Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-26T17:44:15.776Z Has data issue: false hasContentIssue false

Tick immunobiology

Published online by Cambridge University Press:  19 April 2005

M. BROSSARD
Affiliation:
Institute of Zoology, University of Neuchatel, Emile-Argand 11, CH-2007, Neuchatel, Switzerland
S. K. WIKEL
Affiliation:
Center for Microbial Pathogenesis, School of Medicine, University of Connecticut Health Center, 263 Farmington Avenue, MC3710, Farmington, CT 06030, USA

Abstract

Ticks are of vast medical and veterinary public health importance due to direct damage caused by feeding and their roles in transmitting well known and emerging infectious agents. Ticks and tick-borne pathogens stimulate the immune system of the host. Those immune interactions are of importance in tick biology, pathogen transmission and control of ticks and tick-borne diseases. Both innate and specific acquired immune defenses are involved in the responses of vertebrate hosts to infestation. Ticks have evolved countermeasures to circumvent host immune defenses. This review addresses the immunobiology of the tick–host interface from the perspectives of the pharmacology of tick saliva; relationship of tick saliva to pathogen transmission; host immune responses to infestation; tick modulation of host immune defences; and genomic/proteomic strategies for studying tick salivary gland molecules.

Type
Research Article
Copyright
© 2004 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

ADAMS, M. D., KELLEY, J. M., GOCAYNE, J. D., DUBNICK, M., POLYMEROPOULOS, M. H., XIAO, H., MERRIL, C. R., WU, A., OLDE, B., MORENS, D. M., KERLAVAGE, A. R., McCONNELL, D. J. & VENTER, J. C. ( 1991). Complementary DNA sequencing: Expressed sequence tags and human genome project. Science 252, 16511656.CrossRefGoogle Scholar
ALJAMALI, M. N., BIOR, A. D., SAUER, J. R. & ESSENBERG, R. C. ( 2003). RNA interference in ticks: a study using histamine binding protein dsRNA in the female tick Amblyomma americanum. Insect Molecular Biology 12, 299305.CrossRefGoogle Scholar
ALLEN, J. R. ( 1973). Tick resistance: basophils in skin reactions of resistant guinea pigs. International Journal for Parasitology 3, 195200.CrossRefGoogle Scholar
ALLEN, J. R., DOUBE, B. M. & KEMP, D. H. ( 1977). Histology of bovine skin reactions to Ixodes holocyclus, Neuman. Canadian Journal of Comparative Medicine 41, 2635.Google Scholar
ALLEN, J. R. & HUMPHREYS, S. J. ( 1979). Immunisation of guinea pigs and cattle against ticks. Nature 280, 491493.CrossRefGoogle Scholar
ALLEN, J. R., KHALIL, H. M. & WIKEL, S. K. ( 1979). Langerhans cells trap tick salivary gland antigens in tick-resistant guinea pigs. Journal of Immunology 122, 563565.Google Scholar
ANGUITA, J., RAMAMOORTHI, N., HOVIUS, J. W. R., DAS, S., THOMAS, V., PERSINSKI, R., CONZE, D., ASKENASE, P. W., RINCON, M., KANTOR, F. S. & FIKRIG, E. ( 2002). Salp15, and Ixodes scapularis salivary protein, inhibits CD4+ T cell activation. Immunity 16, 849859.CrossRefGoogle Scholar
ASKENASE, P. W., DEBERNARDO, R., TAUBEN, D. & KASHGARIAN, M. ( 1978). Cutaneous basophil anaphylaxis. Immediate vasopermeability increases and anaphylactic degranulation of basophils at delayed hypersensitivity reactions challenged with additional antigen. Immunology 35, 741755.Google Scholar
BELL, J. F., STEWART, S. J. & WIKEL, S. K. ( 1979). Resistance to tick-borne Francisella tularensis by tick-sensitized rabbits: allergic klendusity. American Journal of Tropical Medicine and Hygiene 28, 876880.CrossRefGoogle Scholar
BENEDICT, C., KUWAHARA, K., TODD, G., RYAN, J., MICHALAK, M., EATON, D. & STERN, D. ( 1993). Calreticulin is a novel antithrombotic agent: blockage of electrically induced coronary thrombosis. Clinical Research 41, 275A.Google Scholar
