Skip to main content
SpringerLink
Log in

The Rise and Fall of Oogonial Stem Cells Within the Historical Context of Adult Stem Cells

  • Chapter
Primary Ovarian Insufficiency

  • 803 Accesses

Abstract

For decades, it has been believed that adult human female reproductive potential was determined by a finite number of primordial follicles, which are established in the embryonic gonad. The rise of adult stem cells in other organs inevitably led to investigations that searched for stem cells in various organs of the reproductive tract, including ovaries, endometrium, and uterus. Within ovaries, somatic stem cells that drive granulosa cell proliferation and provide an essential support environment for differentiating oocytes have been characterized with little controversy. No adult stem cell claim has stirred as much controversy as the one that oogonial stem cells exist and can give rise to neo-oogenesis. Such a finding would render women, previously believed to have a nonrenewable gamete supply, remarkably more like men, who are able to replenish their germ cells. We review the rise and fall of oogonial stem cells in the historical context of the general concept of adult stem cells.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 89.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 119.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 119.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Ramalho-Santos M, Willenbring H. On the origin of the term “stem cell”. Cell Stem Cell. 2007;1:35–8.

    Article  CAS  PubMed  Google Scholar 

  2. Richards RJ. The tragic sense of life: Ernst Haeckel and the struggle over evolutionary thought. Chicago: University of Chicago Press; 2008.

    Book  Google Scholar 

  3. Haeckel E. Natürliche Schöpfungsgeschichte. Berlin: Georg Reimer; 1868. 15th lecture.

    Google Scholar 

  4. Haeckel E. Anthropogenie oder Entwickelungsgeschichte des Menschen. 3rd ed. Leipzig: Wilhelm Engelmann; 1877. p. 144. my translation.

    Google Scholar 

  5. Boveri T. Zur Frage der Entstehung maligner Tumoren. Jena: Gustav Fischer; 1914. p. 2.

    Google Scholar 

  6. Weismann A. Die Continuität des Keimplasma’s als Grundlage einer Theorie der Vererbung. Jena: Gustav Fischer; 1885. p. 5–21.

    Google Scholar 

  7. Satzinger H. Differenz und Vererbung. Geschlechterordnungen in der Genetik und Hormonforschung 1890–1950. Cologne: Böhlau Verlag; 2009. p. 85–97.

    Google Scholar 

  8. Baltzer F. Theodor Boveri: life and work of a great biologist 1862–1915. Berkeley, CA: University of California Press; 1967.

    Google Scholar 

  9. Harwood J. Styles of scientific thought. The German genetics community 1900-1933. Chicago: University of Chicago Press; 1993. p. 52–5.

    Google Scholar 

  10. Haecker V. Über Gedächtnis, Vererbung und Pluripotenz. Jena: Gustav Fischer; 1914. p. 63–85.

    Google Scholar 

  11. Haecker R. Das Leben von Valentin Haecker. Zoologischer Anzeiger. 1965;174:1–22.

    Google Scholar 

  12. Pappenheim A. Zwei Fälle akuter grosslymphozytärer Leukämie. Folia Haematologica. 1907;4:301–8. On Pappenheim and his haematological work see: Dinser, Ricarda. Der Beitrag Artur Pappenheims zur Hämatologie um die Jahrhundertwende. Ruhr-Universität Bochum.

    Google Scholar 

  13. Dantschakoff W. Untersuchungen über die Entwickelung des Blutes und Bindegewebes bei den Vögeln. Anatomische Hefte. 1908;37:471–589. On Dantschakoff’s international career see Satzinger, op. cit. (note 19), p. 231–2, 394–6.

    Article  Google Scholar 

  14. Maximow A. Der Lymphozyt als gemeinsame Stammzelle der verschiedenen Blutelemente in der embryonalen Entwicklung und im postfetalen Leben der Säugetiere. Folia Haematologica. 1909;8:125–34. Konstantinov IE. In search of Alexander A. Maximow: the man behin.

    Google Scholar 

  15. Neumann E. Hämatologische Studien I.–III. Virchows Archiv für pathologische Anatomie. 225-77 (1896); 174, 41–78 (1903); 207, 379–412 (1912).

