Immune defenses against Batrachochytrium dendrobatidis, a fungus linked to global amphibian declines, in the South African clawed frog, Xenopus laevis

Infection and Immunity

Volumn 78, Issue 9, 2010, Pages 3981-3992

  Ramsey, Jeremy P ^a   Reinert, Laura K ^a   Harper, Laura K ^a   Woodhams, Douglas C ^a,b   Rollins Smith, Louise A ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ANTIBODY; IMMUNOGLOBULIN M ANTIBODY; IMMUNOGLOBULIN X ANTIBODY; IMMUNOGLOBULIN Y ANTIBODY; NORADRENALIN; POLYPEPTIDE ANTIBIOTIC AGENT; UNCLASSIFIED DRUG; ANTIMICROBIAL CATIONIC PEPTIDE; FUNGUS ANTIBODY;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN BINDING; ARTICLE; BATRACHOCHYTRIUM DENDROBATIDIS; CHYTRIDIOMYCOSIS; CONTROLLED STUDY; EXPERIMENTAL MODEL; IMMUNIZATION; IMMUNOCOMPETENCE; INFECTION SENSITIVITY; INNATE IMMUNITY; IRRADIATION; LEUKOCYTE COUNT; MUCOSAL IMMUNITY; MUCUS SECRETION; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; XENOPUS LAEVIS; ANIMAL; BLOOD; CHYTRIDIOMYCETES; IMMUNOLOGY; MICROBIOLOGY; MUCOSA; MYCOSIS; PHYSIOLOGY; SKIN;

ADAPTIVE IMMUNITY; ANIMALS; ANTIBODIES, FUNGAL; ANTIMICROBIAL CATIONIC PEPTIDES; CHYTRIDIOMYCOTA; IMMUNITY, INNATE; IMMUNIZATION; MUCOUS MEMBRANE; MYCOSES; NOREPINEPHRINE; SKIN; XENOPUS LAEVIS;

EID: 77956623272     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00402-10     Document Type: Article

References (70)

1. a-(4-24)] from skin secretions of Xenopus laevis. Eur. J. Biochem. 149:531-535.
2. Benson, J., and M. E. Hadley. 1969. In vitro characterization of adrenergic receptors controlling skin gland secretion in two anurans Rana pipiens and Xenopus laevis. Comp. Biochem. Physiol. 30:857-864.
3. Berger, L., A. D. Hyatt, R. Speare, and J. E. Longcore. 2005. Life cycle stages of the amphibian chytrid Batrachochytrium dendrobatidis. Dis. Aquat. Organ. 68:51-63.
4. Berger, L., R. Speare, P. Daszak, D. E. Green, A. A. Cunningham, C. L. Goggin, R. Slocombe, M. A. Ragan, A. D. Hyatt, K. R. McDonald, H. B. Hines, K. R. Lips, G. Marantelli, and H. Parkes. 1998. Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proc. Natl. Acad. Sci. U. S. A. 95:9031-9036.
5. Blomberg, B., C. C. A. Bernard, and L. Du Pasquier. 1980. In vitro evidence for T-B lymphocyte collaboration in the clawed toad, Xenopus. Eur. J. Immunol. 10:869-876.
6. Boyle, D. G., D. B. Boyle, V. Olsen, J. A. T. Morgan, and A. D. Hyatt. 2004. Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time TaqMan PCR assay. Dis. Aquat. Organ. 60:141-148.
7. Brucker, R. M., R. N. Harris, C. R. Schwantes, T. N. Gallaher, D. C. Flaherty, B. A. Lam, and K. P. C. Minbiole. 2008. Amphibian chemical defense: antifungal metabolites of the microsymbiont Janthinobacterium lividum on the salamander Plethodon cinereus. J. Chem. Ecol. 34:1422-1429.
