Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori
Abstract
Helicobacter pylori, one of the most common bacterial pathogens of humans, colonizes the gastric mucosa, where it appears to persist throughout the host's life unless the patient is treated. Colonization induces chronic gastric inflammation which can progress to a variety of diseases, ranging in severity from superficial gastritis and peptic ulcer to gastric cancer and mucosal-associated lymphoma. Strain-specific genetic diversity has been proposed to be involved in the organism's ability to cause different diseases or even be beneficial to the infected host and to participate in the lifelong chronicity of infection. Here we compare the complete genomic sequences of two unrelated H. pylori isolates. This is, to our knowledge, the first such genomic comparison. H. pylori was believed to exhibit a large degree of genomic and allelic diversity, but we find that the overall genomic organization, gene order and predicted proteomes (sets of proteins encoded by the genomes) of the two strains are quite similar. Between 6 to 7% of the genes are specific to each strain, with almost half of these genes being clustered in a single hypervariable region.
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The complete genome sequences of H. pylori strains 26695 and J99 demonstrate that this organism contains only two rRNA operons.
“The complete genome sequences of two H. pylori strains, 26695 and J99 (1, 34), have been published elsewhere and demonstrate that this organism contains only two rRNA operons, increasing the likelihood that rRNA mutations could arise.”
From Mutations in the 16S rRNA Genes of<i>Helicobacter pylori</i>Mediate Resistance to Tetracycline (2002) · cites this paper as [1]
Analysis of H. pylori genome sequences indicates that the smallest distances between rdxA and one of the 16S rRNA genes are 193 kb in strain 26695 and 205 kb in strain J99.
“Analysis of the H. pylori genome sequences (1, 34) indicates that the smallest distances between rdxA and one of the 16S rRNA genes are 193 kb in strain 26695 and 205 kb in strain J99.”
From Mutations in the 16S rRNA Genes of<i>Helicobacter pylori</i>Mediate Resistance to Tetracycline (2002) · cites this paper as [1]
Cites
The complete genome sequence of the gastric pathogen Helicobacter pylori
Tomb, J.-F., White, O., Kerlavage, A. R., Clayton, R. A., Sutton, G. G., Fleischmann, R. D., Ketchum, K. A., Klenk, H. P., Gill, S., Dougherty, B. A., et al. (1997) · Nature · doi:10.1038/41483 · Cited by 3,529 · see citing works
Censini, S., Lange, C., Xiang, Z., Crabtree, J. E., GHIARA, P., Borodovsky, M. Y., Rappuoli, R., & Covacci, A. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.25.14648 · Cited by 1,872 · see citing works
Helicobacter pylori Adhesin Binding Fucosylated Histo-Blood Group Antigens Revealed by Retagging
Ilver, D., Arnqvist, A., Ögren, J., Frick, I.-M., Kersulyte, D., Incecik, E. T., Berg, D. E., Covacci, A., Engstrand, L. G., & Borén, T. (1998) · Science · doi:10.1126/science.279.5349.373 · Cited by 1,225 · see citing works
Smith, D. R., Doucette‐Stamm, L., DeLoughery, C., Lee, H., Dubois, J., Aldredge, T., Bashirzadeh, R., Blakely, D. J., Cook, R., Gilbert, K., et al. (1997) · Journal of Bacteriology · doi:10.1128/jb.179.22.7135-7155.1997 · Cited by 1,126 · see citing works
Self-citationAnalyses of the cag pathogenicity island of Helicobacter pylori
Akopyants, N. S., Clifton, S. W., Kersulyte, D., Crabtree, J. E., Youree, B. E., Reece, C. A., Bukanov, N. O., Drazek, E. S., Roe, B. A., & Berg, D. E. (1998) · Molecular Microbiology · doi:10.1046/j.1365-2958.1998.00770.x · Cited by 716 · see citing works
Atherton, J. C., Peek, R. M., Tham, K. T., Cover, T. L., & Blaser, M. J. (1997) · Gastroenterology · doi:10.1016/s0016-5085(97)70223-3 · Cited by 639 · see citing works
Curnow, A. W., Hong, K., Yuan, R., Kim, S.-I., Martins, O., Winkler, W. C., Henkin, T. M., & Söll, D. G. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.22.11819 · Cited by 313 · see citing works
Tatusov, R. L., Mushegian, A. R., Peer Bork, B., Brown, N. P., Hayes, W. S., Borodovsky, M. Y., Rudd, K. E., & Koonin, E. V. (1996) · Current Biology · doi:10.1016/s0960-9822(02)00478-5 · Cited by 301 · see citing works
Helicobacter Pylori and Gastroduodenal Disease
Cover, T. L., & Blaser, M. J. (1992) · Annual Review of Medicine · doi:10.1146/annurev.me.43.020192.001031 · Cited by 265 · see citing works
PCR-based RFLP analysis of DNA sequence diversity in the gastric pathogenHelicobacter pylori
Akopyanz, N., Bukanov, N. O., Westblom, T. U., & Berg, D. E. (1992) · Nucleic Acids Research · doi:10.1093/nar/20.23.6221 · Cited by 250 · see citing works
Sakagami, T., Dixon, M. F., O’Rourke, J., Howlett, R., Alderuccio, F., Vella, J., Shimoyama, T., & Lee, A. (1996) · Gut · doi:10.1136/gut.39.5.639 · Cited by 219 · see citing works
Simple sequence repeats in the Helicobacter pylori genome
Saunders, N. J. S. G., Peden, J. F., Hood, D. W., & Moxon, E. R. (1998) · Molecular Microbiology · doi:10.1046/j.1365-2958.1998.00768.x · Cited by 203 · see citing works
Not all Helicobacter pylori strains are created equal: should all be eliminated?