    Google Scholar 

  16. Ehrlich P, Lazarus A. Histology of the blood: normal and pathological. Cambridge: University Press; 1900. p. 81.

    Google Scholar 

  17. Neumann E. Ueber die Bedeutung des Knochenmarkes für die Blutbildung, Vorläufige Mittheilung. Centralblatt für die medicinischen Wissenschaften. 1868; 6(44). Neumann-Redlin v Meding, E. Der Pathologe Ernst Neumann (1834–1918) und sein Beitrag zur Begründung.

    Google Scholar 

  18. Monti M, Perotti C, Del Fante C, Cervio M, Redi CA. Stem cells: sources and therapies. BiolRes [Internet]. 2012; 45(3):207–14. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23283430

  19. Cairns J. Mutation selection and the natural history of cancer. Nature. 1975;255:197–200.

    Article  CAS  PubMed  Google Scholar 

  20. Cairns J. Somatic stem cells and the kinetics of mutagenesis and carcinogenesis. Proc Natl Acad Sci U S A. 2002;99:10567–70.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  21. Cairns J. Cancer and the immortal strand hypothesis. Genetics. 2006;174:1069–72.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  22. Schofield R. The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells. 1978;4:7–25.

    CAS  PubMed  Google Scholar 

  23. Scheres B. Stem-cell niches: nursery rhymes across kingdoms. Nat Rev Mol Cell Biol [Internet]. 2007 [cited 2014 May 26]; 8(5):345–54. Available from: http://www.ncbi.nlm.nih.gov/pubmed/17450175

    Google Scholar 

  24. Jones DL, Wagers AJ. No place like home: anatomy and function of the stem cell niche. Nat Rev Mol Cell Biol [Internet]. 2008 [cited 2014 May 26]; 9(1):11–21. Available from: http://www.ncbi.nlm.nih.gov/pubmed/18097443

    Google Scholar 

  25. Knoblich JA. Mechanisms of asymmetric stem cell division. Cell [Internet]. 2008 [cited 2014 May 26]; 132(4):583–97. Available from: http://www.ncbi.nlm.nih.gov/pubmed/18295577

    Google Scholar 

  26. Morrison SJ, Spradling AC. Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell [Internet]. 2008 [cited 2014 May 26]; 132(4):598–611. Available from: http://www.ncbi.nlm.nih.gov/pubmed/18295578

  27. Kimble JE, White JG. On the control of germ cell development in Caenorhabditis elegans. Dev Biol [Internet]. 1981; 81(2):208–19. Available from: http://www.ncbi.nlm.nih.gov/pubmed/7202837

    Google Scholar 

  28. Kiger AA, Jones DL, Schulz C, Rogers MB, Fuller MT. Stem cell self-renewal specified by JAK-STAT activation in response to a support cell cue. Science [Internet]. 2001 [cited 2014 May 26]; 294(5551):2542–5. Available from: http://www.ncbi.nlm.nih.gov/pubmed/11752574

    Google Scholar 

  29. Tulina N, Matunis E. Control of stem cell self-renewal in Drosophila spermatogenesis by JAK-STAT signaling. Science [Internet]. 2001 [cited 2014 May 26]; 294(5551):2546–9. Available from: http://www.ncbi.nlm.nih.gov/pubmed/11752575

    Google Scholar 

  30. Fuller MT, Spradling AC. Male and female Drosophila germline stem cells: two versions of immortality. Science [Internet]. 2007 [cited 2014 May 26]; 316(5823):402–4. Available from: http://www.ncbi.nlm.nih.gov/pubmed/17446390

    Google Scholar 

  31. Nagy A, Rossant J, Nagy R, Abramow-Newerly W, Roder JC. Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc Natl Acad Sci U S A [Internet]. 1993; 90(18):8424–8. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=47369&tool=pmcentrez&rendertype=abstract

