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Two novel tyrosine-containing peptides (Tyr4) of the adipokinetic hormone family in beetles of the families Coccinellidae and Silphidae

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Abstract

Novel members of the adipokinetic hormone family of peptides have been identified from the corpora cardiaca (CC) of two species of beetles representing two families, the Silphidae and the Coccinellidae. A crude CC extract (0.3 gland equivalents) of the burying beetle, Nicrophorus vespilloides, was active in mobilizing trehalose in a heterologous assay using the cockroach Periplaneta americana, whereas the CC extract (0.5 gland equivalents) of the ladybird beetle, Harmonia axyridis, exhibited no hypertrehalosemic activity. Primary sequences of one adipokinetic hormone from each species were elucidated by liquid chromatography coupled to electrospray mass spectrometry (LC–MS). The multiple MSN electrospray mass data revealed an octapeptide with an unusual tyrosine residue at position 4 for each species: pGlu-Leu-Thr-Tyr-Ser-Thr-Gly-Trp amide for N. vespilloides (code-named Nicve-AKH) and pGlu-Ile-Asn-Tyr-Ser-Thr-Gly-Trp amide for H. axyridis (code-named Harax-AKH). Assignment of the correct sequences was confirmed by synthesis of the peptides and co-elution in reversed-phase high-performance liquid chromatography with fluorescence detection or by LC–MS. Moreover, synthetic peptides were shown to be active in the heterologous cockroach assay system, but Harax-AKH only at a dose of 30 pmol, which explains the negative result with the crude CC extract. It appears that the tyrosine residue at position 4 can be used as a diagnostic feature for certain beetle adipokinetic peptides, because this feature has not been found in another order other than Coleoptera.

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References

  • Gäde G (1980) Further characteristics of adipokinetic and hyperglycaemic factor(s) of stick insects. J Insect Physiol 26:351–360

    Article  Google Scholar 

  • Gäde G (1985) Isolation of the hypertrehalosaemic factors I and II from the corpus cardiacum of the Indian stick insect, Carausius morosus, by reversed-phase high performance liquid chromatography, and amino acid composition of factor II. Biol Chem Hoppe Seyler 366:195–199

    Article  PubMed  Google Scholar 

  • Gäde G (1991a) A unique charged tyrosine-containing member of the adipokinetic hormone/red-pigment-concentrating hormone peptide family isolated and sequenced from two beetle species. Biochem J 275:671–677

    Article  PubMed Central  PubMed  Google Scholar 

  • Gäde G (1991b) The adipokinetic neuropeptide of Mantodea. Sequence elucidation and evolutionary relationships. Biol Chem Hoppe Seyler 372:193–201

    Article  PubMed  Google Scholar 

  • Gäde G (1992) Structure-activity relationships for the carbohydrate-mobilizing action of further bioanalogues of the adipokinetic hormone/red pigment-concentrating hormone family of peptides. J Insect Physiol 38:259–266

    Article  Google Scholar 

  • Gäde G (1995) Isolation and identification of AKH/RPCH family peptides in blister beetles (Meloidae). Physiol Entomol 20:45–51

    Article  Google Scholar 

  • Gäde G (1997a) The explosion of structural information on insect neuropeptides. In: Herz W, Kirby GW, Moore RE, Steglich W, Tamm CH (eds) Progress in the chemistry of organic natural products, vol 71. Springer, New York, pp 1–128

    Google Scholar 

  • Gäde G (1997b) Distinct sequences of AKH/RPCH family members in beetle (Scarabaeus-species) corpus cardiacum contain three aromatic amino acid residues. Biochem Biophys Res Commun 230:16–21

    Article  PubMed  Google Scholar 

  • Gäde G (1997c) Hyperprolinaemia caused by novel members of the adipokinetic hormone/red pigment-concentrating hormone family of peptides isolated from corpora cardiaca of onitine beetles. Biochem J 321:201–206

    Article  PubMed Central  PubMed  Google Scholar 

  • Gäde G (1997d) Sequences of recently identified adipokinetic peptides: what do they tell us with respect to their hyperlipaemic activity in migratory locusts? Inv Neurosci 3:217–222

    Article  Google Scholar 

  • Gäde G (1999) Control of proline as flight substrate in longhorned and leaf beetles by AKH/RPCH neuropeptides. In: Vaudry H, Roubos E, Wendelaar Bonga SE et al (eds) Recent developments in comparative endocrinology and neurobiology. Shaker Publishing, Maastricht, pp 308–310

    Google Scholar 

  • Gäde G (2009) Peptides of the adipokinetic hormone/red pigment-concentrating hormone family. A new take on biodiversity. Ann NY Acad Sci 1163:125–136

    Article  PubMed  Google Scholar 

  • Gäde G, Auerswald L (2002) Beetles’ choice-proline for energy output: control by AKHs. Comp Biochem Physiol 132B:117–129

