A gene expression signature that correlates with CD8+ T cell expansion in acute EBV infection

Journal of Immunology

Volumn 195, Issue 9, 2015, Pages 4185-4197

  Greenough, Thomas C ^a   Straubhaar, Juerg R ^a   Kamga, Larisa ^a   Weiss, Eric R ^a   Brody, Robin M ^a   McManus, Margaret M ^a   Lambrecht, Linda K ^a   Somasundaran, Mohan ^a   Luzuriaga, Katherine F ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; CD27 ANTIGEN; CD38 ANTIGEN; CD69 ANTIGEN; CHEMOKINE; CHEMOKINE RECEPTOR CCR7; CHEMOKINE RECEPTOR CXCR1; CYTOKINE; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; EOMESODERMIN; FAS ANTIGEN; FAS LIGAND; GAMMA INTERFERON RECEPTOR; HIGH MOBILITY GROUP B3 PROTEIN; HLA A ANTIGEN; INHIBITOR OF DIFFERENTIATION 2; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 7 RECEPTOR; PROGRAMMED DEATH 1 LIGAND 1; PROTEIN KINASE LYN; RANTES; RECEPTOR; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR T BET; TRANSCRIPTION FACTOR ZEB1; TRANSCRIPTION FACTOR; TRANSCRIPTOME;

ADA GENE; ADAM8 GENE; ADULT; ANTIGEN RECOGNITION; ARTICLE; BATF GENE; CCL5 GENE; CCR7 GENE; CD160 GENE; CD8+ T LYMPHOCYTE; CELL DIVISION; CELL EXPANSION; CELL METABOLISM; CELLULAR IMMUNITY; CLINICAL ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; CONVALESCENCE; CR1 GENE; CTLA4 GENE; CX3CR1 GENE; DISEASE SEVERITY; EPITOPE MAPPING; EPSTEIN BARR VIRUS INFECTION; FAS GENE; FASLG GENE; FATIGUE; FCER1G GENE; FEMALE; GATA3 GENE; GENE; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC ASSOCIATION; GFI1 GENE; GZMA GENE; GZMB GENE; GZMH GENE; HEADACHE; HMGB3 GENE; HUMAN; HUMAN CELL; ID2 GENE; IFNG GENE; IFNGR2 GENE; IL13RA1 GENE; IL2RA GENE; IL2RG GENE; IL4R GENE; IL7R GENE; IMMUNOMODULATION; IMMUNOREGULATION; INTRACELLULAR SIGNALING; ITGAL GENE; ITGB2 GENE; KLRG1 GENE; LAG3 GENE; LEF GENE; LOSS OF APPETITE; LYMPHOCYTE COUNT; LYMPHOCYTE DIFFERENTIATION; LYN GENE; MALAISE; MALE; MALT1 GENE; MLL5 GENE; MONONUCLEOSIS; PDCD1 GENE; PERIPHERAL LYMPHOCYTE; PRDM1 GENE; PRF1 GENE; PRIORITY JOURNAL; PRKCD GENE; PROTEIN EXPRESSION; SORE THROAT; SPON2 GENE; SWAP70 GENE; T LYMPHOCYTE ACTIVATION; TBX21 GENE; TCF7 GENE; TCF7L GENE; TIGIT GENE; TIM3 GENE; UPREGULATION; VIRUS LOAD; VIRUS REPLICATION; YOUNG ADULT; ZC3H8 GENE; ZEB1 GENE; ACUTE DISEASE; ADOLESCENT; EPSTEIN BARR VIRUS; GENETICS; IMMUNOLOGY;

ACUTE DISEASE; ADOLESCENT; ADULT; ANTIGENS, CD38; CD8-POSITIVE T-LYMPHOCYTES; FEMALE; HERPESVIRUS 4, HUMAN; HUMANS; INFECTIOUS MONONUCLEOSIS; MALE; RECEPTORS, INTERLEUKIN-7; TRANSCRIPTION FACTORS; TRANSCRIPTOME;

EID: 84945157647     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1401513     Document Type: Article

References (73)

