Hostname: page-component-669899f699-cf6xr Total loading time: 0 Render date: 2025-04-26T19:00:49.570Z Has data issue: false hasContentIssue false

Identification of the proliferative activity of germline progenitor cells in the adult ovary of the bat Artibeus jamaicensis

Published online by Cambridge University Press:  24 October 2024

Tania J. Porras-Gómez
Affiliation:
Department of Cell Biology and Phisiology, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, Apartado Postal 70228 Ciudad de México 04510, Mexico
Norma Moreno-Mendoza*
Affiliation:
Department of Cell Biology and Phisiology, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, Apartado Postal 70228 Ciudad de México 04510, Mexico
*
Corresponding author: Norma Moreno-Mendoza; Email: [email protected]

Summary

Until a few years ago, it was assumed that oocyte renewal did not take place in the ovary of adult organisms; however, the existence of germline progenitor cells (GPCs), which renew the ovarian follicular reserve, has now been documented in mammals. Specifically, in the adult ovary of bats, the presence of cells located in the cortical region with characteristics similar to GPCs, called adult cortical germ cells (ACGC), has been observed. One of the requirements that a GPC must fulfil is to be able to proliferate mitotically, so the evaluation of cell proliferation in ACGC is of utmost importance in order to be able to relate them to a parental lineage. Currently, there are several methods to determine cell proliferation, including BrdU labelling or the use of endogenous proliferation markers. Thus, the aim of this work was to evaluate the proliferative activity of ACGC in the adult ovary of the bat Artibeus jamaicensis, using different proliferation markers and correlating these with the protein expression of the transcription factor Oct4 and the germ line marker Ddx4. We found that the expression pattern of the proliferation markers BrdU, PCNA, Ki-67 and pH3 occurs at different times of the cell cycle, so co-localization of two or more of these markers allows us to identify proliferating cells. This allowed us to identify ACGC with proliferative capacity in the adult ovary of A. jamaicensis, suggesting that GPCs renew the follicle reserve during the adult life of the organism.

Type
Research Article
Copyright
© The Author(s), 2024. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Alison, M.R. (1995) Assessing cellular proliferation: what’s worth measuring? Human Experimetal Toxicology 14, 935944. doi: 10.1177/096032719501401201 CrossRefGoogle ScholarPubMed
Antonio-Rubio, N.R., Porras-Gómez, T.J. and Moreno-Mendoza, N. (2013) Identification of cortical germ cells in adult ovaries from three phyllostomid bats: Artibeus jamaicensis, Glossophaga soricina and Sturnira lilium. Reproduction Fertility and Development 25, 825836. doi: 10.1071/RD12126 CrossRefGoogle ScholarPubMed
Bravo, R. and Macdonald, B. (1987) Existence of two populations of cyclin/proliferating cell nuclear antigen during the cell cycle: association with DNA replication sites. Journal of Cell Biology 105, 15491554. doi: 10.1083/jcb.105.4.1549 CrossRefGoogle ScholarPubMed
Bukovsky, A., Caudle, M.R., Svetlikova, M. and Upadhyaya, N.B. (2004) Origin of germ cells and formation of new primary follicles in adult human ovaries. Reproductive Biology Endocrinology 2, 20. doi: 10.1186/1477-7827-2-2 CrossRefGoogle ScholarPubMed
Coltrera, M.D. and Gown, A.M. (1991) PCNA/cyclin expression and BrdU uptake define different subpopulations in different cell lines. Journal of Histochemistry and Cytochemistry 39, 2330. doi: 10.1177/39.1.1670579 CrossRefGoogle ScholarPubMed