    Article  Google Scholar 

  • Gäde G, Auerswald L (2003) Mode of action of neuropeptides from the adipokinetic hormone family. Gen Comp Endocrinol 132:10–20

    Article  PubMed  Google Scholar 

  • Gäde G, Kellner R (1989) The metabolic neuropeptides of the corpus cardiacum from the potato beetle and the American cockroach are identical. Peptides 10:1287–1289

    Article  PubMed  Google Scholar 

  • Gäde G, Marco HG (2006) Structure, function and mode of action of select arthropod neuropeptides. In: Rahman AU (ed) Studies in natural products chemistry. Bioactive Natural Products (Part M), vol 33. Elsevier, Amsterdam, pp 69–139

  • Gäde G, Marco HG (2011) The adipokinetic hormone family in Chrysomeloidea: structural and functional considerations. ZooKeys 157:81–94

    Article  PubMed  Google Scholar 

  • Gäde G, Rosinski G (1990) The primary structure of the hypertrehalosaemic neuropeptide from tenebrionid beetles: a novel member of the AKH/RPCH family. Peptides 11:455–459

    Article  PubMed  Google Scholar 

  • Gäde G, Šimek P (2010) A novel member of the adipokinetic peptide family in a living fossil, the ice crawler Galloisiana yuasai, is the first identified neuropeptide from the order Grylloblattodea. Peptides 31:372–376

    Article  PubMed  Google Scholar 

  • Gäde G, Goldsworthy GJ, Kegel G et al (1984) Single step purification of locust adipokinetic hormones I and II by reversed phase high-performance liquid chromatography and the amino acid composition of the hormone II. Hoppe Seylers Z physiol Chem 365:393–398

    Article  PubMed  Google Scholar 

  • Gäde G, Auerswald L, Šimek P et al (2003) Red pigment-concentrating hormone is not limited to crustaceans. Biochem Biophys Res Commun 309:972–978

    Google Scholar 

  • Gäde G, Šimek P, Clark KD et al (2006) Unique translational modification of an invertebrate neuropeptide: a phosphorylated member of the adipokinetic hormone peptide family. Biochem J 393:705–713

    Article  PubMed Central  PubMed  Google Scholar 

  • Gäde G, Marco HG, Šimek P et al (2008) Predicted versus expressed adipokinetic hormones, and other small peptides from the corpus cardiacum-corpus allatum: a case study with beetles and moths. Peptides 29:1124–1139

    Article  PubMed  Google Scholar 

  • Gäde G, Simek P, Marco HG (2009) The first identified neuropeptide in the insect order Megaloptera: a novel member of the adipokinetic hormone family in the alderfly Sialis lutaria. Peptides 30:477–482

    Article  PubMed  Google Scholar 

  • Gäde G, Šimek P, Marco HG (2011) An invertebrate [hydroxyproline]-modified neuropeptide: further evidence for a close evolutionary relationship between insect adipokinetic hormone and mammalian gonadotropin hormone family. Biochem Biophys Res Commun 414:592–597

    Article  PubMed  Google Scholar 

  • Gäde G, Šimek P, Clark KD et al (2013) Five functional adipokinetic peptides expressed in the corpus cardiacum of the moth genus Hippotion (Lepidoptera, Sphingidae). Regul Pept 184:85–95

    Article  PubMed  Google Scholar 

  • Goldsworthy G, Opoku-Ware K, Mullen L (2002) Adipokinetic hormone enhances laminarin and bacterial lipopolysaccharide-induced activation of the prophenoloxidase cascade in the African migratory locust, Locusta migratoria. J Insect Physiol 48:601–608

    Article  CAS  PubMed  Google Scholar 

  • Gullan PJ, Cranston PS (2010) The insects. An outline of entomology. Blackwell, Chichester

    Google Scholar 

  • Haberer W, Steiger S, Müller JK (2014) Dynamic changes in volatile emissions of breeding burying beetles. Physiol Entomol 39:153–164

    Article  CAS  Google Scholar 

  • Koch RL, Galvan TL (2008) Bad side of a good beetle: the North American experience with Harmonia axyridis. BioControl 53:23–35

    Article  Google Scholar 

  • Kodrik D, Socha R, Šimek P et al (2000) A new member of the AKH/RPCH family that stimulates locomotory activity in the firebug, Pyrrhocoris apterus (Heteroptera). Insect Biochem Mol Biol 30:489–498

    Article  CAS  PubMed  Google Scholar 

  • Kodrik D, Marco HG, Šimek P et al (2010) The adipokinetic hormones of Heteroptera: a comparative study. Physiol Entomol 35:117–127

    Article  CAS  Google Scholar 

  • Lindemans M, Liu F, Janssen T et al (2009) Adipokinetic hormone signalling through the gonadotropin-releasing hormone receptor modulates egg-laying in Caenorhabditis elegans. Proc Natl Acad Sci USA 106:1642–1647

