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The Progresses of Spermatogonial Stem Cells Sorting Using Fluorescence-Activated Cell Sorting

  • Yihui Cai
  • Jingjing Wang
  • Kang ZouEmail author
Article
  • 77 Downloads

Abstract

In recent years, the research on stem cells has been more and more in-depth, and many achievements have been made in application. However, due to the small number of spermatogonial stem cells (SSCs) and deficiency of efficient markers, it is difficult to obtain very pure SSCs, which results in the research on them being hindered. In fact, many methods have been developed to isolate and purify SSCs, but these methods have their shortcomings. Fluorescence-activated cell sorting (FACS), as a method to enrich SSCs with the help of specific surface markers, has the characteristics of high efficiency and accuracy in enrichment of SSCs, thus it is widely accepted as an effective method for purification of SSCs. This review summarizes the recent studies on the application of FACS in SSCs, and introduces some commonly used markers of effective SSCs sorting, aiming to further optimize the FACS sorting method for SSCs, so as to promote the research of germline stem cells and provide new ideas for the research of reproductive biology.

Keywords

Spermatogonial stem cells Purification Surface markers Fluorescence-activated cell sorting 

Notes

Acknowledgements

This study was supported by the Fundamental Research Funds for the Central Universities in China (KYDS201807 and KYTZ201602).

Compliance with Ethical Standards

Conflict of Interest

The authors have no potential conflicts of interest.

