Four-and-a-half LIM domain proteins inhibit transactivation by hypoxia-inducible factor 1

Journal of Biological Chemistry

Volumn 287, Issue 9, 2012, Pages 6139-6149

  Hubbi, Maimon E ^a   Gilkes, Daniele M ^a   Baek, Jin H ^a   Semenza, Gregg L ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS; CANCER BIOLOGY; COACTIVATORS; FEED-BACK LOOP; FUNCTIONAL INTERACTION; HYPOXIA-INDUCIBLE FACTOR 1; LIM DOMAIN; MOLECULAR MECHANISM; NEGATIVE REGULATORS; TRANSACTIVATION; TRANSACTIVATION DOMAIN; TRANSCRIPTIONAL ACTIVITY; TRANSCRIPTIONAL REGULATION; TUMOR GROWTH;

TRANSCRIPTION FACTORS;

TUMORS;

FOUR AND A HALF LIM DOMAIN PROTEIN; FOUR AND A HALF LIM DOMAIN PROTEIN 1; FOUR AND A HALF LIM DOMAIN PROTEIN 2; FOUR AND A HALF LIM DOMAIN PROTEIN 3; HYPOXIA INDUCIBLE FACTOR 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; LIM PROTEIN; OXYGEN; PROTEIN P300; UNCLASSIFIED DRUG;

ARTICLE; CARCINOMA CELL; CELL HYPOXIA; CONTROLLED STUDY; FEEDBACK SYSTEM; HUMAN; HUMAN CELL; LIVER CELL CARCINOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; TRANSACTIVATION; TRANSCRIPTION REGULATION;

CARCINOMA, HEPATOCELLULAR; CELL HYPOXIA; FEEDBACK, PHYSIOLOGICAL; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HEK293 CELLS; HELA CELLS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KIDNEY NEOPLASMS; LIM DOMAIN PROTEINS; LIM-HOMEODOMAIN PROTEINS; MUSCLE PROTEINS; P300-CBP TRANSCRIPTION FACTORS; PROTEIN STRUCTURE, TERTIARY; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION; UTERINE CERVICAL NEOPLASMS;

EID: 84857496757     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.278630     Document Type: Article

References (53)

