Ixodes ricinus defensins attack distantly-related pathogens

Developmental and Comparative Immunology

Volumn 53, Issue 2, 2015, Pages 358-365

  Tonk, Miray ^a   Cabezas Cruz, Alejandro ^b   Valdés, James J ^c   Rego, Ryan O M ^c   Grubhoffer, Libor ^c,d   Estrada Peña, Agustín ^e   Vilcinskas, Andreas ^a,f   Kotsyfakis, Michalis ^c   Rahnamaeian, Mohammad ^a,e  

^a FRAUNHOFER INSTITUTE FOR MOLECULAR BIOLOGY AND APPLIED ECOLOGY IME   (Germany)

^b INSERM U1019   (France)

^c INSTITUTE OF PARASITOLOGY   (Czech Republic)

^d UNIVERSITY OF SOUTH BOHEMIA   (Czech Republic)

^e UNIVERSIDAD DE ZARAGOZA   (Spain)

^f JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Antimicrobial peptide; Defensin; Escherichia coli; Fusarium spp; Ixodes ricinus; Listeria monocytogenes; Pseudomonas aeruginosa; Staphylococcus aureus; Staphylococcus epidermidis

Indexed keywords

AMINO ACID; DEFENSIN; DEFENSIN MT2; DEFENSIN MT3; DEFENSIN MT5; DEFENSIN MT6; DEFENSIN MT7; UNCLASSIFIED DRUG; INSECT PROTEIN;

ALPHA HELIX; AMINO ACID SUBSTITUTION; ANTIFUNGAL ACTIVITY; ANTIMICROBIAL ACTIVITY; ARTICLE; BETA SHEET; CONTROLLED STUDY; DRUG STRUCTURE; ESCHERICHIA COLI; FUNGUS; FUSARIUM CULMORUM; FUSARIUM GRAMINEARUM; GENETIC DISTANCE; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; IN VITRO STUDY; IXODES RICINUS; LISTERIA FLEISCHMANNII; LISTERIA GRAYI; LISTERIA INNOCUA; LISTERIA MARTHII; LISTERIA MONOCYTOGENES; LISTERIA SEELIGERI; LISTERIA WELSHIMERI; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS; ANIMAL; BACTERIAL INFECTION; CELL CULTURE; EVOLUTION; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INNATE IMMUNITY; IXODES; METABOLISM; MYCOSIS; PROTEIN MOTIF; SPECIES DIFFERENCE;

ANIMALIA; ARTHROPODA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; EUKARYOTA; FUNGI; FUSARIUM; HEXAPODA; IXODES RICINUS; IXODIDA; LISTERIA MONOCYTOGENES; MAMMALIA; NEGIBACTERIA; PROTOZOA; PSEUDOMONAS AERUGINOSA; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS;

AMINO ACID MOTIFS; ANIMALS; BACTERIAL INFECTIONS; BIOLOGICAL EVOLUTION; CELLS, CULTURED; DEFENSINS; HOST-PATHOGEN INTERACTIONS; IMMUNITY, INNATE; INSECT PROTEINS; IXODES; MYCOSES; SPECIES SPECIFICITY;

EID: 84940052444     PISSN: 0145305X     EISSN: 18790089     Source Type: Journal    
DOI: 10.1016/j.dci.2015.08.001     Document Type: Article

References (61)

