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Immunogenetics

, Volume 57, Issue 7, pp 487–498 | Cite as

Evolution of caprine and ovine β-defensin genes

  • Katja LuenserEmail author
  • Jörns Fickel
  • Arne Ludwig
Original Paper

Abstract

Defensins comprise an important family of anti-microbial peptides. Among vertebrates, numerous defensin genes have been detected, but their evolutionary background is still discussed. We investigated the molecular evolution and variability of β-defensins of Caprini via sequence analyses of defensin introns. Screening of several domestic and wild species of Caprini revealed a total of 13 discrete β-defensin coding sequences, with three of them described before this study. Phylogenetic analyses revealed that the array of newly described defensin genes is of monophyletic origin and has arisen in numerous independent duplication events after separation of the ancestral defensins. As a result of that scenario, recent defensin genes are distributed in a species-specific manner. Values of synonymous and non-synonymous substitutions demonstrated that both modes of evolutionary pressure, positive as well as negative selection, have acted. In addition, conservation of some β-defensin exons is demonstrated. Discrimination of certain β-defensin genes was possible only due to intron-specific differences. Therefore, sequence analyses restricted to the exons would result in underestimation of the number of β-defensin genes. Our study shows that for reconstruction of the phylogenetic history data of defensin introns are more appropriated. Comparisons among the amino acid sequences show moderate substitutions without changing the net charge of the mature peptides.

Keywords

Immune defence Innate immunity Molecular evolution Capra Ovis 

Notes

Acknowledgements

We thank A.K. Hett and C. Pitra for helpful comments and discussions. Furthermore, the authors recognise the following veterinarians and biologists: M. Stöck, A. Pauly, G. Straub and G. Wibbelt, for providing samples and information on the health status of feral sheep.

Supplementary material

251_2005_1_Fig6a_ESM.gif (15 kb)

Luenser et al. 2005; Evolution of caprine and ovine β-defensin genes Multiple sequence alignment of complete caprine and ovine defensin genes. Vertical numbers indicate nucleotide positions. Dots indicate identical sites referring to sbd2, and dashes indicate gaps introduced by the alignment. Nucleotides of exon1 (1–57) and 2 (1564–1621) are in bold letters. Sequences solely differing in intron regions are subsequently termed as intron variants of that gene (e.g. sbd2_1/I1, sbd2_1/I2 etc.)

251_2005_1_Fig6b_ESM.gif (14 kb)

Luenser et al. 2005; Evolution of caprine and ovine β-defensin genes Multiple sequence alignment of complete caprine and ovine defensin genes. Vertical numbers indicate nucleotide positions. Dots indicate identical sites referring to sbd2, and dashes indicate gaps introduced by the alignment. Nucleotides of exon1 (1–57) and 2 (1564–1621) are in bold letters. Sequences solely differing in intron regions are subsequently termed as intron variants of that gene (e.g. sbd2_1/I1, sbd2_1/I2 etc.)

251_2005_1_Fig6c_ESM.gif (13 kb)

Luenser et al. 2005; Evolution of caprine and ovine β-defensin genes Multiple sequence alignment of complete caprine and ovine defensin genes. Vertical numbers indicate nucleotide positions. Dots indicate identical sites referring to sbd2, and dashes indicate gaps introduced by the alignment. Nucleotides of exon1 (1–57) and 2 (1564–1621) are in bold letters. Sequences solely differing in intron regions are subsequently termed as intron variants of that gene (e.g. sbd2_1/I1, sbd2_1/I2 etc.)

251_2005_1_Fig6d_ESM.gif (39 kb)

Luenser et al. 2005; Evolution of caprine and ovine β-defensin genes Multiple sequence alignment of complete caprine and ovine defensin genes. Vertical numbers indicate nucleotide positions. Dots indicate identical sites referring to sbd2, and dashes indicate gaps introduced by the alignment. Nucleotides of exon1 (1–57) and 2 (1564–1621) are in bold letters. Sequences solely differing in intron regions are subsequently termed as intron variants of that gene (e.g. sbd2_1/I1, sbd2_1/I2 etc.)

