Biomolecules & Therapeutics

The Korean Society of Applied Pharmacology (한국응용약물학회)
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Role of TAZ in Lysophosphatidic Acid-Induced Migration and Proliferation of Human Adipose-Derived Mesenchymal Stem Cells

  • Mo, Won Min (Department of Physiology, Pusan National University School of Medicine) ;
  • Kwon, Yang Woo (Department of Physiology, Pusan National University School of Medicine) ;
  • Jang, Il Ho (Department of Oral Biochemistry and Molecular Biology, Pusan National University School of Dentistry) ;
  • Choi, Eun Jung (Department of Physiology, Pusan National University School of Medicine) ;
  • Kwon, Sang Mo (Department of Physiology, Pusan National University School of Medicine) ;
  • Kim, Jae Ho (Department of Physiology, Pusan National University School of Medicine)
  • Received : 2016.11.29
  • Accepted : 2017.02.28
  • Published : 2017.07.01
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Abstract

Transcriptional co-activator with a PDZ-binding motif (TAZ) is an important factor in lysophosphatidic acid (LPA)-induced promotion of migration and proliferation of human mesenchymal stem cells (MSCs). The expression of TAZ significantly increased at 6 h after LPA treatment, and TAZ knockdown inhibited the LPA-induced migration and proliferation of MSCs. In addition, embryonic fibroblasts from TAZ knockout mice exhibited the reduction in LPA-induced migration and proliferation. The LPA1 receptor inhibitor Ki16425 blocked LPA responses in MSCs. Although TAZ knockdown or knockout did not reduce LPA-induced phosphorylation of ERK and AKT, the MEK inhibitor U0126 or the ROCK inhibitor Y27632 blocked LPA-induced TAZ expression along with the reduction in the proliferation and migration of MSCs. Our data suggest that TAZ is an important mediator of LPA signaling in MSCs in the downstream of MEK and ROCK signaling.

