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References

  1. Bartlett JG. 2008. Historical perspectives on studies of Clostridium difficile and C. difficile infection. Clin. Infect. Dis. 46: S4-S11.
    Pubmed CrossRef
  2. Black RE, Morris SS, Bryce J. 2003. Where and why are 10 million children dying every year? Lancet 361: 2226-2234.
    CrossRef
  3. Bode L. 2012. Human milk oligosaccharides: every baby needs a sugar mama. Glycobiology 22: 1147-1162.
    Pubmed PMC CrossRef
  4. Borgert CJ, Borgert SA, Findley KC. 2005. Synergism, antagonism, or additivity of dietary supplements: application of theory to case studies. Thromb. Res. 117: 123-132; discussion 145-151.
    Pubmed CrossRef
  5. Chaturvedi P, Warren CD, RuizPalacios GM, Pickering LK, Newburg DS. 1997. Milk oligosaccharide profiles by reversedphase HPLC of their perbenzoylated derivatives. Anal. Biochem. 251: 89-97.
    Pubmed CrossRef
  6. Coppa GV, Pierani P, Zampini L, Carloni I, Carlucci A, Gabrielli O. 1999. Oligosaccharides in human milk during different phases of lactation. Acta Paediatr. Suppl. 88: 89-94.
    Pubmed CrossRef
  7. De Leoz MLA, Kalanetra KM, Bokulich NA, Strum JS, Underwood MA, German JB, et al. 2015. Human milk glycomics and gut microbial genomics in infant feces show a correlation between human milk oligosaccharides and gut microbiota. J. Proteome Res. 14: 491-502.
    Pubmed PMC CrossRef
  8. Dingle T, Wee S, Mulvey GL, Greco A, Kitova EN, Sun JX, et al. 2008. Functional properties of the carboxy-terminal host cell-binding domains of the two toxins, TcdA and TcdB, expressed by Clostridium difficile. Glycobiology 18: 698-706.
    Pubmed CrossRef
  9. Duleba K, Pawlowska M, Wietlicka-Piszcz M. 2014. Clostridium difficile infection in children hospitalized due to diarrhea. Eur. J. Clin. Microbiol. Infect. Dis. 33: 201-209.
    Pubmed PMC CrossRef
  10. Egerer M, Giesemann T, Jank T, Satchell KJ, Aktories K. 2007. Auto-catalytic cleavage of Clostridium difficile toxins A and B depends on cysteine protease activity. J. Biol. Chem. 282: 25314-25321.
    Pubmed CrossRef
  11. El-Hawiet A, Kitova EN, Kitov PI, Eugenio L, Ng KK, Mulvey GL, et al. 2011. Binding of Clostridium difficile toxins to human milk oligosaccharides. Glycobiology 21: 1217-1227.
    Pubmed CrossRef
  12. El-Hawiet A, Kitova EN, Klassen JS. 2015. Recognition of human milk oligosaccharides by bacterial exotoxins. Glycobiology 25: 845-854.
    Pubmed CrossRef
  13. Greco A, Ho JG, Lin SJ, Palcic MM, Rupnik M, Ng KK. 2006. Carbohydrate recognition by Clostridium difficile toxin A. Nat. Struct. Mol. Biol. 13: 460-461.
    Pubmed CrossRef
  14. Idota T, Kawakami H, Murakami Y, Sugawara M. 1995. Inhibition of cholera toxin by human milk fractions and sialyllactose. Biosci. Biotechnol. Biochem. 59: 417-419.
    Pubmed CrossRef
  15. Jangi S, Lamont JT. 2010. Asymptomatic colonization by Clostridium difficile in infants: implications for disease in later life. J. Pediatr. Gastroenterol. Nutr. 51: 2-7.
    Pubmed CrossRef
  16. Kobata A. 2010. Structures and application of oligosaccharides in human milk. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 86: 1-17.
    PMC CrossRef
  17. Liu B, Newburg DS. 2013. Human milk glycoproteins protect infants against human pathogens. Breastfeed. Med. 8: 354-362.
    Pubmed PMC CrossRef
  18. Locascio RG, Ninonuevo MR, Freeman SL, Sela DA, Grimm R, Lebrilla CB, et al. 2007. Glycoprofiling of bifidobacterial consumption of human milk oligosaccharides demonstrates strain specific, preferential consumption of small chain glycans secreted in early human lactation. J. Agric. Food Chem. 55: 8914-8919.
    Pubmed CrossRef
  19. Mitty RD, LaMont JT. 1994. Clostridium difficile diarrhea:pathogenesis, epidemiology, and treatment. Gastroenterologist 2: 61-69.
    Pubmed
