Antiadhesive properties of arabinogalactan protein from ribes nigrum seeds against bacterial adhesion of helicobacter pylori

Molecules

Volumn 19, Issue 3, 2014, Pages 3696-3717

  Messing, Jutta ^a   Niehues, Michael ^a   Shevtsova, Anna ^b   Borén, Thomas ^b   Hensel, Andreas ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b UMEÅ UNIVERSITY   (Sweden)

Author keywords

Adhesion; Antiadhesion; Arabinogalactan protein; BabA; Fibronectin; Helicobacter pylori; Ribes nigrum L.; Virulence factors

Indexed keywords

ADHESIN; ARABINOGALACTAN PROTEINS; CARBOHYDRATE; MUCOPROTEIN; VEGETABLE PROTEIN;

ARTICLE; BACTERIUM ADHERENCE; CELL LINE; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; HELICOBACTER PYLORI; HUMAN; ISOLATION AND PURIFICATION; MOLECULAR WEIGHT; PLANT SEED; RIBES;

ADHESINS, BACTERIAL; BACTERIAL ADHESION; CARBOHYDRATES; CELL LINE; GENE EXPRESSION REGULATION, BACTERIAL; HELICOBACTER PYLORI; HUMANS; MOLECULAR STRUCTURE; MOLECULAR WEIGHT; MUCOPROTEINS; PLANT PROTEINS; RIBES; SEEDS;

EID: 84896913414     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules19033696     Document Type: Article

References (57)