251_2005_1_Fig6e_ESM.gif (16 kb)

Luenser et al. 2005; Evolution of caprine and ovine β-defensin genes Multiple sequence alignment of complete caprine and ovine defensin genes. Vertical numbers indicate nucleotide positions. Dots indicate identical sites referring to sbd2, and dashes indicate gaps introduced by the alignment. Nucleotides of exon1 (1–57) and 2 (1564–1621) are in bold letters. Sequences solely differing in intron regions are subsequently termed as intron variants of that gene (e.g. sbd2_1/I1, sbd2_1/I2 etc.)

251_2005_1_Fig6f_ESM.gif (37 kb)

Luenser et al. 2005; Evolution of caprine and ovine β-defensin genes Multiple sequence alignment of complete caprine and ovine defensin genes. Vertical numbers indicate nucleotide positions. Dots indicate identical sites referring to sbd2, and dashes indicate gaps introduced by the alignment. Nucleotides of exon1 (1–57) and 2 (1564–1621) are in bold letters. Sequences solely differing in intron regions are subsequently termed as intron variants of that gene (e.g. sbd2_1/I1, sbd2_1/I2 etc.)

251_2005_1_Fig6g_ESM.gif (14 kb)

Luenser et al. 2005; Evolution of caprine and ovine β-defensin genes Multiple sequence alignment of complete caprine and ovine defensin genes. Vertical numbers indicate nucleotide positions. Dots indicate identical sites referring to sbd2, and dashes indicate gaps introduced by the alignment. Nucleotides of exon1 (1–57) and 2 (1564–1621) are in bold letters. Sequences solely differing in intron regions are subsequently termed as intron variants of that gene (e.g. sbd2_1/I1, sbd2_1/I2 etc.)

251_2005_1_Fig6h_ESM.gif (12 kb)

Luenser et al. 2005; Evolution of caprine and ovine β-defensin genes Multiple sequence alignment of complete caprine and ovine defensin genes. Vertical numbers indicate nucleotide positions. Dots indicate identical sites referring to sbd2, and dashes indicate gaps introduced by the alignment. Nucleotides of exon1 (1–57) and 2 (1564–1621) are in bold letters. Sequences solely differing in intron regions are subsequently termed as intron variants of that gene (e.g. sbd2_1/I1, sbd2_1/I2 etc.)

251_2005_1_Fig6i_ESM.gif (59 kb)

Luenser et al. 2005; Evolution of caprine and ovine β-defensin genes Multiple sequence alignment of complete caprine and ovine defensin genes. Vertical numbers indicate nucleotide positions. Dots indicate identical sites referring to sbd2, and dashes indicate gaps introduced by the alignment. Nucleotides of exon1 (1–57) and 2 (1564–1621) are in bold letters. Sequences solely differing in intron regions are subsequently termed as intron variants of that gene (e.g. sbd2_1/I1, sbd2_1/I2 etc.)

251_2005_1_Fig6j_ESM.gif (30 kb)

Luenser et al. 2005; Evolution of caprine and ovine β-defensin genes Multiple sequence alignment of complete caprine and ovine defensin genes. Vertical numbers indicate nucleotide positions. Dots indicate identical sites referring to sbd2, and dashes indicate gaps introduced by the alignment. Nucleotides of exon1 (1–57) and 2 (1564–1621) are in bold letters. Sequences solely differing in intron regions are subsequently termed as intron variants of that gene (e.g. sbd2_1/I1, sbd2_1/I2 etc.)

251_2005_1_Fig6k_ESM.gif (56 kb)

Luenser et al. 2005; Evolution of caprine and ovine β-defensin genes Multiple sequence alignment of complete caprine and ovine defensin genes. Vertical numbers indicate nucleotide positions. Dots indicate identical sites referring to sbd2, and dashes indicate gaps introduced by the alignment. Nucleotides of exon1 (1–57) and 2 (1564–1621) are in bold letters. Sequences solely differing in intron regions are subsequently termed as intron variants of that gene (e.g. sbd2_1/I1, sbd2_1/I2 etc.)

