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Ichikawa, K.; Horiuchi, H. Primordial Germ Cells. Encyclopedia. Available online: https://encyclopedia.pub/entry/42219 (accessed on 07 October 2024).
Ichikawa K, Horiuchi H. Primordial Germ Cells. Encyclopedia. Available at: https://encyclopedia.pub/entry/42219. Accessed October 07, 2024.
Ichikawa, Kennosuke, Hiroyuki Horiuchi. "Primordial Germ Cells" Encyclopedia, https://encyclopedia.pub/entry/42219 (accessed October 07, 2024).
Ichikawa, K., & Horiuchi, H. (2023, March 15). Primordial Germ Cells. In Encyclopedia. https://encyclopedia.pub/entry/42219
Ichikawa, Kennosuke and Hiroyuki Horiuchi. "Primordial Germ Cells." Encyclopedia. Web. 15 March, 2023.
Primordial Germ Cells
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This entry is adapted from the peer-reviewed paper 10.3390/genes14030612

Primordial germ cells (PGCs) are precursor cells of sperm and eggs. The fate decisions of chicken PGCs in terms of their development, integrity, and sex determination have unique features, thereby providing insights into evolutionary developmental biology.

avian species chicken primordial germ cells

1. Introduction

The chicken (Gallus gallus) is a valuable species in terms of protein resources. Additionally, chickens have been used as a model organism for amniotes to elucidate embryonic developmental mechanisms [1]. Furthermore, chickens have been used as avian models in various areas of biology, thereby contributing to the understanding of vertebrate evolution. Thus, research using chickens greatly enhances both industrial development and developmental and evolutionary biology.
Primordial germ cells (PGCs) are the precursor cells of sperm and eggs. PGCs are the only cell lineage that can transmit genetic information to the next generation. Thus, elucidating the fate decision of PGCs, namely the mechanisms by which they develop, maintain integrity, differentiate into gametes of optimal sexes, and control their self-renewal, is a valuable research subject. Avian PGCs have characteristic developmental features, such as migration into the gonads using the vascular system [2]. Chicken PGCs have also shown a unique sex determination mechanism in which PGC-intrinsic factors may occur in a cell-autonomous manner [3][4][5]. In addition, several studies have revealed the self-renewal mechanism of chicken PGCs, resulting in the establishment of stable culture protocols for chicken PGCs [6][7]. Currently, culturing PGCs is a fundamental technique to establish genome-edited chickens and conserve avian genetic resources so that objective offspring can be produced via germline chimeras transplanted from cultured PGCs and directly incubated [8][9] or incubated with an ex ovo culture system [10]. Therefore, studies on the fate decisions of avian PGCs have demonstrated their unique features and have aided the development of avian biotechnologies.
With the development of essential technologies such as genome editing and RNA sequencing (RNA-seq) analysis, studies on chicken PGCs have shown rapid advancement over the last ten years. For example, the clustered regularly interspaced short palindromic repeats/CRISPR-associated protein (CRISPR/Cas) system [11] has been used not only to produce genome-edited chickens [12], but also to conduct functional analysis of PGC-intrinsic factors via application of this system to cultured PGCs [13]. Alternatively, RNA-seq technology enables us to predict the fate decision of chicken PGCs even at a single-cell resolution level [14][15].

