, 211:3103–3110. https://doi.org/10.1242/jeb.016451
Bjordal M, Arquier N, Kniazeff J, et al., 2014. Sensing of amino acids in a dopaminergic circuitry promotes rejection of an incomplete diet in Drosophila. Cell, 156(3): 510–521. https://doi.org/10.1016/j.cell.2013.12.024
Carvalho GB, Kapahi P, Anderson DJ, et al., 2006. Allocrine modulation of feeding behavior by the sex peptide of Drosophila. Curr Biol, 16(7):692–696. https://doi.org/10.1016/j.cub.2006.02.064
Chen YCD, Dahanukar A, 2017. Molecular and cellular organization of taste neurons in adult Drosophila pharynx. Cell Rep, 21(10):2978–2991. https://doi.org/10.1016/j.celrep.2017.11.041
Dahanukar A, Foster K, van der Goes van Naters WM, et al., 2001. A Gr receptor is required for response to the sugar trehalose in taste neurons of Drosophila. Nat Neurosci, 4(12):1182–1186. https://doi.org/10.1038/nn765
Dahanukar A, Lei YT, Kwon JY, et al., 2007. Two Gr genes underlie sugar reception in Drosophila. Neuron, 56(3): 503–516. https://doi.org/10.1016/j.neuron.2007.10.024
Dethier VG, 1976. The Hungry Fly. Harvard University Press, Cambridge, p.4–118.
Dus M, Min S, Keene AC, et al., 2011. Taste-independent detection of the caloric content of sugar in Drosophila. Proc Natl Acad Sci USA, 108(28):11644–11649.https://doi.org/10.1073/pnas.1017096108
Dus M, Ai MR, Suh GSB, 2013. Taste-independent nutrient selection is mediated by a brain-specific Na+/solute cotransporter in Drosophila. Nat Neurosci, 16(5):526–528. https://doi.org/10.1038/Nn.3372
Dus M, Lai JSY, Gunapala KM, et al., 2015. Nutrient sensor in the brain directs the action of the brain-gut axis in Drosophila. Neuron, 87(1):139–151. https://doi.org/10.1016/j.neuron.2015.05.032
Edgecomb RS, Harth CE, Schneiderman AM, 1994. Regulation of feeding behavior in adult Drosophila melanogaster varies with feeding regime and nutritional state. J Exp Biol, 197:215–235.
Freeman EG, Dahanukar A, 2015. Molecular neurobiology of Drosophila taste. Curr Opin Neurobiol, 34:140–148. https://doi.org/10.1016/j.conb.2015.06.001
Fujii S, Yavuz A, Slone J, et al., 2015. Drosophila sugar receptors in sweet taste perception, olfaction, and internal nutrient sensing. Curr Biol, 25(5):621–627. https://doi.org/10.1016/j.cub.2014.12.058
Ganguly A, Pang LS, Duong VK, et al., 2017. A molecular and cellular context-dependent role for Ir76b in detection of amino acid taste. Cell Rep, 18(3):737–750. https://doi.org/10.1016/j.celrep.2016.12.071
Géminard C, Rulifson EJ, Léopold P, 2009. Remote control of insulin secretion by fat cells in Drosophila. Cell Metab, 10(3):199–207. https://doi.org/10.1016/j.cmet.2009.08.002
Grönke S, Müller G, Hirsch J, et al., 2007. Dual lipolytic control of body fat storage and mobilization in Drosophila. PLoS Biol, 5(6):e137. https://doi.org/10.1371/journal.pbio.0050137
Hergarden AC, Tayler TD, Anderson DJ, 2012. Allatostatin-A neurons inhibit feeding behavior in adult Drosophila. Proc Natl Acad Sci USA, 109(10):3967–3972. https://doi.org/10.1073/pnas.1200778109
Inagaki HK, De-Leon SBT, Wong AM, et al., 2012. Visualizing neuromodulation in vivo: TANGO-mapping of dopamine signaling reveals appetite control of sugar sensing. Cell, 148(3):583–595. https://doi.org/10.1016/j.cell.2011.12.022
Inagaki HK, Panse KM, Anderson DJ, 2014. Independent, reciprocal neuromodulatory control of sweet and bitter taste sensitivity during starvation in Drosophila. Neuron, 84(4):806–820. https://doi.org/10.1016/j.neuron.2014.09.032
Isabel G, Martin JR, Chidami S, et al., 2005. AKH-producing neuroendocrine cell ablation decreases trehalose and induces behavioral changes in Drosophila. Am J Physiol Regul Integr Comp Physiol, 288(2):R531–R538. https://doi.org/10.1152/ajpregu.00158.2004
Jiao YC, Moon SJ, Montell C, 2007. A Drosophila gustatory receptor required for the responses to sucrose, glucose, and maltose identified by mRNA tagging. Proc Natl Acad Sci USA, 104(35):14110–14115. https://doi.org/10.1073/pnas.0702421104
Jiao YC, Moon SJ, Wang XY, et al., 2008. Gr64f is required in combination with other gustatory receptors for sugar detection in Drosophila. Curr Biol, 18(22):1797–1801. https://doi.org/10.1016/j.cub.2008.10.009
