Juvenile hormone synthesis, metabolism, and resulting haemolymph titre in Heliothis virescens larvae parasitized by Toxoneuron nigriceps

Journal of Insect Physiology

Volumn 49, Issue 11, 2003, Pages 1021-1030

  Li, Sheng ^a,c   Falabella, Patrizia ^a   Kuriachan, Indira ^b   Vinson, S Bradleigh ^b   Borst, David W ^c   Malva, Carla ^d   Pennacchio, Francesco ^a  

^a UNIVERSITY OF BASILICATA   (Italy)

^b TEXAS A AND M UNIVERSITY   (United States)

^c ILLINOIS STATE UNIVERSITY   (United States)

^d INSTITUTE OF GENETICS AND BIOPHYSICS ADRIANO BUZZATI TRAVERSO   (Italy)

Author keywords

Endocrine alterations; Host regulation; Hymenoptera; Juvenile hormone; Parasitoid

Indexed keywords

HORMONE; PARASITISM;

ANIMALIA; HELIOTHIS; HELIOTHIS VIRESCENS; HYMENOPTERA; NICOTIANA TABACUM; TOXONEURON; TOXONEURON NIGRICEPS; VESPIDAE;

EID: 0242350253     PISSN: 00221910     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-1910(03)00185-9     Document Type: Article

References (63)

