B cell responses during secondary dengue virus infection are dominated by highly cross-reactive, memory-derived plasmablasts

Journal of Virology

Volumn 90, Issue 12, 2016, Pages 5574-5585

  Priyamvada, Lalita ^a   Cho, Alice ^a   Onlamoon, Nattawat ^b   Zheng, Nai Ying ^c   Huang, Min ^c   Kovalenkov, Yevgeniy ^a   Chokephaibulkit, Kulkanya ^b   Angkasekwinai, Nasikarn ^b   Pattanapanyasat, Kovit ^b   Ahmed, Rafi ^a   Wilson, Patrick C ^c   Wrammert, Jens ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MAHIDOL UNIVERSITY   (Thailand)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; MONOCLONAL ANTIBODY; VIRUS ENVELOPE PROTEIN; NEUTRALIZING ANTIBODY; VIRUS ANTIBODY;

ADOLESCENT; ADULT; ANTIBODY DEPENDENT ENHANCEMENT; ANTIBODY SCREENING; ARTICLE; CLONAL VARIATION; CONTROLLED STUDY; CROSS REACTION; DENGUE; DENGUE VIRUS 1; DENGUE VIRUS 2; FEMALE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOPROPHYLAXIS; INFECTION PREVENTION; MALE; MEMORY CELL; MIDDLE AGED; MUTATIONAL ANALYSIS; NONHUMAN; PLASMABLAST; PRIORITY JOURNAL; SECONDARY INFECTION; SOMATIC HYPERMUTATION; VIRION; VIRUS ENVELOPE; VIRUS IMMUNITY; VIRUS NEUTRALIZATION; VIRUS REACTIVATION; YOUNG ADULT; B LYMPHOCYTE; DENGUE VIRUS; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; PATHOPHYSIOLOGY; PLASMA CELL; SEROTYPE; VIROLOGY;

ADOLESCENT; ADULT; ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; ANTIBODY-DEPENDENT ENHANCEMENT; B-LYMPHOCYTES; CROSS REACTIONS; DENGUE; DENGUE VIRUS; EPITOPES, B-LYMPHOCYTE; FEMALE; HUMANS; IMMUNOLOGIC MEMORY; MALE; MIDDLE AGED; PLASMA CELLS; SEROGROUP; VIRAL ENVELOPE PROTEINS; YOUNG ADULT;

EID: 84971449627     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03203-15     Document Type: Article

References (56)

1. Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL, Drake JM, Brownstein JS, Hoen AG, Sankoh O. 2013. The global distribution and burden of dengue. Nature 496:504-507. http://dx.doi.org/10.1038/nature12060.
2. Gibbons RV, Vaughn DW. 2002. Dengue: an escalating problem. BMJ 324:1563-1566. http://dx.doi.org/10.1136/bmj.324.7353.1563.
3. WHO. 2009. Dengue guidelines for diagnosis, treatment, prevention and control, new edition. World Health Organization, Geneva, Switzerland.
4. WHO. 2012. Global strategy for dengue prevention and control, 2012-2020. World Health Organization, Geneva, Switzerland.
5. Guzman MG, Halstead SB, Artsob H, Buchy P, Farrar J, Gubler DJ, Hunsperger E, Kroeger A, Margolis HS, Martínez E. 2010. Dengue: a continuing global threat. Nat Rev Microbiol 8:S7-S16. http://dx.doi.org/10.1038/nrmicro2460.
6. Sabin AB. 1952. Research on dengue during World War II. Am J Trop Med Hyg 1:30-50.
7. Halstead SB, Nimmannitya S, Cohen SN. 1970. Observations related to pathogenesis of dengue hemorrhagic fever. IV. Relation of disease severity to antibody response and virus recovered. Yale J Biol Med 42:311-328.
8. Burke DS, Nisalak A, Johnson DE, Scott RM. 1988. A prospective study of dengue infections in Bangkok. Am J Trop Med Hyg 38:172-180.
