A specific and sensitive antigen capture assay for NS1 protein quantitation in Japanese encephalitis virus infection

Journal of Virological Methods

Volumn 179, Issue 1, 2012, Pages 8-16

  Li, Y Z ^a   Counor, D ^a   Lu, P ^a   Liang, G D ^b   Vu, T Q H ^c   Phan, T N ^d   Huynh, T K L ^c   Sun, G ^a   Grandadam, M ^e   Butrapet, S ^f   Lavergne, J P ^g   Flamand, M ^e   Yu, Y X ^h   Solomon, T ^f   Buchy, P ⁱ   Deubel, V ^a,i  

^a INSTITUTE PASTEUR OF SHANGHAI   (China)

^b CHINESE CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

^c PASTEUR INSTITUTE   (Viet Nam)

^d NATIONAL INSTITUTE OF HYGIENE AND EPIDEMIOLOGY   (Viet Nam)

^e INSTITUT PASTEUR   (France)

^f UNIVERSITY OF LIVERPOOL   (United Kingdom)

^g INSTITUT DE BIOLOGIE ET CHIMIE DES PROTÉINES   (France)

^h NATIONAL INSTITUTE FOR THE CONTROL OF PHARMACEUTICAL AND BIOLOGICAL PRODUCTS   (China)

ⁱ INSTITUT PASTEUR DU CAMBODGE   (Cambodia)

Author keywords

Antigen capture; Flavivirus; Genotype; Japanese encephalitis; Monoclonal antibody; NS1 protein

Indexed keywords

EPITOPE; IMMUNOGLOBULIN G1 ANTIBODY; NONSTRUCTURAL PROTEIN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY AFFINITY; ARTICLE; CELL CLONE; CONTROLLED STUDY; DROSOPHILA; FEMALE; IMMUNOASSAY; JAPANESE ENCEPHALITIS; LIMIT OF DETECTION; MAMMAL CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN SECRETION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; QUANTITATIVE ANALYSIS; SENSITIVITY AND SPECIFICITY;

AGOUTI SIGNALING PROTEIN; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, VIRAL; ANTIGENS, VIRAL; BLOOD CHEMICAL ANALYSIS; CALCIUM-BINDING PROTEINS; CELL LINE; CEREBROSPINAL FLUID; CLINICAL LABORATORY TECHNIQUES; CYCLIC GMP-DEPENDENT PROTEIN KINASES; DROSOPHILA; DROSOPHILA PROTEINS; ENCEPHALITIS, JAPANESE; FEMALE; FLAVIVIRUS INFECTIONS; GTP-BINDING PROTEINS; HUMANS; IMMUNOASSAY; IMMUNOGLOBULIN G; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED C3H; VIRAL NONSTRUCTURAL PROTEINS; VIROLOGY;

FLAVIVIRUS; JAPANESE ENCEPHALITIS VIRUS; MAMMALIA; MUS;

EID: 84855213003     PISSN: 01660934     EISSN: 18790984     Source Type: Journal    
DOI: 10.1016/j.jviromet.2011.06.008     Document Type: Article

References (52)