8. Carey, C., J. E. Bruzgul, L. J. Livo, M. L. Walling, K. A. Kuehl, B. F. Dixon, A. P. Pessier, R. A. Alford, and K. B. Rogers. 2006. Experimental exposures of boreal toads (Bufo boreas) to a pathogenic chytrid fungus (Batrachochytrium dendrobatidis). EcoHealth 3:5-21.
9. Carey, C., N. Cohen, and L. Rollins-Smith. 1999. Amphibian declines: an immunological perspective. Dev. Comp. Immunol. 23:459-472.
10. Cerutti, A., and M. Rescigno. 2008. The biology of intestinal immunoglobulin A responses. Immunity 28:740-750.
11. Conlon, J. M., D. C. Woodhams, H. Razaa, L. Coquet, J. Leprince, T. Jouenne, H. Vaudry, and L. A. Rollins-Smith. 2007. Peptides with differential cytolytic activity from skin secretions of the Lemur leaf frog Hylomantis lemur (Hylidae: Phyllomedusinae). Toxicon 50:498-506.
12. Daszak, P., A. A. Cunningham, and A. D. Hyatt. 2003. Infectious disease and amphibian population declines. Divers. Distrib. 9:141-150.
13. Dockray, G. J., and C. R. Hopkins. 1975. Caerulein secretion by dermal glands in Xenopus laevis. J. Cell Biol. 64:724-733.
14. Du Pasquier, L., J. Schwager, and M. F. Flajnik. 1989. The immune system of Xenopus. Annu. Rev. Immunol. 7:251-275.
15. Flajnik, M. F., S. Ferrone, N. Cohen, and L. Du Pasquier. 1990. Evolution of the MHC: antigenicity and unusual tissue distribution of Xenopus (frog) class II molecules. Mol. Immunol. 27:451-462.
16. a and the caerulein and xenopsin precursors from Xenopus laevis. J. Biol. Chem. 261:5341-5349.
17. Giovannini, M. G., L. Poulter, B. W. Gibson, and D. H. Williams. 1987. Biosynthesis and degradation of peptides derived from Xenopus laevis prohormones. Biochem. J. 243:113-120.
18. Harris, R. N., R. M. Brucker, J. B. Walke, M. H. Becker, C. R. Schwantes, D. C. Flaherty, B. A. Lam, D. C. Woodhams, C. J. Briggs, V. T. Vredenburg, and K. P. C. Minbiole. 2009. Skin microbes on frogs prevent morbidity and mortality caused by a lethal skin fungus. ISME J. 3:818-824.
19. Holmes, C., and M. Balls. 1978. In vitro studies on the control of myoepithelial cell contraction in the granular glands of Xenopus laevis skin. Gen. Comp. Endocrinol. 36:255-263.
20. Horton, J. D., J. H. Russ, P. Aitchison, and T. L. Horton. 1987. Thymocyte/stromal cell chimaerism in allothymus-grafted Xenopus: developmental studies using the X. borealis fluorescence marker. Development 100:107-117.
21. Hsu, E., and L. Du Pasquier. 1984. Studies in Xenopus immunoglobulins using monoclonal antibodies. Mol. Immunol. 21:257-270.
22. Hyatt, A. D., D. G. Boyle, V. Olsen, D. B. Boyle, L. Berger, D. Obendorf, A. Dalton, K. Kriger, M. Hero, H. Hines, R. Phillott, R. Campbell, G. Marantelli, F. Gleason, and A. Colling. 2007. Diagnostic assays and sampling protocols for the detection of Batrachochytrium dendrobatidis. Dis. Aquat. Organ. 73:175-192.
23. James, S., B. F. Gibbs, K. Toney, and H. P. J. Bennett. 1994. Purification of antimicrobial peptides from an extract of the skin of Xenopus laevis using heparin-affinity HPLC: characterization by ion-spray mass spectrometry. Anal. Biochem. 217:84-90.
24. Jürgens, G. B., L. A. Gartland, L. Du Pasquier, J. D. Horton, T. W. Göbel, and M. D. Cooper. 1995. Identification of a candidate CD5 homologue in the amphibian Xenopus laevis. J. Immunol. 155:4218-4223.