Darzynkiewicz, Z. and Traganos, F. (1982). RNA content and chromatin structure in cycling and noncycling cell populations studied by flow cytometry. In: Padilla, P. and McCarty, K.S. (eds), Genetic Expression in the Cell Cycle. New York: Academic Press, pp. 103128 CrossRefGoogle Scholar
Drewinko, B., Yang, L.Y., Barlogie, B. and Trujillo, J.M. (1984) Cultured human tumour cells may be arrested in all stages of the cycle during stationary phase: demonstration of quiescent cells in G1, S and G2 phase. Cell and Tissue Kinetics 17, 453463. doi: 10.1111/j.1365-2184.1984.tb00604.x Google ScholarPubMed
Endl, E. and Gerdes, J. (2000) The Ki-67 protein: fascinating forms and an unknown function. Experimental Cell Research 257, 231237. doi: 10.1006/excr.2000.4888 CrossRefGoogle Scholar
Engstrom, Y., Eriksson, S., Jildevik, I., Skog, S., Thelander, L. and Tribukait, B. (1985) Cell cycle-dependent expression of mammalian ribonucleotide reductase. Differential regulation of the two subunits. Journal of Biological Chemistry 260, 91149116.CrossRefGoogle ScholarPubMed
Foley, J.F., Dietrich, D.R., Swenberg, J.A. and Maronpot, R.R. (1991) Detection and duration of proliferating cell nuclear antigen (PCNA) in rat tissue by an improved immunohistochemical procedure. Journal of Histotechnology 14, 237241. doi: 10.1179/his.1991.14.4.237 CrossRefGoogle Scholar
Fujiwara, Y., Komiya, T., Kawabata, H., Sato, M., Fujimoto, H., Furusawa, M., Noce, T. (1994) Isolation of a DEAD-family protein gene that encodes a murine homolog of Drosophila vasa and its specific expression in germ cell linaje. Proceedings of the National Academy of Sciences 91, 1225812262. doi: 10.1073/pnas.91.25.12258 CrossRefGoogle Scholar
Gerdes, J., Lemke, H., Baisch, H., Wacker, H. H., Schab, U., Stein, H. (1984) Cell cycle analysis of a cell proliferation associated human nuclear antigen defined by the monoclonal antibody Ki-67. Journal of Immunology 133, 17101715. PMID: 6206131 CrossRefGoogle ScholarPubMed
Gerdes, J., Schwab, U., Lemke, H., Stein, H. (1983) Production of a mouse monoclonal antibody reactive with a human nuclear antigen associated with cell proliferation. International Journal of Cancer 31, 1320. doi: 10.1002/ijc.2910310104 CrossRefGoogle ScholarPubMed
Gerlach, C., Sakkab, Dy., Scholzen, T., Dassler, R., Alison, M. R., Gerdes, J. (1997) Ki-67 expression during rat liver regeneration after partial hepatectomy. Hepatology 26, 573578. doi: 10.1002/hep.510260307 CrossRefGoogle ScholarPubMed
Goldsworthy, T.L., Morgan, K.T., Popp, J.A. and Butterworth, B.E. (1991) Guidelines formeasuring chemically-induced cell proliferation in specific rodent target organs. In Butterworth, B.E., Slaga, T.J. (Eds), Chemically-induced Cell Proliferation: Implications for Risk Assessment. New York: Wiley-Liss, pp. 253284.Google Scholar
Gould, E., Gross, C.G. (2002) Neurogenesis in adult mammals: some progress and problems. Journal of Neuroscience 22, 619623. doi: 10.1523/JNEUROSCI.22-03-00619.2002 CrossRefGoogle Scholar
Gratzner, H.G. (1982) Monoclonal antibody to 5-bromo and 5-iododeoxyuridine: A new reagent for detection of DNA replication. Science 218, 474475. doi: 10.1126/science.7123245 CrossRefGoogle ScholarPubMed
Greenspan, L.J., de Cuevas, M., Matunis, E. (2015) Genetics of gonadal stem cell renewal. Annual Review of Cell and Developmental Biology 31, 291315. doi: 10.1146/annurev-cellbio-100913-013344 CrossRefGoogle ScholarPubMed
