Significance of prolyl hydroxylase 2 in the interference of aryl hydrocarbon receptor and hypoxia-inducible factor-1α signaling

Chemical Research in Toxicology

Volumn 21, Issue 2, 2008, Pages 341-348

  Seifert, Anja ^a   Katschinski, Dörthe M ^b   Tonack, Sarah ^a   Fischer, Bernd ^a   Santos, Anne Navarrete ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; AROMATIC HYDROCARBON RECEPTOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; ALPHA NAPHTHOFLAVONE; ALPHA-NAPHTHOFLAVONE; BENZOFLAVONE DERIVATIVE; EGLN1 PROTEIN, HUMAN; HIF1A PROTEIN, HUMAN; MESSENGER RNA; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; HYPOXIA; NUCLEOTIDE SEQUENCE; PROMOTER REGION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; BREAST TUMOR; CELL HYPOXIA; DOWN REGULATION; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; LIVER CELL; LIVER CELL CARCINOMA; LIVER TUMOR; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE;

BENZOFLAVONES; BREAST NEOPLASMS; CARCINOMA, HEPATOCELLULAR; CELL HYPOXIA; CELL LINE, TUMOR; DOWN-REGULATION; GENE EXPRESSION REGULATION; HEPATOCYTES; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LIVER NEOPLASMS; PROCOLLAGEN-PROLINE DIOXYGENASE; RECEPTORS, ARYL HYDROCARBON; RNA, MESSENGER; SIGNAL TRANSDUCTION; TETRACHLORODIBENZODIOXIN;

EID: 41649108038     PISSN: 0893228X     EISSN: None     Source Type: Journal    
DOI: 10.1021/tx7001838     Document Type: Article

References (58)

