Atomic structures of enterovirus D68 in complex with two monoclonal antibodies define distinct mechanisms of viral neutralization

Nature Microbiology

Volumn 4, Issue 1, 2019, Pages 124-133

  Zheng, Qingbing ^a   Zhu, Rui ^a   Xu, Longfa ^a   He, Maozhou ^a   Yan, Xiaodong ^a,b   Liu, Dongxiao ^a   Yin, Zhichao ^a   Wu, Yangtao ^a   Li, Yongchao ^a   Yang, Lisheng ^a   Hou, Wangheng ^a   Li, Shuxuan ^a   Li, Zizhen ^a   Chen, Zhenqin ^a   Li, Zhihai ^a   Yu, Hai ^a   Gu, Ying ^a   Zhang, Jun ^a   Baker, Timothy S ^b   Zhou, Z Hong ^c   Graham, Barney S ^d   Cheng, Tong ^a   Li, Shaowei ^a   Xia, Ningshao ^a   more..

^a XIAMEN UNIVERSITY   (China)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

11G1 ANTIBODY; 15C5 ANTIBODY; GLYCOPROTEIN; INTERCELLULAR ADHESION MOLECULE 5; MONOCLONAL ANTIBODY; UNCLASSIFIED DRUG; CELL ADHESION MOLECULE; ICAM5 PROTEIN, HUMAN; NERVE PROTEIN; NEUTRALIZING ANTIBODY;

ANTIBODY STRUCTURE; ANTIGEN ANTIBODY COMPLEX; ANTIGEN BINDING; ANTIGEN RECOGNITION; ARTICLE; ENTEROVIRUS D68; NONHUMAN; PRIORITY JOURNAL; VIRION; VIRUS ATTACHMENT; VIRUS CAPSID; VIRUS MORPHOLOGY; VIRUS NEUTRALIZATION; VIRUS PARTICLE; ANIMAL; BAGG ALBINO MOUSE; CRYOELECTRON MICROSCOPY; ENTEROVIRUS; HUMAN; IMMUNOLOGY; METABOLISM; MOUSE; TUMOR CELL LINE; ULTRASTRUCTURE;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; ANTIGEN-ANTIBODY COMPLEX; CAPSID; CELL ADHESION MOLECULES; CELL LINE, TUMOR; CRYOELECTRON MICROSCOPY; ENTEROVIRUS; HUMANS; MICE; MICE, INBRED BALB C; NERVE TISSUE PROTEINS;

EID: 85056206688     PISSN: None     EISSN: 20585276     Source Type: Journal    
DOI: 10.1038/s41564-018-0275-7     Document Type: Article

References (50)

