Trypsin treatment unlocks barrier for zoonotic bat coronavirus infection

Journal of Virology

Volumn 94, Issue 5, 2020, Pages

  Menachery, Vineet D ^a,b   Dinnon, Kenneth H ^b,c   Yount, Boyd L ^b   McAnarney, Eileen T ^a,b   Gralinski, Lisa E ^b   Hale, Andrew ^c   Graham, Rachel L ^b   Scobey, Trevor ^b   Anthony, Simon J ^d   Wang, Lingshu ^e   Graham, Barney ^e   Randell, Scott H ^c   Lipkin, W Ian ^d   Baric, Ralph S ^b,c  

^a University of Texas Medical Branch School of Medicine   (United States)

^b IL   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d Columbia University ^*  (United States)

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

Author keywords

Coronavirus; Emergence; MERS CoV; PDF2180; Spike; Zoonotic

Indexed keywords

TRYPSIN; VIRUS SPIKE PROTEIN;

ARTICLE; BAT; CONTROLLED STUDY; CORRELATIONAL STUDY; HUMAN; HUMAN CELL; LUNG ALVEOLUS CELL; MIDDLE EAST RESPIRATORY SYNDROME; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN DOMAIN; RECEPTOR BINDING; VERO CELL LINE;

EID: 85079471604     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01774-19     Document Type: Article

References (59)

