Adult stem cells in the human testis

Seminars in Reproductive Medicine

Volumn 31, Issue 1, 2013, Pages 39-48

  Goossens, Ellen ^a   Tournaye, Herman ^b  

^a VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^b CENTRE FOR REPRODUCTIVE MEDICINE   (Belgium)

Author keywords

male infertility; spermatogenesis; stem cell; transplantation

Indexed keywords

ALPHA ACTIN; FOLLITROPIN; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; SOMATOMEDIN B;

ARTICLE; CANCER CELL; CELL DIFFERENTIATION; CELL FUNCTION; CELL POPULATION; CELL RENEWAL; CELL STIMULATION; CELL THERAPY; CELLULAR SECRETION; CRYOPRESERVATION; DNA METHYLATION; FETUS DEVELOPMENT; HORMONE BINDING; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; MALE; MALE FERTILITY; PLURIPOTENT STEM CELL; REGENERATIVE MEDICINE; REPRODUCTIVE PROCEDURE; SERTOLI CELL; SPERMATOGENESIS; SPERMATOGONIAL STEM CELL; STEM CELL; STEM CELL NICHE; STEM CELL TRANSPLANTATION; TESTIS; TESTIS CELL; TISSUE GRAFT;

ADULT STEM CELLS; ANIMALS; CELL DIFFERENTIATION; FERTILITY; HUMANS; MALE; SPERMATOGONIA; SPERMATOZOA; TESTIS;

EID: 84872412762     PISSN: 15268004     EISSN: 15264564     Source Type: Journal    
DOI: 10.1055/s-0032-1331796     Document Type: Article

References (136)

