A型流感病毒感染雪貂造模的研究进展
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摘要
A型流感病毒(influenza A virus,IAV)感染人和动物,严重威胁公共卫生安全。动物模型在IAV研究中发挥着重要作用,不同的动物模型具有不同的优点和限制性。本文比较了雪貂与小鼠、豚鼠和非人灵长类动物模型的优点和限制性,突出说明雪貂在IAV研究中的重要性,并就雪貂在IAV致病性、传播和疫苗研发中的研究进展做了总结,以期为IAV的基础和应用研究提供参考。
Influenza A viruses(IAVs) infect humans and animals, and pose continuous threats to public health. Animal models have pivotal roles in IAV research, and different animal models have different advantages and limitations. We focused on the advantages and disadvantages of the use of ferrets, and compared them with those of mice, guinea pigs, and non-human primate models. We highlighted the important role of ferrets in IAV research. This paper briefly reviews the research progress in use of ferret models in the studies of pathogenesis, transmission and evaluation of IAVs. As such, it provides references for the basic and applied research of IAVs.
Influenza A viruses(IAVs) infect humans and animals, and pose continuous threats to public health. Animal models have pivotal roles in IAV research, and different animal models have different advantages and limitations. We focused on the advantages and disadvantages of the use of ferrets, and compared them with those of mice, guinea pigs, and non-human primate models. We highlighted the important role of ferrets in IAV research. This paper briefly reviews the research progress in use of ferret models in the studies of pathogenesis, transmission and evaluation of IAVs. As such, it provides references for the basic and applied research of IAVs.
引文
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[11] Thangavel RR,Bouvier NM.Animal models for influenza virus pathogenesis,transmission,and immunology [J].J Immunol Methods,2014,410:60-79.
[12] Sally DA,Taubenberger JK,Bray M.The use of nonhuman primates in research on seasonal,pandemic and avian influenza,1893-2014 [J].Antiviral Res,2015,117:75-98.
[13] 邓少嫦,张钰,黄韧.禽流感的哺乳类动物模型研究进展[J].中国比较医学志,2009,19(12):40-43+75.Deng SC,Zhang Y,Huang R,et al.Advances in research on animal models for H5N1 avian influenza [J].Chin J Comp Med,2009,19(12):40-43+75.
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[17] 邓巍,许黎黎,鲍琳琳,等.雪貂感染H7N9禽流感病毒动物模型的建立[J].中国比较医学杂志,2014,24(1):68-71+14.Deng W,Xu LL,Bao LL,et al.The ferret models for studying the novel avian-origin human influenza A (H7N9)virus [J].Chin J Comp Med,2014,24(1):68-71+14.
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[19] Peng XX,Alfoldi J,Gori K,et al.The draft genome sequence of the ferret (Mustela putorius furo) facilitates study of human respiratory disease [J].Nat Biotechnol,2014,32(12):1250-1255.
[20] Ryan KA,Slack GS,Marriott AC,et al.Cellular immune response to human influenza viruses differs between H1N1 and H3N2 subtypes in the ferret lung [J].PLoS One,2018,13:e0202675.
[21] Sun HL,Kaplan BS,Guan MH,et al.Pathogenicity and transmission of a swine influenza A(H6N6) virus [J].Emerg Microbes Infect,2017,6:e17.
[22] Li XY,Shi JZ,Guo J,et al.Genetics,receptor binding property,and transmissibility in mammals of naturally isolated H9N2 avian influenza viruses [J].PLoS Pathog,2014,10:e1004508.
[23] Peng BH,Yun N,Chumakova O,et al.Neuropathology of H5N1 virus infection in ferrets [J].Vet Microbiol,2012,156(3-4):294-304.
[24] Herfst S,Mok CKP,van den Brand JMA,et al.Human clade 2.3.4.4 A/H5N6 influenza virus lacks mammalian adaptation markers and does not transmit via the airborne route between ferrets [J].mSphere,2018,3:e00405-17.
[25] Noh JY,Lee DH,Yuk SS,et al.Limited pathogenicity and transmissibility of Korean highly pathogenic avian influenza H5N6 clade 2.3.4.4 in ferrets [J].Transbound Emerg Dis,2018,65(4):923-926.