References

  1. 1.
    Phillips, B. T., Gassei, K., & Orwig, K. E. (2010). Spermatogonial stem cell regulation and spermatogenesis. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 365, 1663–1678.PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Lee, J., Kanatsu-Shinohara, M., Inoue, K., et al. (2007). Akt mediates self-renewal division of mouse spermatogonial stem cells. Development, 134, 1853–1859.PubMedCrossRefPubMedCentralGoogle Scholar
  3. 3.
    Kubota, H., Avarbock, M. R., & Brinster, R. L. (2003). Spermatogonial stem cells share some, but not all, phenotypic and functional characteristics with other stem cells. Proceedings of the National Academy of Sciences of the United States of America, 100, 6487–6492.PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Fayomi, A. P., & Orwig, K. E. (2018). Spermatogonial stem cells and spermatogenesis in mice, monkeys and men. Stem Cell Research, 29, 207–214.PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Lo, K. C., Brugh, V. M., Parker, M., & Lamb, D. J. (2005). Isolation and enrichment of murine spermatogonial stem cells using rhodamine 123 mitochondrial dye. Biology of Reproduction, 72, 767–771.PubMedCrossRefPubMedCentralGoogle Scholar
  6. 6.
    Buageaw, A., Sukhwani, M., Ben-Yehudah, A., et al. (2005). GDNF family receptor alpha1 phenotype of spermatogonial stem cells in immature mouse testes. Biology of Reproduction, 73, 1011–1016.PubMedCrossRefPubMedCentralGoogle Scholar
  7. 7.
    Kanatsu-Shinohara, M., Mori, Y., & Shinohara, T. (2013). Enrichment of mouse spermatogonial stem cells based on aldehyde dehydrogenase activity. Biology of Reproduction, 89, 140.PubMedCrossRefPubMedCentralGoogle Scholar
  8. 8.
    Lawson, K., & Pedersen, R. (1992). Clonal analysis of cell fate during gastrulation and early neurulation in the mouse. Ciba Foundation Symposia, 165, 3–26.PubMedPubMedCentralGoogle Scholar
  9. 9.
    Clermont, Y., & Perey, B. (1957). Quantitative study of the cell population of the seminiferous tubules in immature rats. The American Journal of Anatomy, 100, 241–267.PubMedCrossRefPubMedCentralGoogle Scholar
  10. 10.
    Yoshida, S., Sukeno, M., Nakagawa, T., et al. (2006). The first round of mouse spermatogenesis is a distinctive program that lacks the self-renewing spermatogonia stage. Development, 133, 1495–1505.PubMedCrossRefPubMedCentralGoogle Scholar
  11. 11.
    Cendron, M., Schned, A. R., & Ellsworth, P. I. (1998). Histological evaluation of the testicular nubbin in the vanishing testis syndrome. The Journal of Urology, 160, 1161–1162; discussion 3.PubMedCrossRefPubMedCentralGoogle Scholar
  12. 12.
    Schofield, R. (1978). The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells, 4, 7–25.PubMedPubMedCentralGoogle Scholar
  13. 13.
    Xie, T., & Spradling, A. C. (2000). A niche maintaining germ line stem cells in the Drosophila ovary. Science, 290, 328–330.PubMedCrossRefPubMedCentralGoogle Scholar
  14. 14.
    Tran, J., Brenner, T. J., & DiNardo, S. (2000). Somatic control over the germline stem cell lineage during Drosophila spermatogenesis. Nature, 407, 754–757.PubMedCrossRefPubMedCentralGoogle Scholar
  15. 15.
    Kiger, A. A., White-Cooper, H., & Fuller, M. T. (2000). Somatic support cells restrict germline stem cell self-renewal and promote differentiation. Nature, 407, 750–754.PubMedCrossRefPubMedCentralGoogle Scholar
  16. 16.
    Monesi, V. (1962). Autoradiographic study of DNA synthesis and the cell cycle in spermatogonia and spermatocytes of mouse testis using tritiated thymidine. The Journal of Cell Biology, 14, 1–18.PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Huckins, C. (1971). The spermatogonial stem cell population in adult rats. I. Their morphology, proliferation and maturation. The Anatomical Record, 169, 533–557.PubMedCrossRefPubMedCentralGoogle Scholar
  18. 18.
    Meistrich, M. L. (1993). Effects of chemotherapy and radiotherapy on spermatogenesis. European Urology, 23, 136–141; discussion 42.PubMedCrossRefPubMedCentralGoogle Scholar
  19. 19.
    de Rooij, D. G. (1973). Spermatogonial stem cell renewal in the mouse. I. Normal situation. Cell and Tissue Kinetics, 6, 281–287.PubMedPubMedCentralGoogle Scholar
  20. 20.
