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Transcriptional Regulation

Regulation of the Human MSH6 Gene by the Sp1 Transcription Factor and Alteration of Promoter Activity and Expression by Polymorphisms

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Pages 7992-8007 | Received 27 Feb 2003, Accepted 05 Aug 2003, Published online: 27 Mar 2023

REFERENCES

  • Acharya, S., T. Wilson, S. Gradia, M. F. Kane, S. Guerrette, G. T. Marsischky, R. Kolodner, and R. Fishel. 1996. hMSH2 forms specific mispair-binding complexes with hMSH3 and hMSH6. Proc. Natl. Acad. Sci. USA 93: 13629–13634.
  • Akiyama, Y., H. Nagasaki, T. Nakajima, H. Sakai, T. Nomizu, and Y. Yuasa. 2001. Infrequent frameshift mutations in the simple repeat sequences of hMLH3 in hereditary nonpolyposis colorectal cancers. Jpn. J. Clin. Oncol. 31: 61–64.
  • Andrew, S. D., P. J. Delhanty, L. M. Mulligan, and B. G. Robinson. 2000. Sp1 and Sp3 transactivate the RET proto-oncogene promoter. Gene 256: 283–291.
  • Aslam, F., L. Palumbo, L. H. Augenlicht, and A. Velcich. 2001. The Sp family of transcription factors in the regulation of the human and mouse MUC2 gene promoters. Cancer Res. 61: 570–576.
  • Bearzatto, A., M. Szadkowski, P. Macpherson, J. Jiricny, and P. Karran. 2000. Epigenetic regulation of the MGMT and hMSH6 DNA repair genes in cells resistant to methylating agents. Cancer Res. 60: 3262–3270.
  • Berends, M. J., Y. Wu, R. H. Sijmons, R. G. Mensink, T. van der Sluis, J. M. Hordijk-Hos, E. G. de Vries, H. Hollema, A. Karrenbeld, C. H. Buys, A. G. van der Zee, R. M. Hofstra, and J. H. Kleibeuker. 2002. Molecular and clinical characteristics of MSH6 variants: an analysis of 25 index carriers of a germline variant. Am. J. Hum. Genet. 70: 26–37.
  • Bonizzi, G., J. Piette, S. Schoonbroodt, M. P. Merville, and V. Bours. 1999. Role of the protein kinase C lambda/iota isoform in nuclear factor-kappaB activation by interleukin-1beta or tumor necrosis factor-alpha: cell type specificities. Biochem. Pharmacol. 57: 713–720.
  • Bowers, J., T. Sokolsky, T. Quach, and E. Alani. 1999. A mutation in the MSH6 subunit of the Saccharomyces cerevisiae MSH2-MSH6 complex disrupts mismatch recognition. J. Biol. Chem. 274: 16115–16125.
  • Brandeis, M., D. Frank, I. Keshet, Z. Siegfried, M. Mendelsohn, A. Nemes, V. Temper, A. Razin, and H. Cedar. 1994. Sp1 elements protect a CpG island from de novo methylation. Nature 371: 435–438.
  • Briggs, M. R., J. T. Kadonaga, S. P. Bell, and R. Tjian. 1986. Purification and biochemical characterization of the promoter-specific transcription factor, Sp1. Science 234: 47–52.
  • Chadwick, R. B., J. E. Meek, T. W. Prior, P. Peltomaki, and A. de La Chapelle. 2000. Polymorphisms in a pseudogene highly homologous to PMS2. Hum. Mutat. 16: 530.
  • Clark, S. J., J. Harrison, and P. L. Molloy. 1997. Sp1 binding is inhibited by (m)Cp(m)CpG methylation. Gene 195: 67–71.
  • Courey, A. J., and R. Tjian. 1988. Analysis of Sp1 in vivo reveals multiple transcriptional domains, including a novel glutamine-rich activation motif. Cell 55: 887–898.
  • Cunningham, J. M., E. R. Christensen, D. J. Tester, C. Y. Kim, P. C. Roche, L. J. Burgart, and S. N. Thibodeau. 1998. Hypermethylation of the hMLH1 promoter in colon cancer with microsatellite instability. Cancer Res. 58: 3455–3460.