[26] Pulit-Penaloza JA,Sun XJ,Creager HM,et al.Pathogenesis and transmission of novel highly pathogenic avian influenza H5N2 and H5N8 viruses in ferrets and mice [J].J Virol,2015,89(20):10286-10293.
[27] Zhang QY,Shi JZ,Deng GH,et al.H7N9 influenza viruses are transmissible in ferrets by respiratory droplet [J].Science,2013,341(6144):410-414.
[28] Watanabe T,Kiso M,Fukuyama S,et al.Characterization of H7N9 influenza A viruses isolated from humans [J].Nature,2013,501(7468):551-555.
[29] Imai M,Watanabe T,Kiso M,et al.A highly pathogenic avian H7N9 influenza virus isolated from a human is lethal in some ferrets infected via respiratory droplets [J].Cell Host & Microbe,2017,22(5):615-626.e618.
[30] Xiao CC,Ma WJ,Sun N,et al.PB2-588 V promotes the mammalian adaptation of H10N8,H7N9 and H9N2 avian influenza viruses [J].Sci Rep,2016,6:19474.
[31] Zhou J,Wei JJ,Choy KT,et al.Defining the sizes of airborne particles that mediate influenza transmission in ferrets [J].Proc Natl Acad Sci U S A,2018,115(10):2386-2392.
[32] Buhnerkempe MG,Gostic K,Park M,et al.Mapping influenza transmission in the ferret model to transmission in humans [J].elife,2015,4:e07969.
[33] Stevens J,Blixt O,Tumpey TM,et al.Structure and receptor specificity of the hemagglutinin from an H5N1 influenza virus [J].Science,2006,312(5772):404-410.
[34] Tumpey TM,Maines TR,Van Hoeven N,et al.A two-amino acid change in the hemagglutinin of the 1918 influenza virus abolishes transmission [J].Science,2007,315(5812):655-659.
[35] Xiong XL,Martin SR,Haire LF,et al.Receptor binding by an H7N9 influenza virus from humans [J].Nature,2013,499(7459):496-499.
[36] Richard M,Schrauwen EJA,de Graaf M,et al.Limited airborne transmission of H7N9 influenza A virus between ferrets [J].Nature,2013,501(7468):560-563.
[37] Zhu H,Wang D,Kelvin DJ,et al.Infectivity,transmission,and pathology of human-isolated H7N9 influenza virus in ferrets and pigs [J].Science,2013,341(6142):183-186.
[38] Lowen AC,Mubareka S,Steel J,et al.Influenza virus transmission is dependent on relative humidity and temperature [J].PLoS Pathog,2007,3(10):1470-1476.
[39] Shi JZ,Deng GH,Ma SJ,et al.Rapid evolution of H7N9 highly pathogenic viruses that emerged in China in 2017 [J].Cell Host Microbe,2018,24(4):558-568.
[40] Yang W,Yin X,Guan L,et al.A live attenuated vaccine prevents replication and transmission of H7N9 highly pathogenic influenza viruses in mammals [J].Emerg Microbes Infect,2018,7(1):153.
[41] Kong HH,Zhang QY,Gu CY,et al.A live attenuated vaccine prevents replication and transmission of H7N9 virus in mammals [J].Sci Rep,2015,5:11233.
[42] Chen ZY,Baz M,Lu J,et al.Development of a high-yield live attenuated H7N9 influenza virus vaccine that provides protection against homologous and heterologous H7 wild-type viruses in ferrets [J].J Virol,2014,88(12):7016-7023.
[43] Hatta M,Zhong GX,Chiba S,et al.Effectiveness of whole,inactivated,low pathogenicity influenza A(H7N9) vaccine against antigenically distinct,highly pathogenic H7N9 virus [J].Emerg Infect Dis,2018,24(10):1910-1913.
[44] Wang LL,Liu SY,Chen HW,et al.Generation of a live attenuated influenza vaccine that elicits broad protection in mice and ferrets [J].Cell Host & Microbe,2017,21(3):334-343.
[45] Rudenko L,Kiseleva I,Krutikova E,et al.Two live attenuated vaccines against recent low and highly pathogenic H7N9 influenza viruses are safe and immunogenic in ferrets [J].Vaccines,2018,6(4).pii:E74.
