Sex ratio shifts in response to temperature are common in fish and reptiles. However, the mechanism linking temperature during early development and sex ratios has remained elusive. We show in the European sea bass (sb), a fish in which temperature effects on sex ratios are maximal before the gonads form, that juvenile males have double the DNA methylation levels of females in the promoter of gonadal aromatase (cyp19a), the enzyme that converts androgens into estrogens. Exposure to high temperature increased the cyp19a promoter methylation levels of females, indicating that induced-masculinization involves DNA methylation-mediated control of aromatase gene expression, with an observed inverse relationship between methylation levels and expression. Although different CpGs within the sb cyp19a promoter exhibited different sensitivity to temperature, we show that the increased methylation of the sb cyp19a promoter, which occurs in the gonads but not in the brain, is not a generalized effect of temperature. Importantly, these effects were also observed in sexually undifferentiated fish and were not altered by estrogen treatment. Thus, methylation of the sb cyp19a promoter is the cause of the lower expression of cyp19a in temperature-masculinized fish. In vitro, induced methylation of the sb cyp19a promoter suppressed the ability of SF-1 and Foxl2 to stimulate transcription. Finally, a CpG differentially methylated by temperature and adjacent to a Sox transcription factor binding site is conserved across species. Thus, DNA methylation of the aromatase promoter may be an essential component of the long-sought-after mechanism connecting environmental temperature and sex ratios in vertebrate species with temperature-dependent sex determination.
Vyšlo v časopise: DNA Methylation of the Gonadal Aromatase () Promoter Is Involved in Temperature-Dependent Sex Ratio Shifts in the European Sea Bass. PLoS Genet 7(12): e32767. doi:10.1371/journal.pgen.1002447 Kategorie: Research Article prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002447
1. ValenzuelaNLanceV 2004 Temperature-dependent sex determination in vertebrates Washington Smithsonian Books
2. PieauCDorizziM 2004 Oestrogens and temperature-dependent sex determination in reptiles: all is in the gonads. Journal of Endocrinology 181 367 377
3. RamseyMCrewsD 2009 Steroid signaling and temperature-dependent sex determination. Reviewing the evidence for early action of estrogen during ovarian determination in turtles. Seminars in Cell & Developmental Biology 20 283 292
4. Ospina-ÁlvarezNPiferrerF 2008 Temperature-dependent sex determination in Fish. Prevalence, existence of a single sex ratio response pattern, and possible effects on climate change. Public Library of Science One 3 e2837
5. Van NesSAndersenO 2006 Temperature effects on sex determination and ontogenetic gene expression of the aromatases cyp19a and cyp19b, and the estrogen receptors esr1 and esr2 in Atlantic halibut (Hippoglossus hippoglossus). Molecular Reproduction and Development 73 1481 1490
6. GuiguenYFostierAPiferrerFChangCF 2009 Ovarian aromatase and estrogens: A pivotal role for gonadal sex differentiation and sex change in fish. General and Comparative Endocrinology 165 352 366
7. D'CottaHFostierAGuiguenYGovorounMBaroillerJF 2001 Aromatase plays a key role during normal and temperature-induced sex differentiation of Tilapia Oreochromis niloticus. Molecular Reproduction and Development 59 265 276
8. LanceVA 2009 Is regulation of aromatase expression in reptiles the key to understanding temperature-dependent sex determination? Journal of Experimental Zoology Part A, Ecological Genetics and Physiology 311 314 322
9. SultanSE 2007 Development in context: the timely emergence of eco-devo. Trends in Ecology & Evolution 22 575 582
10. GorelickR 2003 Evolution of dioecy and sex chromosomes via methylation driving Muller's ratchet. Biological Journal of the Linnean Society 80 353
11. ZhangXHoSM 2011 Epigenetics meets endocrinology. Journal of Molecular Endocrinology 46 R11
12. Martinez-ArguellesDBPapadopoulosV 2010 Epigenetic regulation of the expression of genes involved in steroid hormone biosynthesis and action. Steroids 75 467 476
13. SimpsonER 2004 Aromatase: biologic relevance of tissue-specific expression. Seminars in Reproductive Medicine 22 11 24
14. KnowerKCToSQSimpsonERClyneCD 2010 Epigenetic mechanisms regulating CYP19 transcription in human breast adipose fibroblasts. Molecular and cellular endocrinology 321 123 130
