Regulation of insulin-producing cells in the adult Drosophila brain via the tachykinin peptide receptor DTKR

Journal of Experimental Biology

Volumn 214, Issue 24, 2011, Pages 4201-4208

  Birse, Ryan T ^a   Söderberg, Jeannette A E ^a   Luo, Jiangnan ^a   Winther, Åsa M E ^a,b   Nässel, Dick R ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Drosophila insulin like peptides; G protein coupled receptor; Insulin signaling; Tachykinin receptor; Tachykinin related peptide

Indexed keywords

DILP5 PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; ILP2 PROTEIN, DROSOPHILA; ILP3 PROTEIN, DROSOPHILA; INSULIN; INSULIN DERIVATIVE; NEUROTRANSMITTER RECEPTOR; SIGNAL PEPTIDE; TACHYKININ; TAKR99D PROTEIN, DROSOPHILA;

ANIMAL; ARTICLE; BRAIN; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; MALE; METABOLISM; PANCREAS ISLET BETA CELL; SIGNAL TRANSDUCTION;

ANIMALS; BRAIN; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION; INSULIN; INSULIN-SECRETING CELLS; INSULINS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; RECEPTORS, NEUROTRANSMITTER; SIGNAL TRANSDUCTION; TACHYKININS; TRANSCRIPTION, GENETIC;

EID: 83155172619     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.062091     Document Type: Article

References (64)

