Norepinephrine depletion of antimicrobial peptides from the skin glands of Xenopus laevis

Developmental and Comparative Immunology

Volumn 37, Issue 1, 2012, Pages 19-27

  Gammill, Whitney M ^a   Scott Fites, J ^b   Rollins Smith, Louise A ^a,b,c,d  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY   (United States)

^c VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^d SMITHSONIAN INSTITUTION   (United States)

Author keywords

Antimicrobial peptide; Batrachochytrium dendrobatidis; Chytridiomycosis; Granular gland; Mucus gland; Norepinephrine

Indexed keywords

NORADRENALIN; POLYPEPTIDE ANTIBIOTIC AGENT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOCHEMICAL COMPOSITION; CONTROLLED STUDY; GRANULAR GLAND; HISTOLOGY; MASS SPECTROMETRY; MUCUS GLAND; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN SECRETION; SKIN GLAND; XENOPUS LAEVIS;

BATRACHOCHYTRIUM DENDROBATIDIS; FUNGI; XENOPUS LAEVIS;

EID: 84859822642     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2011.12.012     Document Type: Article

References (83)

1. Andreu D., Aschauer H., Kreil G., Merrifield R.B. Solid-phase synthesis of PYLa and isolation of its natural counterpart PGLa [PYLa - (4-24)] from skin secretions of Xenopus laevis. Eur. J. Biochem. 1985, 149:531-535.
2. Andreu D., Rivas L. Animal antimicrobial peptides: an overview. Biopolymers (Pept. Sci.) 1999, 47:415-433.
3. Apponyi M.A., Pukala T.L., Brinkworth C.S., Maselli V.M., Bowie J.H., Tyler M.J., Booker G.W., Wallace J.C., Carver J.A., Separovic F., Doyle J., Llewellyn L.E. Host-defence peptides of Australian anurans: structure, mechanism of action and evolutionary significance. Peptides 2004, 25:1035-1054.
4. Barbeau T.R., Lillywhite H.B. Body wiping behaviors associated with cutaneous lipids in hylid tree frogs of Florida. J. Exp. Biol. 2005, 208:2147-2156.
5. Becker C.G., Fonseca C.R., Haddad C.F., Batista R.F., Prado P.I. Habitat split and the global decline of amphibians. Science 2007, 318:1775-1777.
6. Benson B.J., Hadley M.E. In vitro characterization of adrenergic receptors controlling skin gland secretion in two anurans Rana pipiens and Xenopus laevis. Comp. Biochem. Physiol. 1969, 30:857-864.
7. Berger L., Hyatt A.D., Speare R., Longcore J.E. Life cycle stages of the amphibian chytrid Batrachochytrium dendrobatidis. Dis. Aquat. Organ. 2005, 68:51-63.
8. Berger L., Speare R., Daszak P., Green D.E., Cunningham A.A., Goggin C.L., Slocombe R., Ragan M.A., Hyatt A.D., McDonald K.R., Hines H.B., Lips K.R., Marantelli G., Parkes H. Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proc. Natl. Acad. Sci. USA 1998, 95:9031-9036.
9. Blaustein A.R., Romansic J.M., Kiesecker J.M., Hatch A.C. Ultraviolet radiation, toxic chemicals and amphibian population declines. Divers. Distrib. 2003, 9:123-140.
10. Bosch J., Martínez-Solano I., García-París M. Evidence of a chytrid fungus infection involved in the decline of the common midwife toad (Alytes obstetricans) in protected areas of central Spain. Biol. Conserv. 2001, 97:331-337.
11. Bradley G.A., Rosen P.C., Sredl M.J., Jones T.R., Longcore J.E. Chytridiomycosis in native Arizona frogs. J. Wildl. Dis. 2002, 38:206-212.
12. Briggs C.J., Vredenburg V.T., Knapp R.A., Rachowicz L.J. Investigating the population-level effects of chytridiomycosis: an emerging infectious disease of amphibians. Ecology 2005, 86:3149-3159.