    Komeya, M., & Ogawa, T. (2015). Spermatogonial stem cells: Progress and prospects. Asian Journal of Andrology, 17, 771–775.PubMedPubMedCentralGoogle Scholar
  21. 21.
    Davis, J. C., & Schuetz, A. W. (1975). Separation of germinal cells from immature rat testes by sedimentation at unit gravity. Experimental Cell Research, 91, 79–86.PubMedCrossRefPubMedCentralGoogle Scholar
  22. 22.
    Romrell, L. J., Bellvé, A. R., & Fawcett, D. W. (1976). Separation of mouse spermatogenic cells by sedimentation velocity. A morphological characterization. Developmental Biology, 49, 119–131.PubMedCrossRefPubMedCentralGoogle Scholar
  23. 23.
    Bellvé, A. R., Cavicchia, J. C., Millette, C. F., O'Brien, D. A., Bhatnagar, Y. M., & Dym, M. (1977). Spermatogenic cells of the prepuberal mouse. Isolation and morphological characterization. The Journal of Cell Biology, 74, 68–85.PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Meistrich, M. L. (1977). Separation of spermatogenic cells and nuclei from rodent testes. Methods in Cell Biology, 15, 15–54.PubMedCrossRefPubMedCentralGoogle Scholar
  25. 25.
    Bucci, L. R., Brock, W. A., Johnson, T. S., & Meistrich, M. L. (1986). Isolation and biochemical studies of enriched populations of spermatogonia and early primary spermatocytes from rat testes. Biology of Reproduction, 34, 195–206.PubMedCrossRefPubMedCentralGoogle Scholar
  26. 26.
    Hermann, B., Sukhwani, M., Simorangkir, D., Chu, T., Plant, T., & Orwig, K. (2009). Molecular dissection of the male germ cell lineage identifies putative spermatogonial stem cells in rhesus macaques. Human Reproduction, 24, 1704–1716.PubMedCrossRefPubMedCentralGoogle Scholar
  27. 27.
    Valli, H., Sukhwani, M., Dovey, S. L., et al. (2014). Fluorescence- and magnetic-activated cell sorting strategies to isolate and enrich human spermatogonial stem cells. Fertility and Sterility, 102, 566–80.e7.PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Sánchez-Luengo, M., Rovira, M., Serrano, M., Fernandez-Marcos, P. J., & Martinez, L. (2017). Analysis of the advantages of cis reporters in optimized FACS-Gal. Cytometry. Part A, 91, 721–729.CrossRefGoogle Scholar
  29. 29.
    Givan, A. L. (2011). Flow cytometry: An introduction. Methods in Molecular Biology, 699, 1–29.PubMedCrossRefPubMedCentralGoogle Scholar
  30. 30.
    Maciorowski, Z., Chattopadhyay, P. K., & Jain, P. (2017). Basic multicolor flow Cytometry. Current Protocols in Immunology, 117, 5.4.1–5.4.38.CrossRefGoogle Scholar
  31. 31.
    Ortega-Ferrusola, C., Gil, M. C., Rodríguez-Martínez, H., Anel, L., Peña, F. J., & Martín-Muñoz, P. (2017). Flow cytometry in Spermatology: A bright future ahead. Reproduction in Domestic Animals, 52, 921–931.PubMedCrossRefPubMedCentralGoogle Scholar
  32. 32.
    Smith, L. G., Weissman, I. L., & Heimfeld, S. (1991). Clonal analysis of hematopoietic stem-cell differentiation in vivo. Proceedings of the National Academy of Sciences of the United States of America, 88, 2788–2792.PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Okada, S., Nakauchi, H., Nagayoshi, K., Nishikawa, S., Miura, Y., & Suda, T. (1992). In vivo and in vitro stem cell function of c-kit- and Sca-1-positive murine hematopoietic cells. Blood, 80, 3044–3050.PubMedCrossRefPubMedCentralGoogle Scholar
  34. 34.
    Shinohara, T., Orwig, K. E., Avarbock, M. R., & Brinster, R. L. (2000). Spermatogonial stem cell enrichment by multiparameter selection of mouse testis cells. Proceedings of the National Academy of Sciences of the United States of America, 97, 8346–8351.PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Brinster, R. L., & Avarbock, M. R. (1994). Germline transmission of donor haplotype following spermatogonial transplantation. Proceedings of the National Academy of Sciences of the United States of America, 91, 11303–11307.PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Brinster, R. L., & Zimmermann, J. W. (1994). Spermatogenesis following male germ-cell transplantation. Proceedings of the National Academy of Sciences of the United States of America, 91, 11298–11302.PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Shinohara, T., Avarbock, M. R., & Brinster, R. L. (1999). beta1- and alpha6-integrin are surface markers on mouse spermatogonial stem cells. Proceedings of the National Academy of Sciences of the United States of America, 96, 5504–5509.PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Ryu, B. Y., Orwig, K. E., Kubota, H., Avarbock, M. R., & Brinster, R. L. (2004). Phenotypic and functional characteristics of spermatogonial stem cells in rats. Developmental Biology, 274, 158–170.PubMedCrossRefPubMedCentralGoogle Scholar
