Primordial Germ Cell (chicken) scanning electron micrograph.
Early in development at the time of gastrulation a small group of cells are "put aside" to later form oocytes and spermatozoa, these cells described as the primordial germ cells (PGCs). The cells migrate initially through the primitive streak into the posterior endoderm that forms the hindgut, and from there later into the genital ridge that will be the site of the developing gonad. The maintenance of pluripotency within this cell population may arise through epigenetic modifications that suppress somatic differentiation programs. These cells differentiate at different times in male testis and female ovary development. Recent molecular studies suggest that final determination occurs after PGCs colonize the developing gonad.
In the male, this population of cells when transformed is also thought to give rise to testicular germ cell tumours.
Some Recent Findings
- Review - Primordial Germ Cell Specification in Vertebrate Embryos: Phylogenetic Distribution and Conserved Molecular Features of Preformation and Induction "The differentiation of primordial germ cells (PGCs) occurs during early embryonic development and is critical for the survival and fitness of sexually reproducing species. Here, we review the two main mechanisms of PGC specification, induction, and preformation, in the context of four model vertebrate species: mouse, axolotl, Xenopus frogs, and zebrafish. We additionally discuss some notable molecular characteristics shared across PGC specification pathways, including the shared expression of products from three conserved germline gene families, DAZ (Deleted in Azoospermia) genes, nanos-related genes, and DEAD-box RNA helicases. Then, we summarize the current state of knowledge of the distribution of germ cell determination systems across kingdom Animalia, with particular attention to vertebrate species, but include several categories of invertebrates - ranging from the "proto-vertebrate" cephalochordates to arthropods, cnidarians, and ctenophores. We also briefly highlight ongoing investigations and potential lines of inquiry that aim to understand the evolutionary relationships between these modes of specification."
- 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 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."
- Hox genes limit germ cell formation in the short germ insect Gryllus bimaculatus "Hox genes are conserved transcription factor-encoding genes that specify the identity of body regions in bilaterally symmetrical animals. In the cricket Gryllus bimaculatus, a member of the hemimetabolous insect group Orthoptera, the induction of a subset of mesodermal cells to form the primordial germ cells (PGCs) is restricted to the second through the fourth abdominal segments (A2 to A4). In numerous insect species, the Hox genes Sex-combs reduced (Scr), Antennapedia (Antp), Ultrabithorax (Ubx), and abdominal-A (abd-A) jointly regulate the identities of middle and posterior body segments, suggesting that these genes may restrict PGC formation to specific abdominal segments in G. bimaculatus Here we show that reducing transcript levels of some or all of these Hox genes results in supernumerary and/or ectopic PGCs, either individually or in segment-specific combinations, suggesting that the role of these Hox genes is to limit PGC development with respect to their number, segmental location, or both. These data provide evidence of a role for this ancient group of genes in PGC development."
- On the origin of the human germline "In mice, primordial germ cells (PGCs), the precursors of eggs and sperm, originate from pregastrulation postimplantation embryos. By contrast, the origin of human PGCs (hPGCs) has been less clear and has been difficult to study because of the technical and ethical constraints that limit direct studies on human embryos. In recent years, however, in vitro simulation models using human pluripotent stem cells, together with surrogate non-rodent mammalian embryos, have provided insights and experimental approaches to address this issue. Here, we review these studies, which suggest that the posterior epiblast and/or the nascent amnion in pregastrulation human embryos is a likely source of hPGCs, and that a different gene regulatory network controls PGCs in humans compared with in the mouse. Such studies on the origins and mechanisms of hPGC specification prompt further consideration of the somatic cell fate decisions that occur during early human development."
|These papers originally appeared in the Some Recent Findings table, but as that list grew in length have now been shuffled down to this collapsible table.
See also the Discussion Page for other references listed by year and References on this current page.
