SARS-CoV-2 Seroconversion in Humans: A Detailed Protocol for a Serological Assay, Antigen Production, and Test Setup

In late 2019, cases of atypical pneumonia were detected in China. The etiological agent was quickly identified as a betacoronavirus (named SARS-CoV-2), which has since caused a pandemic. Several methods allowing for the specific detection of viral nucleic acids have been established, but these only allow detection of the virus during a short period of time, generally during acute infection. Serological assays are urgently needed to conduct serosurveys, to understand the antibody responses mounted in response to the virus, and to identify individuals who are potentially immune to re-infection. Here we describe a detailed protocol for expression of antigens derived from the spike protein of SARS-CoV-2 that can serve as a substrate for immunological assays, as well as a two-stage serological enzyme-linked immunosorbent assay (ELISA). These assays can be used for research studies and for testing in clinical laboratories. © 2020 The Authors. Current Protocols in Microbiology published by Wiley Periodicals LLC.

Basic Protocol 1 : Mammalian cell transfection and protein purification

Basic Protocol 2 : A two-stage ELISA for high-throughput screening of human serum samples for antibodies binding to the spike protein of SARS-CoV-2

Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the virus that causes COronaVIrus Disease 2019 (COVID19; often written COVID-19), emerged in late 2019 in Wuhan, China (Wu et al., 2020; Zhu et al., 2020). Rapid, global spread of the virus is presently causing a pandemic. Currently, no drugs or antivirals are available and countermeasures are limited to non-pharmaceutical interventions (NPIs). Nucleic acid−based tests for detection of the virus during acute disease are in use worldwide (Chu et al., 2020; Corman et al., 2020). However, the development of serological assays is lagging due to lack of suitable reagents. Serological assays are needed to perform serosurveys aimed at determining the real infection rate and infection fatality rate in a given population. Furthermore, they are useful to characterize the immune response to the virus in a detailed qualitative and quantitative manner. Serological assays are also of immediate practical use. They can be used to identify individuals who were infected (including severe, mild, and asymptomatic cases) and who are now potentially immune. A recent study in non-human primates showed that re-infection, at least in the small number of animals used in the study, does not occur (Bao et al., 2020) once antibody responses have been mounted. Infection with coronaviruses circulating in human populations, such as HKU, NL63, etc., also leads to immunity that protects from re-infection for months to years (Callow, Parry, Sergeant, & Tyrrell, 1990). Therefore, individuals who have mounted an immune response to SARS-CoV-2 are likely immune, which means that they are unlikely to transmit the virus to others. As an example, healthcare workers who are immune could potentially care for COVID19 patients with minimal risk to themselves, their colleagues, and other patients. In addition, the use of convalescent plasma may serve as a valuable treatment option for patients with severe COVID19, especially in the absence of other options. A serological assay is critical for identifying potential plasma donors.

The surface glycoprotein of the virus, termed the spike (S) protein, mediates attachment of the virus to human cells via its receptor-binding domain (RBD; Wrapp et al., 2020) and mediates fusion of viral and cellular membranes. Antibodies binding to the spike protein, and especially to the RBD domain, can neutralize SARS-CoV-2. Therefore, we used different recombinant spike protein preparations as the antigens for our ELISA. We reported in our earlier work that individuals not exposed to SARS-CoV-2 are completely naïve to the spike protein, and their serum samples show little or no reactivity in an ELISA (Amanat et al., 2020). It is, therefore, easy to distinguish between exposed/immune and naïve individuals.

In this report, we provide detailed protocols for expressing the required antigen(s) (Basic Protocol 1) as well as setting up the ELISA that we have developed (Basic Protocol 2). An overview of these protocols is shown in Figure 1. We believe that these protocols will be useful not only for research laboratories around the globe, but also for testing in diagnostic/clinical laboratories. The described protocol setup works well for us, but it can easily be modified, adapted to local needs, and improved by the research community in the future. Not every aspect of these protocols has been optimized in detail, and we provide notes and comments whenever further optimizations and testing are recommended. Mammalian expression plasmids for the generation of the recombinant proteins are available from the corresponding author and from BEI Resources.

