The Adipokinetic Peptides in Diptera: Structure, Function, and Evolutionary Trends
Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
32296388
PubMed Central
PMC7136388
DOI
10.3389/fendo.2020.00153
Knihovny.cz E-zdroje
- Klíčová slova
- adipokinetic and hypertrahalosemic biological assays, adipokinetic peptides, diptera, fly phylogeny, mass spectrometry,
- MeSH
- chromatografie kapalinová MeSH
- Diptera chemie klasifikace genetika metabolismus MeSH
- hmotnostní spektrometrie MeSH
- hmyzí hormony analýza chemie genetika metabolismus MeSH
- kyselina pyrrolidonkarboxylová analogy a deriváty analýza chemie metabolismus MeSH
- molekulární evoluce * MeSH
- oligopeptidy analýza chemie genetika metabolismus MeSH
- peptidy analýza chemie genetika metabolismus MeSH
- sekvence aminokyselin MeSH
- vztahy mezi strukturou a aktivitou MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- adipokinetic hormone MeSH Prohlížeč
- hmyzí hormony MeSH
- kyselina pyrrolidonkarboxylová MeSH
- oligopeptidy MeSH
- peptidy MeSH
Nineteen species of various families of the order Diptera and one species from the order Mecoptera are investigated with mass spectrometry for the presence and primary structure of putative adipokinetic hormones (AKHs). Additionally, the peptide structure of putative AKHs in other Diptera are deduced from data mining of publicly available genomic or transcriptomic data. The study aims to demonstrate the structural biodiversity of AKHs in this insect order and also possible evolutionary trends. Sequence analysis of AKHs is achieved by liquid chromatography coupled to mass spectrometry. The corpora cardiaca of almost all dipteran species contain AKH octapeptides, a decapeptide is an exception found only in one species. In general, the dipteran AKHs are order-specific- they are not found in any other insect order with two exceptions only. Four novel AKHs are revealed by mass spectrometry: two in the basal infraorder of Tipulomorpha and two in the brachyceran family Syrphidae. Data mining revealed another four novel AKHs: one in various species of the infraorder Culicumorpha, one in the brachyceran superfamily Asiloidea, one in the family Diopsidae and in a Drosophilidae species, and the last of the novel AKHs is found in yet another Drosophila. In general, there is quite a biodiversity in the lower Diptera, whereas the majority of the cyclorraphan Brachycera produce the octapeptide Phote-HrTH. A hypothetical molecular peptide evolution of dipteran AKHs is suggested to start with an ancestral AKH, such as Glomo-AKH, from which all other AKHs in Diptera to date can evolve via point mutation of one of the base triplets, with one exception.
Biology Centre Czech Academy of Sciences Ceské Budejovice Czechia
Department of Biological Sciences University of Cape Town Cape Town South Africa
Zobrazit více v PubMed
Khamesipour F, Lankarani KB, Honarvar B, Kwenti TE. A systematic review of human pathogens carried by the housefly (Musca domestica L.). BMC Public Health. (2018) 18:1049. 10.1186/s12889-018-5934-3 PubMed DOI PMC
Cheng TC. General Parasitology. České Budějovice: Elsevier Science. (2012). p. 660.
Ssymank A, Kearns CA, Pape T, Thompson FC. Pollinating flies (Diptera): a major contribution to plant diversity and agricultural production. Biodiversity. (2008) 9:86–9. 10.1080/14888386.2008.9712892 DOI
Yakovlev AY, Kruglikova AA, Chernysh SI. Calliphoridae flies in medical biotechnology. Entomol Rev. (2019) 99:292–301. 10.1134/S0013873819030023 DOI
Rumpold BA, Schlüter OK. Potential and challenges of insects as an innovative source for food and feed production. Innovat Food Sci Emerg Technol. (2013) 17:1–11. 10.1016/j.ifset.2012.11.005 DOI
Joseph I, Mathew DG, Sathyan P, Vargheese G. The use of insects in forensic investigations: an overview on the scope of forensic entomology. J Foren Dental Sci. (2011) 3:89–91. 10.4103/0975-1475.92154 PubMed DOI PMC
Grimaldi D, Engel MS. Evolution of the Insects. New York, NY: Cambridge University Press; (2005).