25. Kuchler, K., G. Kriel, and I. Sures. 1989. The genes for the frog skin peptides GLa, xenopsin, levitide and caerulein contain a homologous export exon encoding a signal sequence and part of an amphiphilic peptide. Eur. J. Biochem. 179:281-285.
26. Lips, K. R., F. Brem, R. Brenes, J. D. Reeve, R. A. Alford, J. Voyles, C. Carey, L. Livo, A. P. Pessier, and J. P. Collins. 2006. Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proc. Natl. Acad. Sci. U. S. A. 103:3165-3170.
27. Lips, K. R., J. D. Reeve, and L. R. Witters. 2003. Ecological traits predicting amphibian population declines in Central America. Conserv. Biol. 17:1078-1088.
28. Lobb, C. J., and L. W. Clem. 1981. Phylogeny of immunoglobulin structure and function. XI. Secretory immunoglobulins in the cutaneous mucus of the sheepshead, Archosargus probatocephalus. Dev. Comp. Immunol. 5:587-596.
29. Longcore, J. E., A. P. Pessier, and D. K. Nichols. 1999. Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia 91:219-227.
30. McClanahan, L. J., and R. Baldwin. 1969. Rate of water uptake through the integument of the desert toad, Bufo punctatus. Comp. Biochem. Physiol. 28:381-389.
31. Mestecky, J., and M. W. Russell. 2009. Specific antibody activity, glycan heterogeneity, and polyreactivity contribute to the protective activity of S-IgA at mucosal surfaces. Immunol. Lett. 124:57-62.
32. Moore, S., C. L. Bevins, M. M. Brasseur, N. Tomassini, K. Turner, H. Eck, and M. Zasloff. 1991. Antimicrobial peptides in the stomach of Xenopus laevis. J. Biol. Chem. 266:19851-19857.
33. Mussman, R., L. Du Pasquier, and E. Hsu. 1996. Is Xenopus IgX an analog of IgA? Eur. J. Immunol. 26:2823-2830.
34. Pessier, A. P., D. K. Nichols, J. E. Longcore, and M. S. Fuller. 1999. Cutaneous chytridiomycosis in poison dart frogs (Dendrobates spp.) and White's tree frogs (Litoria caerulea). J. Vet. Diagn. Invest. 11:194-199.
35. Pounds, J. A., M. R. Bustamante, L. A. Coloma, J. A. Consuegra, M. P. L. Fogden, P. N. Foster, E. La Marca, K. L. Masters, A. Merino-Viteri, R. Puschendorf, R. R. Santiago, G. A. Sanchez-Azofeifa, C. J. Still, and B. E. Young. 2006. Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439:161-167.
36. Rachowicz, L. J., R. A. Knapp, J. A. T. Morgan, M. J. Stice, V. T. Vredenburg, J. M. Parker, and C. J. Briggs. 2006. Emerging infectious disease as a proximate cause of amphibian mass mortality. Ecology 87:1671-1683.
37. Retallick, R. W. R., and V. Miera. 2007. Strain differences in the amphibian chytrid Batrachochytrium dendrobatidis and non-permanent, sublethal effects of infection. Dis. Aquat. Organ 75:201-207.
38. Retallick, R. W., H. McCallum, and R. Speare. 2004. Endemic infection of the amphibian chytrid fungus in the frog community post-decline. PLoS Biology 2(e351):1965-1971.
39. Ribas, L., M.-S. Li, B. J. Doddington, J. Robert, J. A. Seidel, J. S. Kroll, L. B. Zimmerman, N. C. Grassly, T. W. J. Garner, and M. C. Fisher. 2009. Expression profiling the temperature-dependent amphibian response to infection by Batrachochytrium dendrobatidis. PLoS One 4:e8408.