1. Reperant LA, Osterhaus A. 2017. AIDS, avian flu, SARS, MERS, Ebola, Zika . . . what next? Vaccine 35:4470 – 4474. https://doi.org/10.1016/j.vaccine.2017.04.082.
2. Perlman S, Netland J. 2009. Coronaviruses post-SARS: update on replication and pathogenesis. Nat Rev Microbiol 7:439–450. https://doi.org/10.1038/nrmicro2147.
3. Morse SS, Mazet JA, Woolhouse M, Parrish CR, Carroll D, Karesh WB, Zambrana-Torrelio C, Lipkin WI, Daszak P. 2012. Prediction and prevention of the next pandemic zoonosis. Lancet 380:1956–1965. https://doi.org/10.1016/S0140-6736(12)61684-5.
4. Cunningham AA, Daszak P, Wood JLN. 2017. One Health, emerging infectious diseases and wildlife: two decades of progress? Philos Trans R Soc Lond B Biol Sci 372:20160167. https://doi.org/10.1098/rstb.2016.0167.
5. Chafekar A, Fielding BC. 2018. MERS-CoV: understanding the latest human coronavirus threat. Viruses 10:E93. https://doi.org/10.3390/ v10020093.
6. Agnihothram S, Yount BL, Jr., Donaldson EF, Huynh J, Menachery VD, Gralinski LE, Graham RL, Becker MM, Tomar S, Scobey TD, Osswald HL, Whitmore A, Gopal R, Ghosh AK, Mesecar A, Zambon M, Heise M, Denison MR, Baric RS. 2014. A mouse model for Betacoronavirus subgroup 2c using a bat coronavirus strain HKU5 variant. mBio 5:e00047-14. https://doi.org/10.1128/mBio.00047-14.
7. Agnihothram S, Gopal R, Yount BL, Jr., Donaldson EF, Menachery VD, Graham RL, Scobey TD, Gralinski LE, Denison MR, Zambon M, Baric RS. 2014. Evaluation of serologic and antigenic relationships between middle eastern respiratory syndrome coronavirus and other coronaviruses to develop vaccine platforms for the rapid response to emerging coronaviruses. J Infect Dis 209:995–1006. https://doi.org/10.1093/infdis/ jit609.
8. Johnson BA, Graham RL, Menachery VD. 2018. Viral metagenomics, protein structure, and reverse genetics: key strategies for investigating coronaviruses. Virology 517:30–37. https://doi.org/10.1016/j.virol.2017.12.009.
9. Becker MM, Graham RL, Donaldson EF, Rockx B, Sims AC, Sheahan T, Pickles RJ, Corti D, Johnston RE, Baric RS, Denison MR. 2008. Synthetic recombinant bat SARS-like coronavirus is infectious in cultured cells and in mice. Proc Natl Acad Sci U S A 105:19944–19949. https://doi.org/10.1073/pnas.0808116105.
10. Rockx B, Baas T, Zornetzer GA, Haagmans B, Sheahan T, Frieman M, Dyer MD, Teal TH, Proll S, van den Brand J, Baric R, Katze MG. 2009. Early upregulation of acute respiratory distress syndrome-associated cytokines promotes lethal disease in an aged-mouse model of severe acute respiratory syndrome coronavirus infection. J Virol 83:7062–7074. https://doi.org/10.1128/JVI.00127-09.
11. Sheahan T, Rockx B, Donaldson E, Sims A, Pickles R, Corti D, Baric R. 2008. Mechanisms of zoonotic severe acute respiratory syndrome coronavirus host range expansion in human airway epithelium. J Virol 82:2274 –2285. https://doi.org/10.1128/JVI.02041-07.
12. Sheahan T, Rockx B, Donaldson E, Corti D, Baric R. 2008. Pathways of cross-species transmission of synthetically reconstructed zoonotic severe acute respiratory syndrome coronavirus. J Virol 82:8721–8732. https://doi.org/10.1128/JVI.00818-08.
13. Menachery VD, Yount BL, Jr., Sims AC, Debbink K, Agnihothram SS, Gralinski LE, Graham RL, Scobey T, Plante JA, Royal SR, Swanstrom J, Sheahan TP, Pickles RJ, Corti D, Randell SH, Lanzavecchia A, Marasco WA, Baric RS. 2016. SARS-like WIV1-CoV poised for human emergence. Proc Natl Acad Sci U S A 113:3048 –3053. https://doi.org/10.1073/pnas .1517719113.
