HA蛋白位点变异影响H7N9亚型流感病毒特性的研究进展

doi:10.11843/j.issn.0366-6964.2021.08.003

Abstract

Abstract: In the spring of 2013, human infections with H7N9 subtype avian influenza emerged in China, posing serious threats to both poultry farming and public health. Additionally, highly pathogenic H7N9 variants with insertional mutation at the cleavage site of hemagglutinin (HA) protein yet evolved during the fifth epidemic wave. As the most abundantly expressed glycoprotein on the surface of influenza A virus, HA protein plays crucial roles in the viral lifecycle such as mediating the linkage between virus and host cell surface receptors, promoting the fusion between viral envelope and cell membrane, and stimulating the production of neutralizing antibodies. In this review, we briefly summarized the structure and function of HA protein, and the research progress of functional amino acid variations effecting on H7N9 biological properties, in order to provide important reference for in-depth analysis of the role of HA protein in H7N9 infection and pathogenesis.

Key words: influenza virus, H7N9, HA protein, functional amino acid sites, infection and pathogenesis

CLC Number:

S852.659.5

YAN Yayao, GU Min, LIU Xiufan. Advance in the Influence of Amino Acid Variation in HA Protein on the Biological Properties of H7N9 Subtype Influenza Virus[J]. Acta Veterinaria et Zootechnica Sinica, 2021, 52(8): 2093-2106.

