Identification of salivary antigenic markers discriminating host exposition between two European ticks: Rhipicephalus sanguineus and Dermacentor reticulatus

Comparative Immunology, Microbiology and Infectious Diseases

Volumn 36, Issue 1, 2013, Pages 39-53

  Vu Hai, Vinh ^a,b   Almeras, Lionel ^a,b   Audebert, Stephane ^c   Pophillat, Matthieu ^d   Boulanger, Nathalie ^e   Parola, Philippe ^a   Raoult, Didier ^a   Pages, Frederic ^a,f  

^a AIX MARSEILLE UNIVERSITÉ   (France)

^b INSTITUT DE RECHERCHE BIOMÉDICALE DES ARMÉES   (France)

^c AIX MARSEILLE UNIVERSITY   (France)

^d CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^e UNIVERSITÉ DE STRASBOURG   (France)

^f CIRE ARS Océan Indien   (France)

Author keywords

Dermacentor reticulatus; Exposure markers; Rhipicephalus sanguineus; Salivary antigens; Tick borne diseases; Vaccine candidates

Indexed keywords

BIOLOGICAL MARKER; IMMUNOGLOBULIN G ANTIBODY; INSECT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIGEN DETECTION; ARTICLE; CONTROLLED STUDY; DERMACENTOR RETICULATUS; DISEASE CARRIER; FEMALE; IMMUNOBLOTTING; NONHUMAN; PROTEIN ANALYSIS; RABBIT; RHIPICEPHALUS SANGUINEUS; SALIVA ANALYSIS; TICK BITE; TICK BORNE DISEASE;

ANIMALS; ANTIGENS; BITES AND STINGS; DERMACENTOR; FEMALE; IMMUNOGLOBULIN G; KINETICS; RABBITS; RHIPICEPHALUS SANGUINEUS; SALIVARY PROTEINS AND PEPTIDES;

DERMACENTOR RETICULATUS; IXODIDA; MAMMALIA; ORYCTOLAGUS CUNICULUS; RHIPICEPHALUS SANGUINEUS;

EID: 84871060516     PISSN: 01479571     EISSN: 18781667     Source Type: Journal    
DOI: 10.1016/j.cimid.2012.09.003     Document Type: Article

References (74)