  39. 39.
    Kanatsu-Shinohara, M., Toyokuni, S., & Shinohara, T. (2004). CD9 is a surface marker on mouse and rat male germline stem cells. Biology of Reproduction, 70, 70–75.PubMedCrossRefGoogle Scholar
  40. 40.
    Lassalle, B., Bastos, H., Louis, J. P., et al. (2004). 'Side Population' cells in adult mouse testis express Bcrp1 gene and are enriched in spermatogonia and germinal stem cells. Development, 131, 479–487.PubMedCrossRefPubMedCentralGoogle Scholar
  41. 41.
    Fujita, K., Ohta, H., Tsujimura, A., et al. (2005). Transplantation of spermatogonial stem cells isolated from leukemic mice restores fertility without inducing leukemia. The Journal of Clinical Investigation, 115, 1855–1861.PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Kanatsu-Shinohara, M., Morimoto, H., & Shinohara, T. (2012). Enrichment of mouse spermatogonial stem cells by melanoma cell adhesion molecule expression. Biology of Reproduction, 87, 139.PubMedCrossRefPubMedCentralGoogle Scholar
  43. 43.
    Di Persio, S., Saracino, R., Fera, S., et al. (2017). Spermatogonial kinetics in humans. Development, 144, 3430–3439.PubMedCrossRefPubMedCentralGoogle Scholar
  44. 44.
    Sohni, A., Tan, K., Song, H. W., et al. (2019). The neonatal and adult human testis defined at the single-cell level. Cell Reports, 26, 1501–17.e4.PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Park, H. J., Lee, W. Y., Park, C., Hong, K., & Song, H. (2019). CD14 is a unique membrane marker of porcine spermatogonial stem cells, regulating their differentiation. Scientific Reports, 9, 9980.PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Morimoto, H., Kanatsu-Shinohara, M., Orwig, K. E., & Shinohara, T. (2019). Expression and functional analyses of EPHA2 in mouse spermatogonial stem cells. Biology of Reproduction.Google Scholar
  47. 47.
    Tanaka, T., Kanatsu-Shinohara, M., Lei, Z., Rao, C. V., & Shinohara, T. (2016). The luteinizing hormone-testosterone pathway regulates mouse Spermatogonial stem cell self-renewal by suppressing WNT5A expression in Sertoli cells. Stem Cell Reports, 7, 279–291.PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Murphey, P., McLean, D. J., McMahan, C. A., Walter, C. A., & McCarrey, J. R. (2013). Enhanced genetic integrity in mouse germ cells. Biology of Reproduction, 88, 6.PubMedCrossRefPubMedCentralGoogle Scholar
  49. 49.
    Wu, X., Schmidt, J. A., Avarbock, M. R., et al. (2009). Prepubertal human spermatogonia and mouse gonocytes share conserved gene expression of germline stem cell regulatory molecules. Proceedings of the National Academy of Sciences of the United States of America, 106, 21672–21677.PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    von Kopylow, K., Kirchhoff, C., Jezek, D., et al. (2010). Screening for biomarkers of spermatogonia within the human testis: A whole genome approach. Human Reproduction, 25, 1104–1112.CrossRefGoogle Scholar
  51. 51.
    Kristensen, D. M., Nielsen, J. E., Skakkebaek, N. E., et al. (2008). Presumed pluripotency markers UTF-1 and REX-1 are expressed in human adult testes and germ cell neoplasms. Human Reproduction, 23, 775–782.PubMedCrossRefPubMedCentralGoogle Scholar
  52. 52.
    von Kopylow, K., Staege, H., Spiess, A. N., et al. (2012). Differential marker protein expression specifies rarefaction zone-containing human Adark spermatogonia. Reproduction, 143, 45–57.CrossRefGoogle Scholar
  53. 53.
    von Kopylow, K., Staege, H., Schulze, W., Will, H., & Kirchhoff, C. (2012). Fibroblast growth factor receptor 3 is highly expressed in rarely dividing human type A spermatogonia. Histochemistry and Cell Biology, 138, 759–772.CrossRefGoogle Scholar
  54. 54.
    Lim, J., Goriely, A., Turner, G. D., et al. (2011). OCT2, SSX and SAGE1 reveal the phenotypic heterogeneity of spermatocytic seminoma reflecting distinct subpopulations of spermatogonia. The Journal of Pathology, 224, 473–483.PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    He, Z., Kokkinaki, M., Jiang, J., Dobrinski, I., & Dym, M. (2010). Isolation, characterization, and culture of human spermatogonia. Biology of Reproduction, 82, 363–372.PubMedCrossRefPubMedCentralGoogle Scholar
