Development and disease: How susceptibility to an emerging pathogen changes through anuran development

PLoS ONE

Volumn 6, Issue 7, 2011, Pages

  Haislip, Nathan A ^a   Gray, Matthew J ^a   Hoverman, Jason T ^a,c   Miller, Debra L ^a,b  

^a UNIVERSITY OF TENNESSEE   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

^c UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA;

AMPHIBIAN DISEASE; ANAXYRUS AMERICANUS; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; FROG; FROG VIRUS 3; HATCHLING; HOST PATHOGEN INTERACTION; HYLA CHRYSOSCELIS; INFECTION SENSITIVITY; IRIDOVIRUS; LARVAL STAGE; LITHOBATES CLAMITANS; LITHOBATES PIPIENS; LITHOBATES SYLVATICUS; METAMORPHOSIS; MORBIDITY; MORTALITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PREVALENCE; PSEUDACRIS FERIARUM; RANAVIRUS INFECTION; SCAPHIOPUS HOLBROOKII; SPECIES COMPARISON; TADPOLE; VIRUS VIRULENCE; ANIMAL; ANIMAL DISEASE; DISEASE PREDISPOSITION; DNA VIRUS INFECTION; FROGS AND TOADS; GROWTH, DEVELOPMENT AND AGING; PATHOGENICITY; VIROLOGY;

AMPHIBIA; METAMORPHA; RANAVIRUS;

ANIMALS; ANURA; DISEASE SUSCEPTIBILITY; DNA VIRUS INFECTIONS; RANAVIRUS;

EID: 79960661542     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0022307     Document Type: Article

References (64)