Wiegmann BM, Trautwein MD, Winkler IS, Barr NB, Kim J-W, Lambkin C, et al. . Episodic radiations in the fly tree of life. Proc Natl Acad Sci USA. (2011) 108:5690–5. 10.1073/pnas.1012675108 PubMed DOI PMC
Gäde G. The hypertrehalosaemic peptides of cockroaches: a phylogenetic study. Gen Compar Endocrinol. (1989) 75:287–300. 10.1016/0016-6480(89)90082-8 PubMed DOI
Gäde G, Marco HG. The adipokinetic hormones of Odonata: a phylogenetic approach. J Insect Physiol. (2005) 51:333–41. 10.1016/j.jinsphys.2004.12.011 PubMed DOI
Marco HG, Šimek P, Gäde G. Adipokinetic hormones of the two extant apterygotan insect orders, Archaeognatha and Zygentoma. J Insect Physiol. (2014) 60, 17–24. 10.1016/j.jinsphys.2013.11.002 PubMed DOI
Gäde G, Marco HG. The adipokinetic hormone of the coleopteran suborder Adephaga: Structure, function, and comparison of distribution in other insects. Arch Insect Biochem Physiol. (2017) 95:e21399. 10.1002/arch.21399 PubMed DOI
Gäde G, Marco HG, Desutter-Grandcolas L. A phylogenetic analysis of the adipokinetic neuropeptides of Ensifera. Physiol Entomol. (2003) 28:283–9. 10.1111/j.1365-3032.2003.00344.x DOI
Hansen KK, Stafflinger E, Schneider M, Hauser F, Cazzamali G, Williamson M, et al. . Discovery of a novel insect neuropeptide signaling system closely related to the insect adipokinetic hormone and corazonin hormonal systems. J Biol Chem. (2010) 285:10736–47. 10.1074/jbc.M109.045369 PubMed DOI PMC
Roch GJ, Busby ER, Sherwood NM. Evolution of GnRH: diving deeper. Gen Comp Endocrinol. (2011) 171:1–16. 10.1016/j.ygcen.2010.12.014 PubMed DOI
Gäde G, Šimek P, Marco HG. 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. (2011) 414:592–7. 10.1016/j.bbrc.2011.09.127 PubMed DOI
Gäde G. Peptides of the adipokinetic hormone/red pigment-concentrating hormone family. A new take on biodiversity. Ann N Y Acad Sci. (2009) 1163:125–36. 10.1111/j.1749-6632.2008.03625.x PubMed DOI
Marco H, Gäde G. Chapter 3: Adipokinetic hormone: a hormone for all seasons? In: Saleuddin S, Lange AB, Orchard I, editors. Advances in Invertebrate (Neuro)Endocrinology: A Collection of Reviews in the Post-Genomic Era, Vol 2. Burlington, ON; Palm Bay, FL: Apple Academic Press; (2020). p. 129–175.
