Depot-specific mRNA expression programs in human adipocytes suggest physiological specialization via distinct developmental programs
Adipose tissue is distributed in diverse locations throughout the human body. Not much is known about the extent to which anatomically distinct adipose depots are functionally distinct, specialized organs, nor whether depot-specific characteristics result from intrinsic developmental programs, as op...
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| description | Adipose tissue is distributed in diverse locations throughout the human body. Not much is known about the extent to which anatomically distinct adipose depots are functionally distinct, specialized organs, nor whether depot-specific characteristics result from intrinsic developmental programs, as opposed to reversible physiological responses to differences in tissue microenvironment. We used DNA microarrays to compare mRNA expression patterns of isolated human adipocytes and cultured adipose stem cells, before and after ex vivo adipocyte differentiation, from seven anatomically diverse adipose tissue depots. Adipocytes from different depots display distinct gene expression programs, which are most closely shared with anatomically related depots. mRNAs whose expression differs between anatomically diverse groups of depots (e.g., subcutaneous vs. internal) suggest important functional specializations. These depot-specific differences in gene expression were recapitulated when adipocyte progenitor cells from each site were differentiated ex vivo, suggesting that progenitor cells from specific anatomic sites are deterministically programmed to differentiate into depot-specific adipocytes. Many developmental transcription factors show striking depot-specific patterns of expression, suggesting that adipocytes in each anatomic depot are programmed during early development in concert with anatomically related tissues and organs. Our results support the hypothesis that adipocytes from different depots are functionally distinct and that their depot-specific specialization reflects distinct developmental programs. |
| doi_str_mv | 10.1371/journal.pone.0311751 |
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Not much is known about the extent to which anatomically distinct adipose depots are functionally distinct, specialized organs, nor whether depot-specific characteristics result from intrinsic developmental programs, as opposed to reversible physiological responses to differences in tissue microenvironment. We used DNA microarrays to compare mRNA expression patterns of isolated human adipocytes and cultured adipose stem cells, before and after ex vivo adipocyte differentiation, from seven anatomically diverse adipose tissue depots. Adipocytes from different depots display distinct gene expression programs, which are most closely shared with anatomically related depots. mRNAs whose expression differs between anatomically diverse groups of depots (e.g., subcutaneous vs. internal) suggest important functional specializations. These depot-specific differences in gene expression were recapitulated when adipocyte progenitor cells from each site were differentiated ex vivo, suggesting that progenitor cells from specific anatomic sites are deterministically programmed to differentiate into depot-specific adipocytes. Many developmental transcription factors show striking depot-specific patterns of expression, suggesting that adipocytes in each anatomic depot are programmed during early development in concert with anatomically related tissues and organs. Our results support the hypothesis that adipocytes from different depots are functionally distinct and that their depot-specific specialization reflects distinct developmental programs.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0311751</identifier><identifier>PMID: 39401200</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Abdomen ; Adipocytes ; Adipocytes - cytology ; Adipocytes - metabolism ; Adipose tissue ; Adipose Tissue - cytology ; Adipose Tissue - metabolism ; Adipose tissues ; Adult ; Amino acids ; Analysis ; Biology and Life Sciences ; Body fat ; Cell differentiation ; Cell Differentiation - genetics ; Cells, Cultured ; Congenital diseases ; Diabetes ; DNA binding proteins ; DNA chips ; DNA microarrays ; Female ; Females ; Gene expression ; Gene Expression Profiling ; Genes ; Humans ; Male ; Medicine and Health Sciences ; Messenger RNA ; Metabolic syndrome ; Microenvironments ; Middle Aged ; Mutation ; Obesity ; Oligonucleotide Array Sequence Analysis ; Organs ; Physiological aspects ; Physiological responses ; Physiology ; Progenitor cells ; Research and Analysis Methods ; RNA, Messenger - genetics ; RNA, Messenger - metabolism ; Specialization ; Stem cells ; Stem Cells - cytology ; Stem Cells - metabolism ; Transcription factors ; Type 2 diabetes</subject><ispartof>PloS one, 2024-10, Vol.19 (10), p.e0311751</ispartof><rights>Copyright: © 2024 Clemons et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</rights><rights>COPYRIGHT 2024 Public Library of Science</rights><rights>2024 Clemons et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2024 Clemons et al 2024 Clemons et al</rights><rights>2024 Clemons et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c506t-85b426b6661df0121b8e4561062929586f3ed541e8da4e2ca424fc9c97af5b7a3</cites><orcidid>0000-0001-5828-0381</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11472956/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11472956/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39401200$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Clemons, Heather J</creatorcontrib><creatorcontrib>Hogan, Daniel J</creatorcontrib><creatorcontrib>Brown, Patrick O</creatorcontrib><title>Depot-specific mRNA expression programs in human adipocytes suggest physiological specialization via distinct developmental programs</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Adipose tissue is distributed in diverse locations throughout the human body. Not much is known about the extent to which anatomically distinct adipose depots are functionally distinct, specialized organs, nor whether depot-specific characteristics result from intrinsic developmental