Abstract
The SARS-CoV-2 nucleocapsid protein has been detected in the plasma of COVID-19 patients, and its levels in the plasma correlate with the severity of the disease. It is also an immunomodulatory protein, triggering the release of proinflammatory cytokines. Complement system dysregulation in COVID-19 patients led us to hypothesize that either nucleocapsid protein or spike protein might interact with the proteins of the complement system, mainly complement regulatory proteins (CRPs). We demonstrate that the nucleocapsid protein, but not the spike protein, binds to multiple CRPs, including C1-inhibitor, C4-binding protein, factor H, and vitronectin. The nucleocapsid protein binds to both the recombinant spike protein and the SARS-CoV-2 virions. We further demonstrated that the virion-nucleocapsid-CRP complex could be formed. Recruitment of the CRPs on SARS-CoV-2 virion mediated by nucleocapsid protein deserves further investigation to reveal complement modulation strategies of SARS-CoV-2.
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Data generated in this study are available from the corresponding author upon reasonable request.
References
Liszewski, M. K. et al. Smallpox inhibitor of complement enzymes (SPICE): dissecting functional sites and abrogating activity. J. Immunol. 183, 3150–3159. https://doi.org/10.4049/jimmunol.0901366 (2009).
Jochum, S., Moosmann, A., Lang, S., Hammerschmidt, W. & Zeidler, R. The EBV Immunoevasins vIL-10 and BNLF2a protect newly infected B cells from immune recognition and elimination. PLoS Pathog. 8, e1002704. https://doi.org/10.1371/journal.ppat.1002704 (2012).
Schatz, M., Tong, P. B. V. & Beaumelle, B. Unconventional secretion of viral proteins. Semin Cell. Dev. Biol. 83, 8–11. https://doi.org/10.1016/j.semcdb.2018.03.008 (2018).
Abou-El-Hassan, H. & Zaraket, H. Viral-derived complement inhibitors: current status and potential role in Immunomodulation. Exp. Biol. Med. (Maywood). 242, 397–410. https://doi.org/10.1177/1535370216675772 (2017).
Dunkelberger, J. R. & Song, W. C. Complement and its role in innate and adaptive immune responses. Cell Res. 20, 34–50. https://doi.org/10.1038/cr.2009.139 (2010).
Zipfel, P. F. & Skerka, C. Complement regulators and inhibitory proteins. Nat. Rev. Immunol. 9, 729–740. https://doi.org/10.1038/nri2620 (2009).
Madar, M. et al. Exploitation of complement regulatory proteins by borrelia and Francisella. Mol. Biosyst. 11, 1684–1695. https://doi.org/10.1039/c5mb00027k (2015).
Moore, S. R., Menon, S. S., Cortes, C. & Ferreira, V. P. Hijacking factor H for complement immune evasion. Front. Immunol. 12 https://doi.org/10.3389/fimmu.2021.602277 (2021).
Potempa, M. et al. Binding of complement inhibitor C4b-binding protein contributes to serum resistance of Porphyromonas gingivalis. J. Immunol. 181, 5537–5544. https://doi.org/10.4049/jimmunol.181.8.5537 (2008).
Pellegrini, A. & Pietrocola, G. Recruitment of Vitronectin by Bacterial Pathogens: A Comprehensive Overview. Microorganisms 12 (2024). https://doi.org/10.3390/microorganisms12071385
Kotwal, G. J. & Moss, B. Vaccinia virus encodes a secretory polypeptide structurally related to complement control proteins. Nature 335, 176–178. https://doi.org/10.1038/335176a0 (1988).
Girgis, N. M. et al. The vaccinia virus complement control protein modulates adaptive immune responses during infection. J. Virol. 85, 2547–2556. https://doi.org/10.1128/jvi.01474-10 (2011).
Rastogi, M., Sharma, N. & Singh, S. K. Flavivirus NS1: a multifaceted enigmatic viral protein. Virol. J. 13, 131. https://doi.org/10.1186/s12985-016-0590-7 (2016).
