[go: up one dir, main page]
More Web Proxy on the site http://driver.im/ Skip to main content

Advertisement

Log in

In vitro evaluation of anticancer properties of exopolysaccharides from Lactobacillus acidophilus in colon cancer cell lines

  • Published:
In Vitro Cellular & Developmental Biology - Animal Aims and scope Submit manuscript

Abstract

The present work aims at studying the effect of exopolysaccharides (EPS) from Lactobacillus acidophilus on the colon cancer cell lines in vitro. Initial analysis showed that EPS has antioxidative properties. EPS was also found to induce cytotoxicity in two colon cancer cell lines, viz. HCT15 and CaCo2 under normoxia and hypoxia. The membrane integrity was also found to be affected in EPS-treated cells. Once the toxic concentration was determined (5 mg/ml), the effect of EPS on the messenger RNA (mRNA) expression of various genes was studied by quantitative real-time (RT)-PCR under both normoxic and hypoxic conditions. The results suggest that EPS downregulated the expression of vascular endothelial growth factor (VEGF) and hypoxia-inducible factor-1α (HIF-1α) and upregulated the expression of tissue inhibitor of metalloproteinases-3 (TIMP-3), hypoxia-inducible factor-2α (HIF-2α), and hemeoxygenase-1 (HO-1). An increase in plasminogen activator inhibitor-1 (PAI-1) was also observed. These results show that EPS may inhibit the expressions of genes involved in tumor angiogenesis and survival. Increase in the expression of HO-1 also shows that EPS have antioxidative properties.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
£29.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (United Kingdom)

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7
Figure 8

Similar content being viewed by others

References

  • Aachary AA, Gobinath D, Srinivasan K, Prapulla SG (2015) Protective effect of xylooligosaccharide from corncob on 1,2-dimethylhydrazine induced colon cancer in rats. Bioact Carbohydr Dietary Fibre 5:146–152

    Article  CAS  Google Scholar 

  • Alfadda AA, Sallam RM (2012) Reactive oxygen species in health and disease. J Biomed Biotechnol. doi:10.1155/2012/936486

    PubMed Central  PubMed  Google Scholar 

  • Anderson JW, Gilliland SE (1999) Effect of fermented milk (yogurt) containing Lactobacillus acidophilus L1 on serum cholesterol in hypercholesterolemic humans. J Am Coll Nutr 18:43–50

    Article  CAS  PubMed  Google Scholar 

  • Arora DS, Chandra P (2011) In vitro antioxidant potential of some soil fungi: screening of functional compounds and their purification from Penicillium citrinum. Appl Biochem Biotechnol 165(2):639–651

    Article  CAS  PubMed  Google Scholar 

  • Badel S, Bernardi T, Michaud P (2011) New perspectives for Lactobacilli exopolysaccharides. Biotechnol Adv 29(1):54–66

    Article  CAS  PubMed  Google Scholar 

  • Baker AH, George SJ, Zaltsman AB, Murphy G, Newby AC (1999) Inhibition of invasion and induction of apoptotic cell death of cancer cell lines by over expression of TIMP-3. Br J Cancer 79(9–10):1347–1355

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bansal S, Biswas G, Avadhani NG (2014) Mitochondria-targeted heme oxygenase-1 induces oxidative stress and mitochondrial dysfunction in macrophages, kidney fibroblasts and in chronic alcohol hepatotoxicity. Redox Biol 2:273–283

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Becker JC, Fukui H, Imai Y, Sekikawa A, Kimura T, Yamagishi H, Yoshitake N, Pohle T, Domschke W, Fujimori T (2007) Colonic expression of heme oxygenase-1 is associated with a better long-term survival in patients with colorectal cancer. Scand J Gastroenterol 42(7):852–858

    Article  CAS  PubMed  Google Scholar 

  • Bian J, Wang Y, Smith MR, Kim H, Jacobs C, Jackman J, Kung H, Colburn NH, Sun Y (1996) Suppression of in vivo tumor growth and induction of suspension cell death by tissue inhibitor of metalloproteinases (TIMP)-3. Carcinogenesis 17(9):1805–1811

    Article  CAS  PubMed  Google Scholar 

  • Bolte S, Talbot C, Boutte Y, Catrice O, Read ND, Satiat‐Jeunemaitre B (2004) FM‐dyes as experimental probes for dissecting vesicle trafficking in living plant cells. J Microsc 214(2):159–173

