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

PLoS Genetics

Volumn 9, Issue 6, 2013, Pages

  Xu, Jingjing ^a   Sheng, Zhentao ^a   Palli, Subba Reddy ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BOVINE INSULIN; INSULIN; INSULIN LIKE PEPTIDE 2; JUVENILE HORMONE; JUVENILE HORMONE ACID METHYLTRANSFERASE; METHOPRENE; METHYLTRANSFERASE; PEPTIDE HORMONE; SOMATOMEDIN C; TREHALOSE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARBOHYDRATE METABOLISM; CARBOHYDRATE TRANSPORT; CONTROLLED STUDY; GENE EXPRESSION; HORMONE ACTION; HORMONE SYNTHESIS; LIFE EXTENSION; LIPID METABOLISM; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; RNA INTERFERENCE; SIGNAL TRANSDUCTION; STARVATION; SURVIVAL; TRIBOLIUM CASTANEUM;

ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INSULIN; INSULIN-LIKE GROWTH FACTOR I; JUVENILE HORMONES; METAMORPHOSIS, BIOLOGICAL; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TREHALOSE; TRIBOLIUM;

BOVINAE; COLEOPTERA; DROSOPHILA MELANOGASTER; TRIBOLIUM CASTANEUM;

EID: 84879630190     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003535     Document Type: Article

References (54)

