IrSPI, a Tick Serine Protease Inhibitor Involved in Tick Feeding and Bartonella henselae Infection

PLoS Neglected Tropical Diseases

Volumn 8, Issue 7, 2014, Pages

  Liu, Xiang Ye ^a   de la Fuente, Jose ^b,c   Cote, Martine ^a   Galindo, Ruth C ^c   Moutailler, Sara ^a   Vayssier Taussat, Muriel ^a   Bonnet, Sarah I ^a  

^a UNIVERSITÉ PARIS EST CRÉTEIL   (France)

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

^c OKLAHOMA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEFENSIN; HEAT SHOCK PROTEIN 20; HEAT SHOCK PROTEIN 70; METALLOPROTEINASE; SERINE PROTEINASE INHIBITOR; SPACER DNA; TRANSCRIPTOME;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; BACTERIAL GROWTH; BACTERIAL INFECTION; BACTERIAL TRANSMISSION; CAT SCRATCH DISEASE; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE EXPRESSION; GENE ONTOLOGY; GENE SILENCING; HIGH THROUGHPUT SEQUENCING; IXODES RICINUS; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PYROSEQUENCING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SALIVARY GLAND; TICK BORNE DISEASE; TICK INFESTATION; UPREGULATION; ANIMAL; BARTONELLA HENSELAE; BARTONELLOSIS; ENZYMOLOGY; FEEDING BEHAVIOR; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; TICK;

ANIMALS; BARTONELLA HENSELAE; BARTONELLA INFECTIONS; FEEDING BEHAVIOR; HOST-PATHOGEN INTERACTIONS; SALIVARY GLANDS; SERINE PROTEINASE INHIBITORS; TICKS; TRANSCRIPTOME;

EID: 84905483168     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0002993     Document Type: Article

References (57)

