Selective expansion of high functional avidity memory CD8 T cell clonotypes during hepatitis C virus reinfection and clearance

PLoS Pathogens

Volumn 13, Issue 2, 2017, Pages

  Abdel Hakeem, Mohamed S ^a,b,c   Boisvert, Maude ^a   Bruneau, Julie ^a,c   Soudeyns, Hugo ^c,d   Shoukry, Naglaa H ^a,c  

^a CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^b CAIRO UNIVERSITY   (Egypt)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

^d UNIVERSITY OF MONTREAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 2; INTERLEUKIN 7 RECEPTOR; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; T LYMPHOCYTE RECEPTOR; TUMOR NECROSIS FACTOR; LYMPHOCYTE ANTIGEN RECEPTOR;

ARTICLE; CD8+ T LYMPHOCYTE; DISEASE CLEARANCE; EC50; ENZYME LINKED IMMUNOSPOT ASSAY; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GENE SEQUENCE; HEPATITIS C; HUMAN; IMMUNE RESPONSE; MICROBIAL DIVERSITY; PERSISTENT VIRUS INFECTION; POLYMERASE CHAIN REACTION; REINFECTION; HEPACIVIRUS; IMMUNOLOGICAL MEMORY; IMMUNOLOGY;

CD8-POSITIVE T-LYMPHOCYTES; FLOW CYTOMETRY; HEPACIVIRUS; HEPATITIS C; HUMANS; IMMUNOLOGIC MEMORY; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA;

EID: 85014123404     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1006191     Document Type: Article

References (54)