  32. Pera MF, Reubinoff B, Trounson A. Human embryonic stem cells. J Cell Sci. 2000;113:5–10.

    CAS  PubMed  Google Scholar 

  33. Donovan PJ, de Miguel MP. Turning germ cells into stem cells. Curr Opin Genet Dev [Internet]. 2003 [cited 2014 Jul 20]; 13(5):463–71. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0959437X03001217

    Google Scholar 

  34. Thomson JA. Embryonic stem cell lines derived from human blastocysts. Science (80-) [Internet]. 1998 [cited 2014 May 23]; 282(5391):1145–7. Available from: http://www.sciencemag.org/cgi/doi/10.1126/science.282.5391.1145

    Google Scholar 

  35. Spradling A, Fuller MT, Braun RE, Yoshida S. Germline stem cells. Cold Spring Harb Perspect Biol [Internet]. 2011 [cited 2014 Jul 9]; 3(11):a002642. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3220357&tool=pmcentrez&rendertype=abstract

  36. Cinquin O. Purpose and regulation of stem cells: a systems-biology view from the Caenorhabditis elegans germ line. J Pathol. 2009;217:186–98.

    Article  PubMed Central  PubMed  Google Scholar 

  37. Crittenden SL, Leonhard KA, Byrd DT, Kimble J. Cellular analyses of the mitotic region in the Caenorhabditis elegans adult germ line. Mol Biol Cell. 2006;17(July):3051–61.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  38. Cinquin O, Crittenden SL, Morgan DE, Kimble J. Progression from a stem cell-like state to early differentiation in the C. elegans germ line. Proc Natl Acad Sci U S A [Internet]. 2010 [cited 2014 Jul 16]; 107(5):2048–53. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2836686&tool=pmcentrez&rendertype=abstract

  39. Wong MD, Jin Z, Xie T. Germline, molecular mechanisms of regulation, stem cell. Annu Rev Genet. 2005;39:173–95.

    Article  CAS  PubMed  Google Scholar 

  40. Spradling AC. Developmental genetics of oogenesis. In: Bate M, Martinez Arias A, editors. The development of Drosophila melanogaster. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 1993.

    Google Scholar 

  41. De Felici M, Barrios F. Seeking the origin of female germline stem cells in the mammalian ovary. Reproduction [Internet]. 2013 [cited 2014 Jul 19]; 146(4):R125–30. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23801781

    Google Scholar 

  42. Böttger SA, Walker CW, Unuma T. Care and maintenance of adult echinoderms. Methods Cell Biol. 2004;74:17–38.

    Article  PubMed  Google Scholar 

  43. Kurimoto K, Yabuta Y, Ohinata Y, Shigeta M, Yamanaka K, Saitou M. Complex genome-wide transcription dynamics orchestrated by Blimp1 for the specification of the germ cell lineage in mice. Genes Dev [Internet]. 2008 [cited 2014 Jul 15]; 22(12):1617–35. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2428060&tool=pmcentrez&rendertype=abstract

  44. Yamaji M, Seki Y, Kurimoto K, Yabuta Y, Yuasa M, Shigeta M, et al. Critical function of Prdm14 for the establishment of the germ cell lineage in mice. Nat Genet [Internet]. 2008 [cited 2014 Jul 15]; 40(8):1016–22. Available from: http://www.ncbi.nlm.nih.gov/pubmed/18622394

    Google Scholar 

  45. Zuckerman S. The number of oocytes in the mature ovary. Recent Prog Horm Res. 1951;6:63–108.

    Google Scholar 

  46. Baker TG. A quantitative and cytological study of germ cells in human ovaries. Proc R Soc Lond B Biol Sci. 1963;158:417–33.

    Article  CAS  PubMed  Google Scholar 

  47. Reynaud K, Cortvrindt R, Verlinde F, De Schepper J, Bourgain C, Smitz J. Number of ovarian follicles in human fetuses with the 45,X karyotype. Fertil Steril. 2004;81:1112–9.