Jaffe H, Raina AK, Riley CT, Fraser BA, Nachman RJ, Vogel VW, et al. . Primary structure of two neuropeptide hormones with adipokinetic and hypotrehalosemic activity isolated from the corpora cardiaca of horse flies (Diptera). Proc Natl Acad Sci USA. (1989) 86:8161–4. 10.1073/pnas.86.20.8161 PubMed DOI PMC
Woodring J, Leprince DJ. The function of corpus cardiacum peptides in horse flies. J Insect Physiol. (1992) 38:775–82. 10.1016/0022-1910(92)90030-H DOI
Gäde G, Wilps H, Kellner R. Isolation and structure of a novel charged member of the red–pigment-concentrating hormone-adipokinetic hormone family of peptides isolated from the corpora cardiaca of the blowfly Phormia terraenovae (Diptera). Biochem J. (1990) 269:309–13. 10.1042/bj2690309 PubMed DOI PMC
Wilps H, Gäde G. Hormonal regulation of carbohydrate metabolism in the blowfly Phormia terraenovae. J Insect Physiol. (1990) 36:441–50. 10.1016/0022-1910(90)90062-K DOI
Schaffer MH, Noyes BE, Slaughter CA, Thorne GC, Gaskell SJ. The fruitfly Drosophila melanogaster contains a novel charged adipokinetic-hormone-family peptide. Biochem J. (1990) 269:315–20. 10.1042/bj2690315 PubMed DOI PMC
Noyes BE, Katz FN, Schaffer MH. Identification and expression of the Drosophila adipokinetic hormone gene. Mol Cell Endocrinol. (1995) 109:133–41. 10.1016/0303-7207(95)03492-P PubMed DOI
Kaufmann C, Merzendorfer H, Gäde G. The adipokinetic hormone system in Culicinae (Diptera: Culicidae): molecular identification and characterization of two adipokinetic hormone (AKH) precursors from Aedes aegypti and Culex pipiens and two putative AKH receptor variants from A. aegypti. Insect Biochem Mol Biol. (2009) 39:770–81. 10.1016/j.ibmb.2009.09.002 PubMed DOI
Predel R, Neupert S, Garczynski SF, Crim JW, Brown MR, Russell WK, et al. . Neuropeptidomics of the mosquito Aedes aegypti. J Proteome Res. (2010) 9:2006–15. 10.1021/pr901187p PubMed DOI PMC
Kaufmann C, Brown MR. Adipokinetic hormones in the African malaria mosquito, Anopheles gambiae: identification and expression of genes for two peptides and a putative receptor. Insect Biochem Mol Biol. (2006) 36:466–81. 10.1016/j.ibmb.2006.03.009 PubMed DOI
Vicoso B, Bachtrog D. Numerous transitions of sex chromosomes in Diptera. PLoS Biol. (2015) 13:e1002078. 10.1371/journal.pbio.1002078 PubMed DOI PMC
Wegener C, Köppler K. Peptide profiling of the retrocerebral complex and identification of an adipokinetic hormone and short neuropeptide F peptides in diapausing and non-diapausing cherry fruit flies Rhagoletis cerasi (Diptera: Tephritidae). Mitt Dtsch Ges Allg Angew Ent. (2014) 19:265–8.
Baggerman G, Cerstiaens A, De Loof A, Schoofs L. Peptidomics of the larval Drosophila melanogaster central nervous system. J Biol Chem. (2002) 277:40368–74. 10.1074/jbc.M206257200 PubMed DOI
Baggerman G, Boonen K, Verleyen P, De Loof A, Schoofs L. 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) 40:250–60. 10.1002/jms.744 PubMed DOI
Predel R, Wegener C, Russell WK, Tichy SE, Russell DH, Nachman RJ. Peptidomics of CNS-associated neurohemal systems of adult Drosophila melanogaster: a mass spectrometric survey of peptides from individual flies. J Comp Neurol. (2004) 474:379–92. 10.1002/cne.20145 PubMed DOI
Wegener C, Reinl T, Jansch L, Predel R. Direct mass spectrometric peptide profiling and fragmentation of larval peptide hormone release sites in Drosophila melanogaster reveals tagma-specific peptide expression and differential processing. J Neurochem. (2006) 96:1362–74. 10.1111/j.1471-4159.2005.03634.x PubMed DOI
