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Advances in Understanding the Generation and Specification of Unique Neuronal Sub-types from Drosophila Neuropeptidergic Neurons

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Abstract

The central nervous system (CNS) contains a daunting diversity of neuronal cell types. One of the major challenges of developmental neurobiology is to understand the regulatory mechanisms underlying this vast complexity. Studies in the Drosophila melanogaster (Drosophila) model system has contributed greatly to our understanding of neuronal cell sub-type specification, and the majority of mechanisms and genes identified in this system has proved to be of great value, and often more or less directly transferable to studies of mammalian neuro-development. In Drosophila, studies of the developmental generation of numerous different neuropeptide neurons have been highly informative, since these neurons are generated in a highly restricted and reproducible manner. In addition, neuropeptides are expressed at high levels and their regulatory regions have proven comparatively condensed, facilitating the generation of a multitude of antibodies and transgenic markers. Here, we first provide a general background to Drosophila CNS development. Then, we focus in more detail on various well studied neuropeptide neurons identified in this system, and describe what has been learned regarding the generation and differentiation of these highly unique neuronal sub-types. We intend this review to provide an overview of the variety of mechanisms that operate throughout the developmental period to generate highly unique neuronal sub-types. Finally, we conclude with some general remarks and perspectives regarding neuronal sub-type specification in general.

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References

  • Aberle, H., Haghighi, A. P., Fetter, R. D., McCabe, B. D., Magalhaes, T. R., & Goodman, C. S. (2002). Wishful thinking encodes a BMP type II receptor that regulates synaptic growth in Drosophila. Neuron, 33, 545–558.

    Article  CAS  PubMed  Google Scholar 

  • Abruzzi, K. C., Rodriguez, J., Menet, J. S., Desrochers, J., Zadina, A., Luo, W., et al. (2011). Drosophila CLOCK target gene characterization: Implications for circadian tissue-specific gene expression. Genes & Development, 25, 2374–2386.

    Article  CAS  Google Scholar 

  • Akam, M. (1987). The molecular basis for metameric pattern in the Drosophila embryo. Development (Cambridge, England) 101, 1–22.

    Google Scholar 

  • Al-Anzi, B., Armand, E., Nagamei, P., Olszewski, M., Sapin, V., Waters, C., et al. (2010). The leucokinin pathway and its neurons regulate meal size in Drosophila. Current Biology, 20, 969–978.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Allan, D. W., Park, D., St Pierre, S. E., Taghert, P. H., & Thor, S. (2005). Regulators acting in combinatorial codes also act independently in single differentiating neurons. Neuron, 45, 689–700.

    Article  CAS  PubMed  Google Scholar 

  • Allan, D. W., Pierre, S. E., Miguel-Aliaga, I., & Thor, S. (2003). Specification of neuropeptide cell identity by the integration of retrograde BMP signaling and a combinatorial transcription factor code. Cell, 113, 73–86.

    Article  CAS  PubMed  Google Scholar 

  • Allan, D. W., & Thor, S. (2015). Transcriptional selectors, masters, and combinatorial codes: Regulatory principles of neural subtype specification. Wiley interdisciplinary reviews Developmental biology.

    Google Scholar 

  • Anderson, K. V. (1998). Pinning down positional information: Dorsal-ventral polarity in the Drosophila embryo. Cell, 95, 439–442.

    Article  CAS  PubMed  Google Scholar 

  • Barad, O., Hornstein, E., & Barkai, N. (2011). Robust selection of sensory organ precursors by the notch-delta pathway. Current Opinion in Cell Biology, 23, 663–667.

    Article  CAS  PubMed  Google Scholar 

  • Baumgardt, M., Karlsson, D., Salmani, B. Y., Bivik, C., MacDonald, R. B., Gunnar, E., et al. (2014). Global programmed switch in neural daughter cell proliferation mode triggered by a temporal gene cascade. Developmental Cell, 30, 192–208.

    Article  CAS  PubMed  Google Scholar 

  • Baumgardt, M., Karlsson, D., Terriente, J., Diaz-Benjumea, F. J., & Thor, S. (2009). Neuronal subtype specification within a lineage by opposing temporal feed-forward loops. Cell, 139, 969–982.

    Article  CAS  PubMed  Google Scholar 

  • Baumgardt, M., Miguel-Aliaga, I., Karlsson, D., Ekman, H., & Thor, S. (2007). Specification of neuronal identities by feedforward combinatorial coding. PLoS Biology, 5, 295–308.

    Article  CAS  Google Scholar 

  • Beatus, P., & Lendahl, U. (1998). Notch and neurogenesis. Journal of Neuroscience Research, 54, 125–136.

    Article  CAS  PubMed  Google Scholar 

  • Beckwith, E. J., Gorostiza, E. A., Berni, J., Rezaval, C., Perez-Santangelo, A., Nadra, A. D., & Ceriani, M. F. (2013). Circadian period integrates network information through activation of the BMP signaling pathway. PLoS Biology, 11, e1001733.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bello, B. C., Hirth, F., & Gould, A. P. (2003). A pulse of the Drosophila Hox protein abdominal-A schedules the end of neural proliferation via neuroblast apoptosis. Neuron, 37, 209–219.

    Article  CAS  PubMed  Google Scholar 

  • Benito-Sipos, J., Estacio-Gomez, A., Moris-Sanz, M., Baumgardt, M., Thor, S., & Diaz-Benjumea, F. J. (2010). A genetic cascade involving klumpfuss, nab and castor specifies the abdominal leucokinergic neurons in the Drosophila CNS. Development (Cambridge, England), 137, 3327–3336.

    Google Scholar 

  • Benito-Sipos, J., Ulvklo, C., Gabilondo, H., Baumgardt, M., Angel, A., Torroja, L., et al. (2011). Seven up acts as a temporal factor during two different stages of neuroblast 5–6 development. Development (Cambridge, England), 138, 5311–5320.

    Google Scholar 

  • Benveniste, R. J., & Taghert, P. H. (1999). Cell type-specific regulatory sequences control expression of the Drosophila FMRF-NH2 neuropeptide gene. Journal of Neurobiology, 38, 507–520.

