Conservation of avian germplasm by xenogeneic transplantation of spermatogonia from sexually mature donors

Stem Cells and Development

Volumn 22, Issue 5, 2013, Pages 735-749

  Pereira, Ricardo J G ^a,b   Napolitano, Angelo ^b   Garcia Pereira, Fernando L ^b   Baldo, Caroline F ^b   Suhr, Steven T ^b   King, Louis E ^c   Cibelli, Jose B ^b,d   Karcher, Darrin M ^b   McNiel, Elizabeth A ^b   Perez, Gloria I ^b,d  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c Michigan State University   (United States)

^d LARCel   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL STRUCTURE; CHICKEN; CONTROLLED STUDY; GAMMA IRRADIATION; GENETIC CONSERVATION; GERMPLASM; IMMUNOHISTOCHEMISTRY; MALE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; QUAIL; ROOSTER; SEMEN ANALYSIS; SPERMATOGENESIS; SPERMATOGONIUM; SPERMATOZOON; TESTIS CELL; XENOTRANSPLANTATION;

ANIMALS; BREEDING; CHICKENS; COTURNIX; ENDANGERED SPECIES; FEMALE; INSEMINATION, ARTIFICIAL; MALE; SPERMATOGENESIS; SPERMATOGONIA; SPERMATOZOA; TESTIS; TRANSPLANTATION, HETEROLOGOUS;

EID: 84874091640     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2012.0497     Document Type: Article

References (87)

1. IUCN. (2011). Red List Statistics, http://iucnredlist.org.
2. Snyder NFR, SR Derrickson, SR Beissinger, JW Wiley, TB Smith, WD Toone and B Miller. (1996). Limitations of captive breeding in endangered species recovery. Conserv Biol 10:338-348.
3. Fickel J, A Wagener and A Ludwig. (2007). Semen cryopreservation and the conservation of endangered species. Eur J Wild Res 53:81-89.
4. Blesbois E, I Grasseau, F Seigneurin, S Mignon-Grasteau, M Saint Jalme and MM Mialon-Richard. (2008). Predictors of success of semen cryopreservation in chickens. Theriogenology 69:252-261.
5. Blanco JM, G Gee, DE Wildt and AM Donoghue. (2000). Species variation in osmotic, cryoprotectant, and cooling rate tolerance in poultry, eagle, and peregrine falcon spermatozoa. Biol Reprod 63:1164-1171.
6. Gee F. (1994). Artificial insemination and cryopreservation of semen from nondomestic birds. In: First International Symposium on the Artificial Insemination of Poultry, University of Maryland, College Park, pp 262-279.
7. Saint Jalme M, R Lecoq, F Seigneurin, E Blesbois and E Plouzeau. (2003). Cryopreservation of semen from endangered pheasants: the first step towards a cryobank for endangered avian species. Theriogenology 59:875-888.
8. Kang SJ, JWChoi, KJ Park, YMLee, TMKim, SHSohn, JMLim and JY Han. (2009). Development of a pheasant interspecies primordial germ cell transfer to chicken embryo: effect of donor cell sex on chimeric semen production. Theriogenology 72:519-527.
9. Song Y and FG Silversides. (2008). Long-term production of donor-derived offspring from chicken ovarian transplants. Poult Sci 87:1818-1822.
10. Brinster RL and MR Avarbock. (1994). Germline transmission of donor haplotype following spermatogonial transplantation. Proc Natl Acad Sci USA 91:11303-11307.
11. Hamra FK, J Gatlin, KM Chapman, DM Grellhesl, JV Garcia, RE Hammer and DL Garbers. (2002). Production of transgenic rats by lentiviral transduction of male germ-line stem cells. Proc Natl Acad Sci U S A 99:14931-14936.
12. Jiang FX and RV Short. (1995). Male germ cell transplantation in rats: apparent synchronization of spermatogenesis between host and donor seminiferous epithelia. Int J Androl 18:326-330.
