Increased adaptive immune responses and proper feedback regulation protect against clinical dengue

Science Translational Medicine

Volumn 9, Issue 405, 2017, Pages

  Simon Lorière, Etienne ^a,b   Duong, Veasna ^c   Tawfik, Ahmed ^a,b   Ung, Sivlin ^c   Ly, Sowath ^c   Casadémont, Isabelle ^a,b   Prot, Matthieu ^a,b   Courtejoie, Noémie ^a,b   Bleakley, Kevin ^d,e   Buchy, Philippe ^c,f   Tarantola, Arnaud ^c,f   Dussart, Philippe ^c   Cantaert, Tineke ^c   Sakuntabhai, Anavaj ^a,b  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

^c INSTITUT PASTEUR DU CAMBODGE   (Cambodia)

^d INRIA SACLAY   (France)

^e CNRS UMR 8628 Université Paris Sud Bâtiment   (France)

^f GLAXOSMITHKLINE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

FC RECEPTOR IIB; VIRUS ANTIBODY; CYTOKINE;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTATION; ARTICLE; ASYMPTOMATIC INFECTION; B LYMPHOCYTE ACTIVATION; CAMBODIAN; CHILD; CONTROLLED STUDY; DENGUE; DENGUE VIRUS 1; DENGUE VIRUS 2; DENGUE VIRUS 3; DENGUE VIRUS 4; FEEDBACK SYSTEM; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; INFLAMMATION; INNATE IMMUNITY; MAJOR CLINICAL STUDY; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCHOOL CHILD; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; UPREGULATION; VIREMIA; VIRUS LOAD; ACUTE DISEASE; APOPTOSIS; BLOOD; CELL DIFFERENTIATION; DEMOGRAPHY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; PATHOLOGY; PHYSIOLOGICAL FEEDBACK; PLASMA CELL; T LYMPHOCYTE; TREATMENT OUTCOME;

ACUTE DISEASE; ADAPTIVE IMMUNITY; ANTIBODIES, VIRAL; ANTIGEN PRESENTATION; APOPTOSIS; CELL DIFFERENTIATION; CHILD; CYTOKINES; DEMOGRAPHY; DENGUE; FEEDBACK, PHYSIOLOGICAL; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY, INNATE; INFLAMMATION; LYMPHOCYTE ACTIVATION; PLASMA CELLS; T-LYMPHOCYTES; TRANSCRIPTION, GENETIC; TREATMENT OUTCOME; VIRAL LOAD; VIREMIA;

EID: 85028754562     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aal5088     Document Type: Article

References (59)

