Protective Efficacy of Serially Up-Ranked Subdominant CD8 T Cell Epitopes against Virus Challenges

English version České info

Immunodominance in T cell responses to complex antigens like viruses is still incompletely understood. Some data indicate that the dominant responses to viruses are not necessarily the most protective, while other data imply that dominant responses are the most important. The issue is of considerable importance to the rational design of vaccines, particularly against variable escaping viruses like human immunodeficiency virus type 1 and hepatitis C virus. Here, we showed that sequential inactivation of dominant epitopes up-ranks the remaining subdominant determinants. Importantly, we demonstrated that subdominant epitopes can induce robust responses and protect against whole viruses if they are allowed at least once in the vaccination regimen to locally or temporally dominate T cell induction. Therefore, refocusing T cell immune responses away from highly variable determinants recognized during natural virus infection towards subdominant, but conserved regions is possible and merits evaluation in humans.

Vyšlo v časopise: Protective Efficacy of Serially Up-Ranked Subdominant CD8 T Cell Epitopes against Virus Challenges. PLoS Pathog 7(5): e32767. doi:10.1371/journal.ppat.1002041
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002041

Souhrn

Zdroje

1. YewdellJW 2006 Confronting complexity: real-world immunodominance in antiviral CD8+ T cell responses. Immunity 25 533 543

2. BrehmMAPintoAKDanielsKASchneckJPWelshRM 2002 T cell immunodominance and maintenance of memory regulated by unexpectedly cross-reactive pathogens. Nat Immunol 3 627 634

3. MoAXvan LelyveldSFCraiuARockKL 2000 Sequences that flank subdominant and cryptic epitopes influence the proteolytic generation of MHC class I-presented peptides. J Immunol 164 4003 4010

4. ProbstHCTschannenKGallimoreAMartinicMBaslerM 2003 Immunodominance of an antiviral cytotoxic T cell response is shaped by the kinetics of viral protein expression. J Immunol 171 5415 5422

5. van der MostRGMurali-KrishnaKLanierJGWherryEJPuglielliMT 2003 Changing immunodominance patterns in antiviral CD8 T-cell responses after loss of epitope presentation or chronic antigenic stimulation. Virology 315 93 102

6. YewdellJWBenninkJR 1999 Immunodominance in major histocompatibility complex class I-restricted T lymphocyte responses. Annu Rev Immunol 17 51 88

7. GaschenBTaylorJYusimKFoleyBGaoF 2002 Diversity considerations in HIV-1 vaccine selection. Science 296 2354 2360

8. BarouchDHKunstmanJKurodaMJSchmitzJESantraS 2002 Eventual AIDS vaccine failure in a rhesus monkey by viral escape from cytotoxic T lymphocytes. Nature 415 335 339

9. GoonetillekeNLiuMKSalazar-GonzalezJFFerrariGGiorgiE 2009 The first T cell response to transmitted/founder virus contributes to the control of acute viremia in HIV-1 infection. J Exp Med 206 1253 1272

10. GoulderPJWatkinsDI 2004 HIV and SIV CTL escape: implications for vaccine design. Nat Rev Immunol 4 630 640

11. MooreCBJohnMJamesIRChristiansenFTWittCS 2002 Evidence of HIV-1 adaptation to HLA-restricted immune responses at a population level. Science 296 1439 1443

12. FrahmNKiepielaPAdamsSLindeCHHewittHS 2006 Control of human immunodeficiency virus replication by cytotoxic T lymphocytes targeting subdominant epitopes. Nat Immunol 7 173 178

13. GallimoreADumreseTHengartnerHZinkernagelRMRammenseeHG 1998 Protective immunity does not correlate with the hierarchy of virus-specific cytotoxic T cell responses to naturally processed peptides. J Exp Med 187 1647 1657

14. LiuJEwaldBALynchDMNandaASumidaSM 2006 Modulation of DNA vaccine-elicited CD8+ T-lymphocyte epitope immunodominance hierarchies. J Virol 80 11991 11997