    Article  CAS  PubMed  Google Scholar 

  • Benveniste, R. J., Thor, S., Thomas, J. B., & Taghert, P. H. (1998). Cell type-specific regulation of the Drosophila FMRF-NH2 neuropeptide gene by Apterous, a LIM homeodomain transcription factor. Development (Cambridge, England), 125, 4757–4765.

    Google Scholar 

  • Berger, C., Kannan, R., Myneni, S., Renner, S., Shashidhara, L. S., & Technau, G. M. (2010). Cell cycle independent role of cyclin E during neural cell fate specification in Drosophila is mediated by its regulation of prospero function. Developmental Biology, 337, 415–424.

    Article  CAS  PubMed  Google Scholar 

  • Berger, C., Pallavi, S. K., Prasad, M., Shashidhara, L. S., & Technau, G. M. (2005). A critical role for cyclin E in cell fate determination in the central nervous system of Drosophila melanogaster. Nature Cell Biology, 7, 56–62.

    Article  CAS  PubMed  Google Scholar 

  • Bhat, K. M. (1999). Segment polarity genes in neuroblast formation and identity specification during Drosophila neurogenesis. BioEssays, 21, 472–485.

    Article  CAS  PubMed  Google Scholar 

  • Bhat, K. M., Gaziova, I., & Katipalla, S. (2011). Neuralized mediates asymmetric division of neural precursors by two distinct and sequential events: Promoting asymmetric localization of numb and enhancing activation of notch-signaling. Developmental Biology, 351, 186–198.

    Article  CAS  PubMed  Google Scholar 

  • Birkholz, O., Rickert, C., Berger, C., Urbach, R., & Technau, G. M. (2013a). Neuroblast pattern and identity in the Drosophila tail region and role of doublesex in the survival of sex-specific precursors. Development (Cambridge, England), 140, 1830–1842.

    Google Scholar 

  • Birkholz, O., Vef, O., Rogulja-Ortmann, A., Berger, C., & Technau, G. M. (2013b). Abdominal-B and caudal inhibit the formation of specific neuroblasts in the Drosophila tail region. Development (Cambridge, England), 140, 3552–3564.

    Google Scholar 

  • Boone, J. Q., & Doe, C. Q. (2008). Identification of Drosophila type II neuroblast lineages containing transit amplifying ganglion mother cells. Developmental neurobiology, 68, 1185–1195.

    Article  PubMed  PubMed Central  Google Scholar 

  • Broadus, J., & Doe, C. Q. (1995). Evolution of neuroblast identity: Seven-up and prospero expression reveal homologous and divergent neuroblast fates in Drosophila and Schistocerca. Development (Cambridge, England), 121, 3989–3996.

    Google Scholar 

  • Brody, T., & Odenwald, W. F. (2000). Programmed transformations in neuroblast gene expression during Drosophila CNS lineage development. Developmental Biology, 226, 34–44.

    Article  CAS  PubMed  Google Scholar 

  • Brown, H. L., Cherbas, L., Cherbas, P., & Truman, J. W. (2006). Use of time-lapse imaging and dominant negative receptors to dissect the steroid receptor control of neuronal remodeling in Drosophila. Development (Cambridge, England), 133, 275–285.

    Google Scholar 

  • Buss, R. R., & Oppenheim, R. W. (2004). Role of programmed cell death in normal neuronal development and function. Anatomical science international, 79, 191–197.

    Article  PubMed  Google Scholar 

  • Buss, R. R., Sun, W., & Oppenheim, R. W. (2006). Adaptive roles of programmed cell death during nervous system development. Annual Review of Neuroscience, 29, 1–35.

    Article  CAS  PubMed  Google Scholar 

  • Capovilla, M., & Botas, J. (1998). Functional dominance among Hox genes: Repression dominates activation in the regulation of Dpp. Development (Cambridge, England), 125, 4949–4957.

    Google Scholar 

  • Cau, E., & Blader, P. (2009). Notch activity in the nervous system: To switch or not switch? Neural development, 4, 36.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cenci, C., & Gould, A. P. (2005). Drosophila grainyhead specifies late programmes of neural proliferation by regulating the mitotic activity and Hox-dependent apoptosis of neuroblasts. Development (Cambridge, England), 132, 3835–3845.

    Google Scholar 

  • Chia, W., & Yang, X. (2002). Asymmetric division of Drosophila neural progenitors. Current Opinion in Genetics & Development, 12, 459–464.

    Article  CAS  Google Scholar 

  • Chin, A., Reynolds, E., & Scheller, R. H. (1990). Organization and expression of the Drosophila FMRFamide-related prohormone gene. DNA and Cell Biology, 9, 263–271.

    Article  CAS  PubMed  Google Scholar 

  • Chitnis, A. B. (1995). The role of notch in lateral inhibition and cell fate specification. Molecular and cellular neurosciences, 6, 311–321.

    Article  CAS  Google Scholar 

  • Choi, S. H., Lee, G., Monahan, P., & Park, J. H. (2008). Spatial regulation of corazonin neuropeptide expression requires multiple cis-acting elements in Drosophila melanogaster. The Journal of Comparative Neurology, 507, 1184–1195.

    Article  CAS  PubMed  Google Scholar 

  • Choi, Y. J., Lee, G., & Park, J. H. (2006). Programmed cell death mechanisms of identifiable peptidergic neurons in Drosophila melanogaster. Development (Cambridge, England), 133, 2223–2232.

    Google Scholar 

  • Cleary, M. D., & Doe, C. Q. (2006). Regulation of neuroblast competence: multiple temporal identity factors specify distinct neuronal fates within a single early competence window. Genes & Development, 20, 429–434.

    Article  CAS  Google Scholar 

  • da Silva, S., & Wang, F. (2011). Retrograde neural circuit specification by target-derived neurotrophins and growth factors. Current Opinion in Neurobiology, 21, 61–67.

    Article  PubMed  CAS  Google Scholar 

  • Deneris, E. S., & Hobert, O. (2014). Maintenance of postmitotic neuronal cell identity. Nature Neuroscience, 17, 899–907.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dewey, E. M., McNabb, S. L., Ewer, J., Kuo, G. R., Takanishi, C. L., Truman, J. W., et al. (2004). Identification of the gene encoding bursicon, an insect neuropeptide responsible for cuticle sclerotization and wing spreading. Current Biology, 14, 1208–1213.

