Morphological characterization of neurons projecting to the ring gland in the larval blow fly, protophormia terraenovae

Zoological Science

Volumn 26, Issue 3, 2009, Pages 227-237

  Hamanaka, Yoshitaka ^a,b   Tanaka, Shinji ^a   Numata, Hideharu ^a   Shiga, Sakiko ^a  

^a Osaka Prefecture University   (Japan)

^b DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Backfill; Immunocytochemistry; Neurosecretory cell; Pars intercerebralis; Pars lateralis; Subesophageal ganglion

Indexed keywords

CHOLECYSTOKININ; CHOLECYSTOKININ OCTAPEPTIDE; PEPTIDE; PEPTIDE FRAGMENT; PHENYLALANYLMETHIONYLARGINYLPHENYLALANINAMIDE;

ANIMAL; ARTICLE; CYTOLOGY; FLY; HISTOLOGY; IMMUNOHISTOCHEMISTRY; LARVA; METABOLISM; NERVE CELL;

ANIMALS; CHOLECYSTOKININ; DIPTERA; FMRFAMIDE; IMMUNOHISTOCHEMISTRY; LARVA; NEURONS; PEPTIDE FRAGMENTS; PEPTIDES;

ARMORACIA RUSTICANA; CALLIPHORIDAE; GRYLLUS; PROTOPHORMIA TERRAENOVAE;

EID: 65949087883     PISSN: 02890003     EISSN: 02890003     Source Type: Journal    
DOI: 10.2108/zsj.26.227     Document Type: Article

References (61)

