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Identification of cortical germ cells in adult ovaries from three phyllostomid bats: Artibeus jamaicensis, Glossophaga soricina and Sturnira lilium

Nivia Rocio Antonio-Rubio A, Tania Janeth Porras-Gómez A and Norma Moreno-Mendoza A B

A Department of Cell Biology and Physiology, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, Ciudad Universitaria, 04510 México, DF, México.
B Corresponding author. Email: angelica@biomedicas.unam.mx

Reproduction, Fertility and Development - http://dx.doi.org/10.1071/RD12126
Submitted: 19 April 2012  Accepted: 12 July 2012   Published online: 4 September 2012


 
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Abstract

It is generally considered that, in mammals, the ovary is endowed with a finite number of oocytes at the time of birth. However, studies concerning rodents, lemurs and humans suggest the existence of stem cells from the germline that may be involved in germ-cell renewal, maintaining postnatal follicle development. This type of work on wild species is scarce; therefore the objective of this study was to determine ovarian morphology and the presence of progenitor cells from the germline of three species of phyllostomid bats (Artibeus jamaicensis, Glossophaga soricina and Sturnira lilium). The morphological characteristics of the ovaries and the expression of specific markers of germline cells, stem cells and proliferation cells were analysed. The morphology of the ovaries of the three bat species was similar. A polarised ovary with follicles at different stages of development and groups of cortical cells similar to primordial germ cells were observed. Immunofluorescent analysis showed that these cortical cells express germline, stem-cell and proliferative markers, indicating the identification of germ cells that could maintain pluripotency, as well as being mitotically active. This suggests that in the adult ovary of phyllostomid bats there may be a mechanism for the self-renewal of the germline.

Additional keywords: cell proliferation, follicle, immunofluorescence, neo-oogenesis.


References

Adams, I. R., and McLaren, A. (2002). Sexually dimorphic development of mouse primordial germ cells: switching from oogenesis to spermatogenesis. Development 129, 1155–1164.
| CAS | PubMed |

Arita, H. T., and Ceballos, G. (1997). The mammals of Mexico: distribution and conservation status. Revista Mexicana de Mastozoología. 2, 33–71.

Bleier, W. J., and Ehteshami, M. (1981). Ovulation following unilateral ovariectomy in the California leaf-nosed bat (Macrotus californicus). J. Reprod. Fertil. 63, 181–183.
CrossRef | CAS | PubMed |

Bortvin, A., Goodheart, M., Liao, M., and Page, D. C. (2004). Dppa3/Pgc7/stella is a maternal factor and is not required for germ-cell specification in mice. BMC Dev. Biol. 4, 2.
CrossRef | PubMed |

Bowles, J., Knight, D., Smith, C., Wilhelm, D., Richman, J., Mamiya, S., Yashiro, K., Chawengsaksophak, K., Wilson, M. J., Rossant, J., Hamada, H., and Koopman, P. (2006). Retinoid signalling determines germ-cell fate in mice. Science 312, 596–600.
CrossRef | CAS | PubMed |

Buehr, M. (1997). The primordial germ cells of mammals: some current perspectives. Exp. Cell Res. 232, 194–207.
CrossRef | CAS | PubMed |

Buehr, M., McLaren, A., Bartley, A., and Darling, S. (1993). Proliferation and migration of primordial germ cells in We/We mouse embryos. Dev. Dyn. 198, 182–189.
CrossRef | CAS | PubMed |

Bukovsky, A., Keenan, J. A., Caudle, M. R., Wimalasena, J., Upadhyaya, N. B., and Van Meter, S. E. (1995). Immunohistochemical studies of the adult human ovary: possible contribution of immune and epithelial factors to folliculogenesis. Am. J. Reprod. Immunol. 33, 323–340.
| CAS | PubMed |

Bukovsky, A., Michael, R. C., Svetlikova, M., and Upadhyaya, N. B. (2004). Origin of germ cells and formation of new primary follicles in adult human ovaries. Reprod. Biol. Endocrinol. 2, 1–30.
CrossRef |

