Advertisement

Neuropeptide Signaling in Insects

  • Miriam AltsteinEmail author
  • Dick R. Nässel
Chapter
Part of the Advances in Experimental Medicine and Biology book series (volume 692)

Abstract

Neuropeptides represent the largest single class of signal compounds and are involved in regulation of development, growth, reproduction, metabolism and behavior of insects. Over the last few years there has been a tremendous increase in our knowledge of neuropeptide signaling due to genome sequencing, peptidomics, gene micro arrays, receptor characterization and targeted gene interference combined with physiological and behavior analysis. In this chapter we review the current knowledge of structure and distribution of insect neuropeptides and their receptors, as well as their diverse functions. We also discuss peptide biosynthesis, processing and expression, as well as classification of insect neuropeptides. Special attention is paid to the role insect neuropeptides play as potential targets for pest management and as a basis for development of insect control agents employing the rational/structural design approaches.

Keywords

Neurosecretory Cell Diuretic Hormone Eclosion Hormone Insect Control Agent Arch Insect 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Hauser F, Cazzamali G, Williamson M et al. A review of neurohormone GPCRs present in the fruitfly Drosophila melanogaster and the honey bee Apis mellifera. Prog Neurobiol 2006; 80:1–19.PubMedCrossRefGoogle Scholar
  2. 2.
    Johnson EC. Postgenomic approaches to resolve neuropeptide signaling in Drosophila. In: Satake H, ed. Invertebrate Neuropeptides and Hormones: Basic Knowledge and Recent Advances. Trivandrum: Transworld Research Network 2006:179–224.Google Scholar
  3. 3.
    Nässel DR. Neuropeptides in the nervous system of Drosophila and other insects: multiple roles as neuromodulators and neurohormones. Prog Neurobiol 2002; 68:1–84.PubMedCrossRefGoogle Scholar
  4. 4.
    Taghert PH, Veenstra JA. Drosophila neuropeptide signaling. Adv Genet 2003; 49:1–65.PubMedCrossRefGoogle Scholar
  5. 5.
    Hewes RS, Taghert PH. Neuropeptides and neuropeptide receptors in the Drosophila melanogaster genome. Genome Res 2001; 11:1126–1142.PubMedCrossRefGoogle Scholar
  6. 6.
    Hummon AB, Richmond TA, Verleyen P et al. From the genome to the proteome: Uncovering peptides in the Apis brain. Science 2006; 314:647–649.PubMedCrossRefGoogle Scholar
  7. 7.
    Riehle MA, Garczynski SF, Crim JW et al. Neuropeptides and peptide hormones in Anopheles gambiae. Science 2002; 298:172–175.PubMedCrossRefGoogle Scholar
  8. 8.
    Meeusen T, Mertens I, De Loof A et al. G protein-coupled receptors in invertebrates: A state of the art. Int Rev Cytol 2003; 230:189−+.PubMedCrossRefGoogle Scholar
  9. 9.
    Baggerman G, Boonen K, Verleyen P et al. Peptidomic analysis of the larval Drosophila melanogaster central nervous system by two-dimensional capillary liquid chromatography quadrupole time-of-flight mass spectrometry. J Mass Spectrom 2005; 40:250–260.PubMedCrossRefGoogle Scholar
  10. 10.
    Garofalo RS. Genetic analysis of insulin signalling in Drosophila. Trends Endocrinol Metablo 2002; 13:156–162.CrossRefGoogle Scholar
  11. 11.
    Cottrell GA. The first peptide-gated ion channel. J Exp Biol 1997; 200:2377–2386.PubMedGoogle Scholar
  12. 12.
    Predel R, Neupert S, Wicher D et al. Unique accumulation of neuropeptides in an insect: FMRFamide-related peptides in the cockroach, Periplaneta americana. Eur J Neurosci 2004; 20:1499–1513.PubMedCrossRefGoogle Scholar
