杯状病毒分子流行病学及病原与宿主互作机制研究
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摘要
杯状病毒科(Caliciviridae)包含4个属,分别为:诺如病毒(Norovirus,NoV)、札幌病毒(Sapovirus,SaV)、囊病毒(Vesivirus)及兔出血热病毒(Lagovirus)。属单股正链RNA病毒,直径约27-40nm,无包膜,衣壳呈二十面体对称结构。杯状病毒科中NoV和SaV为主要的医学病原,均能引发急性胃肠炎;而囊病毒和兔出血热病毒为动物源性病原,其中的猫杯状病毒和兔出血热病毒分别引发猫呼吸系统疾病和兔的致命性出血性疾病。
NoV是导致人急性肠胃炎的最主要的非细菌性感染源之一,经常导致家庭和社区性的爆发流行;而SaV致病性较弱,感染率较低,主要感染对象为婴幼儿。除了人群,NoV和SaV也在猪、鼠、水貂等多种动物里被检测到,这也引发了二者是否均为人畜共患病病原的讨论。
杯状病毒的研究起步较晚,虽然已经取得了很大的进展,但还存在很多问题有待解决。
1中国人及猪杯状病毒分子生物学研究
我国人杯状病毒的研究起步较晚,1995年才首次开始研究,实际上,在我国大部分地区都存在该病毒的感染和发病,过去由于未列入常规检测项目或报告项目,对该病毒感染和发病的状况不甚了解。因此有必要对我国的人杯状病毒分子流行病学情况进行系统研究。
除了流行病学特性,对我国诺如病毒的分子生物学特征,例如病毒的全基因结构、重组和进化等方面还知之甚少。另外,我国动物群体中特别是跟人类关系密切的猪群中的杯状病毒的流行情况等基本处于空白。而越来越多的证据显示,杯状病毒存在着跨种间传播的风险。因此,动物源杯状病毒的研究对人杯状病毒的防控,预警机制建立等都具有重要意义。目前我国对札幌病毒的重视程度不够,流行病学情况、分子生物学特征、致病机制及危害、病毒进化与重组等了解不多,因此,对以上各方面均有必要进行深入研究。
2致病机理与动物模型
目前对杯状病毒的研究主要集中于流行病学研究,对病毒的感染、致病机制,物种与组织嗜性,靶细胞受体,在细胞内的复制过程等基础研究相对较少。由于杯状病毒除极个别毒株外一般都难以体外培养,极大地制约了相关研究的进展。而动物模型是研究致病机理的有效手段之一。因此,采用动物模型模拟疾病的发生对杯状病毒感染、致病机制乃至跨种间传播预测等具有重要意义。
3 SaV的受体研究
病毒受体是公认的引发病毒感染宿主细胞的主要决定因素,也是影响病毒宿主特异性和组织亲嗜性的决定因素之一。因此,鉴定SaV受体及其特性与功能,对于从分子水平阐明病毒感染与免疫的机制,深刻理解病毒与宿主细胞的相互关系,病毒的跨种间感染风险预测,疫苗、诊断试剂的研制等,都具有重大的理论与实践意义。有研究显示,人诺如病毒的受体可能为人类血型组织抗原(histo-blood group antigens,HBGA)。为鉴定SaV的受体是否也为HBGA,Jiang等采用杆状病毒表达系统表达了人源SaV的病毒样颗粒,并测试了它们之间的结合能力。结果发现这些病毒样颗粒不能与HBGA结合,从而排除了HBGA作为SaV受体的可能性。目前,札幌病毒的受体依然未知。
有鉴于此,本研究主要从杯状病毒的分子流行病学、动物模型建立、病毒样颗粒的表达、病毒与宿主细胞的互作机制等方面开展研究,
结果如下:
一杯状病毒的分子流行病学研究
1中国大陆发现猪SaV导致仔猪腹泻
2008年2月上海郊区某规模化生猪养殖场发生仔猪腹泻,两窝仔猪中7只仔猪发生,剩余12只仔猪正常。采集上述腹泻粪便样品和正常仔猪粪便样品,同时从该猪场和邻近猪场分别采集正常粪便标本20和80份。根据腹泻仔猪症状和粪便外观观察,初步排除常见细菌性腹泻可能。通过PCR或RT-PCR检测了PCV、PRC、TGEV、PEDV、猪NoV和猪SaV等常见或者新发的能够导致仔猪腹泻的病毒。结果显示,除SaV为,其它病毒均为阴性。为证实仔猪腹泻是否由SaV感染引起,我们进行了动物回归实验。动物实验结果表明,猪SaV病毒阳性粪便悬液能够导致仔猪腹泻和呕吐,并且能够在实验组仔猪的粪便样品中持续检测到病毒。
2华东地区猪杯状病毒分子流行病学研究
到目前为止,各国猪群中尚无关于杯状病毒的系统性研究。为研究猪群中杯状病毒的感染情况,本实验从中国华东地区(上海、江苏、安徽)采集猪新鲜粪便样品,进行分子流行病学检测和分子系统进化分析,并对不同月龄的感染率进行统计分析。结果显示,中国猪群中存在上述两种病毒的感染,SaV和NoV的感染率分别为0.9%(8/904)和0.2%(2/904)。序列分析显示,猪SaV分离株均属GIII,并可进一步分为两个遗传簇。它们分别与荷兰和韩国的猪SaV分离株同源性最近,这暗示,它们可能分别与这两个毒株有着相同的遗传起源。统计结果显示,小于1月龄的仔猪的感染率显著高于1月龄以上的猪的感染率(P<0.05)。本研究表明,中国华东地区猪群中存在猪NoV的感染,但感染率很低,并非该地区的主要病毒性感染源。
3贵州地区猪杯状病毒和戊型肝炎病毒分子流行病学研究
为研究我国西南地区的杯状病毒和戊型肝炎病毒(HEV)的分子流行情况,2009年5-6月,从贵州省6个规模化生猪养殖场随机采集猪新鲜粪便样品209份,用RT-PCR方法进行上述病毒的检测和分子进化分析。HEV和SaV的猪场阳性率分别为83%(5/6)和33%(2/6),未检测到NoV。另外,未发现HEV和SaV共感染。HEV和猪SaV的总体阳性率分别为6.7%(15/209)和1.0% (2/209)。进化分析结果显示,这10株HEV毒株均为G4。它们之间的核酸同源性为90%-99%,与邻近省份广西的一株人HEV分离株(AF103940)聚为一支,同源性为92%-%94%。两株SaV均为GIII,它们之间的核酸同源性为96%,与一支巴西分离株同源性最高(91%),与中国华东地区的分离株(FJ374683)同源性只有82%-84%。这表明,尽管感染率较低,但贵州地区的猪群中存在猪SaV的感染。
4中国猪SaV代表毒株全基因组分析
研究显示有些毒株(如Sapovirus pig/43/06-18p3/06/ITA)在序列上与人的SaV毒株非常接近,这提示猪SaV有可能是人SaV感染的病原之一。为研究中国猪SaV毒株的分子生物学特征,对首支中国分离株进行了全基因组克隆与分析。结果表明,该毒株(Ch-sw-sav1)基因组序列不含3′poly(A)结构全长为7541 nt, A、C、G、U的所占的比重分别为19%、14.3%、33.3%和33.3%。5′末端含有典型的GTG结构。ORF1含有6765 nt(2255aa),编码非结构蛋白和外壳蛋白VP1(544aa)。ORF2长度为516 nt,编码172 aa的小的外壳蛋白VP2(图1A)。ORF1编码的多聚蛋白包括2C解螺旋酶(2C helicase,GPPGIGKT),3C蛋白酶(3C protease,GDCG),RdRp(GLPSG和YGDD),这些非结构蛋白在所有杯状病毒中均高度保守。在VP1区中同样含有PPG模块。基于全基因组序列的分析显示,本毒株属于GIII SaV。基于ORF2 3′末端的对比结果显示,本分离株含有一个21 nt插入片段。
5上海地区门诊儿童的人杯状病毒感染情况调查及基因重组分析
本研究从上海某三甲医院采集门诊儿童粪便样品452份,用RT-PCR方法检测人杯状病毒的感染情况,并对阳性毒株进行系统进化分析。选取代表性毒株进行全基因组克隆,用相关软件进行系统进化和重组分析。452份儿童粪便样品中有20份呈NoV RNA阳性,总体阳性率为4.4%,无SaV阳性粪样检出。20份NoV阳性样品的PCR产物的测序结果显示20个毒株中19株序列彼此不完全相同。它们之间的同源性为79.5%-98.8%。进化分析显示,这19株序列均为GII,并聚集为3个遗传簇(clusters)。其中两个遗传簇为GII-4,另外一个为GII-3。为分析这些毒株的分子特征,从3个遗传簇中分别选取一个代表性毒株进行全基因组克隆和基因重组分析。结果证明,HU/GII/SHANGHAI/SH312/2008/CHN毒株为重组毒株。