    Article  CAS  PubMed  Google Scholar 

  • Dittrich, R., Bossing, T., Gould, A. P., Technau, G. M., & Urban, J. (1997). The differentiation of the serotonergic neurons in the Drosophila ventral nerve cord depends on the combined function of the zinc finger proteins Eagle and Huckebein. Development (Cambridge, England), 124, 2515–2525.

    Google Scholar 

  • Doe, C. Q. (1992). Molecular markers for identified neuroblasts and ganglion mother cells in the Drosophila central nervous system. Development (Cambridge, England), 116, 855–863.

    Google Scholar 

  • Doe, C. Q. (2008). Neural stem cells: Balancing self-renewal with differentiation. Development (Cambridge, England), 135, 1575–1587.

    Google Scholar 

  • Doe, C. Q., & Goodman, C. S. (1993). Embryonic development of the Drosophila central nervous system. In M. Bate & A. Martinez Arias (Eds.), The Development of Drosophila melanogaster (pp. 1131–1206). Cold Spring Harbor: Cold Spring Harbor Laboratory Press.

    Google Scholar 

  • Doe, C. Q., & Technau, G. M. (1993). Identification and cell lineage of individual neural precursors in the Drosophila CNS. Trends in Neurosciences, 16, 510–514.

    Article  CAS  PubMed  Google Scholar 

  • Dubois, L., & Vincent, A. (2001). The COE–Collier/Olf1/EBF–transcription factors: Structural conservation and diversity of developmental functions. Mechanisms of Development, 108, 3–12.

    Article  CAS  PubMed  Google Scholar 

  • Eade, K. T., & Allan, D. W. (2009). Neuronal phenotype in the mature nervous system is maintained by persistent retrograde bone morphogenetic protein signaling. Journal of Neuroscience, 29, 3852–3864.

    Article  CAS  PubMed  Google Scholar 

  • Eade, K. T., Fancher, H. A., Ridyard, M. S., & Allan, D. W. (2012). Developmental transcriptional networks are required to maintain neuronal subtype identity in the mature nervous system. PLoS Genetics, 8, e1002501.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Egger, B., Chell, J. M., & Brand, A. H. (2008). Insights into neural stem cell biology from flies. Philosophical Transactions of the Royal Society of London, 363, 39–56.

    Article  CAS  PubMed  Google Scholar 

  • Estacio-Gomez, A., Moris-Sanz, M., Schafer, A. K., Perea, D., Herrero, P., & Diaz-Benjumea, F. J. (2013). Bithorax-complex genes sculpt the pattern of leucokinergic neurons in the Drosophila central nervous system. Development (Cambridge, England), 140, 2139–2148.

    Google Scholar 

  • Ewer, J. (2005). Behavioral actions of neuropeptides in invertebrates: Insights from Drosophila. Hormones and Behavior, 48, 418–429.

    Article  CAS  PubMed  Google Scholar 

  • Formosa-Jordan, P., Ibanes, M., Ares, S., & Frade, J. M. (2013). Lateral inhibition and neurogenesis: Novel aspects in motion. The International journal of developmental Biology, 57, 341–350.

    Article  CAS  PubMed  Google Scholar 

  • Gabilondo, H., Losada-Perez, M., del Saz, D., Molina, I., Leon, Y., Canal, I., et al. (2011). A targeted genetic screen identifies crucial players in the specification of the Drosophila abdominal capaergic neurons. Mechanisms of Development, 128, 208–221.

    Article  CAS  PubMed  Google Scholar 

  • Garces, A., and Thor, S. (2006). Specification of Drosophila aCC motoneuron identity by a genetic cascade involving even-skipped, grain and zfh1. Development (Cambridge, England), 133, 1445–1455.

    Google Scholar 

  • Gaspard, N., Bouschet, T., Hourez, R., Dimidschstein, J., Naeije, G., van den Ameele, J., et al. (2008). An intrinsic mechanism of corticogenesis from embryonic stem cells. Nature, 455, 351–357.

    Article  CAS  PubMed  Google Scholar 

  • Gehring, W. J., Kloter, U., & Suga, H. (2009). Evolution of the Hox gene complex from an evolutionary ground state. Current Topics in Developmental Biology, 88, 35–61.

    Article  CAS  PubMed  Google Scholar 

  • Grosskortenhaus, R., Pearson, B. J., Marusich, A., & Doe, C. Q. (2005). Regulation of temporal identity transitions in Drosophila neuroblasts. Developmental Cell, 8, 193–202.

    Article  CAS  PubMed  Google Scholar 

  • Grosskortenhaus, R., Robinson, K. J., & Doe, C. Q. (2006). Pdm and Castor specify late-born motor neuron identity in the NB7-1 lineage. Genes & Development, 20, 2618–2627.

    Article  CAS  Google Scholar 

  • Hamanaka, Y., Park, D., Yin, P., Annangudi, S. P., Edwards, T. N., Sweedler, J., et al. (2010). Transcriptional orchestration of the regulated secretory pathway in neurons by the bHLH protein DIMM. Current Biology, 20, 9–18.

    Article  CAS  PubMed  Google Scholar 

  • Hayes, T. K., Pannabecker, T. L., Hinckley, D. J., Holman, G. M., Nachman, R. J., Petzel, D. H., et al. (1989). Leucokinins, a new family of ion transport stimulators and inhibitors in insect malpighian tubules. Life Sciences, 44, 1259–1266.

    Article  CAS  PubMed  Google Scholar 

  • Herrero, P., Magarinos, M., Molina, I., Benito, J., Dorado, B., Turiegano, E., et al. (2007). Squeeze involvement in the specification of Drosophila leucokinergic neurons: Different regulatory mechanisms endow the same neuropeptide selection. Mechanisms of Development, 124, 427–440.

    Article  CAS  PubMed  Google Scholar 

  • Hewes, R. S., Park, D., Gauthier, S. A., Schaefer, A. M., & Taghert, P. H. (2003). The bHLH protein dimmed controls neuroendocrine cell differentiation in Drosophila. Development (Cambridge, England), 130, 1771–1781.