1. Agui N, Bollenbacher WE, Granger NA, Gilbert LI (1980) Corpus allatum is release site for insect prothoracicotropic hormone. Nature 285: 669-670 (Pubitemid 10058190)
2. Bader R, Colomb J, Pankratz B, Schröck A, Stocker RF, Pankratz MJ (2007) Genetic dissection of neural circuit anatomy underlying feeding behavior in Drosophila: distinct classes of hugin-expressing neurons. J Comp Neurol 502: 848-856 (Pubitemid 46732500)
3. Bollenbacher WE, Goodman W, Vedeckis WV, Gilbert LI (1976) The in vitro synthesis and secretion of α-ecdysone by the ring glands of the fly, Sarcophaga bullata. Steroids 27: 309-324
4. Brown MR, Graf R, Swiderek KM, Fendley D, Stracker TH, Champagne DE, Lea AO (1998) Identification of a steroidogenic neurohormone in female mosquitoes. J Biol Chem 273: 3967-3971 (Pubitemid 28103258)
5. Cantera R (1988) Serotonin and gastrin/cholecystokinin-like immunoreactive neurons in the larval retrocerebral complex of the blowfly Calliphora erythrocephala. Cell Tissue Res 253: 425-433
6. Cantera R, Veenstra JA, Nässel DR (1994) Postembryonic development of corazonin-containing neurons and neurosecretory cells in the blowfly, Phormia terraenovae. J Comp Neurol 350: 559-572 (Pubitemid 24372035)
7. Copenhaver PF, Truman JW (1986) Metamorphosis of the cerebral neuroendocrine system in the moth Manduca sexta. J Comp Neurol 249:186-204 (Pubitemid 16060474)
8. Dircksen H, Zahnow CA, Gaus G, Keller R, Rao KR, Riehm JP (1987) The ultrastructure of nerve endings containing pigmentdispersing hormone (PDH) in crustacean sinus glands: identification by an antiserum against a synthetic PDH. Cell Tissue Res 250:377-387
9. Downer KE, Haselton AT, Nachman RJ, Stoffolano JG Jr (2007) Insect satiety: sulfakinin localization and the effect of drosulfakinin on protein and carbohydrate ingestion in the blow fly, Phormia regina (Diptera: Calliphoridae). J Insect Physiol 53:106-112 (Pubitemid 46027089)
10. Duve H, Thorpe A, Scott AG, Johnsem AH, Rehfeld JF, Hines E, East PD (1995) The sulfakinins of the blowfly Calliphora vomitoria: peptide isolation, gene cloning and expression studies. Eur J Biochem 232: 633-640
11. Eckert M, Ude J (1983) Immunocytochemical techniques for the identification of peptidergic neurons. In "Functional Neuroanatomy" Ed by NJ Strausfeld, Springer-Verlag, Berlin, pp 267-301
12. Giebultowicz JM, Denlinger DL (1985) Identification of neurons innervating the ring gland of the flesh fly larva, Sarcophaga crassipalpis Macquart (Diptera: Sarcophagidae). Int J Insect Morphol Embryol 14:155-161
13. Hamanaka Y, Numata H, Shiga S (2004) Morphology and electrophysiological properties of neurons projecting to the retrocerebral complex in the blow fly, Protophormia terraenovae. Cell Tissue Res 318: 403-418 (Pubitemid 39506509)
14. Hamanaka Y, Yasuyama K, Numata H, Shiga S (2005) Synaptic connections between pigment-dispersing factor-immunoreactive neurons and neurons in the pars lateralis of the blow fly Protophormia terraenovae. J Comp Neurol 491: 390-399 (Pubitemid 41376987)
15. Hamanaka Y, Tanaka S, Numata H, Shiga S (2007) Peptide immunocytochemistry of neurons projecting to the retrocerebral complex in the blow fly, Protophormia terraenovae. Cell Tissue Res 329: 581-593 (Pubitemid 47231298)
16. Helfrich-Forster C (1997) Development of pigment-dispersing hormone-immunoreactive neurons in the nervous system of Drosophila melanogaster. J Comp Neurol 380: 335-354 (Pubitemid 27161325)
17. Honda T, Matsushima A, Sumida K, Chuman Y, Sakaguchi K, Onoue H, Meinertzhagen IA, Shimohigashi Y, Shimohigashi M (2006) Structural isoforms of the circadian neuropeptide PDF expressed in the optic lobes of the cricket Gryllus bimaculatus: immunocytochemical evidence from specific monoclonal antibodies. J Comp Neurol 499: 404-421 (Pubitemid 44571936)
18. Ichikawa T (1991) Architecture of cerebral neurosecretory cell systems in the silkworm Bombyx mori. J Exp Biol 161: 217-237
19. Lloyd GL, Woodhead AP, Stay B (2000) Release of neurosecretory granules within the corpus allatum in relation to the regulation of juvenile hormone synthesis in Diploptera punctata. Insect Biochem Mol Biol 30: 739-746 (Pubitemid 30640981)
