Comparative analysis of the full genome of Helicobacter pylori isolate sahul64 identifies genes of high divergence

Journal of Bacteriology

Volumn 196, Issue 5, 2014, Pages 1073-1083

  Lu, Wei ^a   Wise, Michael J ^a   Tay, Chin Yen ^a   Windsor, Helen M ^a   Marshall, Barry J ^a   Peacock, Christopher ^a,b   Perkins, Tim ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ENVELOPE PROTEIN; LIPOPOLYSACCHARIDE;

ADULT; ARTICLE; AUSTRALIA; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ISOLATION; BIOSYNTHESIS; CASE REPORT; COMPARATIVE STUDY; CONTROLLED STUDY; DNA MODIFICATION; FEMALE; GENE CLUSTER; GENE IDENTIFICATION; GENE LOCUS; HELICOBACTER PYLORI; HUMAN; NUCLEOTIDE SEQUENCE; PATHOGENICITY ISLAND; PRIORITY JOURNAL; PROPHAGE; PSEUDOGENE; SPECIES DIFFERENTIATION;

ADAPTATION, PHYSIOLOGICAL; BACTERIAL PROTEINS; CHROMOSOME MAPPING; CHROMOSOMES, BACTERIAL; FEMALE; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC VARIATION; GENOME, BACTERIAL; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; OCEANIC ANCESTRY GROUP; PHYLOGENY; SPECIES SPECIFICITY;

EID: 84893721427     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01021-13     Document Type: Article

References (73)

1. Marshall BJ, Warren JR. 1984. Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet 1:1311-1315.
2. Gressmann H, Linz B, Ghai R, Pleissner KP, Schlapbach R, Yamaoka Y, Kraft C, Suerbaum S, Meyer TF, Achtman M. 2005. Gain and loss of multiple genes during the evolution of Helicobacter pylori. PLoS Genet. 1:e43. http://dx.doi.org/10.1371/journal.pgen.0010043.
3. Eppinger M, Baar C, Linz B, Raddatz G, Lanz C, Keller H, Morelli G, Gressmann H, Achtman M, Schuster SC. 2006. Who ate whom? Adaptive Helicobacter genomic changes that accompanied a host jump from early humans to large felines. PLoS Genet. 2:e120. http://dx.doi.org/10.1371/journal.pgen.0020120.
4. Linz B, Balloux F, Moodley Y, Manica A, Liu H, Roumagnac P, Falush D, Stamer C, Prugnolle F, van der Merwe SW, Yamaoka Y, Graham DY, Perez-Trallero E, Wadstrom T, Suerbaum S, Achtman M. 2007. An African origin for the intimate association between humans and Helicobacter pylori. Nature 445: 915-918. http://dx.doi.org/10.1038/nature05562.
5. Baltrus DA, Guillemin K, Phillips PC. 2008. Natural transformation increases the rate of adaptation in the human pathogen Helicobacter pylori. Evolution 62:39-49.
6. Baltrus DA, Blaser MJ, Guillemin K. 2009. Helicobacter pylori genome plasticity. Genome Dyn. 6:75-90. http://dx.doi.org/10.1159/000235764.
7. Maiden MC, Bygraves JA, Feil E, Morelli G, Russell JE, Urwin R, Zhang Q, Zhou J, Zurth K, Caugant DA, Feavers IM, Achtman M, Spratt BG. 1998. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc. Natl. Acad. Sci. U. S. A. 95:3140-3145. http://dx.doi.org/10.1073/pnas.95 .6.3140.
8. Jolley KA, Maiden MC. 2010. BIGSdb: scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 11:595. http: //dx.doi.org/10.1186/1471-2105-11-595.
9. García-Ortíz MV, Marsin S, Arana ME, Gasparutto D, Guerois R, Kunkel TA, Radicella JP. 2011. Unexpected role for Helicobacter pylori DNA polymerase I as a source of genetic variability. PLoS Genet. 7:e1002152. http://dx.doi.org/10.1371/journal.pgen.1002152.
