Synthesis of rigidified eIF4E/eIF4G inhibitor-1 (4EGI-1) mimetic and their in vitro characterization as inhibitors of protein-protein interaction

Journal of Medicinal Chemistry

Volumn 57, Issue 12, 2014, Pages 5094-5111

  Mahalingam, Poornachandran ^a   Takrouri, Khuloud ^a,b   Chen, Ting ^a,b   Sahoo, Rupam ^a,b   Papadopoulos, Evangelos ^a   Chen, Limo ^a   Wagner, Gerhard ^a   Aktas, Bertal H ^a,b   Halperin, Jose A ^a,b   Chorev, Michael ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; BRIDGED COMPOUND; CARBENE; EIF4E EIF4G INHIBITOR 1; ETHYLENE; INITIATION FACTOR 4E; INITIATION FACTOR 4G; METHYLENE OXIDE; METHYLENESULFIDE; METHYLENESULFONE; METHYLENESULFOXIDE; SULFONE DERIVATIVE; THIAZOLE DERIVATIVE; UNCLASSIFIED DRUG;

ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CANCER CELL LINE; COMPLEX FORMATION; CONTROLLED STUDY; DRUG DESIGN; DRUG POTENCY; DRUG SYNTHESIS; EUKARYOTE; HUMAN; HUMAN CELL; IN VITRO STUDY; PROTEIN PROTEIN INTERACTION; TRANSLATION INITIATION;

ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CELL PROLIFERATION; DRUG SCREENING ASSAYS, ANTITUMOR; EUKARYOTIC INITIATION FACTOR-4E; EUKARYOTIC INITIATION FACTOR-4G; HETEROCYCLIC COMPOUNDS, 3-RING; HUMANS; HYDRAZONES; MOLECULAR MIMICRY; STEREOISOMERISM; STRUCTURE-ACTIVITY RELATIONSHIP; THIAZOLES;

EID: 84903523080     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm401733v     Document Type: Article

References (65)

1. Sonenberg, N.; Hinnebusch, A. G. Regulation of translation initiation in eukaryotes: mechanisms and biological targets Cell 2009, 136, 731-745
2. De Rubeis, S.; Bagni, C. Regulation of Molecular Pathways in the Fragile X Syndrome: Insights into Autism Spectrum Disorders J. Neurodev. Disord. 2011, 3, 257-269
3. Avdulov, S.; Li, S.; Michalek, V.; Burrichter, D.; Peterson, M.; Perlman, D. M.; Manivel, J. C.; Sonenberg, N.; Yee, D.; Bitterman, P. B.; Polunovsky, V. A. Activation of translation complex eIF4F is essential for the genesis and maintenance of the malignant phenotype in human mammary epithelial cells Cancer Cell 2004, 5, 553-563
4. Gebauer, F.; Hentze, M. W. Molecular mechanisms of translational control Nature Rev. Mol. Cell Biol. 2004, 5, 827-835
5. Pestova, T. V.; Lorsch, J. R.; Hellen, C. U. T. The Mechanism of Translation Initiation in Eukaryotes; Cold Spring Harbor Laboratory Press: Woodbury, NY, 2007; Vol. 48.
