Surfactin suppresses TPA-induced breast cancer cell invasion through the inhibition of MMP-9 expression

Park,Sun  Young; Kim,Ji-Hee; Lee,Young Ji; Lee,Sang  Joon; Kim,Younghee

doi:10.3892/ijo.2012.1695

January 2013 Volume 42 Issue 1

Full Size Image

Cover Legend PDF

Journals

International Journal of Molecular Medicine

International Journal of Molecular Medicine is an international journal devoted to molecular mechanisms of human disease.

International Journal of Oncology

International Journal of Oncology is an international journal devoted to oncology research and cancer treatment.

Molecular Medicine Reports

Covers molecular medicine topics such as pharmacology, pathology, genetics, neuroscience, infectious diseases, molecular cardiology, and molecular surgery.

Oncology Reports

Oncology Reports is an international journal devoted to fundamental and applied research in Oncology.

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine is an international journal devoted to laboratory and clinical medicine.

Oncology Letters

Oncology Letters is an international journal devoted to Experimental and Clinical Oncology.

Biomedical Reports

Explores a wide range of biological and medical fields, including pharmacology, genetics, microbiology, neuroscience, and molecular cardiology.

Molecular and Clinical Oncology

International journal addressing all aspects of oncology research, from tumorigenesis and oncogenes to chemotherapy and metastasis.

World Academy of Sciences Journal

Multidisciplinary open-access journal spanning biochemistry, genetics, neuroscience, environmental health, and synthetic biology.

International Journal of Functional Nutrition

Open-access journal combining biochemistry, pharmacology, immunology, and genetics to advance health through functional nutrition.

International Journal of Epigenetics

Publishes open-access research on using epigenetics to advance understanding and treatment of human disease.

Medicine International

An International Open Access Journal Devoted to General Medicine.

January 2013 Volume 42 Issue 1

Full Size Image

Cover Legend PDF

Article

Surfactin suppresses TPA-induced breast cancer cell invasion through the inhibition of MMP-9 expression

Authors:
- Sun Young Park
- Ji-Hee Kim
- Young Ji Lee
- Sang Joon Lee
- Younghee Kim
View Affiliations / Copyright

Affiliations: Department of Molecular Biology, College of Natural Sciences, Pusan National University, Busan 609-735, Republic of Korea, Department of Microbiology, College of Natural Sciences, Pusan National University, Busan 609-735, Republic of Korea
Pages: 287-296
|
Published online on: November 13, 2012

https://doi.org/10.3892/ijo.2012.1695
Expand metrics +

Abstract

Metastasis is the main cause of cancer mortality. In this study, we investigated the effects of surfactin, a cyclic lipopeptide produced by Bacillus subtilis, on cancer metastasis in vitro and the underlying molecular mechanisms involved. Surfactin inhibited the 12-O-tetradecanoylphorbol-13-acetate (TPA)-induced invasion, migration and colony formation of human breast carcinoma cells. Western blot analysis, gelatin zymography and reverse transcription-PCR analysis revealed that matrix metalloproteinase-9 (MMP-9) expression and activation was significantly suppressed by surfactin in a dose-dependent manner. Surfactin attenuated TPA-induced nuclear translocation and activation of nuclear factor-κB (NF-κB) and activator protein-1 (AP-1). Furthermore, surfactin strongly repressed the TPA-induced phosphorylation of Akt and extracellular signal-regulated kinase (ERK). Treatment with specific inhibitors of Akt and ERK suppressed MMP-9 expression and activation. These results suggest that the surfactin-mediated inhibition of breast cancer cell invasion and MMP-9 expression involves the suppression of the NF-κB, AP-1, phosphatidylinositol 3-kinase (PI-3K)/Akt and the ERK signaling pathways. Thus surfactin may have potential value in therapeutic strategies for the treatment of breast cancer metastasis.