13. Brucker R.M., Harris R.N., Schwantes C.R., Gallaher T.N., Flaherty D.C., Lam B.A., Minbiole K.P. Amphibian chemical defense: antifungal metabolites of the microsymbiont Janthinobacterium lividum on the salamander Plethodon cinereus. J. Chem. Ecol. 2008, 34:1422-1429.
14. Carey C., Alexander M.A. Climate change and amphibian declines: is there a link?. Divers. Distrib. 2003, 9:111-121.
15. Collins J.P. Amphibian decline and extinction: what we know and what we need to learn. Dis. Aquat. Organ. 2010, 92:93-99.
16. Collins J.P., Storfer A. Global amphibian declines: sorting the hypotheses. Divers. Distrib. 2003, 9:89-98.
17. Conlon J.M. The contribution of skin antimicrobial peptides to the system of innate immunity in anurans. Cell Tissue Res. 2011, 343:201-212.
18. Cushman S.A. Effects of habitat loss and fragmentation on amphibians: a review and prospectus. Biol. Conserv. 2006, 128:231-240.
19. Davidson C., Benard M.F., Shaffer H.B., Parker J.M., O'Leary C., Conlon J.M., Rollins-Smith L.A. Effects of chytrid and carbaryl exposure on survival, growth and skin peptide defenses in foothill yellow-legged frogs. Environ. Sci. Technol. 2007, 41:1771-1776.
20. Dockray G.J., Hopkins C.R. Caerulein secretion by dermal glands in Xenopus laevis. J. Cell Biol. 1975, 64:724-733.
21. Dunn A.J. Systemic interleukin-1 administration stimulates hypothalamic norepinephrine metabolism parallelling the increased plasma corticosterone. Life Sci. 1988, 43:429-435.
22. Feldman S., Weidenfeld J. Norepinephrine depletion in the amygdale inhibits CRF-41, ACTH, and corticosterone responses following photic simulation. Brain Res. Bull. 1996, 41:83-86.
23. Fox H. The structure of the integument. Amphibian Biology: The Integument. Chipping Norton 1994, vol. 1:1-92. Surrey Beatty & Sons, NSW.
24. Gibson B.W., Poulter L., Williams D.H., Maggio J.E. Novel peptide fragments originating from PGLa and the caerulein and xenopsin precursors from Xenopus laevis. J. Biol. Chem. 1986, 261:5341-5349.
25. Goraya J., Knoop F.C., Conlon J.M. Ranatuerins: antimicrobial peptides isolated from the skin of the American bullfrog, Rana catesbeiana. Biochem. Biophys. Res. Commun. 1998, 250:589-592.
26. Goraya J., Wang Y., Li Z., O'Flaherty M., Knoop F.C., Platz J.E., Conlon J.M. 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. 2000, 267:894-900.
27. Harris R.N., Brucker R.M., Walke J.B., Becker M.H., Schwantes C.R., Flaherty D.C., Lam B.A., Woodhams D.C., Briggs C.J., Vredenburg V.T., Minbiole K.P. Skin microbes on frogs prevent morbidity and mortality caused by a lethal skin fungus. ISME J. 2009, 3:818-824.
28. James S., Gibbs B.F., Toney K., Bennett H.P.J. 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. 1994, 217:84-90.
29. Johnson P.T., McKenzie V.J., Peterson A.C., Kerby J.L., Brown J., Blaustein A.R., Jackson T. Regional decline of an iconic amphibian associated with elevation, land-use change, and invasive species. Conserv. Biol. 2011, 25:558-566.
30. La Marca E., Lips K.R., Lötters S., Puschendorf R., Ibáñez R., Rueda-Almonacid J.V., Schulte R., Marty C., Castro F., Manzanilla-Puppo J., García-Pérez J.E., Bolaños F., Chaves G., Pounds J.A., Toral E., Young B.E. Catastrophic population declines and extinctions in neotropical harlequin frogs (Bufonidae: Atelopus). Biotropica 2005, 37:190-201.