二猪SaV小型猪感染模型的建立
本研究采用分离的猪SaV中国株Ch-sw-sav1为攻毒株,通过口服感染SPF级巴马小型猪,通过收集感染后临床症状、病理变化的相关信息以及各组织器官中病原的RT-PCR检测,掌握猪SaV感染猪的第一手资料,为疾病感染机制的研究奠定了基础。结果显示,攻毒后第二天实验组猪即出现不同程度腹泻,个别猪出现呕吐现象。剖检结果显示,实验组猪出现腹胀、小肠出血现象。病理切片的光镜检测结果表明:小肠绒毛萎缩、脱落;透射电镜显微观测表明:小肠上皮细胞细胞核或线粒体病变。间接免疫荧光显示,在小肠各段能检测到病毒抗原的存在。血常规检测结果显示,与对照组和空白组相比,实验组猪在攻毒后白细胞上升,第14天达到最高值,随后开始下降;血小板在攻毒第21天急剧上升,然后缓慢下降;与对照组和空白组相比,实验组猪红细胞没有明显变化。RT-PCR结果显示,实验组猪从攻毒第二天即开始排毒,直至实验结束(PID36)。
三猪SaV靶细胞受体初步研究
1连接黏附分子1作为猪SaV受体的可能性研究
杯状病毒中的NoV和猫杯状病毒(feline calicivirus,FCV)的功能性受体分别为人类血型组织抗原(histo-blood group antigens,HBGAs)和连接黏附分子1(junctional adhesion molecule 1,JAM-1)。已有的研究数据均显示识别碳水化合物可能是杯状病毒的共同特征,尽管在长期的进化过程中不同杯状病毒已适应了不同的宿主细胞。对此,研究人员分别测试了NoV和SaV与HBGAs间的结合能力。结果显示,NoV的VLPs能够与HBGAs结合,而SaV GI和GV的VLPs均不能结合HBGAs。为检验JAM-1作为GIII SaV受体的可能性,我们测试了抗JAM-1多抗对SaV病毒感染易感细胞LLC-PK的阻断效果。在病毒感染细胞前用不同浓度抗JAM-1多抗预先与细胞孵育,随后用荧光定量PCR方法检测不同浓度抗体的孵育能否阻断或者降低病毒对细胞的结合和感染。结果显示,JAM-1抗体不能阻断或者降低SaV对易感细胞LLC-PK的感染。这表明,JAM-1作为SaV感染宿主细胞的受体可能性较低。
2 VOPBA和Co-IP法筛选猪SaV候选受体
本研究拟采用VOPBA法和免疫共沉淀法结合质谱探索猪SaV在易感细胞LLC-PK细胞表面受体;采用上述两种方法共鉴定到若干疑似蛋白。根据这些蛋白的细胞内分布和功能结合文献分析,选取MHC-1(major histocompatibility complex class I)进行进一步验证。CO-IP结果显示,MHC-I能够与病毒结合。
四人NoV病毒样颗粒(Virus-like particles)表达
本研究采用杆状病毒表达载体进行GII-4和GII-12毒株的VLPs表达,并用Western-blot和免疫电镜方法进行抗原性和形态学鉴定;尝试将外壳蛋白VP1和绿色荧光蛋白(EGFP)融合表达,以期得到带有EGFP标记的病毒样颗粒。研究结果显示,所有的重组杆状病毒均能在Sf9细胞中表达。除了与EGFP融合的蛋白不能成功纯化外,其它均能得到合适浓度的重组蛋白。Western-blot和免疫电镜显示,这些蛋白均具有抗原性并能自我组织形成病毒样颗粒,而GII-12的VLPs能够被抗GII-4 VLPs的抗体所识别。
The family Caliciviridae is composed of small (27 to 40 nm), nonenveloped, icosahedral viruses that possess a linear, positive-sense, single-stranded 7 to 8 kb RNA (ssRNA) genome. They are 27-35 nm in diameter. Caliciviruses were classified into 4 genera in 2002 by the International Committee on the Taxonomy of Viruses (ICTV): Norovirus (NoV), Sapovirus (SaV), Vesivirus, and Lagovirus. The major medical pathogens in the family are NoV and SaV, which cause acute gastroenteritis. Important veterinary pathogens include vesiviruses such as feline calicivirus (FCV), which causes a respiratory disease in cats, and lagoviruses such as rabbit hemorrhagic disease virus (RHDV), which causes an often fatal hemorrhagic disease in rabbits. Human caliciviruses include both human NoV and SaV. Human NoV is believed to be one of the major causes of nonbacterial epidemic gastroenteritis, a disease that usually occurs in family or community-wide outbreaks. The impact of the SaV has not been fully established, but to date they do not share a predominant role with the NoV in epidemic gastroenteritis. Researches showed that both NoV and sapoviruses have been associated with gastroenteritis in infants and young children. Although no inter-species recombinant strain has been found, an inter-genogroup human calicivirus recombinant has been described. Additional, sometimes human strains genetically closely related to the animal strains. Specifically, porcine NoV are genetically closely related to some human NoV in the GII. All of these finding suggests a potential zoonotic risk and pig is considered as an animal reservoir for such viruses.
