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References

  1. Zin N, Loi C, Sarmin N, Rosli A. 2010. Cultivationdependent characterization of endophytic actinomycetes. Res. J. Microbiol. 5: 717-724.
    CrossRef
  2. Junaidah AS, Suhaini S, Sidek HM, Basri DF, Zin NM. 2015. Anti-methicillin resistant Staphylococcus aureus activity and optimal culture condition of Streptomyces sp. SUK 25. Jundishapur J. Microbiol. 8: 1-7.
    CrossRef
  3. Alshaibani MM, Jalil J, Sidik NM, Edrada-Ebel R, Zin NM. 2016. Isolation and characterization of cyclo-(tryptophanylprolyl) and chloramphenicol from Streptomyces sp. SUK 25 with antimethicillin-resistant Staphylococcus aureus activity. Drug Des. Devel. Ther. 10: 1817-1827.
    Pubmed PMC
  4. Fenical W. 1993. Chemical studies of marine bacteria:developing a new resource. Chem. Rev. 93: 1673-1683.
    CrossRef
  5. Stierle A, Cardellina Ii J, Singleton F. 1988. A marine Micrococcus produces metabolites ascribed to the sponge Tedania ignis. Experientia 44: 1021-1021.
    Pubmed CrossRef
  6. Bugni TS, Ireland CM. 2004. Marine-derived fungi: a chemically and biologically diverse group of microorganisms. Nat. Prod. Rep. 21: 143-163.
    Pubmed CrossRef
  7. Huang R, Zhou X, Xu T, Yang X, Liu Y. 2010. Diketopiperazines from marine organisms. Chem. Biodivers. 7: 2809-2829.
    Pubmed CrossRef
  8. Gerets H, Tilmant K, Gerin B, Chanteux H, Depelchin B, Dhalluin S, et al. 2012. Characterization of primary human hepatocytes, HepG2 cells, and HepaRG cells at the mRNA level and CYP activity in response to inducers and their predictivity for the detection of human hepatotoxins. Cell Biol. Toxicol. 28: 69-87.
    Pubmed PMC CrossRef
  9. Guillouzo A, Corlu A, Aninat C, Glaise D, Morel F, Guguen-Guillouzo C. 2007. The human hepatoma HepaRG cells: a highly differentiated model for studies of liver metabolism and toxicity of xenobiotics. Chem. Biol. Interact. 168: 66-73.
    Pubmed CrossRef
  10. Aninat C, Piton A, Glaise D, Le Charpentier T, Langouët S, Morel F, et al. 2006. Expression of cytochromes P450, conjugating enzymes and nuclear receptors in human hepatoma HepaRG cells. Drug Metab. Dispos. 34: 75-83.
    Pubmed CrossRef
  11. Gripon P, Rumin S, Urban S, Le Seyec J, Glaise D, Cannie I, et al. 2002. Infection of a human hepatoma cell line by hepatitis B virus. Proc. Natl. Acad. Sci. USA 99: 15655-15660.
    Pubmed PMC CrossRef
  12. Dobretsov SV, Qian P-Y. 2002. Effect of bacteria associated with the green alga Ulva reticulata on marine micro- and macrofouling. Biofouling 18: 217-228.
    CrossRef
  13. Mosmann T. 1983. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65: 55-63.
    CrossRef
  14. MacIntyre L, Zhang T, Viegelmann C, Martinez IJ, Cheng C, Dowdells C, et al. 2014. Metabolomic tools for secondary metabolite discovery from marine microbial symbionts. Mar. Drugs 12: 3416-3448.
    Pubmed PMC CrossRef
  15. Abdelmohsen UR, Cheng C, Viegelmann C, Zhang T, Grkovic T, Ahmed S, et al. 2014. Dereplication strategies for targeted isolation of new antitrypanosomal actinosporins A and B from a marine sponge associated-Actinokineospora sp. EG49. Mar. Drugs 12: 1220-1244.
    Pubmed PMC CrossRef
  16. Li X, Dobretsov S, Xu Y, Xiao X, Hung OS, Qian PY. 2006. Antifouling diketopiperazines produced by a deep-sea bacterium, Streptomyces fungicidicus. Biofouling 22: 201-208.
    CrossRef
  17. Stark T, Hofmann T. 2005. Structures, sensory activity, and dose/response functions of 2,5-diketopiperazines in roasted cocoa nibs (Theobroma cacao). J. Agric. Food Chem. 53: 7222-7231.
    Pubmed CrossRef
  18. Adamczeski M, Reed AR, Crews P. 1995. New and known diketopiperazines from the Caribbean sponge, Calyx cf. podatypa. J. Nat. Prod. 58: 201-208.
    Pubmed CrossRef
  19. Rahman H. 2008. Unusual sesquiterpenes: gorgonenes and further bioactive secondary metabolites derived from marine and terrestrial bacteria. PhD Thesis. Göttingen University, Germany.
