Changes in intestinal immunity, gut microbiota and expression of energy metabolism-related genes explain adenoma growth in bilberry and cloudberry-fed ApcMin mice

Essi Päivärinta, Mikael Niku, Johanna Maukonen, Markus Storvik, Anu Heiman-Lindh, Maria Saarela, Anne-Maria Pajari, Marja Mutanen

Research output: Contribution to journalArticleScientificpeer-review

4 Citations (Scopus)

Abstract

We showed previously that ellagitannin-rich cloudberries and anthocyanin-rich bilberries reduce the number of intestinal adenomas in multiple intestinal neoplasia/+ (ApcMin) mice. We also found that cloudberries decreased the size of adenomas, while bilberries increased it. Here we hypothesized that the difference in adenoma growth could be explained by dissimilar effects of the berries on intestinal immune responses and gut microbiota, potentially driven by the distinct polyphenol compositions of the two berries. Our objective was to investigate lymphocyte subtypes and the predominant cecal bacterial diversity in mice fed with bilberries and cloudberries, and to analyze global gene expression profiles in the intestinal mucosa. Immunostainings of CD3+ T lymphocytes, FoxP3+ regulatory T lymphocytes and CD45R+ B lymphocytes revealed a smaller ratio of intraepithelial to all mucosal CD3+ T lymphocytes in the cloudberry-fed mice compared to controls, suggesting an attenuation of inflammation. Bilberry feeding induced no changes in the density of any of the lymphocyte subtypes. The predominant bacterial diversity in cecal contents, analyzed using PCR-denaturating gradient gel electrophoresis, was higher in the bilberry group than in the control or cloudberry groups. The microbial profiles of cloudberry-fed mice clustered together and were associated with small adenoma size. Pathway analyses of gene expression data showed that cloudberry downregulated and bilberry upregulated the expression of energy metabolism-related genes in the intestinal mucosa. In conclusion, attenuation of intestinal inflammation, changes in microbial profiles and downregulation of mucosal energy metabolism may account for the smaller adenoma size in cloudberry-fed mice in comparison to bilberry-fed mice.
Original languageEnglish
Pages (from-to)1285-1297
JournalNutrition Research
Volume36
Issue number11
DOIs
Publication statusPublished - 2016
MoE publication typeA1 Journal article-refereed

Fingerprint

Vaccinium myrtillus
Adenoma
Energy Metabolism
Immunity
Growth
Genes
Intestinal Mucosa
Fruit
Down-Regulation
Lymphocytes
Inflammation
T-Lymphocytes
Anthocyanins
Polyphenols
Regulatory T-Lymphocytes
Gastrointestinal Microbiome
Transcriptome
Electrophoresis
B-Lymphocytes
Gels

Keywords

  • adenomatous
  • polyposis coli
  • polyphenols
  • regulatory T lymphocytes
  • microbiota
  • gene expression
  • mice

Cite this

Päivärinta, Essi ; Niku, Mikael ; Maukonen, Johanna ; Storvik, Markus ; Heiman-Lindh, Anu ; Saarela, Maria ; Pajari, Anne-Maria ; Mutanen, Marja. / Changes in intestinal immunity, gut microbiota and expression of energy metabolism-related genes explain adenoma growth in bilberry and cloudberry-fed ApcMin mice. In: Nutrition Research. 2016 ; Vol. 36, No. 11. pp. 1285-1297.
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abstract = "We showed previously that ellagitannin-rich cloudberries and anthocyanin-rich bilberries reduce the number of intestinal adenomas in multiple intestinal neoplasia/+ (ApcMin) mice. We also found that cloudberries decreased the size of adenomas, while bilberries increased it. Here we hypothesized that the difference in adenoma growth could be explained by dissimilar effects of the berries on intestinal immune responses and gut microbiota, potentially driven by the distinct polyphenol compositions of the two berries. Our objective was to investigate lymphocyte subtypes and the predominant cecal bacterial diversity in mice fed with bilberries and cloudberries, and to analyze global gene expression profiles in the intestinal mucosa. Immunostainings of CD3+ T lymphocytes, FoxP3+ regulatory T lymphocytes and CD45R+ B lymphocytes revealed a smaller ratio of intraepithelial to all mucosal CD3+ T lymphocytes in the cloudberry-fed mice compared to controls, suggesting an attenuation of inflammation. Bilberry feeding induced no changes in the density of any of the lymphocyte subtypes. The predominant bacterial diversity in cecal contents, analyzed using PCR-denaturating gradient gel electrophoresis, was higher in the bilberry group than in the control or cloudberry groups. The microbial profiles of cloudberry-fed mice clustered together and were associated with small adenoma size. Pathway analyses of gene expression data showed that cloudberry downregulated and bilberry upregulated the expression of energy metabolism-related genes in the intestinal mucosa. In conclusion, attenuation of intestinal inflammation, changes in microbial profiles and downregulation of mucosal energy metabolism may account for the smaller adenoma size in cloudberry-fed mice in comparison to bilberry-fed mice.",
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Changes in intestinal immunity, gut microbiota and expression of energy metabolism-related genes explain adenoma growth in bilberry and cloudberry-fed ApcMin mice. / Päivärinta, Essi; Niku, Mikael; Maukonen, Johanna; Storvik, Markus; Heiman-Lindh, Anu; Saarela, Maria; Pajari, Anne-Maria; Mutanen, Marja.