programs, as opposed to reversible physiological responses to differences in tissue microenvironment. We used DNA microarrays to compare mRNA expression patterns of isolated human adipocytes and cultured adipose stem cells, before and after ex vivo adipocyte differentiation, from seven anatomically diverse adipose tissue depots. Adipocytes from different depots display distinct gene expression programs, which are most closely shared with anatomically related depots. mRNAs whose expression differs between anatomically diverse groups of depots (e.g., subcutaneous vs. internal) suggest important functional specializations. These depot-specific differences in gene expression were recapitulated when adipocyte progenitor cells from each site were differentiated ex vivo, suggesting that progenitor cells from specific anatomic sites are deterministically programmed to differentiate into depot-specific adipocytes. Many developmental transcription factors show striking depot-specific patterns of expression, suggesting that adipocytes in each anatomic depot are programmed during early development in concert with anatomically related tissues and organs. Our results support the hypothesis that adipocytes from different depots are functionally distinct and that their depot-specific specialization reflects distinct developmental programs.</description><subject>Abdomen</subject><subject>Adipocytes</subject><subject>Adipocytes - cytology</subject><subject>Adipocytes - metabolism</subject><subject>Adipose tissue</subject><subject>Adipose Tissue - cytology</subject><subject>Adipose Tissue - metabolism</subject><subject>Adipose tissues</subject><subject>Adult</subject><subject>Amino acids</subject><subject>Analysis</subject><subject>Biology and Life Sciences</subject><subject>Body fat</subject><subject>Cell differentiation</subject><subject>Cell Differentiation - genetics</subject><subject>Cells, Cultured</subject><subject>Congenital diseases</subject><subject>Diabetes</subject><subject>DNA binding proteins</subject><subject>DNA chips</subject><subject>DNA microarrays</subject><subject>Female</subject><subject>Females</subject><subject>Gene expression</subject><subject>Gene Expression Profiling</subject><subject>Genes</subject><subject>Humans</subject><subject>Male</subject><subject>Medicine and Health Sciences</subject><subject>Messenger RNA</subject><subject>Metabolic syndrome</subject><subject>Microenvironments</subject><subject>Middle Aged</subject><subject>Mutation</subject><subject>Obesity</subject><subject>Oligonucleotide Array Sequence Analysis</subject><subject>Organs</subject><subject>Physiological aspects</subject><subject>Physiological responses</subject><subject>Physiology</subject><subject>Progenitor cells</subject><subject>Research and Analysis Methods</subject><subject>RNA, Messenger - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Clemons, Heather J</au><au>Hogan, Daniel J</au><au>Brown, Patrick O</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Depot-specific mRNA expression programs in human adipocytes suggest physiological specialization via distinct developmental programs</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2024-10-14</date><risdate>2024</risdate><volume>19</volume><issue>10</issue><spage>e0311751</spage><pages>e0311751-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Adipose tissue is distributed in diverse locations throughout the human body. Not much is known about the extent to which anatomically distinct adipose depots are functionally distinct, specialized organs, nor whether depot-specific characteristics result from intrinsic developmental programs, as opposed to reversible physiological responses to differences in tissue microenvironment. We used DNA microarrays to compare mRNA expression patterns of isolated human adipocytes and cultured adipose stem cells, before and after ex vivo adipocyte differentiation, from seven anatomically diverse adipose tissue depots. Adipocytes from different depots display distinct gene expression programs, which are most closely shared with anatomically related depots. mRNAs whose expression differs between anatomically diverse groups of depots (e.g., subcutaneous vs. internal) suggest important functional specializations. These depot-specific differences in gene expression were recapitulated when adipocyte progenitor cells from each site were differentiated ex vivo, suggesting that progenitor cells from specific anatomic sites are deterministically programmed to differentiate into depot-specific adipocytes. Many developmental transcription factors show striking depot-specific patterns of expression, suggesting that adipocytes in each anatomic depot are programmed during early development in concert with anatomically related tissues and organs. Our results support the hypothesis that adipocytes from different depots are functionally distinct and that their depot-specific specialization reflects distinct developmental programs.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>39401200</pmid><doi>10.1371/journal.pone.0311751</doi><tpages>e0311751</tpages><orcidid>https://orcid.org/0000-0001-5828-0381</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Abdomen Adipocytes Adipocytes - cytology Adipocytes - metabolism Adipose tissue Adipose Tissue - cytology Adipose Tissue - metabolism Adipose tissues Adult Amino acids Analysis Biology and Life Sciences Body fat Cell differentiation Cell Differentiation - genetics Cells, Cultured Congenital diseases Diabetes DNA binding proteins DNA chips DNA microarrays Female Females Gene expression Gene Expression Profiling Genes Humans Male Medicine and Health Sciences Messenger RNA Metabolic syndrome Microenvironments Middle Aged Mutation Obesity Oligonucleotide Array Sequence Analysis Organs Physiological aspects Physiological responses Physiology Progenitor cells Research and Analysis Methods RNA, Messenger - genetics RNA, Messenger - metabolism Specialization Stem cells Stem Cells - cytology Stem Cells - metabolism Transcription factors Type 2 diabetes |
| title | Depot-specific mRNA expression programs in human adipocytes suggest physiological specialization via distinct developmental programs |
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