Loss of Corpus-Specific Lipids in Helicobacter pylori-Induced Atrophic Gastritis

Lin, Aung Soe; Shuman, Jennifer H. B.; Kotnala, Ankita; Shaw, Jeff A; Beckett, Amber C.; Harvey, Jack; Tuck, Michael; Dixon, Beverly R. E. A.; Reyzer, Michelle L.; Algood, Holly M. Scott; Schey, Kevin L.; Piazuelo, M. Blanca; Cover, Timothy L.

doi:10.1128/msphere.00826-21

Cited by 6 publications

(4 citation statements)

References 52 publications

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“…Altered abundance or altered localization of most of these proteins has not been previously described. The loss of corpus-specific proteins detected in H. pylori -infected Mongolian gerbils with atrophic gastritis parallels the loss of corpus-specific lipids detected in a previous study ( 39 ).…”

Section: Discussionsupporting

confidence: 84%

“…Similar to human stomachs, rodent stomachs contain glandular antrum and corpus regions, as well as a non-glandular forestomach not present in human stomachs ( 33 ). Wild-type (WT) mice rarely develop severe disease in response to H. pylori infection, but H. pylori -infected Mongolian gerbils may develop gastric ulceration, premalignant conditions (atrophic gastritis and dysplasia), and gastric adenocarcinoma ( 31 , 34 – 39 ).…”

Section: Introductionmentioning

confidence: 99%

“…Knowledge is limited regarding the molecular alterations that occur in gastric premalignant conditions such as atrophic gastritis ( 40 , 41 ). In a previous study, we used a Mongolian gerbil model of gastric carcinogenesis to show that H. pylori -induced atrophic gastritis was accompanied by a loss of corpus-specific lipids ( 39 ). In the current study, we sought to define additional molecular alterations associated with atrophic gastritis by using transcriptional profiling, imaging mass spectrometry of tryptic peptides, and liquid chromatography with tandem mass spectrometry (LC-MS/MS) analysis of proteins in Mongolian gerbil gastric tissues.…”

Section: Introductionmentioning

confidence: 99%

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Remodeling of the gastric environment in Helicobacter pylori -induced atrophic gastritis

Shuman,

Lin,

Westland

et al. 2024

mSystems

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Helicobacter pylori colonization of the human stomach is a strong risk factor for gastric cancer. To investigate H. pylori -induced gastric molecular alterations, we used a Mongolian gerbil model of gastric carcinogenesis. Histologic evaluation revealed varying levels of atrophic gastritis (a premalignant condition characterized by parietal and chief cell loss) in H. pylori -infected animals, and transcriptional profiling revealed a loss of markers for these cell types. We then assessed the spatial distribution and relative abundance of proteins in the gastric tissues using imaging mass spectrometry and liquid chromatography with tandem mass spectrometry. We detected striking differences in the protein content of corpus and antrum tissues. Four hundred ninety-two proteins were preferentially localized to the corpus in uninfected animals. The abundance of 91 of these proteins was reduced in H. pylori -infected corpus tissues exhibiting atrophic gastritis compared with infected corpus tissues exhibiting non-atrophic gastritis or uninfected corpus tissues; these included numerous proteins with metabolic functions. Fifty proteins localized to the corpus in uninfected animals were diffusely delocalized throughout the stomach in infected tissues with atrophic gastritis; these included numerous proteins with roles in protein processing. The corresponding alterations were not detected in animals infected with a H. pylori ∆ cagT mutant (lacking Cag type IV secretion system activity). These results indicate that H. pylori can cause loss of proteins normally localized to the gastric corpus as well as diffuse delocalization of corpus-specific proteins, resulting in marked changes in the normal gastric molecular partitioning into distinct corpus and antrum regions. IMPORTANCE A normal stomach is organized into distinct regions known as the corpus and antrum, which have different functions, cell types, and gland architectures. Previous studies have primarily used histologic methods to differentiate these regions and detect H. pylori -induced alterations leading to stomach cancer. In this study, we investigated H. pylori -induced gastric molecular alterations in a Mongolian gerbil model of carcinogenesis. We report the detection of numerous proteins that are preferentially localized to the gastric corpus but not the antrum in a normal stomach. We show that stomachs with H. pylori- induced atrophic gastritis (a precancerous condition characterized by the loss of specialized cell types) exhibit marked changes in the abundance and localization of proteins normally localized to the gastric corpus. These results provide new insights into H. pylori -induced gastric molecular alterations that are associated with the development of stomach cancer.

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Section: Discussionsupporting

confidence: 84%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Remodeling of the gastric environment in Helicobacter pylori -induced atrophic gastritis

Shuman,

Lin,

Westland

et al. 2024

mSystems

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“…In this pathogen, lysoPE 16:0 and 18:1 are the most dominant 101,102 . In H. pylori, only lysoPE 18:1 has thus far been detected 103 .…”

Section: Lysophosphatidylethanolaminementioning

confidence: 99%

Lysophospholipids - underestimated molecules of the unique phospholipidome of Campylobacter jejuni

Cao¹

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Chapter 1 General Introduction Chapter 2 Biological functions of bacterial lysophospholipids Advances in microbial physiology. 2022 Chapter 3 The unique phospholipidome of the enteric pathogen Campylobacter jejuni: lysophosholipids are required for motility at low oxygen availability Journal of molecular biology. 2020 Chapter 4 Campylobacter jejuni benefits from the bile salt deoxycholate under low-oxygen condition in a PldA dependent manner Chapter 5 Campylobacter jejuni permeabilizes the host cell membrane by short chain lysophosphatidylethanolamines Gut microbes. 2022

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Biological functions of bacterial lysophospholipids

Cao¹,

Putten²,

Wösten³

2023

Advances in Microbial Physiology

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Loss of Corpus-Specific Lipids in Helicobacter pylori-Induced Atrophic Gastritis

Abstract: H. pylori colonization of the stomach triggers a cascade of gastric alterations that can potentially culminate in stomach cancer. The molecular alterations that occur in gastric tissue prior to development of stomach cancer are not well understood.

Cited by 6 publications

References 52 publications

Remodeling of the gastric environment in Helicobacter pylori -induced atrophic gastritis

Remodeling of the gastric environment in Helicobacter pylori -induced atrophic gastritis

Lysophospholipids - underestimated molecules of the unique phospholipidome of Campylobacter jejuni

Biological functions of bacterial lysophospholipids

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