Establishment of a proteomic profile associated with gonocyte and spermatogonial stem cell maturation and differentiation in neonatal mice

Proteomics

Volumn 14, Issue 2-3, 2014, Pages 274-285

  Zheng, Bo ^a   Zhou, Quan ^a   Guo, Yueshuai ^a   Shao, Binbin ^a   Zhou, Tao ^a   Wang, Lei ^a   Zhou, Zuomin ^a   Sha, Jiahao ^a   Guo, Xuejiang ^a   Huang, Xiaoyan ^a  

^a NANJING MEDICAL UNIVERSITY   (China)

Author keywords

Animal proteomics; Differentiation; Gonocyte; Migration; Spermatogonial stem cell

Indexed keywords

GLO1 PROTEIN; MYBBP1A PROTEIN; NUP153 PROTEIN; OLFM4 PROTEIN; PPM1B PROTEIN; PROTEIN; PROTEOME; SAFB2 PROTEIN; SEC62 PROTEIN; SUZ12 PROTEIN; TINAGL1 PROTEIN; TUBULIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOINFORMATICS; CELL DIFFERENTIATION; CELL MATURATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FUNCTIONAL PROTEOMICS; GONOCYTE; HUMAN; HUMAN CELL; HUMAN VERSUS ANIMAL COMPARISON; IMMUNOLOCALIZATION; MALE; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PUERPERIUM; SPERMATOGENESIS; SPERMATOGONIAL STEM CELL; SPERMATOGONIUM; STEM CELL; TESTIS; TESTIS CELL; TIME; WESTERN BLOTTING;

ANIMAL PROTEOMICS; DIFFERENTIATION; GONOCYTE; MIGRATION; SPERMATOGONIAL STEM CELL;

ANIMALS; ANIMALS, NEWBORN; CELL PROLIFERATION; CELLS, CULTURED; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; MICE; PROTEOME; PROTEOMICS; SPERMATOGENESIS; SPERMATOGONIA; STEM CELLS; TESTIS;

EID: 84892857500     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201300395     Document Type: Article

References (57)

