Testicular stem cells

Seminars in Reproductive Medicine

Volumn 24, Issue 5, 2006, Pages 370-378

  Goossens, Ellen ^a   Tournaye, Herman ^a  

^a CENTRE FOR REPRODUCTIVE MEDICINE   (Belgium)

Author keywords

Fertility preservation; Spermatogenesis; Stem cell; Testis

Indexed keywords

AUTOREGULATION; CANCER PATIENT; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL RENEWAL; CELL SELECTION; CRYOPRESERVATION; GENETIC TRANSFECTION; HUMAN; INFERTILITY THERAPY; MALE FERTILITY; MEDICAL RESEARCH; REVIEW; SPERMATOGENESIS; SPERMATOZOON; STEM CELL; STEM CELL TRANSPLANTATION; TESTICULAR STEM CELL; TESTIS CELL;

ANIMALS; APOPTOSIS; CELL CULTURE TECHNIQUES; CELL PROLIFERATION; CRYOPRESERVATION; HUMANS; MALE; MODELS, BIOLOGICAL; PRIMATES; STEM CELL TRANSPLANTATION; STEM CELLS; TESTIS; TRANSFECTION;

EID: 33845286889     PISSN: 15268004     EISSN: None     Source Type: Journal    
DOI: 10.1055/s-2006-952158     Document Type: Review

References (94)

