Aedes aegypti saliva alters leukocyte recruitment and cytokine signaling by antigen-presenting cells during West Nile virus infection

PLoS ONE

Volumn 5, Issue 7, 2010, Pages

  Schneider, Bradley S ^a,c   Soong, Lynn ^a   Coffey, Lark L ^b   Stevenson, Heather L ^a   McGee, Charles E ^a   Higgs, Stephen ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

^b INSTITUT PASTEUR   (France)

^c Global Viral Forecasting Initiative   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; CYTOKINE; TISSUE EXTRACT;

AEDES AEGYPTI; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN PRESENTING CELL; ARTICLE; CELL POPULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DOWN REGULATION; FEMALE; FLAVIVIRUS INFECTION; FLOW CYTOMETRY; IMMUNOREGULATION; IN VITRO STUDY; IN VIVO STUDY; LEUKOCYTE MIGRATION; LYMPH NODE CELL; LYMPHOCYTIC INFILTRATION; MACROPHAGE ACTIVATION; MOUSE; NONHUMAN; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SALIVA ANALYSIS; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; UPREGULATION; VIRUS DETECTION; VIRUS TRANSMISSION; WEST NILE FLAVIVIRUS; AEDES; ANIMAL; CHEMISTRY; DRUG EFFECT; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; LEUKOCYTE; LYMPH NODE; METABOLISM; PATHOGENICITY; PERITONEUM MACROPHAGE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SALIVA; SINDBIS VIRUS; SKIN; VIROLOGY;

AEDES AEGYPTI; ARBOVIRUS; MUS; VERTEBRATA; WEST NILE VIRUS;

AEDES; ANIMALS; ANTIGEN-PRESENTING CELLS; CYTOKINES; DENDRITIC CELLS; FEMALE; FLOW CYTOMETRY; INTERFERON-BETA; INTERLEUKIN-10; LEUKOCYTES; LYMPH NODES; MACROPHAGES, PERITONEAL; MICE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SALIVA; SINDBIS VIRUS; SKIN; TISSUE EXTRACTS; WEST NILE VIRUS;

EID: 77955400343     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0011704     Document Type: Article

References (64)

