Skip to main content
Log in

Immunocytochemical localization of Bombyx-PTTH-like molecules in neurosecretory cells of the brain of the migratory locust, Locusta migratoria

A comparison with neuroparsin and insulin-related peptide

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

Using a monoclonal antibody directed against a synthetic pentadecapeptide corresponding to the N-terminus of the prothoracicotropic hormone (PTTH) of Bombyx mori, we report the presence of immunoreactive molecules in a large number of median neurosecretory cells of the pars intercerebralis of the migratory locust, Locusta migratoria. These cells correspond to the A1 cell type which we show to contain also neuroparsins, a family of predominant neurohormones of the migratory locust. In contrast, PTTH-like molecules are absent from A2 cells of the pars intercerebralis which contain Locusta insulin-related peptide (LIRP). Developmental studies show the presence of PTTH-related substances in neurosecretory cells of Locusta migratoria from late embryogenesis to adult development, including ageing vitellogenic female adults.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Bodenstein D (1953) Studies on the humoral mechanism in growth and metamorphosis of the coackroach Periplaneta americana. II. The function of the prothoracic gland and the corpus cardiacum. J Exp Zool 123:413–433

    Google Scholar 

  • Bollenbacher WE, Agui N, Granger NA, Gilbert LI (1979) In vitro activation of insect prothoracic glands by prothoracicotropic hormone. Proc Natl Acad Sci USA 76:5148–5152

    Google Scholar 

  • Charlet M, Goltzené F, Hoffmann JA (1979) Experimental evidence for a neuroendocrine control of ecdysone biosynthesis in adult females of Locusta migratoria. J Insect Physiol 25:463–466

    Google Scholar 

  • Girardie A (1964) Action de la pars intercerebralis sur le développement de Locusta migratoria. J Insect Physiol 10:599–609

    Article  Google Scholar 

  • Girardie J, Rossi C (1978) Preuves histologiques et ultrastructurales de deux catégories de cellules neurosécrétrices protocérébrales médianes de type A chez le criquet migrateur. C R Acad Sci Paris 286:97–100

    Google Scholar 

  • Girardie J, Bourême D, Couillaud F, Tamarelle M, Girardie A (1987) Anti-juvenile effect of neuroparsin A, a neuroprotein isolated from locust corpora cardiaca. Insect Biochem 17:977–983

    Article  Google Scholar 

  • Girardie J, Girardie A, Huet JC (1989) Amino-acid sequence of locust neuroparsins. FEBS Lett 245:1–2

    Article  Google Scholar 

  • Girardie J, Huet JC, Pernollet JC (1990) The locust neuroparsin A: sequence and similarities with vertebrate and insect polypeptide hormones. Insect Biochem 20:659–666

    Article  Google Scholar 

  • Golzené F, Lagueux M, Charlet M, Hoffmann JA (1978) The folliclc cell epithelium of maturing ovaries of Locusta migratoria: a new biosynthetic tissue for ecdysone. Hoppe-Seyler's Z Physiol Chem 359:1427–1434

    PubMed  Google Scholar 

  • Hetru C, Wan Li K, Bulet P, Lagueux M, Hoffmann JA (1991) Isolation and structural characterization of an insulin-related molecule, a predominant neuropeptide from Locusta migratoria (Insecta, Orthoptera). Eur J Biochem 201:495–499

    PubMed  Google Scholar 

  • Hietter H, Van Dorsselaer A, Green B, Denoroy L, Hoffmann JA, Luu B (1990) Isolation and structure elucidation of a novel 5 kDa peptide from neurohaemal lobes of the corpora cardiaca of Locusta migratoria (Insecta, Orthoptera). Eur J Biochem 187:241–247

    PubMed  Google Scholar 

  • Hietter H, Van Dorsselaer A, Luu B (1991) Characterization of three structurally related 8 to 9 kDa monomeric peptides present in the corpora cardiaca of Locusta: a revised structure for the neuroparsins. Insect Biochem 21:259–264

    Article  Google Scholar 

  • Holder FC, Lwoff L, Wicker C, Goltzené F, Meister MF, Zachary D, Reichhart JM (1988) Production of monoclonal antibodies against corpora cardiaca extracts of Locusta migratoria: a potential tool for the isolation of insect neurohormones. Int J Invert Repord Dev 14:105–120

    Google Scholar 

  • Iwami M, Adachi T, Kondo H, Kawakami A, Suzuki Y, Nagasawa H, Suzuki A, Ishizaki H (1990) A novel family C of the genes that encode bombyxin, an insulin-related brain secretory peptide of the silkmoth Bombyx mori: isolation and characterization of gene C-1. Insect Biochem 20:295–303

    Article  Google Scholar 

  • Kataoka H, Nagasawa H, Isogai A Tamura S, Mizoguchi A, Fujiwara Y, Suzuki C, Ishizaki H, Suzuki A (1987) Isolation and partial characterization of a prothoracicotropic hormone of the silkworm, Bombyx mori. Agric Biol Chem 51:1067–1076

