Skip to main content Accessibility help
×
Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-18T05:25:44.382Z Has data issue: false hasContentIssue false

4 - Tick saliva: from pharmacology and biochemistry to transcriptome analysis and functional genomics

Published online by Cambridge University Press:  21 August 2009

J. M. Anderson
Affiliation:
Vector Molecular Biology Unit, Laboratory of Malaria and Vector Research, NIAID, National Institute of Health, 12735 Twinbrook Parkway, Room 2E-22, Rockville, MD 20852 USA
J. G. Valenzuela
Affiliation:
Vector Molecular Biology Unit, Laboratory of Malaria and Vector Research, NIAID, National Institute of Health, 12735 Twinbrook Parkway, Room 2E-22, Rockville, MD 20852 USA
Alan S. Bowman
Affiliation:
University of Aberdeen
Patricia A. Nuttall
Affiliation:
Centre for Ecology and Hydrology, Swindon
Get access

Summary

INTRODUCTION

When a tick attaches to a mammalian host to obtain a blood meal it must counteract the well developed haemostatic, inflammatory and immune systems which function to avoid blood loss and to reject unwanted guests. Ticks have been in the blood-feeding business for millions of years and have acquired potent pharmacologically active molecules found in their saliva that can disarm and counteract the haemostatic system of the mammalian host (Ribeiro, 1987b, 1995) and alter the host inflammatory and immune responses (Gillespie et al., 2000; Wikel, 1999). The types of molecules present in tick saliva range from lipids to small peptides and large proteins; each is capable of altering the physiology of the feeding site, consequently affecting pathogen transmission (Ribeiro, 1995; Valenzuela, 2002b; see also Chapter 10). Adaptation of ticks to their natural hosts resulted in the ability of ticks to modulate host immune and haemostatic responses with their saliva. However, tick feeding on non-natural hosts often results in an immune and allergic response, presumably to the injected salivary proteins, resulting in tick rejection (Ribeiro, 1989). Furthermore, in some cases, an immune response to tick feeding confers protection against the pathogens ticks transmit.

Because of the importance of tick saliva, there is increasing interest in the identification and isolation of the molecules in saliva responsible for these effects. The small amount of protein and other biological material present in tick salivary glands has made this a difficult task for many years.

Type
Chapter
Information
Ticks
Biology, Disease and Control
, pp. 92 - 107
Publisher: Cambridge University Press
Print publication year: 2008

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

Alarcon-Chaidez, F. J., Muller-Doblies, U. U. & Wikel, S. (2003). Characterization of a recombinant immunomodulatory protein from the salivary glands of Dermacentor andersoni. Parasite Immunology 25, 69–77.CrossRefGoogle ScholarPubMed
Alarcon-Chaidez, F. J., Sun, J. & Wikel, S. K. (2007). Transcriptome analysis of the salivary glands of Dermacentor andersoni Stiles (Acari: Ixodidae). Insect Biochemistry and Molecular Biology 37, 48–71.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, 299–305.CrossRefGoogle ScholarPubMed
Aljamali, M. N., Bowman, A. S., Dillwith, J. W., et al. (2002 a). Identity and synthesis of prostaglandins in the lone star tick, Amblyomma americanum (L.), as assessed by radio-immunoassay and gas chromatography/mass spectrometry. Insect Biochemistry and Molecular Biology 32, 331–341.CrossRefGoogle Scholar