Blaser, M. J. (1997) · The Lancet · doi:10.1016/s0140-6736(96)09133-7 · Cited by 180 · see citing works
Variability of gene order in different Helicobacter pylori strains contributes to genome diversity
Jiang, Q. L., Hiratsuka, K., & Taylor, D. E. (1996) · Molecular Microbiology · doi:10.1111/j.1365-2958.1996.tb02521.x · Cited by 155 · see citing works
Self-citationKansau, I., Raymond, J., Bingen, É., Courcoux, P., Kalach, N., Bergeret, M., Braimi, N., Dupont, C. M., & Labigne-Roussel, A. (1996) · Research in Microbiology · doi:10.1016/0923-2508(96)84023-x · Cited by 137 · see citing works
Genetic diversity of Helicobacter pylori
Logan, R. P., & Berg, D. (1996) · The Lancet · doi:10.1016/s0140-6736(05)65885-0 · Cited by 63 · see citing works
Suerbaum, S., Brauer-Steppkes, T., Labigne-Roussel, A., Cameron, B., & Drlica, K. (1998) · Gene · doi:10.1016/s0378-1119(98)00065-1 · Cited by 38 · see citing works
Lee, W. K., An, Y. S., Kim, K. H., Kim, S. H., Song, J., Ryu, B., Choi, Y. J., Yoon, Y. H., Baik, S., Rhee, K., et al. (1997) · Applied and Environmental Microbiology · doi:10.1128/aem.63.12.4866-4871.1997 · Cited by 26 · see citing works
Diversity among Clinical Isolates of Helicobacter pylori in Korea
Han, J., Yu, E., Lee, I., & Lee, Y. (1997) · Molecules and Cells · doi:10.1016/s1016-8478(23)13335-8 · Cited by 7 · see citing works
The Validity of Laboratory Evidence in the Diagnosis of the Sequelae of Acute Hepatitis
Tumen, H. J., & Cohn, E. M. (1949) · Gastroenterology · doi:10.1016/s0016-5085(49)80010-2 · Cited by 6 · see citing works
Fock, K., Khor, C., Goh, K. L., Teoh, Y., Seow, A., Chia, K., Ho, B., & Ng, H. S. (1998) · Gastroenterology · doi:10.1016/s0016-5085(98)82429-3 · Cited by 3 · see citing works
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Versatile and open software for comparing large genomes
Kurtz, S., Phillippy, A., Delcher, A. L., Smoot, M., Shumway, M., Antonescu, C., & Salzberg, S. L. (2004) · Genome Biology · doi:10.1186/gb-2004-5-2-r12 · Cited by 5,254 · see citing works
Suerbaum, S., & Michetti, P. (2002) · New England Journal of Medicine · doi:10.1056/nejmra020542 · Cited by 2,984 · see citing works
Pathogenesis of <i>Helicobacter pylori</i> Infection
Kusters, J. G., van Vliet, A. H. M., & Kuipers, E. J. (2006) · Clinical Microbiology Reviews · doi:10.1128/cmr.00054-05 · Cited by 2,526 · see citing works
Epidemiology of gastric cancer
Crew, K. D., & Neugut, A. I. (2006) · World Journal of Gastroenterology · doi:10.3748/wjg.v12.i3.354 · Cited by 2,118 · see citing works
The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences
Parkhill, J., Wren, B. W., Mungall, K., Ketley, J. M., Churcher, C. M., Basham, D., Chillingworth, T., Davies, R. M., Feltwell, T., Holroyd, S. A., et al. (2000) · Nature · doi:10.1038/35001088 · Cited by 1,966 · see citing works
Whole genome sequencing of meticillin-resistant Staphylococcus aureus
Kuroda, M., Ohta, T., Uchiyama, I., Baba, T., Yuzawa, H., Kobayashi, I., Cui, L., Oguchi, A., Aoki, K.-I., Nagai, Y., et al. (2001) · The Lancet · doi:10.1016/s0140-6736(00)04403-2 · Cited by 1,950 · see citing works
Helicobacter pylori and gastrointestinal tract adenocarcinomas
Peek, R. M., & Blaser, M. J. (2002) · Nature reviews. Cancer · doi:10.1038/nrc703 · Cited by 1,807 · see citing works
Sequencing and comparison of yeast species to identify genes and regulatory elements
Kellis, M., Patterson, N. J., Endrizzi, M. G., Birren, B. W., & Lander, E. S. (2003) · Nature · doi:10.1038/nature01644 · Cited by 1,731 · see citing works
The species concept for prokaryotes
Rossello-Mora, R. A., & Amann, R. (2001) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2001.tb00571.x · Cited by 1,475 · see citing works