References 96

[1]	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.
[2]	SHI J Z, DENG G H, KONG H H, et al. H7N9 virulent mutants detected in chickens in China pose an increased threat to humans[J]. Cell Res, 2017, 27(12):1409-1421.
[3]	SU S, GU M, LIU D, et al. Epidemiology, evolution, and pathogenesis of H7N9 influenza viruses in five epidemic waves since 2013 in China[J]. Trends Microbiol, 2017, 25(9):713-728.
[4]	Food and Agriculture Organization. H7N9 situation update[EB/OL].[2021-07-07]. http://www.fao.org/ag/againfo/programmes/en/empres/H7N9/situation_update.html.
[5]	QIU Y, SUN R Z, HOU G Y, et al. Novel reassortant H7N2 originating from the H7N9 highly pathogenic avian influenza viruses in China, 2019[J]. J Infect, 2019, 79(5):462-470.
[6]	WU H B, LU R F, PENG X M, et al. Molecular characterization of a novel reassortant H7N6 subtype avian influenza virus from poultry in Eastern China, in 2016[J]. Arch Virol, 2017, 162(5):1341-1347.
[7]	LI C J, CHEN H L. H7N9 influenza virus in China[J]. Cold Spring Harb Perspect Med, 2020:a038349.
[8]	SHI J Z, DENG G H, MA S J, et al. Rapid evolution of H7N9 highly pathogenic viruses that emerged in China in 2017[J]. Cell Host Microbe, 2018, 24(4):558-568.
[9]	JIANG W M, HOU G Y, LI J P, et al. Antigenic variant of highly pathogenic avian influenza A(H7N9) virus, China, 2019[J]. Emerging Infect Dis, 2020, 26(2):379-380.
[10]	YU D S, XIANG G F, ZHU W F, et al. The re-emergence of highly pathogenic avian influenza H7N9 viruses in humans in mainland China, 2019[J]. Euro Surveill, 2019, 24(21):1900273.
[11]	WEBSTER R G, BEAN W J, GORMAN O T, et al. Evolution and ecology of influenza A viruses[J]. Microbiol Rev, 1992, 56(1):152-179.
[12]	VASIN A V, TEMKINA O A, EGOROV V V, et al. Molecular mechanisms enhancing the proteome of influenza A viruses:an overview of recently discovered proteins[J]. Virus Res, 2014, 185:53-63.
[13]	WU Y, WU Y, TEFSEN B, et al. Bat-derived influenza-like viruses H17N10 and H18N11[J]. Trends Microbiol, 2014, 22(4):183-191.
[14]	WU A P, SU C H, WANG D Y, et al. Sequential reassortments underlie diverse influenza H7N9 genotypes in China[J]. Cell Host Microbe, 2013, 14(4):446-452.
[15]	LIU D, SHI W F, 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.
[16]	ZHANG J H, YE H J, LI H N, et al. Evolution and antigenic drift of influenza A (H7N9) viruses, China, 2017-2019[J]. Emerg Infect Dis, 2020, 26(8):1906-1911.
[17]	崔欢. 一株鹌鹑源甲型H7N9亚型流感病毒的致病性及传播能力研究[D]. 保定:河北农业大学, 2020.CUI H. Pathogenicity and transmissibility of influenza A (H7N9) Virus isolated from Quail[D]. Baoding:Hebei Agricultural University, 2020.(in Chinese)
[18]	MA M J, YANG Y, FANG L Q. Highly pathogenic avian H7N9 influenza viruses:recent challenges[J]. Trends Microbiol, 2019, 27(2):93-95.
[19]	BI Y H, LI J, LI S Q, et al. Dominant subtype switch in avian influenza viruses during 2016-2019 in China[J]. Nat Commun, 2020, 11(1):5909.
[20]	CHANG P X, SEALY J E, SADEYEN J R, et al. Amino acid residue 217 in the hemagglutinin glycoprotein is a key mediator of avian influenza H7N9 virus antigenicity[J]. J Virol, 2018, 93(1):e01627-18.
[21]	CHANG P X, SEALY J E, SADEYEN J R, et al. Immune escape adaptive mutations in the H7N9 avian influenza hemagglutinin protein increase virus replication fitness and decrease pandemic potential[J]. J Virol, 2020, 94(1):e00216-20.
[22]	RUSSELL C J. Acid-induced membrane fusion by the hemagglutinin protein and its role in influenza virus biology[J]. Curr Top Microbiol Immunol, 2014, 385:93-116.
