Berberine-loaded targeted nanoparticles as specific Helicobacter pylori eradication therapy: in vitro and in vivo study

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References

• 1 Beil W, Kilian P. EPs 7630, an extract from Pelargonium sidoides roots inhibits adherence of Helicobacter pylori to gastric epithelial cells. Phytomedicine 14(6), 5–8 (2007).
  MedlineGoogle Scholar
• 2 Graham DY. Campylobacter pylori and peptic ulcer disease. Gastroenterology 96(2), 615–625 (1989).
  Medline CASGoogle Scholar
• 3 Hazell SL, Lee A, Brady L, Hennessy W. Campylobacter pyloridis and gastritis: association with intercellular spaces and adaptation to an environment of mucus as important factors in colonization of the gastric epithelium. J. Infect. Dis. 153(4), 658–663 (1986).
  Medline CASGoogle Scholar
• 4 Fedwick JP, Lapointe TK, Meddings JB, Sherman PM, Buret AG. Helicobacter pylori activates myosin light-chain kinase to disrupt claudin-4 and claudin-5 and increase epithelial permeability. Infect. Immun. 73(12), 7844–7852 (2005).
  Medline CASGoogle Scholar
• 5 Falk P, Roth KA, Borén T, Westblom TU, Gordon JI, Normark S. An in vitro adherence assay reveals that Helicobacter pylori exhibits cell lineage-specific tropism in the human gastric epithelium. Proc. Natl Acad. Sci. USA 90(5), 2035–2039 (1993). •• Reported that Helicobacter pylori  is capable of recognizing specific carbohydrate receptors such as fucose of mucosal epithelial cells.
  Medline CASGoogle Scholar
• 6 Lin YH, Tsai SC, Lai CH, Lee CH, He ZS, Tseng GC. Genipin-cross-linked fucose-chitosan/heparin nanoparticles for the eradication of Helicobacter pylori. Biomaterials 34(18), 4466–4479 (2013).
  Medline CASGoogle Scholar
• 7 Özden A, Seven G, Bektaş M. Effectiveness of different treatment regimens in Helicobacter pylori eradication: ten-year experience of a single institution. Turk. J. Gastroenterol. 21(3), 218–223 (2010).
  MedlineGoogle Scholar
• 8 Rangari VK, Mohammad GM, Jeelani S et al. Synthesis of Ag/CNT hybrid nanoparticles and fabrication of their nylon-6 polymer nanocomposite fibers for antimicrobial applications. Nanotechnology 21(9), 095102 (2010).
  MedlineGoogle Scholar
• 9 Guo CY, Wu YB, Liu HL, Wu JY, Zhong MZ. Clinical evaluation of four one-week triple therapy regimens in eradicating Helicobacter pylori infection. World J. Gastroenterol. 10(5), 747–749 (2004).•• Demonstrated that the high dosages of triple-therapy regimens may induce occurrence of unpleasant side effects.
  Medline CASGoogle Scholar
• 10 Koletzko S, Richy F, Bontems P et al. Prospective multicentre study on antibiotic resistance of Helicobacter pylori strains obtained from children living in Europe. Gut 55(12), 1711–1716 (2006).
  Medline CASGoogle Scholar
• 11 de Bortoli N, Leonardi G, Ciancia E et al. Helicobacter pylori eradication: a randomized prospective study of triple therapy versus triple therapy plus lactoferrin and probiotics. Am. J. Gastroenterol. 102(5), 951–956 (2007).
  Medline CASGoogle Scholar
• 12 Du P, Zhu S, Lü P. Antibacterial activity of 20 kinds of Chinese medicinal materials for Helicobacter pylori in vitro. Zhong Yao Cai. 24(3), 188–189 (2001).
  Medline CASGoogle Scholar
• 13 Yang P, Song DQ, Li YH et al. Synthesis and structure–activity relationships of berberine analogues as a novel class of low-density-lipoprotein receptor up-regulators. Bioorg. Med. Chem. Lett. 18(16), 4675–4677 (2008).
  Medline CASGoogle Scholar
• 14 Tang J, Feng Y, Tsao S, Wang N, Curtain R, Wang Y. Berberine and Coptidis rhizoma as novel antineoplastic agents: a review of traditional use and biomedical investigations. J. Ethnopharmacol. 126(1), 5–17 (2009).
  Medline CASGoogle Scholar
• 15 Amin AH, Subbaiah TV, Abbasi KM. Berberine sulfate: antimicrobial activity, bioassay, and mode of action. Can. J. Microbiol. 15(9), 1067–1076 (1969).
  Medline CASGoogle Scholar
• 16 Chung JG, Wu LT, Chang SH, Lo HH, Hsieh SE. Inhibitory actions of berberine on growth and arylamine N-acetyltransferase activity in strains of Helicobacter pylori from peptic ulcer patients. Int. J. Toxicol. 18(1), 35–40 (1999).•• Reported that berberine inhibited the proliferation of H. pylori.