- Differentiation of primordial germ cells from premature ovarian insufficiency-derived induced pluripotent stem cells "Premature ovarian insufficiency (POI) is a common disease in reproductive women. The pathogenesis of POI is not clear, although it is known that it involves the disorder of oocyte differentiation and development. The introduction of reprogramming human somatic cells into Induced pluripotent stem cells (iPSCs) offers a unique opportunity to study many aspects of POI from cell differentiation in vitro that could ultimately lead to novel drug development and testing to help treat the disorder....We established some novel, systemic cell models for the studying of the pathogenesis of POI patients. Second, DNA demethylation may accelerate the induction of human PGCs from iPSCs in vitro and the conclusion needs further exploration. This represents an important step in the novel approach for the study of the pathophysiology and potential egg resource for POI patients."
- Primate Primordial Germ Cells Acquire Transplantation Potential by Carnegie stage 23 "Primordial germ cells (PGCs) are the earliest embryonic progenitors in the germline. Correct formation of PGCs is critical to reproductive health as an adult. Recent work has shown that primate PGCs can be differentiated from pluripotent stem cells; however, a bioassay that supports their identity as transplantable germ cells has not been reported. Here, we adopted a xenotransplantation assay by transplanting single-cell suspensions of human and nonhuman primate embryonic Macaca mulatta (rhesus macaque) testes containing PGCs into the seminiferous tubules of adult busulfan-treated nude mice. We discovered that both human and nonhuman primate embryonic testis are xenotransplantable, generating colonies while not generating tumors." Carnegie stage 23 | Stem Cells
- Dynamics of male canine germ cell development "Primordial germ cells (PGCs) are precursors of gametes that can generate new individuals throughout life in both males and females. Additionally, PGCs have been shown to differentiate into embryonic germ cells (EGCs) after in vitro culture. Most studies investigating germinative cells have been performed in rodents and humans but not dogs (Canis lupus familiaris). Here, we elucidated the dynamics of the expression of pluripotent (POU5F1 and NANOG), germline (DDX4, DAZL and DPPA3), and epigenetic (5mC, 5hmC, H3K27me3 and H3K9me2) markers that are important for the development of male canine germ cells during the early (22-30 days post-fertilization (dpf)), middle (35-40 dpf) and late (45-50 dpf) gestational periods. ... The PGCs were positive for POU5F1 and H3K27me3 during all assessed developmental periods, including all periods between the gonadal tissue stage and foetal testes development. The number of NANOG, DDX4, DAZL, DPPA3 and 5mC-positive cells increased along with the developing cords from 35-50 dpf. dog
- MicroRNA dynamics at the onset of primordial germ and somatic cells sex differentiation during mouse embryonic gonad development "In mammals, commitment and specification of germ cell lines implies involves complex programs that include sex differentiation, control of proliferation and meiotic initiation. Regulation of these processes is genetically controlled by fine-tuned mechanisms of gene regulation in which microRNAs (miRNAs) are involved. We have characterized, by small-RNAseq and bioinformatics analyses, the miRNA expression patterns of male and female mouse Primordial Germ Cells (PGCs) and gonadal somatic cells at embryonic stages: E11.5, E12.5 and E13.5. Differential expression analyses revealed differences in the regulation of key miRNA clusters such as miR-199-214, miR-182-183-96 and miR-34c-5p whose targets have defined roles during gonadal sexual determination in both germ and somatic cells." MicroRNA
- Review - Key Signaling Events for Committing Mouse Pluripotent Stem Cells to the Germline Fate "The process of germline development carries genetic information and preparatory totipotency across generations. The last decade has witnessed remarkable successes in the generation of germline cells from mouse pluripotent stem cells, especially induced germline cells with the capacity for producing viable offspring, suggesting clinical applications of induced germline cells in humans. However, to date, the culture systems for germline induction with accurate sex-specific meiosis and epigenetic reprogramming have not been well-established. In this study, we primarily focus on the mouse model to discuss key signaling events for germline induction. We review mechanisms of competent regulators on primordial germ cell induction and discuss current achievements and difficulties in inducing sex-specific germline development. Furthermore, we review the developmental identities of mouse embryonic stem cells and epiblast stem cells under certain defined culture conditions as it relates to the differentiation process of becoming germline cells."
