Molecular cloning, characterization, and sexually dimorphic expression of five major sex differentiation-related genes in a Scorpaeniform fish, sablefish (Anoplopoma fimbria)

Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology

Volumn 165, Issue 2, 2013, Pages 125-137

  Smith, Elizabeth K ^a   Guzmán, José M ^a   Luckenbach, J Adam ^a,b  

^a NORTHWEST FISHERIES SCIENCE CENTER   (United States)

^b WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Cyp19a1a; Dmrt1; Foxl2; Gonadal sex differentiation; Sex determination

Indexed keywords

AROMATASE; DMRT1 PROTEIN; MESSENGER RNA; MUELLERIAN INHIBITING FACTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXL2; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL TISSUE; ANOPLOPOMA FIMBRIA; ARTICLE; CONTROLLED STUDY; FISH; GENE; GENE EXPRESSION; KARYOTYPE; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARY; PHYLOGENY; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RNA SEQUENCE; SEX DETERMINATION; SEX DIFFERENTIATION; TESTIS; TISSUE DISTRIBUTION;

AMINO ACID SEQUENCE; ANIMALS; ANTI-MULLERIAN HORMONE; CLONING, MOLECULAR; FISH PROTEINS; FISHES; FORKHEAD TRANSCRIPTION FACTORS; MOLECULAR SEQUENCE DATA; RNA, MESSENGER; SEQUENCE ALIGNMENT; SEX DIFFERENTIATION; SOX9 TRANSCRIPTION FACTOR; STEROIDOGENIC FACTOR 1; TRANSCRIPTION FACTORS;

EID: 84876345868     PISSN: 10964959     EISSN: 18791107     Source Type: Journal    
DOI: 10.1016/j.cbpb.2013.03.011     Document Type: Article

References (69)

