Hematopoietic Stem Cell-Derived Adipocytes Modulate Adipose Tissue Cellularity, Leptin Production and Insulin Responsiveness in Female Mice

A subpopulation of adipocytes in the major adipose depots of mice is produced from hematopoietic stem cells rather than mesenchymal progenitors that are the source of conventional white and brown/beige adipocytes. To analyze the impact of hematopoietic stem cell-derived adipocytes (HSCDAs) in the ad...

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Published inFrontiers in endocrinology (Lausanne) Vol. 13; p. 844877
Main Authors Gavin, Kathleen M, Sullivan, Timothy M, Maltzahn, Joanne K, Jackman, Matthew R, Libby, Andrew E, MacLean, Paul S, Kohrt, Wendy M, Majka, Susan M, Klemm, Dwight J
Format Journal Article
LanguageEnglish
Published Switzerland Frontiers Media S.A 03.06.2022
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Abstract A subpopulation of adipocytes in the major adipose depots of mice is produced from hematopoietic stem cells rather than mesenchymal progenitors that are the source of conventional white and brown/beige adipocytes. To analyze the impact of hematopoietic stem cell-derived adipocytes (HSCDAs) in the adipose niche we transplanted HSCs in which expression of a diphtheria toxin gene was under the control of the adipocyte-specific adiponectin gene promoter into irradiated wild type recipients. Thus, only adipocytes produced from HSC would be ablated while conventional white and brown adipocytes produced from mesenchymal progenitor cells would be spared. Wild type mice transplanted with HSCs from mice containing a reporter gene, but not the diphtheria toxin gene, regulated by the adiponectin gene promoter served as controls. In mice in which HSCDA production was suppressed, adipocyte size declined while adipose depot weights were unchanged and the number of conventional adipocyte progenitors significantly increased. We also measured a paradoxical increase in circulating leptin levels while physical activity was significantly decreased in the HSCDA depleted mice. Finally, insulin sensitivity was significantly reduced in HSCDA depleted mice. In contrast, loss of HSCDA production had no effect on body weight, components of energy balance, or levels of several circulating adipokines and tissue-resident inflammatory cells. These data indicate that ablation of this low-abundance subpopulation of adipocytes is associated with changes in circulating leptin levels and leptin-regulated endpoints associated with adipose tissue function. How they do so remains a mystery, but our results highlight the need for additional studies to explore the role of HSCDAs in other physiologic contexts such as obesity, metabolic dysfunction or loss of sex hormone production.
AbstractList A subpopulation of adipocytes in the major adipose depots of mice is produced from hematopoietic stem cells rather than mesenchymal progenitors that are the source of conventional white and brown/beige adipocytes. To analyze the impact of hematopoietic stem cell-derived adipocytes (HSCDAs) in the adipose niche we transplanted HSCs in which expression of a diphtheria toxin gene was under the control of the adipocyte-specific adiponectin gene promoter into irradiated wild type recipients. Thus, only adipocytes produced from HSC would be ablated while conventional white and brown adipocytes produced from mesenchymal progenitor cells would be spared. Wild type mice transplanted with HSCs from mice containing a reporter gene, but not the diphtheria toxin gene, regulated by the adiponectin gene promoter served as controls. In mice in which HSCDA production was suppressed, adipocyte size declined while adipose depot weights were unchanged and the number of conventional adipocyte progenitors significantly increased. We also measured a paradoxical increase in circulating leptin levels while physical activity was significantly decreased in the HSCDA depleted mice. Finally, insulin sensitivity was significantly reduced in HSCDA depleted mice. In contrast, loss of HSCDA production had no effect on body weight, components of energy balance, or levels of several circulating adipokines and tissue-resident inflammatory cells. These data indicate that ablation of this low-abundance subpopulation of adipocytes is associated with changes in circulating leptin levels and leptin-regulated endpoints associated with adipose tissue function. How they do so remains a mystery, but our results highlight the need for additional studies to explore the role of HSCDAs in other physiologic contexts such as obesity, metabolic dysfunction or loss of sex hormone production.
Author Majka, Susan M
Klemm, Dwight J
MacLean, Paul S
Sullivan, Timothy M
Kohrt, Wendy M
Gavin, Kathleen M
Maltzahn, Joanne K
Jackman, Matthew R
Libby, Andrew E
AuthorAffiliation 4 Division of Endocrinology, Department of Medicine, University of Colorado Anschutz Medical Campus , Aurora, CO , United States
5 Division of Pulmonary, Critical Care and Sleep Medicine, Department of Biomedical Research, National Jewish Health , Denver, CO , United States
1 Geriatric Research, Education and Clinical Center, Rocky Mountain Regional Veterans Administration (VA) Medical Center , Aurora, CO , United States
3 Cardiovascular Pulmonary Research Laboratory, University of Colorado Anschutz Medical Campus , Aurora, CO , United States
6 Charles C. Gates Center for Regenerative Medicine and Stem Cell Biology, University of Colorado Anschutz Medical Campus , Aurora, CO , United States
2 Division of Geriatric Medicine, Department of Medicine, University of Colorado Anschutz Medical Campus , Aurora, CO , United States
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Copyright Copyright © 2022 Gavin, Sullivan, Maltzahn, Jackman, Libby, MacLean, Kohrt, Majka and Klemm.
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Keywords cellularity
insulin resistance
leptin
ablation
adipocyte
physical activity
Language English
License Copyright © 2022 Gavin, Sullivan, Maltzahn, Jackman, Libby, MacLean, Kohrt, Majka and Klemm.
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.
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Notes Reviewed by: Ziru Li, University of Michigan, United States; Jacqueline M. Stephens, Louisiana State University, United States; Friederike Behler-Janbeck, University Medical Center Hamburg-Eppendorf, Germany
Edited by: Carla Lubrano, Sapienza University of Rome, Italy
This article was submitted to Obesity, a section of the journal Frontiers in Endocrinology
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Snippet A subpopulation of adipocytes in the major adipose depots of mice is produced from hematopoietic stem cells rather than mesenchymal progenitors that are the...
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SubjectTerms ablation
adipocyte
Adipocytes - metabolism
Adiponectin - genetics
Adiponectin - metabolism
Adipose Tissue - metabolism
Animals
cellularity
Diphtheria Toxin
Endocrinology
Female
Hematopoietic Stem Cells
Insulin - metabolism
insulin resistance
leptin
Leptin - metabolism
Mice
physical activity
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Title Hematopoietic Stem Cell-Derived Adipocytes Modulate Adipose Tissue Cellularity, Leptin Production and Insulin Responsiveness in Female Mice
URI https://www.ncbi.nlm.nih.gov/pubmed/35721743
https://pubmed.ncbi.nlm.nih.gov/PMC9203959
https://doaj.org/article/22273c03c9774595ab400ccd5f58462a
Volume 13
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