Asian-Australasian Journal of Animal Sciences

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
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Characterization of Bovine NANOG5'-flanking Region during Differentiation of Mouse Embryonic Stem Cells

  • Jang, Hye-Jeong (Laboratory of Developmental Genetics, Department of Biomedical Sciences, Inha University School of Medicine) ;
  • Park, Hwan Hee (Laboratory of Developmental Genetics, Department of Biomedical Sciences, Inha University School of Medicine) ;
  • Tran, Thi Thuy Linh (Laboratory of Developmental Genetics, Department of Biomedical Sciences, Inha University School of Medicine) ;
  • Lee, Hak-Kyo (Department of Animal Biotechnology, Chonbuk National University) ;
  • Song, Ki-Duk (Department of Animal Biotechnology, Chonbuk National University) ;
  • Lee, Woon Kyu (Laboratory of Developmental Genetics, Department of Biomedical Sciences, Inha University School of Medicine)
  • Received : 2015.06.08
  • Accepted : 2015.08.12
  • Published : 2015.12.01
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Abstract

Embryonic stem cells (ESCs) have been used as a powerful tool for research including gene manipulated animal models and the study of developmental gene regulation. Among the critical regulatory factors that maintain the pluripotency and self-renewal of undifferentiated ESCs, NANOG plays a very important role. Nevertheless, because pluripotency maintaining factors and specific markers for livestock ESCs have not yet been probed, few studies of the NANOG gene from domestic animals including bovine have been reported. Therefore, we chose mouse ESCs in order to understand and compare NANOG expression between bovine, human, and mouse during ESCs differentiation. We cloned a 600 bp (-420/+181) bovine NANOG 5'-flanking region, and tagged it with humanized recombinant green fluorescent protein (hrGFP) as a tracing reporter. Very high GFP expression for bovine NANOG promoter was observed in the mouse ESC line. GFP expression was monitored upon ESC differentiation and was gradually reduced along with differentiation toward neurons and adipocyte cells. Activity of bovine NANOG (-420/+181) promoter was compared with already known mouse and human NANOG promoters in mouse ESC and they were likely to show a similar pattern of regulation. In conclusion, bovine NANOG 5-flanking region functions in mouse ES cells and has characteristics similar to those of mouse and human. These results suggest that bovine gene function studied in mouse ES cells should be evaluated and extrapolated for application to characterization of bovine ES cells.

