Seong-Jin Kim, Ph.D.

kims@dce41.nci.nih.gov

Gene Regulation Group Members



BIOGRAPHY:
Dr. Kim is a Senior Investigator in the Laboratory of Cell Regulation and Carcinogenesis, National Cancer Institute. He obtained his Ph.D. in Applied Biochemistry at the University of Tsukuba, Japan, and he joined Michael Sporn's laboratory at the National Cancer Institute in 1987. Dr. Kim was tenured in 1994 and now heads the "Gene Regulation" Group. His current research interests include the molecular basis for altered expression of TGF-ßs and their receptors in multiple pathologies.

RESEARCH INTERESTS:
Molecular Mechanism of Loss of TGF-ß Signaling during Carcinogenesis:

The research objective of my group is to understand the molecular mechanisms responsible for resistance to TGF-ß growth inhibitory activity during carcinogenesis. Recent findings demonstrate that the TGF-ß receptor complex is a new addition to the family of human tumor suppressor genes and that inactivation of these receptors is important in multiple human malignancies. Because human cancer cells frequently demonstrate resistance to the normal growth inhibitory effects of TGF-ß, it has been proposed that the development of such TGF-ß resistance represents a significant step during carcinogenesis. We have demonstrated a strong correlation between the resistance to TGF-ß and gross structural abnormalities in the TGF-ß type II receptor (RII) gene in human gastric cancers. In addition, we have reported that mutation and transcriptional repression of the TGF-ß type II receptor correlated with the loss of responsiveness of tumor cell lines to TGF-ß.

(1) Transcriptional regulation of the TGF-ß RII gene. Several lines of evidence have suggested that the transcriptional repression of the TGF-ß RII gene may be important in modulating TGF-ß responsiveness. Our laboratory has cloned a novel transcription factor, ERT, that interacts with the purine rich sequences in the TGF-ß RII promoter region and regulates TGF-ß RII expression. Recent studies have implicated members of the ets family of transcription factors as pathogenic mechanisms for multiple malignancies. We previously have identified multiple Ets binding sites in the TGF-ß RII promoter, suggesting the functional importance of these sites in the transcriptional regulation of the RII gene. Ewing sarcoma (ES) specific chromosomal translocations fuse the EWS gene to a subset of the ets transcription factor family, the FLI1, ERG, or ETV1 gene. EWS-FLI1, EWS-EGR, and EWS-ETV1 are thought to act as aberrant transcription factors that bind DNA through their ETS DNA binding domains. We have shown that the EWS-Ets fusion proteins act as potent repressors of the TGF-ß type II receptor gene, and that introduction of normal TGF-ß RII into an ES cell line restores TGF-ß sensitivity and blocks tumorigenicity. These results indicate that the transcriptional repression of TGF-ß RII is a major target of the EWS-Ets. We are currently investigating how EWS fusion proteins and various ets family of transcription factors regulate the expression of TGF-ß RII gene.

    Our overall research over the past years has suggested that a pharmacologic augmentation of TGF-ß signaling pathways in human cancers such as stomach and Ewing's sarcomas may be a potential therapeutic strategy. Recently, we have demonstrated that a histone deacetylase inhibitor suppresses the proliferation of human breast cancer cells and specifically enhances TGF-ß signaling by increasing the level of expression of TGF-ß type II receptor. We are currently investigating the molecular mechanisms of induction of TGF-ß RII by a histone deacetylase inhibitor.

(2) The molecular mechanism of resistance to TGF-ß signaling by viral oncoproteins. Many viral oncoproteins are known to modulate the TGF-ß signaling. However, mechanisms are not well characterized. Because Hepatitis B virus (HBV) is closely associated with acute and chronic hepatitis, cirrhosis, and hepatocellular carcinoma, we have explored the potential role of TGF-ß in the pathogenesis of fibrosis in chronic hepatitis and cirrhosis. We have discovered that the HBV encoded oncoprotein pX amplifies and augments TGF-ß signaling through a direct interaction with its signaling intermediate, Smad4. Since HTLV-1-infected T-cell lines become resistant to TGF-ß growth inhibitory activity, we are also investigating whether or not HTVL-1 encoded oncoprotein Tax alters TGF-ß signaling.

(3) Molecular mechanism of TGF-ß-induced apoptosis. Although TGF-ß is known to induce apoptosis in many cells, little information exists regarding the signaling pathways involved in apoptotic endpoints. In collaboration with Dr. Kyeong Sook Choi, Ajou University School of Medicine, Korea, we have recently demonstrated that Cdc2 and Cdk2 kinase activity transiently induced by TGF-ß1 phosphorylates retinoblastoma gene product (RB) as a physiological target in hepatoma cells and that this hyperphosphorylation of RB may trigger abrupt cell cycle progression, leading to irreversible cell death. We are currently investigating the underlying molecular mechanisms. In collaboration with Drs. Sarit Larich and Anita Roberts, we have identified a novel factor, ARTS, which is a mitochondrial septin-like protein derived from an alternative splicing of the H5 gene. Overexpression of ARTS in cells commits them to the TGF-ß-dependent apoptotic pathway. We are currently examining the role of the family of alternatively spliced variants of the human septin H5.