  20. Gebhardt K, Pukall R, Fiedler H-P. 2001. Streptocidins AD, novel cyclic decapeptide antibiotics produced by Streptomyces sp. Tu 6071. I. Taxonomy, fermentation, isolation and biological activities. J. Antibiot. (Tokyo) 54: 428-433.
    CrossRef
  21. Šmelcerović AA, Schiebel M, Đorđević SM. 2002. The isolation of (6S, 9S)-cyclo (prolylvalyl) from marine actinomycete, by use of high speed contercurrent chromatography. J. Serbian Chem. Soc. 67: 27-30.
    CrossRef
  22. Rhee K-H. 2002. Isolation and characterization of Streptomyces sp. KH-614 producing anti-VRE (vancomycin-resistant enterococci) antibiotics. J. Gen. Appl. Microbiol. 48: 321-327.
    Pubmed CrossRef
  23. Jiang Z, Boyd KG, Mearns-Spragg A, Adams DR, Wright PC, Burgess JG. 2000. Two diketopiperazines and one halogenated phenol from cultures of the marine bacterium, Pseudoalteromonas luteoviolacea. Nat. Prod. Lett. 14: 435-440.
    CrossRef
  24. Rhee K-H. 2004. Cyclic dipeptides exhibit synergistic, broad spectrum antimicrobial effects and have anti-mutagenic properties. Int. J. Antimicrob. Agents 24: 423-427.
    Pubmed CrossRef
  25. Furtado NA, Pupo MT, Carvalho I, Campo VL, Duarte MCT, Bastos JK. 2005. Diketopiperazines produced by an Aspergillus fumigatus Brazilian strain. J. Braz. Chem. Soc. 16: 1448-1453.
    CrossRef
  26. de Carvalho MP, Abraham W-R. 2012. Antimicrobial and biofilm inhibiting diketopiperazines. Curr. Med. Chem. 19: 3564-3577.
    Pubmed CrossRef
  27. Huang R, Yan T, Peng Y, Zhou X, Yang X, Liu Y. 2014. Diketopiperazines from the marine sponge Axinella sp. Chem. Nat. Compd. 50: 191-193.
    CrossRef
  28. Khedr AI, Mohamed GA, Orabi MA, Ibrahim SR, Yamada K. 2015. Staphylopeptide A, a new cyclic tetrapeptide from culture broth of Staphylococcus sp. Phytochem. Lett. 13: 11-14.
    CrossRef
  29. Szabo M, Veres Z, Baranyai Z, Jakab F, Jemnitz K. 2013. Comparison of human hepatoma HepaRG cells with human and rat hepatocytes in uptake transport assays in order to predict a risk of drug induced hepatotoxicity. PLoS One 8: e59432.
    Pubmed PMC CrossRef
  30. Vázquez-Rivera D, González O, Guzmán-Rodríguez J, DíazPérez AL, Ochoa-Zarzosa A, López-Bucio J, et al. 2015. Cytotoxicity of cyclodipeptides from Pseudomonas aeruginosa PAO1 leads to apoptosis in human cancer cell lines. Biomed. Res. Int. 2015: 197608.
    Pubmed PMC CrossRef
  31. Cui CB, Usukata M, Kakeya H, Onose R, Okada G, Takahashi I, et al. 1996. Acetophthalidin, a novel inhibitor of mammalian cell cycle, produced by a fungus isolated from a sea sediment. J. Antibiot. (Tokyo) 49: 216-219.
    CrossRef
  32. Kondoh M, Usui T, Mayumi T, Osada H. 1998. Effects of tryprostatin derivatives on microtubule assembly in vitro and in situ. J. Antibiot. (Tokyo) 51: 801-804.
    CrossRef
  33. Folkes A, Brown SD, Canne LE, Chan J, Engelhardt E, Epshteyn S, et al. 2002. Design, synthesis and in vitro evaluation of potent, novel, small molecule inhibitors of plasminogen activator inhibitor-1. Bioorg. Med. Chem. Lett. 12: 1063-1066.
    CrossRef
  34. Martins MB, Carvalho I. 2007. Diketopiperazines: biological activity and synthesis. Tetrahedron 63: 9923-9932.
    CrossRef
  35. McCleland K, Milne P, Lucieto F, Frost C, Brauns S, Venter M, et al. 2004. An investigation into the biological activity of the selected histidine-containing diketopiperazines cyclo (HisPhe) and cyclo (His-Tyr). J. Pharm. Pharmacol. 56: 1143-1153.
    Pubmed CrossRef
  36. Choi E, Park JS, Kim YJ, Jung JH, Lee J, Kwon H, et al. 2011. Apoptosis-inducing effect of diketopiperazine disulfides produced by Aspergillus sp. KMD 901 isolated from marine sediment on HCT116 colon cancer cell lines. J. Appl. Microbiol. 110: 304-313.
    Pubmed CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2017; 27(7): 1249-1256