1. Lawson K. A., Dunn N. R., Roelen B. A., et al. Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev: 1999; 13 4 424 436 (Pubitemid 29108758)
2. Ying Y., Qi X., Zhao G. Q. Induction of primordial germ cells from murine epiblasts by synergistic action of BMP4 and BMP8B signaling pathways. Proc Natl Acad Sci U S A: 2001; 98 14 7858 7862 (Pubitemid 32642651)
3. Ginsburg M., Snow M. H., McLaren A. Primordial germ cells in the mouse embryo during gastrulation. Development: 1990; 110 2 521 528 (Pubitemid 20330528)
4. Fleischman R. A. From white spots to stem cells: the role of the Kit receptor in mammalian development. Trends Genet: 1993; 9 8 285 290 (Pubitemid 23218835)
5. Bendel-Stenzel M., Anderson R., Heasman J., Wylie C. The origin and migration of primordial germ cells in the mouse. Semin Cell Dev Biol: 1998; 9 4 393 400 (Pubitemid 128350665)
6. Sapsford C. S. 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
7. Tam P. P., Snow M. HL. Proliferation and migration of primordial germ cells during compensatory growth in mouse embryos. J Embryol Exp Morphol: 1981; 64 133 147 (Pubitemid 11039715)
8. McLaren A. Primordial germ cells in the mouse. Dev Biol: 2003; 262 1 1 15 (Pubitemid 37153101)
9. Töhönen V., Ritzén E. M., Nordqvist K., Wedell A. Male sex determination and prenatal differentiation of the testis. Endocr Dev: 2003; 5 1 23
10. Huckins C., Clermont Y. Evolution of gonocytes in the rat testis during late embryonic and early post-natal life. Arch Anat Histol Embryol: 1968; 51 1 341 354
11. Vergouwen R. PFA, Jacobs S. GPM, Huiskamp R., Davids J. AG, de Rooij D. G. Proliferative activity of interstitial cells, Sertoli cells and gonocytes during testicular development in the mouse. J Reprod Fertil: 1991; 93 233 243
12. Huckins C. The spermatogonial stem cell population in adult rats. I. Their morphology, proliferation and maturation. Anat Rec: 1971; 169 3 533 557
13. Oakberg E. F. Spermatogonial stem-cell renewal in the mouse. Anat Rec: 1971; 169 3 515 531
14. de Rooij D. G., Russell L. D. All you wanted to know about spermatogonia but were afraid to ask. J Androl: 2000; 21 6 776 798
15. Suzuki H., Sada A., Yoshida S., Saga Y. 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: 2009; 336 2 222 231
16. Zheng K., Wu X., Kaestner K. H., Wang P. J. The pluripotency factor LIN28 marks undifferentiated spermatogonia in mouse. BMC Dev Biol: 2009; 9 38
17. Oatley M. J., Kaucher A. V., Racicot K. E., Oatley J. M. Inhibitor of DNA binding 4 is expressed selectively by single spermatogonia in the male germline and regulates the self-renewal of spermatogonial stem cells in mice. Biol Reprod: 2011; 85 2 347 356
18. Brinster R. L., Zimmermann J. W. Spermatogenesis following male germ-cell transplantation. Proc Natl Acad Sci U S A: 1994; 91 24 11298 11302 (Pubitemid 24356331)
19. Brinster R. L., Avarbock M. R. Germline transmission of donor haplotype following spermatogonial transplantation. Proc Natl Acad Sci U S A: 1994; 91 24 11303 11307 (Pubitemid 24356332)
20. Shinohara T., Orwig K. E., Avarbock M. R., Brinster R. L. Spermatogonial stem cell enrichment by multiparameter selection of mouse testis cells. Proc Natl Acad Sci U S A: 2000; 97 15 8346 8351 (Pubitemid 30639675)
21. Ohbo K., Yoshida S., Ohmura M., et al. Identification and characterization of stem cells in prepubertal spermatogenesis in mice small star, filled. Dev Biol: 2003; 258 1 209 225 (Pubitemid 36627667)
22. Barroca V., Lassalle B., Coureuil M., et al. Mouse differentiating spermatogonia can generate germinal stem cells in vivo. Nat Cell Biol: 2009; 11 2 190 196
23. Clermont Y., Hermo L. Spermatogonial stem cells and their behavior in the seminiferous epithelium of rats and monkeys. In: Cairnie A. B., Lala P. K., Osmond D. G., eds. Stem Cells of Renewing Cell Populations. New York, NY Academic Press: 1976; 273 286
24. van Alphen M. MA, van de Kant H. JG, de Rooij D. G. Depletion of the spermatogonia from the seminiferous epithelium of the rhesus monkey after X irradiation. Radiat Res: 1988; 113 3 473 486 (Pubitemid 18079176)