1. + T cells during the primary immune response to Epstein-Barr virus In vivo. J. Exp. Med. 187: 1395-1402.
2. Balfour, H. H., Jr., C. J. Holman, K. M. Hokanson, M. M. Lelonek, J. E. Giesbrecht, D. R. White, D. O. Schmeling, C. H. Webb, W. Cavert, D. H. Wang, and R. C. Brundage. 2005. A prospective clinical study of Epstein-Barr virus and host interactions during acute infectious mononucleosis. J. Infect. Dis. 192: 1505-1512.
3. Balfour, H. H., Jr., O. A. Odumade, D. O. Schmeling, B. D. Mullan, J. A. Ed, J. A. Knight, H. E. Vezina, W. Thomas, and K. A. Hogquist. 2013. Behavioral, virologic, and immunologic factors associated with acquisition and severity of primary Epstein-Barr virus infection in university students. J. Infect. Dis. 207: 80-88.
4. Hadinoto, V., M. Shapiro, C. C. Sun, and D. A. Thorley-Lawson. 2009. The dynamics of EBV shedding implicate a central role for epithelial cells in amplifying viral output. PLoS Pathog. 5: e1000496.
5. Niederman, J. C., G. Miller, H. A. Pearson, J. S. Pagano, and J. M. Dowaliby. 1976. Infectious mononucleosis. Epstein-Barr-virus shedding in saliva and the oropharynx. N. Engl. J. Med. 294: 1355-1359.
6. + T cells. J. Immunol. 168: 4184-4191.
7. + T cell memory: relationships between epitope specificity, cell phenotype, and immediate effector function. J. Immunol. 167: 2019-2029.
8. Babcock, G. J., L. L. Decker, R. B. Freeman, and D. A. Thorley-Lawson. 1999. Epstein-barr virus-infected resting memory B cells, not proliferating lymphoblasts, accumulate in the peripheral blood of immunosuppressed patients. J. Exp. Med. 190: 567-576.
9. Souza, T. A., B. D. Stollar, J. L. Sullivan, K. Luzuriaga, and D. A. Thorley-Lawson. 2007. Influence of EBV on the peripheral blood memory B cell compartment. J. Immunol. 179: 3153-3160.
10. Keymeulen, B., E. Vandemeulebroucke, A. G. Ziegler, C. Mathieu, L. Kaufman, G. Hale, F. Gorus, M. Goldman, M. Walter, S. Candon, et al. 2005. Insulin needs after CD3-antibody therapy in new-onset type 1 diabetes. N. Engl. J. Med. 352: 2598-2608.
11. Landgren, O., E. S. Gilbert, J. D. Rizzo, G. Socié, P. M. Banks, K. A. Sobocinski, M. M. Horowitz, E. S. Jaffe, D. W. Kingma, L. B. Travis, et al. 2009. Risk factors for lymphoproliferative disorders after allogeneic hematopoietic cell transplantation. Blood 113: 4992-5001.
12. Long, H. M., G. S. Taylor, and A. B. Rickinson. 2011. Immune defence against EBV and EBV-associated disease. Curr. Opin. Immunol. 23: 258-264.
13. + T cell exhaustion versus memory. Immunity 37: 1130-1144.
14. Haining, W. N., B. L. Ebert, A. Subrmanian, E. J. Wherry, Q. Eichbaum, J. W. Evans, R. Mak, S. Rivoli, J. Pretz, J. Angelosanto, et al. 2008. Identification of an evolutionarily conserved transcriptional signature of CD8 memory differentiation that is shared by T and B cells. J. Immunol. 181: 1859-1868.
15. + T cell exhaustion during chronic viral infection. Immunity 27: 670-684.
16. Querec, T. D., R. S. Akondy, E. K. Lee, W. Cao, H. I. Nakaya, D. Teuwen, A. Pirani, K. Gernert, J. Deng, B. Marzolf, et al. 2009. Systems biology approach predicts immunogenicity of the yellow fever vaccine in humans. Nat. Immunol. 10: 116-125.
17. + T cell differentiation. J. Clin. Invest. 120: 4077-4090.
18. Dunmire, S. K., O. A. Odumade, J. L. Porter, J. Reyes-Genere, D. O. Schmeling, H. Bilgic, D. Fan, E. C. Baechler, H. H. Balfour, Jr., and K. A. Hogquist. 2014. Primary EBV infection induces an expression profile distinct from other viruses but similar to hemophagocytic syndromes. PLoS One 9: e85422.
19. + T cells shows that PD-1 inhibits T cell function by upregulating BATF. Nat. Med. 16: 1147-1151.
20. + T cells in hepatitis B and C are characterized by a lack of antigen-specific T-bet induction. J. Exp. Med. 211: 2047-2059.
21. + T cell responses in EBV infection. J. Immunol. 167: 4450-4457.
22. + T cells varies by stage of infection, epitope specificity, and T-cell receptor usage. PLoS One 5: e12926.