31. Leibowitz S.F., Diaz S., Tempel D. Norepinephrine in the paraventricular nucleus stimulates corticosterone release. Brain Res. 1989, 496:219-227.
32. Lepri J.J., Randall J.A. Hormonal regulation of sandbathing in male kangaroo rats (Dipodomys merriami). Behav. Neural Biol. 1983, 37:256-264.
33. Lips K.R., Brem F., Brenes R., Reeve J.D., Alford R.A., Voyles J., Carey C., Livo L., Pessier A.P., Collins J.P. Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proc. Natl. Acad. Sci. USA. 2006, 103:3165-3170.
34. Lips K.R., Diffendorfer J., Mendelson J.R., Sears M.W. Riding the wave: reconciling the roles of disease and climate change in amphibian declines. PLoS Biol. 2008, 6(3):e72.
35. Longcore J.E., Pessier A.P., Nichols D.K. Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia 1999, 91:219-227.
36. Marcum R.D., St. Hilaire S., Murphy P.J., Rodnick K.J. Effects of Batrachochytrium dendrobatidis infection on ion concentrations in the boreal toad Anaxyrus (Bufo) boreas boreas. Dis. Aquat. Organ. 2010, 91:17-21.
37. MbangKollo D., deRoos R. Comparative effects of epinephrine, norepinephrine, and a gentle handling stress on plasma lactate, glucose, and hematocrit levels in the American bullfrog (Rana catesbeiana). Gen. Comp. Endocrinol. 1983, 49:167-175.
38. McClanahan L., Baldwin R. Rate of water uptake through the integument of the desert toad, Bufo punctatus. Comp. Biochem. Physiol. 1969, 28:381-389.
39. McReynolds J.R., Donowho K., Abdi A., McGaugh J.L., Roozendaal B., McIntyre C.K. Memory-enhancing corticosterone treatment increases amygdala norepinephrine and Arc protein expression in hippocampal synaptic fractions. Neurobiol. Learn. Mem. 2010, 93:312-321.
40. Moy R.F. Histology of the subauricular and rump glands of the pronghorn (Antilocapra americana Ord). Am. J. Anat. 1970, 129:65-87.
41. Murphy P.J., St. Hilaire S., Bruer S., Corn P.S., Peterson C.R. Distribution and pathogenicity of Batrachochytrium dendrobatidis in boreal toads from the Grand Teton area of western Wyoming. Ecohealth 2009, 6:109-120.
42. Mutschmann F., Berger L., Zwart P., Gaedicke C. Chytridiomycosis in amphibians - first report in Europe. Berl. Munch. Tieraerztl Wochenschr. 2000, 113:380-383.
43. Nicolas P., Mor A. Peptides as weapons against microorganisms in the chemical defense system of vertebrates. Annu. Rev. Microbiol. 1995, 49:277-304.
44. Nutkins J.C., Williams D.H. Identification of highly acidic peptides from processing of the skin prepropeptides of Xenopus laevis. Eur. J. Biochem. 1989, 181:97-102.
45. Parker J.M., Mikaelian I., Hahn N., Diggs H.E. Clinical diagnosis and treatment of epidermal chytridiomycosis in African clawed frogs (Xenopus tropicalis). Comp. Med. 2002, 52:265-268.
46. Pennisi E. Life and death play out on the skin of frogs. Science 2009, 326:507-508.
47. Pessier A.P., Nichols D.K., Longcore J.E., Fuller M.S. Cutaneous chytridiomycosis in poison dart frogs (Dendrobates spp.) and White's tree frogs (Litoria caerulea). J. Vet. Diagn. Invest. 1999, 11:194-199.
48. Peterson J.D., Wood M.B., Hopkins W.A., Unrine J.M., Mendonça M.T. Prevalence of Batrachochytrium dendrobatidis in American bullfrog and southern leopard frog larvae from wetlands on the Savannah River Site, South Carolina. J. Wildl. Dis. 2007, 43:450-460.
