Dengue virus infection induces broadly cross-reactive human IgM antibodies that recognize intact virions in humanized BLT-NSG mice

Experimental Biology and Medicine

Volumn 240, Issue 1, 2015, Pages 67-78

  Jaiswal, Smita ^a   Smith, Kenneth ^b   Ramirez, Alejandro ^a   Woda, Marcia ^a   Pazoles, Pamela ^a   Shultz, Leonard D ^c   Greiner, Dale L ^a   Brehm, Michael A ^a   Mathew, Anuja ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

^c JACKSON LABORATORY   (United States)

Author keywords

B cells; dengue; human; transgenic mice; viral

Indexed keywords

CD19 ANTIGEN; CD20 ANTIGEN; CD27 ANTIGEN; CD38 ANTIGEN; CD5 ANTIGEN; COMMON ACUTE LYMPHOBLASTIC LEUKEMIA ANTIGEN; CROSS REACTING ANTIBODY; EPITOPE; HUMAN ANTI DENGUE VIRUS ANTIBODY; IMMUNOGLOBULIN D; IMMUNOGLOBULIN M; UNCLASSIFIED DRUG; VIRUS ANTIBODY; VIRUS ENVELOPE PROTEIN; VIRUS RNA; NEUTRALIZING ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY ISOLATION; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ARTICLE; B LYMPHOCYTE; BINDING AFFINITY; CONTROLLED STUDY; CONVALESCENCE; CROSS REACTION; DENGUE; DENGUE VIRUS 2; ENGRAFTMENT; FETAL TISSUE TRANSPLANTATION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOGENICITY; LIVER; MOLECULAR CLONING; MOUSE; NONHUMAN; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; SERODIAGNOSIS; THYMUS; VIRAL LOAD TESTING; VIRION; VIRUS LOAD; VIRUS NEUTRALIZATION; ANIMAL; BLOOD; DENGUE VIRUS; DISEASE MODEL; IMMUNOLOGY; SCID MOUSE; TRANSGENIC MOUSE; VIROLOGY;

ANIMALIA; DENGUE VIRUS; MUS; MUS MUSCULUS;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; B-LYMPHOCYTES; DENGUE; DENGUE VIRUS; DISEASE MODELS, ANIMAL; HUMANS; IMMUNOGLOBULIN M; LIVER; MICE; MICE, SCID; MICE, TRANSGENIC; THYMUS GLAND; VIRAL LOAD;

EID: 84920992684     PISSN: 15353702     EISSN: 15353699     Source Type: Journal    
DOI: 10.1177/1535370214546273     Document Type: Article

References (49)