40. Richter, K., R. Egger, and G. Kreil. 1986. Sequence of preprocaerulein cDNAs cloned from skin of Xenopus laevis: a small family of precursors containing one, three, or four copies of the final product. J. Biol. Chem. 261:3676-3680.
41. Robert, J., and Y. Ohta. 2009. Comparative and developmental study of the immune system in Xenopus. Dev. Dyn. 238:1249-1270.
42. Robert, J., C. Guiet, and L. Du Pasquier. 1995. Ontogeny of the alloimmune response against transplanted tumor in Xenopus laevis. Differentiation 59:135-144.
43. Robert, J., H. Morales, W. Buck, N. Cohen, S. Marr, and J. Gantress. 2005. Histopathogenesis and immune responses to FV3 virus infection in Xenopus. Virology 332:667-675.
44. Rollins-Smith, L. A. 2009. The role of amphibian antimicrobial peptides in protection of amphibians from pathogens linked to global amphibian declines. Biochim. Biophys. Acta 1788:1593-1599.
45. Rollins-Smith, L. A., and J. M. Conlon. 2005. Antimicrobial peptide defenses against chytridiomycosis, an emerging infectious disease of amphibian populations. Dev. Comp. Immunol. 29:589-598.
46. Rollins-Smith, L. A., C. Carey, J. Longcore, J. K. Doersam, A. Boutte, J. E. Bruzgal, and J. M. Conlon. 2002. Activity of antimicrobial skin peptides from ranid frogs against Batrachochytrium dendrobatidis, the chytrid fungus associated with global amphibian declines. Dev. Comp. Immunol. 26:471-479.
47. Rollins-Smith, L. A., C. Carey, J. M. Conlon, L. K. Reinert, J. K. Doersam, T. Bergman, J. Silberring, H. Lankinen, and D. Wade. 2003. Activities of temporin family peptides against the chytrid fungus (Batrachochytrium dendrobatidis) associated with global amphibian declines. Antimicrob. Agents Chemother. 47:1157-1160.
48. Rollins-Smith, L. A., D. C. Woodhams, L. K. Reinert, V. T. Vredenburg, C. J. Briggs, P. F. Nielsen, and J. M. Conlon. 2006. Antimicrobial peptide defenses of the mountain yellow-legged frog (Rana muscosa). Dev. Comp. Immunol. 30:831-842.
49. Rollins-Smith, L. A., J. D. King, P. F. Nielsen, A. Sonnevend, and J. M. Conlon. 2005. An antimicrobial peptide from the skin secretions of the mountain chicken frog Leptodactylus fallax (Anura:Leptodactylidae). Regul. Pept. 124:173-178.
50. Rollins-Smith, L. A., J. K. Doersam, J. E. Longcore, S. K. Taylor, J. C. Shamblin, C. Carey, and M. A. Zasloff. 2002. Antimicrobial peptide defenses against pathogens associated with global amphibian declines. Dev. Comp. Immunol. 26:63-72.
51. Rollins-Smith, L. A., L. K. Reinert, C. J. O'Leary, L. E. Houston, and D. C. Woodhams. 2005. Antimicrobial peptide defenses in amphibian skin. Integr. Comp. Biol. 45:137-142.
52. Rollins-Smith, L. A., L. K. Reinert, V. Miera, and J. M. Conlon. 2002. Antimicrobial peptide defenses of the Tarahumara frog, Rana tarahumarae. Biochem. Biophys. Res. Commun. 297:361-367.
53. Rombout, J. H. W. M., N. Taverne, M. van de Kamp, and A. J. Taverne-Thiele. 1993. Differences in mucus and serum immunoglobulins of carp (Cyprinus carpio L.). Dev. Comp. Immunol. 17:309-317.
54. Rosenblum, E. B., T. J. Poorten, M. Settles, G. K. Murdoch, J. Robert, N. Maddox, and M. B. Eisen. 2009. Genome-wide transcriptional response of Silurana (Xenopus) tropicalis to infection with the deadly chytrid fungus. PLoS One 4:e6494.