1. List, P.H.; Horhammer, L. Ribes. In Hagers Handbuch der Pharmazeutischen Praxis, 4th ed.; Hansel, R., Keller, K., Rimpler, H., Schneider, G., Eds.; Springer: Berlin/Heidelberg, Germany; New York, NY, USA, 1979; Volume 6, pp. 132-135.
2. Traitler, H.; Winter, H.; Richli, U.; Ingenbleek, Y. Characterization of -linolenic acid in Ribes seeds. Lipids 1984, 12, 923-928.
3. Bakowska-Barczak, A.M.; Schieber, A.; Kolodziejczyk, P. Characterization of Canadian black currant (Ribes nigrum L.) seed oils and residues. J. Agric. Food Chem. 2009, 24, 11528-11536.
4. Zippel, J.; Deters, A.; Pappai, D.; Hensel, A. A high molecular arabinogalactan from Ribes nigrum L.: Influence on cell physiology of human skin fibroblasts and keratinocytes and internalization into cells via endosomal transport. Carbohydr. Res. 2009, 344, 1001-1008.
5. Lengsfeld, C.; Deters, A.; Faller, G.; Hensel, A. High molecular weight polysaccharides from black currant seed inhibit adhesion of Helicobacter pylori to human gastric mucosa. Planta Med. 2004, 70, 620-626.
6. Bendaoud, M.; Vinogradov, E.; Balashova, N.V.; Kadouri, D.E.; Kachlany, S.C.; Kapplan, J.B. Broad-Spectrum Biofilm Inhibition by Kingella kingae exopolysaccharide. J. Bacteriol. 2011, 193, 3879-3886.
7. Mysore, J.V.; Wigginton, T.; Simon, P.M.; Zopf, D.; Heman-Ackah, L.M.; Dubois, A. Treatment of Helicobacter pylori infection in rhesus monkeys using a novel antiadhesion compound. Gastroenterology 1999, 117, 1316-1325.
8. Parente, F.; Cucino, C.; Anderloni, A.; Grandinetti, G.; Bianchi Porro, G. Treatment of Helicobacter pylori infection using a novel antiadhesion compound (3'sialyllactose sodium salt). A double blind, placebo-controlled clinical study. Helicobacter 2003, 8, 252-156.
9. Niehues, A.; Euler , M.; Georgi, G.; Mank, M.; Stahl, B.; Hensel, A. Peptides from Pisum sativum L. enzymatic protein digest with anti-Adhesive activity against Helicobacter pylori: Structure-Activity and inhibitory activity against BabA, SabA, HpaA and a fibronectin-binding adhesion. Mol. Nutr. Food Res. 2010, 54, 1-11.
10. Wittschier, N.; Faller, G.; Hensel, A. An extract of Pelargonium sidoides (EPs 7630) inhibits in situ adhesion of Helicobacter pylori to human stomach. Phytomedicine 2007, 14, 285-288.
11. Shmuely, H.; Yahav, J.; Samra, Z.; Niv, Y.; Sharon, N.; Weiss, E.; Athamna, A.; Tabak, M.; Ofek, I. Susceptibility of Helicobacter pylori isolates to the antiadhesion activity of a high-molecular-weight constituent of cranberry. Diagn. Microbiol. Infect. Dis. 2004, 50, 231-235.
12. Hofmann, T.; Deters, A.; Muller, G.; Stark, T.; Wittschier, N.; Hensel, A. Occurence of N-Phenylpropenoyl-L-Amino acids in different herbal drugs and influence on human keratinocytes, human liver cells and against adhesion of H. pylori to human stomach. Planta Med. 2007, 73, 142-150.
13. Wittschier, N.; Faller, G.; Hensel, A. Aqueous extracts and polysaccharides from Liquorice roots (Glycyrrhiza glabra L.) inhibit adhesion of Helicobacter pylori to human gastric mucosa. J. Ethnopharmacol. 2009, 125, 218-223.
14. Lengsfeld, C.; Titgemeyer, F.; Faller, G.; Hensel, A. Glycosylated compounds from Okra inhibit adhesion of Helicobacter pylori to human gastric mucosa. J. Agric. Food Chem. 2004, 52, 1495-1503.
15. Messing, J.; Thole, C.; Niehues, M.; Shevtsova, A.; Glocker, E.; Borén, T.; Hensel, A. Antiadhesive properties of Abelmoschus esculentus (Okra) immature fruit extract against Helicobacter pylori ddhesion. PLoS One 2014, 9, e84836.
16. Ilver, D.; Arnqvist, A.; Ogren, J.; Frick, I.M.; Kersulyte, D.; Incecik, E.T.; Berg, D.E.; Covacci, A.; Engstrand, L.; Borén, T. Helicobacter pylori adhesin binding fucosylated histo-blood group antigens revealed by retagging. Science 1998, 279, 373-377.
17. Khamri, W.; Moran, A.P.; Worku, M.L.; Karimm, Q.N.; Walker, M.M.; Annuk, H.; Ferris, J.A.; Appelmelk, B.J.; Eggleton, P.; Reid, K.B.; et al. Variations in Helicobacter pylori lipopolysaccharide to evade the innate immune component surfactant protein D. Infect. Immun. 2005, 73, 7677-7686.
