Novel N-benzoyl-2-hydroxybenzamide disrupts unique parasite secretory pathway

Antimicrobial Agents and Chemotherapy

Volumn 56, Issue 5, 2012, Pages 2666-2682

  Fomovska, Alina ^a   Huang, Qingqing ^b,h   El Bissati, Kamal ^a   Mui, Ernest J ^a   Witola, William H ^a,i   Cheng, Gang ^b   Zhou, Ying ^a   Sommerville, Caroline ^c   Roberts, Craig W ^c   Bettis, Sam ^a   Prigge, Sean T ^d   Afanador, Gustavo A ^d   Hickman, Mark R ^e   Lee, Patty J ^e   Leed, Susan E ^e   Auschwitz, Jennifer M ^e   Pieroni, Marco ^b,j   Stec, Jozef ^b   Muench, Stephen P ^f   Rice, David W ^g   Kozikowski, Alan P ^b   McLeod, Rima ^a   more..

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c UNIVERSITY OF STRATHCLYDE   (United Kingdom)

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

^e WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

^f UNIVERSITY OF LEEDS   (United Kingdom)

^g UNIVERSITY OF SHEFFIELD   (United Kingdom)

^h EAST CHINA NORMAL UNIVERSITY   (China)

ⁱ TUSKEGEE UNIVERSITY   (United States)

^j UNIVERSITY OF PARMA   (Italy)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIN 3BETA; ANTIPROTOZOAL AGENT; BENZAMIDE DERIVATIVE; CHLOROQUINE; JS 2 40; JS 2 64; MP 4 1; N BENZOYL 2 HYDROXYBENZAMIDE; P CADHERIN; PYRIMETHAMINE; QQ 421; QQ 437; SECRETORY PROTEIN; SULFADIAZINE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIPROTOZOAL ACTIVITY; ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; CONTROLLED STUDY; DRUG SYNTHESIS; FIBROBLAST CULTURE; GENOME ANALYSIS; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PARASITE; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; STRUCTURE ACTIVITY RELATION; TOXOPLASMA GONDII; TOXOPLASMOSIS;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; ANTIMALARIALS; ANTIPROTOZOAL AGENTS; BENZAMIDES; CELLS, CULTURED; FIBROBLASTS; HUMANS; INHIBITORY CONCENTRATION 50; ORGANELLES; PLASMODIUM FALCIPARUM; PROTEIN TRANSPORT; PROTOZOAN PROTEINS; QUANTITATIVE STRUCTURE-ACTIVITY RELATIONSHIP; SECRETORY PATHWAY; TOXOPLASMA;

EID: 84859805655     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.06450-11     Document Type: Article

References (59)

