Mouse spermatogonial stem cells obtain morphologic and functional characteristics of hematopoietic cells in vivo

Human Reproduction

Volumn 25, Issue 12, 2010, Pages 3101-3109

  Ning, Liang ^a,b   Goossens, Ellen ^a   Geens, Mieke ^a   Van Saen, Dorien ^a   Van Riet, Ivan ^a   He, Dalin ^b   Tournaye, Herman ^a,c  

^a VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^b XI'AN JIAOTONG UNIVERSITY   (China)

^c CENTRE FOR REPRODUCTIVE MEDICINE   (Belgium)

Author keywords

hematopoietic cells; pluripotent stem cells; spermatogonial stem cells; stem cell plasticity; transdifferentiation

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD CELL; BONE MARROW; CELL FUNCTION; CELL STRUCTURE; CELL SURVIVAL; FEMALE; HEMATOPOIETIC CELL; MALE; MOUSE; NONHUMAN; PHENOTYPE; SPERMATOGONIUM; SPLEEN CELL; STEM CELL; Y CHROMOSOME;

MURINAE; MUS;

EID: 78649509417     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/deq269     Document Type: Article

References (32)

1. Baeyens L, Bouwens L. Can beta-cells be derived from exocrine pancreas. Diabetes Obes Metab 2008;10(Suppl 4):170-178.
2. Challen GA, Boles N, Lin KK, Goodell MA. Mouse hematopoietic stem cell identification and analysis. Cytometry A 2009;75:14-24.
3. Conrad S, Renninger M, Hennenlotter J, Wiesner T, Just L, Bonin M, Aicher W, Buhring HJ, Mattheus U, Mack A. et al. Generation of pluripotent stem cells from adult human testis. Nature 2008; 456:344-349.
4. Dobrinski I, Ogawa T, Avarbock MR, Brinster RL. Effect of the GnRH-agonist leuprolide on colonization of recipient testes by donor spermatogonial stem cells after transplantation in mice. Tissue Cell 2001;33:200-207.
5. Eberhard D, Tosh D. Transdifferentiation and metaplasia as a paradigm for understanding development and disease. Cell Mol Life Sci 2008; 65:33-40.
6. Glaser T, Opitz T, Kischlat T, Konang R, Sasse P, Fleischmann BK, Engel W, Nayernia K, Brustle O. Adult germ line stem cells as a source of functional neurons and glia. Stem Cells 2008;26:2434-2443.
7. Golestaneh N, Kokkinaki M, Pant D, Jiang J, DeStefano D, Fernandez-Bueno C, Rone JD, Haddad BR, Gallicano GI, Dym M. Pluripotent stem cells derived from adult human testes. Stem Cells Dev 2009;18:1115-1126.
8. Goossens E, Frederickx V, De Block G, Van Steirteghem AC, Tournaye H. Reproductive capacity of sperm obtained after germ cell transplantation in a mouse model. Hum Reprod 2003;18:1874-1880.
9. Guan K, Nayernia K, Maier LS, Wagner S, Dressel R, Lee JH, Nolte J, Wolf F, Li M, Engel W, Hasenfuss G. Pluripotency of spermatogonial stem cells from adult mouse testis. Nature 2006;440:1199-1203.
10. Guan K, Wagner S, Unsold B, Maier LS, Kaiser D, Hemmerlein B, Nayernia K, Engel W, Hasenfuss G. Generation of functional cardiomyocytes from adult mouse spermatogonial stem cells. Circ Res 2007;100:1615-1625.
11. Huang X, Cho S, Spangrude GJ. Hematopoietic stem cells: generation and self-renewal. Cell Death Differ 2007;14:1851-1859.
12. Izadyar F, Pau F, Marh J, Slepko N, Wang T, Gonzalez R, Ramos T, Howerton K, Sayre C, Silva F. Generation of multipotent cell lines from a distinct population of male germ line stem cells. Reproduction 2008;135:771-784.
13. Kanatsu-Shinohara M, Shinohara T. The germ of pluripotency. Nat Biotechnol 2006;24:663-664.
14. Kanatsu-Shinohara M, Inoue K, Lee J, Yoshimoto M, Ogonuki N, Miki H, Baba S, Kato T, Kazuki Y, Toyokuni S. et al. Generation of pluripotent stem cells from neonatal mouse testis. Cell 2004a;119:1001-1012.
