The relationship between the structural characteristics of lactobacilli-EPS and its ability to induce apoptosis in colon cancer cells in vitro

Scientific Reports

Volumn 9, Issue 1, 2019, Pages

  Tukenmez, Ummugulsum ^a   Aktas, Busra ^b   Aslim, Belma ^a   Yavuz, Serkan ^a  

^a GAZI UNIVERSITY   (Turkey)

^b MEHMET AKIF ERSOY UNIVERSITY   (Turkey)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL POLYSACCHARIDE; BCL2 PROTEIN, HUMAN; GLUCOSE; MANNOSE; MONOSACCHARIDE; N ACETYLGLUCOSAMINE; PROTEIN BCL 2; SURVIVIN;

APOPTOSIS; CELL PROLIFERATION; CHEMISTRY; COLON TUMOR; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HT-29 CELL LINE; HUMAN; LACTOBACILLUS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PATHOLOGY; ULTRASTRUCTURE;

ACETYLGLUCOSAMINE; APOPTOSIS; CELL PROLIFERATION; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; COLONIC NEOPLASMS; GENE EXPRESSION REGULATION, NEOPLASTIC; GLUCOSE; HT29 CELLS; HUMANS; LACTOBACILLUS; MAGNETIC RESONANCE SPECTROSCOPY; MANNOSE; MONOSACCHARIDES; POLYSACCHARIDES, BACTERIAL; PROTO-ONCOGENE PROTEINS C-BCL-2; SURVIVIN;

EID: 85066636796     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-019-44753-8     Document Type: Article

References (90)

