Role of α3 domain of class I MHC molecules in the activation of high- and low-avidity CD8+ CTLs

International Immunology

Volumn 19, Issue 12, 2007, Pages 1413-1420

  Belyakov, Igor M ^a   Kozlowski, Steven ^b   Mage, Michael ^c   Ahlers, Jeffrey D ^a   Boyd, Lisa F ^c   Margulies, David H ^c   Berzofsky, Jay A ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

Avidity; Ccytotoxic T lymphocytes; Epitope; MHC class I; Peptide; TCR

Indexed keywords

GAMMA INTERFERON; GLUTAMIC ACID; LYSINE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; GLYCOPROTEIN GP 160; H 2KB PROTEIN, MOUSE; H-2KB PROTEIN, MOUSE; H2 ANTIGEN; HISTOCOMPATIBILITY ANTIGEN H 2D(B); HISTOCOMPATIBILITY ANTIGEN H-2D(B); MUTANT PROTEIN; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CD8+ T LYMPHOCYTE; CELL LINE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXIC T LYMPHOCYTE; IN VITRO STUDY; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; ANIMAL; BAGG ALBINO MOUSE; CHEMISTRY; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; PROTEIN TERTIARY STRUCTURE;

ANIMALS; CELL LINE; H-2 ANTIGENS; HIV ENVELOPE PROTEIN GP160; INTERFERON TYPE II; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; MUTANT PROTEINS; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; T-LYMPHOCYTES, CYTOTOXIC;

EID: 36248979205     PISSN: 09538178     EISSN: 14602377     Source Type: Journal    
DOI: 10.1093/intimm/dxm111     Document Type: Article

References (71)

