Effects of elevated ecdysteroid on tissue expression of three guanylyl cyclases in the tropical land crab Gecarcinus lateralis: Possible roles of neuropeptide signaling in the molting gland

Journal of Experimental Biology

Volumn 210, Issue 18, 2007, Pages 3245-3254

  Sung, Gu Lee ^a   Bader, Brandon D ^a   Chang, Ernest S ^b   Mykles, Donald L ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b UNIVERSITY OF CALIFORNIA DAVIS   (United States)

Author keywords

Arthropoda; Crustacea; Crustacean hyperglycemic hormone; Digestive gland; Ecdysone receptor; Ecdysteroid; Gene expression; Guanylyl cyclase; Molt inhibiting hormone; Molting; mRNA; Nervous system; Skeletal muscle; Y organ

Indexed keywords

ECDYSTERONE; GUANYLATE CYCLASE; NEUROPEPTIDE;

ANIMAL; ARTICLE; BRACHYURA; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; HEART; HEART MUSCLE; METABOLISM; MOLTING; PHYSIOLOGY; SIGNAL TRANSDUCTION; SKELETAL MUSCLE;

ANIMALS; BRACHYURA; ECDYSTERONE; GENE EXPRESSION REGULATION; GUANYLATE CYCLASE; HEART; MOLTING; MUSCLE, SKELETAL; MYOCARDIUM; NEUROPEPTIDES; SIGNAL TRANSDUCTION;

ANIMALIA; ARTHROPODA; CRUSTACEA; DECAPODA (CRUSTACEA); GECARCINIDAE; GECARCINUS LATERALIS;

EID: 35648956688     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.007740     Document Type: Article

References (71)

