Characterization of spermatogonial stem cells lacking intercellular bridges and genetic replacement of a mutation in spermatogonial stem cells

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Iwamori, Naoki ^a   Iwamori, Tokuko ^a   Matzuk, Martin M ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 4 INHIBITOR; CYCLIN E; PROTEIN; PROTEIN SERINE THREONINE KINASE INHIBITOR; TESTIS EXPRESSED GENE 14; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL JUNCTION; CELL PROLIFERATION; CELL RENEWAL; CONTROLLED STUDY; DOWN REGULATION; GENE ACTIVATION; GENE MUTATION; GENE THERAPY; HOMOLOGOUS RECOMBINATION; IN VITRO STUDY; MOUSE; NONHUMAN; REGENERATIVE MEDICINE; REPRODUCTION; SPERMATOGONIAL STEM CELL; SPERMATOGONIUM; STEM CELL; TESTIS; UPREGULATION;

ANIMALS; BASE SEQUENCE; CELL SEPARATION; DNA PRIMERS; HETEROZYGOTE; MALE; MICE; MUTATION; REAL-TIME POLYMERASE CHAIN REACTION; RECOMBINATION, GENETIC; SPERMATOGONIA; STEM CELLS; TESTIS; TRANSCRIPTION FACTORS;

EID: 84862198307     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0038914     Document Type: Article

References (39)