  13. 13.
    Baggerman G, Cerstiaens A, De Loof A et al. Peptidomics of the larval Drosophila melanogaster central nervous system. J Biol Chem 2002; 277:40368–40374.PubMedCrossRefGoogle Scholar
  14. 14.
    Predel R, Wegener C, Russell WK et al. Peptidomics of CNS-associated neurohemal systems of adult Drosophila melanogaster: A mass spectrometric survey of peptides from individual flies. J Comp Neurol 2004; 474:379–392.PubMedCrossRefGoogle Scholar
  15. 15.
    Predel R, Neupert S, Roth S et al. Tachykinin-related peptide precursors in two cockroach species. FEBS J 2005; 272:3365–3375.PubMedCrossRefGoogle Scholar
  16. 16.
    Altstein M, Dunkelblum E, Gabay T et al. PBAN-Induced sex-pheromone biosynthesis in Heliothis-Peltigera: Structure, dose and time-dependent analysis. Arch Insect Biochem Physiol 1995; 30:307–319.CrossRefGoogle Scholar
  17. 17.
    Altstein M, Gazit Y, Ben Aziz O et al. Induction of cuticular melanization in Spodoptera littoralis larvae by PBAN/MRCH: Development of a quantitative bioassay and structure function analysis. Arch Insect Biochem Physiol 1996; 31:355–370.CrossRefGoogle Scholar
  18. 18.
    Coast GM, Orchard I, Phillips JE et al. Insect diuretic and antidiuretic hormones. Advan In Insect Phys 2002; 29:279–409.CrossRefGoogle Scholar
  19. 19.
    Gäde G. The explosion of structural information on insect neuropeptides. Fortschr Chem Org Naturst 1997; 71:1–128.PubMedGoogle Scholar
  20. 20.
    Gäde G, Goldsworthy GJ. Insect peptide hormones: a selective review of their physiology and potential application for pest control. Pest Manag Sci 2003; 59:1063–1075.PubMedCrossRefGoogle Scholar
  21. 21.
    Nachman RJ, Roberts VA, Lange AB et al. Active conformation and mimetic analog development for the pyrokinin-PBAN-diapause-pupariation and myosuppressin insect neuropeptide families. Phytochemicals for Pest Control 1997; 658:277–291.CrossRefGoogle Scholar
  22. 22.
    Rafaeli A, Jurenka R. PBAN regulation of pheromone biosynthesis in female moths. Insect Pheromone Biochemistry and Molecular Biology. NY: Academic Press, 2003; 107–36.Google Scholar
  23. 23.
    Schoofs L, Vandenbroeck J, Deloof A. The myotropic peptides of Locusta migratoria: Structures, distribution, functions and receptors. Insect Biochem Mol Biol 1993; 23:859–881.PubMedCrossRefGoogle Scholar
  24. 24.
    Vanden Broeck J. Neuropeptides and their precursors in the fruitfly, Drosophila melanogaster. Peptides 2001; 22:241–254.PubMedCrossRefGoogle Scholar
  25. 25.
    Yerushalmi Y, Bhargava K, Gilon C et al. Structure-activity relations of the dark-colour-inducing neurohormone of locusts. Insect Biochem Mol Biol 2002; 32:909–917.PubMedCrossRefGoogle Scholar
  26. 26.
    Nässel DR, Homberg U. Neuropeptides in interneurons of the insect brain. Cell Tissue Res 2006; 326:1–24.PubMedCrossRefGoogle Scholar
  27. 27.
    Ewer J, Reynolds S. Neuropeptide control of molting in insects. In: Pfaff DW, Arnold AP, Fahrbach SE et al, eds. Hormones, Brain and Behavior. San Diego: Academic Press, 2002:1–92.CrossRefGoogle Scholar
  28. 28.
    Kastin A. Handbook of biologically active peptides. San Diego: Elsevier, 2006.Google Scholar
  29. 29.
    Kiss T, Pirger Z. Neuropeptides as modulators and hormones in terrestrial snails: their occurrence, distribution and physiological significance. In: Satake H, ed. Invertebrate Neuropeptides And Hormones: Basic Knowledge and Recent Advances. Transworld Research Network, Trivandrum, 2006:75–110.Google Scholar
