Immunization with the receptor-binding domain of SARS-CoV-2 elicits antibodies cross-neutralizing SARS-CoV-2 and SARS-CoV without antibody-dependent enhancement
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Abstract
Abstract Recently emerged severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is the pathogen responsible for the ongoing coronavirus disease 2019 (COVID-19) pandemic. Currently, there is no vaccine available for preventing SARS-CoV-2 infection. Like closely related severe acute respiratory syndrome coronavirus (SARS-CoV), SARS-CoV-2 also uses its receptor-binding domain (RBD) on the spike (S) protein to engage the host receptor, human angiotensin-converting enzyme 2 (ACE2), facilitating subsequent viral entry. Here we report the immunogenicity and vaccine potential of SARS-CoV-2 RBD (SARS2-RBD)-based recombinant proteins. Immunization with SARS2-RBD recombinant proteins potently induced a multi-functional antibody response in mice. The resulting antisera could efficiently block the interaction between SARS2-RBD and ACE2, inhibit S-mediated cell-cell fusion, and neutralize both SARS-CoV-2 pseudovirus entry and authentic SARS-CoV-2 infection. In addition, the anti-RBD sera also exhibited cross binding, ACE2-blockade, and neutralization effects towards SARS-CoV. More importantly, we found that the anti-RBD sera did not promote antibody-dependent enhancement of either SARS-CoV-2 pseudovirus entry or authentic virus infection of Fc receptor-bearing cells. These findings provide a solid foundation for developing RBD-based subunit vaccines for SARS-CoV2.
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The RBD can induce strong humoral and cellular immune responses when used as an antigen in various SARS-CoV and MERS-CoV studies.
“the RBD can induce strong humoral and cellular immune responses when used as an antigen in various SARS-CoV and MERS-CoV studies),8, 9, 10”
From Safety and immunogenicity of the SARS-CoV-2 ARCoV mRNA vaccine in Chinese adults: a randomised, double-blind, placebo-controlled, phase 1 trial (2022) · cites this paper as [10]
The paper’s opening passage (page unavailable) says SARS-CoV and MERS-CoV RBD proteins have been shown to induce protective neutralizing antibodies, supporting the humoral-response claim. It does not report cellular immune responses in those studies; its own immunization experiments also assess antibodies, not cellular immunity. (LLM, conf=0.88)
Experimental — accuracy not yet measuredThe receptor binding domain (RBD) of SARS-CoV-2 spike protein had been identified to play a key role in helping coronaviruses to enter human cells.
“the receptor binding domain (RBD) of SARS-CoV-2 spike protein had been identified to play a key role in helping coronaviruses to enter human cells”
From Safety and immunogenicity of the SARS-CoV-2 ARCoV mRNA vaccine in Chinese adults: a randomised, double-blind, placebo-controlled, phase 1 trial (2022) · cites this paper as [10]
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Cites
A novel coronavirus from patients with pneumonia in China, 2019
Zhu, N., Zhang, D., Wang, W., Li, X., Yang, B., Song, J., Zhao, X., Huang, B., Shi, W., Lu, R., et al. (2020) · New England Journal of Medicine · doi:10.1056/nejmoa2001017 · Cited by 28,244 · see citing works
A pneumonia outbreak associated with a new coronavirus of probable bat origin
Zhou, P., Yang, X.-L., Wang, X.-G., Hu, B., Zhang, L., Zhang, W., Si, H.-R., Zhu, Y., Li, B., Huang, C.-L., et al. (2020) · Nature · doi:10.1038/s41586-020-2012-7 · Cited by 21,969 · see citing works
Wu, Z., & McGoogan, J. M. (2020) · JAMA · doi:10.1001/jama.2020.2648 · Cited by 17,016 · see citing works
Structure, function and antigenicity of the SARS-CoV-2 spike glycoprotein
