The activities of current antimalarial drugs on the life cycle stages of Plasmodium: a comparative study with human and rodent parasites
Malaria remains a disease of devastating global impact, killing more than 800,000 people every year-the vast majority being children under the age of 5. While effective therapies are available, if malaria is to be eradicated a broader range of small molecule therapeutics that are able to target the...
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description | Malaria remains a disease of devastating global impact, killing more than 800,000 people every year-the vast majority being children under the age of 5. While effective therapies are available, if malaria is to be eradicated a broader range of small molecule therapeutics that are able to target the liver and the transmissible sexual stages are required. These new medicines are needed both to meet the challenge of malaria eradication and to circumvent resistance.
Little is known about the wider stage-specific activities of current antimalarials that were primarily designed to alleviate symptoms of malaria in the blood stage. To overcome this critical gap, we developed assays to measure activity of antimalarials against all life stages of malaria parasites, using a diverse set of human and nonhuman parasite species, including male gamete production (exflagellation) in Plasmodium falciparum, ookinete development in P. berghei, oocyst development in P. berghei and P. falciparum, and the liver stage of P. yoelii. We then compared 50 current and experimental antimalarials in these assays. We show that endoperoxides such as OZ439, a stable synthetic molecule currently in clinical phase IIa trials, are strong inhibitors of gametocyte maturation/gamete formation and impact sporogony; lumefantrine impairs development in the vector; and NPC-1161B, a new 8-aminoquinoline, inhibits sporogony.
These data enable objective comparisons of the strengths and weaknesses of each chemical class at targeting each stage of the lifecycle. Noting that the activities of many compounds lie within achievable blood concentrations, these results offer an invaluable guide to decisions regarding which drugs to combine in the next-generation of antimalarial drugs. This study might reveal the potential of life-cycle-wide analyses of drugs for other pathogens with complex life cycles. |
doi_str_mv | 10.1371/journal.pmed.1001169 |
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Little is known about the wider stage-specific activities of current antimalarials that were primarily designed to alleviate symptoms of malaria in the blood stage. To overcome this critical gap, we developed assays to measure activity of antimalarials against all life stages of malaria parasites, using a diverse set of human and nonhuman parasite species, including male gamete production (exflagellation) in Plasmodium falciparum, ookinete development in P. berghei, oocyst development in P. berghei and P. falciparum, and the liver stage of P. yoelii. We then compared 50 current and experimental antimalarials in these assays. We show that endoperoxides such as OZ439, a stable synthetic molecule currently in clinical phase IIa trials, are strong inhibitors of gametocyte maturation/gamete formation and impact sporogony; lumefantrine impairs development in the vector; and NPC-1161B, a new 8-aminoquinoline, inhibits sporogony.
These data enable objective comparisons of the strengths and weaknesses of each chemical class at targeting each stage of the lifecycle. Noting that the activities of many compounds lie within achievable blood concentrations, these results offer an invaluable guide to decisions regarding which drugs to combine in the next-generation of antimalarial drugs. This study might reveal the potential of life-cycle-wide analyses of drugs for other pathogens with complex life cycles.