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References

  1. Boyer, L. A., T. I. Lee, M. F. Cole, S. E. Johnstone, S. S. Levine, J. P. Zucker, M. G. Guenther, R. M. Kumar, H. L. Murray, R. G. Jenner, D. K. Gifford, D. A. Melton, R. Jaenisch, and R. A. Young. 2005. Core transcriptional regulatory circuitry in human embryonic stem. Cell 122:947-956. https://doi.org/10.1016/j.cell.2005.08.020
  2. Buehr, M., S. Meek, K. Blair, J. Yang, J. Ure, J. Silva, R. McLay, J. Hall, Q. L. Ying, and A. Smith. 2008. Capture of authentic embryonic stem cells from rat blastocysts. Cell 135:1287-1298. https://doi.org/10.1016/j.cell.2008.12.007
  3. Chambers, I., D. Colby, M. Robertson, J. Nichols, S. Lee, S. Tweedie, and A. Smith. 2003. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113:643-655. https://doi.org/10.1016/S0092-8674(03)00392-1
  4. Chickarmane, V., C. Troein, U. A. Nuber, H. M. Sauro, and C. Peterson. 2006. Transcriptional dynamics of the embryonic stem cell switch. PLoS Comput. Biol. 2:e123. https://doi.org/10.1371/journal.pcbi.0020123
  5. Doetschman, T., P. Williams, and N. Maeda. 1988. Establishment of hamster blastocyst-derived embryonic stem (ES) cells. Dev. Biol. 127:224-227. https://doi.org/10.1016/0012-1606(88)90204-7
  6. Gerrard, L., D. Zhao, A. J. Clark, and W. Cui. 2005. Stably transfected human embryonic stem cell clones express OCT4-specific green fluorescent protein and maintain self-renewal and pluripotency. Stem Cells 23:124-133. https://doi.org/10.1634/stemcells.2004-0102
  7. Gu, P., D. LeMenuet, A. C. K. Chung, M. Mancini, D. A. Wheeler, and A. J. Cooney. 2005. Orphan nuclear receptor GCNF is required for the repression of pluripotency genes during retinoic acid-induced embryonic stem cell differentiation. Mol. Cell. Biol. 25:8507-8019. https://doi.org/10.1128/MCB.25.19.8507-8519.2005
  8. Hatano, S.Y., M. Tada, H. Kimura, S. Yamaguchi, T. Kono, T. Nakano, H. Suemori, N. Nakatsuji, and T. Tada. 2005. Pluripotential competence of cells associated with Nanog activity. Mech. Dev. 122:67-79. https://doi.org/10.1016/j.mod.2004.08.008
  9. Hatoya, S., R. Torii, Y. Kondo, T. Okuno, K. Kobayashi, V. Wijewardana, N. Kawate, H. Tamada, T. Sawada, D. Kumagai, K. Sugiura, and T. Inaba. 2006. Isolation and characterization of embryonic stemlike cells from canine blastocysts. Mol. Reprod. Dev. 73:298-305. https://doi.org/10.1002/mrd.20392
  10. Hayes, B., S. R. Fagerlie, A. Ramakrishnan, S. Baran, M. Harkey, L. Graf, M. Bar, A. Bendoraite, M. Tewari, and B. Torok-Storb. 2008. Derivation, characterization, and in vitro differentiation of canine embryonic stem cells. Stem Cells 26:465-473. https://doi.org/10.1634/stemcells.2007-0640
  11. Huang, B., T. Li, L. Alonso-Gonzalez, R. Gorre, S. Keatley, A. Green, P. Tumer, P. K. Kallingappa, V. Verma, and B. Oback. 2011. A virus-free poly-promoter vector induces pluripotency in quiescent bovine cells under chemically defined conditions of dual kinase inhibition. PLoS ONE 6:e24501. https://doi.org/10.1371/journal.pone.0024501
  12. Hamazaki, T., M. Oka, S. Yamanaka, and N. Terada. 2004. Aggregation of embryonic stem cells induces Nanog repression and primitive endoderm differentiation. J. Cell. Sci. 117:5681-5686. https://doi.org/10.1242/jcs.01489
  13. Kim, M. J., A. Habiba, J. M. Doherty, J. C. Mills, R. W. Mercer, and J. E. Huettner. 2009. Regulation of mouse embryonic stem cell neural differentiation by retinoic acid. Dev. Biol. 328:456-471. https://doi.org/10.1016/j.ydbio.2009.02.001
  14. Keefer, C. L., H. Baldassarre, R. Keyston, B. Wang, B. Bhatia, A. S. Bilodeau, J. F. Zhou, M. Leduc, B. R. Downey, A. Lazaris, and C. N. Karatzas. 2001. Generation of dwarf goat (Capra hircus) clones following nuclear transfer with transfected and nontransfected fetal fibroblasts and in vitro-matured oocytes. Biol. Reprod. 64:849-856. https://doi.org/10.1095/biolreprod64.3.849
