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Inoculation of salivary gland extracts obtained from female of Rhipicephalus sanguineus (Latreille, 1806) (Acari, Ixodidae) with 2, 4, and 6 days of feeding in rabbit: I—histopathology of the feeding lesion

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Abstract

This study analyzed the histopathology of rabbit skin, previously immunized with SGE2, SGE4, and SGE6 gland extracts prepared from salivary glands of Rhipicephalus sanguineus female with 2, 4, and 6 days of feeding, at the region of the R. sanguineus female feeding lesion 2, 4, and 6 days after tick attachment. In this work, infestation-naïve New Zealand White rabbits were inoculated either with the extracts (test group (TG)) or with phosphate buffer and complete Freund’s adjuvant mixture (control group 2 (CG2)). Each extract-inoculated- (TG and CG2) and non-inoculated (CG1) rabbit was subsequently infested with R. sanguineus. Skin biopsies were collected from the rabbit at the tick feeding lesion at 2, 4, and 6 days of feeding. Results revealed that rabbit immunization with gland extracts induced acquisition of resistance against this species. It should be stated that the SGE4 extract was the most effective in developing an immune–inflammatory response against ectoparasites, being this process characterized by the presence of an early and intense inflammatory cell infiltrate. On the other hand, SGE6 extract caused a later appearance of resistance with less infiltrate occurrence and intense edema at the feeding lesion site. As to the inflammatory process deriving from SGE2 extract inoculation, it was the less intense. It was concluded that immunization with different extracts from R. sanguineus female salivary glands did not change microscope features of the inflammatory process, although an earlier or more intense and later response, which was also dependent on the inoculate extract, was noticed.

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References

  • Allen JR, Khalil HM, Graham J (1979) The location of tick salivary antigens, complement and immunoglobulin in the skin of guinea-pigs infested with Dermacentor andersoni larvae. Immunology 38:467–472

    PubMed  CAS  Google Scholar 

  • Almazán C, Lagunes R, Villar M, Canales M, Rosario-Cruz R, Jongejan F, de la Fuente J (2010) Identification and characterization of Rhipicephalus (Boophilus) microplus candidate protective antigens for the control of cattle tick infestations. Parasitol Res 106:471–479

    Article  PubMed  Google Scholar 

  • Almeida APG, Bechara GH, Varma RMG (1994) Cross-reactivity between hard ticks antigens. Braz J Med Biol Res 27:617–707

    Google Scholar 

  • Balashov YS (1972) Bloodsucking ticks (Ixodidea)—vectors of diseases of man and animals. Misc Publ Entomol Soc Am 8:160–376

    Google Scholar 

  • Barros-Battesti DM (2006) Introdução. In: Barros-Battesti DM, Arzua M, Bechara GH (eds) Carrapatos de importância médico-veterinária da região neotropical. Um guia ilustrado para a identificação de espécies. Butantan, São Paulo, pp 1–3

    Google Scholar 

  • Bechara GH, Szabó MPJ, Ferreira BR, Garcia MV (1995) Rhipicephalus sanguineus tick in Brazil: feeding and reproductive aspects under laboratorial conditions. Braz J Med Biol Res 4:61–66

    Google Scholar 

  • Bowman AS, Sauer JR (2004) Tick salivary glands: function, physiology and future. Parasitology 129:s67–s81

    Article  PubMed  Google Scholar 

  • Brossard M, Wikel SK (1997) Immunology of interactions between ticks and hosts. Med Vet Entomol 11:270–276

    Article  PubMed  CAS  Google Scholar 

  • Christe M, Rutti B, Brossard M (1998) Susceptibility of BALB/c mice to nymphs and larvae of Ixodes ricinus after modulation of IgE production with anti-interleukin-4 or anti-interferon-γ monoclonal antibodies. Parasitol Res 84:388–393

    Article  PubMed  CAS  Google Scholar 

  • Dhadialla TS, Rutt B, Brossard M (1990) Induction of host resistance to Rhipicephalus appendiculatus in rabbits: effects of immunizing with detergent-solubilized tick tissue proteins. Parasitol Res 76:536–539

    Article  PubMed  CAS  Google Scholar 

  • Ferreira BR, Machado RZ, Bechara GH (1996) Western blot analysis of tick antigen from Rhipicephalus sanguineus unfed larval extract and identification of antigenic sites in tick section using immunohistochemistry. A comparative study between resistant and susceptible host species. Vet Parasitol 62:161–174

    Article  PubMed  CAS  Google Scholar 

  • Furquim KCS, Camargo-Mathias MI, Hebling LMGF, Roma GC, Bechara GH (2011) Ticks’ response to feeding on host immunized with glandular extracts of Rhipicephalus sanguineus females fed for 2, 4, and 6 days. I. Inactivity or early degeneration of salivary glands? Parasitol Res 109:147–162

    Article  PubMed  Google Scholar 

  • Gill HS, Boid R, Ross CA (1986) Isolation and characterization of salivary antigens from Hyalomma anatolicum anatolicum. Parasite Immunol 8:11–25

    Article  PubMed  Google Scholar 

  • Girardin P, Brossard M (1989) Effects of cyclosporine A on humoral immunity to ticks and on cutaneous immediate and delayed hypersensitivity reactions to Ixodes ricinus L. salivary-gland antigens in re-infested rabbits. Parasitol Res 75:657–662

