In vivo 6-thioguanine-resistant T cells from melanoma patients have public TCR and share TCR beta amino acid sequences with melanoma-reactive T cells

Journal of Immunological Methods

Volumn 365, Issue 1-2, 2011, Pages 76-86

  Zuleger, Cindy L ^a   Macklin, Michael D ^a   Bostwick, Bret L ^b,d   Pei, Qinglin ^a   Newton, Michael A ^a,b,c   Albertini, Mark R ^a,b,e  

^a UNIVERSITY OF WISCONSIN   (United States)

^b UNIVERSITY OF WISCONSIN   (United States)

^c University of Wisconsin Madison   (United States)

^d UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^e WILLIAM S MIDDLETON MEMORIAL VETERANS HOSPITAL   (United States)

Author keywords

CDR3 sequencing; Hypoxanthine guanine phosphoribosyltransferase; T cell receptor; Tumor immunity

Indexed keywords

COMPLEMENTARY DNA; MELANOMA ANTIGEN; T LYMPHOCYTE RECEPTOR BETA CHAIN; TIOGUANINE;

ADULT; AGED; AMINO ACID SEQUENCE; ARTICLE; CANCER CELL; CANCER PATIENT; CELL SPECIFICITY; CLINICAL ARTICLE; CLONAL VARIATION; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN TISSUE; IN VIVO STUDY; MALE; MELANOMA; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN MOTIF; T LYMPHOCYTE ACTIVATION; TUMOR BIOPSY; WILD TYPE;

ADULT; AGED; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANTIGENS, NEOPLASM; ANTINEOPLASTIC AGENTS; CASE-CONTROL STUDIES; CELLS, CULTURED; DRUG RESISTANCE, NEOPLASM; FEMALE; GENES, T-CELL RECEPTOR BETA; HUMANS; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE; LYMPHOCYTE ACTIVATION; MALE; MELANOMA; MELANOMA-SPECIFIC ANTIGENS; MIDDLE AGED; MOLECULAR SEQUENCE DATA; MUTATION; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; T-LYMPHOCYTES; THIOGUANINE; TUMOR MARKERS, BIOLOGICAL;

EID: 79551621169     PISSN: 00221759     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jim.2010.12.007     Document Type: Article

References (57)

