Serveur d'exploration sur les relations entre la France et l'Australie

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Red cells from ferrochelatase-deficient erythropoietic protoporphyria patients are resistant to growth of malarial parasites.

Identifieur interne : 003031 ( PubMed/Curation ); précédent : 003030; suivant : 003032

Red cells from ferrochelatase-deficient erythropoietic protoporphyria patients are resistant to growth of malarial parasites.

Auteurs : Clare M. Smith [Australie] ; Ante Jerkovic [Australie] ; Hervé Puy [France] ; Ingrid Winship [Australie] ; Jean-Charles Deybach [France] ; Laurent Gouya [France] ; Giel Van Dooren [Australie] ; Christopher Dean Goodman [Australie] ; Angelika Sturm [Australie] ; Hana Manceau [France] ; Geoffrey Ian Mcfadden [Australie] ; Peter David ; Odile Mercereau-Puijalon ; Gaétan Burgio [Australie] ; Brendan J. Mcmorran [Australie] ; Simon J. Foote [Australie]

Source :

RBID : pubmed:25414439

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English descriptors

Abstract

Many red cell polymorphisms are a result of selective pressure by the malarial parasite. Here, we add another red cell disease to the panoply of erythrocytic changes that give rise to resistance to malaria. Erythrocytes from individuals with erythropoietic protoporphyria (EPP) have low levels of the final enzyme in the heme biosynthetic pathway, ferrochelatase. Cells from these patients are resistant to the growth of Plasmodium falciparum malarial parasites. This phenomenon is due to the absence of ferrochelatase and not an accumulation of substrate, as demonstrated by the normal growth of P falciparum parasites in the EPP phenocopy, X-linked dominant protoporphyria, which has elevated substrate, and normal ferrochelatase levels. This observation was replicated in a mouse strain with a hypomorphic mutation in the murine ferrochelatase gene. The parasite enzyme is not essential for parasite growth as Plasmodium berghei parasites carrying a complete deletion of the ferrochelatase gene grow normally in erythrocytes, which confirms previous studies. That ferrochelatase is essential to parasite growth was confirmed by showing that inhibition of ferrochelatase using the specific competitive inhibitor, N-methylprotoporphyrin, produced a potent growth inhibition effect against cultures of P falciparum. This raises the possibility of targeting human ferrochelatase in a host-directed antimalarial strategy.

DOI: 10.1182/blood-2014-04-567149
PubMed: 25414439

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Peter David
<affiliation>
<nlm:affiliation>Institut Pasteur, Unité d'Immunologie Moléculaire des Parasites, Centre Nationale de la Recherche Scientifique, Unite de Recherche Associé 2581, Paris, France; and.</nlm:affiliation>
<wicri:noCountry code="subField">France; and</wicri:noCountry>
</affiliation>
Odile Mercereau-Puijalon
<affiliation>
<nlm:affiliation>Institut Pasteur, Unité d'Immunologie Moléculaire des Parasites, Centre Nationale de la Recherche Scientifique, Unite de Recherche Associé 2581, Paris, France; and.</nlm:affiliation>
<wicri:noCountry code="subField">France; and</wicri:noCountry>
</affiliation>

