Inflammatory stimulation and hypoxia cooperatively activate HIF-1α in bronchial epithelial cells: Involvement of PI3K and NF-κB

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 298, Issue 5, 2010, Pages

  Jiang, Hong ^a   Zhu, Ye Sen ^a   Xu, Hui ^a   Sun, Yu ^a   Li, Qi Fang ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Airway epithelium; Hypoxia inducible factor 1 ; Interleukin 4; Tumor necrosis factor

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INOSITOL PHOSPHATE; INOSITOL PHOSPHATE 3 KINASE; INTERLEUKIN 4; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; RAPAMYCIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VASCULOTROPIN;

ARTICLE; BRONCHUS MUCOSA; CELL STIMULATION; CONTROLLED STUDY; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HYPOXIA; INFLAMMATION; MICROENVIRONMENT; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RESPIRATORY TRACT DISEASE; STIMULATION;

BASE SEQUENCE; BRONCHI; CELL HYPOXIA; CELL LINE; CELLS, CULTURED; EPITHELIAL CELLS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INFLAMMATION MEDIATORS; INTERLEUKIN-4; NF-KAPPA B; PHOSPHATIDYLINOSITOL 3-KINASES; RNA, MESSENGER; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 77951614276     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00394.2009     Document Type: Article

References (54)