[46] Wei SH,Yang JR,Wu HS,et al.Human infection with avian influenza A H6N1 virus:an epidemiological analysis [J].Lancet Respir Med,2013,1(10):771-778.
[47] Zhang RS,Chen TM,Ou XH,et al.Clinical,epidemiological and virological characteristics of the first detected human case of avian influenza A(H5N6) virus [J].Infect Genet Evol,2016,40:236-242.
[48] 郭元吉,李建国,程小雯,等.禽H9N2亚型流感病毒能感染人的发现[J].中华实验和临床病毒学杂志,1999,13(2):105-108.Guo YJ,Li JG,Cheng XW,et al.Discovery of men infected by avian influenza A (H9N2) virus[J].Chin J Exp Clin Virol,1999,13(2):105-108.
[49] Butt KM,Smith GJ,Chen HL,et al.Human infection with an avian H9N2 influenza A virus in Hong Kong in 2003 [J].J Clin Microbiol,2005,43(11):5760-5767.
[50] Shi JZ,Deng GH,Liu PH,et al.Isolation and characterization of H7N9 viruses from live poultry markets — Implication of the source of current H7N9 infection in humans [J].Chin Sci Bull,2013,58(16):1857-1863.
[51] Liu D,Shi WF,Shi Y,et al.Origin and diversity of novel avian influenza A H7N9 viruses causing human infection:phylogenetic,structural,and coalescent analyses [J].Lancet,2013,381(9881):1926-1932.
[2] Wise HM,Foeglein A,Sun J,et al.A complicated message:Identification of a novel PB1-related protein translated from influenza A virus segment 2 mRNA [J].J Virol,2009,83(16):8021-8031.
[3] Jagger BW,Wise HM,Kash JC,et al.An overlapping protein-coding region in influenza A virus segment 3 modulates the host response [J].Science,2012,337(6091):199-204.
[4] Muramoto Y,Noda T,Kawakami E,et al.Identification of novel influenza A virus proteins translated from pa mRNA [J].J Virol,2013,87(5):2455-2462.
[5] Wise HM,Hutchinson EC,Jagger BW,et al.Identification of a novel splice variant form of the influenza A virus M2 ion channel with an antigenically distinct ectodomain [J].PLoS Pathog,2012,8(11):e1002998.
[6] Selman M,Dankar SK,Forbes NE,et al.Adaptive mutation in influenza A virus non-structural gene is linked to host switching and induces a novel protein by alternative splicing [J].Emerg Microbes Infect,2012,1(11):e42.
[7] 傅伟杰,胡茂红,刘晓青,等.江西省1例H10N8禽流感重症肺炎病例回顾性分析[J].中国公共卫生,2014,30(06):818-819.Fu WJ,Hu MH,Liu XQ,et al.Retrospective analysis of a case of severe pneumonia caused by H10N8 avian influenza in JiangxiProvince [J].Chin J Public Health,2014,30(6):818-819.
[8] Chen Y,Liang WF,Yang SG,et al.Human infections with the emerging avian influenza A H7N9 virus from wet market poultry:clinical analysis and characterisation of viral genome [J].Lancet,2013,381(9881):1916-1925.
[9] World Health Organization.Monthly Risk Assessment Summary.http://www.who.int/influenza/human_animal_interface/HAI_Risk_Assessment/en/.
[10] Shi JZ,Deng GH,Kong HH,et al.H7N9 virulent mutants detected in chickens in China pose an increased threat to humans [J].Cell Res,2017,27(12):1409-1421.
[11] Thangavel RR,Bouvier NM.Animal models for influenza virus pathogenesis,transmission,and immunology [J].J Immunol Methods,2014,410:60-79.
[12] Sally DA,Taubenberger JK,Bray M.The use of nonhuman primates in research on seasonal,pandemic and avian influenza,1893-2014 [J].Antiviral Res,2015,117:75-98.
[13] 邓少嫦,张钰,黄韧.禽流感的哺乳类动物模型研究进展[J].中国比较医学志,2009,19(12):40-43+75.Deng SC,Zhang Y,Huang R,et al.Advances in research on animal models for H5N1 avian influenza [J].Chin J Comp Med,2009,19(12):40-43+75.