Gurley, L.R., DÁnna, J.A., Barham, S.S., Deaven, L.L. and Tobey, R.A. (1978) Histone Phosphorylation and chromatin structure during mitosis in Chinese hamster cells. European Journal of Biochemestry 84, 115. doi: 10.1111/j.1432-1033.1978.tb12135.x CrossRefGoogle ScholarPubMed
Gwynn, I.A. (2001) Preservation of tissue for immunocytochemical studies. In: Beesley, J.E. (ed), Immunocytochemistry and In Situ Hybridization in the Biomedical Sciences. Berlín: Birkhäuser, pp. 629.CrossRefGoogle Scholar
Hall, P.A., Levison, D.A, Woods, A.L., Yu, C.C., Kellock, D.B., Watkins, J.A. and Barnes, D.M. (1990) Proliferating cell nuclear antigen (PCNA) immunolocalization in paraffin sections: an index of cell proliferation with evidence of deregulated expression in some neoplasms. Journal of Pathology 162, 285294. doi: 10.1002/path.1711620403 CrossRefGoogle ScholarPubMed
Hendzel, M.J., Wei, Y., Mancini, M.A., Van Hooser, A., Ranalli, T., Brinkley, B.R., Bazett-Jones, D.P. and Allis, C.D. (1997) Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spread in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106, 348360. doi: 10.1007/s004120050256 CrossRefGoogle Scholar
IUCN. (2016). International union for conservation of nature. Red list of threatened species, version 2011.2. Available in: www.iucnredlist.org.Google Scholar
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, 145150. doi: 10.1038/nature02316 CrossRefGoogle ScholarPubMed
Kee, N., Sivalingam, S., Boonstra, R. and Wojtowicz, J.M. (2002) The utility of Ki-67 and BrdU as proliferative markers of adult neurogenesis. Journal of Neuroscience Methods 115, 97105. doi: 10.1016/s0165-0270(02)00007-9 CrossRefGoogle ScholarPubMed
Kerr, C.L., Hill, C.M., Blumenthal, P.D. and Gearhart, J.D. (2008) Expression of pluripotent stem cell markers in the human fetal ovary. Human Reproduction 23, 589599. doi: 10.1093/humrep/dem411. Epub 2008 Jan 17. PMID: 18203707 CrossRefGoogle ScholarPubMed
Kolb, B., Perdersen, B., Ballermann, M., Gibb, R. and Whishaw, I.Q. (1999) Embryonic and postnatal injections of bromodeoxyuridine produce age-dependent morphological and behavioral abnormalities. Journal of Neuroscience 19, 23372346. doi: 10.1523/JNEUROSCI.19-06-02337.1999 CrossRefGoogle ScholarPubMed
Kurki, P., Ogata, K. and Tan, E.M. (1988) Monoclonal antibodies to proliferating cell nuclear antigen (PCNA)/cyclin as probes for proliferating cells by immunofluorescence microscopy and flow cytometry. Journal of Immunology Methods 109, 4959. doi: 10.1016/0022-1759(88)90441-3 CrossRefGoogle ScholarPubMed
Kurki, P., Vanderlaan, M., Dolbeare, F., Gray, J. and Tan, E.M. (1986) Expression of proliferating cell nuclear antigen (PCNA)/cyclin during the cell cycle. Experimental Cell Research 166, 209219. doi: 10.1016/0014-4827(86)90520-3 CrossRefGoogle ScholarPubMed
Ladstein, R.G., Bachmann, I.M., Straume, O. and Akslen, L.A. (2010) Ki-67 expression is superior to mitotic count and novel proliferation markers PHH3, MCM4 and mitosin as a prognostic factor in thick cutaneous melanoma. BMC Cancer 10, 140. https://doi: 10.1186/1471-2407-10-140. PMID: 20398247; PMCID: PMC2868809CrossRefGoogle ScholarPubMed
Lazebnik, Y.A., Medvedeva, N.D. and Zenin, V.V. (1991) Reversible G2 block in the cell cycle of Ehrlich ascites carcinoma cells. Experimental Cell Research 195, 247254. doi: 10.1016/0014-4827(91)90524-x CrossRefGoogle ScholarPubMed
Littleton, R.J., Baker, G.M., Soomro, I.N., Adams, R.L. and Whimster, W.F. (1991) Kinetic aspects of Ki-67 antigen expression in a normal cell line. Virchows Archiv B Cell Pathology Including Molecular Pathology 60, 1519. doi: 10.1007/BF02899522. PMID: 1673272 CrossRefGoogle Scholar