18. Van De Bovenkamp, J.H.; Mahdavi, J.; Korteland-Van Male, A.M.; Buller, H.A.; Einerhand, A.W. The MUC5AC glycoprotein is the primary receptor for Helicobacter pylori in the human stomach. Helicobacter 2003, 8, 521-532.
19. Mahdavi, J.; Hurtig, M.; Olfat, F.O.; Forsberg, L.; Roche, N.; Angstrom, J.; Larsson, T.; Teneberg, S.; Karlsson, K.A.; Altraja, S.; et al. Helicobacter pylori SabA adhesin in persistent infection and chronic inflammation. Science 2002, 297, 573-578.
20. Aspholm, M.; Olfat, F.O.; Nordén, J.; Sondén, B.; Lundberg, C.; Sjostrom, R.; Altraja, S.; Odenbreit, S.; Haas, R.; Wadstrom, T.; et al. SabA is the Helicobacter pylori hemagglutinin and is polymorphic in binding to sialylated glycans. PLoS Pathog. 2006, 2, e110.
21. Simon, P.M.; Goode, P.L.; Mobasseri, A.; Zopf, D. Inhibition of Helicobacter pylori binding to gastrointestinal epithelial cells by sialic acid-containing oligosaccharides. Infect. Immun. 1997, 65, 750-757.
22. Odenbreit, S.; Faller, G.; Haas, R. Role of the alpAB proteins and lipopolysaccharide in adheion of Helicobacter pylori to human gastric tissue. Int. J. Med. Microbiol. 2002, 292, 247-256.
23. Odenbreit, S.; Till, M.; Hofreuter, M.D.; HFaller, G.; Haas, R. Genetic and functional characterisation of the alpAB gene locus essential for bacterial adherence of Helicobacter pylori to human gastric tissue. Mol. Microbiol. 1999, 31, 1537-1548.
24. Yamaoka, Y.; Alm, R.A. Helicobacter outer membrane proteins. In Helicobacter pylori: Molecular Genetics and Cellular Biology Helicobacter pylori Outer Membrane Proteins, 1st ed.; Yamaoka, Y., Ed.; Caister Academic Press: Norfolk, UK, 2008; pp. 37-60.
25. Lengsfeld, C.; Faller, G.; Hensel, A. Okra polysaccharides inhibit adhesion of Campylobacter jejuni to mucosa isolated from poultry in vitro but not in vivo. Anim. Feed Sci. Technol. 2007, 135, 113-125.
26. Valkonen, K.H.; Ringner, M.; Ljungh, A.; Wadstrom, T. High-Affinity binding of laminin by Helicobacter pylori: Evidence for a lectin-like interaction. FEMS 1993, 7, 29-38.
27. Valkonen, K.H.; Wadstrom, T.; Moran, A.P. Identification of the N-Acetylneuraminyllactosespecific laminin-binding protein of Helicobacter pylori. Infect. Immun. 1997, 65, 916-923.
28. Selgrad, M.; Malfertheiner, P. Treatment of Helicobacter pylori. Cur. Opin. Gastroenterol. 2011, 27, 565-570.
29. Van Holst, G.; Clarke, A.E. Quantification of arabinogalactan-protein in plant extracts by single radial gel diffusion. Anal. Biochem. 1995, 148, 446-450.
30. Gilbert, R.G.; Hess, M.; Jenkins, A.D.; Jones, R.G. Dispersity in polymer science (IUPAC recommendations 2009). Pure Appl. Chem. 2009, 81, 351-353.
31. Blumenkranz, N.; Asboe-Hansen, G. New method for quantitative determination of uronic acids. Anal. Biochem. 1973, 54, 484-489.
32. Sommer-Knudsen, J.; Clarke, A.E; Bacic, A. A galactose-rich, cell-wall glycoprotein from styles of Nicotiana alata. Plant J. 1996, 9, 71-83.
33. Sehlbach, M.; Konig, S.; Mormann, M.; Sendker, J.D.; Hensel, A. The arabinogalactan protein cluster isolated from Jatropha curcas L seed embryo contains fasciclin, xylogen and LysM proteins. Carbohydr. Polym. 2013, 98, 522-531.
34. Hermann, A.; Konig, S.; Lechtenberg, M.; Sehlbach, M.; Vakrushev, S.; Peter-Katalinic, J.; Hensel, A. Proteoglycans from Boswellia serrata Roxb. And B. carteri Birdw. and identification of a proteolytic plant basic secretory protein. Glycobiology 2012, 22, 1424-1439.
35. Serpe, M.D.; Nothnagel, E.A. Fractionation and structural characterization of arabinogalactanproteins from the cell wall of rose cells. Plant Physiol. 1995, 109, 1007-1016.
36. Gleeson, P.A.; McNamara, M.; Wettenhall, R.E.H.; Stone, B.A.; Fincher, G.B. Characterization of the hydroxyproline-rich protein core of an arabinogalactan-protein secreted from suspension-cultured Lolium multiflorum (Italian ryegrass) endosperm cells. Biochem. J. 1989, 264, 857-862.