  56. 56.
    Grisanti, L., Falciatori, I., Grasso, M., et al. (2009). Identification of spermatogonial stem cell subsets by morphological analysis and prospective isolation. Stem Cells, 27, 3043–3052.PubMedPubMedCentralGoogle Scholar
  57. 57.
    Zohni, K., Zhang, X., Tan, S. L., Chan, P., & Nagano, M. (2012). CD9 is expressed on human male germ cells that have a long-term repopulation potential after transplantation into mouse testes. Biology of Reproduction, 87, 27.PubMedCrossRefPubMedCentralGoogle Scholar
  58. 58.
    Aeckerle, N., Eildermann, K., Drummer, C., et al. (2012). The pluripotency factor LIN28 in monkey and human testes: A marker for spermatogonial stem cells? Molecular Human Reproduction, 18, 477–488.PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Kossack, N., Terwort, N., Wistuba, J., et al. (2013). A combined approach facilitates the reliable detection of human spermatogonia in vitro. Human Reproduction, 28, 3012–3025.PubMedCrossRefPubMedCentralGoogle Scholar
  60. 60.
    Izadyar, F., Wong, J., Maki, C., et al. (2011). Identification and characterization of repopulating spermatogonial stem cells from the adult human testis. Human Reproduction, 26, 1296–1306.PubMedCrossRefPubMedCentralGoogle Scholar
  61. 61.
    Dovey, S. L., Valli, H., Hermann, B. P., et al. (2013). Eliminating malignant contamination from therapeutic human spermatogonial stem cells. The Journal of Clinical Investigation, 123, 1833–1843.PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Conrad, S., Renninger, M., Hennenlotter, J., et al. (2008). Generation of pluripotent stem cells from adult human testis. Nature, 456, 344–349.PubMedCrossRefPubMedCentralGoogle Scholar
  63. 63.
    Williams, A. F. (1985). Immunoglobulin-related domains for cell surface recognition. Nature, 314, 579–580.PubMedCrossRefPubMedCentralGoogle Scholar
  64. 64.
    Seeger, R. C., Danon, Y. L., Rayner, S. A., & Hoover, F. (1982). Definition of a Thy-1 determinant on human neuroblastoma, glioma, sarcoma, and teratoma cells with a monoclonal antibody. Journal of Immunology, 128, 983–989.Google Scholar
  65. 65.
    Grosche, A., Hauser, A., Lepper, M. F., et al. (2016). The proteome of native adult Müller Glial cells from Murine Retina. Molecular & Cellular Proteomics, 15, 462–480.CrossRefGoogle Scholar
  66. 66.
    Craig, W., Kay, R., Cutler, R. L., & Lansdorp, P. M. (1993). Expression of Thy-1 on human hematopoietic progenitor cells. The Journal of Experimental Medicine, 177, 1331–1342.PubMedCrossRefPubMedCentralGoogle Scholar
  67. 67.
    Rege, T. A., & Hagood, J. S. (2006). Thy-1 as a regulator of cell-cell and cell-matrix interactions in axon regeneration, apoptosis, adhesion, migration, cancer, and fibrosis. The FASEB Journal, 20, 1045–1054.PubMedCrossRefPubMedCentralGoogle Scholar
  68. 68.
    Barboni, E., Gormley, A. M., Pliego Rivero, F. B., Vidal, M., & Morris, R. J. (1991). Activation of T lymphocytes by cross-linking of glycophospholipid-anchored Thy-1 mobilizes separate pools of intracellular second messengers to those induced by the antigen-receptor/CD3 complex. Immunology, 72, 457–463.PubMedPubMedCentralGoogle Scholar
  69. 69.
    Schrans-Stassen, B. H., van de Kant, H. J., de Rooij, D. G., & van Pelt, A. M. (1999). Differential expression of c-kit in mouse undifferentiated and differentiating type A spermatogonia. Endocrinology, 140, 5894–5900.PubMedCrossRefPubMedCentralGoogle Scholar
  70. 70.
    Wixler, V., Laplantine, E., Geerts, D., et al. (1999). Identification of novel interaction partners for the conserved membrane proximal region of alpha-integrin cytoplasmic domains. FEBS Letters, 445, 351–355.PubMedCrossRefPubMedCentralGoogle Scholar
  71. 71.
    Stingl, J., Eirew, P., Ricketson, I., et al. (2006). Purification and unique properties of mammary epithelial stem cells. Nature, 439, 993–997.PubMedCrossRefPubMedCentralGoogle Scholar
  72. 72.