BERGMAN, D. K., PALMER, M. J., CAIMANO, M. J., RADOLF, J. D. & WIKEL, S. K. ( 2000). Isolation and cloning of a secreted immunosuppressant protein from Dermacentor andersoni salivary gland. Journal of Parasitology 86, 516525.CrossRefGoogle Scholar
BERGMAN, D. K., RAMACHANDRA, R. N. & WIKEL, S. K. ( 1998). Characterization of an immunosuppressant protein from Dermacentor andersoni (Acari: Ixodidae) salivary glands. Journal of Medical Entomology 35, 505509.CrossRefGoogle Scholar
BERTHIER, R., MARTINON-EGO, C., LAHARIE, A. M. & MARCHE, P. N. ( 2000). A two-step culture method starting with early growth factors permits enhanced production of functional dendritic cells from murine splenocytes. Journal of Immunological Methods 239, 95107.CrossRefGoogle Scholar
BIOR, A. D., ESSENBERG, R. C. & SAUER, J. R. ( 2002). Comparison of differentially expressed genes in the salivary glands of male ticks, Amblyomma americanum and Dermacentor andersoni. Insect Biochemistry and Molecular Biology 32, 645655.CrossRefGoogle Scholar
BOWESSIDJAOU, J., BROSSARD, M. & AESCHLIMANN, A. ( 1977). Effects and duration of resistance acquired by rabbits on feeding and egg laying in Ixodes ricinus L. Experientia 33, 548550.CrossRefGoogle Scholar
BOWMAN, A. S., DILLWITH, J. W. & SAUER, J. R. ( 1996). Tick salivary prostaglandins: presence, origin and significance. Parasitology Today 12, 388396.CrossRefGoogle Scholar
BROSSARD, M. ( 1976). Relations immunologiques entre Bovins et Tiques, plus particulièrement entre Bovins et Boophilus microplus. Acta Tropica 33, 1536.Google Scholar
BROSSARD, M. ( 1982). Rabbits infested with adult Ixodes ricinus L.: effects of mepyramine on acquired resistance. Experientia 38, 702704.Google Scholar
BROSSARD, M. & FIVAZ, V. ( 1982). Ixodes ricinus L.: mast cells, basophils and eosinophils in the sequence of cellular events in the skin of infested or reinfested rabbits. Parasitology 85, 583592.Google Scholar
BROSSARD, M. & GIRARDIN, P. ( 1979). Passive transfer of resistance in rabbits infested with adult Ixodes ricinus L: Humoral factors influence feeding and egg laying. Experientia 35, 13951396.CrossRefGoogle Scholar
BROSSARD, M., MONNERON, J. P. & PAPTHEODOROU, V. ( 1982). Progressive sensitization of circulating basophils against Ixodes ricinus L. antigens during repeated infestations of rabbits. Parasite Immunology 4, 355361.Google Scholar
BROSSARD, M., RUTTI, B. & HAUG, T. ( 1991). Immunological relationship between hosts and ixodid ticks. In Parasite–Host Associations: Coexistence or Conflict? 1st Edn ( ed. Toft, C. A., Aeschlimann, A. & Bolis, L.), pp. 177200. New York: Oxford University Press.
BROSSARD, M. & WIKEL, S. K. ( 1997). Immunology of interactions between ticks and hosts. Medical and Veterinary Entomology 11, 270276.CrossRefGoogle Scholar
BROWN, S. J. & ASKENASE, P. W. ( 1981). Cutaneous basophil responses and immune resistance of guinea pigs to ticks: passive transfer with peritoneal exudate cells or serum. Journal of Immunology 127, 21632167.Google Scholar
BROWN, S. J., BARKER, R. W. & ASKENASE, P. W. ( 1984). Bovine resistance to Amblyomma americanum ticks: an acquired immune response characterized by cutaneous basophil infiltrates. Veterinary Parasitology 16, 147165.CrossRefGoogle Scholar
CHAMPAGNE, D. E. ( 1994). The role of salivary vasodilators in bloodfeeding and parasite transmission. Parasitology Today 10, 430433.CrossRefGoogle Scholar
CHAMPAGNE, D. E. & VALENZUELA, J. G. ( 1996). Pharmacology of haemathophagous arthropod saliva. In The Immunology of Host-Ectoparasitic Arthropod Relationships ( ed. Wikel, S. K.), pp. 85106. Wallingford: CAB International.
