Dengue virus activates polyreactive, natural IgG B cells after primary and secondary infection

PLoS ONE

Volumn 6, Issue 12, 2011, Pages

  Balakrishnan, Thavamalar ^a   Bela Ong, Dennis B ^b   Toh, Ying Xiu ^a   Flamand, Marie ^c   Devi, Shamala ^d   Koh, Mickey B ^e,i   Hibberd, Martin L ^f   Ooi, Eng Eong ^g   Low, Jenny G ^h   Leo, Yee Sin ^h   Gu, Feng ^b   Fink, Katja ^a  

^a AGENCY FOR SCIENCE   (Singapore)

^b NOVARTIS INSTITUTE FOR TROPICAL DISEASES   (Singapore)

^c INSTITUT PASTEUR   (France)

^d UNIVERSITY OF MALAYA   (Malaysia)

^e SINGAPORE GENERAL HOSPITAL   (Singapore)

^f GENOME INSTITUTE OF SINGAPORE   (Singapore)

^g DUKE NUS MEDICAL SCHOOL   (Singapore)

^h TAN TOCK SENG HOSPITAL   (Singapore)

ⁱ ST GEORGE S HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN G; NEUTRALIZING ANTIBODY; POLYCLONAL ANTIBODY; VIRUS ANTIBODY;

ACUTE DISEASE; ADAPTIVE IMMUNITY; ADULT; ANTIBODY PRODUCTION; ANTIBODY SPECIFICITY; ANTIBODY TITER; ARTICLE; B LYMPHOCYTE ACTIVATION; BLOOD ANALYSIS; BLOOD SAMPLING; CELL MATURATION; CLINICAL ARTICLE; CONTROLLED STUDY; CONVALESCENCE; CROSS REACTION; DENGUE; DENGUE VIRUS; DISEASE COURSE; FEMALE; FEVER; HUMAN; HUMAN CELL; HUMORAL IMMUNITY; INNATE IMMUNITY; MALE; NONHUMAN; PLASMA CELL; PRIMARY INFECTION; PROSPECTIVE STUDY; SECONDARY INFECTION; SEROTYPE; VIRUS CELL INTERACTION; B LYMPHOCYTE; IMMUNOLOGY; PHYSIOLOGY;

B-LYMPHOCYTES; CROSS REACTIONS; DENGUE; DENGUE VIRUS; HUMANS; IMMUNOGLOBULIN G;

EID: 84055207530     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0029430     Document Type: Article

References (47)

