Factor inhibiting HIF-1 (FIH-1) modulates protein interactions of apoptosis-stimulating p53 binding protein 2 (ASPP2)

Journal of Cell Science

Volumn 126, Issue 12, 2013, Pages 2629-2640

  Janke, Kirsten ^a   Brockmeier, Ulf ^a   Kuhlmann, Katja ^b   Eisenacher, Martin ^b   Nolde, Jan ^c   Meyer, Helmut E ^b   Mairbäurl, Heimo ^d   Metzen, Eric ^a  

^a UNIVERSITY OF DUISBURG ESSEN   (Germany)

^b RUHR UNIVERSITY BOCHUM   (Germany)

^c UNIVERSITY OF LÜBECK   (Germany)

^d UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

Author keywords

Cell polarity; Hydroxylation; Hypoxia; Protein interaction

Indexed keywords

APOPTOSIS STIMULATING P53 BINDING PROTEIN 2; ASPARAGINE; BINDING PROTEIN; DIOXYGENASE; FACTOR INHIBITING HIF 1; OXYGENASE INHIBITOR; PROTEIN; PROTEIN PAR 3; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; APOPTOSIS; ARTICLE; CANCER CELL; CELL ADHESION; CELL CONTACT; CELL FUNCTION; CELL HYPOXIA; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOSOL; HYDROXYLATION; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; MASS SPECTROMETRY; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE;

CELL POLARITY; HYDROXYLATION; HYPOXIA; PROTEIN INTERACTION;

AMINO ACID SEQUENCE; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CELL ADHESION; CELL CYCLE PROTEINS; CELL GROWTH PROCESSES; CELL HYPOXIA; CELL LINE; CELL LINE, TUMOR; CELL MOVEMENT; CELL POLARITY; CYTOSOL; HCT116 CELLS; HEK293 CELLS; HUMANS; HYDROXYLATION; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MIXED FUNCTION OXYGENASES; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN INTERACTION MAPS; PROTEIN STRUCTURE, TERTIARY; REPRESSOR PROTEINS; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84879862491     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.117564     Document Type: Article

References (48)