Helicobacter pylori and Gastric Cancer: Factors That Modulate Disease Risk
Wroblewski, L. E., Peek, R. M., & Wilson, K. T. (2010) · Clinical Microbiology Reviews · doi:10.1128/cmr.00011-10 · Cited by 1,455 · see citing works
BLAST 2 Sequences, a new tool for comparing protein and nucleotide sequences
Tatusova, T. A., & Madden, T. L. (1999) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1999.tb13575.x · Cited by 1,789 · see citing works
Malfertheiner, P., Camargo, M. C., El-Omar, E. M., Liou, J., Peek, R. M., Schulz, C., Smith, S. I., & Suerbaum, S. (2023) · Nature Reviews Disease Primers · doi:10.1038/s41572-023-00431-8 · Cited by 1,285 · see citing works
Conti, M., & Beavo, J. A. (2007) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.76.060305.150444 · Cited by 1,188 · see citing works
Classification and phylogeny of hydrogenases
Vignais, P. M., Billoud, B., & Meyer, J. (2001) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2001.tb00587.x · Cited by 1,185 · see citing works
Helicobacter pylori: gastric cancer and beyond
Polk, D. B., & Peek, R. M. (2010) · Nature Reviews Cancer · doi:10.1038/nrc2857 · Cited by 1,158 · see citing works
The protein–protein interaction map of Helicobacter pylori
Rain, J., Selig, L., Reuse, H. D., Battaglia, V., Reverdy, C., Simon, S., Lenzen, G., Petel, F. X., Wojcik, J., Schächter, V., et al. (2001) · Nature · doi:10.1038/35051615 · Cited by 1,142 · see citing works
The primary transcriptome of the major human pathogen Helicobacter pylori
Sharma, C. M., Hoffmann, S., Darfeuille, F., Reignier, J., Findeiß, S., Sittka, A., Chabas, S., Reiche, K., Jörg Hackermüller, A., Reinhardt, R., et al. (2010) · Nature · doi:10.1038/nature08756 · Cited by 1,133 · see citing works
Helicobacter pylori Virulence and Genetic Geography
Covacci, A., Telford, J. L., Giudice, G. D., Parsonnet, J., & Rappuoli, R. (1999) · Science · doi:10.1126/science.284.5418.1328 · Cited by 1,047 · see citing works
Helicobacter pylori persistence: biology and disease
Blaser, M. J., & Atherton, J. C. (2004) · Journal of Clinical Investigation · doi:10.1172/jci20925 · Cited by 941 · see citing works
Helicobacter pylori SabA Adhesin in Persistent Infection and Chronic Inflammation
Mahdavi, J., Sondén, B., Hurtig, M., Olfat, F. O., Forsberg, L., Roche, N., Ångström, J., Larsson, T. P., Teneberg, S., Karlsson, K., et al. (2002) · Science · doi:10.1126/science.1069076 · Cited by 935 · see citing works
Casjens, S., Palmer, N., van Vugt, R., Huang, W. M., Stevenson, B., Rosa, P. A., Lathigra, R. B., Sutton, G. G., Peterson, J. D., Dodson, R. J., et al. (2000) · Molecular Microbiology · doi:10.1046/j.1365-2958.2000.01698.x · Cited by 834 · see citing works
Genome sequences of Chlamydia trachomatis MoPn and Chlamydia pneumoniae AR39
Read, T. D. (2000) · Nucleic Acids Research · doi:10.1093/nar/28.6.1397 · Cited by 768 · see citing works
Phase and Antigenic Variation in Bacteria
van der Woude, M. W., & Bäumler, A. J. (2004) · Clinical Microbiology Reviews · doi:10.1128/cmr.17.3.581-611.2004 · Cited by 766 · see citing works
Mitochondrial Genome Evolution and the Origin of Eukaryotes
Lang, B. F., Gray, M. W., & Burger, G. (1999) · Annual Review of Genetics · doi:10.1146/annurev.genet.33.1.351 · Cited by 724 · see citing works
Cohan, F. M. (2002) · Annual Review of Microbiology · doi:10.1146/annurev.micro.56.012302.160634 · Cited by 714 · see citing works
Whole-Genome Comparison ofMycobacterium tuberculosisClinical and Laboratory Strains
Fleischmann, R. D., Alland, D., Eisen, J. A., Carpenter, L. R., White, O. R., Peterson, J., DeBoy, R. T., Dodson, R. J., Gwinn, M. L., Haft, D. H., et al. (2002) · Journal of Bacteriology · doi:10.1128/jb.184.19.5479-5490.2002 · Cited by 667 · see citing works
