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Tick–host interactions: saliva-activated transmission

Published online by Cambridge University Press:  19 April 2005

P. A. NUTTALL  and
M. LABUDA
P. A. NUTTALL
Affiliation:
Centre for Ecology & Hydrology, Mansfield Rd., Oxford, OX1 3SR, UK
M. LABUDA
Affiliation:
Institute of Zoology, Slovak Academy of Sciences, Dubravska cesta 9, 845 06 Bratislava, Slovakia
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Abstract

The skin site at which ticks attach to their hosts to feed is the critical interface between the tick and its host, and tick-borne pathogens. This site is highly modified by the pharmacologically active molecules secreted in tick saliva. For pathogens, it is an ecologically privileged niche that many exploit. Such exploitation is referred to as saliva-activated transmission (SAT) – the indirect promotion of tick-borne pathogen transmission via the actions of bioactive tick saliva molecules on the vertebrate host. Here we review evidence for SAT and consider what are the most likely candidates for SAT factors among the tick pharmacopoeia of anti-haemostatic, anti-inflammatory and immunomodulatory molecules identified to date. SAT factors appear to differ for different pathogens and tick vector species, and possibly even depend on the vertebrate host species. Most likely we are searching for a suite of molecules that act together to overcome the redundancy in host response mechanisms. Whatever they turn out to be, the quest to identify the tick molecules that mediate SAT is an exciting one, and offers new insights to controlling ticks and tick-borne diseases.

Keywords

Saliva-activated transmissiontick salivapathogen transmission
Type
Research Article
Information
Parasitology , Volume 129 , Issue S1 , October 2004 , pp. S177 - S189
Copyright
© 2004 Cambridge University Press

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References

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, 48–50.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, 28–31.Google Scholar
ALLEN, J. R., KHALIL, H. A. & GRAHAM, J. E. ( 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.Google Scholar
ASTIGARRAGA, A., OLEAGA-PEREZ, A., PEREZ-SANCHEZ, R., BARANDA, J. A. & ENCINAS-GRANDES, A. ( 1997). Host immune response evasion strategies in Ornithodoros erraticus and O. moubata and their relationship to the development of an antiargasid vaccine. Parasite Immunology 19, 401–410.Google Scholar
BAUMGARTH, N. ( 2000). A two-phase model of B-cell activation. Immunology Reviews 176, 171–180.Google Scholar
BELKAID, Y., KAMHAWI, S., MODI, G., VALENZUELA, J., NOBEN-TRAUTH, N., ROWTON, E., RIBEIRO, J. & SACKS, D. ( 1998). Development of a natural model of cutaneous leishmaniasis: powerful effects of vector saliva and saliva pre-exposure on the long-term outcome of Leishmania major infection in the mouse ear dermis. Journal of Experimental Medicine 188, 1941–1953.CrossRefGoogle Scholar
BEZUIDENHOUT, J. D. ( 1987). Natural transmission of heartwater. Onderstepoort Journal of Veterinary Medicine 54, 349–351.Google Scholar
BORJESSON, D. L., SIMON, S. I., HODZIC, E., DECOCK, H. E. V., BALLANTYNE, C. M. & BARTHOLD, S. W. ( 2002). Roles of neutrophil β2 integrins in kinetics of bacteremia, extravasation, and tick acquisition of Anaplasma phagocytophila in mice. Blood 101, 3257–3264.Google Scholar
