{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,9]],"date-time":"2026-10-09T11:43:11Z","timestamp":1791546191422,"version":"4.3.4"},"reference-count":70,"publisher":"American Chemical Society (ACS)","issue":"21","license":[{"start":{"date-parts":[[2015,10,9]],"date-time":"2015-10-09T00:00:00Z","timestamp":1444348800000},"content-version":"vor","delay-in-days":365,"URL":"https:\/\/pubs.acs.org\/page\/policy\/authorchoice_termsofuse.html"}],"funder":[{"DOI":"10.13039\/501100000923","name":"Australian Research Council","doi-asserted-by":"publisher","award":["FT100100690"],"award-info":[{"award-number":["FT100100690"]}],"id":[{"id":"10.13039\/501100000923","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000923","name":"Australian Research Council","doi-asserted-by":"publisher","award":["LP120200557"],"award-info":[{"award-number":["LP120200557"]}],"id":[{"id":"10.13039\/501100000923","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000925","name":"National Health and Medical Research Council","doi-asserted-by":"publisher","award":["1063786"],"award-info":[{"award-number":["1063786"]}],"id":[{"id":"10.13039\/501100000925","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2014,11,13]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Plasmodium parasites, the causative agents of malaria, have developed resistance to most of our current antimalarial therapies, including artemisinin combination therapies which are widely described as our last line of defense. Antimalarial agents with a novel mode of action are urgently required. Two Plasmodium falciparum aminopeptidases, PfA-M1 and PfA-M17, play crucial roles in the erythrocytic stage of infection and have been validated as potential antimalarial targets. Using compound-bound crystal structures of both enzymes, we have used a structure-guided approach to develop a novel series of inhibitors capable of potent inhibition of both PfA-M1 and PfA-M17 activity and parasite growth in culture. Herein we describe the design, synthesis, and evaluation of a series of hydroxamic acid-based inhibitors and demonstrate the compounds to be exciting new leads for the development of novel antimalarial therapeutics.<\/jats:p>","DOI":"10.1021\/jm501323a","type":"journal-article","created":{"date-parts":[[2014,10,9]],"date-time":"2014-10-09T10:58:40Z","timestamp":1412852320000},"page":"9168-9183","source":"Crossref","is-referenced-by-count":67,"title":["Two-Pronged Attack: Dual Inhibition\nof\n                    <i>Plasmodium falciparum<\/i>\n                    M1 and M17\nMetalloaminopeptidases\nby a Novel Series of Hydroxamic Acid-Based Inhibitors"],"prefix":"10.1021","volume":"57","author":[{"given":"Shailesh N.","family":"Mistry","sequence":"first","affiliation":[{"name":"Monash University , , , ,","place":["Parkville, Victoria, Australia, 3052"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nyssa","family":"Drinkwater","sequence":"additional","affiliation":[{"name":"Monash University , , , ,","place":["Clayton, Victoria, Australia, 3800"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chiara","family":"Ruggeri","sequence":"additional","affiliation":[{"name":"Monash University , , , ,","place":["Clayton, Victoria, Australia, 3800"]},{"name":"Sapienza Universita di Roma , , ,","place":["Roma, Italy, 00185"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Komagal Kannan","family":"Sivaraman","sequence":"additional","affiliation":[{"name":"Monash University , , , ,","place":["Clayton, Victoria, Australia, 3800"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sasdekumar","family":"Loganathan","sequence":"additional","affiliation":[{"name":"Griffith