Aljamali, M. N., Sauer, J. R. & Essenberg, R. C. (2002 b). RNA interference: applicability in tick research. Experimental and Applied Acarology 28, 89–96.CrossRefGoogle ScholarPubMed
Altschul, S. F. & Gish, W. (1996). Local alignment statistics. Methods in Enzymology 266, 460–480.CrossRefGoogle ScholarPubMed
Anguita, J., Ramamoorthi, N., Hovius, J. W., et al. (2002). Salp15, an Ixodes scapularis salivary protein, inhibits CD4(+) T cell activation. Immunity 16, 849–859.CrossRefGoogle ScholarPubMed
Antuch, W., Guntert, P., Billeter, M., et al. (1994). NMR solution structure of the recombinant tick anticoagulant protein (rTAP), a factor Xa inhibitor from the tick Ornithodoros moubata. FEBS Letters 352, 251–257.CrossRefGoogle Scholar
Arca, B., Lombardo, F., Capurro, Lara M., et al. (1999). Trapping cDNAs encoding secreted proteins from the salivary glands of the malaria vector Anopheles gambiae. Proceedings of the National Academy of Sciences of the USA 96, 1516–1521.CrossRefGoogle ScholarPubMed
Bergman, D. K., Palmer, M. J., Caimano, M. J., Radolf, J. D. & Wikel, S. K. (2000). Isolation and molecular cloning of a secreted immunosuppressant protein from Dermacentor andersoni salivary gland. Journal of Parasitology 86, 516–525.CrossRefGoogle ScholarPubMed
Binnington, K. C. & Kemp, D. H. (1980). Role of tick salivary glands in feeding and disease transmission. Advances in Parasitology 18, 315–339.CrossRefGoogle ScholarPubMed
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, 645–655.CrossRefGoogle ScholarPubMed
Bowman, A. S., Gengler, C. L., Surdick, M. R., et al. (1997). A novel phospholipase A2 activity in saliva of the lone star tick, Amblyomma americanum (L.). Experimental Parasitology 87, 121–132.CrossRefGoogle Scholar
Brooks, D. R. & Isaac, R. E. (2002). Functional genomics of parasitic worms: the dawn of a new era. Parasitology International 51, 319–325.CrossRefGoogle ScholarPubMed
Champagne, D. E., Smartt, C. T., Ribeiro, J. M. & James, A. A. (1995). The salivary gland-specific apyrase of the mosquito Aedes aegypti is a member of the 5′-nucleotidase family. Proceedings of the National Academy of Sciences of the USA 92, 694–698.CrossRefGoogle ScholarPubMed
Ciprandi, A., Oliveira, S. K., Masuda, A., Horn, F. & Termignoni, C. (2006). Boophilus microplus: its saliva contains microphilin, a small thrombin inhibitor. Experimental Parasitology 114, 40–46.CrossRefGoogle ScholarPubMed
Das, S., Banerjee, G., Deponte, K., et al. (2001). Salp25D, an Ixodes scapularis antioxidant, is 1 of 14 immunodominant antigens in engorged tick salivary glands. Journal of Infectious Diseases 184, 1056–1064.CrossRefGoogle ScholarPubMed
Dickinson, R. G., O'Hagan, J. E., Schotz, M., Binnington, K. C. & Hegarty, M. P. (1976). Prostaglandin in the saliva of the cattle tick Boophilus microplus. Australian Journal of Experimental Biology and Medical Science 54, 475–486.CrossRefGoogle ScholarPubMed
Ehebauer, M. T., Mans, B. J., Gaspar, A. R. & Neitz, A. W. (2002). Identification of extrinsic blood coagulation pathway inhibitors from the tick Ornithodoros savignyi (Acari: Argasidae). Experimental Parasitology 101, 138–148.CrossRefGoogle Scholar