    Lathia, J. D., Gallagher, J., Heddleston, J. M., et al. (2010). Integrin alpha 6 regulates glioblastoma stem cells. Cell Stem Cell, 6, 421–432.PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Kowalski-Chauvel, A., Gouaze-Andersson, V., Baricault, L., et al. (2019). Alpha6-integrin regulates FGFR1 expression through the ZEB1/YAP1 transcription complex in Glioblastoma stem cells resulting in enhanced proliferation and stemness. Cancers (Basel), 11.Google Scholar
  74. 74.
    Cariati, M., Naderi, A., Brown, J. P., et al. (2008). Alpha-6 integrin is necessary for the tumourigenicity of a stem cell-like subpopulation within the MCF7 breast cancer cell line. International Journal of Cancer, 122, 298–304.PubMedCrossRefPubMedCentralGoogle Scholar
  75. 75.
    Cooper, H. M., Tamura, R. N., & Quaranta, V. (1991). The major laminin receptor of mouse embryonic stem cells is a novel isoform of the alpha 6 beta 1 integrin. The Journal of Cell Biology, 115, 843–850.PubMedCrossRefPubMedCentralGoogle Scholar
  76. 76.
    Ito, C., Yamatoya, K., Yoshida, K., Maekawa, M., Miyado, K., & Toshimori, K. (2010). Tetraspanin family protein CD9 in the mouse sperm: Unique localization, appearance, behavior and fate during fertilization. Cell and Tissue Research, 340, 583–594.PubMedCrossRefPubMedCentralGoogle Scholar
  77. 77.
    Takao, Y., Fujiwara, H., Yamada, S., et al. (1999). CD9 is expressed on the cell surface of human granulosa cells and associated with integrin alpha6beta1. Molecular Human Reproduction, 5, 303–310.PubMedCrossRefPubMedCentralGoogle Scholar
  78. 78.
    Zheng, Y., Thomas, A., Schmidt, C. M., & Dann, C. T. (2014). Quantitative detection of human spermatogonia for optimization of spermatogonial stem cell culture. Human Reproduction, 29, 2497–2511.PubMedCrossRefPubMedCentralGoogle Scholar
  79. 79.
    Praest, P., de Buhr, H., & Wiertz, E. J. H. J. (1988). A flow cytometry-based approach to unravel viral interference with the MHC class I antigen processing and presentation pathway. Methods in Molecular Biology, 2019, 187–198.Google Scholar
  80. 80.
    Ema, H., Takano, H., Sudo, K., & Nakauchi, H. (2000). In vitro self-renewal division of hematopoietic stem cells. The Journal of Experimental Medicine, 192, 1281–1288.PubMedPubMedCentralCrossRefGoogle Scholar
  81. 81.
    Fraser, L., Taylor, A. H., & Forrester, L. M. (2013). SCF/KIT inhibition has a cumulative but reversible effect on the self-renewal of embryonic stem cells and on the survival of differentiating cells. Cellular Reprogramming, 15, 259–268.PubMedCrossRefPubMedCentralGoogle Scholar
  82. 82.
    Anderson, R., Fässler, R., Georges-Labouesse, E., et al. (1999). Mouse primordial germ cells lacking beta1 integrins enter the germline but fail to migrate normally to the gonads. Development, 126, 1655–1664.PubMedPubMedCentralGoogle Scholar
  83. 83.
    Yoshinaga, K., Nishikawa, S., Ogawa, M., Hayashi, S., Kunisada, T., & Fujimoto, T. (1991). Role of c-kit in mouse spermatogenesis: Identification of spermatogonia as a specific site of c-kit expression and function. Development, 113, 689–699.PubMedPubMedCentralGoogle Scholar
  84. 84.
    Zhang, L., Tang, J., Haines, C. J., et al. (2013). c-kit expression profile and regulatory factors during spermatogonial stem cell differentiation. BMC Developmental Biology, 13, 38.PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Vincent, S., Segretain, D., Nishikawa, S., et al. (1998). Stage-specific expression of the Kit receptor and its ligand (KL) during male gametogenesis in the mouse: A Kit-KL interaction critical for meiosis. Development, 125, 4585–4593.PubMedPubMedCentralGoogle Scholar
  86. 86.
    Osta, W. A., Chen, Y., Mikhitarian, K., et al. (2004). EpCAM is overexpressed in breast cancer and is a potential target for breast cancer gene therapy. Cancer Research, 64, 5818–5824.PubMedCrossRefPubMedCentralGoogle Scholar
  87. 87.
    Anderson, R., Schaible, K., Heasman, J., & Wylie, C. (1999). Expression of the homophilic adhesion molecule, Ep-CAM, in the mammalian germ line. Journal of Reproduction and Fertility, 116, 379–384.PubMedCrossRefPubMedCentralGoogle Scholar
  88. 88.
    Gassei, K., & Orwig, K. E. (2013). SALL4 expression in gonocytes and spermatogonial clones of postnatal mouse testes. PLoS One, 8, e53976.PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Kirkland, T. N., & Viriyakosol, S. (1998). Structure-function analysis of soluble and membrane-bound CD14. Progress in Clinical and Biological Research, 397, 79–87.PubMedPubMedCentralGoogle Scholar
