Characterization of Sex Determination and Sex Differentiation Genes in Latimeria

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Forconi, Mariko ^a   Canapa, Adriana ^a   Barucca, Marco ^a   Biscotti, Maria A ^a   Capriglione, Teresa ^b   Buonocore, Francesco ^c   Fausto, Anna M ^c   Makapedua, Daisy M ^d   Pallavicini, Alberto ^e   Gerdol, Marco ^e   De Moro, Gianluca ^e   Scapigliati, Giuseppe ^c   Olmo, Ettore ^a   Schartl, Manfred ^f  

^a UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^c UNIVERSITY OF TUSCIA   (Italy)

^d SAM RATULANGI UNIVERSITY   (Indonesia)

^e UNIVERSITY OF TRIESTE   (Italy)

^f UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATASE; FIBROBLAST GROWTH FACTOR 16; FIBROBLAST GROWTH FACTOR 9; TRANSCRIPTION FACTOR SOX10; TRANSCRIPTION FACTOR SOX8; TRANSCRIPTION FACTOR SOX9; TRANSCRIPTOME; WNT4 PROTEIN; FISH PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

AMH GENE; ANIMAL TISSUE; AROMATASE GENE; ARTICLE; CONTROLLED STUDY; DMRT1 GENE; FEMALE; FGF16 GENE; FGF20 GENE; FGF9 GENE; GENE; GENE EXPRESSION; GENE LOCUS; GENE STRUCTURE; GENETIC CONSERVATION; GENETIC IDENTIFICATION; GENOME; GSDF GENE; HUMAN; INHIBIN ALPHA GENE; LATIMERIA; LATIMERIA CHALUMNAE; LATIMERIA MENADOENSIS; LIVER LEVEL; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; SEQUENCE ALIGNMENT; SEX DETERMINATION; SEX DIFFERENTIATION; SOX 10 GENE; SOX 8 GENE; SOX 9 GENE; SYNTENY; TESTIS; UNINDEXED SEQUENCE; WNT4 GENE; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; FISH; GENE EXPRESSION PROFILING; GENETICS; GENOMICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; MOUSE; SEX DETERMINATION PROCESS;

AMPHIBIA; COELACANTHIDAE; GALLUS GALLUS; LATIMERIA; LATIMERIA CHALUMNAE; LATIMERIA MENADOENSIS; MUS; PISCES; REPTILIA; TELEOSTEI; VERTEBRATA;

AMINO ACID SEQUENCE; ANIMALS; FEMALE; FISH PROTEINS; FISHES; GENE EXPRESSION PROFILING; GENOMICS; HUMANS; MALE; MICE; MOLECULAR SEQUENCE DATA; SEX DETERMINATION PROCESSES; SEX DIFFERENTIATION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84876703168     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0056006     Document Type: Article

References (95)

