Skip to main content
SpringerLink
Log in

The hypertrehalosaemic neuropeptide conformational twins of cicadas consist of only l-amino acids: are they cis–trans isomers?

  • Original Article
  • Published:
Amino Acids Aims and scope Submit manuscript

Abstract

It is known for almost 25 years that the corpora cardiaca (neurosecretory glands) of cicadas synthesize two isobaric peptides with hypertrehalosaemic activity denominated Placa-HrTH-I and II. Both decapeptides have the same amino acid sequence (pGlu-Val-Asn-Phe-Ser-Pro-Ser-Trp-Gly-Asn amide) and mass, but differ in their chromatographic retention time. The slightly more hydrophobic peptide, Placa-HrTH-II, co-elutes with the synthetic peptide of the same sequence and is less active in biological assays than Placa-HrTH-I. Ion mobility separation in conjunction with high-resolution mass spectrometry detected the differing structural feature between both peptides in the region Pro6-Ser7-Trp8. Here, it was shown that Placa-HrTH-I co-eluted with a synthetic peptide containing d-Pro in position 6, while dextrorotatory amino acid residues in positions 7 and 8 could be excluded in this way. Amino acid hydrolysis followed by chiral analysis using a relative of Marfey’s reagent was then used to validate the presence of d-Pro in Placa-HrTH-I. Interestingly, this experiment unambiguously proved both the absence of d-Pro and the presence of l-Pro in Placa-HrTH-I. Racemization as a reason for the structural differences of the twin adipokinetic hormones was hence ruled out and cis–trans isomerism as the likely alternative came into focus. It remains to be investigated if Pro6 in cis-conformation is indeed present and responsible for the increased bioactivity of Placa-HrTH-I.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

AKH:

Adipokinetic hormone

MS:

Mass spectrometry

RP-LC:

Reversed-phase liquid chromatography

RT:

Retention time

CC:

Corpora cardiaca

FA:

Formic acid

ACN:

Acetonitrile

MeOH:

Methanol

l-FDVA:

Nα-(2,4-Dinitro-5-fluorophenyl)-l-valine amide

References

  • Abdullah ZS, Butt TM (2015) Preferences of the peripheral olfactory system of Western Flower Thrips, Frankliniella occidentalis towards stereoisomers of common plant volatiles. Chemoecology 25:47–51

    Article  CAS  PubMed  Google Scholar 

  • B’Hymer C, Montes-Bayon M, Caruso JA (2003) Marfey’s reagent: past, present, and future uses of 1-fluoro-2,4-dinitrophenyl-5-l-alanine amide. J Sep Sci 26:7–19

    Article  Google Scholar 

  • Bhushan R, Kumar R (2009) Analysis of multicomponent mixture and simultaneous enantioresolution of proteinogenic and non-proteinogenic amino acids by reversed-phase high-performance liquid chromatography using chiral variants of Sanger’s reagent. Anal Bioanal Chem 394:1697–1705

    Article  CAS  PubMed  Google Scholar 

  • Coste F, Kemp C, Bobezeau V, Hetru C, Kellenberger C, Imler J-L, Roussel A (2012) Crystal structure of Diedel, a marker of the immune response of Drosophila melanogaster. PLoS One 7:e33416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Counterman AE, Clemmer DE (2002) Cis–trans signatures of proline-containing tryptic peptides in the gas phase. Anal Chem 74:1946–1951

    Article  CAS  PubMed  Google Scholar 

  • Craveur P, Joseph AP, Poulain P, de Brevern AG, Rebehmed J (2013) Cis–trans isomerization of omega dihedrals in proteins. Amino Acids 45:279–289

    Article  CAS  PubMed  Google Scholar 

  • Davis TL, Liu AC, Partch CL (2017) A slow conformational switch in the BMAL1 transactivation domain modulates circadian rhythms. Mol Cell 66:447–457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gäde G (2004) Regulation of intermediary metabolism and water balance of insects by neuropeptides. Ann Rev Entomol 49:93–113

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Gäde G, Janssens MPE (1994) Cicadas contain novel members of the AKH/RPCH family peptides with hypertrehalosaemic activity. Biol Chem Hoppe Seyler 375:803–809

    Article  PubMed  Google Scholar 

  • Gäde G, Goldsworthy GJ, Kegel G, Keller R (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-Seyler’s Z Physiol Chem 365:393–398

    Article  PubMed  Google Scholar 

  • Gäde G, Hoffmann KH, Spring JH (1997) Hormonal regulation in insects: facts, gaps, and future directions. Physiol Rev 77:963–1032

