Sequential Waves of Gene Expression in Patients with Clinically Defined Dengue Illnesses Reveal Subtle Disease Phases and Predict Disease Severity

PLoS Neglected Tropical Diseases

Volumn 7, Issue 7, 2013, Pages

  Sun, Peifang ^a,b   García, Josefina ^c   Comach, Guillermo ^d   Vahey, Maryanne T ^e   Wang, Zhining ^b   Forshey, Brett M ^c   Morrison, Amy C ^c,f   Sierra, Gloria ^d   Bazan, Isabel ^c   Rocha, Claudio ^c   Vilcarromero, Stalin ^c   Blair, Patrick J ^g   Scott, Thomas W ^f   Camacho, Daria E ^d   Ockenhouse, Christian F ^e   Halsey, Eric S ^c   Kochel, Tadeusz J ^a  

^a NAVAL MEDICAL RESEARCH CENTER   (United States)

^b HENRY M JACKSON FOUNDATION FOR THE ADVANCEMENT OF MILITARY MEDICINE   (United States)

^c California   (Peru)

^d Instituto de Investigaciones Biomedicas   (Venezuela)

^e WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g American Embassy Singapore   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN M; INTERFERON; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2;

ADAPTIVE IMMUNITY; ADULT; ANTIGEN PRESENTATION; ARTICLE; BLOOD SAMPLING; CHEMOTAXIS; CHILD; DENGUE; DIAGNOSTIC ACCURACY; DISEASE SEVERITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE EXPRESSION; GENE IDENTIFICATION; HEMORRHAGIC FEVER; HUMAN; HUMAN CELL; INNATE IMMUNITY; MAJOR CLINICAL STUDY; MALE; MONITORING; NATURAL KILLER CELL; PREDICTIVE VALUE; PRESCHOOL CHILD; REAL TIME POLYMERASE CHAIN REACTION; SCHOOL CHILD; T LYMPHOCYTE; VIRUS REPLICATION;

EID: 84880769645     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0002298     Document Type: Article

References (48)

