{
"METABOLOMICS WORKBENCH":{"STUDY_ID":"ST001175","ANALYSIS_ID":"AN001950","VERSION":"1","CREATED_ON":"April 30, 2019, 6:31 pm"},

"PROJECT":{"PROJECT_TITLE":"Multi-omics analysis demonstrates unique mode of action of a potent new antimalarial compound, JPC-3210, against Plasmodium falciparum","PROJECT_SUMMARY":"The increasing incidence of antimalarial drug resistance to the first-line artemisinins, and their combination partner drugs, underpins an urgent need for new antimalarial drugs, ideally with a novel mechanism of action. The recently developed 2-aminomethylphenol, JPC-3210, (MMV 892646) is an erythrocytic schizonticide with potent in vitro antimalarial activity against multidrug-resistant Plasmodium falciparum, low cytotoxicity, potent in vivo efficacy against murine malaria, and favourable preclinical pharmacokinetics, including a lengthy plasma elimination half-life. This study demonstrates the application of a “multi-omics” workflow based on high resolution orbitrap mass spectrometry to investigate the impact of JPC-3210 on biochemical pathways within P. falciparum infected red blood cells. Metabolomics and peptidomics analysis revealed a perturbation in hemoglobin metabolism following JPC-3210 exposure. The metabolomics data demonstrated a depletion in short hemoglobin-derived peptides, while peptidomics analysis showed a depletion in longer hemoglobin-derived peptides. In order to further elucidate the mechanism responsible for inhibition of hemoglobin metabolism, we used in vitro β-hematin polymerisation assays and showed JPC-3210 to be an intermediate inhibitor of β-hematin polymerisation, about 10-fold less potent then the quinoline antimalarials. Furthermore, quantitative proteomics analysis showed that JPC-3210 treatment results in a distinct proteomic signature in comparison to other known antimalarials. Whilst JPC-3210 clustered closely with mefloquine in the metabolomics and proteomics analyses, a key differentiating signature for JPC-3210 was the significant enrichment of parasite proteins involved in regulation of translation. In conclusion, multi-omics studies using high resolution mass spectrometry revealed JPC-3210 to possess a unique mechanism of action involving inhibition of hemoglobin digestion, depletion of DNA replication and synthesis proteins, and elevation of regulators of protein translation. Importantly, this mechanism is distinct from currently-used antimalarials, suggesting that JPC-3210 warrants further investigation as a potentially useful new antimalarial agent.","INSTITUTE":"Monash University","LAST_NAME":"Siddiqui","FIRST_NAME":"Ghizal","ADDRESS":"381 Royal Parade, Parkville","EMAIL":"ghizal.siddiqui@monash.edu","PHONE":"99039282"},

