Ovarian germline stem cells: An unlimited source of oocytes?

Fertility and Sterility

Volumn 101, Issue 1, 2014, Pages 20-30

  Hanna, Carol B ^a   Hennebold, Jon D ^a,b  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

fertility; oocytes; Ovarian germline stem cells

Indexed keywords

ARTICLE; CELL GROWTH; CELL ISOLATION; CELL RENEWAL; EMBRYONIC STEM CELL; GERMLINE STEM CELL; HUMAN; INFERTILITY; INVERTEBRATE; NONHUMAN; OOCYTE; OOCYTE DEVELOPMENT; OVARY CELL CULTURE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; VERTEBRATE;

EID: 84891502860     PISSN: 00150282     EISSN: 15565653     Source Type: Journal    
DOI: 10.1016/j.fertnstert.2013.11.009     Document Type: Review

References (82)

1. N.S. Macklon, R.L. Stouffer, L.C. Giudice, and B.C. Fauser The science behind 25 years of ovarian stimulation for in vitro fertilization Endocr Rev 27 2006 170 207
2. A. Spradling, M.T. Fuller, R.E. Braun, and S. Yoshida Germline stem cells Cold Spring Harb Perspect Biol 3 2011 a002642
3. Z.A. Wang, and D. Kalderon Cyclin E-dependent protein kinase activity regulates niche retention of Drosophila ovarian follicle stem cells Proc Natl Acad Sci U S A 106 2009 21701 21706
4. M. de Cuevas, and A.C. Spradling Morphogenesis of the Drosophila fusome and its implications for oocyte specification Development 125 1998 2781 2789 (Pubitemid 28410203)
5. T. Xie, and A.C. Spradling A niche maintaining germ line stem cells in the Drosophila ovary Science 290 2000 328 330
6. X. Song, C.H. Zhu, C. Doan, and T. Xie Germline stem cells anchored by adherens junctions in the Drosophila ovary niches Science 296 2002 1855 1857 (Pubitemid 34596269)
7. A. Gonzalez-Reyes Stem cells, niches and cadherins: a view from Drosophila J Cell Sci 116 2003 949 954 (Pubitemid 36395606)
8. L. Lopez-Onieva, A. Fernandez-Minan, and A. Gonzalez-Reyes Jak/Stat signalling in niche support cells regulates dpp transcription to control germline stem cell maintenance in the Drosophila ovary Development 135 2008 533 540
9. R.E. Harris, and H.L. Ashe Cease and desist: modulating short-range Dpp signalling in the stem-cell niche EMBO Rep 12 2011 519 526
10. X. Wang, R.E. Harris, L.J. Bayston, and H.L. Ashe Type IV collagens regulate Bmp signalling in Drosophila Nature 455 2008 72 77
11. Z. Guo, and Z. Wang The glypican Dally is required in the niche for the maintenance of germline stem cells and short-range Bmp signaling in the Drosophila ovary Development 136 2009 3627 3635
12. D. Chen, and D. McKearin Dpp signaling silences Bam transcription directly to establish asymmetric divisions of germline stem cells Curr Biol 13 2003 1786 1791 (Pubitemid 37269118)
13. Z. Wang, and H. Lin Nanos maintains germline stem cell self-renewal by preventing differentiation Science 303 2004 2016 2019 (Pubitemid 38393276)
14. Y. Li, Q. Zhang, A. Carreira-Rosario, J.Z. Maines, D.M. McKearin, and M. Buszczak Mei-p26 cooperates with Bam, Bgcn and Sxl to promote early germline development in the Drosophila ovary PloS One 8 2013 e58301
15. E.J. Hubbard, and D. Greenstein The Caenorhabditis elegans gonad: a test tube for cell and developmental biology Dev Dyn 218 2000 2 22 (Pubitemid 30249747)
16. A. Kershner, S.L. Crittenden, K. Friend, E.B. Sorensen, D.F. Porter, and J. Kimble Germline stem cells and their regulation in the nematode Caenorhabditis elegans Adv Exp Med Biol 786 2013 29 46
17. O. Cinquin, S.L. Crittenden, D.E. Morgan, and J. Kimble Progression from a stem cell-like state to early differentiation in the C. elegans germ line Proc Natl Acad Sci U S A 107 2010 2048 2053
18. D. Greenstein Control of oocyte meiotic maturation and fertilization WormBook 2005 1 12
19. J. McCarter, B. Bartlett, T. Dang, and T. Schedl Soma-germ cell interactions in Caenorhabditis elegans: multiple events of hermaphrodite germline development require the somatic sheath and spermathecal lineages Dev Biol 181 1997 121 143 (Pubitemid 27089067)
