Ecdysone receptor gene from the freshwater prawn Macrobrachium nipponense: Identification of different splice variants and sexually dimorphic expression, fluctuation of expression in the molt cycle and effect of eyestalk ablation

General and Comparative Endocrinology

Volumn 193, Issue , 2013, Pages 86-94

  Shen, Huaishun ^a   Zhou, Xin ^a   Bai, Aixu ^a,b   Ren, Xiufang ^a,b   Zhang, Yanping ^a  

^a SOUTH CHINA SEA FISHERIES RESEARCH INSTITUTE   (China)

^b SHANGHAI OCEAN UNIVERSITY   (China)

Author keywords

Ecdysone receptor; Macrobrachium nipponense; Molting; Splice variant

Indexed keywords

ECDYSONE RECEPTOR;

AMINO ACID SUBSTITUTION; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DOWN REGULATION; ECDYSONE RECEPTOR GENE; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; GENE DELETION; GENE EXPRESSION; GENE FUNCTION; GENE INSERTION; GENETIC VARIABILITY; GILL; GONAD; HEPATOPANCREAS; MACROBRACHIUM; MACROBRACHIUM NIPPONENSE; MALE; MOLECULAR CLONING; MOLTING; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARY; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SPLICING; SEX DIFFERENCE; TESTIS; UPREGULATION;

ECDYSONE RECEPTOR; MACROBRACHIUM NIPPONENSE; MOLTING; SPLICE VARIANT;

ANIMALS; DNA, COMPLEMENTARY; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; PALAEMONIDAE; RECEPTORS, STEROID; SEX CHARACTERISTICS;

EID: 84882237365     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2013.07.014     Document Type: Article

References (48)

