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Levels of circumsporozoite protein in the Plasmodium oocyst determine sporozoite morphology
The sporozoite stage of the Plasmodium parasite is formed by budding from a multinucleate oocyst in the mosquito midgut. During their life, sporozoites must infect the salivary glands of the mosquito vector and the liver of the mammalian host; both events depend on the major sporozoite surface prote...
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Published in: | The EMBO journal 2002-04, Vol.21 (7), p.1586-1596 |
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creator | Thathy, Vandana Fujioka, Hisashi Gantt, Soren Nussenzweig, Ruth Nussenzweig, Victor Ménard, Robert |
description | The sporozoite stage of the
Plasmodium
parasite is formed by budding from a multinucleate oocyst in the mosquito midgut. During their life, sporozoites must infect the salivary glands of the mosquito vector and the liver of the mammalian host; both events depend on the major sporozoite surface protein, the circumsporozoite protein (CS). We previously reported that
Plasmodium berghei
oocysts in which the
CS
gene is inactivated do not form sporozoites. Here, we analyzed the ultrastructure of
P.berghei
oocyst differentiation in the wild type, recombinants that do not produce or produce reduced amounts of CS, and corresponding complemented clones. The results indicate that CS is essential for establishing polarity in the oocyst. The amounts of CS protein correlate with the extent of development of the inner membranes and associated microtubules underneath the oocyst outer membrane, which normally demarcate focal budding sites. This is a first example of a protein controlling both morphogenesis and infectivity of a parasite stage. |
doi_str_mv | 10.1093/emboj/21.7.1586 |
format | article |
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Plasmodium
parasite is formed by budding from a multinucleate oocyst in the mosquito midgut. During their life, sporozoites must infect the salivary glands of the mosquito vector and the liver of the mammalian host; both events depend on the major sporozoite surface protein, the circumsporozoite protein (CS). We previously reported that
Plasmodium berghei
oocysts in which the
CS
gene is inactivated do not form sporozoites. Here, we analyzed the ultrastructure of
P.berghei
oocyst differentiation in the wild type, recombinants that do not produce or produce reduced amounts of CS, and corresponding complemented clones. The results indicate that CS is essential for establishing polarity in the oocyst. The amounts of CS protein correlate with the extent of development of the inner membranes and associated microtubules underneath the oocyst outer membrane, which normally demarcate focal budding sites. This is a first example of a protein controlling both morphogenesis and infectivity of a parasite stage.</description><identifier>ISSN: 0261-4189</identifier><identifier>ISSN: 1460-2075</identifier><identifier>EISSN: 1460-2075</identifier><identifier>DOI: 10.1093/emboj/21.7.1586</identifier><identifier>PMID: 11927543</identifier><identifier>CODEN: EMJODG</identifier><language>eng</language><publisher>Chichester, UK: John Wiley & Sons, Ltd</publisher><subject>ACS protein ; Animals ; Anopheles ; Aquatic insects ; budding ; cell division ; circumsporozoite protein ; circumsporozoites ; EMBO05 ; EMBO23 ; Humans ; Microtubules - metabolism ; Morphogenesis ; Mosquitoes ; Mutagenesis ; Oocysts ; Parasites ; Phenotype ; Plasmodium berghei ; Plasmodium berghei - genetics ; Plasmodium berghei - metabolism ; Plasmodium berghei - ultrastructure ; Protozoan Proteins - biosynthesis ; Protozoan Proteins - genetics ; Protozoan Proteins - metabolism ; Rats ; Rats, Sprague-Dawley ; sporozoite</subject><ispartof>The EMBO journal, 2002-04, Vol.21 (7), p.1586-1596</ispartof><rights>European Molecular Biology Organization 