Gut Dysbiosis and Adaptive Immune Response in Diet-induced Obesity vs. Systemic Inflammation

A mutual interplay exists between adaptive immune system and gut microbiota. Altered gut microbial ecosystems are associated with the metabolic syndrome, occurring in most obese individuals. However, it is unknown why 10–25% of obese individuals are metabolically healthy, while normal weight individ...

Full description

Bibliographic Details
Main Authors: Jana Pindjakova, Claudio Sartini, Oriana Lo Re, Francesca Rappa, Berengere Coupe, Benjamin Lelouvier, Valerio Pazienza, Manlio Vinciguerra
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-06-01
Series:Frontiers in Microbiology
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fmicb.2017.01157/full
_version_ 1811212139623350272
author Jana Pindjakova
Claudio Sartini
Oriana Lo Re
Francesca Rappa
Berengere Coupe
Benjamin Lelouvier
Valerio Pazienza
Manlio Vinciguerra
Manlio Vinciguerra
author_facet Jana Pindjakova
Claudio Sartini
Oriana Lo Re
Francesca Rappa
Berengere Coupe
Benjamin Lelouvier
Valerio Pazienza
Manlio Vinciguerra
Manlio Vinciguerra
author_sort Jana Pindjakova
collection DOAJ
description A mutual interplay exists between adaptive immune system and gut microbiota. Altered gut microbial ecosystems are associated with the metabolic syndrome, occurring in most obese individuals. However, it is unknown why 10–25% of obese individuals are metabolically healthy, while normal weight individuals can develop inflammation and atherosclerosis. We modeled these specific metabolic conditions in mice fed with a chow diet, an obesogenic but not inflammatory diet—mimicking healthy obesity, or Paigen diet—mimicking inflammation in the lean subjects. We analyzed a range of markers and cytokines in the aorta, heart, abdominal fat, liver and spleen, and metagenomics analyses were performed on stool samples. T lymphocytes infiltration was found in the aorta and in the liver upon both diets, however a significant increase in CD4+ and CD8+ cells was found only in the heart of Paigen-fed animals, paralleled by increased expression of IL-1, IL-4, IL-6, IL-17, and IFN-γ. Bacteroidia, Deltaproteobacteria, and Verrucomicrobia dominated in mice fed Paigen diet, while Gammaproteobacteria, Delataproteobacteria, and Erysipelotrichia were more abundant in obese mice. Mice reproducing human metabolic exceptions displayed gut microbiota phylogenetically distinct from normal diet-fed mice, and correlated with specific adaptive immune responses. Diet composition thus has a pervasive role in co-regulating adaptive immunity and the diversity of microbiota.
first_indexed 2024-04-12T05:24:54Z
format Article
id doaj.art-a357ab91faf84d5b9ede6fe2f64b7c71
institution Directory Open Access Journal
issn 1664-302X
language English
last_indexed 2024-04-12T05:24:54Z
publishDate 2017-06-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Microbiology
spelling doaj.art-a357ab91faf84d5b9ede6fe2f64b7c712022-12-22T03:46:20ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2017-06-01810.3389/fmicb.2017.01157277160Gut Dysbiosis and Adaptive Immune Response in Diet-induced Obesity vs. Systemic InflammationJana Pindjakova0Claudio Sartini1Oriana Lo Re2Francesca Rappa3Berengere Coupe4Benjamin Lelouvier5Valerio Pazienza6Manlio Vinciguerra7Manlio Vinciguerra8Center for Translational Medicine, International Clinical Research Center, St. Anne's University HospitalBrno, CzechiaDepartment of Primary Care and Population Health, University College LondonLondon, United KingdomCenter for Translational Medicine, International Clinical Research Center, St. Anne's University HospitalBrno, CzechiaSection of Human Anatomy, Department of Experimental Biomedicine and Clinical Neurosciences, University of PalermoPalermo, ItalyVaiomerLabège, FranceVaiomerLabège, FranceGastroenterology Unit, IRCCS “Casa Sollievo della