Ultrasensitive detection and phenotyping of CD4+ T cells with optimized HLA class II tetramer staining

Journal of Immunology

Volumn 175, Issue 10, 2005, Pages 6334-6343

  Scriba, Thomas J ^a   Purbhoo, Marco ^b   Day, Cheryl L ^a   Robinson, Nicola ^a   Fidler, Sarah ^c   Fox, Julie ^c   Weber, Jonathan N ^c   Klenerman, Paul ^a   Sewell, Andrew K ^a   Phillips, Rodney E ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b Avidex Ltd   (United Kingdom)

^c ST MARY S HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; HLA ANTIGEN CLASS 2; HLA DR1 ANTIGEN; HLA DR4 ANTIGEN; TETANUS TOXOID;

ARTICLE; CELL CLONE; CELL LINE; CYTOMEGALOVIRUS; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; INFLUENZA VIRUS; INTERNALIZATION; PERIPHERAL LYMPHOCYTE; PHENOTYPE; PRIORITY JOURNAL; STAINING; T LYMPHOCYTE; VIRUS INFECTION;

EID: 27744549817     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.175.10.6334     Document Type: Article

References (52)

1. Sykulev, Y., A. Brunmark, M. Jackson, R. J. Cohen, P. A. Peterson, and H. N. Eisen. 1994. Kinetics and affinity of reactions between an antigen-specific T cell receptor and peptide-MHC complexes. Immunity 1: 15-22.
2. Matsui, K., J. J. Boniface, P. Steffner, P. A. Reay, and M. M. Davis. 1994. Kinetics of T-cell receptor binding to peptide/I-Ek complexes: correlation of the dissociation rate with T-cell responsiveness. Proc. Natl. Acad. Sci. USA 91: 12862-12866.
3. Corr, M., A. E. Slanetz, L. F. Boyd, M. T. Jelonek, S. Khilko, B. K. al-Ramadi, Y. S. Kim, S. E. Maher, A. L. Bothwell, and D. H. Margulies. 1994. T cell receptor-MHC class I peptide interactions: affinity, kinetics, and specificity. Science 265: 946-949.
4. Altman, J. D., P. A. Moss, P. J. Goulder, D. H. Barouch, M. G. McHeyzer-Williams, J. I. Bell, A. J. McMichael, and M. M. Davis. 1996. Phenotypic analysis of antigen-specific T lymphocytes. Science 274: 94-96.
5. Fuller, M. J., and A. J. Zajac. 2003. Ablation of CD8 and CD4 T cell responses by high viral loads. J. Immunol. 170: 477-486.
6. + HIV-specific T cells during progression to AIDS. Blood 99: 2505-2511.
7. Ferlin, W., N. Glaichenhaus, and E. Mougneau. 2000. Present difficulties and future promise of MHC multimers in autoimmune exploration. Curr. Opin. Immunol. 12: 670-675.
8. Crawford, F., H. Kozono, J. White, P. Marrack, and J. Kappler. 1998. Detection of antigen-specific T cells with multivalent soluble class II MHC covalent peptide complexes. Immunity 8: 675-682.
9. + T cells proliferating in response to influenza A antigen. J. Clin. Invest. 104: R63-R67.
10. Novak, E. J., S. A. Masewicz, A. W. Liu, A. Lemmark, W. W. Kwok, and G. T. Nepom. 2001. Activated human epitope-specific T cells identified by class II tetramers reside within a CD4high, proliferating subset. Int. Immunol. 13: 799-806.
11. + T cell responses against HCV: analysis of fluctuating dominant and subdominant HLA-DR11 restricted epitopes. J. Viral. Hepat. 11: 324-331.
12. + T cells in peripheral blood mononuclear cells. Eur. J. Immunol. 32: 3366-3375.
13. + T-cell repertoire directed against an influenza peptide: a step towards TCR proteomics. Immunogenetics 54: 611-620.
14. Reijonen, H., E. J. Novak, S. Kochik, A. Heninger, A. W. Liu, W. W. Kwok, and G. T. Nepom. 2002. Detection of GAD65-specific T-cells by major histocompatibility complex class II tetramers in type 1 diabetic patients and at-risk subjects. Diabetes 51: 1375-1382.
