Role of PTP/PTK trans activated insulin-like signalling pathway in regulation of grasshopper (Oedaleus asiaticus) development

Abstract

Protein tyrosine phosphatase (PTPs) and protein tyrosine kinase (PTKs) genes are responsible for the regulation of insect insulin-like pathway (ILP), cells growth, metabolism initiation, gene transcription and observing immune response. Signal transduction in insect cell is also associated with PTPs and PTKs. The grasshopper (Oedaleus asiaticus) ‘Bey-Bienko’ were treated with dsRNA of protein tyrosine non-receptor type 4 (PTPN4) and protein tyrosine kinase 5 (PTK5) along with control (water). Applying dsPTK5 treatments in 5th instar of Oedaleus asiaticus, significant reduction was recorded in body dry mass, growth rate and overall performance except survival rate. Whereas with PTPN4, no such significant impact on all of these growth parameters was recorded. Expression of genes in ILP 5th instar of Oedaleus asiaticus by the application of dsPTPN4 and dsPTK5 revealed that PTK, INSR (insulin receptor), IRS (insulin receptor substrate), PI3K (phosphoinositide 3-kinase), PDK (3-phosphoinositide-dependent protein kinase), Akt (protein kinase B) and FOXO (forkhead transcription factor) significantly expressed with downregulation except PTPN4, which remained non-significant. On the other hand, the phosphorylation level of ILP four proteins in O. asiaticus with the treatment of dsPTPN4 and dsPTK5 significantly affected P-IRS and P-FOXO, while P-INSR and P-AKT remained stable at the probability level of 5%. This indicated that the stress response in the O. asiaticus insulin-like signalling pathway (ILP) reduced. Regarding association of protective enzymatic activities, ROS (relative oxygen species), CAT (catalase) and PO (phenol oxidase) increased significantly with exposure to dsPTK5 as compared to dsPTPN4 and control, while exposure of 5th instar of O. asiaticus to dsPTPN4 treatment slightly raised CAT and PO activities with but significant contribution. No such significant effect on MFO and POD was seen using dsPTPN4 and dsPTK5. This showed that in the ILP of O. asiaticus, PTK5 was detrimental to growth, body mass and overall performance, which ultimately benefited insect detoxification with high-energy cost.

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References

  1. Alonso SJ, Bottini N, Friedberg I, Iddo F, Osterman A, Godzik A, Hunter T, Dixon J, Mustelin T (2004) Protein tyrosine phosphatases in the human genome. Cell 117:699–711

    CAS  Article  Google Scholar 

  2. Asante-Appiah E, Kennedy BP (2003) Protein tyrosine phosphatases: the quest for negative regulators of insulin action. Am J Physiol Endocrinol Metab 284:E663–E670

    CAS  Article  Google Scholar 

  3. Ashida M (1990) Biochemistry of the phenoloxidase system in insects: with special reference to its activation, in molting and metamorphosis. Japan Sci Soc Press, Tokyo, pp 237–263

    Google Scholar 

  4. Baba T, Shimizu T, Suzuki Y, Ogawara M, Isono K, Koseki H, Kurosawa H, Shirasawa T (2005) Estrogen, insulin, and dietary signals cooperatively regulate longevity signals to enhance resistance to oxidative stress in mice. J Biol Chem 280:16417–16426

    CAS  Article  Google Scholar 

  5. Badisco L, Wielendaele PV, Broeck JV (2013) Eat to reproduce: a key role for the insulin signaling pathway in adult insects. Front Physiol 4:202

    Article  Google Scholar 

  6. Balcazar Morales N, Aguilar de Plata C (2012) Role of AKT/mTORC1 pathway in pancreatic β-cell proliferation. Colomb Méd 43(3):235–243

    Google Scholar 

  7. Behmer ST (2009) Insect herbivore nutrient regulation. Annu Rev Entomol 54:165–187

    CAS  Article  Google Scholar 

  8. Bézier A, Herbinière J, Serbielle C, Lesobre J, Wincker P, Huguet E, Drezen JM (2008) Bracovirus gene products are highly divergent from insect proteins. Arch Insect Biochem Physiol 67(4):172–187

