Double-stranded RNA iS detected by immunofluorescence analysis in RNA and DNA virus infections, including those by negative-stranded RNA viruses

Journal of Virology

Volumn 89, Issue 18, 2015, Pages 9383-9392

  Son, Kyung No ^a   Liang, Zhiguo ^a   Lipton, Howard L ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; DOUBLE STRANDED RNA; SINGLE STRANDED DNA; SINGLE STRANDED RNA; SMALL INTERFERING RNA; DNA VIRUS; VIRUS RNA;

APOPTOSIS; ARTICLE; CONTROLLED STUDY; CYTOPLASM; DNA VIRUS; DNA VIRUS INFECTION; IMMUNE RESPONSE; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; INFLUENZA A VIRUS; INNATE IMMUNITY; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MEASLES VIRUS; NONHUMAN; NYAMANINI VIRUS; PRIORITY JOURNAL; RNA VIRUS; RNA VIRUS INFECTION; VESICULOVIRUS; VIRUS REPLICATION; ANIMAL; CELL LINE; CELL NUCLEUS; FLUORESCENCE MICROSCOPY; HAMSTER; METABOLISM; MOUSE; PATHOLOGY; VIROLOGY;

ANIMALS; APOPTOSIS; CELL LINE; CELL NUCLEUS; CRICETINAE; DNA VIRUS INFECTIONS; DNA VIRUSES; MICE; MICROSCOPY, FLUORESCENCE; RNA VIRUS INFECTIONS; RNA VIRUSES; RNA, DOUBLE-STRANDED; RNA, VIRAL;

EID: 84940477493     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01299-15     Document Type: Article

References (46)