Joseph RM, Carlson JR, 2015. Drosophila chemoreceptors: a molecular interface between the chemical world and the brain. Trends Genet, 31(12):683–695. https://doi.org/10.1016/j.tig.2015.09.005
Joseph RM, Sun JS, Tam E, et al., 2017. A receptor and neuron that activate a circuit limiting sucrose consumption. eLife, 6:e24992. https://doi.org/10.7554/eLife.24992
Kim SK, Rulifson EJ, 2004. Conserved mechanisms of glucose sensing and regulation by Drosophila corpora cardiaca cells. Nature, 431(7006):316–320. https://doi.org/10.1038/nature02897
Kim SM, Su CY, Wang JW, 2017. Neuromodulation of innate behaviors in Drosophila. Annu Rev Neurosci, 40:327–348. https://doi.org/10.1146/annurev-neuro-072116-031558
Ko KI, Root CM, Lindsay SA, et al., 2015. Starvation promotes concerted modulation of appetitive olfactory behavior via parallel neuromodulatory circuits. eLife, 4:e08298. https://doi.org/10.7554/eLife.08298
Koç H, Vinyard CJ, Essick GK, et al., 2013. Food oral processing: conversion of food structure to textural perception. Annu Rev Food Sci Technol, 4:237–266. https://doi.org/10.1146/annurev-food-030212-182637
LeDue EE, Chen YC, Jung AY, et al., 2015. Pharyngeal sense organs drive robust sugar consumption in Drosophila. Nat Commun, 6:6667. https://doi.org/10.1038/ncomms7667
LeDue EE, Mann K, Koch E, et al., 2016. Starvation-induced depotentiation of bitter taste in Drosophila. Curr Biol, 26(21):2854–2861. https://doi.org/10.1016/j.cub.2016.08.028
Lee G, Park JH, 2004. Hemolymph sugar homeostasis and starvation-induced hyperactivity affected by genetic manipulations of the adipokinetic hormone-encoding gene in Drosophila melanogaster. Genetics, 167(1):311–323. https://doi.org/10.1534/genetics.167.1.311
Lee Y, Moon SJ, Montell C, 2009. Multiple gustatory receptors required for the caffeine response in Drosophila. Proc Natl Acad Sci USA, 106(11):4495–4500. https://doi.org/10.1073/pnas.0811744106
Lee Y, Kim SH, Montell C, 2010. Avoiding DEET through insect gustatory receptors. Neuron, 67(4):555–561. https://doi.org/10.1016/j.neuron.2010.07.006
Lee Y, Kang MJ, Shim J, et al., 2012. Gustatory receptors required for avoiding the insecticide L-canavanine. J Neurosci, 32(4):1429–1435.https://doi.org/10.1523/JNEUROSCI.4630-11.2012
Liu QL, Tabuchi M, Liu S, et al., 2017. Branch-specific plasticity of a bifunctional dopamine circuit encodes protein hunger. Science, 356(6337):534–539. https://doi.org/10.1126/science.aal3245
Marella S, Mann K, Scott K, 2012. Dopaminergic modulation of sucrose acceptance behavior in Drosophila. Neuron, 73(5):941–950. https://doi.org/10.1016/j.neuron.2011.12.032
Miyamoto T, Slone J, Song XY, et al., 2012. A fructose receptor functions as a nutrient sensor in the Drosophila brain. Cell, 151(5):1113–1125. https://doi.org/10.1016/j.cell.2012.10.024
Moon SJ, Lee Y, Jiao YC, et al., 2009. A Drosophila gustatory receptor essential for aversive taste and inhibiting male-to-male courtship. Curr Biol, 19(19):1623–1627. https://doi.org/10.1016/j.cub.2009.07.061
Murata S, Brockmann A, Tanimura T, 2017. Pharyngeal stimulation with sugar triggers local searching behavior in Drosophila. J Exp Biol, 220:3231–3237. https://doi.org/10.1242/jeb.161646
Olds WH, Xu T, 2014. Regulation of food intake by mechanosensory ion channels in enteric neurons. eLife, 3:e04402. https://doi.org/10.7554/Elife.04402
Park JY, Dus M, Kim S, et al., 2016. Drosophila SLC5A11 mediates hunger by regulating K+ channel activity. Curr Biol, 26(15):1965–1974. https://doi.org/10.1016/j.cub.2016.05.076
Piper MDW, Blanc E, Leitão-Goncalves R, et al., 2014. A holidic medium for Drosophila melanogaster. Nat Methods, 11(1):100–105. https://doi.org/10.1038/nmeth.2731
Pool AH, Scott K, 2014. Feeding regulation in Drosophila. Curr Opin Neurobiol, 29:57–63. https://doi.org/10.1016/j.conb.2014.05.008
Pool AH, Kvello P, Mann K, et al., 2014. Four gabaergic interneurons impose feeding restraint in Drosophila. Neuron, 83(1):164–177. https://doi.org/10.1016/j.neuron.2014.05.006
Rajan A, Perrimon N, 2012. Drosophila cytokine Unpaired 2 regulates physiological homeostasis by remotely controlling insulin secretion. Cell, 151(1):123–137. https://doi.org/10.1016/j.cell.2012.08.019
