'Side population' cells in adult mouse testis express Bcrp1 gene and are enriched in spermatogonia and germinal stem cells

Development

Volumn 131, Issue 2, 2004, Pages 479-487

  Lassalle, Bruno ^a   Bastos, Henri ^a   Louis, Jean Paul ^b   Riou, Lydia ^a   Testart, Jacques ^a   Dutrillaux, Bernard ^a   Fouchet, Pierre ^a   Allemand, Isabelle ^a  

^a INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

^b CNRS   (France)

Author keywords

BCRP1 ABCG2; Spermatogenesis; Stem cells; Transplantation

Indexed keywords

ABC TRANSPORTER; ALPHA6 INTEGRIN; CELL MARKER; HOE 33342; MESSENGER RNA; PROTEIN INHIBITOR;

ADOLESCENT; ANIMAL CELL; ARTICLE; BONE MARROW; CELL DIFFERENTIATION; CONTROLLED STUDY; DRUG TRANSPORT; GENE ACTIVITY; GENE EXPRESSION; GERM CELL; HEMATOPOIETIC CELL; IN VIVO STUDY; MALE; MOUSE; MOUSE STRAIN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SKELETAL MUSCLE; SPERMATOGONIUM; TESTIS CELL;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BASE SEQUENCE; BENZIMIDAZOLES; CELL DIFFERENTIATION; CRYPTORCHIDISM; DNA, COMPLEMENTARY; DNA-BINDING PROTEINS; FLUORESCENT DYES; GENE EXPRESSION; MALE; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MICE, TRANSGENIC; NEOPLASM PROTEINS; NUCLEAR PROTEINS; PHENOTYPE; SPERMATOGENESIS; SPERMATOGONIA; STEM CELLS; TESTIS;

ANIMALIA;

EID: 0842344610     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.00918     Document Type: Article

References (51)

