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Coronaviruses

SARS-CoV-2 hijacks neutralizing dimeric IgA for nasal infection and injury in Syrian hamsters1

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Article: 2245921 | Received 24 Apr 2023, Accepted 03 Aug 2023, Published online: 21 Aug 2023

References

  • Zhu N, Zhang D, Wang W, et al. A novel coronavirus from patients with pneumonia in China, 2019. N Engl J Med. 2020 Jan 24;382:727–733.
  • Zhou P, Yang XL, Wang XG, et al. A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature. 2020 Feb 3;579:270–273.
  • Wang Q, Zhang Y, Wu L, et al. Structural and functional basis of SARS-CoV-2 entry by using human ACE2. Cell. 2020 May 14;181(4):894–904e9.
  • Wu F, Zhao S, Yu B, et al. A new coronavirus associated with human respiratory disease in China. Nature. 2020 Mar;579(7798):265–269.
  • Hu B, Guo H, Zhou P, et al. Characteristics of SARS-CoV-2 and COVID-19. Nat Rev Microbiol. 2021 Mar;19(3):141–154.
  • WHO. Weekly epidemiological update on COVID-19 – 27 July 2021, https://www.who.int/publications/m/item/weekly-epidemiological-update-on-covid-19 – 27-july-2021 (2021).
  • Cheng VC, Lau SK, Woo PC, et al. Severe acute respiratory syndrome coronavirus as an agent of emerging and reemerging infection. Clin Microbiol Rev. 2007 Oct;20(4):660–694.
  • Chan JF, Yuan S, Kok KH, et al. A familial cluster of pneumonia associated with the 2019 novel coronavirus indicating person-to-person transmission: a study of a family cluster. Lancet. 2020 Jan 24;395(10223):514–523.
  • Hoffmann M, Kleine-Weber H, Schroeder S, et al. SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and Is blocked by a clinically proven protease inhibitor. Cell. 2020 Apr;181(2):271–280e8.
  • Lan J, Ge J, Yu J, et al. Structure of the SARS-CoV-2 spike receptor-binding domain bound to the ACE2 receptor. Nature. 2020 May;581(7807):215–220.
  • Wong YC, Lau SY, To W, et al. Natural transmission of bat-like SARS-CoV-2PRRA variants in COVID-19 patients. Clin Infect Dis. 2020 Jul;73:e437–e444.
  • Gobeil SM, Janowska K, McDowell S, et al. D614g mutation alters SARS-CoV-2 spike conformation and enhances protease cleavage at the S1/S2 junction. Cell Rep. 2021 Jan 12;34(2):108630.
  • Plante JA, Liu Y, Liu J, et al. Spike mutation D614G alters SARS-CoV-2 fitness. Nature. 2020 Oct 26;592:116–121.
  • Peng Q, Zhou R, Liu N, et al. Naturally occurring spike mutations influence the infectivity and immunogenicity of SARS-CoV-2. Cell Mol Immunol. 2022 Nov;19(11):1302–1310.
  • Wang Q, Iketani S, Li Z, et al. Antigenic characterization of the SARS-CoV-2 omicron subvariant BA.2.75. Cell Host Microbe. 2022 Nov 9;30(11):1512–1517e4.
  • Chan JF, Yip CC, To KK, et al. Improved molecular diagnosis of COVID-19 by the novel, highly sensitive and specific COVID-19-RdRp/Hel real-time reverse transcription-PCR assay validated in vitro and with clinical specimens. J Clin Microbiol. 2020 Apr 23;58(5):e00310–20.
  • Chu H, Chan JF-W, Yuen TT-T, et al. Comparative tropism, replication kinetics, and cell damage profiling of SARS-CoV-2 and SARS-CoV with implications for clinical manifestations, transmissibility, and laboratory studies of COVID-19: an observational study. The Lancet Microbe. 2020;1(1):e14–e23.
  • Zhou D, Zhou R, Chen Z. Human neutralizing antibodies for SARS-CoV-2 prevention and immunotherapy. Immunother Adv. 2022;2(1):1–9.
  • Pilette C, Ouadrhiri Y, Godding V, et al. Lung mucosal immunity: immunoglobulin – a revisited. Eur Respir J. 2001 Sep;18(3):571–588.
  • Corthesy B. Multi-faceted functions of secretory IgA at mucosal surfaces. Front Immunol. 2013;4:185.
