Imaging of the hypoxia-inducible factor pathway: Insights into oxygen sensing

European Respiratory Journal

Volumn 32, Issue 1, 2008, Pages 210-217

  Berchner Pfannschmidt, U ^a   Frede, S ^a   Wotzlaw, C ^a   Fandrey, J ^a  

^a UNIVERSITY OF DUISBURG ESSEN   (Germany)

Author keywords

Fluorescence recovery after photo bleaching; Fluorescence resonance energy transfer; Green fluorescent protein fusion proteins; Hypoxia inducible factor 1; Immunohistology; In vivo imaging

Indexed keywords

CYAN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN; HYPOXIA INDUCIBLE FACTOR 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 1BETA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; YELLOW FLUORESCENT PROTEIN; ARNT PROTEIN, HUMAN; HIF1A PROTEIN, HUMAN;

ARTICLE; BLEACHING; CELL HYPOXIA; CELL INTERACTION; CELL MIGRATION; CELL SPECIFICITY; CELLULAR DISTRIBUTION; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; LASER MICROSCOPY; NONHUMAN; OXYGEN CONCENTRATION; OXYGEN SENSING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; SPHEROID CELL; TRANSCRIPTION INITIATION; TUMOR CELL; ANIMAL; ANOXIA; CONFOCAL MICROSCOPY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION PROFILING; METABOLISM; METHODOLOGY; MOUSE; RAT; REVIEW;

ANIMALS; ANOXIA; ARYL HYDROCARBON RECEPTOR NUCLEAR TRANSLOCATOR; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION PROFILING; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IMMUNOHISTOCHEMISTRY; MICE; MICROSCOPY, CONFOCAL; RATS;

EID: 52749085519     PISSN: 09031936     EISSN: 13993003     Source Type: Journal    
DOI: 10.1183/09031936.00013408     Document Type: Article

References (53)

