Conserved role of cyclic nucleotides in the regulation of ecdysteroidogenesis by the crustacean molting gland

Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology

Volumn 152, Issue 4, 2009, Pages 470-477

  Covi, Joseph A ^a   Chang, Ernest S ^b   Mykles, Donald L ^a  

^a Department of Ecosystem Science and Sustainability   (United States)

^b UNIVERSITY OF CALIFORNIA DAVIS   (United States)

Author keywords

cAMP; cGMP; Cholesterol uptake; Crustacean hyperglycemic hormone; Ecdysteroids; Molt inhibiting hormone; Molting gland; Protein synthesis; Y organ

Indexed keywords

CRUSTACEA;

EID: 60549109044     PISSN: 10956433     EISSN: 15314332     Source Type: Journal    
DOI: 10.1016/j.cbpa.2008.12.005     Document Type: Review

References (85)

1. Asazuma H., Nagata S., Katayama H., Ohira T., and Nagasawa H. Characterization of a molt-inhibiting hormone (MIH) receptor in the Y-organ of the Kuruma prawn, Marsupenaeus japonicus. Ann. N.Y. Acad. Sci. 1040 (2005) 215-218
2. Avarre J.C., Khayat M., Michelis R., Nagasawa H., Tietz A., and Lubzens E. Inhibition of de novo synthesis of a jelly layer precursor protein by crustacean hyperglycemic hormone family peptides and posttranscriptional regulation by sinus gland extracts in Penaeus semisulcatus ovaries. Gen. Comp. Endocrinol. 124 (2001) 257-268
3. Blais C., Sefiani M., Toullec J.-Y., and Soyez D. In vitro production of ecdysteroids by Y-organs of Penaeus vannamei (Crustacea, Decapoda). Correlation with hemolymph titers. Invertebr. Reprod. Dev. 26 (1994) 3-11
4. Chan S.M., Chen X.G., and Gu P.L. PCR cloning and expression of the molt-inhibiting hormone gene for the crab (Charybdis feriatus). Gene 224 (1998) 23-33
5. Chang E.S. Crustacean hyperglycemic hormone family: old paradigms and new perspectives. Am. Zool. 41 (2001) 380-388
6. Chang E.S., Chang S.A., Keller R., Reddy P.S., Snyder M.J., and Spees J.L. Quantification of stress in lobsters: crustacean hyperglycemic hormone, stress proteins, and gene expression. Am. Zool. 39 (1999) 487-495
7. Chang E.S., Keller R., and Chang S.A. Quantification of crustacean hyperglycemic hormone by ELISA in hemolymph of the lobster, Homarus americanus, following various stresses. Gen. Comp. Endocrinol. 111 (1998) 359-366
8. Chang E.S., Chang S.A., and Mulder E.P. Hormones in the lives of crustaceans: an overview. Am. Zool. 41 (2001) 1090-1097
9. Chung J.S., and Webster S.G. 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 (2003) 3280-3288
10. Chung J.S., and Webster S.G. Dynamics of in vivo release of molt-inhibiting hormone and crustacean hyperglycemic hormone in the shore crab, Carcinus maenas. Endocrinology 146 (2005) 5545-5551
11. Chung J.S., and Webster S.G. Binding sites of crustacean hyperglycemic hormone and its second messengers on gills and hindgut of the green shore crab, Carcinus maenas: a possible osmoregulatory role. Gen. Comp. Endocrinol. 147 (2006) 206-213
12. Chung J.S., Wilkinson M.C., and Webster S.G. Amino acid sequences of both isoforms of crustacean hyperglycemic hormone (CHH) and corresponding precursor-related peptide in Cancer pagurus. Regul. Pept. 77 (1998) 17-24
13. Covi J., Gomez A., Chang S., Lee K., Chang E., and Mykles D. Repression of Y-organ ecdysteroidogenesis by cyclic nucleotides and agonists of NO-sensitive guanylyl cyclase. In: Morris S., and Vosloo A. (Eds). 4th Meeting of Comparative Physiologists & Biochemists in Africa - Mara 2008 - "Molecules to Migration: The Pressures of Life". Medimond S.r.l. (2008), Monduzzi Editore International, Bologna, Italy 37-46