  15. Kuroda, T., M. Tada, H. Kubota, H. Kimura, S. Y. Hantano, H. Suemori, N. Nakatsuji, and T. Tada. 2005. Octamer and sox elements are required for transcriptional cis regulation of Nanog gene expression. Mol. Cell. Biol. 25:2475-2485. https://doi.org/10.1128/MCB.25.6.2475-2485.2005
  16. Li, P., C. Tong, R. Mehrian-Shai, L. Jia, N. Wu, Y. Yan, R. E. Maxson, E. N. Schulze, H. Song, C. L. Hsieh, M. F. Pera, and Q. L. Ying. 2008. Germline competent embryonic stem cells derived from rat blastocysts. Cell 135:1299-1310. https://doi.org/10.1016/j.cell.2008.12.006
  17. Liu, N., M. Lu, X. Tian, and Z. Han. 2007. Molecular mechanisms involved in self-renewal and pluripotency of embryonic stem cells. J. Cell Physiol. 211:279-286. https://doi.org/10.1002/jcp.20978
  18. Mitsui, K., Y. Tokuzawa, H. Itoh, K. Segawa, M. Murakami, K. Takahashi, M. Maruyama, M. Maeda, and S. Yamanaka. 2003. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113:631-642. https://doi.org/10.1016/S0092-8674(03)00393-3
  19. Pain, B., M.E. Clark, M. Shen, H. Nakazawa, M. Sakurai, J. Samarut, and R. J. Etches. 1996. Long-term in vitro culture and characterization of avian embryonic stem cells with multiple morphogenetic potentialities. Development 122:2339-2348.
  20. Okada, Y., T. Shimazaki, G. Sobue, and H. Okano. 2004. Retinoicacid- concentration-dependent acquisition of neural cell identity during in vitro differentiation of mouse embryonic stem cells. Dev. Biol. 275:124-142. https://doi.org/10.1016/j.ydbio.2004.07.038
  21. Okita, K. and S. Yamanaka. 2006. Intracellular signaling pathways regulating pluripotency of embryonic stem cells. Curr. Stem Cell Res. Ther. 1:103-111. https://doi.org/10.2174/157488806775269061
  22. Rohweddel, J., K. Guan, and A. M. Wobus. 1999. Induction of cellular differentiation by retinoic acid in vitro. Cells Tissues Organs 165:190-202. https://doi.org/10.1159/000016699
  23. Rodda, D. J., J. L. Chew, L. H. Lim, Y. H. Loh, B. Wang, H. H. Ng, and P. Robson. 2005. Transcriptional Regulation of Nanog by $OCT_4$ and $SOX_2$. J. Biol. Chem. 280:24731-24737. https://doi.org/10.1074/jbc.M502573200
  24. Suda, Y., M. Suzuki, Y. Ikawa, and S. Aizawa. 1987. Mouse embryonic stem cells exhibit indefinite proliferative potential. J. Cell. Physiol. 133:197-201. https://doi.org/10.1002/jcp.1041330127
  25. Sukoyan, M. A., S. Y. Vatolin, A. N. Golubitsa, A. I. Zhelezova, L. A. Semenova, and O. L. Serov. 1993. Embryonic stem cells derived from morulae, inner cell mass, and blastocysts of mink: Comparisons of their pluripotencies. Mol. Reprod. Dev. 36:148-158. https://doi.org/10.1002/mrd.1080360205
  26. Sumer, H., J. Liu, L. F. Malaver-Ortega, M. L. Lim, K. Khodadadi, and P. J. Verma. 2011. Nanog is a key factor for induction of pluripotency in bovine adult fibroblasts. J. Anim. Sci. 89:2708-2716. https://doi.org/10.2527/jas.2010-3666
  27. Thomson, J. A., J. Kalishman, T. G. Golos, M. Durning, C. P. Harris, R. A. Becker, and J. P. Heam. 1995. Isolation of a primate embryonic stem cell line. Proc. Natl. Acad. Sci. USA 92:7844-7848. https://doi.org/10.1073/pnas.92.17.7844
  28. Thomson, J. A., J. Itskovitz-Eldor, S. S. Shapiro, M. A.Waknitz, J. J. Swiergiel, V. S. Marshall, and J. M. Jones. 1998. Embryonic stem cell lines derived from human blastocysts. Science 282:1145-1147. https://doi.org/10.1126/science.282.5391.1145
  29. Vallier, L., S. Mendjan, S. Brown, Z. Chng, A. Teo, L. E. Smithers, M. W. Trotter, C. H. Cho, A. Martinez, P. Rugg-Gunn, G. Brons, and R. A. Pedersen. 2009. Activin/Nodal signaling maintains pluripotency by controlling Nanog expression. Development 136:1339-1349. https://doi.org/10.1242/dev.033951
  30. Wobus, A. M. and K. R. Boheler. 2005. Embryonic stem cells: Prospects for developmental biology and cell therapy. Physiol. Rev. 85:635-678. https://doi.org/10.1152/physrev.00054.2003