Inhibition of the HIF1α-p300 interaction by quinone- and indandione-mediated ejection of structural Zn(II)

European Journal of Medicinal Chemistry

Volumn 94, Issue , 2015, Pages 509-516

  Jayatunga, Madura K P ^a   Thompson, Sam ^a   McKee, Tawnya C ^b   Chan, Mun Chiang ^a   Reece, Kelie M ^c   Hardy, Adam P ^a   Sekirnik, Rok ^a   Seden, Peter T ^a   Cook, Kristina M ^c   McMahon, James B ^b   Figg, William D ^c   Schofield, Christopher J ^a   Hamilton, Andrew D ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b Nanobiology Program   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Electrophile; HIF; Hypoxia; p300 CBP; Quinone; Zinc ejection

Indexed keywords

E1A ASSOCIATED P300 PROTEIN; EP300 PROTEIN, HUMAN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INDAN DERIVATIVE; ORGANOMETALLIC COMPOUND; PROTEIN BINDING; QUINONE DERIVATIVE; ZINC;

CHEMICAL STRUCTURE; CHEMISTRY; DOSE RESPONSE; DRUG EFFECTS; HUMAN; METABOLISM; STRUCTURE ACTIVITY RELATION; SYNTHESIS;

DOSE-RESPONSE RELATIONSHIP, DRUG; E1A-ASSOCIATED P300 PROTEIN; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INDANS; MODELS, MOLECULAR; MOLECULAR STRUCTURE; ORGANOMETALLIC COMPOUNDS; PROTEIN BINDING; QUINONES; STRUCTURE-ACTIVITY RELATIONSHIP; ZINC;

EID: 84964908548     PISSN: 02235234     EISSN: 17683254     Source Type: Journal    
DOI: 10.1016/j.ejmech.2014.06.006     Document Type: Article

References (64)

