Targeting of histone acetyltransferase p300 by cyclopentenone prostaglandin Δ 12-PGJ 2 through covalent binding to Cys 1438

Chemical Research in Toxicology

Volumn 25, Issue 2, 2012, Pages 337-347

  Ravindra, Kodihalli C ^a   Narayan, Vivek ^a   Lushington, Gerald H ^b   Peterson, Blake R ^b   Prabhu, K Sandeep ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF KANSAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOPENTENONE DERIVATIVE; CYSTEINE; ELECTROPHILE; HISTONE ACETYLTRANSFERASE PCAF; HISTONE H3; PROSTAGLANDIN J2;

ARTICLE; BIOTINYLATION; CELL ASSAY; COVALENT BOND; ELECTROPHILICITY; HISTONE ACETYLATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; NONHUMAN;

ANIMALS; BINDING SITES; CELL LINE; CELL LINE, TUMOR; CYSTEINE; HEPATOCYTES; HISTONE ACETYLTRANSFERASES; HUMANS; MACROPHAGES; MICE; MODELS, MOLECULAR; PEPTIDES; PROSTAGLANDIN D2; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84859756203     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx200383c     Document Type: Article

References (54)

1. Smith, W. L., DeWitt, D. L., and Garavito, R. M. (2000) Cyclooxygenases: structural, cellular, and molecular biology. Annu. Rev. Biochem. 69, 145-182.
2. Fukushima, M., Kato, T., Narumiya, S., Mizushima, Y., Sasaki, H., Terashima, Y., Nishiyama, Y., and Santoro, M. G. (1989) Prostaglandin A and J: antitumor and antiviral prostaglandins. Adv. Prostaglandins, Thromboxanes, Leukotrienes Res. 19, 415-418.
3. Gandhi, U. H., Kaushal, N., Ravindra, K. C., Hegde, S., Nelson, S. M., Narayan, V., Vunta, H., Paulson, R. F., and Prabhu, K. S. (2011) Selenoprotein-dependent up-regulation of hematopoietic prostaglandin D2 synthase in macrophages is mediated through the activation of peroxisome proliferator-activated receptor (PPAR) {gamma}. J. Biol. Chem. 286, 27471-27482.
4. Itoh, K., Mochizuki, M., Ishii, Y., Ishii, T., Shibata, T., Kawamoto, Y., Kelly, V., Sekizawa, K., Uchida, K., and Yamamoto, M. (2004) Transcription factor Nrf2 regulates inflammation by mediating the effect of 15-deoxy-Delta(12,14)-prostaglandin j(2). Mol. Cell. Biol. 24, 36-45. (Pubitemid 38010033)
5. Kliewer, S. A., Lenhard, J. M., Willson, T. M., Patel, I., Morris, D. C., and Lehmann, J. M. (1995) A prostaglandin J2 metabolite binds peroxisome proliferator-activated receptor gamma and promotes adipocyte differentiation. Cell 83, 813-819. (Pubitemid 3006325)
6. Lee, T. S., Tsai, H. L., and Chau, L. Y. (2003) Induction of heme oxygenase-1 expression in murine macrophages is essential for the anti-inflammatory effect of low dose 15-deoxy-Delta 12,14-prostaglandin J2. J. Biol. Chem. 278, 19325-19330.
7. Rossi, A., Kapahi, P., Natoli, G., Takahashi, T., Chen, Y., Karin, M., and Santoro, M. G. (2000) Anti-inflammatory cyclopentenone prostaglandins are direct inhibitors of IkappaB kinase. Nature 403, 103-108. (Pubitemid 30038530)
8. Straus, D. S., and Glass, C. K. (2001) Cyclopentenone prostaglandins: new insights on biological activities and cellular targets. Med. Res. Rev. 21, 185-210. (Pubitemid 32303994)
9. Atsmon, J., Sweetman, B. J., Baertschi, S. W., Harris, T. M., and Roberts, L. J. II. (1990) Formation of thiol conjugates of 9-deoxy-delta 9,delta 12(E)-prostaglandin D2 and delta 12(E)-prostaglandin D2. Biochemistry 29, 3760-3765.
10. Shiraki, T., Kamiya, N., Shiki, S., Kodama, T. S., Kakizuka, A., and Jingami, H. (2005) Alpha,beta-unsaturated ketone is a core moiety of natural ligands for covalent binding to peroxisome proliferator-activated receptor gamma. J. Biol. Chem. 280, 14145-14153. (Pubitemid 40517317)