1. Alam M.A., Kobayashi Y., Horiguchi R., Hirai T., Nakamura M. Molecular cloning and quantitative expression of sexually dimorphic markers Dmrt1 and Foxl2 during female-to-male sex change in Epinephelus merra. Gen. Comp. Endocrinol. 2008, 157:75-85.
2. Angelopoulou R., Lavranos G., Manolakou P. Sex determination strategies in 2012: towards a common regulatory model?. Reprod. Biol. Endocrinol. 2012, 10:13.
3. Baroiller J.F., D'Cotta H., Bezault E., Wessels S., Hoerstgen-Schwark G. Tilapia sex determination: where temperature and genetics meet. Comp. Biochem. Physiol. A 2009, 153:30-38.
4. Cao M., Duan J., Cheng N., Zhong X., Wang Z., Hu W., Zhao H. Sexually dimorphic and ontogenetic expression of dmrt1, cyp19a1a and cyp19a1b in Gobiocypris rarus. Comp. Biochem. Physiol. A 2012, 162:303-309.
5. Clarkson M.J., Harley V.R. Sex with two SOX on: SRY and SOX9 in testis development. Trends Endocrinol. Metab. 2002, 13:106-111.
6. Cocquet J., De Baere E., Gareil M., Pannetier M., Xia X., Fellous M., Veitia R.A. Structure, evolution and expression of the FOXL2 transcription unit. Cytogenet. Genome Res. 2003, 101:206-211.
7. Crisponi L., Deiana M., Loi A., Chiappe F., Uda M., Amati P., Bisceglia L., Zelante L., Nagaraja R., Porcu S., Ristaldi M.S., Marzella R., Rocchi M., Nicolino M., Lienhardt-Roussie A., Nivelon A., Verloes A., Schlessinger D., Gasparini P., Bonneau D., Cao A., Pilia G. The putative forkhead transcription factor FOXL2 is mutated in blepharophimosis/ptosis/epicanthus inversus syndrome. Nat. Genet. 2001, 27:159-166.
8. Devlin R.H., Nagahama Y. Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 2002, 208:191-364.
9. Dong W., Willett K.L. Local expression of CYP19A1 and CYP19A2 in developing and adult killifish (Fundulus heteroclitus). Gen. Comp. Endocrinol. 2008, 155:307-317.
10. Dong X.L., Chen S.L., Ji X.S., Shao C.W. Molecular cloning, characterization and expression analysis of Sox9a and Foxl2 genes in half-smooth tongue sole (Cynoglossus semilaevis). Acta Oceanol. Sin. 2011, 30:68-77.
11. Guiguen Y., Fostier A., Piferrer F., Chang C.F. Ovarian aromatase and estrogens: a pivotal role for gonadal sex differentiation and sex change in fish. Gen. Comp. Endocrinol. 2010, 165:352-366.
12. Guo Y., Cheng H., Huang X., Gao S., Yu H., Zhou R. Gene structure, multiple alternative splicing, and expression in gonads of zebrafish Dmrt1. Biochem. Biophys. Res. Commun. 2005, 330:950-957.
13. Hattori R.S., Murai Y., Oura M., Masuda S., Majhi S.K., Sakamoto T., Fernandino J.I., Somoza G.M., Yokota M., Strüssmann C.A. A Y-linked anti-Müllerian hormone duplication takes over a critical role in sex determination. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:2955-2959.
14. Haugen T., Almeida F.F., Andersson E., Bogerd J., Male R., Skaar K.S., Schulz R.W., Sørhus E., Wijgerde T., Taranger G.L. Sex differentiation in Atlantic cod (Gadus morhua L.): morphological and gene expression studies. Reprod. Biol. Endocrinol. 2012, 10:47.
15. Ijiri S., Berard C., Trant J.M. Characterization of gonadal and extra-gonadal forms of the cDNA encoding the Atlantic stingray (Dasyatis sabina) cytochrome P450 aromatase (CYP19). Mol. Cell. Endocrinol. 2000, 164:169-181.
16. Ijiri S., Kaneko H., Kobayashi T., Wang D.S., Sakai F., Paul-Prasanth B., Nakamura M., Nagahama Y. Sexual dimorphic expression of genes in gonads during early differentiation of a teleost fish, the Nile tilapia Oreochromis niloticus. Biol. Reprod. 2008, 78:333-341.
17. Johnsen H., Seppola M., Torgersen J.S., Delghandi M., Andersen O. Sexually dimorphic expression of dmrt1 in immature and mature Atlantic cod (Gadus morhua L.). Comp. Biochem. Physiol. B 2010, 156:197-205.
18. Kamiya T., Kai W., Tasumi S., Oka A., Matsunaga T., Mizuno N., Fujita M., Suetake H., Suzuki S., Hosoya S., Tohari S., Brenner S., Miyadai T., Venkatesh B., Suzuki Y., Kikuchi K. A trans-species missense SNP in Amhr2 is associated with sex determination in the tiger pufferfish, Takifugu rubripes (fugu). PLoS Genet. 2012, 8:e1002798.