  30. 30.
    Nusbaum MP, Blitz DM, Swensen AM et al. The roles of cotransmission in neural network modulation. Trends Neurosci 2001; 24:146–154.PubMedCrossRefGoogle Scholar
  31. 31.
    Strand FL. Neuropeptides: Regulators of Physiological Processes. Cambridge, MA: The MIT Press, 1999.Google Scholar
  32. 32.
    Davis NT, Homberg U, Teal PEA et al. Neuroanatomy and immunocytochemistry of the neurosecretory system of the subesophageal ganglion of the tobacco hawkmoth, Manduca sexta: Immunoreactivity to PBAN and other neuropeptides. Microscopy Res Tech 1996; 35:201–229.CrossRefGoogle Scholar
  33. 33.
    McNabb SL, Baker JD, Agapite J et al. Disruption of a behavioral sequence by targeted death of peptidergic neurons in Drosophila. Neuron 1997; 19:813–823.PubMedCrossRefGoogle Scholar
  34. 34.
    Terhzaz S, Rosay P, Goodwin SF et al. The neuropeptide SIFamide modulates sexual behavior in Drosophila. Biochem Biophys Res Commun 2007; 352:305–310.PubMedCrossRefGoogle Scholar
  35. 35.
    Hill CA, Fox AN, Pitts RJ et al. G protein-coupled receptors in Anopheles gambiae. Science 2002; 298:176–178.PubMedCrossRefGoogle Scholar
  36. 36.
    De Loof A, Baggerman G, Breuer M et al. Gonadotropins in insects: An overview. Arch Insect Biochem Physiol 2001; 47:129–138.PubMedCrossRefGoogle Scholar
  37. 37.
    Schoofs L, Clynen E, Cerstiaens A et al. Newly discovered functions for some myotropic neuropeptides in locusts. Peptides 2001; 22:219–227.PubMedCrossRefGoogle Scholar
  38. 38.
    Broughton SL, Piper MD, Ikeya T et al. Longer lifespan, altered metabolism and stress resistance in Drosophila from ablation of cells making insulin-like ligands. Proc Natl Acad Sci USA 2005; 102:3105–3110.PubMedCrossRefGoogle Scholar
  39. 39.
    Melcher C, Pankratz MJ. Candidate gustatory Interneurons modulating feeding behavior in the Drosophila brain. Plos Biology 2005; 3:1618–1629.CrossRefGoogle Scholar
  40. 40.
    Wu O, Wen T, Lee G et al. Developmental control of foraging and social behavior by the Drosophila neuropeptide Y-like system. Neuron 2003; 39:147–161.PubMedCrossRefGoogle Scholar
  41. 41.
    Wu O, Zhao Z, Shen P. Regulation of aversion to noxious food by Drosophila neuropeptide Y-and insulin-like systems. Nature Neurosci 2005; 8:1350–1355.PubMedCrossRefGoogle Scholar
  42. 42.
    Altstein M. Role of neuropeptides in sex pheromone production in moths. Peptides 2004; 25:1491–1501.PubMedCrossRefGoogle Scholar
  43. 42b.
    Altstein M, Hariton A. Rational design of insect control agents: The PK/PBAN family as a study case. In: Ishaaya I, Horowitz R, eds. Biorational Control of Arthropod Pests: Application and Resistance Management. New York: Springer, 2009:49–81.CrossRefGoogle Scholar
  44. 43.
    Matsumoto S, Isogai A, Suzuki A et al. Purification and properties of the melanization and reddish colouration hormone (MRCH) in the armyworm, Leucania Separata (lepidoptera). Insect Biochem 1981; 11:725–733.CrossRefGoogle Scholar
  45. 44.
    Tanaka S. Endocrine Mechanisms Controlling Body-Color Polymorphism in Locust. In: Loof AD, Hoffman KH, eds. Arch Insect Biochem Physiol 2001; 139-49.Google Scholar
  46. 45.
    Lee G, Park JH. Hemolymph sugar homeostasis and starvation-induced hyperactivity affected by genetic manipulations of the adipokinetic hormone-encoding gene in Drosophila melanogaster. Genetics 2004; 167:311–323.PubMedCrossRefGoogle Scholar
  47. 46.