1. Lajtha LG. Stem cell concepts. Differentiation 1979;14:23-34
2. Lawson KA, Pederson RA. Clonal analysis of cell fate during gastrulation and early neurulation in the mouse. In: CIBA Foundation Symposium 165: Post Implantation Development in the Mouse. New York: John Wiley, 1992:3-26
3. Tam P, Snow MHL. Proliferation and migration of primordial germ cells during compensatory growth in the mouse embryo. J Embryol Exp Morphol 1981;64:133-147
4. Fleischman RA. From with spots to stem cells: the role of Kit receptor in mammalian development. Trends Genet 1993;15:285-290
5. Sapsford CS. Changes in the cells of the sex cords and the seminiferous tubules during development of the testis of the rat and the mouse. Aust J Zool 1962;10:178-192
6. Huckins C, Clermont Y. Evolution of gonocytes in the rat testis during late embryonic and post-natal life. Arch Anat Histol Embryol 1968;51:343-354
7. Vergouwen RPFA, Jacobs SGPM, Huiskamp R, Davids JAG, de Rooij DG. Proliferative activity of interstitial cells, Sertoli cells and gonocytes during testicular development in the mouse. J Reprod Fertil 1991;93:233-243
8. Keros V, Rosenlund B, Hultenby K, Aghajanova L, Levkov L, Hovatta O. Optimizing cryopreservation of human testicular tissue: comparison of protocols with glycerol, propanediol and dimethylsulphoxide as cryoprotectants. Hum Reprod 2005; 20:1676-1687
9. Schrans-Stassen BH, van de Kant HJ, de Rooij DG, van Pelt AM. Differential expression of c-kit in mouse undifferentiated and differentiating type A spermatogonia. Endocrinology 1999;140:5894-5900
10. Blanchard KT, Lee J, Boekelheide K. Leuprolide, a gonadotropin-releasing hormone agonist, reestablishes spermatogenesis after 2,5-hexanedione-induced irreversible testicular injury in the rat, resulting in normalized stem cell factor expression. Endocrinology 1998;139:236-244
11. Pellegrini M, Grimaldi P, Rossi P, Geremia R, Dolci S. Developmental expression of BMP4/ALK3/SMAD5 signaling pathway in the mouse testis: a potential role of BMP4 in spermatonia differentiation. J Cell Sci 2003;116:3363-3372
12. Oulad-Abdelghani M, Bouillet P, Decimo D, et al. Characterization of a premeiotic germ cell-specific cytoplasmic protein encoded by Stra8, a novel retinoic acid-responsive gene. J Cell Biol 1996;135:469-477
13. 6-integrin are surface markers on mouse spermatogonial stem cells. Proc Natl Acad Sci USA 1999;96:5504-5509
14. Reijo RA, Dorfman DM, Slee R, et al. DAZ family proteins exist throughout male germ cell development and transit from nucleus to cytoplasm at meiosis in humans and mice. Biol Reprod 2000;63:1490-1496
15. Kubota H, Avarbock MR, Brinster RL. Spermatogonial stem cells share some, but not all, phenotypic and functional characteristics with other stem cells. Proc Natl Acad Sci USA 2003;100:6487-6492
16. Kanatsu-Shinohara M, Toyokuni S, Shinohara T. CD9 is a surface marker on mouse and rat male germline stem cells. Biol Reprod 2004;70:70-75
17. Lassalle B, Bastos H, Louis JP, et al. 'Side Population' cells in adult mouse testis express Bcrp1 gene and are enriched in spermatogonia and germinal stem cells. Development 2004;131:479-487
18. Van Pelt AMM, Roepers-Gajadien HL, Gademan IS, Creemers LB, de Rooij DG, van Dissel-Emiliani FM. Establishment of cell lines with rat spermatogonial stem cell characteristics. Endocrinology 2002;143:1845-1850
19. Hofmann MC, Braydich-Stolle L, Dettin L, Johnson E, Dym M. Immortalization of mouse germ line stem cells. Stem Cells 2005;23:200-210
20. Kanatsu-Shinohara M, Inoue K, Lee J, et al. Generation of pluripotent stem cells from neonatal mouse testis. Cell 2004;119:1001-1012
21. Guan K, Nayernia K, Maier LS, et al. Pluripotency of spermatogonial stem cells from adult mouse testis. Nature 2006;440:1199-1203
22. Huckins C. The spermatogonial stem cell population in adult rats. I. Their morphology, proliferation and maturation. Anat Rec 1971;169:533-558
23. Oakberg EF. Spermatogonial stem-cell renewal in the mouse. Anat Rec 1971;169:515-532
24. Clermont Y, Bustos-Obregon E. Re-examination of spermatogonial renewal in the rat by means of seminiferous tubules mounted in 'toto'. Am J Anat 1968;122:237-248
