DMOG ameliorates IFN-γ-induced intestinal barrier dysfunction by suppressing PHD2-dependent HIF-1α degradation

Journal of Interferon and Cytokine Research

Volumn 34, Issue 1, 2014, Pages 60-69

  Wang, Wen Sheng ^a   Liang, Hong Yin ^b   Cai, Yu Jiao ^a   Yang, Hua ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

^b CHENGDU MILITARY GENERAL HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ACTIN; DECAY ACCELERATING FACTOR; GAMMA INTERFERON; GLYCINE DERIVATIVE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INTESTINAL TREFOIL FACTOR; MUCIN 3; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; DICARBOXYLIC AMINO ACID; EGLN1 PROTEIN, HUMAN; HIF1A PROTEIN, HUMAN; HYPOXIA INDUCIBLE FACTOR PROLINE DIOXYGENASE; IFNG PROTEIN, HUMAN; OXALYLGLYCINE;

ARTICLE; CELL STRAIN HT29; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CYTOKINE RELEASE; ELECTRIC RESISTANCE; ENZYME STABILITY; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HYPOXIA; IN VITRO STUDY; INTESTINAL BARRIER FUNCTION; INTESTINE FUNCTION; INTESTINE FUNCTION DISORDER; LYMPHOCYTE; MONOLAYER CULTURE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSIENT TRANSFECTION; WESTERN BLOTTING; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; GENETICS; HT 29 CELL LINE; INTESTINE MUCOSA; METABOLISM; STRUCTURE ACTIVITY RELATION; TUMOR CELL CULTURE;

AMINO ACIDS, DICARBOXYLIC; HT29 CELLS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; HYPOXIA-INDUCIBLE FACTOR-PROLINE DIOXYGENASES; INTERFERON-GAMMA; INTESTINAL MUCOSA; STRUCTURE-ACTIVITY RELATIONSHIP; TUMOR CELLS, CULTURED;

EID: 84892141876     PISSN: 10799907     EISSN: 15577465     Source Type: Journal    
DOI: 10.1089/jir.2013.0040     Document Type: Article

References (46)

