Summary
The adult optic lobes of the blowfly Calliphora erythrocephala were found to be innervated by more than 2000 neurons immunoreactive to antisera raised against the neuropeptides FMRFamide, its fragment RFamide, and gastrin/cholecystokinin (CCK). All of the CCK-like immunoreactive (CCK-IR) neurons also reacted with antisera to RFamide, FMRFamide and pancreatic polypeptide. A few RFamide/FMRFamide-like immunoreactive (RF-IR) neurons did not react with CCK antisera; they reacted instead with antisera to Leu-enkephalin and Met-enkephalin-Arg6-Phe7. The RF-IR neurons are, thus, heterogeneous with respect to their contents of immunoreactive peptides. Two of the RF-IR neuron types innervating the adult optic lobes could be traced in their entirety only after following their postembryonic development, because of the complexity of the trajectories of the immunoreactive neuronal process in the adult insect. The majority of the cell bodies of the RF-IR and CCK-IR neurons lie within the optic lobes and are derived from imaginal neuroblasts of the inner and outer optic anlagen. Six of the peptidergic neurons are, however, metamorphosing larval neurons with their cell bodies in the central part of the protocerebrum. The full extent of immunoreactivitiy is not attained in some of the neurons until the late pupal or early adult stage. The larval optic center was also found to be innervated by neurons immuno-reactive with both RFamide and CCK antisera. The cell bodies of these RF-IR/CCK-IR neurons are located near the developing lamina (one on each side). In the 24 h pupa, the cell bodies of these neurons are still immunoreactive, but thereafter they cannot be immunolabeled apparently due to cell death or a change in transmitter phenotype.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Campos-Ortega JA, Hartenstein V (1985) Development of the nervous system. In: Kerkut GA, Gilbert LI (eds) Comprehensive Insect Physiology, Biochemistry and Pharmacology. Pergamon Press, New York, Vol 5, pp 49–84
Cantera R, Nässel DR (1987) Postembryonic development of serotonin-immunoreactive neurons in the central nervous system of the blowfly. II. The ventral ganglia. Cell Tissue Res 250:449–459
Dockray GJ, Duve H, Thorpe A (1981) Immunochemical characterization of gastrin/cholecystokinin-like peptides in the brain of the blowfly Calliphora vomitoria. Gen Comp Endocrinol 45:491–496
Duve H, Thorpe A (1980) Localization of pancreatic polypeptide (PP)-like immunoreactive material in neurons of the brain of the blowfly, Calliphora erythrocephala (Diptera). Cell Tissue Res 210:101–109
Duve H, Thorpe A (1981) Gastrin/cholecystokinin (CCK)-like immunoreactive neurons in the brain of the blowfly Calliphora erythrocephala (Diptera). Gen Comp Endocrinol 43:381–391
Duve H, Thorpe A (1982) The distribution of pancreatic polypep-tide in the nervous system and gut of the blowfly Calliphora vomitoria (Diptera). Cell Tissue Res 227:67–77
Duve H, Thorpe A (1988) Mapping of enkephalin-related peptides in the nervous system of the blowfly Calliphora vomitoria and their co-localization with cholecystokinin (CCK.)- and pancreatic polypeptide (PP)-like peptides. Cell Tissue Res 251:399–415
Duve H, Thorpe A, Nässel DR (1988) Light- and electron microscopic immunocytochemistry of peptidergic neurons innervating thoracico-abdominal neurohaemal areas in the blowfly. Cell Tissue Res 253:583–595
Duve H, Thorpe A, Rehfeld JF (1985) Localization and characterization of cholecystokinin (CCK)-like peptides in the brain of the blowfly Calliphora vomitoria. In: Kobayashi H, Bern H, Urano A (eds) Neurosecretion and the Biology of Neuropep- tides. Japan Sci Soc Press, Tokyo/Springer, Berlin Heidelberg New York, pp 401–409