Walls, A. C., Park, Y.-J., Tortorici, M. A., Wall, A., McGuire, A. T., & Veesler, D. (2020) · doi:10.1101/2020.02.19.956581 · Cited by 8,586 · see citing works
Gorbalenya, A. E., Baker, S. C., Baric, R. S., de Groot, R. J., Drosten, C., Gulyaeva, A. A., Haagmans, B. L., Lauber, C., Leontovich, A. M., Neuman, B. W., et al. (2020) · Nature Microbiology · doi:10.1038/s41564-020-0695-z · Cited by 8,436 · see citing works
Structure of the SARS-CoV-2 spike receptor-binding domain bound to the ACE2 receptor
Lan, J., Ge, J., Yu, J., Shan, S., Zhou, H., Fan, S., Zhang, Q., Shi, X., Wang, Q., Zhang, L., et al. (2020) · Nature · doi:10.1038/s41586-020-2180-5 · Cited by 5,983 · see citing works
Structural basis for the recognition of SARS-CoV-2 by full-length human ACE2
Yan, R., Zhang, Y., Li, Y., Xia, L., Guo, Y., & Zhou, Q. (2020) · Science · doi:10.1126/science.abb2762 · Cited by 4,950 · see citing works
Structural basis of receptor recognition by SARS-CoV-2
Shang, J., Ye, G., Shi, K., Wan, Y., Luo, C., Aihara, H., Geng, Q., Auerbach, A., & Li, F. (2020) · Nature · doi:10.1038/s41586-020-2179-y · Cited by 3,661 · see citing works
Structural and Functional Basis of SARS-CoV-2 Entry by Using Human ACE2
Wang, Q., Zhang, Y., Wu, L., Niu, S., Song, C., Zhang, Z., Lu, G., Qiao, C., Hu, Y., Yuen, K.-Y., et al. (2020) · Cell · doi:10.1016/j.cell.2020.03.045 · Cited by 2,892 · see citing works
Genome Composition and Divergence of the Novel Coronavirus (2019-nCoV) Originating in China
Wu, A., Peng, Y., Huang, B., Ding, X. L., Wang, X., Niu, P., Meng, J., Zhu, Z., Zhang, Z., Wang, J., et al. (2020) · Cell Host & Microbe · doi:10.1016/j.chom.2020.02.001 · Cited by 2,363 · see citing works
Development of an inactivated vaccine candidate for SARS-CoV-2
Gao, Q., Bao, L., Mao, H., Wang, L., Xu, K., Yang, M., Li, Y., Zhu, L., Wang, N., Lv, Z., et al. (2020) · Science · doi:10.1126/science.abc1932 · Cited by 1,434 · see citing works
SARS-CoV-2 Vaccines: Status Report
Amanat, F., & Krammer, F. (2020) · Immunity · doi:10.1016/j.immuni.2020.03.007 · Cited by 1,120 · see citing works
A human monoclonal antibody blocking SARS-CoV-2 infection
Wang, C., Li, W., Drabek, D., Okba, N. M. A., van Haperen, R., Osterhaus, A. D. M. E., van Kuppeveld, F. J. M., Haagmans, B. L., Grosveld, F. G., & Bosch, B. (2020) · Nature Communications · doi:10.1038/s41467-020-16256-y · Cited by 1,115 · see citing works
Immunogenicity and structures of a rationally designed prefusion MERS-CoV spike antigen
Pallesen, J., Wang, N., Corbett, K. S., Wrapp, D., Kirchdoerfer, R. N., Turner, H. L., Cottrell, C. A., Becker, M. M., Wang, L., Shi, W., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1707304114 · Cited by 1,073 · see citing works
Liu, L., Wei, Q., Lin, Q., Fang, J., Wang, H., Kwok, H., Tang, H., Nishiura, K., Peng, J., Tan, Z., et al. (2019) · JCI Insight · doi:10.1172/jci.insight.123158 · Cited by 830 · see citing works
Self-citationMolecular Mechanism for Antibody-Dependent Enhancement of Coronavirus Entry
Wan, Y., Shang, J., Sun, S., Tai, W., Chen, J., Geng, Q., He, L., Chen, Y., Wu, J., Shi, Z., et al. (2019) · Journal of Virology · doi:10.1128/jvi.02015-19 · Cited by 662 · see citing works
The SARS-CoV-2 Vaccine Pipeline: an Overview
Chen, W., Strych, U., Hotez, P. J., & Bottazzi, M. E. (2020) · Current Tropical Medicine Reports · doi:10.1007/s40475-020-00201-6 · Cited by 512 · see citing works
The race for coronavirus vaccines: a graphical guide
Callaway, E. (2020) · Nature · doi:10.1038/d41586-020-01221-y · Cited by 492 · see citing works
Bolles, M., Deming, D., Long, K., Agnihothram, S., Whitmore, A., Ferris, M., Funkhouser, W., Gralinski, L., Totura, A., Heise, M., et al. (2011) · Journal of Virology · doi:10.1128/jvi.06048-11 · Cited by 477 · see citing works
Antibody-dependent SARS coronavirus infection is mediated by antibodies against spike proteins
