Reconstitution of mouse spermatogonial stem cell niches in culture

Cell Stem Cell

Volumn 11, Issue 4, 2012, Pages 567-578

  Kanatsu Shinohara, Mito ^a   Inoue, Kimiko ^b   Takashima, Seiji ^a   Takehashi, Masanori ^a,e   Ogonuki, Narumi ^b   Morimoto, Hiroko ^a   Nagasawa, Takashi ^c,d   Ogura, Atsuo ^b   Shinohara, Takashi ^a,d  

^a KYOTO UNIVERSITY   (Japan)

^b INST OF PHYS AND CHEMICAL RESEARCH   (Japan)

^c KYOTO UNIVERSITY   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^e OSAKA OHTANI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; CHEMOTACTIC FACTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR RECEPTOR; PROTEIN RET; STROMAL CELL DERIVED FACTOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CULTURE; CELL HOMING; CELL MIGRATION; CONTROLLED STUDY; HEMATOPOIETIC STEM CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SERTOLI CELL; STEM CELL NICHE; TESTIS CELL; UPREGULATION;

ANIMALS; CELL MOVEMENT; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; CHEMOKINE CXCL12; COCULTURE TECHNIQUES; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR RECEPTORS; MALE; MICE; MICE, INBRED C57BL; RECEPTORS, CXCR4; SEMINIFEROUS TUBULES; SERTOLI CELLS; SPERMATOGONIA; STEM CELL NICHE; TRANSGENES;

EID: 84867377755     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2012.06.011     Document Type: Article

References (43)

