Molecular characterization of insulin-like androgenic gland hormone-binding protein gene from the oriental river prawn Macrobrachium nipponense and investigation of its transcriptional relationship with the insulin-like androgenic gland hormone gene

General and Comparative Endocrinology

Volumn 216, Issue , 2015, Pages 152-160

  Li, Fajun ^a,b   Bai, Hongkun ^a   Xiong, Yiwei ^c   Fu, Hongtuo ^a   Jiang, Sufei ^c   Jiang, Fengwei ^a   Jin, Shubo ^c   Sun, Shengming ^c   Qiao, Hui ^c   Zhang, Wenyi ^c  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

^b WEIFANG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c SOUTH CHINA SEA FISHERIES RESEARCH INSTITUTE   (China)

Author keywords

Insulin like androgenic gland hormone gene; Insulin like androgenic gland hormone binding protein gene; Macrobrachium nipponense; RNA interference

Indexed keywords

COMPLEMENTARY DNA; DOUBLE STRANDED RNA; MESSENGER RNA; ANDROGEN; ARTHROPOD PROTEIN; CARRIER PROTEIN; INSULIN; SEX HORMONE;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; FEMALE; GENE DOSAGE; GENE ISOLATION; GENETIC ANALYSIS; HEPATOPANCREAS; INSULIN LIKE ANDROGENIC GLAND HORMONE BINDING PROTEIN GENE; MACROBRACHIUM; MACROBRACHIUM NIPPONENSE; MALE; MUSCLE TISSUE; NONHUMAN; PRIORITY JOURNAL; REGULATOR GENE; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TESTIS; TRANSCRIPTION REGULATION; AMINO ACID SEQUENCE; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PALAEMONIDAE; PHYLOGENY; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANDROGENS; ANIMALS; ARTHROPOD PROTEINS; BASE SEQUENCE; CARRIER PROTEINS; CLONING, MOLECULAR; DNA, COMPLEMENTARY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GONADAL HORMONES; HEPATOPANCREAS; INSULIN; MALE; MOLECULAR SEQUENCE DATA; PALAEMONIDAE; PHYLOGENY; RNA INTERFERENCE; RNA, DOUBLE-STRANDED; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84943639699     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2014.12.007     Document Type: Article

References (46)

