Wnt signaling promotes proliferation and stemness regulation of spermatogonial stem/progenitor cells

Reproduction

Volumn 138, Issue 1, 2009, Pages 151-162

  Golestaneh, Nady ^a   Beauchamp, Elspeth ^a   Fallen, Shannon ^a   Kokkinaki, Maria ^a   Üren, Aykut ^a   Dym, Martin ^a  

^a GEORGETOWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; TRANSCRIPTION FACTOR; WNT PROTEIN; WNT3A PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL STRUCTURE; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; GERM CELL; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOGONIUM; SPERMATOZOON; TESTIS DEVELOPMENT;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BETA CATENIN; CELL DIFFERENTIATION; CELL MOVEMENT; CELL PROLIFERATION; CELL SHAPE; CELLS, CULTURED; CULTURE MEDIA, CONDITIONED; FRIZZLED RECEPTORS; GENES, REPORTER; HUMANS; MALE; MICE; MICE, INBRED BALB C; PHOSPHOPROTEINS; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SPERMATOGONIA; STEM CELLS; TRANSFECTION; WNT PROTEINS; WNT3A PROTEIN;

MUS;

EID: 70449348455     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-08-0510     Document Type: Article

References (78)

1. Alonso L & Fuchs E 2003 Stem cells in the skin: waste not, Wnt not. Genes and Development 17 1189-1200. (Pubitemid 36583161)
2. Austin TW, Solar GP, Ziegler FC, Liem L & Matthews W 1997 A role for the Wnt gene family in hematopoiesis: expansion of multilineage progenitor cells. Blood 89 3624-3635. (Pubitemid 27227085)
3. Bafico A, Gazit A, Wu-Morgan SS, Yaniv A & Aaronson SA 1998 Characterization of Wnt-1 and Wnt-2 induced growth alterations and signaling pathways in NIH3T3 fibroblasts. Oncogene 16 2819-2825. (Pubitemid 28279349)
4. Behrens J, von Kries JP, Kuhl M, Bruhn L, Wedlich D, Grosschedl R & Birchmeier W 1996 Functional interaction of beta-catenin with the transcription factor LEF-1. Nature 382 638-642. (Pubitemid 26268958)
5. Bellvé AR, Cavicchia JC, Millette CF, O'Brien DA, Bhatnagar YM & Dym M 1977 Spermatogenic cells of the prepuberal mouse. Isolation and morphological characterization. Journal of Cell Biology 74 68-85. (Pubitemid 8141486)
6. Van Den Berg DJ, Sharma AK, Bruno E & Hoffman R 1998 Role of members of the Wnt gene family in human hematopoiesis. Blood 92 3189-3202. (Pubitemid 28492326)
7. Boyer A, Hermo L, Paquet M, Robaire B & Boerboom D 2008 Seminiferous tubule degeneration and infertility in mice with sustained activation of WNT/CTNNB1 signaling in sertoli cells. Biology of Reproduction 79 475-485.
8. Braydich-Stolle L, Nolan C, Dym M & Hofmann MC 2005 Role of glial cell line-derived neurotrophic factor in germ-line stem cell fate. Annals of the New York Academy of Sciences 1061 94-99. (Pubitemid 43211589)
9. Braydich-Stolle L, Kostereva N, Dym M & Hofmann MC 2007 Role of Src family kinases and N-Myc in spermatogonial stem cell proliferation. Developmental Biology 304 34-45. (Pubitemid 46399669)
10. Brinster RL 2002 Germline stem cell transplantation and transgenesis. Science 296 2174-2176. (Pubitemid 34680289)
11. Brown AM 2005 Canonical Wnt signaling: high-throughput RNAi widens the path. Genome Biology 6 231.
12. Bryja V, Schulte G & Arenas E 2007 Wnt-3a utilizes a novel low dose and rapid pathway that does not require casein kinase 1-mediated phosphorylation of Dvl to activate β-catenin. Cellular Signalling 19 610-616. (Pubitemid 46107812)
13. Buageaw A, Sukhwani M, Ben-Yehudah A, Ehmcke J, Rawe VY, Pholpramool C, Orwig KE & Schlatt S 2005 GDNF family receptor alpha1 phenotype of spermatogonial stem cells in immature mouse testes. Biology of Reproduction 73 1011-1016. (Pubitemid 41507506)
14. Cadigan KM & Liu YI 2006 Wnt signaling: complexity at the surface. Journal of Cell Science 119 395-402.
15. Cadigan KM & Nusse R 1997 Wnt signaling: a common theme in animal development. Genes and Development 11 3286-3305. (Pubitemid 28023954)