CHILDS, J. E. & PADDOCK, C. D. ( 2003). The ascendancy of Amblyomma americanum as a vector of pathogens affecting humans in the United States. Annual Review of Entomology 48, 307337.CrossRefGoogle Scholar
CHINERY, W. A. & AYITEY-SMITH, E. ( 1977). Histamine blocking agent in the salivary gland homogenate of the tick, Rhipicephalus sanguineus. Nature 265, 366367.CrossRefGoogle Scholar
CHRISTE, M., RUTTI, B. & BROSSARD, M. ( 1999). Influence of genetic background and parasite load of mice on immune response developed against nymphs of Ixodes ricinus. Parasitology Research 85, 557561.CrossRefGoogle Scholar
CHRISTE, M., RUTTI, B. & BROSSARD, M. ( 2000). Cytokines (IL-4 and IFN-γ) 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, 491496.CrossRefGoogle Scholar
COPPOLINO, M. G. & DEDHAR, S. ( 1998). Calreticulin. International Journal of Biochemistry and Cell Biology 30, 553558.CrossRefGoogle Scholar
CRAMPTON, A. L., MILLER, C., BAXTER, G. D. & BARKER, S. C. ( 1998). Expressed sequence tags and new genes from the cattle tick, Boophilus microplus. Experimental and Applied Acarology 22, 177186.CrossRefGoogle Scholar
CUMBERBATCH, M. & KIMBER, I. ( 1995). Tumour necrosis factor-α is required for accumulation of dendritic cells in draining lymph nodes and for optimal contact sensitization. Immunology 84, 3135.Google Scholar
DAS, S., BANERJEE, G., DEPONTE, K., MARCANTONIO, N., KANTOR, F. S. & FIKRIG, E. ( 2001). Salp 25D, an Ixodes scapularis antioxidant, is 1 of 14 immunodominant antigens in engorged tick salivary glands. Journal of Infectious Diseases 184, 10561064.CrossRefGoogle Scholar
DAS, S., MARCANTONIO, N., DEPONTE, K., TELFORD, S. R. III, ANDERSON, J. F., KANTOR, F. S. & FIKRIG, E. ( 2000). SALP 16, a gene induced in Ixodes scapularis salivary glands during tick feeding. American Journal of Tropical Medicine and Hygiene 62, 99105.CrossRefGoogle Scholar
DASZAK, P., CUNNINGHAM, A. A. & HYATT, A. D. ( 2000). Emerging infectious diseases of wildlife – threats to biodiversity and human health. Science 287, 443449.CrossRefGoogle Scholar
DE CASTRO, J. J. & NEWSON, R. M. ( 1993). Host resistance in cattle tick control. Parasitology Today 9, 1317.CrossRefGoogle Scholar
DEMEURE, C. E., YANG, L. P., DESJARDINS, C., RAYNAULD, P. & DELESPESSE, G. ( 1997). Prostaglandin E2 primes naive T cells for the production of anti-inflammatory cytokines. European Journal of Immunology 27, 35263531.CrossRefGoogle Scholar
DENHOLLANDER, N. & ALLEN, J. R. ( 1985). Dermacentor variabilis: acquired resistance to ticks in BALB/c mice. Experimental Parasitology 59, 118129.CrossRefGoogle Scholar
DENLI, A. M. & HANNON, G. J. ( 2003). RNAi: an ever-growing puzzle. Trends in Biochemical Sciences 28, 196201.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, 83628364.Google Scholar
DICKINSON, R. G., O'HAGAN, J. E., SHOTZ, M., BINNINGTON, K. C. & HEGARTY, M. P. ( 1976). Prostaglandin in saliva of the cattle tick Boophilus microplus. Australian Journal of Experimental Biology and Medical Sciences 54, 475486.CrossRefGoogle Scholar
DIZIJ, A., ARNDT, S., SEITZ, H. M. & KURTENBACH, K. ( 1994). Clethrionomys glareolus acquires resistance to Ixodes ricinus: a mechanism to prevent spirochete inoculation? In Advances in Lyme Borreliosis Research, Proceedings of the VI International Conference on Lyme Borreliosis ( ed. Cevenini, R., Sambi, V. & LaPlaca, M.), pp. 228231. Bologna, Italy.
DIZIJ, A. & KURTENBACH, K. ( 1995). Clethrionomys glareolus, but not Apodemus flavicollis, acquired resistance to Ixodes ricinus L., the main European vector of Borrelia burgdorferi. Parasite Immunology 17, 177183.Google Scholar
EDLOW, J. A. (ed.) ( 2002). Tick-borne diseases. Medical Clinics of North America 86, 205453.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, 261265.CrossRefGoogle Scholar
FEARON, D. T. ( 1998). The complement system and adaptive immunity. Seminars in Immunology 10, 355361.CrossRefGoogle Scholar
FERREIRA, B. R. & SILVA, J. S. ( 1999). Successive tick infestations selectively promote a T-helper 2 cytokine profile in mice. Immunology 96, 434439.CrossRefGoogle Scholar
FERREIRA, C. A. S., VAZ, I. D. S. Jr., DA SILVA, S. S., HAAG, K. L., VALENZUELA, J. G. & MASUDA, A. ( 2002). Cloning and partial characterization of a Boophilus microplus (Acari: Ixodidae) calreticulin. Experimental Parasitology 101, 2534.CrossRefGoogle Scholar
FIVAZ, B. H. ( 1989). Immune suppression induced by the brown ear tick Rhipicephalus appendiculatus Neumann, 1901. Journal of Parasitology 75, 946952.CrossRefGoogle Scholar
FUCHSBERGER, N., KITA, M., HAJNICKA, V., IMANISHI, J., LABUDA, M. & NUTTALL, P. A. ( 1995). Ixodid tick salivary gland extracts inhibit production of lipopolysaccharide-induced mRNA of several different human cytokines. Experimental and Applied Acarology 19, 671676.CrossRefGoogle Scholar
GANAPAMO, F. ( 1996). Mise en place et dynamique de la réponse immunitaire chez des souris BALB/c infestées par des nymphes de la tique Ixodes ricinus. PhD thesis, Université de Neuchâtel.