1. Beaurepaire C, Smyth D, McKay DM. 2009. Interferon-gamma regulation of intestinal epithelial permeability. J Interferon Cytokine Res 29(3):133-144
2. Billiau A, Matthys P. 2009. Interferon-gamma: A historical perspective. Cytokine Growth Factor Rev 20(2):97-113
3. Brahimi-Horn MC, Pouyssegur J. 2009. HIF at a glance. J Cell Sci 122(Pt 8):1055-1057
4. Chan DA, Sutphin PD, Denko NC, Giaccia AJ. 2002. Role of prolyl hydroxylation in oncogenically stabilized hypoxia-inducible factor-1alpha. J Biol Chem 277(42):40112-40117
5. Chan JY, Tsai CY, Wu CH, Li FC, Dai KY, Sun EY, Chan SH, Chang AY. 2011. Sumoylation of hypoxia-inducible factor-1alpha ameliorates failure of brain stem cardiovascular regulation in experimental brain death. PLoS One 6(3):e17375
6. Cheng J, Kang X, Zhang S, Yeh ET. 2007. SUMO-specific protease 1 is essential for stabilization of HIF1alpha during hypoxia. Cell 131(3):584-595
7. Colgan SP, Eltzschig HK. 2012. Adenosine and hypoxia-inducible factor signaling in intestinal injury and recovery. Annu Rev Physiol 74:153-175
8. Colgan SP, Eltzschig HK, Eckle T, Thompson LF. 2006. Physiological roles for ecto-5¢-nucleotidase (CD73). Purinergic Signal 2(2):351-360
9. Colgan SP, Taylor CT. 2010. Hypoxia: An alarm signal during intestinal inflammation. Nat Rev Gastroenterol Hepatol 7(5):281-287
10. Conde E, Alegre L, Blanco-Sanchez I, Saenz-Morales D, Aguado-Fraile E, Ponte B, Ramos E, Saiz A, Jimenez C, Ordonez A, Lopez-Cabrera M, del Peso L, de Landazuri MO, Liano F, Selgas R, Sanchez-Tomero JA, Garcia-Bermejo ML. 2012. Hypoxia inducible factor 1-Alpha (HIF-1 alpha) is induced during reperfusion after renal ischemia and is critical for proximal tubule cell survival. PLoS One 7(3):e33258
11. Cummins EP, Berra E, Comerford KM, Ginouves A, Fitzgerald KT, Seeballuck F, Godson C, Nielsen JE, Moynagh P, Pouyssegur J, Taylor CT. 2006. Prolyl hydroxylase-1 negatively regulates IkappaB kinase-beta, giving insight into hypoxiainduced NFkappaB activity. Proc Natl Acad Sci USA 103(48):18154-18159
12. Cummins EP, Seeballuck F, Keely SJ, Mangan NE, Callanan JJ, Fallon PG, Taylor CT. 2008. The hydroxylase inhibitor dimethyloxalylglycine is protective in a murine model of colitis. Gastroenterology 134(1):156-165
13. Elvidge GP, Glenny L, Appelhoff RJ, Ratcliffe PJ, Ragoussis J, Gleadle JM. 2006. Concordant regulation of gene expression by hypoxia and 2-oxoglutarate-dependent dioxygenase inhibition: The role of HIF-1alpha, HIF-2alpha, and other pathways. J Biol Chem 281(22):15215-15226
14. Feinman R, Deitch EA, Watkins AC, Abungu B, Colorado I, Kannan KB, Sheth SU, Caputo FJ, Lu Q, Ramanathan M, Attan S, Badami CD, Doucet D, Barlos D, Bosch-Marce M, Semenza GL, Xu DZ. 2010. HIF-1 mediates pathogenic inflammatory responses to intestinal ischemia-reperfusion injury. Am J Physiol Gastrointest Liver Physiol 299(4):G833-G843
15. Fujita N, Markova D, Anderson DG, Chiba K, Toyama Y, Shapiro IM, Risbud MV. 2012. Expression of prolyl hydroxylases (PHDs) is selectively controlled by HIF-1 and HIF-2 proteins in nucleus pulposus cells of the intervertebral disc: Distinct roles of PHD2 and PHD3 proteins in controlling HIF-1alpha activity in hypoxia. J Biol Chem 287(20):16975-16986
16. Furuta GT, Turner JR, Taylor CT, Hershberg RM, Comerford K, Narravula S, Podolsky DK, Colgan SP. 2001. Hypoxia-inducible factor 1-dependent induction of intestinal trefoil factor protects barrier function during hypoxia. J Exp Med 193(9): 1027-1034
17. Gerber SA, Yatsula B, Maier CL, Sadler TJ, Whittaker LW, Pober JS. 2009. Interferon-gamma induces prolyl hydroxylase (PHD)3 through a STAT1-dependent mechanism in human endothelial cells. Arterioscler Thromb Vasc Biol 29(9):1363-1369
18. Greer SN, Metcalf JL, Wang Y, Ohh M. 2012. The updated biology of hypoxia-inducible factor. EMBO J 31(11):2448-2460
19. Glover LN, Irizarry K, Scully M, Campbell EL., Bowers BE, Aherne CM, Kominsky DJ, MacManus CF, Colgan SP. 2011. IFN-g attenuates hypoxia-inducible factor (HIF) activity in intestinal epithelial cells through transcriptional repression of HIF-1b. J Immunol 186(3):1790-1798
20. Hiroi M, Mori K, Sakaeda Y, Shimada J, Ohmori Y. 2009. STAT1 represses hypoxia-inducible factor-1-mediated transcription. Biochem Biophys Res Commun 387(4):806-810
21. Jose-Cunilleras E, Viu J, Corradini I, Armengou L, Cesarini C, Monreal L. 2012. Energy expenditure of critically ill neonatal foals. Equine Vet J Suppl (41):48-51
