Determinants for resistance and susceptibility to microfilaraemia in Litomosoides sigmodontis filariasis
Filarial infections of humans are chronic diseases. Despite an ongoing immune response, adult filariae continuously produce their offspring, the microfilariae (Mf), which are able to persist in sufficient numbers to ensure transmission. In this study, host- and parasite-derived factors, which contri...
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| Veröffentlicht in: | Parasitology 2001-06, Vol.122 (6), p.641-649 |
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| creator | HOFFMANN, W. H. PFAFF, A. W. SCHULZ-KEY, H. SOBOSLAV, P. T. |
| description | Filarial infections of humans are chronic diseases. Despite an ongoing immune response, adult filariae continuously produce their offspring, the microfilariae (Mf), which are able to persist in sufficient numbers to ensure transmission. In this study, host- and parasite-derived factors, which contribute to persistence of Mf, were investigated using the filariasis model of Litomosoides sigmodontis in mice. Different strains of mice were found to differ widely in their capability to eliminate circulating Mf. Studies of congenic mouse strains showed that early and rapid clearance of Mf was mediated by activation pathways relevant to innate immunity, whereas late or delayed clearance of Mf was pre-determined by MHC-related factors. Genetic knock-out of genes for the MHC class-II molecules totally abrogated resistance. Most interestingly, the presence of only 1 adult female, but not male worms, renders all mice susceptible, irrespective of the genetic background, enabling Mf to circulate for extended periods of time. Such prolonged microfilaraemia was also observed in L. sigmodontis-infected animals challenged with heterologous Mf of Acanthocheilonema viteae. The use of cytokine gene knock-out mice showed that persistence of L. sigmodontis Mf was facilitated by IL-10, but not by IL-4 or IFN-γ. In conclusion, irrespective of a resistant or susceptible host genetic background, survival of Mf of L. sigmodontis in mice is decisively regulated by the presence of adult female L. sigmodontis which will skew and exploit immune responses to facilitate the survival and persistence of their offspring in the infected host. |
| doi_str_mv | 10.1017/S0031182001007892 |
| format | Article |
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H. ; PFAFF, A. W. ; SCHULZ-KEY, H. ; SOBOSLAV, P. T.</creator><creatorcontrib>HOFFMANN, W. H. ; PFAFF, A. W. ; SCHULZ-KEY, H. ; SOBOSLAV, P. T.</creatorcontrib><description>Filarial infections of humans are chronic diseases. Despite an ongoing immune response, adult filariae continuously produce their offspring, the microfilariae (Mf), which are able to persist in sufficient numbers to ensure transmission. In this study, host- and parasite-derived factors, which contribute to persistence of Mf, were investigated using the filariasis model of Litomosoides sigmodontis in mice. Different strains of mice were found to differ widely in their capability to eliminate circulating Mf. Studies of congenic mouse strains showed that early and rapid clearance of Mf was mediated by activation pathways relevant to innate immunity, whereas late or delayed clearance of Mf was pre-determined by MHC-related factors. Genetic knock-out of genes for the MHC class-II molecules totally abrogated resistance. Most interestingly, the presence of only 1 adult female, but not male worms, renders all mice susceptible, irrespective of the genetic background, enabling Mf to circulate for extended periods of time. Such prolonged microfilaraemia was also observed in L. sigmodontis-infected animals challenged with heterologous Mf of Acanthocheilonema viteae. The use of cytokine gene knock-out mice showed that persistence of L. sigmodontis Mf was facilitated by IL-10, but not by IL-4 or IFN-γ. In conclusion, irrespective of a resistant or susceptible host genetic background, survival of Mf of L. sigmodontis in mice is decisively regulated by the presence of adult female L. sigmodontis which will skew and exploit immune responses to facilitate the survival and persistence of their offspring in the infected host.