An insight into the sialome of the soft tick, Ornithodorus parkeri

Insect Biochemistry and Molecular Biology

Volumn 38, Issue 1, 2008, Pages 1-21

  Francischetti, Ivo M B ^a   Mans, Ben J ^a   Meng, Zhaojing ^b   Gudderra, Nanda ^c   Veenstra, Timothy D ^b   Pham, Van M ^a   Ribeiro, José M C ^a  

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

^b SAIC FREDERICK INC   (United States)

^c GEORGE MASON UNIVERSITY   (United States)

Author keywords

Argasidae; Ixodidae; Ornithodorus parkeri; Salivary gland transcriptome; Sialome; Sialotranscriptomes; Tick salivary glands

Indexed keywords

CYSTATIN; ENZYME; LIPOCALIN; MUCIN; PEPTIDE; POLYVINYL DERIVATIVE; POLYVINYLIDENE FLUORIDE;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; BORRELIA; GENE EXPRESSION PROFILING; GENE LIBRARY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PARASITE VECTOR; PROTEOMICS; SALIVA; SALIVARY GLAND; SECRETION; TANDEM MASS SPECTROMETRY; TICK; TWO DIMENSIONAL GEL ELECTROPHORESIS;

AMINO ACID SEQUENCE; ANIMALS; ARACHNID VECTORS; BORRELIA; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CYSTATINS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ENZYMES; GENE EXPRESSION PROFILING; GENE LIBRARY; IXODIDAE; LIPOCALINS; MOLECULAR SEQUENCE DATA; MUCINS; ORNITHODOROS; PEPTIDES; POLYVINYLS; PROTEOMICS; SALIVA; SALIVARY GLANDS; TANDEM MASS SPECTROMETRY;

ARGASIDAE; ARTHROPODA; BORRELIA; BORRELIA PARKERI; HUMAN IMMUNODEFICIENCY VIRUS; IXODIDA; IXODIDAE; ORNITHODOROS;

EID: 36849082002     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2007.09.009     Document Type: Article

References (96)