14. Menachery VD, Yount BL, Jr., Debbink K, Agnihothram S, Gralinski LE, Plante JA, Graham RL, Scobey T, Ge XY, Donaldson EF, Randell SH, Lanzavecchia A, Marasco WA, Shi ZL, Baric RS. 2015. A SARS-like cluster of circulating bat coronaviruses shows potential for human emergence. Nat Med 21:1508–1513. https://doi.org/10.1038/nm.3985.
15. Sheahan TP, Sims AC, Graham RL, Menachery VD, Gralinski LE, Case JB, Leist SR, Pyrc K, Feng JY, Trantcheva I, Bannister R, Park Y, Babusis D, Mo C, Mackman RL, Spahn JE, Palmiotti CA, Siegel D, Ray AS, Cihlar T, Jordan R, Denison MR, Baric RS. 2017. Broad-spectrum antiviral GS-5734 inhibits both epidemic and zoonotic coronaviruses. Sci Transl Med 9:eaal3653. https://doi.org/10.1126/scitranslmed.aal3653.
16. Anthony SJ, Gilardi K, Menachery VD, Goldstein T, Ssebide B, Mbabazi R, Navarrete-Macias I, Liang E, Wells H, Hicks A, Petrosov A, Byarugaba DK, Debbink K, Dinnon KH, Scobey T, Randell SH, Yount BL, Cranfield M, Johnson CK, Baric RS, Lipkin WI, Mazet JA. 2017. Further evidence for bats as the evolutionary source of Middle East respiratory syndrome coronavirus. mBio 8:e00373-17. https://doi.org/10.1128/mBio.00373-17.
17. Hofmann M, Wyler R. 1988. Propagation of the virus of porcine epidemic diarrhea in cell culture. J Clin Microbiol 26:2235–2239.
18. Menachery VD, Dinnon KH III, Yount BL, Jr., McAnarney ET, Gralinski LE, Hale A, Graham RL, Scobey T, Anthony SJ, Wang L, Graham B, Randell SH, Lipkin WI, Baric RS. 2019. Trypsin treatment unlocks barrier for zoonotic coronaviruses infection. bioRxiv https://doi.org/10.1101/768663.
19. Scobey T, Yount BL, Sims AC, Donaldson EF, Agnihothram SS, Menachery VD, Graham RL, Swanstrom J, Bove PF, Kim JD, Grego S, Randell SH, Baric RS. 2013. Reverse genetics with a full-length infectious cDNA of the Middle East respiratory syndrome coronavirus. Proc Natl Acad Sci U S A 110:16157–16162. https://doi.org/10.1073/pnas.1311542110.
20. Park J-E, Li K, Barlan A, Fehr AR, Perlman S, McCray PB, Jr., Gallagher T. 2016. Proteolytic processing of Middle East respiratory syndrome coronavirus spikes expands virus tropism. Proc Natl Acad Sci U S A 113: 12262–12267. https://doi.org/10.1073/pnas.1608147113.
21. de Wilde AH, Raj VS, Oudshoorn D, Bestebroer TM, van Nieuwkoop S, Limpens RWAL, Posthuma CC, van der Meer Y, Bárcena M, Haagmans BL, Snijder EJ, van den Hoogen BG. 2013. MERS-coronavirus replication induces severe in vitro cytopathology and is strongly inhibited by cyclosporin A or interferon-alpha treatment. J Gen Virol 94:1749–1760. https://doi.org/10.1099/vir.0.052910-0.
22. Banach BS, Orenstein JM, Fox LM, Randell SH, Rowley AH, Baker SC. 2009. Human airway epithelial cell culture to identify new respiratory viruses: coronavirus NL63 as a model. J Virol Methods 156:19 –26. https://doi.org/10.1016/j.jviromet.2008.10.022.
23. Tekes G, Thiel HJ. 2016. Feline coronaviruses: pathogenesis of feline infectious peritonitis. Adv Virus Res 96:193–218. https://doi.org/10.1016/bs.aivir.2016.08.002.
24. Song D, Park B. 2012. Porcine epidemic diarrhoea virus: a comprehensive review of molecular epidemiology, diagnosis, and vaccines. Virus Genes 44:167–175. https://doi.org/10.1007/s11262-012-0713-1.