"STUDY":{"STUDY_TITLE":"Multi-omics analysis demonstrates unique mode of action of a potent new antimalarial compound, JPC-3210, against Plasmodium falciparum","STUDY_SUMMARY":"The increasing incidence of antimalarial drug resistance to the first-line artemisinins, and their combination partner drugs, underpins an urgent need for new antimalarial drugs, ideally with a novel mechanism of action. The recently developed 2-aminomethylphenol, JPC-3210, (MMV 892646) is an erythrocytic schizonticide with potent in vitro antimalarial activity against multidrug-resistant Plasmodium falciparum, low cytotoxicity, potent in vivo efficacy against murine malaria, and favourable preclinical pharmacokinetics, including a lengthy plasma elimination half-life. This study demonstrates the application of a “multi-omics” workflow based on high resolution orbitrap mass spectrometry to investigate the impact of JPC-3210 on biochemical pathways within P. falciparum infected red blood cells. Metabolomics and peptidomics analysis revealed a perturbation in hemoglobin metabolism following JPC-3210 exposure. The metabolomics data demonstrated a depletion in short hemoglobin-derived peptides, while peptidomics analysis showed a depletion in longer hemoglobin-derived peptides. In order to further elucidate the mechanism responsible for inhibition of hemoglobin metabolism, we used in vitro β-hematin polymerisation assays and showed JPC-3210 to be an intermediate inhibitor of β-hematin polymerisation, about 10-fold less potent then the quinoline antimalarials. Furthermore, quantitative proteomics analysis showed that JPC-3210 treatment results in a distinct proteomic signature in comparison to other known antimalarials. Whilst JPC-3210 clustered closely with mefloquine in the metabolomics and proteomics analyses, a key differentiating signature for JPC-3210 was the significant enrichment of parasite proteins involved in regulation of translation. In conclusion, multi-omics studies using high resolution mass spectrometry revealed JPC-3210 to possess a unique mechanism of action involving inhibition of hemoglobin digestion, depletion of DNA replication and synthesis proteins, and elevation of regulators of protein translation. Importantly, this mechanism is distinct from currently-used antimalarials, suggesting that JPC-3210 warrants further investigation as a potentially useful new antimalarial agent.","INSTITUTE":"Monash University","LAST_NAME":"Siddiqui","FIRST_NAME":"Ghizal","ADDRESS":"381 Royal Parade, Parkville","EMAIL":"ghizal.siddiqui@monash.edu","PHONE":"99039282"},