1. Schieble, J. H., Fox, V. L. & Lennette, E. H. A probable new human picornavirus associated with respiratory diseases. Am. J. Epidemiol. 85, 297–310 (1967)
2. Ikeda, T. et al. Acute respiratory infections due to enterovirus 68 in Yamagata, Japan between 2005 and 2010. Microbiol. Immunol. 56, 139–143 (2012)
3. Kaida, A. et al. Distinct genetic clades of enterovirus D68 detected in 2010, 2013, and 2015 in Osaka City, Japan. PLoS ONE 12, e0184335 (2017)
4. Knoester, M. et al. Upsurge of enterovirus D68, the Netherlands, 2016. Emerg. Infect. Dis. 23, 140–143 (2017)
5. Midgley, C. M. et al. Severe respiratory illness associated with enterovirus D68 - Missouri and Illinois, 2014. MMWR. Morb. Mortal. Wkly Rep. 63, 798–799 (2014)
6. Holm-Hansen, C. C., Midgley, S. E. & Fischer, T. K. Global emergence of enterovirus D68: a systematic review. Lancet Infect. Dis. 16, e64–e75 (2016)
7. Messacar, K. et al. A cluster of acute flaccid paralysis and cranial nerve dysfunction temporally associated with an outbreak of enterovirus D68 in children in Colorado, USA. Lancet 385, 1662–1671 (2015)
8. Imamura, T. & Oshitani, H. Global reemergence of enterovirus D68 as an important pathogen for acute respiratory infections. Rev. Med. Virol. 25, 102–114 (2015)
9. Liu, Y. et al. Structure and inhibition of EV-D68, a virus that causes respiratory illness in children. Science 347, 71–74 (2015)
10. Liu, Y. et al. Sialic acid-dependent cell entry of human enterovirus D68. Nat. Commun. 6, 8865 (2015)
11. Hogle, J. M., Chow, M. & Filman, D. J. Three-dimensional structure of poliovirus at 2.9 A resolution. Science 229, 1358–1365 (1985)
12. Rossmann, M. G. et al. Structure of a human common cold virus and functional relationship to other picornaviruses. Nature 317, 145–153 (1985)
13. Wang, X. et al. A sensor–adaptor mechanism for enterovirus uncoating from structures of EV71. Nat. Struct. Mol. Biol. 19, 424–429 (2012)
14. Plevka, P., Perera, R., Cardosa, J., Kuhn, R. J. & Rossmann, M. G. Crystal structure of human enterovirus 71. Science 336, 1274 (2012)
15. Ren, J. et al. Picornavirus uncoating intermediate captured in atomic detail. Nat. Commun. 4, 1929 (2013)
16. Shingler, K. L. et al. The enterovirus 71 A-particle forms a gateway to allow genome release: a cryoEM study of picornavirus uncoating. PLoS Pathog. 9, e1003240 (2013)
17. Xu, L. et al. Atomic structures of Coxsackievirus A6 and its complex with a neutralizing antibody. Nat. Commun. 8, 505 (2017)
18. Wei, W. et al. ICAM-5/Telencephalin is a functional entry receptor for enterovirus D68. Cell Host Microbe 20, 631–641 (2016)
19. Zhang, Y. X. et al. A highly conserved amino acid in VP1 regulates maturation of enterovirus 71. PLoS Pathog. 13, e1006625 (2017)
20. Chong, P. et al. Immunological and biochemical characterization of coxsackie virus A16 viral particles. PLoS ONE 7, e49973 (2012)
21. Plevka, P. et al. Neutralizing antibodies can initiate genome release from human enterovirus 71. Proc. Natl Acad. Sci. USA 111, 2134–2139 (2014)
22. Dong, Y. et al. Antibody-induced uncoating of human rhinovirus B14. Proc. Natl Acad. Sci. USA 114, 8017–8022 (2017)
23. Lee, H. et al. The novel asymmetric entry intermediate of a picornavirus captured with nanodiscs. Sci. Adv. 2, e1501929 (2016)
24. Ye, X. et al. Structural basis for recognition of human enterovirus 71 by a bivalent broadly neutralizing monoclonal antibody. PLoS Pathog. 12, e1005454 (2016)
25. Scheres, S. H. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519–530 (2012)
26. Bergelson, J. M. & Coyne, C. B. Picornavirus entry. Adv. Exp. Med. Biol. 790, 24–41 (2013)
27. Johnson, J. E. & Vogt, P. K. Cell entry by non-enveloped viruses. Curr. Top. Microbiol. Immunol. 343, v–vii (2010)
28. Curry, S., Chow, M. & Hogle, J. M. The poliovirus 135S particle is infectious. J. Virol. 70, 7125–7131 (1996)
29. Kaplan, G., Freistadt, M. S. & Racaniello, V. R. Neutralization of poliovirus by cell receptors expressed in insect cells. J. Virol. 64, 4697–4702 (1990)
30. Tsang, S. K., McDermott, B. M., Racaniello, V. R. & Hogle, J. M. Kinetic analysis of the effect of poliovirus receptor on viral uncoating: the receptor as a catalyst. J. Virol. 75, 4984–4989 (2001)
31. Baggen, J., Thibaut, H. J., Strating, J. & van Kuppeveld, F. J. M. The life cycle of non-polio enteroviruses and how to target it. Nat. Rev. Microbiol. 16, 368–381 (2018)
32. Bubeck, D., Filman, D. J. & Hogle, J. M. Cryo-electron microscopy reconstruction of a poliovirus-receptor-membrane complex. Nat. Struct. Mol. Biol. 12, 615–618 (2005)
33. Bergelson, J. M. et al. Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 275, 1320–1323 (1997)
34. Belnap, D. M. et al. Three-dimensional structure of poliovirus receptor bound to poliovirus. Proc. Natl Acad. Sci. USA 97, 73–78 (2000)
35. Levy, H. C., Bostina, M., Filman, D. J. & Hogle, J. M. Catching a virus in the act of RNA release: a novel poliovirus uncoating intermediate characterized by cryo-electron microscopy. J. Virol. 84, 4426–4441 (2010)
36. Organtini, L. J., Makhov, A. M., Conway, J. F., Hafenstein, S. & Carson, S. D. Kinetic and structural analysis of coxsackievirus B3 receptor interactions and formation of the A-particle. J. Virol. 88, 5755–5765 (2014)
37. Walter, T. S. et al. A plate-based high-throughput assay for virus stability and vaccine formulation. J. Virol. Methods 185, 166–170 (2012)
38. −ΔΔCT method. Methods 25, 402–408 (2001)
39. Zheng, S. Q. et al. MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat. Methods 14, 331–332 (2017)
40. Zhang, K. Gctf: Real-time CTF determination and correction. J. Struct. Biol. 193, 1–12 (2016)
41. Yan, X., Sinkovits, R. S. & Baker, T. S. AUTO3DEM–an automated and high throughput program for image reconstruction of icosahedral particles. J. Struct. Biol. 157, 73–82 (2007)
42. Scheres, S. H. & Chen, S. Prevention of overfitting in cryo-EM structure determination. Nat. Methods 9, 853–854 (2012)
43. Swint-Kruse, L. & Brown, C. S. Resmap: automated representation of macromolecular interfaces as two-dimensional networks. Bioinformatics 21, 3327–3328 (2005)
44. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486–501 (2010)
45. Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213–221 (2010)
46. Chen, V. B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D 66, 12–21 (2010)
47. Gouet, P., Robert, X. & Courcelle, E. ESPript/ENDscript: extracting and rendering sequence and 3D information from atomic structures of proteins. Nucleic Acids Res. 31, 3320–3323 (2003)
48. Pettersen, E. F. et al. UCSF Chimera–a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004)
49. Xiao, C. & Rossmann, M. G. Interpretation of electron density with stereographic roadmap projections. J. Struct. Biol. 158, 182–187 (2007)
50. Collaborative Computational Project, Number 4. TheCCP4 suite: programs for protein crystallography. Acta Crystallogr. D 50, 760–763 (1994)