Differential salivary gland transcript expression profile in Ixodes scapularis nymphs upon feeding or flavivirus infection

Ticks and Tick-borne Diseases

Volumn 3, Issue 1, 2012, Pages 18-26

  McNally, Kristin L ^a   Mitzel, Dana N ^a   Anderson, Jennifer M ^b   Ribeiro, José M C ^b   Valenzuela, Jesus G ^b   Myers, Timothy G ^b   Godinez, Alvaro ^b   Wolfinbarger, James B ^a   Best, Sonja M ^a   Bloom, Marshall E ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

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

Author keywords

Feeding; Flavivirus; Gene expression; Ixodes scapularis; Nymph; Salivary gland; Tick vector

Indexed keywords

COMPLEMENTARY DNA; CYSTATIN; GLYCINE; THREONINE PROTEINASE; TRANSCRIPTION FACTOR;

ARTICLE; CELL CYCLE REGULATION; CONTROLLED STUDY; DNA LIBRARY; DOWN REGULATION; EXPRESSED SEQUENCE TAG; FEEDING; FLAVIVIRUS; FLAVIVIRUS INFECTION; GENE AMPLIFICATION; GENE EXPRESSION; GENE EXPRESSION PROFILING; HISTONE ACETYLATION; IXODES SCAPULARIS; MICROARRAY ANALYSIS; NONHUMAN; NYMPH; PARASITE VECTOR; PRIORITY JOURNAL; RNA ISOLATION; SALIVARY GLAND; TRANSCRIPTION REGULATION; UPREGULATION;

ANIMALS; ARACHNID VECTORS; DNA, COMPLEMENTARY; DOWN-REGULATION; ENCEPHALITIS VIRUSES, TICK-BORNE; ENCEPHALITIS, TICK-BORNE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE LIBRARY; HOST-PATHOGEN INTERACTIONS; HUMANS; IXODES; MICE; NYMPH; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RNA; SALIVARY GLANDS; TIME FACTORS;

FLAVIVIRUS; IXODES SCAPULARIS; IXODIDA; LANGAT VIRUS;

EID: 84856563713     PISSN: 1877959X     EISSN: 18779603     Source Type: Journal    
DOI: 10.1016/j.ttbdis.2011.09.003     Document Type: Article

References (58)