1. The International Agency for Research on Cancer (IARC). Latest Global Cancer Data, 2018. World Health Organization (2018).
2. Bray, F. et al. Global Cancer Statistics 2018: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA Cancer J. Clin 68, 394–424 (2018).
3. Hill, C. et al. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat. Rev. Gastroenterol. Hepatol 11, 506–514 (2014).
4. Gueimonde, M., Ouwehand, A., Huhtinen, H., Salminen, E. & Salminen, S. Qualitative and quantitative analyses of the bifidobacterial microbiota in the colonic mucosa of patients with colorectal cancer, diverticulitis and inflammatory bowel disease. World J Gastroenterol 13, 3985–3989 (2007).
5. Kamada, N. & Núñez, G. Regulation of the immune system by the resident intestinal bacteria. Gastroenterology 146, 1477–88 (2014).
6. Ohno, H. Impact of commensal microbiota on the host pathophysiology: focusing on immunity and inflammation. Semin Immunopathol 37, 1–3 (2015).
7. Wang, Q. et al. Alteration of gut microbiota in association with cholesterol gallstone formation in mice. BMC Gastroenterol. 17, 1–9 (2017).
8. Pedamallu, C. S. et al. Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome Res. 22, 292–298 (2012).
9. Zackular, J. P. et al. The Gut Microbiome Modulates Colon Tumorigenesis. Am Soc Microbiol 4, e00692–13 (2013).
10. Schrezenmeir, J. & de Vrese, M. Probiotics, prebiotics, and synbiotics-approaching a definition. Am J Clin Nutr 73, 361S–364S (2001).
11. Leyer, G. J., Li, S., Mubasher, M. E., Reifer, C. & Ouwehand, A. C. Probiotic effects on cold and influenza-like symptom incidence and duration in children. Pediatrics 124, e172–e179 (2009).
12. Hörmannsperger, G. et al. Post-translational inhibition of IP-10 secretion in IEC by probiotic bacteria: impact on chronic inflammation. PLoS One 4, e4365 (2009).
13. Lebeer, S., Claes, I. J. J., Verhoeven, T. L. A., Vanderleyden, J. & De Keersmaecker, S. C. J. Exopolysaccharides of Lactobacillus rhamnosus GG form a protective shield against innate immune factors in the intestine. Microb. Biotechnol. 4, 368–374 (2011).
14. Kearney, N. et al. Handbook of fermented functional foods. (CRC Press, 2008).
15. Sungur, T., Aslim, B., Karaaslan, C. & Aktas, B. Impact of Exopolysaccharides (EPSs) of Lactobacillus gasseri strains isolated from human vagina on cervical tumor cells (HeLa). Anaerobe 47, 137–144 (2017).
16. Zakostelska, Z. et al. Lysate of probiotic Lactobacillus casei DN-114 001 ameliorates colitis by strengthening the gut barrier function and changing the gut microenvironment. PLoS One 6, e27961 (2011).
17. Liu, C.-T., Chu, F.-J., Chou, C.-C. & Yu, R.-C. Antiproliferative and anticytotoxic effects of cell fractions and exopolysaccharides from Lactobacillus casei 01. Mutat. Res. 721, 157–62 (2011).
18. Caggianiello, G., Kleerebezem, M. & Spano, G. Exopolysaccharides produced by lactic acid bacteria: from health-promoting benefits to stress tolerance mechanisms. Appl. Microbiol. Biotechnol. 100, 3877–3886 (2016).
19. Hong, J.-H. & Hee, K. J. Antioxidant and Antitumor Activities of β-glucan- rich Exopolysaccharides with Different Molecular Weight from Paenibacillus polymyxa JB115. J Korean Soc Appl Biol Chem 57, 105–112 (2014).
20. Ciszek-Lenda, M. et al. Strain specific immunostimulatory potential of lactobacilli-derived exopolysaccharides. Centr Eur J Immunol 36, 121–129 (2011).
21. Ruas-Madiedo, P., Hugenholtz, J. & Zoon, P. An overview of the functionality of exopolysaccharides produced by lactic acid bacteria. Int. Dairy J. 12, 163–171 (2002).
22. Mende, S., Rohm, H. & Jaros, D. Influence of exopolysaccharides on the structure, texture, stability and sensory properties of yoghurt and related products. Int. Dairy J. 52, 57–71 (2016).
23. Gorret, N., Maubois, J. L., Engasser, J. M. & Ghoul, M. Study of the effects of temperature, pH and yeast extract on growth and exopolysaccharides production by Propionibacterium acidi-propionici on milk microfiltrate using a response surface methodology. J. Appl. Microbiol. 788–796 (2001).