251_2005_1_Fig6l_ESM.gif (57 kb)

Luenser et al. 2005; Evolution of caprine and ovine β-defensin genes Multiple sequence alignment of complete caprine and ovine defensin genes. Vertical numbers indicate nucleotide positions. Dots indicate identical sites referring to sbd2, and dashes indicate gaps introduced by the alignment. Nucleotides of exon1 (1–57) and 2 (1564–1621) are in bold letters. Sequences solely differing in intron regions are subsequently termed as intron variants of that gene (e.g. sbd2_1/I1, sbd2_1/I2 etc.)

251_2005_1_Fig6m_ESM.gif (31 kb)

Luenser et al. 2005; Evolution of caprine and ovine β-defensin genes Multiple sequence alignment of complete caprine and ovine defensin genes. Vertical numbers indicate nucleotide positions. Dots indicate identical sites referring to sbd2, and dashes indicate gaps introduced by the alignment. Nucleotides of exon1 (1–57) and 2 (1564–1621) are in bold letters. Sequences solely differing in intron regions are subsequently termed as intron variants of that gene (e.g. sbd2_1/I1, sbd2_1/I2 etc.)

251_2005_1_Fig6n_ESM.gif (40 kb)

Luenser et al. 2005; Evolution of caprine and ovine β-defensin genes Multiple sequence alignment of complete caprine and ovine defensin genes. Vertical numbers indicate nucleotide positions. Dots indicate identical sites referring to sbd2, and dashes indicate gaps introduced by the alignment. Nucleotides of exon1 (1–57) and 2 (1564–1621) are in bold letters. Sequences solely differing in intron regions are subsequently termed as intron variants of that gene (e.g. sbd2_1/I1, sbd2_1/I2 etc.)

251_2005_1_Fig6o_ESM.gif (30 kb)

Luenser et al. 2005; Evolution of caprine and ovine β-defensin genes Multiple sequence alignment of complete caprine and ovine defensin genes. Vertical numbers indicate nucleotide positions. Dots indicate identical sites referring to sbd2, and dashes indicate gaps introduced by the alignment. Nucleotides of exon1 (1–57) and 2 (1564–1621) are in bold letters. Sequences solely differing in intron regions are subsequently termed as intron variants of that gene (e.g. sbd2_1/I1, sbd2_1/I2 etc.)

