Genome sequence analysis of Helicobacter pylori strains associated with gastric ulceration and gastric cancer

Mark S. McClain; Carrie L. Shaffer; Dawn A. Israel; Richard M. Peek; Timothy L. Cover

doi:10.1186/1471-2164-10-13

Genome sequence analysis of Helicobacter pylori strains associated with gastric ulceration and gastric cancer

Mark S. McClain, Carrie L. Shaffer, Dawn A. Israel, Richard M. Peek, Timothy L. Cover

Research output: Contribution to journal › Article › peer-review

90 Scopus citations

Abstract

Background: Persistent colonization of the human stomach by Helicobacter pylori is associated with asymptomatic gastric inflammation (gastritis) and an increased risk of duodenal ulceration, gastric ulceration, and non-cardia gastric cancer. In previous studies, the genome sequences of H. pylori strains from patients with gastritis or duodenal ulcer disease have been analyzed. In this study, we analyzed the genome sequences of an H. pylori strain (98-10) isolated from a patient with gastric cancer and an H. pylori strain (B128) isolated from a patient with gastric ulcer disease. Results: Based on multilocus sequence typing, strain 98-10 was most closely related to H. pylori strains of East Asian origin and strain B128 was most closely related to strains of European origin. Strain 98-10 contained multiple features characteristic of East Asian strains, including a type s1c vacA allele and a cagA allele encoding an EPIYA-D tyrosine phosphorylation motif. A core genome of 1237 genes was present in all five strains for which genome sequences were available. Among the 1237 core genes, a subset of alleles was highly divergent in the East Asian strain 98-10, encoding proteins that exhibited <90% amino acid sequence identity compared to corresponding proteins in the other four strains. Unique strain-specific genes were identified in each of the newly sequenced strains, and a set of strain-specific genes was shared among H. pylori strains associated with gastric cancer or premalignant gastric lesions. Conclusion: These data provide insight into the diversity that exists among H. pylori strains from diverse clinical and geographic origins. Highly divergent alleles and strain-specific genes identified in this study may represent useful biomarkers for analyzing geographic partitioning of H. pylori and for identifying strains capable of inducing malignant or premalignant gastric lesions.

Original language	English
Article number	13
Journal	BMC Genomics
Volume	10
DOIs	https://doi.org/10.1186/1471-2164-10-13
State	Published - Jan 5 2009

Bibliographical note

Funding Information:
This work was supported by a grant from the Fondazione Cariverona call 2003 to P. F. P. and by grant from Association Française contre les Myopathies (AFM) call 2008 to G. L.

Funding

This work was supported by a grant from the Fondazione Cariverona call 2003 to P. F. P. and by grant from Association Française contre les Myopathies (AFM) call 2008 to G. L.

Funders	Funder number
Association Française contre les Myopathies
National Institute of Allergy and Infectious F32-AI286447 Cydney N. Johnson Diseases National Institute of Allergy and Infectious R01AI168214 Jason W. Rosch Diseases National Institute of Allergy and Infectious P30 Cydney N. Johnson Diseases National Institute of Allergy and Infectious R00-AI166116 Christopher D. Radka Diseases National Institute of Allergy and Infectious T32-AI106700 Cydney N. Johnson Diseases National Institute of Allergy and Infectious R01AI192221 Jason W. Rosch Diseases National Inst...	R01AI039657, R01AI068009
National Childhood Cancer Registry – National Cancer Institute	R01CA077955, P01CA116087
National Institute of Diabetes and Digestive and Kidney Diseases	R01DK073902, R01DK058587

ASJC Scopus subject areas

Biotechnology
Genetics

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

Access to Document

10.1186/1471-2164-10-13

Cite this

@article{d931575580e84c8ea3b3f592e6188d1e,

title = "Genome sequence analysis of Helicobacter pylori strains associated with gastric ulceration and gastric cancer",

abstract = "Background: Persistent colonization of the human stomach by Helicobacter pylori is associated with asymptomatic gastric inflammation (gastritis) and an increased risk of duodenal ulceration, gastric ulceration, and non-cardia gastric cancer. In previous studies, the genome sequences of H. pylori strains from patients with gastritis or duodenal ulcer disease have been analyzed. In this study, we analyzed the genome sequences of an H. pylori strain (98-10) isolated from a patient with gastric cancer and an H. pylori strain (B128) isolated from a patient with gastric ulcer disease. Results: Based on multilocus sequence typing, strain 98-10 was most closely related to H. pylori strains of East Asian origin and strain B128 was most closely related to strains of European origin. Strain 98-10 contained multiple features characteristic of East Asian strains, including a type s1c vacA allele and a cagA allele encoding an EPIYA-D tyrosine phosphorylation motif. A core genome of 1237 genes was present in all five strains for which genome sequences were available. Among the 1237 core genes, a subset of alleles was highly divergent in the East Asian strain 98-10, encoding proteins that exhibited <90\% amino acid sequence identity compared to corresponding proteins in the other four strains. Unique strain-specific genes were identified in each of the newly sequenced strains, and a set of strain-specific genes was shared among H. pylori strains associated with gastric cancer or premalignant gastric lesions. Conclusion: These data provide insight into the diversity that exists among H. pylori strains from diverse clinical and geographic origins. Highly divergent alleles and strain-specific genes identified in this study may represent useful biomarkers for analyzing geographic partitioning of H. pylori and for identifying strains capable of inducing malignant or premalignant gastric lesions.",