49. Pounds J.A., Bustamante M.R., Coloma L.A., Consuegra J.A., Fogden M.P., Foster P.N., La Marca E., Masters K.L., Merino-Viteri A., Puschendorf R., Ron S.R., Sánchez-Azofeifa G.A., Still C.J., Young B.E. Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 2006, 439:161-167.
50. Ramakrishnan L., Valdivia R.H., McKerrow J.H., Falkow S. Mycobacterium marinum causes both a long-term subclinical infection and acute disease in the leopard frog (Rana pipiens). Infect. Immun. 1997, 65:767-773.
51. Ramsey J.P., Reinert L.K., Harper L.K., Woodhams D.C., Rollins-Smith L.A. Immune defenses against Batrachochytrium dendrobatidis, a fungus linked to global amphibian declines, in the South African clawed frog, Xenopus laevis. Infect. Immun. 2010, 78:3981-3992.
52. Resnick N.M., Maloy W.L., Guy H.R., Zasloff M. A novel endopeptidase from Xenopus that recognizes α-helical secondary structure. Cell 1991, 66:541-554.
53. Retallick R.W., McCallum H., Speare R. Endemic infection of the amphibian chytrid fungus in a frog community post-decline. PLoS Biol. 2004, 2:e351.
54. Rinaldi A.C. Antimicrobial peptides from amphibian skin: an expanding scenario. Curr. Opin. Chem. Biol. 2002, 6:799-804.
55. Rollins L.A., McKinnell R.G. The influence of glucocorticoids on survival and growth of allografted tumors in the anterior eye chamber of leopard frogs. Dev. Comp. Immunol. 1980, 4:283-294.
56. Rollins-Smith L.A. Neuroendocrine-immune system interactions in amphibians: implications for understanding global amphibian declines. Immunol. Res. 2001, 23(2-3):273-280.
57. Rollins-Smith L.A. The role of amphibian antimicrobial peptides in protection of amphibians from pathogens linked to global amphibian declines. Biochim. Biophys. Acta 2009, 1788:1593-1599.
58. Rollins-Smith L.A., Conlon J.M. Antimicrobial peptide defenses against chytridiomycosis, an emerging infectious disease of amphibian populations. Dev. Comp. Immunol. 2005, 29:589-598.
59. Rollins-Smith L.A., Ramsey J.P., Pask J.D., Reinert L.K., Woodhams D.C. Amphibian immune defenses against chytridiomycosis: impacts of changing environments. Integr. Comp. Biol. 2011, 51:552-562.
60. Rollins-Smith L.A., Reinert L.K., Miera V., Conlon J.M. Antimicrobial peptide defenses of the Tarahumara frog, Rana tarahumarae. Biochem. Biophys. Res. Commun. 2002, 297:361-367.
61. Rollins-Smith L.A., Reinert L.K., O'Leary C.J., Houston L.E., Woodhams D.C. Antimicrobial peptide defenses in amphibian skin. Integr. Comp. Biol. 2005, 45:137-142.
62. Rollins-Smith L.A., Woodhams D.C., Reinert L.K., Vredenburg V.T., Briggs C.J., Nielsen P.F., Conlon J.M. Antimicrobial peptide defenses of the mountain yellow-legged frog (Rana muscosa). Dev. Comp. Immunol. 2006, 30:831-842.
63. Schloegel L., Hero J.-M., Berger L., Speare R., McDonald K., Daszak P. The decline of the sharp-snouted day frog (Taudactylus acutirostris): the first documented case of extinction by infection in a free-ranging wildlife species?. Ecohealth 2006, 3:35-40.
64. Schumacher U., Adam E., Hauser F., Probst J.C., Hoffmann W. Molecular anatomy of a skin gland: histochemical and biochemical investigations on the mucous glands of Xenopus laevis. J. Histochem. Cytochem. 1994, 42:57-65.
65. Simmaco M., Boman A., Mangoni M.L., Mignogna G., Miele R., Barra D., Boman H.G. Effect of glucocorticoids on the synthesis of antimicrobial peptides in amphibian skin. FEBS Lett. 1997, 416:273-275.
