Functional Analysis of Adipokinetic Hormone Signaling in Bombyx mori

. 2020 Dec 11 ; 9 (12) : . [epub] 20201211

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid33322530

Insect adipokinetic hormones (AKHs) are short peptides produced in the corpora cardiaca and are responsible for mobilizing energy stores from the fat body to the hemolymph. Three related peptides, AKH1, AKH2, and AKH/corazonin-related peptide (ACP) as well as three AKH receptors have been reported in Bombyx mori. AKH1 and AKH2 are specific for the AKHR1 receptor, whereas ACP interacts with the other two AKHRs. To assess the effect of the two silkworm AKHs and ACP in the regulation of energy homeostasis we examined the expression pattern of the three peptides and their receptors as well as their effect on the level of carbohydrates and lipids in the hemolymph. Our results support the hypothesis that only AKH1 and AKH2 peptides together with the AKHR1 receptor are involved in the maintenance of energy homeostasis. Because Bombyx AKHR1 (BmAKHR1) seems to be a true AKHR we generated its mutation. The BmAKHR1 mutant larvae display significantly lower carbohydrate and lipid levels in the hemolymph and reduced sensitivity to starvation. Our study clarifies the role of BmAKHR1 in energy homeostasis.

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Gade G. The explosion of structural information on insect neuropeptides. Fortschr. Chem. Org. Naturst. 1997;71:1–128. PubMed

Kodrik D. Adipokinetic hormone functions that are not associated with insect flight. Physiol. Entomol. 2008;33:171–180. doi: 10.1111/j.1365-3032.2008.00625.x. DOI

Park Y., Kim Y.J., Adams M.E. Identification of G protein-coupled receptors for Drosophila PRXamide peptides, CCAP, corazonin, and AKH supports a theory of ligand-receptor coevolution. Proc. Natl. Acad. Sci. USA. 2002;99:11423–11428. doi: 10.1073/pnas.162276199. PubMed DOI PMC

Zhu C., Huang H., Hua R., Li G., Yang D., Luo J., Zhang C., Shi L., Benovic J.L., Zhou N. Molecular and functional characterization of adipokinetic hormone receptor and its peptide ligands in Bombyx mori. FEBS Lett. 2009;583:1463–1468. doi: 10.1016/j.febslet.2009.03.060. PubMed DOI PMC

Conzelmann M., Williams E.A., Tunaru S., Randel N., Shahidi R., Asadulina A., Berger J., Offermanns S., Jekely G. Conserved MIP receptor-ligand pair regulates Platynereis larval settlement. Proc. Natl. Acad. Sci. USA. 2013;110:8224–8229. doi: 10.1073/pnas.1220285110. PubMed DOI PMC

Lindemans M., Liu F., Janssen T., Husson S.J., Mertens I., Gade G., Schoofs L. Adipokinetic hormone signaling through the gonadotropin-releasing hormone receptor modulates egg-laying in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA. 2009;106:1642–1647. doi: 10.1073/pnas.0809881106. PubMed DOI PMC

Mirabeau O., Joly J.S. Molecular evolution of peptidergic signaling systems in bilaterians. Proc. Natl. Acad Sci. USA. 2013;110:E2028–E2037. doi: 10.1073/pnas.1219956110. PubMed DOI PMC

Noyes B.E., Katz F.N., Schaffer M.H. Identification and expression of the Drosophila adipokinetic hormone gene. Mol. Cell. Endocrinol. 1995;109:133–141. doi: 10.1016/0303-7207(95)03492-P. PubMed DOI

Siegert K.J. Locust corpora cardiaca contain an inactive adipokinetic hormone. FEBS Lett. 1999;447:237–240. doi: 10.1016/S0014-5793(99)00299-9. PubMed DOI

Abdel-Latief M., Hoffmann K.H. The adipokinetic hormones in the fall armyworm, Spodoptera frugiperda: cDNA cloning, quantitative real time RT-PCR analysis, and gene specific localization. Insect Biochem. Mol. Biol. 2007;37:999–1014. doi: 10.1016/j.ibmb.2007.05.007. PubMed DOI