1. Barnes PJ. Immunology of asthma and chronic obstructive pulmonary disease. Nat Rev Immunol 8: 183-192, 2008. (Pubitemid 351323287)
2. Belaiba RS, Bonello S, Zahringer C, Schmidt S, Hess J, Kietzmann T, Gorlach A. Hypoxia up-regulates hypoxia-inducible factor-1alpha transcription by involving phosphatidylinositol 3-kinase and nuclear factor kappaB in pulmonary artery smooth muscle cells. Mol Biol 18: 4691-4697, 2007. (Pubitemid 350246672)
3. Blouin CC, Page EL, Soucy GM, Richard DE. Hypoxic gene activation by lipopolysaccharide in macrophages: implication of hypoxia-inducible factor 1alpha. Blood 103: 1124-1130, 2004.
4. Bove PF, Hristova M, Wesley UV, Olson N, Lounsbury KM, van der Vliet A. Inflammatory levels of nitric oxide inhibit airway epithelial cell migration by inhibition of the kinase ERK1/2 and activation of hypoxia-inducible factor-1 alpha. J Biol Chem 283: 17919-17928, 2008.
5. Bove PF, Wesley UV, Greul AK, Hristova M, Dostmann WR, van der Vliet A. Nitric oxide promotes airway epithelial wound repair through enhanced activation of MMP-9. Am J Respir Cell Mol Biol 36: 138-146, 2007. (Pubitemid 46233465)
6. Bracken CP, Whitelaw ML, Peet DJ. The hypoxia-inducible factors: key transcriptional regulators of hypoxic responses. Cell Mol Life Sci 60: 1376-1393, 2003.
7. Burke B, Giannoudis A, Corke KP, Gill D, Wells M, Ziegler-Heitbrock L, Lewis CE. Hypoxia-induced gene expression in human macrophages: implications for ischemic tissues and hypoxia-regulated gene therapy. Am J Pathol 163: 1233-1243, 2003. (Pubitemid 37175073)
8. Cramer T, Johnson RS. A novel role for the hypoxia inducible transcription factor HIF-1alpha: critical regulation of inflammatory cell function. Cell Cycle 2: 192-193, 2003.
9. Cramer T, Yamanishi Y, Clausen BE, Forster I, Pawlinski R, Mackman N, Haase VH, Jaenisch R, Corr M, Nizet V, Firestein GS, Gerber HP, Ferrara N, Johnson RS. HIF-1alpha is essential for myeloid cell-mediated inflammation. Cell 112: 645-657, 2003. (Pubitemid 36331777)
10. Demasi M, Cleland LG, Cook-Johnson RJ, Caughey GE, James MJ. Effects of hypoxia on monocyte inflammatory mediator production: dissociation between changes in cyclooxygenase-2 expression and eicosanoid synthesis. J Biol Chem 278: 38607-38616, 2003. (Pubitemid 37221758)
11. Dery MA, Michaud MD, Richard DE. Hypoxia-inducible factor 1: regulation by hypoxic and non-hypoxic activators. Int J Biochem Cell Biol 37: 535-540, 2005. (Pubitemid 40022930)
12. Frede S, Freitag P, Otto T, Heilmaier C, Fandrey J. The proinflammatory cytokine interleukin 1beta and hypoxia cooperatively induce the expression of adrenomedullin in ovarian carcinoma cells through hypoxia inducible factor 1 activation. Cancer Res 65: 4690-4697, 2005. (Pubitemid 40740805)
13. Frede S, Stockmann C, Freitag P, Fandrey J. Bacterial lipopolysaccharide induces HIF-1 activation in human monocytes via p44/42 MAPK and NF-kappaB. Biochem J 396: 517-527, 2006. (Pubitemid 44228166)
14. Fukuda R, Hirota K, Fan F, Jung YD, Ellis LM, Semenza GL. Insulin-like growth factor 1 induces hypoxia-inducible factor 1-mediated vascular endothelial growth factor expression, which is dependent on MAP kinase and phosphatidylinositol 3-kinase signaling in colon cancer cells. J Biol Chem 277: 38205-38211, 2002. (Pubitemid 35154674)
15. Gingras AC, Gygi SP, Raught B, Polakiewicz RD, Abraham RT, Hoekstra MF, Aebersold R, Sonenberg N. Regulation of 4E-BP1 phosphorylation: a novel two-step mechanism. Genes Dev 13: 1422-1437, 1999. (Pubitemid 29270247)
16. Gorlach A, Diebold I, Schini-Kerth VB, Berchner-Pfannschmidt U, Roth U, Brandes RP, Kietzmann T, Busse R. Thrombin activates the hypoxia-inducible factor-1 signaling pathway in vascular smooth muscle cells: role of the p22(phox)-containing NADPH oxidase. Circ Res 89: 47-54, 2001. (Pubitemid 34135491)
17. Haddad JJ, Harb HL. Cytokines and the regulation of hypoxia-inducible factor (HIF)-1alpha. Int Immunopharma 5: 461-483, 2005. (Pubitemid 40430755)
