CCHamide-2 is an orexigenic brain-gut peptide in Drosophila

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Ren, Guilin R ^a   Hauser, Frank ^a   Rewitz, Kim F ^a   Kondo, Shu ^b   Engelbrecht, Alexander F ^a   Didriksen, Anders K ^a   Schjøtt, Suzanne R ^a   Sembach, Frederikke E ^a   Li, Shizhong ^a   Søgaard, Karen C ^a   Søndergaard, Leif ^a   Grimmelikhuijzen, Cornelis J P ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b NATIONAL INSTITUTE OF GENETICS   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN PEPTIDE; CCHAMIDE 1; CCHAMIDE 2; MESSENGER RNA; UNCLASSIFIED DRUG; CCH-AMIDE-2 NEUROPEPTIDE, DROSOPHILA; DNA; DROSOPHILA PROTEIN; NEUROPEPTIDE;

ARTICLE; CCHAMIDE 1 GENE; CCHAMIDE 2 GENE; DEVELOPMENTAL STAGE; DILP2 GENE; DILP3 GENE; DROSOPHILA MELANOGASTER; FAT BODY; FEEDING BEHAVIOR; FEMALE; GENE; GENE DELETION; GENE EXPRESSION; GENE FUNCTION; HETEROZYGOSITY; HOMOZYGOSITY; INSECT DEVELOPMENT; LARVAL DEVELOPMENT; LOCOMOTION; MALE; NONHUMAN; PHENOTYPE; AMINO ACID SEQUENCE; ANIMAL; BRAIN; DROSOPHILA; GENETICS; GROWTH, DEVELOPMENT AND AGING; INTESTINE; LARVA; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PHYSIOLOGY;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BRAIN; DNA; DROSOPHILA; DROSOPHILA PROTEINS; FEEDING BEHAVIOR; INTESTINES; LARVA; LOCOMOTION; MOLECULAR SEQUENCE DATA; MUTATION; NEUROPEPTIDES;

EID: 84940416598     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0133017     Document Type: Article

References (38)

