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Table 1.

Structure-based computational design of the Fab-mutant set with varied binding affinities to Her2 ectodomain.

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Fig 1.

Structure-based computational design of a Fab mutant set with varied binding affinity to Her2 ectodomain.

(A) Structural overview of the parent antibodies Herceptin and bH1 binding the same epitope of the Her2 antigen. Crystal structures with PDB codes 1N8Z and 3BE1 are used for Herceptin-Fab/Her2 and bH1-Fab/Her2 complexes, respectively (see Materials and methods). Measured Her2 binding affinities of the corresponding Fab fragments are from Bostrom et al. [15] Only the antigen-binding Fv domains of the antibodies are shown as ribbons colored cyan and magenta for the heavy and light chains, respectively. The epitope of the Her2 antigen is rendered as black ribbon inside a translucent gray molecular surface. Mutated positions of the antibodies are shown as CPK models and labeled. The position of a four-residue insert in the CDR-L1 of bH1 relative to Herceptin is also indicated. (B) Molecular details of interactions at the mutated positions of selected antibody mutants. Each sub-panel includes an overlay of molecular models for several antibodies (mutants vs. parent). Mutated antibody residues are labeled and shown as sticks with C atoms colored cyan and magenta for the heavy and light chains, respectively. Her2 residues interacting with mutated Fab positions are shown as stick with white C atoms and labeled in italics.

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Table 2.

Antibody variants ranked according to monovalent Her2 binding affinities measured by SPR.

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Table 2 Expand

Fig 2.

SPR ranking of FSAs and sensorgrams.

(A) SPR monovalent KD measurements and classification of Herceptin antibody variants. The asterisks indicate variants selected for further analysis. (B) Representative sensorgrams from WT/Strong (top), Moderate (middle) and Weak (bottom) variant classifications. The red line indicates the fit modelled to a 1:1 interaction with Her2.

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Table 3.

Her2 binding kinetics of selected antibody variants measured by SPR.

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Table 4.

Relative Her2 receptor levels on cells determined via flow cytometry.

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Table 5.

Binding parameters KD and Bmax determined from flow cytometry.

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Fig 3.

Saturation binding curves and apparent binding affinities (KDs) of selected antibody variants in low-Her2 (MCF7) and high-Her2 (SKOV3) cells, as determined via flow cytometry.

(A, B) MCF7 cells. (C, D) SKOV3 cells.

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Fig 4.

Internalization of antibody variants in SKOV3 cells as measured using indirect detection by pHAb-secondary antibody and high content imaging.

(A) Well-view images of SKOV3 cells treated with the indicated variant antibody plus pHAb-labelled secondary antibody at 37°C for 18 h (top panel). 2nd = secondary antibody alone, Synagis = IgG1 control. The bottom panel shows representative processed images (yellow = antibody; blue = nuclei). (B) Internalization dose response curves, plotting integrated fluorescence intensity/nucleus versus Log10 concentration of antibody. (C) Internalization EC50s (concentration at which the amount of internalized antibody is 50% relative to maximum accumulation) of variants derived from dose response curves. (D) Intracellular fluorescence intensities at selected concentrations of antibody (2 and 6 nM).

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Fig 5.

Internalization in SKOV3 and JIMT-1 cells as measured by direct detection of pHAb-labelled antibody variants and high content imaging.

Internalization dose response curves of variants in (A) SKOV3 cells and (B) JIMT-1 cells, following treatment with antibody at 37°C for 18 h. (C) Internalization EC50s of variants.

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Table 6.

Potencies of antibody variants indirectly conjugated to the DM1 and MMAE cytotoxic drugs.

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Fig 6.

Direct ADC cytotoxicity of DM1 and PNU conjugated variants in Her2 cells.

IC50s of DM1-antibodies (A) and PNU-antibodies (B) in SKOV3 cells. (C) Survival curves in SKOV3, JIMT-1 and MCF7 cells treated with the indicated antibody-PNU variant or Synagis-PNU. Double-head black arrows denote the therapeutic window (concentration range between high-Her2 SKOV3 and low-Her2 MCF7 cells). The data are normalized, based on DAR (Drug Antibody Ratio), to account for small DAR differences between antibody variants.

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Table 7.

Potencies of antibody variants directly conjugated to the DM1 and PNU cytotoxic drugs.

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Fig 7.

(A) Saturation binding of affinity-modulated antibodies on high-density Her2 cells. Shown are binding curves for strong (12–9) and weak (7–5) affinity variants and WT antibody that show the different Bmax levels attained by these antibodies on SKOV3 cells, as determined via flow cytometry. The schematics (boxes) illustrate how affinity affects the number of antibodies and Her2 receptors (brown oval circles) engaged at the cell surface. (B) Schematic that illustrates Her2 avidity resulting in selective binding of weak-affinity ADC to Her2 receptors on SKOV3 tumor cells and cytotoxicity. Left panel: strong-affinity ADC (e.g. variant 11–9 or 12–9) readily binds Her2 receptors on both SKOV3 and MCF7 cells, resulting in cytotoxicity and cell death. Right panel: weak affinity ADC (e.g. variant 7–5 or 14–13) binds well to SKOV3 cells, due to high-density Her2 avidity, but binds poorly to low-density Her2 MCF7 cells, resulting in low cytotoxicity in MCF7 cells.

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