24. Rinker, K. D. & Kelly, R. M. Effect of carbon and nitrogen sources on growth dynamics and exopolysaccharide production for the hyperthermophilic archaeon Thermococcus litoralis and bacterium Thermotoga maritima. Biotechnol. Bioeng. 69, 537–547 (2000).
25. Li, C. et al. Microbiological, physicochemical and rheological properties of fermented soymilk produced with exopolysaccharide (EPS) producing lactic acid bacteria strains. LWT - Food Sci. Technol. 57, 477–485 (2014).
26. Zhang, L. et al. Antioxidant activity of an exopolysaccharide isolated from Lactobacillus plantarum C88. Int. J. Biol. Macromol. 54, 270–275 (2013).
27. Xu, R., Ye, H., Sun, Y., Tu, Y. & Zeng, X. Preparation, preliminary characterization, antioxidant, hepatoprotective and antitumor activities of polysaccharides from the flower of tea plant (Camellia sinensis). Food Chem. Toxicol. 50, 2473–2480 (2012).
28. Li, W. et al. Structural elucidation and antioxidant activities of exopolysaccharides from Lactobacillus helveticus MB2-1. Carbohydr. Polym. 102, 351–359 (2014).
29. Li, W. et al. Characterization of a novel polysaccharide with anti-colon cancer activity from Lactobacillus helveticus MB2-1. Carbohydr. Res. 411, 6–14 (2015).
30. Li, S. et al. Molecular Modification of Polysaccharides and Resulting Bioactivities. ComprehensiveReviewsinFoodScienceandFoodSafety 15, 237–250 (2016).
31. Badel, S., Bernardi, T. & Michaud, P. New perspectives for Lactobacilli exopolysaccharides. Biotechnol. Adv. 29, 54–66 (2010).
32. Ma, L. et al. Preparation, preliminary characterization and inhibitory effect on human colon cancer HT-29 cells of an acidic polysaccharide fraction from Stachys floridana Schuttl. ex Benth. Food Chem. Toxicol. 60, 269–276 (2013).
33. Wang, K. et al. Characterization of a novel exopolysaccharide with antitumor activity from Lactobacillus plantarum 70810. Int. J. Biol. Macromol. 63, 133–139 (2014).
34. Gürsoy, A., Durlu-Özkaya, F., Yıldız, F. & Aslım, B. Ekzopolisakkarit Üretimi Yüksek Yerli Streptococcus thermophilus (W22) ve Lactobacillus delbrueckii ssp. bulgaricus (B3). Kafkas Univ. Vet. Fak. Derg. 16, 81–86 (2009).
35. Yildiz, G. G., Öztürk, M. & Aslim, B. Identification of Lactobacillus strains from breast-fed infant and investigation of their cholesterol-reducing effects. World J. Microbiol. Biotechnol. 27, 2397–2406 (2011).
36. Frengova, G. I., Simova, E. D., Beshkova, D. M. & Simov, Z. I. Production and monomer composition of exopolysaccharides by yogurt starter cultures. Can. J. Microbiol. 46, 1123–1127 (2000).
37. Dubois, M., Gilles, K. A., Hamilton, J. K., Rebers, P. A. & Smith, F. Colorimetric Method for Determination of Sugars and Related Substances. Anal. Chem. 28, 350–356 (1956).
38. Tsuda, H., Hara, K. & Miyamoto, T. Binding of mutagens to exopolysaccharide produced by Lactobacillus plantarum mutant strain 301102S. J. Dairy Sci. 91, 2960–2966 (2008).
39. Ledezma, O. E. V. et al. Characterization of extracellular polymeric substances (EPS) produced by marine Micromonospora sp. J. Chem. Pharm. Res. 8, 442–451 (2016).
40. Boymirzaev, A. S., Shomurotov, S. & Turaev, A. S. Secondary Effects in Aqueous Size-Exclusion Chromatography of Polysaccharides. Chem. Plant Mater. 2, 51–55 (2013).
41. Ismail, B. & Madhavan Nampoothiri, K. Exposition of antitumour activity of a chemically characterized exopolysaccharide from a probiotic Lactobacillus plantarum MTCC 9510*. Biol. Sect. Cell. Mol. Biol. 68, 1041–1047 (2013).
42. Monsalve, D. M. et al. Human VRK2 modulates apoptosis by interaction with Bcl-xL and regulation of BAX gene expression. Cell Death Dis. 4, 1–10 (2013).
43. Moro, L. et al. Placental microparticles and MicroRNAs in pregnant women with Plasmodium falciparum or HIV infection. PLoS One 11, 1–17 (2016).
44. VanGuilder, H. D., Vrana, K. E. & Freeman, W. M. Twenty-five years of quantitative PCR for gene expression analysis. Biotechniques 44, 619–626 (2008).
45. Huang, F. et al. Sepia ink oligopeptide induces apoptosis in prostate cancer cell lines via caspase-3 activation and elevation of Bax/Bcl-2 ratio. Mar. Drugs 10, 2153–2165 (2012).
46. Ramadoss, D. P. & Sivalingam, N. Vanillin Extracted From Proso Millet and Barnyard Millet Induce Apoptosis in Ht-29 and Mcf-7 Cell Line Through Mitochondria Mediated Pathway. Asian J. Pharm. Clin. Res. 10, 226 (2017).