BORUCKI, M. K., KEMPF, B. J., BLITVICH, B. J., BLAIR, C. D. & BEATY, B. J. ( 2002). La Crosse virus: replication in vertebrate and invertebrate hosts. Microbes and Infection 4, 341–350.CrossRefGoogle Scholar
BROSSARD, M. ( 1982). Rabbits infested with adult Ixodes ricinus L.: effects of mepyramine on acquired resistance. Experientia 38, 702–704.Google Scholar
CHRISTE, M., RUTTI, B. & BROSSARD, M. ( 2000). Cytokines (IL-4 and IFN-gamma) and antibodies (IgE and IgG2a) produced in mice infected with Borrelia burgdorferi sensu stricto via nymphs of Ixodes ricinus ticks or syringe inoculations. Parasitology Research 86, 491–496.CrossRefGoogle Scholar
CIRINO, G., NAPOLI, C., BUCCI, M. & CICALA, C. ( 2000). Inflammation-coagulation network: are serine protease receptors the knot? Trends in Pharmacological Science 21, 170–172.Google Scholar
COUILLIN, I., VARGAFTIG, B. B., JACOBS, M., PAESEN, G. C., NUTTALL, P., MAILLET, I., LEFORT, J., MOSER, R., WESTON-DAVIES, W. & RYFFEL, B. ( 2004). Arthropod-derived histamine binding protein prevents murine allergic asthma. Journal of Immunology (in press).CrossRefGoogle Scholar
DESSENS, J. T. & NUTTALL, P. A. ( 1998). Mx1-Based resistance to Thogoto virus in A2G mice is bypassed in tick-mediated virus delivery. Journal of Virology 72, 8362–8364.Google Scholar
EDWARDS, J. F., HIGGS, S. & BEATY, B. J. ( 1998). Mosquito feeding-induced enhancement of Cache Valley virus (Bunyaviridae) infection in mice. Journal of Medical Entomology 35, 261–265.CrossRefGoogle Scholar
EMBER, J. A., JAGELS, M. A. & HUGLI, T. E. ( 1998). Characterisation of complement anaphylatoxins and their biological responses. In The Human Complement System in Health and Disease (ed. Volanakis, J. E. & Frank, M. M.), pp. 241–284. New York, Marcel Dekker.CrossRef
FRANCES, S. P., WATCHARAPICHAT, P., PHULSUKSOMBATI, D. & TANSKUL, P. ( 2000). Transmission of Orientia tsutsugamushi, the aetiological agent of scrub typhus, to co-feeding mites. Parasitology 120, 601–607.CrossRefGoogle Scholar
FUJISAKI, K., KAMIO, T. & KITAOKA, S. ( 1984). Passage of host serum components, including antibodies specific for Theileria sergenti, across the digestive tract of argasid and ixodid ticks. Annals of Tropical Medicine and Parasitology 78, 449–450.CrossRefGoogle Scholar
GERN, L. & RAIS, O. ( 1996). Efficient transmission of Borrelia burgdorferi between cofeeding Ixodes ricinus ticks (Acari: Ixodidae). Journal of Medical Entomology 33, 189–192.CrossRefGoogle Scholar
GILLESPIE, R. D., DOLAN, M. C., PIESMAN, J. & TITUS, R. G. ( 2001). Identification of an IL-2 binding protein in the saliva of the Lyme disease vector tick, Ixodes scapularis. Journal of Immunology 166, 4319–4327.CrossRefGoogle Scholar
GOFF, W., JOHNSON, W., HORN, R., BARRINGTON, G. & KNOWLES, D. ( 2003). The innate response in calves to Boophilus microplus tick transmitted Babesia bovis involves type-1 cytokine induction and NK-like cells in the spleen. Parasite Immunology 25, 185–188.CrossRefGoogle Scholar
GOODBOURN, S., DIDCOCK, L. & RANDALL, R. E. ( 2000). Interferons: cell signalling, immune modulation, antiviral responses and virus countermeasures. Journal of General Virology 81, 2341–2364.CrossRefGoogle Scholar
GORDON, S. W., LINTHICUM, K. J. & MOULTON, J. R. ( 1993). Transmission of Crimean-Congo hemorrhagic fever virus in two species of Hyalomma ticks from infected adults to cofeeding immature forms. American Journal of Tropical Medicine and Hygiene 48, 576–580.CrossRefGoogle Scholar