11. Stamatakis, K., and Perez-Sala, D. (2006) Prostanoids with cyclopentenone structure as tools for the characterization of electrophilic lipid-protein interactomes. Ann. N.Y. Acad. Sci. 1091, 548-570. (Pubitemid 47092266)
12. Suzuki, M., Mori, M., Niwa, T., Hirata, R., Furuta, K., Ishikawa, T., and Noyori, R. (1997) Chemical implications for antitumor and antiviral prostaglandins: reaction of Δ7-prostaglandin A1 and prostaglandin A1methyl esters with thiols. J. Am. Chem. Soc. 119, 2376-2385. (Pubitemid 27167854)
13. Gayarre, J., Stamatakis, K., Renedo, M., and Perez-Sala, D. (2005) Differential selectivity of protein modification by the cyclopentenone prostaglandins PGA1 and 15-deoxy-Delta 12, 14-PGJ2: role of glutathione. FEBS Lett. 579, 5803-5808. (Pubitemid 41455667)
14. Kalantari, P., Narayan, V., Henderson, A. J., and Prabhu, K. S. (2009) 15-Deoxy-Delta 12, 14-prostaglandin J2 inhibits HIV-1 transactivating protein, Tat, through covalent modification. FASEB J. 23, 2366-2373.
15. Kim, D. H., Kim, E. H., Na, H. K., Sun, Y., and Surh, Y. J. (2010) 15-Deoxy-Delta(12,14)-prostaglandin J(2) stabilizes, but functionally inactivates p53 by binding to the cysteine 277 residue. Oncogene 29, 2560-2576.
16. Kobayashi, M., Li, L., Iwamoto, N., Nakajima-Takagi, Y., Kaneko, H., Nakayama, Y., Eguchi, M., Wada, Y., Kumagai, Y., and Yamamoto, M. (2009) The antioxidant defense system Keap1-Nrf2 comprises a multiple sensing mechanism for responding to a wide range of chemical compounds. Mol. Cell. Biol. 29, 493-502.
17. Noyori, R., and Suzuki, M. (1993) Organic synthesis of prostaglandins: advancing biology. Sci 259, 44-45. (Pubitemid 23036085)
18. Oliva, J. L., Perez-Sala, D., Castrillo, A., Martinez, N., Canada, F. J., Bosca, L., and Rojas, J. M. (2003) The cyclopentenone 15-deoxy-delta 12,14-prostaglandin J2 binds to and activates H-Ras. Proc. Natl. Acad. Sci. U.S.A. 100, 4772-4777. (Pubitemid 36469241)
19. Shibata, T., Yamada, T., Ishii, T., Kumazawa, S., Nakamura, H., Masutani, H., Yodoi, J., and Uchida, K. (2003) Thioredoxin as a molecular target of cyclopentenone prostaglandins. J. Biol. Chem. 278, 26046-26054. (Pubitemid 36835372)
20. Cernuda-Morollon, E., Pineda-Molina, E., Canada, F. J., and Perez-Sala, D. (2001) 15-Deoxy-Delta 12,14-prostaglandin J2 inhibition of NF-kappaB-DNA binding through covalent modification of the p50 subunit. J. Biol. Chem. 276, 35530-35536.
21. Batta, K., Das, C., Gadad, S., Shandilya, J., and Kundu, T. K. (2007) Reversible acetylation of non histone proteins: role in cellular function and disease. Subcell. Biochem. 41, 193-212.
22. van Attikum, H., and Gasser, S. M. (2005) The histone code at DNA breaks: a guide to repair? Nat. Rev. Mol. Cell Biol. 6, 757-765. (Pubitemid 41726114)
23. Wei, Y., Yu, L., Bowen, J., Gorovsky, M. A., and Allis, C. D. (1999) Phosphorylation of histone H3 is required for proper chromosome condensation and segregation. Cell 97, 99-109. (Pubitemid 29165893)
24. Grant, P. A., and Berger, S. L. (1999) Histone acetyltransferase complexes. Semin. Cell Dev. Biol. 10, 169-177. (Pubitemid 129502408)
25. Roth, S. Y., Denu, J. M., and Allis, C. D. (2001) Histone acetyltransferases. Annu. Rev. Biochem. 70, 81-120. (Pubitemid 32662206)
26. Barnes, P. J., Adcock, I. M., and Ito, K. (2005) Histone acetylation and deacetylation: importance in inflammatory lung diseases. Eur. Respir. J. 25, 552-563. (Pubitemid 40331188)
27. Iyer, N. G., Ozdag, H., and Caldas, C. (2004) p300/CBP and cancer. Oncogene 23, 4225-4231. (Pubitemid 38758588)
28. McKinsey, T. A., and Olson, E. N. (2004) Cardiac histone acetylation: therapeutic opportunities abound. Trends Genet. 20, 206-213. (Pubitemid 38369192)
