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Displaced tick-parasite interactions at the host interface

Published online by Cambridge University Press:  16 March 2011

P. A. Nuttall
Affiliation:
NERC Institute of Virology & Environmental Microbiology, Mansfield Road, Oxford, OX1 3SR, UK

Summary

Reciprocal interactions of parasites transmitted by blood-sucking arthropod vectors have been studied primarily at the parasite–host and parasite–vector interface. The third component of this parasite triangle, the vector–host interface, has been largely ignored. Now there is growing realization that reciprocal interactions between arthropod vectors and their vertebrate hosts play a pivotal role in the survival of arthropod-borne viruses, bacteria, and protozoa. The vector–host interface is the site where the haematophagous arthropod feeds. To obtain a blood meal, the vector must overcome the host's inflammatory, haemostatic, and immune responses. This problem is greatest for ixodid ticks which may imbibe as much as 15 ml blood whilst continuously attached to their host for 10 days or more. To feed successfully, the interface between tick and host becomes a battle between the host's mechanisms for combating the tick and the tick's armoury of bioactive proteins and other chemicals which it secretes, via saliva, into the feeding lesion formed in the host's skin. Parasites entering this battlefield encounter a privileged site in their vertebrate host that has been profoundly modified by the pharmacological activities of their vector's saliva. For example, ticks suppress natural killer cells and interferons, both of which have potent antiviral activities. Not surprisingly, vector-borne parasites exploit the immunomodulated feeding site to promote their transmission and infection. Certain tick-borne viruses are so successful at this that they are transmitted from one infected tick, through the vertebrate host to a co-feeding uninfected tick, without a detectable viraemia (virus circulating in the host's blood), and with no untoward effect on the host. When such viruses do have an adverse effect on the host, they may impede their vectors' feeding. Thus important interactions between ticks and tick-borne parasites are displaced to the interface with their vertebrate host - the skin site of blood-feeding and infection.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1998