  • Das Gupta, R., and R. D. Kolodner. 2000. Novel dominant mutations in Saccharomyces cerevisiae MSH6. Nat. Genet. 24: 53–56.
  • Dennig, J., M. Beato, and G. Suske. 1996. An inhibitor domain in Sp3 regulates its glutamine-rich activation domains. EMBO J. 15: 5659–5667.
  • Dignam, J. D., R. M. Lebovitz, and R. G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11: 1475–1489.
  • Drummond, J. T., J. Genschel, E. Wolf, and P. Modrich. 1997. DHFR/MSH3 amplification in methotrexate-resistant cells alters the hMutSα/hMutSβ ratio and reduces the efficiency of base-base mismatch repair. Proc. Natl. Acad. Sci. USA 94: 10144–10149.
  • Drummond, J. T., G. M. Li, M. J. Longley, and P. Modrich. 1995. Isolation of an hMSH2-p160 heterodimer that restores DNA mismatch repair to tumor cells. Science 268: 1909–1912.
  • Dynan, W. S., and R. Tjian. 1985. Control of eukaryotic messenger RNA synthesis by sequence-specific DNA-binding proteins. Nature 316: 774–778.
  • Genschel, J., S. J. Littman, J. T. Drummond, and P. Modrich. 1998. Isolation of MutSβ from human cells and comparison of the mismatch repair specificities of MutSβ and MutSα. J. Biol. Chem. 273: 19895–19901.
  • Graff, J. R., J. G. Herman, S. Myohanen, S. B. Baylin, and P. M. Vertino. 1997. Mapping patterns of CpG island methylation in normal and neoplastic cells implicates both upstream and downstream regions in de novo methylation. J. Biol. Chem. 272: 22322–22329.
  • Hagen, G., S. Muller, M. Beato, and G. Suske. 1994. Sp1-mediated transcriptional activation is repressed by Sp3. EMBO J. 13: 3843–3851.
  • Harfe, B. D., and S. Jinks-Robertson. 2000. DNA mismatch repair and genetic instability. Annu. Rev. Genet. 34: 359–399.
  • Herman, J. G., A. Umar, K. Polyak, J. R. Graff, N. Ahuja, J. P. Issa, S. Markowitz, J. K. Willson, S. R. Hamilton, K. W. Kinzler, M. F. Kane, R. D. Kolodner, B. Vogelstein, T. A. Kunkel, and S. B. Baylin. 1998. Incidence and functional consequences of hMLH1 promoter hypermethylation in colorectal carcinoma. Proc. Natl. Acad. Sci. USA 95: 6870–6875.
  • Holler, M., G. Westin, J. Jiricny, and W. Schaffner. 1988. Sp1 transcription factor binds DNA and activates transcription even when the binding site is CpG methylated. Genes Dev. 2: 1127–1135.
  • Ito, E., Y. Yanagisawa, Y. Iwahashi, Y. Suzuki, H. Nagasaki, Y. Akiyama, S. Sugano, Y. Yuasa, and K. Maruyama. 1999. A core promoter and a frequent single-nucleotide polymorphism of the mismatch repair gene hMLH1. Biochem. Biophys. Res. Commun. 256: 488–494.
  • Iwahashi, Y., E. Ito, Y. Yanagisawa, Y. Akiyama, Y. Yuasa, T. Onodera, and K. Maruyama. 1998. Promoter analysis of the human mismatch repair gene hMSH2. Gene 213: 141–147.
  • Jagmohan-Changur, S., T. Poikonen, S. Vilkki, V. Launonen, F. Wikman, T. F. Orntoft, P. Moller, H. Vasen, C. Tops, R. D. Kolodner, J. P. Mecklin, H. Jarvinen, S. Bevan, R. S. Houlston, L. A. Aaltonen, R. Fodde, J. Wijnen, and A. Karhu. 2003. EXO1 variants occur commonly in normal population: evidence against a role in hereditary nonpolyposis colorectal cancer. Cancer Res. 63: 154–158.
  • Kadonaga, J. T., K. R. Carner, F. R. Masiarz, and R. Tjian. 1987. Isolation of cDNA encoding transcription factor Sp1 and functional analysis of the DNA binding domain. Cell 51: 1079–1090.