1. S. Bhatt, P. W. Gething, O. J. Brady, J. P. Messina, A. W. Farlow, C. L. Moyes, J. M. Drake, J. S. Brownstein, A. G. Hoen, O. Sankoh, M. F. Myers, D. B. George, T. Jaenisch, G. R. Wint, C. P. Simmons, T. W. Scott, J. J. Farrar, S. I. Hay, The global distribution and burden of dengue. Nature 496, 504-507 (2013).
2. World Health Organization, Dengue: Guidelines for diagnosis, treatment, prevention and control (World Health Organization, 2009); http://www.who.int/tdr/publications/documents/dengue-diagnosis.pdf.
3. D. S. Shepard, E. A. Undurraga, Y. A. Halasa, J. D. Stanaway, The global economic burden of dengue: A systematic analysis. Lancet Infect. Dis. 16, 935-941 (2016).
4. J. D. Stanaway, D. S. Shepard, E. A. Undurraga, Y. A. Halasa, L. E. Coffeng, O. J. Brady, S. I. Hay, N. Bedi, I. M. Bensenor, C. A. Castañeda-Orjuela, T.-W. Chuang, K. B. Gibney, Z. A. Memish, A. Rafay, K. N. Ukwaja, N. Yonemoto, C. J. L. Murray, The global burden of dengue: An analysis from the Global Burden of Disease Study 2013. Lancet Infect. Dis. 16, 712-723 (2016).
5. L. C. Katzelnick, J. M. Fonville, G. D. Gromowski, J. Bustos Arriaga, A. Green, S. L. James, L. Lau, M. Montoya, C. Wang, L. A. VanBlargan, C. A. Russell, H. M. Thu, T. C. Pierson, P. Buchy, J. G. Aaskov, J. L. Muñoz-Jordán, N. Vasilakis, R. V. Gibbons, R. B. Tesh, A. D. M. E. Osterhaus, R. A. M. Fouchier, A. Durbin, C. P. Simmons, E. C. Holmes, E. Harris, S. S. Whitehead, D. J. Smith, Dengue viruses cluster antigenically but not as discrete serotypes. Science 349, 1338-1343 (2015).
6. C. H. Calisher, N. Karabatsos, J. M. Dalrymple, R. E. Shope, J. S. Porterfield, E. G. Westaway, W. E. Brandt, Antigenic relationships between flaviviruses as determined by crossneutralization tests with polyclonal antisera. J. Gen. Virol. 70, 37-43 (1989).
7. S. B. Halstead, Pathogenesis of dengue: Dawn of a new era. F1000Res. 4, F1000 (2015).
8. B. R. Murphy, S. S. Whitehead, Immune response to dengue virus and prospects for a vaccine. Annu. Rev. Immunol. 29, 587-619 (2011).
9. A. L. Rothman, Immunity to dengue virus: A tale of original antigenic sin and tropical cytokine storms. Nat. Rev. Immunol. 11, 532-543 (2011).
10. L. L. Coffey, E. Mertens, A.-C. Brehin, M. D. Fernandez-Garcia, A. Amara, P. Després, A. Sakuntabhai, Human genetic determinants of dengue virus susceptibility. Microbes Infect. 11, 143-156 (2009).
11. S. B. Halstead, S. Mahalingam, M. A. Marovich, S. Ubol, D. M. Mosser, Intrinsic antibodydependent enhancement of microbial infection in macrophages: Disease regulation by immune complexes. Lancet Infect. Dis. 10, 712-722 (2010).
12. W. Dejnirattisai, A. Jumnainsong, N. Onsirisakul, P. Fitton, S. Vasanawathana, W. Limpitikul, C. Puttikhunt, C. Edwards, T. Duangchinda, S. Supasa, K. Chawansuntati, P. Malasit, J. Mongkolsapaya, G. Screaton, Cross-reacting antibodies enhance dengue virus infection in humans. Science 328, 745-748 (2010).
13. D. Weiskopf, A. Sette, T-cell immunity to infection with dengue virus in humans. Front. Immunol. 5, 93 (2014).
14. R. R. Graham, M. Juffrie, R. Tan, C. G. Hayes, I. Laksono, C. Ma'roef, Erlin, Sutaryo, K. R. Porter, S. B. Halstead, A prospective seroepidemiologic study on dengue in children four to nine years of age in Yogyakarta, Indonesia I. Studies in 1995-1996. Am. J. Trop. Med. Hyg. 61, 412-419 (1999).