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Magro A, Lecompte E, Magné F et al (2010) Phylogeny of ladybirds (Coleoptera: Coccinellidae): are the subfamilies monophyletic? Mol Phylogenet Evol 54:833–848

    Article  CAS  PubMed  Google Scholar 

  • Marco HG, Šimek P, Gäde G (2011) The first decapeptide adipokinetic hormone (AKH) in Heteroptera: a novel AKH from a South African saucer bug, Laccocoris spurcus (Naucoridae, Laccocorinae). Peptides 32:454–460

    Article  CAS  PubMed  Google Scholar 

  • Marco HG, Šimek P, Clark KD et al (2013) Novel adipokinetic hormones in the kissing bugs Rhodnius prolixus, Triatoma infestans, Dipetalogaster maxima and Panstrongylus megistus. Peptides 41:21–30

    Article  CAS  PubMed  Google Scholar 

  • Neupert S (2007) Novel members of the AKH/RPCH peptide family: isolation of AKH from the corpora cardiaca of the two beetle species, Cheilomenes lunata and Coccinella septempunctata. Pestycydy 3–4:39–43

    Google Scholar 

  • O’Shea M, Rayne RC (1992) Adipokinetic hormones: cell and molecular biology. Experentia 48:430–438

    Article  Google Scholar 

  • Roch GJ, Bushby ER, Sherwood NM (2011) Evolution of GnRH: diving deeper. Gen Comp Endocrinol 171:1–16

    Article  CAS  PubMed  Google Scholar 

  • Scarborough RM, Jamieson GC, Kalish F et al (1984) Isolation and primary structure of two peptides with cardioacceleratory and hyperglycemic activity from the corpora cardiaca of Periplaneta americana. Proc Natl Acad Sci USA 81:5575–5579

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Stals R, Prinsloo G (2007) Discovery of an alien invasive, predatory insect in South Africa: the multi-coloured Asian ladybird beetle, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). South African J of Sci 103:123–126

    Google Scholar 

  • Staubli F, Jørgensen TJD, Cazzamali G et al (2002) Molecular identification of the insect adipokinetic hormone receptors. Proc Natl Acad Sci USA 99:3446–3451

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Steiger S, Peschke K, Francke W et al (2007) The smell of parents: breeding status influences cuticular hydrocarbon pattern in the burying beetle Nicrophorus vespilloides. Proc Royal Soc B 274:2211–2220

    Article  CAS  Google Scholar 

  • Urbanski A, Czarniewska E, Baraniak E et al (2014) Developmental changes in the cellular and humoral responses of the burying beetle Nicrophorus vespilloides (Coleoptera, Silphidae). J Insect Physiol 60:98–103

    Article  CAS  PubMed  Google Scholar 

  • Vilcinskas A, Mukherjee K, Vogel H (2012) Expansion of the antimicrobial peptide repertoire in the invasive ladybird Harmonia axyridis. Proc R Soc B 280:20122113

    Article  Google Scholar 

  • Vilcinskas A, Stoecker K, Schmidtberg H et al (2013) Invasive harlequin ladybird carries biological weapons against native competitors. Science 340:862–863

    Article  CAS  PubMed  Google Scholar 

  • Weaver RJ, Marco HG, Šimek P et al (2012) Adipokinetic hormones (AKHs) of sphingid Lepidoptera, including the identification of a second M. sexta AKH. Peptides 34:44–50

    Article  CAS  PubMed  Google Scholar 

  • Witten JL, Schaffer MH, O’Shea M et al (1984) Structures of two cockroach neuropeptides assigned by fast atom bombardment mass spectrometry. Biochem Biophys Res Commun 124:350–358

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was financially supported by funds from the National Research Foundation [Pretoria, South Africa; Grant No. 85768 (IFR13020116790) to GG and IFR2011033100049 to HGM], by staff awards from the Research Council of the University of Cape Town (to GG and HGM) and funds from the Czech Science Foundation (No. 13-18509S to PS). We thank Dr Sandra Steiger (Institute of Experimental Ecology, University of Ulm, Germany), Mr Mike Alsopp (Agricultural Research Council in Stellenbosch, South Africa) and Ms Ingrid A. Minnaar (Center of Excellence for Invasion Biology, University of Stellenbosch, S. Africa) for supplying us with insects. We also acknowledge the assistance of Ms Alukhanyo Xonti in some of the bioassays.

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The authors declare that they have no conflict of interest.

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All applicable international, national and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors.

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Gäde, G., Šimek, P. & Marco, H.G. Two novel tyrosine-containing peptides (Tyr4) of the adipokinetic hormone family in beetles of the families Coccinellidae and Silphidae. Amino Acids 47, 2323–2333 (2015). https://doi.org/10.1007/s00726-015-2011-4

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