Outer membrane protein Q,Helicobacter pylori,Anti-adhesion,Abelmoschus esculentus,Capsicum annum,Curcuma longa," /> Outer membrane protein Q,Helicobacter pylori,Anti-adhesion,Abelmoschus esculentus,Capsicum annum,Curcuma longa,"/> <em>Helicobacter pylori</em> outer membrane protein Q genotypes and their susceptibility to anti-adhesive phytotherapeutic agents
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Journal of Integrative Medicine ›› 2017, Vol. 15 ›› Issue (5): 398-406.doi: 10.1016/S2095-4964(17)60359-5

• Research Article • Previous Articles     Next Articles

Helicobacter pylori outer membrane protein Q genotypes and their susceptibility to anti-adhesive phytotherapeutic agents

Javed Yakooba,b, Zaigham Abbasa, Malik Hassan Mehmoodb, Kanwal Tariqa, Saima Azhar Saleema, Safia Awana, Abdul Malikb, Saeed Hamida, Rustam Khana, Wasim Jafria   

  1. a Department of Medicine, Aga Khan University, Karachi 74800, Pakistan
    b Department of Biological Biomedical Sciences, Aga Khan University, Karachi 74800, Pakistan
  • Received:2017-02-15 Accepted:2017-05-24 Online:2017-09-15 Published:2017-09-15
  • Contact: Javed Yakoob; E-mail: javed.yakoob@aku.edu


Helicobacter pylori is a Gram-negative organism. Its outer membrane protein Q (HopQ) mediates host-pathogen interactions; HopQ genotypes 1 and 2 are found associating with gastroduodenal pathologies. The authors measured the anti-adhesion effects of the extracts of Abelmoschus esculentus, Zingiber officinale, Trachyspermum ammi, Glycyrrhiza glabra, Curcuma longa and Capsicum annum against HopQ genotypes and H. pylori cytotoxin-associated gene A (CagA).


DNA was extracted by polymerase chain reaction of the HopQ genotypes (i.e., type 1, type 2 and CagA) from 115 H. pylori strains. The effect of the extracts from selected dietary ingredients was determined using a gastric adenocarcinoma cell line and a quantitative DNA fragmentation assay. The anti-adhesive effect of these extracts on H. pylori was tested using an anti-adhesion analysis.


C. annum, C. longa and A. esculentus showed prominent anti-adhesion effects with resultant values of 17.3% ± 2.9%, 14.6% ± 3.7%, 13.8% ± 3.6%, respectively, against HopQ type 1 and 13.1% ± 1.7%, 12.1% ± 2%, 11.1% ± 1.6%, respectively, against HopQ type 2. C. longa (93%), C. annum (89%) and A. esculentus (75%) had better anti-adhesive activity against H. pylori with HopQ type 1 compared to HopQ type 2 with respective values of 70%, 64% and 51%. Extracts of C. annum (14.7% ± 4.1%), A. esculentus (12.3% ± 4.1%) and Z. officinale (8.4% ± 2.8%) had an anti-adhesion effect against CagA-positive H. pylori strains compared to CagA-negative strains.


The anti-adhesion properties of the tested phytotherapeutic dietary ingredients were varied with HopQ genotypes. HopQ type 1 was found to be more sensitive to extracts of C. annum, C. longa and A. esculentus compared to the HopQ type 2 genotype.

Key words: Outer membrane protein Q, Helicobacter pylori, Anti-adhesion, Abelmoschus esculentus, Capsicum annum, Curcuma longa