University , , , ,","place":["Nathan, Queensland, Australia, 4111"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sabine","family":"Fletcher","sequence":"additional","affiliation":[{"name":"Griffith University , , , ,","place":["Nathan, Queensland, Australia, 4111"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marcin","family":"Drag","sequence":"additional","affiliation":[{"name":"Wroclaw University of Technology , , Wyb. Wyspianskiego 27 , ,","place":["Wroclaw, Poland, 50-370"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alessandro","family":"Paiardini","sequence":"additional","affiliation":[{"name":"Sapienza Universita di Roma , , ,","place":["Roma, Italy, 00185"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vicky M.","family":"Avery","sequence":"additional","affiliation":[{"name":"Griffith University , , , ,","place":["Nathan, Queensland, Australia, 4111"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peter J.","family":"Scammells","sequence":"additional","affiliation":[{"name":"Monash University , , , ,","place":["Parkville, Victoria, Australia, 3052"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sheena","family":"McGowan","sequence":"additional","affiliation":[{"name":"Monash University , , , ,","place":["Clayton, Victoria, Australia, 3800"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2014,10,9]]},"reference":[{"key":"2026090123293676500_cit1","doi-asserted-by":"crossref","first-page":"8840","DOI":"10.1073\/pnas.0601876103","article-title":"Plasmodium falciparum ensures its amino acid supply\nwith multiple acquisition pathways and redundant proteolytic enzyme\nsystems","volume":"103","author":"Liu","year":"2006","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"2026090123293676500_cit2","doi-asserted-by":"crossref","first-page":"140","DOI":"10.1097\/00062752-200203000-00010","article-title":"Hydrolysis\nof erythrocyte proteins by proteases of malaria parasites","volume":"9","author":"Rosenthal","year":"2002","journal-title":"Curr. Opin. Hematol."},{"key":"2026090123293676500_cit3","doi-asserted-by":"crossref","first-page":"353","DOI":"10.1016\/j.bcmd.2004.01.006","article-title":"Excess haemoglobin\ndigestion by malaria parasites: a strategy to prevent premature host\ncell lysis","volume":"32","author":"Lew","year":"2004","journal-title":"Blood Cells Mol. Dis."},{"key":"2026090123293676500_cit4","doi-asserted-by":"crossref","first-page":"43000","DOI":"10.1074\/jbc.M408123200","article-title":"A Plasmodium falciparum dipeptidyl aminopeptidase I\nparticipates in vacuolar hemoglobin\ndegradation","volume":"279","author":"Klemba","year":"2004","journal-title":"J. Biol. Chem."},{"key":"2026090123293676500_cit5","doi-asserted-by":"crossref","first-page":"2069","DOI":"10.1074\/jbc.M609251200","article-title":"Characterization of the Plasmodium falciparum M17 leucyl aminopeptidase. A protease involved in amino acid regulation\nwith potential for antimalarial drug development","volume":"282","author":"Stack","year":"2007","journal-title":"J. Biol. Chem."},{"key":"2026090123293676500_cit6","doi-asserted-by":"crossref","first-page":"828","DOI":"10.1016\/j.sbi.2013.07.015","article-title":"Working in\nconcert: the metalloaminopeptidases from Plasmodium falciparum","volume":"23","author":"McGowan","year":"2013","journal-title":"Curr. Opin. Struct.\nBiol."},{"key":"2026090123293676500_cit7","doi-asserted-by":"crossref","first-page":"2537","DOI":"10.1073\/pnas.0807398106","article-title":"Structural basis\nfor the inhibition of the essential Plasmodium falciparum M1 neutral aminopeptidase","volume":"106","author":"McGowan","year":"2009","journal-title":"Proc. Natl. Acad.