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Characterization of East-Asian Helicobacter pylori encoding Western EPIYA-ABC CagA

  • Microbial Pathogenesis and Host-Microbe Interaction
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Abstract

The polymorphic bacterial oncoprotein, CagA shows geography-dependent variation in the C-terminal Glu-Pro-Ile-Tyr-Ala (EPIYA) motifs; East-Asian H. pylori isolates carry the ABD type while Western isolates carry the ABC type. In Western isolates, the EPIYA-C motif is sometimes found in multi-copy and this genotype is associated with disease severity. Interestingly, a small number of East-Asian H. pylori isolates have been found to carry Western ABC-type CagA. To gain a better understanding of these unusual isolates, the genomes of four Korean H. pylori clinical isolates carrying ABC-type CagA were sequenced via third generation (Pac-Bio SMRT) sequencing technology. The obtained data were utilized for phylogenetic analysis as well as comparison of additional virulence factors that are known to show geographic-dependent polymorphisms. Three of four isolates indeed belonged to the hpEastAsia group and showed typical East-Asian polymorphism in virulence factors such as homA/B/C, babA/B/C, and oipA. One isolate grouped to HpAfrica and showed typical Western polymorphism of virulence factors such as cagA, homA/B/C, and oipA. To understand the occurrence of the multi-copy EPIYA-C motif genotype in an East-Asian H. pylori background, the Korean clinical isolate, K154 was analyzed; this strain belonged to hpEastAsia but encoded CagA EPIYA-ABCCCC. Based on DNA sequence homology within the CagA multimerization (CM) sequence that flanked the EPIYA-C motifs, we predicted that the number of C motifs might change via homologous recombination. To test this hypothesis, K154 was cultured for one generation and 287 single colonies were analyzed for the number of EPIYA-C motifs using PCR-based screening and DNA sequencing verification. Three out of 284 (1%) single colony isolates showed changes in the number of EPIYA-C motifs in vitro; one isolate increased to five EPIYA-C motifs, one decreased to three EPIYA-C motifs, and one completely deleted the EPIYA-C motifs. The capacity for dynamic changes in the number of EPIYA-C repeats of CagA may play a role in generating important intraspecies diversity in East-Asian H. pylori.

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References

  • Azuma, T., Yamakawa, A., Yamazaki, S., Ohtani, M., Ito, Y., Muramatsu, A., Suto, H., Yamazaki, Y., Keida, Y., and Higashi, H. 2004. Distinct diversity of the cag pathogenicity island among Helicobacter pylori strains in Japan. J. Clin. Microbiol. 42, 2508–2517.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Batista, S.A., Rocha, G.A., Rocha, A.M.C., Saraiva, I.E.B., Cabral, M.M.D.A., Oliveira, R.C., and Queiroz, D.M.M. 2011. Higher number of Helicobacter pylori CagA EPIYA C phosphorylation sites increases the risk of gastric cancer, but not duodenal ulcer. BMC Microbiol. 11, 61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blaser, M.J. 1998. Helicobacter pylori and gastric diseases. Br. Med. J. 316, 1507–1510.

    Article  CAS  Google Scholar 

  • Blom, J., Kreis, J., Spänig, S., Juhre, T., Bertelli, C., Ernst, C., and Goesmann, A. 2016. EDGAR 2.0: an enhanced software platform for comparative gene content analyses. Nucleic Acids Res. 44, W22–W28.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bray, F., Ferlay, J., Soerjomataram, I., Siegel, R.L., Torre, L.A., and Jemal, A. 2018. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 68, 394–424.

    Article  PubMed  Google Scholar 

  • Bridge, D.R., Blum, F.C., Jang, S., Kim, J., Cha, J.H., and Merrell, D.S. 2017. Creation and initial characterization of isogenic Helicobacter pylori CagA EPIYA variants reveals differential activation of host cell signaling pathways. Sci. Rep. 7, 11057.

    Article  PubMed  PubMed Central  Google Scholar 

  • Carpenter, B.M., McDaniel, T.K., Whitmire, J.M., Gancz, H., Guidotti, S., Censini, S., and Merrell, D.S. 2007. Expanding the Helicobacter pylori genetic toolbox: modification of an endogenous plasmid for use as a transcriptional reporter and complementation vector. Appl. Environ. Microbiol. 73, 7506–7514.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Draper, J.L., Hansen, L.M., Bernick, D.L., Abedrabbo, S., Underwood, J.G., Kong, N., Huang, B.C., Weis, A.M., Weimer, B.C., Van Vliet, A.H., et al. 2017. Fallacy of the unique genome: sequence diversity within single Helicobacter pylori strains. mBio 8, e02321–16.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • El Khadir, M., Alaoui Boukhris, S., Benajah, D.A., Ibrahimi, S.A., Chbani, L., Bouguenouch, L., El Rhazi, K., El Abkari, M., Nejjari, C., Mahmoud, M., et al. 2018. Helicobacter pylori CagA EPIYA-C motifs and gastric diseases in Moroccan patients. Infect. Genet. Evol. 66, 120–129.