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References

Alekseev, A. N. & Chunikhin, S. P. (1990). Exchange of tick-borne encephalitis virus between Ixodidae simultaneously feeding on animals with subthreshold levels of viraemia. Meditsinskaya Parazitologiya i Parazitarnye Bolezni 2, 4850.Google Scholar
Alekseev, A. N., Chunikhin, S. P., Rukhkyan, M. Y. & Stefutkina, L. F. (1991). Possible role of Ixodidae salivary gland substrate as an adjuvant enhancing arbovirus transmission. Meditsinskaya Parazitologiya i Parazitarnye Bolezni 1, 2831.Google Scholar
Anastopoulos, P., Thurn, M. J. & Broady, K. W. (1991). Anticoagulant in the tick Ixodes holocyclus. Australian Veterinary Journal 68, 366367.Google Scholar
Austyn, J. M. (1992). Antigen uptake and presentation by dendritic leukocytes. Seminars in Immunology 4, 227236.Google Scholar
Ben-Yakir, D., Fox, J. C., Homer, J. T. & Barker, R. W. (1986). Quantitative studies of host immunoglobulin G passage into the haemocoel of the tick Amblyomma americanum and Dermacentor variabilis. In Morphology, Physiology and Behavioral Biology of Ticks (ed. Sauer, R. J. & Hair, J. A.), pp. 329339. Chichester, UK: Ellis Horwood.Google Scholar
Bezuidenhout, J. D. (1987). Natural transmission of heartwater. Onderstepoort Journal of Veterinary Medicine 54, 525528.Google ScholarPubMed
Davies, C. R., Jones, L. D. & Nuttall, P. A. (1986). Experimental studies on the transmission cycle of Thogoto virus, a candidate orthomyxovirus, in Rhipicephalus appendiculatus ticks. American Journal of Tropical Medicine and Hygiene 35, 12561262.CrossRefGoogle Scholar
Gern, L. & Rais, O. (1996). Efficient transmission of Borrelia burgdorferi between cofeeding Ixodes ricinus ticks (Acari: Ixodidae). Journal of Medical Entomology 33, 189192.Google Scholar
Gresikova, M. & Calisher, C. H. (1988). Tick-borne encephalitis. In The Arboviruses: Epidemiology and Ecology(ed. Monath, T. P.), pp. 177202. Boca Raton, Florida: CRC Press Inc.Google Scholar
Hajnicka, V., Fuchsberger, N., Slovak, M., Kocakova, P., Labuda, M. & Nuttall, P. A. (1998). Tick salivary gland extracts promote virus growth in vitro. Parasitology in press.CrossRefGoogle Scholar
Jaworski, D. C., Simmen, F. A., Lamoreaux, W., Coons, L. B., Muller, M. T. & Needham, G. R. (1995). A secreted calreticulin protein in ixodid tick {Amblyomma americanum) saliva. Journal of Insect Physiology 41, 369375.CrossRefGoogle Scholar
Jones, L. D. & Nuttall, P. A. (1989 a). The effect of virus-immune hosts on Thogoto virus infection of the tick, Rhipicephalus appendiculatus. Virus Research 14, 129140.CrossRefGoogle Scholar
Jones, L. D. & Nuttall, P. A. (1989 b). Non-viraemic transmission of Thogoto virus: influence of time and distance. Transactions of the Royal Society of Tropical Medicine and Hygiene 83, 712714.CrossRefGoogle Scholar
Jones, L. D. & Nuttall, P. A. (1990). The effect of host resistance to tick infestation on the transmission of Thogoto virus by ticks. Journal of General Virology 71, 10391043.CrossRefGoogle Scholar
Jones, L. D., Davies, C. R., Steele, G. M. & Nuttall, P. A. (1987). A novel mode of arbovirus transmission involving a nonviraemic host. Science 237', 775777.CrossRefGoogle Scholar
Jones, L. D., Hodgson, E. & Nuttall, P. A. (1989). Enhancement of virus transmission by tick salivary glands. Journal of General Virology 70, 18951898.Google Scholar
Jones, L. D., Hodgson, E. & Nuttall, P. A. (1990). Characterization of tick salivary gland factor(s) that enhance Thogoto virus transmission. Archives of Virology Supplement 1, 227–234.Google Scholar
Jones, L. D., Hodgson, E., Williams, T., Higgs, S. & Nuttall, P. A. (1992 a). Saliva activated transmission (SAT) of Thogoto virus: relationship with vector potential of different haematophagous arthropods. Medical and Veterinary Entomology 6, 261265.CrossRefGoogle Scholar
Jones, L. D., Kaufman, W. R. & Nuttall, P. A. (1992 b ). Modification of the skin feeding site by tick saliva mediates virus transmission. Experientia 48, 779782.Google Scholar
Jones, L. D., Gaunt, M., Hails, R. S., Laurenson, K., Hudson, P. J., Reid, H., Henbest, P. & Gould, E. A. (1997). Transmission of louping-ill virus between infected and uninfected ticks co-feeding on mountain hares. Medical and Veterinary Entomology 11, 172176.CrossRefGoogle Scholar
Karczewski, J., Endris, R. & Connolly, T. M. (1994). Disagregin is a fibrinogen receptor antagonist lacking the Arg-Gly-Asp sequence from the tick, Ornithodoros moubata. Journal of Biological Chemistry 269, 67026708.Google Scholar
Karczewski, J., Waxman, L., Endris, R. & Connolly, T. M. (1995). An inhibitor from the argasid tick Ornithodoros moubata of cell adhesion to collagen. Biochemical and Biophysical Research Communications 208, 532541.CrossRefGoogle Scholar
Kaufman, W. (1989). Tick-host interaction: a synthesis of current concepts. Parasitology Today 5, 4756.CrossRefGoogle ScholarPubMed
Kaufman, W. R. & Nuttall, P. A. (1996). Amblyomma variegatum (Acari: Ixodidae): Mechanism and control of arbovirus secretion in tick saliva. Experimental Parasitology 82, 316323.CrossRefGoogle Scholar
