Neuropeptide Mapping of Dimmed Cells of Adult Drosophila Brain

Journal of the American Society for Mass Spectrometry

Volumn 29, Issue 5, 2018, Pages 890-902

  Diesner, Max ^a   Predel, Reinhard ^a   Neupert, Susanne ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Dimmed; DIMMED; Drosophila melanogaster; Individual cell mapping; Neuropeptides; Peptidomics; Single cell mass spectrometry

Indexed keywords

CYTOLOGY; FACSIMILE; MAPPING; MASS SPECTROMETRY; NEURONS; PEPTIDES; TRANSCRIPTION;

DIMMED; DROSOPHILA MELANOGASTER; INDIVIDUAL CELLS; NEUROPEPTIDES; PEPTIDOMICS; SINGLE CELLS;

BRAIN MAPPING;

GREEN FLUORESCENT PROTEIN; NEUROPEPTIDE; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; DIMM PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN GANGLION; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; FEMALE; INSECT CELL; INTERNEURON; MALE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NEUROSECRETORY CELL; NONHUMAN; PEPTIDE MAPPING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; AMINO ACID SEQUENCE; ANATOMY AND HISTOLOGY; ANIMAL; BRAIN CHEMISTRY; CHEMISTRY; CYTOLOGY; MATRIX-ASSISTED LASER DESORPTION-IONIZATION MASS SPECTROMETRY; NERVE CELL; PROCEDURES;

AMINO ACID SEQUENCE; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BRAIN CHEMISTRY; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; MALE; NEURONS; NEUROPEPTIDES; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 85046698088     PISSN: 10440305     EISSN: 18791123     Source Type: Journal    
DOI: 10.1007/s13361-017-1870-1     Document Type: Article

References (51)