1. Sabin AB.Research on dengue during World War II.Am J Tropic Med Hygiene. 1952;1:30-50
2. Burke DS,Nisalak A,Johnson DE,Scott RM.A prospective study of dengue infections in Bangkok.Am J Tropic Med Hygiene. 1988;38:172-80
3. Thein S,Aung MM,Shwe TN,Aye M,Zaw A,Aye K,Aye KM,Aaskov J.Risk factors in dengue shock syndrome.Am J Tropic Med Hygiene. 1997;56:566-72
4. Rothman AL.Immunity to dengue virus: a tale of original antigenic sin and tropical cytokine storms.Nat Rev. 2011;11:532-43
5. Murphy BR,Whitehead SS.Immune response to dengue virus and prospects for a vaccine.Ann Rev Immunol. 2011;29:587-619
6. Kaufman BM,Summers PL,Dubois DR,Eckels KH.Monoclonal antibodies against dengue 2 virus E-glycoprotein protect mice against lethal dengue infection.Am J Tropic Med Hygiene. 1987;36:427-34
7. Sukupolvi-Petty S,Austin SK,Engle M,Brien JD,Dowd KA,Williams KL,Johnson S,Rico-Hesse R,Harris E,Pierson TC,Fremont DH,Diamond MS.Structure and function analysis of therapeutic monoclonal antibodies against dengue virus type 2.J Virol. 2010;84:9227-39
8. Endy TP,Nisalak A,Chunsuttitwat S,Vaughn DW,Green S,Ennis FA,Rothman AL,Libraty DH.Relationship of pre-existing dengue virus (DV) neutralizing antibody levels to viremia and disease severity in a prospective cohort study of DV infection in Thailand.J infect Dis. 2004;189:990-1000
9. Goncalvez AP, Engle RE, St Claire M, Purcell RH, Lai CJ. Monoclonal antibody-mediated enhancement of dengue virus infection in vitro and in vivo and strategies for prevention. In: Proceedings of the National Academy of Sciences of the United States of America, 2007;104:9422–7.
10. Kliks SC,Nimmanitya S,Nisalak A,Burke DS.Evidence that maternal dengue antibodies are important in the development of dengue hemorrhagic fever in infants.Am J Tropic Med Hygiene. 1988;38:411-9
11. Kliks SC,Nisalak A,Brandt WE,Wahl L,Burke DS.Antibody-dependent enhancement of dengue virus growth in human monocytes as a risk factor for dengue hemorrhagic fever.Am J Tropic Med Hygiene. 1989;40:444-51
12. 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.Rapid and massive virus-specific plasmablast responses during acute dengue virus infection in humans.J Virol. 2012;86:2911-8
13. Xu M,Hadinoto V,Appanna R,Joensson K,Toh YX,Balakrishnan T,Ong SH,Warter L,Leo YS,Wang CI,Fink K.Plasmablasts generated during repeated dengue infection are virus glycoprotein-specific and bind to multiple virus serotypes.J Immunol. 2012;189:5877-85
14. Garcia-Bates TM,Cordeiro MT,Nascimento EJ,Smith AP,Soares de Melo KM,McBurney SP,Evans JD,Marques ET,Barratt-Boyes SM.Association between magnitude of the virus-specific plasmablast response and disease severity in dengue patients.J Immunol. 2012;190:80-7
15. Zompi S,Montoya M,Pohl MO,Balmaseda A,Harris E.Dominant cross-reactive B cell response during secondary acute dengue virus infection in humans.PLoS Neglect Tropic Dis. 2012;6:e1568-e1568
16. 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.The human immune response to Dengue virus is dominated by highly cross-reactive antibodies endowed with neutralizing and enhancing activity.Cell Host Microbe. 2010;8:271-83
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.Cross-reacting antibodies enhance dengue virus infection in humans.Science. 2010;328:745-8
18. Schieffelin JS,Costin JM,Nicholson CO,Orgeron NM,Fontaine KA,Isern S,Michael SF,Robinson JE.Neutralizing and non-neutralizing monoclonal antibodies against dengue virus E protein derived from a naturally infected patient.Virol J. 2010;7:28-28
19. de Alwis R,Beltramello M,Messer WB,Sukupolvi-Petty S,Wahala WM,Kraus A,Olivarez NP,Pham Q,Brian J,Tsai WY,Wang WK,Halstead S,Kliks S,Diamond MS,Baric R,Lanzavecchia A,Sallusto F,de Silva AM.In-depth analysis of the antibody response of individuals exposed to primary dengue virus infection.PLoS Neglect Tropic Dis. 2010;5:e1188-e1188
20. Smith SA,Zhou Y,Olivarez NP,Broadwater AH,de Silva AM,Crowe JE.Persistence of circulating B memory cell clones with potential for dengue virus disease enhancement for decades following infection.J Virol. 2011;:
21. Setthapramote C,Sasaki T,Puiprom O,Limkittikul K,Pitaksajjakul P,Pipattanaboon C,Sasayama M,Leuangwutiwong P,Phumratanaprapin W,Chamnachanan S,Kusolsuk T,Jittmittraphap A,Asai A,Arias JF,Hirai I,Kuhara M,Okuno Y,Kurosu T,Ramasoota P,Ikuta K.Human monoclonal antibodies to neutralize all dengue virus serotypes using lymphocytes from patients at acute phase of the secondary infection.Biochem Biophys Res Commun. 2012;423:867-72
22. Wahala WM,Silva AM.The human antibody response to dengue virus infection.Viruses. 2011;3:2374-95
23. Cox J,Mota J,Sukupolvi-Petty S,Diamond MS,Rico-Hesse R.Mosquito bite delivery of dengue virus enhances immunogenicity and pathogenesis in humanized mice.J Virol. 2012;86:7637-49
24. Jaiswal S,Pazoles P,Woda M,Shultz LD,Greiner DL,Brehm MA,Mathew A.Enhanced humoral and HLA-A2-restricted dengue virus-specific T-cell responses in humanized BLT NSG mice.Immunology. 2012;136:334-43
25. Jaiswal S,Pearson T,Friberg H,Shultz LD,Greiner DL,Rothman AL,Mathew A.Dengue virus infection and virus-specific HLA-A2 restricted immune responses in humanized NOD-scid IL2rgammanull mice.PloS One. 2009;4:e7251-e7251