Although some of great progress have been made in the research field of caliciviruses, there are still some unclear points, including (1) The interaction mechanism between caliciviruses and host cells; (2) The replication mechanism of caliciviruses in host cell and animal model; (3) Are caliciviruses zoonotic agents; (4) Pathogenesis of caliciviruses; (5) Recombinants between animal and human caliciviruses; (5) The receptor of SaV. In order to elucidate some points mentioned above, we performed the following researches:
1 Study of molecular epidemiology of caliciviruses
(1) The first Chinese porcine sapovirus strain that contributed to an outbreak of gastroenteritis in piglets
We report the first outbreak of gastroenteritis caused by porcine SaV in piglets in China. This outbreak occurred in February 2008 on a small commercial pig farm that lies in Shanghai suburb. Seven stool specimens were collected from seven piglets which showed symptoms of diarrhea and vomiting in two neighboring farrows on the farm. At the beginning, we first examined the seven specimens from the ill piglets for porcine circovirus, porcine rotavirus, porcine transmissible gastroenteritis virus, and porcine epidemic diarrhea virus using reverse transcription-PCR (RT-PCR), and all specimens showed negative results. All specimens were then examined for SaV by using RT-PCR as described previously. Our results showed that all seven piglets that showed clinical symptoms were positive for SaV RNA, suggesting this outbreak of gastroenteritis may due to porcine SaV infection.
In order to elucidate whether the fecal samples contained infectious SaV, the eight SaV-positive fecal specimens were used to infect piglets. Results indicated that all of those experimental infection piglets showed symptoms of diarrhea and vomiting, and shed virus after inoculation.
(2) Molecular detection and prevalence of porcine caliciviruses in eastern China Caliciviruses that causes diarrhea were reported in both industrial and developing countries including China recent years. Porcine caliciviruses closely related to human sapovirus and norovirus were also detected in swine group, which caused discussions about the animal reservoir and the potential risk for zoonotic transmission to humans. The objective of this work was to determine the frequency and distribution in the different age of swine for porcine sapovirus and norovirus, and characterize the strains prevalent in eastern China. A total of 904 stool samples from different ages of pigs were collected from eastern China from April 2008 to March 2009, and tested for both SaVs and NoVs using reverse transcription-polymerase chain reaction (RT–PCR). Our results indicated that 8 (0.9%) stool samples were positive for SaV and 2 (0.2%) for NoV. Phylogenetic analyses based on the partial RNA polymerase gene sequences indicated that all of the SaV isolates belonged to GIII, while the 2 NoV isolates belonged to GII. The 8 SaV isolates were further divided into 2 different groups in the GIII cluster, one of which clustered closely with the Netherland isolate (AY615804) and the other one with the Chinese strain (EU599212). Our results suggested that SaV infection was more frequently (p <0.01) in 0-1 month age of swine than that of other ages. In conclusion, the present study provided evidence that infection of PoSaV and PoNoV existed in pig groups of eastern China.
