Obesity increases inflammation and impairs lymphatic function in a mouse model of lymphedema.
Identifieur interne : 001508 ( PubMed/Corpus ); précédent : 001507; suivant : 001509Obesity increases inflammation and impairs lymphatic function in a mouse model of lymphedema.
Auteurs : Ira L. Savetsky ; Jeremy S. Torrisi ; Daniel A. Cuzzone ; Swapna Ghanta ; Nicholas J. Albano ; Jason C. Gardenier ; Walter J. Joseph ; Babak J. MehraraSource :
- American journal of physiology. Heart and circulatory physiology [ 1522-1539 ] ; 2014.
English descriptors
- KwdEn :
- Adiposity, Animals, Croton Oil, Diet, High-Fat, Disease Models, Animal, Fibrosis, Inflammation (chemically induced), Inflammation (etiology), Inflammation (immunology), Inflammation (physiopathology), Lymphatic System (immunology), Lymphatic System (pathology), Lymphatic System (physiopathology), Lymphedema (etiology), Lymphedema (immunology), Lymphedema (pathology), Lymphedema (physiopathology), Macrophages (immunology), Male, Mice, Mice, Inbred C57BL, Neutrophil Infiltration, Neutrophils (immunology), Obesity (complications), Obesity (immunology), Obesity (physiopathology), Phenotype, Severity of Illness Index, Subcutaneous Fat (physiopathology), Time Factors.
- MESH :
- chemical : Croton Oil.
- chemically induced : Inflammation.
- complications : Obesity.
- etiology : Inflammation, Lymphedema.
- immunology : Inflammation, Lymphatic System, Lymphedema, Macrophages, Neutrophils, Obesity.
- pathology : Lymphatic System, Lymphedema.
- physiopathology : Inflammation, Lymphatic System, Lymphedema, Obesity, Subcutaneous Fat.
- Adiposity, Animals, Diet, High-Fat, Disease Models, Animal, Fibrosis, Male, Mice, Mice, Inbred C57BL, Neutrophil Infiltration, Phenotype, Severity of Illness Index, Time Factors.
Abstract
Although obesity is a major clinical risk factor for lymphedema, the mechanisms that regulate this effect remain unknown. Recent reports have demonstrated that obesity is associated with acquired lymphatic dysfunction. The purpose of this study was to determine how obesity-induced lymphatic dysfunction modulates the pathological effects of lymphatic injury in a mouse model. We used a diet-induced model of obesity in adult male C57BL/6J mice in which experimental animals were fed a high-fat diet and control animals were fed a normal chow diet for 8-10 wk. We then surgically ablated the superficial and deep lymphatics of the midportion of the tail. Six weeks postoperatively, we analyzed changes in lymphatic function, adipose deposition, inflammation, and fibrosis. We also compared responses to acute inflammatory stimuli in obese and lean mice. Compared with lean control mice, obese mice had baseline decreased lymphatic function. Lymphedema in obese mice further impaired lymphatic function and resulted in increased subcutaneous adipose deposition, increased CD45(+) and CD4(+) cell inflammation (P < 0.01), and increased fibrosis, but caused no change in the number of lymphatic vessels. Interestingly, obese mice had a significantly increased acute inflammatory reaction to croton oil application. In conclusion, obese mice have impaired lymphatic function at baseline that is amplified by lymphatic injury. This effect is associated with increased chronic inflammation, fibrosis, and adipose deposition. These findings suggest that obese patients are at higher risk for lymphedema due to impaired baseline lymphatic clearance and an increased propensity for inflammation in response to injury.
