About this Journal Submit a Manuscript Table of Contents
BioMed Research International
Volume 2014 (2014), Article ID 138350, 17 pages
http://dx.doi.org/10.1155/2014/138350
Research Article

Differential Gene Expression Profiling of Enriched Human Spermatogonia after Short- and Long-Term Culture

1Institute of Anatomy, University of Tübingen, Österbergstraße 3, 72074 Tübingen, Germany
2Institute for Anatomy and Cell Biology, Medical Faculty, University of Heidelberg, Im Neuenheimer Feld 307, 69120 Heidelberg, Germany
3Amol University of Special Modern Technologies, Special Modern Technologies, P.O. Box 46168-49767, Amol, Iran
4Department of Stem Cells and Developmental Biology, Royan Institute, P.O. Box 19395-4644, Tehran, Iran
5TATAA Biocenter AB, Odinsgatan 28, 41103 Göteborg, Sweden and Institute of Biotechnology at the Czech Academy of Sciences, Vídenská 1083, 14220 Prague 4, Czech Republic
6Institute of Anthropology and Human Genetics, Microarray Facility, University Clinic, Calwerstraße 7, 72076 Tübingen, Germany
7Department of Urology, University Clinic Tübingen, Hoppe-Seyler-Straße 3, 72076 Tübingen, Germany