15. L. Grange, E. Simon-Loriere, A. Sakuntabhai, L. Gresh, R. Paul, E. Harris, Epidemiological risk factors associated with high global frequency of inapparent dengue virus infections. Front. Immunol. 5, 280 (2014).
16. A. Mathew, A. L. Rothman, Understanding the contribution of cellular immunity to dengue disease pathogenesis. Immunol. Rev. 225, 300-313 (2008).
17. V. Duong, L. Lambrechts, R. E. Paul, S. Ly, R. S. Lay, K. C. Long, R. Huy, A. Tarantola, T. W. Scott, A. Sakuntabhai, P. Buchy, Asymptomatic humans transmit dengue virus to mosquitoes. Proc. Natl. Acad. Sci. U. S. A. 112, 14688-14693 (2015).
18. V. Duong, S. Ly, P. Lorn Try, A. Tuiskunen, S. Ong, N. Chroeung, A. Lundkvist, I. Leparc-Goffart, V. Deubel, S. Vong, P. Buchy, Clinical and virological factors influencing the performance of a NS1 antigen-capture assay and potential use as a marker of dengue disease severity. PLOS Negl. Trop. Dis. 5, e1244 (2011).
19. P. Dussart, L. Baril, L. Petit, L. Beniguel, L. C. Quang, S. Ly, R. d. S. S. Azevedo, J.-B. Meynard, S. Vong, L. Chartier, A. Diop, O. Sivuth, V. Duong, C. M. Thang, M. Jacobs, A. Sakuntabhai, M. R. T. Nunes, V. T. Q. Huong, P. Buchy, P. F. d. C. Vasconcelos, Clinical and virological study of dengue cases and the members of their households: The multinational DENFRAME Project. PLOS Negl. Trop. Dis. 6, e1482 (2012).
20. I.-K. Yoon, A. Getis, J. Aldstadt, A. L. Rothman, D. Tannitisupawong, C. J. M. Koenraadt, T. Fansiri, J. W. Jones, A. C. Morrison, R. G. Jarman, A. Nisalak, M. P. Mammen Jr., S. Thammapalo, A. Srikiatkhachorn, S. Green, D. H. Libraty, R. V. Gibbons, T. Endy, C. Pimgate, T. W. Scott, Fine scale spatiotemporal clustering of dengue virus transmission in children and Aedes aegypti in rural Thai villages. PLOS Negl. Trop. Dis. 6, e1730 (2012).
21. T. P. Endy, S. Chunsuttiwat, A. Nisalak, D. H. Libraty, S. Green, A. L. Rothman, D. W. Vaughn, F. A. Ennis, Epidemiology of inapparent and symptomatic acute dengue virus infection: A prospective study of primary school children in Kamphaeng Phet, Thailand. Am. J. Epidemiol. 156, 40-51 (2002).
22. M. Montoya, L. Gresh, J. C. Mercado, K. L. Williams, M. J. Vargas, G. Gutierrez, G. Kuan, A. Gordon, A. Balmaseda, E. Harris, Symptomatic versus inapparent outcome in repeat dengue virus infections is influenced by the time interval between infections and study year. PLOS Negl. Trop. Dis. 7, e2357 (2013).
23. K. B. Anderson, R. V. Gibbons, D. A. Cummings, A. Nisalak, S. Green, D. H. Libraty, R. G. Jarman, A. Srikiatkhachorn, M. P. Mammen, B. Darunee, I. K. Yoon, T. P. Endy, A shorter time interval between first and second dengue infections is associated with protection from clinical illness in a school-based cohort in Thailand. J. Infect. Dis. 209, 360-368 (2014).
24. World Health Organization, Dengue haemorrhagic fever: Diagnosis, treatment, prevention and control (World Health Organization, 1997); http://www.who.int/csr/resources/publications/dengue/itoviii.pdf.
25. C.-C. Liu, K.-J. Huang, Y.-S. Lin, T.-M. Yeh, H.-S. Liu, H.-Y. Lei, Transient CD4/CD8 ratio inversion and aberrant immune activation during dengue virus infection. J. Med. Virol. 68, 241-252 (2002).