    Google Scholar 

  • Hewes, R. S., & Taghert, P. H. (2001). Neuropeptides and neuropeptide receptors in the Drosophila melanogaster genome. Genome Research, 11, 1126–1142.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Higashijima, S., Shishido, E., Matsuzaki, M., & Saigo, K. (1996). Eagle, a member of the steroid receptor gene superfamily, is expressed in a subset of neuroblasts and regulates the fate of their putative progeny in the Drosophila CNS. Development (Cambridge, England), 122, 527–536.

    Google Scholar 

  • Hippenmeyer, S., Kramer, I., & Arber, S. (2004). Control of neuronal phenotype: What targets tell the cell bodies. Trends in Neurosciences, 27, 482–488.

    Article  CAS  PubMed  Google Scholar 

  • Hirth, F., Hartmann, B., & Reichert, H. (1998). Homeotic gene action in embryonic brain development of Drosophila. Development (Cambridge, England), 125, 1579–1589.

    Google Scholar 

  • Hirth, F., Therianos, S., Loop, T., Gehring, W. J., Reichert, H., & Furukubo-Tokunaga, K. (1995). Developmental defects in brain segmentation caused by mutations of the homeobox genes orthodenticle and empty spiracles in Drosophila. Neuron, 15, 769–778.

    Article  CAS  PubMed  Google Scholar 

  • Hobert, O. (2008). Regulatory logic of neuronal diversity: Terminal selector genes and selector motifs. Proceedings of the National Academy of Sciences of the United States of America, 105, 20067–20071.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hobert, O., Carrera, I., & Stefanakis, N. (2010). The molecular and gene regulatory signature of a neuron. Trends in Neurosciences, 33, 435–445.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Honegger, H. W., Dewey, E. M., & Ewer, J. (2008). Bursicon, the tanning hormone of insects: Recent advances following the discovery of its molecular identity. Journal of Comparative Physiology A, Neuroethology, Sensory, Neural, and Behavioral Physiology, 194, 989–1005.

    Article  CAS  PubMed  Google Scholar 

  • Isshiki, T., Pearson, B., Holbrook, S., & Doe, C. Q. (2001). Drosophila neuroblasts sequentially express transcription factors which specify the temporal identity of their neuronal progeny. Cell, 106, 511–521.

    Article  CAS  PubMed  Google Scholar 

  • Jacob, J., Maurange, C., & Gould, A. P. (2008). Temporal control of neuronal diversity: Common regulatory principles in insects and vertebrates? Development (Cambridge, England), 135, 3481–3489.

    Google Scholar 

  • Kambadur, R., Koizumi, K., Stivers, C., Nagle, J., Poole, S. J., & Odenwald, W. F. (1998). Regulation of POU genes by castor and hunchback establishes layered compartments in the Drosophila CNS. Genes & Development, 12, 246–260.

    Article  CAS  Google Scholar 

  • Kanai, M. I., Okabe, M., & Hiromi, Y. (2005). Seven-up controls switching of transcription factors that specify temporal identities of Drosophila neuroblasts. Developmental Cell, 8, 203–213.

    Article  CAS  PubMed  Google Scholar 

  • Karcavich, R., & Doe, C. Q. (2005). Drosophila neuroblast 7-3 cell lineage: A model system for studying programmed cell death, notch/numb signaling, and sequential specification of ganglion mother cell identity. The Journal of Comparative Neurology, 481, 240–251.

    Article  PubMed  Google Scholar 

  • Karlsson, D., Baumgardt, M., & Thor, S. (2010). Segment-specific neuronal subtype specification by the integration of anteroposterior and temporal cues. PLoS Biology, 8, e1000368.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kean, L., Cazenave, W., Costes, L., Broderick, K. E., Graham, S., Pollock, V. P., et al. (2002). Two nitridergic peptides are encoded by the gene capability in Drosophila melanogaster. American Journal of Physiology, 282, R1297–R1307.

    CAS  PubMed  Google Scholar 

  • Kearney, J. B., Wheeler, S. R., Estes, P., Parente, B., & Crews, S. T. (2004). Gene expression profiling of the developing Drosophila CNS midline cells. Developmental Biology, 275, 473–492.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim, N. C., & Marques, G. (2010). Identification of downstream targets of the bone morphogenetic protein pathway in the Drosophila nervous system. Developmental Dynamics, 239, 2413–2425.

    Article  CAS  PubMed  Google Scholar 

  • Kim, Y. J., Spalovska-Valachova, I., Cho, K. H., Zitnanova, I., Park, Y., Adams, M. E., et al. (2004). Corazonin receptor signaling in ecdysis initiation. Proceedings of the National Academy of Sciences of the United States of America, 101, 6704–6709.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klose, M. K., Dason, J. S., Atwood, H. L., Boulianne, G. L., & Mercier, A. J. (2010). Peptide-induced modulation of synaptic transmission and escape response in Drosophila requires two G-protein-coupled receptors. Journal of Neuroscience, 30, 14724–14734.

    Article  CAS  PubMed  Google Scholar 

  • Knoblich, J. A. (2010). Asymmetric cell division: Recent developments and their implications for tumour biology. Nature Reviews, 11, 849–860.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kohwi, M., & Doe, C. Q. (2013). Temporal fate specification and neural progenitor competence during development. Nature Reviews Neuroscience, 14, 823–838.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kohwi, M., Hiebert, L. S., & Doe, C. Q. (2011). The pipsqueak-domain proteins distal antenna and distal antenna-related restrict Hunchback neuroblast expression and early-born neuronal identity. Development (Cambridge, England), 138, 1727–1735.

    Google Scholar 

  • Lahr, E. C., Dean, D., & Ewer, J. (2012). Genetic analysis of ecdysis behavior in Drosophila reveals partially overlapping functions of two unrelated neuropeptides. Journal of Neuroscience, 32, 6819–6829.

    Article  CAS  PubMed  Google Scholar 

  • Lawrence, P. A., Sanson, B., & Vincent, J. P. (1996). Compartments, wingless and engrailed: Patterning the ventral epidermis of Drosophila embryos. Development (Cambridge, England), 122, 4095–4103.

    Google Scholar 

  • Lee, G., Kim, K. M., Kikuno, K., Wang, Z., Choi, Y. J., & Park, J. H. (2008). Developmental regulation and functions of the expression of the neuropeptide corazonin in Drosophila melanogaster. Cell and Tissue Research, 331, 659–673.