15. Kanatsu-Shinohara M, Toyokuni S, Shinohara T. CD9 is a surface marker on mouse and rat male germline stem cells. Biol Reprod 2004b; 70:70-75.
16. Kanatsu-Shinohara M, Lee J, Inoue K, Ogonuki N, Miki H, Toyokuni S, Ikawa M, Nakamura T, Ogura A, Shinohara T. Pluripotency of a single spermatogonial stem cell in mice. Biol Reprod 2008;78: 681-687.
17. Kossack N, Meneses J, Shefi S, Nguyen HN, Chavez S, Nicholas C, Gromoll J, Turek PJ, Reijo-Pera RA. Isolation and characterization of pluripotent human spermatogonial stem cell-derived cells. Stem Cells 2009;27:138-149.
18. Kubota H, Brinster RL. Technology insight: in vitro culture of spermatogonial stem cells and their potential therapeutic uses. Nat Clin Pract Endocrinol Metab 2006;2:99-108.
19. Kubota H, Avarbock MR, Brinster RL. Spermatogonial stem cells share some, but not all, phenotypic and functional characteristics with other stem cells. Proc Natl Acad Sci USA 2003;100: 6487-6492.
20. Kushida T, Inaba M, Hisha H, Ichioka N, Esumi T, Ogawa R, Iida H, Ikehara S. Intra-bone marrow injection of allogeneic bone marrow cells: a powerful new strategy for treatment of intractable autoimmune diseases in MRL/lpr mice. Blood 2001;97:3292-3299.
21. 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.
22. Nagano M, Brinster RL. Spermatogonial transplantation and reconstitution of donor cell spermatogenesis in recipient mice. APMIS 1998; 106:47-55; discussion 56-47
23. Shinohara T, Avarbock MR, Brinster RL. beta1- and alpha6-integrin are surface markers on mouse spermatogonial stem cells. Proc Natl Acad Sci USA 1999;96:5504-5509.
24. Simon L, Ekman GC, Kostereva N, Zhang Z, Hess RA, Hofmann MC, Cooke PS. Direct transdifferentiation of stem/progenitor spermatogonia into reproductive and nonreproductive tissues of all germ layers. Stem Cells 2009;27:1666-1675.
25. Slack JM. Metaplasia and transdifferentiation: from pure biology to the clinic. Nat Rev Mol Cell Biol 2007;8:369-378.
26. Streckfuss-Bomeke K, Vlasov A, Hulsmann S, Yin D, Nayernia K, Engel W, Hasenfuss G, Guan K. Generation of functional neurons and glia from multipotent adult mouse germ-line stem cells. Stem Cell Res 2009; 2:139-154.
27. Thowfeequ S, Myatt EJ, Tosh D. Transdifferentiation in developmental biology, disease, and in therapy. Dev Dyn 2007;236:3208-3217.
28. Van Saen D, Goossens E, De Block G, Tournaye H. Bone marrow stem cells transplanted to the testis of sterile mice do not differentiate into spermatogonial stem cells and have no protective effect on fertility. Fertil Steril 2009a;91:1549-1552.
29. Van Saen D, Goossens E, De Block G, Tournaye H. Regeneration of spermatogenesis by grafting testicular tissue or injecting testicular cells into the testes of sterile mice: a comparative study. Fertil Steril 2009b; 91:2264-2272.
30. Wagers AJ, Weissman IL. Plasticity of adult stem cells. Cell 2004; 116:639-648.
31. Yamanaka S. Strategies and new developments in the generation of patient-specific pluripotent stem cells. Cell Stem Cell 2007;1:39-49.
32. Yoshimoto M, Heike T, Chang H, Kanatsu-Shinohara M, Baba S, Varnau JT, Shinohara T, Yoder MC, Nakahata T. Bone marrow engraftment but limited expansion of hematopoietic cells from multipotent germ line stem cells derived from neonatal mouse testis. Exp Hematol 2009; 37:1400-1410.