    Rulifson EJ, Kin SK, Nusse R. Ablation of insulin-producing neurons in flies: growth and diabetic phenotypes. Science 2002; 296:1118–1120.PubMedCrossRefGoogle Scholar
  48. 47.
    Renn SC, Park JH, Rosbash M et al. A pdf neuropeptide gene mutation and ablation of PDF neurons each cause severe abnormalities of behavioral circadian rhythms in Drosophila. Cell 1999; 99:791–802.PubMedCrossRefGoogle Scholar
  49. 48.
    Lee KS, You KH, Choo JK et al. Drosophila short neuropeptide F regulates food intake and body size. J Biol Chem 2004; 279:50781–50789.PubMedCrossRefGoogle Scholar
  50. 49.
    Brown MR, Klowden MJ, Crim JW et al. Endogenous regulation of mosquito host-seeking behavior by a neuropeptide. J Insect Physiol 1994; 40:399–406.CrossRefGoogle Scholar
  51. 50.
    Hökfelt T, Bartfai T, Bloom F. Neuropeptides: opportunities for drug discovery. Lancet Neurol 2003; 2:463–472.PubMedCrossRefGoogle Scholar
  52. 51.
    Quartara L, Altamura M. Tachykinin receptors antagonists: from research to clinic. Curr Drug Targets 2006; 7:975–992.PubMedCrossRefGoogle Scholar
  53. 52.
    Gurrath M. Peptide-binding G protein-coupled receptors: new opportunities for drug design. Curr Med Chem 2001; 8:1605–1648.PubMedGoogle Scholar
  54. 53.
    Zeltser I, Gilon C, Ben-Aziz O et al. Discovery of a linear lead antagonist to the insect pheromone biosynthesis activating neuropeptide (PBAN). Peptides 2000; 21:1457–1465.PubMedCrossRefGoogle Scholar
  55. 54.
    Altstein M, Ben-Aziz O, Daniel S et al. Backbone cyclic peptide antagonists, derived from the insect pheromone biosynthesis activating neuropeptide, inhibit sex pheromone biosynthesis in moths. J Biol Chem 1999; 274:17573–17579.PubMedCrossRefGoogle Scholar
  56. 55.
    Altstein M. Novel insect control agents based on neuropeptide antagonists—The PK/PBAN family as a case study. Journal of Molecular Neuroscience 2003; 22:147–157.CrossRefGoogle Scholar
  57. 56.
    Altstein M, Ben-Aziz O, Zeltser I et al. Inhibition of PK/PBAN-mediated functions in insects: Discovery of selective and nonselective inhibitors. Peptides 2007; 28:574–584.PubMedCrossRefGoogle Scholar
  58. 57.
    Ben-Aziz O, Zeltser I, Bhargava K et al. Backbone cyclic pheromone biosynthesis activating neuropeptide (PBAN) antagonists: Inhibition of melanization in the moth Spodoptera Littoralis (Insecta, Lepidoptera). Peptides 2006; 27:2147–2156.PubMedCrossRefGoogle Scholar
  59. 58.
    Cazzamali G, Torp M, Hauser F et al. The Drosophila gene CG9918 codes for a pyrokinin-1 receptor. Biochem Biophys Res Commun 2005; 335:14–19.PubMedCrossRefGoogle Scholar
  60. 59.
    Choi MY, Fuerst EJ, Rafaeli A et al. Identification of a G protein-coupled receptor for pheromone biosynthesis activating neuropeptide from pheromone glands of the moth Helicoverpa zea. Proc Natl Acad Sci U S A 2003; 100:9721–9726.PubMedCrossRefGoogle Scholar
  61. 60.
    Hull JJ, Ohnishi A, Moto K et al. Cloning and characterization of the pheromone biosynthesis activating neuropeptide receptor from the silkmoth, Bombyx mori—Significance of the carboxyl terminus in receptor internalization. J Biol Chem 2004; 279:51500–51507.PubMedCrossRefGoogle Scholar
  62. 61.
    Zheng L, Lytle C, Njauw C-N et al. Cloning and characterization of the pheromone biosynthesis activating neuropeptide receptor gene in Spodoptera littoralis larvae. Gene 2007; 393:20–30.PubMedCrossRefGoogle Scholar
  63. 62.