Drosophila 12 Genomes Consortium, Clark AG, Eisen MB, Smith DR, Bergman CM, Oliver B, et al. Evolution of genes and genomes on the Drosophila phylogeny. Nature. (2007) 450:203–18. 10.1038/nature06341 PubMed DOI
Wegener C, Gorbashov A. Molecular evolution of neuropeptides in the genus Drosophila. Genome Biol. (2008) 9:R131. 10.1186/gb-2008-9-8-r131 PubMed DOI PMC
Attardo GM, Benoit JB, Michalkova V, Yang GX, Roller L, Bohova J, et al. . Analysis of lipolysis underlying lactation in the tsetse fly, Glossina morsitans. Insect Biochem Mol Biol. (2012) 42:360–70. 10.1016/j.ibmb.2012.01.007 PubMed DOI PMC
Caers J, Boonen K, Van Den Abbeele J, Van Rompay L, Schoofs L, Van Hiel MB. Peptidomics of neuropeptidergic tissues of the tsetse fly Glossina morsitans morsitans. J Am Soc Mass Spectrom. (2015) 26:2024–38. 10.1007/s13361-015-1248-1 PubMed DOI
Attardo GM, Abd-Alla AMM, Acosta-Serrano A, Allen JE, Bateta R, Benoit JB, et al. . Comparative genomic analysis of six Glossina genomes, vectors of African trypanosomes. Genome Biol. (2019) 20:1–30. 10.1186/s13059-019-1768-2 PubMed DOI PMC
Audsley N, Matthews HJ, Down RE, Weaver RJ. Neuropeptides associated with the central nervous system of the cabbage root fly, Delia radicum (L.). Peptides. (2011) 32:434–40. 10.1016/j.peptides.2010.08.028 PubMed DOI
Zoephel J, Reiher W, Rexer KH, Kahnt J, Wegener C. Peptidomics of the agriculturally damaging larval stage of the cabbage root fly Delia radicum (Diptera: Anthomyiidae). PLoS ONE. (2012) 7:e41543. 10.1371/journal.pone.0041543 PubMed DOI PMC
Verleyen P, Huybrechts J, Sas F, Clynen E, Baggerman G, De Loof A, et al. . Neuropeptidomics of the grey flesh fly Neobellieria bullata. Biochem Biophys Res Commun. (2004) 316:763–70. 10.1016/j.bbrc.2004.02.115 PubMed DOI
Rahman MM, Neupert S, Predel R. Neuropeptidomics of the Australian sheep blowfly Lucilia cuprina (Wiedemann) and related Diptera. Peptides. (2013) 41:31–7. 10.1016/j.peptides.2012.12.021 PubMed DOI
Inosaki A, Yasuda A, Shinada T, Ohfune Y, Numata H, Shiga S. Mass spectrometric analysis of peptides in brain neurosecretory cells and neurohemal organs in the adult blowfly Protophormia terraenovae. Comp Biochem Physiol A. (2010) 155:190–9. 10.1016/j.cbpa.2009.10.036 PubMed DOI
Stoffolano JG, Jr, Croke K, Chambers J, Gäde G, Solari P, Liscia A. Role of Phote-HrTH. (Phormia terraenovae hypertrehalosemic hormone) in modulating the supercontractile muscles of the crop of adult Phormia regina Meigen. J Insect Physiol. (2014) 71:147–55. 10.1016/j.jinsphys.2014.10.014 PubMed DOI
Gáliková M, Klepsatel P. Obesity and aging in the Drosophila model. Int J Mol Sci. (2018) 19:1896. 10.3390/ijms19071896 PubMed DOI PMC
Riehle MA, Garczynski SF, Crim JW, Hill CA, Brown MR. Neuropeptides and peptide hormones in Anopheles gambiae. Science. (2002) 298:172–5. 10.1126/science.1076827 PubMed DOI
Kaufmann C, Brown MR. Regulation of carbohydrate metabolism and flight performance by a hypertrehalosaemic hormone in the mosquito Anopheles gambiae. J Insect Physiol. (2008) 54:367–77. 10.1016/j.jinsphys.2007.10.007 PubMed DOI PMC
Nene V, Wortman JR, Lawson D, Haas B, Kodira C, Tu ZJ, et al. . Genome sequence of Aedes aegypti, a major arbovirus vector. Science. (2007) 316:1718–23. 10.1126/science.1138878 PubMed DOI PMC