14. Dauphin-Villemant C., Bocking D., and Sedlmeier D. Regulation of steroidogenesis in crayfish molting glands-involvement of protein synthesis. Mol. Cell. Endocrinol. 109 (1995) 97-103
15. Dauphin-Villemant C., Bocking D., Tom M., Maibeche M., and Lafont R. Cloning of a novel cytochrome P450 (CYP4C15) differentially expressed in the steroidogenic glands of an arthropod. Biochem. Biophys. Res. Comm. 264 (1999) 413-418
16. García U., and Aréchiga H. Regulation of crustacean neurosecretory cell activity. Cell. Mol. Neurobiol. 18 (1998) 81-99
17. Gersch M., Richter K., and Eibisch H. Untersuchungen zur Kennzeichnung und zur Wirkung des Häutungs-Hemmhormons aus der Sinusdrüse (molt-inhibiting hormone = MIH) von Orconectes limosus Rafinesque (Crustacea-Decapoda). Zool. Jahrb. Abt. Allg. Zool. Physiol. 81 (1977) 133-152
18. Goy M.F. Activation of membrane guanylate cyclase by an invertebrate peptide hormone. J. Biol. Chem. 265 (1990) 20220-20227
19. Gu P.-L., Tobe S.S., Chow B.K.C., Chu K.H., He J.-G., and Chan S.-M. Characterization of an additional molt inhibiting hormone-like neuropeptide from the shrimp Metapenaeus ensis. Peptides 23 (2002) 1875-1883
20. Han D.W., and Watson R.D. Trimeric G proteins in crustacean (Callinectes sapidus) Y-organs: occurrence and functional link to protein synthesis. J. Exp. Zool. 303A (2005) 441-447
21. Han D.W., Patel N., and Watson R.D. Regulation of protein synthesis in Y-organs of the blue crab (Callinectes sapidus): involvement of cyclic AMP. J. Exp. Zool. 305A (2006) 328-334
22. Huberman A. Shrimp endocrinology. A review. Aquacilture 191 (2000) 191-208
23. Jegla T.C., Ruland C., Kegel G., and Keller R. The role of the Y-organ and cephalic gland in ecdysteroid production and the control of molting in the crayfish, Orconectes limosus. J. Comp. Physiol. 152 (1983) 91-95
24. Kang B.K., and Spaziani E. Uptake of high-density lipoprotein by Y-organs of the crab Cancer antennarius: III. Evidence for adsorptive endocytosis and the absence of lysosomal processing. J. Exp. Zool. 273 (1995) 425-433
25. Kang B.K., and Spaziani E. Uptake of high-density lipoprotein by Y-organs of the crab, Cancer antennarius. I. Characterization in vitro and effects of stimulators and inhibitors. Arch. Insect Biochem. Physiol. 30 (1995) 61-75
26. Kang B.K., and Spaziani E. Uptake of high-density lipoprotein by Y-organs of the crab, Cancer antennarius. II. Formal characterization of receptor mediation with isolated membranes. Arch. Insect Biochem. Physiol. 30 (1995) 77-91
27. Katayama H., Nagata K., Ohira T., Yumoto F., Tanokura M., and Nagasawa H. The solution structure of molt-inhibiting hormone from the kuruma prawn Marsupenaeus japonicus. J. Biol. Chem. 278 (2003) 9620-9623
28. Kim H.W., Batista L.A., Hoppes J.L., Lee K.J., and Mykles D.L. 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 (2004) 2845-2857
29. Krungkasem C., Ohira T., Yang W.J., Abdullah R., Nagasawa H., and Aida K. Identification of two distinct molt-inhibiting hormone-related peptides from the giant tiger prawn Penaeus monodon. Mar. Biotechnol. 4 (2002) 132-140
30. Kummer G., and Keller R. High-affinity binding of crustacean hyperglycaemic hormone (CHH) to hepatopancreatic plasma membranes of the crab Carcinus maenas and the crayfish Orconectes limosus. Peptides 14 (1993) 103-108