1. Raoult D., Parola P. Rickettsial diseases 2007, Informa Healthcare USA, Inc., New York.
2. Steen N.A., Barker S.C., Alewood P.F. Proteins in the saliva of the Ixodida (ticks): pharmacological features and biological significance. Toxicon 2006, 47(1):1-20.
3. Francischetti I.M., Sa-Nunes A., Mans B.J., Santos I.M., Ribeiro J.M. The role of saliva in tick feeding. Frontiers in Bioscience 2009, 14:2051-2088.
4. Anatriello E., Ribeiro J.M., de Miranda-Santos I.K., Brandao L.G., Anderson J.M., Valenzuela J.G., et al. An insight into the sialotranscriptome of the brown dog tick, Rhipicephalus sanguineus. BMC Genomics 2010, 11:450.
5. Bowman A.S., Nuttall P.A. Ticks: biology, disease and control 2008, Cambridge University Press.
6. Alarcon-Chaidez F., Ryan R., Wikel S., Dardick K., Lawler C., Foppa I.M., et al. Confirmation of tick bite by detection of antibody to Ixodes calreticulin salivary protein. Clinical and Vaccine Immunology 2006, 13(11):1217-1222.
7. Schwartz B.S., Ford D.P., Childs J.E., Rothman N., Thomas R.J. Anti-tick saliva antibody: a biologic marker of tick exposure that is a risk factor for Lyme disease seropositivity. American Journal of Epidemiology 1991, 134(1):86-95.
8. Jaworski D.C., Rosell R., Coons L.B., Needham G.R. Tick (Acari: Ixodidae) attachment cement and salivary gland cells contain similar immunoreactive polypeptides. Journal of Medical Entomology 1992, 29(2):305-309.
9. Sanders M.L., Glass G.E., Scott A.L., Schwartz B.S. Kinetics and cross-species comparisons of host antibody responses to lone star ticks and American dog ticks (Acari: Ixodidae). Journal of Medical Entomology 1998, 35(5):849-856.
10. Almazan C., Kocan K.M., Bergman D.K., Garcia-Garcia J.C., Blouin E.F., de la Fuente J. Identification of protective antigens for the control of Ixodes scapularis infestations using cDNA expression library immunization. Vaccine 2003, 21(13-14):1492-1501.
11. Carreon D., de la Lastra J.M., Almazan C., Canales M., Ruiz-Fons F., Boadella M., et al. Vaccination with BM86, subolesin and akirin protective antigens for the control of tick infestations in white tailed deer and red deer. Vaccine 2012, 30(2):273-279.
12. de la Fuente J., Almazan C., Canales M., Perez de la Lastra J.M., Kocan K.M., Willadsen P. A ten-year review of commercial vaccine performance for control of tick infestations on cattle. Animal Health Research Reviews 2007, 8(1):23-28.
13. de V.S., Zeinstra L., Taoufik O., Willadsen P., Jongejan F. Evidence for the utility of the Bm86 antigen from Boophilus microplus in vaccination against other tick species. Experimental and Applied Acarology 2001, 25(3):245-261.
14. Perez-Perez D., Bechara G.H., Machado R.Z., Andrade G.M., Del Vecchio R.E., Pedroso M.S., et al. Efficacy of the Bm86 antigen against immature instars and adults of the dog tick Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae). Veterinary Parasitology 2010, 167(2-4):321-326.
15. Prevot P.P., Couvreur B., Denis V., Brossard M., Vanhamme L., Godfroid E. Protective immunity against Ixodes ricinus induced by a salivary serpin. Vaccine 2007, 25(17):3284-3292.
16. You M.J. Immunization effect of recombinant P27/30 protein expressed in Escherichia coli against the hard tick Haemaphysalis longicornis (Acari: Ixodidae) in rabbits. Korean Journal of Parasitology 2004, 42(4):195-200.
17. Imamura S., Namangala B., Tajima T., Tembo M.E., Yasuda J., Ohashi K., et al. Two serine protease inhibitors (serpins) that induce a bovine protective immune response against Rhipicephalus appendiculatus ticks. Vaccine 2006, 24(13):2230-2237.
18. Yamada S., Konnai S., Imamura S., Ito T., Onuma M., Ohashi K. Cloning and characterization of Rhipicephalus appendiculatus voraxinalpha and its effect as anti-tick vaccine. Vaccine 2009, 27(43):5989-5997.
19. You M., Fujisaki K. Vaccination effects of recombinant chitinase protein from the hard tick Haemaphysalis longicornis (Acari: Ixodidae). Journal of Veterinary Medical Science 2009, 71(6):709-712.
20. Nuttall P.A., Trimnell A.R., Kazimirova M., Labuda M. Exposed and concealed antigens as vaccine targets for controlling ticks and tick-borne diseases. Parasite Immunology 2006, 28(4):155-163.