1. O'Flaherty JT, Cordes JF (1994) Human neutrophil degranulation responses to nucleotides. Lab Invest 70: 816-821.
2. Byrne SN, Halliday GM, Johnston LJ, King NJ (2001) Interleukin-1beta but not tumor necrosis factor is involved in West Nile virus-induced Langerhans cell migration from the skin in C57BL/6 mice. J Invest Dermatol 117: 702-709.
3. Demeure CE, Brahimi K, Hacini F, Marchand F, Peronet R, et al. (2005) Anopheles mosquito bites activate cutaneous mast cells leading to a local inflammatory response and lymph node hyperplasia. J Immunol 174: 3932-3940.
4. Johnston LJ, Halliday GM, King NJ (2000) Langerhans cells migrate to local lymph nodes following cutaneous infection with an arbovirus. J Invest Dermatol 114: 560-568.
5. Owhashi M, Harada M, Suguri S, Ohmae H, Ishii A (2001) The role of saliva of Anopheles stephensi in inflammatory response: identification of a high molecular weight neutrophil chemotactic factor. Parasitol Res 87: 376-382.
6. Stark KR, James AA (1998) Isolation and characterization of the gene encoding a novel factor Xa-directed anticoagulant from the yellow fever mosquito, Aedes aegypti. J Biol Chem 273: 20802-20809.
7. Anjili CO, Mbati PA, Mwangi RW, Githure JI, Olobo JO, et al. (1995) The chemotactic effect of Phlebotomus duboscqi (Diptera: Psychodidae) salivary gland lysates to murine monocytes. Acta Trop 60: 97-100.
8. Montgomery RR, Lusitani D, De Boisfleury Chevance A, Malawista SE (2004) Tick saliva reduces adherence and area of human neutrophils. Infect Immun 72: 2989-2994.
9. Macaluso KR, Wikel SK (2001) Dermacentor andersoni: effects of repeated infestations on lymphocyte proliferation, cytokine production, and adhesionmolecule expression by BALB/c mice. Ann Trop Med Parasitol 95: 413-427.
10. Maxwell SS, Stoklasek TA, Dash Y, Macaluso KR, Wikel SK (2005) Tick modulation of the in-vitro expression of adhesion molecules by skin-derived endothelial cells. Ann Trop Med Parasitol 99: 661-672.
11. Wanasen N, Nussenzveig RH, Champagne DE, Soong L, Higgs S (2004) Differential modulation of murine host immune response by salivary gland extracts from the mosquitoes Aedes aegypti and Culex quinquefasciatus. Med Vet Entomol 18: 191-199.
12. Wasserman HA, Singh S, Champagne DE (2004) Saliva of the Yellow Fever mosquito, Aedes aegypti, modulates murine lymphocyte function. Parasite Immunol 26: 295-306.
13. Chambers TJ, Diamond MS (2003) The Flaviviruses: Pathogenesis and Immunity; Chambers TJ, T.P. Monath, editor. San Diego: Elsevier Academic Press. 486 p.
14. Ben-Nathan D, Huitinga I, Lustig S, van Rooijen N, Kobiler D (1996) West Nile virus neuroinvasion and encephalitis induced by macrophage depletion in mice. Arch Virol 141: 459-469.
15. Lin YL, Huang YL, Ma SH, Yeh CT, Chiou SY, et al. (1997) Inhibition of Japanese encephalitis virus infection by nitric oxide: antiviral effect of nitric oxide on RNA virus replication. J Virol 71: 5227-5235.
16. Davis CW, Nguyen HY, Hanna SL, Sanchez MD, Doms RW, et al. (2006) West Nile virus discriminates between DC-SIGN and DC-SIGNR for cellular attachment and infection. J Virol 80: 1290-1301.
17. Silva MC, Guerrero-Plata A, Gilfoy FD, Garofalo RP, Mason PW (2007) Differential activation of human monocyte-derived and plasmacytoid dendritic cells by West Nile virus generated in different host cells. J Virol 81: 13640-13648.
18. Martina BE, Koraka P, van den Doel P, Rimmelzwaan GF, Haagmans BL, et al. (2008) DC-SIGN enhances infection of cells with glycosylated West Nile virus in vitro and virus replication in human dendritic cells induces production of IFN-alpha and TNF-alpha. Virus Res 135: 64-71.
19. Thomson SA, Sherritt MA, Medveczky J, Elliott SL, Moss DJ, et al. (1998) Delivery of multiple CD8 cytotoxic T cell epitopes by DNA vaccination. J Immunol 160: 1717-1723.
20. Pacsa AS, Agarwal R, Elbishbishi EA, Chaturvedi UC, Nagar R, et al. (2000) Role of interleukin-12 in patients with dengue hemorrhagic fever. FEMS Immunol Med Microbiol 28: 151-155.
