Adaptive Evolution of MERS-CoV to Species Variation in DPP4

Cell Reports

Volumn 24, Issue 7, 2018, Pages 1730-1737

  Letko, Michael ^a   Miazgowicz, Kerri ^a,b   McMinn, Rebekah ^a,c   Seifert, Stephanie N ^a   Sola, Isabel ^d   Enjuanes, Luis ^d   Carmody, Aaron ^a   van Doremalen, Neeltje ^a   Munster, Vincent ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

^c Department of Environmental and Radiological Health Sciences   (United States)

^d CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

Author keywords

Adaptation; Bat; Coronavirus; Desmodus rotundus; Dipeptidyl peptidase IV; DPP4; Evolution; MERS; Species barrier; Spike; Zoonosis

Indexed keywords

DIPEPTIDYL PEPTIDASE IV; CORONAVIRUS SPIKE GLYCOPROTEIN; PROTEIN BINDING; VIRUS RECEPTOR;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DESMODUS ROTUNDUS; EVOLUTIONARY ADAPTATION; GENE IDENTIFICATION; GENETIC VARIABILITY; GENETIC VARIATION; HOST RANGE; HUMAN; HUMAN CELL; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; MUTATION ACCUMULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SPECIES DIVERSITY; STRUCTURE ANALYSIS; SURFACE CHARGE; VIRUS CHARACTERIZATION; VIRUS CULTURE; VIRUS ENTRY; VIRUS MUTATION; VIRUS REPLICATION; VIRUS SPIKE; ADAPTATION; ALPHA HELIX; AMINO ACID SEQUENCE; ANIMAL; BAT; BETA SHEET; BINDING SITE; CHEMISTRY; CHLOROCEBUS AETHIOPS; COEVOLUTION; CRICETULUS; GENE EXPRESSION; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; MOLECULAR MODEL; MUTATION; PROTEIN DOMAIN; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; VERO CELL LINE;

ADAPTATION, PHYSIOLOGICAL; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; BIOLOGICAL COEVOLUTION; CERCOPITHECUS AETHIOPS; CHIROPTERA; CRICETULUS; DIPEPTIDYL PEPTIDASE 4; GENE EXPRESSION; HOST SPECIFICITY; HOST-PATHOGEN INTERACTIONS; HUMANS; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; MODELS, MOLECULAR; MUTATION; PROTEIN BINDING; PROTEIN CONFORMATION, ALPHA-HELICAL; PROTEIN CONFORMATION, BETA-STRAND; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECEPTORS, VIRUS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SPIKE GLYCOPROTEIN, CORONAVIRUS; VERO CELLS; VIRUS INTERNALIZATION;

EID: 85050876135     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2018.07.045     Document Type: Article

References (37)

