Mutation tryptophan to leucine at position 222 of haemagglutinin could facilitate H3N2 influenza A virus infection in dogs

Yang, Guohua; Li, Shoujun; Blackmon, Sherry; Ye, Jianqiang; Bradley, Konrad C.; Cooley, Jim; Smith, Dave F.; Hanson, Larry A.; Cardona, Carol J.; Steinhauer, David A.; Webby, Richard J.; Liao, Ming; Wan, Xiu Feng

doi:10.1099/vir.0.054692-0

Cited by 45 publications

(39 citation statements)

References 56 publications

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“…H3N2 viruses generated by reverse genetics that contained either Trp-222 or Leu-222 were observed to have similarly small differences in receptor binding properties to those reported here, which led to the suggestion that this amino acid substitution could facilitate infection of dogs (23).…”

Section: Significancementioning

confidence: 80%

Recent evolution of equine influenza and the origin of canine influenza

Collins¹,

Vachieri²,

Haire³

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Significance Equine influenza viruses of the H3N8 subtype have caused outbreaks of respiratory disease in horses throughout the world since their discovery in 1963 in Florida. In 2004 an equine virus in circulation was transmitted to dogs and subsequently spread throughout the United States and to Europe. Comparative analyses of the structures of hemagglutinin glycoproteins of equine and canine viruses by X-ray crystallography locate the sites of variation on the molecules, indicate a role in determining binding specificity for an amino acid sequence difference in the receptor binding site, and describe a unique structural difference in the membrane fusion region in recent equine and canine virus HAs by comparison with all other known HAs. These differences are proposed to have facilitated cross-species transfer.

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Section: Significancementioning

confidence: 80%

Recent evolution of equine influenza and the origin of canine influenza

Collins¹,

Vachieri²,

Haire³

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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“…The W222L mutation is located in the sialic acid receptor binding pocket, and studies have shown that HA mutations in the 220 loop can alter binding to ␣2-3-and ␣2-6-linked sialic acids (35,49,63). There is also evidence that the W222L mutation in CIV H3N2 allowed the virus to infect dogs more efficiently (64), and so the species jump and subsequent adaptation of EIV H3N8 in dogs may have been mediated by changes in receptor recognition as well. However, no infectivity differences were seen between the viruses (or the reassortants) when those were inoculated into CHO or into 6H4 cells.…”

Section: Discussionmentioning

confidence: 99%

Equine and Canine Influenza H3N8 Viruses Show Minimal Biological Differences Despite Phylogenetic Divergence

Feng

Gonzalez

Deng

et al. 2015

J Virol

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The A/H3N8 canine influenza virus (CIV) emerged from A/H3N8 equine influenza virus (EIV) around the year 2000 through the transfer of a single virus from horses to dogs. We defined and compared the biological properties of EIV and CIV by examining their genetic variation, infection, and growth in different cell cultures, receptor specificity, hemagglutinin (HA) cleavage, and infection and growth in horse and dog tracheal explant cultures. Comparison of sequences of viruses from horses and dogs revealed mutations that may be linked to host adaptation and tropism. We prepared infectious clones of representative EIV and CIV strains that were similar to the consensus sequences of viruses from each host. The rescued viruses, including HA and neuraminidase (NA) double reassortants, exhibited similar degrees of long-term growth in MDCK cells. Different host cells showed various levels of susceptibility to infection, but no differences in infectivity were seen when comparing viruses. All viruses preferred ␣2-3-over ␣2-6-linked sialic acids for infections, and glycan microarray analysis showed that EIV and CIV HA-Fc fusion proteins bound only to ␣2-3-linked sialic acids. Cleavage assays showed that EIV and CIV HA proteins required trypsin for efficient cleavage, and no differences in cleavage efficiency were seen. Inoculation of the viruses into tracheal explants revealed similar levels of infection and replication by each virus in dog trachea, although EIV was more infectious in horse trachea than CIV. IMPORTANCEInfluenza A viruses can cross species barriers and cause severe disease in their new hosts. Infections with highly pathogenic avian H5N1 virus and, more recently, avian H7N9 virus have resulted in high rates of lethality in humans. Unfortunately, our current understanding of how influenza viruses jump species barriers is limited. Our aim was to provide an overview and biological characterization of H3N8 equine and canine influenza viruses using various experimental approaches, since the canine virus emerged from horses approximately 15 years ago. We showed that although there were numerous genetic differences between the equine and canine viruses, this variation did not result in dramatic biological differences between the viruses from the two hosts, and the viruses appeared phenotypically equivalent in most assays we conducted. These findings suggest that the crossspecies transmission and adaptation of influenza viruses may be mediated by subtle changes in virus biology. Influenza A viruses are maintained in aquatic birds as intestinal infections, occasionally transfer to and become established as respiratory infections in mammals, including humans, and sometimes spread from one mammal to another (1, 2). Mammalian hosts that have been commonly seen to maintain avian-derived viruses include swine, horses, humans, mink, seals, and, recently, dogs (2-5). Host transfers between different birds, from birds to mammals, or between different mammalian hosts are relatively common but mostly result in single infe...