Bukovsky, A., Caudle, M. R., Gupta, S. K., Svetlikova, M., Selleck-White, R., Ayala, A. M., and Dominguez, R. (2008). Mammalian neo-oogenesis and expression of meiosis-specific protein SCP3 in adult human and monkey ovaries. Cell Cycle 7, 683–686.
CrossRef | CAS | PubMed |

Castrillon, D. H., Quade, B. J., Wang, T. H., Quigley, C., and Crum, C. P. (2000). The human VASA gene is specifically expressed in the germ-cell lineage. Proc. Natl. Acad. Sci. USA 97, 9585–9590.
CrossRef | CAS | PubMed |

Childs, A. J., Cowan, G., Kinnell, H. L., Anderson, R. A., and Saunders, P. T. K. (2011). Retinoic acid signalling and the control of meiotic entry in the human fetal gonad. PLoS ONE 6, e20249.
CrossRef | CAS | PubMed |

David, G. F., Anand, K. T. C., and Baker, T. G. (1974). Uptake of tritiated thymidine by primordial germinal cells in the ovaries of the adult slender loris. J. Reprod. Fertil. 41, 447–451.
CrossRef | CAS | PubMed |

Duke, K. L. (1967). Ovogenetic activity of the fetal-type in the ovary of the adult slow loris, Nycticebus cougang. Folia Primatol. (Basel) 7, 150–154.
CrossRef | CAS |

Geyer, C. B., Saba, R., Kato, Y., Anderson, A. J., Chappell, V. K., Saga, Y., and Eddy, E. M. (2011). Rhox13 is translated in pre-meiotic germ cells in male and female mice and is regulated by NANOS2 in the male. Biol. Reprod. , .
CrossRef |

Høyer, P. E., Byskov, A. G., and Møllgård, K. (2005). Stem cell factor and c-Kit in human primordial germ cells and fetal ovaries. Mol. Cell. Endocrinol. 234, 1–10.
CrossRef | PubMed |

IUCN (2011). 2011 database: IUCN Red List of Threatened Species [internet]. Version 2011.2 Downloaded on 23 March 2012. Available at http://www.iucnredlist.org [Verified 1 August 2012].

Johnson, J., Canning, J., Kaneko, T., Pru, J. K., and Tilly, J. L. (2004). Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature 428, 145–150.
CrossRef | CAS | PubMed |

Kehler, J., Tolkunova, E., Koschorz, B., Pesce, M., Gentile, L., Boiani, M., Lomelí, H., Nagy, A., McLaughlin, K. J., Schöler, H. R., and Tomilin, A. (2004). Oct4 is required for primordial germ cell survival. EMBO Rep. 5, 1078–1083.
CrossRef | CAS | PubMed |

Kerr, C. L., Hill, C. M., Blumenthal, P. D., and Gearhart, J. D. (2007). Expression of pluripotent stem-cell markers in the human fetal ovary. Hum. Reprod. , .
CrossRef |

Komar, C. M., Zacharachis-Jutz, F., Cretekos, C. J., Behringer, R. R., and Rasweiler, J. J. I. V. (2007). Polarized ovaries of the long-tongued bat, Glossophaga soricina: a novel model for studying ovarian development, folliculogenesis and ovulation. Anat. Rec. 290, 1439–1448.
CrossRef |

Lee, J., Iwai, T., Yokota, T., and Yamashita, M. (2003). Temporally- and spatially-selective loss of Rec8 protein from meiotic chromosomes during mammalian meiosis. J. Cell Sci. 116, 2781–2790.
CrossRef | CAS | PubMed |

Liu, Y., Wu, C., Lyu, Q., Yang, D., Albertini, D. F., Keefe, D. L., and Liu, L. (2007). Germline stem cells and neo-oogenesis in the adult human ovary. Dev. Biol. 306, 112–120.
CrossRef | CAS | PubMed |

