Adaptive evolution influences the infectious dose of MERS-CoV necessary to achieve severe respiratory disease

Virology

Volumn 517, Issue , 2018, Pages 98-107

  Douglas, Madeline G ^a   Kocher, Jacob F ^a   Scobey, Trevor ^a   Baric, Ralph S ^a,b   Cockrell, Adam S ^a  

^a IL   (United States)

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

Author keywords

Acute respiratory distress syndrome; Coronavirus; MERS CoV; Middle East respiratory syndrome; Respiratory disease; Spike protein

Indexed keywords

ADAPTIVE EVOLUTION; ADULT RESPIRATORY DISTRESS SYNDROME; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLEEDING; BODY WEIGHT LOSS; CHRONIC RESPIRATORY TRACT DISEASE; CONTROLLED STUDY; EVOLUTION; FEMALE; INFECTIOUS DOSE; MALE; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; STRUCTURAL HOMOLOGY; VIRAL GENETICS; VIRUS GENOME; VIRUS LOAD; VIRUS MUTATION; VIRUS VIRULENCE; ANIMAL; CORONAVIRUS INFECTION; LUNG; PATHOLOGY; PHYSIOLOGY; TRANSGENIC ORGANISM; VIROLOGY;

ANIMALS; BIOLOGICAL EVOLUTION; CORONAVIRUS INFECTIONS; LUNG; MICE; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; ORGANISMS, GENETICALLY MODIFIED;

EID: 85038865669     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2017.12.006     Document Type: Article

References (45)

