Spermatogonial stem cells, in vivo transdifferentiation and human regenerative medicine

Expert Opinion on Biological Therapy

Volumn 10, Issue 4, 2010, Pages 519-530

  Simon, Liz ^a   Hess, Rex A ^a   Cooke, Paul S ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Cell based therapy; Germ cells; Pluripotency; Transdifferentiation

Indexed keywords

CELL INTERACTION; CELL TRANSDIFFERENTIATION; CELL TYPE; EMBRYONIC STEM CELL; GENE EXPRESSION; GENETIC MANIPULATION; HUMAN; HUMAN CELL CULTURE; IN VIVO STUDY; MULTIPOTENT STEM CELL; NONHUMAN; PLASTICITY; PLURIPOTENT STEM CELL; PRIMORDIAL GERM CELL; REGENERATIVE MEDICINE; REVIEW; SPERMATOGONIUM; STEM CELL; STEM CELL TRANSPLANTATION;

CELL DIFFERENTIATION; HUMANS; MALE; REGENERATIVE MEDICINE; SPERMATOGONIA; STEM CELLS;

MURINAE;

EID: 77949468337     PISSN: 14712598     EISSN: None     Source Type: Journal    
DOI: 10.1517/14712591003614731     Document Type: Review

References (110)

1. Thomson JA, Itskovitz-Eldor J, Shapiro SS, et al. Embryonic stem cell lines derived from human blastocysts. Science 1998;282(5391):1145-1147
2. Evans MJ, Kaufman MH. Establishment in culture of pluripotential cells from mouse embryos. Nature 1981;292(5819):154-156
3. Martin GR. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci USA 1981;78(12):7634-7638
4. Martin GR, Evans MJ. Differentiation of clonal lines of teratocarcinoma cells: formation of embryoid bodies in vitro. Proc Natl Acad Sci USA 1975;72(4):1441-1445
5. Stice SL, Boyd NL, Dhara SK, et al. Human embryonic stem cells: challenges and opportunities. Reprod Fertil Dev 2006;18(8):839-846
6. Trounson A. The production and directed differentiation of human embryonic stem cells. Endocr Rev 2006;27(2):208-219
7. Yu J, Thomson JA. Pluripotent stem cell lines. Genes Dev 2008;22(15):1987-1997
8. Peura TT, Bosman A, Stojanov T. Derivation of human embryonic stem cell lines. Theriogenology 2007;67(1):32-42
9. Lerou PH, Daley GQ. Therapeutic potential of embryonic stem cells. Blood Rev 2005;19(6):321-331
10. Guhr A, Kurtz A, Friedgen K, Loser P. Current state of human embryonic stem cell research: an overview of cell lines and their use in experimental work. Stem Cells 2006;24(10):2187-2191
11. Turksen K, Troy TC. Human embryonic stem cells: isolation, maintenance, and differentiation. Methods Mol Biol 2006;331:1-12
12. Blum B, Benvenisty N. The tumorigenicity of human embryonic stem cells. Adv Cancer Res 2008;100:133-158
13. Fujikawa T, Oh SH, Pi L, et al. Teratoma formation leads to failure of treatment for type I diabetes using embryonic stem cell-derived insulin-producing cells. Am J Pathol 2005;166(6):1781-1791
14. Strulovici Y, Leopold PL, O'connor TP, et al. Human embryonic stem cells and gene therapy. Mol Ther 2007;15(5):850-866
15. Takahashi K, Tanabe K, Ohnuki M, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007;131(5):861-872
16. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006;126(4):663-676
17. Yu J, Vodyanik MA, Smuga-Otto K, et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007;318(5858):1917-1920
18. Aoi T, Yae K, Nakagawa M, et al. Generation of pluripotent stem cells from adult mouse liver and stomach cells. Science 2008;321(5889):699-702
19. Eminli S, Utikal J, Arnold K, et al. Reprogramming of neural progenitor cells into induced pluripotent stem cells in the absence of exogenous Sox2 expression. Stem Cells 2008;26(10):2467-2474
20. Stadtfeld M, Brennand K, Hochedlinger K. Reprogramming of pancreatic beta cells into induced pluripotent stem cells. Curr Biol 2008;18(12):890-894
