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Nasal Vaccination Drives Modifications of Nasal and Systemic Antibody Repertoires in Rainbow Trout

Susana Magadan, Luc Jouneau, Pierre Boudinot and Irene Salinas
J Immunol September 15, 2019, 203 (6) 1480-1492; DOI: https://doi.org/10.4049/jimmunol.1900157
Susana Magadan
*Center of Evolutionary and Theoretical Immunology, Department of Biology, University of New Mexico, Albuquerque, NM 87131;
†Immunology Laboratory, Biomedical Research Center (CINBIO), University of Vigo, Vigo, 36310 Pontevedra, Spain; and
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Luc Jouneau
‡Virologie et Immunologie Moleculaires, Institut National de la Recherche Agronomique, Université Paris-Saclay, 78352 Jouy-en-Josas Cedex, France
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Pierre Boudinot
‡Virologie et Immunologie Moleculaires, Institut National de la Recherche Agronomique, Université Paris-Saclay, 78352 Jouy-en-Josas Cedex, France
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Irene Salinas
*Center of Evolutionary and Theoretical Immunology, Department of Biology, University of New Mexico, Albuquerque, NM 87131;
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  • FIGURE 1.
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    FIGURE 1.

    IgM and IgT repertoire diversity in spleen and NALT in naive juvenile trout. (A) Overall IGHV family usage by IgM and IgT in Spleen and NALT of naive trouts. Bar plots showing the percentage of IgM (up) and IgT (bottom) MID barcoded consensus sequences belonging to each IGHV. (B) IgM and IgT clonotype diversity as measured by the Shannon Entropy calculated from seven IGHV families. Data were analyzed by one-way ANOVA with post hoc Tukey HSD test (***p ≤ 0.01). (C) Normalized distributions of clonotypes determined n times in the consensus sequence datasets from control fish. Red bars correspond to IgM clonotypes and blue bars to IgT. (D) Accumulated frequency for the top 20 most prevalent clonotypes for IgM and IgT repertoire observed in spleen and NALT of each control fish.

  • FIGURE 2.
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    FIGURE 2.

    (A) Detection of IgM (left panel) and IgT (right panel) specific to ERM bacterin in serum from controls, i.p., or i.n. ERM-immunized fish. Serum dilutions, 1/100 for IgM and 1/20 for IgT were evaluated by indirect ELISA, and the results are represented as relative values to the most positive serum. (B) Effect of i.p. and intranasal (IN) immunization on the IGHV gene family usage by trout IgM and IgT repertoire. Mean IGHV gene family usage in spleen and NALT of controls (C) and i.p. or i.n. ERM- immunized fish (n = 6 fish per group). Graphics show mean + SD of IGHV family usage for IgM or IgT considering MID barcoded consensus sequences. Significant difference in IGHV family usage was detected by one-way ANOVA posthoc Tukey HSD test and Bonferroni. aSignificant difference p < 0.05 between C and i.p. bSignificant difference p < 0.05 between C and IN.

  • FIGURE 3.
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    FIGURE 3.

    Clonotype diversity in spleen and NALT after ERM i.p. or intranasal (IN) immunization. (A) IgM and IgT repertoire diversity considering the Shannon Index calculated from seven IGHV families or (B) considering each IGHV family. Data were analyzed by one-way ANOVA with post hoc Tukey HSD test and Bonferroni (**p ≤ 0.01, *p ≤ 0.05). If the statistical significance relative to control group was obtained by Student t test, ^p ≤ 0.05. (C) IgM clonotype size distribution from control and ERM-immunized fish are represented IGHV5 and IGHV4 families. Large clonal expansions are indicated by high number of consensus sequence counts.

  • FIGURE 4.
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    FIGURE 4.

    Size distribution of splenic IgM and IgT clonotypes shared by individual. dot/box plots showing the size distribution for each VH-C combination and for clonotypes found among n fish (n = 1 in dark gray, 2 in gray, 3 in yellow, 4 in blue, 5 in green, or 6 in pink) within each treatment group (control, i.p., i.n.). Dots are computed from the values corresponding to clonotypes found in one to six fish, over 10 subsamplings in the selected IGHV families that are indicated on the right. Each dot represents a clonotype in a fish. Relative clonotype size value (y-axis) in log10 scale.

  • FIGURE 5.
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    FIGURE 5.

    Size distribution of NALT IgM and IgT clonotypes shared by individual. Dot/box plots showing the size distribution for each VH-C combination and for clonotypes found among n fish (n = 1 in dark gray, 2 in gray, 3 in yellow, 4 in blue, 5 in green, or 6 in pink) within each treatment group (control, i.p., i.n.). Dots are computed from the values corresponding to clonotypes found in one to six fish, over 10 subsamplings in the selected IGHV families indicated on the right. Each dot represents a clonotype in a fish. Relative clonotype size value (y-axis) in log10 scale.

  • FIGURE 6.
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    FIGURE 6.

    Identification of HSR clonotypes. Expression heat maps of IgM (up) and IgT (low) clonotypes shared by at least four fish ERM i.p. immunized (A) or four fish ERM i.n. immunized (B) and found, on average, >10 times compared to controls. Heat maps were obtained with Heatmap.2, and the values were scaled by rows to have mean 0 and SD 1. Each column corresponds to one fish and each arrow to one clonotype. The identified CDR3 amino acid sequence and JH segment are indicated on the right of each heat map. Sequences belonging to IGHV5 family are shown in blue and those coming from IGHV4 (for IGHM heat maps) and IGHV6 (for IGHT heat maps) are shown in black. Sequences in bold and underlined represent clonotypes detected in Spleen and NALT. Venn diagrams showing the overlap of these clonotypes detected in Spleen and NALT are shown on the right of corresponding heat maps.