15. RodriguezFSlifkaMKHarkinsSWhittonJL 2001 Two overlapping subdominant epitopes identified by DNA immunization induce protective CD8(+) T-cell populations with differing cytolytic activities. J Virol 75 7399 7409

16. van der MostRGConcepcionRJOseroffCAlexanderJSouthwoodS 1997 Uncovering subdominant cytotoxic T-lymphocyte responses in lymphocytic choriomeningitis virus-infected BALB/c mice. J Virol 71 5110 5114

17. von HerrathMGDockterJNerenbergMGairinJEOldstoneMB 1994 Thymic selection and adaptability of cytotoxic T lymphocyte responses in transgenic mice expressing a viral protein in the thymus. J Exp Med 180 1901 1910

18. McMichaelAJHankeT 2003 HIV vaccines 1983-2003. Nat Med 9 874 880

19. BridgemanARoshormYLockettLJXuZZHopkinsR 2010 Ovine atadenovirus, a novel and highly immunogenic vector in prime-boost studies of a candidate HIV-1 vaccine. Vaccine 28 474 483

20. ImEJSaubiNVirgiliGSanderCTeohD 2007 Vaccine platform for prevention of tuberculosis and mother-to-child transmission of human immunodeficiency virus type 1 through breastfeeding. J Virol 81 9408 9418

21. NitkiewiczJChaoWBentsmanGLiJKimSY 2004 Productive infection of primary murine astrocytes, lymphocytes, and macrophages by human immunodeficiency virus type 1 in culture. J Neurovirol 10 400 408

22. PotashMJChaoWBentsmanGParisNSainiM 2005 A mouse model for study of systemic HIV-1 infection, antiviral immune responses, and neuroinvasiveness. Proc Natl Acad Sci U S A 102 3760 3765

23. RoshormYHongJPKobayashiNMcMichaelAJVolskyDJ 2009 Novel HIV-1 clade B candidate vaccines designed for HLA-B*5101+ patients protected mice against chimaeric EcoHIV challenge. Eur J Immunol 39 1831 1840

24. HankeTMcMichaelAJ 2000 Design and construction of an experimental HIV-1 vaccine for a year-2000 clinical trial in Kenya. Nat Med 6 951 955

25. ImEJHankeT 2007 Short communication: preclinical evaluation of candidate HIV type 1 vaccines in inbred strains and an outbred stock of mice. AIDS Res Hum Retroviruses 23 857 862

26. LarkeNImE-JWagnerRWilliamsonCWilliamsonA-L 2007 Combined single-clade candidate HIV-1 vaccines induce T cell responses limited by multiple forms of in vivo immune interference. Eur J Immunol 37 566 577

27. LiuYMcNevinJRollandMZhaoHDengW 2009 Conserved HIV-1 epitopes continuously elicit subdominant cytotoxic T-lymphocyte responses. J Infect Dis 200 1825 1833

28. LetourneauSImE-JMashishiTBreretonCBridgemanA 2007 Design and pre-clinical evaluation of a universal HIV-1 vaccine. PLoS ONE 2 e984

29. RosarioMBridgemanAQuakkelaarEDQuigleyMFHillBJ 2010 Long peptides induce polyfunctional T cells against conserved regions of HIV-1 with superior breadth to single-gene vaccines in macaques. Eur J Immunol 40 1973 1984

30. HankeTGoonetillekeNMcMichaelAJDorrellL 2007 Clinical experience with plasmid DNA- and modified vaccinia vaccine Ankara (MVA)-vectored HIV-1 clade A vaccine inducing T cells. J Gen Virol 88 1 12

31. TakahashiHCohenJHosmalinACeaseKBHoughtenR 1988 An immunodominant epitope of the human immunodeficiency virus envelope glycoprotein gp160 recognized by class I major histocompatibility molecule-restricted murine cytotoxic T lymphocytes. Proc Natl Acad Sci USA 85 3105 3109