    Article  CAS  PubMed  Google Scholar 

  • Lee, G., Wang, Z., Sehgal, R., Chen, C. H., Kikuno, K., Hay, B., & Park, J. H. (2011). Drosophila caspases involved in developmentally regulated programmed cell death of peptidergic neurons during early metamorphosis. The Journal of Comparative Neurology, 519, 34–48.

    Article  CAS  PubMed  Google Scholar 

  • Losada-Perez, M., Gabilondo, H., del Saz, D., Baumgardt, M., Molina, I., Leon, Y., et al. (2010). Lineage-unrelated neurons generated in different temporal windows and expressing different combinatorial codes can converge in the activation of the same terminal differentiation gene. Mechanisms of Development, 127, 458–471.

    Article  CAS  PubMed  Google Scholar 

  • Lundell, M. J., Lee, H. K., Perez, E., & Chadwell, L. (2003). The regulation of apoptosis by Numb/Notch signaling in the serotonin lineage of Drosophila. Development (Cambridge, England), 130, 4109–4121.

    Google Scholar 

  • Lundgren, S. E., Callahan, C. A., Thor, S., & Thomas, J. B. (1995). Control of neuronal pathway selection by the Drosophila LIM homeodomain gene apterous. Development (Cambridge, England), 121, 1769–1773.

    Google Scholar 

  • Maeda, R. K., & Karch, F. (2006). The ABC of the BX-C: The bithorax complex explained. Development (Cambridge, England), 133, 1413–1422.

    Google Scholar 

  • Mangan, S., & Alon, U. (2003). Structure and function of the feed-forward loop network motif. Proceedings of the National Academy of Sciences of the United States of America, 100, 11980–11985.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mangan, S., Zaslaver, A., & Alon, U. (2003). The coherent feedforward loop serves as a sign-sensitive delay element in transcription networks. Journal of Molecular Biology, 334, 197–204.

    Article  CAS  PubMed  Google Scholar 

  • Mann, R. S., & Affolter, M. (1998). Hox proteins meet more partners. Current Opinion in Genetics & Development, 8, 423–429.

    Article  CAS  Google Scholar 

  • Marques, G., Bao, H., Haerry, T. E., Shimell, M. J., Duchek, P., Zhang, B., & O’Connor, M. B. (2002). The Drosophila BMP type II receptor wishful thinking regulates neuromuscular synapse morphology and function. Neuron, 33, 529–543.

    Article  CAS  PubMed  Google Scholar 

  • Marques, G., Haerry, T. E., Crotty, M. L., Xue, M., Zhang, B., & O’Connor, M. B. (2003). Retrograde Gbb signaling through the Bmp type 2 receptor wishful thinking regulates systemic FMRFa expression in Drosophila. Development (Cambridge, England), 130, 5457–5470.

    Google Scholar 

  • Maurange, C., Cheng, L., & Gould, A. P. (2008). Temporal transcription factors and their targets schedule the end of neural proliferation in Drosophila. Cell, 133, 891–902.

    Article  CAS  PubMed  Google Scholar 

  • Maurange, C., & Gould, A. P. (2005). Brainy but not too brainy: Starting and stopping neuroblast divisions in Drosophila. Trends in Neurosciences, 28, 30–36.

    Article  CAS  PubMed  Google Scholar 

  • McCabe, B. D., Marques, G., Haghighi, A. P., Fetter, R. D., Crotty, M. L., Haerry, T. E., et al. (2003). The BMP homolog Gbb provides a retrograde signal that regulates synaptic growth at the Drosophila neuromuscular junction. Neuron, 39, 241–254.

    Article  CAS  PubMed  Google Scholar 

  • McClure, K. D., & Heberlein, U. (2013). A small group of neurosecretory cells expressing the transcriptional regulator apontic and the neuropeptide corazonin mediate ethanol sedation in Drosophila. Journal of Neuroscience, 33, 4044–4054.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McDonald, J. A., Holbrook, S., Isshiki, T., Weiss, J., Doe, C. Q., & Mellerick, D. M. (1998). Dorsoventral patterning in the Drosophila central nervous system: The vnd homeobox gene specifies ventral column identity. Genes & Development, 12, 3603–3612.

    Article  CAS  Google Scholar 

  • McGuire, S. E., Mao, Z., & Davis, R. L. (2004). Spatiotemporal gene expression targeting with the TARGET and gene-switch systems in Drosophila. Science’s STKE: Signal Transduction Knowledge Environment, 2004, pl6.

    Google Scholar 

  • Merabet, S., Pradel, J., & Graba, Y. (2005). Getting a molecular grasp on Hox contextual activity. Trends in Genetics, 21, 477–480.

    Article  CAS  PubMed  Google Scholar 

  • Mettler, U., Vogler, G., & Urban, J. (2006). Timing of identity: Spatiotemporal regulation of hunchback in neuroblast lineages of Drosophila by seven-up and prospero. Development (Cambridge, England), 133, 429–437.

    Google Scholar 

  • Miguel-Aliaga, I., Allan, D. W., & Thor, S. (2004). Independent roles of the dachshund and eyes absent genes in BMP signaling, axon pathfinding and neuronal specification. Development (Cambridge, England), 131, 5837–5848.

    Google Scholar 

  • Miguel-Aliaga, I., & Thor, S. (2004). Segment-specific prevention of pioneer neuron apoptosis by cell-autonomous, postmitotic Hox gene activity. Development (Cambridge, England), 131, 6093–6105.

    Google Scholar 

  • Miguel-Aliaga, I., & Thor, S. (2009). Programmed cell death in the nervous system–a programmed cell fate? Current Opinion in Neurobiology, 19, 127–133.

    Google Scholar 

  • Miguel-Aliaga, I., Thor, S., & Gould, A. P. (2008). Postmitotic specification of Drosophila insulinergic neurons from pioneer neurons. PLoS Biology, 6, e58.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Milakovic, M., Ormerod, K. G., Klose, M. K., & Mercier, A. J. (2014). Mode of action of a Drosophila FMRFamide in inducing muscle contraction. The Journal of experimental biology, 217, 1725–1736.

