2020, Vol. 46扩展功能
文章信息
- 徐娜, 桓晨, 郑柏松
- XU Na, HENG Chen, ZHENG Baisong
- 含缬酪肽蛋白促进单链RNA和双链DNA病毒复制或释放机制的研究进展
- Research progress in mechanism of valosin-containing protein in promoting replication or release of single-stranded RNA and double-stranded DNA viruses
- 吉林大学学报(医学版), 2020, 46(05): 1099-1104
- Journal of Jilin University (Medicine Edition), 2020, 46(05): 1099-1104
- 10.13481/j.1671-587x.20200534
-
文章历史
- 收稿日期: 2019-12-24
含缬酪肽蛋白(valosin-containing protein，VCP)又名P97，属三磷酸腺苷酸酶超家族(ATPases associated with various cellular activities，AAA)成员之一。自1982年首次从酵母中分离后[1]，VCP先后在多种哺乳动物中被发现[2]。作为一种普遍存在于各种哺乳动物细胞质中的蛋白，VCP在结构上为一种环状同源六聚体复合物[3]。每个单体包含4个结构域：1个可移动的N端结构域、2个保守的AAA结构域(称为D1和D2)和1个无序的C端尾部结构域[4-5]。每个AAA结构域都包含保守的核苷酸结合基序和水解基序以及有效水解所必需的第二同源区域[6-7]。以往研究[8-10]表明：VCP的核心功能是依赖于其ATPase活性的泛素化蛋白水解作用，这一功能使得VCP不仅能够参与细胞内核酸重建、内质网和线粒体相关蛋白降解[11-12]、细胞周期调控[13-14]、核转录因子-κB(nuclear transcription factor-κB，NF-κB)活化[15]、膜融合和囊泡运输[16]等重要细胞活动，还具有抗细胞凋亡和促进细胞增殖及浸润等作用。
近年来，围绕VCP的功能研究已经证实VCP与蛋白稳态失调相关疾病及癌症有关联，其中包括亨廷顿舞蹈病(Huntington’s disease，HD)[17]、雄激素非依赖性前列腺癌(androgen-independent prostate cancer，AIPC)[18]和多发性骨髓瘤(multiple myeloma，MM)[19]等。VCP能有效杀伤癌细胞，可能是一种广泛的抗肿瘤因子。随着研究的深入，VCP与感染性疾病的联系愈加紧密，其作为宿主因子参与病毒相关的感染性疾病的研究已受到广泛关注。目前，围绕VCP研究的综述主要在2个方面：一方面是围绕VCP介导的蛋白质降解及其机制，包括蛋白酶体降解、内质网相关降解(endoplasmic reticulum-associated degradation，ERAD)和自噬[14]；另一方面是关于VCP参与DNA复制和染色质动力学等细胞周期的调控和机制研究[13, 20]。目前，关于VCP参与的ERAD相关的蛋白降解途径的研究较为深入。尽管VCP借助蛋白质降解和DNA调控等功能参与多种疾病的发生发展，但未见针对VCP作为宿主因子在病毒性疾病中的作用及其分子机制方面的报道。现针对近年来报道的VCP同多种病毒在人体内的复制或释放的相关研究进行综述(表 1)，为病毒感染性疾病的诊治提供参考。
| Name | Classify | Envelop | Active domain | Pathway | Virus life cycle | Reference |
| WNV | +ss RNA Virus | Yes | — | — | Entry and Replication | [29] |
| HCV | +ss RNA Virus | Yes | ATPase Domain | VCP inhibition first results in aberrant NS5A aggregation, and then by interfering with the accessibility of NS5A, affects NS5A hyperphosphorylation and protein–protein interaction and finally abolishes viral replicase assembly | Replication | |
