Germ Cell Movements and Sex Differentiation of the Gonads in the Drosophila Embryo

Sonnenblick, B. P.

doi:10.1073/pnas.27.10.484

Cited by 84 publications

(55 citation statements)

References 2 publications

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“…In addition, the movements of PGCs through the developing embryo are well characterized. PGCs form at the posterior pole of the embryo and divide 0-2 times to produce ~30-40 cells (Rabinowitz, 1941;Sonnenblick, 1941;Underwood et al, 1980;Technau and Campos-Ortega, 1986;Hay et al, 1988;Williamson and Lehmann, 1996). Soon after these divisions, wild-type PGCs enter mitotic arrest and remain nonproliferative until the end of embryogenesis (Sonnenblick, 1941;Deshpande et al, 1999).…”

Section: Introductionmentioning

confidence: 99%

Programmed cell death of primordial germ cells inDrosophilais regulated by p53 and the Outsiders monocarboxylate transporter

2008

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Primordial germ cell development uses programmed cell death to remove abnormal, misplaced or excess cells. Precise control of this process is essential to maintain the continuity and integrity of the germline, and to prevent germ cells from colonizing locations other than the gonads. Through careful analyses of primordial germ cell distribution in developing Drosophila melanogaster embryos, we show that normal germ cell development involves extensive programmed cell death during stages 10-12 of embryogenesis. This germ cell death is mediated by Drosophila p53 (p53). Mutations in p53 result in excess primordial germ cells that are ectopic to the gonads. Initial movements of the germ cells appear normal, and wild-type numbers of germ cells populate the gonads, indicating that p53 is required for germ cell death, but not migration. To our knowledge, this is the first report of a loss-of-function phenotype for Drosophila p53 in a non-sensitized background. The p53 phenotype is remarkably similar to that of outsiders (out) mutants. Here, we show that the out gene encodes a putative monocarboxylate transporter. Mutations in p53 and out show nonallelic noncomplementation. Interestingly, overexpression of p53 in primordial germ cells of out mutant embryos partially suppresses the out germ cell death phenotype, suggesting that p53 functions in germ cells either downstream of out or in a closely linked pathway. These findings inform models in which signaling between p53 and cellular metabolism are integrated to regulate programmed cell death decisions.

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Section: Introductionmentioning

confidence: 99%

Programmed cell death of primordial germ cells inDrosophilais regulated by p53 and the Outsiders monocarboxylate transporter

2008

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“…SGPs can be identified by their expression of the 68-77 LacZ line or the nuclear proteins Eyes Absent (Eya) or Zfh-1 (51-53). On adherence of migratory PGCs and the gonadal precursors, they migrate anteriorly to form bilateral groups of cells in ps10, each including on average 12 PGCs and 30 mesodermal cells that coalesce into a round and compact gonad (37,54,55). After coalescence, SGPs intermingle with and individually ensheath PGCs in a process that requires the cell adhesion molecule E-Cadherin (E-Cad) and a novel transmembrane protein Fear-of-Intimacy (56,57).…”