</description><identifier>ISSN: 1549-1676</identifier><identifier>ISSN: 1549-1277</identifier><identifier>EISSN: 1549-1676</identifier><identifier>DOI: 10.1371/journal.pmed.1001169</identifier><identifier>PMID: 22363211</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Antimalarials ; Antimalarials - chemistry ; Antimalarials - classification ; Antimalarials - pharmacology ; Blood ; Chemistry ; Culicidae - parasitology ; Drug Resistance, Multiple ; Experiments ; Health aspects ; Humans ; Life cycles (Biology) ; Liver - parasitology ; Malaria ; Malaria - drug therapy ; Malaria - parasitology ; Malaria - transmission ; Malaria, Falciparum - drug therapy ; Malaria, Falciparum - parasitology ; Malaria, Falciparum - transmission ; Medicine ; Mice - parasitology ; Parasites ; Physiological aspects ; Plasmodium ; Plasmodium berghei - drug effects ; Plasmodium berghei - growth & development ; Plasmodium falciparum - drug effects ; Plasmodium falciparum - growth & development ; Plasmodium yoelii - drug effects ; Plasmodium yoelii - growth & development ; Rodents ; Species Specificity</subject><ispartof>PLoS medicine, 2012-02, Vol.9 (2), p.e1001169-e1001169</ispartof><rights>COPYRIGHT 2012 Public Library of Science</rights><rights>2012 Delves et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Delves M, Plouffe D, Scheurer C, Meister S, Wittlin S, et al. (2012) The Activities of Current Antimalarial Drugs on the Life Cycle Stages of Plasmodium: A Comparative Study with Human and Rodent Parasites. PLoS Med 9(2): e1001169. doi:10.1371/journal.pmed.1001169</rights><rights>Delves et al. 2012</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c763t-d5f650cf4d8e6ec9875014e563510565ab26861419fbb60c7236024fbaa416063</citedby><cites>FETCH-LOGICAL-c763t-d5f650cf4d8e6ec9875014e563510565ab26861419fbb60c7236024fbaa416063</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3283556/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3283556/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22363211$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Beeson, James G.</contributor><creatorcontrib>Delves, Michael</creatorcontrib><creatorcontrib>Plouffe, David</creatorcontrib><creatorcontrib>Scheurer, Christian</creatorcontrib><creatorcontrib>Meister, Stephan</creatorcontrib><creatorcontrib>Wittlin, Sergio</creatorcontrib><creatorcontrib>Winzeler, Elizabeth A</creatorcontrib><creatorcontrib>Sinden, Robert E</creatorcontrib><creatorcontrib>Leroy, Didier</creatorcontrib><title>The activities of current antimalarial drugs on the life cycle stages of Plasmodium: a comparative study with human and rodent parasites</title><title>PLoS medicine</title><addtitle>PLoS Med</addtitle><description>Malaria remains a disease of devastating global impact, killing more than 800,000 people every year-the vast majority being children under the age of 5. While effective therapies are available, if malaria is to be eradicated a broader range of small molecule therapeutics that are able to target the liver and the transmissible sexual stages are required. These new medicines are needed both to meet the challenge of malaria eradication and to circumvent resistance.
Little is known about the wider stage-specific activities of current antimalarials that were primarily designed to alleviate symptoms of malaria in the blood stage. To overcome this critical gap, we developed assays to measure activity of antimalarials against all life stages of malaria parasites, using a diverse set of human and nonhuman parasite species, including male gamete production (exflagellation) in Plasmodium falciparum, ookinete development in P. berghei, oocyst development in P. berghei and P. falciparum, and the liver stage of P. yoelii. We then compared 50 current and experimental antimalarials in these assays. We show that endoperoxides such as OZ439, a stable synthetic molecule currently in clinical phase IIa trials, are strong inhibitors of gametocyte maturation/gamete formation and impact sporogony; lumefantrine impairs development in the vector; and NPC-1161B, a new 8-aminoquinoline, inhibits sporogony.
These data enable objective comparisons of the strengths and weaknesses of each chemical class at targeting each stage of the lifecycle. Noting that the activities of many compounds lie within achievable blood concentrations, these results offer an invaluable guide to decisions regarding which drugs to combine in the next-generation of antimalarial drugs. This study might reveal the potential of life-cycle-wide analyses of drugs for other pathogens with complex life cycles.