1. Allen, J. D., Brinkhuis, R. F., Wijnholds, J. and Schinkel, A. H. (1999). The mouse Bcrp1/Mxr/Abcp gene: amplification and overexpression in cell lines selected for resistance to topotecan, mitoxantrone, or doxorubicin. Cancer Res. 59, 4237-4241.
2. Allen, J. D., van Loevezijn, A., Lakhai, J. M., van der Valk, M., van Tellingen, O., Reid, G., Schellens, J. H., Koomen, G. J. and Schinkel, A. H. (2002). Potent and specific inhibition of the breast cancer resistance protein multidrug transporter in vitro and in mouse intestine by a novel analogue of fumitremorgin C. Mol. Cancer Ther. 6, 417-425.
3. Bart, J., Groen, H. J., van der Graaf, W. T., Hollema, H., Hendrikse, N. H., Vaalburg, W., Sleijfer, D. T. and de Vries, E. G. (2002). An oncological view on the blood-testis barrier. Lancet Oncol. 3, 357-363.
4. Bellve, A. R. (1993). Purification, culture, and fractionation of spermatogenic cells. Methods Enzymol. 225, 84-113.
5. Brinster, R. L. and Zimmermann, J. W. (1994). Spermatogenesis following male germ-cell transplantation. Proc. Natl. Acad. Sci. USA 91, 11298-11302.
6. Bunting, K. (2002). ABC Transporters as Phenotypic Markers and Functional Regulators of Stem Cells. Stem Cells 20, 11-20.
7. Chiarini-Garcia, H. and Russell, L. D. (2001). High-resolution light microscopic characterization of mouse spermatogonia. Biol. Reprod. 65, 1170-1178.
8. de Rooij, D. G., Okabe, M. and Nishimune, Y. (1999). Arrest of spermatogonial differentiation in jsd/jsd, S117H/S117H, and cryptorchid mice. Biol. Reprod. 61, 842-847.
9. Dix, D. J., Rosario-Herrle, M., Gotoh, H., Mori, C., Goulding, E. H., Barrett, C. V. and Eddy, E. M. (1996). Developmentally regulated expression of Hsp70-2 and a Hvp70-2/lacZ transgene during spermatogenesis. Dev. Biol. 174, 310-321.
10. Drabent, B., Bode, C., Miosge, N., Herken, R. and Doenecke, D. (1998). Expression of the mouse histone gene H1t begins at premeiotic stages of spermatogenesis. Cell Tissue Res. 291, 127-132.
11. Escalier, D. (2001). Impact of genetic engineering on the understanding of spermatogenesis. Hum. Reprod. Update 7, 191-210.
12. Foulkes, N. S., Schlotter, F., Pevet, P. and Sassone-Corsi, P. (1993). Pituitary hormone FSH directs the CREM functional switch during spermatogenesis. Nature 362, 264-267.
13. Giuili, G., Tomljenovic, A., Labrecque, N., Oulad-Abdelghani, M., Rassoulzadegan, M. and Cuzin, E. (2002). Murine spermatogonial stem cells: targeted transgene expression and purification in an active state. EMBO Rep. 3, 753-759.
14. Goodell, M. A., Brose, K., Paradis, G., Conner, A. S. and Mulligan, R. C. (1996). Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J. Exp. Med. 183, 1797-1806.
15. Goodell, M. A., Rosenzweig, M., Kim, H., Marks, D. F., DeMaria, M., Paradis, G., Grupp, S. A., Sieff, C. A., Mulligan, R. C. and Johnson, R. P. (1997). Dye efflux studies suggest that hematopoietic stem cells expressing low or undetectable levels of CD34 antigen exist in multiple species. Nat. Med. 3, 1337-1345.
16. Gottesman, M. M., Fojo, T. and Bates, S. E. (2002). Multidrug resistance in cancer: role of ATP-dependent transporters. Nat. Rev. Cancer 2, 48-58.
17. Gussoni, E., Soneoka, Y., Strickland, C. D., Buzney, E. A., Khan, M. K., Flint, A. F., Kunkel, L. M. and Mulligan, R. C. (1999). Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature 401, 390-394.
18. Hulspas, R. and Quesenberry, P. J. (2000). Characterization of neurosphere cell phenotypes by flow cytometry. Cytometry 40, 245-250.
19. Jackson, K. A., Mi, T. and Goodell, M. A. (1999). Hematopoietic potential of stem cells isolated from murine skeletal muscle. Proc. Natl. Acad. Sci. USA 96, 14482-14486.
20. Jonker, J. W., Buitelaar, M., Wagenaar, E., van Der Valk, M. A., Scheffer, G. L., Scheper, R. J., Plosch, T., Kuipers, F., Elferink, R. P., Rosing, H. et al. (2002). The breast cancer resistance protein protects against a major chlorophyll-derived dietary phototoxin and protoporphyria. Proc. Natl. Acad. Sci. USA 99, 15649-15654.
21. Kleene, K. C. (2001). A possible meiotic function of the peculiar patterns of gene expression in mammalian spermatogenic cells. Mech. Dev. 106, 3-23.
22. 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.
23. Lowell, S. (2000). Stem cells show their potential. Trends Cell Biol. 10, 210-211.
24. Manova, K., Nocka, K., Besmer, P. and Bachvarova, R. F. (1990). Gonadal expression of c-kit encoded at the W locus of the mouse. Development 110, 1057-1069.
25. Melaine, N., Lienard, M. O., Dorval, I., le Goascogne, C., Lejeune, H. and Jegou, B. (2002). Multidrug resistance genes and p-glycoprotein in the testis of the rat, mouse, Guinea pig, and human. Biol. Reprod. 67, 1699-1707.
26. Miyake, K., Mickley, L., Litman, T., Zhan, Z., Robey, R., Cristensen, B., Brangi, M., Greenberger, L., Dean, M., Fojo, T. et al. (1999). Molecular cloning of cDNAs which are highly overexpressed in mitoxantrone-resistant cells: demonstration of homology to ABC transport genes. Cancer Res. 59, 8-13.
27. Niederberger, C., Agulnik, A. I., Cho, Y., Lamb, D. and Bishop, C. E. (1997). In situ hybridization shows that Dazla expression in mouse testis is restricted to premeiotic stages IV-VI of spermatogenesis. Mamm. Genome 8, 277-278.