    Article  CAS  Google Scholar 

  9. Bishop JM (1991) Molecular themes in oncogenesis. Cell 64:235–248

    CAS  Article  Google Scholar 

  10. Boman HG, Faye I, Gudmundsson GH, Lee JY, Lidholm DA (1991) Cell-free immunity in Cecropia. In EJB Reviews 1991 (pp. 189–197). Springer, Berlin, Heidelberg

  11. Bonner-Weir S (2000) Life and death of the pancreatic β cells. Trends Endocrinol Metab 11(9):375–378

    CAS  Article  Google Scholar 

  12. Brogiolo W, Stocker H, Ikeya T, Rintelen F, Fernandez R, Hafen E (2001) An evolutionarily conserved function of the Drosophila insulin receptor and insulin-like peptides in growth control. Curr Biol 11:213–221

    CAS  Article  Google Scholar 

  13. Cease AJ, Hao S, Kang L, Elser JJ, Harrison JF (2010) Are color or high rearing density related to migratory polyphenism in the band-winged grasshopper, Oedaleus asiaticus? J Insect Physiol 56:926–936

    CAS  Article  Google Scholar 

  14. Cease AJ, Elser JJ, Ford CF, Hao SG, Kang L, Harrison JF (2012) Heavy livestock grazing promotes locust outbreaks by lowering plant nitrogen content. Science 335:467–469

    CAS  Article  Google Scholar 

  15. Cease AJ, Harrison JF, Hao S, Niren DC, Zhang G, Kang L, Elser JJ (2017) Nutritional imbalance suppresses migratory phenotypes of the Mongolian locust (Oedaleus asiaticus). R Soc Open Sci 4:161039

    Article  CAS  Google Scholar 

  16. Chang CC, Rahmawaty A, Chang ZW (2013) Molecular and immunological responses of the giant freshwater prawn, Macrobrachium rosenbergii, to the organophosphorus insecticide, trichlorfon. Aquat Toxicol 130–131:18–26. https://doi.org/10.1016/j.aquatox.2012.12.024

    CAS  Article  Google Scholar 

  17. Chen Z, Zheng S, Li L, Jiang H (2014) Metabolism of flavonoids in human: a comprehensive review. Curr Drug Metab 15(1):48–61

    CAS  Article  Google Scholar 

  18. Cheng A, Dube N, Gu F, Tremblay ML (2002) Coordinated action of protein tyrosine phosphatases in insulin signal transduction. Eur J Biochem 269:1050–1059

    CAS  Article  Google Scholar 

  19. Claeys I, Simonet G, Poels J, Van Loy T, Vercammen L, De Loof A, Vanden Broeck J (2002) Insulin-related peptides and their conserved signal transduction pathway. Peptides 23:807–816

    CAS  Article  Google Scholar 

  20. Cross DAE, Alessi DR (1995) Inhibition of glycogen synthase kinase-3 by insulin. Nature 378:785–789

    CAS  Article  Google Scholar 

  21. Duan C, Bauchat JR, Hsieh T (2000) Phosphatidylinositol 3-kinase is required for insulin-like growth factor-I-induced vascular smooth muscle cell proliferation and migration. Circ Res 86:15–23

    CAS  Article  Google Scholar 

  22. Engelman JA, Luo J, Cantley LC (2006) The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism. Nat Rev Genet 7:606–619

    CAS  Article  Google Scholar 

  23. Floyd PD, Li L, Rubakhin SS, Sweedler JV, Charles C (1999) Insulin prohormone processing, distribution, and relation to metabolism in Aplysia californica. Neuroscience 19:7732–7741

    CAS  Article  Google Scholar 

  24. Fraser HB, Khaitovich P, Plotkin JB (2005) Aging and gene expression in the primate brain. PLoS Biol 3(9):e274–e274

    Article  CAS  Google Scholar 

  25. Garofalo RS (2002) Genetic analysis of insulin signaling in Drosophila. Trends Endocrinol Metab 13:156–162

    CAS  Article  Google Scholar 

  26. Gatehouse JA (2002) Plant resistance towards insect herbivores: a dynamic interaction. New Phytol 156(2):145–169

    CAS  Article  Google Scholar 

  27. Giannakou ME, Partridge L (2007) Role of insulin-like signalling in Drosophila lifespan. Trends Biochem Sci 32:180–188