    Article  PubMed  Google Scholar 

  • Gäde G, Šimek P, Marco HG (2015) Two novel tyrosine-containing peptides (Tyr4) of the adipokineic hormone family in beetles of the families Coccinellidae and Silphidae. Amino Acids 47:2323–2333

    Article  CAS  PubMed  Google Scholar 

  • Glover MS, Bellinger EP, Radivojac P, Clemmer DE (2015) Penultimate proline in neuropeptides. Anal Chem 87:8466–8472

    Article  CAS  PubMed  Google Scholar 

  • Gustafson CL, Parsley NC, Aimgil H, Lee H-W, Ahlbach C, Michael AK, Xu H, Williams OL, Davis HG, McDonough LM, Burditt AK Jr, Bierl-Leonhardt BA (1984) Filbertworm sex pheromone. Identification and field tests of (E,E)- and (E,Z)-8,10-dodecadien-1-ol acetates. J Chem Ecol 10:53–61

    Article  Google Scholar 

  • König S, Marco H, Gäde G (2017a) The hypertrehalosemic neuropeptides of cicadas are structural isomers - evidence by ion mobility mass spectrometry. Anal Bioanal Chem 409:6415–6420

    Article  CAS  PubMed  Google Scholar 

  • König S, Marco H, Gäde G (2017b) d-Proline—comment to “An overview on d-amino acids”. Amino Acids 50:359–361

    Article  CAS  PubMed  Google Scholar 

  • Munte CE, Gäde G, Domogolla B, Kremer W, Kellner R, Kalbitzer HR (2008) C-mannosylation in the hypertrehalosaemic hormone from the stick insect Carausius morosus. FEBS J 275:1163–1173

    Article  CAS  PubMed  Google Scholar 

  • Quistad GB, Staiger LE, Schooley DA (1975) Environmental degradation of the insect growth regulator methoprene (isopropyl (2E,4E)-11-methoxy-3,7,11-trimethyl-2,4-dodecadienoate) III. Photodecomposition. J Agric Food Chem 23:299–303

    Article  CAS  Google Scholar 

  • Raina A, Pannell L, Kochansky J, Jaffe H (1995) Primary structure of a novel neuropeptide isolated from the corpora cardiaca of periodical cicadas having adipokinetic and hypertrehalosemic activities. Insect Biochem Mol Biol 25:929–932

    Article  CAS  PubMed  Google Scholar 

  • Schmid FX (2002) Prolyl isomerases. Adv Protein Chem 59:243–282

    Article  CAS  Google Scholar 

  • Shukolyukov SA, Denisova NA (1992) Opsin biosynthesis and trans-cis isomerization of aldehyde form chromophore in the blowfly Calliphora erythrocephala eye. Insect Biochem Mol Biol 22:925–935

    Article  CAS  Google Scholar 

  • Veenstra JA, Hagedorn HH (1995) Isolation of two AKH-related peptides from cicadas. Arch Insect Biochem Physiol 29:391–396

    Article  CAS  PubMed  Google Scholar 

  • Voolstra O, Oberhauser V, Sumser E, Meyer NE, Maguire ME, Huber A, von Lintig J (2010) NinaB is essential for Drosophila vision but induces retinal degeneration in opsin-deficient photoreceptors. J Biol Chem 285:2130–2139

    Article  CAS  PubMed  Google Scholar 

  • Witzgall P, Bengtsson M, Unelius CR, Loefqvist J (1993) Attraction of pea moth Cydia nigricana F. (Lepidoptera: Tortricidae) to female sex pheromone (E,E)-8,10-dodecadien-1-yl acetate, is inhibited by geometric isomers E,Z, Z,E, and Z,Z. J Chem Ecol 19:1917–1928

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Author notes

  1. Simone König and Malte Bayer share the first authorship.

Authors and Affiliations

  1. IZKF Core Unit Proteomics, Interdisciplinary Center for Clinical Research, University of Münster, Röntgenstr. 21, 48149, Münster, Germany

    Simone König & Malte Bayer

  2. Department of Biological Sciences, University of Cape Town, Cape Town, South Africa

    Heather Marco & Gerd Gäde

Authors
  1. Simone König
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Malte Bayer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Heather Marco
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gerd Gäde
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Simone König.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

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.

Additional information

Handling Editor: V. Soloshonok.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 180 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

König, S., Bayer, M., Marco, H. et al. The hypertrehalosaemic neuropeptide conformational twins of cicadas consist of only l-amino acids: are they cis–trans isomers?. Amino Acids 51, 1023–1028 (2019). https://doi.org/10.1007/s00726-019-02742-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00726-019-02742-1

Keywords

Search

Navigation