Sexual differences in the sialomes of the zebra tick, Rhipicephalus pulchellus

Journal of Proteomics

Volumn 117, Issue , 2015, Pages 120-144

  Tan, Angelina W L ^a,b   Francischetti, Ivo M B ^c   Slovak, Mirko ^d   Kini, R Manjunatha ^a,b,e,f   Ribeiro, José M C ^c  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^d INSTITUTE OF CHEMISTRY   (Slovakia)

^e VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

Author keywords

Salivary glands; Tick; Transcriptome

Indexed keywords

COMPLEMENTARY DNA; PROTEOME; SALIVA PROTEIN; TRANSCRIPTOME; ARTHROPOD PROTEIN;

ADULT; ANIMAL TISSUE; ANTICOAGULATION; ARTICLE; DNA LIBRARY; DNA SEQUENCE; FEMALE; MALE; NONHUMAN; PRIORITY JOURNAL; RHIPICEPHALUS; RHIPICEPHALUS PULCHELLUS; SALIVARY GLAND; SEX DIFFERENCE; AMINO ACID SEQUENCE; ANIMAL; GENETICS; METABOLISM; MOLECULAR GENETICS; SALIVA; SEXUAL DEVELOPMENT;

ANIMALIA; EQUUS SUBG. HIPPOTIGRIS; IXODIDA; RHIPICEPHALUS PULCHELLUS; VERTEBRATA;

AMINO ACID SEQUENCE; ANIMALS; ARTHROPOD PROTEINS; FEMALE; MALE; MOLECULAR SEQUENCE DATA; RHIPICEPHALUS; SALIVA; SALIVARY PROTEINS AND PEPTIDES; SEX CHARACTERISTICS;

EID: 84922430752     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2014.12.014     Document Type: Article

References (135)

1. Nava S., Guglielmone A.A., Mangold A.J. An overview of systematics and evolution of ticks. Front Biosci 2009, 14:2857-2877.
2. Francischetti I.M.B., Sá-Nunes A., Mans B.J., Santos I.M., Ribeiro J.M.C. The role of saliva in tick feeding. Front Biosci 2009, 14:2051-2088.
3. Mans B.J., Francischetti I.M.B. Sialomic perspectives on the evolution of blood-feeding behavior in Arthropods: future therapeutics by natural design. Toxins and Hemostasis: From Bench to Bed-side 2010, Springer. R.M. Kini, K.J. Clemetson, F.S. Markland, M.A. McLane, T. Morita (Eds.).
4. Mans B.J., Neitz A.W. Adaptation of ticks to a blood-feeding environment: evolution from a functional perspective. Insect Biochem Mol Biol 2004, 34:1-17.
5. Lehane M.J. The biology of blood-sucking in insects 2005, Cambridge University Press, Cambridge. 2nd ed.
6. Calvo E., Pham V.M., Lombardo F., Arca B., Ribeiro J.M. The sialotranscriptome of adult male Anopheles gambiae mosquitoes. Insect Biochem Mol Biol 2006, 36:570-575.
7. Arca B., Lombardo F., Valenzuela J.G., Francischetti I.M., Marinotti O., Coluzzi M., et al. An updated catalogue of salivary gland transcripts in the adult female mosquito, Anopheles gambiae. J Exp Biol 2005, 208:3971-3986.
8. Chen Z., Li Y., Liu Z., Yang J., Yin H. The life cycle of Hyalomma rufipes (Acari: Ixodidae) under laboratory conditions. Exp Appl Acarol 2012, 56:85-92.
9. Chen X., Yu Z., Guo L., Li L., Meng H., Wang D., et al. Life cycle of Haemaphysalis doenitzi (Acari: Ixodidae) under laboratory conditions and its phylogeny based on mitochondrial 16S rDNA. Exp Appl Acarol 2012, 56:143-150.
10. Ma M., Guan G., Chen Z., Liu Z., Liu A., Gou H., et al. The life cycle of Haemaphysalis qinghaiensis (Acari: Ixodidae) ticks under laboratory conditions. Exp Appl Acarol 2013, 59:493-500.