    Article  PubMed  CAS  Google Scholar 

  • Guglielmone A, Szabó MJP, Martins JRS, Estrada-Pena A (2006) Diversidade e importância de carrapatos na sanidade animal. In: Barros-Battesti DM, Arzua M, Bechara GH (eds) Carrapatos de importância médico-veterinária da região neotropical. Um guia ilustrado para a identificação de espécies. Butantan, São Paulo, pp 115–138

    Google Scholar 

  • Jittapalapong S, Stich RW, Gordon JC, Wittum TE, Barriga OO (2000) Performance of female Rhipicephalus sangineus (Acari: Ixodidae) fed on dogs exposed to multiple infestation or immunization with tock salivary gland or midgut tissues. J Med Entomol 37:601–611

    Article  PubMed  CAS  Google Scholar 

  • Mejri N, Rutti B, Brossard M (2002) Immunosuppressive effects of Ixodes ricinus tick saliva or salivary gland extracts on innate and acquired immune response of BALB/c mice. Parasitol Res 88:192–197

    Article  PubMed  Google Scholar 

  • Monteiro GER, Bechara GH (2008) Cutaneous basophilia in the resistance of goats to Amblyomma cajennense nymphs after repeated infestations. Ann NY Acad Sci 1149:221–225

    Article  PubMed  Google Scholar 

  • Nunes PH, Bechara GH, Camargo-Mathias MI (2011) Secretory process of salivary glands of female Amblyomma cajennense Fabricius, 1787, (Acari: Ixodidae) ticks fed on resistant rabbits. Exp Appl Acarol 53:179–187

    Article  PubMed  CAS  Google Scholar 

  • Ramachandra RN, Wikel SK (1992) Modulation of host-immune response by ticks (Acari: Ixodidae): effect of salivary gland extracts on host macrophages and lymphocyte cytokine production. J Med Entomol 29:818–826

    PubMed  CAS  Google Scholar 

  • Sauer JR, McSwain AS, Bowman AS, Essenberg RC (1995) Tick salivary gland physiology. Ann Rev Entomol 40:245–267

    Article  CAS  Google Scholar 

  • Sedmark JJ, Grossberg SE (1977) A rapid sensitive and versatile assay for protein using Coomassie brilliant blue G250. Anal Biochem 79:544–552

    Article  Google Scholar 

  • Sonnenshine DE (1991) Biology of ticks. Oxford University Press, New York

    Google Scholar 

  • Szabó MPJ, Arantes GJ, Bechara GH (1995) Immunological characterization of adult tick Rhipicephalus sanguineus (Latreille, 1806) antigens by Western blot analysis using sera from infested or vaccinated dogs and guinea pigs. Braz J Vet Parasitol 4:79–83

    Google Scholar 

  • Turni C, Lee RP, Jackson LA (2002) Effect of salivary gland extracts from the tick, Boophilus microplus, on leucocytes from Brahman and Hereford cattle. Parasite Immunol 24:355–361

    Article  PubMed  Google Scholar 

  • Veronez VA, Castro MB, Bechara GH, Szabó MPJ (2010) Histopathology of Rhipicephalus sanguineus (Acari: Ixodidae) ticks fed on resistant hosts. Exp Appl Acarol 50:151–161

    Article  PubMed  Google Scholar 

  • Walker A (1994) Arthropods of domestic animals. A guide to preliminary identification. Chapman and Hall, London

    Google Scholar 

  • Wikel SK (1981) The induction of host resistance to tick infestation with a salivary gland antigen. AmJTrop Med Hyg 30:284–288

    CAS  Google Scholar 

  • Wikel SK, Allen JR (1977) Acquired resistance to ticks. III. Cobra venom factor and the resistance response. Immunology 32:457–465

    PubMed  CAS  Google Scholar 

  • Wikel SK, Graham JE, Allen JR (1978) Acquired resistance to ticks. IV—Skin reactivity and in vitro lymphocyte responsiveness to salivary gland antigen. Immunology 34:257–263

    PubMed  CAS  Google Scholar 

  • Willadsen P, Wood GM, Riding GA (1979) The relation between skin histamine concentration, histamine sensitivity, and the resistance of cattle to the tick, Boophilus microplus. Z Parasitenkd 59:87–93

    Article  PubMed  CAS  Google Scholar 

  • Zhou J, Gong H, Zhou Y, Xuan X, Fujisaki K (2006) Identification of a glycina-rich protein from the tick Rhipicephalus haemophysaloides and evaluation of its vaccine potential against tick feeding. Parasitol Res 100:77–84

    Article  PubMed  Google Scholar 

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Correspondence to Maria Izabel Camargo-Mathias.

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Hebling, L.M.G.F., Furquim, K.C.S., Bechara, G.H. et al. Inoculation of salivary gland extracts obtained from female of Rhipicephalus sanguineus (Latreille, 1806) (Acari, Ixodidae) with 2, 4, and 6 days of feeding in rabbit: I—histopathology of the feeding lesion. Parasitol Res 112, 577–584 (2013). https://doi.org/10.1007/s00436-012-3169-2

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  • DOI: https://doi.org/10.1007/s00436-012-3169-2

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