1. Hayes TB, (1998) Sex determination and primary sex differentiation in amphibian: genetic and developmental mechanisms. J Exp Zool 281: 373-399.
2. Graves JAM, Peichel CL, (2010) Are homologies in vertebrate sex determination due to shared ancestry or to limited options? Genome Biol 11: 205.
3. McClelland K, Bowles J, Koopman P, (2012) Male sex determination: insights into molecular mechanisms. Asian J Androl 14: 164-171.
4. Uhlenhaut NH, Jakob S, Anlag K, Eisenberger T, Sekido R, et al. (2009) Somatic sex reprogramming of adult ovaries to testes by FOXL2 ablation. Cell 139: 1130-1142.
5. Matson CK, Murphy MW, Sarver AL, Griswold MD, Bardwell VJ, et al. (2011) DMRT1 prevents female reprogramming in the postnatal mammalian testis. Nature 476: 101-104.
6. Herpin A, Schartl M, (2011) Sex determination: switch and suppress. Curr Biol 21: R656-9.
7. Clinton M, Zhao D, Nandi S, McBride D, (2012) Evidence for avian cell autonomous sex identity (CASI) and implications for the sex-determination process? Chromosome Res 20: 177-190.
8. Zarkower D (2006) Somatic sex determination (February 10, 2006), in WormBook. Edited by The C. elegans Research Community.doi/10.1895/wormbook.1.84.1, http://www.wormbook.org.
9. Abinawanto, Shimada K, Yoshida K, Saito N, (1996) Effects of aromatase inhibitor on sex differentiation and levels of P45017 alpha and P450arom messenger ribonucleic acid of gonads in chicken embryos. Gen Comp Endocrinol 102: 241-246.
10. Akazome Y, Mori T, (1999) Evidence of sex reversal in the gonads of chicken embryos after oestrogen treatment as detected by expression of lutropin receptor. J Reprod Fertil 115: 9-14.
11. Baker PJ, Moore HD, Burgess AM, Mittwoch U, (1993) Gonadal sex differentiation in embryos and neonates of the marsupial, Monodelphis domestica: arrest of testis development in postterm embryos. J Anat 182: 267-273.
12. Coveney D, Shaw G, Renfree MB, (2001) Estrogen-induced gonadal sex reversal in the tammar wallaby. Biol Reprod 65: 613-621.
13. Fadem BH, (2000) Perinatal exposure to estradiol masculinizes aspects of sexually dimorphic behavior and morphology in gray short-tailed opossums (Monodelphis domestica). Horm Behav 37: 79-85.
14. Guiguen Y, Baroiller JF, Ricordel MJ, Iseki K, Mcmeel OM, et al. (1999) Involvement of estrogens in the process of sex differentiation in two fish species: the rainbow trout (Oncorhynchus mykiss) and a tilapia (Oreochromis niloticus). Mol Reprod Dev 54: 154-162.
15. Kobayashi T, Kajiura-Kobayashi H, Nagahama Y, (2003) Induction of XY sex reversal by estrogen involves altered gene expression in a teleost, tilapia. Cytogenet Genome Res 101: 289-294.
16. Mackenzie CA, Berrill M, Metcalfe C, Pauli BD, (2003) Gonadal differentiation in frogs exposed to estrogenic and antiestrogenic compounds. Environ Toxicol Chem 22: 2466-2475.
17. Mittwoch U, (1998) Phenotypic manifestations during the development of the dominant and default gonads in mammals and birds. J Exp Zool 281: 466-471.
18. Pieau C, Dorizzi M, (2004) Oestrogens and temperature-dependent sex determination in reptiles: all is in the gonads. J Endocrinol 181: 367-377.
19. Renfree MB, Coveney D, Shaw G, (2001) The influence of estrogen on the developing male marsupial. Reprod Fertil Dev 13: 231-240.
20. Shaw G, Renfree MB, Short RV, WS O, (1988) Experimental manipulation of sexual differentiation in wallaby pouch young treated with exogenous steroids. Development 104: 689-701.
21. Ramsey M, Crews D, (2009) Steroid signaling and temperature-dependent sex determination. Reviewing the evidence for early action of estrogen during ovarian determination in turtles. Semin Cell Dev Biol 20: 283-292.
22. Schartl M, (2004) Sex chromosome evolution in non-mammalian vertebrates. Curr Opin Genet Dev 14: 634-641.
23. Uller T, Helanterä H, (2011) From the origin of sex-determining factors to the evolution of sex-determining systems. Q Rev Biol 86: 163-180.
24. Biason-Lauber A, (2010) Control of sex development. Best Pract Res Clin Endocrinol Metab 24: 163-186.
25. Kashimada K, Koopman P, (2010) Sry: the master switch in mammalian sex determination. Development 137: 3921-3930.