1. Gillies, R.J., Gatenby, R.A., Hypoxia and adaptive landscapes in the evolution of carcinogenesis. Cancer Metastasis Rev. 26 (2007), 311–317.
2. 2 homeostasis by hypoxia-inducible factor 1α. Genes. Dev. 12 (1998), 149–162.
3. Rofstad, E.K., Danielsen, T., Hypoxia-induced angiogenesis and vascular endothelial growth factor secretion in human melanoma. Br. J. Cancer 77 (1998), 897–902.
4. Young, S.D., Marshall, R.S., Hill, R.P., Hypoxia induces DNA overreplication and enhances metastatic potential of murine tumor cells. Proc. Natl. Acad. Sci. U. S. A. 85 (1988), 9533–9537.
5. 2 tension. Proc. Natl. Acad. Sci. U. S. A. 92 (1995), 5510–5514.
6. Baba, Y., Nosho, K., Shima, K., Irahara, N., Chan, A.T., Meyerhardt, J.A., et al. HIF-1α overexpression is associated with poor prognosis in a cohort of 731 colorectal cancers. Am. J. Pathol. 176 (2010), 2292–2301.
7. Akakura, N., Kobayashi, M., Horiuchi, I., Suzuki, A., Wang, J., Chen, J., et al. Constitutive expression of hypoxia-inducible factor-1α renders pancreatic cancer cells resistant to apoptosis induced by hypoxia and nutrient deprivation. Cancer Res. 61 (2001), 6548–6554.
8. Zhong, H., Marzo, A.M.D., Laughner, E., Lim, M., Hilton, D.A., Zagzag, D., et al. Overexpression of hypoxia-inducible factor-1α in common human cancers and their metastases. Cancer Res. 59 (1999), 5830–5835.
9. Arany, Z., Huang, L.E., Eckner, R., Bhattacharya, S., Jiang, C., Goldberg, M.A., et al. An essential role for p300/CBP in the cellular response to hypoxia. Proc. Natl. Acad. Sci. U. S. A. 93 (1996), 12969–12973.
10. Jiang, B.H., Rue, E., Wang, G.L., Roe, R., Semenza, G.L., Dimerization, DNA binding, and transactivation properties of hypoxia-inducible factor 1. J. Biol. Chem. 271 (1996), 17771–17778.
11. Giaccia, A., Siim, B.G., Johnson, R.S., HIF-1 as a target for drug development. Nat. Rev. Drug. Discov. 2 (2003), 803–811.
12. Semenza, G.L., Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer 3 (2003), 721–732.
13. Semenza, G.L., Physiology meets biophysics: visualizing the interaction of hypoxia-inducible factor-1α with p300 and CBP. Proc. Natl. Acad. Sci. U. S. A. 99 (2002), 11570–11572.
14. Freedman, S.J., Sun, Z.-Y.J., Poy, F., Kung, A.L., Livingston, D.M., Wagner, G., et al. Structural basis for recruitment of CBP/p300 by hypoxia-inducible factor-1α. Proc. Natl. Acad. Sci. U. S. A. 99 (2002), 5367–5372.
15. Gu, J., Milligan, J., Huang, L.E., Molecular mechanism of hypoxia-inducible factor 1alpha-p300 interaction. A leucine-rich interface regulated by a single cysteine. J. Biol. Chem. 276 (2001), 3550–3554.
16. Kung, A.L., Wang, S., Klco, J.M., Kaelin, W.G., Livingston, D.M., Suppression of tumor growth through disruption of hypoxia-inducible transcription. Nat. Med. 6 (2000), 1335–1340.
17. Stites, W.E., Protein−protein interactions: interface structure, binding thermodynamics, and mutational analysis. Chem. Rev. 97 (1997), 1233–1250.
18. Jones, S., Thornton, J.M., Principles of protein-protein interactions. Proc. Natl. Acad. Sci. U. S. A. 93 (1996), 13–20.
19. Henchey, L.K., Kushal, S., Dubey, R., Chapman, R.N., Olenyuk, B.Z., Arora, P.S., Inhibition of hypoxia inducible factor 1—transcription coactivator interaction by a hydrogen bond surrogate α-Helix. J. Am. Chem. Soc. 132 (2010), 941–943.
20. Kushal, S., Lao, B.B., Henchey, L.K., Dubey, R., Mesallati, H., Traaseth, N.J., et al. Protein domain mimetics as in vivo modulators of hypoxia-inducible factor signaling. Proc. Natl. Acad. Sci. U. S. A., 2013, 15602–15607.
21. Burslem, G.M., Kyle, H.F., Breeze, A.L., Edwards, T.A., Nelson, A., Warriner, S.L., et al. Small-molecule proteomimetic inhibitors of the HIF-1α–p300 protein–protein interaction. ChemBioChem, 2014, 1083–1087.
22. Lao, B.B., Grishagin, I., Mesallati, H., Brewer, T.F., Olenyuk, B.Z., Arora, P.S., In vivo modulation of hypoxia-inducible signaling by topographical helix mimetics. Proc. Natl. Acad. Sci. U. S. A., 2014, 7531–7536.
23. Huang, W., Huang, R., Attene-Ramos, M.S., Sakamuru, S., Englund, E.E., Inglese, J., et al. Synthesis and evaluation of quinazolin-4-ones as hypoxia-inducible factor-1α inhibitors. Bioorg. Med. Chem. Lett. 21 (2011), 5239–5243.
24. Moreno-Manzano, V., Rodríguez-Jiménez, F.J., Aceña-Bonilla, J.L., Fustero-Lardíes, S., Erceg, S., Dopazo, J., et al. FM19G11, a new hypoxia-inducible factor (HIF) modulator, affects stem cell differentiation status. J. Biol. Chem. 285 (2010), 1333–1342.