</description><identifier>ISSN: 0031-1820</identifier><identifier>EISSN: 1469-8161</identifier><identifier>DOI: 10.1017/S0031182001007892</identifier><identifier>PMID: 11444617</identifier><identifier>CODEN: PARAAE</identifier><language>eng</language><publisher>Cambridge, UK: Cambridge University Press</publisher><subject>Animals ; Antibodies, Helminth - analysis ; Biological and medical sciences ; Cells ; congenic and knock-out mice ; Cytokines ; Cytokines - biosynthesis ; Female ; Females ; filariasis ; Filariasis - immunology ; Filariasis - parasitology ; Filarioidea - growth & development ; Filarioidea - immunology ; Fundamental and applied biological sciences. Psychology ; Genes, MHC Class II - immunology ; Host parasite relation; pathogenicity ; Host-Parasite Interactions - immunology ; immune modulation ; Immune response ; Immunity, Innate - genetics ; Immunity, Innate - immunology ; Immunization ; Interleukin-10 - biosynthesis ; Interleukin-10 - immunology ; Invertebrates ; Investigations ; Litomosoides sigmodontis ; Male ; Mice ; Mice, Inbred BALB C ; Mice, Inbred C3H ; Mice, Inbred C57BL ; Mice, Inbred DBA ; Mice, Knockout - genetics ; Mice, Knockout - parasitology ; microfilaraemia ; Microfilariae - growth & development ; Microfilariae - immunology ; Nemathelminthia. Plathelmintha ; Offspring ; parasite persistence ; Parasitemia - immunology ; Parasitemia - parasitology ; Parasites ; Rodents ; Spleen - parasitology ; Tropical diseases ; Worms</subject><ispartof>Parasitology, 2001-06, Vol.122 (6), p.641-649</ispartof><rights>2001 Cambridge University Press</rights><rights>2001 INIST-CNRS</rights><rights>Copyright Cambridge University Press Jun 2001</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c483t-68f95a30bf5a5e9d085ecada1ec205bda7751ddfd1db8334a54de5a8903d9743</citedby><cites>FETCH-LOGICAL-c483t-68f95a30bf5a5e9d085ecada1ec205bda7751ddfd1db8334a54de5a8903d9743</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.cambridge.org/core/product/identifier/S0031182001007892/type/journal_article$$EHTML$$P50$$Gcambridge$$H</linktohtml><link.rule.ids>164,314,780,784,27923,27924,55627</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=1059433$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/11444617$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>HOFFMANN, W. H.</creatorcontrib><creatorcontrib>PFAFF, A. W.</creatorcontrib><creatorcontrib>SCHULZ-KEY, H.</creatorcontrib><creatorcontrib>SOBOSLAV, P. T.</creatorcontrib><title>Determinants for resistance and susceptibility to microfilaraemia in Litomosoides sigmodontis filariasis</title><title>Parasitology</title><addtitle>Parasitology</addtitle><description>Filarial infections of humans are chronic diseases. Despite an ongoing immune response, adult filariae continuously produce their offspring, the microfilariae (Mf), which are able to persist in sufficient numbers to ensure transmission. In this study, host- and parasite-derived factors, which contribute to persistence of Mf, were investigated using the filariasis model of Litomosoides sigmodontis in mice. Different strains of mice were found to differ widely in their capability to eliminate circulating Mf. Studies of congenic mouse strains showed that early and rapid clearance of Mf was mediated by activation pathways relevant to innate immunity, whereas late or delayed clearance of Mf was pre-determined by MHC-related factors. Genetic knock-out of genes for the MHC class-II molecules totally abrogated resistance. Most interestingly, the presence of only 1 adult female, but not male worms, renders all mice susceptible, irrespective of the genetic background, enabling Mf to circulate for extended periods of time. Such prolonged microfilaraemia was also observed in L. sigmodontis-infected animals challenged with heterologous Mf of Acanthocheilonema viteae. The use of cytokine gene knock-out mice showed that persistence of L. sigmodontis Mf was facilitated by IL-10, but not by IL-4 or IFN-γ. In conclusion, irrespective of a resistant or susceptible host genetic background, survival of Mf of L. sigmodontis in mice is decisively regulated by the presence of adult female L. sigmodontis which will skew and exploit immune responses to facilitate the survival and persistence of their offspring in the infected host.