Antimicrobial activity of cyclic dipeptides produced by Lactobacillus plantarum LBP-K10 against multidrug-resistant bacteria, pathogenic fungi, and influenza A virus

Food Control

Volumn 85, Issue , 2018, Pages 223-234

  Kwak, Min Kyu ^a   Liu, Rui ^a   Kang, Sa Ouk ^a  

^a Seoul National University   (South Korea)

Author keywords

Anion exchange chromatography; Cyclic dipeptides; Influenza A virus; Lactobacillus plantarum LBP K10; Multidrug resistant bacteria; Pathogenic fungi

Indexed keywords

EID: 85042184005     PISSN: 09567135     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.foodcont.2017.10.001     Document Type: Article

References (71)

1. Anon, Cane sugar refining with ion exchange resins. 2009, The Purolite Company.
2. Archer, A.C., Halami, P.M., Probiotic attributes of Lactobacillus fermentum isolated from human feces and dairy products. Applied Microbiology and Biotechnology 99 (2015), 8113–8123.
3. Barua, R., Al Masud, H.A., Mahmud, M.N., Hakim, M.A., Assessment of potential probiotic Lactobacillus strains isolated from goat milk. International Organization of Scientific Research Journal of Pharmacy and Biological Sciences 10:4 (2015), 9–15.
4. Bellezza, I., Peirce, M.J., Minelli, A., Cyclic dipeptides: From bugs to brain. Trends in Molecular Medicine 20 (2014), 551–558.
5. Bhushan, R., Dixit, S., HPLC enantioresolution of (R,S)-baclofen using three newly synthesized dichloro-s-triazine reagents having amines and five others having amino acids as chiral auxiliaries. Biomedical Chromatography 26 (2012), 743–748.
6. Bivi, M.R., Farhana, M.S.N., Khairulmazmi, A., Idris, A., Control of Ganoderma boninense: A causal agent of basal stem rot disease in oil palm with endophyte bacteria in vitro. International Journal of Agriculture and Biology 12 (2010), 833–839.
7. Borthwick, A.D., 2,5-Diketopiperazines: Synthesis, reactions, medicinal chemistry, and bioactive natural products. Chemical Reviews 112 (2012), 3641–3716.
8. Borthwick, A.D., Da Costa, N.C., 2,5-diketopiperazines in food and beverages: Taste and bioactivity. Critical Reviews in Food Science and Nutrition 57 (2017), 718–742.
9. Brückner, C., Fahr, A., Imhof, D., Scriba, G.K., Degradation kinetics of an aspartyl-tripeptide-derived diketopiperazine under forced conditions. Journal of Pharmaceutical Sciences 101 (2012), 4178–4190.
10. Campbell, J., Lin, Q., Geske, G.D., Blackwell, H.E., New and unexpected insights into the modulation of LuxR-type quorum sensing by cyclic dipeptides. American Chemical Society Chemical Biology 4 (2009), 1051–1059.
11. Chong, K.P., Rossall, S., Atong, M., In vitro antimicrobial activity and fungitoxicity of syringic acid, caffeic acid and 4-hydroxybenzoic acid against Ganoderma boninense. Journal of Agricultural Science 1 (2009), 15–20.
12. Dal Bello, F., Clarke, C.I., Ryan, L.A.M., Ulmer, H., Schober, T.J., Ström, K., et al. Improvement of the quality and shelf life of wheat bread by fermentation with the antifungal strain Lactobacillus plantarum FST 1.7. Journal of Cereal Science 45 (2007), 309–318.
13. Damodharan, K., Palaniyandi, S.A., Yang, S.H., Suh, J.-W., In vitro probiotic characterization of Lactobacillus strains from fermented radish and their anti-adherence activity against enteric pathogens. Canadian Journal of Microbiology 61:11 (2015), 837–850.
14. Dec, M., Puchalski, A., Urban-Chmiel, R., Wernicki, A., Screening of Lactobacillus strains of domestic goose origin against bacterial poultry pathogens for use as probiotics. Poultry Science 93 (2014), 2464–2472.
15. Deepa, I., Kumar, S.N., Sreerag, R.S., Nath, V.S., Mohandas, C., Purification and synergistic antibacterial activity of arginine derived cyclic dipeptides, from Achromobacter sp. associated with a rhabditid entomopathogenic nematode against major clinically relevant biofilm forming wound bacteria. Frontiers in Microbiology, 6, 2015, 876.
16. Devi, S.M., Halami, P.M., Detection and characterization of pediocin PA-1/AcH like bacteriocin producing lactic acid bacteria. Current Microbiology 63 (2011), 181–185.