\nSci. U.S.A."},{"key":"2026090123293676500_cit8","doi-asserted-by":"crossref","first-page":"6024","DOI":"10.1021\/jm070733v","article-title":"Identification of phosphinate dipeptide\nanalog inhibitors directed against the Plasmodium falciparum M17 leucine aminopeptidase as lead antimalarial compounds","volume":"50","author":"Skinner-Adams","year":"2007","journal-title":"J. Med. Chem."},{"key":"2026090123293676500_cit9","doi-asserted-by":"crossref","first-page":"2449","DOI":"10.1073\/pnas.0911813107","article-title":"Structure of the Plasmodium falciparum M17 aminopeptidase and significance for the design of drugs targeting\nthe neutral exopeptidases","volume":"107","author":"McGowan","year":"2010","journal-title":"Proc. Natl. Acad.\nSci. U.S.A."},{"key":"2026090123293676500_cit10","doi-asserted-by":"crossref","first-page":"10909","DOI":"10.1021\/jm301506h","article-title":"Structure\u2013activity\nrelationships and blood distribution of antiplasmodial aminopeptidase-1\ninhibitors","volume":"55","author":"Deprez-Poulain","year":"2012","journal-title":"J. Med. Chem."},{"key":"2026090123293676500_cit11","doi-asserted-by":"crossref","first-page":"1322","DOI":"10.1021\/jm061169b","article-title":"Novel selective inhibitors of the\nzinc plasmodial aminopeptidase PfA-M1 as potential\nantimalarial agents","volume":"50","author":"Flipo","year":"2007","journal-title":"J. Med. Chem."},{"key":"2026090123293676500_cit12","doi-asserted-by":"crossref","first-page":"2659","DOI":"10.1016\/S0960-894X(03)00550-X","article-title":"Design, synthesis and antimalarial\nactivity of novel,\nquinoline-based, zinc metallo-aminopeptidase inhibitors","volume":"13","author":"Flipo","year":"2003","journal-title":"Bioorg. Med. Chem. Lett."},{"key":"2026090123293676500_cit13","doi-asserted-by":"crossref","first-page":"5213","DOI":"10.1021\/jm4005972","article-title":"Synthesis and structure\u2013activity\nrelationships of phosphonic arginine mimetics as inhibitors of the\nM1 and M17 aminopeptidases from Plasmodium falciparum","volume":"56","author":"Kannan Sivaraman","year":"2013","journal-title":"J. Med. Chem."},{"key":"2026090123293676500_cit14","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1021\/cr50015a003","article-title":"The preparation and properties of phosphonic acids","volume":"57","author":"Freedman","year":"1957","journal-title":"Chem. Rev."},{"key":"2026090123293676500_cit15","doi-asserted-by":"crossref","first-page":"1359","DOI":"10.1021\/cr960370z","article-title":"Molecular recognition of protein-ligand complexes:\napplications to drug design","volume":"97","author":"Babine","year":"1997","journal-title":"Chem. Rev."},{"key":"2026090123293676500_cit16","doi-asserted-by":"crossref","first-page":"289","DOI":"10.2174\/156802606776287045","article-title":"Matrix\nmetalloproteinase inhibitors as prospective\nagents for the prevention and treatment of cardiovascular and neoplastic\ndiseases","volume":"6","author":"Sang","year":"2006","journal-title":"Curr. Top. Med. Chem."},{"key":"2026090123293676500_cit17","doi-asserted-by":"crossref","first-page":"6790","DOI":"10.1021\/jm900648x","article-title":"Hydroxamates:\nrelationships between\nstructure and plasma stability","volume":"52","author":"Flipo","year":"2009","journal-title":"J. Med. Chem."},{"key":"2026090123293676500_cit18","doi-asserted-by":"crossref","first-page":"1509","DOI":"10.1016\/j.biochi.2010.04.026","article-title":"Metallo-aminopeptidase\ninhibitors","volume":"92","author":"Mucha","year":"2010","journal-title":"Biochimie"},{"key":"2026090123293676500_cit19","doi-asserted-by":"crossref","first-page":"934","DOI":"10.1002\/anie.200603173","article-title":"Efficient iron\/copper\nco-catalyzed arylation of nitrogen\nnucleophiles","volume":"46","author":"Taillefer","year":"2007","journal-title":"Angew. Chem., Int. Ed."