1. Mathew A, Rothman AL, (2008) Understanding the contribution of cellular immunity to dengue disease pathogenesis. Immunol Rev 225: 300-313.
2. Brady OJ, Gething PW, Bhatt S, Messina JP, Brownstein JS, et al. (2012) Refining the global spatial limits of dengue virus transmission by evidence-based consensus. PLoS Negl Trop Dis 6: e1760.
3. Nishiura H, Halstead SB, (2007) Natural history of dengue virus (DENV)-1 and DENV-4 infections: reanalysis of classic studies. J Infect Dis 195: 1007-1013.
4. Halstead SB, (1988) Pathogenesis of dengue: challenges to molecular biology. Science 239: 476-481.
5. Gubler DJ, (1989) Surveillance for dengue and dengue hemorrhagic fever. Bull Pan Am Health Organ 23: 397-404.
6. Srikiatkhachorn A, (2009) Plasma leakage in dengue haemorrhagic fever. Thromb Haemost 102: 1042-1049.
7. Srikiatkhachorn A, Krautrachue A, Ratanaprakarn W, Wongtapradit L, Nithipanya N, et al. (2007) Natural history of plasma leakage in dengue hemorrhagic fever: a serial ultrasonographic study. Pediatr Infect Dis J 26: 283-290; discussion 291-282.
8. Libraty DH, Endy TP, Houng HS, Green S, Kalayanarooj S, et al. (2002) Differing influences of virus burden and immune activation on disease severity in secondary dengue-3 virus infections. J Infect Dis 185: 1213-1221.
9. Vaughn DW, Green S, Kalayanarooj S, Innis BL, Nimmannitya S, et al. (2000) Dengue viremia titer, antibody response pattern, and virus serotype correlate with disease severity. J Infect Dis 181: 2-9.
10. Green S, Rothman A, (2006) Immunopathological mechanisms in dengue and dengue hemorrhagic fever. Curr Opin Infect Dis 19: 429-436.
11. Fink J, Gu F, Ling L, Tolfvenstam T, Olfat F, et al. (2007) Host gene expression profiling of dengue virus infection in cell lines and patients. PLoS Negl Trop Dis 1: e86.
12. Simmons CP, Popper S, Dolocek C, Chau TN, Griffiths M, et al. (2007) Patterns of host genome-wide gene transcript abundance in the peripheral blood of patients with acute dengue hemorrhagic fever. J Infect Dis 195: 1097-1107.
13. Loke P, Hammond SN, Leung JM, Kim CC, Batra S, et al. (2010) Gene expression patterns of dengue virus-infected children from nicaragua reveal a distinct signature of increased metabolism. PLoS Negl Trop Dis 4: e710.
14. Ubol S, Masrinoul P, Chaijaruwanich J, Kalayanarooj S, Charoensirisuthikul T, et al. (2008) Differences in global gene expression in peripheral blood mononuclear cells indicate a significant role of the innate responses in progression of dengue fever but not dengue hemorrhagic fever. J Infect Dis 197: 1459-1467.
15. Innis BL, Nisalak A, Nimmannitya S, Kusalerdchariya S, Chongswasdi V, et al. (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.
16. Morrison AC, Minnick SL, Rocha C, Forshey BM, Stoddard ST, et al. (2010) Epidemiology of dengue virus in Iquitos, Peru 1999 to 2005: interepidemic and epidemic patterns of transmission. PLoS Negl Trop Dis 4: e670.
17. Morens DM, (1994) Antibody-dependent enhancement of infection and the pathogenesis of viral disease. Clin Infect Dis 19: 500-512.
18. Comach G, Blair PJ, Sierra G, Guzman D, Soler M, et al. (2008) Dengue Virus Infections in a Cohort of Schoolchildren from Maracay, Venezuela: A 2-Year Prospective Study. Vector Borne Zoonotic Dis 9: 87-92.
19. Johnson BW, Russell BJ, Lanciotti RS, (2005) Serotype-specific detection of dengue viruses in a fourplex real-time reverse transcriptase PCR assay. J Clin Microbiol 43: 4977-4983.
20. Vahey MT, Nau ME, Taubman M, Yalley-Ogunro J, Silvera P, et al. (2003) Patterns of gene expression in peripheral blood mononuclear cells of rhesus macaques infected with SIVmac251 and exhibiting differential rates of disease progression. AIDS Res Hum Retroviruses 19: 369-387.
21. Vahey MT, Wang Z, Kester KE, Cummings J, Heppner DG Jr, et al. (2010) Expression of genes associated with immunoproteasome processing of major histocompatibility complex peptides is indicative of protection with adjuvanted RTS,S malaria vaccine. J Infect Dis 201: 580-589.
22. Li C, Wong WH, (2001) Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc Natl Acad Sci U S A 98: 31-36.
23. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, et al. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25: 25-29.
24. Kanehisa M, Goto S, (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28: 27-30.
25. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, et al. (2003) DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 4: P3.