19. Kitano T., Takamune K., Kobayashi T., Nagahama Y., Abe S.I. Suppression of P450 aromatase gene expression in sex-reversed males produced by rearing genetically female larvae at a high water temperature during a period of sex differentiation in the Japanese flounder (Paralichthys olivaceus). J. Mol. Endocrinol. 1999, 23:167-176.
20. Klüver N., Pfennig F., Pala I., Storch K., Schlieder M., Froschauer A., Gutzeit H.O., Schartl M. Differential expression of anti-Mullerian hormone (amh) and anti-Müllerian hormone receptor type II (amhrII) in the teleost medaka. Dev. Dyn. 2007, 236:271-281.
21. Kobayashi T., Kajiura-Kobayashi H., Nagahama Y. Induction of XY sex reversal by estrogen involves altered gene expression in a teleost, tilapia. Cytogenet. Genome Res. 2003, 101:289-294.
22. Kobayashi Y., Kobayashi T., Nakamura M., Sunobe T., Morrey C.E., Suzuki N., Nagahama Y. Characterization of two types of cytochrome P450 aromatase in the serial-sex changing gobiid fish, Trimma okinawae. Zool. Sci. 2004, 21:417-425.
23. Liu Z., Wu F., Jiao B., Zhang X., Hu C., Huang B., Zhou L., Huang X., Wang Z., Zhang Y., Nagahama Y., Cheng C.H., Wang D. Molecular cloning of doublesex and mab-3-related transcription factor 1, forkhead transcription factor gene 2, and two types of cytochrome P450 aromatase in Southern catfish and their possible roles in sex differentiation. J. Endocrinol. 2007, 194:223-241.
24. Liu Z.H., Zhang Y.G., Wang D.S. Studies on feminization, sex determination, and differentiation of the Southern catfish, Silurus meridionalis-a review. Fish Physiol. Biochem. 2010, 36:223-235.
25. Loffler K.A., Zarkower D., Koopman P. Etiology of ovarian failure in blepharophimosis ptosis epicanthus inversus syndrome: FOXL2 is a conserved, early-acting gene in vertebrate ovarian development. Endocrinology 2003, 144:3237-3243.
26. Luckenbach J.A., Godwin J., Daniels H.V., Borski R.J. Gonadal differentiation and effects of temperature on sex determination in southern flounder (Paralichthys lethostigma). Aquaculture 2003, 216:315-327.
27. Luckenbach J.A., Early L.W., Rowe A.H., Borski R.J., Daniels H.V., Godwin J. Aromatase cytochrome P450: cloning, intron variation, and ontogeny of gene expression in southern flounder (Paralichthys lethostigma). J. Exp. Zool. 2005, 303A:643-656.
28. Luckenbach J.A., Iliev D.B., Goetz F.W., Swanson P. Identification of differentially expressed ovarian genes during primary and early secondary oocyte growth in coho salmon, Oncorhynchus kisutch. Reprod. Biol. Endocrinol. 2008, 6:2.
29. Luckenbach J.A., Borski R.J., Daniels H.V., Godwin J. Sex determination in flatfishes: mechanisms and environmental influences. Semin. Cell Dev. Biol. 2009, 20:256-263.
30. Luckenbach J.A., Dickey J.T., Swanson P. Follicle-stimulating hormone regulation of ovarian transcripts for steroidogenesis-related proteins and cell survival, growth and differentiation factors in vitro during early secondary oocyte growth in coho salmon. Gen. Comp. Endocrinol. 2011, 171:52-63.
31. Luo Y.S., Hu W., Liu X.C., Lin H.R., Zhu Z.Y. Molecular cloning and mRNA expression pattern of Sox9 during sex reversal in orange-spotted grouper (Epinephelus coioides). Aquaculture 2010, 306:322-328.
32. Mason J.C., Beamish R.J., McFarlane G.A. Sexual maturity, fecundity, spawning, and early life history of sablefish (Anoplopoma fimbria) off the Pacific coast of Canada. Can. J. Fish. Aquat. Sci. 1983, 40:2126-2134.
33. Matsuda M., Nagahama Y., Shinomiya A., Sato T., Matsuda C., Kobayashi T., Morrey C.E., Shibata N., Asakawa S., Shimizu N., Hori H., Hamaguchi S., Sakaizumi M. DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 2002, 417:559-563.
