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

Volumn 432, Issue 2, 2012, Pages 435-443

  De Jesús Andino, Francisco ^a   Chen, Guangchun ^a   Li, Zhenghui ^a   Grayfer, Leon ^a   Robert, Jacques ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Amphibian; Anti viral immunity; Innate immunity; Viral infection

Indexed keywords

AGE DISTRIBUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FROG VIRUS 3; GENE; GENE EXPRESSION; IFN GAMMA GENE; IL 1BETA GENE; INFECTION RATE; INFECTION SENSITIVITY; INFLAMMATION; INNATE IMMUNITY; LARVA; MX1 GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RANAVIRUS INFECTION; TADPOLE; TNF ALPHA GENE; UPREGULATION; VIRUS RESISTANCE; XENOPUS LAEVIS;

ANIMALS; DNA VIRUS INFECTIONS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; IMMUNITY, INNATE; LARVA; LEUKOCYTES; RANAVIRUS; TIME FACTORS; XENOPUS LAEVIS;

AMPHIBIA; ANURA; BACTERIA (MICROORGANISMS); FROG VIRUS 3; RANAVIRUS; XENOPUS LAEVIS;

EID: 84865303556     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2012.07.001     Document Type: Article

References (59)

1. Bartee E., Mohamed M.R., McFadden G. Tumor necrosis factor and interferon: cytokines in harmony. Curr. Opin. Microbiol. 2008, 11(4):378-383.
2. Bird S., Wang T., Zou J., Cunningham C., Secombes C.J. The first cytokine sequence within cartilaginous fish: IL-1 beta in the small spotted catshark (Scyliorhinus canicula). J. Immunol. 2002, 168(7):3329-3340.
3. Campbell S., McBeath A., Secombes C., Snow M., Collet B. Interferon response following infection with genetically similar isolates of viral haemorrhagic septicaemia virus (VHSV) exhibiting contrasting virulence in rainbow trout. Fish Shellfish Immunol. 2011, 30(1):287-294.
4. Chardonnens X., Du Pasquier L. Induction of skin allograft tolerance during metamorphosis of the toad Xenopus laevis: a possible model for studying generation of self tolerance to histocompatibility antigens. Eur. J. Immunol. 1973, 3(9):569-573.
5. Chen, G., Ward, B.M., Yu, E.K., Chinchar, V.G., and Robert, J. (2011). Improved knockout methodology reveals that Frog Virus 3 mutants lacking either the 18K immediate-early gene or the truncated vIF2-{alpha} gene are defective for replication and growth in vivo. J. Virol.
6. Chinchar V.G., Hyatt A., Miyazaki T., Williams T. Family Iridoviridae: poor viral relations no longer. Curr. Top. Microbiol. Immunol. 2009, 328:123-170.
7. Cilloniz, C., Pantin-Jackwood, M.J., Ni, C., Carter, V.S., Korth, M.J., Swayne, D.E., Tumpey, T.M., and Katze, M.G. Molecular signatures associated with Mx1-mediated resistance to highly pathogenic influenza virus infection: mechanisms of survival. J. Virol. 86(5), 2437-2446.
8. Cuesta A., Tafalla C. Transcription of immune genes upon challenge with viral hemorrhagic septicemia virus (VHSV) in DNA vaccinated rainbow trout (Oncorhynchus mykiss). Vaccine 2009, 27(2):280-289.
9. Diel D.G., Luo S., Delhon G., Peng Y., Flores E.F., Rock D.L. A nuclear inhibitor of NF-kappaB encoded by a poxvirus. J. Virol. 2011, 85(1):264-275.
10. DiMarzo S.J., Cohen N. An in vivo study of the ontogeny of alloreactivity in the frog, Xenopus laevis. Immunology 1982, 45(1):39-48.
11. DiMarzo S.J., Cohen N. Immunogenetic aspects of in vivo allotolerance induction during the ontogeny of Xenopus laevis. Immunogenetics 1982, 16(2):103-116.
12. Du Pasquier L., Robert J., Courtet M., Mussmann R. B-cell development in the amphibian Xenopus. Immunol. Rev. 2000, 175:201-213.
13. Du Pasquier L., Schwager J., Flajnik M.F. The immune system of Xenopus. Annu. Rev. Immunol. 1989, 7:251-275.
14. Duffus A.L., Pauli B.D., Wozney K., Brunetti C.R., Berrill M. Frog Virus 3-like infections in aquatic amphibian communities. J. Wildl. Dis. 2008, 44(1):109-120.
15. Flajnik M.F., Du Pasquier L. MHC class I antigens as surface markers of adult erythrocytes during the metamorphosis of Xenopus. Dev. Biol. 1988, 128(1):198-206.
16. Flajnik M.F., Kaufman J.F., Hsu E., Manes M., Parisot R., Du Pasquier L. Major histocompatibility complex-encoded class I molecules are absent in immunologically competent Xenopus before metamorphosis. J. Immunol. 1986, 137(12):3891-3899.
17. Gantress J., Maniero G.D., Cohen N., Robert J. Development and characterization of a model system to study amphibian immune responses to iridoviruses. Virology 2003, 311(2):254-262.