1. Aonuma, H. (2002). Distribution of NO-induced cGMP-like immunoreactive neurones in the abdominal nervous system of the crayfish, Procambarus clarkii. Zool. Sci. 19, 969-979.
2. Asazuma, H., Nagata, S., Katayama, H., Ohira, T. and Nagasawa, H. (2005). Characterization of a molt-inhibiting hormone (MIH) receptor in the Y-organ of the kuruma prawn, Marsupenaeus japonicus. Ann. N. Y. Acad. Sci. 1040, 215-218.
3. Baghdassarian, D., de Besse, N., Saidi, B., Somme, G. and Lachaise, F. (1996). Neuropeptide-induced inhibition of steroidogenesis in crab molting glands: involvement of cGMP-dependent protein kinase. Gen. Comp. Endocrinol. 104, 41-51.
4. Böcking, D. and Sedlmeier, D. (1994). Protein phosphorylation in the molting gand of the crayfish, Orconectes limosus - role of cyclic nucleotides, calcium, and molt inhibiting hormone (MIH). Invert. Reprod. Dev. 26, 237-245.
5. Bulau, P., Meisen, I., Reichwein-Roderburg, B., Peter-Katalinic, J. and Keller, R. (2003). Two genetic variants of the crustacean hyperglycemic hormone (CHH) from the Australian crayfish, Cherax destructor, detection of chiral isoforms due to posttranslational modification. Peptides 24, 1871-1879.
6. Bulau, P., Okuno, A., Thome, E., Schmitz, T., Peter-Katalinic, J. and Keller, R. (2005). Characterization of a molt-inhibiting hormone (MIH) of the crayfish, Orconectes limosus, by cDNA cloning and mass spectrometric analysis. Peptides 26, 2129-2136.
7. Chang, E. S. (1993). Comparative endocrinology of molting and reproduction: Insects and crustaceans. Annu. Rev. Entomol. 38, 161-180.
8. Chang, E. S. and O'Connor, J. D. (1979). Arthropod molting hormones. In Methods of Hormone Radioimmunoassay (ed. B. M. Jaffe and H. R. Behrman), pp. 797-814. New York: Academic Press.
9. Chang, E. S., Keller, R. and Chang, S. A. (1998). Quantification of crustacean hyperglycemic hormone by ELISA in hemolymph of the lobster, Homarus americanus, following various stresses. Gen. Comp. Endocrinol. 111, 359-366.
10. Chen, H. Y., Watson, R. D., Chen, J. C., Liu, H. F. and Lee, C. Y. (2007). Molecular characterization and gene expression pattern of two putative molt-inhibiting hormones from Litopenaeus vannamei. Gen. Comp. Endocrinol. 151, 72-81.
11. Chung, J. S. and Webster, S. G. (2003). Moult cycle-related changes in biological activity of moult-inhibiting hormone (MIH) and crustacean hyperglycaemic hormone (CHH) in the crab, Carcinus maenas. From target to transcript. Eur. J. Biochem. 270, 3280-3288.
12. Chung, J. S. and Webster, S. G. (2005). Dynamics of in vivo release of molt-inhibiting hormone and crustacean hyperglycemic hormone in the shore crab, Carcinus maenas. Endocrinology 146, 5545-5551.
13. Chung, J. S., Wilkinson, M. C. and Webster, S. G. (1998). Amino acid sequences of both isoforms of crustacean hyperglycemic hormone (CHH) and corresponding precursor-related peptide in Cancer pagurus. Regul. Pept. 77, 17-24.
14. Chung, J. S., Dircksen, H. and Webster, S. G. (1999). A remarkable, precisely timed release of hyperglycemic hormone from endocrine cells in the gut is associated with ecdysis in the crab Carcinus maenas. Proc. Natl. Acad. Sci. USA 96, 13103-13107.
15. Collmann, C., Carlsson, M. A., Hansson, B. S. and Nighorn, A. (2004). Odorant-evoked nitric oxide signals in the antennal lobe of Manduca sexta. J. Neurosci. 24, 6070-6077.
16. Dell, S., Sedlmeier, D., Böcking, D. and Dauphin-Villemant, C. (1999). Ecdysteroid biosynthesis in crayfish Y-organs: feedback regulation by circulating ecdysteroids. Arch. Insect Biochem. Physiol. 41, 148-155.