View Figures

View References

1.	Weigelt B, Peterse JL and van ’t Veer LJ: Breast cancer metastasis: Markers and models. Nat Rev Cancer. 5:591–602. 2005. View Article : Google Scholar : PubMed/NCBI
2.	Jemal A, Siegel R, Xu J and Ward E: Cancer statistics, 2010. CA Cancer J Clin. 60:277–300. 2010. View Article : Google Scholar
3.	Steeg PS: Tumor metastasis: Mechanistic insights and clinical challenges. Nat Med. 12:895–904. 2006. View Article : Google Scholar : PubMed/NCBI
4.	Hughes L, Malone C, Chumsri S, Burger AM and McDonnell S: Characterisation of breast cancer cell lines and establishment of a novel isogenic subclone to study migration, invasion and tumourigenicity. Clin Exp Metastasis. 25:549–557. 2008. View Article : Google Scholar : PubMed/NCBI
5.	Johnson LL, Dyer R and Hupe DJ: Matrix metalloproteinases. Curr Opin Chem Biol. 2:466–471. 1998. View Article : Google Scholar
6.	Stamenkovic I: Matrix metalloproteinases in tumor invasion and metastasis. Semin Cancer Biol. 10:415–433. 2000. View Article : Google Scholar : PubMed/NCBI
7.	Liotta LA, Steeg PS and Stetler-Stevenson WG: Cancer metastasis and angiogenesis: An imbalance of positive and negative regulation. Cell. 64:327–336. 1991. View Article : Google Scholar : PubMed/NCBI
8.	Brinckerhoff CE and Matrisian LM: Matrix metalloproteinases: A tail of a frog that became a prince. Nat Rev Mol Cell Biol. 3:207–214. 2002. View Article : Google Scholar : PubMed/NCBI
9.	Chakraborti S, Mandal M, Das S, Mandal A and Chakraborti T: Regulation of matrix metalloproteinases: An overview. Mol Cell Biochem. 253:269–285. 2003. View Article : Google Scholar : PubMed/NCBI
10.	Egeblad M and Werb Z: New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer. 2:161–174. 2002. View Article : Google Scholar : PubMed/NCBI
11.	Kajanne R, Miettinen P, Mehlem A, et al: EGF-R regulates MMP function in fibroblasts through MAPK and AP-1 pathways. J Cell Physiol. 212:489–497. 2007. View Article : Google Scholar : PubMed/NCBI
12.	Leber TM and Balkwill FR: Regulation of monocyte MMP-9 production by TNF-alpha and a tumour-derived soluble factor (MMPSF). Br J Cancer. 78:724–732. 1998. View Article : Google Scholar : PubMed/NCBI
13.	Singh P and Cameotra SS: Potential applications of microbial surfactants in biomedical sciences. Trends Biotechnol. 22:142–146. 2004. View Article : Google Scholar : PubMed/NCBI
14.	Cao X, Wang AH, Jiao RZ, Wang CL, Mao DZ, Yan L and Zeng B: Surfactin induces apoptosis and G(2)/M arrest in human breast cancer MCF-7 cells through cell cycle factor regulation. Cell Biochem Biophys. 55:163–171. 2009. View Article : Google Scholar : PubMed/NCBI
15.	Kim SY, Kim JY, Kim SH, et al: Surfactin from Bacillus subtilis displays anti-proliferative effect via apoptosis induction, cell cycle arrest and survival signaling suppression. FEBS Lett. 581:865–871. 2007.PubMed/NCBI
16.	Park SY and Kim Y: Surfactin inhibits immunostimulatory function of macrophages through blocking NK-kappaB, MAPK and Akt pathway. Int Immunopharmacol. 9:886–893. 2009. View Article : Google Scholar : PubMed/NCBI
17.	Park SY, Kim YH, Kim EK, Ryu EY and Lee SJ: Heme oxygenase-1 signals are involved in preferential inhibition of pro-inflammatory cytokine release by surfactin in cells activated with Porphyromonas gingivalis lipopolysaccharide. Chem Biol Interact. 188:437–445. 2010. View Article : Google Scholar : PubMed/NCBI
18.	Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(−delta delta C(T)) method. Methods. 25:402–408. 2001.
19.	Johnson KD and Bresnick EH: Dissecting long-range transcriptional mechanisms by chromatin immunoprecipitation. Methods. 26:27–36. 2002. View Article : Google Scholar : PubMed/NCBI
20.	Kim Y, Moon JS, Lee KS, et al: Ca²⁺/calmodulin-dependent protein phosphatase calcineurin mediates the expression of iNOS through IKK and NF-kappaB activity in LPS-stimulated mouse peritoneal macrophages and RAW 264.7 cells. Biochem Biophys Res Commun. 314:695–703. 2004.PubMed/NCBI
21.	Taylor CT and Colgan SP: Hypoxia and gastrointestinal disease. J Mol Med. 85:1295–1300. 2007. View Article : Google Scholar : PubMed/NCBI
22.	Bond M, Fabunmi RP, Baker AH and Newby AC: Synergistic upregulation of metalloproteinase-9 by growth factors and inflammatory cytokines: An absolute requirement for transcription factor NF-kappa B. FEBS Lett. 435:29–34. 1998. View Article : Google Scholar : PubMed/NCBI