  CASGoogle Scholar
• 17 Mahady GB, Pendland SL, Stoia A, Chadwick LR. In vitro susceptibility of Helicobacter pylori to isoquinoline alkaloids from Sanguinaria canadensis and Hydrastis canadensis. Phytother. Res. 17(3), 217–221 (2003).
  Medline CASGoogle Scholar
• 18 Wang YX, Zheng YM. Ionic mechanism responsible for prolongation of cardiac action-potential duration by berberine. J. Cardiovasc. Pharmacol. 30(2), 214–222 (1997).
  Medline CASGoogle Scholar
• 19 Panyam J, Labhasetwar V. Biodegradable nanoparticles for drug and gene delivery to cells and tissue. Adv. Drug Deliv. Rev. 55(3), 329–347 (2003).
  Medline CASGoogle Scholar
• 20 Khan MK, Minc LD, Nigavekar SS et al. Fabrication of {¹⁹⁸Au⁰} radioactive composite nanodevices and their use for nanobrachytherapy. Nanomedicine 4(1), 57–69 (2008).
  Medline CASGoogle Scholar
• 21 Pinto Reis C, Neufeld RJ, Ribeiro AJ, Veiga F. Nanoencapsulation II. Biomedical applications and current status of peptide and protein nanoparticulate delivery systems. Nanomedicine 2(2), 53–65 (2006).•• Reported that polymeric nanoparticles can be an oral delivery carrier for peptide drug.
  MedlineGoogle Scholar
• 22 Chang CH, Huang WY, Lai CH et al. Development of novel nanoparticles shelled with heparin for berberine delivery to treat Helicobacter pylori. Acta Biomater. 7(2), 593–603 (2011).
  Medline CASGoogle Scholar
• 23 Becker DJ, Lowe JB. Fucose: biosynthesis and biological function in mammals. Glycobiology 13(7), 41R–53R (2003).
  Medline CASGoogle Scholar
• 24 Mitchell E, Houles C, Sudakevitz D et al. Structural basis for oligosaccharide-mediated adhesion of Pseudomonas aeruginosa in the lungs of cystic fibrosis patients. Nat. Struct. Biol. 9(12), 918–921 (2002).
  Medline CASGoogle Scholar
• 25 Loris R, Tielker D, Jaeger KE, Wyns L. Structural basis of carbohydrate recognition by the lectin LecB from Pseudomonas aeruginosa. J. Mol. Biol. 331(4), 861–870 (2003).
  Medline CASGoogle Scholar
• 26 Thanou M, Verhoef JC, Junginger HE. Chitosan and its derivatives as intestinal absorption enhancers. Adv. Drug Deliv. Rev. 50(1), S91–S101 (2001).
  Medline CASGoogle Scholar
• 27 Mansouri S, Cuie Y, Winnik F et al. Characterization of folate-chitosan-DNA nanoparticles for gene therapy. Biomaterials 27(9), 2060–2065 (2006).
  Medline CASGoogle Scholar
• 28 Sameti M, Bohr G, Ravi Kumar MN et al. Stabilisation by freeze-drying of cationically modified silica nanoparticles for gene delivery. Int. J. Pharm. 266(1–2), 51–60 (2003).
  Medline CASGoogle Scholar
• 29 Elbein AD, Pan YT, Pastuszak I, Carroll D. New insights on trehalose: a multifunctional molecule. Glycobiology 13(4), 17R–27R (2003).
  Medline CASGoogle Scholar
• 30 Sashiwa H, Aiba S. Chemically modified chitin and chitosan as biomaterials. Prog. Polym. Sci. 29(9), 887–908 (2004).
  CASGoogle Scholar
• 31 Donati I, Stredanska S, Silvestrini G et al. The aggregation of pig articular chondrocyte and synthesis of extracellular matrix by a lactose-modified chitosan. Biomaterials 26(9), 987–998 (2005).
  Medline CASGoogle Scholar
• 32 Wang SD, Song BS, Li K. Determination of berberine in decocted liquid from shenshu granules with water by reversed-phase liquid chromatography. Se Pu. 18(3), 261–262 (2000).
  Medline CASGoogle Scholar
• 33 Richards CL, Buchholz BJ, Ford TE, Broadaway SC, Pyle BH, Camper AK. Optimizing the growth of stressed Helicobacter pylori. J. Microbiol. Methods 84(2), 174–182 (2011).
  Medline CASGoogle Scholar
• 34 Lin YH, Lin JH, Peng SF et al. Multifunctional gentamicin supplementation of poly (γ-glutamic acid)-based hydrogels for wound dressing application. J. Appl. Polym. Sci. 120(2), 1057–1068 (2011).
  CASGoogle Scholar
• 35 Huang WY, Yeh CL, Lin JH, Yang JS, Ko TH, Lin YH. Development of fibroblast culture in three-dimensional activated carbon fiber-based scaffold for wound healing. J. Mater. Sci. Mater. Med. 23(6), 1465–1478 (2012).