1. Kadrmas, J. L., and Beckerle, M. C. (2004) The LIM domain. From the cytoskeleton to the nucleus. Nat. Rev. Mol. Cell Biol. 5, 920-931
2. Johannessen, M., Møller, S., Hansen, T., Moens, U., and Van Ghelue, M. (2006) The multifunctional roles of the four-and-a-half-LIM only protein FHL2. Cell Mol. Life Sci. 63, 268-284 (Pubitemid 43202310)
3. Kleiber, K., Strebhardt, K., and Martin, B. T. (2007) The biological relevance of FHL2 in tumour cells and its role as a putative cancer target. Anticancer Res. 27, 55-61
4. Ding, L., Wang, Z., Yan, J., Yang, X., Liu, A., Qiu, W., Zhu, J., Han, J., Zhang, H., Lin, J., Cheng, L., Qin, X., Niu, C., Yuan, B., Wang, X., Zhu, C., Zhou, Y., Li, J., Song, H., Huang, C., and Ye, Q. (2009) Human four-anda- half LIM family members suppress tumor cell growth through a TGF- β-like signaling pathway. J. Clin. Invest. 119, 349-361
5. Cowling, B. S., McGrath, M. J., Nguyen, M. A., Cottle, D. L., Kee, A. J., Brown, S., Schessl, J., Zou, Y., Joya, J., Bönnemann, C. G., Hardeman, E. C., and Mitchell, C. A. (2008) Identification of FHL1 as a regulator of skeletal muscle mass. Implications for human myopathy. J. Cell Biol. 183, 1033-1048
6. Schessl, J., Zou, Y., McGrath, M. J., Cowling, B. S., Maiti, B., Chin, S. S., Sewry, C., Battini, R., Hu, Y., Cottle, D. L., Rosenblatt, M., Spruce, L., Ganguly, A., Kirschner, J., Judkins, A. R., Golden, J. A., Goebel, H. H., Muntoni, F., Flanigan, K. M., Mitchell, C. A., and Bönnemann, C. G. (2008) Proteomic identification of FHL1 as the protein mutated in human reducing body myopathy. J. Clin. Invest. 118, 904-912 (Pubitemid 351364598)
7. Sheikh, F., Raskin, A., Chu, P. H., Lange, S., Domenighetti, A. A., Zheng, M., Liang, X., Zhang, T., Yajima, T., Gu, Y., Dalton, N. D., Mahata, S. K., Dorn, G. W., 2nd, Heller-Brown, J., Peterson, K. L., Omens, J. H., Mc- Culloch, A. D., and Chen, J. (2008) An FHL1-containing complex within the cardiomyocyte sarcomere mediates hypertrophic biomechanical stress responses in mice. J. Clin. Invest. 118, 3870-3880
8. Kong, Y., Shelton, J. M., Rothermel, B., Li, X., Richardson, J. A., Bassel- Duby, R., and Williams, R. S. (2001) Cardiac-specific LIM protein FHL2 modifies the hypertrophic response to β-adrenergic stimulation. Circulation 103, 2731-2738 (Pubitemid 32538790)
9. Martin, B., Schneider, R., Janetzky, S., Waibler, Z., Pandur, P., Kühl, M., Behrens, J., von der Mark, K., Starzinski-Powitz, A., and Wixler, V. (2002) The LIM-only protein FHL2 interacts with β-catenin and promotes differentiation of mouse myoblasts. J. Cell Biol. 159, 113-122 (Pubitemid 35191523)
10. 2 tension. Proc. Natl. Acad. Sci. U.S.A. 92, 5510-5514
11. Semenza, G. L. (2009) Physiology (Bethesda) 24, 97-106
12. Semenza, G. L. (2003) Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer 3, 721-732
13. Patel, S. A., and Simon, M. C. (2008) Biology of hypoxia-inducible factor-2α in development and disease. Cell Death Differ. 15, 628-634 (Pubitemid 351405065)
14. Ebert, B. L., Firth, J. D., and Ratcliffe, P. J. (1995) Hypoxia and mitochondrial inhibitors regulate expression of glucose transporter-1 via distinct cis-acting sequences. J. Biol. Chem. 270, 29083-29089
15. Kim, J. W., Tchernyshyov, I., Semenza, G. L., and Dang, C. V. (2006) HIF-1-mediated expression of pyruvate dehydrogenase kinase. A metabolic switch required for cellular adaptation to hypoxia. Cell Metab. 3, 177-185
16. Forsythe, J. A., Jiang B. H., Iyer, N. V., Agani, F., Leung S. W., Koos, R. D., and Semenza, G. L. (1996) Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol. Cell Biol. 16, 4604-4613 (Pubitemid 26272112)
17. 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
18. Scortegagna, M., Ding, K., Oktay, Y., Gaur, A., Thurmond, F., Yan, L. J., Marck, B. T., Matsumoto, A. M., Shelton, J. M., Richardson, J. A., Bennett, M. J., and Garcia, J. A. (2003) Multiple organ pathology, metabolic abnormalities and impaired homeostasis of reactive oxygen species in Epas1-/-mice. Nat. Genet. 35, 331-340 (Pubitemid 37486916)
19. Melillo, G. (2007) Targeting hypoxia cell signaling for cancer therapy. Cancer Metastasis Rev. 26, 341-352