26. Matsuda M, Nagahama Y, Shinomiya A, Sato T, Matsuda C, et al. (2002) DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 417: 559-563.
27. Nanda I, Kondo M, Hornung U, Asakawa S, Winkler C, et al. (2002) A duplicated copy of DMRT1 in the sex-determining region of the Y chromosome of the medaka, Oryzias latipes. Proc Natl Acad Sci USA 99: 11778-11783.
28. Yoshimoto S, Okada E, Umemoto H, Tamura K, Uno Y, et al. (2008) A W-linked DM-domain gene, DM-W, participates in primary ovary development in Xenopus laevis. Proc Natl Acad Sci USA 105: 2469-2474.
29. Myosho T, Otake H, Masuyama H, Matsuda M, Kuroki Y, et al. (2012) Tracing the emergence of a novel sex-determining gene in medaka, Oryzias luzonensis. Genetics 191: 163-170.
30. Hattori RS, Murai Y, Oura M, Masuda S, Majhi SK, et al. (2012) A Y-linked anti-Müllerian hormone duplication takes over a critical role in sex determination. Proc Natl Acad Sci USA 109: 2955-2959.
31. Kamiya T, Kai W, Tasumi S, Oka A, Matsunaga T, et al. (2012) A Trans-Species Missense SNP in Amhr2 Is Associated with Sex Determination in the Tiger Pufferfish, Takifugu rubripes (Fugu). PLoS Genet 8: e1002798.
32. Angelopoulou R, Lavranos G, Manolakou P, (2012) Sex determination strategies in 2012: towards a common regulatory model? Reprod Biol Endocrinol 10: 13.
33. Graves JAM, (1995) The evolution of mammalian sex chromosomes and the origin of sex-determining genes. Philos Trans R Soc Lond B Biol Sci 350: 305-311.
34. Graves JAM, (2008) Weird animal genomes and the evolution of vertebrate sex and sex chromosomes. Annu Rev Genet 42: 565-586.
35. Borg B, (1994) Androgens in teleost fishes. Comp Biochem Physiol Part C 109: 219-245.
36. Brunner B, Hornung U, Shan Z, Nanda I, Kondo M, et al. (2001) Genomic organization and expression of the doublesex-related gene cluster in vertebrates and detection of putative regulatory regions for DMRT1. Genomics 77: 8-17.
37. Chardard D, Kuntz S, Chesnel A, Flament S, (2003) Effects of androgens on sex differentiation of the urodele Pleurodeles waltl. J Exp Zoolog A Comp Exp Biol 296: 46-55.
38. El-Mogharbel N, Wakefield M, Deakin JE, Tsend-Ayush E, Grützner F, et al. (2007) DMRT gene cluster analysis in the platypus: new insights into genomic organization and regulatory regions. Genomics 89: 10-21.
39. Gautier A, Le Gac F, Lareyre JJ, (2011) The gsdf gene locus harbors evolutionary conserved and clustered genes preferentially expressed in fish previtellogenic oocytes. Gene 472: 7-17.
40. Gautier A, Sohm F, Joly JS, Le Gac F, Lareyre JJ, (2011) The proximal promoter region of the zebrafish gsdf gene is sufficient to mimic the spatio-temporal expression pattern of the endogenous gene in Sertoli and granulosa cells. Biol Reprod 85: 1240-1251.
41. Gnessi L, Emidi A, Jannini EA, Carosa E, Maroders M, et al. (1995) Testicular development involves the spatiotemporal control of PDGFs and PDGF receptors gene expression and action. J Cell Biol 131: 1105-1121.
42. Gnessi L, Basciani S, Mariani S, Arizzi M, Spera G, et al. (2000) Leydig cell loss and spermatogenic arrest in platelet-derived growth factor (PDGF)-A-deficient mice. J Cell Biol 149: 1019-1025.
43. Kim S, Kettlewell JR, Anderson RC, Bardwell VJ, Zarkower D, (2003) Sexually dimorphic expression of multiple doublesex-related genes in the embryonic mouse gonad. Gene Expr Patterns 3: 77-82.
44. O'Donnell L, Stanton PG, Wreford NG, Robertson DM, McLachlan RI, (1996) Inhibition of 5-alpha-reductase activity impairs the testosterone-dependent restoration of spermiogenesis in adult rats. Endocrinology 137: 2703-2710.
45. Shibata Y, Paul-Prasanth B, Suzuki A, Usami T, Nakamoto M, et al. (2010) Expression of gonadal soma derived factor (GSDF) is spatially and temporally correlated with early testicular differentiation in medaka. Gene Expr Patterns 10: 283-289.
46. Smith CA, McClive PJ, Hudson Q, Sinclair AH, (2005) Male-specific cell migration into the developing gonad is a conserved process involving PDGF signaling. Dev Biol 284: 337-350.