Ferguson, J. J. & Zaqqa, M. (1999). Platelet glycoprotein IIb/IIIa receptor antagonists: current concepts and future directions. Drugs 58, 965–982.CrossRefGoogle ScholarPubMed
Fogaca, A. C., Almeida, I. C., Eberlin, M. N., et al. (2006). Ixodidin, a novel antimicrobial peptide from the hemocytes of the cattle tick Boophilus microplus with inhibitory activity against serine proteinases. Peptides 27, 667–674.CrossRefGoogle ScholarPubMed
Fogaca, A. C., Lorenzini, D. M., Kaku, L. M., et al. (2004). Cysteine-rich antimicrobial peptides of the cattle tick Boophilus microplus: isolation, structural characterization and tissue expression profile. Developmental and Comparative Immunology 28, 191–200.CrossRefGoogle ScholarPubMed
Francischetti, I. M., Andersen, J. F. & Ribeiro, J. M. (2002 a). Biochemical and functional characterization of recombinant Rhodnius prolixus platelet aggregation inhibitor 1 as a novel lipocalin with high affinity for adenosine diphosphate and other adenine nucleotides. Biochemistry 41, 3810–3818.CrossRefGoogle ScholarPubMed
Francischetti, I. M., Mather, T. N. & Ribeiro, J. M. (2003). Cloning of a salivary gland metalloprotease and characterization of gelatinase and fibrin(ogen)lytic activities in the saliva of the Lyme disease tick vector Ixodes scapularis. Biochemical and Biophysical Research Communications 305, 869–875.CrossRefGoogle ScholarPubMed
Francischetti, I. M., Mather, T. N. & Ribeiro, J. M. (2004). Penthalaris, a novel recombinant five-Kunitz tissue factor pathway inhibitor (TFPI) from the salivary gland of the tick vector of Lyme disease, Ixodes scapularis. Thrombosis and Haemostasis 91, 886–898.Google ScholarPubMed
Francischetti, I. M., Pham, My V., Mans, B. J., et al. (2005). The transcriptome of the salivary glands of the female western black-legged tick Ixodes pacificus (Acari: Ixodidae). Insect Biochemistry and Molecular Biology 35, 1142–1161.CrossRefGoogle Scholar
Francischetti, I. M., Valenzuela, J. G., Andersen, J. F., Mather, T. N. & Ribeiro, J. M. (2002 b). Ixolaris, a novel recombinant tissue factor pathway inhibitor (TFPI) from the salivary gland of the tick, Ixodes scapularis: identification of factor X and factor Xa as scaffolds for the inhibition of factor VIIa/tissue factor complex. Blood 99, 3602–3612.CrossRefGoogle ScholarPubMed
Garg, R., Juncadella, I. J., Ramamoorthi, N., et al. (2006). Cutting edge: CD4 is the receptor for the tick saliva immunosuppressor, Salp15. Journal of Immunology 177, 6579–6583.CrossRefGoogle ScholarPubMed
Gillespie, R. D., Mbow, M. L. & Titus, R. G. (2000). The immunomodulatory factors of blood feeding arthropod saliva. Parasite Immunology 22, 319–331.CrossRefGoogle Scholar
Gordon, J. R. & Allen, J. R. (1991). Factors V and VII anticoagulant activities in the salivary glands of feeding Dermacentor andersoni ticks. Journal of Parasitology 77, 167–170.CrossRefGoogle ScholarPubMed
Grunclova, L., Horn, M., Vancova, M., et al. (2006). Two secreted cystatins of the soft tick Ornithodoros moubata: differential expression pattern and inhibitory specificity. Biological Chemistry 387, 1635–1644.CrossRefGoogle ScholarPubMed
Hajnicka, V., Kocakova, P., Slavikova, M., et al. (2001). Anti-interleukin-8 activity of tick salivary gland extracts. Parasite Immunology 23, 483–489.CrossRefGoogle ScholarPubMed