29. Pumfery, A., Deng, L., Maddukuri, A., de la Fuente, C., Li, H., Wade, J. D., Lambert, P., Kumar, A., and Kashanchi, F. (2003) Chromatin remodeling and modification during HIV-1 Tat-activated transcription. Curr. HIV Res. 1, 343-362.
30. Sterner, D. E., and Berger, S. L. (2000) Acetylation of histones and transcription-related factors. Microbiol. Mol. Biol. Rev. 64, 435-459. (Pubitemid 30412680)
31. Balasubramanyam, K., Altaf, M., Varier, R. A., Swaminathan, V., Ravindran, A., Sadhale, P. P., and Kundu, T. K. (2004) Polyisoprenylated benzophenone, garcinol, a natural histone acetyltransferase inhibitor, represses chromatin transcription and alters global gene expression. J. Biol. Chem. 279, 33716-33726. (Pubitemid 39063021)
32. Balasubramanyam, K., Swaminathan, V., Ranganathan, A., and Kundu, T. K. (2003) Small molecule modulators of histone acetyltransferase p300. J. Biol. Chem. 278, 19134-19140. (Pubitemid 36799302)
33. Balasubramanyam, K., Varier, R. A., Altaf, M., Swaminathan, V., Siddappa, N. B., Ranga, U., and Kundu, T. K. (2004) Curcumin, a novel p300/CREB-binding protein-specific inhibitor of acetyltransferase, represses the acetylation of histone/nonhistone proteins and histone acetyltransferase-dependent chromatin transcription. J. Biol. Chem. 279, 51163-51171. (Pubitemid 40017859)
34. Lau, O. D., Kundu, T. K., Soccio, R. E., Ait-Si-Ali, S., Khalil, E. M., Vassilev, A., Wolffe, A. P., Nakatani, Y., Roeder, R. G., and Cole, P. A. (2000) HATs off: selective synthetic inhibitors of the histone acetyltransferases p300 and PCAF. Mol. Cell 5, 589-595.
35. Mantelingu, K., Reddy, B. A., Swaminathan, V., Kishore, A. H., Siddappa, N. B., Kumar, G. V., Nagashankar, G., Natesh, N., Roy, S., Sadhale, P. P., Ranga, U., Narayana, C., and Kundu, T. K. (2007) Specific inhibition of p300-HAT alters global gene expression and represses HIV replication. Chem. Biol. 14, 645-657. (Pubitemid 46929090)
36. Ravindra, K. C., Selvi, B. R., Arif, M., Reddy, B. A., Thanuja, G. R., Agrawal, S., Pradhan, S. K., Nagashayana, N., Dasgupta, D., and Kundu, T. K. (2009) Inhibition of lysine acetyltransferase KAT3B/p300 activity by a naturally occurring hydroxynaphthoquinone, plumbagin. J. Biol. Chem. 284, 24453-24464.
37. Bowers, E. M., Yan, G., Mukherjee, C., Orry, A., Wang, L., Holbert, M. A., Crump, N. T., Hazzalin, C. A., Liszczak, G., Yuan, H., Larocca, C., Saldanha, S. A., Abagyan, R., Sun, Y., Meyers, D. J., Marmorstein, R., Mahadevan, L. C., Alani, R. M., and Cole, P. A. (2010) Virtual ligand screening of the p300/CBP histone acetyltransferase: identification of a selective small molecule inhibitor. Chem. Biol. 17, 471-482.
38. Liu, X., Wang, L., Zhao, K., Thompson, P. R., Hwang, Y., Marmorstein, R., and Cole, P. A. (2008) The structural basis of protein acetylation by the p300/CBP transcriptional coactivator. Nature 451, 846-850. (Pubitemid 351253165)
39. Kundu, T. K., Palhan, V. B., Wang, Z., An, W., Cole, P. A., and Roeder, R. G. (2000) Activator-dependent transcription from chromatin in vitro involving targeted histone acetylation by p300. Mol. Cell 6, 551-561.
40. Bai, X., Wu, L., Liang, T., Liu, Z., Li, J., Li, D., Xie, H., Yin, S., Yu, J., Lin, Q., and Zheng, S. (2008) Overexpression of myocyte enhancer factor 2 and histone hyperacetylation in hepatocellular carcinoma. J. Cancer Res. Clin. Oncol. 134, 83-91. (Pubitemid 350060688)
41. Vunta, H., Davis, F., Palempalli, U. D., Bhat, D., Arner, R. J., Thompson, J. T., Peterson, D. G., Reddy, C. C., and Prabhu, K. S. (2007) The anti-inflammatory effects of selenium are mediated through 15-deoxy-Delta 12, 14-prostaglandin J2 in macrophages. J. Biol. Chem. 282, 17964-17973. (Pubitemid 47100228)