1. Alarcon-Chaidez F.J., Sun J., and Wikel S.K. Transcriptome analysis of the salivary glands of Dermacentor andersoni Stiles (Acari: Ixodidae). Insect Biochem. Mol. Biol. 37 (2007) 48-71
2. Altschul S.F., Gish W., Miller W., Myers E.W., and Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 215 (1990) 403-410
3. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., and Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25 (1997) 3389-3402
4. Andersen J.F., Gudderra N.P., Francischetti I.M., and Ribeiro J.M. The role of salivary lipocalins in blood feeding by Rhodnius prolixus. Arch. Insect Biochem. Physiol. 58 (2005) 97-105
5. Arca B., Lombardo F., Valenzuela J.G., Francischetti I.M., Marinotti O., Coluzzi M., and Ribeiro J.M. An updated catalogue of salivary gland transcripts in the adult female mosquito, Anopheles gambiae. J. Exp. Biol. 208 (2005) 3971-3986
6. Ascenzi P., Bocedi A., Bolognesi M., Spallarossa A., Coletta M., De Cristofaro R., and Menegatti E. The bovine basic pancreatic trypsin inhibitor (Kunitz inhibitor): a milestone protein. Curr. Protein Pept. Sci. 4 (2003) 231-251
7. Ashburner M., Ball C.A., Blake J.A., Botstein D., Butler H., Cherry J.M., Davis A.P., Dolinski K., Dwight S.S., Eppig J.T., et al. Gene ontology: tool for the unification of biology. The gene ontology consortium. Nat. Genet. 25 (2000) 25-29
8. Bajaj M.S., Birktoft J.J., Steer S.A., and Bajaj S.P. Structure and biology of tissue factor pathway inhibitor. Thromb. Haemostasis 86 (2001) 959-972
9. Bateman A., Birney E., Durbin R., Eddy S.R., Howe K.L., and Sonnhammer E.L. The Pfam protein families database. Nucleic Acids Res. 28 (2000) 263-266
10. Black Jr. W.C., and Piesman J. Phylogeny of hard- and soft-tick taxa (Acari: Ixodida) based on mitochondrial 16S rDNA sequences. Proc. Natl. Acad. Sci. USA 91 (1994) 10034-10038
11. Bowman A.S., Gengler C.L., Surdick M.R., Zhu K., Essenberg R.C., Sauer J.R., and Dillwith J.W. A novel phospholipase A2 activity in saliva of the lone star tick, Amblyomma americanum (L.). Exp. Parasitol. 87 (1997) 121-132
12. Calvo E., Mans B.J., Andersen J.F., and Ribeiro J.M. Function and evolution of a mosquito salivary protein family. J. Biol. Chem. 281 (2006) 1935-1942
13. Campbell C.L., Vandyke K.A., Letchworth G.J., Drolet B.S., Hanekamp T., and Wilson W.C. Midgut and salivary gland transcriptomes of the arbovirus vector Culicoides sonorensis (Diptera: Ceratopogonidae). Insect Mol. Biol. 14 (2005) 121-136
14. Castedo M., Perfettini J.L., Andreau K., Roumier T., Piacentini M., and Kroemer G. Mitochondrial apoptosis induced by the HIV-1 envelope. Ann. N. Y. Acad. Sci. 1010 (2003) 19-28
15. Couillault C., Pujol N., Reboul J., Sabatier L., Guichou J.F., Kohara Y., and Ewbank J.J. TLR-independent control of innate immunity in Caenorhabditis elegans by the TIR domain adaptor protein TIR-1, an ortholog of human SARM. Nat. Immunol. 5 (2004) 488-494
16. Flower D.R. Multiple molecular recognition properties of the lipocalin protein family. J. Mol. Recognition 8 (1995) 185-195
17. Flower D.R. The lipocalin protein family: structure and function. Biochem. J. 318 (1996) 1-14
18. Fogaca A.C., Lorenzini D.M., Kaku L.M., Esteves E., Bulet P., and Daffre S. Cysteine-rich antimicrobial peptides of the cattle tick Boophilus microplus: isolation, structural characterization and tissue expression profile. Dev. Comp. Immunol. 28 (2004) 191-200
19. Francischetti I.M., Valenzuela J.G., Andersen J.F., Mather T.N., and 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 99 (2002) 3602-3612
20. Francischetti I.M., Valenzuela J.G., Pham V.M., Garfield M.K., and Ribeiro J.M. Toward a catalog for the transcripts and proteins (sialome) from the salivary gland of the malaria vector Anopheles gambiae. J. Exp. Biol. 205 (2002) 2429-2451