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“…The vicinal Leu222 in the seal11 HA, however, is a Trp in avian and equine A(H3N8) viruses, as well as early human A(H3N2) virus. Interestingly, Leu222 is present in canine A(H3N8) viruses and has been implicated in the adaptation of the equine viruses to a canine host (63,64), and thus, it may be similarly important in A(H3N8) virus adaptation to seals.…”

Section: Resultsmentioning

confidence: 99%

Structural and Functional Analysis of Surface Proteins from an A(H3N8) Influenza Virus Isolated from New England Harbor Seals

Yang

Nguyen

Carney

et al. 2015

J Virol

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In late 2011, an A(H3N8) influenza virus infection resulted in the deaths IMPORTANCECross-species transmission of zoonotic influenza viruses increases public health concerns. Here, we report a molecular and structural study of the major surface proteins from an A(H3N8) influenza virus isolated from New England harbor seals. The results improve our understanding of these viruses as they evolve and provide important information to aid ongoing risk assessment analyses as these zoonotic influenza viruses continue to circulate and adapt to new hosts. Influenza A viruses (IAVs) are classified into subtypes according to the serological reactivity of their surface glycoproteins, hemagglutinin (HA) and neuraminidase (NA) (1, 2). While 16 HA (H1 to H16) and 9 NA (N1 to N9) subtypes have been identified in wild aquatic birds in the last 100 years, only 3 have adapted to the human population, resulting in four pandemics: H1N1 in 1918 and 2009, H2N2 in 1957, and H3N2 in 1968 (3-6). Although aquatic birds are believed to be the natural reservoir for influenza viruses (7), two novel subtypes of influenza A viruses, H17N10 and H18N11, were recently described in New World bats, which thus may be an alternate reservoir of influenza viruses in nature (8,9).Since the first isolation of H1N1 IAV in swine (10) and the subsequent observation that ferrets were susceptible to IAV (11), it became evident that multiple IAV subtypes of either avian or human descent can infect a number of mammalian species (1). Indeed, over the last decade, the perception and impact of influenza virus infections in animals have changed dramatically as a result of a number of recent outbreaks in poultry involving viruses from the H5, H7, and H9 subtypes that resulted in Ͼ1,000 human infections, as well as the swine origin of the recent A(H1N1)pdm09 pandemic virus (4,(12)(13)(14). This has prompted some governments to invest heavily in global surveillance, research, and capacity building. Public health officials now have a keen interest in all IAVs, but particularly in whether animals, such as pigs, that are closely associated with humans can represent a possible pathway for increased interspecies virus adaptation and transmission.Similar to the infection of pigs, IAV (i.e., H7N7, H4N5, H3N3, H13N2, H13N9, and H4N6 subtypes) and influenza B virus infections have been detected in marine mammals, including seals, whales, and sea otters (15)(16)(17)(18)(19)(20)(21)(22). In November 2011, a marine mammal "unusual mortality event" was declared for Maine, New Hampshire, and northern Massachusetts in response to a large number of deaths in the New England harbor seal population. Sequence analysis revealed that an avian-like H3N8 influenza A virus, A/harbor seal/Massachusetts/1/2011 (seal11), was the cause of the outbreak (23). Although A(H3N8), usually found in avian, canine, equine, and swine hosts (24-27), had been isolated from a seal prior to this event (28), the high mortality observed increased interest from public health officials.Here, we focus our...

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Mutation tryptophan to leucine at position 222 of haemagglutinin could facilitate H3N2 influenza A virus infection in dogs

Cited by 45 publications

References 56 publications

Recent evolution of equine influenza and the origin of canine influenza

Recent evolution of equine influenza and the origin of canine influenza

Equine and Canine Influenza H3N8 Viruses Show Minimal Biological Differences Despite Phylogenetic Divergence

Structural and Functional Analysis of Surface Proteins from an A(H3N8) Influenza Virus Isolated from New England Harbor Seals

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