34. Matsuoka M.P., van Nes S., Andersen Ø., Benfey T.J., Reith M. Real-time PCR analysis of ovary- and brain-type aromatase gene expression during Atlantic halibut (Hippoglossus hippoglossus) development. Comp. Biochem. Physiol. B 2006, 144:128-135.
35. Morias da Silva S., Hacker A., Harley V., Goodfellow P., Swain A., Lovell-Badge R. Sox9 expression during gonadal development implies a conserved role for the gene in testis differentiation in mammals and birds. Nat. Genet. 1996, 14:62-68.
36. Morinaga C., Saito D., Nakamura S., Sasaki T., Asakawa S., Shimizu N., Mitani H., Furutani-Seiki M., Tanaka M., Kondoh H. The hotei mutation of medaka in the anti-Müllerian hormone receptor causes the dysregulation of germ cell and sexual development. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:9691-9696.
37. Morita S.H., Morita K., Nishimura A. Sex-biased dispersal and growth in sablefish (Anoplopoma fimbria) in the northeastern Pacific Ocean. Environ. Biol. Fish. 2012, 94:505-511.
38. Myosho T., Otake H., Masuyama H., Matsuda M., Kuroki Y., Fujiyama A., Naruse K., Hamaguchi S., Sakaizumi M. Tracing the emergence of a novel sex-determining gene in medaka, Oryzias luzonensis. Genetics 2012, 191:163-170.
39. Nakamoto M., Suzuki A., Matsuda M., Nagahama Y., Shibata N. Testicular type Sox9 is not involved in sex determination but might be in the development of testicular structures in the medaka, Oryzias latipes. Biochem. Biophys. Res. Commun. 2005, 333:729-736.
40. Nakamura S., Watakabe I., Nishimura T., Toyoda A., Taniguchi Y., Tanaka M. Analysis of medaka sox9 orthologue reveals a conserved role in germ cell maintenance. PLoS One 2012, 7:e29982.
41. Pannetier M., Fabre S., Batista F., Kocer A., Renault L., Jolivet G., Mandon-Pépin B., Cotinot C., Veitia R., Pailhoux E. FOXL2 activates P450 aromatase gene transcription: towards a better characterization of the early steps of mammalian ovarian development. J. Mol. Endocrinol. 2006, 36:399-413.
42. Phillips, R.B., Faber-Hammond, J., Luckenbach, J.A., in press. The sablefish (Anoplopoma fimbria) karyotype including the location of 5S and 18S rDNA and information on cell culture conditions. Aquac. Res. doi:10.1111/j.1365-2109.2012.03177.x.
43. Piferrer F., Guiguen Y. Fish gonadogenesis. Part II: molecular biology and genomics of sex differentiation. Rev. Fish. Sci. 2008, 16:35-55.
44. Raghuveer K., Senthilkumaran B., Sudhakumari C.C., Sridevi P., Rajakumar A., Singh R., Murugananthkumar R., Majumdar K.C. Dimorphic expression of various transcription factor and steroidogenic enzyme genes during gonadal ontogeny in the air-breathing catfish, Clarias gariepinus. Sex. Dev. 2011, 5:213-223.
45. Raymond C.S., Murphy M.W., O'Sullivan M.G., Bardwell V.J., Zarkower D. Dmrt1, a gene related to worm and fly sexual regulators, is required for mammalian testis differentiation. Genes Dev. 2000, 14:2587-2595.
46. Rodríguez-Marí A., Yan Y.L., BreMiller R.A., Wilson C., Cañestro C., Postlethwait J.H. Characterization and expression pattern of zebrafish anti-Mullerian hormone (amh) relative to sox9a, sox9b, and cyp19a1a, during gonad development. Gene Expr. Patterns 2005, 5:655-667.
47. Sandra G.E., Norma M.M. Sexual determination and differentiation in teleost fish. Rev. Fish Biol. Fish. 2010, 20:101-121.
48. Shen X., Cui J., Yang G., Gong Q., Gu Q. Expression detection of DMRTs and two sox9 genes in Takifugu rubripes (Tetraodontidae, Vertebrata). J. Ocean Univ. China 2007, 6:182-186.
49. Shiraishi E., Yoshinaga N., Miura T., Yokoi H., Wakamatsu Y., Abe S., Kitano T. Müllerian inhibiting substance is required for germ cell proliferation during early gonadal differentiation in medaka (Oryzias latipes). Endocrinology 2008, 149:1813-1819.
50. Siegfried K.R. In search of determinants: gene expression during gonadal sex differentiation. J. Fish Biol. 2010, 76:1879-1902.