11. Zheng H., Yu Z., Chen Z., Zhou L., Zheng B., Ma H., et al. Development and biological characteristics of Haemaphysalis longicornis (Acari: Ixodidae) under field conditions. Exp Appl Acarol 2011, 53:377-388.
12. Kiszewski A.E., Matuschka F.R., Spielman A. Mating strategies and spermiogenesis in ixodid ticks. Annu Rev Entomol 2001, 46:167-182.
13. Feldman-Muhsam B., Borut S., Saliternik-Givant S. Salivary secretion of the male tick during copulation. J Insect Physiol 1970, 16:1945-1949.
14. Slovak M., Labuda M., Marley S.E. Mass laboratory rearing of Dermacentor reticulatus ticks (Acarina, Ixodidae). Biologia (Bratisl) 2002, 57:261-266.
15. Birol I., Jackman S.D., Nielsen C.B., Qian J.Q., Varhol R., Stazyk G., et al. De novo transcriptome assembly with ABySS. Bioinformatics (Oxford, England) 2009, 25:2872-2877.
16. Simpson J.T., Wong K., Jackman S.D., Schein J.E., Jones S.J., Birol I. ABySS: a parallel assembler for short read sequence data. Genome Res 2009, 19:1117-1123.
17. Zhao Q.Y., Wang Y., Kong Y.M., Luo D., Li X., Hao P. Optimizing de novo transcriptome assembly from short-read RNA-Seq data: a comparative study. BMC Bioinformatics 2011, 12(Suppl. 14):S2.
18. Grabherr M.G., Haas B.J., Yassour M., Levin J.Z., Thompson D.A., Amit I., et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 2011, 29:644-652.
19. Karim S., Singh P., Ribeiro J.M. A deep insight into the sialotranscriptome of the Gulf Coast tick, Amblyomma maculatum. PLoS One 2011, 6:e28525.
20. Nielsen H., Brunak S., von Heijne G. Machine learning approaches for the prediction of signal peptides and other protein sorting signals. Protein Eng 1999, 12:3-9.
21. Duckert P., Brunak S., Blom N. Prediction of proprotein convertase cleavage sites. Protein Eng Des Sel 2004, 17:107-112.
22. Sonnhammer E.L., von Heijne G., Krogh A. A hidden Markov model for predicting transmembrane helices in protein sequences. Proc Int Conf Intell Syst Mol Biol 1998, 6:175-182.
23. Julenius K., Molgaard A., Gupta R., Brunak S. Prediction, conservation analysis, and structural characterization of mammalian mucin-type O-glycosylation sites. Glycobiology 2005, 15:153-164.
24. Jeanmougin F., Thompson J.D., Gouy M., Higgins D.G., Gibson T.J. Multiple sequence alignment with Clustal X. Trends Biochem Sci 1998, 23:403-405.
25. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28:2731-2739.
26. Galperin M.Y., Koonin E.V. 'Conserved hypothetical' proteins: prioritization of targets for experimental study. Nucleic Acids Res 2004, 32:5452-5463.
27. Szabo C., Ischiropoulos H., Radi R. Peroxynitrite: biochemistry, pathophysiology and development of therapeutics. Nat Rev Drug Discov 2007, 6:662-680.
28. Dickinson R.G., O'Hagan J.E., Shotz M., Binnington K.C., Hegarty M.P. Prostaglandin in the saliva of the cattle tick Boophilus microplus. Aust J Exp Biol Med Sci 1976, 54:475-486.
29. Higgs G.A., Vane J.R., Hart R.J., Porter C., Wilson R.G. Prostaglandins in the saliva of the cattle tick, Boophilus microplus (Canestrini) (Acarina, Ixodidae). Bull Entomol Res 1976, 66:665-670.
30. Ribeiro J.M., Makoul G.T., Robinson D.R. Ixodes dammini: evidence for salivary prostacyclin secretion. J Parasitol 1988, 74:1068-1069.
31. Ribeiro J.M.C., Evans P.M., MacSwain J.L., Sauer J. Amblyomma americanum: characterization of salivary prostaglandins E2 and F2alpha by RP-HPLC/bioassay and gas chromatography-mass spectrometry. Exp Parasitol 1992, 74:112-116.