20. J.R. von Stetina, and T.L. Orr-Weaver Developmental control of oocyte maturation and egg activation in metazoan models Cold Spring Harb Perspect Biol 3 2011 a005553
21. J. McCarter, B. Bartlett, T. Dang, and T. Schedl On the control of oocyte meiotic maturation and ovulation in Caenorhabditis elegans Dev Biol 205 1999 111 128 (Pubitemid 29042662)
22. S.T. Henderson, D. Gao, E.J. Lambie, and J. Kimble Lag-2 may encode a signaling ligand for the Glp-1 and Lin-12 receptors of C. elegans Development 120 1994 2913 2924 (Pubitemid 24312059)
23. D. Gao, and J. Kimble Apx-1 can substitute for its homolog Lag-2 to direct cell interactions throughout Caenorhabditis elegans development Proc Natl Acad Sci U S A 92 1995 9839 9842
24. J. Austin, and J. Kimble Glp-1 is required in the germ line for regulation of the decision between mitosis and meiosis in C. elegans Cell 51 1987 589 599
25. L.W. Berry, B. Westlund, and T. Schedl Germ-line tumor formation caused by activation of Glp-1, a Caenorhabditis elegans member of the Notch family of receptors Development 124 1997 925 936 (Pubitemid 27107440)
26. L.B. Lamont, S.L. Crittenden, D. Bernstein, M. Wickens, and J. Kimble Fbf-1 and Fbf-2 regulate the size of the mitotic region in the C. elegans germline Dev Cell 7 2004 697 707 (Pubitemid 39462690)
27. S.L. Crittenden, C.R. Eckmann, L. Wang, D.S. Bernstein, M. Wickens, and J. Kimble Regulation of the mitosis/meiosis decision in the Caenorhabditis elegans germline Philos Trans R Soc Lond, B, Biol Sci 358 2003 1359 1362 (Pubitemid 37053984)
28. S.L. Crittenden, D.S. Bernstein, J.L. Bachorik, B.E. Thompson, M. Gallegos, and A.G. Petcherski et al. A conserved RNA-binding protein controls germline stem cells in Caenorhabditis elegans Nature 417 2002 660 663 (Pubitemid 34614826)
29. M.H. Lee, B. Hook, L.B. Lamont, M. Wickens, and J. Kimble Lip-1 phosphatase controls the extent of germline proliferation in Caenorhabditis elegans EMBO J 25 2006 88 96 (Pubitemid 43077298)
30. J. Jeong, J.M. Verheyden, and J. Kimble Cyclin E and Cdk2 control Gld-1, the mitosis/meiosis decision, and germline stem cells in Caenorhabditis elegans PLoS Genet 7 2011 e1001348
31. B. Biedermann, J. Wright, M. Senften, I. Kalchhauser, G. Sarathy, and M.H. Lee et al. Translational repression of cyclin E prevents precocious mitosis and embryonic gene activation during C. elegans meiosis Dev Cell 17 2009 355 364
32. K.W. Kim, K. Nykamp, N. Suh, J.L. Bachorik, L. Wang, and J. Kimble Antagonism between Gld-2 binding partners controls gamete sex Dev Cell 16 2009 723 733
33. K.W. Kim, T.L. Wilson, and J. Kimble Gld-2/Rnp-8 cytoplasmic poly(A) polymerase is a broad-spectrum regulator of the oogenesis program Proc Natl Acad Sci U S A 107 2010 17445 17450
34. D. Hansen, L. Wilson-Berry, T. Dang, and T. Schedl Control of the proliferation versus meiotic development decision in the C. elegans germline through regulation of Gld-1 protein accumulation Development 131 2004 93 104 (Pubitemid 38111418)
35. S. Nakamura, K. Kobayashi, T. Nishimura, and M. Tanaka Ovarian germline stem cells in the teleost fish, medaka (Oryzias latipes) J Biol Sci 7 2011 403 409
36. I. Quagio-Grassiotto, H. Grier, T.S. Mazzoni, R.H. Nobrega, and J.P. de Arruda Amorim Activity of the ovarian germinal epithelium in the freshwater catfish, Pimelodus maculatus (Teleostei: Ostariophysi: Siluriformes): germline cysts, follicle formation and oocyte development J Morphol 272 2011 1290 1306
37. S. Nakamura, K. Kobayashi, T. Nishimura, S. Higashijima, and M. Tanaka Identification of germline stem cells in the ovary of the teleost medaka Science 328 2010 1561 1563
38. B.W. Draper, C.M. McCallum, and C.B. Moens Nanos1 is required to maintain oocyte production in adult zebrafish Dev Biol 305 2007 589 598 (Pubitemid 46705412)