18. Hara K, Yonezawa K, Kozlowski MT, Sugimoto T, Andrabi K, Weng QP, Kasuga M, Nishimoto I, Avruch J. Regulation of eIF-4E BP1 phosphorylation by mTOR. J Biol Chem 272: 26457-26463, 1997. (Pubitemid 27458864)
19. Hellwig-Burgel T, Rutkowski K, Metzen E, Fandrey J, Jelkmann W. Interleukin-1beta and tumor necrosis factor-alpha stimulate DNA binding of hypoxia-inducible factor-1. Blood 94: 1561-1567, 1999. (Pubitemid 29411306)
20. Hopfl G, Ogunshola O, Gassmann M. HIFs and tumors- causes and consequences. Am J Physiol Regul Integr Comp Physiol 286: R608-R623, 2004.
21. Huang LE, Gu J, Schau M, Bunn HF. Regulation of hypoxia-inducible factor 1alpha is mediated by an O2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc Natl Acad Sci USA 95: 7987-7992, 1998. (Pubitemid 28326053)
22. Jung Y, Isaacs JS, Lee S, Trepel J, Liu ZG, Neckers L. Hypoxia-inducible factor induction by tumour necrosis factor in normoxic cells requires receptor-interacting protein-dependent nuclear factor kappa B activation. Biochem J 370: 1011-1017, 2003. (Pubitemid 36399095)
23. Jung YJ, Isaacs JS, Lee S, Trepel J, Neckers L. IL-1beta-mediated up-regulation of HIF-1alpha via an NFkappaB/COX-2 pathway identifies HIF-1 as a critical link between inflammation and oncogenesis. FASEB J 17: 2115-2117, 2003.
24. Jung YJ, Isaacs JS, Lee S, Trepel J, Neckers L. Microtubule disruption utilizes an NFkappa B-dependent pathway to stabilize HIF-1alpha protein. J Biol Chem 278: 7445-7452, 2003. (Pubitemid 36800750)
25. Kietzmann T, Samoylenko A, Roth U, Jungermann K. Hypoxia-inducible factor-1 and hypoxia response elements mediate the induction of plasminogen activator inhibitor-1 gene expression by insulin in primary rat hepatocytes. Blood 101: 907-914, 2003. (Pubitemid 36139358)
26. Laughner E, Taghavi P, Chiles K, Mahon PC, Semenza GL. HER2 (neu) signaling increases the rate of hypoxia-inducible factor 1alpha (HIF-1alpha) synthesis: novel mechanism for HIF-1-mediated vascular endothelial growth factor expression. Mol Cell Biol 21: 3995-4004, 2001. (Pubitemid 32476461)
27. Leigh R, Oyelusi W, Wiehler S, Koetzler R, Zaheer RS, Newton R, Proud D. Human rhinovirus infection enhances airway epithelial cell production of growth factors involved in airway remodeling. J Allergy Clin Immunol 121: 1238-1245, e1234, 2008.
28. Li QF, Wang XR, Yang YW, Lin H. Hypoxia upregulates hypoxia inducible factor (HIF)-3alpha expression in lung epithelial cells: characterization and comparison with HIF-1alpha. Cell Res 16: 548-558, 2006. (Pubitemid 43920283)
29. Li QF, Wang XR, Yang YW, Su DS. Up-regulation of hypoxia inducible factor 1alpha by isoflurane in Hep3B cells. Anesthesiology 105: 1211-1219, 2006.
30. Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME, Wykoff CC, Pugh CW, Maher ER, Ratcliffe PJ. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399: 271-275, 1999.
31. Mayerhofer M, Valent P, Sperr WR, Griffin JD, Sillaber C. BCR/ABL induces expression of vascular endothelial growth factor and its transcriptional activator, hypoxia inducible factor-1alpha, through a pathway involving phosphoinositide 3-kinase and the mammalian target of rapamycin. Blood 100: 3767-3775, 2002. (Pubitemid 35303950)
32. Maynard MA, Ohh M. The role of hypoxia-inducible factors in cancer. Cell Mol Life Sci 64: 2170-2180, 2007.
33. McMahon S, Charbonneau M, Grandmont S, Richard DE, Dubois CM. Transforming growth factor beta1 induces hypoxia-inducible factor- 1 stabilization through selective inhibition of PHD2 expression. J Biol Chem 281: 24171-24181, 2006. (Pubitemid 44274191)
34. Metzen E, Ratcliffe PJ. HIF hydroxylation and cellular oxygen sensing. Biol Chem 385: 223-230, 2004. (Pubitemid 38679067)
35. Nave BT, Ouwens M, Withers DJ, Alessi DR, Shepherd PR. Mammalian target of rapamycin is a direct target for protein kinase B: identification of a convergence point for opposing effects of insulin and amino-acid deficiency on protein translation. Biochem J 344: 427-431, 1999.
