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A Systematic Analysis of Drosophila Regulatory Peptide Expression in Enteroendocrine Cells
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  • Journal title : Molecules and Cells
  • Volume 39, Issue 4,  2016, pp.358-366
  • Publisher : Korea Society for Molecular and Cellular Biology
  • DOI : 10.14348/molcells.2016.0014
 Title & Authors
A Systematic Analysis of Drosophila Regulatory Peptide Expression in Enteroendocrine Cells
Chen, Ji; Kim, Seol-min; Kwon, Jae Young;
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 Abstract
The digestive system is gaining interest as a major regulator of various functions including immune defense, nutrient accumulation, and regulation of feeding behavior, aside from its conventional function as a digestive organ. The Drosophila midgut epithelium is completely renewed every 1-2 weeks due to differentiation of pluripotent intestinal stem cells in the midgut. Intestinal stem cells constantly divide and differentiate into enterocytes that secrete digestive enzymes and absorb nutrients, or enteroendocrine cells that secrete regulatory peptides. Regulatory peptides have important roles in development and metabolism, but study has mainly focused on expression and functions in the nervous system, and not much is known about the roles in endocrine functions of enteroendocrine cells. We systemically examined the expression of 45 regulatory peptide genes in the Drosophila midgut, and verified that at least 10 genes are expressed in the midgut enteroendocrine cells through RT-PCR, in situ hybridization, antisera, and 25 regulatory peptide-GAL transgenes. The Drosophila midgut is highly compartmentalized, and individual peptides in enteroendocrine cells were observed to express in specific regions of the midgut. We also confirmed that some peptides expressed in the same region of the midgut are expressed in mutually exclusive enteroendocrine cells. These results indicate that the midgut enteroendocrine cells are functionally differentiated into different subgroups. Through this study, we have established a basis to study regulatory peptide functions in enteroendocrine cells as well as the complex organization of enteroendocrine cells in the Drosophila midgut.
 Keywords
Drosophila melanogaster;enteroendocrine cells;regulatory peptides;
 Language
English
 Cited by
1.
Atg16 promotes enteroendocrine cell differentiation via regulation of intestinal Slit/Robo signaling, Development, 2017, 144, 21, 3990  crossref(new windwow)
 References
1.
Beehler-Evans, R., and Micchelli, C.A. (2015). Generation of enteroendocrine cell diversity in midgut stem cell lineages. Development 142, 654-664. crossref(new window)

2.
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. crossref(new window)

3.
Brown, M.R., Crim, J.W., Arata, R.C., Cai, H.N., Chun, C., and Shen, P. (1999). Identification of a Drosophila brain-gut peptide related to the neuropeptide Y family. Peptides 20, 1035-1042. crossref(new window)

4.
Chen, Y., Veenstra, J.A., Davis, N.T., and Hagedorn, H.H. (1994). comparative study of leucokinin-immunoreactive neurons in insects. Cell Tissue Res. 276, 69-83. crossref(new window)

5.
Chen, J., Choi, M.S., Mizoguchi, A., Veenstra, J.A., Kang, K., Kim, Y.J., and Kwon, J.Y. (2015). Isoform-specific expression of the neuropeptide orcokinin in Drosophila melanogaster. Peptides 68, 50-57. crossref(new window)

6.
Dubreuil, R.R. (2004). Copper cells and stomach acid secretion in the Drosophila midgut. Int. J. Biochem. Cell Biol. 36, 745-752.

7.
Engelstoft, M.S., Egerod, K.L., Lund, M.L., and Schwartz, T.W. (2013). Enteroendocrine cell types revisited. Curr. Opin. Pharmacol. 13, 912-921. crossref(new window)

8.
Hansen, K.K., Hauser, F., Williamson, M., Weber, S.B., and Grimmelikhuijzen, C.J. (2011). The Drosophila genes CG14593 and CG30106 code for G-protein-coupled receptors specifically activated by the neuropeptides CCHamide-1 and CCHamide-2. Biochem. Biophys. Res. Commun. 404, 184-189. crossref(new window)

9.
Hergarden, A.C., Tayler, T.D., and Anderson, D.J. (2012). Allatostatin- A neurons inhibit feeding behavior in adult Drosophila. Proc. Natl. Acad. Sc.i USA 109, 3967-3972. crossref(new window)

10.
LaJeunesse, D.R., Johnson, B., Presnell, J.S., Catignas, K.K., and Zapotoczny, G. (2010). Peristalsis in the junction region of the Drosophila larval midgut is modulated by DH31 expressing enteroendocrine cells. BMC Physiol. 10, 14. crossref(new window)

11.
Lee, T., and Luo, L. (1999). Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22, 451-461. crossref(new window)

12.
Lee, G., and Park, J.H. (2004). Hemolymph sugar homeostasis and starvation-induced hyperactivity affected by genetic manipulations of the adipokinetic hormone-encoding gene in Drosophila melanogaster. Genetics 167, 311-323. crossref(new window)

13.
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. crossref(new window)

14.
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 signalling regulates growth by ERKmediated insulin signalling. Nat. Cell Biol. 10, 468-475. crossref(new window)

15.
Li, S., Torre-Muruzabal, T., Sogaard, K.C., Ren, G.R., Hauser, F., Engelsen, S.M., Podenphanth, M.D., Desjardins, A., and Grimmelikhuijzen, C.J. (2013). Expression patterns of the Drosophila neuropeptide CCHamide-2 and its receptor may suggest hormonal signaling from the gut to the brain. PLoS ONE 8, e76131. crossref(new window)

16.
Luan, H., Lemon, W.C., Peabody, N.C., Pohl, J.B., Zelensky, P.K., Wang, D., Nitabach, M.N., Holmes, T.C., and White, B.H. (2006). Functional dissection of a neuronal network required for cuticle tanning and wing expansion in Drosophila. J. Neurosci. 26, 573-584. crossref(new window)

17.
Melcher, C., and Pankratz, M.J. (2005). Candidate gustatory interneurons modulating feeding behavior in the Drosophila brain. PLoS Biol. 3, e305. crossref(new window)

18.
Micchelli, C.A., and Perrimon, N. (2006). Evidence that stem cells reside in the adult Drosophila midgut epithelium. Nature 439, 475-479. crossref(new window)

19.
Min, S., Chae, B., Jang, Y.H., Choi, S., Lee, S., Jeong, Y.T., Jones, W.D., Moon, S.J., Kim, Y.J., and Chung, J. (2016). Identification of a peptidergic pathway critical to satiety responses in Drosophila. Curr. Biol., in press.