1. Kewley, R. J., Whitelaw, M. L., and Chapman-Smith, A. (2004) The mammalian basic helix-loop-helix/PAS family of transcriptional regulators. Int. J. Biochem. Cell Biol. 36, 189-204.
2. Hord, N. G., and Perdew, G. H. (1994) Physicochemical and immunocytochemical analysis of the aryl hydrocarbon receptor nuclear translocator: Characterization of two monoclonal antibodies to the aryl hydrocarbon receptor nuclear translocator. Mol. Pharmacol. 46, 618-626.
3. Antonsson, C., Arulampalam, V., Whitelaw, M. L., Pettersson, S., and Poellinger, L. (1995) Constitutive function of the basic helix-loop-helix/PAS factor Arnt. Regulation of target promoters via the E box motif. J. Biol. Chem. 270, 13968-13972.
4. Sogawa, K., Nakano, R., Kobayashi, A., Kikuchi, Y., Ohe, N., Matsushita, N., and Fujii-Kuriyama, Y. (1995) Possible function of Ah receptor nuclear translocator (Arnt) homodimer in transcriptional regulation. Proc. Natl. Acad. Sci. U.S.A. 92, 1936-1940.
5. Schmidt, J. V., and Bradfield, C. A. (1996) Ah receptor signaling pathways. Annu. Rev. Cell Dev. Biol. 12, 55-89.
6. Schrenk, D. (1998) Impact of dioxin-type induction of drug-metabolizing enzymes on the metabolism of endo- and xenobiotics. Biochem. Pharmacol. 55, 1155-1162.
7. Zhou, J., Schmid, T., Schnitzer, S., and Brune, B. (2006) Tumor hypoxia and cancer progression. Cancer Lett. 237, 10-21.
8. Lee, J. W., Bae, S. H., Jeong, J. W., Kim, S. H., and Kim, K. W. (2004) Hypoxia-inducible factor (HIF-1)alpha: Its protein stability and biological functions. Exp. Mol. Med. 36, 1-12.
9. Chapman-Smith, A., Lutwyche, J. K., and Whitelaw, M. L. (2004) Contribution of the Per/Arnt/Sim (PAS) domains to DNA binding by the basic helix-loop-helix PAS transcriptional regulators. J. Biol. Chem. 279, 5353-5362.
10. Goldberg, M. A., and Schneider, T. J. (1994) Similarities between the oxygen-sensing mechanisms regulating the expression of vascular endothelial growth factor and erythropoietin. J. Biol. Chem. 269, 4355-4359.
11. Semenza, G. L., and Wang, G. L. (1992) A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol. Cell. Biol. 12, 5447-5454.
12. Choi, K. S., Bae, M. K., Jeong, J. W., Moon, H. E., and Kim, K. W. (2003) Hypoxia-induced angiogenesis during carcinogenesis. J. Biochem. Mol. Biol. 36, 120-127.
13. Semenza, G. L. (2000) Hypoxia, clonal selection, and the role of HIF-1 in tumor progression. Crit. Rev. Biochem. Mol. Biol. 35, 71-103.
14. Stiehl, D. P., Jelkmann, W., Wenger, R. H., and Hellwig-Burgel, T. (2002) Normoxic induction of the hypoxia-inducible factor 1 alpha by insulin and interleukin-1beta involves the phosphatidylinositol 3-kinase pathway. FEBS Lett 512, 157-162.
15. Masson, N., Appelhoff, R. J., Tuckerman, J. R., Tian, Y. M., Demol, H., Puype, M., Vandekerckhove, J., Ratcliffe, P. J., and Pugh, C. W. (2004) The HIF prolyl hydroxylase PHD3 is a potential substrate of the TRiC chaperonin. FEBS Lett. 570, 166-170.
16. Jaakkola, P., Mole, D. R., Tian, Y. M., Wilson, M. I., Gielbert, J., Gaskell, S. J., Kriegsheim, A., Hebestreit, H. F., Mukherji, M., Schofield, C. J., Maxwell, P. H., Pugh, C. W., and Ratcliffe, P. J. (2001) Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292, 468-472.
17. Ivan, M., Kondo, K., Yang, H., Kim, W., Valiando, J., Ohh, M., Salic, A., Asara, J. M., Lane, W. S., and Kaelin, W. G., Jr. (2001) HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: Implications for O2 sensing. Science 292, 464-468.
18. Yu, F., White, S. B., Zhao, Q., and Lee, F. S. (2001) HIF-1alpha binding to VHL is regulated by stimulus-sensitive proline hydroxylation. Proc. Natl. Acad. Sci. U.S.A. 98, 9630-9635.
19. Maxwell, P. H., Wiesener, M. S., Chang, G. W., Clifford, S. C., Vaux, E. C., Cockman, M. E., Wykoff, C. C., Pugh, C. W., Maher, E. R., and Ratcliffe, P. J. (1999) The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399, 271-275.
20. Kallio, P. J., Wilson, W. J., O'Brien, S., Makino, Y., and Poellinger, L. (1999) Regulation of the hypoxia-inducible transcription factor lalpha by the ubiquitin-proteasome pathway. J. Biol. Chem. 274, 6519-6525.
21. Salceda, S., and Caro, J. (1997) Hypoxia-inducible factor 1alpha (HIF-1alpha) protein is rapidly degraded by the ubiquitin-proteasome system under normoxic conditions. Its stabilization by hypoxia depends on redox-induced changes. J. Biol. Chem. 272, 22642-22647.