- Sall4 is Essential for Mouse Primordial Germ Cell Specification by Suppressing Somatic Cell Program Genes "The Sall4 zinc finger protein is a critical transcription factor for pluripotency in embryonic stem cells (ESCs). ...Given that Sall4 and Prdm1 are known to associate with the histone deacetylase repressor complex, our findings suggest that Sall4 suppresses the somatic cell program possibly by recruiting the repressor complex in conjunction with Prdm1; therefore, it is essential for PGC specification."
- Loss of Lhx1 activity impacts on the localization of primordial germ cells in the mouse "To dissect the specific role of Lhx1 in germ cell development, we studied embryos with conditional inactivation of Lhx1 activity in epiblast derivatives, which, in contrast to completely null embryos, develop normally through gastrulation before manifesting a head truncation phenotype. Initially, PGCs are localized properly to the definitive endoderm of the posterior gut in the conditional mutant embryos, but they depart from the embryonic gut prematurely. The early exit of PGCs from the gut is accompanied by the failure to maintain a strong expression of Ifitm1 in the mesoderm enveloping the gut, which may mediate the repulsive activity that facilitates the retention of PGCs in the hindgut during early organogenesis. Lhx1 therefore may influence the localization of PGCs by modulating Ifitm1-mediated repulsive activity."
- Dazl functions in maintenance of pluripotency and genetic and epigenetic programs of differentiation in mouse primordial germ cells in vivo and in vitro"We demonstrate that disruption of Dazl results in a post-migratory, pre-meiotic reduction in PGC number accompanied by aberrant expression of pluripotency genes and failure to erase and re-establish genomic imprints in isolated male and female PGCs, as well as subsequent defect in progression through meiosis. Moreover, the phenotypes observed in vivo were mirrored by those in vitro, with inability of isolated mutant PGCs to establish pluripotent EG (embryonic germ) cell lines and few residual Oct-4-expressing cells remaining after somatic differentiation of mESCs carrying a Dazl null mutation. Finally, we observed that even within undifferentiated mESCs, a nascent germ cell subpopulation exists that was effectively eliminated with ablation of Dazl."
- Steel factor controls primordial germ cell survival and motility from the time of their specification in the allantois, and provides a continuous niche throughout their migration "Steel factor is an essential survival and proliferation factor for primordial germ cells (PGCs) during their migration in the early mouse embryo. ...These data, together with previously published data, show that PGCs are Steel factor dependent from their initial specification until they colonize the genital ridges, and suggest the existence of a ;spatio-temporal niche' that travels with this important pluripotential cell population in the embryo."
- Human Embryology (2nd ed.) Larson Chapter 10 p261-306
- The Developing Human: Clinically Oriented Embryology (6th ed.) Moore and Persaud Chapter 13 p303-346
- Before We Are Born (5th ed.) Moore and Persaud Chapter 14 p289-326
- Essentials of Human Embryology, Larson Chapter 10 p173-205
- Human Embryology, Fitzgerald and Fitzgerald Chapter 21-22 p134-152
- Developmental Biology (6th ed.) Gilbert Chapter 14 Intermediate Mesoderm
Mouse and Human Ovarian PGC Timeline Comparison
Electron microscopy has showed apoptosis features in about 50% of mouse cells and a recent study has shown apoptosis molecular markers expressed in human.
Primordial Germ Cell Migration
Primordial Germ Cells (PGCs) are thought to be the first population of cells to migrate through the primitive streak in early gastrulation.
Human Embryonic Disc (Stage 7 week 3, GA week 5)
Week 3 - GA Week 5
- Human embryonic disc showing the primitive streak region where gastrulation occurs, generation the trilaminar embryo.
- Arrows indicate direction of cell migration through the streak.
This population of cells then lie at the hindgut and yolk sac junctional region and later migrate into the germinal ridge in early embryonic development.
Human Embryo (Stage 9 GA week 5) primordial germ cell region (green)
- Sacrococcygeal teratomas - Remnant primitive streak cells (most common solid tumor in newborn infants)
- Germline teratoma - (Germinoma) abnormally differentiated/located PGCs fail to die.
