Improvement of Expression of α6 and β1 Integrins by the Co-culture of Adult Mouse Spermatogonial Stem Cells with SIM Mouse Embryonic Fibroblast Cells (STO) and Growth Factors

Document Type: Original Article


1 Department of Anatomy Sciences, Faculty of Medicine, Tehran University of Medical Sciences, Tehran, Iran

2 Research Center, Iran’s Blood Transfusion Organization (IBTO), Tehran, Iran


Oatley JM, Brinster RL. Spermatogonial stem cells. Methods Enzy
mol 2006; 419:259-282.
2. Dadoune JP. New insights into male gametogenesis: what about the spermatogonial stem cell niche? Folia Histochem Cytobiol 2007; 45:141-147.
3. De Rooij D, Russell L. All you wanted to know about spermatogonia but were afraid to ask. J Androl 2000; 21:776-789.
4. Khaira H, McLean D, Ohl DA, Smith GD. Spermatogonial stem cell isolation, storage, and transplantation. J Androl 2005; 26:442- 450.
5. Shinohara T, Avarbock MR, Brinster RL. beta1- and alpha6-integrin are surface markers on mouse spermatogonial stem cells. Proc Natl Acad Sci 1999; 96:5504-5509.
6. Dirami G, Ravindranath N, Pursel V. Effects of stem cell factor and granulocyte macrophage-colony stimulating factor on survival of porcine type A spermatogonia cultured in KSOM. Biol Reprod 1999; 61:225-230.
7. Morena A, Boitani C, Pesce M, De Felici M, Stefanini M. Isolation of highly purified type A spermatogonia from prepubertal rat testis. J Androl 1996; 17:708-118.
8. Izadyar F, Ouden K, Creemers LB, Posthuma G, Parvinen M, de Rooij D. Proliferation and differentiation of bovine type A spermatogonia during long-term culture. Biol Reprod 2003; 68:272- 278.
9. Guan K, Wolf F, Becker A, Engel W, Nayernia K, Hasenfuss G. Isolation and cultivation of stem cells from adult mouse testes. Nat Protoc 2009; 4:143-154.
10. Kubota H, Avarbock MR, Brinster RL. Culture conditions and single growth factors affect fate determination of mouse spermatogonial stem cells. Biol Reprod 2004; 71:722-731.
11. Van der Wee K, Johnson EW, Dirami G, Dym TM, Hofmann MC. Immunomagnetic isolation and long-term culture of mouse type A spermatogonia. J Androl 2001; 22:696-704.
12. Aslam I, Robins A, Dowell K, Fishel S. Isolation, purification and assessment of viability of spermatogenic cells from testicular biopsies of azoospermic men. Hum Reprod 1998; 13:639-647.
13. Hamra FK, Schultz N , Chapman KM. Defining the spermatogonial stem cell. Dev Biol 2004; 269:393-410.
14. Yeh J, Nagano M. Spermatogonial stem cell biomarkers: improved outcomes of spermatogonial transplantation in male fertility restoration? Expert Rev Mol Diagn 2009; 9:109-114.
15. Sofikitis N, Pappas E, Kawatani A , Baltogiannis D , Loutradis D , Kanakas N,
et al
. Efforts to create an artificial testis: culture systems of male germ cells under biochemical conditions resembling the seminiferous tubular biochemical environment. Hum Reprod Update 2005; 11: 229-259.
16. De Rooij DG. Regulation of the proliferation of spermatogonial
stem cells. J Cell Sci Suppl 1988; 10: 181-194.
17. Nagano M, Avarbock MR, Leonida EB, Brinster CJ .Culture of mouse spermatogonial stem cells. Tissue Cell 1998; 30:389-97.
18. Feng L, Chen Y, Dettin L, Reijo Pera RA, Herr J, Goldberg E,
et al. Generation and in vitro
differentiation of a spermatogonial cell line. Science 2002; 297:392-399.
19. Wahab-Wahlgren A, Martinelle N, Holst M. EGF stimulates rat spermatogonial DNA synthesis in seminiferous tubule segments
in vitro
. Mol Cell Endocrinol 2003; 201:39-46.
20. Kubota H, Avarbock MR, Brinster RL. Growth factors essential for self-renewal and expansion of mouse spermatogonial stem cells. Proc Natl Acad Sci 2004; 101:16489-16494.
21. Meng X, Lindahl M, Hyvönen M, Parvinen M, de Rooij D, Hess MW,
et al
. Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science 2000; 287:1489-1493.
22. Creemers L, Meng X, Ouden K, van Pelt A MM, Izadyar F, Santoro M,
et al
. Transplantation of germ cells from glial cell line-derived neurotrophic factor-overexpressing mice to host testes depleted of endogenous spermatogenesis by fractionated irradiation. Biol Repod 2002; 66:1579-1685.
23. Aponte PM, Soda T, Van De Kant HJG, de Rooij DG. Basic features of bovine spermatogonial culture and effects of glial cell line-derived neurotrophic factor. Theriogenology 2006; 65:1828-1847.
24. Kanatsu-Shinohara M, Ogonuki N, Inoue K, Miki H, Ogura A, Toyokuni Sh. Long-term proliferation in culture and germline transmission of mouse male germline stem cells. Biol Reprod 2003; 69:612-616.
25. Paratcha G, Ledda F, Ibáñez CF. Released GFR (alpha) 1 potentiates downstream signaling, neuronal survival, and differentiation via a novel mechanism of recruitment of c-Ret to lipid rafts. Neuron 2001; 29:171-184.
26. Yomogida K, Yagura Y, Tadokoro Y, Nishimune Y. Dramatic expansion of germinal stem cells by ectopically expressed human glial cell line-derived neurotrophic factor in mouse Sertoli cells. Biol Reprod 2003; 69:1303-1309.
27. Haneji T, Koide SS, Tajima Y, Nishimune Y. Differential effects of epidermal growth factor on the differentiation of type A spermatogonia in adult mouse cryptorchid testes
in vitro
. J Endocrinol 1991; 128:383-389.