1. Asazuma H., Nagata S., Kono M., Nagasawa H. Molecular cloning and expression analysis of ecdysone receptor and retinoid X receptor from the kuruma prawn, Marsupenaeus japonicus. Comp. Biochem. Physiol. B: Biochem. Mol. Biol. 2007, 148:139-150.
2. Bender M., Imam F.B., Talbot W.S., Ganetzky B., Hogness D.S. Drosophila ecdysone receptor mutations reveal functional differences among receptor isoforms. Cell 1997, 91:777-788.
3. Bernardi F., Romani P., Tzertzinis G., Gargiulo G., Cavaliere V. EcR-B1 and Usp nuclear hormone receptors regulate expression of the VM32E eggshell gene during Drosophila oogenesis. Dev. Biol. 2009, 328:541-551.
4. Cesara J.R.d.O., Zhao B., Malechaa S., Akob H., Yang J. Morphological and biochemical changes in the muscle of the marine shrimp Litopenaeus vannamei during the molt cycle. Aquaculture 2006, 261:688-694.
5. Chan S.-M., Rankin S.M., Keeley L.L. Characterization of the molt stages in Penaeus vannamei: setogenesis and hemolymph levels of total protein, ecdysteroids, and glucose. Biol. Bull. 1988, 175:185-192.
6. Chang E.S., Bruce M.J. Ecdysteroid titers of juvenile lobsters following molt induction. J. Exp. Zool. 1980, 214:157-160.
7. Chang E.S., Mykles D.L. Regulation of crustacean molting: a review and our perspectives. Gen. Comp. Endocrinol. 2011, 172:323-330.
8. Chen H., Wang W.-q., Zhu X.-l. Clon ing of cDNA encoding EcR and its' expression analysis during embryogenesis in the freshwater prawn, Macrobrachium nipponense. Mar. Fish. (China) 2009, 31:347-356.
9. Chen H.Y., Dillaman R.M., Roer R.D., Watson R.D. Stage-specific changes in calcium concentration in crustacean (Callinectes sapidus) Y-organs during a natural molting cycle, and their relation to the hemolymphatic ecdysteroid titer. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 2012, 163:170-173.
10. Chen Y., Zhu Q., Chen H., Zhu X.-l., Cui Z., Qiu G.-f. The morphological and histological observation of embryonic development in the oriental river prawn Macrobrachium nipponense. J. Shanghai Ocean Univ. (China) 2012, 21:33-40.
11. Christie A.E., Stemmler E.A., Dickinson P.S. Crustacean neuropeptides. Cell. Mol. Life Sci. 2010, 67:4135-4169.
12. Chung A.C., Durica D.S., Clifton S.W., Roe B.A., Hopkins P.M. Cloning of crustacean ecdysteroid receptor and retinoid-X receptor gene homologs and elevation of retinoid-X receptor mRNA by retinoic acid. Mol. Cell. Endocrinol. 1998, 139:209-227.
13. Chung A.C., Durica D.S., Hopkins P.M. Tissue-specific patterns and steady-state concentrations of ecdysteroid receptor and retinoid-X-receptor mRNA during the molt cycle of the fiddler crab, Uca pugilator. Gen. Comp. Endocrinol. 1998, 109:375-389.
14. Covi J.A., Chang E.S., Mykles D.L. Conserved role of cyclic nucleotides in the regulation of ecdysteroidogenesis by the crustacean molting gland. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 2009, 152:470-477.
15. Cunha C.H., Oshiro L.M.Y. The influence of eyestalk ablation on the reproduction of the freshwater Macrobrachium acanthurus shrimp in captivity. Acta Sci. Bio. Sci. 2010, 32:217-221.
16. Dela Cruz F.E., Kirsch D.R., Heinrich J.N. Transcriptional activity of Drosophila melanogaster ecdysone receptor isoforms and ultraspiracle in Saccharomyces cerevisiae. J. Mol. Endocrinol. 2000, 24:183-191.
17. Kim H.W., Chang E.S., Mykles D.L. 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. 2005, 208:3177-3197.
18. Kim H.W., Lee S.G., Mykles D.L. 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. 2005, 242:80-95.
19. Ma K., Qiu G., Feng J., Li J. Transcriptome analysis of the oriental river prawn, Macrobrachium nipponense using 454 pyrosequencing for discovery of genes and markers. PLoS ONE 2012, 7:e39727.
20. Ma K.Y., Lin J.Y., Guo S.Z., Chen Y., Li J.L., Qiu G.F. Molecular characterization and expression analysis of an insulin-like gene from the androgenic gland of the oriental river prawn, Macrobrachium nipponense. Gen. Comp. Endocrinol. 2013, 185C:90-96.
21. McDonald A.A., Chang E.S., Mykles D.L. Cloning of a nitric oxide synthase from green shore crab, Carcinus maenas: a comparative study of the effects of eyestalk ablation on expression in the molting glands (Y-organs) of C. maenas, and blackback land crab, Gecarcinus lateralis. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 2011, 158:150-162.
22. Mouillet J.F., Henrich V.C., Lezzi M., Vogtli M. Differential control of gene activity by isoforms A, B1 and B2 of the Drosophila ecdysone receptor. Eur. J. Biochem. 2001, 268:1811-1819.
23. Murmu K., Sahu N.P., Mallik S.K., Reddy A.K., Kohli M.P.S. Rematuration of spent Macrobrachium rosenbergii female broodstock through dietary manipulation and eyestalk ablation Isr. J. Aquacult-Bamid. 2007, 59:104-110.
24. Nagaraju G.P. Reproductive regulators in decapod crustaceans: an overview. J. Exp. Biol. 2011, 214:3-16.
25. Nagaraju G.P., Rajitha B., Borst D.W. Molecular cloning and sequence of retinoid X receptor in the green crab Carcinus maenas: a possible role in female reproduction. J. Endocrinol. 2011, 210:379-390.
