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Immunological evidence for an allatostatin-like neuropeptide in the central nervous system of Schistocerca gregaria, Locusta migratoria and Neobellieria bullata

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Abstract

Methanolic brain extracts of Locusta migratoria inhibit in vitro juvenile hormone biosynthesis in both the locust L. migratoria and the cockroach Diploptera punctata. A polyclonal antibody against allatostatin-5 (AST-5) (dipstatin-2) of this cockroach was used to immunolocalize allatostatin-5-like peptides in the central nervous system of the locusts Schistocerca gregaria and L. migratoria and of the fleshfly Neobellieria bullata. In both locust species, immunoreactivity was found in many cells and axons of the brain-retrocerebral complex, the thoracic and the abdominal ganglia. Strongly immunoreactive cells were stained in the pars lateralis of the brain with axons (NCC II and NCA I) extending to and arborizing in the corpus cardiacum and the corpora allata. Although many neurosecretory cells of the pars intercerebralis project into the corpus cardiacum, only 12 of them were immunoreactive and the nervi corporis cardiaci I (NCC I) and fibers in the nervi corporis allati II (NCA II) connecting the corpora allata to the suboesophageal ganglion remained unstained. S. gregaria and L. migratoria seem to have an allatostatin-like neuropeptide present in axons of the NCC II and the NCA I leading to the corpus cardiacum and the corpora allata. All these data suggest that in locusts allatostatin-like neuropeptides might be involved in controlling the production of juvenile hormone by the corpora allata and, perhaps, some aspects of the functioning of the corpus cardiacum as well. However, when tested in a L. migratoria in-vitro juvenile hormone-biosynthesis assay, allatostatin-5 did not yield an inhibitory or stimulatory effect. There is abundant AST-5 immunoreactivity in cell bodies of the fleshfly N. bullata, but none in the CA-CC complexes. Apparently, factors that are immunologically related to AST-5 do occur in locusts and fleshflies but, the active protion of the peptide required to inhibit JH biosynthesis in locusts is probably different from that of AST-5.

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References

  • Ashby G (1972) Locusts. In: The UFAW handbook on the care and management of laboratory animals. Edited by UFAW. Churchill Livingstone, Edingburgh London, pp 582–587

    Google Scholar 

  • Bhaskaran G, Dahm KH, Barrera P, Pacheco JL, Peck KE Muszynska-Pytel (1990) Allatinhibin, a neurohormonal inhibitor of juvenile hormone synthesis in Manduca sexta. Gen Comp Endocrinol 78:123–136

    Google Scholar 

  • Borovsky D, Carlson DA, Hancock RG, Rembold H, Van Handel E (1994) De novo biosynthesis of juvenile hormone III and I by the accessory glands of the male mosquito. Insect Biochem Mol Biology 24:437–444

    Google Scholar 

  • Cassier P, Fain-Maurel MA (1970) Contribution a, l'étude infrastructurale du système neurosécréteur retrocérébral chez Locusta migratoria migratorioides (R. et F.) II Le transit des neurosecrétions. Z Zellforsch Mikrosk Anat 111:483–492

    Google Scholar 

  • Couillaud F Girardie A (1985) Control of C-16 juvenile hormone biosynthesis in active corpora allata of female African locust. Int Invert Reprod Develop 8:303–315

    Google Scholar 

  • Couillaud F, Girardie A (1990) Disconnected corpora allata provide a novel assay for allatostimulating factors. J Exp Zool 253:330–333

    Google Scholar 

  • Couillaud F, Mauchamp B, Girardie A (1987) Regulation of juvenile hormone titer in African locust. Experientia 41:1165–1167

    Google Scholar 

  • Couillaud F, Mauchamp B, Girardie A (1987) Biological, radiochemical and physicochemical evidence for the low activity of disconnected corpora allata in locust. J Insect Physiol 33:223–228

    Google Scholar 

  • Donly BC, Ding Q, Tobe SS, Bendena WG (1993) Molecular cloning of the gene for the allatostatin family of neuropeptides from the cockroach Diploptera punctata. Proc Natl Acad Sci USA 90:8807–8811

    Google Scholar 

  • Duve H, Thorpe A (1994) Distribution and functional significance of Leu-callatostatins in the blowfly Calliphora vomitoria. Cell Tissue Res 276:367–379

    Google Scholar 

  • Duve H, Johnson AH, Scott AG, Yu CG, Yagi KJ, Tobe SS, Thorpe A (1993) Callatostatins: neuropeptides from the blowfly Calliphora vomitoria with sequence homology to cockroach allatostatins. Proc Natl Acad Sci USA 90:2456–60

