The amphibian (xenopus laevis) type I interferon response to frog virus 3: New insight into ranavirus pathogenicity

Journal of Virology

Volumn 88, Issue 10, 2014, Pages 5766-5777

  Grayfer, Leon ^a   De Jesús Andino, Francisco ^a   Robert, Jacques ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; CYTOKINE RESPONSE; FROG VIRUS 3; GENE EXPRESSION; HISTOLOGY; IN VITRO STUDY; IN VIVO STUDY; MORTALITY; MULTIPLE ORGAN FAILURE; NECROSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SURVIVAL TIME; TADPOLE; VIRUS INFECTION; VIRUS LOAD; VIRUS REPLICATION; VIRUS RESISTANCE; VIRUS VIRULENCE; XENOPUS LAEVIS;

ANIMAL STRUCTURES; ANIMALS; CELL LINE; DNA VIRUS INFECTIONS; GENE EXPRESSION PROFILING; HISTOCYTOCHEMISTRY; INTERFERON TYPE I; RANAVIRUS; RECOMBINANT PROTEINS; SURVIVAL ANALYSIS; VIRAL LOAD; XENOPUS LAEVIS;

EID: 84899054498     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00223-14     Document Type: Article

References (52)

1. Chinchar VG. 2002. Ranaviruses (family Iridoviridae): emerging coldblooded killers. Arch. Virol. 147:447-470. http://dx.doi.org/10.1007 /s007050200000.
2. Williams T, Barbosa-Solomieu V, Chinchar VG. 2005. A decade of advances in iridovirus research. Adv. Virus Res. 65:173-248. http://dx.doi .org/10.1016/S0065-3527(05)65006-3.
3. Chinchar VG, Hyatt A, Miyazaki T, Williams T. 2009. Family Iridoviridae: poor viral relations no longer. Curr. Top. Microbiol. Immunol. 328:123-170.
4. Granoff A, Came PE, Breeze DC. 1966. Viruses and renal carcinoma of Rana pipiens. I. The isolation and properties of virus from normal and tumor tissue. Virology 29:133-148.
5. Granoff A, Came PE, Rafferty KA, Jr. 1965. The isolation and properties of viruses from Rana pipiens: their possible relationship to the renal adenocarcinoma of the leopard frog. Ann. N. Y. Acad. Sci. 126:237-255. http: //dx.doi.org/10.1111/j.1749-6632.1965.tb14278.x.
6. Zhan QY, Xiao F, Li ZQ, Gui JF, Mao J, Chinchar VG. 2001. Characterization of an iridovirus from the cultured pig frog Rana grylio with lethal syndrome. Dis. Aquat. Organ. 48:27-36. http://dx.doi.org/10.3354 /dao048027.
7. Speare R, Freeland WJ, Bolton SJ. 1991. A possible iridovirus in erythrocytes of Bufo marinus in Costa Rica. J. Wildl. Dis. 27:457-462. http://dx .doi.org/10.7589/0090-3558-27.3.457.
8. Speare R, Smith JR. 1992. An iridovirus-like agent isolated from the ornate burrowing frog Limnodynastes ornatus in northern Australia. Dis. Aquat. Organ. 14:51-57. http://dx.doi.org/10.3354/dao014051.
9. Cunningham AA, Langton TE, Bennett PM, Lewin JF, Drury SE, Gough RE, Macgregor SK. 1996. Pathological and microbiological findings from incidents of unusual mortality of the common frog (Rana temporaria). Philos. Trans. R. Soc. Lond. B Biol. Sci. 351:1539-1557. http://dx.doi.org /10.1098/rstb.1996.0140.
10. Drury SE, Gough RE, Cunningham AA. 1995. Isolation of an iridoviruslike agent from common frogs (Rana temporaria). Vet. Rec. 137:72-73. http://dx.doi.org/10.1136/vr.137.3.72.
11. Bollinger TK, Mao J, Schock D, Brigham RM, Chinchar VG. 1999. Pathology, isolation, and preliminary molecular characterization of a novel iridovirus from tiger salamanders in Saskatchewan. J. Wildl. Dis. 35:413-429. http://dx.doi.org/10.7589/0090-3558-35.3.413.