42. Ott, M., Schnolzer, M., Garnica, J., Fischle, W., Emiliani, S., Rackwitz, H. R., and Verdin, E. (1999) Acetylation of the HIV-1 Tat protein by p300 is important for its transcriptional activity. Curr. Biol. 9, 1489-1492. (Pubitemid 30023485)
43. Millan, O., Rico, D., Peinado, H., Zarich, N., Stamatakis, K., Perez-Sala, D., Rojas, J. M., Cano, A., and Bosca, L. (2006) Potentiation of tumor formation by topical administration of 15-deoxy-delta 12, 14-prostaglandin J2 in a model of skin carcinogenesis. Carcinogenesis 27, 328-336. (Pubitemid 43159887)
44. Rajakariar, R., Hilliard, M., Lawrence, T., Trivedi, S., Colville-Nash, P., Bellingan, G., Fitzgerald, D., Yaqoob, M. M., and Gilroy, D. W. (2007) Hematopoietic prostaglandin D2 synthase controls the onset and resolution of acute inflammation through PGD2 and 15-deoxyDelta12 14 PGJ2. Proc. Natl. Acad. Sci. U.S.A. 104, 20979-20984.
45. Hironaka, A., Morisugi, T., Kawakami, T., Miyagi, I., and Tanaka, Y. (2009) 15-Deoxy-Delta(12,14)-prostaglandin J(2) impairs the functions of histone acetyltransferases through their insolubilization in cells. Biochem. Biophys. Res. Commun. 390, 290-294.
46. Doyle, K., and Fitzpatrick, F. A. (2010) Redox signaling, alkylation (carbonylation) of conserved cysteines inactivates class I histone deacetylases 1, 2, and 3 and antagonizes their transcriptional repressor function. J. Biol. Chem. 285, 17417-17424.
47. Wang, L., Tang, Y., Cole, P. A., and Marmorstein, R. (2008) Structure and chemistry of the p300/CBP and Rtt109 histone acetyltransferases: implications for histone acetyltransferase evolution and function. Curr. Opin. Struct. Biol. 18, 741-747.
48. Maxey, K. M., Hessler, E., MacDonald, J., and Hitchingham, L. (2000) The nature and composition of 15-deoxy-Delta(12,14)PGJ(2). Prostaglandins Other Lipid Mediators 62, 15-21.
49. Koharudin, L. M., Liu, H., Di Maio, R., Kodali, R. B., Graham, S. H., and Gronenborn, A. M. (2010) Cyclopentenone prostaglandin-induced unfolding and aggregation of the Parkinson disease-associated UCH-L1. Proc. Natl. Acad. Sci. U.S.A. 107, 6835-6840.
50. Sanchez-Gomez, F. J., Diez-Dacal, B., Pajares, M. A., Llorca, O., and Perez-Sala, D. (2010) Cyclopentenone prostaglandins with dienone structure promote cross-linking of the chemoresistance-inducing enzyme glutathione transferase P1-1. Mol. Pharmacol. 78, 723-733.
51. Sun, Y. P., Oh, S. F., Uddin, J., Yang, R., Gotlinger, K., Campbell, E., Colgan, S. P., Petasis, N. A., and Serhan, C. N. (2007) Resolvin D1 and its aspirin-triggered 17R epimer. Stereochemical assignments, anti-inflammatory properties, and enzymatic inactivation. J. Biol. Chem. 282, 9323-9334. (Pubitemid 47104612)
52. Clements, A., Rojas, J. R., Trievel, R. C., Wang, L., Berger, S. L., and Marmorstein, R. (1999) Crystal structure of the histone acetyltransferase domain of the human PCAF transcriptional regulator bound to coenzyme A. EMBO J. 18, 3521-3532. (Pubitemid 29308833)
53. Biel, M., Kretsovali, A., Karatzali, E., Papamatheakis, J., and Giannis, A. (2004) Design, synthesis, and biological evaluation of a small-molecule inhibitor of the histone acetyltransferase Gcn5. Angew. Chem., Int. Ed. 43, 3974-3976. (Pubitemid 39257485)
54. Stimson, L., Rowlands, M. G., Newbatt, Y. M., Smith, N. F., Raynaud, F. I., Rogers, P., Bavetsias, V., Gorsuch, S., Jarman, M., Bannister, A., Kouzarides, T., McDonald, E., Workman, P., and Aherne, G. W. (2005) Isothiazolones as inhibitors of PCAF and p300 histone acetyltransferase activity. Mol. Cancer Ther. 4, 1521-1532. (Pubitemid 41556434)