    Article  PubMed  Google Scholar 

  48. Kurilo LF. Oogenesis in antenatal development in man. Hum Genet. 1981;57:86–92.

    Article  CAS  PubMed  Google Scholar 

  49. Johnson J, Bagley J, Skaznik-Wikiel M, Lee H-J, Adams GB, Niikura Y, et al. Oocyte generation in adult mammalian ovaries by putative germ cells in bone marrow and peripheral blood. Cell [Internet]. 2005 29 [cited 2014 Jul 20]; 122(2):303–15. Available from: http://www.ncbi.nlm.nih.gov/pubmed/16051153

    Google Scholar 

  50. Mork L, Tang H, Batchvarov I, Capel B. Mouse germ cell clusters form by aggregation as well as clonal divisions. Mech Dev. 2012;128:591–6.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  51. Pepling ME, Spradling AC. Mouse ovarian germ cell cysts undergo programmed breakdown to form primordial follicles. Dev Biol [Internet]. 2001 [cited 2014 Jul 16]; 234(2):339–51. Available from: http://www.ncbi.nlm.nih.gov/pubmed/11397004

    Google Scholar 

  52. Lechowska A, Bilinski S, Choi Y, Shin Y, Kloc M, Rajkovic A. Premature ovarian failure in nobox-deficient mice is caused by defects in somatic cell invasion and germ cell cyst breakdown. J Assist Reprod Genet. 2011;28:583–9.

    Article  PubMed Central  PubMed  Google Scholar 

  53. Pangas SA, Rajkovic A. Follicular development: mouse, sheep, and human models [Internet]. In: Plant TM, Zeleznik AJ, editors. Knobil and Neill’s physiology of reproduction. Elsevier Inc., Amsterdam. Available from: http://dx.doi.org/10.1016/B978-0-12-3971

  54. Sullivan SD, Castrillon DH. Insights into primary ovarian insufficiency through genetically engineered mouse models. Semin Reprod Med. 2011;29(4):283–98.

    Article  CAS  PubMed  Google Scholar 

  55. Driancourt MA, Reynaud K, Cortvrindt R, Smitz J. Roles of KIT and KIT LIGAND in ovarian function. Rev Reprod. 2000;5:143–52.

    Article  CAS  PubMed  Google Scholar 

  56. Nilsson EE, Skinner MK. Bone morphogenetic protein-4 acts as an ovarian follicle survival factor and promotes primordial follicle development. Biol Reprod. 2003;69:1265–72.

    Article  CAS  PubMed  Google Scholar 

  57. Parrott JA, Skinner MK. NoKit-ligand/stem cell factor induces primordial follicle development and initiates folliculogenesis. Endocrinology. 1999;140:4262–71.

    CAS  PubMed  Google Scholar 

  58. Nilsson E, Parrott JA, Skinner MK. Basic fibroblast growth factor induces primordial follicle development and initiates folliculogenesis. Mol Cell Endocrinol. 2001;175:123–30.

    Article  CAS  PubMed  Google Scholar 

  59. Nilsson EE, Kezele P, Skinner MK. Leukemia inhibitory factor (LIF) promotes the primordial to primary follicle transition in rat ovaries. Mol Cell Endocrinol. 2002;188:65–73.

    Article  CAS  PubMed  Google Scholar 

  60. John GB, Gallardo TD, Shirley LJ, Castrillon DH. Foxo3 is a PI3K dependent molecular switch controlling the initiation of oocyte growth. Dev Biol. 2008;321:197–204.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  61. Castrillon DH, Miao L, Kollipara R, Horner JW, DePinho RA. Suppression of ovarian follicle activation in mice by the transcription factor Foxo3a. Science. 2003;301:215–8.

    Article  CAS  PubMed  Google Scholar 

  62. Gallardo TD, John GB, Bradshaw K, et al. Sequence variation at the human FOXO3 locus: a study of premature ovarian failure and primary amenorrhea. Hum Reprod. 2008;23:216–21.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  63. Dunlop CE, Telfer EE, Anderson RA. Ovarian stem cells--potential roles in infertility treatment and fertility preservation. Maturitas [Internet]. Elsevier Ireland Ltd; 2013 [cited 2014 Apr 28]; 76(3):279–83. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23693139

  64. Reddy P, Liu L, Adhikari D, Jagarlamudi K, Rajareddy S, Shen Y, et al. Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool. Science. 2008;319(February):611–3.