Avirutnan, P. et al. Binding of flavivirus nonstructural protein NS1 to C4b binding protein modulates complement activation. J. Immunol. 187, 424–433. https://doi.org/10.4049/jimmunol.1100750 (2011).
Chung, K. M. et al. West Nile virus nonstructural protein NS1 inhibits complement activation by binding the regulatory protein factor H. Proceedings of the National Academy of Sciences 103, 19111–19116 (2006). https://doi.org/10.1073/pnas.0605668103
Conde, J. N. et al. Inhibition of the membrane attack complex by dengue virus NS1 through interaction with vitronectin and terminal complement proteins. J. Virol. 90, 9570–9581. https://doi.org/10.1128/jvi.00912-16 (2016).
Kumar, J., Dhyani, S., Kumar, P., Sharma, N. R. & Ganguly, S. SARS-CoV-2-encoded ORF8 protein possesses complement inhibitory properties. J. Biol. Chem. 299, 102930. https://doi.org/10.1016/j.jbc.2023.102930 (2023).
Pintér, C., Siccardi, A. G., Lopalco, L., Longhi, R. & Clivio, A. HIV glycoprotein 41 and complement factor H interact with each other and share functional as well as antigenic homology. AIDS Res. Hum. Retroviruses. 11, 971–980. https://doi.org/10.1089/aid.1995.11.971 (1995).
Johnson, J. B., Borisevich, V., Rockx, B. & Parks, G. D. A novel factor I activity in Nipah virus inhibits human complement pathways through cleavage of C3b. J. Virol. 89, 989–998. https://doi.org/10.1128/jvi.02427-14 (2015).
Nag, J. et al. A factor I-Like activity associated with Chikungunya virus contributes to its resistance to the human complement system. J. Virol. 94 https://doi.org/10.1128/jvi.02062-19 (2020).
Gebetsberger, L. et al. SARS-CoV-2 hijacks host CD55, CD59 and factor H to impair antibody-dependent complement-mediated Lysis. Emerg. Microbes Infect. 13, 2417868. https://doi.org/10.1080/22221751.2024.2417868 (2024).
Gao, T. et al. Highly pathogenic coronavirus N protein aggravates inflammation by MASP-2-mediated lectin complement pathway overactivation. Signal. Transduct. Target. Therapy. 7, 318. https://doi.org/10.1038/s41392-022-01133-5 (2022).
Kocsis, A. et al. SARS-CoV-2 nucleocapsid protein is not responsible for Over-Activation of complement lectin pathway. Int. J. Mol. Sci. 25 https://doi.org/10.3390/ijms25137343 (2024).
Bally, I. et al. Revisiting the interaction between complement lectin pathway protease MASP-2 and SARS-CoV-2 nucleoprotein. Front. Immunol. 15, 1419165. https://doi.org/10.3389/fimmu.2024.1419165 (2024).
Bai, Z., Cao, Y., Liu, W. & Li, J. The SARS-CoV-2 nucleocapsid protein and its role in viral Structure, biological Functions, and a potential target for drug or vaccine mitigation. Viruses 13 https://doi.org/10.3390/v13061115 (2021).
Huang, Y. et al. Molecular characterization of SARS-CoV-2 nucleocapsid protein. Front. Cell. Infect. Microbiol. 14 https://doi.org/10.3389/fcimb.2024.1415885 (2024).
Wick, K. D. et al. Plasma SARS-CoV-2 nucleocapsid antigen levels are associated with progression to severe disease in hospitalized COVID-19. Crit. Care. 26, 278. https://doi.org/10.1186/s13054-022-04153-3 (2022).
Zhang, Y. et al. Diagnostic value of nucleocapsid protein in blood for SARS-CoV-2 infection. Clin. Chem. 68, 240–248. https://doi.org/10.1093/clinchem/hvab148 (2021).
Bhatt, P., Sabeena, S. P., Varma, M. & Arunkumar, G. Current Understanding of the pathogenesis of dengue virus infection. Curr. Microbiol. 78, 17–32. https://doi.org/10.1007/s00284-020-02284-w (2021).