17. Dircksen, H., Böcking, D., Heyn, U., Mandel, C., Chung, J. S., Baggerman, G., Verhaert, P., Daufeldt, S., Plösch, T., Jaros, P. P. et al. (2001). Crustacean hyperglycaemic hormone (CHH)-like peptides and CHH-precursor-related peptides from pericardial organ neurosecretory cells in the shore crab, Carcinus maenas, are putatively spliced and modified products of multiple genes. Biochem. J. 356, 159-170.
18. Durica, D. S., Wu, X. H., Anilkumar, G., Hopkins, P. M. and Chung, A. C. K. (2002). Characterization of crab EcR and RXR homologs and expression during limb regeneration and oocyte maturation. Mol. Cell. Endocrinol. 189, 59-76.
19. Fanjul-Moles, M. L. (2006). Biochemical and functional aspects of crustacean hyperglycemic hormone in decapod crustaceans: review and update. Comp. Biochem. Physiol. 142C, 390-400.
20. Goy, M. F. (1990). Activation of membrane guanylate cyclase by an invertebrate peptide hormone. J. Biol. Chem. 265, 20220-20227.
21. Goy, M. F. (2005). Nitric oxide: an inhibitory retrograde modulator in the crustacean heart. Comp. Biochem. Physiol. 142A, 151-163.
22. Goy, M. F., Mandelbrot, D. A. and York, C. M. (1987). Identification and characterization of a polypeptide from a lobster neurosecretory gland that induces cyclic-GMP accumulation in lobster neuromuscular preparations. J. Neurochem. 48, 954-966.
23. Gu, P. L. and Chan, S. M. (1998). The shrimp hyperglycemic hormone-like neuropeptide is encoded by multiple copies of genes arranged in a cluster. FEBS Lett. 441, 397-403.
24. Han, D. W. and Watson, R. D. (2005). Trimeric G proteins in crustacean (Callinectes sapidus) Y-organs: occurrence and functional link to protein synthesis. J. Exp. Zool. 303A, 441-447.
25. Kim, H. W., Batista, L. A., Hoppes, J. L., Lee, K. J. and Mykles, D. L. (2004). A crustacean nitric oxide synthase expressed in nerve ganglia, Y-organ, gill and gonad of the tropical land crab, Gecarcinus lateralis. J. Exp. Biol. 207, 2845-2857.
26. Kim, H. W., Chang, E. S. and Mykles, D. L. (2005a). Three calpains and ecdysone receptor in the land crab, Gecarcinus lateralis: sequences, expression, and effects of elevated ecdysteroid induced by eyestalk ablation. J. Exp. Biol. 208, 3177-3197.
27. Kim, H. W., Lee, S. G. and Mykles, D. L. (2005b). Ecdysteroid-responsive genes, RXR and E75, in the tropical land crab, Gecarcinus lateralis: differential tissue expression of multiple RXR isoforms generated at three alternative splicing sites in the hinge and ligand-binding domains. Mol. Cell. Endocrinol. 242, 80-95.
28. Kozlova, T. and Thummel, C. S. (2000). Steroid regulation of postembryonic development and reproduction in Drosophila. Trends Endocrinol. Metab. 11, 276-280.
29. Kummer, G. and Keller, R. (1993). High-affinity binding of crustacean hyperglycemic hormone (CHH) to hepatopancreatic plasma membranes of the crab Carcinus maenas and the crayfish Orconectes limosus. Peptides 14, 103-108.
30. Lachaise, A., Le Roux, A., Hubert, M. and Lafont, R. (1993). The molting gland of crustaceans: localization, activity, and endocrine control (a review). J. Crust. Biol. 13, 198-234.
31. Lee, K. J., Watson, R. D. and Roer, R. D. (1998). Molt-inhibiting hormone mRNA levels and ecdysteroid titer during a molt cycle of the blue crab, Callinectes sapidus. Biochem. Biophys. Res. Commun. 249, 624-627.
32. Lee, S. G. and Mykles, D. L. (2006). Proteomics and signal transduction in the crustacean molting gland. Integr. Comp. Biol. 46, 965-977.
33. Lee, S. G., Kim, H. W. and Mykles, D. L. (2007). Guanylyl cyclases in the tropical land crab, Gecarcinus lateralis: cloning of soluble (NO-sensitive and -insensitive) and membrane receptor forms. Comp. Biochem. Physiol. D In press.
34. Liu, H. F., Lai, C. Y., Watson, R. D. and Lee, C. Y. (2004). Molecular cloning of a putative membrane form guanylyl cyclase from the crayfish Procambarus clarkii. J. Exp. Zool. A 301, 512-520.