Wang, S., Tseng, S., Yen, C., Yang, J.-Y., Tsao, C.-H., Shen, C.-W., Chen, K.-H., Liu, F., Liu, W.-T., Chen, Y. A., et al. (2014) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2014.07.090 · Cited by 421 · see citing works
Jaume, M., Yip, M., Cheung, C. Y., Leung, N., Li, P. H., Kien, F., Dutry, I., Callendret, B., Escriou, N., Altmeyer, R. M., et al. (2011) · Journal of Virology · doi:10.1128/jvi.00671-11 · Cited by 312 · see citing works
Wang, Q., Zhang, L., Kuwahara, K., Li, L., Liu, Z., Li, T., Zhu, H., Liu, J., Xu, Y., Xie, J., et al. (2016) · ACS Infectious Diseases · doi:10.1021/acsinfecdis.6b00006 · Cited by 297 · see citing works
Physiological and molecular triggers for SARS-CoV membrane fusion and entry into host cells
Millet, J. K., & Whittaker, G. R. (2017) · Virology · doi:10.1016/j.virol.2017.12.015 · Cited by 291 · see citing works
Antibody-dependent infection of human macrophages by severe acute respiratory syndrome coronavirus
Yip, M., Leung, N., Cheung, C. Y., Li, P. H., Lee, H. H. Y., Daëron, M., Peiris, M. J. S., Bruzzone, R., & Jaume, M. (2014) · Virology Journal · doi:10.1186/1743-422x-11-82 · Cited by 249 · see citing works
Weiss, R. C., & Scott, F. W. (1981) · Comparative Immunology Microbiology and Infectious Diseases · doi:10.1016/0147-9571(81)90003-5 · Cited by 242 · see citing works
Vaccine-induced enhancement of viral infections
Huisman, W., Martina, B., Rimmelzwaan, G., Gruters, R., & Osterhaus, A. (2008) · Vaccine · doi:10.1016/j.vaccine.2008.10.087 · Cited by 183 · see citing works
Olsen, C. W., Corapi, W. V., Ngichabe, C. K., Baines, J. D., & Scott, F. W. (1992) · Journal of Virology · doi:10.1128/jvi.66.2.956-965.1992 · Cited by 179 · see citing works
COVID-19 vaccine design: the Janus face of immune enhancement
Hotez, P. J., Corry, D. B., & Bottazzi, M. E. (2020) · Nature reviews. Immunology · doi:10.1038/s41577-020-0323-4 · Cited by 168 · see citing works
Ligation of Fc gamma receptor IIB inhibits antibody-dependent enhancement of dengue virus infection
Chan, K. R., Zhang, S. L.-X., Tan, H. C., Chan, Y., Chow, A. Y., Lim, A. P. C., Vasudevan, S. G., Hanson, B. J., & Ooi, E. E. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1106568108 · Cited by 143 · see citing works
Corapi, W. V., Olsen, C. W., & Scott, F. (1992) · Journal of Virology · doi:10.1128/jvi.66.11.6695-6705.1992 · Cited by 129 · see citing works
Prospects for a MERS-CoV spike vaccine
Zhou, Y., Jiang, S., & Du, L. (2018) · Expert Review of Vaccines · doi:10.1080/14760584.2018.1506702 · Cited by 126 · see citing works
Tseng, C.-T., Sbrana, E., Iwata-Yoshikawa, N., Newman, P. C., Garron, T., Atmar, R. L., Peters, C. J., & Couch, R. B. (2012) · PLoS ONE · doi:10.1371/annotation/2965cfae-b77d-4014-8b7b-236e01a35492 · Cited by 122 · see citing works
CTLA-4 regulates cell cycle progression during a primary immune response
Greenwald, R. J., Oosterwegel, M. A., van der Woude, D., Kubal, A., Mandelbrot, D. A., Boussiotis, V. A., & Sharpe, A. H. (2002) · European Journal of Immunology · doi:10.1002/1521-4141(200202)32:2 · Cited by 120 · see citing works
Luo, F., Liao, F., Wang, H., Tang, H.-B., Yang, Z.-Q., & Hou, W. (2018) · Virologica Sinica · doi:10.1007/s12250-018-0009-2 · Cited by 82 · see citing works
Self-citationYe, X., Ku, Z., Liu, Q., Wang, X., Shi, J., Zhang, Y., Kong, L., Cong, Y., & Huang, Z. W. (2013) · Journal of Virology · doi:10.1128/jvi.01848-13 · Cited by 70 · see citing works
Self-citationBlock, O. K. T., Rodrigo, W. W. S. I., Quinn, M., Jin, X., Rose, R. C., & Schlesinger, J. J. (2010) · Vaccine · doi:10.1016/j.vaccine.2010.10.004 · Cited by 60 · see citing works
Structural basis for receptor recognition by the novel coronavirus from WuhanPreprint
