Oogonial stem cells

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Oogonial stem cells (OSCs), also known as egg precursor cells or female germline cells, are diploid germline cells with stem cell characteristics: the ability to renew and differentiate into other cell types, different from their tissue of origin. [1] Present in invertebrates and some lower vertebrate species, they have been extensively studied in Caenorhabditis elegans , Drosophila melanogaster . OSCs allow the production of new female reproductive cells (oocytes) by the process of oogenesis during an organism's reproductive life. [2] [3]

Contents

Invertebrates

Caenorhabditis elegans

Development of oogonial stem cells in C. elegans adult hermaphrodites C. elegans diagram.png
Development of oogonial stem cells in C. elegans adult hermaphrodites

The nematode Caenorhabditis elegans (C. elegans) are nematodes can have hermaphroditic or male reproductive capabilities. In males, only spermatogenesis occurs; hermaphrodites can produce spermatozoa until adulthood, when oogenesis takes over. [4]

All oogonial stem cells in C. elegans are derived from one distal-tip cell (DTC), which acts as a niche to ensure that germline proliferation continues. As the DTC undergoes mitosis, the cells move proximally along the organism and passing from the mitotic-proliferative region into the meiotic cycle. During this cycle, the cells complete meiotic prophase before passing into the zone of oogenesis (or spermatogenesis, depending on the sex and age of the organism). [2] [4] [5]

D. melanogaster

Drosophila ovary DrosophilaOvary.png
Drosophila ovary

Drosophila melanogaster (D. melanogaster), commonly known as the fruit fly, is a dioecious (two-sex) invertebrate. Female D. melanogasters have two ovaries, each of which have 16 ovarioles. The linear development from oogonial stem cells to mature oocyte is similar to that of C. elegans. In D. melanogaster, the 14-stage development of the oocyte is from the anterior to the posterior ovariole. [6] Mature oocytes are then stored in the uterus after passing through the oviduct, to wait for the egg deposition.

Vertebrates

In mammals, oogenesis is believed to be primarily prenatal. The existence of oogonial stem cells in mammals is controversial, [7] except for the finding of OSCs in two species of loris [8] [9] and three species of bat. [10]

In 2004, considerable evidence was provided for the existence of germline stem cells in adult mouse ovaries capable of generating oocytes to form new follicles. [11] [12] [13] Questions exist about cell-sorting techniques used to isolate the OSCs, [14] and some researchers prefer the less-conclusive term "female germline stem cells" to "OSCs". [15] New research indicates that oogonial stem cells do not exist in mice and there is no convincing evidence they exist in other mammals. [16] [17]

Research

A study published in 2015 reported that the formation of new oocytes from newly-discovered germline stem cells, known as oogonial stem cells, has opened new avenues for the treatment of female infertility. [18] [19]

Research by Zuckerman et al. published in 1951, established a central dogma that neo-oogenesis in mammals does not occur postnatally. [20] These conclusions were supported by other researches, such as Peters et al., who investigated DNA synthesis in oocytes during embryonic development. However, since they didn’t study oogenesis postnatally, they could not make any conclusions about postnatal oogenesis. [21] In 1967, Loannou et al., studied proliferation of oogonia and sought to identify whether they were undergoing mitosis. They would be able to show this if there was observance of mitotic activity and whether or not they were contributing to stem cell populations. To do this, they used haematoxylin stains to stain for mitotic divisions. However, these results were inconclusive as they did not have oocyte markers and thus could not say for sure that these cells were a part of the stem cell population. [22] A number of scientists have since then used mathematical models to suggest that, without an oocyte stem cell (OSC) population, the female mammal will not have enough oocytes to complete their reproductive lives due to rate of atresia during the normal cycle is significant. However, in 2004, new research by Jonathan Tilly and colleagues came about to suggest that a new population of stem cells in female mammals does exist, which could possibly be used for personalized therapeutics. Using mouse studies, they were able to detect OSCs that were able to generate new eggs within these mouse ovaries. Tilly et al. used GFP to try to label the OSCs, but they didn’t know exactly where to find these stem cell populations, so it is difficult to say whether somatic cells or stem cells were labeled. This study challenged previously expected notions, as it contradicted the central dogma of oogenesis, and has thus led to a rapid increase in the amount of researching being conducted to suggest whether there does indeed exist oocyte stem cells in the mammalian ovary. [23] Lineage tracing and other studies, following initial observations in Tilly's lab, have found no supporting evidence for oogonial stem cells. [24] [25] [26]


Related Research Articles

Egg cell Female reproductive cell in most anisogamous organisms

The egg cell, or ovum, is the female reproductive cell, or gamete, in most anisogamous organisms. The term is used when the female gamete is not capable of movement (non-motile). If the male gamete (sperm) is capable of movement, the type of sexual reproduction is also classified as oogamous. A nonmotile female gamete formed in the oogonium of some algae, fungi, oomycetes, or bryophytes is an oosphere. When fertilized the oosphere becomes the oospore.

