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Mouse Melanoma Cell Migration is Dependent on Production of Reactive Oxygen Species under Normoxia Condition

  • Im, Yun-Sun (Department of Bioscience and Biotechnology, Sejong University) ;
  • Ryu, Yun-Kyoung (Department of Bioscience and Biotechnology, Sejong University) ;
  • Moon, Eun-Yi (Department of Bioscience and Biotechnology, Sejong University)
  • Received : 2012.01.03
  • Accepted : 2012.02.21
  • Published : 2012.03.31

Abstract

Cell migration plays a role in many physiological and pathological processes. Reactive oxygen species (ROS) produced in mammalian cells influence intracellular signaling processes which in turn regulate various biological activities. Here, we investigated whether melanoma cell migration could be controlled by ROS production under normoxia condition. Cell migration was measured by wound healing assay after scratching confluent monolayer of B16F10 mouse melanoma cells. Cell migration was enhanced over 12 h after scratching cells. In addition, we found that ROS production was increased by scratching cells. ERK phosphorylation was also increased by scratching cells but it was decreased by the treatment with ROS scavengers, N-acetylcysteine (NAC). Tumor cell migration was inhibited by the treatment with PD98059, ERK inhibitor, NAC or DPI, well-known ROS scavengers. Tumor cell growth as judged by succinate dehydrogenase activity was inhibited by NAC treatment. When mice were intraperitoneally administered with NAC, the intracellular ROS production was reduced in peripheral blood mononuclear cells. In addition, B16F10 tumor growth was significantly inhibited by in vivo treatment with NAC. Collectively, these findings suggest that tumor cell migration and growth could be controlled by ROS production and its downstream signaling pathways, in vitro and in vivo.

Acknowledgement

Supported by : Ministry of Health and Welfare, National Research Foundation of Korea (NRF)

