An insight into the proteome of the saliva of the argasid tick Ornithodoros moubata reveals important differences in saliva protein composition between the sexes

Journal of Proteomics

Volumn 80, Issue , 2013, Pages 216-235

  Díaz Martín, Verónica ^a   Manzano Román, Raúl ^a   Valero, Luz ^b   Oleaga, Ana ^a   Encinas Grandes, Antonio ^c   Pérez Sánchez, Ricardo ^a  

^a INSTITUTO DE RECURSOS NATURALES Y AGROBIOLOGÍA DE SALAMANCA   (Spain)

^b UNIVERSITY OF VALENCIA   (Spain)

^c UNIVERSITY OF SALAMANCA   (Spain)

Author keywords

LC MS MS; Ornithodoros moubata; Protein equalization; Proteome; Saliva; Sialome

Indexed keywords

PROTEIN; PROTEOME; SALIVA PROTEIN; SIALOME; UNCLASSIFIED DRUG; ACTIN; ENOLASE; RECOMBINANT PROTEIN;

ANIMAL EXPERIMENT; ARGASIDAE; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; EXOSOME; FEMALE; INTRACELLULAR MEMBRANE; IXODIDAE; LIQUID CHROMATOGRAPHY; LIQUID CHROMATOGRAPHY TANDEM MASS SPECTROMETRY; MALE; NONHUMAN; ORNITHODOROS MOUBATA; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEOMICS; SALIVA; SEX DIFFERENCE; TANDEM MASS SPECTROMETRY; ANIMAL; BIOLOGY; EXPRESSED SEQUENCE TAG; METABOLISM; ORNITHODOROS; PHYSIOLOGY; POLYACRYLAMIDE GEL ELECTROPHORESIS;

ACTINS; ANIMALS; CHROMATOGRAPHY, LIQUID; COMPUTATIONAL BIOLOGY; ELECTROPHORESIS, POLYACRYLAMIDE GEL; EXOSOMES; EXPRESSED SEQUENCE TAGS; FEMALE; MALE; ORNITHODOROS; PHOSPHOPYRUVATE HYDRATASE; PROTEOME; PROTEOMICS; RECOMBINANT PROTEINS; SALIVA; SEX FACTORS; TANDEM MASS SPECTROMETRY;

EID: 84874442360     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2013.01.015     Document Type: Article

References (66)

