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Microarray assessment of N-glycan-specific IgE and IgG profiles associated with Schistosoma mansoni infection in rural and urban Uganda

Nkurunungi, Gyaviira, van Diepen, Angela, Nassuuna, Jacent, Sanya, Richard E., Nampijja, Margaret, Nambuya, Irene, Kabagenyi, Joyce, Serna, Sonia, Reichardt, Niels-Christian, van Ree, Ronald, Webb, Emily L., Elliott, Alison M., Yazdanbakhsh, Maria, Hokke, Cornelis H.·2019·Scientific Reports
DOI 10.1038/s41598-019-40009-7PMC PMC6401159
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Abstract

Core β-1,2-xylose and α-1,3-fucose are antigenic motifs on schistosome N-glycans, as well as prominent IgE targets on some plant and insect glycoproteins. To map the association of schistosome infection with responses to these motifs, we assessed plasma IgE and IgG reactivity using microarray technology among Ugandans from rural Schistosoma mansoni(Sm)-endemic islands (n = 209), and from proximate urban communities with lower Sm exposure (n = 62). IgE and IgG responses to core β-1,2-xylose and α-1,3-fucose modified N-glycans were higher in rural versus urban participants. Among rural participants, IgE and IgG to core β-1,2-xylose were positively associated with Sm infection and concentration peaks coincided with the infection intensity peak in early adolescence. Responses to core α-1,3-fucose were elevated regardless of Sm infection status and peaked before the infection peak. Among urban participants,Sm infection intensity was predominantly light and positively associated with responses to both motifs. Principal component and hierarchical cluster analysis reduced the data to a set of variables that captured core β-1,2-xylose- and α-1,3-fucose-specific responses, and confirmed associations with Sm and the rural environment. Responses to core β-1,2-xylose and α-1,3-fucose have distinctive relationships with Sm infection and intensity that should further be explored for associations with protective immunity, and cross-reactivity with other exposures.