    Google Scholar 

  • Kataoka H, Nagasawa H, Kawakami A, Mizoguchi A, Iwami M, Ishizaki H, Suzuki A (1990) Bombyx prothoracicotropic hormone. In: Biologically active peptides in insects ACS Symp Ser (in press)

  • Kataoka H, Nagasawa H, Isogai A, Ishizaki H, Suzuki A (1991) Prothoracicotropic hormone of the silkworm, Bombyx mori: amino acid sequence and dimeric structure. Agric Biol Chem 55:73–86

    PubMed  Google Scholar 

  • Kawakami A, Iwami M, Nagasawa H, Suzuki A, Ishizaki H (1989) Structure and organization of four clustered genes that encode bombyxin, an insulin-related brain secretory peptide of the silkmonth Bombyx mori. Proc Natl Acad Sci USA 86:6843–6847

    PubMed  Google Scholar 

  • Kawakami A, Kataoka H, Oka T, Mizoguchi A, Kimura-Kawakani M, Adachi T, Iwami M, Nagasawa H, Suzuki A, Ishizaki H (1990) Molecular cloning of the Bombyx mori prothoracicotropic hormone. Science 247:1333–1335

    PubMed  Google Scholar 

  • Lacy MJ, Voss EW Jr (1986) A modified method to induce immune polyclonal ascites fluid in BALB/c mice using Sp2/0-Ag 14 cells. J Immunol Methods 87:169–177

    Article  PubMed  Google Scholar 

  • Lagueux M, Sall C, Hoffmann JA (1981) Ecdysteroids during embryogenesis of Locusta migratoria. Am Zool 21:715–726

    Google Scholar 

  • Lagueux M, Lwoff L, Meister M, Goltzené F, Hoffmann JA (1990) cDNAs from neurosecretory cells of brains of Locusta migratoria (Insecta, Orthoptera) encoding a novel member of the superfamily of insulins. Eur J Biochem 187:249–254

    PubMed  Google Scholar 

  • 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 silkmonth, Bombyx mori: characterization and immunocytochemistry. Mol Cell Endocrinol 51:227–235

    Article  PubMed  Google Scholar 

  • 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 Diff 32:591–598

    Google Scholar 

  • Nagasawa H, Kataoka H, Isogai A, Tamura S, Suzuki A, Ishizaki H, Mizoguchi A, Fujiwara Y, Suzuki A (1984) Aminoterminal amino-acid sequence of the silkworm prothoracicotropic hormone: homology with insulin. Science 226:1344–1345

    Google Scholar 

  • Nagasawa H, Kataoka H, Isogai A, Tamura S, Suzuki A, Mizoguchi A, Fujiwara Y, Suzuki A, Takahashi SY, Ishizaki H (1986) Amino acid sequence of a prothoracicotropic hormone of the silkworm Bombyx mori. Proc Natl Acad Sci USA 83:5840–5843

    Google Scholar 

  • O'Brien M, Katahira EJ, Flanagan TR, Arnold LW, Haughton G, Bollenbacher WE (1988) A monoclonal antibody to the insect prothoracicotropic hormone. J Neurosci 8:3247–3257

    PubMed  Google Scholar 

  • Possompes B (1953) Recherches expérimentales sur le déterminisme de la métamorphose de Calliphora erythrocephala. Meig Archiv Zool Exp Gen 89:203–364

    Google Scholar 

  • Raabe M (1989) Recent developments in insect neurohormones. Plenum Press, New York London

    Google Scholar 

  • Reichhart JM, Charlet M (1986) Ecdysiotropic activity in brains and corpora cardiaca of larvae and adults of Locusta migratoria: in vitro assays. Int J Invert Reprod Dev 10:17–25

    Google Scholar 

  • Wigglesworth V (1952) Hormone balance and the control of metamorphosis In Rhodnius prolixus (Hemiptera). J Exp Biol 29:620–631

    Google Scholar 

  • Williams CM (1947) Physiology of insect diapause. II. Interaction between the pupal brain and prothoracic glands in the metamorphosis of the giant silkworm Platysamia cecropia. Biol Bull 93:89–98

    Google Scholar 

  • Zachary D, Goltzené F, Holder FC, Berchtold JP, Nagasawa H, Suzuki C, Mizoguchi H, Ishizaki H, Hoffmann JA (1988) Presence of bombyxin-(4K-PTTH)-like molecules in neurosecretory granules of brain-corpora cardiaca complexes of Locusta migratoria. Developmental aspects. Int J Invert Reprod Dev 14:1–10

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Goltzené, F., Holder, F., Charlet, M. et al. Immunocytochemical localization of Bombyx-PTTH-like molecules in neurosecretory cells of the brain of the migratory locust, Locusta migratoria . Cell Tissue Res 269, 133–140 (1992). https://doi.org/10.1007/BF00384733

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00384733

Key words

Navigation