17. Elayaraja, S., Annamalai, N., Mayavu, P., Balasubramanian, T., Production, purification and characterization of bacteriocin from Lactobacillus murinus AU06 and its broad antibacterial spectrum. Asian Pacific Journal of Tropical Biomedicine 4:Suppl 1 (2014), S305–S311.
18. Elkahoui, S., Abdel rahim, H., Tabbene, O., Shaaban, M., Limam, F., Laatsch, H., Cyclo-(His, Leu): A new microbial diketopiperazine from a terrestrial Bacillus subtilis strain B38. Natural Product Research 27:2 (2013), 108–116.
19. Fonzi, W.A., Irwin, M.Y., Isogenic strain construction andgene mapping in Candidaalbicans. Genetics 134 (1993), 717–728.
20. Funasaki, N., Hada, S., Neya, S., Conformational effects in reversed-phase liquid chromatographic separation of diastereomers of cyclic dipeptides. Analaytical Chemistry 65 (1993), 1861–1867.
21. Gao, Q., Liu, F., Zhang, T., Zhang, J., Jia, S., Yu, C., et al. The role of lactic acid adsorption by ion exchange chromatography. PLoS One, 5, 2010, e13948.
22. Gu, Q., Fu, L., Wang, Y., Lin, J., Identification and characterization of extracellular cyclic dipeptides as quorum-sensing signal molecules from Shewanella baltica, the specific spoilage organism of Pseudosciaena crocea during 4 °C storage. Journal of Agricultural and Food Chemistry 61 (2013), 11645–11652.
23. Hedberg, M., Hasslöf, P., Sjöström, I., Twetman, S., Stecksén-Blicks, C., Sugar fermentation in probiotic bacteria-an in vitro study. Oral Microbiology and Immunology 23 (2008), 482–485.
24. Houston, D.R., Synstad, B., Eijsink, V.G., Stark, M.J., Eggleston, I.M., van Aalten, et al. Structure-basedexplorationofcyclic dipeptidechitinaseinhibitors. Journal of Medicinal Chemistry 47 (2004), 5713–5720.
25. Huang, R., Zhou, X., Xu, T., Yang, X., Liu, Y., Diketopiperazines from marine organisms. Chemistry & Biodiversity 7 (2010), 2809–2829.
26. Ishikawa, K., Hosoe, T., Itabashi, T., Wakana, D., Takizawa, K., Yaguchi, T., et al. Novoamauromine and ent-Cycloechinulin: two new diketopiperazine derivatives from Aspergillus novofumigatus. Chemical and Pharmaceutical Bulletin 58 (2010), 717–719.
27. Ji, K., Jang, N.Y., Kim, Y.T., Isolation of Lactic Acid Bacteria Showing Antioxidative and Probiotic Activities from Kimchi and Infant Feces. Journal of Microbiology and Biotechnology 25 (2015), 1568–1577.
28. Jung, E.Y., Hong, Y.H., Park, C., Suh, H.J., Effects of Cyclo-His-Pro-enriched yeast hydrolysate on blood glucose levels and lipid metabolism in obese diabetic ob/ob mice. Nutrition Research and Practice 10 (2016), 154–160.
29. Kiran, G.S., Hassan, S., Sajayan, A., Selvin, J., Quorum Quenching Compounds from Natural Sources. Bioresources and bioprocess in biotechnology, 2017, Springer, 351–364.
30. Kumar, S.N., Lankalapalli, R.S., Kumar, B.S., In vitro antibacterial screening of six proline-based cyclic dipeptides in combination with β-lactam antibiotics against medically important bacteria. Applied Biochemistry and Biotechnology 173 (2014), 116–128.
31. Kumar, S.N., Mohandas, C., Nambisan, B., Sreerag, R.S., Jayaprakas, C.A., Cyclo(L-Pro-D-Arg): a new antibacterial and antitumour diketopiperazine from Bacillus cereus associated with a rhabditid entomopathogenic. Folia Microbiologica 59 (2014), 197–202.
32. Kumar, S.N., Sreekala, S.R., Chandrasekaran, D., Nambisan, B., Anto, R.J., Biocontrol of Aspergillus species on peanut kernels by antifungal diketopiperazine producing Bacillus cereus associated with entomopathogenic nematode. PLoS One, 9, 2014, 106041.
33. Kwak, M.-K., Liu, R., Kim, M.-K., Moon, D., Song, S.-H., Kang, S.-O., Cyclic dipeptides originated from lactic acid bacteria inhibit the proliferation of pathogenic fungi. Journal of Microbiology 52 (2014), 64–70.
34. Kwak, M.-K., Liu, R., Kwon, J.-O., Kim, M.-K., Kim, A.H., Kang, S.-O., Cyclic dipeptides originated from lactic acid bacteria inhibit the proliferation of influenza A virus. Journal of Microbiology 51 (2013), 836–843.