12. Donnelly TM, Davidson EW, Jancovich JK, Borland S, Newberry M, Gresens J. 2003. What's your diagnosis? Ranavirus infection. Lab. Anim. (NY) 32:23-25.
13. Greer AL, Berrill M, Wilson PJ. 2005. Five amphibian mortality events associated with ranavirus infection in south central Ontario, Canada. Dis. Aquat. Organ. 67:9-14. http://dx.doi.org/10.3354/dao067009.
14. Jancovich JK, Davids EW, Seiler A, Jacobs BL, Collins JP. 2001. Transmission of the Ambystoma tigrinum virus to alternative hosts. Dis. Aquat. Organ. 46:159-163. http://dx.doi.org/10.3354/dao046159.
15. Jancovich JK, Bremont M, Touchman JW, Jacobs BL. 2010. Evidence for multiple recent host species shifts among the ranaviruses (family Iridoviridae). J. Virol. 84:2636-2647. http://dx.doi.org/10.1128/JVI.01991-09.
16. Becker JA, Tweedie A, Gilligan D, Asmus M, Whittington RJ. 2003. Experimental infection of Australian freshwater fish with epizootic haematopoietic necrosis virus (EHNV). J. Aquat. Anim. Health 25:66-76. http://dx.doi.org/10.1080/08997659.2012.747451.
17. Haislip NA, Gray MJ, Hoverman JT, Miller DL. 2011. Development and disease: how susceptibility to an emerging pathogen changes through anuran development. PLoS One 6:e22307. http://dx.doi.org/10.1371 /journal.pone.0022307.
18. Hyatt AD, Gould AR, Zupanovic Z, Cunningham AA, Hengstberger S, Whittington RJ, Kattenbelt J, Coupar BE. 2000. Comparative studies of piscine and amphibian iridoviruses. Arch. Virol. 145:301-331. http://dx .doi.org/10.1007/s007050050025.
19. Robert J, Abramowitz L, Gantress J, Morales HD. 2007. Xenopus laevis: a possible vector of Ranavirus infection? J. Wildl. Dis. 43:645-652. http: //dx.doi.org/10.7589/0090-3558-43.4.645.
20. Chen G, Robert J. 2011. Antiviral immunity in amphibians. Viruses 3:2065-2086. http://dx.doi.org/10.3390/v3112065.
21. De Jesus Andino F, Chen G, Li Z, Grayfer L, Robert J. 2012. Susceptibility of Xenopus laevis tadpoles to infection by the ranavirus frog-virus 3 correlates with a reduced and delayed innate immune response in comparison with adult frogs. Virology 432:435-443. http://dx.doi.org/10 .1016/j.virol.2012.07.001.
22. Morales HD, Abramowitz L, Gertz J, Sowa J, Vogel A, Robert J. 2010. Innate immune responses and permissiveness to ranavirus infection of peritoneal leukocytes in the frog Xenopus laevis. J. Virol. 84:4912-4922. http://dx.doi.org/10.1128/JVI.02486-09.
23. Hervas-Stubbs S, Perez-Gracia JL, Rouzaut A, Sanmamed MF, Le Bon A, Melero I. 2011. Direct effects of type I interferons on cells of the immune system. Clin. Cancer Res. 17:2619-2627. http://dx.doi.org/10 .1158/1078-0432.CCR-10-1114.
24. Robertsen B. 2006. The interferon system of teleost fish. Fish Shellfish Immunol. 20:172-191. http://dx.doi.org/10.1016/j.fsi.2005.01.010.
25. Zou J, Secombes CJ. 2011. Teleost fish interferons and their role in immunity. Dev. Comp. Immunol. 35:1376-1387. http://dx.doi.org/10 .1016/j.dci.2011.07.001.