DOI: 10.1152/ajpheart.00244.2014
PubMed: 24858842
Links to Exploration step
pubmed:24858842Le document en format XML
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Cuzzone</name><affiliation><nlm:affiliation>Division of Plastic and Reconstructive Surgery, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, New York.</nlm:affiliation></affiliation></author><author><name sortKey="Ghanta, Swapna" sort="Ghanta, Swapna" uniqKey="Ghanta S" first="Swapna" last="Ghanta">Swapna Ghanta</name><affiliation><nlm:affiliation>Division of Plastic and Reconstructive Surgery, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, New York.</nlm:affiliation></affiliation></author><author><name sortKey="Albano, Nicholas J" sort="Albano, Nicholas J" uniqKey="Albano N" first="Nicholas J" last="Albano">Nicholas J. 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Savetsky</name><affiliation><nlm:affiliation>Division of Plastic and Reconstructive Surgery, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, New York.</nlm:affiliation></affiliation></author><author><name sortKey="Torrisi, Jeremy S" sort="Torrisi, Jeremy S" uniqKey="Torrisi J" first="Jeremy S" last="Torrisi">Jeremy S. Torrisi</name><affiliation><nlm:affiliation>Division of Plastic and Reconstructive Surgery, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, New York.</nlm:affiliation></affiliation></author><author><name sortKey="Cuzzone, Daniel A" sort="Cuzzone, Daniel A" uniqKey="Cuzzone D" first="Daniel A" last="Cuzzone">Daniel A. Cuzzone</name><affiliation><nlm:affiliation>Division of Plastic and Reconstructive Surgery, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, New York.</nlm:affiliation></affiliation></author><author><name sortKey="Ghanta, Swapna" sort="Ghanta, Swapna" uniqKey="Ghanta S" first="Swapna" last="Ghanta">Swapna Ghanta</name><affiliation><nlm:affiliation>Division of Plastic and Reconstructive Surgery, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, New York.</nlm:affiliation></affiliation></author><author><name sortKey="Albano, Nicholas J" sort="Albano, Nicholas J" uniqKey="Albano N" first="Nicholas J" last="Albano">Nicholas J. Albano</name><affiliation><nlm:affiliation>Division of Plastic and Reconstructive Surgery, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, New York.</nlm:affiliation></affiliation></author><author><name sortKey="Gardenier, Jason C" sort="Gardenier, Jason C" uniqKey="Gardenier J" first="Jason C" last="Gardenier">Jason C. Gardenier</name><affiliation><nlm:affiliation>Division of Plastic and Reconstructive Surgery, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, New York.</nlm:affiliation></affiliation></author><author><name sortKey="Joseph, Walter J" sort="Joseph, Walter J" uniqKey="Joseph W" first="Walter J" last="Joseph">Walter J. Joseph</name><affiliation><nlm:affiliation>Division of Plastic and Reconstructive Surgery, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, New York.</nlm:affiliation></affiliation></author><author><name sortKey="Mehrara, Babak J" sort="Mehrara, Babak J" uniqKey="Mehrara B" first="Babak J" last="Mehrara">Babak J. Mehrara</name><affiliation><nlm:affiliation>Division of Plastic and Reconstructive Surgery, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, New York mehrarab@mskcc.org.</nlm:affiliation></affiliation></author></analytic><series><title level="j">American journal of physiology. Heart and circulatory physiology</title><idno type="eISSN">1522-1539</idno><imprint><date when="2014" type="published">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Adiposity</term><term>Animals</term><term>Croton Oil</term><term>Diet, High-Fat</term><term>Disease Models, Animal</term><term>Fibrosis</term><term>Inflammation (chemically induced)</term><term>Inflammation (etiology)</term><term>Inflammation (immunology)</term><term>Inflammation (physiopathology)</term><term>Lymphatic System (immunology)</term><term>Lymphatic System (pathology)</term><term>Lymphatic System (physiopathology)</term><term>Lymphedema (etiology)</term><term>Lymphedema (immunology)</term><term>Lymphedema (pathology)</term><term>Lymphedema (physiopathology)</term><term>Macrophages (immunology)</term><term>Male</term><term>Mice</term><term>Mice, Inbred C57BL</term><term>Neutrophil Infiltration</term><term>Neutrophils (immunology)</term><term>Obesity (complications)</term><term>Obesity (immunology)</term><term>Obesity (physiopathology)</term><term>Phenotype</term><term>Severity of Illness Index</term><term>Subcutaneous Fat (physiopathology)</term><term>Time Factors</term></keywords><keywords scheme="MESH" type="chemical" xml:lang="en"><term>Croton Oil</term></keywords><keywords scheme="MESH" qualifier="chemically induced" xml:lang="en"><term>Inflammation</term></keywords><keywords scheme="MESH" qualifier="complications" xml:lang="en"><term>Obesity</term></keywords><keywords scheme="MESH" qualifier="etiology" xml:lang="en"><term>Inflammation</term><term>Lymphedema</term></keywords><keywords scheme="MESH" qualifier="immunology" xml:lang="en"><term>Inflammation</term><term>Lymphatic System</term><term>Lymphedema</term><term>Macrophages</term><term>Neutrophils</term><term>Obesity</term></keywords><keywords scheme="MESH" qualifier="pathology" xml:lang="en"><term>Lymphatic System</term><term>Lymphedema</term></keywords><keywords scheme="MESH" qualifier="physiopathology" xml:lang="en"><term>Inflammation</term><term>Lymphatic System</term><term>Lymphedema</term><term>Obesity</term><term>Subcutaneous Fat</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Adiposity</term><term>Animals</term><term>Diet, High-Fat</term><term>Disease Models, Animal</term><term>Fibrosis</term><term>Male</term><term>Mice</term><term>Mice, Inbred C57BL</term><term>Neutrophil Infiltration</term><term>Phenotype</term><term>Severity of Illness Index</term><term>Time Factors</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Although obesity is a major clinical risk factor for lymphedema, the mechanisms that regulate this effect remain unknown. Recent reports have demonstrated that obesity is associated with acquired lymphatic dysfunction. The purpose of this study was to determine how obesity-induced lymphatic dysfunction modulates the pathological effects of lymphatic injury in a mouse model. We used a diet-induced model of obesity in adult male C57BL/6J mice in which experimental animals were fed a high-fat diet and control animals were fed a normal chow diet for 8-10 wk. We then surgically ablated the superficial and deep lymphatics of the midportion of the tail. Six weeks postoperatively, we analyzed changes in lymphatic function, adipose deposition, inflammation, and fibrosis. We also compared responses to acute inflammatory stimuli in obese and lean mice. Compared with lean control mice, obese mice had baseline decreased lymphatic function. Lymphedema in obese mice further impaired lymphatic function and resulted in increased subcutaneous adipose deposition, increased CD45(+) and CD4(+) cell inflammation (P < 0.01), and increased fibrosis, but caused no change in the number of lymphatic vessels. Interestingly, obese mice had a significantly increased acute inflammatory reaction to croton oil application. In conclusion, obese mice have impaired lymphatic function at baseline that is amplified by lymphatic injury. This effect is associated with increased chronic inflammation, fibrosis, and adipose deposition. These findings suggest that obese patients are at higher risk for lymphedema due to impaired baseline lymphatic clearance and an increased propensity for inflammation in response to injury.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">24858842</PMID><DateCreated><Year>2014</Year><Month>07</Month><Day>16</Day></DateCreated><DateCompleted><Year>2014</Year><Month>09</Month><Day>05</Day></DateCompleted><DateRevised><Year>2016</Year><Month>10</Month><Day>19</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1522-1539</ISSN><JournalIssue CitedMedium="Internet"><Volume>307</Volume><Issue>2</Issue><PubDate><Year>2014</Year><Month>Jul</Month><Day>15</Day></PubDate></JournalIssue><Title>American journal of physiology. Heart and circulatory physiology</Title><ISOAbbreviation>Am. J. Physiol. Heart Circ. Physiol.</ISOAbbreviation></Journal><ArticleTitle>Obesity increases inflammation and impairs lymphatic function in a mouse model of lymphedema.