1. Adeghate, E., Ponery, A. S., Pallot, D. J. and Singh, J. (2001). Distribution of vasoactive intestinal polypeptide, neuropeptide-Y and substance P and their effects on insulin secretion from the in vitro pancreas of normal and diabetic rats. Peptides 22, 99-107. (Pubitemid 32146688)
2. Baker, K. D. and Thummel, C. S. (2007). Diabetic larvae and obese flies-emerging studies of metabolism in Drosophila. Cell Metab. 6, 257-266. (Pubitemid 47450188)
3. Bauer, J. H., Chang, C., Morris, S. N., Hozier, S., Andersen, S., Waitzman, J. S. and Helfand, S. L. (2007). Expression of dominant-negative Dmp53 in the adult fly brain inhibits insulin signaling. Proc. Natl. Acad. Sci. USA 104, 13355-13360. (Pubitemid 47293949)
4. Birse, R. T., Johnson, E. C., Taghert, P. H. and Nässel, D. R. (2006). Widely distributed Drosophila G-protein-coupled receptor (CG7887) is activated by endogenous tachykinin-related peptides. J. Neurobiol. 66, 33-46. (Pubitemid 41829026)
5. Birse, R. T., Choi, J., Reardon, K., Rodriguez, J., Graham, S., Diop, S., Ocorr, K., Bodmer, R. and Oldham, S. (2010). High-fat-diet-induced obesity and heart dysfunction are regulated by the TOR pathway in Drosophila. Cell Metab. 12, 533-544.
6. Brogiolo, W., Stocker, H., Ikeya, T., Rintelen, F., Fernandez, R. and Hafen, E. (2001). An evolutionarily conserved function of the Drosophila insulin receptor and insulin-like peptides in growth control. Curr. Biol. 11, 213-221. (Pubitemid 32185323)
7. Broughton, S. J., Piper, M. D., Ikeya, T., Bass, T. M., Jacobson, J., Driege, Y., Martinez, P., Hafen, E., Withers, D. J., Leevers, S. J. et al. (2005). Longer lifespan, altered metabolism, and stress resistance in Drosophila from ablation of cells making insulin-like ligands. Proc. Natl. Acad. Sci. USA 102, 3105-3110. (Pubitemid 40299923)
8. Broughton, S., Alic, N., Slack, C., Bass, T., Ikeya, T., Vinti, G., Tommasi, A. M., Driege, Y., Hafen, E. and Partridge, L. (2008). Reduction of DILP2 in Drosophila triages a metabolic phenotype from lifespan revealing redundancy and compensation among DILPs. PLoS ONE 3, e3721.
9. Broughton, S. J., Slack, C., Alic, N., Metaxakis, A., Bass, T. M., Driege, Y. and Partridge, L. (2010). DILP-producing median neurosecretory cells in the Drosophila brain mediate the response of lifespan to nutrition. Aging Cell 9, 336-346.
10. Buch, S., Melcher, C., Bauer, M., Katzenberger, J. and Pankratz, M. J. (2008). Opposing effects of dietary protein and sugar regulate a transcriptional target of Drosophila insulin-like peptide signaling. Cell Metab. 7, 321-332. (Pubitemid 351455218)
11. Cao, C. and Brown, M. R. (2001). Localization of an insulin-like peptide in brains of two flies. Cell Tissue Res. 304, 317-321. (Pubitemid 32448997)
12. Clancy, D. J., Gems, D., Harshman, L. G., Oldham, S., Stocker, H., Hafen, E., Leevers, S. J. and Partridge, L. (2001). Extension of life-span by loss of CHICO, a Drosophila insulin receptor substrate protein. Science 292, 104-106. (Pubitemid 32289136)
13. Cognigni, P., Bailey, A. P. and Miguel-Aliaga, I. (2011). Enteric neurons and systemic signals couple nutritional and reproductive status with intestinal homeostasis. Cell Metab. 13, 92-104.
14. Corl, A. B., Rodan, A. R. and Heberlein, U. (2005). Insulin signaling in the nervous system regulates ethanol intoxication in Drosophila melanogaster. Nat. Neurosci. 8, 18-19. (Pubitemid 41236724)
15. Crocker, A., Shahidullah, M., Levitan, I. B. and Sehgal, A. (2010). Identification of a neural circuit that underlies the effects of octopamine on sleep:wake behavior. Neuron 65, 670-681.
16. Enell, L. E., Kapan, N., Söderberg, J. A., Kahsai, L. and Nässel, D. R. (2010). Insulin signaling, lifespan and stress resistance are modulated by metabotropic GABA receptors on insulin producing cells in the brain of Drosophila. PLoS ONE 5, e15780.
17. Gäde, G., Hoffmann, K. H. and Spring, J. H. (1997). Hormonal regulation in insects: facts, gaps, and future directions. Physiol. Rev. 77, 963-1032. (Pubitemid 27459578)
18. Garofalo, R. S. (2002). Genetic analysis of insulin signaling in Drosophila. Trends Endocrinol. Metab. 13, 156-162. (Pubitemid 36733989)
19. Geminard, C., Rulifson, E. J. and Leopold, P. (2009). Remote control of insulin secretion by fat cells in Drosophila. Cell Metab. 10, 199-207.
20. Géminard, G., Arquier, N., Layalle, S., Bourouis, M., Slaidina, M., Delanoue, R., Bjordal, M., Ohanna, M., Ma, M., Colombani, J. et al. (2006). Control of metabolism and growth through insulin-like peptides in Drosophila. Diabetes 55, S5-S8. (Pubitemid 44927026)
