Influenza virus subpopulations: Exchange of lethal H5N1 virus ns for H1N1 virus NS triggers de novo generation of defective-interfering particles and enhances interferon-inducing particle efficiency

Journal of Interferon and Cytokine Research

Volumn 33, Issue 3, 2013, Pages 99-107

  Ngunjiri, John M ^a   Buchek, Gregory M ^a,b   Mohni, Kareem N ^a,c   Sekellick, Margaret J ^a   Marcus, Philip I ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b EASTERN VIRGINIA MEDICAL SCHOOL   (United States)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON; NONSTRUCTURAL PROTEIN 1;

ANIMAL CELL; ARTICLE; EMBRYO; GENE DELETION; GENE REPRESSION; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H5N1; INTERFERON INDUCTION; LOSS OF FUNCTION MUTATION; MAMMAL CELL; NONHUMAN; PARTICLE SIZE; PHENOTYPE; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; ANIMALS; CELLS, CULTURED; CHICK EMBRYO; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA VACCINES; INTERFERONS; SEQUENCE DELETION; VIRAL NONSTRUCTURAL PROTEINS;

EID: 84875018894     PISSN: 10799907     EISSN: 15577465     Source Type: Journal    
DOI: 10.1089/jir.2012.0070     Document Type: Article

References (65)