    Article  CAS  PubMed  Google Scholar 

  • Brahimi-Horn MC, Chiche J, Pouysségur J (2007) Hypoxia and cancer. J Mol Med 85(12):1301–1307

    Article  PubMed  Google Scholar 

  • Chan AT, Giovannucci EL (2010) Primary prevention of colorectal cancer. Gastroenterology 138(6):2029–2043

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Choi SS, Kim Y, Han KS, You S, Oh S, Kim SH (2006) Effects of Lactobacillus strains on cancer cell proliferation and oxidative stress in vitro. Lett App Microbiol 42(5):452–458

    Article  CAS  Google Scholar 

  • Clarke G, Ting KN, Wiart C, Fry J (2013) High correlation of 2, 2-diphenyl-1-picrylhydrazyl (DPPH) radical scavenging, ferric reducing activity potential and total phenolics content indicates redundancy in use of all three assays to screen for antioxidant activity of extracts of plants from the malaysian rainforest. Antioxidants 2(1):1–10

  • Contreras MF, Sougrat R, Zaher A, Ravasi T, Kosel J (2015) Non-chemotoxic induction of cancer cell death using magnetic nanowires. Int J Nanomed 10:2141–2153

    Article  CAS  Google Scholar 

  • Dang DT, Chen F, Gardner LB, Cummins JM, Rago C, Bunz F, Kantsevoy SV, Dang LH (2006) Hypoxia-inducible factor-1α promotes nonhypoxia-mediated proliferation in colon cancer cells and xenografts. Cancer Res 66(3):1684–1693

    Article  CAS  PubMed  Google Scholar 

  • Deepak V, Ramachandran S, Pandian SRK, Sivasubramaniam SD, Nellaiah H, Sundar K (2014) Exopolysaccharides from L. acidophilus for Colon Cancer Treatment. Proceedings of International conference on beneficial microbes- ICOBM2014, 116–119.

  • Deepak V, Pandian SRK, Sivasubramaniam SD, Nellaiah H, Sundar K (2015) Optimization of anticancer exopolysaccharide production from probiotic Lactobacillus acidophilus by response surface methodology. Prep Biochem Biotechnol. doi:10.1080/10826068.2015.1031386

    PubMed  Google Scholar 

  • Deraz S, Karlsson NE, Khalil AA, Mattiasson B (2007) Mode of action of acidocin D20079, a bacteriocin produced by the potential probiotic strain, Lactobacillus acidophilus DSM 20079. J Ind Microbiol Biotechnol 34:373–379

    Article  CAS  PubMed  Google Scholar 

  • Destouches D, Huet E, Sader M, Frechault S, Carpentier G, Ayoul F, Briand JP, Menashi S, Courty J (2012) Multivalent pseudopeptides targeting cell surface nucleoproteins inhibit cancer cell invasion through tissue inhibitor of metalloproteinases 3 (TIMP-3) release. J Biol Chem 287(52):43685–43693

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dkhissi F, Lu H, Soria C, Opolon P, Griscelli F, Liu H, Khattar P, Mishal Z, Perricaudet M, Li H (2003) Endostatin exhibits a direct antitumor effect in addition to its antiangiogenic activity in colon cancer cells. Hum Gene Ther 14(10):997–1008

    Article  CAS  PubMed  Google Scholar 

  • Ellis LM, Takahashi Y, Liu W, Shaheen RM (2000) Vascular endothelial growth factor in human colon cancer: biology and therapeutic implications. Oncologist 5(Suppl 1):11–15

    Article  CAS  PubMed  Google Scholar 

  • Ferrara N (2005) VEGF as a therapeutic target in cancer. Oncology 69(Suppl 3):11–16

    Article  CAS  PubMed  Google Scholar 

  • Ferrara N, Hillan KJ, Gerber HP, Novotny W (2004) Discovery and development of bevacizumab, an anti-VEGF antibody for treating cancer. Nat Rev Drug Disc 3(5):391–400

    Article  CAS  Google Scholar 

  • Folkman J (2006) Antiangiogenesis in cancer therapy-endostatin and its mechanisms of action. Exp Cell Res 312(5):594–607

