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Effects of Extracellular Matrix Protein-derived Signaling on the Maintenance of the Undifferentiated State of Spermatogonial Stem Cells from Porcine Neonatal Testis

  • Park, Min Hee (Department of Animal Life Science, Kangwon National University) ;
  • Park, Ji Eun (Department of Animal Life Science, Kangwon National University) ;
  • Kim, Min Seong (Department of Animal Life Science, Kangwon National University) ;
  • Lee, Kwon Young (College of Veterinary Medicine and Institute of Veterinary Science, Kangwon National University) ;
  • Hwang, Jae Yeon (Division of Applied Animal Science, Kangwon National University) ;
  • Yun, Jung Im (Division of Animal Resource Science, Kangwon National University) ;
  • Choi, Jung Hoon (College of Veterinary Medicine and Institute of Veterinary Science, Kangwon National University) ;
  • Lee, Eunsong (College of Veterinary Medicine and Institute of Veterinary Science, Kangwon National University) ;
  • Lee, Seung Tae (Department of Animal Life Science, Kangwon National University)
  • Received : 2015.10.20
  • Accepted : 2016.01.25
  • Published : 2016.10.01

Abstract

In general, the seminiferous tubule basement membrane (STBM), comprising laminin, collagen IV, perlecan, and entactin, plays an important role in self-renewal and spermatogenesis of spermatogonial stem cells (SSCs) in the testis. However, among the diverse extracellular matrix (ECM) proteins constituting the STBM, the mechanism by which each regulates SSC fate has yet to be revealed. Accordingly, we investigated the effects of various ECM proteins on the maintenance of the undifferentiated state of SSCs in pigs. First, an extracellular signaling-free culture system was optimized, and alkaline phosphatase (AP) activity and transcriptional regulation of SSC-specific genes were analyzed in porcine SSCs (pSSCs) cultured for 1, 3, and 5 days on non-, laminin- and collagen IV-coated Petri dishes in the optimized culture system. The microenvironment consisting of glial cell-derived neurotrophic factor (GDNF)-supplemented mouse embryonic stem cell culture medium (mESCCM) (GDNF-mESCCM) demonstrated the highest efficiency in the maintenance of AP activity. Moreover, under the established extracellular signaling-free microenvironment, effective maintenance of AP activity and SSC-specific gene expression was detected in pSSCs experiencing laminin-derived signaling. From these results, we believe that laminin can serve as an extracellular niche factor required for the in vitro maintenance of undifferentiated pSSCs in the establishment of the pSSC culture system.

Keywords

Porcine;Spermatogonial Stem Cells;Undifferentiation;Extracellular Matrix Proteins

Acknowledgement

Supported by : Korea Institute of Planning and Evaluation for Technology in Food, Agriculture, Forestry and Fisheries (IPET)