References

  1. Aghajanian, A., Wittchen, E. S., Campbell, S. L. and Burridge, K. (2009) Direct activation of RhoA by reactive oxygen species requires a redox-sensitive motif. PLoS One 4, e8045. https://doi.org/10.1371/journal.pone.0008045
  2. Borisy, G. G. and Svitkina, T. M. (2000) Actin machinery: pushing the envelope. Curr. Opin. Cell Biol. 12, 104-112. https://doi.org/10.1016/S0955-0674(99)00063-0
  3. Cheng, G. C., Schulze, P. C., Lee, R. T., Sylvan, J., Zetter, B. R. and Huang, H. (2004) Oxidative stress and thioredoxin-interacting protein promote intravasation of melanoma cells. Exp. Cell Res. 300, 297-307. https://doi.org/10.1016/j.yexcr.2004.07.014
  4. Chetram, M. A., Don-Salu-Hewage, A. S. and Hinton, C. V. (2011) ROS enhances CXCR4-mediated functions through inactivation of PTEN in prostate cancer cells. Biochem. Biophys. Res. Commun. 410, 195-200. https://doi.org/10.1016/j.bbrc.2011.05.074
  5. Denizot, F. and Lang, R. (1986) Rapid colorimetric assay for cell growth and survival. Modifi cations to the tetrazolium dye procedure giving improved sensitivity and reliability. J. Immunol. Methods. 89, 271-277. https://doi.org/10.1016/0022-1759(86)90368-6
  6. Finkel, T. (2003) Oxidant signals and oxidative stress. Curr. Opin. Cell Biol. 15, 247-254. https://doi.org/10.1016/S0955-0674(03)00002-4
  7. Folkman, J. (1990) What is the evidence that tumors are angiogenesis dependent? J. Natl. Cancer Inst. 82, 4-6. https://doi.org/10.1093/jnci/82.1.4
  8. Han, Y. H., Kwon, J. H., Yu, D. Y. and Moon, E. Y. (2006) Inhibitory effect of peroxiredoxin II (Prx II) on Ras-ERK-NFkappaB pathway in mouse embryonic fi broblast (MEF) senescence. Free Radic. Res. 40, 1182-1189. https://doi.org/10.1080/10715760600868552
  9. Jiang, B. H., Liu, L. Z., Schafer, R., Flynn, D. C. and Barnett, J. B. (2006) A novel role for 3, 4-dichloropropionanilide (DCPA) in the inhibition of prostate cancer cell migration, proliferation, and hypoxiainducible factor 1alpha expression. BMC. Cancer 6, 204. https://doi.org/10.1186/1471-2407-6-204
  10. Kim, H. S. (2009) Reactive oxygen species-induced expression of B cell activating factor (BAFF) is independent of toll-like receptor 4 and myeloid differentiation primary response gene 88. Biomol. Ther. 17, 144-150. https://doi.org/10.4062/biomolther.2009.17.2.144
  11. Kim, J. S., Huang, T. Y. and Bokoch, G. M. (2009) Reactive oxygen species regulate a slingshot-cofi lin activation pathway. Mol. Biol. Cell. 20, 2650-2660. https://doi.org/10.1091/mbc.E09-02-0131
  12. Lauffenburger, D. A. and Horwitz, A. F. (1996) Cell migration: a physically integrated molecular process. Cell 84, 359-369. https://doi.org/10.1016/S0092-8674(00)81280-5
  13. Lee, J., Ishihara, A., Theriot, J. A. and Jacobson, K. (1993) Principles of locomotion for simple-shaped cells. Nature 362, 167-171. https://doi.org/10.1038/362167a0
  14. Lei, Y., Huang, K., Gao, C., Lau, Q. C., Pan, H., Xie, K., Li, J., Liu, R., Zhang, T., Xie, N., Nai, H. S., Wu, H., Dong, Q., Zhao, X., Nice, E. C., Huang, C. and Wei, Y. (2011) Proteomics identifi cation of ITGB3 as a key regulator in reactive oxygen species-induced migration and invasion of colorectal cancer cells. Mol. Cell Proteomics. 10, M110.005397.
  15. Lin, S., Sun, L., Hu, J., Wan, S., Zhao, R., Yuan, S. and Zhang, L. (2009) Chemokine C-X-C motif receptor 6 contributes to cell migration during hypoxia. Cancer Lett. 279, 108-117. https://doi.org/10.1016/j.canlet.2009.01.029
  16. Luanpitpongm, S., Talbottm, S. J., Rojanasakulm, Y., Nimmannitm, U., Pongrakhananonm, V., Wangm, L. and Chanvorachote, P. (2010) Regulation of lung cancer cell migration and invasion by reactive oxygen species and caveolin-1. J. Biol. Chem. 285, 38832-38840. https://doi.org/10.1074/jbc.M110.124958
