Mammalian germ cells are determined after PGC colonization of the nascent gonad

Mammalian primordial germ cells (PGCs) are induced in the embryonic epiblast, before migrating to the nascent gonads. In fish, frogs, and birds, the germline segregates even earlier, through the action of maternally inherited germ plasm. Across vertebrates, migrating PGCs retain a broad developmenta...

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Veröffentlicht in:Proceedings of the National Academy of Sciences - PNAS 2019-12, Vol.116 (51), p.25677-25687
Hauptverfasser: Nicholls, Peter K., Schorle, Hubert, Naqvi, Sahin, Hu, Yueh-Chiang, Fan, Yuting, Carmell, Michelle A., Dobrinski, Ina, Watson, Adrienne L., Carlson, Daniel F., Fahrenkrug, Scott C., Page, David C.
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container_issue 51
container_start_page 25677
container_title Proceedings of the National Academy of Sciences - PNAS
container_volume 116
creator Nicholls, Peter K.
Schorle, Hubert
Naqvi, Sahin
Hu, Yueh-Chiang
Fan, Yuting
Carmell, Michelle A.
Dobrinski, Ina
Watson, Adrienne L.
Carlson, Daniel F.
Fahrenkrug, Scott C.
Page, David C.
description Mammalian primordial germ cells (PGCs) are induced in the embryonic epiblast, before migrating to the nascent gonads. In fish, frogs, and birds, the germline segregates even earlier, through the action of maternally inherited germ plasm. Across vertebrates, migrating PGCs retain a broad developmental potential, regardless of whether they were induced or maternally segregated. In mammals, this potential is indicated by expression of pluripotency factors, and the ability to generate teratomas and pluripotent cell lines. How the germline loses this developmental potential remains unknown. Our genome-wide analyses of embryonic human and mouse germlines reveal a conserved transcriptional program, initiated in PGCs after gonadal colonization, that differentiates germ cells from their germline precursors and from somatic lineages. Through genetic studies in mice and pigs, we demonstrate that one such gonad-induced factor, the RNA-binding protein DAZL, is necessary in vivo to restrict the developmental potential of the germline; DAZL’s absence prolongs expression of a Nanog pluripotency reporter, facilitates derivation of pluripotent cell lines, and causes spontaneous gonadal teratomas. Based on these observations in humans, mice, and pigs, we propose that germ cells are determined after gonadal colonization in mammals. We suggest that germ cell determination was induced late in embryogenesis—after organogenesis has begun—in the common ancestor of all vertebrates, as in modern mammals, where this transition is induced by somatic cells of the gonad. We suggest that failure of this process of germ cell determination likely accounts for the origin of human testis cancer.
doi_str_mv 10.1073/pnas.1910733116
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In fish, frogs, and birds, the germline segregates even earlier, through the action of maternally inherited germ plasm. Across vertebrates, migrating PGCs retain a broad developmental potential, regardless of whether they were induced or maternally segregated. In mammals, this potential is indicated by expression of pluripotency factors, and the ability to generate teratomas and pluripotent cell lines. How the germline loses this developmental potential remains unknown. Our genome-wide analyses of embryonic human and mouse germlines reveal a conserved transcriptional program, initiated in PGCs after gonadal colonization, that differentiates germ cells from their germline precursors and from somatic lineages. Through genetic studies in mice and pigs, we demonstrate that one such gonad-induced factor, the RNA-binding protein DAZL, is necessary in vivo to restrict the developmental potential of the germline; DAZL’s absence prolongs expression of a Nanog pluripotency reporter, facilitates derivation of pluripotent cell lines, and causes spontaneous gonadal teratomas. Based on these observations in humans, mice, and pigs, we propose that germ cells are determined after gonadal colonization in mammals. We suggest that germ cell determination was induced late in embryogenesis—after organogenesis has begun—in the common ancestor of all vertebrates, as in modern mammals, where this transition is induced by somatic cells of the gonad. 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In fish, frogs, and birds, the germline segregates even earlier, through the action of maternally inherited germ plasm. Across vertebrates, migrating PGCs retain a broad developmental potential, regardless of whether they were induced or maternally segregated. In mammals, this potential is indicated by expression of pluripotency factors, and the ability to generate teratomas and pluripotent cell lines. How the germline loses this developmental potential remains unknown. Our genome-wide analyses of embryonic human and mouse germlines reveal a conserved transcriptional program, initiated in PGCs after gonadal colonization, that differentiates germ cells from their germline precursors and from somatic lineages. Through genetic studies in mice and pigs, we demonstrate that one such gonad-induced factor, the RNA-binding protein DAZL, is necessary in vivo to restrict the developmental potential of the germline; DAZL’s absence prolongs expression of a Nanog pluripotency reporter, facilitates derivation of pluripotent cell lines, and causes spontaneous gonadal teratomas. Based on these observations in humans, mice, and pigs, we propose that germ cells are determined after gonadal colonization in mammals. We suggest that germ cell determination was induced late in embryogenesis—after organogenesis has begun—in the common ancestor of all vertebrates, as in modern mammals, where this transition is induced by somatic cells of the gonad. 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subjects Animals
Biological Sciences
Biotechnology
Birds
Cell differentiation
Cell Differentiation - genetics
Colonization
Embryo, Mammalian - cytology
Embryo, Mammalian - physiology
Embryogenesis
Embryonic growth stage
Female
Frogs
Gene Expression Regulation, Developmental - genetics
Genomes
Germ cells
Germ Cells - metabolism
Germ Cells - physiology
Germplasm
Gonads
Gonads - cytology
Gonads - physiology
Male
Mammals
Mice
Organogenesis
Ovarian Neoplasms - genetics
Pluripotency
Pluripotent Stem Cells - metabolism
Pluripotent Stem Cells - physiology
Ribonucleic acid
RNA
RNA-binding protein
RNA-Binding Proteins - genetics
RNA-Binding Proteins - metabolism
Somatic cells
Swine
Teratoma - genetics
Testicular Neoplasms - genetics
Transcription
Vertebrates
title Mammalian germ cells are determined after PGC colonization of the nascent gonad
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