Juvenile Hormone and Insulin Regulate Trehalose Homeostasis in the Red Flour Beetle,

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Insulin/IGF-1 signaling (IIS) has been well studied for its role in the control of life span extension and resistance to a variety of stresses. The Drosophila melanogaster insulin-like receptor (InR) mutant showed extended life span due to reduced juvenile hormone (JH) levels. However, little is known about the mechanism of cross talk between IIS and JH in regulation of life span extension and resistance to starvation. In the current study, we investigated the role of IIS and JH signaling in regulation of resistance to starvation. Reduction in JH biosynthesis, JH action, or insulin-like peptide 2 (ILP2) syntheses by RNA interference (RNAi)-aided knockdown in the expression of genes coding for juvenile hormone acid methyltransferase (JHAMT), methoprene-tolerant (Met), or ILP2 respectively decreased lipid and carbohydrate metabolism and extended the survival of starved beetles. Interestingly, the extension of life span could be restored by injection of bovine insulin into JHAMT RNAi beetles but not by application of JH III to ILP2 RNAi beetles. These data suggest that JH controls starvation resistance by regulating synthesis of ILP2. More importantly, JH regulates trehalose homeostasis, including trehalose transport and metabolism, and controls utilization of stored nutrients in starved adults.

Vyšlo v časopise: Juvenile Hormone and Insulin Regulate Trehalose Homeostasis in the Red Flour Beetle,. PLoS Genet 9(6): e32767. doi:10.1371/journal.pgen.1003535
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003535

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Zdroje

1. JindraM, PalliSR, RiddifordLM (2013) The Juvenile hormone signaling pathway in insect development. Annu Rev Entomol 58: 181–204.

2. RiddifordLM (2012) How does juvenile hormone control insect metamorphosis and reproduction? Gen Comp Endocrinol 179: 477–484.

3. MinakuchiC, NamikiT, ShinodaT (2009) Kruppel homolog 1, an early juvenile hormone-response gene downstream of Methoprene-tolerant, mediates its anti-metamorphic action in the red flour beetle Tribolium castaneum. Dev Biol 325: 341–350.

4. TrumanJW, HirumaK, AlleeJP, MacwhinnieSG, ChamplinDT, et al. (2006) Juvenile hormone is required to couple imaginal disc formation with nutrition in insects. Science 312: 1385–1388.

5. KoyamaT, SyropyatovaMO, RiddifordLM (2008) Insulin/IGF signaling regulates the change in commitment in imaginal discs and primordia by overriding the effect of juvenile hormone. Dev Biol 324: 258–265.

6. ToblerA, NijhoutHF (2010) A switch in the control of growth of the wing imaginal disks of Manduca sexta. PLoS One 5: e10723.

7. ParthasarathyR, TanA, SunZ, ChenZ, RankinM, et al. (2009) Juvenile hormone regulation of male accessory gland activity in the red flour beetle, Tribolium castaneum. Mech Dev 126: 563–579.

8. WilsonTG, DeMoorS, LeiJ (2003) Juvenile hormone involvement in Drosophila melanogaster male reproduction as suggested by the Methoprene-tolerant(27) mutant phenotype. Insect Biochem Mol Biol 33: 1167–1175.

9. ShengZ, XuJ, BaiH, ZhuF, PalliSR (2011) Juvenile hormone regulates vitellogenin gene expression through insulin-like peptide signaling pathway in the red flour beetle, Tribolium castaneum. J Biol Chem 286: 41924–41936.

10. MinakuchiC, ZhouX, RiddifordLM (2008) Kruppel homolog 1 (Kr-h1) mediates juvenile hormone action during metamorphosis of Drosophila melanogaster. Mech Dev 125: 91–105.

11. KayukawaT, MinakuchiC, NamikiT, TogawaT, YoshiyamaM, et al. (2012) Transcriptional regulation of juvenile hormone-mediated induction of Kruppel homolog 1, a repressor of insect metamorphosis. Proc Natl Acad Sci U S A 109: 11729–11734.

12. ZhangZ, XuJ, ShengZ, SuiY, PalliSR (2011) Steroid receptor co-activator is required for juvenile hormone signal transduction through a bHLH-PAS transcription factor, methoprene tolerant. J Biol Chem 286: 8437–8447.