1. Ahn H.-s., Cho W., Kang S.-H., Ko S.-S., Park M.-S., Cho H., Lee K.-H. Design and synthesis of novel antimicrobial peptides on the basis of α helical domain of Tenecin 1, an insect defensin protein, and structure-activity relationship study. Peptides 2006, 27:640-648.
2. Anisimova M., Gascuel O. Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst. Biol. 2006, 55:539-552.
3. Bell-Sakyi L., Zweygarth E., Blouin E.F., Gould E.A., Jongejan F. Tick cell lines: tools for tick and tick-borne disease research. Trends Parasitol. 2007, 23:450-457.
4. Biernat B., Cieniuch S., Stanczak J. Detection of TBEV RNA in Ixodes ricinus ticks in north-eastern Poland. Ann. Agric. Environ. Med. 2014, 21:689-692.
5. Buchmann K. Evolution of innate immunity: clues from invertebrates via fish to mammals. Front. Immunol. 2014, 5:459.
6. Bulet P., Stocklin R. Insect antimicrobial peptides: structures, properties and gene regulation. Protein Pept. Lett. 2005, 12:3-11.
7. Bulet P., Stocklin R., Menin L. Anti-microbial peptides: from invertebrates to vertebrates. Immunol. Rev. 2004, 198:169-184.
8. Cabezas-Cruz A., Valdes J.J. Are ticks venomous animals?. Front. Zool. 2014, 11:47.
9. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 2000, 17:540-552.
10. Crippa M., Rais O., Gern L. Investigations on the mode and dynamics of transmission and infectivity of Borrelia burgdorferi sensu stricto and Borrelia afzelii in Ixodes ricinus ticks. Vector Borne Zoonotic Dis. 2002, 2:3-9.
11. De Samblanx G.W., Fernandez del Carmen A., Sijtsma L., Plasman H.H., Schaaper W.M., Posthuma G.A., Fant F., Meloen R.H., Broekaert W.F., van Amerongen A. Antifungal activity of synthetic 15-mer peptides based on the Rs-AFP2 (Raphanus sativus antifungal protein 2) sequence. Pept. Res. 1996, 9:262-268.
12. De Samblanx G.W., Goderis I.J., Thevissen K., Raemaekers R., Fant F., Borremans F., Acland D.P., Osborn R.W., Patel S., Broekaert W.F. Mutational analysis of a plant defensin from radish (Raphanus sativus L.) reveals two adjacent sites important for antifungal activity. J. Biol. Chem. 1997, 272:1171-1179.
13. Diego-Garcia E., Abdel-Mottaleb Y., Schwartz E.F., de la Vega R.C., Tytgat J., Possani L.D. Cytolytic and K+ channel blocking activities of beta-KTx and scorpine-like peptides purified from scorpion venoms. Cell Mol. Life Sci. 2008, 65:187-200.
14. Fogaça A.C., Lorenzini D.M., Kaku L.M., Esteves E., Bulet P., Daffre S. Cysteine-rich antimicrobial peptides of the cattle tick Boophilus microplus: isolation, structural characterization and tissue expression profile. Dev. Comp. Immunol. 2004, 28:191-200.
15. Galay R.L., Maeda H., Aung K.M., Umemiya-Shirafuji R., Xuan X., Igarashi I., Tsuji N., Tanaka T., Fujisaki K. Anti-babesial activity of a potent peptide fragment derived from longicin of Haemaphysalis longicornis. Trop. Anim. Health Prod. 2012, 44:343-348.
16. Ganz T., Lehrer R.I. Defensins. Curr. Opin. Immunol. 1994, 6:584-589.
17. Gao B., Zhu S. Identification and characterization of the parasitic wasp Nasonia defensins: positive selection targeting the functional region?. Dev. Comp. Immunol. 2010, 34:659-668.
18. Gillespie J.P., Kanost M.R., Trenczek T. Biological mediators of insect immunity. Annu. Rev. Entomol. 1997, 42:611-643.
19. Guindon S., Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 2003, 52:696-704.
20. Haase D., Rieger J.K., Witten A., Stoll M., Bornberg-Bauer E., Kalbe M., Reusch T.B. Specific gene expression responses to parasite genotypes reveal redundancy of innate immunity in vertebrates. PLoS One 2014, 9:e108001.
21. Hajdusek O., Sima R., Ayllon N., Jalovecka M., Perner J., de la Fuente J., Kopacek P. Interaction of the tick immune system with transmitted pathogens. Front. Cell Infect. Microbiol. 2013, 3:26.
22. Hazlett L., Wu M. Defensins in innate immunity. Cell Tissue Res. 2011, 343:175-188.