    Article  CAS  PubMed  Google Scholar 

  65. Adhikari D, Zheng W, Shen Y, Gorre N, Hämäläinen T, Cooney AJ, et al. Tsc/mTORC1 signaling in oocytes governs the quiescence and activation of primordial follicles. Hum Mol Genet. 2009;19(3):397–410.

    Article  PubMed Central  PubMed  Google Scholar 

  66. Li J, Kawamura K, Cheng Y, et al. Activation of dormant ovarian follicles to generate mature eggs. Proc Natl Acad Sci U S A. 2010;107:10280–4.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  67. Kawamura K, Cheng Y, Suzuki N, Deguchi M, Sato Y, Takae S, et al. Hippo signaling disruption and Akt stimulation of ovarian follicles for infertility treatment. Proc Natl Acad Sci U S A [Internet]. 2013;110(43):17474–9. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3808580&tool=pmcentrez&rendertype=abstract.

    Article  CAS  Google Scholar 

  68. Dong J, Albertini DF, Nishimori K, Kumar TR, Lu N, Matzuk M. Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature. 1996;383(6600):531–5.

    Article  CAS  PubMed  Google Scholar 

  69. Dierich A, Sairam MR, Monaco L, Fimia GM, Gansmuller A, LeMeur M, et al. Impairing follicle-stimulating hormone (FSH) signaling in vivo: targeted disruption of the FSH receptor leads to aberrant gametogenesis and hormonal imbalance. Proc Natl Acad Sci U S A. 1998;95(22):13612–7.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  70. Baker J, Hardy MP, Zhou J, Bondy C, Lupu F, Bellvé AR, Efstratiadis A. Effects of an Igf1 gene null mutation on mouse reproduction. Mol Endocrinol. 1996;10(7):903–18.

    CAS  PubMed  Google Scholar 

  71. Matzuk MM, Finegold MJ, Su JG, Hsueh AJ, Bradley A. Alpha-inhibin is a tumour-suppressor gene with gonadal specificity in mice. Nature. 1992;360:313–9.

    Article  CAS  PubMed  Google Scholar 

  72. Sicinski P, Donaher JL, Geng Y, Parker SB, Gardner H, Park MY, et al. Cyclin D2 is an FSH-responsive gene involved in gonadal cell proliferation and oncogenesis. Nature. 1996;384:470–4.

    Article  CAS  PubMed  Google Scholar 

  73. Tomic D, Miller KP, Kenny HA, Woodruff TK, Hoyer P, Flaws JA. Ovarian follicle development requires Smad3. Mol Endocrinol. 2004;18(February):2224–40.

    Article  CAS  PubMed  Google Scholar 

  74. Freiman RN, Albright SR, Zheng S, Sha WC, Hammer RE, Tjian R. Requirement of tissue-selective TBP-associated factor TAFII105 in ovarian development. Science. 2001;293:2084–7.

    Article  CAS  PubMed  Google Scholar 

  75. Kumar TR, Wang Y, Lu N, Matzuk MM. Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility. Nat Genet. 1997;15(2):201–4.

    Article  CAS  PubMed  Google Scholar 

  76. Lubahn DB, Moyer JS, Golding TS, Couse JF, Korach KS, Smithies O. Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc Natl Acad Sci U S A. 1993;90(December):11162–6.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  77. Krege JH, Hodgin JB, Couse JF, Enmark E, Warner M, Mahler JF, et al. Generation and reproductive phenotypes of mice lacking estrogen receptor beta. Proc Natl Acad Sci U S A. 1998;95(December):15677–82.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  78. Simon AM, Goodenough DA, Li E, Paul DL. Female infertility in mice lacking connexin 37. Nature. 1997;385:525–9.

    Article  CAS  PubMed  Google Scholar 

  79. Matzuk MM, Kumar TR, Bradley A. Different phenotypes for mice deficient in either activins or activin receptor type II. Nature. 1995;374:356–60.

    Article  CAS  PubMed  Google Scholar 

  80. Johnson J, Canning J, Kaneko T, Pru JK, Tilly JL. Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature [Internet]. 2004;428(6979):145–50. Available from: http://www.ncbi.nlm.nih.gov/pubmed/15014492.