[23]	LIU D, ZHANG Z J, HE L H, et al. Characteristics of the emerging chicken-origin highly pathogenic H7N9 viruses:a new threat to public health and poultry industry[J]. J Infect, 2018, 76(2):217-220.
[24]	BAI R, SIKKEMA R S, MUNNINK B B O, et al. Exploring utility of genomic epidemiology to trace origins of highly pathogenic influenza A/H7N9 in Guangdong[J]. Virus Evol, 2020, 6(2):veaa097.
[25]	SUN X J, BELSER J A, YANG H, et al. Identification of key hemagglutinin residues responsible for cleavage, acid stability, and virulence of fifth-wave highly pathogenic avian influenza A(H7N9) viruses[J]. Virology, 2019, 535:232-240.
[26]	CHUTINIMITKUL S, VAN RIEL D, MUNSTER V J, et al. In vitro assessment of attachment pattern and replication efficiency of H5N1 influenza A viruses with altered receptor specificity[J]. J Virol, 2010, 84(13):6825-6833.
[27]	WAN H Q, SORRELL E M, SONG H C, et al. Replication and transmission of H9N2 influenza viruses in ferrets:evaluation of pandemic potential[J]. PLoS One, 2008, 3(8):e2923.
[28]	SHIRYAEV S A, CHERNOV A V, GOLUBKOV V S, et al. High-resolution analysis and functional mapping of cleavage sites and substrate proteins of furin in the human proteome[J]. PLoS One, 2013, 8(1):e54290.
[29]	ISIN B, DORUKER P, BAHAR I. Functional motions of influenza virus hemagglutinin:a structure-based analytical approach[J]. Biophys J, 2002, 82:569-581.
[30]	SHI Y, WU Y, ZHANG W, et al. Enabling the ‘host jump’:structural determinants of receptor-binding specificity in influenza A viruses[J]. Nat Rev Microbiol, 2014, 12(12):822-831.
[31]	SHI Y, ZHANG W, WANG F, et al. Structures and receptor binding of hemagglutinins from human-infecting H7N9 influenza viruses[J]. Science, 2013, 342(6155):243-247.
[32]	RUSSELL R J, STEVENS D J, HAIRE L F, et al. Avian and human receptor binding by hemagglutinins of influenza A viruses[J]. Glycoconj J, 2006, 23(1-2):85-92.
[33]	BANKS J, SPEIDEL E S, MOORE E, et al. Changes in the haemagglutinin and the neuraminidase genes prior to the emergence of highly pathogenic H7N1 avian influenza viruses in Italy[J]. Arch Virol, 2001, 146(5):963-973.
[34]	GU M, LI Q H, GAO R Y, et al. The T160A hemagglutinin substitution affects not only receptor binding property but also transmissibility of H5N1 clade 2. 3.4 avian influenza virus in guinea pigs[J]. Vet Res, 2017, 48(1):7.
[35]	ROSENTHAL P B, ZHANG X D, FORMANOWSKI F, et al. Structure of the haemagglutinin-esterase-fusion glycoprotein of influenza C virus[J]. Nature, 1998, 396(6706):92-96.
[36]	PAUL S S, MOK C K, MAK T M, et al. A cross-clade H5N1 influenza A virus neutralizing monoclonal antibody binds to a novel epitope within the vestigial esterase domain of hemagglutinin[J]. Antiviral Res, 2017, 144:299-310.
[37]	平继辉. H9N2亚型禽流感病毒抗原变异及感染哺乳动物分子机制的研究[D]. 南京:南京农业大学, 2008.PING J H. The molecular basis of antigenic variation and crossing host barrier to infect mammalian model of H9N2 avian influenza viruses[D]. Nanjing:Nanjing Agricultural University, 2008.(in Chinese)
[38]	DUNAND C J H, LEON P E, HUANG M, et al. Both neutralizing and non-neutralizing human H7N9 influenza vaccine-induced monoclonal antibodies Confer Protection[J]. Cell Host Microbe, 2016, 19(6):800-813.
[39]	EKIERT D C, BHABHA G, ELSLIGER M A, et al. Antibody recognition of a highly conserved influenza virus epitope[J]. Science, 2009, 324(5924):246-251.
[40]	EKIERT D C, FRIESEN R H E, BHABHA G, et al. A highly conserved neutralizing epitope on group 2 influenza A viruses[J]. Science, 2011, 333(6044):843-850.
