Bmp15 Is an Oocyte-Produced Signal Required for Maintenance of the Adult Female Sexual Phenotype in Zebrafish
Although the zebrafish is a major model organism, how they determine sex is not well understood. In domesticated zebrafish, sex determination appears to be polygenic, being influenced by multiple genetic factors that may vary from strain to strain, and additionally can be influenced by environmental...
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| creator | Dranow, Daniel B Hu, Kevin Bird, April M Lawry, S Terese Adams, Melissa T Sanchez, Angelica Amatruda, James F Draper, Bruce W |
| description | Although the zebrafish is a major model organism, how they determine sex is not well understood. In domesticated zebrafish, sex determination appears to be polygenic, being influenced by multiple genetic factors that may vary from strain to strain, and additionally can be influenced by environmental factors. However, the requirement of germ cells for female sex determination is well documented: animals that lack germ cells, or oocytes in particular, develop exclusively as males. Recently, it has been determined that oocytes are also required throughout the adult life of the animal to maintain the differentiated female state. How oocytes control sex differentiation and maintenance of the sexual phenotype is unknown. We therefore generated targeted mutations in genes for two oocyte produced signaling molecules, Bmp15 and Gdf9 and here report a novel role for Bmp15 in maintaining adult female sex differentiation in zebrafish. Females deficient in Bmp15 begin development normally but switch sex during the mid- to late- juvenile stage, and become fertile males. Additionally, by generating mutations in the aromatase cyp19a1a, we show that estrogen production is necessary for female development and that the function of Bmp15 in female sex maintenance is likely linked to the regulation of estrogen biosynthesis via promoting the development of estrogen-producing granulosa cells in the oocyte follicle. |
| doi_str_mv | 10.1371/journal.pgen.1006323 |
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In domesticated zebrafish, sex determination appears to be polygenic, being influenced by multiple genetic factors that may vary from strain to strain, and additionally can be influenced by environmental factors. However, the requirement of germ cells for female sex determination is well documented: animals that lack germ cells, or oocytes in particular, develop exclusively as males. Recently, it has been determined that oocytes are also required throughout the adult life of the animal to maintain the differentiated female state. How oocytes control sex differentiation and maintenance of the sexual phenotype is unknown. We therefore generated targeted mutations in genes for two oocyte produced signaling molecules, Bmp15 and Gdf9 and here report a novel role for Bmp15 in maintaining adult female sex differentiation in zebrafish. Females deficient in Bmp15 begin development normally but switch sex during the mid- to late- juvenile stage, and become fertile males. Additionally, by generating mutations in the aromatase cyp19a1a, we show that estrogen production is necessary for female development and that the function of Bmp15 in female sex maintenance is likely linked to the regulation of estrogen biosynthesis via promoting the development of estrogen-producing granulosa cells in the oocyte follicle.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1006323</identifier><identifier>PMID: 27642754</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adults ; Animal reproduction ; Animals ; Aromatase - genetics ; Aromatase - metabolism ; Biology and Life Sciences ; Bone Morphogenetic Protein 15 - genetics ; Bone Morphogenetic Protein 15 - metabolism ; Cellular biology ; Colleges & universities ; Danio rerio ; Deoxyribonucleic acid ; DNA ; Estrogens - metabolism ; Female ; Funding ; Genetic aspects ; Genotype & phenotype ; Growth Differentiation Factor 9 - genetics ; Growth Differentiation Factor 9 - metabolism ; Male ; Males ; Medicine and Health Sciences ; Molecular biology ; Mutation ; Observations ; Oocytes - metabolism ; Pediatrics ; Phenotype ; Phenotypes ; Research and Analysis Methods ; Sex Determination Processes - genetics ; Sexes ; Signal Transduction ; Zebrafish ; Zebrafish - genetics ; Zebrafish - growth & development ; Zebrafish Proteins - genetics ; Zebrafish Proteins - metabolism</subject><ispartof>PLoS genetics, 2016-09, Vol.12 (9), p.e1006323-e1006323</ispartof><rights>COPYRIGHT 2016 Public Library of Science</rights><rights>2016 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Dranow DB, Hu K, Bird AM, Lawry ST, Adams MT, Sanchez A, et al. (2016) Bmp15 Is an Oocyte-Produced Signal Required for Maintenance of the Adult Female Sexual Phenotype in Zebrafish. PLoS Genet 12(9): e1006323. doi:10.1371/journal.pgen.1006323</rights><rights>2016 Dranow et al 2016 Dranow et al</rights><rights>2016 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Dranow DB, Hu K, Bird AM, Lawry ST, Adams MT, Sanchez A, et al. (2016) Bmp15 Is an Oocyte-Produced Signal Required for Maintenance of the Adult Female Sexual Phenotype in Zebrafish. 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| subjects | Adults Animal reproduction Animals Aromatase - genetics Aromatase - metabolism Biology and Life Sciences Bone Morphogenetic Protein 15 - genetics Bone Morphogenetic Protein 15 - metabolism Cellular biology Colleges & universities Danio rerio Deoxyribonucleic acid DNA Estrogens - metabolism Female Funding Genetic aspects Genotype & phenotype Growth Differentiation Factor 9 - genetics Growth Differentiation Factor 9 - metabolism Male Males Medicine and Health Sciences Molecular biology Mutation Observations Oocytes - metabolism Pediatrics Phenotype Phenotypes Research and Analysis Methods Sex Determination Processes - genetics Sexes Signal Transduction Zebrafish Zebrafish - genetics Zebrafish - growth & development Zebrafish Proteins - genetics Zebrafish Proteins - metabolism |
| title | Bmp15 Is an Oocyte-Produced Signal Required for Maintenance of the Adult Female Sexual Phenotype in Zebrafish |
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