Galactose-NlGr11 inhibits AMPK phosphorylation by activating the PI3K-AKT-PKF-ATP signaling cascade via insulin receptor and Gβγ.
AMP-Activated Protein Kinase Kinases
Animals
Galactose
/ metabolism
Hemiptera
/ metabolism
Insect Proteins
/ metabolism
Phosphatidylinositol 3-Kinase
/ metabolism
Phosphorylation
Protein Kinase Inhibitors
/ metabolism
Protein Kinases
/ metabolism
Receptor, Insulin
/ metabolism
Signal Transduction
Sugars
/ metabolism
AMPK
Gβγ
IIS pathway
galactose
sugar gustatory receptor
Journal
Insect science
ISSN: 1744-7917
Titre abrégé: Insect Sci
Pays: Australia
ID NLM: 101266965
Informations de publication
Date de publication:
Jun 2021
Jun 2021
Historique:
revised:
13
04
2020
received:
23
02
2020
accepted:
23
04
2020
pubmed:
30
4
2020
medline:
9
6
2021
entrez:
30
4
2020
Statut:
ppublish
Résumé
As ligands of the sugar gustatory receptors, sugars have been known to activate the insulin/insulin-like growth factor signaling pathway; however, the precise pathways that are activated by the sugar-bound gustatory receptors in insects remain unclear. In this study, we aimed to investigate the signaling cascades activated by NlGr11, a sugar gustatory receptor in the brown planthopper Nilaparvata lugens (Stål), and its ligand. Galactose-bound NlGr11 (galactose-NlGr11) activated the -phosphatidylinositol 3-kinase (PI3K)-AKT signaling cascade via insulin receptor (InR) and Gβγ in vitro. In addition, galactose-NlGr11 inhibited the adenosine monophosphate-activated protein kinase (AMPK) phosphorylation by activating the AKT-phosphofructokinase (PFK)-ATP signaling cascade in vitro. Importantly, the InR-PI3K-AKT-PFK-AKT signaling cascade was activated and the AMPK phosphorylation was inhibited after feeding the brown planthoppers with galactose solution. Collectively, these findings confirm that NlGr11 can inhibit AMPK phosphorylation by activating the PI3K-AKT-PFK-ATP signaling cascades via both InR and Gβγ when bound to galactose. Thus, our study provides novel insights into the signaling pathways regulated by the sugar gustatory receptors in insects.
Identifiants
pubmed: 32348014
doi: 10.1111/1744-7917.12795
doi:
Substances chimiques
Insect Proteins
0
Protein Kinase Inhibitors
0
Sugars
0
Protein Kinases
EC 2.7.-
Phosphatidylinositol 3-Kinase
EC 2.7.1.137
Receptor, Insulin
EC 2.7.10.1
AMP-Activated Protein Kinase Kinases
EC 2.7.11.3
Galactose
X2RN3Q8DNE
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
735-745Subventions
Organisme : National Natural Science Foundation of China
ID : U1401212
Organisme : China Postdoctoral Science Foundation
ID : 2017M612808
Informations de copyright
© 2020 Institute of Zoology, Chinese Academy of Sciences.
Références
Berggreen, C., Gormand, A., Omar, B., Degerman, E. and Göransson, O. (2009) Protein kinase B activity is required for the effects of insulin on lipid metabolism in adipocytes. American Journal of Physiology-Endocrinology and Metabolism, 296, E635-E646.
Bertrand, L., Ginion, A., Beauloye, C., Hebert, A.D., Guigas, B., Hue, L. et al. (2006) AMPK activation restores the stimulation of glucose uptake in an in vitro model of insulin-resistant cardiomyocytes via the activation of protein kinase B. American Journal of Physiology-Heart and Circulatory Physiology, 291, 239-250.
Bredendiek, N., Hütte, J., Steingräber, A., Hatt, H., Gisselmann, G. and Neuhaus, E.M. (2011) Goα is involved in sugar perception in Drosophila. Chemical Senses, 36, 69-81.
Chen, W.W., Kang, K., Yang, P. and Zhang, W.Q. (2019) Identification of a sugar gustatory receptor and its effect on fecundity of the brown planthopper Nilaparvata lugens. Insect Science, 26, 441-452.
Djouder, N., Tuerk, R.D., Suter, M., Salvioni, P., Thali, R.F., Scholz, R. et al. (2010) PKA phosphorylates and inactivates AMPKα to promote efficient lipolysis. EMBO Journal, 29, 469-481.
Dorsam, R.T. and Gutkind, J.S. (2007) G-protein-coupled receptors and cancer. Nature Reviews Cancer, 7, 79-94.
Fu, Q., Zhang, Z., Hu, C., Lai, F.X., and Sun, Z.X. (2001) A chemically defined diet enables continuous rearing of the brown planthopper, Nilaparvata lugens (Stål) (Homoptera: Delphacidae). Applied Entomology and Zoology, 36, 111-116.
Hahn-Windgassen, A., Nogueira, V., Chen, C.C., Skeen, J.E., Sonenberg, N. and Hay, N. (2005) Akt activates the mammalian target of rapamycin by regulating cellular ATP level and AMPK activity. Journal of Biological Chemistry, 280, 32081-32089.