21. Francischetti I.M., Mather T.N., and 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. 305 (2003) 869-875
22. Francischetti I.M., Mather T.N., and Ribeiro J.M. Penthalaris, a novel recombinant five-Kunitz tissue factor pathway inhibitor (TFPI) from the salivary gland of the tick vector of Lyme disease, Ixodes scapularis. Thromb. Haemostasis 91 (2004) 886-898
23. Francischetti I.M., My Pham V., Mans B.J., Andersen J.F., Mather T.N., Lane R.S., and Ribeiro J.M. The transcriptome of the salivary glands of the female western black-legged tick Ixodes pacificus (Acari: Ixodidae). Insect Biochem. Mol. Biol. 35 (2005) 1142-1161
24. Frauenschuh A., Power C.A., Deruaz M., Ferreira B.R., da Silva J.M., Teixeira M.M., Dias J., Martin T., Wells T.N., and Proudfoot A.E. Molecular cloning and characterization of a highly selective chemokine binding protein from the tick Rhipicephalus sanguineus. J. Biol. Chem. 282 (2007) 27250-27258
25. Galperin M.Y., and Koonin E.V. 'Conserved hypothetical' proteins: prioritization of targets for experimental study. Nucleic Acids Res. 32 (2004) 5452-5463
26. Gaspar A.R., Joubert A.M., Crause J.C., and Neitz A.W. Isolation and characterization of an anticoagulant from the salivary glands of the tick, Ornithodoros savignyi (Acari: Argasidae). Exp. Appl. Acarol. 20 (1996) 583-598
27. Gillespie R.D., Dolan M.C., Piesman J., and Titus R.G. Identification of an IL-2 binding protein in the saliva of the Lyme disease vector tick, Ixodes scapularis. J. Immunol. 166 (2001) 4319-4326
28. Grubhoffer L., Kovar V., and Rudenko N. Tick lectins: structural and functional properties. Parasitology 129 Suppl. (2004) S113-S125
29. Grunclova L., Horn M., Vancova M., Sojka D., Franta Z., Mares M., and Kopacek P. Two secreted cystatins of the soft tick Ornithodoros moubata: differential expression pattern and inhibitory specificity. Biol. Chem. 387 (2006) 1635-1644
30. Gudderra N.P., Ribeiro J.M., and Andersen J.F. Structural determinants of factor IX(a) binding in nitrophorin 2, a lipocalin inhibitor of the intrinsic coagulation pathway. J. Biol. Chem. 280 (2005) 25022-25028
31. Hajnicka V., Kocakova P., Slavikova M., Slovak M., Gasperik J., Fuchsberger N., and Nuttall P.A. Anti-interleukin-8 activity of tick salivary gland extracts. Parasite Immunol. 23 (2001) 483-489
32. Hajnicka V., Vancova I., Kocakova P., Slovak M., Gasperik J., Slavikova M., Hails R.S., Labuda M., and Nuttall P.A. Manipulation of host cytokine network by ticks: a potential gateway for pathogen transmission. Parasitology 130 (2005) 333-342
33. Hansen J.E., Lund O., Tolstrup N., Gooley A.A., Williams K.L., and Brunak S. NetOglyc: prediction of mucin type O-glycosylation sites based on sequence context and surface accessibility. Glycoconjugate J. 15 (1998) 115-130
34. Harnnoi T., Sakaguchi T., Nishikawa Y., Xuan X., and Fujisaki K. Molecular characterization and comparative study of 6 salivary gland metalloproteases from the hard tick, Haemaphysalis longicornis. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 147 (2007) 93-101
35. Hoogstraal H., and Aechlimann A. Tick host specificity. Bull. Soc. Entomol. Suisse 55 (1982) 5-32
36. Huang X., and Madan A. CAP3: a DNA sequence assembly program. Genome Res. 9 (1999) 868-877
37. Isawa H., Yuda M., Orito Y., and Chinzei Y. A mosquito salivary protein inhibits activation of the plasma contact system by binding to factor XII and high molecular weight kininogen. J. Biol. Chem. 13 (2002) 13
38. Joubert A.M., Louw A.I., Joubert F., and Neitz A.W. Cloning, nucleotide sequence and expression of the gene encoding factor Xa inhibitor from the salivary glands of the tick, Ornithodoros savignyi. Exp. Appl. Acarol. 22 (1998) 603-619
39. Keller P.M., Waxman L., Arnold B.A.S.L.D., Condra C., and Connolly T.M. Cloning of the cDNA and expression of moubatin, an inhibitor of platelet-aggregation. J. Biol. Chem. 268 (1993) 5445-5449