1. Alarcon-Chaidez F., Ryan R., Wikel S., Dardick K., Lawler C., Foppa I.M., Tomas P., Cushman A., Hsieh A., Spielman A., Bouchard K.R., Dias F., Aslanzadeh J., Krause P.J. Confirmation of tick bite by detection of antibody to Ixodes calreticulin salivary protein. Clin. Vaccine Immunol. 2006, 13:1217-1222.
2. Anguita J., Ramamoorthi N., Hovius J.W., Das S., Thomas V., Persinski R., Conze D., Askenase P.W., Rincon M., Kantor F.S., Fikrig E. Salp15, an Ixodes scapularis salivary protein, inhibits CD4(+) T cell activation. Immunity 2002, 16:849-859.
3. Arca B., Lombardo F., Valenzuela J.G., Francischetti I.M., Marinotti O., Coluzzi M., Ribeiro J.M. An updated catalogue of salivary gland transcripts in the adult female mosquito, Anopheles gambiae. J. Exp. Biol. 2005, 208:3971-3986.
4. Burgdorfer W., Barbour A.G., Hayes S.F., Benach J.L., Grunwaldt E., Davis J.P. Lyme disease - a tick-borne spirochetosis?. Science 1982, 216:1317-1319.
5. Capy P., Gasperi G., Biemont C., Bazin C. Stress and transposable elements: co-evolution or useful parasites?. Heredity 2000, 85(Pt 2):101-106.
6. Charrel R.N., Zaki A.M., Attoui H., Fakeeh M., Billoir F., Yousef A.I., de Chesse R., De Micco P., Gould E.A., de Lamballerie X. Complete coding sequence of the Alkhurma virus, a tick-borne flavivirus causing severe hemorrhagic fever in humans in Saudi Arabia. Biochem. Biophys. Res. Commun. 2001, 287:455-461.
7. Chmelar J., Anderson J.M., Mu J., Jochim R.C., Valenzuela J.G., Kopecky J. Insight into the sialome of the castor bean tick, Ixodes ricinus. BMC Genomics 2008, 9:233.
8. Couillault C., Pujol N., Reboul J., Sabatier L., Guichou J.F., Kohara Y., 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. 2004, 5:488-494.
9. 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, 6:e1001205.
10. Dai J., Wang P., Adusumilli S., Booth C.J., Narasimhan S., Anguita J., Fikrig E. Antibodies against a tick protein, Salp15, protect mice from the Lyme disease agent. Cell Host Microbe 2009, 6:482-492.
11. de la Fuente J., Almazan C., Blouin E.F., Naranjo V., Kocan K.M. Reduction of tick infections with Anaplasma marginale and A. phagocytophilum by targeting the tick protective antigen subolesin. Parasitol. Res. 2006, 100:85-91.
12. Deshpande R.A., Shankar V. Ribonucleases from T2 family. Crit. Rev. Microbiol. 2002, 28:79-122.
13. Ebel G.D., Kramer L.D. Short report: duration of tick attachment required for transmission of powassan virus by deer ticks. Am. J. Trop. Med. Hyg. 2004, 71:268-271.
14. Fialova A., Cimburek Z., Iezzi G., Kopecky J. Ixodes ricinus tick saliva modulates tick-borne encephalitis virus infection of dendritic cells. Microbes Infect. 2010, 12:580-585.
15. 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.
16. Georgieva S., Nabirochkina E., Dilworth F.J., Eickhoff H., Becker P., Tora L., Georgiev P., Soldatov A. The novel transcription factor e(y)2 interacts with TAF(II)40 and potentiates transcription activation on chromatin templates. Mol. Cell Biol. 2001, 21:5223-5231.
17. Gillespie R.D., Mbow M.L., Titus R.G. The immunomodulatory factors of bloodfeeding arthropod saliva. Parasite Immunol. 2000, 22:319-331.
18. Gregson J. Observations on the movement of fluids in the vicinity of the mouthparts of naturally feeding Dermacentor andersoni Stiles. Parasitology 1967, 57:1-8.
19. Hill C.A., Wikel S.K. The Ixodes scapularis Genome Project: an opportunity for advancing tick research. Trends Parasitol. 2005, 21:151-153.
20. Ishimi Y., Kikuchi A. Identification and molecular cloning of yeast homolog of nucleosome assembly protein I which facilitates nucleosome assembly in vitro. J. Biol. Chem. 1991, 266:7025-7029.
21. Kharitonova, N.N., Leoniv, Y.A., 1985. Omsk Hemorrhagic Fever.
22. Kotsyfakis M., Anderson J.M., Andersen J.F., Calvo E., Francischetti I.M., Mather T.N., Valenzuela J.G., Ribeiro J.M. 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.
23. 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.
24. 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.
25. Labuda M., Jones L.D., Williams T., Nuttall P.A. Enhancement of tick-borne encephalitis virus transmission by tick salivary gland extracts. Med. Vet. Entomol. 1993, 7:193-196.
26. Labuda M., Trimnell A.R., Lickova M., Kazimirova M., Davies G.M., Lissina O., Hails R.S., Nuttall P.A. An antivector vaccine protects against a lethal vector-borne pathogen. PLoS Pathog. 2006, 2:e27.
27. Mitzel D.N., Wolfinbarger J.B., Long R.D., Masnick M., Best S.M., Bloom M.E. Tick-borne flavivirus infection in Ixodes scapularis larvae: development of a novel method for synchronous viral infection of ticks. Virology 2007, 365:410-418.
28. Mulenga A., Macaluso K.R., Simser J.A., Azad A.F. The American dog tick, Dermacentor variabilis, encodes a functional histamine release factor homolog. Insect Biochem. Mol. Biol. 2003, 33:911-919.
29. Narasimhan S., Deponte K., Marcantonio N., Liang X., Royce T.E., Nelson K.F., Booth C.J., Koski B., Anderson J.F., Kantor F., Fikrig E. Immunity against Ixodes scapularis salivary proteins expressed within 24hours of attachment thwarts tick feeding and impairs Borrelia transmission. PLoS One 2007, 2:e451.
30. Narasimhan S., Sukumaran B., Bozdogan U., Thomas V., Liang X., DePonte K., Marcantonio N., Koski R.A., Anderson J.F., Kantor F., Fikrig E. A tick antioxidant facilitates the Lyme disease agent's successful migration from the mammalian host to the arthropod vector. Cell Host Microbe 2007, 2:7-18.