15. + T cells with class II MHC oligomers. J. Immunol. Methods 268: 51-69.
16. Yang, J., A. Jaramillo, R. Shi, W. W. Kwok, and T. Mohanakumar. 2004. In vivo biotinylation of the major histocompatibility complex (MHC) class II/peptide complex by coexpression of BirA enzyme for the generation of MHC class II/tetramers. Hum. Immunol. 65: 692-699.
17. Meyer, A. L., C. Trollmo, F. Crawford, P. Marrack, A. C. Steere, B. T. Huber, J. Kappler, and D. A. Hafler. 2000. Direct enumeration of Borrelia-reactive CD4 T cells ex vivo by using MHC class II tetramers. Proc. Natl. Acad. Sci. USA 97: 11433-11438.
18. Day, C. L., N. P. Seth, M. Lucas, H. Appel, L. Gauthier, G. M. Lauer, G. K. Robbins, Z. M. Szczepiorkowski, D. R. Casson, R. T. Chung, et al. 2003. Ex vivo analysis of human memory CD4 T cells specific for hepatitis C virus using MHC class II tetramers. J. Clin. Invest. 112: 831-842.
19. Lucas, M., C. L. Day, J. R. Wyer, S. L. Cunliffe, A. Loughry, A. J. McMichael, and P. Klenerman. 2004. Ex vivo phenotype and frequency of influenza virus-specific CD4 memory T cells. J. Virol. 78: 7284-7287.
20. + T lymphocyte turnover and activation increase upon viral rebound. J. Clin. Invest. 115: 443-450.
21. + T cells using MHC class II multimer bead sorting and immunoscope analysis. Eur. J. Immunol. 34: 2941-2949.
22. + T cell epitopes from complex antigens. J. Immunol. 166: 6665-6670.
23. Reijonen, H., and W. W. Kwok. 2003. Use of HLA class II tetramers in tracking antigen-specific T cells and mapping T-cell epitopes. Methods 29: 282-288.
24. Kotzin, B. L., M. T. Falta, F. Crawford, E. F. Rosloniec, J. Bill, P. Marrack, and J. Kappler. 2000. Use of soluble peptide-DR4 tetramers to detect synovial T cells specific for cartilage antigens in patients with rheumatoid arthritis. Proc. Natl. Acad. Sci. USA 97: 291-296.
25. + T cells by HLA-DR1 oligomers is dependent on the T cell activation state. J. Immunol. 166: 741-745.
26. Savage, P. A., J. J. Boniface, and M. M. Davis. 1999. A kinetic basis for T cell receptor repertoire selection during an immune response. Immunity 10: 485-492.
27. Reichstetter, S., R. A. Ettinger, A. W. Liu, J. A. Gebe, G. T. Nepom, and W. W. Kwok. 2000. Distinct T cell interactions with HLA class II tetramers characterize a spectrum of TCR affinities in the human antigen-specific T cell response. J. Immunol. 165: 6994-6998.
28. Davis, M. M., J. J. Boniface, Z. Reich, D. Lyons, J. Hampl, B. Arden, and Y. Chien. 1998. Ligand recognition by αβ T cell receptors. Annu. Rev. Immunol. 16: 523-544.
29. Purbhoo, M. A., J. M. Boulter, D. A. Price, A. L. Vuidepot, C. S. Hourigan, P. R. Dunbar, K. Olson, S. J. Dawson, R. E. Phillips, B. K. Jakobsen, et al. 2001. The human CD8 coreceptor effects cytotoxic T cell activation and antigen sensitivity primarily by mediating complete phosphorylation of the T cell receptor ζ chain. J. Biol. Chem. 276: 32786-32792.
30. Wooldridge, L., S. L. Hutchinson, E. M. Choi, A. Lissina, E. Jones, F. Mirza, P. R. Dunbar, D. A. Price, V. Cerundolo, and A. K. Sewell. 2003. Anti-CD8 antibodies can inhibit or enhance peptide-MHC class I (pMHCI) multimer binding: this is paralleled by their effects on CTL activation and occurs in the absence of an interaction between pMHCI and CD8 on the cell surface. J. Immunol. 171: 6650-6660.
31. Bunce, M., C. M. O'Neill, M. C. Barnardo, P. Krausa, M. J. Browning, P. J. Morris, and K. I. Welsh. 1995. Phototyping: comprehensive DNA typing for HLA-A, B, C, DRB1, DRB3, DRB4, DRB5 & DQB1 by PCR with 144 primer mixes utilizing sequence-specific primers (PCR-SSP). Tissue Antigens 46: 355-367.