Rogers, A. J. et al. The association of baseline plasma SARS-CoV-2 nucleocapsid antigen level and outcomes in patients hospitalized with COVID-19. Ann. Intern. Med. 175, 1401–1410. https://doi.org/10.7326/m22-0924 (2022).
Wang, Y. C. et al. SARS-CoV-2 nucleocapsid protein, rather than Spike protein, triggers a cytokine storm originating from lung epithelial cells in patients with COVID-19. Infection 52, 955–983. https://doi.org/10.1007/s15010-023-02142-4 (2024).
López-Muñoz, A. D., Kosik, I., Holly, J. & Yewdell, J. W. Cell surface SARS-CoV-2 nucleocapsid protein modulates innate and adaptive immunity. Sci. Adv. 8, eabp9770. https://doi.org/10.1126/sciadv.abp9770 (2022).
Edalat, F. et al. Immunological mechanisms of the nucleocapsid protein in COVID-19. Sci. Rep. 14, 3711. https://doi.org/10.1038/s41598-024-53906-3 (2024).
Carvelli, J. et al. Association of COVID-19 inflammation with activation of the C5a-C5aR1 axis. Nature 588, 146–150. https://doi.org/10.1038/s41586-020-2600-6 (2020).
Devalaraja-Narashimha, K. et al. Association of complement pathways with COVID-19 severity and outcomes. Microbes Infect. 25, 105081. https://doi.org/10.1016/j.micinf.2022.105081 (2023).
Hawley, H. B. & Chang, J. C. Complement-Induced Endotheliopathy-Associated vascular microthrombosis in coronavirus disease 2019. J. Infect. Dis. 223, 2198–2199. https://doi.org/10.1093/infdis/jiab136 (2021).
Perico, L. et al. Immunity, endothelial injury and complement-induced coagulopathy in COVID-19. Nat. Rev. Nephrol. 17, 46–64. https://doi.org/10.1038/s41581-020-00357-4 (2021).
Agrawal, P., Nawadkar, R., Ojha, H., Kumar, J. & Sahu, A. Complement evasion strategies of viruses: an overview. Front. Microbiol. 8 https://doi.org/10.3389/fmicb.2017.01117 (2017).
Pintér, C., Siccardi, A. G., Longhi, R. & Clivio, A. Direct interaction of complement factor H with the C1 domain of HIV type 1 glycoprotein 120. AIDS Res. Hum. Retroviruses. 11, 577–588. https://doi.org/10.1089/aid.1995.11.577 (1995).
Blitvich, B. J., Mackenzie, J. S., Coelen, R. J., Howard, M. J. & Hall, R. A. A novel complex formed between the flavivirus E and NS1 proteins: analysis of its structure and function. Arch. Virol. 140, 145–156. https://doi.org/10.1007/bf01309729 (1995).
Park, B. K. et al. MERS-CoV and SARS-CoV-2 replication can be inhibited by targeting the interaction between the viral Spike protein and the nucleocapsid protein. Theranostics 11, 3853–3867. https://doi.org/10.7150/thno.55647 (2021).
Khani-Habibabadi, F. & O’Connor, K. C. In Reference Module in Neuroscience and Biobehavioral Psychology (Elsevier, 2024).
Díaz-Salinas, M. A., Jain, A., Durham, N. D. & Munro, J. B. Single-molecule imaging reveals allosteric stimulation of SARS-CoV-2 Spike receptor binding domain by host Sialic acid. Sci. Adv. 10, eadk4920. https://doi.org/10.1126/sciadv.adk4920 (2024).
Rosa, A. et al. SARS-CoV-2 can recruit a Heme metabolite to evade antibody immunity. Sci. Adv. 7 https://doi.org/10.1126/sciadv.abg7607 (2021).