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Figure 1 Non-mammalian carbohydrate substitutions on the N-glycan core. Non-mammalian monosaccharide substitutions are denoted by blue brackets. ±implies that motifs in brackets are present or absent in different species. Figure drawn using GlycoWorkbench software, version 2.1 (European Carbohydrates Database Project).
Figure 1 Non-mammalian carbohydrate substitutions on the N-glycan core. Non-mammalian monosaccharide substitutions are denoted by blue brackets. ±implies that motifs in brackets are present or absent in different species. Figure drawn using GlycoWorkbench software, version 2.1 (European Carbohydrates Database Project).CC BY · PubMed Central
Figure 2 Associations between S. mansoni infection and IgE and IgG reactivity to N-glycans carrying non-mammalian core modifications. Plasma from S. mansoni infected and uninfected rural and urban individuals were assessed for IgE and IgG reactivity to N-glycan structural variants with and without α-1,3-fucosylation and β-1,2-xylosylation, on a microarray platform. Box-and-whisker plots show background-subtracted and log2-transformed median fluorescence intensities (MFI) representing IgE (a–c,g,h) and IgG (d–f,i,j) reactivity to the Man3GlcNAc2 core structure (G42) and to α3Fuc- and/or β2Xyl-carrying Man3GlcNAc2 core structures (G34, G73 and G37). The plots show a horizontal line denoting the median, a box indicating the interquartile range (IQR), and whiskers drawn using the Tukey method (1.5 times IQR). Outliers (greater than 1.5 times IQR away from the median) are plotted as individual points. Mann-Whitney (IgE responses) and unpaired t test (IgG responses) were conducted within the framework of a Monte Carlo simulation algorithm based on 1000 permutations (in order to adjust for multiple testing), to assess differences between infected and uninfected individuals. The Kruskal-Wallis (IgE responses) and one-way ANOVA test (IgG responses) were also conducted using the permutation approach to assess differences along the infection intensity gradient (b and e) in the rural survey. #Infection prevalence and intensity was relatively low in the urban survey so analysis by Sm intensity is not shown for the urban setting. *p < 0.05; **p < 0.01; ***p < 0.001. Sm: S. mansoni infection determined by detection of eggs in a single stool sample by Kato-Katz and/or PCR (rural infected n = 84, uninfected n = 113; urban infected n = 6, uninfected n = 42); CCA: S. mansoni infection determined by a positive urine circulating cathodic antigen (CCA) result (rural infected n = 118, uninfected n = 81; urban infected n = 21, uninfected n = 37).
Figure 2 Associations between S. mansoni infection and IgE and IgG reactivity to N-glycans carrying non-mammalian core modifications. Plasma from S. mansoni infected and uninfected rural and urban individuals were assessed for IgE and IgG reactivity to N-glycan structural variants with and without α-1,3-fucosylation and β-1,2-xylosylation, on a microarray platform. Box-and-whisker plots show background-subtracted and log2-transformed median fluorescence intensities (MFI) representing IgE (a–c,g,h) and IgG (d–f,i,j) reactivity to the Man3GlcNAc2 core structure (G42) and to α3Fuc- and/or β2Xyl-carrying Man3GlcNAc2 core structures (G34, G73 and G37). The plots show a horizontal line denoting the median, a box indicating the interquartile range (IQR), and whiskers drawn using the Tukey method (1.5 times IQR). Outliers (greater than 1.5 times IQR away from the median) are plotted as individual points. Mann-Whitney (IgE responses) and unpaired t test (IgG responses) were conducted within the framework of a Monte Carlo simulation algorithm based on 1000 permutations (in order to adjust for multiple testing), to assess differences between infected and uninfected individuals. The Kruskal-Wallis (IgE responses) and one-way ANOVA test (IgG responses) were also conducted using the permutation approach to assess differences along the infection intensity gradient (b and e) in the rural survey. #Infection prevalence and intensity was relatively low in the urban survey so analysis by Sm intensity is not shown for the urban setting. *p < 0.05; **p < 0.01; ***p < 0.001. Sm: S. mansoni infection determined by detection of eggs in a single stool sample by Kato-Katz and/or PCR (rural infected n = 84, uninfected n = 113; urban infected n = 6, uninfected n = 42); CCA: S. mansoni infection determined by a positive urine circulating cathodic antigen (CCA) result (rural infected n = 118, uninfected n = 81; urban infected n = 21, uninfected n = 37).CC BY · PubMed Central
Figure 3 Age-stratified prevalence of S. mansoni infection and median IgE and IgG reactivity to SWA, SEA and α-1,3-fucosylated and β-1,2-xylosylated N-glycans. (a,e) Rural and urban prevalence and intensity of S. mansoni infection, by age group. (b,f) Median IgG, IgG4 and IgE reactivity to SWA and SEA, by age group, among rural and urban participants, respectively. (c,g) Median IgE reactivity to the Man3GlcNAc2 core and to α3Fuc- and/or β2Xyl modified Man3GlcNAc2 core structures, by age group, among rural and urban participants, respectively. Plotted results are from all participants, irrespective of Sm infection status. (d,h) Median IgG reactivity to the Man3GlcNAc2 core and to α3Fuc- and/or β2Xyl-modified Man3GlcNAc2 core structures, by age group, among rural and urban participants, respectively. Plotted results are from all participants, irrespective of Sm infection status. CCA: S. mansoni infection determined by a positive urine circulating cathodic antigen (CCA) result; KK: S. mansoni infection determined by detection of eggs in a single stool sample by Kato-Katz (KK); epg: Eggs per gram of stool; SWA: Schistosoma adult worm antigen; SEA: Schistosoma egg antigen.
Figure 3 Age-stratified prevalence of S. mansoni infection and median IgE and IgG reactivity to SWA, SEA and α-1,3-fucosylated and β-1,2-xylosylated N-glycans. (a,e) Rural and urban prevalence and intensity of S. mansoni infection, by age group. (b,f) Median IgG, IgG4 and IgE reactivity to SWA and SEA, by age group, among rural and urban participants, respectively. (c,g) Median IgE reactivity to the Man3GlcNAc2 core and to α3Fuc- and/or β2Xyl modified Man3GlcNAc2 core structures, by age group, among rural and urban participants, respectively. Plotted results are from all participants, irrespective of Sm infection status. (d,h) Median IgG reactivity to the Man3GlcNAc2 core and to α3Fuc- and/or β2Xyl-modified Man3GlcNAc2 core structures, by age group, among rural and urban participants, respectively. Plotted results are from all participants, irrespective of Sm infection status. CCA: S. mansoni infection determined by a positive urine circulating cathodic antigen (CCA) result; KK: S. mansoni infection determined by detection of eggs in a single stool sample by Kato-Katz (KK); epg: Eggs per gram of stool; SWA: Schistosoma adult worm antigen; SEA: Schistosoma egg antigen.CC BY · PubMed Central