Kubes, M., Fuchsberger, N., Labuda, M., Zuffova, E. & Nuttall, P. A. (1994). Salivary gland extracts of partially fed Dermacentor reticulatus ticks decrease natural killer cell activity in vitro. Immunology 82, 113116.Google Scholar
Labuda, M., Jones, L. D., Williams, T., Danielova, D. & Nuttall, P. A. (1993 a). Efficient transmission of tickborne encephalitis virus between cofeeding ticks. Journal of Medical Entomology 30, 295299.CrossRefGoogle Scholar
Labuda, M., Jones, L. D., Williams, T. & Nuttall, P. A. (1993 b). Enhancement of tick-borne encephalitis virus transmission by tick salivary gland extracts. Medical and Veterinary Entomology 7, 193196.CrossRefGoogle Scholar
Labuda, M., Nuttall, P. A., Kozuch, O., Eleckova, E., Williams, T., Zuffova, E. & Sabo, A. (1993 c). Non-viraemic transmission of tick-borne encephalitis virus: a mechanism for arbovirus survival in nature. Experientia 49, 802805.CrossRefGoogle Scholar
Labuda, M., Austyn, J., Zuffova, E., Kozuch, O., Fuchsberger, N., Lysy, J. & Nuttall, P. (1996). Importance of localized skin infection in tick-borne encephalitis virus transmission. Virology 219, 357366.CrossRefGoogle Scholar
Labuda, M., Kozuch, O., Zuffova, E., Eleckova, E., Hails, R. S. & Nuttall, P. A. (1997). Tick-borne encephalitis virus transmission between ticks cofeeding on specific immune natural rodent hosts. Virology 235, 138143.CrossRefGoogle Scholar
Limo, M. K., Voigt, W. P., Tumbo-Oeri, A. G., Njogu, R. M. & Ole-Moiyoi, O. K. (1991). Purification and characterization of an anticoagulant from the salivary glands of the ixodid tick, Rhipicephalus appendiculatus. Experimental Parasitology 72, 418429.Google Scholar
Monath, T. & Heinz, F. (1996). Flaviviruses. In Fields Virology(ed. Fields, B. N.), pp. 9611034. Philadelphia: Lippincott-Raven.Google Scholar
Nuttall, P. A. & Jones, L. D. (1991). Non-viraemic tickborne virus transmission: mechanism and significance. In Modern acarology(ed. Dusbabek, F. & Bukva, V.), pp. 36. Prague and The Hague: Academia and SPB Academic Publishing bv.Google Scholar
Ogden, N. H., Nuttall, P. A. & Randolph, S. E. (1997). Natural Lyme disease cycles maintained via sheep by co-feeding ticks. Parasitology 115, 591599.Google Scholar
Randolph, S. E., Gern, L. & Nuttall, P. A. (1996). Cofeeding ticks: epidemiological significance for tickborne pathogen transmission. Parasitology Today 12, 472479.CrossRefGoogle Scholar
Rechav, Y. (1992). Naturally acquired resistance to ticks - a global view. Insect Science Applications 13, 495504.Google Scholar
Ribeiro, J. M. C. (1987). Ixodes dammini: salivary anticomplement activity. Experimental Parasitology 64, 347353.Google Scholar
Samuelson, J., Lerner, E., Tesh, R. & Titus, R. (1991). A mouse model of Leishmania braziliensis braziliensis infection produced by coinjection with sand fly saliva. Journal of Experimental Medicine 173, 4954.Google Scholar
Sauer, J. R., Mcswain, J. L. & Essenberg, R. C. (1994). Cell membrane receptors and regulation of cell function in ticks and blood-sucking insects. International Journal for Parasitology 24, 3352.Google Scholar
Sonenshine, D. E. (1991). Biology of Ticks, First edn. New York, Oxford. Oxford University Press.Google Scholar
Titus, R. G. & Ribeiro, J. C. (1988). Salivary gland lysates from the sandfly Lutzomyia longipalpis enhance Leishmania infectivity. Science 239, 1306–1239.Google Scholar
Wang, H. & Nuttall, P. A. (1994). Excretion of host immunoglobulin in tick saliva and detection of IgGbinding proteins in tick haemolymph and salivaryglands. Journal of Parasitology 109, 525530.CrossRefGoogle Scholar
Wang, H. & Nuttall, P. A. (1995). Immunoglobulin-G binding proteins in the ixodid ticks, Rhipicephalus appendiculatus, Amblyomma variegatum and Ixodes hexagonus. Parasitology 111, 161165.CrossRefGoogle Scholar
Wang, H., Paesen, G., Barbour, A. & Nuttall, P. (1998). Tick immunoglobulin binding proteins. Nature (in press.)Google Scholar
Waxman, L., Smith, D. E., Arcuri, K. E. & Vlasuk, G. P. (1990). Tick anticoagulant peptide (Tap) is a novel inhibitor of blood coagulation factor Xa. Science 248, 593596.Google Scholar
Waxman, L. & Connolly, T. M. (1993). Isolation of an inhibitor selective for collagen-stimulated platelet aggregation from the soft tick Ornithodorus moubata. Journal of Biological Chemistry 268, 54455449.Google Scholar
Wikel, s. K. (1996). The Immunology of Host-Ectoparasitic Arthropod Relationships,First edn. Wallingford, UK., CAB International.Google Scholar
Wikel, S. K. & Bergman, D. (1997). Tick-host immunology: significant advances and challenging opportunities. Parasitology Today 13, 383389.Google Scholar
Zeller, H. G., Cornet, J.-P. & Camicas, J.-L. (1994). Experimental transmission of Crimean-Congo haemorrhagic fever virus by West African wild ground-feeding birds to Hyalomma marginatum rufipes ticks. American Journal of Tropical Medicine and Hygiene 50, 676681.CrossRefGoogle Scholar