10. Yang Z, Bielawski JP. 2000. Statistical methods for detecting molecular adaptation. Trends Ecol. Evol. 15:496-503. http://dx.doi.org/10.1016/S0169-5347(00)01994-7.
11. Olbermann P, Josenhans C, Moodley Y, Uhr M, Stamer C, Vauterin M, Suerbaum S, Achtman M, Linz B. 2010. A global overview of the genetic and functional diversity in the Helicobacter pylori cag pathogenicity island. PLoS Genet. 6:e1001069. http://dx.doi.org/10.1371/journal.pgen.1001069.
12. Duncan SS, Valk PL, McClain MS, Shaffer CL, Metcalf JA, Bordenstein SR, Cover TL. 2013. Comparative genomic analysis of East Asian and non-Asian Helicobacter pylori strains identifies rapidly evolving genes. PLoS One 8:e55120. http://dx.doi.org/10.1371/journal.pone.0055120.
13. Humbert O, Dorer MS, Salama NR. 2011. Characterization of Helicobacter pylori factors that control transformation frequency and integration length during inter-strain DNA recombination. Mol. Microbiol. 79: 387-401. http://dx.doi.org/10.1111/j.1365-2958.2010.07456.x.
14. Alm RA, Ling LS, Moir DT, King BL, Brown ED, Doig PC, Smith DR, Noonan B, Guild BC, deJonge BL, Carmel G, Tummino PJ, Caruso A, Uria-Nickelsen M, Mills DM, Ives C, Gibson R, Merberg D, Mills SD, Jiang Q, Taylor DE, Vovis GF, Trust TJ. 1999. Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 397:176-180. http://dx.doi.org/10.1038/16495.
15. Vernikos GS, Parkhill J. 2006. Interpolated variable order motifs for identification of horizontally acquired DNA: revisiting the Salmonella pathogenicity islands. Bioinformatics 22:2196-2203. http://dx.doi.org/10 .1093/bioinformatics/btl369.
16. McClain MS, Shaffer CL, Israel DA, Peek RM, Jr, Cover TL. 2009. Genome sequence analysis of Helicobacter pylori strains associated with gastric ulceration and gastric cancer. BMC Genomics 10:3. http://dx.doi.org/10.1186/1471-2164-10-3.
17. Farnbacher M, Jahns T, Willrodt D, Daniel R, Haas R, Goesmann A, Kurtz S, Rieder G. 2010. Sequencing, annotation and comparative genome analysis of the gerbil-adapted Helicobacter pylori strain B8. BMC Genomics 11:335. http://dx.doi.org/10.1186/1471-2164-11-335.
18. Fischer W, Windhager L, Rohrer S, Zeiller M, Karnholz A, Hoffmann R, Zimmer R, Haas R. 16 May 2010. Strain-specific genes of Helicobacter pylori: genome evolution driven by a novel type IV secretion system and genomic island transfer. Nucleic Acids Res. http://dx.doi.org/10.1093/nar/gkq378.
19. Tettelin H, Masignani V, Cieslewicz MJ, Donati C, Medini D, Ward NL, Angiuoli SV, Crabtree J, Jones AL, Durkin AS, Deboy RT, Davidsen TM, Mora M, Scarselli M, Margarit y Ros I, Peterson JD, Hauser CR, Sundaram JP, Nelson WC, Madupu R, Brinkac LM, Dodson RJ, Rosovitz MJ, Sullivan SA, Daugherty SC, Haft DH, Selengut J, Gwinn ML, Zhou L, Zafar N, Khouri H, Radune D, Dimitrov G, Watkins K, O'Connor KJ, Smith S, Utterback TR, White O, Rubens CE, Grandi G, Madoff LC, Kasper DL, Telford JL, Wessels MR, Rappuoli R, Fraser CM. 2005. Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial"pan-genome". Proc. Natl. Acad. Sci. U. S. A. 102:13950-13955. http://dx.doi.org/10.1073/pnas.0506758102.