    CAS  Article  Google Scholar 

  28. Goberdhan DC, Wilson C (2003) The functions of insulin signalling: size isn’t everything, even in Drosophila. Differentiation 71:375–397

    CAS  Article  Google Scholar 

  29. González-Santoyo I, Córdoba-Aguilar A (2012) Phenoloxidase: a key component of the insect immune system. Entomol Exp Appl 142(1):1–16

    Article  CAS  Google Scholar 

  30. Guo ZW, Li HC, Gan YL (2006) Grasshopper (Orthoptera: Acrididae) biodiversity and grassland ecosystems. Insect Sci 13(3):221–227

    Article  Google Scholar 

  31. Hanks SK, Quinn AM, Hunter T (1988) The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241:42–52

    CAS  Article  Google Scholar 

  32. Hendriks WJ, Elson A, Harroch S, Pulido R, Stoker A, den Hertog J (2013) Protein tyrosine phosphatases in health and disease. FEBS J 280(2):708–730. https://doi.org/10.1111/febs.12000

    CAS  Article  Google Scholar 

  33. Hollman PC (2004) Absorption, bioavailability, and metabolism of flavonoids. Pharm Biol 42(sup1):74–83

    CAS  Article  Google Scholar 

  34. Huang X, McNeill M, Zhang ZH (2016) Quantitative analysis of plant consumption and preference by Oedaleus asiaticus (Acrididae: Oedipodinae) in changed plant communities consisting of three grass species. Environ Entomol 45:163–170

    CAS  Article  Google Scholar 

  35. Huang X, Ma J, Qin X, Tu X, Cao G, Wang G, Nong X, Zhang Z (2017a) Biology, physiology and gene expression of grasshopper Oedaleus asiaticus exposed to diet stress from plant secondary compounds. Sci Rep 7(1):8655

    Article  CAS  Google Scholar 

  36. Huang X, Whitman DW, Ma J, McNeill MR, Zhang Z (2017b) Diet alters performance and transcription patterns in Oedaleus asiaticus (Orthoptera: Acrididae) grasshoppers. PLoS One 12(10):e0186397

    Article  CAS  Google Scholar 

  37. Hubbard SR, Till JH (2000) Protein tyrosine kinase structure and function. Annu Rev Biochem 69:373–398

    CAS  Article  Google Scholar 

  38. Hughes KA, Reynolds RM (2005) Evolutionary and mechanistic theories of aging. Annu Rev Entomol 50:421–445

    CAS  Article  Google Scholar 

  39. Hunter T (1987) A thousand and one protein kinases. Cell 50:823–829

    CAS  Article  Google Scholar 

  40. Lee YH, White MF (2004) Insulin receptor substrate proteins and diabetes. Arch Pharm Res 27:361–370

    CAS  Article  Google Scholar 

  41. Li X, Schuler MA, Berenbaum MR (2007) Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu Rev Entomol 52:231–253

    Article  CAS  Google Scholar 

  42. Liu Y, Zhou S, Ma L, Tian L, Wang S, Sheng Z, Li S (2010) Transcriptional regulation of the insulin signaling pathway genes by starvation and 20-hydroxyecdysone in the Bombyx fat body. J Insect Physiol 56:1436–1444

    CAS  Article  Google Scholar 

  43. Liu GH, Hao SG, Shao XQ, Zhang YJ, Wang SP (2013) Diet composition and trophic niche of Oedaleus asiaticus (Orthoptera: Acrididae) in natural grasslands under different grazing pressure in Inner Mongolia, northern China. Acta Entomol Sin 56:537–547

    Google Scholar 

  44. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    CAS  Article  Google Scholar 

  45. Lu H, Yu M, Zhang L, Zhang Z, Long R (2005) Effects of foraging by different instar and density of {Oedaleus asiaticus} B. Bienko on forage yield. Plant Prot 31(4):55–58

    Google Scholar 

  46. Luo Y, Wang X, Wang X, Yu D, Chen B, Kang L (2013) Differential responses of migratory locusts to systemic RNA interference via double-stranded RNA injection and feeding. Insect Mol Biol 22(5):574–583