25. Ehmcke J., Luetjens C. M., Schlatt S. Clonal organization of proliferating spermatogonial stem cells in adult males of two species of non-human primates, Macaca mulatta and Callithrix jacchus. Biol Reprod: 2005; 72 2 293 300 (Pubitemid 40129704)
26. Ehmcke J., Simorangkir D. R., 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 5 1185 1193 (Pubitemid 40790240)
27. Shinohara T., Avarbock M. R., Brinster R. L. beta1- and alpha6-integrin are surface markers on mouse spermatogonial stem cells. Proc Natl Acad Sci U S A: 1999; 96 10 5504 5509 (Pubitemid 29234647)
28. Kubota H., Avarbock M. R., Brinster R. L. Spermatogonial stem cells share some, but not all, phenotypic and functional characteristics with other stem cells. Proc Natl Acad Sci U S A: 2003; 100 11 6487 6492 (Pubitemid 36666608)
29. Kanatsu-Shinohara M., Toyokuni S., Shinohara T. CD9 is a surface marker on mouse and rat male germline stem cells. Biol Reprod: 2004; 70 1 70 75 (Pubitemid 38063552)
30. Buageaw A., Sukhwani M., Ben-Yehudah A., et al. GDNF family receptor alpha1 phenotype of spermatogonial stem cells in immature mouse testes. Biol Reprod: 2005; 73 5 1011 1016 (Pubitemid 41507506)
31. Tokuda M., Kadokawa Y., Kurahashi H., Marunouchi T. CDH1 is a specific marker for undifferentiated spermatogonia in mouse testes. Biol Reprod: 2007; 76 1 130 141 (Pubitemid 46013456)
32. Fujita K., Ohta H., Tsujimura A., et al. Transplantation of spermatogonial stem cells isolated from leukemic mice restores fertility without inducing leukemia. J Clin Invest: 2005; 115 7 1855 1861 (Pubitemid 40979724)
33. Ohmura M., Yoshida S., Ide Y., Nagamatsu G., Suda T., Ohbo K. Spatial analysis of germ stem cell development in Oct-4/EGFP transgenic mice. Arch Histol Cytol: 2004; 67 4 285 296 (Pubitemid 40215902)
34. Meng X., Lindahl M., Hyvönen M. E., et al. Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science: 2000; 287 5457 1489 1493 (Pubitemid 30127143)
35. Costoya J. A., Hobbs R. M., Barna M., et al. Essential role of Plzf in maintenance of spermatogonial stem cells. Nat Genet: 2004; 36 6 653 659 (Pubitemid 38715996)
36. Yoshida S., Takakura A., Ohbo K., et al. Neurogenin3 delineates the earliest stages of spermatogenesis in the mouse testis. Dev Biol: 2004; 269 2 447 458 (Pubitemid 38521110)
37. Raverot G., Weiss J., Park S. Y., Hurley L., Jameson J. L. Sox3 expression in undifferentiated spermatogonia is required for the progression of spermatogenesis. Dev Biol: 2005; 283 1 215 225 (Pubitemid 40828853)
38. Sada A., Suzuki A., Suzuki H., Saga Y. The RNA-binding protein NANOS2 is required to maintain murine spermatogonial stem cells. Science: 2009; 325 5946 1394 1398
39. Giuili G., Tomljenovic A., Labrecque N., Oulad-Abdelghani M., Rassoulzadegan M., Cuzin F. Murine spermatogonial stem cells: targeted transgene expression and purification in an active state. EMBO Rep: 2002; 3 8 753 759 (Pubitemid 34966014)
40. Sadate-Ngatchou P. I., Payne C. J., Dearth A. T., Braun R. E. Cre recombinase activity specific to postnatal, premeiotic male germ cells in transgenic mice. Genesis: 2008; 46 12 738 742
41. Nakagawa T., Nabeshima Y., Yoshida S. Functional identification of the actual and potential stem cell compartments in mouse spermatogenesis. Dev Cell: 2007; 12 2 195 206 (Pubitemid 46172906)
42. Reijo R. A., Dorfman D. M., 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 5 1490 1496
43. Yang J., Chai L., Fowles T. C., et al. Genome-wide analysis reveals Sall4 to be a major regulator of pluripotency in murine-embryonic stem cells. Proc Natl Acad Sci U S A: 2008; 105 50 19756 19761
44. Phillips B. T., Gassei K., Orwig K. E. Spermatogonial stem cell regulation and spermatogenesis. Philos Trans R Soc Lond B Biol Sci: 2010; 365 1546 1663 1678
45. Grisanti L., Falciatori I., Grasso M., et al. Identification of spermatogonial stem cell subsets by morphological analysis and prospective isolation. Stem Cells: 2009; 27 12 3043 3052
46. Dym M., He Z., Jiang J., Pant D., Kokkinaki M. Spermatogonial stem cells: unlimited potential. Reprod Fertil Dev: 2009; 21 1 15 21
47. Conrad S., Renninger M., Hennenlotter J., et al. Generation of pluripotent stem cells from adult human testis. Nature: 2008; 456 7220 344 349
