Protein O-fucosyltransferase 2–mediated O-glycosylation of the adhesin MIC2 is dispensable for Toxoplasma gondii tachyzoite infection

Toxoplasma gondii is a ubiquitous, obligate intracellular eukaryotic parasite that causes congenital birth defects, disease in immunocompromised individuals, and blindness. Protein glycosylation plays an important role in the infectivity and evasion of immune responses of many eukaryotic parasites a...

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Published inThe Journal of biological chemistry Vol. 294; no. 5; pp. 1541 - 1553
Main Authors Khurana, Sachin, Coffey, Michael J., John, Alan, Uboldi, Alessandro D., Huynh, My-Hang, Stewart, Rebecca J., Carruthers, Vern B., Tonkin, Christopher J., Goddard-Borger, Ethan D., Scott, Nichollas E.
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 01.02.2019
American Society for Biochemistry and Molecular Biology
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Abstract Toxoplasma gondii is a ubiquitous, obligate intracellular eukaryotic parasite that causes congenital birth defects, disease in immunocompromised individuals, and blindness. Protein glycosylation plays an important role in the infectivity and evasion of immune responses of many eukaryotic parasites and is also of great relevance to vaccine design. Here we demonstrate that micronemal protein 2 (MIC2), a motility-associated adhesin of T. gondii, has highly glycosylated thrombospondin repeat (TSR) domains. Using affinity-purified MIC2 and MS/MS analysis along with enzymatic digestion assays, we observed that at least seven C-linked and three O-linked glycosylation sites exist within MIC2, with >95% occupancy at these O-glycosylation sites. We found that addition of O-glycans to MIC2 is mediated by a protein O-fucosyltransferase 2 homolog (TgPOFUT2) encoded by the TGGT1_273550 gene. Even though POFUT2 homologs are important for stabilizing motility-associated adhesins and for host infection in other apicomplexan parasites, loss of TgPOFUT2 in T. gondii had only a modest impact on MIC2 levels and the wider parasite proteome. Consistent with this, both plaque formation and tachyzoite invasion were broadly similar in the presence or absence of TgPOFUT2. These findings indicate that TgPOFUT2 O-glycosylates MIC2 and that this glycan, in contrast to previous findings in another study, is dispensable in T. gondii tachyzoites and for T. gondii infectivity.
AbstractList Toxoplasma gondii is a ubiquitous, obligate intracellular eukaryotic parasite that causes congenital birth defects, disease in immunocompromised individuals, and blindness. Protein glycosylation plays an important role in the infectivity and evasion of immune responses of many eukaryotic parasites and is also of great relevance to vaccine design. Here we demonstrate that micronemal protein 2 (MIC2), a motility-associated adhesin of T. gondii , has highly glycosylated thrombospondin repeat (TSR) domains. Using affinity-purified MIC2 and MS/MS analysis along with enzymatic digestion assays, we observed that at least seven C- linked and three O -linked glycosylation sites exist within MIC2, with >95% occupancy at these O -glycosylation sites. We found that addition of O -glycans to MIC2 is mediated by a protein O -fucosyltransferase 2 homolog (TgPOFUT2) encoded by the TGGT1 _ 273550 gene. Even though POFUT2 homologs are important for stabilizing motility-associated adhesins and for host infection in other apicomplexan parasites, loss of TgPOFUT2 in T. gondii had only a modest impact on MIC2 levels and the wider parasite proteome. Consistent with this, both plaque formation and tachyzoite invasion were broadly similar in the presence or absence of TgPOFUT2. These findings indicate that TgPOFUT2 O- glycosylates MIC2 and that this glycan, in contrast to previous findings in another study, is dispensable in T. gondii tachyzoites and for T. gondii infectivity.