GANAPAMO, F., RUTTI, B. & BROSSARD, M. ( 1995). In vitro production of interleukin-4 and interferon-gamma by lymph node cells from BALB/c mice infested with nymphal Ixodes ricinus ticks. Immunology 85, 120124.Google Scholar
GANAPAMO, F., RUTTI, B. & BROSSARD, M. ( 1996 a). Cytokine production by lymph node cells from mice infested with Ixodes ricinus ticks and the effect of tick salivary gland extracts on IL-2 production. Scandinavian Journal of Immunology 44, 388393.Google Scholar
GANAPAMO, F., RUTTI, B. & BROSSARD, M. ( 1996 b). Immunosuppression and cytokine production in mice infested with Ixodes ricinus ticks: A possible role of laminin and interleukin-10 on the in vitro responsiveness of lymphocytes to mitogens. Immunology 87, 259263.Google Scholar
GANAPAMO, F., RUTTI, B. & BROSSARD, M. ( 1997). Identification of an Ixodes ricinus salivary gland fraction through its ability to stimulate CD4 T cells present in BALB/c mice lymph nodes draining the tick fixation site. Parasitology 115, 9196.CrossRefGoogle Scholar
GEORGE, J. E., OSBURN, R. L. & WIKEL, S. K. ( 1985). Acquisition and expression of resistance by Bos indicus and Bos indicus X Bos taurus calves to Amblyomma americanum infestation. Journal of Parasitology 71, 174182.CrossRefGoogle Scholar
GILL, H. S. ( 1986). Kinetics of mast cell, basophil and eosinophil populations at Hyalomma anatolicum anatolicum feeding sites on cattle and the acquisition of resistance. Parasitology 93, 305315.CrossRefGoogle Scholar
GILL, H. S. & WALKER, A. R. ( 1985). Differential cellular responses at Hyalomma anatolicum anatolicum feeding sites on susceptible and tick-resistant rabbits. Parasitology 91, 591607.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, 43194327.CrossRefGoogle Scholar
GILLESPIE, R. D., MBOW, M. L. & TITUS, R. G. ( 2000). The immunomodulatory factors of blood feeding arthropod saliva. Parasite Immunology 22, 319331.CrossRefGoogle Scholar
GIRARDIN, P. & BROSSARD, M. ( 1989). Effects of cyclosporin-A on the humoral immunity to ticks, and on the cutaneous immediate (type I) and delayed (type IV) hypersensitivity reactions to Ixodes ricinus, L. salivary gland antigens in re-infested rabbits. Parasitology Research 75, 657662.Google Scholar
GIRARDIN, P. & BROSSARD, M. ( 1990). Rabbits infested with Ixodes ricinus L. adults: Effects of treatment with cyclosporin A on the biology of ticks fed on resistant or naive hosts. Annals Parasitologie Human et Comparative 65, 262266.Google Scholar
GRATZ, N. G. ( 1999). Emerging and resurging vector-borne diseases. Annual Review of Entomology 44, 5175.CrossRefGoogle Scholar
GWAKISA, P., YOSHIHARA, K., TO, T. L., GOTOH, H., AMANO, F. & MOMOTANI, E. ( 2001). Salivary gland extract of Rhipicephalus appendiculatus ticks inhibits in vitro transcription and secretion of cytokines and production of nitric oxide by LPS-stimulated JA-4 cells. Veterinary Parasitology 99, 5361.CrossRefGoogle Scholar
HAJNICKÁ, V., FUCHSBERGER, N., SLOVAK, M., KOCAKOVA, P., LABUDA, M. & NUTTALL, P. A. ( 1998). Tick salivary gland extracts promote virus growth in vitro. Parasitology 116, 533538.CrossRefGoogle Scholar
HAJNICKÁ, V., KOCÁKOVÁ, P., SLÁVIKOVÁ, M., SLOVÁK, M., GASPERÍK, J., FUCHSBERGER, N. & NUTTALL, P. A. ( 2001). Anti-interleukin-8 activity of tick salivary gland extracts. Parasite Immunology 23, 483489.CrossRefGoogle Scholar
HAJNICKÁ, V., KOCAKOVA, P., SLOVAK, M., LABUDA, M., FUCHSBERGER, N. & NUTTALL, P. A. ( 2000). Inhibition of the antiviral action of interferon by tick salivary gland extract. Parasite Immunology 22, 201206.CrossRefGoogle 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, 2737.CrossRefGoogle Scholar
HARRIS, S. G., PADILLA, J., KOUMAS, L., RAY, D. & PHIPPS, R. P. ( 2002). Prostaglandins as modulators of immunity. Trends in Immunology 23, 144150.CrossRefGoogle Scholar
HIGGS, G. A., VANE, J. R., HART, R. J., PORTER, C. & WILSON, R. G. ( 1976). Prostaglandins in the saliva of the cattle tick, Boophilus microplus (Canestrini) (Acarina, Ixodidae). Bulletin of Entomological Research 66, 665670.CrossRefGoogle Scholar
HILL, C. A. & GUTIERREZ, J. A. ( 2000). Analysis of the expressed genome of the Lone Star tick, Amblyomma americanum (Acari: Ixodidae) using expressed sequence tag approach. Microbial and Comparative Genomics 5, 89101.CrossRefGoogle Scholar
INOKUMA, H., KEMP, D. H. & WILLADSEN, P. ( 1994). Prostaglandin E2 production by the cattle tick (Boophilus microplus) into feeding sites and its effect on the response of bovine mononuclear cells to mitogen. Veterinary Parasitology 53, 293299.CrossRefGoogle Scholar
JANEWAY, C. A. Jr., TRAVERS, P., WALPORT, M. & SHLOMCHIK, M. J. ( 2001). Immunobiology, 5th Edn. Garland Publishing, New York.