1. Abdu U., Davis C., Khalaila I., Sagi A. The vitellogenin cDNA of Cherax quadricarinatus encodes a lipoprotein with calcium binding ability, and its expression is induced following the removal of the androgenic gland in a sexually plastic system. Gen. Comp. Endocrinol. 2002, 127:263-272.
2. Aflalo E., Hoang T., Nguyen V., Lam Q., Nguyen D., Trinh Q., Raviv S., Sagi A. A novel two-step procedure for mass production of all-male populations of the giant freshwater prawn, Macrobrachium rosenbergii. Aquaculture 2006, 256:468-478.
3. Akam M., Dawson I., Tear G. Homeotic genes and the control of segment diversity. Development 1988, 104:123-133.
4. Averof M. Arthropod Hox genes: insights on the evolutionary forces that shape gene functions. Curr. Opin. Genet. Dev. 2002, 12:386-392.
5. Barki A., Karplus I., Manor R., Sagi A. Intersexuality and behavior in crayfish: the de-masculinization effects of androgenic gland ablation. Horm. Behav. 2006, 50:322-331.
6. Charniaux-Cotton H. Etude du determinisme des caracteres sexuels secondaires castration chirurgicale et implantation dovaire chez un crustace amphipode (Orchestia gammarella). Comptes Rendus de l' Academie des Sciences, Pairs 1953, 236:141-143.
7. Charniaux-Cotton H. Decouverte chez un crustace Amphipode (Orchestia gammarella) d'une glande endocrine responsable de la differenciation de caracteres sexuels primaires et secondaires males. Comptes Rendus de l'Academie des sciences, Pairs 1954, 239:780-782.
8. Chen Y., Zhu Q., Chen H., Zhu X., Cui Z., Qiu G. The morphological and histological observation of embryonic development in the oriental river prawn Macrobrachium nipponense. J. Shanghai Ocean Univ. (China) 2012, 21:33-40.
9. Chung J.S. An insulin-like growth factor found in hepatopancreas implicates carbohydrate metabolism of the blue crab Callinectes sapidus. Gen. Comp. Endocrinol. 2014, 199:56-64.
10. Cronin L.E. Anatomy and histology of the male reproductive system of Callinectes sapidus. Rathbun. J. Morphol. 1947, 81:209-239.
11. Daza D.O., Sundström G., Bergqvist C.A., Duan C., Larhammar D. Evolution of the insulin-like growth factor binding protein (IGFBP) family. Endocrinology 2011, 152:2278-2289.
12. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985, 39:783-791.
13. Firth S.M., Baxter R.C. Cellular actions of the insulin-like growth factor binding proteins. Endocr. Rev. 2002, 23:824-854.
14. Fu P., Thompson J.A., Bach L.A. Promotion of Cancer Cell Migration an insulin-like growth factor (IGF)-independent action of IGF-binding protein-6. J. Biol. Chem. 2007, 282:22298-22306.
15. Gu Z., Cavalcanti A., Chen F., Bouman P., Li W.H. Extent of gene duplication in the genomes of Drosophila, nematode, and yeast. Mol. Biol. Evol. 2002, 19:256-262.
16. Hongtuo F., Sufei J., Yiwei X. Current status and prospects of farming the giant river prawn (Macrobrachium rosenbergii) and the oriental river prawn (Macrobrachium nipponense) in China. Aquac. Res. 2012, 43:993-998.
17. Hwa V., Oh Y., Rosenfeld R.G. The insulin-like growth factor-binding protein (IGFBP) superfamily. Endocr. Rev. 1999, 20:761-787.
18. Jin S., Fu H., Zhou Q., Sun S., Jiang S., Xiong Y., Gong Y., Qiao H., Zhang W. Transcriptome Analysis of Androgenic Gland for Discovery of Novel Genes from the Oriental River Prawn, Macrobrachium nipponense, Using Illumina Hiseq 2000. PLoS One 2013, 8:e76840.
19. Jin S., Jiang S., Xiong Y., Qiao H., Sun S., Zhang W., Li F., Gong Y., Fu H. Molecular cloning of two tropomyosin family genes and expression analysis during development in oriental river prawn, Macrobrachium nipponense. Gene 2014, 546:390-397.
20. 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.
21. Khalaila I., Manor R., Weil S., Granot Y., Keller R., Sagi A. The eyestalk-androgenic gland-testis endocrine axis in the crayfish Cherax quadricarinatus. Gen. Comp. Endocrinol. 2002, 127:147-156.
22. Lewis E.B. A gene complex controlling segmentation in Drosophila. Nature 1978, 276:565-570.
23. 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.
24. 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, 185:90-96.
25. 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.
26. Manor R., Weil S., Oren S., Glazer L., Aflalo E.D., Ventura T., Chalifa 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.
27. Mareddy V., Rosen O., Thaggard H., Manor R., Kuballa A., Aflalo E., 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.
28. Miyako K., Cobb L.J., Francis M., Huang A., Peng B., Pintar J.E., Ariga H., Cohen P. PAPA-1 is a nuclear binding partner of IGFBP-2 and modulates its growth-promoting actions. Mol. Endocrinol. 2009, 23:169-175.
29. Montagné N., Desdevises Y., Soyez D., Toullec J.Y. Molecular evolution of the crustacean hyperglycemic hormone family in ecdysozoans. BMC Evol. Biol. 2010, 10:62.
30. Ohira T., Hasegawa Y., Tominaga S., Okuno A., Nagasawa H. Molecular cloning and expression analysis of cDNAs encoding androgenic gland hormone precursors from two porcellionidae species, Porcellio scaber and P. dilatatus. Zool. Sci. 2003, 20:75-81.
31. Oufattole M., Lin S.W.-J., Liu B., Mascarenhas D., Cohen P., Rodgers B.D. Ribonucleic acid polymerase II binding subunit 3 (Rpb3), a potential nuclear target of insulin-like growth factor binding protein-3. Endocrinology 2006, 147:2138-2146.
32. 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.
33. Rosen O., Weil S., Manor R., Roth Z., Khalaila I., Sagi A. A Crayfish Insulin-like-binding Protein another piece in the androgenic gland insulin-like hormone puzzle is revealed. J. Biol. Chem. 2013, 288:22289-22298.
34. Sagi A., Manor R., Segall C., Khalaila I. On intersexuality in the crayfish Cherax quadricarinatus: an inducible sexual plasticity model. Invertebr. Reprod. Dev. 2002, 41:27-33.
35. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 1987, 4:406-425.
36. Shen H., Zhou X., Bai A., Ren X., Zhang Y. 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. Gen. Comp. Endocrinol. 2013, 193:86-94.
37. Suzuki S., Yamasaki K. Sex-reversal of male Armadillidium vulgare (isopoda, malacostraca, crustacea) following antrectomy and partial gonadectomy. Gen. Comp. Endocrinol. 1991, 83:375-378.
38. Suzuki S., Yamasaki K. Sexual Bipotentiality of Developing Ovaries in the Terrestrial Isopod Armadillidium vulgare (Malacostraca, Crustacea). Gen. Comp. Endocrinol. 1997, 107:136-146.
39. Suzuki S., Yamasaki K., Katakura Y. Vitellogenin synthesis in andrectomized males of the terrestrial isopod, Armadillidium vulgare (Malacostracan Crustacea). Gen. Comp. Endocrinol. 1990, 77:283-291.
40. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28:2731-2739.
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. 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.
43. Ventura T., Manor R., Aflalo E.D., Weil S., Rosen O., Sagi A. Timing sexual differentiation: full functional sex reversal achieved through silencing of a single insulin-like gene in the prawn, Macrobrachium rosenbergii. Biol. Reprod. 2012, 86:90.
44. Zhang Y., Fu H., Qiao H., Jin S., Jiang S., Xiong Y., Gong Y., Zhang X. Molecular cloning and expression analysis of transformer-2 gene during development in Macrobrachium nipponense (de Haan 1849). J. World Aquacult. Soc. 2013, 44:338-349.
45. Zhang Y., Jiang S., Xiong Y., Sun S., Qiao H., Jin S., Gong Y., Fu H. Molecular cloning and expression analysis of extra sex combs gene during development in Macrobrachium nipponense. Turk. J. Fish. Aquat. Sci. 2013, 13:331-340.
46. Zhu W., Shiojima I., Ito Y., Li Z., Ikeda H., Yoshida M., Naito A.T., Nishi J., Ueno H., Umezawa A. IGFBP-4 is an inhibitor of canonical Wnt signalling required for cardiogenesis. Nature 2008, 454:345-349.