Coptisine-induced inhibition of Helicobacter pylori: elucidation of specific mechanisms by probing urease active site and its maturation process

References

• Atherton JC. The pathogenesis of Helicobacter pylori-induced gastro-duodenal diseases. Annu Rev Pathol 2006;1:63–96.
   PubMed Web of Science ®Google Scholar
• Franco AT, Johnston E, Krishna U, et al. Regulation of gastric carcinogenesis by Helicobacter pylori virulence factors. Cancer Res 2008;68:379–87.
   PubMed Web of Science ®Google Scholar
• Marshall BJ, Warren JR. Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet 1984;1:1311–15.
   PubMed Web of Science ®Google Scholar
• Cid TP, Fernández MC, Martinez SB, et al. Pathogenesis of Helicobacter pylori Infection. Helicobacter 2013;18:12–7.
   PubMed Web of Science ®Google Scholar
• Listed N. Schistosomes, liver flukes and Helicobacter pylori. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Lyon, 7–14 June 1994. IARC Monogr Eval Carcinog Risks Hum 1994;61:1–241.
   PubMedGoogle Scholar
• Glupczynski Y, Burette A. Drug therapy for Helicobacter pylori infection: problems and pitfalls. Am J Gastroenterol 1990;85:1545–51.
   PubMed Web of Science ®Google Scholar
• Marshall BJ. Treatment strategies for Helicobacter pylori infection. Gastroenterol Clin North Am 1993;22:183–98.
   PubMed Web of Science ®Google Scholar
• Adamek RJ, Suerbaum S, Pfaffenbach B, et al. Primary and acquired Helicobacter pylori resistance to clarithromycin, metronidazole, and amoxicillin-influence on treatment outcome. Am J Gastroenterol 1998;93:386–9.
   PubMed Web of Science ®Google Scholar
• Ng KM, Ferreyra JA, Higginbottom SK, et al. Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature 2013;502:96–9.
   PubMed Web of Science ®Google Scholar
• Babincova M, Schronerova K, Sourivong P. Antiulcer activity of water extract of Scoparia dulcis. Fitoterapia 2008;79:587–8.
   PubMed Web of Science ®Google Scholar
• Falcao HS, Mariath IR, Diniz MF, et al. Plants of the American continent with antiulcer activity. Phytomedicine 2008;15:132–46.
   PubMed Web of Science ®Google Scholar
• Shaikh RU, Dawane AA, Pawar RP, et al. Inhibition of Helicobacter pylori and its associate urease by labdane diterpenoids isolated from Andrographis paniculata. Phytother Res 2016;30:412–17.
   PubMed Web of Science ®Google Scholar
• Follmer C. Ureases as a target for the treatment of gastric and urinary infections. J Clin Pathol 2010;63:424–30.
   PubMed Web of Science ®Google Scholar
• Zeer-Wanklyn CJ, Zamble DB. Microbial nickel: cellular uptake and delivery to enzyme centers. Curr Opin Chem Biol 2017;37:80–8.
   PubMed Web of Science ®Google Scholar
• Zambelli B, Musiani F, Benini S, et al. Chemistry of Ni2+ in urease: sensing, trafficking, and catalysis. Acc Chem Res 2011;44:520–30.
   PubMed Web of Science ®Google Scholar
• Krajewska B, Zaborska W. Jack bean urease: the effect of active-site binding inhibitors on the reactivity of enzyme thiol groups. Bioorg Chem 2007;35:355–65.
   PubMed Web of Science ®Google Scholar
• Kumar S, Kayastha AM. Soybean (Glycine max) urease: significance of sulfhydryl groups in urea catalysis. Plant Physiol Bioch 2010;48:746–50.
   PubMed Web of Science ®Google Scholar
• Benini S, Rypniewski WR, Wilson KS, et al. The complex of Bacillus pasteurii urease with acetohydroxamate anion from X-ray data at 1.55 A resolution. J Biol Inorg Chem 2000;5:110–18.
   PubMed Web of Science ®Google Scholar
• Dixon NE, Blakeley RL, Zerner B. Jack bean urease (EC 3.5.1.5). III. The involvement of active-site nickel ion in inhibition by beta-mercaptoethanol, phosphoramidate, and fluoride. Can J Biochem 1980;58:481–8.
   PubMedGoogle Scholar
• Bano B, Kanwal, Khan KM, et al. Synthesis, in vitro urease inhibitory activity, and molecular docking studies of thiourea and urea derivatives. Bioorg Chem 2018;80:129–44.