  • Kane, M. F., M. Loda, G. M. Gaida, J. Lipman, R. Mishra, H. Goldman, J. M. Jessup, and R. Kolodner. 1997. Methylation of the hMLH1 promoter correlates with lack of expression of hMLH1 in sporadic colon tumors and mismatch repair-defective human tumor cell lines. Cancer Res. 57: 808–811.
  • Knight, S. W., T. J. Vulliamy, B. Morgan, K. Devriendt, P. J. Mason, and I. Dokal. 2001. Identification of novel DKC1 mutations in patients with dyskeratosis congenita: implications for pathophysiology and diagnosis. Hum. Genet. 108: 299–303.
  • Kolodner, R. D., and G. T. Marsischky. 1999. Eukaryotic DNA mismatch repair. Curr. Opin. Genet. Dev. 9: 89–96.
  • Kolodner, R. D., J. D. Tytell, J. L. Schmeits, M. F. Kane, R. D. Gupta, J. Weger, S. Wahlberg, E. A. Fox, D. Peel, A. Ziogas, J. E. Garber, S. Syngal, H. Anton-Culver, and F. P. Li. 1999. Germ-line msh6 mutations in colorectal cancer families. Cancer Res. 59: 5068–5074.
  • Kwon, H. S., M. S. Kim, H. J. Edenberg, and M. W. Hur. 1999. Sp3 and Sp4 can repress transcription by competing with Sp1 for the core cis-elements on the human ADH5/FDH minimal promoter. J. Biol. Chem. 274: 20–28.
  • Lania, L., B. Majello, and P. De Luca. 1997. Transcriptional regulation by the Sp family proteins. Int. J. Biochem. Cell Biol. 29: 1313–1323.
  • LeVan, T. D., J. W. Bloom, T. J. Bailey, C. L. Karp, M. Halonen, F. D. Martinez, and D. Vercelli. 2001. A common single nucleotide polymorphism in the CD14 promoter decreases the affinity of Sp protein binding and enhances transcriptional activity. J. Immunol. 167: 5838–5844.
  • Lipkin, S. M., V. Wang, D. L. Stoler, G. R. Anderson, I. Kirsch, D. Hadley, H. T. Lynch, and F. S. Collins. 2001. Germline and somatic mutation analyses in the DNA mismatch repair gene MLH3: evidence for somatic mutation in colorectal cancers. Hum. Mutat. 17: 389–396.
  • Liu, T., H. Yan, S. Kuismanen, A. Percesepe, M. L. Bisgaard, M. Pedroni, P. Benatti, K. W. Kinzler, B. Vogelstein, M. Ponz de Leon, P. Peltomaki, and A. Lindblom. 2001. The role of hPMS1 and hPMS2 in predisposing to colorectal cancer. Cancer Res. 61: 7798–7802.
  • Macleod, D., J. Charlton, J. Mullins, and A. P. Bird. 1994. Sp1 sites in the mouse aprt gene promoter are required to prevent methylation of the CpG island. Genes Dev. 8: 2282–2292.
  • Marra, G., I. Iaccarino, T. Lettieri, G. Roscilli, P. Delmastro, and J. Jiricny. 1998. Mismatch repair deficiency associated with overexpression of the MSH3 gene. Proc. Natl. Acad. Sci. USA 95: 8568–8573.
  • Marsischky, G. T., N. Filosi, M. F. Kane, and R. Kolodner. 1996. Redundancy of Saccharomyces cerevisiae MSH3 and MSH6 in MSH2-dependent mismatch repair. Genes Dev. 10: 407–420.
  • Mastrangelo, I. A., A. J. Courey, J. S. Wall, S. P. Jackson, and P. V. Hough. 1991. DNA looping and Sp1 multimer links: a mechanism for transcriptional synergism and enhancement. Proc. Natl. Acad. Sci. USA 88: 5670–5674.
  • McKnight, S. L., and R. Kingsbury. 1982. Transcriptional control signals of a eukaryotic protein-coding gene. Science 217: 316–324.
  • Miyaki, M., M. Konishi, K. Tanaka, R. Kikuchi-Yanoshita, M. Muraoka, M. Yasuno, T. Igari, M. Koike, M. Chiba, and T. Mori. 1997. Germline mutation of MSH6 as the cause of hereditary nonpolyposis colorectal cancer. Nat. Genet. 17: 271–272.