25. Corti D, Zhao J, Pedotti M, Simonelli L, Agnihothram S, Fett C, Fernandez-Rodriguez B, Foglierini M, Agatic G, Vanzetta F, Gopal R, Langrish CJ, Barrett NA, Sallusto F, Baric RS, Varani L, Zambon M, Perlman S, Lanzavecchia A. 2015. Prophylactic and postexposure efficacy of a potent human monoclonal antibody against MERS coronavirus. Proc Natl Acad Sci U S A 112:10473–10478. https://doi.org/10.1073/pnas .1510199112.
26. Kleine-Weber H, Elzayat MT, Hoffmann M, Pöhlmann S. 2018. Functional analysis of potential cleavage sites in the MERS-coronavirus spike protein. Sci Rep 8:16597. https://doi.org/10.1038/s41598-018-34859-w.
27. Biniossek ML, Nagler DK, Becker-Pauly C, Schilling O. 2011. Proteomic identification of protease cleavage sites characterizes prime and non-prime specificity of cysteine cathepsins B, L, and S. J Proteome Res 10:5363–5373. https://doi.org/10.1021/pr200621z.
28. Yang Y, Liu C, Du L, Jiang S, Shi Z, Baric RS, Li F. 2015. Two mutations were critical for bat-to-human transmission of Middle East respiratory syndrome coronavirus. J Virol 89:9119–9123. https://doi.org/10.1128/JVI.01279-15.
29. Zheng Y, Shang J, Yang Y, Liu C, Wan Y, Geng Q, Wang M, Baric R, Li F, Zheng Y, Shang J, Yang Y, Liu C, Wan Y, Geng Q, Wang M, Baric R, Li F. 2018. Lysosomal proteases are a determinant of coronavirus tropism. J Virol 92:e01504-18. https://doi.org/10.1128/JVI.01504-18.
30. Yang Y, Du L, Liu C, Wang L, Ma C, Tang J, Baric RS, Jiang S, Li F. 2014. Receptor usage and cell entry of bat coronavirus HKU4 provide insight into bat-to-human transmission of MERS coronavirus. Proc Natl Acad Sci U S A 111:12516–12521. https://doi.org/10.1073/pnas.1405889111.
31. Graham RL, Baric RS. 2010. Recombination, reservoirs, and the modular spike: mechanisms of coronavirus cross-species transmission. J Virol 84:3134–3146. https://doi.org/10.1128/JVI.01394-09.
32. Ge X-Y, Li J-L, Yang X-L, Chmura AA, Zhu G, Epstein JH, Mazet JK, Hu B, Zhang W, Peng C, Zhang Y-J, Luo C-M, Tan B, Wang N, Zhu Y, Crameri G, Zhang S-Y, Wang L-F, Daszak P, Shi Z-L. 2013. Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor. Nature 503:535–538. https://doi.org/10.1038/nature12711.
33. Luo C-M, Wang N, Yang X-L, Liu H-Z, Zhang W, Li B, Hu B, Peng C, Geng Q-B, Zhu G-J, Li F, Shi Z-L, Luo C-M, Wang N, Yang X-L, Liu H-Z, Zhang W, Li B, Hu B, Peng C, Geng Q-B, Zhu G-J, Li F, Shi Z-L. 2018. Discovery of novel bat coronaviruses in South China that use the same receptor as Middle East respiratory syndrome coronavirus. J Virol 92:e00116-18. https://doi.org/10.1128/JVI.00116-18.
34. Klenk H-D, Rott R, Orlich M, Blödorn J. 1975. Activation of influenza A viruses by trypsin treatment. Virology 68:426–439. https://doi.org/10.1016/0042-6822(75)90284-6.
35. Luczo JM, Stambas J, Durr PA, Michalski WP, Bingham J. 2015. Molecular pathogenesis of H5 highly pathogenic avian influenza: the role of the haemagglutinin cleavage site motif. Rev Med Virol 25:406–430. https://doi.org/10.1002/rmv.1846.
36. Clark SM, Roth JR, Clark ML, Barnett BB, Spendlove RS. 1981. Trypsin enhancement of rotavirus infectivity: mechanism of enhancement. J Virol 39:816–822.
37. Roivainen M, Hovi T. 1987. Intestinal trypsin can significantly modify antigenic properties of polioviruses: implications for the use of inactivated poliovirus vaccine. J Virol 61:3749–3753.
38. Hu H, Jung K, Vlasova AN, Chepngeno J, Lu Z, Wang Q, Saif LJ. 2015. Isolation and characterization of porcine deltacoronavirus from pigs with diarrhea in the United States. J Clin Microbiol 53:1537–1548. https://doi.org/10.1128/JCM.00031-15.