   PubMed Web of Science ®Google Scholar
• Zaborska W, Krajewska B, Kot M, et al. Quinone-induced inhibition of urease: elucidation of its mechanisms by probing thiol groups of the enzyme. Bioorg Chem 2007;35:233–42.
   PubMed Web of Science ®Google Scholar
• Wu DW, Yu XD, Xie JH, et al. Inactivation of jack bean urease by scutellarin: elucidation of inhibitory efficacy, kinetics and mechanism. Fitoterapia 2013;91:60–7.
   PubMed Web of Science ®Google Scholar
• Carter EL, Flugga N, Boer JL, et al. Interplay of metal ions and urease. Metallomics 2009;1:207–21.
   PubMed Web of Science ®Google Scholar
• Soriano A, Hausinger RP. GTP-dependent activation of urease apoprotein in complex with the UreD, UreF, and UreG accessory proteins. Proc Natl Acad Sci USA 1999;96:11140–4.
   PubMed Web of Science ®Google Scholar
• Yang XM, Li HY, Lai TP, et al. UreE-UreG complex facilitates nickel transfer and preactivates GTPase of UreG in Helicobacter pylori. J Biol Chem 2015;290:12474–85.
   PubMed Web of Science ®Google Scholar
• Fong YH, Wong HC, Yuen MH, et al. Structure of UreG/UreF/UreH complex reveals how urease accessory proteins facilitate maturation of Helicobacter pylori urease. PLoS Biol 2013;11:e1001678.
   PubMed Web of Science ®Google Scholar
• Gasper R, Meyer S, Gotthardt K, et al. It takes two to tango: regulation of G proteins by dimerization. Nat Rev Mol Cell Biol 2009;10:423–9.
   PubMed Web of Science ®Google Scholar
• Ma F, Chen Y, Li J, et al. Screening test for anti-Helicobacter pylori activity of traditional Chinese herbal medicines. World J Gastroenterol 2010;16:5629–34.
   PubMed Web of Science ®Google Scholar
• Li CL, Xie JH, Chen XY, et al. Comparison of Helicobacter pylori urease inhibition by Rhizoma Coptidis, cortex phellodendri and berberine: mechanisms of interaction with the sulfhydryl group. Planta Med 2016;82:305–11.
   PubMed Web of Science ®Google Scholar
• Li B, Liu HR, Pan YQ, et al. Protective effects of total alkaloids from rhizoma Coptis chinensis on alcohol-induced gastric lesion in rats. China J Chin Mater Med 2006;31:51–4.
   Google Scholar
• Iizuka N, Oka M, Yamamoto K, et al. Identification of common or distinct genes related to antitumor activities of a medicinal herb and its major component by oligonucleotide microarray. Int J Cancer 2003;107:666–72.
   PubMed Web of Science ®Google Scholar
• Tan LH, Li CL, Chen HB, et al. Epiberberine, a natural protoberberine alkaloid, inhibits urease of Helicobacter pylori and jack bean: susceptibility and mechanism. Eur J Pharm Sci 2017;110:77–86.
   PubMed Web of Science ®Google Scholar
• Zhou JT, Li CL, Tan LH, et al. Inhibition of Helicobacter pylori and its associated urease by palmatine: investigation on the potential mechanism. PloS One 2017;12:e0168944.
   PubMed Web of Science ®Google Scholar
• Jang MH, Kim HY, Kang KS, et al. Hydroxyl radical scavenging activities of isoquinoline alkaloids isolated from Coptis chinensis. Arch Pharm Res 2009;32:341–5.
   PubMed Web of Science ®Google Scholar
• Yan D, Wei L, Xiao XH, et al. Microcalorimetric investigation of effect of berberine alkaloids from Coptis chinensis Franch on intestinal diagnostic flora growth. Sci Bull 2009; 54:369–73.
   Web of Science ®Google Scholar
• Tanabe H, Suzuki H, Nagatsu A, et al. Selective inhibition of vascular smooth muscle cell proliferation by coptisine isolated from Coptis rhizoma, one of the crude drugs composing Kampo medicines Unsei-in. Phytomedicine 2006;13:334–42.
   PubMed Web of Science ®Google Scholar
• Shin JS, Kim EI, Kai M, et al. Inhibition of dopamine biosynthesis by protoberberine alkaloids in PC12 cells. Neurochem Res 2000;25:363–8.
