An insulin-like androgenic gland hormone gene in the mud crab, Scylla paramamosain, extensively expressed and involved in the processes of growth and female reproduction

General and Comparative Endocrinology

Volumn 204, Issue , 2014, Pages 229-238

  Huang, Xiaoshuai ^a   Ye, Haihui ^a   Huang, Huiyang ^a   Yang, Yanan ^a   Gong, Jie ^a  

^a XIAMEN UNIVERSITY   (China)

Author keywords

Androgenic gland; Insulin insulin like growth factor family; Molting cycle; Ovarian development; Scylla paramamosain

Indexed keywords

ANDROGEN; COMPLEMENTARY DNA; GENOMIC DNA; RNA; SOMATOMEDIN BINDING PROTEIN; HORMONE; INSULIN; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY GROWTH; CONTROLLED STUDY; CRUSTACEA; DEVELOPMENTAL STAGE; EXON; FEMALE; GENE EXPRESSION; GENETIC ANALYSIS; IN SITU HYBRIDIZATION; INTRON; MALE; MOLTING; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE DEVELOPMENT; OVARY DEVELOPMENT; PRIORITY JOURNAL; REPRODUCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCYLLA (CRAB); SCYLLA PARAMAMOSAIN; SEQUENCE ALIGNMENT; SEX DIFFERENTIATION; VITELLOGENESIS; AMINO ACID SEQUENCE; ANIMAL; BRACHYURA; EXOCRINE GLAND; GENETICS; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; OVARY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANDROGENS; ANIMALS; BRACHYURA; CLONING, MOLECULAR; DNA, COMPLEMENTARY; EXOCRINE GLANDS; FEMALE; IN SITU HYBRIDIZATION; INSULIN; INVERTEBRATE HORMONES; MALE; MOLECULAR SEQUENCE DATA; OOGENESIS; OVARY; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEQUENCE HOMOLOGY, AMINO ACID; SEX DIFFERENTIATION; VITELLOGENESIS;

EID: 84904698732     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2014.06.002     Document Type: Article

References (52)

