CURRENT STATUS OF GERMLINE STEM CELLS IN ADULT MAMMALIAN OVARY

Year 2019, , 63 - 66, 01.02.2019

Enes Taylan , Yodo Sugishita Kenan Kirteke

https://doi.org/10.23902/trkjnat.483495

Abstract

The evolutionary and biological mechanisms underlying female
reproductive aging have long been a matter of interest. Reproductive biologists
have tackled with the relatively limited fertile period in female lifespan
compared to male fertility that continues until the late ages. For more than
five decades, it has been believed that females are born with a fixed number of
germ cells that constitute ovarian follicle reserve and depletion of this
reserve causes menopause. However, researchers recently reported findings that
support the presence of oogenesis in postnatal mammalian ovaries, which caused
a paradigm shift in our current knowledge of reproductive biology. In this
minireview, we provide a brief history of one of the central dogmas in
reproductive biology and subsequently present recent studies on the existence
of germline stem cells in the mammalian ovary.

Keywords

Ovary, fertility preservation, stem cells, female germline

References

• Abban, G. & Johnson, J. 2009. Stem cell support of oogenesis in the human. Human Reproduction, 24(12): 2974-2978.
• Brinster, R.L. 2007. Male germline stem cells: from mice to men. Science, 316(5823): 404-405.
• Bristol-Gould, S.K., Kreeger, P.K., Selkirk, C.G., Kilen, S.M., Mayo, K.E., Shea, LD. & Woodruff, T.K. 2006. Fate of the initial follicle pool: empirical and mathematical evidence supporting its sufficiency for adult fertility. Developmental Biology, 298(1): 149-154.
• Broekmans, F.J., Soules, MR. & Fauser, B.C. 2009. Ovarian Aging: Mechanisms and Clinical Consequences. Endocrine Reviews, 30(5): 465-493.
• Bukovsky, A., Svetlikova, M. & Caudle, M.R. 2005. Oogenesis in cultures derived from adult human ovaries. Reproductive Biology and Endocrinology, 3: 17.
• David, G.F., Anand-Kumar, T.C. & Baker, T.C. 1974. Uptake of tritiated thymidine by primordial germ cells in the ovaries of adult slender loris. Journal of Reproduction and Fertility, 41: 447-451.
• Eggan, K., Jurga, S., Gosden, R., Min, I.M. & Wagers, A.J. 2006. Ovulated oocytes in adult mice derive from non-circulating germ cells. Nature, 441(7097): 1109-1114.
• Ermolaeva, M., Neri, F., Ori, A. & Rudolph, K.L. 2018. Cellular and epigenetic drivers of stem cell ageing. Nature Reviews Molecular Cellular Biology, 19(9): 594-610.
• Ioannou, J.M. 1967. Oogenesis in adult prosimians. Journal of Embryology and Experimental Morphology, 17: 139-145.
• Johnson, J., Canning, J., Kaneko, T., Pru, J.K. & Tilly J.L. 2004. Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature, 428(6979): 145-150.
• Johnson, J., Bagley, J., Skaznik-Wikiel, M., Lee, H.J., Adams, G.B., Niikura, Y., Tschudy, K.S., Tilly, J.C., Cortes, M.L., Forkert, R., Spitzer, T., Iacomini, J., Scadden, D.T. & Tilly, J.L. 2005. Oocyte generation in adult mammalian ovaries by putative germ cells in bone marrow and peripheral blood. Cell, 122(2): 303-315.
• Kerr, J.B., Brogan, L., Myers, M., Hutt, K.J., Mladenovska, T., Ricardo, S., Hamza, K., Scott, C.L., Strasser, A. & Findlay, J.K. 2012. The primordial follicle reserve is not renewed after chemical or irradiation mediated depletion. Reproduction, 143(4): 469-476.
• Lee, H.J., Selesniemi, K., Niikura, T., Klein, R., Dombkowski, D.M. & Tilly, J.L. 2007. Bone marrow transplantation generates immature oocytes and rescues long-term fertility in a preclinical mouse model of chemotherapy-induced premature ovarian failure. Journal of Clinical Oncology, 25(22): 3198-3204.
• Liu, Y., Wu, C., Lyu, Q., Yang, D., Albertini, D.F., Keefe, D.L. & Liu, L. 2007. Germline stem cells and neo-oogenesis in the adult human ovary. Developmental Biology, 306(1): 112-120.