1. Jindra M, Palli SR, Riddiford LM, (2013) The Juvenile hormone signaling pathway in insect development. Annu Rev Entomol 58: 181-204.
2. Riddiford LM, (2012) How does juvenile hormone control insect metamorphosis and reproduction? Gen Comp Endocrinol 179: 477-484.
3. Minakuchi C, Namiki T, Shinoda T, (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. Truman JW, Hiruma K, Allee JP, Macwhinnie SG, Champlin DT, et al. (2006) Juvenile hormone is required to couple imaginal disc formation with nutrition in insects. Science 312: 1385-1388.
5. Koyama T, Syropyatova MO, Riddiford LM, (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. Tobler A, Nijhout HF, (2010) A switch in the control of growth of the wing imaginal disks of Manduca sexta. PLoS One 5: e10723.
7. Parthasarathy R, Tan A, Sun Z, Chen Z, Rankin M, et al. (2009) Juvenile hormone regulation of male accessory gland activity in the red flour beetle, Tribolium castaneum. Mech Dev 126: 563-579.
8. Wilson TG, DeMoor S, Lei J, (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. Sheng Z, Xu J, Bai H, Zhu F, Palli SR, (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. Minakuchi C, Zhou X, Riddiford LM, (2008) Kruppel homolog 1 (Kr-h1) mediates juvenile hormone action during metamorphosis of Drosophila melanogaster. Mech Dev 125: 91-105.
11. Kayukawa T, Minakuchi C, Namiki T, Togawa T, Yoshiyama M, 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. Zhang Z, Xu J, Sheng Z, Sui Y, Palli SR, (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. Li M, Mead EA, Zhu J, (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, J P, Iwema T, Epa, V C, Takaki K, Rynes J, Jindra M, (2011) Ligand-binding properties of a juvenile hormone receptor, Methoprene-tolerant. Proc Natl Acad Sci U S A 108: 21128-21133.
15. Shin, S W, Zou Z, Saha TT, Raikhel AS, (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. Herman WS, Tatar M, (2001) Juvenile hormone regulation of longevity in the migratory monarch butterfly. Proc Biol Sci 268: 2509-2514.
17. Tatar M, Kopelman A, Epstein D, Tu MP, Yin CM, et al. (2001) A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science 292: 107-110.
18. Fontana L, Partridge L, Longo VD, (2010) Extending healthy life span-from yeast to humans. Science 328: 321-326.
19. Kramer JM, Davidge JT, Lockyer JM, Staveley BE, (2003) Expression of Drosophila FOXO regulates growth and can phenocopy starvation. BMC Dev Biol 3: 5.
20. Essers MA, Weijzen S, de Vries-Smits AM, Saarloos I, de Ruiter ND, et al. (2004) FOXO transcription factor activation by oxidative stress mediated by the small GTPase Ral and JNK. EMBO J 23: 4802-4812.
21. Henderson ST, Johnson TE, (2001) daf-16 integrates developmental and environmental inputs to mediate aging in the nematode Caenorhabditis elegans. Curr Biol 11: 1975-1980.
22. Sengupta A, Molkentin JD, Yutzey KE, (2009) FoxO transcription factors promote autophagy in cardiomyocytes. J Biol Chem 284: 28319-28331.
23. Gross DN, van den Heuvel AP, Birnbaum MJ, (2008) The role of FoxO in the regulation of metabolism. Oncogene 27: 2320-2336.
24. Becker A, Schloder P, Steele JE, Wegener G, (1996) The regulation of trehalose metabolism in insects. Experientia 52: 433-439.
25. Kikawada T, Saito A, Kanamori Y, Nakahara Y, Iwata K, 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. Bounias M, Bahjou A, Gourdoux L, Moreau R, (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. Trumbo ST, Robinson GE, (2004) Nutrition, hormones and life history in burying beetles. J Insect Physiol 50: 383-391.
28. Tu MP, Yin CM, Tatar M, (2005) Mutations in insulin signaling pathway alter juvenile hormone synthesis in Drosophila melanogaster. Gen Comp Endocrinol 142: 347-356.
29. Wang Y, Brent CS, Fennern E, Amdam GV, (2012) Gustatory perception and fat body energy metabolism are jointly affected by vitellogenin and juvenile hormone in honey bees. PLoS Genet 8: e1002779.
30. Enell LE, Kapan N, Soderberg JA, Kahsai L, Nassel DR, (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. Broughton S, Alic N, Slack C, Bass T, Ikeya T, 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. Broughton SJ, Piper MD, Ikeya T, Bass TM, Jacobson J, 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. Rubin BR, Bogan JS, (2009) Intracellular retention and insulin-stimulated mobilization of GLUT4 glucose transporters. Vitam Horm 80: 155-192.
34. Zaid H, Antonescu CN, Randhawa VK, Klip A, (2008) Insulin action on glucose transporters through molecular switches, tracks and tethers. Biochem J 413: 201-215.
35. Stralfors P, (1988) Insulin stimulation of glucose uptake can be mediated by diacylglycerol in adipocytes. Nature 335: 554-556.
36. Goodyear LJ, Kahn BB, (1998) Exercise, glucose transport, and insulin sensitivity. Annu Rev Med 49: 235-261.
37. Hansen PA, Nolte LA, Chen MM, Holloszy JO, (1998) Increased GLUT-4 translocation mediates enhanced insulin sensitivity of muscle glucose transport after exercise. J Appl Physiol 85: 1218-1222.
38. Belgacem YH, Martin JR, (2006) Disruption of insulin pathways alters trehalose level and abolishes sexual dimorphism in locomotor activity in Drosophila. J Neurobiol 66: 19-32.
39. Honda Y, Tanaka M, Honda S, (2010) Trehalose extends longevity in the nematode Caenorhabditis elegans. Aging Cell 9: 558-569.
40. Lamitina ST, Strange K, (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. Zheng Xiao JLY, Pen Zhang, Zhang Jie, Li Xiao, Li Cao Guang, Yu Xue Ren, Liang Gong 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. Iwami M, (2000) Bombyxin: An Insect Brain Peptide that Belongs to the Insulin Family. Zoolog Sci 17: 1035-1044.
43. Satake S, Masumura M, Ishizaki H, Nagata K, Kataoka H, 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. Rockstein M, Srivastava PN, (1967) Trehalose in the flight muscle of the house fly, Musca domestica L., in relation to age. Experientia 23: 636-637.
45. Wyatt GR, Meyer WL, (1959) The chemistry of insect hemolymph. III. Glycerol. J Gen Physiol 42: 1005-1011.
46. Wyatt GR, Kale GF, (1957) The chemistry of insect hemolymph. II. Trehalose and other carbohydrates. J Gen Physiol 40: 833-847.
47. Wyatt GR, Loughheed TC, Wyatt SS, (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. Thompson SN, Redak RA, Wang LW, (2001) Altered dietary nutrient intake maintains metabolic homeostasis in parasitized larvae of the insect Manduca sexta L. J Exp Biol 204: 4065-4080.
49. Clegg JS, Evans DR, (1961) Blood trehalose and flight metabolism in the blowfly. Science 134: 54-55.
50. Erkut C, Penkov S, Khesbak H, Vorkel D, Verbavatz JM, et al. (2011) Trehalose renders the dauer larva of Caenorhabditis elegans resistant to extreme desiccation. Curr Biol 21: 1331-1336.
51. Sarkar S, Davies JE, Huang Z, Tunnacliffe A, Rubinsztein DC, (2007) Trehalose, a novel mTOR-independent autophagy enhancer, accelerates the clearance of mutant huntingtin and alpha-synuclein. J Biol Chem 282: 5641-5652.
52. Casarejos MJ, Solano RM, Gomez A, Perucho J, de Yebenes JG, 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 Handel E, (1985) Quenching of carbohydrate reactions by azide. Anal Biochem 148: 434-435.
54. Van Handel E, (1985) Rapid determination of total lipids in mosquitoes. J Am Mosq Control Assoc 1: 302-304.