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Increased adipose tissue lymphatic vessel density inhibits thermogenesis through elevated neurotensin levels

During cold exposure, white adipose tissue can remodel to dissipate energy as heat under cold similar to thermogenic brown adipose tissue. This “browning” and the regulation of body temperature is under the control of neural and hormonal signaling. It was recently discovered that neurotensin, a smal...

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Autores principales: Phan, Thien T., Chakraborty, Adri, Tatum, Madison A., Lima-Orellana, Ana, Reyna, Andrea J., Rutkowski, Joseph M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9911872/
https://www.ncbi.nlm.nih.gov/pubmed/36776563
http://dx.doi.org/10.3389/fcell.2023.1100788
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author Phan, Thien T.
Chakraborty, Adri
Tatum, Madison A.
Lima-Orellana, Ana
Reyna, Andrea J.
Rutkowski, Joseph M.
author_facet Phan, Thien T.
Chakraborty, Adri
Tatum, Madison A.
Lima-Orellana, Ana
Reyna, Andrea J.
Rutkowski, Joseph M.
author_sort Phan, Thien T.
collection PubMed
description During cold exposure, white adipose tissue can remodel to dissipate energy as heat under cold similar to thermogenic brown adipose tissue. This “browning” and the regulation of body temperature is under the control of neural and hormonal signaling. It was recently discovered that neurotensin, a small neuropeptide, not only acts to inhibit thermogenesis, but also that lymphatic vessels may be a surprisingly potent source of neurotensin production. We hypothesized that the induction of adipose tissue lymphangiogenesis would therefore increase tissue neurotensin levels and impair thermogenesis. Methods: We utilized AdipoVD mice that have inducible expression of vascular endothelial growth factor (VEGF)-D, a potent lymphangiogenic stimulator, specifically in adipose tissue. Overexpression of VEGF-D induced significant lymphangiogenesis in both white and brown adipose tissues of AdipoVD mice. Results: Obese Adipo-VD mice demonstrated no differences in adipose morphology or browning under room temperature conditions compared to controls but did express significantly higher levels of neurotensin in their adipose tissues. Upon acute cold exposure, AdipoVD mice were markedly cold intolerant; inhibition of neurotensin signaling ameliorated this cold intolerance as AdipoVD mice were then able to maintain body temperature on cold challenge equivalent to their littermates. Conclusion: In total, these data demonstrate that adipose tissue lymphatic vessels are a potent paracrine source of neurotensin and that lymphangiogenesis therefore impairs the tissues’ thermogenic ability.
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spelling pubmed-99118722023-02-11 Increased adipose tissue lymphatic vessel density inhibits thermogenesis through elevated neurotensin levels Phan, Thien T. Chakraborty, Adri Tatum, Madison A. Lima-Orellana, Ana Reyna, Andrea J. Rutkowski, Joseph M. Front Cell Dev Biol Cell and Developmental Biology During cold exposure, white adipose tissue can remodel to dissipate energy as heat under cold similar to thermogenic brown adipose tissue. This “browning” and the regulation of body temperature is under the control of neural and hormonal signaling. It was recently discovered that neurotensin, a small neuropeptide, not only acts to inhibit thermogenesis, but also that lymphatic vessels may be a surprisingly potent source of neurotensin production. We hypothesized that the induction of adipose tissue lymphangiogenesis would therefore increase tissue neurotensin levels and impair thermogenesis. Methods: We utilized AdipoVD mice that have inducible expression of vascular endothelial growth factor (VEGF)-D, a potent lymphangiogenic stimulator, specifically in adipose tissue. Overexpression of VEGF-D induced significant lymphangiogenesis in both white and brown adipose tissues of AdipoVD mice. Results: Obese Adipo-VD mice demonstrated no differences in adipose morphology or browning under room temperature conditions compared to controls but did express significantly higher levels of neurotensin in their adipose tissues. Upon acute cold exposure, AdipoVD mice were markedly cold intolerant; inhibition of neurotensin signaling ameliorated this cold intolerance as AdipoVD mice were then able to maintain body temperature on cold challenge equivalent to their littermates. Conclusion: In total, these data demonstrate that adipose tissue lymphatic vessels are a potent paracrine source of neurotensin and that lymphangiogenesis therefore impairs the tissues’ thermogenic ability. Frontiers Media S.A. 2023-01-27 /pmc/articles/PMC9911872/ /pubmed/36776563 http://dx.doi.org/10.3389/fcell.2023.1100788 Text en Copyright © 2023 Phan, Chakraborty, Tatum, Lima-Orellana, Reyna and Rutkowski. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cell and Developmental Biology
Phan, Thien T.
Chakraborty, Adri
Tatum, Madison A.
Lima-Orellana, Ana
Reyna, Andrea J.
Rutkowski, Joseph M.
Increased adipose tissue lymphatic vessel density inhibits thermogenesis through elevated neurotensin levels
title Increased adipose tissue lymphatic vessel density inhibits thermogenesis through elevated neurotensin levels
title_full Increased adipose tissue lymphatic vessel density inhibits thermogenesis through elevated neurotensin levels
title_fullStr Increased adipose tissue lymphatic vessel density inhibits thermogenesis through elevated neurotensin levels
title_full_unstemmed Increased adipose tissue lymphatic vessel density inhibits thermogenesis through elevated neurotensin levels
title_short Increased adipose tissue lymphatic vessel density inhibits thermogenesis through elevated neurotensin levels
title_sort increased adipose tissue lymphatic vessel density inhibits thermogenesis through elevated neurotensin levels
topic Cell and Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9911872/
https://www.ncbi.nlm.nih.gov/pubmed/36776563
http://dx.doi.org/10.3389/fcell.2023.1100788
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