26. E. Eden, R. Navon, I. Steinfeld, D. Lipson, Z. Yakhini, GOrilla: A tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics 10, 48 (2009).
27. Ingenuity Systems, Calculating and interpreting the p-values for functions, pathways and lists in IPA; https://ingenuity.com/wp-content/themes/ingenuity-qiagen/pdf/ipa/functions-pathways-pval-whitepaper.pdf.
28. S. J. Popper, A. Gordon, M. Liu, A. Balmaseda, E. Harris, D. A. Relman, Temporal dynamics of the transcriptional response to dengue virus infection in Nicaraguan children. PLOS Negl. Trop. Dis. 6, e1966 (2012).
29. M. E. Ritchie, B. Phipson, D. Wu, Y. Hu, C. W. Law, W. Shi, G. K. Smyth, limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 43, e47 (2015).
30. M. R. Müller, A. Rao, NFAT, immunity and cancer: A transcription factor comes of age. Nat. Rev. Immunol. 10, 645-656 (2010).
31. J. M. Slavik, J. E. Hutchcroft, B. E. Bierer, CD80 and CD86 are not equivalent in their ability to induce the tyrosine phosphorylation of CD28. J. Biol. Chem. 274, 3116-3124 (1999).
32. Y. Zheng, C. N. Manzotti, M. Liu, F. Burke, K. I. Mead, D. M. Sansom, CD86 and CD80 differentially modulate the suppressive function of human regulatory T cells. J. Immunol. 172, 2778-2784 (2004).
33. J. Mongkolsapaya, W. Dejnirattisai, X.-n. Xu, S. Vasanawathana, N. Tangthawornchaikul, A. Chairunsri, S. Sawasdivorn, T. Duangchinda, T. Dong, S. Rowland-Jones, P.-t. Yenchitsomanus, A. McMichael, P. Malasit, G. Screaton, Original antigenic sin and apoptosis in the pathogenesis of dengue hemorrhagic fever. Nat. Med. 9, 921-927 (2003).
34. F. J. Li, W. J. Won, E. J. Becker Jr., J. L. Easlick, E. M. Tabengwa, R. Li, M. Shakhmatov, K. Honjo, P. D. Burrows, R. S. Davis, Emerging roles for the FCRL family members in lymphocyte biology and disease. Curr. Top. Microbiol. Immunol. 382, 29-50 (2014).
35. D. Weiskopf, D. J. Bangs, J. Sidney, R. V. Kolla, A. D. De Silva, A. M. de Silva, S. Crotty, B. Peters, A. Sette, Dengue virus infection elicits highly polarized CX3CR1+ cytotoxic CD4+ T cells associated with protective immunity. Proc. Natl. Acad. Sci. U. S. A. 112, E4256-E4263 (2015).
36. L. E. Yauch, R. M. Zellweger, M. F. Kotturi, A. Qutubuddin, J. Sidney, B. Peters, T. R. Prestwood, A. Sette, S. Shresta, A protective role for dengue virus-specific CD8+ T cells. J. Immunol. 182, 4865-4873 (2009).
37. A. Elong Ngono, H. W. Chen, W. W. Tang, Y. Joo, K. King, D. Weiskopf, J. Sidney, A. Sette, S. Shresta, Protective role of cross-reactive CD8 T cells against dengue virus infection. EBioMedicine 284-293 (2016).
38. D. Weiskopf, M. A. Angelo, E. L. de Azeredo, J. Sidney, J. A. Greenbaum, A. N. Fernando, A. Broadwater, R. V. Kolla, A. D. De Silva, A. M. de Silva, K. A. Mattia, B. J. Doranz, H. M. Grey, S. Shresta, B. Peters, A. Sette, Comprehensive analysis of dengue virus-specific responses supports an HLA-linked protective role for CD8+ T cells. Proc. Natl. Acad. Sci. U. S. A. 110, E2046-E2053 (2013).
39. D. Weiskopf, M. A. Angelo, A. Grifoni, P. H. O'Rourke, J. Sidney, S. Paul, A. D. De Silva, E. Phillips, S. Mallal, S. Premawansa, G. Premawansa, A. Wijewickrama, B. Peters, A. Sette, HLA-DRB1 alleles are associated with different magnitudes of dengue virus-specific CD4+ T-cell responses. J. Infect. Dis. 214, 1117-1124 (2016).