40. Konik P., Slavikova V., Salat J., Reznickova J., Dvoroznakova E., and Kopecky J. Anti-tumour necrosis factor-alpha activity in Ixodes ricinus saliva. Parasite Immunol. 28 (2006) 649-656
41. Kotsyfakis M., Sa-Nunes A., Francischetti I.M., Mather T.N., Andersen J.F., and Ribeiro J.M. Antiinflammatory and immunosuppressive activity of sialostatin L, a salivary cystatin from the tick Ixodes scapularis. J. Biol. Chem. 281 (2006) 26298-26307
42. Kovar V., Kopacek P., and Grubhoffer L. Isolation and characterization of Dorin M, a lectin from plasma of the soft tick Ornithodoros moubata. Insect Biochem. Mol. Biol. 30 (2000) 195-205
43. Kumar S., Tamura K., and Nei M. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinf. 5 (2004) 150-163
44. Lai R., Takeuchi H., Jonczy J., Rees H.H., and Turner P.C. A thrombin inhibitor from the ixodid tick, Amblyomma hebraeum. Gene 342 (2004) 243-249
45. Lai R., Takeuchi H., Lomas L.O., Jonczy J., Rigden D.J., Rees H.H., and Turner P.C. A new type of antimicrobial protein with multiple histidines from the hard tick, Amblyomma hebraeum. FASEB J. 18 (2004) 1447-1449
46. Lambson B., Nene V., Obura M., Shah T., Pandit P., Ole-Moiyoi O., Delroux K., Welburn S., Skilton R., de Villiers E., et al. Identification of candidate sialome components expressed in ixodid tick salivary glands using secretion signal complementation in mammalian cells. Insect Mol. Biol. 14 (2005) 403-414
47. Lima C.A., Sasaki S.D., and Tanaka A.S. Bmcystatin, a cysteine proteinase inhibitor characterized from the tick Boophilus microplus. Biochem. Biophys. Res. Commun. 347 (2006) 44-50
48. Mans B.J., and Neitz A.W. Adaptation of ticks to a blood-feeding environment: evolution from a functional perspective. Insect Biochem. Mol. Biol. 34 (2004) 1-17
49. Mans B.J., and Neitz A.W. The mechanism of alphaIIbbeta3 antagonism by savignygrin and its implications for the evolution of anti-hemostatic strategies in soft ticks. Insect Biochem. Mol. Biol. 34 (2004) 573-584
50. Mans B.J., and Neitz A.W. Molecular crowding as a mechanism for tick secretory granule biogenesis. Insect Biochem. Mol. Biol. 34 (2004) 1187-1193
51. Mans B.J., Venter J.D., Vrey P.J., Louw A.I., and Neitz A.W. Identification of putative proteins involved in granule biogenesis of tick salivary glands. Electrophoresis 22 (2001) 1739-1746
52. Mans B.J., Louw A.I., and Neitz A.W. Amino acid sequence and structure modeling of savignin, a thrombin inhibitor from the tick, Ornithodoros savignyi. Insect Biochem. Mol. Biol. 32 (2002) 821-828
53. Mans B.J., Louw A.I., and Neitz A.W. Savignygrin, a platelet aggregation inhibitor from the soft tick Ornithodoros savignyi, presents the RGD integrin recognition motif on the Kunitz-BPTI fold. J. Biol. Chem. 277 (2002) 21371-21378
54. Mans B.J., Steinmann C.M., Venter J.D., Louw A.I., and Neitz A.W. Pathogenic mechanisms of sand tampan toxicoses induced by the tick, Ornithodoros savignyi. Toxicon 40 (2002) 1007-1016
55. Mans B.J., Louw A.I., and Neitz A.W. 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. Mol. Biol. Evol. 20 (2003) 1158-1167
56. Mans, B.J., Andersen, J.F., Francischetti, I.M.B., Valenzuela, J.G., Schwan, T.G., Pham, V.M., Garfield, M.K., Hammer, C.H., Ribeiro, J.M.C., 2007. Comparative sialomics between hard and soft ticks: Implication for the evolution of blood feeding behavior. Insect Biochem. Mol. Biol., in press, doi:10.1016/j.ibmb.2007.09.003.
57. Marchler-Bauer A., Panchenko A.R., Shoemaker B.A., Thiessen P.A., Geer L.Y., and Bryant S.H. CDD: a database of conserved domain alignments with links to domain three-dimensional structure. Nucleic Acids Res. 30 (2002) 281-283
58. Narasimhan S., Koski R.A., Beaulieu B., Anderson J.F., Ramamoorthi N., Kantor F., Cappello M., and Fikrig E. A novel family of anticoagulants from the saliva of Ixodes scapularis. Insect Mol. Biol. 11 (2002) 641-650