9. Sangkawibha N, Rojanasuphot S, Ahandrik S, Viriyapongse S, Jatanasen S, Salitul V, Phanthumachinda B, Halstead SB. 1984. Risk factors in dengue shock syndrome: a prospective epidemiologic study in Rayong, Thailand. I. The 1980 outbreak. Am J Epidemiol 120:653-669.
10. Thein S, Aung MM, Shwe TN, Aye M, Zaw A, Aye K, Aye KM, Aaskov J. 1997. Risk factors in dengue shock syndrome. Am J Trop Med Hyg 56:566-572.
11. Guzman MG, Alvarez M, Halstead SB. 2013. Secondary infection as a risk factor for dengue hemorrhagic fever/dengue shock syndrome: an historical perspective and role of antibody-dependent enhancement of infection. Arch Virol 158:1445-1459. http://dx.doi.org/10.1007/s00705-013-1645-3.
12. Vaughn DW, Green S, Kalayanarooj S, Innis BL, Nimmannitya S, Suntayakorn S, Rothman AL, Ennis FA, Nisalak A. 1997. Dengue in the early febrile phase: viremia and antibody responses. J Infect Dis 176:322-330. http://dx.doi.org/10.1086/514048.
13. Tricou V, Minh NN, Farrar J, Tran HT, Simmons CP. 2011. Kinetics of viremia and NS1 antigenemia are shaped by immune status and virus serotype in adults with dengue. PLoS Negl Trop Dis 5:e1309. http://dx.doi.org/10.1371/journal.pntd.0001309.
14. Rothman AL. 2011. Immunity to dengue virus: a tale of original antigenic sin and tropical cytokine storms. Nat Rev Immunol 11:532-543. http://dx.doi.org/10.1038/nri3014.
15. Wahala WM, Silva AM. 2011. The human antibody response to dengue virus infection. Viruses 3:2374-2395. http://dx.doi.org/10.3390/v3122374.
16. Halstead SB, Chow JS, Marchette NJ. 1973. Immunological enhancement of dengue virus replication. Nat New Biol 243:24-26.
17. 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. 2010. Cross-reacting antibodies enhance dengue virus infection in humans. Science 328:745-748. http://dx.doi.org/10.1126/science.1185181.
18. Mathew A, Rothman AL. 2008. Understanding the contribution of cellular immunity to dengue disease pathogenesis. Immunol Rev 225:300-313. http://dx.doi.org/10.1111/j.1600-065X.2008.00678.x.
19. + T cell responses in relation to commencement of capillary leakage in children with dengue. J Immunol 184:7281-7287. http://dx.doi.org/10.4049/jimmunol.0903262.
20. Green S, Vaughn DW, Kalayanarooj S, Nimmannitya S, Suntayakorn S, Nisalak A, Lew R, Innis BL, Kurane I, Rothman AL. 1999. Early immune activation in acute dengue illness is related to development of plasma leakage and disease severity. J Infect Dis 179:755-762. http://dx.doi.org/10.1086/314680.
21. Halstead SB. 2003. Neutralization and antibody-dependent enhancement of dengue viruses. Adv Virus Res 60:421-467. http://dx.doi.org/10.1016/S0065-3527(03)60011-4.
22. Halstead SB, O'Rourke EJ. 1977. Dengue viruses and mononuclear phagocytes. I. Infection enhancement by non-neutralizing antibody. J Exp Med 146:201-217.
23. Beltramello M, Williams KL, Simmons CP, Macagno A, Simonelli L, Quyen NT, Sukupolvi-Petty S, Navarro-Sanchez E, Young PR, de Silva AM, Rey FA, Varani L, Whitehead SS, Diamond MS, Harris E, Lanzavecchia A, Sallusto F. 2010. The human immune response to Dengue virus is dominated by highly cross-reactive antibodies endowed with neutralizing and enhancing activity. Cell Host Microbe 8:271-283. http://dx.doi.org/10.1016/j.chom.2010.08.007.