Species Comparison of Migration
Stages of primordial germ cell migration
Mouse Migration Movies
Labeled mouse primordial germ cells (E7.5)
Labeled mouse primordial germ cells (E10.5) See Mouse Migration Movies]]
The movies below show labeled primordial germ cells (green) migrating within the mouse embryo between the periods of E9.0 to E10.5 into the genital ridge region that will later form the gonad.
Mouse Template:ME11.0 to Template:ME12.0
- Female - genital ridge granulosa cells
- Male - Sertoli cells and Leydig cells
- E11.5 - PGCs are bipotential
|Mouse Primordial Germ Cell Migration
- Links: Mouse Development
Fetal Ovary Meiosis
Fetal ovary meiosis
Ectopic PGC's in human adrenal gland in first trimester male week 8 (GA week 10) and female week 11 (GA week 13).
- A B - Germ cells were identified by expression of POU5F1 (red) and/or DDX4 (green)
- C D - DDX4+ (green) germ cells do not express H2AFX (red), however, many H2AFX+ cells were present in the adrenals (white arrows)
- E F - DDX4+ (red) germ cells were not TUNEL-positive (green), however, many TUNEL+ cells were present in the adrenals (white arrows)
male and female adrenal PGC
male adrenal (and adjacent kidney) week 8 (GA week 10)
female adrenal (and adjacent kidney) week 11 (GA week 13)
The images below are scanning electron micrographs of the surface of a chicken primordial germ cell that has been grown in culture.
The first image shows the whole cell and the second image shows detail of the cell surface showing extensions.
|Mouse primordial germ cell DNA methylation
- Global DNA demethylation occurs in primordial germ cells about the time when they colonize the genital ridges.
- Male - prospermatogonia methylation occurs during fetal stages.
- Female - oocytes methylation occurs postnatally.
- Links: Molecular Development - Epigenetics
X-linked Gene Expression
Mouse- X-linked gene expression during primordial germ cell development.
Each circle graph indicates the ratio of cells that are positive (yellow) and negative (black) for each gene, and biallelically (red) and monoallelically (blue) expressed in cells positive for each gene.
- Links: X Inactivation | Mouse Development
File:Model of Dazl germ cell function
- Prdm1 and Prdm14 - PR domain proteins expressed in mouse (E6.25), suppresses somatic differentiation.
- Sall4 - zinc finger protein, inactivation of this transcription factor in mouse can reduce PGC number.
A study has recently identified 11 genes that are specifically expressed in male and female fetal germ cells, both in vivo and in vitro, but are not expressed in embryonic stem cells.
PGC Markers: alkaline phosphatase-positive, Oct4 (POU5F1), Fragilis (IFITM1), Stella (DPPA3), Dazl, and Vasa (DDX4).
- Steel factor - (KITLG) a ligand for the KIT tyrosine kinase receptor.
- dead end - coding an RNA binding protein mainly expressed in the germ cells of vertebrates.
- Blimp1 - B-Lymphocyte induced maturation protein-1 (PRDM1)
- Prmt5 - protein arginine methyltransferase-5
- Nanog - knockdown induces apoptotic cell death in mouse migrating primordial germ cells.
- AID - Activation-Induced cytidine Deaminase enzyme required for demethylation (removal of CpG methylation). Within the genome, DNA methylation is associated with epigenetic mechanisms and occurs at cytosine residues that are followed by guanines.
- OMIM Links: POU5F1 | DAZL | DPPA3 | IFITM1 | DDX4 | KITLG | PRDM1
A recent study in chicken has shown that only two key factors are required to convert stem cells into haploid spermatids:
- retinoic acid (RA)
- stem cell factor (SCF)
Common group of fetal tumors occuring along the body midline, anywhere from the coccyx to the pineal gland, reflecting the developmental PGC migration pathway (for review see).
- Histologically classified as either mature or immature.
- Immature elements consisting principally of primitive neuroglial tissue and neuroepithelial rosettes and have have a generally favorable prognosis.
- Sacrococcygeal teratomas - most common site (70%–80% of all teratomas).
- classified into four types based on the amount of mass present externally versus internally.