1. Audsley, N., Weaver, R.J., Edwards, J.P., 2000. Juvenile hormone biosynthesis by corpora allata of larval tomato moth, Lacanobia oleracea, and regulation by Manduca sexta allatostatin and allatotropin. Insect Biochemistry and Molecular Biology 30, 681-689.
2. Balgopal, M.M., Dover, B.A., Goodman, W.G., Strand, M.R., 1996. Parasitism by Microplitis demolitor induces alterations in the juvenile hormone titers and juvenile hormone esterase activity of its host, Pseudoplusia includens. Journal of Insect Physiology 42, 337-345.
3. Bollenbacher, W.E., 1988. The interendocrine regulation of larvalpupal development in the tobacco hornworm, Manduca sexta: a model. Journal of Insect Physiology 34, 941-947.
4. Borst, D.W., Eskew, M.R., Wagner, S.J., Shores, K., Hunter, J., Luker, L., Hatle, J.D., Hecht, L.B., 2000. Quantification of juvenile hormone III, vitellogenin, and vitellogenin-mRNA during the oviposition cycle of the lubber grasshopper. Insect Biochemistry and Molecular Biology 30, 813-819.
5. Cole, T.J., Beckage, N.E., Tan, F.F., Srinivasan, A., Ramaswamy, S.B., 2002. Parasitoid-host endocrine relations: self-reliance or co-optation? Insect Biochemistry and Molecular Biology 32, 1673-1679.
6. Cusson, M., Miller, D., Goodman, W.G., 1997. Characterization of antibody 444 using chromatographically purified enantiomers of juvenile hormone I, II and III: implication for radioimmunoassay. Analytical Biochemistry 249, 83-87.
7. Cusson, M., Laforge, M., Miller, D., Cloutier, C., Stoltz, D., 2000. Functional significance of parasitism-induced suppression of juvenile hormone esterase activity in developmentally delayed Choristoneura fumiferana larvae. General and Comparative Endocrinology 117, 343-354.
8. Dong, K., Zhang, D., Dahlman, D.L., 1996. Down-regulation of juvenile hormone esterase and arylphorin in Heliothis virescens larvae parasitized by Microplitis croceipes. Archives of Insect Biochemistry and Physiology 32, 237-248.
9. Dover, B.A., Davies, D.H., Vinson, S.B., 1988. Degeneration of last instar Heliothis virescens prothoracic glands by Campoletis sonorensis polydnavirus. Journal of Invertebrate Pathology 51, 80-91.
10. Dover, B.A., Menon, A., Brown, R.C., Strand, M.R., 1995a. Suppression of juvenile hormone esterase in Heliothis virescens by Microplitis demolitor calyx fluid. Journal of Insect Physiology 41, 809-817.
11. Dover, B.A., Tanaka, T., Vinson, S.B., 1995b. Stadium-specific degeneration of host prothoracic glands by Campoletis sonorensis calyx fluid and its association with host ecdysteroid titers. Journal of Insect Physiology 41, 947-955.
12. Edwards, J.P., Weaver, R.J., Marris, G.C., 2001. Endocrine changes in lepidopteran larvae: challenges to parasitoid development and survival. In: Edwards, J.P., Weaver, R.J. (Eds.), Endocrine Interactions of Insect Parasites and Pathogens. Experimental Biology Reviews. BIOS Scientific Publications, Oxford, UK, pp. 1-32.
13. Falabella, P., Varricchio, P., Gigliotti, S., Tranfaglia, A., Pennacchio, F., Malva, C., 2003. Toxoneuron (=Cardiochiles) nigriceps polydnavirus encodes a putative aspartyl protease highly expressed in parasitised host larvae. Insect Molecular Biology 12, 9-17.
14. Feyereisen, R., 1985. Radiochemical assay for juvenile hormone in vitro. Methods in Enzymology 111, 530-539.
15. Gilbert, L.I., Granger, N.A., Roe, R.M., 2000. The juvenile hormone: historical facts and speculations on future research directions. Insect Biochemistry and Molecular Biology 30, 617-644.
16. Gilbert, L.I., Rybczynski, R., Warren, J.T., 2002. Control and biochemical nature of the ecdysteroidogenic pathway. Annual Review of Entomology 47, 883-916.
17. Gruetzmacher, M.C., Gilbert, L.I., Bollenbacher, W.E., 1984. Indirect stimulation of the prothoracic glands of Manduca sexta by juvenile hormone: evidence for a fat body stimulatory factor. Journal of Insect Physiology 30, 771-778.
18. Halarnkar, P.P., Schooley, D.A., 1990. Reverse-phase liquid chromatographic separation of juvenile hormone and its metabolites, and its application for an in vivo juvenile hormone catabolism study in Manduca sexta. Analytical Biochemistry 188, 394-397.
19. Hammock, B.D., Sparks, T.C., 1977. A rapid assay for insect juvenile hormone esterase activity. Analytical Biochemistry 82, 573-579.
20. Hayakawa, Y., 1995. Growth-blocking peptide: an insect biogenic peptide that prevents the onset of metamorphosis. Journal of Insect Physiology 41, 1-6.
21. Hoffmann, K.H., Fibinger, S.C., Hoffmann, G., 1994. Haemolymph juvenile hormone III esterase activity during adult life of female and male crickets, Gryllus bimaculatus de Geer (Ensifera, Gryllidae). Comparative Biochemistry and Physiology 109A, 285-291.
22. Hoffmann, K.H., Lorenz, M.W., Braig, W., 1995. Synthesis and degradation of juvenile hormone III during the final two larval stages of female and male crickets, Gryllus bimaculatus de Geer (Ensifera, Gryllidae). Comparative Biochemistry and Physiology 112B, 355-360.