1. Banzai K., Ishizaka N., Asahina K., Suitoh K., Izumi S., Ohira T. Molecular cloning of a cDNA encoding insulin-like androgenic gland factor from the kuruma prawn Marsupenaeus japonicus and analysis of its expression. Fish. Sci. 2011, 77:329-335.
2. Barki A., Karplus I., Khalaila I., Manor R., Sagi A. Male-like behavioral patterns and physiological alterations induced by androgenic gland implantation in female crayfish. J. Exp. Biol. 2003, 206:1791-1797.
3. Charniaux-Cotton H. Etude du déterminisme des caractères sexuels secondaires par castration chirurgicale et implantation d'ovaire chez un Crustacé Amphipode (Orchestia gammarella). CR Acad. Sci. Paris 1953, 236:141-143.
4. Charniaux-Cotton H. Androgenic gland of crustaceans. Gen. Comp. Endocrinol. 1962, 1:241-247.
5. Charniaux-Cotton H., Payen G. Crustacean reproduction. Endocrinology of Selected Invertebrate Types 1988, 279-303. Alan R Liss, New York. H. Laufer, R.G.H. Downer (Eds.).
6. Chung A.C.K., 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.
7. Chung J.S., Manor R., Sagi A. Cloning of an insulin-like androgenic gland factor (IAG) from the blue crab, Callinectes sapidus: implications for eyestalk regulation of IAG expression. Gen. Comp. Endocrinol. 2011, 173:4-10.
8. Colombani J., Bianchini L., Layalle S., Pondeville E., Dauphin-Villemant C., Antoniewski C., Carré C., Noselli S., Léopold P. Antagonistic actions of ecdysone and insulins determine final size in Drosophila. Science 2005, 310:667-670.
9. Covi J.A., Chang E.S., Mykles D.L. Neuropeptide signaling mechanisms in crustacean and insect molting glands. Invertebr. Reprod. Dev. 2012, 56:33-49.
10. Cronin L.E. Anatomy and histology of the male reproductive system of Callinectes sapidus Rathbun. J. Morphol. 1947, 81:209-239.
11. Cui Z., Liu H., Lo S.T., Chu K.H. Inhibitory effects of the androgenic gland on ovarian development in the mud crab Scylla paramamosain. Comp. Biochem. Physiol. 2005, 104:343-348.
12. Delanoue R., Léopold P. Developmental biology: a DOR connecting growth and clocks. Curr. Biol. 2010, 20:R884-R886.
13. Delanoue R., Slaidina M., Leopold P. The steroid hormone ecdysone controls systemic growth by repressing dMyc function in Drosophila fat cells. Dev. Cell 2010, 18:1012-1021.
14. Francis V.A., Zorzano A., Teleman A.A. DDOR is an EcR coactivator that forms a feed-forward loop connecting insulin and ecdysone signaling. Curr. Biol. 2010, 20:1799-1808.
15. Gouy M., Guindon S., Gascuel O. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol. Biol. Evol. 2010, 27:221-224.
16. Han V.K.M., Lund P.K., Lee D.C., D'ercole A.J. Expression of somatomedin/insulin-like growth factor messenger ribonucleic acids in the human fetus: identification, characterization, and tissue distribution. J. Clin. Endocrinol. Metab. 1988, 66:422-429.
17. Huang J., Huang H., Ye H., Li S. Cloning and analysis of β-actin gene from Scylla paramamosain. J. Xiamen Univ. 2012, 51:274-279.
18. Huang H., Li W., Huang J., Ye H. Two transcripts and the expression profiles of cyclin A in ovary of the mud crab, Scylla paramamosain. Mar. Freshwater Behav. Physiol. 2013, 46:45-58.
19. Juchault P., Legrand J.J. Function of the androgen gland in crossed implantations between two species of isopod terrestrial crustacean, Porcellio dilatatus Brandt and Armadillidium vulgare Latreille: specificity of androgenic hormones and neurohormones implicated in the control of androgenic function. Gen. Comp. Endocrinol. 1978, 36:175-186.
20. Kaestner K.H. The hepatocyte nuclear factor 3 (HNF3 or FOXA) family in metabolism. Trends Endocrinol. Metab. 2000, 11:281-285.
21. Karplus I., Sagi A., Khalaila I., Barki A. The influence of androgenic gland implantation on the agonistic behavior of female crayfish (Cherax quadricarinatus) in interactions with males. Behaviour 2003, 140:649-664.
22. Katakura Y., Hasegawa Y. Masculinization of females of the isopod crustacean, Armadillidium vulgare, following injections of an active extract of the androgenic gland. Gen. Comp. Endocrinol. 1983, 49:57-62.
23. Khalaila I., Weil S., Sagi A. Endocrine balance between male and female components of the reproductive system in intersex Cherax quadricarinatus (Decapoda: Parastacidae). J. Exp. Zool. 1999, 283:286-294.
24. Khalaila I., Katz T., Abdu U., Yehezkel G., Sagi A. Effects of implantation of hypertrophied androgenic glands on sexual characters and physiology of the reproductive system in the female red claw crayfish, Cherax quadricarinatus. Gen. Comp. Endocrinol. 2001, 121:242-249.
25. Le Vay L., Lebata M.J.H., Walton M., Primavera J., Quinitio E., Lavilla-Pitogo C., Parado-Estepa F., Rodriguez E., Ngoc Ut V., Nghia T.T., Sorgeloos P., Wille M. Approaches to stock enhancement in mangrove-associated crab fisheries. Rev. Fish. Sci. 2008, 16:72-80.
26. Li S., Li F., Sun Z., Xiang J. Two spliced variants of insulin-like androgenic gland hormone gene in the Chinese shrimp, Fenneropenaeus chinensis. Gen. Comp. Endocrinol. 2012, 177:246-255.
27. Liu H., Cheung K.C., Chu K.H. Cell structure and seasonal changes of the androgenic gland of the mud crab Scylla paramamosain (Decapoda: Portunidae). Zool. Stud. 2008, 47:720-732.