1. Behnke MS, et al. 2010. Coordinated progression through two subtranscriptomes underlies the tachyzoite cycle of Toxoplasma gondii. PLoS One. 25:e12354.
2. Behnke MS, et al. 2008.The transcription of bradyzoite genes in Toxoplasma gondii is controlled by autonomous promoter elements. Mol. Microbiol. 68:1502-1518. (Pubitemid 351725261)
3. Benková E, et al. 2003. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591-602. (Pubitemid 37506047)
4. Blilou I, et al. 2005. The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39-44.
5. Boehm M, Bonifacino JS. 2002. Genetic analyses of adaptin function from yeast to mammals. Gene 286:175-186. (Pubitemid 34273874)
6. Braun L, et al. 2008. Purification of Toxoplasma dense granule proteins reveals that they are in complexes throughout the secretory pathway. Mol. Biochem. Parasitol. 157:13-21. (Pubitemid 350167477)
7. Breinich MS, et al. 2009. A dynamin is required for the biogenesis of secretory organelles in Toxoplasma gondii. Curr. Biol. 19:277-286.
8. Cesbron-Delauw MF, et al. 1989. Molecular characterization of a 23-kilodalton major antigen secreted by Toxoplasma gondii. Proc. Natl. Acad. Sci. U. S. A. 86:7537-7541. (Pubitemid 19254491)
9. Cowles CR, Odorizzi G, Payne GS, Emr SD. 1997. The AP-3 adaptor complex is essential for cargo-selective transport to the yeast vacuole. Cell 91:109-118. (Pubitemid 27431317)
10. Dacks JB, Poon PP, Field MC. 2008. Phylogeny of endocytic components yields insight into the process of nonendosymbiotic organelle evolution. Proc. Natl. Acad. Sci. U. S. A. 105:588-593. (Pubitemid 351171752)
11. Dell'Angelica EC, Shotelersuk V, Aquilar RC, Gahl WA, Bonifacino JS. 1999. Altered trafficking of lysosomal proteins in Hermansky-Pudlak Syndrome due to mutations in the β3A subunit of the AP-3 adaptor. Mol. Cell 3:11-21. (Pubitemid 29292473)
12. Denny PW, Morgan GW, Field MC, Smith DF. 2005. Leishmania major: clathrin and adaptin complexes of an intra-cellular parasite. Exp. Parasitol. 109:33-37. (Pubitemid 40082594)
13. +-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell 18:715-730.
14. Dhonukshe P, et al. 2008. Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions. Nature 456:962-966.
15. Docampo R, Jimenez V, King-Keller S, Li ZH, Moreno SN. 2011. The role of acidocalcisomes in the stress response of Trypanosoma cruzi. Adv. Parasitol. 75:307-324.
16. Docampo R, Moreno SN. 2011. Acidocalcisomes. Cell Calcium 50:113-119.
17. Feraru E, et al. 2010. The AP-3 β adaptin mediates the biogenesis and function of lytic vacuoles in Arabidopsis. Plant Cell 22:2812-2824.
18. Gaji RY, Flammer HP, Carruthers VB. 2011. Forward targeting of Toxoplasma gondii proproteins to the micronemes involves conserved aliphatic amino acids. Traffic 12:840-853.
19. Geyer M, Fackler OT, Peterlin BM. 2002. Subunit H of the V-ATPase involved in endocytosis shows homology to β-adaptins. Mol. Biol. Cell 13:2045-2056. (Pubitemid 34651491)
20. Happel N, et al. 2004. Arabidopsis mu A-adaptin interacts with the tyrosine motif of the vacuolar sorting receptor VSR-PS1. Plant J. 37:678-693. (Pubitemid 38300513)
21. Hoppe HC, Ngô HM, Yang M, Joiner KA. 2000. Targeting to rhoptry organelles of Toxoplasma gondii involves evolutionarily conserved mechanisms. Nat. Cell Biol. 2:449-456.
22. Huang G, et al. 2011. Adaptor protein-3 (AP-3) complex mediates the biogenesis of acidocalcisomes and is essential for growth and virulence of Trypanosoma brucei. J. Biol. Chem. 286:36619-36630.
23. Hutson SL, et al. 2010. T. gondii RP promoters and knockdown reveal molecular pathways associated with proliferation and cell-cycle arrest. PLoS One 5:e14057.
24. Jani D, et al. 2008. HDP - a novel heme detoxification protein from the malaria parasite. PLoS Pathog. 4:1-15.
25. Johnson JD, et al. 2007. Assessment and continued validation of the malaria SYBR green I-based fluorescence assay for use in malaria drug screening. Antimicrob. Agents Chemother. 51:1926-1933. (Pubitemid 46903075)
26. Knoll LJ, Furie GL, Boothroyd JC. 2001. Adaptation of signature-tagged mutagenesis for Toxoplasma gondii: a negative screening strategy to isolate genes that are essential in restrictive growth conditions. Mol. Biochem. Parasitol. 116:11-16. (Pubitemid 32706422)
27. Larson ET, et al. 2009.Toxoplasma gondii cathepsin L is the primary target of the invasion-inhibitory compound morpholinurea-leucylhomophenyl-vinyl sulfone phenyl.J Biol Chem. 284:26839-26850.
28. Li ZH, et al. 2011. Hyperosmotic stress induces aquaporin-dependent cell shrinkage, polyphosphate synthesis, amino acid accumulation and global gene expression changes in Trypanosoma cruzi. J. Biol. Chem. 286:43959-43971.
29. Lipinski CA, Lombardo F, Dominy BW, Feeney PJ. 2001. Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv. Drug Deliv. Rev. 46:3-26. (Pubitemid 33653411)
30. Mattera R, Tsai YC, Weissman AM, Bonifacino JS. 2006. The Rab5 guanine nucleotide exchange factor Rabex-5 binds ubiquitin (Ub) and functions as a Ub ligase through an atypical Ub-interacting motif and a zinc finger domain. J. Biol. Chem. 281:6874-6883. (Pubitemid 43847623)
