Transplantation of Goat Bone Marrow Mesenchymal Stem Cells (gMSCs) Help Restore Spermatogenesis in Endogenous Germ Cells-Depleted Mouse Models

Journal of Integrative Agriculture

Volumn 12, Issue 3, 2013, Pages 483-494

  WANG, Fang ^a   LIU, Chao ^a   ZHANG, Shan shan ^a   LIU, Wei shuai ^b   HUA, Jin lian ^a  

^a NORTHWEST A F UNIVERSITY   (China)

^b Yangling Demonstration Zone Hospital   (China)

Author keywords

Dairy goat bone marrow mesenchymal stem cells (gMSCs); Male germ cells; Spermatogenesis; Spermatozoa

Indexed keywords

ANIMALIA; CAPRA HIRCUS;

EID: 84875762796     PISSN: 20953119     EISSN: None     Source Type: Journal    
DOI: 10.1016/S2095-3119(13)60249-X     Document Type: Article

References (51)

1. Abrishami M, Anzar M, Yang Y, Honaramooz A Cryopreservation of immature porcine testis tissue to maintain its developmental potential after xenografting into recipient mice. Theriogenology 2010, 73:86-96.
2. Abbasi S, Honaramooz A The number of grafted fragments affects the outcome of testis tissue xenografting frompiglets into recipientmice. Veterinary Medicine International 2011, 10.4061/2011/686570.
3. Anderson EL, Baltus AE, Roepers-Gajadien HL, Hassold TJ, de Rooij DG, van Pelt AMM, Page DC Stra8 and its inducer, retinoic acid, regulate meiotic initiation in both spermatogenesis and oogenesis in mice. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:14976-14980.
4. Brinster RL Germline stem cell transplantation and ransgenesis. Science 2002, 296:2174-2176.
5. Brinster RL, Zimmermann JW Spermatogenesis following male germ-cell transplantation. Proceedings of the National Academy of Sciences of the United States of America 1994, 91:11298-11302.
6. Cao H, Chu Y, Zhu H, Sun J, Pu Y, Gao Z, Yang C, Peng S, Dou Z, Hua J Characterization of immortalized mesenchymal stem cells derived from fetal porcine pancreas. Cell Proliferation 2011, 44:19-32.
7. Clark AT, Bodnar MS, Fox M, Rodriquez RT, Abeyta MJ, Firpo MT, Pera RAR Spontaneous differentiation of germ cells from human embryonic stem cells in vitro. Human Molecular Genetics 2004, 13:727-739.
8. Danner S, Kajahn J, Geismann C, Klink E, Kruse C Derivation of oocyte-like cells from a clonal pancreatic stem cell line. Molecular Human Reproduction 2007, 13:11-20.
9. Dobrinski I, Avarbock MR, Brinster RL Germ cell transplantation from large domestic animals into mouse testes. Molecular Reproduction and Development 2000, 57:270-279.
10. Drusenheimer N, Wulf G, Nolte J, Lee JH, Dev A, Dressel R, Gromoll J, Schmidtke J, Engel W, Nayernia K Putative human male germ cells from bone marrow stem cells. Society of Reproduction and Fertility Supplement 2007, 63:69-76.
11. Dyce PW, Wen LH, Li JL In vitro germline potential of stem cells derived from fetal porcine skin. Nature Cell Biology 2006, 8:384. 350.
12. Geijsen N, Horoschak M, Kim K, Gribnau J, Eggan K, Daley GQ Derivation of embryonic germ cells and male gametes from embryonic stem cells. Nature 2004, 427:148-154.
13. He Z, Jiang J, Hofmann MC, Dym M Gfra1 silencing in mouse spermatogonial stem cells results in their differentiation via the inactivation of ret tyrosine kinase. Biology of Reproduction 2007, 77:723-733.
14. Hill JR, Dobrinski I Male germ cell transplantation in livestock. Reproduction, Fertility and Development 2006, 18:13-18.
15. Honaramooz A, Behboodi E, Megee SO, Overton SA, Galantino-Homer H, Echelard Y, Dobrinski I Fertility and germline transmission of donor haplotype following germ cell transplantation in immunocompetent goats. Biology of Reproduction 2003, 69:1260-1264.
16. Hua JL, Pan SH, Yang CR, Dong WZ, Dou ZY, Sidhu KS Derivation of male germ cell-like lineage from human fetal bone marrow stern cells. Reproductive Biomedicine Online 2009, 19:99-105.
