Adipose tissue natriuretic peptide receptor expression is related to insulin sensitivity in obesity and diabetes
Objective Cardiac natriuretic peptides (NPs) bind to two receptors (NPRA‐mediator of signaling; NPRC‐clearance receptor) whose ratio, NPRR (NPRA/NPRC), determines the NP bioactivity. This study investigated the relationship of NP receptor gene expression in adipose tissue and muscle with obesity and...
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| Published in | Obesity (Silver Spring, Md.) Vol. 24; no. 4; pp. 820 - 828 |
|---|---|
| Main Authors | , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Blackwell Publishing Ltd
01.04.2016
John Wiley and Sons Inc |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1930-7381 1930-739X 1930-739X |
| DOI | 10.1002/oby.21418 |
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| Abstract | Objective
Cardiac natriuretic peptides (NPs) bind to two receptors (NPRA‐mediator of signaling; NPRC‐clearance receptor) whose ratio, NPRR (NPRA/NPRC), determines the NP bioactivity. This study investigated the relationship of NP receptor gene expression in adipose tissue and muscle with obesity and glucose intolerance. Prospectively, the study also assessed whether changes in NP receptor expression and thermogenic gene markers accompanied improvements of insulin sensitivity.
Methods
A cross‐sectional study of subjects with a wide range of BMI and glucose tolerance (n = 50) was conducted, as well as a randomized 12‐week trial of subjects with type 2 diabetes mellitus (T2DM) treated with pioglitazone (n = 9) or placebo (n = 10).
Results
NPRR mRNA was significantly lower in adipose tissue of subjects with obesity when compared with lean subjects (P ≤ 0.001). NPRR decreased with progression from normal glucose tolerance to T2DM (P < 0.01) independently of obesity. Treatment of subjects with T2DM with pioglitazone increased NPRR in adipose tissue (P ≤ 0.01) in conjunction with improvements in insulin sensitivity and increases of the thermogenic markers PPARγ coactivator‐1α and uncoupling protein 1 (P ≤ 0.01).
Conclusions
Decreased adipose tissue NPRR was associated with obesity, glucose intolerance, and insulin resistance. This relationship was not observed for skeletal muscle NPRR. Pharmacological improvement of insulin sensitivity in subjects with T2DM was tied to improvement in NPRR and increased expression of genes involved in thermogenic processes. |
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| AbstractList | Cardiac natriuretic peptides (NPs) bind to two receptors (NPRA-mediator of signaling; NPRC-clearance receptor) whose ratio, NPRR (NPRA/NPRC), determines the NP bioactivity. This study investigated the relationship of NP receptor gene expression in adipose tissue and muscle with obesity and glucose intolerance. Prospectively, the study also assessed whether changes in NP receptor expression and thermogenic gene markers accompanied improvements of insulin sensitivity.
A cross-sectional study of subjects with a wide range of BMI and glucose tolerance (n = 50) was conducted, as well as a randomized 12-week trial of subjects with type 2 diabetes mellitus (T2DM) treated with pioglitazone (n = 9) or placebo (n = 10).
NPRR mRNA was significantly lower in adipose tissue of subjects with obesity when compared with lean subjects (P ≤ 0.001). NPRR decreased with progression from normal glucose tolerance to T2DM (P < 0.01) independently of obesity. Treatment of subjects with T2DM with pioglitazone increased NPRR in adipose tissue (P ≤ 0.01) in conjunction with improvements in insulin sensitivity and increases of the thermogenic markers PPARγ coactivator-1α and uncoupling protein 1 (P ≤ 0.01).
