Dynamics of GFRα1-positive spermatogonia at the early stages of colonization in the recipient testes of W/Wν male mice

Developmental Dynamics

Volumn 241, Issue 8, 2012, Pages 1374-1384

  Nagai, Ryohei ^a   Shinomura, Mai ^a   Kishi, Kasane ^a   Aiyama, Yoshimi ^a   Harikae, Kyoko ^a   Sato, Takeshi ^a   Kanai Azuma, Masami ^b   Kurohmaru, Masamichi ^a   Tsunekawa, Naoki ^a   Kanai, Yoshiakira ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

Author keywords

GDNF; GFR 1; Mouse; Spermatogonial stem cells; Spermatogonial transplantation

Indexed keywords

GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR RECEPTOR;

ANIMAL TISSUE; ARTICLE; CELL AGGREGATION; CELL DIFFERENTIATION; CELL TRANSPLANTATION; IMMUNOREACTIVITY; MALE; MORULA; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPERMATOGONIUM; STEM CELL; SURVIVAL; TESTIS;

ANIMALS; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR RECEPTORS; IMMUNOHISTOCHEMISTRY; MALE; MICE; SPERMATOGONIA; TESTIS;

MUS;

EID: 84864000040     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.23824     Document Type: Article

References (42)

1. Aponte PM, de Rooij DG, Bastidas P. 2005. Testicular development in Brahman bulls. Theriogenology 64: 1440-1455.
2. Aponte PM, Soda T, Teerds KJ, Mizrak SC, van de Kant HJ, de Rooij DG. 2008. Propagation of bovine spermatogonial stem cells in vitro. Reproduction 136: 543-557.
3. Araki Y, Sato T, Katagiri K, Kubota Y, Ogawa T. 2010. Proliferation of mouse spermatogonial stem cells in microdrop culture. Biol Reprod 83: 951-957.
4. Brinster RL. 2002. Germline stem cell transplantation and transgenesis. Science 296: 2174-2176.
5. Brinster RL. 2007. Male germline stem cells: from mice to men. Science 316: 404-405.
6. Brinster RL, Avarbock MR. 1994. Germline transmission of donor haplotype following spermatogonial transplantation. Proc Natl Acad Sci USA 91: 11303-11307.
7. Brinster RL, Zimmermann JW. 1994. Spermatogenesis following male germ-cell transplantation. Proc Natl Acad Sci USA 91: 11298-11302.
8. de Rooij DG, Grootegoed JA. 1998. Spermatogonial stem cells. Curr Opin Cell Biol 10: 694-701.
9. de Rooij DG, Russell LD. 2000. All you wanted to know about spermatogonia but were afraid to ask. J Androl 21: 776-798.
10. Dobrinski I, Ogawa T, Avarbock MR, Brinster RL. 1999. Computer assisted image analysis to assess colonization of recipient seminiferous tubules by spermatogonial stem cells from transgenic donor mice. Mol Reprod Dev 53: 142-148.
11. He Z, Jiang J, Hofmann MC, Dym M. 2007. Gfra1 silencing in mouse spermatogonial stem cells results in their differentiation via the inactivation of RET tyrosine kinase. Biol Reprod 77: 723-733.
12. Hofmann MC. 2008. Gdnf signaling pathways within the mammalian spermatogonial stem cell niche. Mol Cell Endocrinol 288: 95-103.
13. Hofmann MC, Braydich-Stolle L, Dym M. 2005. Isolation of male germ-line stem cells; influence of GDNF. Dev Biol 279: 114-124.
14. Kanatsu-Shinohara M, Inoue K, Miki H, Ogonuki N, Takehashi M, Morimoto T, Ogura A, Shinohara T. 2006a. Clonal origin of germ cell colonies after spermatogonial transplantation in mice. Biol Reprod 75: 68-74.
15. Kanatsu-Shinohara M, Inoue K, Lee J, Miki H, Ogonuki N, Toyokuni S, Ogura A, Shinohara T. 2006b. Anchorage-independent growth of mouse male germline stem cells in vitro. Biol Reprod 74: 522-529.
16. Kanatsu-Shinohara M, Ogonuki N, Inoue K, Miki H, Ogura A, Toyokuni S, Shinohara T. 2003. Long-term proliferation in culture and germline transmission of mouse male germline stem cells. Biol Reprod 69: 612-616.
17. Kanatsu-Shinohara M, Muneto T, Lee J, Takenaka M, Chuma S, Nakatsuji N, Horiuchi T, Shinohara T. 2008. Long-term culture of male germline stem cells from hamster testes. Biol Reprod 78: 611-617.
18. Kanatsu-Shinohara M, Inoue K, Ogonuki N, Morimoto H, Ogura A, Shinohara T. 2011. Serum- and feeder-free culture of mouse germline stem cells. Biol Reprod 84: 97-105.
19. Kubota H, Avarbock MR, Brinster RL. 2004. Growth factors essential for self-renewal and expansion of mouse spermatogonial stem cells. Proc Natl Acad Sci USA 101: 16489-16494.