13. LiM, MeadEA, ZhuJ (2011) Heterodimer of two bHLH-PAS proteins mediates juvenile hormone-induced gene expression. Proc Natl Acad Sci U S A 108: 638–643.

14. Charles, JP, IwemaT, Epa, VC, TakakiK, RynesJ, JindraM (2011) Ligand-binding properties of a juvenile hormone receptor, Methoprene-tolerant. Proc Natl Acad Sci U S A 108: 21128–21133.

15. Shin, SW, ZouZ, SahaTT, RaikhelAS (2012) bHLH-PAS heterodimer of methoprene-tolerant and Cycle mediates circadian expression of juvenile hormone-induced mosquito genes. Proc Natl Acad Sci U S A 109: 16576–16581.

16. HermanWS, TatarM (2001) Juvenile hormone regulation of longevity in the migratory monarch butterfly. Proc Biol Sci 268: 2509–2514.

17. TatarM, KopelmanA, EpsteinD, TuMP, YinCM, et al. (2001) A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science 292: 107–110.

18. FontanaL, PartridgeL, LongoVD (2010) Extending healthy life span–from yeast to humans. Science 328: 321–326.

19. KramerJM, DavidgeJT, LockyerJM, StaveleyBE (2003) Expression of Drosophila FOXO regulates growth and can phenocopy starvation. BMC Dev Biol 3: 5.

20. EssersMA, WeijzenS, de Vries-SmitsAM, SaarloosI, de RuiterND, et al. (2004) FOXO transcription factor activation by oxidative stress mediated by the small GTPase Ral and JNK. EMBO J 23: 4802–4812.

21. HendersonST, JohnsonTE (2001) daf-16 integrates developmental and environmental inputs to mediate aging in the nematode Caenorhabditis elegans. Curr Biol 11: 1975–1980.

22. SenguptaA, MolkentinJD, YutzeyKE (2009) FoxO transcription factors promote autophagy in cardiomyocytes. J Biol Chem 284: 28319–28331.

23. GrossDN, van den HeuvelAP, BirnbaumMJ (2008) The role of FoxO in the regulation of metabolism. Oncogene 27: 2320–2336.

24. BeckerA, SchloderP, SteeleJE, WegenerG (1996) The regulation of trehalose metabolism in insects. Experientia 52: 433–439.

25. KikawadaT, SaitoA, KanamoriY, NakaharaY, IwataK, et al. (2007) Trehalose transporter 1, a facilitated and high-capacity trehalose transporter, allows exogenous trehalose uptake into cells. Proc Natl Acad Sci U S A 104: 11585–11590.

26. BouniasM, BahjouA, GourdouxL, MoreauR (1993) Molecular activation of a trehalase purified from the fat body of a coleopteran insect (Tenebrio molitor), by an endogenous insulin-like peptide. Biochem Mol Biol Int 31: 249–266.

27. TrumboST, RobinsonGE (2004) Nutrition, hormones and life history in burying beetles. J Insect Physiol 50: 383–391.

28. TuMP, YinCM, TatarM (2005) Mutations in insulin signaling pathway alter juvenile hormone synthesis in Drosophila melanogaster. Gen Comp Endocrinol 142: 347–356.

29. WangY, BrentCS, FennernE, AmdamGV (2012) Gustatory perception and fat body energy metabolism are jointly affected by vitellogenin and juvenile hormone in honey bees. PLoS Genet 8: e1002779.

30. EnellLE, KapanN, SoderbergJA, KahsaiL, NasselDR (2010) Insulin signaling, lifespan and stress resistance are modulated by metabotropic GABA receptors on insulin producing cells in the brain of Drosophila. PLoS One 5: e15780.

31. BroughtonS, AlicN, SlackC, BassT, IkeyaT, et al. (2008) Reduction of DILP2 in Drosophila triages a metabolic phenotype from lifespan revealing redundancy and compensation among DILPs. PLoS One 3: e3721.

32. BroughtonSJ, PiperMD, IkeyaT, BassTM, JacobsonJ, et al. (2005) Longer lifespan, altered metabolism, and stress resistance in Drosophila from ablation of cells making insulin-like ligands. Proc Natl Acad Sci U S A 102: 3105–3110.

