Development of novel strategies for the isolation of piglet testis cells with a high proportion of gonocytes

Reproduction, Fertility and Development

Volumn 22, Issue 7, 2010, Pages 1057-1065

  Yang, Yanfei ^a   Yarahmadi, Mehran ^a   Honaramooz, Ali ^a  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

enzymatic cell isolation; pig; spermatogonial stem cell

Indexed keywords

COLLAGENASE; DEOXYRIBONUCLEASE; HYALURONIDASE; TRYPSIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ISOLATION; CELL MATURATION; CONTROLLED STUDY; EMBRYO; ENZYME CHEMISTRY; ERYTHROCYTE; LYSIS; MALE; NONHUMAN; PIGLET; TESTIS CELL; VORTEX MOTION;

ANIMALS; ANIMALS, NEWBORN; CELL SEPARATION; CELL SURVIVAL; COLLAGENASES; DEOXYRIBONUCLEASES; HYALURONOGLUCOSAMINIDASE; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY, CONFOCAL; SPERMATOZOA; SWINE; TESTIS;

SUIDAE;

EID: 77956243579     PISSN: 10313613     EISSN: None     Source Type: Journal    
DOI: 10.1071/RD09316     Document Type: Article

References (43)

1. Bellvé, A., Cavicchia, J., Millette, C., OBrien, D., Bhatnagar, Y., and Dym, M. (1977). Spermatogenic cells of the prepuberal mouse: isolation and morphological characterization. J. Cell Biol. 74, 68-85. doi:10.1083/JCB.74.1.68
2. Crabbé, E., Verheyen, G., Tournaye, H., and van Steirteghem, A. (1997). The use of enzymatic procedures to recover testicular germ cells. Hum. Reprod. 12, 1682-1687. doi:10.1093/HUMREP/12.8.1682
3. de Rooij, D. G. (1998). Stem cells in the testis. Int. J. Exp. Pathol. 79, 67-80. doi:10.1046/J.1365-2613.1998.00057.X
4. de Rooij, D. G., and Mizrak, S. C. (2008). Deriving multipotent stem cells from mouse spermatogonial stem cells: a new tool for developmental and clinical research. Development 135, 2207-2213. doi:10.1242/DEV.015453
5. Dobrinski, I., and Travis, A. J. (2007). Germ cell transplantation for the propagation of companion animals, non-domestic and endangered species. Reprod. Fertil. Dev. 19, 732-739. doi:10.1071/RD07036
6. Erdmann, A. A., Jung, U., Foley, J. E., Toda, Y., and Fowler, D. H. (2004). Co-stimulated/Tc2 cells abrogate murine marrow graft rejection. Biol. Blood Marrow Transplant. 10, 604-613. doi:10.1016/J.BBMT.2004.06.006
7. Franca, L. R., Silva, V. A., Jr, Chiarini-Garcia, H., Garcia, S. K., and Debeljuk, L. (2000). Cell proliferation and hormonal changes during postnatal development of the testis in the pig. Biol. Reprod. 63, 1629-1636. doi:10.1095/BIOLREPROD63.6.1629
8. Frankenhuis, M. T., Wensing, C. J. G., and Kremer, J. (1981). The influence of elevated testicular temperature and scrotal surgery on the number of gonocytes in the newborn pig. Int. J. Androl. 4, 105-110. doi:10.1111/J.1365-2605.1981.TB00696.X
9. Goel, S., Sugimoto, M., Minami, N., Yamada, M., Kume, S., and Imai, H. (2007). Identification, isolation, and in vitro culture of porcine gonocytes. Biol. Reprod. 77, 127-137. doi:10.1095/BIOLREPROD.106.056879
10. Herrid, M., Davey, R. J., Hutton, K., Colditz, I. G., and Hill, J. R. (2009). A comparison of methods for preparing enriched populations of bovine spermatogonia. Reprod. Fertil. Dev. 21, 393-399. doi:10.1071/RD08129
11. Honaramooz, A., Megee, S. O., and Dobrinski, I. (2002). Germ cell transplantation in pigs. Biol. Reprod. 66, 21-28. doi:10.1095/BIOLREPROD66.1.21
12. Honaramooz, A., Behboodi, E., Megee, S. O., Overton, S. A., Galantino-Homer, H., Echelard, Y., and Dobrinski, I. (2003a). Fertility and germline transmission of donor haplotype following germ cell transplantation in immunocompetent goats. Biol. Reprod. 69, 1260-1264. doi:10.1095/BIOLREPROD.103. 018788