| PV | +ss RNA Virus | No | ATPase Domain | ATPase activity of VCP is involved in virus replication, and VCP interacts with PV-2BC/3AB protein to participate in virus release | Replication and Release | [24] |
| EV71 | +ss RNA Virus | No | ATPase Domain | ERAD pathway | Replication | [33-34] |
| CoV | +ss RNA Virus | Yes | — | VCP promote virus particles from exiting endosomes anduncoating and N protein degradation hence inhibits the subsequent | Replication | [38] |
| SINV | +ss RNA Virus | Yes | — | VCP regulates NRAMP2 receptor trafficking | Entry | [27] |
| CHIKV | +ss RNA Virus | Yes | — | VCP participates in the activation of CHIKV virus replicase | Replication | [28] |
| AcMNPV | ds DNA Virus | Yes | ATPase Domain | Ubiquitin-proteasome pathway | Replication | [39] |
| HCMV | ds DNA Virus | Yes | — | VCP controls the viral gene expression of IE2 | Replication | [41] |
| RVFV | +ss RNA Virus | Yes | — | ER membrane remodeling | Release | [43] |
| “－”:No data. | ||||||
在修饰的宿主细胞内膜上组装病毒复制酶以形成复制复合物(replication complex，RC)是几乎所有正链RNA病毒成功复制的标志[21]。VCP与单链RNA病毒的复制有关联，其中包括西尼罗河病毒(West Nile virus，WNV)[22]、丙型肝炎病毒(hepatitis C virus，HCV)[23]、脊髓灰质炎病毒(poliovirus，PV)[24]、肠道病毒71型(enterovirus 71，EV71)[25]、冠状病毒(coronavirus，CoV)[26]、辛德毕斯病毒(Sindbis virus，SINV)[27]和基孔肯雅病毒(Chikungunya virus，CHIKV)[28]。
1.1 VCP参与黄病毒科黄病毒属病毒成员的复制WNV和HCV均是黄病毒科黄病毒属的成员，属于有包膜结构的单股正链RNA病毒[22-23]。WNV主要导致西尼罗河脑炎，HCV主要引起丙型肝炎。PHONGPHAEW等[29]研究发现：在HeLa细胞中使用VCP抑制剂或siRNA抑制内源性VCP表达后，WNV病毒感染能力及RNA表达水平明显降低，表明VCP可能在WNV病毒生命周期的吸附或进入的早期步骤中起作用。该研究通过构建WNV病毒样颗粒和基于WNV-DNA的复制子，证明VCP参与合成新的WNV病毒基因组并介导WNV病毒复制[29]。研究[30]发现：在Huh7.5细胞中利用分子生物学技术敲除VCP或加入VCP生理抑制剂EerI和NMS-873后，能够降低HCV病毒的复制水平。在此过程中，VCP通过与HCV病毒的一种无酶活性的多功能非结构蛋白NS5A DI相互作用，达到参与HCV病毒复制的目的。VCP表达受抑制后，促使HCV NS5A聚集并减少NS5A的高度磷酸化，影响HCV病毒复制酶的组装，进而影响复制复合物的形成[30-31]，最终影响HCV病毒的复制。综上所述，在HCV复制过程中，VCP发挥解聚作用，利用腺苷三磷酸酶(ATPase)酶活性(氨基酸位点：241~647位)防止HCV NS5A聚集，帮助HCV病毒复制。