[41]	EKIERT D C, KASHYAP A K, STEEL J, et al. Cross-neutralization of influenza A viruses mediated by a single antibody loop[J]. Nature, 2012, 489(7417):526-532.
[42]	BYRD-LEOTIS L, GALLOWAY S E, AGBOGU E, et al. Influenza hemagglutinin (HA) stem region mutations that stabilize or destabilize the structure of multiple HA subtypes[J]. J Virol, 2015, 89(8):4504-4516.
[43]	WAGNER R, HERWIG A, AZZOUZ N, et al. Acylation-mediated membrane anchoring of avian influenza virus hemagglutinin is essential for fusion pore formation and virus infectivity[J]. J Virol, 2005, 79(10):6449-6458.
[44]	TAKEDA M, LESER G P, RUSSELL C J, et al. Influenza virus hemagglutinin concentrates in lipid raft microdomains for efficient viral fusion[J]. Proc Natl Acad Sci U S A, 2003, 100(25):14610-14617.
[45]	OHUCHI M, OHUCHI R, MATSUMOTO A. Control of biological activities of influenza virus hemagglutinin by its carbohydrate moiety[J]. Microbiol Immunol, 1999, 43(12):1071-1076.
[46]	YIN Y C, ZHANG X J, QIAO Y Y, et al. Glycosylation at 11Asn on hemagglutinin of H5N1 influenza virus contributes to its biological characteristics[J]. Vet Res, 2017, 48(1):81.
[47]	ROBERTS P C, GARTEN W, KLENK H D. Role of conserved glycosylation sites in maturation and transport of influenza A virus hemagglutinin[J]. J Virol, 1993, 67(6):3048-3060.
[48]	VARKI A, SCHAUER R. Sialic acids[M]//VARKI A, CUMMINGS R D, ESKO J D, et al. Essentials of Glycobiology. 2nd ed. Cold Spring Harbor, N. Y.:Cold Spring Harbor Laboratory Press, 2009.
[49]	TRAVING C, SCHAUER R. Structure, function and metabolism of sialic acids[J]. Cell Mol Life Sci, 1998, 54(12):1330-1349.
[50]	ROGERS G N, PRITCHETT T J, LANE J L, et al. Differential sensitivity of human, avian, and equine influenza A viruses to a glycoprotein inhibitor of infection:selection of receptor specific variants[J]. Virology, 1983, 131(2):394-408.
[51]	MAIR C M, LUDWIG K, HERRMANN A, et al. Receptor binding and pH stability-how influenza A virus hemagglutinin affects host-specific virus infection[J]. Biochim Biophys Acta, 2014, 1838(4):1153-1168.
[52]	XU Y, PENG RC, ZHANG W, et al. Avian-to-Human receptor-binding adaptation of avian H7N9 influenza virus hemagglutinin[J]. Cell Rep, 2019, 29(8):2217-2228.
[53]	DE VRIES R P, PENG W J, GRANT O C, et al. Three mutations switch H7N9 influenza to human-type receptor specificity[J]. PLoS Pathog, 2017, 13(6):e1006390.
[54]	THARAKARAMAN K, JAYARAMAN A, RAMAN R, et al. Glycan receptor binding of the influenza A virus H7N9 hemagglutinin[J]. Cell, 2013, 153(7):1486-1493.
[55]	BRADLEY K C, GALLOWAY S E, LASANAJAK Y, et al. Analysis of influenza virus hemagglutinin receptor binding mutants with limited receptor recognition properties and conditional replication characteristics[J]. J Virol, 2011, 85(23):12387-12398.
[56]	MATROSOVICH M, TUZIKOV A, BOVIN N, et al. Early alterations of the receptor-binding properties of H1, H2, and H3 avian influenza virus hemagglutinins after their introduction into mammals[J]. J Virol, 2000, 74(18):8502-8512.
[57]	PENG W J, BOUWMAN K M, MCBRIDE R, et al. Enhanced human-type receptor binding by ferret-transmissible H5N1 with a K193T mutation[J]. J Virol, 2018, 92(10):e02016-17.
[58]	GAMBARYAN A S, MATROSOVICH T Y, PHILIPP J, et al. Receptor-binding profiles of H7 subtype influenza viruses in different host species[J]. J Virol, 2012, 86(8):4370-4379.