  20. Morris GM, Goodsell DS, Halliday RS, Huey R, Hart WE, Belew RK, Olson AJ. 1998. Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function. J. Comput. Chem. 19: 1639-1662.
    CrossRef
  21. Morrow AL, Ruiz-Palacios GM, Jiang X, Newburg DS. 2005. Human-milk glycans that inhibit pathogen binding protect breast-feeding infants against infectious diarrhea. J. Nutr. 135: 1304-1307.
    Pubmed
  22. Newburg DS. 2009. Neonatal protection by an innate immune system of human milk consisting of oligosaccharides and glycans. J. Anim. Sci. 87(13 Suppl): 26-34.
    Pubmed
  23. Nguyen TT, Woo HJ, Kang HK, Nguyen VD, Kim YM, Kim DW, et al. 2012. Flavonoid-mediated inhibition of SARS coronavirus 3C-like protease expressed in Pichia pastoris. Biotechnol. Lett. 34: 831-838.
    Pubmed CrossRef
  24. Nguyen TTH, Kang HK, Kim YM, Jang TS, Kim D. 2014. Inhibition effect of flavonoid compounds against neuraminidase expressed in Pichia pastoris. Biotechnol. Bioproc. Eng. 19: 70-75.
    CrossRef
  25. Nguyen TTH, Ryu HJ, Lee SH, Hwang S, Breton V, Rhee JH, Kim D. 2011. Virtual screening identification of novel severe acute respiratory syndrome 3C-like protease inhibitors and in vitro confirmation. Bioorg. Med. Chem. Lett. 21: 3088-3091.
    Pubmed CrossRef
  26. Ninonuevo MR, Park Y, Yin HF, Zhang JH, Ward RE, Clowers BH, et al. 2006. A strategy for annotating the human milk glycome. J. Agric. Food Chem. 54: 7471-7480.
    Pubmed CrossRef
  27. Ranalli A, Lucera L, Contento S. 2003. Antioxidizing potency of phenol compounds in olive oil mill wastewater. J. Agric. Food Chem. 51: 7636-7641.
    Pubmed CrossRef
  28. Roberts AK, Shone CC. 2001. Modification of surface histidine residues abolishes the cytotoxic activity of Clostridium difficile toxin A. Toxicon 39: 325-333.
    CrossRef
  29. Sauerborn M, Leukel P, von Eichel-Streiber C. 1997. The Cterminal ligand-binding domain of Clostridium difficile toxin A (TcdA) abrogates TcdA-specific binding to cells and prevents mouse lethality. FEMS Microbiol. Lett. 155: 45-54.
    Pubmed CrossRef
  30. Shang J, Piskarev VE, Xia M, Huang PW, Jiang X, Likhosherstov LM, et al. 2013. Identifying human milk glycans that inhibit norovirus binding using surface plasmon resonance. Glycobiology 23: 1491-1498.
    Pubmed PMC CrossRef
  31. Smilowitz JT, Lebrilla CB, Mills DA, German JB, Freeman SL. 2014. Breast milk oligosaccharides: structure-function relationships in the neonate. Annu. Rev. Nutr. 34: 143-169.
    Pubmed PMC CrossRef
  32. Thi THN, Moon YH, Ryu YB, Kim YM, Nam SH, Kim MS, et al. 2013. The influence of flavonoid compounds on the in vitro inhibition study of a human fibroblast collagenase catalytic domain expressed in E. coli. Enzyme Microb. Technol. 52: 26-31.
    Pubmed CrossRef
  33. Totten SM, Zivkovic AM, Wu S, Ngyuen U, Freeman SL, Ruhaak LR, et al. 2012. Comprehensive profiles of human milk oligosaccharides yield highly sensitive and specific markers for determining secretor status in lactating mothers. J. Proteome Res. 11: 6124-6133.
    CrossRef
  34. Urashima T, Asakuma S, Leo F, Fukuda K, Messer M, Oftedal OT. 2012. The predominance of type I oligosaccharides is a feature specific to human breast milk. Adv. Nutr. 3: 473s-482s.
    Pubmed PMC CrossRef
  35. Wallace AC, Laskowski RA, Thornton JM. 1995. Ligplot - a program to generate schematic diagrams of protein ligand interactions. Protein Eng. 8: 127-134.
    Pubmed CrossRef
  36. Wultanska D, Obuch-Woszczatynski P, Banaszkiewicz A, Radzikowski A, Pituch H, Mlynarczyk G. 2010. Prevalence of Clostridium difficile in the gastrointestinal tract of hospitalized children under two years of age. Med. Dosw. Mikrobiol. 62:77-84.
    Pubmed
  37. Zilberberg MD, Shorr AF, Kollef MH. 2008. Increase in adult Clostridium difficile-related hospitalizations and casefatality rate, United States, 2000-2005. Emerg. Infect. Dis. 14:929-931.
    Pubmed PMC CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2016; 26(4): 659-665