</ArticleTitle><Pagination><MedlinePgn>H165-72</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1152/ajpheart.00244.2014</ELocationID><Abstract><AbstractText>Although obesity is a major clinical risk factor for lymphedema, the mechanisms that regulate this effect remain unknown. Recent reports have demonstrated that obesity is associated with acquired lymphatic dysfunction. The purpose of this study was to determine how obesity-induced lymphatic dysfunction modulates the pathological effects of lymphatic injury in a mouse model. We used a diet-induced model of obesity in adult male C57BL/6J mice in which experimental animals were fed a high-fat diet and control animals were fed a normal chow diet for 8-10 wk. We then surgically ablated the superficial and deep lymphatics of the midportion of the tail. Six weeks postoperatively, we analyzed changes in lymphatic function, adipose deposition, inflammation, and fibrosis. We also compared responses to acute inflammatory stimuli in obese and lean mice. Compared with lean control mice, obese mice had baseline decreased lymphatic function. Lymphedema in obese mice further impaired lymphatic function and resulted in increased subcutaneous adipose deposition, increased CD45(+) and CD4(+) cell inflammation (P < 0.01), and increased fibrosis, but caused no change in the number of lymphatic vessels. Interestingly, obese mice had a significantly increased acute inflammatory reaction to croton oil application. In conclusion, obese mice have impaired lymphatic function at baseline that is amplified by lymphatic injury. This effect is associated with increased chronic inflammation, fibrosis, and adipose deposition. These findings suggest that obese patients are at higher risk for lymphedema due to impaired baseline lymphatic clearance and an increased propensity for inflammation in response to injury.</AbstractText><CopyrightInformation>Copyright © 2014 the American Physiological Society.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Savetsky</LastName><ForeName>Ira L</ForeName><Initials>IL</Initials><AffiliationInfo><Affiliation>Division of Plastic and Reconstructive Surgery, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, New York.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Torrisi</LastName><ForeName>Jeremy S</ForeName><Initials>JS</Initials><AffiliationInfo><Affiliation>Division of Plastic and Reconstructive Surgery, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, New York.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Cuzzone</LastName><ForeName>Daniel A</ForeName><Initials>DA</Initials><AffiliationInfo><Affiliation>Division of Plastic and Reconstructive Surgery, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, New York.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ghanta</LastName><ForeName>Swapna</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Division of Plastic and Reconstructive Surgery, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, New York.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Albano</LastName><ForeName>Nicholas J</ForeName><Initials>NJ</Initials><AffiliationInfo><Affiliation>Division of Plastic and Reconstructive Surgery, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, New York.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Gardenier</LastName><ForeName>Jason C</ForeName><Initials>JC</Initials><AffiliationInfo><Affiliation>Division of Plastic and Reconstructive Surgery, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, New York.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Joseph</LastName><ForeName>Walter J</ForeName><Initials>WJ</Initials><AffiliationInfo><Affiliation>Division of Plastic and Reconstructive Surgery, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, New York.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Mehrara</LastName><ForeName>Babak J</ForeName><Initials>BJ</Initials><AffiliationInfo><Affiliation>Division of Plastic and Reconstructive Surgery, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, New York mehrarab@mskcc.org.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>T32 CA009501</GrantID><Acronym>CA</Acronym><Agency>NCI NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>R01-HL111130-01</GrantID><Acronym>HL</Acronym><Agency>NHLBI NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>P30 CA008748</GrantID><Acronym>CA</Acronym><Agency>NCI NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>S10 RR028889</GrantID><Acronym>RR</Acronym><Agency>NCRR NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>5-T32-CA009501</GrantID><Acronym>CA</Acronym><Agency>NCI NIH HHS</Agency><Country>United States</Country></Grant><Grant><GrantID>R01 HL111130</GrantID><Acronym>HL</Acronym><Agency>NHLBI NIH HHS</Agency><Country>United States</Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D052061">Research Support, N.I.H., Extramural</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2014</Year><Month>05</Month><Day>23</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Am J Physiol Heart Circ Physiol</MedlineTA><NlmUniqueID>100901228</NlmUniqueID><ISSNLinking>0363-6135</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>8001-28-3</RegistryNumber><NameOfSubstance UI="D003436">Croton Oil</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><CommentsCorrectionsList><CommentsCorrections RefType="Cites"><RefSource>Eur J Cancer. 