Hypoxia: An alarm signal during intestinal inflammation

Nature Reviews Gastroenterology and Hepatology

Volumn 7, Issue 5, 2010, Pages 281-287

  Colgan, Sean P ^a   Taylor, Cormac T ^b  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

2 OXOGLUTARIC ACID; DIMETHYLOXALOYLGLYCINE; ENZYME INHIBITOR; FG 4497; HYDROXAMIC ACID DERIVATIVE; HYPOXIA INDUCIBLE FACTOR; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE INHIBITOR; UNCLASSIFIED DRUG;

CELL FUNCTION; CELL TYPE; ENTERITIS; ENZYME INHIBITION; GASTROINTESTINAL MUCOSA; GENE CONTROL; HUMAN; HYPOXIA; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; INTESTINE EPITHELIUM CELL; LAMINA PROPRIA; MUCOSA INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; UPREGULATION;

ANIMALS; ANOXIA; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; INFLAMMATORY BOWEL DISEASES; INTESTINAL MUCOSA; OXIDATIVE STRESS;

EID: 77952092406     PISSN: 17595045     EISSN: 17595053     Source Type: Journal    
DOI: 10.1038/nrgastro.2010.39     Document Type: Review

References (61)

1. Laukoetter, G. G., Bruewer, M. & Nusrat, A. Regulation of the intestinal epithelial barrier by the apical junctional complex. Curr. Opin. Gastroenterol. 22, 85-89 (2006).
2. Turner, J. R. Intestinal mucosal barrier function in health and disease. Nat. Rev. Immunol. 9, 799-809 (2009).
3. Taylor, C. T. & Colgan, S. P. Hypoxia and gastrointestinal disease. J. Mol. Med. 85, 1295-1300 (2008).
4. Furuta, G. T. et al. Hypoxia-inducible factor 1-dependent induction of intestinal trefoil factor protects barrier function during hypoxia. J. Exp. Med. 193, 1027-1034 (2001).
5. Pollard, T. D. & Borisy, G. G. Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453-465 (2003).
6. Borregaard, N. & Herlin, T. Energy metabolism of human neutrophils during phagocytosis. J. Clin. Invest. 70, 550-557 (1982).
7. El-Benna, J., Dang, P. M. & Gougerot-Pocidalo, M. A. Priming of the neutrophil NADPH oxidase activation: role of p47phox phosphorylation and NOX2 mobilization to the plasma membrane. Semin. Immunopathol. 30, 279-289 (2008).
8. Gabig, G. G., Bearman, S. I. & Babior, B. M. Effects of oxygen tension and pH on the respiratory burst of human neutrophils. Blood 53, 1133-1139 (1979).
9. Fox, J. J., Hammerman, P. S. & Thompson, C. B. Fuel feeds function: energy metabolism and the T-cell response. Nat. Rev. Immunol. 5, 844-852 (2005).
10. Sitkovsky, M. & Lukashev, D. Regulation of immune cells by local-tissue oxygen tension: HIF1 alpha and adenosine receptors. Nat. Rev. Immunol. 5, 712-721 (2005).
11. Hatoum, A. A., Heidemann, J. & Binion, D. G. The intestinal microvasculature as a therapeutic target in inflammatory bowel disease. Ann. NY Acad. Sci. 1072, 78-97 (2006).
12. Danese, S., Dejana, E. & Fiocchi, C. Immune regulation by microvascular endothelial cells: directing innate and adaptive immunity, coagulation, and inflammation. J. Immunol. 178, 6017-6022 (2007).
13. Karhausen, J. et al. Epithelial hypoxiainducible factor-1 is protective in murine experimental colitis. J. Clin. Invest. 114, 1098-1106 (2004).
14. Evans, S. M. et al. Detection of hypoxia in human squamous cell carcinoma by EF5 binding. Cancer Res. 60, 2018-2024 (2000).
15. Takasawa, M., Moustafa, R. R. & Baron, J. C. Applications of nitroimidazole in vivo hypoxia imaging in ischemic stroke. Stroke 39, 1629-1637 (2008).
16. Overgaard, J. Hypoxic radiosensitization: adored and ignored. J. Clin. Oncol. 25, 4066-4074 (2007).
17. Kizaka-Kondoh, S. & Konse-Nagasawa, H. Significance of nitroimidazole compounds and hypoxia-inducible factor-1 for imaging tumor hypoxia. Cancer Sci. 100, 1366-1373 (2009).
