A novel reporter system for neutralizing and enhancing antibody assay against dengue virus

BMC Microbiology

Cheng-Feng Qin⁵  E-De Qin⁵  Fu-Chun Zhang³  Bo Zhang⁴  Pei-Yong Shi²  Shun-Ya Zhu⁵  Tao Jiang⁵  Yong-Qiang Deng⁵  Xiao-Feng Li⁵  Zhen-You Jiang¹  Hui Zhao⁵  Ke-Yu Song¹ 

[1] Department of Microbiology and Immunology, School of Medicine Jinan University, Guangzhou 510632, China;Novartis Institute for Tropical Diseases, Singapore 138670, Singapore;Guangzhou No.8 People’s Hospital, Guangzhou 510060, China;State Key Laboratory of Virology, Wuhan Institute of Virology, CAS, Wuhan 430072, China;Department of Virology, State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, China

关键词: Luciferase assay;    Enhancing antibody;    Neutralizing antibody;    Dengue virus;   

Others  :  1141832
DOI  :  10.1186/1471-2180-14-44

 received in 2013-11-05, accepted in 2014-02-12,  发布年份 2014

【 摘 要 】

Background

Dengue virus (DENV) still poses a global public health threat, and no vaccine or antiviral therapy is currently available. Antibody plays distinct roles in controlling DENV infections. Neutralizing antibody is protective against DENV infection, whereas sub-neutralizing concentration of antibody can increase DENV infection, termed antibody-dependent enhancement (ADE). Plaque-based assay represents the most widely accepted method measuring neutralizing or enhancing antibodies.

Results

In this study, a novel reporter virus-based system was developed for measuring neutralization and ADE activity. A stable Renilla luciferase reporter DENV (Luc-DENV) that can produce robust luciferase signals in BHK-21 and K562 cells were used to establish the assay and validated against traditional plaque-based assay. Luciferase value analysis using various known DENV-specific monoclonal antibodies showed good repeatability and a well linear correlation with conventional plaque-based assays. The newly developed assay was finally validated with clinical samples from infected animals and individuals.

Conclusions

This reporter virus-based assay for neutralizing and enhancing antibody evaluation is rapid, lower cost, and high throughput, and will be helpful for laboratory detection and epidemiological investigation for DENV antibodies.

【 授权许可】

   
2014 Song et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 1.

Figure 5.