40. S. Hatch, T. P. Endy, S. Thomas, A. Mathew, J. Potts, P. Pazoles, D. H. Libraty, R. Gibbons, A. L. Rothman, Intracellular cytokine production by dengue virus-specific T cells correlates with subclinical secondary infection. J. Infect. Dis. 203, 1282-1291 (2011).
41. P. G. Livingston, I. Kurane, L. C. Dai, Y. Okamoto, C. J. Lai, R. Men, S. Karaki, M. Takiguchi, F. A. Ennis, Dengue virus-specific, HLA-B35-restricted, human CD8+ cytotoxic T lymphocyte (CTL) clones. Recognition of NS3 amino acids 500 to 508 by CTL clones of two different serotype specificities. J. Immunol. 154, 1287-1295 (1995).
42. I. Kurane, L. Zeng, M. A. Brinton, F. A. Ennis, Definition of an epitope on NS3 recognized by human CD4+ cytotoxic T lymphocyte clones cross-reactive for dengue virus types 2, 3, and 4. Virology 240, 169-174 (1998).
43. T. Duangchinda, W. Dejnirattisai, S. Vasanawathana, W. Limpitikul, N. Tangthawornchaikul, P. Malasit, J. Mongkolsapaya, G. Screaton, Immunodominant T-cell responses to dengue virus NS3 are associated with DHF. Proc. Natl. Acad. Sci. U. S. A. 107, 16922-16927 (2010).
44. L. Rivino, A. T. Tan, A. Chia, E. A. Kumaran, G. M. Grotenbreg, P. A. MacAry, A. Bertoletti, Defining CD8+ T cell determinants during human viral infection in populations of Asian ethnicity. J. Immunol. 191, 4010-4019 (2013).
45. S. R. Hadinegoro, J. L. Arredondo-García, M. R. Capeding, C. Deseda, T. Chotpitayasunondh, R. Dietze, H. I. Muhammad Ismail, H. Reynales, K. Limkittikul, D. M. Rivera-Medina, H. N. Tran, A. Bouckenooghe, D. Chansinghakul, M. Cortes, K. Fanouillere, R. Forrat, C. Frago, S. Gailhardou, N. Jackson, F. Noriega, E. Plennevaux, T. A. Wartel, B. Zambrano, M. Saville; CYD-TDV Dengue Vaccine Working Group, Efficacy and long-term safety of a dengue vaccine in regions of endemic disease. N. Engl. J. Med. 373, 1195-1206 (2015).
46. M. R. Capeding, N. H. Tran, S. R. S. Hadinegoro, H. I. H. J. M. Ismail, T. Chotpitayasunondh, M. N. Chua, C. Q. Luong, K. Rusmi, D. N. Wirawan, R. Nallusamy, P. Pitisuttithum, U. Thisyakorn, I. K. Yoon, D. van der Vliet, E. Langevin, T. Laot, Y. Hutagalung, C. Frago, M. Boaz, T. A. Wartel, N. G. Tornieporth, M. Saville, A. Bouckenooghe; CYD14 Study Group, Clinical efficacy and safety of a novel tetravalent dengue vaccine in healthy children in Asia: A phase 3, randomised, observer-masked, placebo-controlled trial. Lancet 384, 1358-1365 (2014).
47. L. Villar, G. H. Dayan, J. L. Arredondo-García, D. M. Rivera, R. Cunha, C. Deseda, H. Reynales, M. S. Costa, J. O. Morales-Ramírez, G. Carrasquilla, L. C. Rey, R. Dietze, K. Luz, E. Rivas, M. C. Miranda Montoya, M. Cortés Supelano, B. Zambrano, E. Langevin, M. Boaz, N. Tornieporth, M. Saville, F. Noriega; CYD15 Study Group, Efficacy of a tetravalent dengue vaccine in children in Latin America. N. Engl. J. Med. 372, 113-123 (2015).
48. T. Balakrishnan, D. B. Bela-Ong, Y. X. Toh, M. Flamand, S. Devi, M. B. Koh, M. L. Hibberd, E. E. Ooi, J. G. Low, Y. S. Leo, F. Gu, K. Fink, Dengue virus activates polyreactive, natural IgG B cells after primary and secondary infection. PLOS ONE 6, e29430 (2011).
49. T. M. Garcia-Bates, M. T. Cordeiro, E. J. M. Nascimento, A. P. Smith, K. M. Soares de Melo, S. P. McBurney, J. D. Evans, E. T. A. Marques Jr., S. M. Barratt-Boyes, Association between magnitude of the virus-specific plasmablast response and disease severity in dengue patients. J. Immunol. 190, 80-87 (2013).