59. Nene V., Lee D., Kang'a S., Skilton R., Shah T., de Villiers E., Mwaura S., Taylor D., Quackenbush J., and Bishop R. Genes transcribed in the salivary glands of female Rhipicephalus appendiculatus ticks infected with Theileria parva. Insect Biochem. Mol. Biol. 34 (2004) 1117-1128
60. Nene V., Lee D., Kang'a S., Skilton R., Shah T., de Villiers E., Mwaura S., Taylor D., Quackenbush J., and Bishop R. Genes transcribed in the salivary glands of female Rhipicephalus appendiculatus ticks infected with Theileria parva. Insect Biochem. Mol. Biol. 34 (2004) 1117-1128
61. Nielsen H., Engelbrecht J., Brunak S., and von Heijne G. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10 (1997) 1-6
62. Nienaber J., Gaspar A.R., and Neitz A.W. Savignin, a potent thrombin inhibitor isolated from the salivary glands of the tick Ornithodoros savignyi (Acari: Argasidae). Exp. Parasitol. 93 (1999) 82-91
63. Nunn M.A., Sharma A., Paesen G.C., Adamson S., Lissina O., Willis A.C., and Nuttall P.A. Complement inhibitor of C5 activation from the soft tick Ornithodoros moubata. J. Immunol. 174 (2005) 2084-2091
64. Paesen G.C., Adams P.L., Nuttall P.A., and Stuart D.L. Tick histamine-binding proteins: lipocalins with a second binding cavity. Biochim. Biophys. Acta 1482 (2000) 92-101
65. Page R.D. TreeView: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12 (1996) 357-358
66. Perfettini J.L., Castedo M., Roumier T., Andreau K., Nardacci R., Piacentini M., and Kroemer G. Mechanisms of apoptosis induction by the HIV-1 envelope. Cell Death Differ. 12 Suppl. 1 (2005) 916-923
67. Rego R.O., Hajdusek O., Kovar V., Kopacek P., Grubhoffer L., and 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. 35 (2005) 991-1004
68. Rego R.O., Kovar V., Kopacek P., Weise C., Man P., Sauman I., and Grubhoffer L. The tick plasma lectin, Dorin M, is a fibrinogen-related molecule. Insect Biochem. Mol. Biol. 36 (2006) 291-299
69. Ribeiro J.M., and Francischetti I.M. Role of arthropod saliva in blood feeding: sialome and post-sialome perspectives. Annu. Rev. Entomol. 48 (2003) 73-88
70. Ribeiro J.M., Andersen J., Silva-Neto M.A., Pham V.M., Garfield M.K., and Valenzuela J.G. Exploring the sialome of the blood-sucking bug Rhodnius prolixus. Insect Biochem. Mol. Biol. 34 (2004) 61-79
71. Ribeiro J.M., Charlab R., Pham V.M., Garfield M., and Valenzuela J.G. An insight into the salivary transcriptome and proteome of the adult female mosquito Culex pipiens quinquefasciatus. Insect Biochem. Mol. Biol. 34 (2004) 543-563
72. Ribeiro J.M., Alarcon-Chaidez F., Francischetti I.M., Mans B.J., Mather T.N., Valenzuela J.G., and Wikel S.K. An annotated catalog of salivary gland transcripts from Ixodes scapularis ticks. Insect Biochem. Mol. Biol. 36 (2006) 111-129
73. Ribeiro J.M.C., Schneider M., and Guimaraes J.A. Purification and characterization of Prolixin S (Nitrophorin 2), the salivary anticoagulant of the blood sucking bug, Rhodnius prolixus. Biochem. J. 308 (1995) 243-249
74. Sangamnatdej S., Paesen G.C., Slovak M., and Nuttall P.A. A high affinity serotonin- and histamine-binding lipocalin from tick saliva. Insect Mol. Biol. 11 (2002) 79-86
75. Santos I.K., Valenzuela J.G., Ribeiro J.M., de Castro M., Costa J.N., Costa A.M., da Silva E.R., Neto O.B., Rocha C., Daffre S., et al. Gene discovery in Boophilus microplus, the cattle tick: the transcriptomes of ovaries, salivary glands, and hemocytes. Ann. N. Y. Acad. Sci. 1026 (2004) 242-246
76. Schultz J., Copley R.R., Doerks T., Ponting C.P., and Bork P. SMART: a web-based tool for the study of genetically mobile domains. Nucleic Acids Res. 28 (2000) 231-234
77. Takeya H., Miyata T., Nishino N., Omori-Satoh T., and Iwanaga S. Snake venom hemorrhagic and nonhemorrhagic metalloendopeptidases. Meth. Enzymol. 223 (1993) 365-378