HAGMAIER, K., JENNINGS, S., BUSE, J., WEBER, F. & KOCHS, G. ( 2003). Novel gene product of Thogoto virus segment 6 codes for an interferon antagonist. Journal of Virology 77, 2747–2752.CrossRefGoogle Scholar
HAJNICKÁ, V., FUCHSBERGER, N., SLOVAK, M., KOCAKOVA, P., LABUDA, M. & NUTTALL, P. A. ( 1998). Tick salivary glands extracts promote virus growth in vitro. Parasitology 116, 533–538.CrossRefGoogle Scholar
HAJNICKÁ, V., KOCÁKOVÁ, P., SLÁVIKOVÁ, M., SLOVÁK, M., GAšPERÍK, J., FUCHSBERGER, N. & NUTTALL, P. A. ( 2001). Anti-interleukin-8 activity of tick salivary gland extracts. Parasite Immunology 23, 483–489.CrossRefGoogle Scholar
HAJNICKÁ, V., KOCÁKOVÁ, P., SLOVÁK, M., LABUDA, M., FUCHSBERGER, N. & NUTTALL, P. A. ( 2000). Inhibition of the antiviral action of interferon by tick salivary gland extract. Parasite Immunology 22, 201–206.CrossRefGoogle Scholar
HALLER, O., ACKLIN, M. & STAEHLI, P. ( 1987). Influenza virus resistance in wild mice: wild-type and mutant Mx alleles occur at comparable frequencies. Journal of Interferon Research 7, 647–656.CrossRefGoogle Scholar
HALLER, O., FRESE, M., ROST, D., NUTTALL, P. A. & KOCHS, G. ( 1995). Tick-borne Thogoto virus infection in mice is inhibited by the orthomyxovirus resistance gene product Mx 1. Journal of Virology 69, 2596–2601.Google Scholar
HANNIER, S., LIVERSIDGE, J., STERNBERG, J. M. & BOWMAN, A. S. ( 2003). Ixodes ricinus tick salivary gland extract inhibits IL-10 secretion and CD69 expression by mitogen-stimulated murine splenocytes and induces hyporesponsiveness in B lymphocytes. Parasite Immunology 25, 27–37.CrossRefGoogle Scholar
HELLWAGE, J., MERI, T., HEIKKILA, T., ALITALO, A., PANELIUS, J., LAHDENNE, P., SEPPALA, I. J. T. & MERI, S. ( 2001). The complement regulator factor H binds to the surface protein OspE of Borrelia burgdorferi. Journal of Biological Chemistry 276, 8427–8435.CrossRefGoogle Scholar
HODZIC, E., BORJESSON, D. L., FENG, S. & BARTHOLD, S. W. ( 2001). Acquisition dynamics of Borrelia burgdorferi and the agent of human granulocytic ehrlichiosis at the host-vector interface. Vector Borne Zoonotic Disease 1, 149–158.CrossRefGoogle Scholar
JASINSKAS, A., JAWORSKI, D. C. & BARBOUR, A. G. ( 2000). Amblyomma americanum: specific uptake of immunoglobulins into tick hemolymph during feeding. Experimental Parasitology 96, 213–221.CrossRefGoogle Scholar
JAWORSKI, D. C., JASINSKAS, A., METZ, C. N., BUCALA, R. & BARBOUR, A. G. ( 2001). Identification and characterization of a homologue of the pro-inflammatory cytokine Macrophage Migration Inhibitory Factor in the tick, Amblyomma americanum. Insect Molecular Biology 10, 323–331.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, 775–777.CrossRefGoogle Scholar
JONES, L. D., DAVIES, C. R., WILLIAMS, T., CORY, J. & NUTTALL, P. A. ( 1990 b). Non-viraemic transmission of Thogoto virus: vector efficiency of Rhipicephalus appendiculatus and Amblyomma variegatum. Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 846–848.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, 172–176.CrossRefGoogle Scholar
JONES, L. D., HODGSON, E. & NUTTALL, P. A. ( 1989). Enhancement of virus transmission by tick salivary glands. Journal of General Virology 70, 1895–1898.CrossRefGoogle Scholar
