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DINeR

A Database for Insect Neuropeptide Research

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Insect Neuropeptides - Allatostatin B

Introduction

The first member of this family in insects was isolated from CNS extracts of Locusta migratoria (Schoofs et al., 1991). This peptide was termed locust-myoinhibiting peptide (LOM-MIP) due to its ability to inhibit locust hindgut and oviduct contractions. Additional members of this family were later isolated from Manduca sexta and also shown to inhibit hindgut contractions (Blackburn et al., 1995). Soon after this discovery, four additional peptides were isolated from the cricket, Gryllus bimaculatus (Lorenz et al., 1995). Interestingly, these peptides were capable of inhibiting juvenile hormone biosynthesis by the cricket corpora allata. These amidated peptides are characterized by two tryptophan residues at the C-terminus, denoted as the W(X6)Wamide motif. Hence these peptides are referred to as allatostatin-B (AST-B), myoinhibitory peptides (MIPs) or W(X6)Wamides. The first gene encoding AstBs was cloned from Drosophila melanogaster (Williamson et al., 2001). This precursor encodes 5 copies of AstBs, but this copy number varies between species (Bendena and Tobe, 2012). AstBs bind to and activate a rhodopsin-type GPCR. The first AstB receptor was deorphanized in Bombyx mori (Yamanaka et al., 2010) and soon afterwards in D. melanogaster (Kim et al., 2010). Interestingly, this receptor was previously shown to be activated by the sex peptide in Drosophila (Yapici et al., 2008). Since sex peptide is not found outside Drosophila this might be a derived function. Moreover, genes encoding AstBs and its receptors are absent in hymenopteran genomes (Bendena and Tobe, 2012). Despite the initial claims, AstBs are not related to the vertebrate galanin (Mirabeau and Joly, 2013).

Location

Drosophila and G. bimaculatus AstBs are brain-gut peptides as they expressed in both the CNS and gut (Veenstra, 2009; Wang et al., 2004; Williamson et al., 2001). However, in Rhodnius prolixus, AstB-like immunoreactivity is not found in the midgut endocrine cells (Lange et al., 2012). In Drosophila, AstBs are expressed in neurons throughout the CNS; in particular, they are expressed in the antennal lobe, lamina of the visual system and a subset of neurons in the ventral nerve cord that regulate ecdysis behavior (Carlsson et al., 2010; Y. J. Kim et al., 2006; Kolodziejczyk and Nässel, 2011; Min et al., 2016).

Function

AstBs function as allatostatins in G. bimaculatus, Tenebrio mollitor and Tribolium castaneum (Abdel-latief and Hoffmann, 2014, 2010; Lorenz et al., 1995). The myoinhibitory nature of AstBs has been shown in various insect species (Blackburn et al., 1995; Lange et al., 2012; Schoofs et al., 1991). In Bombyx mori, AstBs are prothoracicostatic as they inhibit ecdysteroid production by prothoracic glands and also play a role in ecdysis behaviour (Hua et al., 1999; Kim et al., 2006; Yamanaka et al., 2010). In Drosophila, AstBs regulate satiety in addition to their role in ecdysis (Kim et al., 2006; Min et al., 2016).

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Suggested Reviews

  • Bendena, W.G., Tobe, S.S., 2012. Families of allatoregulator sequences : a 2011 perspective. Can. J. Zool. 90, 521–544. doi:10.1139/Z2012-012
    View Review
  • Nässel, D.R., Winther, Å.M.E., 2010. Drosophila neuropeptides in regulation of physiology and behavior. Prog. Neurobiol. 92, 42–104. doi:10.1016/j.pneurobio.2010.04.010
    View Review
  • Stay, B., Tobe, S.S., 2007. The role of allatostatins in juvenile hormone synthesis in insects and crustaceans. Annu. Rev. Entomol. 52, 277–299. doi:10.1146/annurev.ento.51.110104.151050
    View Review
  • Verlinden, H., Gijbels, M., Lismont, E., Lenaerts, C., Vanden Broeck, J., Marchal, E., 2015. The pleiotropic allatoregulatory neuropeptides and their receptors: A mini-review. J. Insect Physiol. 80, 2–14. doi:10.1016/j.jinsphys.2015.04.004
    View Review