23. Hudson P.J., Norman R., Laurenson M.K., Newborn D., Gaunt M., Jones L., Reid H., Gould E., Bowers R., Dobson A. Persistence and transmission of tick-borne viruses: Ixodes ricinus and louping-ill virus in red grouse populations. Parasitology 1995, 111(Suppl. l):S49-S58.
24. Hynes W.L., Ceraul S.M., Todd S.M., Seguin K.C., Sonenshine D.E. A defensin-like gene expressed in the black-legged tick, Ixodes scapularis. Med. Vet. Entomol. 2005, 19:339-344.
25. Johns R., Sonenshine D.E., Hynes W.L. Identification of a defensin from the hemolymph of the American dog tick, Dermacentor variabilis. Insect Biochem. Mol. Biol. 2001, 31:857-865.
26. Katoh K., Standley D.M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 2013, 30:772-780.
27. Kembel S.W., Cowan P.D., Helmus M.R., Cornwell W.K., Morlon H., Ackerly D.D., Blomberg S.P., Webb C.O. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 2010, 26:1463-1464.
28. Kocan K.M., de la Fuente J., Manzano-Roman R., Naranjo V., Hynes W.L., Sonenshine D.E. Silencing expression of the defensin, varisin, in male Dermacentor variabilis by RNA interference results in reduced Anaplasma marginale infections. Exp. Appl. Acarol. 2008, 46:17-28.
29. Lai R., Lomas L.O., Jonczy J., Turner P.C., Rees H.H. Two novel non-cationic defensin-like antimicrobial peptides from haemolymph of the female tick, Amblyomma hebraeum. Biochem. J. 2004, 379:681-685.
30. Masso-Silva J.A., Diamond G. Antimicrobial peptides from fish. Pharm. (Basel) 2014, 7:265-310.
31. Miedaner T., Reinbrecht C., Schilling A.G. Association among aggressiveness, fungal colonization, and mycotoxin production of 26 isolates of Fusarium graminearum in winter rye head blight. Zeitsch Pflanzenkrank Pflanzenschutz 2000, 107:124-134.
32. Nakajima Y., Ishibashi J., Yukuhiro F., Asaoka A., Taylor D., Yamakawa M. Antibacterial activity and mechanism of action of tick defensin against Gram-positive bacteria. Biochim. Biophys. Acta 2003, 1624:125-130.
33. Nakajima Y., van der Goes van Naters-Yasui A., Taylor D., Yamakawa M. Two isoforms of a member of the arthropod defensin family from the soft tick, Ornithodoros moubata (Acari: Argasidae). Insect Biochem. Mol. Biol. 2001, 31:747-751.
34. Nakajima Y., van der Goes van Naters-Yasui A., Taylor D., Yamakawa M. Antibacterial peptide defensin is involved in midgut immunity of the soft tick, Ornithodoros moubata. Insect Mol. Biol. 2002, 11:611-618.
35. Nawrot R., Barylski J., Nowicki G., Broniarczyk J., Buchwald W., Gozdzicka-Jozefiak A. Plant antimicrobial peptides. Folia Microbiol. (Praha) 2014, 59:181-196.
36. Pichu S., Ribeiro J.M., Mather T.N. Purification and characterization of a novel salivary antimicrobial peptide from the tick, Ixodes scapularis. Biochem. Biophys. Res. Commun. 2009, 390:511-515.
37. Rahnamaeian M. Antimicrobial peptides: modes of mechanism, modulation of defense responses. Plant Signal Behav. 2011, 6:1325-1332.
38. Rahnamaeian M., Cytryńska M., Zdybicka-Barabas A., Dobslaff K., Wiesner J., Twyman R.M., Zuchner T., Sadd B.M., Regoes R.R., Schmid-Hempel P., Vilcinskas A. Insect antimicrobial peptides show potentiating functional interactions against Gram-negative bacteria. Proc. Biol. Sci. 2015, 282(1806):20150293. 10.1098/rspb.2015.0293.
39. Rahnamaeian M., Langen G., Imani J., Khalifa W., Altincicek B., von Wettstein D., Kogel K.H., Vilcinskas A. Insect peptide metchnikowin confers on barley a selective capacity for resistance to fungal ascomycetes pathogens. J. Exp. Bot. 2009, 60:4105-4114.
40. Rahnamaeian M., Vilcinskas A. Defense gene expression is potentiated in transgenic barley expressing antifungal peptide Metchnikowin throughout powdery mildew challenge. J. Plant Res. 2012, 125:115-124.
41. Rahnamaeian M., Vilcinskas A. Short antimicrobial peptides as cosmetic ingredients to deter dermatological pathogens. Appl. Microbiol. Biotechnol. 2015, (in press).