13. Kanatsu-Shinohara M, M Ikawa, M Takehashi, N Ogonuki, H Miki, K Inoue, Y Kazuki, J Lee, S Toyokuni, et al. (2006). Production of knockout mice by random or targeted mutagenesis in spermatogonial stem cells. Proc Natl Acad Sci U S A 103:8018-8023.
14. Ogawa T, I Dobrinski, MR Avarbock and RL Brinster. (2000). Transplantation of male germ line stem cells restores fertility in infertile mice. Nat Med 6:29-34.
15. Zhang Z, MB Renfree and RV Short. (2003). Successful intraand interspecific male germ cell transplantation in the rat. Biol Reprod 68:961-967.
16. Honaramooz A, E Behboodi, S Blash, SO Megee and I Dobrinski. (2003). Germ cell transplantation in goats. Mol Reprod Dev 64:422-428.
17. Honaramooz A, SO Megee and I Dobrinski. (2002). Germ cell transplantation in pigs. Biol Reprod 66:21-28.
18. Izadyar F, K Den Ouden, TA Stout, J Stout, J Coret, DP Lankveld, TJ Spoormakers, B Colenbrander, JK Oldenbroek, et al. (2003). Autologous and homologous transplantation of bovine spermatogonial stem cells. Reproduction 126:765-774.
19. Mikkola M, A Sironen, C Kopp, J Taponen, A Sukura, J Vilkki, T Katila and M Andersson. (2006). Transplantation of normal boar testicular cells resulted in complete focal spermatogenesis in a boar affected by the immotile short-tail sperm defect. Reprod Domest Anim 41:124-128.
20. Rodriguez-Rosa JR, H Dobson and A Hahnel. (2006). Isolation and transplantation of spermatogonia in sheep. Theriogenology 66:2091-2103.
21. Schlatt S, L Foppiani, C Rolf, GF Weinbauer and E Nieschlag. (2002). Germ cell transplantation into X-irradiated monkey testes. Hum Reprod 17:55-62.
22. Lacerda SM, SR Batlouni, GM Costa, TM Segatelli, BR Quirino, BM Queiroz, E Kalapothakis and LR Franca. (2010). A new and fast technique to generate offspring after germ cells transplantation in adult fish: the Nile tilapia (Oreochromis niloticus) model. PLoS One 5:e10740.
23. Okutsu T, S Shikina, M Kanno, Y Takeuchi and G Yoshizaki. (2007). Production of trout offspring from triploid salmon parents. Science 317:1517.
24. Okutsu T, K Suzuki, Y Takeuchi, T Takeuchi and G Yoshizaki. (2006). Testicular germ cells can colonize sexually undifferentiated embryonic gonad and produce functional eggs in fish. Proc Natl Acad Sci U S A 103:2725-2729.
25. Kalina J, F Senigl, A Micakova, J Mucksova, J Blazkova, H Yan, M Poplstein, J Hejnar and P Trefil. (2007). Retrovirusmediated in vitro gene transfer into chicken male germ line cells. Reproduction 134:445-453.
26. Lee YM, JG Jung, JN Kim, TS Park, TM Kim, SS Shin, DK Kang, JM Lim and JY Han. (2006). A testis-mediated germline chimera production based on transfer of chicken testicular cells directly into heterologous testes. Biol Reprod 75:380-386.
27. Song Y and FG Silversides. (2007). Production of offspring from cryopreserved chicken testicular tissue. Poult Sci 86:1390-1396.
28. Song Y and FG Silversides. (2007). Offspring produced from orthotopic transplantation of chicken ovaries. Poult Sci 86:107-111.
29. Trefil P, A Micakova, J Mucksova, J Hejnar, M Poplstein, MR Bakst, J Kalina and JP Brillard. (2006). Restoration of spermatogenesis and male fertility by transplantation of dispersed testicular cells in the chicken. Biol Reprod 75:575-581.
30. Dobrinski I. (2008). Male germ cell transplantation. Reprod Domest Anim 43 Suppl 2:288-294.
31. Russell LD and MD Griswold. (2000). Spermatogonial transplantation-an update for the millennium. Mol Cell Endocrinol 161:117-120.