• Niikura, Y., Niikura, T. & Tilly, J.L. 2009. Aged mouse ovaries possess rare premeiotic germ cells that can generate oocytes following transplantation into a young host environment. Aging, 1(12): 971-978.
• Oktay, K., Taylan, E., Sugishita, Y. & Goldberg, G.M. 2017. Robot-assisted Laparoscopic Transplantation of Frozen-thawed Ovarian Tissue. Journal of Minimally Invasive Gynecology, 24(6): 897-898.
• Pacchiarotti, J., Maki, C., Ramos, T., Marh, J., Howerton, K., Wong, J., Pham, J., Anorve, S., Chow, Y.C. & Izadyar, F. 2010. Differentiation potential of germ line stem cells derived from the postnatal mouse ovary. Differentiation, 79(3): 159-170.
• Parte, S., Bhartiya, D., Telang, J., Daithankar, V., Salvi, V., Zaveri, K. & Hinduja, I. 2011. Detection, characterization, and spontaneous differentiation in vitro of very small embryonic-like putative stem cells in the adult mammalian ovary. Stem Cells and Development, 20(8): 1451-1464.
• Pearl, R. & Schoppe, WE. 1921. Studies on the physiology of reproduction in the domestic fowl. Journal of Experimental Zoology, 34(1): 100-118.
• Selesniemi, K., Lee, H.J., Niikura, T. & Tilly, J.L. 2009. Young adult donor bone marrow infusions into female mice postpone age-related reproductive failure and improve offspring survival. Aging, 1(1): 49-57.
• Taylan, E. & Oktay, K. 2019. Autologous Transplantation of Human Ovarian Tissue, 493-500. In: Peter CK Leung and Eli Y Adashi, The Ovary. 3rd Edition, Elsevier. (https://doi.org/10.1016/B978-0-12-813209-8.00030-3)
• Taylan, E. & Oktay, K.H. 2017. Current state and controversies in fertility preservation with breast cancer. World Journal of Clinical Oncology, 8(3): 241-248.
• Truman, A.M., Tilly, J.L. & Woods, D.C. 2017. Ovarian regeneration: The potential for stem cell contribution in the postnatal ovary to sustain endocrine function. Molecular and Cellular Endocrinology, 445: 74-84.
• Turksen, K. (Editor). 2014. Adult Stem Cells. Second Edition. Springer.
• Waldeyer, W. 1870. Eirstock und Ei. Germany: Engelmann.
• Wang, N., Satirapod, C., Ohguchi, Y., Park, E-S., Woods, D.C. & Tilly, J.L. 2017. Genetic studies in mice directly link oocytes produced during adulthood to ovarian function and natural fertility. Scientific Reports, 7(1): 10011.
• White, Y.A.R., Woods, D.C., Takai, Y., Ishihara, O., Seki, H. & Tilly, J. 2012. Oocyte formation by mitotically active germ cells purified from ovaries of reproductive-age women. Nature Medicine, 18(3): 413-421.
• Zarate-Garcia, L., Lane, S.I.R., Merriman, J.A. & Jones, K.T. 2016. FACS-sorted putative oogonial stem cells from the ovary are neither DDX4-positive nor germ cells. Scientific Reports, 6: 27991.
• Zhang, H., Liu, L., Li, X., Busayavalasa, K., Shen, Y., Hovatta, O., Gustafsson, J.A. & Liu, K. 2014. Life-long in vivo cell-lineage tracing shows no oogenesis originates putative germline stem cells in adult mice. Proceedings of the National Academy of Sciences of the United States, 111(50): 17983-17988.
• Zhang, H., Zheng, W., Shen, Y., Adhikari, D., Ueno, H. & Liu, K. 2012. Experimental evidence showing that no mitotically active female germline progenitors exist in postnatal mouse ovaries. Proceedings of the National Academy of Sciences of the United States, 109(31): 12580-12585.
• Zhou, L., Wang, L., Kang, J.X., Xie, W., Li, X., Wu, C., Xu, B. & Wu, J. 2014. Production of fat-1 transgenic rats using a postnatal female germline stem cell line. Molecular Human Reproduction, 20(3): 271-281.
• Zou, K., Yuan, Z., Yang, Z., Luo, H., Sun, K., Zhou, L., Xiang, J., Shi, L., Yu, Q., Zhang, Y., Hou, R. & Wu, J. 2009. Production of offspring from a germline stem cell line derived from neonatal ovaries. Nature Cell Biology, 11(5): 631-636.