20. Zhong, H., De Marzo, A. M., Laughner, E., Lim, M., Hilton, D. A., Zagzag, D., Buechler, P., Isaacs, W. B., Semenza, G. L., and Simons, J. W. (1999) Overexpression of hypoxia-inducible factor 1α in common human cancers and their metastases. Cancer Res. 59, 5830-5835
21. Semenza, G. L. (2010) Defining the role of hypoxia-inducible factor 1 in cancer biology and therapeutics. Oncogene 29, 625-634
22. 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) HIFα targeted for VHL-mediated destruction by proline hydroxylation. Implications for O2sensing. Science 292, 464-468 (Pubitemid 32335941)
23. 2-regulated prolyl hydroxylation. Science 292, 468-472
24. Yu, F., White, S. B., Zhao, Q., and Lee, F. S. (2001) HIF-1α binding to VHL is regulated by stimulus-sensitive proline hydroxylation. Proc. Natl. Acad. Sci. U.S.A. 98, 9630-9635 (Pubitemid 32769354)
25. Baek, J. H., Mahon, P. C., Oh, J., Kelly, B., Krishnamachary, B., Pearson, M., Chan, D. A., Giaccia, A. J., and Semenza, G. L. (2005) OS-9 interacts with hypoxia-inducible factor 1α and prolyl hydroxylases to promote oxygen-dependent degradation of HIF-1α. Mol. Cell 17, 503-512 (Pubitemid 40269115)
26. Baek, J. H., Liu, Y. V., McDonald, K. R., Wesley, J. B., Hubbi, M. E., Byun, H., and Semenza, G. L. (2007) Spermidine/spermine-N1-acetyltransferase 2 is an essential component of the ubiquitin ligase complex that regulates hypoxia-inducible factor 1α. J. Biol. Chem. 282, 23572-23580 (Pubitemid 47311906)
27. Hubbi, M. E., Luo, W., Baek, J. H., and Semenza, G. L. (2011) MCM proteins are negative regulators of hypoxia-inducible factor 1. Mol. Cell 42, 700-712
28. Mahon, P. C., Hirota, K., and Semenza, G. L. (2001) FIH-1.Anovel protein that interacts with HIF-1α and VHL to mediate repression of HIF-1 transcriptional activity. Genes Dev. 15, 2675-2686 (Pubitemid 32988878)
29. Lando, D., Peet, D. J., Whelan, D. A., Gorman, J. J., and Whitelaw, M. L. (2002) Asparagine hydroxylation of the HIF transactivation domain a hypoxic switch. Science 295, 858-861 (Pubitemid 34118367)
30. Lando, D., Peet, D. J., Gorman, J. J., Whelan, D. A., Whitelaw, M. L., and Bruick, R. K. (2002) FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor. Genes Dev. 16, 1466-1471 (Pubitemid 34686328)
31. 2-independent and HSP90 inhibitor-induced degradation of HIF-1α. Mol. Cell 25, 207-217
32. Liu, Y. V., Hubbi, M. E., Pan, F., McDonald, K. R., Mansharamani, M., Cole, R. N., Liu, J. O., and Semenza, G. L. (2007) Calcineurin promotes hypoxia-inducible factor 1α expression by dephosphorylating RACK1 and blocking RACK1 dimerization. J. Biol. Chem. 282, 37064-37073
33. Baek, J. H., Liu, Y. V., McDonald, K. R., Wesley, J. B., Zhang, H., and Semenza, G. L. (2007) Spermidine/spermine N(1)-acetyltransferase-1 binds to hypoxia-inducible factor-1α (HIF-1α) and RACK1 and promotes ubiquitination and degradation of HIF-1α. J. Biol. Chem. 282, 33358-33366 (Pubitemid 350159504)
34. Amir, S., Wang, R., Simons, J. W., and Mabjeesh, N. J. (2009) SEPT9-v1 up-regulates hypoxia-inducible factor 1 by preventing its RACK1-mediated degradation. J. Biol. Chem. 284, 11142-11151
35. Koh, M. Y., Darnay, B. G., and Powis, G. (2008) Hypoxia-associated factor, a novel E3-ubiquitin ligase, binds and ubiquitinates hypoxia-inducible factor 1α, leading to its oxygen-independent degradation. Mol. Cell. Biol. 28, 7081-7095
36. Luo, W., Zhong, J., Chang, R., Hu, H., Pandey, A., and Semenza, G. L. (2010) Hsp70 and CHIP selectively mediate ubiquitination and degradation of hypoxia-inducible factor (HIF)-1α but not HIF-2α. J. Biol. Chem. 285, 3651-3663
37. Lee, J. S., Kim, Y., Kim, I. S., Kim, B., Choi, H. J., Lee, J. M., Shin, H. J., Kim, J. H., Kim, J. Y., Seo, S. B., Lee, H., Binda, O., Gozani, O., Semenza, G. L., Kim, M., Kim, K. I., Hwang, D., and Baek, S. H. (2010) Negative regulation of hypoxic responses via induced Reptin methylation. Mol. Cell 39, 71-85
38. Koh, M. Y., Lemos, R., Jr., Liu, X., and Powis, G. (2011) The hypoxia-associated factor switches cells from HIF-1α- to HIF-2α-dependent signaling promoting stem cell characteristics, aggressive tumor growth and invasion. Cancer Res. 71, 4015-4027