    Article  PubMed  Google Scholar 

  • El Khadir, M., Alaoui Boukhris, S., Benajah, D.A., Ibrahimi, S.A., Chbani, L., El Abkari, M., and Bennani, B. 2020. VacA genotypes and cagA-EPIYA-C motifs of Helicobacter pylori and gastric histopathological lesions. Int. J. Cancer 147, 3206–3214.

    Article  CAS  PubMed  Google Scholar 

  • Falush, D., Kraft, C., Taylor, N.S., Correa, P., Fox, J.G., Achtman, M., and Suerbaum, S. 2001. Recombination and mutation during long-term gastric colonization by Helicobacter pylori: estimates of clock rates, recombination size, and minimal age. Proc. Natl. Acad. Sci. USA 98, 15056–15061.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujitani, Y. and Kobayashi, I. 1999. Effect of DNA sequence divergence on homologous recombination as analyzed by a random-walk model. Genetics 153, 1973–1988.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujitani, Y., Yamamoto, K., and Kobayashi, I. 1995. Dependence of frequency of homologous recombination on the homology length. Genetics 140, 797–809.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Furuta, Y., Yahara, K., Hatakeyama, M., and Kobayashi, I. 2011. Evolution of cagA oncogene of Helicobacter pylori through recombination. PLoS ONE 6, e23499.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haft, D.H., DiCuccio, M., Badretdin, A., Brover, V., Chetvernin, V., O’Neill, K., Li, W., Chitsaz, F., Derbyshire, M.K., Gonzales, N.R., et al. 2018. RefSeq: an update on prokaryotic genome annotation and curation. Nucleic Acids Res. 46, D851–D860.

    Article  CAS  PubMed  Google Scholar 

  • Higashi, H., Tsutsumi, R., Fujita, A., Yamazaki, S., Asaka, M., Azuma, T., and Hatakeyama, M. 2002a. Biological activity of the Helicobacter pylori virulence factor CagA is determined by variation in the tyrosine phosphorylation sites. Proc. Natl. Acad. Sci. USA 99, 14428–14433.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Higashi, H., Tsutsumi, R., Muto, S., Sugiyama, T., Azuma, T., Asaka, M., and Hatakeyama, M. 2002b. SHP-2 tyrosine phosphatase as an intracellular target of Helicobacter pylori CagA protein. Science 295, 683–686.

    Article  CAS  PubMed  Google Scholar 

  • Honarmand-Jahromy, S., Siavoshi, F., Malekzadeh, R., Sattari, T.N., and Latifi-Navid, S. 2015. Multiple repeats of Helicobacter pylori CagA EPIYA-C phosphorylation sites predict risk of gastric ulcer in Iran. Microb. Pathog. 89, 87–92.

    Article  CAS  PubMed  Google Scholar 

  • Jang, S., Jones, K.R., Olsen, C.H., Joo, Y.M., Yoo, Y.J., Chung, I.S., Cha, J.H., and Merrell, D.S. 2010. Epidemiological link between gastric disease and polymorphisms in VacA and CagA. J. Clin. Microbiol. 48, 559–567.

    Article  CAS  PubMed  Google Scholar 

  • Jang, S., Su, H., Blum, F.C., Bae, S., Choi, Y.H., Kim, A., Hong, Y.A., Kim, J., Kim, J.H., Gunawardhana, N., et al. 2017. Dynamic expansion and contraction of cagA copy number in Helicobacter pylori impact development of gastric disease. mBio 8, e01779–16.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones, K.R., Joo, Y.M., Jang, S., Yoo, Y.J., Lee, H.S., Chung, I.S., Olsen, C.H., Whitmire, J.M., Merrell, D.S., and Cha, J.H. 2009. Polymorphism in the CagA EPIYA motif impacts development of gastric cancer. J. Clin. Microbiol. 47, 959–968.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jung, S.W., Sugimoto, M., Graham, D.Y., and Yamaoka, Y. 2009. homB status of Helicobacter pylori as a novel marker to distinguish gastric cancer from duodenal ulcer. J. Clin. Microbiol. 47, 3241–3245.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kang, J., Jones, K.R., Jang, S., Olsen, C.H., Yoo, Y.J., Merrell, D.S., and Cha, J.H. 2012. The geographic origin of Helicobacter pylori influences the association of the homB gene with gastric cancer. J. Clin. Microbiol. 50, 1082–1085.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karlsson, A., Ryberg, A., Nosouhi Dehnoei, M., Borch, K., and Monstein, H.J. 2012. Variation in number of cagA EPIYA-C phosphorylation motifs between cultured Helicobacter pylori and biopsy strain DNA. Infect. Genet. Evol. 12, 175–179.

