Skip to main content
Log in

Expression of defensins in non-infected araneomorph spiders

  • Research Article
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

Defensins are a major family of antimicrobial peptides found throughout the phylogenetic tree. From the spider species: Cupiennius salei, Phoneutria reidyi, Polybetes pythagoricus, Tegenaria atrica, and Meta menardi, defensins belonging to the ‘ancestral’ class of invertebrate defensins were cloned and sequenced. The deduced amino acid sequences contain the characteristic six cysteines of this class of defensins and reveal precursors of 60 or 61 amino acid residues. The mature peptides consist of 37 amino acid residues, showing up to 70% identities with tick and scorpion defensins. In C. salei, defensin mRNA was found to be constitutively expressed in hemocytes, ovaries, subesophageal nerve mass, hepatopancreas, and muscle tissue. This is the first report presenting and comparing antimicrobial peptides belonging to the family of defensins from spiders.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Jiravanichpaisal P, Lee BL, Söderhäll K (2006) Cell-mediated immunity in arthropods: hematopoiesis, coagulation, melanization and opsonization. Immunobiology 211:213–236

    Article  CAS  PubMed  Google Scholar 

  2. Hoffmann JA, Kafatos FC, Janeway CA, Ezekowitz RA (1999) Phylogenetic perspectives in innate immunity. Science 284:1313–1318

    Article  CAS  PubMed  Google Scholar 

  3. Bulet P, Stöcklin R, Menin L (2004) Anti-microbial peptides: from invertebrates to vertebrates. Immunol Rev 198:169–184

    Article  CAS  PubMed  Google Scholar 

  4. Hwang PM, Zhou N, Shan X, Arrowsmith CH, Vogel HJ (1998) Three-dimensional solution structure of lactoferricin B, an antimicrobial peptide derived from bovine lactoferrin. Biochemistry 37:4288–4298

    Article  CAS  PubMed  Google Scholar 

  5. Patel SU, Osborn R, Rees S, Thornton JM (1998) Structural studies of Impatiens balsamina antimicrobial protein (Ib-AMP1). Biochemistry 37:983–990

    Article  CAS  PubMed  Google Scholar 

  6. Froy O, Gurevitz M (2003) Arthropod and mollusk defensins-evolution by exon-shuffling. Trends Genet 19:684–687

    Article  CAS  PubMed  Google Scholar 

  7. Rodríguez de la Vega RC, Possani LD (2005) On the evolution of invertebrate defensins. Trends Genet 21:330–332

    Article  PubMed  Google Scholar 

  8. Wong JA, Xia L, Ng TB (2007) A review of defensins of diverse origins. Curr Prot Pept Sci 5:446–459

    Article  Google Scholar 

  9. Cornet B, Bonmatin JM, Hetru C, Hoffmann JA, Ptak M, Vovelle F (1995) Refined three-dimensional solution structure of insect defensin A. Structure 3:435–448

    Article  CAS  PubMed  Google Scholar 

  10. Hanzawa H, Shimada I, Kuzuhara T, Komano H, Kohda D, Inagaki F, Natori S, Arata Y (1990) 1H nuclear magnetic resonance study of the solution conformation of an antibacterial protein, sapecin. FEBS Lett 269:413–420

    Article  CAS  PubMed  Google Scholar 

  11. Yang YS, Mitta G, Chavanieu A, Calas B, Sanchez JF, Roch P, Aumelas A (2000) Solution structure and activity of the synthetic four-disulfide bond Mediterranean mussel defensin (MGD-1). Biochemistry 39:14436–14447

    Article  CAS  PubMed  Google Scholar 

  12. Mygind PH, Fischer RL, Schnorr KM, Hansen MT, Sonksen CP, Ludvigsen S, Raventos D, Buskov S, Christensen B, De Maria L, Taboureau O, Yaver D, Elvig-Jorgensen SG, Sorensen MV, Christensen BE, Kjaerulff S, Frimodt-Moller N, Lehrer RI, Zasloff M, Kristensen HH (2005) Plectasin is a peptide antibiotic with therapeutic potential from a saprophytic fungus. Nature 437:975–980

    Article  CAS  PubMed  Google Scholar 

  13. Mandard N, Bulet P, Caille A, Daffre S, Vovelle F (2002) The solution structure of gomesin, an antimicrobial cysteine-rich peptide from the spider. Eur J Biochem 269:1190–1198

    Article  CAS  PubMed  Google Scholar 

  14. Silva PI Jr, Daffre S, Bulet P (2000) Isolation and characterization of gomesin, an 18-residue cysteine-rich defense peptide from the spider Acanthoscurria gomesiana hemocytes with sequence similarities to horseshoe crab antimicrobial peptides of the tachyplesin family. J Biol Chem 275:33464–33470