  • Miyakura, Y., K. Sugano, F. Konishi, N. Fukayama, S. Igarashi, K. Kotake, T. Matsui, Y. Koyama, M. Maekawa, and H. Nagai. 2003. Methylation profile of the MLH1 promoter region and their relationship to colorectal carcinogenesis. Genes Chromosomes Cancer. 36: 17–25.
  • Miyakura, Y., K. Sugano, F. Konishi, A. Ichikawa, M. Maekawa, K. Shitoh, S. Igarashi, K. Kotake, Y. Koyama, and H. Nagai. 2001. Extensive methylation of hMLH1 promoter region predominates in proximal colon cancer with microsatellite instability. Gastroenterology 121: 1300–1309.
  • Nicolaides, N. C., K. W. Kinzler, and B. Vogelstein. 1995. Analysis of the 5′ region of PMS2 reveals heterogeneous transcripts and a novel overlapping gene. Genomics 29: 329–334.
  • Palombo, F., I. Iaccarino, E. Nakajima, M. Ikejima, T. Shimada, and J. Jiricny. 1996. hMutSβ, a heterodimer of hMSH2 and hMSH3, binds to insertion/deletion loops in DNA. Curr. Biol. 6: 1181–1184.
  • Pascal, E., and R. Tjian. 1991. Different activation domains of Sp1 govern formation of multimers and mediate transcriptional synergism. Genes Dev. 5: 1646–1656.
  • Pearson, W. R., and D. J. Lipman. 1988. Improved tools for biological sequence comparison. Proc. Natl. Acad. Sci. USA 85: 2444–2448.
  • Peltomaki, P., H. F. Vasen, et al. 1997. Mutations predisposing to hereditary nonpolyposis colorectal cancer: database and results of a collaborative study. Gastroenterology 113: 1146–1158.
  • Rajakumar, R. A., S. Thamotharan, R. K. Menon, and S. U. Devaskar. 1998. Sp1 and Sp3 regulate transcriptional activity of the facilitative glucose transporter isoform-3 gene in mammalian neuroblasts and trophoblasts. J. Biol. Chem. 273: 27474–27483.
  • Risinger, J. I., A. Umar, J. Boyd, A. Berchuck, T. A. Kunkel, and J. C. Barrett. 1996. Mutation of MSH3 in endometrial cancer and evidence for its functional role in heteroduplex repair. Nat. Genet. 14: 102–105.
  • Sakai, T., N. Ohtani, T. L. McGee, P. D. Robbins, and T. P. Dryja. 1991. Oncogenic germ-line mutations in Sp1 and ATF sites in the human retinoblastoma gene. Nature 353: 83–86.
  • Shin, K. H., J. H. Shin, J. H. Kim, and J. G. Park. 2002. Mutational analysis of promoters of mismatch repair genes hMSH2 and hMLH1 in hereditary nonpolyposis colorectal cancer and early onset colorectal cancer patients: identification of three novel germ-line mutations in promoter of the hMSH2 gene. Cancer Res. 62: 38–42.
  • Sia, E. A., R. J. Kokoska, M. Dominska, P. Greenwell, and T. D. Petes. 1997. Microsatellite instability in yeast: dependence on repeat unit size and DNA mismatch repair genes. Mol. Cell. Biol. 17: 2851–2858.
  • Suske, G. 1999. The Sp-family of transcription factors. Gene 238: 291–300.
  • Suske, G. 2000. Transient transfection of Schneider cells in the study of transcription factors. Methods Mol. Biol. 130: 175–187.
  • Szadkowski, M., and J. Jiricny. 2002. Identification and functional characterization of the promoter region of the human MSH6 gene. Genes Chromosomes Cancer 33: 36–46.
  • Umar, A., J. I. Risinger, W. E. Glaab, K. R. Tindall, J. C. Barrett, and T. A. Kunkel. 1998. Functional overlap in mismatch repair by human MSH3 and MSH6. Genetics 148: 1637–1646.
  • Urban, A., S. Neukirchen, and K. E. Jaeger. 1997. A rapid and efficient method for site-directed mutagenesis using one-step overlap extension PCR. Nucleic Acids Res. 25: 2227–2228.