26. Chang M, Nie P, Collet B, Secombes CJ, Zou J. 2009. Identification of an additional two-cysteine containing type I interferon in rainbow trout Oncorhynchus mykiss provides evidence of a major gene duplication event within this gene family in teleosts. Immunogenetics 61: 315-325. http://dx.doi.org/10.1007/s00251-009-0366-y.
27. Qi Z, Nie P, Secombes CJ, Zou J. 2010. Intron-containing type I and type III IFN coexist in amphibians: refuting the concept that a retroposition event gave rise to type I IFNs. J. Immunol. 184:5038-5046. http://dx.doi .org/10.4049/jimmunol.0903374.
28. Zou J, Tafalla C, Truckle J, Secombes CJ. 2007. Identification of a second group of type I IFNs in fish sheds light on IFN evolution in vertebrates. J. Immunol. 179:3859-3871.
29. Sun B, Robertsen B, Wang Z, Liu B. 2009. Identification of an Atlantic salmon IFN multigene cluster encoding three IFN subtypes with very different expression properties. Dev. Comp. Immunol. 33:547-558. http: //dx.doi.org/10.1016/j.dci.2008.10.001.
30. Li Z, Strunk JJ, Lamken P, Piehler J, Walz T. 2008. The EM structure of a type I interferon-receptor complex reveals a novel mechanism for cytokine signaling. J. Mol. Biol. 377:715-724. http://dx.doi.org/10.1016/j.jmb .2007.12.005.
31. Samuel CE. 2001. Antiviral actions of interferons. Clin. Microbiol. Rev. 14:778-809. http://dx.doi.org/10.1128/CMR.14.4.778-809.2001.
32. Aggad D, Mazel M, Boudinot P, Mogensen KE, Hamming OJ, Hartmann R, Kotenko S, Herbomel P, Lutfalla G, Levraud JP. 2009. The two groups of zebrafish virus-induced interferons signal via distinct receptors with specific and shared chains. J. Immunol. 183:3924-3931. http://dx.doi .org/10.4049/jimmunol.0901495.
33. Altmann SM, Mellon MT, Distel DL, Kim CH. 2003. Molecular and functional analysis of an interferon gene from the zebrafish, Danio rerio. J. Virol. 77:1992-2002. http://dx.doi.org/10.1128/JVI.77.3.1992-2002.2003.
34. Long S, Wilson M, Bengten E, Bryan L, Clem LW, Miller NW, Chinchar VG. 2004. Identification of a cDNA encoding channel catfish interferon. Dev. Comp. Immunol. 28:97-111. http://dx.doi.org/10.1016/S0145-305X (03)00122-8.
35. Lopez-Munoz A, Roca FJ, Meseguer J, Mulero V. 2009. New insights into the evolution of IFNs: zebrafish group II IFNs induce a rapid and transient expression of IFN-dependent genes and display powerful antiviral activities. J. Immunol. 182:3440-3449. http://dx.doi.org/10.4049/jimmunol.0802528.
36. Robertsen B, Bergan V, Rokenes T, Larsen R, Albuquerque A. 2003. Atlantic salmon interferon genes: cloning, sequence analysis, expression, and biological activity. J. Interferon Cytokine Res. 23:601-612. http://dx .doi.org/10.1089/107999003322485107.
37. Levraud JP, Boudinot P, Colin I, Benmansour A, Peyrieras N, Herbomel P, Lutfalla G. 2007. Identification of the zebrafish IFN receptor: implications for the origin of the vertebrate IFN system. J. Immunol. 178: 4385-4394.
38. Li Z, Xu X, Huang L, Wu J, Lu Q, Xiang Z, Liao J, Weng S, Yu X, He J. 2010. Administration of recombinant IFN1 protects zebrafish (Danio rerio) from ISKNV infection. Fish Shellfish Immunol. 29:399-406. http: //dx.doi.org/10.1016/j.fsi.2010.04.020.