    Article  CAS  PubMed  Google Scholar 

  15. Lorenzini DM, da Silva PI, Fogaça AC Jr, Bulet P, Daffre S (2003) Acanthoscurrin: a novel glycine-rich antimicrobial peptide constitutively expressed in the hemocytes of the spider Acanthoscurria gomesiana. Dev Comp Immunol 27:781–791

    Article  CAS  PubMed  Google Scholar 

  16. Bachère E, Gueguen Y, Gonzalez M, de Lorgeril J, Garnier J, Romestand B (2004) Insights into the anti-microbial defense of marine invertebrates: the penaeid shrimps and the oyster Crassostrea gigas. Immunol Rev 198:149–168

    Article  PubMed  Google Scholar 

  17. Mitta G, Vandenbulcke F, Noel T, Romestand B, Beauvillain JC, Salzet M, Roch P (2000) Differential distribution and defence involvement of antimicrobial peptides in mussel. J Cell Sci 113:2759–2769

    CAS  PubMed  Google Scholar 

  18. Shigenaga T, Muta T, Toh Y, Tokunaga F, Iwanaga S (1990) Antimicrobial tachyplesin peptide precursor. cDNA cloning and cellular localization in the horseshoe crab (Tachypleus tridentatus). J Biol Chem 265:21350–21354

    CAS  PubMed  Google Scholar 

  19. Gillespie JP, Kanost MR, Trenczek T (1997) Biological mediators of insect immunity. Annu Rev Entomol 42:611–643

    Article  CAS  PubMed  Google Scholar 

  20. Hoffmann JA, Reichhart JM (2002) Drosophila innate immunity: an evolutionary perspective. Nat Immunol 3:121–126

    Article  CAS  PubMed  Google Scholar 

  21. Söderhäll K, Smith VJ (1983) Separation of the haemocyte populations of Carcinus maenas and other marine decapods, and prophenoloxidase distribution. Dev Comp Immunol 7:229–239

    Article  PubMed  Google Scholar 

  22. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  23. Bendtsen JD, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340:783–795

    Article  PubMed  Google Scholar 

  24. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed  Google Scholar 

  25. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  26. Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282

    CAS  PubMed  Google Scholar 

  27. Felsenstein J (1989) PHYLIP, phylogeny inference package (Version 3.2). Cladistics 5:164–166

    Google Scholar 

  28. Fukuzawa AH, Vellutini BC, Lorenzini DM, Silva PI Jr, Mortara RA, da Silva JM, Daffre S (2008) The role of hemocytes in the immunity of the spider Acanthoscurria gomesiana. Dev Comp Immunol 32:716–725

    Article  CAS  PubMed  Google Scholar 

  29. Lorenzini DM, Fukuzawa AH, da Silva PI, Machado-Santelli G Jr, Bijovsky AT, Daffre S (2003) Molecular cloning, expression analysis and cellular localization of gomesin, an anti-microbial peptide from hemocytes of the spider Acanthoscurria gomesiana. Insect Biochem Mol Biol 33:1011–1016

    Article  CAS  PubMed  Google Scholar 

  30. Kuhn-Nentwig L, Müller J, Schaller J, Walz A, Dathe M, Nentwig W (2002) Cupiennin 1, a new family of highly basic antimicrobial peptides in the venom of the spider Cupiennius salei (Ctenidae). J Biol Chem 277:11208–11216

    Article  CAS  PubMed  Google Scholar 

  31. Kuhn-Nentwig L, Trachsel C, Nentwig W (2009) Spider venom and hemolymph-derived cytolytic and antimicrobial peptides. In: Howl J, Jones S (eds) Bioactive Peptides. CRC Press, Boca Raton, pp 447–464

    Google Scholar 

  32. Hynes WL, Ceraul SM, Todd SM, Seguin KC, Sonenshine DE (2005) A defensin-like gene expressed in the black-legged tick, Ixodes scapularis. Med Vet Entomol 19:339–344

    Article  CAS  PubMed  Google Scholar 

  33. Nakajima Y, van Naters-Yasui A, Taylor D, Yamakawa M (2002) Antibacterial peptide defensin is involved in midgut immunity of the soft tick, Ornithodoros moubata. Insect Mol Biol 11:611–618

    Article  CAS  PubMed  Google Scholar 

  34. Fogaça AC, Lorenzini DM, Kaku LM, Esteves E, Bulet P, Daffre S (2004) Cysteine-rich antimicrobial peptides of the cattle tick Boophilus microplus: isolation, structural characterization and tissue expression profile. Dev Comp Immunol 28:191–200