1. Turner SJ, La Gruta NL, Kedzierska K, Thomas PG, Doherty PC, Functional implications of T cell receptor diversity. Curr Opin Immunol. 2009;21(3):286–90. Epub 2009/06/16. PubMed Central PMCID: PMCPMC2706259. doi: 10.1016/j.coi.2009.05.00419524428
2. Blackman MA, Woodland DL, The narrowing of the CD8 T cell repertoire in old age. Curr Opin Immunol. 2011;23(4):537–42. Epub 2011/06/10. PubMed Central PMCID: PMCPMC3163762. doi: 10.1016/j.coi.2011.05.00521652194
3. Welsh RM, Che JW, Brehm MA, Selin LK, Heterologous immunity between viruses. Immunol Rev. 2010;235(1):244–66. Epub 2010/06/12. PubMed Central PMCID: PMCPMC2917921. doi: 10.1111/j.0105-2896.2010.00897.x20536568
4. Nikolich-Zugich J, Slifka MK, Messaoudi I, The many important facets of T-cell repertoire diversity. Nat Rev Immunol. 2004;4(2):123–32. Epub 2004/03/26. doi: 10.1038/nri129215040585
5. Venturi V, Price DA, Douek DC, Davenport MP, The molecular basis for public T-cell responses?Nat Rev Immunol. 2008;8(3):231–8. http://www.nature.com/nri/journal/v8/n3/suppinfo/nri2260_S1.html. doi: 10.1038/nri226018301425
6. Li H, Ye C, Ji G, Han J, Determinants of public T cell responses. Cell Research. 2012;22(1):33–42. PubMed Central PMCID: PMCPMC3351923. doi: 10.1038/cr.2012.122212481
7. Price DA, Brenchley JM, Ruff LE, Betts MR, Hill BJ, Roederer M, et al. Avidity for antigen shapes clonal dominance in CD8+ T cell populations specific for persistent DNA viruses. J Exp Med. 2005;202(10):1349–61. Epub 2005/11/17. PubMed Central PMCID: PMCPMC2212993. doi: 10.1084/jem.2005135716287711
8. Almeida JR, Price DA, Papagno L, Arkoub ZA, Sauce D, Bornstein E, et al. Superior control of HIV-1 replication by CD8+ T cells is reflected by their avidity, polyfunctionality, and clonal turnover. J Exp Med. 2007;204(10):2473–85. Epub 2007/09/26. doi: 10.1084/jem.2007078417893201
9. Almeida JR, Sauce D, Price DA, Papagno L, Shin SY, Moris A, et al. Antigen sensitivity is a major determinant of CD8+ T-cell polyfunctionality and HIV-suppressive activity. Blood. 2009;113(25):6351–60. Epub 2009/04/25. PubMed Central PMCID: PMC2710928. doi: 10.1182/blood-2009-02-20655719389882
10. Chen H, Ndhlovu ZM, Liu D, Porter LC, Fang JW, Darko S, et al. TCR clonotypes modulate the protective effect of HLA class I molecules in HIV-1 infection. Nat Immunol. 2012;13(7):691–700. Epub 2012/06/12. PubMed Central PMCID: PMC3538851. doi: 10.1038/ni.234222683743
11. Iglesias MC, Almeida JR, Fastenackels S, van Bockel DJ, Hashimoto M, Venturi V, et al. Escape from highly effective public CD8+ T-cell clonotypes by HIV. Blood. 2011;118(8):2138–49. Epub 2011/07/08. PubMed Central PMCID: PMC3162351. doi: 10.1182/blood-2011-01-32878121734237
12. Dong T, Stewart-Jones G, Chen N, Easterbrook P, Xu X, Papagno L, et al. HIV-specific cytotoxic T cells from long-term survivors select a unique T cell receptor. J Exp Med. 2004;200(12):1547–57. PubMed Central PMCID: PMC2212004. doi: 10.1084/jem.2003204415596521
13. Mendoza D, Royce C, Ruff LE, Ambrozak DR, Quigley MF, Dang T, et al. HLA B*5701-positive long-term nonprogressors/elite controllers are not distinguished from progressors by the clonal composition of HIV-specific CD8+ T cells. J Virol. 2012;86(7):4014–8. PubMed Central PMCID: PMC3302536. doi: 10.1128/JVI.06982-1122278241
14. Ladell K, Hashimoto M, Iglesias MC, Wilmann PG, McLaren JE, Gras S, et al. A molecular basis for the control of preimmune escape variants by HIV-specific CD8+ T cells. Immunity. 2013;38(3):425–36. Epub 2013/03/26. doi: 10.1016/j.immuni.2012.11.02123521884