Duve H, Thorpe A, Scott A (1986) Localization of opiod-like peptides in the nervous system of the blowfly Calliphora vomitoria. In: Stefano GB (ed) Handbook of comparative opioid and related neuropeptide mechanisms. CRC Press Inc., Boca Raton, Florida, pp 197–211
Duve H, Thorpe A, Lazarus NR, Lowry PJ (1982) A neuropeptide in the blowfly Calliphora erythrocephala with an amino acid composition homologous with vertebrate pancreatic polypeptide. Biochem J 201:429–432
Ebbebrink RHM, Price DA, Loenhout H van, Boble KE, Riehm JP, Geraerts WPM, Greenberg MJ (1987) The brain of Lymnea contains a family of FMRFamide like peptides. Peptides 8:515–522
Grimmelikhuijzen CJP (1983) FMRFamide is generally occurring in the nervous system of coelenterates. Histochemistry 78:361–381
Grimmelikhuijzen CJP (1985) Antisera to the sequence Arg-Pheamide visualize neuronal centralization in hydroid polyps. Cell Tissue Res 241:171–182
Hofbauer A (1979) Die Entwicklung der optischen Ganglien bei Drosophila melanogaster. Inaugural-Dissertation, University of Freiburg
Hofbauer A, Campos-Ortega JA (1988) Proliferation pattern and early differentiation of the optic lobes in Drosophila melanogaster. W Roux's Arch Dev Biol (in press)
Holman GM, Cook BJ, Nachman RJ (1986) Isolation, primary structure and synthesis of leucomyosuppressin, an insect neuropeptide that inhibits spontaneous contractions of the cockroach hindgut. Comp Biochem Physiol 85C: 329–333
Keshishian H, O'Shea M (1985) The acquisition and expression of peptidergic phenotype in the grasshopper embryo. J Neurosci 5:1005–1015
Larsson LI, Rehfeld JF (1979) Localization and molecular heterogeneity of cholecystokinin in the central and peripheral nervous system. Brain Res 165:201–218
Levine RB, Truman JB (1982) Metamorphosis of the insect nervous system: Changes in morphology and synaptic interaction of identified neurons. Nature 229:250–252
Meinertzhagen IA (1973) Development of compound eye and optic lobe of insects. In: Young D (ed) Developmental Neurobiology of Arthropods. Cambridge University Press, London, pp 51–104
Meyer EP, Matute C, Streit P, Nässel DR (1986) Insect optic lobe neuron identifiable with monoclonal antibodies to GABA. Histochemistry 84:207–216
Myers CM, Evans PD (1985) The distribution of bovine pancreatic polypeptide/FMRFamide-like immunoreactivity in the ventral nervous system of the locust. J Comp Neurol 243:1–16
Myers CM, Evans PD (1987) An FMRFamide antiserum differentiates between populations of antigens in the brain and retrocerebral complex of the locust, Schistocerca gregaria. Cell Tissue Res 250:93–99
Nachman RJ, Holman GM, Cook BJ, Haddon WF, Ling N (1986a) Leucosulfakinin-II a blocked sulfated insect neuropeptide with homology to cholecystokinin and gastrin. Biochem Biophys Res Comm 140:357–364
Nachman RJ, Holman GM, Haddon WF, Ling N (1986b) Leucosulfakinin, a sulfated insect neuropeptide with homology to gastrin and cholecystokinin. Science 234:71–73
Nambu JR, Andrews PC, Feistner GJ, Scheller RH (1987) Purification and characterization of the FMRFamide related peptide of Drosophila melanogaster. Soc Neurosci [Abstr] 13:1256
Nässel DR (1987) Neuroactive substances in the insect CNS. In: Ali MA (ed) Nervous Systems of Invertebrates. Plenum Press, New York, pp 171–212
Nässel DR, Elekes K (1984) Ultrastructural demonstration ofserotonin-immunoreactivity in the nervous system of an insect (Calliphora erythrocephala). Neurosci Lett 48:203–210
Nässel DR, O'Shea M (1987) Proctolin-like immunoreactive neurons in the blowfly central nervous system. J Comp Neurol 265:437–454
Nässel DR, Ohlsson LG, Sivasubramanian P (1987) Postembryonic differentiation of serotonin-immunoreactive neurons in flesh fly optic lobes developing in situ or cultured in vivo without eye discs. J Comp Neurol 255:327–340