Decreased adipose tissue NPRR was associated with obesity, glucose intolerance, and insulin resistance. This relationship was not observed for skeletal muscle NPRR. Pharmacological improvement of insulin sensitivity in subjects with T2DM was tied to improvement in NPRR and increased expression of genes involved in thermogenic processes. Objective Cardiac natriuretic peptides (NPs) bind to two receptors (NPRA‐mediator of signaling; NPRC‐clearance receptor) whose ratio, NPRR (NPRA/NPRC), determines the NP bioactivity. This study investigated the relationship of NP receptor gene expression in adipose tissue and muscle with obesity and glucose intolerance. Prospectively, the study also assessed whether changes in NP receptor expression and thermogenic gene markers accompanied improvements of insulin sensitivity. Methods A cross‐sectional study of subjects with a wide range of BMI and glucose tolerance (n = 50) was conducted, as well as a randomized 12‐week trial of subjects with type 2 diabetes mellitus (T2DM) treated with pioglitazone (n = 9) or placebo (n = 10). Results NPRR mRNA was significantly lower in adipose tissue of subjects with obesity when compared with lean subjects (P ≤ 0.001). NPRR decreased with progression from normal glucose tolerance to T2DM (P < 0.01) independently of obesity. Treatment of subjects with T2DM with pioglitazone increased NPRR in adipose tissue (P ≤ 0.01) in conjunction with improvements in insulin sensitivity and increases of the thermogenic markers PPARγ coactivator‐1α and uncoupling protein 1 (P ≤ 0.01). Conclusions Decreased adipose tissue NPRR was associated with obesity, glucose intolerance, and insulin resistance. This relationship was not observed for skeletal muscle NPRR. Pharmacological improvement of insulin sensitivity in subjects with T2DM was tied to improvement in NPRR and increased expression of genes involved in thermogenic processes. Cardiac natriuretic peptides (NPs) bind to two receptors (NPRA-mediator of signaling; NPRC-clearance receptor) whose ratio, NPRR (NPRA/NPRC), determines the NP bioactivity. This study investigated the relationship of NP receptor gene expression in adipose tissue and muscle with obesity and glucose intolerance. Prospectively, the study also assessed whether changes in NP receptor expression and thermogenic gene markers accompanied improvements of insulin sensitivity. A cross-sectional study of subjects with a wide range of BMI and glucose tolerance (n = 50) was conducted, as well as a randomized 12-week trial of subjects with type 2 diabetes mellitus (T2DM) treated with pioglitazone (n = 9) or placebo (n = 10). NPRR mRNA was significantly lower in adipose tissue of subjects with obesity when compared with lean subjects (P ≤ 0.001). NPRR decreased with progression from normal glucose tolerance to T2DM (P < 0.01) independently of obesity. Treatment of subjects with T2DM with pioglitazone increased NPRR in adipose tissue (P ≤ 0.01) in conjunction with improvements in insulin sensitivity and increases of the thermogenic markers PPARγ coactivator-1α and uncoupling protein 1 (P ≤ 0.01). Decreased adipose tissue NPRR was associated with obesity, glucose intolerance, and insulin resistance. This relationship was not observed for skeletal muscle NPRR. Pharmacological improvement of insulin sensitivity in subjects with T2DM was tied to improvement in NPRR and increased expression of genes involved in thermogenic processes. Cardiac natriuretic peptides (NPs) bind to two receptors (NPRA-mediator of signaling; NPRC-clearance receptor) whose ratio, NPRR (NPRA/NPRC), determines the NP bioactivity. This study investigated the relationship of NP receptor gene expression in adipose tissue and muscle with obesity and glucose intolerance. Prospectively, the study also assessed whether changes in NP receptor expression and thermogenic gene markers accompanied improvements of insulin sensitivity.OBJECTIVECardiac natriuretic peptides (NPs) bind to two receptors (NPRA-mediator of signaling; NPRC-clearance receptor) whose ratio, NPRR (NPRA/NPRC), determines the NP bioactivity. This study investigated the relationship of