   PubMed Web of Science ®Google Scholar
• Zhao HQ, Zhou SD, Zhang MM, et al. An in vitro AchE inhibition assay combined with UF-HPLC-ESI-Q-TOF/MS approach for screening and characterizing of AchE inhibitors from roots of Coptis chinensis Franch. J Pharm Biomed Anal 2016;120:235–40.
   PubMed Web of Science ®Google Scholar
• Huang T, Xiao YB, Yi L, et al. Coptisine from Rhizoma Coptidis suppresses HCT-116 cells-related tumor growth in vitro and in vivo. Sci Rep 2017;7:38524.
   PubMed Web of Science ®Google Scholar
• Hirano H, Osawa E, Yamaoka Y, et al. Gastric-mucous membrane protection activity of coptisine derivatives. Biol Pharm Bull 2001;24:1277–81.
   PubMed Web of Science ®Google Scholar
• Tan LR, Inhibition efficacy of baicalin on jack bean urease [master's thesis]. Guangzhou: Guangzhou University of Chinese Medicine; 2013.
   Google Scholar
• Matsubara S, Shibata H, Ishikawa F, et al. Suppression of Helicobacter pylori-induced gastritis by green tea extract in Mongolian gerbils. Biochem Bioph Res 2003;310:715–9.
   PubMed Web of Science ®Google Scholar
• Xu YF, Lian DW, Chen YQ, et al. In vitro and in vivo antibacterial activities of patchouli alcohol, a natural-occurring tricyclic sesquiterpene against Helicobacter pylori infection. Antimicrob Agents Chemother 2017;61:e00122–17.
   PubMed Web of Science ®Google Scholar
• Mooney C, Munster DJ, Bagshaw PF, et al. Helicobacter pylori acid resistance. Lancet 1990;335:1232.
   PubMed Web of Science ®Google Scholar
• Weatherburn M. Phenol-hypochlorite reaction for determination of ammonia. Anal Chem 1967; 39:971–4.
   Web of Science ®Google Scholar
• Jadhav SG, Meshram RJ, Gond DS, et al. Inhibition of growth of Helicobacter pylori and its urease by coumarin derivatives: molecular docking analysis. J Pharm Res 2013;7:705–11.
   Google Scholar
• Morris GMGD, Halliday RS, Huey R, et al. Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function. J Comput Chem 1998;19:1639–62.
   Web of Science ®Google Scholar
• Baykov AA, Evtushenko OA, Avaeva SM. A malachite green procedure for orthophosphate determination and its use in alkaline phosphatase-based enzyme immunoassay. Anal Biochem 1988;171:266–70.
   PubMed Web of Science ®Google Scholar
• French GL. Bactericidal agents in the treatment of MRSA infections—the potential role of daptomycin. J Antimicrob Chemother 2006;58:1107–17.
   PubMed Web of Science ®Google Scholar
• Dixon NE, Hinds JA, Fihelly AK, et al. Jack bean urease (EC 3.5.1.5). IV. The molecular size and the mechanism of inhibition by hydroxamic acids. Spectrophotometric titration of enzymes with reversible inhibitors. Can J Biochem 1980;58:1323–34.
   PubMedGoogle Scholar
• Breitenbach JM, Hausinger RP. Proteus mirabilis urease. Partial purification and inhibition by boric acid and boronic acids. Biochem J 1988;250:917–20.
   PubMed Web of Science ®Google Scholar
• Mo ZZ, Wang XF, Zhang X, et al. Andrographolide sodium bisulphite-induced inactivation of urease: inhibitory potency, kinetics and mechanism. BMC Complement Altern Med 2015;15:238.
   PubMed Web of Science ®Google Scholar
• Krajewska B. Hydrogen peroxide-induced inactivation of urease: mechanism, kinetics and inhibitory potency. J Mol Catal B Enzym 2011;68:262–9.
   Google Scholar
• Morrison JF, Walsh CT. The behavior and significance of slow-binding enzyme inhibitors. Adv Enzymol Relat Areas Mol Biol 1988;61:201–301.
   PubMedGoogle Scholar
• Yan D, Jin C, Xiao XH, et al. Antimicrobial properties of berberines alkaloids in Coptis chinensis Franch by microcalorimetry. J Biochem Biophys Methods 2008;70:845–9.
