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Recent Evolution of Equine Influenza and the Origin of Canine Influenza

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Recent Evolution of Equine Influenza and the Origin of Canine Influenza Recent evolution of equine influenza and the origin of canine influenza Patrick J. Collinsa,b,1, Sebastien G. Vachieria,b,1, Lesley F. Haireb, Roksana W. Ogrodowiczb, Stephen R. Martinc, Philip A. Walkerb, Xiaoli Xionga,b, Steven J. Gamblinb, and John J. Skehela,2 Divisions of aVirology, bMolecular Structure, and cPhysical Biochemistry, Medical Research Council, National Institute for Medical Research, London NW7 1AA, United Kingdom Edited by Robert A. Lamb, Northwestern University, Evanston, IL, and approved June 24, 2014 (received for review April 10, 2014) In 2004 an hemagglutinin 3 neuraminidase 8 (H3N8) equine human and avian viruses indicates that in general they are closely influenza virus was transmitted from horses to dogs in Florida similar. However, the structures of α-helix A, in the fusion sub- and subsequently spread throughout the United States and to domain (13), of the HAs of Ef and C are distinctly different from Europe. To understand the molecular basis of changes in the those of the HAs of all other known equine, avian, or human antigenicity of H3 hemagglutinins (HAs) that have occurred during influenza viruses. We have defined the genetic and structural virus evolution in horses, and to investigate the role of HA in the basis of the novel fusion subdomain structure by X-ray crystal- equine to canine cross-species transfer, we used X-ray crystallog- lography of site-specific mutant HAs and consider its possible raphy to determine the structures of the HAs from two antigen- consequences for HA stability and function in membrane fusion. ically distinct equine viruses and from a canine virus. Structurally Because of the importance of receptor binding by HA in virus all three are very similar with the majority of amino acid sequence transmission and cross-species transfer, we have used biolayer differences between the two equine HAs located on the virus interferometry to compare the avidity and specificity of equine membrane-distal molecular surface. HAs of canine viruses are and canine virus binding to a range of sialoside receptor analogs. distinct in containing a Trp-222→Leu substitution in the receptor binding site that influences specificity for receptor analogs. In the We have also used X-ray crystallography to determine the struc- fusion subdomain of canine and recent equine virus HAs a unique tures of equine and canine virus HAs in complex with some of difference is observed by comparison with all other HAs exam- these receptor analogs. From these studies we deduce the mo- MICROBIOLOGY ined to date. Analyses of site-specific mutant HAs indicate that a sin- lecular basis of the observed differences in specificity and avidity gle amino acid substitution, Thr-30→Ser, influences interactions and we consider their possible role in virus transmission. between N-terminal and C-terminal regions of the subdomain that are important in the structural changes required for membrane fu- Results and Discussion sion activity. Both structural modifications may have facilitated the Equine and Canine HA Structures. All three structures can be seen transmission of H3N8 influenza from horses to dogs. in Fig. 1 to be very similar to each other and to other HAs of the H3 subtype described before (14). This similarity was expected quine influenza viruses of the hemagglutinin 3 neuraminidase from their sequence identities: Ee vs. Ef, 95%; Ef vs. C, 96%; E8 (H3N8) subtype were first isolated in 1963 from race horses in Miami (1). Since then they have caused numerous outbreaks Significance of infection in horses around the world with serious disease and economic consequences (2). In 2004, again in Florida, an H3N8 Equine influenza viruses of the H3N8 subtype have caused virus was isolated from an outbreak of canine influenza (3) and outbreaks of respiratory disease in horses throughout the similar viruses have since been isolated from dogs in the United world since their discovery in 1963 in Florida. In 2004 an equine States and in Europe (4, 5). Genetic comparisons indicate that virus in circulation was transmitted to dogs and subsequently the canine viruses are closely related to equine viruses that were spread throughout the United States and to Europe. Compar- in circulation in horses around 2000 (3, 5). In studies of differ- ative analyses of the structures of hemagglutinin glycoproteins ences in equine viruses isolated since 1963 (6–8) and between of equine and canine viruses by X-ray crystallography locate equine and canine viruses (3, 