Regulation of cell fate decision of undifferentiated spermatogonia by GDNF

Science

Volumn 287, Issue 5457, 2000, Pages 1489-1493

  Meng, Xiaojuan ^a   Lindahl, Maria ^a   Hyvönen, Mervi E ^a   Parvinen, Martti ^a   De Rooij, Dirk G ^a   Hess, Michael W ^a   Raatikainen Ahokas, Anne ^a   Sainio, Kirsi ^a   Rauvala, Heikki ^a   Lakso, Merja ^a   Pichel, José G ^a   Westphal, Heiner ^a   Saarma, Mart ^a   Sariola, Hannu ^a  

^a NONE

Author keywords

[No Author keywords available]

Indexed keywords

GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; RETINOIC ACID;

APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL FATE; CELL RENEWAL; GENE OVEREXPRESSION; GENE TARGETING; MOUSE; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; REGULATORY MECHANISM; SPERMATOGONIUM; STEM CELL; TESTIS TUMOR;

ANIMALS; APOPTOSIS; CELL CYCLE; CELL DIFFERENTIATION; COBALT; DROSOPHILA PROTEINS; FEMALE; GENE EXPRESSION; GENE TARGETING; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR RECEPTORS; MALE; MICE; MICE, TRANSGENIC; MITOSIS; NERVE GROWTH FACTORS; NERVE TISSUE PROTEINS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-RET; RECEPTOR PROTEIN-TYROSINE KINASES; SERTOLI CELLS; SPERMATOGENESIS; SPERMATOGONIA; STEM CELLS; TESTICULAR NEOPLASMS; TESTIS; VITAMIN A;

EID: 17944401554     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.287.5457.1489     Document Type: Article

References (46)

