Hypoxia-inducible factor 1-dependent induction of intestinal trefoil factor protects barrier function during hypoxia

Journal of Experimental Medicine

Volumn 193, Issue 9, 2001, Pages 1027-1034

  Furuta, Glenn T ^a   Turner, Jerrold R ^c   Taylor, Cormac T ^a   Hershberg, Robert M ^b   Comerford, Katrina ^a   Narravula, Sailaja ^a   Podolsky, Daniel K ^a   Colgan, Sean P ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Endothelium; Epithelium; Gastrointestinal disease; Intestinal permeability; Transcription factor

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1; INTESTINAL TREFOIL FACTOR; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; CONTROLLED STUDY; ELECTROPHORETIC MOBILITY; HUMAN; HUMAN CELL; HYPOXIA; INTESTINE EPITHELIUM; INTESTINE MUCOSA PERMEABILITY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN INDUCTION;

ANIMALS; CACO-2 CELLS; CELL HYPOXIA; CELL LINE; COLON; DNA-BINDING PROTEINS; DOGS; GENE EXPRESSION; GROWTH SUBSTANCES; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INTESTINAL MUCOSA; MICE; MUCINS; MUSCLE PROTEINS; NEUROPEPTIDES; NUCLEAR PROTEINS; PEPTIDES; TRANSCRIPTION FACTORS;

EID: 0035821249     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.193.9.1027     Document Type: Article

References (44)