Published online July 28, 2017 https://doi.org/10.4014/jmb.1608.08032

Copyright © The Korean Society for Microbiology and Biotechnology.

Isolation, Purification, and Characterization of Five Active Diketopiperazine Derivatives from Endophytic Streptomyces SUK 25 with Antimicrobial and Cytotoxic Activities

Muhanna M. Alshaibani 1, Noraziah M. Zin 1*, Juriyati Jalil 2, Nik M. Sidik 3, Siti Junaidah Ahmad 1, Nurkhalida Kamal 4 and Ruangelie Edrada-Ebel 4

1Programme of Biomedical Science, School of Diagnostic and Applied Health Sciences, Faculty of Health Sciences, Universiti Kebangsaan Malaysia, Jalan Raja Muda Abdul Aziz, 50300 Kuala Lumpur, Malaysia, 2Drug and Herbal Research Centre, Faculty of Pharmacy, Universiti Kebangsaan Malaysia, Jalan Raja Muda Abdul Aziz, 50300 Kuala Lumpur, Malaysia, 3Faculty of Ago-based Industry, Universiti Malaysia Kelantan, 17600 Jeli, Kelantan, Malaysia, 4Strathclyde Institute of Pharmacy and Biomedical Sciences, University of Strathclyde, Glasgow G4 0RE, Scotland, 5Department of Pharmaceutical Sciences, Faculty of Pharmacy, Cyberjaya University College of Medical Sciences, 63000 Cyberjaya, Selangor Malaysia

Received: August 13, 2016; Accepted: May 21, 2017

Abstract

In our search for new sources of bioactive secondary metabolites from Streptomyces sp., the
ethyl acetate extracts from endophytic Streptomyces SUK 25 afforded five active
diketopiperazine (DKP) compounds. The aim of this study was to characterize the bioactive
compounds isolated from endophytic Streptomyces SUK 25 and evaluate their bioactivity
against multiple drug resistance (MDR) bacteria such as Enterococcus raffinosus, Staphylococcus
aureus, Klebsiella pneumoniae, Acinetobacter baumanii, Pseudomonas aeruginosa, and Enterobacter
spp., and their cytotoxic activities against the human hepatoma (HepaRG) cell line. The
production of secondary metabolites by this strain was optimized through Thornton’s
medium. Isolation, purification, and identification of the bioactive compounds were carried
out using high-performance liquid chromatography, high-resolution mass liquid
chromatography-mass spectrometry, Fourier transform infrared spectroscopy, and nuclear
magnetic resonance, and cryopreserved HepaRG cells were selected to test the cytotoxicity.
The results showed that endophytic Streptomyces SUK 25 produces four active DKP
compounds and an acetamide derivative, which were elucidated as cyclo-(L-Val-L-Pro), cyclo-
(L-Leu-L-Pro), cyclo-(L-Phe-L-Pro), cyclo-(L-Val-L-Phe), and N-(7-hydroxy-6-methyl-octyl)-
acetamide. These active compounds exhibited activity against methicillin-resistant S. aureus
ATCC 43300 and Enterococcus raffinosus, with low toxicity against human hepatoma HepaRG
cells. Endophytic Streptomyces SUK 25 has the ability to produce DKP derivatives biologically
active against some MDR bacteria with relatively low toxicity against HepaRG cells line.

Keywords: Cytotoxicity, diketopiperazines, Enterococcus raffinosus, HepaRG, MRSA, Streptomyces SUK 25

