Determination of protein interactome of transcription factor Sox2 in embryonic stem cells engineered for inducible expression of four reprogramming factors

Journal of Biological Chemistry

Volumn 287, Issue 14, 2012, Pages 11384-11397

  Gao, Zhiguang ^a,d   Cox, Jesse L ^a   Gilmore, Joshua M ^b,c   Ormsbee, Briana D ^a   Mallanna, Sunil K ^a,e   Washburn, Michael P ^b,c   Rizzino, Angie ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^c UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^e UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DETERMINATION OF PROTEINS; EMBRYONIC STEM CELLS; HIGHLY INTEGRATED; INDUCIBLE EXPRESSION; MASTER REGULATORS; MULTIDIMENSIONAL PROTEINS; PROTEIN-PROTEIN INTERACTION NETWORKS; PROTEIN-PROTEIN INTERACTIONS;

ANTIGENS; TRANSCRIPTION FACTORS;

ANTIBODIES;

KRUPPEL LIKE FACTOR 4; MYC PROTEIN; NUCLEAR RECEPTOR DAX 1; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN ESRRB; PROTEIN NAC1; PROTEIN POLB; PROTEIN RBPJ; PROTEIN REX1; PROTEIN RPA1; PROTEIN RPA2; PROTEIN RPA3; PROTEIN SALL4; PROTEIN SMARCD1; PROTEIN TCFCP211; PROTEIN TOP2A; PROTEIN XRCC5; PROTEIN XRCC7; PROTEIN ZFP281; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; XRCC1 PROTEIN;

ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL ENGINEERING; CELL RENEWAL; CONTROLLED STUDY; EMBRYONIC STEM CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEOMICS; SELF RENEW;

ANIMALS; CELL DIFFERENTIATION; CELL ENGINEERING; CHROMOSOMAL PROTEINS, NON-HISTONE; EMBRYONIC STEM CELLS; EPITOPE MAPPING; GENE EXPRESSION; GENE KNOCKDOWN TECHNIQUES; HUMANS; KINESIN; MICE; OCTAMER TRANSCRIPTION FACTOR-3; PROTEIN INTERACTION MAPPING; PROTEOMICS; PROTO-ONCOGENE PROTEINS C-MYC; SOXB1 TRANSCRIPTION FACTORS;

EID: 84859313829     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.320143     Document Type: Article

References (40)