39. Wicht O, Li W, Willems L, Meuleman TJ, Wubbolts RW, van Kuppeveld FJ, Rottier PJ, Bosch BJ. 2014. Proteolytic activation of the porcine epidemic diarrhea coronavirus spike fusion protein by trypsin in cell culture. J Virol 88:7952–7961. https://doi.org/10.1128/JVI.00297-14.
40. Zhou P, Fan H, Lan T, Yang X-L, Shi W-F, Zhang W, Zhu Y, Zhang Y-W, Xie Q-M, Mani S, Zheng X-S, Li B, Li J-M, Guo H, Pei G-Q, An X-P, Chen J-W, Zhou L, Mai K-J, Wu ZX, Li D, Anderson DE, Zhang L-B, Li S-Y, Mi Z-Q, He T-T, Cong F, Guo P-J, Huang R, Luo Y, Liu X-L, Chen J, Huang Y, Sun Q, Zhang X-L-L, Wang Y-Y, Xing S-Z, Chen Y-S, Sun Y, Li J, Daszak P, Wang L-F, Shi Z-L, Tong Y-G, Ma J-Y. 2018. Fatal swine acute diarrhoea syndrome caused by an HKU2-related coronavirus of bat origin. Nature 556:255–258. https://doi.org/10.1038/s41586-018-0010-9.
41. Li K, Wohlford-Lenane CL, Channappanavar R, Park J-E, Earnest JT, Bair TB, Bates AM, Brogden KA, Flaherty HA, Gallagher T, Meyerholz DK, Perlman S, McCray PB, Jr. 2017. Mouse-adapted MERS coronavirus causes lethal lung disease in human DPP4 knockin mice. Proc Natl Acad Sci U S A 114:E3119–E3128. https://doi.org/10.1073/pnas.1619109114.
42. Matsuyama S, Ujike M, Morikawa S, Tashiro M, Taguchi F. 2005. Protease-mediated enhancement of severe acute respiratory syndrome coronavirus infection. Proc Natl Acad Sci U S A 102:12543–12547. https://doi .org/10.1073/pnas.0503203102.
43. Zeng L-P, Gao Y-T, Ge X-Y, Zhang Q, Peng C, Yang X-L, Tan B, Chen J, Chmura AA, Daszak P, Shi Z-L. 2016. Bat severe acute respiratory syndrome-like coronavirus WIV1 encodes an extra accessory protein, ORFX, involved in modulation of the host immune response. J Virol 90:6573–6582. https://doi.org/10.1128/JVI.03079-15.
44. Millet JK, Whittaker GR. 2015. Host cell proteases: critical determinants of coronavirus tropism and pathogenesis. Virus Res 202:120 –134. https://doi.org/10.1016/j.virusres.2014.11.021.
45. Earnest JT, Hantak MP, Li K, McCray PB, Jr., Perlman S, Gallagher T. 2017. The tetraspanin CD9 facilitates MERS-coronavirus entry by scaffolding host cell receptors and proteases. PLoS Pathog 13:e1006546. https://doi.org/10.1371/journal.ppat.1006546.
46. Zhou J, Li C, Zhao G, Chu H, Wang D, Yan HH, Poon VK, Wen L, Wong BH-Y, Zhao X, Chiu MC, Yang D, Wang Y, Au-Yeung RKH, Chan IH-Y, Sun S, Chan JF-W, To KK-W, Memish ZA, Corman VM, Drosten C, Hung IF-N, Zhou Y, Leung SY, Yuen K-Y. 2017. Human intestinal tract serves as an alternative infection route for Middle East respiratory syndrome coronavirus. Sci Adv 3:eaao4966. https://doi.org/10.1126/sciadv.aao4966.
47. Ding Y, He L, Zhang Q, Huang Z, Che X, Hou J, Wang H, Shen H, Qiu L, Li Z, Geng J, Cai J, Han H, Li X, Kang W, Weng D, Liang P, Jiang S. 2004. Organ distribution of severe acute respiratory syndrome (SARS) associated coronavirus (SARS-CoV) in SARS patients: implications for pathogenesis and virus transmission pathways. J Pathol 203:622–630. https://doi.org/10.1002/path.1560.
48. Zhang X, Hasoksuz M, Spiro D, Halpin R, Wang S, Stollar S, Janies D, Hadya N, Tang Y, Ghedin E, Saif L. 2007. Complete genomic sequences, a key residue in the spike protein and deletions in nonstructural protein 3b of US strains of the virulent and attenuated coronaviruses, transmissible gastroenteritis virus and porcine respiratory coronavirus. Virology 358:424–435. https://doi.org/10.1016/j.virol.2006.08.051.
