A GFP expressing influenza a virus to report in vivo tropism and protection by a matrix protein 2 ectodomain-specific monoclonal antibody

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  De Baets, Sarah ^a,b,c   Verhelst, Judith ^a,b   Van Den Hoecke, Silvie ^a,b   Smet, Anouk ^a,b   Schotsaert, Michael ^a,b,d   Job, Emma R ^a,b   Roose, Kenny ^a,b   Schepens, Bert ^a,b   Fiers, Walter ^a,b   Saelens, Xavier ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c Labo Medische Analyse Centrum Voor Radio Immunologie   (Belgium)

^d MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ANTIVIRUS AGENT; GREEN FLUORESCENT PROTEIN; MATRIX PROTEIN 2; MONOCLONAL ANTIBODY; NONSTRUCTURAL PROTEIN 1; OSELTAMIVIR; PROTEIN; UNCLASSIFIED DRUG; FUSION PROTEIN; INS1 PROTEIN, INFLUENZA VIRUS; M2 PROTEIN, INFLUENZA A VIRUS; MATRIX PROTEIN; VIRAL NONSTRUCTURAL PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN PRESENTATION; ARTICLE; BONE MARROW CELL; CELLS BY BODY ANATOMY; CONTROLLED STUDY; DENDRITIC CELL; DIMERIZATION; DISEASE SEVERITY; DRUG EFFICACY; EPITHELIUM CELL; FLOW CYTOMETRY; GENE EXPRESSION; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; INFLUENZA; INFLUENZA VIRUS A; MONOCYTE; MOUSE; NONHUMAN; OPEN READING FRAME; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN STABILITY; REPORTER GENE; SEQUENCE ANALYSIS; TROPISM; ANIMAL; CELL CULTURE; CHEMISTRY; DOG; DRUG EFFECT; GENETICS; INFLUENZA A VIRUS; MDCK CELL LINE; METABOLISM; ORTHOMYXOVIRUS INFECTION; PHYSIOLOGY; PREVENTION AND CONTROL; VIRAL TROPISM; VIROLOGY; VIRUS REPLICATION;

INFLUENZA A VIRUS; MUS; ORTHOMYXOVIRIDAE;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIVIRAL AGENTS; CELLS, CULTURED; DENDRITIC CELLS; DOGS; GREEN FLUORESCENT PROTEINS; INFLUENZA A VIRUS; MADIN DARBY CANINE KIDNEY CELLS; MICE; MONOCYTES; ORTHOMYXOVIRIDAE INFECTIONS; OSELTAMIVIR; PROTEIN STABILITY; RECOMBINANT FUSION PROTEINS; VIRAL MATRIX PROTEINS; VIRAL NONSTRUCTURAL PROTEINS; VIRAL TROPISM; VIRUS REPLICATION;

EID: 84926299054     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0121491     Document Type: Article

References (60)

1. Everitt AR, Clare S, Pertel T, John SP, Wash RS, Smith SE, et al. IFITM3 restricts the morbidity and mortality associated with influenza. Nature. 2012; 484(7395):519-23. doi: 10.1038/nature10921 PMID: 22446628
2. Katz JM, Plowden J, Renshaw-Hoelscher M, Lu X, Tumpey TM, Sambhara S. Immunity to influenza: the challenges of protecting an aging population. Immunologic research. 2004; 29(1-3):113-24. PMID: 15181286
3. Poehling KA, Edwards KM, Griffin MR, Szilagyi PG, Staat MA, Iwane MK, et al. The burden of influenza in young children, 2004-2009. Pediatrics. 2013; 131(2):207-16. doi: 10.1542/peds.2012-1255 PMID: 23296444
4. Peiris JS, Hui KP, Yen HL. Host response to influenza virus: protection versus immunopathology. Curr Opin Immunol. 2010; 22(4):475-81. doi: 10.1016/j.coi.2010.06.003 PMID: 20594815