1. Alsaad, K.O., Hajeer, A.H., Al Balwi, M., Al Moaiqel, M., Al Oudah, N., Al Ajlan, A., AlJohani, S., Alsolamy, S., Gmati, G.E., Balkhy, H., Al-Jahdali, H.H., Baharoon, S.A., Arabi, Y.M., Histopathology of Middle East respiratory syndrome coronovirus (MERS-CoV) infection - clinicopathological and ultrastructural study. Histopathology, 2017.
2. Angelini, M.M., Akhlaghpour, M., Neuman, B.W., Buchmeier, M.J., Severe acute respiratory syndrome coronavirus nonstructural proteins 3, 4, and 6 induce double-membrane vesicles. mBio, 2013, 4.
3. Arabi, Y.M., Balkhy, H.H., Hayden, F.G., Bouchama, A., Luke, T., Baillie, J.K., Al-Omari, A., Hajeer, A.H., Senga, M., Denison, M.R., Nguyen-Van-Tam, J.S., Shindo, N., Bermingham, A., Chappell, J.D., Van Kerkhove, M.D., Fowler, R.A., Middle east respiratory syndrome. N. Engl. J. Med. 376 (2017), 584–594.
4. Baez-Santos, Y.M., St John, S.E., Mesecar, A.D., The SARS-coronavirus papain-like protease: structure, function and inhibition by designed antiviral compounds. Antivir. Res. 115 (2015), 21–38.
5. Bin, S.Y., Heo, J.Y., Song, M.S., Lee, J., Kim, E.H., Park, S.J., Kwon, H.I., Kim, S.M., Kim, Y.I., Si, Y.J., Lee, I.W., Baek, Y.H., Choi, W.S., Min, J., Jeong, H.W., Choi, Y.K., Environmental contamination and viral shedding in MERS patients during MERS-CoV outbreak in South Korea. Clin. Infect. Dis. 62 (2016), 755–760.
6. Chan, J.F., Yao, Y., Yeung, M.L., Deng, W., Bao, L., Jia, L., Li, F., Xiao, C., Gao, H., Yu, P., Cai, J.P., Chu, H., Zhou, J., Chen, H., Qin, C., Yuen, K.Y., Treatment With Lopinavir/Ritonavir or interferon-beta1b improves outcome of MERS-CoV infection in a nonhuman primate model of common marmoset. J. Infect. Dis. 212 (2015), 1904–1913.
7. Cockrell, A.S., Yount, B.L., Scobey, T., Jensen, K., Douglas, M., Beall, A., Tang, X.C., Marasco, W.A., Heise, M.T., Baric, R.S., A mouse model for MERS coronavirus-induced acute respiratory distress syndrome. Nat. Microbiol., 2, 2016, 16226.
8. Coleman, C.M., Sisk, J.M., Halasz, G., Zhong, J., Beck, S.E., Matthews, K.L., Venkataraman, T., Rajagopalan, S., Kyratsous, C.A., Frieman, M.B., CD8+ T cells and macrophages regulate pathogenesis in a mouse model of middle east respiratory syndrome. J. Virol., 2017, 91.
9. Egloff, M.P., Malet, H., Putics, A., Heinonen, M., Dutartre, H., Frangeul, A., Gruez, A., Campanacci, V., Cambillau, C., Ziebuhr, J., Ahola, T., Canard, B., Structural and functional basis for ADP-ribose and poly(ADP-ribose) binding by viral macro domains. J. Virol. 80 (2006), 8493–8502.
10. Falzarano, D., de Wit, E., Feldmann, F., Rasmussen, A.L., Okumura, A., Peng, X., Thomas, M.J., van Doremalen, N., Haddock, E., Nagy, L., LaCasse, R., Liu, T., Zhu, J., McLellan, J.S., Scott, D.P., Katze, M.G., Feldmann, H., Munster, V.J., Infection with MERS-CoV causes lethal pneumonia in the common marmoset. PLoS Pathog., 10, 2014, e1004250.
11. Fehr, A.R., Athmer, J., Channappanavar, R., Phillips, J.M., Meyerholz, D.K., Perlman, S., The nsp3 macrodomain promotes virulence in mice with coronavirus-induced encephalitis. J. Virol. 89 (2015), 1523–1536.
12. Hulswit, R.J., de Haan, C.A., Bosch, B.J., Coronavirus spike protein and tropism changes. Adv. Virus Res. 96 (2016), 29–57.
13. Johnson, R.F., Via, L.E., Kumar, M.R., Cornish, J.P., Yellayi, S., Huzella, L., Postnikova, E., Oberlander, N., Bartos, C., Ork, B.L., Mazur, S., Allan, C., Holbrook, M.R., Solomon, J., Johnson, J.C., Pickel, J., Hensley, L.E., Jahrling, P.B., Intratracheal exposure of common marmosets to MERS-CoV Jordan-n3/2012 or MERS-CoV EMC/2012 isolates does not result in lethal disease. Virology 485 (2015), 422–430.
14. Johnson, R.F., Bagci, U., Keith, L., Tang, X., Mollura, D.J., Zeitlin, L., Qin, J., Huzella, L., Bartos, C.J., Bohorova, N., Bohorov, O., Goodman, C., Kim do, H., Paulty, M.H., Velasco, J., Whaley, K.J., Johnson, J.C., Pettitt, J., Ork, B.L., Solomon, J., Oberlander, N., Zhu, Q., Sun, J., Holbrook, M.R., Olinger, G.G., Baric, R.S., Hensley, L.E., Jahrling, P.B., Marasco, W.A., 3B11-N, a monoclonal antibody against MERS-CoV, reduces lung pathology in rhesus monkeys following intratracheal inoculation of MERS-CoV Jordan-n3/2012. Virology 490 (2016), 49–58.