32. Clouthier DE, MR Avarbock, SD Maika, RE Hammer and RL Brinster. (1996). Rat spermatogenesis in mouse testis. Nature 381:418-421.
33. Ogawa T, I Dobrinski, MR Avarbock and RL Brinster. (1999). Xenogeneic spermatogenesis following transplantation of hamster germ cells to mouse testes. Biol Reprod 60:515-521.
34. Ogawa T, I Dobrinski and RL Brinster. (1999). Recipient preparation is critical for spermatogonial transplantation in the rat. Tissue Cell 31:461-472.
35. Russell LD and RL Brinster. (1996). Ultrastructural observations of spermatogenesis following transplantation of rat testis cells into mouse seminiferous tubules. J Androl 17:615-627.
36. Dobrinski I, MR Avarbock and RL Brinster. (1999). Transplantation of germ cells from rabbits and dogs into mouse testes. Biol Reprod 61:1331-1339.
37. Dobrinski I, MR Avarbock and RL Brinster. (2000). Germ cell transplantation from large domestic animals into mouse testes. Mol Reprod Dev 57:270-279.
38. Kim Y, V Selvaraj, I Dobrinski, H Lee, MC McEntee and AJ Travis. (2006). Recipient preparation and mixed germ cell isolation for spermatogonial stem cell transplantation in domestic cats. J Androl 27:248-256.
39. Nagano M, JR McCarrey and RL Brinster. (2001). Primate spermatogonial stem cells colonize mouse testes. Biol Reprod 64:1409-1416.
40. Dobrinski I. (2005). Germ cell transplantation and testis tissue xenografting in domestic animals. Anim Reprod Sci 89:137-145.
41. Arregui L, R Rathi, SO Megee, A Honaramooz, M Gomendio, ER Roldan and I Dobrinski. (2008). Xenografting of sheep testis tissue and isolated cells as a model for preservation of genetic material from endangered ungulates. Reproduction 136:85-93.
42. Dobrinski I and AJ Travis. (2007). Germ cell transplantation for the propagation of companion animals, non-domestic and endangered species. Reprod Fertil Dev 19:732-739.
43. Honaramooz A, W Zeng, R Rathi, J Koster, O Ryder and I Dobrinski. (2005). Testis tissue xenografting to preserve germ cells from a cloned banteng calf. Reprod Fert Dev 17:247-247.
44. Snedaker AK, A Honaramooz and I Dobrinski. (2004). A game of cat and mouse: xenografting of testis tissue from domestic kittens results in complete cat spermatogenesis in a mouse host. J Androl 25:926-930.
45. Kang SJ, JW Choi, SY Kim, KJ Park, TM Kim, YM Lee, H Kim, JM Lim and JY Han. (2008). Reproduction of wild birds via interspecies germ cell transplantation. Biol Reprod 79:931-937.
46. Li ZD, H Deng, CH Liu, YH Song, J Sha, N Wang and H Wei. (2002). Production of duck-chicken chimeras by transferring early blastodermal cells. Poult Sci 81:1360-1364.
47. Wernery U, C Liu, V Baskar, Z Guerineche, KA Khazanehdari, S Saleem, J Kinne, R Wernery, DK Griffin and IK Chang. (2010). Primordial germ cell-mediated chimera technology produces viable pure-line Houbara bustard offspring: potential for repopulating an endangered species. PLoS One 5:e15824.
48. Lavial F and B Pain. (2010). Chicken embryonic stem cells as a non-mammalian embryonic stem cell model. Dev Growth Differ 52:101-114.
49. Park TS, YH Hong, SC Kwon, JM Lim and JY Han. (2003). Birth of germline chimeras by transfer of chicken embryonic germ (EG) cells into recipient embryos. Mol Reprod Dev 65:389-395.
50. Guan K, F Wolf, A Becker, W Engel, K Nayernia and G Hasenfuss. (2009). Isolation and cultivation of stem cells from adult mouse testes. Nat Protoc 4:143-154.
51. Lin M and RC Jones. (1992). Renewal and proliferation of spermatogonia during spermatogenesis in the Japanese quail, Coturnix coturnix japonica. Cell Tissue Res 267:591-601.