Liu, Y. J., Nakamura, T., and Nakano, T. (2012). Essential role of DPPA3 for chromatin condensation in mouse oocytogenesis. Biol. Reprod. 86, 40.
CrossRef | PubMed |

MacGregor, G. R., Zambrowicz, B. P., and Soriano, P. (1995). Tissue non-specific alkaline phosphatase is expressed in both embryonic and extraembryonic lineages during mouse embryogenesis but is not required for migration of primordial germ cells. Development 121, 1487–1496.
| CAS | PubMed |

Manova, K., Nocka, K., Besmer, P., and Bachvarova, R. F. (1990). Gonadal expression of c-kit encoded at the W locus of the mouse. Development 110, 1057–1069.
| CAS | PubMed |

McClellan, K. A., Gosden, R., and Taketo, T. (2003). Continuous loss of oocytes throughout meiotic prophase in the normal mouse ovary. Dev. Biol. 258, 334–348.
CrossRef | CAS | PubMed |

McLaren, A. (2003). Primordial germ cells in the mouse. Dev. Biol. 262, 1–15.
CrossRef | CAS | PubMed |

McLaren, A., and Southee, D. (1997). Entry of mouse embryonic germ cells into meiosis. Dev. Biol. 187, 107–113.
CrossRef | CAS | PubMed |

Molyneaux, K., and Wylie, C. (2004). Primordial germ cell migration. Int. J. Dev. Biol. 48, 537–543.
CrossRef | CAS | PubMed |

Morelli, M. A., and Cohen, P. E. (2005). Not all germ cells are created equal: aspects of sexual dimorphism in mammalian meiosis. Reproduction 130, 761–781.
CrossRef | CAS | PubMed |

Myers, M., Britt, K. L., Wreford, N. G. M., Ebling, F. J. P., and Kerr, J. B. (2004). Methods for quantifying follicular numbers within the mouse ovary. Reproduction 127, 569–580.
CrossRef | CAS | PubMed |

National Research Council (1996). ‘Guide for the Care and Use of Laboratory Animals.’ (Institute for Laboratory Animal Research (ILAR) of the National Academy of Science: Bethesda, MD.)

Nichols, J., Zevnik, B., Anastassiadis, K., Niwa, H., Klewe-Nebenius, D., Chambers, I., Schöler, H., and Smith, A. (1998). Formation of pluripotent stem cells in the mammalian embryo depends on the pou transcription factor oct4. Cell 95, 379–391.
CrossRef | CAS | PubMed |

Oulad-Abdelghani, M., Bouillet, P., Décimo, D., Gansmuller, A., Heyberger, S., Dollé, P., Bronner, S., Lutz, Y., and Chambon, P. (1996). Characterization of a pre-meiotic germ cell-specific cytoplasmic protein encoded by Stra8, a novel retinoic acid-responsive gene. J. Cell Biol. 135, 469–477.
CrossRef | CAS | PubMed |

Parte, S., Bhartiya, D., Telang, J., Daithankar, V., Salvi, V., Zaveri, K., and Hinduja, I. (2011). Detection, characterization, and spontaneous differentiation in vitro of very small embryonic-like putative stem cells in adult mammalian ovary. Stem Cells Dev. 20, 1451–1464.
CrossRef | CAS | PubMed |

Payer, B., Saitou, M., Barton, S. C., Thresher, R., Dixon, J. P. C., Zahn, D., Colledge, W. H., Carlton, M. B. L., Nakano, T., and Surani, M. A. (2003). Stella is a maternal-effect gene required for normal early development in mice. Curr. Biol. 13, 2110–2117.
CrossRef | CAS | PubMed |

Pepling, M. E., and Spradling, A. C. (2001). Mouse ovarian germ-cell cysts undergo programmed breakdown to form primordial follicles. Dev. Biol. 234, 339–351.
CrossRef | CAS | PubMed |