Nässel DR, Elekes K, Johansson KUI (1988a) Dopamine-immunoreactive neurons in the blowfly visual system: light and electron microscopic immunocytochemistry. J Chem Neuroanat (in press)
Nässel DR, Ohlsson LG, Cantera R (1988b) Metamorphosis of identified neurons innervating thoracic neurohaemal organs in the blowfly: Transformation of cholecystokinin-like immunore- active neurons. J Comp Neurol 267:343–356
Nässel DR, Ohlsson LG, Johansson KUI, Grimmelikhuijzen CJP (1988c) Light and electron microscopic immunocytochemistry of neurons in the blowfly optic lobe reacting with antisera to RFamide and FMRFamide. Neuroscience 27:347–362
Nässel DR, Holmqvist MH, Hardie RC, Håkanson R, Sundler F (1988d) Histamine-like immunoreactivity in photoreceptors of the compound eyes and ocelli of the flies Calliphora erythrocephala and Musca domestica. Cell Tissue Res 253:639–646
Nordlander RH, Edwards JS (1969) Postembryonic brain development in the monarch butterfly, Danaus plexippus plexippus, I Cellular events during brain morphogenesis. Roux's Arch 162:197–217
Ohlsson LG, Nässel DR (1987) Postembryonic development of serotonin-immunoreactive neurons in the central nervous system of the blowfly. I. The optic lobes. Cell Tissue Res 249:669–679
Price DA, Greenberg MJ (1977) Structure of a molluscan cardioex- citatory neuropetide. Science 197:670–671
Rossier J, Audigier Y, Ling N, Cros J, Udenfriend S (1980) Metenkephalin Arg6-Phe7, presnet in high amounts of brain of rat, cattle and man is an opioid agonist. Nature 288:88–90
Schneider LE, Taghert PH (1988) Isolation and characterization of a Drosophila gene that encodes multiple neuropeptides related to Phe-Met-Arg-Phe-NH2 (FMRFamide). Proc Natl Acad Sci USA 85:1993–1997
Schoofs L, Jegou S, Vaudry H, Verhart P, De Loof A (1987) Localization of melanotropin-like peptides in the central nervous system of two insect species, the migratory locust, Locusta migratoria, and the fleshfly Sarcophaga bullata. Cell Tissue Res 248:25–31
Steller H, Fischbach K-F, Rubin GM (1987) Disconnected: A locus required for neuronal pathway formation in the visual system of Drosophila. Cell 50:1139–1153
Thorpe A, Duve H (1987) Purification, characterization and cellular distribution of insect neuropeptides with special emphasis on their relationship to biologically active peptides of vertebrates. In: Ali MA (ed) Nervous Systems of Invertebrates, Plenum Press, New York, pp 133–169
Triepel J, Grimmelikhuijzen CJP (1984) A critical examination of the occurrence of FMRFamide immunoreactivity in the brain of the guinea pig and the rat. Histochemistry 80:63–71
Truman JW, Reiss SE (1976) Dendritic reorganization of an identified motorneuron during metamorphosis of the tobacco hornworm moth. Science 192:477–479
Veenstra P, Schoonefeld H (1984) Immunocytochemical localization of neurons in the nervous system of the Colorado potato beetle with antisera against FMRFamide and bovine pancreatic polypeptide. Cell Tissue Res 235:303–308
Vcrhaert P, Grimmelikhuijzen CJP, De Loof A (1985) Distinct localization of FMRFamide and pancreatic polypeptide-like material in the brain, retrocerebral complex and suboesophageal ganglion of the cockroach Periplaneta americana L. Brain Res 348:331–338
White K, Hurteau T, Punsal P (1986) Neuropeptide-FMRFamide-like immunoreactivity in Drosophila: Development and distribution. J Comp Neurol 430–438
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Ohlsson, L.G., Johansson, K.U.I. & Nässel, D.R. Postembryonic development of Arg-Phe-amide-like and cholecystokinin-like immunoreactive neurons in the blowfly optic lobe. Cell Tissue Res. 256, 199–211 (1989). https://doi.org/10.1007/BF00224735
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00224735