Sofferenza” HospitalSan Giovanni Rotondo, ItalyCenter for Translational Medicine, International Clinical Research Center, St. Anne's University HospitalBrno, CzechiaDivision of Medicine, Institute for Liver and Digestive Health, University College LondonLondon, United KingdomA mutual interplay exists between adaptive immune system and gut microbiota. Altered gut microbial ecosystems are associated with the metabolic syndrome, occurring in most obese individuals. However, it is unknown why 10–25% of obese individuals are metabolically healthy, while normal weight individuals can develop inflammation and atherosclerosis. We modeled these specific metabolic conditions in mice fed with a chow diet, an obesogenic but not inflammatory diet—mimicking healthy obesity, or Paigen diet—mimicking inflammation in the lean subjects. We analyzed a range of markers and cytokines in the aorta, heart, abdominal fat, liver and spleen, and metagenomics analyses were performed on stool samples. T lymphocytes infiltration was found in the aorta and in the liver upon both diets, however a significant increase in CD4+ and CD8+ cells was found only in the heart of Paigen-fed animals, paralleled by increased expression of IL-1, IL-4, IL-6, IL-17, and IFN-γ. Bacteroidia, Deltaproteobacteria, and Verrucomicrobia dominated in mice fed Paigen diet, while Gammaproteobacteria, Delataproteobacteria, and Erysipelotrichia were more abundant in obese mice. Mice reproducing human metabolic exceptions displayed gut microbiota phylogenetically distinct from normal diet-fed mice, and correlated with specific adaptive immune responses. Diet composition thus has a pervasive role in co-regulating adaptive immunity and the diversity of microbiota.http://journal.frontiersin.org/article/10.3389/fmicb.2017.01157/fullobesityinflammationgut microbiotaadaptive immune system
spellingShingle Jana Pindjakova
Claudio Sartini
Oriana Lo Re
Francesca Rappa
Berengere Coupe
Benjamin Lelouvier
Valerio Pazienza
Manlio Vinciguerra
Manlio Vinciguerra
Gut Dysbiosis and Adaptive Immune Response in Diet-induced Obesity vs. Systemic Inflammation
Frontiers in Microbiology
obesity
inflammation
gut microbiota
adaptive immune system
title Gut Dysbiosis and Adaptive Immune Response in Diet-induced Obesity vs. Systemic Inflammation
title_full Gut Dysbiosis and Adaptive Immune Response in Diet-induced Obesity vs. Systemic Inflammation
title_fullStr Gut Dysbiosis and Adaptive Immune Response in Diet-induced Obesity vs. Systemic Inflammation
title_full_unstemmed Gut Dysbiosis and Adaptive Immune Response in Diet-induced Obesity vs. Systemic Inflammation
title_short Gut Dysbiosis and Adaptive Immune Response in Diet-induced Obesity vs. Systemic Inflammation
title_sort gut dysbiosis and adaptive immune response in diet induced obesity vs systemic inflammation
topic obesity
inflammation
gut microbiota
adaptive immune system
url http://journal.frontiersin.org/article/10.3389/fmicb.2017.01157/full
work_keys_str_mv AT janapindjakova gutdysbiosisandadaptiveimmuneresponseindietinducedobesityvssystemicinflammation
AT claudiosartini gutdysbiosisandadaptiveimmuneresponseindietinducedobesityvssystemicinflammation
AT orianalore gutdysbiosisandadaptiveimmuneresponseindietinducedobesityvssystemicinflammation
AT francescarappa gutdysbiosisandadaptiveimmuneresponseindietinducedobesityvssystemicinflammation
AT berengerecoupe gutdysbiosisandadaptiveimmuneresponseindietinducedobesityvssystemicinflammation
AT benjaminlelouvier gutdysbiosisandadaptiveimmuneresponseindietinducedobesityvssystemicinflammation
AT valeriopazienza gutdysbiosisandadaptiveimmuneresponseindietinducedobesityvssystemicinflammation
AT manliovinciguerra gutdysbiosisandadaptiveimmuneresponseindietinducedobesityvssystemicinflammation
AT manliovinciguerra gutdysbiosisandadaptiveimmuneresponseindietinducedobesityvssystemicinflammation