1. Vilcek J, Ng MH, Friedman-Kien AE, Krawciw T. 1968. Induction of interferon synthesis by synthetic double-stranded polynucleotides. J Virol 2:648-650.
2. Long WF, Burke DC. 1971. Interferon production by double-stranded RNA: a comparison of induction by reovirus to that by a synthetic doublestranded polynucleotide. J Gen Virol 12:1-11. http://dx.doi.org/10.1099/0022-1317-12-1-1.
3. Williams BR. 2001. Signal integration via PKR. Sci STKE 2001:re2.
4. Munir M, Berg M. 2014. The multiple faces of proteinkinase R in antiviral defense. Virulence 13:85-89. http://dx.doi.org/10.4161/viru.23134.
5. Silverman RH. 2007. Viral encounters with 2=5=-oligoadenylate synthetase and RNase L during the interferon antiviral response. J Virol 81: 12720-12729. http://dx.doi.org/10.1128/JVI.01471-07.
6. Kristiansen H, Gad HH, Eskildsen-Larsen S, Despres P, Hartmann R. 2011. The oligoadenylate synthetase family: an ancient protein family with multiple antiviral activities. J Interferon Cytokine Res 31:41-47. http://dx.doi.org/10.1089/jir.2010.0107.
7. Schneider WM, Dittmann Chevillote M, Rice CM. 2014. Interferonstimulated genes: a complex web of host defenses. Annu Rev Immunol 32: 513-545. http://dx.doi.org/10.1146/annurev-immunol-032713-120231.
8. Dermody TS, Parker JSL, Sherry B. 2013. Orthoreoviruses, p 1304-1346. In Knipe DM, Howley PM, Cohen JI, Griffin DE, Lamb RA, Martin MA, Racaniello VR, Roizman B (ed), Fields virology, 6th ed, vol 2. Lippincott Williams and Wilkins, Philadelphia, PA.
9. Kato H, Takeuchi O, Mikamo-Satoh E, Hirai R, Kawai T, Matsushita K, Hiiragi A, Dermody TS, Fujita T, Akira S. 2008. Length-dependent recognition of double-stranded ribonucleic acids by retinoic acidinducible gene I and melanoma differentiation-associated gene 5. J Exp Med 205:1601-1610. http://dx.doi.org/10.1084/jem.20080091.
10. Peisley A, Hur S. 2013. Multi-level regulation of cellular recognition of viral dsRNA. Cell Mol Life Sci 70:1949-1963. http://dx.doi.org/10.1007/s00018-012-1149-4.
11. Ha M, Kim N. 2014. Regulation of microRNA biogenesis. Nat Mol Cell Biol 15:509-524. http://dx.doi.org/10.1038/nrm3838.
12. Ralph RK. 1969. Double-stranded viral RNA. Adv Virus Res 15:61-158. http://dx.doi.org/10.1016/S0065-3527(08)60874-X.
13. Stollar V, Stollar BD. 1970. Immunochemical measurement of doublestranded RNA of uninfected and arbovirus-infected mammalian cells. Proc Natl Acad Sci U S A 65:993-1000. http://dx.doi.org/10.1073/pnas.65.4.993.
14. Colby C, Jurale C, Kates JR. 1971. Mechanism of synthesis of vaccinia virus double-stranded ribonucleic acid in vivo and in vitro. J Virol 7:71-76.
15. Kisseljov FL, Semjonova IS, Irlin IS, Shatalova GG. 1972. Partiallydouble-stranded RNA in mouse spleen cells: the effect of Rauscher virus infection. Arch Virol 36:265-274.
16. Weber F, Wagner V, Rasmussen SB, Hartmann R, Paludan SR. 2006. Double-stranded RNA is produced by positive-strand RNA viruses and DNA viruses but not in detectable amounts by negative-strand viruses. J Virol 80:5059-5064. http://dx.doi.org/10.1128/JVI.80.10.5059-5064.2006.
17. Pfaller CK, Radeke MJ, Cattaneo R, Samuel CE. 2014. Measles virus C protein impairs production of defective copyback double-stranded viral RNA and activation of protein kinase R. J Virol 88:456-468. http://dx.doi.org/10.1128/JVI.02572-13.
18. Jelachich ML, Lipton HL. 1999. Restricted Theiler's murine encephalomyelitis virus infection in murine macrophages induces apoptosis. J Gen Virol 80:1701-1705.
19. Rozhon EJ, Kratochvil JD, Lipton HL. 1983. Analysis of genetic variation in Theiler's virus during persistent infection in the mouse central nervous system. Virology 128:16-32. http://dx.doi.org/10.1016/0042-6822(83)90315-X.
