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Hypoxia-Inducible Factor/MAZ-Dependent Induction of Caveolin-1 Regulates Colon Permeability through Suppression of Occludin, Leading to Hypoxia-Induced Inflammation

Liwei Xie, Xiang Xue, Matthew Taylor, Sadeesh K. Ramakrishnan, Kenjiro Nagaoka, Cathy Hao, Frank J. Gonzalez, Yatrik M. Shah
Liwei Xie
aDepartment of Molecular & Integrative Physiology, University of Michigan Medical School, Ann Arbor, Michigan, USA
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Xiang Xue
aDepartment of Molecular & Integrative Physiology, University of Michigan Medical School, Ann Arbor, Michigan, USA
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Matthew Taylor
aDepartment of Molecular & Integrative Physiology, University of Michigan Medical School, Ann Arbor, Michigan, USA
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Sadeesh K. Ramakrishnan
aDepartment of Molecular & Integrative Physiology, University of Michigan Medical School, Ann Arbor, Michigan, USA
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Kenjiro Nagaoka
aDepartment of Molecular & Integrative Physiology, University of Michigan Medical School, Ann Arbor, Michigan, USA
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Cathy Hao
aDepartment of Molecular & Integrative Physiology, University of Michigan Medical School, Ann Arbor, Michigan, USA
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Frank J. Gonzalez
cLaboratory of Metabolism, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, Maryland, USA
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Yatrik M. Shah
aDepartment of Molecular & Integrative Physiology, University of Michigan Medical School, Ann Arbor, Michigan, USA
bDepartment of Internal Medicine, Division of Gastroenterology, University of Michigan Medical School, Ann Arbor, Michigan, USA
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DOI: 10.1128/MCB.00324-14
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ABSTRACT

Caveolae are specialized microdomains on membranes that are critical for signal transduction, cholesterol transport, and endocytosis. Caveolin-1 (CAV1) is a multifunctional protein and a major component of caveolae. Cav1 is directly activated by hypoxia-inducible factor (HIF). HIFs are heterodimers of an oxygen-sensitive α subunit, HIF1α or HIF2α, and a constitutively expressed β subunit, aryl hydrocarbon receptor nuclear translocator (ARNT). Whole-genome expression analysis demonstrated that Cav1 is highly induced in mouse models of constitutively activated HIF signaling in the intestine. Interestingly, Cav1 was increased only in the colon and not in the small intestine. Currently, the mechanism and role of HIF induction of CAV1 in the colon are unclear. In mouse models, mice that overexpressed HIF1α or HIF2α specifically in intestinal epithelial cells demonstrated an increase in Cav1 gene expression in the colon but not in the duodenum, jejunum, or ileum. HIF2α activated the Cav1 promoter in a HIF response element-independent manner. myc-associated zinc finger (MAZ) protein was essential for HIF2α activation of the Cav1 promoter. Hypoxic induction of CAV1 in the colon was essential for intestinal barrier integrity by regulating occludin expression. This may provide an additional mechanism by which chronic hypoxia can activate intestinal inflammation.

FOOTNOTES

    • Received 10 March 2014.
    • Returned for modification 7 April 2014.
    • Accepted 26 May 2014.
    • Accepted manuscript posted online 2 June 2014.
  • Supplemental material for this article may be found at http://dx.doi.org/10.1128/MCB.00324-14.

  • Copyright © 2014, American Society for Microbiology. All Rights Reserved.
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Hypoxia-Inducible Factor/MAZ-Dependent Induction of Caveolin-1 Regulates Colon Permeability through Suppression of Occludin, Leading to Hypoxia-Induced Inflammation
Liwei Xie, Xiang Xue, Matthew Taylor, Sadeesh K. Ramakrishnan, Kenjiro Nagaoka, Cathy Hao, Frank J. Gonzalez, Yatrik M. Shah
Molecular and Cellular Biology Jul 2014, 34 (16) 3013-3023; DOI: 10.1128/MCB.00324-14

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Hypoxia-Inducible Factor/MAZ-Dependent Induction of Caveolin-1 Regulates Colon Permeability through Suppression of Occludin, Leading to Hypoxia-Induced Inflammation
Liwei Xie, Xiang Xue, Matthew Taylor, Sadeesh K. Ramakrishnan, Kenjiro Nagaoka, Cathy Hao, Frank J. Gonzalez, Yatrik M. Shah
Molecular and Cellular Biology Jul 2014, 34 (16) 3013-3023; DOI: 10.1128/MCB.00324-14
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