Functional demonstration of the ability of a primary spermatogonium as a stem cell by tracing a single cell destiny in Xenopus laevis

Development Growth and Differentiation

Volumn 48, Issue 8, 2006, Pages 525-535

  Kawasaki, Toshihiro ^a   Imura, Fumito ^a   Nakada, Akira ^a   Kubota, Hiroshi ^a   Sakamaki, Kazuhiro ^b   Abe, Shin Ichi ^a   Takamune, Kazufumi ^a  

^a KUMAMOTO UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

Spermatogenesis; Stem cell; Testis; Xenopus

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL SIZE; DEVELOPMENTAL STAGE; FEMALE; MALE; MITOSIS; NONHUMAN; SPERMATOGONIUM; STEM CELL; TESTIS; XENOPUS LAEVIS;

ANIMALS; MALE; MITOSIS; ORGAN CULTURE TECHNIQUES; SPERMATOGONIA; STEM CELLS; TESTIS; XENOPUS LAEVIS;

XENOPUS LAEVIS;

EID: 33749416306     PISSN: 00121592     EISSN: 1440169X     Source Type: Journal    
DOI: 10.1111/j.1440-169X.2006.00890.x     Document Type: Article

References (46)

1. Abe, S. 2004. Hormonal control of meiosis initiation in the testis from Japanese newt, Cynops pyrrhogaster. Zool. Sci. 21, 691-704.
2. Bergmann, M., Greven, H. & Schindelmeiser, J. 1983. Observations on the blood-testis barrier in a frog and a salamander. Cell Tissue Res. 232, 189-200.
3. Boitani, C., Politi, M. G. & Menna, T. 1993. Spermatogonial cell proliferation in organ culture of immature rat testis. Biol. Reprod. 48, 761-767.
4. Brinster, R. L. & Avarbock, M. R. 1994. Germline transmission of donor haplotype following spermatogonial transplantation. Proc. Natl Acad. Sci. USA 91, 11303-11307.
5. Brinster, R. L. & Zimmermann, J. W. 1994. Spermatogenesis following male germ-cell transplantation. Proc. Natl Acad. Sci. USA 91, 11298-11302.
6. Cavicchia, J. C. & Moviglia, G. A. 1983. The blood-testis barrier in the toad (Bufo arenarum Hensel): a freeze-fracture and lanthanum tracer study. Anat. Rec. 205, 387-396.
7. Chen, C., Ouyang, W., Grigura, V. et al. 2005. ERM is required for transcriptional control of the spermatogonial stem cell niche. Nature 436, 1030-1034.
8. Ciosk, R., DePalma, M. & Priess, J. R. 2004. ATX-2, the C. elegans ortholog of ataxin 2, functions in translational regulation in the germline. Development 131, 4831-4841.
9. Crittenden, S. L., Bernstein, D. S., Bachorik, J. L. et al. 2002. A conserved RNA-binding protein controls germline stem cells in Caenorhabditis elegans. Nature 417, 660-663.
10. Hardy, R. W., Tokuyasu, K. T., Lindsley, D. L. & Garavito, M. 1979. The germinal proliferation center in the testis of Drosophila melanogaster. J. Ultrastruct. Res. 69, 180-190.
11. Henderson, S. T., Gao, D., Lambie, E. J. & Kimble, J. 1994. lag-2 may encode a signaling ligand for the GLP-1 and LIN-12 receptors of C. Elegans. Development 120, 2913-2924.
12. Hiyoshi, M., Nakajo, N., Abe, S. & Takamune, K. 2005. Involvement of Xtr (Xenopus tudor repeat) in microtubule assembly around nucleus and karyokinesis during cleavage in Xenopus laevis. Dev. Growth Differ. 47, 109-117.
13. Honaramooz, A., Snedaker, A., Boiani, M., Schöler, H., Dobrinski, I. & Schlatt, S. 2002. Sperm from neonatal mammalian testes grafted in mice. Nature 15, 778-781.
14. Horton, J. D. 1969. Ontogeny of the immune response to skin allografts in relation to lymphoid organ development in the amphibian Xenopus laevis Daudin. J. Exp. Zool. 170, 449-466.
15. Ito, R. & Abe, S. 1999. FSH-initiated differentiation of newt spermatogonia to primary spermatocytes in germ-somatic cell reaggregates cultured within a collagen matrix. Int. J. Dev. Biol. 43, 111-116.
16. Ji, Z., Kubokawa, K., Ishii, S. & Abe, S. 1992. Differentiation of secondary spermatogonia to primary spermatocytes by mammalian follicle-stimulating hormone in organ culture of testes fragments from the newt, Cynops pyrrhogaster. Dev. Growth Differ. 34, 649-660.
17. Kalt, M. R. 1976. Morphology and kinetics of spermatogenesis in Xenopus laevis. J. Exp. Zool. 195, 393-407.
18. Kang, L., Marin, M. & Kelley, D. 1995. Androgen biosynthesis and secretion in developing Xenopus laevis. General Comp. Endocrinol. 100, 293-307.
19. Kawase, E., Wong, M. D., Ding, B. C. & Xie, T. 2004. Gbb/Bmp signaling is essential for maintaining germline stem cells and for repressing bam transcription in the Drosophila testis. Development 131, 1365-1375.
20. Kelley, D. B. 1996. Sexual differentiation in Xenopus laevis. In: The Biology of Xenopus (eds R. C. Tinsley & H. R. Kobel), pp. 143-176. Clarendon Press, Oxford.
21. Kiger, A. A., White-Cooper, H. & Fuller M. T. 2000. Somatic support cells restrict germline stem cell self-renewal and promote differentiation. Nature 407, 750-754.