15. Kelley, L.A., Mezulis, S., Yates, C.M., Wass, M.N., Sternberg, M.J., The Phyre2 web portal for protein modeling, prediction and analysis. Nat. Protoc. 10 (2015), 845–858.
16. Kirchdoerfer, R.N., Cottrell, C.A., Wang, N., Pallesen, J., Yassine, H.M., Turner, H.L., Corbett, K.S., Graham, B.S., McLellan, J.S., Ward, A.B., Pre-fusion structure of a human coronavirus spike protein. Nature 531 (2016), 118–121.
17. Lamers, M.M., Raj, V.S., Shafei, M., Ali, S.S., Abdallh, S.M., Gazo, M., Nofal, S., Lu, X., Erdman, D.D., Koopmans, M.P., Abdallat, M., Haddadin, A., Haagmans, B.L., Deletion variants of middle east respiratory syndrome coronavirus from humans, Jordan, 2015. Emerg. Infect. Dis. 22 (2016), 716–719.
18. Lee, S.I., Costly lessons from the 2015 middle east respiratory syndrome coronavirus outbreak in Korea. J. Prev. Med. Public Health 48 (2015), 274–276.
19. Li, K., Wohlford-Lenane, C.L., Channappanavar, R., Park, J.E., Earnest, J.T., Bair, T.B., Bates, A.M., Brogden, K.A., Flaherty, H.A., Gallagher, T., Meyerholz, D.K., Perlman, S., McCray, P.B. Jr., Mouse-adapted MERS coronavirus causes lethal lung disease in human DPP4 knockin mice. Proc. Natl. Acad. Sci. USA 114 (2017), E3119–E3128.
20. Li, W., Hulswit, R.J.G., Widjaja, I., Raj, V.S., McBride, R., Peng, W., Widagdo, W., Tortorici, M.A., van Dieren, B., Lang, Y., van Lent, J.W.M., Paulson, J.C., de Haan, C.A.M., de Groot, R.J., van Kuppeveld, F.J.M., Haagmans, B.L., Bosch, B.J., Identification of sialic acid-binding function for the Middle East respiratory syndrome coronavirus spike glycoprotein. Proc. Natl. Acad. Sci. USA, 2017.
21. Lui, P.Y., Wong, L.Y., Fung, C.L., Siu, K.L., Yeung, M.L., Yuen, K.S., Chan, C.P., Woo, P.C., Yuen, K.Y., Jin, D.Y., Middle East respiratory syndrome coronavirus M protein suppresses type I interferon expression through the inhibition of TBK1-dependent phosphorylation of IRF3. Emerg. Microbes Infect., 5, 2016, e39.
22. Lundin, A., Dijkman, R., Bergstrom, T., Kann, N., Adamiak, B., Hannoun, C., Kindler, E., Jonsdottir, H.R., Muth, D., Kint, J., Forlenza, M., Muller, M.A., Drosten, C., Thiel, V., Trybala, E., Targeting membrane-bound viral RNA synthesis reveals potent inhibition of diverse coronaviruses including the middle East respiratory syndrome virus. PLoS Pathog., 10, 2014, e1004166.
23. Matthews, K.L., Coleman, C.M., van der Meer, Y., Snijder, E.J., Frieman, M.B., The ORF4b-encoded accessory proteins of Middle East respiratory syndrome coronavirus and two related bat coronaviruses localize to the nucleus and inhibit innate immune signalling. J. Gen. Virol. 95 (2014), 874–882.
24. Menachery, V.D., Mitchell, H.D., Cockrell, A.S., Gralinski, L.E., Yount, B.L. Jr., Graham, R.L., McAnarney, E.T., Douglas, M.G., Scobey, T., Beall, A., Dinnon, K. 3rd, Kocher, J.F., Hale, A.E., Stratton, K.G., Waters, K.M., Baric, R.S., MERS-CoV accessory ORFs play key role for infection and pathogenesis. mBio, 2017, 8.
25. Meyerholz, D.K., Lambertz, A.M., McCray, P.B. Jr., Dipeptidyl peptidase 4 distribution in the human respiratory tract: implications for the middle east respiratory syndrome. Am. J. Pathol. 186 (2016), 78–86.
26. Millet, J.K., Whittaker, G.R., Host cell entry of Middle East respiratory syndrome coronavirus after two-step, furin-mediated activation of the spike protein. Proc. Natl. Acad. Sci. USA 111 (2014), 15214–15219.
27. Munster, V.J., de Wit, E., Feldmann, H., Pneumonia from human coronavirus in a macaque model. N. Engl. J. Med. 368 (2013), 1560–1562.
28. Ng, D.L., Al Hosani, F., Keating, M.K., Gerber, S.I., Jones, T.L., Metcalfe, M.G., Tong, S., Tao, Y., Alami, N.N., Haynes, L.M., Mutei, M.A., Abdel-Wareth, L., Uyeki, T.M., Swerdlow, D.L., Barakat, M., Zaki, S.R., Clinicopathologic, immunohistochemical, and ultrastructural findings of a fatal case of middle east respiratory syndrome coronavirus infection in the United Arab Emirates, April 2014. Am. J. Pathol. 186 (2016), 652–658.
29. Oh, M.D., Park, W.B., Choe, P.G., Choi, S.J., Kim, J.I., Chae, J., Park, S.S., Kim, E.C., Oh, H.S., Kim, E.J., Nam, E.Y., Na, S.H., Kim, D.K., Lee, S.M., Song, K.H., Bang, J.H., Kim, E.S., Kim, H.B., Park, S.W., Kim, N.J., Viral load kinetics of MERS coronavirus infection. N. Engl. J. Med. 375 (2016), 1303–1305.