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References

  1. Aggarwal, S. and Pittenger, M. F. (2005) Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 105, 1815-1822. https://doi.org/10.1182/blood-2004-04-1559
  2. Anliker, B. and Chun, J. (2004) Cell surface receptors in lysophospholipid signaling. Semin. Cell Dev. Biol. 15, 457-465. https://doi.org/10.1016/j.semcdb.2004.05.005
  3. Badri, L. and Lama, V. N. (2012) Lysophosphatidic acid induces migration of human lung-resident mesenchymal stem cells through the ${\beta}$-catenin pathway. Stem Cells 30, 2010-2019. https://doi.org/10.1002/stem.1171
  4. Binder, B. Y., Genetos, D. C. and Leach, J. K. (2014) Lysophosphatidic acid protects human mesenchymal stromal cells from differentiation-dependent vulnerability to apoptosis. Tissue Eng. Part A 20, 1156-1164. https://doi.org/10.1089/ten.tea.2013.0487
  5. Chan, S. W., Lim, C. J., Guo, K., Ng, C. P., Lee, I., Hunziker, W., Zeng, Q. and Hong, W. (2008) A role for TAZ in migration, invasion, and tumorigenesis of breast cancer cells. Cancer Res. 68, 2592-2598. https://doi.org/10.1158/0008-5472.CAN-07-2696
  6. Chen, J., Baydoun, A. R., Xu, R., Deng, L., Liu, X., Zhu, W., Shi, L., Cong, X., Hu, S. and Chen, X. (2008) Lysophosphatidic acid protects mesenchymal stem cells against hypoxia and serum deprivation-induced apoptosis. Stem Cells 26, 135-145. https://doi.org/10.1634/stemcells.2007-0098
  7. Chen, X., Yang, X. Y., Wang, N. D., Ding, C., Yang, Y. J., You, Z. J., Su, Q. and Chen, J. H. (2003) Serum lysophosphatidic acid concentrations measured by dot immunogold filtration assay in patients with acute myocardial infarction. Scand. J. Clin. Lab. Invest. 63, 497-503. https://doi.org/10.1080/00365510310003265
  8. Cordenonsi, M., Zanconato, F., Azzolin, L., Forcato, M., Rosato, A., Frasson, C., Inui, M., Montagner, M., Parenti, A. R., Poletti, A., Daidone, M. G., Dupont, S., Basso, G., Bicciato, S. and Piccolo, S. (2011) The Hippo transducer TAZ confers cancer stem cell-related traits on breast cancer cells. Cell 147, 759-772. https://doi.org/10.1016/j.cell.2011.09.048
  9. Cselenyak, A., Pankotai, E., Horvath, E. M., Kiss, L. and Lacza, Z. (2010) Mesenchymal stem cells rescue cardiomyoblasts from cell death in an in vitro ischemia model via direct cell-to-cell connections. BMC Cell Biol. 11, 29. https://doi.org/10.1186/1471-2121-11-29
  10. Frankel, A. and Mills, G. B. (1996) Peptide and lipid growth factors decrease cis-diamminedichloroplatinum-induced cell death in human ovarian cancer cells. Clin. Cancer Res. 2, 1307-1313.
  11. Geng, Y. J. (2003) Molecular mechanisms for cardiovascular stem cell apoptosis and growth in the hearts with atherosclerotic coronary disease and ischemic heart failure. Ann. N. Y. Acad. Sci. 1010, 687-697. https://doi.org/10.1196/annals.1299.126
  12. Halder, G. and Johnson, R. L. (2011) Hippo signaling: growth control and beyond. Development 138, 9-22. https://doi.org/10.1242/dev.045500
  13. Hao, Y., Chun, A., Cheung, K., Rashidi, B. and Yang, X. (2008) Tumor suppressor LATS1 is a negative regulator of oncogene YAP. J. Biol. Chem. 283, 5496-5509. https://doi.org/10.1074/jbc.M709037200
  14. Hong, W. and Guan, K. L. (2012) The YAP and TAZ transcription coactivators: key downstream effectors of the mammalian Hippo pathway. Semin. Cell Dev. Biol. 23, 785-793. https://doi.org/10.1016/j.semcdb.2012.05.004
  15. Hu, X., Haney, N., Kropp, D., Kabore, A. F., Johnston, J. B. and Gibson, S. B. (2005) Lysophosphatidic acid (LPA) protects primary chronic lymphocytic leukemia cells from apoptosis through LPA receptor activation of the anti-apoptotic protein AKT/PKB. J. Biol. Chem. 280, 9498-9508. https://doi.org/10.1074/jbc.M410455200
  16. Iyer, S. S. and Rojas, M. (2008) Anti-inflammatory effects of mesenchymal stem cells: novel concept for future therapies. Expert Opin. Biol. Ther. 8, 569-581. https://doi.org/10.1517/14712598.8.5.569
  17. Johnson, R. and Halder, G. (2014) The two faces of Hippo: targeting the Hippo pathway for regenerative medicine and cancer treatment. Nat. Rev. Drug Discov. 13, 63-79. https://doi.org/10.1038/nrd4161
  18. Li, N., Sarojini, H., An, J. and Wang, E. (2010a) Prosaposin in the secretome of marrow stroma-derived neural progenitor cells protects neural cells from apoptotic death. J. Neurochem. 112, 1527-1538. https://doi.org/10.1111/j.1471-4159.2009.06565.x