1. Albertini R.J. HPRT mutations in humans: biomarkers for mechanistic studies. Mutat. Res. 2001, 489:1.
2. Albertini R.J., Ardell S.K., Judice S.A., Jacobson S., Allegretta M. Hypoxanthine-guanine phosphoribosyltransferase reporter gene mutation for analysis of in vivo clonal amplification in patients with HTLV type 1-associated Myelopathy/Tropical spastic paraparesis. AIDS Res. Hum. Retroviruses 2000, 16:1747.
3. Albertini M.R., King D.M., Newton M.A., Vacek P.M. In vivo mutant frequency of thioguanine-resistant T-cells in the peripheral blood and lymph nodes of melanoma patients. Mutat. Res. 2001, 476:83.
4. Albertini M.R., Macklin M.D., Zuleger C.L., Newton M.A., Judice S.A., Albertini R.J. Clonal expansions of 6-thioguanine resistant T lymphocytes in the blood and tumor of melanoma patients. Environ. Mol. Mutagen. 2008, 49:676.
5. Allegretta M., Nicklas J.A., Sriram S., Albertini R.J. T cells responsive to myelin basic protein in patients with multiple sclerosis. Science 1990, 247:718.
6. Appay V., Jandus C., Voelter V., Reynard S., Coupland S.E., Rimoldi D., Lienard D., Guillaume P., Krieg A.M., Cerottini J.C., Romero P., Leyvraz S., Rufer N., Speiser D.E. New generation vaccine induces effective melanoma-specific CD8+ T cells in the circulation but not in the tumor site. J. Immunol. 2006, 177:1670.
7. Argaet V.P., Schmidt C.W., Burrows S.R., Silins S.L., Kurilla M.G., Doolan D.L., Suhrbier A., Moss D.J., Kieff E., Sculley T.B., Misko I.S. Dominant selection of an invariant T cell antigen receptor in response to persistent infection by Epstein-Barr virus. J. Exp. Med. 1994, 180:2335.
8. Arstila T.P., Casrouge A., Baron V., Even J., Kanellopoulos J., Kourilsky P. A direct estimate of the human alphabeta T cell receptor diversity. Science 1999, 286:958.
9. Balch C.M., Gershenwald J.E., Soong S.J., Thompson J.F., Atkins M.B., Byrd D.R., Buzaid A.C., Cochran A.J., Coit D.G., Ding S., Eggermont A.M., Flaherty K.T., Gimotty P.A., Kirkwood J.M., McMasters K.M., Mihm M.C., Morton D.L., Ross M.I., Sober A.J., Sondak V.K. Final version of 2009 AJCC melanoma staging and classification. J. Clin. Oncol. 2009, 27:6199.
10. Baner J., Marits P., Nilsson M., Winqvist O., Landegren U. Analysis of T-cell receptor V beta gene repertoires after immune stimulation and in malignancy by use of padlock probes and microarrays. Clin. Chem. 2005, 51:768.
11. Bayarri M.J., Berger J.O. Quantifying surprise in the data and model verification. Bayesian Statistics 1999, 53. Oxford University Press, Oxford. 6 ed. J.M. Bernardo, J.O. Berger, A.P. Dawid, A.F.M. Smith (Eds.).
12. Brochet X., Lefranc M.P., Giudicelli V. IMGT/V-QUEST: the highly customized and integrated system for IG and TR standardized V-J and V-D-J sequence analysis. Nucleic Acids Res. 2008, 36:W503.
13. Callan M.F., Annels N., Steven N., Tan L., Wilson J., McMichael A.J., Rickinson A.B. T cell selection during the evolution of CD8+ T cell memory in vivo. Eur. J. Immunol. 1998, 28:4382.
14. Cannons J.L., Karsh J., Birnboim H.C., Goldstein R. HPRT- mutant T cells in the peripheral blood and synovial tissue of patients with rheumatoid arthritis. Arthritis Rheum. 1998, 41:1772.
15. Cole D.J., Wilson M.C., Rivoltini L., Custer M., Nishimura M.I. T-cell receptor repertoire in matched MART-1 peptide-stimulated peripheral blood lymphocytes and tumor-infiltrating lymphocytes. Cancer Res. 1997, 57:5320.
16. Cole D.K., Yuan F., Rizkallah P.J., Miles J.J., Gostick E., Price D.A., Gao G.F., Jakobsen B.K., Sewell A.K. Germ line-governed recognition of a cancer epitope by an immunodominant human T-cell receptor. J. Biol. Chem. 2009, 284:27,281.
17. Curiel T.J., Coukos G., Zou L., Alvarez X., Cheng P., Mottram P., Evdemon-Hogan M., Conejo-Garcia J.R., Zhang L., Burow M., Zhu Y., Wei S., Kryczek I., Daniel B., Gordon A., Myers L., Lackner A., Disis M.L., Knutson K.L., Chen L., Zou W. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat. Med. 2004, 10:942.
18. Degauque N., Schadendorf D., Brouard S., Guillet M., Sebille F., Hohn H., Pallier A., Ruiz C., Dupont A., Chapin S., Hofmann U., Maeurer M., Soulillou J.P. Blood T-cell Vbeta transcriptome in melanoma patients. Int. J. Cancer 2004, 110:721.
19. Dietrich P.Y., Le Gal F.A., Dutoit V., Pittet M.J., Trautman L., Zippelius A., Cognet I., Widmer V., Walker P.R., Michielin O., Guillaume P., Connerotte T., Jotereau F., Coulie P.G., Romero P., Cerottini J.C., Bonneville M., Valmori D. Prevalent role of TCR alpha-chain in the selection of the preimmune repertoire specific for a human tumor-associated self-antigen. J. Immunol. 2003, 170:5103.
20. Dutoit V., Rubio-Godoy V., Pittet M.J., Zippelius A., Dietrich P.Y., Legal F.A., Guillaume P., Romero P., Cerottini J.C., Houghten R.A., Pinilla C., Valmori D. Degeneracy of antigen recognition as the molecular basis for the high frequency of naive A2/Melan-a peptide multimer(+) CD8(+) T cells in humans. J. Exp. Med. 2002, 196:207.