5. Sridhar S, Begom S, Bermingham A, Hoschler K, Adamson W, Carman W, et al. Cellular immune correlates of protection against symptomatic pandemic influenza. Nature medicine. 2013; 19(10):1305-12. doi: 10.1038/nm.3350 PMID: 24056771
6. Michiels B, Govaerts F, Remmen R, Vermeire E, Coenen S. A systematic review of the evidence on the effectiveness and risks of inactivated influenza vaccines in different target groups. Vaccine. 2011; 29 (49):9159-70. doi: 10.1016/j.vaccine.2011.08.008 PMID: 21840359
7. Hertz T, Oshansky CM, Roddam PL, DeVincenzo JP, Caniza MA, Jojic N, et al. HLA targeting efficiency correlates with human T-cell response magnitude and with mortality from influenza A infection. Proc Natl Acad Sci U S A. 2013; 110(33):13492-7. doi: 10.1073/pnas.1221555110 PMID: 23878211
8. Brandes M, Klauschen F, Kuchen S, Germain RN. A systems analysis identifies a feedforward inflammatory circuit leading to lethal influenza infection. Cell. 2013; 154(1):197-212. doi: 10.1016/j.cell.2013.06.013 PMID: 23827683
9. Matrosovich MN, Matrosovich TY, Gray T, Roberts NA, Klenk HD. Human and avian influenza viruses target different cell types in cultures of human airway epithelium. Proc Natl Acad Sci U S A. 2004; 101 (13):4620-4. PMID: 15070767
10. Xiong X, Coombs PJ, Martin SR, Liu J, Xiao H, McCauley JW, et al. Receptor binding by a ferret-transmissible H5 avian influenza virus. Nature. 2013; 497(7449):392-6. doi: 10.1038/nature12144 PMID: 23615615
11. de Graaf M, Fouchier RA. Role of receptor binding specificity in influenza A virus transmission and pathogenesis. The EMBO journal. 2014; 33(8):823-41. doi: 10.1002/embj.201387442 PMID: 24668228
12. Connor RJ, Kawaoka Y, Webster RG, Paulson JC. Receptor specificity in human, avian, and equine H2 and H3 influenza virus isolates. Virology. 1994; 205(1):17-23. PMID: 7975212
13. Matrosovich M, Stech J, Klenk HD. Influenza receptors, polymerase and host range. Revue scientifique et technique. 2009; 28(1):203-17. PMID: 19618627
14. Naffakh N, Tomoiu A, Rameix-Welti MA, van der Werf S. Host restriction of avian influenza viruses at the level of the ribonucleoproteins. Annual review of microbiology. 2008; 62:403-24. doi: 10.1146/annurev.micro.62.081307.162746 PMID: 18785841
15. Heaton NS, Leyva-Grado VH, Tan GS, Eggink D, Hai R, Palese P. In vivo bioluminescent imaging of influenza a virus infection and characterization of novel cross-protective monoclonal antibodies. J Virol. 2013; 87(15):8272-81. doi: 10.1128/JVI.00969-13 PMID: 23698304
16. Manicassamy B, Manicassamy S, Belicha-Villanueva A, Pisanelli G, Pulendran B, Garcia-Sastre A. Analysis of in vivo dynamics of influenza virus infection in mice using a GFP reporter virus. Proc Natl Acad Sci U S A. 2010; 107(25):11531-6. doi: 10.1073/pnas.0914994107 PMID: 20534532
17. Pan W, Dong Z, Li F, Meng W, Feng L, Niu X, et al. Visualizing influenza virus infection in living mice. Nature communications. 2013; 4:2369. doi: 10.1038/ncomms3369 PMID: 24022374