References

  1. Antcheva N, Boniotto M, Zelezetsky I, Pacor S, Falzacappa MV, Crovella S, Tossi A (2004) Effects of positively selected sequence variations in human and Macaca fascicularis beta-defensins 2 on antimicrobial activity. Antimicrob Agents Chemother 48:685–688CrossRefPubMedGoogle Scholar
  2. Bals R, Goldman MJ, Wilson JM (1998) Mouse beta-defensin 1 is a salt-sensitive antimicrobial peptide present in epithelia of the lung and urogenital tract. Infect Immun 66:1225–1232PubMedGoogle Scholar
  3. Bensch KW, Raida M, Magert HJ, Schulz-Knappe P, Forssmann WG (1995) hBD-1: a novel beta-defensin from human plasma. FEBS Lett 368:331–335CrossRefPubMedGoogle Scholar
  4. Boman HG (1991) Antibacterial peptides: key components needed in immunity. Cell 65:205–207CrossRefPubMedGoogle Scholar
  5. Boniotto M, Antcheva N, Zelezetsky I, Tossi A, Palumbo V, Verga Falzacappa MV, Sgubin S, Braida L, Amoroso A, Crovella S (2003a) A study of host defence peptide beta-defensin 3 in primates. Biochem J 374:707–714CrossRefPubMedGoogle Scholar
  6. Boniotto M, Tossi A, DelPero M, Sgubin S, Antcheva N, Santon D, Masters J, Crovella S (2003b) Evolution of the beta defensin 2 gene in primates. Genes Immun 4:251–257CrossRefPubMedGoogle Scholar
  7. Brockus CW, Jackwood MW, Harmon BG (1998) Characterization of beta-defensin prepropeptide mRNA from chicken and turkey bone marrow. Anim Genet 29:283–289CrossRefPubMedGoogle Scholar
  8. Clark AG (1994) Invasion and maintenance of a gene duplication. Proc Natl Acad Sci U S A 91:2950–2954PubMedCrossRefGoogle Scholar
  9. Del Pero M, Boniotto M, Zuccon D, Cervella P, Spano A, Amoroso A, Crovella S (2002) Beta-defensin 1 gene variability among non-human primates. Immunogenetics 53:907–913CrossRefPubMedGoogle Scholar
  10. Diamond G, Bevins CL (1998) beta-Defensins: endogenous antibiotics of the innate host defense response. Clin Immunol Immunopathol 88:221–225CrossRefPubMedGoogle Scholar
  11. Diamond G, Zasloff M, Eck H, Brasseur M, Maloy WL, Bevins CL (1991) Tracheal antimicrobial peptide, a cysteine-rich peptide from mammalian tracheal mucosa: peptide isolation and cloning of a cDNA. Proc Natl Acad Sci U S A 88:3952–3956PubMedCrossRefGoogle Scholar
  12. Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531–1545PubMedGoogle Scholar
  13. Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709PubMedGoogle Scholar
  14. Gabay JE, Scott RW, Campanelli D, Griffith J, Wilde C, Marra MN, Seeger M, Nathan CF (1989) Antibiotic proteins of human polymorphonuclear leukocytes. Proc Natl Acad Sci U S A 86:5610–5614PubMedCrossRefGoogle Scholar
  15. Ganz T (2003) Defensins: antimicrobial peptides of innate immunity. Nat Rev Immunol 3:710–720CrossRefPubMedGoogle Scholar
  16. Ganz T, Selsted ME, Szklarek D, Harwig SS, Daher K, Bainton DF, Lehrer RI (1985) Defensins. Natural peptide antibiotics of human neutrophils. J Clin Invest 76:1427–1435PubMedCrossRefGoogle Scholar
  17. Hancock RE, Lehrer RI (1998) Cationic peptides: a new source of antibiotics. Trends Biotechnol 16:82–88CrossRefPubMedGoogle Scholar
  18. Harder J, Bartels J, Christophers E, Schroder JM (1997) A peptide antibiotic from human skin. Nature 387:861CrossRefPubMedGoogle Scholar
  19. Harwig SS, Swiderek KM, Kokryakov VN, Tan L, Lee TD, Panyutich EA, Aleshina GM, Shamova OV, Lehrer RI (1994) Gallinacins: cysteine-rich antimicrobial peptides of chicken leukocytes. FEBS Lett 342:281–285CrossRefPubMedGoogle Scholar
  20. Hoover DM, Boulegue C, Yang D, Oppenheim JJ, Tucker K, Lu W, Lubkowski J (2002) The structure of human macrophage inflammatory protein-3alpha /CCL20. Linking antimicrobial and CC chemokine receptor-6-binding activities with human beta-defensins. J Biol Chem 40:37647–37654CrossRefGoogle Scholar
  21. Hudson RR, Kreitman M, Aguade M (1987) A test of neutral molecular evolution based on nucleotide data. Genetics 116:153–159PubMedGoogle Scholar