22. Kannan KB, Colorado I, Reino D, Palange D, Lu Q, Qin X, Abungu B, Watkins A, Caputo FJ, Xu DZ, Semenza GL, Deitch EA, Feinman R. 2011. Hypoxia-inducible factor plays a gut-injurious role in intestinal ischemia reperfusion injury. Am J Physiol Gastrointest Liver Physiol 300(5):G853-G861
23. Koh MY, Powis G. 2009. HAF: The new player in oxygenindependent HIF-1alpha degradation. Cell Cycle 8(9):1359-1366
24. Kosugi M, Ahmad R, Alam M, Uchida Y, Kufe D. 2011. MUC1-C oncoprotein regulates glycolysis and pyruvate kinase M2 activity in cancer cells. PLoS One 6(11):e28234
25. Kress S, Stein A, Maurer P, Weber B, Reichert J, Buchmann A, Huppert P, Schwarz M. 1998. Expression of hypoxia-inducible genes in tumor cells. J Cancer Res Clin Oncol 124(6):315-320
26. Louis NA, Hamilton KE, Canny G, Shekels LL, Ho SB, Colgan SP. 2006. Selective induction of mucin-3 by hypoxia in intestinal epithelia. J Cell Biochem 99(6):1616-1627
27. Louis NA, Hamilton KE, Kong T, Colgan SP. 2005. HIF-dependent induction of apical CD55 coordinates epithelial clearance of neutrophils. FASEB J 19(8):950-959
28. Luo W, Hu H, Chang R, Zhong J, Knabel M, O'Meally R, Cole RN, Pandey A, Semenza GL. 2011. Pyruvate kinase M2 is a PHD3-stimulated coactivator for hypoxia-inducible factor 1. Cell 145(5):732-744
29. Marchiando AM, Graham WV, Turner Jr. 2010. Epithelial barriers in homeostasis and disease. Annu Rev Pathol 5:119-144
30. Milkiewicz M, Pugh CW, Egginton S. 2004. Inhibition of endogenous HIF inactivation induces angiogenesis in ischaemic skeletal muscles of mice. J Physiol 560(Pt 1):21-26
31. Nakayama K. 2009. Cellular signal transduction of the hypoxia response. J Biochem 146(6):757-765
32. Ratcliffe PJ. 2007. HIF-1 and HIF-2: Working alone or together in hypoxiä J Clin Invest 117(4):862-865
33. Roman J, Rangasamy T, Guo J, Sugunan S, Meednu N, Packirisamy G, Shimoda LA, Golding A, Semenza G, Georas SN. 2010. T-cell activation under hypoxic conditions enhances IFNgamma secretion. Am J Respir Cell Mol Biol 42(1):123-128
34. Rosenberger P, Khoury J, Kong T, Weissmuller T, Robinson AM, Colgan SP. 2007. Identification of vasodilator-stimulated phosphoprotein (VASP) as an HIF-regulated tissue permeability factor during hypoxia. FASEB J 21(10):2613-2621
35. Semenza GL. 2012. Hypoxia-inducible factors: Mediators of cancer progression and targets for cancer therapy. Trends Pharmacol Sci 33(4):207-214
36. Shah YM, Ito S, Morimura K, Chen C, Yim SH, Haase VH, Gonzalez FJ. 2008. Hypoxia-inducible factor augments experimental colitis through an MIF-dependent inflammatory signaling cascade. Gastroenterology 134(7):2036-2048, 2048.e1-3
37. Shibahara T, Miyazaki K, Sato D, Matsui H, Yanaka A, Nakahara A, Tanaka N. 2005. Alteration of intestinal epithelial function by intraepithelial lymphocyte homing. J Gastroenterol 40(9):878-886
38. Sun L, Wang W, Xiao W, Liang H, Yang Y, Yang H. 2012. Angiotensin II induces apoptosis in intestinal epithelial cells through the AT2 receptor, GATA-6 and the Bax pathway. Biochem Biophys Res Commun 424(4):663-668
39. Synnestvedt K, Furuta GT, Comerford KM, Louis N, Karhausen J, Eltzschig HK, Hansen KR, Thompson LF, Colgan SP. 2002. Ecto-5¢-nucleotidase (CD73) regulation by hypoxia-inducible factor-1 mediates permeability changes in intestinal epithelia. J Clin Invest 110(7):993-1002
40. Taylor CT, Colgan SP. 2007. Hypoxia and gastrointestinal disease. J Mol Med (Berl) 85(12):1295-1300
41. Tennant DA. 2011. PK-M2 Makes Cells Sweeter on HIF1. Cell 145(5):647-649
42. Turner Jr. 2009. Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 9(11):799-809
43. Ulrich HD. 2007. SUMO teams up with ubiquitin to manage hypoxia. Cell 131(3):446-447
44. Vannay A, Sziksz E, Prokai A, Veres G, Molnar K, Szakal DN, Onody A, Korponay-Szabo IR, Szabo A, Tulassay T, Arato A, Szebeni B. 2010. Increased expression of hypoxia-inducible factor 1alpha in coeliac disease. Pediatr Res 68(2):118-122
45. Xu A, Yao M, Xu G, Ying J, Ma W, Li B, Jin Y. 2012. A physical model for the size-dependent cellular uptake of nanoparticles modified with cationic surfactants. Int J Nanomedicine 7:3547-3554
46. Yang H, Fan Y, Teitelbaum DH. 2003. Intraepithelial lymphocyte-derived interferon-gamma evokes enterocyte apoptosis with parenteral nutrition in mice. Am J Physiol Gastrointest Liver Physiol 284(4):G629-G637