Regulation of major vault protein expression by upstream stimulating factor 1 in SW620 human colon cancer cells

Ikeda,Ryuji; Nishizawa,Yukihiko; Tajitsu,Yusuke; Minami,Kentaro; Mataki,Hironori; Masuda,Shogo; Furukawa,Tatsuhiko; Akiyama,Shin-Ichi; Yamada,Katsushi; Takeda,Yasuo

doi:10.3892/or.2013.2818

Regulation of major vault protein expression by upstream stimulating factor 1 in SW620 human colon cancer cells

Authors:
- Ryuji Ikeda
- Yukihiko Nishizawa
- Yusuke Tajitsu
- Kentaro Minami
- Hironori Mataki
- Shogo Masuda
- Tatsuhiko Furukawa
- Shin-Ichi Akiyama
- Katsushi Yamada
- Yasuo Takeda
View Affiliations

Affiliations: Department of Clinical Pharmacy and Pharmacology, Graduate School of Medical and Dental Sciences, Kagoshima University, Kagoshima 890-8520, Japan, Department of Molecular Oncology, Graduate School of Medical and Dental Sciences, Kagoshima University, Kagoshima 890-8520, Japan, Department of Respiratory Medicine and Rheumatology, Institute of Health Biosciences, the University of Tokushima Graduate School, Tokushima 770-8503, Japan, Department of Clinical Pharmacology, Faculty of Pharmaceutical Sciences, Nagasaki International University, Nagasaki 859-3298, Japan
Published online on: October 25, 2013 https://doi.org/10.3892/or.2013.2818
Pages: 197-201

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Major vault protein (MVP) is the main constituent of the vault ribonucleoprotein particle and is identical to lung resistance-related protein (LRP). Although MVP is also expressed in several types of normal tissues, little is known about its physiological role. In the present study, we identified the crucial MVP promoter elements that regulate MVP expression. An examination of tissue expression profiles revealed that MVP was expressed in the heart, placenta, lung, liver, kidney and pancreas. Elements of the MVP promoter contain binding sites for transcription factors, STAT, p53, Sp1, E-box, GATA, MyoD and Y-box. By deletion analysis, a conserved proximal E-box binding site was demonstrated to be important for human MVP promoter transactivation. Introduction of siRNA against upstream stimulating factor (USF) 1, which is known to bind the E-box binding site, decreased the expression of MVP in SW620 and ACHN cells. Using a chromatin immunoprecipitation (ChIP) assay, USF1 bound the MVP promoter in SW620 cells. These findings suggest that USF1 binding to an E-box element may be critical for basal MVP promoter activation. The results of the present study are useful in understanding the molecular mechanisms regulating MVP gene expression, and may aid in elucidating the physiological functions of MVP.