21. Almazan C., Lagunes R., Villar M., Canales M., Rosario-Cruz R., Jongejan F., et al. Identification and characterization of Rhipicephalus (Boophilus) microplus candidate protective antigens for the control of cattle tick infestations. Parasitology Research 2010, 106(2):471-479.
22. Garcia-Varas S., Manzano-Roman R., Fernandez-Soto P., Encinas-Grandes A., Oleaga A., Perez-Sanchez R. Purification and characterisation of a P-selectin-binding molecule from the salivary glands of Ornithodoros moubata that induces protective anti-tick immune responses in pigs. International Journal for Parasitology 2010, 40(3):313-326.
23. Sahibi H., Rhalem A., Barriga O.O. Comparative immunizing power of infections, salivary extracts, and intestinal extracts of Hyalomma marginatum marginatum in cattle. Veterinary Parasitology 1997, 68(4):359-366.
24. Xu Y., Bruno J.F., Luft B.J. Identification of novel tick salivary gland proteins for vaccine development. Biochemical and Biophysical Research Communications 2005, 326(4):901-904.
25. Dantas-Torres F. The brown dog tick, Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae): from taxonomy to control. Veterinary Parasitology 2008, 152(3-4):173-185.
26. Parola P., Paddock C.D., Raoult D. Tick-borne rickettsioses around the world: emerging diseases challenging old concepts. Clinical Microbiology Reviews 2005, 18(4):719-756.
27. Szabo M.P., Bechara G.H. Sequential histopathology at the Rhipicephalus sanguineus tick feeding site on dogs and guinea pigs. Experimental and Applied Acarology 1999, 23(11):915-928.
28. Inokuma H., Mukai M., Ohno K., Yamamoto Y., Takahashi S., Onishi T. Duration of antibodies against 24 kD protein of Rhipicephalus sanguineus extract in dogs infested with the adult ticks. Journal of Veterinary Medical Science 1999, 61(2):179-181.
29. Inokuma H., Ohno K., Onishi T. Is the detection of anti-Rhipicephalus sanguineus (Rs24p) antibodies a valuable epidemiological tool of tick infestation in dogs?. Veterinary Research 2000, 31(3):365-369.
30. Nebreda M.T., Merino F.J., Serrano J.L., Fernandez-Soto P., Encinas A., Perez-Sanchez R. Detection of antibodies to tick salivary antigens among patients from a region of Spain. European Journal of Epidemiology 2004, 19(1):79-83.
31. Parola P., Rovery C., Rolain J.M., Brouqui P., Davoust B., Raoult D. Rickettsia slovaca and R. raoultii in tick-borne Rickettsioses. Emerging Infectious Diseases 2009, 15(7):1105-1108.
32. Socolovschi C., Mediannikov O., Raoult D., Parola P. Update on tick-borne bacterial diseases in Europe. Parasite 2009, 16(4):259-273.
33. Kubes M., Fuchsberger N., Labuda M., Zuffova E., Nuttall P.A. Salivary gland extracts of partially fed Dermacentor reticulatus ticks decrease natural killer cell activity in vitro. Immunology 1994, 82(1):113-116.
34. Hajnicka V., Vancova I., Kocakova P., Slovak M., Gasperik J., Slavikova M., et al. Manipulation of host cytokine network by ticks: a potential gateway for pathogen transmission. Parasitology 2005, 130(3):333-342.
35. Almeras L., Fontaine A., Belghazi M., Bourdon S., Boucomont-Chapeaublanc E., Orlandi-Pradines E., et al. Salivary gland protein repertoire from Aedes aegypti mosquitoes. Vector-Borne and Zoonotic Diseases 2010, 10(4):391-402.
36. Almeras L., Orlandi-Pradines E., Fontaine A., Villard C., Boucomont E., de Senneville L.D., et al. Sialome individuality between Aedes aegypti colonies. Vector-Borne and Zoonotic Diseases 2009, 9(5):531-541.
37. Fontaine A., Pascual A., Diouf I., Bakkali N., Bourdon S., Fusai T., et al. Mosquito salivary gland protein preservation in the field for immunological and biochemical analysis. Parasites & Vectors 2011, 4:33.
38. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227(5259):680-685.
39. Fontaine A., Pophillat M., Bourdon S., Villard C., Belghazi M., Fourquet P., et al. Specific antibody responses against membrane proteins of erythrocytes infected by Plasmodium falciparum of individuals briefly exposed to malaria. Malaria Journal 2010, 9:276.