Clinical relevance of the Helicobacter pylori gene for blood-group antigen-binding adhesin
Gerhard, M., Lehn, N., Neumayer, N., Borén, T., Rad, R., Schepp, W., Miehlke, S., Classen, M., & Prinz, C. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.22.12778 · Cited by 612 · see citing works
Divergence and Redundancy of 16S rRNA Sequences in Genomes with Multiple rrn Operons
Acinas, S. G., Marcelino, L. A., Klepac‐Ceraj, V., & Polz, M. F. (2004) · Journal of Bacteriology · doi:10.1128/jb.186.9.2629-2635.2004 · Cited by 604 · see citing works
Stein, M., Rappuoli, R., & Covacci, A. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.3.1263 · Cited by 578 · see citing works
Higashi, H., Tsutsumi, R., Fujita, A., Yamazaki, S., Asaka, M., Azuma, T., & Hatakeyama, M. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.222375399 · Cited by 573 · see citing works
THE PATHOGENESIS OFHELICOBACTER PYLORI–INDUCED GASTRO-DUODENAL DISEASES
Atherton, J. C. (2006) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev.pathol.1.110304.100125 · Cited by 568 · see citing works
A whole-genome microarray reveals genetic diversity among Helicobacter pylori strains
Salama, N. R., Guillemin, K. J., McDaniel, T. K., Sherlock, G. J., Tompkins, L. S., & Falkow, S. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.26.14668 · Cited by 559 · see citing works
Helicobacter infection and gastric neoplasia
Peek, R. M., & Crabtree, J. E. (2005) · The Journal of Pathology · doi:10.1002/path.1868 · Cited by 549 · see citing works
Essential Genes Are More Evolutionarily Conserved Than Are Nonessential Genes in BacteriaPreprint
Jordan, I. K., Rogozin, I. B., Wolf, Y. I., & Koonin, E. V. (2002) · Genome Research · doi:10.1101/gr.87702 · Cited by 546 · see citing works
Fouts, D. E., Mongodin, E. F., Mandrell, R. E., Miller, W. G., Rasko, D. A., Ravel, J., Brinkac, L. M., DeBoy, R. T., Parker, C. T., Daugherty, S. C., et al. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0030015 · Cited by 539 · see citing works
Living dangerously: how Helicobacter pylori survives in the human stomach
Montecucco, C., & Rappuoli, R. (2001) · Nature Reviews Molecular Cell Biology · doi:10.1038/35073084 · Cited by 538 · see citing works
Introduction to the Proteobacteria
Kersters, K., Vos, P. D., Gillis, M., Swings, J., Vandamme, P. A. R., & Stackebrandt, E. S. (2006) · Springer eBooks · doi:10.1007/0-387-30745-1_1 · Cited by 534 · see citing works
Helicobacter pylori infection: An overview of bacterial virulence factors and pathogenesis
Kao, C., Sheu, B., & Wu, J.-J. (2016) · Biomedical Journal · doi:10.1016/j.bj.2015.06.002 · Cited by 527 · see citing works
Kobayashi, I. (2001) · Nucleic Acids Research · doi:10.1093/nar/29.18.3742 · Cited by 513 · see citing works
Fischer, W. H., Püls, J., Buhrdorf, R., Gebert, B., Odenbreit, S., & Haas, R. (2001) · Molecular Microbiology · doi:10.1046/j.1365-2958.2001.02714.x · Cited by 506 · see citing works
Purine nucleoside phosphorylases: properties, functions, and clinical aspects
Bzowska, A., Kulikowska, E., & Shugar, D. (2000) · Pharmacology & Therapeutics · doi:10.1016/s0163-7258(00)00097-8 · Cited by 494 · see citing works
Search and Discovery Strategies for Biotechnology: the Paradigm Shift
Bull, A. T., Ward, A. C., & Goodfellow, M. (2000) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.64.3.573-606.2000 · Cited by 476 · see citing works
A phylogenomic study of DNA repair genes, proteins, and processes
Eisen, J. A., & Hanawalt, P. C. (1999) · Mutation Research/DNA Repair · doi:10.1016/s0921-8777(99)00050-6 · Cited by 464 · see citing works