"SUBJECT":{"SUBJECT_TYPE":"Other","SUBJECT_SPECIES":"Plasmodium falciparum","TAXONOMY_ID":"5833"},
"SUBJECT_SAMPLE_FACTORS":[
{
"Subject ID":"-",
"Sample ID":"Blank_1",
"Factors":{"Condition":"Blank"},
"Additional sample data":{"Replicates":"1"}
},
{
"Subject ID":"-",
"Sample ID":"Blank_2",
"Factors":{"Condition":"Blank"},
"Additional sample data":{"Replicates":"2"}
},
{
"Subject ID":"-",
"Sample ID":"Blank_3",
"Factors":{"Condition":"Blank"},
"Additional sample data":{"Replicates":"3"}
},
{
"Subject ID":"-",
"Sample ID":"Blank_4",
"Factors":{"Condition":"Blank"},
"Additional sample data":{"Replicates":"4"}
},
{
"Subject ID":"-",
"Sample ID":"Blank_5",
"Factors":{"Condition":"Blank"},
"Additional sample data":{"Replicates":"5"}
},
{
"Subject ID":"-",
"Sample ID":"Blank_6",
"Factors":{"Condition":"Blank"},
"Additional sample data":{"Replicates":"6"}
},
{
"Subject ID":"-",
"Sample ID":"P_Aqm_1",
"Factors":{"Condition":"Aqm treated"},
"Additional sample data":{"Replicates":"1"}
},
{
"Subject ID":"-",
"Sample ID":"P_Aqm_2",
"Factors":{"Condition":"Aqm treated"},
"Additional sample data":{"Replicates":"2"}
},
{
"Subject ID":"-",
"Sample ID":"P_Aqm_3",
"Factors":{"Condition":"Aqm treated"},
"Additional sample data":{"Replicates":"3"}
},
{
"Subject ID":"-",
"Sample ID":"P_Aqm_4",
"Factors":{"Condition":"Aqm treated"},
"Additional sample data":{"Replicates":"4"}
},
{
"Subject ID":"-",
"Sample ID":"P_Atov_1",
"Factors":{"Condition":"Atov treated"},
"Additional sample data":{"Replicates":"1"}
},
{
"Subject ID":"-",
"Sample ID":"P_Atov_2",
"Factors":{"Condition":"Atov treated"},
"Additional sample data":{"Replicates":"2"}
},
{
"Subject ID":"-",
"Sample ID":"P_Atov_3",
"Factors":{"Condition":"Atov treated"},
"Additional sample data":{"Replicates":"3"}
},
{
"Subject ID":"-",
"Sample ID":"P_Atov_4",
"Factors":{"Condition":"Atov treated"},
"Additional sample data":{"Replicates":"4"}
},
{
"Subject ID":"-",
"Sample ID":"P_CQ_1",
"Factors":{"Condition":"CQ treated"},
"Additional sample data":{"Replicates":"1"}
},
{
"Subject ID":"-",
"Sample ID":"P_CQ_2",
"Factors":{"Condition":"CQ treated"},
"Additional sample data":{"Replicates":"2"}
},
{
"Subject ID":"-",
"Sample ID":"P_CQ_3",
"Factors":{"Condition":"CQ treated"},
"Additional sample data":{"Replicates":"3"}
},
{
"Subject ID":"-",
"Sample ID":"P_CQ_4",
"Factors":{"Condition":"CQ treated"},
"Additional sample data":{"Replicates":"4"}
},
{
"Subject ID":"-",
"Sample ID":"P_DHA_1",
"Factors":{"Condition":"DHA treated"},
"Additional sample data":{"Replicates":"1"}
},
{
"Subject ID":"-",
"Sample ID":"P_DHA_2",
"Factors":{"Condition":"DHA treated"},
"Additional sample data":{"Replicates":"2"}
},
{
"Subject ID":"-",
"Sample ID":"P_DHA_3",
"Factors":{"Condition":"DHA treated"},
"Additional sample data":{"Replicates":"3"}
},
{
"Subject ID":"-",
"Sample ID":"P_DHA_4",
"Factors":{"Condition":"DHA treated"},
"Additional sample data":{"Replicates":"4"}
},
{
"Subject ID":"-",
"Sample ID":"P_DMSO_2",
"Factors":{"Condition":"DMSO treated"},
"Additional sample data":{"Replicates":"1"}
},
{
"Subject ID":"-",
"Sample ID":"P_DMSO_3",
"Factors":{"Condition":"DMSO treated"},
"Additional sample data":{"Replicates":"2"}
},
{
"Subject ID":"-",
"Sample ID":"P_DMSO_4",
"Factors":{"Condition":"DMSO treated"},
"Additional sample data":{"Replicates":"3"}
},
{
"Subject ID":"-",
"Sample ID":"P_DMSO_5",
"Factors":{"Condition":"DMSO treated"},
"Additional sample data":{"Replicates":"4"}
},
{
"Subject ID":"-",
"Sample ID":"P_DMSO_6",
"Factors":{"Condition":"DMSO treated"},
"Additional sample data":{"Replicates":"5"}
},
{
"Subject ID":"-",
