Antiproliferative effects on colon adenocarcinoma cells induced by co-administration of vitamin K1 and Lactobacillus rhamnosus GG

Orlando,Antonella; Linsalata,Michele; Russo,Francesco

doi:10.3892/ijo.2016.3463

Antiproliferative effects on colon adenocarcinoma cells induced by co-administration of vitamin K1 and Lactobacillus rhamnosus GG

Authors:
- Antonella Orlando
- Michele Linsalata
- Francesco Russo
View Affiliations

Affiliations: Laboratory of Nutritional Pathophysiology, National Institute for Digestive Diseases I.R.C.C.S. ‘Saverio de Bellis’, Castellana Grotte, Ι-70013 Bari, Italy
Published online on: March 29, 2016 https://doi.org/10.3892/ijo.2016.3463
Pages: 2629-2638

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

Vitamin K (VK), an essential nutrient associated with the clotting cascade, has also been demonstrated to have anticancer properties in various cancer cells including colon cancer cells. Also probiotics have gained interest as potential anticancer agents. Among them, Lactobacillus rhamnosus GG (L.GG) has been shown to inhibit cell proliferation and polyamine biosynthesis as well as to induce apoptosis in different human gastrointestinal cancer cells. Nevertheless, the exact mechanisms involved in these actions are not completely elucidated. Therefore, the aims of the present study were to evaluate in three differently graded human colon cancer cells (namely Caco-2, HT-29 and SW480) the effects of increasing VK1 concentrations, administered alone or in combination with viable L.GG, on the cell proliferation evaluated by MTT test, apoptosis investigated by Bax/Bcl-2 ratio and the percentage of the apoptotic cells, and the cell cycle evaluated by MUSE cell analyzer. Both VK1 and L.GG administered alone up to 72 h, caused inhibition of proliferation, induction of apoptosis and the cell cycle arrest in all the tested colon cancer cells. When VK1 and L.GG were co-administered, the addition of increasing VK1 concentrations potentiated the probiotic antiproliferative effect in a dose-dependent manner, being also related to the individual features of each cell line. The effect was more evident in Caco-2 and HT-29 cells compared to the less differentiated SW480. The enhanced antiproliferative efficacy due to co-administration of L.GG and VK1 could represent a suitable option in a functional food strategy for cancer growth inhibition and chemoprevention.