References

  1. Zin N, Loi C, Sarmin N, Rosli A. 2010. Cultivationdependent characterization of endophytic actinomycetes. Res. J. Microbiol. 5: 717-724.
    CrossRef
  2. Junaidah AS, Suhaini S, Sidek HM, Basri DF, Zin NM. 2015. Anti-methicillin resistant Staphylococcus aureus activity and optimal culture condition of Streptomyces sp. SUK 25. Jundishapur J. Microbiol. 8: 1-7.
    CrossRef
  3. Alshaibani MM, Jalil J, Sidik NM, Edrada-Ebel R, Zin NM. 2016. Isolation and characterization of cyclo-(tryptophanylprolyl) and chloramphenicol from Streptomyces sp. SUK 25 with antimethicillin-resistant Staphylococcus aureus activity. Drug Des. Devel. Ther. 10: 1817-1827.
    Pubmed KoreaMed
  4. Fenical W. 1993. Chemical studies of marine bacteria:developing a new resource. Chem. Rev. 93: 1673-1683.
    CrossRef
  5. Stierle A, Cardellina Ii J, Singleton F. 1988. A marine Micrococcus produces metabolites ascribed to the sponge Tedania ignis. Experientia 44: 1021-1021.
    Pubmed CrossRef
  6. Bugni TS, Ireland CM. 2004. Marine-derived fungi: a chemically and biologically diverse group of microorganisms. Nat. Prod. Rep. 21: 143-163.
    Pubmed CrossRef
  7. Huang R, Zhou X, Xu T, Yang X, Liu Y. 2010. Diketopiperazines from marine organisms. Chem. Biodivers. 7: 2809-2829.
    Pubmed CrossRef
  8. Gerets H, Tilmant K, Gerin B, Chanteux H, Depelchin B, Dhalluin S, et al. 2012. Characterization of primary human hepatocytes, HepG2 cells, and HepaRG cells at the mRNA level and CYP activity in response to inducers and their predictivity for the detection of human hepatotoxins. Cell Biol. Toxicol. 28: 69-87.
    Pubmed KoreaMed CrossRef
  9. Guillouzo A, Corlu A, Aninat C, Glaise D, Morel F, Guguen-Guillouzo C. 2007. The human hepatoma HepaRG cells: a highly differentiated model for studies of liver metabolism and toxicity of xenobiotics. Chem. Biol. Interact. 168: 66-73.
    Pubmed CrossRef
  10. Aninat C, Piton A, Glaise D, Le Charpentier T, Langouët S, Morel F, et al. 2006. Expression of cytochromes P450, conjugating enzymes and nuclear receptors in human hepatoma HepaRG cells. Drug Metab. Dispos. 34: 75-83.
    Pubmed CrossRef
  11. Gripon P, Rumin S, Urban S, Le Seyec J, Glaise D, Cannie I, et al. 2002. Infection of a human hepatoma cell line by hepatitis B virus. Proc. Natl. Acad. Sci. USA 99: 15655-15660.
    Pubmed KoreaMed CrossRef
  12. Dobretsov SV, Qian P-Y. 2002. Effect of bacteria associated with the green alga Ulva reticulata on marine micro- and macrofouling. Biofouling 18: 217-228.
    CrossRef
  13. Mosmann T. 1983. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65: 55-63.
    CrossRef
  14. MacIntyre L, Zhang T, Viegelmann C, Martinez IJ, Cheng C, Dowdells C, et al. 2014. Metabolomic tools for secondary metabolite discovery from marine microbial symbionts. Mar. Drugs 12: 3416-3448.
    Pubmed KoreaMed CrossRef
  15. Abdelmohsen UR, Cheng C, Viegelmann C, Zhang T, Grkovic T, Ahmed S, et al. 2014. Dereplication strategies for targeted isolation of new antitrypanosomal actinosporins A and B from a marine sponge associated-Actinokineospora sp. EG49. Mar. Drugs 12: 1220-1244.
    Pubmed KoreaMed CrossRef
  16. Li X, Dobretsov S, Xu Y, Xiao X, Hung OS, Qian PY. 2006. Antifouling diketopiperazines produced by a deep-sea bacterium, Streptomyces fungicidicus. Biofouling 22: 201-208.
    CrossRef
  17. Stark T, Hofmann T. 2005. Structures, sensory activity, and dose/response functions of 2,5-diketopiperazines in roasted cocoa nibs (Theobroma cacao). J. Agric. Food Chem. 53: 7222-7231.
    Pubmed CrossRef
  18. Adamczeski M, Reed AR, Crews P. 1995. New and known diketopiperazines from the Caribbean sponge, Calyx cf. podatypa. J. Nat. Prod. 58: 201-208.
    Pubmed CrossRef