20. Sells MA, Chen M-L, Acs G. 1987. Production of hepatitis B virus particles in HepG2 cells transfected with cloned hepatitis B virus DNA. Proc Natl Acad Sci U S A 84:1005-1009. http://dx.doi.org/10.1073/pnas.84.4.1005.
21. Stollar BD, Stollar V. 1970. Immunofluorescent demonstration of double- stranded RNA in the cytoplasm of Sindbis virus-infected cells. Virology 42:276-280. http://dx.doi.org/10.1016/0042-6822(70)90270-9.
22. Bonin M, Oberstrab J, Lukacs N, Ewert K, Oesterschulze E, Kassing R, Nellen W. 2000. Determination of preferential binding sites for antidsRNA antibodies on double-stranded RNA by scanning force microscopy. RNA 6:563-570. http://dx.doi.org/10.1017/S1355838200992318.
23. Yagi S, Schnurr D, Lin J. 1992. Spectrum of monoclonal antibodies to coxsackievirus B-3 includes type- and group-specific antibodies. J Clin Virol 30:2498-2501.
24. Takeuchi K, Komatsu T, Kitagawa Y, Sada K, Gotoh B. 2008. Sendai virus C protein plays a role in restricting PKR activation by limiting the generation of intracellular double-stranded RNA. J Virol 82:10102-10110. http://dx.doi.org/10.1128/JVI.00599-08.
25. Herrel M, Hoefs N, Staeheli P, Schneider U. 2012. Tick-borne Nyamanini virus replicates in the nucleus and exhibits unusual genome and matrix protein properties. J Virol 86:10739-10747. http://dx.doi.org/10.1128/JVI.00571-12.
26. Fujikura D, Uto M, Chiba S, Harada T, Perez F, Reed JC, Uede T, Miyazaki T. 2012. CLIPR-59 regulates TNF-α-induced apoptosis by controlling ubiquitination of RIP1. Cell Death Dis 3:e264. http://dx.doi.org/10.1038/cddis.2012.3.
27. Min J-Y, Krug RM. 2006. The primary function of RNA binding by the influenza A NS1 protein in infected cells: inhibiting the 2=-5= oligo(A) synthetase/RNase L pathway. Proc Natl Acad Sci U S A 103:7100-7105. http://dx.doi.org/10.1073/pnas.0602184103.
28. Olland AM, Jane-Valbuena J, Schiff LA, Nibert MI, Harrison SC. 2001. Structure of the reovirus outer capsid and dsRNA-binding protein sigma 3 at 1.8A°resolution.EMBOJ 20:979-989. http://dx.doi.org/10.1093/emboj/20.5.979.
29. Sherry B. 2009. Rotavirus and reovirus modulation of the interferon response. J Interferon Cytokine Res 29:559-567. http://dx.doi.org/10.1089/jir.2009.0072.
30. Ye C, Jia L, Sun Y, Hu B, Wang L, Lu X, Zhou J. 2014. Inhibition of antiviral innate immunity by birnavirus VP3 protein via blockage of viral double-stranded RNA to the host cytoplasmic RNA detector MDA5. J Virol 88:11154-11165. http://dx.doi.org/10.1128/JVI.01115-14.
31. Mihindukulasuriya KA, Nguyen NL, Wu G, Huang HV, Travassos da Rosa APA, Popov VL, Tesh RB, Wang D. 2009. Nyamanini and Midway viruses define a novel taxon of RNA viruses in the order Mononegavirales. J Virol 83:5109-5116. http://dx.doi.org/10.1128/JVI.02667-08.
32. Kuhn JH, Bekal S, Cai Y, Clawson AN, Domier LL, Herrel M, Jahrling PB, Kondo H, Lambert KN, Mihindukulasuriya KA, Nowotny N, Radoshitzky SR, Schneider U, Staeheli P, Suzuki N, Tesh RB, Wand D, Wang L-F, Dietzgen RG. 2013. Nyamiviridae: proposal for a new family in the order Mononegavirales. Arch Virol 158:2209-2226. http://dx.doi.org/10.1007/s00705-013-1674-y.
33. Matsumoto Y, Hayashi Y, Omori H, Honda T, Saito T, Horie M, Ikuta K, Fujino K, Nakamura S, Schneider U, Chase G, Yoshimori T, Schwemmie M, Tomonaga K. 2012. Bornavirus closely associates and segregates with host chromosome to ensure persistent intranuclear infection. Cell Host Microbe 11:492-503. http://dx.doi.org/10.1016/j.chom.2012.04.009.