1. Adney, D.R., van Doremalen, N., Brown, V.R., Bushmaker, T., Scott, D., de Wit, E., Bowen, R.A., Munster, V.J., Replication and shedding of MERS-CoV in upper respiratory tract of inoculated dromedary camels. Emerg. Infect. Dis. 20 (2014), 1999–2005.
2. Agrawal, A.S., Garron, T., Tao, X., Peng, B.H., Wakamiya, M., Chan, T.S., Couch, R.B., Tseng, C.T., Generation of a transgenic mouse model of Middle East respiratory syndrome coronavirus infection and disease. J. Virol. 89 (2015), 3659–3670.
3. Almazán, F., DeDiego, M.L., Sola, I., Zuñiga, S., Nieto-Torres, J.L., Marquez-Jurado, S., Andrés, G., Enjuanes, L., Engineering a replication-competent, propagation-defective Middle East respiratory syndrome coronavirus as a vaccine candidate. MBio, 4, 2013 e00650–13.
4. Azhar, E.I., El-Kafrawy, S.A., Farraj, S.A., Hassan, A.M., Al-Saeed, M.S., Hashem, A.M., Madani, T.A., Evidence for camel-to-human transmission of MERS coronavirus. N. Engl. J. Med. 370 (2014), 2499–2505.
5. Baker, N.A., Sept, D., Joseph, S., Holst, M.J., McCammon, J.A., Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl. Acad. Sci. USA 98 (2001), 10037–10041.
6. Baric, R.S., Sullivan, E., Hensley, L., Yount, B., Chen, W., Persistent infection promotes cross-species transmissibility of mouse hepatitis virus. J. Virol. 73 (1999), 638–649.
7. Barlan, A., Zhao, J., Sarkar, M.K., Li, K., McCray, P.B. Jr., Perlman, S., Gallagher, T., Receptor variation and susceptibility to Middle East respiratory syndrome coronavirus infection. J. Virol. 88 (2014), 4953–4961.
8. Caì Y., Yú S.Q., Postnikova, E.N., Mazur, S., Bernbaum, J.G., Burk, R., Zhāng, T., Radoshitzky, S.R., Müller, M.A., Jordan, I., et al. CD26/DPP4 cell-surface expression in bat cells correlates with bat cell susceptibility to Middle East respiratory syndrome coronavirus (MERS-CoV) infection and evolution of persistent infection. PLoS ONE, 9, 2014, e112060.
9. Cockrell, A.S., Peck, K.M., Yount, B.L., Agnihothram, S.S., Scobey, T., Curnes, N.R., Baric, R.S., Heise, M.T., Mouse dipeptidyl peptidase 4 is not a functional receptor for Middle East respiratory syndrome coronavirus infection. J. Virol. 88 (2014), 5195–5199.
10. 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.
11. Corman, V.M., Eckerle, I., Bleicker, T., Zaki, A., Landt, O., Eschbach-Bludau, M., van Boheemen, S., Gopal, R., Ballhause, M., Bestebroer, T.M., et al. Detection of a novel human coronavirus by real-time reverse-transcription polymerase chain reaction. Euro Surveill., 17, 2012, 20285.
12. de Wit, E., Rasmussen, A.L., Falzarano, D., Bushmaker, T., Feldmann, F., Brining, D.L., Fischer, E.R., Martellaro, C., Okumura, A., Chang, J., et al. Middle East respiratory syndrome coronavirus (MERS-CoV) causes transient lower respiratory tract infection in rhesus macaques. Proc. Natl. Acad. Sci. USA 110 (2013), 16598–16603.
13. Dolinsky, T.J., Nielsen, J.E., McCammon, J.A., Baker, N.A., PDB2PQR: an automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations. Nucleic Acids Res., 32, 2004 W665-7.
14. Falzarano, D., de Wit, E., Feldmann, F., Rasmussen, A.L., Okumura, A., Peng, X., Thomas, M.J., van Doremalen, N., Haddock, E., Nagy, L., et al. Infection with MERS-CoV causes lethal pneumonia in the common marmoset. PLoS Pathog., 10, 2014, e1004250.
15. Haagmans, B.L., Al Dhahiry, S.H., Reusken, C.B., Raj, V.S., Galiano, M., Myers, R., Godeke, G.J., Jonges, M., Farag, E., Diab, A., et al. Middle East respiratory syndrome coronavirus in dromedary camels: an outbreak investigation. Lancet Infect. Dis. 14 (2014), 140–145.
16. Ithete, N.L., Stoffberg, S., Corman, V.M., Cottontail, V.M., Richards, L.R., Schoeman, M.C., Drosten, C., Drexler, J.F., Preiser, W., Close relative of human Middle East respiratory syndrome coronavirus in bat, South Africa. Emerg. Infect. Dis. 19 (2013), 1697–1699.
17. Letko, M., Booiman, T., Kootstra, N., Simon, V., Ooms, M., Identification of the HIV-1 Vif and Human APOBEC3G Protein Interface. Cell Rep. 13 (2015), 1789–1799.
18. Li, F., Receptor recognition and cross-species infections of SARS coronavirus. Antiviral Res. 100 (2013), 246–254.