21. Vargin VV, Zschiesche W, Semenov BF (1977) Effects of tilorone hydrochloride on experimental flavivirus infections in mice. Acta Virol 21: 114-118.
22. Taylor JL, Schoenherr C, Grossberg SE (1980) Protection against Japanese encephalitis virus in mice and hamsters by treatment with carboxymethylacridanone, a potent interferon inducer. J Infect Dis 142: 394-399.
23. Haahr S (1971) The influence of Poly I:C on the course of infection in mice inoculated with West Nile virus. Arch Gesamte Virusforsch 35: 1-9.
24. Lobigs M, Pavy M, Hall R (2003) Cross-protective and infection-enhancing immunity in mice vaccinated against flaviviruses belonging to the Japanese encephalitis virus serocomplex. Vaccine 21: 1572-1579.
25. Kuthejlova M, Kopecky J, Stepanova G, Macela A (2001) Tick salivary gland extract inhibits killing of Borrelia afzelii spirochetes by mouse macrophages. Infect Immun 69: 575-578.
26. Waitumbi J, Warburg A (1998) Phlebotomus papatasi saliva inhibits protein phosphatase activity and nitric oxide production by murine macrophages. Infect Immun 66: 1534-1537.
27. Theodos CM, Titus RG (1993) Salivary gland material from the sand fly Lutzomyia longipalpis has an inhibitory effect on macrophage function in vitro. Parasite Immunol 15: 481-487.
28. Soares MB, Titus RG, Shoemaker CB, David JR, Bozza M (1998) The vasoactive peptide maxadilan from sand fly saliva inhibits TNF-alpha and induces IL-6 by mouse macrophages through interaction with the pituitary adenylate cyclase-activating polypeptide (PACAP) receptor. J Immunol 160: 1811-1816.
29. Bishop JV, Mejia JS, Perez de Leon AA, Tabachnick WJ, Titus RG (2006) Salivary gland extracts of culicoides sonorensis inhibit murine lymphocyte proliferation and no production by macrophages. Am J Trop Med Hyg 75: 532-536.
30. Schneider BS, Soong L, Zeidner NS, Higgs S (2004) Aedes aegypti salivary gland extracts modulate anti-viral and TH1/TH2 cytokine responses to sindbis virus infection. Viral Immunol 17: 565-573.
31. Limesand KH, Higgs S, Pearson LD, Beaty BJ (2003) Effect of mosquito salivary gland treatment on vesicular stomatitis New Jersey virus replication and interferon alpha/beta expression in vitro. J Med Entomol 40: 199-205.
32. Hajnicka V, Kocakova P, Slovak M, Labuda M, Fuchsberger N, et al. (2000) Inhibition of the antiviral action of interferon by tick salivary gland extract. Parasite Immunol 22: 201-206.
33. Schneider BS, McGee CE, Jordan JM, Stevenson HL, Soong L, et al. (2007) Prior exposure to uninfected mosquitoes enhances mortality in naturallytransmitted West Nile virus infection. PLoS One 2: e1171.
34. Wang LY (1975) Host preference of mosquito vectors of Japanese encephalitis. Zhonghua Min Guo Wei Sheng Wu Xue Za Zhi 8: 274-279.
35. Turell MJ, Dohm DJ, Sardelis MR, Oguinn ML, Andreadis TG, et al. (2005) An update on the potential of north American mosquitoes (Diptera: Culicidae) to transmit West Nile Virus. J Med Entomol 42: 57-62.
36. Higgs S, Schneider BS, Vanlandingham DL, Klingler KA, Gould EA (2005) Nonviremic transmission of West Nile virus. Proc Natl Acad Sci U S A 102: 8871-8874.
37. Zhang X, Goncalves R, Mosser DM (2008) The isolation and characterization of murine macrophages. Curr Protoc Immunol Chapter 14: Unit 14 11.
38. Sanabria MX, Vargas-Inchaustegui DA, Xin L, Soong L (2008) Role of natural killer cells in modulating dendritic cell responses to Leishmania amazonensis infection. Infect Immun 76: 5100-5109.
39. Schneider BS, Soong L, Girard YA, Campbell G, Mason P, et al. (2006) Potentiation of West Nile encephalitis by mosquito feeding. Viral Immunol 19: 74-82.
40. McGee CE, Schneider BS, Girard YA, Vanlandingham DL, Higgs S (2007) Nonviremic transmission of West Nile virus: evaluation of the effects of space, time, and mosquito species. Am J Trop Med Hyg 76: 424-430.
41. Styer LM, Bernard KA, Kramer LD (2006) Enhanced early West Nile virus infection in young chickens infected by mosquito bite: effect of viral dose. Am J Trop Med Hyg 75: 337-345.
42. Schneider BS, Higgs S (2008) The enhancement of arbovirus transmission and disease by mosquito saliva is associated with modulation of the host immune response. Trans R Soc Trop Med Hyg 102: 400-408.