Lee G., Park J.H. 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. doi: 10.1534/genetics.167.1.311. PubMed DOI PMC

Galikova M., Diesner M., Klepsatel P., Hehlert P., Xu Y., Bickmeyer I., Predel R., Kuhnlein R.P. Energy Homeostasis Control in Drosophila Adipokinetic Hormone Mutants. Genetics. 2015;201:665–683. doi: 10.1534/genetics.115.178897. PubMed DOI PMC

Sajwan S., Sidorov R., Staskova T., Zaloudikova A., Takasu Y., Kodrik D., Zurovec M. Targeted mutagenesis and functional analysis of adipokinetic hormone-encoding gene in Drosophila. Insect Biochem. Mol. Biol. 2015;61:79–86. doi: 10.1016/j.ibmb.2015.01.011. PubMed DOI

Bharucha K.N., Tarr P., Zipursky S.L. A glucagon-like endocrine pathway in Drosophila modulates both lipid and carbohydrate homeostasis. J. Exp. Biol. 2008;211:3103–3110. doi: 10.1242/jeb.016451. PubMed DOI PMC

Gronke S., Muller G., Hirsch J., Fellert S., Andreou A., Haase T., Jackle H., Kuhnlein R.P. Dual lipolytic control of body fat storage and mobilization in Drosophila. PLoS Biol. 2007;5:e137. doi: 10.1371/journal.pbio.0050137. PubMed DOI PMC

Gade G., Auerswald L. Mode of action of neuropeptides from the adipokinetic hormone family. Gen. Comp. Endocrinol. 2003;132:10–20. doi: 10.1016/S0016-6480(03)00159-X. PubMed DOI

Ziegler R., Eckart K., Schwarz H., Keller R. Amino acid sequence of Manduca sexta adipokinetic hormone elucidated by combined fast atom bombardment (FAB)/tandem mass spectrometry. Biochem. Biophys. Res. Commun. 1985;133:337–342. doi: 10.1016/0006-291X(85)91880-7. PubMed DOI

Ishibashi J., Kataoka H., Nagasawa H., Isogai A., Suzuki A. Isolation and Identification of Adipokinetic Hormone of the Silkworm, Bombyx-Mori. Biosci. Biotech. Bioch. 1992;56:66–70. doi: 10.1271/bbb.56.66. DOI

Jaffe H., Raina A.K., Riley C.T., Fraser B.A., Bird T.G., Tseng C.M., Zhang Y.S., Hayes D.K. Isolation and primary structure of a neuropeptide hormone from Heliothis zea with hypertrehalosemic and adipokinetic activities. Biochem. Biophys. Res. Commun. 1988;155:344–350. doi: 10.1016/S0006-291X(88)81091-X. PubMed DOI

Staubli F., Jorgensen T.J., Cazzamali G., Williamson M., Lenz C., Sondergaard L., Roepstorff P., Grimmelikhuijzen C.J. Molecular identification of the insect adipokinetic hormone receptors. Proc. Natl. Acad. Sci. USA. 2002;99:3446–3451. doi: 10.1073/pnas.052556499. PubMed DOI PMC

Roller L., Yamanaka N., Watanabe K., Daubnerova I., Zitnan D., Kataoka H., Tanaka Y. The unique evolution of neuropeptide genes in the silkworm Bombyx mori. Insect Biochem. Molec. 2008;38:1147–1157. doi: 10.1016/j.ibmb.2008.04.009. PubMed DOI

Gade G., Marco H.G., Simek P., Audsley N., Clark K.D., Weaver R.J. Predicted versus expressed adipokinetic hormones, and other small peptides from the corpus cardiacum-corpus allatum: A case study with beetles and moths. Peptides. 2008;29:1124–1139. doi: 10.1016/j.peptides.2008.03.002. PubMed DOI