JONES, L. D., HODGSON, E. & NUTTALL, P. A. ( 1990 a). Characterization of tick salivary gland factor(s) that enhance Thogoto virus transmission. Archives of Virology (Suppl.) 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, 261–265.Google 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, 779–782.Google Scholar
JONES, L. D., MATTHEWSON, M. & NUTTALL, P. A. ( 1992 c). Saliva-activated transmission (SAT) of Thogoto virus: dynamics of SAT activity in the salivary glands of Rhipicephalus appendiculatus, Amblyomma variegatum, and Boophilus microplus. Experimental and Applied Acarology 13, 241–248.Google Scholar
JONES, L. D. & NUTTALL, P. A. ( 1989). The effect of virus-immune hosts on Thogoto virus infection of the tick, Rhipicephalus appendiculatus. Virus Research 14, 129–140.CrossRefGoogle Scholar
KEMP, D. H., STONE, B. F. & BINNINGTON, K. C. ( 1982). Tick attachment and feeding: Role of the mouthparts, feeding apparatus, salivary gland secretions and host response. In Physiology of Ticks (ed. Obenchain, F. D. & Galun, R.), pp. 119–168. Oxford, Pergamon Press.CrossRef
KOCAN, K. M. & DE LA FUENTE, J. ( 2003). Co-feeding studies of ticks infected with Anaplasma marginale. Veterinary Parasitology 112, 295–305.CrossRefGoogle Scholar
KOHL, J. ( 2001). Anaphylatoxins and infectious and non-infectious inflammatory diseases. Molecular Immunology 38, 175–187.CrossRefGoogle Scholar
KOPECKY, J. & KUTHEJLOVA, M. ( 1998). Suppressive effect of Ixodes ricinus salivary gland extract on mechanisms of natural immunity in vitro. Parasite Immunology 20, 169–174.Google Scholar
KROCOKA, Z., MACELA, A., HERNYCHOVA, L., KROCA, M., PECHOVA, J. & KOPECKY, J. ( 2003). Tick salivary gland extract accelerates proliferation of Franciscella tularensis in the host. Journal of Parasitology 89, 14–20.CrossRefGoogle Scholar
KUBEš, 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, 113–116.Google Scholar
KUBEš, M., KOCÁKOVÁ, P., SLOVÁK, M., SLÁVIKOVÁ, M., FUCHSBERGER, N. & NUTTALL, P. A. ( 2002). Heterogenity in the effect of different ixodid tick species on human natural killer cell activity. Parasite Immunology 24, 23–28.CrossRefGoogle Scholar
KURTENBACH, K., SEWELL, H., OGDEN, N., RANDOLPH, S. E. & NUTTALL, P. A. ( 1998). Serum complement sensitivity as a key factor in Lyme disease ecology. Infection and Immunity 66, 1248–1251.Google Scholar
KUTHEJLOVA, M., KOPECKY, J., STEPANOVA, G. & MACELA, A. ( 2001). Tick salivary gland extract inhibits killing of Borrelia afzelii spirochaetes by mouse macrophages. Infection and Immunity 69, 575–578.CrossRefGoogle Scholar
LABUDA, M., ALVES, M. J., ELECKOVA, E., KOZUCH, O. & FILIPE, A. R. ( 1997 a). Transmission of tick-borne bunyaviruses by cofeeding ixodid ticks. Acta Virologica 41, 325–328.Google Scholar
LABUDA, M., JONES, L. D., WILLIAMS, T., DANIELOVA, D. & NUTTALL, P. A. ( 1993 a). Efficient transmission of tick-borne encephalitis virus between cofeeding ticks. Journal of Medical Entomology 30, 295–299.Google 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, 193–196.Google Scholar
LABUDA, M., KOZUCH, O., ZUFFOVA, E., ELECKOVA, E., HAILS, R. S. & NUTTALL, P. A. ( 1997 b). Tick-borne encephalitis virus transmission between ticks co-feeding on specific immune natural rodent hosts. Virology 235, 138–143.Google 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, 802–805.Google Scholar
LANIER, L. ( 2000). The origin and functions of natural killer cells. Clinical Immunology 95, S14–S18.CrossRefGoogle Scholar
LAW, S. K. & REID, K. B. M. ( 1995). Complement. New York, Oxford University Press.