26. Kuruvilla JG,Troyer RM,Devi S,Akkina R.Dengue virus infection and immune response in humanized RAG2(-/-)gamma(c)(-/-) (RAG-hu) mice.Virology. 2007;369:143-52
27. Mota J,Rico-Hesse R.Humanized mice show clinical signs of dengue fever according to infecting virus genotype.J Virol. 2009;83:8638-45
28. Costin JM,Zaitseva E,Kahle KM,Nicholson CO,Rowe DK,Graham AS,Bazzone LE,Hogancamp G,Figueroa Sierra M,Fong RH,Yang ST,Lin L,Robinson JE,Doranz BJ,Chernomordik LV,Michael SF,Schieffelin JS,Isern S.Mechanistic study of broadly neutralizing human monoclonal antibodies against dengue virus that target the fusion loop.J Virol. 2013;87:52-66
29. 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. Identification of human neutralizing antibodies that bind to complex epitopes on dengue virions. In: Proceedings of the National Academy of Sciences of the United States of America, 2012;109:7439–44.
30. Covassin L,Jangalwe S,Jouvet N,Laning J,Burzenski L,Shultz LD,Brehm MA.Human immune system development and survival of non-obese diabetic (NOD)-scid IL2rgamma(null) (NSG) mice engrafted with human thymus and autologous haematopoietic stem cells.Clin Experiment Immunol. 2013;174:372-88
31. Traggiai E,Becker S,Subbarao K,Kolesnikova L,Uematsu Y,Gismondo MR,Murphy BR,Rappuoli R,Lanzavecchia A.An efficient method to make human monoclonal antibodies from memory B cells: potent neutralization of SARS coronavirus.Nat Med. 2004;10:871-5
32. Smith K,Garman L,Wrammert J,Zheng NY,Capra JD,Ahmed R,Wilson PC.Rapid generation of fully human monoclonal antibodies specific to a vaccinating antigen.Nat Protocol. 2009;4:372-84
33. Biswas S,Chang H,Sarkis PT,Fikrig E,Zhu Q,Marasco WA.Humoral immune responses in humanized BLT mice immunized with West Nile virus and HIV-1 envelope proteins are largely mediated via human CD5+ B cells.Immunology. 2011;134:419-33
34. Kaveri SV,Silverman GJ,Bayry J.Natural IgM in immune equilibrium and harnessing their therapeutic potential.J Immunol. 2012;188:939-45
35. Sims GP,Ettinger R,Shirota Y,Yarboro CH,Illei GG,Lipsky PE.Identification and characterization of circulating human transitional B cells.Blood. 2005;105:4390-8
36. Friberg H,Jaiswal S,West K,O'Ketch M,Rothman AL,Mathew A.Analysis of human monoclonal antibodies generated by dengue virus-specific memory B cells.Viral Immunol. 2012;25:348-59
37. Robinson JE,Holton D,Liu J,McMurdo H,Murciano A,Gohd R.A novel enzyme-linked immunosorbent assay (ELISA) for the detection of antibodies to HIV-1 envelope glycoproteins based on immobilization of viral glycoproteins in microtiter wells coated with concanavalin A.J Immunol Method. 1990;132:63-71
38. 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;45:3777-80
39. Mathew A,West K,Kalayanarooj S,Gibbons RV,Srikiatkhachorn A,Green S,Libraty D,Jaiswal S,Rothman AL.B-cell responses during primary and secondary dengue virus infections in humans.J Infect Dis. 2011;204:1514-22
40. Brainard DM,Seung E,Frahm N,Cariappa A,Bailey CC,Hart WK,Shin HS,Brooks SF,Knight HL,Eichbaum Q,Yang YG,Sykes M,Walker BD,Freeman GJ,Pillai S,Westmoreland SV,Brander C,Luster AD,Tager AM.Induction of robust cellular and humoral virus-specific adaptive immune responses in human immunodeficiency virus-infected humanized BLT mice.J Virol. 2009;83:7305-21
41. Watanabe Y,Takahashi T,Okajima A,Shiokawa M,Ishii N,Katano I,Ito R,Ito M,Minegishi M,Minegishi N,Tsuchiya S,Sugamura K.The analysis of the functions of human B and T cells in humanized NOD/shi-scid/gammac(null) (NOG) mice (hu-HSC NOG mice).Int Immunol. 2009;21:843-58
42. Calisher CH,Karabatsos N,Dalrymple JM,Shope RE,Porterfield JS,Westaway EG,Brandt WE.Antigenic relationships between flaviviruses as determined by cross-neutralization tests with polyclonal antisera.J Gen Virol. 1989;70:37-43
43. Innis BAntibody responses to dengue virus infection; Dengue and dengue hemorrhagic fever. Gubler DJKuno G, ed. Cambridge, UK: CAB International; 1997:221-43.
44. Lang J,Kelly M,Freed BM,McCarter MD,Kedl RM,Torres RM,Pelanda R.Studies of lymphocyte reconstitution in a humanized mouse model reveal a requirement of T cells for human B cell maturation.J Immunol. 2013;190:2090-101
45. Asito AS,Moormann AM,Kiprotich C,Ng'ang'a ZW,Ploutz-Snyder R,Rochford R.Alterations on peripheral B cell subsets following an acute uncomplicated clinical malaria infection in children.Malaria J. 2008;7:238-238
46. Malaspina A,Moir S,Ho J,Wang W,Howell ML,O'Shea MA,Roby GA,Rehm CA,Mican JM,Chun TW,Fauci AS.Appearance of immature/transitional B cells in HIV-infected individuals with advanced disease: correlation with increased IL-7.Proc Natl Acad Sci USA. 2006;103:2262-7
47. Jones DD,DeIulio GA,Winslow GM.Antigen-driven induction of polyreactive IgM during intracellular bacterial infection.J Immunol. 2012;189:1440-7
48. Vuyyuru R,Liu H,Manser T,Alugupalli KR.Characteristics of Borrelia hermsii infection in human hematopoietic stem cell-engrafted mice mirror those of human relapsing fever.Proc Natl Acad Sci USA. 2012;108:20707-12
49. Shultz LD,Brehm MA,Garcia-Martinez JV,Greiner DL.Humanized mice for immune system investigation: progress, promise and challenges.Nat Rev. 2012;12:786-98