Proteomic Analysis and the Antimetastatic Effect of N-(4methyl)phenyl-O-(4-methoxy) phenyl-thionocarbamate-Induced Apoptosis in Human Melanoma SK-MEL-28 cells

  • Choi Su-La (Clinical Biochemistry Lab, Department of Pharmacy, College of Pharmacy, Chungnam National University, Research Center for Transgenic Cloned Pigs, Chungnam National University) ;
  • Choi Yun-Sil (Clinical Biochemistry Lab, Department of Pharmacy, College of Pharmacy, Chungnam National University, Research Center for Transgenic Cloned Pigs, Chungnam National University) ;
  • Kim Young-Kwan (Clinical Biochemistry Lab, Department of Pharmacy, College of Pharmacy, Chungnam National University, Research Center for Transgenic Cloned Pigs, Chungnam National University) ;
  • Sung Nack-Do (Division of Applied Biology & Chemistry, College of Agriculture & Life Sciences, Chungnam National University, Research Center for Transgenic Cloned Pigs, Chungnam National University) ;
  • Kho Chang-Won (Division of Life Sciences, Korea Research Institute of Bioscience and Biotechnology, Research Center for Transgenic Cloned Pigs, Chungnam National University) ;
  • Park Byong-Chul (Division of Life Sciences, Korea Research Institute of Bioscience and Biotechnology) ;
  • Kim Eun-Mi (Division of Life Sciences, Korea Research Institute of Bioscience and Biotechnology) ;
  • Lee Jung-Hyung (Division of Life Sciences, Korea Research Institute of Bioscience and Biotechnology) ;
  • Kim Kyung-Mee (Angio Lab.) ;
  • Kim Min-Yung (Angio Lab.) ;
  • Myung Pyung-Keun (Clinical Biochemistry Lab, Department of Pharmacy, College of Pharmacy, Chungnam National University, Research Center for Transgenic Cloned Pigs, Chungnam National University)
  • Published : 2006.03.01

Abstract

We employed human SK-MEL-28 cells as a model system to identify cellular proteins that accompany N-(4-methyl)phenyl-O-(4-methoxy)phenyl-thionocarbamate (MMTC)-induced apoptosis based on a proteomic approach. Cell viability tests revealed that SK-MEL-28 skin cancer cells underwent more cell death than normal HaCaT cells in a dose-dependent manner after treatment with MMTC. Two-dimensional electrophoresis in conjunction with matrixassisted laser desorption/ionization-time of flight (MALDI-TOF) mass spectrometry analysis or computer matching with a protein database further revealed that the MMTC-induced apoptosis is accompanied by increased levels of caspase-1, checkpoint suppressor-1, caspase-4, NF-kB inhibitor, AP-2, c-Jun-N-terminal kinase, melanoma inhibitor, granzyme K, G1/S specific cyclin D3, cystein rich protein, Ras-related protein Rab-37 or Ras-related protein Rab-13, and reduced levels of EMS (oncogene), ATP synthase, tyrosine-phosphatase, Cdc25c, 14-3-3 protein or specific structure of nuclear receptor. The migration suppressing effect of MMTC on SK-MEL-28 cell was tested. MMTC suppressed the metastasis of SK-MEL-8 cells. It was also identified that MMTC had little angiogenic effect because it did not suppress the proliferation of HUVEC cell line. These results suggest that MMTC is a novel chemotherapeutic and metastatic agents against the SK-MEL-28 human melanoma cell line.