},{"key":"2026090123293676500_cit20","doi-asserted-by":"crossref","first-page":"6678","DOI":"10.1002\/ejoc.201000964","article-title":"Copper iodide as\na recyclable catalyst for Buchwald\nN-arylation","volume":"34","author":"Swapna","year":"2010","journal-title":"Eur. J. Org. Chem."},{"key":"2026090123293676500_cit21","doi-asserted-by":"crossref","first-page":"2673","DOI":"10.1002\/adsc.200700408","article-title":"Ligand-free copper-catalyzed\nN-arylation of nitrogen nucleophiles","author":"Correa","year":"2007","journal-title":"Adv. Synth.\nCatal."},{"key":"2026090123293676500_cit22","doi-asserted-by":"crossref","first-page":"4291","DOI":"10.1021\/ol701792j","article-title":"Cascade coupling\/cyclization\nprocess\nto N-substituted 1,3-dihydrobenzimidazol-2-ones","volume":"9","author":"Zou","year":"2007","journal-title":"Org. Lett."},{"key":"2026090123293676500_cit23","doi-asserted-by":"crossref","first-page":"2517","DOI":"10.1055\/s-0029-1216890","article-title":"Cu-Al hydrotalcite: an efficient and reusable ligand-free catalyst\nfor the coupling of aryl chlorides with aliphatic, aromatic, and N\n(H)-heterocyclic amines","author":"Sreedhar","year":"2009","journal-title":"Synthesis"},{"key":"2026090123293676500_cit24","doi-asserted-by":"crossref","first-page":"4187","DOI":"10.1016\/j.tet.2008.02.092","article-title":"Efficient catalysis\nof Ullmann-type arylation reactions by a novel trinuclear copper(I)\ncomplex with a chelating tricarbene ligand","volume":"64","author":"Tubaro","year":"2008","journal-title":"Tetrahedron"},{"key":"2026090123293676500_cit25","doi-asserted-by":"crossref","first-page":"778","DOI":"10.1039\/b316147a","article-title":"Synthesis of Cu2O coated\nCu nanoparticles and their successful applications to Ullmann-type\namination coupling reactions of aryl chlorides","author":"Uk Son","year":"2004","journal-title":"Chem. Commun. (Cambridge, U.K.)"},{"key":"2026090123293676500_cit26","doi-asserted-by":"crossref","first-page":"2692","DOI":"10.1002\/ejoc.201100112","article-title":"Use of acylhydrazine-\nand acylhydrazone-type ligands to promote CuI-catalyzed C\u2013N\ncross-coupling reactions of aryl bromides with N-heterocycles","volume":"2011","author":"Li","year":"2011","journal-title":"Eur. J. Org. Chem."},{"key":"2026090123293676500_cit27","doi-asserted-by":"crossref","first-page":"5733","DOI":"10.1021\/om800728m","article-title":"Thiazolyl phosphine\nligands for copper-catalyzed arylation and vinylation of nucleophiles\nin organic and aqueous media","volume":"27","author":"Oshovsky","year":"2008","journal-title":"Organometallics"},{"key":"2026090123293676500_cit28","doi-asserted-by":"crossref","first-page":"7223","DOI":"10.1039\/b906730b","article-title":"Trinuclear copper(I)\ncomplexes with triscarbene ligands: catalysis of C-N and C-C coupling\nreactions","author":"Biffis","year":"2009","journal-title":"Dalton Trans."},{"key":"2026090123293676500_cit29","doi-asserted-by":"crossref","first-page":"234","DOI":"10.1039\/c0cy00074d","article-title":"Sulfonic acid containing cation-exchanger\nresin \u201cINDION-770\u201d and copper (I) salts: a novel reusable\ncatalyst for N-arylation of NH-heterocycles with haloarenes","author":"Joseph","year":"2011","journal-title":"Catal. Sci. Technol."