1. Semenza GL. Hypoxia-inducible factor 1: oxygen homeostasis and disease pathophysiology. Trends Mol Med 2001; 7: 345-350.
2. Ema M, Taya S, Yokotani N, Sogawa K, Matsuda Y, Fujii-Kuriyama Y. A novel bHLH-PAS factor with close sequence similarity to hypoxia-inducible factor 1α regulates the VEGF expression and is potentially involved in lung and vascular development. Proc Natl Acad Sci USA 1997; 94: 4273-4278.
3. O'Rourke JF, Tian YM, Ratcliffe PJ, Pugh CW. Oxygen-regulated and transactivating domains in endothelial PAS protein 1: comparison with hypoxia-inducible factor-1α. J Biol Chem 1999; 274: 2060-2071.
4. Makino Y, Cao R, Svensson K, et al. Inhibitory PAS domain protein is a negative regulator of hypoxia-inducible gene expression. Nature 2001; 414: 550-554.
5. Fandrey J, Gorr TA, Gassmann M. Regulating cellular oxygen sensing by hydroxylation. Cardiovasc Res 2006; 71: 642-651.
6. Schofield CJ, Ratcliffe PJ. Signalling hypoxia by HIF hydroxylases. Biochem Biophys Res Commun 2005; 338: 617-626.
7. Berra E, Ginouvès A, Pouysségur J. The hypoxia-inducible- factor hydroxylases bring fresh air into hypoxia signalling. EMBO Rep 2006; 7: 41-45.
8. Wenger RH, Stiehl DP, Camenisch G. Integration of oxygen signaling at the consensus HRE. Sci STKE 2005; 2005: re12.
9. Ruas JL, Poellinger L. Hypoxia-dependent activation of HIF into a transcriptional regulator. Semin Cell Dev Biol 2005; 16: 514-522.
10. Lando D, Peet DJ, Whelan DA, Gorman JJ, Whitelaw ML. Asparagine hydroxylation of the HIF transactivation domain a hypoxic switch. Science 2002; 295: 858-861.
11. Kallio PJ, Okamoto K, O'Brien S, et al. Signal transduction in hypoxic cells: inducible nuclear translocation and recruitment of the CBP/p300 coactivator by the hypoxia-inducible factor-1α. EMBO J 1998; 17: 6573-6586.
12. Stroka DM, Burkhardt T, Desbaillets I, et al. HIF-1 is expressed in normoxic tissue and displays an organ-specific regulation under systemic hypoxia. FASEB J 2001; 15: 2445-2453.
13. Acker H, Berchner-Pfannschmidt U, Wotzlaw C, Huckstorf C, Streller T. Optical analysis of the oxygen-sensing signal pathway. In: Lahiri S, Semenza GL, Prabhakar NR, eds. Oxygen Sensing: Responses and Adaptation to Hypoxia (Lung Biology in Health and Disease). New York, Marcel Dekker, Inc., 2003; pp. 519-533.
14. 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 1998; 275: L818-L826.
15. Wiesener MS, Jürgensen JS, Rosenberger C, et al. Widespread hypoxia-inducible expression of HIF-2α in distinct cell populations of different organs. FASEB J 2003; 17: 271-273.
16. Rosenberger C, Mandriota S, Jü rgensen JS, et al. Expression of hypoxia-inducible factor-1α and -2α in hypoxic and ischemic rat kidneys. J Am Soc Nephrol 2002; 13: 1721-1732.
17. Jü rgensen JS, Rosenberger C, Wiesener MS, et al. Persistent induction of HIF-1α and -2α in cardiomyocytes and stromal cells of ischemic myocardium. FASEB J 2004; 18: 1415-1417.
18. Bernhardt WM, Câmpean V, Kany S, et al. Preconditional activation of hypoxia-inducible factors ameliorates ischemic acute renal failure. J Am Soc Nephrol 2006; 17: 1970-1978.
19. Groenman FA, Rutter M, Wang J, Caniggia I, Tibboel D, Post M. Effect of chemical stabilizers of hypoxia-inducible factors on early lung development. Am J Physiol Lung Cell Mol Physiol 2007; 293: L557-L567.
20. Talks KL, Turley H, Gatter KC, et al. The expression and distribution of the hypoxia-inducible factors HIF-1α and HIF-2α in normal human tissues, cancers, and tumor-associated macrophages. Am J Pathol 2000; 157: 411-421.
21. Zhong H, De Marzo AM, Laughner E, et al. Overexpression of hypoxia-inducible factor 1α in common human cancers and their metastases. Cancer Res 1999; 59: 5830-5835.
22. Zagzag D, Zhong H, Scalzitti JM, Laughner E, Simons JW, Semenza GL. Expression of hypoxia-inducible factor 1α in brain tumors: association with angiogenesis, invasion, and progression. Cancer 2000; 88: 2606-2618.
23. Bos R, Zhong H, Hanrahan CF, et al. Levels of hypoxia-inducible factor-1α during breast carcinogenesis. J Natl Cancer Inst 2001; 93: 309-314.
24. Serganova I, Doubrovin M, Vider J, et al. Molecular imaging of temporal dynamics and spatial heterogeneity of hypoxia-inducible factor-1 signal transduction activity in tumors in living mice. Cancer Res 2004; 64: 6101-6108.
25. Liu J, Qu R, Ogura M, Shibata T, Harada H, Hiraoka M. Real-time imaging of hypoxia-inducible factor-1 activity in tumor xenografts. J Radiat Res (Tokyo) 2005; 46: 93-102.
26. Indovina P, Collini M, Chirico G, Santini MT. Three-dimensional cell organization leads to almost immediate HRE activity as demonstrated by molecular imaging of MG-63 spheroids using two-photon excitation microscopy. FEBS Lett 2007; 581: 719-726.
27. Blasberg R. Imaging gene expression and endogenous molecular processes: molecular imaging. J Cereb Blood Flow Metab 2002; 22: 1157-1164.
28. Wartenberg M, Ling FC, Mü schen M, et al. Regulation of the multidrug resistance transporter P-glycoprotein in multicellular tumor spheroids by hypoxia-inducible factor (HIF-1) and reactive oxygen species. FASEB J 2003; 17: 503-505.