1. Abramoff MD, Magelhaes PJ, Ram SJ. 2004. Image processingwith ImageJ. Biophotonics Int 11:36-42.
2. Akkina RK, Chambers TM, Nayak DP. 1984. Mechanism of interferenceby defective-interfering particles of influenza virus:differential reduction of intracellular synthesis of specificpolymerase proteins. Virus Res 1:687-702. (Pubitemid 15195316)
3. Baum A, Sachidanandam R, Garc?́a-Sastre A. 2010. Preference ofRIG-I for short viral RNA molecules in infected cells revealedby next-generation sequencing. Proc Natl Acad Sci USA107:16303-16308.
4. Bean WJ, Kawaoka Y, Wood JM, Pearson JE, Webster RG. 1985. Characterization of virulent and avirulent A/Chicken/Pennsylvania/83 influenza viruses: potential role of defective interferingRNAs in nature. J Virol 54:151-160. (Pubitemid 15136857)
5. Bracci L, Canini I, Puzelli S, Sestili P, Vanditti M, Spada M,Donatelli I, Belardelli F, Proietti E. 2005. Type I interferon is apowerful mucosal adjuvant for a selective intranasal vaccinationagainst influenza virus in mice and affects antigencapture at mucosal level. Vaccine 23:2994-3004. (Pubitemid 40462438)
6. Cauthen AN, Swayne DE, Sekellick MJ, Marcus PI, Suarez DL.2007. Amelioration of influenza virus pathogenesis in chickensis attributed to the enhanced interferon-inducing capacityof a virus with a truncated NS1 gene. J Virol 61:1838-1847. (Pubitemid 46214456)
7. Chambers TM, Webster RG. 1987. Defective interfering virusassociated with A/Chicken/Pennsylvania/83 influenza virus.J Virol 61:1517-1523. (Pubitemid 17069757)
8. Chen LM, Davis CT, Zhou H, Cox NJ, Donis RO. 2008. Geneticcompatibility and virulence of reassortants derived fromcontemporary avian H5N1 and human H3N2 influenza Aviruses. PLoS Pathog 4:e1000072.
9. Cheung CY, Poon LLM, Lau AS, Luk W, Lau YL, Shortridge KF,Gordon S, Guan Y, Peiris JSM. 2002. Induction of proin-flammatory cytokines in human macrophages by influenza A(H5N1) viruses: a mechanism for the unusual severity of humandisease? Lancet 360:1831-1837. (Pubitemid 35449422)
10. Dankar SK, Wang S, Ping J, Forbes NE, Keleta L, Li Y, BrownEG. 2011. Influenza A virus NS1 gene mutations F103L andM106I increase replication and virulence. Virol J 8:13.
11. Donald HB, Isaacs A. 1954. Counts of influenza virus particles. JGen Microbiol 10:457-464.Drake JW. 1993. Rates of spontaneous mutation among RNAviruses. Proc Natl Acad Sci USA 90:4171-4175.
12. Drake JW, Holland JJ. 1999. Mutation rates among RNA viruses.Proc Natl Acad Sci USA 96:13910-13913.
13. Easton AJ, Scott PD, Edworthy NL, Meng B, Marriott AC,Dimmock NJ. 2011. A novel broad-spectrum treatment forrespiratory virus infections: influenza-based defective interferingvirus provides protection against pneumovirus infectionin vivo. Vaccine 29:2777-2784.
14. Graef KM, Vreede FT, Lau Y-F, McCall AW, Carr SM, SubbaraoK, Fodor E. 2010. The PB2 subunit of the influenza virus RNApolymerase affects virulence by interacting with the mitochondrialantiviral signaling protein and inhibiting expressionof beta interferon. J Virol 84:8433-8445.
15. Haasbach E, Droebner K, Vogel AB, Planz OJ. 2011. Low-doseinterferon type I treatment is effective against H5N1 andSwine-Origin H1N1 influenza A viruses in vitro and in vivo. JInterferon Cytokine Res 31:515-525.
16. Hai R, Martinez-Sobrido L, Fraser KA, Ayllon J, Garcia-Sastre A,Palese P. 2008. Influenza B virus NS1-truncated mutants: liveattenuatedvaccine approach. J Virol 82:10580-10590. (Pubitemid 352691164)
17. Hayman A, Comely S, Lackenby A, Murphy S, McCauley J,Goodbourn S, Barclay W. 2006. Variation in the ability ofhuman influenza viruses to induce and inhibit the IFN-bpathway. Virology 347:52-64.
18. Isaacs A, Lindenmann J. 1957. Virus interference. I. The interferon.Proc R Soc Ser B 147:258-267.
19. Iwai A, Shiozaki T, Kawai T, Akira S, Kawaoka Y, Takada A,Kida H, Miyazaki T. 2010. Influenza A virus polymerase inhibitstype I interferon induction by binding to interferon bpromoter stimulator 1. J Biol Chem 285:32064-32074.
20. Jiao P, Tian G, Li Y, Deng G, Jiang Y, Liu C, Liu W, Bu Z,Kawaoka Y, Chen H. 2008. A single-amino-acid substitutionin the NS1 protein changes the pathogenicity of H5N1 avianinfluenza viruses in mice. J Virol 82:1146-1154.
21. Lee C-W, Suarez DL. 2008. Reverse genetics of the avian influenzavirus. Methods Mol Biol 436:99-111.
22. Li C, Hatta M, Nidom CA, Muramoto Y, Watanabe S, NeumannG, Kawaoka Y. 2010. Reassortment between avian H5N1 andhuman H3N2 influenza viruses creates hybrid viruses withsubstantial virulence. Proc Natl Acad Sci USA 107:4687-4692.
