Kuss Sharon K, Etheredge Chris A, Pfeiffer Julie K
Department of Microbiology, University of Texas Southwestern Medical Center, Dallas, Texas, United States of America.
PLoS Pathog. 2008 Jun 6;4(6):e1000082. doi: 10.1371/journal.ppat.1000082.
RNA viruses such as poliovirus have high mutation rates, and a diverse viral population is likely required for full virulence. We previously identified limitations on poliovirus spread after peripheral injection of mice expressing the human poliovirus receptor (PVR), and we hypothesized that the host interferon response may contribute to the viral bottlenecks. Here, we examined poliovirus population bottlenecks in PVR mice and in PVR mice that lack the interferon alpha/beta receptor (PVR-IFNAR-/-), an important component of innate immunity. To monitor population dynamics, we developed a pool of ten marked polioviruses discriminated by a novel hybridization-based assay. Following intramuscular or intraperitoneal injection of the ten-virus pool, a major bottleneck was observed during transit to the brain in PVR mice, but was absent in PVR-IFNAR-/- mice, suggesting that the interferon response was a determinant of the peripheral site-to-brain bottleneck. Since poliovirus infects humans by the fecal-oral route, we tested whether bottlenecks exist after oral inoculation of PVR-IFNAR-/- mice. Despite the lack of a bottleneck following peripheral injection of PVR-IFNAR-/- mice, we identified major bottlenecks in orally inoculated animals, suggesting physical barriers may contribute to the oral bottlenecks. Interestingly, two of the three major bottlenecks we identified were partially overcome by pre-treating mice with dextran sulfate sodium, which damages the colonic epithelium. Overall, we found that viral trafficking from the gut to other body sites, including the CNS, is a very dynamic, stochastic process. We propose that multiple host barriers and the resulting limited poliovirus population diversity may help explain the rare occurrence of viral CNS invasion and paralytic poliomyelitis. These natural host barriers are likely to play a role in limiting the spread of many microbes.
脊髓灰质炎病毒等RNA病毒具有很高的突变率,可能需要多样化的病毒群体才能具备完全的毒力。我们之前发现,在对表达人脊髓灰质炎病毒受体(PVR)的小鼠进行外周注射后,脊髓灰质炎病毒的传播存在限制,我们推测宿主的干扰素反应可能导致了病毒瓶颈。在此,我们研究了PVR小鼠以及缺乏干扰素α/β受体(PVR-IFNAR-/-)的PVR小鼠体内的脊髓灰质炎病毒群体瓶颈,干扰素α/β受体是先天免疫的一个重要组成部分。为了监测群体动态,我们构建了一组由十种通过基于杂交的新型检测方法区分的标记脊髓灰质炎病毒。在对这十种病毒混合液进行肌肉注射或腹腔注射后,在PVR小鼠向脑部传播的过程中观察到一个主要瓶颈,但在PVR-IFNAR-/-小鼠中不存在,这表明干扰素反应是外周部位到脑部瓶颈的一个决定因素。由于脊髓灰质炎病毒通过粪-口途径感染人类,我们测试了对PVR-IFNAR-/-小鼠进行口服接种后是否存在瓶颈。尽管对PVR-IFNAR-/-小鼠进行外周注射后不存在瓶颈,但我们在口服接种的动物中发现了主要瓶颈,这表明物理屏障可能导致了口服瓶颈。有趣的是,我们发现的三个主要瓶颈中的两个可以通过用硫酸葡聚糖钠预处理小鼠来部分克服,硫酸葡聚糖钠会损伤结肠上皮。总体而言,我们发现病毒从肠道向包括中枢神经系统在内的其他身体部位的传播是一个非常动态、随机的过程。我们提出,多种宿主屏障以及由此导致的脊髓灰质炎病毒群体多样性有限,可能有助于解释病毒中枢神经系统入侵和麻痹性脊髓灰质炎罕见发生的原因。这些天然宿主屏障可能在限制许多微生物的传播中发挥作用。