Molecular basis for the antiparasitic activity of a mercaptoacetamide derivative that inhibits histone deacetylase 8 (HDAC8) from the human pathogen schistosoma mansoni

Journal of Molecular Biology

Volumn 426, Issue 20, 2014, Pages 3442-3453

  Stolfa, Diana A ^a,f   Marek, Martin ^b   Lancelot, Julien ^c   Hauser, Alexander Thomas ^a   Walter, Alexandra ^a,d   Leproult, Emeline ^b   Melesina, Jelena ^e   Rumpf, Tobias ^a   Wurtz, Jean Marie ^b   Cavarelli, Jean ^b   Sippl, Wolfgang ^e   Pierce, Raymond J ^c   Romier, Christophe ^b   Jung, Manfred ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^c UNIV LILLE   (France)

^d GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^e MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^f UNIVERSITY OF BARI   (Italy)

Author keywords

antiparasitic activity; docking; epigenetics; thiol; X ray crystallography

Indexed keywords

ACETAMIDE DERIVATIVE; ANTISCHISTOSOMAL AGENT; CREBINOSTAT; HEXANOYLHYDROXAMATE; HISTONE DEACETYLASE 8; HISTONE DEACETYLASE INHIBITOR; HYDROXAMIC ACID; M 344; MERCAPTOACETAMIDE DERIVATIVE; PCI 34051; ST 80; SUBERANILIC ACID; THIOL DERIVATIVE; TYROSINE; UNCLASSIFIED DRUG; VORINOSTAT; ZINC ION; ANTIPARASITIC AGENT; HELMINTH PROTEIN; HISTONE DEACETYLASE; PROTEIN BINDING; THIOACETAMIDE;

ANTHELMINTIC ACTIVITY; ARTICLE; CRYSTAL STRUCTURE; DRUG INHIBITION; ENZYME ACTIVITY; HUMAN; IN VITRO STUDY; MOLECULAR DOCKING; SCHISTOSOMA MANSONI; STRUCTURE ACTIVITY RELATION; ANIMAL; ANTAGONISTS AND INHIBITORS; APOPTOSIS; BIOCATALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECTS; ENZYMOLOGY; IC50; METABOLISM; PARASITOLOGY; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; SCHISTOSOMIASIS MANSONI; X RAY CRYSTALLOGRAPHY;

SCHISTOSOMA MANSONI;

ANIMALS; ANTIPARASITIC AGENTS; APOPTOSIS; BIOCATALYSIS; CRYSTALLOGRAPHY, X-RAY; HELMINTH PROTEINS; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HUMANS; HYDROXAMIC ACIDS; INHIBITORY CONCENTRATION 50; MODELS, MOLECULAR; MOLECULAR STRUCTURE; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS MANSONI; THIOACETAMIDE;

EID: 84907575993     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2014.03.007     Document Type: Article

References (52)