LAWRIE, C. H., RANDOLPH, S. E. & NUTTALL, P. A. ( 1999). Ixodes ticks: serum species sensitivity of anti-complement activity. Experimental Parasitology 93, 207–214.CrossRefGoogle Scholar
LAWRIE, C. H., SIM, R. B. & NUTTALL, P. A. ( 2004). Investigation of the mechanisms of anti-complement activity in Ixodes ticks. Molecular Immunology (in press).Google Scholar
LAWRIE, C. H., UZCATEGUI, N. Y., GOULD, E. A. & NUTTALL, P. A. ( 2004). Ixodid and argasid ticks and West Nile virus. Emerging Infectious Diseases 10, 653–657.CrossRefGoogle Scholar
MA, Y. & WEIS, J. ( 1993). Borrelia burgdorferi outer surface lipoproteins OspA and OspB possess B-cell mitogenic and cytokine-stimulatory properties. Infection and Immunity 61, 3843–3853.Google Scholar
MBOW, M. L., ZEIDNER, N. S., GILMORE, R. D. J., DOLAN, M., PIESMAN, J. & TITUS, R. G. ( 2001). Major histocompatibility complex class II-independent generation of neutralizing antibodies against T-cell-dependent Borrrelia burgdorferi antigens presented by dendritic cells: regulation by NK and γδ T cells. Infection and Immunity 69, 2407–2425.CrossRefGoogle Scholar
MEAD, D. G., RAMBERG, F. B., BESSELSEN, D. G. & MARE, C. J. ( 2000). Transmission of vesicular stomatitis virus from infected to uninfected black flies co-feeding on nonviremic deer mice. Science 287, 485–487.CrossRefGoogle Scholar
MINOURA, H., CHINZEI, Y. & KITAMURA, S. ( 1985). Ornithodoros moubata: host immunoglobulin G in tick haemolymph. Experimental Parasitology 60, 355–363.CrossRefGoogle Scholar
MULENGA, A., MACALUSO, K. R., SIMSER, J. A. & AZAD, A. F. ( 2003). The Amercian dog tick, Dermacentor variabilis, encodes a functional histamine release factor homolog. Insect Biochemistry and Molecular Biology 33, 911–919.CrossRefGoogle Scholar
NUNN, M. A., SHARMA, A., PAESEN, G. C., ADAMSON, S., WILLIS, A. C. & NUTTALL, P. A. ( 2004). Complement inhibitor of C5 activation from the soft tick Ornithodoros moubata. Journal of Immunology (in press).Google Scholar
NUTTALL, P. A. ( 1998). Displaced tick-parasite interactions at the host interface. Parasitology 116 (Suppl.), S65–S72.CrossRefGoogle Scholar
NUTTALL, P. A. & JONES, L. D. ( 1991). Non-viraemic tick-borne virus transmission: mechanism and significance. In Modern Acarology (ed. Dusbabek, F. & Bukva, V.), pp. 3–6. Prague and The Hague, Academia and SPB Academic Publishing bv.