1. Jongejan F., Uilenberg G. The global importance of ticks. Parasitology 2004, 129:S3-S14.
2. Francischetti I.M., Sa-Nunes A., Mans B.J., Santos I.M., Ribeiro J.M. The role of saliva in tick feeding. Front Biosci 2009, 14:2051-2088.
3. Fontaine A., Diouf I., Bakkali N., Missé D., Pagès F., Fusai T., et al. Implication of haematophagous arthropod salivary proteins in host-vector interactions. Parasit Vectors 2011, 4:187-204.
4. Chemlar J., Calvo E., Pedra J.H.F., Francischetti I.M., Kotsyfakis M. Tick salivary secretion as a source of antihemostatics. J Proteomics 2012, 75:3842-3854.
5. Brossard M., Wikel S.K. Tick immunobiology. Ticks: biology, disease and control 2008, 186-204. Cambridge University Press, Cambridge. A.S. Bowman, P. Nuttall (Eds.).
6. Randolph S.E. Tick-borne disease systems emerge from the shadows: the beauty lies in molecular detail, the message in epidemiology. Parasitology 2009, 136:1403-1413.
7. Maritz-Olivier C., Christian Stutzer C., Jongejan F., Neitz A.W.H., Gaspar A.R.M. Tick anti-hemostatics: targets for future vaccines and therapeutics. Trends Parasitol 2007, 23:397-407.
8. Karim S., Singh P., Ribeiro J.M. A deep insight into the sialotranscriptome of the gulf coast tick, Amblyomma maculatum. PLoS One 2011, 6(12):e28525. 10.1371/journal.pone.0028525.
9. 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, 12:136-147.
10. Vial L. Biological and ecological characteristics of soft ticks (Ixodida: Argasidae) and their impact for predicting tick and associated disease distribution. Parasite 2009, 16:191-202.
11. Díaz-Martín V., Manzano-Román R., Siles-Lucas M., Oleaga A., Pérez-Sánchez R. Cloning, characterization and diagnostic performance of the salivary lipocalin protein TSGP1 from Ornithodoros moubata. Vet Parasitol 2011, 178:163-172.
12. Cutler S. Possibilities for relapsing fever re-emergence. Emerg Infec Dis 2006, 2:369-374.
13. Costard S., Wieland B., de Glanville W., Jori F., Rowlands R., Vosloo W., et al. African swine fever: how can global spread be prevented?. Phil Trans R Soc B 2009, 364:2683-2696.
14. Sánchez-Vizcaíno J.M., Mur L., Martínez-López B. African swine fever: an epidemiological update. Transbound Emerg Dis 2012, 10.1111/j.1865-1682.2011.01293.x.
15. Astigarraga A., Oleaga-Pérez A., Pérez-Sánchez R., Encinas-Grandes A. A study of the vaccinal value of various extracts of concealed antigens and salivary gland extracts against Ornithodoros erraticus and Ornithodoros moubata. Vet Parasitol 1995, 60:133-147.
16. García-Varas S., Manzano-Román R., Fernández-Soto P., Encinas-Grandes A., Oleaga A., Pérez-Sánchez R. Purification and characterization of a P-selectin binding molecule from the salivary glands of Ornithodoros moubata that induces protective anti-tick immune responses in pigs. Int J Parasitol 2010, 40:313-326.
17. Oleaga A., Escudero-Población A., Camafeita E., Pérez-Sánchez R. A proteomic approach to the identification of salivary proteins from the argasid ticks Ornithodoros moubata and Ornithodoros erraticus. Insect Biochem Mol Biol 2007, 37:1149-1159.
18. Pérez-Sánchez R., Oleaga A., Siles-Lucas M., Díaz-Martín V., De La Torre E., Hernández-González A., et al. Aplicación de ecualizadores de proteínas para la identificación de antígenos minoritarios de Ornithodoros moubata. Proteómica 2010, 5:143-145.
19. Baranda J.A., Pérez-Sánchez R., Oleaga-Pérez A., Encinas-Grandes A. Antigens of interest for the diagnosis of parasitism in pigs by Ornithodoros erraticus and Ornithodoros moubata. J Parasitol 1997, 83:831-838.
20. Ribeiro J.M., Endris T.M., Endris R. Saliva of the soft tick, Ornithodoros moubata, contains anti-platelet and apyrase activities. Comp Biochem Physiol 1991, 100A:109-112.
21. Oliveira C.J.F., Cavassani K.A., More D.D., Garlet G.P., Aliberti J.C., Silva J.S., et al. Tick saliva inhibits the chemotactic function of MIP-1a and selectively impairs chemotaxis of immature dendritic cells by down-regulating cell-surface CCR5. Int J Parasitol 2008, 38:705-716.
22. De la Torre-Escudero E., Manzano-Román R., Valero L., Oleaga A., Pérez-Sánchez R., Hernández-González A., et al. Comparative proteomic analysis of Fasciola hepatica juveniles and Schistosoma bovis schistosomula. J Proteomics 2011, 74:1534-1544.