    Article  CAS  Google Scholar 

  81. Fujiwara Y, Komiya T, Kawabata H, Sato M, Fujimoto H, Furusawa M, et al. Isolation of a DEAD-family protein gene that encodes a murine homolog of Drosophila vasa and its specific expression in germ cell lineage. Proc Natl Acad Sci U S A [Internet]. 1994;91(25):12258–62. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=45416&tool=pmcentrez&rendertype=abstract.

    Article  CAS  Google Scholar 

  82. Noce T, Okamoto-Ito S, Tsunekawa N. Vasa homolog genes in mammalian germ cell development. Cell Struct Funct [Internet]. 2001;26(3):131–6. Available from: http://www.ncbi.nlm.nih.gov/pubmed/11565805.

    Article  CAS  Google Scholar 

  83. Johnson J, Skaznik-wikiel M, Lee H, Tilly JC, Tilly JL. Setting the record straight on data supporting postnatal oogenesis in female mammals. Cell Cycle. 2005;4(November):1471–7.

    CAS  PubMed  Google Scholar 

  84. Telfer EE, Gosden RG, Byskov AG, Spears N, Albertini D, Andersen CY, et al. On regenerating the ovary and generating controversy. Cell [Internet]. 2005 [cited 2014 Jul 21]; 122(6):821–2. Available from: http://www.ncbi.nlm.nih.gov/pubmed/16179247

    Google Scholar 

  85. Bristol-Gould SK, Kreeger PK, Selkirk CG, Kilen SM, Mayo KE, Shea LD, et al. Fate of the initial follicle pool: empirical and mathematical evidence supporting its sufficiency for adult fertility. Dev Biol [Internet]. 2006 [cited 2014 Jul 21]; 298(1):149–54. Available from: http://www.ncbi.nlm.nih.gov/pubmed/16925987

    Google Scholar 

  86. Krarup T. Effect of 9,10-dimethyl-1,2-benzanthracene on the mouse ovary. Ovarian tumorigenesis. Br J Cancer. 1970;24(1):168–86.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  87. Krarup T. Oocyte survival in the mouse ovary after treatment with 9,10-dimethyl-1,2-benzanthracene. J Endocrinol. 1970;46(4):483–95.

    Article  CAS  PubMed  Google Scholar 

  88. Motta PM, Makabe S. 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. 1986;18(2):271–90.

    CAS  PubMed  Google Scholar 

  89. Motta PM, Makabe S. Elimination of germ cells during differentiation of the human ovary: an electron microscopic study. Eur J Obstet Gynecol Reprod Biol. 1986;22(5–6):271–86.

    Article  CAS  PubMed  Google Scholar 

  90. Eppig JJ, Wigglesworth K. Development of mouse and rat oocytes in chimeric reaggregated ovaries after interspecific exchange of somatic and germ cell components. Biol Reprod [Internet]. 2000;63(4):1014–23. Available from: http://www.ncbi.nlm.nih.gov/pubmed/10993822.

    Article  CAS  Google Scholar 

  91. Carroll J, Whittingham DG, Wood MJ, Telfer E, Gosden RG. Extra-ovarian production of mature viable mouse oocytes from frozen primary follicles. J Reprod Fertil. 1990;90(1):321–7.

    Article  CAS  PubMed  Google Scholar 

  92. Ballas CB, Zielske SP, Gerson SL. Adult bone marrow stem cells for cell and gene therapies: implications for greater use. J Cell Biochem Suppl. 2002;38:20–8.

    Article  PubMed  Google Scholar 

  93. Jadczyk T, Pedziwiatr D, Wojakowski W. New advances in stem cell research: practical implications for regenerative medicine. Polish Arch Intern Med. 2014;124:417–26.

    Google Scholar 

  94. Lawson KA, Hage WJ. Clonal analysis of the origin of primordial germ cells in the mouse. Ciba Found Symp. 1994;182:68–84.