18. Tran V, Moser LA, Poole DS, Mehle A. Highly sensitive real-time in vivo imaging of an influenza reporter virus reveals dynamics of replication and spread. J Virol. 2013; 87(24):13321-9. doi: 10.1128/JVI.02381-13 PMID: 24089552
19. Hashimoto K, Ono N, Tatsuo H, Minagawa H, Takeda M, Takeuchi K, et al. SLAM (CD150)-independent measles virus entry as revealed by recombinant virus expressing green fluorescent protein. J Virol. 2002; 76(13):6743-9. PMID: 12050387
20. de Swart RL, Ludlow M, de Witte L, Yanagi Y, van Amerongen G, McQuaid S, et al. Predominant infection of CD150+ lymphocytes and dendritic cells during measles virus infection of macaques. PLoS pathogens. 2007; 3(11):e178. PMID: 18020706
21. Fujii K, Fujii Y, Noda T, Muramoto Y, Watanabe T, Takada A, et al. Importance of both the coding and the segment-specific noncoding regions of the influenza A virus NS segment for its efficient incorporation into virions. J Virol. 2005; 79(6):3766-74. PMID: 15731270
22. Kittel C, Ferko B, Kurz M, Voglauer R, Sereinig S, Romanova J, et al. Generation of an influenza A virus vector expressing biologically active human interleukin-2 from the NS gene segment. J Virol. 2005; 79 (16):10672-7. PMID: 16051859
23. Kittel C, Sereinig S, Ferko B, Stasakova J, Romanova J, Wolkerstorfer A, et al. Rescue of influenza virus expressing GFP from the NS1 reading frame. Virology. 2004; 324(1):67-73. PMID: 15183054
24. Li F, Feng L, Pan W, Dong Z, Li C, Sun C, et al. Generation of replication-competent recombinant influenza A viruses carrying a reporter gene harbored in the neuraminidase segment. J Virol. 2010; 84 (22):12075-81. doi: 10.1128/JVI.00046-10 PMID: 20826692
25. Pena L, Sutton T, Chockalingam A, Kumar S, Angel M, Shao H, et al. Influenza viruses with rearranged genomes as live-attenuated vaccines. Journal of virology. 2013; 87(9):5118-27. doi: 10.1128/JVI.02490-12 PMID: 23449800
26. Lakdawala SS, Shih AR, Jayaraman A, Lamirande EW, Moore I, Paskel M, et al. Receptor specificity does not affect replication or virulence of the 2009 pandemic H1N1 influenza virus in mice and ferrets. Virology. 2013; 446(1-2):349-56. doi: 10.1016/j.virol.2013.08.015 PMID: 24074596
27. Lakdawala SS, Wu Y, Wawrzusin P, Kabat J, Broadbent AJ, Lamirande EW, et al. Influenza a virus assembly intermediates fuse in the cytoplasm. PLoS Pathog. 2014; 10(3):e1003971. doi: 10.1371/journal.ppat.1003971 PMID: 24603687
28. Didcock L, Young DF, Goodbourn S, Randall RE. The V protein of simian virus 5 inhibits interferon signalling by targeting STAT1 for proteasome-mediated degradation. J Virol. 1999; 73(12):9928-33. PMID: 10559305
29. Young DF, Andrejeva L, Livingstone A, Goodbourn S, Lamb RA, Collins PL, et al. Virus replication in engineered human cells that do not respond to interferons. J Virol. 2003; 77(3):2174-81. PMID: 12525652
30. Hoffmann E, Krauss S, Perez D, Webby R, Webster RG. Eight-plasmid system for rapid generation of influenza virus vaccines. Vaccine. 2002; 20(25-26):3165-70. PMID: 12399193
