Maternal High-Fat Diet Programs White and Brown Adipose Tissues In Vivo in Mice, with Different Metabolic and Microbiota Patterns in Obesity-Susceptible or Obesity-Resistant Offspring
Maternal obesity causes metabolic dysfunction in the offspring, including dysbiosis, overeating, obesity, and type 2 diabetes. Early-life phases are fundamental for developing subcutaneous (SAT) and brown adipose tissues (BAT), handling energy excesses. Imaging of 18F-fluorodeoxyglucose by positron emission tomography (PET) and radiodensity by computerized tomography (CT) allows assessing adipose tissue (AT) whitening and browning in vivo and the underlying metabolic efficiency. Our aim was to examine these in vivo traits in SAT and BAT concerning gut microbiota composition in 1- and 6-month-old mice born to normal (NDoff) and high-fat diet-fed dams (HFDoff), accounting for body weight responses. We found low radiodensity (high lipids) in HFDoff SAT at 1 month, relating to an increased abundance of Dorea genus in the caecum and activation of the fatty acid biosynthetic pathway. Instead, low BAT radiodensity and glucose uptake were seen in adult HFDoff. Glucose was shifted in favor of BAT at 1 month and SAT at 6 months. In adults, unclassified Enterococcaceae and Rikenellaceae, and Bacillus genera were negatively related to BAT, whereas unclassified Clostridiales genera were related to SAT metabolism. Stratification of HFDoff based on weight-response, namely maternal induced obesity (MIO-HFDoff) or obesity-resistant (MIOR-HFDoff), showed sex dimorphism. Both subgroups were hyperphagic, but only obese mice had hyper-leptinemia and hyper-resistinemia, together with BAT dysfunction, whereas non-obese HFDoff had hyperglycemia and SAT hypermetabolism. In the caecum, unclassified Rikenellaceae (10-fold enrichment in MIO-HFDoff) and Clostridiales genera (4-fold deficiency in MIOR-HFDoff) were important discriminators of these two phenotypes. In conclusion, SAT whitening is an early abnormality in the offspring of HFD dams. In adult life, maternal HFD and the induced excessive food intake translates into a dimorphic phenotype involving SAT, BAT, and microbiota distinctively, reflecting maternal diet*sex interaction. This helps explain inter-individual variability in fetal programming and the higher rates of type 2 diabetes observed in adult women born to obese mothers, supporting personalized risk assessment, prevention, and treatment.
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Multidisciplinary Digital Publishing Institute
2022-09-02
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Subjects: | Adipokines, Adipose tissue, Fetal programming, Glucose uptake, Maternal high-fat diet, Microbiota, Positron emission tomography, Radiodensity, |
Online Access: | http://hdl.handle.net/10261/282888 http://dx.doi.org/10.13039/501100000780 http://dx.doi.org/10.13039/501100003407 https://api.elsevier.com/content/abstract/scopus_id/85138666067 |
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dig-iata-es-10261-2828882024-05-15T20:45:02Z Maternal High-Fat Diet Programs White and Brown Adipose Tissues In Vivo in Mice, with Different Metabolic and Microbiota Patterns in Obesity-Susceptible or Obesity-Resistant Offspring Guzzardi, Maria Angela Collado, María Carmen Panetta, Daniele Tripodi, Maria Iozzo, Patricia European Commission Ministero dell'Istruzione, dell'Università e della Ricerca 0000-0001-9574-5088 0000-0002-6204-4864 0000-0002-4184-0175 Adipokines Adipose tissue Fetal programming Glucose uptake Maternal high-fat diet Microbiota Positron emission tomography Radiodensity Maternal obesity causes metabolic dysfunction in the offspring, including dysbiosis, overeating, obesity, and type 2 diabetes. Early-life phases are fundamental for developing subcutaneous (SAT) and brown adipose tissues (BAT), handling energy excesses. Imaging of 18F-fluorodeoxyglucose by positron emission tomography (PET) and radiodensity by computerized tomography (CT) allows assessing adipose tissue (AT) whitening and browning in vivo and the underlying metabolic efficiency. Our