35. Kwon, O.S., Park, S.H., Yun, B., Pyun, Y.R., Kim, C., Cyclo(dehydroala-L-Leu), an α-glucosidase inhibitor from Penicillium sp. F70614. The Journal of Antibiotics 53 (2000), 954–958.
36. Lesma, G., Cecchi, R., Crippa, S., Giovanelli, P., Meneghetti, F., Musolino, M., et al. Ugi 4-CR/Pictet-Spengler reaction as a short route to tryptophan-derived peptidomimetics. Organic & Biomolecular Chemistry 10 (2012), 9004–9012.
37. Li, H., Liu, L., Zhang, S., Cui, W., Lv, J., Identification of antifungal compounds produced by Lactobacillus casei AST18. Current Microbiology 65 (2012), 156–161.
38. Li, J., Wang, W., Xu, S.X., Magarvey, N.A., McCormick, J.K., Lactobacillus reuteri-produced cyclic dipeptides quench agr-mediated expression of toxic shock syndrome toxin-1 in staphylococci. Proceedings of the National Academy of Sciences of the United States of America 108 (2011), 3360–3365.
39. Lim, S.M., Im, D.S., Screening and characterization of probiotic lactic acid bacteria isolated from Korean fermented foods. Journal of Microbiology and Biotechnology 19 (2009), 178–186.
40. Lind, H., Sjögren, J., Gohil, S., Kenne, L., Schnürer, J., Broberg, A., Antifungal compounds from cultures of dairy propionibacteria type strains. FEMS Microbiology Letters 271 (2007), 310–315.
41. Liu, R., Kim, A., Kwak, M.-K., Kang, S.-O., Proline-Based Cyclic Dipeptides from Korean Fermented Vegetable Kimchi and from Leuconostoc mesenteroides LBP-K06 Have Activities against Multidrug-Resistant Bacteria. Frontiers in Microbiology, 8, 2017, 761.
42. Liu, C.J., Wang, R., Gong, F.M., Liu, X.F., Zheng, H.J., Luo, Y.Y., et al. Complete genome sequences and comparative genome analysis of Lactobacillus plantarum strain 5-2 isolated from fermented soybean. Genomics 106 (2015), 404–411.
43. Mayo, B., van Sinderen, D., Ventura, M., Genome analysis of food grade lactic acid-producing bacteria: from basics to applications. Current Genomics 9 (2008), 169–183.
44. McCleland, K., Milne, P.J., Lucieto, F.R., Frost, C., Brauns, S.C., Van De Venter, M., et al. An investigation into the biological activity of the selected histidine-containing diketopiperazines cyclo(His-Phe) and cyclo(His-Tyr). Journal of Pharmacy and Pharmacology 56 (2004), 1143–1153.
45. Minelli, A., Bellezza, I., Grottelli, S., Galli, F., Focus on cyclo (His-Pro): history and perspectives as antioxidant peptide. Amino Acids 35:2 (2008), 283–289.
46. Nagia, M.M.S., Shaaban, M., Abdel-Aziz, M.S., El-Zalabani, S.M., Hanna, A.G., Secondary metabolites and bioactivity of two fungal strains. Egyptian Pharmaceutical Journal, 11(1), 2012, 16.
47. Özogul, F., Hamed, I., The importance of lactic acid bacteria for the prevention of bacterial growth and their biogenic amines formation: A review. Critical Reviews in Food Science and Nutrition 27 (2017), 1–11.
48. Pardali, E., Paramithiotis, S., Papadelli, M., Mataragas, M., Drosinos, E.H., Lactic acid bacteria population dynamics during spontaneous fermentation of radish (Raphanus sativus L.) roots in brine. World Journal of Microbiology and Biotechnology, 33, 2017, 110.
49. Patel, M., Bassi, A.S., Zhu, J.J., Gomaa, H., Investigation of a dual-particle liquid-solid circulating fluidized bed bioreactor for extractive fermentation of lactic acid. Biotechnology Progress 24 (2008), 821–831.
50. Perzborn, M., Syldatk, C., Rudat, J., Separation of cyclic dipeptides (diketopiperazines) from their corresponding linear dDipeptides by RP-HPLC and method validation. Chromatography Research International 2013 (2013), 1–8.
51. Prakash, K.R., Tang, Y., Kozikowski, A.P., Flippen-Anderson, J.L., Knoblach, S.M., Faden, A.I., Synthesis and biological activity of novel neuroprotective diketopiperazines. Bioorganic & Medicinal Chemistry 10 (2002), 3043–3048.
52. Ren, D., Li, C., Qin, Y., Yin, R., Du, S., Ye, F., et al. In vitro evaluation of the probiotic and functional potential of Lactobacillus strains isolated from fermented food and human intestine. Anaerobe 30 (2014), 1–10.
53. Rhee, K.H., Isolation and characterization of Streptomyces sp. KH-614 producing anti-VRE (vancomycin-resistant enterococci) antibiotics. The Journal of General and Applied Microbiology 48 (2002), 327–331.