Le document en format XML

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<name sortKey="Van Dooren, Giel" sort="Van Dooren, Giel" uniqKey="Van Dooren G" first="Giel" last="Van Dooren">Giel Van Dooren</name>
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<nlm:affiliation>Research School of Biology, Australian National University, Canberra, ACT, Australia;</nlm:affiliation>
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<name sortKey="Goodman, Christopher Dean" sort="Goodman, Christopher Dean" uniqKey="Goodman C" first="Christopher Dean" last="Goodman">Christopher Dean Goodman</name>
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<name sortKey="Manceau, Hana" sort="Manceau, Hana" uniqKey="Manceau H" first="Hana" last="Manceau">Hana Manceau</name>
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<nlm:affiliation>Centre Français des Porphyries, Hôpital Louis Mourier, Assistance Publique-Hôpitaux de Paris, Colombes, France; Centre de Recherche sur l'Inflammation, INSERM U1149, Paris, France;</nlm:affiliation>
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<name sortKey="Mcfadden, Geoffrey Ian" sort="Mcfadden, Geoffrey Ian" uniqKey="Mcfadden G" first="Geoffrey Ian" last="Mcfadden">Geoffrey Ian Mcfadden</name>
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<nlm:affiliation>School of Botany, University of Melbourne, Parkville, VIC, Australia;</nlm:affiliation>
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<name sortKey="David, Peter" sort="David, Peter" uniqKey="David P" first="Peter" last="David">Peter David</name>
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<name sortKey="Mercereau Puijalon, Odile" sort="Mercereau Puijalon, Odile" uniqKey="Mercereau Puijalon O" first="Odile" last="Mercereau-Puijalon">Odile Mercereau-Puijalon</name>
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<name sortKey="Burgio, Gaetan" sort="Burgio, Gaetan" uniqKey="Burgio G" first="Gaétan" last="Burgio">Gaétan Burgio</name>
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<name sortKey="Mcmorran, Brendan J" sort="Mcmorran, Brendan J" uniqKey="Mcmorran B" first="Brendan J" last="Mcmorran">Brendan J. Mcmorran</name>
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<name sortKey="Foote, Simon J" sort="Foote, Simon J" uniqKey="Foote S" first="Simon J" last="Foote">Simon J. Foote</name>
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<keywords scheme="KwdEn" xml:lang="en">
<term>Animals</term>
<term>Erythrocytes (enzymology)</term>
<term>Erythrocytes (parasitology)</term>
<term>Female</term>
<term>Ferrochelatase (antagonists & inhibitors)</term>
<term>Ferrochelatase (physiology)</term>
<term>Heme (metabolism)</term>
<term>Humans</term>
<term>Malaria, Falciparum (enzymology)</term>
<term>Malaria, Falciparum (parasitology)</term>
<term>Malaria, Falciparum (prevention & control)</term>
<term>Male</term>
<term>Mice</term>
<term>Mice, Inbred C57BL</term>
<term>Phenotype</term>
<term>Plasmodium berghei (growth & development)</term>
<term>Protoporphyria, Erythropoietic (enzymology)</term>
<term>Protoporphyria, Erythropoietic (parasitology)</term>
<term>Protoporphyria, Erythropoietic (prevention & control)</term>
<term>Protoporphyrins (pharmacology)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Animaux</term>
<term>Femelle</term>
<term>Ferrochelatase (antagonistes et inhibiteurs)</term>
<term>Ferrochelatase (physiologie)</term>
<term>Humains</term>
<term>Hème (métabolisme)</term>
<term>Mâle</term>
<term>Paludisme à Plasmodium falciparum ()</term>
<term>Paludisme à Plasmodium falciparum (enzymologie)</term>
<term>Paludisme à Plasmodium falciparum (parasitologie)</term>
<term>Phénotype</term>
<term>Plasmodium berghei (croissance et développement)</term>
<term>Protoporphyrie érythropoïétique ()</term>
<term>Protoporphyrie érythropoïétique (enzymologie)</term>
<term>Protoporphyrie érythropoïétique (parasitologie)</term>
<term>Protoporphyrines (pharmacologie)</term>
<term>Souris</term>
<term>Souris de lignée C57BL</term>
<term>Érythrocytes (enzymologie)</term>
<term>Érythrocytes (parasitologie)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="antagonists & inhibitors" xml:lang="en">
<term>Ferrochelatase</term>
</keywords>
<keywords scheme="MESH" qualifier="antagonistes et inhibiteurs" xml:lang="fr">
<term>Ferrochelatase</term>
</keywords>
<keywords scheme="MESH" qualifier="croissance et développement" xml:lang="fr">
<term>Plasmodium berghei</term>
</keywords>
<keywords scheme="MESH" qualifier="enzymologie" xml:lang="fr">
<term>Paludisme à Plasmodium falciparum</term>
<term>Protoporphyrie érythropoïétique</term>
