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Regulatory B Cell Function Is Suppressed by Smoking and Obesity in H. pylori-Infected Subjects and Is Correlated with Elevated Risk of Gastric Cancer.

Li G, Wulan H, Song Z, Paik PA, Tsao ML, Goodman GM, MacEachern PT, Downey RS, Jankowska AJ, Rabinowitz YM, Learch TB, Song DZ, Yuan JJ, Zheng S, Zheng Z - PLoS ONE (2015)

Bottom Line: We found that B cells from H. pylori-infected patients presented altered composition and function compared to uninfected patients.Interestingly, in H. pylori-infected smoking subjects and obese subjects, the number of IL-10+ B cells and CD24+CD38+ B cells were reduced compared to H. pylori-infected asymptomatic subjects.Regulatory functions mediated by CD24+CD38+ B cells were also impaired.

View Article: PubMed Central - PubMed

Affiliation: Affiliated Bayi Brain Hospital, General Hospital of Beijing Military Command, Beijing, 100700, China.

ABSTRACT
Helicobacter pylori infection occurs in more than half of the world's population and is the main cause for gastric cancer. A series of lifestyle and nutritional factors, such as tobacco smoking and obesity, have been found to elevate the risk for cancer development. In this study, we sought to determine the immunological aspects during H. pylori infection and gastric cancer development. We found that B cells from H. pylori-infected patients presented altered composition and function compared to uninfected patients. IL-10-expressing CD24+CD38+ B cells were upregulated in H. pylori-infected patients, contained potent regulatory activity in inhibiting T cell pro-inflammatory cytokine secretion, and responded directly to H. pylori antigen stimulation. Interestingly, in H. pylori-infected smoking subjects and obese subjects, the number of IL-10+ B cells and CD24+CD38+ B cells were reduced compared to H. pylori-infected asymptomatic subjects. Regulatory functions mediated by CD24+CD38+ B cells were also impaired. In addition, gastric cancer positive patients had reduced IL-10-producing B cell frequencies after H. pylori-stimulation. Altogether, these data suggest that in H. pylori-infection, CD24+CD38+ B cell is upregulated and plays a role in suppressing pro-inflammatory responses, possibly through IL-10 production, a feature that was not observed in smoking and obese patients.

No MeSH data available.


Related in: MedlinePlus

Frequencies of IL-10+ B cells and CD24+CD38+ B cells in study subjects with or without gastric cancer development.Patients’ gastric cancer status was tracked for 5 years after initial sample collection. (A) The frequencies of IL-10+ cells in CD24+CD38+ B cells after direct H. pylori stimulation in H. pylori-infected smoking subjects and obese subjects (B) The percentages of CD24+CD38+ B cells in total B cells in H. pylori-infected smoking subjects and obese subjects. N = 8 for every group. *: P< 0.05. (Student’s t test).
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pone.0134591.g005: Frequencies of IL-10+ B cells and CD24+CD38+ B cells in study subjects with or without gastric cancer development.Patients’ gastric cancer status was tracked for 5 years after initial sample collection. (A) The frequencies of IL-10+ cells in CD24+CD38+ B cells after direct H. pylori stimulation in H. pylori-infected smoking subjects and obese subjects (B) The percentages of CD24+CD38+ B cells in total B cells in H. pylori-infected smoking subjects and obese subjects. N = 8 for every group. *: P< 0.05. (Student’s t test).

Mentions: Smoking and obesity were known to increase the risk for gastric cancer development in H. pylori-infected subjects. Since smoking and obesity also suppressed normal regulatory B cell functions, we examined whether these two phenomena were linked. We found that in smoking subjects and obese subjects, those who became positive for gastric cancer status had significantly lower frequencies of IL-10+ cells in CD24+CD38+ B cells after H. pylori stimulation than those who remained negative for gastric cancer development (Fig 5A. P<0.05 for both). On the other hand, we did not find that cancer positive and cancer negative patients were significantly different in terms of their frequencies of CD24+CD38+ B cells in total B cells (Fig 5B). No H. pylori-infected asymptomatic patients in this study became gastric cancer positive.