1. Hewes, R.S., Taghert, P.H.: Neuropeptides and neuropeptide receptors in the Drosophila melanogaster genome. Genome Res. 11, 1126–1142 (2001)
2. Vanden Broeck, J.: Neuropeptides and their precursors in the fruitfly. Drosophila melanogaster. Peptides. 22, 241–254 (2001)
3. Hauser, F., Cazzamali, G., Williamson, M., Blenau, W., Grimmelikhuijzen, C.J.: A review of neurohormone GPCRs present in the fruitfly Drosophila melanogaster and the honey bee Apis mellifera. Prog. Neurobiol. 80, 1–19 (2006)
4. Pauls, D., Chen, J., Reiher, W., Vanselow, J.T., Schlosser, A., Kahnt, J., Wegener, C.: Peptidomics and processing of regulatory peptides in the fruit fly Drosophila. EuPA Open Proteomics. 3, 114–127 (2014)
5. Nässel, D.R., Winther, A.M.: Drosophila neuropeptides in regulation of physiology and behavior. Prog. Neurobiol. 92, 42–104 (2010)
6. Taghert, P.H., Nitabach, M.N.: Peptide neuromodulation in invertebrate model systems. Neuron. 76, 82–97 (2012)
7. Park, D., Veenstra, J.A., Park, J.H., Taghert, P.H.: Mapping peptidergic cells in Drosophila: where DIMM fits in. PLoS ONE. 3, e1896 (2008)
8. Park, D., Taghert, P.H.: Peptidergic neurosecretory cells in insects: organization and control by the bHLH protein DIMMED. Gen. Comp. Endocrinol. 162, 2–7 (2009)
9. Hamanaka, Y., Park, D., Yin, P., Annangudi, S.P., Edwards, T.N., Sweedler, J., Meinertzhagen, I.A., Taghert, P.H.: Transcriptional orchestration of the regulated secretory pathway in neurons by the bHLH protein DIMM. Curr. Biol. 20, 9–18 (2010)
10. Hadžić, T., Park, D., Abruzzi, K.C., Yang, L., Trigg, J.S., Rohs, R., Rosbash, M, Taghert, P.H.: Genome-wide features of neuroendocrine regulation in Drosophila by the basic helix-loop-helix transcription factor DIMMED Nucl. Acids Res: gku 1377 (2015)
11. Liu, Y., Luo, J., Nässel, D.R.: The Drosophila transcription factor Dimmed affects neuronal growth and differentiation in multiple ways depending on neuron type and developmental stage. Front Mol Neurosci. 13, 97 (2016)
12. Gauthier, S.A., Hewes, R.S.: Transcriptional regulation of neuropeptide and peptide hormone expression by the Drosophila dimmed and cryptocephal genes. J. Exp. Biol. 209, 1803–1815 (2006)
13. Hewes, R.S., Park, D., Gauthier, S.A., Schaefer, A.M., Taghert, P.H.: The bHLH protein Dimmed controls neuroendocrine cell differentiation in Drosophila. Development. 130, 1771–1781 (2003)
14. Yew, J.Y., Wang, Y., Barteneva, N., Dikler, S., Kutz-Naber, K.K., Li, L., Kravitz, E.A.: 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 (2009) Erratum in: J. Proteome Res. 8, 3786 (2009)
15. Neupert, S., Predel, R.: Mass spectrometric analysis of single identified neurons of an insect. Biochem. Biophys. Res. Commun. 327, 640–645 (2005)
16. Lee, T., Luo, L.: Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron. 22, 451–461 (1999)
17. Veenstra, J.A.: Mono- and dibasic proteolytic cleavage sites in insect neuroendocrine peptide precursors. Arch. Insect Biochem. Physiol. 2, 49–63 (2000)
18. Pitman, J.L., Huetteroth, W., Burke, C.J., Krashes, M.J., Lai, S.L., Lee, T., Waddell, S.: A pair of inhibitory neurons are required to sustain labile memory in the Drosophila mushroom body. Curr. Biol. 21, 855–861 (2011)
19. Zitnan, D., Sehnal, F., Bryant, P.J.: Neurons producing specific neuropeptides in the central nervous system of normal and pupariation-delayed Drosophila. Dev. Biol. 156, 117–135 (1993)
20. Siegmund,T., Korge, G.: Innervation of the ring gland of Drosophila melanogaster. J. Comp. Neurol. 431, 481–491 (2001)
21. McCormick, J., Nichols, R.: Spatial and temporal expression identify dromyosuppressin as a brain-gut peptide in Drosophila melanogaster. J. Comp. Neurol. 338, 278–288 (1993)
22. Jiang, H., Lkhagva, A., Daubnerová, I., Chae, H.S., Šimo, L., Jung, S.H., Yoon, Y.K., Lee, N.R., Seong, J.Y., Žitňan, D., Park, Y., Kim, Y.J.: Natalisin, a tachykinin-like signaling system, regulates sexual activity and fecundity in insects. Proc. Natl. Acad. Sci. USA. 110, E3526–E3534 (2013)
23. Min, S., Chae, H.S., Jang, Y.H., Choi, S., Lee, S., Jeong, Y.T., Jones, W.D., Moon, S.J., Kim, Y.J., Chung, J.: Identification of a peptidergic pathway critical to satiety responses in Drosophila. Curr. Biol. 26, 814–820 (2016)
24. Huang, J., Liu, W., Qi, Y.X., Luo, L., Montell, C.: Neuromodulation of courtship drive through tyramine-responsive neurons in the Drosophila brain. Current Biology. 26, 2246–2256 (2016)
25. Yoon, J.G., Stay, B.: Immunocytochemical localization of Diploptera punctata allatostatin-like peptide in Drosophila melanogaster. J. Comp. Neurol. 363, 475–488 (1995)
26. Derst, C., Dircksen, H., Meusemann, K., Zhou, X., Liu, S., Predel, R.: Evolution of neuropeptides in non-pterygote hexapods. BMC Evol. Biol. 16, 51 (2016)
27. Veenstra, J.A.: The contribution of the genomes of a termite and a locust to our understanding of insect neuropeptides and neurohormones. Front. Physiol. 19, 454 (2014)
28. Predel, R., Wegener, C.: Biology of the CAPA peptides in insects. Cell Mol. Life Sci. 63, 2477–2490 (2006)