17. Hubner K, Fuhrmann G, Christenson LK, Kehler J, Reinbold R, de La Fuente R, Wood J, Strauss JF, Boiani M, Scholer HR Derivation of oocytes from mouse embryonic stem cells. Science 2003, 300:1251-1256.
18. Iammarrone E, Balet R, Gillott C, Grudzinskas JG Male infertility. Best Practice & Research Clinical Obstetrics & Gynaecology 2003, 17:211-229.
19. Izadyar F, Den Ouden K, Stout TAE, Stout J, Coret J, Lankveld DPK, Spoormakers TJP, Colenbrander B, Oldenbroek JK, van der Ploeg KD, et al. Autologous and homologous transplantation of bovine spermatogonial stem cells. Reproduction 2003, 126:765-774.
20. Jiang YH, Jahagirdar BN, Reinhardt RL, Schwartz RE, Keene CD, Ortiz-Gonzalez XR, Reyes M, Lenvik T, Lund T, Blackstad M, et al. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002, 418:41-49.
21. Kee K, Angeles VT, Flores M, Nguyen HN, Pera RAR Human DAZL, DAZ and BOULE genes modulate primordial germ-cell and haploid gamete formation. Nature 2009, 462:222-225.
22. Ko K, Tapia N, Wu G, Kim JB, Bravo MJA, Sasse P, Glaser T, Ruau D, Han DW, Greber B, et al. Induction of pluripotency in adult unipotent germline stem cells. Cell Stem Cell 2009, 5:87-96.
23. Koubova J, Menke DB, Zhou Q, Capel B, Griswold MD, Page DC Retinoic acid regulates sex-specific timing of meiotic initiation in mice. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:2474-2479.
24. Lambard S, Galeraud-Denis I, Martin G, Levy R, Chocat A, Carreau S Analysis and significance of mRNA in human ejaculated sperm from normozoospermic donors: relationship to sperm motility and capacitation. Molecular Human Reproduction 2004, 10:535-541.
25. Lassalle B, Mouthon MA, Riou L, Barroca V, Coureuil M, Boussin F, Testart J, Allemand I, Fouchet P Bone marrow-derived stem cells do not reconstitute spermatogenesis in vivo. Stem Cells 2008, 26:1385-1386.
26. Lee DR, Kim KS, Yang YH, Oh HS, Lee SH, Chung TG, Cho JH, Kim HJ, Yoon TK, Cha KY Isolation of male germ stem cell-like cells from testicular tissue of non-obstructive azoospermic patients and differentiation into haploid male germ cells in vitro. Human Reproduction 2006, 21:471-476.
27. Li W, Dou Z, Hua J, Wang H Activation of stra 8 gene during the differentiation of spermatogonial stem cells. Chinese Journal of Biotechnology 2007, 23:639-644. (in Chinese).
28. Liu FH, Yang DZ, Wang YF, Liang XP, Peng WM, Cao CA, Chen XG, Guo ZM Mesenchymal stem cells do not differentiate into "quasi-sperm" Zhonghua Nan Ke Xue 2007, 13:309-311. (in Chinese).
29. Lue Y, Erkkila K, Liu PY, Ma K, Wang C, Hikim AS, Swerdloff RS Fate of bone marrow stem cells transplanted into the testis-potential implication for men with testicular failure. American Journal of Pathology 2007, 170:899-908.
30. Mansouri A, Phi-van L, Geithe HP, Engel W Proacrosin/acrosin activity during spermiohistogenesis of the bull. Differentiation 1983, 24:149-152.
31. Nagano M, Brinster CJ, Orwig KE, Ryu BY, Avarbock MR, Brinster RL Transgenic mice produced by retroviral transduction of male germ-line stem cells. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:13090-13095.
32. Nakai M, Kaneko H, Somfai T, Maedomari N, Ozawa M, Noguchi J, Ito J, Kashiwazaki N, Kikuchi K Production of viable piglets for the first time using sperm derived from ectopic testicular xenografts. Reproduction 2010, 139:331-335.
33. Nayernia K, Lee JH, Drusenheimer N, Nolte J, Wulf G, Dressel R, Gromoll J, Engel W Derivation of male germ cells from bone marrow stem cells. Laboratory Investigation 2006, 86:654-663.