47. Harlow, E. D., Lane, D. A laboratory manual. (Cold Spring Harbor Laboratory, 1988).
48. Baselga, J. & Arteaga, C. L. Critical update and emerging trends in epidermal growth factor receptor targeting in cancer. J. Clin. Oncol. 23, 2445–2459 (2005).
49. Lebeer, S., Vanderleyden, J. & De Keersmaecker, S. C. J. Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens. Nat. Rev. Microbiol. 8, 171–84 (2010).
50. Burns, P. et al. Technological characterization and survival of the exopolysaccharide-producing strain Lactobacillus delbrueckii subsp. lactis 193 and its bile-resistant derivative 193 + in simulated gastric and intestinal juices. J. Dairy Res. 78, 357–364 (2011).
51. Mozzi, F. et al. Diversity of Heteropolysaccharide-Producing Lactic Acid Bacterium Strains and Their Biopolymers. Appl. Environ. Microbiol. 72, 4431–4435 (2006).
52. Donnarumma, G. et al. Lactobacillus crispatus L1: high cell density cultivation and exopolysaccharide structure characterization to highlight potentially beneficial effects against vaginal pathogens. BMC Microbiol. 14, 137 (2014).
53. Van Geel-Schutten, G. H., Flesch, F., Ten Brink, B., Smith, M. R. & Dijkhuizen, L. Screening and characterization of Lactobacillus strains producing large amounts of exopolysaccharides. Appl. Microbiol. Biotechnol. 50, 697–703 (1998).
54. Broadbent, J. R., McMahon, D. J., Welker, D. L., Oberg, C. J. & Moineau, S. Biochemistry, genetics, and applications of exopolysaccharide production in Streptococcus thermophilus: a review. J. Dairy Sci. 86, 407–23 (2003).
55. Gientka, I., Błażejak, S., Stasiak-Różańska, L. & Chlebowska-Śmigiel, A. Exopolysaccharides from yeast: insight into optimal conditions for biosynthesis, chemical composition and functional properties – review. Acta Sci. Pol. Technol. Aliment 14, 283–292 (2015).
56. Shao, B. M., Dai, H., Xu, W., Lin, Z. B. & Gao, X. M. Immune receptors for polysaccharides from Ganoderma lucidum. Biochem. Biophys. Res. Commun. 323, 133–141 (2004).
57. Vidhyalakshmi, R. & Vallinachiyar, C. Apoptosis of Human Breast Cancer Cells (MCF-7) Induced by Polysacccharides Produced by Bacteria. J. Cancer Sci. Ther. 5, 031–034 (2013).
58. Ghada, S., Mahmoud, G., Asker, M. S. & Ghazy, A. Production and Biological Evaluation of Exopolysaccharide From Isolated Rhodotorula glutinins. Aust. J. Basic Appl. Sci. 6, 401–408 (2012).
59. Jin, Y. et al. Antitumor activities of heteropolysaccharides of Poria cocos mycelia from different strains and culture media. Carbohydr. Res. 338, 1517–1521 (2003).
60. Cerning, J. Production of exopolysaccharides by lactic acid bacteria and dairy propionibacteria. Lait 75, 463–472 (1995).
61. Tallon, R., Bressollier, P. & Urdaci, M. C. Isolation and characterization of two exopolysaccharides produced by Lactobacillus plantarum EP56. Res. Microbiol. 154, 705–712 (2003).
62. Wang, J., Zhao, X., Yang, Y., Zhao, A. & Yang, Z. Characterization and bioactivities of an exopolysaccharide produced by Lactobacillus plantarum YW32. Int. J. Biol. Macromol. 74, 119–126 (2015).
63. Hamet, M. F., Piermaria, J. A. & Abraham, A. G. Selection of EPS-producing Lactobacillus strains isolated from kefir grains and rheological characterization of the fermented milks. LWT - Food Sci. Technol. 63, 129–135 (2015).
64. Xu, R., Qian, S., Ding, X., Wengeng, G. & Li, P. Chemical characterization and antioxidant activity of an exopolysaccharide fraction isolated from Bifidobacterium animalis RH. Eur Food Res Technol 232, 231–240 (2011).
65. Zarour, K. et al. Rheology and bioactivity of high molecular weight dextrans synthesised by lactic acid bacteria. Carbohydr. Polym. 174, 646–657 (2017).
66. Nwodo, U. U., Green, E. & Okoh, A. I. Bacterial exopolysaccharides: Functionality and prospects. Int. J. Mol. Sci. 13, 14002–14015 (2012).
67. Wasser, S. Medicinal mushrooms as a source of antitumor and immunomodulating polysaccharides. Appl. Microbiol. Biotechnol. 60, 258–274 (2002).
68. Ooi, V. E. C. & Liu, F. Immunomodulation and Anti-Cancer Activity of Polysaccharide- Protein Complexes. Curr. Med. Chem. 7, 715–729 (2000).