1. WHO Mediacentre; Schistosomiasis (No. 115, January 2012) available at: http://www.who.int/mediacentre/factsheets/fs115/en/index.html
2. M.S. Wilson, M.M. Mentink-Kane, J.T. Pesce, T.R. Ramalingam, R. Thompson, and T.A. Wynn Immunopathology of schistosomiasis Immunol Cell Biol 85 2007 148 154
3. M.J. Doenhoff, J.R. Kusel, G.C. Coles, and D. Cioli Resistance of Schistosoma mansoni to praziquantel: is there a problem? Trans R Soc Trop Med Hyg 96 2002 465 469
4. M.J. Doenhoff, and L. Pica-Mattoccia Praziquantel for the treatment of schistosomiasis: its use for control in areas with endemic disease and prospects for drug resistance Expert Rev Anti Infect Ther 4 2006 199 210
5. S.M. Messerli, R.S. Kasinathan, W. Morgan, S. Spranger, and R.M. Greenberg Schistosoma mansoni P-glycoprotein levels increase in response to praziquantel exposure and correlate with reduced praziquantel susceptibility Mol Biochem Parasitol 167 2009 54 59
6. Y.P. Zhou, Z.D. Wu, L.L. Yang, X. Sun, X. You, and X.B. Yu Cloning, molecular characterization of a 13-kDa antigen from Schistosoma japonicum, Sj13, a putative salivary diagnosis candidate for Schistosomiasis japonica Parasitol Res 105 2009 1435 1444
7. M. Berriman, B.J. Haas, P.T. LoVerde, R.A. Wilson, G.P. Dillon, and G.C. Cerqueira The genome of the blood fluke Schistosoma mansoni Nature 460 2009 352 358
8. A.V. Protasio, I.J. Tsai, A. Babbage, S. Nichol, M. Hunt, and M.A. Aslett A systematically improved high quality genome and transcriptome of the human blood fluke Schistosoma mansoni PLoS Negl Trop Dis 6 2012 e1455
9. N.D. Young, A.R. Jex, B. Li, S. Liu, L. Yang, and Z. Xiong Whole-genome sequence of Schistosoma haematobium Nat Genet 44 2012 221 225
10. T. Jenuwein, and C.D. Allis Translating the histone code Science 293 2001 1074 1080
11. K.E. Gardner, C.D. Allis, and B.D. Strahl Operating on chromatin, a colorful language where context matters J Mol Biol 409 2011 36 46
12. R. Margueron, and D. Reinberg Chromatin structure and the inheritance of epigenetic information Nat Rev Genet 11 2010 285 296
13. S. Thiagalingam, K.H. Cheng, H.J. Lee, N. Mineva, A. Thiagalingam, and J.F. Ponte Histone deacetylases: unique players in shaping the epigenetic histone code Ann N Y Acad Sci 983 2003 84 100
14. T. Kouzarides Chromatin modifications and their function Cell 128 2007 693 705
15. F. Dubois, S. Caby, F. Oger, C. Cosseau, M. Capron, and C. Grunau Histone deacetylase inhibitors induce apoptosis, histone hyperacetylation and up-regulation of gene transcription in Schistosoma mansoni Mol Biochem Parasitol 168 2009 7 15
16. F. Oger, F. Dubois, S. Caby, C. Noel, J. Cornette, and B. Bertin The class I histone deacetylases of the platyhelminth parasite Schistosoma mansoni Biochem Biophys Res Commun 377 2008 1079 1084
17. M. Marek, S. Kannan, A.T. Hauser, M. Moraes Mourao, S. Caby, and V. Cura Structural basis for the inhibition of histone deacetylase 8 (HDAC8), a key epigenetic player in the blood fluke Schistosoma mansoni PLoS Pathog 9 2013 e1003645
18. M. Jung, G. Brosch, D. Kolle, H. Scherf, C. Gerhauser, and P. Loidl Amide analogues of trichostatin A as inhibitors of histone deacetylase and inducers of terminal cell differentiation J Med Chem 42 1999 4669 4679
19. G.K. Scott, C. Marx, C.E. Berger, L.R. Saunders, E. Verdin, and S. Schafer Destabilization of ERBB2 transcripts by targeting 3′ untranslated region messenger RNA associated HuR and histone deacetylase-6 Mol Cancer Res 6 2008 1250 1258
20. D.M. Fass, S.A. Reis, B. Ghosh, K.M. Hennig, N.F. Joseph, and W.N. Zhao Crebinostat: a novel cognitive enhancer that inhibits histone deacetylase activity and modulates chromatin-mediated neuroplasticity Neuropharmacology 64 2013 81 96
21. J.C. Stowell, R.I. Huot, and L. Van Voast The synthesis of N-hydroxy-N′-phenyloctanediamide and its inhibitory effect on proliferation of AXC rat prostate cancer cells J Med Chem 38 1995 1411 1413
22. T. Suzuki, A. Matsuura, A. Kouketsu, H. Nakagawa, and N. Miyata Identification of a potent non-hydroxamate histone deacetylase inhibitor by mechanism-based drug design Bioorg Med Chem Lett 15 2005 331 335
23. T. Suzuki, Y. Nagano, A. Kouketsu, A. Matsuura, S. Maruyama, and M. Kurotaki Novel inhibitors of human histone deacetylases: design, synthesis, enzyme inhibition, and cancer cell growth inhibition of SAHA-based non-hydroxamates J Med Chem 48 2005 1019 1032
24. B. Chen, P.A. Petukhov, M. Jung, A. Velena, E. Eliseeva, and A. Dritschilo Chemistry and biology of mercaptoacetamides as novel histone deacetylase inhibitors Bioorg Med Chem Lett 15 2005 1389 1392
25. W. Gu, I. Nusinzon, R.D. Smith, C.M. Horvath, and R.B. Silverman Carbonyl- and sulfur-containing analogs of suberoylanilide hydroxamic acid: potent inhibition of histone deacetylases Bioorg Med Chem 14 2006 3320 3329
26. H. Ueda, H. Nakajima, Y. Hori, T. Fujita, M. Nishimura, and T. Goto FR901228, a novel antitumor bicyclic depsipeptide produced by Chromobacterium violaceum No. 968. I. Taxonomy, fermentation, isolation, physico-chemical and biological properties, and antitumor activity J Antibiot (Tokyo) 47 1994 301 310