[59]	ZHENG B J, CHAN K H, ZHANG A J X, et al. D225G mutation in hemagglutinin of pandemic influenza H1N1(2009) virus enhances virulence in mice[J]. Exp Biol Med, 2010, 235(8):981-988.
[60]	GLASER L, STEVENS J, ZAMARIN D, et al. A single amino acid substitution in 1918 influenza virus hemagglutinin changes receptor binding specificity[J]. J Virol, 2005, 79(17):11533-11536.
[61]	SANTOS J J S, ABENTE E J, OBADAN A O, et al. Plasticity of amino acid residue 145 near the receptor binding site of H3 swine influenza A viruses and its impact on receptor binding and antibody recognition[J]. J Virol, 2019, 93(2):e01413-18.
[62]	LI Y, BOSTICK D L, SULLIVAN C B, et al. Single hemagglutinin mutations that alter both antigenicity and receptor binding avidity influence influenza virus antigenic clustering[J]. J Virol, 2013, 87(17):9904-9910.
[63]	XIONG X L, COOMBS P J, MARTIN S R, et al. Receptor binding by a ferret-transmissible H5 avian influenza virus[J]. Nature, 2013, 497(7449):392-396.
[64]	LAZAROWITZ S G, COMPANS R W, CHOPPIN P W. Proteolytic cleavage of the hemagglutinin polypeptide of influenza virus. Function of the uncleaved polypeptide HA[J]. Virology, 1973, 52(1):199-212.
[65]	STEINHAUER D A. Role of hemagglutinin cleavage for the pathogenicity of influenza virus[J]. Virology, 1999, 258(1):1-20.
[66]	WALKER J A, MOLLOY S S, THOMAS G, et al. Sequence specificity of furin, a proprotein-processing endoprotease, for the hemagglutinin of a virulent avian influenza virus[J]. J Virol, 1994, 68(2):1213-1218.
[67]	HORIMOTO T, NAKAYAMA K, SMEEKENS S P, et al. Proprotein-Processing endoproteases PC6 and furin both activate hemagglutinin of virulent avian influenza viruses[J]. J Virol, 1994, 68(9):6074-6078.
[68]	ZHIRNOV O P, IKIZLER M R, WRIGHT P F. Cleavage of influenza a virus hemagglutinin in human respiratory epithelium is cell associated and sensitive to exogenous antiproteases[J]. J Virol, 2002, 76(17):8682-8689.
[69]	WEBSTER R G, ROTT R. Influenza virus a pathogenicity:the pivotal role of hemagglutinin[J]. Cell, 1987, 50(5):665-666.
[70]	CROSS K J, LANGLEY W A, RUSSELL R J, et al. Composition and functions of the influenza fusion peptide[J]. Protein Pept Lett, 2009, 16(7):766-778.
[71]	HOLDBROOK D A, BURMANN B M, HUBER R G, et al. A spring-loaded mechanism governs the clamp-like dynamics of the skp chaperone[J]. Structure, 2017, 25(7):1079-1088.
[72]	WEBER T, PAESOLD G, GALLI C, et al. Evidence for H+-induced insertion of influenza hemagglutinin HA2 N-terminal segment into viral membrane[J]. J Biol Chem, 1994, 269(28):18353-18358.
[73]	GRUENKE J A, ARMSTRONG R T, NEWCOMB W W, et al. New insights into the spring-loaded conformational change of influenza virus hemagglutinin[J]. J Virol, 2002, 76(9):4456-4466.
[74]	WAGNER R, HEUERA D, WOLFF T, et al. N-glycans attached to hemagglutinin in the head region and the stem domain control growth of influenza viruses by different mechanisms[J]. Int Congr Ser, 2001, 1219:375-382.
[75]	SCHOLTISSEK C. Stability of infectious influenza A viruses to treatment at low pH and heating[J]. Arch Virol, 1985, 85(1-2):1-11.
[76]	GALLOWAY S E, REED M L, RUSSELL C J, et al. Influenza HA subtypes demonstrate divergent phenotypes for cleavage activation and pH of fusion:implications for host range and adaptation[J]. PLoS Pathog, 2013, 9(2):e1003151.
[77]	HERFST S, MOK C K P, VAN DEN BRAND J M A, 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(1):e00405-17.
[78]	GABBARD J D, DLUGOLENSKI D, VAN RIEL D, et al. Novel H7N9 influenza virus shows low infectious dose, high growth rate, and efficient contact transmission in the guinea pig model[J]. J Virol, 2014, 88(3):1502-1512.
