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Rhipicephalus appendiculatus salivary glands: Identification of bioactive molecules and antigens

Published online by Cambridge University Press:  19 September 2011

Moses K. H. Limo
Affiliation:
International Laboratory for Research on Animal Diseases (ILRAD), P. O. Box 30709, Nairobi Kenya
David C. Seldin
Affiliation:
Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston Massachusetts 02115, USA
Wolf P. Voigt
Affiliation:
International Laboratory for Research on Animal Diseases (ILRAD), P. O. Box 30709, Nairobi Kenya
Onesmo K. Ole Moiyoi
Affiliation:
International Laboratory for Research on Animal Diseases (ILRAD), P. O. Box 30709, Nairobi Kenya
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Abstract

Rhipicephalus appendiculatus salivary glands extracts and saliva contain both biochemically active and pharmacological agents with various effector functions, including inhibition of host enzymes or inactivation of other host molecules that may be important in mounting tick rejection. The majority of these salivary biochemicals may interact with host antibodies at the feeding site or in the gut (or both), that interfere with proper tick attachment and feeding. The possible role of these biochemicals in tick feeding is discussed. Of particular interest is a salivary anticoagulant, which increased as feeding phase progressed and was present in all life cycle stages of the tick. Antibodies raised in rabbits against salivary gland extracts obtained from female if. appendiculatus fed on rabbits for various days, recognized several antigens on Western blots of salivary gland extracts, but failed to react with the purified tick salivary anticoagulant molecule. Thus, tick anticoagulant was poorly immunogenic compared to other salivary moieties. These results may help to explain the strategies adopted by the tick to circumvent biochemical detachment by the damaging host-protective immune responses, thereby enabling the vector to co-exist with its mammalian hosts.

Résumé

Les extraits de glandes salivaires et la sali ve de Rhipicephalus appendiculatus contiennent des substances biochimiques actives dont les diverses fonctions incluent entre autres l'inhibition des enzymes ou l'inactivation d'autres molecules de l'hôte; el les pourraient jouer un ròle important dans la rejection de la tique. La majorité de ces composes biochimiques pourraient réagir avec les anticorps de l'hôte au niveau de la prise de nourriture ou de l'estomac (ou les deux à la fois), et influencer la fixation de la tique sur l'hôte et la prise de nourriture. Le rôle possible de ces composes biochimiques au niveau de la tique est discuté. lin intérét particulier est porté sur un anticoagulant contenu dans la salive et present à tous les stades de développement du vecteur; le volume secrete de cet anticoagulant augmente au fur et à mesure que se poursuite le processus de prise de nourriture. Des anticorps produits à partir des lapins centre les extraits de glandes salivaires obtenus de la femelle de R. appendiculatus nourris plusiers jours sur de lapins, detectent plusiers antigens grace à la technique de “Western blot” utilisant des extraits de glandes salivaires, mais ne peuvant réagir avec la molecule purifiée de l'anticoagulant. II a été déduit que l'anticoagulant contenu dans la salive de la tique est très peu immunogéne en comparaison avec d'autres molecules salivaires.

Ces résultats pourraient expliquer des strategies adoptees par la tique pour empècher un detachment biochimique, par la destruction des réponses immunitaires de l'héres nôtes.