    CAS  PubMed  Google Scholar 

  95. Edelmann W, Keeney S, Jasin M, Di Giacomo M, Barchi M. Distinct DNA-damage-dependent and -independent responses drive the loss of oocytes in recombination-defective mouse mutants. Proc Natl Acad Sci U S A. 2005;102(3):737–42.

    Article  PubMed Central  PubMed  Google Scholar 

  96. Hematti P, Sloand EM, Carvallo CA, Albert MR, Yee CL, Fuehrer MM, et al. Absence of donor-derived keratinocyte stem cells in skin tissues cultured from patients after mobilized peripheral blood hematopoietic stem cell transplantation. Exp Hematol [Internet]. 2002;30(8):943–9. Available from: http://www.ncbi.nlm.nih.gov/pubmed/12160846.

    Article  Google Scholar 

  97. Ainsworth C. Bone cells linked to creation of fresh eggs in mammals. Nature [Internet]. 2005;436(7051):609. Available from: http://www.ncbi.nlm.nih.gov/pubmed/16079804.

    Article  CAS  Google Scholar 

  98. Skeptics demand duplication of controversial fertility claim. Maine company falls a-fowl for smuggling bird flu. As the virulent bird flu sweeping through Asia. 2005;11(9):2005.

    Google Scholar 

  99. Eggan K, Jurga S, Gosden R, Min IM, Wagers AJ. Ovulated oocytes in adult mice derive from non-circulating germ cells. Nature. 2006;441(June):1109–14.

    Article  CAS  PubMed  Google Scholar 

  100. Zou K, Yuan Z, Yang Z, Luo H, Sun K, Zhou L, et al. Production of offspring from a germline stem cell line derived from neonatal ovaries. Nat Cell Biol [Internet]. 2009 [cited 2014 Jul 21]; 11(5):631–6. Available from: http://www.ncbi.nlm.nih.gov/pubmed/19363485

    Google Scholar 

  101. Toyooka Y, Tsunekawa N, Takahashi Y, Matsui Y, Satoh M, Noce T. Expression and intracellular localization of mouse Vasa-homologue protein during germ cell development. Mech Dev. 2000;93(1–2):139–49.

    Article  CAS  PubMed  Google Scholar 

  102. Castrillon DH, Quade BJ, Wang TY, Quigley C, Crum CP. The human VASA gene is specifically expressed in the germ cell lineage. Proc Natl Acad Sci U S A. 2000;97:9585–90.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  103. Pacchiarotti J, Maki C, Ramos T, Marh J, Howerton K, Wong J, et al. Differentiation potential of germ line stem cells derived from the postnatal mouse ovary. Differentiation [Internet]. Elsevier; 2010 [cited 2014 Jul 10]; 79(3):159–70. Available from: http://www.ncbi.nlm.nih.gov/pubmed/20138422

    Google Scholar 

  104. Zhang H, Zheng W, Shen Y, Adhikari D, Ueno H, Liu K. Experimental evidence showing that no mitotically active female germline progenitors exist in postnatal mouse ovaries. Proc Natl Acad Sci U S A [Internet]. 2012 [cited 2014 May 26]; 109(31):12580–5. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3411966&tool=pmcentrez&rendertype=abstract

  105. Red-Horse K, Ueno H, Weissman IL, Krasnow MA. Coronary arteries form by developmental reprogramming of venous cells. Nature [Internet]. Nature Publishing Group; 2010 [cited 2014 Jul 11]; 464(7288):549–53. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2924433&tool=pmcentrez&rendertype=abstract

  106. Rinkevich Y, Lindau P, Ueno H, Longaker MT, Weissman IL. Germ-layer and lineage-restricted stem/progenitors regenerate the mouse digit tip. Nature [Internet]. Nature Publishing Group; 2011 [cited 2014 Jul 17]; 476(7361):409–13. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3812235&tool=pmcentrez&rendertype=abstract

  107. Lei L, Spradling AC. Female mice lack adult germ-line stem cells but sustain oogenesis using stable primordial follicles. Proc Natl Acad Sci U S A [Internet]. 2013 [cited 2014 May 26]; 110(21):8585–90. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3666718&tool=pmcentrez&rendertype=abstract

  108. Hayashi S, McMahon AP. Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev Biol [Internet]. 2002 [cited 2014 Jul 11]; 244(2):305–18. Available from: http://www.ncbi.nlm.nih.gov/pubmed/11944939

    Google Scholar 

  109. Srinivas S, Watanabe T, Lin CS, William CM, Tanabe Y, Jessell TM, et al. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol [Internet]. 2001;1:4. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=31338&tool=pmcentrez&rendertype=abstract.