<term>Érythrocytes</term>
</keywords>
<keywords scheme="MESH" qualifier="enzymology" xml:lang="en">
<term>Erythrocytes</term>
<term>Malaria, Falciparum</term>
<term>Protoporphyria, Erythropoietic</term>
</keywords>
<keywords scheme="MESH" qualifier="growth & development" xml:lang="en">
<term>Plasmodium berghei</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en">
<term>Heme</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Hème</term>
</keywords>
<keywords scheme="MESH" qualifier="parasitologie" xml:lang="fr">
<term>Paludisme à Plasmodium falciparum</term>
<term>Protoporphyrie érythropoïétique</term>
<term>Érythrocytes</term>
</keywords>
<keywords scheme="MESH" qualifier="parasitology" xml:lang="en">
<term>Erythrocytes</term>
<term>Malaria, Falciparum</term>
<term>Protoporphyria, Erythropoietic</term>
</keywords>
<keywords scheme="MESH" qualifier="pharmacologie" xml:lang="fr">
<term>Protoporphyrines</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="pharmacology" xml:lang="en">
<term>Protoporphyrins</term>
</keywords>
<keywords scheme="MESH" qualifier="physiologie" xml:lang="fr">
<term>Ferrochelatase</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="physiology" xml:lang="en">
<term>Ferrochelatase</term>
</keywords>
<keywords scheme="MESH" qualifier="prevention & control" xml:lang="en">
<term>Malaria, Falciparum</term>
<term>Protoporphyria, Erythropoietic</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Animals</term>
<term>Female</term>
<term>Humans</term>
<term>Male</term>
<term>Mice</term>
<term>Mice, Inbred C57BL</term>
<term>Phenotype</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Animaux</term>
<term>Femelle</term>
<term>Humains</term>
<term>Mâle</term>
<term>Paludisme à Plasmodium falciparum</term>
<term>Phénotype</term>
<term>Protoporphyrie érythropoïétique</term>
<term>Souris</term>
<term>Souris de lignée C57BL</term>
</keywords>
</textClass>
</profileDesc>
</teiHeader>
<front>
<div type="abstract" xml:lang="en">Many red cell polymorphisms are a result of selective pressure by the malarial parasite. Here, we add another red cell disease to the panoply of erythrocytic changes that give rise to resistance to malaria. Erythrocytes from individuals with erythropoietic protoporphyria (EPP) have low levels of the final enzyme in the heme biosynthetic pathway, ferrochelatase. Cells from these patients are resistant to the growth of Plasmodium falciparum malarial parasites. This phenomenon is due to the absence of ferrochelatase and not an accumulation of substrate, as demonstrated by the normal growth of P falciparum parasites in the EPP phenocopy, X-linked dominant protoporphyria, which has elevated substrate, and normal ferrochelatase levels. This observation was replicated in a mouse strain with a hypomorphic mutation in the murine ferrochelatase gene. The parasite enzyme is not essential for parasite growth as Plasmodium berghei parasites carrying a complete deletion of the ferrochelatase gene grow normally in erythrocytes, which confirms previous studies. That ferrochelatase is essential to parasite growth was confirmed by showing that inhibition of ferrochelatase using the specific competitive inhibitor, N-methylprotoporphyrin, produced a potent growth inhibition effect against cultures of P falciparum. This raises the possibility of targeting human ferrochelatase in a host-directed antimalarial strategy.</div>
</front>
</TEI>
<pubmed>
<MedlineCitation Status="MEDLINE" Owner="NLM">
<PMID Version="1">25414439</PMID>
<DateCreated>
<Year>2015</Year>
<Month>01</Month>
<Day>16</Day>
</DateCreated>
<DateCompleted>
<Year>2015</Year>
<Month>03</Month>
<Day>12</Day>
</DateCompleted>
<DateRevised>
<Year>2015</Year>
<Month>10</Month>
<Day>28</Day>
</DateRevised>
<Article PubModel="Print-Electronic">
<Journal>
<ISSN IssnType="Electronic">1528-0020</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>125</Volume>
<Issue>3</Issue>
<PubDate>
<Year>2015</Year>
<Month>Jan</Month>
<Day>15</Day>
</PubDate>
</JournalIssue>
<Title>Blood</Title>
<ISOAbbreviation>Blood</ISOAbbreviation>
</Journal>
<ArticleTitle>Red cells from ferrochelatase-deficient erythropoietic protoporphyria patients are resistant to growth of malarial parasites.</ArticleTitle>
<Pagination>
<MedlinePgn>534-41</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1182/blood-2014-04-567149</ELocationID>
<Abstract>