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    Table I. Number of distinct clonotypes detected in controls for each VH-C combination and organ
    IgMIgT
    MIDsOrganC1C2C3C4C5C6MeanTotalC1C2C3C4C5C6MeanTotal
    IGHV1175Sp14491279107681978610711080648012179601001348113812719895935
    NALT7441182447920110324814895882992042225723033642188
    IGHV2100Sp81078261529353858560336236264084761586376604942965
    NALT4362871231168856184110629712610298240129165992
    IGHV4175Sp15181149980615998869102161291085707750187111610538164898
    NALT8033241012001851052861718448661501852641512101264
    IGHV5180Sp13391283104182568765297158271163905922295125012309605765
    NALT4812991202006093208a1253559297241215625225360a2162
    IGHV6390Sp272428361917146612622319208712,52424621722186564423121621177110,626
    NALT17389974641344762196714028117251338140110175756764059
    IGHV8189Sp1637151212177517579481137a682210055927801321007943743a4459
    NALT9514411359224572322193635815697118280961841105
    IGHV9146Sp104386372546585476178547119696817312017638627014207
    NALT374283121541294616810074301901771454501472561539
    • Average values over 10 subsamplings of corresponding MIDs (see the Materials and Methods section) per IGHV family and C region (VH-C) combination and individual fish. Organ: Spleen (Sp) and NALT. Total spleen (IgM): 46,116. Total IgM clonotypes: Sp (46,116), NALT (12,537). Total IgT clonotypes: Sp (38,855), NALT (13,309).

    • ↵a Significant difference, p < 0.1, data analyzed by Student t test.

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    Table II. Number of distinct clonotypes detected in spleen and NALT from controls and after ERM vaccination
    IgMIgT
    MIDsOrganControli.p.i.n.Controli.p.i.n.
    IGHV1175Sp1080.00 ± 257.06800.167 ± 257.23567.33 ± 106.96989.16 ± 336.32998.67 ± 211.74746 ± 353.14
    NALT248.17 ± 250.89400.33 ± 186.86383.83 ± 327.79364.67 ± 171.55395.00 ± 191.32414.33 ± 237.95
    IGHV2100Sp603.83 ± 187.44518.33 ± 191.72333.66 ± 103.69494.16 ± 192.89482 ± 117.46380.67 ± 190.90
    NALT184.33 ± 147.01245.17 ± 114.35200.33 ± 153.05165.33 ± 82.85182.50 ± 102.23185.17 ± 102.91
    IGHV4175Sp1021.50 ± 301.17427.16 ± 190.29607.83 ± 280.73816.33 ± 355.08725.83 ± 205.41581.83 ± 336.46
    NALT286.33 ± 265.83377.17 ± 178.93334.33 ± 305.63210.67 ± 132.66259.33 ± 147.37288.83 ± 195.52
    IGHV5180Sp971.16 ± 297.11671.5 ± 281.35484.83 ± 115.33960.83 ± 359.14943.16 ± 230.64718 ± 372.11
    NALT208.83 ± 158.58428.00 ± 190.11309.83 ± 185.33360.33 ± 182.87357.50 ± 182.47401.83 ± 223.07
    IGHV6390Sp2087.33 ± 650.501900.16 ± 643.831219.33 ± 397.881771 ± 644.051841.33 ± 511.741451.5 ± 724.07
    NALT671.33 ± 603.04869.83 ± 513.50661.83 ± 540.01676.5 ± 335.17719.33 ± 356.49719.17 ± 445.93
    IGHV8189Sp1137.00 ± 381.08863.5 ± 309.53591.83 ± 166.15743.17 ± 339.36647.5 ± 274.45535 ± 342.43
    NALT322.67 ± 336.48419.16 ± 248.11292.67 ± 181.77184.17 ± 109.49198.67 ± 126.56199.50 ± 150.98
    IGHV9146Sp785.16 ± 191.82625.5 ± 249.75476.66 ± 150.32701.17 ± 265.66700.33 ± 231.4584.5 ± 283.98
    NALT167.83 ± 132.11286.83 ± 121.22273.00 ± 312.36256.5 ± 143.32293.67 ± 131.00312.33 ± 184.93
    TotalSp1098.00 ± 552.04829.48 ± 558.67611.64 ± 331.79925.12 ± 518.91905.55 ± 492.90713.93 ± 494.09
    NALT298.50 ± 329.67433.62 ± 298.92350.83 ± 319.88316 ± 236.59343.71 ± 247.67360.17 ± 281.09
    • Average values over 10 subsamplings of corresponding MIDs (see the Materials and Methods section) per IGHV family and C region (VH-C) combination and individual fish. Organ: Spleen (Sp) and NALT. Those values with significant difference p < 0.05 compared with controls are in bold. Data analyzed by Student t test.

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The Journal of Immunology: 203 (6)
The Journal of Immunology
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15 Sep 2019
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Nasal Vaccination Drives Modifications of Nasal and Systemic Antibody Repertoires in Rainbow Trout
Susana Magadan, Luc Jouneau, Pierre Boudinot, Irene Salinas
The Journal of Immunology September 15, 2019, 203 (6) 1480-1492; DOI: 10.4049/jimmunol.1900157

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Nasal Vaccination Drives Modifications of Nasal and Systemic Antibody Repertoires in Rainbow Trout
Susana Magadan, Luc Jouneau, Pierre Boudinot, Irene Salinas
The Journal of Immunology September 15, 2019, 203 (6) 1480-1492; DOI: 10.4049/jimmunol.1900157
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