    Article  CAS  PubMed  Google Scholar 

  • Gasparotto J, Somensi N, Kunzler A, Girardi CS, de Bittencourt Pasquali MA, Ramos VM, Simoes-Pires A, Quintans-Junior LJ, Branco A, Moreira JC, Gelain DP (2014) Hecogenin acetate inhibits reactive oxygen species production and induces cell cycle arrest and senescence in the A549 human lung cancer cell line. Anticancer Agents Med Chem 14(8):1128–1135

    Article  CAS  PubMed  Google Scholar 

  • Han PP, Sun Y, Wu XY, Yuan YJ, Dai YJ, Jia SR (2014) Emulsifying, flocculating, and physicochemical properties of exopolysaccharide produced by cyanobacterium Nostoc flagelliforme. Appl Biochem Biotechnol 172(1):36–49

    Article  CAS  PubMed  Google Scholar 

  • Holzapfel WH, Haberer P, Snel J, Schillinger U, Veld JH (1998) Overview of gut flora and probiotics. Int J Food Microbiol 41:85–101

    Article  CAS  PubMed  Google Scholar 

  • Hu W, Zhang C, Wu R, Sun Y, Levine A, Feng Z (2010) Glutaminase 2, a novel p53 target gene regulating energy metabolism and antioxidant function. Proc Natl Acad Sci 107(16):7455–7460

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Imamura T, Kikuchi H, Herraiz MT, Park DY, Mizukami Y, Mino‐Kenduson M, Lynch MP, Rueda BR, Benita Y, Xavier RJ, Chung DC (2009) HIF‐1α and HIF‐2α have divergent roles in colon cancer. Int J Cancer 124(4):763–771

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kallio JP, Hopkins‐Donaldson S, Baker AH, Kähäri VM (2011) TIMP‐3 promotes apoptosis in nonadherent small cell lung carcinoma cells lacking functional death receptor pathway. Int J Cancer 128(4):991–996

    Article  CAS  PubMed  Google Scholar 

  • Li L, Lin X, Staver M, Shoemaker A, Semizarov D, Fesik SW, Shen Y (2005) Evaluating hypoxia-inducible factor-1α as a cancer therapeutic target via inducible RNA interference in vivo. Cancer Res 65(16):7249–7258

    Article  CAS  PubMed  Google Scholar 

  • Li S, Zhao Y, Zhang L, Zhang X, Huang L, Li D, Li D, Niu C, Yang Z, Wang Q (2002) Antioxidant activity of Lactobacillus plantarum strains isolated from traditional Chinese fermented foods. Food Chem 135(3):1914–1919

  • Liu CF, Tseng KC, Chiang SS, Lee BH, Hsu WH, Pan TM (2011a) Immunomodulatory and antioxidant potential of Lactobacillus exopolysaccharides. J Sci Food Agric 91(12):2284–2291

    CAS  PubMed  Google Scholar 

  • Liu CT, Chu FJ, Chou CC, Yu RC (2011b) Antiproliferative and anticytotoxic effects of cell fractions and exopolysaccharides from Lactobacillus casei 01. Mutat Res Genet Toxicol Environ Mutagen 721(2):157–162

    Article  CAS  Google Scholar 

  • Liu B, Xu Y, Voss C, Qiu FH, Zhao MZ, Liu YD, Nie J, Wang ZL (2012) Altered protein expression in gestational diabetes mellitus placentas provides insight into insulin resistance and coagulation/fibrinolysis pathways. PLoS One 7(9), e44701

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mohandas KM, Desai DC (1999) Epidemiology of digestive tract cancers in India. V. Large and small bowel. Indian J Gastroenterol 18(3):118–121

    CAS  PubMed  Google Scholar 

  • Nielsen HJ, Pappot H, Christensen IJ, Brünner N, Thorlacius-Ussing O, Moesgaard F, Danø K, Grøndahl-Hansen J (1998) Association between plasma concentrations of plasminogen activator inhibitor-1 and survival in patients with colorectal cancer. BMJ 316(7134):829–830

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pachner M, Su K, Grant P (2014) High-frequency stimulus and high-K+ solution cause kiss-and-run fusion at the crayfish neuromuscular junction. Pioneering Neurosci J 14:69–72