[79]	RUSSIER M, YANG G H, REHG J E, et al. Molecular requirements for a pandemic influenza virus:an acid-stable hemagglutinin protein[J]. Prod Natl Acad Sci U S A, 2016, 113(6):1636-1641.
[80]	RUSSELL C J, HU M, OKDA F A. Influenza hemagglutinin protein stability, activation, and pandemic risk[J]. Trends Microbiol, 2018, 26(10):841-853.
[81]	ZARAKET H, BRIDGES O A, RUSSELL C J. The pH of activation of the hemagglutinin protein regulates H5N1 influenza virus replication and pathogenesis in mice[J]. J Virol, 2013, 87(9):4826-4834.
[82]	YIN X, DENG G H, ZENG X Y, et al. Genetic and biological properties of H7N9 avian influenza viruses detected after application of the H7N9 poultry vaccine in China[J]. PLoS Pathog, 2021, 17(4):e1009561.
[83]	WANG Y, LV Y H, NIU X F, et al. L226Q mutation on influenza H7N9 virus hemagglutinin increases receptor-binding avidity and leads to biased antigenicity evaluation[J]. J Virol, 2020, 94(20):e00667-20.
[84]	HENSLEY S E, DAS S R, BAILEY A L, et al. Hemagglutinin receptor binding avidity drives influenza a virus antigenic drift[J]. Science, 2009, 326(5953):734-736.
[85]	DANIELS F S, DOWNIE J C, HAY A J, et al. Fusion mutants of the influenza virus hemagglutinin glycoprotein[J]. Cell, 1985, 40(2):431-439.
[86]	HE F, PRABAKARAN M, TAN Y R, et al. Development of dual-function ELISA for effective antigen and antibody detection against H7 avian influenza virus[J]. BMC Microbiol, 2013, 13:219.
[87]	IGNATIEVA A V, TIMOFEEVA T A, RUDNEVA I A, et al. Effect of amino acid substitutions in the small subunit of the avian H5N2 influenza virus hemagglutinin on selection of the mutants, resistant to neutralizing monoclonal antibodies[J]. Mol Biol, 2015, 49(2):303-311.
[88]	PING J H, LI C J, DENG G H, et al. Single-amino-acid mutation in the HA alters the recognition of H9N2 influenza virus by a monoclonal antibody[J]. Biochem Biophys Res Commun, 2008, 371(1):168-171.
[89]	CHEN Z Y, 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.
[90]	DANIELS P S, JEFFRIES S, YATES P, et al. The receptor-binding and membrane-fusion properties of influenza virus variants selected using anti-haemagglutinin monoclonal antibodies[J]. ENBO J, 1987, 6(5):1459-1465.
[91]	LI X, GAO Y M, YE Z P. A single amino acid substitution at residue 218 of hemagglutinin improves the growth of influenza A(H7N9) candidate vaccine viruses[J]. J Virol, 2019, 93(19):e00570-19.
[92]	LIU L Q, LU J, LI Z, et al. 220 mutation in the hemagglutinin of avian influenza A (H7N9) virus alters antigenicity during vaccine strain development[J]. Hum Vaccin Immunother, 2018, 14(3):532-539.
[93]	XU R, DE VRIES R P, ZHU X Y, et al. Preferential recognition of avian-like receptors in human influenza A H7N9 viruses[J]. Science, 2013, 342(6163):1230-1235.
[94]	RAMOS I, KRAMMER F, HAI R, et al. H7N9 influenza viruses interact preferentially with α2, 3-linked sialic acids and bind weakly to α2, 6-linked sialic acids[J]. J Gen Virol, 2013, 94(11):2417-2423.
[95]	LIN Y P, WHARTON S A, MARTÍN J, et al. Adaptation of egg-grown and transfectant influenza viruses for growth in mammalian cells:selection of hemagglutinin mutants with elevated pH of membrane fusion[J]. Virology, 1997, 233(2):402-410.
[96]	SCHRAUWEN E J, RICHARD M, BURKE D F, et al. Amino acid substitutions that affect receptor binding and stability of the hemagglutinin of influenza A/H7N9 Virus[J]. J Virol, 2016, 90(7):3794-3799.