25. Clermont Y, Hermo L. Spermatogonial stem cells in the albino rat. Am J Anat 1975;142:159-176
26. Dym M, Clermont Y. Role of spermatogonia in the repair of the seminiferous epithelium following x-irradiation of the rat testis. Am J Anat 1970;128:265-282
27. Clermont Y, Hermo L. Spermatogonial stem cells and their behavior in the seminiferous epithelium of rats and monkeys. In: Cairnie AB, Lala PK, Osmond DG, eds. Stem Cells of Renewing Cell Populations. New York: Academic Press; 1976:273-286
28. van Alphen MMA, van de Kant HJG, de Rooij DG. Depletion of the spermatogonia from the seminiferous epithelium of the Rhesus monkey after x-irradiation. Radiat Res 1988;113:473-486
29. Ehmcke J, Luetjens CM, Schlatt S. Clonal organization of proliferating spermatogonial stem cells in adult males of two species of non-human primates, Macaca mulatta and Callitrix jacchus. Biol Reprod 2005;72:293-300
30. Ehmcke J, Simorangkir DR, Schlatt S. Identification of the starting point for spermatogenesis and characterization of the testicular stem cell in adult male rhesus monkeys. Hum Reprod 2005;20:1185-1193
31. Russell L. Sertoli-germ cell interrelations: a review. Gamete Res 1980;3:179-202
32. Dobrinski I, Avarbock MR, Brinster RL. Transplantation of germ cells from rabbits and dogs into mouse testes. Biol Reprod 1999;61:1331-1339
33. Brinster RL, Zimmermann JW. Spermatogenesis following male germ-cell transplantation. Proc Natl Acad Sci USA 1994;91:11298-11302
34. Avarbock MR, Brinster CJ, Brinster RL. Reconstitution of spermatogenesis from frozen spermatogonial stem cells. Nat Med 1996;2:693-696
35. de Rooij DG, Lok D, Weenk D. Feedback regulation of the proliferation of the undifferentiated spermatogonia in the Chinese hamster by the differentiating spermatogonia. Cell Tissue Kinet 1985;18:71-81
36. de Rooij DG, Janssen JM. The regulation of the density of spermatogonia in the seminiferous epithelium of the Chinese hamster. I. Undifferentiated spermatogonia. Anat Rec 1987;217:124-130
37. de Rooij DG, Lok D. The regulation of the density of spermatogonia in the seminiferous epithelium of the Chinese hamster. II. Differentiated spermatogonia. Anat Rec 1987;217:131-136
38. Van Keulen CJG, de Rooij DG. Spermatogenic clones developing from repopulating stem cells surviving a high dose of an alkylating agent. I. First 15 days after injury. Cell Tissue Kinet 1975;8:543-551
39. van Beek MEAB, Meistrich ML, de Rooij DG. Probability of self-renewing divisions of spermatogonial stem cells in colonies formed after fission neutron irradiation. Cell Tissue Kinet 1990;23:1-16
40. Dirami G, Ravindranath N, Pursel V, Dym M. Effects of stem cell factor and granulocyte macrophage-colony stimulating factor on survival of porcine type A spermatogonia cultured in KSOM. Biol Reprod 1999;61:225-230
41. Meng X, Lindahl M, Hyvonen ME, Parvinen M, de Rooij DG, Hess MW. Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science 2000;287:1489-1493
42. Kubota H, Avarbock MR, Brinster RL. Culture conditions and single growth factors affect fate determination of mouse spermatogonial stem cells. Biol Reprod 2004;71:722-731
43. Kubota H, Avarbock MR, Brinster RL. Growth factors essential for self-renewal and expansion of mouse spermatogonial stem cells. Proc Natl Acad Sci U S A 2004;101:16489-16494
44. Kanatsu-Shinohara M, Ogonuki N, Inoue K, et al. Long-term proliferation in culture and germline transmission of mouse male germline stem cells. Biol Reprod 2003;69:612-616
45. Buaas FW, Kirsh AL, Sharma M, et al. Plzf is required in adult male germ cells for stem cell self-renewal. Nat Genet 2004;36:647-652
46. Costoya JA, Hobbs RM, Barna M, et al. Essential role of Plzf in maintenance of spermatogonial stem cells. Nat Genet 2004;36:653-659
47. Falender AE, Freiman RN, Geles KG, et al. Maintenance of spermatogenesis requires TAF4b, a gonad-specific subunit of TFIID. Genes Dev 2005;19:794-803
48. Nishimune Y, Haneji T. Testicular DNA synthesis in vivo: comparison between unilaterally cryptorchid testis and contralateral intact testis in mouse. Arch Androl 1981;6:61-65