Matsumoto, K., Moriuchi, T., Koji, T. and Nakane, P.K. (1987) Molecular cloning of cDNA coding for rat proliferating cell nuclear antigen (PCNA)/cyclin. EMBO Journal 6, 637642. doi: 10.1002/j.1460-2075.1987.tb04802.x CrossRefGoogle ScholarPubMed
Medellin, R.A., Arita, H.T. and Sanchez, O. (2008) Morfología externa de un murciélago. Phyllostomidae. In: Identificación de los Murciélagos de México. Clave de Campo 2nd ed, pp. 3250. Ciudad de México, Instituto de Ecología, UNAM.Google Scholar
Memo, M. (2006). Intracellular pathways involved in DNA damage and repair to neuronal apoptosis. In: Srivastava, R. (Ed.) Apoptosis, Cell Signaling, and Human Diseases. Humana Press, pp. 335346. doi: 10.1007/978-1-59745-199-4_16 Google Scholar
Miller, B., Reid, F., Arroyo-Cabrales, J., Cuarón, A.D. and Grammont, P.C. (2016). Artibeus jamaicensis. The IUCN Red List of Threatened Species. e.T88109731A21995883Google Scholar
Miyachi, K., Fritzler, M.J. and Tan, E.M. (1978) Autoantibody to a nuclear antigen in proliferating cells. Journal of Immunology 121, 22282234. PMID: 102692 CrossRefGoogle ScholarPubMed
Morris, G.F. and Mathews, M.B. (1989) Regulation of proliferating cell nuclear antigen during the cell cycle. Journal of Biological Chemistry 264, 1385613864. PMID: 2569465 CrossRefGoogle ScholarPubMed
Muskhelishvili, L., Latendresse, J.R., Kodell, R.L. and Henderson, E.B. (2003) Evaluation of cell proliferation in rat tissues with BrdU, PCNA Ki-67(MIB-5) immunohistochemistry and in situ hybridization for histone mRNA. Journal of Histochemistry and Cytochemistry 51, 16811688. doi: 10.1177/002215540305101212 CrossRefGoogle ScholarPubMed
National Research Council. (1996). Guide for the Care and Use of Laboratory Animals, Bethesda, MD: Institute for Laboratory Animal Research (ILAR) of the National Academy of Science..Google Scholar
Noce, T., Okamoto-Ito, S. and Tsunekawa, N. (2001) Vasa Homolog genes in mammalian germ cell development. Cell Structure and Function 26, 131136. doi: 10.1247/csf.26.131 CrossRefGoogle ScholarPubMed
Paulson, J.R. and Taylor, S.S. (1982) Phosphorylation of histones 1 and 3 nonhistone high mobility group 14 by an endogenous kinase in HeLa Metaphase chromosomes. Journal of Biological Chemistry 257, 60646072. PMID: 6281254 CrossRefGoogle Scholar
Porras-Gómez, T.J. and Moreno-Mendoza, N. (2017) Neo-ogenesis in mammals. Zygote 25, 404422. doi: 10.1017/S0967199417000363 CrossRefGoogle ScholarPubMed
Saitou, M. and Yamaji, M. (2012) Primordial germ cells in mice. Cold Spring Harbor Perspectives in Biology 4(11), a008375. doi: 10.1101/cshperspect.a008375 CrossRefGoogle ScholarPubMed
Schlüter, C., Duchrow, M., Wohlenberg, C., Becker, M.H., Key, G., Flad, H.D. and Gerdes, J. (1993) The cell proliferation-associated antigen of antibody Ki-67: a very large, ubiquitous nuclear protein with numerous repeated elements, representing a new kind of cell cycle-mantaining proteins. Journal of Cell Biology 123, 513522. doi: 10.1083/jcb.123.3.513 CrossRefGoogle ScholarPubMed
Scholzen, T. and Gerdes, J. (2000). The Ki-67 protein: from the known and the unknown. Journal of Cell Physiology 182, 311322. doi: 10.1002/(SICI)1097-4652(200003)182:3<311::AID-JCP1>3.0.CO;2-93.0.CO;2-9>CrossRefGoogle ScholarPubMed
Schwarting, R. (1993) Little missed markers and Ki-67. Laboratory Investigation 68, 597599. PMID: 8099985 Google ScholarPubMed
Somanathan, S., Suchyna, T.M., Siegel, A.J. and Berezney, R. (2001) Targeting of PCNA to sites of DNA replication in the mammalian cell nucleus. Journal of Cellular Biochemistry 81, 5667. doi: 10.1002/1097-4644(20010401)81:1<56::aid-jcb1023>3.0.co;2-#3.0.CO;2-#>CrossRefGoogle ScholarPubMed