55. Russ, J. H., and J. D. Horton. 1987. Cytoarchitecture of the Xenopus thymus following gamma-irradiation. Development 100:95-105.
56. Shepherd, S. P., and M. A. Holzwarth. 2001. Chromaffin-adrenocortical cell interactions: effects of chromaffin cell activation in adrenal cell cocultures. Am. J. Physiol. Cell Physiol. 280:61-71.
57. Simmaco, M., G. Mignona, and D. Barra. 1998. Antimicrobial peptides from amphibian skin: what do they tell us? Biopolymers 47:435-450.
58. Sjoberg, E., and A. Flock. 1976. Innervation of skin glands in the frog. Cell Tissue Res. 172:81-91.
59. Stice, M. J., and C. J. Briggs. 2010. Immunization is ineffective at preventing infection and mortality due to the amphibian chytrid fungus Batrachochytrium dendrobatidis. J. Wildl. Dis. 46:70-77.
60. Sures, I., and M. Crippa. 1984. Xenopsin: the neurotensin-like octapeptide from Xenopus skin at the carboxyl terminus of its precursor. Proc. Natl. Acad. Sci. U. S. A. 81:380-384.
61. Tennessen, J. A., D. C. Woodhams, P. Chaurand, L. K. Reinert, D. Billheimer, Y. Shyr, R. M. Caprioli, M. S. Blouin, and L. A. Rollins-Smith. 2009. Variations in the expressed antimicrobial peptide repertoire of northern leopard frog (Rana pipiens) populations suggest intraspecies differences in resistance to pathogens. Dev. Comp. Immunol. 33:1247-1257.
62. Turner, R. J., and M. J. Manning. 1974. Thymic dependence of amphibian antibody responses. Eur. J. Immunol. 4:343-346.
63. Voyles, J., L. Berger, S. Young, R. Speare, R. Webb, J. Warner, D. Rudd, R. Campbell, and L. F. Skerratt. 2007. Electrolyte depletion and osmotic imbalance in amphibians with chytridiomycosis. Dis. Aquat. Organ 77:113-118.
64. Voyles, J., S. Young, L. Berger, C. Campbell, W. F. Voyles, A. Dinudom, D. Cook, R. Webb, R. A. Alford, L. F. Skerratt, and R. Speare. 2009. Pathogenesis of chytridiomycosis, a cause of catastrophic amphibian declines. Science 326:582-585.
65. Weldon, C., L. H. du Preez, A. D. Hyatt, R. Muller, and R. Speare. 2004. Origin of the amphibian chytrid fungus. Emerg. Infect. Dis. 10:2100-2105.
66. Woodhams, D. C., J. Voyles, K. R. Lips, C. Carey, and L. A. Rollins-Smith. 2005. Predicted disease susceptibility in a Panamanian amphibian assemblage based on skin peptide defenses. J. Wildl. Dis. 42:207-218.
67. Woodhams, D. C., K. Ardipradja, R. A. Alford, G. Marantelli, L. K. Reinert, and L. A. Rollins-Smith. 2007. Resistance to chytridiomycosis varies by amphibian species and is correlated with skin peptide defenses. Anim. Conserv. 10:409-417.
68. Woodhams, D. C., L. A. Rollins-Smith, C. Carey, L. Reinert, M. J. Tyler, and R. Alford. 2006. Population trends associated with antimicrobial peptide defenses against chytridiomycosis in Australian frogs. Oecologia 46:531-540.
69. Woodhams, D. C., R. A. Alford, C. J. Briggs, M. Johnson, and L. A. Rollins-Smith. 2008. Life-history trade-offs influence disease in changing climates: strategies of an amphibian pathogen. Ecology 89:1627-1639.
70. Zasloff, M. 1987. Magainins, a class of antimicrobial peptides from Xenopus skin: isolation, characterization of two active forms, and partial cDNA sequence of a precursor. Proc. Natl. Acad. Sci. U. S. A. 84:5449-5453.