1. Boer, B., Kopp, J., Mallanna, S., Desler, M., Chakravarthy, H., Wilder, P. J., Bernadt, C., and Rizzino, A. (2007) Elevating the levels of Sox2 in embryonal carcinoma cells and embryonic stem cells inhibits the expression of Sox2:Oct-3/4 target genes. Nucleic Acids Res. 35, 1773-1786 (Pubitemid 47061649)
2. Rizzino, A. (2009) Sox2 and Oct-3/4. A versatile pair of master regulators that orchestrate the self-renewal and pluripotency of embryonic stem cells. Wiley Interdiscip. Rev. Syst. Biol. Med. 1, 228-236
3. Niwa, H., Miyazaki, J., and Smith, A. G. (2000) Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation, or self-renewal of ES cells. Nat. Genet. 24, 372-376 (Pubitemid 30187435)
4. Chew, J. L., Loh, Y. H., Zhang, W., Chen, X., Tam, W. L., Yeap, L. S., Li, P., Ang, Y. S., Lim, B., Robson, P., and Ng, H. H. (2005) Reciprocal transcriptional regulation of Pou5f1 and Sox2 via the Oct4/Sox2 complex in embryonic stem cells. Mol. Cell. Biol. 25, 6031-6046 (Pubitemid 40946556)
5. Kopp, J. L., Ormsbee, B. D., Desler, M., and Rizzino, A. (2008) Small increases in the level of Sox2 trigger the differentiation of mouse embryonic stem cells. Stem Cells 26, 903-911
6. Mitsui, K., Tokuzawa, Y., Itoh, H., Segawa, K., Murakami, M., Takahashi, K., Maruyama, M., Maeda, M., and Yamanaka, S. (2003) The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113, 631-642 (Pubitemid 36694188)
7. Chambers, I., Silva, J., Colby, D., Nichols, J., Nijmeijer, B., Robertson, M., Vrana, J., Jones, K., Grotewold, L., and Smith, A. (2007) Nanog safeguards pluripotency and mediates germ line development. Nature 450, 1230-1234
8. Zhang, P., Andrianakos, R., Yang, Y., Liu, C., and Lu, W. (2010) Kruppel-like factor 4 (Klf4) prevents embryonic stem (ES) cell differentiation by regulating Nanog gene expression. J. Biol. Chem. 285, 9180-9189
9. Cartwright, P., McLean, C., Sheppard, A., Rivett, D., Jones, K., and Dalton, S. (2005) LIF/STAT3 controls ES cell self-renewal and pluripotency by a Myc-dependent mechanism. Development 132, 885-896 (Pubitemid 40484924)
10. Boyer, L. A., Lee, T. I., Cole, M. F., Johnstone, S. E., Levine, S. S., Zucker, J. P., Guenther, M. G., Kumar, R. M., Murray, H. L., Jenner, R. G., Gifford, D. K., Melton, D. A., Jaenisch, R., and Young, R. A. (2005) Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122, 947-956 (Pubitemid 41345211)
11. Chen, X., Xu, H., Yuan, P., Fang, F., Huss, M., Vega, V. B., Wong, E., Orlov, Y. L., Zhang, W., Jiang, J., Loh, Y. H., Yeo, H. C., Yeo, Z. X., Narang, V., Govindarajan, K. R., Leong, B., Shahab, A., Ruan, Y., Bourque, G., Sung, W. K., Clarke, N. D., Wei, C. L., and Ng, H. H. (2008) Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133, 1106-1117 (Pubitemid 351787745)
12. Wang, J., Rao, S., Chu, J., Shen, X., Levasseur, D. N., Theunissen, T. W., and Orkin, S. H. (2006) A protein interaction network for pluripotency of embryonic stem cells. Nature 444, 364-368 (Pubitemid 44764111)
13. Liang, J., Wan, M., Zhang, Y., Gu, P., Xin, H., Jung, S. Y., Qin, J., Wong, J., Cooney, A. J., Liu, D., and Songyang, Z. (2008) Nanog and Oct4 associate with unique transcriptional repression complexes in embryonic stem cells. Nat. Cell Biol. 10, 731-739 (Pubitemid 351772939)
14. van den Berg, D. L., Snoek, T., Mullin, N. P., Yates, A., Bezstarosti, K., Demmers, J., Chambers, I., and Poot, R. A. (2010) An Oct4-centered protein interaction network in embryonic stem cells. Cell Stem Cell 6, 369-381
15. Pardo, M., Lang, B., Yu, L., Prosser, H., Bradley, A., Babu, M. M., and Choudhary, J. (2010) An expanded Oct4 interaction network. Implications for stem cell biology, development, and disease. Cell Stem Cell 6, 382-395
16. Ding, J., Xu, H., Faiola, F., Ma'ayan, A., and Wang, J. (2012) Oct4 links multiple epigenetic pathways to the pluripotency network. Cell Res. 22, 155-167
17. Mallanna, S. K., Ormsbee, B. D., Iacovino, M., Gilmore, J. M., Cox, J. L., Kyba, M., Washburn, M. P., and Rizzino, A. (2010) Proteomic analysis of Sox2-associated proteins during early stages of mouse embryonic stem cell differentiation identifies Sox21 as a novel regulator of stem cell fate. Stem Cells 28, 1715-1727
18. Cox, J. L., Mallanna, S. K., Ormsbee, B. D., Desler, M., Wiebe, M. S., and Rizzino, A. (2011) Banf1 is required to maintain the self-renewal of both mouse and human embryonic stem cells. J. Cell Sci. 124, 2654-2665
19. Scherer, P. E., Lewis, R. Y., Volonte, D., Engelman, J. A., Galbiati, F., Couet, J., Kohtz, D. S., van Donselaar, E., Peters, P., and Lisanti, M. P. (1997) Cell-type and tissue-specific expression of caveolin-2. Caveolins 1 and 2 co-localize and form a stable hetero-oligomeric complex in vivo. J. Biol. Chem. 272, 29337-29346 (Pubitemid 27498228)
