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Cross-Neutralization of Human and Palm Civet Severe Acute Respiratory Syndrome Coronaviruses by Antibodies Targeting the Receptor-Binding Domain of Spike Protein

Yuxian He, Jingjing Li, Wenhui Li, Sara Lustigman, Michael Farzan and Shibo Jiang
J Immunol May 15, 2006, 176 (10) 6085-6092; DOI: https://doi.org/10.4049/jimmunol.176.10.6085
Yuxian He
*Lindsley F. Kimball Research Institute, New York Blood Center, New York, NY 10021; and
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Jingjing Li
*Lindsley F. Kimball Research Institute, New York Blood Center, New York, NY 10021; and
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Wenhui Li
† Department of Microbiology and Molecular Genetics, Harvard Medical School, New England Primate Research Center, Southborough, MA 01772
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Sara Lustigman
*Lindsley F. Kimball Research Institute, New York Blood Center, New York, NY 10021; and
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Michael Farzan
† Department of Microbiology and Molecular Genetics, Harvard Medical School, New England Primate Research Center, Southborough, MA 01772
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Shibo Jiang
*Lindsley F. Kimball Research Institute, New York Blood Center, New York, NY 10021; and
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  • FIGURE 1.
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    FIGURE 1.

    Design, expression and characterization of recombinant RBD variants. A, Schematic diagram of SARS-CoV S protein and the fusion protein RBD-Fc. The RBD of S protein contains residues 318–510 in the S1 domain. RBD-Fc consists of RBD and a human IgG1-Fc fragment. B, Amino acid differences among the RBDs of the S proteins of the indicated isolates (Tor2, GD03T0013, and SZ3). C, Characterization of purified RBD-Fc fusion proteins by SDS-PAGE with 10% gel and Western blot with anti-RBD mAb 17H9. D, Binding of RBD variants to human or palm civet ACE2 analyzed by flow cytometry.

  • FIGURE 2.
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    FIGURE 2.

    Ab responses in mice and rabbits immunized with RBD-Fc fusion proteins. A, Reactivity of mouse sera with RBD-Fc variants in ELISA. B, Binding of serially diluted mouse antisera collected after the third boost to S1-C9. C, Reactivity of rabbit sera with RBD-Fc variants in ELISA. D, Binding of serially diluted rabbit antisera collected after the third boost to S1-C9.

  • FIGURE 3.
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    FIGURE 3.

    Infection of SARS pseudoviruses expressing S protein of the Tor2, GD03, or SZ3 isolate in HEK293 cells expressing human and palm civet ACE2, respectively. Infection, measured as luciferase activity of cell lysates, was assayed 2 days postinfection.

  • FIGURE 4.
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    FIGURE 4.

    Potent neutralization of SARS pseudovirus infection by mouse anti-RBD Abs. Infection of HEK293 cells expressing human ACE2 or palm civet ACE2 by SARS pseudoviruses (Tor2, GD03, or SZ3) was determined in the presence of mouse antisera at a series of 3-fold dilutions. Percentage of neutralization was calculated for each sample, and the average values were plotted.

  • FIGURE 5.
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    FIGURE 5.

    Cross-neutralization of SARS pseudoviruses (Tor2, GD03, or SZ3) by rabbit anti-RBD Abs. The neutralizing activity of the Abs against SARS pseudovirus infection in HEK293 cells expressing human or palm civet ACE2 was determined as described above.

Tables

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    Table I.

    Neutralization of SARS pseudoviruses by anti-RBD mAbs

    GroupmAbInhibition of ACE2 BindingND50 of Pseudovirus (μg/ml)
    Tor2GD03SZ3
    Conf I9F7−6.220.15>50
    12B11−4.560.7>50
    29G2−3.240.16>50
    Conf II26A4−2.850.49>50
    27C1−1.470.06>50
    31H12−0.210.02>50
    Conf III11E 12+1.283.91>50
    18D9+0.035.29>50
    Conf IV28D6+0.210.160.64
    30F9+0.020.080.21
    35B5+0.090.060.35
    Conf V24F4+0.053.610.14
    33G4+0.010.020.01
    38D4+0.3535.140.36
    Conf VI13B6−1.321.51.25
    19B2−0.760.620.41
    Linear4D5−>50>50>50
    17H9−>50>50>50
    • View popup
    Table II.