Germ cell Gamete-producing cell

A germ cell is any biological cell that gives rise to the gametes of an organism that reproduces sexually. In many animals, the germ cells originate in the primitive streak and migrate via the gut of an embryo to the developing gonads. There, they undergo meiosis, followed by cellular differentiation into mature gametes, either eggs or sperm. Unlike animals, plants do not have germ cells designated in early development. Instead, germ cells can arise from somatic cells in the adult, such as the floral meristem of flowering plants.

Germline Population of a multicellular organisms cells that pass on their genetic material to the progeny

In biology and genetics, the germline is the population of a multicellular organism's cells that pass on their genetic material to the progeny (offspring). In other words, they are the cells that form the egg, sperm and the fertilised egg. They are usually differentiated to perform this function and segregated in a specific place away from other bodily cells.

An oocyte, oöcyte, or ovocyte is a female gametocyte or germ cell involved in reproduction. In other words, it is an immature ovum, or egg cell. An oocyte is produced in a female fetus in the ovary during female gametogenesis. The female germ cells produce a primordial germ cell (PGC), which then undergoes mitosis, forming oogonia. During oogenesis, the oogonia become primary oocytes. An oocyte is a form of genetic material that can be collected for cryoconservation.

Oogenesis The process of the production of egg cells

Oogenesis, ovogenesis, or oögenesis is the differentiation of the ovum into a cell competent to further develop when fertilized. It is developed from the primary oocyte by maturation. Oogenesis is initiated in the embryonic stage.

Reproductive biology includes both sexual and asexual reproduction.

<span class="mw-page-title-main">Human reproductive system</span> Organs involved in reproduction.

The human reproductive system includes the male reproductive system which functions to produce and deposit sperm; and the female reproductive system which functions to produce egg cells, and to protect and nourish the fetus until birth. Humans have a high level of sexual differentiation. In addition to differences in nearly every reproductive organ, there are numerous differences in typical secondary sex characteristics.

Gametogonium are stem cells for gametes located within the gonads. They originate from primordial germ cells, which have migrated to the gonads. Male gametogonia which are located within the testes during development and adulthood are called spermatogonium. Female gametogonia, known as oogonium, are found within the ovaries of the developing foetus and were thought to be depleted at or after birth. Spermatogonia and oogonia are classified as sexually differentiated germ cells.

An oogonium is a small diploid cell which, upon maturation, forms a primordial follicle in a female fetus or the female gametangium of certain thallophytes.

The cells that give rise to the gametes are often set aside during embryonic cleavage. During development, these cells will differentiate into primordial germ cells, migrate to the location of the gonad, and form the germline of the animal.

Piwi-interacting RNA (piRNA) is the largest class of small non-coding RNA molecules expressed in animal cells. piRNAs form RNA-protein complexes through interactions with piwi-subfamily Argonaute proteins. These piRNA complexes are mostly involved in the epigenetic and post-transcriptional silencing of transposable elements and other spurious or repeat-derived transcripts, but can also be involved in the regulation of other genetic elements in germ line cells.

Piwi

Piwi genes were identified as regulatory proteins responsible for stem cell and germ cell differentiation. Piwi is an abbreviation of P-elementInduced WImpy testis in Drosophila. Piwi proteins are highly conserved RNA-binding proteins and are present in both plants and animals. Piwi proteins belong to the Argonaute/Piwi family and have been classified as nuclear proteins. Studies on Drosophila have also indicated that Piwi proteins have no slicer activity conferred by the presence of the Piwi domain. In addition, Piwi associates with heterochromatin protein 1, an epigenetic modifier, and piRNA-complementary sequences. These are indications of the role Piwi plays in epigenetic regulation. Piwi proteins are also thought to control the biogenesis of piRNA as many Piwi-like proteins contain slicer activity which would allow Piwi proteins to process precursor piRNA into mature piRNA.