(3) Prevalence of porcine caliciviruses and Hepatitis E Virus in pig farms of Guizhou province, China
A total of 209 stool samples from pigs of different age groups were collected from 6 pig farms in Guizhou province from May to June 2009, and tested for HEV, SaV and NoV using reverse transcription-polymerase chain reaction (RT–PCR). The overall prevalence of porcine HEV and porcine SaV were 6.7% (15/209) and 1.0% (2/209), respectively. No NoV infection was detected in the current study. The prevalence rates of porcine HEV infection for different ages of pigs were 15.4% (4/26; piglet, age<1 month), 6.8% (3/44; 4 month1 month), 12.5% (6/48, age≈4 month), and 1.1% (2/91, sow, 146 month), respectively. Porcine SaV was only detected in piglets (7.7%, 2/26). All 10 HEV isolates in the current study belong to genotype 4, clustering with a human HEV strain (AF103940) isolated from an adjacent province.This is the first report that porcine SaV exists in swine groups of Guizhou province, China. The porcine HEV isolates clustering with a human strain suggests the potential cross-species transmission between swine and human in this area.
(4) Molecular characterization and phylogenetic analysis of the complete genome of a porcine sapovirus from Chinese swine The whole genome of Ch-sw-sav1 was amplified by RT-PCR and was sequenced. Sequence alignment of the complete genome or RNA dependent RNA polymerase (RdRp) gene was done. 3′end of ORF2 with 21-nt nucleotide insertion was further analyzed using softwares. Sequence analysis indicated that the genome of Ch-sw-sav1 was 7541 nucleotide long with two ORFs, excluding the 17 nucleotides ploy (A) at the 3′end. Phylogenetic analysis based on part of RdRp gene of this strain showed that it was classified into subgroup GIII. Sequence alignment indicated that there was an inserted 21-nt long nucleotide sequence at the 3′end of ORF2. The insertion showed high antigenicity index comparing to other regions in ORF2.
(5) Prevalence and recombination of NoV in outpatients of Shanghai 452 stool samples from outpatients were collected from Shanghai, China. The fecal samples were tested for human caliciviruses. The full-genome of representative strains were then chosen and determined. Results showed that 20 NoV RNA positive samples were identified and the overall prevalence of NoV was 4.4%. No SaV positive were found in current study. In the present study, three full-length genomes of human NoV from China were determined and the genomic organization and recombination were analyzed. They had similar genome organization and contained three predicted ORFs, though the 5’UTR of those three strains were 2, 4 and 8 nucleotides, respectively. Phylogenetic analysis showed that the HU/GII/SHANGHAI/SH312/2008/CHN strain may be a recombinant of GII-3 capsid and GII-4 polymerase. To confirm the finding and detect the breakpoints where the recombination event occurred, we performed recombination analysis based on the genomic sequences of HU/GII/SHANGHAI/SH312/2008/CHN as the query sequence, and AB220921/NOV/JP/GII-4 and AB365435/NOV/US/GII-3 as the background sequences, using RPD software. Results indicated that the two parental strains were AB220921/NOV/JP/GII-4 and AB365435/NOV/US/GII-3. The breakpoint for this recombination event located at position 5107nt of the genome (in the ORF1 and ORF2 overlap).
2 The interaction mechanism between SaV and host
(1) Construction of animal models of porcine SaV infection In this study, 2mL of porcine SaV strain (Ch-sw-sav1) was orally inoculated to 11 Bama miniature pigs. Control group was orally inoculated with 2 mL of PBS. Clinical symptoms were supersied for each day. Piglets in both control group and tested groups were euthanized at 1,2,3,5,7,9,11,14,21,30,36 days post infection (PID) to observe possible pathological changes in heart, liver, spleen, lung, kidney, stomach, different part of intestines and inguinal lymph nodes. Pathological sections were inspected by optimal microscopy indirect immunofluorescence, scanning electron microscope and transmission electron microscopy. Results showed that comparing to control group, experimental groups piglets presented clinical symptoms such as diarrhea and vomiting. Pathological sections showed that mild to severe villous atrophy, mild tomoderate and multifocal villous fusion, and crypt hyperplasia were observed in the small intestine (mainly in the duodenum and jejunum). Viruses were detected by indirect immunofluorescence in epithelial cells of the mucosa. Transmission electron microscopy observations indicated that mitochondria of small intestine and stomach had visible. RT-PCR detection of virus in tissues showed that the piglets shed virus from PID 2 to the end of the experiment (PID36).
(2) Relationship between porcine SaV and JAM-A
The available data strongly suggest that the recognition of a carbohydrate receptor may be a common feature of caliciviruses, even though they have adapted to different host species after a long course of evolution. Researches showed that histo-blood group antigens (HBGAs) and junctional adhesion molecule A (JAM-A) were the receptor of NoV and feline calicivirus (FCV), respectively. The binding assay confirmed that SaV VLPs can’t bind the HBGAs molecular. In order to identify the relationship between SaV and JAM-A, rabbit fJAM-A-specific antiserum was used to block the infection. RT-PCR showed that none of the different diluted antiserum can block or decrease the infection, which mean that the JAM-A was not the receptor of SaV.
(3) Screening the receptor of SaV from LLC-PK cells using VOPBA and Co-IP methods; MHC-I interacts with SaV in vitro To date, the receptor of SaV is still unknown. To screening and identify the receptor, both VOPBA and Co-IP assays were performed to screen interactive proteins from susceptible cell LLC-PK. After screening, target protein bands were determined using Mass Spectrum. Several proteins were isolated and MHC-I was chosen for the further analysis. Co-IP results showed that MHC-I interacted with Sav in vitro.