1. + progenitors to peripheral blood J. Exp. Med. 185 1997 111 120
2. T. Ara, Y. Nakamura, T. Egawa, T. Sugiyama, K. Abe, T. Kishimoto, Y. Matsui, and T. Nagasawa Impaired colonization of the gonads by primordial germ cells in mice lacking a chemokine, stromal cell-derived factor-1 (SDF-1) Proc. Natl. Acad. Sci. USA 100 2003 5319 5323
3. E. Arighi, M.G. Borrello, and H. Sariola RET tyrosine kinase signaling in development and cancer Cytokine Growth Factor Rev. 16 2005 441 467
4. B. Boldajipour, H. Mahabaleshwar, E. Kardash, M. Reichman-Fried, H. Blaser, S. Minina, D. Wilson, Q. Xu, and E. Raz Control of chemokine-guided cell migration by ligand sequestration Cell 132 2008 463 473
5. R.L. Brinster, and J.W. Zimmermann Spermatogenesis following male germ-cell transplantation Proc. Natl. Acad. Sci. USA 91 1994 11298 11302
6. M.D. Castellone, V. Guarino, V. De Falco, F. Carlomagno, F. Basolo, P. Faviana, M. Kruhoffer, T. Orntoft, J.P. Russell, and J.L. Rothstein Functional expression of the CXCR4 chemokine receptor is induced by RET/PTC oncogenes and is a common event in human papillary thyroid carcinomas Oncogene 23 2004 5958 5967
7. C. Chen, W. Ouyang, V. Grigura, Q. Zhou, K. Carnes, H. Lim, G.-Q. Zhao, S. Arber, N. Kurpios, and T.L. Murphy ERM is required for transcriptional control of the spermatogonial stem cell niche Nature 436 2005 1030 1034
8. D.G. de Rooij, and L.D. Russell All you wanted to know about spermatogonia but were afraid to ask J. Androl. 21 2000 776 798
9. T.M. Dexter, T.D. Allen, and L.G. Lajtha Conditions controlling the proliferation of haemopoietic stem cells in vitro J. Cell. Physiol. 91 1977 335 344
10. M. Doitsidou, M. Reichman-Fried, J. Stebler, M. Köprunner, J. Dörries, D. Meyer, C.V. Esguerra, T. Leung, and E. Raz Guidance of primordial germ cell migration by the chemokine SDF-1 Cell 111 2002 647 659
11. G.A. Donzella, D. Schols, S.W. Lin, J.A. Esté, K.A. Nagashima, P.J. Maddon, G.P. Allaway, T.P. Sakmar, G. Henson, E. De Clercq, and J.P. Moore AMD3100, a small molecule inhibitor of HIV-1 entry via the CXCR4 co-receptor Nat. Med. 4 1998 72 77
12. E.N. Geissler, M.A. Ryan, and D.E. Housman The dominant-white spotting (W) locus of the mouse encodes the c-kit proto-oncogene Cell 55 1988 185 192
13. M. Ikawa, V. Tergaonkar, A. Ogura, N. Ogonuki, K. Inoue, and I.M. Verma Restoration of spermatogenesis by lentiviral gene transfer: offspring from infertile mice Proc. Natl. Acad. Sci. USA 99 2002 7524 7529
14. S. Jain, C.K. Naughton, M. Yang, A. Strickland, K. Vij, M. Encinas, J. Golden, A. Gupta, R. Heuckeroth, E.M. Johnson Jr., and J. Milbrandt Mice expressing a dominant-negative Ret mutation phenocopy human Hirschsprung disease and delineate a direct role of Ret in spermatogenesis Development 131 2004 5503 5513
15. M. Kanatsu-Shinohara, N. Ogonuki, K. Inoue, H. Miki, A. Ogura, S. Toyokuni, and T. Shinohara Long-term proliferation in culture and germline transmission of mouse male germline stem cells Biol. Reprod. 69 2003 612 616
16. M. Kanatsu-Shinohara, M. Takehashi, S. Takashima, J. Lee, H. Morimoto, S. Chuma, A. Raducanu, N. Nakatsuji, R. Fässler, and T. Shinohara Homing of mouse spermatogonial stem cells to germline niche depends on β1-integrin Cell Stem Cell 3 2008 533 542
17. H.A. Kodama, Y. Amagai, H. Koyama, and S. Kasai Hormonal responsiveness of a preadipose cell line derived from newborn mouse calvaria J. Cell. Physiol. 112 1982 83 88
18. J. Lee, M. Kanatsu-Shinohara, K. Inoue, N. Ogonuki, H. Miki, S. Toyokuni, T. Kimura, T. Nakano, A. Ogura, and T. Shinohara Akt mediates self-renewal division of mouse spermatogonial stem cells Development 134 2007 1853 1859
19. B.C. Lu, C. Cebrian, X. Chi, S. Kuure, R. Kuo, C.M. Bates, S. Arber, J. Hassell, L. MacNeil, and M. Hoshi Etv4 and Etv5 are required downstream of GDNF and Ret for kidney branching morphogenesis Nat. Genet. 41 2009 1295 1302
20. M.L. Meistrich, and M.E.A.B. van Beek Spermatogonial stem cells C. Desjardins, L.L. Ewing, Cell and Molecular Biology of the Testis 1993 Oxford University Press New York 266 295
21. X. Meng, M. Lindahl, M.E. Hyvönen, M. Parvinen, D.G. de Rooij, M.W. Hess, A. Raatikainen-Ahokas, K. Sainio, H. Rauvala, and M. Lakso Regulation of cell fate decision of undifferentiated spermatogonia by GDNF Science 287 2000 1489 1493
