Neuroinvasive West Nile Infection Elicits Elevated and Atypically Polarized T Cell Responses That Promote a Pathogenic Outcome

PLoS Pathogens

Volumn 12, Issue 1, 2016, Pages

  James, Eddie A ^a   Gates, Theresa J ^a   LaFond, Rebecca E ^a   Yamamoto, Shinobu ^a   Ni, Chester ^a   Mai, Duy ^a   Gersuk, Vivian H ^a   O’Brien, Kimberly ^a   Nguyen, Quynh Anh ^a   Zeitner, Brad ^a   Lanteri, Marion C ^b   Norris, Philip J ^b,c   Chaussabel, Damien ^a   Malhotra, Uma ^d,e   Kwok, William W ^a,e  

^a BENAROYA RESEARCH INSTITUTE   (United States)

^b BLOOD SYSTEMS RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d VIRGINIA MASON MEDICAL CENTER   (United States)

^e UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; GAMMA INTERFERON; INTERLEUKIN 4;

ADULT; AGED; ARTICLE; CLINICAL ARTICLE; EPITOPE MAPPING; FEMALE; HLA TYPING; HUMAN; IMMUNE RESPONSE; MALE; MIDDLE AGED; PHENOTYPE; RNA SEQUENCE; T LYMPHOCYTE; TRANSCRIPTOMICS; UPREGULATION; WEST NILE FEVER; YOUNG ADULT; FLOW CYTOMETRY; IMMUNOLOGY; T LYMPHOCYTE SUBPOPULATION;

ADULT; AGED; EPITOPES, T-LYMPHOCYTE; FEMALE; FLOW CYTOMETRY; HUMANS; MALE; MIDDLE AGED; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES; WEST NILE FEVER; YOUNG ADULT;

EID: 84956770018     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005375     Document Type: Article

References (46)