aim was to examine these in vivo traits in SAT and BAT concerning gut microbiota composition in 1- and 6-month-old mice born to normal (NDoff) and high-fat diet-fed dams (HFDoff), accounting for body weight responses. We found low radiodensity (high lipids) in HFDoff SAT at 1 month, relating to an increased abundance of Dorea genus in the caecum and activation of the fatty acid biosynthetic pathway. Instead, low BAT radiodensity and glucose uptake were seen in adult HFDoff. Glucose was shifted in favor of BAT at 1 month and SAT at 6 months. In adults, unclassified Enterococcaceae and Rikenellaceae, and Bacillus genera were negatively related to BAT, whereas unclassified Clostridiales genera were related to SAT metabolism. Stratification of HFDoff based on weight-response, namely maternal induced obesity (MIO-HFDoff) or obesity-resistant (MIOR-HFDoff), showed sex dimorphism. Both subgroups were hyperphagic, but only obese mice had hyper-leptinemia and hyper-resistinemia, together with BAT dysfunction, whereas non-obese HFDoff had hyperglycemia and SAT hypermetabolism. In the caecum, unclassified Rikenellaceae (10-fold enrichment in MIO-HFDoff) and Clostridiales genera (4-fold deficiency in MIOR-HFDoff) were important discriminators of these two phenotypes. In conclusion, SAT whitening is an early abnormality in the offspring of HFD dams. In adult life, maternal HFD and the induced excessive food intake translates into a dimorphic phenotype involving SAT, BAT, and microbiota distinctively, reflecting maternal diet*sex interaction. This helps explain inter-individual variability in fetal programming and the higher rates of type 2 diabetes observed in adult women born to obese mothers, supporting personalized risk assessment, prevention, and treatment. P.I. acknowledges the support of the FP7-HEALTH-DORIAN project (Developmental origins of Healthy and Unhealthy Ageing: the Role of Maternal Obesity, European Commission GA #278603) and CNR Flagship Project InterOmics (Italian Ministry of Education, University and Research), as well as the JPI-HDHL-INTIMIC GUTMOM Project (ERA-NET H2020 Co-fund, project no. INTIMIC-085, Italian Ministry of Education, University and Research Decree no. 946/2019). M.C.C. would like to acknowledge the support of H2020-ERC Starting grant MAMI (ref. 639226). Peer reviewed 2022-11-15T09:34:21Z 2022-11-15T09:34:21Z 2022-09-02 artículo http://purl.org/coar/resource_type/c_6501 Metabolites 2022; 12 (9): 828 http://hdl.handle.net/10261/282888 10.3390/metabo12090828 2218-1989 http://dx.doi.org/10.13039/501100000780 http://dx.doi.org/10.13039/501100003407 36144232 2-s2.0-85138666067 https://api.elsevier.com/content/abstract/scopus_id/85138666067 en #PLACEHOLDER_PARENT_METADATA_VALUE# #PLACEHOLDER_PARENT_METADATA_VALUE# info:eu-repo/grantAgreement/EC/FP7/278603 info:eu-repo/grantAgreement/EC/H2020/639226 Metabolites Publisher's version https://doi.org/10.3390/metabo12090828 Sí open Multidisciplinary Digital Publishing Institute |
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Adipokines Adipose tissue Fetal programming Glucose uptake Maternal high-fat diet Microbiota Positron emission tomography Radiodensity Adipokines Adipose tissue Fetal programming Glucose uptake Maternal high-fat diet Microbiota Positron emission tomography Radiodensity |
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Adipokines Adipose tissue Fetal programming Glucose uptake Maternal high-fat diet Microbiota Positron emission tomography Radiodensity Adipokines Adipose tissue Fetal programming Glucose uptake Maternal high-fat diet Microbiota Positron emission tomography Radiodensity Guzzardi, Maria Angela Collado, María Carmen Panetta, Daniele Tripodi, Maria Iozzo, Patricia Maternal High-Fat Diet Programs White and Brown Adipose Tissues In Vivo in Mice, with Different Metabolic and Microbiota Patterns in Obesity-Susceptible or Obesity-Resistant Offspring |
description |