3 VLPs expression of human NoV GII-4 and GII-12 strains
Most recombinant EIAs developed for human caliciviruses are based on use of baculovirus-expressed viral capsid antigens. The baculovirus-expressed human calicivirus capsid antigens self-assemble into virus-like particles that are morphologically and antigenically similar to the authentic viruses found in stool specimens, providing excellent reagents for development of immunologic assays. Results showed that both GII-4 and GII-12 capsid gene fragments were successfully expressed, moreover, those proteins can self-assemble into virus-like particles. Western-blot results indicated that those VLPs can be recognized by the antibodies which product from native virion. However, the VP1 fragment fusion expressed with EGFP can not be purified well though they express in Sf9 cells.
NoV是导致人急性肠胃炎的最主要的非细菌性感染源之一,经常导致家庭和社区性的爆发流行;而SaV致病性较弱,感染率较低,主要感染对象为婴幼儿。除了人群,NoV和SaV也在猪、鼠、水貂等多种动物里被检测到,这也引发了二者是否均为人畜共患病病原的讨论。
杯状病毒的研究起步较晚,虽然已经取得了很大的进展,但还存在很多问题有待解决。
1中国人及猪杯状病毒分子生物学研究
我国人杯状病毒的研究起步较晚,1995年才首次开始研究,实际上,在我国大部分地区都存在该病毒的感染和发病,过去由于未列入常规检测项目或报告项目,对该病毒感染和发病的状况不甚了解。因此有必要对我国的人杯状病毒分子流行病学情况进行系统研究。
除了流行病学特性,对我国诺如病毒的分子生物学特征,例如病毒的全基因结构、重组和进化等方面还知之甚少。另外,我国动物群体中特别是跟人类关系密切的猪群中的杯状病毒的流行情况等基本处于空白。而越来越多的证据显示,杯状病毒存在着跨种间传播的风险。因此,动物源杯状病毒的研究对人杯状病毒的防控,预警机制建立等都具有重要意义。目前我国对札幌病毒的重视程度不够,流行病学情况、分子生物学特征、致病机制及危害、病毒进化与重组等了解不多,因此,对以上各方面均有必要进行深入研究。
2致病机理与动物模型
目前对杯状病毒的研究主要集中于流行病学研究,对病毒的感染、致病机制,物种与组织嗜性,靶细胞受体,在细胞内的复制过程等基础研究相对较少。由于杯状病毒除极个别毒株外一般都难以体外培养,极大地制约了相关研究的进展。而动物模型是研究致病机理的有效手段之一。因此,采用动物模型模拟疾病的发生对杯状病毒感染、致病机制乃至跨种间传播预测等具有重要意义。
3 SaV的受体研究
病毒受体是公认的引发病毒感染宿主细胞的主要决定因素,也是影响病毒宿主特异性和组织亲嗜性的决定因素之一。因此,鉴定SaV受体及其特性与功能,对于从分子水平阐明病毒感染与免疫的机制,深刻理解病毒与宿主细胞的相互关系,病毒的跨种间感染风险预测,疫苗、诊断试剂的研制等,都具有重大的理论与实践意义。有研究显示,人诺如病毒的受体可能为人类血型组织抗原(histo-blood group antigens,HBGA)。为鉴定SaV的受体是否也为HBGA,Jiang等采用杆状病毒表达系统表达了人源SaV的病毒样颗粒,并测试了它们之间的结合能力。结果发现这些病毒样颗粒不能与HBGA结合,从而排除了HBGA作为SaV受体的可能性。目前,札幌病毒的受体依然未知。
有鉴于此,本研究主要从杯状病毒的分子流行病学、动物模型建立、病毒样颗粒的表达、病毒与宿主细胞的互作机制等方面开展研究,
结果如下:
一杯状病毒的分子流行病学研究
1中国大陆发现猪SaV导致仔猪腹泻
2008年2月上海郊区某规模化生猪养殖场发生仔猪腹泻,两窝仔猪中7只仔猪发生,剩余12只仔猪正常。采集上述腹泻粪便样品和正常仔猪粪便样品,同时从该猪场和邻近猪场分别采集正常粪便标本20和80份。根据腹泻仔猪症状和粪便外观观察,初步排除常见细菌性腹泻可能。通过PCR或RT-PCR检测了PCV、PRC、TGEV、PEDV、猪NoV和猪SaV等常见或者新发的能够导致仔猪腹泻的病毒。结果显示,除SaV为,其它病毒均为阴性。为证实仔猪腹泻是否由SaV感染引起,我们进行了动物回归实验。动物实验结果表明,猪SaV病毒阳性粪便悬液能够导致仔猪腹泻和呕吐,并且能够在实验组仔猪的粪便样品中持续检测到病毒。
2华东地区猪杯状病毒分子流行病学研究
到目前为止,各国猪群中尚无关于杯状病毒的系统性研究。为研究猪群中杯状病毒的感染情况,本实验从中国华东地区(上海、江苏、安徽)采集猪新鲜粪便样品,进行分子流行病学检测和分子系统进化分析,并对不同月龄的感染率进行统计分析。结果显示,中国猪群中存在上述两种病毒的感染,SaV和NoV的感染率分别为0.9%(8/904)和0.2%(2/904)。序列分析显示,猪SaV分离株均属GIII,并可进一步分为两个遗传簇。它们分别与荷兰和韩国的猪SaV分离株同源性最近,这暗示,它们可能分别与这两个毒株有着相同的遗传起源。统计结果显示,小于1月龄的仔猪的感染率显著高于1月龄以上的猪的感染率(P<0.05)。本研究表明,中国华东地区猪群中存在猪NoV的感染,但感染率很低,并非该地区的主要病毒性感染源。
3贵州地区猪杯状病毒和戊型肝炎病毒分子流行病学研究
为研究我国西南地区的杯状病毒和戊型肝炎病毒(HEV)的分子流行情况,2009年5-6月,从贵州省6个规模化生猪养殖场随机采集猪新鲜粪便样品209份,用RT-PCR方法进行上述病毒的检测和分子进化分析。HEV和SaV的猪场阳性率分别为83%(5/6)和33%(2/6),未检测到NoV。另外,未发现HEV和SaV共感染。HEV和猪SaV的总体阳性率分别为6.7%(15/209)和1.0% (2/209)。进化分析结果显示,这10株HEV毒株均为G4。它们之间的核酸同源性为90%-99%,与邻近省份广西的一株人HEV分离株(AF103940)聚为一支,同源性为92%-%94%。两株SaV均为GIII,它们之间的核酸同源性为96%,与一支巴西分离株同源性最高(91%),与中国华东地区的分离株(FJ374683)同源性只有82%-84%。这表明,尽管感染率较低,但贵州地区的猪群中存在猪SaV的感染。
4中国猪SaV代表毒株全基因组分析
研究显示有些毒株(如Sapovirus pig/43/06-18p3/06/ITA)在序列上与人的SaV毒株非常接近,这提示猪SaV有可能是人SaV感染的病原之一。为研究中国猪SaV毒株的分子生物学特征,对首支中国分离株进行了全基因组克隆与分析。结果表明,该毒株(Ch-sw-sav1)基因组序列不含3′poly(A)结构全长为7541 nt, A、C、G、U的所占的比重分别为19%、14.3%、33.3%和33.3%。5′末端含有典型的GTG结构。ORF1含有6765 nt(2255aa),编码非结构蛋白和外壳蛋白VP1(544aa)。ORF2长度为516 nt,编码172 aa的小的外壳蛋白VP2(图1A)。ORF1编码的多聚蛋白包括2C解螺旋酶(2C helicase,GPPGIGKT),3C蛋白酶(3C protease,GDCG),RdRp(GLPSG和YGDD),这些非结构蛋白在所有杯状病毒中均高度保守。在VP1区中同样含有PPG模块。基于全基因组序列的分析显示,本毒株属于GIII SaV。基于ORF2 3′末端的对比结果显示,本分离株含有一个21 nt插入片段。