25. Kong, D., Park, E.J., Stephen, A.G., Calvani, M., Cardellina, J.H., Monks, A., et al. Echinomycin, a small-molecule inhibitor of hypoxia-inducible factor-1 DNA-binding activity. Cancer Res. 65 (2005), 9047–9055.
26. Tan, C., de Noronha, R.G., Roecker, A.J., Pyrzynska, B., Khwaja, F., Zhang, Z., et al. Identification of a novel small-molecule inhibitor of the hypoxia-inducible factor 1 pathway. Cancer Res. 65 (2005), 605–612.
27. Lee, K., Lee, J.H., Boovanahalli, S.K., Jin, Y., Lee, M., Jin, X., et al. (Aryloxyacetylamino)benzoic acid analogues: a new class of hypoxia-inducible factor-1 inhibitors. J. Med. Chem. 50 (2007), 1675–1684.
28. Kwon, H.S., Kim, D.-R., Yang, E.G., Park, Y.K., Ahn, H.-C., Min, S.-J., et al. Inhibition of VEGF transcription through blockade of the hypoxia inducible factor-1α–p300 interaction by a small molecule. Bioorg. Med. Chem. Lett. 22 (2012), 5249–5252.
29. Na, Y.-R., Han, K.-C., Park, H., Yang, E.G., Menadione and ethacrynic acid inhibit the hypoxia-inducible factor (HIF) pathway by disrupting HIF-1α interaction with p300. Biochem. Biophys. Res. Commun. 434 (2013), 879–884.
30. Welsh, S.J., Williams, R.R., Birmingham, A., Newman, D.J., Kirkpatrick, D.L., Powis, G., The thioredoxin redox inhibitors 1-methylpropyl 2-imidazolyl disulfide and pleurotin inhibit hypoxia-induced factor 1α and vascular endothelial growth factor formation 1. Mol. Cancer Ther. 2 (2003), 235–243.
31. Yang, H., Pinello, C.E., Luo, J., Li, D., Wang, Y., Zhao, L.Y., et al. Small-molecule inhibitors of acetyltransferase p300 identified by high-throughput screening are potent anticancer agents. Mol. Cancer Ther. 12 (2013), 610–620.
32. Olenyuk, B.Z., Zhang, G.-J., Klco, J.M., Nickols, N.G., Kaelin, W.G., Dervan, P.B., Inhibition of vascular endothelial growth factor with a sequence-specific hypoxia response element antagonist. Proc. Natl. Acad. Sci. U. S. A. 101 (2004), 16768–16773.
33. Nickols, N.G., Jacobs, C.S., Farkas, M.E., Dervan, P.B., Modulating hypoxia-inducible transcription by disrupting the HIF-1–DNA interface. ACS Chem. Biol. 2 (2007), 561–571.
34. Kung, A.L., Zabludoff, S.D., France, D.S., Freedman, S.J., Tanner, E.A., Vieira, A., et al. Small molecule blockade of transcriptional coactivation of the hypoxia-inducible factor pathway. Cancer Cell 6 (2004), 33–43.
35. Block, K.M., Wang, H., Szabo, L.Z., Polaske, N.W., Henchey, L.K., Dubey, R., et al. Direct inhibition of hypoxia-inducible transcription factor complex with designed dimeric epidithiodiketopiperazine. J. Am. Chem. Soc. 131 (2009), 18078–18088.
36. Dubey, R., Levin, M.D., Szabo, L.Z., Laszlo, C.F., Kushal, S., Singh, J.B., et al. Suppression of tumor growth by designed dimeric epidithiodiketopiperazine targeting hypoxia-inducible transcription factor complex. J. Am. Chem. Soc. 135 (2013), 4537–4549.
37. Kushal, S., Wang, H., László, C.F., Szábo, L.Z., Olenyuk, B.Z., Inhibition of hypoxia-inducible transcription factor complex with designed epipolythiodiketopiperazine. Biopolymers 95 (2011), 8–16.
38. Cook, K.M., Hilton, S.T., Mecinovic, J., Motherwell, W.B., Figg, W.D., Schofield, C.J., Epidithiodiketopiperazines block the interaction between hypoxia-inducible factor-1alpha (HIF-1alpha) and p300 by a zinc ejection mechanism. J. Biol. Chem. 284 (2009), 26831–26838.
39. Cherblanc, F.L., Chapman, K.L., Brown, R., Fuchter, M.J., Chaetocin is a nonspecific inhibitor of histone lysine methyltransferases. Nat. Chem. Biol. 9 (2013), 136–137.
40. Cherblanc, F.L., Chapman, K.L., Reid, J., Borg, A.J., Sundriyal, S., Alcazar-Fuoli, L., et al. On the histone lysine methyltransferase activity of fungal metabolite chaetocin. J. Med. Chem. 56 (2013), 8616–8625.
41. Tibodeau, J.D., Benson, L.M., Isham, C.R., Owen, W.G., Bible, K.C., The anticancer agent chaetocin is a competitive substrate and inhibitor of thioredoxin reductase. Antioxid. Redox Signal 11 (2009), 1097–1106.
42. Klupfel, L., Redox Characteristics of Quinones in Natural Organic Matter (NOM). 2009, PhD term paper, ETH Zurich.
43. Beheshti, A., Norouzi, P., Ganjali, M.R., A simple and robust model for predicting the reduction potential of quinones family; electrophilicity index effect. Int. J. Electrochem. Sci., 2012, 4811–4821.