15. FürbassRSelimyanRVanselowJ 2008 DNA methylation and chromatin accessibility of the proximal Cyp19 promoter region 1.5/2 correlate with expression levels in sheep placentomes. Molecular Reproduction and Development 75 1 7
16. VanselowJSelimyanRFürbassR 2008 DNA methylation of placenta-specific Cyp19 promoters of cattle and sheep. Experimental and Clinical Endocrinology and Diabetes 116 437 442
17. MongaRGhaiSDattaTKSinghD 2011 Tissue-specific promoter methylation and histone modifications regulate CYP19 gene expression during folliculogenesis and luteinization in buffalo ovary. General and Comparative Endocrinology 173 205 215
18. VandeputteMDupont-NivetMChavanneHChatainB 2007 A polygenic hypothesis for sex determination in the European sea bass Dicentrarchus labrax. Genetics 176 1049 1057
19. PiferrerFBlázquezMNavarroLGonzálezA 2005 Genetic, endocrine, and environmental components of sex determination and differentiation in the European sea bass (Dicentrarchus labrax L.). General and Comparative Endocrinology 142 102 110
20. Navarro-MartínLBlázquezMViñasJJolySPiferrerF 2009 Balancing the effects of rearing at low temperature during early development on sex ratios, growth and maturation in the European sea bass (Dicentrarchus labrax). Limitations and opportunities for the production of highly female-biased stocks. Aquaculture 296 347 358
21. BlázquezMZanuySCarrilloMPiferrerF 1998 Effects of rearing temperature on sex differentiation in the European sea bass (Dicentrarchus labrax L.). Journal of Experimental Zoology 281 207 216
22. PavlidisMKoumoundourosGSteriotiASomarakisSDivanachP 2000 Evidence of temperature-dependent sex determination in the European sea bass (Dicentrarchus labrax L.). Journal of Experimental Zoology 287 225 232
23. KoumoundourosGPavlidisMAnezakiLKokkariCSteriotiK 2002 Temperature sex determination in the European sea bass, Dicentrarchus labrax (L., 1758) (Teleostei, Perciformes, Moronidae): Critical sensitive ontogenetic phase. Journal of Experimental Zoology 292 573 579
24. SaillantEFostierAHaffrayPMenuBThimonierJ 2002 Temperature effects and genotype-temperature interactions on sex determination in the European sea bass (Dicentrarchus labrax L.). Journal of Experimental Zoology 292 494 505
25. MylonasCCAnezakiLDivanachPZanuySPiferrerF 2005 Influence of rearing temperature during the larval and nursery periods on growth and sex differentiation in two Mediterranean strains of Dicentrarchus labrax. Journal of Fish Biology 67 652 668
26. RoblinCBrusléJ 1983 Gonadal ontogenesis and sex differentiation in the sea bass, Dicentrarchus labrax, under fish-farming conditions. Reproduction Nutrition Development 23 115 127
27. Galay-BurgosMGealyCNavarro-MartínLPiferrerFZanuyS 2006 Cloning of the promoter from the gonadal aromatase gene of the European sea bass and identification of single nucleotide polymorphisms. Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology 145 47 53
28. WangD-SKobayashiTZhouL-YPaul-PrasanthBIjiriS 2007 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. Molecular Endocrinology 21 712 725
29. NakamotoMWangDSSuzukiAMatsudaMNagahamaY 2007 Dax1 suppresses P450arom expression in medaka ovarian follicles. Molecular Reproduction and Development 74 1239 1246
30. HsiehCL 2000 Dynamics of DNA methylation pattern. Current Opinion in Genetics & Development 10 224 228
31. NishinoKHattoriNTanakaSShiotaK 2004 DNA methylation-mediated control of Sry gene expression in mouse gonadal development. Journal of Biological Chemistry 279 22306 22313
32. MhanniAAYoderJADubeskyCMcGowanRA 2001 Cloning and sequence analysis of a zebrafish cDNA encoding DNA(cytosine-5)-methyltransferase-1. Genesis 30 213 219
33. Navarro-MartínLBlázquezMPiferrerF 2009 Masculinization of the European sea bass (Dicentrarchus labrax) by treatment with an androgen or aromatase inhibitor involves different gene expression and has distinct lasting effects on maturation. General and Comparative Endocrinology 160 3 11
34. ContractorRGForanCMLiSFWillettKL 2004 Evidence of gender - and tissue-specific promoter methylation and the potential for ethinylestradiol-induced changes in Japanese medaka (Oryzias latipes) estrogen receptor and aromatase genes. Journal of Toxicology and Environmental Health Part A 67 1 22