6. Poulin, F.; Sonenberg, N. Mechanism of Translation Initiation in Eukaryotes; Landes Bioscience: Austin, TX, 2003.
7. Sonenberg, N. eIF4E, the mRNA cap-binding protein: from basic discovery to translational research Biochem. Cell. Biol. 2008, 86, 178-183
8. De Benedetti, A.; Graff, J. R. eIF-4E expression and its role in malignancies and metastases Oncogene 2004, 23, 3189-3199
9. Goodfellow, I. G.; Roberts, L. O. Eukaryotic initiation factor 4E Int. J. Biochem. Cell Biol. 2008, 40, 2675-2680
10. Raught, B.; Gingras, A. C. eIF4E activity is regulated at multiple levels Int. J. Biochem. Cell Biol. 1999, 31, 43-57
11. Gingras, A. C.; Raught, B.; Sonenberg, N. eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation Annu. Rev. Biochem. 1999, 68, 913-963
12. Koromilas, A. E.; Lazaris-Karatzas, A.; Sonenberg, N. mRNAs containing extensive secondary structure in their 5′ non-coding region translate efficiently in cells overexpressing initiation factor eIF-4E EMBO J. 1992, 11, 4153-4158
13. Graff, J. R.; Konicek, B. W.; Carter, J. H.; Marcusson, E. G. Targeting the eukaryotic translation initiation factor 4E for cancer therapy Cancer Res. 2008, 68, 631-634
14. Gkogkas, C. G.; Khoutorsky, A.; Ran, I.; Rampakakis, E.; Nevarko, T.; Weatherill, D. B.; Vasuta, C.; Yee, S.; Truitt, M.; Dallaire, P.; Major, F.; Lasko, P.; Ruggero, D.; Nader, K.; Lacaille, J. C.; Sonenberg, N. Autism-related deficits via dysregulated eIF4E-dependent translational control Nature 2013, 493, 371-377
15. Napoli, I.; Mercaldo, V.; Boyl, P. P.; Eleuteri, B.; Zalfa, F.; De Rubeis, S.; Di Marino, D.; Mohr, E.; Massimi, M.; Falconi, M.; Witke, W.; Costa-Mattioli, M.; Sonenberg, N.; Achsel, T.; Bagni, C. The fragile X syndrome protein represses activity-dependent translation through CYFIP1, a new 4E-BP Cell 2007, 134, 1042-1054
16. Tsai, P. T.; Hull, C.; Chu, Y.; Greene-Colozzi, E.; Sadowski, A. R.; Leech, J. M.; Steinberg, J.; Crawley, J. N.; Regehr, W. G.; Sahin, M. Autistic-like behaviour and cerebellar dysfunction in Purkinje cell Tsc1 mutant mice Nature 2012, 488, 647-651
17. Jia, Y.; Polunovsky, V. A.; Bitterman, P. B.; Wagner, C. R. Cap-dependent translation initiation factor eIF4E: an emerging anticancer drug target Med. Res. Rev. 2012, 32, 786-814
18. Rousseau, D.; Gingras, A. C.; Pause, A.; Sonenberg, N. The eIF4E-binding proteins 1 and 2 are negative regulators of cell growth Oncogene 1996, 13, 2415-2420
19. Meric, F.; Hunt, K. K. Translation initiation in cancer: a novel target for therapy Mol. Cancer Ther. 2002, 1, 971-979
20. Aktas, B. H.; Halperin, J. A.; wagner, G.; Chorev, M. Inhibition of Translation Initiation as a Novel Paradigm for Cancer Therapy. Elsevier Inc Academic Press: New York, 2011.
21. Kong, J.; Lasko, P. Translational control in cellular and developmental processes Nature Rev. Genet. 2012, 13, 383-394
22. Moerke, N. J.; Aktas, H.; Chen, H.; Cantel, S.; Reibarkh, M. Y.; Fahmy, A.; Gross, J. D.; Degterev, A.; Yuan, J.; Chorev, M.; Halperin, J. A.; Wagner, G. Small-molecule inhibition of the interaction between the translation initiation factors eIF4E and eIF4G Cell 2007, 128, 257-267
23. Tamburini, J.; Green, A. S.; Bardet, V.; Chapuis, N.; Park, S.; Willems, L.; Uzunov, M.; Ifrah, N.; Dreyfus, F.; Lacombe, C.; Mayeux, P.; Bouscary, D. Protein synthesis is resistant to rapamycin and constitutes a promising therapeutic target in acute myeloid leukemia Blood 2009, 114, 1618-1627
24. Chen, L.; Aktas, B. H.; Wang, Y.; He, X.; Sahoo, R.; Zhang, N.; Denoyelle, S.; Kabha, E.; Yang, H.; Freedman, R. Tumor suppression by small molecule inhibitors of translation initiation Oncotarget 2012, 3, 869-881
25. Hoeffer, C. A.; Cowansage, K. K.; Arnold, E. C.; Banko, J. L.; Moerke, N. J.; Rodriguez, R.; Schimdt, E. K.; Klosi, E.; Chorev, M.; Lloyd, R. E.; Pierre, P.; Wagner, G.; LeDoux, J. E.; Klann, E. Inhibition of the interactions between eukaryotic initiation factors 4E and 4G impairs long-term associative memory consolidation but not reconsolidation Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 3383-3388
26. Santini, E.; Huynh, T. N.; MacAskill, A. F.; Carter, A. G.; Pierre, P.; Ruggero, D.; Kaphzan, H.; Klann, E. Exaggerated translation causes synaptic and behavioural aberrations associated with autism Nature 2013, 493, 411-415
27. McMahon, R.; Zaborowska, I.; Walsh, D. Noncytotoxic Inhibition of Viral Infection through eIF4F-Independent Suppression of Translation by 4EGI-1 J. Virol. 2011, 85, 853-864
28. Kabha, E.; Wang, Y.; Chen, L.; Zhang, N.; Rodriguez, R.; Papadopoulos, P.; Wagner, G.; Aktas, B. H.; Halperin, J. A.; Chorev, M. Identification of the pharmacophore of 4EGI-1, an inhibitor of translation initiation with anti-cancer activity. In 240th ACS National Meeting & Exposition, Boston, MA, United States, August 22-26; American Chemical Society: Boston, 2010; pp MEDI-28.