Keywords

References

  1. Ashkenazi, A., Death receptor: Signaling and modulation. Science, 281, 1322-1326 (1998) https://doi.org/10.1126/science.281.5381.1322
  2. Berke, G., The CTL's kiss of death. Cell, 81, 9-12 (1995) https://doi.org/10.1016/0092-8674(95)90365-8
  3. Berke, G., Unlocking the secrets of CTL and NK cells. Immunol. Today., 16, 343-346 (1995)
  4. Boldin, M. P., Goncharov, T. M., Goltsev, Y. V., and Wallach, D., Involvement of MACH, a novel MORT1/FADD interacting protease, in Fas/APO-1 and TNFReceptor-induced cell death. Cell, 85, 803-815 (1996) https://doi.org/10.1016/S0092-8674(00)81265-9
  5. Casano, F. J., Rolando, A. M., Mudgett, J. S., and Molineaux, S. M., The structure and complete nucleotide sequence of the murine gene encoding $interlekin-1{\beta}$ converting enzyme (ICE). Genomics, 20, 474-481 (1994) https://doi.org/10.1006/geno.1994.1203
  6. Cen, D., Gonzalez, R. I., Buckmeier, J. A., Kahlon, R. S., Tohidian, N. B., and Meyskens, F. L. Jr., Disulfiram induces apoptosis human melanoma cell via redox-related process, Mol. Cancer Ther., 1, 197-204 (2002)
  7. Chen, C. Y. and Faller, D. V., Direction of p21 ras-generated signals towards cell growth or apoptosis is determined by protein kinase C and Bcl-2. Oncogene, 11, 1487-1698 (1995)
  8. Chinnaiyan, A. M., O`Rourke, K., Tewari, M., and Dixit, V. M., FADD, a novel death domain-containing protein, interacts with the death domain of Das and initiates apoptosis. Cell, 81, 505-512 (1995) https://doi.org/10.1016/0092-8674(95)90071-3
  9. Elledge, S. J., Cell cycle checkpoints: Preventing an identity crisis. Science, 274, 1664-1667 (1996) https://doi.org/10.1126/science.274.5293.1664
  10. Estus, S., Zaks, W. J., Freeman, R. S., Gruda, M., Bravo, R., and Johnson, E. M., Altered gene expression in neurons during programmed cell death.: identification of c-JUN as necessary for neuronal apoptosis. J. cell Biol., 127, 1717-1727 (1994) https://doi.org/10.1083/jcb.127.6.1717
  11. Fidler, I. J., Schackert, G., Zhang, R. D., Radinsky, R., and Fujimaki, T., Cancer and Metastasis Reviews, 18, 387-400 (1999) https://doi.org/10.1023/A:1006329410433
  12. Folkman, J. and Shing, Y., Angiogenesis. J. Biol. Chem., 267, 10931-10934 (1992)
  13. Ham, J., Babij, C., Whitfield, J., Pfarrc, M., Lallemand, D., Yamiv, M., and Rubin, L., A c-Jun dominant negative mutant protects sympathetic neurons against programmed cell death. Neuron, 14, 927-939 (1995) https://doi.org/10.1016/0896-6273(95)90331-3
  14. Hanabuchi, S., Koyanagi, M., Yonehara, S., Yagita, H., and Okumura, K., Fas and its ligand in a general mechanism of Tcell mediated cytotoxicity. Proc. Natl. Acad. Sci., USA., 91, 4930-4934 (1994)
  15. Hanahan, D. and Weinberg, R. A., The hall-mark of cancer, Cell, 100, 57-70 ( 2000 ) https://doi.org/10.1016/S0092-8674(00)81683-9
  16. Henkart, P. A., Lymphocyte-mediated cytotoxicity : Two pathways and multiple effector. Immunity, 1, 343-346 (1994) https://doi.org/10.1016/1074-7613(94)90063-9
  17. Henkart, P. A., ICE-family proteases : Mediators of all apoptotic cell death? Immunity, 4, 195-201 (1996) https://doi.org/10.1016/S1074-7613(00)80428-8
  18. Hofmann, K., Bucher, P., and Tschopp, J., The CARD domain : a new apoptotic signaling motif. Trends Biochem. Sci., 22, 155-156 (1997) https://doi.org/10.1016/S0968-0004(97)01043-8
  19. Kamens, J., Paskind, M., Hugunin, M., Talanian, R. V., Allen, H., Banach, D., Bump, N., Hackett, M., Johnston, C. G., Li, P., Mankovich, J. A., Terranova, M., and Ghayur, T., Identification and characterization of ICH-2, a novel member of the interleukin-$1{\beta}$-converting enzyme family of cystein proteases. J. Biol. Chem., 270, 15250-15256 (1995) https://doi.org/10.1074/jbc.270.25.15250