Toxoplasma gondii is a ubiquitous, obligate intracellular eukaryotic parasite that causes congenital birth defects, disease in immunocompromised individuals, and blindness. Protein glycosylation plays an important role in the infectivity and evasion of immune responses of many eukaryotic parasites and is also of great relevance to vaccine design. Here we demonstrate that micronemal protein 2 (MIC2), a motility-associated adhesin of T. gondii, has highly glycosylated thrombospondin repeat (TSR) domains. Using affinity-purified MIC2 and MS/MS analysis along with enzymatic digestion assays, we observed that at least seven C-linked and three O-linked glycosylation sites exist within MIC2, with >95% occupancy at these O-glycosylation sites. We found that addition of O-glycans to MIC2 is mediated by a protein O-fucosyltransferase 2 homolog (TgPOFUT2) encoded by the TGGT1_273550 gene. Even though POFUT2 homologs are important for stabilizing motility-associated adhesins and for host infection in other apicomplexan parasites, loss of TgPOFUT2 in T. gondii had only a modest impact on MIC2 levels and the wider parasite proteome. Consistent with this, both plaque formation and tachyzoite invasion were broadly similar in the presence or absence of TgPOFUT2. These findings indicate that TgPOFUT2 O-glycosylates MIC2 and that this glycan, in contrast to previous findings in another study, is dispensable in T. gondii tachyzoites and for T. gondii infectivity.
is a ubiquitous, obligate intracellular eukaryotic parasite that causes congenital birth defects, disease in immunocompromised individuals, and blindness. Protein glycosylation plays an important role in the infectivity and evasion of immune responses of many eukaryotic parasites and is also of great relevance to vaccine design. Here we demonstrate that micronemal protein 2 (MIC2), a motility-associated adhesin of , has highly glycosylated thrombospondin repeat (TSR) domains. Using affinity-purified MIC2 and MS/MS analysis along with enzymatic digestion assays, we observed that at least seven linked and three -linked glycosylation sites exist within MIC2, with >95% occupancy at these -glycosylation sites. We found that addition of -glycans to MIC2 is mediated by a protein -fucosyltransferase 2 homolog (TgPOFUT2) encoded by the _ gene. Even though POFUT2 homologs are important for stabilizing motility-associated adhesins and for host infection in other apicomplexan parasites, loss of TgPOFUT2 in had only a modest impact on MIC2 levels and the wider parasite proteome. Consistent with this, both plaque formation and tachyzoite invasion were broadly similar in the presence or absence of TgPOFUT2. These findings indicate that TgPOFUT2 glycosylates MIC2 and that this glycan, in contrast to previous findings in another study, is dispensable in tachyzoites and for infectivity.
Author Khurana, Sachin
Stewart, Rebecca J.
Tonkin, Christopher J.
John, Alan
Scott, Nichollas E.
Coffey, Michael J.
Goddard-Borger, Ethan D.
Huynh, My-Hang
Carruthers, Vern B.
Uboldi, Alessandro D.
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  organization: Department of Microbiology and Immunology, University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Parkville, Victoria 3010, Australia
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Issue 5
Keywords glycosylation
fucosyltransferase
Toxoplasma gondii
proteomics
MS
Language English
License This is an open access article under the CC BY license.
2019 Khurana et al.
Published under exclusive license by The American Society for Biochemistry and Molecular Biology, Inc.
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Both authors contributed equally to this work.
Edited by Gerald W. Hart
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Snippet Toxoplasma gondii is a ubiquitous, obligate intracellular eukaryotic parasite that causes congenital birth defects, disease in immunocompromised individuals,...
is a ubiquitous, obligate intracellular eukaryotic parasite that causes congenital birth defects, disease in immunocompromised individuals, and blindness....
Toxoplasma gondii is a ubiquitous, obligate intracellular eukaryotic parasite that causes congenital birth defects, disease in immunocompromised individuals,...
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SubjectTerms Cells, Cultured
Fibroblasts - cytology
Fibroblasts - metabolism
Fibroblasts - parasitology
fucosyltransferase
Fucosyltransferases - metabolism
Glycobiology and Extracellular Matrices
Glycosylation
Host-Parasite Interactions
Humans
Membrane Proteins - metabolism
Proteome - analysis
proteomics
Protozoan Proteins - metabolism
Toxoplasma - pathogenicity
Toxoplasma gondii
Toxoplasmosis - metabolism
Toxoplasmosis - parasitology
Title Protein O-fucosyltransferase 2–mediated O-glycosylation of the adhesin MIC2 is dispensable for Toxoplasma gondii tachyzoite infection
URI https://dx.doi.org/10.1074/jbc.RA118.005357
https://www.ncbi.nlm.nih.gov/pubmed/30514763
https://search.proquest.com/docview/2150525934
https://pubmed.ncbi.nlm.nih.gov/PMC6364784
Volume 294
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