13. Honaramooz, A., Behboodi, E., Blash, S., Megee, S. O., and Dobrinski, I. (2003b). Germ cell transplantation in goats. Mol. Reprod. Dev. 64, 422-428. doi:10.1002/MRD.10205
14. Honaramooz, A., Behboodi, E., Hausler, C., Blash, S., Ayres, S., Azuma, C., Echelard, Y., and Dobrinski, I. (2005). Depletion of endogenous germ cells in male pigs and goats in preparation for germ cell transplantation. J. Androl. 26, 698-705. doi:10.2164/JANDROL.05032
15. Honaramooz, A., Megee, S., Zeng, W., Destrempes, M. M., Overton, S. A., et al. (2008). Adeno-associated virus (AAV)-mediated transduction of male germ line stem cells results in transgene transmission after germ cell transplantation. FASEB J. 22, 374-382. doi:10.1096/FJ.07-8935COM
16. Hughes, P. E., and Varley, M. A. (1980). Reproduction in the Pig. (Butterworth: London.)
17. Jiang, F. X. (2001). Male germ cell transplantation: promise and problems. Reprod. Fertil. Dev. 13, 609-614. doi:10.1071/RD01059
18. Jiang, F. X., and Short, R. V. (1995). Male germ cell transplantation in rats: apparent synchronization of spermatogenesis between host and donor seminiferous epithelia. Int. J. Androl. 18, 326-330. doi:10.1111/J.1365-2605. 1995.TB00570.X
19. Jiang, F. X., and Short, R. V. (1998a). Different fate of primordial germ cells and gonocytes following transplantation. APMIS 106, 58-62, discussion 62-63. doi:10.1111/J.1699-0463.1998.TB01319.X
20. Jiang, F. X., and Short, R. V. (1998b). Male germ cell transplantation: present achievements and future prospects. Int. J. Dev. Biol. 42, 1067-1073.
21. Khaira, H., McLean, D., Ohl, D. A., and Smith, G. D. (2005). Spermatogonial stem cell isolation, storage, and transplantation. J. Androl. 26, 442-450. doi:10.2164/JANDROL.05062
22. Klein, A. B., Witonsky, S. G., Ahmed, S. A., Holladay, S. D., Gogal, R. M., Jr, Link, L., and Reilly, C. M. (2006). Impact of different cell isolation techniques on lymphocyte viability and function. J. Immunoassay Immunochem. 27, 61-76. doi:10.1080/15321810500403755
23. Lal, G., Shaila, M. S., and Nayak, R. (2006). Booster immunization of antigen primed mice with anti-idiotypic T cells generates antigenspecific memory T cell response. Vaccine 24, 1149-1158. doi:10.1016/J.VACCINE.2005.08.099
24. Leng, C., Gries, M., Ziegler, J., Lokshin, A., Mascagni, P., Lentzsch, S., and Mapara, M. Y. (2006). Reduction of graft-versus-host disease by histone deacetylase inhibitor suberonylanilide hydroxamic acid is associated with modulation of inflammatory cytokine milieu and involves inhibition of STAT1. Exp. Hematol. 34, 776-787. doi:10.1016/J.EXPHEM. 2006.02.014
25. Li, H., Papadopoulos, V., Vidic, B., Dym, M., and Culty, M. (1997). Regulation of rat testis gonocyte proliferation by platelet-derived growth factor and estradiol: identification of signaling mechanisms involved. Endocrinology 138, 1289-1298. doi:10.1210/EN.138.3.1289
26. Lo, K. C., Brugh, V. M., III, Parker, M., and Lamb, D. J. (2005). Isolation and enrichment of murine spermatogonial stem cells using rhodamine 123 mitochondrial dye. Biol. Reprod. 72, 767-771. doi:10.1095/BIOLREPROD.104.033464
27. Luo, J., Megee, S., Rathi, R., and Dobrinski, I. (2006). Protein gene product 9.5 is a spermatogonia-specific marker in the pig testis: application to enrichment and culture of porcine spermatogonia. Mol. Reprod. Dev. 73, 1531-1540. doi:10.1002/MRD.20529