1. Petersen LR, Carson PJ, Biggerstaff BJ, Custer B, Borchardt SM, Busch MP, Estimated cumulative incidence of West Nile virus infection in US adults, 1999–2010. Epidemiol Infect. 2013;141(3):591–5. S0950268812001070 [pii]; doi: 10.1017/S0950268812001070 22640592
2. Gould LH, Fikrig E, West Nile virus: a growing concern? J Clin Invest. 2004;113(8):1102–7. doi: 10.1172/JCI21623 15085186
3. Hubalek Z, Halouzka J, West Nile fever—a reemerging mosquito-borne viral disease in Europe. Emerg Infect Dis. 1999;5(5):643–50. doi: 10.3201/eid0505.990505 10511520
4. Samuel MA, Diamond MS, Pathogenesis of West Nile Virus infection: a balance between virulence, innate and adaptive immunity, and viral evasion. J Virol. 2006;80(19):9349–60. 80/19/9349 [pii]; doi: 10.1128/JVI.01122-06 16973541
5. Brien JD, Uhrlaub JL, Nikolich-Zugich J, West Nile virus-specific CD4 T cells exhibit direct antiviral cytokine secretion and cytotoxicity and are sufficient for antiviral protection. J Immunol. 2008;181(12):8568–75. 181/12/8568 [pii]. 19050276
6. Sitati EM, Diamond MS, CD4+ T-cell responses are required for clearance of West Nile virus from the central nervous system. J Virol. 2006;80(24):12060–9. JVI.01650-06 [pii]; doi: 10.1128/JVI.01650-06 17035323
7. Lanteri MC, Diamond MS, Law JP, Chew GM, Wu S, Inglis HC, et al. Increased frequency of Tim-3 expressing T cells is associated with symptomatic West Nile virus infection. PLoS One. 2014;9(3):e92134. doi: 10.1371/journal.pone.0092134;PONE-D-13-53257 [pii]. 24642562
8. Leis AA, Stokic DS, Neuromuscular manifestations of west nile virus infection. Front Neurol. 2012;3:37. doi: 10.3389/fneur.2012.00037 22461779
9. Licon Luna RM, Lee E, Mullbacher A, Blanden RV, Langman R, Lobigs M, Lack of both Fas ligand and perforin protects from flavivirus-mediated encephalitis in mice. J Virol. 2002;76(7):3202–11. 11884544
10. Lanteri MC, O'Brien KM, Purtha WE, Cameron MJ, Lund JM, Owen RE, et al. Tregs control the development of symptomatic West Nile virus infection in humans and mice. J Clin Invest. 2009;119(11):3266–77. 39387 [pii]; doi: 10.1172/JCI39387 19855131
11. Netland J, Bevan MJ, CD8 and CD4 T cells in west nile virus immunity and pathogenesis. Viruses. 2013;5(10):2573–84. v5102573 [pii]; doi: 10.3390/v5102573 24153060
12. Hayes EB, Gubler DJ, West Nile virus: epidemiology and clinical features of an emerging epidemic in the United States. Annu Rev Med. 2006;57:181–94. doi: 10.1146/annurev.med.57.121304.131418 16409144
13. Becattini S, Latorre D, Mele F, Foglierini M, De GC, Cassotta A, et al. T cell immunity. Functional heterogeneity of human memory CD4(+) T cell clones primed by pathogens or vaccines. Science. 2015;347(6220):400–6. science.1260668 [pii]; doi: 10.1126/science.1260668 25477212
14. Carson PJ, Borchardt SM, Custer B, Prince HE, Dunn-Williams J, Winkelman V, et al. Neuroinvasive disease and West Nile virus infection, North Dakota, USA, 1999–2008. Emerg Infect Dis. 2012;18(4):684–6. doi: 10.3201/eid1804.111313 22469465
15. Kim CH, Rott L, Kunkel EJ, Genovese MC, Andrew DP, Wu L, et al. Rules of chemokine receptor association with T cell polarization in vivo. J Clin Invest. 2001;108(9):1331–9. doi: 10.1172/JCI13543 11696578
16. Araya N, Sato T, Ando H, Tomaru U, Yoshida M, Coler-Reilly A, et al. HTLV-1 induces a Th1-like state in CD4+CCR4+ T cells. J Clin Invest. 2014;124(8):3431–42. 75250 [pii]; doi: 10.1172/JCI75250 24960164
17. Ichii H, Sakamoto A, Arima M, Hatano M, Kuroda Y, Tokuhisa T, Bcl6 is essential for the generation of long-term memory CD4+ T cells. Int Immunol. 2007;19(4):427–33. dxm007 [pii]; doi: 10.1093/intimm/dxm007 17307796
18. Kohout TA, Nicholas SL, Perry SJ, Reinhart G, Junger S, Struthers RS, Differential desensitization, receptor phosphorylation, beta-arrestin recruitment, and ERK1/2 activation by the two endogenous ligands for the CC chemokine receptor 7. J Biol Chem. 2004;279(22):23214–22. doi: 10.1074/jbc.M402125200 [pii]. 15054093
19. Ness TL, Ewing JL, Hogaboam CM, Kunkel SL, CCR4 is a key modulator of innate immune responses. J Immunol. 2006;177(11):7531–9. 177/11/7531 [pii]. 17114422
20. Shevach EM, Mechanisms of foxp3+ T regulatory cell-mediated suppression. Immunity. 2009;30(5):636–45. doi: 10.1016/j.immuni.2009.04.010 19464986.
21. Brien JD, Uhrlaub JL, Hirsch A, Wiley CA, Nikolich-Zugich J, Key role of T cell defects in age-related vulnerability to West Nile virus. J Exp Med. 2009;206(12):2735–45. jem.20090222 [pii]; doi: 10.1084/jem.20090222 19901080
22. Han YW, Singh SK, Eo SK, The Roles and Perspectives of Toll-Like Receptors and CD4(+) Helper T Cell Subsets in Acute Viral Encephalitis. Immune Netw. 2012;12(2):48–57. doi: 10.4110/in.2012.12.2.48 22740790
23. Bigham AW, Buckingham KJ, Husain S, Emond MJ, Bofferding KM, Gildersleeve H, et al. Host genetic risk factors for West Nile virus infection and disease progression. PLoS One. 2011;6(9):e24745. doi: 10.1371/journal.pone.0024745;PONE-D-11-09427 [pii]. 21935451
24. James EA, LaFond RE, Gates TJ, Mai DT, Malhotra U, Kwok WW, Yellow fever vaccination elicits broad functional CD4+ T cell responses that recognize structural and nonstructural proteins. J Virol. 2013;87(23):12794–804. JVI.01160-13 [pii]; doi: 10.1128/JVI.01160-13 24049183