31. Lachaise F., Meister M.F., Hetru C., and Lafont R. Studies on the biosynthesis of ecdysone by the Y-organs of Carcinus maenas. Mol. Cell. Endocrinol. 45 (1986) 253-261
32. Lachaise F., Carpentier G., Somme G., Colardeau J., and Beydon P. Ecdysteroid synthesis by crab Y-organs. J. Exp. Zool. 252 (1989) 283-292
33. Lachaise A., Le Roux A., Hubert M., and Lafont R. The molting gland of crustaceans: localization, activity, and endocrine control (a review). J. Crust. Biol. 13 (1993) 198-234
34. Lachaise F., Ghislaine S., Carpentier G., Granjeon E., Webster S., and Baghdassarian D. A transaldolase-an enzyme implicated in crab steroidogenesis. Endocrine 5 (1996) 22-32
35. Lee S.G., and Mykles D.L. Proteomics and signal transduction in the crustacean molting gland. Integ. Comp. Biol. 46 (2006) 965-977
36. Lee K.J., Elton T.S., Bej A.K., Watts S.A., and Watson R.D. Molecular cloning of a cDNA encoding putative molt-inhibiting hormone from the blue crab, Callinectes sapidus. Biochem. Biophys. Res. Commun. 209 (1995) 1126-1131
37. Lee K.J., Kim H.W., Gomez A.M., Chang E.S., Covi J.A., and Mykles D.L. Molt-inhibiting hormone from the tropical land crab, Gecarcinus lateralis: cloning, tissue expression, and expression of biologically active recombinant peptide in yeast. Gen. Comp. Endocrinol. 150 (2007) 505-513
38. Lee S.G., Bader B.D., Chang E.S., and Mykles D.L. 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. J. Exp. Biol. 219 (2007) 3245-3254
39. Lee S.G., Kim H.W., and Mykles D.L. Guanylyl cyclases in the tropical land crab, Gecarcinus lateralis: Cloning of soluble (NO-sensitive and -insensitive) and membrane receptor forms. Comp. Biochem. Physiol. D 2 (2007) 332-344
40. Liu H.F., Lai C.Y., Watson R.D., and Lee C.Y. Molecular cloning of a putative membrane form guanylyl cyclase from the crayfish Procambarus clarkii. J. Exp. Zool. 301A (2004) 512-520
41. Lu W.Q., Wainwright G., Olohan L.A., Webster S.G., Rees H.H., and Turner P.C. Characterization of cDNA encoding molt-inhibiting hormone of the crab, Cancer pagurus; expression of MIH in non-X-organ tissues. Gene 278 (2001) 149-159
42. Mantel L.H., Bliss D.E., Sheehan S.W., and Martinez E.A. Physiology of hemolymph, gut fluid, and hepatopancreas of land crab Gecarcinus-lateralis (Freminville) in various neuroendocrine states. Comp. Biochem. Physiol. A 51 (1975) 663-671
43. Mattson M.P. New insights into neuroendocrine regulation of the crustacean molt cycle. Zool. Sci. 3 (1986) 733-744
44. Mattson M.P., and Spaziani E. Cyclic AMP mediates the negative regulation of Y-organ ecdysteroid production. Mol. Cell. Endocrinol. 42 (1985) 185-189
45. Mattson M.P., and Spaziani E. Regulation of crab Y-organ steroidogenesis in vitro-evidence that ecdysteroid production increases through activation of cAMP-phosphodiesterase by calcium-calmodulin. Mol. Cell. Endocrinol. 48 (1986) 135-151
46. Mattson M.P., and Spaziani E. Regulation of Y-organ ecdysteroidogenesis by molt-inhibiting hormone in crabs: involvement of cyclic AMP-mediated protein synthesis. Gen. Comp. Endocrinol. 63 (1986) 414-423
47. Mattson M.P., and Spaziani E. Demonstration of protein kinase C activity in crustacean Y-organs, and partial definition of its role in regulation of ecdysteroidogenesis. Mol. Cell. Endocrinol. 49 (1987) 159-171
48. Mykles D.L. Interactions between limb regeneration and molting in decapod crustaceans. Am. Zool. 41 (2001) 399-406