1. Ahlers, J. D., Belyakov, I. M. and Berzofsky, J. A. 2003. Cytokine, chemokine and costimulatory molecule modulation to enhance efficacy of HIV vaccines. Curr. Mol. Med. 3:285.
2. Ahlers, J. D., Belyakov, I. M., Terabe, M. et al. 2002. A push-pull approach to maximize vaccine efficacy: Abrogating suppression with an IL-13 inhibitor while augmenting help with GM-CSF and CD40L. Proc. Natl Acad. Sci. USA 99:13020.
3. Ahlers, J. D., Belyakov, I. M., Thomas, E. K. and Berzofsky, J. A. 2001. High affinity T-helper epitope induces complementary helper and APC polarization, increased CTL and protection against viral infection. J. Clin. Invest. 108:1677.
4. Ahlers, J. D., Belyalkov, I. M., Matsui, S. and Berzofsky, J. A. 2001. Mechanisms of cytokine synergy essential for vaccine protection against viral challenge. Int. Immunol. 13:897.
5. Belyakov, I. M., Hammond, S. A., Ahlers, J. D., Glenn, G. M. and Berzofsky, J. A. 2004. Transcutaneous immunization induces mucosal CTL and protective immunity by migration of primed skin dendritic cells. J Clin. Invest. 113:998.
6. Kaech, S. M., Wherry, E. J. and Ahmed, R. 2002. Effector and memory T-cell differentiation: Implications for vaccine development. Nat. Rev. Immunol. 2:251.
7. Belyakov, I. M., Ahlers, J. D., Clements, J. D., Strober, W. and Berzofsky, J. A. 2000. Interplay of cytokines and adjuvants in the regulation of mucosal and systemic HIV-specific cytotoxic T lymphocytes. J. Immunol. 165:6454.
8. + T-cell approach feasible. Nat. Rev. Immunol. 2:283.
9. Belyakov, I. M., Derby, M. A., Ahlers, J. D. et al. 1998. Mucosal immunization with HIV-1 peptide vaccine induces mucosal and systemic cytotoxic T lymphocytes and protective immunity in mice against intrarectal recombinant HIV-vaccinia challenge. Proc. Natl Acad. Sci. USA 95:1709.
10. Belyakov, I. M., Ahlers, J. D., Brandwein, B. Y. et al. 1998. The importance of local mucosal HIV-specific CD8+ cytotoxic T lymphocytes for resistance to mucosal-viral transmission in mice and enhancement of resistance by local administration of IL-12. J Clin. Invest. 102:2072.
11. Samberg, N. L., Scarlett, E. C. and Stauss, H. J. 1989. The a3 domain of major histocompatibility complex class 1 molecules plays a critical role in cytotoxic T lymphocyte stimulation. Eur. J. Immunol. 19:2349.
12. Sabzevari, H., Kantor, J., Jaigirdar, A. et al. 2001. Acquisition of CD80 (B7-1) by T cells. J. Immunol. 166:2505.
13. Cai, Z. and Sprent, J. 1994. Resting and. activated T cells display different requirements for CD8 molecules. J. Exp. Med. 179:2005.
14. Townsend, A. R.M., Rothbard, J., Gotch, F. M., Bahadur, G., Wraith, D: and McMichael, A. J. 1986. The epitopes of influenza nucleoprotein recognized by cytotoxic T lymphocytes can be defined with short synthetic peptides. Cell 44:959.
15. Germain, R. N. 1986. The ins and outs of antigen processing and presentation. Nature 322:687.
16. Krogsgaard, M. and Davis, M. M. 2005. How T cells 'see' antigen. Nat. Immunol. 6:239.
17. Pecht, I. and Gakamsky, D. M. 2005. Spatial coordination of CD8 and TCR molecules controls antigen recognition by CD8+ T-cells. FEBS Lett. 579:3336.
18. Yachi, P. P., Ampudia, J., Gascoigne, N. R. and Zal, T. 2005. Nonstimulatory peptides contribute to antigen-induced CD8-T cell receptor interaction at the immunological synapse. Nat. Immunol. 6:785.
19. Schwartz, R. H. 1985. T-lymphocyte recognition of antigen in association with gene products of the major histocompatibility complex. Annu. Rev. Immunol. 3:237.
20. Cai, Z., Brunmark, A. B., Luxembourg, A. T. et al. 1998. Probing the activation requirements for naive CD8+ T cells with Drosophila cell transfectants as antigen presenting cells. Immunol. Rev. 165:249.
21. Garcia, K. C., Scott, C. A., Brunmark, A. et al. 1996. CD8 enhances formation of stable T-cell receptor/MHC class I molecule complexes. Nature 384:577.
22. Thome M., Germain, V., DiSanto, J. P and Acuto, O. 1996. The p56lck SH2 domain mediates recruitment of CD8/p56lck to the activated T cell receptor/CD3/zeta complex. Eur J. Immunol. 26:2093.
23. Zamoyska, R. 1998. CD4 and CD8: Modulators of T-cell receptor recognition of antigen and of immune responses? Curr. Opin Immunol. 10:82.
24. Shen, L., Potter, T. A. and Kane, K. P. 1996. Glu227→Lys substitution in the acidic loop of major histocompatibility complex class 1 alpha 3 domain distinguishes low avidity CD8 coreceptor and avidity-enhanced CD8 accessory functions. J. Exp. Med. 184:1671.
25. Knall, C., Ingold, A. and Potter, T. A. 1994. Analysis of coreceptor versus accessory molecule function of CD8 as a corretate of exogenous peptide concentration. Mol. Immunol. 31:875.
26. Knall, C., Smith-P. A. and Potter, T. A. 1995. CD8-dependent CTL require oo-engagement of CD8 and the TCR for phosphatidylinositol hydrolysis, but CD8-independent CTL,do not and can kill in the absence of phosphatidylinositol hydrolysis. Int. Immunol. 7:995.