Regulatory B Cell Function Is Suppressed by Smoking and Obesity in H. pylori-Infected Subjects and Is Correlated with Elevated Risk of Gastric Cancer.

Li G, Wulan H, Song Z, Paik PA, Tsao ML, Goodman GM, MacEachern PT, Downey RS, Jankowska AJ, Rabinowitz YM, Learch TB, Song DZ, Yuan JJ, Zheng S, Zheng Z - PLoS ONE (2015)

Frequencies of IL-10+ B cells and CD24+CD38+ B cells in study subjects with or without gastric cancer development.Patients’ gastric cancer status was tracked for 5 years after initial sample collection. (A) The frequencies of IL-10+ cells in CD24+CD38+ B cells after direct H. pylori stimulation in H. pylori-infected smoking subjects and obese subjects (B) The percentages of CD24+CD38+ B cells in total B cells in H. pylori-infected smoking subjects and obese subjects. N = 8 for every group. *: P< 0.05. (Student’s t test).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4520600&req=5

pone.0134591.g005: Frequencies of IL-10+ B cells and CD24+CD38+ B cells in study subjects with or without gastric cancer development.Patients’ gastric cancer status was tracked for 5 years after initial sample collection. (A) The frequencies of IL-10+ cells in CD24+CD38+ B cells after direct H. pylori stimulation in H. pylori-infected smoking subjects and obese subjects (B) The percentages of CD24+CD38+ B cells in total B cells in H. pylori-infected smoking subjects and obese subjects. N = 8 for every group. *: P< 0.05. (Student’s t test).
Mentions: Smoking and obesity were known to increase the risk for gastric cancer development in H. pylori-infected subjects. Since smoking and obesity also suppressed normal regulatory B cell functions, we examined whether these two phenomena were linked. We found that in smoking subjects and obese subjects, those who became positive for gastric cancer status had significantly lower frequencies of IL-10+ cells in CD24+CD38+ B cells after H. pylori stimulation than those who remained negative for gastric cancer development (Fig 5A. P<0.05 for both). On the other hand, we did not find that cancer positive and cancer negative patients were significantly different in terms of their frequencies of CD24+CD38+ B cells in total B cells (Fig 5B). No H. pylori-infected asymptomatic patients in this study became gastric cancer positive.

Bottom Line: We found that B cells from H. pylori-infected patients presented altered composition and function compared to uninfected patients.Interestingly, in H. pylori-infected smoking subjects and obese subjects, the number of IL-10+ B cells and CD24+CD38+ B cells were reduced compared to H. pylori-infected asymptomatic subjects.Regulatory functions mediated by CD24+CD38+ B cells were also impaired.

View Article: PubMed Central - PubMed

Affiliation: Affiliated Bayi Brain Hospital, General Hospital of Beijing Military Command, Beijing, 100700, China.

ABSTRACT
Helicobacter pylori infection occurs in more than half of the world's population and is the main cause for gastric cancer. A series of lifestyle and nutritional factors, such as tobacco smoking and obesity, have been found to elevate the risk for cancer development. In this study, we sought to determine the immunological aspects during H. pylori infection and gastric cancer development. We found that B cells from H. pylori-infected patients presented altered composition and function compared to uninfected patients. IL-10-expressing CD24+CD38+ B cells were upregulated in H. pylori-infected patients, contained potent regulatory activity in inhibiting T cell pro-inflammatory cytokine secretion, and responded directly to H. pylori antigen stimulation. Interestingly, in H. pylori-infected smoking subjects and obese subjects, the number of IL-10+ B cells and CD24+CD38+ B cells were reduced compared to H. pylori-infected asymptomatic subjects. Regulatory functions mediated by CD24+CD38+ B cells were also impaired. In addition, gastric cancer positive patients had reduced IL-10-producing B cell frequencies after H. pylori-stimulation. Altogether, these data suggest that in H. pylori-infection, CD24+CD38+ B cell is upregulated and plays a role in suppressing pro-inflammatory responses, possibly through IL-10 production, a feature that was not observed in smoking and obese patients.

No MeSH data available.


Related in: MedlinePlus