24. Friberg H, Jaiswal S, West K, O'Ketch M, Rothman AL, Mathew A. 2012. Analysis of human monoclonal antibodies generated by dengue virus-specific memory B cells. Viral Immunol 25:348-359. http://dx.doi.org/10.1089/vim.2012.0010.
25. Smith SA, Zhou Y, Olivarez NP, Broadwater AH, de Silva AM, Crowe JE, Jr. 2012. Persistence of circulating memory B cell clones with potential for dengue virus disease enhancement for decades following infection. J Virol 86:2665-2675. http://dx.doi.org/10.1128/JVI.06335-11.
26. Toh YX, Gan V, Balakrishnan T, Zuest R, Poidinger M, Wilson S, Appanna R, Thein TL, Ong AK, Ng LC, Leo YS, Fink K. 2014. Dengue serotype cross-reactive, anti-E protein antibodies confound specific immune memory for 1 year after infection. Front Immunol 5:388. http://dx.doi.org/10.3389/fimmu.2014.00388.
27. Wrammert J, Onlamoon N, Akondy RS, Perng GC, Polsrila K, Chandele A, Kwissa M, Pulendran B, Wilson PC, Wittawatmongkol O, Yoksan S, Angkasekwinai N, Pattanapanyasat K, Chokephaibulkit K, Ahmed R. 2012. Rapid and massive virus-specific plasmablast responses during acute dengue virus infection in humans. J Virol 86:2911-2918. http://dx.doi.org/10.1128/JVI.06075-11.
28. Garcia-Bates TM, Cordeiro MT, Nascimento EJ, Smith AP, Soares de Melo KM, McBurney SP, Evans JD, Marques ET, Jr, Barratt-Boyes SM. 2013. Association between magnitude of the virus-specific plasmablast response and disease severity in dengue patients. J Immunol 190:80-87. http://dx.doi.org/10.4049/jimmunol.1103350.
29. Xu M, Hadinoto V, Appanna R, Joensson K, Toh YX, Balakrishnan T, Ong SH, Warter L, Leo YS, Wang CI, Fink K. 2012. Plasmablasts generated during repeated dengue infection are virus glycoproteinspecific and bind to multiple virus serotypes. J Immunol 189:5877-5885. http://dx.doi.org/10.4049/jimmunol.1201688.
30. Yenchitsomanus PT, Sricharoen P, Jaruthasana I, Pattanakitsakul SN, Nitayaphan S, Mongkolsapaya J, Malasit P. 1996. Rapid detection and identification of dengue viruses by polymerase chain reaction (PCR). Southeast Asian J Trop Med Public Health 27:228-236.
31. Innis BL, Nisalak A, Nimmannitya S, Kusalerdchariya S, Chongswasdi V, Suntayakorn S, Puttisri P, Hoke CH. 1989. An enzyme-linked immunosorbent assay to characterize dengue infections where dengue and Japanese encephalitis co-circulate. Am J Trop Med Hyg 40:418-427.
32. Wrammert J, Smith K, Miller J, Langley WA, Kokko K, Larsen C, Zheng NY, Mays I, Garman L, Helms C, James J, Air GM, Capra JD, Ahmed R, Wilson PC. 2008. Rapid cloning of high-affinity human monoclonal antibodies against influenza virus. Nature 453:667-671. http://dx.doi.org/10.1038/nature06890.
33. Smith K, Garman L, Wrammert J, Zheng N-Y, Capra JD, Ahmed R, Wilson PC. 2009. Rapid generation of fully human monoclonal antibodies specific to a vaccinating antigen. Nat Protoc 4:372-384. http://dx.doi.org/10.1038/nprot.2009.3.
34. Crotty S, Aubert RD, Glidewell J, Ahmed R. 2004. Tracking human antigen-specific memory B cells: a sensitive and generalized ELISPOT system. J Immunol Methods 286:111-122. http://dx.doi.org/10.1016/j.jim.2003.12.015.