20. Maestro J, Aguilar R, Pascual N, Valero ML, Piulachs MD, Andreu D, Navarro I, Belles X (2001) Screening of antifeedant activity in brain extracts led to the identification of sulfakinin as a satiety promoter in the German cockroach. Eur J Biochem 268: 5824-5830
21. McBrayer Z, Ono H, Shimell M, Parvy J-P, Beckstead RB, Warren JT, Thummel CS, Dauphin-Villemant C, Gilbert LI, O'Connor MB (2007) Prothoracicotropic hormone regulates developmental timing and body size in Drosophila. Dev Cell 13: 857-871 (Pubitemid 350176296)
22. Melcher C, Pankratz MJ (2005) Candidate gustatory interneurons modulating feeding behavior in the Drosophila brain. PLoS Biol 3: e305 (Pubitemid 41306445)
23. Meng X, Wahlström G, Immonen T, Kolmer M, Tirronen M, Predel R, Kalkkinen N, Heino Tl, Sariola H, Roos C (2002) The Drosophila hugin gene codes for myostimulatory and ecdysismodifying neuropeptides. Mech Dev 117: 5-13
24. Mizoguchi A, Ishizaki H, Nagasawa H, Kataoka H, Isogai A, Tamura S, Suzuki A, Fujino M, Kitada C (1987) A monoclonal antibody against a synthetic fragment of bombyxin (4K-prothoracicotropic hormone) from the silkmoth, Bombyx mori: characterization and immunohistochemistry. Mol Cell Endocrinol 51: 227-235
25. Mizoguchi A, Oka T, Kataoka H, Nagasawa H, Suzuki A, Ishizaki H (1990) Immunohistochemical localization of prothoracicotropic hormone-producing neurosecretory cells in the brain of Bombyx mori. Dev Growth Differ 32: 591-598
26. Nassel DR (1982) Transneuronal uptake of horseradish peroxidase in the central nervous system of dipterous insects. Cell Tissue Res 225: 639-662
27. Nassel DR (2002) Neuropeptides in the nervous system of Drosophila and other insects: multiple roles as neuromodulators and neurohormones. Prog Neurobiol 68: 1-84 (Pubitemid 35339441)
28. Nassel DR, Shiga S, Mohrherr CJ, Rao KR (1993) Pigmentdispersing hormone-like peptide in the nervous system of the flies Phormia and Drosophila: Immunocytochemistry and partial characterization. J Comp Neurol 331: 183-198 (Pubitemid 23121857)
29. Nässel DR, Enell LE, Santos JG, Wegener C, Johard HAD (2008) A large population of diverse neurons in the Drosophila central nervous system expresses short neuropeptide F, suggesting multiple distributed peptide functions. BMC Neurosci 9: 90
30. Neupert S, Johard HAD, Nässel DR, Predel R (2007) Single-cell peptidomics of Drosophila melanogaster neurons identified by Gal4-driven fluorescence. Anal Chem 79: 3690-3694 (Pubitemid 46799064)
31. Nichols R, Lim IA (1996) Spatial and temporal immunocytochemical analysis of drosulfakinin (Dsk) gene products in the Drosophila melanogaster central nervous system. Cell Tissue Res 283: 107-116
32. Nichols R, Schneuwly SA, Dixon JE (1988) Identification and characterization of a Drosophila homologue to the vertebrate neuropeptide cholecystokinin. J Biol Chem 263: 12167-12170
33. Nijhout HF (1994) Insect Hormones. Princeton University Press, Princeton
34. Numata H, Shiga S (1995) Induction of adult diapause by photoperiod and temperature in Protophormia terraenovae (Diptera: Calliphoridae) in Japan. Environ Entomol 24:1633-1636
35. O'Brien MA, Katahira EJ, Flanagan TR, Arnold LW, Haughton G, Bollenbacher WE (1988) A monoclonal antibody to the insect prothoracicotropic hormone. J Neurosci 8: 3247-3257 (Pubitemid 18232435)
36. Orchard I, Loughton BG (1985) Neurosecretion. In "Comprehensive Insect Physiology, Biochemistry and Pharmacology, Vol 7, Endocrinology I" Ed by GA Kerkut, LI Gilbert, Pergamon Press, Oxford, pp 61-107
37. Orchard I, Lange AB, Bendena WG (2001) FMRFamide-related peptides: a multifunctional family of structurally related neuropeptides in insects. Adv Insect Physiol 28: 267-329 (Pubitemid 33804481)
38. Park JH, Helfrich-Förster C, Lee G, Liu L, Rosbash M, Hall JC (2000) Differential regulation of circadian pacemaker output by separate clock genes in Drosophila. Proc Natl Acad Sci USA 97:3608-3613 (Pubitemid 30183350)
39. Persson MGS, Eklund MB, Dircksen H, Muren JE, Nassel DR (2001) Pigment-dispersing factor in the locust abdominal ganglia may have roles as circulating neurohormone and central neuromodulator. J Neurobiol 48: 19-41 (Pubitemid 32564883)