Ribeiro C, Dickson BJ, 2010. Sex peptide receptor and neuronal TOR/S6K signaling modulate nutrient balancing in Drosophila. Curr Biol, 20(11):1000–1005. https://doi.org/10.1016/j.cub.2010.03.061
Root CM, Ko KI, Jafari A, et al., 2011. Presynaptic facilitation by neuropeptide signaling mediates odor-driven food search. Cell, 145(1):133–144. https://doi.org/10.1016/j.cell.2011.02.008
Sánchez-Alcañiz JA, Zappia G, Marion-Poll F, et al., 2017. A mechanosensory receptor required for food texture detection in Drosophila. Nat Commun, 8:14192. https://doi.org/10.1038/ncomms14192
Scott K, 2018. Gustatory processing in Drosophila melanogaster. Annu Rev Entomol, 63:15–30. https://doi.org/10.1146/annurev-ento-020117-043331
Slone J, Daniels J, Amrein H, 2007. Sugar receptors in Drosophila. Curr Biol, 17(20):1809–1816. https://doi.org/10.1016/j.cub.2007.09.027
Steck K, Walker SJ, Itskov PM, et al., 2018. Internal amino acid state modulates yeast taste neurons to support protein homeostasis in Drosophila. eLife, 7:e31625. https://doi.org/10.7554/eLife.31625
Stocker RF, 1994. The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res, 275(1):3–26. https://doi.org/10.1007/BF00305372.
Sun JH, Liu C, Bai XB, et al., 2017. Drosophila FIT is a protein-specific satiety hormone essential for feeding control. Nat Commun, 8:14161. https://doi.org/10.1038/ncomms14161
Thorne N, Chromey C, Bray S, et al., 2004. Taste perception and coding in Drosophila. Curr Biol, 14(12):1065–1079. https://doi.org/10.1016/j.cub.2004.05.019
Tian YJ, Wang LM, 2018. Octopamine mediates proteinseeking behavior in mated female Drosophila. Cell Discov, 4:66. https://doi.org/10.1038/s41421-018-0063-9
Ueno K, Ohta M, Morita H, et al., 2001. Trehalose sensitivity in Drosophila correlates with mutations in and expression of the gustatory receptor gene Gr5a. Curr Biol, 11(18): 1451–1455. https://doi.org/10.1016/S0960-9822(01)00450-X
Vargas MA, Luo NG, Yamaguchi A, et al., 2010. A role for S6 kinase and serotonin in postmating dietary switch and balance of nutrients in D. melanogaster. Curr Biol, 20(11):1006–1011. https://doi.org/10.1016/j.cub.2010.04.009
Walker SJ, Corrales-Carvajal VM, Ribeiro C, 2015. Postmating circuitry modulates salt taste processing to increase reproductive output in Drosophila. Curr Biol, 25(20): 2621–2630. https://doi.org/10.1016/j.cub.2015.08.043
Weiss LA, Dahanukar A, Kwon JY, et al., 2011. The molecular and cellular basis of bitter taste in Drosophila. Neuron, 69(2):258–272. https://doi.org/10.1016/j.neuron.2011.01.001
Yang Z, Yu Y, Zhang V, et al., 2015. Octopamine mediates starvation-induced hyperactivity in adult Drosophila. Proc Natl Acad Sci USA, 112(16):5219–5224. https://doi.org/10.1073/pnas.1417838112
Yang Z, Huang R, Fu X, et al., 2018. A post-ingestive amino acid sensor promotes food consumption in Drosophila. Cell Res, 28(10):1013–1025. https://doi.org/10.1038/s41422-018-0084-9
Yapici N, Cohn R, Schusterreiter C, et al., 2016. A taste circuit that regulates ingestion by integrating food and hunger signals. Cell, 165(3):715–729. https://doi.org/10.1016/j.cell.2016.02.061
Yu Y, Huang R, Ye J, et al., 2016. Regulation of starvation-induced hyperactivity by insulin and glucagon signaling in adult Drosophila. eLife, 5:e15693. https://doi.org/10.7554/eLife.15693
Zhan YP, Liu L, Zhu Y, 2016. Taotie neurons regulate appetite in Drosophila. Nat Commun, 7:13633. https://doi.org/10.1038/ncomms13633
Zhang YV, Aikin TJ, Li ZZ, et al., 2016. The basis of food texture sensation in Drosophila. Neuron, 91(4):863–877. https://doi.org/10.1016/j.neuron.2016.07.013
Author information
Authors and Affiliations
Corresponding author
Additional information
Project supported by the National Natural Science Foundation of China (No. 31522026) and the Fundamental Research Funds for the Zhejiang Provincial Universities (No. 2019XZZX003-12), China
Rights and permissions
About this article
Cite this article
Wang, Gh., Wang, Lm. Recent advances in the neural regulation of feeding behavior in adult Drosophila. J. Zhejiang Univ. Sci. B 20, 541–549 (2019). https://doi.org/10.1631/jzus.B1900080
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1631/jzus.B1900080