31. Reed LJaM, A simple method of estimating fifty percent endpoints. Am J Hygiene. 1938; 27:493-7.
32. Van den Hoecke S, Verhelst J, Vuylsteke M, Saelens X. Analysis of the genetic diversity of influenza A viruses using next-generation DNA sequencing. BMC Genomics. 2015; 16:79. PMID: 25758772
33. Watson SJ, Welkers MR, Depledge DP, Coulter E, Breuer JM, de Jong MD, et al. Viral population analysis and minority-variant detection using short read next-generation sequencing. Philosophical transactions of the Royal Society of London Series B, Biological sciences. 2013; 368(1614):20120205. doi: 10.1098/rstb.2012.0205 PMID: 23382427
34. Hale BG, Randall RE, Ortin J, Jackson D. The multifunctional NS1 protein of influenza A viruses. J Gen Virol. 2008; 89(Pt 10):2359-76. doi: 10.1099/vir.0.2008/004606-0 PMID: 18796704
35. Qian XY, Chien CY, Lu Y, Montelione GT, Krug RM. An amino-terminal polypeptide fragment of the influenza virus NS1 protein possesses specific RNA-binding activity and largely helical backbone structure. RNA. 1995; 1(9):948-56. PMID: 8548659
36. Wang X, Li M, Zheng H, Muster T, Palese P, Beg AA, et al. Influenza A virus NS1 protein prevents activation of NF-kappaB and induction of alpha/beta interferon. J Virol. 2000; 74(24):11566-73. PMID: 11090154
37. Wang X, Basler CF, Williams BR, Silverman RH, Palese P, Garcia-Sastre A. Functional replacement of the carboxy-terminal two-thirds of the influenza A virus NS1 protein with short heterologous dimerization domains. J Virol. 2002; 76(24):12951-62. PMID: 12438621
38. Ryan MD, Drew J. Foot-and-mouth disease virus 2A oligopeptide mediated cleavage of an artificial polyprotein. The EMBO journal. 1994; 13(4):928-33. PMID: 8112307
39. Ryan MD, King AM, Thomas GP. Cleavage of foot-and-mouth disease virus polyprotein is mediated by residues located within a 19 amino acid sequence. The Journal of general virology. 1991; 72:2727-32. PMID: 1658199
40. Basler CF, Reid AH, Dybing JK, Janczewski TA, Fanning TG, Zheng H, et al. Sequence of the 1918 pandemic influenza virus nonstructural gene (NS) segment and characterization of recombinant viruses bearing the 1918 NS genes. Proceedings of the National Academy of Sciences of the United States of America. 2001; 98(5):2746-51. PMID: 11226311
41. Percy N, Barclay WS, Garcia-Sastre A, Palese P. Expression of a foreign protein by influenza A virus. Journal of virology. 1994; 68(7):4486-92. PMID: 8207822
42. Kim JH, Lee SR, Li LH, Park HJ, Park JH, Lee KY, et al. High cleavage efficiency of a 2A peptide derived from porcine teschovirus-1 in human cell lines, zebrafish and mice. PloS one. 2011; 6(4):e18556. doi: 10.1371/journal.pone.0018556 PMID: 21602908
43. Donnelly ML, Hughes LE, Luke G, Mendoza H, ten Dam E, Gani D, et al. The 'cleavage' activities of foot-and-mouth disease virus 2A site-directed mutants and naturally occurring '2A-like' sequences. The Journal of general virology. 2001; 82(Pt 5):1027-41.