Hajnicka, V., Vancova, I., Kocakova, P., et al. (2005). Manipulation of host cytokine network by ticks: a potential gateway for pathogen transmission. Parasitology 130, 333–342.CrossRefGoogle ScholarPubMed
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 ScholarPubMed
Hawkins, R. I. & Hellmann, K. (1966). Factors affecting blood clotting from the tick Ornithodoros moubata. Journal of Physiology 185, 70.Google Scholar
Holt, R. A., Subramanian, G. M., Halpern, A., Sutton, G. G., Charlab, R., Nusskern, D. R., Wincker, P., Clark, A. G., Ribeiro, J. M., Wides, R., Salzberg, S. L., Loftus, B., Yandell, M., Majoros, W. H., Rusch, D. B., Lai, Z., Kraft, C. L., Abril, J. F., Anthouard, V., Arensburger, P., Atkinson, P. W., Baden, H., Berardinis, V., Baldwin, D., Benes, V., Biedler, J., Blass, C., Bolanos, R., Boscus, D., Barnstead, M., Cai, S., Center, A., Chaturverdi, K., Christophides, G. K., Chrystal, M. A., Clamp, M., Cravchik, A., Curwen, V., Dana, A., Delcher, A., Dew, I., Evans, C. A., Flanigan, M., Grundschober-Freimoser, A., Friedli, L., Gu, Z., Guan, P., Guigo, R., Hillenmeyer, M. E., Hladun, S. L., Hogan, J. R., Hong, Y. S., Hoover, J., Jaillon, O., Ke, Z., Kodira, C., Kokoza, E., Koutsos, A., Letunic, I., Levitsky, A., Liang, Y., Lin, J. J., Lobo, N. F., Lopez, J. R., Malek, J. A., Mcintosh, T. C., Meister, S., Miller, J., Mobarry, C., Mongin, E., Murphy, S. D., O'Brochta, D. A., Pfannkoch, C., Qi, R., Regier, M. A., Remington, K., Shao, H., Sharakhova, M. V., Sitter, C. D., Shetty, J., Smith, T. J., Strong, R., Sun, J., Thomasova, D., Ton, L. Q., Topalis, P., Tu, Z., Unger, M. F., Walenz, B., Wang, A., Wang, J., Wang, M., Wang, X., Woodford, K. J., Wortman, J. R., Wu, M., Yao, A., Zdobnov, E. M., Zhang, H., Zhao, Q., Zhao, S., Zhu, S. C., Zhimulev, I., Coluzzi, M., Torre, Della A., Roth, C. W., Louis, C., Kalush, F., Mural, R. J., Myers, E. W., Adams, M. D., Smith, H. O., Broder, S., Gardner, M. J., Fraser, C. M., Birney, E., Bork, P., Brey, P. T., Venter, J. C., Weissenbach, J., Kafatos, F. C., Collins, F. H. & Hoffman, S. L. (2002). The genome sequence of the malaria mosquito Anopheles gambiae. Science 298, 129–149.CrossRefGoogle ScholarPubMed
Horn, F., Santos, Dos P. C. & Termignoni, C. (2000). Boophilus microplus anticoagulant protein: an antithrombin inhibitor isolated from the cattle tick saliva. Archives of Biochemistry and Biophysics 384, 68–73.CrossRefGoogle ScholarPubMed
Huang, X. & Madan, A. (1999). CAP3: a DNA sequence assembly program. Genome Research 9, 868–877.CrossRefGoogle ScholarPubMed
Hugli, T. E. & Muller-Eberhard, H. J. (1978). Anaphylatoxins: C3a and C5a. Advances in Immunology 26, 1–53.CrossRefGoogle ScholarPubMed
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, 293–299.CrossRefGoogle ScholarPubMed
Iwanaga, S., Okada, M., Isawa, H., et al. (2003). Identification and characterization of novel salivary thrombin inhibitors from the ixodidae tick, Haemaphysalis longicornis. European Journal of Biochemistry 270, 1926–1934.CrossRefGoogle ScholarPubMed
Joiner, K. A. (1988). Complement evasion by bacteria and parasites. Annual Review of Microbiology 42, 201–230.CrossRefGoogle ScholarPubMed
Joubert, A. M., Crause, J. C., Gaspar, A. R., et al. (1995). Isolation and characterization of an anticoagulant present in the salivary glands of the bont-legged tick, Hyalomma truncatum. Experimental and Applied Acarology 19, 79–92.CrossRefGoogle ScholarPubMed