44. Frontana, C., Vázquez-Mayagoitia, Á., Garza, J., Vargas, R., González, I., Substituent effect on a family of quinones in aprotic solvents: an experimental and theoretical approach. J. Phys. Chem. A 110 (2006), 9411–9419.
45. The half-wave potential for DDQ was not found in the study by Frontana. The value quoted is for the 2,3,5,6-tetrachloro-1,4-quinone which is expected to be similar to 2,3-dichloro-5,6-cyano-1,4-quinone., DDQ half wave potential.
46. Sella, E., Shabat, D., Hydroquinone–quinone oxidation by molecular oxygen: a simple tool for signal amplification through auto-generation of hydrogen peroxide. Org. Biomol. Chem. 11 (2013), 5074–5078.
47. Hirakawa, K., Oikawa, S., Hiraku, Y., Hirosawa, I., Kawanishi, S., Catechol and hydroquinone have different redox properties responsible for their differential DNA-damaging ability. Chem. Res. Toxicol. 15 (2002), 76–82.
48. Ehmke, V., Quinsaat, J.E.Q., Rivera-Fuentes, P., Heindl, C., Freymond, C., Rottmann, M., et al. Tuning and predicting biological affinity: aryl nitriles as cysteine protease inhibitors. Org. Biomol. Chem. 10 (2012), 5764–5768.
49. Li, W.-W., Heinze, J., Haehnel, W., Site-specific binding of quinones to proteins through thiol addition and addition-elimination reactions. J. Am. Chem. Soc. 127 (2005), 6140–6141.
50. Sekirnik, R., Rose, N.R., Thalhammer, A., Seden, P.T., Mecinović, J., Schofield, C.J., Inhibition of the histone lysine demethylase JMJD2A by ejection of structural Zn(II). Chem. Commun., 2009, 6376–6378.
51. Isaac, M., Latour, J.-M., Sénèque, O., Nucleophilic reactivity of zinc-bound thiolates: subtle interplay between coordination set and conformational flexibility. Chem. Sci. 3 (2012), 3409–3420.
52. Chen, Z., Zang, J., Kappler, J., Hong, X., Crawford, F., Wang, Q., et al. Structural basis of the recognition of a methylated histone tail by JMJD2A. Proc. Natl. Acad. Sci. U. S. A. 104 (2007), 10818–10823.
53. Alberts, I.L., Nadassy, K., Wodak, S.J., Analysis of zinc binding sites in protein crystal structures. Protein Sci. 7 (1998), 1700–1716.
54. Vallee, B.L., Coleman, J.E., Auld, D.S., Zinc fingers, zinc clusters, and zinc twists in DNA-binding protein domains. Proc. Natl. Acad. Sci. U. S. A. 88 (1991), 999–1003.
55. Tsuruda, L.S., Lamé, M.W., Jones, A.D., Formation of epoxide and quinone protein adducts in B6C3F1 mice treated with naphthalene, sulfate conjugate of 1,4-dihydroxynaphthalene and 1,4-naphthoquinone. Arch. Toxicol. 69 (1995), 362–367.
56. Thompson, D.C., Perera, K., London, R., Spontaneous hydrolysis of 4-trifluoromethylphenol to a quinone methide and subsequent protein alkylation. Chem. Biol. Interact. 126 (2000), 1–14.
57. Grugni, M., Cassin, M., Colella, G., De Munari, S., Pardi, G., Pavesi, P., Indole Derivatives with Antitumor Activity. Eur. Pat. Appl., EP 1835908 A2, 2007.
58. Mabjeesh, N.J., Post, D.E., Willard, M.T., Kaur, B., Van Meir, E.G., Simons, J.W., et al. Geldanamycin induces degradation of hypoxia-inducible factor 1alpha protein via the proteosome pathway in prostate cancer cells. Cancer Res. 62 (2002), 2478–2482.
59. Stebbins, C.E., Russo, A.A., Schneider, C., Rosen, N., Hartl, F.U., Pavletich, N.P., Crystal structure of an Hsp90–geldanamycin complex: targeting of a protein chaperone by an antitumor agent. Cell 89 (1997), 239–250.
60. Mooring, S.R., Wang, B., HIF-1 inhibitors as anti-cancer therapy. Sci. China Chem. 54 (2011), 24–30.
61. Stepan, A.F., Walker, D.P., Bauman, J., Price, D.A., Baillie, T.A., Kalgutkar, A.S., et al. Structural alert/reactive metabolite concept as applied in medicinal chemistry to mitigate the risk of idiosyncratic drug toxicity: a perspective based on the critical examination of trends in the top 200 drugs marketed in the United States. Chem. Res. Toxicol. 24 (2011), 1345–1410.
62. Baell, J.B., Holloway, G.A., New substructure filters for removal of pan assay interference compounds (PAINS) from screening libraries and for their exclusion in bioassays. J. Med. Chem. 53 (2010), 2719–2740.
63. Friedman, M., Mechanism of the ninhydrin reaction. II. Preparation and spectral properties of reaction products from primary aromatic amines and ninhydrin hydrate. Can. J. Chem. 45 (2011), 2271–2275.
64. Santos, J.L., Yamasaki, P.R., Chin, C.M., Takashi, C.H., Pavan, F.R., Leite, C.Q.F., Synthesis and in vitro anti Mycobacterium tuberculosis activity of a series of phthalimide derivatives. Bioorg. Med. Chem. 17 (2009), 3795–3799.