21. Stadtfeld M, Nagaya M, Utikal J, et al. Induced pluripotent stem cells generated without viral integration. Science 2008;322(5903):945-949
22. Wernig M, Meissner A, Cassady JP, Jaenisch R. c-Myc is dispensable for direct reprogramming of mouse fibroblasts. Cell Stem Cell 2008;2(1):10-12
23. Nakagawa M, Koyanagi M, Tanabe K, et al. Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat Biotechnol 2008;26(1):101-106
24. Zhao XY, Li W, Lv Z, et al. iPS cells produce viable mice through tetraploid complementation. Nature 2009;461(7260):86-90
25. Boland MJ, Hazen JL, Nazor KL, et al. Adult mice generated from induced pluripotent stem cells. Nature 2009;461(7260):91-94
26. Gonzalez F, Barragan Monasterio M, Tiscornia G, et al. Generation of mouse-induced pluripotent stem cells by transient expression of a single nonviral polycistronic vector. Proc Natl Acad Sci USA 2009;106(22):8918-8922
27. Okita K, Ichisaka T, Yamanaka S. Generation of germline-competent induced pluripotent stem cells. Nature 2007;448(7151):313-317
28. Okita K, Nakagawa M, Hyenjong H, et al. Generation of mouse induced pluripotent stem cells without viral vectors. Science 2008;322(5903):949-953
29. Zhou H WS, Joo JY, Zhu S, et al. Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell 2009;4(5):381-384
30. Guan K, Nayernia K, Maier LS, et al. Pluripotency of spermatogonial stem cells from adult mouse testis. Nature 2006;440(7088):1199-1203
31. 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
32. Kanatsu-Shinohara M, Inoue K, Lee J, et al. Generation of pluripotent stem cells from neonatal mouse testis. Cell 2004;119(7):1001-1012
33. Kanatsu-Shinohara M, Lee J, Inoue K, et al. Pluripotency of a single spermatogonial stem cell in mice. Biol Reprod 2008;78(4):681-687
34. Seandel M, James D, Shmelkov SV, et al. Generation of functional multipotent adult stem cells from GPR125+ germline progenitors. Nature 2007;449(7160):346-350
35. Geijsen N, Jones DL. Seminal discoveries in regenerative medicine: contributions of the male germ line to understanding pluripotency. Hum Mol Genet 2008;17(R1):R16-22
36. Kanatsu-Shinohara M, Takehashi M, Shinohara T. Brief history, pitfalls, and prospects of mammalian spermatogonial stem cell research. Cold Spring Harb Symp Quant Biol 2008;73:17-23
37. Mardanpour P, Guan K, Nolte J, et al. Potency of germ cells and its relevance for regenerative medicine. J Anat 2008;213(1):26-29
38. Brinster RL. Germline stem cell transplantation and transgenesis. Science 2002;296(5576):2174-2176
39. Dym M. Spermatogonial stem cells of the testis. Proc Natl Acad Sci USA 1994;91(24):11287-11289
40. De Rooij DG, Russell LD. All you wanted to know about spermatogonia but were afraid to ask. J Androl 2000;21(6):776-798
41. De Rooij DG. The spermatogonial stem cell niche. Microsc Res Tech 2009;72(8):580-585
42. Hess RA, Cooke PS, Hofmann MC, Murphy KM. Mechanistic insights into the regulation of the spermatogonial stem cell niche. Cell Cycle 2006;5(11):1164-1170
43. Kostereva N, Hofmann MC. Regulation of the spermatogonial stem cell niche. Reprod Domest Anim 2008;43(Suppl 2):386-392
44. Hofmann MC. Gdnf signaling pathways within the mammalian spermatogonial stem cell niche. Mol Cell Endocrinol 2008;288(1-2):95-103
45. Jones DL, Wagers AJ. No place like home: anatomy and function of the stem cell niche. Nat Rev Mol Cell Biol 2008;9(1):11-21
46. Lawson KA, Hage WJ. Clonal analysis of the origin of primordial germ cells in the mouse. Ciba Found Symp 1994;182:68-84; discussion -91