Shang, J., Ye, G., Shi, K., et al. (2020) · Research Square · doi:10.21203/rs.2.24749/v1 · Cited by 49 · see citing works
Jiang, S., Lu, L., Liu, Q., Xu, W., & Du, L. (2012) · Emerging Microbes & Infections · doi:10.1038/emi.2012.1 · Cited by 40 · see citing works
Zhao, F., Xu, Y., Lavillette, D., Zhong, J., Zou, G., & Long, G. (2018) · Scientific Reports · doi:10.1038/s41598-018-28890-0 · Cited by 33 · see citing works
Self-citationAntibody-dependent enhancement and vaccine development
Thomas, S., Redfern, J. B., Lidbury, B. A., & Mahalingam, S. (2006) · Expert Review of Vaccines · doi:10.1586/14760584.5.4.409 · Cited by 31 · see citing works
Sun, J., Li, M., Wang, Y., Hao, P., & Jin, X. (2017) · Vaccine · doi:10.1016/j.vaccine.2017.09.063 · Cited by 29 · see citing works
Huisman, W., Karlas, J. A., Siebelink, K. H. J., Huisman, R. C., de Ronde, A., Francis, M. J., Rimmelzwaan, G. F., & Osterhaus, A. D. M. E. (1998) · Vaccine · doi:10.1016/s0264-410x(97)00184-9 · Cited by 24 · see citing works
Zhang, W., Qu, P., Li, D., Zhang, C., Liu, Q., Zou, G., Dupont‐Rouzeyrol, M., Lavillette, D., Jin, X., Yin, F., et al. (2019) · Antiviral Research · doi:10.1016/j.antiviral.2019.104578 · Cited by 21 · see citing works
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Flagged first, then by citations
Cited by
Sorted by citations
Starr, T. N., Greaney, A. J., Hilton, S. K., Ellis, D., Crawford, K. H. D., Dingens, A. S., Navarro, M. J., Bowen, J. E., Tortorici, M. A., Walls, A. C., et al. (2020) · Cell · doi:10.1016/j.cell.2020.08.012 · Cited by 1,956 · see citing works
Molecular mechanism of interaction between SARS-CoV-2 and host cells and interventional therapy
Zhang, Q., Xiang, R., Huo, S., Zhou, Y., Jiang, S., Wang, Q., & Yu, F. (2021) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-021-00653-w · Cited by 341 · see citing works
Zhou, Y., Liu, Z., Li, S. N., Xu, W., Zhang, Q., da Silva, I. T., Li, C., Wu, Y., Jiang, Q., Liu, Z., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.108699 · Cited by 134 · see citing works
Self-citationCarrillo, J., Izquierdo‐Useros, N., Ávila‐Nieto, C., Pradenas, E., Clotet, B., & Blanco, J. (2020) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2020.10.108 · Cited by 114 · see citing works
Valdés-Balbín, Y., Santana-Mederos, D., Quintero, L., Fernández-Castillo, S., Rodríguez, L., Ramírez, B. S., Pérez-Nicado, R., Acosta, C., Méndez, Y., Ricardo, M. G., et al. (2021) · ACS Chemical Biology · doi:10.1021/acschembio.1c00272 · Cited by 86 · see citing works
COVID-19 Vaccines: “Warp Speed” Needs Mind Melds, Not Warped Minds
Moore, J. P., & Klasse, P. J. (2020) · Journal of Virology · doi:10.1128/jvi.01083-20 · Cited by 86 · see citing works
Chen, G.-L., Li, X.-F., Dai, X.-H., Li, N., Cheng, M.-L., Huang, Z., Shen, J., Ge, Y.-H., Shen, Z.-W., Deng, Y.-Q., et al. (2022) · The Lancet Microbe · doi:10.1016/s2666-5247(21)00280-9 · Cited by 82 · see citing works
Self-citationLandscape and selection of vaccine epitopes in SARS-CoV-2
Smith, C. C., Olsen, K. S., Gentry, K. M., Sambade, M. J., Beck, W. A., Garness, J. A., Entwistle, S., Willis, C., Vensko, S. P., II, Woods, A., et al. (2021) · Genome Medicine · doi:10.1186/s13073-021-00910-1 · Cited by 64 · see citing works
Zhao, H., Wang, T.-C., Li, X.-F., Zhang, N.-N., Li, L., Zhou, C., Deng, Y.-Q., Cao, T.-S., Yang, G., Li, R.-T., et al. (2021) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-021-00861-4 · Cited by 60 · see citing works
Self-citationValdés-Balbín, Y., Santana-Mederos, D., Paquet, F., Fernández-Castillo, S., Climent, Y., Chiodo, F., Rodríguez, L., Ramírez, B. S., León, K., Hernández, T., et al. (2021) · ACS Central Science · doi:10.1021/acscentsci.1c00216 · Cited by 53 · see citing works
Zang, J., Zhu, Y., Zhou, Y., Gu, C., Yi, Y., Wang, S., Xu, S., Hu, G., Du, S., Yin, Y., et al. (2021) · Cell Discovery · doi:10.1038/s41421-021-00315-9 · Cited by 58 · see citing works