23. Rappsilber J., Ryder U., Lamond A.I., Mann M. Large scale proteomic analysis of the human spliceosome. Genome Res 2002, 12:1231-1245.
24. Ishihama Y., Oda Y., Tabata T., Sato T., Nagasu T., Rappsilber J., et al. Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol Cell Proteomics 2005, 4:1265-1272.
25. Neilson K.A., Ali N.A., Muralidharan S., Mirzaei M., Mariani M., Assadourian G., et al. Less label, more free: approaches in label-free quantitative mass spectrometry. Proteomics 2011, 11:535-553.
26. Bendtsen J.D., Nielsen H., von Heijne G., Brunak S. Improved prediction of signal peptides: SignalP 3.0. J. Mol Biol 2004, 340:783-795.
27. Dyrløv Bendtsen J., Juhl Jensen L., Blom N., von Heijne G., Brunak S. Feature based prediction of non-classical and leaderless protein secretion. Protein Eng Des Sel 2004, 17:349-356.
28. Eisenhaber B., Bork P., Yuan Y., Loeffler G., Eisenhaber F. Automated annotation of GPI anchor sites: case study C. elegans. TIBS 2000, 25:340-341.
29. Francischetti I.M., Mans B.J., Meng Z., Gudderra N., Veenstra T.D., Pham V.M., et al. An insight into the sialome of the soft tick, Ornithodoros parkeri. Insect Biochem Mol Biol 2008, 38:1-21.
30. Francischetti I.M., Meng Z., Mans B.J., Gudderra N., Hall M., Veenstra T.D., et al. An insight into the salivary transcriptome and proteome of the soft tick and vector of epizootic bovine abortion, Ornithodoros coriaceus. J Proteomics 2008, 71:423-512.
31. Díaz-Martín V., Manzano-Román R., Oleaga A., Encinas-Grades A., Pérez-Sánchez R. Cloning and characterization of a plasminogen-binding enolase from the saliva of the argasid tick Ornithodoros moubata. Vet Parasitol 2012, 191:301-314.
32. Manzano-Román R., Díaz-Martín V., Oleaga A., Siles-Lucas M., Pérez-Sánchez R. Subolesin/akirin orthologs from Ornithodoros spp. soft ticks: cloning, RNAi gene silencing and protective effect of the recombinant proteins. Vet Parasitol 2012, 185:248-259.
33. Baranda J.A., Pérez-Sánchez R., Oleaga A., Manzano R., Encinas-Grandes A. Purification, N-terminal sequencing and diagnostic value of the major antigens of Ornithodoros erraticus and O. moubata. Vet Parasitol 2000, 87:193-206.
34. Chinzei Y., Minoura H. Host immunoglobulin G titre and antibody activity in haemolymph of the tick, Ornithodoros moubata. Med Vet Entomol 1987, 1:409-416.
35. Wang H., Nuttall P. Excretion of host immunoglobulin in tick saliva and detection of IgG-binding proteins in tick haemolymph and salivary glands. Parasitology 1994, 109:525-530.
36. Mans B.J., Andersen J.F., Francischetti I.M., Valenzuela J.G., Schwan T.G., Pham V.M., et al. Comparative sialomics between hard and soft ticks: implications for the evolution of blood-feeding behavior. Insect Biochem Mol Biol 2008, 38:42-58.
37. Waxman L., Smith D.E., Arcuri K.E., Vlasuk G.P. Tick anticoagulant peptide (TAP) is a novel inhibitor of blood coagulation factor Xa. Science 1990, 248:593-596.
38. van de Locht A., Stubbs M.T., Bode W., Friedrich T., Bollschweiler C., Höffken W., et al. The ornithodorin-thrombin crystal structure, a key to the TAP enigma?. EMBO J 1996, 15:6011-6017.
39. Roversi P., Lissina O., Johnson S., Ahmat N., Paesen G.C., Ploss K., et al. The structure of OMCI, a novel lipocalin inhibitor of the complement system. J Mol Biol 2007, 369:784-793.
40. Mulenga A., Macaluso K.R., Simser J.A., Azad A.F. The American dog tick, Dermacentor variabilis, encodes a functional histamine release factor homolog. The American dog tick, Dermacentor variabilis. Insect Biochem Mol Biol 2003, 33:911-919.
41. Dai J., Narasimhan S., Zhang L., Liu L., Wang P., Fikrig E. Tick histamine release factor is critical for Ixodes scapularis engorgement and transmission of the lyme disease agent. PLoS Pathog 2010, 11:e1001205.
42. Radisky D.C., Stallis-Mann M., Hirai Y., Bissell M.J. Single proteins might have dual but related functions in intracellular and extracellular microenvironments. Nat Rev 2009, 10:228-234.
43. Madureira P., Vieira M., Magalhães V., Camelo A., Oliveira L., Ribeiro A., et al. Streptococcus agalactiae GAPDH is a virulence-associated immunomodulatory protein. J Immunol 2007, 178:1379-1387.