15. Ndhlovu ZM, Stampouloglou E, Cesa K, Mavrothalassitis O, Alvino DM, Li JZ, et al. The Breadth of Expandable Memory CD8+ T Cells Inversely Correlates with Residual Viral Loads in HIV Elite Controllers. J Virol. 2015;89(21):10735–47. Epub 2015/08/14. PubMed Central PMCID: PMCPMC4621138. doi: 10.1128/JVI.01527-1526269189
16. Hoofnagle JH, Course and outcome of hepatitis C. Hepatology. 2002;36(5 Suppl 1):S21–9. Epub 2002/10/31.
17. Meyer-Olson D, Shoukry NH, Brady KW, Kim H, Olson DP, Hartman K, et al. Limited T cell receptor diversity of HCV-specific T cell responses is associated with CTL escape. J Exp Med. 2004;200(3):307–19. doi: 10.1084/jem.2004063815289502
18. Neveu B, Debeaupuis E, Echasserieau K, le Moullac-Vaidye B, Gassin M, Jegou L, et al. Selection of high-avidity CD8 T cells correlates with control of hepatitis C virus infection. Hepatology. 2008;48(3):713–22. Epub 2008/08/21. doi: 10.1002/hep.2237918712791
19. Miles JJ, Thammanichanond D, Moneer S, Nivarthi UK, Kjer-Nielsen L, Tracy SL, et al. Antigen-driven patterns of TCR bias are shared across diverse outcomes of human hepatitis C virus infection. J Immunol. 2011;186(2):901–12. Epub 2010/12/17. doi: 10.4049/jimmunol.100316721160049
20. Wolfl M, Rutebemberwa A, Mosbruger T, Mao Q, Li HM, Netski D, et al. Hepatitis C virus immune escape via exploitation of a hole in the T cell repertoire. J Immunol. 2008;181(9):6435–46. Epub 2008/10/23. PubMed Central PMCID: PMC2742502. 18941234
21. Ramalingam RK, Meyer-Olson D, Shoukry NH, Bowen DG, Walker CM, Kalams SA, Kinetic analysis by real-time PCR of hepatitis C virus (HCV)-specific T cells in peripheral blood and liver after challenge with HCV. J Virol. 2008;82(21):10487–92. PubMed Central PMCID: PMC2573177. doi: 10.1128/JVI.00588-0818715926
22. Blattman JN, Sourdive DJ, Murali-Krishna K, Ahmed R, Altman JD, Evolution of the T cell repertoire during primary, memory, and recall responses to viral infection. J Immunol. 2000;165(11):6081–90. Epub 2000/11/22. 11086040
23. Abdel-Hakeem MS, Bedard N, Murphy D, Bruneau J, Shoukry NH, Signatures of protective memory immune responses during hepatitis C virus reinfection. Gastroenterology. 2014;147(4):870–81.e8. Epub 2014/07/20. PubMed Central PMCID: PMCPmc4170061. doi: 10.1053/j.gastro.2014.07.00525038432
24. Simpson EH, Measurement of Diversity. Nature. 1949;163:688-.
25. Venturi V, Kedzierska K, Turner SJ, Doherty PC, Davenport MP, Methods for comparing the diversity of samples of the T cell receptor repertoire. J Immunol Methods. 2007;321(1–2):182–95. Epub 2007/03/06. doi: 10.1016/j.jim.2007.01.01917337271
26. Magurran AE, Measuring richness and evenness. Trends in ecology & evolution. 1998;13(4):165–6. Epub 1998/04/01.
27. Venturi V, Kedzierska K, Tanaka MM, Turner SJ, Doherty PC, Davenport MP, Method for assessing the similarity between subsets of the T cell receptor repertoire. J Immunol Methods. 2008;329(1–2):67–80. Epub 2007/11/16. doi: 10.1016/j.jim.2007.09.01618001765
28. Yu X, Almeida JR, Darko S, van der Burg M, DeRavin SS, Malech H, et al. Human syndromes of immunodeficiency and dysregulation are characterized by distinct defects in T-cell receptor repertoire development. J Allergy Clin Immunol. 2014;133(4):1109–15. Epub 2014/01/11. PubMed Central PMCID: PMCPMC3972286. doi: 10.1016/j.jaci.2013.11.01824406074