27. K.M. VanderMolen, W. McCulloch, C.J. Pearce, and N.H. Oberlies Romidepsin (Istodax, NSC 630176, FR901228, FK228, depsipeptide): a natural product recently approved for cutaneous T-cell lymphoma J Antibiot (Tokyo) 64 2011 525 531
28. M. Kijima, M. Yoshida, K. Sugita, S. Horinouchi, and T. Beppu Trapoxin, an antitumor cyclic tetrapeptide, is an irreversible inhibitor of mammalian histone deacetylase J Biol Chem 268 1993 22429 22435
29. S. Uesato, M. Kitagawa, Y. Nagaoka, T. Maeda, H. Kuwajima, and T. Yamori Novel histone deacetylase inhibitors: N-hydroxycarboxamides possessing a terminal bicyclic aryl group Bioorg Med Chem Lett 12 2002 1347 1349
30. J. Lancelot, S. Caby, F. Dubois-Abdesselem, M. Vanderstraete, J. Trolet, and G. Oliveira Schistosoma mansoni sirtuins: characterization and potential as chemotherapeutic targets PLoS Negl Trop Dis 7 2013 e2428
31. +-dependent histone deacetylases, from kinase to sirtuin inhibition J Med Chem 49 2006 7307 7316
32. L. Whitehead, M.R. Dobler, B. Radetich, Y. Zhu, P.W. Atadja, and T. Claiborne Human HDAC isoform selectivity achieved via exploitation of the acetate release channel with structurally unique small molecule inhibitors Bioorg Med Chem 19 2011 4626 4634
33. S. Balasubramanian, J. Ramos, W. Luo, M. Sirisawad, E. Verner, and J.J. Buggy A novel histone deacetylase 8 (HDAC8)-specific inhibitor PCI-34051 induces apoptosis in T-cell lymphomas Leukemia 22 2008 1026 1034
34. K.E. Cole, D.P. Dowling, M.A. Boone, A.J. Phillips, and D.W. Christianson Structural basis of the antiproliferative activity of largazole, a depsipeptide inhibitor of the histone deacetylases J Am Chem Soc 133 2011 12474 12477
35. Y.M. Sung, T. Lee, H. Yoon, A.M. DiBattista, J.M. Song, and Y. Sohn Mercaptoacetamide-based class II HDAC inhibitor lowers Abeta levels and improves learning and memory in a mouse model of Alzheimer's disease Exp Neurol 239 2013 192 201
36. J.H. Kalin, H. Zhang, S. Gaudrel-Grosay, G. Vistoli, and A.P. Kozikowski Chiral mercaptoacetamides display enantioselective inhibition of histone deacetylase 6 and exhibit neuroprotection in cortical neuron models of oxidative stress ChemMedChem 7 2012 425 439
37. A.P. Kozikowski, Y. Chen, A. Gaysin, B. Chen, M.A. D'Annibale, and C.M. Suto Functional differences in epigenetic modulators-superiority of mercaptoacetamide-based histone deacetylase inhibitors relative to hydroxamates in cortical neuron neuroprotection studies J Med Chem 50 2007 3054 3061
38. M.L. Diebold, S. Fribourg, M. Koch, T. Metzger, and C. Romier Deciphering correct strategies for multiprotein complex assembly by co-expression: application to complexes as large as the histone octamer J Struct Biol 175 2011 178 188
39. B. Maurer, T. Rumpf, M. Scharfe, D.A. Stolfa, M.L. Schmitt, and W.J. He Inhibitors of the NAD(+)-dependent protein desuccinylase and demalonylase Sirt5 ACS Med Chem Lett 3 2012 1050 1053
40. B. Heltweg, J. Trapp, and M. Jung In vitro assays for the determination of histone deacetylase activity Methods 36 2005 332 337
41. Z. Otwinowski, and W. Minor Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol 276 1997 307 326
42. P.D. Adams, P.V. Afonine, G. Bunkoczi, V.B. Chen, I.W. Davis, and N. Echols PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr Sect D Biol Crystallogr 66 2010 213 221
43. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr Sect D Biol Crystallogr 60 2004 2126 2132
44. E. Blanc, P. Roversi, C. Vonrhein, C. Flensburg, S.M. Lea, and G. Bricogne Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT Acta Crystallogr Sect D Biol Crystallogr 60 2004 2210 2221
45. V.B. Chen, W.B. Arendall, J.J. Headd, D.A. Keedy, R.M. Immormino, and G.J. Kapral MolProbity: all-atom structure validation for macromolecular crystallography Acta Crystallogr Sect D Biol Crystallogr 66 2010 12 21
46. The Research Collaboratory for Structural Bioinformatics Protein Data Bank http://www.rcsb.org/pdb/
47. A. Vannini, C. Volpari, P. Gallinari, P. Jones, M. Mattu, and A. Carfi Substrate binding to histone deacetylases as shown by the crystal structure of the HDAC8-substrate complex EMBO Rep 8 2007 879 884
48. Suite 2012: Maestro version 9.3, Protein Preparation Wizard, Epik version 2.3, Glide version 5.8 2012 Schrödinger, LLC New York, NY
49. Molecular Operating Environment (MOE), 2012.10 2012 Chemical Computing Group Inc. Montreal, QC, Canada
50. G. Jones, P. Willett, R.C. Glen, A.R. Leach, and R. Taylor Development and validation of a genetic algorithm for flexible docking J Mol Biol 267 1997 727 748
51. B. Bertin, F. Oger, J. Cornette, S. Caby, C. Noel, and M. Capron Schistosoma mansoni CBP/p300 has a conserved domain structure and interacts functionally with the nuclear receptor SmFtz-F1 Mol Biochem Parasitol 146 2006 180 191
52. F.J. Ramalho-Pinto, G. Gazzinelli, R.E. Howells, T.A. Mota-Santos, E.A. Figueiredo, and J. Pellegrino Schistosoma mansoni: defined system for stepwise transformation of cercaria to schistosomule in vitro Exp Parasitol 36 1974 360 372