Variations in the expressed antimicrobial peptide repertoire of northern leopard frog (Rana pipiens) populations suggest intraspecies differences in resistance to pathogens

Developmental and Comparative Immunology

Volumn 33, Issue 12, 2009, Pages 1247-1257

  Tennessen, Jacob A ^a   Woodhams, Douglas C ^b   Chaurand, Pierre ^b   Reinert, Laura K ^b   Billheimer, Dean ^b   Shyr, Yu ^b   Caprioli, Richard M ^b   Blouin, Michael S ^a   Rollins Smith, Louise A ^b,c  

^a OREGON STATE UNIVERSITY   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Aeromonas hydrophila; Antimicrobial peptides; Batrachochytrium dendrobatidis; Brevinin 1; Lithobates; Mass spectrometry; Peptidomics; Rana palustris; Rana pipiens; Ranatuerin 2; Staphylococcus epidermidis; Temporin

Indexed keywords

AMPHIBIAN PROTEIN; BREVININ 1PG; BREVININ 1PL; POLYPEPTIDE ANTIBIOTIC AGENT; RANATUERIN 2PB; RANATUERIN 2PC; UNCLASSIFIED DRUG;

AEROMONAS HYDROPHILA; ALLELE; ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL GROWTH; CONTROLLED STUDY; FROG; GENE LOCUS; GEOGRAPHIC DISTRIBUTION; GROWTH INHIBITION; MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; PEPTIDOMICS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; SKIN SECRETION; SPECIES DIFFERENCE; STAPHYLOCOCCUS EPIDERMIDIS;

AEROMONAS HYDROPHILA; AMPHIBIA; ANURA; BACTERIA (MICROORGANISMS); BATRACHOCHYTRIUM DENDROBATIDIS; LITHOBATES; RANA PALUSTRIS; RANA PIPIENS; STAPHYLOCOCCUS EPIDERMIDIS;

EID: 69949085718     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2009.07.004     Document Type: Article

References (72)