1. Madara, J.L. 1998. Regulation of the movement of solutes across tight junctions. Annu. Rev. Physiol. 60:143-159.
2. Taylor, C.T., and S.P. Colgan. 1999. Therapeutic targets for hypoxia-elicited pathways. Pharmacol. Res. 16:1498-1505.
3. Semenza, G.L. 1999. Perspectives on oxygen sensing. Cell. 98:281-284.
4. 2 homeostasis. Curr. Opin. Genet. Dev. 8:588-594.
5. Wang, G.L., and G.L. Semenza. 1995. Purification and characterization of hypoxia-inducible factor 1. J. Biol. Chem. 270: 1230-1237.
6. Wang, G.L., B.H. Jiang, E.A. Rue, and G.L. Semenza. 1995. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular oxygen tension. Proc. Natl. Acad. Sci. USA. 92:5510-5514.
7. 2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc. Natl. Acad. Sci. USA. 95:7987-7992.
8. +-dependent glucose cotransporter (SGLT1): maintenance of surface expression and global transport function with selective perturbation of transport kinetics and polarized expression. J. Bid. Chem. 271:7738-7744.
9. Madara, J.L., J. Stafford, K. Dharmsathaphorn, and S. Carlson. 1987. Structural analysis of a human intestinal epithelial cell line. Gastroenterology. 92:1133-1145.
10. Eagle, H. 1955. Propagation in a fluid medium of a human epidermoid carcinoma, strain KB. Proc. Soc. Exp. Biol. Med. 94:362-364.
11. 2B receptor activation. J. Exp. Med. 188:1433-1443.
12. Sambuy, Y., and E. Rodriguez-Boulan. 1988. Isolation and characterization of the apical surface of polarized Madin-Darby canine kidney epithelial cells. Proc. Natl. Acad. Sci. USA. 85:1529-1533.
13. Colgan, S.P., A.L. Dzus, and C.A. Parkos. 1996. Epithelial exposure to hypoxia modulates neutrophil transepithelial migration. J. Exp. Med. 184:1003-1015.
14. Taylor, C.T., N. Fueki, A. Agah, R.M. Hershberg, and S.P. Colgan. 1999. Critical role of cAMP response element binding protein expression in hypoxia-elicited induction of epithelial TNFα. J. Biol. Chem. 274:19447-19450.
15. Zünd, G., D.P. Nelson, E.J. Neufeld, A.L. Dzus, J. Bischoff, J.E. Mayer, and S.P. Colgan. 1996. Hypoxia enhances stimulus-dependent induction of E-selectin on aortic endothelial cells. Proc. Natl. Acad. Sci. USA. 93:7075-7080.
16. Lockhart, D.J., H. Dong, M.C. Byrne, M.T. Follettie, M.V. Gallo, M.S. Chee, M. Mittmann, C. Wang, M. Kobayashi, H. Horton, and E.L. Brown. 1996. Expression monitoring by hybridization to high-density oligonucleotide arrays. Nat. Biotechnol. 14:1675-1680.
17. Seib, T., S. Dooley, and C. Welter. 1995. Characterization of the genomic structure and the promoter region of the human intestinal trefoil factor. Biochem. Biophys. Res. Commun. 214: 195-199.
18. Zünd, G., S. Uezono, G.L. Stahl, A.L. Dzus, F.X. McGowan, P.R. Hickey, and S.P. Colgan. 1997. Hypoxia enhances endotoxin-stimulated induction of functional intercellular adhesion molecule-1 (ICAM-1). Am. J. Physiol. 273: C1571-C1580.
19. Ogata, H., and D.K. Podolsky. 1997. Trefoil peptide expression and secretion is regulated by neuropeptides and acetylcholine. Am. J. Physiol. 273:G348-G354.
20. Caniggia, I., H. Mostachfi, J. Winter, M. Gassmann, S.J. Lye, M. Kuliszewski, and M. Post. 2000. Hypoxia-inducible factor-1 mediates the biological effects of oxygen on human trophoblast differentiation through TGFβ(3). J. Clin. Invest. 105:577-587.
21. Mashimo, H., D.C. Wu, D.K. Podolsky, and M.C. Fishman. 1996. Impaired defense of intestinal mucosa in mice lacking intestinal trefoil factor. Science. 274:262-265.
22. Napolitano, L.M., M.J. Koruda, A.A. Meyer, and C.C. Baker. 1996. The impact of femur fracture with associated soft tissue injury on immune function and intestinal permeability. Shock. 5:202-207.
23. Shreeniwas, R., S. Ogawa, F. Cozzolino, G. Torcia, N. Braunstein, C. Butura, J. Brett, H.B. Leiberman, M.B. Furie, J. Joseph-Silverstien, and D. Stern. 1991. Macrovascular and microvascular endothelium during long-term hypoxia: alterations in cell growth, monolayer permeability, and cell surface coagulant properties. J. Cell. Physiol. 146:8-17.
24. Furuta, G.T., A.L. Dzus, C.T. Taylor, and S.P. Colgan. 2000. Parallel induction of epithelial surface-associated chemokine and proteoglycan by cellular hypoxia: implications for neutrophil activation. J. Leukoc. Biol. 68:251-259.
25. Taylor, C.T., G.T. Furuta, K. Synnestvedt, and S.P. Colgan. 2000. Phosphorylation-dependent targeting of cAMP response element binding protein to the ubiquitin/proteasome pathway in hypoxia. Proc. Natl. Acad. Sci. USA. 97:12091-12096.
26. Zweiger, G. 1999. Knowledge discovery in gene-expression-microarray data: mining the information output of the genome. Trends Biotechnol. 17:429-436.
27. Thim, L. 1997. Trefoil peptides: from structure to function. Cell. Mol. Life Sci. 53:888-903.
28. Giraud, A.S. 2000. X. Trefoil peptide and EGF receptor/ ligand transgenic mice. Am. J. Physiol. Gastrointest. Liver Physiol. 278:G501-G506.
29. Beck, P.L., and D.K. Podolsky. 1999. Growth factors in inflammatory bowel disease. Inflamm. Bowel Dis. 5:44-60.
30. Ogata, H., N. Inoue, and D.K. Podolsky. 1998. Identification of a goblet cell-specific enhancer element in the rat intestinal trefoil factor gene promoter bound by a goblet cell nuclear protein. J. Biol. Chem. 273:3060-3067.
31. Efstathiou, J.A., M. Noda, A. Rowan, C. Dixon, R. Chinery, A. Jawhari, T. Hattori, N.A. Wright, W.F. Bodmer, and M. Pignatelli. 1998. Intestinal trefoil factor controls the expression of the adenomatous polyposis coli-catenin and the E-cadherin-catenin complexes in human colon carcinoma cells. Proc. Natl. Acad. Sci. USA. 95:3122-3127.
32. Kanai, M., C. Mullen, and D.K. Podolsky. 1998. Intestinal trefoil factor induces inactivation of extracellular signal-regulated protein kinase in intestinal epithelial cells. Proc. Natl. Acad. Sci. USA. 95:178-182.
33. Kinoshita, K., D.R. Taupin, H. Itoh, and D.K. Podolsky. 2000. Distinct pathways of cell migration and antiapoptotic response to epithelial injury: structure-function analysis of human intestinal trefoil factor. Mol. Cell. Biol. 20:4680-4690.
34. Kinugasa, T., T. Sakaguchi, X. Gu, and H.C. Reinecker. 2000. Claudins regulate the intestinal barrier in response to immune mediators. Gastroenterology, 118:1001-1011.
35. Bunn, H.F., and R.O. Poyton. 1996. Oxygen sensing and molecular adaptation to hypoxia. Physiol. Rev. 76:839-885.
36. Gassmann, M., and R.H. Wenger. 1997. HIF-1, a mediator of the molecular response to hypoxia. News Physiol. Sci. 12: 214-218.
37. Ratcliffe, P.J., J.F. O'Rourke, P.H. Maxwell, and C.W. Pugh. 1998. Oxygen sensing, hypoxia-inducible factor-1 and the regulation of mammalian gene expression. J. Exp. Biol. 201:1153-1162.
38. Presta, L.G., H. Chen, S.J. O'Conner, V. Chisholm, Y.G. Meng, L. Krummen, M. Winkler, and N. Ferrara. 1997. Humunization of an anti-vascular endothelial growth factor monoclonal antibody for the therapy of solid tumors and other disorders. Cancer Res. 57:4593-4599.
39. Kallio, P.J., W.J. Wilson, S. O'Brien, Y. Makino, and L. Poellinger. 1999. Regulation of the hypoxia-inducible transcription factor 1α by the ubiquitin-proteasome pathway. J. Biol. Chem. 274:6519-6525.
40. Minet, E., D. Mottet, G. Michel, I. Roland, M. Raes, J. Remacle, and C. Michiels. 1999. Hypoxia-induced activation of HIF-1: role of HIF-1α-Hsp90 interaction. FEBS Lett. 460:251-256.
41. De Maria, R., A. Zeuner, A. Eramo, C. Domenichelli, D. Bonci, F. Grignani, S.M. Srinivasula, E.S. Alnemri, U. Testa, and C. Peschle. 1999. Negative regulation of erythropoiesis by caspase-mediated cleavage of GATA-1. Nature. 401:489-493.
42. Kramer, M.F., P. Gunaratne, and G.C. Ferreira 2000. Transcriptional regulation ot the murine erythroid-specific 5-aminolevulinate synthase gene. Gene. 247:153-166.
43. Tarumoto, T., S. Imagawa, K. Ohmine, T. Nagai, M. Higuchi, N. Imai, N. Suzuki, M. Yamamoto, and K. Ozawa. 2000. N(G)-monomethyl-L-arginine inhibits erythropoietin gene expression by stimulating GATA-2. Blood. 96:1716-1722.
44. Unno, N., and M.P. Fink. 1998. Intestinal epithelial hyperpermeability. Mechanisms and relevance to disease. Gastroenterol. Clin. North Am. 27:289-307.