Amino Acids and TOR Signaling Promote Prothoracic Gland Growth and the Initiation of Larval Molts in the Tobacco Hornworm Manduca sexta

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Kemirembe, Karen ^a   Liebmann, Kate ^a   Bootes, Abigail ^b   Smith, Wendy A ^b   Suzuki, Yuichiro ^a  

^a WELLESLEY COLLEGE   (United States)

^b NORTHEASTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ECDYSONE; RAPAMYCIN; TARGET OF RAPAMYCIN KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BODY GROWTH; CONTROLLED STUDY; ENDOCRINE SYSTEM; FEEDING; GROWTH INHIBITION; GROWTH RATE; HORMONAL REGULATION; LARVAL DEVELOPMENT; MANDUCA SEXTA; MOLTING; NONHUMAN; NUTRITIONAL REQUIREMENT; NUTRITIONAL STATUS; ORGANOGENESIS; PROTHORACIC GLAND GROWTH; SIGNAL TRANSDUCTION; STEROID RELEASE; STEROIDOGENESIS;

AMINO ACIDS; ANIMAL FEED; ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; ECDYSTERONE; ENDOCRINE SYSTEM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LARVA; MANDUCA; MODELS, BIOLOGICAL; MOLTING; SIGNAL TRANSDUCTION; SIROLIMUS; SUCROSE; TOR SERINE-THREONINE KINASES;

ARTHROPODA; MANDUCA SEXTA;

EID: 84866313002     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0044429     Document Type: Article

References (50)