NUTTALL, P. A. & LABUDA, M. ( 2003). Dynamics of infection in tick vectors and at the tick-host interface. Advances in Virus Research 60, 233–272.CrossRefGoogle Scholar
OCHSENBEIN, A. F., FEHR, T., LUTZ, C., SUTER, M., BROMBACHER, F., HENGARTNER, H. & ZINKERNAGEL, R. ( 1999). Control of early viral and bacterial distribution and disease by natural antibodies. Science 286, 2156–2159.CrossRefGoogle Scholar
OSORIO, J. E., GODSEY, M. S., DEFOLIART, G. R. & YUILL, T. M. ( 1996). La Crosse viremias in white-tailed deer and chipmunks exposed by injection or mosquito bite. American Journal of Tropical Medicine and Hygiene 54, 338–342.CrossRefGoogle Scholar
PACKILA, M. & GUILFOILE, P. G. ( 2002). Mating, male Ixodes scapularis express several genes including those with sequence similarity to immunoglobulin-binding proteins and metalloproteases. Experimental and Applied Acarology 27, 151–160.CrossRefGoogle Scholar
PAESEN, G. C., ADAMS, P. L., HARLOS, K., NUTTALL, P. A. & STUART, D. I. ( 1999). Tick histamine-binding proteins: isolation, cloning, and three-dimensional structure. Molecular Cell 3, 661–671.CrossRefGoogle Scholar
PAESEN, G. C., ADAMS, P. L., NUTTALL, P. A. & STUART, D. L. ( 2000). Tick histamine-binding proteins: lipocalins with a second binding cavity. Biochimica et Biophysica Acta 1482, 92–101.CrossRefGoogle Scholar
PATRICAN, L. ( 1997). Acquisition of Lyme disease spirochetes by cofeeding Ixodes scapularis ticks. American Journal of Tropical Medicine and Hygiene 57, 589–593.CrossRefGoogle Scholar
PAUSA, M. P. V., CINCO, M., GIULIANINI, P. G., PRESANI, G., PERTICARARI, S., MURGIA, R. & TEDESCO, F. ( 2003). Serum-resistant strains of Borrelia burgdorferi evade complement-mediated killing by expressing a CD59-like complement inhibitory molecule. Journal of Immunology 170, 3214–3222.CrossRefGoogle Scholar
PECHOVA, J., STEPANOVA, G., KOVAR, L. & KOPECKY, J. ( 2002). Tick salivary gland extract-activated transmission of Borrelia afzelii spirochaetes. Folia Parasitologica 49, 153–159.CrossRefGoogle Scholar
RANDOLPH, S. E., GERN, L. & NUTTALL, P. A. ( 1996). Co-feeding ticks: epidemiological significance for tick-borne pathogen transmission. Parasitology Today 12, 472–479.CrossRefGoogle Scholar
RANDOLPH, S. E., MIKLISOVA, D., LYSY, J., ROGERS, D. J. & LABUDA, M. ( 1999). Incidence from coincidence: patterns of tick infestations on rodents facilitate transmission of tick-borne encephalitis virus. Parasitology 118, 177–186.CrossRefGoogle Scholar
RIBEIRO, J. M. C. ( 1987). Ixodes dammini: salivary anti-complement activity. Experimental Parasitology 64, 347–353.CrossRefGoogle Scholar
RIBEIRO, J. & SPIELMAN, A. ( 1986). Ixodes dammini: salivary anaphylatoxin inactivating activity. Experimental Parasitology 62, 292–297.CrossRefGoogle Scholar
RIBEIRO, J. M. C., WEISS, J. J. & TELFORD, S. R. III ( 1990). Saliva of the tick Ixodes dammini inhibits neutrophil function. Experimental Parasitology 70, 382–388.CrossRefGoogle Scholar
RICHTER, D., ALLGOWER, R. & MATUSCHKA, F.-R. ( 2002). Co-feeding transmission and its contribution to the perpetuation of the Lyme disease spirochaete Borrelia afzelii. Emerging Infectious Diseases 8, 1421–1425.CrossRefGoogle Scholar