69. Ferreira, J. A. et al. Identification of cell-surface mannans in a virulent Helicobacter pylori strain. Carbohydr. Res. 345, 830–838 (2010).
70. Nordmark, E.-L. Structural and Interaction Studies of Bacterial Polysaccharides by NMR Spectroscopy. (Stockholm University, 2004).
71. Diemer, S. K. et al. Binding Interactions Between α-glucans from Lactobacillus reuteri and Milk Proteins Characterised by Surface Plasmon Resonance. Food Biophys. 7, 220–226 (2012).
72. Wang, Y.-Y. et al. Studies on the Immuno-Modulating and Antitumor Activities of Ganoderma lucidum (Reishi) Polysaccharides: Functional and Proteomic Analyses of a Fucose-Containing Glycoprotein Fraction Responsible for the Activities. Bioorg. Med. Chem. 10, 1057–1062 (2002).
73. Haroun, B. M., Refaat, B. M., Menoufy, H. A. E.-, Amin, H. A. & Amr, A. Structure Analysis and Antitumor Activity of the Exopolysaccharide from Probiotic. J. Appl. Sci. Res. 9, 425–434 (2013).
74. Oleksy, M., Klewicka, E. & Zbieta Klewicka, E. Critical Reviews in Food Science and Nutrition Exopolysaccharides produced by Lactobacillus sp.: Biosynthesis and applications. Crit. Rev. Food Sci. Nutr. 58, 450–462 (2018).
75. Cao, W. et al. A novel polysaccharide, isolated from Angelica sinensis (Oliv.) Diels induces the apoptosis of cervical cancer HeLa cells through an intrinsic apoptotic pathway. Phytomedicine 17, 598–605 (2010).
76. Riedl, S. J. & Shi, Y. Molecular mechanisms of caspase regulation during apoptosis. Nat. Rev. Mol. Cell Biol. 5, 897–907 (2004).
77. Bergamo, A., Dyson, P. J. & Sava, G. The mechanism of tumour cell death by metal-based anticancer drugs is not only a matter of DNA interactions. Coord. Chem. Rev. J. 360, 17–33 (2018).
78. Reed, J. C. Bcl-2 on the brink of breakthroughs in cancer treatment. Nat. Publ. Gr. 25, 3–6 (2018).
79. Adams, J. M. & Cory, S. The BCL-2 arbiters of apoptosis and their growing role as cancer targets. Nat. Publ. Gr. 25, 27–36 (2018).
80. Fan, T. J., Han, L. H., Cong, R. S. & Liang, J. Caspase family proteases and apoptosis. Acta Biochim. Biophys. Sin. (Shanghai). 37, 719–727 (2005).
81. Wu, H. et al. Caspases: A molecular switch node in the crosstalk between autophagy and apoptosis. Int. J. Biol. Sci. 10, 1072–1083 (2014).
82. Wu, Y. J., Wong, B. S., Yea, S. H., Lu, C. I. & Weng, S. H. Sinularin induces apoptosis through mitochondria dysfunction and inactivation of the pI3K/Akt/mTOR pathway in gastric carcinoma cells. Mar. Drugs 14 (2016).
83. Stolfi, C. et al. 2-Methoxy-5-Amino-N-Hydroxybenzamide Sensitizes Colon Cancer Cells to TRAIL-Induced Apoptosis by Regulating Death Receptor 5 and Survivin Expression. Mol Cancer Ther 10, 1969–81 (2011).
84. Ou, Y., Xu, S., Zhu, D. & Yang, X. Molecular mechanisms of exopolysaccharide from Aphanothece halaphytica (EPSAH) induced apoptosis in HeLa cells. PLoS One 9, e87223 (2014).
85. Altonsy, M. O., Andrews, S. C. & Tuohy, K. M. Differential induction of apoptosis in human colonic carcinoma cells (Caco-2) by Atopobium, and commensal, probiotic and enteropathogenic bacteria: Mediation by the mitochondrial pathway. Int. J. Food Microbiol. 137, 190–203 (2010).
86. Wan, Y. et al. Fermentation supernatants of lactobacillus delbrueckii inhibit growth of human colon cancer cells and induce apoptosis through a caspase 3-dependent pathway. Oncol. Lett. 7, 1738–1742 (2014).
87. Chen, Z.-Y., Hsieh, Y.-M., Huang, C.-C. & Tsai, C.-C. Inhibitory Effects of Probiotic Lactobacillus on the Growth of Human Colonic Carcinoma Cell Line HT-29. Molecules 22, 107 (2017).
88. Zhao, K., Jin, M., Chen, Q. & Zheng, P. S. Polysaccharides produced by enterobacter cloacae induce apoptosis in cervical cancer cells. Int. J. Biol. Macromol. 72, 960–964 (2015).
89. Liu, G., Kuang, S., Wu, S., Jin, W. & Sun, C. A novel polysaccharide from Sargassum integerrimum induces apoptosis in A549 cells and prevents angiogensis in vitro and in vivo. Sci. Rep. 6, 1–12 (2016).
90. Di, W. et al. Exopolysaccharides produced by Lactobacillus strains suppress HT-29 cell growth via induction of G0/G1 cell cycle arrest and apoptosis. Oncol. Lett. 16, 3577–3586 (2018).