1. Zdárek J, Nachman RJ, Denlinger DL (2000) Parturition hormone in the tsetse Glossina morsitans: activity in reproductive tissues from other species and response of tsetse to identified neuropeptides and other neuroactive compounds. J Insect Physiol 46: 213-219. PMID: 12770225
2. Roller L, Yamanaka N, Watanabe K, Daubnerová I, Zitnan D, Kataoka H et al. (2008) The unique evolution of neuropeptide genes in the silkworm Bombyx mori. Insect Biochem Mol Biol 38: 1147-1157. PMID: 19280707
3. Hansen KK, Hauser F, Williamson M, Weber SB, Grimmelikhuijzen CJP (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. doi: 10.1016/j.bbrc.2010.11.089 PMID: 21110953
4. Reiher W, Shirras C, Kahnt J, Baumeister S, Isaac RE, Wegener C (2011) Peptidomics and peptide hormone processing in the Drosophila midgut. J Proteome Res 10: 1881-1892. doi: 10.1021/pr101116g PMID: 21214272
5. Ida T, Takahashi T, Tominaga H, Sato T, Sano H, Kume K et al. (2012) Isolation of the bioactive peptides CCHamide-1 and CCHamide-2 from Drosophila and their putative role in appetite regulation as ligands for G protein-coupled receptors. Front Endocrinol 3: 177.
6. Zoephel J, Reiher W, Rexer KH, Kahnt J, Wegener C (2012) Peptidomics of the agriculturally damaging larval stage of the cabbage root fly Delia radicum (Diptera: Anthomyiidae). PLoS One 7:e41543. doi: 10.1371/journal.pone.0041543 PMID: 22848525
7. Nygaard S, Zhang G, Schiøtt M, Li C, Wurm Y, Hu H et al. (2011) The genome of the leaf-cutting ant Acromyrmex echinatior suggests key adaptations to advanced social life and fungus farming. Genome Res 21: 1339-1348. doi: 10.1101/gr.121392.111 PMID: 21719571
8. Poulsen M, Hu H, Li C, Chen Z, Xu L, Otani S et al. (2014) Complementary symbiont contributions to plant decomposition in a fungus-farming termite. Proc NatI Acad Sci U S A 111: 14500-14505.
9. Dircksen H, Neupert S, Predel R, Verleyen P, Huybrechts J, Strauss J et al. (2011) Genomics, transcriptomics and peptidomics of Daphnia pulex neuropeptides and protein hormones. J Proteome Res 10: 4478-4504. doi: 10.1021/pr200284e PMID: 21830762
10. Christie AE (2014) Expansion of the Litopenaeus vannamei and Penaeus monodon peptidomes using transcriptome shotgun assembly sequence data. Gen Comp Endocrinol: 206: 235-254. doi: 10.1016/j.ygcen.2014.04.015 PMID: 24787055
11. Christie AE (2015) In silico characterization of the neuropeptidome of the Western black widow spider Latrodectus hesperus. Gen Comp Endocrinol 210: 63-80. doi: 10.1016/j.ygcen.2014.10.005 PMID: 25449184
12. Chipman AD, Ferrier DE, Brena C, Qu J, Hughes DS, Schröder R et al. (2014). The first myriapod genome sequence reveals conservative arthropod gene content and genome organization in the centipede Strigamia maritima. PLoS Biol 12:e1002005. doi: 10.1371/journal.pbio.1002005 PMID: 25423365
13. Li S, Torre-Muruzabal T, Søgaard KC, Ren GR, Hauser F, Engelsen SM et al. (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. doi: 10.1371/journal.pone.0076131 PMID: 24098432
14. Veenstra JA, Ida T (2014) More Drosophila enteroendocrine peptides: Orcokinin B and the CCHamides 1 and 2. Cell Tissue Res 357: 607-621. doi: 10.1007/s00441-014-1880-2 PMID: 24850274
15. Kondo S, Ueda R (2013) Highly improved gene targeting by germline-specific Cas9 expression in Drosophila. Genetics 195: 715-721. doi: 10.1534/genetics.113.156737 PMID: 24002648
16. Kondo S (2014) New horizons in genome engineering of Drosophila melanogaster. Genes Genet Syst 89: 3-8. PMID: 24817756
17. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: R0034.1-R0034.11.
18. Sano H, Nakamura A, Texada MJ, Truman JW, Ishimoto H, Kamikouchi A et al. (2015) The nutrient-responsive hormone CCHamide-2 controls growth by regulating insulin-like peptides in the brain of Drosophila melanogaster. PLoS Genet 11:e1005209. doi: 10.1371/journal.pgen.1005209 PMID: 26020940