1. A-Nuegoonpipat A., Panthuyosri N., Anantapreecha S., Chanama S., Sa-Ngasang A., Sawanpanyalert P., Kurane I. Cross-reactive IgM responses in patients with dengue or Japanese encephalitis. J. Clin. Virol. 2008, 42:75-77.
2. Alcon S., Talarmin A., Debruyne M., Falconar A., Deubel V., Flamand M. Enzyme-linked immunosorbent assay specific to dengue virus type 1 nonstructural protein NS1 reveals circulation of the antigen in the blood during the experiencing primary acute phase of disease in patients or secondary infections. J. Clin. Microbiol. 2002, 40:376-381.
3. Burke D.S., Nisalak A., Ussery M.A., Laorakpongse T., Chantavibul S. Kinetics of IgM and IgG responses to Japanese encephalitis virus in human serum and cerebrospinal fluid. J. Infect. Dis. 1985, 151:1093-1099.
4. Busch M.P., Caglioti S., Robertson E.F., McAuley J.D., Tobler L.H., Kamel H., Linnen J.M., Shyamala V., Tomasulo P., Kleinman S.H. Screening the blood supply for West Nile virus RNA by nucleic acid amplification testing. N. Engl. J. Med. 2005, 353:460-467.
5. Chambers T.J., Hahn C.S., Galler R., Rice C.M. Flavivirus genome organization, expression, and replication. Annu. Rev. Microbiol. 1990, 44:649-688.
6. Chen Y., Pan Y., Guo Y., Qiu L., Ding X., Che X. Comprehensive mapping of immunodominant and conserved serotype- and group-specific B-cell epitopes of nonstructural protein 1 from dengue virus type 1. Virology 2010, 398:290-298.
7. Chung K.M., Diamond M.S. Defining the levels of secreted non-structural protein NS1 after West Nile virus infection in cell culture and mice. J. Med. Virol. 2008, 80:547-556.
8. Chung K.M., Liszewski M.K., Nybakken G., Davis A.E., Townsend R.R., Fremont D.H., Atkinson J.P., Diamond M.S. West Nile virus nonstructural protein NS1 inhibits complement activation by binding the regulatory protein factor H. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:19111-19116.
9. Chung K.M., Nybakken G.E., Thompson B.S., Engle M.J., Marri A., Fremont D.H., Diamond M.S. Antibodies against West Nile virus nonstructural protein NS1 prevent lethal infection through Fc gamma receptor-dependent and -independent mechanisms. J. Virol. 2008, 80:1340-1351.
10. Dejnirattisai W., Jumnainsong A., Onsirisakul N., Fitton P., Vasanawathana S., Limpitikul W., Puttikhunt C., Edwards C., Duangchinda T., Supasa S., Chawansuntati K., Malasit P., Mongkolsapaya J., Screaton G. Cross-reacting antibodies enhance dengue virus infection in humans. Science 2010, 328:745-748.
11. Falconar A.K., Young P.R. Production of dimer-specific and dengue virus group cross-reactive mouse monoclonal antibodies to the dengue 2 virus non-structural glycoprotein NS1. J. Gen. Virol. 1991, 72(Pt 4):961-965.
12. Falconar A.K., Young P.R., Miles M.A. Precise location of sequential dengue virus subcomplex and complex B cell epitopes on the nonstructural-1 glycoprotein. Arch. Virol. 1994, 137:315-326.
13. Flamand M., Megret F., Mathieu M., Lepault J., Rey F.A., Deubel V. Dengue virus type 1 nonstructural glycoprotein NS1 is secreted from mammalian cells as a soluble hexamer in a glycosylation-dependent fashion. J. Virol. 1999, 73:6104-6110.
14. Guilarde A.O., Turchi M.D., Siqueira J.B., Feres V.C.R., Rocha B., Levi J.E., Souza V.A.U.F., Boas L.S.V., Pannuti C.S., Martelli C.M.T. Dengue and dengue hemorrhagic fever among adults: clinical outcomes related to viremia, serotypes, and antibody response. J. Infect. Dis. 2008, 197:817-824.
15. Gutsche I., Coulibaly F., Voss J.E., Salmon J., d'Alayer J., Ermonval M., Larquet E., Charneau P., Krey T., Mégret F., Guittet E., Rey F.A., Flamand M. Secreted dengue virus nonstructural protein NS1 is an atypical barrel-shaped high-density lipoprotein. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:8003-8008.
16. Hale J.H., Lim K.A., Chee P.H. Japanese type B encephalitis in Malaya. Ann. Trop. Med. Parasitol. 1952, v46:220-226.