1. Johnson PJ, Kellermanns E, Bowerman J, (2011) Critical windows of disease risk: amphibian pathology driven by developmental changes in host resistance and tolerance. Functional Ecology In press.
2. Pryor JL, Hughes C, Foster W, Hales B, Robaire B, (2000) Critical windows of exposure for children's health: the reproductive sustem in animals and humans. Environmental Health Perspectives 108: 491-503.
3. Webster WS, (1998) Teratogen update: congenital rubella. Teratology 58: 12-23.
4. Tabin CJ, (1998) A developmental model for thalidomide defects. Nature 396: 322-323.
5. Wake DB, Vredenburg VT, (2008) Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proceedings of the National Academy of Sciences 105: 11466-11473.
6. Wright KM, Whitaker BR, (2001) Amphibian medicine and captive husbandry Malabar, Florida Krieger Publishing Company.
7. Green DE, Converse KA, Schrader AK, (2002) Epizootiology of sixty-four amphibian morbidity and mortality events in the USA, 1996-2001. Annals of the New York Academy of Sciences 969: 323-339.
8. Muths E, Gallant AL, Campbell EHC, Battaglin WA, Green DE, et al. (2006) The Amphibian Research and Monitoring Initiative (ARMI): 5-year report: U.S. Geological Survey Scientific Investigations Report 2006-5224.
9. Converse KA, Green DE, (2005) Diseases of tadpoles. In: Majumdar SK, Huffman JE, Brenner FJ, Panah AI, editors. Wildlife diseases: Landscape epidemiology, spatial distribution and utilization of remote sensing technology Easton, Pennsylvania The Pennsylvania Academy of Science pp. 72-88.
10. Chinchar VG, (2002) Ranaviruses (family Iridoviridae): emerging cold-blooded killers- Brief review. Archives of Virology 147: 447-470.
11. Chinchar VG, Essbauer S, He JG, Hyatt A, Miyazaki T, et al. (2005) Iridoviridae. In: Fauguet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA, editors. Virus taxonomy: 8th report of the international committee on the taxonomy of viruses London Elsevier pp. 163-175.
12. Gray MJ, Miller DL, Hoverman JT, (2009) Ecology and pathology of amphibian ranaviruses. Diseases of Aquatic Organisms 87: 243-266.
13. Du Pasquier L, Schwager J, Flajnik MF, (1989) The immune system of Xenopus. Annual Review of Immunology 7: 251-275.
14. Rollins-Smith LA, (1998) Metamorphosis and the amphibian immune system. Immunological Reviews 166: 221-230.
15. Gantress J, Maniero GD, Cohen N, Robert J, (2003) Development and characterization of a model system to study amphibian immune responses to iridoviruses. Virology 311: 254-262.
16. Scotthoefer AM, Cole RA, Beasley VR, (2003) Relationship of tadpole stage to location of echinostome cercariae encystment and the consequences for tadpole survival. Journal of Parasitology 89: 475-482.
17. Daszak P, Cunningham AA, Hyatt AD, (2000) Wildlife ecology- Emerging infectious diseases of wildlife: threats to biodiversity and human health. Science 287: 443-449.
18. Dobson A, Foufopoulos J, (2001) Emerging infectious pathogens of wildlife. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 356: 1001-1012.
19. Woolhouse MEJ, Haydon DT, Antia R, (2005) Emerging pathogens: the epidemiology and evolution of species jumps. Trends in Ecology & Evolution 20: 238-244.
20. Johnson PTJ, Hartson RB, (2009) All hosts are not equal: explaining differential patterns of malformations in an amphibian community. Journal of Animal Ecology 78: 191-201.
21. Schock DM, Bollinger TK, Chinchar VG, Jancovich JK, Collins JP, (2008) Experimental evidence that amphibian ranaviruses are multi-host pathogens. Copeia pp. 133-143.
22. Hoverman JT, Gray MJ, Miller DL, (2010) Anuran susceptibilities to ranaviruses: role of species identity, exposure route, and a novel virus isolate. Diseases of Aquatic Organisms 89: 97-107.
23. Kilpatrick AM, Briggs CJ, Daszak P, (2010) The ecology and impact of chytridiomycosis: an emerging disease of amphibians. Trends in Ecology & Evolution 25: 109-118.
24. Schock DM, Ruthig GR, Collins JP, Kutz SJ, Carriere S, et al. (2009) Amphibian chytrid fungus and ranaviruses in the Northwest territories, Canada. Diseases of Aquatic Organisms 92: 231-240.
25. Cullen BR, Owens L, (2002) Experimental challenge and clinical cases of Bohle iridovirus (BIV) in native Australian anurans. Diseases of Aquatic Organisms 49: 83-92.
26. Cullen BR, Owens L, Whittington RJ, (1995) Experimental infection of Australian anurans (Limnodynastes terraereginae and Litoria latopalmata) with Bohle iridovirus. Diseases of Aquatic Organisms 23: 83-92.
27. Lang E, Gerhardt C, Davidson C, (2009) The frogs and toads of North America New York, New York, USA Houghton Mifflin Company.
28. Miller DL, Rajeev S, Gray MJ, Baldwin CA, (2007) Frog virus 3 infection, cultured American bullfrogs. Emerging Infectious Diseases 13: 342-343.
29. Gosner KL, (1960) A simplified table for staging anuran embryos and larvae with notes and identification. Herpetologica 16: 183-190.
30. Bollinger TK, Mao JH, Schock D, Brigham RM, Chinchar VG, (1999) Pathology, isolation, and preliminary molecular characterization of a novel iridovirus from tiger salamanders in Saskatchewan. Journal of Wildlife Diseases 35: 413-429.
31. Brunner JL, Richards K, Collins JP, (2005) Dose and host characteristics influence virulence of ranavirus infections. Oecologia 144: 399-406.
32. Pearman PB, Garner TWJ, (2005) Susceptibility of Italian agile frog populations to an emerging strain of ranavirus parallels population genetic diversity. Ecology Letters 8: 401-408.
33. Rojas S, Richards K, Jancovich JK, Davidson EW, (2005) Influence of temperature on Ranavirus infection in larval salamanders Ambystoma tigrinum. Diseases of Aquatic Organisms 63: 95-100.
