Applied Entomology and Zoology

, Volume 46, Issue 1, pp 87–93 | Cite as

Remodeling of the corpora cardiaca and the corpora allata during adult metamorphosis in Bombyx mori: identification of invisible corpora cardiaca by the expression of adipokinetic hormone

Original Research Paper

Abstract

It is problematic to identify the corpora cardiaca (CC) of pupal and adult stages of Bombyx mori because of the presence of tissues similar in appearance near the associated corpora allata (CA). To find the CC, we performed in situ hybridization experiments using the adipokinetic hormone II (AKH-II) gene as a probe, as AKH-II expression occurs only in the CC. Shortly after pupation, the CC and CA began to move toward the esophagus and had attached there tightly by 4 days; during this period, the distance between the CC and CA increased from 65 to 507 μm. The CC became flattened during the remodeling period, although the CA stayed globular until adult ecdysis. In situ hybridization analyses, after the CC had been correctly identified during adult development, showed that the mRNA expression of all the mevalonate enzymes and juvenile hormone acid O-methyltransferase involved in JH synthesis occurred only in CA cells, indicating that the fluctuations of enzyme mRNA amounts in CC-CA complexes (Kinjoh et al. in Insect Biochem Mol Biol 37:808–818, 2007) were derived solely from those in the CA.

Keywords

Corpora cardiaca Corpora allata Adipokinetic hormone Juvenile hormone Bombyx mori 