22. Cockman, M. E., Masson, N., Mole, D. R., Jaakkola, P., Chang, G. W., Clifford, S. C., Maher, E. R., Pugh, C. W., Ratcliffe, P. J., and Maxwell, P. H. (2000) Hypoxia inducible factor-alpha binding and ubiquitylation by the von Hippel-Lindau tumor suppressor protein. J. Biol. Chem. 275, 25733-25741.
23. Tanimoto, K., Makino, Y., Pereira, T., and Poellinger, L. (2000) Mechanism of regulation of the hypoxia-inducible factor-1 alpha by the von Hippel-Lindau tumor suppressor protein. EMBO J. 19, 4298-4309.
24. Bruick, R. K. (2003) Oxygen sensing in the hypoxic response pathway: Regulation of the hypoxia-inducible transcription factor. Genes Dev. 17, 2614-2623.
25. Appelhoff, R. J., Tian, Y. M., Raval, R. R., Turley, H., Harris, A. L., Pugh, C. W., Ratcliffe, P. J., and Gleadle, J. M. (2004) Differential function of the prolyl hydroxylases PHD1, PHD2, and PHD3 in the regulation of hypoxia-inducible factor. J. Biol. Chem. 279, 38458-38465.
26. Huang, J., Zhao, Q., Mooney, S. M., and Lee, F. S. (2002) Sequence determinants in hypoxia-inducible factor-1alpha for hydroxylation by the prolyl hydroxylases PHD1, PHD2, and PHD3. J. Biol. Chem. 277, 39792-39800.
27. Hirsila, M., Koivunen, P., Gunzler, V., Kivirikko, K. I., and Myllyharju, J. (2003) Characterization of the human prolyl 4-hydroxylases that modify the hypoxia-inducible factor. J. Biol. Chem. 278, 30772-30780.
28. Berra, E., Benizri, E., Ginouves, A., Volmat, V., Roux, D., and Pouyssegur, J. (2003) HIF prolyl-hydroxylase 2 is the key oxygen sensor setting low steady-state levels of HIF-1alpha in normoxia. EMBO J. 22, 4082-4090.
29. Marxsen, J. H., Stengel, P., Doege, K., Heikkinen, P., Jokilehto, T., Wagner, T., Jelkmann, W., Jaakkola, P., and Metzen, E. (2004) Hypoxia-inducible factor-1 (HIF-1) promotes its degradation by induction of HIF-alpha-prolyl-4- hydroxylases. Biochem. J. 381, 761-767.
30. Aprelikova, O., Chandramouli, G. V., Wood, M., Vasselli, J. R., Riss, J., Maranchie, J. K., Linehan, W. M., and Barrett, J. C. (2004) Regulation of HIF prolyl hydroxylases by hypoxia-inducible factors. J. Cell. Biochem. 92, 491-501.
31. D'Angelo, G., Duplan, E., Boyer, N., Vigne, P., and Frelin, C. (2003) Hypoxia up-regulates prolyl hydroxylase activity: A feedback mechanism that limits HIF-1 responses during reoxygenation. J. Biol. Chem. 278, 38183-38187.
32. Hofer, T., Pohjanvirta, R., Spielmann, P., Viluksela, M., Buchmann, D. P., Wenger, R. H., and Gassmann, M. (2004) Simultaneous exposure of rats to dioxin and carbon monoxide reduces the xenobiotic but not the hypoxic response. Biol. Chem. 385, 291-294.
33. Pollenz, R. S., Davarinos, N. A., and Shearer, T. P. (1999) Analysis of aryl hydrocarbon receptor-mediated signaling during physiological hypoxia reveals lack of competition for the aryl hydrocarbon nuclear translocator transcription factor. Mol. Pharmacol. 56, 1127-1137.
34. Ishimura, R., Ohsako, S., Kawakami, T., Sakaue, M., Aoki, Y., and Tohyama, C. (2002) Altered protein profile and possible hypoxia in the placenta of 2,3,7,8-tetrachlorodibenzo-p-dioxin-exposed rats. Toxicol. Appl. Pharmacol. 185, 197-206.
35. Thackaberry, E. A., Gabaldon, D. M., Walker, M. K., and Smith, S. M. (2002) Aryl hydrocarbon receptor null mice develop cardiac hypertrophy and increased hypoxia-inducible factor-1alpha in the absence of cardiac hypoxia. Cardiovasc. Toxicol. 2, 263-274.
36. Davidson, T., Salnikow, K., and Costa, M. (2003) Hypoxia inducible factor-1 alpha-independent suppression of aryl hydrocarbon receptor-regulated genes by nickel. Mol. Pharmacol. 64, 1485-1493.
37. Kim, J. E., and Sheen, Y. Y. (2000) Nitric oxide inhibits dioxin action for the stimulation of Cyp1a1 promoter activity. Biol. Pharm. Bull. 23, 575-580.
38. Park, H. (1999) Aromatic hydrocarbon nuclear translocator as a common component for the hypoxia- and dioxin-induced gene expression. Mol. Cells 9, 172-178.
39. Chan, W. K., Yao, G., Gu, Y. Z., and Bradfield, C. A. (1999) Cross-talk between the aryl hydrocarbon receptor and hypoxia inducible factor signaling pathways. Demonstration of competition and compensation. J. Biol. Chem. 274, 12115-12123.
