Type I interferon elevates co-regulatory receptor expression on CMV- and EBV-specific CD8 T cells in chronic hepatitis C

Frontiers in Immunology

Volumn 6, Issue JUN, 2015, Pages

  Owusu Sekyere, Solomon ^a   Suneetha, Pothakamuri Venkata ^a   Hardtke, Svenja ^a   Falk, Christine Susanne ^a,b   Hengst, Julia ^a   Manns, Michael Peter ^a,b   Cornberg, Markus ^a,b   Wedemeyer, Heiner ^a,b   Schlaphoff, Verena ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b German Center for Infectious Diesease (DZIF)   (Germany)

Author keywords

2B4; Co regulation; Cytokines; Hepatitis C; IFN alpha; PD 1; T cell regulation; TIM 3

Indexed keywords

ALPHA2 INTERFERON; CHEMOKINE RECEPTOR CXCR3; COLONY STIMULATING FACTOR 1; CUTANEOUS T CELL ATTRACTING CHEMOKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; HLA ANTIGEN CLASS 1; INTERCELLULAR ADHESION MOLECULE 1; INTERFERON; INTERLEUKIN 12P40; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 3; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 3; NATURAL KILLER CELL RECEPTOR 2B4; PEGINTERFERON ALPHA2A; PEPTIDE; PROGRAMMED DEATH 1 RECEPTOR; PROTEIN; RANTES; RECOMBINANT INTERCELLULAR ADHESION MOLECULE 1; RIBAVIRIN; SCATTER FACTOR; SOFOSBUVIR; STEM CELL FACTOR; STEM CELL GROWTH FACTOR BETA; T CELL IMMUNOGLOBULIN AND MUCIN DOMAIN CONTAINING PROTEIN 3; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG; UNINDEXED DRUG; VASCULAR CELL ADHESION MOLECULE 1;

ADULT; AGED; ARTICLE; CD8+ T LYMPHOCYTE; CELL FUNCTION; CELL PROLIFERATION; CELL STIMULATION; CELLULAR IMMUNITY; CHRONIC HEPATITIS C; CONTROLLED STUDY; CYTOMEGALOVIRUS; DEGRANULATION ASSAY; EPSTEIN BARR VIRUS; FEMALE; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IN VITRO STUDY; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PROSPECTIVE STUDY; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; STAINING; VERY ELDERLY; YOUNG ADULT;

EID: 84935098723     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2015.00270     Document Type: Article

References (48)