29. Appay V, Iglesias MC, Antigen sensitivity and T-cell receptor avidity as critical determinants of HIV control. Curr Opin HIV AIDS. 2011;6(3):157–62. Epub 2011/03/15. doi: 10.1097/COH.0b013e3283453dfd21399498
30. Lissina A, Fastenackels S, Inglesias MC, Ladell K, McLaren JE, Briceno O, et al. The link between CD8(+) T-cell antigen-sensitivity and HIV-suppressive capacity depends on HLA restriction, target epitope and viral isolate. AIDS. 2014;28(4):477–86. Epub 2014/01/05. doi: 10.1097/QAD.000000000000017524384691
31. Larsen M, Sauce D, Arnaud L, Fastenackels S, Appay V, Gorochov G, Evaluating cellular polyfunctionality with a novel polyfunctionality index. PLoS One. 2012;7(7):e42403. Epub 2012/08/04. PubMed Central PMCID: PMCPMC3408490. doi: 10.1371/journal.pone.004240322860124
32. Badr G, Bedard N, Abdel-Hakeem MS, Trautmann L, Willems B, Villeneuve JP, et al. Early interferon therapy for hepatitis C virus infection rescues polyfunctional, long-lived CD8+ memory T cells. J Virol. 2008;82(20):10017–31. Epub 2008/08/01. doi: 10.1128/JVI.01083-0818667516
33. Ciuffreda D, Comte D, Cavassini M, Giostra E, Buhler L, Perruchoud M, et al. Polyfunctional HCV-specific T-cell responses are associated with effective control of HCV replication. Eur J Immunol. 2008;38(10):2665–77. Epub 2008/10/30. doi: 10.1002/eji.20083833618958874
34. Sourdive DJ, Murali-Krishna K, Altman JD, Zajac AJ, Whitmire JK, Pannetier C, et al. Conserved T cell receptor repertoire in primary and memory CD8 T cell responses to an acute viral infection. J Exp Med. 1998;188(1):71–82. 9653085
35. Wedemeyer H, Mizukoshi E, Davis AR, Bennink JR, Rehermann B, Cross-reactivity between hepatitis C virus and Influenza A virus determinant-specific cytotoxic T cells. J Virol. 2001;75(23):11392–400. doi: 10.1128/JVI.75.23.11392-11400.200111689620
36. Urbani S, Amadei B, Fisicaro P, Pilli M, Missale G, Bertoletti A, et al. Heterologous T cell immunity in severe hepatitis C virus infection. J Exp Med. 2005;201(5):675–80. Epub 2005/03/09. PubMed Central PMCID: PMCPMC2212827. doi: 10.1084/jem.2004105815753202
37. Kasprowicz V, Ward SM, Turner A, Grammatikos A, Nolan BE, Lewis-Ximines L, et al. Defining the directionality and quality of influenza virus-specific CD8 T cell cross-reactivity in individuals infected with hepatitis C virus. J Clin Invest. 2008. Epub 2008/02/05.
38. Zhang S, Bakshi RK, Suneetha PV, Fytili P, Antunes DA, Vieira GF, et al. Frequency, Private Specificity, and Cross-Reactivity of Preexisting Hepatitis C Virus (HCV)-Specific CD8+ T Cells in HCV-Seronegative Individuals: Implications for Vaccine Responses. J Virol. 2015;89(16):8304–17. Epub 2015/06/05. PubMed Central PMCID: PMCPMC4524240. doi: 10.1128/JVI.00539-1526041301
39. Berger CT, Frahm N, Price DA, Mothe B, Ghebremichael M, Hartman KL, et al. High-functional-avidity cytotoxic T lymphocyte responses to HLA-B-restricted Gag-derived epitopes associated with relative HIV control. J Virol. 2011;85(18):9334–45. Epub 2011/07/15. PubMed Central PMCID: PMC3165743. doi: 10.1128/JVI.00460-1121752903
40. Lissina A, Chakrabarti LA, Takiguchi M, Appay V, TCR clonotypes: molecular determinants of T-cell efficacy against HIV. Current opinion in virology. 2016;16:77–85. Epub 2016/02/15. doi: 10.1016/j.coviro.2016.01.01726874617
41. Utzschneider DT, Alfei F, Roelli P, Barras D, Chennupati V, Darbre S, et al. High antigen levels induce an exhausted phenotype in a chronic infection without impairing T cell expansion and survival. J Exp Med. 2016;213(9):1819–34. Epub 2016/07/28. doi: 10.1084/jem.2015059827455951