40. Lefranc D., Almeras L., Dubucquoi S., de S.J., Vermersch P., Prin L. Distortion of the self-reactive IgG antibody repertoire in multiple sclerosis as a new diagnostic tool. Journal of Immunology 2004, 172(1):669-678.
41. Torrentino-Madamet M., Almeras L., Desplans J., Le P.Y., Belghazi M., Pophillat M., et al. Global response of Plasmodium falciparum to hyperoxia: a combined transcriptomic and proteomic approach. Malaria Journal 2011, 10:4.
42. Sauer J.R., Essenberg R.C., Bowman A.S. Salivary glands in ixodid ticks: control and mechanism of secretion. Journal of Insect Physiology 2000, 46(7):1069-1078.
43. Till W.M. A contribution to the anatomy and histology of the brown ear tick Rhipicephalus appendiculatus Neumann. Memoirs of the Entomological Society of Southern Africa 1961, 6:1-124.
44. Almeras L., Lefranc D., Drobecq H., de S.J., Dubucquoi S., Vermersch P., et al. New antigenic candidates in multiple sclerosis: identification by serological proteome analysis. Proteomics 2004, 4(7):2184-2194.
45. Beugnet F., Marie J.L. Emerging arthropod-borne diseases of companion animals in Europe. Veterinary Parasitology 2009, 163(4):298-305.
46. Parola P., Raoult D. Ticks and tickborne bacterial diseases in humans: an emerging infectious threat. Clinical Infectious Diseases 2001, 32(6):897-928.
47. Inokuma H., Aita T., Ohno K., Onishi T. Effects of infestation by Rhipicephalus sanguineus on lymphocyte blastogenic responses to mitogens in dogs. Journal of Veterinary Medical Science 1998, 60(9):1013-1016.
48. Ruzek D., Yakimenko V.V., Karan L.S., Tkachev S.E. Omsk haemorrhagic fever. Lancet 2010, 376(9758):2104-2113.
49. Mans B.J., Neitz A.W. Adaptation of ticks to a blood-feeding environment: evolution from a functional perspective. Insect Biochemisry and Molecular Biology 2004, 34(1):1-17.
50. Gao J., Luo J., Fan R., Guan G., Ren Q., Ma M., et al. Molecular characterization of a myosin alkali light chain-like protein, a " concealed" antigen from the hard tick Haemaphysalis qinghaiensis. Veterinary Parasitology 2007, 147(1-2):140-149.
51. Gao J., Luo J., Fan R., Schulte-Spechtel U.C., Fingerle V., Guan G., et al. Characterization of a concealed antigen Hq05 from the hard tick Haemaphysalis qinghaiensis and its effect as a vaccine against tick infestation in sheep. Vaccine 2009, 27(3):483-490.
52. Kotsyfakis M., Anderson J.M., Andersen J.F., Calvo E., Francischetti I.M., Mather T.N., et al. Cutting edge: Immunity against a " silent" salivary antigen of the Lyme vector Ixodes scapularis impairs its ability to feed. Journal of Immunology 2008, 181(8):5209-5212.
53. Decrem Y., Mariller M., Lahaye K., Blasioli V., Beaufays J., Zouaoui B.K., et al. The impact of gene knock-down and vaccination against salivary metalloproteases on blood feeding and egg laying by Ixodes ricinus. International Journal for Parasitology 2008, 38(5):549-560.
54. Sanders M.L., Jaworski D.C., Sanchez J.L., DeFraites R.F., Glass G.E., Scott A.L., et al. Antibody to a cDNA-derived calreticulin protein from Amblyomma americanum as a biomarker of tick exposure in humans. American Journal of Tropical Medicine and Hygiene 1998, 59(2):279-285.
55. Sanders M.L., Glass G.E., Nadelman R.B., Wormser G.P., Scott A.L., Raha S., et al. Antibody levels to recombinant tick calreticulin increase in humans after exposure to Ixodes scapularis (Say) and are correlated with tick engorgement indices. American Journal of Epidemiology 1999, 149(8):777-784.
56. Tian Z., Liu G., Zhang L., Yin H., Wang H., Xie J., et al. Identification of the heat shock protein 70 (HLHsp70) in Haemaphysalis longicornis. Veterinary Parasitology 2011, 181(2-4):282-290.
57. Brown S.J., Shapiro S.Z., Askenase P.W. Characterization of tick antigens inducing host immune resistance, I. Immunization of guinea pigs with Amblyomma americanum-derived salivary gland extracts and identification of an important salivary gland protein antigen with guinea pig anti-tick antibodies. Journal of Immunology 1984, 133(6):3319-3325.
58. Harnnoi T., Watchabunsook S., Sakaguchi T., Xuan X., Fujisaki K. Characterization of Haemaphysalis longicornis recombinant cement-like antigens and preliminary study of their vaccination effects. Journal of Veterinary Medical Science 2006, 68(12):1289-1295.