1. Blaustein A.R., and Wake D.B. Declining amphibian populations-a global phenomenon. Trends Ecol Evol 5 (1990) 203-204
2. Alford R.A., and Richards S.J. Global amphibian declines: a problem in applied ecology. Annu Rev Ecol Syst 30 (1999) 133-165
3. Houlahan J.E., Findlay C.S., Schmidt B.R., Meyer A.H., and Kuzmin S.L. Quantitative evidence for global amphibian population declines. Nature 404 (2000) 752-755
4. Collins J.P., and Storfer A. Global amphibian declines: sorting the hypotheses. Divers Distrib 9 (2003) 89-98
5. Stuart S.N., Chanson J.S., Cox N.A., Young B.E., Rodrigues A.S., Fischman D.L., et al. Status and trends of amphibian declines and extinctions worldwide. Science 306 (2004) 1783-1786
6. Carey C., Cohen N., and Rollins-Smith L. Amphibian declines: an immunological perspective. Dev Comp Immunol 23 (1999) 459-472
7. Daszak P., Berger L., Cunningham A.A., Hyatt A.D., Green D.E., and Spear R. Emerging infectious diseases and amphibian population declines. Emerg Infect Dis 5 (1999) 735-748
8. Daszak P., Cunningham A.A., and Hyatt A.D. Infectious disease and amphibian population declines. Divers Distrib 9 (2003) 141-150
9. Storfer A. Amphibian declines: future directions. Divers Distrib 9 (2003) 151-163
10. Hillis D.M. Systematics of the Rana pipiens complex: puzzle and paradigm. Annu Rev Ecol Syst 19 (1988) 39-63
11. Frost D.R., Grant T., Faivovich J., Bain R.H., Haas A., Haddad C.F.B., et al. The amphibian tree of life. Bull Am Mus Nat Hist 297 (2006) 1-370
12. Hillis D.M. Constraints in naming parts of the tree of life. Mol Phylogenet Evol 42 (2007) 331-338
13. Gibbs E.L., Nance G.W., and Emmons M.B. The live frog is almost dead. Bioscience 21 (1971) 1027-1034
14. Roberts W.E. What happened to the leopard frogs?. Alberta Nat 11 (1981) 1-4
15. Corn P.S., and Fogelman J.C. Extinctions of montane populations of the northern leopard frog (Rana pipiens) in Colorado. J Herpetol 18 (1984) 147-152
16. Green D.E., Converse K.A., and Schrader A.K. Epizootiology of sixty-four amphibian mortality and morbidity events in the USA, 1996-2001. Ann NY Acad Sci 969 (2002) 323-339
17. Greer A.L., Berrill M., and Wilson P.J. Five amphibian mortality events associated with ranavirus infection in south central Ontario, Canada. Dis Aquat Organ 67 (2005) 9-14
18. Rorabaugh J.C. Rana pipiens Schreber, 1782. In: Lannoo M.J. (Ed). Amphibian declines: the conservation status of United States species (2005), University of California Press, Berkeley, CA 570-577
19. Redmer M. Rana palustris, LeConte, 1825. In: Lannoo M.J. (Ed). Amphibian declines: the conservation of United States species (2005), University of California Press, Berkeley, CA 568-570
20. Nicolas P., and Mor A. Peptides as weapons against microorganisms in the chemical defense system of vertebrates. Annu Rev Microbiol 49 (1995) 277-304
21. Simmaco M., Mignogna G., and Barra D. Antimicrobial peptides from amphibian skin: what do they tell us?. Biopolymers (Peptide Science) 47 (1998) 435-450
22. Hancock R.E.W. Cationic peptides: effectors in innate immunity and novel antimicrobials. Lancet Infect Dis 1 (2001) 156-164
23. Zasloff M. Antimicrobial peptides of multicellular organisms. Nature 415 (2002) 389-395
24. Rinaldi A.C. Antimicrobial peptides from amphibian skin: an expanding scenario. Curr Opin Chem Biol 6 (2002) 799-804
25. Conlon J.M., Kolodziejek J., and Nowotny N. Antimicrobial peptides from ranid frogs: taxonomic and phylogenetic markers and a potential source of new therapeutic agents. Biochim Biophys Acta 1696 (2004) 1-14
26. Apponyi M.A., Pukala T.L., Brinkworth C.S., Vaselli V.M., Bowie J.H., Tyler M.J., et al. Host-defence peptides of Australian anurans: structure, mechanisms of action and evolutionary significance. Peptides 25 (2004) 1035-1054
27. Rollins-Smith L.A., Doersam J.K., Longcore J.E., Taylor S.K., Shamblin J.C., Carey C., et al. Antimicrobial peptide defenses against pathogens associated with global amphibian declines. Dev Comp Immunol 26 (2002) 63-72
28. Rollins-Smith L.A., Carey C., Longcore J., Doersam J.K., Boutte A., Bruzgal J.E., et al. Activity of antimicrobial skin peptides from ranid frogs against Batrachochytrium dendrobatidis, the chytrid fungus associated with global amphibian declines. Dev Comp Immunol 26 (2002) 471-479