<AbstractText>Many red cell polymorphisms are a result of selective pressure by the malarial parasite. Here, we add another red cell disease to the panoply of erythrocytic changes that give rise to resistance to malaria. Erythrocytes from individuals with erythropoietic protoporphyria (EPP) have low levels of the final enzyme in the heme biosynthetic pathway, ferrochelatase. Cells from these patients are resistant to the growth of Plasmodium falciparum malarial parasites. This phenomenon is due to the absence of ferrochelatase and not an accumulation of substrate, as demonstrated by the normal growth of P falciparum parasites in the EPP phenocopy, X-linked dominant protoporphyria, which has elevated substrate, and normal ferrochelatase levels. This observation was replicated in a mouse strain with a hypomorphic mutation in the murine ferrochelatase gene. The parasite enzyme is not essential for parasite growth as Plasmodium berghei parasites carrying a complete deletion of the ferrochelatase gene grow normally in erythrocytes, which confirms previous studies. That ferrochelatase is essential to parasite growth was confirmed by showing that inhibition of ferrochelatase using the specific competitive inhibitor, N-methylprotoporphyrin, produced a potent growth inhibition effect against cultures of P falciparum. This raises the possibility of targeting human ferrochelatase in a host-directed antimalarial strategy.</AbstractText>
<CopyrightInformation>© 2015 by The American Society of Hematology.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Smith</LastName>
<ForeName>Clare M</ForeName>
<Initials>CM</Initials>
<AffiliationInfo>
<Affiliation>Menzies Research Institute Tasmania and School of Medicine, University of Tasmania, Hobart, TAS, Australia;</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Jerkovic</LastName>
<ForeName>Ante</ForeName>
<Initials>A</Initials>
<AffiliationInfo>
<Affiliation>Australian School of Advanced Medicine, Macquarie University, North Ryde, NSW, Australia;</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Puy</LastName>
<ForeName>Hervé</ForeName>
<Initials>H</Initials>
<AffiliationInfo>
<Affiliation>Centre Français des Porphyries, Hôpital Louis Mourier, Assistance Publique-Hôpitaux de Paris, Colombes, France; Centre de Recherche sur l'Inflammation, INSERM U1149, Paris, France; Groupe d'Excellence, Pôle de Recherche et d'Enseignement Supérieur, Sorbonne Paris-Cité, Paris, France;</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Winship</LastName>
<ForeName>Ingrid</ForeName>
<Initials>I</Initials>
<AffiliationInfo>
<Affiliation>Department of Medicine, University of Melbourne, Melbourne, VIC, Australia; Office of Research, Royal Melbourne Hospital, Parkville, VIC, Australia;</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Deybach</LastName>
<ForeName>Jean-Charles</ForeName>
<Initials>JC</Initials>
<AffiliationInfo>
<Affiliation>Centre Français des Porphyries, Hôpital Louis Mourier, Assistance Publique-Hôpitaux de Paris, Colombes, France; Centre de Recherche sur l'Inflammation, INSERM U1149, Paris, France;</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Gouya</LastName>
<ForeName>Laurent</ForeName>
<Initials>L</Initials>
<AffiliationInfo>
<Affiliation>Centre de Recherche sur l'Inflammation, INSERM U1149, Paris, France; Groupe d'Excellence, Pôle de Recherche et d'Enseignement Supérieur, Sorbonne Paris-Cité, Paris, France;</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>van Dooren</LastName>
<ForeName>Giel</ForeName>
<Initials>G</Initials>
<AffiliationInfo>
<Affiliation>Research School of Biology, Australian National University, Canberra, ACT, Australia;</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Goodman</LastName>
<ForeName>Christopher Dean</ForeName>
<Initials>CD</Initials>
<AffiliationInfo>
<Affiliation>School of Botany, University of Melbourne, Parkville, VIC, Australia;</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Sturm</LastName>
<ForeName>Angelika</ForeName>
<Initials>A</Initials>
<AffiliationInfo>
<Affiliation>School of Botany, University of Melbourne, Parkville, VIC, Australia;</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Manceau</LastName>
<ForeName>Hana</ForeName>
<Initials>H</Initials>
<AffiliationInfo>
<Affiliation>Centre Français des Porphyries, Hôpital Louis Mourier, Assistance Publique-Hôpitaux de Paris, Colombes, France; Centre de Recherche sur l'Inflammation, INSERM U1149, Paris, France;</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>McFadden</LastName>
<ForeName>Geoffrey Ian</ForeName>
<Initials>GI</Initials>
<AffiliationInfo>
<Affiliation>School of Botany, University of Melbourne, Parkville, VIC, Australia;</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>David</LastName>
<ForeName>Peter</ForeName>
<Initials>P</Initials>