25. Jung KO, Khan AM, Tan BY, Hu Y, Simon GG, Nascimento EJ, et al. West Nile virus T-cell ligand sequences shared with other flaviviruses: a multitude of variant sequences as potential altered peptide ligands. J Virol. 2012;86(14):7616–24. JVI.00166-12 [pii]; doi: 10.1128/JVI.00166-12 22573867
26. Kawamata T, Ohno N, Sato K, Kobayashi M, Jo N, Yuji K, et al. A case of post-transplant adult T-cell leukemia/lymphoma presenting myelopathy similar to but distinct from human T-cell leukemia virus type I (HTLV- I)-associated myelopathy. Springerplus. 2014;3:581. doi: 10.1186/2193-1801-3-581;1291 [pii]. 25332881
27. Graham JB, Da CA, Lund JM, Regulatory T cells shape the resident memory T cell response to virus infection in the tissues. J Immunol. 2014;192(2):683–90. jimmunol.1202153 [pii]; doi: 10.4049/jimmunol.1202153 24337378
28. Qian F, Thakar J, Yuan X, Nolan M, Murray KO, Lee WT, et al. Immune markers associated with host susceptibility to infection with West Nile virus. Viral Immunol. 2014;27(2):39–47. doi: 10.1089/vim.2013.0074 24605787
29. Garcia MN, Hause AM, Walker CM, Orange JS, Hasbun R, Murray KO, Evaluation of prolonged fatigue post-West Nile virus infection and association of fatigue with elevated antiviral and proinflammatory cytokines. Viral Immunol. 2014;27(7):327–33. doi: 10.1089/vim.2014.0035 25062274
30. Piazza P, McMurtrey CP, Lelic A, Cook RL, Hess R, Yablonsky E, et al. Surface phenotype and functionality of WNV specific T cells differ with age and disease severity. PLoS One. 2010;5(12):e15343. doi: 10.1371/journal.pone.0015343 21179445
31. Gibson L, Barysauskas CM, McManus M, Dooley S, Lilleri D, Fisher D, et al. Reduced Frequencies of Polyfunctional CMV-Specific T Cell Responses in Infants with Congenital CMV Infection. J Clin Immunol. 2015;35(3):289–301. doi: 10.1007/s10875-015-0139-3 25712611
32. Kumar D, Drebot MA, Wong SJ, Lim G, Artsob H, Buck P, et al. A seroprevalence study of west nile virus infection in solid organ transplant recipients. Am J Transplant. 2004;4(11):1883–8. AJT592 [pii]; doi: 10.1111/j.1600-6143.2004.00592.x 15476490
33. Lanteri MC, Lee TH, Wen L, Kaidarova Z, Bravo MD, Kiely NE, et al. West Nile virus nucleic acid persistence in whole blood months after clearance in plasma: implication for transfusion and transplantation safety. Transfusion. 2014;54(12):3232–41. doi: 10.1111/trf.12764 24965017
34. Murray K, Walker C, Herrington E, Lewis JA, McCormick J, Beasley DW, et al. Persistent infection with West Nile virus years after initial infection. J Infect Dis. 2010;201(1):2–4. doi: 10.1086/648731 19961306
35. Stewart BS, Demarest VL, Wong SJ, Green S, Bernard KA, Persistence of virus-specific immune responses in the central nervous system of mice after West Nile virus infection. BMC Immunol. 2011;12:6. 1471-2172-12-6 [pii]; doi: 10.1186/1471-2172-12-6 21251256
36. Sejvar JJ, The long-term outcomes of human West Nile virus infection. Clin Infect Dis. 2007;44(12):1617–24. CID50140 [pii]; doi: 10.1086/518281 17516407
37. Busch MP, Tobler LH, Saldanha J, Caglioti S, Shyamala V, Linnen JM, et al. Analytical and clinical sensitivity of West Nile virus RNA screening and supplemental assays available in 2003. Transfusion. 2005;45(4):492–9. doi: 10.1111/j.0041-1132.2005.04382.x 15819668.
38. Novak EJ, Liu AW, Nepom GT, Kwok WW, MHC class II tetramers identify peptide-specific human CD4(+) T cells proliferating in response to influenza A antigen. J Clin Invest. 1999;104(12):R63–R7. doi: 10.1172/JCI8476 10606632
39. Novak EJ, Liu AW, Gebe JA, Falk BA, Nepom GT, Koelle DM, et al. Tetramer-guided epitope mapping: rapid identification and characterization of immunodominant CD4+ T cell epitopes from complex antigens. J Immunol. 2001;166(11):6665–70. 11359821
40. Kwok WW, Roti M, Delong JH, Tan V, Wambre E, James EA, et al. Direct ex vivo analysis of allergen-specific CD4+ T cells. J Allergy Clin Immunol. 2010;125(6):1407–9. S0091-6749(10)00583-X [pii]; doi: 10.1016/j.jaci.2010.03.037 20513526
41. WN V, DM S, Team RC. An Introduction to R. R Foundation for Statistical Computing Vienna, Austria: The R Project for Statistical Computing; 2015 [updated 1/1/2015]. 40–5]. Available from: http://www.R-project.org.
42. Robinson MD, Smyth GK, Small-sample estimation of negative binomial dispersion, with applications to SAGE data. Biostatistics. 2008;9(2):321–32. kxm030 [pii]; doi: 10.1093/biostatistics/kxm030 17728317
43. Robinson MD, Smyth GK, Moderated statistical tests for assessing differences in tag abundance. Bioinformatics. 2007;23(21):2881–7. btm453 [pii]; doi: 10.1093/bioinformatics/btm453 17881408
44. Robinson MD, McCarthy DJ, Smyth GK, edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26(1):139–40. btp616 [pii]; doi: 10.1093/bioinformatics/btp616 19910308
45. Robinson MD, Oshlack A, A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol. 2010;11(3):R25. gb-2010-11-3-r25 [pii]; doi: 10.1186/gb-2010-11-3-r25 20196867
46. McCarthy DJ, Chen Y, Smyth GK, Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Res. 2012;40(10):4288–97. gks042 [pii]; doi: 10.1093/nar/gks042 22287627