Self-citationvan Dülmen, M., Muthmann, N., & Rentmeister, A. (2021) · Angewandte Chemie International Edition · doi:10.1002/anie.202100352 · Cited by 54 · see citing works
Spike Glycoprotein-Mediated Entry of SARS Coronaviruses
Wang, L., & Xiang, Y. (2020) · Viruses · doi:10.3390/v12111289 · Cited by 51 · see citing works
Design of a highly thermotolerant, immunogenic SARS-CoV-2 spike fragment
Malladi, S. K., Singh, R., Pandey, S., Gayathri, S., Kanjo, K., Ahmed, S., Khan, M. S. A. A., Kalita, P., Girish, N., Upadhyaya, A., et al. (2020) · Journal of Biological Chemistry · doi:10.1074/jbc.ra120.016284 · Cited by 52 · see citing works
Multiple Routes of Antibody-Dependent Enhancement of SARS-CoV-2 Infection
Okuya, K., Hattori, T., Saito, T., Takadate, Y., Sasaki, M., Furuyama, W., Marzi, A., Ohiro, Y., Konno, S., Hattori, T., et al. (2022) · Microbiology Spectrum · doi:10.1128/spectrum.01553-21 · Cited by 51 · see citing works
Wo, J., Lv, Z.-Y., Sun, J., Tang, H., Qi, N., & Ye, B. (2022) · iScience · doi:10.1016/j.isci.2022.105772 · Cited by 50 · see citing works
Self-citationMerkuleva, I. A., Shcherbakov, D., Borgoyakova, M. B., Shanshin, D., Rudometov, A. P., Karpenko, L., Belenkaya, S., Isaeva, A. A., Nesmeyanova, V. S., Kazachinskaia, E., et al. (2022) · Vaccines · doi:10.3390/vaccines10010096 · Cited by 42 · see citing works
Malladi, S. K., Patel, U. R., Rajmani, R. S., Singh, R., Pandey, S., Kumar, S., Khaleeq, S., van Vuren, P. J., Riddell, S., Goldie, S., et al. (2021) · ACS Infectious Diseases · doi:10.1021/acsinfecdis.1c00276 · Cited by 38 · see citing works
Liu, X., Drelich, A. K., Li, W., Chen, C., Sun, Z., Shi, M., Adams, C., Mellors, J. W., Tseng, C.-T. K., & Dimitrov, D. S. (2020) · Vaccine · doi:10.1016/j.vaccine.2020.09.058 · Cited by 39 · see citing works
The role and uses of antibodies in COVID-19 infections: a living review
Scourfield, D. O., Reed, S. G., Quastel, M. N., Alderson, J., Bart, V. M. T., Crespo, A. T., Jones, R. E., Pring, E., Richter, F. C., Ahern, D., et al. (2021) · Oxford Open Immunology · doi:10.1093/oxfimm/iqab003 · Cited by 28 · see citing works
Relationship between SARS-CoV-2 antibody titer and the severity of COVID-19
Park, J. H., Cha, M. J., Choi, H., Kim, M., Chung, J.-W., Lee, K., Jeong, D. G., Baek, M. S., Kim, W., Lim, Y., et al. (2022) · Journal of Microbiology Immunology and Infection · doi:10.1016/j.jmii.2022.04.005 · Cited by 28 · see citing works
Laing, E. D., Sterling, S. L., Richard, S. A., Epsi, N. J., Coggins, S. A., Samuels, E. C., Phogat, S., Yan, L., Moreno, N., Coles, C. L., et al. (2021) · medRxiv · doi:10.1101/2021.02.10.21251518 · Cited by 29 · see citing works
Cao, M., Su, X., & Jiang, S. (2021) · Stem Cell Reports · doi:10.1016/j.stemcr.2020.12.010 · Cited by 27 · see citing works
Santana-Mederos, D., Pérez-Nicado, R., Climent-Ruíz, Y., Rodríguez, L., Ramírez, B. S., Perez-Rodriguez, S., Rodriguez, M., Labrada, C., Hernández, T., Díaz-Hernández, M., et al. (2021) · RSC Chemical Biology · doi:10.1039/d1cb00200g · Cited by 26 · see citing works
Development of an LNP-Encapsulated mRNA-RBD Vaccine against SARS-CoV-2 and Its Variants
Liu, C., Rcheulishvili, N., Shen, Z., Papukashvili, D., Xie, F., Wang, Z., Wang, X., He, Y., & Wang, P. G. (2022) · Pharmaceutics · doi:10.3390/pharmaceutics14051101 · Cited by 26 · see citing works
Xu, K., An, Y., Li, Q., Huang, W.-J., Han, Y., Zheng, T., Fang, F., Liu, H., Liu, C.-Y., Gao, P., et al. (2021) · Emerging Microbes and Infections · doi:10.1080/22221751.2021.1959270 · Cited by 25 · see citing works
Self-citationOrtega-Rivera, O. A., Shukla, S., Shin, M. D., Chen, A., Beiss, V., Moreno‐Gonzalez, M. A., Zheng, Y., Clark, A. E., Carlin, A. F., Pokorski, J. K., et al. (2021) · ACS Infectious Diseases · doi:10.1021/acsinfecdis.1c00410 · Cited by 26 · see citing works