  22. Hughes AL (1999) Evolutionary diversification of the mammalian defensins. Cell Mol Life Sci 56:94–103CrossRefPubMedGoogle Scholar
  23. Hughes AL, Yeager M (1997) Coordinated amino acid changes in the evolution of mammalian defensins. J Mol Evol 44:675–682PubMedCrossRefGoogle Scholar
  24. Huttner KM, Kozak CA, Bevins CL (1997) The mouse genome encodes a single homolog of the antimicrobial peptide human beta-defensin 1. FEBS Lett 413:45–49CrossRefPubMedGoogle Scholar
  25. Huttner KM, Lambeth MR, Burkin HR, Burkin DJ, Broad TE (1998) Localization and genomic organization of sheep antimicrobial peptide genes. Gene 206:85–91CrossRefPubMedGoogle Scholar
  26. Jia HP, Wowk SA, Schutte BC, Lee SK, Vivado A, Tack BF, Bevins CL, McCray PB Jr (2000) A novel murine beta-defensin expressed in tongue, esophagus, and trachea. J Biol Chem 275:33314–33320CrossRefPubMedGoogle Scholar
  27. Jones DE, Bevins CL (1992) Paneth cells of the human small intestine express an antimicrobial peptide gene. J Biol Chem 267:23216–23225PubMedGoogle Scholar
  28. Jones DE, Bevins CL (1993) Defensin-6 mRNA in human Paneth cells: implications for antimicrobial peptides in host defense of the human bowel. FEBS Lett 315:187–192CrossRefPubMedGoogle Scholar
  29. Jukes T, Cantor C (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic, New York, pp 21–132Google Scholar
  30. Kagan BL, Selsted ME, Ganz T, Lehrer RI (1990) Antimicrobial defensin peptides form voltage-dependent ion-permeable channels in planar lipid bilayer membranes. Proc Natl Acad Sci U S A 87:210–214PubMedCrossRefGoogle Scholar
  31. Kimura M (1969) The number of heterozygous nucleotide sites maintained in a finite population due to steady flux of mutations. Genetics 61:893–903PubMedGoogle Scholar
  32. Kimura M (1977) Preponderance of synonymous changes as evidence for the neutral theory of molecular evolution. Nature 267:275–276CrossRefPubMedGoogle Scholar
  33. Kumar S, Tamura K, Nei M (1993) MEGA: Molecular Evolutionary Genetics Analysis, version 1.01. Pennsylvania State University, University Park, PAGoogle Scholar
  34. Lehrer RI, Ganz T (2002) Defensins of vertebrate animals. Curr Opin Immunol 14:96–102CrossRefPubMedGoogle Scholar
  35. Lehrer RI, Ganz T, Szklarek D, Selsted ME (1988) Modulation of the in vitro candidacidal activity of human neutrophil defensins by target cell metabolism and divalent cations. J Clin Invest 8:1829–1835Google Scholar
  36. Lehrer RI, Lichtenstein AK, Ganz T (1993) Defensins: antimicrobial and cytotoxic peptides of mammalian cells. Annu Rev Immunol 11:105–128CrossRefPubMedGoogle Scholar
  37. Liu L, Zhao C, Heng HH, Ganz T (1997) The human beta-defensin-1 and alpha-defensins are encoded by adjacent genes: two peptide families with differing disulfide topology share a common ancestry. Genomics 43:316–320CrossRefPubMedGoogle Scholar
  38. Ludwig A, Fischer S (1998) New aspects of an old discussion—phylogenetic relationships of Ammotragus and Pseudois within the subfamily Caprinae based on comparison of the 12S rDNA sequences. J Zoolog Syst Evol Res 36:173–178Google Scholar
  39. Luenser K, Ludwig A (2005) Variability and evolution of bovine beta-defensin genes. Genes Immun 6:115–122CrossRefPubMedGoogle Scholar
  40. Lynn DJ, Lloyd AT, Fares MA, O'Farrelly C (2004) Evidence of positively selected sites in mammalian alpha-defensins. Mol Biol Evol 21:819–827CrossRefPubMedGoogle Scholar
  41. Martin E, Ganz T, Lehrer RI (1995) Defensins and other endogenous peptide antibiotics of vertebrates. J Leukoc Biol 58:128–136PubMedGoogle Scholar
  42. Maxwell AI, Morrison GM, Dorin JR (2003) Rapid sequence divergence in mammalian beta-defensins by adaptive evolution. Mol Immunol 40:413–421CrossRefPubMedGoogle Scholar
  43. McDonald JH, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652–654CrossRefPubMedGoogle Scholar