16. Cai L, Ye Z, Zhou BY, Mali P, Zhou C & Cheng L 2007 Promoting human embryonic stem cell renewal or differentiation by modulating Wnt signal and culture conditions. Cell Research 17 62-72. (Pubitemid 46096426)
17. Chen K, Fallen S, Abaan HO, Hayran M, Gonzalez C, Wodajo F, MacDonald T, Toretsky JA & Uren A 2008 WNT10B induces chemotaxis of osteosarcoma and correlates with reduced survival. Pediatric Blood and Cancer 51 349-355.
18. Coveney D, Ross AJ, Slone JD & Capel B 2007 A microarray analysis of the XX Wnt4 mutant gonad targeted at the identification of genes involved in testis vascular differentiation. Gene Expression Patterns 7 82-92. (Pubitemid 44712730)
19. DasGupta R & Fuchs E 1999 Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development 126 4557-4568.
20. Dravid G, Ye Z, Hammond H, Chen G, Pyle A, Donovan P, Yu X & Cheng L 2005 Defining the role of Wnt/beta-catenin signaling in the survival, proliferation, and self-renewal of human embryonic stem cells. Stem Cells 23 1489-1501. (Pubitemid 41740998)
21. Du SJ, Purcell SM, Christian JL, McGrew LL & Moon RT 1995 Identification of distinct classes and functional domains of Wnts through expression of wild-type and chimeric proteins in Xenopus embryos. Molecular and Cellular Biology 15 2625-2634.
22. Dym M 1994 Spermatogonial stem cells of the testis. PNAS 91 11287-11289.
23. Dym M, Jia MC, Dirami G, Price JM, Rabin SJ, Mocchetti I & Ravindranath N 1995 Expression of c-kit receptor and its autophosphorylation in immature rat type A spermatogonia. Biology of Reproduction 52 8-19.
24. Golestaneh N, Gallicano GI, Kokkinaki M, Pant D, Jiang J, Destefano D, Fernandez-Bueno C, Rone JD, Haddad BR & Gallicano GI 2009 Pluripotent stem cells derived from adult human testes. Stem Cells and Development [in press]. DOI: 10.1089/scd.2008.0347.
25. Gonzalez-Sancho JM, Brennan KR, Castelo-Soccio LA & Brown AM 2004 Wnt proteins induce dishevelled phosphorylation via an LRP5/6- independent mechanism, irrespective of their ability to stabilize β-catenin. Molecular and Cellular Biology 24 4757-4768.
26. Guan K, Nayernia K, Maier LS, Wagner S, Dressel R, Lee JH, Nolte J, Wolf F, Li M, Engel W et al. 2006 Pluripotency of spermatogonial stem cells from adult mouse testis. Nature 440 1199-1203.
27. Hao J, Li TG, Qi X, Zhao DF & Zhao GQ 2006 WNT/beta-catenin pathway up-regulates Stat3 and converges on LIF to prevent differentiation of mouse embryonic stem cells. Developmental Biology 290 81-91. (Pubitemid 43083605)
28. He XC, Zhang J, Tong WG, Tawfik O, Ross J, Scoville DH, Tian Q, Zeng X, He X, Wiedemann LM et al. 2004 BMP signaling inhibits intestinal stem cell self-renewal through suppression of Wnt-beta-catenin signaling. Nature Genetics 36 1117-1121. (Pubitemid 41184475)
29. He Z, Jiang J, Hofmann MC & Dym M 2007 Gfra1 silencing in mouse spermatogonial stem cells results in their differentiation via the inactivation of RET tyrosine kinase. Biology of Reproduction 77 723-733. (Pubitemid 47494388)
30. He Z, Jiang J, Kokkinaki M, Golestaneh N, Hofmann MC & Dym M 2008 Gdnf upregulates c-Fos transcription via the Ras/Erk1/2 pathway to promote mouse spermatogonial stem cell proliferation. Stem Cells 26 266-278.
31. Hofmann MC, Braydich-Stolle L, Dettin L, Johnson E & Dym M 2005a Immortalization of mouse germ line stem cells. Stem Cells 23 200-210. (Pubitemid 40239515)
32. Hofmann MC, Braydich-Stolle L & Dym M 2005b Isolation of male germ-line stem cells; influence of GDNF. Developmental Biology 279 114-124. (Pubitemid 40222173)
33. Hsieh M, Boerboom D, Shimada M, Lo Y, Parlow AF, Luhmann UF, Berger W & Richards JS 2005 Mice null for Frizzled4 (Fzd4-/-) are infertile and exhibit impaired corpora lutea formation and function. Biology of Reproduction 73 1135-1146. (Pubitemid 41698603)
34. Huelsken J, Vogel R, Brinkmann V, Erdmann B, Birchmeier C & Birchmeier W 2000 Requirement for beta-catenin in anterior-posterior axis formation in mice. Journal of Cell Biology 148 567-578. (Pubitemid 30682568)