44. Avilán L., Gualdrón-López M., Quiñones W., González-González L., Hannaert V., Michels P.A., et al. Enolase: a key player in the metabolism and a probable virulence factor of trypanosomatid parasites-perspectives for its use as a therapeutic target. Enzyme Res 2011, 932549. [Epub 2011 Apr 7].
45. Lakkaraju A., Rodriguez-Boulan E. Itinerant exosomes: emerging roles in cell and tissue polarity. Trends Cell Biol 2008, 18:199-209.
46. Ludwig A.K., Giebel B. Exosomes: small vesicles participating in intercellular communication. Int J Biochem Cell Biol 2012, 44:11-15.
47. Mathivanan S., Ji H., Simpson R.J. Exosomes: extracellular organelles important in intercellular communication. J Proteomics 2010, 73:1907-1920.
48. Raimondo F., Morosi L., Chinello C., Magni F., Pitto M. Advances in membranous vesicle and exosome proteomics improving biological understanding and biomarker discovery. Proteomics 2011, 11:709-720.
49. Simons M., Raposo G. Exosomes-vesicular carriers for intercellular communication. Curr Opin Cell Biol 2009, 21:575-581.
50. Mans B.J., Ribeiro J.M.C. A novel clade of cysteinyl leukotriene scavengers in soft ticks. Insect Biochem Mol Biol 2008, 38:862-870.
51. Mans B.J., Ribeiro J.M.C. Function, mechanism and evolution of the moubatin-clade of soft tick lipocalins. Insect Biochem Mol Biol 2008, 3:841-852.
52. Mans B.J., Ribeiro J.M.C., Anderson J.F. Structure, function, and evolution of biogenic amine-binding proteins in soft ticks. J Biol Chem 2008, 283:18721-18733.
53. De la Torre-Escudero E., Manzano-Román R., Pérez-Sánchez R., Siles-Lucas M., Oleaga A. Cloning and characterization of a plasminogen-1 binding, surface-associated enolase from Schistosoma bovis. Vet Parasitol 2010, 173:76-84.
54. Bowman A.S., Ball A., Sauer J.R. Tick salivary glands: the physiology of tick water balance and their role to pathogen trafficking and transmission. Ticks: biology, disease and control 2008, 73-91. Cambridge University Press, Cambridge. A.S. Bowman, P. Nuttall (Eds.).
55. 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.
56. Packila M., Guilfoile P.G. Mating, male Ixodes scapularis express several genes including those with sequence similarity to immunoglobulin-binding proteins and metalloproteases. Exp Appl Acarol 2002, 27:151-160.
57. Aljamali M.N., Ramakrishnan V.G., Weng H., Tucker J.S., Sauer J.R., Essenberg R.C. Microarray analysis of gene expression changes in feeding female and male lone star ticks, Amblyomma americanum (L). Arch Insect Biochem Physiol 2009, 71:236-253.
58. Hajnická V., Vancová I., Kocáková P., Slovák M., Gasperík J., Sláviková M., et al. Manipulation of host cytokine network by ticks: a potential gateway for pathogen transmission. Parasitology 2005, 130(Pt 3):333-342.
59. Wang H., Paesen G., Nutall P., Barbour A. Male ticks help their mates to feed. Nature 1998, 391:753-754.
60. Coons L.B., Roshdy M.A. Ultrastructure of granule secretion in salivary glands of Argas (Persicargas) arboreus during feeding. Z Parasitenkd 1981, 65:225-234.
61. El Shoura S.M. Ultrastructure of salivary glands of Ornithodoros (Omithodoros) moubata (Ixodoidea: Argasidae). J Morphol 1985, 186:45-52.
62. Roshdy M.A. The subgenus Persicargas (Ixodoidea, Argasidae, Argas). 15. Histology and histochemistry of the salivary glands of A. (P.) persicus (Oken). J Med Entomol 1972, 9:143-148.
63. Roshdy M.A., Coons L.B. The subgenus Persicargas (Ixodoidea: Argasidae: Argas). 23. Fine structure of the salivary glands of unfed A. (P.) arboreus Kaiser, Hoogstraal, and Kohls. J Parasitol 1975, 61:743-752.
64. Mans B.J., Venter J.D., Coons L.B., Louw A.I., Neitz A.W.H. A reassessment of argasid tick salivary gland ultrastructure from an immuno-cytochemical perspective. Exp Appl Acarol 2004, 33:119-129.
65. Horigane M., Shinoda T., Honda H., Taylor D. Characterization of a vitellogenin gene reveals two phase regulation of vitellogenesis by engorgement and mating in the soft tick Ornithodoros moubata (Acari: Argasidae). Insect Mol Biol 2010, 19:501-515.
66. 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.