This protocol can be used for both expression vectors: the one expressing secreted RBD as well as the one expressing a soluble, trimeric version of the SARS-CoV-2 spike protein. Expression levels of the RBD are very high in our hands (>20 mg/L culture), while expression levels for the full-length spike are lower (approximately 4 to 5 mg/L). Therefore, we use the recombinant RBD for initial screening ELISAs and the full-length spike for confirmatory ELISAs (as described in Basic Protocol 2). The expression vector constructs were described previously (Amanat et al., 2020). In brief, the sequences used for both proteins are based on the genomic sequence of the first isolate, Wuhan-Hu-1, which was released on January 10, 2020 (GenBank: MN908947.3). Sequences were codon-optimized for mammalian cell expression. The full-length spike protein sequence was modified to remove the polybasic cleavage site, which is recognized by furin, and to add a pair of stabilizing mutations (Figure 2). These two modifications were included to enhance the stability of the protein based on published literature (Amanat et al., 2020). The plasmids are grown in E. coli at 37°C (or 30°C) at 225 rpm in Luria-Bertani (LB) broth with ampicillin (LB-amp) in shaker flasks overnight. High-quality plasmid DNA can be obtained using commercially available maxiprep kits (ideally with an endotoxin-removal step). Importantly, other cell lines (293T, CHO, etc.), other media, transfection reagents, and more sophisticated protein purification methods might be used as alternatives if available.

• RBD = receptor-binding domain of SARS-CoV-2 (NR-52306)
• PBS = phosphate-buffered saline
• RT = room temperature (18° to 25°C)
• MEM = Minimum Essential Medium
• DNA = deoxyribonucleic acid
• Ni-NTA = nickel-nitrilotriacetic acid

The purpose of this protocol is to describe the procedure for measuring human antibody responses to the recombinant receptor-binding domain (RBD) of the spike protein or full-length spike protein of SARS-CoV-2 and to ensure the reproducibility and consistency of the obtained results.

We developed this as a two-stage ELISA in which the first stage (‘a’ steps below) includes relatively high-throughput screening of samples in a single serum dilution against the RBD (which expresses very well and therefore can be produced in greater quantities). This is followed by a second stage (‘b’ steps below) in which positive samples from the first stage undergo a confirmatory ELISA against the full-length spike protein (which is harder to express; therefore there is usually less available). For the second stage, a dilution curve is performed. Typically, if only one operator is available, screening ELISAs can be run in the morning (760 samples/10 plates per run) and confirmatory ELISAs can be run in the afternoon (140 samples/10 plates per run). Of note, we describe the assay here as it is set up in our laboratory. We use a plate washer and a plate reader, but no automated system. The protocol can be adapted to use with an automated liquid handler. In addition, one of the difficulties in setting up the assay is the availability of appropriate negative and positive controls. Negative controls are easier to come by, and can be serum pools taken before 2020. Positive controls can be convalescent samples from COVID19 patients or monoclonal antibodies (mAbs) like CR3022 (ter Meulen et al., 2006; Tian et al., 2020). If no human sera or mAbs are available, mouse mAbs, mouse sera against SARS-CoV-2, other animal sera against SARS-CoV-2, or anti−His tag antibodies (the proteins are His-tagged) can be used. However, in this case, a different secondary antibody for the species from which the primary antibody is derived is needed for the positive control. Also, we recommend generating large batches of positive controls, which can be used for many runs. The positive control should be selected to result in a strong signal (recommend OD₄₉₀ of about 2.0), and should be clearly distinguishable from the negative controls. ELISAs can be run with either serum or plasma.

CAUTION : Before starting to work with COVID19 samples, please consult with your local biosafety officer regarding which precautions, personal protective equipment and protective measures are required.

NOTE:

• ELISA = enzyme-linked immunosorbent assay
• PBS = phosphate-buffered saline
• RT = room temperature (18° to 25°C)
• HRP = horseradish peroxidase
• HCl = hydrochloric acid
• OPD = O -phenylenediamine dihydrochloride

NOTE : RBD or full-length spike might be used for both ELISA stages if only one antigen is available. In addition, only the “a” steps (not recommended) or only the “b” steps might be performed, if fewer resources are available.

Elution buffer (4 L)

• 31.74 g NaH₂PO_4.·H₂O
• 70.16 g NaCl
• 64.0 g imidazole (Sigma-Aldrich # I5513 or equivalent; final concentration is 235 mM)
• 4 L distilled water
• Store at room temperature up to 4 months

Use distilled water filtered using a 0.22-µm Stericup vacuum filtration system.