54. Rhee, K.H., Cyclic dipeptides exhibit synergistic, broad spectrum antimicrobial effects and have anti-mutagenic properties. International Journal of Antimicrobial Agents 24 (2004), 423–427.
55. Rouse, S., van Sinderen, D., Bioprotective potential of lactic acid bacteria in malting and brewing. Journal of Food Protection 71 (2008), 1724–1733.
56. Shan, Z., Xiong, Y., Yi, J., Hu, X., Heterocomplexation of a chiral dipeptide and quantitative enantiomeric enrichment of nonracemic 1,1’-bi-2-naphthol. The Journal of Organic Chemistry 73 (2008), 9158–9160.
57. Shigemura, Y., Iwai, K., Morimatsu, F., Iwamoto, T., Mori, T., Oda, C., et al. Effect of Prolyl-hydroxyproline (Pro-Hyp), a food-derived collagen peptide in human blood, on growth of fibroblasts from mouse skin. Journal of Agricultural and Food Chemistry 57 (2009), 444–449.
58. Silva, M.M.D., Andrade, M.D.S., Bauermeister, A., Merfa, M.V., Forim, M.R., Fernandes, J.B., et al. A Simple Defined Medium for the Production of True Diketopiperazines in Xylella fastidiosa and Their Identification by Ultra-Fast Liquid Chromatography-Electrospray Ionization Ion Trap Mass Spectrometry. Molecules, 22, 2017, E985.
59. Singh, A.K., Mukherjee, S., Adhikari, M.D., Ramesh, A., Fluorescence-Based Comparative Evaluation of Bactericidal Potency and Food Application Potential of Anti-listerial Bacteriocin Produced by Lactic Acid Bacteria Isolated from Indigenous Samples. Probiotics and Antimicrobial Proteins 4 (2012), 122–132.
60. Ström, K., Sjögren, J., Broberg, A., Schnürer, J., Lactobacillus plantarum MiLAB 393 produces the antifungal cyclic dipeptides cyclo(L-Phe-L-Pro) and cyclo(L-Phe-trans-4-OH-L-Pro) and 3-phenyllactic acid. Applied and Environmental Microbiology 68 (2002), 4322–4327.
61. Swadesh, J.K., HPLC: Practical and industrial applications. 2nd ed., 2000, CRC Press, 167–169.
62. Trabelsi, I., Slima, S.B., Chaabane, H., Riadh, B.S., Purification and characterization of a novel exopolysaccharides produced by Lactobacillus sp. Ca 6. International Journal of Biological Macromolecules 74 (2015), 541–546.
63. Uyemura, K., Dhanani, S., Yamaguchi, D.T., Song, M.K., Metabolism and toxicity of high doses of cyclo (His-Pro) plus zinc in healthy human subjects. Journal of Drug Metabolism and Toxicology, 1, 2010, 105.
64. Wang, J.H., Quan, C.S., Qi, X.H., Li, X., Fan, S.D., Determination of diketopiperazines of Burkholderia cepacia CF-66 by gas chromatography-mass spectrometry. Analytical and Bioanalytical Chemistry 396 (2010), 1773–1779.
65. Wang, Y., Wang, P., Ma, H., Zhu, W., Developments around the bioactive diketopiperazines: a patent review. Expert Opinion on Therapeutic Patents 23 (2013), 1415–1433.
66. Wattana-Amorn, P., Charoenwongsa, W., Williams, C., Crump, M.P., Apichaisataienchote, B., Antibacterial activity of cyclo(L-Pro-L-Tyr) and cyclo(D-Pro-L-Tyr) from Streptomyces sp. strain 22-4 against phytopathogenic bacteria. Natural Product Research. 15 (2015), 1–4.
67. Wiegand, I., Hilpert, K., Hancock, R.E.W., Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nature Protocols 3 (2008), 163–175.
68. Wikler, M.A., Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically: Approved standard. 2006, Clinical and laboratory standards institute.
69. Wu, J., Hu, Y., Zhou, J., Qian, W., Lin, X., Chen, Y., et al. Separation of d-lactic acid from aqueous solutions based on the adsorption technology. Colloids and Surfaces A: Physicochemical and Engineering Aspects 407 (2012), 29–37.
70. Yan, P.-S., Song, Y., Sakuno, E., Nakajima, H., Nakagawa, H., Yabe, K., Cyclo(Lleucyl-L-prolyl) produced by Achromobacter xylosoxidans inhibits aflatoxin production by Aspergillus parasiticus. Applied and Environmental Microbiology 70 (2004), 7466–7473.
71. Yang, E.J., Kim, Y.S., Chang, H.C., Purification and characterization of antifungal δ-dodecalactone from Lactobacillus plantarum AF1 isolated from kimchi. Journal of Food Protection 74 (2011), 651–657.