View Figures

View References

1	Lepage C, Hamza S and Faivre J: Epidemiology and screening of colon cancer. Rev Prat. 60:1062–1067. 2010.(In French).
2	Johnson JJ and Mukhtar H: Curcumin for chemoprevention of colon cancer. Cancer Lett. 255:170–181. 2007. View Article : Google Scholar : PubMed/NCBI
3	Bazuro GE, Torino F, Gasparini G and Capurso L: Chemo-prevention in gastrointestinal adenocarcinoma: For few but not for all? Minerva Gastroenterol Dietol. 54:429–444. 2008.PubMed/NCBI
4	Linsalata M and Russo F: Nutritional factors and polyamine metabolism in colorectal cancer. Nutrition. 24:382–389. 2008. View Article : Google Scholar : PubMed/NCBI
5	Shearer MJ and Newman P: Metabolism and cell biology of vitamin K. Thromb Haemost. 100:530–547. 2008.PubMed/NCBI
6	Lamson DW and Plaza SM: The anticancer effects of vitamin K. Altern Med Rev. 8:303–318. 2003.PubMed/NCBI
7	Mizuta T and Ozaki I: Hepatocellular carcinoma and vitamin K. Vitam Horm. 78:435–442. 2008. View Article : Google Scholar : PubMed/NCBI
8	Ozaki I, Zhang H, Mizuta T, Ide Y, Eguchi Y, Yasutake T, Sakamaki T, Pestell RG and Yamamoto K: Menatetrenone, a vitamin K2 analogue, inhibits hepatocellular carcinoma cell growth by suppressing cyclin D1 expression through inhibition of nuclear factor kappaB activation. Clin Cancer Res. 13:2236–2245. 2007. View Article : Google Scholar : PubMed/NCBI
9	Du W, Zhou JR, Wang DL, Gong K and Zhang QJ: Vitamin K1 enhances sorafenib-induced growth inhibition and apoptosis of human malignant glioma cells by blocking the Raf/MEK/ERK pathway. World J Surg Oncol. 10:602012. View Article : Google Scholar : PubMed/NCBI
10	Orlando A, Linsalata M, Tutino V, D'Attoma B, Notarnicola M and Russo F: Vitamin K1 exerts antiproliferative effects and induces apoptosis in three differently graded human colon cancer cell lines. BioMed Res Int. 2015:2967212015. View Article : Google Scholar : PubMed/NCBI
11	Linsalata M, Orlando A, Tutino V, Notarnicola M, D'Attoma B and Russo F: Inhibitory effect of vitamin K1 on growth and polyamine biosynthesis of human gastric and colon carcinoma cell lines. Int J Oncol. 47:773–781. 2015.PubMed/NCBI
12	Thomas T and Thomas TJ: Polyamine metabolism and cancer. J Cell Mol Med. 7:113–126. 2003. View Article : Google Scholar : PubMed/NCBI
13	Aureli P, Capurso L, Castellazzi AM, Clerici M, Giovannini M, Morelli L, Poli A, Pregliasco F, Salvini F and Zuccotti GV: Probiotics and health: an evidence-based review. Pharmacol Res. 63:366–376. 2011. View Article : Google Scholar : PubMed/NCBI
14	Kumar M, Kumar A, Nagpal R, Mohania D, Behare P, Verma V, Kumar P, Poddar D, Aggarwal PK, Henry CJ, et al: Cancer-preventing attributes of probiotics: An update. Int J Food Sci Nutr. 61:473–496. 2010. View Article : Google Scholar : PubMed/NCBI
15	Linsalata M, Russo F, Berloco P, Valentini AM, Caruso ML, De Simone C, Barone M, Polimeno L and Di Leo A: Effects of probiotic bacteria (VSL#3) on the polyamine biosynthesis and cell proliferation of normal colonic mucosa of rats. In Vivo. 19:989–995. 2005.PubMed/NCBI
16	Uccello M, Malaguarnera G, Basile F, D'agata V, Malaguarnera M, Bertino G, Vacante M, Drago F and Biondi A: Potential role of probiotics on colorectal cancer prevention. BMC Surg. 12(Suppl 1): S352012. View Article : Google Scholar : PubMed/NCBI
17	You HJ, Oh DK and Ji GE: Anticancerogenic effect of a novel chiroinositol-containing polysaccharide from Bifidobacterium bifidum BGN4. FEMS Microbiol Lett. 240:131–136. 2004. View Article : Google Scholar : PubMed/NCBI
18	Orlando A, Messa C, Linsalata M, Cavallini A and Russo F: Effects of Lactobacillus rhamnosus GG on proliferation and polyamine metabolism in HGC-27 human gastric and DLD-1 colonic cancer cell lines. Immunopharmacol Immunotoxicol. 31:108–116. 2009. View Article : Google Scholar : PubMed/NCBI
19	Orlando A, Refolo MG, Messa C, Amati L, Lavermicocca P, Guerra V and Russo F: Antiproliferative and proapoptotic effects of viable or heat-killed Lactobacillus paracasei IMPC2.1 and Lactobacillus rhamnosus GG in HGC-27 gastric and DLD-1 colon cell lines. Nutr Cancer. 64:1103–1111. 2012. View Article : Google Scholar : PubMed/NCBI
20	Roberfroid M: Prebiotics: The concept revisited. J Nutr. 137(Suppl 2): 830S–837S. 2007.PubMed/NCBI
21	Gibson GR and Roberfroid MB: Dietary modulation of the human colonic microbiota: Introducing the concept of prebiotics. J Nutr. 125:1401–1412. 1995.PubMed/NCBI
22	Bomba A, Nemcová R, Gancarcíková S, Herich R, Guba P and Mudronová D: Improvement of the probiotic effect of micro-organisms by their combination with maltodextrins, fructo-oligosaccharides and polyunsaturated fatty acids. Br J Nutr. 88(Suppl 1): S95–S99. 2002. View Article : Google Scholar : PubMed/NCBI
23	Wyss C: Growth of Porphyromonas gingivalis, Treponema denticola, T. pectinovorum, T. socranskii, and T. vincentii in a chemically defined medium. J Clin Microbiol. 30:2225–2229. 1992.PubMed/NCBI