29. Takrouri, K.; Chen, T.; Papadopoulos, E.; Sahoo, R.; Kabha, E.; Chen, H.; Cantel, S.; Wagner, G.; Halperin, J. A.; Aktas, B. H.; Chorev, M. Structure-activity relationship study of 4EGI-1, small molecule eIF4E/eIF4G protein-protein interaction inhibitors Eur. J. Med. Chem. 2014, 77, 361-377
30. Caprathe, B. W.; Jaen, J. C.; Wise, L. D.; Heffner, T. G.; Pugsley, T. A.; Meltzer, L. T.; Parvez, M. Dopamine autoreceptor agonists as potential antipsychotics. 3.6-Propyl-4,5,5a,6,7,8-hexahydrothiazolo[4,5- f ]quinolin-2-amine J. Med. Chem. 1991, 34, 2736-2746
31. Hu, Q.; Negri, M.; Jahn-Hoffmann, K.; Zhuang, Y.; Olgen, S.; Bartels, M.; Müller-Vieira, U.; Lauterbach, T.; Hartmann, R. W. Synthesis, biological evaluation, and molecular modeling studies of methylene imidazole substituted biaryls as inhibitors of human 17α-hydroxylase-17,20-lyase (CYP17)-Part II: Core rigidification and influence of substituents at the methylene bridge Bioorg. Med. Chem. 2008, 16, 7715-7727
32. Lucas, S.; Negri, M.; Heim, R.; Zimmer, C.; Hartmann, R. W. Fine-tuning the selectivity of aldosterone synthase inhibitors: structure-activity and structure-selectivity insights from studies of heteroaryl substituted 1,2,5,6-tetrahydropyrrolo[3,2,1- ij ]quinolin-4-one derivatives J. Med. Chem. 2011, 54, 2307-2319
33. Jenkins, P. R.; Wilson, J.; Emmerson, D.; Garcia, M. D.; Smith, M. R.; Gray, S. J.; Britton, R. G.; Mahale, S.; Chaudhuri, B. Design, synthesis and biological evaluation of new tryptamine and tetrahydro-beta-carboline-based selective inhibitors of CDK4 Bioorg. Med. Chem. 2008, 16, 7728-773939
34. Sander, K.; Kottke, T.; Tanrikulu, Y.; Proschak, E.; Weizel, L.; Schneider, E. H.; Seifert, R.; Schneider, G.; Stark, H. 2,4-Diaminopyrimidines as histamine H4 receptor ligands-scaffold optimization and pharmacological characterization Bioorg. Med. Chem. 2009, 17, 7186-7196
35. Chowdhury, S.; Chafeev, M.; Liu, S.; Sun, J.; Raina, V.; Chui, R.; Young, W.; Kwan, R.; Fu, J.; Cadieux, J. A. Discovery of XEN907, a spirooxindole blocker of NaV1.7 for the treatment of pain Bioorg. Med. Chem. Lett. 2011, 21, 3676-3681
36. Spadaro, A.; Negri, M.; Marchais-Oberwinkler, S.; Bey, E.; Frotscher, M. Hydroxybenzothiazoles as new nonsteroidal inhibitors of 17beta-hydroxysteroid dehydrogenase type 1 (17beta-HSD1) PloS One 2012, 7, e29252
37. Perrone, R.; Berardi, F.; Colabufo, N. A.; Tortorella, V.; Lograno, M. D.; Daniele, E.; Govoni, S. Conformationally restricted thiazole derivatives as novel class of 5-HT3 receptor ligands Farmaco 1995, 50, 77-82