1 Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM.Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008.Int J Cancer. 2010; 127(12): 2893-2917.
2 Shiotani A, Lu H, Dore MP, Graham DY.TreatingHelicobacter pylori effectively while minimizing misuse of antibiotics. Cleve Clin J Med. 2017; 84(4): 310-318.
3 Tegtmeyer N, Wessler S, Backert S.Role of the cagpathogenicity island encoded type IV secretion system inHelicobacter pylori pathogenesis. FEBS J. 2011; 278(8): 1190-1202.
4 Palframan SL, Kwok T, Gabriel K.Vacuolating cytotoxin A (VacA), a key toxin forHelicobacter pylori pathogenesis. Front Cell Infect Microbiol. 2012; 2: 92.
5 Skoog EC, Padra M, Åberg A, Gideonsson P, Obi I, Quintana-Hayashi MP, Arnqvist A, Lindén SK.BabA dependent binding ofHelicobacter pylori to human gastric mucins causes aggregation that inhibits proliferation and is regulated via ArsS. Sci Rep. 2017; 7: 40656.
6 Harvey VC, Acio CR, Bredehoft AK, Zhu L, Hallinger DR, Quinlivan-Repasi V, Harvey SE, Forsyth MH.Repetitive sequence variations in the promoter region of the adhesin-encoding gene sabA ofHelicobacter pylori affect transcription. J Bacteriol. 2014; 196(19): 3421-3429.
7 Zhang J, Qian J, Zhang X, Zou Q.Outer membrane inflammatory protein A, a new virulence factor involved in the pathogenesis ofHelicobacter pylori. Mol Biol Rep. 2014; 41(12): 7807-7814.
8 Lu H, Wu JY, Beswick EJ, Ohno T, Odenbreit S, Haas R, Reyes VE, Kita M, Graham DY, Yamaoka Y.Functional and intracellular signaling differences associated with theHelicobacter pylori AlpAB adhesin from Western and East Asian strains. J Biol Chem. 2007; 282(9): 6242-6254.
9 Cao P, Cover TL.Two different families ofhopQ alleles in Helicobacter pylori. J Clin Microbiol. 2002; 40(12): 4504-4511.
10 Oleastro M, Ménard A.The role ofHelicobacter pylori outer membrane proteins in adherence and pathogenesis. Biology (Basel). 2013; 2(3): 1110-1134.
11 Senkovich OA, Yin J, Ekshyyan V, Conant C, Traylor J, Adegboyega P, McGee DJ, Rhoads RE, Slepenkov S, Testerman TL.Helicobacter pylori AlpA and AlpB bind host laminin and influence gastric inflammation in Gerbils. Infect Immun. 2011; 79(8): 3106-3116.
12 Loh JT, Torres VJ, Algood HM, McClain MS, Cover TL.Helicobacter pylori HopQ outer membrane protein attenuates bacterial adherence to gastric epithelial cells. FEMS Microbiol Lett. 2008; 289(1): 53-58.
13 Belogolova E, Bauer B, Pompaiah M, Asakura H, Brinkman V, Ertl C, Bartfeld S, Nechitaylo TY, Haas R, Machuy N, Salama N, Churin Y, Meyer TF.Helicobacter pylori outer membrane protein HopQ identified as a novel T4SSassociated virulence factor. Cell Microbiol. 2013; 15(11): 1896-1912.
14 Oleastro M, Cordeiro R, Ferrand J, Nunes B, Lehours P, Carvalho-Oliveira I, Mendes AI, Penque D, Monteiro L, Mégraud F, Ménard A.Evaluation of the clinical significance of homB, a novel candidate marker ofHelicobacter pylori strains associated with peptic ulcer disease. J Infect Dis. 2008; 198(9): 1379-1387.
15 Cao P, Lee KJ, Blaser MJ, Cover TL.Analysis ofhopQ alleles in East Asian and Western strains of Helicobacter pylori. FEMS Microbiol Lett. 2005; 251(1): 37-43.
16 Yakoob J, Abbas Z, Khan R, Salim SA, Awan S, Abrar A, Jafri W.Helicobacter pylori outer membrane protein Q allele distribution is associated with distinct pathologies in Pakistan. Infect Genet Evol. 2016; 37: 57-62.
17 Burger O, Ofek I, Tabak M, Weiss EI, Sharon N, Neeman I.A high molecular mass constituent of cranberry juice inhibitsHelicobacter pylori adhesion to human gastric mucus. FEMS Immunol Med Microbiol. 2000; 29(4): 295-301.
