Porotto Matteo, Murrell Matthew, Greengard Olga, Moscona Anne
Department of Pediatrics, Mount Sinai School of Medicine, New York, New York 10029, USA.
J Virol. 2003 Mar;77(6):3647-54. doi: 10.1128/jvi.77.6.3647-3654.2003.
For human parainfluenza virus type 3 and many other paramyxoviruses, membrane fusion mediated by the fusion protein (F) has a stringent requirement for the presence of the homotypic hemagglutinin-neuraminidase protein (HN). With the goal of gaining further insight into the role of HN in the fusion process, we developed a simple method for quantitative comparison of the ability of wild-type and variant HNs to activate F. In this method, HN/F-coexpressing cells with red blood cells (RBC) bound to them at 4 degrees C are transferred to 22 degrees C, and at different times after transfer 4-guanidino-neu5Ac2en (4-GU-DANA) is added; this inhibitor of the HN-receptor interaction then releases all reversibly bound RBC but not those in which F insertion in the target membrane or fusion has occurred. Thus, the amount of irreversibly bound (nonreleased) RBC provides a measure of F activation, and the use of fluorescently labeled RBC permits microscopic assessment of the extent to which F insertion has progressed to fusion. We studied two neuraminidase-deficient HN variants, C28a, which has two mutations, P111S and D216N, and C28, which possesses the D216N mutation only. C28a but not C28 exhibits a slow fusion phenotype, although determination of the HNs' receptor-binding avidity (with our sensitive method, employing RBC with different degrees of receptor depletion) showed that the receptor-binding avidity of C28a or C28 HN was not lower than that of the wild type. The F activation assay, however, revealed fusion-triggering defects in C28a HN. After 10 and also 20 min at 22 degrees C, irreversible RBC binding was significantly less for cells coexpressing wild-type F with C28a HN than for cells coexpressing wild-type F with wild-type HN. In addition, F insertion progressed to fusion more slowly in the case of C28a HN-expressing cells than of wild-type HN-expressing cells. Identical defects were found for P111S HN, whereas for C28 HN, representing the 216 mutation of C28a, F activation and fusion were as rapid as for wild-type HN. The diminished fusion promotion capacity of C28a HN is therefore attributable to P111S, a mutation in the stalk region of the molecule that causes no decrease in receptor-binding avidity. C28a HN is the first parainfluenza virus variant found so far to be specifically defective in HN's F-triggering and fusion promotion functions and may contribute to our understanding of transmission of the activating signal from HN to F.
对于人副流感病毒3型及许多其他副粘病毒而言,融合蛋白(F)介导的膜融合对同型血凝素神经氨酸酶蛋白(HN)的存在有严格要求。为了进一步深入了解HN在融合过程中的作用,我们开发了一种简单方法,用于定量比较野生型和变异型HN激活F的能力。在该方法中,将在4℃时结合有红细胞(RBC)的HN/F共表达细胞转移至22℃,并在转移后的不同时间加入4-胍基-neu5Ac2en(4-GU-DANA);这种HN-受体相互作用的抑制剂随后会释放所有可逆结合的RBC,但不会释放那些F已插入靶膜或已发生融合的RBC。因此,不可逆结合(未释放)的RBC数量可衡量F的激活程度,使用荧光标记的RBC可在显微镜下评估F插入进展到融合的程度。我们研究了两种神经氨酸酶缺陷的HN变异体,C28a有两个突变,即P111S和D216N,而C28仅具有D216N突变。C28a表现出缓慢融合表型,而C28则没有,尽管通过我们的灵敏方法(使用不同程度受体耗竭的RBC)测定HN的受体结合亲和力表明,C28a或C28 HN的受体结合亲和力并不低于野生型。然而,F激活试验揭示了C28a HN存在融合触发缺陷。在22℃下孵育10分钟和20分钟后,共表达野生型F与C28a HN的细胞中不可逆RBC结合明显少于共表达野生型F与野生型HN的细胞。此外,表达C28a HN的细胞中F插入进展到融合的速度比表达野生型HN的细胞慢。对于P111S HN也发现了相同的缺陷,而对于代表C28a的216突变的C28 HN,F激活和融合与野生型HN一样迅速。因此,C28a HN融合促进能力的降低归因于P111S,这是分子茎区的一个突变,不会导致受体结合亲和力降低。C28a HN是迄今为止发现的首个在HN的F触发和融合促进功能方面存在特异性缺陷的副流感病毒变异体,可能有助于我们理解从HN到F的激活信号传递。