20. Meng X, Lindahl M, Hyvonen ME, Parvinen M, de Rooij DG, Hess MW, Raatikainen-Ahokas A, Sainio K, Rauvala H, Lakso M, Pichel JG, Westphal H, Saarma M, Sariola H. 2000. Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science 287: 1489-1493.
21. Morimoto H, Kanatsu-Shinohara M, Takashima S, Chuma S, Nakatsuji N, Takehashi M, Shinohara T. 2009. Phenotypic plasticity of mouse spermatogonial stem cells. PLoS One 4: e7909.
22. Nagano MC. 2003. Homing efficiency and proliferation kinetics of male germ line stem cells following transplantation in mice. Biol Reprod 69: 701-707.
23. Nagano M, Avarbock MR, Brinster RL. 1999. Pattern and kinetics of mouse donor spermatogonial stem cell colonization in recipient testes. Biol Reprod 60: 1429-1436.
24. Nakagawa T, Sharma M, Nabeshima Y, Braun RE, Yoshida S. 2010. Functional hierarchy and reversibility within the murine spermatogenic stem cell compartment. Science 328: 62-67.
25. Naughton CK, Jain S, Strickland AM, Gupta A, Milbrandt J. 2006. Glial cell-line derived neurotrophic factor-mediated RET signaling regulates spermatogonial stem cell fate. Biol Reprod 74: 314-321.
26. Oatley JM, Brinster RL. 2006. Spermatogonial stem cells. Methods Enzymol 419: 259-282.
27. Oatley JM, Brinster RL. 2008. Regulation of spermatogonial stem cell self-renewal in mammals. Annu Rev Cell Dev Biol 24: 263-286.
28. Oatley JM, Reeves JJ, McLean DJ. 2005. Establishment of spermatogenesis in neonatal bovine testicular tissue following ectopic xenografting varies with donor age. Biol Reprod 72: 358-364.
29. Ogawa T, Arechaga JM, Avarbock MR, Brinster RL. 1997. Transplantation of testis germinal cells into mouse seminiferous tubules. Int J Dev Biol 41: 111-122.
30. Ogawa T, Dobrinski I, Avarbock MR, Brinster RL. 1999. Xenogeneic spermatogenesis following transplantation of hamster germ cells to mouse testes. Biol Reprod 60: 515-521.
31. Russell LD, Ettlin RA, Sinha Hikim AP, Clegg ED. 1990. Histological and histopathological evaluation of the testis. Clearwater, FL: Cache River Press.
32. Ryu BY, Kubota H, Avarbock MR, Brinster RL. 2005. Conservation of spermatogonial stem cell self-renewal signaling between mouse and rat. Proc Natl Acad Sci USA 102: 14302-14307.
33. Sada A, Suzuki A, Suzuki H, Saga Y. 2009. The RNA-binding protein NANOS2 is required to maintain murine spermatogonial stem cells. Science 325: 1394-1398.
34. Sadri-Ardekani H, Mizrak SC, van Daalen SK, Korver CM, Roepers-Gajadien HL, Koruji M, Hovingh S, de Reijke TM, de la Rosette JJ, van der Veen F, de Rooij DG, Repping S, van Pelt AM. 2009. Propagation of human spermatogonial stem cells in vitro. JAMA 302: 2127-2134.
35. Sariola H, Saarma M. 2003. Novel functions and signalling pathways for GDNF. J Cell Sci 116: 3855-3862.
36. Sato T, Aiyama Y, Ishii-Inagaki M, Hara K, Tsunekawa N, Harikae K, Uemura-Kamata M, Shinomura M, Zhu XB, Maeda S, Kuwahara-Otani S, Kudo A, Kawakami H, Kanai-Azuma M, Fujiwara M, Miyamae Y, Yoshida S, Seki M, Kurohmaru M, Kanai Y. 2011. Cyclical and patch-like GDNF distribution along the basal surface of Sertoli cells in mouse and hamster testes. PLoS One 6: e28367.
37. Suzuki H, Sada A, Yoshida S, Saga Y. 2009. The heterogeneity of spermatogonia is revealed by their topology and expression of marker proteins including the germ cell-specific proteins Nanos2 and Nanos3. Dev Biol 336: 222-231.
38. Tadokoro Y, Yomogida K, Ohta H, Tohda A, Nishimune Y. 2002. Homeostatic regulation of germinal stem cell proliferation by the GDNF/FSH pathway. Mech Dev 113: 29-39.
39. Wong CH, Cheng CY. 2005. The blood-testis barrier: its biology, regulation, and physiological role in spermatogenesis. Curr Top Dev Biol 71: 263-296.
40. Yeh JR, Zhang X, Nagano MC. 2007. Establishment of a short-term in vitro assay for mouse spermatogonial stem cells. Biol Reprod 77: 897-904.
41. Yoshida S. 2010. Stem cells in mammalian spermatogenesis. Dev Growth Differ 52: 311-317.
42. Zhang X, Ebata KT, Nagano MC. 2003. Genetic analysis of the clonal origin of regenerating mouse spermatogenesis following transplantation. Biol Reprod 69: 1872-1878.