    Article  CAS  PubMed  Google Scholar 

  • Kennemann, L., Didelot, X., Aebischer, T., Kuhn, S., Drescher, B., Droege, M., Reinhardt, R., Correa, P., Meyer, T.F., Josenhans, C., et al. 2011. Helicobacter pylori genome evolution during human infection. Proc. Natl. Acad. Sci. USA 108, 5033–5038.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim, A., Lai, J., Merrell, D.S., Kim, J.H., Su, H., and Cha, J.H. 2021. Geographic diversity in Helicobacter pylori oipA genotype between Korean and United States isolates. J. Microbiol. 59, In press. doi: https://doi.org/10.1007/s12275-021-1450-8.

  • Kim, A., Servetas, S.L., Kang, J., Kim, J., Jang, S., Cha, H.J., Lee, W.J., Kim, J., Romero-Gallo, J., Peek, R.M. Jr, et al. 2015. Helicobacter pylori bab paralog distribution and association with cagA, vacA, and homA/B genotypes in American and South Korean clinical isolates. PLoS ONE 10, e0137078.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kraft, C. and Suerbaum, S. 2005. Mutation and recombination in Helicobacter pylori: mechanisms and role in generating strain diversity. Int. J. Med. Microbiol. 295, 299–305.

    Article  CAS  PubMed  Google Scholar 

  • Kumar, S., Stecher, G., and Tamura, K. 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, B., Du, D., Sun, W., Cao, Q., Zhang, Z., and Du, Z. 2013. Analysis of the 3’ variable region of cytotoxin-associated gene A (cagA) in Helicobacter pylori isolates in China. Pharmacol. Pharm. 4, 13–18.

    Article  Google Scholar 

  • Li, Q., Liu, J., Gong, Y., and Yuan, Y. 2017. Association of CagA EPIYA-D or EPIYA-C phosphorylation sites with peptic ulcer and gastric cancer risks: a meta-analysis. Medicine 96, e6620.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu, H.S., Saito, Y., Umeda, M., Murata-Kamiya, N., Zhang, H.M., Higashi, H., and Hatakeyama, M. 2008. Structural and functional diversity in the PAR1b/MARK2-binding region of Helicobacter pylori CagA. Cancer Sci. 99, 2004–2011.

    CAS  PubMed  Google Scholar 

  • Marshall, B.J. and Warren, J.R. 1984. Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet 1, 1311–1315.

    Article  CAS  PubMed  Google Scholar 

  • Matsunari, O., Shiota, S., Suzuki, R., Watada, M., Kinjo, N., Murakami, K., Fujioka, T., Kinjo, F., and Yamaoka, Y. 2012. Association between Helicobacter pylori virulence factors and gastroduodenal diseases in Okinawa, Japan. J. Clin. Microbiol. 50, 876–883.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Møller, H., Heseltine, E., and Vainio, H. 1995. Working group report on schistosomes, liver flukes and Helicobacter pylori. Int. J. Cancer 60, 587–589.

    Article  PubMed  Google Scholar 

  • Nell, S., Estibariz, I., Krebes, J., Bunk, B., Graham, D.Y., Overmann, J., Song, Y., Spröer, C., Yang, I., Wex, T., et al. 2018. Genome and methylome variation in Helicobacter pylori with a cag pathogenicity island during early stages of human infection. Gastroenterology 154, 612–623. e7.

    Article  CAS  PubMed  Google Scholar 

  • Nguyen, L.T., Uchida, T., Murakami, K., Fujioka, T., and Moriyama, M. 2008. Helicobacter pylori virulence and the diversity of gastric cancer in Asia. J. Med. Microbiol. 57, 1445–1453.

    Article  CAS  PubMed  Google Scholar 

  • Nomura, A.M., Lee, J., Stemmermann, G.N., Nomura, R.Y., Perez-Perez, G.I., and Blaser, M.J. 2002. Helicobacter pylori CagA seropositivity and gastric carcinoma risk in a Japanese American population. J. Infect. Dis. 186, 1138–1144.