<AffiliationInfo>
<Affiliation>Institut Pasteur, Unité d'Immunologie Moléculaire des Parasites, Centre Nationale de la Recherche Scientifique, Unite de Recherche Associé 2581, Paris, France; and.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Mercereau-Puijalon</LastName>
<ForeName>Odile</ForeName>
<Initials>O</Initials>
<AffiliationInfo>
<Affiliation>Institut Pasteur, Unité d'Immunologie Moléculaire des Parasites, Centre Nationale de la Recherche Scientifique, Unite de Recherche Associé 2581, Paris, France; and.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Burgio</LastName>
<ForeName>Gaétan</ForeName>
<Initials>G</Initials>
<AffiliationInfo>
<Affiliation>Australian School of Advanced Medicine, Macquarie University, North Ryde, NSW, Australia;</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>McMorran</LastName>
<ForeName>Brendan J</ForeName>
<Initials>BJ</Initials>
<AffiliationInfo>
<Affiliation>Australian School of Advanced Medicine, Macquarie University, North Ryde, NSW, Australia;</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Foote</LastName>
<ForeName>Simon J</ForeName>
<Initials>SJ</Initials>
<AffiliationInfo>
<Affiliation>Australian School of Advanced Medicine, Macquarie University, North Ryde, NSW, Australia; The John Curtin School of Medical Research, Australian National University, Canberra, ACT, Australia.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<PublicationTypeList>
<PublicationType UI="D016428">Journal Article</PublicationType>
<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic">
<Year>2014</Year>
<Month>11</Month>
<Day>20</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>United States</Country>
<MedlineTA>Blood</MedlineTA>
<NlmUniqueID>7603509</NlmUniqueID>
<ISSNLinking>0006-4971</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D011524">Protoporphyrins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>42VZT0U6YR</RegistryNumber>
<NameOfSubstance UI="D006418">Heme</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>79236-56-9</RegistryNumber>
<NameOfSubstance UI="C028842">N-methylprotoporphyrin IX</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>EC 4.99.1.1</RegistryNumber>
<NameOfSubstance UI="D005294">Ferrochelatase</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>AIM</CitationSubset>
<CitationSubset>IM</CitationSubset>
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<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D004912" MajorTopicYN="N">Erythrocytes</DescriptorName>
<QualifierName UI="Q000201" MajorTopicYN="N">enzymology</QualifierName>
<QualifierName UI="Q000469" MajorTopicYN="Y">parasitology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D005260" MajorTopicYN="N">Female</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D005294" MajorTopicYN="N">Ferrochelatase</DescriptorName>
<QualifierName UI="Q000037" MajorTopicYN="N">antagonists & inhibitors</QualifierName>
<QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D006418" MajorTopicYN="N">Heme</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D006801" MajorTopicYN="N">Humans</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D016778" MajorTopicYN="N">Malaria, Falciparum</DescriptorName>
<QualifierName UI="Q000201" MajorTopicYN="N">enzymology</QualifierName>
<QualifierName UI="Q000469" MajorTopicYN="N">parasitology</QualifierName>
<QualifierName UI="Q000517" MajorTopicYN="Y">prevention & control</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D008297" MajorTopicYN="N">Male</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D051379" MajorTopicYN="N">Mice</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D008810" MajorTopicYN="N">Mice, Inbred C57BL</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010641" MajorTopicYN="N">Phenotype</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010962" MajorTopicYN="N">Plasmodium berghei</DescriptorName>
<QualifierName UI="Q000254" MajorTopicYN="Y">growth & development</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D046351" MajorTopicYN="N">Protoporphyria, Erythropoietic</DescriptorName>
<QualifierName UI="Q000201" MajorTopicYN="N">enzymology</QualifierName>
<QualifierName UI="Q000469" MajorTopicYN="N">parasitology</QualifierName>
<QualifierName UI="Q000517" MajorTopicYN="Y">prevention & control</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D011524" MajorTopicYN="N">Protoporphyrins</DescriptorName>
<QualifierName UI="Q000494" MajorTopicYN="N">pharmacology</QualifierName>
</MeshHeading>
</MeshHeadingList>
<OtherID Source="NLM">PMC4296013</OtherID>
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