    Article  PubMed  Google Scholar 

  35. Todd SM, Sonenshine DE, Hynes WL (2007) Tissue and life-stage distribution of a defensin gene in the Lone Star tick, Amblyomma americanum. Med Vet Entomol 21:141–147

    Article  CAS  PubMed  Google Scholar 

  36. Ceraul SM, Dreher-Lesnick SM, Gillespie JJ, Rahman MS, Azad AF (2007) New tick defensin isoform and antimicrobial gene expression in response to Rickettsia montanensis challenge. Infect Immun 75:1973–1983

    Article  CAS  PubMed  Google Scholar 

  37. Zhou J, Liao M, Ueda M, Gong H, Xuan X, Fujisaki K (2007) Sequence characterization and expression patterns of two defensin-like antimicrobial peptides from the tick Haemaphysalis longicornis. Peptides 28:1304–1310

    Article  CAS  PubMed  Google Scholar 

  38. Saito Y, Konnai S, Yamada S, Imamura S, Nishikado H, Ito T, Onuma M, Ohashi K (2009) Identification and characterization of antimicrobial peptide, defensin, in the taiga tick, Ixodes persulcatus. Insect Mol Biol 18:531–539

    Article  CAS  PubMed  Google Scholar 

  39. Mitta G, Vandenbulcke F, Hubert F, Roch P (1999) Mussel defensins are synthesised and processed in granulocytes then released into the plasma after bacterial challenge. J Cell Sci 112:4233–4242

    CAS  PubMed  Google Scholar 

  40. Gonzalez M, Gueguen Y, Desserre G, de Lorgeril J, Romestand B, Bachère E (2007) Molecular characterization of two isoforms of defensin from hemocytes of the oyster Crassostrea gigas. Dev Comp Immunol 31:332–339

    Article  CAS  PubMed  Google Scholar 

  41. Gueguen Y, Herpin A, Aumelas A, Garnier J, Fievet J, Escoubas JM, Bulet P, Gonzalez M, Lelong C, Favrel P, Bachère E (2006) Characterization of a defensin from the oyster Crassostrea gigas. Recombinant production, folding, solution structure, antimicrobial activities, and gene expression. J Biol Chem 281:313–323

    Article  CAS  PubMed  Google Scholar 

  42. Mitta G, Hubert F, Dyrynda EA, Boudry P, Roch P (2000) Mytilin B and MGD2, two antimicrobial peptides of marine mussels: gene structure and expression analysis. Dev Comp Immunol 24:381–393

    Article  CAS  PubMed  Google Scholar 

  43. Rodríguez de la Vega RC, García BI, D’Ambrosio C, Diego-García E, Scaloni A, Possani LD (2004) Antimicrobial peptide induction in the haemolymph of the Mexican scorpion Centruroides limpidus limpidus in response to septic injury. Cell Mol Life Sci 61:1507–1519

    Article  PubMed  Google Scholar 

  44. Huber KC, Haider TS, Müller MW, Huber BA, Schweyen RJ, Barth FG (1993) DNA-sequence data indicates the polyphyly of the family Ctenidae (Araneae). J Arachnol 21:194–201

    Google Scholar 

  45. Lorenzini DM, da Silva PI, Soares MB Jr, Arruda P, Setubal J, Daffre S (2006) Discovery of immune-related genes expressed in hemocytes of the tarantula spider Acanthoscurria gomesiana. Dev Comp Immunol 30:545–556

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Dr. C. Kropf for kindly providing M. menardi, Prof. Dr. J. Schaller for MS measurements, Dr. D. Destoumieux-Garzón and Dr. H. Murray for critical comments on the manuscript, and the Swiss National Science Foundation for funding.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lucia Kuhn-Nentwig.

Electronic supplementary material

Below is the link to the electronic supplementary material.

18_2010_354_MOESM1_ESM.tif

Fig. S1 Partial C. salei defensin gene structure. PCR products of hemocyte cDNA and genomic DNA with defensin-specific primers. The 50-bp molecular weight marker is marked with MW; band sizes are in bp. (TIFF 4753 kb)

Supplementary material (DOC 50 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Baumann, T., Kuhn-Nentwig, L., Largiadèr, C.R. et al. Expression of defensins in non-infected araneomorph spiders. Cell. Mol. Life Sci. 67, 2643–2651 (2010). https://doi.org/10.1007/s00018-010-0354-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-010-0354-2

Keywords

Navigation