48. Izadyar F., Wong J., Maki C., et al. Identification and characterization of repopulating spermatogonial stem cells from the adult human testis. Hum Reprod: 2011; 26 6 1296 1306
49. Tran J., Brenner T. J., DiNardo S. Somatic control over the germline stem cell lineage during Drosophila spermatogenesis. Nature: 2000; 407 6805 754 757
50. Cheng C. Y., Mruk D. D. Cell junction dynamics in the testis: Sertoli-germ cell interactions and male contraceptive development. Physiol Rev: 2002; 82 4 825 874
51. Oatley J. M., Oatley M. J., Avarbock M. R., Tobias J. W., Brinster R. L. Colony stimulating factor 1 is an extrinsic stimulator of mouse spermatogonial stem cell self-renewal. Development: 2009; 136 7 1191 1199
52. Yoshida S., Sukeno M., Nabeshima Y. A vasculature-associated niche for undifferentiated spermatogonia in the mouse testis. Science: 2007; 317 5845 1722 1726 (Pubitemid 47461832)
53. Ogawa T., Ohmura M., Ohbo K. The niche for spermatogonial stem cells in the mammalian testis. Int J Hematol: 2005; 82 5 381 388 (Pubitemid 46638685)
54. De Rooij D. G., Lok D. Regulation of the density of spermatogonia in the seminiferous epithelium of the Chinese hamster: II. Differentiating spermatogonia. Anat Rec: 1987; 217 2 131 136 (Pubitemid 17017632)
55. Van Keulen C. JG, de Rooij D. G. 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
56. van Beek M. EAB, Meistrich M. L., de Rooij D. G. Probability of self-renewing divisions of spermatogonial stem cells in colonies, formed after fission neutron irradiation. Cell Tissue Kinet: 1990; 23 1 1 16 (Pubitemid 20230554)
57. Nagano M., Avarbock M. R., Leonida E. B., Brinster C. J., Brinster R. L. Culture of mouse spermatogonial stem cells. Tissue Cell: 1998; 30 4 389 397 (Pubitemid 28444790)
58. Nagano M., Shinohara T., Avarbock M. R., Brinster R. L. Retrovirus-mediated gene delivery into male germ line stem cells. FEBS Lett: 2000; 475 1 7 10 (Pubitemid 30331067)
59. 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 2 612 616 (Pubitemid 36885967)
60. Kubota H., Avarbock M. R., Brinster R. L. Growth factors essential for self-renewal and expansion of mouse spermatogonial stem cells. Proc Natl Acad Sci U S A: 2004; 101 47 16489 16494 (Pubitemid 39557740)
61. Kanatsu-Shinohara M., Ogonuki N., Iwano T., et al. Genetic and epigenetic properties of mouse male germline stem cells during long-term culture. Development: 2005; 132 18 4155 4163 (Pubitemid 41488864)
62. Kanatsu-Shinohara M., Inoue K., Ogonuki N., Morimoto H., Ogura A., Shinohara T. Serum- and feeder-free culture of mouse germline stem cells. Biol Reprod: 2011; 84 1 97 105
63. Ryu B. Y., Kubota H., Avarbock M. R., Brinster R. L. Conservation of spermatogonial stem cell self-renewal signaling between mouse and rat. Proc Natl Acad Sci U S A: 2005; 102 40 14302 14307 (Pubitemid 41429693)
64. Wu Z., Falciatori I., Molyneux L. A., Richardson T. E., Chapman K. M., Hamra F. K. Spermatogonial culture medium: an effective and efficient nutrient mixture for culturing rat spermatogonial stem cells. Biol Reprod: 2009; 81 1 77 86
65. Kanatsu-Shinohara M., Muneto T., Lee J., et al. Long-term culture of male germline stem cells from hamster testes. Biol Reprod: 2008; 78 4 611 617 (Pubitemid 351469351)
66. Aponte P. M., Soda T., Teerds K. J., Mizrak S. C., van de Kant H. J., de Rooij D. G. Propagation of bovine spermatogonial stem cells in vitro. Reproduction: 2008; 136 5 543 557
67. Sadri-Ardekani H., Mizrak S. C., van Daalen S. K., et al. Propagation of human spermatogonial stem cells in vitro. JAMA: 2009; 302 19 2127 2134
68. Sadri-Ardekani H., Akhondi M. A., van der Veen F., Repping S., van Pelt A. M. In vitro propagation of human prepubertal spermatogonial stem cells. JAMA: 2011; 305 23 2416 2418
69. Kanatsu-Shinohara M., Inoue K., Lee J., et al. Generation of pluripotent stem cells from neonatal mouse testis. Cell: 2004; 119 7 1001 1012 (Pubitemid 40037613)
70. Guan K., Nayernia K., Maier L. S., et al. Pluripotency of spermatogonial stem cells from adult mouse testis. Nature: 2006; 440 7088 1199 1203
