Regulation of HSulf-1 expression by variant hepatic nuclear factor 1 in ovarian cancer

Cancer Res. 2009 Jun 1;69(11):4843-50. doi: 10.1158/0008-5472.CAN-08-3065.

Abstract

We recently identified HSulf-1 as a down-regulated gene in ovarian carcinomas. Our previous analysis indicated that HSulf-1 inactivation in ovarian cancers is partly mediated by loss of heterozygosity and epigenetic silencing. Here, we show that variant hepatic nuclear factor 1 (vHNF1), encoded by transcription factor 2 gene (TCF2, HNF1beta), negatively regulates HSulf-1 expression in ovarian cancer. Immunoblot assay revealed that vHNF1 is highly expressed in HSulf-1-deficient OV207, SKOV3, and TOV-21G cell lines but not in HSulf-1-expressing OSE, OV167, and OV202 cells. By short hairpin RNA-mediated down-regulation of vHNF1 in TOV-21G cells and transient enhanced vHNF1 expression in OV202 cells, we showed that vHNF1 suppresses HSulf-1 expression in ovarian cancer cell lines. Reporter assay and chromatin immunoprecipitation experiments showed that vHNF1 is specifically recruited to HSulf-1 promoter at two different vHNF1-responsive elements in OV207 and TOV-21G cells. Additionally, down-regulation of vHNF1 expression in OV207 and TOV-21G cells increased cisplatin- or paclitaxel-mediated cytotoxicity as determined by both 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide and clonogenic assays and this effect was reversed by down-regulation of HSulf-1. Moreover, nude mice bearing TOV-21G cell xenografts with stably down-regulated vHNF1 were more sensitive to cisplatin- or paclitaxel-induced cytotoxicity compared with xenografts of TOV-21G clonal lines with nontargeted control short hairpin RNA. Finally, immunohistochemical analysis of 501 ovarian tumors including 140 clear-cell tumors on tissue microarrays showed that vHNF1 inversely correlates to HSulf-1 expression. Collectively, these results indicate that vHNF1 acts as a repressor of HSulf-1 expression and might be a molecular target for ovarian cancer therapy.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Carcinoma / genetics*
  • Carcinoma / pathology
  • Cell Line, Tumor
  • Female
  • Gene Expression Profiling
  • Gene Expression Regulation, Neoplastic* / drug effects
  • Hepatocyte Nuclear Factor 1-beta / antagonists & inhibitors
  • Hepatocyte Nuclear Factor 1-beta / genetics
  • Hepatocyte Nuclear Factor 1-beta / metabolism
  • Hepatocyte Nuclear Factor 1-beta / physiology*
  • Humans
  • Mice
  • Mice, Nude
  • Oligonucleotide Array Sequence Analysis
  • Ovarian Neoplasms / genetics*
  • Ovarian Neoplasms / pathology
  • Protein Binding
  • RNA, Small Interfering / pharmacology
  • Response Elements
  • Sulfotransferases / genetics*
  • Sulfotransferases / physiology
  • Transfection
  • Xenograft Model Antitumor Assays

Substances

  • RNA, Small Interfering
  • Hepatocyte Nuclear Factor 1-beta
  • SULF1 protein, human
  • Sulfotransferases