    Google Scholar 

  • Pan D, Mei X (2010) Antioxidant activity of an exopolysaccharide purified from Lactococcus lactis subsp. lactis 12. Carbohyd Polym 80(3):908–914

  • Qi JH, Anand-Apte B (2015) Tissue inhibitor of metalloproteinase-3 (TIMP3) promotes endothelial apoptosis via a caspase-independent mechanism. Apoptosis 20(4):523–534

    Article  CAS  PubMed  Google Scholar 

  • Reid TM, Feig DI, Loeb LA (1994) Mutagenesis by metal-induced oxygen radicals. Environ Health Perspect 102(Suppl 3):57–61

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ryter SW, Tyrrell RM (2000) The heme synthesis and degradation pathways: role in oxidant sensitivity: heme oxygenase has both pro-and antioxidant properties. Free Radical Biol Med 28(2):289–309

    Article  CAS  Google Scholar 

  • Sakakibara T, Hibi K, Koike M, Fujiwara M, Kodera Y, Ito K, Nakao A (2005) Plasminogen activator inhibitor-1 as a potential marker for the malignancy of colorectal cancer. Br J Cancer 93(7):799–803

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Semenza GL (2010) HIF-1: upstream and downstream of cancer metabolism. Curr Opin Genet Dev 20(1):51–56

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Suzuki J, Nagata S (2014) Phospholipid scrambling on the plasma membrane. Methods Enzymol 544:381–393

    Article  CAS  PubMed  Google Scholar 

  • Tappel A (2007) Heme of consumed red meat can act as a catalyst of oxidative damage and could initiate colon, breast and prostate cancers, heart disease and other diseases. Med Hypotheses 68(3):562–564

    Article  CAS  PubMed  Google Scholar 

  • Thevenot P, Cho J, Wavhal, D, Timmons RB, Tang L (2008) Surface chemistry influences cancer killing effect of TiO2 nanoparticles. Nanomed Nanotechnol Biol Med 4(3):226–236

  • Trédan O, Galmarini CM, Patel K, Tannock IF (2007) Drug resistance and the solid tumor microenvironment. J Nat Cancer I 99(19):1441–1454

    Article  Google Scholar 

  • Ugun-Klusek A, Tamang A, Loughna P, Billett E, Buckley G, Sivasubramaniam S (2011) Reduced placental vascular reactivity to 5-hydroxytryptamine in pre-eclampsia and the status of 5HT2A receptors. Vasc Pharm 55(5):157–162

    Article  CAS  Google Scholar 

  • Valko M, Rhodes CJ, Moncol J, Izakovic MM, Mazur M (2006) Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem Biol Interact 160(1):1–40

    Article  CAS  PubMed  Google Scholar 

  • Wang K, Li W, Rui X, Chen X, Jiang M, Dong M (2014) Characterization of a novel exopolysaccharide with antitumor activity from Lactobacillus plantarum 70810. Int J Biol Macromol 63:133–139

    Article  CAS  PubMed  Google Scholar 

  • Wollowski I, Rechkemmer G, Pool-Zobel BL (2001) Protective role of probiotics and prebiotics in colon cancer. Am J Clin Nutr 73:451S–455S

    CAS  PubMed  Google Scholar 

  • Zhang L, Liu C, Li D, Zhao Y, Zhang X, Zeng X, Yang Z, Li S (2013) Antioxidant activity of an exopolysaccharide isolated from Lactobacillus plantarum C88. Int J Biol Macromol 54:270–275

  • Zong A, Cao H, Wang F (2012) Anticancer polysaccharides from natural resources: a review of recent research. Carbohyd Polym 90(4):1395–1410

    Article  CAS  Google Scholar 

Download references

Acknowledgment

One of the authors, DV, is grateful to CSIR, India, for a Senior Research Fellowship.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Krishnan Sundar.

Additional information

Editor: Tetsuji Okamoto

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Deepak, V., Ramachandran, S., Balahmar, R.M. et al. In vitro evaluation of anticancer properties of exopolysaccharides from Lactobacillus acidophilus in colon cancer cell lines. In Vitro Cell.Dev.Biol.-Animal 52, 163–173 (2016). https://doi.org/10.1007/s11626-015-9970-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11626-015-9970-3

Keywords

Navigation