Advance in the Influence of Amino Acid Variation in HA Protein on the Biological Properties of H7N9 Subtype Influenza Virus

PDF (PC)

Knowledge

Abstract

Cite this article

share this article

References 96

Related Articles 15

Recommended Articles

Metrics

Comments

[1]	LÜ Yadi, YANG Jie, XIE Wenting, XU Ting, CHEN Ruiai. Construction and Evaluation of the Immune Effect of Recombinant Genotype Ⅶ NDV Strain Co-expressing Membrane-bound and Water-soluble HA Protein of Avian Influenza Virus H9N2 [J]. Acta Veterinaria et Zootechnica Sinica, 2024, 55(5): 2123-2134.
[2]	MAO Qiuyan, ZHOU Shuning, LIU Shuo, PENG Cheng, YIN Xin, ZHANG Yaxin, ZHOU Wanting, LI Jinping, HOU Guangyu, JIANG Wenming, SONG Houhui, LIU Hualei. Establishment and Application of Fluorescent Quantitative RT-PCR for Detection of H3 Subtype Avian Influenza Virus [J]. Acta Veterinaria et Zootechnica Sinica, 2024, 55(3): 1137-1146.
[3]	YANG Zhiyi, WANG Xinkai, SHI Yuting, FU Siyuan, ZHANG Yuxin, CAO Chenfu, JIA Weixin. Establishment of Nucleic Acid Detection Methods for Avian Influenza H5 Subtype Based on CRISPR-Cas13a and RT-RAA [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(9): 3803-3811.
[4]	SUN Min, HAO Fei, ZHANG Wenwen, LI Wenliang, YANG Leilei, MAO Li, CHENG Zilong, LIU Maojun. The Antiviral Activity of Goat Interferon Alpha to Caprine Parainfluenza Virus 3 [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(2): 736-743.
[5]	ZHANG Ao, TAN Bin, LIU Kexin, LIU Jiali, ZHANG Shuqin. Genomic Characterization Analysis of a H1N1 Subtype Swine Influenza Virus [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(11): 4866-4871.
[6]	ZHOU Yong, LI Zhixin, LU Hongwei, SUN Yan, LI Tian, DU Fanshu, PU Juan. Surveillance and Outbreak Analysis of H5 and H7N9 Subtypes of Highly Pathogenic Avian Influenza in China [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(9): 3093-3106.
[7]	CUI Mingxian, WANG Xingbo, HUANG Yanming, BIAN Xiyi, FENG Mengke, YAN Yan, DONG Weiren, ZHOU Jiyong. Genetic Characterization and Evolution of Three Strains of H3N2 Avian Influenza Viruses [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(11): 4116-4122.
[8]	LI Jingyun, LIAN Pengjing, BAI Yu, XI Liuqing, ZHANG Zihui, NIU Xiaofei, YANG Junqi, QIAO Jian. The Impact of H9N2 Subtype Avian Influenza Viral Infection on the Gut Flora in Mice [J]. Acta Veterinaria et Zootechnica Sinica, 2021, 52(5): 1359-1368.
[9]	LI Li, TANG Guoyi, FENG Helong, XUE Yuhan, REN Zhu, WANG Guokang, JIA Miaomiao, SHANG Yu, LUO Qingping, SHAO Huabin, WEN Guoyuan. Evaluation of Immune Efficacy of H9 Subtype Avian Influenza Virus Inactivated Vaccine Based on Mosaic HA Sequence [J]. Acta Veterinaria et Zootechnica Sinica, 2021, 52(12): 3569-3577.
[10]	ZHAO Yuzhong, DING Guofei, LIU Jiaqi, LI Li, LI Yingchao, WANG Bin, SHAO Qingyuan, FENG Jian, GUO Lihong, LIU Sidang, XIAO Yihong. Molecular Characterization of a H9N2 Subtype Swine Influenza Virus [J]. Acta Veterinaria et Zootechnica Sinica, 2020, 51(9): 2312-2318.
[11]	YANG Shuaike, ZOU Jiahui, JIANG Meijun, ZHAO Yaxin, CAO Jiyue, ZHOU Hongbo. Effect of ALG5 on Swine Influenza Virus Replication [J]. Acta Veterinaria et Zootechnica Sinica, 2020, 51(7): 1719-1727.
[12]	ZHAO Yuzhong, DING Guofei, LIU Jiaqi, LI Li, LI Yingchao, WANG Bin, SHAO Qingyuan, FENG Jian, GUO Lihong, LIU Sidang, XIAO Yihong. Genomic and Evolutionary Characterization of a H1N1 Swine Influenza Virus and Its Pathogenicity in Mice [J]. Acta Veterinaria et Zootechnica Sinica, 2020, 51(7): 1768-1774.
[13]	WANG Suchun, ZHONG Huanxiang, JIANG Nan, JIANG Lijian, PAN Zihao, SUN Fuliang, LIU Hualei, HUANG Baoxu, WANG Kaicheng. Establishment of the Quadruple Real-time Fluorescence RT-PCR for Detection of H5, H7 and H9 Subtypes Avian Influenza Virus [J]. Acta Veterinaria et Zootechnica Sinica, 2020, 51(6): 1429-1437.
[14]	ZHAO Bingqian, LUO Chang, LIU Jianxin, LI Huizi, ZHANG Pengtao, YU Xianglong, LIU Boyang, NING Zhangyong. Inhibitory Effect of Forsythiae Fructus Aqueous Extracts on the Proliferation of Avian Influenza Virus and the Expression of Inflammation Factors in vitro [J]. Acta Veterinaria et Zootechnica Sinica, 2020, 51(6): 1466-1474.
[15]	YU Liangzheng, DING Yangbao, HE Jianqiao, LIU Linlin, CUI Baiyang, WEI Zuzhang, OUYANG Kang, HUANG Weijian, CHEN Ying. Phylogenetic Analysis of Four Strains of H3N2 Swine Influenza Virus Isolated from the Same Pig Farm [J]. Acta Veterinaria et Zootechnica Sinica, 2020, 51(4): 801-809.