23. Hasley, R. B., C. Hong, W. Li, T. Friesen, Y. Nakamura, G. Y. Kim, J. H. Park, J. A. Hixon, S. Durum, Z. Hu, et al. 2013. HIV immune activation drives increased Eomes expression in memory CD8 T cells in association with transcriptional downregulation of CD127. AIDS 27: 1867-1877.
24. Roederer, M., J. L. Nozzi, and M. C. Nason. 2011. SPICE: exploration and analysis of post-cytometric complex multivariate datasets. Cytometry A 79: 167-174.
25. Geiss, G. K., R. E. Bumgarner, B. Birditt, T. Dahl, N. Dowidar, D. L. Dunaway, H. P. Fell, S. Ferree, R. D. George, T. Grogan, et al. 2008. Direct multiplexed measurement of gene expression with color-coded probe pairs. Nat. Biotechnol. 26: 317-325.
26. Irizarry, R. A., B. Hobbs, F. Collin, Y. D. Beazer-Barclay, K. J. Antonellis, U. Scherf, and T. P. Speed. 2003. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264.
27. Langfelder, P., R. Luo, M. C. Oldham, and S. Horvath. 2011. Is my network module preserved and reproducible? PLOS Comput. Biol. 7: e1001057.
28. Oldham, M. C., G. Konopka, K. Iwamoto, P. Langfelder, T. Kato, S. Horvath, and D. H. Geschwind. 2008. Functional organization of the transcriptome in human brain. Nat. Neurosci. 11: 1271-1282.
29. Reich, M., T. Liefeld, J. Gould, J. Lerner, P. Tamayo, and J. P. Mesirov. 2006. GenePattern 2.0. Nat. Genet. 38: 500-501.
30. Smyth, G. K., J. Michaud, and H. S. Scott. 2005. Use of within-array replicate spots for assessing differential expression in microarray experiments. Bioinformatics 21: 2067-2075.
31. Gentleman, R. C., V. J. Carey, D. M. Bates, B. Bolstad, M. Dettling, S. Dudoit, B. Ellis, L. Gautier, Y. Ge, J. Gentry, et al. 2004. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5: R80.
32. Huang, D. W., B. T. Sherman, X. Zheng, J. Yang, T. Imamichi, R. Stephens, and R. A. Lempicki. 2009. Extracting biological meaning from large gene lists with DAVID. Curr. Protoc. Bioinformatics Chapter 13: Unit 13.11. doi:10.1002/0471250953.bi1311s27.
33. Huang, W., B. T. Sherman, and R. A. Lempicki. 2009. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37: 1-13.
34. Hadinoto, V., M. Shapiro, T. C. Greenough, J. L. Sullivan, K. Luzuriaga, and D. A. Thorley-Lawson. 2008. On the dynamics of acute EBV infection and the pathogenesis of infectious mononucleosis. Blood 111: 1420-1427.
35. + T cell responses from primary to persistent phases of Epstein-Barr virus infection. J. Exp. Med. 195: 893-905.
36. + T cell responses after natural primary infection of humans with Epstein-Barr virus. Viral Immunol. 16: 3-16.
37. Hislop, A. D., G. S. Taylor, D. Sauce, and A. B. Rickinson. 2007. Cellular responses to viral infection in humans: lessons from Epstein-Barr virus. Annu. Rev. Immunol. 25: 587-617.
38. + T-cell memory and exhaustion. Immunol. Rev. 236: 167-175.
39. + T cell exhaustion by multiple inhibitory receptors during chronic viral infection. Nat. Immunol. 10: 29-37.
40. hi CD8 T cells in healthy human adults. J. Immunol. 186: 4200-4212.
41. + T cell differentiation. Nat. Rev. Immunol. 12: 749-761.
42. Rutishauser, R. L., and S. M. Kaech. 2010. Generating diversity: transcriptional regulation of effector and memory CD8 T-cell differentiation. Immunol. Rev. 235: 219-233.
43. + T cells differently expressing three cytolytic effector molecules. J. Immunol. 177: 4330-4340.
44. Kaech, S. M., E. J. Wherry, and R. Ahmed. 2002. Effector and memory T-cell differentiation: implications for vaccine development. Nat. Rev. Immunol. 2: 251-262.
45. + T cell levels: results of 6 years of follow-up. The Los Angeles Center, Multicenter AIDS Cohort Study. J. Acquir. Immune Defic. Syndr. 6: 904-912.
46. + T-lymphocyte activation in HIV-1 disease reflects an aspect of pathogenesis distinct from viral burden and immunodeficiency. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 18: 332-340.
47. Kaech, S. M., J. T. Tan, E. J. Wherry, B. T. Konieczny, C. D. Surh, and R. Ahmed. 2003. Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat. Immunol. 4: 1191-1198.
48. + T cells in acute infectious mononucleosis. Nat. Med. 2: 906-911.