20. Yamaoka Y. 2010. Mechanisms of disease: Helicobacter pylori virulence factors. Nat. Rev. Gastroenterol. Hepatol. 7:629-641. http://dx.doi.org /10.1038/nrgastro.2010.154.
21. Cascales E, Christie PJ. 2003. The versatile bacterial type IV secretion systems. Nat. Rev. Microbiol. 1:137-149. http://dx.doi.org/10.1038/nrmicro753.
22. Odenbreit S, Puls J, Sedlmaier B, Gerland E, Fischer W, Haas R. 2000. Translocation of Helicobacter pylori CagA into gastric epithelial cells by type IV secretion. Science 287:1497-1500. http://dx.doi.org/10.1126/science.287.5457.1497.
23. Censini S, Lange C, Xiang Z, Crabtree JE, Ghiara P, Borodovsky M, Rappuoli R, Covacci A. 1996. cag, a pathogenicity island of Helicobacter pylori, encodes type I-specific and disease-associated virulence factors. Proc. Natl. Acad. Sci. U. S. A. 93:14648-14653. http://dx.doi.org/10.1073/pnas.93.25.14648.
24. Tegtmeyer N, Wessler S, Backert S. 2011. Role of the cag-pathogenicity island encoded type IV secretion system in Helicobacter pylori pathogenesis. FEBS J. 278:1190-1202. http://dx.doi.org/10.1111/j.1742-4658.2011.08035.x.
25. Patra R, Chattopadhyay S, De R, Datta S, Chowdhury A, Ramamurthy T, Nair GB, Berg DE, Mukhopadhyay AK. 2011. Intact cag pathogenicity island of Helicobacter pylori without disease association in Kolkata, India. Int. J. Med. Microbiol. 301:293-302. http://dx.doi.org/10.1016/j.ijmm.2010.10.003.
26. Thiberge JM, Boursaux-Eude C, Lehours P, Dillies MA, Creno S, Coppee JY, Rouy Z, Lajus A, Ma L, Burucoa C, Ruskone-Foumestraux A, Courillon-Mallet A, De Reuse H, Boneca IG, Lamarque D, Megraud F, Delchier JC, Medigue C, Bouchier C, Labigne A, Raymond J. 2010. From array-based hybridization of Helicobacter pylori isolates to the complete genome sequence of an isolate associated with MALT lymphoma. BMC Genomics 11:368. http://dx.doi.org/10.1186/1471-2164-11-368.
27. Hofreuter D, Odenbreit S, Henke G, Haas R. 1998. Natural competence for DNA transformation in Helicobacter pylori: identification and genetic characterization of the comB locus. Mol. Microbiol. 28:1027-1038. http://dx.doi.org/10.1046/j.1365-2958.1998.00879.x.
28. Whiteside MD, Winsor GL, Laird MR, Brinkman FS. 2013. OrtholugeDB: a bacterial and archaeal orthology resource for improved comparative genomic analysis. Nucleic Acids Res. 41:D366-D376. http://dx.doi.org/10.1093/nar/gks1241.
29. Kersulyte D, Velapatino B, Mukhopadhyay AK, Cahuayme L, Bussalleu A, Combe J, Gilman RH, Berg DE. 2003. Cluster of type IV secretion genes in Helicobacter pylori's plasticity zone. J. Bacteriol. 185:3764-3772. http://dx.doi.org/10.1128/JB.185.13.3764-3772.2003.
30. Kersulyte D, Lee W, Subramaniam D, Anant S, Herrera P, Cabrera L, Balqui J, Barabas O, Kalia A, Gilman RH, Berg DE. 2009. Helicobacter Pylori's plasticity zones are novel transposable elements. PLoS One 4:e6859. http://dx.doi.org/10.1371/journal.pone.0006859.
31. Lu H, Hsu PI, Graham DY, Yamaoka Y. 2005. Duodenal ulcer promoting gene of Helicobacter pylori. Gastroenterology 128:833-848. http://dx .doi.org/10.1053/j.gastro.2005.01.009.