Joubert, A. M., Louw, A. I., Joubert, F. & Neitz, A. W. (1998). Cloning, nucleotide sequence and expression of the gene encoding factor Xa inhibitor from the salivary glands of the tick, Ornithodoros savignyi. Experimental and Applied Acarology 22, 603–619.CrossRefGoogle ScholarPubMed
Jutel, M., Watanabe, T., Klunker, S., et al. (2001). Histamine regulates T-cell and antibody responses by differential expression of H1 and H2 receptors. Nature 413, 420–425.CrossRefGoogle ScholarPubMed
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, 6702–6708.Google ScholarPubMed
Karczewski, J., Waxman, L., Endris, R. G. & Connolly, T. M. (1995). An inhibitor from the argasid tick Ornithodoros moubata of cell adhesion to collagen. Biochemical and Biophysical Research Communications 208, 532–541.CrossRefGoogle Scholar
Karim, S., Miller, N. J., Valenzuela, J., Sauer, J. R. & Mather, T. N. (2005). RNAi-mediated gene silencing to assess the role of synaptobrevin and cystatin in tick blood feeding. Biochemical and Biophysical Research Communications 334, 1336–1342.CrossRefGoogle ScholarPubMed
Kato, N., Iwanaga, S., Okayama, T., et al. (2005). Identification and characterization of the plasma kallikrein–kinin system inhibitor, haemaphysalin, from hard tick, Haemaphysalis longicornis. Thrombosis and Haemostasis 93, 359–367.Google ScholarPubMed
Keller, P. M., Waxman, L., Arnold, B. A., et al. (1993). Cloning of the cDNA and expression of moubatin, an inhibitor of platelet aggregation. Journal of Biological Chemistry 268, 5450–5456.Google ScholarPubMed
Konik, P., Slavikova, V., Salat, J., et al. (2006). Anti-tumour necrosis factor-alpha activity in Ixodes ricinus saliva. Parasite Immunology 28, 649–656.CrossRefGoogle ScholarPubMed
Kotsyfakis, M., Sa-Nuñes, A., Francischetti, I. M., et al. (2006). Anti-inflammatory and immunosuppressive activity of sialostatin L, a salivary cystatin from the tick Ixodes scapularis. Journal of Biological Chemistry 281, 26298–26307.CrossRefGoogle ScholarPubMed
Lawrie, C. H., Randolph, S. E. & Nuttall, P. A. (1999). Ixodes ticks: serum species sensitivity of anticomplement activity. Experimental Parasitology 93, 207–214.CrossRefGoogle ScholarPubMed
Lawrie, C. H., Sim, R. B. & Nuttall, P. A. (2005). Investigation of the mechanisms of anti-complement activity in Ixodes ricinus ticks. Molecular Immunology 42, 31–38.CrossRefGoogle ScholarPubMed
Leboulle, G., Crippa, M., Decrem, Y., et al. (2002 a). Characterization of a novel salivary immunosuppressive protein from Ixodes ricinus ticks. Journal of Biological Chemistry 277, 10083–10089.CrossRefGoogle ScholarPubMed
Leboulle, G., Rochez, C., Louahed, J., et al. (2002 b). Isolation of Ixodes ricinus salivary gland mRNA encoding factors induced during blood feeding. American Journal of Tropical Medicine and Hygiene 66, 225–233.CrossRefGoogle ScholarPubMed
Lee, W. H. & Vega, V. B. (2004). Heterogeneity detector: finding heterogeneous positions in Phred/Phrap assemblies. Bioinformatics 20, 2863–2864.CrossRefGoogle ScholarPubMed
Lima, C. A., Sasaki, S. D. & Tanaka, A. S. (2006). Bmcystatin, a cysteine proteinase inhibitor characterized from the tick Boophilus microplus. Biochemical and Biophysical Research Communications 347, 44–50.CrossRefGoogle ScholarPubMed
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, 418–429.CrossRefGoogle ScholarPubMed