Hawley, S.A., Boudeau, J., Reid, J.L., Mustard, K.J., Udd, L., Mäkelä, T.P. et al. (2003) Complexes between the LKB1 tumor suppressor, STRADα/β and MO25α/β are upstream kinases in the AMP-activated protein kinase cascade. Journal of Biology, 2, 28.
Hurley, R.L., Barré, L.K., Wood, S.D., Anderson, K.A., Kemp, B.E., Means, A.R. et al. (2006) Regulation of AMP-activated protein kinase by multisite phosphorylation in response to agents that elevate cellular cAMP. Journal of Biological Chemistry, 281, 36662-36672.
Ishimoto, H., Takahashi, K., Ueda, R. and Tanimura, T. (2014) G-protein gamma subunit 1 is required for sugar reception in Drosophila. EMBO Journal, 24, 3259-3265.
Kain, P., Chakraborty, T.S., Sundaram, S., Siddiqi, O., Rodrigues, V. and Hasan, G. (2008) Reduced odor responses from antennal neurons of Gqα, phospholipase Cβ, and rdgA mutants in Drosophila support a role for a phospholipid intermediate in insect olfactory transduction. Journal of Neuroscience, 28, 4745-4755.
Kan, H., Kataoka-Shirasugi, N. and Amakawa, T. (2008) Transduction pathways mediated by second messengers including cAMP in the sugar receptor cell of the blow fly: Study by the whole cell clamp method. Journal of Insect Physiology, 54, 1028-1034.
Kimball, S.R., Siegfried, B.A. and Jefferson, L.S. (2004) Glucagon represses signaling through the mammalian target of rapamycin in rat liver by activating AMP-activated protein kinase. Journal of Biological Chemistry, 279, 54103-54109.
Koganezawa, M. and Shimada, I. (1997) The effects of G protein modulators on the labellar taste receptor cells of the fleshfly (Boettcherisca peregrina). Journal of Insect Physiology, 43, 225-233.
Koganezawa, M. and Shimada, I. (2002) Inositol 1, 4, 5-trisphosphate transduction cascade in taste reception of the fleshfly, Boettcherisca peregrina. Journal of Neurobiology, 51, 66-83.
Kovacic, S., Soltys, C.L., Barr, A.J., Shiojima, I., Walsh, K. and Dyck, J.R. (2003) Akt activity negatively regulates phosphorylation of AMP-activated protein kinase in the heart. Journal of Biological Chemistry, 278, 39422-39427.
Kyriazis, G.A., Soundarapandian, M.M. and Tyrberg, B. (2012) Sweet taste receptor signaling in beta cells mediates fructose-induced potentiation of glucose-stimulated insulin secretion. Proceedings of the National Academy of Sciences USA, 109, 2713-2714.
Leem, J., Shim, H.M., Cho, H.C. and Park, J.H. (2018) Octanoic acid potentiates glucose-stimulated insulin secretion and expression of glucokinase through the olfactory receptor in pancreatic β-cells. Biochemical and Biophysical Research Communications, 503, 278-284.
Levine, Y.C., Li, G.K. and Michel, T. (2007) Agonist-modulated regulation of AMP-activated protein kinase (AMPK) in endothelial cells. Journal of Biological Chemistry, 282, 20351-20364.
Lin, X.D., Xu, Y.L., Jiang, J.R., Lavine, M. and Lavine, L.C. (2018) Host quality induces phenotypic plasticity in a wing polyphenic insect. Proceedings of the National Academy of Sciences USA, 115, 7563-7568.
Longnus, S. L., Ségalen, C., Giudicelli, J., Sajan, M.P., Farese, R.V. and Van, O.E. (2005) Insulin signalling downstream of protein kinase B is potentiated by 5′AMP-activated protein kinase in rat hearts in vivo. Diabetologia, 48, 2591-2601.
Mitsumasu, K., Azuma, M., Niimi, T., Yamashita, O. and Yaginuma, T. (2008) Changes in the expression of soluble and integral-membrane trehalases in the midgut during metamorphosis in Bombyx mori. Zoological Science, 25, 693-698.
Munakata, Y., Yamada, T., Imai, J., Takahashi, K., Tsukita, S., Shirai, Y. etal. (2018) Olfactory receptors are expressed in pancreatic β-cells and promote glucose-stimulated insulin secretion. Scientific Reports, 8, 1-11.
Nakagawa, Y., Ohtsu, Y., Nagasawa, M., Shibata, H. and Kojima, I. (2014) Glucose promotes its own metabolism by acting on the cell-surface glucose-sensing receptor T1R3. Endocrine Journal, 61, 119-131.
Nin, V., Escande, C., Chini, C.C., Giri, S., Camachopereira, J., Matalonga, J. et al. (2012) Role of deleted in breast cancer 1 (DBC1) protein in SIRT1 deacetylase activation induced by protein kinase A and AMP-activated protein kinase. Journal of Biological Chemistry, 287, 23489-23501.