1. Plant TM, (2002) Neurophysiology of puberty. J Adolesc Health 31: 185-191.
2. Kirkwood RN, Cumming DC, Aherne FX, (1987) Nutrition and puberty in the female. Proc Nutr Soc 46: 177-192.
3. Sisk CL, Foster DL, (2004) The neural basis of puberty and adolescence. Nat Neurosci 7: 1040-1047.
4. Nijhout HF, (1981) Physiological control of molting in insects. Am Zool 21: 631-640.
5. Riddiford LM, (2008) Juvenile hormone action: A 2007 perspective. J Insect Physiol 54: 895-901.
6. Nijhout HF (1998) Insect Hormones. Princeton, NJ.: Princeton University Press.
7. Heming BS (2003) Insect Development and Evolution. Ithaca, NY Cornell University Press.
8. Truman JW, (1981) Interaction between ecdysteroid, eclosion hormone, and bursicon titers in Manduca-sexta. Am Zool 21: 655-661.
9. Warren JT, Sakurai S, Rountree DB, Gilbert LI, Lee SS, et al. (1988) Regulation of the ecdysteroid titer of Manduca-sexta- reappraisal of the role of the prothoracic glands. Proc Natl Acad Sci U S A 85: 958-962.
10. Smith WA, Rybczynski R (2011) Prothoracicotropic hormone. In: Gilbert LI, editor. Insect Endocrinology. New York: Academic Press. 1-62.
11. Agui N, Granger NA, Gilbert LI, Bollenbacher WE, (1979) Cellular-localization of the insect prothoracicotropic hormone - in vitro assay of a single neurosecretory cell. Proc Natl Acad Sci U S A 76: 5694-5698.
12. Carrow GM, Calabrese RL, Williams CM, (1981) Spontaneous and evoked release of prothoracicotropin from multiple neurohemal organs of the tobacco hornworm. Proc Natl Acad Sci U S A 78: 5866-5870.
13. Sakurai S, Warren JT, Gilbert LI, (1989) Mediation of ecdysone synthesis in Manduca-sexta by a hemolymph enzyme. Arch Insect Biochem Physiol 10: 179-197.
14. Gilbert LI, Rybczynski R, Warren JT, (2002) Control and biochemical nature of the ecdysteroidogenic pathway. Ann Rev Entomol 47: 883-916.
15. Wigglesworth VB (1934) Memoirs: The physiology of ecdysis in Rhodnius prolixus (Hemiptera). II. Factors controlling moulting and 'metamorphosis'. Q J Microsc Sci 77.
16. Nijhout HF, (1979) Stretch-induced moulting in Oncopeltus fasciatus. J Insect Physiol 25: 277-281.
17. Callier V, Nijhout HF, (2011) Control of body size by oxygen supply reveals size-dependent and size-independent mechanisms of molting and metamorphosis. Proc Natl Acad Sci U S A 108: 14664-14669.
18. Nijhout HF, Williams CM, (1974) Control of molting and metamorphosis in tobacco hornworm, Manduca-sexta (L)- Cessation of juvenile-hormone secretion as a trigger for pupation. J Exp Biol 61: 493-501.
19. Mirth CK, Riddiford LM, (2007) Size assessment and growth control: how adult size is determined in insects. Bioessays 29: 344-355.
20. Mirth C, Truman JW, Riddiford LM, (2005) The role of the prothoracic gland in determining critical weight to metamorphosis in Drosophila melanogaster. Curr Biol 15: 1796-1807.
21. Colombani J, Bianchini L, Layalle S, Pondeville E, Dauphin-Villemant C, et al. (2005) Antagonistic actions of ecdysone and insulins determine final size in Drosophila. Science 310: 667-670.
22. Caldwell PE, Walkiewicz M, Stern M, (2005) Ras activity in the Drosophila prothoracic gland regulates body size and developmental rate via ecdysone release. Curr Biol 15: 1785-1795.
23. Walsh AL, Smith WA, (2011) Nutritional sensitivity of fifth instar prothoracic glands in the tobacco hornworm, Manduca sexta. J Insect Physiol 57: 809-818.
24. Layalle S, Arquier N, Leopold P, (2008) The TOR pathway couples nutrition and developmental timing in Drosophila. Dev Cell 15: 568-577.
25. Song QS, Gilbert LI, (1994) S6 phosphorylation results from prothoracicotropic hormone stimulation of insect prothoracic glands- a role for S6 kinase. Dev Genet 15: 332-338.
26. Nijhout HF, Williams CM, (1974) Control of moulting and metamorphosis in the tobacco hornworm, Manduca sexta (L.): Cessation of juvenile hormone secretion as a trigger for pupation. J Exp Biol 61: 493-501.
27. Davidowitz G, D'Amico LJ, Nijhout HF, (2003) Critical weight in the development of insect body size. Evol Dev 5: 188-197.
28. Warren JT, Smith W, Gilbert LI, (1984) Simplification of the ecdysteroid radioimmunoassay by the use of protein-a from Staphylococcus-aureus. Experientia 40: 393-394.
29. Gu SH, Lin JL, Lin PL, Chen CH, (2009) Insulin stimulates ecdysteroidogenesis by prothoracic glands in the silkworm, Bombyx mori. Insect Biochem Mol Biol 39: 171-179.
30. Gu SH, Young SC, Lin JL, Lin PL, (2011) Involvement of PI3K/Akt signaling in PTTH-stimulated ecdysteroidogenesis by prothoracic glands of the silkworm, Bombyx mori. Insect Biochem Mol Biol 41: 197-202.
31. Masumura M, Satake SI, Saegusa H, Mizoguchi A, (2000) Glucose stimulates the release of bombyxin, an insulin-related peptide of the silkworm Bombyx mori. Gen Comp Endocrinol 118: 393-399.
32. Parker NF, Shingleton AW, (2011) The coordination of growth among Drosophila organs in response to localized growth-perturbation. Dev Biol 357: 318-325.
33. Gu SH, Yeh WL, Young SC, Lin PL, Li S, (2012) TOR signaling is involved in PTTH-stimulated ecdysteroidogenesis by prothoracicglands in the silkworm, Bombyx mori. Insect Biochem Mol Biol 42: 296-303.
34. Colombani J, Raisin S, Pantalacci S, Radimerski T, Montagne J, et al. (2003) A nutrient sensor mechanism controls Drosophila growth. Cell 114: 739-749.
35. Watson RD, Ciancio MJ, Gunnar WP, Gilbert LI, Bollenbacher WE, (1985) Regulation of insect prothoracic glands- existence of a hemolymph stimulatory factor in Manduca-sexta. J Insect Physiol 31: 487-494.
36. Gruetzmacher MC, Gilbert LI, Bollenbacher WE, (1984) Indirect stimulation of the prothoracic glands of Manduca-sexta by juvenile-hormone- evidence for a fat-body stimulatory factor. J Insect Physiol 30: 771-778.
37. Bateman JM, McNeill H, (2004) Temporal control of differentiation by the insulin receptor/Tor pathway in Drosophila. Cell 119: 87-96.
38. Ackerman D, Gems D, (2012) Insulin/IGF-1 and hypoxia signaling act in concert to regulate iron homeostasis in Caenorhabditis elegans. PLoS Genet 8: e1002498.
39. Wouters BG, Koritzinsky M, (2008) Hypoxia signalling through mTOR and the unfolded protein response in cancer. Nat Rev Cancer 8: 851-864.
40. Arsham AM, Howell JJ, Simon MC, (2003) A novel hypoxia-inducible factor-independent hypoxic response regulating mammalian target of rapamycin and its targets. J Biol Chem 278: 29655-29660.
41. Reiling JH, Hafen E, (2004) The hypoxia-induced paralogs scylla and charybdis inhibit growth by down-regulating S6K activity upstream of TSC in Drosophila. Genes Dev 18: 2879-2892.
42. Gajdos ZKZ, Henderson KD, Hirschhorn JN, Palmert MR, (2010) Genetic determinants of pubertal timing in the general population. Mol Cell Endocrinol 324: 21-29.
43. Teles MG, Silveira LFG, Tusset C, Latronico AC, (2011) New genetic factors implicated in human GnRH-dependent precocious puberty: The role of kisspeptin system. Mol Cell Endocrinol 346: 84-90.
44. Sharpe RM, Franks S, (2002) Environment, lifestyle and infertility - an inter-generational issue. Nat Cell Biol 4: S33-S40.
45. Ebling FJP, (2005) The neuroendocrine timing of puberty. Reproduction 129: 675-683.
46. Kaplowitz PB, (2008) Link between body fat and the timing of puberty. Pediatrics 121: S208-S217.
47. Tena-Sempere M, Roa JA, (2010) Energy balance and puberty onset: emerging role of central mTOR signaling. Trends Endocrinol Metab 21: 519-528.
48. Roa J, Garcia-Galiano D, Varela L, Sanchez-Garrido MA, Pineda R, et al. (2009) The mammalian target of rapamycin as novel central regulator of puberty onset via modulation of hypothalamic Kiss1 system. Endocrinology 150: 5016-5026.
49. Seminara SB, Messager S, Chatzidaki EE, Thresher RR, Acierno JS, et al. (2003) The GPR54 gene as a regulator of puberty. N Engl J Med 349: 1614-U1618.
50. Shahab M, Mastronardi C, Seminara SB, Crowley WF, Ojeda SR, et al. (2005) Increased hypothalamic GPR54 signaling: A potential mechanism for initiation of puberty in primates. Proc Natl Acad Sci U S A 102: 2129-2134.