"Sample ID":"P_DMSO_7",
"Factors":{"Condition":"DMSO treated"},
"Additional sample data":{"Replicates":"6"}
},
{
"Subject ID":"-",
"Sample ID":"P_DMSO_8",
"Factors":{"Condition":"DMSO treated"},
"Additional sample data":{"Replicates":"7"}
},
{
"Subject ID":"-",
"Sample ID":"P_JPC_1",
"Factors":{"Condition":"JPC treated"},
"Additional sample data":{"Replicates":"1"}
},
{
"Subject ID":"-",
"Sample ID":"P_JPC_2",
"Factors":{"Condition":"JPC treated"},
"Additional sample data":{"Replicates":"2"}
},
{
"Subject ID":"-",
"Sample ID":"P_JPC_3",
"Factors":{"Condition":"JPC treated"},
"Additional sample data":{"Replicates":"3"}
},
{
"Subject ID":"-",
"Sample ID":"P_MQ_1",
"Factors":{"Condition":"MQ treated"},
"Additional sample data":{"Replicates":"1"}
},
{
"Subject ID":"-",
"Sample ID":"P_MQ_2",
"Factors":{"Condition":"MQ treated"},
"Additional sample data":{"Replicates":"2"}
},
{
"Subject ID":"-",
"Sample ID":"P_MQ_3",
"Factors":{"Condition":"MQ treated"},
"Additional sample data":{"Replicates":"3"}
},
{
"Subject ID":"-",
"Sample ID":"P_MQ_4",
"Factors":{"Condition":"MQ treated"},
"Additional sample data":{"Replicates":"4"}
},
{
"Subject ID":"-",
"Sample ID":"P_PYN_1",
"Factors":{"Condition":"PYN treated"},
"Additional sample data":{"Replicates":"1"}
},
{
"Subject ID":"-",
"Sample ID":"P_PYN_2",
"Factors":{"Condition":"PYN treated"},
"Additional sample data":{"Replicates":"2"}
},
{
"Subject ID":"-",
"Sample ID":"P_PYN_3",
"Factors":{"Condition":"PYN treated"},
"Additional sample data":{"Replicates":"3"}
},
{
"Subject ID":"-",
"Sample ID":"P_PYN_4",
"Factors":{"Condition":"PYN treated"},
"Additional sample data":{"Replicates":"4"}
},
{
"Subject ID":"-",
"Sample ID":"P_TQ_1",
"Factors":{"Condition":"TQ treated"},
"Additional sample data":{"Replicates":"1"}
},
{
"Subject ID":"-",
"Sample ID":"P_TQ_2",
"Factors":{"Condition":"TQ treated"},
"Additional sample data":{"Replicates":"2"}
},
{
"Subject ID":"-",
"Sample ID":"P_TQ_3",
"Factors":{"Condition":"TQ treated"},
"Additional sample data":{"Replicates":"3"}
},
{
"Subject ID":"-",
"Sample ID":"P_TQ_4",
"Factors":{"Condition":"TQ treated"},
"Additional sample data":{"Replicates":"4"}
},
{
"Subject ID":"-",
"Sample ID":"QC_P_1",
"Factors":{"Condition":"QC"},
"Additional sample data":{"Replicates":"1"}
},
{
"Subject ID":"-",
"Sample ID":"QC_P_2",
"Factors":{"Condition":"QC"},
"Additional sample data":{"Replicates":"2"}
},
{
"Subject ID":"-",
"Sample ID":"QC_P_3",
"Factors":{"Condition":"QC"},
"Additional sample data":{"Replicates":"3"}
},
{
"Subject ID":"-",
"Sample ID":"QC_P_4",
"Factors":{"Condition":"QC"},
"Additional sample data":{"Replicates":"4"}
},
{
"Subject ID":"-",
"Sample ID":"QC_P_5",
"Factors":{"Condition":"QC"},
"Additional sample data":{"Replicates":"5"}
},
{
"Subject ID":"-",
"Sample ID":"QC_P_6",
"Factors":{"Condition":"QC"},
"Additional sample data":{"Replicates":"6"}
},
{
"Subject ID":"-",
"Sample ID":"P_LF_1",
"Factors":{"Condition":"LF treated"},
"Additional sample data":{"Replicates":"1"}
},
{
"Subject ID":"-",
"Sample ID":"P_LF_2",
"Factors":{"Condition":"LF treated"},
"Additional sample data":{"Replicates":"2"}
},
{
"Subject ID":"-",
"Sample ID":"P_LF_3",
"Factors":{"Condition":"LF treated"},
"Additional sample data":{"Replicates":"3"}
},
{
"Subject ID":"-",
"Sample ID":"P_LF_4",
"Factors":{"Condition":"LF treated"},
"Additional sample data":{"Replicates":"4"}
}
],
"COLLECTION":{"COLLECTION_SUMMARY":"Plasmodium falciparum infected red blood cells treated with different drugs were counted washed and metabolites extracted used 100% methanol","SAMPLE_TYPE":"Plasmodium cells"},