Published online April 28, 2016 https://doi.org/10.4014/jmb.1509.09034

Copyright © The Korean Society for Microbiology and Biotechnology.

Identification of Oligosaccharides in Human Milk Bound onto the Toxin A Carbohydrate Binding Site of Clostridium difficile

Thi Thanh Hanh Nguyen 1, Jong Woon Kim 2, Jun-Seong Park 3, Kyeong Hwan Hwang 3, Tae-Su Jang 1, Chun-Hyung Kim 1 and Doman Kim 1, 4*

1Institute of Food Industrialization, Institutes of Green Bio Science & Technology, Seoul National University, Pyeongchang 25354, Republic of Korea, 2Department of Obstetrics and Gynecology, Chonnam National University Medical School, Gwangju 61469, Republic of Korea, 3Amorepacific Corp. R&D Ctr., Gyeonggi-do 17074, Republic of Korea, 4Graduate School of International Agricultural Technology, Seoul National University, Pyeongchang 25354, Republic of Korea

Received: September 11, 2015; Accepted: December 23, 2015

Abstract

The oligosaccharides in human milk constitute a major innate immunological mechanism by
which breastfed infants gain protection against infectious diarrhea. Clostridium difficile is the
most important cause of nosocomial diarrhea, and the C-terminus of toxin A with its
carbohydrate binding site, TcdA-f2, demonstrates specific abolishment of cytotoxicity and
receptor binding activity upon diethylpyrocarbonate modification of the histidine residues in
TcdA. TcdA-f2 was cloned and expressed in E. coli BL21 (DE3). A human milk oligosaccharide
(HMO) mixture displayed binding with TcdA-f2 at 38.2 respond units (RU) at the
concentration of 20 μg/ml, whereas the eight purified HMOs showed binding with the
carbohydrate binding site of TcdA-f2 at 3.3 to 14 RU depending on their structures via a
surface plasma resonance biosensor. Among them, Lacto-N-fucopentaose V (LNFPV) and
Lacto-N-neohexaose (LNnH) demonstrated tight binding to TcdA-f2 with docking energy of
−9.48 kcal/mol and −12.81 kcal/mol, respectively. It displayed numerous hydrogen bonding
and hydrophobic interactions with amino acid residues of TcdA-f2.

Keywords: Clostridium difficile, human milk oligosaccharides, molecular docking, surface plasmon resonance, toxin A