Wang, Z. et al. Analysis of memory B cells identifies conserved neutralizing epitopes on the N-terminal domain of variant SARS-Cov-2 Spike proteins. Immunity 55, 998–1012e1018. https://doi.org/10.1016/j.immuni.2022.04.003 (2022).
Lan, J. et al. Structure of the SARS-CoV-2 Spike receptor-binding domain bound to the ACE2 receptor. Nature 581, 215–220. https://doi.org/10.1038/s41586-020-2180-5 (2020).
Beirag, N. et al. Complement Activation-Independent Attenuation of SARS-CoV-2 infection by C1q and C4b–Binding protein. Viruses 15, 1269. https://doi.org/10.3390/v15061269 (2023).
Thomson, T. M., Toscano-Guerra, E., Casis, E. & Paciucci, R. C1 esterase inhibitor and the contact system in COVID-19. Br. J. Haematol. 190, 520–524. https://doi.org/10.1111/bjh.16938 (2020).
Davis, A. E. 3, Mejia, P., Lu, F. & rd, & Biological activities of C1 inhibitor. Mol. Immunol. 45, 4057–4063. https://doi.org/10.1016/j.molimm.2008.06.028 (2008).
Werner, L. M. & Criss, A. K. Diverse functions of C4b-Binding protein in health and disease. J. Immunol. 211, 1443–1449. https://doi.org/10.4049/jimmunol.2300333 (2023).
Ferreira, V. P., Pangburn, M. K. & Cortés, C. Complement control protein factor H: the good, the bad, and the inadequate. Mol. Immunol. 47, 2187–2197. https://doi.org/10.1016/j.molimm.2010.05.007 (2010).
Yu, J. et al. Complement dysregulation is associated with severe COVID-19 illness. Haematologica 107, 1095–1105. https://doi.org/10.3324/haematol.2021.279155 (2022).
Sheehan, M., Morris, C. A., Pussell, B. A. & Charlesworth, J. A. Complement Inhibition by human vitronectin involves non-heparin binding domains. Clin. Exp. Immunol. 101, 136–141. https://doi.org/10.1111/j.1365-2249.1995.tb02289.x (1995).
Singh, B., Su, Y. C. & Riesbeck, K. Vitronectin in bacterial pathogenesis: a host protein used in complement escape and cellular invasion. Mol. Microbiol. 78, 545–560. https://doi.org/10.1111/j.1365-2958.2010.07373.x (2010).
Mertinková, P. et al. A simple and rapid pipeline for identification of receptor-binding sites on the surface proteins of pathogens. Sci. Rep. 10, 1163. https://doi.org/10.1038/s41598-020-58305-y (2020).
Wu, Y., Li, Q. & Chen, X. Z. Detecting protein–protein interactions by Far Western blotting. Nat. Protoc. 2, 3278–3284. https://doi.org/10.1038/nprot.2007.459 (2007).
Acknowledgements
We thank Ing. Martina Cepková and Ing. Viera Rusnáková for their technical assistance.
Funding
Research was funded by research projects VEGA 1/0381/23 and APVV-22-0084. A part of the work was also funded from the project awarded to Jakub Víglaský as a doctoral fellow (NextGenerationEU through the Recovery and Resilience Plan for Slovakia project No. 09I03-03-V05-00017).
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JV and MB designed an experimental plan. J.V. and M.B. prepared the manuscript. K.B. performed cell culture for virus amplification. L.T., K.B, J.V and M.B worked in BSL-3 laboratory to concentrate and titrate the virus for assays. LF produced and purified the recombinant Spike protein. All ELISA, Western blots, CRP purification and BLITZ assays were performed by JV. All authors checked manuscript.
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Work with SARS-CoV-2 was performed in BSL-3 biocontainment laboratory.
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Víglaský, J., Bhide, K., Talpasova, L. et al. SARS-CoV-2 nucleocapsid protein forms complexes with soluble complement regulatory proteins that can bind to the virion. Sci Rep (2026). https://doi.org/10.1038/s41598-026-37866-4
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DOI: https://doi.org/10.1038/s41598-026-37866-4