(4) Role of loss of TGF-ß responsiveness in gastrointestinal tract in vivo in transgenic mice. To study the role of the TGF-ß signaling pathway during carcinogenesis in vivo, transgenic mice expressing a dominant negative mutant form of the TGF-ß RII (dnRII) targeted to the colon using the ITF promoter, and to the stomach and pancreas using pS2 promoter have been generated. ITF-dnRII transgenic mice showed an increased susceptibility to inflammatory diseases. We are currently studying the role of the inactivation of the TGF-ß signaling during colorectal and gastric tumorigenesis using ITF-dnRII, pS2-dnRII, and TGF-ß type II receptor heterozygous.


Representative Publications:
  1. Lee, D. K., Park, S. H., Yi, Y., Choi, S.-G., Lee, C., Parks, W. T., Cho, H., de Caestecker, M. P., Shaul, Y., Roberts, A. B., and Kim, S.-J. The hepatitis B virus encoded oncoprotein pX amplifies TGF-ß family signaling through direct interaction with smad4: potential mechanism of HBV-induced liver fibrosis. Genes & Develop., in press, 2001.
  2. Lee, B. I., Park, S. H., Kim, J. W., Sausville, E. A., Kim, H. T., Nakanishi, O., Trepel, J. B., and Kim, S.-J.MS-275, an histone deacetylase inhibitor, selectively induces TGF-ß type II receptor expression in human breast cancer cells.Cancer Res., in press, 2001.
  3. Park, S. H., Kim, Y. S., Park, B.-K., Hargaad, S., and Kim, S.-J.Inactivation of a Sequence-Specific Enhancer Binding Protein Is Responsible for the Loss of Expression of ERT/ELF-3/ESX/ESE-1/jen in Human Gastric Cancer Cell Lines. Oncogene, in press, 2001.
  4. Larisch, S., Yi, Y., Lotan, R., Kerner, H., Eimerl, S., Parks, W. T., de Caestecker, M. P., Danielpour, D., Book-Melamed, N., Timberg, R., Lechleider, R. J., Orly, J., Kim, S.-J., and Roberts, A. B. A novel mitochondrial septin, ARTS, mediates TGF-ß-induced apoptosis via its P-loop motif. Nature Cell Biology, 2, 915-921, 2000.
  5. Kim, S.-J., Young-Hyuck Im, Markowitz, S. D., and Bang, Y.-J. Molecular Mechanisms of Inactivation of TGF-ß Receptors during Carcinogenesis.C ytokine & Growth Factor Rev. 11, 159-168, 2000.
  6. Hahm, K.-B., Im, Y.-H., Lee, C., Parks, W. T., Bang, Y.-J., Green, J., and Kim, S.-J. Loss of transforming growth factor-ß signaling as a pathogenic factor of pancreatitis through an autoimmune mechanism. J. Clin. Invest. 105, 1057-1065, 2000.
  7. Im, Y.-H., Kim, H.-T., Lee, C., Poulin, D., Welford, S., Sorensen, P. H. B., and Denny, C. T., and Kim, S.-J. EWS-FLI1, EWS-ERG, and EWS-ETV1 oncoproteins of Ewing tumor family all suppress transcription of TGF-ß type II receptor gene. Cancer Res. 60, 1536-1540, 2000.
  8. Hahm, K.-B., Cho, K., Lee, C., Im, Y.-H., Chang, J., Choi, S.-G., Sorensen, P. H., Thiele, C. J., and Kim, S.-J. The EWS-FLI1 oncogene of Ewing sarcoma represses TGF-ß type II receptor gene expression. Nature Genetics, 23, 222-227, 1999.
  9. Choi, K. S., Eom, Y. W., Kang, Y., Ha, M. J., Rhee, H., Yoon, J.-W., and Kim, S.-J.Cdc2 and cdk2 kinase activated by transforming growth factor ß1 triggers apoptosis through the phosphorylation of retinoblastoma protein in FaO hepatoma cells. J. Biol. Chem., 274, 31775-31783, 1999.
  10. Kang, S. H., Bang, Y.-J., Im, Y.-H., Yang, H. K., Lee, H. Y., Lee, H. S., Kim, N. K., and Kim, S.-J. Transcriptional repression of the transforming growth factor-ß type I receptor by DNA methylation results in the development of TGF-ß resistance in human gastric cancer. Oncogene, 18, 7280-7286, 1999.

Last revised on June 7th, 2002 by Sintha Huff

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