1. Parola P, Raoult D, (2001) Ticks and tickborne bacterial diseases in humans: an emerging infectious threat. Clin Infect Dis 32: 897-928.
2. Billeter SA, Levy MG, Chomel BB, Breitschwerdt EB, (2008) Vector transmission of Bartonella species with emphasis on the potential for tick transmission. Med Vet Entomol 22: 1-15.
3. Telford SR 3rd, Wormser GP, (2010) Bartonella spp. transmission by ticks not established. Emerg Infect Dis 16: 379-384.
4. Angelakis E, Billeter SA, Breitschwerdt EB, Chomel BB, Raoult D, (2010) Potential for tick-borne bartonelloses. Emerg Infect Dis 16: 385-391.
5. Cotte V, Bonnet S, Le Rhun D, Le Naour E, Chauvin A, et al. (2008) Transmission of Bartonella henselae by Ixodes ricinus. Emerg Infect Dis 14: 1074-1080.
6. Reis C, Cote M, Le Rhun D, Lecuelle B, Levin ML, et al. (2011) Vector competence of the tick Ixodes ricinus for transmission of Bartonella birtlesii. PLoS Negl Trop Dis 5: e1186.
7. Vayssier-Taussat M, Le Rhun D, Bonnet S, Cotte V, (2009) Insights in Bartonella host specificity. Ann N Y Acad Sci 1166: 127-132.
8. Merino O, Alberdi P, Perez de la Lastra JM, de la Fuente J, (2013) Tick vaccines and the control of tick-borne pathogens. Front Cell Infect Microbiol 3: 30.
9. Merino O, Antunes S, Mosqueda J, Moreno-Cid JA, Perez de la Lastra JM, et al. (2013) Vaccination with proteins involved in tick-pathogen interactions reduces vector infestations and pathogen infection. Vaccine 31: 5889-5896.
10. Andreotti R, Cunha RC, Soares MA, Guerrero FD, Leite FP, et al. (2012) Protective immunity against tick infestation in cattle vaccinated with recombinant trypsin inhibitor of Rhipicephalus microplus. Vaccine 30: 6678-6685.
11. Sojka D, Franta Z, Horn M, Caffrey CR, Mares M, et al. (2013) New insights into the machinery of blood digestion by ticks. Trends Parasitol 29: 276-285.
12. Andersen JF, (2010) Structure and mechanism in salivary proteins from blood-feeding arthropods. Toxicon 56: 1120-1129.
13. Wikel SK, (1999) Tick modulation of host immunity: an important factor in pathogen transmission. Int J Parasitol 29: 851-859.
14. Liu X, Bonnet S, (2014) Hard tick factors implicated in pathogen transmission. PLoS neglected tropical diseases 8: e2566.
15. Mulenga A, Sugimoto C, Onuma M, (2000) Issues in tick vaccine development: identification and characterization of potential candidate vaccine antigens. Microbes Infect 2: 1353-1361.
16. Schwarz A, von Reumont BM, Erhart J, Chagas AC, Ribeiro JM, et al. (2013) De novo Ixodes ricinus salivary gland transcriptome analysis using two next-generation sequencing methodologies. Faseb J 10.1096/fj.13-232140: Epub ahead of print.
17. Bonnet S, Jouglin M, Malandrin L, Becker C, Agoulon A, et al. (2007) Transstadial and transovarial persistence of Babesia divergens DNA in Ixodes ricinus ticks fed on infected blood in a new skin-feeding technique. Parasitology 134: 197-207.
18. Li H, Durbin R, (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
19. Stekel DJ, Git Y, Falciani F, (2000) The comparison of gene expression from multiple cDNA libraries. Genome Res 10: 2055-2061.
20. Romualdi C, Bortoluzzi S, D'Alessi F, Danieli GA, (2003) IDEG6: a web tool for detection of differentially expressed genes in multiple tag sampling experiments. Physiol Genomics 12: 159-162.
21. Schmittgen TD, Livak KJ, (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3: 1101-1108.
22. Kocan KM, Blouin E, de la Fuente J, (2011) RNA interference in ticks. J Vis Exp 10.3791/2474: e2427.
23. Houpikian P, Raoult D, (2001) 16S/23S rRNA intergenic spacer regions for phylogenetic analysis, identification, and subtyping of Bartonella species. J Clin Microbiol 39: 2768-2778.
24. Islam MK, Tsuji N, Miyoshi T, Alim MA, Huang X, et al. (2009) The Kunitz-like modulatory protein haemangin is vital for hard tick blood-feeding success. PLoS Pathog 5: e1000497.
25. Dai SX, Zhang AD, Huang JF, (2012) Evolution, expansion and expression of the Kunitz/BPTI gene family associated with long-term blood feeding in Ixodes Scapularis. BMC Evol Biol 12: 4.
26. Ceraul SM, Dreher-Lesnick SM, Mulenga A, Rahman MS, Azad AF, (2008) Functional characterization and novel rickettsiostatic effects of a Kunitz-type serine protease inhibitor from the tick Dermacentor variabilis. Infect Immun 76: 5429-5435.
27. Ceraul SM, Chung A, Sears KT, Popov VL, Beier-Sexton M, et al. (2011) A Kunitz protease inhibitor from Dermacentor variabilis, a vector for spotted fever group rickettsiae, limits Rickettsia montanensis invasion. Infect Immun 79: 321-329.
28. Kocan KM, de la Fuente J, Manzano-Roman R, Naranjo V, Hynes WL, et al. (2008) Silencing expression of the defensin, varisin, in male Dermacentor variabilis by RNA interference results in reduced Anaplasma marginale infections. Exp Appl Acarol 46: 17-28.
29. Couvreur B, Beaufays J, Charon C, Lahaye K, Gensale F, et al. (2008) Variability and action mechanism of a family of anticomplement proteins in Ixodes ricinus. PLoS One 3: e1400.
30. Daix V, Schroeder H, Praet N, Georgin JP, Chiappino I, et al. (2007) Ixodes ticks belonging to the Ixodes ricinus complex encode a family of anticomplement proteins. Insect Mol Biol 16: 155-166.