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 americaum. Insect Molecular Biology 10, 323331.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., HODGSON, E. & NUTTALL, P. A. ( 1989). Enhancement of virus transmission by tick salivary glands. Journal of General Virology 70, 18951898.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
KAUFMAN, W. R. ( 1989). Tick-host interaction: a synthesis of current concepts. Parasitology Today 5, 4756.CrossRefGoogle Scholar
KOCAKOVA, P., HAJNICKA, V., SLOVAK, M., NUTTALL, P. A. & FUCHSBERGER, N. ( 1999). Promotion of vesicular stomatitis virus nucleocapsid protein production by arthropod saliva. Acta Virologica 43, 251254.Google Scholar
KOPECKY, J. & KUTHEJLOVA, M. ( 1998). Suppressive effect of Ixodes ricinus salivary gland extract on mechanisms of natural immunity in vitro. Parasite Immunology 20, 169174.Google Scholar
KOUDSTAAL, D., KEMP, D. H. & KERR, J. D. ( 1978). Boophilus microplus: rejection of larvae from British breed cattle. Parasitology 76, 379386.CrossRefGoogle Scholar
KOVACS, H., CAMPBELL, I. D., STRONG, P., JOHNSON, S., WARD, F. J., REID, K. B. M. & EGGLETON, P. ( 1998). Evidence that C1q binds specifically to CH2-like immunoglobulin γ motifs present in the autoantigen calreticulin and interferes with complement activation. Biochemistry 37, 1786517874.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
KUBES, M., KOCAKOVA, P., SLOVAK, M., SLAVIKOVA, M., FUCHSBERGER, N. & NUTTALL, P. A. ( 2002). Heterogeneity in the effect of different ixodid tick species on natural killer cell activity. Parasite Immunology 24, 2328.CrossRefGoogle Scholar
KUTHEJLOVA, M., KOPECKY, J., STEPANOVA, G. & MACELA, A. ( 2001). Tick salivary gland extract inhibits killing of Borrelia afzelli spirochetes by mouse macrophages. Infection and Immunity 69, 575578.CrossRefGoogle Scholar
LABUDA, M., JONES, L. D., WILLIAMS, T. & NUTTALL, P. A. ( 1993). Enhancement of tick-borne encephalitis virus transmission by tick salivary gland extracts. Medical and Veterinary Entomology 7, 193196.CrossRefGoogle Scholar
LATIF, A. A. ( 1984). Resistance to Hyalomma anatolicum anatolicum Koch (1844) and Rhipicephalus evertsi Neumann (1897) (Ixodoidea:Ixodidae) by cattle in Sudan. Insect Science Applications 5, 509511.Google Scholar
LATIF, A. A., PUNYUA, D. K., CAPSTICK, P. B. & NEWSON, R. M. ( 1991). Tick infestations on Zebu cattle in Western Kenya: host resistance to Rhipicephalus appendiculatus (Acari: Ixodidae). Journal of Medical Entomology 28, 127132.CrossRefGoogle Scholar
LAWRIE, C. H., RANDOLPH, S. E. & NUTTALL, P. A. ( 1999). Ixodes ticks: serum species sensitivity of anti-complement activity. Experimental Parasitology 93, 207214.CrossRefGoogle Scholar
LEBOULLE, G., CRIPPA, M., DECREM, Y., MEJRI, N., BROSSARD, M., BOLLEN, A. & GODFROID, E. ( 2002 a). Characterization of a novel salivary immunosuppressive protein from Ixodes ricinus ticks. Journal of Biological Chemistry 277, 1008310089.Google Scholar
LEBOULLE, G., ROCHEZ, C., LOUAHED, J., RUTTI, B., BROSSARD, M., BOLLEN, A. & GODFROID, E. ( 2002 b). Isolation of Ixodes ricinus salivary gland mRNA encoding factors induced during blood feeding. American Journal of Tropical Medicine and Hygiene 66, 225233.Google Scholar
LUE, H., KLEEMAN, R., CALANDRA, T., ROGER, T. & BERNHAGEN, J. ( 2002). Macrophage migration inhibitory factor (MIF): mechanisms of action and role in disease. Microbes and Infection 4, 449460.CrossRefGoogle Scholar
MACALUSO, K. R. & WIKEL, S. K. ( 2001). Dermacentor andersoni: effects of repeated infestations on lymphocyte proliferation, cytokine production, and adhesion-molecule expression by BALB/c mice. Annals of Tropical Medicine and Parasitology 95, 413427.CrossRefGoogle Scholar