1. Kolasa, A., Misiakiewicz, K., Marchlewicz, M., Wiszniewska, B., The generation of spermatogonial stem cells and spermatogonia in mammals. Reprod. Biol. 2012, 12, 5-23.
2. Wu, Z., Luby-Phelps, K., Bugde, A., Molyneux, L. A. et al., Capacity for stochastic self-renewal and differentiation in mammalian spermatogonial stem cells. J. Cell. Biol. 2009, 187, 513-524.
3. McLean, D. J., Friel, P. J., Johnston, D. S., Griswold, M. D., Characterization of spermatogonial stem cell maturation and differentiation in neonatal mice. Biol. Reprod. 2003, 69, 2085-2091.
4. Bellve, A. R., Cavicchia, J. C., Millette, C. F., O'Brien, D. A. et al., Spermatogenic cells of the prepuberal mouse. Isolation and morphological characterization. J. Cell. Biol. 1977, 74, 68-85.
5. Dettin, L., Ravindranath, N., Hofmann, M. C., Dym, M., Morphological characterization of the spermatogonial subtypes in the neonatal mouse testis. Biol. Reprod. 2003, 69, 1565-1571.
6. Culty, M., Gonocytes, the forgotten cells of the germ cell lineage. Birth Defects Res. C. Embryo Today 2009, 87, 1-26.
7. Nagano, R., Tabata, S., Nakanishi, Y., Ohsako, S. et al., Reproliferation and relocation of mouse male germ cells (gonocytes) during prespermatogenesis. Anat. Rec. 2000, 258, 210-220.
8. Li, H., Papadopoulos, V., Vidic, B., Dym, M., Culty, M., Regulation of rat testis gonocyte proliferation by platelet-derived growth factor and estradiol: identification of signaling mechanisms involved. Endocrinology 1997, 138, 1289-1298.
9. Delbes, G., Levacher, C., Pairault, C., Racine, C. et al., Estrogen receptor beta-mediated inhibition of male germ cell line development in mice by endogenous estrogens during perinatal life. Endocrinology 2004, 145, 3395-3403.
10. De Miguel, M. P., De Boer-Brouwer, M., Paniagua, R., van den Hurk, R. et al., Leukemia inhibitory factor and ciliary neurotropic factor promote the survival of Sertoli cells and gonocytes in coculture system. Endocrinology 1996, 137, 1885-1893.
11. Zhou, Q., Li, Y., Nie, R., Friel, P. et al., Expression of stimulated by retinoic acid gene 8 (Stra8) and maturation of murine gonocytes and spermatogonia induced by retinoic acid in vitro. Biol. Reprod. 2008, 78, 537-545.
12. Orth, J. M., Qiu, J., Jester, W. F., Jr., Pilder, S., Expression of the c-kit gene is critical for migration of neonatal rat gonocytes in vitro. Biol. Reprod. 1997, 57, 676-683.
13. Tres, L. L., Kierszenbaum, A. L., The ADAM-integrin-tetraspanin complex in fetal and postnatal testicular cords. Birth Defects Res. C. Embryo Today 2005, 75, 130-141.
14. Rosselot, C., Kierszenbaum, A. L., Rivkin, E., Tres, L. L., Chronological gene expression of ADAMs during testicular development: prespermatogonia (gonocytes) express fertilin beta (ADAM2). Dev. Dyn. 2003, 227, 458-467.
15. de Rooij, D. G., The spermatogonial stem cell niche. Microsc Res. Tech. 2009, 72, 580-585.
16. Ting, L., Rad, R., Gygi, S. P., Haas, W., MS3 eliminates ratio distortion in isobaric multiplexed quantitative proteomics. Nat. Methods 2011, 8, 937-940.
17. Cox, J., Mann, M., MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 2008, 26, 1367-1372.
18. Magrane, M., Consortium, U., UniProt Knowledgebase: a hub of integrated protein data. Database 2011, 2011, bar009.
19. Deutsch, E. W., Mendoza, L., Shteynberg, D., Farrah, T. et al., A guided tour of the Trans-Proteomic Pipeline. Proteomics 2010, 10, 1150-1159.
20. Cox, J., Mann, M., 1D and 2D annotation enrichment: a statistical method integrating quantitative proteomics with complementary high-throughput data. BMC Bioinformatics 2012, 13 (Suppl 16), S12.
21. Dysvik, B., Jonassen, I., J-Express: exploring gene expression data using Java. Bioinformatics 2001, 17, 369-370.
22. Dennis, G, Jr., Sherman, B. T., Hosack, D. A., Yang, J., DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome. Biol. 2003, 4, P3.
23. Huang, X. Y., Guo, X. J., Shen, J., Wang, Y. F. et al., Construction of a proteome profile and functional analysis of the proteins involved in the initiation of mouse spermatogenesis. J. Proteome Res. 2008, 7, 3435-3446.
24. Wu, X, Schmidt, J. A., Avarbock, M. R., Tobias, J. W. 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, 21672-21677.
25. Jameson, S. A., Natarajan, A., Cool, J., DeFalco, T. et al., Temporal transcriptional profiling of somatic and germ cells reveals biased lineage priming of sexual fate in the fetal mouse gonad. PLoS Genet. 2012, 8, e1002575.
26. Sanz, E., Evanoff, R., Quintana, A., Evans, E. et al., RiboTag analysis of actively translated mRNAs in Sertoli and Leydig cells in vivo. PLoS One 2013, 8, e66179.
27. Costoya, J. A., Hobbs, R. M., Barna, M., Cattoretti, G. et al., Essential role of Plzf in maintenance of spermatogonial stem cells. Nat. Genet. 2004, 36, 653-659.
28. Huang, X. Y., Sha, J. H., Proteomics of spermatogenesis: from protein lists to understanding the regulation of male fertility and infertility. Asian J. Androl. 2011, 13, 18-23.
29. Terentiev, A. A., Moldogazieva, N. T., Alpha-fetoprotein: a renaissance. Tumour Biol. 2013, 34, 2075-2091.