23. Huang, Z.-H., Robinson, G.E., Borst, D.W., 1994. Physiological correlated of division of labor among similarly aged honey bees. Journal of Comparative Physiology 174A, 731-739.
24. Ismail, S.M., Goin, C., Muthumani, K., Kim, M., Dahm, K.H., Bhaskaran, G., 2000. Juvenile hormone acid and ecdysteroid together induce competence for metamorphosis of the Verson's gland in Manduca sexta. Journal of Insect Physiology 46, 59-68.
25. Li, S., Jiang, R.-J., Cao, M.-X., 2002a. Developmental changes in the ability to synthesize juvenile hormone in vitro by corpora allata from the Eri silkworm, Samia cynthia ricini. European Journal of Entomology 99, 413-419.
26. Li, S., Jiang, R.-J., Cao, M.-X., 2002b. Allatotropic and allatostatic activities in brain extracts of the Eri silkworm, Samia cynthia ricini, and the effects of Manduca sexta allatotropin and Manduca sexta allatostatin on juvenile hormone in vitro. Physiological Entomology 27, 322-329.
27. Nijhout, H.F., 1976. The role of ecdysone in pupation of Manduca sexta. Journal of Insect Physiology 22, 453-463.
28. Oeh, U., Lorenz, M.W., Dyker, H., Lösel, P., Hoffmann, K.H., 2000. Interaction between Manduca sexta allatotropin and Manduca sexta allatostatin in the fall armyworm Spodoptera frugiperda. Insect Biochemistry and Molecular Biology 30, 719-727.
29. Pennacchio, F., Vinson, S.B., Tremblay, E., 1992. Host regulation effects of Heliothis virescens (F.) larvae induced by teratocytes of Cardiochiles nigriceps Viereck (Lepidoptera, Noctuidae-Hymenoptera, Braconidae). Archives of Insect Biochemistry and Physiology 19, 177-192.
30. Pennacchio, F., Vinson, S.B., Tremblay, E., 1993. Growth and development of Cardiochiles nigriceps Viereck (Hymenoptera, Braconidae) larvae and their synchronization with some changes of the hemolymph composition of their host, Heliothis virescens (F.) (Lepidoptera, Noctuidae). Archives of Insect Biochemistry and Physiology 24, 65-77.
31. Pennacchio, F., Vinson, S.B., Tremblay, E., Ostuni, A., 1994a. Alteration of ecdysone metabolism in Heliothis virescens (F.) (Lepidoptera, Noctuidae) larvae induced by Cardiochiles nigriceps Viereck (Hymenoptera, Braconidae) teratocytes. Insect Biochemistry and Molecular Biology 24, 383-394.
32. Pennacchio, F., Vinson, S.B., Tremblay, E., 1994b. Morphology and ultrastructure of the serosal cells (teratocytes) in Cardiochiles nigriceps Viereck (Hymenoptera, Braconidae) embryos. International Journal of Insect Morphology and Embryology 23, 93-104.
33. Pennacchio, F., Sordetti, R., Falabella, P., Vinson, S.B., 1997. Biochemical and ultrastructural alterations in prothoracic glands of Heliothis virescens (F.) (Lepidoptera, Noctuidae) last instar larvae parasitized by Cardiochiles nigriceps Viereck (Hymenoptera, Braconidae). Insect Biochemistry and Molecular Biology 27, 439-450.
34. Pennacchio, F., Falabella, P., Sordetti, R., Varricchio, P., Malva, C., Vinson, S.B., 1998a. Prothoracic gland inactivation in Heliothis virescens (F.) (Lepidoptera, Noctuidae) larvae parasitized by Cardiochiles nigriceps Viereck (Hymenoptera, Braconidae). Journal of Insect Physiology 44, 845-857.
35. Pennacchio, F., Falabella, P., Vinson, S.B., 1998b. Regulation of Heliothis virescens prothoracic glands by Cardiochiles nigriceps polydnavirus. Archives of Insect Biochemistry and Physiology 38, 1-10.
36. Pennacchio, F., Malva, C., Vinson, S.B., 2001. Regulation of host endocrine system by the endophagous braconid Cardiochiles nigriceps and its polydnavirus. In: Edwards, J.P., Weaver, R.J. (Eds.), Endocrine Interactions of Insect Parasites and Pathogens. Experimental Biology Reviews. BIOS Scientific Publications, Oxford, UK, pp. 123-132.
37. Pratt, G.E., Tobe, S.S., 1974. Juvenile hormones radiobiosynthesized by corpora allata of adult female locusts in vitro. Life Science 14, 575-586.
38. Pringle, J.W.S., 1938. Proprioreception in insects. Journal of Experimental Biology 15, 101-113.
39. Riddiford, L.M., 1978. Ecdysone-induced change in cellular commitment of the epidermis of the tobacco hornworm, Manduca sexta, at the initiation of metamorphosis. General and Comparative Endocrinology 34, 438-446.
40. Riddiford, L.M., 1985. Hormone action at the cellular level. In: Kerkut, G.A., Gilbert, L.I. (Eds.), Comprehensive Insect Physiology, Biochemistry and Pharmacology, vol. 8. Pergamon Press, Oxford, UK, pp. 37-84.
41. Rountree, D.B., Combest, W.L., Gilbert, L.I., 1987. Protein phosphorylation in the prothoracic glands as a cellular model for juvenile hormone-prothoracicotropic hormone interactions. Insect Biochemistry 17, 943-948.
42. Rybczynski, R., Gilbert, L.I., 1994. Changes in general and specific protein synthesis that accompany ecdysteroid synthesis in stimulated prothoracic glands of Manduca sexta. Insect Biochemistry and Molecular Biology 24, 175-189.
