Antiviral immunity in amphibians

Viruses

Volumn 3, Issue 11, 2011, Pages 2065-2086

  Chen, Guangchun ^a   Robert, Jacques ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Amphibian; Iridovirus; Viral infection

Indexed keywords

ADAPTIVE IMMUNITY; AMBYSTOMA TIGRINUM; AMPHIBIA; ANTIVIRAL IMMUNITY; ARTICLE; GENETIC SUSCEPTIBILITY; GENOTYPE; HOST RESISTANCE; IMMUNE EVASION; IMMUNE SYSTEM; IMMUNITY; INFECTION CONTROL; INNATE IMMUNITY; IRIDOVIRUS; LARVA; MACROPHAGE; MAJOR HISTOCOMPATIBILITY COMPLEX; MAMMAL; NONHUMAN; PATHOGENESIS; PERSISTENT VIRUS INFECTION; RANAVIRUS INFECTION; SALAMANDER; SPECIES DIFFERENCE; VERTEBRATE; VIRUS TRANSMISSION; VIRUS VIRULENCE; XENOPUS;

AMPHIBIAN PROTEINS; AMPHIBIANS; ANIMALS; DNA VIRUS INFECTIONS; HUMANS; RANAVIRUS; URODELA; XENOPUS LAEVIS;

EID: 82155191835     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v3112065     Document Type: Article

References (83)