References

  1. Lee, W. Y., H. J. Park, R. Lee, K. H. Lee, Y. H. Kim, B. Y. Ryu, N. H. Kim, J. H. Kim, J. H. Kim, S. H. Moon, J. K. Park, H. J. Chung, D. H. Kim, and H. Song. 2013. Establishment and in vitro culture of porcine spermatogonial germ cells in low temperature culture conditions. Stem Cell Res. 11:1234-1249. https://doi.org/10.1016/j.scr.2013.08.008
  2. Lim, J. J., H. J. Kim, K. S. Kim, J. Y. Hong, and D. R. Lee. 2013. In vitro culture-induced pluripotency of human spermatogonial stem cells. Biomed. Res. Int. 2013:143028.
  3. Luo, J., S. Megee, and I. Dobrinski. 2009. Asymmetric distribution of UCH-L1 in spermatogonia is associated with maintenance and differentiation of spermatogonial stem cells. J. Cell. Physiol. 220:460-468. https://doi.org/10.1002/jcp.21789
  4. McLaren, A. 2003. Primordial germ cells in the mouse. Dev. Biol. 262:1-15. https://doi.org/10.1016/S0012-1606(03)00214-8
  5. McLean, D. J. 2008. Spermatogonial stem cell transplantation, testicular function, and restoration of male fertility in mice. Methods Mol. Biol. 450:149-162. https://doi.org/10.1007/978-1-60327-214-8_11
  6. Nagano, M., C. J. Brinster, K. E. Orwig, B. Y. Ryu, M. R. Avarbock, and R. L. Brinster. 2001. Transgenic mice produced by retroviral transduction of male germ-line stem cells. Proc. Natl. Acad. Sci. USA. 98:13090-13095. https://doi.org/10.1073/pnas.231473498
  7. Oatley, J. M. and R. L. Brinster. 2006. Spermatogonial stem cells. Methods Enzymol. 419:259-282. https://doi.org/10.1016/S0076-6879(06)19011-4
  8. Oatley, J. M. and R. L. Brinster. 2008. Regulation of spermatogonial stem cell self-renewal in mammals. Annu. Rev. Cell Dev. Biol. 24:263-286. https://doi.org/10.1146/annurev.cellbio.24.110707.175355
  9. Ohlund, D., O. Franklin, E. Lundberg, C. Lundin, and M. Sund. 2013. Type IV collagen stimulates pancreatic cancer cell proliferation, migration, and inhibits apoptosis through an autocrine loop. BMC Cancer 13:154. https://doi.org/10.1186/1471-2407-13-154
  10. Ooba, T., T. Ishikawa, K. Yamaguchi, Y. Kondo, Y. Sakamoto, and M. Fujisawa. 2008. Expression and distribution of laminin chains in the testis for patients with azzospermia. J. Androl. 29:147-152.
  11. Park, M. H., J. E. Park, M. S. Kim, K. Y. Lee, H. J. Park, J. I. Yun, J. H. Choi, E. S. Lee, and S. T. Lee. 2014. Development of a high-yield technique to isolate spermatogonial stem cells from porcine testes. J. Assist. Reprod. Genet. 31:983-991. https://doi.org/10.1007/s10815-014-0271-7
  12. Phillips, B. T., K. Gassei, and K. E. Orwig. 2010. Spermatogonial stem cell regulation and spermatogenesis. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 365:1663-1678. https://doi.org/10.1098/rstb.2010.0026
  13. Poschl, E., U. Schlotzer-Schrehardt, B. Brachvogel, K. Saito, Y. Ninomiya, and U. Mayer. 2004. Collagen IV is essential for basement membrane stability but dispensable for initiation of its assembly during early development. Development 131:1619-1628. https://doi.org/10.1242/dev.01037
  14. Brinster, R. L. 2002. Germline stem cell transplantation and transgenesis. Science 296:2174-2176. https://doi.org/10.1126/science.1071607
  15. Carpenter, G. and S. Cohen. 1990. Epidermal growth factor. J. Biol. Chem. 265:7709-7712.
  16. Chen, S., M. Lewallen, and T. Xie. 2013. Adhesion in the stem cell niche: biological roles and regulation. Development 140:255-265. https://doi.org/10.1242/dev.083139
  17. Daley, G. Q. and D. T. Scadden. 2008. Prospects for stem cellbased therapy. Cell 132:544-548. https://doi.org/10.1016/j.cell.2008.02.009
  18. de Barros, F. R. O., M. I. Giassetti, and J. A. Visintin. 2012. Spermatogonial stem cells and animal transgenesis In:Innovations in Biotechnology (Ed. Eddy C. Agbo). InTech, Rijeka, Croatia. pp. 303-318.
  19. de Rooij, D. G. and J. A. Grootegoed. 1998. Spermatogonial stem cells. Curr. Opin. Cell Biol. 10:694-701. https://doi.org/10.1016/S0955-0674(98)80109-9