71. Izadyar F., Pau F., Marh J., et al. Generation of multipotent cell lines from a distinct population of male germ line stem cells. Reproduction: 2008; 135 6 771 784 (Pubitemid 351837390)
72. Kossack N., Meneses J., Shefi S., et al. Isolation and characterization of pluripotent human spermatogonial stem cell-derived cells. Stem Cells: 2009; 27 1 138 149
73. Ko K., Araúzo-Bravo M. J., Tapia N., et al. Human adult germline stem cells in question. Nature: 2010; 465 7301 E1; discussion E3
74. Seandel M., James D., Shmelkov S. V., et al. Generation of functional multipotent adult stem cells from GPR125+ germline progenitors. Nature: 2007; 449 7160 346 350 (Pubitemid 47443477)
75. Geijsen N., Hochedlinger K. gPS navigates germ cells to pluripotency. Cell Stem Cell: 2009; 5 1 3 4
76. Hawkins M. M., Stevens M. C. The long-term survivors. Br Med Bull: 1996; 52 4 898 923
77. Bleyer W. A. The impact of childhood cancer on the United States and the world. CA Cancer J Clin: 1990; 40 6 355 367
78. Aksglaede L., Wikström A. M., Rajpert-De Meyts E., Dunkel L., Skakkebaek N. E., Juul A. Natural history of seminiferous tubule degeneration in Klinefelter syndrome. Hum Reprod Update: 2006; 12 1 39 48 (Pubitemid 43013745)
79. Yamada K., Fujita K., Quan J., et al. Increased apoptosis of germ cells in patients with AZFc deletions. J Assist Reprod Genet: 2010; 27 6 293 297
80. de Rooij D. G. The spermatogonial stem cell niche. Microsc Res Tech: 2009; 72 8 580 585
81. Schlatt S. Spermatogonial stem cell preservation and transplantation. Mol Cell Endocrinol: 2002; 187 1-2 107 111 (Pubitemid 34436938)
82. Luetjens C. M., Stukenborg J. B., Nieschlag E., Simoni M., Wistuba J. Complete spermatogenesis in orthotopic but not in ectopic transplants of autologously grafted marmoset testicular tissue. Endocrinology: 2008; 149 4 1736 1747 (Pubitemid 351468358)
83. Milazzo J. P., Vaudreuil L., Cauliez B., et al. Comparison of conditions for cryopreservation of testicular tissue from immature mice. Hum Reprod: 2008; 23 1 17 28 (Pubitemid 351767325)
84. Milazzo J. P., Travers A., Bironneau A., et al. Rapid screening of cryopreservation protocols for murine prepubertal testicular tissue by histology and PCNA immunostaining. J Androl: 2010; 31 6 617 630
85. 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 12 3039 3045 (Pubitemid 35469250)
86. Kvist K., Thorup J., Byskov A. G., Hoyer P. E., Mollgård K., Yding Andersen C. Cryopreservation of intact testicular tissue from boys with cryptorchidism. Hum Reprod: 2006; 21 2 484 491 (Pubitemid 43159927)
87. Keros V., Hultenby K., Borgström B., Fridström M., Jahnukainen K., Hovatta O. Methods of cryopreservation of testicular tissue with viable spermatogonia in pre-pubertal boys undergoing gonadotoxic cancer treatment. Hum Reprod: 2007; 22 5 1384 1395 (Pubitemid 47062811)
88. Honaramooz A., Snedaker A., Boiani M., Schöler H., Dobrinski I., Schlatt S. Sperm from neonatal mammalian testes grafted in mice. Nature: 2002; 418 6899 778 781
89. Ohta H., Sakaide Y., Wakayama T. The birth of mice from testicular spermatozoa retrieved from frozen testicular sections. Biol Reprod: 2008; 78 5 807 811 (Pubitemid 351657377)
90. Jahnukainen K., Ehmcke J., Hergenrother S. D., Schlatt S. Effect of cold storage and cryopreservation of immature non-human primate testicular tissue on spermatogonial stem cell potential in xenografts. Hum Reprod: 2007; 22 4 1060 1067
91. Goossens E., Frederickx V., Geens M., De Block G., Tournaye H. Cryosurvival and spermatogenesis after allografting prepubertal mouse tissue: comparison of two cryopreservation protocols. Fertil Steril: 2008; 89 3 725 727 (Pubitemid 351343819)
92. Zeng W., Snedaker A. K., Megee S., et al. Preservation and transplantation of porcine testis tissue. Reprod Fertil Dev: 2009; 21 3 489 497
93. Abrishami M., Anzar M., Yang Y., Honaramooz A. Cryopreservation of immature porcine testis tissue to maintain its developmental potential after xenografting into recipient mice. Theriogenology: 2010; 73 1 86 96
94. Curaba M., Verleysen M., Amorim C. A., et al. Cryopreservation of prepubertal mouse testicular tissue by vitrification. Fertil Steril: 2011; 95 4 1229 1234, e1