23. Li Z, Jiang Y, Jiao P, Wang A, Zhao F, Tian G, Wang X, Yu K, BuZ, Chen H. 2006. The NS1 gene contributes to the virulence ofH5N1 avian influenza viruses. J Virol 80:11115-11123. (Pubitemid 44706552)
24. Liniger M, Moulin HR, Sakoda Y, Ruggli N, Summerfield A.2012. Highly pathogenic avian influenza virus H5N1 controlstype I IFN induction in chicken macrophage HD-11 cells: apolygeneic trait that involves NS1 and the polymerase complex.Virology J 9:7
25. Malinoski CP, Marcus PI. 2012a. Influenza virus: A single noninfectiousinterferon induction-suppressing particle blocksexpression of interferon-inducing particles. J Interferon CytokineRes 32:121-126.
26. Malinoski CP, Marcus PI. 2012b. Influenza virus subpopulations:interferon induction suppressing particles require expressionof NS1 and act globally in cells: UV-irradiation of interferoninductingparticles blocks global shut-off and enhance interferonproduction. J Interferon Cytokine Res 33:72-79.
27. Marcus PI. 1986. Interferon induction dose-response curves.Methods Enzymol 119:106-114.
28. Marcus PI, Ngunjiri JM, Sekellick MJ. 2009. Dynamics of biologicallyactive subpopulations in influenza virus: plaqueforming, noninfectious cell-killing, and defective-interferingparticles. J Virol 83:8122-8130.
29. Marcus PI, Ngunjiri JM, Sekellick MJ, Wang L, Lee CW. 2010.In Vitro analysis of virus particle subpopulations in candidatelive-attenuated influenza vaccines distinguishes effective fromineffective vaccines. J Virol 84:10974-10981.
30. Marcus PI, Rojek JM, Sekellick MJ. 2005. Interferon inductionand/or production and its suppression in influenza viruses. JVirol 79:2880-2890. (Pubitemid 40270566)
31. Mok KP, Wong CH, Cheung CY, Chan MC, Lee SM, NichollsJM, Guan Y, Peiris JS. 2009. Viral genetic determinants ofH5N1 influenza viruses that contribute to cytokine dysregulation.J Infect Dis 200:1104-1112.
32. Moresco KA, Stallknecht DE, Swayne DE. 2010. Evaluation andattempted optimization of avian embryos and cell culturemethods for efficient isolation and propagation of low pathogenicityavian influenza viruses. Avian Dis 54:622-626.
33. Nayak DP, Chambers TM, Akkina RK. 1985. Defective-interfering(DI) RNAs of influenza viruses: origin, structure, expression,and interference. Curr Top Microbiol Immunol 114:103-151.
34. Nayak DP, Tobita K, Janda JM, Davis AR, De BK. 1978.Homologous interference mediated by defective interferinginfluenza virus derived from a temperature-sensitive mutantof influenza virus. J Virol 26:375-386. (Pubitemid 9029995)
35. Neumann G, NodaT, Kawaoka Y. 2009. Emergence and pandemicpotential of swine-origin H1N1 influenza virus. Nature459:931-939.
36. Ngunjiri JM, Lee CW, Ali A, Marcus PI. 2012a. Influenza virusinterferon-inducing particle efficiency is reversed in avianand mammalian cells, and enhanced in cells co-infected withdefective-interfering particles. J Interferon Cytokine Res 32:280-285.
37. Ngunjiri JM, Mohni KN, Sekellick MJ, Schultz-Cherry S, WebsterRG, Marcus PI. 2012b. Lethal H5N1 influenza viruses are notresistant to interferon action in human, simian, porcine, orchicken cells. Nat Med 18:1456-1457.
38. Ngunjiri JM, Sekellick MJ, Marcus PI. 2008. Clonogenic assay oftype A influenza viruses reveals noninfectious cell-killing(apoptosis-inducing) particles. J Virol 82:2673-2680. (Pubitemid 351329158)
39. Nobusawa E, Sato K. 2006. Comparison of the mutation rates ofhuman influenza A and B viruses. J Virol 80:3675-3678.
40. Odagiri T, Tobita K. 1990. Mutation in NS2, a non-structuralprotein of influenza A virus, extragenically causes aberrantreplication and expression of the PA gene and leads to generationof defective interfering particles. Proc Natl Acad SciUSA 87:5988-5992.
41. Odagiri T, Tominaga K, Tobita K, Ohta S. 1994. An amino acidchange in the non-structural NS2 protein of an influenza Avirus mutant is responsible for the generation of defective
42. Parvin JD, Moscona A, Pan WT, Leider JM, Palese P. 1986.Measurement of the mutation rates of animal viruses: influenzaA virus and poliovirus type 1. J Virol 59:377-383. (Pubitemid 16013985)
43. Portnoy J, Merigan TC. 1971. The effect of interferon and interferoninducers on avian influenza. J Infect Dis 124:2425-2432.
44. Richt JA, Garc?́a-Sastre A. 2009. Attenuated influenza virusvaccines with modified NS1 proteins. Curr Top MicrobiolImmunol 333:177-195.