[14] Belser JA,Tumpey TM.H5N1 pathogenesis studies in mammalian models [J].Virus Res,2013,178(1):168-185.
[15] de Graaf M,Fouchier RA.Role of receptor binding specificity in influenza A virus transmission and pathogenesis [J].EMBO J,2014,33(8):823-841.
[16] Matsuoka Y,Lamirande EW,Subbarao K.The ferret model for influenza [J].Curr Protoc Microbiol,2009,Chapter 15:Unit 15G.2.
[17] 邓巍,许黎黎,鲍琳琳,等.雪貂感染H7N9禽流感病毒动物模型的建立[J].中国比较医学杂志,2014,24(1):68-71+14.Deng W,Xu LL,Bao LL,et al.The ferret models for studying the novel avian-origin human influenza A (H7N9)virus [J].Chin J Comp Med,2014,24(1):68-71+14.
[18] 张涛,徐娟,杨凤梅,等.流感病毒感染雪貂的标准化操作程序建立[J].动物医学进展,2014,35(10):25-29.Zhang T,Xu J,Yang TM,et al.Standard operation procedures of Influenza virus infertion model in ferret [J].Progr Vet Med,2014,35(10):25-29.
[19] Peng XX,Alfoldi J,Gori K,et al.The draft genome sequence of the ferret (Mustela putorius furo) facilitates study of human respiratory disease [J].Nat Biotechnol,2014,32(12):1250-1255.
[20] Ryan KA,Slack GS,Marriott AC,et al.Cellular immune response to human influenza viruses differs between H1N1 and H3N2 subtypes in the ferret lung [J].PLoS One,2018,13:e0202675.
[21] Sun HL,Kaplan BS,Guan MH,et al.Pathogenicity and transmission of a swine influenza A(H6N6) virus [J].Emerg Microbes Infect,2017,6:e17.
[22] Li XY,Shi JZ,Guo J,et al.Genetics,receptor binding property,and transmissibility in mammals of naturally isolated H9N2 avian influenza viruses [J].PLoS Pathog,2014,10:e1004508.
[23] Peng BH,Yun N,Chumakova O,et al.Neuropathology of H5N1 virus infection in ferrets [J].Vet Microbiol,2012,156(3-4):294-304.
[24] Herfst S,Mok CKP,van den Brand JMA,et al.Human clade 2.3.4.4 A/H5N6 influenza virus lacks mammalian adaptation markers and does not transmit via the airborne route between ferrets [J].mSphere,2018,3:e00405-17.
[25] Noh JY,Lee DH,Yuk SS,et al.Limited pathogenicity and transmissibility of Korean highly pathogenic avian influenza H5N6 clade 2.3.4.4 in ferrets [J].Transbound Emerg Dis,2018,65(4):923-926.
[26] Pulit-Penaloza JA,Sun XJ,Creager HM,et al.Pathogenesis and transmission of novel highly pathogenic avian influenza H5N2 and H5N8 viruses in ferrets and mice [J].J Virol,2015,89(20):10286-10293.
[27] Zhang QY,Shi JZ,Deng GH,et al.H7N9 influenza viruses are transmissible in ferrets by respiratory droplet [J].Science,2013,341(6144):410-414.
[28] Watanabe T,Kiso M,Fukuyama S,et al.Characterization of H7N9 influenza A viruses isolated from humans [J].Nature,2013,501(7468):551-555.
[29] Imai M,Watanabe T,Kiso M,et al.A highly pathogenic avian H7N9 influenza virus isolated from a human is lethal in some ferrets infected via respiratory droplets [J].Cell Host & Microbe,2017,22(5):615-626.e618.
[30] Xiao CC,Ma WJ,Sun N,et al.PB2-588 V promotes the mammalian adaptation of H10N8,H7N9 and H9N2 avian influenza viruses [J].Sci Rep,2016,6:19474.
[31] Zhou J,Wei JJ,Choy KT,et al.Defining the sizes of airborne particles that mediate influenza transmission in ferrets [J].Proc Natl Acad Sci U S A,2018,115(10):2386-2392.
[32] Buhnerkempe MG,Gostic K,Park M,et al.Mapping influenza transmission in the ferret model to transmission in humans [J].elife,2015,4:e07969.