Received 17 September 2013; Accepted 19 November 2013; Published 12 March 2014

Academic Editor: Irma Virant-Klun

Copyright © 2014 Sabine Conrad et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. Y. Clermont, “Renewal of spermatogonia in man,” American Journal of Anatomy, vol. 118, no. 2, pp. 509–524, 1966.
  2. L. Gillan, D. Matei, D. A. Fishman, C. S. Gerbin, B. Y. Karlan, and D. D. Chang, “Periostin secreted by epithelial ovarian carcinoma is a ligand for αVβ3 and αVβ5 integrins and promotes cell motility,” Cancer Research, vol. 62, no. 18, pp. 5358–5364, 2002. View at Scopus
  3. H. Sadri-Ardekani, M. A. Akhondi, F. van der Veen, S. Repping, and A. M. M. Van Pelt, “In vitro propagation of human prepubertal spermatogonial stem cells,” Journal of the American Medical Association, vol. 305, no. 23, pp. 2416–2418, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. J. Lee and T. Shinohara, “Epigenetic modifications and self-renewal regulation of mouse germline stem cells,” Cell Research, vol. 21, no. 8, pp. 1164–1171, 2011.
  5. S. Conrad, M. Renninger, J. Hennenlotter, et al., “Generation of pluripotent stem cells from adult human testis,” Nature, vol. 456, no. 7220, pp. 344–349, 2008.
  6. H. Sadri-Ardekani, S. C. Mizrak, S. K. M. van Daalen et al., “Propagation of human spermatogonial stem cells in vitro,” Journal of the American Medical Association, vol. 302, no. 19, pp. 2127–2134, 2009. View at Publisher · View at Google Scholar · View at Scopus
  7. B. Chen, Y. B. Wang, Z. L. Zhang, et al., “Xeno-free culture of human spermatogonial stem cells supported by human embryonic stem cell-derived fibroblast-like cells,” Asian Journal of Andrology, vol. 11, no. 5, pp. 557–565, 2009.
  8. Z. He, M. Kokkinaki, J. Jiang, I. Dobrinski, and M. I. Dym, “Isolation, characterization, and culture of human spermatogonia,” Biology of Reproduction, vol. 82, no. 2, pp. 363–372, 2010.
  9. J. J. Lim, S.-Y. Sung, H. J. Kim et al., “Long-term proliferation and characterization of human spermatogonial stem cells obtained from obstructive and non-obstructive azoospermia under exogenous feeder-free culture conditions,” Cell Proliferation, vol. 43, no. 4, pp. 405–417, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. F. Izadyar, J. Wong, C. Maki, et al., “Identification and characterization of repopulating spermatogonial stem cells from the adult human testis,” Human Reproduction, vol. 26, no. 6, pp. 1296–1306, 2011.
  11. T. Mirzapour, M. Movahedin, T. A. Tengku Ibrahim, et al., “Effects of basic fibroblast growth factor and leukaemia inhibitory factor on proliferation and short-term culture of human spermatogonial stem cells,” Andrologia, vol. 44, supplement 1, pp. 41–55, 2012.
  12. N. Golestaneh, M. Kokkinaki, D. Pant, et al., “Pluripotent stem cells derived from adult human testes,” Stem Cells and Development, vol. 18, no. 8, pp. 1115–1126, 2009.
  13. N. Kossack, J. Meneses, S. Shefi et al., “Isolation and characterization of pluripotent human spermatogonial stem cell-derived cells,” Stem Cells, vol. 27, no. 1, pp. 138–149, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. S. C. Mizrak, J. V. Chikhovskaya, H. Sadri-Ardekani et al., “Embryonic stem cell-like cells derived from adult human testis,” Human Reproduction, vol. 25, no. 1, pp. 158–167, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. J. V. Chikhovskaya, M. J. Jonker, A. Meissner, T. M. Breit, S. Repping, and A. M. M. van Pelt, “Human testis-derived embryonic stem cell-like cells are not pluripotent, but possess potential of mesenchymal progenitors,” Human Reproduction, vol. 27, no. 1, pp. 210–221, 2012. View at Publisher · View at Google Scholar · View at Scopus
  16. R. Gonzalez, L. Griparic, V. Vargas et al., “A putative mesenchymal stem cells population isolated from adult human testes,” Biochemical and Biophysical Research Communications, vol. 385, no. 4, pp. 570–575, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. M. Stimpfel, T. Skutella, M. Kubista, E. Malicev, S. Conrad, and I. Virant-Klun, “Potential stemness of frozen-thawed testicular biopsies without sperm in infertile men included into the in vitro fertilization programme,” Journal of Biomedicine and Biotechnology, vol. 2012, Article ID 291038, 15 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. J. J. Lim, H. J. Kim, K. S. Kim, J. Y. Hong, and D. R. Lee, “In vitro culture-induced pluripotency of human spermatogonial stem cells,” BioMed Research International, vol. 2013, Article ID 143028, 9 pages, 2013. View at Publisher · View at Google Scholar
  19. R. Heer, A. C. Hepburn, S. C. Williamson, et al., “Renal differentiation from adult spermatogonial stem cells,” Renal failure, vol. 35, no. 10, pp. 1387–1391, 2013.
  20. Z. Zhang, J. Liu, Y. Liu, et al., “Generation, characterization and potential therapeutic applications of mature and functional hepatocytes from stem cells,” Journal of Cellular Physiology, vol. 228, no. 2, pp. 298–305, 2013.
  21. N. Kossack, N. Terwort, J. Wistuba, et al., “A combined approach facilitates the reliable detection of human spermatogonia in vitro,” Human Reproduction, vol. 28, no. 11, pp. 3012–3025, 2013.
  22. K. Ko, M. J. Arauzo-Bravo, N. Tapia, et al., “Human adult germline stem cells in question,” Nature, vol. 465, no. 7301, pp. E1–E3, 2010.
  23. A. Tichopad, R. Kitchen, I. Riedmaier, C. Becker, A. Ståhlberg, and M. Kubista, “Design and optimization of reverse-transcription quantitative PCR experiments,” Clinical Chemistry, vol. 55, no. 10, pp. 1816–1823, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. D. H. Castrillon, B. J. Quade, T. Y. Wang, C. Quigley, and C. P. Crum, “The human VASA gene is specifically expressed in the germ cell lineage,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 17, pp. 9585–9590, 2000.
  25. D. B. Menke, G. L. Mutter, and D. C. Page, “Expression of DAZ, an Azoospermia factor candidate, in human spermatogonia,” American Journal of Human Genetics, vol. 60, no. 1, pp. 237–241, 1997. View at Scopus
  26. A. Szczerba, A. Jankowska, M. Andrusiewicz, M. Karczewski, W. Turkiewicz, and J. B. Warchoł, “Distribution of the DAZ gene transcripts in human testis,” Folia Histochemica et Cytobiologica, vol. 42, no. 2, pp. 119–121, 2004. View at Scopus