49. Koshimizu U, Sawada K, Tajima Y, Watanabe D, Nishimune Y. White-spotting mutations affect the regenerative differentiation of testicular germ cells: demonstration by experimental cryptorchidism and its surgical reversal. Biol Reprod 1991;45:642-648
50. Tajima Y, Sakamaki K, Watanabe D, Koshimizu U, Matsuwaza T, Nishimune Y. Steel-Dickie (Sld) mutation affects both maintenance and differentiation of testicular germ cells in mice. J Reprod Fertil 1991;91:441-449
51. van Pelt AM, van Dissel-Emiliani FMF, Gaemers IC, Van de Burg M, Tanke HJ, de Rooij DG. Characteristics of A spermatogonia and preleptotene spermatocytes in the vitamin A deficient rat testis. Biol Reprod 1995;53:570-578
52. Huang HFS, Humbree WC. Spermatogenic response to vitamin A in vitamin A deficient rats. Biol Reprod 1979;21:891-904
53. van Pelt AM, de Rooij DG. Retinoic acid is able to reinitiate spermatogenesis in vitamin A-deficient rats and high, replicate doses support the full development of spermatogenic cells. Endocrinology 1991;128:697-704
54. Beamer WG, Cunliffe-Beamer TL, Shultz KL, Langley SH, Roderick TH. Juvenile spermatogonial depletion (jsd): a genetic defect of germ cell proliferation of male mice. Biol Reprod 1988;38:899-908
55. Mizunuma M, Dohmae K, Tajima Y, Koshimizu U, Watanabe D, Nishimune Y. Loss of sperm in juvenile spermatogonial depletion (jsd) mutant mice is ascribed to a defect of intratubular environment to support germ cell differentiation. J Cell Physiol 1992;150:188-193
56. Boekelheide K. Rat testis during 2,5-hexanedione intoxication and recovery. I. Dose response and the reversibility of germ cell loss. Toxicol Appl Pharmacol 1988;92:18-27
57. Allard EK, Hall SJ, Boekelheide K. Stem cell kinetics in rat testis after irreversible injury induced by 2,5-hexanedione. Biol Reprod 1995;53:186-192
58. Kangasniemi M, Huhtaniemi I, Meistrich ML. Failure of spermatogenesis to recover despite the presence of A spermatogonia in the irradiated LBNF1 rat. Biol Reprod 1996;54:1200-1208
59. Meistrich ML, Kangasniemi M. Hormone treatment after irradiation stimulates recovery of rat spermatogenesis from surviving spermatogonia. J Androl 1997;18:80-87
60. Beumer TL, Roepers-Gajadien HL, van Buul PPW, et al. The role of the tumor suppressor gene p53 in spermatogenesis. Cell Death Differ 1998;5:669-677
61. Rodriguez I, Ody C, Araki K, Garcia I, Vassalli P. An early and massive wave of germinal cell apoptosis is required for the development of functional spermatogenesis. EMBO J 1997;16:2262-2270
62. Yan W, Samson M, Jegou B, Toppari J. Bcl-w forms complexes with Bax and Bak, and elevated ratios of Bax/Bcl-w and Bak/Bcl-w correspond to spermatogonial and spermatocyte apoptosis in the testis. Mol Endocrinol 2000;14:682-699
63. Brinster RL, Avarbock MR. Germline transmission of donor haplotype following spermatogonial transplantation. Proc Natl Acad Sci USA 1994;91:11303-11307
64. Nagano M, Avarbock MR, Leonida EB, Brinster CJ, Brinster RL. Culture of mouse spermatogonial stem cells. Tissue Cell 1998;30:389-397
65. Tournaye H, Goossens E, Verheyen G, et al. Preserving the reproductive potential of men and boys with cancer: current concepts and future prospects. Hum Reprod Update 2004;10:525-532
66. Nagano M, Shinohara T, Avarbock MR, Brinster RL. Retrovirus-mediated gene delivery into male germ line stem cells. FEBS Lett 2000;475:7-10
67. Nagano M, Avarbock MR, Brinster RL. Pattern and kinetics of mouse donor spermatogonial stem cell colonization in recipient testes. Biol Reprod 1999;60:1429-1436
68. Clouthier DE, Avarbock MR, Maika SD, Hammer RE, Brinster RL. Rat spermatogenesis in mouse testis. Nature 1996;381:418-421
69. França LR, Ogawa T, Avarbock MR, Brinster RL, Russell LD. Germ cell genotype controls cell cycle during spermatogenesis in the rat. Biol Reprod 1998;59:1371-1377
70. Ogawa T, Dobrinski I, Avarbock MR, Brinster RL. Xenogeneic spermatogenesis following transplantation of hamster germ cells to mouse testes. Biol Reprod 1999; 60:515-521
71. Nagano M, McCarrey JR, Brinster RL. Primate spermatogonial stem cells colonize mouse testes. Biol Reprod 2001;64:1409-1416