32. Oliveira C.J., Sa-Nunes A., Francischetti I.M., Carregaro V., Anatriello E., Silva J.S., et al. Deconstructing Tick Saliva: Non protein molecules with potent immunomodullatory properties. J Biol Chem 2011, 286:10960-10969.
33. Marino J.P. Soluble epoxide hydrolase, a target with multiple opportunities for cardiovascular drug discovery. Curr Top Med Chem 2009, 9:452-463.
34. Spector A.A., Fang X., Snyder G.D., Weintraub N.L. Epoxyeicosatrienoic acids (EETs): metabolism and biochemical function. Prog Lipid Res 2004, 43:55-90.
35. Utermohlen O., Herz J., Schramm M., Kronke M. Fusogenicity of membranes: the impact of acid sphingomyelinase on innate immune responses. Immunobiology 2008, 213:307-314.
36. Wartha F., Beiter K., Normark S., Henriques-Normark B. Neutrophil extracellular traps: casting the NET over pathogenesis. Curr Opin Microbiol 2007, 10:52-56.
37. Pichu S., Yalcin E.B., Ribeiro J.M., King R.S., Mather T.N. Molecular characterization of novel sulfotransferases from the tick, Ixodes scapularis. BMC Biochem 2011, 12:32.
38. Kivirikko K.I., Pihlajaniemi T. Collagen hydroxylases and the protein disulfide isomerase subunit of prolyl 4-hydroxylases. Adv Enzymol Relat Areas Mol Biol 1998, 72:325-398.
39. Baker B.S., Wolfner M.F. A molecular analysis of doublesex, a bifunctional gene that controls both male and female sexual differentiation in Drosophila melanogaster. Genes Dev 1988, 2:477-489.
40. Wicker T., Sabot F., Hua-Van A., Bennetzen J.L., Capy P., Chalhoub B., et al. A unified classification system for eukaryotic transposable elements. Nat Rev 2007, 8:973-982.
41. Bao W., Jurka M.G., Kapitonov V.V., Jurka J. New superfamilies of eukaryotic DNA transposons and their internal divisions. Mol Biol Evol 2009, 26:983-993.
42. Kapitonov V.V., Jurka J. A universal classification of eukaryotic transposable elements implemented in Repbase. Nat Rev 2008, 9:411-412. [author reply 4].
43. Kelley D.R., Rinn J.L. Transposable elements reveal a stem cell specific class of long noncoding RNAs. Genome Biol 2012, 13:R107.
44. Schwarz A., von Reumont B.M., Erhart J., Chagas A.C., Ribeiro J.M., Kotsyfakis M. De novo Ixodes ricinus salivary gland transcriptome analysis using two next-generation sequencing methodologies. FASEB J 2013, 12:4745-4756.
45. Anatriello E., Ribeiro J.M., de Miranda-Santos I.K., Brandao L.G., Anderson J.M., Valenzuela J.G., et al. An insight into the sialotranscriptome of the brown dog tick, Rhipicephalus sanguineus. BMC Genomics 2010, 11:450.
46. Francischetti I.M., Anderson J.M., Manoukis N., Pham V.M., Ribeiro J.M. An insight into the sialotranscriptome and proteome of the coarse bontlegged tick, Hyalomma marginatum rufipes. J Proteome 2011, 74:2892-2908.
47. Klein T., Bischoff R. Active metalloproteases of the A Disintegrin and Metalloprotease (ADAM) family: biological function and structure. J Proteome Res 2011, 10:17-33.
48. Wolfsberg T.G., Primakoff P., Myles D.G., White J.M. ADAM, a novel family of membrane proteins containing A Disintegrin And Metalloprotease domain: multipotential functions in cell-cell and cell-matrix interactions. J Cell Biol 1995, 131:275-278.
49. Hati R., Mitra P., Sarker S., Bhattacharyya K.K. Snake venom hemorrhagins. Crit Rev Toxicol 1999, 29:1-19.
50. Francischetti I.M., Mather T.N., Ribeiro J.M. 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. Biochem Biophys Res Commun 2003, 305:869-875.