34. Nayernia K, Li MY, Jaroszynski L, Khusainov R, Wulf G, Schwandt I, Korabiowska M, Michelmann HW, Meinhardt A, Engel W Stem cell based therapeutical approach of male infertility by teratocarcinoma derived germ cells. Human Molecular Genetics 2004, 13:1451-1460.
35. Nayernia K, Nolte J, Michelmann HW, Lee JH, Rathsack K, Drusenheimer N, Dev A, Wulf G, Ehrmann IE, Elliott DJ, et al. In vitro-differentiated embryonic stem cells give rise to male gametes that can generate offspring mice. Developmental Cell 2006, 11:125-132.
36. Oatley JM, de Avila DM, McLean DJ, Griswold MD, Reeves JJ Transplantation of bovine germinal cells into mouse testes. Journal of Animal Science 2002, 80:1925-1931.
37. Oatley JM, Reeves JJ, McLean DJ Establishment of spermatogenesis in neonatal bovine testicular tissue following ectopic xenografting varies with donor age. Biology of Reproduction 2005, 72:358-364.
38. Ogawa T, Arechaga JM, Avarbock MR, Brinster RL Transplantation of tesis germinal cells into mouse seminiferous tubules. International Journal of Development Biology 1997, 41:111-122.
39. Oulad-Abdelghani M, Bouillet P, Decimo D, Gansmuller A, Heyberger S, Dolle P, Bronner S, Lutz Y, Chambon P Characterization of a premeiotic germ cell-specific cytoplasmic protein encoded by Stra8, a novel retinoic acid-responsive gene. Journal of Cell Biology 1996, 135:469-477.
40. Pawar SS, Malakar D, De AK, Akshey YS Stem cell-like outgrowths from in vitro fertilized goat blastocysts. Indian Journal of Experiment Biology 2009, 47:635-642.
41. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR Multilineage potential of adult human mesenchymal stem cells. Science 1999, 284:143-147.
42. Rathi R, Honaramooz A, Zeng W, Turner R, Dobrinski I Germ cell development in equine testis tissue xenografted into mice. Reproduction 2006, 131:1091-1098.
43. Revel A, Revel-Vilk S Fertility preservation in young cancer patients. Journal of Human Reproductive Sciences 2010, 3:2-7. (in Chinese).
44. Shao ZH, Wang PJ, Li MH, Zhang W, Zheng SQ, Zhao XH, Wang GL, Shang MY, Mao XQ Effects of mesenchymal stem cell transplantation on growth of liver cancer: experiment with rats. Zhonghua Yi Xue Za Zhi 2009, 89:491-496. (in Chinese).
45. Shen FJ, Zhang C, Zheng HY, Xiong YH, Wang X, Liao WB, Du XJ, Yang SX, Wang LL Long-term culture and transplantation of spermatogonial stem cells from BALB/c mice. Cells Tissues Organs 2010, 191:372-381.
46. Toyooka Y, Tsunekawa N, Akasu R, Noce T Embryonic stem cells can form germ cells in vitro. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:11457-11462.
47. Wang DZ, Zhou XH, Yuan YL, Zheng XM Optimal dose of busulfan for depleting testicular germ cells of recipient mice before spermatogonial transplantation. Asian Journal of Andrology 2010, 12:263-270.
48. Yazawa T, Mizutani T, Yamada K, Kawata H, Sekiguchi T, Yoshino M, Kajitani T, Shou Z, Umezawa A, Miyamoto K Differentiation of adult stem cells derived from bone marrow stroma into leydig or adrenocortical cells. Endocrinology 2006, 147:4104-4111.
49. Yu F, Ding LJ, Sun GB, Sun PX, He XH, Ni LG, Li BC Transgenic sperm produced by electrotransfection and allogeneic transplantation of chicken fetal spermatogonial stem cells. Molecular Reproduction and Development 2010, 77:340-347.
50. Zhang Z, Shao S, Shetty G, Meistrich ML Donor Sertoli cells transplanted into irradiated rat testes stimulate partial recovery of endogenous spermatogenesis. Reproduction 2009, 137:497-508.
51. Zhang Y, Shen W, Hua J, Lei A, Lv C, Wang H, Yang C, Gao Z, Dou Z Pancreatic islet-like clusters from bone marrow mesenchymal stem cells of human first-trimester abortus can cure streptozocin-induced mouse diabetes. Rejuvenation Research 2010, 13:695-706.