20.
Nassel, D.R., and Winther, A.M. (2010). Drosophila neuropeptides in regulation of physiology and behavior. Prog. Neurobiol. 92, 42-104. crossref(new window)

21.
Ohlstein, B., and Spradling, A. (2006). The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature 439, 470-474. crossref(new window)

22.
Park, J.H., and Kwon, J.Y. (2011). A systematic analysis of Drosophila gustatory receptor gene expression in abdominal neurons which project to the central nervous system. Mol. Cells 32, 375-381. crossref(new window)

23.
Park, S., Sonn J.Y., Oh Y., Lim C., and Choe J. (2014). SIFamide and SIFamide receptor defines a novel neuropeptide signaling to promote sleep in Drosophila. Mol. Cells 37, 295-301. crossref(new window)

24.
Park, J.H., Chen, J., Jang, S., Ahn, T.J., Kang, K., Choi, M.S., and Kwon, J.Y. (2016). A subset of enteroendocrine cells is activated by amino acids in the Drosophila midgut. FEBS Lett., in press.

25.
Price, M.D., Merte, J., Nichols, R., Koladich, P.M., Tobe, S.S., and Bendena, W.G. (2002). Drosophila melanogaster flatline encodes a myotropin orthologue to Manduca sexta allatostatin. Peptides 23, 787-794. crossref(new window)

26.
Psichas, A., Reimann, F., and Gribble, F.M. (2015). Gut chemosensing mechanisms. J. Clin. Invest. 125, 908-917. crossref(new window)

27.
Reiher, W., Shirras, C., Kahnt, J., Baumeister, S., Isaac, R.E., and Wegener, C. (2011). Peptidomics and peptide hormone processing in the Drosophila midgut. J. Proteome Res. 10, 1881-1892. crossref(new window)

28.
Scopelliti, A., Cordero, J.B., Diao, F., Strathdee, K., White, B.H., Sansom, O.J., and Vidal, M. (2014). Local control of intestinal stem cell homeostasis by enteroendocrine cells in the adult Drosophila midgut. Curr. Biol. 24, 1199-1211. crossref(new window)

29.
Siviter, R.J., Coast, G.M., Winther, A.M., Nachman, R.J., Taylor, C.A., Shirras, A.D., Coates, D., Isaac, R.E., and Nassel, D.R. (2000). Expression and functional characterization of a Drosophila neuropeptide precursor with homology to mammalian preprotachykinin A. J. Biol. Chem. 275, 23273-23280. crossref(new window)

30.
Song, W., Veenstra, J.A., and Perrimon, N. (2014). Control of lipid metabolism by tachykinin in Drosophila. Cell Rep. 9, 40-47. crossref(new window)

31.
Vanderveken, M., and O'Donnell, M.J. (2014). Effects of diuretic hormone 31, drosokinin, and allatostatin A on transepithelial K(+) transport and contraction frequency in the midgut and hindgut of larval Drosophila melanogaster. Arch. Insect Biochem. Physiol. 85, 76-93. crossref(new window)

32.
Veenstra, J.A. (2009). Peptidergic paracrine and endocrine cells in the midgut of the fruit fly maggot. Cell Tissue Res. 336, 309-323. crossref(new window)

33.
Veenstra, J.A., and Ida, T. (2014). More Drosophila enteroendocrine peptides: Orcokinin B and the CCHamides 1 and 2. Cell Tissue Res. 357, 607-621. crossref(new window)

34.
Veenstra, J.A., Agricola, H.J., and Sellami, A. (2008). Regulatory peptides in fruit fly midgut. Cell Tissue Res. 334, 499-516. crossref(new window)

35.
Wang, C., Guo, X., Dou, K., Chen, H., and Xi, R. (2015). Ttk69 acts as a master repressor of enteroendocrine cell specification in Drosophila intestinal stem cell lineages. Development 142, 3321-3331. crossref(new window)

36.
Wegener, C., and Veenstra, J.A. (2015). Chemical identity, function and regulation of enteroendocrine peptides in insects. Curr. Opin. Insect Sci. 11, 8-13. crossref(new window)

37.
Williamson, M., Lenz, C., Winther, A.M., Nassel, D.R., and Grimmelikhuijzen, C.J. (2001). Molecular cloning, genomic organization, and expression of a B-type (cricket-type) allatostatin preprohormone from Drosophila melanogaster. Biochem. Biophys. Res. Commun. 281, 544-550. crossref(new window)

38.
Wu, Q., Wen, T., Lee, G., Park, J.H., Cai, H.N., and Shen, P. (2003). Developmental control of foraging and social behavior by the Drosophila neuropeptide Y-like system. Neuron 39, 147-161. crossref(new window)

39.
Zeng, X., and Hou, S.X. (2015). Enteroendocrine cells are generated from stem cells through a distinct progenitor in the adult Drosophila posterior midgut. Development 142, 644-653. crossref(new window)