18. Gray M.J., Miller D.L., Hoverman J.T. Ecology and pathology of amphibian ranaviruses. Dis. Aquat. Organ. 2009, 87(3):243-266.
19. Gray M.J., Miller D.L., Schmutzer A.C., Baldwin C.A. Frog Virus 3 prevalence in tadpole populations inhabiting cattle-access and non-access wetlands in Tennessee, USA. Dis. Aquat. Organ. 2007, 77(2):97-103.
20. Grayfer L., Belosevic M. Molecular characterization, expression and functional analysis of goldfish (Carassius aurutus L.) interferon gamma. Dev. Comp. Immunol. 2009, 33(2):235-246.
21. Grayfer L., Garcia E.G., Belosevic M. Comparison of macrophage antimicrobial responses induced by type II interferons of the goldfish (Carassius auratus L.). J. Biol. Chem. 2010, 285(31):23537-23547.
22. Grayfer L., Walsh J.G., Belosevic M. Characterization and functional analysis of goldfish (Carassius auratus L.) tumor necrosis factor-alpha. Dev. Comp. Immunol. 2008, 32(5):532-543.
23. Green D.E., Converse K.A., Schrader A.K. Epizootiology of sixty-four amphibian morbidity and mortality events in the USA, 1996-2001. Ann. N.Y. Acad. Sci. 2002, 969:323-339.
24. Haller O., Staeheli P., Kochs G. Interferon-induced Mx proteins in antiviral host defense. Biochimie 2007, 89(6-7):812-818.
25. Hirono I., Nam B.H., Kurobe T., Aoki T. Molecular cloning, characterization, and expression of TNF cDNA and gene from Japanese flounder Paralychthys olivaceus. J. Immunol. 2000, 165(8):4423-4427.
26. Horton T.L., Stewart R., Cohen N., Rau L., Ritchie P., Watson M.D., Robert J., Horton J.D. Ontogeny of Xenopus NK cells in the absence of MHC class I antigens. Dev. Comp. Immunol. 2003, 27(8):715-726.
27. Hsu E. Mutation, selection, and memory in B lymphocytes of exothermic vertebrates. Immunol. Rev. 1998, 162:25-36.
28. Hsu E., Du Pasquier L. Ontogeny of the immune system in Xenopus. I. Larval immune response. Differentiation 1984, 28:109-115.
29. Huang X., Huang Y., Ouyang Z., Cai J., Yan Y., Qin Q. Roles of stress-activated protein kinases in the replication of Singapore grouper iridovirus and regulation of the inflammatory responses in grouper cells. J. Gen. Virol 2011.
30. Igawa D., Sakai M., Savan R. An unexpected discovery of two interferon gamma-like genes along with interleukin (IL)-22 and -26 from teleost: IL-22 and -26 genes have been described for the first time outside mammals. Mol. Immunol. 2006, 43(7):999-1009.
31. Jorgensen J.B., Johansen A., Hegseth M.N., Zou J., Robertsen B., Collet B., Secombes C.J. A recombinant CHSE-214 cell line expressing an Mx1 promoter-reporter system responds to both interferon type I and type II from salmonids and represents a versatile tool to study the IFN-system in teleost fish. Fish Shellfish Immunol. 2007, 23(6):1294-1303.
32. Keesing F., Belden L.K., Daszak P., Dobson A., Harvell C.D., Holt R.D., Hudson P., Jolles A., Jones K.E., Mitchell C.E., Myers S.S., Bogich T., Ostfeld R.S. Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 2010, 468(7324):647-652.
33. Maniero G.D., Morales H., Gantress J., Robert J. Generation of a long-lasting, protective, and neutralizing antibody response to the ranavirus FV3 by the frog Xenopus. Dev. Comp. Immunol. 2006, 30(7):649-657.
34. Marr S., Goyos A., Gantress J., Maniero G.D., Robert J. CD91 up-regulates upon immune stimulation in Xenopus adult but not larval peritoneal leukocytes. Immunogenetics 2005, 56(10):735-742.
35. Marr S., Morales H., Bottaro A., Cooper M., Flajnik M., Robert J. Localization and differential expression of activation-induced cytidine deaminase in the amphibian Xenopus upon antigen stimulation and during early development. J. Immunol. 2007, 179(10):6783-6789.
36. Mawaribuchi S., Tamura K., Okano S., Takayama S., Yaoita Y., Shiba T., Takamatsu N., Ito M. Tumor necrosis factor-alpha attenuates thyroid hormone-induced apoptosis in vascular endothelial cell line XLgoo established from Xenopus tadpole tails. Endocrinology 2008, 149(7):3379-3389.
37. Mazzoni R., de Mesquita A.J., Fleury L.F., de Brito W.M., Nunes I.A., Robert J., Morales H., Coelho A.S., Barthasson D.L., Galli L., Catroxo M.H. Mass mortality associated with a Frog Virus 3-like ranavirus infection in farmed tadpoles Rana catesbeiana from Brazil. Dis. Aquat. Organ. 2009, 86(3):181-191.