2001 May;37(8):991-9</RefSource><PMID Version="1">11334724</PMID></CommentsCorrections><CommentsCorrections RefType="Cites"><RefSource>Cancer. 2001 Sep 15;92(6):1368-77</RefSource><PMID Version="1">11745212</PMID></CommentsCorrections><CommentsCorrections RefType="Cites"><RefSource>Ann Surg Oncol. 2004 Jun;11(6):573-80</RefSource><PMID Version="1">15172932</PMID></CommentsCorrections><CommentsCorrections 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Oil</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D059305" MajorTopicYN="N">Diet, High-Fat</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D004195" MajorTopicYN="N">Disease Models, Animal</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D005355" MajorTopicYN="N">Fibrosis</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D007249" MajorTopicYN="N">Inflammation</DescriptorName><QualifierName UI="Q000139" MajorTopicYN="N">chemically induced</QualifierName><QualifierName UI="Q000209" MajorTopicYN="Y">etiology</QualifierName><QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName><QualifierName UI="Q000503" MajorTopicYN="N">physiopathology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D008208" MajorTopicYN="N">Lymphatic System</DescriptorName><QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName><QualifierName UI="Q000473" MajorTopicYN="N">pathology</QualifierName><QualifierName UI="Q000503" MajorTopicYN="Y">physiopathology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D008209" MajorTopicYN="N">Lymphedema</DescriptorName><QualifierName UI="Q000209" MajorTopicYN="Y">etiology</QualifierName><QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName><QualifierName UI="Q000473" MajorTopicYN="N">pathology</QualifierName><QualifierName UI="Q000503" MajorTopicYN="N">physiopathology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D008264" MajorTopicYN="N">Macrophages</DescriptorName><QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D008297" MajorTopicYN="N">Male</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D051379" MajorTopicYN="N">Mice</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D008810" MajorTopicYN="N">Mice, Inbred C57BL</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D020556" MajorTopicYN="N">Neutrophil Infiltration</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D009504" MajorTopicYN="N">Neutrophils</DescriptorName><QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D009765" MajorTopicYN="N">Obesity</DescriptorName><QualifierName UI="Q000150" MajorTopicYN="Y">complications</QualifierName><QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName><QualifierName UI="Q000503" MajorTopicYN="N">physiopathology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D010641" MajorTopicYN="N">Phenotype</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D012720" MajorTopicYN="N">Severity of Illness Index</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D050151" MajorTopicYN="N">Subcutaneous Fat</DescriptorName><QualifierName UI="Q000503" MajorTopicYN="N">physiopathology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D013997" MajorTopicYN="N">Time Factors</DescriptorName></MeshHeading></MeshHeadingList><OtherID Source="NLM">PMC4101643</OtherID><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">fibrosis</Keyword><Keyword MajorTopicYN="N">inflammation</Keyword><Keyword MajorTopicYN="N">lymphedema</Keyword><Keyword MajorTopicYN="N">obesity</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="entrez"><Year>2014</Year><Month>5</Month><Day>27</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2014</Year><Month>5</Month><Day>27</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2014</Year><Month>9</Month><Day>6</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">24858842</ArticleId><ArticleId IdType="pii">ajpheart.00244.2014</ArticleId><ArticleId IdType="doi">10.1152/ajpheart.00244.2014</ArticleId><ArticleId 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