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A selection and optimization strategy for single-domain antibodies targeting the PHF6 linear peptide within the tau intrinsically disordered protein

Mortelecque, Justine, Zejneli, Orgeta, Bégard, Séverine, Simões, Margarida C., ElHajjar, Lea, Nguyen, Marine, Cantrelle, François-Xavier, Hanoulle, Xavier, Rain, Jean-Christophe, Colin, Morvane, Gomes, Cláudio M., Buée, Luc, Landrieu, Isabelle, Danis, Clément, Dupré, Elian·2024·Journal of Biological Chemistry
DOI 10.1016/j.jbc.2024.107163PMC PMC11007443

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Figures

Figure 1 Selected mutations for VHH optimization.A, sequence of VHH Z70 and selected substitutions. CDR1, 2, and 3 sequences are represented in pink, blue, and red respectively. The three amino acids in bold italic are the most frequently substituted. When different substitutions exist that differ in frequency, the most frequent is in bold. B, overview of the mutants selected for further analysis. CDR, complementarity-defining region; VHH, variable heavy-chain of the heavy-chain–only antibody.
Figure 1 Selected mutations for VHH optimization.A, sequence of VHH Z70 and selected substitutions. CDR1, 2, and 3 sequences are represented in pink, blue, and red respectively. The three amino acids in bold italic are the most frequently substituted. When different substitutions exist that differ in frequency, the most frequent is in bold. B, overview of the mutants selected for further analysis. CDR, complementarity-defining region; VHH, variable heavy-chain of the heavy-chain–only antibody.CC BY · PubMed Central
Figure 2 Epitope verification of Z70 mutants.A, Western blot against tau using TAMRA-labeled VHHs. B, spectrum overlay of tau alone (in red), tau with Z70 (in blue, 1:1 M ratio), or tau with mutant 1 (in cyan, 1:1 M ratio). TAMRA, carboxytetramethylrhodamine; VHH, variable heavy-chain of the heavy-chain–only antibody.
Figure 2 Epitope verification of Z70 mutants.A, Western blot against tau using TAMRA-labeled VHHs. B, spectrum overlay of tau alone (in red), tau with Z70 (in blue, 1:1 M ratio), or tau with mutant 1 (in cyan, 1:1 M ratio). TAMRA, carboxytetramethylrhodamine; VHH, variable heavy-chain of the heavy-chain–only antibody.CC BY · PubMed Central
Figure 3 Epitope of Z70 and variant VHHs.A, schematic representation of the tau protein. N-terminal domain (1–163) is represented in red and may contain N1 and N2 inserted sequences depending on tau isoforms. The proline-rich domain (PRD) is subdivided in P1 and P2 regions. The microtubule binding domain consists of four partially repeated regions, R1 to R4 (in tau 4R). The R2 repeat is not present in tau 3R. C-ter is for the C-terminal domain. B, normalized intensity ratios I/I0 of corresponding resonances in the two-dimensional spectra of tau with equimolar quantity of Z70, mutant 1, 3, or 20 (I) or free in solution (I0) for residues along the tau sequence.
Figure 3 Epitope of Z70 and variant VHHs.A, schematic representation of the tau protein. N-terminal domain (1–163) is represented in red and may contain N1 and N2 inserted sequences depending on tau isoforms. The proline-rich domain (PRD) is subdivided in P1 and P2 regions. The microtubule binding domain consists of four partially repeated regions, R1 to R4 (in tau 4R). The R2 repeat is not present in tau 3R. C-ter is for the C-terminal domain. B, normalized intensity ratios I/I0 of corresponding resonances in the two-dimensional spectra of tau with equimolar quantity of Z70, mutant 1, 3, or 20 (I) or free in solution (I0) for residues along the tau sequence.CC BY · PubMed Central
Figure 4 Comparison of Z70, mutant 1, 3, and 20 structures. Superposition of Z70 (in green, PDB 7qcq), mutant 1 (in gold, PDB 8opi), mutant 3 (in pale green, PDB 8pii), and mutant 20 (in orange, PDB 8op0). Their CDR1 are in pink, CDR2 in blue, and CDR3 in purple. Tau PHF6 peptide is colored cyan. CDR, complementarity-defining region; PDB, Protein Data Bank.
Figure 4 Comparison of Z70, mutant 1, 3, and 20 structures. Superposition of Z70 (in green, PDB 7qcq), mutant 1 (in gold, PDB 8opi), mutant 3 (in pale green, PDB 8pii), and mutant 20 (in orange, PDB 8op0). Their CDR1 are in pink, CDR2 in blue, and CDR3 in purple. Tau PHF6 peptide is colored cyan. CDR, complementarity-defining region; PDB, Protein Data Bank.CC BY · PubMed Central