Hansen K.K., Stafflinger E., Schneider M., Hauser F., Cazzamali G., Williamson M., Kollmann M., Schachtner J., Grimmelikhuijzen C.J. Discovery of a novel insect neuropeptide signaling system closely related to the insect adipokinetic hormone and corazonin hormonal systems. J. Biol. Chem. 2010;285:10736–10747. doi: 10.1074/jbc.M109.045369. PubMed DOI PMC

Fan Y., Sun P., Wang Y., He X., Deng X., Chen X., Zhang G., Chen X., Zhou N. The G protein-coupled receptors in the silkworm, Bombyx mori. Insect Biochem. Mol. Biol. 2010;40:581–591. doi: 10.1016/j.ibmb.2010.05.005. PubMed DOI

Yamanaka N., Yamamoto S., Zitnan D., Watanabe K., Kawada T., Satake H., Kaneko Y., Hiruma K., Tanaka Y., Shinoda T., et al. Neuropeptide receptor transcriptome reveals unidentified neuroendocrine pathways. PLoS ONE. 2008;3:e3048. doi: 10.1371/journal.pone.0003048. PubMed DOI PMC

Shi Y., Huang H., Deng X., He X., Yang J., Yang H., Shi L., Mei L., Gao J., Zhou N. Identification and functional characterization of two orphan G-protein-coupled receptors for adipokinetic hormones from silkworm Bombyx mori. J. Biol. Chem. 2011;286:42390–42402. doi: 10.1074/jbc.M111.275602. PubMed DOI PMC

Takasu Y., Sajwan S., Daimon T., Osanai-Futahashi M., Uchino K., Sezutsu H., Tamura T., Zurovec M. Efficient TALEN construction for Bombyx mori gene targeting. PLoS ONE. 2013;8:e73458. doi: 10.1371/annotation/c544ae05-f54d-488a-912a-9c4a21eb9117. PubMed DOI PMC

Cermak T., Doyle E.L., Christian M., Wang L., Zhang Y., Schmidt C., Baller J.A., Somia N.V., Bogdanove A.J., Voytas D.F. Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res. 2011;39:e82. doi: 10.1093/nar/gkr218. PubMed DOI PMC

Takasu Y., Kobayashi I., Beumer K., Uchino K., Sezutsu H., Sajwan S., Carroll D., Tamura T., Zurovec M. Targeted mutagenesis in the silkworm Bombyx mori using zinc finger nuclease mRNA injection. Insect Biochem. Mol. Biol. 2010;40:759–765. doi: 10.1016/j.ibmb.2010.07.012. PubMed DOI

Takasu Y., Kobayashi I., Tamura T., Uchino K., Sezutsu H., Zurovec M. Precise genome editing in the silkworm Bombyx mori using TALENs and ds- and ssDNA donors—A practical approach. Insect Biochem. Mol. Biol. 2016;78:29–38. doi: 10.1016/j.ibmb.2016.08.006. PubMed DOI

Peng R., Zhai Y., Ding H., Di T., Zhang T., Li B., Shen W., Wei Z. Analysis of reference gene expression for real-time PCR based on relative quantitation and dual spike-in strategy in the silkworm Bombyx mori. Acta Biochim. Biophys. Sin. 2012;44:614–622. doi: 10.1093/abbs/gms040. PubMed DOI

Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001;29:e45. doi: 10.1093/nar/29.9.e45. PubMed DOI PMC

Levine J.D., Sauman I., Imbalzano M., Reppert S.M., Jackson F.R. Period protein from the giant silkmoth Antheraea pernyi functions as a circadian clock element in Drosophila melanogaster. Neuron. 1995;15:147–157. doi: 10.1016/0896-6273(95)90072-1. PubMed DOI

Sauman I., Reppert S.M. Molecular characterization of prothoracicotropic hormone (PTTH) from the giant silkmoth Antheraea pernyi: Developmental appearance of PTTH-expressing cells and relationship to circadian clock cells in central brain. Dev. Biol. 1996;178:418–429. doi: 10.1006/dbio.1996.0228. PubMed DOI