  • Ejemel M, Li Q, Hou S, et al. A cross-reactive human IgA monoclonal antibody blocks SARS-CoV-2 spike-ACE2 interaction. Nat Commun. 2020 Aug 21;11(1):4198.
  • Sterlin D, Mathian A, Miyara M, et al. IgA dominates the early neutralizing antibody response to SARS-CoV-2. Sci Transl Med. 2021 Jan 20;13(577):eabd2223.
  • Dos Santos JMB, Soares CP, Monteiro FR, et al. In nasal mucosal secretions, distinct IFN and IgA responses Are found in severe and mild SARS-CoV-2 infection. Front Immunol. 2021;12:595343.
  • Smith N, Goncalves P, Charbit B, et al. Distinct systemic and mucosal immune responses during acute SARS-CoV-2 infection. Nat Immunol. 2021 Sep 1;22:1428–1439.
  • Wang Z, Lorenzi JCC, Muecksch F, et al. Enhanced SARS-CoV-2 neutralization by dimeric IgA. Sci Transl Med. 2021 Jan 20;13(577):eabf1555.
  • Zhou D, Chan JF, Zhou B, et al. Robust SARS-CoV-2 infection in nasal turbinates after treatment with systemic neutralizing antibodies. Cell Host Microbe. 2021 Feb 25;29:551–563.
  • Chan JF-W, Zhang AJ, Yuan S, et al. Simulation of the clinical and pathological manifestations of coronavirus disease 2019 (COVID-19) in golden Syrian hamster model: implications for disease pathogenesis and transmissibility. Clin Infect Dis. 2020;71:2428–2446.
  • Liu L, Wei Q, Lin Q, et al. Anti-spike IgG causes severe acute lung injury by skewing macrophage responses during acute SARS-CoV infection. JCI Insight. 2019 Feb 21;4(4):e123158.
  • Kong L, Ju B, Chen Y, et al. Key gp120 glycans pose roadblocks to the rapid development of VRC01-class antibodies in an HIV-1-infected Chinese donor. Immunity. 2016 Apr 19;44(4):939–950.
  • Smith K, Garman L, Wrammert J, et al. Rapid generation of fully human monoclonal antibodies specific to a vaccinating antigen. Nat Protoc. 2009;4(3):372–384.
  • Poeran J, Zhong H, Wilson L, et al. Cancellation of elective surgery and intensive care unit capacity in New York state: a retrospective cohort analysis. Anesth Analg. 2020 Jun 23;131:1337–1341.
  • Robinot R, Hubert M, de Melo GD, et al. SARS-CoV-2 infection induces the dedifferentiation of multiciliated cells and impairs mucociliary clearance. Nat Commun. 2021 Jul 16;12(1):4354.
  • Ahn JH, Kim J, Hong SP, et al. Nasal ciliated cells are primary targets for SARS-CoV-2 replication in the early stage of COVID-19. J Clin Invest. 2021 Jul 1;131(13):e148517.
  • Yeung ML, Teng JLL, Jia L, et al. Soluble ACE2-mediated cell entry of SARS-CoV-2 via interaction with proteins related to the renin-angiotensin system. Cell. 2021 Apr 15;184(8):2212–2228e12.
  • Korsunsky I, Millard N, Fan J, et al. Fast, sensitive and accurate integration of single-cell data with harmony. Nat Methods. 2019 Dec;16(12):1289–1296.
  • Arvin AM, Fink K, Schmid MA, et al. A perspective on potential antibody-dependent enhancement of SARS-CoV-2. Nature. 2020 Aug;584(7821):353–363.
  • Liu L, Wei Q, Nishiura K, et al. Spatiotemporal interplay of severe acute respiratory syndrome coronavirus and respiratory mucosal cells drives viral dissemination in rhesus macaques. Mucosal Immunol. 2016 Jul;9(4):1089–1101.
  • Baumann J, Park CG, Mantis NJ. Recognition of secretory IgA by DC-SIGN: implications for immune surveillance in the intestine. Immunol Lett. 2010 Jun 15;131(1):59–66.
  • Junqueira C, Crespo A, Ranjbar S, et al. FcgammaR-mediated SARS-CoV-2 infection of monocytes activates inflammation. Nature. 2022 Apr 6;606:576–584.
  • Yang D, Chu H, Hou Y, et al. Attenuated interferon and proinflammatory response in SARS-CoV-2-infected human dendritic cells Is associated With viral antagonism of STAT1 phosphorylation. J Infect Dis. 2020 Aug 4;222(5):734–745.