39. Svingerud T, Solstad T, Sun B, Nyrud ML, Kileng O, Greiner-Tollersrud L, Robertsen B. 2012. Atlantic salmon type I IFN subtypes show differences in antiviral activity and cell-dependent expression: evidence for high IFNb/IFNc-producing cells in fish lymphoid tissues. J. Immunol. 189:5912-5923. http://dx.doi.org/10.4049/jimmunol.1201188.
40. Kawasaki ES, Ladner MB, Wang AM, Van Arsdell J, Warren MK, Coyne MY, Schweickart VL, Lee MT, Wilson KJ, Boosman A. 1985. Molecular cloning of a complementary DNA encoding human macrophage-specific colony-stimulating factor (CSF-1). Science 230:291-296. http://dx.doi .org/10.1126/science.2996129.
41. Bakheet T, Frevel M, Williams BR, Greer W, Khabar KS. 2001. ARED: human AU-rich element-containing mRNA database reveals an unexpectedly diverse functional repertoire of encoded proteins. Nucleic Acids Res. 29:246-254. http://dx.doi.org/10.1093/nar/29.1.246.
42. Whitley DS, Yu K, Sample RC, Sinning A, Henegar J, Norcross E, Chinchar VG. 2010. Frog virus 3 ORF 53R, a putative myristoylated membrane protein, is essential for virus replication in vitro. Virology 405:448- 456. http://dx.doi.org/10.1016/j.virol.2010.06.034.
43. Kik M, Martel A, Sluijs AS, Pasmans F, Wohlsein P, Grone A, Rijks JM. 2011. Ranavirus-associated mass mortality in wild amphibians, the Netherlands, 2010: a first report. Vet. J. 190:284-286. http://dx.doi.org/10.1016 /j.tvjl.2011.08.031.
44. Lutfalla G, Roest Crollius H, Stange-Thomann N, Jaillon O, Mogensen K, Monneron D. 2003. Comparative genomic analysis reveals independent expansion of a lineage-specific gene family in vertebrates: the class II cytokine receptors and their ligands in mammals and fish.BMCGenomics 4:29. http://dx.doi.org/10.1186/1471-2164-4-29.
45. Dixon LJ, Barnes M, Tang H, Pritchard MT, Nagy LE. 2013. Kupffer cells in the liver. Compr. Physiol. 3:785-797. http://dx.doi.org/10.1002 /cphy.c120026.
46. Gut JP, Anton M, Bingen A, Vetter JM, Kirn A. 1981. Frog virus 3 induces a fatal hepatitis in rats. Lab. Invest. 45:218-228.
47. Kirn A, Bingen A, Steffan AM, Wild MT, Keller F, Cinqualbre J. 1982. Endocytic capacities of Kupffer cells isolated from the human adult liver. Hepatology 2:216-222.
48. Kirn A, Steffan AM, Bingen A. 1980. Inhibition of erythrophagocytosis by cultured rat Kupffer cells infected with frog virus 3. J. Reticuloendothel. Soc. 28:381-388.
49. Aubertin AM, Hirth C, Travo C, Nonnenmacher H, Kirn A. 1973. Preparation and properties of an inhibitory extract from frog virus 3 particles. J. Virol. 11:694-701.
50. Gendrault JL, Steffan AM, Bingen A, Kirn A. 1981. Penetration and uncoating of frog virus 3 (FV3) in cultured rat Kupffer cells. Virology 112:375-384. http://dx.doi.org/10.1016/0042-6822(81)90284-1.
51. Elharrar M, Hirth C, Blanc J, Kirn A. 1973. Pathogenesis of the toxic hepatitis of mice provoked by FV 3 (frog virus 3): inhibition of liver macromolecular synthesis. Biochim. Biophys. Acta 319:91-102. http://dx.doi .org/10.1016/0005-2787(73)90044-0. (In French.).
52. Bingen-Brendel A, Batzenschlager A, Gut JP, Hirth C, Vetter JM, Kirn A. 1972. Histological and virological study of acute degenerative hepatitis produced by the FV3 (frog virus 3) in mice. Ann. Inst. Pasteur (Paris) 122:125-142. (In French.)