Takahashi, T. and Caviness, V.S. Jr (1993) PCNA-binding to DNA at the G1/S transition in proliferating cells of the developing cerebral wall. Journal of Neurocytology 22, 10961102. doi: 10.1007/BF01235751 CrossRefGoogle ScholarPubMed
Tanaka, R., Tainaka, M., Ota, T., Mizuguchi, N., Kato, H., Urabe, S., Chen, Y., Fustin, J.M., Yamaguchi, Y., Doi, M., Hamada, S. and Okamura, H. (2011) Accurate determination of S-phase fraction in proliferative cells by dual fluorescence and peroxidase immunohistochemistry with 5-bromo-2’-deoxyuridine (BrdU) and Ki67 antibodies. Journal of Histochemistry and Cytochemistry 59, 791798. doi: 10.1369/0022155411411090 CrossRefGoogle ScholarPubMed
Tanapat, P., Hastings, N.B., Reeves, A.J. and Gould, E. (1999) Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. Journal of Neuroscience 19, 57925801. doi: 10.1523/JNEUROSCI.19-14-05792.1999 CrossRefGoogle ScholarPubMed
Telfer, E.E. and Anderson, R.A. (2019) The existence and potential of germline stem cells in the adult mammalian ovary. Climacteric 22(1), 2226. doi: 10.1080/13697137.2018.1543264 CrossRefGoogle ScholarPubMed
Thavarajah, R., Mudimbaimannar, V.K., Elizabeth, J., Rao, U.K. and Ranganathan, K. (2012) Chemical and physical basics of routine formaldehyde fixation. Journal of Oral and Maxillofacial Pathology 16, 400405. doi: 10.4103/0973-029X.102496 CrossRefGoogle ScholarPubMed
Valero, J., Weruaga, E., Murias, A.R., Recio, J.S. and Alonso, J.R. (2005) Proliferation markers in the adult rodent brain: Bromodeoxyuridine and proliferating cell nuclear antigen. Brain Research Protocols 15, 127134. doi: 10.1016/j.brainresprot.2005.06.001.CrossRefGoogle ScholarPubMed
Wei, W., Nurse, P. and Broek, D. (1993) Yeast cells can enter a quiescent state through G1, S, G2, or M phase of the cell cycle. Cancer Research 53, 18671870. PMID: 8467507 Google ScholarPubMed
Whitfield, M.L., George, L.K., Grant, G.D. and Perou, C.M. (2006) Common markers of proliferation. Nature Reviews Cancer 6, 99106. doi: 10.1038/nrc1802 CrossRefGoogle ScholarPubMed
Zacchetti, A., van Garderen, E., Teske, E., Nederbragt, H., Dierendonck, J.H. and Rutteman, G.R. (2003) Validation of the use of proliferation markers in canine neoplastic and non-neoplastic tissues: comparison of KI-67 and proliferating cell nuclear antigen (PCNA) expression versus in vivo bromodeoxyuridine labelling by immunohistochemistry. APMIS 111, 430438. doi: 10.1034/j.1600-0463.2003.t01-1-1110208.x CrossRefGoogle ScholarPubMed
Zhang, G., Gibbs, E., Kelman, Z., O’Donnell, M. and Hurwitz, J. (1999) Studies on the interactions between human replication factors C human proliferating cell nuclear antigen. Proceedings of the National Academy of Sciences of the United States of America 96, 18691874. doi: 10.1073/pnas.96.5.1869 CrossRefGoogle Scholar
Zhu, H., Dahlstrom, A. and Hansson, H.A. (2005) Characterization of cell proliferation in the adult dentate under normal conditions and after kainate induced seizures using ribonucleotide reductase and BrdU. Brain Research 1036, 717. doi: 10.1016/j.brainres.2004.12.053 CrossRefGoogle ScholarPubMed
Zhu, H., Wang, Z.Y. and Hansson, H.A. (2003) Visualization of proliferating cells in the adult mammalian brain with the aid of ribonucleotide reductase. Brain Research 977, 180189. doi: 10.1016/s0006-8993(03)02627-1 CrossRefGoogle ScholarPubMed
Zuckerman, S. (1951) The number of oocytes in the mature ovary. Recent Progress in Hormone Research 6, 63108.Google Scholar