17. Hills S.L., Griggs A.C., Fischer M. Japanese encephalitis in travelers from non-endemic countries, 1973-2008. Am. J. Trop. Med. Hyg. 2010, 82:930-936.
18. Huang C.H., Wong C. Relation of the peripheral multiplication of Japanese B encephalitis virus to the pathogenesis of the infection in mice. Acta Virol. 1963, 7:322-329.
19. Jackson S.T., Mullings A., Bennett F., Khan C., Gordon-Strachan G., Rhoden T. Dengue infection in patients presenting with neurological manifestations in a dengue endemic population. West Ind. Med. J. 2008, 57:373-376.
20. Krishna V.D., Rangappa M., Satchidanandam V. Virus-specific cytolytic antibodies to nonstructural protein 1 of japanese encephalitis virus effect reduction of virus output from infected cells. J. Virol. 2009, 83:4766-4777.
21. Kumar J.S., Parida m., Rao P.V.L. Monoclonal antibody-based antigen capture immunoassay for detection of circulating non-structural protein NS1: implication for early diagnosis of japanese encephalitis virus infection. J. Med. Virol. 2011, 83:1063-1070.
22. Libraty D.H., Young P.R., Pickering D., Endy T.P., Kalayanarooj S., Green S., Vaughn D.W., Nisalak A., Ennis F.A., Rothman A.L. High circulating levels of the dengue virus nonstructural protein NS1 early in dengue illness correlate with the development of dengue hemorrhagic fever. J. Infect. Dis. 2002, 186:1165-1168.
23. Lindenbach B.D., Rice C.M. Genetic interaction of flavivirus nonstructural proteins NS1 and NS4A as a determinant of replicase function. J. Virol. 1999, 73:4611-4621.
24. Macdonald J., Tonry J., Hall R.A., Williams B., Palacios G., Ashok M.S., Jabado O., Clark D., Tesh R.B., Briese T., Lipkin W.I. NS1 protein secretion during the acute phase of West Nile virus infection. J. Virol. 2005, 79:13924-13933.
25. Mackenzie J.S., Gubler D.J., Petersen L.R. Emerging flaviviruses: the spread and resurgence of Japanese encephalitis, West Nile and dengue viruses. Nat. Med. 2004, 10:S98-109.
26. Mason P.W. Maturation of Japanese encephalitis virus glycoproteins produced by infected mammalian and mosquito cells. Virology 1989, 169:354-364.
27. Mohammed M.A.F., Galbraith S.E., Radford A.D., Dove W., Takasaki T., Kurane I., Solomon T. Molecular phylogenetic and evolutionary analysis of Muar strain of Japanese encephalitis virus reveal it is the missing fifth genotype. Infect. Gen. Evol. 2011, 11:855-862.
28. Muylaert I.R., Galler R., Rice C.M. Genetic analysis of the yellow fever virus NS1 protein: identification of a temperature-sensitive mutation which blocks RNA accumulation. J. Virol. 1997, 71:291-298.
29. Myint K.S.A., Gibbons R.V., Perng G.C., Solomon T. Unravelling the neuropathogenesis of Japanese encephalitis. T. Roy. Soc. Trop. Med. H. 2007, 101:955-956.
30. Nguyen T.H., Lei H.Y., Nguyen T.L., Lin Y.S., Huang K.J., Le B.L., Lin C.F., Yeh T.M., Do Q.H., Vu T.Q., Chen L.C., Huang J.H., Lam T.M., Liu C.C., Halstead S.B. Dengue hemorrhagic fever in infants: a study of clinical and cytokine profiles. J. Infect. Dis. 2004, 189:221-232.
31. Noisakran S., Dechtawewat T., Avirutnan P., Kinoshita T., Siripanyaphinyo U., Puttikhunt C., Kasinrerk W., Malasit P., Sittisombut N. Association of dengue virus NS1 protein with lipid rafts. J. Gen. Virol. 2008, 89:2492-2500.
32. Parida M., Dash P.K., Tripathi N.K., Sannarangaiah A.S., Saxena P., Agarwal S., Sahni A.K., Singh S.P., Rathi A.K., Bhargava R., Abhyankar A., Verma S.K., Rao P.V.L., Sekhar K. Japanese encephalitis outbreak, India, 2005. Emerg. Infect. Dis. 2006, 12:1427-1430.
33. Saxena V., Mishra V.K., Dhole T.N. Evaluation of reverse-transcriptase PCR as a diagnostic tool to confirm Japanese encephalitis virus infection. T. Roy. Soc. Trop. Med. H. 2009, 103:403-406.
34. Shirato K., Miyoshi H., Kariwa H., Takashima I. Detection of West Nile virus and Japanese encephalitis virus using real-time PCR with a probe common to both viruses. J. Virol. Methods 2005, 126:119-125.
35. Solomon T. Control of Japanese encephalitis - within our grasp?. N. Engl. J. Med. 2006, 355:869-871.