47. Stevens LC. Experimental production of testicular teratomas in mice. Proc Nal Acad Sci USA 1964;52:654-661
48. Matsui Y, Zsebo K, Hogan BL. Derivation of pluripotential embryonic stem cells from murine primordial germ cells in culture. Cell 1992;70(5):841-847
49. Shamblott MJ, Axelman J, Wang S, et al. Derivation of pluripotent stem cells from cultured human primordial germ cells. Proc Natl Acad Sci USA 1998;95(23):13726-13731
50. Zwaka TP, Thomson JA. A germ cell origin of embryonic stem cells? Development 2005;132(2):227-233
51. Baba S, Heike T, Umeda K, et al. Generation of cardiac and endothelial cells from neonatal mouse testis-derived multipotent germline stem cells. Stem Cells 2007;25(6):1375-1383
52. Guan K, Wagner S, Unsold B, et al. Generation of functional cardiomyocytes from adult mouse spermatogonial stem cells. Circ Res 2007;100(11):1615-1625
53. 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
54. Streckfuss-Bomeke K, Vlasov A, Hulsmann S, et al. Generation of functional neurons and glia from multipotent adult mouse germ-line stem cells. Stem Cell Res 2009;2(2):139-154
55. Ko K, Tapia N, Wu G, et al. Induction of pluripotency in adult unipotent germline stem cells. Cell Stem Cell 2009;5(1):87-96
56. Conrad S, Renninger M, Hennenlotter J, et al. Generation of pluripotent stem cells from adult human testis. Nature 2008;456(7220):344-349
57. Golestaneh N, KokkinakiM, Pant D, et al. Pluripotent stem cells derived from adult human testes. Stem Cells Dev 2009;18(8):1115-1126
58. 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
59. Dym M, He Z, Jiang J, et al. Spermatogonial stem cells: unlimited potential. Reprod Fertil Dev 2009;21(1):15-21
60. Kristensen DM, Nielsen JE, Skakkebaek NE, et al. Presumed pluripotency markers UTF-1 and REX-1 are expressed in human adult testes and germ cell neoplasms. Hum Reprod 2008;23(4):775-782
61. Simon L, Ekman GC, 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
62. Grobstein C. Inductive epitheliomesenchymal interaction in cultured organ rudiments of the mouse. Science 1953;118(3054):52-55
63. Buchanan DL, Setiawan T, Lubahn DB, et al. Tissue compartment-specific estrogen receptor-alpha participation in the mouse uterine epithelial secretory response. Endocrinology 1999;140(1):484-491
64. Cooke PS, Buchanan DL, Young P, et al. Stromal estrogen receptors mediate mitogenic effects of estradiol on uterine epithelium. Proc Natl Acad Sci USA 1997;94(12):6535-6540
65. Simon L, Spiewak KA, Ekman GC, et al. Stromal progesterone receptors mediate induction of Indian Hedgehog (IHH) in uterine epithelium and its downstream targets in uterine stroma. Endocrinology 2009;150(8):3871-3876
66. Nelson CM, Bissell MJ. Of extracellular matrix, scaffolds, and signaling: tissue architecture regulates development, homeostasis, and cancer. Annu Rev Cell Dev Biol 2006;22:287-309
67. Spemann H, Mangold H. Induction of embryonic primordia by implantation of organizers from a different species. 1923. Int J Dev Biol 2001;45(1):13-38
68. Cairns Jm JW Jr. The influence of embryonic mesoderm on the regional specification of epidermal derivatives in the chick. J Exp Zool 1954;127:221-248
69. Saunders JW Jr, Gasseling MT. The origin of pattern and feather germ tract specificity. J Exp Zool 1957;135:503-527
70. Cunha GR, Fujii H, Neubauer BL, et al. Epithelial-mesenchymal interactions in prostatic development. I. morphological observations of prostatic induction by urogenital sinus mesenchyme in epithelium of the adult rodent urinary bladder. J Cell Biol 1983;96(6):1662-1670