95. Baert Y., Goossens E., Van Saen D., et al. Orthotopic grafting of cryopreserved prepubertal testicular tissue: in search of a simple yet effective cryopreservation protocol. Fertil Steril: 2012; 97 5 1152 1157
96. Parreira G. G., Ogawa T., Avarbock M. R., França L. R., Brinster R. L., Russell L. D. Development of germ cell transplants in mice. Biol Reprod: 1998; 59 6 1360 1370 (Pubitemid 28549850)
97. Avarbock M. R., Brinster C. J., Brinster R. L. Reconstitution of spermatogenesis from frozen spermatogonial stem cells. Nat Med: 1996; 2 6 693 696 (Pubitemid 26191959)
98. Schlatt S., Rosiepen G., Weinbauer G. F., Rolf C., Brook P. F., Nieschlag E. Germ cell transfer into rat, bovine, monkey and human testes. Hum Reprod: 1999; 14 1 144 150 (Pubitemid 29046329)
99. Honaramooz A., Behboodi E., Blash S., Megee S. O., Dobrinski I. Germ cell transplantation in goats. Mol Reprod Dev: 2003; 64 4 422 428 (Pubitemid 36330688)
100. Mikkola M., Sironen A., Kopp C., et al. Transplantation of normal boar testicular cells resulted in complete focal spermatogenesis in a boar affected by the immotile short-tail sperm defect. Reprod Domest Anim: 2006; 41 2 124 128 (Pubitemid 43356845)
101. Kim Y., Turner D., Nelson J., Dobrinski I., McEntee M., Travis A. J. Production of donor-derived sperm after spermatogonial stem cell transplantation in the dog. Reproduction: 2008; 136 6 823 831
102. Hermann B. P., Sukhwani M., Hansel M. C., Orwig K. E. Spermatogonial stem cells in higher primates: are there differences from those in rodents? Reproduction: 2010; 139 3 479 493
103. Dobrinski I., Avarbock M. R., Brinster R. L. Transplantation of germ cells from rabbits and dogs into mouse testes. Biol Reprod: 1999; 61 5 1331 1339 (Pubitemid 29503782)
104. Ogawa T., Dobrinski I., Avarbock M. R., Brinster R. L. Xenogeneic spermatogenesis following transplantation of hamster germ cells to mouse testes. Biol Reprod: 1999; 60 2 515 521 (Pubitemid 29063897)
105. Goossens E., Frederickx V., De Block G., Van Steirteghem A. C., Tournaye H. Reproductive capacity of sperm obtained after germ cell transplantation in a mouse model. Hum Reprod: 2003; 18 9 1874 1880 (Pubitemid 37107561)
106. Goossens E., De Block G., Tournaye H. Computer-assisted motility analysis of spermatozoa obtained after spermatogonial stem cell transplantation in the mouse. Fertil Steril: 2008; 90 4, Suppl 1411 1416
107. Goossens E., De Rycke M., Haentjens P., Tournaye H. DNA methylation patterns of spermatozoa and two generations of offspring obtained after murine spermatogonial stem cell transplantation. Hum Reprod: 2009; 24 9 2255 2263
108. Goossens E., de Vos P., Tournaye H. Array comparative genomic hybridization analysis does not show genetic alterations in spermatozoa and offspring generated after spermatogonial stem cell transplantation in the mouse. Hum Reprod: 2010; 25 7 1836 1842
109. Goossens E., Bilgec T., Van Saen D., Tournaye H. Mouse germ cells go through typical epigenetic modifications after intratesticular tissue grafting. Hum Reprod: 2011; 26 12 3388 3400
110. Honaramooz A., Snedaker A., Boiani M., Schöler H., Dobrinski I., Schlatt S. Sperm from neonatal mammalian testes grafted in mice. Nature: 2002; 418 6899 778 781
111. Schlatt S., Honaramooz A., Boiani M., Schöler H. R., Dobrinski I. Progeny from sperm obtained after ectopic grafting of neonatal mouse testes. Biol Reprod: 2003; 68 6 2331 2335 (Pubitemid 36687029)
112. Honaramooz A., Li M. W., Penedo M. C., Meyers S., Dobrinski I. Accelerated maturation of primate testis by xenografting into mice. Biol Reprod: 2004; 70 5 1500 1503 (Pubitemid 38509699)
113. Schlatt S., Kim S., Gosden R. Spermatogenesis and steroidogenesis in mouse, hamster and monkey testicular tissue after cryopreservation and grafting. Reproduction: 2002; 124 323 329
114. Oatley J. M., de Avila D. M., Reeves J. J., McLean D. J. Spermatogenesis and germ cell transgene expression in xenografted bovine testicular tissue. Biol Reprod: 2004; 71 2 494 501 (Pubitemid 38970524)