5上海地区门诊儿童的人杯状病毒感染情况调查及基因重组分析
本研究从上海某三甲医院采集门诊儿童粪便样品452份,用RT-PCR方法检测人杯状病毒的感染情况,并对阳性毒株进行系统进化分析。选取代表性毒株进行全基因组克隆,用相关软件进行系统进化和重组分析。452份儿童粪便样品中有20份呈NoV RNA阳性,总体阳性率为4.4%,无SaV阳性粪样检出。20份NoV阳性样品的PCR产物的测序结果显示20个毒株中19株序列彼此不完全相同。它们之间的同源性为79.5%-98.8%。进化分析显示,这19株序列均为GII,并聚集为3个遗传簇(clusters)。其中两个遗传簇为GII-4,另外一个为GII-3。为分析这些毒株的分子特征,从3个遗传簇中分别选取一个代表性毒株进行全基因组克隆和基因重组分析。结果证明,HU/GII/SHANGHAI/SH312/2008/CHN毒株为重组毒株。
二猪SaV小型猪感染模型的建立
本研究采用分离的猪SaV中国株Ch-sw-sav1为攻毒株,通过口服感染SPF级巴马小型猪,通过收集感染后临床症状、病理变化的相关信息以及各组织器官中病原的RT-PCR检测,掌握猪SaV感染猪的第一手资料,为疾病感染机制的研究奠定了基础。结果显示,攻毒后第二天实验组猪即出现不同程度腹泻,个别猪出现呕吐现象。剖检结果显示,实验组猪出现腹胀、小肠出血现象。病理切片的光镜检测结果表明:小肠绒毛萎缩、脱落;透射电镜显微观测表明:小肠上皮细胞细胞核或线粒体病变。间接免疫荧光显示,在小肠各段能检测到病毒抗原的存在。血常规检测结果显示,与对照组和空白组相比,实验组猪在攻毒后白细胞上升,第14天达到最高值,随后开始下降;血小板在攻毒第21天急剧上升,然后缓慢下降;与对照组和空白组相比,实验组猪红细胞没有明显变化。RT-PCR结果显示,实验组猪从攻毒第二天即开始排毒,直至实验结束(PID36)。
三猪SaV靶细胞受体初步研究
1连接黏附分子1作为猪SaV受体的可能性研究
杯状病毒中的NoV和猫杯状病毒(feline calicivirus,FCV)的功能性受体分别为人类血型组织抗原(histo-blood group antigens,HBGAs)和连接黏附分子1(junctional adhesion molecule 1,JAM-1)。已有的研究数据均显示识别碳水化合物可能是杯状病毒的共同特征,尽管在长期的进化过程中不同杯状病毒已适应了不同的宿主细胞。对此,研究人员分别测试了NoV和SaV与HBGAs间的结合能力。结果显示,NoV的VLPs能够与HBGAs结合,而SaV GI和GV的VLPs均不能结合HBGAs。为检验JAM-1作为GIII SaV受体的可能性,我们测试了抗JAM-1多抗对SaV病毒感染易感细胞LLC-PK的阻断效果。在病毒感染细胞前用不同浓度抗JAM-1多抗预先与细胞孵育,随后用荧光定量PCR方法检测不同浓度抗体的孵育能否阻断或者降低病毒对细胞的结合和感染。结果显示,JAM-1抗体不能阻断或者降低SaV对易感细胞LLC-PK的感染。这表明,JAM-1作为SaV感染宿主细胞的受体可能性较低。
2 VOPBA和Co-IP法筛选猪SaV候选受体
本研究拟采用VOPBA法和免疫共沉淀法结合质谱探索猪SaV在易感细胞LLC-PK细胞表面受体;采用上述两种方法共鉴定到若干疑似蛋白。根据这些蛋白的细胞内分布和功能结合文献分析,选取MHC-1(major histocompatibility complex class I)进行进一步验证。CO-IP结果显示,MHC-I能够与病毒结合。
四人NoV病毒样颗粒(Virus-like particles)表达
本研究采用杆状病毒表达载体进行GII-4和GII-12毒株的VLPs表达,并用Western-blot和免疫电镜方法进行抗原性和形态学鉴定;尝试将外壳蛋白VP1和绿色荧光蛋白(EGFP)融合表达,以期得到带有EGFP标记的病毒样颗粒。研究结果显示,所有的重组杆状病毒均能在Sf9细胞中表达。除了与EGFP融合的蛋白不能成功纯化外,其它均能得到合适浓度的重组蛋白。Western-blot和免疫电镜显示,这些蛋白均具有抗原性并能自我组织形成病毒样颗粒,而GII-12的VLPs能够被抗GII-4 VLPs的抗体所识别。
The family Caliciviridae is composed of small (27 to 40 nm), nonenveloped, icosahedral viruses that possess a linear, positive-sense, single-stranded 7 to 8 kb RNA (ssRNA) genome. They are 27-35 nm in diameter. Caliciviruses were classified into 4 genera in 2002 by the International Committee on the Taxonomy of Viruses (ICTV): Norovirus (NoV), Sapovirus (SaV), Vesivirus, and Lagovirus. The major medical pathogens in the family are NoV and SaV, which cause acute gastroenteritis. Important veterinary pathogens include vesiviruses such as feline calicivirus (FCV), which causes a respiratory disease in cats, and lagoviruses such as rabbit hemorrhagic disease virus (RHDV), which causes an often fatal hemorrhagic disease in rabbits. Human caliciviruses include both human NoV and SaV. Human NoV is believed to be one of the major causes of nonbacterial epidemic gastroenteritis, a disease that usually occurs in family or community-wide outbreaks. The impact of the SaV has not been fully established, but to date they do not share a predominant role with the NoV in epidemic gastroenteritis. Researches showed that both NoV and sapoviruses have been associated with gastroenteritis in infants and young children. Although no inter-species recombinant strain has been found, an inter-genogroup human calicivirus recombinant has been described. Additional, sometimes human strains genetically closely related to the animal strains. Specifically, porcine NoV are genetically closely related to some human NoV in the GII. All of these finding suggests a potential zoonotic risk and pig is considered as an animal reservoir for such viruses.