71. Cunha GR, Lung B, Reese B. Glandular epithelial induction by embryonic mesenchyme in adult bladder epithelium of BALB/c mice. Invest Urol 1980;17(4):302-304
72. Cunha GR, Sekkingstad M, Meloy BA. Heterospecific induction of prostatic development in tissue recombinants prepared with mouse, rat, rabbit and human tissues. Differentiation 1983;24(2):174-180
73. Cunha GR. Stromal induction and specification of morphogenesis and cytodifferentiation of the epithelia of the Mullerian ducts and urogenital sinus during development of the uterus and vagina in mice. J Exp Zool 1976;196(3):361-370
74. Taylor RA, Cowin PA, Cunha GR, et al. Formation of human prostate tissue from embryonic stem cells. Nat Methods 2006;3(3):179-181
75. Oottamasathien S, Wang Y, Williams K, et al. Directed differentiation of embryonic stem cells into bladder tissue. Dev Biol 2007;304(2):556-566
76. Anumanthan G, Makari JH, Honea L, et al. Directed differentiation of bone marrow derived mesenchymal stem cells into bladder urothelium. J Urol 2008;180(4 Suppl):1778-1783
77. Boulanger CA, Mack DL, Booth BW, Smith GH. Interaction with the mammary microenvironment redirects spermatogenic cell fate in vivo. Proc Natl Acad Sci USA 2007;104(10):3871-3876
78. Wu X, Schmidt JA, Avarbock MR, et al. Prepubertal human spermatogonia and mouse gonocytes share conserved gene expression of germline stem cell regulatory molecules. Proc Natl Acad Sci USA 2009;106(51):21672-21677
79. Aberdam D. Derivation of keratinocyte progenitor cells and skin formation from embryonic stem cells. Int J Dev Biol 2004;48(2-3):203-206
80. Orlic D, Kajstura J, Chimenti S. Transplanted adult bone marrow cells repair myocardial infarcts in mice. Ann NY Acad Sci 2001;938:221-229; discussion 229-230
81. Scudellari M. The regeneration recipe. Can natural regenerators such as the newt teach scientists about the ingredients needed to grow new limbs and organs? Even in, say, mammals? Scientist 2009;26(8):26-32
82. Dressel R, Guan K, Nolte J, et al. Multipotent adult germ-line stem cells, like other pluripotent stem cells, can be killed by cytotoxic T lymphocytes despite low expression of major histocompatibility complex class I molecules. Biol Direct 2009;4(1):31. Published online 28 August 2009, doi: 10.1186/1745-6150-4-31
83. He Z, Kokkinaki M, Jiang J, et al. Isolation, characterization, and culture of human spermatogonia. Biol Reprod 2009: published online 21 October 2009, doi: 10.1095/biolreprod.109.078550
84. Brinster RL, Zimmermann JW. Spermatogenesis following male germ-cell transplantation. Proc Natl Acad Sci USA 1994;91(24):11298-11302
85. Brinster RL, Avarbock MR. Germline transmission of donor haplotype following spermatogonial transplantation. Proc Natl Acad Sci USA 1994;91(24):11303-11307
86. Schlatt S, Ehmcke J, Jahnukainen K. Testicular stem cells for fertility preservation: preclinical studies on male germ cell transplantation and testicular grafting. Pediatr Blood Cancer 2009;53(2):274-280
87. Chiquoine AD. The identification, origin, and migration of the primordial germ cells in the mouse embryo. Anat Rec 1954;118(2):135-146
88. Macgregor GR, Zambrowicz BP, Soriano P. Tissue non-specific alkaline phosphatase is expressed in both embryonic and extraembryonic lineages during mouse embryogenesis but is not required for migration of primordial germ cells. Development 1995;121(5):1487-1496