NP receptor gene expression in adipose tissue and muscle with obesity and glucose intolerance. Prospectively, the study also assessed whether changes in NP receptor expression and thermogenic gene markers accompanied improvements of insulin sensitivity.A cross-sectional study of subjects with a wide range of BMI and glucose tolerance (n = 50) was conducted, as well as a randomized 12-week trial of subjects with type 2 diabetes mellitus (T2DM) treated with pioglitazone (n = 9) or placebo (n = 10).METHODSA cross-sectional study of subjects with a wide range of BMI and glucose tolerance (n = 50) was conducted, as well as a randomized 12-week trial of subjects with type 2 diabetes mellitus (T2DM) treated with pioglitazone (n = 9) or placebo (n = 10).NPRR mRNA was significantly lower in adipose tissue of subjects with obesity when compared with lean subjects (P ≤ 0.001). NPRR decreased with progression from normal glucose tolerance to T2DM (P < 0.01) independently of obesity. Treatment of subjects with T2DM with pioglitazone increased NPRR in adipose tissue (P ≤ 0.01) in conjunction with improvements in insulin sensitivity and increases of the thermogenic markers PPARγ coactivator-1α and uncoupling protein 1 (P ≤ 0.01).RESULTSNPRR mRNA was significantly lower in adipose tissue of subjects with obesity when compared with lean subjects (P ≤ 0.001). NPRR decreased with progression from normal glucose tolerance to T2DM (P < 0.01) independently of obesity. Treatment of subjects with T2DM with pioglitazone increased NPRR in adipose tissue (P ≤ 0.01) in conjunction with improvements in insulin sensitivity and increases of the thermogenic markers PPARγ coactivator-1α and uncoupling protein 1 (P ≤ 0.01).Decreased adipose tissue NPRR was associated with obesity, glucose intolerance, and insulin resistance. This relationship was not observed for skeletal muscle NPRR. Pharmacological improvement of insulin sensitivity in subjects with T2DM was tied to improvement in NPRR and increased expression of genes involved in thermogenic processes.CONCLUSIONSDecreased adipose tissue NPRR was associated with obesity, glucose intolerance, and insulin resistance. This relationship was not observed for skeletal muscle NPRR. Pharmacological improvement of insulin sensitivity in subjects with T2DM was tied to improvement in NPRR and increased expression of genes involved in thermogenic processes. |
| Author | Wei, Wan Kovacova, Zuzana Pratley, Richard E. Tharp, William G. Collins, Sheila Liu, Dianxin Xie, Hui |
| AuthorAffiliation | 1 Translational Research Institute for Metabolism and Diabetes Florida Hospital Orlando Florida USA 2 Division of Endocrinology, Diabetes and Metabolism University of Vermont College of Medicine Burlington Vermont USA 3 Center for Metabolic Origins of Disease Sanford Burnham Prebys Medical Discovery Institute Orlando Florida USA |
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| Author_xml | – sequence: 1 givenname: Zuzana surname: Kovacova fullname: Kovacova, Zuzana organization: Florida Hospital – sequence: 2 givenname: William G. surname: Tharp fullname: Tharp, William G. organization: University of Vermont College of Medicine – sequence: 3 givenname: Dianxin surname: Liu fullname: Liu, Dianxin organization: Sanford Burnham Prebys Medical Discovery Institute – sequence: 4 givenname: Wan surname: Wei fullname: Wei, Wan organization: Sanford Burnham Prebys Medical Discovery Institute – sequence: 5 givenname: Hui surname: Xie fullname: Xie, Hui organization: Florida Hospital – sequence: 6 givenname: Sheila surname: Collins fullname: Collins, Sheila organization: Sanford Burnham Prebys Medical Discovery Institute – sequence: 7 givenname: Richard E. surname: Pratley fullname: Pratley, Richard E. organization: Sanford Burnham Prebys Medical Discovery Institute |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/26887289$$D View this record in MEDLINE/PubMed |
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| Copyright | 2016 The Authors Obesity published by Wiley Periodicals, Inc. on behalf of The Obesity Society (TOS) 2016 The Authors Obesity published by Wiley Periodicals, Inc. on behalf of The Obesity Society (TOS). Copyright Blackwell Publishing Ltd. Apr 2016 |
