Mosquito saliva induced cutaneous events augment Chikungunya virus replication and disease progression

Infection, Genetics and Evolution

Volumn 40, Issue , 2016, Pages 126-135

  Agarwal, Ankita ^a   Joshi, Gaurav ^a   Nagar, Durga P ^b   Sharma, Ajay K ^c   Sukumaran, D ^c   Pant, Satish C ^b   Parida, Man Mohan ^a   Dash, Paban Kumar ^a  

^a Division of Virology   (India)

^b Div of Pharmacology and Toxicology   (India)

^c Vector Management Division   (India)

Author keywords

Chikungunya; Cutaneous immune response; Mosquito saliva; Pathogenesis

Indexed keywords

BETA INTERFERON; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 4; TOLL LIKE RECEPTOR 3; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN LOCALIZATION; ARTICLE; BLEEDING; CELL INFILTRATION; CELL MIGRATION; CHIKUNGUNYA; CHIKUNGUNYA VIRUS; CONTROLLED STUDY; CUTANEOUS IMMUNE RESPONSE; CUTANEOUS PARAMETERS; DERMIS; DISEASE COURSE; DOWN REGULATION; GENETIC REGULATION; HISTOPATHOLOGY; HYPEREMIA; IMMUNE RESPONSE; IMMUNOREGULATION; INFLAMMATORY CELL; INOCULATION; MOSQUITO; MOSQUITO BITE; MOUSE; MOUSE MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SALIVA; SKIN BLOOD VESSEL; SUBCUTANEOUS TISSUE; SUCKLING ANIMAL; UPREGULATION; VIREMIA; VIRUS LOAD; VIRUS REPLICATION; ANIMAL; CELL LINE; CHEMISTRY; DISEASE MODEL; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; TRANSMISSION; VIROLOGY;

ANIMALS; CELL LINE; CHIKUNGUNYA FEVER; CHIKUNGUNYA VIRUS; CULICIDAE; CYTOKINES; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; MICE; SALIVA; VIRUS REPLICATION;

EID: 84959341720     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2016.02.033     Document Type: Article

References (46)