1. Acker, T. and Acker, H. (2004). Cellular oxygen sensing need in CNS function: physiological and pathological implications. J. Exp. Biol. 207, 3171-3188.
2. Aylon, Y., Ofir-Rosenfeld, Y., Yabuta, N., Lapi, E., Nojima, H., Lu, X. and Oren, M. (2010). The Lats2 tumor suppressor augments p53-mediated apoptosis by promoting the nuclear proapoptotic function of ASPP1. Genes Dev. 24, 2420-2429.
3. Bergamaschi, D., Samuels, Y., O'Neil, N. J., Trigiante, G., Crook, T., Hsieh, J. K., O'Connor, D. J., Zhong, S., Campargue, I., Tomlinson, M. L. et al. (2003). iASPP oncoprotein is a key inhibitor of p53 conserved from worm to human. Nat. Genet. 33, 162-167.
4. Brockmeier, U., Platzek, C., Schneider, K., Patak, P., Bernardini, A., Fandrey, J. and Metzen, E. (2011). The function of hypoxia-inducible factor (HIF) is independent of the endoplasmic reticulum protein OS-9. PLoS ONE 6, e19151.
5. Bunz, F., Dutriaux, A., Lengauer, C., Waldman, T., Zhou, S., Brown, J. P., Sedivy, J. M., Kinzler, K. W. and Vogelstein, B. (1998). Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science 282, 1497-1501.
6. Chikh, A., Matin, R. N., Senatore, V., Hufbauer, M., Lavery, D., Raimondi, C., Ostano, P., Mello-Grand, M., Ghimenti, C., Bahta, A. et al. (2011). iASPP/p63 autoregulatory feedback loop is required for the homeostasis of stratified epithelia. EMBO J. 30, 4261-4273.
7. Cockman, M. E., Lancaster, D. E., Stolze, I. P., Hewitson, K. S., McDonough, M. A., Coleman, M. L., Coles, C. H., Yu, X., Hay, R. T., Ley, S. C. et al. (2006). 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.
8. Cockman, M. E., Webb, J. D. and Ratcliffe, P. J. (2009). FIH-dependent asparaginyl hydroxylation of ankyrin repeat domain-containing proteins. Ann. New York Acad. Sci. 1177, 9-18.
9. Coleman, M. L. and Ratcliffe, P. J. (2009). Signalling cross talk of the HIF system: involvement of the FIH protein. Curr. Pharm. Des. 15, 3904-3907.
10. Coleman, M. L., McDonough, M. A., Hewitson, K. S., Coles, C., Mecinovic, J., Edelmann, M., Cook, K. M., Cockman, M. E., Lancaster, D. E., Kessler, B. M. et al. (2007). Asparaginyl hydroxylation of the Notch ankyrin repeat domain by factor inhibiting hypoxia-inducible factor. J. Biol. Chem. 282, 24027-24038.
11. Cong, W., Hirose, T., Harita, Y., Yamashita, A., Mizuno, K., Hirano, H. and Ohno, S. (2010). ASPP2 regulates epithelial cell polarity through the PAR complex. Curr. Biol. 20, 1408-1414.
12. Cummins, E. P., Berra, E., Comerford, K. M., Ginouves, A., Fitzgerald, K. T., Seeballuck, F., Godson, C., Nielsen, J. E., Moynagh, P., Pouyssegur, J. et al. (2006). Prolyl hydroxylase-1 negatively regulates IkappaB kinase-beta, giving insight into hypoxia-induced NFkappaB activity. Proc. Natl. Acad. Sci. USA 103, 18154- 18159.
13. Dames, S. A., Martinez-Yamout, M., De Guzman, R. N., Dyson, H. J. and Wright, P. E. (2002). Structural basis for Hif-1 alpha/CBP recognition in the cellular hypoxic response. Proc. Natl. Acad. Sci. USA 99, 5271-5276.
14. Devries, I. L., Hampton-Smith, R. J., Mulvihill, M. M., Alverdi, V., Peet, D. J. and Komives, E. A. (2010). Consequences of IkappaB alpha hydroxylation by the factor inhibiting HIF (FIH). FEBS Lett. 584, 4725-4730.
15. Elkins, J. M., Hewitson, K. S., McNeill, L. A., Seibel, J. F., Schlemminger, I., Pugh, C. W., Ratcliffe, P. J. and Schofield, C. J. (2003). Structure of factor-inhibiting hypoxia-inducible factor (HIF) reveals mechanism of oxidative modification of HIF-1 alpha. J. Biol. Chem. 278, 1802-1806.
16. Hardy, A. P., Prokes, I., Kelly, L., Campbell, I. D. and Schofield, C. J. (2009). Asparaginyl beta-hydroxylation of proteins containing ankyrin repeat domains influences their stability and function. J. Mol. Biol. 392, 994-1006.