2002</rights><rights>Copyright © 2002 European Molecular Biology Organization</rights><rights>Copyright Oxford University Press(England) Apr 01, 2002</rights><rights>Copyright © 2002 European Molecular Biology Organization 2002</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c6628-bdb37c596e5782209509b3b13cff49253d50fe33713a00165705e53d3f8aeed73</citedby></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC125957/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC125957/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/11927543$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Thathy, Vandana</creatorcontrib><creatorcontrib>Fujioka, Hisashi</creatorcontrib><creatorcontrib>Gantt, Soren</creatorcontrib><creatorcontrib>Nussenzweig, Ruth</creatorcontrib><creatorcontrib>Nussenzweig, Victor</creatorcontrib><creatorcontrib>Ménard, Robert</creatorcontrib><title>Levels of circumsporozoite protein in the Plasmodium oocyst determine sporozoite morphology</title><title>The EMBO journal</title><addtitle>EMBO J</addtitle><addtitle>EMBO J</addtitle><description>The sporozoite stage of the
Plasmodium
parasite is formed by budding from a multinucleate oocyst in the mosquito midgut. During their life, sporozoites must infect the salivary glands of the mosquito vector and the liver of the mammalian host; both events depend on the major sporozoite surface protein, the circumsporozoite protein (CS). We previously reported that
Plasmodium berghei
oocysts in which the
CS
gene is inactivated do not form sporozoites. Here, we analyzed the ultrastructure of
P.berghei
oocyst differentiation in the wild type, recombinants that do not produce or produce reduced amounts of CS, and corresponding complemented clones. The results indicate that CS is essential for establishing polarity in the oocyst. The amounts of CS protein correlate with the extent of development of the inner membranes and associated microtubules underneath the oocyst outer membrane, which normally demarcate focal budding sites. This is a first example of a protein controlling both morphogenesis and infectivity of a parasite stage.</description><subject>ACS protein</subject><subject>Animals</subject><subject>Anopheles</subject><subject>Aquatic insects</subject><subject>budding</subject><subject>cell division</subject><subject>circumsporozoite protein</subject><subject>circumsporozoites</subject><subject>EMBO05</subject><subject>EMBO23</subject><subject>Humans</subject><subject>Microtubules - metabolism</subject><subject>Morphogenesis</subject><subject>Mosquitoes</subject><subject>Mutagenesis</subject><subject>Oocysts</subject><subject>Parasites</subject><subject>Phenotype</subject><subject>Plasmodium berghei</subject><subject>Plasmodium berghei - genetics</subject><subject>Plasmodium berghei - metabolism</subject><subject>Plasmodium berghei - ultrastructure</subject><subject>Protozoan Proteins - biosynthesis</subject><subject>Protozoan Proteins - genetics</subject><subject>Protozoan Proteins - metabolism</subject><subject>Rats</subject><subject>Rats, Sprague-Dawley</subject><subject>sporozoite</subject><issn>0261-4189</issn><issn>1460-2075</issn><issn>1460-2075</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2002</creationdate><recordtype>article</recordtype><recordid>eNqFkc1v0zAYhy0EYmVw5gSKOHBL64_Yjg8cYBplUwdMfB04WE7ypnWXxMFOBt1fT7pUXUFCSJYi-X2e17_oh9BTgqcEKzaDOnPrGSVTOSU8FffQhCQCxxRLfh9NMBUkTkiqjtCjENYYY55K8hAdEaKo5AmboO8LuIYqRK6Mcuvzvg6t8-7G2Q6i1rsObBMNp1tB9LEyoXaF7evIuXwTuqiADnxtG4gOrNr5duUqt9w8Rg9KUwV4svseoy9vTz-fvIsXH-ZnJ68XcS4ETeOsyJjMuRLAZUopVhyrjGWE5WWZKMpZwXEJjEnCDMZEcIk5DLesTA1AIdkxejXubfushiKHpvOm0q23tfEb7YzVf04au9JLd60J5Ypv_Zc737sfPYRO1zbkUFWmAdcHTVKqWCLUAL74C1y73jfDv2miOOUkYXSAZiOUexeCh3IfhGC9LU3flqYp0VJvSxuM54f57_hdSwOQjsBPW8Hmf_v06cWbc8lVwmQ6qHhUw2A1S_AHkf8Z59moNKbrPeyfu1sZj3MbOvi1Hxt_pYVkkutv7-f66zy5vBCXnzRjvwFeltCU</recordid><startdate>20020401</startdate><enddate>20020401</enddate><creator>Thathy, 