"TREATMENT":{"TREATMENT_SUMMARY":"The metabolism of mid-trophozoite stage parasites (24-28 h post invasion) in response to treatment with a panel of antimalarial compounds was investigated. Cultures (200 μl) were adjusted to 8% parasitemia and 2% hematocrit before being exposed to test compounds; JPC-3210, AQm, PYN, ATQ, DHA, CQ, MQ, LF and TQ (1 μM) for 1 h in a flat bottom 96 well plate. At least three replicates of each compound and seven replicates of an untreated control which contained an equivalent volume of DMSO vehicle (0.01% final concentration) were analysed."},

"SAMPLEPREP":{"SAMPLEPREP_SUMMARY":"Following drug incubation, metabolites were extracted as detailed. In short, after incubation with drug, culture medium was aspirated from each well, and the metabolism of infected red blood cells (iRBCs) was quenched by the addition of ice-cold phosphate-buffered saline (PBS). Cells were pelleted by centrifugation for 5 min at 1,000 × g, and the PBS supernatant was removed prior to the addition of 135 μL ice cold methanol (containing the internal standard compounds; CHAPS (3-[(3-cholamidopropyl)-dimethylammonio]-1-propanesulfonate), CAPS [N-cyclohexyl-3-aminopropane-sulfonic acid], and PIPES [piperazine-N,N′-bis(2-ethanesulfonic acid)]). Samples were rapidly mixed by pipetting three times to extract iRBC metabolites. Samples were left on ice with gentle agitation for 60 min and then centrifuged at 3,000 × g to remove insoluble material. Supernatants were transferred to glass high-performance liquid chromatography (HPLC) vials and stored at −80°C until analysis. An aliquot (10 μL) of each sample was combined to generate a pooled biological quality control (PBQC) sample, which was used to monitor downstream sample stability and analytical reproducibility."},

"CHROMATOGRAPHY":{"CHROMATOGRAPHY_SUMMARY":"Briefly, samples (10 μL) were injected onto a Dionex RSLC U3000 LC system (Thermo) fitted with a ZIC-pHILIC column (5 μm particle size, 4.6 by 150 mm; Merck) and 20 mM ammonium carbonate (A) and acetonitrile (B) were used as the mobile phases. A 30 min gradient starting from 80% B to 40% B over 20 min, followed by washing at 5% B for 3 min and re-equilibration at 80% B, was used.","CHROMATOGRAPHY_TYPE":"HILIC","INSTRUMENT_NAME":"Thermo Dionex Ultimate 3000","COLUMN_NAME":"ZIC-pHILIC column (5 µm particle size, 4.6 by 150 mm; Merck)"},

"ANALYSIS":{"ANALYSIS_TYPE":"MS"},

"MS":{"INSTRUMENT_NAME":"Thermo Q Exactive Orbitrap","INSTRUMENT_TYPE":"Orbitrap","MS_TYPE":"ESI","ION_MODE":"POSITIVE","MS_COMMENTS":"-"},