22. H. Morimoto, M. Kanatsu-Shinohara, S. Takashima, S. Chuma, N. Nakatsuji, M. Takehashi, and T. Shinohara Phenotypic plasticity of mouse spermatogonial stem cells PLoS ONE 4 2009 e7909
23. M.C. Nagano Homing efficiency and proliferation kinetics of male germ line stem cells following transplantation in mice Biol. Reprod. 69 2003 701 707
24. M. Nagano, M.R. Avarbock, and R.L. Brinster Pattern and kinetics of mouse donor spermatogonial stem cell colonization in recipient testes Biol. Reprod. 60 1999 1429 1436
25. C.K. Naughton, S. Jain, A.M. Strickland, A. Gupta, and J. Milbrandt Glial cell-line derived neurotrophic factor-mediated RET signaling regulates spermatogonial stem cell fate Biol. Reprod. 74 2006 314 321
26. M.J. Oatley, K.E. Racicot, and J.M. Oatley Sertoli cells dictate spermatogonial stem cell niches in the mouse testis Biol. Reprod. 84 2011 639 645
27. T. Ogawa, J.M. Aréchaga, M.R. Avarbock, and R.L. Brinster Transplantation of testis germinal cells into mouse seminiferous tubules Int. J. Dev. Biol. 41 1997 111 122
28. C.J. Payne, S.J. Gallagher, O. Foreman, J.H. Dannenberg, R.A. Depinho, and R.E. Braun Sin3a is required by sertoli cells to establish a niche for undifferentiated spermatogonia, germ cell tumors, and spermatid elongation Stem Cells 28 2010 1424 1434
29. R.E. Ploemacher, J.P. van der Sluijs, J.S.A. Voerman, and N.H.C. Brons An in vitro limiting-dilution assay of long-term repopulating hematopoietic stem cells in the mouse Blood 74 1989 2755 2763
30. M. Rassoulzadegan, V. Paquis-Flucklinger, B. Bertino, J. Sage, M. Jasin, K. Miyagawa, V. van Heyningen, P. Besmer, and F. Cuzin Transmeiotic differentiation of male germ cells in culture Cell 75 1993 997 1006
31. R. Schofield The relationship between the spleen colony-forming cell and the haemopoietic stem cell Blood Cells 4 1978 7 25
32. T. Shinohara, M.R. Avarbock, and R.L. Brinster β1- and α6-integrin are surface markers on mouse spermatogonial stem cells Proc. Natl. Acad. Sci. USA 96 1999 5504 5509
33. T. Shinohara, K.E. Orwig, M.R. Avarbock, and R.L. Brinster Remodeling of the postnatal mouse testis is accompanied by dramatic changes in stem cell number and niche accessibility Proc. Natl. Acad. Sci. USA 98 2001 6186 6191
34. T. Shinohara, K.E. Orwig, M.R. Avarbock, and R.L. Brinster Germ line stem cell competition in postnatal mouse testes Biol. Reprod. 66 2002 1491 1497
35. P. Soriano Generalized lacZ expression with the ROSA26 Cre reporter strain Nat. Genet. 21 1999 70 71
36. A. Spradling, D. Drummond-Barbosa, and T. Kai Stem cells find their niche Nature 414 2001 98 104
37. S.J. Szilvassy, K.P. Weller, W. Lin, A.K. Sharma, A.S.Y. Ho, A. Tsukamoto, R. Hoffman, K.R. Leiby, and D.P. Gearing Leukemia inhibitory factor upregulates cytokine expression by a murine stromal cell line enabling the maintenance of highly enriched competitive repopulating stem cells Blood 87 1996 4618 4628
38. Y. Tadokoro, K. Yomogida, H. Ohta, A. Tohda, and Y. Nishimune Homeostatic regulation of germinal stem cell proliferation by the GDNF/FSH pathway Mech. Dev. 113 2002 29 39
39. M.J. Tang, D. Worley, M. Sanicola, and G.R. Dressler The RET-glial cell-derived neurotrophic factor (GDNF) pathway stimulates migration and chemoattraction of epithelial cells J. Cell Biol. 142 1998 1337 1345
40. K. Tokoyoda, T. Egawa, T. Sugiyama, B.I. Choi, and T. Nagasawa Cellular niches controlling B lymphocyte behavior within bone marrow during development Immunity 20 2004 707 718
41. Y.-S. Tzeng, H. Li, Y.-L. Kang, W.-C. Chen, W.-C. Cheng, and D.-M. Lai Loss of Cxcl12/Sdf-1 in adult mice decreases the quiescent state of hematopoietic stem/progenitor cells and alters the pattern of hematopoietic regeneration after myelosuppression Blood 117 2011 429 439
42. K. Yomogida, Y. Yagura, Y. Tadokoro, and Y. Nishimune Dramatic expansion of germinal stem cells by ectopically expressed human glial cell line-derived neurotrophic factor in mouse Sertoli cells Biol. Reprod. 69 2003 1303 1307
43. S. Yoshida, M. Sukeno, and Y. Nabeshima A vasculature-associated niche for undifferentiated spermatogonia in the mouse testis Science 317 2007 1722 1726