35. Tiller T, Meffre E, Yurasov S, Tsuiji M, Nussenzweig MC, Wardemann H. 2008. Efficient generation of monoclonal antibodies from single human B cells by single cell RT-PCR and expression vector cloning. J Immunol Methods 329:112-124. http://dx.doi.org/10.1016/j.jim.2007.09.017.
36. Pauli NT, Kim HK, Falugi F, Huang M, Dulac J, Henry Dunand C, Zheng NY, Kaur K, Andrews SF, Huang Y, DeDent A, Frank KM, Charnot-Katsikas A, Schneewind O, Wilson PC. 2014. Staphylococcus aureus infection induces protein A-mediated immune evasion in humans. J Exp Med 211:2331-2339. http://dx.doi.org/10.1084/jem.20141404.
37. WHO. 1997. Dengue hemorrhagic fever: diagnosis, treatment, prevention and control. World Health Organization, Geneva, Switzerland.
38. Wrammert J, Koutsonanos D, Li GM, Edupuganti S, Sui J, Morrissey M, McCausland M, Skountzou I, Hornig M, Lipkin WI, Mehta A, Razavi B, Del Rio C, Zheng NY, Lee JH, Huang M, Ali Z, Kaur K, Andrews S, Amara RR, Wang Y, Das SR, O'Donnell CD, Yewdell JW, Subbarao K, Marasco WA, Mulligan MJ, Compans R, Ahmed R, Wilson PC. 2011. Broadly cross-reactive antibodies dominate the human B cell response against 2009 pandemic H1N1 influenza virus infection. J Exp Med 208:181-193. http://dx.doi.org/10.1084/jem.20101352.
39. Puerta-Guardo H, Mosso C, Medina F, Liprandi F, Ludert JE, del Angel RM. 2010. Antibody-dependent enhancement of dengue virus infection in U937 cells requires cholesterol-rich membrane microdomains. J Gen Virol 91:394-403. http://dx.doi.org/10.1099/vir.0.015420-0.
40. Liao HX, Chen X, Munshaw S, Zhang R, Marshall DJ, Vandergrift N, Whitesides JF, Lu X, Yu JS, Hwang KK, Gao F, Markowitz M, Heath SL, Bar KJ, Goepfert PA, Montefiori DC, Shaw GC, Alam SM, Margolis DM, Denny TN, Boyd SD, Marshal E, Egholm M, Simen BB, Hanczaruk B, Fire AZ, Voss G, Kelsoe G, Tomaras GD, Moody MA, Kepler TB, Haynes BF. 2011. Initial antibodies binding to HIV-1 gp41 in acutely infected subjects are polyreactive and highly mutated. J Exp Med 208: 2237-2249. http://dx.doi.org/10.1084/jem.20110363.
41. Zheng NY, Wilson K, Jared M, Wilson PC. 2005. Intricate targeting of immunoglobulin somatic hypermutation maximizes the efficiency of affinity maturation. J Exp Med 201:1467-1478. http://dx.doi.org/10.1084/jem.20042483.
42. Tsai WY, Lai CY, Wu YC, Lin HE, Edwards C, Jumnainsong A, Kliks S, Halstead S, Mongkolsapaya J, Screaton GR, Wang WK. 2013. Highavidity and potently neutralizing cross-reactive human monoclonal antibodies derived from secondary dengue virus infection. J Virol 87:12562-12575. http://dx.doi.org/10.1128/JVI.00871-13.
43. Vaughan K, Greenbaum J, Blythe M, Peters B, Sette A. 2010. Metaanalysis of all immune epitope data in the Flavivirus genus: inventory of current immune epitope data status in the context of virus immunity and immunopathology. Viral Immunol 23:259-284. http://dx.doi.org/10.1089/vim.2010.0006.
44. Dejnirattisai W, Wongwiwat W, Supasa S, Zhang X, Dai X, Rouvinski A, Jumnainsong A, Edwards C, Quyen NT, Duangchinda T, Grimes JM, Tsai WY, Lai CY, Wang WK, Malasit P, Farrar J, Simmons CP, Zhou ZH, Rey FA, Mongkolsapaya J, Screaton GR. 2015. A new class of highly potent, broadly neutralizing antibodies isolated from viremic patients infected with dengue virus. Nat Immunol 16:170-177. http://dx.doi.org/10.1038/ni.3058.