51. Smith C.A., Roeszler K.N., Ohnesorg T., Cummins D.M., Farlie P.G., Doran T.J., Sinclair A.H. The avian Z-linked gene DMRT1 is required for male sex determination in the chicken. Nature 2009, 461:267-271.
52. Swain A., Lovell-Badge R. Mammalian sex determination: a molecular drama. Genes Dev. 1999, 13:755-767.
53. 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.
54. Uhlenhaut N.H., Treier M. Foxl2 function in ovarian development. Mol. Genet. Metab. 2006, 88:225-234.
55. Vigier B., Forest M.G., Eychenne B., Bézard J., Garrigou O., Robel P., Josso N. Anti-MülIerian hormone produces endocrine sex reversal of fetal ovaries. Proc. Natl. Acad. Sci. U. S. A. 1989, 86:3684-3688.
56. Vizziano D., Randuineau G., Baron D., Cauty C., Guiguen Y. Characterization of early molecular sex differentiation in rainbow trout, Oncorhynchus mykiss. Dev. Dyn. 2007, 236:2198-2206.
57. Vizziano-Cantonnet D., Baron D., Mahè S., Cauty C., Fostier A., Guiguen Y. Estrogen treatment up-regulates female genes but does not suppress all early testicular markers during rainbow trout male-to-female gonadal transdifferentiation. J. Mol. Endocrinol. 2008, 41:277-288.
58. Wang X.G., Orban L. Anti-Müllerian hormone and 11 β-hydroxylase show reciprocal expression to that of aromatase in the transforming gonad of zebrafish males. Dev. Dyn. 2007, 236:1329-1338.
59. Wang D., Kobayashi T., Zhou L., Nagahama Y. Molecular cloning and gene expression of Foxl2 in the Nile tilapia, Oreochromis niloticus. Biochem. Biophys. Res. Commun. 2004, 320:83-89.
60. Wang D.S., Kobayashi T., Zhou L.Y., Paul-Prasanth B., Ijiri S., Sakai F., Okubo K., Morohashi K., Nagahama Y. Foxl2 up-regulates aromatase gene transcription in a female-specific manner by binding to the promoter as well as interacting with Ad4 binding protein/steroidogenic factor 1. Mol. Endocrinol. 2007, 21:712-725.
61. Wang D.S., Zhou L.Y., Kobayashi T., Matsuda M., Shibata Y., Sakai F., Nagahama Y. Doublesex- and Mab-3-related transcription factor-1 repression of aromatase transcription, a possible mechanism favoring the male pathway in tilapia. Endocrinology 2010, 151:1331-1340.
62. Western P.S., Harry J.L., Graves J.A., Sinclair A.H. Temperature-dependent sex determination in the American alligator: AMH precedes SOX9 expression. Dev. Dyn. 1999, 216:411-419.
63. Wilhelm D., Palmer S., Koopman P. Sex determination and gonadal development in mammals. Physiol. Rev. 2007, 87:1-28.
64. Wu G.C., Chiu P.C., Lin C.J., Lyu Y.S., Lan D.S., Chang C.F. Testicular dmrt1 is involved in the sexual fate of the ovotestis in the protandrous black porgy. Biol. Reprod. 2012, 86:1-11.
65. Yamaguchi T., Yamaguchi S., Hirai T., Kitano T. Follicle-stimulating hormone signaling and Foxl2 are involved in transcriptional regulation of aromatase gene during gonadal sex differentiation in Japanese flounder, Paralichthys olivaceus. Biochem. Biophys. Res. Commun. 2007, 359:935-940.
66. Yano A., Guyomard R., Nicol B., Jouanno E., Quillet E., Klopp C., Cabau C., Bouchez O., Fostier A., Guiguen Y. An immune-related gene evolved into the master sex-determining gene in rainbow trout, Oncorhynchus mykiss. Curr. Biol. 2012, 22:1423-1428.
67. Yao H.H. The pathway to femaleness: current knowledge on embryonic development of the ovary. Mol. Cell. Endocrinol. 2005, 230:87-93.
68. Yokoi H., Kobayashi T., Tanaka M., Nagahama Y., Wakamatsu Y., Takeda H., Araki K., Morohashi K., Ozato K. sox9 in a teleost fish, medaka (Oryzias latipes): evidence for diversified function of Sox9 in gonad differentiation. Mol. Reprod. Dev. 2002, 63:5-16.
69. Yoshinaga N., Shiraishi E., Yamamoto T., Iguchi T., Abe S., Kitano T. Sexually dimorphic expression of a teleost homologue of Müllerian inhibiting substance during gonadal sex differentiation in Japanese flounder, Paralichthys olivaceus. Biochem. Biophys. Res. Commun. 2004, 322:508-513.