27. Kane, K. P., Sherman, L. A. and Mescher, M. F. 1989. Molecular interactions required for triggering alloantigen-specific cytolytic T lymphocytes. J. Immunol. 142:4153.
28. O'Rourke, A. M., Rogers, J. and Mescher, M. F. 1990. Activated CD8 binding to class 1 protein mediated by the T-cell receptor results in signalling. Nature 346:187.
29. Ratnofsky, S. E., Peterson, A., Greenstein, J. L. and Burakoff, S. J. 1987. Expression and function of CD8 in a murine T cell hybridoma. J. Exp. Med. 166:1747.
30. Lustgarten, J., Waks, T. and Eshhar, Z. 1991. CD4 and CD8 accessory molecules function through interactions with major histocompatibility complex molecules which are not directly associated with the T cell receptor-antigen complex. Eur. J. Immunol. 21:2507.
31. Takeshita, T., Kozlowski, S., England, R. D. et al. 1993. Role of conserved regions of class 1 MHC molecules in the activation of CD8+CTL by peptide and purified cell-free class 1 molecules. Int. Immunol. 5:1129.
32. Aldrich, C. J., Lowen, L. C., Mann, D. et al. 1991. The Q7 a3 domain alters T cell recognition of class 1-antigens. J. Immunol. 146:3082.
33. Potter, T. A., Rajan, T. V., Dick, R. F II and Bluestone, J. A. 1989. Substitution at residue 227 of H-2 class 1 molecules abrogates recognition by CD8-dependent, but not CD8-independent, cytotoxic T lymphocytes. Nature 337:73.
34. Connolly, J. M., Hansen, T. H., Ingold, A. L. and Potter, T. A. 1990, Recognition by CD8 on cytotoxic T. lymphocytes is ablated by several substitutions in the class 1 a3 domain: CD8 and the T-cell receptor recognize the samq class 1 molecule. Proc. Natl Acad Sci. USA 87:2137.
35. Salter, R. D., Benjamin, R. J. Wesley, P. K. et al. 1990. A binding site for the T-cell co-receptor CD8 on the a3 domain. of HLA-A2. Nature 345:41.
36. Snyder, J. T, Alexander-Miller, M. A., Berzofsky, J. A. and Belyakov, I. M. 2003. Molecular mechanisms and biological significance of CTL avidity. Curr. HlV Res., 1:287.
37. Alexander-Miller, M. A. 2005. High avidity CD8+ T cells: Optimal soldiers in the war against viruses and tumor Immunol. Res. 31:13.
38. Earl, P. L., Hugin, A. W. and Moss, B. 1990.,Removal of cryptic poxvirus transcription termination sidnals from the human immunodeficiency virus type 1. envelope gene enhances expression and immunogenicity of a recombinant vaccinia virus. J. Virol. 64:24:48.
39. Belyakov, I. M., Isakov. D., Zhu, Q., Dzutsev, A., Klinman, D. and Berzofsky, J. A. 2006. Enhancement of CD8+ T cell immunity in the lung by CpG ODN increases protective efficacy of a Modified Vaccinia Ankara vaccine against lethal poxvirus infection even in CD4-deficient host. J. Immunol. 177:6336.
40. Belyakov, I. M., Wyatt, L. S., Ahlers, J. D. et al. 1998. Induction of mucosal CTL response by intrarectal immunization with a replication-deficient recombinant vaccinia virus expressing HIV 89.6 envelope protein. J. Virol. 72:8264.
41. Alexander-Miller, M. A., Leggatt, G. R. and Berzofsky, J. A. 1996. Selective expansion of high or low avidity cytotoxic T lymphocytes and efficacy for adoptive immunotherapy. Proc. Natl Acad. Sci. USA 93:4102.
42. Belyakov, I. M., Kuznetsov, V. A., Kelsall, B. et al. 2006. Impact of vaccine-induced mucosal high avidity CD8+ CTLs in delay of AIDS-viral dissemination from mucosa. Blood 107:3258.
43. Kozlowski, S., Takeshita, T., Boehncke, W.-H. et al. 1991. Excess b2-microglobulin promotes functional peptide association with purified soluble class I MHC molecules. Nature 349:74.
44. Margulies, D. H., Ramsey, A. L., Boyd, L. F. and McCluskey, J. 1986. Genetic engineering of an H-2Dd/Q10b chimeric histocompatibility antigen: Purification of soluble protein from transformant cell supernatants. Proc. Natl Acad. Sci. USA 83:5252.
45. Belyakov, I. M., Earl, P., Dzutsev, A. et al. 2003. Shared modes of protection against poxvirus infection by attenuated and conventional smallpox vaccine viruses. Proc. Natl Acad. Sci. USA 100:9458.
46. Belyakov, I. M., Moss, B., Strober, W. and Berzofsky, J. A. 1999. Mucosal vaccination overcomes the barrier to recombinant vaccinia immunization caused by preexisting poxvirus immunity. Proc. Natl Acad. Sci. USA 96:4512.
47. Belyakov, I. M., Wang, J., Koka, R. et al. 2001. Activating CTL precursors to reveal CTL function without skewing the repertoire by in vitro expansion. Eur. J. Immunol. 31:3557.
48. Takahashi, H., Cohen, J., Hosmalin, A. et al. 1988. An immunodominant epitope of the HIV gp160 envelope glycoprotein recognized by class I MHC molecule-restricted murine cytotoxic T lymphocytes. Proc. Natl Acad. Sci. USA 85:3105.