References

  1. Bartlett JG. 2008. Historical perspectives on studies of Clostridium difficile and C. difficile infection. Clin. Infect. Dis. 46: S4-S11.
    Pubmed CrossRef
  2. Black RE, Morris SS, Bryce J. 2003. Where and why are 10 million children dying every year? Lancet 361: 2226-2234.
    CrossRef
  3. Bode L. 2012. Human milk oligosaccharides: every baby needs a sugar mama. Glycobiology 22: 1147-1162.
    Pubmed KoreaMed CrossRef
  4. Borgert CJ, Borgert SA, Findley KC. 2005. Synergism, antagonism, or additivity of dietary supplements: application of theory to case studies. Thromb. Res. 117: 123-132; discussion 145-151.
    Pubmed CrossRef
  5. Chaturvedi P, Warren CD, RuizPalacios GM, Pickering LK, Newburg DS. 1997. Milk oligosaccharide profiles by reversedphase HPLC of their perbenzoylated derivatives. Anal. Biochem. 251: 89-97.
    Pubmed CrossRef
  6. Coppa GV, Pierani P, Zampini L, Carloni I, Carlucci A, Gabrielli O. 1999. Oligosaccharides in human milk during different phases of lactation. Acta Paediatr. Suppl. 88: 89-94.
    Pubmed CrossRef
  7. De Leoz MLA, Kalanetra KM, Bokulich NA, Strum JS, Underwood MA, German JB, et al. 2015. Human milk glycomics and gut microbial genomics in infant feces show a correlation between human milk oligosaccharides and gut microbiota. J. Proteome Res. 14: 491-502.
    Pubmed KoreaMed CrossRef
  8. Dingle T, Wee S, Mulvey GL, Greco A, Kitova EN, Sun JX, et al. 2008. Functional properties of the carboxy-terminal host cell-binding domains of the two toxins, TcdA and TcdB, expressed by Clostridium difficile. Glycobiology 18: 698-706.
    Pubmed CrossRef
  9. Duleba K, Pawlowska M, Wietlicka-Piszcz M. 2014. Clostridium difficile infection in children hospitalized due to diarrhea. Eur. J. Clin. Microbiol. Infect. Dis. 33: 201-209.
    Pubmed KoreaMed CrossRef
  10. Egerer M, Giesemann T, Jank T, Satchell KJ, Aktories K. 2007. Auto-catalytic cleavage of Clostridium difficile toxins A and B depends on cysteine protease activity. J. Biol. Chem. 282: 25314-25321.
    Pubmed CrossRef
  11. El-Hawiet A, Kitova EN, Kitov PI, Eugenio L, Ng KK, Mulvey GL, et al. 2011. Binding of Clostridium difficile toxins to human milk oligosaccharides. Glycobiology 21: 1217-1227.
    Pubmed CrossRef
  12. El-Hawiet A, Kitova EN, Klassen JS. 2015. Recognition of human milk oligosaccharides by bacterial exotoxins. Glycobiology 25: 845-854.
    Pubmed CrossRef
  13. Greco A, Ho JG, Lin SJ, Palcic MM, Rupnik M, Ng KK. 2006. Carbohydrate recognition by Clostridium difficile toxin A. Nat. Struct. Mol. Biol. 13: 460-461.
    Pubmed CrossRef
  14. Idota T, Kawakami H, Murakami Y, Sugawara M. 1995. Inhibition of cholera toxin by human milk fractions and sialyllactose. Biosci. Biotechnol. Biochem. 59: 417-419.
    Pubmed CrossRef
  15. Jangi S, Lamont JT. 2010. Asymptomatic colonization by Clostridium difficile in infants: implications for disease in later life. J. Pediatr. Gastroenterol. Nutr. 51: 2-7.
    Pubmed CrossRef
  16. Kobata A. 2010. Structures and application of oligosaccharides in human milk. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 86: 1-17.
    KoreaMed CrossRef
  17. Liu B, Newburg DS. 2013. Human milk glycoproteins protect infants against human pathogens. Breastfeed. Med. 8: 354-362.
    Pubmed KoreaMed CrossRef
  18. Locascio RG, Ninonuevo MR, Freeman SL, Sela DA, Grimm R, Lebrilla CB, et al. 2007. Glycoprofiling of bifidobacterial consumption of human milk oligosaccharides demonstrates strain specific, preferential consumption of small chain glycans secreted in early human lactation. J. Agric. Food Chem. 55: 8914-8919.
    Pubmed CrossRef
  19. Mitty RD, LaMont JT. 1994. Clostridium difficile diarrhea:pathogenesis, epidemiology, and treatment. Gastroenterologist 2: 61-69.
    Pubmed