18. Mastrogiannaki, M. et al. HIF-2alpha, but not HIF-1alpha, promotes iron absorption in mice. J. Clin. Invest. 119, 1159-1166 (2009).
19. Ratcliffe, P. J. HIF-1 and HIF-2: working alone or together in hypoxia? J. Clin. Invest. 117, 862-865 (2007).
20. Comerford, K. M. et al. Hypoxia-inducible factor-1-dependent regulation of the multidrug resistance (MDR1) gene. Cancer Res. 62, 3387-3394 (2002).
21. Synnestvedt, K. et al. Ecto-5'-nucleotidase (CD73) regulation by hypoxia-inducible factor-1 (HIF-1) mediates permeability changes in intestinal epithelia. J. Clin. Invest. 110, 993-1002 (2002).
22. 2B receptors. J. Exp. Med. 198, 783-796 (2003).
23. Cummins, E. P. et al. The hydroxylase inhibitor dimethyloxalylglycine is protective in a murine model of colitis. Gastroenterology 134, 156-165 (2008).
24. Han, O. O., Kim, S. S., Kim, C. C., Joe, E. H. & Kim, W. K. Synergistic expression of inducible nitric oxide synthase by phorbol ester and interferon-gamma is mediated through NF-kappaB and ERK in microglial cells. J. Neurosci. Res. 73, 659-669 (2003).
25. Morote-Garcia, C. C., Rosenberger, P., Nivillac, M. M., Coe, I. R. & Eltzschig, H. K. Hypoxia-inducible factor-dependent repression of equilibrative nucleoside transporter 2 attenuates mucosal inflammation during intestinal hypoxia. Gastroenterology 136, 607-618 (2009).
26. Robinson, A. et al. Mucosal protection by hypoxia-inducible factor prolyl hydroxylase inhibition. Gastroenterology 134, 145-155 (2008).
27. Shah, Y. M. et al. Hypoxia-inducible factor augments experimental colitis through an MIF-dependent inflammatory signaling cascade. Gastroenterology 134, 2036-2048 (2008).
28. Giatromanolaki, A. et al. Hypoxia inducible factor 1alpha and 2alpha overexpression in inflammatory bowel disease. J. Clin. Pathol. 56, 209-213 (2003).
29. Mariani, F. et al. Cyclooxygenase-2 and hypoxiainducible factor-1alpha protein expression is related to inflammation, and up-regulated since the early steps of colorectal carcinogenesis. Cancer Lett. 279, 221-229 (2009).
30. Matthijsen, R. A. et al. Enterocyte shedding and epithelial lining repair following ischemia of the human small intestine attenuate inflammation. PLoS One 4, e7045 (2009).
31. Louis, N. A. et al. Selective induction of mucin-3 by hypoxia in intestinal epithelia. J. Cell Biochem. 99, 1616-1627 (2006).
32. Makino, Y. et al. Hypoxia-inducible factor regulates survival of antigen receptor-driven T cells. J. Immunol. 171, 6534-6540 (2003).
33. Nizet, v. & Johnson, R. S. Interdependence of hypoxic and innate immune responses. Nat. Rev. Immunol. 9, 609-617 (2009).
34. Kong, T., Eltzschig, K. K., Karhausen, J., Colgan, S. P. & Shelley, C. S. Leukocyte adhesion during hypoxia is mediated by HIF-1-dependent induction of beta2 integrin gene expression. Proc. Natl Acad. Sci. USA 101, 10440-10445 (2004).
35. Kong, T., Scully, M., Shelley, C. S. & Colgan, S. P. Identification of Pur alpha as a new hypoxia response factor responsible for coordinated induction of the beta 2 integrin family. J. Immunol. 179, 1934-1941 (2007).
36. Kuhl, A. A. et al. Aggravation of different types of experimental colitis by depletion or adhesion blockade of neutrophils. Gastroenterology 133, 1882-1892 (2007).
37. Kaelin, W. G. Jr & Ratcliffe, P. J. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol. Cell 30, 393-402 (2008).
38. Cummins, E. P. et al. Prolyl hydroxylase-1 negatively regulates IkappaB kinase-beta, giving insight into hypoxia-induced NFkappaB activity. Proc. Natl Acad. Sci. USA 103, 18154-18159 (2006).