Type I Restriction Systems: Sophisticated Molecular Machines (a Legacy of Bertani and Weigle)
Murray, N. E. (2000) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.64.2.412-434.2000 · Cited by 447 · see citing works
Linking pangenomes and metagenomes: the Prochlorococcus metapangenome
Delmont, T. O., & Eren, A. M. (2018) · PeerJ · doi:10.7717/peerj.4320 · Cited by 433 · see citing works
Fucosylation in prokaryotes and eukaryotes
Ma, B., Simala‐Grant, J. L., & Taylor, D. E. (2006) · Glycobiology · doi:10.1093/glycob/cwl040 · Cited by 430 · see citing works
Self-citationQian, W., Jia, Y., Ren, S., He, Y.-Q., Feng, J., Lu, L.-F., Sun, Q., Ying, G., Tang, D., Tang, H., et al. (2005) · Genome Research · doi:10.1101/gr.3378705 · Cited by 412 · see citing works
A M r 34,000 proinflammatory outer membrane protein ( oipA ) of Helicobacter pylori
Yamaoka, Y., Kwon, D. H., & Graham, D. Y. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.130079797 · Cited by 408 · see citing works
Backert, S., Ziska, E., Brinkmann, V., Zimny‐Arndt, U., Fauconnier, A., Jungblut, P. R., Naumann, M., & Meyer, T. F. (2000) · Cellular Microbiology · doi:10.1046/j.1462-5822.2000.00043.x · Cited by 403 · see citing works
Bacterial Species and Speciation
Cohan, F. M. (2001) · Systematic Biology · doi:10.1080/10635150118398 · Cited by 398 · see citing works
Recombination and clonal groupings within Helicobacter pylori from different geographical regions
Achtman, M., Azuma, T., Berg, D. E., Ito, Y., Morelli, G., Pan, Z., Suerbaum, S., Thompson, S. A., ENDE, A. V. D., & van Doorn, L. (1999) · Molecular Microbiology · doi:10.1046/j.1365-2958.1999.01382.x · Cited by 397 · see citing works
Helicobacter pylori evolution and phenotypic diversification in a changing host
Suerbaum, S., & Josenhans, C. (2007) · Nature Reviews Microbiology · doi:10.1038/nrmicro1658 · Cited by 384 · see citing works
Involvement of a Plasmid in Virulence of Campylobacter jejuni 81-176
Bacon, D., Alm, R. A., Burr, D. H., Hu, L., Kopecko, D. J., Ewing, C. P., Trevor J. TRUST, & Guerry, P. (2000) · Infection and Immunity · doi:10.1128/iai.68.8.4384-4390.2000 · Cited by 382 · see citing works
Self-citationEfflux-Mediated Resistance to Fluoroquinolones in Gram-Negative Bacteria
Poole, K. (2000) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.44.9.2233-2241.2000 · Cited by 372 · see citing works
Helicobacter pylori genetic diversity and risk of human disease
Blaser, M. J., & Berg, D. E. (2001) · Journal of Clinical Investigation · doi:10.1172/jci12672 · Cited by 370 · see citing works
Genotypic Diversity Within a Natural Coastal Bacterioplankton Population
Thompson, J. R., Preheim, S. P., Pharino, C., Klepac‐Ceraj, V., Hunt, D. E., Benoit, J., Sarma-Rupavtarm, R. B., Distel, D. L., & Polz, M. F. (2005) · Science · doi:10.1126/science.1106028 · Cited by 360 · see citing works
Genetics of O-Antigen Biosynthesis inPseudomonas aeruginosa
Rocchetta, H. L., Burrows, L. L., & Lam, J. S. (1999) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.63.3.523-553.1999 · Cited by 359 · see citing works
Tsolaki, A. G., Hirsh, A. E., DeRiemer, K., Enciso, J. A., Wong, M. Z., Hannan, M. M., de la Salmonière, Y.-O. L. G., Aman, K., Kato‐Maeda, M., & Small, P. M. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0305634101 · Cited by 355 · see citing works
Emergence of DiverseHelicobacterSpecies in the Pathogenesis of Gastric and Enterohepatic Diseases
Solnick, J. V., & Schauer, D. B. (2001) · Clinical Microbiology Reviews · doi:10.1128/cmr.14.1.59-97.2001 · Cited by 352 · see citing works
Microbiology in the post-genomic era