  20. Morris GM, Goodsell DS, Halliday RS, Huey R, Hart WE, Belew RK, Olson AJ. 1998. Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function. J. Comput. Chem. 19: 1639-1662.
    CrossRef
  21. Morrow AL, Ruiz-Palacios GM, Jiang X, Newburg DS. 2005. Human-milk glycans that inhibit pathogen binding protect breast-feeding infants against infectious diarrhea. J. Nutr. 135: 1304-1307.
    Pubmed
  22. Newburg DS. 2009. Neonatal protection by an innate immune system of human milk consisting of oligosaccharides and glycans. J. Anim. Sci. 87(13 Suppl): 26-34.
    Pubmed
  23. Nguyen TT, Woo HJ, Kang HK, Nguyen VD, Kim YM, Kim DW, et al. 2012. Flavonoid-mediated inhibition of SARS coronavirus 3C-like protease expressed in Pichia pastoris. Biotechnol. Lett. 34: 831-838.
    Pubmed CrossRef
  24. Nguyen TTH, Kang HK, Kim YM, Jang TS, Kim D. 2014. Inhibition effect of flavonoid compounds against neuraminidase expressed in Pichia pastoris. Biotechnol. Bioproc. Eng. 19: 70-75.
    CrossRef
  25. Nguyen TTH, Ryu HJ, Lee SH, Hwang S, Breton V, Rhee JH, Kim D. 2011. Virtual screening identification of novel severe acute respiratory syndrome 3C-like protease inhibitors and in vitro confirmation. Bioorg. Med. Chem. Lett. 21: 3088-3091.
    Pubmed CrossRef
  26. Ninonuevo MR, Park Y, Yin HF, Zhang JH, Ward RE, Clowers BH, et al. 2006. A strategy for annotating the human milk glycome. J. Agric. Food Chem. 54: 7471-7480.
    Pubmed CrossRef
  27. Ranalli A, Lucera L, Contento S. 2003. Antioxidizing potency of phenol compounds in olive oil mill wastewater. J. Agric. Food Chem. 51: 7636-7641.
    Pubmed CrossRef
  28. Roberts AK, Shone CC. 2001. Modification of surface histidine residues abolishes the cytotoxic activity of Clostridium difficile toxin A. Toxicon 39: 325-333.
    CrossRef
  29. Sauerborn M, Leukel P, von Eichel-Streiber C. 1997. The Cterminal ligand-binding domain of Clostridium difficile toxin A (TcdA) abrogates TcdA-specific binding to cells and prevents mouse lethality. FEMS Microbiol. Lett. 155: 45-54.
    Pubmed CrossRef
  30. Shang J, Piskarev VE, Xia M, Huang PW, Jiang X, Likhosherstov LM, et al. 2013. Identifying human milk glycans that inhibit norovirus binding using surface plasmon resonance. Glycobiology 23: 1491-1498.
    Pubmed KoreaMed CrossRef
  31. Smilowitz JT, Lebrilla CB, Mills DA, German JB, Freeman SL. 2014. Breast milk oligosaccharides: structure-function relationships in the neonate. Annu. Rev. Nutr. 34: 143-169.
    Pubmed KoreaMed CrossRef
  32. Thi THN, Moon YH, Ryu YB, Kim YM, Nam SH, Kim MS, et al. 2013. The influence of flavonoid compounds on the in vitro inhibition study of a human fibroblast collagenase catalytic domain expressed in E. coli. Enzyme Microb. Technol. 52: 26-31.
    Pubmed CrossRef
  33. Totten SM, Zivkovic AM, Wu S, Ngyuen U, Freeman SL, Ruhaak LR, et al. 2012. Comprehensive profiles of human milk oligosaccharides yield highly sensitive and specific markers for determining secretor status in lactating mothers. J. Proteome Res. 11: 6124-6133.
    CrossRef
  34. Urashima T, Asakuma S, Leo F, Fukuda K, Messer M, Oftedal OT. 2012. The predominance of type I oligosaccharides is a feature specific to human breast milk. Adv. Nutr. 3: 473s-482s.
    Pubmed KoreaMed CrossRef
  35. Wallace AC, Laskowski RA, Thornton JM. 1995. Ligplot - a program to generate schematic diagrams of protein ligand interactions. Protein Eng. 8: 127-134.
    Pubmed CrossRef
  36. Wultanska D, Obuch-Woszczatynski P, Banaszkiewicz A, Radzikowski A, Pituch H, Mlynarczyk G. 2010. Prevalence of Clostridium difficile in the gastrointestinal tract of hospitalized children under two years of age. Med. Dosw. Mikrobiol. 62:77-84.
    Pubmed
  37. Zilberberg MD, Shorr AF, Kollef MH. 2008. Increase in adult Clostridium difficile-related hospitalizations and casefatality rate, United States, 2000-2005. Emerg. Infect. Dis. 14:929-931.
    Pubmed KoreaMed CrossRef