32. HankeTSchneiderJGilbertSCHillAVSMcMichaelA 1998 DNA multi-CTL epitope vaccines for HIV and Plasmodium falciparum: Immunogenicity in mice. Vaccine 16 426 435

33. NakagawaYKikuchiHTakahashiH 2007 Molecular analysis of TCR and peptide/MHC interaction using P18-I10-derived peptides with a single D-amino acid substitution. Biophys J 92 2570 2582

34. MataMTraversPJLiuQFrankelFRPatersonY 1998 The MHC class I-restricted immune response to HIV-gag in BALB/c mice selects a single epitope that does not have a predictable MHC-binding motif and binds to Kd through interactions between a glutamine at P3 and pocket D. J Immunol 161 2985 2993

35. DidierlaurentARamirezJCGherardiMZimmerliSCGrafM 2004 Attenuated poxviruses expressing a synthetic HIV protein stimulate HLA-A2-restricted cytotoxic T-cell responses. Vaccine 22 3395 3403

36. MwauMMcMichaelAJHankeT 2002 Design and Validation of an ELISPOT Assay for Use in Clinical Trials of Candidate HIV Vaccines. AIDS Res Hum Retroviruses 18 611 618

37. ShastriNSerwoldTGonzalezF 1995 Presentation of endogenous peptide/MHC class I complexes is profoundly influenced by specific C-terminal flanking residues. J Immunol 155 4339 4346

38. BettsMRBrenchleyJMPriceDADe RosaSCDouekDC 2003 Sensitive and viable identification of antigen-specific CD8+ T cells by a flow cytometric assay for degranulation. J Immunol Methods 281 65 78

39. SchulzODieboldSSChenMNaslundTINolteMA 2005 Toll-like receptor 3 promotes cross-priming to virus-infected cells. Nature 433 887 892

40. HarringtonLEMost RvRWhittonJLAhmedR 2002 Recombinant vaccinia virus-induced T-cell immunity: quantitation of the response to the virus vector and the foreign epitope. J Virol 76 3329 3337

41. TscharkeDCWooWPSakalaIGSidneyJSetteA 2006 Poxvirus CD8+ T-cell determinants and cross-reactivity in BALB/c mice. J Virol 80 6318 6323

42. HankeTBarnfieldCWeeEG-TÅgrenLSamuelRV 2003 Construction and immunogenicity in a prime-boost regimen of a Semliki Forest virus-vectored experimental HIV clade A vaccine. J Gen Virol 84 361 368

43. RollandMNickleDCMullinsJI 2007 HIV-1 group M conserved elements vaccine. PLoS Pathog 3 e157

44. ZajacAJBlattmanJNMurali-KrishnaKSourdiveDJSureshM 1998 Viral Immune evasion due to persistence of activated T cells without effector function. J Exp Med 188 2205 2213

45. AltfeldMAddoMMRosenbergESHechtFMLeePK 2003 Influence of HLA-B57 on clinical presentation and viral control during acute HIV-1 infection. AIDS 17 2581 2591

46. KelleherADLongCHolmesECAllenRLWilsonJ 2001 Clustered mutations in HIV-1 gag are consistently required for escape from HLA-B27-restricted cytotoxic T lymphocyte responses. J Exp Med 193 375 386

47. GoulderPJAltfeldMARosenbergESNguyenTTangY 2001 Substantial differences in specificity of HIV-specific cytotoxic T cells in acute and chronic HIV infection. J Exp Med 193 181 194

48. McMichaelAJBorrowPTomarasGDGoonetillekeNHaynesBF 2010 The immune response during acute HIV-1 infection: clues for vaccine development. Nat Rev Immunol 10 11 23