49. Newberg, M. H., Ridge, J. P., Vining, D. R., Salter, R. D. and Engelhard, V. H. 1992. Species specificity in the interaction of CD8 with the a3 domain of MHC class I molecules. J. Immunol. 149:136.
50. Wesley, P. K., Clayberger, C., Lyu, S. C. and Krensky, A. M. 1993. The CD8 coreceptor interaction with the alpha 3 domain of HLA class I is critical to the differentiation of human cytotoxic T-lymphocytes specific for HLA-A2 and HLA-Cw4. Hum. Immunol. 36:149.
51. Killeen, N., Moriarty, A., Teh, H.-S. and Littman, D. R. 1992. Requirement for CD8-major histocompatibility complex class I interaction in positive and negative selection of developing T cells. J. Exp. Med. 176:89.
52. Shepherd, S. E., Sun, R., Nathenson, S. G. and Sheil, J. M. 1992. Selective reactivity of CD8-independent T lymphocytes to a cytotoxic T lymphocyte-selected H-2Kb mutant altered at position 222 in the alpha 3 domain. Eur. J. Immunol. 22:647.
53. Zal, T., Zal, M. A. and Gascoigne, N. R. 2002. Inhibition of T cell receptor-coreceptor interactions by antagonist ligands visualized by live FRET imaging of the T-hybridoma immunological synapse. Immunity 16:521.
54. Berzofsky, J. A., Ahlers, J. D. and Belyakov, I. M. 2001. Strategies for designing and optimizing new generation vaccines. Nat. Rev. Immunol. 1:209.
55. Berzofsky, J. A., Ahlers, J. D., Derby, M. A., Pendleton, C. D., Arichi, T. and Belyakov, I. M. 1999. Approaches to improve engineered vaccines for human immunodeficiency virus (HIV) and other viruses that cause chronic infections. Immunol. Rev. 170:151.
56. Gray, P. M., Parks, G. D. and Alexander-Miller, M. A. 2001. A novel CD8-independent high-avidity cytotoxic T-lymphocyte response directed against an epitope in the phosphoprotein of the paramyxovirus simian virus 5. J. Virol. 75:10065.
57. Derby, M. A., Alexander-Miller, M. A., Tse, R. and Berzofsky, J. A. 2001. High avidity CTL exploit two complementary mechanisms to provide better protection against viral infection than low avidity CTL. J. Immunol. 166:1690.
58. Estcourt, M. J., Ramsay, A. J., Brooks, A., Thomson, S. A., Medveckzy, C. J. and Ramshaw, I. A. 2002. Prime-boost immunization generates a high frequency, high-avidity CD8(+) cytotoxic T lymphocyte population. Int. Immunol. 14:31.
59. Gallimore, A., Dumrese, T., Hengartner, H., Zinkernagel, R. M. and Rammensee, H. G. 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.
60. Belyakov, I. M., Isakov, D., Zhu, Q., Dzutsev, A. and Berzofsky, J. A. 2007. A novel functional CTL avidity/activity compartmentalization to the site of mucosal immunization contributes to protection of macaques against simian/human immunodeficiency viral depletion of mucosal CD4+ T cells. J. Immunol. 178:7211.
61. Belyakov, I. M., Ahlers, J. D. and Berzofsky, J. A. 2004. Mucosal AIDS vaccines: Current status and future directions. Expert Rev. Vaccines 3 (Suppl):65.
62. Zeh, H. J. III, Perry-Lalley, D., Dudley, M. E., Rosenberg, S. A. and Yang, J. C. 1999. High avidity CTLs for two self-antigens demonstrate superior in vitro and in vivo antitumor efficacy. J. Immunol. 162:989.
63. Gervois, N., Labarriere, N., Le Guiner, S. et al. 2000. High avidity melanoma-reactive cytotoxic T lymphocytes are efficiently induced from peripheral blood lymphocytes on stimulation by peptide-pulsed melanoma cells. Clin. Cancer. Res. 6:1459.
64. Nugent, C. T., Morgan, D. J., Biggs, J. A. et al. 2000. Characterization of CD8+ T lymphocytes that persist after peripheral tolerance to a self antigen expressed in the pancreas. J. Immunol. 164:191.
65. Yee, C., Savage, P. A., Lee, P. P., Davis, M. M. and Greenberg, P. D. 1999. Isolation of high avidity melanoma-reactive CTL from heterogeneous populations using peptide-MHC tetramers. J. Immunol. 162:2227.
66. Zheng, L., Fisher, G., Miller, R. E., Peschon, J., Lynch, D. H. and Lenardo, M. J. 1995. Induction of apoptosis in mature T cells by tumour necrosis factor. Nature 377:348.
67. Cawthon, A. G., Lu, H. and Alexander-Miller, M. A. 2001. Peptide requirement for CTL activation reflects the sensitivity to CD3 engagement: Correlation with CD8alphabeta versus CD8alphaalpha expression. J. Immunol. 167:2577.
68. Berzofsky, J. A., Ahlers, J., Janik, J. et al. 2004. Progress on new vaccine strategies against chronic viral infections. J. Clin. Invest. 114:450.
69. Berzofsky, J. A., Terabe, M., Oh, S. et al. 2004. Progress on new vaccine strategies for the immunotherapy and prevention of cancer. J. Clin. Invest. 113:1515.
70. Belyakov, I. M., Hel, Z., Kelsall, B. et al. 2001. Mucosal AIDS vaccine reduces disease and viral load in gut reservoir and blood after mucosal infection of macaques. Nat. Med. 7:1320.
71. Belyakov, I. M. and Berzofsky, J. A. 2004. Immunobiology of mucosal HIV infection and the basis for development of a new generation of mucosal AIDS vaccines. Immunity 20:247.