42. Rizzoli A., Silaghi C., Obiegala A., Rudolf I., Hubalek Z., Foldvari G., Plantard O., Vayssier-Taussat M., Bonnet S., Spitalska E., Kazimirova M. Ixodes ricinus and its transmitted pathogens in urban and peri-urban areas in Europe: new hazards and relevance for public health. Front. Public Health 2014, 2:251.
43. Romestand B., Molina F., Richard V., Roch P., Granier C. Key role of the loop connecting the two beta strands of mussel defensin in its antimicrobial activity. Eur. J. Biochem. 2003, 270:2805-2813.
44. Rudenko N., Golovchenko M., Grubhoffer L. Gene organization of a novel defensin of Ixodes ricinus: first annotation of an intron/exon structure in a hard tick defensin gene and first evidence of the occurrence of two isoforms of one member of the arthropod defensin family. Insect Mol. Biol. 2007, 16:501-507.
45. Sagaram U.S., Pandurangi R., Kaur J., Smith T.J., Shah D.M. Structure-activity determinants in antifungal plant defensins MsDef1 and MtDef4 with different modes of action against Fusarium graminearum. PLoS One 2011, 6:e18550.
46. Saito Y., Konnai S., Yamada S., Imamura S., Nishikado H., Ito T., Onuma M., Ohashi K. Identification and characterization of antimicrobial peptide, defensin, in the taiga tick, Ixodes persulcatus. Insect Mol. Biol. 2009, 18:531-539.
47. Schrödinger Schrödinger maestro package. Maestro, Version 9.9 2014, (New York, LLC).
48. Taylor D. Innate immunity in ticks: a review. J. Acarol. Soc. Jpn. 2006, 15:109-127.
49. Tonk M., Cabezas-Cruz A., Valdes J.J., Rego R., Chrudimska T., Strnad M., Ima R., Bell-Sakyi L., Franta Z.K., Vilcinskas A., Grubhoffer L., Rahnamaeian M. Defensins from the tick Ixodes scapularis are effective against phytopathogenic fungi and the human bacterial pathogen Listeria grayi. Parasit. Vectors 2014, 7:554.
50. Tonk M., Cabezas-Cruz A., Valdes J.J., Rego R.O., Rudenko N., Golovchenko M., Bell-Sakyi L., de la Fuente J., Grubhoffer L. Identification and partial characterisation of new members of the Ixodes ricinus defensin family. Gene 2014, 540:146-152.
51. Varkey J., Singh S., Nagaraj R. Antibacterial activity of linear peptides spanning the carboxy-terminal beta-sheet domain of arthropod defensins. Peptides 2006, 27:2614-2623.
52. Wang G. Human antimicrobial peptides and proteins. Pharmaceuticals (Basel) 2014, 7:545-594.
53. Wang J., Bian G., Pan W., Feng T., Dai J. Molecular characterization of a defensin gene from a hard tick, Dermacentor silvarum. Parasit. Vectors 2015, 8:25.
54. Wang Y., Zhu S. The defensin gene family expansion in the tick Ixodes scapularis. Dev. Comp. Immunol. 2011, 35:1128-1134.
55. Wiesner J., Vilcinskas A. Antimicrobial peptides: the ancient arm of the human immune system. Virulence 2010, 1:440-464.
56. Yount N.Y., Yeaman M.R. Multidimensional signatures in antimicrobial peptides. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:7363-7368.
57. Yu D., Sheng Z., Xu X., Li J., Yang H., Liu Z., Rees H.H., Lai R. A novel antimicrobial peptide from salivary glands of the hard tick, Ixodes sinensis. Peptides 2006, 27:31-35.
58. Zhang G., Sunkara L.T. Avian antimicrobial host defense peptides: from biology to therapeutic applications. Pharmaceuticals (Basel) 2014, 7:220-247.
59. Zhang H., Gao S., Lercher M.J., Hu S., Chen W.H. EvolView, an online tool for visualizing, annotating and managing phylogenetic trees. Nucleic Acids Res. 2012, 40:W569-W572.
60. Zhang Z.T., Zhu S.Y. Drosomycin, an essential component of antifungal defence in Drosophila. Insect Mol. Biol. 2009, 18:549-556.
61. Zheng H., Zhou L., Yang X., Wang D., Liu J. Cloning and characterization of a male-specific defensin-like antimicrobial peptide from the tick Haemaphysalis longicornis. Dev. Comp. Immunol. 2012, 37:207-211.