39. Bracken, C. P., Whitelaw, M. L., and Peet, D. J. (2005) Activity of hypoxia-inducible factor 2α is regulated by association with the NF-kappaB essential modulator. J. Biol. Chem. 280, 14240-14251 (Pubitemid 40517326)
40. Wong, C. C., Gilkes, D. M., Zhang, H., Chen, J., Wei, H., Chaturvedi, P., Fraley, S. I., Wong, C. M., Khoo, U. S., Ng, I. O., Wirtz, D., and Semenza, G. L. (2011) Hypoxia-inducible factor 1 is a master regulator of breast cancer metastatic niche formation. Proc. Natl. Acad. Sci. U.S.A. 108, 16369-16374
41. Luo, W., Hu, H., Chang, R., Zhong, J., Knabel, M., O'Meally, R., Cole, R. N., Pandey, A., and Semenza, G. L. (2011) Pyruvate kinase M2 is a PHD3- stimulated co-activator for hypoxia-inducible factor 1. Cell 145, 732-744
42. Semenza, G. L., Jiang, B. H., Leung, S. W., Passantino, R., Concordet, J. P., Maire, P., and Giallongo, A. (1996) Hypoxia response elements in the aldolase A, enolase 1, and lactate dehydrogenase A gene promoters contain essential binding sites for hypoxia-inducible factor 1. J. Biol. Chem. 271, 32529-32537
43. Dioum, E. M., Chen, R., Alexander, M. S., Zhang, Q., Hogg, R. T., Gerard, R. D., and Garcia, J. A. (2009) Regulation of hypoxia-inducible factor 2αsignaling by the stress-responsive deacetylase sirtuin 1. Science 324, 1289-1293
44. Kwapiszewska, G., Wygrecka, M., Marsh, L. M., Schmitt, S., Trösser, R., Wilhelm, J., Helmus, K., Eul, B., Zakrzewicz, A., Ghofrani, H. A., Schermuly, R. T., Bohle, R. M., Grimminger, F., Seeger, W., Eickelberg, O., Fink, L., and Weissmann, N. (2008) Fhl-1, a new key protein in pulmonary hypertension. Circulation 118, 1183-1194
45. Zhang, H., Qian, D. Z., Tan, Y. S., Lee, K., Gao, P., Ren, Y. R., Rey, S., Hammers, H., Chang, D., Pili, R., Dang, C. V., Liu, J. O., and Semenza, G. L. (2008) Digoxin and other cardiac glycosides inhibit HIF-1α synthesis and block tumor growth. Proc. Natl. Acad. Sci. U.S.A. 105, 19579-19586
46. Yang, Y., Hou, H., Haller, E. M., Nicosia, S. V., and Bai, W. (2005) Suppression of FOXO1 activity by FHL2 through SIRT1-mediated deacetylation. EMBO J. 24, 1021-1032 (Pubitemid 40470150)
47. Freedman, S. J., Sun, Z. Y., Poy, F., Kung, A. L., Livingston, D. M., Wagner, G., and Eck, M. J. (2002) Structural basis for recruitment of CBP/p300 by hypoxia-inducible factor 1 alpha. Proc. Natl. Acad. Sci. U.S.A. 99, 5367-5372 (Pubitemid 34411554)
48. Wei, Y., Renard, C. A., Labalette, C., Wu, Y., Lévy, L., Neuveut, C., Prieur, X., Flajolet, M., Prigent, S., and Buendia, M. A. (2003) Identification of the LIM protein FHL2 as a co-activator of β-catenin. J. Biol. Chem. 278, 5188-5194 (Pubitemid 36801031)
49. Labalette, C., Renard, C. A., Neuveut, C., Buendia, M. A., and Wei, Y. (2004) Interaction and functional cooperation between the LIM protein FHL2, CBP/p300, and β-catenin. Mol. Cell Biol. 24, 10689-10702 (Pubitemid 39603127)
50. Bhattacharya, S., Michels, C. L., Leung, M. K., Arany, Z. P., Kung, A. L., and Livingston, D. M. (1999) Functional role of p35srj, a novel p300/CBP binding protein, during transactivation by HIF-1. Genes Dev. 13, 64-75 (Pubitemid 29045116)
51. Bamforth, S. D., Bragança, J., Eloranta, J. J., Murdoch, J. N., Marques, F. I., Kranc, K. R., Farza, H., Henderson, D. J., Hurst, H. C., and Bhattacharya, S. (2001) Cardiac malformations, adrenal agenesis, neural crest defects and exencephaly in mice lacking Cited2, a new Tfap2 co-activator. Nat. Genet. 29, 469-474 (Pubitemid 34326700)
52. Yin, Z., Haynie, J., Yang, X., Han, B., Kiatchoosakun, S., Restivo, J., Yuan, S., Prabhakar, N. R., Herrup, K., Conlon, R. A., Hoit, B. D., Watanabe, M., and Yang, Y. C. (2002) The essential role of Cited2, a negative regulator for HIF-1α, in heart development and neurulation. Proc. Natl. Acad. Sci. U.S.A. 99, 10488-10493
53. Xu, B., Doughman, Y., Turakhia, M., Jiang, W., Landsettle, C. E., Agani, F. H., Semenza, G. L., Watanabe, M., and Yang, Y. C. (2007) Partial rescue of defects in Cited2-deficient embryos by HIF-1α heterozygosity. Dev. Biol. 301, 130-140 (Pubitemid 46001381)