35. Lucas, K. A., Pitari, G. M., Kazerounian, S., Ruiz-Stewart, I., Park, J., Schulz, S., Chepenik, K. P. and Waldman, S. A. (2000). Guanylyl cyclases and signaling by cyclic GMP. Pharmacol. Rev. 52, 375-413.
36. Mahadevan, A., Lappe, J., Rhyne, R. T., Cruz-Bermudez, N. D., Marder, E. and Goy, M. F. (2004). Nitric oxide inhibits the rate and strength of cardiac contractions in the lobster Homarus americanus by acting on the cardiac ganglion. J. Neurosci. 24, 2813-2824.
37. Maniere, G., Vanhems, E., Gautron, F. and Delbecque, J. P. (2003). Inhibition of ovarian steroidogenesis by cyclic GMP in a fly. J. Endocrinol. 177, 35-44.
38. Marco, H. G., Hansen, I. A., Scheller, K. and Gade, G. (2003). Molecular cloning and localization of a cDNA encoding a crustacean hyperglycemic hormone from the South African spiny lobster, Jasus lalandii. Peptides 24, 845-851.
39. Mattson, M. P. and Spaziani, E. (1985). Cyclic AMP mediates the negative regulation of Y-organ ecdysteroid production. Mol. Cell. Endocrinol. 42, 185-189.
40. Mattson, M. P. and Spaziani, E. (1986). Regulation of Y-organ ecdysteroidogenesis by molt-inhibiting hormone in crabs: involvement of cyclic AMP-mediated protein synthesis. Gen. Comp. Endocrinol. 63, 414-423.
41. Morton, D. B. and Hudson, M. L. (2002). Cyclic GMP regulation and function in insects. In Advances in Insect Physiology. Vol. 29, pp. 1-54. London: Academic Press.
42. Morton, D. B. and Simpson, P. J. (2002). Cellular signaling in eclosion hormone action. J. Insect Physiol. 48, 1-13.
43. Mykles, D. L. (1997). Crustacean muscle plasticity: molecular mechanisms determining mass and contractile properties. Comp. Biochem. Physiol. 117B, 367-378.
44. Nakatsuji, T. and Sonobe, H. (2004). Regulation of ecdysteroid secretion from the Y-organ by molt-inhibiting hormone in the American crayfish, Procambarus clarkii. Gen. Comp. Endocrinol. 135, 358-364.
45. Nakatsuji, T., Sonobe, H. and Watson, R. D. (2006). Molt-inhibiting hormone-mediated regulation of ecdysteroid synthesis in Y-organs of the crayfish (Procambarus clarkii): involvement of cyclic GMP and cycle nucleotide phosphodiesterase. Mol. Cell. Endocrinol. 253, 76-82.
46. Nighorn, A., Gibson, N. J., Rivers, D. M., Hildebrand, J. G. and Morton, D. B. (1998). The nitric oxide-cGMP pathway may mediate communication between sensory afferents and projection neurons in the antennal lobe of Manduca sexta. J. Neurosci. 18, 7244-7255.
47. Nighorn, A., Simpson, P. J. and Morton, D. B. (2001). The novel guanylyl cyclase MsGC-I is strongly expressed in higher-order neuropils in the brain of Manduca sexta. J. Exp. Biol. 204, 305-314.
48. Padayatti, P. S., Pattanaik, P., Ma, X. L. and van den Akker, F. (2004). Structural insights into the regulation and the activation mechanism of mammalian guanylyl cyclases. Pharmacol. Ther. 104, 83-99.
49. Pavloff, M. S. and Goy, M. F. (1990). Purification and chemical characterization of peptide-G1, an invertebrate neuropeptide that stimulates cyclic GMP metabolism. J. Neurochem. 55, 788-797.
50. Potter, L. R. (2005). Domain analysis of human transmembrane guanylyl cyclase receptors: implications for regulation. Front. Biosci. 10, 1205-1220.
51. Prabhakar, S., Short, D. B., Scholz, N. L. and Goy, M. F. (1997). Identification of nitric oxide-sensitive and -insensitive forms of cytoplasmic guanylate cyclase. J. Neurochem. 69, 1650-1660.
52. Pyriochou, A. and Papapetropoulos, A. (2005). Soluble guanylyl cyclase: more secrets revealed. Cell. Signal. 17, 407-413.
53. Saïdi, B., De Bessé, N., Webster, S. G., Sedlmeier, D. and Lachaise, F. (1994). Involvement of cAMP and cGMP in the mode of action of molt-inhibiting hormone (MIH) a neuropeptide which inhibits steroidogenesis in a crab. Mol. Cell. Endocrinol. 102, 53-61.