MASTELLOS, D. & LAMBRIS, J. D. ( 2002). Complement: more than a ‘guard’ against invading pathogens? Trends in Immunology 23, 485491.Google Scholar
MBOW, M. L., CHRISTE, M., RUTTI, B. & BROSSARD, M. ( 1994). Absence of acquired resistance to nymphal Ixodes ricinus ticks in BALB/c mice developing cutaneous reactions. Journal of Parasitology 80, 8187.CrossRefGoogle Scholar
MEJRI, N., FRANSCINI, N., RUTTI, B. & BROSSARD, M. ( 2001). Th2 polarization of the immune response of BALB/c mice to Ixodes ricinus instars, importance of several antigens in activation of specific Th2 subpopulations. Parasite Immunology 23, 6169.CrossRefGoogle 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. Parasitology Research 88, 192197.CrossRefGoogle Scholar
MITCHELL, M. ( 1996). Acaricide resistance – back to basics. Tropical Animal Production 28, 53S58S.CrossRefGoogle Scholar
MOLYNEUX, D. H. ( 1998). Vector-borne parasitic diseases – an overview of recent changes. International Journal for Parasitology 28, 927934.CrossRefGoogle Scholar
MOSMANN, T. R. & COFFMAN, R. L. ( 1989). Th1 and Th2 cells: Different patterns of lymphokine secretion lead to different functional properties. Annual Review of Immunology 7, 145173.CrossRefGoogle Scholar
NAZARIO, S., DAS, S., DE SILVA, A. M., DEPONTE, K., MARCANTONIO, N., ANDERSON, J. F., FISH, D., FIKRIG, E. & KANTOR, F. S. ( 1998). Prevention of Borrelia burgdorferi transmission in guinea pigs by tick immunity. American Journal of Tropical Medicine and Hygiene 58, 780785.CrossRefGoogle Scholar
NITHIUTHAI, S. & ALLEN, J. R. ( 1984 a). Significant changes in epidermal Langerhans cells of guinea-pigs infested with ticks (Dermacentor andersoni). Immunology 51, 133141.Google Scholar
NITHIUTHAI, S. & ALLEN, J. R. ( 1984 b). Effects of ultraviolet irradiation on the acquisition and expression of tick resistance in guinea-pigs. Immunology 51, 153159.Google 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, 661671.CrossRefGoogle Scholar
PAINE, S. H., KEMP, D. H. & ALLEN, J. R. ( 1983). In vitro feeding of Dermacentor andersoni (Stiles): effects of histamine and other mediators. Parasitology 86, 419428.CrossRefGoogle Scholar
PANDEY, A. & LEWITTER, F. ( 1999). Nucleotide sequence databases: A gold mine for biologists. Trends in Biochemical Sciences 24, 276280.CrossRefGoogle Scholar
PAPATHEODOROU, V. & BROSSARD, M. ( 1987). C3 levels in the sera of rabbits infested and reinfested with Ixodes ricinus L. and in midguts of fed ticks. Experimental and Applied Acarology 3, 5359.CrossRefGoogle Scholar
PAROLA, P. & RAOULT, D. ( 2001). Ticks and tickborne bacterial diseases in humans: an emerging infectious threat. Clinical Infectious Diseases 32, 897928.CrossRefGoogle Scholar
PETROVSKY, N. & BUCALA, R. ( 2000). Macrophage migration inhibitory factor (MIF) a critical neurohumoral mediator. Annals of the New York Academy of Sciences 917, 665671.CrossRefGoogle Scholar
RAMACHANDRA, R. N. & WIKEL, S. K. ( 1992). Modulation of host-immune responses by ticks (Acari: Ixodidae): effect of salivary gland extracts on host macrophages and lymphocyte cytokine production. Journal of Medical Entomology 29, 818826.CrossRefGoogle Scholar
RAMACHANDRA, R. N. & WIKEL, S. K. ( 1995). Effects of Dermacentor andersoni (Acari: Ixodidae) salivary gland extracts on Bos indicus and B. taurus lymphocytes and macrophages: in vitro cytokine elaboration and lymphocyte blastogenesis. Journal of Medical Entomology 32, 338345.Google Scholar