36. Page EL, Chan DA, Giaccia AJ, Levine M, Richard DE. Hypoxia-inducible factor-1alpha stabilization in nonhypoxic conditions: role of oxidation and intracellular ascorbate depletion. Mol Biol 19: 86-94, 2008. (Pubitemid 351186135)
37. Page EL, Robitaille GA, Pouyssegur J, Richard DE. Induction of hypoxia-inducible factor-1alpha by transcriptional and translational mechanisms. J Biol Chem 277: 48403-48409, 2002. (Pubitemid 35470797)
38. Peterson RT, Desai BN, Hardwick JS, Schreiber SL. Protein phosphatase 2A interacts with the 70-kDa S6 kinase and is activated by inhibition of FKBP12-rapamycin associated protein. Proc Natl Acad Sci USA 96: 4438-4442, 1999.
39. Polosukhin VV, Lawson WE, Milstone AP, Egunova SM, Kulipanov AG, Tchuvakin SG, Massion PP, Blackwell TS. Association of progressive structural changes in the bronchial epithelium with subepithelial fibrous remodeling: a potential role for hypoxia. Virchows Arch 451: 793-803, 2007.
40. Rosenwald IB, Kaspar R, Rousseau D, Gehrke L, Leboulch P, Chen JJ, Schmidt EV, Sonenberg N, London IM. Eukaryotic translation initiation factor 4E regulates expression of cyclin D1 at transcriptional and post-transcriptional levels. J Biol Chem 270: 21176-21180, 1995.
41. Scharte M, Jurk K, Kehrel B, Zarbock A, Van Aken H, Singbartl K. IL-4 enhances hypoxia induced HIF-1alpha protein levels in human transformed intestinal cells. FEBS Lett 580: 6399-6404, 2006. (Pubitemid 44750927)
42. Schleimer RP, Kato A, Kern R, Kuperman D, Avila PC. Epithelium: at the interface of innate and adaptive immune responses. J Allergy Clin Immunol 120: 1279-1284, 2007. (Pubitemid 350216601)
43. Schofield CJ, Ratcliffe PJ. Oxygen sensing by HIF hydroxylases. Nature Rev 5: 343-354, 2004.
44. Sekulic A, Hudson CC, Homme JL, Yin P, Otterness DM, Karnitz LM, Abraham RT. A direct linkage between the phosphoinositide 3-kinase- AKT signaling pathway and the mammalian target of rapamycin in mitogen-stimulated and transformed cells. Cancer Res 60: 3504-3513, 2000. (Pubitemid 30482170)
45. Sonenberg N, Gingras AC. The mRNA 5′ cap-binding protein eIF4E and control of cell growth. Current Opin Cell Biol 10: 268-275, 1998. (Pubitemid 28174770)
46. Stiehl DP, Jelkmann W, Wenger RH, Hellwig-Burgel T. Normoxic induction of the hypoxia-inducible factor 1alpha by insulin and interleukin- 1beta involves the phosphatidylinositol 3-kinase pathway. FEBS Lett 512: 157-162, 2002. (Pubitemid 34164471)
47. Tacchini L, De Ponti C, Matteucci E, Follis R, Desiderio MA. Hepatocyte growth factor-activated NF-kappaB regulates HIF-1 activity and ODC expression, implicated in survival, differently in different carcinoma cell lines. Carcinogenesis 25: 2089-2100, 2004. (Pubitemid 39534845)
48. Taylor CT. Interdependent roles for hypoxia inducible factor and nuclear factor-kappaB in hypoxic inflammation. J Physiol 586: 4055-4059, 2008.
49. Treins C, Giorgetti-Peraldi S, Murdaca J, Semenza GL, Van Obberghen E. Insulin stimulates hypoxia-inducible factor 1 through a phosphatidylinositol 3-kinase/target of rapamycin-dependent signaling pathway. J Biol Chem 277: 27975-27981, 2002. (Pubitemid 34966746)
50. van Uden P, Kenneth NS, Rocha S. Regulation of hypoxia-inducible factor-1alpha by NF-kappaB. Biochem J 412: 477-484, 2008.
51. Yu AY, Frid MG, Shimoda LA, Wiener CM, Stenmark K, Semenza GL. Temporal, spatial, and oxygen-regulated expression of hypoxia-inducible factor-1 in the lung. Am J Physiol Lung Cell Mol Physiol 275: L818-L826, 1998. (Pubitemid 28491865)
52. Zhai Y, Zhong Z, Chen CY, Xia Z, Song L, Blackburn MR, Shyu AB. Coordinated changes in mRNA turnover, translation, and RNA processing bodies in bronchial epithelial cells following inflammatory stimulation. Mol Cell Biol 28: 7414-7426, 2008.
53. Zhou J, Brune B. Cytokines and hormones in the regulation of hypoxia inducible factor-1alpha (HIF-1alpha). Cardiovasc Hematol Agents Med Chem 4: 189-197, 2006.
54. Zhou J, Schmid T, Brune B. Tumor necrosis factor-alpha causes accumulation of a ubiquitinated form of hypoxia inducible factor-1alpha through a nuclear factor-kappaB-dependent pathway. Mol Biol Cell 14: 2216-2225, 2003.