Negative selection by an endogenous retrovirus promotes a higher-avidity CD4+ T cell response to retroviral infection

PLoS Pathogens

Volumn 8, Issue 5, 2012, Pages

  Young, George R ^a   Ploquin, Mickaël J Y ^a,b   Eksmond, Urszula ^a   Wadwa, Munisch ^a,c   Stoye, Jonathan P ^a   Kassiotis, George ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b INSTITUT PASTEUR   (France)

^c UNIVERSITY OF DUISBURG ESSEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; T LYMPHOCYTE RECEPTOR; LYMPHOCYTE ANTIGEN RECEPTOR; VIRUS ENVELOPE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIVIRAL ACTIVITY; ARTICLE; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CROSS REACTION; FRIEND LEUKEMIA VIRUS; MOLECULAR CLONING; MOUSE; NONHUMAN; PROTEIN EXPRESSION; RETROVIRUS; RETROVIRUS INFECTION; VIRUS REPLICATION; A J MOUSE; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; ENDOGENOUS RETROVIRUS; HUMAN; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM;

FRIEND MURINE LEUKEMIA VIRUS; MUS;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; ENDOGENOUS RETROVIRUSES; FRIEND MURINE LEUKEMIA VIRUS; GENE PRODUCTS, ENV; HUMANS; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED A; MICE, INBRED C57BL; RECEPTORS, ANTIGEN, T-CELL; RETROVIRIDAE INFECTIONS;

EID: 84863636728     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002709     Document Type: Article

References (65)