    Google Scholar 

  • Ferenz HJ (1984) Isolation of an allatotropic factor in Locusta migratoria and its effect on corpus allatum activity in vitro. In: Hoffman J, Prochet M (eds) Biosynthesis, Metabolism and mode of action of invertebrate hormones. Springer, Berlin, pp 92–96

    Google Scholar 

  • Ferenz HJ, Diehl I (1983) Stimulation of juvenile hormone biosynthesis in vitro by locust allatotropin. Z Naturforsch [C] 38:856–858

    Google Scholar 

  • Gadot M, Applebaum SW (1985) Rapid in vitro activation of corpora allata by extracted locust brain allatotropic factor. Arch Insect Biochem Physiol 2:117–129

    Google Scholar 

  • Giraride A (1967) La pars intercérébralis chez Locusta migratoria et son role dans le développement. Thèse, Strasbourg, pp124

  • Girardie J, Tobe SS, Girardie A (1981) Biosynthèse de l'hormone juvenile C-16 (JH-III) et maturation ovarienne chez le criquet migratuer. C R Acad Sci [III] 293:443–446

    Google Scholar 

  • Granger NA, Mitchell LJ Janzen WP, Bollenbacher WE (1984) Activation of Manduca sexta corpora allata in vitro by a cerebral neuropeptide. Mol Cell Endocrinol 37:349–358

    Google Scholar 

  • Huybrechts R, De Loof A (1981) Effect of ecdysteron on vitellogenin concentration in haemolymph of male and female Sarcophaga. Int J Invert Reprod 3:91–98

    Google Scholar 

  • Konings PNM, Vullings HGB, Kok OJM, Diederen JHB, Jansen WF (1989) The innervation of the corpus cardiacum of Locusta migratoria: a neuroanatomical study with the use of lucifer yellow. Cell Tissue Res 258:301–308

    Google Scholar 

  • Kramer SJ, Toschi A, Miller CA, Kataoka H, Quistad GB, Li JP, Carney RL, Schooley DA (1991) Identification of an allatostatin from the tobacco hornworm Manduca sexta. Proc Natl Acad Sci USA 88:9458–62

    Google Scholar 

  • Lange AB, Chan KK, Stay B (1993) Effect of allatostatin and proctolin on antennal pulsatile organ and hindgut muscle in the cockroach, Diploptera punctata. Arch Insect Biochem Physiol 24:79–92

    Google Scholar 

  • Lehmberg E, Ferenz HJ Applebaum SW (1992) Maturation and responsiveness to extracts of corpora allata from male Locusta migratoria containing allatotropic factors. Z Naturforsch 47:449–452

    Google Scholar 

  • Mason CA (1973) New features of the brain-retrocerebral neuroendocrine complex of the locust Schistocerca vaga (Scudder). Z Zellforsch Mikroskop Anat 141:19–32

    Google Scholar 

  • Mauchamp B, Couillaud F, Malosse C (1985) GC-MS analysis of juvenile hormone release by insect corpora allata. Analyt Biochem 145:251–256

    Google Scholar 

  • Poras M, Baehr JC, Cassier P (1983) Control of corpus allatum activity during the imaginal diapause in females of Locusta migratoria migratorioides L. Int J Invert Reprod 6:110–112

    Google Scholar 

  • Pratt GE, Tobe SS (1974) Juvenile hormone radiobiosynthesized by corpora allata of adult female. Life Sci 14:575–587

    Google Scholar 

  • Pratt GE, Farnsworth DE Siegel NR, Fok KF, Feyereisen R (1989) Identification of an allatostatin from adult Diploptera punctata. Biochem Biophys Res Comm 163:1243–1247

    Google Scholar 

  • Pratt GE, Farnsworth DE, Fok KF, Siegel NR, McCormack AL, Shabanowitz J, Hunt DF, Feyereisen R (1991) Identity of a second type of allatostatin from the cockroach brains: an octadecapeptide amide with a tyrosine-rich address sequence. Proc Natl Acad Sci USA 88:2412–2416

    Google Scholar 

  • Rademakers LHPM (1977) Identification of a secretomotor centre in the brain of Locusta migratoria, controlling secretory activity of the adipokinetic hormone producing, cells of the corpus cardiacum. Cell Tissue Res 184:381–395