34. Relyea RA, (2002) Competitor-induced plasticity in tadpoles: Consequences, cues, and connections to predator-induced plasticity. Ecological Monographs 72: 523-540.
35. Thibaudeau G, Altig R, (1999) Endotrophic anurans. In: McDiarmid RW, Altig R, editors. Tadpoles: the biology of anuran larvae Chicago, Illinois, USA University of Chicago Press pp. 170-188.
36. Picco AM, Brunner JL, Collins JP, (2007) Susceptibility of the endangered California tiger salamander, Ambystoma californiense, to ranavirus infection. Journal of Wildlife Diseases 43: 286-290.
37. Stokes ME, Davis CS, Kock GG, (2000) Categorical data analysis using the SAS® system Cary North Carolina, USA SAS Institute.
38. Zar JH, (1999) Biostatistical analysis Upper Saddle River, New Jersey, USA Prentice Hall.
39. Tweedell K, Granoff A, (1968) Viruses and renal carcinoma of Rana pipiens. V. Effect of Frog Virus 3 on developing frog embryos and larvae. Journal of the National Cancer Institute 40: 407-410.
40. Berrill M, Coulson DR, McGillivray L, Pauli BD, (1998) Toxicity of endosulfan to aquatic stages of anuran amphibians. Environmental Toxicology and Chemistry 17: 1738-1744.
41. Pauli BD, Coulson DR, Berrill M, (1999) Sensitivity of amphibian embryos and tadpoles to MIMIC 240LV insecticide following single or double exposures. Environmental Toxicology and Chemistry 18: 2538-2544.
42. Han Y, Yu H, Yang X, Rees HH, Liu J, et al. (2008) A serine proteinase inhibitor from frog eggs with bacteriostatic activity. Comparative Biochemistry and Physiology B-Biochemistry & Molecular Biology 149: 58-62.
43. Green DE, Converse KA, (2005) Diseases of frogs and toads. In: Majumdar SK, Huffman JE, Brenner FJ, Panah AI, editors. Wildlife diseases: Landscape epidemiology, spatial distribution and utilization of remote sensing technology Easton, Pennsylvania The Pennsylvania Academy of Science pp. 89-117.
44. Greer AL, Berrill M, Wilson PJ, (2005) Five amphibian mortality events associated with ranavirus infection in south central Ontario, Canada. Diseases of Aquatic Organisms 67: 9-14.
45. Warne RW, Crespi EJ, Brunner JL, (2011) Escape from the pond: stress and developmental responses to ranavirus infection in wood frog tadpoles. Functional Ecology 25: 139-146.
46. Flajnik MF, Hsu E, Kaufman JF, Du Pasquier L, (1987) Changes in the immune system during metamorphosis of Xenopus. Immunology Today 8: 58-64.
47. Rollins-Smith LA, (2001) Neuroendocrine-immune system interactions in amphibians- Implications for understanding global amphibian declines. Immunologic Research 23: 273-280.
48. Rollins-Smith LA, Blair PJ, (1993) The effects of corticosteroid hormones and thyroid hormones on lymphocyte viability and proliferation during development and metamorphosis of Xenopus laevis. Differentiation 54: 155-160.
49. Grant PR, Clothier H, Johnson RO, Ruben LN, (1998) In situ lymphocyte apoptosis in larval Xenopus laevis, the South African clawed toad. Developmental and Comparative Immunology 22: 449-455.
50. Pallister JA, Halliday DC, Robinson AJ, Venables D, Voysey RD, et al. (2011) Assessment of Virally Vectored Autoimmunity as a Biocontrol Strategy for Cane Toads. PLoS ONE 6 (1): e14576 doi:10.1371/journal.pone.0014576.
51. Newman RA, (1992) Adaptive plasticity in amphibian metamorphosis. Bioscience 42: 671-678.
52. Denver RJ, (1997) Environmental stress as a developmental cue: Corticotropin-releasing hormone is a proximate mediator of adaptive phenotypic plasticity in amphibian metamorphosis. Hormones and Behavior 31: 169-179.
53. Zettergren LD, (2000) Ontogeny of B cells expressing IgM in embryonic and larval tissues of the American grass frog, Rana pipiens. Journal of Experimental Zoology 286: 737-744.
54. Maniero GD, Morales H, Gantress J, Robert J, (2006) Generation of a long-lasting, protective, and neutralizing antibody response to the ranavirus FV3 by the frog Xenopus. Developmental and Comparative Immunology 30: 649-657.
55. Morales HD, Abramowitz L, Gertz J, Sowa J, Vogel A, et al. (2010) Innate immune responses and permissiveness to ranavirus infection of peritoneal leukocytes in the frog Xenopus laevis. American Society of Microbiology 84: 4912-4922.
56. Harp EM, Petranka JW, (2006) Ranavirus in wood frogs (Rana sylvatica): Potential sources of transmission within and between ponds. Journal of Wildlife Diseases 42: 307-318.
57. Gahl MK, Calhoun AJK, (2010) The role of multiple stressors in ranavirus-caused amphibian mortalities in Acadia National Park wetlands. Canadian Journal of Zoology 88: 108-121.
58. Cotter JD, Storfer A, Page RB, Beachy CK, Voss SR, (2008) Transcriptional response of Mexican axolotls to Ambystoma tigrinum virus (ATV) infection. BMC Genomics 9: 493.
59. Haimovich J, Du Pasquier L, (1973) Specificity of antibodies in amphibian larvae possessing a small number of lymphocytes. Proceeding of the National Academy of Science (USA) 70: 1898-1902.
60. Hsu E, Du Pasquier L, (1984) Ontogenyof the immune system in Xenopus. II. Antibody repertoire differences between larvae and adults. Differentiation 28: 116-122.
61. Robert J, Abramowitz L, Gantress J, Morales HD, (2007) Xenopus laevis: A possible vector of ranavirus infection? Journal of Wildlife Diseases 43: 645-652.
62. Richmond JQ, Savage AE, Zamudio KR, Rosenblum EB, (2009) Toward immunogenetic studies of amphibian chytridiomycosis: Linking innate and acquired immunity. Bioscience 59: 311-320.
63. ter Braak CJF, (1986) Canonical correspondence analysis: a new eigenvector technique for multivariate direct gradient analysis. Ecology 67: 1167-1179.
64. Allen LJS, (2006) An Introduction to Mathematical Biology Upper Saddle River, New Jersey Prentice Hall.