Characterization of the Pathogenesis of H10N3, H10N7, and H10N8 Subtype Avian Influenza Viruses Circulating in Ducks

Zhang, Miaomiao; Zhang, Xingxing; Xu, K.; Teng, Quincy; Liu, Qinfang; Li, Xuesong; Yang, Jianmei; Xu, Jianqing; Chen, Hongjun; Zhang, Xiaoyan; Li, Zejun

doi:10.1038/srep34489

Cited by 15 publications

(17 citation statements)

References 53 publications

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“…By comparison, H10N8 strains are relatively rare, circulating predominantly in wild aquatic birds, though also somewhat in poultry, and largely isolated to mainland China ( 129 , 130 ). Similar to H6N1, H10N8 infections in humans are extremely rare, with only three confirmed cases to date; however, two of these resulted in fatal disease ( 111 , 131 ).…”

Section: Receptor Specificity Of Avian Influenza Viruses That Cause Smentioning

confidence: 99%

Adaptation of influenza viruses to human airway receptors

Thompson

Paulson

2021

Journal of Biological Chemistry

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Through annual epidemics and global pandemics, influenza A viruses (IAVs) remain a significant threat to human health as the leading cause of severe respiratory disease. Within the last century, four global pandemics have resulted from the introduction of novel IAVs into humans, with components of each originating from avian viruses. IAVs infect many avian species wherein they maintain a diverse natural reservoir, posing a risk to humans through the occasional emergence of novel strains with enhanced zoonotic potential. One natural barrier for transmission of avian IAVs into humans is the specificity of the receptor-binding protein, hemagglutinin (HA), that recognizes sialic acid-containing glycans on host cells. HAs from human IAVs exhibit “human-type” receptor specificity, binding exclusively to glycans on cells lining the human airway where terminal sialic acids are attached in the α2-6 configuration (NeuAcα2-6Gal). In contrast, HAs from avian viruses exhibit specificity for “avian-type” α2-3-linked (NeuAcα2-3Gal) receptors, and thus require adaptive mutations to bind human-type receptors. Since all human IAV pandemics can be traced to avian origins, there remains ever-present concern over emerging IAVs with human-adaptive potential that might lead to the next pandemic. This concern has been brought into focus through emergence of SARS-CoV-2, aligning both scientific and public attention to the threat of novel respiratory viruses from animal sources. In this review we summarize receptor-binding adaptations underlying the emergence of all prior IAV pandemics in humans, maintenance and evolution of human-type receptor specificity in subsequent seasonal IAVs, and potential for future human-type receptor adaptation in novel avian HAs.

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Section: Receptor Specificity Of Avian Influenza Viruses That Cause Smentioning

confidence: 99%

Adaptation of influenza viruses to human airway receptors

Thompson

Paulson

2021

Journal of Biological Chemistry

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“…Interestingly, a few natural non-H5/H7 viruses also fulfill the criteria of HPAIV. Several H10Nx viruses with monobasic CS exhibit an intravenous pathogenicity index (IVPI) higher than 1.2 resembling the HPAIV H5/H7 [14][15][16]. Moreover, in August 2012, an H4N2 virus was isolated from quails in California that possessed the polybasic CS motif 322 PEKRRTR/G 329 [17].…”

Section: Introductionmentioning

confidence: 99%

Insertion of Basic Amino Acids in the Hemagglutinin Cleavage Site of H4N2 Avian Influenza Virus (AIV)—Reduced Virus Fitness in Chickens is Restored by Reassortment with Highly Pathogenic H5N1 AIV

Gischke

Ulrich

Fatola

et al. 2020

IJMS

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Highly pathogenic (HP) avian influenza viruses (AIVs) are naturally restricted to H5 and H7 subtypes with a polybasic cleavage site (CS) in hemagglutinin (HA) and any AIV with an intravenous pathogenicity index (IVPI) ≥ 1.2. Although only a few non-H5/H7 viruses fulfill the criteria of HPAIV; it remains unclear why these viruses did not spread in domestic birds. In 2012, a unique H4N2 virus with a polybasic CS 322PEKRRTR/G329 was isolated from quails in California which, however, was avirulent in chickens. This is the only known non-H5/H7 virus with four basic amino acids in the HACS. Here, we investigated the virulence of this virus in chickens after expansion of the polybasic CS by substitution of T327R (322PEKRRRR/G329) or T327K (322PEKRRKR/G329) with or without reassortment with HPAIV H5N1 and H7N7. The impact of single mutations or reassortment on virus fitness in vitro and in vivo was studied. Efficient cell culture replication of T327R/K carrying H4N2 viruses increased by treatment with trypsin, particularly in MDCK cells, and reassortment with HPAIV H5N1. Replication, virus excretion and bird-to-bird transmission of H4N2 was remarkably compromised by the CS mutations, but restored after reassortment with HPAIV H5N1, although not with HPAIV H7N7. Viruses carrying the H4-HA with or without R327 or K327 mutations and the other seven gene segments from HPAIV H5N1 exhibited high virulence and efficient transmission in chickens. Together, increasing the number of basic amino acids in the H4N2 HACS was detrimental for viral fitness particularly in vivo but compensated by reassortment with HPAIV H5N1. This may explain the absence of non-H5/H7 HPAIV in poultry.