Mans, B. J., Coetzee, J., Louw, A. I., Gaspar, A. R. & Neitz, A. W. (2000). Disaggregation of aggregated platelets by apyrase from the tick, Ornithodoros savignyi (Acari: Argasidae). Experimental and Applied Acarology 24, 271–282.CrossRefGoogle Scholar
Mans, B. J., Louw, A. I. & Neitz, A. W. (2002 a). Evolution of hematophagy in ticks: common origins for blood coagulation and platelet aggregation inhibitors from soft ticks of the genus Ornithodoros. Molecular Biology and Evolution 19, 1695–1705.CrossRefGoogle ScholarPubMed
Mans, B. J., Louw, A. I. & Neitz, A. W. (2002 b). Savignygrin, a platelet aggregation inhibitor from the soft tick Ornithodoros savignyi, presents the RGD integrin recognition motif on the Kunitz–BPTI fold. Journal of Biological Chemistry 277, 21371–21378.CrossRefGoogle ScholarPubMed
Mans, B. J., Louw, A. I. & Neitz, A. W. (2003). The major tick salivary gland proteins and toxins from the soft tick, Ornithodoros savignyi, are part of the tick lipocalin family: implications for the origins of tick toxicoses. Molecular Biology and Evolution 20, 1158–1167.CrossRefGoogle ScholarPubMed
Nakajima, C., Da, Silva Vaz I.Jr, Imamura, S., et al. (2005). Random sequencing of cDNA library derived from partially-fed adult female Haemaphysalis longicornis salivary gland. Journal of Veterinary Medical Science 67, 1127–1131.CrossRefGoogle ScholarPubMed
Nakajima, C., Imamura, S., Konnai, S., et al. (2006). A novel gene encoding a thrombin inhibitory protein in a cDNA library from Haemaphysalis longicornis salivary gland. Journal of Veterinary Medical Science 68, 447–452.CrossRefGoogle Scholar
Narasimhan, S., Koski, R. A., Beaulieu, B., et al. (2002). A novel family of anticoagulants from the saliva of Ixodes scapularis. Insect Molecular Biology 11, 641–650.CrossRefGoogle ScholarPubMed
Narasimhan, S., Montgomery, R. R., Deponte, K., et al. (2004). Disruption of Ixodes scapularis anticoagulation by using RNA interference. Proceedings of the National Academy of Sciences of the USA 101, 1141–1146.CrossRefGoogle ScholarPubMed
Nazareth, R. A., Tomaz, L. S., Ortiz-Costa, S., et al. (2006). Antithrombotic properties of ixolaris, a potent inhibitor of the extrinsic pathway of the coagulation cascade. Thrombosis and Haemostasis 96, 7–13.CrossRefGoogle ScholarPubMed
Nene, V., Lee, D., Kang'A, S., et al. (2004). Genes transcribed in the salivary glands of female Rhipicephalus appendiculatus ticks infected with Theileria parva. Insect Biochemistry and Molecular Biology 34, 1117–1128.CrossRefGoogle ScholarPubMed
Nene, V., Lee, D., Quackenbush, J., et al. (2002). AvGI, an index of genes transcribed in the salivary glands of the ixodid tick Amblyomma variegatum. International Journal of Parasitology 32, 1447–1456.CrossRefGoogle ScholarPubMed
Nienaber, J., Gaspar, A. R. & Neitz, A. W. (1999). Savignin, a potent thrombin inhibitor isolated from the salivary glands of the tick Ornithodoros savignyi (Acari: Argasidae). Experimental Parasitology 93, 82–91.CrossRefGoogle Scholar
Nunn, M. A., Sharma, A., Paesen, G. C., et al. (2005). Complement inhibitor of C5 activation from the soft tick Ornithodoros moubata. Journal of Immunology 174, 2084–2091.CrossRefGoogle ScholarPubMed
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 ScholarPubMed