5), the sequences of genes for the the sites of variation on the molecules, indicate a role in de- hemagglutinin membrane glycoprotein (HA) have been com- termining binding specificity for an amino acid sequence dif- pared. Sequence data for equine virus HAs indicate the evolu- ference in the receptor binding site, and describe a unique tion of four distinct lineages. The first was associated with structural difference in the membrane fusion region in recent antigenic drift, between 1963 and 1980 (6, 7, 9), and following equine and canine virus HAs by comparison with all other this three separate branches formed a “Eurasian” lineage, an known HAs. These differences are proposed to have facilitated “American” lineage, and a divided lineage containing two clades, cross-species transfer. “Florida” clade 1 and Florida clade 2 (10, 11). The HAs of the canine viruses are most similar to those of Florida clade 1 Author contributions: P.J.C., S.G.V., L.F.H., R.W.O., S.R.M., S.J.G., and J.J.S. designed research; P.J.C., S.G.V., L.F.H., R.W.O., S.R.M., P.A.W., X.X., S.J.G., and J.J.S. performed equines. The majority of amino acid sequence changes revealed research; P.J.C., S.G.V., L.F.H., R.W.O., S.R.M., P.A.W., X.X., S.J.G., and J.J.S. contributed from the analyses are in the HA1 component of HA, some in new reagents/analytic tools; P.J.C., S.G.V., S.R.M., S.J.G., and J.J.S. analyzed data; and regions known to be antigenically important in H3 HAs, and P.J.C., S.G.V., S.J.G., and J.J.S. wrote the paper. several near the receptor binding site (12) (Fig. 1). The authors declare no conflict of interest. To understand the structural consequences of these changes, This article is a PNAS Direct Submission. in particular those that distinguish equine from canine virus Freely available online through the PNAS open access option. HAs, we have used X-ray crystallography to determine their Data deposition: The atomic coordinates and structure factors have been deposited in the structures. We have examined the HAs from two equine viruses Protein Data Bank, www.pdb.org (PDB ID codes 4UNW–4UNZ, 4UO0–4UO9, and 4UOA). and one canine virus: A/Equine/Newmarket/2/93, from the Eurasian 1P.J.C. and S.G.V. contributed equally to this work. lineage, “Ee”; A/Equine/Richmond/07, from Florida clade 2, 2To whom correspondence should be addressed. Email: [email protected]. “ ” “ ” Ef ; and A/Canine/Colorado/06, C . Comparison of the overall This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. structures of the three HAs with those of other H3 HAs from 1073/pnas.1406606111/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1406606111 PNAS | July 29, 2014 | vol. 111 | no. 30 | 11175–11180 Downloaded by guest on October 6, 2021 Fig. 1. The structure of monomers of Ee, Ef, and C HAs compared with A/Duck/Ukraine/63 avian H3 HA. (A) Superposition of the A/Duck/Ukraine/63 avian H3 HA (14) (colored in green) with the Ee structure (colored in blue for the HA1 chain and in red for the HA2 chain). The position of Thr-30 of chain HA1 is also indicated. (B) Structure of the Ef HA (light shades of blue and red for the HA1 and HA2 chains, respectively). The side-chain atoms of amino acids differing from those of the Ee HA are shown as spheres. The position of Ser-30 of chain HA1 and the location of the modified HA2 α-helix are indicated. (C) Structure of the C HA (darker shades of blue and red for the HA1 and HA2 chains, respectively). The positions of the five amino acids specific to canine HAs are indicated and colored as corresponding to the chain they belong to. Also indicated is the position of HA1 Ser-30 and the location of the modified HA2 α-helix. and Ef vs. the HAs of the H3 avian and H3 human viruses, Ef and C HAs, Asn-54→Lys, Asn-83→Ser, and Ile-328→Thr (3), A/duck/Ukraine/63, 86%, and A/Aichi/2/68, 85%. It is also is not clarified by comparison of the HA structures. Residues 83 reflected in the rmsd of the α-carbon atoms shown in Table S1. and 54 are on the surface of HA, about 20 Å and 35 Å from the Of the 20-aa sequence differences noted between Ee and Ef receptor binding site, respectively, toward the virus membrane. (Fig. 1B and Fig. S1) 19 are accessible on the surface of HA. Of Amino acid substitutions at either position might influence HA these, 15 by comparison with the locations of amino acid changes antigenicity (Fig. 1). Residue 328 is the C terminus of HA1 (Fig. 1). in antigenic variants of human H3 HAs might result in antigenic The substitution Ile-328→Thr, which is conserved in canine differences (12). viruses, could have been selected to ensure the required cleavage In HA1, in the receptor binding site just one change, the of precursor HA0 into HA1 and HA2.
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