  19. Li, Z., Wei, H., Liu, X., Hu, S., Cong, X. and Chen, X. (2010b) LPA rescues ER stress-associated apoptosis in hypoxia and serum deprivation-stimulated mesenchymal stem cells. J. Cell. Biochem. 111, 811-820. https://doi.org/10.1002/jcb.22731
  20. Lindroos, B., Suuronen, R. and Miettinen, S. (2011) The potential of adipose stem cells in regenerative medicine. Stem Cell Rev. 7, 269-291. https://doi.org/10.1007/s12015-010-9193-7
  21. Liu, C. Y., Zha, Z. Y., Zhou, X., Zhang, H., Huang, W., Zhao, D., Li, T., Chan, S. W., Lim, C. J., Hong, W., Zhao, S., Xiong, Y., Lei, Q. Y. and Guan, K. L. (2010) The hippo tumor pathway promotes TAZ degradation by phosphorylating a phosphodegron and recruiting the SCF{beta}-TrCP E3 ligase. J. Biol. Chem. 285, 37159-37169. https://doi.org/10.1074/jbc.M110.152942
  22. Liu, X., Hou, J., Shi, L., Chen, J., Sang, J., Hu, S., Cong, X. and Chen, X. (2009) Lysophosphatidic acid protects mesenchymal stem cells against ischemia-induced apoptosis in vivo. Stem Cells Dev. 18, 947-954. https://doi.org/10.1089/scd.2008.0352
  23. Mangi, A. A., Noiseux, N., Kong, D., He, H., Rezvani, M., Ingwall, J. S. and Dzau, V. J. (2003) Mesenchymal stem cells modified with Akt prevent remodeling and restore performance of infarcted hearts. Nat. Med. 9, 1195-1201. https://doi.org/10.1038/nm912
  24. Murphy, M. B., Moncivais, K. and Caplan, A. I. (2013) Mesenchymal stem cells: environmentally responsive therapeutics for regenerative medicine. Exp. Mol. Med. 45, e54. https://doi.org/10.1038/emm.2013.94
  25. Ohta, H., Sato, K., Murata, N., Damirin, A., Malchinkhuu, E., Kon, J., Kimura, T., Tobo, M., Yamazaki, Y., Watanabe, T., Yagi, M., Sato, M., Suzuki, R., Murooka, H., Sakai, T., Nishitoba, T., Im, D. S., Nochi, H., Tamoto, K., Tomura, H. and Okajima, F. (2003) Ki16425, a subtype-selective antagonist for EDG-Family lysophosphatidic acid receptors. Mol. Pharmacol. 64, 994-1005. https://doi.org/10.1124/mol.64.4.994
  26. Orlic, D., Kajstura, J., Chimenti, S., Limana, F., Jakoniuk, I., Quaini, F., Nadal-Ginard, B., Bodine, D. M., Leri, A. and Anversa, P. (2001) Mobilized bone marrow cells repair the infarcted heart, improving function and survival. Proc. Natl. Acad. Sci. U.S.A. 98, 10344-10349. https://doi.org/10.1073/pnas.181177898
  27. Overholtzer, M., Zhang, J., Smolen, G. A., Muir, B., Li, W., Sgroi, D. C., Deng, C. X., Brugge, J. S. and Haber, D. A. (2006) Transforming properties of YAP, a candidate oncogene on the chromosome 11q22 amplicon. Proc. Natl. Acad. Sci. U.S.A. 103, 12405-12410. https://doi.org/10.1073/pnas.0605579103
  28. Pebay, A., Bonder, C. S. and Pitson, S. M. (2007) Stem cell regulation by lysophospholipids. Prostaglandins Other Lipid Mediat. 84, 83-97. https://doi.org/10.1016/j.prostaglandins.2007.08.004
  29. Ramos, A. and Camargo, F. D. (2012) The Hippo signaling pathway and stem cell biology. Trends Cell Biol. 22, 339-346. https://doi.org/10.1016/j.tcb.2012.04.006
  30. Tang, N., Zhao, Y., Feng, R., Liu, Y., Wang, S., Wei, W., Ding, Q., An, M. S., Wen, J. and Li, L. (2014) Lysophosphatidic acid accelerates lung fibrosis by inducing differentiation of mesenchymal stem cells into myofibroblasts. J. Cell. Mol. Med. 18, 156-169. https://doi.org/10.1111/jcmm.12178
  31. van Meeteren, L. A. and Moolenaar, W. H. (2007) Regulation and biological activities of the autotaxin-LPA axis. Prog. Lipid Res. 46, 145-160. https://doi.org/10.1016/j.plipres.2007.02.001
  32. Varelas, X. (2014) The Hippo pathway effectors TAZ and YAP in development, homeostasis and disease. Development 141, 1614-1626. https://doi.org/10.1242/dev.102376
  33. Willier, S., Butt, E. and Grunewald, T. G. (2013) Lysophosphatidic acid (LPA) signalling in cell migration and cancer invasion: a focussed review and analysis of LPA receptor gene expression on the basis of more than 1700 cancer microarrays. Biol. Cell 105, 317-333. https://doi.org/10.1111/boc.201300011
  34. Yu, F. X., Zhao, B., Panupinthu, N., Jewell, J. L., Lian, I., Wang, L. H., Zhao, J., Yuan, H., Tumaneng, K., Li, H., Fu, X. D., Mills, G. B. and Guan, K. L. (2012) Regulation of the Hippo-YAP pathway by Gprotein-coupled receptor signaling. Cell 150, 780-791. https://doi.org/10.1016/j.cell.2012.06.037

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