42. Campos-Lima PO, Levitsky V, Imreh MP, Gavioli R, Masucci MG, Epitope-dependent selection of highly restricted or diverse T cell receptor repertoires in response to persistent infection by Epstein-Barr virus. J Exp Med. 1997;186(1):83–9. Epub 1997/07/07. PubMed Central PMCID: PMCPMC2198955. 9207000
43. Cukalac T, Chadderton J, Handel A, Doherty PC, Turner SJ, Thomas PG, et al. Reproducible selection of high avidity CD8+ T-cell clones following secondary acute virus infection. Proc Natl Acad Sci U S A. 2014;111(4):1485–90. Epub 2014/01/30. PubMed Central PMCID: PMCPMC3910643. doi: 10.1073/pnas.132373611124474775
44. Benati D, Galperin M, Lambotte O, Gras S, Lim A, Mukhopadhyay M, et al. Public T cell receptors confer high-avidity CD4 responses to HIV controllers. J Clin Invest. 2016;126(6):2093–108. Epub 2016/04/26. PubMed Central PMCID: PMCPMC4887161. doi: 10.1172/JCI8379227111229
45. Boyd A, Almeida JR, Darrah PA, Sauce D, Seder RA, Appay V, et al. Pathogen-Specific T Cell Polyfunctionality Is a Correlate of T Cell Efficacy and Immune Protection. PloS one. 2015;10(6):e0128714. PubMed Central PMCID: PMC4457486. doi: 10.1371/journal.pone.012871426046523
46. Tilg H, Wilmer A, Vogel W, Herold M, Nolchen B, Judmaier G, et al. Serum levels of cytokines in chronic liver diseases. Gastroenterology. 1992;103(1):264–74. Epub 1992/07/01. 1612333
47. Park J, Kang W, Ryu SW, Kim WI, Chang DY, Lee DH, et al. Hepatitis C virus infection enhances TNFalpha-induced cell death via suppression of NF-kappaB. Hepatology. 2012;56(3):831–40. Epub 2012/03/21. doi: 10.1002/hep.2572622430873
48. Ando K, Hiroishi K, Kaneko T, Moriyama T, Muto Y, Kayagaki N, et al. Perforin, Fas/Fas ligand, and TNF-alpha pathways as specific and bystander killing mechanisms of hepatitis C virus-specific human CTL. J Immunol. 1997;158(11):5283–91. Epub 1997/06/01. 9164947
49. Osburn WO, Fisher BE, Dowd KA, Urban G, Liu L, Ray SC, et al. Spontaneous control of primary hepatitis C virus infection and immunity against persistent reinfection. Gastroenterology. 2010;138(1):315–24. Epub 2009/09/29. doi: 10.1053/j.gastro.2009.09.01719782080
50. Boisvert M, Zhang W, Elrod EJ, Bernard NF, Villeneuve JP, Bruneau J, et al. Novel E2 Glycoprotein Tetramer Detects Hepatitis C Virus-Specific Memory B Cells. J Immunol. 2016;197(12):4848–58. Epub 2016/11/17. PubMed Central PMCID: PMCPMC5136319. doi: 10.4049/jimmunol.160076327849172
51. Grebely J, Morris MD, Rice TM, Bruneau J, Cox AL, Kim AY, et al. Cohort profile: the International Collaboration of Incident HIV and Hepatitis C in Injecting Cohorts (InC3) Study. Int J Epidemiol. 2013;42(6):1649–59. PubMed Central PMCID: PMC3887561. doi: 10.1093/ije/dys16723203695
52. Mariani S, Hwang SY, Foglietta M, Bonello L, Vitale C, Coscia M, et al. Comprehensive assessment of the TCRBV repertoire in small T-cell samples by means of an improved and convenient multiplex PCR method. Experimental hematology. 2009;37(6):728–38. Epub 2009/05/26. doi: 10.1016/j.exphem.2009.03.00319463773
53. Carlson CS, Emerson RO, Sherwood AM, Desmarais C, Chung MW, Parsons JM, et al. Using synthetic templates to design an unbiased multiplex PCR assay. Nature communications. 2013;4:2680. Epub 2013/10/26. doi: 10.1038/ncomms368024157944
54. Roederer M, Nozzi JL, Nason MC, SPICE: exploration and analysis of post-cytometric complex multivariate datasets. Cytometry A. 2011;79(2):167–74. Epub 2011/01/26. PubMed Central PMCID: PMC3072288. doi: 10.1002/cyto.a.2101521265010