51. Francischetti I.M., Mather T.N., Ribeiro J.M. Tick saliva is a potent inhibitor of endothelial cell proliferation and angiogenesis. Thromb Haemost 2005, 94:167-174.
52. Xu X., Yang H., Ma D., Wu J., Wang Y., Song Y., et al. Toward an understanding of the molecular mechanism for successful blood feeding by coupling proteomics analysis with pharmacological testing of horsefly salivary glands. Mol Cell Proteomics 2008, 7:582-590.
53. LaFlamme B.A., Ram K.R., Wolfner M.F. The Drosophila melanogaster seminal fluid protease "seminase" regulates proteolytic and post-mating reproductive processes. PLoS Genet 2012, 8:e1002435.
54. Bilhartz D.L., Tindall D.J., Oesterling J.E. Prostate-specific antigen and prostatic acid phosphatase: biomolecular and physiologic characteristics. Urology 1991, 38:95-102.
55. Veveris-Lowe T.L., Kruger S.J., Walsh T., Gardiner R.A., Clements J.A. Seminal fluid characterization for male fertility and prostate cancer: kallikrein-related serine proteases and whole proteome approaches. Semin Thromb Hemost 2007, 33:87-99.
56. Ribeiro J.M., Mather T.N. Ixodes scapularis: salivary kininase activity is a metallo dipeptidyl carboxypeptidase. Exp Parasitol 1998, 89:213-221.
57. Champagne D.E., Smartt C.T., Ribeiro J.M., James A.A. The salivary gland-specific apyrase of the mosquito Aedes aegypti is a member of the 5'-nucleotidase family. Proc Natl Acad Sci U S A 1995, 92:694-698.
58. Stutzer C., Mans B.J., Gaspar A.R., Neitz A.W., Maritz-Olivier C. Ornithodoros savignyi: soft tick apyrase belongs to the 5'-nucleotidase family. Exp Parasitol 2009, 122:318-327.
59. Schluter H., Tepel M., Zidek W. Vascular actions of diadenosine phosphates. J Auton Pharmacol 1996, 16:357-362.
60. Ogilvie A., Blasius R., Schulze-Lohoff E., Sterzel R.B. Adenine dinucleotides: a novel class of signalling molecules. J Auton Pharmacol 1996, 16:325-328.
61. Ascenzi P., Bocedi A., Bolognesi M., Spallarossa A., Coletta M., De Cristofaro R., et al. The bovine basic pancreatic trypsin inhibitor (Kunitz inhibitor): a milestone protein. Curr Protein Pept Sci 2003, 4:231-251.
62. Castaneda O., Harvey A.L. Discovery and characterization of cnidarian peptide toxins that affect neuronal potassium ion channels. Toxicon 2009, 54:1119-1124.
63. Francischetti I.M., Valenzuela J.G., Andersen J.F., Mather T.N., Ribeiro J.M. 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 2002, 99:3602-3612.
64. Monteiro R.Q., Rezaie A.R., Ribeiro J.M., Francischetti I.M. Ixolaris: a factor Xa heparin-binding exosite inhibitor. Biochem J 2005, 387:871-877.
65. Nazareth R.A., Tomaz L.S., Ortiz-Costa S., Atella G.C., Ribeiro J.M., Francischetti I.M., et al. Antithrombotic properties of Ixolaris, a potent inhibitor of the extrinsic pathway of the coagulation cascade. Thromb Haemost 2006, 96:7-13.
66. Monteiro R.Q., Rezaie A.R., Bae J.S., Calvo E., Andersen J.F., Francischetti I.M. Ixolaris binding to factor X reveals a precursor state of factor Xa heparin-binding exosite. Protein Sci 2008, 17:146-153.
67. Carneiro-Lobo T.C., Konig S., Machado D.E., Nasciutti L.E., Forni M.F., Francischetti I.M., et al. Ixolaris, a tissue factor inhibitor, blocks primary tumor growth and angiogenesis in a glioblastoma model. J Thromb Haemost 2009, 7:1855-1864.