Phosphate-buffered saline with 0.1% Tween 20 (PBS-T; 50 L)

• 45 L distilled water
• 5 L 10× PBS (Corning™ #46013CM or equivalent))
• 50 ml Tween 20 (Fisher Bioreagents #BP337-500 or equivalent)
• Store at room temperature for to 4 months

Wash buffer (4 L)

• 31.74 g NaH₂PO_4·H₂O
• 70.16 g NaCl
• 5.44 g imidazole (Sigma-Aldrich # I5513 or equivalent; final concentration is 20 mM)
• 4 L distilled water
• Store at room temperature up to 4 months

Use distilled water filtered using a 0.22-µm Stericup vacuum filtration system.

Background Information

The protein expression and purification methods (Basic Protocol 1) described in this article are based on well-established techniques. The expression plasmids and protein sequences have been optimized to increase protein stability and yield (Amanat et al., 2020). Plasmids can be requested from the Krammer laboratory or can be found on BEI Resources. The ELISA protocol (Basic Protocol 2) has been designed to allow for high-throughput screening of many samples per day, followed by a confirmatory step to verify presumptive positive results. The ELISA assay itself is based on well-established protocols and has been optimized for the use of SARS-CoV-2 antigens.

Critical Parameters and Troubleshooting

The most common problem for the transfection (Basic Protocol 1) is low cell viability before performing the transfection. The cells need to be 90% to 95% viable. The absence of antibiotics/antifungals requires good sterile technique to prevent contamination. Sterile plasmid preparations are also recommended, and it is important to add the enhancer to the shaking flasks 16 hr post-transfection.

For the protein purification, we recommend always using fresh Ni-NTA resin to prevent cross-contamination with other proteins. Harvested supernatant should be ideally processed immediately to ensure protein integrity. To make filtering of the supernatant easier, an additional centrifugation step (after pelleting the cells) is recommended to pellet residual cells and other particles. When performing buffer exchange using Amicon Ultra Centrifugal Filter Units, make sure to use the right-size cut-off (use smaller cut-off for RBD). It is recommended that purified protein be diluted to a concentration of about 2 mg/ml. Storage at higher concentrations may result in aggregation of protein.

For the ELISA (Basic Protocol 2), performing all of the washing steps and adhering to the incubation times are important to achieve low background reactivity. Most critical are the incubation times for the secondary antibody and the substrate (OPD and HCl for stopping the reaction). In addition, touching wells with tips when transferring secondary antibody and substrate can result in higher background and possibly false positive wells, and needs to be avoided. In preparing the OPD, it is also important to dissolve the gold tablet fully and only add the silver tablet right before the substrate is added to the ELISA plate.

Understanding Results

We expect expression levels of the RBD to be above 20 mg per L of culture cells and expression of the full-length spike protein to be approximately 4 mg per L of 293Fs, using a gravity-flow protein-purification strategy. When running the SDS-PAGE to confirm protein integrity, clear single bands are expected for the RBD and full-length spike at around 25 to 30 kDa and ∼190 kDa, respectively. Additionally, ELISAs with positive and negative controls (e.g., monoclonal antibodies) are performed to confirm correct protein folding. We expect a good binding profile for the positive control and low-to-no background reactivity for the negative control.

Time Considerations

Basic Protocols 1 and 2 can be completed in about 6 days. Basic Protocol 1 takes about 4 days. Growing up a cryostock of 293F cells, bringing them to passage 4 (recommended before transfection), and obtaining a sufficient cell number would take another few days; this is not taken into account in the protocol. Basic Protocol 2 takes at least 2 days (antigen coating on day 1 and running the ELISA on day 2). The screening ELISA could be performed in the morning and the confirmatory ELISA in the afternoon, or the assays can be done on consecutive days.

Acknowledgements

We thank Dr. Raffael Nachbagauer (Icahn School for Medicine at Mount Sinai) and Dr. Aubree Gordon (University of Michigan) for critical reading and constructive comments. Development of this protocol was partially supported by the NIAID Centers of Excellence for Influenza Research and Surveillance (CEIRS) contract HHSN272201400008C.

Philanthropic donations in support of our work are much appreciated, since the reagents are shared free of charge with the scientific community. Please contact Vanesa Saric (vanesa.saric@mountsinai.org) for further information.

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