38. Chordia, M. D.; Murphree, L. J.; Macdonald, T. L.; Linden, J.; Olsson, R. A. 2-Aminothiazoles: a new class of agonist allosteric enhancers of A1 adenosine receptors Bioorg. Med. Chem. Lett. 2002, 12, 1563-1566
39. Malviya, N. J.; Kulkarni, A. M.; Jaimini, D.; Jadhav, B. L.; Karnik, A. V. Chemoselective synthesis of heterocyclic derivatives of 18-norequilenine, 16-substituted 12 H -11-oxa-15-aza-17-thiacyclopenta[ a ]phenanthrenene and their in vitro evaluation of antibacterial and antifungal activity Indian J. Chem., Sect. B 2006, 45B, 1499-1503
40. Khazi, I. A. M.; Gadad, A. K.; Mahajanshetti, C. S. Synthesis and biological activity of some 2-amino/arylamino-4 H -(1)benzothiopyrano[4,3- d ]thiazoles Indian J. Heterocycl. Chem. 1995, 4, 243-248
41. Kikuchi, T.; Nishio, M.; Ito, T.; Sekizawa, Y. Anesthetics for black carp. Japanese Patent JP 46024259, 1971.
42. Guo, C.; Fang, L.; Liu, Y.; Su, X.; Li, C.; Sun, L.; Luo, W.; Liang, L.; Huang, Y. Preparation of thiochromanone (thio)semicarbazone derivatives as antifungal agents. Canadian Patent CN 101434595, 2009.
43. Wagner, G.; Chorev, M.; Moerke, N. J.; Aktas, H.; Halperin, J. A. Preparation of cyclic inhibitors of eukaryotic translation initiation factor interaction and use in treating cancer. World Patent WO 200678942 A2, July 27, 2006.
44. Quallich, G. J.; Williams, M. T.; Friedmann, R. C. Friedel-Crafts synthesis of 4-(3,4-dichlorophenyl)-3,4-dihydro-1(2 H)-naphthalenone, a key intermediate in the preparation of the antidepressant sertraline J. Org. Chem. 1990, 55, 4971-4973
45. Sato, Y.; Mizobuchi, S.; Tanabe, K.; Inoue, H. 2-Bromo-1-tetralone derivatives. European Patent EP 125695 November 21, 1984.
46. Balsamo, A.; Breschi, M.; Giannaccinia, G.; Lapuccil, A.; Lucacchiniz, A.; Macchial, B.; Maneral, C.; Martinottiz, C. M. E.; Nencettil, S.; Rossellol, A.; Scatizziz, R. Synthesis and P-adrenergic properties of tetrahydronaphthalene analogs of dichloroisoproterenol Eur. J. Med. Chem. 1993, 28, 735-741
47. House, H. O.; McCaully, R. J. Polyphosphoric Acid-Catalyzed Reaction of Anisole with γ-Butyrolactone J. Org. Chem. 1959, 24, 725-726
48. Baker, B. R.; Hopkins, S. E. Irreversible enzyme inhibitors. CLXVII. Thymidine phosphorylase. 10. On the nature and dimensions of the hydrophobic bonding region. A J. Med. Chem. 1970, 13, 87-89
49. Arndt, F.; Franke, W.; Klose, W.; Lorenz, J.; Schwarz, K. Synthesen von Thiazolo- und [1,3]Thiazino[1,2,4]triazinonen Liebigs Ann. Chem. 1984, 1302-1307
50. E.I. Du Pont de Nemours and Co., Novel substituted chromanone oxides and their preparations. UK Patent GB 1265212 (A) 19720301, 1972