Jeong, H., Choi, Y.-M., Seo, H., & Kim, B. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.637654 · Cited by 21 · see citing works
Cobb, R. R., Nkolola, J. P., Gilchuk, P., Chandrashekar, A., Yu, J.-Y., House, R., Earnhart, C., Dorsey, N., Hopkins, S., Snow, D. M., et al. (2022) · i Medicina · doi:10.1016/j.medj.2022.01.004 · Cited by 20 · see citing works
Clark, N. M., Janaka, S., Hartman, W., Stramer, S., Goodhue, E., Weiss, J., Evans, D. T., & Connor, J. (2022) · PLoS ONE · doi:10.1371/journal.pone.0257930 · Cited by 15 · see citing works
Núñez-Muñoz, L. A., Marcelino-Pérez, G., Calderón-Pérez, B., Pérez-Saldívar, M., Acosta-Virgen, K. B., González-Conchillos, H., Vargas-Hernández, B. Y., Olivares-Martínez, A., Ruíz‐Medrano, R., Roa-Velázquez, D., et al. (2021) · Vaccines · doi:10.3390/vaccines9080928 · Cited by 17 · see citing works
Nechooshtan, R., Ehrlich, S., Vitikainen, M., Makovitzki, A., Dor, E., Marcus, H., Hefetz, I., Pitel, S., Wiebe, M., Huuskonen, A., et al. (2022) · Vaccines · doi:10.3390/vaccines10122119 · Cited by 10 · see citing works
Marcos-Villar, L., Perdiguero, B., López‐Bravo, M., Zamora, C., Sin, L., Álvarez, E., Sorzano, C. Ó. S., Sánchez-Cordón, P. J., Casasnovas, J. M., Astorgano, D., et al. (2024) · Emerging Microbes & Infections · doi:10.1080/22221751.2024.2387906 · Cited by 11 · see citing works
Design and Immunological Properties of the Novel Subunit Virus-like Vaccine against SARS-CoV-2
Krasilnikov, I. V., Kudriavtsev, A. V., Vakhrusheva, A., Frolova, M. E., Ivanov, A. V., Stukova, M., Romanovskaya-Romanko, E., Vasilyev, K., Mushenkova, N. V., & Isaev, A. A. (2022) · Vaccines · doi:10.3390/vaccines10010069 · Cited by 11 · see citing works
Sulbarán, G., Maisonnasse, P., Amen, A., Effantin, G., Guilligay, D., Dereuddre‐Bosquet, N., Burger, J. A., Poniman, M., Grobben, M., Buisson, M., et al. (2022) · Cell Reports Medicine · doi:10.1016/j.xcrm.2022.100528 · Cited by 10 · see citing works
Laing, E. D., Sterling, S. L., Richard, S. A., Phogat, S., Samuels, E. C., Epsi, N. J., Yan, L., Moreno, N., Coles, C. L., Mehalko, J. L., et al. (2020) · medRxiv · doi:10.1101/2020.10.14.20207050 · Cited by 10 · see citing works
Laing, E. D., Sterling, S. L., Richard, S. A., Epsi, N. J., Phogat, S., Samuels, E. C., Yan, L., Moreno, N., Coles, C. L., Drew, M. R., et al. (2020) · Research Square · doi:10.21203/rs.3.rs-105768/v1 · Cited by 10 · see citing works
Peptide candidates for the development of therapeutics and vaccines against β-coronavirus infection
Chourasia, R., Padhi, S., Phukon, L. C., Abedin, M. M., Sirohi, R., Singh, S. P., & Rai, A. K. (2022) · Bioengineered · doi:10.1080/21655979.2022.2060453 · Cited by 9 · see citing works
Yang, Y. P., Zang, J., Xu, S., Zhang, X., Yuan, S., Wang, H., Lavillette, D., Zhang, C., & Huang, Z. W. (2021) · Viruses · doi:10.3390/v13081421 · Cited by 8 · see citing works
Self-citationDesign of a Multi-Valent SARS-CoV-2 Peptide Vaccine for Broad Immune Protection via Deep Learning
Feng, Z., Pang, X., Xu, Q., Gu, Z., Li, S., Zhu, L., & Li, H. (2025) · Engineering · doi:10.1016/j.eng.2025.04.025 · Cited by 7 · see citing works
Lv, H., Tsang, O., So, R. T. Y., Wang, Y.-Q., Yuan, M., Liu, H., Yip, G. K., Teo, Q., Lin, Y., Liang, W.-W., et al. (2021) · European Journal of Immunology · doi:10.1002/eji.202149234 · Cited by 6 · see citing works
A Naïve Phage Display Library-Derived Nanobody Neutralizes SARS-CoV-2 and Three Variants of Concern
Wu, D., Cong, J., Wei, J., Hu, J., Sun, W., Ran, W., Liao, C., Zheng, H., & Ye, L. (2023) · International Journal of Nanomedicine · doi:10.2147/ijn.s427990 · Cited by 7 · see citing works
Trivalent mRNA Vaccine against SARS-CoV-2 and Variants with Effective Immunization