68. Rodriguez-Valle M., Vance M., Moolhuijzen P.M., Tao X., Lew-Tabor A.E. Differential recognition by tick-resistant cattle of the recombinantly expressed Rhipicephalus microplus serine protease inhibitor-3 (RMS-3). Ticks Tick Borne Dis 2012, 3:159-169.
69. Chmelar J., Oliveira C.J., Rezacova P., Francischetti I.M., Kovarova Z., Pejler G., et al. A tick salivary protein targets cathepsin G and chymase and inhibits host inflammation and platelet aggregation. Blood 2011, 117:736-744.
70. Chalaire K.C., Kim T.K., Garcia-Rodriguez H., Mulenga A. Amblyomma americanum (L.) (Acari: Ixodidae) tick salivary gland serine protease inhibitor (serpin) 6 is secreted into tick saliva during tick feeding. J Exp Biol 2011, 214:665-673.
71. Walker M.J., Rylett C.M., Keen J.N., Audsley N., Sajid M., Shirras A.D., et al. Proteomic identification of Drosophila melanogaster male accessory gland proteins, including a pro-cathepsin and a soluble gamma-glutamyl transpeptidase. Proteome Sci 2006, 4:9.
72. Wolfner M.F., Harada H.A., Bertram M.J., Stelick T.J., Kraus K.W., Kalb J.M., et al. New genes for male accessory gland proteins in Drosophila melanogaster. Insect Biochem Mol Biol 1997, 27:825-834.
73. Seregni E., Botti C., Ballabio G., Bombardieri E. Biochemical characteristics and recent biological knowledge on prostate-specific antigen. Tumori 1996, 82:72-77.
74. Horka H., Staudt V., Klein M., Taube C., Reuter S., Dehzad N., et al. The tick salivary protein sialostatin L inhibits the Th9-derived production of the asthma-promoting cytokine IL-9 and is effective in the prevention of experimental asthma. J Immunol 2012, 188:2669-2676.
75. Schwarz A., Valdes J.J., Kotsyfakis M. The role of cystatins in tick physiology and blood feeding. Ticks Tick Borne Dis 2012, 3:117-127.
76. Kotsyfakis M., Horka H., Salat J., Andersen J.F. The crystal structures of two salivary cystatins from the tick Ixodes scapularis and the effect of these inhibitors on the establishment of Borrelia burgdorferi infection in a murine model. Mol Microbiol 2010, 77:456-470.
77. Salat J., Paesen G.C., Rezacova P., Kotsyfakis M., Kovarova Z., Sanda M., et al. Crystal structure and functional characterization of an immunomodulatory salivary cystatin from the soft tick Ornithodoros moubata. Biochem J 2010, 429:103-112.
78. Yamaji K., Tsuji N., Miyoshi T., Islam M.K., Hatta T., Alim M.A., et al. A salivary cystatin, HlSC-1, from the ixodid tick Haemaphysalis longicornis play roles in the blood-feeding processes. Parasitol Res 2009, 106:61-68.
79. Kotsyfakis M., Anderson J.M., Andersen J.F., Calvo E., Francischetti I.M., Mather T.N., et al. Cutting edge: Immunity against a "silent" salivary antigen of the Lyme vector Ixodes scapularis impairs its ability to feed. J Immunol 2008, 181:5209-5212.
80. Kotsyfakis M., Karim S., Andersen J.F., Mather T.N., Ribeiro J.M. Selective cysteine protease inhibition contributes to blood-feeding success of the tick Ixodes scapularis. J Biol Chem 2007, 282:29256-29263.
81. Kotsyfakis M., Sa-Nunes A., Francischetti I.M., Mather T.N., Andersen J.F., Ribeiro J.M. Antiinflammatory and immunosuppressive activity of sialostatin L, a salivary cystatin from the tick Ixodes scapularis. J Biol Chem 2006, 281:26298-26307.
82. Moura A.A., Souza C.E., Stanley B.A., Chapman D.A., Killian G.J. Proteomics of cauda epididymal fluid from mature Holstein bulls. J Proteome 2010, 73:2006-2020.