1. Stuart, S.N.; Chanson, J.S.; Cox, N.A.; Young, B.E.; Rodrigues, A.S.; Fischman, D.L.; Waller, R.W. Status and trends of amphibian declines and extinctions worldwide. Science 2004, 306, 1783-1786.
2. The International Union for Conservation of Nature and Natural Resources (IUCN) Red List of Threatened Species (Amphibians). Available online: http://www.iucnredlist.org/initiatives/amphibians (28 October 2011).
3. Daszak, P.; Berger, L.; Cunningham, A.A.; Hyatt, A.D.; Green, D.E.; Speare, R. Emerging infectious diseases and amphibian population declines. Emerg. Infect. Dis. 1999, 5, 735-748.
4. Collins, J.P. Amphibian decline and extinction: What we know and what we need to learn. Dis. Aquat. Organ. 2010, 92, 93-99.
5. Kilpatrick, A.M.; Briggs, C.J.; Daszak, P. The ecology and impact of chytridiomycosis: An emerging disease of amphibians. Trends Ecol. Evol. 2010, 25, 109-118.
6. 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.
7. Robert, J.; Gregory Chinchar, V. Ranaviruses: An emerging threat to ectothermic vertebrates report of the first international symposium on ranaviruses, Minneapolis MN July 8, 2011. Dev. Comp. Immunol. 2011, doi:10.1016/j.dci.2011.08.008.
8. Lesbarréres, D.; Balseiro, A.; Brunner, J.; Chinchar, V.G.; Duffus, A.; Kerby, J.; Miller, D.L.; Robert, J.; Schock, D.M.; Waltzek, T.; et al. Symposium report:Ranavirus: Past, present and future. Biol. Lett. 2011. in press.
9. Kerby, J. Global focus: 1st international symposium on Ranaviruses. FrogLog 2011, 98, 33-35.
10. 2011 International Ranavirus Symposium. Available online: http://Fwf.Ag.Utk.Edu/Mgray/Ranavirus/2011ranavirus.htm (accessed on 28 October 2011).
11. Global Ranavirus Consortium. Available online: http://fwf.Ag.Utk.Edu/mgray/ranavirus/ranavirus.htm (accessed on 28 October 2011).
12. The World Organisation for Animal Health. Available online: http://www.Oie.Int/ (accessed on 28 October 2011).
13. 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, 101-108.
14. Gray, M.J.; Miller, D.L.; Hoverman, J.T. Ecology and pathology of amphibian ranaviruses. Dis. Aquat. Organ. 2009, 87, 243-266.
15. Chinchar, V.G.; Hyatt, A.; Miyazaki, T.; Williams, T. Family iridoviridae: Poor viral relations no longer. Curr. Top. Microbiol. Immunol. 2009, 328, 123-170.
16. Chinchar, V.G. Ranaviruses (family iridoviridae): Emerging cold-blooded killers. Arch. Virol. 2002, 147, 447-470.
17. Carey, C.; Cohen, N.; Rollins-Smith, L. Amphibian declines: An immunological perspective. Dev. Comp. Immunol. 1999, 23, 459-472.
18. Hayes, T.B.; Falso, P.; Gallipeau, S.; Stice, M. The cause of global amphibian declines: A developmental endocrinologist's perspective. J. Exp. Biol. 2010, 213, 921-933.
19. Workenhe, S.T.; Rise, M.L.; Kibenge, M.J.; Kibenge, F.S. The fight between the teleost fish immune response and aquatic viruses. Mol. Immunol. 2010, 47, 2525-2536.
20. Robert, J.; Ohta, Y. Comparative and developmental study of the immune system in xenopus. Dev. Dyn. 2009, 238, 1249-1270.
21. Goodbourn, S.; Didcock, L.; Randall, R.E. Interferons: Cell signalling, immune modulation, antiviral response and virus countermeasures. J. Gen. Virol. 2000, 81, 2341-2364.
22. Janeway, C.A., Jr. The immune system evolved to discriminate infectious nonself from noninfectious self. Immunol. Today 1992, 13, 11-16.
23. Lee, S.H.; Miyagi, T.; Biron, C.A. Keeping nk cells in highly regulated antiviral warfare. Trends Immunol. 2007, 28, 252-259.
24. Prince, L.R.; Whyte, M.K.; Sabroe, I.; Parker, L.C. The role of tlrs in neutrophil activation. Curr. Opin. Pharmacol. 2011, 11, 397-403.
25. Viret, C.; Janeway, C.A., Jr. Mhc and t cell development. Rev. Immunogenet. 1999, 1, 91-104.
26. Du Pasquier, L.; Schwager, J.; Flajnik, M.F. The immune system of xenopus. Annu. Rev. Immunol. 1989, 7, 251-275.
27. 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, 6783-6789.
28. Li, J.; Barreda, D.R.; Zhang, Y.A.; Boshra, H.; Gelman, A.E.; Lapatra, S.; Tort, L.; Sunyer, J.O. B lymphocytes from early vertebrates have potent phagocytic and microbicidal abilities. Nat. Immunol. 2006, 7, 1116-1124.
29. Ishii, A.; Kawasaki, M.; Matsumoto, M.; Tochinai, S.; Seya, T. Phylogenetic and expression analysis of amphibian xenopus toll-like receptors. Immunogenetics 2007, 59, 281-293.
30. Roach, J.C.; Glusman, G.; Rowen, L.; Kaur, A.; Purcell, M.K.; Smith, K.D.; Hood, L.E.; Aderem, A. The evolution of vertebrate toll-like receptors. Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 9577-9582.
