A switch in the control of growth of the wing imaginal disks of Manduca sexta

PLoS ONE

Volumn 5, Issue 5, 2010, Pages

  Tobler, Alexandra ^a,b   Frederik Nijhout, H ^a  

^a DUKE UNIVERSITY   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; INSULIN; JUVENILE HORMONE; TREHALOSE;

ANIMAL CELL; ANIMAL FOOD; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CARBOHYDRATE ANALYSIS; CELL PROLIFERATION; CONTROLLED STUDY; FORELIMB; GROWTH REGULATION; HEMOLYMPH; IMAGINAL DISC; INSULIN RELEASE; LARVAL STAGE; LIMB DEVELOPMENT; MANDUCA SEXTA; METABOLIC REGULATION; METAMORPHOSIS; NONHUMAN; SIGNAL TRANSDUCTION; STARVATION;

ABDOMEN; ANIMALS; BRAIN; CARBOHYDRATES; CELL PROLIFERATION; FOOD; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLUCOSE; HEMOLYMPH; INJECTIONS; JUVENILE HORMONES; LARVA; MANDUCA; NEUROPEPTIDES; ORGAN SIZE; RECEPTOR, INSULIN; RNA, MESSENGER; STARVATION; TREHALOSE; WING;

HEXAPODA; MANDUCA SEXTA;

EID: 77956495696     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0010723     Document Type: Article

References (56)