1. Agarwal A., Singh A.K., Sharma S., Soni M., Thakur A.K., Gopalan N., Parida M.M., Rao P.V., Dash P.K. Application of real-time RT-PCR in vector surveillance and assessment of replication kinetics of an emerging novel ECSA genotype of Chikungunya virus in Aedes aegypti. J. Virol. Methods 2013, 193:419-425.
2. Bissonnette E.Y., Rossignol P.A., Befus A.D. Extracts of mosquito salivary gland inhibit tumour necrosis factor alpha release from mast cells. Parasite Immunol. 1993, 15:27-33.
3. Bortel W.V., Dorleans F., Rosine J., Blateau A., Rousset D., Matheus S., Leparc-Goffart I., Flusin O., Prat C., Cesaire R., Najioullah F., Ardillon V., Balleydier E., Carvalho L., Lemaître A., Noel H., Servas V., Six C., Zurbaran M., Leon L., Guinard A., van den Kerkhof J., Henry M., Fanoy E., Braks M., Reimerink J., Swaan C., Georges R., Brooks L., Freedman J., Sudre B., Zeller H. Chikungunya outbreak in the Caribbean region, December 2013 to March 2014, and the significance for Europe. Euro. Surveill. 2014, 19:20759.
4. Briant L., Despres P., Choumet V., Misse D. Role of skin immune cells on the host susceptibility to mosquito-borne viruses. Virology 2014, 464-465:26-32.
5. Calvo E., Tokumasu F., Marinotti O., Villeval J.L., Ribeiro J.M., Francischetti I.M. Aegyptin, a novel mosquito salivary gland protein, specifically binds to collagen and prevents its interaction with platelet glycoprotein VI, integrin alpha2beta1, and von Willebrand factor. J. Biol. Chem. 2007, 282:26928-26938.
6. Champagne D.E., Ribeiro J.M. Sialokinin I and II: vasodilatory tachykinins from the yellow fever mosquito Aedes aegypti. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:138-142.
7. 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.
8. Conway M.J., Watson A.M., Colpitts T.M., Dragovic S.M., Li Z., Wang P., Feitosa F., Shepherd D.T., Ryman K.D., Klimstra W.B., Anderson J.F., Fikrig E. Mosquito saliva serine protease enhances dissemination of dengue virus into the mammalian host. J. Virol. 2014, 88:164-175.
9. Couderc T., Chretien F., Schilte C., Disson O., Brigitte M., Guivel-Benhassine F., Touret Y., Barau G., Cayet N., Schuffenecker I., Desprès P., Arenzana-Seisdedos F., Michault A., Albert M.L., Lecuit M. A mouse model for Chikungunya: young age and inefficient type-I interferon signaling are risk factors for severe disease. PLoS Pathog. 2008, 4.
10. Coupanec A.L., Babin D., Fiette L., Jouvion G., Ave P., Misse D., Bouloy M., Choumet V. Aedes mosquito saliva modulates Rift Valley fever virus pathogenicity. PLoS Negl. Trop. Dis. 2013, 7.
11. Cox J., Mota J., Sukupolvi-Petty S., Diamond M.S., Rico-Hesse R. Mosquito bite delivery of dengue virus enhances immunogenicity and pathogenesis in humanized mice. J. Virol. 2012, 86:7637-7649.
12. Dash P.K., Parida M.M., Santhosh S.R., Verma S.K., Tripathi N.K., Ambuj S., Saxena P., Gupta N., Chaudhary M., Babu J.P., Lakshmi V., Mamidi N., Subhalaxmi M.V., Lakshmana Rao P.V., Sekhar K. East Central South African genotype as the causative agent in reemergence of Chikungunya outbreak in India. Vector Borne Zoonotic Dis. 2007, 7:519-527.
13. Dhanwani R., Khan M., Alam S.I., Rao P.V., Parida M. Differential proteome analysis of Chikungunya virus infected new-born mice tissues reveal implication of stress, inflammatory and apoptotic pathways in disease pathogenesis. Proteomics 2011, 11:1936-1951.
14. Dhanwani R., Khan M., Lomash V., Rao P.V., Ly H., Parida M. Characterization of Chikungunya virus induced host response in a mouse model of viral myositis. PLoS One 2014, 9.
15. Erichsen J.T., Reiner A., Karten H.J. Co-occurrence of substance P-like and Leu-enkephalin-like immunoreactivities in neurones and fibres of avian nervous system. Nature 1982, 295:407.
16. Flint S.J., Enquist L.W., Racaniello V.R., Skalka A.M. Principles of Virology: Molecular Biology, Pathogenesis and Control of Animal viruses 2004, ASM Press, Washington, D.C., (31-32 pp.). second ed.
17. Fontaine A., Diouf I., Bakkali N., Misse D., Pages F., Fusai T., Rogier C., Almeras L. Implication of haematophagous arthropod salivary proteins in host-vector interactions. Parasit. Vectors 2011, 4:187.
18. Gardner J., Anraku I., Le T.T., Larcher T., Major L., Roques P., Schroder W.A., Higgs S., Suhrbier A. Chikungunya virus arthritis in adult wild-type mice. J. Virol. 2010, 84:8021-8032.
19. Hapuarachchi H.C., Bandara K.B., Sumanadasa S.D., Hapugoda M.D., Lai Y.L., Lee K.S., Tan L.K., Lin R.T., Ng L.F., Bucht G., Abeyewickreme W., Ng L.C. Re-emergence of Chikungunya virus in South-east Asia: virological evidence from Sri Lanka and Singapore. J. Gen. Virol. 2010, 91:1067-1076.
20. Heath W.R., Carbone F.R. The skin-resident and migratory immune system in steady state and memory: innate lymphocytes, dendritic cells and T cells. Nat. Immunol. 2013, 14:978-985.
