Defensins from the tick Ixodes scapularis are effective against phytopathogenic fungi and the human bacterial pathogen Listeria grayi

Parasites and Vectors

Volumn 7, Issue 1, 2014, Pages

  Tonk, Miray ^a,b   Cabezas Cruz, Alejandro ^c,d   Valdés, James J ^a   Rego, Ryan O M ^a   Chrudimská, Tereza ^a,b   Strnad, Martin ^a,b   Šíma, Radek ^a   Bell Sakyi, Lesley ^e   Franta, Zdeněk ^f   Vilcinskas, Andreas ^f,g   Grubhoffer, Libor ^a,b   Rahnamaeian, Mohammad ^f,g  

^a INSTITUTE OF PARASITOLOGY   (Czech Republic)

^b UNIVERSITY OF SOUTH BOHEMIA   (Czech Republic)

^c INSTITUTO DE INVESTIGACIÓN EN RECURSOS CINEGÉTICOS IREC CSIC UCLM JCCM   (Spain)

^d UNIV LILLE   (France)

^e INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

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

^g JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Antimicrobial peptide; Defensin; Fusarium spp; Ixodes scapularis; Listeria grayi; Tick cell line

Indexed keywords

DEFENSIN; SCAPULARISIN 3; SCAPULARISIN 6; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT;

ANIMAL CELL; ANTIBIOTIC RESISTANCE; ANTIFUNGAL ACTIVITY; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; ESCHERICHIA COLI; FUNGUS; FUSARIUM CULMORUM; FUSARIUM GRAMINEARUM; GENE EXPRESSION; IC50; IN VITRO STUDY; INNATE IMMUNITY; IXODES SCAPULARIS; LISTERIA GRAYI; MIDGUT; NONHUMAN; PEPTIDE SYNTHESIS; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; PSEUDOMONAS AERUGINOSA; SALIVARY GLAND; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS; STRUCTURE ANALYSIS; TICK; TISSUE SPECIFICITY; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECTS; FUSARIUM; GUINEA PIG; HUMAN; ISOLATION AND PURIFICATION; IXODES; LISTERIA; MICROBIAL SENSITIVITY TEST; PROTEIN CONFORMATION; SYNTHESIS;

ANIMALS; ANTI-INFECTIVE AGENTS; DEFENSINS; FUSARIUM; GUINEA PIGS; HUMANS; IXODES; LISTERIA; MICROBIAL SENSITIVITY TESTS; MODELS, MOLECULAR; PROTEIN CONFORMATION; STAPHYLOCOCCUS EPIDERMIDIS;

EID: 84964696429     PISSN: None     EISSN: 17563305     Source Type: Journal    
DOI: 10.1186/s13071-014-0554-y     Document Type: Article

References (60)