    Article  CAS  PubMed  Google Scholar 

  • Mills, J. C., & Taghert, P. H. (2012). Scaling factors: Transcription factors regulating subcellular domains. BioEssays, 34, 10–16.

    Article  CAS  PubMed  Google Scholar 

  • Nassel, D. R., & Winther, A. M. (2010). Drosophila neuropeptides in regulation of physiology and behavior. Progress in Neurobiology, 92, 42–104.

    Article  PubMed  CAS  Google Scholar 

  • Neumuller, R. A., & Knoblich, J. A. (2009). Dividing cellular asymmetry: Asymmetric cell division and its implications for stem cells and cancer. Genes & Development, 23, 2675–2699.

    Article  CAS  Google Scholar 

  • Novotny, T., Eiselt, R., & Urban, J. (2002). Hunchback is required for the specification of the early sublineage of neuroblast 7-3 in the Drosophila central nervous system. Development (Cambridge, England), 129, 1027–1036.

    Google Scholar 

  • Nusslein-Volhard, C., & Wieschaus, E. (1980). Mutations affecting segment number and polarity in Drosophila. Nature, 287, 795–801.

    Article  CAS  PubMed  Google Scholar 

  • O’Brien, M. A., & Taghert, P. H. (1998). A peritracheal neuropeptide system in insects: Release of myomodulin-like peptides at ecdysis. The Journal of experimental biology, 201(Pt 2), 193–209.

    PubMed  Google Scholar 

  • Okano, H., & Temple, S. (2009). Cell types to order: Temporal specification of CNS stem cells. Current Opinion in Neurobiology, 19, 112–119.

    Article  CAS  PubMed  Google Scholar 

  • Park, J. H., Schroeder, A. J., Helfrich-Forster, C., Jackson, F. R., & Ewer, J. (2003). Targeted ablation of CCAP neuropeptide-containing neurons of Drosophila causes specific defects in execution and circadian timing of ecdysis behavior. Development (Cambridge, England), 130, 2645–2656.

    Google Scholar 

  • Park, D., & Taghert, P. H. (2009). Peptidergic neurosecretory cells in insects: Organization and control by the bHLH protein DIMMED. General and Comparative Endocrinology, 162, 2–7.

    Article  CAS  PubMed  Google Scholar 

  • Park, D., Veenstra, J. A., Park, J. H., & Taghert, P. H. (2008). Mapping peptidergic cells in Drosophila: Where DIMM fits in. PLoS One, 3, e1896.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pearson, B. J., & Doe, C. Q. (2003). Regulation of neuroblast competence in Drosophila. Nature, 425, 624–628.

    Article  CAS  PubMed  Google Scholar 

  • Pearson, B. J., & Doe, C. Q. (2004). Specification of temporal identity in the developing nervous system. Annual Review of Cell and Developmental Biology, 20, 619–647.

    Article  CAS  PubMed  Google Scholar 

  • Peterson, C., Carney, G. E., Taylor, B. J., & White, K. (2002). Reaper is required for neuroblast apoptosis during Drosophila development. Development (Cambridge, England), 129, 1467–1476.

    Google Scholar 

  • Price, D. A., & Greenberg, M. J. (1977a). Purification and characterization of a cardioexcitatory neuropeptide from the central ganglia of a bivalve mollusc. Preparative biochemistry, 7, 261–281.

    Article  CAS  PubMed  Google Scholar 

  • Price, D. A., & Greenberg, M. J. (1977b). Structure of a molluscan cardioexcitatory neuropeptide. Science (New York, NY), 197, 670–671.

    Article  CAS  Google Scholar 

  • Prokop, A. (2006). Organization of the efferent system and structure of neuromuscular junctions in Drosophila. International Review of Neurobiology, 75, 71–90.

    Article  CAS  PubMed  Google Scholar 

  • Prokop, A., Bray, S., Harrison, E., & Technau, G. M. (1998). Homeotic regulation of segment-specific differences in neuroblast numbers and proliferation in the Drosophila central nervous system. Mechanisms of Development, 74, 99–110.

    Article  CAS  PubMed  Google Scholar 

  • Prokop, A., & Technau, G. M. (1994). Early tagma-specific commitment of Drosophila CNS progenitor NB1-1. Development (Cambridge, England), 120, 2567–2578.

    Google Scholar 

  • Rogulja-Ortmann, A., Luer, K., Seibert, J., Rickert, C., & Technau, G. M. (2007). Programmed cell death in the embryonic central nervous system of Drosophila melanogaster. Development (Cambridge, England), 134, 105–116.

    Google Scholar 

  • Rogulja-Ortmann, A., Picao-Osorio, J., Villava, C., Patraquim, P., Lafuente, E., Aspden, J., Thomsen, S., Technau, G. M., & Alonso, C. R. (2014). The RNA-binding protein ELAV regulates Hox RNA processing, expression and function within the Drosophila nervous system. Development (Cambridge, England), 141, 2046–2056.

    Google Scholar 

  • Rogulja-Ortmann, A., Renner, S., & Technau, G. M. (2008). Antagonistic roles for Ultrabithorax and Antennapedia in regulating segment-specific apoptosis of differentiated motoneurons in the Drosophila embryonic central nervous system. Development (Cambridge, England), 135, 3435–3445.

    Google Scholar 

  • Roth, K. A., & D’Sa, C. (2001). Apoptosis and brain development. Mental retardation and developmental disabilities research reviews, 7, 261–266.

    Article  CAS  PubMed  Google Scholar 

  • Santos, J. G., Pollak, E., Rexer, K. H., Molnar, L., & Wegener, C. (2006). Morphology and metamorphosis of the peptidergic Va neurons and the median nerve system of the fruit fly, Drosophila melanogaster. Cell and Tissue Research, 326, 187–199.

    Article  CAS  PubMed  Google Scholar 

  • Schmid, A., Chiba, A., & Doe, C. Q. (1999). Clonal analysis of Drosophila embryonic neuroblasts: Neural cell types, axon projections and muscle targets. Development (Cambridge, England), 126, 4653–4689.

    Google Scholar 

  • Schmidt, H., Rickert, C., Bossing, T., Vef, O., Urban, J., & Technau, G. M. (1997). The embryonic central nervous system lineages of Drosophila melanogaster. II. Neuroblast lineages derived from the dorsal part of the neuroectoderm. Developmental Biology, 189, 186–204.