  44. Morrison GM, Semple CA, Kilanowski FM, Hill RE, Dorin JR (2003) Signal sequence conservation and mature peptide divergence within subgroups of the murine beta-defensin gene family. Mol Biol Evol 20:460–470CrossRefPubMedGoogle Scholar
  45. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York, pp 79–83Google Scholar
  46. Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426PubMedGoogle Scholar
  47. Nguyen TX, Cole AM, Lehrer RI (2003) Evolution of primate theta-defensins: a serpentine path to a sweet tooth. Peptides 24:1647–1654CrossRefPubMedGoogle Scholar
  48. Nicholas P, Mor A (1995) Peptides as weapons against microorganisms in the chemical defense system of vertebrates. Annu Rev Microbiol 49:227–304Google Scholar
  49. Nowak MA, Boerlijst MC, Cooke J, Smith JM (1997) Evolution of genetic redundancy. Nature 388:167–171CrossRefPubMedGoogle Scholar
  50. Ohno S (1970) Evolution by gene duplication. Springer, Berlin Heidelberg New YorkGoogle Scholar
  51. Ohno S (1973) Ancient linkage groups and frozen accidents. Nature 244:259–262CrossRefGoogle Scholar
  52. Ouellette AJ (2004) Defensin-mediated innate immunity in the small intestine. Best Pract Res Clin Gastroenterol 18:405–419CrossRefPubMedGoogle Scholar
  53. Ouellette AJ, Miller SI, Henschen AH, Selsted ME (1992) Purification and primary structure of murine cryptdin-1, a Paneth cell defensin. FEBS Lett 304:146–148CrossRefPubMedGoogle Scholar
  54. Ouellette AJ, Hsieh MM, Nosek MT, Cano-Gauci DF, Huttner KM, Buick RN, Selsted ME (1994) Mouse Paneth cell defensins: primary structures and antibacterial activities of numerous cryptdin isoforms. Infect Immun 62:5040–5047PubMedGoogle Scholar
  55. Ouellette AJ, Satchell DP, Hsieh MM, Hagen SJ, Selsted ME (2000) Characterization of luminal Paneth cell alpha-defensins in mouse small intestine. Attenuated antimicrobial activities of peptides with truncated amino termini. J Biol Chem 275:33969–33973CrossRefPubMedGoogle Scholar
  56. Patil A, Hughes AL, Zhang G (2004) Rapid evolution and diversification of mammalian alpha-defensins as revealed by comparative analysis of rodent and primate genes. Physiol Genomics 20:1–11CrossRefPubMedGoogle Scholar
  57. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818CrossRefPubMedGoogle Scholar
  58. Raj PA, Dentino AR (2002) Current status of defensins and their role in innate and adaptive immunity. FEMS Microbiol Lett 206:9–18CrossRefPubMedGoogle Scholar
  59. Raj PA, Antonyraj KJ, Karunakaran T (2000) Large-scale synthesis and functional elements for the antimicrobial activity of defensins. Biochem J 347:633–641CrossRefPubMedGoogle Scholar
  60. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497CrossRefPubMedGoogle Scholar
  61. Russell JP, Diamond G, Tarver AP, Scanlin TF, Bevins CL (1996) Coordinate induction of two antibiotic genes in tracheal epithelial cells exposed to the inflammatory mediators lipopolysaccharide and tumor necrosis factor alpha. Infect Immun 64:1565–1568PubMedGoogle Scholar
  62. Satchell DP, Sheynis T, Shirafuji Y, Kolusheva S, Ouellette AJ, Jelinek R (2003) Interactions of mouse Paneth cell alpha-defensins and alpha-defensin precursors with membranes. Prosegment inhibition of peptide association with biomimetic membranes. J Biol Chem 278:13838–13846CrossRefPubMedGoogle Scholar
  63. Schonwetter BS, Stolzenberg ED, Zasloff MA (1995) Epithelial antibiotics induced at sites of inflammation. Science 267:1645–1648PubMedCrossRefGoogle Scholar
  64. Schröder JM (1999) Epithelial antimicrobial peptides: innate local host response elements. Cell Mol Life Sci 56:32–46CrossRefPubMedGoogle Scholar
  65. Schutte BC, McCray PB Jr (2002) [beta]-Defensins in lung host defense. Annu Rev Physiol 64:709–748CrossRefPubMedGoogle Scholar
  66. Schutte BC, Mitros JP, Bartlett JA, Walters JD, Jia HP, Welsh MJ, Casavant TL, McCray PB Jr (2002) Discovery of five conserved beta-defensin gene clusters using a computational search strategy. Proc Natl Acad Sci U S A 99:2129–2133CrossRefPubMedGoogle Scholar