45. Tsai WY, Durbin A, Tsai JJ, Hsieh SC, Whitehead S, Wang WK. 2015. Complexity of neutralizing antibodies against multiple dengue virus serotypes after heterotypic immunization and secondary infection revealed by in-depth analysis of cross-reactive antibodies. J Virol 89:7348-7362. http://dx.doi.org/10.1128/JVI.00273-15.
46. de Alwis R, Smith SA, Olivarez NP, Messer WB, Huynh JP, Wahala WM, White LJ, Diamond MS, Baric RS, Crowe JE, Jr, de Silva AM. 2012. Identification of human neutralizing antibodies that bind to complex epitopes on dengue virions. Proc Natl Acad SciUSA109:7439-7444. http://dx.doi.org/10.1073/pnas.1200566109.
47. Kim JH, Skountzou I, Compans R, Jacob J. 2009. Original antigenic sin responses to influenza viruses. J Immunol 183:3294-3301. http://dx.doi.org/10.4049/jimmunol.0900398.
48. Choi YS, Baek YH, Kang W, Nam SJ, Lee J, You S, Chang DY, Youn JC, Choi YK, Shin EC. 2011. Reduced antibody responses to the pandemic (H1N1) 2009 vaccine after recent seasonal influenza vaccination. Clin Vaccine Immunol 18:1519-1523. http://dx.doi.org/10.1128/CVI.05053-11.
49. Fazekas de St Groth, Webster RG. 1966. Disquisitions of Original Antigenic Sin. I. Evidence in man. J Exp Med 124:331-345.
50. Pyhala R. 1985. Antibody status to influenza A/Singapore/1/57(H2N2) in Finland during a period of outbreaks caused by H3N2 and H1N1 subtype viruses. J Hyg 95:437-445. http://dx.doi.org/10.1017/S0022172400062860.
51. Halstead SB, Rojanasuphot S, Sangkawibha N. 1983. Original antigenic sin in dengue. Am J Trop Med Hyg 32:154-156.
52. Midgley CM, Bajwa-Joseph M, Vasanawathana S, Limpitikul W, Wills B, Flanagan A, Waiyaiya E, Tran HB, Cowper AE, Chotiyarnwong P, Grimes JM, Yoksan S, Malasit P, Simmons CP, Mongkolsapaya J, Screaton GR. 2011. An in-depth analysis of original antigenic sin in dengue virus infection. J Virol 85:410-421. http://dx.doi.org/10.1128/JVI.01826-10.
53. Vaughn DW, Green S, Kalayanarooj S, Innis BL, Nimmannitya S, Suntayakorn S, Endy TP, Raengsakulrach B, Rothman AL, Ennis FA, Nisalak A. 2000. Dengue viremia titer, antibody response pattern, and virus serotype correlate with disease severity. J Infect Dis 181:2-9. http://dx.doi.org/10.1086/315215.
54. Guzman MG, Kouri G, Valdes L, Bravo J, Vazquez S, Halstead SB. 2002. Enhanced severity of secondary dengue-2 infections: death rates in 1981 and 1997 Cuban outbreaks. Rev Panam Salud Publica 11:223-227. http://dx.doi.org/10.1590/S1020-49892002000400003.
55. Kliks SC, Nisalak A, Brandt WE, Wahl L, Burke DS. 1989. Antibodydependent enhancement of dengue virus growth in human monocytes as a risk factor for dengue hemorrhagic fever. Am J Trop Med Hyg 40:444-451.
56. Nimmannitya S, Halstead SB, Cohen SN, Margiotta MR. 1969. Dengue and chikungunya virus infection in man in Thailand, 1962-1964. I. Observations on hospitalized patients with hemorrhagic fever. Am J Trop Med Hyg 18:954.