Author ORCID Identifier

https://orcid.org/0000-0002-9337-5519

Semester

Summer

Date of Graduation

2024

Document Type

Dissertation

Degree Type

PhD

College

School of Medicine

Department

Microbiology, Immunology, and Cell Biology

Committee Chair

Jonathan Busada

Committee Co-Chair

Cory Robinson

Committee Member

Cory Robinson

Committee Member

Richard Peek

Committee Member

Brian Boone

Committee Member

Jennifer Franko

Abstract

Gastric cancer is the fifth most common cancer and the fifth leading cause of cancer deaths worldwide. Helicobacter pylori infection is the number one risk factor for gastric cancer development. Roughly 50% of the world’s population is infected with H. pylori, though only 1-3% of those infected will develop cancer. H. pylori drives chronic inflammation that creates the requisite environment for carcinogenesis, yet it remains unclear why some individuals develop cancer and others do not. Most mechanistic studies are done in mice, however H. pylori is not a natural mouse pathogen. Research is typically done either with mouse-adapted strains of H. pylori or the natural mouse pathogen Helicobacter felis. While both are common models, few have directly compared their effects on mice. We hypothesize that inflammation caused by H. felis better models the inflammation caused by H. pylori in humans, thereby making it a better model for H. pylori pathogenesis. We began by co-culturing the PMSS1 H. pylori strain or the CS1 H. felis strain with mouse peritoneal macrophages to assess their immunostimulatory effects. The bacteria induced similar cytokine production from the cultured macrophages, indicating similar immunostimulatory effects in vitro. We then infected C57BL/6J mice with H. pylori or H. felis. Two months post-inoculation, H. pylori caused modest gastric inflammation and no significant atrophy while H. felis induced severe inflammation and caused significant glandular atrophy. H. felis exhibited increased immunogenicity in vivo, there was increased CD4+ T cell activation, which is associated with gastric cancer risk in humans. Based on our data, we concluded that H. felis is better suited for studies on gastric inflammation and tumorigenesis while H. pylori is better suited for studies on colonization and effects on the microbiome. Inflammation is a key factor that drives H. pylori-mediated carcinogenesis. Research has shown that immune-deficient mice do not exhibit the disease progression seen in immune-sufficient mice. Our lab has previously shown that glucocorticoids are critical mediators of gastric immune homeostasis. To determine the role of endogenous glucocorticoids on Helicobacter-mediated disease, we adrenalectomized (ADX) C57BL/6J mice and infected them with H. felis within a week of surgery. Two months post-infection, intact-infected and ADX-infected mice had similar levels of gastric atrophy and pyloric metaplasia development. However, ADX-infected mice had significantly increased T cell infiltration, specifically CD4+ T cells. Quantitativ real-time PCR (qRT-PCR) indicated that ADX-infected mice had higher T cell activation as well. The ADX-infected mice consistently eliminated their infections by the two month timepoint. When mice were treated with antibiotics two months post-inoculation, the intact group was able to recover but not the ADX group. When treated with antibiotics and then given corticosterone replacement therapy, both intact and ADX groups were able to recover, indicating that glucocorticoids are necessary to restore homeostasis. Data one year post-inoculation revealed that while intact-infected mice dependably had more inflammation and dysplastic changes to the gastric mucosa, ADX-infected mice tended to be protected yet there was an outlier group of mice still exhibiting neoplastic lesions and inflammation. These data suggest that glucocorticoid signaling in the stomach prevents from pathogenic inflammation, however this limits the effectiveness of the immune response. Chronic inflammation persists and predisposes intact mice to neoplastic lesions. This challenges the longstanding idea that tolerance, rather than immunity, protects from carcinogenesis.

Embargo Reason

Publication Pending

Available for download on Wednesday, July 23, 2025

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