Medini, D., Serruto, D., Parkhill, J., Relman, D. A., Donati, C., Moxon, R. E., Falkow, S., & Rappuoli, R. (2008) · Nature Reviews Microbiology · doi:10.1038/nrmicro1901 · Cited by 351 · see citing works
Twenty years of bacterial genome sequencing
Loman, N. J., & Pallen, M. J. (2015) · Nature Reviews Microbiology · doi:10.1038/nrmicro3565 · Cited by 346 · see citing works
Helicobacter pylori genetic diversity within the gastric niche of a single human host
Israel, D. A., Salama, N. R., Krishna, U. S., Rieger, U. M., Atherton, J. C., Falkow, S., & Peek, R. M. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.251551698 · Cited by 335 · see citing works
Israel, D. A., Salama, N. R., Arnold, C. N., Moss, S. F., Ando, T., Wirth, H.-P., Tham, K. T., Camorlinga, M., Blaser, M. J., Falkow, S., et al. (2001) · Journal of Clinical Investigation · doi:10.1172/jci11450 · Cited by 334 · see citing works
Comparative Genomics ofHelicobacter pylori: Analysis of the Outer Membrane Protein Families
Alm, R. A., Bina, J. E., Andrews, B. M., Doig, P. C., Hancock, R. E. W., & Trevor J. TRUST (2000) · Infection and Immunity · doi:10.1128/iai.68.7.4155-4168.2000 · Cited by 332 · see citing works
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Gerrits, M. M., van Vliet, A. H. M., Kuipers, E. J., & Kusters, J. G. (2006) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(06)70627-2 · Cited by 329 · see citing works
Helicobacter pylori Uses Motility for Initial Colonization and To Attain Robust Infection
Ottemann, K. M., & Lowenthal, A. C. (2002) · Infection and Immunity · doi:10.1128/iai.70.4.1984-1990.2002 · Cited by 328 · see citing works
Sluys, M. V., Oliveira, M. C., Monteiro-Vitorello, C. B., Miyaki, C. Y., Furlan, L. R., Camargo, L. E. A., da Silva, A. C. R., Moon, D. H., Takita, M. A., Lemos, E. G. D. M., et al. (2003) · Journal of Bacteriology · doi:10.1128/jb.185.3.1018-1026.2003 · Cited by 326 · see citing works
Evolution in Health and Disease
(2007) · doi:10.1093/acprof:oso/9780199207466.001.0001 · Cited by 322 · see citing works
Epidemiology of upper gastrointestinal malignancies
Crew, K. D. (2004) · Seminars in Oncology · doi:10.1053/j.seminoncol.2004.04.021 · Cited by 321 · see citing works
Global Transposon Mutagenesis and Essential Gene Analysis of Helicobacter pylori
Salama, N. R., Shepherd, B., & Falkow, S. (2004) · Journal of Bacteriology · doi:10.1128/jb.186.23.7926-7935.2004 · Cited by 309 · see citing works
Duodenal ulcer promoting gene of Helicobacter pylori
Lü, H., Hsu, P., Graham, D. Y., & Yamaoka, Y. (2005) · Gastroenterology · doi:10.1053/j.gastro.2005.01.009 · Cited by 308 · see citing works
Evidence for symmetric chromosomal inversions around the replication origin in bacteria
Eisen, J. A., Heidelberg, J. F., White, O. R., & Salzberg, S. L. (2000) · Genome biology · doi:10.1186/gb-2000-1-6-research0011 · Cited by 307 · see citing works
Polyketide synthases and nonribosomal peptide synthetases: the emerging view from bacterial genomics
Donadio, S., Monciardini, P., & Sosio, M. (2007) · Natural Product Reports · doi:10.1039/b514050c · Cited by 307 · see citing works
NF-κB signaling, liver disease and hepatoprotective agents
Sun, B., & Karin, M. (2008) · Oncogene · doi:10.1038/onc.2008.300 · Cited by 307 · see citing works
Rasko, D. A. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh258 · Cited by 307 · see citing works
Doumith, M., Cazalet, C., Simoes, N., Frangeul, L., Jacquet, C., Kunst, F., Martin, P. B., Cossart, P., Glaser, P., & Buchrieser, C. (2004) · Infection and Immunity · doi:10.1128/iai.72.2.1072-1083.2004 · Cited by 307 · see citing works
Pathogenesis and clinical management of Helicobacter pylori gastric infection