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“…These viruses caused lethal infections in poultry and were defined as highly pathogenic (HP) using the intravenous pathogenicity index (IVPI), despite the absence of a polybasic cleavage site in the HA (13,14). In 2007 and in 2009 and 2010, additional H10 viruses were isolated in Italy and China that also fulfilled these criteria (15,16). Pathogenesis studies with the isolate from 2007 determined that lethality and virulence in poultry were the result of high levels of viral replication in the kidneys (15), a pattern that was quite distinct from that of the multisystem hemorrhagic disease seen with H5 and H7 HP avian influenza viruses.…”

mentioning

confidence: 99%

Evaluation of the Biological Properties and Cross-Reactive Antibody Response to H10 Influenza Viruses in Ferrets

Sutton

Lamirande

Czakó

et al. 2017

J Virol

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The recent outbreak of avian origin H10N7 influenza among seals in Northern Europe, and two fatal human infections with an avian H10N8 virus in China, have demonstrated that H10 viruses can spread between mammals and cause severe disease in humans. To gain insight into the potential for H10 viruses to cross the species barrier and identify a candidate vaccine strain, we evaluated the in vitro and in vivo properties and antibody response in ferrets to 20 diverse H10 viruses. H10 virus infection of ferrets caused variable weight loss and all 20 viruses replicated throughout the respiratory tract; however, replication in the lungs was highly variable. In glycan-binding assays, the H10 viruses preferentially bound "avian-like" α2,3-linked sialic acids. Importantly, several isolates also displayed strong binding to long-chain "human-like" α2,6-linked sialic acids, and exhibited comparable or elevated neuraminidase activity relative to human H1N1, H2N2, and H3N2 viruses. In hemagglutination inhibition assays, 12 antisera cross-reacted with ≥ 14 of 20 H10 viruses, and 7 viruses induced neutralizing activity against ≥ 15 of the 20 viruses. By combining data on weight loss, viral replication, and the cross-reactive antibody response, we identified A/mallard/Portugal/79906/2009 (H10N7) as a suitable virus for vaccine development. Collectively, our findings suggest that H10 viruses may continue to sporadically infect humans and other mammals, underscoring the importance of developing an H10 vaccine for pandemic preparedness. Avian origin H10 influenza viruses sporadically infect humans and other mammals; however, little is known about viruses of this subtype. Thus, we characterized the biological properties of 20 H10 viruses in vitro and in ferrets. Infection caused mild to moderate weight loss (5-15%), with robust viral replication in the nasal tissues and variable replication in the lung. H10 viruses preferentially bind "avian-like" sialic acids, although several isolates also displayed binding to "human-like" sialic acid receptors. This is consistent with the ability of H10 viruses to cross the species barrier, and warrants selection of an H10 vaccine strain. By evaluating the cross-reactive antibody response to the H10 viruses, and combining this analysis with viral replication and weight loss findings, we identified A/mallard/Portugal/79906/2009 (H10N7) as a suitable H10 vaccine strain.

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Characterization of the Pathogenesis of H10N3, H10N7, and H10N8 Subtype Avian Influenza Viruses Circulating in Ducks

Cited by 15 publications

References 53 publications

Adaptation of influenza viruses to human airway receptors

Adaptation of influenza viruses to human airway receptors

Insertion of Basic Amino Acids in the Hemagglutinin Cleavage Site of H4N2 Avian Influenza Virus (AIV)—Reduced Virus Fitness in Chickens is Restored by Reassortment with Highly Pathogenic H5N1 AIV

Evaluation of the Biological Properties and Cross-Reactive Antibody Response to H10 Influenza Viruses in Ferrets

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