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A novel coronavirus designated severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) emerged and caused an outbreak of unusual viral pneumonia. Several reports have shown that cross-reactive antibodies against SARS-CoV-2 also exist in people unexposed to this virus. However, the neutralizing activity of cross-reactive antibodies is controversial. Here, we subjected plasma samples from SARS-CoV-2-unexposed elderly Korean people (n = 119) to bead-based IgG antibody analysis. SARS-CoV-2 S1 subunit-reactive IgG antibody analysis detected positive signals in some samples (59 of 119, 49.6%). SARS-CoV-2 receptor-binding domain (RBD)-reactive antibody levels were most significantly correlated with human coronavirus-HKU1 S1 subunit-reactive antibody levels. To check the neutralizing activity of plasma samples, the SARS-CoV-2 spike pseudotype neutralizing assay was used. However, the levels of cross-reactive antibodies did not correlate with neutralizing activity. Instead, SARS-CoV-2 pseudovirus infection was neutralized by some RBD-reactive plasma samples (n = 9, neutralization ≥ 25%, P ≤ 0.05), but enhanced by other RBD-reactive plasma samples (n = 4, neutralization ≤ -25%, P ≤ 0.05). Interestingly, the blood plasma groups with enhancing and neutralizing effects had high levels of SARS-CoV-2 RBD-reactive antibodies than the plasma group that had no effect. These results suggest that some SARS-CoV-2 RBD-reactive antibodies from pre-pandemic elderly people exert two opposing functions during SARS-CoV-2 pseudovirus infection. In conclusion, preformed RBD-reactive antibodies may have two opposing functions, namely, protecting against and enhancing viral infection. Analysis of the epitopes of preformed antibodies will be useful to elucidate the underlying mechanism.

Two Opposing Roles of SARS-CoV-2 RBD-Reactive Antibodies in Pre-Pandemic Plasma Samples From Elderly People in ACE2-Mediated Pseudovirus Infection