1.2 VCP参与小核糖核酸病毒科肠道病毒属病毒成员的复制PV和EV71同属于小核糖核酸病毒科肠道病毒属成员，是无包膜结构的单股正链RNA病毒[24-25]。PV主要引起脊髓灰质炎，EV71是导致手足口病的重要病原体之一。ARITA等[24]针对膜转运基因对PV病毒复制所需的宿主因子进行小干扰RNA(siRNA)筛选，发现VCP与PV病毒复制有关。为了确定VCP与PV病毒复制相关的主要活性位点，研究者对VCP ATPase活性位点进行点突变[32]，获得K524A失活突变体和R191Q及A232E活性增强突变体。通过在沉默VCP的HEK293T细胞中过表达野生型VCP和2种突变体VCP[32]，结果显示：与转染了野生型和活性增强突变体VCP的细胞比较，PV病毒在转染K524A失活突变体细胞中的复制能力明显降低，表明VCP的ATPase活性对于维持PV病毒的复制至关重要。WU等[33]首次针对EV71病毒易感细胞——横纹肌肉瘤细胞(RD)中21 121个人类全基因组siRNA文库进行了基于免疫荧光的表型筛选，鉴定出促进EV71病毒复制的因子(host susceptibility factors，HSFs，又称宿主易感性因子)和抑制EV71病毒复制的因子(host resistance factors，HRFs，又称宿主抗性因子)；最终发现可能参与EV71病毒复制所涉及的256个宿主因子，其中宿主抗性因子包含细胞周期调节剂极光激酶B(aurora kinase B，AURKB)和细胞周期蛋白依赖性激酶6(cyclin-dependent kinase 6，CDK6)，而EV71可能通过诱导CDK6的出核而对EV71病毒的复制进行调节。另外，ERAD成分N-聚糖酶1(N-glycanase 1，NGLY1)和VCP被证明是EV71宿主易感因子，能够在特定的细胞周期阶段促进EV71的复制。WANG等[34]通过探讨EV71病毒感染过程中ERAD底物的变化发现：EV71病毒感染能够通过多重位点——HES相关抑制蛋白(hes-related repressor protein，Herp)、羟甲基戊二酰辅酶A还原酶降解蛋白1(Hmg-Co A reductase degradation 1，Hrd1)、E2泛素结合酶(E2 ubiquitin-conjugating enzymes，Ubc6e)、VCP相关膜蛋白(VCP-interacting membrane protein，VIMP)和泛素调节X结构域的膜蛋白8(ubiquitin regulatory X domain-containing protein 8，UBXD8)将ERAD底物锚定在内质网上，VCP能够促进EV71病毒的复制。其中，EV71 3C蛋白能够在Q219G、Q260S和Q273G3个位点[35]处切割E2泛素结合酶Ubc6e，而EV71 2A蛋白则抑制Herp和VIMP的合成，导致ERAD途径受到抑制。其中，VIMP是一种与VCP具有相互作用的膜蛋白[36]，能够招募VCP和其他辅助因子至内质网[37]。免疫共沉淀实验[34]表明：VCP ATPase活性区域能够与EV71病毒相结合，而且VCP能与EV71 2C蛋白在复制复合物中发生共定位，致使内质网膜发生重塑，促进EV71病毒的复制。VCP并不能作用于肠道病毒属柯萨奇病毒B3(coxsackievirus B3，CVB3)的复制[24]，表明VCP对肠道病毒属病毒的促进作用具有偏好性，有待进一步研究。
1.3 VCP参与CoV的复制CoV是一类有包膜的正链RNA病毒，可在人类和多种哺乳动物中引起呼吸道和肠道疾病[26]。WONG等[38]以CoV家族成员之一的传染性支气管炎病毒(infectious bronchitis virus，IBV)为模型，发现VCP在IBV病毒复制早期发挥作用。