Wang, J., Zhang, Y., Liu, C., Zha, W., Dong, S., Wang, Y., Jiang, Y., Xing, H., & Li, X. (2023) · Molecular Pharmaceutics · doi:10.1021/acs.molpharmaceut.2c00860 · Cited by 7 · see citing works
Zhang, X., Su, Y., Ao, D., Hong, Y., Zou, M., Xie, J., Zhou, Q., Wang, Y., He, W., & Chen, Y. (2025) · Journal of Applied Electrochemistry · doi:10.1007/s10800-025-02264-7 · Cited by 6 · see citing works
Clark, N. M., Janaka, S., Hartman, W., Stramer, S., Goodhue, E., Weiss, J., Evans, D. T., & Connor, J. (2021) · bioRxiv · doi:10.1101/2021.09.14.460394 · Cited by 5 · see citing works
Chiu, C.-T., Tsai, H., Chen, J.-Y., Hu, C. J., & Chen, H. (2024) · International Journal of Nanomedicine · doi:10.2147/ijn.s463546 · Cited by 3 · see citing works
Exploring COVID-19: Relating the spike protein to infectivity, pathogenicity and Immunogenicity
Nikhra, V. (2021) · International Journal of Clinical Virology · doi:10.29328/journal.ijcv.1001029 · Cited by 3 · see citing works
van Dülmen, M., Muthmann, N., & Rentmeister, A. (2021) · Angewandte Chemie · doi:10.1002/ange.202100352 · Cited by 3 · see citing works
Design of a highly thermotolerant, immunogenic SARS-CoV-2 spike fragment immunogenPreprint
Malladi, S. K., Singh, R., Pandey, S., Gayathri, S., Kanjo, K., Ahmed, S., Khan, M. S., Kalita, P., Girish, N., Upadhyaya, A., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.08.15.252437 · Cited by 3 · see citing works
Gromova, M. S., Gromov, A. V., Grunina, T. M., Lyashchuk, A. M., Galushkina, Z. M., Субботина, М. Е., Esmagambetov, I. B., Ryabova, E. I., Prokofiev, V. V., Витальевна, К. А., et al. (2023) · Molecular Genetics Microbiology and Virology · doi:10.3103/s0891416823020052 · Cited by 2 · see citing works
Dulin, H., Barre, R. S., Xu, D., Neal, A., Vizcarra, E., Chavez, J. R., Ulu, A., Yang, M. S., Khan, S. R., Wuang, K., et al. (2024) · Journal of Virology · doi:10.1128/jvi.01571-23 · Cited by 2 · see citing works
Doroud, D., Larijani, M. S., Biglari, A., Ashrafian, F., Sabouni, T., Eybpoosh, S., Verez-Bencomo, V., Valdés-Balbín, Y., García-Rivera, D., Herrera-Rojas, Y., et al. (2024) · Scientific Reports · doi:10.1038/s41598-024-77331-8 · Cited by 2 · see citing works
Skin patch delivery of a SARS-CoV-2 spike DNA vaccine produces broad neutralising antibody responses
McMillan, C. L. D., Corner, A. V., Wijesundara, D. K., Choo, J. J. Y., Pittayakhajonwut, D., Poredi, I. K., Parry, R. H., Bindra, G. K., Bruce, K. L., Khromykh, A. A., et al. (2025) · Heliyon · doi:10.1016/j.heliyon.2025.e42533 · Cited by 2 · see citing works
Design and Immunogenicity of SARS-CoV-2 DNA Vaccine Encoding RBD-PVXCP Fusion Protein
Dormeshkin, D., Katsin, M., Stegantseva, M. V., Golenchenko, S., Shapira, M. A., Dubovik, S., Lutskovich, D. V., Kavaleuski, A., & Meleshko, A. (2023) · Vaccines · doi:10.3390/vaccines11061014 · Cited by 2 · see citing works
Design of Replication-Competent VSV- and Ervebo-Vectored Vaccines Against SARS-CoV-2
Liu, Q., Ding, Z., Lan, J., & Wong, G. (2021) · Methods in molecular biology · doi:10.1007/978-1-0716-1884-4_9 · Cited by 2 · see citing works
Antibodies Produced Toward Recombinant RBD and Nucleocapsid Neutralize SARS-COV-2
Rezaei, A., Nazarian, S., Samiei-Abianeh, H., Kordbacheh, E., Alizadeh, Z., & Gargari, S. L. M. (2022) · Avicenna Journal of Medical Biotechnology · doi:10.18502/ajmb.v14i4.10481 · Cited by 2 · see citing works
Volosnikova, E. A., Merkuleva, I. A., Esina, T. I., Щербаков, Д. Н., Borgoyakova, M. B., Исаева, А. А., Nesmeyanova, V. S., Волкова, Н. В., Belenkaya, S. V., Zaykovskaya, A. V., et al. (2023) · Vaccines · doi:10.3390/vaccines11040808 · Cited by 2 · see citing works
Lim, C. P., Bingöl, E. N., de Oliveira, J. J., Chuah, C., Khan, M. A., Douradinha, B. G., Leow, C. Y., & Leow, C. Y. (2026) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-026-05714-x · Cited by 1 · see citing works
