Identification of an Atg8-Atg3 protein-protein interaction inhibitor from the medicines for malaria venture malaria box active in blood and liver stage plasmodium falciparum parasites

Journal of Medicinal Chemistry

Volumn 57, Issue 11, 2014, Pages 4521-4531

  Hain, Adelaide U P ^a   Bartee, David ^b   Sanders, Natalie G ^a   Miller, Alexia S ^a   Sullivan, David J ^a   Levitskaya, Jelena ^a   Meyers, Caren Freel ^b   Bosch, Jürgen ^a  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMALARIAL AGENT; ATG3 PROTEIN; ATG8 PROTEIN; PHOSPHATIDYLETHANOLAMINE; PROTEIN; PROTEIN INHIBITOR; UNCLASSIFIED DRUG;

APICOMPLEXA; APICOPLAST; ARTICLE; CONTROLLED STUDY; NONHUMAN; PLASMODIUM FALCIPARUM; PROTEIN LIPID INTERACTION; PROTEIN PROTEIN INTERACTION; SURFACE PLASMON RESONANCE;

ANTIMALARIALS; BINDING SITES; BLOOD; DATABASES, CHEMICAL; LIFE CYCLE STAGES; LIVER; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; PYRIDINES; THIAZOLES;

EID: 84902440363     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm401675a     Document Type: Article

References (46)