28. Mustafa, A., Gillmeister, L., Hernandez, W. P., Larsen, C. T., Witonsky, S., Holladay, S. D., Kerr, R. P., Ahmed, S. A., Santo, A., and Gogal, R. M., Jr (2008). Viability and function in lymphocytes cultured from the horse, chicken, and mouse: effects of different leukocyte enrichment techniques. J. Immunoassay Immunochem. 29, 370-389. doi:10.1080/15321810802329823
29. Oatley, J. M., and Brinster, R. L. (2008). Regulation of spermatogonial stem cell self-renewal in mammals. Annu. Rev. Cell Dev. Biol. 24, 263-286. doi:10.1146/ANNUREV.CELLBIO.24.110707.175355
30. Ohbo, K., Yoshida, S., Ohmura, M., Ohneda, O., Ogawa, T., et al. (2003). Identification and characterization of stem cells in prepubertal spermatogenesis in mice. Dev. Biol. 258, 209-225. doi:10.1016/S0012-1606(03)00111-8
31. Ohmura, M., Yoshida, S., Ide, Y., Nagamatsu, G., Suda, T., and Ohbo, K. (2004). Spatial analysis of germ stem cell development in Oct-4/EGFP transgenic mice. Arch. Histol. Cytol. 67, 285-296. doi:10.1679/AOHC.67.285
32. Ohta, H., Wakayama, T., and Nishimune, Y. (2004). Commitment of fetal male germ cells to spermatogonial stem cells during mouse embryonic development. Biol. Reprod. 70, 1286-1291. doi:10.1095/BIOLREPROD.103.024612
33. Orth, J. M., and Boehm, R. (1990). Functional coupling of neonatal rat Sertoli cells and gonocytes in coculture. Endocrinology 127, 2812-2820. doi:10.1210/ENDO-127-6-2812
34. Orwig, K. E., Ryu, B.-Y., Avarbock, M. R., and Brinster, R. L. (2002). Male germ-line stem cell potential is predicted by morphology of cells in neonatal rat testes. Proc. Natl Acad. Sci. USA 99, 11 706-11 711. doi:10.1073/PNAS.182412099
35. Pelliniemi, L. J. (1975). Ultrastructure of the early ovary and testis in pig embryos. Am. J. Anat. 144, 89-111. doi:10.1002/AJA.1001440106
36. Ryu, B. Y., Orwig, K. E., Avarbock,M. R., and Brinster, R. L. (2003). Stem cell and niche development in the postnatal rat testis. Dev. Biol. 263, 253-263. doi:10.1016/J.YDBIO.2003.07.010
37. Ryu, B. Y., Orwig, K. E., Kubota, H., Avarbock, M. R., and Brinster, R. L. (2004). Phenotypic and functional characteristics of spermatogonial stem cells in rats. Dev. Biol. 274, 158-170. doi:10.1016/J.YDBIO.2004.07.004
38. Sethu, P., Anahtar, M., Moldawer, L. L., Tompkins, R. G., and Toner, M. (2004). Continuous flow microfluidic device for rapid erythrocyte lysis. Anal. Chem. 76, 6247-6253. doi:10.1021/AC049429P
39. Shinohara, T., Orwig, K. E., Avarbock, M. R., and Brinster, R. L. (2002). Germ line stem cell competition in postnatal mouse testes. Biol. Reprod. 66, 1491-1497. doi:10.1095/BIOLREPROD66.5.1491
40. Smith, K., Garman, L., Wrammert, J., Zheng, N.-Y., Capra, J. D., Ahmed, R., and Wilson, P. C. (2009). Rapid generation of fully human monoclonal antibodies specific to a vaccinating antigen. Nat. Protoc. 4, 372-384. doi:10.1038/NPROT.2009.3
41. van Dissel-Emiliani, F. M. F., de Rooji, D. G., and Meistrich, M. L. (1989). Isolation of rat gonocytes by velocity sedimentation at unit gravity. J. Reprod. Fertil. 86, 759-766. doi:10.1530/JRF.0.0860759
42. van Straaten, H. W., and Wensing, C. J. (1977). Histomorphometric aspects of testicular morphogenesis in the pig. Biol. Reprod. 17, 467-472. doi:10.1095/BIOLREPROD17.4.467
43. van Vorstenbosch, C. J., Colenbrander, B., and Wensing, C. J. (1984). Leydig cell development in the pig testis during the late fetal and early postnatal period: an electron microscopic study with attention to the influence of fetal decapitation. Am. J. Anat. 169, 121-136. doi:10.1002/AJA.1001690202