1. Gower E, Estes C, Blach S, Razavi-Shearer K, Razavi H. Global epidemiology and genotype distribution of the hepatitis C virus infection. J Hepatol (2014) 61(1 Suppl):S45-57. doi: 10.1016/j.jhep.2014.07.027
2. Park SH, Rehermann B. Immune responses to HCV and other hepatitis viruses. Immunity (2014) 40(1):13-24. doi:10.1016/j.immuni.2013.12.010
3. Klenerman P, Thimme R. T cell responses in hepatitis C: the good, the bad and the unconventional. Gut (2012) 61(8):1226-34. doi:10.1136/gutjnl-2011-300620
4. Bowen DG, Walker CM. Adaptive immune responses in acute and chronic hepatitis C virus infection. Nature (2005) 436(7053):946-52. doi:10.1038/nature04079
5. Fallahi P, Ferri C, Ferrari SM, Corrado A, Sansonno D, Antonelli A. Cytokines and HCV-related disorders. Clin Dev Immunol (2012) 2012:468107. doi:10.1155/2012/468107
6. Fahey S, Dempsey E, Long A. The role of chemokines in acute and chronic hepatitis C infection. Cell Mol Immunol (2014) 11(1):25-40. doi:10.1038/cmi.2013.37
7. Cacoub P, Gragnani L, Comarmond C, Zignego AL. Extrahepatic manifestations of chronic hepatitis C virus infection. Dig Liver Dis (2014) 46(Suppl 5):S165-73. doi:10.1016/j.dld.2014.10.005
8. Keeffe EB, Iwarson S, McMahon BJ, Lindsay KL, Koff RS, Manns M, et al. Safety and immunogenicity of hepatitis A vaccine in patients with chronic liver disease. Hepatology (1998) 27(3):881-6. doi:10.1002/hep.510270336
9. Majda-Stanislawska E, Bednarek M, Kuydowicz J. Immunogenicity of inactivated hepatitis A vaccine in children with chronic liver disease. Pediatr Infect Dis J (2004) 23(6):571-4. doi:10.1097/01.inf.0000130076.33497.6c
10. Wiedmann M, Liebert UG, Oesen U, Porst H, Wiese M, Schroeder S, et al. Decreased immunogenicity of recombinant hepatitis B vaccine in chronic hepatitis C. Hepatology (2000) 31(1):230-4. doi:10.1002/hep.510310134
11. Moorman JP, Zhang CL, Ni L, Ma CJ, Zhang Y, Wu XY, et al. Impaired hepatitis B vaccine responses during chronic hepatitis C infection: involvement of the PD-1 pathway in regulating CD4(+) T cell responses. Vaccine (2011) 29(17):3169-76. doi:10.1016/j.vaccine.2011.02.052
12. Gaeta GB, Stornaiuolo G, Precone DF, Amendola A, Zanetti AR. Immunogenicity and safety of an adjuvanted influenza vaccine in patients with decompensated cirrhosis. Vaccine (2002) 20(Suppl 5):B33-5. doi:10.1016/S0264-410X(02)00510-8
13. Monaco S, Ferrari S, Gajofatto A, Zanusso G, Mariotto S. HCV-related nervous system disorders. Clin Dev Immunol (2012) 2012:236148. doi:10.1155/2012/236148
14. van Riet E, Adegnika AA, Retra K, Vieira R, Tielens AG, Lell B, et al. Cellular and humoral responses to influenza in gabonese children living in rural and semi-urban areas. J Infect Dis (2007) 196(11):1671-8. doi:10.1086/522010
15. Harcourt GC, Donfield S, Gomperts E, Daar ES, Goulder P Jr, Phillips RE, et al. Longitudinal analysis of CD8 T-cell responses to HIV and hepatitis C virus in a cohort of co-infected haemophiliacs. AIDS (2005) 19(11):1135-43. doi:10.1097/01.aids.0000176213.10367.05
16. Lucas M, Vargas-Cuero AL, Lauer GM, Barnes E, Willberg CB, Semmo N, et al. Pervasive influence of hepatitis C virus on the phenotype of antiviral CD8+ T cells. J Immunol (2004) 172(3):1744-53. doi:10.4049/jimmunol.172.3.1744
17. Stelekati E, Shin H, Doering TA, Dolfi DV, Ziegler CG, Beiting DP, et al. Bystander chronic infection negatively impacts development of CD8(+) T cell memory. Immunity (2014) 40(5):801-13. doi:10.1016/j.immuni.2014.04.010