2. Early Development of Chicken PGCs

2.1. Origin and Identification of Chicken PGCs

In vertebrates, PGC formation is generally classified into two models: preformation and epigenesis [16]. The preformation model has been observed in zebrafish (Danio rerio) [17] and anuran amphibians (Xenopus laevis) [18]. In this model, germplasm, a maternal factor, acts as a determinant of germ cell formation. The germplasm is composed of maternally inherited RNAs and proteins and is partially asymmetrically partitioned to cells during cleavage divisions and development. As a result, PGCs arise from the partitioned cells. This mechanism is conserved in several non-vertebrate species, including Drosophila melanogaster [19] and Caenorhabditis elegans [20]. In contrast, the epigenesis model has been shown in urodele amphibians (Ambystoma mexicanum) [21] and mammals (Mus musculus) [22]. In these species, PGCs are induced in somatic cells via “epigenetic” regulation during embryonic development; thus, the germplasm is absent.
Several studies have been conducted to determine the origins of avian PGCs. In particular, studies focusing on the vasa gene have strongly supported the preformation model for avian PGC formation. VASA is a germ-cell-specific RNA helicase that is localized in germ cells as a germplasm component across various species, such as X. laevis and D. melanogaster. Tsunekawa et al. demonstrated the expression patterns of the chicken vasa homolog (CVH) [23]. The CVH is localized in cleavage furrows and asymmetrically distributed to limited cells. Additionally, the CVH is colocalized with the mitochondrial cloud, corresponding to the germplasm feature in D. melanogaster. Recent functional analyses have shown that the CVH significantly contributes to germ cell development in both males and females [24][25]. These studies suggest that chickens possess germplasm-like features and follow the preformation model for PGC formation.
Previous studies targeting deletion in the azoospermia-like (DAZL) protein also support the preformation model in chickens. DAZL is a germ-cell-specific RNA-binding protein localized in the germplasm in some vertebrates [26][27]. In chickens, DAZL is also localized in cleavage furrows as well as the CVH and is specifically expressed in germ cells [28]. Additionally, knockdown of DAZL in chicken PGCs causes apoptosis and aberrant expression patterns of germ-cell-characteristic genes, albeit under culture conditions [28]. Recently, whole transcriptome analysis predicted that chicken DAZL was co-expressed with its potential interacting genes according to zygotic genome activation, suggesting its central role in germ-cell specification [29].
Therefore, nowadays, avian germ cells are thought to be specified by the preformation model; however, the possibility that avian PGCs are formed via epigenetic regulation cannot be excluded [30]. Thus, while several studies have supported the preformation model in avian PGC formation, the origin of PGCs remains unknown.

2.2. Migration of Chicken PGCs into Embryonic Gonads

A chick embryo in an egg incubates for 0 h, corresponding to Eyal-Giladi and Kochav (EG & K) stage X, and consists of approximately 60,000 cells [31]. At this embryonic stage, approximately 30 CVH-positive cells, namely the origin of PGCs, are scattered at the center of the area pellucida in the blastoderm (Figure 1) [23]. The CVH-positive cells then start to migrate into the germinal crescent, an anterior extraembryonic region. At Hamburger–Hamilton (HH) stage 4 (chick embryos in eggs after 18–19 h of incubation), PGCs accumulated at a high density in the germinal crescent (Figure 1) [32]. Previously, it was thought that PGCs passively translocate into the germinal crescent via the morphogenetic movement of hypoblasts [33]. However, Kang et al. demonstrated that chick fibroblasts exogenously transplanted into the subgerminal cavity of the recipient could not settle in the germinal crescent, whereas transplanted PGCs could [34]. This indicates that PGC-intrinsic factors are also related to this migration. Recently, Huss et al. revealed that quail (Coturnix japonica) PGCs contribute to the extracellular matrix in the germinal crescent [35]. Although the molecular mechanism of PGC migration remains unclear, these previous studies showed their “active” role.
Genes 14 00612 g001 550
Figure 1. A schematic illustration of chicken primordial germ cell (PGC) development.
After the settlement of PGCs into the germinal crescent, PGCs begin to migrate to the gonads. In many vertebrates, such as mice and zebrafish, PGCs migrate into gonads via “amoeboid migration” [36]. However, in birds (and reptiles), PGCs use the vascular system to migrate into the gonads. Several studies have attempted to elucidate this unique migration system in avian PGCs.
Around HH stage 6 (chick embryos in eggs incubated for 23–25 h), aggregations of endothelial cell progenitors and blood cell progenitors, called blood islands, appear in the extraembryonic mesoderm [37]. Murai et al. demonstrated that more than 60% of quail PGCs in an embryo were enveloped by differentiating endothelial cells forming blood islands in the germinal crescent [38]. Then, the PGCs flowed along with the heartbeat at HH stage 12 (after 48–49 h of incubation). This indicates that most avian PGCs were passively translocated into the vascular system.
Once avian PGCs are translocated into the blood vessels, they start circulating. The concentration of chicken PGCs in the bloodstream reaches a peak at HH stage 14 (after 50–53 h of incubation), and these settle in gonads from HH stage 15 (after 50–55 h of incubation) to HH stage 17 (after 52–64 h of incubation) (Figure 1) [39][40]. Recent studies have demonstrated the molecular mechanisms involved in gonadal migration of avian PGCs. The role of the interaction between chemotactic molecular stromal cell-derived factor 1 (SDF1) and its receptor C-X-C chemokine receptor type 4 (CXCR4) is a well-known system that directs PGCs to the gonads in vertebrates, whose PGCs utilize amoeboid migration [41][42][43][44][45]. In chickens, the expression of CXCR4 has also been observed in PGCs [46], and PGCs are attracted to ectopically expressed SDF1s [47]. Furthermore, the transplantation of CXCR4 knockout (KO) PGCs into recipient embryos resulted in a reduction in their capacity to migrate into gonads, suggesting a critical role of the CXCR4–SDF1 interaction in this migration [13]. In contrast, recent studies have proposed other factors for gonadal migration of avian PGCs. Saito et al. showed that circulating avian PGCs were stiffer than blood cells; thus, PGCs were efficiently occluded at the vascular plexus near presumptive gonads, resulting in their homing to developing gonads [48]. Huang et al. proposed that platelet-derived growth factor signaling could be involved in the migration of avian PGCs into gonads using RNA-seq analysis [49]. These molecular studies have advanced the understanding of how avian PGCs migrate to gonads. Notably, previous research focusing on the migration of avian PGCs has been conducted mainly using chickens and quails. Thus, whether the molecular mechanism of this migration is conserved across avian species remains unknown.