    Google Scholar 

  • Rembold H, Schlagintweit B, Ulrich GM (1986) Activation of juvenile hormone sythesis in vitro by a corpus cardiacum factor from Locusta migratoria. J Insect Physiol 32:91–94

    Google Scholar 

  • Schoofs L, Tips A, Holman GM, Nachman RJ, De Loof A (1992) Distribution of locustamyotropin-like immunoreactivity in the nervous system of Locusta migratoria. Regul Peptides 37:237–254

    Google Scholar 

  • Schoofs L, Holman GM, Paemen L, Veelaert D, Amelinckx M, De Loof A (1993a) Isolation, identification and synthesis of PDVDHVFLRFamide (SchistoFLRFamide) in Locusta migratoria and its association with the male accessory glands, the salivary glands, the heart, and the oviduct. Peptides 14:409–421

    Google Scholar 

  • Schoofs L, Vanden Broeck J, De Loof A (1993b) The myotropic peptides of Locusta migratoria: structures, distribution, functions and receptors. Insect Biochem Molec Biol 23:859–881

    Google Scholar 

  • Stay B, Tobe SS, Bendena WG (1994) Allatostatins: identification, primary structures, functions and distribution. Adv Insect Physiol 25:267–338

    Google Scholar 

  • Tobe SS, Clarke N (1985) The effect of L-methionine concentration on juvenile hormone biosynthesis by corpora allata of the cockroach D. punctata. Insect Biochem 15:175–179

    Google Scholar 

  • Tobe SS, Pratt GE (1974) The influence of substrate concentrations on the rate of insect juvenile hormone biosynthesis by corpora allata of the desert locust in vitro. Biochem J 144: 107–113

    Google Scholar 

  • Tobe SS, Stay B (1985) Structure and regulation of the corpus allatum. Adv Insect Physiol 18:305–432

    Google Scholar 

  • Tobe SS, Chapman CS, Pratt GE (1977) Delay in juvenile hormone biosynthesis by corpora allata after nerve transsection. Nature 268:728–730

    Google Scholar 

  • Tobe SS, Yu CG, Bendena WG (1994) Allatostatins, peptide inhibitors of juvenile hormone production in insects. In: Davey KG, Peter RE, Tobe SS (eds) Perspectives in Comparative Endocrinology. NRC Journals, Ottawa, pp 12–19

    Google Scholar 

  • Tyrer NM, Gregory GE (1982) A guide to the neuroanatomy of locust suboesophageal and thoracic ganglia. Phil. Trans R Soc Lond [Biol] 297:91–123

    Google Scholar 

  • Unni BG, Bhaskaran G, Dahm KH, Hayes TK (1991) Stimulation of juvenile hormone biosynthesis by analogues of a Manduca sexta allatotropin in vitro studies. Arch Insect Biochem Physiol 17:129–142

    Google Scholar 

  • Vandesande F, Dierickx K (1976) Immunocytochemical demonstration of separate vasotocinergic neurons in the amphibian magnocellular neurosecretory system. Cell Tissue Res 176:289–296

    Google Scholar 

  • Weaver RJ, Freeman ZA, Pickering MG, Edwards JP (1994) Identification of two allatostatins from the CNS of the cockroach Periplaneta americana: novel members of a family of neuropeptide inhibitors of insect juvenile hormone biosynthesis. Comp Biochem Physiol [C] 107:119–127

    Google Scholar 

  • Woodhead AP, Stay B, Seidel SL, Khan MA, Tobe SS (1989) Primary structure of four allatostatins: neuropeptide inhibitors of juvenile hormone synthesis. Proc Natl Acad Sci USA 86:5997–6001

    Google Scholar 

  • Woodhead AP, Stoltzman CA, Stay B (1992) Allatostatins in the nerves of the antennal pulsatile organ of the cockroach Diploptera punctata. Arch Insect Biochem Physiol 20:253–63

    Google Scholar 

  • Woodhead AP, Khan MA, Stay B, Tobe SS (1994) Two new allatostatins from brains of Diploptera punctata. Insect Biochem Mol Biol 24:257–263

    Google Scholar 

  • 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: quantification by ELISA and bioassay. J Insect Physiol 38:111–122

    Google Scholar 

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Veelaert, D., Schoofs, L., Tobe, S.S. et al. Immunological evidence for an allatostatin-like neuropeptide in the central nervous system of Schistocerca gregaria, Locusta migratoria and Neobellieria bullata . Cell Tissue Res 279, 601–611 (1995). https://doi.org/10.1007/BF00318172

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