35. Jeays-Ward K, Hoyle C, Brennan J, Dandonneau M, Alldus G, Capel B & Swain A 2003 Endothelial and steroidogenic cell migration are regulated by WNT4 in the developing mammalian gonad. Development 130 3663-3670. (Pubitemid 37039072)
36. Jordan BK, Shen JH, Olaso R, Ingraham HA & Vilain E 2003 Wnt4 overexpression disrupts normal testicular vasculature and inhibits testosterone synthesis by repressing steroidogenic factor 1/beta-catenin synergy. PNAS 100 10866-10871. (Pubitemid 37140119)
37. Kanatsu-Shinohara M, Ogonuki N, Inoue K, Miki H, Ogura A, Toyokuni S & Shinohara T 2003 Long-term proliferation in culture and germline transmission of mouse male germline stem cells. Biology of Reproduction 69 612-616. (Pubitemid 36885967)
38. Katoh M 2001 Molecular cloning and characterization of human WNT3. International Journal of Oncology 19 977-982.
39. Kirstetter P, Anderson K, Porse BT, Jacobsen SE & Nerlov C 2006 Activation of the canonical Wnt pathway leads to loss of hematopoietic stem cell repopulation and multilineage differentiation block. Nature Immunology 7 1048-1056. (Pubitemid 44420649)
40. Kleber M & Sommer L 2004 Wnt signaling and the regulation of stem cell function. Current Opinion in Cell Biology 16 681-687. (Pubitemid 39463120)
41. Kohn AD & Moon RT 2005 Wnt and calcium signaling: beta-cateninindependent pathways. Cell Calcium 38 439-446. (Pubitemid 41283282)
42. Kubota H, Avarbock MR & Brinster RL 2004a Culture conditions and single growth factors affect fate determination of mouse spermatogonial stem cells. Biology of Reproduction 71 722-731. (Pubitemid 39108631)
43. Kubota H, Avarbock MR & Brinster RL 2004b Growth factors essential for self-renewal and expansion of mouse spermatogonial stem cells. PNAS 101 16489-16494. (Pubitemid 39557740)
44. 2+ pathway: a new vertebrate Wnt signaling pathway takes shape. Trends in Genetics 16 279-283.
45. Lee C & Cho Y 2002 Interactions of SV40 large T antigen and other viral proteins with retinoblastoma tumour suppressor. Reviews in Medical Virology 12 81-92. (Pubitemid 34273043)
46. Lin H 1997 The tao of stem cells in the germline. Annual Review of Genetics 31 455-491.
47. Logan CY & Nusse R 2004 The Wnt signaling pathway in development and disease. Annual Review of Cell and Developmental Biology 20 781-810. (Pubitemid 39488658)
48. Ma P, Wang H, Guo R, Ma Q, Yu Z, Jiang Y, Ge Y, Ma J, Xue S & Han D 2006 Stage-dependent Dishevelled-1 expression during mouse spermatogenesis suggests a role in regulating spermatid morphological changes. Molecular Reproduction and Development 73 774-783.
49. Meng X, Lindahl M, Hyvonen ME, Parvinen M, de Rooij DG, Hess MW, Raatikainen-Ahokas A, Sainio K, Rauvala H, Lakso M et al. 2000 Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science 287 1489-1493. (Pubitemid 30127143)
50. Molenaar M, van de Wetering M, Oosterwegel M, Peterson-Maduro J, Godsave S, Korinek V, Roose J, Destree O & Clevers H 1996 XTcf-3 transcription factor mediates beta-catenin-induced axis formation in Xenopus embryos. Cell 86 391-399. (Pubitemid 26272079)
51. Moon RT, Kohn AD, De Ferrari GV & Kaykas A 2004 WNTand beta-catenin signalling: diseases and therapies. Nature Reviews. Genetics 5 691-701. (Pubitemid 39150127)
52. Murdoch B, Chadwick K, Martin M, Shojaei F, Shah KV, Gallacher L, Moon RT & Bhatia M 2003 Wnt-5A augments repopulating capacity and primitive hematopoietic development of human blood stem cells in vivo. PNAS 100 3422-3427. (Pubitemid 36356599)
53. Nelson WJ & Nusse R 2004 Convergence of Wnt, beta-catenin, and cadherin pathways. Science 303 1483-1487. (Pubitemid 38314410)
54. Nusse R 2008 Wnt signaling and stem cell control. Cell Research 18 523-527. (Pubitemid 351630946)
55. Ogawa K, Nishinakamura R, Iwamatsu Y, Shimosato D & Niwa H 2006 Synergistic action of Wnt and LIF in maintaining pluripotency of mouse ES cells. Biochemical and Biophysical Research Communications 343 159-166.