1. Phyo, A. P.; Nkhoma, S.; Stepniewska, K.; Ashley, E. A.; Nair, S.; McGready, R.; ler Moo, C.; Al-Saai, S.; Dondorp, A. M.; Lwin, K. M.; Singhasivanon, P.; Day, N. P.; White, N. J.; Anderson, T. J.; Nosten, F. Emergence of artemisinin-resistant malaria on the western border of Thailand: a longitudinal study Lancet 2012, 379, 1960-1966
2. Tarlov, A. R.; Brewer, G. J.; Carson, P. E.; Alving, A. S. Primaquine sensitivity. Glucose-6-phosphate dehydrogenase deficiency: an inborn error of metabolism of medical and biological significance Arch. Int. Med. 1962, 109, 209-234
3. Kitamura, K.; Kishi-Itakura, C.; Tsuboi, T.; Sato, S.; Kita, K.; Ohta, N.; Mizushima, N. Autophagy-related Atg8 localizes to the apicoplast of the human malaria parasite Plasmodium falciparum PLoS One 2012, 7, e42977
4. Eickel, N.; Kaiser, G.; Prado, M.; Burda, P. C.; Roelli, M.; Stanway, R. R.; Heussler, V. T. Features of autophagic cell death in Plasmodium liver-stage parasites Autophagy 2013, 9, 568-580
5. Jayabalasingham, B.; Voss, C.; Ehrenman, K.; Romano, J. D.; Smith, M. E.; Fidock, D. A.; Bosch, J.; Coppens, I. Characterization of the ATG8-conjugation system in 2 Plasmodium species with special focus on the liver stage: Possible linkage between the apicoplastic and autophagic systems? Autophagy 2014, 10, 1-16
6. Cervantes, S.; Bunnik, E. M.; Saraf, A.; Conner, C. M.; Escalante, A.; Sardiu, M. E.; Ponts, N.; Prudhomme, J.; Florens, L.; Le Roch, K. G. The multifunctional autophagy pathway in the human malaria parasite, Plasmodium falciparum Autophagy 2014, 10, 80-92
7. Yeh, E.; DeRisi, J. L. Chemical rescue of malaria parasites lacking an apicoplast defines organelle function in blood-stage Plasmodium falciparum PLoS Biol. 2011, 9, e1001138
8. Tomlins, A. M.; Ben-Rached, F.; Willams, R. A. M.; Proto, W. R.; Coppens, I.; Ruch, U.; Gilberger, T. W.; Coombs, G. H.; Mottram, J. C.; Müller, S.; Langsley, G. Plasmodium falciparum Atg8 implicated in both autophagy and apicoplast formation Autophagy 2013, 9, 1540-1552
9. Duszenko, M.; Ginger, M. L.; Brennand, A.; Gualdron-Lopez, M.; Colombo, M. I.; Coombs, G. H.; Coppens, I.; Jayabalasingham, B.; Langsley, G.; de Castro, S. L.; Menna-Barreto, R.; Mottram, J. C.; Navarro, M.; Rigden, D. J.; Romano, P. S.; Stoka, V.; Turk, B.; Michels, P. A. Autophagy in protists Autophagy 2011, 7, 127-158
10. Ichimura, Y.; Kirisako, T.; Takao, T.; Satomi, Y.; Shimonishi, Y.; Ishihara, N.; Mizushima, N.; Tanida, I.; Kominami, E.; Ohsumi, M.; Noda, T.; Ohsumi, Y. A ubiquitin-like system mediates protein lipidation Nature 2000, 408, 488-492
11. Yamaguchi, M.; Noda, N. N.; Nakatogawa, H.; Kumeta, H.; Ohsumi, Y.; Inagaki, F. Autophagy-related protein 8 (Atg8) family interacting motif in Atg3 mediates the Atg3-Atg8 interaction and is crucial for the cytoplasm-to-vacuole targeting pathway J. Biol. Chem. 2010, 285, 29599-29607
12. Walker, D. M.; Mahfooz, N.; Kemme, K. A.; Patel, V. C.; Spangler, M.; Drew, M. E. Plasmodium falciparum erythrocytic stage parasites require the putative autophagy protein PfAtg7 for normal growth PLoS One 2013, 8, e67047
13. Hain, A. U.; Weltzer, R. R.; Hammond, H.; Jayabalasingham, B.; Dinglasan, R. R.; Graham, D. R.; Colquhoun, D. R.; Coppens, I.; Bosch, J. Structural characterization and inhibition of the Plasmodium Atg8-Atg3 interaction J. Struct. Biol. 2012, 180, 551-562
14. Spangenberg, T.; Burrows, J. N.; Kowalczyk, P.; McDonald, S.; Wells, T. N.; Willis, P. The open access malaria box: a drug discovery catalyst for neglected diseases PLoS One 2013, 8, e62906
15. McGann, M. FRED and HYBRID docking performance on standardized datasets J. Comput.-Aided Mol. Des. 2012, 26, 897-906
16. Plouffe, D.; Brinker, A.; McNamara, C.; Henson, K.; Kato, N.; Kuhen, K.; Nagle, A.; Adrian, F.; Matzen, J. T.; Anderson, P.; Nam, T. G.; Gray, N. S.; Chatterjee, A.; Janes, J.; Yan, S. F.; Trager, R.; Caldwell, J. S.; Schultz, P. G.; Zhou, Y.; Winzeler, E. A. In silico activity profiling reveals the mechanism of action of antimalarials discovered in a high-throughput screen Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 9059-9064