54. Scholz, N. L. (2001). NO/cGMP signaling and the flexible organization of motor behavior in crustaceans. Am. Zool. 41, 292-303.
55. Scholz, N. L., Goy, M. F., Truman, J. W. and Graubard, K. (1996). Nitric oxide and peptide neurohormones activate cGMP synthesis in the crab stomatogastric nervous system. J. Neurosci. 16, 1614-1622.
56. Scholz, N. L., Labenia, J. S., De Vente, J., Graubard, K. and Goy, M. F. (2002). Expression of nitric oxide synthase and nitric oxide-sensitive guanylate cyclase in the crustacean cardiac ganglion. J. Comp. Neurol. 454, 158-167.
57. Sedlmeier, D. and Fenrich, R. (1993). Regulation of ecdysteroid biosynthesis in crayfish Y-organs. I. Role of cyclic nucleotides. J. Exp. Zool. 265, 448-453.
58. Sedlmeier, D. and Keller, R. (1981). The mode of action of the crustacean neurosecretory hyperglycemic hormone. 1. Involvement of cyclic-nucleotides. Gen. Comp. Endocrinol. 45, 82-90.
59. Serrano, L., Blanvillain, G., Soyez, D., Charmantier, G., Grousset, E., Aujoulat, F. and Spanings-Pierrot, C. (2003). Putative involvement of crustacean hyperglycemic hormone isoforms in the neuroendocrine mediation of osmoregulation in the crayfish Astacus leptodactylus. J. Exp. Biol. 206, 979-988.
60. Simpson, P. J., Nighorn, A. and Morton, D. B. (1999). Identification of a novel guanylyl cyclase that is related to receptor guanylyl cyclases, but lacks extracellular and transmembrane domains. J. Biol. Chem. 274, 4440-4446.
61. Skinner, D. M. (1985). Molting and regeneration. In The Biology of Crustacea (ed. D. E. Bliss and L. H. Mantel), pp. 43-146. New York: Academic Press.
62. Soyez, D., Van Herp, F., Rossier, J., Le Caer, J. P., Tensen, C. P. and Lafont, R. (1994). Evidence for a conformational polymorphism of invertebrate neurohormones. D-amino acid residue in crustacean hyperglycemic peptides. J. Biol. Chem. 269, 18295-18298.
63. Spaziani, E., Mattson, M. P., Wang, W. N. L. and McDougall, H. E. (1999). Signaling pathways for ecdysteroid hormone synthesis in crustacean Y-organs. Am. Zool. 39, 496-512.
64. Truman, J. W. and Riddiford, L. M. (1999). The origins of insect metamorphosis. Nature 401, 447-452.
65. Von Gliscynski, U. and Sedlmeier, D. (1993). Regulation of ecdysteroid biosynthesis in crayfish Y-organs. II. Role of cyclic nucleotide-dependent protein kinases. J. Exp. Zool. 265, 454-458.
66. Webster, S. G. (1993). High-affinity binding of putative moult-inhibiting hormone (MIH) and crustacean hyperglycaemic hormone (CHH) to membrane-bound receptors on the Y-organ of the shore crab Carcinus maenus. Proc. R. Soc. Lond. B Biol. Sci. 251, 53-59.
67. Webster, S. G. and Keller, R. (1986). Purification, characterisation and amino acid composition of the putative moult-inhibiting hormone (MIH) of Carcinus maenas (Crustacea, Decapoda). J. Comp. Physiol. 156, 617-624.
68. Wu, X. H., Hopkins, P. M., Palli, S. R. and Durica, D. S. (2004). Crustacean retinoid-X receptor isoforms: distinctive DNA binding and receptor-receptor interaction with a cognate ecdysteroid receptor. Mol. Cell. Endocrinol. 218, 21-38.
69. Yang, W. J., Aida, K. and Nagasawa, H. (1997). Amino acid sequences and activities of multiple hyperglycemic hormones from the Kuruma prawn, Penaeus japonicus. Peptides 18, 479-485.
70. Yasuda, A., Yasuda, Y., Fujita, T. and Naya, Y. (1994). Characterization of crustacean hyperglycemic hormone from the crayfish (Procambarus clarkii): multiplicity of molecular forms by stereoinversion and diverse functions. Gen. Comp. Endocrinol. 95, 387-398.
71. Zheng, J. Y., Lee, C. Y. and Watson, R. D. (2006). Molecular cloning of a putative receptor guanylyl cyclase from Y-organs of the blue crab, Callinectes sapidus. Gen. Comp. Endocrinol. 146, 329-336.