  19. Rahman H. 2008. Unusual sesquiterpenes: gorgonenes and further bioactive secondary metabolites derived from marine and terrestrial bacteria. PhD Thesis. Göttingen University, Germany.
  20. Gebhardt K, Pukall R, Fiedler H-P. 2001. Streptocidins AD, novel cyclic decapeptide antibiotics produced by Streptomyces sp. Tu 6071. I. Taxonomy, fermentation, isolation and biological activities. J. Antibiot. (Tokyo) 54: 428-433.
    CrossRef
  21. Šmelcerović AA, Schiebel M, Đorđević SM. 2002. The isolation of (6S, 9S)-cyclo (prolylvalyl) from marine actinomycete, by use of high speed contercurrent chromatography. J. Serbian Chem. Soc. 67: 27-30.
    CrossRef
  22. Rhee K-H. 2002. Isolation and characterization of Streptomyces sp. KH-614 producing anti-VRE (vancomycin-resistant enterococci) antibiotics. J. Gen. Appl. Microbiol. 48: 321-327.
    Pubmed CrossRef
  23. Jiang Z, Boyd KG, Mearns-Spragg A, Adams DR, Wright PC, Burgess JG. 2000. Two diketopiperazines and one halogenated phenol from cultures of the marine bacterium, Pseudoalteromonas luteoviolacea. Nat. Prod. Lett. 14: 435-440.
    CrossRef
  24. Rhee K-H. 2004. Cyclic dipeptides exhibit synergistic, broad spectrum antimicrobial effects and have anti-mutagenic properties. Int. J. Antimicrob. Agents 24: 423-427.
    Pubmed CrossRef
  25. Furtado NA, Pupo MT, Carvalho I, Campo VL, Duarte MCT, Bastos JK. 2005. Diketopiperazines produced by an Aspergillus fumigatus Brazilian strain. J. Braz. Chem. Soc. 16: 1448-1453.
    CrossRef
  26. de Carvalho MP, Abraham W-R. 2012. Antimicrobial and biofilm inhibiting diketopiperazines. Curr. Med. Chem. 19: 3564-3577.
    Pubmed CrossRef
  27. Huang R, Yan T, Peng Y, Zhou X, Yang X, Liu Y. 2014. Diketopiperazines from the marine sponge Axinella sp. Chem. Nat. Compd. 50: 191-193.
    CrossRef
  28. Khedr AI, Mohamed GA, Orabi MA, Ibrahim SR, Yamada K. 2015. Staphylopeptide A, a new cyclic tetrapeptide from culture broth of Staphylococcus sp. Phytochem. Lett. 13: 11-14.
    CrossRef
  29. Szabo M, Veres Z, Baranyai Z, Jakab F, Jemnitz K. 2013. Comparison of human hepatoma HepaRG cells with human and rat hepatocytes in uptake transport assays in order to predict a risk of drug induced hepatotoxicity. PLoS One 8: e59432.
    Pubmed KoreaMed CrossRef
  30. Vázquez-Rivera D, González O, Guzmán-Rodríguez J, DíazPérez AL, Ochoa-Zarzosa A, López-Bucio J, et al. 2015. Cytotoxicity of cyclodipeptides from Pseudomonas aeruginosa PAO1 leads to apoptosis in human cancer cell lines. Biomed. Res. Int. 2015: 197608.
    Pubmed KoreaMed CrossRef
  31. Cui CB, Usukata M, Kakeya H, Onose R, Okada G, Takahashi I, et al. 1996. Acetophthalidin, a novel inhibitor of mammalian cell cycle, produced by a fungus isolated from a sea sediment. J. Antibiot. (Tokyo) 49: 216-219.
    CrossRef
  32. Kondoh M, Usui T, Mayumi T, Osada H. 1998. Effects of tryprostatin derivatives on microtubule assembly in vitro and in situ. J. Antibiot. (Tokyo) 51: 801-804.
    CrossRef
  33. Folkes A, Brown SD, Canne LE, Chan J, Engelhardt E, Epshteyn S, et al. 2002. Design, synthesis and in vitro evaluation of potent, novel, small molecule inhibitors of plasminogen activator inhibitor-1. Bioorg. Med. Chem. Lett. 12: 1063-1066.
    CrossRef
  34. Martins MB, Carvalho I. 2007. Diketopiperazines: biological activity and synthesis. Tetrahedron 63: 9923-9932.
    CrossRef
  35. McCleland K, Milne P, Lucieto F, Frost C, Brauns S, Venter M, et al. 2004. An investigation into the biological activity of the selected histidine-containing diketopiperazines cyclo (HisPhe) and cyclo (His-Tyr). J. Pharm. Pharmacol. 56: 1143-1153.
    Pubmed CrossRef
  36. Choi E, Park JS, Kim YJ, Jung JH, Lee J, Kwon H, et al. 2011. Apoptosis-inducing effect of diketopiperazine disulfides produced by Aspergillus sp. KMD 901 isolated from marine sediment on HCT116 colon cancer cell lines. J. Appl. Microbiol. 110: 304-313.
    Pubmed CrossRef