  Medline CASGoogle Scholar
• 36 Lin YH, Chiou SF, Lai CH et al. Formulation and evaluation of water-in-oil amoxicillin-loaded nanoemulsions using for Helicobacter pylori eradication. Process Biochem. 47(10), 1469–1478 (2012).
  CASGoogle Scholar
• 37 Sogias IA, Williams AC, Khutoryanskiy VV. Why is chitosan mucoadhesive? Biomacromolecules 9(7), 1837–1842 (2008).
  Medline CASGoogle Scholar
• 38 Ramesan RM, Sharma CP. Modification of chitosan nanoparticles for improved gene delivery. Nanomedicine (Lond). 7(1), 5–8 (2012).•• Reported that chitosan has adhesive properties, which can prolong interaction between the delivered drug and the cell membrane.
  CASGoogle Scholar
• 39 Madrid JF, Leis O, Díaz-Flores L, Sáez FJ, Hernández F. Lectin-gold localization of fucose residues in human gastric mucosa. J. Histochem. Cytochem. 46(11), 1311–1320 (1998).
  Medline CASGoogle Scholar
• 40 Moriwaki K, Miyoshi E. Fucosylation and gastrointestinal cancer. World J. Hepatol. 2(4), 151–161 (2010).
  MedlineGoogle Scholar
• 41 Kim YS, Kim YW, Siddiqui B, Tsao D. Membrane-associated, fucose-containing glycoproteins and glycolipids of cultured epithelial cells from human colonic adenocarcinoma and fetal intestine. Eur. J. Cancer Clin. Oncol. 18(12), 1329–1336 (1982).
  Medline CASGoogle Scholar
• 42 Wen S, Moss SF. Helicobacter pylori virulence factors in gastric carcinogenesis. Cancer Lett. 282(1), 1–8 (2009).
  Medline CASGoogle Scholar
• 43 Wroblewski LE, Peek RM Jr, Wilson KT. Helicobacter pylori and gastric cancer: factors that modulate disease risk. Clin. Microbiol. Rev. 23(4), 713–739 (2010).
  Medline CASGoogle Scholar
• 44 Khanvilkar K, Donovan MD, Flanagan DR. Drug transfer through mucus. Adv. Drug Deliv. Rev. 48(2–3), 173–193 (2001).•• Reports that the mucous layer can afford protection but can also pose a potential barrier to drug absorption. The particles with nanosize have translocation permeability through gastrointestinal mucin property.
  Medline CASGoogle Scholar
• 45 Lehr CM, Bouwstra JA, Schacht EH, Junginger HE. In vitro evaluation of mucoadhesive properties of chitosan and some other natural polymers. Int. J. Pharm. 78(1–3), 43–48 (1992).
  CASGoogle Scholar
• 46 Miyazaki S, Nakayama A, Oda M, Takada M, Attwood D. Chitosan and sodium alginate based bioadhesive tablets for intraoral drug delivery. Biol. Pharm. Bull. 17(5), 745–747 (1994).
  Medline CASGoogle Scholar
• 47 Amiji MM. Tetracycline-containing chitosan microspheres for local treatment of Helicobacter pylori infection. Cellulose 14(1), 3–14 (2007).
  CASGoogle Scholar
• 48 Yang P, Song DQ, Li YH et al. Synthesis and structure–activity relationships of berberine analogues as a novel class of low-density-lipoprotein receptor up-regulators. Bioorg. Med. Chem. Lett. 18(16), 4675–4677 (2008).
  Medline CASGoogle Scholar
• 49 Casu B, Gennaro U. A conductimetric method for the determination of sulphate and carboxyl groups in heparin and other mucopolysaccharides. Carbohydr. Res. 39(1), 168–176 (1975).
  Medline CASGoogle Scholar
• 50 Li Y, Wang HY, Cho CH. Association of heparin with basic fibroblast growth factor, epidermal growth factor, and constitutive nitric oxide synthase on healing of gastric ulcer in rats. J. Pharmacol. Exp. Ther. 290(2), 789–796 (1999).
  Medline CASGoogle Scholar
• 51 Konturek PC, Konturek SJ, Brzozowski T, Ernst H. Epidermal growth factor and transforming growth factor-alpha: role in protection and healing of gastric mucosal lesions. Eur. J. Gastroenterol. Hepatol. 7(10), 933–937 (1995).
  Medline CASGoogle Scholar
• 52 Hall AJ, Tripp M, Howell T, Darland G, Bland JS, Babish JG. Gastric mucosal cell model for estimating relative gastrointestinal toxicity of non-steroidal anti-inflammatory drugs. Prostaglandins Leukot. Essent. Fatty Acids 75(1), 9–17 (2006).
  Medline CASGoogle Scholar
• 53 van der Lubben IM, Verhoef JC, Borchard G, Junginger HE. Chitosan and its derivatives in mucosal drug and vaccine delivery. Eur. J. Pharm. Sci. 14(3), 201–207 (2001).
  Medline CASGoogle Scholar