Figure 4 Principal component analysis of anti-glycan antibody responses. Scatterplots of first (PC1) and second factor (PC2) loadings derived from principal component analysis of IgE and IgG responses to 135 synthetic N-glycans. Box-and-whisker plots show comparison of PC1 and PC2 scores between S. mansoni infected and uninfected individuals. The plots show a horizontal line denoting the median, a box indicating the interquartile range (IQR), and whiskers drawn using the Tukey method (1.5 times IQR). Outliers (greater than 1.5 times IQR away from the median) are plotted as individual points. Panels a and b show IgE and IgG profiles, respectively, among rural participants. Panels c and d show IgE and IgG profiles, respectively, among urban participants. Associations between factor loading scores and S. mansoni infection and intensity were assessed by linear regression analysis in Stata 13.1. Crude and age- and sex-adjusted p values are shown for significant associations. All analyses were adjusted for survey design using the ‘svy’ command in Stata. PC1: Principal Component 1; PC2: Principal Component 2; Sm: S. mansoni infection determined by detection of eggs in a single stool sample by Kato-Katz and/or PCR (rural infected n = 84, uninfected n = 113; urban infected n = 6, uninfected n = 42); CCA: S. mansoni infection determined by a positive urine circulating cathodic antigen (CCA) result (rural infected n = 118, uninfected n = 81; urban infected n = 21, uninfected n = 37).
Figure 4 Principal component analysis of anti-glycan antibody responses. Scatterplots of first (PC1) and second factor (PC2) loadings derived from principal component analysis of IgE and IgG responses to 135 synthetic N-glycans. Box-and-whisker plots show comparison of PC1 and PC2 scores between S. mansoni infected and uninfected individuals. The plots show a horizontal line denoting the median, a box indicating the interquartile range (IQR), and whiskers drawn using the Tukey method (1.5 times IQR). Outliers (greater than 1.5 times IQR away from the median) are plotted as individual points. Panels a and b show IgE and IgG profiles, respectively, among rural participants. Panels c and d show IgE and IgG profiles, respectively, among urban participants. Associations between factor loading scores and S. mansoni infection and intensity were assessed by linear regression analysis in Stata 13.1. Crude and age- and sex-adjusted p values are shown for significant associations. All analyses were adjusted for survey design using the ‘svy’ command in Stata. PC1: Principal Component 1; PC2: Principal Component 2; Sm: S. mansoni infection determined by detection of eggs in a single stool sample by Kato-Katz and/or PCR (rural infected n = 84, uninfected n = 113; urban infected n = 6, uninfected n = 42); CCA: S. mansoni infection determined by a positive urine circulating cathodic antigen (CCA) result (rural infected n = 118, uninfected n = 81; urban infected n = 21, uninfected n = 37).CC BY · PubMed Central
Figure 5 Rural-urban comparisons of anti-glycan antibody responses. (a,e) Box-and-whisker plots showing background-subtracted and log2-transformed median fluorescence intensities (MFI) representing IgE and IgG reactivity to individual α3Fuc- and/or β2Xyl-carrying Man3GlcNAc2 core structures in rural versus urban participants. The plots show a horizontal line denoting the median, a box indicating the interquartile range (IQR), and whiskers drawn using the Tukey method (1.5 times IQR). Outliers (greater than 1.5 times IQR away from the median) are plotted as individual points. Mann-Whitney (IgE responses) and unpaired t test (IgG responses) were conducted within the framework of a Monte Carlo simulation algorithm based on 1000 permutations, to assess differences between rural and urban individuals. (b,f) First and second principal component loadings of N-glycan-specific IgE and IgG responses among all participants, irrespective of survey setting. (c,d,g,h) Box-and-whisker plots showing comparison of PC1 and PC2 scores between rural and urban individuals. Associations between PC scores and survey setting were assessed by linear regression in Stata 13.1. Crude and age- and sex-adjusted p values are shown for significant associations. All analyses were adjusted for survey design using the ‘svy’ command in Stata. *p < 0.05; **p < 0.01; ***p < 0.001. PC1: Principal Component 1; PC2: Principal Component 2.
Figure 5 Rural-urban comparisons of anti-glycan antibody responses. (a,e) Box-and-whisker plots showing background-subtracted and log2-transformed median fluorescence intensities (MFI) representing IgE and IgG reactivity to individual α3Fuc- and/or β2Xyl-carrying Man3GlcNAc2 core structures in rural versus urban participants. The plots show a horizontal line denoting the median, a box indicating the interquartile range (IQR), and whiskers drawn using the Tukey method (1.5 times IQR). Outliers (greater than 1.5 times IQR away from the median) are plotted as individual points. Mann-Whitney (IgE responses) and unpaired t test (IgG responses) were conducted within the framework of a Monte Carlo simulation algorithm based on 1000 permutations, to assess differences between rural and urban individuals. (b,f) First and second principal component loadings of N-glycan-specific IgE and IgG responses among all participants, irrespective of survey setting. (c,d,g,h) Box-and-whisker plots showing comparison of PC1 and PC2 scores between rural and urban individuals. Associations between PC scores and survey setting were assessed by linear regression in Stata 13.1. Crude and age- and sex-adjusted p values are shown for significant associations. All analyses were adjusted for survey design using the ‘svy’ command in Stata. *p < 0.05; **p < 0.01; ***p < 0.001. PC1: Principal Component 1; PC2: Principal Component 2.CC BY · PubMed Central

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Cited by

Sorted by citations

Metadata

Authors
Nkurunungi, G., van Diepen, A., Nassuuna, J., Sanya, R. E., Nampijja, M., Nambuya, I., Kabagenyi, J., Serna, S., Reichardt, N.-C., van Ree, R., Webb, E. L., Elliott, A. M., Yazdanbakhsh, M., & Hokke, C. H.
Venue
Scientific Reports
Publisher
Springer Science and Business Media LLC
Published
2019-03-05
Volume
9
Issue
1
ISSN
2045-2322
DOI
10.1038/s41598-019-40009-7
PMC
PMC6401159
Cited by
19
References
2
Language
en
Licence

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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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