1. Hasenkrug KJ, Chesebro B, (1997) Immunity to retroviral infection: The Friend virus model. Proc Natl Acad Sci U S A 94: 7811-7816.
2. Miyazawa M, Tsuji-Kawahara S, Kanari Y, (2008) Host genetic factors that control immune responses to retrovirus infections. Vaccine 26: 2981-2996.
3. McMichael AJ, Borrow P, Tomaras GD, Goonetilleke N, Haynes BF, (2010) The immune response during acute HIV-1 infection: clues for vaccine development. Nat Rev Immunol 10: 11-23.
4. Handunnetthi L, Ramagopalan SV, Ebers GC, Knight JC, (2010) Regulation of major histocompatibility complex class II gene expression, genetic variation and disease. Genes Immun 11: 99-112.
5. Kosmrlj A, Read EL, Qi Y, Allen TM, Altfeld M, et al. (2010) Effects of thymic selection of the T-cell repertoire on HLA class I-associated control of HIV infection. Nature 465: 350-354.
6. The International HIV Controllers Study (2010) The Major Genetic Determinants of HIV-1 Control Affect HLA Class I Peptide Presentation. Science 330: 1551-1557.
7. Berger CT, Frahm N, Price DA, Mothe B, Ghebremichael M, et al. (2011) High-Functional-Avidity Cytotoxic T Lymphocyte Responses to HLA-B-Restricted Gag-Derived Epitopes Associated with Relative HIV Control. J Virol 85: 9334-9345.
8. Iglesias MC, Almeida JR, Fastenackels Sn, van Bockel DJ, Hashimoto M, et al. (2011) Escape from highly effective public CD8+ T-cell clonotypes by HIV. Blood 118: 2138-2149.
9. Price DA, Asher TE, Wilson NA, Nason MC, Brenchley JM, et al. (2009) Public clonotype usage identifies protective Gag-specific CD8+ T cell responses in SIV infection. J Exp Med 206: 923-936.
10. Turner SJ, Doherty PC, McCluskey J, Rossjohn J, (2006) Structural determinants of T-cell receptor bias in immunity. Nat Rev Immunol 6: 883-894.
11. Bridgeman JS, Sewell AK, Miles JJ, Price DA, Cole DK, (2011) Structural and biophysical determinants of alphabeta T-cell antigen recognition. Immunology 135: 9-18.
12. Davenport MP, Price DA, McMichael AJ, (2007) The T cell repertoire in infection and vaccination: implications for control of persistent viruses. Curr Opin Immunol 19: 294-300.
13. Welsh RM, Che JW, Brehm MA, Selin LK, (2010) Heterologous immunity between viruses. Immunol Rev 235: 244-266.
14. Antunes I, Tolaini M, Kissenpfennig A, Iwashiro M, Kuribayashi K, et al. (2008) Retrovirus-specificity of regulatory T cells is neither present nor required in preventing retrovirus-induced bone marrow immune pathology. Immunity 29: 782-794.
15. Ploquin MJ, Eksmond U, Kassiotis G, (2011) B cells and TCR avidity determine distinct functions of CD4+ T cells in retroviral infection. J Immunol 187: 3321-3330.
16. Shimizu T, Uenishi H, Teramura Y, Iwashiro M, Kuribayashi K, et al. (1994) Fine structure of a virus-encoded helper T-cell epitope expressed on FBL-3 tumor cells. J Virol 68: 7704-7708.
17. Carson RT, Vignali KM, Woodland DL, Vignali DA, (1997) T cell receptor recognition of MHC class II-bound peptide flanking residues enhances immunogenicity and results in altered TCR V region usage. Immunity 7: 387-399.
18. Rudensky AY, Preston-Hurlburt P, Hong SC, Barlow A, Janeway CA Jr, (1991) Sequence analysis of peptides bound to MHC class II molecules. Nature 353: 622-627.
19. Sim BC, Wung JL, Gascoigne NRJ, (1998) Polymorphism within a TCRAV family influences the repertoire through Class I/II restriction. J Immunol 160: 1204-1211.
20. Robertson SJ, Ammann CG, Messer RJ, Carmody AB, Myers L, et al. (2008) Suppression of acute anti-friend virus CD8+ T-cell responses by coinfection with lactate dehydrogenase-elevating virus. J Virol 82: 408-418.
21. Nair SR, Zelinskyy G, Schimmer S, Gerlach N, Kassiotis G, et al. (2010) Mechanisms of control of acute Friend virus infection by CD4+ T helper cells and their functional impairment by regulatory T cells. J Gen Virol 91: 440-451.
22. Schepers K, Toebes M, Sotthewes G, Vyth-Dreese FA, Dellemijn TA, et al. (2002) Differential kinetics of antigen-specific CD4+ and CD8+ T cell responses in the regression of retrovirus-induced sarcomas. J Immunol 169: 3191-3199.