43. Marletta MA (1994) Approaches toward selective inhibition of nitric oxide synthase. J Med Chem 37: 1899-1907.
44. Bogdan C (2001) Nitric oxide and the immune response. Nat Immunol 2: 907-916.
45. Takhampunya R, Padmanabhan R, Ubol S (2006) Antiviral action of nitric oxide on dengue virus type 2 replication. J Gen Virol 87: 3003-3011.
46. Grisham MB, Granger DN, Lefer DJ (1998) Modulation of leukocyteendothelial interactions by reactive metabolites of oxygen and nitrogen: relevance to ischemic heart disease. Free Radic Biol Med 25: 404-433.
47. Pestka S, Krause CD, Walter MR (2004) Interferons, interferon-like cytokines, and their receptors. Immunol Rev 202: 8-32.
48. Daffis S, Samuel MA, Suthar MS, Keller BC, Gale M, Jr., et al. (2008) Interferon regulatory factor IRF-7 induces the antiviral alpha interferon response and protects against lethal West Nile virus infection. J Virol 82: 8465-8475.
49. Samuel MA, Diamond MS (2005) Alpha/beta interferon protects against lethal West Nile virus infection by restricting cellular tropism and enhancing neuronal survival. J Virol 79: 13350-13361.
50. Guo JT, Hayashi J, Seeger C (2005) West Nile virus inhibits the signal transduction pathway of alpha interferon. J Virol 79: 1343-1350.
51. Depinay N, Hacini F, Beghdadi W, Peronet R, Mecheri S (2006) Mast celldependent down-regulation of antigen-specific immune responses by mosquito bites. J Immunol 176: 4141-4146.
52. Kopecky J, Kuthejlova M, Pechova J (1999) Salivary gland extract from Ixodes ricinus ticks inhibits production of interferon-gamma by the upregulation of interleukin-10. Parasite Immunol 21: 351-356.
53. Zeidner NS, Higgs S, Happ CM, Beaty BJ, Miller BR (1999) Mosquito feeding modulates Th1 and Th2 cytokines in flavivirus susceptible mice: an effect mimicked by injection of sialokinins, but not demonstrated in flavivirus resistant mice. Parasite Immunol 21: 35-44.
54. Brooks DG, Trifilo MJ, Edelmann KH, Teyton L, McGavern DB, et al. (2006) Interleukin-10 determines viral clearance or persistence in vivo. Nat Med 12: 1301-1309.
55. Chaturvedi UC, Elbishbishi EA, Agarwal R, Raghupathy R, Nagar R, et al. (1999) Sequential production of cytokines by dengue virus-infected human peripheral blood leukocyte cultures. J Med Virol 59: 335-340.
56. Ejrnaes M, Filippi CM, Martinic MM, Ling EM, Togher LM, et al. (2006) Resolution of a chronic viral infection after interleukin-10 receptor blockade. J Exp Med 203: 2461-2472.
57. Bai F, Town T, Qian F, Wang P, Kamanaka M, et al. (2009) IL-10 signaling blockade controls murine West Nile virus infection. PLoS Pathog 5: e1000610.
58. Wang T, Scully E, Yin Z, Kim JH, Wang S, et al. (2003) IFN-gamma-producing gamma delta T cells help control murine West Nile virus infection. J Immunol 171: 2524-2531.
59. Agrati C, D'Offizi G, Narciso P, Abrignani S, Ippolito G, et al. (2001) Vdelta1 T lymphocytes expressing a Th1 phenotype are the major gammadelta T cell subset infiltrating the liver of HCV-infected persons. Mol Med 7: 11-19.
60. Agrati C, D'Offizi G, Narciso P, Selva C, Pucillo LP, et al. (2001) Gammadelta T cell activation by chronic HIV infection may contribute to intrahepatic vdelta1 compartmentalization and hepatitis C virus disease progression independent of highly active antiretroviral therapy. AIDS Res Hum Retroviruses 17: 1357-1363.
61. Rakasz E, Mueller A, Perlman S, Lynch RG (1999) Gammadelta T cell response induced by vaginal Herpes simplex 2 infection. Immunol Lett 70: 89-93.
62. Wang T, Gao Y, Scully E, Davis CT, Anderson JF, et al. (2006) Gamma delta T cells facilitate adaptive immunity against West Nile virus infection in mice. J Immunol 177: 1825-1832.
63. Sitati EM, Diamond MS (2006) CD4+ T Cell Responses are Required for Clearance of West Nile Virus from the Central Nervous System. J Virol 80: 12060-12069.
64. Shrestha B, Diamond MS (2004) Role of CD8+ T cells in control of West Nile virus infection. J Virol 78: 8312-8321.