Figure 5 Comparison of Z70, mutant 1, 3, and 20 electron density maps. Z70, mutants 1, 3, and 20 are represented in green, gold, pale green and orange, respectively. Tau PHF6 peptide is colored cyan. A, environment of the peptide in all three structures remains unchanged. B, electron density (2fo-fc map contoured at 1 σ), shown as mesh representation, corresponding to the region surrounding residues 115 to 117 (left) and 46 to 48 (right) in VHH Z70 (top), mutant 1 (middle) and mutant 20 (bottom), respectively, showing the appearance of density for residue 115 from Z70 to mutant 20. A salt bridge is shown between K47 and E115 of mutant 20 in red dashes. VHH, variable heavy-chain of the heavy-chain–only antibody.
Figure 5 Comparison of Z70, mutant 1, 3, and 20 electron density maps. Z70, mutants 1, 3, and 20 are represented in green, gold, pale green and orange, respectively. Tau PHF6 peptide is colored cyan. A, environment of the peptide in all three structures remains unchanged. B, electron density (2fo-fc map contoured at 1 σ), shown as mesh representation, corresponding to the region surrounding residues 115 to 117 (left) and 46 to 48 (right) in VHH Z70 (top), mutant 1 (middle) and mutant 20 (bottom), respectively, showing the appearance of density for residue 115 from Z70 to mutant 20. A salt bridge is shown between K47 and E115 of mutant 20 in red dashes. VHH, variable heavy-chain of the heavy-chain–only antibody.CC BY · PubMed Central
Figure 6 Conformational stabilization of mutant 20.A, cartoon representation of mutant 20 showing the salt bridge between residues K47 and E115 as red dashes. The framework region is colored orange, CDR 1 is represented in pink, CDR2 in blue, and CDR3 in purple, while the PHF6 peptide is colored cyan. B, superimposition of 1H 15N HSQC spectra of 15N labeled mutant 20 in blue and VHH Z70 in red showing the detection of additional resonances in the spectrum of mutant 20 indicating a change in the conformational dynamics that could be favored by the K47-E115 salt bridge. CDR, complementarity-defining region; HSQC, heteronuclear single quantum coherence; VHH, variable heavy-chain of the heavy-chain–only antibody.
Figure 6 Conformational stabilization of mutant 20.A, cartoon representation of mutant 20 showing the salt bridge between residues K47 and E115 as red dashes. The framework region is colored orange, CDR 1 is represented in pink, CDR2 in blue, and CDR3 in purple, while the PHF6 peptide is colored cyan. B, superimposition of 1H 15N HSQC spectra of 15N labeled mutant 20 in blue and VHH Z70 in red showing the detection of additional resonances in the spectrum of mutant 20 indicating a change in the conformational dynamics that could be favored by the K47-E115 salt bridge. CDR, complementarity-defining region; HSQC, heteronuclear single quantum coherence; VHH, variable heavy-chain of the heavy-chain–only antibody.CC BY · PubMed Central
Figure 7 Thermal stabilities of the different VHHsin NMR buffer. VHH, variable heavy-chain of the heavy-chain–only antibody.
Figure 7 Thermal stabilities of the different VHHsin NMR buffer. VHH, variable heavy-chain of the heavy-chain–only antibody.CC BY · PubMed Central
Figure 8 In-cell stabilities of the VHHs.A, percentage of mCherry-positive HEK293 cells showing aggregates (puncta) of VHH-mCherry 48 h after transfection. B, Pearson plot of the percentage of cells with aggregates in the self-aggregation assay versus melting temperatures in NMR buffer. VHH, variable heavy-chain of the heavy-chain–only antibody.
Figure 8 In-cell stabilities of the VHHs.A, percentage of mCherry-positive HEK293 cells showing aggregates (puncta) of VHH-mCherry 48 h after transfection. B, Pearson plot of the percentage of cells with aggregates in the self-aggregation assay versus melting temperatures in NMR buffer. VHH, variable heavy-chain of the heavy-chain–only antibody.CC BY · PubMed Central
Figure 9 In vitro inhibition of tau aggregation by the VHHs.A, inhibition of tau-K18 aggregation by Z70 at VHH:Tau-K18 M ratios between 0.1 and 0.4 (n = 4) B, inhibition efficiency of different Z70-derived VHHs over tau aggregation tested at a molar ratio of 0.5:1 VHH:tau. Positive and negative controls correspond to tau in the presence of heparin (tau +) and the absence of heparin (tau −), respectively. The other conditions correspond to tau in the presence of heparin and the different VHHs at a VHH:tau ratio of 0.5:1. The percentage of aggregation corresponds to the fluorescence intensity ratio between tau in the presence of a VHH and tau alone (tau +) during the aggregation process. Data are represented as mean ± SEM, the mean value is written above the bars (n = 3). VHH, variable heavy-chain of the heavy-chain–only antibody.