    Article  CAS  PubMed  Google Scholar 

  • Schneider, L. E., Roberts, M. S., & Taghert, P. H. (1993a). Cell type-specific transcriptional regulation of the Drosophila FMRFamide neuropeptide gene. Neuron, 10, 279–291.

    Article  CAS  PubMed  Google Scholar 

  • Schneider, L. E., Sun, E. T., Garland, D. J., & Taghert, P. H. (1993b). An immunocytochemical study of the FMRFamide neuropeptide gene products in Drosophila. The Journal of Comparative Neurology, 337, 446–460.

    Article  CAS  PubMed  Google Scholar 

  • Schneider, L. E., & Taghert, P. H. (1990). Organization and expression of the Drosophila Phe-Met-Arg-Phe-NH2 neuropeptide gene. The Journal of biological chemistry, 265, 6890–6895.

    CAS  PubMed  Google Scholar 

  • Schotzinger, R. J., & Landis, S. C. (1988). Cholinergic phenotype developed by noradrenergic sympathetic neurons after innervation of a novel cholinergic target in vivo. Nature, 335, 637–639.

    Article  CAS  PubMed  Google Scholar 

  • Schubiger, M., Tomita, S., Sung, C., Robinow, S., & Truman, J. W. (2003). Isoform specific control of gene activity in vivo by the Drosophila ecdysone receptor. Mechanisms of Development, 120, 909–918.

    Article  CAS  PubMed  Google Scholar 

  • Schubiger, M., Wade, A. A., Carney, G. E., Truman, J. W., & Bender, M. (1998). Drosophila EcR-B ecdysone receptor isoforms are required for larval molting and for neuron remodeling during metamorphosis. Development (Cambridge, England), 125, 2053–2062.

    Google Scholar 

  • Sha, K., Choi, S. H., Im, J., Lee, G. G., Loeffler, F., & Park, J. H. (2014). Regulation of ethanol-related behavior and ethanol metabolism by the corazonin neurons and corazonin receptor in Drosophila melanogaster. PLoS ONE, 9, e87062.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shafer, O. T., Helfrich-Forster, C., Renn, S. C., & Taghert, P. H. (2006). Reevaluation of Drosophila melanogaster’s neuronal circadian pacemakers reveals new neuronal classes. The Journal of Comparative Neurology, 498, 180–193.

    Article  PubMed  PubMed Central  Google Scholar 

  • Skeath, J. B. (1999). At the nexus between pattern formation and cell-type specification: The generation of individual neuroblast fates in the Drosophila embryonic central nervous system. BioEssays, 21, 922–931.

    Article  CAS  PubMed  Google Scholar 

  • Skeath, J. B., & Doe, C. Q. (1998). Sanpodo and Notch act in opposition to Numb to distinguish sibling neuron fates in the Drosophila CNS. Development (Cambridge, England), 125, 1857–1865.

    Google Scholar 

  • Skeath, J. B., & Thor, S. (2003). Genetic control of Drosophila nerve cord development. Current Opinion in Neurobiology, 13, 8–15.

    Article  CAS  PubMed  Google Scholar 

  • Smith, R. B., Machamer, J. B., Kim, N. C., Hays, T. S., & Marques, G. (2012). Relay of retrograde synaptogenic signals through axonal transport of BMP receptors. Journal of Cell Science, 125, 3752–3764.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sousa-Nunes, R., Cheng, L. Y., & Gould, A. P. (2010). Regulating neural proliferation in the Drosophila CNS. Current Opinion in Neurobiology, 20, 50–57.

    Article  CAS  PubMed  Google Scholar 

  • Southall, T. D., Egger, B., Gold, K. S., & Brand, A. H. (2008). Regulation of self-renewal and differentiation in the Drosophila nervous system. Cold Spring Harbor Symposia on Quantitative Biology, 73, 523–528.

    Article  CAS  PubMed  Google Scholar 

  • Spana, E. P., & Doe, C. Q. (1996). Numb antagonizes notch signaling to specify sibling neuron cell fates. Neuron, 17, 21–26.

    Article  CAS  PubMed  Google Scholar 

  • Spana, E. P., Kopczynski, C., Goodman, C. S., & Doe, C. Q. (1995). Asymmetric localization of numb autonomously determines sibling neuron identity in the Drosophila CNS. Development (Cambridge, England), 121, 3489–3494.

    Google Scholar 

  • Sulston, J. E., & Horvitz, H. R. (1977). Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Developmental Biology, 56, 110–156.

    Article  CAS  PubMed  Google Scholar 

  • Sulston, J. E., Schierenberg, E., White, J. G., & Thomson, J. N. (1983). The embryonic cell lineage of the nematode Caenorhabditis elegans. Developmental Biology, 100, 64–119.

    Article  CAS  PubMed  Google Scholar 

  • Suska, A., Miguel-Aliaga, I., & Thor, S. (2011). Segment-specific generation of Drosophila capability neuropeptide neurons by multi-faceted Hox cues. Developmental Biology, 353, 72–80.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taghert, P. H., & Nitabach, M. N. (2012). Peptide neuromodulation in invertebrate model systems. Neuron, 76, 82–97.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tayler, T. D., Pacheco, D. A., Hergarden, A. C., Murthy, M., & Anderson, D. J. (2012). A neuropeptide circuit that coordinates sperm transfer and copulation duration in Drosophila. Proceedings of the National Academy of Sciences of the United States of America, 109, 20697–20702.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Terhzaz, S., O’Connell, F. C., Pollock, V. P., Kean, L., Davies, S. A., Veenstra, J. A., et al. (1999). Isolation and characterization of a leucokinin-like peptide of Drosophila melanogaster. The Journal of experimental biology, 202(Pt 24), 3667–3676.

    CAS  PubMed  Google Scholar 

  • Terriente Felix, J., Magarinos, M., & Diaz-Benjumea, F. J. (2007). Nab controls the activity of the zinc-finger transcription factors squeeze and rotund in Drosophila development. Development (Cambridge, England), 134, 1845–1852.

    Google Scholar 

  • Therianos, S., Leuzinger, S., Hirth, F., Goodman, C. S., & Reichert, H. (1995). Embryonic development of the Drosophila brain: Formation of commissural and descending pathways. Development (Cambridge, England), 121, 3849–3860.