47. Zaccanti F, Petrini S, Rubatta ML, Stagni AM, Giorgi PP, (1994) Accelerated female differentiation of the gonad by inhibition of steroidogenesis in amphibia. Comp Biochem Physiol A 107: 171-179.
48. Amemiya CT, Alföldi J, Lee AP, Fan S, Brinkmann H, et al. (2013) The African coelacanth genome provides insights into the tetrapod evolution. Nature (in press).
49. Pallavicini A, Canapa A, Barucca M, Alföldi J, Biscotti MA, et al. (2013) Analysis of the transcriptome of the Indonesian coelacanth Latimeria menadoensis. (submitted).
50. Canapa A, Olmo E, Forconi M, Pallavicini A, Makapedua MD, et al. (2012) Composition and phylogenetic analysis of vitellogenin coding sequences in the Indonesian coelacanth Latimeria menadoensis. J Exp Zool B Mol Dev Evol 318: 404-416.
51. Makapedua DM, Barucca M, Forconi M, Antonucci N, Bizzaro D, et al. (2011) Genome size, GC percentage and 5 mC level in the Indonesian coelacanth Latimeria menadoensis. Mar Genomics 4: 167-172.
52. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, et al. (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29: 644-652.
53. Zhang Z, Li J, Zhao XQ, Wang J, Wong GK, et al. (2006) KaKs Calculator: Calculating Ka and Ks through model selection and model averaging. Geno Prot Bioinfo 4: 259-263.
54. Nei M, Gojobori T, (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3: 418-426.
55. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
56. Zhang J, Rosenberg HF, Nei M, (1998) Positive Darwinian selection after gene duplication in primate ribonuclease genes. Proc Natl Acad Sci USA 95: 3708-3713.
57. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) ClustalW and ClustalX version 2 (2007). Bioinformatics 23: 2947-2948.
58. Eisenberg E, Levanon EY, (2003) Human housekeeping genes are compact. Trends Genet 19: 362-365.
59. Huelsenbeck JP, Ronquist F, Nielsen R, Bollback JP, (2001) Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294: 2310-2314.
60. Dayhoff M, Schwartz R, Orcutt B, (1978) A model of evolutionary change in protein. Atlas Protein Seq Struct 5: 345-352.
61. Jones DT, Taylor WR, Thornton JM, (1992) The rapid generation of mutation data matrices from protein sequences. CABIOS 8: 275-282.
62. Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (* and other methods) version 4. Sunderland, MA: Sinauer Associates.
63. Itoh N, Konishi M, (2007) The zebrafish FGF family. Zebrafish 4: 179-186.
64. Sun YL, Zeng S, Ye K, Yang C, Li MH, et al. (2012) Involvement of FGF9/16/20 subfamily in female germ cell development of the Nile tilapia, Oreochromis niloticus. Fish Physiol Biochem 38: 1427-1439.
65. Herpin A, Schartl M, (2011) Dmrt1 genes at the crossroads: a widespread and central class of sexual development factors in fish. FEBS J 278: 1010-1019.
66. Matson CK, Zarkower D, (2012) Sex and the singular DM domain: insights into sexual regulation, evolution and plasticity. Nat Rev Genet 13: 163-174.
67. Chue J, Smith CA, (2011) Sex determination and sexual differentiation in the avian model. FEBS J 278: 1027-1034.
68. Raymond CS, Shamu CE, Shen MM, Seifert KJ, Hirsch B, et al. (1998) Evidence for evolutionary conservation of sex-determining genes. Nature 391: 691-695.
69. Rhen T, Schroeder T, (2010) Molecular mechanisms of sex determination in reptiles. Sex Dev 4: 16-28.
70. Anand A, Patel M, Lalremruata A, Singh AP, Agrawal R, et al. (2008) Multiple alternative splicing of DMRT1 during gonadogenesis in Indian mugger, a species exhibiting temperature-dependent sex determination. Gene 425: 56-63.
71. Guo Y, Cheng H, Huang X, Gao S, Yu H, et al. (2005) Gene structure, multiple alternative splicing, and expression in gonads of zebrafish DMRT1. Biochem Biophys Res Commun 330: 950-957.
72. Zhao Y, Lu H, Yu H, Cheng H, Zhou R, (2007) Multiple alternative splicing in gonads of chicken DMRT1. Dev Genes Evol 217: 119-126.
73. Shinomiya A, Otake H, Togashi K, Hamaguchi S, Sakaizumi M, (2004) Field survey of sex-reversals in the medaka, Oryzias latipes: genotypic sexing of wild populations. Zoolog Sci 21: 613-619.
74. Bogart JP, Balon EK, Bruton MN, (1994) The chromosomes of the living coelacanth and their remarkable similarity to those of one of the most ancient frogs. J Hered 85: 322-325.