26. Vaughn DW, Green S, Kalayanarooj S, Innis BL, Nimmannitya S, et al. (1997) Dengue in the early febrile phase: viremia and antibody responses. J Infect Dis 176: 322-330.
27. Moi ML, Lim CK, Kotaki A, Takasaki T, Kurane I, (2011) Detection of higher levels of dengue viremia using FcgammaR-expressing BHK-21 cells than FcgammaR-negative cells in secondary infection but not in primary infection. J Infect Dis 203: 1405-1414.
28. Potts JA, Gibbons RV, Rothman AL, Srikiatkhachorn A, Thomas SJ, et al. (2010) Prediction of dengue disease severity among pediatric Thai patients using early clinical laboratory indicators. PLoS Negl Trop Dis 4: e769.
29. Green S, Pichyangkul S, Vaughn DW, Kalayanarooj S, Nimmannitya S, et al. (1999) Early CD69 expression on peripheral blood lymphocytes from children with dengue hemorrhagic fever. J Infect Dis 180: 1429-1435.
30. Myint KS, Endy TP, Mongkolsirichaikul D, Manomuth C, Kalayanarooj S, et al. (2006) Cellular immune activation in children with acute dengue virus infections is modulated by apoptosis. J Infect Dis 194: 600-607.
31. 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.
32. Mathew A, Kurane I, Green S, Vaughn DW, Kalayanarooj S, et al. (1999) Impaired T cell proliferation in acute dengue infection. J Immunol 162: 5609-5615.
33. Downey GP, (1994) Mechanisms of leukocyte motility and chemotaxis. Curr Opin Immunol 6: 113-124.
34. Cassatella MA, (1999) Neutrophil-derived proteins: selling cytokines by the pound. Adv Immunol 73: 369-509.
35. Scapini P, Laudanna C, Pinardi C, Allavena P, Mantovani A, et al. (2001) Neutrophils produce biologically active macrophage inflammatory protein-3alpha (MIP-3alpha)/CCL20 and MIP-3beta/CCL19. Eur J Immunol 31: 1981-1988.
36. Long HT, Hibberd ML, Hien TT, Dung NM, Van Ngoc T, et al. (2009) Patterns of gene transcript abundance in the blood of children with severe or uncomplicated dengue highlight differences in disease evolution and host response to dengue virus infection. J Infect Dis 199: 537-546.
37. Popper SJ, Gordon A, Liu M, Balmaseda A, Harris E, et al. (2012) Temporal dynamics of the transcriptional response to dengue virus infection in Nicaraguan children. PLoS Negl Trop Dis 6: e1966.
38. Avirutnan P, Malasit P, Seliger B, Bhakdi S, Husmann M, (1998) Dengue virus infection of human endothelial cells leads to chemokine production, complement activation, and apoptosis. J Immunol 161: 6338-6346.
39. Bosch I, Xhaja K, Estevez L, Raines G, Melichar H, et al. (2002) Increased production of interleukin-8 in primary human monocytes and in human epithelial and endothelial cell lines after dengue virus challenge. J Virol 76: 5588-5597.
40. Hober D, Poli L, Roblin B, Gestas P, Chungue E, et al. (1993) Serum levels of tumor necrosis factor-alpha (TNF-alpha), interleukin-6 (IL-6), and interleukin-1 beta (IL-1 beta) in dengue-infected patients. Am J Trop Med Hyg 48: 324-331.
41. Kurane I, Brinton MA, Samson AL, Ennis FA, (1991) Dengue virus-specific, human CD4+ CD8- cytotoxic T-cell clones: multiple patterns of virus cross-reactivity recognized by NS3-specific T-cell clones. J Virol 65: 1823-1828.
42. Suharti C, van Gorp EC, Dolmans WM, Setiati TE, Hack CE, et al. (2003) Cytokine patterns during dengue shock syndrome. Eur Cytokine Netw 14: 172-177.
43. Yen YT, Chen HC, Lin YD, Shieh CC, Wu-Hsieh BA, (2008) Enhancement by tumor necrosis factor alpha of dengue virus-induced endothelial cell production of reactive nitrogen and oxygen species is key to hemorrhage development. J Virol 82: 12312-12324.
44. Brasier AR, Garcia J, Wiktorowicz JE, Spratt HM, Comach G, et al. (2012) Discovery proteomics and nonparametric modeling pipeline in the development of a candidate biomarker panel for dengue hemorrhagic fever. Clin Transl Sci 5: 8-20.
45. Mehlhop E, Ansarah-Sobrinho C, Johnson S, Engle M, Fremont DH, et al. (2007) Complement protein C1q inhibits antibody-dependent enhancement of flavivirus infection in an IgG subclass-specific manner. Cell Host Microbe 2: 417-426.
46. Malasit P, (1987) Complement and dengue haemorrhagic fever/shock syndrome. Southeast Asian J Trop Med Public Health 18: 316-320.
47. Nascimento EJ, Braga-Neto U, Calzavara-Silva CE, Gomes AL, Abath FG, et al. (2009) Gene expression profiling during early acute febrile stage of dengue infection can predict the disease outcome. PLoS One 4: e7892.
48. Devignot S, Sapet C, Duong V, Bergon A, Rihet P, et al. (2010) Genome-wide expression profiling deciphers host responses altered during dengue shock syndrome and reveals the role of innate immunity in severe dengue. PLoS One 5: e11671.