39. Aragones, J. et al. Deficiency or inhibition of oxygen sensor Phd1 induces hypoxia tolerance by reprogramming basal metabolism. Nat. Genet. 40, 170-180 (2008).
40. Schneider, M. et al. Loss or silencing of the PHD1 prolyl hydroxylase protects livers of mice against ischemia/reperfusion injury. Gastroenterology doi:10/1053/j.gastro.2009.09.057.
41. Mazzone, M. et al. Heterozygous deficiency of PHD2 restores tumor oxygenation and inhibits metastasis via endothelial normalization. Cell 136, 839-851 (2009).
42. Ozolins, T. R. et al. Defects in embryonic development of EGLN1/PHD2 knockdown transgenic mice are associated with induction of Igfbp in the placenta. Biochem. Biophys. Res. Commun. 390, 372-376 (2009).
43. Bishop, T. et al. Abnormal sympathoadrenal development and systemic hypotension in PHD3-/-mice. Mol. Cell Biol. 28, 3386-3400 (2008).
44. Taylor, C. T. Interdependent roles for hypoxia inducible factor and nuclear factor-kappaB in hypoxic inflammation. J. Physiol. 586, 4055-4059 (2008).
45. Rosenberger, P. et al. Identification of vasodilatorstimulated phosphoprotein (vASP) as an HIF-regulated tissue permeability factor during hypoxia. FASEB J. 21, 2613-2621 (2007).
46. Chen, Z. et al. Signal-induced site-specific phosphorylation targets I kappa B alpha to the ubiquitin-proteasome pathway. Genes Dev. 9, 1586-1597 (1995).
47. Luo, L. L., Kamata, H. & Karin, M. IKK/NF-kappaB signaling: balancing life and death-a new approach to cancer therapy. J. Clin. Invest. 115, 2625-2632 (2005).
48. Chen, Z. J. Ubiquitin signalling in the NF-kappaB pathway. Nat. Cell Biol. 7, 758-765 (2005).
49. Cockman, M. E. et al. Posttranslational hydroxylation of ankyrin repeats in IkappaB proteins by the hypoxia-inducible factor (HIF) asparaginyl hydroxylase, factor inhibiting HIF (FIH). Proc. Natl Acad. Sci. USA 103, 14767-14772 (2006).
50. Zaph, C. et al. Epithelial-cell-intrinsic IKK-beta expression regulates intestinal immune homeostasis. Nature 446, 552-556 (2007).
51. Rius, J. et al. NF-kappaB links innate immunity to the hypoxic response through transcriptional regulation of HIF-1alpha. Nature 453, 807-811 (2008).
52. Coleman, M. L. et al. Asparaginyl hydroxylation of the Notch ankyrin repeat domain by factor inhibiting hypoxia-inducible factor. J. Biol. Chem. 282, 24027-24038 (2007).
53. Koditz, J. et al. Oxygen-dependent ATF-4 stability is mediated by the PHD3 oxygen sensor. Blood 110, 3610-3617 (2007).
54. Mole, D. R. et al. 2-oxoglutarate analogue inhibitors of HIF prolyl hydroxylase. Bioorg. Med. Chem. Lett. 13, 2677-2680 (2003).
55. Masson, N. & Ratcliffe, P. J. HIF prolyl and asparaginyl hydroxylases in the biological response to intracellular O (2) levels. J. Cell Sci. 116, 3041-3049 (2003).
56. Schofield, C. J. & Ratcliffe, P. J. Oxygen sensing by HIF hydroxylases. Nat. Rev. Mol. Cell Biol. 5, 343-354 (2004).
57. Bruick, R. K. Oxygen sensing in the hypoxic response pathway: regulation of the hypoxiainducible transcription factor. Genes Dev. 17, 2614-2623 (2003).
58. Nwogu, J. I. et al. Inhibition of collagen synthesis with prolyl 4-hydroxylase inhibitor improves left ventricular function and alters the pattern of left ventricular dilatation after myocardial infarction. Circulation 104, 2216-2221 (2001).
59. Schlemminger, I. et al. Analogues of dealanylalahopcin are inhibitors of human HIF prolyl hydroxylases. Bioorg. Med. Chem. Lett. 13, 1451-1454 (2003).
60. Jelkmann, W. Control of erythropoietin gene expression and its use in medicine. Methods Enzymol. 435, 179-197 (2007).
61. Semenza, G. Defining the role of hypoxiainducible factor in cancer biology and therapeutics. Oncogene 29, 625-634 (2010).