59. Zhou J., Gong H., Zhou Y., Xuan X., Fujisaki K. Identification of a glycine-rich protein from the tick Rhipicephalus haemaphysaloides and evaluation of its vaccine potential against tick feeding. Parasitology Research 2006, 100(1):77-84.
60. Trimnell A.R., Davies G.M., Lissina O., Hails R.S., Nuttall P.A. A cross-reactive tick cement antigen is a candidate broad-spectrum tick vaccine. Vaccine 2005, 23(34):4329-4341.
61. Pohl P.C., Sorgine M.H., Leal A.T., Logullo C., Oliveira P.L., Vaz Ida S., et al. An extraovarian aspartic protease accumulated in tick oocytes with vitellin-degradation activity. Comparative Biochemistry and Physiology. Part B: Biochemistry and Molecular Biology 2008, 151(4):392-399.
62. Sorgine M.H., Logullo C., Zingali R.B., Paiva-Silva G.O., Juliano L., Oliveira P.L. A heme-binding aspartic proteinase from the eggs of the hard tick Boophilus microplus. Journal of Biological Chemistry 2000, 275(37):28659-28665.
63. Seixas A., Leal A.T., Nascimento-Silva M.C., Masuda A., Termignoni C., da Silva V.I. Vaccine potential of a tick vitellin-degrading enzyme (VTDCE). Veterinary Immunology and Immunopathology 2008, 124(3-4):332-340.
64. Munderloh U.G., Liu Y., Wang M., Chen C., Kurtti T.J. Establishment, maintenance and description of cell lines from the tick Ixodes scapularis. Journal of Parasitology 1994, 80(4):533-543.
65. Radulovic Z., Milutinovic M., Andelkovic M., Vujcic Z., Tomanovic S., Bozic N., et al. Allozyme polymorphism of Mdh and alpha-Gpdh in Ixodes ricinus populations: comparison of borreliae-infected and uninfected ticks. Experimental and Applied Acarology 2006, 40(2):113-121.
66. Semenov A.V., Alekseev A.N., Dubinina E.V., Kaufmann U., Jensen R.M. Detection of the genotypic heterogeneity of Ixodes persulcatus Schulze (Acari: Ixodidae) of the North-West region of Russia and characteristics of distribution of tick-borne pathogens causing Lyme disease and Ehrlichia infections in various genotypes. Meditsinskaia Parazitologiia i Parazitarnye Bolezni 2001, (3):11-15.
67. Siddall N.A., McLaughlin E.A., Marriner N.L., Hime G.R. The RNA-binding protein Musashi is required intrinsically to maintain stem cell identity. Proceedings of the National Academy of Sciences of the United States of America 2006, 103(22):8402-8407.
68. Jittapalapong S., Jansawan W., Barriga O.O., Stich R.W. Reduced incidence of Babesia bigemina infection in cattle immunized against the cattle tick, Boophilus microplus. Annals of the New York Academy of Sciences 2004, 1026:312-318.
69. Ribeiro J.M., Alarcon-Chaidez F., Francischetti I.M., Mans B.J., Mather T.N., Valenzuela J.G., et al. An annotated catalog of salivary gland transcripts from Ixodes scapularis ticks. Insect Biochemisry and Molecular Biology 2006, 36(2):111-129.
70. McNally K.L., Mitzel D.N., Anderson J.M., Ribeiro J.M., Valenzuela J.G., Myers T.G., et al. Differential salivary gland transcript expression profile in Ixodes scapularis nymphs upon feeding or flavivirus infection. Ticks and Tick-borne Diseases 2012, 3(1):18-26.
71. Oliveira C.J., Sa-Nunes A., Francischetti I.M., Carregaro V., Anatriello E., Silva J.S., et al. Deconstructing tick saliva: non-protein molecules with potent immunomodulatory properties. Journal of Biological Chemistry 2011, 286(13):10960-10969.
72. Bartosik K., Sitarz M., Szymanska J., Buczek A. Tick bites on humans in the agricultural and recreational areas in south-eastern Poland. Annals of Agricultural and Environmental Medicine 2011, 18(1):151-157.
73. Beugnet F., Kolasinski M., Michelangeli P.A., Vienne J., Loukos H. Mathematical modelling of the impact of climatic conditions in France on Rhipicephalus sanguineus tick activity and density since 1960. Geospat Health 2011, 5(2):255-263.
74. Cochez C., Lempereur L., Madder M., Claerebout E., Simons L., WN D.E., et al. Foci report on indigenous Dermacentor reticulatus populations in Belgium and a preliminary study of associated babesiosis pathogens. Medical and Veterinary Entomology 2012, 26(3):355-358.