36. Solomon T., Ni H., Beasley D.W., Ekkelenkamp M., Cardosa M.J., Barrett A.D. Origin and evolution of Japanese encephalitis virus in southeast Asia. J. Virol 2003, 77:3091-3098.
37. Solomon T., Thao L.T.T., Dung N.M., Kneen R., Hung N.T., Nisalak A., Vaughn D.W., Farrar J., Hien T.T., White N.J., Cardosa M.J. Rapid diagnosis of Japanese encephalitis by using an immunoglobulin M dot enzyme immunoassay. J. Clin. Microbiol. 1998, 36:2030-2034.
38. Swami R., Ratho R.K., Mishra B., Singh M.P. Usefulness of RT-PCR for the diagnosis of Japanese encephalitis in clinical samples. Scand. J. Infect. Dis. 2008, 40:815-820.
39. Tang Y.L., Hapip C.A., Liu B., Fang C.T. Highly sensitive TaqMan RT-PCR assay for detection and quantification of both lineages of West Nile virus RNA. J. Clin. Virol. 2006, 36:177-182.
40. Vaughn D.W., Hoke C.H. The epidemiology of Japanese encephalitis: prospects for prevention. Epidemiol. Rev. 1992, 14:197-221.
41. Wallis T.P., Huang C.Y., Nimkar S.B., Young P.R., Gorman J.J. Determination of the disulfide bond arrangement of dengue virus NS1 protein. J. Biol. Chem. 2004, 279:20729-20741.
42. Wang B., Hua R.H., Tian Z.J., Chen N.S., Zhao F.R., Liu T.Q., Wang Y.F., Tong G.Z. Identification of a virus-specific and conserved B-cell epitope on NS1 protein of Japanese encephalitis virus. Virus Res. 2009, 141:90-95.
43. Wang H.Y., Takasaki T., Fu S.H., Sun X.H., Zhang H.L., Wang Z.X., Hao Z.Y., Zhang J.K., Tang Q., Kotaki A., Tajima S., Liang X.F., Yang W.Z., Kurane I., Liang G.D. Molecular epidemiological analysis of Japanese encephalitis virus in China. J. Gen. Virol. 2007, 88:885-894.
44. Wang L.H., Fu S.H., Wang H.Y., Liang X.F., Cheng J.X., Jing H.M., Cai G.L., Li X.W., Ze W.Y., Lv X.J., Wang H.Q., Zhang D.L., Feng Y., Yin Z.D., Sun X.H., Shui T.J., Li M.H., Li Y.X., Liang G.D. Japanese encephalitis outbreak, Yuncheng, China, 2006. Emerg. Infect. Dis. 2007, 13:1123-1125.
45. Wang W.K., Chen H.L., Yang C.F., Hsieh S.C., Juan C.C., Chang S.M., Yu C.C., Lin L.H., Huang J.H., King C.C. Slower rates of clearance of viral load and virus-containing immune complexes in patients with dengue hemorrhagic fever. Clin. Infect. Dis. 2006, 43:1023-1030.
46. Wang Y., Zhou L., Shi H., Xu H., Yao H., Xi X.G., Toyoda T., Wang X., Wang T. Monoclonal antibody recognizing SLLTEVET epitope of M2 protein potently inhibited the replication of influenza A viruses in MDCK cells. Biochem. Biophys. Res. Commun. 2009, 385:118-122.
47. Winkler G., Randolph V.B., Cleaves G.R., Ryan T.E., Stollar V. Evidence that the mature form of the flavivirus nonstructural protein NS1 is a dimer. Virology 1988, 162:187-196.
48. Xu H., Di B., Pan Y.X., Qiu L.W., Wang Y.D., Hao W., He L.J., Yuen K.Y., Che X.Y. Serotype 1-specific monoclonal antibody-based antigen capture immunoassay for detection of circulating nonstructural protein NS1: Implications for early diagnosis and serotyping of dengue virus infections. J. Clin. Microbiol. 2006, 44:2872-2878.
49. Ye X.F., Wang H.Y., Fu S.H., Gao X.Y., Zhao S.Y., Liu C.T., Li M.H., Zhai Y.G., Liang G.D. Etiological spectrum of clinically diagnosed Japanese encephalitis cases reported in Guizhou Province, China, in 2006. J. Clin. Microbiol. 2010, 48:1343-1349.
50. Youn S., Cho H., Fremont D.H., Diamond M.S. A short N-terminal peptide motif on flavivirus nonstructural protein NS1 modulates cellular targeting and immune recognition. J. Virol. 2010, 84:9516-9532.
51. Young P.R., Hilditch P.A., Bletchly C., Halloran W. An antigen capture enzyme-linked immunosorbent assay reveals high levels of the dengue virus protein NS1 in the sera of infected patients. J. Clin. Microbiol. 2000, 38:1053-1057.
52. Zainah S., Wahab A.H., Mariam M., Fauziah M.K., Khairul A.H., Roslina I., Sairulakhma A., Kadimon S.S., Jais M.S., Chua K.B. Performance of a commercial rapid dengue NS1 antigen immunochromatography test with reference to dengue NS1 antigen-capture ELISA. J. Virol. Methods 2009, 155:157-160.