22. Kiger, A. A., Jones, D. L., Schulz, C., Rogers, M. B. & Fuller, M. T. 2001. Stem cell self-renewal specified by JAK-STAT activation in response to a support cell cue. Science 294, 2542-2545.
23. Kubota, H., Avarbock, M. R. & Brinster, R. L. 2003. Spermatogonial stem cells share some, but not all, phenotypic and functional characteristics with other stem cells. Proc. Natl Acad. Sci. USA 100, 6487-6492.
24. Lofts, B. 1974. Reproduction. In: Physiology of the Amphibia, Vol. 2 (ed. B. Lofts), pp. 107-218. Academic Press, New York.
25. Matunis, E., Tran, J., Gonczy, P., Caldwell, K. & DiNardo, S. 1997. punt and schnurri regulate a somatically derived signal that restricts proliferation of committed progenitors in the germline. Development 124, 4383-4391.
26. Meng, X., Lindahl, M., Hyvonen, M. E. et al. 2000. Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science 287, 1489-1493.
27. Mikamo, K. & Witschi, E. 1966. The mitotic chromosomes in Xenopus laevis (Daudin): normal, sex reversed and female WW. Cytogenetics 5, 1-19.
28. Minucci, S., Di Matteo, L., Chieffi, P., Pierantoni, R. & Fasano, S. 1997. 17β-estradiol effects on mast cell number and spermatogonial mitotic index in the testis of the frog, Rana esculenta. J. Exp. Zool. 278, 93-100.
29. Miura, T., Miura, C., Ohta, T., Nader, M. R., Todo, T. & Yamauchi, K. 1999. Estradiol-17β stimulates the renewal of spermatogonial stem cells in males. Biochem. Biophys. Res. Commun. 264, 230-234.
30. Nagai, T., Ibata, K., Park, E. S., Kubota, M., Mikoshiba, K. & Miyawaki, A. 2002. A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat. Biotechnol. 20, 87-90.
31. Nakamura, T., Maeno, M., Tochinai, S. & Katagiri, C. 1987. Tolerance induced by grafting semi-allogeneic adult skin to larval Xenopus laevis: possible involvement of specific suppressor cell activity. Differentiation 35, 108-114.
32. Nieuwkoop, P. D. & Faber, J. 1967. Normal Table of Xenopus Laevis (Daudin). North-Holland Publishing Co., Amsterdam.
33. Ogawa, T., Arechaga, J. M., Avarbock, M. R. & Brinster, R. L. 1997. Transplantation of testis germinal cells into mouse seminiferous tubules. Int. J. Dev. Biol. 41, 111-122.
34. Ogawa, T., Ohmura, M., Yumura, Y., Sawada, H. & Kubota, Y. 2003. Expansion of murine spermatogonial stem cells through serial transplantation. Biol. Reprod. 68, 316-322.
35. Risley, M. S., Miller, A. & Bumcrot, D. A. 1987. In vitro maintenance of spermatogenesis in Xenopus laevis testis explants cultured in serum-free media. Biol. Reprod. 36, 985-997.
36. de Rooij, D. G. 2001. Proliferation and differentiation of spermatogonial stem cells. Reproduction 121, 347-354.
37. Sakamaki, K., Takagi, C., Yoshino, J. et al. 2005. Transgenic frogs expressing the highly fluorescent protein Venus under the control of a strong mammalian promoter suitable for monitoring living cells. Dev. Dyn. 233, 562-569.
38. Shinohara, T., Orwig, K. E., Avarbock, M. R. & Brinster, R. L. 2000. Spermatogonial stem cell enrichment by multiparameter selection of mouse testis cells. Proc. Natl Acad. Sci. USA 97, 8346-8351.
39. Shinohara, T., Orwig, K. E., Avarbock, M. R. & Brinster, R. L. 2001. Remodeling of the postnatal mouse testis is accompanied by dramatic changes in stem cell number and niche accessibility. Proc. Natl Acad. Sci. USA 98, 6186-6191.
40. Spradling, A., Drummond-Barbosa, D. & Kai, T. 2001. Stem cells find their niche. Nature 414, 98-104.
41. Takamune, K., Kawasaki, T. & Ukon, S. 2001. The first and the second mitotic phases of spermatogonial stage in Xenopus laevis: Secondary spermatogonia which have differentiated after completion of the first mitotic phase acquire an ability of mitosis to meiosis conversion. Zool. Sci. 18, 577-583.
42. Takamune, K., Teshima, K., Maeda, M. & Abe, S. 1995. Characteristic features of preleptotene spermatocytes in Xenopus laevis: Increase in the nuclear volume and first appearance of flattened vesicles in these cells. J. Exp. Zool. 273, 264-270.
43. Tochinai, S. & Katagiri, C. 1975. Complete abrogation of immune response to skin allografts and rabbit erythrocytes in the early thymectomized Xenopus. Dev. Growth Differ. 17, 383-394.
44. Tran, J., Brenner, T. J. & DiNardo, S. 2000. Somatic control over the germline stem cell lineage during Drosophila spermatogenesis. Nature 407, 754-757.
45. Tulina, N. & Matunis, E. 2001. Control of stem cell self-renewal in Drosophila spermatogenesis by JAK-STAT signaling. Science 294, 2546-2549.
46. Watt, F. M. & Hogan, B. L. M. 2000. Out of Eden: stem cells and their niches. Science 287, 1427-1430.