23. Pike R, Filby A, Ploquin MJ, Eksmond U, Marques R, et al. (2009) Race between retroviral spread and CD4+ T-cell response determines the outcome of acute Friend virus infection. J Virol 83: 11211-11222.
24. King SR, Berson BJ, Risser R, (1988) Mechanism of interaction between endogenous ecotropic murine leukemia viruses in (BALB/c X C57BL/6) hybrid cells. Virology 162: 1-11.
25. Marques R, Antunes I, Eksmond U, Stoye J, Hasenkrug K, et al. (2008) B lymphocyte activation by coinfection prevents immune control of friend virus infection. J Immunol 181: 3432-3440.
26. Green WR, (1999) Cytotoxic T lymphocytes to endogenous mouse retroviruses and mechanisms of retroviral escape. Immunol Rev 168: 271-286.
27. Ruan KS, Lilly F, (1991) Identification of an epitope encoded in the env gene of Friend murine leukemia virus recognized by anti-Friend virus cytotoxic T lymphocytes. Virology 181: 91-100.
28. Chen W, Qin H, Chesebro B, Cheever MA, (1996) Identification of a gag-encoded cytotoxic T-lymphocyte epitope from FBL- 3 leukemia shared by Friend, Moloney, and Rauscher murine leukemia virus-induced tumors. J Virol 70: 7773-7782.
29. Brawand P, Biasi G, Horvath C, Cerottini JC, MacDonald HR, (1998) Flow-Microfluorometric Monitoring of Oligoclonal CD8+ T Cell Responses to an Immunodominant Moloney Leukemia Virus-Encoded Epitope In Vivo. J Immunol 160: 1659-1665.
30. Hasenkrug KJ, Brooks DM, Dittmer U, (1998) Critical Role for CD4+ T Cells in Controlling Retrovirus Replication and Spread in Persistently Infected Mice. J Virol 72: 6559-6564.
31. Iwanami N, Niwa A, Yasutomi Y, Tabata N, Miyazawa M, (2001) Role of natural killer cells in resistance against friend retrovirus-induced leukemia. J Virol 75: 3152-3163.
32. Goff SP, (2004) Retrovirus Restriction Factors. Molecular Cell 16: 849-859.
33. Nethe M, Berkhout B, van der Kuyl AC, (2005) Retroviral superinfection resistance. Retrovirology 2: 52.
34. Lowy DR, Chattopadhyay SK, Teich NM, Rowe WP, Levine AS, (1974) AKR murine leukemia virus genome: frequency of sequences in DNA of high-, low-, and non-virus-yielding mouse strains. Proc Natl Acad Sci U S A 71: 3555-3559.
35. Chattopadhyay SK, Lander MR, Rands E, Lowy DR, (1980) Structure of endogenous murine leukemia virus DNA in mouse genomes. Proc Natl Acad Sci U S A 77: 5774-5778.
36. Jenkins MK, Chu HH, McLachlan JB, Moon JJ, (2010) On the composition of the preimmune repertoire of T cells specific for Peptide-major histocompatibility complex ligands. Annu Rev Immunol 28: 275-294.
37. Huseby ES, Crawford F, White J, Kappler J, Marrack P, (2003) Negative selection imparts peptide specificity to the mature T cell repertoire. Proc Natl Acad Sci U S A 100: 11565-11570.
38. Virgin HW, Walker BD, (2010) Immunology and the elusive AIDS vaccine. Nature 464: 224-231.
39. Chevalier MF, Julg B, Pyo A, Flanders M, Ranasinghe S, et al. (2011) HIV-1-Specific Interleukin-21+ CD4+ T Cell Responses Contribute to Durable Viral Control through the Modulation of HIV-Specific CD8+ T Cell Function. J Virol 85: 733-741.
40. Yue FY, Lo C, Sakhdari A, Lee EY, Kovacs CM, et al. (2010) HIV-Specific IL-21 Producing CD4+ T Cells Are Induced in Acute and Chronic Progressive HIV Infection and Are Associated with Relative Viral Control. J Immunol 185: 498-506.
41. Vingert B, Perez-Patrigeon S, Jeannin P, Lambotte O, Boufassa F, et al. (2010) HIV controller CD4+ T cells respond to minimal amounts of gag antigen due to high TCR avidity. PLoS Pathog 6: e1000780.
42. Ortiz AM, Klatt NR, Li B, Yi Y, Tabb B, et al. (2011) Depletion of CD4+ T cells abrogates post-peak decline of viremia in SIV-infected rhesus macaques. J Clin Invest 121: 4433-4445.
43. Portis JL, (1994) Endogenous retroviral envelope antigens recognized by B lymphocytes during graft-versus-host reaction. Tohoku J Exp Med 173: 83-89.
44. Gras S, Chen Z, Miles JJ, Liu YC, Bell MJ, et al. (2010) Allelic polymorphism in the T cell receptor and its impact on immune responses. J Exp Med 207: 1555-1567.