49. Mykles D.L., and Skinner D.M. Atrophy of crustacean somatic muscle and the proteinases that do the job. A review. J. Crust. Biol. 10 (1990) 577-594
50. Nakatsuji T., and Sonobe H. Regulation of ecdysteroid secretion from the Y-organ by molt-inhibiting hormone in the American crayfish, Procambarus clarkii. Gen. Comp. Endocrinol. 135 (2004) 358-364
51. Nakatsuji T., Han D.-W., Jablonsky M.J., Harville S.R., Muccio D.D., and Watson R.D. Expression of crustacean (Callinectes sapidus) molt-inhibiting hormone in Escherichia coli: characterization of the recombinant peptide and assessment of its effects on cellular signaling pathways in Y-organs. Mol. Cell. Endocrinol. 253 (2006) 96-104
52. Nakatsuji T., Sonobe H., and Watson R.D. 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 (2006) 76-82
53. Nakatsuji T., Lee C., and Watson R.D. Crustacean molt-inhibiting hormone: structure, function, and cellular mode of action. Comp. Biochem. Physiol. A 152 (2009) 139-148
54. Ohira T., Watanabe T., Nagasawa H., and Aida K. Molecular cloning of a molt-inhibiting hormone cDNA from the kuruma prawn Penaeus japonicus. Zool. Sci. 14 (1997) 785-789
55. Rewitz K.F., and Gilbert L.I. Daphnia Halloween genes that encode cytochrome P450s mediating the synthesis of the arthropod molting hormone: evolutionary implications. BMC Evol. Biol. 8 (2008) 60-67
56. Saïdi B., De Bessé N., Webster S.G., Sedlmeier D., and Lachaise F. 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 (1994) 53-61
57. Santos E.A., Nery L.E.M., Keller R., and Goncalves A.A. Evidence for the involvement of the crustacean hyperglycemic hormone in the regulation of lipid metabolism. Physiol. Zool. 70 (1997) 415-420
58. Schoettker P.J., and Gist D.H. In vitro ecdysteroid produciton by Y-organs of the blue crab Callinectes sapidus. J. Crustac. Biol. 10 (1990) 487-491
59. Sedlmeier D., and Fenrich R. Regulation of ecdysteroid biosynthesis in crayfish Y-organs: I. Role of cyclic nucleotides. J. Exp. Zool. 265 (1993) 448-453
60. Sefiani M., Le Caer J.P., and Soyez D. Characterization of hyperglycemic and molt-inhibiting activity from sinus glands of the penaeid shrimp Penaeus vannamei. Gen. Comp. Endocrinol. 103 (1996) 41-53
61. Shechter A., Tom M., Yudkovski Y., Weil S., Chang S.A., Chang E.S., Chalifa-Caspi V., Berman A., and Sagi A. Search for hepatopancreatic ecdysteroid-responsive genes during the crayfish molt cycle: from a single gene to multigenicity. J. Exp. Biol. 210 (2007) 3525-3537
62. Simione F.P., and Hoffman D.L. Some effects of eyestalk removal on Y-organs of Cancer irroratus Say. Biol. Bull. 148 (1975) 440-447
63. Skinner D.M. The structure and metabolism of a crustacean integumentary tissue during a molt cycle. Biol. Bull. 123 (1962) 635-647
64. Skinner D.M. Breakdown and reformation of somatic muscle during the molt cycle of the land crab, Gecarcinus lateralis. J. Exp. Zool. 163 (1966) 115-124
65. Skinner D.M. Interacting factors in the control of the crustacean molt cycle. Am. Zool. 25 (1985) 275-284
66. Skinner D.M. Molting and regeneration. In: Bliss D.E., and Mantel L.H. (Eds). The Biology of Crustacea (1985), Academic Press, New York 43-146
67. Sonobe H., Nishimura T., Sonobe M., Nakatsuji T., Yanagihara R., Kawakami T., and Aimoto S. The molt-inhibiting hormone in the American crayfish Procambarus clarkii: its chemical synthesis and biological activity. Gen. Comp. Endocrinol. 121 (2001) 196-204