30. Ohnuma, K., Dang, N.H., Morimoto, C., Revisiting an old acquaintance: CD26 and its molecular mechanisms in T cell function. Trends Immunol. 29 (2008), 295–301.
31. Pacciarini, F., Ghezzi, S., Canducci, F., Sims, A., Sampaolo, M., Ferioli, E., Clementi, M., Poli, G., Conaldi, P.G., Baric, R., Vicenzi, E., Persistent replication of severe acute respiratory syndrome coronavirus in human tubular kidney cells selects for adaptive mutations in the membrane protein. J. Virol. 82 (2008), 5137–5144.
32. Rabouw, H.H., Langereis, M.A., Knaap, R.C., Dalebout, T.J., Canton, J., Sola, I., Enjuanes, L., Bredenbeek, P.J., Kikkert, M., de Groot, R.J., van Kuppeveld, F.J., Middle east respiratory coronavirus accessory protein 4a inhibits PKR-mediated antiviral stress responses. PLoS Pathog., 12, 2016, e1005982.
33. Roberts, A., Deming, D., Paddock, C.D., Cheng, A., Yount, B., Vogel, L., Herman, B.D., Sheahan, T., Heise, M., Genrich, G.L., Zaki, S.R., Baric, R., Subbarao, K., A mouse-adapted SARS-coronavirus causes disease and mortality in BALB/c mice. PLoS Pathog., 3, 2007, e5.
34. Rohrborn, D., Wronkowitz, N., Eckel, J., DPP4 in diabetes. Front. Immunol., 6, 2015, 386.
35. Saikatendu, K.S., Joseph, J.S., Subramanian, V., Clayton, T., Griffith, M., Moy, K., Velasquez, J., Neuman, B.W., Buchmeier, M.J., Stevens, R.C., Kuhn, P., Structural basis of severe acute respiratory syndrome coronavirus ADP-ribose-1’’-phosphate dephosphorylation by a conserved domain of nsP3. Structure 13 (2005), 1665–1675.
36. Siu, K.L., Chan, C.P., Kok, K.H., Chiu-Yat Woo, P., Jin, D.Y., Suppression of innate antiviral response by severe acute respiratory syndrome coronavirus M protein is mediated through the first transmembrane domain. Cell Mol. Immunol. 11 (2014), 141–149.
37. Snijder, E.J., Decroly, E., Ziebuhr, J., The nonstructural proteins directing coronavirus RNA synthesis and processing. Adv. Virus Res. 96 (2016), 59–126.
38. Subissi, L., Posthuma, C.C., Collet, A., Zevenhoven-Dobbe, J.C., Gorbalenya, A.E., Decroly, E., Snijder, E.J., Canard, B., Imbert, I., One severe acute respiratory syndrome coronavirus protein complex integrates processive RNA polymerase and exonuclease activities. Proc. Natl. Acad. Sci. USA 111 (2014), E3900–E3909.
39. Thornbrough, J.M., Jha, B.K., Yount, B., Goldstein, S.A., Li, Y., Elliott, R., Sims, A.C., Baric, R.S., Silverman, R.H., Weiss, S.R., Middle east respiratory syndrome coronavirus NS4b protein inhibits host RNase L activation. mBio, 7, 2016, e00258.
40. Walls, A.C., Tortorici, M.A., Bosch, B.J., Frenz, B., Rottier, P.J.M., DiMaio, F., Rey, F.A., Veesler, D., Cryo-electron microscopy structure of a coronavirus spike glycoprotein trimer. Nature 531 (2016), 114–117.
41. WHO, 2017. WHO | Middle East respiratory syndrome coronavirus (MERS-CoV). 〈http://www.who.int/emergencies/mers-cov/en/〉.
42. Widagdo, W., Raj, V.S., Schipper, D., Kolijn, K., van Leenders, G.J., Bosch, B.J., Bensaid, A., Segales, J., Baumgartner, W., Osterhaus, A.D., Koopmans, M.P., van den Brand, J.M., Haagmans, B.L., Differential expression of the middle east respiratory syndrome coronavirus receptor in the upper respiratory tracts of humans and dromedary camels. J. Virol. 90 (2016), 4838–4842.
43. Yang, Y., Zhang, L., Geng, H., Deng, Y., Huang, B., Guo, Y., Zhao, Z., Tan, W., The structural and accessory proteins M, ORF 4a, ORF 4b, and ORF 5 of Middle East respiratory syndrome coronavirus (MERS-CoV) are potent interferon antagonists. Protein Cell 4 (2013), 951–961.
44. Yang, Y., Ye, F., Zhu, N., Wang, W., Deng, Y., Zhao, Z., Tan, W., Middle East respiratory syndrome coronavirus ORF4b protein inhibits type I interferon production through both cytoplasmic and nuclear targets. Sci. Rep., 5, 2015, 17554.
45. Yuan, Y., Cao, D., Zhang, Y., Ma, J., Qi, J., Wang, Q., Lu, G., Wu, Y., Yan, J., Shi, Y., Zhang, X., Gao, G.F., Cryo-EM structures of MERS-CoV and SARS-CoV spike glycoproteins reveal the dynamic receptor binding domains. Nat. Commun., 8, 2017, 15092.