32. Lamb, J. R., D. D. Eckels, P. Lake, J. N. Woody, and N. Green. 1982. Human T-cell clones recognize chemically synthesized peptides of influenza haemagglutinin. Nature 300: 66-69.
33. + T cells directed to self-antigens. Eur. J. Immunol. 33: 1409-1417.
34. Wong, R., R. Lau, J. Chang, T. Kuus-Reichel, V. Brichard, C. Bruck, and J. Weber. 2004. Immune responses to a class II helper peptide epitope in patients with stage III/IV resected melanoma. Clin. Cancer Res. 10: 5004-5013.
35. Whelan, J. A., P. R. Dunbar, D. A. Price, M. A. Purbhoo, F. Lechner, G. S. Ogg, G. Griffiths, R. E. Phillips, V. Cerundolo, and A. K. Sewell. 1999. Specificity of CTL interactions with peptide-MHC class I tetrameric complexes is temperature dependent. J. Immunol. 163: 4342-4348.
36. Mallone, R., and G. T. Nepom, 2004. MHC class II tetramers and the pursuit of antigen-specific T cells: define, deviate, delete. Clin. Immunol. 110: 232-242.
37. + T cells. Eur. J. Immunol. 34: 1570-1577.
38. Lechner, F., D. K. Wong, P. R. Dunbar, R. Chapman, R. T. Chung, P. Dohrenwend, G. Robbins, R. Phillips, P. Klenerman, and B. D. Walker. 2000. Analysis of successful immune responses in persons infected with hepatitis C virus. J. Exp. Med. 191: 1499-1512.
39. Harari, A., S. Petitpierre, F. Vallelian, and G. Pantaleo. 2004. Skewed representation of functionally distinct populations of virus-specific CD4 T cells in HIV-1-infected subjects with progressive disease: changes after antiretroviral therapy. Blood 103: 966-972.
40. Harari, A., F. Vallelian, and G. Pantaleo. 2004. Phenotypic heterogeneity of antigen-specific CD4 T cells under different conditions of antigen persistence and antigen load. Eur. J. Immunol. 34: 3525-3533.
41. Chao, C. C., R. Jensen, and M. O. Dailey. 1997. Mechanisms of L-selectin regulation by activated T cells. J. Immunol. 159: 1686-1694.
42. Sallusto, F., E. Kremmer, B. Palermo, A. Hoy, P. Ponath, S. Qin, R. Forster, M. Lipp, and A. Lanzavecchia. 1999. Switch in chemokine receptor expression upon TCR stimulation reveals novel homing potential for recently activated T cells. Eur. J. Immunol. 29: 2037-2045.
43. Murali-Krishna, K., J. D. Altman, M. Suresh, D. J. Sourdive, A. J. Zajac, J. D. Miller, J. Slansky, and R. Ahmed. 1998. Counting antigen-specific CD8 T cells: a reevaluation of bystander activation during viral infection. Immunity 8: 177-187.
44. + T cells specific for EBV in healthy virus carriers. J. Immunol. 162: 1827-1835.
45. + T cells. J. Immunol. 166: 7009-7013.
46. + T cell response to a rheumatoid arthritis-associated antigen. Arthritis Rheum. 52: 1885-1896.
47. + T cells vary in differentiation phenotype in different persistent virus infections. Nat. Med. 8: 379-385.
48. + T cells. J. Immunol. 172: 2476-2486.
49. + T cell response to Epstein-Barr virus during primary and persistent infection. J. Exp. Med. 198: 903-911.
50. Vallejo, A. N., J. C. Brandes, C. M. Weyand, and J. J. Goronzy. 1999. Modulation of CD28 expression: distinct regulatory pathways during activation and replicative senescence. J. Immunol. 162: 6572-6579.
51. Eck, S. C., D. Chang, A. D. Wells, and L. A. Turka. 1997. Differential down-regulation of CD28 by B7-1 and B7-2 engagement. Transplantation 64: 1497-1499.
52. Sallusto, F., J. Geginat, and A. Lanzavecchia. 2004. Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu. Rev. Immunol. 22: 745-763.