RUDOLF, I. & HUBALEK, Z. ( 2003). Effect of the salivary gland and midgut extracts from Ixodes ricinus and Dermacentor reticulatus (Acari: Ixodidae) on the growth of Borrelia garinii in vitro. Folia Parasitologica 50, 159–160.CrossRefGoogle Scholar
SATO, Y. & NAKAO, M. ( 1997). Transmission of the Lyme disease spirochaete, Borrelia garinii, between infected and uninfected Ixodes persulcatus during cofeeding on mice. Journal of Parasitology 83, 547–550.CrossRefGoogle Scholar
SHAW, M. K., TILNEY, L. G. & McKEEVER, D. J. ( 1993). Tick salivary gland extract and interleukin-2 stimulation enhance susceptibility of lymphocytes to infection by Theileria parva sporozoites. Infection and Immunity 61, 1486–1495.Google Scholar
SHIH, C.-M., CHAO, L. L. & YU, C. P. ( 2002). Chemotactic migration of the Lyme disease spirochete (Borrelia burgdorferi) to salivary gland extracts of vector ticks. American Journal of Tropical Medicine and Hygiene 66, 616–621.CrossRefGoogle Scholar
SINGH, K. R. P., GOVERDHAN, M. K. & BHAT, U. K. M. ( 1971). Transmission of Kyasanur forest disease virus by soft tick, Argas persicus (Ixodoidea: Argasidae). Indian Journal of Medical Research 59, 213–218.Google Scholar
STARK, G. R., KERR, I. M., WILLIAMS, B. R., SILVERMAN, R. H. & SCHREIBER, R. D. ( 1998). How cells respond to interferons. Annual Review of Biochemistry 67, 227–254.CrossRefGoogle Scholar
STEBBINGS, J. H. J. ( 1974). Immediate hypersensitivity: a defense against arthropods? Perspectives in Biology and Medicine 17, 233–239.Google Scholar
STEELE, G. M. & NUTTALL, P. A. ( 1989). Difference in vector competence of two species of sympatric ticks, Amblyomma variegatum and Rhipicephalus appendiculatus, for Dugbe virus (Nairovirus, Bunyaviridae). Virus Research 14, 73–84.CrossRefGoogle Scholar
SUHONEN, J., HARTIALA, K. & VILJANEN, M. K. ( 1998). Tube phagocytosis, a novel way for neutrophils to phagocytize Borrelia burgdorferi. Infection and Immunity 66, 3433–3435.Google Scholar
TAKAMATSU, H., MELLOR, P. S., MERTENS, P. P., KIRKHAM, P. A., BURROUGHS, J. N. & PARKHOUSE, R. M. ( 2003). A possible overwintering mechanism for bluetongue virus in the absence of the insect vector. Journal of General Virology 84, 227–235.CrossRefGoogle Scholar
TAKESHITA, K., SAKAI, K., BACON, K. B. & GANTNER, F. ( 2003). Critical role of histamine H4 receptor in leukotriene B4 production and mast cell-dependent neutrophil recruitment inuced by zymosan in vivo. Journal of Pharmacology and Experimental Therapeutics 307, 1–7.Google Scholar
TITUS, R. G. & RIBEIRO, J. C. ( 1988). Salivary gland lysates from the sandfly Lutzomyia longipalpis enhance Leishmania infectivity. Science 239, 1306–1308.CrossRefGoogle Scholar
ULLMANN, A. J., LANE, R. S., KURTENBACH, K., MILLER, M., SCHRIEFER, M. E., ZELDNER, N. & PIESMAN, J. ( 2003). Bacteriolytic activity of selected vertebrate sera for Borrelia burgdorferi sensu stricto and Borrelia bissettii. Journal of Parasitology 89, 1256–1257.CrossRefGoogle Scholar
VALENZUELA, J. G., CHARLAB, R., MATHER, T. N. & RIBEIRO, J. M. C. ( 2000). Purification, cloning, and expression of a novel salivary anticomplement protein from the tick, Ixodes scapularis. Journal of Biological Chemistry 275, 18717–18723.CrossRefGoogle Scholar
