Lymphatic function is regulated by a coordinated expression of lymphangiogenic and anti-lymphangiogenic cytokines
Identifieur interne : 002B75 ( Pmc/Curation ); précédent : 002B74; suivant : 002B76Lymphatic function is regulated by a coordinated expression of lymphangiogenic and anti-lymphangiogenic cytokines
Auteurs : Jamie C. Zampell ; Tomer Avraham ; Nicole Yoder ; Nicholas Fort ; Alan Yan ; Evan S. Weitman ; Babak J. MehraraSource :
- American Journal of Physiology - Cell Physiology [ 0363-6143 ] ; 2011.
Abstract
Lymphangiogenic cytokines such as vascular endothelial growth factor-C (VEGF-C) are critically required for lymphatic regeneration; however, in some circumstances, lymphatic function is impaired despite normal or elevated levels of these cytokines. The recent identification of anti-lymphangiogenic molecules such as interferon-γ (IFN-γ), transforming growth factor-β1, and endostatin has led us to hypothesize that impaired lymphatic function may represent a dysregulated balance in the expression of pro/anti-lymphangiogenic stimuli. We observed that nude mice have significantly improved lymphatic function compared with wild-type mice in a tail model of lymphedema. We show that gradients of lymphatic fluid stasis regulate the expression of lymphangiogenic cytokines (VEGF-A, VEGF-C, and hepatocyte growth factor) and that paradoxically the expression of these molecules is increased in wild-type mice. More importantly, we show that as a consequence of T-cell-mediated inflammation, these same gradients also regulate expression patterns of anti-lymphangiogenic molecules corresponding temporally and spatially with impaired lymphatic function in wild-type mice. We show that neutralization of IFN-γ significantly increases inflammatory lymph node lymphangiogenesis independently of changes in VEGF-A or VEGF-C expression, suggesting that alterations in the balance of pro- and anti-lymphangiogenic cytokine expression can regulate lymphatic vessel formation. In conclusion, we show that gradients of lymphatic fluid stasis regulate not only the expression of pro-lymphangiogenic cytokines but also potent suppressors of lymphangiogenesis as a consequence of T-cell inflammation and that modulation of the balance between these stimuli can regulate lymphatic function.
Url:
DOI: 10.1152/ajpcell.00306.2011
PubMed: 21940662
PubMed Central: 3328842
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<front><div type="abstract" xml:lang="en"><p>Lymphangiogenic cytokines such as vascular endothelial growth factor-C (VEGF-C) are critically required for lymphatic regeneration; however, in some circumstances, lymphatic function is impaired despite normal or elevated levels of these cytokines. The recent identification of anti-lymphangiogenic molecules such as interferon-γ (IFN-γ), transforming growth factor-β1, and endostatin has led us to hypothesize that impaired lymphatic function may represent a dysregulated balance in the expression of pro/anti-lymphangiogenic stimuli. We observed that nude mice have significantly improved lymphatic function compared with wild-type mice in a tail model of lymphedema. We show that gradients of lymphatic fluid stasis regulate the expression of lymphangiogenic cytokines (VEGF-A, VEGF-C, and hepatocyte growth factor) and that paradoxically the expression of these molecules is increased in wild-type mice. More importantly, we show that as a consequence of T-cell-mediated inflammation, these same gradients also regulate expression patterns of anti-lymphangiogenic molecules corresponding temporally and spatially with impaired lymphatic function in wild-type mice. We show that neutralization of IFN-γ significantly increases inflammatory lymph node lymphangiogenesis independently of changes in VEGF-A or VEGF-C expression, suggesting that alterations in the balance of pro- and anti-lymphangiogenic cytokine expression can regulate lymphatic vessel formation. In conclusion, we show that gradients of lymphatic fluid stasis regulate not only the expression of pro-lymphangiogenic cytokines but also potent suppressors of lymphangiogenesis as a consequence of T-cell inflammation and that modulation of the balance between these stimuli can regulate lymphatic function.</p>
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<front><journal-meta><journal-id journal-id-type="nlm-ta">Am J Physiol Cell Physiol</journal-id>
<journal-id journal-id-type="iso-abbrev">Am. J. Physiol., Cell Physiol</journal-id>
<journal-id journal-id-type="hwp">ajpcell</journal-id>
<journal-id journal-id-type="pmc">ajpcell</journal-id>
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<publisher><publisher-name>American Physiological Society</publisher-name>
<publisher-loc>Bethesda, MD</publisher-loc>