56. Ohta H, Yomogida K, Dohmae K & Nishimune Y 2000 Regulation of proliferation and differentiation in spermatogonial stem cells: the role of c-kit and its ligand SCF. Development 127 2125-2131. (Pubitemid 30386676)
57. Otero JJ, Fu W, Kan L, Cuadra AE & Kessler JA 2004 Beta-catenin signaling is required for neural differentiation of embryonic stem cells. Development 131 3545-3557. (Pubitemid 39199366)
58. Peifer M & Polakis P 2000 Wnt signaling in oncogenesis and embryogenesis - a look outside the nucleus. Science 287 1606-1609. (Pubitemid 30127755)
59. Peters JM, McKay RM, McKay JP & Graff JM 1999 Casein kinase I transduces Wnt signals. Nature 401 345-350.
60. Pinto D & Clevers H 2005 Wnt control of stem cells and differentiation in the intestinal epithelium. Experimental Cell Research 306 357-363. (Pubitemid 40732761)
61. Rena G, Bain J, Elliott M & Cohen P 2004 D4476, a cell-permeant inhibitor of CK1, suppresses the site-specific phosphorylation and nuclear exclusion of FOXO1a. EMBO Reports 5 60-65. (Pubitemid 38228529)
62. Reya T, Morrison SJ, Clarke MF & Weissman IL 2001 Stem cells, cancer, and cancer stem cells. Nature 414 105-111.
63. Ricken A, Lochhead P, Kontogiannea M & Farookhi R 2002 Wnt signaling in the ovary: identification and compartmentalized expression of wnt-2, wnt-2b, and frizzled-4 mRNAs. Endocrinology 143 2741-2749. (Pubitemid 34701338)
64. de Rooij DG 1998 Stem cells in the testis. International Journal of Experimental Pathology 79 67-80.
65. de Rooij DG 2001 Proliferation and differentiation of spermatogonial stem cells. Reproduction 121 347-354. (Pubitemid 32243678)
66. Sato N, Meijer L, Skaltsounis L, Greengard P & Brivanlou AH 2004 Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nature Medicine 10 55-63. (Pubitemid 38524699)
67. von Schalburg KR, McCarthy SP, Rise ML, Hutson JC, Davidson WS & Koop BF 2006 Expression of morphogenic genes in mature ovarian and testicular tissues: potential stem-cell niche markers and patterning factors. Molecular Reproduction and Development 73 142-152.
68. Scheller M, Huelsken J, Rosenbauer F, Taketo MM, Birchmeier W, Tenen DG & Leutz A 2006 Hematopoietic stem cell and multilineage defects generated by constitutive beta-catenin activation. Nature Immunology 7 1037-1047. (Pubitemid 44420648)
69. Seandel M, James D, Shmelkov SV, Falciatori I, Kim J, Chavala S, Scherr DS, Zhang F, Torres R, Gale NW et al. 2007 Generation of functional multipotent adult stem cells from GPR125+ germline progenitors. Nature 449 346-350. (Pubitemid 47443477)
70. Shibamoto S, Higano K, Takada R, Ito F, Takeichi M & Takada S 1998 Cytoskeletal reorganization by soluble Wnt-3a protein signalling. Genes to Cells 3 659-670. (Pubitemid 28557207)
71. Trowbridge JJ, Moon RT & Bhatia M 2006 Hematopoietic stem cell biology: too much of a Wnt thing. Nature Immunology 7 1021-1023. (Pubitemid 44420645)
72. Tumbar T, Guasch G, Greco V, Blanpain C, Lowry WE, Rendl M & Fuchs E 2004 Defining the epithelial stem cell niche in skin. Science 303 359-363. (Pubitemid 38095773)
73. Uren A, Wolf V, Sun YF, Azari A, Rubin JS & Toretsky JA 2004 Wnt/Frizzled signaling in Ewing sarcoma. Pediatric Blood and Cancer 43 243-249.
74. Veeman MT, Axelrod JD & Moon RT 2003 A second canon. Functions and mechanisms of beta-catenin-independent Wnt signaling. Developmental Cell 5 367-377.
75. van deWetering M, Cavallo R, Dooijes D, van Beest M, van Es J, Loureiro J, Ypma A, Hursh D, Jones T, Bejsovec A et al. 1997 Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell 88 789-799.
76. Willert K & Jones KA 2006 Wnt signaling: is the party in the nucleus? Genes and Development 20 1394-1404.
77. Willert K, Brown JD, Danenberg E, Duncan AW, Weissman IL, Reya T, Yates JR III & Nusse R 2003 Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 423 448-452. (Pubitemid 36626997)
78. Yoshida S, Sukeno M & Nabeshima Y 2007 A vasculature-associated niche for undifferentiated spermatogonia in the mouse testis. Science 317 1722-1726. (Pubitemid 47461832)