83. Yadav V.K., Chhikara N., Gill K., Dey S., Singh S., Yadav S. Three low molecular weight cysteine proteinase inhibitors of human seminal fluid: purification and enzyme kinetic properties. Biochimie 2013, 95:1552-1559.
84. Fogaca A.C., Almeida I.C., Eberlin M.N., Tanaka A.S., Bulet P., Daffre S. Ixodidin, a novel antimicrobial peptide from the hemocytes of the cattle tick Boophilus microplus with inhibitory activity against serine proteinases. Peptides 2005, 27:667-674.
85. Blandin S., Levashina E.A. Thioester-containing proteins and insect immunity. Mol Immunol 2004, 40:903-908.
86. Kopacek P., Hajdusek O., Buresova V., Daffre S. Tick innate immunity. Adv Exp Med Biol 2010, 708:137-162.
87. Horackova J., Rudenko N., Golovchenko M., Havlikova S., Grubhoffer L. IrML - a gene encoding a new member of the ML protein family from the hard tick, Ixodes ricinus. J Vector Ecol 2010, 35:410-418.
88. Kim Y.S., Ryu J.H., Han S.J., Choi K.H., Nam K.B., Jang I.H., et al. Gram-negative bacteria-binding protein, a pattern recognition receptor for lipopolysaccharide and beta-1,3-glucan that mediates the signaling for the induction of innate immune genes in Drosophila melanogaster cells. J Biol Chem 2000, 275:32721-32727.
89. Rego R.O., Hajdusek O., Kovar V., Kopacek P., Grubhoffer L., Hypsa V. Molecular cloning and comparative analysis of fibrinogen-related proteins from the soft tick Ornithodoros moubata and the hard tick Ixodes ricinus. Insect Biochem Mol Biol 2005, 35:991-1004.
90. Fogaca A.C., Lorenzini D.M., Kaku L.M., Esteves E., Bulet P., Daffre S. Cysteine-rich antimicrobial peptides of the cattle tick Boophilus microplus: isolation, structural characterization and tissue expression profile. Dev Comp Immunol 2004, 28:191-200.
91. Ribeiro J.M., Alarcon-Chaidez F., Francischetti I.M., Mans B.J., Mather T.N., Valenzuela J.G., et al. An annotated catalog of salivary gland transcripts from Ixodes scapularis ticks. Insect Biochem Mol Biol 2006, 36:111-129.
92. Pichu S., Ribeiro J.M., Mather T.N. Purification and characterization of a novel salivary antimicrobial peptide from the tick, Ixodes scapularis. Biochem Biophys Res Commun 2009, 390:511-515.
93. Arolas J.L., Lorenzo J., Rovira A., Castella J., Aviles F.X., Sommerhoff C.P. A carboxypeptidase inhibitor from the tick Rhipicephalus bursa: isolation, cDNA cloning, recombinant expression, and characterization. J Biol Chem 2005, 280:3441-3448.
94. Arolas J.L., Popowicz G.M., Lorenzo J., Sommerhoff C.P., Huber R., Aviles F.X., et al. The three-dimensional structures of tick carboxypeptidase inhibitor in complex with A/B carboxypeptidases reveal a novel double-headed binding mode. J Mol Biol 2005, 350:489-498.
95. Gong H., Zhou J., Liao M., Hatta T., Harnnoi T., Umemiya R., et al. Characterization of a carboxypeptidase inhibitor from the tick Haemaphysalis longicornis. J Insect Physiol 2007, 53:1079-1087.
96. Narasimhan S., Koski R.A., Beaulieu B., Anderson J.F., Ramamoorthi N., Kantor F., et al. A novel family of anticoagulants from the saliva of Ixodes scapularis. Insect Mol Biol 2002, 11:641-650.
97. Sauer J.R., McSwain J.L., Bowman A.S., Essenberg R.C. Tick salivary gland physiology. Annu Rev Entomol 1995, 40:245-267.
98. Bishop R., Lambson B., Wells C., Pandit P., Osaso J., Nkonge C., et al. A cement protein of the tick Rhipicephalus appendiculatus, located in the secretory e cell granules of the type III salivary gland acini, induces strong antibody responses in cattle. Int J Parasitol 2002, 32:833-842.