    Article  PubMed  Google Scholar 

  • Noto, J.M. and Peek, R.M. Jr. 2012. Helicobacter pylori: an overview. Methods Mol. Biol. 921, 7–10.

    Article  CAS  PubMed  Google Scholar 

  • Odenbreit, S., Püls, J., Sedlmaier, B., Gerland, E., Fischer, W., and Haas, R. 2000. Translocation of Helicobacter pylori CagA into gastric epithelial cells by type IV secretion. Science 287, 1497–1500.

    Article  CAS  PubMed  Google Scholar 

  • Oleastro, M., Cordeiro, R., Ferrand, J., Nunes, B., Lehours, P., Carvalho-Oliveira, I., Mendes, A.I., Penque, D., Monteiro, L., Mégraud, F., et al. 2008. Evaluation of the clinical significance of homB, a novel candidate marker of Helicobacter pylori strains associated with peptic ulcer disease. J. Infect. Dis. 198, 1379–1387.

    Article  CAS  PubMed  Google Scholar 

  • Oleastro, M., Cordeiro, R., Ménard, A., Yamaoka, Y., Queiroz, D., Mégraud, F., and Monteiro, L. 2009. Allelic diversity and phylogeny of homB, a novel co-virulence marker of Helicobacter pylori. BMC Microbiol. 9, 248.

    Article  PubMed  PubMed Central  Google Scholar 

  • Parsonnet, J., Friedman, G.D., Orentreich, N., and Vogelman, H. 1997. Risk for gastric cancer in people with CagA positive or CagA negative Helicobacter pylori infection. Gut 40, 297–301.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rawla, P. and Barsouk, A. 2019. Epidemiology of gastric cancer: global trends, risk factors and prevention. Prz. Gastroenterol. 14, 26–38.

    CAS  PubMed  Google Scholar 

  • Ren, S., Higashi, H., Lu, H., Azuma, T., and Hatakeyama, M. 2006. Structural basis and functional consequence of Helicobacter pylori CagA multimerization in cells. J. Biol. Chem. 281, 32344–32352.

    Article  CAS  PubMed  Google Scholar 

  • Rodríguez Gómez, E.R., Otero Regino, W., Monterrey, P.A., and Trespalacios Rangel, A.A. 2020. cagA gene EPIYA motif genetic characterization from Colombian Helicobacter pylori isolates: standardization of a molecular test for rapid clinical laboratory detection. PLoS ONE 15, e0227275.

    Article  PubMed  PubMed Central  Google Scholar 

  • Saadat, I., Higashi, H., Obuse, C., Umeda, M., Murata-Kamiya, N., Saito, Y., Lu, H., Ohnishi, N., Azuma, T., Suzuki, A., et al. 2007. Helicobacter pylori CagA targets PAR1/MARK kinase to disrupt epithelial cell polarity. Nature 447, 330–333.

    Article  CAS  PubMed  Google Scholar 

  • Salih, B.A., Bolek, B.K., and Arikan, S. 2010. DNA sequence analysis of cagA 3′ motifs of Helicobacter pylori strains from patients with peptic ulcer diseases. J. Med. Microbiol. 59, 144–148.

    Article  CAS  PubMed  Google Scholar 

  • Satomi, S., Yamakawa, A., Matsunaga, S., Masaki, R., Inagaki, T., Okuda, T., Suto, H., Ito, Y., Yamazaki, Y., Kuriyama, M., et al. 2006. Relationship between the diversity of the cagA gene of Helicobacter pylori and gastric cancer in Okinawa, Japan. J. Gastroenterol. 41, 668–673.

    Article  CAS  PubMed  Google Scholar 

  • Satou, K., Shiroma, A., Teruya, K., Shimoji, M., Nakano, K., Juan, A., Tamotsu, H., Terabayashi, Y., Aoyama, M., Teruya, M., et al. 2014. Complete genome sequences of eight Helicobacter pylori strains with different virulence factor genotypes and methylation profiles, isolated from patients with diverse gastrointestinal diseases on Okinawa island, Japan, determined using PacBio single-molecule real-time technology. Genome Announc. 2, e00286–14.

    Article  PubMed  PubMed Central  Google Scholar 

  • Servetas, S.L., Kim, A., Su, H., Cha, J.H., and Merrell, D.S. 2018. Comparative analysis of the Hom family of outer membrane proteins in isolates from two geographically distinct regions: the United States and South Korea. Helicobacter 23, e12461.

  • Su, H., Tissera, K., Jang, S., Choi, Y.H., Kim, A., Cho, Y.J., Li, M., Gunawardhana, N., Merrell, D.S., Ge, L., et al. 2019. Evolutionary mehanism leading to the multi-cagA genotype in Helicobacter pylori. Sci. Rep. 9, 11203.