Stem-cell niche refers to a microenvironment, within the specific anatomic location where stem cells are found, which interacts with stem cells to regulate cell fate. The word 'niche' can be in reference to the in vivo or in vitro stem-cell microenvironment. During embryonic development, various niche factors act on embryonic stem cells to alter gene expression, and induce their proliferation or differentiation for the development of the fetus. Within the human body, stem-cell niches maintain adult stem cells in a quiescent state, but after tissue injury, the surrounding micro-environment actively signals to stem cells to promote either self-renewal or differentiation to form new tissues. Several factors are important to regulate stem-cell characteristics within the niche: cell–cell interactions between stem cells, as well as interactions between stem cells and neighbouring differentiated cells, interactions between stem cells and adhesion molecules, extracellular matrix components, the oxygen tension, growth factors, cytokines, and the physicochemical nature of the environment including the pH, ionic strength and metabolites, like ATP, are also important. The stem cells and niche may induce each other during development and reciprocally signal to maintain each other during adulthood.

Ovariole

An ovariole is a tubular component of the insect ovary, and the basic unit of egg production. Each ovariole is composed of a germarium at the anterior tip, a set of developing oocytes contained within follicles, and a posterior connection to a common oviduct. While most insects have two ovaries, the number of ovarioles within each ovary varies across insect species. This number may also be variable across individuals within a species, or between the left and right ovaries within an individual.

Vasa is an RNA binding protein with an ATP-dependent RNA helicase that is a member of the DEAD box family of proteins. The vasa gene is essential for germ cell development and was first identified in Drosophila melanogaster, but has since been found to be conserved in a variety of vertebrates and invertebrates including humans. The Vasa protein is found primarily in germ cells in embryos and adults, where it is involved in germ cell determination and function, as well as in multipotent stem cells, where its exact function is unknown.

FIGLA Protein-coding gene in the species Homo sapiens

Folliculogenesis-specific basic helix-loop-helix, also known as factor in the germline alpha (FIGalpha) or transcription factor FIGa, is a protein that in humans is encoded by the FIGLA gene. The FIGLA gene is a germ cell-specific transcription factor preferentially expressed in oocytes that can be found on human chromosome 2p13.3.

Norbert Perrimon is a geneticist and developmental biologist at Harvard Medical School. He is known for developing a number of techniques for use of Drosophila, as well as specific substantive contributions to signal transduction and developmental biology. Perrimon co-developed the GAL4/UAS system method, described as “a fly geneticist's Swiss army knife”, with Andrea Brand to control gene expression. With Tze-bin Chou he developed the FLP-FRT DFS method to analyze the maternal effect of zygotic lethal mutations. With Jianquan Ni, he developed and improved methods for in vivo RNAi. His lab has pioneered high-throughput whole-genome RNAi screening.

Fusome

The fusome is a membranous structure found in the developing germ cell cysts of many insect orders. Initial description of the fusome occurred in the 19th century and since then the fusome has been extensively studied in Drosophila melanogaster male and female germline development. This structure has roles in maintaining germline cysts, coordinating the number of mitotic divisions prior to meiosis, and oocyte determination by serving as a structure for intercellular communication.

The signaled by retinoic acid 8 (Stra8) gene is activated only upon stimulation by retinoic acid and expresses a cytoplasmic protein in the gonads of male and female vertebrates. This protein functions to initiate the transition between mitosis and meiosis, aiding in spermatogenesis and oogenesis. In females, its signaling begins 12.5 days after conception, is localized in the primordial germ cells of female ovaries, and ushers in the first stage of meiosis. Male expression begins postnatally and continues throughout life, matching the need of spermatogenesis compared to the limited window of oogenesis in females. Sperm of mice that had induced null mutations for Stra8 gene were able to undergo mitotic divisions, and while some sperm were able to transition into the early stages of meiosis I, but could not transition into further sub-stages of meiosis I. Errors in chromosome pairing and chromosome condensation were observed following these failures. In female mice, loss of Stra8 signaling shows failure to enter into meiosis. Both males and females are left infertile if Stra8 signaling is absent.

X chromosome reactivation (XCR) is the process by which the inactive X chromosome is re-activated in the cells of eutherian female mammals. Therian female mammalian cells have two X chromosomes, while males have only one, requiring X-chromosome inactivation (XCI) for sex-chromosome dosage compensation. In eutherians, XCI is the random inactivation of one of the X chromosomes, silencing its expression. Much of the scientific knowledge currently known about XCR comes from research limited to mouse models or stem cells.