21. Falta M.T., Magin G.K., Allegretta M., Steinman L., Atkinson M.A., Brostoff S.W., Albertini R.J. Selection of hprt mutant T cells as surrogates for dividing cells reveals a restricted T cell receptor BV repertoire in insulin-dependent diabetes mellitus. Clin. Immunol. 1999, 90:340.
22. Gmelig-Meyling F., Dawisha S., Steinberg A.D. Assessment of in vivo frequency of mutated T cells in patients with systemic lupus erythematosus. J. Exp. Med. 1992, 175:297.
23. Hodi F.S., O'Day S.J., McDermott D.F., Weber R.W., Sosman J.A., Haanen J.B., Gonzalez R., Robert C., Schadendorf D., Hassel J.C., Akerley W., van den Eertwegh A.J., Lutzky J., Lorigan P., Vaubel J.M., Linette G.P., Hogg D., Ottensmeier C.H., Lebbe C., Peschel C., Quirt I., Clark J.I., Wolchok J.D., Weber J.S., Tian J., Yellin M.J., Nichol G.M., Hoos A., Urba W.J. Improved survival with Ipilimumab in patients with metastatic melanoma. N. Engl. J. Med. 2010, 363:711.
24. Jager E., Hohn H., Necker A., Forster R., Karbach J., Freitag K., Neukirch C., Castelli C., Salter R.D., Knuth A., Maeurer M.J. Peptide-specific CD8+ T-cell evolution in vivo: response to peptide vaccination with Melan-A/MART-1. Int. J. Cancer 2002, 98:376.
25. Killian M.S., Matud J., Detels R., Giorgi J.V., Jamieson B.D. MaGiK method of T-Cell receptor repertoire analysis. Clin. Diagn. Lab. Immunol. 2002, 9:858.
26. Le Gal F.A., Ayyoub M., Dutoit V., Widmer V., Jager E., Cerottini J.C., Dietrich P.Y., Valmori D. Distinct structural TCR repertoires in naturally occurring versus vaccine-induced CD8+ T-cell responses to the tumor-specific antigen NY-ESO-1. J. Immunother. 2005, 28:252.
27. Lehner P.J., Wang E.C., Moss P.A., Williams S., Platt K., Friedman S.M., Bell J.I., Borysiewicz L.K. Human HLA-A0201-restricted cytotoxic T lymphocyte recognition of influenza A is dominated by T cells bearing the V beta 17 gene segment. J. Exp. Med. 1995, 181:79.
28. Manne J., Mastrangelo M.J., Sato T., Berd D. TCR rearrangement in lymphocytes infiltrating melanoma metastases after administration of autologous dinitrophenyl-modified vaccine. J. Immunol. 2002, 169:3407.
29. May E., Dulphy N., Frauendorf E., Duchmann R., Bowness P., Lopez de Castro J.A., Toubert A., Marker-Hermann E. Conserved TCR beta chain usage in reactive arthritis; evidence for selection by a putative HLA-B27-associated autoantigen. Tissue Antigens 2002, 60:299.
30. Miller A.M., Lundberg K., Ozenci V., Banham A.H., Hellstrom M., Egevad L., Pisa P. CD4+ CD25high T cells are enriched in the tumor and peripheral blood of prostate cancer patients. J. Immunol. 2006, 177:7398.
31. Moss P.A., Moots R.J., Rosenberg W.M., Rowland-Jones S.J., Bodmer H.C., McMichael A.J., Bell J.I. Extensive conservation of alpha and beta chains of the human T-cell antigen receptor recognizing HLA-A2 and influenza A matrix peptide. Proc. Natl. Acad. Sci. U.S.A. 1991, 88:8987.
32. Mourmouras V., Fimiani M., Rubegni P., Epistolato M.C., Malagnino V., Cardone C., Cosci E., Nisi M.C., Miracco C. Evaluation of tumour-infiltrating CD4+CD25+FOXP3+ regulatory T cells in human cutaneous benign and atypical naevi, melanomas and melanoma metastases. Br. J. Dermatol. 2007, 157:531.
33. Newton M.A., Clipson L., Thliveris A.T., Halberg R.B. A statistical test of the hypothesis that polyclonal intestinal tumors arise by random collision of initiated clones. Biometrics 2006, 62:721.
34. Nuovo G.J., Morrison C., Porcu P., Caligiuri M.A., Suster S. In situ determination of T-cell receptor beta expression patterns. J. Histochem. Cytochem. 2001, 49:139.
35. Oksenberg J.R., Panzara M.A., Begovich A.B., Mitchell D., Erlich H.A., Murray R.S., Shimonkevitz R., Sherritt M., Rothbard J., Bernard C.C. Selection for T-cell receptor V beta-D beta-J beta gene rearrangements with specificity for a myelin basic protein peptide in brain lesions of multiple sclerosis. Nature 1993, 362:68.
36. O'Neill J.P., McGinniss M.J., Berman J.K., Sullivan L.M., Nicklas J.A., Albertini R.J. Refinement of a T-lymphocyte cloning assay to quantify the in vivo thioguanine-resistant mutant frequency in humans. Mutagenesis 1987, 2:87.
37. Pittet M.J., Valmori D., Dunbar P.R., Speiser D.E., Lienard D., Lejeune F., Fleischhauer K., Cerundolo V., Cerottini J.C., Romero P. High frequencies of naive Melan-A/MART-1-specific CD8(+) T cells in a large proportion of human histocompatibility leukocyte antigen (HLA)-A2 individuals. J. Exp. Med. 1999, 190:705.
38. Prisco A., Troncone R., Mazzarella G., Gianfrani C., Auricchio S., Even J., Tiberio C., Guardiola J., De Berardinis P. Identical T-cell receptor beta chain rearrangements are present in T cells infiltrating the jejunal mucosa of untreated celiac patients. Hum. Immunol. 1997, 55:22.
39. PubMed home Last accessed: November 23, 2009. http://www.ncbi.nlm.nih.gov/pubmed/.
40. Ralph S.J. An update on malignant melanoma vaccine research: insights into mechanisms for improving the design and potency of melanoma therapeutic vaccines. Am. J. Clin. