A sexual shift induced by silencing of a single insulin-like gene in crayfish: Ovarian upregulation and testicular degeneration

PLoS ONE

Volumn 5, Issue 12, 2010, Pages

  Rosen, Ohad ^a   Manor, Rivka ^a   Weil, Simy ^a   Gafni, Ohad ^a   Linial, Assaf ^a   Aflalo, Eliahu D ^a   Ventura, Tomer ^a   Sagi, Amir ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; COMPLEMENTARY DNA; DOUBLE STRANDED RNA; INSULIN LIKE HORMONE; SEX HORMONE; UNCLASSIFIED DRUG; VITELLOGENIN; YOLK PROTEIN; INSULIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHERAX QUADRICARINATUS; CONTROLLED STUDY; CRAYFISH; DNA LIBRARY; ENDOCRINE CELL; FEMALE; FEMINIZATION; FUNCTIONAL GENOMICS; GENE SILENCING; HERMAPHRODITISM; HORMONE SYNTHESIS; MALE; MALE GENITAL SYSTEM; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE DEVELOPMENT; OVARY DISEASE; SEX DIFFERENTIATION; SEXUAL DEVELOPMENT; SPERMATOGENESIS; TESTIS ATROPHY; UPREGULATION; ANIMAL; BIOLOGICAL MODEL; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOHISTOCHEMISTRY; METABOLISM; METHODOLOGY; MOLECULAR EVOLUTION; OVARY; PH; PHENOTYPE; PHYSIOLOGY; TESTIS;

ASTACOIDEA; CHERAX QUADRICARINATUS; CRUSTACEA;

ANIMALS; ASTACOIDEA; EVOLUTION, MOLECULAR; FEMALE; GENE SILENCING; HYDROGEN-ION CONCENTRATION; IMMUNOHISTOCHEMISTRY; INSULIN; MALE; MODELS, GENETIC; OVARY; PHENOTYPE; RNA, DOUBLE-STRANDED; TESTIS; UP-REGULATION;

EID: 78650088252     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0015281     Document Type: Article

References (44)