68. Soumoff C., O, and Connor J.D. Repression of Y-organ secretory activity by molt-inhibiting hormone in the crab Pachygrapsus crassipes. Gen. Comp. Endocrinol. 48 (1982) 432-439
69. Soyez D., Noel P.Y., Van Deijnen J.E., Martin M., Morel A., and Payen G.G. Neuropeptides from the sinus gland of the lobster Homarus americanus: characterization of hyperglycemic peptides. Gen. Comp. Endocrinol. 79 (1990) 261-274
70. Spaziani E., and Wang W.L. Biosynthesis of ecdysteroid hormones by crustacean Y-organs: Conversion of cholesterol to 7-dehydrocholesterol is suppressed by a steroid 5α-reductase inhibitor. Mol. Cell. Endocrinol. 95 (1993) 111-114
71. Spaziani E., Mattson M.P., Wang W.N.L., and McDougall H.E. Signaling pathways for ecdysteroid hormone synthesis in crustacean Y-organs. Am. Zool. 39 (1999) 496-512
72. Spaziani E., Jegla T.C., Wang W.L., Booth J.A., Connolly S.M., Conrad C.C., Dewall M.J., Sarno C.M., Stone D.K., and Montgomery R. Further studies on signaling pathways for ecdysteroidogenesis in crustacean Y-organs. Am. Zool. 41 (2001) 418-429
73. Sun P.S. Expression of the molt-inhibiting hormone-like gene in the eyestalk and brain of the white shrimp Penaeus vannamei. Mol. Mar. Biol. Biotechnol. 4 (1995) 262-268
74. Toullec J.Y., and Dauphin-Villemant C. Dissociated cell suspensions of Carcinus maenas Y-organs as a tool to study ecdysteroid production and its regulation. Experientia 50 (1994) 153-158
75. Umphrey H.R., Lee K.J., Watson R.D., and Spaziani E. Molecular cloning of a cDNA encoding molt-inhibiting hormone of the crab, Cancer magister. Mol. Cell. Endocrinol. 136 (1998) 145-149
76. Van den Oord A. Absence of cholesterol synthesis in crab Cancer pagarus L. Comp. Biochem. Physiol. 13 (1964) 461-467
77. Watson R.D., and Spaziani E. Biosynthesis of ecdysteroids from cholesterol by crab Y-organs, and eyestalk suppression of cholesterol uptake and secretory activity in vitro. Gen. Comp. Endocrinol. 59 (1985) 140-148
78. Watson R.D., and Spaziani E. Effects of eyestalk removal on cholesterol uptake and ecdysone secretion by crab (Cancer antennarius) Y-organs in vitro. Gen. Comp. Endocrinol. 57 (1985) 360-370
79. Webster S.G. Neurohormonal control of ecdysteroid biosynthesis by Carcinus maenas Y-organs in vitro, and preliminary characterization of the putative molt-inhibiting hormone (MIH). Gen. Comp. Endocrinol. 61 (1986) 237-247
80. Webster S.G. 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. 251 (1993) 53-59
81. Webster S.G. Neuropeptides inhibiting growth and reproduction in crustaceans. Soc. Exp. Biol. 65 (1998) 33-52
82. Webster S.G., and Keller R. Purification, characterisation and amino acid composition of the putative moult-inhibiting hormone (MIH) of Carcinus maenas (Crustacea, Decapoda). J. Comp. Physiol. 156 (1986) 617-624
83. Zandee D. Absence of cholesterol synthesis as contrasted with presence of fatty acid synthesis in some arthropods. Comp. Biochem. Physiol. 20 (1967) 811-822
84. Zarubin, T.P., Chang, E.S., Mykles, D.L., in press. Expression of recombinant eyestalk crustacean hyperglycemic hormone from the tropical land crab, Gecarcinus lateralis, that inhibits Y-organ ecdysteroidogenesis in vitro. Molec. Biol. Rep. doi:10.1007/s11033-008-9302-8.
85. Zheng J.Y., Lee C.Y., and Watson R.D. Molecular cloning of a putative receptor guanylyl cyclase from Y-organs of the blue crab, Callinectes sapidus. Gen. Comp. Endocrinol. 146 (2006) 329-336