3. Integrity of Chicken PGCs

3.1. Epigenetic Regulation

Epigenetic regulation is essential for PGCs to maintain their properties for germinal transmission, namely, establishing their integrity. In mice, PGCs undergo genome-wide epigenetic reprogramming between embryonic day (E) 8.5 and E13.5, and these embryonic stages correspond to the migration and colonization of PGCs to the gonads [50]. Epigenetic reprogramming is required to establish germ cell specification and erase somatic epigenetic memory [51]. The importance of epigenetic modifications in the establishment of PGC integrity has also been observed across species [52].
Several studies have been conducted to reveal epigenetic modifications of chicken PGCs. Yu et al. demonstrated that chicken PGCs undergo global DNA demethylation via ten-eleven translocation 1 during HH stage 21 (after 3.5 d of incubation) to HH stage 28 (after 5.5 d of incubation) [53]. These embryonic stages correspond to states in which chicken PGCs migrate to the gonads and form colonies within the gonads. Rengaraj et al. investigated the expression patterns of the DNA methyltransferase (DNMT) families DNMT1, DNMT 3 α (DNMT3A), and DNMT 3 β (DNMT3B) in chicken PGCs during embryogenesis and suggested that DNMT3B-dependent de novo DNA methylation occurred after PGCs settled into the gonads [54]. Jang et al. showed the characteristic DNA methylation patterns of gonadal PGCs by comparing them with those of chicken embryonic fibroblasts [55]. Although the understanding of DNA methylation in PGCs is not yet complete, these analyses are beginning to elucidate the underlying mechanism.
Furthermore, several studies have been reported concerning the elucidation of histone modification in avian PGCs. In mice, after the transient loss of histone modifications during epigenetic reprogramming, PGCs regain both histone H3 lysine 9 (H3K9) and H3K27 trimethylation (me3) around E12.5 [56]. However, histone modification of chicken PGCs was based on H3K9me3 rather than H3K27me3, suggesting the existence of avian-specific epigenetic regulation in PGCs [57]. For other modifications, H3K4me2 activates signaling pathways essential for avian PGC formation, such as bone morphogenetic protein 4 (BMP4) signaling [58]. Additionally, H3K9 acetylation (H3K9ac) contributes to maintaining the integrity of avian PGCs via the regulation of NANOG, a key transcription factor for germ cell development [59] (described below). These analyses have revealed histone modifications in avian PGCs, including avian-specific H3K9me3-dominant gene expression regulation.

3.2. Key Molecules for the Integrity of Avian PGC

Key molecules for the integrity of PGCs, including transcription factors, are well-conserved in vertebrates. Recently, several researchers conducted functional analyses of these molecules in avian PGCs. Interestingly, these key molecules exhibited bird-like features. Researchers describe the functions and characteristics of the molecules involved in the integrity of chicken PGCs, along with their differences from those in other model organisms.

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Subjects: Reproductive Biology
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Kennosuke Ichikawa
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