References

  • Abdel-latief, M., Hoffmann, K.H., 2014. Functional activity of allatotropin and allatostatin in the pupal stage of a holometablous insect, Tribolium castaneum (Coleoptera, Tenebrionidae). Peptides 53, 172–184. doi:10.1016/j.peptides.2013.10.007
  • Abdel-latief, M., Hoffmann, K.H., 2010. Neuropeptide regulators of the juvenile hormone biosynthesis (in vitro) in the beetle, Tenebrio molitor (Coleoptera, Tenebrionidae). Arch. Insect Biochem. Physiol. 74, 135–46. doi:10.1002/arch.20359
  • Bendena, W.G., Tobe, S.S., 2012. Families of allatoregulator sequences : a 2011 perspective. Can. J. Zool. 90, 521–544. doi:10.1139/Z2012-012
  • Blackburn, M.B., Wagner, R.M., Kochansky, J.P., Harrison, D.J., Thomas-Laemont, P., Raina, A.K., 1995. The identification of two myoinhibitory peptides, with sequence similarities to the galanins, isolated from the ventral nerve cord of Manduca sexta. Regul. Pept. 57, 213–219. doi:10.1016/0167-0115(95)00034-9
  • Carlsson, M.A., Diesner, M., Schachtner, J., Nässel, D.R., 2010. Multiple neuropeptides in the Drosophila antennal lobe suggest complex modulatory circuits. J. Comp. Neurol. 518, 3359–80. doi:10.1002/cne.22405
  • Hua, Y.-J., Tanaka, Y., Nakamura, K., Sakakibara, M., Nagata, S., Kataoka, H., 1999. Identification of a Prothoracicostatic Peptide in the Larval Brain of the Silkworm, Bombyx mori. J. Biol. Chem. 274, 31169–31173. doi:10.1074/jbc.274.44.31169
  • Kim, Y.-J., Zitnan, D., Cho, K.-H., Schooley, D. a, Mizoguchi, A., Adams, M.E., 2006. Central peptidergic ensembles associated with organization of an innate behavior. Proc. Natl. Acad. Sci. U. S. A. 103, 14211–14216. doi:10.1073/pnas.0603459103
  • Kim, Y.-J.Y.-C., Bartalska, K., Audsley, N., Yamanaka, N., Yapici, N., Lee, J.-Y., Markovic, M., Isaac, E., Tanaka, Y., Dickson, B.J., 2010. MIPs are ancestral ligands for the sex peptide receptor. Proc. Natl. Acad. Sci. 107, 6520–5. doi:10.1073/pnas.0914764107
  • Kim, Y.J., Žitňan, D., Galizia, C.G., Cho, K.H., Adams, M.E., 2006. A Command Chemical Triggers an Innate Behavior by Sequential Activation of Multiple Peptidergic Ensembles. Curr. Biol. 16, 1395–1407. doi:10.1016/j.cub.2006.06.027
  • Kolodziejczyk, A., Nässel, D.R., 2011. A novel wide-field neuron with branches in the lamina of the Drosophila visual system expresses myoinhibitory peptide and may be associated with the clock. Cell Tissue Res. 343, 357–69. doi:10.1007/s00441-010-1100-7
  • Lange, A.B., Alim, U., Vandersmissen, H.P., Mizoguchi, A., Broeck, J. Vanden, Orchard, I., 2012. The distribution and physiological effects of the myoinhibiting peptides in the kissing bug, Rhodnius prolixus. Front. Neurosci. 6, 1–9. doi:10.3389/fnins.2012.00098
  • Lorenz, M.W., Kellner, R., Hoffmann, K.H., 1995. A family of neuropeptides that inhibit juvenile hormone biosynthesis in the cricket, Gryllus bimaculatus. J. Biol. Chem. 270, 21103–8.
  • Min, S., Chae, H.-S., Jang, Y.-H., Choi, S., Lee, S., Jeong, Y.T., Jones, W.D., Moon, S.J., Kim, Y.-J., Chung, J., 2016. Identification of a Peptidergic Pathway Critical to Satiety Responses in Drosophila. Curr. Biol. 1–7. doi:10.1016/j.cub.2016.01.029
  • Mirabeau, O., Joly, J.-S., 2013. Molecular evolution of peptidergic signaling systems in bilaterians. Proc. Natl. Acad. Sci. U. S. A. 110, E2028–37. doi:10.1073/pnas.1219956110
  • Schoofs, L., Holman, G.M., Hayes, T.K., Nachman, R.J., De Loof, A., 1991. Isolation, identification and synthesis of locustamyoinhibiting peptide (LOM-MIP), a novel biologically active neuropeptide from Locusta migratoria. Regul. Pept. 36, 111–9.
  • Veenstra, J. a., 2009. Peptidergic paracrine and endocrine cells in the midgut of the fruit fly maggot. Cell Tissue Res. 336, 309–323. doi:10.1007/s00441-009-0769-y
  • Wang, J., Meyering-Vos, M., Hoffmann, K.H., 2004. Cloning and tissue-specific localization of cricket-type allatostatins from Gryllus bimaculatus. Mol. Cell. Endocrinol. 227, 41–51. doi:10.1016/j.mce.2004.07.014
  • Williamson, M., Lenz, C., Winther, M.E., Nässel, D.R., Grimmelikhuijzen, C.J.P., 2001. Molecular Cloning, Genomic Organization, and Expression of a B-Type (Cricket-Type) Allatostatin Preprohormone from Drosophila melanogaster. Biochem. Biophys. Res. Commun. 281, 544–550. doi:10.1006/bbrc.2001.4402
  • Yamanaka, N., Hua, Y.-J., Roller, L., Spalovská-Valachová, I., Mizoguchi, A., Kataoka, H., Tanaka, Y., 2010. Bombyx prothoracicostatic peptides activate the sex peptide receptor to regulate ecdysteroid biosynthesis. Proc. Natl. Acad. Sci. U. S. A. 107, 2060–5. doi:10.1073/pnas.0907471107
  • Yapici, N., Kim, Y.-J., Ribeiro, C., Dickson, B.J., 2008. A receptor that mediates the post-mating switch in Drosophila reproductive behaviour. Nature 451, 33–7. doi:10.1038/nature06483