38. Morales H.D., Abramowitz L., Gertz J., Sowa J., Vogel A., Robert J. Innate immune responses and permissiveness to ranavirus infection of peritoneal leukocytes in the frog Xenopus laevis. J. Virol. 2010, 84(10):4912-4922.
39. Morales H.D., Robert J. Characterization of primary and memory CD8 T-cell responses against ranavirus (FV3) in Xenopus laevis. J. Virol. 2007, 81(5):2240-2248.
40. Netherton C.L., Simpson J., Haller O., Wileman T.E., Takamatsu H.H., Monaghan P., Taylor G. Inhibition of a large double-stranded DNA virus by MxA protein. J. Virol. 2009, 83(5):2310-2320.
41. Nishikawa A., Murata E., Akita M., Kaneko K., Moriya O., Tomita M., Hayashi H. Roles of macrophages in programmed cell death and remodeling of tail and body muscle of Xenopus laevis during metamorphosis. Histochem. Cell Biol. 1998, 109(1):11-17.
42. Ordas M.C., Costa M.M., Roca F.J., Lopez-Castejon G., Mulero V., Meseguer J., Figueras A., Novoa B. Turbot TNFalpha gene: molecular characterization and biological activity of the recombinant protein. Mol. Immunol. 2007, 44(4):389-400.
43. Pearman P.B., Garner T.W., Straub M., Greber U.F. Response of the Italian agile frog (Rana latastei) to a ranavirus, Frog Virus 3: a model for viral emergence in naive populations. J. Wildl. Dis. 2004, 40(4):660-669.
44. Purcell M.K., Kurath G., Garver K.A., Herwig R.P., Winton J.R. Quantitative expression profiling of immune response genes in rainbow trout following infectious haematopoietic necrosis virus (IHNV) infection or DNA vaccination. Fish Shellfish Immunol. 2004, 17(5):447-462.
45. Purcell M.K., Nichols K.M., Winton J.R., Kurath G., Thorgaard G.H., Wheeler P., Hansen J.D., Herwig R.P., Park L.K. Comprehensive gene expression profiling following DNA vaccination of rainbow trout against infectious hematopoietic necrosis virus. Mol. Immunol. 2006, 43(13):2089-2106.
46. Qi Z.T., Nie P. Comparative study and expression analysis of the interferon gamma gene locus cytokines in Xenopus tropicalis. Immunogenetics 2008, 60(11):699-710.
47. Reed L., Muench H. A simple method of estimating fifty percent endpoints. Am. J. Hyg. 1983, 27:493-497.
48. Robert J., George E., De Jesus Andino F., Chen G. Waterborne infectivity of the ranavirus Frog Virus 3 in Xenopus laevis. Virology 2011.
49. Robert J., Guiet C., Du Pasquier L. Ontogeny of the alloimmune response against a transplanted tumor in Xenopus laevis. Differentiation 1995, 59(3):135-144.
50. Robert J., Morales H., Buck W., Cohen N., Marr S., Gantress J. Adaptive immunity and histopathology in Frog Virus 3-infected Xenopus. Virology 2005, 332(2):667-675.
51. Robert J., Ohta Y. Comparative and developmental study of the immune system in Xenopus. Dev. Dyn. 2009, 238(6):1249-1270.
52. Robertsen B. The interferon system of teleost fish. Fish Shellfish Immunol. 2006, 20(2):172-191.
53. Rollins-Smith L.A., Flajnik M.F., Blair P.J., Davis A.T., Green W.F. Involvement of thyroid hormones in the expression of MHC class I antigens during ontogeny in Xenopus. Dev. Immunol. 1997, 5(2):133-144.
54. Sadler A.J., Williams B.R. Interferon-inducible antiviral effectors. Nat. Rev. Immunol. 2008, 8(7):559-568.
55. Schloegel L.M., Daszak P., Cunningham A.A., Speare R., Hill B. Two amphibian diseases, chytridiomycosis and ranaviral disease, are now globally notifiable to the World Organization for Animal Health (OIE): an assessment. Dis. Aquat. Organ. 2010, 92(2-3):101-108.
56. Schoenborn J.R., Wilson C.B. Regulation of interferon-gamma during innate and adaptive immune responses. Adv. Immunol. 2007, 96:41-101.
57. Xiao J., Zhou Z.C., Chen C., Huo W.L., Yin Z.X., Weng S.P., Chan S.M., Yu X.Q., He J.G. Tumor necrosis factor-alpha gene from mandarin fish, Siniperca chuatsi: molecular cloning, cytotoxicity analysis and expression profile. Mol. Immunol. 2007, 44(14):3615-3622.
58. Yu Z., Zeng Z., Huang Z., Lian J., Yang J., Deng Q., Zeng W. Increased mRNA expression of interferon-induced Mx1 and immunomodulation following oral administration of IFN-alpha2b-transformed B. longum to mice. Arch. Microbiol. 2010, 192(8):633-638.
59. Zou J., Bird S., Minter R., Horton J., Cunningham C., Secombes C.J. Molecular cloning of the gene for interleukin-1beta from Xenopus laevis and analysis of expression in vivo and in vitro. Immunogenetics 2000, 51(4-5):332-338.