35. HashidaSNKitamuraKMikamiTKishimaY 2003 Temperature shift coordinately changes the activity and the methylation state of transposon Tam3 in Antirrhinum majus. Plant Physiology 132 1207 1216
36. JaenischRBirdA 2003 Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nature Genetics 33 Suppl 245 254
37. KucharskiRMaleszkaJForetSMaleszkaR 2008 Nutritional Control of Reproductive Status in Honeybees via DNA Methylation. Science 319 1827
38. KamakuraM 2011 Royalactin induces queen differentiation in honeybees. Nature 473 478 483
39. BlázquezMGonzalezAPapadakiMMylonasCPiferrerF 2008 Sex-related changes in estrogen receptors and aromatase gene expression and enzymatic activity during early development and sex differentiation in the European sea bass (Dicentrarchus labrax). General and Comparative Endocrinology 158 95 101
40. SaillantEFostierAHaffrayPMenuBLaureauS 2003 Effects of rearing density, size grading and parental factors on sex ratios of the sea bass (Dicentrarchus labrax L.) in intensive aquaculture. Aquaculture 221 183 206
41. BlázquezMNavarro-MartínLPiferrerF 2009 Expression profiles of sex differentiation-related genes during ontogenesis in the European sea bass acclimated to two different temperatures. Journal of Experimental Zoology 312B 686 700
42. HyldigSMWOstrupOVejlstedMThomsenPD 2011 Changes of DNA Methylation Level and Spatial Arrangement of Primordial Germ Cells in Embryonic Day 15 to Embryonic Day 28 Pig Embryos. Biology of Reproduction
43. Lees-MurdockDJWalshCP 2008 DNA methylation reprogramming in the germ line. Genomic Imprinting 1 15
44. SekiYHayashiKItohKMizugakiMSaitouM 2005 Extensive and orderly reprogramming of genome-wide chromatin modifications associated with specification and early development of germ cells in mice. Developmental Biology 278 440 458
45. PiferrerFBlázquezM 2005 Aromatase distribution and regulation in fish. Fish Physiology and Biochemistry 31 215 226
46. WalterRBSungHMIntanoGWWalterCA 2001 Characterization of O6-methylguanine-DNA-methyltransferase (O6-MGMT) activity in Xiphophorus fishes. Mutation Research 493 11 22
47. PannetierMFabreSBatistaFKocerARenaultL 2006 FOXL2 activates P450 aromatase gene transcription: towards a better characterization of the early steps of mammalian ovarian development. Journal of Molecular Endocrinology 36 399 413
48. JanzenFJKrenzJG 2004 Phylogenetics: Which was first, TSD or GSD? ValenzuelaNLanceV Temperature-dependent sex determination in vertebrates Washington Smithsonian Books 121 130
49. FujiiGNakamuraYTsukamotoDItoMShibaT 2006 CpG methylation at the USF-binding site is important for the liver-specific transcription of the chipmunk HP-27 gene. Biochemical Journal 395 203 209
50. JonesBChenJ 2006 Inhibition of IFN - transcription by site-specific methylation during T helper cell development. The EMBO journal 25 2443 2452
51. MirandaTBJonesPA 2007 DNA methylation: the nuts and bolts of repression. Journal of Cellular Physiology 213 384 390
52. MittwochU 2006 Sex is a threshold dichotomy mimicking a single gene effect. Trends in Genetics 22 96 100
53. MorettiAPedini Fernandez-CriadoMCittolinGGuidastriR 1999 Manual on Hatchery Production of Seabass and Gilthead Seabream Roma FAO 194
54. KuhlHTineMBeckATimmermannBKodiraC 2011 Directed sequencing and annotation of three Dicentrarchus labrax L. chromosomes by applying Sanger - and pyrosequencing technologies on pooled DNA of comparatively mapped BAC clones. Genomics doi:10.1016/j.ygeno.2011.1006.1004
55. WidschwendterMBergerJHermannMMullerHMAmbergerA 2000 Methylation and silencing of the retinoic acid receptor-ß2 gene in breast cancer. Journal of the National Cancer Institute 92 826 832
56. RohdeCZhangYReinhardtRJeltschA 2010 BISMA-Fast and accurate bisulfite sequencing data analysis of individual clones from unique and repetitive sequences. BMC Bioinformatics 11 230
57. ViñasJPiferrerF 2008 Stage-specific gene expression during fish spermatogenesis as determined by laser-capture microdissection and quantitative-PCR in sea bass (Dicentrarchus labrax) gonads. Biology of Reproduction 79 738 747
58. VillaRMoreyLRakerVABuschbeckMGutierrezA 2006 The methyl-CpG binding protein MBD1 is required for PML-RARa function. Proceedings of the National Academy of Sciences of the United States of America 103 1400 1405
59. ExcoffierLSmousePEQuattroJM 1992 Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics 131 479 491
Zvýšte si kvalifikáciu online z pohodlia domova
Nemáte účet? Registrujte sa
Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.