45. Kjer-Nielsen L, Clements CS, Purcell AW, Brooks AG, Whisstock JC, et al. (2003) A structural basis for the selection of dominant alphabeta T cell receptors in antiviral immunity. Immunity 18: 53-64.
46. Sabatino JJ Jr, Huang J, Zhu C, Evavold BD, (2011) High prevalence of low affinity peptide-MHC II tetramer-negative effectors during polyclonal CD4+ T cell responses. J Exp Med 208: 81-90.
47. Munitic I, Decaluwe H, Evaristo C, Lemos S, Wlodarczyk M, et al. (2009) Epitope specificity and relative clonal abundance do not affect CD8 differentiation patterns during lymphocytic choriomeningitis virus infection. J Virol 83: 11795-11807.
48. Ebert PJR, Jiang S, Xie J, Li QJ, Davis MM, (2009) An endogenous positively selecting peptide enhances mature T cell responses and becomes an autoantigen in the absence of microRNA miR-181a. Nat Immunol 10: 1162-1169.
49. Pothlichet J, Mangeney M, Heidmann T, (2006) Mobility and integration sites of a murine C57BL/6 melanoma endogenous retrovirus involved in tumor progression in vivo. Int J Cancer 119: 1869-1877.
50. Stoye JP, (1999) The pathogenic potential of endogenous retroviruses: a sceptical view. Trends Microbiol 7: 430.
51. Baudino L, Yoshinobu K, Morito N, Santiago-Raber ML, Izui S, (2010) Role of endogenous retroviruses in murine SLE. Autoimmun Rev 10: 27-34.
52. Nakagawa K, Harrison LC, (1996) The potential roles of endogenous retroviruses in autoimmunity. Immunol Rev pp. 193-236.
53. Christensen T, (2005) Association of human endogenous retroviruses with multiple sclerosis and possible interactions with herpes viruses. Rev Med Virol 15: 179-211.
54. Perl A, Nagy G, Koncz A, Gergely P, Fernandez D, et al. (2008) Molecular mimicry and immunomodulation by the HRES-1 endogenous retrovirus in SLE. Autoimmunity 41: 287-297.
55. Kleiman A, Senyuta N, Tryakin A, Sauter M, Karseladze A, et al. (2004) HERV-K(HML-2) GAG/ENV antibodies as indicator for therapy effect in patients with germ cell tumors. Int J Cancer 110: 459-461.
56. Humer J, Waltenberger A, Grassauer A, Kurz M, Valencak J, et al. (2006) Identification of a melanoma marker derived from melanoma-associated endogenous retroviruses. Cancer Res 66: 1658-1663.
57. Contreras-Galindo R, Kaplan MH, Markovitz DM, Lorenzo E, Yamamura Y, (2006) Detection of HERV-K(HML-2) viral RNA in plasma of HIV type 1-infected individuals. AIDS Res Hum Retroviruses 22: 979-984.
58. Garrison KE, Jones RB, Meiklejohn DA, Anwar N, Ndhlovu LC, et al. (2007) T Cell Responses to Human Endogenous Retroviruses in HIV-1 Infection. PLoS Pathog 3: e165.
59. Fellay J, Shianna KV, Ge D, Colombo S, Ledergerber B, et al. (2007) A Whole-Genome Association Study of Major Determinants for Host Control of HIV-1. Science 317: 944-947.
60. Takahashi Y, Harashima N, Kajigaya S, Yokoyama H, Cherkasova E, et al. (2008) Regression of human kidney cancer following allogeneic stem cell transplantation is associated with recognition of an HERV-E antigen by T cells. J Clin Invest 118: 1099-1109.
61. Mombaerts P, Iacomini J, Johnson RS, Herrup K, Tonegawa S, et al. (1992) RAG-1-deficient mice have no mature B and T lymphocytes. Cell 68: 869-877.
62. Philpott KL, Viney JL, Kay G, Rastan S, Gardiner EM, et al. (1992) Lymphoid development in mice congenitally lacking T cell receptor alpha beta-expressing cells. Science 256: 1448-1452.
63. Casanova JL, Romero P, Widmann C, Kourilsky P, Maryanski JL, (1991) T cell receptor genes in a series of class I major histocompatibility complex-restricted cytotoxic T lymphocyte clones specific for a Plasmodium berghei nonapeptide: implications for T cell allelic exclusion and antigen-specific repertoire. J Exp Med 174: 1371-1383.
64. Martin RM, Brady JL, Lew AM, (1998) The need for IgG2c specific antiserum when isotyping antibodies from C57BL/6 and NOD mice. J Immunol Methods 212: 187-192.
65. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.