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confidence: 99%

The Development of Germline Stem Cells in Drosophila

Dansereau

Lasko

2008

Methods in Molecular Biology™

100

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SummaryGermline stem cells (GSCs) in Drosophila are a valuable model to explore of how adult stem cells are regulated in vivo. Genetic dissection of this system has shown that stem cell fate is determined and maintained by the stem cell's somatic microenvironment or niche. In Drosophila gonads, the stem cell niche-the cap cell cluster in females and the hub in males-acts as a signaling center to recruit GSCs from among a small population of undifferentiated primordial germ cells (PGCs). Shortrange signals from the niche specify and regulate stem cell fate by maintaining the undifferentiated state of the PGCs next to the niche. Germline cells that do not receive the niche signals because of their location assume the default fate and differentiate. Once GSCs are specified, adherens junctions maintain close association between the stem cells and their niche and help to orient stem cell division so that one daughter is displaced from the niche and differentiates. In females, stem cell fate depends on bone morphogenetic protein (BMP) signals from the cap cells; in males, hub cells express the cytokine-like ligand Unpaired, which activates the Janus kinase-signal transducers and activators of transcription (Jak-Stat) pathway in stem cells. Although the signaling pathways operating between the niche and stem cells are different, there are common general features in both males and females, including the arrangement of cell types, many of the genes used, and the logic of the system that maintains stem cell fate. KeywordsDrosophila; germline stem cell; GSC; PGC; primordial germ cell; stem cell fate; stem cell niche IntroductionStem cells are defined by their capacity to self-renew and to generate daughters that differentiate into one or more terminal cell types. Proper regulation of this property is critical for animal development, growth control, and reproduction. Understanding stem cell function is potentially very important for future developments in gene therapies and regenerative medicine. Research in Drosophila on germline stem cells (GSCs) has been instrumental in defining the important function of the stem cell's somatic microenvironment or niche in the control of its division and self-renewal (1,2). The Drosophila germline is an excellent model of stem cell biology because the system is genetically tractable, the sterility and rudimentary gonads resulting from GSC loss are easily recognized, and the stem cells can be easily identified based on molecular markers and position in the gonad. Germline morphology and development, from embryogenesis to the differentiation of gametes in adult flies, has been well characterized and offers a solid basis for the study of GSC fate determination, maintenance, and differentiation.Drosophila GSCs are derived from embryonic pole cells, the first cell type defined in the embryo. They migrate from the posterior to meet the somatic gonadal precursors (SGPs) and form the embryonic gonad, a simple structure made up of about ten primordial germ cells (PGCs) intermingled with and surr...

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“…In Drosophila melanogaster (fruit fly), the process of PGC migration is completed within 4 h (Sonnenblick, 1941;. During gastrulation, the PGCs are passively carried into the midgut pocket of the developing embryo (Jaglarz and Howard, 1995).…”

Section: Conservation Of Primordial Germ Cell Migrationmentioning

confidence: 99%

“…1; Kunwar et al, 2008). Once outside the midgut, Drosophila PGCs migrate dorsally then anteriorly along the midgut, incorporate into the posterior mesoderm, and bifurcate laterally to join somatic gonadal precursor cells (SGPCs) and form the gonads (Sonnenblick, 1941;Warrior, 1994). This migratory route is defined by the precise expression of Wunens (Wun, Wun2) in the neighboring somatic tissues, such as the midgut, which act as repellant signals to guide PGCs toward the SGPCs and restrict movement into ectopic locations (Zhang et al, 1996(Zhang et al, , 1997.…”

Section: Conservation Of Primordial Germ Cell Migrationmentioning

confidence: 99%

Primordial germ cell migration and the Wnt signaling pathway

Cantu

Laird

2017

Anim Reprod

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A critical step in the development of gametes is the migration of their primordial germ cell (PGC) precursors to the forming gonads. Although the location and mode of PGC specification differs between organisms, the formation of a committed germline before organogenesis creates a need for migration through the growing embryo in order to reach the site of gonadogenesis. Failure of PGC migration can, in many cases, compromise fertility or conversely lead to the formation of teratomas in sites outside of the gonad. Here we review the mechanism of migration employed by PGCs and compare the timing and routes across several model organisms. We summarize recent work on the role of the Wnt signaling pathway in cell migration and the lineage specific function in PGCs, mainly through the ligand Wnt5a and its receptor Ror2.

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Germ Cell Movements and Sex Differentiation of the Gonads in the Drosophila Embryo

Cited by 84 publications

References 2 publications

Programmed cell death of primordial germ cells inDrosophilais regulated by p53 and the Outsiders monocarboxylate transporter

Programmed cell death of primordial germ cells inDrosophilais regulated by p53 and the Outsiders monocarboxylate transporter

The Development of Germline Stem Cells in Drosophila

Primordial germ cell migration and the Wnt signaling pathway

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