17. Guiguemde, W. A.; Shelat, A. A.; Bouck, D.; Duffy, S.; Crowther, G. J.; Davis, P. H.; Smithson, D. C.; Connelly, M.; Clark, J.; Zhu, F.; Jimenez-Diaz, M. B.; Martinez, M. S.; Wilson, E. B.; Tripathi, A. K.; Gut, J.; Sharlow, E. R.; Bathurst, I.; El Mazouni, F.; Fowble, J. W.; Forquer, I.; McGinley, P. L.; Castro, S.; Angulo-Barturen, I.; Ferrer, S.; Rosenthal, P. J.; Derisi, J. L.; Sullivan, D. J.; Lazo, J. S.; Roos, D. S.; Riscoe, M. K.; Phillips, M. A.; Rathod, P. K.; Van Voorhis, W. C.; Avery, V. M.; Guy, R. K. Chemical genetics of Plasmodium falciparum Nature 2010, 465, 311-315
18. Derbyshire, E. R.; Prudencio, M.; Mota, M. M.; Clardy, J. Liver-stage malaria parasites vulnerable to diverse chemical scaffolds Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 8511-8516
19. Meister, S.; Plouffe, D. M.; Kuhen, K. L.; Bonamy, G. M.; Wu, T.; Barnes, S. W.; Bopp, S. E.; Borboa, R.; Bright, A. T.; Che, J.; Cohen, S.; Dharia, N. V.; Gagaring, K.; Gettayacamin, M.; Gordon, P.; Groessl, T.; Kato, N.; Lee, M. C.; McNamara, C. W.; Fidock, D. A.; Nagle, A.; Nam, T. G.; Richmond, W.; Roland, J.; Rottmann, M.; Zhou, B.; Froissard, P.; Glynne, R. J.; Mazier, D.; Sattabongkot, J.; Schultz, P. G.; Tuntland, T.; Walker, J. R.; Zhou, Y.; Chatterjee, A.; Diagana, T. T.; Winzeler, E. A. Imaging of Plasmodium liver stages to drive next-generation antimalarial drug discovery Science 2011, 334, 1372-1377
20. Ma, J.; Trop, S.; Baer, S.; Rakhmanaliev, E.; Arany, Z.; Dumoulin, P.; Zhang, H.; Romano, J.; Coppens, I.; Levitsky, V.; Levitskaya, J. Dynamics of the major histocompatibility complex class I processing and presentation pathway in the course of malaria parasite development in human hepatocytes: implications for vaccine development PLoS One 2013, 8, e75321
21. Sattabongkot, J.; Yimamnuaychoke, N.; Leelaudomlipi, S.; Rasameesoraj, M.; Jenwithisuk, R.; Coleman, R. E.; Udomsangpetch, R.; Cui, L.; Brewer, T. G. Establishment of a human hepatocyte line that supports in vitro development of the exo-erythrocytic stages of the malaria parasites Plasmodium falciparum and P. vivax Am. J. Trop. Med. Hyg. 2006, 74, 708-715 (Pubitemid 46774383)
22. Lim, P. L.; Tan, W.; Latchoumycandane, C.; Mok, W. C.; Khoo, Y. M.; Lee, H. S.; Sattabongkot, J.; Beerheide, W.; Lim, S. G.; Tan, T. M.; Boelsterli, U. A. Molecular and functional characterization of drug-metabolizing enzymes and transporter expression in the novel spontaneously immortalized human hepatocyte line HC-04 Toxicol. In Vitro 2007, 21, 1390-1401 (Pubitemid 350086855)
23. Talman, A. M.; Blagborough, A. M.; Sinden, R. E. A Plasmodium falciparum strain expressing GFP throughout the parasite's life-cycle PLoS One 2010, 5, e9156
24. Jiang, Y. L.; Krosky, D. J.; Seiple, L.; Stivers, J. T. Uracil-directed ligand tethering: an efficient strategy for uracil DNA glycosylase (UNG) inhibitor development J. Am. Chem. Soc. 2005, 127, 17412-17420 (Pubitemid 41791060)
25. Bennett, T. N.; Paguio, M.; Gligorijevic, B.; Seudieu, C.; Kosar, A. D.; Davidson, E.; Roepe, P. Novel, rapid, and inexpensive cell-based quantification of antimalarial drug efficacy Antimicrob. Agents Chemother. 2004, 48, 1807-1810 (Pubitemid 38544393)
26. Mullard, A. Protein-protein interaction inhibitors get into the groove Nat. Rev. Drug Discovery 2012, 11, 173-175
27. Zimmermann, G.; Papke, B.; Ismail, S.; Vartak, N.; Chandra, A.; Hoffmann, M.; Hahn, S. A.; Triola, G.; Wittinghofer, A.; Bastiaens, P. I.; Waldmann, H. Small molecule inhibition of the KRAS-PDEdelta interaction impairs oncogenic KRAS signalling Nature 2013, 497, 638-642
28. Semba, C. P.; Torkildsen, G. L.; Lonsdale, J. D.; McLaurin, E. B.; Geffin, J. A.; Mundorf, T. K.; Kennedy, K. S.; Ousler, G. W. A phase 2 randomized, double-masked, placebo-controlled study of a novel integrin antagonist (SAR 1118) for the treatment of dry eye Am. J. Ophthalmol. 2012, 153, 1050-1060
29. Hain, A. U. P.; Bosch, J. Autophagy in Plasmodium, a multifunctional pathway? Comput. Struct. Biotechnol. J. 2013, 8, 1-9
30. Huang, W. P.; Scott, S. V.; Kim, J.; Klionsky, D. J. The itinerary of a vesicle component, Aut7p/Cvt5p, terminates in the yeast vacuole via the autophagy/Cvt pathways J. Biol. Chem. 2000, 275, 5845-5851 (Pubitemid 30115231)
