Phagocytic Cells Contribute to the Antibody-mediated Elimination of Pulmonary-infected SARS Coronavirus

Overview

Journal Virology

Specialty Microbiology

Date 2014 Apr 15

PMID 24725942

Citations 59

Authors

Fumihiko Yasui

Michinori Kohara

Masahiro Kitabatake

Tetsu Nishiwaki

Hideki Fujii

Chise Tateno

Misako Yoneda

Kouichi Morita

Kouji Matsushima

Shigeo Koyasu

Chieko Kai

Affiliations

Soon will be listed here.

Abstract

While the 2002-2003 outbreak of severe acute respiratory syndrome (SARS) resulted in 774 deaths, patients who were affected with mild pulmonary symptoms successfully recovered. The objective of the present work was to identify, using SARS coronavirus (SARS-CoV) mouse infection models, immune factors responsible for clearing of the virus. The elimination of pulmonary SARS-CoV infection required the activation of B cells by CD4(+) T cells. Furthermore, passive immunization (post-infection) with homologous (murine) anti-SARS-CoV antiserum showed greater elimination efficacy against SARS-CoV than that with heterologous (rabbit) antiserum, despite the use of equivalent titers of neutralizing antibodies. This distinction was mediated by mouse phagocytic cells (monocyte-derived infiltrating macrophages and partially alveolar macrophages, but not neutrophils), as demonstrated both by adoptive transfer from donors and by immunological depletion of selected cell types. These results indicate that the cooperation of anti-SARS-CoV antibodies and phagocytic cells plays an important role in the elimination of SARS-CoV.

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References

Huang K, Su I, Theron M, Wu Y, Lai S, Liu C . An interferon-gamma-related cytokine storm in SARS patients. J Med Virol. 2004; 75(2):185-94. PMC: 7166886. DOI: 10.1002/jmv.20255. View

Yang L, Peng H, Zhu Z, Li G, Huang Z, Zhao Z . Long-lived effector/central memory T-cell responses to severe acute respiratory syndrome coronavirus (SARS-CoV) S antigen in recovered SARS patients. Clin Immunol. 2006; 120(2):171-8. PMC: 7106132. DOI: 10.1016/j.clim.2006.05.002. View

Yang L, Peng H, Zhu Z, Li G, Huang Z, Zhao Z . Persistent memory CD4+ and CD8+ T-cell responses in recovered severe acute respiratory syndrome (SARS) patients to SARS coronavirus M antigen. J Gen Virol. 2007; 88(Pt 10):2740-2748. PMC: 2362397. DOI: 10.1099/vir.0.82839-0. View

Li C, Wu H, Yan H, Ma S, Wang L, Zhang M . T cell responses to whole SARS coronavirus in humans. J Immunol. 2008; 181(8):5490-500. PMC: 2683413. DOI: 10.4049/jimmunol.181.8.5490. View

Stockman L, Massoudi M, Helfand R, Erdman D, Siwek A, Anderson L . Severe acute respiratory syndrome in children. Pediatr Infect Dis J. 2007; 26(1):68-74. DOI: 10.1097/01.inf.0000247136.28950.41. View

Chen J, Lau Y, Lamirande E, Paddock C, Bartlett J, Zaki S . Cellular immune responses to severe acute respiratory syndrome coronavirus (SARS-CoV) infection in senescent BALB/c mice: CD4+ T cells are important in control of SARS-CoV infection. J Virol. 2009; 84(3):1289-301. PMC: 2812346. DOI: 10.1128/JVI.01281-09. View

Yang Z, Kong W, Huang Y, Roberts A, Murphy B, Subbarao K . A DNA vaccine induces SARS coronavirus neutralization and protective immunity in mice. Nature. 2004; 428(6982):561-4. PMC: 7095382. DOI: 10.1038/nature02463. View

Huber V, Lynch J, Bucher D, Le J, Metzger D . Fc receptor-mediated phagocytosis makes a significant contribution to clearance of influenza virus infections. J Immunol. 2001; 166(12):7381-8. DOI: 10.4049/jimmunol.166.12.7381. View

Zhao J, Zhao J, Perlman S . T cell responses are required for protection from clinical disease and for virus clearance in severe acute respiratory syndrome coronavirus-infected mice. J Virol. 2010; 84(18):9318-25. PMC: 2937604. DOI: 10.1128/JVI.01049-10. View

10.