37. Hunter, W.M.; Greenwood, F.C. Preparation of iodine-131 labelled human growth hormone of high specific activity. Nature 1962, 194, 495-496.
38. Aspholm-Hurtig, M.; Dailide, G.; Lahmann, M.; Kalia, A; Ilver, D.; Roche, N.; Vikstrom, S.; Sjostrom, R.; Lindén, S.; Backstrom, A.; et al. Functional adaptation of BabA, the H. pylori ABO blood group antigen binding adhesin. Science 2004, 305, 519-522.
39. Sun, H.Y.; Lin, S.W.; Ko, T.P.; Pan, J.F.; Liu, C.L.; Lin, C.L.; Wang, A.H.; Lin, C.H. Structure and mechanism of Helicobacter pylori fucosyltransferase. A basis for lipopolysaccharide variation and inhibitor design. J. Biol. Chem. 2007, 282, 9973-9982.
40. Stingl, K.; de Reuse, H. Staying alive overdosed: How does Helicobacter pylori control urease activity? Int. J. Med. Microbiol. 2005, 295, 305-315.
41. Kieliszewski, M.J.; Lamport, D.T.A.; Tan, L.; Cannon, M.C. Hydroxyproline-rich glycoproteins: Form and Function. Annu. Plant Rev.: Plant Polysacch. 2011, 41, 321-342.
42. Gisbert, J.P. The recurrence of Helicobacter pylori infection: Incidence and variables influencing it. A critical review. Am. J. Gastrenterol. 2005, 100, 2083-2099.
43. Niv, Y. H. pylori recurrence after successful eradication. World J. Gastroenterol. 2008, 14, 1477-1478.
44. Niehues, M.; Georgi, G.; Euler, M.; Mank, M.; Klapperich, M.; Hensel, A. Pea protein peptides with anti Helicobacter pylori activity. WO2011122937 A1, 6 October 2011.
45. Rasko, D.A.; Sperandion, V. Anti-virulence strategies to combat bacteria-mediated disease. Nat. Rev. 2010, 4, 117-127.
46. Hensel, A. Antiadhesive polysaccharides. University of Munster, Munster, Germany, 2012, unpublished results
47. Niehues, M.; Stark, T.; Keller, D.; Hofmann, T.; Hensel, A. Antiadhesion as a functional concept: Antiadhesive N-phenylpropenoyl-L-Amino acid amides as specific inhibitors of the Helicobacter pylori BabA outer membrane protein: Structure-Activity relationship and functional aspects. Mol. Nutr. Food Res. 2011, 55, 1104-1117.
48. Skoog, E.M.; Sjoling, A.; Navabi, N.; Holgersson, J.; Lundin, S.B.; Lindén, S.K. Human gastric mucins differently regulate Helicobacter pylori proliferation, gene expression and interactions with host cells. PLoS One 2012, 7, e36378.
49. Radziejewska, I.; Leszczynska, K.; Borzym-Kluczyk, M. Influence of monoclonal anti-Lewis b, anti-H type 1, and anti-sialyl Lewis x antibodies on binding of Helicobacter pylori to MUC1 mucin. Mol. Cell Biochem. 2014, 385, 249-255.
50. Kalia, V.C.; Wood, T.K.; Kumar, P. Evolution of Resistance to Quorum-Sensing Inhibitors. Microb. Ecol. 2014, In press.
51. Mellbye, B.; Schuster, M. The sociomicrobiology of antivirulence drug resistance: A proof of concept. mBio 2011, 2, e00131-11.
52. Maeda, T.; Garcia-Contreras, R.; Pu, M.; Sheng, L.; Garcia, L.R.; Tomas, M.; Wood, T.K.; Quorum quenching quandary: Resistance to antivirulence compounds. ISME J. 2012, 6, 493-501.
53. Sharon, N. Safe as mother's milk: Carbohydrates as future anti-Adhesion drugs for bacterial diseases. Glycoconjugate J. 2000, 17, 659-664.
54. Ilver, D.; Arnqvist, A.; Ogren, J.; Frick, I.; Kersulyte, D. Helicobacter pylori adhesin binding fucosylated histo-blood group antigens revealed by retagging. Science 1989, 279, 5349-373.
55. Dubois, A.; Berg, D.E.; Incecik, E.T.; Fiala, N.; Heman-Ackah, L.M.; Del Valle, J.; Yang, M.; Wirth, H.P.; Perez-Perez, G.I.; Blaser, M.J. Host specificity of Helicobacter pylori strains and host responses in experimentally challenged nonhuman primates. Gastroenterology 1999, 116, 90-96.
56. Linden, S.; Nordman, H.; Hedenbro, J.; Hurtig, M.; Boren, T.; Carlstedt, I. Strain- and blood group-dependent binding of Helicobacter pylori to human gastric MUC5AC glycoforms. Gastroenterology 2002, 6, 1923-1930.
57. Motulsky, H.; Christopoulos, A. Fitting Models TO Biological Data Using Linear and Nonlinear Regression: A Practical Guide To Curve Fitting; Oxford: New York, NY, USA, 2004; pp. 1-10.