29. Rosenkilde, C., Cazzamali, G., Williamson, M., Hauser, F., Søndergaard, L., DeLotto, R., Grimmelikhuijzen, C.J.: Molecular cloning, functional expression, and gene silencing of two Drosophila receptors for the Drosophila neuropeptide pyrokinin-2. Biochem. Biophys. Res. Commun. 309, 485–494 (2003)
30. Predel, R., Wegener, C., Russell, W.K., Tichy, S.E., Russell, D.H., Nachman, R.J.: Peptidomics of CNS-associated neurohemal systems of adult Drosophila melanogaster: a mass spectrometric survey of peptides from individual flies. J. Comp. Neurol. 474, 379–392 (2004)
31. Wegener, C., Reinl, T., Jänsch, L., Predel, R.: Direct mass spectrometric peptide profiling and fragmentation of larval peptide hormone release sites in Drosophila melanogaster reveals tagma-specific peptide expression and differential processing. J. Neurochem. 96, 1362–1374 (2006)
32. Kean, L., Cazenave, W., Costes, L., Broderick,K.E., Graham, S., Pollock, V.P., Davies, S.A., Veenstra, J.A., Dow, J.A.: Two nitridergic peptides are encoded by the gene capability in Drosophila melanogaster. Am. J. Physiol. Regul. Integr. Comp. Physiol. 282, 1297–1307 (2002)
33. Bader, R., Wegener, C., Pankratz, M.J.: Comparative neuroanatomy and genomics of hugin and pheromone biosynthesis activating neuropeptide (PBAN). Fly (Austin). 4, 228–231 (2007)
34. Schlegel, P., Texada, M.J., Miroschnikow, A., Schoofs, A., Hückesfeld, S., Peters, M., Schneider-Mizell, C.M., Lacin, H., Li, F., Fetter, R.D., Truman, J.W., Cardona, A., Pankratz, M.J.: Synaptic transmission parallels neuromodulation in a central food-intake circuit. Elife. 5, e16799 (2016)
35. Hückesfeld, S., Peters, M., Pankratz, M.J.: Central relay of bitter taste to the protocerebrum by peptidergic interneurons in the Drosophila brain. Nat. Commun. 7, 12796 (2016)
36. Melcher, C., Pankratz, M.J.: Candidate gustatory interneurons modulating feeding behavior in the Drosophila brain. PLoS Biol. 3, e305 (2005)
37. Neupert, S., Johard, H.A., Nässel, D.R., Predel, R.: Single-cell peptidomics of Drosophila melanogaster neurons identified by Gal4-driven fluorescence. Anal. Chem. 79, 3690–3694 (2007). Erratum in: Anal. Chem. 84, 5164 (2012)
38. Meng, X., Wahlström, G., Immonen, T., Kolmer, M., Tirronen, M., Predel, R., Kalkkinen, N., Heino, T.I., Sariola, H., Roos, C.: The Drosophila hugin gene codes for myostimulatory and ecdysis-modifying neuropeptides. Mech. Dev. 117, 5–13 (2002)
39. Kubiak, T.M., Larsen, M.J., Burton, K.J., Bannow, C.A., Martin, R.A., Zantello, M.R., Lowery, D.E.: Cloning and functional expression of the first Drosophila melanogaster sulfakinin receptor DSK-R1. Biochem. Biophys. Res. Commun. 291, 313–320 (2002)
40. Nichols, R., Lim, I.A.: Spatial and temporal immunocytochemical analysis of drosulfakinin (Dsk) gene products in the Drosophila melanogaster central nervous system. Cell Tissue Res. 283, 107–116 (1996)
41. Agricola, H.J., Bräunig, P.: Comparative aspects of peptidergic signaling pathways in the nervous systems of arthropods. EXS. 72, 303–327 (1995)
42. Choi, Y.J., Lee, G., Hall, J.C., Park, J.H.: Comparative analysis of corazonin-encoding genes (Crz's) in Drosophila species and functional insights into Crz-expressing neurons. J. Comp. Neurol. 482, 372–385 (2005)
43. Nässel, D.R., Enell, L.E., Santos, J.G., Wegener, C., Johard, H.A.: A large population of diverse neurons in the Drosophila central nervous system expresses short neuropeptide F, suggesting multiple distributed peptide functions. BMC Neurosci. 19, 9–90 (2008)
44. Helfrich-Förster, C.: The neuroarchitecture of the circadian clock in the brain of Drosophila melanogaster. Microsc. Res. Technol. 62, 94–102 (2003)
45. Schoofs, L., Baggerman, G.: Peptidomics in Drosophila melanogaster. Brief Funct. Genomic Proteom. 2, 114–120 (2003)
46. Salisbury, J.P., Boggio, K.J., Hsu, Y.W., Quijada, J., Sivachenko, A., Gloeckner, G., Kowalski, P.J., Easterling, M.L., Rosbash, M., Agar, J.N.: A rapid MALDI-TOF mass spectrometry workflow for Drosophila melanogaster differential neuropeptidomics. Mol. Brain. 6, 60 (2013)
47. Predel, R., Neupert, S., Garczynski, S.F., Crim, J.W., Brown, M.R., Russell, W.K., Kahnt, J., Russell, D.H., Nachman, R.J.: Neuropeptidomics of the mosquito Aedes aegypti. J. Proteome Res. 9, 2006–2015 (2010)
48. Verleyen, P., Baggerman, G., Wiehar,t U., Schoeters, E., Van Lommel, A., De Loof, A., Schoofs, L.: Expression of a novel neuropeptide, NVGTLARDFQLPIPNamide, in the larval and adult brain of Drosophila melanogaster. J. Neurochem. 88, 311–319 (2004)
49. Brown, M.R., Crim, J.W., Arata, R.C., Cai, H.N., Chun, C., Shen, P.: Identification of a Drosophila brain-gut peptide related to the neuropeptide Y family. Peptides. 20, 1035–1042 (1999)
50. Wen, T., Parrish, C.A., Xu, D., Wu, Q., Shen, P.: Drosophila neuropeptide F and its receptor, NPFR1, define a signaling pathway that acutely modulates alcohol sensitivity. Proc. Natl. Acad. Sci. USA. 102, 2141–2146 (2005)
51. Krashes, M.J., DasGupta, S., Vreede, A., White, B., Armstrong, J.D., Waddell, S.: A neural circuit mechanism integrating motivational state with memory expression in Drosophila. Cell. 139, 416–427 (2009)