18 Yakoob J, Hu GL, Fan XG, Yang HX, Liu SH, Tan DM, Li TG, Zhang Z.Diversity ofHelicobacter pylori among Chinese persons with H. pylori infection. APMIS. 2000; 108(7-8): 482-486.
19 Lee A, Megraud F.Helicobacter pylori: techniques for clinical diagnosis and basic research. Philadelphia: Saunders (W.B.) Co Ltd. 1995: 94-109.
20 Williamson EM, Okpako DT, Evans FJ.Pharmacological methods in phytotherapy research. Chichester: John Wiley & Sons Ltd. 1996: 15-23.
21 Sellins KS, Cohen JJ.Gene induction by gamma-irradiation leads to DNA fragmentation in lymphocytes.J Immunol. 1987; 139(10): 3199-3206.
22 Zaidi SF, Muhammad JS, Shahryar S, Usmanghani K, Gilani AH, Jafri W, Sugiyama T.Anti-inflammatory and cytoprotective effects of selected Pakistani medicinal plants inHelicobacter pylori-infected gastric epithelial cells. J Ethnopharmacol. 2012; 141(1): 403-410.
23 Zaidi SF, Yamamoto T, Refaat A, Ahmed K, Sakurai H, Saiki I, Kondo T, Usmanghani K, Kadowaki M, Sugiyama T.Modulation of activation-induced cytidine deaminase by curcumin inHelicobacter pylori-infected gastric epithelial cells. Helicobacter. 2009; 141(1): 588-595.
24 Meyer F, Wilson KT, James SP.Modulation of innate cytokine responses by products ofHelicobacter pylori. Infect Immun. 2000; 68(11): 6265-6272.
25 Cwikla C, Schmidt K, Matthias A, Bone KM, Lehmann R, Tiralongo E.Investigations into the antibacterial activities of phytotherapeutics againstHelicobacter pylori and Campylobacter jejuni. Phytother Res. 2010; 24(5): 649-656.
26 Gaus K, Huang Y, Israel DA, Pendland SL, Adeniyi BA, Mahady GB.Standardized ginger (Zingiber officinale) extract reduces bacterial load and suppresses acute and chronic inflammation in Mongolian gerbils infected with CagA Helicobacter pylori. Pharm Biol. 2009; 47(1): 92-98.
27 Mahady GB, Pendland SL, Yun GS, Lu ZZ, Stoia A.Ginger (Zingiber officinale Roscoe) and the gingerols inhibit the growth of CagA+ strains of Helicobacter pylori. Anticancer Res. 2003; 23(5A): 3699-3702.
28 Holt PR, Katz S, Kirshoff R.Curcumin therapy in inflammatory bowel disease: a pilot study.Dig Dis Sci. 2005; 50(11): 2191-2193.
29 Egan ME, Pearson M, Weiner SA, Rajendran V, Rubin D, Glöckner-Pagel J, Canny S, Du K, Lukacs GL, Caplan MJ.Curcumin, a major constituent of turmeric, corrects cystic fibrosis defects.Science. 2004; 304(5670): 600-602.
30 Bengmark S.Curcumin, an atoxic antioxidant and natural NF-kappaB, cyclooxygenase-2, lipooxygenase, and inducible nitric oxide synthase inhibitor: a shield against acute and chronic diseases.JPEN J Parenter Enteral Nutr. 2006; 30(1): 45-51.
31 Cheng WC, Chen YF, Wang HJ, Hsu KC, Lin SC, Chen TJ, Yang JM, Wang WC.Structures ofHelicobacter pylori shikimate kinase reveal a selective inhibitor-induced-fit mechanism. PLoS One. 2012; 7(3): e33481.
32 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(2): 218-223.
33 Merrell DS, Goodrich ML, Otto G, Tompkins LS, Falkow S. pH-regulated gene expression of the gastric pathogenHelicobacter pylori. Infect Immun. 2003; 71(6): 3529-3539.
34 Lengsfeld C, Titgemeyer F, Faller G, Hensel A.Glycosylated compounds from okra inhibits adhesion ofHelicobacter pylori to human gastric mucosa. J Agric Food Chem. 2004; 52(6): 1495-1503.
35 Piotrowski J, Slomiany A, Murty VL, Fekete Z, Slomiany BL.Inhibition ofHelicobacter pylori colonization by sulfated gastric mucin. Biochem Int. 1991; 24(4): 749-775.
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