99. Maruyama S.R., Anatriello E., Anderson J.M., Ribeiro J.M., Brandao L.G., Valenzuela J.G., et al. The expression of genes coding for distinct types of glycine-rich proteins varies according to the biology of three metastriate ticks, Rhipicephalus (Boophilus) microplus, Rhipicephalus sanguineus and Amblyomma cajennense. BMC Genomics 2010, 11:363.
100. Zhou J., Gong H., Zhou Y., Xuan X., Fujisaki K. Identification of a glycine-rich protein from the tick Rhipicephalus haemaphysaloides and evaluation of its vaccine potential against tick feeding. Parasitol Res 2006, 100:77-84.
101. Tian E., Ten Hagen K.G. Recent insights into the biological roles of mucin-type O-glycosylation. Glycoconj J 2009, 26:325-334.
102. Flower D.R., North A.C., Sansom C.E. The lipocalin protein family: structural and sequence overview. Biochim Biophys Acta 2000, 1482:9-24.
103. Mans B.J., Ribeiro J.M., Andersen J.F. Structure, function, and evolution of biogenic amine-binding proteins in soft ticks. J Biol Chem 2008, 283:18721-18733.
104. Paesen G.C., Adams P.L., Harlos K., Nuttall P.A., Stuart D.I. Tick histamine-binding proteins: isolation, cloning, and three-dimensional structure. Mol Cell 1999, 3:661-671.
105. Paesen G.C., Adams P.L., Nuttall P.A., Stuart D.L. Tick histamine-binding proteins: lipocalins with a second binding cavity. Biochim Biophys Acta 2000, 1482:92-101.
106. Mans B.J., Ribeiro J.M. Function, mechanism and evolution of the moubatin-clade of soft tick lipocalins. Insect Biochem Mol Biol 2008, 38:841-852.
107. Mans B.J., Ribeiro J.M. A novel clade of cysteinyl leukotriene scavengers in soft ticks. Insect Biochem Mol Biol 2008, 38:862-870.
108. Nunn M.A., Sharma A., Paesen G.C., Adamson S., Lissina O., Willis A.C., et al. Complement inhibitor of C5 activation from the soft tick Ornithodoros moubata. J Immunol 2005, 174:2084-2091.
109. Francischetti I.M., My Pham V., Mans B.J., Andersen J.F., Mather T.N., Lane R.S., et al. The transcriptome of the salivary glands of the female western black-legged tick Ixodes pacificus (Acari: Ixodidae). Insect Biochem Mol Biol 2005, 35:1142-1161.
110. Calvete J.J., Moreno-Murciano M.P., Theakston R.D., Kisiel D.G., Marcinkiewicz C. Snake venom disintegrins: novel dimeric disintegrins and structural diversification by disulphide bond engineering. Biochem J 2003, 372:725-734.
111. Huang T.F., Niewriarowski S. Disintegrins: the naturally-occurring antagonists of platelet fibrinogen receptors. J Toxicol Toxin Rev 1994, 13:253-273.
112. Bergman D.K., Palmer M.J., Caimano M.J., Radolf J.D., Wikel S.K. Isolation and molecular cloning of a secreted immunosuppressant protein from Dermacentor andersoni salivary gland. J Parasitol 2000, 86:516-525.
113. Deruaz M., Frauenschuh A., Alessandri A.L., Dias J.M., Coelho F.M., Russo R.C., et al. Ticks produce highly selective chemokine binding proteins with antiinflammatory activity. J Exp Med 2008, 205:2019-2031.
114. Frauenschuh A., Power C.A., Deruaz M., Ferreira B.R., Silva J.S., Teixeira M.M., et al. Molecular cloning and characterization of a highly selective chemokine-binding protein from the tick Rhipicephalus sanguineus. J Biol Chem 2007, 282:27250-27258.
115. Wang H., Nuttall P.A. Immunoglobulin-binding proteins in ticks: new target for vaccine development against a blood-feeding parasite. Cell Mol Life Sci 1999, 56:286-295.