References

  1. ↑ "stem cell - definition of stem cell in English | Oxford Dictionaries". Oxford Dictionaries | English. Archived from the original on October 2, 2016. Retrieved 2016-09-28.
  2. 1 2 Hubbard, E. Jane Albert (2007-12-01). "The C. elegans germ line: a model for stem cell biology". Developmental Dynamics. 236 (12): 3343–3357. doi:10.1002/dvdy.21335. ISSN   1058-8388. PMC   2949268 . PMID   17948315.
  3. ↑ Felici, Massimo De; Barrios, Florencia (2013-10-01). "Seeking the origin of female germline stem cells in the mammalian ovary". Reproduction. 146 (4): R125–R130. doi: 10.1530/REP-13-0069 . ISSN   1470-1626. PMID   23801781.
  4. 1 2 3 Byrd, Dana T.; Kimble, Judith (2009-12-01). "Scratching the Niche That Controls C. elegans Germline Stem Cells". Seminars in Cell & Developmental Biology. 20 (9): 1107–13. doi:10.1016/j.semcdb.2009.09.005. ISSN   1084-9521. PMC   2820558 . PMID   19765664.
  5. ↑ Cinquin, Olivier; Crittenden, Sarah L.; Morgan, Dyan E.; Kimble, Judith (2010-02-02). "Progression from a stem cell–like state to early differentiation in the C. elegans germ line". Proceedings of the National Academy of Sciences of the United States of America. 107 (5): 2048–2053. Bibcode:2010PNAS..107.2048C. doi: 10.1073/pnas.0912704107 . ISSN   0027-8424. PMC   2836686 . PMID   20080700.
  6. ↑ White, R. A.; Perrimon, N.; Gehring, W. J. (1984-12-01). "Differentiation markers in the Drosophila ovary". Journal of Embryology and Experimental Morphology. 84: 275–286. ISSN   0022-0752. PMID   6442733.
  7. ↑ Grieve, Kelsey M.; McLaughlin, Marie; Dunlop, Cheryl E.; Telfer, Evelyn E.; Anderson, Richard A. (2015). "The controversial existence and functional potential of oogonial stem cells". Maturitas. 82 (3): 278–281. doi: 10.1016/j.maturitas.2015.07.017 . PMID   26278874.
  8. ↑ Duke, K. L. (1967-01-01). "Ovogenetic activity of the fetal-type in the ovary of the adult slow loris, Nycticebus coucang". Folia Primatologica; International Journal of Primatology. 7 (2): 150–154. doi:10.1159/000155114. ISSN   0015-5713. PMID   6069717.
  9. ↑ David, G. F.; Anand Kumar, T. C.; Baker, T. G. (1974-12-01). "Uptake of tritiated thymidine by primordial germinal cells in the ovaries of the adult slender loris". Journal of Reproduction and Fertility. 41 (2): 447–451. doi: 10.1530/jrf.0.0410447 . ISSN   0022-4251. PMID   4476797.
  10. ↑ Antonio-Rubio, Nivia Rocio; Porras-Gómez, Tania Janeth; Moreno-Mendoza, Norma (2013-01-01). "Identification of cortical germ cells in adult ovaries from three phyllostomid bats: Artibeus jamaicensis, Glossophaga soricina and Sturnira lilium". Reproduction, Fertility, and Development. 25 (5): 825–836. doi:10.1071/RD12126. ISSN   1031-3613. PMID   22953782.
  11. ↑ Zou, Kang; Yuan, Zhe; Yang, Zhaojuan; Luo, Huacheng; Sun, Kejing; Zhou, Li; Xiang, Jie; Shi, Lingjun; Yu, Qingsheng (2009-05-01). "Production of offspring from a germline stem cell line derived from neonatal ovaries". Nature Cell Biology. 11 (5): 631–636. doi:10.1038/ncb1869. ISSN   1476-4679. PMID   19363485. S2CID   2172739.
  12. ↑ Zhang, Yong; Yang, Zhaojuan; Yang, Yunze; Wang, Shuzeng; Shi, Lingjun; Xie, Wenhai; Sun, Kejing; Zou, Kang; Wang, Lei (2011-04-01). "Production of transgenic mice by random recombination of targeted genes in female germline stem cells". Journal of Molecular Cell Biology. 3 (2): 132–141. doi:10.1093/jmcb/mjq043. ISSN   1759-4685. PMID   21149239.
  13. ↑ Oatley, Jon; Hunt, Patricia A. (2012-06-01). "Of Mice and (wo)Men: Purified Oogonial Stem Cells from Mouse and Human Ovaries". Biology of Reproduction. 86 (6): 196. doi:10.1095/biolreprod.112.100297. ISSN   0006-3363. PMC   6322432 . PMID   22402962.