【 参考文献 】

• [1]Gubler DJ: Epidemic dengue/dengue hemorrhagic fever as a public health, social and economic problem in the 21st century. Trends Microbiol 2002, 10:100-103.
• [2]Simmons CP, Farrar JJ, Nguyen vV, Wills B: Dengue. N Engl J Med 2012, 366:1423-1432.
• [3]Adams B, Holmes EC, Zhang C, Mammen MP Jr, Nimmannitya S, Kalayanarooj S, Boots M: Cross-protective immunity can account for the alternating epidemic pattern of dengue virus serotypes circulating in Bangkok. Proc Natl Acad Sci U S A 2006, 103:14234-14239.
• [4]Halstead SB: Dengue. Lancet 2007, 370:1644-1652.
• [5]Halstead SB: Neutralization and antibody-dependent enhancement of dengue viruses. Adv Virus Res 2013, 60:421-467.
• [6]Halstead SB, O’Rourke EJ: Dengue viruses and mononuclear phagocytes. I. Infection enhancement by non-neutralizing antibody. J Exp Med 1977, 146:201-217.
• [7]Russell PK, Nisalak A: Dengue virus identification by the plaque reduction neutralization test. J Immunol 1967, 99:291-296.
• [8]Jin X, Block OT, Rse R, Schlesinger J: Dengue vaccine development and dengue viral neutralization and enhancement assays. Antivir Ther 2009, 14:739-749.
• [9]Zou G, Xu HY, Qing M, Wang QY, Shi PY: Development and characterization of a stable luciferase dengue virus for high-throughput screening. Antiviral Res 2011, 91:11-19.
• [10]Henchal EA, Gentry MK, McCown JM, Brandt WE: Dengue virus-specific and flavivirus group determinants identified with monoclonal antibodies by indirect immunofluorescence. Am J Trop Med Hyg 1982, 31:830-836.
• [11]Deng YQ, Dai JX, Ji GH, Jiang T, Wang HJ, Yang HO, Tan WL, Liu R, Yu M, Ge BX, Zhu QY, Qin ED, Guo YJ, Qin CF: A broadly flavivirus cross-neutralizing monoclonal antibody that recognizes a novel epitope within the fusion loop of E protein. PLoS One 2011, 6:e16059.
• [12]Kramski M, Drozd A, Lichtfuss GF, Dabrowski PW, Ellerbrok H: Rapid detection of anti-Vaccinia virus neutralizing antibodies. Virol J 2011, 8:139. BioMed Central Full Text
• [13]Kraus AA, Messer W, Haymore LB, de Silva AM: Comparison of plaque- and flow cytometry-based methods for measuring dengue virus neutralization. J Clin Microbiol 2007, 45:3777-3780.
• [14]Minor P, Pipkin P, Jarzebek Z, Knowles W: Studies of neutralising antibodies to SV40 in human sera. J Med Viol 2003, 70:490-495.
• [15]Pierson TC, Diamond MS, Ahmed AA, Valentine LE, Davis CW, Samuel MA, Hanna SL, Puffer BA, Doms RW: An infectious West Nile virus that expresses a GFP reporter gene. Virology 2005, 334:28-40.
• [16]Pierson TC, Sanchez MD, Puffer BA, Ahmed AA, Geiss BJ, Valentine LE, Altamura LA, Diamond MS, Doms RW: A rapid and quantitative assay for measuring antibody-mediated neutralization of West Nile virus infection. Virology 2006, 346:53-65.
• [17]Putnak JR, de la Barrera R, Burgess T, Pardo J, Dessy F, Gheysen D, Lobet Y, Green S, Endy TP, Thomas SJ, Eckels KH, Innis BL, Sun W: Comparative evaluation of three assays for measurement of dengue virus neutralizing antibodies. Am J Trop Med Hyg 2008, 79:115-122.
• [18]Vorndam V, Beltran M: Enzyme-linked immunosorbent assay-format microneutralization test for dengue viruses. Am J Trop Med Hyg 2002, 66:208-212.
• [19]Liu L, Wen K, Li J, Hu D, Huang Y, Qiu L, Cai J, Che X: Comparison of plaque- and enzyme-linked immunospot-based assays to measure the neutralizing activities of monoclonal antibodies specific to domain III of dengue virus envelope protein. Clin Vaccine Immunol 2012, 19:73-78.
• [20]Mattia K, Puffer BA, Williams KL, Gonzalez R, Murray M, Sluzas E, Pagano D, Ajith S, Bower M, Berdougo E, Harris E, Doranz BJ: Dengue reporter virus particles for measuring neutralizing antibodies against each of the four dengue serotypes. PLoS One 2011, 6:e27252.
• [21]Burke CW, Mason JN, Surman SL, Jones BG, Dalloneau E, Hurwitz JL, Russell CJ: Illumination of parainfluenza virus infection and transmission in living animals reveals a tissue-specific dichotomy. PLoS Pathog 2011, 7:e1002134.
• [22]Koutsoudakis G, Kaul A, Steinmann E, Kallis S, Lohmann V, Pietschmann T, Bartenschlager R: Characterization of the early steps of hepatitis C virus infection by using luciferase reporter viruses. J Virol 2006, 80:5308-5320.
• [23]Suree N, Koizumi N, Sahakyan A, Shimizu S, An DS: A novel HIV-1 reporter virus with a membrane-bound Gaussia princeps luciferase. J Virol Methods 2012, 183:49-56.
• [24]van den Worm SH, Eriksson KK, Zevenhoven JC, Weber F, Zust R, Kuri T, Dijkman R, Chang G, Siddell SG, Snijder EJ, Thiel V, Davidson AD: Reverse genetics of SARS-related coronavirus using vaccinia virus-based recombination. PLoS One 2012, 7:e32857.
• [25]Wang X, Deng Y, Li S, Wang G, Qin E, Xu X, Tang R, Qin C: Biomineralization-based virus shell-engineering: towards neutralization escape and tropism expansion. Adv Healthc Mater 2012, 1:443-449.
• [26]Samsa MM, Mondotte JA, Iglesias NG, Assuncao-Miranda I, Barbosa-Lima G, Da Poian AT, Bozza PT, Gamarnik AV: Dengue virus capsid protein usurps lipid droplets for viral particle formation. PLoS Pathog 2009, 5:e1000632.
• [27]Konishi E, Tabuchi Y, Yamanaka A: A simple assay system for infection-enhancing and -neutralizing antibodies to dengue type 2 virus using layers of semi-adherent K562 cells. J Virol Methods 2010, 163:360-367.
• [28]Wu SJ, Grouard-Vogel G, Sun W, Mascola JR, Brachtel E, Putvatana R, Louder MK, Filgueira L, Marovich MA, Wong HK, Blauvelt A, Murphy GS, Robb ML, Innes BL, Birx DL, Hayes CG, Frankel SS: Human skin Langerhans cells are targets of dengue virus infection. Nat Med 2000, 6:816-820.
• [29]Conceicao TM, Da Poian AT, Sorgine MH: A real-time PCR procedure for detection of dengue virus serotypes 1, 2, and 3, and their quantitation in clinical and laboratory samples. J Virol Methods 2010, 163:1-9.
• [30]Halstead SB, O’Rourke EJ, Allison AC: Dengue viruses and mononuclear phagocytes. II. Identity of blood and tissue leukocytes supporting in vitro infection. J Exp Med 1977, 146:218-229.
• [31]Yamanaka A, Kosugi S, Konishi E: Infection-enhancing and -neutralizing activities of mouse monoclonal antibodies against dengue type 2 and 4 viruses are controlled by complement levels. J Virol 2008, 82:927-937.
• [32]Kou Z, Quinn M, Chen H, Rodrigo WW, Rose RC, Schlesinger JJ, Jin X: Monocytes, but not T or B cells, are the principal target cells for dengue virus (DV) infection among human peripheral blood mononuclear cells. J Med Virol 2008, 80:134-146.
• [33]Lambeth CR, White LJ, Johnston RE, de Silva AM: Flow cytometry-based assay for titrating dengue virus. J Clin Microbiol 2005, 43:3267-3272.
• [34]Li J, Hu DM, Ding XX, Chen Y, Pan YX, Qiu LW, Che XY: Enzyme-linked immunosorbent assay-format tissue culture infectious dose-50 test for titrating dengue virus. PLoS One 2011, 6:e22553.
• [35]Moi ML, Lim CK, Kotaki A, Takasaki T, Kurane I: Development of an antibody-dependent enhancement assay for dengue virus using stable BHK-21 cell lines expressing Fc gammaRIIA. J Virol Methods 2010, 163:205-209.
• [36]Boonnak K, Slike BM, Burgess TH, Mason RM, Wu SJ, Sun P, Porter K, Rudiman IF, Yuwono D, Puthavathana P, Marovich MA: Role of dendritic cells in antibody-dependent enhancement of dengue virus infection. J Virol 2008, 82:3939-3951.