"MS_METABOLITE_DATA":{
"Units":"Signal Intensity",

"Data":[{"Metabolite":"Adenosine","P_Aqm_1":"124545","P_Aqm_2":"135396","P_Aqm_3":"175120","P_Aqm_4":"111348","P_Atov_1":"238839","P_Atov_2":"210124","P_Atov_3":"172604","P_Atov_4":"131988","Blank_1":"0","Blank_2":"0","Blank_3":"0","Blank_4":"30117","Blank_5":"0","Blank_6":"0","P_CQ_1":"182814","P_CQ_2":"154569","P_CQ_3":"141795","P_CQ_4":"143204","P_DHA_1":"134075","P_DHA_2":"123419","P_DHA_3":"188746","P_DHA_4":"134677","P_DMSO_2":"154845","P_DMSO_3":"213957","P_DMSO_4":"156618","P_DMSO_5":"129763","P_DMSO_6":"203802","P_DMSO_7":"153668","P_DMSO_8":"170200","P_JPC_1":"153910","P_JPC_2":"97997","P_JPC_3":"83646","P_LF_1":"137331","P_LF_2":"141757","P_LF_3":"110178","P_LF_4":"171676","P_MQ_1":"149389","P_MQ_2":"174721","P_MQ_4":"137145","P_PYN_1":"215840","P_PYN_2":"119797","P_PYN_3":"89944","P_PYN_4":"156919","QC_P_1":"177378","QC_P_2":"258950","QC_P_3":"270758","QC_P_4":"194691","QC_P_5":"193977","QC_P_6":"210238","P_TQ_1":"172025","P_TQ_2":"175413","P_TQ_3":"140486","P_TQ_4":"132541","":""},{"Metabolite":"ADP","P_Aqm_1":"226703","P_Aqm_2":"530441","P_Aqm_3":"209339","P_Aqm_4":"584539","P_Atov_1":"217819","P_Atov_2":"360513","P_Atov_3":"526205","P_Atov_4":"877995","Blank_1":"0","Blank_2":"0","Blank_3":"0","Blank_4":"0","Blank_5":"0","Blank_6":"0","P_CQ_1":"389577","P_CQ_2":"445716","P_CQ_3":"600264","P_CQ_4":"233441","P_DHA_1":"306599","P_DHA_2":"219503","P_DHA_3":"269325","P_DHA_4":"228149","P_DMSO_2":"381389","P_DMSO_3":"540433","P_DMSO_4":"423275","P_DMSO_5":"284718","P_DMSO_6":"346160","P_DMSO_7":"317512","P_DMSO_8":"331591","P_JPC_1":"315750","P_JPC_2":"177723","P_JPC_3":"457238","P_LF_1":"272385","P_LF_2":"663817","P_LF_3":"264099","P_LF_4":"232367","P_MQ_1":"293559","P_MQ_2":"388678","P_MQ_4":"318485","P_PYN_1":"287750","P_PYN_2":"174719","P_PYN_3":"170066","P_PYN_4":"303137","QC_P_1":"728247","QC_P_2":"1229069","QC_P_3":"1210494","QC_P_4":"1058508","QC_P_5":"1074476","QC_P_6":"1152579","P_TQ_1":"244312","P_TQ_2":"245540","P_TQ_3":"195843","P_TQ_4":"289430","":""},{"Metabolite":"5-[2H-Pyrrol-4-(3H)-ylidenemethyl]-2-furanmethanol","P_Aqm_1":"137031","P_Aqm_2":"174850","P_Aqm_3":"268934","P_Aqm_4":"164056","P_Atov_1":"358459","P_Atov_2":"286096","P_Atov_3":"295762","P_Atov_4":"302831","Blank_1":"0","Blank_2":"0","Blank_3":"0","Blank_4":"0","Blank_5":"0","Blank_6":"0","P_CQ_1":"266227","P_CQ_2":"172928","P_CQ_3":"217916","P_CQ_4":"382827","P_DHA_1":"234328","P_DHA_2":"242041","P_DHA_3":"319326","P_DHA_4":"290339","P_DMSO_2":"268711","P_DMSO_3":"178454","P_DMSO_4":"197487","P_DMSO_5":"229058","P_DMSO_6":"245115","P_DMSO_7":"289724","P_DMSO_8":"304376","P_JPC_1":"193598","P_JPC_2":"213579","P_JPC_3":"271304","P_LF_1":"262429","P_LF_2":"193900","P_LF_3":"127747","P_LF_4":"268417","P_MQ_1":"82675","P_MQ_2":"96678","P_MQ_4":"264312","P_PYN_1":"98646","P_PYN_2":"172869","P_PYN_3":"148432","P_PYN_4":"245199","QC_P_1":"254175","QC_P_2":"361468","QC_P_3":"269999","QC_P_4":"253334","QC_P_5":"362625","QC_P_6":"287513","P_TQ_1":"400464","P_TQ_2":"274478","P_TQ_3":"258082","P_TQ_4":"191178","":""},{"Metabolite":"Nicotinamide 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}

}