Testicular germ cell tumours (seminoma)
- ↑ 1.0 1.1 Choi JW, Kim S, Kim TM, Kim YM, Seo HW, Park TS, Jeong JW, Song G & Han JY. (2010). Basic fibroblast growth factor activates MEK/ERK cell signaling pathway and stimulates the proliferation of chicken primordial germ cells. PLoS ONE , 5, e12968. PMID: 20886037 DOI.
- ↑ Fujimoto T, Miyayama Y & Fuyuta M. (1977). The origin, migration and fine morphology of human primordial germ cells. Anat. Rec. , 188, 315-30. PMID: 900520 DOI.
- ↑ 3.0 3.1 Nicholls PK, Schorle H, Naqvi S, Hu YC, Fan Y, Carmell MA, Dobrinski I, Watson AL, Carlson DF, Fahrenkrug SC & Page DC. (2019). Mammalian germ cells are determined after PGC colonization of the nascent gonad. Proc. Natl. Acad. Sci. U.S.A. , 116, 25677-25687. PMID: 31754036 DOI.
- ↑ Hansen CL & Pelegri F. (2021). Primordial Germ Cell Specification in Vertebrate Embryos: Phylogenetic Distribution and Conserved Molecular Features of Preformation and Induction. Front Cell Dev Biol , 9, 730332. PMID: 34604230 DOI.
- ↑ Barnett AA, Nakamura T & Extavour CG. (2019). Hox genes limit germ cell formation in the short germ insect Gryllus bimaculatus. Proc. Natl. Acad. Sci. U.S.A. , 116, 16430-16435. PMID: 31346080 DOI.
- ↑ Kobayashi T & Surani MA. (2018). On the origin of the human germline. Development , 145, . PMID: 30037844 DOI.
- ↑ Yang S, Ding S, He S, He L, Gao K, Peng S & Shuai C. (2019). Differentiation of primordial germ cells from premature ovarian insufficiency-derived induced pluripotent stem cells. Stem Cell Res Ther , 10, 156. PMID: 31151408 DOI.
- ↑ Gallinat A. (1995). [Ambulatory endoscopic surgery--ovary and leiomyoma]. Arch. Gynecol. Obstet. , 257, 17-21. PMID: 8579394
- ↑ de Souza AF, Pieri NCG, Roballo KCS, Bressan FF, Casals JB, Ambrósio CE, Perecin F & Martins DS. (2018). Dynamics of male canine germ cell development. PLoS ONE , 13, e0193026. PMID: 29489867 DOI.
- ↑ Fernández-Pérez D, Brieño-Enríquez MA, Isoler-Alcaraz J, Larriba E & Del Mazo J. (2018). MicroRNA dynamics at the onset of primordial germ and somatic cell sex differentiation during mouse embryonic gonad development. RNA , 24, 287-303. PMID: 29187591 DOI.
- ↑ Wang JQ & Cao WG. (2016). Key Signaling Events for Committing Mouse Pluripotent Stem Cells to the Germline Fate. Biol. Reprod. , 94, 24. PMID: 26674564 DOI.
- ↑ 12.0 12.1 Yamaguchi YL, Tanaka SS, Kumagai M, Fujimoto Y, Terabayashi T, Matsui Y & Nishinakamura R. (2015). Sall4 is essential for mouse primordial germ cell specification by suppressing somatic cell program genes. Stem Cells , 33, 289-300. PMID: 25263278 DOI.
- ↑ Tanaka SS, Yamaguchi YL, Steiner KA, Nakano T, Nishinakamura R, Kwan KM, Behringer RR & Tam PP. (2010). Loss of Lhx1 activity impacts on the localization of primordial germ cells in the mouse. Dev. Dyn. , 239, 2851-9. PMID: 20845430 DOI.
- ↑ 14.0 14.1 Haston KM, Tung JY & Reijo Pera RA. (2009). Dazl functions in maintenance of pluripotency and genetic and epigenetic programs of differentiation in mouse primordial germ cells in vivo and in vitro. PLoS ONE , 4, e5654. PMID: 19468308 DOI.