   PubMedGoogle Scholar
• Yan D, Jin C, Xiao XH, et al. Investigation of the effect of berberines alkaloids in Coptis chinensis Franch on Bacillus shigae growth by microcalorimetry. Sci China Chem 2007;50:638–42.
   Web of Science ®Google Scholar
• Tanaka T, Metori K, Mineo S, et al. Inhibitory effects of berberine-type alkaloids on elastase. Planta Med 1993;59:200–2.
   PubMed Web of Science ®Google Scholar
• Qu Q, Qu J, Han L, et al. Inhibitory effects of phytochemicals on metabolic capabilities of CYP2D6(*)1 and CYP2D6(*)10 using cell-based models in vitro. Acta Pharmacol Sin 2014;35:685–96.
   PubMed Web of Science ®Google Scholar
• Yu D, Tao BB, Yang YY, et al. The IDO inhibitor coptisine ameliorates cognitive impairment in a mouse model of Alzheimer’s disease. J Alzheimers Dis 2015;43:291–302.
   PubMed Web of Science ®Google Scholar
• Jung HA, Yoon NY, Bae HJ, et al. Inhibitory activities of the alkaloids from Coptidis Rhizoma against aldose reductase. Arch Pharm Res 2008;31:1405–12.
   PubMed Web of Science ®Google Scholar
• Ro JS, Lee SS, Lee KS, et al. Inhibition of type A monoamine oxidase by coptisine in mouse brain. Life Sci 2001;70:639–45.
   PubMed Web of Science ®Google Scholar
• Tanaka T, Metori K, Mineo S, et al. Studies on collagenase inhibitors. IV. Inhibitors of bacterial collagenase in Coptidis rhizoma. Yakugaku Zasshi 1991;111:538–41.
   PubMed Web of Science ®Google Scholar
• Scott DR, Weeks D, Hong C, et al. The role of internal urease in acid resistance of Helicobacter pylori. Gastroenterology 1998;114:58–70.
   PubMed Web of Science ®Google Scholar
• Ha NC, Oh ST, Sung JY, et al. Supramolecular assembly and acid resistance of Helicobacter pylori urease. Nat Struct Biol 2001;8:505–9.
   PubMedGoogle Scholar
• Diaz-Sanchez AG, Alvarez-Parrilla E, Martinez-Martinez A, et al. Inhibition of urease by disulfiram, an FDA-approved thiol reagent used in humans. Molecules 2016;21:E1628.
   PubMed Web of Science ®Google Scholar
• Mao WJ, Lv PC, Shi L, et al. Synthesis, molecular docking and biological evaluation of metronidazole derivatives as potent Helicobacter pylori urease inhibitors. Bioorg Med Chem 2009;17:7531–6.
   PubMed Web of Science ®Google Scholar
• Xiao ZP, Peng ZY, Dong JJ, et al. Synthesis, molecular docking and kinetic properties of beta-hydroxy-beta-phenylpropionyl-hydroxamic acids as Helicobacter pylori urease inhibitors. Eur J Med Chem 2013;68:212–21.
   PubMed Web of Science ®Google Scholar
• Xia W, Li H, Sze KH, et al. Structure of a nickel chaperone, HypA, from Helicobacter pylori reveals two distinct metal binding sites. J Am Chem Soc 2009;131:10031–40.
   PubMed Web of Science ®Google Scholar
• Yang XM, Li HY, Cheng TF, et al. Nickel translocation between metallochaperones HypA and UreE in Helicobacter pylori. Metallomics 2014;6:1731–6.
   PubMed Web of Science ®Google Scholar
• Leipe DD, Wolf YI, Koonin EV, et al. Classification and evolution of P-loop GTPases and related ATPases. J Mol Biol 2002;317:41–72.
   PubMed Web of Science ®Google Scholar
• Hirano H, Tokuhira T, Yokoi T, et al. Gastric mucous membrane-protective principles of Coptidis Rhizoma. Nat Med 1997;51:516–18.
   Google Scholar
• He K, Ye XL, WU H, et al. The safety and anti-hypercholesterolemic effect of coptisine in Syrian golden hamsters. Lipids 2015;50:185–94.
   PubMed Web of Science ®Google Scholar
• Yi J, Ye XL, Wang DZ, et al. Safety evaluation of main alkaloids from Rhizoma Coptidis. J Ethnopharmacol 2013;145:303–10.
   PubMed Web of Science ®Google Scholar