  20. Kauffmann-Zeh, A., Rodriguez-Viciana, E., Ulrich, P., Gilbert, C., Coffer, P., Downward, J., and Evan, G., Suppression of c- Myc-induced apoptosis by Ras signaling through PI(3)K and PKB. Nature, 385, 544-548 (1997) https://doi.org/10.1038/385544a0
  21. Kaufmann, S. H., Desnoyers, S., Ottaviano, Y., Davidson, N. E., and Poirier, G. G., Specific proteolytic cleavage of poly (ADPribose) polymerase : an early marker of chemotherapyinduced apoptosis. Cancer Res., 53, 3976-3985 (1993)
  22. Liu, G. Y., Frank, N., Bartsch, H., and Lin, J. K., Induction of apoptosis by thiuramdisulfides, the reactive metabolites of dithiocarbamates, through coordinative modulation of NFkappa B, c-fos/c-jun, and p53 proteins. Mol. Carcinog., 22, 235-246 (1998) https://doi.org/10.1002/(SICI)1098-2744(199808)22:4<235::AID-MC5>3.0.CO;2-I
  23. Menashe, B. E., Role pf AP-2 in tumor growth and metastasis of human melanoma. Cancer and Metastasis Reviews, 18, 377-385 (1999) https://doi.org/10.1023/A:1006377309524
  24. Mesner, P. W., Epiting, C. L., Megarty, J. L., and Green, S. H., A time table of events during programmed cell death induced by trophic factor withdrawal from neuronal PC12 cells. J. Neurosci., 15, 7357-7366 (1995) https://doi.org/10.1523/JNEUROSCI.15-11-07357.1995
  25. Moellering, D., McAndrew, J., Jo, Ho., and Darley-Usmar, V. M., Effect of pyrolidine dithiocarbamate on endothelial cells: Protection against oxidative stress. Free Radical Biol. Med., 26, 1138-1145 (1999) https://doi.org/10.1016/S0891-5849(98)00300-1
  26. Morton, D. L. and Barth, A., Vaccine therapy for malignant melanoma. CA. Cancer J. Clin., 46, 225-244 (1996) https://doi.org/10.3322/canjclin.46.4.225
  27. Muzio, M., Chinnaiyan, A. M., Kischkel, F. C., O`Rourke, K., Shevchenko, A., Ni, J., Scaffidi, C., Bretz, J. D., Zhang, M., Gentz, R., Mann, M., Krammer, K. H., Peter, M. E., and Dixit, V. M., FLICE, a novel FADD-Homologous ICE/CED-3 like protease is recruited to the CD95 (Fas/APO-1) death inducing-signaling complex. Cell, 85, 817-827 (1996) https://doi.org/10.1016/S0092-8674(00)81266-0
  28. Qu, C. K., Role of the SHP-2-tyrosine phosphatase in cytokineinduced signaling and cellular response. Biochim. Biophys. Acta., 1592, 297-301 (2002) https://doi.org/10.1016/S0167-4889(02)00322-1
  29. Rodriguez-Vicente, J., Vicente-Ortega, V., and Canteras- Jordana, M., Effects of different antineoplastic agents and a pretreatment by modulators n three melanoma lines. Cancer, 82, 495-502 (1988) https://doi.org/10.1002/(SICI)1097-0142(19980201)82:3<495::AID-CNCR11>3.0.CO;2-X
  30. Rudolfo, M., Daniotti, M., and Vallacchi, V., Genetic progression of metastatic melanoma. Cancer Lett., 214, 133-147 ( 2004 ) https://doi.org/10.1016/j.canlet.2004.06.049
  31. Satyamoorthy, K., Meler, F., Ksu, M. Y., Berking, C., and Herhyn, M., Human xenografts, human skin and skin reconstructs for studies in melanoma development and progression. Cancer and Metastasis Reviews, 18, 401-405 (1995) https://doi.org/10.1023/A:1006333627271
  32. Schadendorf, D., Worm, M., Algermissen, B., Kohlmus, C. M., and Czarnetzki, B. M., Chemosensitivity testing of human malignant melanoma. A retrospective analysis of clinical reponse and in vitro drug sensitivity. Cancer, 73, 103-108 (1994) https://doi.org/10.1002/1097-0142(19940101)73:1<103::AID-CNCR2820730119>3.0.CO;2-K