32. Hussein NR, Argent RH, Marx CK, Patel SR, Robinson K, Atherton JC. 2010. Helicobacter pylori dupA is polymorphic, and its active form induces proinflammatory cytokine secretion by mononuclear cells. J. Infect. Dis. 202:261-269. http://dx.doi.org/10.1086/653587.
33. Matteo MJ, Armitano RI, Granados G, Wonaga AD, Sanches C, Olmos M, Catalano M. 2010. Helicobacter pylori oipA, vacA and dupA genetic diversity in individual hosts. J. Med. Microbiol. 59:89-95. http://dx.doi.org/10.1099/jmm.0.011684-0.
34. Nguyen LT, Uchida T, Tsukamoto Y, Kuroda A, Okimoto T, Kodama M, Murakami K, Fujioka T, Moriyama M. 2010. Helicobacter pylori dupA gene is not associated with clinical outcomes in the Japanese population. Clin. Microbiol. Infect. 16:1264-1269. http://dx.doi.org/10.1111/j.1469-0691.2009.03081.x.
35. Gomes LI, Rocha GA, Rocha AM, Soares TF, Oliveira CA, Bittencourt PF, Queiroz DM. 2008. Lack of association between Helicobacter pylori infection with dupA-positive strains and gastroduodenal diseases in Brazilian patients. Int. J. Med. Microbiol. 298:223-230. http://dx.doi.org/10.1016/j.ijmm.2007.05.006.
36. Jung SW, Sugimoto M, Shiota S, Graham DY, Yamaoka Y. 2012. The intact dupA cluster is a more reliable Helicobacter pylori virulence marker than dupA alone. Infect. Immun. 80:381-387. http://dx.doi.org/10.1128/IAI.05472-11.
37. Rohrer S, Holsten L, Weiss E, Benghezal M, Fischer W, Haas R. 2012. Multiple pathways of plasmid DNA transfer in Helicobacter pylori. PLoS One 7:e45623. http://dx.doi.org/10.1371/journal.pone.0045623.
38. Palframan SL, Kwok T, Gabriel K. 2012. Vacuolating cytotoxin A (VacA), a key toxin for Helicobacter pylori pathogenesis. Front. Cell. Infect. Microbiol. 2:92. http://dx.doi.org/10.3389/fcimb.2012.00092.
39. Windsor HM, Abioye-Kuteyi EA, Leber JM, Morrow SD, Bulsara MK, Marshall BJ. 2005. Prevalence of Helicobacter pylori in indigenous Western Australians: comparison between urban and remote rural populations. Med. J. Aust. 182:210-213.
40. Moodley Y, Linz B, Yamaoka Y, Windsor HM, Breurec S, Wu JY, Maady A, Bernhoft S, Thiberge JM, Phuanukoonnon S, Jobb G, Siba P, Graham DY, Marshall BJ, Achtman M. 2009. The peopling of the Pacific from a bacterial perspective. Science 323:527-530. http://dx.doi.org/10.1126/science.1166083.
41. Moodley Y, Linz B, Bond RP, Nieuwoudt M, Soodyall H, Schlebusch CM, Bernhoft S, Hale J, Suerbaum S, Mugisha L, van der Merwe SW, Achtman M. 2012. Age of the association between Helicobacter pylori and man. PLoS Pathog. 8:e1002693. http://dx.doi.org/10.1371/journal.ppat.1002693.
42. Zerbino DR, Birney E. 2008. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18:821-829. http://dx.doi .org/10.1101/gr.074492.107.
43. Lagesen K, Hallin P, Rodland EA, Staerfeldt HH, Rognes T, Ussery DW. 2007. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res. 35:3100-3108. http://dx.doi.org/10.1093/nar/gkm160.
44. Lowe TM, Eddy SR. 1997. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25: 955-964.
45. Delcher AL, Bratke KA, Powers EC, Salzberg SL. 2007. Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23:673-679. http://dx.doi.org/10.1093/bioinformatics/btm009.
46. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O. 2008. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 9:75. http://dx.doi.org/10.1186/1471-2164-9-75.