  • Vaisman, A., M. Varchenko, A. Umar, T. A. Kunkel, J. I. Risinger, J. C. Barrett, T. C. Hamilton, and S. G. Chaney. 1998. The role of hMLH1, hMSH3, and hMSH6 defects in cisplatin and oxaliplatin resistance: correlation with replicative bypass of platinum-DNA adducts. Cancer Res. 58: 3579–3585.
  • Viel, A., E. Novella, M. Genuardi, E. Capozzi, M. Fornasarig, M. Pedroni, M. Santarosa, M. P. De Leon, L. Della Puppa, M. Anti, and M. Boiocchi. 1998. Lack of PMS2 gene-truncating mutations in patients with hereditary colorectal cancer. Int. J. Oncol. 13: 565–569.
  • Wagner, A., Y. Hendriks, E. J. Meijers-Heijboer, W. J. de Leeuw, H. Morreau, R. Hofstra, C. Tops, E. Bik, A. H. Brocker-Vriends, C. van Der Meer, D. Lindhout, H. F. Vasen, M. H. Breuning, C. J. Cornelisse, C. van Krimpen, M. F. Niermeijer, A. H. Zwinderman, J. Wijnen, and R. Fodde. 2001. Atypical HNPCC owing to MSH6 germline mutations: analysis of a large Dutch pedigree. J. Med. Genet. 38: 318–322.
  • Wang, Q., C. Lasset, F. Desseigne, J. C. Saurin, C. Maugard, C. Navarro, E. Ruano, L. Descos, V. Trillet-Lenoir, J. F. Bosset, and A. Puisieux. 1999. Prevalence of germline mutations of hMLH1, hMSH2, hPMS1, hPMS2, and hMSH6 genes in 75 French kindreds with nonpolyposis colorectal cancer. Hum. Genet. 105: 79–85.
  • Wijnen, J., W. de Leeuw, H. Vasen, H. van der Klift, P. Moller, A. Stormorken, H. Meijers-Heijboer, D. Lindhout, F. Menko, S. Vossen, G. Moslein, C. Tops, A. Brocker-Vriends, Y. Wu, R. Hofstra, R. Sijmons, C. Cornelisse, H. Morreau, and R. Fodde. 1999. Familial endometrial cancer in female carriers of MSH6 germline mutations. Nat. Genet. 23: 142–144.
  • Wu, Y., M. J. Berends, R. G. Mensink, C. Kempinga, R. H. Sijmons, A. G. van Der Zee, H. Hollema, J. H. Kleibeuker, C. H. Buys, and R. M. Hofstra. 1999. Association of hereditary nonpolyposis colorectal cancer-related tumors displaying low microsatellite instability with MSH6 germline mutations. Am. J. Hum. Genet. 65: 1291–1298.
  • Wu, Y., M. J. Berends, J. G. Post, R. G. Mensink, E. Verlind, T. Van Der Sluis, C. Kempinga, R. H. Sijmons, A. G. van der Zee, H. Hollema, J. H. Kleibeuker, C. H. Buys, and R. M. Hofstra. 2001. Germline mutations of EXO1 gene in patients with hereditary nonpolyposis colorectal cancer (HNPCC) and atypical HNPCC forms. Gastroenterology 120: 1580–1587.
  • Wu, Y., M. J. Berends, R. H. Sijmons, R. G. Mensink, E. Verlind, K. A. Kooi, T. van der Sluis, C. Kempinga, A. G. van der Zee, H. Hollema, C. H. Buys, J. H. Kleibeuker, and R. M. Hofstra. 2001. A role for MLH3 in hereditary nonpolyposis colorectal cancer. Nat. Genet. 29: 137–138.
  • Yanagisawa, Y., E. Ito, Y. Iwahashi, Y. Akiyama, Y. Yuasa, and K. Maruyama. 1998. Isolation and characterization of the 5′ region of the human mismatch repair gene hPMS1. Biochem. Biophys. Res. Commun. 243: 738–743.
  • Zaveri, N. T., C. J. Green, W. E. Polgar, N. Huynh, and L. Toll. 2002. Regulation of transcription of the human prepronociceptin gene by Sp1. Gene 290: 45–52.
  • Zhao, L., and L. S. Chang. 1997. The human POLD1 gene: identification of an upstream activator sequence, activation by Sp1 and Sp3, and cell cycle regulation. J. Biol. Chem. 272: 4869–4882.

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