    Article  PubMed  PubMed Central  Google Scholar 

  • Suerbaum, S. and Josenhans, C. 2007. Helicobacter pylori evolution and phenotypic diversification in a changing host. Nat. Rev. Microbiol. 5, 441–452.

    Article  CAS  PubMed  Google Scholar 

  • Suerbaum, S., Smith, J.M., Bapumia, K., Morelli, G., Smith, N.H., Kunstmann, E., Dyrek, I., and Achtman, M. 1998. Free recombination within Helicobacter pylori. Proc. Natl. Acad. Sci. USA 95, 12619–12624.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki, M., Mimuro, H., Kiga, K., Fukumatsu, M., Ishijima, N., Morikawa, H., Nagai, S., Koyasu, S., Gilman, R.H., Kersulyte, D., et al. 2009. Helicobacter pylori CagA phosphorylation-independent function in epithelial proliferation and inflammation. Cell Host Microbe 5, 23–34.

    Article  CAS  PubMed  Google Scholar 

  • Torre, L.A., Bray, F., Siegel, R.L., Ferlay, J., Lortet-Tieulent, J., and Jemal, A. 2015. Global cancer statistics, 2012. CA Cancer J. Clin. 65, 87–108.

    Article  PubMed  Google Scholar 

  • Tsutsumi, R., Takahashi, A., Azuma, T., Higashi, H., and Hatakeyama, M. 2006. Focal adhesion kinase is a substrate and downstream effector of SHP-2 complexed with Helicobacter pylori CagA. Mol. Cell. Biol. 26, 261–276.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xue, Z., You, Y., He, L., Gong, Y., Sun, L., Han, X., Fan, R., Zhai, K., Yang, Y., Zhang, M., et al. 2021. Diversity of 3’ variable region of cagA gene in Helicobacter pylori strains isolated from Chinese population. Gut Pathog. 13, 23.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaoka, Y., Kodama, T., Kashima, K., Graham, D.Y., and Sepulveda, A.R. 1998. Variants of the 3′ region of the cagA gene in Helicobacter pylori isolates from patients with different H. pylori-associated diseases. J. Clin. Microbiol. 36, 2258–2263.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamazaki, S., Yamakawa, A., Okuda, T., Ohtani, M., Suto, H., Ito, Y., Yamazaki, Y., Keida, Y., Higashi, H., Hatakeyama, M., et al. 2005. Distinct diversity of vacA, cagA, and cagE genes of Helicobacter pylori associated with peptic ulcer in Japan. J. Clin. Microbiol. 43, 3906–3916.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yong, X., Tang, B., Li, B.S., **e, R., Hu, C.J., Luo, G., Qin, Y., Dong, H., and Yang, S.M. 2015. Helicobacter pylori virulence factor CagA promotes tumorigenesis of gastric cancer via multiple signaling pathways. Cell Commun. Signal. 13, 30.

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This study was supported by the National Natural Science Foundation of China (NO. 31870124).

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  1. These authors contributed equally to this work.

Authors and Affiliations

  1. Guangzhou Key Laboratory of Basic and Applied Research of Oral Regenerative Medicine, Affiliated Stomatology Hospital of Guangzhou Medical University, Guangzhou, Guangdong, 510182, P. R. China

    Kavinda Tissera, Hanfu Su & Jeong-Heon Cha

  2. Department of Oral Biology, Oral Science Research Center, Department of Applied Life Science, The Graduate School, BK21 FOUR Project, Yonsei University College of Dentistry, Seoul, 03722, Republic of Korea

    Kavinda Tissera, Myeong-A Kim, **g Lai, Sacheera Angulmaduwa & Jeong-Heon Cha

  3. Department of Medical Laboratory Science, Faculty of Allied Health Sciences, University of Ruhuna, Galle, 80000, Sri Lanka

    Kavinda Tissera

  4. Department of Dental Hygiene, Gangdong University, Eumseong, 27600, Republic of Korea

    Aeryun Kim

  5. Department of Microbiology and Immunology, Uniformed Services University of the Health Sciences, Bethesda, Maryland, 20814, USA

    D. Scott Merrell

  6. Department of Dental Hygiene, Baekseok University, Cheonan, 31065, Republic of Korea

    Ji-Hye Kim

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  1. Kavinda Tissera
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Tissera, K., Kim, MA., Lai, J. et al. Characterization of East-Asian Helicobacter pylori encoding Western EPIYA-ABC CagA. J Microbiol. 60, 207–214 (2022). https://doi.org/10.1007/s12275-022-1483-7

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