50. J. Wrammert, N. Onlamoon, R. S. Akondy, G. C. Perng, K. Polsrila, A. Chandele, M. Kwissa, B. Pulendran, P. C. Wilson, O. Wittawatmongkol, S. Yoksan, N. Angkasekwinai, K. Pattanapanyasat, K. Chokephaibulkit, R. Ahmed, Rapid and massive virus-specific plasmablast responses during acute dengue virus infection in humans. J. Virol. 86, 2911-2918 (2012).
51. M. Kwissa, H. I. Nakaya, N. Onlamoon, J. Wrammert, F. Villinger, G. C. Perng, S. Yoksan, K. Pattanapanyasat, K. Chokephaibulkit, R. Ahmed, B. Pulendran, Dengue virus infection induces expansion of a CD14+CD16+ monocyte population that stimulates plasmablast differentiation. Cell Host Microbe 16, 115-127 (2014).
52. A. R. Brasier, H. Ju, J. Garcia, H. M. Spratt, S. S. Victor, B. M. Forshey, E. S. Halsey, G. Comach, G. Sierra, P. J. Blair, C. Rocha, A. C. Morrison, T. W. Scott, I. Bazan, T. J. Kochel; Venezuelan Dengue Fever Working Group, A three-component biomarker panel for prediction of dengue hemorrhagic fever. Am. J. Trop. Med. Hyg. 86, 341-348 (2012).
53. R. Appanna, S. Kg, M. H. Xu, Y. X. Toh, S. Velumani, D. Carbajo, C. Y. Lee, R. Zuest, T. Balakrishnan, W. Xu, B. Lee, M. Poidinger, F. Zolezzi, Y. S. Leo, T. L. Thein, C. I. Wang, K. Fink, Plasmablasts during acute dengue infection represent a small subset of a broader virus-specific memory B cell pool. EBioMedicine 12, 178-188 (2016).
54. W. Dejnirattisai, W. Wongwiwat, S. Supasa, X. Zhang, X. Dai, A. Rouvinski, A. Jumnainsong, C. Edwards, N. T. Quyen, T. Duangchinda, J. M. Grimes, W.-Y. Tsai, C.-Y. Lai, W.-K. Wang, P. Malasit, J. Farrar, C. P. Simmons, Z. H. Zhou, F. A. Rey, J. Mongkolsapaya, G. R. Screaton, A new class of highly potent, broadly neutralizing antibodies isolated from viremic patients infected with dengue virus. Nat. Immunol. 16, 170-177 (2015).
55. L. Priyamvada, A. Cho, N. Onlamoon, N. Y. Zheng, M. Huang, Y. Kovalenkov, K. Chokephaibulkit, N. Angkasekwinai, K. Pattanapanyasat, R. Ahmed, P. C. Wilson, J. Wrammert, B cell responses during secondary dengue virus infection are dominated by highly cross-reactive, memory-derived plasmablasts. J. Virol. 90, 5574-5585 (2016).
56. A. S. L. Yeo, A. Rathakrishnan, S. M. Wang, S. Ponnampalavanar, R. Manikam, J. Sathar, S. Kumari Natkunam, S. D. Sekaran, Dengue patients exhibit higher levels of PrM and E antibodies than their asymptomatic counterparts. Biomed. Res. Int. 2015, 420867 (2015).
57. A. S. L. Yeo, N. A. Azhar, W. Yeow, C. C. Talbot Jr., M. A. Khan, E. M. Shankar, A. Rathakrishnan, A. Azizan, S. M. Wang, S. K. Lee, M. Y. Fong, R. Manikam, S. Devi Sekaran, Lack of clinical manifestations in asymptomatic dengue infection is attributed to broad down-regulation and selective up-regulation of host defence response genes. PLOS ONE 9, e92240 (2014).
58. K. D. Hue, T. V. Tuan, H. T. Thi, C. T. Bich, H. H. Anh, B. A. Wills, C. P. Simmons, Validation of an internally controlled one-step real-time multiplex RT-PCR assay for the detection and quantitation of dengue virus RNA in plasma. J. Virol. Methods 177, 168-173 (2011).
59. R. S. G. Sealfon, M. A. Hibbs, C. Huttenhower, C. L. Myers, O. G. Troyanskaya, GOLEM: An interactive graph-based gene-ontology navigation and analysis tool. BMC Bioinformatics 7, 443 (2006).