1. C. Huckins, Anat. Rec. 169, 533 (1971); E. F. Oakberg, Anat. Rec. 169, 515 (1971).
2. C. Huckins, Anat. Rec. 169, 533 (1971); E. F. Oakberg, Anat. Rec. 169, 515 (1971).
3. D. G. De Rooij and J. A. Grootegoed, Curr. Opin. Cell Biol. 10, 694 (1998); D. G. De Rooij, M. Okabe, Y. Nishimune, Biol. Reprod. 61, 842 (1999).
4. D. G. De Rooij and J. A. Grootegoed, Curr. Opin. Cell Biol. 10, 694 (1998); D. G. De Rooij, M. Okabe, Y. Nishimune, Biol. Reprod. 61, 842 (1999).
5. O. H. Pescovitz, C. H. Srivastava, P. R. Breyer, B. A. Monts, Trends Endocrinol. Metab. 5, 126 (1994).
6. M. Trupp et al., J. Cell Biol. 130, 137 (1995); H. L. Hellmich, L. Kos, E. S. Cho, K. A. Mahon, A. Zimmer, Mech. Dev. 54, 95 (1996); J. P. Golden, J. A. DeMaro, P. A. Osborne, J. Milbrandt, E. M. Johnson, Exp. Neurol. 158, 504 (1999).
7. M. Trupp et al., J. Cell Biol. 130, 137 (1995); H. L. Hellmich, L. Kos, E. S. Cho, K. A. Mahon, A. Zimmer, Mech. Dev. 54, 95 (1996); J. P. Golden, J. A. DeMaro, P. A. Osborne, J. Milbrandt, E. M. Johnson, Exp. Neurol. 158, 504 (1999).
8. M. Trupp et al., J. Cell Biol. 130, 137 (1995); H. L. Hellmich, L. Kos, E. S. Cho, K. A. Mahon, A. Zimmer, Mech. Dev. 54, 95 (1996); J. P. Golden, J. A. DeMaro, P. A. Osborne, J. Milbrandt, E. M. Johnson, Exp. Neurol. 158, 504 (1999).
9. L. F. Lin, D. H. Doherty, J. D. Lile, S. Bektesh, F. Collins, Science 260, 1130 (1993).
10. A. Tomac et al., Nature 373, 335 (1995); E. Arenas, M. Trupp, P. Åkerud, C. Ibáñez, Neuron 15, 1465 (1995); R. W. Oppenheim et al., Nature 373, 344 (1995); Q. Yan, C. Matheson, O. T. Lopez, Nature 373, 341 (1995); Q. T. Nguyen, A. S. Parsadanian, W. D. Snider, J. W. Lichtman, Science 279, 1725 (1998).
11. A. Tomac et al., Nature 373, 335 (1995); E. Arenas, M. Trupp, P. Åkerud, C. Ibáñez, Neuron 15, 1465 (1995); R. W. Oppenheim et al., Nature 373, 344 (1995); Q. Yan, C. Matheson, O. T. Lopez, Nature 373, 341 (1995); Q. T. Nguyen, A. S. Parsadanian, W. D. Snider, J. W. Lichtman, Science 279, 1725 (1998).
12. A. Tomac et al., Nature 373, 335 (1995); E. Arenas, M. Trupp, P. Åkerud, C. Ibáñez, Neuron 15, 1465 (1995); R. W. Oppenheim et al., Nature 373, 344 (1995); Q. Yan, C. Matheson, O. T. Lopez, Nature 373, 341 (1995); Q. T. Nguyen, A. S. Parsadanian, W. D. Snider, J. W. Lichtman, Science 279, 1725 (1998).
13. A. Tomac et al., Nature 373, 335 (1995); E. Arenas, M. Trupp, P. Åkerud, C. Ibáñez, Neuron 15, 1465 (1995); R. W. Oppenheim et al., Nature 373, 344 (1995); Q. Yan, C. Matheson, O. T. Lopez, Nature 373, 341 (1995); Q. T. Nguyen, A. S. Parsadanian, W. D. Snider, J. W. Lichtman, Science 279, 1725 (1998).
14. A. Tomac et al., Nature 373, 335 (1995); E. Arenas, M. Trupp, P. Åkerud, C. Ibáñez, Neuron 15, 1465 (1995); R. W. Oppenheim et al., Nature 373, 344 (1995); Q. Yan, C. Matheson, O. T. Lopez, Nature 373, 341 (1995); Q. T. Nguyen, A. S. Parsadanian, W. D. Snider, J. W. Lichtman, Science 279, 1725 (1998).
15. J. G. Pichel et al., Nature 382, 73 (1996).
16. K. Sainio et al., Development 124, 4077 (1997).
17. M. Saarma and H. Sariola, Microsc. Res. Tech. 45, 292 (1999).
18. A. Schuchardt, V. D'Agati, L. Larsson-Blomberg, F. Costantini, V. Pachnis, Nature 367, 380 (1994); M.W. Moore et al., Nature 382, 76 (1996); H. Enomoto et al., Neuron 21, 317 (1998).
19. A. Schuchardt, V. D'Agati, L. Larsson-Blomberg, F. Costantini, V. Pachnis, Nature 367, 380 (1994); M.W. Moore et al., Nature 382, 76 (1996); H. Enomoto et al., Neuron 21, 317 (1998).
20. A. Schuchardt, V. D'Agati, L. Larsson-Blomberg, F. Costantini, V. Pachnis, Nature 367, 380 (1994); M.W. Moore et al., Nature 382, 76 (1996); H. Enomoto et al., Neuron 21, 317 (1998).
21. J. Hu, H. Shima, H. Nakagawa, Endocrinology 140, 3416 (1999).
22. Testes were fixed in Bouin or 4% paraformialdehyde, processed in paraffin, sectioned, and stained with hematoxylin/eosin solution. Monoclonal antibodies to EE2 (1:200) and GATA-1 (1:50) (Santa Cruz, Santa Cruz, CA) were incubated on deparaffinized sections overnight and detected by indirect biotin-streptavidin-peroxidase (BSP) labeling (Vector, Burlingame, CA). Species-crossreactive rabbit polyclonal antibodies to GDNF (1:500; Santa Cruz), c-Kit (1:200; Santa Cruz), and c-Ret (1:500; IBL, Fujioka, Japan) were incubated for 48 hours at 4°C and detected with BSP Labeling.
23. Web figs. 1 through 5 are available at Science Online at www.sciencemag.org/features/data/1046816/shl.