31. Bleicher, P.A.; Rollins-Smith, L.A.; Jacobs, D.M.; Cohen, N. Mitogenic responses of frog lymphocytes to crude and purified preparations of bacterial lipopolysaccharide (lps). Dev. Comp. Immunol. 1983, 7, 483-496.
32. Mescher, A.L.; Wolf, W.L.; Moseman, E.A.; Hartman, B.; Harrison, C.; Nguyen, E.; Neff, A.W. Cells of cutaneous immunity in xenopus: Studies during larval development and limb regeneration. Dev. Comp. Immunol. 2007, 31, 383-393.
33. 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, 4912-4922.
34. Du Pasquier, L.; Robert, J.; Courtet, M.; Mussmann, R. B-cell development in the amphibian xenopus. Immunol. Rev. 2000, 175, 201-213.
35. Hsu, E. Mutation, selection, and memory in b lymphocytes of exothermic vertebrates. Immunol. Rev. 1998, 162, 25-36.
36. Wilson, M.; Hsu, E.; Marcuz, A.; Courtet, M.; Du Pasquier, L.; Steinberg, C. What limits affinity maturation of antibodies in xenopus-The rate of somatic mutation or the ability to select mutants? EMBO J. 1992, 11, 4337-4347.
37. 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, 198-206.
38. 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, 715-726.
39. 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, 254-262.
40. Robert, J. Comparative study of infectivity of frog virus 3, rana catesbeiana virus z, and ambystoma tigrinum virus in xenopus laevis and xenopus tropicalis. University of Rochester Medical Center, Rocherster, NY, USA. Unpublished work, 2011.
41. 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, 667-675.
42. Morales, H.D.; Robert, J. Characterization of primary and memory cd8 t-cell responses against ranavirus (fv3) in xenopus laevis. J. Virol. 2007, 81, 2240-2248.
43. Panchanathan, V.; Chaudhri, G.; Karupiah, G. Antiviral protection following immunization correlates with humoral but not cell-mediated immunity. Immunol. Cell Biol. 2010, 88, 461-467.
44. 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, 649-657.
45. Zupanovic, Z.; Lopez, G.; Hyatt, A.D.; Green, B.; Bartran, G.; Parkes, H.; Whittington, R.J.; Speare, R. Giant toads bufo marinus in australia and venezuela have antibodies against 'ranaviruses'. Dis. Aquat. Organ. 1998, 32, 1-8.
46. Majji, S.; LaPatra, S.; Long, S.M.; Sample, R.; Bryan, L.; Sinning, A.; Chinchar, V.G. Rana catesbeiana virus z (rcv-z): A novel pathogenic ranavirus. Dis. Aquat. Organ. 2006, 73, 1-11.
47. Cunningham, A.A.; Tems, C.A.; Russell, P.H. Immunohistochemical demonstration of ranavirus antigen in the tissues of infected frogs (rana temporaria) with systemic haemorrhagic or cutaneous ulcerative disease. J. Comp. Pathol. 2008, 138, 3-11.
48. Chinchar, V.G.; Bryan, L.; Silphadaung, U.; Noga, E.; Wade, D.; Rollins-Smith, L. Inactivation of viruses infecting ectothermic animals by amphibian and piscine antimicrobial peptides. Virology 2004, 323, 268-275.
49. Chinchar, V.G.; Wang, J.; Murti, G.; Carey, C.; Rollins-Smith, L. Inactivation of frog virus 3 and channel catfish virus by esculentin-2p and ranatuerin-2p, two antimicrobial peptides isolated from frog skin. Virology 2001, 288, 351-357.
50. Tweedell, K.; Granoff, A. Viruses and renal carcinoma of rana pipiens. V. Effect of frog virus 3 on developing frog embryos and larvae. J. Natl. Cancer Inst. 1968, 40, 407-410.
51. Miller, D.L.; Rajeev, S.; Gray, M.J.; Baldwin, C.A. Frog virus 3 infection, cultured American bullfrogs. Emerg. Infect. Dis. 2007, 13, 342-343.
52. 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. et al. Mass mortality associated with a frog virus 3- like ranavirus infection in farmed tadpoles rana catesbeiana from brazil. Dis. Aquat. Organ. 2009, 86, 181-191.
53. Chen, G.; Robert, J. Susceptibility of xenopus laevis tadpoles to infection by the ranavirus frogvirus 3 correlates with a weak and delayed innate immune response. Eur. J. Immunol. Submitted for publication, 2011.
54. 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, 11-17.
55. Whitley, D.S.; Yu, K.; Sample, R.C.; Sinning, A.; Henegar, J.; Norcross, E.; Chinchar, V.G. Frog virus 3 orf 53r, a putative myristoylated membrane protein, is essential for virus replication in vitro. Virology 2010, 405, 448-456.
56. Robert, J.; George, E.; De Jesus Andino, F.; Chen, G. Waterborne infectivity of the ranavirus frog virus 3 in xenopus laevis. Virology 2011, 417, 410-417.
57. Haislip, N.A.; Gray, M.J.; Hoverman, J.T.; Miller, D.L. Development and disease: How susceptibility to an emerging pathogen changes through anuran development. PLoS One 2011, 6, e22307.
58. Gray, M.J. Are ranaviruses capable of contributing to amphibian species declines? Available online: http://fwf.ag.utk.edu/mgray/ranavirus/2011Symposium/Gray.pdf (accessed on 28 October 2011).