  17. Luedde, T. (2010) MicroRNA-151 and its hosting gene FAK (focal adhesion kinase) regulate tumor cell migration and spreading of hepatocellular carcinoma. Hepatology 52, 1164-1166.
  18. Maulik, N. and Das, D. K. (2002) Redox signaling in vascular angiogenesis. Free Radic. Biol. Med. 33, 1047-1060. https://doi.org/10.1016/S0891-5849(02)01005-5
  19. Moon, E. Y. (2008) Serum deprivation enhances apoptoticcell death by increasing mitochondrial enzyme aActivity. Biomol. Ther. 16, 1-8. https://doi.org/10.4062/biomolther.2008.16.1.001
  20. Moon, E. Y., Han, Y. H., Lee, D. S., Han, Y. M. and Yu, D. Y. (2004) Reactive oxygen species induced by the deletion of peroxiredoxin II (PrxII) increases the number of thymocytes resulting in the enlargement of PrxII-null thymus. Eur. J. Immunol. 34, 2119-2128. https://doi.org/10.1002/eji.200424962
  21. Moon, E. Y., Im, Y. S., Ryu, Y. K. and Kang, J. H. (2010) Actin-sequestering protein, thymosin beta-4, is a novel hypoxia responsive regulator. Clin. Exp. Metastasis. 27, 601-609. https://doi.org/10.1007/s10585-010-9350-z
  22. Moon, E. Y., Lee, J. H., Lee, J. W., Song, J. H. and Pyo, S. (2011) ROS/Epac1-mediated Rap1/NF-kappaB activation is required for the expression of BAFF in Raw264.7 murine macrophages. Cell Signal 23, 1479-1488. https://doi.org/10.1016/j.cellsig.2011.05.001
  23. Oh, J. H., Ryu, Y. K., Lim, J. S. and Moon, E. Y. (2010) Hypoxia induces paclitaxel-resistance through ROS production. Biomolecules & Therapeutics. 18, 145-151. https://doi.org/10.4062/biomolther.2010.18.2.145
  24. Oh, J. M. and Moon, E. Y. (2010) Actin-sequestering protein, thymosin beta-4, induces paclitaxel resistance through ROS/HIF-1alpha stabilization in HeLa human cervical tumor cells. Life Sci. 87, 286-293. https://doi.org/10.1016/j.lfs.2010.07.002
  25. Park, S. Y., Jeong, K. J., Lee, J., Yoon, D. S., Choi, W. S., Kim, Y. K., Han, J. W., Kim, Y. M., Kim, B. K. and Lee, H. Y. (2007) Hypoxia enhances LPA-induced HIF-1alpha and VEGF expression: their inhibition by resveratrol. Cancer Lett. 258, 63-69. https://doi.org/10.1016/j.canlet.2007.08.011
  26. Rhee, S. G., Bae, Y. S., Lee, S. R. and Kwon, J. (2000) Hydrogen peroxide: a key messenger that modulates protein phosphorylation through cysteine oxidation. Sci. STKE. 2000, pe1.
  27. Ryu, Y. K., Im, Y. S. and Moon, E. Y. (2010) Cooperation of actin-sequestering protein, thymosin $\beta$-4 and hypoxia inducible factor-$1{\alpha}$ in tumor cell migration. Oncol. Rep. 24, 1389-1394.
  28. Shim, H., Shim, E., Lee, H., Hahn, J., Kang, D., Lee, Y. S. and Jeoung, D. (2006) CAGE, a novel cancer/testis antigen gene, promotes cell motility by activation ERK and p38 MAPK and downregulating ROS. Mol. Cells 21, 367-375.
  29. Singer, S. J. and Kupfer, A. (1986) The directed migration of eukaryotic cells. Annu. Rev. Cell Biol. 2, 337-365. https://doi.org/10.1146/annurev.cb.02.110186.002005
  30. Tobar, N., Guerrero, J., Smith, P. C. and Martínez, J. (2010) NOX4- dependent ROS production by stromal mammary cells modulates epithelial MCF-7 cell migration. Br. J. Cancer 103, 1040-1047. https://doi.org/10.1038/sj.bjc.6605847
  31. Tonomura, N., McLaughlin, K., Grimm, L., Goldsby, R. A. and Osborne, B. A. (2003) Glucocorticoid-induced apoptosis of thymocytes: requirement of proteasome-dependent mitochondrial activity. J. Immunol. 170, 2469-2478. https://doi.org/10.4049/jimmunol.170.5.2469
  32. Webb, D. J., Parsons, J. T. and Horwitz, A. F. (2002) Adhesion assembly, disassembly and turnover in migrating cells -- over and over and over again. Nat. Cell Biol. 4, E97-100. https://doi.org/10.1038/ncb0402-e97
  33. Welch, M. D., Iwamatsu, A. and Mitchison, T. J. (1997) Actin polymerization is induced by Arp2/3 protein complex at the surface of Listeria monocytogenes. Nature 385, 265-269. https://doi.org/10.1038/385265a0

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