[33] Stevens J,Blixt O,Tumpey TM,et al.Structure and receptor specificity of the hemagglutinin from an H5N1 influenza virus [J].Science,2006,312(5772):404-410.
[34] Tumpey TM,Maines TR,Van Hoeven N,et al.A two-amino acid change in the hemagglutinin of the 1918 influenza virus abolishes transmission [J].Science,2007,315(5812):655-659.
[35] Xiong XL,Martin SR,Haire LF,et al.Receptor binding by an H7N9 influenza virus from humans [J].Nature,2013,499(7459):496-499.
[36] Richard M,Schrauwen EJA,de Graaf M,et al.Limited airborne transmission of H7N9 influenza A virus between ferrets [J].Nature,2013,501(7468):560-563.
[37] Zhu H,Wang D,Kelvin DJ,et al.Infectivity,transmission,and pathology of human-isolated H7N9 influenza virus in ferrets and pigs [J].Science,2013,341(6142):183-186.
[38] Lowen AC,Mubareka S,Steel J,et al.Influenza virus transmission is dependent on relative humidity and temperature [J].PLoS Pathog,2007,3(10):1470-1476.
[39] Shi JZ,Deng GH,Ma SJ,et al.Rapid evolution of H7N9 highly pathogenic viruses that emerged in China in 2017 [J].Cell Host Microbe,2018,24(4):558-568.
[40] Yang W,Yin X,Guan L,et al.A live attenuated vaccine prevents replication and transmission of H7N9 highly pathogenic influenza viruses in mammals [J].Emerg Microbes Infect,2018,7(1):153.
[41] Kong HH,Zhang QY,Gu CY,et al.A live attenuated vaccine prevents replication and transmission of H7N9 virus in mammals [J].Sci Rep,2015,5:11233.
[42] Chen ZY,Baz M,Lu J,et al.Development of a high-yield live attenuated H7N9 influenza virus vaccine that provides protection against homologous and heterologous H7 wild-type viruses in ferrets [J].J Virol,2014,88(12):7016-7023.
[43] Hatta M,Zhong GX,Chiba S,et al.Effectiveness of whole,inactivated,low pathogenicity influenza A(H7N9) vaccine against antigenically distinct,highly pathogenic H7N9 virus [J].Emerg Infect Dis,2018,24(10):1910-1913.
[44] Wang LL,Liu SY,Chen HW,et al.Generation of a live attenuated influenza vaccine that elicits broad protection in mice and ferrets [J].Cell Host & Microbe,2017,21(3):334-343.
[45] Rudenko L,Kiseleva I,Krutikova E,et al.Two live attenuated vaccines against recent low and highly pathogenic H7N9 influenza viruses are safe and immunogenic in ferrets [J].Vaccines,2018,6(4).pii:E74.
[46] Wei SH,Yang JR,Wu HS,et al.Human infection with avian influenza A H6N1 virus:an epidemiological analysis [J].Lancet Respir Med,2013,1(10):771-778.
[47] Zhang RS,Chen TM,Ou XH,et al.Clinical,epidemiological and virological characteristics of the first detected human case of avian influenza A(H5N6) virus [J].Infect Genet Evol,2016,40:236-242.
[48] 郭元吉,李建国,程小雯,等.禽H9N2亚型流感病毒能感染人的发现[J].中华实验和临床病毒学杂志,1999,13(2):105-108.Guo YJ,Li JG,Cheng XW,et al.Discovery of men infected by avian influenza A (H9N2) virus[J].Chin J Exp Clin Virol,1999,13(2):105-108.
[49] Butt KM,Smith GJ,Chen HL,et al.Human infection with an avian H9N2 influenza A virus in Hong Kong in 2003 [J].J Clin Microbiol,2005,43(11):5760-5767.
[50] Shi JZ,Deng GH,Liu PH,et al.Isolation and characterization of H7N9 viruses from live poultry markets — Implication of the source of current H7N9 infection in humans [J].Chin Sci Bull,2013,58(16):1857-1863.
[51] Liu D,Shi WF,Shi Y,et al.Origin and diversity of novel avian influenza A H7N9 viruses causing human infection:phylogenetic,structural,and coalescent analyses [J].Lancet,2013,381(9881):1926-1932.