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Interaction between oocytes, cortical germ cells and granulosa cells of the mouse and bat, following the dissociation–re-aggregation of adult ovaries

Published online by Cambridge University Press:  03 March 2020

Tania Janeth Porras-Gómez
Affiliation:
Laboratorio de Biología Tisular y Reproductora, Departamento de Biología Comparada, Facultad de Ciencias, Universidad Nacional Autónoma de México
Norma Moreno-Mendoza*
Affiliation:
Department of Cell Biology and Physiology, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, Ciudad Universitaria, 04510México, DF, México
*
Author for correspondence: Norma Moreno-Mendoza. Department of Cell Biology and Physiology, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, Ciudad Universitaria, Apartado Postal 70228 México, D.F.04510México. Tel: +52 55 56 22 38 66. Fax: +52 55 55 50 38 93. E-mail: [email protected]

Summary

It is widely accepted that the oocyte plays a very active role in promoting the growth of the follicle by directing the differentiation of granulosa cells and secreting paracrine growth factors. In turn, granulosa cells regulate the development of the oocytes, establishing close bidirectional communication between germ and somatic cells. The presence of cortical cells with morphological characteristics, similar to primordial germ cells that express specific germline markers, stem cells and cell proliferation, known as adult cortical germ cells (ACGC) have been reported in phyllostomid bats. Using magnetic cell separation techniques, dissociation–cellular re-aggregation and organ culture, the behaviour of oocytes and ACGC was analyzed by interacting in vitro with mouse ovarian cells. Bat ACGC was mixed with disaggregated ovaries from a transgenic mouse that expressed green fluorescent protein. The in vitro reconstruction of the re-aggregates was evaluated. We examined the viability, integration, cellular interaction and ovarian morphogenesis by detecting the expression of Vasa, pH3, Cx43 and Laminin. Our results showed that the interaction between ovarian cells is carried out in the adult ovary of two species, without them losing their capacity to form follicular structures, even after having been enzymatically dissociated.