Quackenbush, J., Cho, J., Lee, D., et al. (2001). The TIGR Gene Indices: analysis of gene transcript sequences in highly sampled eukaryotic species. Nucleic Acids Research 29, 159–164.CrossRefGoogle ScholarPubMed
Ramakrishnan, V. G., Aljamali, M. N., Sauer, J. R. & Essenberg, R. C. (2005). Application of RNA interference in tick salivary gland research. Journal of Biomolecular Techniques 16, 297–305.Google ScholarPubMed
Ramamoorthi, N., Narasimhan, S., Pal, U., et al. (2005). The Lyme disease agent exploits a tick protein to infect the mammalian host. Nature 436, 573–577.CrossRefGoogle ScholarPubMed
Ribeiro, J. M. (1987 a). Ixodes dammini: salivary anti-complement activity. Experimental Parasitology 64, 347–353.CrossRefGoogle ScholarPubMed
Ribeiro, J. M. (1987 b). Role of saliva in blood-feeding by arthropods. Annual Review of Entomology 32, 463–478.CrossRefGoogle ScholarPubMed
Ribeiro, J. M. (1989). Role of saliva in tick/host interactions. Experimental and Applied Acarology 7, 15–20.CrossRefGoogle ScholarPubMed
Ribeiro, J. M. (1995). How ticks make a living. Parasitology Today 11, 91–93.CrossRefGoogle ScholarPubMed
Ribeiro, J. M. & Mather, T. N. (1998). Ixodes scapularis: salivary kininase activity is a metallo dipeptidyl carboxypeptidase. Experimental Parasitology 89, 213–221.CrossRefGoogle ScholarPubMed
Ribeiro, J. M., Alarcon-Chaidez, F., Francischetti, I. M., et al. (2006). An annotated catalog of salivary gland transcripts from Ixodes scapularis ticks. Insect Biochemistry and Molecular Biology 36, 111–129.CrossRefGoogle ScholarPubMed
Ribeiro, J. M., Endris, T. M. & Endris, R. (1991). Saliva of the soft tick, Ornithodoros moubata, contains anti-platelet and apyrase activities. Comparative Biochemistry and Physiology A 100, 109–112.CrossRefGoogle ScholarPubMed
Ribeiro, J. M., Evans, P. M., McSwain, J. L. & Sauer, J. (1992). Amblyomma americanum: characterization of salivary prostaglandins E2 and F2α by RP-HPLC/bioassay and gas chromatography-mass spectrometry. Experimental Parasitology 74, 112–116.CrossRefGoogle Scholar
Ribeiro, J. M., 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, 332–344.CrossRefGoogle ScholarPubMed
Ribeiro, J. M., Makoul, G. T. & Robinson, D. R. (1988). Ixodes dammini: evidence for salivary prostacyclin secretion. Journal of Parasitology 74, 1068–1069.CrossRefGoogle ScholarPubMed
Ribeiro, J. M., Weis, J. J. & Telford, S. R. III (1990). Saliva of the tick Ixodes dammini inhibits neutrophil function. Experimental Parasitology 70, 382–388.CrossRefGoogle ScholarPubMed
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, 79–86.CrossRefGoogle ScholarPubMed
Soares, C. A., Lima, C. M., Dolan, M. C., et al. (2005). Capillary feeding of specific dsRNA induces silencing of the isac gene in nymphal Ixodes scapularis ticks. Insect Molecular Biology 14, 443–452.CrossRefGoogle ScholarPubMed
Charles, St R., Padmanabhan, K., Arni, R. V., Padmanabhan, K. P. & Tulinsky, A. (2000). Structure of tick anticoagulant peptide at 1.6 Å resolution complexed with bovine pancreatic trypsin inhibitor. Protein Science 9, 265–272.CrossRefGoogle Scholar
Sukumaran, B., Narasimhan, S., Anderson, J. F., et al. (2006). An Ixodes scapularis protein required for survival of Anaplasma phagocytophilum in tick salivary glands. Journal of Experimental Medicine 203, 1507–1517.CrossRefGoogle ScholarPubMed
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. & Higgins, D. G. (1997). The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.CrossRefGoogle ScholarPubMed