89. Kurimoto K, Yabuta Y, Ohinata Y, et al. Complex genome-wide transcription dynamics orchestrated by Blimp1 for the specification of the germ cell lineage in mice. Genes Dev 2008;22(12):1617-1635
90. Saitou M, Barton SC, Surani MA. A molecular programme for the specification of germ cell fate in mice. Nature 2002;418(6895):293-300
91. Skutella T. Induced pluripotent stem cells from adult testis: a new source of stem cells? Regenerative Med 2009;4(1):3-5
92. Cartwright P, Mclean C, Sheppard A, et al. LIF/STAT3 controls ES cell self-renewal and pluripotency by a Myc-dependent mechanism. Development 2005;132(5):885-896
93. Durcova-Hills G, Tang F, Doody G, et al. Reprogramming primordial germ cells into pluripotent stem cells. PloS one 2008;3(10):e3531. Published online 27 October 2008, doi:10.1371/journal.pone.0003531
94. Oatley JM, Brinster RL. Regulation of spermatogonial stem cell self-renewal in mammals. Annu Rev Cell Dev Biol 2008;24:263-286
95. Clark AT, Bodnar MS, Fox M, et al. Spontaneous differentiation of germ cells from human embryonic stem cells in vitro. Hum Mol Genet 2004;13(7):727-739
96. 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(5):1490-1496
97. Toyooka Y, Tsunekawa N, Akasu R, Noce T. Embryonic stem cells can form germ cells in vitro. Proc Natl Acad Sci USA 2003;100(20):11457-11462
98. Fujiwara Y, Komiya T, Kawabata H, et al. Isolation of a DEAD-family protein gene that encodes a murine homolog of Drosophila vasa and its specific expression in germ cell lineage. Proc Natl Acad Sci USA 1994;91(25):12258-12262
99. Payer B, Saitou M, Barton SC, et al. stella is a maternal effect gene required for normal early development in mice. Curr Biol 2003;13(23):2110-2117
100. Huang YH, Chin CC, Ho HN, et al. Pluripotency of mouse spermatogonial stem cells maintained by IGF-1-dependent pathway. FASEB J 2009;23(7):2076-2087
101. Oatley JM, Avarbock MR, Telaranta AI, et al. Identifying genes important for spermatogonial stem cell self-renewal and survival. Proc Natl Acad Sci USA 2006;103(25):9524-9529
102. Horie K, Takakura K, Taii S, et al. The expression of c-kit protein during oogenesis and early embryonic development. Biol Reprod 1991;45(4):547-552
103. Manova K, Bachvarova RF. Expression of c-kit encoded at the W locus of mice in developing embryonic germ cells and presumptive melanoblasts. Dev Biol 1991;146(2):312-324
104. Nakatake Y, Fukui N, Iwamatsu Y, et al. Klf4 cooperates with Oct3/4 and Sox2 to activate the Lefty1 core promoter in embryonic stem cells. Mol Cell Biol 2006;26(20):7772-7782
105. Chambers I, Colby D, Robertson M, et al. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 2003;113(5):643-655
106. Hart AH, Hartley L, Parker K, et al. The pluripotency homeobox gene NANOG is expressed in human germ cell tumors. Cancer 2005;104(10):2092-2098
107. Pesce M, Scholer HR. Oct-4: gatekeeper in the beginnings of mammalian development. Stem Cells 2001;19(4):271-278
108. Dann CT, Alvarado AL, Molyneux LA, et al. Spermatogonial stem cell self-renewal requires OCT4, a factor downregulated during retinoic acid-induced differentiation. Stem Cells 2008;26(11):2928-2937
109. Catena R, Tiveron C, Ronchi A, et al. Conserved POU binding DNA sites in the Sox2 upstream enhancer regulate gene expression in embryonic and neural stem cells. J Biol Chem 2004;279(40):41846-41857
110. Western P, Maldonado-Saldivia J, van den Bergen J, et al. Analysis of Esg1 expression in pluripotent cells and the germline reveals similarities with Oct4 and Sox2 and differences between human pluripotent cell lines. Stem Cells 2005;23(10):1436-1442