47. Otto TD, Dillon GP, Degrave WS, Berriman M. 2011. RATT: rapid annotation transfer tool. Nucleic Acids Res. 39:e57. http://dx.doi.org/10.1093/nar/gkq1268.
48. Darling AC, Mau B, Blattner FR, Perna NT. 2004. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res. 14:1394-1403. http://dx.doi.org/10.1101/gr.2289704.
49. Guy L, Kultima JR, Andersson SG. 2010. genoPlotR: comparative gene and genome visualization in R. Bioinformatics 26:2334-2335. http://dx .doi.org/10.1093/bioinformatics/btq413.
50. Suyama M, Torrents D, Bork P. 2006. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 34:W609-W612. http://dx.doi.org/10.1093/nar/gkl315.
51. Yang Z. 1997. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. 13:555-556.
52. Li L, Stoeckert CJ, Jr, Roos DS. 2003. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13:2178-2189. http://dx.doi.org/10.1101/gr.1224503.
53. Francisco AP, Vaz C, Monteiro PT, Melo-Cristino J, Ramirez M, Carrico JA. 2012. PHYLOViZ: phylogenetic inference and data visualization for sequence based typing methods. BMC Bioinformatics 13:87. http://dx.doi.org/10.1186/1471-2105-13-87.
54. Turner KM, Hanage WP, Fraser C, Connor TR, Spratt BG. 2007. Assessing the reliability of eBURST using simulated populations with known ancestry. BMC Microbiol. 7:30. http://dx.doi.org/10.1186/1471-2180-7-30.
55. Francisco AP, Bugalho M, Ramirez M, Carrico JA. 2009. Global optimal eBURST analysis of multilocus typing data using a graphic matroid approach. BMCBioinformatics 10:152. http://dx.doi.org/10.1186/1471-2105-10-152.
56. Salama NR, Hartung ML, Muller A. 2013. Life in the human stomach: persistence strategies of the bacterial pathogen Helicobacter pylori. Nat. Rev. Microbiol. 11:385-399. http://dx.doi.org/10.1038/nrmicro3016.
57. Hug I, Couturier MR, Rooker MM, Taylor DE, Stein M, Feldman MF. 2010. Helicobacter pylori lipopolysaccharide is synthesized via a novel pathway with an evolutionary connection to protein N-glycosylation. PLoS Pathog. 6:e1000819. http://dx.doi.org/10.1371/journal.ppat.1000819.
58. Luo CH, Chiou PY, Yang CY, Lin NT. 13 June 2012. Genome, integration and transduction of a novel temperate phage of Helicobacter pylori. J. Virol. http://dx.doi.org/10.1128/JVI.00446-12.
59. Hussein NR, Mohammadi M, Talebkhan Y, Doraghi M, Letley DP, Muhammad MK, Argent RH, Atherton JC. 2008. Differences in virulence markers between Helicobacter pylori strains from Iraq and those from Iran: potential importance of regional differences in H. pyloriassociated disease. J. Clin. Microbiol. 46:1774-1779. http://dx.doi.org/10.1128/JCM.01737-07.
60. Atherton JC, Blaser MJ. 2009. Coadaptation of Helicobacter pylori and humans: ancient history, modern implications. J. Clin. Invest. 119:2475-2487. http://dx.doi.org/10.1172/JCI38605.
61. Dumrese C, Slomianka L, Ziegler U, Choi SS, Kalia A, Fulurija A, Lu W, Berg DE, Benghezal M, Marshall B, Mittl PR. 2009. The secreted Helicobacter cysteine-rich protein A causes adherence of human monocytes and differentiation into a macrophage-like phenotype. FEBS Lett. 583: 1637-1643. http://dx.doi.org/10.1016/j.febslet.2009.04.027.
62. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer EL, Tate J, Punta M. 27 November 2013. Pfam: the protein families database. Nucleic Acids Res. http://dx.doi.org/10.1093/nar/gkt1223.