1. Kato Y, Riddiford LM (1987) The role of 20-hydroxyecdysone in stimulating epidermal mitoses during the laval-pupal transformation of the tobacco hornworm, Manduca sexta. Development 100: 227-236.
2. Nijhout HF, Grunert LW (2002) Bombyxin is a growth factor for wing imaginal disks in Lepidoptera. Proceedings of the National Academy of Sciences of the United States of America 99: 15446-15450.
3. Nijhout HF, Smith WA, Schachar I, Subramanian S, Tobler A, et al. (2007) The control of growth and differentiation of the wing imaginal disks of Manduca sexta. Developmental Biology 302: 569-576.
4. Britton JS, Lockwood WK, Li L, Cohen SM, Edgar BA (2002) Drosophila's insulin/P13-kinase pathway coordinates cellular metabolism with nutritional conditions. Developmental Cell 2: 239-249.
5. Ikeya T, Galic M, Belawat P, Nairz K, Hafen E (2002) Nutrient-dependent expression of insulin-like peptides from neuroendocrine cells in the CNS contributes to growth regulation in Drosophila. Current Biology 12: 1293-1300.
6. Bohni R, Riesgo-Escovar J, Oldham S, Brogiolo W, Stocker H, et al. (1999) Autonomous control of cell and organ size by CHICO, a Drosophila homolog of vertebrate IRS1-4. Cell 97: 865-875.
7. Masumura M, Satake SI, Saegusa H, Mizoguchi A (2000) Glucose stimulates the release of bombyxin, an insulin-related peptide of the silkworm Bombyx mori. General and Comparative Endocrinology 118: 393-399.
8. Iwami M, Furuya I, Kataoka H (1996) Bombyxin-related peptides, cDNA structure and expression in the brain of the hornworm Agrius convoluvuli. Insect Biochemistry and Molecular Biology 26: 25-32.
9. Kimura-Kawakami M, Iwami M, Kawakami A, Nagasawa H, Suzuki A, et al. (1992) Structure and expression of bombyxin-related peptide genes of the moth Samia cynthia ricini. General and Comparative Endocrinology 86: 257-268.
10. Nagasawa H, Kataoka H, Isogai A, Tamura S, Suzuki A, et al. (1986) Aminoacid sequence af a prothoracicotropic hormone of the silkworm Bombyx mori. Proceedings of the National Academy of Sciences of the United States of America 83: 5840-5843.
11. Garofalo R (2002) Genetic analysis of insulin signaling in Drosophila. Trends in Endocrinology & Metabolism 13: 156-162.
12. Rulifson EJ, Kim SK, Nusse R (2002) Ablation of insulin-producing neurons in flies: growth and diabetic phenotypes. Science 296: 1118-1120.
13. Brogiolo W, Stocker H, Ikeya T, Rintelen F, Fernandez R, et al. (2001) An evolutionarily conserved function of the Drosophila insulin receptor and insulinlike peptides in growth control. Current Biology 11: 213-221.
14. Dai J, Mizoguchi A, Gilbert L (1994) Immunoreactivity of neurosecretory granules in the brain-retrocerebral complex of Manduca sexta to heterologous antibodies against Bombyx prothoracicotropic hormone and bombyxin. Invertebrate Reproduction and Development 26: 187-187.
15. Baker F, LW T, Reuter C, Schooley D. (1987) In vivo fluctuation of JH, JH acid, and ecdysteroid titer, and JH esterase activity, during development of fifth stadium Manduca sexta. Insect Biochemistry 17: 989-996.
16. Bollenbacher WE, Smith SL, Goodman W, Gilbert LI (1981) Ecdysteroid titer during larval-pupal-adult development of the tobacco hornworm, Manduca sexta. General and Comparative Endocrinology 44: 302-306.
17. Nijhout F (1994) Insect hormones. New Jersey: Princeton University Press. pp 267.
18. Wolfgang WJ, Riddiford LM (1986) Larval cuticular morphogenesis in the tobacco hornworm, Manduca sexta, and its hormonal regulation. Developmental Biology 113: 305-316.
19. Britton JS, Edgar BA (1998) Environmental control of the cell cycle in Drosophila: nutrition activates mitotic and endoreplicative cells by distinct mechanisms. Development 125: 2149-2158.
20. Colombani J, Raisin S, Pantalacci S, Radimerski T, Montagne J, et al. (2003) A nutrient sensor mechanism controls Drosophila growth. Cell 114: 739-749.
21. Haunerland N, Shirk P (1995) Regional and functional differentiation in the insect fat body. Annual Review of Entomology 40: 121-145.
22. Dominick OS, Truman JW (1985) The physiology of wandering behaviour in Manduca sexta. II. The endocrine control of wandering behaviour. Journal of Experimental Biology 117: 45-68.
23. Browder MH, D'Amico LJ, Nijhout HF (2001) The role of low levels of juvenile hormone esterase in the metamorphosis of Manduca sexta. J Insect Sci 1: 11.
24. Jesudason P, Venkatesh K, Roe RM (1990) Haemolymph juvenile hormone esterase during the life cycle of the tobacco hornworm, Manduca sexta (L.). Insect Biochemistry 20: 593-604.
25. Davidowitz G, D'Amico LJ, Nijhout HF (2003) Critical weight in the development of insect body size. Evolution & Development 5: 188-197.