75. Kim Y, Kobayashi A, Sekido R, DiNapoli L, Brennan J, et al. (2006) Fgf9 and Wnt4 Act as Antagonistic Signals to Regulate Mammalian Sex Determination. PLoS Biol 4: e187.
76. Nakatani M, Takehara Y, Sugino H, Matsumoto M, Hashimoto O, et al. (2008) Transgenic expression of a myostatin inhibitor derived from follistatin increases skeletal muscle mass and ameliorates dystrophic pathology in mdx mice. FASEB J 22: 477-487.
77. Higasa K, Nikaido M, Saito TL, Yoshimura J, Suzuki Y, et al. (2012) Extremely slow rate of evolution in the HOX cluster revealed by comparison between Tanzanian and Indonesian coelacanths. Gene 505: 324-332.
78. Johnsen H, Andersen Ø, (2012) Sex dimorphic expression of five dmrt genes identified in the Atlantic cod genome. The fish-specific dmrt2b diverged from dmrt2a before the fish whole-genome duplication. Gene 505: 221-232.
79. Herpin A, Schindler D, Kraiss A, Hornung U, Winkler C, et al. (2007) Inhibition of primordial germ cell proliferation by the medaka male determining gene DmrtIbY. BMC Dev Biol 7: 99.
80. Hornung U, Herpin A, Schartl M, (2007) Expression of the male determining gene dmrtIbY and its autosomal coorthologue dmrt1a in medaka. Sex Dev 1: 197-206.
81. Bratus A, Slota E, (2009) Comparative cytogenetic and molecular studies of DM domain genes in pig and cattle. Cytogenet Genome Res 126: 180-185.
82. Smith CA, Hurley TM, McClive PJ, Sinclair AH, (2002) Restricted expression of DMRT3 in chicken and mouse embryos. Gene Expr Patterns 2: 69-72.
83. Winkler C, Hornung U, Kondo M, Neuner C, Duschl J, et al. (2004) Developmentally regulated and non-sex-specific expression of autosomal dmrt genes in embryos of the Medaka fish (Oryzias latipes). Mech Dev 121: 997-1005.
84. Kapoor BG, Khanna B (2004) Ichthyology Handbook. Berlin: Springer 487.
85. Nakamura S, Watakabe I, Nishimura T, Picard JY, Toyoda A, et al. (2012) Hyperproliferation of mitotically active germ cells due to defective anti-Müllerian hormone signaling mediates sex reversal in medaka. Development 139: 2283-2287.
86. Klüver N, Pfennig F, Pala I, Storch K, Schlieder M, et al. (2007) Differential expression of anti-Müllerian hormone (amh) and anti-Müllerian hormone receptor type II (amhrII) in the teleost medaka. Dev Dyn 236: 271-281.
87. Pala I, Klüver N, Thorsteinsdóttir S, Schartl M, Coelho MM, (2008) Expression pattern of anti-Müllerian hormone (amh) in the hybrid fish complex of Squalius alburnoides. Gene 410: 249-258.
88. Halm S, Rocha A, Miura T, Prat F, Zanuy S, (2006) Anti-Müllerian hormone (AMH/AMH) in the European sea bass: its gene structure, regulatory elements, and the expression of alternatively-spliced isoforms. Gene 388: 148-158.
89. Beau C, Rauch M, Joulin V, Jégou B, Guerrier D, (2000) GATA-1 is a potential repressor of anti-Müllerian hormone expression during the establishment of puberty in the mouse. Mol Reprod Dev 56: 124-138.
90. Ooe H, Chen Q, Kon J, Sasaki K, Miyoshi H, et al. (2012) Proliferation of rat small hepatocytes requires follistatin expression. J Cell Physiol 227: 2363-2370.
91. Rey R, Lukas-Croisier C, Lasala C, Bedecarrás P, (2003) AMH/MIS: what we know already about the gene, the protein and its regulation. Mol Cell Endocrinol 211: 21-31.
92. El-Awady MK, El-Garf W, El-Houssieny L, (2004) Steroid 5alpha reductase mRNA type 1 is differentially regulated by androgens and glucocorticoids in the rat liver. Endocr J 51: 37-46.
93. Barrionuevo F, Georg I, Scherthan H, Lécureuil C, Guillou F, et al. (2009) Testis cord differentiation after the sex determination stage is independent of Sox9 but fails in the combined absence of Sox9 and Sox8. Dev Biol 327: 301-312.
94. Nakamura S, Watakabe I, Nishimura T, Toyoda A, Taniguchi Y, et al. (2012) Analysis of Medaka sox9 Orthologue Reveals a Conserved Role in Germ Cell Maintenance. PLoS ONE 7: e29982.
95. Bertrand S, Camasses A, Somorjai I, Belgacem MR, Chabrol O, et al. (2011) Amphioxus FGF signaling predicts the acquisition of vertebrate morphological traits. Proc Natl Acad Sci USA 108: 9160-9165.