17. Hewitson, K. S., McNeill, L. A., Riordan, M. V., Tian, Y. M., Bullock, A. N., Welford, R. W., Elkins, J. M., Oldham, N. J., Bhattacharya, S., Gleadle, J. M. et al. (2002). Hypoxia-inducible factor (HIF) asparagine hydroxylase is identical to factor inhibiting HIF (FIH) and is related to the cupin structural family. J. Biol. Chem. 277, 26351-26355.
18. Ho, S. N., Hunt, H. D., Horton, R. M., Pullen, J. K. and Pease, L. R. (1989). Sitedirected mutagenesis by overlap extension using the polymerase chain reaction. Gene 77, 51-59.
19. Kaelin, W. G., Jr and Ratcliffe, P. J. (2008). Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol. Cell 30, 393-402.
20. Kelly, L., McDonough, M. A., Coleman, M. L., Ratcliffe, P. J. and Schofield, C. J. (2009). Asparagine beta-hydroxylation stabilizes the ankyrin repeat domain fold. Mol. Biosyst. 5, 52-58.
21. Khan, M. N., Bhattacharyya, T., Andrikopoulos, P., Esteban, M. A., Barod, R., Connor, T., Ashcroft, M., Maxwell, P. H. and Kiriakidis, S. (2011). Factor inhibiting HIF (FIH-1) promotes renal cancer cell survival by protecting cells from HIF-1a-mediated apoptosis. Br. J. Cancer 104, 1151-1159.
22. Köditz, J., Nesper, J., Wottawa, M., Stiehl, D. P., Camenisch, G., Franke, C., Myllyharju, J., Wenger, R. H. and Katschinski, D. M. (2007). Oxygen-dependent ATF-4 stability is mediated by the PHD3 oxygen sensor. Blood 110, 3610-3617.
23. Kohl, A., Binz, H. K., Forrer, P., Stumpp, M. T., Plückthun, A. and Grü tter, M. G. (2003). Designed to be stable: crystal structure of a consensus ankyrin repeat protein. Proc. Natl. Acad. Sci. USA 100, 1700-1705.
24. Koivunen, P., Hirsila , M., Gü nzler, V., Kivirikko, K. I. and Myllyharju, J. (2004). Catalytic properties of the asparaginyl hydroxylase (FIH) in the oxygen sensing pathway are distinct from those of its prolyl 4-hydroxylases. J. Biol. Chem. 279, 9899- 9904.
25. Kuzmanov, A., Wielockx, B., Rezaei, M., Kettelhake, A. and Breier, G. (2011). Overexpression of factor inhibiting HIF-1 enhances vessel maturation and tumor growth via platelet-derived growth factor-C. Int. J. Cancer 131, E603-E613.
26. Lando, D., Peet, D. J., Gorman, J. J., Whelan, D. A., Whitelaw, M. L. and Bruick, R. K. (2002a). FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor. Genes Dev. 16, 1466-1471.
27. Lando, D., Peet, D. J., Gorman, J. J., Whelan, D. A., Whitelaw, M. L. and Bruick, R. K. (2002b). FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor. Genes Dev. 16, 1466-1471.
28. Linke, S., Stojkoski, C., Kewley, R. J., Booker, G. W., Whitelaw, M. L. and Peet, D. J. (2004). Substrate requirements of the oxygen-sensing asparaginyl hydroxylase factor-inhibiting hypoxia-inducible factor. J. Biol. Chem. 279, 14391-14397.
29. Lochhead, J. J., McCaffrey, G., Quigley, C. E., Finch, J., DeMarco, K. M., Nametz, N. and Davis, T. P. (2010). Oxidative stress increases blood-brain barrier permeability and induces alterations in occludin during hypoxia-reoxygenation. J. Cereb. Blood Flow Metab. 30, 1625-1636.
30. Mahon, P. C., Hirota, K. and Semenza, G. L. (2001). FIH-1: a novel protein that interacts with HIF-1alpha and VHL to mediate repression of HIF-1 transcriptional activity. Genes Dev. 15, 2675-2686.
31. Natah, S. S., Srinivasan, S., Pittman, Q., Zhao, Z. and Dunn, J. F. (2009). Effects of acute hypoxia and hyperthermia on the permeability of the blood-brain barrier in adult rats. J. Appl. Physiol. 107, 1348-1356.
32. Notari, M., Hu, Y., Koch, S., Lu, M., Ratnayaka, I., Zhong, S., Baer, C., Pagotto, A., Goldin, R., Salter, V. et al. (2011). Inhibitor of apoptosis-stimulating protein of p53 (iASPP) prevents senescence and is required for epithelial stratification. Proc. Natl. Acad. Sci. USA 108, 16645-16650.
