Structural basis for recognition of the central conserved region of RSV G by neutralizing human antibodies

Jones, Harrison G.; Ritschel, Tina; Pascual, Gabriel; Brakenhoff, Just P. J.; Keogh, Elissa; Furmanova-Hollenstein, Polina; Lanckacker, Ellen; Wadia, Jehangir S.; Gilman, Morgan S. A.; Williamson, R. Anthony; Roymans, Dirk; van ‘t Wout, Angélique B.; Langedijk, Johannes P.; McLellan, Jason S.; Pierson, Ted C.

doi:10.1371/journal.ppat.1006935

Structural basis for recognition of the central conserved region of RSV G by neutralizing human antibodies

Journal Article · Tue Mar 06 00:00:00 EST 2018 · PLoS Pathogens

DOI:https://doi.org/10.1371/journal.ppat.1006935· OSTI ID:1484790

Jones, Harrison G. ^[1]; ^[2]; ^[3]; Brakenhoff, Just P. J. ^[2]; ^[3]; Furmanova-Hollenstein, Polina ^[2]; ^[4]; Wadia, Jehangir S. ^[5]; Gilman, Morgan S. A. ^[1]; ^[6]; Roymans, Dirk ^[4]; ^[7]; ^[2]; ^[1]; Pierson, Ted C. ^[8]

Univ. of Texas, Austin, TX (United States); Geisel School of Medicine at Dartmouth, Hanover, NH (United States)
Janssen Vaccines & Prevention, Leiden (The Netherlands)
Janssen Pharmaceutical Companies of Johnson and Johnson, San Diego, CA (United States)
Janssen Pharmaceutica NV, Beerse (Belgium)
Janssen R&D US, San Diego, CA (United States)
Janssen Pharmaceutical Companies of Johnson and Johnson, London (United Kingdom)
Janssen Vaccines & Prevention B.V., Leiden (The Netherlands)
National Inst. of Health (NIH), Bethesda, MD (United States)

Respiratory syncytial virus (RSV) is a major cause of severe lower respiratory tract infections in infants and the elderly, and yet there remains no effective treatment or vaccine. The surface of the virion is decorated with the fusion glycoprotein (RSV F) and the attachment glycoprotein (RSV G), which binds to CX3CR1 on human airway epithelial cells to mediate viral attachment and subsequent infection. RSV G is a major target of the humoral immune response, and antibodies that target the central conserved region of G have been shown to neutralize both subtypes of RSV and to protect against severe RSV disease in animal models. However, the molecular underpinnings for antibody recognition of this region have remained unknown. Therefore, we isolated two human antibodies directed against the central conserved region of RSV G and demonstrated that they neutralize RSV infection of human bronchial epithelial cell cultures in the absence of complement. Moreover, the antibodies protected cotton rats from severe RSV disease. Both antibodies bound with high affinity to a secreted form of RSV G as well as to a peptide corresponding to the unglycosylated central conserved region. High-resolution crystal structures of each antibody in complex with the G peptide revealed two distinct conformational epitopes that require proper folding of the cystine noose located in the C-terminal part of the central conserved region. Comparison of these structures with the structure of fractalkine (CX3CL1) alone or in complex with a viral homolog of CX3CR1 (US28) suggests that RSV G would bind to CX3CR1 in a mode that is distinct from that of fractalkine. Collectively, these results build on recent studies demonstrating the importance of RSV G in antibody-mediated protection from severe RSV disease, and the structural information presented here should guide the development of new vaccines and antibody-based therapies for RSV.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: NIH, Office of Research Infrastructure Programs; USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22). Scientific User Facilities Division

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1484790

Journal Information:: PLoS Pathogens, Journal Name: PLoS Pathogens Journal Issue: 3 Vol. 14; ISSN 1553-7374

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

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Respiratory syncytial virus reduces STAT3 phosphorylation in human memory CD8 T cells stimulated with IL-21 Antunes, Krist Helen; Becker, André; Franceschina, Caroline Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-54240-9	journal	November 2019
Effects of Alterations to the CX3C Motif and Secreted Form of Human Respiratory Syncytial Virus (RSV) G Protein on Immune Responses to a Parainfluenza Virus Vector Expressing the RSV G Protein Liang, Bo; Kabatova, Barbora; Kabat, Juraj Journal of Virology, Vol. 93, Issue 7 https://doi.org/10.1128/jvi.02043-18	journal	January 2019
Protective antigenic sites in respiratory syncytial virus G attachment protein outside the central conserved and cysteine noose domains Lee, Jeehyun; Klenow, Laura; Coyle, Elizabeth M. PLOS Pathogens, Vol. 14, Issue 8 https://doi.org/10.1371/journal.ppat.1007262	journal	August 2018
Role of Type I Interferon (IFN) in the Respiratory Syncytial Virus (RSV) Immune Response and Disease Severity Hijano, Diego R.; Vu, Luan D.; Kauvar, Lawrence M. Frontiers in Immunology, Vol. 10 https://doi.org/10.3389/fimmu.2019.00566	journal	March 2019

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59 BASIC BIOLOGICAL SCIENCES
antibodies
crystal structure
enzyme-linked immunoassays
epithelial cells
prophylaxis
respiratory infections
viral attachment
virus glycoproteins

Structural basis for recognition of the central conserved region of RSV G by neutralizing human antibodies

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