Although some of great progress have been made in the research field of caliciviruses, there are still some unclear points, including (1) The interaction mechanism between caliciviruses and host cells; (2) The replication mechanism of caliciviruses in host cell and animal model; (3) Are caliciviruses zoonotic agents; (4) Pathogenesis of caliciviruses; (5) Recombinants between animal and human caliciviruses; (5) The receptor of SaV. In order to elucidate some points mentioned above, we performed the following researches:
1 Study of molecular epidemiology of caliciviruses
(1) The first Chinese porcine sapovirus strain that contributed to an outbreak of gastroenteritis in piglets
We report the first outbreak of gastroenteritis caused by porcine SaV in piglets in China. This outbreak occurred in February 2008 on a small commercial pig farm that lies in Shanghai suburb. Seven stool specimens were collected from seven piglets which showed symptoms of diarrhea and vomiting in two neighboring farrows on the farm. At the beginning, we first examined the seven specimens from the ill piglets for porcine circovirus, porcine rotavirus, porcine transmissible gastroenteritis virus, and porcine epidemic diarrhea virus using reverse transcription-PCR (RT-PCR), and all specimens showed negative results. All specimens were then examined for SaV by using RT-PCR as described previously. Our results showed that all seven piglets that showed clinical symptoms were positive for SaV RNA, suggesting this outbreak of gastroenteritis may due to porcine SaV infection.
In order to elucidate whether the fecal samples contained infectious SaV, the eight SaV-positive fecal specimens were used to infect piglets. Results indicated that all of those experimental infection piglets showed symptoms of diarrhea and vomiting, and shed virus after inoculation.
(2) Molecular detection and prevalence of porcine caliciviruses in eastern China Caliciviruses that causes diarrhea were reported in both industrial and developing countries including China recent years. Porcine caliciviruses closely related to human sapovirus and norovirus were also detected in swine group, which caused discussions about the animal reservoir and the potential risk for zoonotic transmission to humans. The objective of this work was to determine the frequency and distribution in the different age of swine for porcine sapovirus and norovirus, and characterize the strains prevalent in eastern China. A total of 904 stool samples from different ages of pigs were collected from eastern China from April 2008 to March 2009, and tested for both SaVs and NoVs using reverse transcription-polymerase chain reaction (RT–PCR). Our results indicated that 8 (0.9%) stool samples were positive for SaV and 2 (0.2%) for NoV. Phylogenetic analyses based on the partial RNA polymerase gene sequences indicated that all of the SaV isolates belonged to GIII, while the 2 NoV isolates belonged to GII. The 8 SaV isolates were further divided into 2 different groups in the GIII cluster, one of which clustered closely with the Netherland isolate (AY615804) and the other one with the Chinese strain (EU599212). Our results suggested that SaV infection was more frequently (p <0.01) in 0-1 month age of swine than that of other ages. In conclusion, the present study provided evidence that infection of PoSaV and PoNoV existed in pig groups of eastern China.