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of circumsporozoite protein in the Plasmodium oocyst determine sporozoite morphology</title><author>Thathy, Vandana ; Fujioka, Hisashi ; Gantt, Soren ; Nussenzweig, Ruth ; Nussenzweig, Victor ; Ménard, Robert</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c6628-bdb37c596e5782209509b3b13cff49253d50fe33713a00165705e53d3f8aeed73</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2002</creationdate><topic>ACS protein</topic><topic>Animals</topic><topic>Anopheles</topic><topic>Aquatic insects</topic><topic>budding</topic><topic>cell division</topic><topic>circumsporozoite protein</topic><topic>circumsporozoites</topic><topic>EMBO05</topic><topic>EMBO23</topic><topic>Humans</topic><topic>Microtubules - metabolism</topic><topic>Morphogenesis</topic><topic>Mosquitoes</topic><topic>Mutagenesis</topic><topic>Oocysts</topic><topic>Parasites</topic><topic>Phenotype</topic><topic>Plasmodium berghei</topic><topic>Plasmodium berghei - genetics</topic><topic>Plasmodium berghei - metabolism</topic><topic>Plasmodium berghei - ultrastructure</topic><topic>Protozoan Proteins - biosynthesis</topic><topic>Protozoan Proteins - genetics</topic><topic>Protozoan Proteins - metabolism</topic><topic>Rats</topic><topic>Rats, Sprague-Dawley</topic><topic>sporozoite</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Thathy, Vandana</creatorcontrib><creatorcontrib>Fujioka, Hisashi</creatorcontrib><creatorcontrib>Gantt, Soren</creatorcontrib><creatorcontrib>Nussenzweig, Ruth</creatorcontrib><creatorcontrib>Nussenzweig, Victor</creatorcontrib><creatorcontrib>Ménard, Robert</creatorcontrib><collection>Istex</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE 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J</addtitle><date>2002-04-01</date><risdate>2002</risdate><volume>21</volume><issue>7</issue><spage>1586</spage><epage>1596</epage><pages>1586-1596</pages><issn>0261-4189</issn><issn>1460-2075</issn><eissn>1460-2075</eissn><coden>EMJODG</coden><abstract>The sporozoite stage of the
Plasmodium
parasite is formed by budding from a multinucleate oocyst in the mosquito midgut. During their life, sporozoites must infect the salivary glands of the mosquito vector and the liver of the mammalian host; both events depend on the major sporozoite surface protein, the circumsporozoite protein (CS). We previously reported that
Plasmodium berghei
oocysts in which the
CS
gene is inactivated do not form sporozoites. Here, we analyzed the ultrastructure of
P.berghei
oocyst differentiation in the wild type, recombinants that do not produce or produce reduced amounts of CS, and corresponding complemented clones. The results indicate that CS is essential for establishing polarity in the oocyst. The amounts of CS protein correlate with the extent of development of the inner membranes and associated microtubules underneath the oocyst outer membrane, which normally demarcate focal budding sites. This is a first example of a protein controlling both morphogenesis and infectivity of a parasite stage.</abstract><cop>Chichester, UK</cop><pub>John Wiley & Sons, Ltd</pub><pmid>11927543</pmid><doi>10.1093/emboj/21.7.1586</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record> |
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subjects | ACS protein Animals Anopheles Aquatic insects budding cell division circumsporozoite protein circumsporozoites EMBO05 EMBO23 Humans Microtubules - metabolism Morphogenesis Mosquitoes Mutagenesis Oocysts Parasites Phenotype Plasmodium berghei Plasmodium berghei - genetics Plasmodium berghei - metabolism Plasmodium berghei - ultrastructure Protozoan Proteins - biosynthesis Protozoan Proteins - genetics Protozoan Proteins - metabolism Rats Rats, Sprague-Dawley sporozoite |
title | Levels of circumsporozoite protein in the Plasmodium oocyst determine sporozoite morphology |
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