24. S. Mizushima and S. Nagata, Nucleic Acids Res. 18, 5322 (1990). The human GDNF cDNA (GenBank accession number L15306) was cloned into the Xba I site of the pEF-BOS vector under the EF-1α promoter. The 2.7-kb Pvu I-Hind III fragment of the construct was sequenced, and GDNF expression was verified by Cos cell transfection and Western blotting. Transgenic FVB mice were produced by a standard procedure. Founders and their offspring were screened with Southern blotting and polymerase chain reaction from tail DNA. Primers for human GDNF were from exon 1 (5′-TGT CGT GGC TGT CTG CCT GGT GC-3′) and exon 2 (5′-AAG GCG ATG GGT CTG CAA CAT GCC-3′).
25. T. Furuchi, K. Masuko, Y. Nishimune, M. Obinata, Y. Matsui, Development 122, 1703 (1996).
26. 32P]dCTP. All probes were the same as in the in situ hybridization, except that the c-Ret probe was a 3.3-kb full-length cDNA. Testes were homogenized in lysis buffer containing 1M NaCl and immuno-precipitated with species-crossreactive human recombinant GDNF antibody (R&D Systems, Minneapolis, MN). After 20% SDS-polyacrylamide gel electrophoresis, Western blotting was done on Hybond ECL membranes (Amersham). GDNF was detected with rabbit polyclonal antibody to human GDNF (Santa Cruz), followed by horseradish peroxidase-conjugated antibody (Sigma) and ECL chemiluminescence (Amersham).
27. U. Koshimizu, H. Nishioka, D. Watanabe, K. Dohmae, Y. Nishimune, Mol. Reprod. Dev. 40, 221 (1995).
28. M. Parvinen et al., Histochem. Cell Biol. 108, 77 (1997).
29. 35S]uridine 5′-triphosphate-labeled cRNA probes to GDNF, Ret, and GFR-α1 were as described [Z. Kokaia et al., Eur. J. Neurosci. 11, 1202 (1999)]. The slides were exposed for 2 to 4 weeks and photographed with an Olympus Provis microscope equipped with a charge-coupled device camera (Photometrics, Munich, Germany). In the Adobe PhotoShop 4.0 program, the dark-field images were inverted, artificially stained red, and recombined with the bright- field images. The sense controls did not show grain density above background levels.
30. 35S]uridine 5′-triphosphate-labeled cRNA probes to GDNF, Ret, and GFR-α1 were as described [Z. Kokaia et al., Eur. J. Neurosci. 11, 1202 (1999)]. The slides were exposed for 2 to 4 weeks and photographed with an Olympus Provis microscope equipped with a charge-coupled device camera (Photometrics, Munich, Germany). In the Adobe PhotoShop 4.0 program, the dark-field images were inverted, artificially stained red, and recombined with the bright-field images. The sense controls did not show grain density above background levels.
31. K. Yoshinaka et al., Development 113, 689 (1991); B. H. Schrans-Stassen, G. J. van de Kant, D. G. de Rooij, A. M. M. van Pelt, endocrinology 140, 5894 (1999).
32. K. Yoshinaka et al., Development 113, 689 (1991); B. H. Schrans-Stassen, G. J. van de Kant, D. G. de Rooij, A. M. M. van Pelt, endocrinology 140, 5894 (1999).
33. K. Yomogida et al., Development 120, 1756 (1994).
34. The mice were injected intraperitoneally (ip) with BrdU (Amersham). After 2 hours, testes were dissected, fixed in Bouin, and processed in paraffin. BrdU incorporation was detected by monoclonal BrdU antibody (Amersham) and indirect immunofluorescence [tetramethyl rhodamine isothiocyanate (TRITC) -antibody to mouse immunoglobulin G (IgG), 1:100; Jackson Immunoresearch] or BSP labeling. Apoptotic cells were detected with the ApopTag kit (Intergen, Purchase, NY).
35. Electron microscopic biopsies were processed by standard methods and examined with a JEM 1200EX microscope (JEOL, Tokyo, Japan).
36. J. Widenfalk et al., J. Neurosci. 17, 8506 (1997).
37. X. Meng and H. Sariola, unpublished data.
38. K. Akmal, J. Dufour, M. Vo, S. Higginson, K. Kim, Endocrinology 139, 1239 (1998);
39. T. Lufkin et al., Proc. Natl. Acad. Sci. U.S.A. 90, 7225 (1993).
40. Wild-type and transgenic mice at 3 weeks of age (n = 9 mice in both groups) were injected ip with all-trans retinol (Sigma) (10 mg per kg of body weight per day). Testes were processed for histology after 3 or 8 days.
41. E. M. Eddy et al., Endocrinology 137, 4796 (1996)
42. R. M. Pelletier and S. W. Byers, Microsc. Res. Tech. 20, 3 (1992).
43. M. L. Meistrich and M. E. van Beek, in Cell and Molecular Biology of Testis, C. Desjardins and L. L. Ewing, Eds. (Oxford Univ. Press, Oxford, 1993), pp. 266-295; Y. Clermont, Am. J. Anat. 112, 35 (1963).
44. M. L. Meistrich and M. E. van Beek, in Cell and Molecular Biology of Testis, C. Desjardins and L. L. Ewing, Eds. (Oxford Univ. Press, Oxford, 1993), pp. 266-295; Y. Clermont, Am. J. Anat. 112, 35 (1963).
45. E. F. Oakberg, Am. J. Anat. 99, 391 (1956).
46. We thank A. Hanninen, K. Westerdahl, and P. Leikas-Lazanyi. K. Wartiovaara (University of Helsinki) cloned human GDNF cDNA. EE2 antibody was from Y. Nishimune (Osaka University, Japan). Supported by the Sigrid Jusélius Foundation, Technology Advancement Center of Finland (TEKES), the Academy of Finland, and EUBioMedII (contract BMH 4-CT97-2157).