  • Thepaut M, Luczkowiak J, Vives C, et al. DC/L-SIGN recognition of spike glycoprotein promotes SARS-CoV-2 trans-infection and can be inhibited by a glycomimetic antagonist. PLoS Pathog. 2021 May;17(5):e1009576.
  • Wang R, Zhang Q, Ge J, et al. Analysis of SARS-CoV-2 variant mutations reveals neutralization escape mechanisms and the ability to use ACE2 receptors from additional species. Immunity. 2021 Jul 13;54(7):1611–1621e5.
  • Watkins JD, Sholukh AM, Mukhtar MM, et al. Anti-HIV IgA isotypes: differential virion capture and inhibition of transcytosis are linked to prevention of mucosal R5 SHIV transmission. AIDS. 2013 Jun 1;27(9):F13–F20.
  • Merrill WW, Goodenberger D, Strober W, et al. Free secretory component and other proteins in human lung lavage. Am Rev Respir Dis. 1980 Jul;122(1):156–161.
  • Taylor RA, Xiao S, Carias AM, et al. PET/CT targeted tissue sampling reveals virus specific dIgA can alter the distribution and localization of HIV after rectal exposure. PLoS Pathog. 2021 Jun;17(6):e1009632.
  • Beltramello M, Williams KL, Simmons CP, et al. The human immune response to dengue virus Is dominated by highly cross-reactive antibodies endowed with neutralizing and enhancing activity. Cell Host Microbe. 2010 Sep 16;8(3):271–283.
  • Bournazos S, Vo HTM, Duong V, et al. Antibody fucosylation predicts disease severity in secondary dengue infection. Science. 2021 Jun 4;372(6546):1102–1105.
  • van Erp EA, Luytjes W, Ferwerda G, et al. Fc-Mediated antibody effector functions during respiratory syncytial virus infection and disease. Front Immunol. 2019;10:548.
  • Cao Y, Su B, Guo X, et al. Potent neutralizing antibodies against SARS-CoV-2 identified by high-throughput single-cell sequencing of convalescent patients’ B cells. Cell. 2020 Jul 9;182(1):73–84e16.
  • Haynes BF, Corey L, Fernandes P, et al. Prospects for a safe COVID-19 vaccine. Sci Transl Med. 2020 Nov 4;12:eabe0948.
  • Larsen MD, de Graaf EL, Sonneveld ME, et al. Afucosylated IgG characterizes enveloped viral responses and correlates with COVID-19 severity. Science. 2021 Feb 26;371:eabc8378.
  • Baum A, Ajithdoss D, Copin R, et al. REGN-COV2 antibodies prevent and treat SARS-CoV-2 infection in rhesus macaques and hamsters. Science. 2020 Nov 27;370(6520):1110–1115.
  • Liu Y, Soh WT, Kishikawa JI, et al. An infectivity-enhancing site on the SARS-CoV-2 spike protein targeted by antibodies. Cell. 2021 Jun 24;184(13):3452–3466e18.
  • Soh WT, Liu Y, Nakayama EE, et al. The N-terminal domain of spike glycoprotein mediates SARS-CoV-2 infection by associating with L-SIGN and DC-SIGN. bioRxiv. 2020.11.05.369264.
  • Geijtenbeek TBH, Kwon DS, Torensma R, et al. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell. 2000 Mar 3;100(5):587–597.
  • Bracq L, Xie M, Benichou S, et al. Mechanisms for cell-to-cell transmission of HIV-1. Front Immunol. 2018;9:260.
  • Hartmann E, Graefe H, Hopert A, et al. Analysis of plasmacytoid and myeloid dendritic cells in nasal epithelium. Clin Vaccine Immunol. 2006 Nov;13(11):1278–1286.
  • Hui KPY, Ho JCW, Cheung MC, et al. SARS-CoV-2 omicron variant replication in human bronchus and lung ex vivo. Nature. 2022 Mar;603(7902):715–720.
  • Krammer F. SARS-CoV-2 vaccines in development. Nature. 2020 Oct;586(7830):516–527.
  • Wang Q, Iketani S, Li Z, et al. Alarming antibody evasion properties of rising SARS-CoV-2 BQ and XBB subvariants. Cell. 2023 Jan 19;186(2):279–286e8.