author = "McClain, \{Mark S.\} and Shaffer, \{Carrie L.\} and Israel, \{Dawn A.\} and Peek, \{Richard M.\} and Cover, \{Timothy L.\}",

note = "Funding Information: This work was supported by a grant from the Fondazione Cariverona call 2003 to P. F. P. and by grant from Association Fran{\c c}aise contre les Myopathies (AFM) call 2008 to G. L.",

year = "2009",

month = jan,

day = "5",

doi = "10.1186/1471-2164-10-13",

language = "English",

volume = "10",

}

TY - JOUR

T1 - Genome sequence analysis of Helicobacter pylori strains associated with gastric ulceration and gastric cancer

AU - McClain, Mark S.

AU - Shaffer, Carrie L.

AU - Israel, Dawn A.

AU - Peek, Richard M.

AU - Cover, Timothy L.

N1 - Funding Information: This work was supported by a grant from the Fondazione Cariverona call 2003 to P. F. P. and by grant from Association Française contre les Myopathies (AFM) call 2008 to G. L.

PY - 2009/1/5

Y1 - 2009/1/5

N2 - Background: Persistent colonization of the human stomach by Helicobacter pylori is associated with asymptomatic gastric inflammation (gastritis) and an increased risk of duodenal ulceration, gastric ulceration, and non-cardia gastric cancer. In previous studies, the genome sequences of H. pylori strains from patients with gastritis or duodenal ulcer disease have been analyzed. In this study, we analyzed the genome sequences of an H. pylori strain (98-10) isolated from a patient with gastric cancer and an H. pylori strain (B128) isolated from a patient with gastric ulcer disease. Results: Based on multilocus sequence typing, strain 98-10 was most closely related to H. pylori strains of East Asian origin and strain B128 was most closely related to strains of European origin. Strain 98-10 contained multiple features characteristic of East Asian strains, including a type s1c vacA allele and a cagA allele encoding an EPIYA-D tyrosine phosphorylation motif. A core genome of 1237 genes was present in all five strains for which genome sequences were available. Among the 1237 core genes, a subset of alleles was highly divergent in the East Asian strain 98-10, encoding proteins that exhibited <90% amino acid sequence identity compared to corresponding proteins in the other four strains. Unique strain-specific genes were identified in each of the newly sequenced strains, and a set of strain-specific genes was shared among H. pylori strains associated with gastric cancer or premalignant gastric lesions. Conclusion: These data provide insight into the diversity that exists among H. pylori strains from diverse clinical and geographic origins. Highly divergent alleles and strain-specific genes identified in this study may represent useful biomarkers for analyzing geographic partitioning of H. pylori and for identifying strains capable of inducing malignant or premalignant gastric lesions.

AB - Background: Persistent colonization of the human stomach by Helicobacter pylori is associated with asymptomatic gastric inflammation (gastritis) and an increased risk of duodenal ulceration, gastric ulceration, and non-cardia gastric cancer. In previous studies, the genome sequences of H. pylori strains from patients with gastritis or duodenal ulcer disease have been analyzed. In this study, we analyzed the genome sequences of an H. pylori strain (98-10) isolated from a patient with gastric cancer and an H. pylori strain (B128) isolated from a patient with gastric ulcer disease. Results: Based on multilocus sequence typing, strain 98-10 was most closely related to H. pylori strains of East Asian origin and strain B128 was most closely related to strains of European origin. Strain 98-10 contained multiple features characteristic of East Asian strains, including a type s1c vacA allele and a cagA allele encoding an EPIYA-D tyrosine phosphorylation motif. A core genome of 1237 genes was present in all five strains for which genome sequences were available. Among the 1237 core genes, a subset of alleles was highly divergent in the East Asian strain 98-10, encoding proteins that exhibited <90% amino acid sequence identity compared to corresponding proteins in the other four strains. Unique strain-specific genes were identified in each of the newly sequenced strains, and a set of strain-specific genes was shared among H. pylori strains associated with gastric cancer or premalignant gastric lesions. Conclusion: These data provide insight into the diversity that exists among H. pylori strains from diverse clinical and geographic origins. Highly divergent alleles and strain-specific genes identified in this study may represent useful biomarkers for analyzing geographic partitioning of H. pylori and for identifying strains capable of inducing malignant or premalignant gastric lesions.

UR - https://www.scopus.com/pages/publications/59449109546

UR - https://www.scopus.com/inward/citedby.url?scp=59449109546&partnerID=8YFLogxK

U2 - 10.1186/1471-2164-10-13

DO - 10.1186/1471-2164-10-13

M3 - Article

C2 - 19123947

AN - SCOPUS:59449109546

SN - 1471-2164

VL - 10

JO - BMC Genomics

JF - BMC Genomics

M1 - 13

ER -

Genome sequence analysis of Helicobacter pylori strains associated with gastric ulceration and gastric cancer

Abstract

Bibliographical note

Funding

ASJC Scopus subject areas

UN SDGs

Access to Document

Other files and links

Fingerprint

Cite this