</description><subject>Animals</subject><subject>Antibodies, Helminth - analysis</subject><subject>Biological and medical sciences</subject><subject>Cells</subject><subject>congenic and knock-out mice</subject><subject>Cytokines</subject><subject>Cytokines - biosynthesis</subject><subject>Female</subject><subject>Females</subject><subject>filariasis</subject><subject>Filariasis - immunology</subject><subject>Filariasis - parasitology</subject><subject>Filarioidea - growth & development</subject><subject>Filarioidea - immunology</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Genes, MHC Class II - immunology</subject><subject>Host parasite relation; pathogenicity</subject><subject>Host-Parasite Interactions - immunology</subject><subject>immune modulation</subject><subject>Immune response</subject><subject>Immunity, Innate - genetics</subject><subject>Immunity, Innate - immunology</subject><subject>Immunization</subject><subject>Interleukin-10 - biosynthesis</subject><subject>Interleukin-10 - immunology</subject><subject>Invertebrates</subject><subject>Investigations</subject><subject>Litomosoides sigmodontis</subject><subject>Male</subject><subject>Mice</subject><subject>Mice, Inbred BALB C</subject><subject>Mice, Inbred C3H</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Inbred DBA</subject><subject>Mice, Knockout - genetics</subject><subject>Mice, Knockout - parasitology</subject><subject>microfilaraemia</subject><subject>Microfilariae - growth & development</subject><subject>Microfilariae - immunology</subject><subject>Nemathelminthia. Plathelmintha</subject><subject>Offspring</subject><subject>parasite persistence</subject><subject>Parasitemia - immunology</subject><subject>Parasitemia - parasitology</subject><subject>Parasites</subject><subject>Rodents</subject><subject>Spleen - parasitology</subject><subject>Tropical diseases</subject><subject>Worms</subject><issn>0031-1820</issn><issn>1469-8161</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2001</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><recordid>eNp1kUFv1DAQhS0EotvCD-CCIoR6C4xjO7aP0NKCtBKg9sTFmsROcUnire1I9N_j1UYUgTjN4X3z9GYeIS8ovKFA5dsrAEapagAogFS6eUQ2lLe6VrSlj8lmL9d7_Ygcp3QLAC1rm6fkiFLOeUvlhnw_d9nFyc8451QNIVbRJZ8yzr2rcLZVWlLvdtl3fvT5vsqhmnwfw-BHjOgmj5Wfq63PYQopeOtSlfzNFGyYsy-Ge8xjcXxGngw4Jvd8nSfk-uLD9dnHevv58tPZu23dc8Vy3apBC2TQDQKF0xaUcD1apK5vQHQWpRTU2sFS2ynGOApunUClgVktOTshpwfbXQx3i0vZTL4cMI44u7AkI0Er0NAU8NVf4G1Y4lyimab8sBFNqwpED1C5OKXoBrOLfsJ4byiYfQXmnwrKzsvVeOkmZx821p8X4PUKYOpxHGL5tU9_OAvNGStYfcBKG-7nbxnjD9NKJoVpL7-aK_5Nv7_4Isx54dmaFacuenvjHi76f9pfz_quOw</recordid><startdate>20010601</startdate><enddate>20010601</enddate><creator>HOFFMANN, W. 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H. ; PFAFF, A. W. ; SCHULZ-KEY, H. ; SOBOSLAV, P. T.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c483t-68f95a30bf5a5e9d085ecada1ec205bda7751ddfd1db8334a54de5a8903d9743</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2001</creationdate><topic>Animals</topic><topic>Antibodies, Helminth - analysis</topic><topic>Biological and medical sciences</topic><topic>Cells</topic><topic>congenic and knock-out mice</topic><topic>Cytokines</topic><topic>Cytokines - biosynthesis</topic><topic>Female</topic><topic>Females</topic><topic>filariasis</topic><topic>Filariasis - immunology</topic><topic>Filariasis - parasitology</topic><topic>Filarioidea - growth & development</topic><topic>Filarioidea - immunology</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Genes, MHC Class II - immunology</topic><topic>Host parasite relation; pathogenicity</topic><topic>Host-Parasite Interactions - immunology</topic><topic>immune modulation</topic><topic>Immune response</topic><topic>Immunity, Innate - genetics</topic><topic>Immunity, Innate - immunology</topic><topic>Immunization</topic><topic>Interleukin-10 - biosynthesis</topic><topic>Interleukin-10 - immunology</topic><topic>Invertebrates</topic><topic>Investigations</topic><topic>Litomosoides sigmodontis</topic><topic>Male</topic><topic>Mice</topic><topic>Mice, Inbred BALB C</topic><topic>Mice, Inbred C3H</topic><topic>Mice, Inbred C57BL</topic><topic>Mice, Inbred DBA</topic><topic>Mice, Knockout - genetics</topic><topic>Mice, Knockout - parasitology</topic><topic>microfilaraemia</topic><topic>Microfilariae - growth & development</topic><topic>Microfilariae - immunology</topic><topic>Nemathelminthia. Plathelmintha</topic><topic>Offspring</topic><topic>parasite persistence</topic><topic>Parasitemia - immunology</topic><topic>Parasitemia - parasitology</topic><topic>Parasites</topic><topic>Rodents</topic><topic>Spleen - parasitology</topic><topic>Tropical diseases</topic><topic>Worms</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>HOFFMANN, W. H.