72. Reis MM, Tsai MC, Schlegel PN, et al. Xenogeneic transplantation of human spermatogonia. Zygote 2000;8:97-105
73. Nagano M, Patrizio P, Brinster RL. Long-term survival of human spermatogonial stem cells in mouse testes. Fertil Steril 2002;78:1225-1233
74. Goossens E, Frederickx V, De Block G, Van Steirteghem AC, Tournaye H. Reproductive capacity of sperm obtained after germ cell transplantation in a mouse model. Hum Reprod 2003;18:1874-1880
75. Honaramooz A, Snedaker A, Boiani M, Scholer H, Dobrinski I, Schlatt S. Sperm from neonatal mammalian testis grafted in mice. Nature 2002;418:778-781
76. Honaramooz A, Li MW, Penedo MC, Meyers S, Dobrinski I. Accelerated maturation of primate testis by xenografting into mouse. Biol Reprod 2004;70:1500-1503
77. Schlatt S, Kim SS, Gosden R. Spermatogenesis and steroidogenesis in mouse, hamster and monkey testicular tissue after cryopreservation and heterotropic grafting to castrated hosts. Reproduction 2002;124:339-346
78. Schlatt S, Honaramooz A, Boiani M, Scholer HR, Dobrinski I. Progeny from sperm obtained after ectopic grafting of neonatal mouse testes. Biol Reprod 2003;68:2331-2335
79. Oatley JM, de Avila DM, Reeves JJ, McLean DJ. Spermatogenesis and germ cell transgene expression in xenografted bovine testicular tissue. Biol Reprod 2004;71:494-501
80. Ma P, Ge Y, Wang S, Ma J, Xue S, Han D. Spermatogenesis following syngeneic testicular transplantation in Balb/c mice. Reproduction 2004;128:163-170
81. Shinohara T, Inoue K, Ogonuki N, et al. Birth of offspring following transplantation of cryopreserved immature testicular pieces and in-vitro microinsemination. Hum Reprod 2002;17:3039-3045
82. Geens M, De Block G, Goossens E, Frederickx V, Van Steirteghem AC, Tournaye H. Spermatogonial survival after grafting human testicular tissue to immunodeficient mice. Hum Reprod 2006;21:390-396
83. Schlatt S, Honaramooz A, Ehmcke J, et al. Limited survival of adult human testicular tissue as ectopic xenograft. Hum Reprod 2006;21:384-389
84. Meistrich ML, Van Beek MEAB. Spermatogonial stem cells. In: Desjardins C, Ewing LL, eds. Cell and Molecular Biology of the Testis. New York: Oxford University Press; 1993:266-295
85. Shinohara T, Orwig KE, Avarbock MR, Brinster RL. Spermatogonial stem cell enrichment by multiparameter selection of mouse testis cells. Proc Natl Acad Sci USA 2000;97:8346-8351
86. Nagano M, Ryu BY, Brinster CJ, Avarbock MR, Brinster RL. Maintenance of mouse male germ line stem cells in vitro. Biol Reprod 2003;68:2207-2214
87. Kanatsu-Shinohara M, Ogonuki N, Inoue K, Ogura A, Toyokuni S, Shinohara T. Restoration of fertility in infertile mice by transplantation of cryopreserved male germline stem cells. Hum Reprod 2003;18:2660-2667
88. Kanatsu-Shinohara M, Miki H, Inoue K, et al. Long-term culture of mouse male germline stem cells under serum- or feeder-free conditions. Biol Reprod 2005;72:985-991
89. Creemers LB, den Ouden K, van Pelt AM, de Rooij DG. Maintenance of adult mouse type A spermatogonia in vitro: influence of serum and growth factors and comparison with prepubertal spermatogonial cell culture. Reproduction 2002;124:791-799
90. Izadyar F, den Ouden K, Creemers LB, Posthuma G, Parvinen M, de Rooij DG. Proliferation and differentiation of bovine type A spermatogonia during long-term culture. Biol Reprod 2003;68:272-281
91. Oatley JM, de Avila DM, Reeves JJ, McLean DJ. Testis tissue explant culture supports survival and proliferation of bovine spermatogonial stem cells. Biol Reprod 2004;70:625-631
92. Izadyar F, Matthijs-Rijsenbilt JJ, den Ouden K, Creemers LB, Woelders H, de Rooij DG. Development of a cryopreservation protocol for type A spermatogonia. J Androl 2002;23:537-545
93. Frederickx V, Michiels A, Goossens E, De Block G, Van Steirteghem AC, Tournaye H. Recovery, survival and functional evaluation by transplantation of frozen-thawed mouse germ cells. Hum Reprod 2004;19:948-953
94. Kanatsu-Shinohara M, Toyokuni S, Shinohara T. Transgenic mice produced by retroviral transduction of male germ line stem cells in vivo. Biol Reprod 2004;71:1202-1207