21. Her Z., Teng T.S., Tan J.J., Teo T.H., Kam Y.W., Lum F.M., Lee W.W., Gabriel C., Melchiotti R., Andiappan A.K., Lulla V., Lulla A., Win M.K., Chow A., Biswas S.K., Leo Y.S., Lecuit M., Merits A., Rénia L., Ng L.F. Loss of TLR3 aggravates CHIKV replication and pathology due to an altered virus-specific neutralizing antibody response. EMBO Mol. Med. 2014, 7:24-41.
22. Jupp P.G., McIntosh B.M. Chikungunya virus disease. CRC Press 1988, vol. II:137-157. Boca Raton, FL. T.P. Monath (Ed.).
23. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real time quantitative PCR and the 2 delta Ct method. Methods 2001, 25:402-408.
24. McCracken M.K., Christofferson R.C., Chisenhall D.M., Mores C.N. Analysis of early dengue virus infection in mice as modulated by Aedes aegypti probing. J. Virol. 2014, 88:1881-1889.
25. McMannus J.F.A., Mowry R.W. General methods for study of the cell and its structure. Staining Methods: Histologic and Histochemical 1965, 73-90. Harper, New York.
26. Monath T.P., Hinz F.X. The alpha viruses. Fields Virology 1996, 843-898. Lippincott-Raven, Philadelphia. third ed. B.N. Fields, D.M. Knipe, P.M. Howley (Eds.).
27. Mores C.N., Christofferson R.C., Davidson S.A. The role of the mosquito in a dengue human infection model. J. Infect. Dis. 2014, 209:S71-S78.
28. Priya Raj, Patro I.K., Parida M.M. TLR3 mediated innate immune response in mice brain following infection with Chikungunya virus. Virus Res. 2014, 189:194-205.
29. Rezza G., Nicoletti L., Angelini R., Romi R., Finarelli A.C., Panning M., Cordioli P., Fortuna C., Boros S., Magurano F., Silvi G., Angelini P., Dottori M., Ciufolini M.G., Majori G.C., Cassone A. Infection with Chikungunya virus in Italy: an outbreak in a temperate region. Lancet 2007, 370:1840-1846.
30. Ribeiro J.M., Francischetti I.M. Role of arthropod saliva in blood feeding: sialome and post-sialome perspectives. Annu. Rev. Entomol. 2003, 48:73-88.
31. Rohousova I., Volf P. Sand fly saliva: effects on host immune response and Leishmania transmission. Folia Parasitol. 2006, 53:161-171.
32. Schaeffer E., Flacher V., Papageorgiou V., Decossas M., Fauny J.D., Kramer M., Mueller C.G. Dermal Cd14+ dendritic cell and macrophage infection by Dengue virus is stimulated by interleukin-4. J. Investig. Dermatol. 2015, 135:1743-1751.
33. Schneider B.S., Higgs S. 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. 2008, 102:400-408.
34. Schneider B.S., Soong L., Girard Y.A., Campbell G., Mason P., Higgs S. Potentiation of West Nile encephalitis by mosquito feeding. Viral Immunol. 2006, 19:74-82.
35. Schneider B.S., McGee C.E., Jordan J.M., Stevenson H.L., Soong L., Higgs S. Prior exposure to uninfected mosquitoes enhances mortality in naturally transmitted West Nile virus infection. PLoS One 2007, 2.
36. Schneider B.S., Soong L., Coffey L.L., Stevenson H.L., McGee C.E., Higgs S. Aedes aegypti saliva alters leukocyte recruitment and cytokine signaling by antigen-presenting cells during West Nile virus infection. PLoS One 2010, 5.
37. Schuffenecker I., Iteman I., Michault A., Murri S., Frangeul L., Vaney M.C., Lavenir R., Pardigon N., Reynes J.M., Pettinelli F., Biscornet L., Diancourt L., Michel S., Duquerroy S., Guigon G., Frenkiel M.P., Bréhin A.C., Cubito N., Desprès P., Kunst F., Rey F.A., Zeller H., Brisse S. Genome microevolution of Chikungunya viruses causing the Indian Ocean outbreak. PLoS Med. 2006, 3.
38. Sergon K., Njuguna C., Kalani R., Ofula V., Onyango C., Konongoi L.S., Bedno S., Burke H., Dumilla A.M., Konde J., Njenga M.K., Sang R., Breiman R.F. Seroprevalence of Chikungunya virus (CHIKV) infection on Lamu Island, Kenya. Am.J.Trop. Med. Hyg. 2004, 78:333-337.
39. Styer L.M., Lim P.Y., Louie K.L., Albright R.G., Kramer L.D., Bernard K.A. Mosquito saliva causes enhancement of West Nile virus infection in mice. J. Virol. 2011, 85:1517-1527.
40. Teo T.H., Lum F.M., Lee W.W., Ng L.F. Mouse models for Chikungunya virus: deciphering immune mechanisms responsible for disease and pathology. Immunol. Res. 2012, 53:136-147.
41. Thangamani S., Higgs S., Ziegler S., Vanlandingham D., Tesh R., Wikel S. Host immune response to mosquito transmitted Chikungunya virus differs from that elicited by needle inoculated virus. PLoS One 2010, 5.
42. Wasserman H.A., Singh S., Champagne D.E. Saliva of the Yellow Fever mosquito, Aedes aegypti, modulates murine lymphocyte function. Parasite Immunol. 2004, 26:295-306.
43. Weaver S.C., Lecuit M. Chikungunya virus and the global spread of a mosquito-borne disease. N. Engl. J. Med. 2015, 372:13.
44. Wei Chiam C., Fun Chan Y., Chai Ong K., Thong Wong K., Sam I.C. Neurovirulence comparison of chikungunya virus isolates of the Asian and East/Central/South African genotypes from Malaysia. J. Gen. Virol. 2015, 96:3243-3254.
45. Zeidner N.S., Higgs S., Happ C.M., Beaty B.J., Miller B.R. 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. 1999, 21:35-44.
46. Ziegler S.A., Lu L., da Rosa A.P., Xiao S.Y., Tesh R.B. An animal model for studying the pathogenesis of chikungunya virus infection. Am.J.Trop. Med. Hyg. 2008, 79:133-139.