43. Schepers, E.J., Dahlman, D.L., Zhang, D., 1998. Microplitis croceipes teratocytes: in vitro culture and biological activity of teratocyte secreted protein. Journal of Insect Physiology 44, 767-777.
44. Schooley, D.A., Baker, F.C., 1985. Juvenile hormone biosynthesis. In: Kerkut, G.A., Gilbert, L.I. (Eds.), Comprehensive Insect Physiology, Biochemistry and Pharmacology, vol. 7. Pergamon Press, Oxford, UK, pp. 363-389.
45. Schopf, A., Rembold, H., 1993. Changes in the juvenile hormone titer of gypsy moth larvae by parasitism of Glyptapanteles liparidis. Naturwissenschaften 80, 527-528.
46. Song, Q., Gilbert, L.I., 1994. S6 phosphorylation results from prothoracicotropic hormone stimulation of insect prothoracic glands: a role for S6 kinase. Developmental Genetics 15, 332-338.
47. Sparagana, S.P., Bhaskaran, G., Dahm, K., Ridde, V., 1984. Juvenile hormone acid production, juvenile hormone esterase, and juvenile hormone acid methyltransferase in corpora allata of Manduca sexta. Journal of Experimental Zoology 230, 309-313.
48. Sparagana, S.P., Bhaskaran, G., Barrera, P., 1985. Juvenile hormone acid methyltransferase activity in imaginai discs of Manduca sexta prepupae. Archives of Insect Biochemistry and Physiology 2, 191-202.
49. Steiner, B., Pfister-Wilhelm, R., Grossniklaus-Bürgin, C., Rembold, H., Treiblmayr, K., Lanzrein, B., 1999. Titers of juvenile hormone I, II and III in Spodoptera littoralis (Noctuidae) from the egg to pupal moult and their modification by the egg-larval parasitoid Chelonis inanitus (Braconidae). Journal of Insect Physiology 45, 401-413.
50. Tanaka, T., Vinson, S.B., 1991. Depression of prothoracic gland activity of Heliothis virescens by venom and calyx fluids from the parasitoid, Cardiochiles nigriceps. Journal of Insect Physiology 37, 139-144.
51. Tanaka, T., Agui, N., Hiruma, K., 1987. The parasitoid Apanteles kariyai inhibits pupation of its host, Pseudaletia separata, via disruption of prothoracicotropic hormone release. General and Comparative Endocrinology 67, 364-374.
52. Tobe, S.S., Pratt, G.E., 1974. The influence of substrate concentrations on the rate of insect juvenile hormone biosynthesis by corpora allata of the desert locust in vitro. Biochemistry Journal 144, 107-113.
53. Truman, J.W., Riddiford, L.M., Safranek, L., 1974. Temporal patterns of response to ecdysone and juvenile hormone in the epidermis of tobacco hornworm, Manduca sexta. Developmental Biology 39, 247-262.
54. Varricchio, P., Falabella, P., Sordetti, R., Graziani, F., Malva, C., Pennacchio, F., 1999. Cardiochiles nigriceps polydnavirus: molecular characterization and gene expression in parasitized Heliothis virescens larvae. Insect Biochemistry and Molecular Biology 29, 1087-1096.
55. Vinson, S.B., Guillot, F.S., Hays, D.B., 1973. Rearing of Cardiochiles nigriceps in the laboratory, with Heliothis virescens as hosts. Annals of the Entomological Society of America 66, 1170-1172.
56. Vinson, S.B., Pennacchio, F., Cônsoli, F.L., 2001. The parasitoid-host interaction from a nutritional perspective. In: Edwards, J.P., Weaver, RJ. (Eds.), Endocrine Interactions of Insect Parasites and Pathogens. Experimental Biology Reviews. BIOS Scientific Publications, Oxford, UK, pp. 187-205.
57. Watson, R.D., Ciancio, M.J., Gunnar, W.P., Gilbert, L.I., Bollenbacher, W.E., 1985. Regulation of insect prothoracic glands: existence of a haemolymph stimulatory factor in Manduca sexta. Journal of Insect Physiology 31, 487-494.
58. Watson, R.D., Spaziani, E., Bollenbacher, W.E., 1989. Regulation of ecdysone biosynthesis in insects and crustaceans: a comparison. In: Koolman, J. (Ed.), Ecdysone from Chemistry to Mode of Action. George Thieme Verlag, Stuttgart-New York, pp. 188-203.
59. Webb, B.A., Dahlman, D.L., 1985. Developmental pathology of Heliothis virescens larvae by Microplitis croceipes: parasitized-mediated host developmental arrest. Archives of Insect Biochemistry and Physiology 2, 131-139.
60. Webb, B.A., Riddiford, L.M., 1988. Synthesis of two storage proteins during larval development of the tobacco hornworm, Manduca sexta. Developmental Biology 130, 671-681.
61. Whitfield, J.B., Dangerfield, P.D., 1997. Subfamily Cardiochilinae. In: Wharton, R.A., Marsh, P., Sharkey, M. (Eds.), Identification Manual to the New World Genera of the Family of Braconidae (Hymenoptera). Special Publications No. 1. International Society of Hymenopterists, Washington, DC, pp. 177-183.
62. Zhang, D., Dahlman, D.L., 1989. Microplitis crosceipes teratocytes cause developmental arrest of Heliothis virescens larvae. Archives of Insect Biochemistry and Physiolgy 12, 51-61.
63. Zhang, D., Dahlman, D.L., Gelman, D.B., 1992. Juvenile hormone esterase activity and ecdysteroid titer in Heliothis virescens larvae injected with Microplitis croceipes teratocytes. Archives of Insect Biochemistry and Physiology 20, 231-242.