49. PriceDAGoulderPJKlenermanPSewellAKEasterbrookPJ 1997 Positive selection of HIV-1 cytotoxic T lymphocyte escape variants during primary infection. Proc Natl Acad Sci USA 94 1890 1895

50. WalkerBDGoulderPJ 2000 AIDS. Escape from the immune system. Nature 407 313 314

51. KastenmullerWGasteigerGGronauJHBaierRLjapociR 2007 Cross-competition of CD8+ T cells shapes the immunodominance hierarchy during boost vaccination. J Exp Med 204 2187 2198

52. BelzGTXieWAltmanJDDohertyPC 2000 A previously unrecognized H-2D(b)-restricted peptide prominent in the primary influenza A virus-specific CD8(+) T-cell response is much less apparent following secondary challenge. J Virol 74 3486 3493

53. ChenWPangKMastermanKAKennedyGBastaS 2004 Reversal in the immunodominance hierarchy in secondary CD8+ T cell responses to influenza A virus: roles for cross-presentation and lysis-independent immunodomination. J Immunol 173 5021 5027

54. NugentCTMcNallyJMChervenakRWolcottRMJenningsSR 1995 Differences in the recognition of CTL epitopes during primary and secondary responses to herpes simplex virus infection in vivo. Cell Immunol 165 55 64

55. HislopADTaylorGSSauceDRickinsonAB 2007 Cellular responses to viral infection in humans: Lessons from Epstein-Barr virus. Annu Rev Immunol 25 587 617

56. KedlRMSchaeferBCKapplerJWMarrackP 2002 T cells down-modulate peptide-MHC complexes on APCs in vivo. Nat Immunol 3 27 32

57. WillisRAKapplerJWMarrackPC 2006 CD8 T cell competition for dendritic cells in vivo is an early event in activation. Proc Natl Acad Sci U S A 103 12063 12068

58. PalmowskiMJChoiEMHermansIFGilbertSCChenJL 2002 Competition between CTL narrows the immune response induced by prime-boost vaccination protocols. J Immunol 168 4391 4398

59. YewdellJW 2010 Designing CD8+ T cell vaccines: it's not rocket science (yet). Curr Opin Immunol 22 402 410

60. LeslieAJPfafferottKJChettyPDraenertRAddoMM 2004 HIV evolution: CTL escape mutation and reversion after transmission. Nat Med 10 282 289

61. BennettMSNgHLAliAYangOO 2008 Cross-clade detection of HIV-1-specific cytotoxic T lymphocytes does not reflect cross-clade antiviral activity. J Infect Dis 197 390 397

62. D'SouzaMPAltfeldM 2008 Measuring HIV-1-specific T cell immunity: how valid are current assays? J Infect Dis 197 337 339

63. Le GallSStamegnaPWalkerBD 2007 Portable flanking sequences modulate CTL epitope processing. J Clin Invest 117 3563 3575

64. TenzerSWeeEBurgevinAStewart-JonesGFriisL 2009 Antigen processing influences HIV-specific cytotoxic T lymphocyte immunodominance. Nat Immunol 10 636 646

65. SchneiderJGilbertSCBlanchardTJHankeTRobsonKJ 1998 Enhanced immunogenicity for CD8+ T cell induction and complete protective efficacy of malaria DNA vaccination by boosting with modified vaccinia virus Ankara. Nature Med 4 397 402

66. SedlikCDadaglioGSaronMFDeriaudERojasM 2000 In vivo induction of a high-avidity, high-frequency cytotoxic T-lymphocyte response is associated with antiviral protective immunity. J Virol 74 5769 5775

67. ValentineLEWatkinsDI 2008 Relevance of studying T cell responses in SIV-infected rhesus macaques. Trends Microbiol 16 605 611

68. HermansIFSilkJDYangJPalmowskiMJGileadiU 2004 The VITAL assay: a versatile fluorometric technique for assessing CTL- and NKT-mediated cytotoxicity against multiple targets in vitro and in vivo. J Immunol Methods 285 25 40