63. Karp PD, Paley SM, Krummenacker M, Latendresse M, Dale JM, Lee TJ, Kaipa P, Gilham F, Spaulding A, Popescu L, Altman T, Paulsen I, Keseler IM, Caspi R. 2010. Pathway Tools version 130: integrated software for pathway/genome informatics and systems biology. Brief. Bioinform. 11:40-79. http://dx.doi.org/10.1093/bib/bbp043.
64. Atherton JC, Peek RM, Jr, Tham KT, Cover TL, Blaser MJ. 1997. Clinical and pathological importance of heterogeneity in vacA, the vacuolating cytotoxin gene of Helicobacter pylori. Gastroenterology 112:92-99. http://dx.doi.org/10.1016/S0016-5085(97)70223-3.
65. Gangwer KA, Shaffer CL, Suerbaum S, Lacy DB, Cover TL, Bordenstein SR. 2010. Molecular evolution of the Helicobacter pylori vacuolating toxin gene vacA. J. Bacteriol. 192:6126-6135. http://dx.doi.org/10.1128/JB.01081-10.
66. Tomb JF, White O, Kerlavage AR, Clayton RA, Sutton GG, Fleischmann RD, Ketchum KA, Klenk HP, Gill S, Dougherty BA, Nelson K, Quackenbush J, Zhou L, Kirkness EF, Peterson S, Loftus B, Richardson D, Dodson R, Khalak HG, Glodek A, McKenney K, Fitzegerald LM, Lee N, Adams MD, Hickey EK, Berg DE, Gocayne JD, Utterback TR, Peterson JD, Kelley JM, Cotton MD, Weidman JM, Fujii C, Bowman C, Watthey L, Wallin E, Hayes WS, Borodovsky M, Karp PD, Smith HO, Fraser CM, Venter JC. 1997. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388:539-547. http://dx.doi.org/10.1038/41483.
67. Suerbaum S, Smith JM, Bapumia K, Morelli G, Smith NH, Kunstmann E, Dyrek I, Achtman M. 1998. Free recombination within Helicobacter pylori. Proc. Natl. Acad. Sci. U. S. A. 95:12619-12624. http://dx.doi.org/10.1073/pnas.95.21.12619.
68. Achtman M, Azuma T, Berg DE, Ito Y, Morelli G, Pan ZJ, Suerbaum S, Thompson SA, van der Ende A, van Doorn LJ. 1999. Recombination and clonal groupings within Helicobacter pylori from different geographical regions. Mol. Microbiol. 32:459-470. http://dx.doi.org/10.1046/j.1365-2958.1999.01382.x.
69. Amieva MR, El-Omar EM. 2008. Host-bacterial interactions in Helicobacter pylori infection. Gastroenterology 134:306-323. http://dx.doi.org /10.1053/j.gastro.2007.11.009.
70. Philpott DJ, Belaid D, Troubadour P, Thiberge JM, Tankovic J, Labigne A, Ferrero RL. 2002. Reduced activation of inflammatory responses in host cells by mouse-adapted Helicobacter pylory isolates. Cell Microbiol. 4:285-296. http://dx.doi.org/10.1046/j.1462-5822.2002.00189.x.
71. Alm RA, Trust TJ. 1999. Analysis of the genetic diversity of Helicobacter pylori: the tale of two genomes. J. Mol. Med. 77:834-846. http://dx.doi .org/10.1007/s001099900067.
72. Shiota S, Graham DY, Yamaoka Y. 2012. Reply to "dupA1 Is Associated with Duodenal Ulcer and High Interleukin-8 Secretion from the Gastric Mucosa." Infect. Immun. 80:2973.
73. Takahashi A, Shiota S, Matsunari O, Watada M, Suzuki R, Nakachi S, Kinjo N, Kinjo F, Yamaoka Y. 22 August 2012. Intact Long-Type dupA as a Marker for Gastroduodenal Diseases in Okinawan Subpopulation, Japan. Helicobacter http://dx.doi.org/10.1111/j.1523-5378.2012.00994.x.