  33. Shi, L., Kam, C. M., Powers, J. C., Aebersold, R., and Greenberg, A. H., Purification of three cytotoxic lymphocyte granule serine proteases that inducd apoptosis through distinct substrate and target cell interactions. J. Exp. Med., 176, 1521-1529 (1992) https://doi.org/10.1084/jem.176.6.1521
  34. Shi, L., Kraut, R. P., Aerersold, R., and Greenberg, A. H., A natural killer cell granule protein that induces DNA fragmentation and apoptosis. J. Exp. Med., 175, 553-566 (1992) https://doi.org/10.1084/jem.175.2.553
  35. Singh, A. K., Seth, P., Anthony, P., Husain, M. M., Madhavan, S., Mukhtar, H., and Maheshwari, R. K., Green tea constituent epigallocatechin-3-gallate inhibits angiogenic differentiation of human endothelial cells. Archives of Biochemistry and Biophysics, 401, 29-37 (2002) https://doi.org/10.1016/S0003-9861(02)00013-9
  36. Smyth, M. J. and Trapani, J. A., Granzymes: exogenous porteinases that induce target cell apoptosis. Immunol. Today, 16, 202-206 (1995) https://doi.org/10.1016/0167-5699(95)80122-7
  37. Suda, T., Takahashi, T., Golstein, P., and Nagata, S., Molecular cloning and expression of the Fas ligand, a novel member of the Tumor Necrosis Factor family. Cell, 75, 1169-1178 (1993) https://doi.org/10.1016/0092-8674(93)90326-L
  38. Sung, N. D., Myung, P. K., Seong, M. G., Yu, S. J., and Choi, S. L., QSAR anlyses on the cell cytotoxicity of some N-phenyl- O-phenylthionocarbamate derivatives using Comparative Molecular Field Analysis (CoMFA) based on different alignment approaches and Holographic Quantitative Structure- Activity Relationship (QSAR), Agri. Chem. Biotechnol., 46, 137-143 (2003)
  39. Sung, N. D. and Soung, M. K., Phenyl substituents effect on the fungicidal activity of N-phenyl-O-phenylthiono carbamate derivatives. Kor. J. Pestic. Sci., 3, 29-36 (1999)
  40. Takahashi, T., Tanaka, M., Brannan, C. I., Jenkins, N. A., Copeland, N. G., Suda, T., and Nagata, S., Generalized lymphoproliferative disease in mice, caused by a point mutation in the Fas ligand. Cell, 76, 969-976 (1994) https://doi.org/10.1016/0092-8674(94)90375-1
  41. Takakura, K., Sano, K., Hojo, S., and Hirano, A., Metastatic tumors of the central nervous system. Igaku- shoin Ltd. Tokyo, Japan, (1982)
  42. Tewari, M., Telford, W. G., Miller, R. A., and Dixit, V. M., Crm A, a poxvirus-encoded serpin, Inhibits cytotoxic T-lymphocytemediated apoptosis. J. Biol. Chem., 270, 22705-22708 (1995) https://doi.org/10.1074/jbc.270.39.22705
  43. Tom, J. and Dafna, B. S., Suppression of Ras-induced apoptosis by the RacGTPase. Mol. Cell Biol., 19, 5892-5901 (1999) https://doi.org/10.1128/MCB.19.9.5892
  44. Toru, T., Akio, S., and John, D. M., The prodomain of caspase-1 enhances Fas-mediated apoptosis through facilitation of caspase-8 activation. J. Biol. Chem., 275, 14248-14254 (2000) https://doi.org/10.1074/jbc.275.19.14248
  45. Trede, N. S., Tsytsykova, A. V., Chatila, T., Goldfeld, A. E., and Geha, R. S., Transcriptional activation of the human TNFalpha promoter by super antigen in human monocytic cells: role of NF-kappa B. J. Immunol., 155, 902-908 (1995)
  46. Wheeler, M. A., Townsend, M. K., Yunker, L. A., and Mauro, L. J., Transcriptional activation of the tyrosine phosphatase gene, OST-PTP during osteoblast differentiation. J. Cell. Biochem., 87, 363-376 (2002) https://doi.org/10.1002/jcb.10297
  47. Wu, H. and Lozano, G., NF-kappa B activation of p53. A potential mechanism for suppressing cell growth in response to stress. J. Biol. Chem., 269, 20067-20074 (1994)
  48. Xia, Z., Dickens, M., Rainge, J., Davis, R. J., and Greenberg, M. E., Opposing effects of ERK and JNK- p38 MAP kinases on apoptosis. Science, 270, 1326-1331 (1995) https://doi.org/10.1126/science.270.5240.1326