    Characterization of neutralization epitopes with natural mutants by ELISAa

    mAbRBD VariantTor2 to SZ3 Point Mutation
    Tor2GD03SZ3K344RF360SN479KT487S
    Conf I9F7 2.72 2.97 3.13 2.34 2.07 2.01 1.91
    10E 7 2.83 3.23 3.29 3.00 2.08 2.19 1.93
    12B11 2.96 3.53 3.10 2.71 1.80 2.04 2.13
    18C2 2.75 3.35 3.32 2.75 1.93 2.13 1.75
    24H8 2.70 2.89 2.96 2.91 2.03 2.11 2.07
    29G2 2.56 2.88 2.63 2.27 1.84 1.98 1.96
    32H5 2.59 2.86 2.86 2.66 2.10 2.16 2.03
    Conf II20E 7 2.72 2.54 2.58 2.43 1.95 1.90 1.90
    26A4 2.78 3.60 3.38 2.63 2.23 2.09 1.91
    27C1 2.59 2.75 2.57 2.83 2.08 2.13 2.12
    31H12 2.69 3.15 2.86 2.69 2.17 2.32 2.08
    34E 10 2.65 3.22 3.06 3.07 2.31 2.46 1.97
    Conf III11E 12 2.51 1.80 2.66 1.99 1.39 1.64 1.57
    18D9 2.49 2.28 2.77 2.28 1.48 1.30 1.78
    Conf IV28D6 2.68 3.21 3.03 3.10 2.23 2.18 2.05
    30F9 2.73 3.15 3.35 3.28 2.24 2.26 2.17
    35B5 2.59 3.42 3.22 3.21 2.29 2.38 2.20
    Conf V24F4 2.75 2.53 3.31 3.58 2.41 2.39 1.95
    33G4 2.68 2.85 3.05 3.11 2.50 2.48 2.34
    38D4 2.56 2.02 2.98 2.85 2.09 2.40 1.96
    Conf VI13B6 2.73 2.75 2.80 3.14 1.67 2.06 2.02
    19B2 2.72 2.72 2.67 2.77 1.94 1.78 2.00
    44B5 2.61 3.11 2.76 2.77 2.07 2.12 2.02
    45F6 2.56 3.10 2.78 2.66 2.06 2.17 2.08
    Linear4D5 2.72 3.19 3.56 1.42 1.04 1.08 1.22
    17H9 2.75 3.51 3.38 3.77 2.32 2.62 2.16
    Control3A3b0.030.050.020.030.040.030.02
    • a Ags were coated to ELISA plates at 1 μg/ml and mAbs were tested at 10 μg/ml. OD450 value >0.2 was considered positive reaction and highlighted in boldface.

    • b 3A3 is a control mAb targeting the S2 domain.

    • View popup
    Table III.

    Characterization of neutralization epitopes with non-natural RBD mutants by ELISAa

    GroupMAbDeletion ofSingle-Point Mutation
    aa 318–326aa 491–510K390AD429AR441AE452AD454AD463A
    Conf I9F70.080.00 2.15 0.180.02 1.36 0.01 1.47
    10E 70.110.00 2.39 0.190.01 1.44 0.03 1.71
    12B110.030.00 2.40 0.090.030.190.00 0.45
    18C20.030.01 2.45 0.120.010.030.00 0.34
    24H80.07−0.01 2.32 0.190.02 0.29 0.00 1.35
    29G20.060.00 2.41 0.170.01 0.71 0.02 1.37
    32H50.080.00 2.51 0.200.01 0.82 0.01 1.46
    Conf II20E 70.02−0.01 2.36 0.120.02 0.65 0.00 1.24
    26A40.020.00 2.42 0.140.02 0.65 0.00 1.08
    27C10.070.03 2.36 0.190.12 0.79 0.01 1.32
    31H120.080.00 2.48 0.200.01 1.03 0.00 1.87
    34E 100.08−0.01 2.74 0.200.01 1.02 0.01 1.72
    Conf III11E 120.010.00 2.05 0.010.02 0.25 0.010.05
    18D90.010.00 2.18 0.010.02 0.39 0.00 0.44
    Conf IV28D60.070.00 2.37 0.070.02 1.69 0.00 1.49
    30F90.060.00 2.43 0.050.02 1.59 0.00 1.37
    35B50.08−0.01 2.48 0.110.02 1.65 0.01 1.57
    Conf V24F4 1.73 1.22 2.75 1.45 0.73 2.59 1.95 0.86
    33G4 2.03 1.56 2.50 1.71 1.05 2.56 2.06 2.02
    38D4 1.27 1.06 2.49 0.77 0.50 2.41 1.30 0.77
    Conf VI13B60.00−0.01 2.32 0.150.02 1.40 0.00 1.28
    19B20.04−0.01 2.36 0.000.01 1.15 0.00 0.86
    44B50.130.00 2.41 0.200.03 1.70 0.04 1.99
    45F60.080.00 2.43 0.200.02 1.78 0.03 1.62
    Linear4D5 2.70 2.20 1.75 0.89 0.83 3.03 2.44 0.82
    17H9 2.95 3.62 2.63 2.78 3.59 3.23 0.19 4.18
    Control3A30.010.020.020.000.030.020.010.03
    • a Ags were coated to ELISA plates at 1 μg/ml, and mAbs were tested at 10 μg/ml. OD450 value >0.2 was considered positive reaction and highlighted in boldface.

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The Journal of Immunology: 176 (10)
The Journal of Immunology
Vol. 176, Issue 10
15 May 2006
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Cross-Neutralization of Human and Palm Civet Severe Acute Respiratory Syndrome Coronaviruses by Antibodies Targeting the Receptor-Binding Domain of Spike Protein
Yuxian He, Jingjing Li, Wenhui Li, Sara Lustigman, Michael Farzan, Shibo Jiang
The Journal of Immunology May 15, 2006, 176 (10) 6085-6092; DOI: 10.4049/jimmunol.176.10.6085

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Cross-Neutralization of Human and Palm Civet Severe Acute Respiratory Syndrome Coronaviruses by Antibodies Targeting the Receptor-Binding Domain of Spike Protein
Yuxian He, Jingjing Li, Wenhui Li, Sara Lustigman, Michael Farzan, Shibo Jiang
The Journal of Immunology May 15, 2006, 176 (10) 6085-6092; DOI: 10.4049/jimmunol.176.10.6085
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