Type
Research Article
Copyright
© Cambridge University Press 2020

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References

Anthony, EL (1988) Age determination in bats. In Ecological and Behavioral Methods for the Study of Bats (ed. Kunz, HT), pp. 4758. Washington DC: Smithsonian Institution Press.Google Scholar
Antonio-Rubio, RN, Porras-Gómez, TJ and Moreno-Mendoza, N (2013) Identification of cortical germ cells in adult ovaries from three phyllostomid bats: Artibeus jamaicensis, Glossophaga soricina and Sturnira lilium. Reprod Fertil Dev 25, 825–36.CrossRefGoogle ScholarPubMed
Arita, HT and Ceballos, G (1997) The mammals of Mexico: distribution and conservation status. Rev Mex Mastozool 2, 3371.Google Scholar
Bui, HT, Van Thuan, N, Kwon, DN, Choi, YJ, Kang, MH, Han, JW, Kim, T and Kim, JH (2014) Identification and characterization of putative stem cells in the adult pig ovary. Development 141, 2235–44.CrossRefGoogle ScholarPubMed
Cretekos, CJ, Wang, Y, Green, ED, Martin, JF, Rasweiler, JJ IV and Behringer, RR (2008) Regulatory divergence modifies limb length between mammals. Genes Dev 22, 141–51.CrossRefGoogle ScholarPubMed
Eppig, JJ (1991) Intercommunication between mammalian oocytes and companion somatic cells. BioEssays 13, 569–74.CrossRefGoogle ScholarPubMed
Eppig, JJ and Wigglesworth, K (2000) Development of mouse and rat oocytes in chimeric reaggregated ovaries after interspecific exchange of somatic and germ cell components. Biol Reprod 63, 1014–23.CrossRefGoogle ScholarPubMed
Eppig, JJ, Wigglesworth, K and Pendola, FL (2002) The mammalian oocyte orchestrates the rate of ovarian follicular development. Proc Natl Acad Sci USA 99, 2890–4.CrossRefGoogle ScholarPubMed
Erickson, GF and Shimasaki, S (2000) The role of the oocyte in folliculogenesis. Trends Endocrinol Metab 11, 193–8.CrossRefGoogle ScholarPubMed
Esmaeilian, Y, Dedeoglu, BG, Atalay, A and Erdemli, E (2012) Investigation of stem cells in adult and prepubertal mouse ovaries. Adv Biosci Biotechnol 3, 936–44.CrossRefGoogle Scholar
Gilchrist, RB, Ritter, LJ and Armstrong, DT (2004) Oocyte-somatic cell interactions during follicle development in mammals. Anim Reprod Sci 82–83, 431–46.CrossRefGoogle ScholarPubMed
Gougeon, A and Chainey, GB (1987) Morphometric studies of small follicles in ovaries of women of different ages. J Reprod Fertil 81, 433–42.CrossRefGoogle ScholarPubMed
Ikawa, M, Kominami, K, Yoshimura, Y, Tanaka, K, Nishimune, Y and Okabe, M (1995) Green fluorescent protein as a marker in transgenic mice. Dev Growth Differ 37, 455–9.CrossRefGoogle Scholar
IUCN (2012) International union for conservation of nature. Red list of threatened species, version 2011.2. Available at www.iucnredlist.org.Google Scholar
Jiménez, R (2009) Ovarian organogenesis in mammals: mice cannot tell us everything. Sex Dev 3, 291301.CrossRefGoogle ScholarPubMed
Johnson, J, Canning, J, Kaneko, T, Pru, JK and Tilly, JL (2004) Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature 428, 145–50.CrossRefGoogle ScholarPubMed
Karnovsky, MJ (1965) A formaldehyde–glutaraldehyde fixative high osmolality for use in electron microscopy. J Cell Biol 27, 137A.Google Scholar
Matzuk, MM, Burns, KH, Viveiros, MM and Eppig, JJ (2002) Intercellular communication in the mammalian ovary: oocytes carry the conversation. Science 296, 2178–80.CrossRefGoogle ScholarPubMed
Medellín, RA, Arita, HT and Sanchez, O (2008) Morfología externa de un murciélago. Phyllostomidae. In Identificación de los Murciélagos de México. Clave de Campo, 2nd edn, pp. 3250. Ciudad de México, Instituto de Ecología, UNAM.Google Scholar
Monniaux, D (2016) Driving folliculogenesis by the oocyte-somatic cell dialog: lessons from genetic models. Theriogenology 86, 4153.CrossRefGoogle ScholarPubMed
Moscona, AA (1957) The development in vitro of chimeric aggregates of dissociated embryonic chick and mouse cells. Proc Natl Acad Sci USA 43, 184–94.CrossRefGoogle ScholarPubMed
Murphy, WJ, Pevzner, PA and O’Brien, SJ (2004) Mammalian phylogenomics comes of age. Trends Genet 20, 631–9.CrossRefGoogle ScholarPubMed
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.Google Scholar
Ol, A, Tasaki, H, Munakata, Y, Shirasuna, K, Kuwayama, T and Iwata, H (2015) Effects of reaggregated granulosa cells and oocytes derived from early antral follicles on the properties of oocytes grown in vitro. J Reprod Dev 61, 191–7.Google Scholar
Picton, HM (2001) Activation of follicle development: the primordial follicle. Theriogenology 55, 1193–210.CrossRefGoogle ScholarPubMed
Rasweiler, JJ IV and Badwaik, NK (2000). Anatomy and physiology of the female tract. In Reproductive Biology of Bats. (eds Crichton, EG and Krutzsch, PH), pp. 157219. London: Academic Press.CrossRefGoogle Scholar
Rinaldini, LM (1959) An improved method for isolation and quantitative cultivation of embryonic cells. Exp Cell Res 16, 477505.CrossRefGoogle ScholarPubMed
Saitou, M, Barton, SC and Surani, MA (2002) A molecular programme for the specification of germ cell fate in mice. Nature 418, 293300.CrossRefGoogle ScholarPubMed
Sato, M, Jimura, 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, 91–4.CrossRefGoogle ScholarPubMed
Song, K, Ma, W, Huang, C, Ding, J, Cui, D and Zhang, M (2016) Expression pattern of mouse Vasa homologue (MVH) in the ovaries of C57BL/6 female mice. Med Sci Monit 22, 2656–63.CrossRefGoogle ScholarPubMed
Štefková, K, Procházková, J and Pacherník, J (2015) Alkaline phosphatase in stem cells. Stem Cell Int 2015, 628368.Google ScholarPubMed
Stimpfel, M, Skutella, T, Cvjeticanin, B, Meznaric, M, Dovc, P, Novakovic, S, Cerkovnik, P, Vrtacnik-Bokal, E and Virant-Klun, I (2013) Isolation, characterization and differentiation of cells expressing pluripotent/multipotent markers from adult human ovaries. Cell Tissue Res 354, 593607.CrossRefGoogle ScholarPubMed
Thomas, FH and Vanderhyden, BC (2006) Oocyte–granulosa cell interactions during mouse follicular development: regulation of kit ligand expression and its role in oocyte growth. Reprod Biol Endocrinol 4, 19.CrossRefGoogle ScholarPubMed
Wongtrakoongate, P, Jones, M, Gokhale, PJ and Andrews, PW (2013) STELLA facilitates differentiation of germ cell and endodermal lineages of human embryonic stem cells. PLoS One 8, e56893.CrossRefGoogle ScholarPubMed
Young, F, Drummond, J, Akers, E, Bartle, L, Kennedy, D and Asaduzzaman, M (2017) Effects of ovarian disaggregation on adult murine follicle yield and viability. Reprod Fertil Dev 29, 2400–10.CrossRefGoogle ScholarPubMed
Zenzes, MT and Engel, W (1981) The capacity of ovarian cells of the postnatal rat to reorganize into histiotypic structures. Differentiation 19, 199202.CrossRefGoogle ScholarPubMed
Zhang, D, Fouad, H, Zoma, WD, Salama, SA, Wentz, MJ and Al-Hendy, A (2008) Expression of stem and germ cell markers within nonfollicle structures in adult mouse ovary. Reprod Sci 15, 139–46.CrossRefGoogle ScholarPubMed
Zuckerman, S (1951) The number of oocytes in the mature ovary. Recent Prog Horm Res 6, 63108.Google Scholar