116. Wang H., Nuttall P.A. Immunoglobulin G binding proteins in male Rhipicephalus appendiculatus ticks. Parasite Immunol 1995, 17:517-524.
117. Wang H., Nuttall P.A. Immunoglobulin-G binding proteins in the ixodid ticks, Rhipicephalus appendiculatus, Amblyomma variegatum and Ixodes hexagonus. Parasitology 1995, 111:161-165.
118. Wang H., Paesen G.C., Nuttall P.A., Barbour A.G. Male ticks help their mates to feed. Nature 1998, 391:753-754.
119. Ribeiro J.M., Anderson J.M., Manoukis N.C., Meng Z., Francischetti I.M. A further insight into the sialome of the tropical bont tick, Amblyomma variegatum. BMC Genomics 2011, 12:136.
120. Wang H., Nuttall P.A. Excretion of host immunoglobulin in tick saliva and detection of IgG-binding proteins in tick haemolymph and salivary glands. Parasitology 1994, 109(Pt 4):525-530.
121. Bowman A.S., Gengler C.L., Surdick M.R., Zhu K., Essenberg R.C., Sauer J.R., et al. A novel phospholipase A2 activity in saliva of the lone star tick, Amblyomma americanum (L.). Exp Parasitol 1997, 87:121-132.
122. Sonenshine D.E. Pheromones and other semiochemicals of the Acari. Annu Rev Entomol 1985, 30:1-28.
123. Shukla J.N., Nagaraju J. Doublesex: a conserved downstream gene controlled by diverse upstream regulators. J Genet 2010, 89:341-356.
124. Portman D.S. Genetic control of sex differences in C. elegans neurobiology and behavior. Adv Genet 2007, 59:1-37.
125. Kaufman W.R. Assuring paternity in a promiscuous world: are there lessons for ticks among the insects?. Parasitology 2004, 129:S145-S160.
126. Chinery W.A. Studies on the various glands of the tick Haemaphysalis spinigera Neumann 1897. 3. The salivary glands. Acta Trop 1965, 22:321-349.
127. Till W.M. A contribution to the anatomy and histology of the brown ear tick Rhipicephalus appendiculatus Neumann. Mem Entomol Soc South Afr 1961, 6:3-122.
128. Furquim K.C., Bechara G.H., Camargo Mathias M.I. Morpho-histochemical characterization of salivary gland cells of males of the tick Rhipicephalus sanguineus (Acari: Ixodidae) at different feeding stages: description of new cell types. Exp Appl Acarol 2010, 50:59-70.
129. Anyomi F.M., Bior A.D., Essenberg R.C., Sauer J.R. Gene expression in male tick salivary glands is affected by feeding in the presence of females. Arch Insect Biochem Physiol 2006, 63:159-168.
130. Bior A.D., Essenberg R.C., Sauer J.R. Comparison of differentially expressed genes in the salivary glands of male ticks, Amblyomma americanum and Dermacentor andersoni. Insect Biochem Mol Biol 2002, 32:645-655.
131. Xiang F.Y., Zhou Y.Z., Zhou J.L. Identification of differentially expressed genes in the salivary gland of Rhipicephalus haemaphysaloides by the suppression subtractive hybridization approach. J Integr Agr 2012, 11:1528-1536.
132. van de Locht A., Stubbs M.T., Bode W., Friedrich T., Bollschweiler C., Hoffken W., et al. The ornithodorin-thrombin crystal structure, a key to the TAP enigma?. EMBO J 1996, 15:6011-6017.
133. Soares T.S., Watanabe R.M., Tanaka-Azevedo A.M., Torquato R.J., Lu S., Figueiredo A.C., et al. Expression and functional characterization of boophilin, a thrombin inhibitor from Rhipicephalus (Boophilus) microplus midgut. Vet Parasitol 2012, 187:521-528.
134. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987, 4:406-425.
135. Zuckerkand E., Pauling L. Evolutionary divergence and convergence in proteins. Evolving Genes and Proteins 1965, 97-166. Academic Press, New York. V. Bryson, H.J. Vogel (Eds.).