RIBEIRO, J. M. C. ( 1987). Role of saliva in blood-feeding by arthropods. Annual Review of Entomology 32, 463478.CrossRefGoogle Scholar
RIBEIRO, J. M. C. ( 1989). Role of saliva in tick/host interactions. Experimental and Applied Acarology 7, 1520.CrossRefGoogle Scholar
RIBEIRO, J. M. C. ( 1995 a). Blood-feeding arthropods: Live syringes or invertebrate pharmacologists? Infectious Agents and Disease 4, 143152.Google Scholar
RIBEIRO, J. M. C. ( 1995 b). How ticks make a living. Parasitology Today 11, 9193.Google Scholar
RIBEIRO, J. M. C., EVANS, P. M., McSWAIN, J. L. & SAUER, J. ( 1992). Amblyomma americanum: characterization of salivary prostaglandins E2 and F2 by RP-HPLC/bioassay and gas chromatography-mass spectrometry. Experimental Parasitology 74, 112116.CrossRefGoogle Scholar
RIBEIRO, J. M. C., MAKOUL, G. T., LEVINE, J., ROBINSON, D. R. & SPIELMAN, A. ( 1985). Antihemostatic, antiinflammatory, and immunosuppressive properties of the saliva of a tick, Ixodes dammini. Journal of Experimental Medicine 161, 332344.CrossRefGoogle Scholar
RIBEIRO, J. M. C. & MATHER, T. N. ( 1998). Ixodes scapularis: salivary kininase activity is a metallo dipeptidyl carboxypeptidase. Experimental Parasitology 89, 213221.CrossRefGoogle Scholar
RIBEIRO, J. M. C. & SPIELMAN, A. ( 1986). Ixodes dammini: salivary anaphylatoxin inactivating activity. Experimental Parasitology 62, 292297.CrossRefGoogle Scholar
ROBERTS, J. A. & KERR, J. D. ( 1976). Boophilus microplus: passive transfer of resistance in cattle. Journal of Parasitology 62, 485488.CrossRefGoogle Scholar
SAHIBI, H. F., RHALEM, A., TIKKI, N., BEN KOUKA, F. & BARRIGA, O. ( 1997). Hyalomma ticks: bovine resistance under field conditions as related to host age and breed. Parasite 4, 159165.CrossRefGoogle Scholar
SALMON, J. K., ARMSTRONG, C. A. & ANSEL, J. C. ( 1994). The skin as an immune organ. Western Journal of Medicine 160, 146152.Google Scholar
SANDERS, M. L., JAWORSKI, D. C., SANCHEZ, J. L., DEFRAITES, R. F., GLASS, G. E., SCOTT, A. L., RAHA, S., RITCHIE, B. C., NEEDHAM, G. R. & SCHWARTZ, B. S. ( 1998). 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 59, 279285.CrossRefGoogle Scholar
SANGAMNATDEJ, S., PAESEN, G. C., SLOVAK, M. & NUTTALL, P. A. ( 2002). A high affinity serotonin- and histamine-binding lipocalin from tick saliva. Insect Molecular Biology 11, 7986.CrossRefGoogle Scholar
SCHLEGER, A. V., LINCOLN, D. T., McKENNA, R. V., KEMP, D. H. & ROBERTS, J. A. ( 1976). Boophilus microplus: cellular responses to larval attachment and their relationship to host resistance. Australian Journal of Biological Science 29, 499512.CrossRefGoogle Scholar
SCHOELER, G. B., MANWEILER, S. A. & WIKEL, S. K. ( 2000). Cytokine responses of C3H/HeN mice infested with Ixodes scapularis or Ixodes pacificus nymphs. Parasite Immunology 22, 3140.CrossRefGoogle Scholar
SCHOELER, G. B. & WIKEL, S. K. ( 2001). Modulation of host immunity by haematophagous arthropods. Annals of Tropical Medicine and Parasitology 95, 755771.CrossRefGoogle Scholar
SCHORDERET, S. & BROSSARD, M. ( 1994). Effects of human recombinant interleukin-2 on the resistance, and on the humoral and cellular response of rabbits infested with adult Ixodes ricinus ticks. Veterinary Parasitology 54, 375387.CrossRefGoogle Scholar
SHAPIRO, E. D. ( 1998). Tick-borne diseases. Advances in Pediatric Infectious Diseases 13, 187218.Google 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, 14861495.Google Scholar
SONENSHINE, D. E. ( 1991). Biology of Ticks. Vol. 1. Oxford University Press, New York. p. 447.
SONENSHINE, D. E. ( 1993). Biology of Ticks. Vol. 2. Oxford University Press, New York. p. 465.