Gäde G, Šimek P, Marco HG. The first identified neuropeptide in the insect order Megaloptera: a novel member of the adipokinetic hormone family in the alderfly Sialis lutaria. Peptides. (2009) 30:477–82. 10.1016/j.peptides.2008.07.022 PubMed DOI
International Glossina Genome Consortium Genome sequence of the tsetse fly (Glossina morsitans): vector of African trypanosomiasis. Science. (2014) 344:380–86. 10.1126/science.1249656 PubMed DOI PMC
Pape T, Blagoderov VA, Mostovski MB. Order Diptera Linnaeus, 1758. Zootaxa. (2011) 3148:222–9. 10.11646/zootaxa.3148.1.42 DOI
Zöllner N, Kirsch K. Über die quantitative Bestimmung von Lipoiden. (Mikromethode) mittels der vielen natürlichen Lipoiden (allen bekannten Plasmalipoiden) gemeinsamen Sulfophosphovanillin-Reaktion. Zeitschrift für die gesamte experimentelle Medizin. (1962) 135:545–61. 10.1007/BF02045455 DOI
Spik G, Montreuil J. Deux causes d‘erreur dans les dosages colorimetriques des oses neutres totaux. Bull Soc Chimie Biol. (1964) 46:739–49. PubMed
Holwerda DA, van Doorn J, Beenakkers AMT. Characterization of the adipokinetic and hyperglycaemic substances from the locust corpus cardiacum. Insect Biochem. (1977) 7:151–7. 10.1016/0020-1790(77)90008-7 DOI
Gäde G, Goldsworthy GJ, Kegel G, Keller R. Single step purification of locust adipokinetic hormones I and II by reversed-phase high-performance liquid-chromatography, and amino acid composition of the hormone II. Hoppe-Seyler's Zeitschrift für Physiologische Chemie. (1984) 365:393–8. 10.1515/bchm2.1984.365.1.393 PubMed DOI
Kodrík D, Marco HG, Šimek P, Socha R, Štys P, Gäde G. The adipokinetic hormones of Heteroptera: a comparative study. Physiol Entomol. (2010) 35:117–127. 10.1111/j.1365-3032.2009.00717.x DOI
Gäde G. The explosion of structural information on insect neuropeptides. In: Herz W, Kirby GW, Moore RE, Steglich W, Tamm CH, editors. Progress in the Chemistry of Organic Natural Products, Vol 71. New York, NY: Springer; (1997). p. 1–128. 10.1007/978-3-7091-6529-4_1 PubMed DOI
Gäde G, Auerswald L, Šimek P, Marco HG, Kodriḱ D. Red pigment-concentrating hormone is not limited to crustaceans. Biochem Biophys Res Commun. (2003) 309:967–73. 10.1016/j.bbrc.2003.08.107 PubMed DOI
Gäde G, Šimek P, Marco HG. Novel members of the adipokinetic hormone family in beetles of the superfamily Scarabaeoidea. Amino Acids. (2016) 48:2785–98. 10.1007/s00726-016-2314-0 PubMed DOI
Marco HG, Gäde G. Structure and function of adipokinetic hormones of the large white butterfly Pieris brassicae. Physiol. Entomol. (2017) 42:103–12. 10.1111/phen.12175 DOI
Gäde G, Šimek P, Marco HG. Structural diversity of adipokinetic hormones in the hyperdiverse coleopteran Cucujiformia. Arch Insect Biochem Physiol. (2019) 2019:e21611 10.1002/arch.21611 PubMed DOI
Gäde G, Marco HG. Peptides of the adipokinetic hormone/red pigment-concentrating hormone family with special emphasis on Caelifera: primary sequences and functional considerations contrasting grasshoppers and locusts. Gen Comp Endocrinol. (2009) 162:59–68. 10.1016/j.ygcen.2008.06.007 PubMed DOI
Wiegmann BM, Trautwein MD, Kim J-W, Cassel BK, Bertone MA, Winterton SL, et al. . Single-copy nuclear genes resolve the phylogeny of the holometabolous insects. BMC Biol. (2009) 7:34. 10.1186/1741-7007-7-34 PubMed DOI PMC
Gäde G, Simek P, Fescemyer HW. Adipokinetic hormones provide inference for the phylogeny of Odonata. J Insect Physiol. (2011) 57:174–8. 10.1016/j.jinsphys.2010.11.002 PubMed DOI