34. Shaw ML, Palese P. 2013. Orthomyxoviridae, p 1151-1185. In Knipe DM, Howley PM, Cohen JI, Griffin DE, Lamb RA, Martin MA, Racaniello VR, Roizman B (ed), Fields virology, 6th ed, vol 2. Lippincott Williams and Wilkins, Philadelphia, PA.
35. Kaneko H, Dridi S, Tarallo V, Gelfand BD, Fowler BJ, Cho WG, Kleinman ME, Ponicsan SL, Hauswirth WW, Chiodo VA, Karikó K, Yoo JW, Lee DK, Hadziahmetovic M, Song Y, Misra S, Chaudhuri G, Buaas FW, Braun RE, Hinton DR, Zhang Q, Grossniklaus HE, Provis JM, Madigan MC, Milam AH, Justice NL, Albuquerque RJ, Blandford AD, Bogdanovich S, Hirano Y, Witta J, Fuchs E, Littman DR, Ambati BK, Rudin CM, Chong MM, Provost P, Kugel JF, Goodrich JA, Dunaief JL, Baffi JZ, Ambati J. 2011. DICER1 deficit induces Alu RNA toxicity in age-related macular degeneration. Nature 471:325-332. http://dx.doi.org/10.1038/nature09830.
36. Kimj Y, Tarallo V, Kerur N, Yasuma T, Gelfand BD, Bastos-Carvalho A, Hirano Y, Yasuma R, Mizutani T, Fowler BJL, Kaneko SH, Boddanovich S, Ambati BK, Hinton DR, Hauswirth WW, Hakem R, Wright C, Ambati J. 2014. DICER1/Alu dysmetabolism induces caspase-8-mediated cell death in age-related macular degeneration. Proc Natl Acad Sci U S A 111:16082-16097. http://dx.doi.org/10.1073/pnas.1403814111.
37. Liu WM, Chu MW, Choudary PV, Schmid CW. 1995. Cell stress and translational inhibitors transiently increase the abundance of mammalian SINE transcripts. Nucleic Acids Res 23:1758-1765. http://dx.doi.org/10.1093/nar/23.10.1758.
38. Li TH, Schmid CW. 2001. Differential stress induction of individual Alu loci: implications for transcription and retrotransposition. Gene 276:135-141. http://dx.doi.org/10.1016/S0378-1119(01)00637-0.
39. Richardson SJ, Willcox A, Hilton DA, Tauriainen S, Hyoty H, Bone AJ, Foulis AK, Morgan NG. 2010. Use of antisera directed against dsRNA to detect infections in formalin-fixed paraffin-embedded tissue. J Clin Virol 180-185. http://dx.doi.org/10.1016/j.jcv.2010.07.015.
40. Bowden DS, Pedersent JS, Toh BH, Westaway EG. 1987. Distribution of immunofluorescence of viral products and actin-containing cytoskeletal filaments in rubella virus-infected cells. Arch Virol 92:211-219. http://dx.doi.org/10.1007/BF01317478.
41. Lee JY, Marshall JA, Bowden DS. 1994. Characterization of rubella virus replication complexes using antibodies to double-stranded RNA. Virology 200:307-312. http://dx.doi.org/10.1006/viro.1994.1192.
42. Westaway EG, Mackenzie JM, Kenney MT, Jones MK, Khromykh AA. 1997. Ultrastructure of Kunjin virus-infected cells: colocalization of NS1 and NS3 with double-stranded RNA, and of NS2B and NS3, in virusinduced membrane structures. J Virol 71:6650-6661.
43. DeWitte-Orr SJ, Mehta DR, Collins SE, Suthar MS, Gale M, Jr, Mossman KL. 2009. Long double-stranded RNA induces an antiviral response independent of FIN regulatory factor 3, IFN-beta promoter stimulator 1, and IFN. J Immunol 183:6545-6553. http://dx.doi.org/10.4049/jimmunol.0900867.
44. Uchida L, Espada-Murao LA, Takamatsu Y, Okamoto K, Hayasaka D, Yu F, Nabeshima T, Buerano CC, Marita K. 2014. The dengue virus conceals double-stranded RNA in the intracellular membrane to escape from an interferon response. Sci Rep 4:7395. http://dx.doi.org/10.1038/srep07395.
45. Targett-Adams P, Boulant S, McLauchlan J. 2008. Visualization of double-stranded RNA in cells supporting hepatitis C virus RNA replication. J Virol 82:2182-2195. http://dx.doi.org/10.1128/JVI.01565-07.
46. Zhang S, Sun Y, Chen H, Dai Y, Zhan Y, Yu S, Qiu X, Tan L, Song C, Ding C. 2014. Activation of the PKR/eIF2a signaling cascade inhibits replication of Newcastle disease virus. Virol J 11:62. http://dx.doi.org/10.1186/1743-422X-11-62