- ↑ Gu Y, Runyan C, Shoemaker A, Surani A & Wylie C. (2009). Steel factor controls primordial germ cell survival and motility from the time of their specification in the allantois, and provides a continuous niche throughout their migration. Development , 136, 1295-303. PMID: 19279135 DOI.
- ↑ Sun YC, Sun XF, Dyce PW, Shen W & Chen H. (2017). The role of germ cell loss during primordial follicle assembly: a review of current advances. Int. J. Biol. Sci. , 13, 449-457. PMID: 28529453 DOI.
- ↑ Wang RA, Nakane PK & Koji T. (1998). Autonomous cell death of mouse male germ cells during fetal and postnatal period. Biol. Reprod. , 58, 1250-6. PMID: 9603260 DOI.
- ↑ Sakashita A, Kawabata Y, Jincho Y, Tajima S, Kumamoto S, Kobayashi H, Matsui Y & Kono T. (2015). Sex Specification and Heterogeneity of Primordial Germ Cells in Mice. PLoS ONE , 10, e0144836. PMID: 26700643 DOI.
- ↑ Richardson BE & Lehmann R. (2010). Mechanisms guiding primordial germ cell migration: strategies from different organisms. Nat. Rev. Mol. Cell Biol. , 11, 37-49. PMID: 20027186 DOI.
- ↑ Cao L, Shitara H, Sugimoto M, Hayashi J, Abe K & Yonekawa H. (2009). New evidence confirms that the mitochondrial bottleneck is generated without reduction of mitochondrial DNA content in early primordial germ cells of mice. PLoS Genet. , 5, e1000756. PMID: 19997484 DOI.
- ↑ 21.0 21.1 Heeren AM, He N, de Souza AF, Goercharn-Ramlal A, van Iperen L, Roost MS, Gomes Fernandes MM, van der Westerlaken LA & Chuva de Sousa Lopes SM. (2016). On the development of extragonadal and gonadal human germ cells. Biol Open , 5, 185-94. PMID: 26834021 DOI.
- ↑ Abe M, Tsai SY, Jin SG, Pfeifer GP & Szabó PE. (2011). Sex-specific dynamics of global chromatin changes in fetal mouse germ cells. PLoS ONE , 6, e23848. PMID: 21886830 DOI.
- ↑ Sugimoto M & Abe K. (2007). X chromosome reactivation initiates in nascent primordial germ cells in mice. PLoS Genet. , 3, e116. PMID: 17676999 DOI.
- ↑ Sabour D, Araúzo-Bravo MJ, Hübner K, Ko K, Greber B, Gentile L, Stehling M & Schöler HR. (2011). Identification of genes specific to mouse primordial germ cells through dynamic global gene expression. Hum. Mol. Genet. , 20, 115-25. PMID: 20940145 DOI.
- ↑ Lange UC, Saitou M, Western PS, Barton SC & Surani MA. (2003). The fragilis interferon-inducible gene family of transmembrane proteins is associated with germ cell specification in mice. BMC Dev. Biol. , 3, 1. PMID: 12659663
- ↑ Yamaguchi S, Kurimoto K, Yabuta Y, Sasaki H, Nakatsuji N, Saitou M & Tada T. (2009). Conditional knockdown of Nanog induces apoptotic cell death in mouse migrating primordial germ cells. Development , 136, 4011-20. PMID: 19906868 DOI.
- ↑ Sanz LA, Kota SK & Feil R. (2010). Genome-wide DNA demethylation in mammals. Genome Biol. , 11, 110. PMID: 20236475 DOI.
- ↑ Ji M, Tang S, Pei W, Ning M, Ma Y, Li X & Guan W. (2018). Generation of haploid spermatids from chicken embryonal primordial germ cells. Int. J. Mol. Med. , , . PMID: 29620249 DOI.
- ↑ Woodward PJ, Sohaey R, Kennedy A & Koeller KK. (2005). From the archives of the AFIP: a comprehensive review of fetal tumors with pathologic correlation. Radiographics , 25, 215-42. PMID: 15653597 DOI.
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