29. Rollins-Smith L.A., Reinert L.K., Miera V., and Conlon J.M. Antimicrobial peptide defenses of the Tarahumara frog, Rana tarahumarae. Biochem Biophys Res Commun 297 (2002) 361-367
30. Woodhams D.C., Rollins-Smith L.A., Carey C., Reinert L., Tyler M.J., and Alford R. Population trends associated with antimicrobial peptide defenses against chytridiomycosis in Australian frogs. Oecologia 146 (2006) 531-540
31. Woodhams D.C., Voyles J., Lips K.R., Carey C., and Rollins-Smith L.A. Predicted disease susceptibility in a Panamanian amphibian assemblage based on skin peptide defenses. J Wildl Dis 42 (2006) 207-218
32. Rollins-Smith L.A., and Conlon J.M. Antimicrobial peptide defenses against chytridiomycosis, an emerging infectious disease of amphibian populations. Dev Comp Immunol 29 (2005) 589-598
33. Rollins-Smith L.A., Reinert L.K., O'Leary C.J., Houston L.E., and Woodhams D.C. Antimicrobial peptide defenses in amphibian skin. Integr Comp Biol 45 (2005) 137-142
34. Rollins-Smith L.A. The role of amphibian antimicrobial peptides in protection of amphibians from pathogens linked to global amphibian declines. Biochim Biophys Acta 8 (2009) 1593-1599
35. Horikawa R., Parker D.S., Herring P.L., and Pisano J.J. Pipinins: new mast cell degranulating peptides from Rana pipiens. Fed Proc 44 (1985) 695
36. Goraya J., Wang Y., Li Z., O'Flaherty M., Knoop F.C., Platz J.E., et al. Peptides with antimicrobial activity from four different families isolated from the skins of the North American frogs, Rana luteiventris, Rana berlandieri and Rana pipiens. Eur J Biochem 267 (2000) 894-900
37. Chen T., Farragher S., Bjourson A.J., Orr D.F., Rao P., and Shaw C. Granular gland transcriptomes in stimulated amphibian skin secretions. Biochem J 371 (2003) 125-130
38. Basir Y.J., Knoop F.C., Dulka J., and Conlon J.M. Multiple antimicrobial peptides and peptides related to bradykinin and neuromedin N isolated from skin secretions of the pickerel frog, Rana palustris. Biochim Biophys Acta 1543 (2000) 95-105
39. Tennessen J.A., and Blouin M.S. Balancing selection at a frog antimicrobial peptide locus: fluctuating immune effector alleles?. Mol Biol Evol 25 (2008) 2669-2680
40. Tennessen J.A., and Blouin M.S. Selection for antimicrobial peptide diversity in frogs leads to gene duplication and low allelic variation. J Mol Evol 65 (2007) 605-615
41. Zhou M., Wang L., Owens D.E., Chen T., Walker B., and Shaw C. Rapid identification of precursor cDNAs encoding five structural classes of antimicrobial peptides from pickerel frog (Rana palustris) skin secretion by single step "shotgun" cloning. Peptides 28 (2007) 1605-1610
42. Rollins-Smith L.A., Carey C., Conlon J.M., Reinert L.K., Doersam J.K., Bergman T., et al. Activities of temporin family peptides against the chytrid fungus (Batrachochytrium dendrobatidis) associated with global amphibian declines. Antimicrob Agents Chemother 47 (2003) 1157-1160
43. Rollins-Smith L.A., Woodhams D.C., Reinert L.K., Vredenburg V.T., Briggs C.J., Nielsen P.F., et al. Antimicrobial peptide defenses of the mountain yellow-legged frog (Rana muscosa). Dev Comp Immunol 30 (2006) 831-842
44. Davidson C., Benard M.F., Shaffer H.B., Parker J., O'Leary C., Conlon J.M., et al. Effects of chytrid and carbaryl exposure on survival, growth, and skin peptide defenses in foothill yellow-legged frogs. Environ Sci Technol 41 (2007) 1771-1776
45. Austin R.M. Cutaneous microbial flora and antibiosis in Plethodon ventralis. In: Bruce R.C., Jaeger R.G., and Houck L.D. (Eds). The biology of plethodontid salamanders (2000), Kluwer Academic/Plenum Press, New York 127-136
46. Harris R.N., James T.Y., Lauer A., Simon M.A., and Patel A. Amphibian pathogen Batrachochytrium dendrobatidis is inhibited by the cutaneous bacteria of amphibian species. Ecohealth 3 (2006) 53-56
47. Lauer A., Simon M.A., Banning J.L., André E., Dungan K., and Harris R.N. Common cutaneous bacteria from the Eastern red-backed salamander can inhibit pathogenic fungi. Copeia 3 (2007) 630-640
48. Woodhams D.C., Vredenburg V.T., Simon M.-A., Billheimer D., Shakhtour B., Shyr Y., et al. Symbiotic bacteria contribute to innate immune defenses of the threatened mountain yellow-legged frog, Rana muscosa. Biol Conserv 138 (2007) 390-398
49. Lauer A., Simon M.A., Banning J.L., Lam B.A., and Harris R.N. Diversity of cutaneous bacteria with antifungal activity isolated from female four-toed salamanders. ISME J 2 (2008) 145-157