23.	Eberhardt W, Huwiler A, Beck KF, Walpen S and Pfeilschifter J: Amplification of IL-1 beta-induced matrix metalloproteinase-9 expression by superoxide in rat glomerular mesangial cells is mediated by increased activities of NF-kappa B and activating protein-1 and involves activation of the mitogen-activated protein kinase pathways. J Immunol. 165:5788–5797. 2000.
24.	Lee YR, Noh EM, Oh HJ, et al: Dihydroavenanthramide D inhibits human breast cancer cell invasion through suppression of MMP-9 expression. Biochem Biophys Res Commun. 405:552–557. 2011. View Article : Google Scholar : PubMed/NCBI
25.	Esteve PO, Robledo O, Potworowski EF and St-Pierre Y: Induced expression of MMP-9 in C6 glioma cells is inhibited by PDGF via a PI 3-kinase-dependent pathway. Biochem Biophys Res Commun. 296:864–869. 2002. View Article : Google Scholar : PubMed/NCBI
26.	Reddy KB, Krueger JS, Kondapaka SB and Diglio CA: Mitogen-activated protein kinase (MAPK) regulates the expression of progelatinase B (MMP-9) in breast epithelial cells. Int J Cancer. 82:268–273. 1999. View Article : Google Scholar : PubMed/NCBI
27.	King TA, Ghazaleh RA, Juhn SK, Adams GL and Ondrey FG: Induction of heat shock protein 70 inhibits NF-kappa-B in squamous cell carcinoma. Otolaryngol Head Neck Surg. 133:70–79. 2005. View Article : Google Scholar : PubMed/NCBI
28.	Bylund J, Macdonald KL, Brown KL, Mydel P, Collins LV, Hancock RE and Speert DP: Enhanced inflammatory responses of chronic granulomatous disease leukocytes involve ROS-independent activation of NF-kappa B. Eur J Immunol. 37:1087–1096. 2007. View Article : Google Scholar : PubMed/NCBI
29.	Park B: Acute oral toxicity of surfactin C in mice. Toxicol Res. 22:453–458. 2006.
30.	Deryugina EI and Quigley JP: Matrix metalloproteinases and tumor metastasis. Cancer Metastasis Rev. 25:9–34. 2006. View Article : Google Scholar
31.	Woo JH, Park JW, Lee SH, et al: Dykellic acid inhibits phorbol myristate acetate-induced matrix metalloproteinase-9 expression by inhibiting nuclear factor kappa B transcriptional activity. Cancer Res. 63:3430–3434. 2003.
32.	Aggarwal BB, Kumar A and Bharti AC: Anticancer potential of curcumin: Preclinical and clinical studies. Anticancer Res. 23:363–398. 2003.PubMed/NCBI
33.	Cao XH, Wang AH, Wang CL, Mao DZ, Lu MF, Cui YQ and Jiao RZ: Surfactin induces apoptosis in human breast cancer MCF-7 cells through a ROS/JNK-mediated mitochondrial/caspase pathway. Chem Biol Interact. 183:357–362. 2010. View Article : Google Scholar : PubMed/NCBI
34.	Ahn YO: Diet and stomach cancer in Korea. Int J Cancer (Suppl). 10:7–9. 1997. View Article : Google Scholar
35.	Choi YH, Choi BT, Lee WH, Rhee SH and Park KY: Doenjang hexane fraction-induced G1 arrest is associated with the inhibition of pRB phosphorylation and induction of Cdk inhibitor p21 in human breast carcinoma MCF-7 cells. Oncol Rep. 8:1091–1096. 2001.PubMed/NCBI
36.	Jung KO, Park SY and Park KY: Longer aging time increases the anticancer and antimetastatic properties of doenjang. Nutrition. 22:539–545. 2006. View Article : Google Scholar : PubMed/NCBI
37.	Ohuchi Y, Myojin Y, Shimamoto F, Kashimoto N, Kamiya K and Watanabe H: Decrease in size of azoxymethane induced colon carcinoma in F344 rats by 180-day fermented miso. Oncol Rep. 14:1559–1564. 2005.PubMed/NCBI
38.	Seo HR, Kim JY, Kim JH and Park KY: Identification of Bacillus cereus in a chungkukjang that showed high anticancer effects against AGS human gastric adenocarcinoma cells. J Med Food. 12:1274–1280. 2009.
39.	Sonoda T, Nagata Y, Mori M, et al: A case-control study of diet and prostate cancer in Japan: possible protective effect of traditional Japanese diet. Cancer Sci. 95:238–242. 2004. View Article : Google Scholar : PubMed/NCBI

Journals

International Journal of Molecular Medicine

International Journal of Oncology

Molecular Medicine Reports

Oncology Reports

Experimental and Therapeutic Medicine

Oncology Letters

Biomedical Reports

Molecular and Clinical Oncology

World Academy of Sciences Journal

International Journal of Functional Nutrition

International Journal of Epigenetics

Medicine International

Surfactin suppresses TPA-induced breast cancer cell invasion through the inhibition of MMP-9 expression

This article is mentioned in:

Abstract

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Figure 6

Figure 7

Related Articles