Carroll N.V., Longley R.W., Roe J.H. The determination of glycogen in liver and muscle by use of anthrone reagent. J. Biol. Chem. 1956;220:583–593. PubMed

Zölner N., Kirsch K. Über die quantitative Bestimmung von Lipoide (Mikromethode) mittels der vielen natürlichen Lipoiden (allen bekannten Plasmalipoiden) gemeinsamen Sulfophosphovanillin Reaktion. Ges. Exp. Med. 1962;135:545–561. doi: 10.1007/BF02045455. DOI

Oda Y., Uejuma M., Iwami M., Sakurai S. Involvement of adipokinetic hormone in the homeostatic control of hemolymph trehalose concentration in the larvae of Bombyx mori. Arch. Insect Biochem. 2000;45:156–165. doi: 10.1002/1520-6327(200012)45:4<156::AID-ARCH3>3.0.CO;2-E. PubMed DOI

Kaufmann C., Brown M.R. 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;36:466–481. doi: 10.1016/j.ibmb.2006.03.009. PubMed DOI

Ziegler R., Isoe J., Moore W., Riehle M.A., Wells M.A. The putative AKH receptor of the tobacco hornworm, Manduca sexta, and its expression. J. Insect Sci. 2011;11:40. doi: 10.1673/031.011.0140. PubMed DOI PMC

Jedlicka P., Steinbauerova V., Simek P., Zahradnickova H. Functional characterization of the adipokinetic hormone in the pea aphid, Acyrthosiphon pisum. Comp. Biochem. Phys. A. 2012;162:51–58. doi: 10.1016/j.cbpa.2012.02.004. PubMed DOI

Patel R.T., Soulages J.L., Arrese E.L. Adipokinetic hormone-induced mobilization of fat body triglyceride stores in Manduca sexta: Role of TG-lipase and lipid droplets. Arch. Insect Biochem. Physiol. 2006;63:73–81. doi: 10.1002/arch.20143. PubMed DOI

Andersson D.T. The Development of Holometabolous Insects. In: Counce S.J., Wadding C.H., editors. Developmental Systems—Insects. Volume 1. Academic Press; New York, NY, USA: 1972. pp. 165–242.

Pakkianathan B.C., Singh N.K., Krishnan M., Konig S. A proteomic view on the developmental transfer of homologous 30 kDa lipoproteins from peripheral fat body to perivisceral fat body via hemolymph in silkworm, Bombyx mori. BMC Biochem. 2012;13:5. doi: 10.1186/1471-2091-13-5. PubMed DOI PMC

Lorenz M.W. Adipokinetic hormone inhibits the formation of energy stores and egg production in the cricket Gryllus bimaculatus. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2003;136:197–206. doi: 10.1016/S1096-4959(03)00227-6. PubMed DOI

Fukumura K., Konuma T., Tsukamoto Y., Nagata S. Adipokinetic hormone signaling determines dietary fatty acid preference through maintenance of hemolymph fatty acid composition in the cricket Gryllus bimaculatus. Sci. Rep. 2018;8:4737. doi: 10.1038/s41598-018-22987-2. PubMed DOI PMC

Golebiowski M., Cerkowniak M., Urbanek A., Slocinska M., Rosinski G., Stepnowski P. Adipokinetic hormone induces changes in the fat body lipid composition of the beetle Zophobas atratus. Peptides. 2014;58:65–73. doi: 10.1016/j.peptides.2014.05.013. PubMed DOI

Kodrik D., Goldsworthy G.J. Inhibition of Rna-Synthesis by Adipokinetic Hormones and Brain Factor in Adult Fat-Body of Locusta-Migratoria. J. Insect Physiol. 1995;41:127–133. doi: 10.1016/0022-1910(94)00096-Y. DOI

Candy D.J. Adipokinetic hormones concentrations in the haemolymph of Schistocerca gregaria, measured by radioimmunoassay. Insect Biochem. Mol. 2002;32:1361–1367. doi: 10.1016/S0965-1748(02)00056-5. PubMed DOI

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