59. Flajnik, M.F.; Du Pasquier, L. The major histocompatibility complex of frogs. Immunol. Rev. 1990, 113, 47-63.
60. Teacher, A.G.; Garner, T.W.; Nichols, R.A. Evidence for directional selection at a novel major histocompatibility class i marker in wild common frogs (rana temporaria) exposed to a viral pathogen (ranavirus). PLoS One 2009, 4, e4616.
61. Cotter, J.D.; Storfer, A.; Page, R.B.; Beachy, C.K.; Voss, S.R. Transcriptional response of mexican axolotls to ambystoma tigrinum virus (atv) infection. BMC Genomics 2008, 9, 493.
62. Manning, M.J. Histological organization of the spleen: Implications for immune functions in amphibians. Res. Immunol. 1991, 142, 355-359.
63. Ching, Y.C.; Wedgwood, R.J. Immunologic responses in the axolotl, siredon mexicanum. J. Immunol. 1967, 99, 191-200.
64. Charlemagne, J. Thymus independent anti-horse erythrocyte antibody response and suppressor t cells in the mexican axolotl (amphibia, urodela, ambystoma mexicanum). Immunology 1979, 36, 643-648.
65. Kaufman, J.; Volk, H.; Wallny, H.J. A minimal essential mhc and an unrecognized hc: Two extremes in selection for polymorphism. Immunol. Rev. 1995, 143, 63-88.
66. Tournefier, A.; Laurens, V.; Chapusot, C.; Ducoroy, P.; Padros, M.R.; Salvadori, F.; Sammut, B. Structure of mhc class i and class ii cdnas and possible immunodeficiency linked to class ii expression in the mexican axolotl. Immunol. Rev. 1998, 166, 259-277.
67. Cohen, N. Amphibian transplantation reactions. Amer. Zool. 1971, 11, 93-205.
68. Rojas, S.; Richards, K.; Jancovich, J.K.; Davidson, E.W. Influence of temperature on ranavirus infection in larval salamanders ambystoma tigrinum. Dis. Aquat. Organ. 2005, 63, 95-100.
69. Sheafor, B.; Davidson, E.W.; Parr, L.; Rollins-Smith, L. Antimicrobial peptide defenses in the salamander, ambystoma tigrinum, against emerging amphibian pathogens. J. Wildl. Dis. 2008, 44, 226-236.
70. Whitley, D.S.; Sample, R.C.; Sinning, A.R.; Henegar, J.; Chinchar, V.G. Antisense approaches for elucidating ranavirus gene function in an infected fish cell line. Dev. Comp. Immunol. 2011, 35, 937-948.
71. Chen, G.; Ward, B.M.; Yu, E.K.; Chinchar, V.G.; Robert, J. 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. 2011, 85, 11131-11138.
72. Langland, J.O.; Cameron, J.M.; Heck, M.C.; Jancovich, J.K.; Jacobs, B.L. Inhibition of pkr by rna and DNA viruses. Virus Res. 2006, 119, 100-110.
73. Jancovich, J.K.; Jacobs, B.L. Innate immune evasion mediated by the ambystoma tigrinum virus eukaryotic translation initiation factor 2alpha homologue. J. Virol. 2011, 85, 5061-5069.
74. Rothenburg, S.; Chinchar, V.G.; Dever, T.E. Characterization of a ranavirus inhibitor of the antiviral protein kinase pkr. BMC Microbiol. 2011, 11, 56.
75. Maniero, G.D.; Carey, C. Changes in selected aspects of immune function in the leopard frog, rana pipiens, associated with exposure to cold. J. Comp. Physiol. B 1997, 167, 256-263.
76. Kiesecker, J.M.; Blaustein, A.R.; Belden, L.K. Complex causes of amphibian population declines. Nature 2001, 410, 681-684.
77. Bancroft, B.A.; Baker, N.J.; Blaustein, A.R. A meta-analysis of the effects of ultraviolet b radiation and its synergistic interactions with ph, contaminants, and disease on amphibian survival. Conserv. Biol. 2008, 22, 987-996.
78. Langerveld, A.J.; Celestine, R.; Zaya, R.; Mihalko, D.; Ide, C.F. Chronic exposure to high levels of atrazine alters expression of genes that regulate immune and growth-related functions in developing xenopus laevis tadpoles. Environ. Res. 2009, 109, 379-389.
79. Christin, M.S.; Menard, L.; Gendron, A.D.; Ruby, S.; Cyr, D.; Marcogliese, D.J.; Rollins-Smith, L.; Fournier, M. Effects of agricultural pesticides on the immune system of xenopus laevis and rana pipiens. Aquat. Toxicol. 2004, 67, 33-43.
80. Kerby, J.L.; Hart, A.J.; Storfer, A. Combined effects of virus, pesticide, and predator cue on the larval tiger salamander (ambystoma tigrinum). Ecohealth 2011, doi:10.1007/s10393-011-0682-1.
81. Williams, T.; Barbosa-Solomieu, V.; Chinchar, V.G. A decade of advances in iridovirus research. Adv. Virus Res. 2005, 65, 173-248.
82. Forson, D.D.; Storfer, A. Atrazine increases ranavirus susceptibility in the tiger salamander, ambystoma tigrinum. Ecol. Appl. 2006, 16, 2325-2332.
83. Greer, A.L.; Brunner, J.L.; Collins, J.P. Spatial and temporal patterns of ambystoma tigrinum virus (atv) prevalence in tiger salamanders ambystoma tigrinum nebulosum. Dis. Aquat. Organ. 2009, 85, 1-6.