1. Hammond SN, Balmaseda A, Perez L, Tellez Y, Saborio SI, et al. (2005) Differences in dengue severity in infants, children, and adults in a 3-year hospital-based study in Nicaragua. Am J Trop Med Hyg 73: 1063-1070.
2. Mongkolsapaya J, Dejnirattisai W, Xu XN, Vasanawathana S, Tangthawornchaikul N, et al. (2003) Original antigenic sin and apoptosis in the pathogenesis of dengue hemorrhagic fever. Nat Med 9: 921-927.
3. 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.
4. Halstead SB, (1970) Observations related to pathogensis of dengue hemorrhagic fever. VI. Hypotheses and discussion. Yale J Biol Med 42: 350-362.
5. Woods A, Monneaux F, Soulas-Sprauel P, Muller S, Martin T, et al. (2007) Influenza virus-induced type I interferon leads to polyclonal B-cell activation but does not break down B-cell tolerance. J Virol 81: 12525-12534.
6. De Vita S, Quartuccio L, Fabris M, (2008) Hepatitis C virus infection, mixed cryoglobulinemia and BLyS upregulation: targeting the infectious trigger, the autoimmune response, or both? Autoimmun Rev 8: 95-99.
7. Moir S, Fauci AS, (2009) B cells in HIV infection and disease. Nat Rev Immunol 9: 235-245.
8. Donati D, Zhang LP, Chene A, Chen Q, Flick K, et al. (2004) Identification of a polyclonal B-cell activator in Plasmodium falciparum. Infect Immun 72: 5412-5418.
9. Mei HE, Yoshida T, Sime W, Hiepe F, Thiele K, et al. (2009) Blood-borne human plasma cells in steady state are derived from mucosal immune responses. Blood 113: 2461-2469.
10. Odendahl M, Mei H, Hoyer BF, Jacobi AM, Hansen A, et al. (2005) Generation of migratory antigen-specific plasma blasts and mobilization of resident plasma cells in a secondary immune response. Blood 105: 1614-1621.
11. Sabin AB, (1952) Research on dengue during World War II. Am J Trop Med Hyg 1: 30-50.
12. Mei HE, Yoshida T, Muehlinghaus G, Hiepe F, Dorner T, et al. (2007) Phenotypic analysis of B-cells and plasma cells. Methods Mol Med 136: 3-18.
13. Low JG, Ooi EE, Tolfvenstam T, Leo YS, Hibberd ML, et al. (2006) Early Dengue infection and outcome study (EDEN)- study design and preliminary findings. Ann Acad Med Singapore 35: 783-789.
14. Bossen C, Cachero TG, Tardivel A, Ingold K, Willen L, et al. (2008) TACI, unlike BAFF-R, is solely activated by oligomeric BAFF and APRIL to support survival of activated B cells and plasmablasts. Blood 111: 1004-1012.
15. Green S, Vaughn DW, Kalayanarooj S, Nimmannitya S, Suntayakorn S, et al. (1999) Elevated plasma interleukin-10 levels in acute dengue correlate with disease severity. J Med Virol 59: 329-334.
16. Mackay F, Browning JL, (2002) BAFF: a fundamental survival factor for B cells. Nat Rev Immunol 2: 465-475.
17. Nardelli B, Belvedere O, Roschke V, Moore PA, Olsen HS, et al. (2001) Synthesis and release of B-lymphocyte stimulator from myeloid cells. Blood 97: 198-204.
18. Marovich M, Grouard-Vogel G, Louder M, Eller M, Sun W, et al. (2001) Human dendritic cells as targets of dengue virus infection. J Investig Dermatol Symp Proc 6: 219-224.
19. Wu SJ, Grouard-Vogel G, Sun W, Mascola JR, Brachtel E, et al. (2000) Human skin Langerhans cells are targets of dengue virus infection. Nat Med 6: 816-820.
20. Yoksan S, Tubthong K, Kanitwithayanun W, Jirakanjanakit N, (2009) Laboratory assays and field dengue vaccine evaluation at Ratchaburi province, Thailand: a preliminary result. J Clin Virol 46 (Suppl 2): S13-15.
21. Lane HC, Masur H, Edgar LC, Whalen G, Rook AH, et al. (1983) Abnormalities of B-cell activation and immunoregulation in patients with the acquired immunodeficiency syndrome. N Engl J Med 309: 453-458.
22. Bernasconi NL, Traggiai E, Lanzavecchia A, (2002) Maintenance of serological memory by polyclonal activation of human memory B cells. Science 298: 2199-2202.
23. Lacroix-Desmazes S, Kaveri SV, Mouthon L, Ayouba A, Malanchere E, et al. (1998) Self-reactive antibodies (natural autoantibodies) in healthy individuals. J Immunol Methods 216: 117-137.
24. Ochsenbein AF, Fehr T, Lutz C, Suter M, Brombacher F, et al. (1999) Control of early viral and bacterial distribution and disease by natural antibodies. Science 286: 2156-2159.