115. Geens M., De Block G., Goossens E., Frederickx V., Van Steirteghem A. C., Tournaye H. Spermatogonial survival after grafting human testicular tissue to immunodeficient mice. Hum Reprod: 2006; 21 2 390 396 (Pubitemid 43159913)
116. Schlatt S., Honaramooz A., Ehmcke J., et al. Limited survival of adult human testicular tissue as ectopic xenograft. Hum Reprod: 2006; 21 2 384 389 (Pubitemid 43159912)
117. Sato Y., Nozawa S., Yoshiike M., Arai M., Sasaki C., Iwamoto T. Xenografting of testicular tissue from an infant human donor results in accelerated testicular maturation. Hum Reprod: 2010; 25 5 1113 1122
118. Wyns C., Van Langendonckt A., Wese F. X., Donnez J., Curaba M. Long-term spermatogonial survival in cryopreserved and xenografted immature human testicular tissue. Hum Reprod: 2008; 23 11 2402 2414
119. 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 12 3039 3045 (Pubitemid 35469250)
120. Van Saen D., Goossens E., De Block G., Tournaye H. Regeneration of spermatogenesis by grafting testicular tissue or injecting testicular cells into the testes of sterile mice: a comparative study. Fertil Steril: 2009; 91 5, Suppl 2264 2272
121. Jahnukainen K., Hou M., Petersen C., Setchell B., Söder O. Intratesticular transplantation of testicular cells from leukemic rats causes transmission of leukemia. Cancer Res: 2001; 61 2 706 710 (Pubitemid 32128636)
122. Fujita K., Ohta H., Tsujimura A., et al. Transplantation of spermatogonial stem cells isolated from leukemic mice restores fertility without inducing leukemia. J Clin Invest: 2005; 115 7 1855 1861 (Pubitemid 40979724)
123. Fujita K., Tsujimura A., Miyagawa Y., et al. Isolation of germ cells from leukemia and lymphoma cells in a human in vitro model: potential clinical application for restoring human fertility after anticancer therapy. Cancer Res: 2006; 66 23 11166 11171 (Pubitemid 46009943)
124. Geens M., Van de Velde H., De Block G., Goossens E., Van Steirteghem A., Tournaye H. The efficiency of magnetic-activated cell sorting and fluorescence-activated cell sorting in the decontamination of testicular cell suspensions in cancer patients. Hum Reprod: 2007; 22 3 733 742
125. Geens M., Goossens E., Tournaye H. Cell selection by selective matrix adhesion is not sufficiently efficient for complete malignant cell depletion from contaminated human testicular cell suspensions. Fertil Steril: 2011; 95 2 787 791
126. Glaser T., Opitz T., Kischlat T., et al. Adult germ line stem cells as a source of functional neurons and glia. Stem Cells: 2008; 26 9 2434 2443
127. Streckfuss-Bömeke K., Vlasov A., Hülsmann S., et al. Generation of functional neurons and glia from multipotent adult mouse germ-line stem cells. Stem Cell Res (Amst): 2009; 2 2 139 154
128. Guan K., Wagner S., Unsöld B., et al. Generation of functional cardiomyocytes from adult mouse spermatogonial stem cells. Circ Res: 2007; 100 11 1615 1625 (Pubitemid 46897265)
129. Simon L., Ekman G. C., Kostereva N., et al. Direct transdifferentiation of stem/progenitor spermatogonia into reproductive and nonreproductive tissues of all germ layers. Stem Cells: 2009; 27 7 1666 1675
130. Ning L., Goossens E., Geens M., et al. Mouse spermatogonial stem cells obtain morphologic and functional characteristics of hematopoietic cells in vivo. Hum Reprod: 2010; 25 12 3101 3109
131. Baeyens L., Bouwens L. Can beta-cells be derived from exocrine pancreas? Diabetes Obes Metab: 2008; 10 04 170 178
132. Eberhard D., Tosh D. Transdifferentiation and metaplasia as a paradigm for understanding development and disease. Cell Mol Life Sci: 2008; 65 1 33 40
133. Kanatsu-Shinohara M., Shinohara T. The germ of pluripotency. Nat Biotechnol: 2006; 24 6 663 664 (Pubitemid 43884435)
134. Izadyar F., Pau F., Marh J., et al. Generation of multipotent cell lines from a distinct population of male germ line stem cells. Reproduction: 2008; 135 6 771 784 (Pubitemid 351837390)
135. Nagano M., Shinohara T., Avarbock M. R., Brinster R. L. Retrovirus-mediated gene delivery into male germ line stem cells. FEBS Lett: 2000; 475 1 7 10 (Pubitemid 30331067)
136. 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 4 1202 1207