26. Nakagawa Y., Henrich V.C. Arthropod nuclear receptors and their role in molting. FEBS J. 2009, 276:6128-6157.
27. Okumura T. Effects of bilateral and unilateral eyestalk ablation on vitellogenin synthesis in immature female kuruma prawns, Marsupenaeus japonicus. Zoolog. Sci. 2007, 24:233-240.
28. Okumura T., Kim Y.K., Kawazoe I., Yamano K., Tsutsui N., Aida K. Expression of vitellogenin and cortical rod proteins during induced ovarian development by eyestalk ablation in the kuruma prawn, Marsupenaeus japonicus. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 2006, 143:246-253.
29. Perera S.C., Sundaram M., Krell P.J., Retnakaran A., Dhadialla T.S., Palli S.R. An analysis of ecdysone receptor domains required for heterodimerization with ultraspiracle. Arch. Insect Biochem. Physiol. 1999, 41:61-70.
30. Perera S.C., Zheng S., Feng Q.L., Krell P.J., Retnakaran A., Palli S.R. Heterodimerization of ecdysone receptor and ultraspiracle on symmetric and asymmetric response elements. Arch. Insect Biochem. Physiol. 2005, 60:55-70.
31. Rahman M.K., Subramoniam T. Molting and its control in the female sand lobsterThenus orientalis (Lund). J. Exp. Mar. Biol. Ecol. 1989, 128:105-115.
32. Renaud J.P., Moras D. Structural studies on nuclear receptors. Cell. Mol. Life Sci. 2000, 57:1748-1769.
33. Schubiger M., Wade A.A., Carney G.E., Truman J.W., Bender M. Drosophila EcR-B ecdysone receptor isoforms are required for larval molting and for neuron remodeling during metamorphosis. Development 1998, 125:2053-2062.
34. Shechter A., Tom M., Yudkovski Y., Weil S., Chang S.A., Chang E.S., Chalifa-Caspi V., Berman A., Sagi A. Search for hepatopancreatic ecdysteroid-responsive genes during the crayfish molt cycle: from a single gene to multigenicity. J. Exp. Biol. 2007, 210:3525-3537.
35. Sroyraya M., Chotwiwatthanakun C., Stewart M.J., Soonklang N., Kornthong N., Phoungpetchara I., Hanna P.J., Sobhon P. Bilateral eyestalk ablation of the blue swimmer crab, Portunus pelagicus, produces hypertrophy of the androgenic gland and an increase of cells producing insulin-like androgenic gland hormone. Tissue Cell 2010, 42:293-300.
36. Subramoniam T. Crustacean ecdysteriods in reproduction and embryogenesis. Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 2000, 125:135-156.
37. Tarrant A.M., Behrendt L., Stegeman J.J., Verslycke T. Ecdysteroid receptor from the American lobster Homarus americanus: EcR/RXR isoform cloning and ligand-binding properties. Gen. Comp. Endocrinol. 2011, 173:346-355.
38. Thomson S.A., Baldwin W.S., Wang Y.H., Kwon G., Leblanc G.A. Annotation, phylogenetics, and expression of the nuclear receptors in Daphnia pulex. BMC Genomics 2009, 10:500.
39. Tiu S.H., Hult E.F., Yagi K.J., Tobe S.S. Farnesoic acid and methyl farnesoate production during lobster reproduction: possible functional correlation with retinoid X receptor expression. Gen. Comp. Endocrinol. 2012, 175:259-269.
40. Uawisetwathana U., Leelatanawit R., Klanchui A., Prommoon J., Klinbunga S., Karoonuthaisiri N. Insights into eyestalk ablation mechanism to induce ovarian maturation in the black tiger shrimp. PLoS ONE 2011, 6:e24427.
41. Ventura T., Manor R., Aflalo E.D., Weil S., Raviv S., Glazer L., Sagi A. Temporal silencing of an androgenic gland-specific insulin-like gene affecting phenotypical gender differences and spermatogenesis. Endocrinology 2009, 150:1278-1286.
42. Verhaegen Y., Parmentier K., Swevers L., Renders E., Rouge P., De Coen W., Cooreman K., Smagghe G. The heterodimeric ecdysteroid receptor complex in the brown shrimp Crangon crangon: EcR and RXR isoform characteristics and sensitivity towards the marine pollutant tributyltin. Gen. Comp. Endocrinol. 2011, 172:158-169.
43. Wang Y.H., Wang G., LeBlanc G.A. Cloning and characterization of the retinoid X receptor from a primitive crustacean Daphnia magna. Gen. Comp. Endocrinol. 2007, 150:309-318.
44. Wang Y.T., Mao H., Hou C.C., Sun X., Wang D.H., Zhou H., Yang W.X. Characterization and expression pattern of KIFC1-like kinesin gene in the testis of the Macrobrachium nipponense with discussion of its relationship with structure lamellar complex (LCx) and acroframosome (AFS). Mol. Biol. Rep. 2012, 39:7591-7598.
45. Webster S.G., Keller R., Dircksen H. The CHH-superfamily of multifunctional peptide hormones controlling crustacean metabolism, osmoregulation, moulting, and reproduction. Gen. Comp. Endocrinol. 2012, 175:217-233.
46. Wu X., Hopkins P.M., Palli S.R., Durica D.S. Crustacean retinoid-X receptor isoforms: distinctive DNA binding and receptor-receptor interaction with a cognate ecdysteroid receptor. Mol. Cell. Endocrinol. 2004, 218:21-38.
47. Yokota H., Eguchi S., Nakai M. Development of an in vitro binding assay for ecdysone receptor of mysid shrimp (Americamysis bahia). Aquat. Toxicol. 2011, 105:708-716.
48. Zhang F., Chen L., Qin J., Zhao W., Wu P. A novel gene with a vWD domain and three Kazal-type domains: molecular cloning and expression in the ovary of the oriental river prawn, Macrobrachium nipponense. Genetika 2011, 47:1190-1195.