</description><subject>Animals</subject><subject>Antimalarials</subject><subject>Antimalarials - chemistry</subject><subject>Antimalarials - classification</subject><subject>Antimalarials - pharmacology</subject><subject>Blood</subject><subject>Chemistry</subject><subject>Culicidae - parasitology</subject><subject>Drug Resistance, Multiple</subject><subject>Experiments</subject><subject>Health aspects</subject><subject>Humans</subject><subject>Life cycles (Biology)</subject><subject>Liver - parasitology</subject><subject>Malaria</subject><subject>Malaria - drug therapy</subject><subject>Malaria - parasitology</subject><subject>Malaria - transmission</subject><subject>Malaria, Falciparum - drug therapy</subject><subject>Malaria, Falciparum - parasitology</subject><subject>Malaria, Falciparum - transmission</subject><subject>Medicine</subject><subject>Mice - parasitology</subject><subject>Parasites</subject><subject>Physiological aspects</subject><subject>Plasmodium</subject><subject>Plasmodium berghei - drug effects</subject><subject>Plasmodium berghei - growth & development</subject><subject>Plasmodium falciparum - drug effects</subject><subject>Plasmodium falciparum - growth & development</subject><subject>Plasmodium yoelii - drug effects</subject><subject>Plasmodium yoelii - growth & development</subject><subject>Rodents</subject><subject>Species Specificity</subject><issn>1549-1676</issn><issn>1549-1277</issn><issn>1549-1676</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>DOA</sourceid><recordid>eNqVk12L1DAUhoso7rr6D0QDguLFjEmapK0XwrL4MbC4oqu34TRNO1nSZkzS1fkH_mxTZ3aZkblQepGSPO97vjhZ9pjgOckL8urKjX4AO1_1upkTjAkR1Z3smHBWzYgoxN2d_6PsQQhXGNMKV_h-dkRpLnJKyHH263KpEahork00OiDXIjV6r4eIYIimBwvegEWNH7v0OqCYeGtajdRaWY1ChG4j-2Qh9K4xY_8aAVKuX4GH5DsxY7NGP0xcouXYw5CcG-RdMwWZoGCiDg-zey3YoB9tz5Ps67u3l2cfZucX7xdnp-czVYg8zhreCo5Vy5pSC62qsuCYMM1FzgnmgkNNRSkII1Vb1wKrIlWKKWtrAEYEFvlJ9nTju7IuyG0TgyS0LHHFGcaJWGyIxsGVXPnUBL-WDoz8c-F8J8FHk6qXGmrGBVWiqEqmaVlTXTFQuRZtozBuktebbbSxTnNSqWQPds90_2UwS9m5a5nTMud8SvfF1sC776MOUfYmKG0tDNqNQVY050VJBEvks7_Iw8VtqQ5S_mZoXQqrJk95mkISXjI6UbMDVKcHnXJ0g25Nut7j5wf49DW6N-qg4OWeIDFR_4wdjCHIxZfP_8F-_Hf24ts--3yHXWqwcRmcHaNxQ9gH2QZU3oXgdXs7P4LltIs3nZbTLsrtLibZk93Z34puli__Db1uLiY</recordid><startdate>20120201</startdate><enddate>20120201</enddate><creator>Delves, Michael</creator><creator>Plouffe, David</creator><creator>Scheurer, Christian</creator><creator>Meister, Stephan</creator><creator>Wittlin, Sergio</creator><creator>Winzeler, Elizabeth A</creator><creator>Sinden, Robert E</creator><creator>Leroy, Didier</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISN</scope><scope>ISR</scope><scope>3V.</scope><scope>7TK</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BENPR</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>K9.</scope><scope>M0S</scope><scope>M1P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><scope>CZK</scope></search><sort><creationdate>20120201</creationdate><title>The activities of current antimalarial drugs on the life cycle stages of Plasmodium: a comparative study with human and rodent parasites</title><author>Delves, Michael ; Plouffe, David ; Scheurer, Christian ; Meister, Stephan ; Wittlin, Sergio ; Winzeler, Elizabeth A ; Sinden, Robert E ; Leroy, Didier</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c763t-d5f650cf4d8e6ec9875014e563510565ab26861419fbb60c7236024fbaa416063</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Animals</topic><topic>Antimalarials</topic><topic>Antimalarials - chemistry</topic><topic>Antimalarials - classification</topic><topic>Antimalarials - pharmacology</topic><topic>Blood</topic><topic>Chemistry</topic><topic>Culicidae - parasitology</topic><topic>Drug Resistance, Multiple</topic><topic>Experiments</topic><topic>Health aspects</topic><topic>Humans</topic><topic>Life cycles (Biology)</topic><topic>Liver - parasitology</topic><topic>Malaria</topic><topic>Malaria - drug therapy</topic><topic>Malaria - parasitology</topic><topic>Malaria - transmission</topic><topic>Malaria, Falciparum - drug therapy</topic><topic>Malaria, Falciparum - parasitology</topic><topic>Malaria, Falciparum - transmission</topic><topic>Medicine</topic><topic>Mice - parasitology</topic><topic>Parasites</topic><topic>Physiological aspects</topic><topic>Plasmodium</topic><topic>Plasmodium berghei - drug effects</topic><topic>Plasmodium berghei - growth & development</topic><topic>Plasmodium falciparum - drug effects</topic><topic>Plasmodium falciparum - growth & development</topic><topic>Plasmodium yoelii - drug effects</topic><topic>Plasmodium yoelii - growth & development</topic><topic>Rodents</topic><topic>Species