    Article  CAS  Google Scholar 

  110. Ng A, Tan S, Singh G, Rizk P, Swathi Y, Tan TZ, et al. Lgr5 marks stem/progenitor cells in ovary and tubal epithelia. Nat Cell Biol [Internet]. 2014 [cited 2014 Dec 5]; 16(8):745–57. Available from: http://www.ncbi.nlm.nih.gov/pubmed/24997521

    Google Scholar 

  111. Zheng W, Zhang H, Gorre N, Risal S, Shen Y, Liu K. Two classes of ovarian primordial follicles exhibit distinct developmental dynamics and physiological functions. Hum Mol Genet [Internet]. 2014 [cited 2014 Dec 10]; 23(4):920–8. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3900105&tool=pmcentrez&rendertype=abstract

  112. Capel B. Ovarian epithelium regeneration by Lgr5(+) cells. Nat Cell Biol [Internet]. Nature Publishing Group; 2014 [cited 2014 Dec 10]; 16(8):743–4. Available from: http://www.ncbi.nlm.nih.gov/pubmed/25082199

  113. Mork L, Maatouk DM, McMahon JA, Guo JJ, Zhang P, McMahon AP, et al. Temporal differences in granulosa cell specification in the ovary reflect distinct follicle fates in mice. Biol Reprod [Internet]. 2012 [cited 2014 Dec 8]; 86(2):37. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3290667&tool=pmcentrez&rendertype=abstract

  114. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell [Internet]. 2007 [cited 2014 Jul 9]; 131(5):861–72. Available from: http://www.ncbi.nlm.nih.gov/pubmed/18035408

    Google Scholar 

  115. Sun N, Zhao H. Seamless correction of the sickle cell disease mutation of the HBB gene in human induced pluripotent stem cells using TALENs. Biotechnol Bioeng. 2014;111(5):1048–53.

    Article  CAS  PubMed  Google Scholar 

  116. Sebastiano V, Maeder ML, Angstman JF, Haddad B, Khayter C, Yeo DT, et al. In situ genetic correction of the sickle cell anemia mutation in human induced pluripotent stem cells using engineered zinc finger nucleases. Stem Cells. 2011;29:1717–26.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  117. Hayashi K, Saitou M. Generation of eggs from mouse embryonic stem cells and induced pluripotent stem cells. Nat Protoc [Internet]. Nature Publishing Group; 2013; 8(8):1513–24. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23845963

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Obstetrics, Gynecology, and Reproductive Sciences, Magee-Womens Research Institute, University of Pittsburgh, Pittsburgh, PA, 15213, USA

    Shweta Nayak MD, Yu Ren PhD & Aleksandar Rajkovic MD, PhD

Authors
  1. Shweta Nayak MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yu Ren PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Aleksandar Rajkovic MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aleksandar Rajkovic MD, PhD .

Editor information

Editors and Affiliations

  1. Obstetrics and Gynecology, University of Colorado, Aurora, Colorado, USA

    Nanette F. Santoro

  2. Obstetrics and Gynecology, Washington University, St. Louis, Missouri, USA

    Amber R. Cooper

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Nayak, S., Ren, Y., Rajkovic, A. (2016). The Rise and Fall of Oogonial Stem Cells Within the Historical Context of Adult Stem Cells. In: Santoro, N., Cooper, A. (eds) Primary Ovarian Insufficiency. Springer, Cham. https://doi.org/10.1007/978-3-319-22491-6_11

Download citation

  • DOI: https://doi.org/10.1007/978-3-319-22491-6_11

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-319-22490-9

  • Online ISBN: 978-3-319-22491-6

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics

Search

Navigation