  14. ↑ Woods, Dori C.; White, Yvonne A. R.; Tilly, Jonathan L. (2013-01-01). "Purification of Oogonial Stem Cells From Adult Mouse and Human Ovaries: An Assessment of the Literature and a View Toward the Future". Reproductive Sciences. 20 (1): 7–15. doi:10.1177/1933719112462632. ISSN   1933-7191. PMC   3676240 . PMID   23024060.
  15. ↑ Dunlop, Cheryl E.; Telfer, Evelyn E.; Anderson, Richard A. (2014-01-01). "Ovarian germline stem cells". Stem Cell Research & Therapy. 5 (4): 98. doi:10.1186/scrt487. ISSN   1757-6512. PMC   4282152 . PMID   25157949.
  16. ↑ Zhang, H; Panula, S; Petropoulos, S; Edsgärd, D; Busayavalasa, K; Liu, L; Li, X; Risal, S; Shen, Y; Shao, J; Liu, M; Li, S; Zhang, D; Zhang, X; Gerner, RR; Sheikhi, M; Damdimopoulou, P; Sandberg, R; Douagi, I; Gustafsson, JÅ; Liu, L; Lanner, F; Hovatta, O; Liu, K (2015). "Adult human and mouse ovaries lack DDX4-expressing functional oogonial stem cells". Nat Med. 21 (10): 1116–8. doi:10.1038/nm.3775. hdl: 10616/44674 . PMID   26444631. S2CID   2949653.
  17. ↑ Lei, L; Spradling, AC (2013). "Female mice lack adult germ-line stem cells but sustain oogenesis using stable primordial follicles". Proc Natl Acad Sci U S A. 110 (21): 8585–90. Bibcode:2013PNAS..110.8585L. doi: 10.1073/pnas.1306189110 . PMC   3666718 . PMID   23630252.
  18. ↑ Garg, Neha; Sinclair, David A. (2015-07-29). "Oogonial stem cells as a model to study age-associated infertility in women". Reproduction, Fertility and Development. 27 (6): 969–974. doi:10.1071/RD14461. ISSN   1448-5990. PMC   4851909 . PMID   25897831.
  19. ↑ Garg, Neha; Sinclair, David A. (July 2015). "Oogonial stem cells as a model to study age-associated infertility in women". Reproduction, Fertility, and Development. 27 (6): 969–974. doi:10.1071/RD14461. ISSN   1031-3613. PMC   4851909 . PMID   25897831.
  20. ↑ Zuckerman, S (1951). "The number of oocytes in the mature ovary". Recent Progress in Hormone Research. 6: 63–108.
  21. ↑ Peters, H; Levy, E; Crone, M (1962). "Deoxyribonucleic acid synthesis in oocytes of mouse embryos". Nature. 195 (4844): 915–916. Bibcode:1962Natur.195..915P. doi:10.1038/195915a0. PMID   14485731. S2CID   4207567.
  22. ↑ Horan C H & Williams S A 2017 Oocyte stem cells: fact or fantasy? Reproduction Review 1470-1626
  23. ↑ Tilly, J L; Telfer, EE (2009). "Purification of germ line stem cells from adult mammalian ovaries: a step closer towards control of the female biological clock?". Molecular Human Reproduction. 15 (7): 393–398. doi:10.1093/molehr/gap036. PMC   2696346 . PMID   19509111.
  24. ↑ Zhang, H; Panula, S; Petropoulos, S; Edsgärd, D; Busayavalasa, K; Liu, L; Li, X; Risal, S; Shen, Y; Shao, J; Liu, M; Li, S; Zhang, D; Zhang, X; Gerner, RR; Sheikhi, M; Damdimopoulou, P; Sandberg, R; Douagi, I; Gustafsson, JÅ; Liu, L; Lanner, F; Hovatta, O; Liu, K (Oct 2015). "Adult human and mouse ovaries lack DDX4-expressing functional oogonial stem cells". Nat. Med. 21 (10): 1116–8. doi:10.1038/nm.3775. hdl: 10616/44674 . PMID   26444631. S2CID   2949653.
  25. ↑ Lei, L; Spradling, AC (May 2013). "Female mice lack adult germ-line stem cells but sustain oogenesis using stable primordial follicles". Proc Natl Acad Sci U S A. 110 (21): 8585–90. Bibcode:2013PNAS..110.8585L. doi: 10.1073/pnas.1306189110 . PMC   3666718 . PMID   23630252.
  26. ↑ Zarate-Garcia, L; Lane, SI; Merriman, JA; Jones, KT (Jun 2016). "FACS-sorted putative oogonial stem cells from the ovary are neither DDX4-positive nor germ cells". Sci. Rep. 6: 27991. Bibcode:2016NatSR...627991Z. doi:10.1038/srep27991. PMC   4908409 . PMID   27301892.
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