Type
Research Articles
Copyright
Copyright © ICIPE 1993

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References

REFERENCES

Allen, J. R. (1973) Tick resistance: basophils in skin reactions of resistant guinea pigs. Int. J. Parasitol. 3, 195200.CrossRefGoogle ScholarPubMed
Allen, J. R. and Humpreys, S. J. (1979) Immunization of guinea pigs and cattle against ticks. Nature 280, 491–193.CrossRefGoogle ScholarPubMed
Askenase, P. W., Bagnall, B. G. and Worms, M. J. (1982) Cutaneous basophil - associated resistance of ectoparasites (ticks). I. Transfer with immune serum or immune cells. Immunology 45, 501511.Google ScholarPubMed
Brown, S. J., Graxiano, F. M. and Askenase, P. W. (1982) Immune serum transfer of cutaneous basophil-associated resistance to ticks: Mediation by 7s IgG antibodies. J. Immunol. 129, 24072412.CrossRefGoogle Scholar
Brown, S. J. and Askenase, P. W. (1983) Immune rejection of ectoparasites (ticks) by T cell and IgG, antibody recruitment of basophils and eosinophils. Fed. Proc. 42, 17441749.Google Scholar
Brown, S. J., Shapiro, S. Z. and Askenase, P. W. (1984) 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. J. Immunol. 133, 33193325.CrossRefGoogle ScholarPubMed
Burnette, W. N. (1982) “Western blotting” Electrophoretic transfer of proteins from sodium dodecyl sulfate polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Anal. Biochem. 112, 195203.CrossRefGoogle Scholar
Buscher, G. and Tangu, B. (1986) Quantitative studies on Theileria parva in the salivary glands of Rhipicephalus appendiculatus adults: Quantitation and prediction of infection. International J. Parasitol. 93100.CrossRefGoogle ScholarPubMed
Chinery, W. A. and Aitey-Smith, E. (1977) Histamine blocking agent of the tick Rhipicephalus sanguineus sanguineus. Nature (London) 265, 366367.CrossRefGoogle ScholarPubMed
Dickinson, R. G., O'Hagan, J. E., Schultz, M., Binnington, K. C. and Hegarty, M. P. (1976) Prostaglandin in the saliva of the cattle tick Boophilus microplus. Australian J. Exp. Biol. Med. Sci. 54, 475, 486.CrossRefGoogle ScholarPubMed
Fawcett, D. S., Buscher, G. and Doxsey, S. (1982) Salivary gland of the tick vector of East Coast Fever. III. The ultrastructure and sporogony in Theileria parva. Tissue and Cell 14, 183206.CrossRefGoogle ScholarPubMed
Ferreira, S. H. (1972) Prostagladins, aspirin-like drugs and analgesia. Nature (London) 240, 200209.Google Scholar
Fivaz, G. H., Noral, R. A. I. and Lawrance, J. A. (1989) Transmission of Theileria parva bovis (strain boleni) to cattle resistant to the brown ear tick Rhipicephalus appendiculatus (Neuman). Trop. Anim. Health Prod. 21, 21292134.CrossRefGoogle Scholar
Gebrand, F. B. S. and Schill, Wolf-Bemhad (1972) Radial diffusion in gel for microdetermination of enzymes. II. Plasminogen activator, elastase and non-specific proteases. Anal. Biochem. 48, 921.Google Scholar
Geczy, A. F., Naughton, M. A., Clegy, J. B. and Hewetson, R. W. (1971) Esterases and carbohydrate-splitting enzyme in the saliva of the cattle tick Boophilus microplus. J. Parasitol. 57, 437438.CrossRefGoogle ScholarPubMed
Gill, H. S. (1984) Tick feeding and the development of immunity to Hyalomma anatolicum anatolicum. Ph.D. Thesis. University of Edinburgh.Google Scholar
Gill, H. S., Boid, R. and Ross, C. A. (1986) Isolation and characterization of salivary antigens from Hyalomma anatolicum anatolicum. Parasite Immunol. 8, 1125.CrossRefGoogle ScholarPubMed
Gordon, J. R. and Allen, J. R. (1991) Factors V and VII anticoagulant activities in the salivary glands of feediag Dermacentor andersoni ticks. J. parasitol. 167170.CrossRefGoogle ScholarPubMed
Gwynne, H. L., Starnes, W. L. and Behall, F. J. (1976) Human liver aminopeptidase. In Methods in Enzymology. Academic Press London. Vol. XLV, pp. 495504.Google Scholar
Hawkins, R. I. and Hellman, K. (1966) Factors affecting blood clotting from salivary glands and crop of Glossina austeni. Nature (London) 212, 738739.CrossRefGoogle Scholar
Hugli, T. E. and Muller-Eberhard, H. J. (1979) Anaphylatoxins: C3a and C5a. Adv. Immunol. 26, 148.Google Scholar
Jackson, L. A. and Opdebeck, J. P. (1990) Humoral immune responses of Hereford cattle vaccinated with midgut antigens of the cattle tick, Boophilus microplus. Parasite Immunol. 12, 141151.CrossRefGoogle ScholarPubMed
Jordan, S. P., Waxman, L., Smith, D. E. and Vlasuk, G. P. (1990) Tick anticoagulant peptide: Kinetic analysis of the recombinant inhibitor with blood coagulation factor Xa. Biochemistry 29, 1109511100.CrossRefGoogle ScholarPubMed
Irvin, A. D. and Brocklesby, D. W. (1970) Rearing and maintaining Rhipicephalus appendiculatus in the laboratory. J. Inst. Anim. Technol. 21, 3112.Google Scholar
Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680685,CrossRefGoogle ScholarPubMed
Limo, M. K., Voigt, W. P., Tumboh-Oeri, A. G., Njogu, R. M. and Onesmo ole Moiyoi, K. (1991) Purification and characterization of an anticoagulant from the salivary glands of the ixodid tick Rhiphicepalus appendiculatus. Exp. Parasitol. 72, 418429.CrossRefGoogle ScholarPubMed