40. Nie, M., Blankenship, A. L., and Giesy, J. P. (2001) Interactions between aryl hydrocarbon receptor (AhR) and hypoxia signaling pathways. Environ. Toxicol. Pharmacol. 10, 17-27.
41. Gradin, K., McGuire, J., Wenger, R. H., Kvietikova, I., Fhitelaw, M. L., Toftgard, R., Tora, L., Gassmann, M., and Poellinger, L. (1996) Functional interference between hypoxia and dioxin signal transduction pathways: Ccompetition for recruitment of the Arnt transcription factor. Mol. Cell. Biol. 16, 5221-5231.
42. Tomita, S., Sinai, C. J., Yim, S. H., and Gonzalez, F. J. (2000) Conditional disruption of the aryl hydrocarbon receptor nuclear translocator (Arnt) gene leads to loss of target gene induction by the aryl hydrocarbon receptor and hypoxia-inducible factor 1alpha. Mol. Endocrinol. 14, 1674-1681.
43. Chomczynski, P., and Sacchi, N. (1987) Single-step method of RNA isolation by acid guanidiniumthiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159.
44. Pfaffl, M. W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45.
45. Tonack, S., Kind, K., Thompson, J. G., Wobus, A. M., Fischer, B., and Santos, A. N. (2007) Dioxin affects glucose transport via the arylhydrocarbon receptor signal cascade in pluripotent embryonic carcinoma cells. Endocrinology [Online early access]. DOI: 10.1210/en.2007-0254. Published Online: Sep 13, 2007. http://endo.endojournals.org/cgi/content/short/en.2007- 0254v1.
46. Martin, F., Linden, T., Katschinski, D. M., Oehme, F., Flamme, I., Mukhopadhyay, C. K., Eckhardt, K., Troger, J., Barth, S., Camenisch, G., and Wenger, R. H. (2005) Copper-dependent activation of hypoxia-inducible factor (HIF)-1: Implications for ceruloplasmin regulation. Blood 105, 4613-4619.
47. Metzen, E., Stiehl, D. P., Doege, K., Marxsen, J. H., Hellwig-Burgel, T., and Jelkmann, W. (2005) Regulation of the prolyl hydroxylase domain protein 2 (phd2/egln-1) gene: Identification of a functional hypoxia-responsive element. Biochem. J. 387, 711-717.
48. Graham, F. L., and van der Eb, A. J. (1973) A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology 52, 456-467.
49. Parker, B. A., and Stark, G. R. (1979) Regulation of simian virus 40 transcription: Sensitive analysis of the RNA species present early in infections by virus or viral DNA. J. Virol. 31, 360-369.
50. Mimura, J., and Fujii-Kuriyama, Y. (2003) Functional role of AhR in the expression of toxic effects by TCDD. Biochim. Biophys. Acta 1619, 263-268.
51. Vaupel, P., Briest, S., and Hockel, M. (2002) Hypoxia in breast cancer: pathogenesis, characterization and biological/therapeutic implications. Wien. Med. Wochenschr. 152, 334-342.
52. Tacchini, L., Dansi, P., Matteucci, E., and Desiderio, M. A. (2001) Hepatocyte growth factor signalling stimulates hypoxia inducible factor-1 (HIF-1) activity in HepG2 hepatoma cells. Carcinogenesis 22, 1363-1371.
53. Prasch, A. L., Andreasen, E. A., Peterson, R. E., and Heideman, W. (2004) Interactions between 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) and hypoxia signaling pathways in zebrafish: Hypoxia decreases responses to TCDD in zebrafish embryos. Toxicol. Sci. 78, 68-77.
54. Cummins, E. P., and Taylor, C. T. (2005) Hypoxia-responsive transcription factors. Pflugers Arch. 450, 363-371.
55. To, K. K., and Huang, L. E. (2005) Suppression of hypoxia-inducible factor lalpha (HIF-1alpha) transcriptional activity by the HIF prolyl hydroxylase EGLN1. J. Biol. Chem. 280, 38102-38107.
56. Stiehl, D. P., Wirthner, R., Koditz, J., Spielmann, P., Camenisch, G., and Wenger, R. H. (2006) Increased prolyl 4-hydroxylase domain proteins compensate for decreased oxygen levels. Evidence for an autoregulatory oxygen-sensing system. J. Biol. Chem. 281, 23482-23491.
57. Chandel, N. S., McClintock, D. S., Feliciano, C. E., Wood, T. M., Melendez, J. A., Rodriguez, A. M., and Schumacker, P. T. (2000) Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1alpha during hypoxia: a mechanism of O2 sensing. J. Biol. Chem. 275, 25130-25138.
58. Callapina, M., Zhou, J., Schmid, T., Kohl, R., and Brune, B. (2005) NO restores HIF-1alpha hydroxylation during hypoxia: Role of reactive oxygen species. Free Radical Biol. Med. 39, 925-936.