39. T.T. Wong, T. Saito, J. Crodian, and P. Collodi Zebrafish germline chimeras produced by transplantation of ovarian germ cells into sterile host larvae Biol Reprod 84 2011 1190 1197
40. R. Pearl, and W.F. Schoppe Studies on the physiology of reproduction in the domestic fowl. XVIII. Further observations on the anatomical basis of fecundity J Exp Zool 34 1921 100 118
41. E. Allen Ovogenesis during sexual maturity Am J Anat 31 1923 439 481
42. S. Zuckerman The number of oocytes in the mouse ovary Recent Prog Horm Res 6 1951 63 108
43. J. Johnson, J. Canning, T. Kaneko, J.K. Pru, and J.L. Tilly Germline stem cells and follicular renewal in the postnatal mammalian ovary Nature 428 2004 145 150 (Pubitemid 38374304)
44. J.B. Kerr, R. Duckett, M. Myers, K.L. Britt, T. Mladenovska, and J.K. Findlay Quantification of healthy follicles in the neonatal and adult mouse ovary: evidence for maintenance of primordial follicle supply Reproduction 132 2006 95 109 (Pubitemid 44123387)
45. B. Pansky, and H.W. Mossman The regenerative capacity of the rabbit ovary Anat Rec 116 1953 19 51
46. G.J. Vermande-van Eck Neo-ovogenesis in the adult monkey; consequences of atresia of ovocytes Anat Rec 125 1956 207 224
47. K.L. Duke Ovogenetic activity of the fetal-type in the ovary of the adult slow loris, Nycticebus coucang Folia Primatol (Basel) 7 1967 150 154
48. G.F. David, T.C. Anand Kumar, and T.G. Baker Uptake of tritiated thymidine by primordial germinal cells in the ovaries of the adult slender loris J Reprod Fertil 41 1974 447 451
49. J. Johnson, M. Skaznik-Wikiel, H.J. Lee, Y. Niikura, J.C. Tilly, and J.L. Tilly Setting the record straight on data supporting postnatal oogenesis in female mammals Cell Cycle 4 2005 1469 1475 (Pubitemid 41609122)
50. R.G. Gosden Germline stem cells in the postnatal ovary: is the ovary more like a testis? Humanit Rep Update 10 2004 193 195 (Pubitemid 38744865)
51. C. Greenfeld, and J.A. Flaws Renewed debate over postnatal oogenesis in the mammalian ovary Bioessays 26 2004 829 832 (Pubitemid 39128097)
52. A.G. Byskov, M.J. Faddy, J.G. Lemmen, and C.Y. Andersen Eggs forever? Differentiation 73 2005 438 446
53. S.K. Bristol-Gould, P.K. Kreeger, C.G. Selkirk, S.M. Kilen, K.E. Mayo, and L.D. Shea et al. Fate of the initial follicle pool: empirical and mathematical evidence supporting its sufficiency for adult fertility Dev Biol 298 2006 149 154 (Pubitemid 44414800)
54. G.B. John, L.J. Shirley, T.D. Gallardo, and D.G. Castrillon Specificity of the requirement for Foxo3 in primordial follicle activation Reproduction 133 2007 855 863 (Pubitemid 47162577)
55. P.M. Motta, and S. Makabe Germ cells in the ovarian surface during fetal development in humans. A three-dimensional microanatomical study by scanning and transmission electron microscopy J Submicrosc Cytol 18 1986 271 290 (Pubitemid 16111495)
56. D.F. Albertini Micromanagement of the ovarian follicle reserve - do stem cells play into the ledger? Reproduction 127 2004 513 514 (Pubitemid 38745068)
57. M. Skaznik-Wikiel, J.C. Tilly, H.J. Lee, Y. Niikura, T. Kaneko-Tarui, and J. Johnson et al. Serious doubts over "eggs forever?" Differentiation 75 2007 93 99
58. J. Johnson, J. Bagley, M. Skaznik-Wikiel, H.J. Lee, G.B. Adams, and Y. Niikura et al. Oocyte generation in adult mammalian ovaries by putative germ cells in bone marrow and peripheral blood Cell 122 2005 303 315 (Pubitemid 41032992)
59. E.E. Telfer, R.G. Gosden, A.G. Byskov, N. Spears, D. Albertini, and C.Y. Andersen et al. On regenerating the ovary and generating controversy Cell 122 2005 821 822 (Pubitemid 41345195)
60. K. Eggan, S. Jurga, R. Gosden, I.M. Min, and A.J. Wagers Ovulated oocytes in adult mice derive from noncirculating germ cells Nature 441 2006 1109 1114 (Pubitemid 43990726)