  20. Del Angel-Mosqueda, C., Y. Gutierrez-Puente, A. P. Lopez-Lozano, R. E. Romero-Zavaleta, A. Mendiola-Jimenez, C. E. Medina-De la Garza, M. Marquez-M, and M. A. De la Garza-Ramos. 2015. Epidermal growth factor enhances osteogenic differentiation of dental pulp stem cells in vitro. Head Face Med. 11:29. https://doi.org/10.1186/s13005-015-0086-5
  21. Gattazzo, F., A. Urciuolo, and P. Bonaldo. 2014. Extracellular matrix: A dynamic microenviroment for stem cell niche. Biochim. Biophys. Acta 1840:2506-2519. https://doi.org/10.1016/j.bbagen.2014.01.010
  22. Aponte, P. M., M. P. van Bragt, D. G. de Rooij, and A. M. van Pelt. 2005. Spermatogonial stem cells: Characteristics and experimental possibilities. APMIS 113:727-742. https://doi.org/10.1111/j.1600-0463.2005.apm_302.x
  23. Aumailley, M. and R. Timpl. 1986. Attachment of cells to basement membrane collagen type IV. J. Cell Biol. 103:1569-1575. https://doi.org/10.1083/jcb.103.4.1569
  24. Guan, K., K. Nayernia, L. S. Maier, S. Wagner, R. Dressel, J. H. Lee, J. Nolte, F. Wolf, M. Li, W. Engel, and G. Hasenfuss. 2006. Pluripotency of spermatogonial stem cells from adult mouse testis. Nature 440:1199-1203. https://doi.org/10.1038/nature04697
  25. Hofmann, M. C. 2008. Gdnf signaling pathways within the mammalian spermatogonial stem cell niche. Mol. Cell. Endocrinol. 288:95-103. https://doi.org/10.1016/j.mce.2008.04.012
  26. Kanatsu-Shinohara, M., J. Lee, K. Inoue, N. Ogonuki, H. Miki, S. Toyokuni, M. Ikawa, T. Nakamura, A. Ogura, and T. Shinohara. 2008. Pluripotency of a single spermatogonial stem cell in mice. Biol. Reprod. 78:681-687. https://doi.org/10.1095/biolreprod.107.066068
  27. Kanatsu-Shinohara, M. and T. Shinohara. 2013. Spermatogonial stem cell self-renewal and development. Annu. Rev. Cell Dev. Biol. 29:163-187. https://doi.org/10.1146/annurev-cellbio-101512-122353
  28. Khoshnoodi, J., V. Pedchenko, and B. G. Hudson. 2008. Mammalian collagen IV. Microsc. Res. Tech. 71:357-370. https://doi.org/10.1002/jemt.20564
  29. Kubota, H. and R. L. Brinster. 2006. Reproductive endocrinology (including placental hormones): Technology Insight: In vitro culture of spermatogonial stem cells and their potential therapeutic uses. Nat. Rev. Endocrinol. 2:99-108. https://doi.org/10.1038/ncpendmet0098
  30. Lavitrano, M., M. Busnelli, M. G. Cerrito, R. Giovannoni, S. Manzini, and A. Vargiolu. 2005. Sperm-mediated gene transfer. Reprod. Fertil. Dev. 18:19-23.
  31. Schuldiner, M., O. Yanuka, J. Itskovitz-Eldor, D. A. Melton, and N. Benvenisty. 2000. Effects of eight growth factors on the differentiation of cells derived from human embryonic stem cells. Proc. Natl. Acad. Sci. USA. 97:11307-11312. https://doi.org/10.1073/pnas.97.21.11307
  32. Shinohara, T., M. R. Avarbock, and R. L. Brinster. 1999. Beta1-and alpha6-integrin are surface markers on mouse spermatogonial stem cells. Proc. Natl. Acad. Sci. USA. 96:5504-5509. https://doi.org/10.1073/pnas.96.10.5504
  33. Simon, L., R. A. Hess, and P. S. Cooke. 2010. Spermatogonial stem cells, in vivo transdifferentiation and human regenerative medicine. Expert Opin. Biol. Ther. 10:519-530. https://doi.org/10.1517/14712591003614731
  34. Siu, M. K. and C. Y. Cheng. 2004. Extracellular matrix: recent advances on its role in junction dynamics in the seminiferous epithelium during spermatogenesis. Biol. Reprod. 71:375-391. https://doi.org/10.1095/biolreprod.104.028225
  35. Siu, M. K. and C. Y. Cheng. 2008. Extracellular matrix and its role in spermatogenesis. Adv. Exp. Med. Biol. 636:74-91.
  36. Timpl, R., H. Rohde, P. G. Robey, S. I. Rennard, J. M. Foidart, and G. R. Martin. 1979. Laminin-a glycoprotein from basement membranes. J. Biol. Chem. 254:9933-9937.
  37. Vlajkovic, S., R. Cukuranovic, M. D. Bjelakovic, and V. Stefanovic. 2012. Possible therapeutic use of spermatogonial stem cells in the treatment of male infertility: A brief overview. Sci. World J. 2012:Article ID 374151.
  38. Yazama, F., M. Esaki, and H. Sawada. 1997. Immunocytochemistry of extracellular matrix components in the rat seminiferous tubule: Electron microscopic localization with improved methodology. Anat. Rec. 248:51-62. https://doi.org/10.1002/(SICI)1097-0185(199705)248:1<51::AID-AR6>3.0.CO;2-I