33. RubinBR, BoganJS (2009) Intracellular retention and insulin-stimulated mobilization of GLUT4 glucose transporters. Vitam Horm 80: 155–192.

34. ZaidH, AntonescuCN, RandhawaVK, KlipA (2008) Insulin action on glucose transporters through molecular switches, tracks and tethers. Biochem J 413: 201–215.

35. StralforsP (1988) Insulin stimulation of glucose uptake can be mediated by diacylglycerol in adipocytes. Nature 335: 554–556.

36. GoodyearLJ, KahnBB (1998) Exercise, glucose transport, and insulin sensitivity. Annu Rev Med 49: 235–261.

37. HansenPA, NolteLA, ChenMM, HolloszyJO (1998) Increased GLUT-4 translocation mediates enhanced insulin sensitivity of muscle glucose transport after exercise. J Appl Physiol 85: 1218–1222.

38. BelgacemYH, MartinJR (2006) Disruption of insulin pathways alters trehalose level and abolishes sexual dimorphism in locomotor activity in Drosophila. J Neurobiol 66: 19–32.

39. HondaY, TanakaM, HondaS (2010) Trehalose extends longevity in the nematode Caenorhabditis elegans. Aging Cell 9: 558–569.

40. LamitinaST, StrangeK (2005) Transcriptional targets of DAF-16 insulin signaling pathway protect C. elegans from extreme hypertonic stress. Am J Physiol Cell Physiol 288: C467–474.

41. ZhengXiao JLY, PenZhang, ZhangJie, LiXiao, LiCao Guang, YuXue Ren, LiangGong Cheng (2012) Effect of inhibiting the expression of insulin-like peptide gene BBX-B8 on development and reproduction of silkworm, Bombyx mori. Afr J Biotechnol 11: 2548–2554.

42. IwamiM (2000) Bombyxin: An Insect Brain Peptide that Belongs to the Insulin Family. Zoolog Sci 17: 1035–1044.

43. SatakeS, MasumuraM, IshizakiH, NagataK, KataokaH, et al. (1997) Bombyxin, an insulin-related peptide of insects, reduces the major storage carbohydrates in the silkworm Bombyx mori. Comp Biochem Physiol B Biochem Mol Biol 118: 349–357.

44. RocksteinM, SrivastavaPN (1967) Trehalose in the flight muscle of the house fly, Musca domestica L., in relation to age. Experientia 23: 636–637.

45. WyattGR, MeyerWL (1959) The chemistry of insect hemolymph. III. Glycerol. J Gen Physiol 42: 1005–1011.

46. WyattGR, KaleGF (1957) The chemistry of insect hemolymph. II. Trehalose and other carbohydrates. J Gen Physiol 40: 833–847.

47. WyattGR, LoughheedTC, WyattSS (1956) The chemistry of insect hemolymph; organic components of the hemolymph of the silkworm, Bombyx mori, and two other species. J Gen Physiol 39: 853–868.

48. ThompsonSN, RedakRA, WangLW (2001) Altered dietary nutrient intake maintains metabolic homeostasis in parasitized larvae of the insect Manduca sexta L. J Exp Biol 204: 4065–4080.

49. CleggJS, EvansDR (1961) Blood trehalose and flight metabolism in the blowfly. Science 134: 54–55.

50. ErkutC, PenkovS, KhesbakH, VorkelD, VerbavatzJM, et al. (2011) Trehalose renders the dauer larva of Caenorhabditis elegans resistant to extreme desiccation. Curr Biol 21: 1331–1336.

51. SarkarS, DaviesJE, HuangZ, TunnacliffeA, RubinszteinDC (2007) Trehalose, a novel mTOR-independent autophagy enhancer, accelerates the clearance of mutant huntingtin and alpha-synuclein. J Biol Chem 282: 5641–5652.

52. CasarejosMJ, SolanoRM, GomezA, PeruchoJ, de YebenesJG, et al. (2011) The accumulation of neurotoxic proteins, induced by proteasome inhibition, is reverted by trehalose, an enhancer of autophagy, in human neuroblastoma cells. Neurochem Int 58: 512–520.

53. Van HandelE (1985) Quenching of carbohydrate reactions by azide. Anal Biochem 148: 434–435.

54. Van HandelE (1985) Rapid determination of total lipids in mosquitoes. J Am Mosq Control Assoc 1: 302–304.