(3) Prevalence of porcine caliciviruses and Hepatitis E Virus in pig farms of Guizhou province, China
A total of 209 stool samples from pigs of different age groups were collected from 6 pig farms in Guizhou province from May to June 2009, and tested for HEV, SaV and NoV using reverse transcription-polymerase chain reaction (RT–PCR). The overall prevalence of porcine HEV and porcine SaV were 6.7% (15/209) and 1.0% (2/209), respectively. No NoV infection was detected in the current study. The prevalence rates of porcine HEV infection for different ages of pigs were 15.4% (4/26; piglet, age<1 month), 6.8% (3/44; 4 month
(4) Molecular characterization and phylogenetic analysis of the complete genome of a porcine sapovirus from Chinese swine The whole genome of Ch-sw-sav1 was amplified by RT-PCR and was sequenced. Sequence alignment of the complete genome or RNA dependent RNA polymerase (RdRp) gene was done. 3′end of ORF2 with 21-nt nucleotide insertion was further analyzed using softwares. Sequence analysis indicated that the genome of Ch-sw-sav1 was 7541 nucleotide long with two ORFs, excluding the 17 nucleotides ploy (A) at the 3′end. Phylogenetic analysis based on part of RdRp gene of this strain showed that it was classified into subgroup GIII. Sequence alignment indicated that there was an inserted 21-nt long nucleotide sequence at the 3′end of ORF2. The insertion showed high antigenicity index comparing to other regions in ORF2.
(5) Prevalence and recombination of NoV in outpatients of Shanghai 452 stool samples from outpatients were collected from Shanghai, China. The fecal samples were tested for human caliciviruses. The full-genome of representative strains were then chosen and determined. Results showed that 20 NoV RNA positive samples were identified and the overall prevalence of NoV was 4.4%. No SaV positive were found in current study. In the present study, three full-length genomes of human NoV from China were determined and the genomic organization and recombination were analyzed. They had similar genome organization and contained three predicted ORFs, though the 5’UTR of those three strains were 2, 4 and 8 nucleotides, respectively. Phylogenetic analysis showed that the HU/GII/SHANGHAI/SH312/2008/CHN strain may be a recombinant of GII-3 capsid and GII-4 polymerase. To confirm the finding and detect the breakpoints where the recombination event occurred, we performed recombination analysis based on the genomic sequences of HU/GII/SHANGHAI/SH312/2008/CHN as the query sequence, and AB220921/NOV/JP/GII-4 and AB365435/NOV/US/GII-3 as the background sequences, using RPD software. Results indicated that the two parental strains were AB220921/NOV/JP/GII-4 and AB365435/NOV/US/GII-3. The breakpoint for this recombination event located at position 5107nt of the genome (in the ORF1 and ORF2 overlap).
2 The interaction mechanism between SaV and host
(1) Construction of animal models of porcine SaV infection In this study, 2mL of porcine SaV strain (Ch-sw-sav1) was orally inoculated to 11 Bama miniature pigs. Control group was orally inoculated with 2 mL of PBS. Clinical symptoms were supersied for each day. Piglets in both control group and tested groups were euthanized at 1,2,3,5,7,9,11,14,21,30,36 days post infection (PID) to observe possible pathological changes in heart, liver, spleen, lung, kidney, stomach, different part of intestines and inguinal lymph nodes. Pathological sections were inspected by optimal microscopy indirect immunofluorescence, scanning electron microscope and transmission electron microscopy. Results showed that comparing to control group, experimental groups piglets presented clinical symptoms such as diarrhea and vomiting. Pathological sections showed that mild to severe villous atrophy, mild tomoderate and multifocal villous fusion, and crypt hyperplasia were observed in the small intestine (mainly in the duodenum and jejunum). Viruses were detected by indirect immunofluorescence in epithelial cells of the mucosa. Transmission electron microscopy observations indicated that mitochondria of small intestine and stomach had visible. RT-PCR detection of virus in tissues showed that the piglets shed virus from PID 2 to the end of the experiment (PID36).
(2) Relationship between porcine SaV and JAM-A
The available data strongly suggest that the recognition of a carbohydrate receptor may be a common feature of caliciviruses, even though they have adapted to different host species after a long course of evolution. Researches showed that histo-blood group antigens (HBGAs) and junctional adhesion molecule A (JAM-A) were the receptor of NoV and feline calicivirus (FCV), respectively. The binding assay confirmed that SaV VLPs can’t bind the HBGAs molecular. In order to identify the relationship between SaV and JAM-A, rabbit fJAM-A-specific antiserum was used to block the infection. RT-PCR showed that none of the different diluted antiserum can block or decrease the infection, which mean that the JAM-A was not the receptor of SaV.
(3) Screening the receptor of SaV from LLC-PK cells using VOPBA and Co-IP methods; MHC-I interacts with SaV in vitro To date, the receptor of SaV is still unknown. To screening and identify the receptor, both VOPBA and Co-IP assays were performed to screen interactive proteins from susceptible cell LLC-PK. After screening, target protein bands were determined using Mass Spectrum. Several proteins were isolated and MHC-I was chosen for the further analysis. Co-IP results showed that MHC-I interacted with Sav in vitro.
3 VLPs expression of human NoV GII-4 and GII-12 strains
Most recombinant EIAs developed for human caliciviruses are based on use of baculovirus-expressed viral capsid antigens. The baculovirus-expressed human calicivirus capsid antigens self-assemble into virus-like particles that are morphologically and antigenically similar to the authentic viruses found in stool specimens, providing excellent reagents for development of immunologic assays. Results showed that both GII-4 and GII-12 capsid gene fragments were successfully expressed, moreover, those proteins can self-assemble into virus-like particles. Western-blot results indicated that those VLPs can be recognized by the antibodies which product from native virion. However, the VP1 fragment fusion expressed with EGFP can not be purified well though they express in Sf9 cells.
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