Hypoxia-Inducible Factor 1–Dependent Induction of Intestinal Trefoil Factor Protects Barrier Function during Hypoxia
Open accessAbstract
Mucosal organs such as the intestine are supported by a rich and complex underlying vasculature. For this reason, the intestine, and particularly barrier-protective epithelial cells, are susceptible to damage related to diminished blood flow and concomitant tissue hypoxia. We sought to identify compensatory mechanisms that protect epithelial barrier during episodes of intestinal hypoxia. Initial studies examining T84 colonic epithelial cells revealed that barrier function is uniquely resistant to changes elicited by hypoxia. A search for intestinal-specific, barrier-protective factors revealed that the human intestinal trefoil factor (ITF) gene promoter bears a previously unappreciated binding site for hypoxia-inducible factor (HIF)-1. Hypoxia resulted in parallel induction of ITF mRNA and protein. Electrophoretic mobility shift assay analysis using ITF-specific, HIF-1 consensus motifs resulted in a hypoxia-inducible DNA binding activity, and loading cells with antisense oligonucleotides directed against the α chain of HIF-1 resulted in a loss of ITF hypoxia inducibility. Moreover, addition of anti-ITF antibody resulted in a loss of barrier function in epithelial cells exposed to hypoxia, and the addition of recombinant human ITF to vascular endothelial cells partially protected endothelial cells from hypoxia-elicited barrier disruption. Extensions of these studies in vivo revealed prominent hypoxia-elicited increases in intestinal permeability in ITF null mice. HIF-1–dependent induction of ITF may provide an adaptive link for maintenance of barrier function during hypoxia.
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Intestinal epithelial cells seem uniquely resistant to hypoxia, and extremely low oxygenation within the normal intestinal epithelial barrier (physiologic hypoxia) may be a regulatory adaptation mechanism to the steep oxygen gradient.
“In fact, studies comparing functional responses between epithelial cells from different tissues have revealed that intestinal epithelial cells seem to be uniquely resistant to hypoxia and that an extremely low level of oxygenation within the normal intestinal epithelial barrier (so-called “physiologic hypoxia”) may be a regulatory adaptation mechanism to the steep oxygen gradient4.”
From Hypoxia: an alarm signal during intestinal inflammation (2010) · cites this paper as [4]
Amelioration of disease occurs, at least in part, through transcriptional up-regulation of non-classical epithelial barrier genes.
“Amelioration of disease occurs, at least in part, through transcriptional up-regulation of non-classical epithelial barrier genes.”
From Hypoxia: an alarm signal during intestinal inflammation (2010) · cites this paper as [4]
HIF regulates the expression of a family of barrier protective factors including intestinal trefoil factor, the mucins and actin cytoskeletal crosslinkers.
“For example, HIF regulates the expression of a family of barrier protective factors including intestinal trefoil factor4, the mucins31 and actin cytoskeletal crosslinkers45.”
From Hypoxia: an alarm signal during intestinal inflammation (2010) · cites this paper as [4]
HIF-1 triggers the transcription of many genes that enable intestinal epithelial cells to act as an effective barrier.
“Several studies have shown that HIF-1 triggers the transcription of many genes that enable intestinal epithelial cells to act as an effective barrier4,20–22.”
From Hypoxia: an alarm signal during intestinal inflammation (2010) · cites this paper as [4]
HIF-dependent pathways are more to do with overall tissue integrity, ranging from increased mucin production, including molecules that modify mucins such as intestinal trefoil factor, to xenobiotic clearance by P-glycoprotein, to nucleotide metabolism (by ecto-5′-nucleotidase and CD73) and nucleotide signaling through the adenosine A2B receptor.
“Rather, the HIF-dependent pathways are more to do with overall tissue integrity, ranging from increased mucin production,31 including molecules that modify mucins, such as, intestinal trefoil factor4, to xenobiotic clearance by P-glycoprotein,20 to nucleotide metabolism (by ecto-5′-nucleotidase and CD73)21,22 and nucleotide signaling through the adenosine A2B receptor22.”
From Hypoxia: an alarm signal during intestinal inflammation (2010) · cites this paper as [4]
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Self-citation
- Authors
- Furuta, G. T., Turner, J. R., Taylor, C. T., Hershberg, R. M., Comerford, K., Narravula, S., Podolsky, D. K., & Colgan, S. P.
- Affiliations
- Brigham and Women's Hospital (US)
- Wayne State University (US)
- Harvard University (US)
- Venue
- The Journal of Experimental Medicine
- Publisher
- Rockefeller University Press
- Published
- 2001-04-30
- Volume
- 193
- Issue
- 9
- Pages
- 1027-1034
- ISSN
- 0022-1007 (ISSN-L)
- 1540-9538
- PMC
- PMC2193432
- OpenAlex
- W2108780695
- Cited by
- 449
- References
- 46
- Citations by year
- 2026: 12 · 2025: 16 · 2024: 25 · 2023: 36 · 2022: 26 · 2021: 17 · 2020: 22 · 2019: 22 · 2018: 15 · 2017: 19 · 2016: 29 · 2015: 24 · 2014: 23 · 2013: 20 · 2012: 17
- FWCI
- 7.41
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The Journal of Experimental Medicine (publishedVersion)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5k08dk002564-04, 5k08dk002503-02, 1k01dk002682-01, DK 43351, DK-50189)
- National Heart, Lung, and Blood Institute (R01HL060569, HL-60569)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK02564, DK-02503, R01DK050189, DK02682, R37DK050189, R29DK050189, DK-50189, P30DK043351)
- Topics
- Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Digestive system and related health
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Keywords
- HIF-1, TFF3, intestinal barrier function, intestinal hypoxia, epithelial permeability, colonic epithelial cells, endothelial cells, intestinal permeability, compensatory mechanisms
- MeSH terms
- Trefoil Factor-2, Trefoil Factor-3, Animals, Cell Line, Colon, DNA-Binding Proteins, Dogs, Growth Substances, Humans, Intestinal Mucosa, Mucins, Muscle Proteins, Neuropeptides, Nuclear Proteins, Peptides, Transcription Factors, Cell Hypoxia, Gene Expression, Caco-2 Cells, Mice, Hypoxia-Inducible Factor 1, Hypoxia-Inducible Factor 1, alpha Subunit
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