52. Jones RC and M Lin. (1993). Spermatogenesis in birds. Oxf Rev Reprod Biol 15:233-264.
53. Burrows WH and JP Quinn. (1937). The collection of spermatozoa from the domestic fowl and turkey. Poult Sci 23:15-20.
54. Soh T, Y Inoue, YM Xi, Y Kato and MA Hattori. (2004). Production of interspecific germline chimera between quail and chicken utilizing the cells from central disk of blastoderm and germinal crescent region. J Fac Agr 49:69-75.
55. Liu CH, IK Chang, J Sasse, CJ Dumatol, JV Basker and U Wernery. (2007). Xenogenic oogenesis of chicken (Gallus domesticus) female primordial germ cells in germline chimeric quail (Coturnix japonica) ovary. Anim Reprod Sci 101:344-350.
56. D'Costa S, SL Pardue and JN Petitte. (2002). Production of interspecific embryonic germ line chimeras by the intravascular transfer of gonadal PGCs. Transgenic Res 11:84.
57. Han JY. (2009). Germ cells and transgenesis in chickens. Comp Immunol Microbiol Infect Dis 32:61-80.
58. Jung JG, YM Lee, JN Kim, TM Kim, JH Shin, TH Kim, JM Lim and JY Han. (2010). The reversible developmental unipotency of germ cells in chicken. Reproduction 139:113-119.
59. Nagano M, P Patrizio and RL Brinster. (2002). Long-term survival of human spermatogonial stem cells in mouse testes. Fertil Steril 78:1225-1233.
60. Fijak M, S Bhushan and A Meinhardt. (2011). Immunoprivileged sites: the testis. Methods Mol Biol 677:459-470.
61. Herrid M, S Vignarajan, R Davey, I Dobrinski and JR Hill. (2006). Successful transplantation of bovine testicular cells to heterologous recipients. Reproduction 132:617-624.
62. Honaramooz A, E Behboodi, SO Megee, SA Overton, H Galantino-Homer, Y Echelard and I Dobrinski. (2003). Fertility and germline transmission of donor haplotype following germ cell transplantation in immunocompetent goats. Biol Reprod 69:1260-1264.
63. Mital P, G Kaur and JM Dufour. (2010). Immunoprotective sertoli cells: making allogeneic and xenogeneic transplantation feasible. Reproduction 139:495-504.
64. Tanaka A, M Nagayoshi, M Awata, Y Mawatari, I Tanaka and N Sofikitis. (1997). Conclusions from the transplantation of human or hamster spermatogonia/primary spermatocytes to rat or mouse testis. Fertil Steril 68:S61.
65. Shinohara T, KE Orwig, MR Avarbock and RL Brinster. (2001). Remodeling of the postnatal mouse testis is accompanied by dramatic changes in stem cell number and niche accessibility. Proc Natl Acad Sci U S A 98:6186-6191.
66. Herrid M, J Olejnik, M Jackson, N Suchowerska, S Stockwell, R Davey, K Hutton, S Hope and JR Hill. (2009). Irradiation enhances the efficiency of testicular germ cell transplantation in sheep. Biol Reprod 81:898-905.
67. Honaramooz A and Y Yang. (2010). Recent advances in application of male germ cell transplantation in farm animals. Vet Med Intpii:657860.
68. Zhang Z, S Shao and ML Meistrich. (2006). Irradiated mouse testes efficiently support spermatogenesis derived from donor germ cells of mice and rats. J Androl 27:365-375.
69. Trefil P, J Polak, M Poplstein, T Mikus, A Kotrbova and J Rozinek. (2003). Preparation of fowl testes as recipient organs to germ-line chimeras by means of gamma-radiation. Br Poult Sci 44:643-650.
70. Herrid M, RJ Davey, K Hutton, IG Colditz and JR Hill. (2009). A comparison of methods for preparing enriched populations of bovine spermatogonia. Reprod Fertil Dev 21:393-399.