31. McLeod R, et al. 2001. Triclosan inhibits the growth of Plasmodium falciparum and Toxoplasma gondii by inhibition of apicomplexan Fab I. Int. J. Parasitol. 31:109-113. (Pubitemid 32181796)
32. McLeod R, et al. 2006. Outcome of treatment for congenital toxoplasmosis, 1981-2004: the National Collaborative Chicago-Based, Congenital Toxoplasmosis Study. Clin. Infect. Dis. 42:1383-1394.
33. McLeod R, et al. 2006. Severe sulfadiazine hypersensitivity in a child with reactivated congenital toxoplasmic chorioretinitis. Pediatr. Infect. Dis. J. 25:270-272. (Pubitemid 43379074)
34. Meyer DM, et al. 2005. Oligomerization and dissociation of AP-1 adaptors are regulated by cargo signals and by ArfGAP1-induced GTP hydrolysis. Mol. Biol. Cell 16:4745-4754. (Pubitemid 41416457)
35. Miranda K, et al. 2010. Characterization of a novel organelle in Toxoplasma gondii with similar composition and function to the plant vacuole. Mol. Microbiol. 76:1358-1375.
36. Mui EJ, et al. 2008. Novel triazine JPC-2067-B inhibits Toxoplasma gondii in vitro and in vivo. PLoS Negl Trop. Dis. 2:e190.
37. Nagamune K, Xiong L, Chini E, Sibley LD. 2008. Plants, endosymbionts and parasites: abscisic acid and calcium signaling. Commun. Integr. Biol. 1:62-65.
38. Nagamune K, et al. 2008. Abscisic acid controls calcium-dependent egress and development in Toxoplasma gondii. Nature 7175:207-210.
39. Nevin WD, Dacks JB. 2009. Repeated secondary loss of adaptin complex genes in the Apicomplexa. Parasitology 58:86-94.
40. Ngô HM, et al. 2003. AP-1 in Toxoplasma gondii mediates biogenesis of the rhoptry secretory organelle from a post-Golgi compartment. J. Biol. Chem. 278:5343-5352. (Pubitemid 36801050)
41. Ojo KK, et al. 2010. Toxoplasma gondii calcium-dependent protein kinase 1 is a target for selective kinase inhibitors. Nat. Struct. Mol. Biol. 5:602-607.
42. Parussini F, Coppens I, Shah PP, Diamond SL, Carruthers VB. 2010. Cathepsin L occupies a vacuolar compartment and is a protein maturase within the endo/exocytic system of Toxoplasma gondii. Mol. Microbiol. 76:1340-1357.
43. Plouffe D, et al. 2008. In silico activity profiling reveals the mechanism of action of antimalarials discovered in a high-throughput screen. Proc. Natl. Acad. Sci. U. S. A. 105:9059-9064.
44. Rathore D, Jani D, Nagarkatti R. June 2007. Novel therapeutic target for protozoal diseases. US patent 20070148185(A1).
45. Ricotta D, Hansen J, Preiss C, Teichert D, Höning S. 2008. Characterization of a protein phosphatase 2A holoenzyme that dephosphorylates the clathrin adaptors AP-1 and AP-2. J. Biol. Chem. 283:5510-5517.
46. Roberts CW, et al. 2004. Evidence for mitochondrial-derived alternative oxidase in the apicomplexan parasite Cryptosporidium parvum: a potential anti-microbial agent target. Int. J. Parasitol. 34:297-308. (Pubitemid 38299180)
47. Roberts F, et al. 1998. Evidence for the shikimate pathway in apicomplexan parasites. Nature 393:801-805. (Pubitemid 28299493)
48. Rohloff P, et al. 2011. Calcium uptake and proton transport by acidocalcisomes of Toxoplasma gondii. PLoS One 6:e18390.
49. Rojo E, Gillmor CS, Kovaleva V, Somerville CR, Raikhel NV. 2001. Vacuoleless1 is an essential gene required for vacuole formation and morphogenesis in Arabidopsis. Dev. Cell 1:303-310. (Pubitemid 33653064)
50. Samuel BU, et al. 2003. Delivery of antimicrobials into parasites. Proc. Natl. Acad. Sci. U. S. A. 100:14281-14286. (Pubitemid 37499228)
51. Sanmartín M, et al. 2007. Divergent functions of VTI12 and VTI11 in trafficking to storage and lytic vacuoles in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 104:3645-3650. (Pubitemid 46364212)
52. Somerville CR, et al. 2008. The secretory system of Arabidopsis. In Somerville CR, Meyerowitz EM (ed), The Arabidopsis book. American Society of Plant Biologists, Rockville, MD.
53. Stec J, et al. 21 February 2012, posting date. Synthesis, biological evaluation and structure-activity relationships of N-benzoyl-2-hydroxybenzamides as agents active against P. falciparum (K1 strain), trypanosomes, and Leishmania. J. Med. Chem. doi:10.1021/jm2015183.
54. Stepp JD, Huang K, Lemmon SK. 1997. The yeast adaptor protein complex, AP-3, is essential for the efficient delivery of alkaline phosphatase by the alternate pathway to the vacuole. J. Cell Biol. 139:1761-1774. (Pubitemid 28079240)
55. Sullivan WJ, Jr, Narasimhan J, Bhatti MM, Wek RC. 2004. Parasite-specific eIF2 (eukaryotic initiation factor-2) kinase required for stressinduced translation control. Biochem J. 380:523-531. (Pubitemid 38788125)
56. Surpin M, et al. 2003. The VTI family of SNARE proteins is necessary for plant viability and mediates different protein transport pathways. Plant Cell 15:2885-2899. (Pubitemid 37546258)
57. Tipparaju SK, et al. 2010. Identification and development of novel inhibitors of Toxoplasma gondii enoyl reductase. J. Med. Chem. 53:6287-6300.
58. Turetzky JM, Chu DK, Hajagos BE, Bradley PJ. 2010. Processing and secretion of ROP13: a unique Toxoplasma effector protein. Int. J. Parasitol. 40:1037-1044.
59. Vonlaufen N, Naguleswaran A, Coppens I, Sullivan WJ, Jr. 2010. MYST family lysine acetyltransferase facilitates ataxia telangiectasia mutated (ATM) kinase-mediated DNA damage response in Toxoplasma gondii. J. Biol. Chem. 28515:11154-11161.