    Nachman RJ, Teal PEA, Ujvary I. Comparative topical pheromonotropic activity of insect pyrokinin/ PBAN amphiphilic analogs incorporating different fatty and/or cholic acid components. Peptides 2001; 22:279–285.PubMedCrossRefGoogle Scholar
  64. 63.
    Nachman RJ, Teal PEA, Strey A. Enhanced oral availability/pheromonotropic activity of peptidase-resistant topical amphiphilic analogs of pyrokinin/PBAN insect neuropeptides. Peptides 2002; 23:2035–2043.PubMedCrossRefGoogle Scholar
  65. 64.
    Nachman RJ, Ben-Aziz O, Davidovitch M et al. Biostable b-amino acid PK/PBAN analogs: Agonist and antagonist properties. Peptides 2008; 30:608–615.PubMedCrossRefGoogle Scholar
  66. 65.
    Nachman RJ, Teal PEA, Ben Aziz O et al. An amphiphilic, PK/PBAN analog is a selective pheromonotropic antagonist that penetrates the cuticle of a heliothine insect. Peptides 2009; 30:616–621.PubMedCrossRefGoogle Scholar
  67. 66.
    Hauser F, Cazzamali G, Williamson M et al. A genome-wide inventory of neurohormone GPCRs in the red flour beetle Tribolium castaneum. Front Neuroendocrinol 2008; 29:142–165.PubMedCrossRefGoogle Scholar
  68. 67.
    Roller L, Yamanaka N, Watanabe K et al. The unique evolution of neuropeptide genes in the silkworm Bombyx mori. Insect Biochem Mol Biol 2008; 38:1147–1157.PubMedCrossRefGoogle Scholar
  69. 68.
    Yamanaka N, Yamamoto S, Zitnan D et al. Neuropeptide receptor transcriptome reveals unidentified neuroendocrine pathways. PLoS ONE 2008; 3:e3048.PubMedCrossRefGoogle Scholar
  70. 69.
    Brockmann A, Annangudi SP, Richmond TA et al. Quantitative peptidomics reveal brain peptide signatures of behavior. Proc Natl Acad Sci USA 2009; 17;106:2383–2388.CrossRefGoogle Scholar
  71. 70.
    Yew JY, Wang Y, Barteneva N et al. Analysis of neuropeptide expression and localization in adult Drosophila melanogaster central nervous system by affinity cell-capture mass spectrometry. J Proteome Res 2009; 8:1271–1284.PubMedCrossRefGoogle Scholar
  72. 71.
    Chang JC, Yang RB, Adams ME, Lu KH. Receptor guanylyl cyclases in Inka cells targeted by eclosion hormone. Proc Natl Acad Sci USA 2009; 106:13371–13376.PubMedCrossRefGoogle Scholar
  73. 72.
    Barnes AI, Wigby S, Boone JM et al. Feeding, fecundity and lifespan in female Drosophila melanogaster. Proc Biol Sci 2008; 275:1675–1683.PubMedCrossRefGoogle Scholar
  74. 73.
    Broughton S, Partridge L. Insulin/IGF-like signalling, the central nervous system and aging. Biochem J 2009; 418:1–12.PubMedCrossRefGoogle Scholar
  75. 74.
    Giannakou ME, Partridge L. Role of insulin-like signalling in Drosophila lifespan. Trends Biochem Sci 2007; 32:180–188.PubMedCrossRefGoogle Scholar
  76. 75.
    Hariton A, Ben-Aziz O, Davidovitch M et al. Bioavailability of insect neuropeptides: The PK/PBAN family as a case study. Peptides 2009a; 30:1034–1041.PubMedCrossRefGoogle Scholar
  77. 76.
    Hariton A, Ben-Aziz O, Davidovitch M et al. Bioavailability of b-amino acid and C-terminally derived PK/PBAN analogs. Peptides 2009b; 30:2174–2181PubMedCrossRefGoogle Scholar
  78. 77.
    Hariton A, Ben Aziz O, Davidovitch M, Altstein M. Bioavailability of backbone cyclic PK/PBAN antagonists: inhibition of sex pheromone biosynthesis elicited by the natural mechanism in Heliothis peltigera females. FEBS J 2010; 277:1035–1044.PubMedCrossRefGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2010

Authors and Affiliations

  1. 1.Department of EntomologyThe Volcani CenterBet DaganIsrael
  2. 2.Department of ZoologyStockholm UniversityStockholmSweden

Personalised recommendations