Pesce, M., Farrace, M. G., Piacentini, M., Dolci, S., and De Felici, M. (1993). Stem cell factor and leukaemia inhibitory factor promote primordial germ-cell survival by suppressing programmed cell death (apoptosis). Development 118, 1089–1094.
| CAS | PubMed |

Pesce, M., Wang, X., Wolgemuth, D. J., and Schöler, H. (1998). Differential expression of the Oct-4 transcription factor during mouse germ-cell differentiation. Mech. Dev. 71, 89–98.
CrossRef | CAS | PubMed |

Rasweiler, J. J. (1972). Reproduction in the long-tongued bat, Glossophaga soricina. I. Preimplantation development and histology of the oviduct. J. Reprod. Fertil. 31, 249–262.
CrossRef | PubMed |

Rasweiler, J. J., IV, and Badwaik, N. K. (2000). Anatomy and physiology of the female tract. In ‘Reproductive Biology of Bats’. (Eds E. G. Crichton and P. H. Krutzsch.) pp. 157–219. (Academic Press: London.)

Raz, E. (2000). The function and regulation of vasa-like genes in germ-cell development. Genome Biol. 1, reviews1017.1–1017.6.
CrossRef |

Saitou, M., Barton, S. C., and Surani, A. (2002). A molecular programme for the specification of germ-cell fate in mice. Nature 418, 293–300.
CrossRef | CAS | PubMed |

Sato, M., Kimura, T., Kurokawa, K., Fujita, Y., Abe, K., Masuhara, M., Yasunaga, T., Ryo, A., Yamamoto, M., and Nakano, T. (2002). Identification of PGC7, a new gene expressed specifically in preimplantation embryos and germ cells. Mech. Dev. 113, 91–94.
CrossRef | CAS | PubMed |

Schöler, H. R., Hatzopoulos, A. K., Balling, R., Suzuki, N., and Gruss, P. (1989). A family of octamer-specific proteins present during mouse embryogenesis: evidence for germline-specific expression of an Oct factor. EMBO J. 8, 2543–2550.
| PubMed |

Tanaka, S. S., Toyooka, Y., Akasu, R., Katoh-Fukui, Y., Nakahara, Y., Suzuki, R., Yokoyama, M., and Noce, T. (2000). The mouse homolog of Drosophila Vasa is required for the development of male germ cells. Genes Dev. 14, 841–853.
| CAS | PubMed |

Toyooka, Y., Tsunekawa, N., Takahashi, Y., Matsui, Y., Satoh, M., and Noce, T. (2000). Expression and intracellular localization of mouse Vasa-homologue protein during germ cell development. Mech. Dev. 93, 139–149.
CrossRef | CAS | PubMed |

White, Y. A. R., Woods, D. C., Takai, Y., Ishihara, O., Seki, H., and Tilly, J. L. (2012). Oocyte formation by mitotically active germ cells purified from ovaries of reproductive-age women. Nat. Med. 18, 413–421.
CrossRef | CAS |

Wylie, C. (1999). Germ Cells. Cell 96, 165–174.
CrossRef | CAS | PubMed |

Zamboni, L., and Merchant, H. (1973). The fine morphology of mouse primordial germ cells in extragonadal locations. Am. J. Anat. 137, 299–335.
CrossRef | CAS | PubMed |

Zhang, P., Lv, L. X., and Xing, W. J. (2010). Early meiotic-specific protein expression in postnatal rat ovaries. Reprod. Domest. Anim. , .
CrossRef | PubMed |

Zuccotti, M., Merico, V., Sacchi, L., Bellone, M., Brink, T. C., Stefanelli, M., Redi, C. A., Bellazzi, R., Adjaye, J., and Garagna, S. (2009). Oct-4 regulates the expression of Stella and Foxj2 at the Nanog locus: implications for the developmental competence of mouse oocytes. Hum. Reprod. 24, 2225–2237.
CrossRef | CAS | PubMed |


   
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