45. Robertson JS, Nicolson C, Harvey R, Johnson R, Major D,Guilfoyle K, Roseby S, Newman R, Collin R, Wallis C, EngelhardtOG, Wood JM, Le J, Manojkumar R, Pokorny BA,Silverman J, Devis R, Bucher D, Verity E, Agius C, CamugliaS, Ong C, Rockman S, Curtis A, Schoofs P, Zoueva O, Xie H,Li X, Lin Z, Ye Z, Chen LM, O'Neill E, Balish A, Lipatov AS,Guo Z, Isakova I, Davis CT, Rivailler P, Gustin KM, Belser JA,Maines TR, Tumpey TM, Xu X, Katz JM, Klimov A, Cox NJ,Donis RO. 2011. The development of vaccine viruses againstpandemic A (H1N1) influenza. Vaccine 29:1836-1843.
46. Rodriguez A, Pérez-González A, Hossain MJ, Chen L-M, RollingT, Pérez-Breñ a P, Donis R, Kochs G, Nieto A. 2009. Attenuatedstrains of influenza virus A viruses do not induce degradationof RNA poymerase II. J Virol 83:1166-1174.
47. Rodriguez A, Pérez-González A, Nieto A. 2007. Influenza virusinfection causes specific degradation of the largest subunit ofcellular RNA polymerase II. J Virol 81:5315-5324. (Pubitemid 46744440)
48. Sekellick MJ, Biggers WJ, Marcus PI. 1990. Development of theinterferon system. I In chicken cells development in ovo continueson time in vitro. In Vitro Cellular Dev Biol 26:997-1003.
49. Sekellick MJ, Carra SA, Bowman A, Hopkins DA, Marcus PI.2000. Transient resistance of influenza virus to interferon actionattributed to random multiple packaging and activity ofNS genes. J Interferon Cytokine Res 20:963-970.
50. SekellickMJ, Marcus PI. 1982. Interferon induction by viruses. VIII.Vesicular Stomatitis virus: [ +/-[ DI-011 particles induce interferonin the absence of standard virions. Virology 117:280-285. (Pubitemid 12170212)
51. Sekellick MJ, Marcus PI. 1986. Induction of high titer chickeninterferon. Methods Enzymol 119:115-125.
52. Slemons RD, Condobery PK, Swayne DE. 1991. Assessingpathogenicity potential of waterfowl-origin type A influenzaviruses in chickens. Avian Dis 35:210-215.
53. Suarez P, Valcá rcel J, Ort?́n J. 1992. Heterogeneity of the mutationrates of influenza A viruses: isolation of mutator mutants.J Virol 66:2491-2494.
54. Subbarao K, Webster RG, Kawaoka Y, Murphy BR. 1995. Arethere alternative avian influenza viruses for generation ofstable attenuated avian-human influenza A reassortant viruses?Virus Res 39:105-118. (Pubitemid 26054780)
55. Sun Y, Qin K, Wang J, Pu J, Tang Q, Hu Y, Bi Y, Zhao X, Yang H,Shu Y, Liu J. 2011. High genetic compatibility and increasedpathogenicity of reassortants derived from avian H9N2 andpandemic H1N1/2009 influenza viruses. Proc Natl Acad SciUSA 108:4164-4169.
56. Szretter KJ, Gangappa S, Belser JA, Zeng H, Chen H, MatsuokaY, Sambhara S, Swayne DE, Tumpey TM, Katz JM. 2009. Earlycontrol of H5N1 Influenza virus replication by the Type Iinterferon response in mice. J Virol 83:5825-5834.
57. Triana-Baltzer GB, Sanders RL, Hedlund M, Jensen KA,Aschenbrenner LM, Larson JL, Fang F. 2010. Phenotypic andgenotypic characterization of influenza virus mutants selectedwith the sialidase fusion protein DAS181. J Antimicrob Chemother66:15-28.
58. Uiprasertkul M, Kitphati R, Puthavathana P, Kriwong R,Kongchanagul A, Ungchusak K, Angkasekwinai S, ChokephaibulkitK, Srisook K, Vanprapar N, Auewarakul P. 2007.Apoptosis and pathogenesis of avian influenza A (H5N1) virusin humans. Emerg Infect Dis 13:708-712. (Pubitemid 46698732)
59. Vreede FT, Fodor E. 2010. The role of the influenza virus RNApolymerase in host shut-off. Virulence 1:436-439.
60. Wang L, Suarez DL, Pantin-Jackwood M, Mibayashi M, Garc?́a-Sastre A, Saif YM. Lee CW. 2008. Characterization of influenzavirus variants with different sizes of the non-structural(NS) genes and their potential as a live influenza vaccine inpoultry. Vaccine 26:3580-3586.
61. Wang Z, Robb NC, Lenz E, Wolff T, Fodor E, Pleschka S. 2010.NS reassortment of an H7-type highly pathogenic avian in-fluenza virus affects its propagation by altering the regulationof viral RNA production and antiviral host response. J Virol84:11323-11335.
62. Webby RJ, Webster RG. 2001. Emergence of influenza A viruses.Philos Trans R Soc London B 356:1817-1828. (Pubitemid 34099086)
63. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y.1992. Evolution and ecology of influenza A viruses. MicrobiolRev 56:152-179.
64. Wolff T, Ludwig S. 2009. Influenza viruses control the vertebratetype I interferon systems: factors, mechanisms, and consequences.J Interferon Cytokine Res 29:549-557.
65. Zhirnov OP, Konakova TE, Wolff T, Klenk H-D. 2002. NS1Protein of Influenza A Virus Down-Regulates Apoptosis. JVirol 76:1617-1625. (Pubitemid 34094608)