    CAS  Article  Google Scholar 

  47. Mustelin T, Abraham RT, Rudd CE, Alonso A, Merlo JJ (2002) Protein tyrosine phosphorylation in T cell signaling. Front Biosci 7:d918–d969

    CAS  Article  Google Scholar 

  48. Oldham S, Hafen E (2003) Insulin/IGF and target of rapamycin signaling: a TOR de force in growth control. Trends Cell Biol 13:79–85

    CAS  Article  Google Scholar 

  49. Rudolph J (2007) Inhibiting transient protein-protein interactions: lessons from the Cdc25 protein tyrosine phosphatases. Nat Rev Cancer 7:202–211

    CAS  Article  Google Scholar 

  50. Salmeen A, Andersen JN, Myers MP, Tonks NK, Barford D (2000) Molecular basis for the dephosphorylation of the activation segment of the insulin receptor by protein tyrosine phosphatase 1B. Mol Cell 6(6):1401–1412

    CAS  Article  Google Scholar 

  51. Simmonds MS (2003) Flavonoid–insect interactions: recent advances in our knowledge. Phytochemistry 64(1):21–30

    CAS  Article  Google Scholar 

  52. Simpson SJ, Sibly RM, Lee KP, Behmer ST, Raubenheimer D (2004) Optimal foraging when regulating intake of multiple nutrients. Anim Behav 68(6):1299–1311

    Article  Google Scholar 

  53. Smit AB, van Kesteren RE, Li KW, van Minnen J, Spijker S, van Heerikhuizen H, Geraerts WP (1998) Towards understanding the role of insulin in the brain: lessons from insulin-related signaling systems in the invertebrate brain. Prog Neurobiol 54:35–54

    CAS  Article  Google Scholar 

  54. Soulsby M, Bennett AM (2009) Physiological signaling specificity by protein tyrosine phosphatases. Physiology (Bethesda) 24:281–289

    CAS  Google Scholar 

  55. Stam JM, Kroes A, Li Y, Gols R, van Loon JJ, Poelman EH, Dicke M (2014) Plant interactions with multiple insect herbivores: from community to genes. Annu Rev Plant Biol 65:689–713. https://doi.org/10.1146/annurev-arplant-050213-035937

    CAS  Article  Google Scholar 

  56. Steffen Y, Gruber C, Schewe T, Sies H (2008) Mono-O-methylated flavonoids and other flavonoids as inhibitors of endothelial NADPH oxidase. Arch Biochem Biophys 469(2):209–219

    CAS  Article  Google Scholar 

  57. Stephens L, Anderson K, Stokoe D (1998) Protein kinase B kinases that mediate phosphatidylinositol 3,4,5-trisphosphate-dependent activation of protein kinase B. Science 279:710–714

    CAS  Article  Google Scholar 

  58. Taguchi A, White MF (2008) Insulin-like signaling, nutrient homeostasis, and life span. Annu Rev Physiol 70:191–212

    CAS  Article  Google Scholar 

  59. Taniguchi CM, Emanuelli B, Kahn CR (2006) Critical nodes in signalling pathways: insights into insulin action. Nat Rev Mol Cell Biol 7:85–96

    CAS  Article  Google Scholar 

  60. Tatar M, Bartke A, Antebi A (2003) The endocrine regulation of aging by insulin-like signals. Science 299:1346–1351

    CAS  Article  Google Scholar 

  61. Teleman AA (2010) Molecular mechanisms of metabolic regulation by insulin in Drosophila. Biochem J 425(1):13–26

    CAS  Article  Google Scholar 

  62. Vang T, Miletic AV, Arimura Y, Tautz L, Rickert RC, Mustelin T (2008) Protein tyrosine phosphatases in autoimmunity. Annu Rev Immunol 26:29–55

    CAS  Article  Google Scholar 

  63. Verdu J, Buratovich MA, Wilder EL, Birnbaum MJ (1999) Cell-autonomous regulation of cell and organ growth in Drosophila by Akt/PKB. Nat Cell Biol 1:500–506

    CAS  Article  Google Scholar 

  64. Walton KM, Dixon JE (1993) Protein tyrosine phosphatases. Annu Rev Biochem 62:101–120

    CAS  Article  Google Scholar 

  65. Wolkow CA, Muñoz MJ, Riddle DL, Ruvkun G (2002) Insulin receptor substrate and p55 orthologous adaptor proteins function in the Caenorhabditis elegans daf-2/insulin-like signalling pathway. J Biol Chem 277(51):49591–49597