Ouchi, N., Kobayashi, H., Kihara, S., Kumada, M., Sato, K., Inoue, T. et al. (2004) Adiponectin stimulates angiogenesis by promoting cross-talk between AMP-activated protein kinase and Akt signaling in endothelial cells. Journal of Biological Chemistry, 279, 1304-1309.
Sakamoto, K., McCarthy, A., Smith, D., Green, K.A., Hardie, G.D., Ashworth, A. et al. (2005) Deficiency of LKB1 in skeletal muscle prevents AMPK activation and glucose uptake during contraction. EMBO Journal, 24, 1810-1820.
Sakamoto, K., Zarrinpashneh, E., Budas, G.R., Pouleur, A.C., Dutta, A., Prescott, A.R., et al. (2006) Deficiency of LKB1 in heart prevents ischemia-mediated activation of AMPKα2 but not AMPKα1. American Journal of Physiology-Endocrinology and Metabolism, 290, E780.
Saltiel, A.R. and Kahn, C.R. (2001) Insulin signalling and the regulation of glucose and lipid metabolism. Nature, 414, 799-806.
Sato, K., Tanaka, K. and Touhara, K. (2011) Sugar-regulated cation channel formed by an insect gustatory receptor. Proceedings of the National Academy of Sciences USA, 108, 11680-11685.
Scott, K., Brady Jr., R.J., Cravchik, A., Morozov, P., Rzhetsky, A., Zuker, C. et al. (2001) A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila. Cell, 104, 661-673.
Seno, K., Fujikawa, K., Nakamura, T. and Ozaki, M. (2005) Gqα subunit mediates receptor site-specific adaptation in the sugar taste receptor cell of the blowfly, Phormia regina. Neuroscience Letters, 377, 200-205.
Stahmann, N., Woods, A., Carling, D. and Heller, R. (2006) Thrombin activates AMP-activated protein kinase in endothelial cells via a pathway involving Ca2+/calmodulin-dependent protein kinase kinase beta. Molecular and Cellular Biology, 26, 5933-5945.
Tamas, P., Hawley, S.A., Clarke, R.G., Mustard, K.J., Green, K., Hardie, D.G. et al. (2006) Regulation of the energy sensor AMP-activated protein kinase by antigen receptor and Ca2+ in T lymphocytes. Journal of Experimental Medicine, 203, 1665-1670.
Taniguchi, C. M., Emanuelli, B. and Kahn, C.R. (2006) Critical nodes in signalling pathways: insights into insulin action. Nature Reviews Molecular Cell Biology, 7, 85-96.
Ueno, K., Kohatsu, S., Clay, C., Forte, M., Isono, K. and Kidokoro, Y. (2006) Gsα is involved in sugar perception in Drosophila melanogaster. Journal of Neuroscience, 26, 6143-6152.
Usui-Aoki, K., Matsumoto, K., Koganezawa, M., Kohatsu, S., Isono, K., Matsubayashi, H. et al. (2005) Targeted expression of IP3 sponge and IP3 dsRNA impairs sugar taste sensation in Drosophila. Journal of Neurogenetic, 19, 123-141.
Vadas, O., Burke, J.E., Zhang, X.X., Berndt, A. and Williams, R.L. (2011) Structural basis for activation and inhibition of class I phosphoinositide 3-kinases. Science Signaling, 4, re2.
Valentine, R.J., Coughlan, K.A., Ruderman, N.B. and Saha, A.K. (2014) Insulin inhibits AMPK activity and phosphorylates AMPK Ser485/491 through Akt in hepatocytes, myotubes and incubated rat skeletal muscle. Archives of Biochemistry and Biophysics, 562, 62-69.
Woods, A., Johnstone, S.R., Dickerson, K., Leiper, F.C., Fryer, L.G., Neumann, D. et al. (2003) LKB1 is the upstream kinase in the AMP-activated protein kinase cascade. Current Biology, 13, 2004-2008.
Wu, H.M., Yang, Y.M. and Kim, S.G. (2011) Rimonabant, a cannabinoid receptor type 1 inverse agonist, inhibits hepatocyte lipogenesis by activating liver kinase B1 and AMP-activated protein kinase axis downstream of Gαi/o inhibition. Molecular Pharmacology, 80, 859-869.
Xu, H.J., Xue, J., Lu, B., Zhang, X.C., Zhuo, J.C., He, S.F. et al. (2015) Two insulin receptors determine alternative wing morphs in planthoppers. Nature, 519, 464-467.
Xu, W. (2020) How do moth and butterfly taste? - Molecular basis of gustatory receptors in Lepidoptera. Insect Science, 27, 1148-1157.
Yin, W., Mu, J. and Birnbaum, M.J. (2003) Role of AMP-activated protein kinase in cyclic AMP-dependent lipolysis in 3T3-L1 adipocytes. Journal of Biological Chemistry, 278, 43074-43080.
Zhang, H.J., Anderson, A.R., Trowell, S.C., Luo, A.R. and Xia, Q.Y. (2011) Topological and functional characterization of an insect gustatory receptor. PLoS ONE, 6, e24111.