25. 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.
26. Chau TN, Hieu NT, Anders KL, Wolbers M, Lien le B, et al. (2009) Dengue virus infections and maternal antibody decay in a prospective birth cohort study of Vietnamese infants. J Infect Dis 200: 1893-1900.
27. Hubert B, Halstead SB, (2009) Dengue 1 virus and dengue hemorrhagic fever, French Polynesia, 2001. Emerg Infect Dis 15: 1265-1270.
28. Stoiber H, (2009) Complement, Fc receptors and antibodies: a Trojan horse in HIV infection? Curr Opin HIV AIDS 4: 394-399.
29. Tamura M, Webster RG, Ennis FA, (1994) Subtype cross-reactive, infection-enhancing antibody responses to influenza A viruses. J Virol 68: 3499-3504.
30. Beltramello M, Williams KL, Simmons CP, Macagno A, Simonelli L, et al. (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.
31. Halstead SB, O'Rourke EJ, (1977) Dengue viruses and mononuclear phagocytes. I. Infection enhancement by non-neutralizing antibody. J Exp Med 146: 201-217.
32. Dejnirattisai W, Jumnainsong A, Onsirisakul N, Fitton P, Vasanawathana S, et al. (2010) Cross-reacting antibodies enhance dengue virus infection in humans. Science 328: 745-748.
33. Schieffelin JS, Costin JM, Nicholson CO, Orgeron NM, Fontaine KA, et al. (2010) Neutralizing and non-neutralizing monoclonal antibodies against dengue virus E protein derived from a naturally infected patient. Virol J 7: 28.
34. de Alwis R, Beltramello M, Messer WB, Sukupolvi-Petty S, Wahala WM, et al. (2011) In-depth analysis of the antibody response of individuals exposed to primary dengue virus infection. PLoS Negl Trop Dis 5: e1188.
35. Mathew A, West K, Kalayanarooj S, Gibbons RV, Srikiatkhachorn A, et al. (2011) B-cell responses during primary and secondary dengue virus infections in humans. J Infect Dis 204: 1514-1522.
36. Baumgarth N, Tung JW, Herzenberg LA, (2005) Inherent specificities in natural antibodies: a key to immune defense against pathogen invasion. Springer Semin Immunopathol 26: 347-362.
37. Lutz HU, Binder CJ, Kaveri S, (2009) Naturally occurring auto-antibodies in homeostasis and disease. Trends Immunol 30: 43-51.
38. Recher M, Lang KS, Hunziker L, Freigang S, Eschli B, et al. (2004) Deliberate removal of T cell help improves virus-neutralizing antibody production. Nat Immunol 5: 934-942.
39. Gorelik L, Gilbride K, Dobles M, Kalled SL, Zandman D, et al. (2003) Normal B cell homeostasis requires B cell activation factor production by radiation-resistant cells. J Exp Med 198: 937-945.
40. Bombardieri M, Kam NW, Brentano F, Choi K, Filer A, et al. (2011) A BAFF/APRIL-dependent TLR3-stimulated pathway enhances the capacity of rheumatoid synovial fibroblasts to induce AID expression and Ig class-switching in B cells. Ann Rheum Dis 70: 1857-1865.
41. Ittah M, Miceli-Richard C, Gottenberg JE, Sellam J, Lepajolec C, et al. (2009) B-cell-activating factor expressions in salivary epithelial cells after dsRNA virus infection depends on RNA-activated protein kinase activation. Eur J Immunol 39: 1271-1279.
42. Lee FE, Halliley JL, Walsh EE, Moscatiello AP, Kmush BL, et al. (2011) Circulating human antibody-secreting cells during vaccinations and respiratory viral infections are characterized by high specificity and lack of bystander effect. J Immunol 186: 5514-5521.
43. Meffre E, Wardemann H, (2008) B-cell tolerance checkpoints in health and autoimmunity. Curr Opin Immunol 20: 632-638.
44. Lin CF, Lei HY, Shiau AL, Liu CC, Liu HS, et al. (2003) Antibodies from dengue patient sera cross-react with endothelial cells and induce damage. J Med Virol 69: 82-90.
45. McBride W, Vasudevan S, (1995) Relationship of a dengue 2 isolate from Townsville,1993, to international isolates. Comm Dis Intelligence 19: 522-523.
46. Kraus AA, Messer W, Haymore LB, de Silva AM, (2007) Comparison of plaque- and flow cytometry-based methods for measuring dengue virus neutralization. J Clin Microbiol 45: 3777-3780.
47. Falconar AK, Young PR, (1990) Immunoaffinity purification of native dimer forms of the flavivirus non-structural glycoprotein, NS1. J Virol Methods 30: 323-332.