STEEVES, E. B. & ALLEN, J. R. ( 1991). Tick resistance in mast cell-deficient mice: histological studies. International Journal for Parasitology 21, 265268.CrossRefGoogle Scholar
TITUS, R. G. & RIBEIRO, J. M. C. ( 1988). Salivary gland lysates from the sand fly, Lutzomyia longipalpis, enhance Leishmania infectivity. Science 239, 13061308.CrossRefGoogle Scholar
TITUS, R. G. & RIBEIRO, J. M. C. ( 1990). The role of vector saliva in transmission of arthropod-borne disease. Parasitology Today 6, 157160.CrossRefGoogle Scholar
TRAGER, W. ( 1939). Acquired immunity to ticks. Journal of Parasitology 25, 5781.CrossRefGoogle Scholar
URIOSTE, S., HALL, L. R., TELFORD, S. R. III & TITUS, R. G. ( 1994). Saliva of the Lyme disease vector, Ixodes dammini, blocks cell activation by a nonprostaglandin E2-dependent mechanism. Journal of Experimental Medicine 180, 10771085.CrossRefGoogle Scholar
VALENZUELA, J. G. ( 2002 a). Editorial: exploring the messages of the salivary glands of Ixodes ricinus. American Journal of Tropical Medicine and Hygiene 66, 223224.Google Scholar
VALENZUELA, J. G. ( 2002 b). High-throughput approaches to study salivary proteins and genes from vectors of disease. Insect Biochemistry and Molecular Biology 32, 11991209.Google Scholar
VALENZUELA, J. G., BELKAID, Y., GARFIELD, M. K., MENDEZ, S., KAMHAWI, S., ROWTON, E. D., SACKS, D. L. & RIBEIRO, J. M. C. ( 2001). Toward a defined anti-Leishmania vaccine targeting vector antigens: characterization of a protective salivary protein. Journal of Experimental Medicine 194, 331342.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, 1871718723.CrossRefGoogle Scholar
VALENZUELA, J. G., FRANCISCHETTI, I. M. B., PHAM, V. M., GARFIELD, M. K., MATHER, T. N. & RIBEIRO, J. M. C. ( 2002). Exploring the sialome of the tick Ixodes scapularis. Journal of Experimental Biology 205, 28432864.Google Scholar
WALKER, D. H. ( 1998). Tick-transmitted infectious diseases in the United States. Annual Review of Public Health 19, 237269.CrossRefGoogle Scholar
WANG, H. & NUTTALL, P. A. ( 1994). Comparison of the proteins in salivary glands, saliva and haemolymph of Rhipicephalus appendiculatus female ticks during feeding. Parasitology 109, 517523.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., KAUFMAN, W. R. & NUTTALL, P. A. ( 1999). Molecular individuality: polymorphism of salivary gland proteins in three species of ixodid tick. Experimental and Applied Acarology 23, 969975.CrossRefGoogle Scholar
WIKEL, S. K. ( 1979). Acquired resistance to ticks. Expression of resistance by C4-deficient guinea pigs. American Journal of Tropical Medicine and Hygiene 28, 586590.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, 179185.CrossRefGoogle Scholar
WIKEL, S. K. ( 1985). Effects of tick infestation on the plaque-forming cell response to a thymic dependent antigen. Annals of Tropical Medicine and Parasitology 79, 195198.CrossRefGoogle Scholar
WIKEL, S. K. ( 1996). Host immunity to ticks. Annual Review of Entomology 41, 122.CrossRefGoogle Scholar
WIKEL, S. K. ( 1999). Tick modulation of host immunity: An important factor in pathogen transmission. International Journal for Parasitology 29, 851859.CrossRefGoogle Scholar
WIKEL, S. K., ALARCON-CHAIDEZ, F. J. & MUELLER-DOBLIES, U. ( 2003). Immunological control of vectors. In Biology of Disease Vectors ( ed. Hemingway, J.), Academic Press, San Diego, In press.
WIKEL, S. K. & ALLEN, J. R. ( 1976). Acquired resistance to ticks. I. Passive transfer of resistance. Immunology 30, 311316.Google Scholar
WIKEL, S. K. & ALLEN, J. R. ( 1977). Acquired resistance to ticks. III. Cobra venom factor and the resistance response. Immunology 32, 457465.Google Scholar
WIKEL, S. K., GRAHAM, J. E. & ALLEN, J. R. ( 1978). Acquired resistance to ticks: IV. Skin reactivity and in vitro lymphocyte responsiveness to salivary gland antigen. Immunology 34, 257263.Google Scholar
WIKEL, S. K., RAMACHANDRA, R. N. & BERGMAN, D. K. ( 1994). Tick-induced modulation of the host immune response. International Journal for Parasitology 24, 5966.CrossRefGoogle 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, 335338.Google Scholar
WILLADSEN, P. ( 1980). Immunity to ticks. Advances in Parasitology 18, 293313.CrossRefGoogle Scholar
WILLADSEN, P. ( 1987). Immunological approaches to the control of ticks. International Journal for Parasitology 17, 671677.CrossRefGoogle Scholar
WILLADSEN, P. & JONGEJAN, F. ( 1999). Immunology of the tick–host interaction and the control of ticks and tick–borne diseases. Parasitology Today 15, 258262.CrossRefGoogle 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, 8793.CrossRefGoogle Scholar
ZEIDNER, N., DOLAN, M., MASSUNG, R., PIESMAN, J. & FISH, D. ( 2000). Coinfection with Borrelia burgdorferi and the agent of human granulocytic ehrlichiosis suppresses IL-2 and IFN-gamma production and promotes an IL-4 response in C3H/HeJ mice. Parasite Immunology 22, 581588.CrossRefGoogle Scholar
ZEIDNER, N., DREITZ, M., BELASCO, D. & FISH, D. ( 1996). Suppression of acute Ixodes scapularis-induced Borrelia burgdorferi infection using tumor necrosis factor-α, interleukin-2, and interferon-gamma. Journal of Infectious Diseases 173, 187195.CrossRefGoogle Scholar
ZEIDNER, N., MBOW, M. L., DOLAN, M., MASSUNG, R., BACA, E. & PIESMAN, J. ( 1997). Effects of Ixodes scapularis and Borrelia burgdorferi on modulation of the host immune response: Induction of a TH2 cytokine response in Lyme disease-susceptible (C3H/HeJ) mice but not in disease-resistant (BALB/c) mice. Infection and Immunity 65, 31003106.Google Scholar