  27. F. Wang, Q. Zhang, J. Cao, Q. Huang, and X. Zhu, “The microtubule plus end-binding protein EB1 is involved in Sertoli cell plasticity in testicular seminiferous tubules,” Experimental Cell Research, vol. 314, no. 1, pp. 213–226, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. A. Reid, A. Gould, N. Brand et al., “Leukemia translocation gene, PLZF, is expressed with a speckled nuclear pattern in early hematopoietic progenitors,” Blood, vol. 86, no. 12, pp. 4544–4552, 1995. View at Scopus
  29. F. W. Buaas, A. L. Kirsh, M. Sharma, et al., “Plzf is required in adult male germ cells for stem cell self-renewal,” Nature Genetics, vol. 36, no. 6, pp. 647–652, 2004.
  30. O. Tureci, U. Sahin, M. Koslowski, et al., “A novel tumour associated leucine zipper protein targeting to sites of gene transcription and splicing,” Oncogene, vol. 21, no. 24, pp. 3879–3888, 2002.
  31. I. Mendoza-Lujambio, P. Burfeind, C. Dixkens et al., “The Hook1 gene is non-functional in the abnormal spermatozoon head shape (azh) mutant mouse,” Human Molecular Genetics, vol. 11, no. 14, pp. 1647–1658, 2002. View at Scopus
  32. J. Bowles, R. P. Teasdale, K. James, and P. Koopman, “Dppa3 is a marker of pluripotency and has a human homologue that is expressed in germ cell tumours,” Cytogenetic and Genome Research, vol. 101, no. 3-4, pp. 261–265, 2003. View at Publisher · View at Google Scholar · View at Scopus
  33. J. A. West, S. R. Viswanathan, A. Yabuuchi et al., “A role for Lin28 in primordial germ-cell development and germ-cell malignancy,” Nature, vol. 460, no. 7257, pp. 909–913, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. N. Zhang, H. J. Yeh, R. Zhong, Y. S. Li, and T. F. Deuel, “A dominant-negative pleiotrophin mutant introduced by homologous recombination leads to germ-cell apoptosis in male mice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 12, pp. 6734–6738, 1999.
  35. R. J. H. L. M. van Gurp, J. W. Oosterhuis, V. Kalscheuer, E. C. M. Mariman, and L. H. J. Looijenga, “Biallelic expression of the H19 and IGF2 genes in human testicular germ cell tumors,” Journal of the National Cancer Institute, vol. 86, no. 14, pp. 1070–1075, 1994. View at Scopus
  36. A. Bafico, A. Gazit, T. Pramila, P. W. Finch, A. Yaniv, and S. A. Aaronson, “Interaction of Frizzled Related Protein (FRP) with Wnt ligands and the frizzled receptor suggests alternative mechanisms for FRP inhibition of Wnt signaling,” Journal of Biological Chemistry, vol. 274, no. 23, pp. 16180–16187, 1999. View at Publisher · View at Google Scholar · View at Scopus
  37. J. Walsh and P. W. Andrews, “Expression of Wnt and Notch pathway genes in a pluripotent human embryonal carcinoma cell line and embryonic stem cell,” Acta Pathologica, Microbiologica, et Immunologica Scandinavica, vol. 111, no. 1, pp. 197–210, 2003.
  38. S. J. Freemantle, J. S. Kerley, S. L. Olsen, R. H. Gross, and M. J. Spinella, “Developmentally-related candidate retinoic acid target genes regulated early during neuronal differentiation of human embryonal carcinoma,” Oncogene, vol. 21, no. 18, pp. 2880–2889, 2002. View at Publisher · View at Google Scholar · View at Scopus
  39. M. G. Pezzolesi, K. M. Zbuk, K. A. Waite, and C. Eng, “Comparative genomic and functional analyses reveal a novel cis-acting PTEN regulatory element as a highly conserved functional E-box motif deleted in Cowden syndrome,” Human Molecular Genetics, vol. 16, no. 9, pp. 1058–1071, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. C. Q. F. Wang, D. D. Mruk, W. M. Lee, and C. Y. Cheng, “Coxsackie and Adenovirus Receptor (CAR) is a product of Sertoli and germ cells in rat testes which is localized at the Sertoli-Sertoli and Sertoli-germ cell interface,” Experimental Cell Research, vol. 313, no. 7, pp. 1373–1392, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. M. I. Mosevitsky, E. S. Snigirevskaya, and Y. Y. Komissarchik, “Immunoelectron microscopic study of BASP1 and MARCKS location in the early and late rat spermatids,” Acta Histochemica, vol. 114, no. 3, pp. 237–243, 2012. View at Publisher · View at Google Scholar · View at Scopus
  42. H. Chang and M. M. Matzuk, “Smad5 is required for mouse primordial germ cell development,” Mechanisms of Development, vol. 104, no. 1-2, pp. 61–67, 2001.
  43. C. Itman and K. L. Loveland, “SMAD expression in the testis: an insight into BMP regulation of spermatogenesis,” Developmental Dynamics, vol. 237, no. 1, pp. 97–111, 2008.
  44. M. Pellegrini, P. Grimaldi, P. Rossi, R. Geremia, and S. Dolci, “Developmental expression of BMP4ALK3SMAD5 signaling pathway in the mouse testis: a potential role of BMP4 in spermatogonia differentiation,” Journal of Cell Science, vol. 116, no. 16, pp. 3363–3372, 2003. View at Publisher · View at Google Scholar · View at Scopus
  45. J.-W. Wu, R.-Y. Wang, Q.-S. Guo, and C. Xu, “Expression of the retinoic acid-metabolizing enzymes RALDH2 and CYP26b1 during mouse postnatal testis development,” Asian Journal of Andrology, vol. 10, no. 4, pp. 569–576, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. S. Wang, H. Zheng, Y. Esaki, F. Kelly, and W. Yan, “Cullin3 is a KLHL10-interacting protein preferentially expressed during late spermiogenesis,” Biology of Reproduction, vol. 74, no. 1, pp. 102–108, 2006.
  47. G. Vinci, R. Brauner, A. Tar et al., “Mutations in the TSPYL1 gene associated with 46,XY disorder of sex development and male infertility,” Fertility and Sterility, vol. 92, no. 4, pp. 1347–1350, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. K. Mizuno, A. Tokumasu, A. Nakamura, et al., “Genes associated with the formation of germ cells from embryonic stem cells in cultures containing different glucose concentrations,” Molecular Reproduction and Development, vol. 73, no. 4, pp. 437–445, 2006.
  49. T. Sato, K. Katagiri, A. Gohbara et al., “In vitro production of functional sperm in cultured neonatal mouse testes,” Nature, vol. 471, no. 7339, pp. 504–507, 2011. View at Publisher · View at Google Scholar · View at Scopus
  50. J. Quackenbush, “Microarray data normalization and transformation,” Nature Genetics, vol. 32, pp. 496–501, 2002.