20. Kelly, D., Scholtz, B., Orten, D. J., Hinrichs, S. H., and Rizzino, A. (1995) Regulation of the transforming growth factor-β 2 gene promoter in embryonal carcinoma cells and their differentiated cells. Differential utilization of transcription factors. Mol. Reprod. Dev. 40, 135-145
21. Zhang, Y., Wen, Z., Washburn, M. P., and Florens, L. (2010) Refinements to label free proteome quantitation: how to deal with peptides shared by multiple proteins. Anal. Chem. 82, 2272-2281
22. Elias, J. E., Haas, W., Faherty, B. K., and Gygi, S. P. (2005) Comparative evaluation of mass spectrometry platforms used in large-scale proteomics investigations. Nat. Methods 2, 667-675 (Pubitemid 41223093)
23. Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., Amin, N., Schwikowski, B., and Ideker, T. (2003) Cytoscape. A software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504 (Pubitemid 37428274)
24. Wiebe, M. S., and Traktman, P. (2007) Poxviral B1 kinase overcomes barrier to autointegration factor, a host defense against virus replication. Cell Host Microbe 1, 187-197 (Pubitemid 46706362)
25. Doetschman, T. C., Eistetter, H., Katz, M., Schmidt, W., and Kemler, R. (1985) The in vitro development of blastocyst-derived embryonic stem cell lines. Formation of visceral yolk sac, blood islands, and myocardium. J. Embryol. Exp. Morphol. 87, 27-45 (Pubitemid 15029925)
26. Beard, C., Hochedlinger, K., Plath, K., Wutz, A., and Jaenisch, R. (2006) Efficient method to generate single-copy transgenic mice by site-specific integration in embryonic stem cells. Genesis 44, 23-28 (Pubitemid 43222207)
27. Karantzali, E., Lekakis, V., Ioannou, M., Hadjimichael, C., Papamatheakis, J., and Kretsovali, A. (2011) Sall1 regulates embryonic stem cell differentiation in association with nanog. J. Biol. Chem. 286, 1037-1045
28. Ivanova, N., Dobrin, R., Lu, R., Kotenko, I., Levorse, J., DeCoste, C., Schafer, X., Lun, Y., and Lemischka, I. R. (2006) Dissecting self-renewal in stem cells with RNA interference. Nature 442, 533-538 (Pubitemid 44167907)
29. Stopka, T., and Skoultchi, A. I. (2003) The ISWI ATPase Snf2h is required for early mouse development. Proc. Natl. Acad. Sci. U.S.A. 100, 14097-14102 (Pubitemid 37499197)
30. Ho, L., Ronan, J. L., Wu, J., Staahl, B. T., Chen, L., Kuo, A., Lessard, J., Nesvizhskii, A. I., Ranish, J., and Crabtree, G. R. (2009) An embryonic stem cell chromatin remodeling complex, esBAF, is essential for embryonic stem cell self-renewal and pluripotency. Proc. Natl. Acad. Sci. U.S.A. 106, 5181-5186
31. Farthing, C. R., Ficz, G., Ng, R. K., Chan, C. F., Andrews, S., Dean, W., Hemberger, M., and Reik, W. (2008) Global mapping of DNA methylation in mouse promoters reveals epigenetic reprogramming of pluripotency genes. PLoS Genet. 4, e1000116
32. Takahashi, K., and Yamanaka, S. (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676 (Pubitemid 44233629)
33. Mallanna, S. K., and Rizzino, A. (2012) Systems biology provides new insights into the molecular mechanisms that control the fate of embryonic stem cells. J. Cell. Physiol. 227, 27-34
34. Sikorski, T. W., Ficarro, S. B., Holik, J., Kim, T., Rando, O. J., Marto, J. A., and Buratowski, S. (2011) Sub1 and RPA associate with RNA polymerase II at different stages of transcription. Mol. Cell 44, 397-409
35. Fong, Y. W., Inouye, C., Yamaguchi, T., Cattoglio, C., Grubisic, I., and Tjian, R. (2011) A DNA repair complex functions as an Oct4/Sox2 coactivator in embryonic stem cells. Cell 147, 120-131
36. Bártová, E., Šustáčková, G., Stixová, L., Kozubek, S., Legartová, S., and Foltá nková, V. (2011) Recruitment of Oct4 protein to UV-damaged chromatin in embryonic stem cells. PLoS One 6, e27281
37. Seki, Y., Kurisaki, A., Watanabe-Susaki, K., Nakajima, Y., Nakanishi, M., Arai, Y., Shiota, K., Sugino, H., and Asashima, M. (2010) TIF1β regulates the pluripotency of embryonic stem cells in a phosphorylation-dependent manner. Proc. Natl. Acad. Sci. U.S.A. 107, 10926-10931
38. Moretto-Zita, M., Jin, H., Shen, Z., Zhao, T., Briggs, S. P., and Xu, Y. (2010) Phosphorylation stabilizes Nanog by promoting its interaction with Pin1. Proc. Natl. Acad. Sci. U.S.A. 107, 13312-13317
39. Van Hoof, D., Muñoz, J., Braam, S. R., Pinkse, M. W., Linding, R., Heck, A. J., Mummery, C. L., and Krijgsveld, J. (2009) Phosphorylation dynamics during early differentiation of human embryonic stem cells. Cell Stem Cell 5, 214-226
40. Murphy, C. L., and Polak, J. M. (2002) Differentiating embryonic stem cells. GAPDH, but neither HPRT nor β-tubulin, is suitable as an internal standard for measuring RNA levels. Tissue Eng. 8, 551-559 (Pubitemid 34857792)