},{"key":"2026090123293676500_cit30","doi-asserted-by":"crossref","first-page":"4809","DOI":"10.1039\/b711298j","article-title":"Magnetic nanoparticle-supported\nproline\nas a recyclable and recoverable ligand for the CuI catalyzed arylation\nof nitrogen nucleophiles","author":"Chouhan","year":"2007","journal-title":"Chem. Commun. (Cambridge,\nU.K.)"},{"key":"2026090123293676500_cit31","doi-asserted-by":"crossref","first-page":"695","DOI":"10.1002\/ejoc.200300709","article-title":"Mild conditions\nfor copper-catalysed N-arylation of pyrazoles","author":"Cristau","year":"2004","journal-title":"Eur. J. Org. Chem."},{"key":"2026090123293676500_cit32","doi-asserted-by":"crossref","first-page":"5282","DOI":"10.1016\/j.tet.2011.05.025","article-title":"Cu(OAc)2\u00b7H2O-catalyzed N-arylation\nof nitrogen-containing heterocycles","volume":"67","author":"Xu","year":"2011","journal-title":"Tetrahedron"},{"key":"2026090123293676500_cit33","first-page":"10585","article-title":"Facile synthesis\nof nitrogen tetradentate ligands and\ntheir applications in CuI-catalyzed N-arylation and azide\u2013alkyne\ncycloaddition","volume":"15","author":"Li","year":"2009","journal-title":"Chem.\u2500Eur. J."},{"key":"2026090123293676500_cit34","doi-asserted-by":"crossref","first-page":"4434","DOI":"10.1080\/00397910802369554","article-title":"Synthesis of arylglyoxylic\nacids and their collision-induced\ndissociation","volume":"38","author":"Wadhwa","year":"2013","journal-title":"Synth. Commun."},{"key":"2026090123293676500_cit35","doi-asserted-by":"crossref","first-page":"3849","DOI":"10.1021\/jo960057x","article-title":"Reductive amination\nof aldehydes\nand ketones with sodium triacetoxyborohydride. Studies on direct and\nindirect reductive amination procedures","volume":"61","author":"Abdel-Magid","year":"1996","journal-title":"J.\nOrg. Chem."},{"key":"2026090123293676500_cit36","doi-asserted-by":"crossref","first-page":"927","DOI":"10.1080\/00397910903026723","article-title":"Synthesis of hydroxamic\nacids by activation of carboxylic acids with N,N\u2032-carbonyldiimidazole: exploring the efficiency\nof the method","volume":"40","author":"Usachova","year":"2013","journal-title":"Synth. Commun."},{"key":"2026090123293676500_cit37","doi-asserted-by":"crossref","first-page":"1645","DOI":"10.1016\/S0040-4039(00)84337-3","article-title":"Nitrone-based\nsynthesis of the pyrrolizidine alkaloid\ncroalbinecine","volume":"27","author":"Tufariello","year":"1986","journal-title":"Tetrahedron Lett."},{"key":"2026090123293676500_cit38","doi-asserted-by":"crossref","first-page":"4668","DOI":"10.1016\/j.bmcl.2012.05.084","article-title":"Photoinduced DNA cleavage by anthracene\nbased hydroxamic acids","volume":"22","author":"Chowdhury","year":"2012","journal-title":"Bioorg. Med. Chem. Lett."},{"key":"2026090123293676500_cit39","doi-asserted-by":"crossref","first-page":"3540","DOI":"10.1021\/jo900144h","article-title":"Efficient\ncontinuous flow synthesis of hydroxamic acids and suberoylanilide\nhydroxamic acid preparation","volume":"74","author":"Riva","year":"2013","journal-title":"J. Org. Chem."},{"key":"2026090123293676500_cit40","doi-asserted-by":"crossref","first-page":"6757","DOI":"10.1021\/jm901112f","article-title":"Searching for new cures for tuberculosis: design, synthesis,\nand biological evaluation of 2-methylbenzothiazoles","volume":"52","author":"Huang","year":"2013","journal-title":"J. Med. Chem."},{"key":"2026090123293676500_cit41","doi-asserted-by":"crossref","first-page":"206","DOI":"10.1002\/chir.530070405","article-title":"Synthesis of (+)-(S)-ibuproxam\nand preparation of some new complexes of racemic and (+)-(S)-ibuproxam\nwith B-cyclodextrin and its derivatives","volume":"7","author":"Zmitek","year":"1995","journal-title":"Chirality"},{"key":"2026090123293676500_cit42","unstructured":"Watkins, C. J.; Romero Maria Rosario, M.; Finn, P. W.; Kalvinsh, I.; Loza, E.; Lolya, D.; Starchenkov, I.; Bokaldere, R. M.; Semenikhina, V.; Harris, C. J.; Duffy, J. E. S.