Trimnell, A. R., Davies, G. M., Lissina, O., Hails, R. S. & Nuttall, P. A. (2005). A cross-reactive tick cement antigen is a candidate broad-spectrum tick vaccine. Vaccine 23, 4329–4341.CrossRefGoogle ScholarPubMed
Trimnell, A. R., Hails, R. S. & Nuttall, P. A. (2002). Dual action ectoparasite vaccine targeting ‘exposed’ and ‘concealed’ antigens. Vaccine 20, 3560–3568.CrossRefGoogle ScholarPubMed
Valenzuela, J. G. (2002 a). Exploring the messages of the salivary glands of Ixodes ricinus. American Journal of Tropical Medicine and Hygiene 66, 223–224.CrossRefGoogle ScholarPubMed
Valenzuela, J. G. (2002 b). High-throughput approaches to study salivary proteins and genes from vectors of disease. Insect Biochemistry and Molecular Biology 32, 1199–1209.CrossRefGoogle Scholar
Valenzuela, J. G., Belkaid, Y., Rowton, E. & Ribeiro, J. M. (2001). The salivary apyrase of the blood-sucking sand fly Phlebotomus papatasi belongs to the novel Cimex family of apyrases. Journal of Experimental Biology 204, 229–237.Google ScholarPubMed
Valenzuela, J. G., Charlab, R., Galperin, M. Y. & Ribeiro, J. M. (1998). Purification, cloning, and expression of an apyrase from the bed bug Cimex lectularius: a new type of nucleotide-binding enzyme. Journal of Biological Chemistry 273, 30583–30590.CrossRefGoogle ScholarPubMed
Valenzuela, J. G., Charlab, R., Mather, T. N. & Ribeiro, J. M. (2000). Purification, cloning, and expression of a novel salivary anticomplement protein from the tick, Ixodes scapularis. Journal of Biological Chemistry 275, 18717–18723.CrossRefGoogle ScholarPubMed
Valenzuela, J. G., Francischetti, I. M., Pham, V. M., et al. (2002). Exploring the sialome of the tick Ixodes scapularis. Journal of Experimental Biology 205, 2843–2864.Google ScholarPubMed
Van, Locht A., Stubbs, M. T., Bode, W., et al. (1996). The ornithodorin–thrombin crystal structure, a key to the TAP enigma?EMBO Journal 15, 6011–6017.Google Scholar
Wang, X., Coons, L. B., Taylor, D. B., Stevens, S. E. Jr & Gartner, T. K. (1996). Variabilin, a novel RGD-containing antagonist of glycoprotein IIb–IIIa and platelet aggregation inhibitor from the hard tick Dermacentor variabilis. Journal of Biological Chemistry 271, 17785–17790.CrossRefGoogle ScholarPubMed
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, 593–596.CrossRefGoogle ScholarPubMed
Wikel, S. K. (1999). Tick modulation of host immunity: an important factor in pathogen transmission. International Journal for Parasitology 29, 851–859.CrossRefGoogle ScholarPubMed
Zhu, K., Bowman, A. S., Brigham, D. L., et al. (1997 a). Isolation and characterization of americanin, a specific inhibitor of thrombin, from the salivary glands of the lone star tick Amblyomma americanum (L.). Experimental Parasitology 87, 30–38.CrossRefGoogle Scholar
Zhu, K., Dillwith, J. W., Bowman, A. S. & Sauer, J. R. (1997 b). Identification of hemolytic activity in saliva of the lone star tick (Acari: Ixodidae). Journal of Medical Entomology 34, 160–166.CrossRefGoogle Scholar
Zhu, K., Sauer, J. R., Bowman, A. S. & Dillwith, J. W. (1997 c). Identification and characterization of anticoagulant activities in the saliva of the lone star tick, Amblyomma americanum (L.). Journal of Parasitology 83, 38–43.CrossRefGoogle Scholar

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×