    CAS  Article  Google Scholar 

  66. Wu JQ, Baldwin IT (2010) New insights into plant responses to the attack from insect herbivores. Annu Rev Genet 44:1–24

    CAS  Article  Google Scholar 

  67. Wu Q, Brown MR (2006) Signaling and function of insulin-like peptides in insects. Annu Rev Entomol 51:1–24

    CAS  Article  Google Scholar 

  68. Wu G, Chen FJ, Xiao NW, Ge F (2010) Plant allocation to defensive compounds of transgenic Bt cotton in response to infestation by cotton bollworm under conditions of elevated CO2. Int J Pest Manag 56(2):81–89

    CAS  Article  Google Scholar 

  69. Wu QJ, Zhang YJ, Xu BY, Zhang WJ (2011) The defending enzymes in abamectin resistant Plutella xylostella. Chin J Appl Entomol 48(2):291–295

    CAS  Google Scholar 

  70. Wu HH, Xu YH, Cao GC, Gexigedu R, Liu ZY, He B, Ererdengba T, Wang GJ (2012) Ecological effects of typical grassland types in Inner Mongolia on grasshopper community. Sci Agric Sin 45:4178–4186

    Google Scholar 

  71. Yonglin LHWZC (1987) Food consumption and utilization by three species of Acridoids (adult stage) in typical steppe. Acta Ecol Sin 4:005

    Google Scholar 

  72. Zhang ZY (2002) Protein tyrosine phosphatases: structure and function, substrate specificity, and inhibitor development. Annu Rev Pharmacol Toxicol 42:209–234

    CAS  Article  Google Scholar 

  73. Zhang WZ, He B, Cao GC, Zhang ZH, Wu YH, Liu SC, Wang HR (2013) Quantitative analysis of the effects of Stipa krylovii and Leymus chinensis on the factors of vitality of Oedaleus decorus asiaticus. Acta Pratacultuae Sin 22(5):302–309

    Google Scholar 

  74. Zhang ZJ, Elser JJ, Cease AJ, Zhang XMYQ (2014) Grasshoppers regulate N:P stoichiometric homeostasis by changing phosphorus contents in their frass. PLoS One 9:e103697

    Article  CAS  Google Scholar 

  75. Zhao X, Jia M, Wang L, Cao GC, Zhang ZH (2014) Effects of glutamate and Na+ on the development and enzyme activity of the oriental migratory locust, Locusta migratoria manilensis (Meyen) in successive generations. J Integr Agric 13(4):819–826

    CAS  Article  Google Scholar 

  76. Zhou J, Wan B, Shan J, Shi H, Li Y, Huo K (2013) PTPN4 negatively regulates CrkI in human cell lines. Cell Mol Biol Lett 18(2):297–314. https://doi.org/10.2478/s11658-013-0090-3

    CAS  Article  Google Scholar 

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Acknowledgments

We are grateful to anonymous reviewers for their constructive comments on earlier draft of this manuscript. We also thank PhD Mohamed Diaby (Institute of Animal Sciences CAAS, Beijing) and Arthur Mitchell (University of Lincoln, England) for their invaluable suggestions on manuscript organization and linguistic revision. We also thank Beijing Novogene Experimental Department for the help of sequencing.

Funding

This study was supported by the National Natural Science Foundation of China (No. 31672485), the Earmarked Fund for China Agriculture Research System (No. CARS-34-07) and the Innovation Project of Chinese Academy of Agricultural Science.

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Chang, B.H., Cui, B., Ullah, H. et al. Role of PTP/PTK trans activated insulin-like signalling pathway in regulation of grasshopper (Oedaleus asiaticus) development. Environ Sci Pollut Res 26, 8312–8324 (2019). https://doi.org/10.1007/s11356-019-04212-3

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Keywords

  • Insulin-like signalling pathway
  • Protein tyrosine phosphatase
  • Protein tyrosine kinase, insect descriptive parameters
  • Performance
  • Protective enzyme
  • Oedaleus asiaticus