28. Nishimune, Y., Aizawa, S. and Komatsu, T. (1978). Testicular germ cell differentiation in vivo. Fertil. Steril. 29, 95-102.
29. Nocka, K., Tan, J. C., Chiu, E., Chu, T. Y., Ray, P., Traktman, P. and Besmer, P. (1990). Molecular bases of dominant negative and loss of function mutations at the marine c-kit/white spotting locus: W37, Wv, W41 and W. EMBO J. 9,1805-1813.
30. Ogawa, T., Arechaga, J. M., Avarbock, M. R. and Brinster, R. L. (1997). Transplantation of testis germinal cells into mouse seminiferous tubules. Int. J. Dev. Biol. 41, 111-122.
31. Ogawa, T., Dobrinski, I., Avarbock, M. R. and Brinster, R. L. (1998). Leuprolide, a gonadotropin-releasing hormone agonist, enhances colonization after spermatogonial transplantation into mouse testes. Tissue Cell. 30, 583-588.
32. Ohta, H., Yomogida, K., Yamada, S., Okabe, M. and Nishimune, Y. (2000). Real-time observation ot transplanted 'green germ cells': proliferation and differentiation of stem cells. Dev. Growth Differ. 42, 105-112.
33. Okabe, M., Ikawa, M., Kominami, K., Nakanishi, T. and Nishimune, Y. (1997). 'Green mice' as a source of ubiquitous green cells. FEBS Lett. 407, 313-319.
34. Ory, K., Lebeau, J., Levalois, C., Bishay, K., Fouchet, P., Allemand, L, Therwath, A. and Chevillard, S. (2001). Apoptosis inhibition mediated by medroxyprogesterone acetate treatment of breast cancer cell lines. Breast Cancer Res. Treat. 68, 187-198.
35. Oulad-Abdelghani, M., Bouillet, P., Decimo, D., Gansmuller, A., Heyberger, S., Dolle, P., Bronner, S., Lutz, Y. and Chambon, P. (1996). Characterization of a premeiotic germ cell-specific cytoplasmic protein encoded by Stra8, a novel retinoic acid-responsive gene. J. Cell Biol. 135, 469-477.
36. Ruggiu, M., Speed, R., Taggart, M., McKay, S. J., Kilanowski, F., Saunders, P., Dorin, J. and Cooke, H. J. (1997). The mouse Dazla gene encodes a cytoplasmic protein essential for gametogenesis. Nature 389, 73-77.
37. Russell, L., Ettlin, A., Sinha Hikim, A. and Clegg, E. (1990). Histological and Histopathological Evaluation of the Testis. Clearwater, FL: Cache River Press.
38. Scharenberg, C. W., Harkey, M. A. and Torok-Storb, B. (2002). The ABCG2 transporter is an efficient Hoechst 33342 efflux pump and is preferentially expressed by immature human hematopoietic progenitors. Blood 99, 507-512.
39. 6 integrin are surface markers on mouse spermatogonial stem cells. Proc. Natl. Acad. Sci . USA 96, 5504-5509.
40. Shinohara, T., Avarbock, M. and Brinster, R. L. (2000a). Functional analysis of spermatogonial stem cells in Steel and cryptorchid infertile mouse models. Dev. Biol. 220, 401-411.
41. Shinohara, T., Orwig, K. E., Avarbock, M. R and Brinster, R. L. (2000b). Spermatogonial stem cell enrichment by multiparameter selection of mouse testis cells. Proc. Natl. Acad. Sci. USA 97, 8346-8351.
42. Suzuki, A., Zheng, Y., Kondo, R., Kusakabe, M., Takada, Y., Fukao, K., Nakauchi, H. and Taniguchi, H. (2000). Flow-cytometric separation and enrichment of hepatic progenitor cells in the developing mouse liver. Hepatology 32, 1230-1239.
43. van der Pol, M. A., Broxterman, H. J., Pater, J. M., Feller, N., van der Maas, M., Weijers, G. W., Scheffer, G. L., Allen, J. D., Scheper, R. J., van Loevezijn, A., Ossenkoppele, G. J. and Schuurhuis, G. J. (2003). Function of the ABC transporters, P-glycoprotein, multidrug resistance protein and breast cancer resistance protein, in minimal residual disease in acute myeloid leukemia. Haematologica 88, 134-147.
44. Vincent, S., Segretain, D., Nishikawa, S., Nishikawa, S. I., Sage, J., Cuzin, F. and Rassoulzadegan, M. (1998). Stage-specific expression of the Kit receptor and its ligand (KL) during male gametogenesis in the mouse: a Kit-KL interaction critical for meiosis. Development 125, 4585-4593.
45. Wang, P. J., McCarrey, J. R., Yang, F. and Page, D. C. (2001). An abundance of X-linked genes expressed in spermatogonia. Nat. Genet. 27, 422-426.
46. Watt, F. M. (2002). Role of integrins in regulating epidermal adhesion, growth and differentiation. EMBO J. 21, 3919-3926.
47. Wijnholds, J., Scheffer, G. L., van der Valk, M., van der Valk, P., Beijnen, J. H., Scheper, R. J. and Borst, P. (1998). Multidrug resistance protein 1 protects the oropharyngeal mucosal layer and the testicular tubules against drug-induced damage. J. Exp. Med. 188, 797-808.
48. Zakeri, Z. F., Wolgemuth, D. J. and Hunt, C. R. (1988). Identification and sequence analysis of a new member of the mouse HSP70 gene family and characterization of its unique cellular and developmental pattern of expression in the male germ line. Mol. Cell. Biol. 8, 2925-2932.
49. Zhao, G. Q. and Garbers, D. L. (2002). Male germ cell specification and differentiation. Dev. Cell 2, 537-547.
50. Zhou, S., Schuetz, J. D., Bunting, K. D., Colapietro, A. M., Sampath, J., Morris, J. J., Lagutina, I., Grosveld, G. C., Osawa, M., Nakauchi, H. et al. (2001). The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat. Med. 7, 1028-1034.
51. Zhou, S., Morris, J. J., Barnes, Y., Lan, L., Schuetz, J. D. and Sorrentino, B. P. (2002). Bcrp1 gene expression is required for normal numbers of side population stem cells in mice, and confers relative protection to mitoxantrone in hematopoietic cells in vivo. Proc. Natl. Acad. Sci. USA 99, 12339-12344.