78. Tatusov R.L., Fedorova N.D., Jackson J.D., Jacobs A.R., Kiryutin B., Koonin E.V., Krylov D.M., Mazumder R., Mekhedov S.L., Nikolskaya A.N., et al. The COG database: an updated version includes eukaryotes. BMC Bioinf. 4 (2003) 41
79. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., and Higgins D.G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25 (1997) 4876-4882
80. Urieli-Shoval S., Linke R.P., and Matzner Y. Expression and function of serum amyloid A, a major acute-phase protein, in normal and disease states. Curr. Opin. Hematol. 7 (2000) 64-69
81. Valenzuela J.G., Francischetti I.M.B., Pham V.M., Garfield M.K., Mather T.N., and Ribeiro J.M.C. Exploring the sialome of the tick, Ixodes scapularis. J. Exp. Biol. 205 (2002) 2843-2864
82. Valenzuela J.G., Francischetti I.M., Pham V.M., Garfield M.K., and Ribeiro J.M. Exploring the salivary gland transcriptome and proteome of the Anopheles stephensi mosquito. Insect Biochem. Mol. Biol. 33 (2003) 717-732
83. van de Locht A., Stubbs M.T.B.W., Friedrich T.B.C., Hoffken W., and Huber R. The ornithodorin-thrombin crystal structure, a key to the TAP enigma?. EMBO J. 15 (1996) 6011-6017
84. Visintin A., Iliev D.B., Monks B.G., Halmen K.A., and Golenbock D.T. Md-2. Immunobiology 211 (2006) 437-447
85. Wang X., Zhao Q., and Christensen B.M. Identification and characterization of the fibrinogen-like domain of fibrinogen-related proteins in the mosquito, Anopheles gambiae, and the fruitfly, Drosophila melanogaster, genomes. BMC Genomics 6 (2005) 114
86. Waxman L., and Connolly T.M. Isolation of an inhibitor selective for collagen-stimulated platelet aggregation from the soft tick Ornithodorus moubata. J. Biol. Chem. 268 (1993) 5445-5449
87. Waxman L., Smith D.E., Arcuri K.E., and Vlasuk G.P. Tick anticoagulant peptide (TAP) is a novel inhibitor of blood coagulation Factor Xa. Science 248 (1990) 593-596
88. Yamauchi T., Umeda F., Masakado M., Ono Y., and Nawata H. Serum-free conditioned medium of human diploid fibroblast cells contains an activity that stimulates prostacyclin production by cultured bovine aortic endothelial cells. Biochem. Mol. Biol. Int. 31 (1993) 65-71
89. Yamauchi T., Umeda F., Masakado M., Isaji M., Mizushima S., and Nawata H. Purification and molecular cloning of prostacyclin-stimulating factor from serum-free conditioned medium of human diploid fibroblast cells. Biochem. J. 303 Part 2 (1994) 591-598
90. Zhang S.M., and Loker E.S. The FREP gene family in the snail Biomphalaria glabrata: additional members, and evidence consistent with alternative splicing and FREP retrosequences. Fibrinogen-related proteins. Dev. Comp. Immunol. 27 (2003) 175-187
91. Zhang Y., Ribeiro J.M., Guimaraes J.A., and Walsh P.N. Nitrophorin-2: a novel mixed-type reversible specific inhibitor of the intrinsic factor-X activating complex. Biochemistry 37 (1998) 10681-10690
92. Zhou J., Ueda M., Umemiya R., Battsetseg B., Boldbaatar D., Xuan X., and Fujisaki K. A secreted cystatin from the tick Haemaphysalis longicornis and its distinct expression patterns in relation to innate immunity. Insect Biochem. Mol. Biol. 36 (2006) 527-535
93. Zhu K., Dillwith J.W., Bowman A.S., and Sauer J.R. Identification of hemolytic activity in saliva of the lone star tick (Acari:Ixodidae). J. Med. Entomol. 34 (1997) 160-166
94. Zhu K., Bowman A.S., Dillwith J.W., and Sauer J.R. Phospholipase A2 activity in salivary glands and saliva of the lone star tick (Acari: Ixodidae) during tick feeding. J. Med. Entomol. 35 (1998) 500-504
95. Zimlichman S., Danon A., Nathan I., Mozes G., and Shainkin-Kestenbaum R. Serum amyloid A, an acute phase protein, inhibits platelet activation. J. Lab. Clin. Med. 116 (1990) 180-186
96. Zudaire E., Portal-Nunez S., and Cuttitta F. The central role of adrenomedullin in host defense. J. Leukoc. Biol. 80 (2006) 237-244