Relating the SARS-CoV-2 Spike Protein to Infectivity, Pathogenicity, and Immunogenicity in COVID-19
Nikhra, V. (2021) · Annals of Immunology & Immunotherapy · doi:10.23880/aii-16000131
Homologous and heterologous serological response to the N-terminal domain of SARS-CoV-2Preprint
Lv, H., Tsang, O., So, R. T. Y., Wang, Y.-Q., Yuan, M., Liu, H., Yip, G. K., Teo, Q., Lin, Y., Liang, W.-W., et al. (2021) · bioRxiv · doi:10.1101/2021.02.17.431722
A combination of two human neutralizing antibodies prevents SARS-CoV-2 infection in rhesus macaquesPreprint
Cobb, R. R., Nkolola, J. P., Gilchuk, P., Chandrashekar, A., House, R. V., Earnhart, C. G., Dorsey, N., Hopkins, S. A., Snow, D. M., Chen, R. E., et al. (2021) · bioRxiv · doi:10.1101/2021.09.27.462074 · Cited by 1 · see citing works
Gromova, M. S., Gromov, A. V., Grunina, T. M., Lyashchuk, A. M., Galushkina, Z. M., Субботина, М. Е., Esmagambetov, I. B., Ryabova, E. I., Prokofiev, V. V., Витальевна, К. А., et al. (2023) · Molecular Genetics Microbiology and Virology (Russian) · doi:10.17116/molgen20234102128
Zareinejad, M. R., Behdani, M., Goodarzi, M. T., Oghalaie, A., Hosseininejad-Chafi, M., Bagheri, K. P., & Shahbazzadeh, D. (2025) · New Microbes and New Infections · doi:10.1016/j.nmni.2025.101634
Delta-Vac’ subunit vaccine induces strong humoral immune response against SARS-CoV-2
Nesmeyanova, V. S., Merkuleva, I. A., Исаева, А. А., Волкова, Н. В., Belenkaya, S. V., Borgoyakova, M. B., Volosnikova, E. A., Esina, T. I., Даниленко, Е. Д., Zaikovskaya, A. V., et al. (2025) · Medical Immunology (Russia) · doi:10.15789/1563-0625-dvc-2901
Additional file 1 of Landscape and selection of vaccine epitopes in SARS-CoV-2
Smith, C. C., Olsen, K. S., Gentry, K. M., Sambade, M., Beck, W. A., Garness, J. A., Entwistle, S., Willis, C., Vensko, S. P., II, Woods, A., et al. (2021) · Figshare · doi:10.6084/m9.figshare.14782768
Masangkay, C. B., Vinarao, J. G., Malbas, F. F., Quiñones, G. J., Lenon, M. S. L., Noveno, E. K., Diagmel, P. A., Babad, L., Noroña, M.-G., Demetria, C. S., et al. (2026) · International Journal of Infectious Diseases · doi:10.1016/j.ijid.2026.108461
Mechanisms of antibody-dependent enhancement and its research progress in animal coronaviruses
Zhou, Z., Liu, Y., Yang, M., Qiu, C., Xia, J., Huang, Y., & Zhou, Y. (2026) · Veterinary Research · doi:10.1186/s13567-026-01837-4
- Authors
- Zang, J., Gu, C., Zhou, B., Zhang, C., Yang, Y., Xu, S., Bai, L., Zhang, R., Deng, Q., Yuan, Z., Tang, H., Qu, D., Lavillette, D., Xie, Y., & Huang, Z.
- Affiliations
- Chinese Academy of Sciences (CN)
- Shanghai Medical College of Fudan University (CN)
- Corresponding author
- Lavillette, Dimitri
- Xie, Youhua
- Huang, Zhong
- Venue
- Cell Discovery
- Published
- 2020-09-03
- Volume
- 6
- Issue
- 1
- Pages
- 61-61
- ISSN
- 2056-5968 (ISSN-L)
- PMC
- PMC7471522
- OpenAlex
- W3082164758
- Cited by
- 67
- References
- 42
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 4 · 2023: 6 · 2022: 13 · 2021: 27 · 2020: 9
- FWCI
- 1.80
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Cell Discovery (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- HAL (submittedVersion, cc-by)
- Funders
- Ministry of Science and Technology of the People’;s Republic of China (2020YFC0845900)
- Chinese Academy of Sciences (XDB29040300)
- Topics
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Virus Infections Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › vaccines and immunoinformatics approaches
- Keywords
- SARS-CoV-2, receptor binding domain, spike protein, SARS-CoV, cross-neutralizing antibodies, antibody-dependent enhancement, vaccine immunization, ACE2 receptor, S1 subunit, COVID-19 pandemic
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