71. Kim BG, CM Cho, YA Lee, BJ Kim, KJ Kim, YH Kim, KS Min, CG Kim and BY Ryu. (2010). Enrichment of testicular gonocytes and genetic modification using lentiviral transduction in pigs. Biol Reprod 82:1162-1169.
72. Luo J, S Megee, R Rathi and I Dobrinski. (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.
73. Orwig KE, T Shinohara, MR Avarbock and RL Brinster. (2002). Functional analysis of stem cells in the adult rat testis. Biol Reprod 66:944-949.
74. Shinohara T, MR Avarbock and RL Brinster. (1999). Beta1-and alpha6-integrin are surface markers on mouse spermatogonial stem cells. Proc Natl Acad Sci U S A 96:5504-5509.
75. Trefil P, MR Bakst, H Yan, J Hejnar, J Kalina and J Mucksova. (2010). Restoration of spermatogenesis after trans-plantation of c-Kit positive testicular cells in the fowl. Theriogenology 74:1670-1676.
76. Hu KX, QY Sun, M Guo and HS Ai. (2010). The radiation protection and therapy effects of mesenchymal stem cells in mice with acute radiation injury. Br J Radiol 83:52-58.
77. Lange C, B Brunswig-Spickenheier, H Cappallo-Obermann, K Eggert, UM Gehling, C Rudolph, B Schlegelberger, K Cornils, J Zustin, AN Spiess and AR Zander. (2011). Radiation rescue: mesenchymal stromal cells protect from lethal irradiation. PLoS One 6:e14486.
78. Li T and Y Wu. (2011). Paracrine molecules of mesenchymal stem cells for hematopoietic stem cell niche. Bone Marrow Res 2011:353878.
79. Guitton N, AM Touzalin, RM Sharpe, CY Cheng, G Pinon-Lataillade, H Meritte, C Chenal and B Jegou. (2000). Regulatory influence of germ cells on sertoli cell function in the pre-pubertal rat after acute irradiation of the testis. Int J Androl 23:332-339.
80. O'Shaughnessy PJ, L Hu and PJ Baker. (2008). Effect of germ cell depletion on levels of specific mRNA transcripts in mouse Sertoli cells and Leydig cells. Reproduction 135:839-850.
81. Vidal F, P Lopez, LA Lopez-Fernandez, F Ranc, JC Scimeca, F Cuzin and M Rassoulzadegan. (2001). Gene trap analysis of germ cell signaling to Sertoli cells: NGF-TrkA mediated induction of Fra1 and Fos by post-meiotic germ cells. J Cell Sci 114:435-443.
82. Fujino RS, K Tanaka, M Morimatsu, K Tamura, H Kogo and T Hara. (2006). Spermatogonial cell-mediated activation of an IkappaBzeta-independent nuclear factor-kappaB pathway in Sertoli cells induces transcription of the lipocalin-2 gene. Mol Endocrinol 20:904-915.
83. Korn N, RJ Thurston, BP Pooser and TR Scott. (2000). Ultrastructure of spermatozoa from Japanese quail. Poult Sci 79:407-414.
84. Aubele M, U Jutting, K Rodenacker, P Gais, G Burger and U Hacker-Klom. (1990). Quantitative evaluation of radiationinduced changes in sperm morphology and chromatin distribution. Cytometry 11:586-594.
85. Otitoloju AA, IA Obe, OA Adewale, OA Otubanjo and VO Osunkalu. (2010). Preliminary study on the induction of sperm head abnormalities in mice, Mus musculus, exposed to radiofrequency radiations from global system for mobile communication base stations. Bull Environ Contam Toxicol 84:51-54.
86. Shin SC, YM Kang, YW Jin and HS Kim. (2009). Relative morphological abnormalities of sperm in the caudal epididymis of high-and low-dose-rate gamma-irradiated ICR mice. J Radiat Res 50:261-266.
87. Woon JH, SC Shin, YM Kang and HS Kim. (2011). Sperm abnormalities in high-and low-dose-rate gamma-irradiated Korean dark-striped field mice, Apodemus agrarius coreae. Radiat Prot Dosimetry 146:280-282.