51. Chem. Abstr. 1972, 76, 140531t.
52. Eaton, P. E.; Carlson, G. R.; Lee, J. T. Phosphorus pentoxide- methanesulfonic acid. Convenient alternative to polyphosphoric acid J. Org. Chem. 1973, 38, 4071-4073
53. Habermann, J.; Ley, S. V.; Scicinski, J. J.; Scott, J. S.; Smits, R.; Thomas, A. W. Clean synthesis of.alpha.-bromo ketones and their utilisation in the synthesis of 2-alkoxy-2,3-dihydro-2-aryl-1,4-benzodioxanes, 2-amino-4-aryl-1,3-thiazoles and piperidino-2-amino-1,3-thiazoles using polymer-supported reagents J. Chem. Soc., Perkin Trans. 1 1999, 17, 2425-2427
54. Sarges, R. Hydantoin derivatives as therapeutic agents. U.S. Patent US 4147795, April 3, 1979.
55. Patonay, T.; Juhasz-Toth, E.; Benyei, A. Base-induced coupling of a-azido ketones with aldehydes-an easy and efficient route to trifunctionalized synthons 2-azido-3-hydroxy ketones, 2-acylaziridines, and 2-acylspiroaziridines Eur. J. Org. Chem. 2002, 2, 285-295
56. MacKenzie, N. E.; Thomson, R. H. Ring contractions of thiochroman-4-ones and thiochromen-4-ones J. Chem. Soc., Perkin Trans. 1 1982, 2, 395-402
57. Birch, H. F.; Robertson, A.; Subramaniam, T. S. Synthesis of rotenone and its derivatives. X. 6,7-Dimethoxychroman-4-one J. Chem. Soc. 1936, 1832-1834
58. Mahapatra, T.; Jana, N.; Nanda, S. Chemoenzymatic synthesis and resolution of compounds containing a quaternary stereocenters adjacent to a carbonyl group Tetrahedron: Asymmetry 2008, 19, 1224-1232
59. Tanada, Y.; Mori, K. Synthesis and absolute configuration of (-)-neuchromenin, a neurotrophic metabolite of Eupenicillium javanicum var. meloforme, and its enantiomer Eur. J. Org. Chem. 2001, 10, 1963-1966
60. Pfeiffer, P.; Haack, E.; Willems, J. Brasilin and hematoxylin question. VI. Synthesis of tetramethylanhydrohematoxylin Ber. Dtsch. Chem. Ges., Abt. B: Abhandlungen 1928, 61B, 294-299
61. Sugihara, H.; Sanno, Y. Stereoselective synthesis of cis-and trans -3-amino-4-chromanols Chem. Pharm. Bull. 1977, 25, 859-866
62. Bandaranayake, W. M.; Riggs, N. V. Anomalous acetoxylation of aromatic nuclei: some structural requirements in the substrate Aust. J. Chem. 1981, 34, 115-129
63. Paraiso, K. H. T.; Xiang, Y.; Rebecca, V. W.; Abel, E. V.; Chen, Y. A.; Munko, A. C.; Wood, E.; Fedorenko, I. V.; Sondak, V. K.; Anderson, A. R. A.; Ribas, A.; Dalla Palma, M.; Nathanson, K. L.; Koomen, J. M.; Messina, J. L.; Smalley, K. S. M. PTEN Loss Confers BRAF Inhibitor Resistance to Melanoma Cells through the Suppression of BIM Expression Cancer Res. 2011, 71, 2750-2760
64. Palakurthi, S. S.; Aktas, H.; Grubissich, L. M.; Mortensen, R. M.; Halperin, J. A. Anticancer effects of thiazolidinediones are independent of peroxisome proliferator-activated receptor gamma and mediated by inhibition of translation initiation Cancer Res. 2001, 61, 6213-6218
65. Ziegeler, G.; Ming, J.; Koseki, J. C.; Sevinc, S.; Chen, T.; Ergun, S.; Qin, X.; Aktas, B. H. Embryonic lethal abnormal vision-like HuR-dependent mRNA stability regulates post-transcriptional expression of cyclin-dependent kinase inhibitor p27Kip1 J. Biol. Chem. 2010, 285, 15408-15419