de Brito, B. B., da Silva, F. A. F., Soares, A. S., Pereira, V. A., Santos, M. L. C., Sampaio, M. M., Neves, P. H. M., & de Melo, F. F. (2019) · World Journal of Gastroenterology · doi:10.3748/wjg.v25.i37.5578 · Cited by 302 · see citing works
Velayudhan, J., Hughes, N. J., McColm, A. A., Bagshaw, J. A., Clayton, C. L., Andrews, S. C., & Kelly, D. J. (2000) · Molecular Microbiology · doi:10.1046/j.1365-2958.2000.01987.x · Cited by 298 · see citing works
Helicobacter pylori Flagellin Evades Toll‐Like Receptor 5–Mediated Innate Immunity
Gewirtz, A. T., Yu, Y., Krishna, U. S., Israel, D. A., Lyons, S., & Peek, R. M. (2004) · The Journal of Infectious Diseases · doi:10.1086/386289 · Cited by 295 · see citing works
Domain Architectures of σ54-Dependent Transcriptional Activators
Studholme, D. J., & Dixon, R. A. (2003) · Journal of Bacteriology · doi:10.1128/jb.185.6.1757-1767.2003 · Cited by 294 · see citing works
Staying in Shape: the Impact of Cell Shape on Bacterial Survival in Diverse Environments
Yang, D. C., Blair, K. M., & Salama, N. R. (2016) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00031-15 · Cited by 283 · see citing works
From Genetic Footprinting to Antimicrobial Drug Targets: Examples in Cofactor Biosynthetic Pathways
Gerdes, S., Scholle, M. D., D’Souza, M., Bernal, A., Baev, M. V., Farrell, M., Kurnasov, O. V., Daugherty, M. D., Mseeh, F., Polanuyer, B. M., et al. (2002) · Journal of Bacteriology · doi:10.1128/jb.184.16.4555-4572.2002 · Cited by 282 · see citing works
Houghton, J., & Wang, T. C. (2005) · Gastroenterology · doi:10.1053/j.gastro.2005.03.037 · Cited by 279 · see citing works
Comparing Genomes within the Species Mycobacterium tuberculosisPreprint
Kato‐Maeda, M., Rhee, J. T., Gingeras, T., Salamon, H., Drenkow, J., Smittipat, N., & Small, P. M. (2001) · Genome Research · doi:10.1101/gr166401 · Cited by 275 · see citing works
Nakagawa, I., Kurokawa, K., Yamashita, A., Nakata, M., Tomiyasu, Y., Okahashi, N., Kawabata, S., Yamazaki, K., Shiba, T., Yasunaga, T., et al. (2003) · Genome Research · doi:10.1101/gr.1096703 · Cited by 275 · see citing works
Detecting anomalous gene clusters and pathogenicity islands in diverse bacterial genomes
Karlin, S. (2001) · Trends in Microbiology · doi:10.1016/s0966-842x(01)02079-0 · Cited by 271 · see citing works
Jordan, I. K., Wolf, Y. I., & Koonin, E. V. (2003) · BMC Evolutionary Biology · doi:10.1186/1471-2148-3-1 · Cited by 265 · see citing works
Identification and Characterization of Helicobacter pylori Genes Essential for Gastric Colonization
Kavermann, H., Burns, B. P., Angermüller, K., Odenbreit, S., Fischer, W. H., Melchers, K., & Haas, R. (2003) · The Journal of Experimental Medicine · doi:10.1084/jem.20021531 · Cited by 263 · see citing works
Towards a conceptual and operational union of bacterial systematics, ecology, and evolution
Cohan, F. M. (2006) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2006.1918 · Cited by 259 · see citing works
A novel sheathed surface organelle of the Helicobacter pylori cag type IV secretion system
Rohde, M., Püls, J., Buhrdorf, R., Fischer, W. H., & Haas, R. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03549.x · Cited by 255 · see citing works
Differences in Genotypes ofHelicobacter pylorifrom Different Human Populations
Kersulyte, D., Mukhopadhyay, A. K., Velapatiño, B., Su, W. W., Pan, Z., Garcia, C. M., Hernandez, V., Valdez, Y., Mistry, R. S., Gilman, R. H., et al. (2000) · Journal of Bacteriology · doi:10.1128/jb.182.11.3210-3218.2000 · Cited by 253 · see citing works
Helicobacter pylori outer membrane proteins and gastroduodenal disease
