Lakdawala Seema S, Jayaraman Akila, Halpin Rebecca A, Lamirande Elaine W, Shih Angela R, Stockwell Timothy B, Lin Xudong, Simenauer Ari, Hanson Christopher T, Vogel Leatrice, Paskel Myeisha, Minai Mahnaz, Moore Ian, Orandle Marlene, Das Suman R, Wentworth David E, Sasisekharan Ram, Subbarao Kanta
Laboratory of infectious Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland 20892, USA.
Department of Biological Engineering, Koch Institute for Integrative Cancer Research, Singapore-MIT Alliance for Research and Technology, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA.
Nature. 2015 Oct 1;526(7571):122-5. doi: 10.1038/nature15379. Epub 2015 Sep 23.
Influenza A viruses pose a major public health threat by causing seasonal epidemics and sporadic pandemics. Their epidemiological success relies on airborne transmission from person to person; however, the viral properties governing airborne transmission of influenza A viruses are complex. Influenza A virus infection is mediated via binding of the viral haemagglutinin (HA) to terminally attached α2,3 or α2,6 sialic acids on cell surface glycoproteins. Human influenza A viruses preferentially bind α2,6-linked sialic acids whereas avian influenza A viruses bind α2,3-linked sialic acids on complex glycans on airway epithelial cells. Historically, influenza A viruses with preferential association with α2,3-linked sialic acids have not been transmitted efficiently by the airborne route in ferrets. Here we observe efficient airborne transmission of a 2009 pandemic H1N1 (H1N1pdm) virus (A/California/07/2009) engineered to preferentially bind α2,3-linked sialic acids. Airborne transmission was associated with rapid selection of virus with a change at a single HA site that conferred binding to long-chain α2,6-linked sialic acids, without loss of α2,3-linked sialic acid binding. The transmissible virus emerged in experimentally infected ferrets within 24 hours after infection and was remarkably enriched in the soft palate, where long-chain α2,6-linked sialic acids predominate on the nasopharyngeal surface. Notably, presence of long-chain α2,6-linked sialic acids is conserved in ferret, pig and human soft palate. Using a loss-of-function approach with this one virus, we demonstrate that the ferret soft palate, a tissue not normally sampled in animal models of influenza, rapidly selects for transmissible influenza A viruses with human receptor (α2,6-linked sialic acids) preference.
甲型流感病毒通过引发季节性流行和偶发性大流行对公众健康构成重大威胁。它们在流行病学上的成功依赖于人际间的空气传播;然而,控制甲型流感病毒空气传播的病毒特性十分复杂。甲型流感病毒感染是通过病毒血凝素(HA)与细胞表面糖蛋白末端连接的α2,3或α2,6唾液酸结合来介导的。人类甲型流感病毒优先结合α2,6连接的唾液酸,而禽流感病毒则结合气道上皮细胞复合聚糖上的α2,3连接的唾液酸。从历史上看,优先与α2,3连接的唾液酸结合的甲型流感病毒在雪貂中不能通过空气传播途径有效传播。在此,我们观察到一种经过基因工程改造以优先结合α2,3连接的唾液酸的2009年大流行H1N1(H1N1pdm)病毒(A/California/07/2009)实现了高效的空气传播。空气传播与病毒在单个HA位点发生变化从而获得与长链α2,6连接的唾液酸结合能力的快速选择相关,而不会丧失与α2,3连接的唾液酸的结合能力。可传播的病毒在感染后24小时内在实验感染的雪貂体内出现,并在软腭中显著富集,在鼻咽表面长链α2,6连接的唾液酸占主导地位。值得注意的是,雪貂、猪和人类的软腭中都存在长链α2,6连接的唾液酸。使用针对这一种病毒的功能丧失方法,我们证明,雪貂的软腭,一种在流感动物模型中通常不进行采样的组织,会迅速选择具有人类受体(α2,6连接的唾液酸)偏好的可传播甲型流感病毒。