1. Hajdušek O, Šíma R, Ayllón N, Jalovecká M, Perner J, de la Fuente J, Kopacek P: Interaction of the tick immune system with transmitted pathogens. Front Cell Infec Microbio 2013, 3:26.
2. Taylor D: Innate immunity in ticks: a review. J Acarol Soc Japan 2006, 15:109-127.
3. Kopáček P, Hajdušek O, Burešová V, Daffre S: Tick innate immunity. Adv Exp Med Biol 2010, 708:137-162. Review.
4. Nakajima Y, van Naters-Yasui AV, Taylor D, Yamakawa M: Antimicrobial peptide defensin is involved in midgut immunity of the soft tick, Ornithodoros moubata. Insect Mol Biol 2002, 11:611-618.
5. Wang Y, Zhu S: The defensin gene family expansion in the tick Ixodes scapularis. Dev Comp Immunol 2011, 35:1128-1134.
6. Ganz T, Lehrer RI: Defensins. Curr Opin Immunol 1994, 6:584-589.
7. Lai R, Lomas LO, Jonczy J, Turner PC, Ress HH: Two novel non-cationic defensin-like antimicrobial peptides from haemolymph of the female tick, Amblyomma hebraeum. Biochem J 2004, 379:681-685.
8. Tonk M, Cabezas-Cruz A, Valdés JJ, Rego ROM, 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.
9. Bulet P, Stöcklin R, Menin L: Anti-microbial peptides: from invertebrates to vertebrates. Immunol Rev 2004, 198:169-184.
10. Kocan KM, de la Fuente J, Manzano-Roman R, Naranjo V, Hynes WL, Sonenshine DE: 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.
11. Pasupuleti M, Schmidtchen A, Malmsten M: Antimicrobial peptides: key components of the innate immune system. Crit Rev Biotechnol 2012, 32:143-171.
12. Bajard S, Rosso L, Fardel G, Flandrois JP: The particular behaviour of Listeria monocytogenes under sub-optimal conditions. Int J Food Microbiol 1996, 29:201-211.
13. Farber JM, Peterkin PI: Listeria monocytogenes, a food-borne pathogen. Microbiol Rev 1991, 55:476-511.
14. Hage E, Mpamugo O, Ohai C, Sapkota S, Swift C, Wooldridge D, Amar CFL: Identification of six Listeria species by real-time PCR assay. Lett Appl Microbiol 2014, 58(6):535-540.
15. Garrity GM, Bell JA, Lilburn TG: Taxonomic Outline of the Prokaryotes. Bergey's Manual of Systematic Bacteriology. 2. New York: Springer; 2004.
16. Liu D: Identification, subtyping and virulence determination of Listeria monocytogenes, an important foodborne pathogen. J Med Microbiol 2006, 55:645-659.
17. Graves LM, Helsel LO, Steigerwalt AG, Morey RE, Daneshvar MI, Roof SE, Orsi RH, Fortes ED: Listeria marthii sp. nov., isolated fromthe natural environment, Finger Lakes National Forest. Int J Syst Evol Microbiol 2010, 60:1280-1288.
18. Leclercq A, Clermont D, Bizet C, Grimont PAD, Le Fléche-Matéos A, Roche SM, Buchrieser C, Cadet-Daniel V: Listeria rocourtiae sp. nov. Int J Syst Evol Microbiol 2010, 60:2210-2214.
19. Bertsch D, Rau J, Eugster MR, Haug MC, Lawson PA, Lacroix C, Meile L: Listeria fleischmannii sp. nov., isolated from cheese. Int J Syst Evol Microbiol 2013, 63:526-532.
20. Lang HE, Neuhaus K, Scherer S: Listeria weihenstephanensis sp. nov., isolated from the water plant Lemna trisulca taken from a freshwater pond. Int J Syst Evol Microbiol 2013, 63:641-647.
21. Cummins AJ, Fielding AK, McLauchlin J: Listeria ivanovii infection in a patient with AIDS. J Infect 1994, 28:89-91.
22. Lessing MPA, Curtis GDW, Bowler ICJ: Listeria ivanovii infection. J Infect 1994, 29:230-231.
23. Guillet C, Join-Lambert O, Le Monnier A, Leclercq A, Mechai F, Mamzer-Bruneel MF, Bielecka MK, Scortti M: Human listeriosis caused by Listeria ivanovii. Emerg Infect Dis 2010, 16:136-138.
24. Rapose A, Lick SD, Ismail N: Listeria grayi bacteremia in a heart transplant recipient. Transpl Infect Dis 2008, 10:434-436.
25. Rocourt J, Hof H, Schrettenbrunner A, Malinverni R, Bille J: Acute purulent Listeria seeligeri meningitis in an immunocompetent adult. Schweiz Med Wochenschr 1986, 116:248-251.
26. Perrin M, Bemer M, Delamare C: Fatal case of Listeria innocua bacteremia. J Clin Microbiol 2003, 41:5308-5309.
27. Walker JK, Morgan JH, McLauchlin J, Grant KA, Shallcross JA: Listeria innocua isolated from a case of ovine meningoencephalitis. Vet Microbiol 1994, 42:245-253.
28. Salimnia H, Patel D, Lephart PR, Fairfax MR, Chandrasekar PH: Listeria grayi: vancomycin-resistant, gram-positive rod causing bacteremia in a stem celll transplant recipient. Transp Infect Dis 2010, 12:526-528.
29. Lucas S, Baştaş K, Budak H: Exploring the interaction between small RNAs and R genes during Brachypodium response to Fusarium culmorum infection. Gene 2014, 536:254-264.
30. Scherm B, Virgilio BS, Francesca S, Giovanna P, Giovanna D, Matias P, Quirico M: Fusarium culmorum: causal agent of foot and root rot and head blight on wheat. Molec Plant Pathol 2013, 14:323-341.
31. Bormann J, Boenisch MJ, Brückner E, Firat D, Schäfer W: The adenylyl cyclase plays a regulatory role in the morphogenetic switch from vegetative to pathogenic lifestyle of Fusarium graminearum on wheat. PLoS ONE 2014, 9:e91135.
32. Pagnussatt FA, Del Ponte EM, Garda-Buffon J, Badiale-Furlong E: Inhibition of Fusarium graminearum growth and mycotoxin production by phenolic extract from Spirulina sp. Pestic Biochem Physiol 2014, 108:21-26.