50. Harris R.N., Brucker R.M., Walke J.B., Becker M.H., Schwantes C.R., Flaherty D.C., et al. Skin microbes on frogs prevent morbidity and mortality caused by a lethal skin fungus. ISME J 3 (2009) 818-824
51. Berger L., Speare R., Daszak P., Green D.E., Cunningham A.A., Goggin C.L., et al. Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proc Natl Acad Sci USA 95 (1998) 9031-9036
52. Longcore J.E., Pessier A.P., and Nichols D.K. Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia 91 (1999) 219-227
53. Pessier A.P., Nichols D.K., Longcore J.E., and Fuller M.S. Cutaneous chytridiomycosis in poison dart frogs (Dendrobates spp.) and White's tree frogs (Litoria caerulea). J Vet Diagn Invest 11 (1999) 194-199
54. Berger L., Hyatt A.D., Speare R., and Longcore J.E. Life cycle stages of the amphibian chytrid Batrachochytrium dendrobatidis. Dis Aquat Org 68 (2005) 51-63
55. Woodhams D.C., Ardipradja K., Alford R.A., Marantelli G., Reinert L.K., and Rollins-Smith L.A. Resistance to chytridiomycosis varies among amphibian species and is correlated with skin peptide defenses. Anim Conserv 10 (2007) 409-417
56. Woodhams D.C., Boyle D.G., Hyatt A.D., and Rollins-Smith L.A. The northern leopard frog Rana pipiens is a widespread reservoir species harboring Batrachochytrium dendrobatidis in North America. Herpetol Rev 39 (2008) 66-68
57. Rigney M.M., Zilinsky J.W., and Rouf M.A. Pathogenicity of Aeromonas hydrophila in red leg disease in frogs. Curr Microbiol 1 (1978) 175-179
58. Taylor S.K., Green D.E., Wright K.M., and Whitaker B.M. Bacterial diseases. In: Wright K.M., and Whitaker B.R. (Eds). Amphibian medicine and captive husbandry (2001), Krieger Publishing, Malabar, FL 159-179
59. Lee D.S., and Franz L.R. Red leg in a subterranean population of pickerel frogs. Bull Maryland Herp Soc 9 (1973) 111
60. Hird D.W., Diesch S.L., McKinnell R.G., Gorham E., Martin F.B., Meadows C.A., et al. Enterobacteriaceae and Aeromanas hydrophila in Minnesota frogs and tadpoles (Rana pipiens). Appl Environ Microbiol 46 (1983) 1423-1425
61. Hubbard G.B. Aeromonas hydrophila infection in Xenopus laevis. Lab Anim Sci 31 (1981) 297-300
62. Carr A.A., Amborski R.L., Culley D.D., and Amborski G.F. Aerobic bacteria in the intestinal tracts of bullfrogs (Rana catesbeiana) maintained at low temperatures. Herpetologia 32 (1976) 239-244
63. Gibbs E.L., Gibbs T.J., and Van Dyck P.C. Rana pipiens: health and disease. Lab Anim Care 16 (1966) 142-160
64. Culp C.E., Falkinham III J.O., and Belden L.K. Identification of the natural bacterial microflora on the skin of eastern newts, bullfrog tadpoles, and redback salamanders. Herpetologica 63 (2007) 66-71
65. Ramsay J.O., and Silverman B.W. Functional data analysis (1997), Springer, New York
66. Fukuyama Y., Iwamoto S., and Tanaka K. Rapid sequencing and disulfide mapping of peptides containing disulfide bonds by using 1,5-diaminonaphthalene as a reductive matrix. J Mass Spectrom 41 (2006) 191-201
67. Simmaco M., Boman A., Mangoni M.L., Mignogna G., Miele R., Barra D., et al. Effect of glucocorticoids on the synthesis of antimicrobial peptides in amphibian skin. FEBS Lett 416 (1997) 273-275
68. Ohnuma A., Conlon J.M., Kawasaki H., and Iwamuro S. Developmental and triiodothyronine-induced expression of genes encoding preprotemporins in the skin of Tago's brown frog Rana tagoi. Gen Comp Endocrinol 146 (2006) 242-250
69. Longcore J.R., Longcore J.E., Pessier A.P., and Halteman W.A. Chytridiomycosis widespread in anurans of Northeastern United States. J Wildl Manage 71 (2007) 435-444
70. Brucker R.M., Baylor C.M., Walters R.L., Lauer A., Harris R.N., and Minbiole K.P.C. The identification of 2,4-diacetylphloroglucinol as an antifungal metabolite produced by cutaneous bacteria of the salamander Plethodon cinereus. J Chem Ecol 34 (2008) 39-43
71. Brucker R.M., Harris R.N., Schwantes C.R., Gallaher T.N., Glaherty D.C., Lam B.A., et al. Amphibian chemical defense: antifungal metabolites of the microsymbiont Janthinobacterium lividum on the salamander Plethodon cinereus. J Chem Ecol 34 (2008) 1422-1429
72. Conlon J.M., Kolodziejek J., and Nowotny N. Antimicrobial peptides from the skins of North American frogs. Biochim Biophys Acta 8 (2009) 1556-1563