Maternal obesity causes metabolic dysfunction in the offspring, including dysbiosis, overeating, obesity, and type 2 diabetes. Early-life phases are fundamental for developing subcutaneous (SAT) and brown adipose tissues (BAT), handling energy excesses. Imaging of 18F-fluorodeoxyglucose by positron emission tomography (PET) and radiodensity by computerized tomography (CT) allows assessing adipose tissue (AT) whitening and browning in vivo and the underlying metabolic efficiency. Our aim was to examine these in vivo traits in SAT and BAT concerning gut microbiota composition in 1- and 6-month-old mice born to normal (NDoff) and high-fat diet-fed dams (HFDoff), accounting for body weight responses. We found low radiodensity (high lipids) in HFDoff SAT at 1 month, relating to an increased abundance of Dorea genus in the caecum and activation of the fatty acid biosynthetic pathway. Instead, low BAT radiodensity and glucose uptake were seen in adult HFDoff. Glucose was shifted in favor of BAT at 1 month and SAT at 6 months. In adults, unclassified Enterococcaceae and Rikenellaceae, and Bacillus genera were negatively related to BAT, whereas unclassified Clostridiales genera were related to SAT metabolism. Stratification of HFDoff based on weight-response, namely maternal induced obesity (MIO-HFDoff) or obesity-resistant (MIOR-HFDoff), showed sex dimorphism. Both subgroups were hyperphagic, but only obese mice had hyper-leptinemia and hyper-resistinemia, together with BAT dysfunction, whereas non-obese HFDoff had hyperglycemia and SAT hypermetabolism. In the caecum, unclassified Rikenellaceae (10-fold enrichment in MIO-HFDoff) and Clostridiales genera (4-fold deficiency in MIOR-HFDoff) were important discriminators of these two phenotypes. In conclusion, SAT whitening is an early abnormality in the offspring of HFD dams. In adult life, maternal HFD and the induced excessive food intake translates into a dimorphic phenotype involving SAT, BAT, and microbiota distinctively, reflecting maternal diet*sex interaction. This helps explain inter-individual variability in fetal programming and the higher rates of type 2 diabetes observed in adult women born to obese mothers, supporting personalized risk assessment, prevention, and treatment. |
author2 |
European Commission |
author_facet |
European Commission Guzzardi, Maria Angela Collado, María Carmen Panetta, Daniele Tripodi, Maria Iozzo, Patricia |
format |
artículo |
topic_facet |
Adipokines Adipose tissue Fetal programming Glucose uptake Maternal high-fat diet Microbiota Positron emission tomography Radiodensity |
author |
Guzzardi, Maria Angela Collado, María Carmen Panetta, Daniele Tripodi, Maria Iozzo, Patricia |
author_sort |
Guzzardi, Maria Angela |
title |
Maternal High-Fat Diet Programs White and Brown Adipose Tissues In Vivo in Mice, with Different Metabolic and Microbiota Patterns in Obesity-Susceptible or Obesity-Resistant Offspring |
title_short |
Maternal High-Fat Diet Programs White and Brown Adipose Tissues In Vivo in Mice, with Different Metabolic and Microbiota Patterns in Obesity-Susceptible or Obesity-Resistant Offspring |
title_full |
Maternal High-Fat Diet Programs White and Brown Adipose Tissues In Vivo in Mice, with Different Metabolic and Microbiota Patterns in Obesity-Susceptible or Obesity-Resistant Offspring |
title_fullStr |
Maternal High-Fat Diet Programs White and Brown Adipose Tissues In Vivo in Mice, with Different Metabolic and Microbiota Patterns in Obesity-Susceptible or Obesity-Resistant Offspring |
title_full_unstemmed |
Maternal High-Fat Diet Programs White and Brown Adipose Tissues In Vivo in Mice, with Different Metabolic and Microbiota Patterns in Obesity-Susceptible or Obesity-Resistant Offspring |
title_sort |
maternal high-fat diet programs white and brown adipose tissues in vivo in mice, with different metabolic and microbiota patterns in obesity-susceptible or obesity-resistant offspring |
publisher |
Multidisciplinary Digital Publishing Institute |
publishDate |
2022-09-02 |
url |
http://hdl.handle.net/10261/282888 http://dx.doi.org/10.13039/501100000780 http://dx.doi.org/10.13039/501100003407 https://api.elsevier.com/content/abstract/scopus_id/85138666067 |
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