References

  1. Arrese EL, Soulages JL (2010) Insect fat body: energy, metabolism, and regulation. Annu Rev Entomol 55:207–225CrossRefPubMedGoogle Scholar
  2. Bollenbacher WE, Granger NA (1985) Endocrinology or the prothoracicotropic hormone. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology, vol 7. Pergamon Press, Oxford, pp 109–151Google Scholar
  3. Calvez B, Hirn M, De Reggi M (1976) Ecdysone changes in the haemolymph of two silkworms (Bombyx mori and Philosamia cynthia) during larval and pupal development. FEBS Lett 71:57–61CrossRefGoogle Scholar
  4. Cassier P (1979) The corpora allata in insects. Int Rev Cytol 57:1–73CrossRefGoogle Scholar
  5. Cazal P (1948) Les glandes endocrines retro-cerebrales des insectes. Bull Biol Fr Belg (Suppl) 32:1–227Google Scholar
  6. Dai JD, Gilbert LI (1991) Metamorphosis of the corpus allatum and degeneration of the prothoracic glands during the larval-pupal-adult transformation of Drosophila melanogaster: a cytophysiological analysis of the ring gland. Dev Biol 144:309–326CrossRefPubMedGoogle Scholar
  7. Dubrovsky EB (2005) Hormonal cross talk in insect development. Trend Endocrinol Metab 16:6–11CrossRefGoogle Scholar
  8. Duve H, Audsley N, Weaver R, Thorpe A (2003) Allatostatins and allatotropin in the corpus cardiacum/corpus allatum complex of larval and adult lepidopterans studied by confocal laser scanning microscopy: correlation to juvenile hormone biosynthesis. Cell Tissue Res 314:281–295CrossRefPubMedGoogle Scholar
  9. Gäde G, Marco HG, Simek PS, Audsley N, Clark KD, Weaver RJ (2008) Predicted versus expressed adipokinetic hormones, and other small peptides from the corpus cardiacum–corpus allatum: a case study with beetles and moths. Peptides 29:1124–1139CrossRefPubMedGoogle Scholar
  10. Gilbert LI, Warren JT (2005) A molecular genetic approach to the biosynthesis of the insect steroid molting hormone. Vitam Horm 73:31–57CrossRefPubMedGoogle Scholar
  11. Goldsworthy GJ, Mordue W, Guthkelch J (1972) Studies on insect adipokinetic hormones. Gen Comp Endocrinol 18:545–551CrossRefPubMedGoogle Scholar
  12. Goodman WG, Granger NA (2005) The juvenile hormones. In: Gilbert LI, Iatrou K, Gill SS (eds) Comprehensive Molecular Insect Science, vol 3. Elsevier Ltd., Oxford, pp 319–408CrossRefGoogle Scholar
  13. Hanaoka K, Ohnishi E (1974) Changes in ecdysone titre during pupal–adult development in the silkworm, Bombyx mori. J Insect Physiol 20:2375–2384CrossRefPubMedGoogle Scholar
  14. Hiruma K (2003) Juvenile hormone action in insect development. In: Henry HL, Norman AW (eds) Encyclopedia of hormones and related cell regulators, vol 2. Academic Press, San Diego, pp 528–535CrossRefGoogle Scholar
  15. Hiruma K, Riddiford LM (2009) The molecular mechanisms of cuticular melanization: the ecdysone cascade leading to dopa decarboxylase expression in Manduca sexta. Insect Biochem Mol Biol 39:245–253CrossRefPubMedGoogle Scholar
  16. Ichikawa T (1991) Architecture of cerebral neurosecretory cell systems in the silkworm Bombyx mori. J Exp Biol 161:217–237Google Scholar
  17. Ishibashi J, Kataoka H, Nagasawa H, Isogai A, Suzuki A (1992) Isolation and identification of adipokinetic hormone of the silkworm, Bombyx mori. Biosci Biotech Biochem 56:66–70CrossRefGoogle Scholar
  18. King-Jones K, Thummel CS (2005) Nuclear receptors—a perspective from Drosophila. Nature Rev Genet 6:311–323CrossRefPubMedGoogle Scholar
  19. Kinjoh T, Kaneko Y, Itoyama K, Mita K, Hiruma K, Shinoda T (2007) Control of juvenile hormone biosynthesis in Bombyx mori: cloning of the enzymes in the mevalonate pathway and assessment of their developmental expression in the corpora allata. Insect Biochem Mol Biol 37:808–818CrossRefPubMedGoogle Scholar
  20. 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 324:258–265CrossRefPubMedGoogle Scholar
  21. Muramatsu D, Kinjoh T, Shinoda T, Hiruma K (2008) The role of 20-hydroxyecdysone and juvenile hormone in pupal commitment of the epidermis of the silkworm, Bombyx mori. Mech Dev 125:411–420CrossRefPubMedGoogle Scholar
  22. Nijhout HF (1975) Axonal pathways in the brain-retrocerebral neuroendocrine complex of Manduca sexta (L.) (Lepidoptera: Sphingidae). Int J Insect Morphol Embryol 4:529–538CrossRefGoogle Scholar
  23. Pittendrigh CS (1965) On the mechanism of entrainment of a circadian rhythm by light cycle. In: Aschoff J (ed) Circadian clocks. North Holland, Amsterdam, pp 276–291Google Scholar
  24. Riddiford LM (1976) Hormonal control of insect epidermal cell commitment in vitro. Nature 259:115–117CrossRefPubMedGoogle Scholar
  25. Riddiford LM (2008) Juvenile hormone action: a 2007 perspective. J Insect Physiol 54:895–901CrossRefPubMedGoogle Scholar
  26. Riddiford LM, Hewes RS, Truman JW (1994) Dynamics and metamorphosis of an identifiable peptidergic neuron in an insect. J Neurobiol 25:819–830CrossRefPubMedGoogle Scholar
  27. Riddiford LM, Hiruma K, Zhou X, Nelson CA (2003) Insights into the molecular basis of the hormonal control of molting and metamorphosis from Manduca sexta and Drosophila melanogaster. Insect Biochem Mol Biochem 33:1327–1338CrossRefGoogle Scholar
  28. Roller L, Yamanaka N, Watanabe K, Daubnerova I, Zitnan D, Kataoka H, Tanaka Y (2008) The unique evolution of neuropeptide genes in the silkworm Bombyx mori. Insect Biochem Mol Biol 38:1147–1157CrossRefPubMedGoogle Scholar
  29. Schooley DA, Horodyski FM, Coast GM (2005) Hormones controlling homeostasis in insects. In: Gilbert LI, Iatrou K, Gill SS (eds) Comprehensive molecular insect science, vol 3. Elsevier, Amsterdam, pp 493–550CrossRefGoogle Scholar
  30. Sedlak BJ (1985) Structure of endocrine glands. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology biochemistry and pharmacology, vol 7. Pergamon Press, Oxford, pp 25–60Google Scholar
  31. Sehadová H, Markova EP, Sehnal F, Takeda M (2004) Distribution of circadian clock related proteins in the cephalic nervous system of the silkworm, Bombyx mori. J Biol Rhythms 19:466–482CrossRefPubMedGoogle Scholar
  32. Shinoda T, Itoyama K (2003) Juvenile hormone acid methyltransferase: a key regulatory enzyme for insect metamorphosis. Proc Natl Acad Sci USA 100:11986–11991CrossRefPubMedGoogle Scholar
  33. Stone JV, Mordue W, Batley KE, Morris HR (1976) Structure of locust adipokinetic hormone, a neurohormone that regulates lipid utilization during flight. Nature 263:207–211CrossRefPubMedGoogle Scholar
  34. Tobe SS, Stay B (1985) Structure and regulation of the corpus allatum. Adv Insect Physiol 18:305–432CrossRefGoogle Scholar
  35. Truman JW (2005) Hormonal control of the form and function of the nervous system. In: Gilbert LI, Iatrou K, Gill SS (eds) Comprehensive molecular insect science, vol 2. Elsevier, Amsterdam, pp 135–163CrossRefGoogle Scholar
  36. Truman JW, Hiruma K, Allee JP, MacWhinnie SGB, Champlin DT, Riddiford LM (2006) Juvenile hormone is required to couple imaginal disc formation with nutrition in insects. Science 312:1385–1388CrossRefPubMedGoogle Scholar
  37. Ueda H, Shinoda T, Hiruma K (2009) Spatial expression of the mevalonate enzymes involved in juvenile hormone biosynthesis in the corpora allata in Bombyx mori. J Insect Physiol 55:798–804CrossRefPubMedGoogle Scholar
  38. Van der Horst DJ, Van Marrewijk WJA, Diederen JHB (2001) Adipokinetic hormones of insects: release, signal transduction, and responses. Int Rev Cytol 211:179–240CrossRefPubMedGoogle Scholar
  39. Yamanaka N, Zitnan D, Kim Y-J, Adams ME, Hua Y-J, Suzuki Y, Suzuki M, Suzuki A, Satake H, Mizoguchi A, Asaoka K, Tanaka Y, Kataoka H (2006) Regulation of insect steroid hormone biosynthesis by innervating peptidergic neurons. Proc Natl Acad Sci USA 103:8622–8627CrossRefPubMedGoogle Scholar

Copyright information

© The Japanese Society of Applied Entomology and Zoology 2010

Authors and Affiliations

  1. 1.Faculty of Agriculture and Life SciencesHirosaki UniversityHirosakiJapan
  2. 2.National Institute of Agrobiological SciencesTsukubaJapan
  3. 3.Graduate School of Agricultural SciencesIwate UniversityMoriokaJapan

Personalised recommendations