21. Giannakou, M. E. and Partridge, L. (2007). Role of insulin-like signalling in Drosophila lifespan. Trends Biochem. Sci. 32, 180-188. (Pubitemid 46603282)
22. Goberdhan, D. C. and Wilson, C. (2003). The functions of insulin signaling: size isn'teverything, even in Drosophila. Differentiation 71, 375-397. (Pubitemid 37249224)
23. Grönke, S., Muller, G., Hirsch, J., Fellert, S., Andreou, A., Haase, T., Jäckle, H. and Kuhnlein, R. P. (2007). Dual lipolytic control of body fat storage and mobilization in Drosophila. PLoS Biol. 5, e137.
24. Grönke, S., Clarke, D. F., Broughton, S., Andrews, T. D. and Partridge, L. (2010). Molecular evolution and functional characterization of Drosophila insulin-like peptides. PLoS Genet. 6, e1000857.
25. Hwangbo, D. S., Gershman, B., Tu, M. P., Palmer, M. and Tatar, M. (2004). Drosophila dFOXO controls lifespan and regulates insulin signalling in brain and fat body. Nature 429, 562-566. (Pubitemid 38737660)
26. Ignell, R., Root, C. M., Birse, R. T., Wang, J. W., Nässel, D. R. and Winther, A. M. (2009). Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila. Proc. Natl. Acad. Sci. USA 106, 13070-13075.
27. Ikeya, T., Galic, M., Belawat, P., Nairz, K. and Hafen, E. (2002). Nutrient-dependent expression of insulin-like peptides from neuroendocrine cells in the CNS contributes to growth regulation in Drosophila. Curr. Biol. 12, 1293-1300. (Pubitemid 34869879)
28. Isabel, G., Martin, J. R., Chidami, S., Veenstra, J. A. and Rosay, P. (2005). AKHproducing neuroendocrine cell ablation decreases trehalose and induces behavioral changes in Drosophila. Am J. Physiol. Regul. Integr. Comp. Physiol. 288, R531-R538. (Pubitemid 40129621)
29. Kahsai, L., Martin, J. R. and Winther, A. M. (2010). Neuropeptides in the Drosophila central complex in modulation of locomotor behavior. J. Exp. Biol. 213, 2256-2265.
30. Kaplan, D. D., Zimmermann, G., Suyama, K., Meyer, T. and Scott, M. P. (2008). A nucleostemin family GTPase, NS3, acts in serotonergic neurons to regulate insulin signaling and control body size. Genes Dev. 22, 1877-1893. (Pubitemid 352008637)
31. Kim, S. K. and Rulifson, E. J. (2004). Conserved mechanisms of glucose sensingand regulation by Drosophila corpora cardiaca cells. Nature 431, 316-320. (Pubitemid 39265667)
32. Kreneisz, O., Chen, X., Fridell, Y. W. and Mulkey, D. K. (2010). Glucose increases activity and Ca2+ in insulin-producing cells of adult Drosophila. Neuroreport 21, 1116-1120.
33. Lee, G. and Park, J. H. (2004). Hemolymph sugar homeostasis and starvationinduced hyperactivity affected by genetic manipulations of the adipokinetic hormoneencoding gene in Drosophila melanogaster. Genetics 167, 311-323. (Pubitemid 38736390)
34. Lee, K. S., You, K. H., Choo, J. K., Han, Y. M. and Yu, K. (2004). Drosophila short neuropeptide F regulates food intake and body size. J. Biol. Chem. 279, 50781-50789. (Pubitemid 40017816)
35. Lee, K. S., Kwon, O. Y., Lee, J. H., Kwon, K., Min, K. J., Jung, S. A., Kim, A. K., You, K. H., Tatar, M. and Yu, K. (2008). Drosophila short neuropeptide F signaling regulates growth by ERK-mediated insulin signalling. Nat. Cell Biol. 10, 468-475.
36. Li, X. J., Wolfgang, W., Wu, Y. N., North, R. A. and Forte, M. (1991). Cloning, heterologous expression and developmental regulation of a Drosophila receptor for tachykinin-like peptides. EMBO J. 10, 3221-3229. (Pubitemid 21905346)
37. Luo, J., Becnel, J., Nichols, C. D. and Nässel, D. R. (2011). Insulin-producing cells in the brain of adult Drosophila are regulated by the serotonin 5-HT(1A) receptor. Cell. Mol. Life. Sci. doi:10.1007/s00018-011-0789- 0.
38. Mattaliano, M. D., Montana, E. S., Parisky, K. M., Littleton, J. T. and Griffith, L. C. (2007). The Drosophila ARC homolog regulates behavioral responses to starvation. Mol. Cell. Neurosci. 36, 211-221. (Pubitemid 47418613)
39. Maywood, E. S., Chesham, J. E., O'Brien, J. A. and Hastings, M. H. (2011). A diversity of paracrine signals sustains molecular circadian cycling in suprachiasmatic nucleus circuits. Proc. Natl. Acad. Sci. USA 108, 14306-14311.
40. Miguel-Aliaga, I., Thor, S. and Gould, A. P. (2008). Postmitotic specification of Drosophila insulinergic neurons from pioneer neurons. PLoS Biol. 6, e58.
41. Nässel, D. R. (2009). Neuropeptide signaling near and far: how localized and timed is the action of neuropeptides in brain circuits? Invert. Neurosci. 9, 57-75.
42. Nässel, D. R. and Winther, A. M. (2010). Drosophila neuropeptides in regulation of physiology and behavior. Prog. Neurobiol. 92, 42-104.