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| Keywords | adipose tissue type 2 diabetes mellitus natriuretic peptide receptors obesity |
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| Notes | Z.K. performed experiments, researched and analyzed the data, and wrote the manuscript. W.G.T. assisted in the conduct of the clinical study 2 and data analysis. H.X. performed the statistical data analysis. W.W. and D.L. performed experiments. S.C. contributed to study design and discussions and reviewed and edited the manuscript. R.E.P. designed and conducted the clinical studies, reviewed/edited the manuscript, and contributed to discussion. R.E.P. and S.C. are the guarantors of this work, have full access to the data in the study, and take responsibility for the integrity of the data and the accuracy of the data analysis. ClinicalTrials.gov Clinical trial registration identifier NCT00656864 R.E.P. has received research funding from Takeda Pharmaceuticals USA, Inc. S.C. has received research funding from Novo Nordisk and AstraZeneca. The other authors declared no conflict of interest. This work was supported by institutional funds from Florida Hospital Translational Research Institute for Metabolism and Diabetes; institutional funds from Sanford Burnham Prebys Medical Discovery Institute; and an investigator initiated grant from Takeda Pharmaceuticals USA, Inc. : Disclosure Funding agencies Author contributions SourceType-Scholarly Journals-1 ObjectType-Feature-1 content type line 14 ObjectType-Article-1 ObjectType-Feature-2 content type line 23 ObjectType-Undefined-3 Funding agencies: This work was supported by institutional funds from Florida Hospital Translational Research Institute for Metabolism and Diabetes; institutional funds from Sanford Burnham Prebys Medical Discovery Institute; and an investigator initiated grant from Takeda Pharmaceuticals USA, Inc. Author contributions: Z.K. performed experiments, researched and analyzed the data, and wrote the manuscript. W.G.T. assisted in the conduct of the clinical study 2 and data analysis. H.X. performed the statistical data analysis. W.W. and D.L. performed experiments. S.C. contributed to study design and discussions and reviewed and edited the manuscript. R.E.P. designed and conducted the clinical studies, reviewed/edited the manuscript, and contributed to discussion. R.E.P. and S.C. are the guarantors of this work, have full access to the data in the study, and take responsibility for the integrity of the data and the accuracy of the data analysis. Clinical trial registration: ClinicalTrials.gov identifier NCT00656864 Disclosure: R.E.P. has received research funding from Takeda Pharmaceuticals USA, Inc. S.C. has received research funding from Novo Nordisk and AstraZeneca. The other authors declared no conflict of interest. |
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Cardiac natriuretic peptides (NPs) bind to two receptors (NPRA‐mediator of signaling; NPRC‐clearance receptor) whose ratio, NPRR (NPRA/NPRC),... Cardiac natriuretic peptides (NPs) bind to two receptors (NPRA-mediator of signaling; NPRC-clearance receptor) whose ratio, NPRR (NPRA/NPRC), determines the NP... |
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| SubjectTerms | adipose tissue Adult Body fat Cross-Sectional Studies Diabetes Mellitus, Type 2 - drug therapy Diabetes Mellitus, Type 2 - metabolism Diabetes Mellitus, Type 2 - physiopathology Female Glucose Humans Hypoglycemic Agents - therapeutic use Insulin resistance Insulin Resistance - physiology Kinases Male Metabolic disorders Middle Aged natriuretic peptide receptors Obesity Obesity - metabolism Obesity - physiopathology Original Receptors, Atrial Natriuretic Factor - analysis Receptors, Atrial Natriuretic Factor - metabolism Rodents Thiazolidinediones - therapeutic use type 2 diabetes mellitus |
| Title | Adipose tissue natriuretic peptide receptor expression is related to insulin sensitivity in obesity and diabetes |
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