1. Hochedlinger K, Rideout WM, Kyba M, Daley GQ, Blelloch R, et al. (2004) Nuclear transplantation, embryonic stem cells and the potential for cell therapy. Hematol J 5: S114-117.
2. Lerou PH, Daley GQ, (2005) Therapeutic potential of embryonic stem cells. Blood Rev 19: 321-331.
3. Rideout WM III, Hochedlinger K, Kyba M, Daley GQ, Jaenisch R, (2002) Correction of a genetic defect by nuclear transplantation and combined cell and gene therapy. Cell 109: 17-27.
4. Hanna J, Wernig M, Markoulaki S, Sun CW, Meissner A, et al. (2007) Treatment of sickle cell anemia mouse model with iPS cells generated from autologous skin. Science 318: 1920-1923.
5. Howden SE, Gore A, Li Z, Fung HL, Nisler BS, et al. (2011) Genetic correction and analysis of induced pluripotent stem cells from a patient with gyrate atrophy. Proc Natl Acad Sci U S A 108: 6537-6542.
6. Brinster RL, Avarbock MR, (1994) Germline transmission of donor haplotype following spermatogonial transplantation. Proc Natl Acad Sci U S A 91: 11303-11307.
7. Kanatsu-Shinohara M, Ogonuki N, Inoue K, Miki H, Ogura A, et al. (2003) Long-term proliferation in culture and germline transmission of mouse male germline stem cells. Biol Reprod 69: 612-616.
8. Seandel M, James D, Shmelkov SV, Falciatori I, Kim J, et al. (2007) Generation of functional multipotent adult stem cells from GPR125+ germline progenitors. Nature 449: 346-350.
9. Ko K, Tapia N, Wu G, Kim JB, Bravo MJ, et al. (2009) Induction of pluripotency in adult unipotent germline stem cells. Cell Stem Cell 5: 87-96.
10. Oatley JM, Brinster RL, (2008) Regulation of spermatogonial stem cell self-renewal in mammals. Annu Rev Cell Dev Biol 24: 263-286.
11. Caires K, Broady J, McLean D, (2010) Maintaining the male germline: regulation of spermatogonial stem cells. J Endocrinol 205: 133-145.
12. Kanatsu-Shinohara M, Toyokuni S, Shinohara T, (2004) CD9 is a surface marker on mouse and rat male germline stem cells. Biol Reprod 70: 70-75.
13. Tokuda M, Kadokawa Y, Kurahashi H, Marunouchi T, (2007) CDH1 is a specific marker for undifferentiated spermatogonia in mouse testes. Biol Reprod 76: 130-141.
14. Ryu BY, Orwig KE, Kubota H, Avarbock MR, Brinster RL, (2004) Phenotypic and functional characteristics of spermatogonial stem cells in rats. Dev Biol 274: 158-170.
15. Kanatsu-Shinohara M, Takashima S, Ishii K, Shinohara T, (2011) Dynamic changes in EPCAM expression during spermatogonial stem cell differentiation in the mouse testis. PLoS One 6: e23663.
16. Naughton CK, Jain S, Strickland AM, Gupta A, Milbrandt J, (2006) Glial cell-line derived neurotrophic factor-mediated RET signaling regulates spermatogonial stem cell fate. Biol Reprod 74: 314-321.
17. Oatley JM, Avarbock MR, Telaranta AI, Fearon DT, Brinster RL, (2006) Identifying genes important for spermatogonial stem cell self-renewal and survival. Proc Natl Acad Sci U S A 103: 9524-9529.
18. Buaas FW, Kirsh AL, Sharma M, McLean DJ, Morris JL, et al. (2004) Plzf is required in adult male germ cells for stem cell self-renewal. Nat Genet 36: 647-652.
19. Costoya JA, Hobbs RM, Barna M, Cattoretti G, Manova K, et al. (2004) Essential role of Plzf in maintenance of spermatogonial stem cells. Nat Genet 36: 653-659.
20. Oatley MJ, Kaucher AV, Racicot KE, Oatley JM, (2011) 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 85: 347-356.
21. Sada A, Suzuki A, Suzuki H, Saga Y, (2009) The RNA-binding protein NANOS2 is required to maintain murine spermatogonial stem cells. Science 325: 1394-1398.
22. Falender AE, Freiman RN, Geles KG, Lo KC, Hwang K, et al. (2005) Maintenance of spermatogenesis requires TAF4b, a gonad-specific subunit of TFIID. Genes Dev 19: 794-803.
23. Yoshida S, Takakura A, Ohbo K, Abe K, Wakabayashi J, et al. (2004) Neurogenin3 delineates the earliest stages of spermatogenesis in the mouse testis. Dev Biol 269: 447-458.
24. Sadate-Ngatchou PI, Payne CJ, Dearth AT, Braun RE, (2008) Cre recombinase activity specific to postnatal, premeiotic male germ cells in transgenic mice. Genesis 46: 738-742.
25. Zhou Q, Li Y, Nie R, Friel P, Mitchell D, et al. (2008) Expression of stimulated by retinoic acid gene 8 (Stra8) and maturation of murine gonocytes and spermatogonia induced by retinoic acid in vitro. Biol Reprod 78: 537-545.
26. Shinohara T, Avarbock MR, Brinster RL, (1999) beta1- and alpha6-integrin are surface markers on mouse spermatogonial stem cells. Proc Natl Acad Sci U S A 96: 5504-5509.
27. Toyooka Y, Tsunekawa N, Takahashi Y, Matsui Y, Satoh M, et al. (2000) Expression and intracellular localization of mouse Vasa-homologue protein during germ cell development. Mech Dev 93: 139-149.
28. Huckins C, Oakberg EF, (1978) Morphological and quantitative analysis of spermatogonia in mouse testes using whole mounted seminiferous tubules, I. The normal testes. Anat Rec 192: 519-528.
29. Greenbaum MP, Iwamori T, Buchold GM, Matzuk MM, (2011) Germ cell intercellular bridges. Cold Spring Harb Perspect Biol 3: a005850.
30. Greenbaum MP, Yan W, Wu MH, Lin YN, Agno JE, et al. (2006) TEX14 is essential for intercellular bridges and fertility in male mice. Proc Natl Acad Sci U S A 103: 4982-4987.
31. Greenbaum MP, Ma L, Matzuk MM, (2007) Conversion of midbodies into germ cell intercellular bridges. Dev Biol 305: 389-396.
32. Iwamori T, Iwamori N, Ma L, Edson MA, Greenbaum MP, et al. (2010) TEX14 interacts with CEP55 to block cell abscission. Mol Cell Biol 30: 2280-2292.
33. Ogawa T, Arechaga JM, Avarbock MR, Brinster RL, (1997) Transplantation of testis germinal cells into mouse seminiferous tubules. Int J Dev Biol 41: 111-122.
34. Wu MH, Rajkovic A, Burns KH, Yan W, Lin YN, et al. (2003) Sequence and expression of testis-expressed gene 14 (Tex14): a gene encoding a protein kinase preferentially expressed during spermatogenesis. Gene Expr Patterns 3: 231-236.
35. Zhou Q, Griswold MD, (2008) Regulation of spermatogonia. StemBook 2010/07/09 ed. Cambridge (MA): Harvard Stem Cell Institute.
36. Yoshida S, Sukeno M, Nabeshima Y, (2007) A vasculature-associated niche for undifferentiated spermatogonia in the mouse testis. Science 317: 1722-1726.
37. Nakagawa T, Sharma M, Nabeshima Y, Braun RE, Yoshida S, (2010) Functional hierarchy and reversibility within the murine spermatogenic stem cell compartment. Science 328: 62-67.
38. Kanatsu-Shinohara M, Ikawa M, Takehashi M, Ogonuki N, Miki H, et al. (2006) Production of knockout mice by random or targeted mutagenesis in spermatogonial stem cells. Proc Natl Acad Sci U S A 103: 8018-8023.
39. Kanatsu-Shinohara M, Kato-Itoh M, Ikawa M, Takehashi M, Sanbo M, et al. (2011) Homologous recombination in rat germline stem cells. Biol Reprod 85: 208-217.