29. Görlach A, Diebold I, Schini-Kerth VB, et al. Thrombin activates the hypoxia-inducible factor-1 signaling pathway in vascular smooth muscle cells: role of the p22(phox)-containing NADPH oxidase. Circ Res 2001; 89: 47-54.
30. Stolze I, Berchner-Pfannschmidt U, Freitag P, et al. Hypoxia-inducible erythropoietin gene expression in human neuroblastoma cells. Blood 2002; 100: 2623-2628.
31. Liu Q, Berchner-Pfannschmidt U, Möller U, et al. A Fenton reaction at the endoplasmic reticulum is involved in the redox control of hypoxia-inducible gene expression. Proc Natl Acad Sci USA 2004; 101: 4302-4307.
32. Frede S, Freitag P, Otto T, Heilmaier C, Fandrey J. The proinflammatory cytokine interleukin 1β and hypoxia cooperatively induce the expression of adrenomedullin in ovarian carcinoma cells through hypoxia inducible factor 1 activation. Cancer Res 2005; 65: 4690-4697.
33. Berchner-Pfannschmidt U, Petrat F, Doege K, et al. Chelation of cellular calcium modulates hypoxia-inducible gene expression through activation of hypoxia-inducible factor-1α. J Biol Chem 2004; 279: 44976-44986.
34. Berchner-Pfannschmidt U, Yamac H, Trinidad B, Fandrey J. Nitric oxide modulates oxygen sensing by hypoxia-inducible factor 1-dependent induction of prolyl hydroxylase 2. J Biol Chem 2007; 282: 1788-1796.
35. Groulx I, Lee S. Oxygen-dependent ubiquitination and degradation of hypoxia-inducible factor requires nuclear-cytoplasmic trafficking of the von Hippel-Lindau tumor suppressor protein. Mol Cell Biol 2002; 22: 5319-5336.
36. Chilov D, Camenisch G, Kvietikova I, Ziegler U, Gassmann M, Wenger RH. Induction and nuclear translocation of hypoxia-inducible factor-1 (HIF-1): heterodimerization with ARNT is not necessary for nuclear accumulation of HIF-1α. J Cell Sci 1999; 112: 1203-1212.
37. 2-driven proteasomal degradation irrespective of its subcellular localization: nucleus or cytoplasm. EMBO Rep 2001; 2: 615-620.
38. Lee S, Chen DY, Humphrey JS, Gnarra JR, Linehan WM, Klausner RD. Nuclear/cytoplasmic localization of the von Hippel-Lindau tumor suppressor gene product is determined by cell density. Proc Natl Acad Sci USA 1996; 93: 1770-1775.
39. Wójcik C, DeMartino GN. Intracellular localization of proteasomes. Int J Biochem Cell Biol 2003; 35: 579-589.
40. Karhausen J, Kong T, Narravula S, Colgan SP. Induction of the von Hippel-Lindau tumor suppressor gene by late hypoxia limits HIF-1 expression. J Cell Biochem 2005; 95: 1264-1275.
41. Metzen E, Berchner-Pfannschmidt U, Stengel P, et al. Intracellular localisation of human HIF-1α hydroxylases: implications for oxygen sensing. J Cell Sci 2003; 116: 1319-1326.
42. Soilleux EJ, Turley H, Tian YM, Pugh CW, Gatter KC, Harris AL. Use of novel monoclonal antibodies to determine the expression and distribution of the hypoxia regulatory factors PHD-1, PHD-2, PHD-3 and FIH in normal and neoplastic human tissues. Histopathology 2005; 47: 602-610.
43. Jokilehto T, Rantanen K, Luukkaa M, et al. Overexpression and nuclear translocation of hypoxia-inducible factor prolyl hydroxylase PHD2 in head and neck squamous cell carcinoma is associated with tumor aggressiveness. Clin Cancer Res 2006; 12: 1080-1087.
44. Zheng X, Ruas JL, Cao R, et al. Cell-type-specific regulation of degradation of hypoxia-inducible factor 1α: role of subcellular compartmentalization. Mol Cell Biol 2006; 26: 4628-4641.
45. Mylonis I, Chachami G, Samiotaki M, et al. Identification of MAPK phosphorylation sites and their role in the localization and activity of hypoxia-inducible factor-1α. J Biol Chem 2006; 281: 33095-33106.
46. Salceda S, Beck I, Caro J. Absolute requirement of aryl hydrocarbon receptor nuclear translocator protein for gene activation by hypoxia. Arch Biochem Biophys 1996; 334: 389-394.
47. Berchner-Pfannschmidt U, Wotzlaw C, Merten E, Acker H, Fandrey J. Visualization of the three-dimensional organization of hypoxia-inducible factor-1α and interacting cofactors in subnuclear structures. Biol Chem 2004; 385: 231-237.
48. Wotzlaw C, Otto T, Berchner-Pfannschmidt U, Metzen E, Acker H, Fandrey J. Optical analysis of the HIF-1 complex in living cells by FRET and FRAP. FASEB J 2007; 21: 700-707.
49. Erbel PJ, Card PB, Karakuzu O, Bruick RK, Gardner KH. Structural basis for PAS domain heterodimerization in the basic helix-loop-helix-PAS transcription factor hypoxia-inducible factor. Proc Natl Acad Sci USA 2003; 100: 15504-15509.
50. Feige JN, Sage D, Wahli W, Desvergne B, Gelman L. PixFRET, an ImageJ plug-in for FRET calculation that can accommodate variations in spectral bleed-throughs. Microsc Res Tech 2005; 68: 51-58.
51. Ruas JL, Poellinger L, Pereira T. Functional analysis of hypoxia-inducible factor-1α-mediated transactivation. Identification of amino acid residues critical for transcriptional activation and/or interaction with CREB-binding protein. J Biol Chem 2002; 277: 38723-38730.
52. Ruas JL, Poellinger L, Pereira T. Role of CBP in regulating HIF-1-mediated activation of transcription. J Cell Sci 2005; 118: 301-311.
53. Stockmann C, Fandrey J. Hypoxia-induced erythropoietin production: a paradigm for oxygen-regulated gene expression. Clin Exp Pharmacol Physiol 2006; 33: 968-979.