49. Pallesen J, Wang N, Corbett KS, Wrapp D, Kirchdoerfer RN, Turner HL, Cottrell CA, Becker MM, Wang L, Shi W, Kong W-P, Andres EL, Kettenbach AN, Denison MR, Chappell JD, Graham BS, Ward AB, McLellan JS. 2017. Immunogenicity and structures of a rationally designed prefusion MERS-CoV spike antigen. Proc Natl Acad Sci U S A 114:E7348 –E7357. https://doi.org/10.1073/pnas.1707304114.
50. Gallagher TM, Buchmeier MJ, Perlman S. 1992. Cell receptor-independent infection by a neurotropic murine coronavirus. Virology 191:517–522. https://doi.org/10.1016/0042-6822(92)90223-c.
51. Li W, Hulswit RJG, Widjaja I, Raj VS, McBride R, Peng W, Widagdo W, Tortorici MA, van Dieren B, Lang Y, van Lent JWM, Paulson JC, de Haan CAM, de Groot RJ, van Kuppeveld FJM, Haagmans BL, Bosch B-J. 2017. Identification of sialic acid-binding function for the Middle East respiratory syndrome coronavirus spike glycoprotein. Proc Natl Acad Sci U S A 114:E8508–E8517. https://doi.org/10.1073/pnas.1712592114.
52. Sims AC, Tilton SC, Menachery VD, Gralinski LE, Schafer A, Matzke MM, Webb-Robertson B-J, Chang J, Luna ML, Long CE, Shukla AK, Bankhead AR, III, Burkett SE, Zornetzer G, Tseng C-TK, Metz TO, Pickles R, Mc-Weeney S, Smith RD, Katze MG, Waters KM, Baric RS. 2013. Release of severe acute respiratory syndrome coronavirus nuclear import block enhances host transcription in human lung cells. J Virol 87:3885–3902. https://doi.org/10.1128/JVI.02520-12.
53. Sims AC, Burkett SE, Yount B, Pickles RJ. 2008. SARS-CoV replication and pathogenesis in an in vitro model of the human conducting airway epithelium. Virus Res 133:33–44. https://doi.org/10.1016/j.virusres.2007.03.013.
54. Almazán F, DeDiego ML, Sola I, Zuñiga S, Nieto-Torres JL, Marquez-Jurado S, Andrés G, Enjuanes L. 2013. Engineering a replication-competent, propagation-defective Middle East respiratory syndrome coronavirus as a vaccine candidate. mBio 4:e00650-13. https://doi.org/10.1128/mBio.00650-13.
55. Agnihothram S, Menachery VD, Yount BL, Lindesmith LC, Scobey T, Whitmore A, Schafer A, Heise MT, Baric RS. 2018. Development of a broadly accessible Venezuelan equine encephalitis virus replicon particle vaccine platform. J Virol 92:e00027-18. https://doi.org/10.1128/JVI.00027-18.
56. Bolles M, Deming D, Long K, Agnihothram S, Whitmore A, Ferris M, Funkhouser W, Gralinski L, Totura A, Heise M, Baric RS. 2011. A double-inactivated severe acute respiratory syndrome coronavirus vaccine provides incomplete protection in mice and induces increased eosinophilic proinflammatory pulmonary response upon challenge. J Virol 85: 12201–12215. https://doi.org/10.1128/JVI.06048-11.
57. Sheahan T, Whitmore A, Long K, Ferris M, Rockx B, Funkhouser W, Donaldson E, Gralinski L, Collier M, Heise M, Davis N, Johnston R, Baric RS. 2011. Successful vaccination strategies that protect aged mice from lethal challenge from influenza virus and heterologous severe acute respiratory syndrome coronavirus. J Virol 85:217–230. https://doi.org/10.1128/JVI.01805-10.
58. Huynh J, Li S, Yount B, Smith A, Sturges L, Olsen JC, Nagel J, Johnson JB, Agnihothram S, Gates JE, Frieman MB, Baric RS, Donaldson EF. 2012. Evidence supporting a zoonotic origin of human coronavirus strain NL63. J Virol 86:12816–12825. https://doi.org/10.1128/JVI.00906-12.
59. Zaki AM, van Boheemen S, Bestebroer TM, Osterhaus AD, Fouchier RA. 2012. Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med 367:1814–1820. https://doi.org/10.1056/ NEJMoa1211721.