Lowry, O. H., Rosebrough, N. J., Farr, A. L. and Randall, R. J. (1951) Protein measurement with the folin phenol reagent. J. Biol. Chem. 193, 265275.CrossRefGoogle ScholarPubMed
Markwardt, F. (1963) Blutgerinnungshemmende Wirkstoffe aus Blutsaugenden Tiernen. pp. 8889. G. Fischer, Jena, West Germany.Google Scholar
McGowan, M. J., Barker, P. W., Homer, J. J., McNew, R. W. and Holscher, K. H. (1981) Success of tick feeding on calves immunized with Amblyomma americanum (Acari:Ixodidae) extract. J. Med. Entomol. 18, 328332.CrossRefGoogle ScholarPubMed
Mongi, A. O., Shapiro, S. Z., Doyle, J. J., and Cunninghum, M. P. (1986) Immunization of rabbits with Rhipicephalus appendiculatus antigen-antibody complexes. Insect Sci. Applic. 4, 471477.Google Scholar
Neeper, M. P., Waxman, L., Smith, D. E., Schulam, C. A., Sardana, M., Ellis, R. W., Schaffers, L. W., Sieggl, P. K. S. and Vlasuk, G. P. (1990) Characterisation of recombinant tick anticoagulant peptide. The. Biol. Chem. 265, 1774617752.CrossRefGoogle ScholarPubMed
Nyindo, M., Essuman, S. and Dhadialla, T. S. (1989) Immunisation against ticks: Use of salivary gland antigens and infestation with Rhiphicephalus appendiculatus (Acari:Ixodidae) in rabbits. J. Med. Entomol. 26, 430434.CrossRefGoogle Scholar
Obenchain, F. D. and Galun, R. (1982) Preface. In Physiology of Ticks (Edited by Obenchain, F. D. and Galun, R.), pp. vii–ix. Pergamon Press, Oxford UK.CrossRefGoogle Scholar
Purnell, R. E. and Joyner, L. P. (1968) The development of Theileria parva in the salivary glands of the tick Rhipicephalus appendiculatus. Parasitology 58, 725732.CrossRefGoogle ScholarPubMed
Ribeiro, J. M. C., Makoul, G. T., Levine, J., Robin, D. R., and Speilman, A. (1985) Antihemostatic, anti-inflammatory and immunosuppressive properties of the saliva of a tick, Ixodes dammini. J. Exp. Med. 161, 332334.CrossRefGoogle ScholarPubMed
Ribeiro, J. M. C. (1989) Role of saliva in tick/host interactions. Exp. Appl. Acarol. 7, 1520.CrossRefGoogle ScholarPubMed
Riek, R. F. (1962) Studies on the reactions of animals to infestation with ticks. VI. Resistance of cattle to infestation with Boophilus microplus (Canestrini). Australian J. Agric. Res. 13, 532550.CrossRefGoogle Scholar
Roberts, J. A. and Kerr, J. D. (1976) Boophilus microplus: passive transfer of resistance in cattle. J. Parasitol. 62, 485488.CrossRefGoogle ScholarPubMed
Shapiro, S. Z., Voigt, W. P. and Ellis, J. A. (1989) Acquired resistance to ixodid ticks induced by cement antigen. Exp. Appl. Acarol. 7, 3341.CrossRefGoogle ScholarPubMed
Steelman, C. D. (1976) Effects of external and internal arthropod parasites on domestic livestock production. Annu. Rev. Entomol. 21, 155178.CrossRefGoogle ScholarPubMed
Tatchell, R. J. (1967) A modified method for obtaining tick oral secretion. J. Parasitol. 53, 11061107.CrossRefGoogle ScholarPubMed
Tatchell, R. J. (1967) The significance of host-parasite relationship in the feeding of the cattle tick. Boophilus microplus. Proceedings of the 2nd Int. Cong. Acarol. pp. 341343.Google Scholar
Trager, W. (1939) Acquired immunity to ticks. J. Parasitol. 25, 5781.CrossRefGoogle Scholar
Waxman, L., Smith, D. E., Arcuri, K. E. and Vlasuk, G. P. (1990) Tick anticoagulant peptide (TAP) is a novel inhibitor of blood coagulation factor Xa. Science 248, 593595.CrossRefGoogle ScholarPubMed
Webster, M. and Prado, E. S. (1970) Glandular kallikreins from horse and human urine and from hog pancreas. In Methods of Enzymology (Edited by Permann, G. E. and Lorand, L.), Vol. 19, 681699. Academic Press, Orlando, FL.Google Scholar
Wikel, S. K. (1981) The induction of host resistance to tick infestation with a salivary gland antigen. Am. J. Trap. Med. Hyg. 30, 284288.CrossRefGoogle ScholarPubMed
Wikel, S. K. (1982) Immunological basis of Host resistance to ticks. In Physiology of Ticks (Edited by Obenchain, F. D. and Galun, R.), pp. 169196, Pergamon Press, Oxford, UK.CrossRefGoogle Scholar
Willadsen, P. (1980) Immunity to ticks. Adv. Parasitol. 18, 293313.Google Scholar
Willadsen, P. and Kemp, D. H. (1988) Vaccination with concealed antigens for tick control. Parasitol. Today 4, 196198.CrossRefGoogle ScholarPubMed
Willadsen, P., Riding, G. A., McKenna, R. V., Kemp, D. H., Tell, M. R. L., Nielsen, J. N., Lahnstein, J., Cobon, G. S., andGough, J. M. (1989) Immunologic control of a parasitic arthropod. Identification of a protective antigen from Boophilus microplus. J. Immunol. 143, 13461351.CrossRefGoogle ScholarPubMed
Willadsen, P., andRiding, G. A. (1980) On the biological role of a proteolytic enzyme inhibitor from the ectoparasite tick Boophilus microplus. Biochem. J. 189, 295303.CrossRefGoogle ScholarPubMed
Wong, J. Y. M. and Opdebeeck, J. P. (1989) Protective efficacy of antigens solubilized from gut membrane of the cattle tick Boophilus microplus. Parasite Immunol. 12, 7579.CrossRefGoogle Scholar