Figure 9 In vitro inhibition of tau aggregation by the VHHs.A, inhibition of tau-K18 aggregation by Z70 at VHH:Tau-K18 M ratios between 0.1 and 0.4 (n = 4) B, inhibition efficiency of different Z70-derived VHHs over tau aggregation tested at a molar ratio of 0.5:1 VHH:tau. Positive and negative controls correspond to tau in the presence of heparin (tau +) and the absence of heparin (tau −), respectively. The other conditions correspond to tau in the presence of heparin and the different VHHs at a VHH:tau ratio of 0.5:1. The percentage of aggregation corresponds to the fluorescence intensity ratio between tau in the presence of a VHH and tau alone (tau +) during the aggregation process. Data are represented as mean ± SEM, the mean value is written above the bars (n = 3). VHH, variable heavy-chain of the heavy-chain–only antibody.CC BY · PubMed Central
Figure 10 In cellulo inhibition of tau seeding by the VHHs. The percentage of FRET-positive cells, corresponding to cells with aggregated tau, is given for the mCherry-gated population, corresponding to transfected cells. Values are normalized relative to the experiment with F8-2 VHH-mCherry. Data are represented as mean ± SEM, the mean value is given above the bars and individual points are plotted. Statistical comparison between each VHH and F8-2 was carried out using post hoc Dunn’s test after Kruskall–Wallis test with p = 2.9∗10-5, ∗∗∗ is p < 0.001, ∗∗ p < 0.01, and – is not significant. VHH, variable heavy-chain of the heavy-chain–only antibody.
Figure 10 In cellulo inhibition of tau seeding by the VHHs. The percentage of FRET-positive cells, corresponding to cells with aggregated tau, is given for the mCherry-gated population, corresponding to transfected cells. Values are normalized relative to the experiment with F8-2 VHH-mCherry. Data are represented as mean ± SEM, the mean value is given above the bars and individual points are plotted. Statistical comparison between each VHH and F8-2 was carried out using post hoc Dunn’s test after Kruskall–Wallis test with p = 2.9∗10-5, ∗∗∗ is p < 0.001, ∗∗ p < 0.01, and – is not significant. VHH, variable heavy-chain of the heavy-chain–only antibody.CC BY · PubMed Central
Figure 11 Pearson correlation plots.A, mean values of percentage of tau seeding in HEK293 tau repeat domain (RD) P301S FRET Biosensor seeding reporter cells (cellular seeding assay) versus mean values of in vitro aggregation assay with a ratio of 0.5 VHH for 1 tau. Dashed line is omitting the outlier mutant 9. B, mean values of percentage of tau seeding in HEK293 tau repeat domain (RD) P301S FRET biosensor seeding reporter cells (cellular seeding assay) versus percentage of cells showing punctate aggregates in HEK293 cells. VHH, variable heavy-chain of the heavy-chain–only antibody.
Figure 11 Pearson correlation plots.A, mean values of percentage of tau seeding in HEK293 tau repeat domain (RD) P301S FRET Biosensor seeding reporter cells (cellular seeding assay) versus mean values of in vitro aggregation assay with a ratio of 0.5 VHH for 1 tau. Dashed line is omitting the outlier mutant 9. B, mean values of percentage of tau seeding in HEK293 tau repeat domain (RD) P301S FRET biosensor seeding reporter cells (cellular seeding assay) versus percentage of cells showing punctate aggregates in HEK293 cells. VHH, variable heavy-chain of the heavy-chain–only antibody.CC BY · PubMed Central

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Cited by

Metadata

Authors
Mortelecque, J., Zejneli, O., Bégard, S., Simões, M. C., ElHajjar, L., Nguyen, M., Cantrelle, F.-X., Hanoulle, X., Rain, J.-C., Colin, M., Gomes, C. M., Buée, L., Landrieu, I., Danis, C., & Dupré, E.
Venue
Journal of Biological Chemistry
Publisher
Elsevier BV
Published
2024-04
Volume
300
Issue
4
Pages
107163
ISSN
0021-9258
DOI
10.1016/j.jbc.2024.107163
PMC
PMC11007443
Cited by
12
References
1
Language
en
Licence
Funders
  • Fundação para a Ciência e a Tecnologia (GA 101079147, UIDP/MULTI/04046/2020, UIDB/04046/2020, 2022.11023)
  • Institute Pasteur De Lille
  • French National Research Agency (ANR-18-CE44-0016, ANR-22-CE92-0061, ANR-11-LABX-01)
  • Campus France
  • Labex
  • Centre National de la Recherche Scientifique
  • European Commission

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