30. Ruoslahti, E., Seppala, M., Alpha-fetoprotein in cancer and fetal development. Adv. Cancer Res. 1979, 29, 275-346.
31. Hales, D. B., Xiong, Y., Tur-Kaspa, I., The role of cytokines in the regulation of Leydig cell P450c17 gene expression. J. Steroid Biochem. Mol. Biol. 1992, 43, 907-914.
32. Shi, Y., Schonemann, M. D., Mellon, S. H., Regulation of P450c17 expression in the early embryo depends on GATA factors. Endocrinology 2009, 150, 946-956.
33. Bair, S. R., Mellon, S. H., Deletion of the mouse P450c17 gene causes early embryonic lethality. Mol. Cell. Biol. 2004, 24, 5383-5390.
34. Wang, Z. F., Sirotkin, A. M., Buchold, G. M., Skoultchi, A. I., Marzluff, W. F., The mouse histone H1 genes: gene organization and differential regulation. J. Mol. Biol. 1997, 271, 124-138.
35. Franke, K., Drabent, B., Doenecke, D., Expression of murine H1 histone genes during postnatal development. Biochim. Biophys. Acta 1998, 1398, 232-242.
36. Vani, G., Vanisree, A. J., Shyamaladevi, C. S., Histone H1 inhibits the proliferation of MCF 7 and MDA MB 231 human breast cancer cells. Cell. Biol. Int. 2006, 30, 326-331.
37. Hsu, L. W., Goto, S., Nakano, T., Chen, K. D. et al., The effect of exogenous histone H1 on rat adipose-derived stem cell proliferation, migration, and osteogenic differentiation in vitro. J. Cell. Physiol. 2012, 227, 3417-3425.
38. Hemmings, B. A., Yellowlees, D., Kernohan, J. C., Cohen, P., Purification of glycogen synthase kinase 3 from rabbit skeletal muscle. Copurification with the activating factor (FA) of the (Mg-ATP) dependent protein phosphatase. Eur. J. Biochem. 1981, 119, 443-451.
39. Woodgett, J. R., Molecular cloning and expression of glycogen synthase kinase-3/factor A. EMBO J. 1990, 9, 2431-2438.
40. Kerkela, R., Kockeritz, L., Macaulay, K., Zhou, J. et al., Deletion of GSK-3beta in mice leads to hypertrophic cardiomyopathy secondary to cardiomyoblast hyperproliferation. J. Clin. Invest. 2008, 118, 3609-3618.
41. Liu, H., Remedi, M. S., Pappan, K. L., Kwon, G. et al., Glycogen synthase kinase-3 and mammalian target of rapamycin pathways contribute to DNA synthesis, cell cycle progression, and proliferation in human islets. Diabetes 2009, 58, 663-672.
42. Liu, Y., Tanabe, K., Baronnier, D., Patel, S. et al., Conditional ablation of Gsk-3beta in islet beta cells results in expanded mass and resistance to fat feeding-induced diabetes in mice. Diabetologia 2010, 53, 2600-2610.
43. Lapid, K., Itkin, T., D'Uva, G., Ovadya, Y. et al., GSK3beta regulates physiological migration of stem/progenitor cells via cytoskeletal rearrangement. J. Clin. Invest. 2013, 123, 1705-1717.
44. Sukegawa, J., Blobel, G., A nuclear pore complex protein that contains zinc finger motifs, binds DNA, and faces the nucleoplasm. Cell 1993, 72, 29-38.
45. Nakielny, S., Shaikh, S., Burke, B., Dreyfuss, G., Nup153 is an M9-containing mobile nucleoporin with a novel Ran-binding domain. EMBO J. 1999, 18, 1982-1995.
46. Ullman, K. S., Shah, S., Powers, M. A., Forbes, D. J., The nucleoporin nup153 plays a critical role in multiple types of nuclear export. Mol. Biol. Cell 1999, 10, 649-664.
47. Doye, V., Hurt, E., From nucleoporins to nuclear pore complexes. Curr. Opin. Cell Biol. 1997, 9, 401-411.
48. Hogarth, C., Itman, C., Jans, D. A., Loveland, K. L., Regulated nucleocytoplasmic transport in spermatogenesis: a driver of cellular differentiation? Bioessays 2005, 27, 1011-1025.
49. Cao, R., Zhang, Y., SUZ12 is required for both the histone methyltransferase activity and the silencing function of the EED-EZH2 complex. Mol. Cell 2004, 15, 57-67.
50. Czermin, B., Melfi, R., McCabe, D., Seitz, V. et al., Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 2002, 111, 185-196.
51. Faust, C., Lawson, K. A., Schork, N. J., Thiel, B., Magnuson, T., The Polycomb-group gene eed is required for normal morphogenetic movements during gastrulation in the mouse embryo. Development 1998, 125, 4495-4506.
52. O'Carroll, D., Erhardt, S., Pagani, M., Barton, S. C. et al., The polycomb-group gene Ezh2 is required for early mouse development. Mol. Cell Biol. 2001, 21, 4330-4336.
53. Pasini, D., Bracken, A. P., Jensen, M. R., Lazzerini Denchi, E., Helin, K., Suz12 is essential for mouse development and for EZH2 histone methyltransferase activity. EMBO J. 2004, 23, 4061-4071.
54. Pasini, D., Bracken, A. P., Hansen, J. B., Capillo, M., Helin, K., The polycomb group protein Suz12 is required for embryonic stem cell differentiation. Mol. Cell Biol. 2007, 27, 3769-3779.
55. Renz, A., Fackelmayer, F. O., Purification and molecular cloning of the scaffold attachment factor B (SAF-B), a novel human nuclear protein that specifically binds to S/MAR-DNA. Nucleic Acids Res. 1996, 24, 843-849.
56. Townson, S. M., Dobrzycka, K. M., Lee, A. V., Air, M. et al., SAFB2, a new scaffold attachment factor homolog and estrogen receptor corepressor. J. Biol. Chem. 2003, 278, 20059-20068.
57. Sergeant, K. A., Bourgeois, C. F., Dalgliesh, C., Venables, J. P. et al., Alternative RNA splicing complexes containing the scaffold attachment factor SAFB2. J. Cell Sci. 2007, 120, 309-319.