31. Deng H, Le Rhun D, Buffet JP, Cotte V, Read A, et al. (2012) Strategies of exploitation of mammalian reservoirs by Bartonella species. Vet Res 43: 15.
32. Ganz T, Lehrer RI, (1994) Defensins. Curr Opin Immunol 6: 584-589.
33. Chrudimska T, Slaninova J, Rudenko N, Ruzek D, Grubhoffer L, (2011) Functional characterization of two defensin isoforms of the hard tick Ixodes ricinus. Parasit Vectors 4: 63.
34. Matsuo T, Okoda Y, Badgar B, Inoue N, Xuan X, et al. (2004) Fate of GFP-expressing Escherichia coli in the midgut and response to ingestion in a tick, Ornithodoros moubata (Acari: Argasidae). Exp Parasitol 108: 67-73.
35. Nakajima Y, Saido-Sakanaka H, Taylor D, Yamakawa M, (2003) Up-regulated humoral immune response in the soft tick, Ornithodoros moubata (Acari: Argasidae). Parasitol Res 91: 476-481.
36. Jaworski DC, Zou Z, Bowen CJ, Wasala NB, Madden R, et al. (2010) Pyrosequencing and characterization of immune response genes from the American dog tick, Dermacentor variabilis (L.). Insect Mol Biol 19: 617-630.
37. 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.
38. McNally KL, Mitzel DN, Anderson JM, Ribeiro JM, Valenzuela JG, et al. (2012) Differential salivary gland transcript expression profile in Ixodes scapularis nymphs upon feeding or flavivirus infection. Ticks Tick Borne Dis 3: 18-26.
39. Fogaca AC, Lorenzini DM, Kaku LM, Esteves E, Bulet P, et al. (2004) Cysteine-rich antimicrobial peptides of the cattle tick Boophilus microplus: isolation, structural characterization and tissue expression profile. Dev Comp Immunol 28: 191-200.
40. Francischetti IM, My Pham V, Mans BJ, Andersen JF, Mather TN, et al. (2005) The transcriptome of the salivary glands of the female western black-legged tick Ixodes pacificus (Acari: Ixodidae). Insect Biochem Mol Biol 35: 1142-1161.
41. Tutar L, Tutar Y, (2010) Heat shock proteins; an overview. Curr Pharm Biotechnol 11: 216-222.
42. Villar M, Ayllon N, Busby AT, Galindo RC, Blouin EF, et al. (2010) Expression of Heat Shock and Other Stress Response Proteins in Ticks and Cultured Tick Cells in Response to Anaplasma spp. Infection and Heat Shock. Int J Proteomics 2010: 657261.
43. Busby AT, Ayllon N, Kocan KM, Blouin EF, de la Fuente G, et al. (2012) Expression of heat shock proteins and subolesin affects stress responses, Anaplasma phagocytophilum infection and questing behaviour in the tick, Ixodes scapularis. Med Vet Entomol 26: 92-102.
44. Anguita J, Ramamoorthi N, Hovius JW, Das S, Thomas V, et al. (2002) Salp15, an ixodes scapularis salivary protein, inhibits CD4(+) T cell activation. Immunity 16: 849-859.
45. Garg R, Juncadella IJ, Ramamoorthi N, Ashish, Ananthanarayanan SK, et al. (2006) Cutting edge: CD4 is the receptor for the tick saliva immunosuppressor, Salp15. J Immunol 177: 6579-6583.
46. Juncadella IJ, Garg R, Ananthnarayanan SK, Yengo CM, Anguita J, (2007) T-cell signaling pathways inhibited by the tick saliva immunosuppressor, Salp15. FEMS Immunol Med Microbiol 49: 433-438.
47. Hovius JW, Schuijt TJ, de Groot KA, Roelofs JJ, Oei GA, et al. (2008) Preferential protection of Borrelia burgdorferi sensu stricto by a Salp15 homologue in Ixodes ricinus saliva. J Infect Dis 198: 1189-1197.
48. Ramamoorthi N, Narasimhan S, Pal U, Bao F, Yang XF, et al. (2005) The Lyme disease agent exploits a tick protein to infect the mammalian host. Nature 436: 573-577.
49. Mori A, Konnai S, Yamada S, Hidano A, Murase Y, et al. (2010) Two novel Salp15-like immunosuppressant genes from salivary glands of Ixodes persulcatus Schulze tick. Insect Mol Biol 19: 359-365.
50. Flower DR, North AC, Attwood TK, (1993) Structure and sequence relationships in the lipocalins and related proteins. Protein Sci 2: 753-761.
51. Flower DR, (1996) The lipocalin protein family: structure and function. Biochem J 318 (Pt 1):: 1-14.
52. Paesen GC, Adams PL, Harlos K, Nuttall PA, Stuart DI, (1999) Tick histamine-binding proteins: isolation, cloning, and three-dimensional structure. Mol Cell 3: 661-671.
53. Francischetti IM, Mather TN, Ribeiro JM, (2003) Cloning of a salivary gland metalloprotease and characterization of gelatinase and fibrin(ogen)lytic activities in the saliva of the Lyme disease tick vector Ixodes scapularis. Biochem Biophys Res Commun 305: 869-875.
54. Decrem Y, Mariller M, Lahaye K, Blasioli V, Beaufays J, et al. (2008) The impact of gene knock-down and vaccination against salivary metalloproteases on blood feeding and egg laying by Ixodes ricinus. Int J Parasitol 38: 549-560.
55. Harnnoi T, Sakaguchi T, Nishikawa Y, Xuan X, Fujisaki K, (2007) Molecular characterization and comparative study of 6 salivary gland metalloproteases from the hard tick, Haemaphysalis longicornis. Comp Biochem Physiol B Biochem Mol Biol 147: 93-101.
56. Barnard AC, Nijhof AM, Gaspar AR, Neitz AW, Jongejan F, et al. (2012) Expression profiling, gene silencing and transcriptional networking of metzincin metalloproteases in the cattle tick, Rhipicephalus (Boophilus) microplus. Vet Parasitol 186: 403-414.
57. Maritz-Olivier C, Stutzer C, Jongejan F, Neitz AW, Gaspar AR, (2007) Tick anti-hemostatics: targets for future vaccines and therapeutics. Trends Parasitol 23: 397-407.