49. Rickinson, A. B., H. M. Long, U. Palendira, C. Münz, and A. D. Hislop. 2014. Cellular immune controls over Epstein-Barr virus infection: new lessons from the clinic and the laboratory. Trends Immunol. 35: 159-169.
50. Boyman, O., and J. Sprent. 2012. The role of interleukin-2 during homeostasis and activation of the immune system. Nat. Rev. Immunol. 12: 180-190.
51. - subsets suggest differentiation independent of CD45RA expression. Blood 109: 2863-2870.
52. + T cell response to infection and memory T cell formation. Nat. Immunol. 14: 404-412.
53. Huang, W., B. T. Sherman, and R. A. Lempicki. 2009. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4: 44-57.
54. + T cells during primary infection differentiates the capacity for durable immune control. J. Immunol. 193: 5709-5722.
55. + T-cell cytotoxic potential in HIV elite controllers is associated with T-bet expression. Blood 117: 3799-3808.
56. + T cells contribute to lymphoproliferation in Epstein-Barr virus-associated infectious mononucleosis. J. Clin. Invest. 115: 3602-3612.
57. Cornberg, M., S. C. Clute, L. B. Watkin, F. M. Saccoccio, S. K. Kim, Y. N. Naumov, M. A. Brehm, N. Aslan, R. M. Welsh, and L. K. Selin. 2010. CD8 T cell cross-reactivity networks mediate heterologous immunity in human EBV and murine vaccinia virus infections. J. Immunol. 184: 2825-2838.
58. Welsh, R. M., J. W. Che, M. A. Brehm, and L. K. Selin. 2010. Heterologous immunity between viruses. Immunol. Rev. 235: 244-266.
59. + lineages. J. Immunol. 179: 7406-7414.
60. Willinger, T., T. Freeman, H. Hasegawa, A. J. McMichael, and M. F. Callan. 2005. Molecular signatures distinguish human central memory from effector memory CD8 T cell subsets. J. Immunol. 175: 5895-5903.
61. Cox, M. A., L. E. Harrington, and A. J. Zajac. 2011. Cytokines and the inception of CD8 T cell responses. Trends Immunol. 32: 180-186.
62. Sauce, D., M. Larsen, S. J. Curnow, A. M. Leese, P. A. Moss, A. D. Hislop, M. Salmon, and A. B. Rickinson. 2006. EBV-associated mononucleosis leads to long-term global deficit in T-cell responsiveness to IL-15. Blood 108: 11-18.
63. + T cell differentiation: contrasting pictures in blood and tonsillar lymphoid tissue. J. Infect. Dis. 195: 268-278.
64. Wang, Y., I. Misumi, A. D. Gu, T. A. Curtis, L. Su, J. K. Whitmire, and Y. Y. Wan. 2013. GATA-3 controls the maintenance and proliferation of T cells downstream of TCR and cytokine signaling. Nat. Immunol. 14: 714-722.
65. Chandele, A., N. S. Joshi, J. Zhu, W. E. Paul, W. J. Leonard, and S. M. Kaech. 2008. Formation of IL-7Ralphahigh and IL-7Ralphalow CD8 T cells during infection is regulated by the opposing functions of GABPalpha and Gfi-1. J. Immunol. 180: 5309-5319.
66. + T cell responses during chronic infection. Nat. Immunol. 12: 663-671. doi:10.1038/ni.2046.
67. + T cells. Nat. Immunol. 15: 373-383.
68. Baitsch, L., A. Legat, L. Barba, S. A. Fuertes Marraco, J. P. Rivals, P. Baumgaertner, C. Christiansen-Jucht, H. Bouzourene, D. Rimoldi, H. Pircher, et al. 2012. Extended co-expression of inhibitory receptors by human CD8 T-cells depending on differentiation, antigen-specificity and anatomical localization. PLoS One 7: e30852.
69. + T cells is linked to antigen recognition and T cell differentiation. PLoS Pathog. 6: e1000947.
70. Jin, H. T., A. C. Anderson, W. G. Tan, E. E. West, S. J. Ha, K. Araki, G. J. Freeman, V. K. Kuchroo, and R. Ahmed. 2010. Cooperation of Tim-3 and PD-1 in CD8 T-cell exhaustion during chronic viral infection. Proc. Natl. Acad. Sci. USA 107: 14733-14738.
71. + T-cell response that disappears following primary Epstein-Barr virus infection. J. Virol. 83: 9068-9078.
72. + T cell exhaustion during chronic viral infection. Immunity 31: 309-320.
73. van Gisbergen, K. P., N. A. Kragten, K. M. Hertoghs, F. M. Wensveen, S. Jonjic, J. Hamann, M. A. Nolte, and R. A. van Lier. 2012. Mouse Hobit is a homolog of the transcriptional repressor Blimp-1 that regulates NKT cell effector differentiation. Nat. Immunol. 13: 864-871.