VAN DAM, A. P. ( 2002). Diversity of Ixodes-borne Borrelia species: clinical, pathogenetic, and diagnostic implications and impact on vaccine development. Vector Borne Zoonotic Disease 2, 249–254.CrossRefGoogle Scholar
VAN DAM, A. P., OEI, A., JASPARS, R., FIJEN, C., WILSKE, B., SPANJAARD, L. & DANKERT, J. ( 1997). Complement-mediated serum sensitivity among spirochetes that cause Lyme disease. Infection and Immunity 65, 1228–1236.Google Scholar
WANG, H. & NUTTALL, P. A. ( 1994). Excretion of host immunoglobulin in tick saliva and detection of IgG-binding proteins in tick haemolymph and salivary glands. Parasitology 109, 525–530.CrossRefGoogle Scholar
WANG, H. & NUTTALL, P. A. ( 1999). Immunoglobulin binding proteins in ticks: new target for vaccine development against a blood-feeding parasite. Cellular and Molecular Life Sciences 56, 286–295.CrossRefGoogle Scholar
WANG, H., PAESEN, G. C., NUTTALL, P. A. & BARBOUR, A. G. ( 1998). Male ticks help their mates to feed. Nature 391, 753–754.CrossRefGoogle Scholar
WIKEL, S. K. ( 1982). Histamine content of tick attachment sites and the effects of H1 and H2 histamine antagonists on the expression of resistance. Annals of Tropical Medicine and Parasitology 76, 179–185.CrossRefGoogle Scholar
WIKEL, S. K. ( 1985). Effect of tick infestation on the plaque-forming cell response to a thymic dependent antigen. Annals of Tropical Medicine and Parasitology 79, 195–198.CrossRefGoogle Scholar
WIKEL, S. K. & ALLEN, J. R. ( 1977). Acquired resistance to ticks. III. Cobra venom factor and the resistance response. Immunology 32, 457–465.Google Scholar
WIKEL, S. K., RAMACHANDRA, R. N., BERGMAN, D. K., BURKOT, T. R. & PIESMAN, J. ( 1997). Infestation with pathogen-free nymphs of the tick Ixodes scapularis induces host resistance to transmission of Borrelia burgdorferi by ticks. Infection and Immunity 65, 335–338.Google Scholar
WILLADSEN, P., WOOD, G. M. & RIDING, G. A. ( 1979). The relation between skin histamine concentration, histamine sensitivity and the resistance of cattle to the tick Boophilus microplus. Zeitschrift für Parasitenkunde 59, 87–93.CrossRefGoogle Scholar
ZEIDNER, N., DREITZ, M., BELASCO, W. & FISH, D. ( 1996). Suppression of acute Ixodes scapularis-induced Borrelia burgdorferi infection using tumour necrosis factor-alpha, interleukin-2 and interferon-gamma. Journal of Infectious Diseases 173, 187–195.CrossRefGoogle Scholar
ZEIDNER, N., MBOW, M., DOLAN, M., BACCA, E., MASSLING, R. & PIESMAN, J. ( 1997). Effects of Ixodes scapularis and Borrelia burgdorferi on modulation of the host immune response: Induction of the Th2 cytokine response in Lyme disease-susceptible (C3H/HeJ) mice but not in disease-resistant (BALB/c) mice. Infection and Immunity 65, 3100–3106.Google Scholar
ZEIDNER, N. S., SCHNEIDER, B. S., NUNCIO, M. S., GERN, L. & PIESMAN, J. ( 2002). Coinoculation of Borrelia spp. with tick salivary gland lysate enhances spirochaete load in mice and is tick species-specific. Journal of Parasitology 88, 1276–1278.Google Scholar
ZELLER, H. G., CORNET, J.-P. & CAMICAS, J.-L. ( 1994). Experimental transmission of Crimean-Congo hemorrhagic fever virus by West African wild ground-feeding birds to Hyalomma marginatum rufipes ticks. American Journal of Tropical Medicine and Hygiene 50, 676–681.CrossRefGoogle Scholar