Specificity</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Delves, Michael</creatorcontrib><creatorcontrib>Plouffe, David</creatorcontrib><creatorcontrib>Scheurer, Christian</creatorcontrib><creatorcontrib>Meister, Stephan</creatorcontrib><creatorcontrib>Wittlin, Sergio</creatorcontrib><creatorcontrib>Winzeler, Elizabeth A</creatorcontrib><creatorcontrib>Sinden, Robert E</creatorcontrib><creatorcontrib>Leroy, Didier</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Neurosciences Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>ProQuest Central</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Access via ProQuest (Open Access)</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><collection>PLoS Medicine</collection><jtitle>PLoS medicine</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Delves, Michael</au><au>Plouffe, David</au><au>Scheurer, Christian</au><au>Meister, Stephan</au><au>Wittlin, Sergio</au><au>Winzeler, Elizabeth A</au><au>Sinden, Robert E</au><au>Leroy, Didier</au><au>Beeson, James G.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The activities of current antimalarial drugs on the life cycle stages of Plasmodium: a comparative study with human and rodent parasites</atitle><jtitle>PLoS medicine</jtitle><addtitle>PLoS Med</addtitle><date>2012-02-01</date><risdate>2012</risdate><volume>9</volume><issue>2</issue><spage>e1001169</spage><epage>e1001169</epage><pages>e1001169-e1001169</pages><issn>1549-1676</issn><issn>1549-1277</issn><eissn>1549-1676</eissn><abstract>Malaria remains a disease of devastating global impact, killing more than 800,000 people every year-the vast majority being children under the age of 5. While effective therapies are available, if malaria is to be eradicated a broader range of small molecule therapeutics that are able to target the liver and the transmissible sexual stages are required. These new medicines are needed both to meet the challenge of malaria eradication and to circumvent resistance.
Little is known about the wider stage-specific activities of current antimalarials that were primarily designed to alleviate symptoms of malaria in the blood stage. To overcome this critical gap, we developed assays to measure activity of antimalarials against all life stages of malaria parasites, using a diverse set of human and nonhuman parasite species, including male gamete production (exflagellation) in Plasmodium falciparum, ookinete development in P. berghei, oocyst development in P. berghei and P. falciparum, and the liver stage of P. yoelii. We then compared 50 current and experimental antimalarials in these assays. We show that endoperoxides such as OZ439, a stable synthetic molecule currently in clinical phase IIa trials, are strong inhibitors of gametocyte maturation/gamete formation and impact sporogony; lumefantrine impairs development in the vector; and NPC-1161B, a new 8-aminoquinoline, inhibits sporogony.
These data enable objective comparisons of the strengths and weaknesses of each chemical class at targeting each stage of the lifecycle. Noting that the activities of many compounds lie within achievable blood concentrations, these results offer an invaluable guide to decisions regarding which drugs to combine in the next-generation of antimalarial drugs. This study might reveal the potential of life-cycle-wide analyses of drugs for other pathogens with complex life cycles.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>22363211</pmid><doi>10.1371/journal.pmed.1001169</doi><oa>free_for_read</oa></addata></record> |
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subjects | Animals Antimalarials Antimalarials - chemistry Antimalarials - classification Antimalarials - pharmacology Blood Chemistry Culicidae - parasitology Drug Resistance, Multiple Experiments Health aspects Humans Life cycles (Biology) Liver - parasitology Malaria Malaria - drug therapy Malaria - parasitology Malaria - transmission Malaria, Falciparum - drug therapy Malaria, Falciparum - parasitology Malaria, Falciparum - transmission Medicine Mice - parasitology Parasites Physiological aspects Plasmodium Plasmodium berghei - drug effects Plasmodium berghei - growth & development Plasmodium falciparum - drug effects Plasmodium falciparum - growth & development Plasmodium yoelii - drug effects Plasmodium yoelii - growth & development Rodents Species Specificity |
title | The activities of current antimalarial drugs on the life cycle stages of Plasmodium: a comparative study with human and rodent parasites |
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