\n          Carbamic acid compounds comprising\nan ether linkage as HDAC inhibitors. Patent WO2002026703\nA1, 2002."},{"key":"2026090123293676500_cit43","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1055\/s-1987-27874","article-title":"Direct conversion of\nhydroxamic acids into nitriles","volume":"1987","author":"Liguori","year":"1987","journal-title":"Synthesis"},{"key":"2026090123293676500_cit44","doi-asserted-by":"crossref","first-page":"3201","DOI":"10.1055\/s-2007-990803","article-title":"Microwave-assisted\ntransformation of esters into hydroxamic acids","volume":"2007","author":"Massaro","year":"2007","journal-title":"Synthesis"},{"key":"2026090123293676500_cit45","doi-asserted-by":"crossref","first-page":"495","DOI":"10.1016\/j.jmb.2012.06.006","article-title":"X-ray crystal structure\nand specificity of the Plasmodium falciparum malaria aminopeptidase PfM18AAP","volume":"422","author":"Sivaraman","year":"2012","journal-title":"J. Mol. Biol."},{"key":"2026090123293676500_cit46","doi-asserted-by":"crossref","first-page":"e31938","DOI":"10.1371\/journal.pone.0031938","article-title":"Fingerprinting the\nsubstrate specificity\nof M1 and M17 neutral aminopeptidases of human malaria, Plasmodium falciparum","volume":"2","author":"Poreba","year":"2012","journal-title":"PLoS\nOne"},{"key":"2026090123293676500_cit47","doi-asserted-by":"crossref","first-page":"84","DOI":"10.4269\/ajtmh.2012.11-0302","article-title":"Development and\noptimization of a novel 384-well anti-malarial\nimaging assay validated for high-throughput screening","volume":"86","author":"Duffy","year":"2012","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"2026090123293676500_cit48","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1016\/j.bmcl.2004.10.010","article-title":"N-Hydroxy-2-(naphthalene-2-ylsulfanyl)-acetamide, a novel\nhydroxamic acid-based inhibitor of aminopeptidase N and its anti-angiogenic\nactivity","volume":"15","author":"Lee","year":"2005","journal-title":"Bioorg. Med. Chem. 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Parasitol."},{"key":"2026090123293676500_cit52","doi-asserted-by":"crossref","first-page":"419","DOI":"10.1586\/14787210.3.3.419","article-title":"Therapeutic\nstrategies for human microsporidia infections","volume":"3","author":"Didier","year":"2005","journal-title":"Expert Rev. Anti-Infect. Ther."},{"key":"2026090123293676500_cit53","doi-asserted-by":"crossref","first-page":"791","DOI":"10.1515\/hsz-2012-0308","article-title":"The Staphylococcus aureus leucine aminopeptidase is localized\nto the bacterial cytosol and demonstrates a broad substrate range\nthat extends beyond leucine","volume":"394","author":"Carroll","year":"2013","journal-title":"Biol. Chem."},{"key":"2026090123293676500_cit54","doi-asserted-by":"crossref","first-page":"2017","DOI":"10.1099\/mic.0.27767-0","article-title":"The leucyl aminopeptidase\nfrom Helicobacter pylori is an allosteric enzyme","volume":"151","author":"Dong","year":"2005","journal-title":"Microbiology"},{"key":"2026090123293676500_cit55","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1107\/S0907444910048675","article-title":"iMOSFLM: a\nnew graphical interface for diffraction-image processing with MOSFLM","volume":"67","author":"Battye","year":"2011","journal-title":"Acta. Crystallogr., D: Biol. 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