Cameron M, Ran L, Xu L, Danesh A, Bermejo-Martin J, Cameron C . Interferon-mediated immunopathological events are associated with atypical innate and adaptive immune responses in patients with severe acute respiratory syndrome. J Virol. 2007; 81(16):8692-706. PMC: 1951379. DOI: 10.1128/JVI.00527-07. View

11.

Varol C, Yona S, Jung S . Origins and tissue-context-dependent fates of blood monocytes. Immunol Cell Biol. 2008; 87(1):30-8. DOI: 10.1038/icb.2008.90. View

12.

Iijima N, Mattei L, Iwasaki A . Recruited inflammatory monocytes stimulate antiviral Th1 immunity in infected tissue. Proc Natl Acad Sci U S A. 2010; 108(1):284-9. PMC: 3017177. DOI: 10.1073/pnas.1005201108. View

13.

Christensen J, Cardin R, Branum K, Doherty P . CD4(+) T cell-mediated control of a gamma-herpesvirus in B cell-deficient mice is mediated by IFN-gamma. Proc Natl Acad Sci U S A. 1999; 96(9):5135-40. PMC: 21829. DOI: 10.1073/pnas.96.9.5135. View

14.

Kam Y, Kien F, Roberts A, Cheung Y, Lamirande E, Vogel L . Antibodies against trimeric S glycoprotein protect hamsters against SARS-CoV challenge despite their capacity to mediate FcgammaRII-dependent entry into B cells in vitro. Vaccine. 2006; 25(4):729-40. PMC: 7115629. DOI: 10.1016/j.vaccine.2006.08.011. View

15.

Pribul P, Harker J, Wang B, Wang H, Tregoning J, Schwarze J . Alveolar macrophages are a major determinant of early responses to viral lung infection but do not influence subsequent disease development. J Virol. 2008; 82(9):4441-8. PMC: 2293049. DOI: 10.1128/JVI.02541-07. View

16.

Rockx B, Donaldson E, Frieman M, Sheahan T, Corti D, Lanzavecchia A . Escape from human monoclonal antibody neutralization affects in vitro and in vivo fitness of severe acute respiratory syndrome coronavirus. J Infect Dis. 2010; 201(6):946-55. PMC: 2826557. DOI: 10.1086/651022. View

17.

Lee N, Hui D, Wu A, Chan P, Cameron P, Joynt G . A major outbreak of severe acute respiratory syndrome in Hong Kong. N Engl J Med. 2003; 348(20):1986-94. DOI: 10.1056/NEJMoa030685. View

18.

Peiris J, Chu C, Cheng V, Chan K, Hung I, Poon L . Clinical progression and viral load in a community outbreak of coronavirus-associated SARS pneumonia: a prospective study. Lancet. 2003; 361(9371):1767-72. PMC: 7112410. DOI: 10.1016/s0140-6736(03)13412-5. View

19.

Fan Y, Huang Z, Li L, Wu M, Yu T, Koup R . Characterization of SARS-CoV-specific memory T cells from recovered individuals 4 years after infection. Arch Virol. 2009; 154(7):1093-9. PMC: 2796960. DOI: 10.1007/s00705-009-0409-6. View

20.

Appay V, Zaunders J, Papagno L, Sutton J, Jaramillo A, Waters A . Characterization of CD4(+) CTLs ex vivo. J Immunol. 2002; 168(11):5954-8. DOI: 10.4049/jimmunol.168.11.5954. View