28. Lomenick J.P., Hubert M.A., Handwerger S. Transcription factor FOXF1 regulates growth hormone variant gene expression. Am. J. Physiol. Endocrinol. Metab. 2006, 291:E947-E951.
29. Malecha S.R., Nevin P.A., Ha P., Barck L.E., Lamadrid-Rose Y., Masuno S., Hedgecock D. Sex-ratios and sex-determination in progeny from crosses of surgically sex-reversed freshwater prawns, Macrobrachium rosenbergii. Aquaculture 1992, 105:201-218.
30. Manor R., Aflalo E.D., Segall C., Weil S., Azulay D., Ventura T., Sagi A. Androgenic gland implantation promotes growth and inhibits vitellogenesis in Cherax quadricarinatus females held in individual compartments. Invertebr. Reprod. Dev. 2004, 45:151-159.
31. Manor R., Weil S., Oren S., Glazer L., Aflalo E.D., Ventura T., Chalifa-Caspi V., Lapidot M., Sagi A. Insulin and gender: an insulin-like gene expressed exclusively in the androgenic gland of the male crayfish. Gen. Comp. Endocrinol. 2007, 150:326-336.
32. Mareddy V.R., Rosen O., Thaggard H.B., Manor R., Kuballa A.V., Aflalo E.D., Sagi A., Paterson B., Elizur A. Isolation and characterization of the complete cDNA sequence encoding a putative insulin-like peptide from the androgenic gland of Penaeus monodon. Aquaculture 2011, 318:364-370.
33. Martin G., Sorokine O., Moniatte M., Bulet P., Hetru C., Van Dorsselaer A. The structure of a glycosylated protein hormone responsible for sex determination in the isopod, Armadillidium vulgare. Eur. J. Biochem. 1999, 262:727-736.
34. Murphy L.J., Bell G.I., Friesen H.G. Tissue distribution of insulin-like growth factor I and II messenger ribonucleic acid in the adult rat. Endocrinology 1987, 120:1279-1282.
35. Nagamine C., Knight A.W., Maggenti A., Paxman G. Masculinization of female Macrobrachium rosenbergii (de Man) (Decapoda, Palaemonidae) by androgenic gland implantation. Gen. Comp. Endocrinol. 1980, 41:442-457.
36. Nagamine C., Knight A.W., Maggenti A., Paxman G. Effects of androgenic gland ablation on male primary and secondary sexual characteristics in the Malaysian prawn, Macrobrachium rosenbergii (de Man) (Decapoda, Palaemonidae), with first evidence of induced feminization in a nonhermaphroditic decapod. Gen. Comp. Endocrinol. 1980, 41:423-441.
37. Quinitio E.T., Estepa F.D.P. Survival and growth of mud crab, Scylla serrata, juveniles subjected to removal or trimming of chelipeds. Aquaculture 2011, 318:229-234.
38. Rosen O., Manor R., Weil S., Gafni O., Linial A., Aflalo E.D., Ventura T., Sagi A. A sexual shift induced by silencing of a single insulin-like gene in crayfish: ovarian upregulation and testicular degeneration. PLoS ONE 2010, 5:e15281.
39. Rusten T.E., Lindmo K., Juhasz G., Sass M., Seglen P.O., Brech A., Stenmark H. Programmed autophagy in the Drosophila fat body is induced by ecdysone through regulation of the PI3K pathway. Dev. Cell 2004, 7:179-192.
40. Sagi A., Cohen D., Milner Y. Effect of androgenic gland ablation on morphotypic differentiation and sexual characteristics of male freshwater prawns, Macrobrachium rosenbergii. Gen. Comp. Endocrinol. 1990, 77:15-22.
41. Shechter A., Aflalo E.D., Davis C., Sagi A. Expression of the reproductive female-specific vitellogenin gene in endocrinologically induced male and intersex Cherax quadricarinatus crayfish. Biol. Reprod. 2005, 73:72-79.
42. Sroyraya M., Chotwiwatthanakun C., Stewart M.J., Soonklang N., Kornthong N., Phoungpetchara N., 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.
43. Suzuki S., Yamasaki K. Sex-reversal of male Armadillidium vulgare (Isopoda, Malacostraca, Crustacea) following andrectomy and partial gonadectomy. Gen. Comp. Endocrinol. 1991, 83:375-378.
44. Suzuki S., Yamasaki K. Sexual bipotentiality of developing ovaries in the terrestrial isopod Armadillidium vulgare (Malacostraca, Crustacea). Gen. Comp. Endocrinol. 1997, 107:136-146.
45. Techa S., Chung J.S. Ecdysone and retinoid-X receptors of the blue crab, Callinectes sapidus: cloning and their expression patterns in eyestalks and Y-organs during the molt cycle. Gene 2013, 527:139-153.
46. Tropea C., Hermida G.N., López Greco L.S. Effects of androgenic gland ablation on growth and reproductive parameters of Cherax quadricarinatus males Parastacidae (Parastacidae, Decapoda). Decapoda. Gen. Comp. Endocrinol. 2011, 174:211-218.
47. Tuteja G., Kaestner K.H. Forkhead transcription factors II. Cell 2007, 131:192.
48. 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.
49. Ventura T., Manor R., Aflalo E.D., Weil S., Khalaila I., Rosen O., Sagi A. Expression of an androgenic gland-specific insulin-like peptide during the course of prawn sexual and morphotypic differentiation. ISRN Endocrinol. 2011, 2011:1-11.
50. Wang G., Li S., Zeng C., Lin S., Kong X., Ai C., Lin Q. Status of biological studies and aquaculture development of the mud crab, Scylla serrata, in China: an experimental ecological studies. Aquacult. Int. 2005, 13:459-468.
51. Wang S., Liu S., Liu H., Wang J., Zhou S., Jiang R.J., Bendena W.G., Li S. 20-hydroxyecdysone reduces insect food consumption resulting in fat body lipolysis during molting and pupation. J. Mol. Cell Biol. 2010, 2:128-138.
52. Xie Y., Huang H., Ye H., Gong J., Jin Z., Li S. Molecular cloning and expression analysis of the follistatin related protein gene in Scylla paramamosain. Shuichan Xuebao 2012, 36:1201-1208.