Adipose tissue macrophages impair preadipocyte differentiation in humans.
AIM:The physiologic mechanisms underlying the relationship between obesity and insulin resistance are not fully understood. Impaired adipocyte differentiation and localized inflammation characterize adipose tissue from obese, insulin-resistant humans. The directionality of this relationship is not k...
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2017-01-01
|
| Series: | PLoS ONE |
| Online Access: | http://europepmc.org/articles/PMC5289462?pdf=render |
| _version_ | 1818318129269309440 |
|---|---|
| author | Li Fen Liu Colleen M Craig Lorna L Tolentino Okmi Choi John Morton Homero Rivas Samuel W Cushman Edgar G Engleman Tracey McLaughlin |
| author_facet | Li Fen Liu Colleen M Craig Lorna L Tolentino Okmi Choi John Morton Homero Rivas Samuel W Cushman Edgar G Engleman Tracey McLaughlin |
| author_sort | Li Fen Liu |
| collection | DOAJ |
| description | AIM:The physiologic mechanisms underlying the relationship between obesity and insulin resistance are not fully understood. Impaired adipocyte differentiation and localized inflammation characterize adipose tissue from obese, insulin-resistant humans. The directionality of this relationship is not known, however. The aim of the current study was to investigate whether adipose tissue inflammation is causally-related to impaired adipocyte differentiation. METHODS:Abdominal subcutaneous(SAT) and visceral(VAT) adipose tissue was obtained from 20 human participants undergoing bariatric surgery. Preadipocytes were isolated, and cultured in the presence or absence of CD14+ macrophages obtained from the same adipose tissue sample. Adipocyte differentiation was quantified after 14 days via immunofluorescence, Oil-Red O, and adipogenic gene expression. Cytokine secretion by mature adipocytes cultured with or without CD14+macrophages was quantified. RESULTS:Adipocyte differentiation was significantly lower in VAT than SAT by all measures (p<0.001). With macrophage removal, SAT preadipocyte differentiation increased significantly as measured by immunofluorescence and gene expression, whereas VAT preadipocyte differentiation was unchanged. Adipocyte-secreted proinflammatory cytokines were higher and adiponectin lower in media from VAT vs SAT: macrophage removal reduced inflammatory cytokine and increased adiponectin secretion from both SAT and VAT adipocytes. Differentiation of preadipocytes from SAT but not VAT correlated inversely with systemic insulin resistance. CONCLUSIONS:The current results reveal that proinflammatory immune cells in human SAT are causally-related to impaired preadipocyte differentiation, which in turn is associated with systemic insulin resistance. In VAT, preadipocyte differentiation is poor even in the absence of tissue macrophages, pointing to inherent differences in fat storage potential between the two depots. |
| first_indexed | 2024-12-13T09:48:18Z |
| format | Article |
| id | doaj.art-32aeb8c8d27e4a08a2e885651ba423ef |
| institution | Directory Open Access Journal |
| issn | 1932-6203 |
| language | English |
| last_indexed | 2024-12-13T09:48:18Z |
| publishDate | 2017-01-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS ONE |
| spelling | doaj.art-32aeb8c8d27e4a08a2e885651ba423ef2022-12-21T23:51:59ZengPublic Library of Science (PLoS)PLoS ONE1932-62032017-01-01122e017072810.1371/journal.pone.0170728Adipose tissue macrophages impair preadipocyte differentiation in humans.Li Fen LiuColleen M CraigLorna L TolentinoOkmi ChoiJohn MortonHomero RivasSamuel W CushmanEdgar G EnglemanTracey McLaughlinAIM:The physiologic mechanisms underlying the relationship between obesity and insulin resistance are not fully understood. Impaired adipocyte differentiation and localized inflammation characterize adipose tissue from obese, insulin-resistant humans. The directionality of this relationship is not known, however. The aim of the current study was to investigate whether adipose tissue inflammation is causally-related to impaired adipocyte differentiation. METHODS:Abdominal subcutaneous(SAT) and visceral(VAT) adipose tissue was obtained from 20 human participants undergoing bariatric surgery. Preadipocytes were isolated, and cultured in the presence or absence of CD14+ macrophages obtained from the same adipose tissue sample. Adipocyte differentiation was quantified after 14 days via immunofluorescence, Oil-Red O, and adipogenic gene expression. Cytokine secretion by mature adipocytes cultured with or without CD14+macrophages was quantified. RESULTS:Adipocyte differentiation was significantly lower in VAT than SAT by all measures (p<0.001). With macrophage removal, SAT preadipocyte differentiation increased significantly as measured by immunofluorescence and gene expression, whereas VAT preadipocyte differentiation was unchanged. Adipocyte-secreted proinflammatory cytokines were higher and adiponectin lower in media from VAT vs SAT: macrophage removal reduced inflammatory cytokine and increased adiponectin secretion from both SAT and VAT adipocytes. Differentiation of preadipocytes from SAT but not VAT correlated inversely with systemic insulin resistance. CONCLUSIONS:The current results reveal that proinflammatory immune cells in human SAT are causally-related to impaired preadipocyte differentiation, which in turn is associated with systemic insulin resistance. In VAT, preadipocyte differentiation is poor even in the absence of tissue macrophages, pointing to inherent differences in fat storage potential between the two depots.http://europepmc.org/articles/PMC5289462?pdf=render |
| spellingShingle | Li Fen Liu Colleen M Craig Lorna L Tolentino Okmi Choi John Morton Homero Rivas Samuel W Cushman Edgar G Engleman Tracey McLaughlin Adipose tissue macrophages impair preadipocyte differentiation in humans. PLoS ONE |
| title | Adipose tissue macrophages impair preadipocyte differentiation in humans. |
| title_full | Adipose tissue macrophages impair preadipocyte differentiation in humans. |
| title_fullStr | Adipose tissue macrophages impair preadipocyte differentiation in humans. |
| title_full_unstemmed | Adipose tissue macrophages impair preadipocyte differentiation in humans. |
| title_short | Adipose tissue macrophages impair preadipocyte differentiation in humans. |
| title_sort | adipose tissue macrophages impair preadipocyte differentiation in humans |
| url | http://europepmc.org/articles/PMC5289462?pdf=render |
| work_keys_str_mv | AT lifenliu adiposetissuemacrophagesimpairpreadipocytedifferentiationinhumans AT colleenmcraig adiposetissuemacrophagesimpairpreadipocytedifferentiationinhumans AT lornaltolentino adiposetissuemacrophagesimpairpreadipocytedifferentiationinhumans AT okmichoi adiposetissuemacrophagesimpairpreadipocytedifferentiationinhumans AT johnmorton adiposetissuemacrophagesimpairpreadipocytedifferentiationinhumans AT homerorivas adiposetissuemacrophagesimpairpreadipocytedifferentiationinhumans AT samuelwcushman adiposetissuemacrophagesimpairpreadipocytedifferentiationinhumans AT edgargengleman adiposetissuemacrophagesimpairpreadipocytedifferentiationinhumans AT traceymclaughlin adiposetissuemacrophagesimpairpreadipocytedifferentiationinhumans |