66. Simmaco M., Mignogna G., Barra D. Antimicrobial peptides from amphibian skin: what do they tell us?. Biopolymers 1998, 47:435-450.
67. Sjöberg E., Flock A. Innervation of skin glands in the frog. Cell Tissue Res. 1976, 172:81-91.
68. Smith P.K., Krohn R.I., Hermanson G.T., Mallia A.K., Gartner F.H., Provenzano M.D., Fujimoto E.K., Goeke N.M., Olson B.J., Klenk D.C. Measurement of protein using bicinchoninic acid. Anal. Biochem. 1985, 150:76-85.
69. Sparling D.W., Fellers G.M., McConnell L.L. Pesticides and amphibian population declines in California, USA. Environ. Toxicol. Chem. 2001, 20:1591-1595.
70. Stebbins R.C., Cohen N.W. A Natural History of Amphibians 1997, Princeton University Press, New Jersey, West Sussex.
71. Steinborner S.T., Waugh R.J., Bowie J.H., Wallace J.C., Tyler M.J., Ramsay S.L. New caerin antibacterial peptides from the skin glands of the Australian tree frog Litoria xanthomera. J. Pept. Sci. 1997, 3:181-185.
72. Sun Z., Fan Y., Zha Q., Zhu M.Y. Corticosterone up-regulates expression and function of norepinephrine transporter in SK-N-BE(2)C cells. J. Neurochem. 2010, 113:105-116.
73. Sures I., Crippa M. Xenopsin: the neurotensin-like octapeptide from Xenopus skin at the carboxyl terminus of its precursor. Proc. Natl. Acad. Sci. USA 1984, 81:380-384.
74. Tennessen J.A., Woodhams D.C., Chaurand P., Reinert L.K., Billheimer D., Shyr Y., Caprioli R.M., Blouin M.S., Rollins-Smith L.A. Variations in the expressed antimicrobial peptide repertoire of northern leopard frog (Rana pipiens) populations suggest intraspecies differences in resistance to pathogens. Dev. Comp. Immunol. 2009, 331:1247-1257.
75. Toledo R.C., Jared C. Cutaneous granular glands and amphibian venoms. Comp. Biochem. Physiol. 1995, 111A:1-29.
76. Weldon C., du Preez L.H., Hyatt A.D., Muller R., Speare R. Origin of the amphibian chytrid fungus. Emerg. Infect. Dis. 2004, 10:2100-2105.
77. Woodhams D.C., Ardipradja K., Alford R.A., Marantelli G., Reinert L.K., Rollins-Smith L.A. Resistance to chytridiomycosis varies by amphibian species and is correlated with skin peptide defenses. Anim. Conserv. 2007, 10:409-417.
78. Woodhams D.C., Rollins-Smith L.A., Carey C., Reinert L., Tyler M.J., Alford R.A. Population trends associated with skin peptide defenses against chytridiomycosis in Australian frogs. Oecologia 2006, 146:531-540.
79. Woodhams D.C., Voyles J., Lips K.R., Carey C., Rollins-Smith L.A. Predicted disease susceptibility in a Panamanian amphibian assemblage based on skin peptide defenses. J. Wildl. Dis. 2006, 42:207-218.
80. Voyles J., Berger L., Young S., Speare R., Webb R., Warner J., Rudd D., Campbell R., Skerratt L.F. Electrolyte depletion and osmotic imbalance in amphibians with chytridiomycosis. Dis. Aquat. Organ. 2007, 77:113-118.
81. Voyles J., Young S., Berger L., Campbell C., Voyles W.F., Dinudom A., Cook D., Webb R., Alford R.A., Skerratt L.F., Speare R. Pathogenesis of chytridiomycosis, a cause of catastrophic amphibian declines. Science 2009, 26:582-585.
82. Vredenburg V.T. Reversing introduced species effects: experimental removal of introduced fish leads to rapid recovery of a declining frog. Proc. Natl. Acad. Sci. USA 2004, 101:7646-7650.
83. Zasloff M. 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. USA 1987, 84:5443-5449.