44. Chua MA, Schmid S, Perez JT, Langlois RA, Tenoever BR. Influenza A virus utilizes suboptimal splicing to coordinate the timing of infection. Cell reports. 2013; 3(1):23-9. doi: 10.1016/j.celrep.2012.12.010 PMID: 23333274
45. Wolschek M, Samm E, Seper H, Sturlan S, Kuznetsova I, Schwager C, et al. Establishment of a chimeric, replication-deficient influenza A virus vector by modulation of splicing efficiency. J Virol. 2011; 85(5):2469-73. doi: 10.1128/JVI.01650-10 PMID: 21177819
46. Neirynck S, Deroo T, Saelens X, Vanlandschoot P, Jou WM, Fiers W. A universal influenza A vaccine based on the extracellular domain of the M2 protein. Nature medicine. 1999; 5(10):1157-63. PMID: 10502819
47. Song JM, Wang BZ, Park KM, Van Rooijen N, Quan FS, Kim MC, et al. Influenza virus-like particles containing M2 induce broadly cross protective immunity. PloS one. 2011; 6(1):e14538. doi: 10.1371/journal.pone.0014538 PMID: 21267073
48. El Bakkouri K, Descamps F, De Filette M, Smet A, Festjens E, Birkett A, et al. Universal vaccine based on ectodomain of matrix protein 2 of influenza A: Fc receptors and alveolar macrophages mediate protection. J Immunol. 2011; 186(2):1022-31. doi: 10.4049/jimmunol.0902147 PMID: 21169548
49. Schotsaert M, Ysenbaert T, Neyt K, Ibanez LI, Bogaert P, Schepens B, et al. Natural and long-lasting cellular immune responses against influenza in the M2e-immune host. Mucosal immunology. 2013; 6(2):276-87. doi: 10.1038/mi.2012.69 PMID: 22806098
50. De Baets S, Schepens B, Sedeyn K, Schotsaert M, Roose K, Bogaert P, et al. Recombinant influenza virus carrying the RSV F85-93 CTL epitope reduces respiratory syncytial virus replication in mice. J Virol. 2013; 87(6):3314-23. doi: 10.1128/JVI.03019-12 PMID: 23302879
51. Short KR, Brooks AG, Reading PC, Londrigan SL. The fate of influenza A virus after infection of human macrophages and dendritic cells. J Gen Virol. 2012; 93(Pt 11):2315-25. doi: 10.1099/vir.0.045021-0 PMID: 22894921
52. Bender A, Albert M, Reddy A, Feldman M, Sauter B, Kaplan G, et al. The distinctive features of influenza virus infection of dendritic cells. Immunobiology. 1998; 198(5):552-67. PMID: 9561373
53. Dougan SK, Ashour J, Karssemeijer RA, Popp MW, Avalos AM, Barisa M, et al. Antigen-specific B-cell receptor sensitizes B cells to infection by influenza virus. Nature. 2013; 503(7476):406-9. doi: 10.1038/nature12637 PMID: 24141948
54. Hao X, Kim TS, Braciale TJ. Differential response of respiratory dendritic cell subsets to influenza virus infection. J Virol. 2008; 82(10):4908-19. doi: 10.1128/JVI.02367-07 PMID: 18353940
55. Hartmann BM, Li W, Jia J, Patil S, Marjanovic N, Martinez-Romero C, et al. Mouse dendritic cell (DC) influenza virus infectivity is much lower than that for human DCs and is hemagglutinin subtype dependent. J Virol. 2013; 87(3):1916-8. doi: 10.1128/JVI.02980-12 PMID: 23192878
56. Adey A, Morrison HG, Asan, Xun X, Kitzman JO, Turner EH, et al. Rapid, low-input, low-bias construction of shotgun fragment libraries by high-density in vitro transposition. Genome biology. 2010; 11(12):R119. doi: 10.1186/gb-2010-11-12-r119 PMID: 21143862
57. Gack MU, Albrecht RA, Urano T, Inn KS, Huang IC, Carnero E, et al. Influenza A virus NS1 targets the ubiquitin ligase TRIM25 to evade recognition by the host viral RNA sensor RIG-I. Cell host & microbe. 2009; 5(5):439-49.
58. Mueller SN, Langley WA, Carnero E, Garcia-Sastre A, Ahmed R. Immunization with live attenuated influenza viruses that express altered NS1 proteins results in potent and protective memory CD8+ T-cell responses. J Virol. 2010; 84(4):1847-55. doi: 10.1128/JVI.01317-09 PMID: 19939929
59. Chen YC, Liu T, Yu CH, Chiang TY, Hwang CC. Effects of GC bias in next-generation-sequencing data on de novo genome assembly. PloS one. 2013; 8(4):e62856. doi: 10.1371/journal.pone.0062856 PMID: 23638157
60. Ibricevic A, Pekosz A, Walter MJ, Newby C, Battaile JT, Brown EG, et al. Influenza virus receptor specificity and cell tropism in mouse and human airway epithelial cells. J Virol. 2006; 80(15):7469-80. PMID: 16840327