26. Nijhout H, Davidowitz G, Roff D (2006) A quantitative analysis of the mechanism that controls body size in Manduca sexta. Journal of Biology 5: 16.
27. Nijhout HF, Williams CM (1974) Control of moulting and metamorphosis in the tobacco hornworm, Manduca sexta (L.): growth of the last-instar larva and the decision to pupate. The Journal of Experimental Biology 61: 481-491.
28. Cymborowski B, Bogus M, Beckage NE, Williams CM, Riddiford LM (1982) Juvenile-hormone titers and metabolism during starvation-induced supernumerary larval molting of the tobacco hornworm Manduca sexta L. Journal of Insect Physiology 28: 129-135.
29. Kremen C, Nijhout H (1998) Control of pupal commitment in the imaginal disks of Precis coenia (Lepidoptera: Nymphalidae). Journal of Insect Physiology 44: 287-296.
30. 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.
31. Becker A, Schloder P, Steele JE, Wegener G (1996) The regulation of trehalose metabolism in insects. Experientia 52: 433-439.
32. Wigglesworth V (1965) The Principles of Insect Physiology. London: Methuen.
33. 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.
34. 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. The Journal of Experimental Biology 61: 493-501.
35. Davis K, Shearn A (1977) In vitro growth of imaginal disks from Drosophila melanogaster. Science 196: 438-440.
36. Dutkowski A, Oberlander H (1974) Interactions between beta-ecdysone and fat body during wing disk development in vitro. Journal of Insect Physiology 20: 743-749.
37. Smagghe G, Loeb M, Tirry L (2001) In vitro and in vivo effects of a fat body extract on Spodoptera littoralis. In Vitro Cellular & Developmental Biology-Animal 37: 90-92.
38. Zhang H, Stallock J, Ng J, Reinhard C, Neufeld T (2000) Regulation of cellular growth by the Drosophila target of rapamycin dTOR. Genes & Development 14: 2712-2724.
39. Shingleton AW, Mirth CK, Bates PW (2008) Developmental model of static allometry in holometabolous insects. Proceedings of the Royal Society B: Biological Sciences 275: 1875-1885.
40. Beadle GW, Tatum EL, Clancy CW (1938) Food level in relation to rate of development and eye pigmentation in Drosophila Melanogaster. Biological Bulletin 75: 447-462.
41. Mirth C, Truman JW, Riddiford LM (2005) The Role of the Prothoracic Gland in Determining Critical Weight for Metamorphosis in Drosophila melanogaster. Current Biology 15: 1796-1807.
42. Mirth CK, Truman JW, Riddiford LM (2009) The Ecdysone receptor controls the post-critical weight switch to nutrition-independent differentiation in Drosophila wing imaginal discs. Development 136: 2345-2353.
43. Shingleton AW, Frankino WA, Flatt T, Nijhout HF, Emlen DJ (2007) Size and shape: the developmental regulation of static allometry in insects. BioEssays 29: 536-548.
44. D'Amico LJ, Davidowitz G, Nijhout HF (2001) The developmental and physiological basis of body size evolution in an insect. Proceedings of the Royal Society of London Series B: Biological Sciences 268: 1589-1593.
45. Nijhout H (2003) The control of body size in insects. Developmental Biology 261: 1-9.
46. Nijhout HF, Williams CM (1974) Control of moulting and metamorphosis in the tobacco hornworm, Manduca sexta (L.): Growth of the last-instar larva and the decision to pupate. J Exp Biol 61: 481-491.
47. Watson RD, Bollenbacher WE (1988) Juvenile hormone regulates the steroidogenic competence of Manduca sexta prothoracic glands. Molecular and Cellular Endocrinology 57: 251-259.
48. 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.
49. Rountree D, Bollenbacher W (1986) The release of the prothoracicotropic hormone in the tobacco hornworm, Manduca sexta, is controlled intrinsically by juvenile hormone. Journal of Experimental Biology 120: 41-58.
50. Davidowitz G, D'Amico LJ, Nijhout HF (2004) The effects of environmental variation on a mechanism that controls insect body size. Evolutionary Ecology Research 6: 49-62.
51. Nijhout HF (1975) Dynamics of juvenile hormone action in larvae of the tobacco hornworm, Manduca sexta (L.). Biol Bull 149: 568-579.
52. Mirth C, Truman J, Riddiford L (2005) The role of the prothoracic gland in determining critical weight for metamorphosis in Drosophila melanogaster. Current Biology 15: 1796-1807.
53. Shingleton AW, Mirth CK, Bates PW (2008) Developmental model of static allometry in holometabolous insects. Proc Biol Sci 275: 1875-1885.
54. Layalle S, Arquier N, Lèopold P (2008) The TOR pathway couples nutrition and developmental timing in Drosophila. Developmental Cell 15: 568-577.
55. Shafiei M, Moczek AP, Nijhout HF (2001) Food availability controls the onset of metamorphosis in the dung beetle Onthophagus taurus (Coleoptera: Scarabaeidae). Physiological Entomology 26: 173-180.
56. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ddCT method. Methods 25: 402-408.