</creatorcontrib><creatorcontrib>PFAFF, A. W.</creatorcontrib><creatorcontrib>SCHULZ-KEY, H.</creatorcontrib><creatorcontrib>SOBOSLAV, P. 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H.</au><au>PFAFF, A. W.</au><au>SCHULZ-KEY, H.</au><au>SOBOSLAV, P. T.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Determinants for resistance and susceptibility to microfilaraemia in Litomosoides sigmodontis filariasis</atitle><jtitle>Parasitology</jtitle><addtitle>Parasitology</addtitle><date>2001-06-01</date><risdate>2001</risdate><volume>122</volume><issue>6</issue><spage>641</spage><epage>649</epage><pages>641-649</pages><issn>0031-1820</issn><eissn>1469-8161</eissn><coden>PARAAE</coden><abstract>Filarial infections of humans are chronic diseases. Despite an ongoing immune response, adult filariae continuously produce their offspring, the microfilariae (Mf), which are able to persist in sufficient numbers to ensure transmission. In this study, host- and parasite-derived factors, which contribute to persistence of Mf, were investigated using the filariasis model of Litomosoides sigmodontis in mice. Different strains of mice were found to differ widely in their capability to eliminate circulating Mf. Studies of congenic mouse strains showed that early and rapid clearance of Mf was mediated by activation pathways relevant to innate immunity, whereas late or delayed clearance of Mf was pre-determined by MHC-related factors. Genetic knock-out of genes for the MHC class-II molecules totally abrogated resistance. Most interestingly, the presence of only 1 adult female, but not male worms, renders all mice susceptible, irrespective of the genetic background, enabling Mf to circulate for extended periods of time. Such prolonged microfilaraemia was also observed in L. sigmodontis-infected animals challenged with heterologous Mf of Acanthocheilonema viteae. The use of cytokine gene knock-out mice showed that persistence of L. sigmodontis Mf was facilitated by IL-10, but not by IL-4 or IFN-γ. In conclusion, irrespective of a resistant or susceptible host genetic background, survival of Mf of L. sigmodontis in mice is decisively regulated by the presence of adult female L. sigmodontis which will skew and exploit immune responses to facilitate the survival and persistence of their offspring in the infected host.</abstract><cop>Cambridge, UK</cop><pub>Cambridge University Press</pub><pmid>11444617</pmid><doi>10.1017/S0031182001007892</doi><tpages>9</tpages></addata></record> |
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| ispartof | Parasitology, 2001-06, Vol.122 (6), p.641-649 |
| issn | 0031-1820 1469-8161 |
| language | eng |
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| subjects | Animals Antibodies, Helminth - analysis Biological and medical sciences Cells congenic and knock-out mice Cytokines Cytokines - biosynthesis Female Females filariasis Filariasis - immunology Filariasis - parasitology Filarioidea - growth & development Filarioidea - immunology Fundamental and applied biological sciences. Psychology Genes, MHC Class II - immunology Host parasite relation pathogenicity Host-Parasite Interactions - immunology immune modulation Immune response Immunity, Innate - genetics Immunity, Innate - immunology Immunization Interleukin-10 - biosynthesis Interleukin-10 - immunology Invertebrates Investigations Litomosoides sigmodontis Male Mice Mice, Inbred BALB C Mice, Inbred C3H Mice, Inbred C57BL Mice, Inbred DBA Mice, Knockout - genetics Mice, Knockout - parasitology microfilaraemia Microfilariae - growth & development Microfilariae - immunology Nemathelminthia. Plathelmintha Offspring parasite persistence Parasitemia - immunology Parasitemia - parasitology Parasites Rodents Spleen - parasitology Tropical diseases Worms |
| title | Determinants for resistance and susceptibility to microfilaraemia in Litomosoides sigmodontis filariasis |
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