    Google Scholar 

  • Thor, S. (1995). The genetics of brain-development—conserved programs in flies and mice. Neuron, 15, 975–977.

    Article  CAS  PubMed  Google Scholar 

  • Tissot, M., & Stocker, R. F. (2000). Metamorphosis in Drosophila and other insects: The fate of neurons throughout the stages. Progress in Neurobiology, 62, 89–111.

    Article  CAS  PubMed  Google Scholar 

  • Tran, K. D., & Doe, C. Q. (2008). Pdm and castor close successive temporal identity windows in the NB3-1 lineage. Development (Cambridge, England), 135, 3491-3499.

    Google Scholar 

  • Tsuji, T., Hasegawa, E., & Isshiki, T. (2008). Neuroblast entry into quiescence is regulated intrinsically by the combined action of spatial Hox proteins and temporal identity factors. Development (Cambridge, England), 135, 3859–3869.

    Google Scholar 

  • Udolph, G., Luer, K., Bossing, T., & Technau, G. M. (1995). Commitment of CNS progenitors along the dorsoventral axis of Drosophila neuroectoderm. Science (New York, NY), 269, 1278–1281.

    Article  CAS  Google Scholar 

  • Ulvklo, C., Macdonald, R., Bivik, C., Baumgardt, M., Karlsson, D., & Thor, S. (2012). Control of neuronal cell fate and number by integration of distinct daughter cell proliferation modes with temporal progression. Development (Cambridge, England), 139, 678–689.

    Google Scholar 

  • Urbach, R., Schnabel, R., & Technau, G. M. (2003). The pattern of neuroblast formation, mitotic domains and proneural gene expression during early brain development in Drosophila. Development (Cambridge, England), 130, 3589–3606.

    Google Scholar 

  • Urbach, R., & Technau, G. M. (2003a). Early steps in building the insect brain: Neuroblast formation and segmental patterning in the developing brain of different insect species. Arthropod structure & development, 32, 103–123.

    Google Scholar 

  • Urbach, R., & Technau, G. M. (2003b). Molecular markers for identified neuroblasts in the developing brain of Drosophila. Development (Cambridge, England), 130, 3621–3637.

    Google Scholar 

  • Urbach, R., & Technau, G. M. (2003c). Segment polarity and DV patterning gene expression reveals segmental organization of the Drosophila brain. Development (Cambridge, England), 130, 3607–3620.

    Google Scholar 

  • Urbach, R., & Technau, G. M. (2004). Neuroblast formation and patterning during early brain development in Drosophila. BioEssays, 26, 739–751.

    Article  CAS  PubMed  Google Scholar 

  • Veenstra, J. A. (1989). Isolation and structure of corazonin, a cardioactive peptide from the American cockroach. FEBS Letters, 250, 231–234.

    Article  CAS  PubMed  Google Scholar 

  • Veenstra, J. A. (1994). Isolation and structure of the Drosophila corazonin gene. Biochemical and biophysical research communications, 204, 292–296.

    Article  CAS  PubMed  Google Scholar 

  • Veenstra, J.A. (2009). Does corazonin signal nutritional stress in insects? Insect Biochemistry and Molecular Biology, 39, 755–762.

    Google Scholar 

  • Verleyen, P., Baggerman, G., Wiehart, U., Schoeters, E., Van Lommel, A., De Loof, A., & Schoofs, L. (2004). Expression of a novel neuropeptide, NVGTLARDFQLPIPNamide, in the larval and adult brain of Drosophila melanogaster. Journal of Neurochemistry, 88, 311–319.

    Article  CAS  PubMed  Google Scholar 

  • Veverytsa, L., & Allan, D. W. (2011). Retrograde BMP signaling controls Drosophila behavior through regulation of a peptide hormone battery. Development (Cambridge, England), 138, 3147–3157.

    Google Scholar 

  • Veverytsa, L., & Allan, D. W. (2012). Temporally tuned neuronal differentiation supports the functional remodeling of a neuronal network in Drosophila. Proceedings of the National Academy of Sciences of the United States of America, 109, E748–E756.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Veverytsa, L., & Allan, D. W. (2013). Subtype-specific neuronal remodeling during Drosophila metamorphosis. Fly, 7, 78–86.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • von Ohlen, T., & Doe, C. Q. (2000). Convergence of dorsal, dpp, and egfr signaling pathways subdivides the Drosophila neuroectoderm into three dorsal-ventral columns. Developmental Biology, 224, 362–372.

    Article  CAS  Google Scholar 

  • Wheeler, S. R., Kearney, J. B., Guardiola, A. R., & Crews, S. T. (2006). Single-cell mapping of neural and glial gene expression in the developing Drosophila CNS midline cells. Developmental Biology, 294, 509–524.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • White, B. H., & Ewer, J. (2014). Neural and hormonal control of postecdysial behaviors in insects. Annual Review of Entomology, 59, 363–381.

    Article  CAS  PubMed  Google Scholar 

  • Wu, P. S., Egger, B., & Brand, A. H. (2008). Asymmetric stem cell division: Lessons from Drosophila. Seminars in Cell & Developmental Biology, 19, 283–293.

    Article  CAS  Google Scholar 

  • Zhao, Y., Bretz, C. A., Hawksworth, S. A., Hirsh, J., & Johnson, E. C. (2010). Corazonin neurons function in sexually dimorphic circuitry that shape behavioral responses to stress in Drosophila. PLoS ONE, 5, e9141.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgments

We thank the Swedish Research Council, Knut and Alice Wallenberg Foundation, Swedish Cancer Foundation, and Swedish Royal Academy of Sciences for funding to ST, and the Canadian Institutes of Health Research and the National Sciences and Engineering Research Council of Canada for funding to DWA. We would like to thank Lyubov Veverytsa for assistance in generating figures.

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Thor, S., Allan, D.W. (2016). Advances in Understanding the Generation and Specification of Unique Neuronal Sub-types from Drosophila Neuropeptidergic Neurons. In: Castelli-Gair Hombría, J., Bovolenta, P. (eds) Organogenetic Gene Networks. Springer, Cham. https://doi.org/10.1007/978-3-319-42767-6_3

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