43. Okamoto, N., Yamanaka, N., Yagi, Y., Nishida, Y., Kataoka, H., O'Connor, M. B. and Mizoguchi, A. (2009). A fat body-derived IGF-like peptide regulates postfeeding growth in Drosophila. Dev. Cell 17, 885-891.
44. Poels, J., Birse, R. T., Nachman, R. J., Fichna, J., Janecka, A., Vanden Broeck, J. and Nässel, D. R. (2009). Characterization and distribution of NKD, a receptor for Drosophila tachykinin-related peptide 6. Peptides 30, 545-556.
45. Root, C. M., Ko, K. I., Jafari, A. and Wang, J. W. (2011). Presynaptic facilitation by neuropeptide signaling mediates odor-driven food search. Cell 145, 133-144.
46. Rulifson, E. J., Kim, S. K. and Nusse, R. (2002). Ablation of insulin-producing neurons in flies: growth and diabetic phenotypes. Science 296, 1118-1120. (Pubitemid 34517128)
47. Schmidt, P. T., Tornoe, K., Poulsen, S. S., Rasmussen, T. N. and Holst, J. J. (2000). Tachykinins in the porcine pancreas: potent exocrine and endocrine effects via NK-1 receptors. Pancreas 20, 241-247. (Pubitemid 30171776)
48. Service, F. J., O'Brien, P. C. and Rizza, R. A. (1987). Measurements of glucose control. Diabetes Care 10, 225-237. (Pubitemid 17065817)
49. Siviter, R. J., Coast, G. M., Winther, A. M., Nachman, R. J., Taylor, C. A., Shirras, A. D., Coates, D., Isaac, R. E. and Nässel, D. R. (2000). Expression and functional characterization of a Drosophila neuropeptide precursor with homology to mammalian preprotachykinin A. J. Biol. Chem. 275, 23273-23280. (Pubitemid 30646227)
50. Slaidina, M., Delanoue, R., Grönke, S., Partridge, L. and Leopold, P. (2009). A Drosophila insulin-like peptide promotes growth during nonfeeding states. Dev. Cell 17, 874-884.
51. Söderberg, J. A., Birse, R. T. and Nässel, D. R. (2011). Insulin production and signaling in renal tubules of Drosophila is under control of tachykinin-related peptide and regulates stress resistance. PLoS ONE 6, e19866.
52. Taguchi, A. and White, M. F. (2008). Insulin-like signaling, nutrient homeostasis, and life span. Annu. Rev. Physiol. 70, 191-212. (Pubitemid 351738177)
53. Tatar, M., Kopelman, A., Epstein, D., Tu, M. P., Yin, C. M. and Garofalo, R. S. (2001). A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science 292, 107-110. (Pubitemid 32289137)
54. Tatar, M., Bartke, A. and Antebi, A. (2003). The endocrine regulation of aging by insulin-like signals. Science 299, 1346-1351. (Pubitemid 36254639)
55. Van der Horst, D. J., Van Marrewijk, W. J. and Diederen, J. H. (2001). Adipokinetic hormones of insect: release, signal transduction, and responses. Int. Rev. Cytol. 211, 179-240. (Pubitemid 32937614)
56. Wang, M. C., Bohmann, D. and Jasper, H. (2005). JNK extends life span and limits growth by antagonizing cellular and organism-wide responses to insulin signaling. Cell 121, 115-125.
57. Winther, A. M. and Nässel, D. R. (2001). Intestinal peptides as circulating hormones:release of tachykinin-related peptide from the locust and cockroach midgut. J. Exp. Biol. 204, 1269-1280. (Pubitemid 34861095)
58. Winther, A. M., Siviter, R. J., Isaac, R. E., Predel, R. and Nässel, D. R. (2003). Neuronal expression of tachykinin-related peptides and gene transcript during postembryonic development of Drosophila. J. Comp. Neurol. 464, 180-196. (Pubitemid 36980608)
59. Winther, A. M., Acebes, A. and Ferrus, A. (2006). Tachykinin-related peptides modulate odor perception and locomotor activity in Drosophila. Mol. Cell. Neurosci. 31, 399-406. (Pubitemid 43361925)
60. Wu, Q., Zhang, Y., Xu, J. and Shen, P. (2005). Regulation of hunger-driven behaviors by neural ribosomal S6 kinase in Drosophila. Proc. Natl. Acad. Sci. USA 102, 13289-13294. (Pubitemid 41325016)
61. Yang, C. H., Belawat, P., Hafen, E., Jan, L. Y. and Jan, Y. N. (2008). Drosophila egg-laying site selection as a system to study simple decision-making processes. Science 319, 1679-1683. (Pubitemid 351432508)
62. Yew, J. Y., Wang, Y., Barteneva, N., Dikler, S., Kutz-Naber, K. K., Li, L. and Kravitz, E. A. (2009). Analysis of neuropeptide expression and localization in adult Drosophila melanogaster central nervous system by affinity cell-capture mass spectrometry. J. Proteome Res. 8, 1271-1284.
63. Zhang, H., Liu, J., Li, C. R., Momen, B., Kohanski, R. A. and Pick, L. (2009). Deletion of Drosophila insulin-like peptides causes growth defects and metabolic abnormalities. Proc. Natl. Acad. Sci. USA 106, 19617-19622.
64. Zupanc, G. K. (1996). Peptidergic transmission: from morphological correlates to functional implications. Micron 27, 35-91. (Pubitemid 27099094)