18. Penna A, Pilli M, Zerbini A, Orlandini A, Mezzadri S, Sacchelli L, et al. Dysfunction and functional restoration of HCV-specific CD8 responses in chronic hepatitis C virus infection. Hepatology (2007) 45(3):588-601. doi:10.1002/hep.21541
19. Suneetha PV, Schlaphoff V, Wang C, Stegmann KA, Fytili P, Sarin SK, et al. Effect of peptide pools on effector functions of antigen-specific CD8+ T cells. J Immunol Methods (2009) 342(1-2):33-48. doi:10.1016/j.jim.2008.11.020
20. Schlaphoff V, Lunemann S, Suneetha PV, Jaroszewicz J, Grabowski J, Dietz J, et al. Dual function of the NK cell receptor 2B4 (CD244) in the regulation of HCV-specific CD8+ T cells. PLoS Pathog (2011) 7(5):e1002045. doi:10.1371/journal.ppat.1002045
21. Baitsch L, Legat A, Barba L, Fuertes Marraco SA, Rivals JP, Baumgaertner P, et al. Extended co-expression of inhibitory receptors by human CD8 T-cells depending on differentiation, antigen-specificity and anatomical localization. PLoS One (2012) 7(2):e30852. doi:10.1371/journal.pone.0030852
22. Kroy DC, Ciuffreda D, Cooperrider JH, Tomlinson M, Hauck GD, Aneja J, et al. Liver environment and HCV replication affect human T-cell phenotype and expression of inhibitory receptors. Gastroenterology (2014) 146(2):550-61. doi:10.1053/j.gastro.2013.10.022
23. Legat A, Speiser DE, Pircher H, Zehn D, Fuertes Marraco SA. Inhibitory receptor expression depends more dominantly on differentiation and activation than "exhaustion" of human CD8 T cells. Front Immunol (2013) 4:455. doi:10.3389/fimmu.2013.00455
24. Golden-Mason L, Palmer BE, Kassam N, Townshend-Bulson L, Livingston S, McMahon BJ, et al. Negative immune regulator Tim-3 is overexpressed on T cells in hepatitis C virus infection and its blockade rescues dysfunctional CD4+ and CD8+ T cells. J Virol (2009) 83(18):9122-30. doi:10.1128/JVI.00639-09
25. Rogalska-Taranta M, Markova A, Taranta A, Lunemann S, Schlaphoff V, Flisiak R, et al. Altered effector functions of NK cells in chronic hepatitis C are associated with IFNL3 polymorphism. J Leukocyte Bio (in press).
26. Wherry EJ. T cell exhaustion. Nat Immunol (2011) 12(6):492-9. doi:10.1038/ni.2035
27. Golden-Mason L, Palmer B, Klarquist J, Mengshol JA, Castelblanco N, Rosen HR. Upregulation of PD-1 expression on circulating and intrahepatic hepatitis C virus-specific CD8+ T cells associated with reversible immune dysfunction. J Virol (2007) 81(17):9249-58. doi:10.1128/JVI.00409-07
28. Owusu Sekyere S, Suneetha PV, Kraft AR, Zhang S, Dietz J, Sarrazin C, et al. A heterogeneous hierarchy of co-regulatory receptors regulates exhaustion of HCV-specific CD8 T cells in patients with chronic hepatitis C. J Hepatol (2015) 62(1):31-40. doi:10.1016/j.jhep.2014.08.008
29. Bengsch B, Seigel B, Ruhl M, Timm J, Kuntz M, Blum HE, et al. Coexpression of PD-1, 2B4, CD160 and KLRG1 on exhausted HCV-specific CD8+ T cells is linked to antigen recognition and T cell differentiation. PLoS Pathog (2010) 6(6):e1000947. doi:10.1371/journal.ppat.1000947
30. Blackburn SD, Shin H, Haining WN, Zou T, Workman CJ, Polley A, et al. Coregulation of CD8+ T cell exhaustion by multiple inhibitory receptors during chronic viral infection. Nat Immunol (2009) 10(1):29-37. doi:10.1038/ni.1679
31. Utzschneider DT, Legat A, Fuertes Marraco SA, Carrie L, Luescher I, Speiser DE, et al. T cells maintain an exhausted phenotype after antigen withdrawal and population reexpansion. Nat Immunol (2013) 14(6):603-10. doi:10.1038/ni.2606