  90. 90.
    Ziegler-Heitbrock, H. W., & Ulevitch, R. J. (1993). CD14: Cell surface receptor and differentiation marker. Immunology Today, 14, 121–125.PubMedCrossRefPubMedCentralGoogle Scholar
  91. 91.
    Fearns, C., Kravchenko, V. V., Ulevitch, R. J., & Loskutoff, D. J. (1995). Murine CD14 gene expression in vivo: Extramyeloid synthesis and regulation by lipopolysaccharide. The Journal of Experimental Medicine, 181, 857–866.PubMedCrossRefPubMedCentralGoogle Scholar
  92. 92.
    Orwig, K. E., Ryu, B. Y., Master, S. R., et al. (2008). Genes involved in post-transcriptional regulation are overrepresented in stem/progenitor spermatogonia of cryptorchid mouse testes. Stem Cells, 26, 927–938.PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Arvanitis, D., & Davy, A. (2008). Eph/ephrin signaling: Networks. Genes & Development, 22, 416–429.CrossRefGoogle Scholar
  94. 94.
    Kullander, K., & Klein, R. (2002). Mechanisms and functions of Eph and ephrin signalling. Nature Reviews. Molecular Cell Biology, 3, 475–486.PubMedCrossRefPubMedCentralGoogle Scholar
  95. 95.
    Chan, F., Oatley, M. J., Kaucher, A. V., et al. (2014). Functional and molecular features of the Id4+ germline stem cell population in mouse testes. Genes & Development, 28, 1351–1362.CrossRefGoogle Scholar
  96. 96.
    Mutoji, K., Singh, A., Nguyen, T., et al. (2016). TSPAN8 expression distinguishes spermatogonial stem cells in the prepubertal mouse testis. Biology of Reproduction, 95, 117.PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Li, C. H., Yan, L. Z., Ban, W. Z., et al. (2017). Long-term propagation of tree shrew spermatogonial stem cells in culture and successful generation of transgenic offspring. Cell Research, 27, 241–252.PubMedCrossRefPubMedCentralGoogle Scholar
  98. 98.
    Fan, Y., Ye, M. S., Zhang, J. Y., et al. (2019). Chromosomal level assembly and population sequencing of the Chinese tree shrew genome. Zoological Research, 40(6), 506–521.PubMedCrossRefPubMedCentralGoogle Scholar
  99. 99.
    Oatley, M., Kaucher, A., Racicot, K., & Oatley, J. (2011). Inhibitor of DNA binding 4 is expressed selectively by single Spermatogonia in the male Germline and regulates the self-renewal of Spermatogonial stem cells in mice. Biology of Reproduction, 85, 347–356.PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Aloisio, G., Nakada, Y., Saatcioglu, H., et al. (2014). PAX7 expression defines germline stem cells in the adult testis. Journal of Clinical Investigation, 124, 3929–3944.PubMedCrossRefPubMedCentralGoogle Scholar
  101. 101.
    Komai, Y., Tanaka, T., Tokuyama, Y., et al. (2014). Bmi1 expression in long-term germ stem cells. Scientific Reports, 4, 6175.PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Kim, Y. H., Kim, B. J., Kim, B. G., et al. (2013). Stage-specific embryonic antigen-1 expression by undifferentiated spermatogonia in the prepubertal boar testis. Journal of Animal Science, 91, 3143–3154.PubMedCrossRefPubMedCentralGoogle Scholar
  103. 103.
    Sun, Y. Z., Liu, S. T., Li, X. M., & Zou, K. (2019). Progress in. Zoological Research, 40, 343–348.PubMedCrossRefPubMedCentralGoogle Scholar
  104. 104.
    Bedford-Guaus, S. J., Kim, S., Mulero, L., et al. (2017). Molecular markers of putative spermatogonial stem cells in the domestic cat. Reproduction in Domestic Animals, 52(Suppl 2), 177–186.PubMedCrossRefPubMedCentralGoogle Scholar
  105. 105.
    He, Z., Kokkinaki, M., Jiang, J., Zeng, W., Dobrinski, I., & Dym, M. (2012). Isolation of human male germ-line stem cells using enzymatic digestion and magnetic-activated cell sorting. Methods in Molecular Biology, 825, 45–57.PubMedCrossRefPubMedCentralGoogle Scholar
  106. 106.
    Yu, X., Riaz, H., Dong, P., et al. (2014). Identification and IVC of spermatogonial stem cells in prepubertal buffaloes. Theriogenology, 81, 1312–1322.PubMedCrossRefPubMedCentralGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Germline Stem Cells and Microenvironment Lab, College of Animal Science and TechnologyNanjing Agricultural UniversityNanjingChina

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