  67. Selsted ME, Brown DM, DeLange RJ, Harwig SS, Lehrer RI (1985) Primary structures of six antimicrobial peptides of rabbit peritoneal neutrophils. J Biol Chem 260:4579–4584PubMedGoogle Scholar
  68. Selsted ME, Tang YQ, Morris WL, McGuire PA, Novotny MJ, Smith W, Henschen AH, Cullor JS (1993) Purification, primary structures, and antibacterial activities of beta-defensins, a new family of antimicrobial peptides from bovine neutrophils. J Biol Chem 268:6641–6648PubMedGoogle Scholar
  69. Semple CA, Rolfe M, Dorin JR (2003) Duplication and selection in the evolution of primate beta-defensin genes. Genome Biol 4:R31. DOI  10.1186/gb-2003-4-5-r31 CrossRefPubMedGoogle Scholar
  70. Shackleton DM, IUCN/SSC Caprinae Specialist Group (1997) Wild sheep and goats and their relatives. Status survey and conservation action plan for Caprinae. IUCN, Gland, SwitzerlandGoogle Scholar
  71. Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (*and other methods). Sinauer Associates, Sunderland, MAGoogle Scholar
  72. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedGoogle Scholar
  73. Tanabe H, Yuan J, Zaragoza MM, Dandekar S, Henschen-Edman A, Selsted ME, Ouellette AJ (2004) Paneth cell alpha-defensins from rhesus macaque small intestine. Infect Immun 72:1470–1478CrossRefPubMedGoogle Scholar
  74. Tang YQ, Yuan J, Miller CJ, Selsted ME (1999a) Isolation, characterization, cDNA cloning, and antimicrobial properties of two distinct subfamilies of alpha-defensins from rhesus macaque leukocytes. Infect Immun 67:6139–6144PubMedGoogle Scholar
  75. Tang YQ, Yuan J, Osapay G, Osapay K, Tran D, Miller CJ, Ouellette AJ, Selsted ME (1999b) A cyclic antimicrobial peptide produced in primate leukocytes by the ligation of two truncated alpha-defensins. Science 286:498–502CrossRefPubMedGoogle Scholar
  76. Territo MC, Ganz T, Selsted ME, Lehrer RI (1989) Monocyte-chemotactic activity of defensins from human neutrophils. J Clin Invest 84:2017–2020PubMedGoogle Scholar
  77. Wang W, Cole AM, Hong T, Waring AJ, Lehrer RI (2003) Retrocyclin, an antiretroviral theta-defensin, is a lectin. J Immunol 170:4708–4716PubMedGoogle Scholar
  78. Wilde CG, Griffith JE, Marra MN, Snable JL, Scott RW (1989) Purification and characterization of human neutrophil peptide 4, a novel member of the defensin family. J Biol Chem 264:11200–11203PubMedGoogle Scholar
  79. Xiao Y, Hughes AL, Ando J, Matsuda Y, Cheng JF, Skinner-Noble D, Zhang G (2004) A genome-wide screen identifies a single beta-defensin gene cluster in the chicken: implications for the origin and evolution of mammalian defensins. BMC Genomics 5:56CrossRefPubMedGoogle Scholar
  80. Yang D, Chertov O, Bykovskaia SN, Chen Q, Buffo MJ, Shogan J, Anderson M, Schroder JM, Wang JM, Howard OM, Oppenheim JJ (1999) Beta-defensins: linking innate and adaptive immunity through dendritic and T cell CCR6. Science 286:525–528CrossRefPubMedGoogle Scholar
  81. Yang D, Biragyn A, Hoover DM, Lubkowski J, Oppenheim JJ (2004) Multiple roles of antimicrobial defensins, cathelicidins, and eosinophil-derived neurotoxin in host defense. Annu Rev Immunol 22:181–215CrossRefPubMedGoogle Scholar
  82. Zeya HI, Spitznagel JK (1966) Antimicrobial specificity of leukocyte lysosomal cationic proteins. Science 154:1049–1051PubMedCrossRefGoogle Scholar
  83. Zhang J (2003) Evolution by gene duplication. Trends Ecol Evol 18:292–298CrossRefGoogle Scholar
  84. Zhao C, Nguyen T, Liu L, Shamova O, Brogden K, Lehrer RI (1999) Differential expression of caprine beta-defensins in digestive and respiratory tissues. Infect Immun 67:6221–6224PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  1. 1.Department of Evolutionary GeneticsLeibniz Institute for Zoo and Wildlife ResearchBerlinGermany
  2. 2.Department of Breeding Biology and Molecular Genetics, Institute for Animal SciencesHumboldt University BerlinBerlinGermany

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