33. Pelletier, J., Dayan, F., Durivault, J., Ilc, K., Pe'cou, E., Pouysse'gur, J. and Mazure, N. M. (2012). The asparaginyl hydroxylase factor-inhibiting HIF is essential for tumor growth through suppression of the p53-p21 axis. Oncogene 31, 2989-3001.
34. Pugh, C. W., O'Rourke, J. F., Nagao, M., Gleadle, J. M. and Ratcliffe, P. J. (1997). Activation of hypoxia-inducible factor-1; definition of regulatory domains within the alpha subunit. J. Biol. Chem. 272, 11205-11214.
35. Samuels-Lev, Y., O'Connor, D. J., Bergamaschi, D., Trigiante, G., Hsieh, J. K., Zhong, S., Campargue, I., Naumovski, L., Crook, T. and Lu, X. (2001). ASPP proteins specifically stimulate the apoptotic function of p53. Mol. Cell 8, 781-794.
36. Schofield, C. J. and Ratcliffe, P. J. (2004). Oxygen sensing by HIF hydroxylases. Nat. Rev. Mol. Cell Biol. 5, 343-354.
37. Semenza, G. L. (2012). Hypoxia-inducible factors in physiology and medicine. Cell 148, 399-408.
38. Singleton, R. S., Trudgian, D. C., Fischer, R., Kessler, B. M., Ratcliffe, P. J. and Cockman, M. E. (2011). Quantitative mass spectrometry reveals dynamics of factorinhibiting hypoxia-inducible factor-catalyzed hydroxylation. J. Biol. Chem. 286, 33784-33794.
39. Sottocornola, R., Royer, C., Vives, V., Tordella, L., Zhong, S., Wang, Y., Ratnayaka, I., Shipman, M., Cheung, A., Gaston-Massuet, C. et al. (2010). ASPP2 binds Par-3 and controls the polarity and proliferation of neural progenitors during CNS development. Dev. Cell 19, 126-137.
40. Trigiante, G. and Lu, X. (2006). ASPP [corrected] and cancer. Nat. Rev. Cancer 6, 217- 226.
41. Vigneron, A. M., Ludwig, R. L. and Vousden, K. H. (2010). Cytoplasmic ASPP1 inhibits apoptosis through the control of YAP. Genes Dev. 24, 2430-2439.
42. Wilkins, S. E., Hyvärinen, J., Chicher, J., Gorman, J. J., Peet, D. J., Bilton, R. L. and Koivunen, P. (2009). Differences in hydroxylation and binding of Notch and HIF-1alpha demonstrate substrate selectivity for factor inhibiting HIF-1 (FIH-1). Int. J. Biochem. Cell Biol. 41, 1563-1571.
43. Wilkins, S. E., Karttunen, S., Hampton-Smith, R. J., Murchland, I., Chapman- Smith, A. and Peet, D. J. (2012). Factor inhibiting HIF (FIH) recognizes distinct molecular features within hypoxia-inducible factor-a (HIF-a) versus ankyrin repeat substrates. J. Biol. Chem. 287, 8769-8781.
44. Yang, M., Chowdhury, R., Ge, W., Hamed, R. B., McDonough, M. A., Claridge, T. D., Kessler, B. M., Cockman, M. E., Ratcliffe, P. J. and Schofield, C. J. (2011a). Factor-inhibiting hypoxia-inducible factor (FIH) catalyses the posttranslational hydroxylation of histidinyl residues within ankyrin repeat domains. FEBS J. 278, 1086-1097.
45. Yang, M., Ge, W., Chowdhury, R., Claridge, T. D., Kramer, H. B., Schmierer, B., McDonough, M. A., Gong, L., Kessler, B. M., Ratcliffe, P. J. et al. (2011b). Asparagine and aspartate hydroxylation of the cytoskeletal ankyrin family is catalyzed by factor-inhibiting hypoxia-inducible factor. J. Biol. Chem. 286, 7648- 7660.
46. Zhang, N., Fu, Z., Linke, S., Chicher, J., Gorman, J. J., Visk, D., Haddad, G. G., Poellinger, L., Peet, D. J., Powell, F. et al. (2010). The asparaginyl hydroxylase factor inhibiting HIF-1alpha is an essential regulator of metabolism. Cell Metab. 11, 364-378.
47. Zheng, X., Linke, S., Dias, J. M., Zheng, X., Gradin, K., Wallis, T. P., Hamilton, B. R., Gustafsson, M., Ruas, J. L., Wilkins, S. et al. (2008). Interaction with factor inhibiting HIF-1 defines an additional mode of cross-coupling between the Notch and hypoxia signaling pathways. Proc. Natl. Acad. Sci. USA 105, 3368-3373.
48. Zhou, J., Schmid, T., Schnitzer, S. and Brü ne, B. (2006). Tumor hypoxia and cancer progression. Cancer Lett. 237, 10-21.