1. Kloas W, Urbatzka R, Opitz R, Wurtz S, Behrends T, et al. (2009) Endocrine disruption in aquatic vertebrates. Ann N Y Acad Sci 1163: 187-200.
2. Kokokiris L, Fostier A, Athanassopoulou F, Petridis D, Kentouri M (2006) Gonadal changes and blood sex steroids levels during natural sex inversion in the protogynous Mediterranean red porgy, Pagrus pagrus (Teleostei: Sparidae). Gen Comp Endocrinol 149: 42-48.
3. Telonis-Scott M, Kopp A, Wayne ML, Nuzhdin SV, McIntyre LM (2009) Sexspecific splicing in Drosophila: widespread occurrence, tissue specificity and evolutionary conservation. Genetics 181: 421-434.
4. Glenner H, Thomsen PF, Hebsgaard MB, Sorensen MV, Willerslev E (2006) Evolution. The origin of insects. Science 314: 1883-1884.
5. Charniaux-Cotton H (1962) Androgenic gland of crustaceans. Gen Comp Endocrinol Suppl 1: 241-247.
6. Charniaux-Cotton H, Payen G (1988) Crustacean reproduction. In: Laufer H, Downer RGH, eds. Endocrinology of Selected Invertebrate Types. New York: Alan R. Liss. pp 279-303.
7. Charniaux-Cotton H (1954) Implantation of gonads from the opposite sex to male and female Orchestia gammarella. C R Hebd Seances Acad Sci 238: 953- 955.
8. Suzuki S, Yamasaki K (1998) Sex reversal by implantation of ethanol-treated androgenic glands of female isopods, Armadillidium vulgare (Malacostraca, Crustacea). Gen Comp Endocrinol 111: 367-375.
9. Taketomi Y, Nishikawa S (1996) Implantation of androgenic glands into immature female crayfish, Procambarus clarkii, with masculinization of sexual characteristics. J Crustac Biol 16: 232-239.
10. Khalaila I, Katz T, Abdu U, Yehezkel G, Sagi A (2001) 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 121: 242-249.
11. Khalaila I, Weil S, Sagi A (1999) Endocrine balance between male and female components of the reproductive system in intersex Cherax quadricarinatus (Decapoda: Parastacidae). J Exp Zool 283: 286-294.
12. Manor R, Aflalo ED, Segall C, Weil S, Azulay D, et al. (2004) Androgenic gland implantation promotes growth and inhibits vitellogenesis in Cherax quadricarinatus females held in individual compartments. Invertebr Reprod Dev 45: 151-159.
13. Ohira T, Hasegawa Y, Tominaga S, Okuno A, Nagasawa H (2003) Molecular cloning and expression analysis of cDNAs encoding androgenic gland hormone precursors from two porcellionidae species, Porcellio scaber and P. dilatatus. Zool Sci 20: 75-81.
14. Okuno A, Hasegawa Y, Ohira T, Katakura Y, Nagasawa H (1999) Characterization and cDNA cloning of androgenic gland hormone of the terrestrial isopod Armadillidium vulgare. Biochem Biophys Res Commun 264: 419-423.
15. Manor R, Weil S, Oren S, Glazer L, Aflalo ED, et al. (2007) Insulin and gender: An insulin-like gene expressed exclusively in the androgenic gland of the male crayfish. Gen Comp Endocrinol 150: 326-336.
16. Ventura T, Manor R, Aflalo ED, Weil S, Raviv S, et al. (2009) Temporal silencing of an androgenic gland-specific insulin-like gene affecting phenotypical gender differences and spermatogenesis. Endocrinology 150: 1278-1286.
17. Nef S, Verma-Kurvari S, Merenmies J, Vassalli JD, Efstratiadis A, et al. (2003) Testis determination requires insulin receptor family function in mice. Nature 426: 291-295.
18. Charniaux-Cotton H (1958) The androgenic gland of some decapodal crustaceans and particularly of Lysmata seticaudata, a species with functional protandrous hermaphroditism. C R Hebd Seances Acad Sci 246: 2814-2817.
19. Thorn MJ, Fielder DR (1991) The red cuticle on the claw of male Cherax quadricarinatus (Decapoda: Parastacidae). Mem Queensl Mus 31: 277.
20. Abdu U, Davis C, Khalaila I, Sagi A (2002) 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 127: 263-272.
21. Parnes S, Khalaila I, Hulata G, Sagi A (2003) Sex determination in crayfish: are intersex Cherax quadricarinatus (Decapoda, Parastacidae) genetically females? Genet Res 82: 107-116.
22. Sagi A, Khalaila I, Barki A, Hulata G, Karplus I (1996) Intersex red claw crayfish, Cherax quadricarinatus (von Martens): functional males with previtellogenic ovaries. Biol Bull 190: 16-23.