Yamaoka, Y., Ojo, O., Fujimoto, S., Odenbreit, S., Haas, R., Gutierrez, O., El-Zimaity, H. M. T., Reddy, R., Arnqvist, A., & Graham, D. Y. (2005) · Gut · doi:10.1136/gut.2005.083014 · Cited by 252 · see citing works
Cellular and molecular aspects of gastric cancer
Smith, M. G. (2006) · World Journal of Gastroenterology · doi:10.3748/wjg.v12.i19.2979 · Cited by 251 · see citing works
Helicobacter pylori genome evolution during human infection
Kennemann, L., Didelot, X., Aebischer, T., Kuhn, S., Drescher, B., Droege, M., Reinhardt, R., Correa, P., Meyer, T. F., Josenhans, C., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1018444108 · Cited by 249 · see citing works
Intraspecies variation in bacterial genomes: the need for a species genome concept
Lan, R., & Reeves, P. R. (2000) · Trends in Microbiology · doi:10.1016/s0966-842x(00)01791-1 · Cited by 248 · see citing works
Oh, J. D., Bäckhed, H. K., Giannakis, M., Xu, J., Fulton, R. S., Fulton, L. A., Cordum, H. S., Wang, C., Elliott, G., Edwards, J., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0603784103 · Cited by 247 · see citing works
Deep-sea vent ε-proteobacterial genomes provide insights into emergence of pathogens
Nakagawa, S., Takaki, Y., Shimamura, S., Reysenbach, A., Takai, K., & Horikoshi, K. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0700687104 · Cited by 246 · see citing works
The complete genome sequence of the carcinogenic bacterium Helicobacter hepaticus
Suerbaum, S., Josenhans, C., Sterzenbach, T., Drescher, B., Brandt, P., Bell, M., Dröge, M., Fartmann, B., Fischer, H., Ge, Z., et al. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1332093100 · Cited by 244 · see citing works
Helicobacter pylori and MALT Lymphoma
Farinha, P., & Gascoyne, R. D. (2005) · Gastroenterology · doi:10.1053/j.gastro.2005.03.083 · Cited by 241 · see citing works
Solnick, J. V., Hansen, L. M., Salama, N. R., Boonjakuakul, J. K., & Syvanen, M. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0308573100 · Cited by 241 · see citing works
- Authors
- Alm, R. A., Ling, L.-S. L., Moir, D. T., King, B. L., Brown, E. D., Doig, P. C., Smith, D. R., Noonan, B., Guild, B. C., deJonge, B. L., Carmel, G., Tummino, P. J., Caruso, A., Uria-Nickelsen, M., Mills, D. M., Ives, C., Gibson, R., Merberg, D., Mills, S. D., Jiang, Q., Taylor, D. E., Vovis, G. F., & Trust, T. J.
- Affiliations
- University of Alberta (CA)
- Corresponding author
- Alm, Richard A.
- ORCID
- Venue
- Nature
- Published
- 1999-01-14
- Volume
- 397
- Issue
- 6715
- Pages
- 176-180
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2016299826
- Cited by
- 1,893
- References
- 21
- Citations by year
- 2026: 9 · 2025: 18 · 2024: 21 · 2023: 18 · 2022: 16 · 2021: 25 · 2020: 21 · 2019: 24 · 2018: 33 · 2017: 30 · 2016: 46 · 2015: 53 · 2014: 94 · 2013: 49 · 2012: 56
- FWCI
- 171.93
- Type
- journal article
- Language
- en
- Update notices
- erratum (1999-02-25)
- Open access
- closed
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Topics
- Health Sciences › Medicine › Surgery › Helicobacter pylori-related gastroenterology studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Life Sciences › Immunology and Microbiology › Microbiology › Microbial infections and disease research
- Keywords
- Helicobacter pylori, comparative genomics, hypervariable region, gene order, proteome, gastric colonization, chronic gastritis, peptic ulcer, gastric cancer, bacterial genomics
- MeSH terms
- Duodenal Ulcer, Humans, Molecular Sequence Data, Species Specificity, Gene Expression Regulation, Bacterial, Sequence Alignment, Helicobacter pylori, Helicobacter Infections, Genome, Bacterial, Sequence Analysis, DNA
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