19. Lu, G., Hu, Y., Wang, Q., Qi, J., Gao, F., Li, Y., Zhang, Y., Zhang, W., Yuan, Y., Bao, J., et al. Molecular basis of binding between novel human coronavirus MERS-CoV and its receptor CD26. Nature 500 (2013), 227–231.
20. McRoy, W.C., Baric, R.S., Amino acid substitutions in the S2 subunit of mouse hepatitis virus variant V51 encode determinants of host range expansion. J. Virol. 82 (2008), 1414–1424.
21. Munster, V.J., Adney, D.R., van Doremalen, N., Brown, V.R., Miazgowicz, K.L., Milne-Price, S., Bushmaker, T., Rosenke, R., Scott, D., Hawkinson, A., et al. Replication and shedding of MERS-CoV in Jamaican fruit bats (Artibeus jamaicensis). Sci. Rep., 6, 2016, 21878.
22. Ohnuma, K., Haagmans, B.L., Hatano, R., Raj, V.S., Mou, H., Iwata, S., Dang, N.H., Bosch, B.J., Morimoto, C., Inhibition of Middle East respiratory syndrome coronavirus infection by anti-CD26 monoclonal antibody. J. Virol. 87 (2013), 13892–13899.
23. Peck, K.M., Cockrell, A.S., Yount, B.L., Scobey, T., Baric, R.S., Heise, M.T., Glycosylation of mouse DPP4 plays a role in inhibiting Middle East respiratory syndrome coronavirus infection. J. Virol. 89 (2015), 4696–4699.
24. Peck, K.M., Scobey, T., Swanstrom, J., Jensen, K.L., Burch, C.L., Baric, R.S., Heise, M.T., Permissivity of Dipeptidyl Peptidase 4 Orthologs to Middle East Respiratory Syndrome Coronavirus Is Governed by Glycosylation and Other Complex Determinants. J. Virol., 91, 2017 e00534-17.
25. Raj, V.S., Mou, H., Smits, S.L., Dekkers, D.H., Müller, M.A., Dijkman, R., Muth, D., Demmers, J.A., Zaki, A., Fouchier, R.A., et al. Dipeptidyl peptidase 4 is a functional receptor for the emerging human coronavirus-EMC. Nature 495 (2013), 251–254.
26. Roberts, A., Deming, D., Paddock, C.D., Cheng, A., Yount, B., Vogel, L., Herman, B.D., Sheahan, T., Heise, M., Genrich, G.L., et al. A mouse-adapted SARS-coronavirus causes disease and mortality in BALB/c mice. PLoS Pathog., 3, 2007, e5.
27. Sheahan, T., Rockx, B., Donaldson, E., Sims, A., Pickles, R., Corti, D., Baric, R., Mechanisms of zoonotic severe acute respiratory syndrome coronavirus host range expansion in human airway epithelium. J. Virol. 82 (2008), 2274–2285.
28. Song, W., Wang, Y., Wang, N., Wang, D., Guo, J., Fu, L., Shi, X., Identification of residues on human receptor DPP4 critical for MERS-CoV binding and entry. Virology 471-473 (2014), 49–53.
29. Takada, A., Robison, C., Goto, H., Sanchez, A., Murti, K.G., Whitt, M.A., Kawaoka, Y., A system for functional analysis of Ebola virus glycoprotein. Proc. Natl. Acad. Sci. USA 94 (1997), 14764–14769.
30. van Doremalen, N., Miazgowicz, K.L., Milne-Price, S., Bushmaker, T., Robertson, S., Scott, D., Kinne, J., McLellan, J.S., Zhu, J., Munster, V.J., Host species restriction of Middle East respiratory syndrome coronavirus through its receptor, dipeptidyl peptidase 4. J. Virol. 88 (2014), 9220–9232.
31. van Doremalen, N., Miazgowicz, K.L., Munster, V.J., Mapping the Specific Amino Acid Residues That Make Hamster DPP4 Functional as a Receptor for Middle East Respiratory Syndrome Coronavirus. J. Virol. 90 (2016), 5499–5502.
32. Wang, N., Shi, X., Jiang, L., Zhang, S., Wang, D., Tong, P., Guo, D., Fu, L., Cui, Y., Liu, X., et al. Structure of MERS-CoV spike receptor-binding domain complexed with human receptor DPP4. Cell Res. 23 (2013), 986–993.
33. World Health Organization, East respiratory syndrome coronavirus. 2018, MERS-CoV http://www.who.int/emergencies/mers-cov/en/.
34. Woo, P.C., Lau, S.K., Li, K.S., Tsang, A.K., Yuen, K.Y., Genetic relatedness of the novel human group C betacoronavirus to Tylonycteris bat coronavirus HKU4 and Pipistrellus bat coronavirus HKU5. Emerg. Microbes Infect., 1, 2012, e35.
35. Wu, K., Peng, G., Wilken, M., Geraghty, R.J., Li, F., Mechanisms of host receptor adaptation by severe acute respiratory syndrome coronavirus. J. Biol. Chem. 287 (2012), 8904–8911.
36. Yang, Y., Du, L., Liu, C., Wang, L., Ma, C., Tang, J., Baric, R.S., Jiang, S., Li, F., Receptor usage and cell entry of bat coronavirus HKU4 provide insight into bat-to-human transmission of MERS coronavirus. Proc. Natl. Acad. Sci. USA 111 (2014), 12516–12521.
37. Zaki, A.M., van Boheemen, S., Bestebroer, T.M., Osterhaus, A.D., Fouchier, R.A., Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N. Engl. J. Med. 367 (2012), 1814–1820.