31. Kirisako, T.; Baba, M.; Ishihara, N.; Miyazawa, K.; Ohsumi, M.; Yoshimori, T.; Noda, T.; Ohsumi, Y. Formation process of autophagosome is traced with Apg8/Aut7p in yeast J. Cell. Biol. 1999, 147, 435-446 (Pubitemid 29496349)
32. McNamara, C. W.; Lee, M. C.; Lim, C. S.; Lim, S. H.; Roland, J.; Nagle, A.; Simon, O.; Yeung, B. K.; Chatterjee, A. K.; McCormack, S. L.; Manary, M. J.; Zeeman, A. M.; Dechering, K. J.; Kumar, T. R.; Henrich, P. P.; Gagaring, K.; Ibanez, M.; Kato, N.; Kuhen, K. L.; Fischli, C.; Rottmann, M.; Plouffe, D. M.; Bursulaya, B.; Meister, S.; Rameh, L.; Trappe, J.; Haasen, D.; Timmerman, M.; Sauerwein, R. W.; Suwanarusk, R.; Russell, B.; Renia, L.; Nosten, F.; Tully, D. C.; Kocken, C. H.; Glynne, R. J.; Bodenreider, C.; Fidock, D. A.; Diagana, T. T.; Winzeler, E. A. Targeting Plasmodium PI(4)K to eliminate malaria Nature 2013, 504, 248-253
33. May, P. C.; Dean, R. A.; Lowe, S. L.; Martenyi, F.; Sheehan, S. M.; Boggs, L. N.; Monk, S. A.; Mathes, B. M.; Mergott, D. J.; Watson, B. M.; Stout, S. L.; Timm, D. E.; Smith Labell, E.; Gonzales, C. R.; Nakano, M.; Jhee, S. S.; Yen, M.; Ereshefsky, L.; Lindstrom, T. D.; Calligaro, D. O.; Cocke, P. J.; Greg Hall, D.; Friedrich, S.; Citron, M.; Audia, J. E. Robust central reduction of amyloid-β in humans with an orally available, non-peptidic β-secretase inhibitor J. Neurosci. 2011, 31, 16507-16516
34. Townsend, K. N.; Hughson, L. R.; Schlie, K.; Poon, V. I.; Westerback, A.; Lum, J. J. Autophagy inhibition in cancer therapy: metabolic considerations for antitumor immunity Immunol. Rev. 2012, 249, 176-194
35. Ho, K. H.; Chang, H. E.; Huang, W. P. Mutation at the cargo-receptor binding site of Atg8 also affects its general autophagy regulation function Autophagy 2009, 5, 461-471
36. Noda, N. N.; Ohsumi, Y.; Inagaki, F. Atg8-family interacting motif crucial for selective autophagy FEBS Lett. 2010, 584, 1379-1385
37. Tung, Y. T.; Hsu, W. M.; Lee, H.; Huang, W. P.; Liao, Y. F. The evolutionarily conserved interaction between LC3 and p62 selectively mediates autophagy-dependent degradation of mutant huntingtin Cell. Mol. Neurobiol. 2010, 30, 795-806
38. Thielmann, Y.; Weiergräber, O. H.; Mohrlüder, J.; Willbold, D. Structural framework of the GABARAP-calreticulin interface - implications for substrate binding to endoplasmic reticulum chaperones FEBS J. 2009, 276, 1140-1152
39. Trager, W.; Jensen, J. B. Human malaria parasites in continuous culture Science 1976, 193, 673-675
40. Gaviria, D.; Paguio, M. F.; Turnbull, L. B.; Tan, A.; Siriwardana, A.; Ghosh, D.; Ferdig, M. T.; Sinai, A. P.; Roepe, P. D. A Process Similar to Autophagy Is Associated with Cytocidal Chloroquine Resistance in Plasmodium falciparum PLoS One 2013, 8, e79059
41. Abramoff, M. D.; Magalhaes, P. J.; Ram, S. J. Image Processing with ImageJ Biophotonics Int. 2004, 11, 36-42
42. Hawkins, P. C.; Skillman, A. G.; Warren, G. L.; Ellingson, B. A.; Stahl, M. T. Conformer generation with OMEGA: algorithm and validation using high quality structures from the Protein Databank and Cambridge Structural Database J. Chem. Inf. Model. 2010, 50, 572-584
43. Hawkins, P. C.; Nicholls, A. Conformer generation with OMEGA: learning from the data set and the analysis of failures J. Chem. Inf. Model. 2012, 52, 2919-2936
44. Roy, A.; Kucukural, A.; Zhang, Y. I-TASSER: a unified platform for automated protein structure and function prediction Nat. Protoc. 2010, 5, 725-738
45. Aurrecoechea, C.; Brestelli, J.; Brunk, B. P.; Dommer, J.; Fischer, S.; Gajria, B.; Gao, X.; Gingle, A.; Grant, G.; Harb, O. S.; Heiges, M.; Innamorato, F.; Iodice, J.; Kissinger, J. C.; Kraemer, E.; Li, W.; Miller, J. A.; Nayak, V.; Pennington, C.; Pinney, D. F.; Roos, D. S.; Ross, C.; Stoeckert, C. J., Jr.; Treatman, C.; Wang, H. PlasmoDB: a functional genomic database for malaria parasites Nucleic Acids Res. 2009, 37, D539-543
46. Hawkins, P. C.; Skillman, A. G.; Nicholls, A. Comparison of shape-matching and docking as virtual screening tools J. Med. Chem. 2007, 50, 74-82 (Pubitemid 46105500)