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<article-id pub-id-type="doi">10.1152/ajpcell.00306.2011</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Vascular Biology</subject>
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<title-group><article-title>Lymphatic function is regulated by a coordinated expression of lymphangiogenic and anti-lymphangiogenic cytokines</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Zampell</surname>
<given-names>Jamie C.</given-names>
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<contrib contrib-type="author"><name><surname>Avraham</surname>
<given-names>Tomer</given-names>
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<contrib contrib-type="author"><name><surname>Yoder</surname>
<given-names>Nicole</given-names>
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<contrib contrib-type="author"><name><surname>Fort</surname>
<given-names>Nicholas</given-names>
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<contrib contrib-type="author"><name><surname>Yan</surname>
<given-names>Alan</given-names>
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<contrib contrib-type="author"><name><surname>Weitman</surname>
<given-names>Evan S.</given-names>
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<contrib contrib-type="author" corresp="yes"><name><surname>Mehrara</surname>
<given-names>Babak J.</given-names>
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<aff>The Division of Plastic and Reconstructive Surgery, Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York, New York</aff>
</contrib-group>
<author-notes><corresp>Address for reprint requests and other correspondence: B. J. Mehrara,
<addr-line>1275 York Ave., Rm. MRI 1005, New York, NY 10065</addr-line>
(e-mail: <email>mehrarab@mskcc.org</email>
).</corresp>
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<pub-date pub-type="ppub"><day>15</day>
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<pub-date pub-type="epub"><day>21</day>
<month>9</month>
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<pmc-comment> PMC Release delay is 12 months and 0 days and was based on the
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<volume>302</volume>
<issue>2</issue>
<fpage>C392</fpage>
<lpage>C404</lpage>
<history><date date-type="received"><day>17</day>
<month>8</month>
<year>2011</year>
</date>
<date date-type="accepted"><day>19</day>
<month>9</month>
<year>2011</year>
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<permissions><copyright-statement>Copyright © 2012 the American Physiological Society</copyright-statement>
<copyright-year>2012</copyright-year>
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<abstract><p>Lymphangiogenic cytokines such as vascular endothelial growth factor-C (VEGF-C) are critically required for lymphatic regeneration; however, in some circumstances, lymphatic function is impaired despite normal or elevated levels of these cytokines. The recent identification of anti-lymphangiogenic molecules such as interferon-γ (IFN-γ), transforming growth factor-β1, and endostatin has led us to hypothesize that impaired lymphatic function may represent a dysregulated balance in the expression of pro/anti-lymphangiogenic stimuli. We observed that nude mice have significantly improved lymphatic function compared with wild-type mice in a tail model of lymphedema. We show that gradients of lymphatic fluid stasis regulate the expression of lymphangiogenic cytokines (VEGF-A, VEGF-C, and hepatocyte growth factor) and that paradoxically the expression of these molecules is increased in wild-type mice. More importantly, we show that as a consequence of T-cell-mediated inflammation, these same gradients also regulate expression patterns of anti-lymphangiogenic molecules corresponding temporally and spatially with impaired lymphatic function in wild-type mice. We show that neutralization of IFN-γ significantly increases inflammatory lymph node lymphangiogenesis independently of changes in VEGF-A or VEGF-C expression, suggesting that alterations in the balance of pro- and anti-lymphangiogenic cytokine expression can regulate lymphatic vessel formation. In conclusion, we show that gradients of lymphatic fluid stasis regulate not only the expression of pro-lymphangiogenic cytokines but also potent suppressors of lymphangiogenesis as a consequence of T-cell inflammation and that modulation of the balance between these stimuli can regulate lymphatic function.</p>
</abstract>
<kwd-group><kwd>lymphangiogenesis</kwd>
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<kwd>lymphedema</kwd>
<kwd>transforming growth factor-β1</kwd>
<kwd>interferon-γ</kwd>
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