61. H.J. Lee, K. Selesniemi, Y. Niikura, T. Niikura, R. Klein, and D.M. Dombkowski et al. Bone marrow transplantation generates immature oocytes and rescues long-term fertility in a preclinical mouse model of chemotherapy-induced premature ovarian failure J Clin Oncol 25 2007 3198 3204 (Pubitemid 47325602)
62. J.L. Tilly, and B.R. Rueda Minireview: Stem cell contribution to ovarian development, function, and disease Endocrinology 149 2008 4307 4311
63. S. Begum, V.E. Papaioannou, and R.G. Gosden The oocyte population is not renewed in transplanted or irradiated adult ovaries Hum Reprod 23 2008 2326 2330
64. K. Zou, Z. Yuan, Z. Yang, H. Luo, K. Sun, and L. Zhou et al. Production of offspring from a germline stem cell line derived from neonatal ovaries Nat Cell Biol 11 2009 631 636
65. E.A. Gustafson, and G.M. Wessel Vasa genes: emerging roles in the germ line and in multipotent cells Bioessays 32 2010 626 637
66. J. Pacchiarotti, C. Maki, T. Ramos, J. Marh, K. Howerton, and J. Wong et al. Differentiation potential of germ line stem cells derived from the postnatal mouse ovary Differentiation 79 2010 159 170
67. J.L. Tilly, and E.E. Telfer Purification of germline stem cells from adult mammalian ovaries: a step closer toward control of the female biological clock? Mol Hum Reprod 15 2009 393 398
68. Y.A.R. White, D.C. Woods, Y. Takai, O. Ishihara, H. Seki, and J.L. Tilly Oocyte formation by mitotically active germ cells purified from ovaries of reproductive-age women Nat Med 18 2012 413 421
69. J. Oatley, and P.A. Hunt Of mice and (wo)men: purified oogonial stem cells from mouse and human ovaries Biol Reprod 86 2012 1 2
70. H. Zhang, W. Zheng, Y. Shen, D. Adhikari, H. Ueno, and K. Liu Experimental evidence showing that no mitotically active female germline progenitors exist in postnatal mouse ovaries Proc Natl Acad Sci U S A 109 2012 12580 12585
71. L. Lei, and A.C. Spradling Female mice lack adult germ-line stem cells but sustain oogenesis using stable primordial follicles Proc Natl Acad Sci U S A 110 2013 8585 8590
72. C.E. Dunlop, E.E. Telfer, and R.A. Anderson Ovarian stem cells - potential roles in infertility treatment and fertility preservation Maturitas 76 2013 279 283
73. S. Ghazal Oogonial stem cells: do they exist and may they have an impact on future fertility treatment? Curr Opin Obstet Gynecol 25 2013 223 228
74. J. Yuan, D. Zhang, L. Wang, M. Liu, J. Mao, and Y. Yin et al. No evidence for neo-oogenesis may link to ovarian senescence in adult monkey Stem Cells 31 2013 2538 2550
75. S. Wei, L. Zan, G.J. Hausman, T.P. Rasmussen, W.G. Bergen, and M.V. Dodson Dedifferentiated adipocyte-derived progeny cells (DFAT cells): Potential stem cells of adipose tissue Adipocyte 2 2013 122 127
76. M. Herreros-Villanueva, J.S. Zhang, A. Koenig, E.V. Abel, T.C. Smyrk, and W.R. Bamlet et al. SOX2 promotes dedifferentiation and imparts stem cell-like features to pancreatic cancer cells Oncogene 2 2013 e61
77. S.T. Lee, S.P. Gong, K.E. Yum, E.J. Lee, C.H. Lee, and J.H. Choi et al. Transformation of somatic cells into stem cell-like cells under a stromal niche FASEB J 27 2013 2644 2656
78. D. Bhartiya, S. Unni, S. Parte, and S. Anand Very small embryonic-like stem cells: implications in reproductive biology Biomed Res Int 2013 2013 682326
79. M. Miyanishi, Y. Mori, J. Seita, J.Y. Chen, S. Karten, and C.K. Chan et al. Do pluripotent stem cells exist in adult mice as very small embryonic stem cells? Stem Cell Rep 1 2013 198 208
80. D.C. Woods, Y.A. White, and J.L. Tilly Purification of oogonial stem cells from adult mouse and human ovaries: an assessment of the literature and a view toward the future Reprod Sci 20 2013 7 15
81. D.C. Woods, and J.L. Tilly The next (re)generation of ovarian biology and fertility in women: is current science tomorrow's practice? Fertil Steril 98 2012 3 10
82. J.L. Tilly, and D.A. Sinclair Germline energetics, aging, and female infertility Cell Metab 17 2013 838 850