33. Ward TJ, Clear RM, Rooney AP, O'Donnell K, Gaba D, Patrick S, Starkey DE, Gilbert J, Geiser DM, Nowicki TW: An adaptive evolutionary shift in Fusarium head blight pathogen populations is driving the rapid spread of more toxigenic Fusarium graminearum in North America. Fungal Genet Biol 2008, 45:473-484.
34. Rahnamaeian M, Langen G, Imani J, Khalifa W, Altincicek B, von Wettstein D: Insect peptide metchnikowin confers on barley a selective capacity for resistance to fungal ascomycetes pathogens. J Exp Bot 2009, 60:4105-4114.
35. Miedaner T, Reinbrecht C, Schilling AG: 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.
36. 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.
37. Fogaça AC, Lorenzini DM, Kaku LM, 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.
38. Kurtti TJ, Munderloh UG, Andreadis TG, Magnarelli LA, Mather TN: Tick cell culture isolation of an intracellular prokaryote from the tick Ixodes scapularis. J Invert Pathol 1996, 67:318-321.
39. Munderloh UG, Liu Y, Wang M, Chen C, Kurtti TJ: Establishment, maintenance and description of cell lines from the tick Ixodes scapularis. J Parasitol 1994, 80:533-543.
40. Bell-Sakyi L, Zweygarth E, Blouin EF, Gould EA, Jongejan F: Tick cell lines: tools for tick and tick-borne disease research. Trends Parasitol 2007, 23:450-457.
41. Kelley LA, Sternberg MJE: Protein structure prediction on the Web: a case study using the Phyre server. Nat Protocols 2009, 4:363-371.
42. Li X, Jacobson MP, Zhu K, Zhao S, Friesner RA: Assignment of polar states for protein amino acid residues using an interaction cluster decomposition algorithm and its application to high resolution protein structure modeling. Proteins Struct Funct Bioinformatics 2007, 66:824-837.
43. Landon C, Barbault F, Legrain M, Guenneugues M, Vovelle F: Rational design of peptides active against the gram positive bacteria Staphylococcus aureus. Proteins 2008, 72:229-239.
44. Chrudimská T, Chrudimsky' T, Golovchenko M, Rudenko N, Grubhoffer L: New defensins from hard and soft ticks: similarities, differences, and phylogenetic analyses. Vet Parasitol 2010, 167:298-303.
45. Saito Y, Konnai S, Yamada S, Imamura S, Nishikado H, Ito T, Onuma M, Ohashi K: Identification and characterisation of antimicrobial peptide, defensin, in the taiga tick, Ixodes persulcatus. Insect Mol Biol 2009, 18:531-539.
46. Yu D, Sheng Z, Xu X, Li J, Yang H, Liu Z, Rees HH, Lai R: A novel antimicrobial peptide from salivary glands of the hard tick, Ixodes sinensis. Peptides 2006, 27:31-35.
47. Lu X, Che Q, Lv Y, Wang M, Lu Z, Feng F, Liu J, Yu H: A novel defensin-like peptide from salivary glands of the hard tick, Haemaphysalis longicornis. Protein Sci 2010, 19:392-397.
48. Nakajima Y, van Naters-Yasui AV, 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.
49. Tsuji N, Battsetseg B, Boldbaatar D, Miyoshi T, Xuan X, Oliver JH Jr, Fujisaki K: Babesial vector tick defensin against Babesia sp. parasites. Infect Immun 2007, 75:3633-3640.
50. Schwaiger K, Schmied EM, Bauer J: Comparative analysis on antibiotic resistance characteristics of Listeria spp. and Enterococcus spp. isolated from laying hens and eggs in conventional and organic keeping systems in Bavaria, Germany. Zoonoses Pub Hlth 2009, 57:171-180.
51. Mukherjee K, Abu Mraheil M, Silva S, Müller D, Cemic F, Hemberger J, Hain T, Vilcinskas A, Chakraborty T: Anti-Listeria activities of Galleria mellonella hemolymph proteins. Appl Env Microbiol 2011, 77:4237-4240.
52. Nielsen LK, Cook DJ, Edwards SG, Ray RV: The prevalence and impact of Fusarium head blight pathogens and mycotoxins on malting barley quality in UK. Int J Food Microbiol 2014, 28(179C):38-49.
53. Dean R, Van Kan JA, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J, Foster GD: The Top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 2012, 13:414-430.
54. Li Z, Zhou M, Zhang Z, Ren L, Du L, Zhang B, Xu H, Xin Z: Expression of a radish defensin in transgenic wheat confers increased resistance to Fusarium graminearum and Rhizoctonia cerealis. Funct Integr Genomics 2011, 11:63-70.
55. Gomes VM, Carvalho AO, Da Cunha M, Keller MN, Bloch C Jr, Deolindo P, Alves EW: Purification and characterization of a novel peptide with antifungal activity from Bothrops jararaca venom. Toxicon 2005, 45:817-827.
56. Dracatos PM, van der Weerden NL, Carroll KT, Johnson ED, Plummer KM, Anderson MA: Inhibition of cereal rust fungi by both class I and II defensins derived from the flowers of Nicotiana alata. Mol Plant Pathol 2014, 15:67-79.
57. Kolar SS, Baidouri H, Hanlon S, McDermott AM: Protective role of murine β-defensins 3 and 4 and cathelin-related antimicrobial peptide in Fusarium solani keratitis. Infect Immun 2013, 81:2669-2677.
58. Sagaram US, Pandurangi R, Kaur J, Smith TJ, Shah DM: Structure-activity determinants in antifungal plant defensins MsDef1 and MtDef4 with different modes of action against Fusarium graminearum. PLoS ONE 2011, 6:e18550.
59. Rahnamaeian M: Antimicrobial peptides: modes of mechanism, modulation of defense responses. Plant Signal Behav 2011, 6(9):1325-1332.
60. Hynes WL, Ceraul SM, Todd SM, Seguin KC, Sonenshine DE: A defensin-like gene expressed in the black-legged tick. Ixodes scapularis. Med Vet Entomol 2005, 19(4):339-344.