19. Deshpande SA, Carvalho GB, Amador A, Phillips AM, Hoxha S, Lizotte KJ et al. (2014) Quantifying Drosophila food intake: comparative analysis of current methodology. Nat Methods 11: 535-540. doi: 10.1038/nmeth.2899 PMID: 24681694
20. Wu Q, Wen T, Lee G, Park JH, Cai HN, Shen P (2003) Developmental control of foraging and social behavior by the Drosophila neuropeptide Y-like system. Neuron 39: 147-161. PMID: 12848939
21. Schoofs A, Hückesfeld S, Schlegel P, Miroschnikow A, Peters M, Zeymer M et al. (2014) Selection of motor programs for suppressing food intake and inducing locomotion is the Drosophila brain. PLoS Biol 12:e1001893. doi: 10.1371/journal.pbio.1001893 PMID: 24960360
22. Wong R, Piper MD, Wertheim B, Partridge L (2009) Quantification of food intake in Drosophila. PLoS One 4:e6063. doi: 10.1371/journal.pone.0006063 PMID: 19557170
23. Galagovsky D, Katz MJ, Acevedo JM, Sorianello E, Glavic A, Wappner P (2014) The Drosophila insulin-degrading enzyme restricts growth by modulating the PI3K pathway in a cell-autonomous manner. Mol Biol Cell 25: 916-924. doi: 10.1091/mbc.E13-04-0213 PMID: 24430872
24. Chiu JC, Low KH, Pike DH, Yildrim E, Edery I (2010) Assaying locomotor activity to study circadian rhythms and sleep parameters in Drosophila. J Vis Exp 43: Pii: 2157. doi: 10.3791/2157 PMID: 20972399
25. Ro J, Harvanek ZM, Pletcher SD (2014) FLIC: high-throughput, continuous analysis of feeding behaviors in Drosophila. PLoS One 9:e101107. doi: 10.1371/journal.pone.0101107 PMID: 24978054
26. Rulifson EJ, Kim SK, Nusse R (2002) Ablation of insulin-producing neurons in flies: Growth and diabetic phenotypes. Science 296: 1118-1120. PMID: 12004130
27. Parker J (2011) Morphogens, nutrients, and the basis of organ scaling. Evol Dev 13: 304-314. doi: 10.1111/j.1525-142X.2011.00481.x PMID: 21535468
28. Nijhout HF, Riddiford LM, Mirth CK, Shingleton AW, Suziki Y, Callier V (2014) The developmental control of size in insects. Wiley Interdiscip Rev Dev Biol 3: 113-134. doi: 10.1002/wdev.124 PMID: 24902837
29. Mirth CK, Shingleton AW (2012) Integrating body and organ size in Drosophila: recent advances and outstanding problems. Front Endocrinol (Lausanne) 3:49
30. Söderberg JA, Carlsson MA, Nässel DR (2012). Insulin-producing cells in the Drosophila brain also express satiety inducing cholecystokinin-like peptide, drosulfakinin. Front. Endocrinol. 3: 109.
31. Erion R, Sehgal A (2013) Regulation of insect behavior via the insulin-signaling pathway. Front Physiol 4: 353. doi: 10.3389/fphys.2013.00353 PMID: 24348428
32. Park S, Alfa RW, Topper SM, Kim GE, Kockel L, Kim SK (2014) A genetic strategy to measure circulating Drosophila insulin reveals genes regulating insulin production and secretion. PLoS Genet 10: e1004555 doi: 10.1371/journal.pgen.1004555 PMID: 25101872
33. Géminard C, Rulifson EJ, Léopold P (2009) Remote control of insulin secretion by fat cells in Drosophila. Cell metab 10: 199-207. doi: 10.1016/j.cmet.2009.08.002 PMID: 19723496
34. Lee KS, You KH, Choo JK, Han YM, Yu K (2004) Drosophila short neuropeptide F regulates food intake and body size. J Biol Chem 279: 50781-50789. PMID: 15385546
35. Nässel DR, Wegener C (2011) A comparative review of short and long neuropeptide F signaling in invertebrates: Any similarities to vertebrate neuropeptide Y signaling? Peptides 32: 1335-1355. doi: 10.1016/j.peptides.2011.03.013 PMID: 21440021
36. Veenstra JA (2009) Peptidergic paracrine and endocrine cells in the midgut of the fruit fly maggot. Cell Tissue Res 336: 309-323. doi: 10.1007/s00441-009-0769-y PMID: 19319573
37. Hergarden AC, Tayler TD, Anderson DJ (2012) Allatostatin-A neurons inhibit feeding behavior in adult Drosophila. Proc Natl Acad Sci U S A 109: 3967-3972. doi: 10.1073/pnas.1200778109 PMID: 22345563
38. Eipper BA, Stoffers DA, Mains RE (1992) The biosynthesis of neuropeptides: peptide alpha-amidation. Annu Rev Neurosci 15: 57-85. PMID: 1575450