40. Possompes B (1953) Recherches expérimentales sur le déterminisme de la métamorphose de Calliphora erythrocephala Meig. Arch Zool Exp 89: 203-364
41. Pyza E, Siuta T, Tanimura T (2003) Development of PDF-immunoreactive cells, possible clock neurons, in the housefly Musca domestica. Micros Res Tech 62: 103-113 (Pubitemid 37102476)
42. Raabe M (1989) Recent Developments in Insect Neurohormones. Plenum Press, New York
43. Renn SCP, Park JH, Rosbash M, Hall JC, Taghert PH (1999) A pdf neuropeptide gene mutation and ablation of PDF neurons each cause severe abnormalities of behavioral circadian rhythms in Drosophila. Cell 99: 791-802 (Pubitemid 30017649)
44. Rulifson EJ, Kim SK, Nusse R (2002) Ablation of insulin-producing neurons in flies: growth and diabetic phenotypes. Science 296: 1118-1120 (Pubitemid 34517128)
45. Satake S, Masumura M, Ishizaki H, Nagata K, Kataoka H, Suzuki A, Mizoguchi A (1997) Bombyxin, an insulin-related peptide of insects, reduces the major storage carbohydrates in the silkworm Bombyx mori. Comp Biochem Physiol B 118: 349-357 (Pubitemid 28006061)
46. Schneider LE, O'Brien MA, Taghert PH (1991) In situ hybridization analysis of the FMRFamide neuropeptide gene in Drosophila. I. Restricted expression in embryonic and larval stages. J Comp Neurol 304: 608-622
47. Schneider LE, Sun ET, Garland DJ, Taghert PH (1993) An immunocytochemical study of the FMRFamide neuropeptide gene products in Drosophila. J Comp Neurol 337: 446-460 (Pubitemid 23320779)
48. Shiga S, Toyoda I, Numata H (2000) Neurons projecting to the retrocerebral complex of the adult blow fly, Protophormia terraenovae. Cell Tissue Res 299: 427-439 (Pubitemid 30160452)
49. Siegmund T, Korge G (2001) Innervation of the ring gland of Drosophila melanogaster. J Comp Neurol 431: 481-491 (Pubitemid 32178950)
50. Stay B, Chan KK, Woodhead AP (1992) Allatostatin-immunoreactive neurons projecting to the corpora allata of adult Diploptera punctata. Cell Tissue Res 270: 15-23
51. Stay B, Zhang JR, Kwok RD, Tobe SS (2003) Localization and physiological effects of RFamides in the corpora allata of the cockroach Diploptera punctata in relation to allatostatins. Peptides 24: 1501-1510 (Pubitemid 38045562)
52. Strand FL (1999) Neuropeptides: Regulators of Physiological Processes. MIT Press, Cambridge
53. Thomsen M (1951) Weismann's ring and related organs in larvae of Diptera. Kongel Danske Vidensk Sel 6: 1-32
54. Veenstra JA, Lehman HK, Davis NT (1994) Allatotropin is a cardioacceleratory peptide in Manduca sexta. J Exp Biol 188: 347-354 (Pubitemid 2057224)
55. Verleyen P, Clynen E, Huybrechts J, Van Lommel A, Vanden Bosch L, De Loof A, Zdarek J, Schoofs L (2004) Fraenkel's pupariation factor identified at last. Dev Biol 273: 38-47 (Pubitemid 39078365)
56. Weber E, Evans CJ, Samuelsson SJ, Barchas JD (1981) Novel peptide neuronal system in rat brain and pituitary. Science 214: 1248-1251 (Pubitemid 12167332)
57. Wegener C, Reinl T, Jänsch L, Predel R (2006) Direct mass spectrometric peptide profiling and fragmentation of larval peptide hormone release sites in Drosophila melanogaster reveals tag ma-specific peptide expression and differential processing. J Neurochem 96: 1362-1374
58. Wei Z, Baggerman G, Nachman RJ, Goldsworthy G, Verheart P, De Loof A, Schoofs L (2000) Sulfakinins reduce food intake in the desert locust, Schistocerca gregaria. J Insect Physiol 46: 1259-1265 (Pubitemid 30483210)
59. White K, Hurteau T, Punsal P (1986) Neuropeptide-FMRFamide-like immunoreactivity in Drosophila: development and distribution. J Comp Neurol 247: 430-138 (Pubitemid 16076548)
60. Yu CG, Stay B, Joshi S, Tobe SS (1993) Allatostatin content of brain, corpora allata and haemolymph at different developmental stages of the cockroach, Diploptera punctata: quantitation by ELISA and bioassay. J Insect Physiol 39: 111-122
61. Zithan D, Kingan TG, Kramer SJ, Beckage NE (1995) Accumulation of neuropeptides in the cerebral neurosecretory system of Manduca sexta larvae parasitized by the braconid wasp Cotesia congregata. J Comp Neurol 356: 83-100