32. Duraiswamy J, Ibegbu CC, Masopust D, Miller JD, Araki K, Doho GH, et al. Phenotype, function, and gene expression profiles of programmed death-1(hi) CD8 T cells in healthy human adults. J Immunol (2011) 186(7):4200-12. doi:10.4049/jimmunol.1001783
33. Khaitan A, Unutmaz D. Revisiting immune exhaustion during HIV infection. Curr HIV/AIDS Rep (2011) 8(1):4-11. doi:10.1007/s11904-010-0066-0
34. Verbrugge I, Hagekyriakou J, Sharp LL, Galli M, West A, McLaughlin NM, et al. Radiotherapy increases the permissiveness of established mammary tumors to rejection by immunomodulatory antibodies. Cancer Res (2012) 72(13):3163-74. doi:10.1158/0008-5472.CAN-12-0210
35. Brodin P, Jojic V, Gao T, Bhattacharya S, Angel CJ, Furman D, et al. Variation in the human immune system is largely driven by non-heritable influences. Cell (2015) 160(1-2):37-47. doi:10.1016/j.cell.2014.12.020
36. Berg RE, Forman J. The role of CD8 T cells in innate immunity and in antigen non-specific protection. Curr Opin Immunol (2006) 18(3):338-43. doi:10.1016/j.coi.2006.03.010
37. Freeman BE, Hammarlund E, Raue HP, Slifka MK. Regulation of innate CD8+ T-cell activation mediated by cytokines. Proc Natl Acad Sci U S A (2012) 109(25):9971-6. doi:10.1073/pnas.1203543109
38. Cox MA, Kahan SM, Zajac AJ. Anti-viral CD8 T cells and the cytokines that they love. Virology (2013) 435(1):157-69. doi:10.1016/j.virol.2012.09.012
39. Kim JJ, Nottingham LK, Sin JI, Tsai A, Morrison L, Oh J, et al. CD8 positive T cells influence antigen-specific immune responses through the expression of chemokines. J Clin Invest (1998) 102(6):1112-24. doi:10.1172/JCI3986
40. Bachmann MF, McKall-Faienza K, Schmits R, Bouchard D, Beach J, Speiser DE, et al. Distinct roles for LFA-1 and CD28 during activation of naive T cells: adhesion versus costimulation. Immunity (1997) 7(4):549-57. doi:10.1016/S1074-7613(00)80376-3
41. Xu HC, Grusdat M, Pandyra AA, Polz R, Huang J, Sharma P, et al. Type I interferon protects antiviral CD8+ T cells from NK cell cytotoxicity. Immunity (2014) 40(6):949-60. doi:10.1016/j.immuni.2014.05.004
42. Chlewicki LK, Velikovsky CA, Balakrishnan V, Mariuzza RA, Kumar V. Molecular basis of the dual functions of 2B4 (CD244). J Immunol (2008) 180(12):8159-67. doi:10.4049/jimmunol.180.12.8159
43. Wang L, Zhao C, Peng Q, Shi J, Gu G. Expression levels of CD28, CTLA-4, PD-1 and Tim-3 as novel indicators of T-cell immune function in patients with chronic hepatitis B virus infection. Biomed Rep (2014) 2(2):270-4. doi:10.3892/br.2014.217
44. Pawlotsky JM. New hepatitis C therapies: the toolbox, strategies, and challenges. Gastroenterology (2014) 146(5):1176-92. doi:10.1053/j.gastro.2014.03.003
45. Werner JM, Serti E, Chepa-Lotrea X, Stoltzfus J, Ahlenstiel G, Noureddin M, et al. Ribavirin improves the IFN-gamma response of natural killer cells to IFN-based therapy of hepatitis C virus infection. Hepatology (2014) 60(4):1160-9. doi:10.1002/hep.27092
46. Suarez-Ramirez JE, Tarrio ML, Kim K, Demers DA, Biron CA. CD8 T cells in innate immune responses: using STAT4-dependent but antigen-independent pathways to gamma interferon during viral infection. MBio (2014) 5(5):e1978-1914. doi:10.1128/mBio.01978-14
47. Su LF, Kidd BA, Han A, Kotzin JJ, Davis MM. Virus-specific CD4(+) memory-phenotype T cells are abundant in unexposed adults. Immunity (2013) 38(2):373-83. doi:10.1016/j.immuni.2012.10.021
48. Welsh RM, Che JW, Brehm MA, Selin LK. Heterologous immunity between viruses. Immunol Rev (2010) 235(1):244-66. doi:10.1111/j.0105-2896.2010.00897.x