1.4 VCP参与披膜病毒科甲病毒属病毒的复制1955年分离的SINV和1952年分离的CHIKV同属于披膜病毒科甲病毒属，是具有囊膜结构的单股正链RNA病毒。VCP能够调节SINV [27]进入受体天然抗性相关的巨噬细胞蛋白2(natural resistance-associated macrophage protein 2，NRAMP2)的运输，在果蝇细胞中敲除VCP后，将改变NRAMP2的运输途径导致NRAMP2被溶酶体降解和SINV病毒的复制受到抑制[27]。VCP在CHIKV生命周期中的病毒RNA复制中起作用[28]，但不影响CHIKVA病毒的吸附或进入。
2 VCP促进双链DNA病毒的复制尽管VCP参与多种单链RNA病毒的复制，但截止目前为止VCP同DNA病毒相互关系的研究鲜有报道。加州苜蓿多核核型多角体病毒(autographa californica multiple nucleopolyhedrovirus，AcMNPV)属于昆虫细胞杆状病毒，是一种双链DNA病毒。LYUPINA等[39]发现：利用药物NMS-873抑制VCP可阻断杆状病毒AcMNPV的感染周期，导致芽状病毒粒子产生受到抑制，并且VCP通过其ATPase活性参与泛素-蛋白酶体途径，促进AcMNPV病毒的复制。
人类巨细胞病毒(human cytomegalovirus，HCMV)作为一种感染人类的双链DNA病毒，是疱疹病毒家族中基因组最大的成员，先天性感染在HCMV病毒感染中占据较高比例[40]。HCMV的早期蛋白质IE1和IE2是HCMV复制的关键，能够平衡激活感染和潜伏感染。LIN等[41]敲除VCP后导致IE2表达丢失，表明VCP是HCMV蛋白IE2表达所必需的。RNAseq分析[41]显示：敲除VCP后，IE1剪接水平增加，IE2剪接水平相应减少。病毒转录的整体分析显示：尽管IE2表达丢失，但包括UL112/113在内的病毒基因的子集表达水平并未降低，表明VCP敲低引起的IE1和IE2水平变化不是病毒复制延迟所导致。免疫荧光实验研究[41]结果显示：VCP与细胞核中的病毒复制区具有共定位，进一步表明VCP对于HCMV的复制具有重要意义。
3 VCP参与病毒粒子的释放除影响病毒复制外，VCP与病毒粒子释放相关。裂谷热病毒(rift valley fever virus，RVFV)属于布尼亚病毒目白纤病毒科白蛉病毒属，RVFV病毒是裂谷热(rift valley fever，RVF)的病原体，RVF是一种人畜共患病毒，可导致人畜共患病[42]。BRAHMS等[43]研究发现：在分泌途径中涉及膜重塑功能的VCP对RVFV病毒的释放很重要；Vero细胞中敲除VCP后导致RVFV病毒复制减少，且RVFV病毒糖蛋白Gn与高尔基复合体定位减少，而在ER的积累增加；在用靶向VCP的siRNA转染的细胞中也观察到RVFV病毒粒子在细胞内的积累。该研究结果提示：siVCP后RVFV病毒粒子的组装发生在高尔基体中，但在组装后将其锚定至内质网来阻止病毒粒子释放。
在关于PV病毒的研究中，ARITA等[24]通过在PV病毒感染的RD细胞和HEK293T细胞中进行VCP与病毒蛋白共定位及相互作用分析发现：VCP与PV-2BC/2C蛋白和3AB/3B蛋白存在共定位情况，邻位连接作用(proximity ligation assay，PLA)分析显示VCP与2BC和3AB蛋白相互作用，但不与2C蛋白和3A蛋白相互作用；敲除VCP后，PV病毒蛋白表达相应减少。该研究发现了细胞蛋白分泌与病毒RNA复制之间的新型联系。
4 总结与展望目前，VCP不仅可以通过参与病毒复制体的组装实现促进病毒基因复制的作用，还可以通过膜重塑功能参与病毒粒子的释放。VCP不参与负链RNA病毒水疱性口炎病毒(vesicular stomatitis virus，VSV)的生命活动。目前针对VCP与单股正链RNA病毒的研究较多，其中VCP对肠道病毒属PV和EV71均能有效的促进病毒复制，但不影响CVB3病毒的复制，表明不同肠道病毒的致病机制不同。针对VCP参与正链RNA病毒WNV、HCV、PV、EV71、CoV、SINV、CHIKV和RVFV病毒生命周期的广谱性，以及对于DNA病毒AcMNPV、疱疹病毒HCMV特异的促进作用及依据VCP能够有效调控ERAD和自噬等相关途径的特点，将有助于设计新的抗病毒药物，为感染性疾病的诊治提供新的思路。
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