31. Negishi M., Pedersen L.G., Petrotchenko E., Shevtsov S., Gorokhov A., Kakuta Y., Pedersen L.C. Structure and function of sulfotransferases. Arch. Biochem. Biophys. 2001, 390:149-157.
32. Nelson N. A journey from mammals to yeast with vacuolar H+-ATPase (V-ATPase). J. Bioenerg. Biomembr. 2003, 35:281-289.
33. Nene V., Lee D., Kang'a S., Skilton R., Shah T., de Villiers E., Mwaura S., Taylor D., Quackenbush J., Bishop R. Genes transcribed in the salivary glands of female Rhipicephalus appendiculatus ticks infected with Theileria parva. Insect Biochem. Mol. Biol. 2004, 34:1117-1128.
34. Nosek J., Ciampor F., Kožuch O., Rajcani J. Localization of tick-borne encephalitis virus in alveolar cells of salivary glands of Dermacentor marginatus and Haemaphysalis inermis ticks. Acta Virol. 1972, 16:493-497.
35. Nuttall P., Jones L. Non-viraemic Tick-borne Transmission: Mechanism and Significance 1991, Modern Acarology 2, Academia, Prague ADN SPB Academic Publishing BV.
36. Nuttall P.A., Jones L.D., Labuda M., Kaufman W.R. Adaptations of arboviruses to ticks. J. Med. Entomol. 1994, 31:1-9.
37. Ohad N., Yadegari R., Margossian L., Hannon M., Michaeli D., Harada J.J., Goldberg R.B., Fischer R.L. Mutations in FIE, a WD polycomb group gene, allow endosperm development without fertilization. Plant Cell 1999, 11:407-416.
38. Orita M., Yamamoto S., Katayama N., Fujita S. Macrophage migration inhibitory factor and the discovery of tautomerase inhibitors. Curr. Pharm. Des. 2002, 8:1297-1317.
39. Otvos L. Antibacterial peptides isolated from insects. J. Pept. Sci. 2000, 6:497-511.
40. Pagel Van Zee J., Geraci N.S., Guerrero F.D., Wikel S.K., Stuart J.J., Nene V.M., Hill C.A. Tick genomics: the Ixodes genome project and beyond. Int. J. Parasitol. 2007, 37:1297-1305.
41. Pancholi P., Kolbert C.P., Mitchell P.D., Reed K.D., Dumler J.S., Bakken J.S., Telford S.R., Persing D.H. Ixodes dammini as a potential vector of human granulocytic ehrlichiosis. J. Infect. Dis. 1995, 172:1007-1012.
42. 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.
43. Pletnev A.G., Men R. Attenuation of the Langat tick-borne flavivirus by chimerization with mosquito-borne flavivirus dengue type 4. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:1746-1751.
44. Ramamoorthi N., Narasimhan S., Pal U., Bao F., Yang X.F., Fish D., Anguita J., Norgard M.V., Kantor F.S., Anderson J.F., Koski R.A., Fikrig E. The Lyme disease agent exploits a tick protein to infect the mammalian host. Nature 2005, 436:573-577.
45. Ribeiro J.M., Alarcon-Chaidez F., Francischetti I.M., Mans B.J., Mather T.N., Valenzuela J.G., Wikel S.K. An annotated catalog of salivary gland transcripts from Ixodes scapularis ticks. Insect Biochem. Mol. Biol. 2006, 36:111-129.
46. Ribeiro J.M., Evans P.M., MacSwain J.L., Sauer J. Amblyomma americanum: characterization of salivary prostaglandins E2 and F2 alpha by RP-HPLC/bioassay and gas chromatography-mass spectrometry. Exp. Parasitol. 1992, 74:112-116.
47. Ribeiro J.M., Makoul G.T., Levine J., Robinson D.R., Spielman A. Antihemostatic, antiinflammatory, and immunosuppressive properties of the saliva of a tick, Ixodes dammini. J. Exp. Med. 1985, 161:332-344.
48. Sa-Nunes A., Bafica A., Lucas D.A., Conrads T.P., Veenstra T.D., Andersen J.F., Mather T.N., Ribeiro J.M., Francischetti I.M. Prostaglandin E2 is a major inhibitor of dendritic cell maturation and function in Ixodes scapularis saliva. J. Immunol. 2007, 179:1497-1505.
49. Smith C.E. A virus resembling Russian spring-summer encephalitis virus from an ixodid tick in malaya. Nature 1956, 178:581-582.
50. Spielman A., Clifford C. Human babesiosis on Natucket Island, USA: description of the vector, Ixodes (Ixodes) dammini, n. sp. (Acarina: Ixodidae). J. Med. Entomol. 1979, 15:218-234.
51. Sukumaran B., Narasimhan S., Anderson J.F., DePonte K., Marcantonio N., Krishnan M.N., Fish D., Telford S.R., Kantor F.S., Fikrig E. An Ixodes scapularis protein required for survival of Anaplasma phagocytophilum in tick salivary glands. J. Exp. Med. 2006, 203:1507-1517.
52. Trimnell A.R., Davies G.M., Lissina O., Hails R.S., Nuttall P.A. A cross-reactive tick cement antigen is a candidate broad-spectrum tick vaccine. Vaccine 2005, 23:4329-4341.
53. Trimnell A.R., Hails R.S., Nuttall P.A. Dual action ectoparasite vaccine targeting 'exposed' and 'concealed' antigens. Vaccine 2002, 20:3560-3568.
54. Tyson K., Elkins C., Patterson H., Fikrig E., de Silva A. Biochemical and functional characterization of Salp20, an Ixodes scapularis tick salivary protein that inhibits the complement pathway. Insect Mol. Biol. 2007, 16:469-479.
55. Valenzuela J.G., Francischetti I.M., Pham V.M., Garfield M.K., Mather T.N., Ribeiro J.M. Exploring the sialome of the tick Ixodes scapularis. J. Exp. Biol. 2002, 205:2843-2864.
56. Wikel S.K. Tick modulation of host immunity: an important factor in pathogen transmission. Int. J. Parasitol. 1999, 29:851-859.
57. Work T. Russian spring-summer encephalitis virus in India. Kyasanur Forest disease. Prog. Med. Virol. 1958, 1.
58. Zilber A., Clifford C. Far Eastern tick-borne spring-summer encephalitis. Am. Rev. Sov. Med. 1946, special supplement, 80 pp.