View Figures

View References

1	Scheffer GL, Wijngaard PL, Flens MJ, Izquierdo MA, Slovak ML, Pinedo HM, Meijer CJ, Clevers HC and Scheper RJ: The drug resistance-related protein LRP is the human major vault protein. Nat Med. 1:578–582. 1995. View Article : Google Scholar : PubMed/NCBI
2	Scheper RJ, Broxterman HJ, Scheffer GL, Kaaijk P, Dalton WS, van Heijningen TH, van Kalken CK, Slovak ML, de Vries EG, van der Valk P, Meijer CJ and Pinedo HM: Overexpression of a M(r) 110,000 vesicular protein in non-P-glycoprotein-mediated multidrug resistance. Cancer Res. 53:1475–1479. 1993.PubMed/NCBI
3	Scheffer GL, Schroeijers AB, Izquierdo MA, Wiemer EA and Scheper RJ: Lung resistance-related protein/major vault protein and vaults in multidrug-resistant cancer. Curr Opin Oncol. 12:550–556. 2000. View Article : Google Scholar : PubMed/NCBI
4	Kitazono M, Sumizawa T, Takebayashi Y, Chen ZS, Furukawa T, Nagayama S, Tani A, Takao S, Aikou T and Akiyama S: Multidrug resistance and the lung resistance-related protein in human colon carcinoma SW-620 cells. J Natl Cancer Inst. 91:1647–1653. 1999. View Article : Google Scholar : PubMed/NCBI
5	Pohl G, Suchomel RW, Stranzl T, Depisch D, Stiglbauer W, Filipits M and Pirker R: Expression of the lung resistance protein in primary colorectal carcinomas. Anticancer Res. 21:201–204. 2001.PubMed/NCBI
6	Meijer GA, Schroeijers AB, Flens MJ, Meuwissen SG, van der Valk P, Baak JP and Scheper RJ: Increased expression of multidrug resistance related proteins Pgp, MRP1, and LRP/MVP occurs early in colorectal carcinogenesis. J Clin Pathol. 52:450–454. 1999. View Article : Google Scholar : PubMed/NCBI
7	Ikeda R, Iwashita K, Sumizawa T, Beppu S, Tabata S, Tajitsu Y, Shimamoto Y, Yoshida K, Furukawa T, Che XF, Yamaguchi T, Ushiyama M, Miyawaki A, Takeda Y, Yamamoto M, Zhao HY, Shibayama Y, Yamada K and Akiyama S: Hyperosmotic stress up-regulates the expression of major vault protein in SW620 human colon cancer cells. Exp Cell Res. 314:3017–3026. 2008. View Article : Google Scholar : PubMed/NCBI
8	Sugawara I, Akiyama S, Scheper RJ and Itoyama S: Lung resistance protein (LRP) expression in human normal tissues in comparison with that of MDR1 and MRP. Cancer Lett. 112:23–31. 1997. View Article : Google Scholar : PubMed/NCBI
9	Lange C, Walther W, Schwabe H and Stein U: Cloning and initial analysis of the human multidrug resistance-related MVP/LRP gene promoter. Biochem Biophys Res Commun. 278:125–133. 2000. View Article : Google Scholar : PubMed/NCBI
10	Asakuno K, Kohno K, Uchiumi T, Kubo T, Sato S, Isono M and Kuwano M: Involvement of a DNA binding protein, MDR-NF1/YB-1, in human MDR1 gene expression by actinomycin D. Biochem Biophys Res Commun. 199:1428–1435. 1994. View Article : Google Scholar : PubMed/NCBI
11	Ohga T, Uchiumi T, Makino Y, Koike K, Wada M, Kuwano M and Kohno K: Direct involvement of the Y-box binding protein YB-1 in genotoxic stress-induced activation of the human multidrug resistance 1 gene. J Biol Chem. 273:5997–6000. 1998. View Article : Google Scholar : PubMed/NCBI
12	Stein U, Jürchott K, Walther W, Bergmann S, Schla PM and Royer HD: Hyperthermia-induced nuclear translocation of transcription factor YB-1 leads to enhanced expression of multidrug resistance-related ABC transporters. J Biol Chem. 276:28562–28569. 2001. View Article : Google Scholar
13	Steiner E, Holzmann K, Pirker C, Elbling L, Micksche M, Sutterlüty H and Berger W: The major vault protein is responsive to and interferes with interferon-γ-mediated STAT1 signals. J Cell Sci. 119:459–469. 2006.
14	Steiner E, Holzmann K, Pirker C, Elbling L, Micksche M and Berger W: SP-transcription factors are involved in basal MVP promoter activity and its stimulation by HDAC inhibitors. Biochem Biophys Res Commun. 317:235–243. 2004. View Article : Google Scholar : PubMed/NCBI
15	Sawadogo M, Van Dyke MW, Gregor PD and Roeder RG: Multiple forms of the human gene-specific transcription factor USF. I Complete purification and identification of USF from HeLa cell nuclei. J Biol Chem. 263:11985–11993. 1988.
16	Sawadogo M: Multiple forms of the human gene-specific transcription factor USF. II DNA binding properties and transcriptional activity of the purified HeLa USF. J Biol Chem. 263:11994–12001. 1988.PubMed/NCBI
17	Gregor PD, Sawadogo M and Roeder RG: The adenovirus major late transcription factor USF is a member of the helix-loop-helix group of regulatory proteins and binds to DNA as a dimer. Genes Dev. 4:1730–1740. 1990. View Article : Google Scholar : PubMed/NCBI
18	Sirito M, Walker S, Lin Q, Kozlowski MT, Klein WH and Sawadogo M: Members of the USF family of helix-loop-helix proteins bind DNA as homo- as well as heterodimers. Gene Expr. 2:231–240. 1992.PubMed/NCBI
19	Miyamoto NG, Moncollin V, Wintzerith M, Hen R, Egly JM and Chambon P: Stimulation of in vitro transcription by the upstream element of the adenovirus-2 major late promoter involves a specific factor. Nucleic Acids Res. 12:8779–8799. 1984. View Article : Google Scholar : PubMed/NCBI
20	Yu YT and Manley JL: Generation and functional analyses for base substitution mutants of the adenovirus 2 major late promoter. Nucleic Acids Res. 12:9309–9321. 1984. View Article : Google Scholar : PubMed/NCBI
21	Sirito M, Lin Q, Maity T and Sawadogo M: Ubiquitous expression of the 43- and 44-kDa forms of transcription factor USF in mammalian cells. Nucleic Acids Res. 22:427–433. 1994. View Article : Google Scholar : PubMed/NCBI
22	Shimamoto Y, Sumizawa T, Haraguchi M, Gotanda T, Jueng HC, Furukawa T, Sakata R and Akiyama S: Direct activation of the human major vault protein gene by DNA-damaging agents. Oncol Rep. 15:645–652. 2006.PubMed/NCBI