23. Sagi A, Khalaila I, Abdu U, Shoukrun R, Weil S (1999) A newly established ELISA showing the effect of the androgenic gland on secondary-vitellogenicspecific protein in the hemolymph of the crayfish Cherax quadricarinatus. Gen Comp Endocrinol 115: 37-45.
24. Sagi A, Manor R, Segall C, Davis C, Khalaila I (2002) On intersexuality in the crayfish Cherax quadricarinatus: an inducible sexual plasticity model. Invertebr Reprod Dev 41: 27-33.
25. Bauer RT (1986) Sex change and life history pattern in the shrimp thor manningi (decapoda: caricidea): a novel case of partial protandric hermaphroditism. Biol Bull 170: 11-31.
26. Bauer RT (2002) Tests of hypotheses on the adaptive value of an extended male phase in the hermaphroditic shrimp Lysmata wurdemanni (Caridea: Hippolytidae). Biol Bull 203: 347-357.
27. Boscolo HK, Silveira FL (2005) Reproductive biology of Palythoa caribaeorum and Protopalythoa valilbilis (Cnidaria, Anthozoa, Zoanthidea) from the southeastern coast of Brazil. Braz J Biol 65: 29-41.
28. Brook HJ, Rawlings TA, Davies RW (1994) Protogynous sex-change in the intertidal isopod Gnorimosphaeroma Oregonense (Crustacea, Isopoda). Biol Bull 187: 99-111.
29. Uchida D, Yamashita M, Kitano T, Iguchi T (2002) Oocyte apoptosis during the transition from ovary-like tissue to testes during sex differentiation of juvenile zebrafish. J Exp Biol 205: 711-718.
30. Kawamura K, Kumagai J, Sudo S, Chun SY, Pisarska M, et al. (2004) Paracrine regulation of mammalian oocyte maturation and male germ cell survival. Proc Natl Acad Sci U S A 101: 732-738.
31. Lugo JM, Morera Y, Rodriguez T, Huberman A, Ramos L, et al. (2006) Molecular cloning and characterization of the crustacean hyperglycemic hormone cDNA from Litopenaeus schmitti. Functional analysis by double-stranded RNA interference technique. FEBS J 273: 5669-5677.
32. Khalaila I, Manor R, Weil S, Granot Y, Keller R, et al. (2002) The eyestalkandrogenic gland-testis endocrine axis in the crayfish Cherax quadricarinatus. Gen Comp Endocrinol 127: 147-156.
33. Lelbach A, Muzes G, Feher J (2005) The insulin-like growth factor system: IGFs, IGF-binding proteins and IGFBP-proteases. Acta Physiol Hung 92: 97-107.
34. Belgacem YH, Martin JR (2006) Disruption of insulin pathways alters trehalose level and abolishes sexual dimorphism in locomotor activity in Drosophila. J Neurobiol 66: 19-32.
35. Nakahara Y, Matsumoto H, Kanamori Y, Kataoka H, Mizoguchi A, et al. (2006) Insulin signaling is involved in hematopoietic regulation in an insect hematopoietic organ. J Insect Physiol 52: 105-111.
36. Nijhout HF, Grunert LW (2002) Bombyxin is a growth factor for wing imaginal disks in Lepidoptera. Proc Natl Acad Sci U S A 99: 15446-15450.
37. Biondi B, Cooper DS (2008) The clinical significance of subclinical thyroid dysfunction. Endocr Rev 29: 76-131.
38. Nandi S, Banerjee PP, Zirkin BR (1999) Germ cell apoptosis in the testes of Sprague Dawley rats following testosterone withdrawal by ethane 1,2- dimethanesulfonate administration: relationship to Fas? Biol Reprod 61: 70-75.
39. Okuno A, Hasegawa Y, Nishiyama M, Ohira T, Ko R, et al. (2002) Preparation of an active recombinant peptide of crustacean androgenic gland hormone. Peptides 23: 567-572.
40. Warner RR (1975) The adaptive significance of sequential hermaphroditism in animals. Am Nat 109: 61-82.
41. Olmstead AW, LeBlanc GA (2007) The environmental-endocrine basis of gynandromorphism (intersex) in a crustacean. Int J Biol Sci 3: 77-84.
42. Aflalo ED, Hoang TTT, Nguyen VH, Lam Q, Nguyen DM, et al. (2006) A novel two-step procedure for mass production of all-male populations of the giant freshwater prawn Macrobrachium rosenbergii. Aquaculture 256: 468-478.
43. Maniatis T, Fritsch EF, Sambrook J (1982) in Molecular Cloning: A Laboratory Manual; Laboratory CSH, ed. New York.
44. Shechter A, Glazer L, Cheled S, Mor E, Weil S, et al. (2008) A gastrolith protein serving a dual role in the formation of an amorphous mineral containing extracellular matrix. Proc Natl Acad Sci U S A 105: 7129-7134.