24	Bowler PG, Duerden BI and Armstrong DG: Wound microbiology and associated approaches to wound management. Clin Microbiol Rev. 14:244–269. 2001. View Article : Google Scholar : PubMed/NCBI
25	Hojo K, Nagaoka S, Murata S, Taketomo N, Ohshima T and Maeda N: Reduction of vitamin K concentration by salivary Bifidobacterium strains and their possible nutritional competition with Porphyromonas gingivalis. J Appl Microbiol. 103:1969–1974. 2007. View Article : Google Scholar : PubMed/NCBI
26	Brunner H, Hausmann F, Krieg RC, Endlicher E, Schölmerich J, Knuechel R and Messmann H: The effects of 5-aminolevulinic acid esters on protoporphyrin IX production in human adenocarcinoma cell lines. Photochem Photobiol. 74:721–725. 2001. View Article : Google Scholar : PubMed/NCBI
27	Linsalata M, Notarnicola M, Tutino V, Bifulco M, Santoro A, Laezza C, Messa C, Orlando A and Caruso MG: Effects of anandamide on polyamine levels and cell growth in human colon cancer cells. Anticancer Res. 30:2583–2589. 2010.PubMed/NCBI
28	Siegel RL, Miller KD and Jemal A: Cancer statistics, 2015. CA Cancer J Clin. 65:5–29. 2015. View Article : Google Scholar : PubMed/NCBI
29	Chan AT and Giovannucci EL: Primary prevention of colorectal cancer. Gastroenterology. 138:2029–2043.e2010. 2010. View Article : Google Scholar : PubMed/NCBI
30	Ligibel J: Lifestyle factors in cancer survivorship. J Clin Oncol. 30:3697–3704. 2012. View Article : Google Scholar : PubMed/NCBI
31	Reid G, Jass J, Sebulsky MT and McCormick JK: Potential uses of probiotics in clinical practice. Clin Microbiol Rev. 16:658–672. 2003. View Article : Google Scholar : PubMed/NCBI
32	Liong MT: Roles of probiotics and prebiotics in colon cancer prevention: Postulated mechanisms and in-vivo evidence. Int J Mol Sci. 9:854–863. 2008. View Article : Google Scholar
33	Lam EK, Tai EK, Koo MW, Wong HP, Wu WK, Yu L, So WH, Woo PC and Cho CH: Enhancement of gastric mucosal integrity by Lactobacillus rhamnosus GG. Life Sci. 80:2128–2136. 2007. View Article : Google Scholar : PubMed/NCBI
34	Drisko JA, Giles CK and Bischoff BJ: Probiotics in health maintenance and disease prevention. Altern Med Rev. 8:143–155. 2003.PubMed/NCBI
35	Yan F and Polk DB: Probiotic bacterium prevents cytokine-induced apoptosis in intestinal epithelial cells. J Biol Chem. 277:50959–50965. 2002. View Article : Google Scholar : PubMed/NCBI
36	Linsalata M, Cavallini A, Messa C, Orlando A, Refolo MG and Russo F: Lactobacillus rhamnosus GG influences polyamine metabolism in HGC-27 gastric cancer cell line: A strategy toward nutritional approach to chemoprevention of gastric cance. Curr Pharm Des. 16:847–853. 2010. View Article : Google Scholar : PubMed/NCBI
37	Showalter SL, Wang Z, Costantino CL, Witkiewicz AK, Yeo CJ, Brody JR and Carr BI: Naturally occurring K vitamins inhibit pancreatic cancer cell survival through a caspase-dependent pathway. J Gastroenterol Hepatol. 25:738–744. 2010. View Article : Google Scholar
38	Moreno-Vilet L, Garcia-Hernandez MH, Delgado-Portales RE, Corral-Fernandez NE, Cortez-Espinosa N, Ruiz-Cabrera MA and Portales-Perez DP: In vitro assessment of agave fructans (Agave salmiana) as prebiotics and immune system activators. Int J Biol Macromol. 63:181–187. 2014. View Article : Google Scholar
39	Tokita H, Tsuchida A, Miyazawa K, Ohyashiki K, Katayanagi S, Sudo H, Enomoto M, Takagi Y and Aoki T: Vitamin K2-induced antitumor effects via cell-cycle arrest and apoptosis in gastric cancer cell lines. Int J Mol Med. 17:235–243. 2006.PubMed/NCBI
40	Mouradov D, Sloggett C, Jorissen RN, Love CG, Li S, Burgess AW, Arango D, Strausberg RL, Buchanan D, Wormald S, et al: Colorectal cancer cell lines are representative models of the main molecular subtypes of primary cancer. Cancer Res. 74:3238–3247. 2014. View Article : Google Scholar : PubMed/NCBI
41	Flatmark K, Maelandsmo GM, Martinsen M, Rasmussen H and Fodstad Ø: Twelve colorectal cancer cell lines exhibit highly variable growth and metastatic capacities in an orthotopic model in nude mice. Eur J Cancer. 40:1593–1598. 2004. View Article : Google Scholar : PubMed/NCBI
42	Glick MC, Zilliken F and Gyorgy P: Supplementary growth promoting effect of 2-methyl-1,4 -naphthoquinone of Lactobacillus bifidus var. pennsylvanicus. J Bacteriol. 77:230–236. 1959.PubMed/NCBI
43	Alander M, Satokari R, Korpela R, Saxelin M, Vilpponen-Salmela T, Mattila-Sandholm T and von Wright A: Persistence of colonization of human colonic mucosa by a probiotic strain, Lactobacillus rhamnosus GG, after oral consumption. Appl Environ Microbiol. 65:351–354. 1999.PubMed/NCBI
44	Wei G, Wang M, Hyslop T, Wang Z and Carr BI: Vitamin K enhancement of sorafenib-mediated HCC cell growth inhibition in vitro and in vivo. Int J Cancer. 127:2949–2958. 2010. View Article : Google Scholar :