In: Nutrition Research, Vol. 36, No. 11, 2016, p. 1285-1297.

Research output: Contribution to journalArticleScientificpeer-review

TY - JOUR

T1 - Changes in intestinal immunity, gut microbiota and expression of energy metabolism-related genes explain adenoma growth in bilberry and cloudberry-fed ApcMin mice

AU - Päivärinta, Essi

AU - Niku, Mikael

AU - Maukonen, Johanna

AU - Storvik, Markus

AU - Heiman-Lindh, Anu

AU - Saarela, Maria

AU - Pajari, Anne-Maria

AU - Mutanen, Marja

PY - 2016

Y1 - 2016

N2 - We showed previously that ellagitannin-rich cloudberries and anthocyanin-rich bilberries reduce the number of intestinal adenomas in multiple intestinal neoplasia/+ (ApcMin) mice. We also found that cloudberries decreased the size of adenomas, while bilberries increased it. Here we hypothesized that the difference in adenoma growth could be explained by dissimilar effects of the berries on intestinal immune responses and gut microbiota, potentially driven by the distinct polyphenol compositions of the two berries. Our objective was to investigate lymphocyte subtypes and the predominant cecal bacterial diversity in mice fed with bilberries and cloudberries, and to analyze global gene expression profiles in the intestinal mucosa. Immunostainings of CD3+ T lymphocytes, FoxP3+ regulatory T lymphocytes and CD45R+ B lymphocytes revealed a smaller ratio of intraepithelial to all mucosal CD3+ T lymphocytes in the cloudberry-fed mice compared to controls, suggesting an attenuation of inflammation. Bilberry feeding induced no changes in the density of any of the lymphocyte subtypes. The predominant bacterial diversity in cecal contents, analyzed using PCR-denaturating gradient gel electrophoresis, was higher in the bilberry group than in the control or cloudberry groups. The microbial profiles of cloudberry-fed mice clustered together and were associated with small adenoma size. Pathway analyses of gene expression data showed that cloudberry downregulated and bilberry upregulated the expression of energy metabolism-related genes in the intestinal mucosa. In conclusion, attenuation of intestinal inflammation, changes in microbial profiles and downregulation of mucosal energy metabolism may account for the smaller adenoma size in cloudberry-fed mice in comparison to bilberry-fed mice.

AB - We showed previously that ellagitannin-rich cloudberries and anthocyanin-rich bilberries reduce the number of intestinal adenomas in multiple intestinal neoplasia/+ (ApcMin) mice. We also found that cloudberries decreased the size of adenomas, while bilberries increased it. Here we hypothesized that the difference in adenoma growth could be explained by dissimilar effects of the berries on intestinal immune responses and gut microbiota, potentially driven by the distinct polyphenol compositions of the two berries. Our objective was to investigate lymphocyte subtypes and the predominant cecal bacterial diversity in mice fed with bilberries and cloudberries, and to analyze global gene expression profiles in the intestinal mucosa. Immunostainings of CD3+ T lymphocytes, FoxP3+ regulatory T lymphocytes and CD45R+ B lymphocytes revealed a smaller ratio of intraepithelial to all mucosal CD3+ T lymphocytes in the cloudberry-fed mice compared to controls, suggesting an attenuation of inflammation. Bilberry feeding induced no changes in the density of any of the lymphocyte subtypes. The predominant bacterial diversity in cecal contents, analyzed using PCR-denaturating gradient gel electrophoresis, was higher in the bilberry group than in the control or cloudberry groups. The microbial profiles of cloudberry-fed mice clustered together and were associated with small adenoma size. Pathway analyses of gene expression data showed that cloudberry downregulated and bilberry upregulated the expression of energy metabolism-related genes in the intestinal mucosa. In conclusion, attenuation of intestinal inflammation, changes in microbial profiles and downregulation of mucosal energy metabolism may account for the smaller adenoma size in cloudberry-fed mice in comparison to bilberry-fed mice.

KW - adenomatous

KW - polyposis coli

KW - polyphenols

KW - regulatory T lymphocytes

KW - microbiota

KW - gene expression

KW - mice

U2 - 10.1016/j.nutres.2016.10.003

DO - 10.1016/j.nutres.2016.10.003

M3 - Article

VL - 36

SP - 1285

EP - 1297

JO - Nutrition Research

JF - Nutrition Research

SN - 0271-5317

IS - 11

ER -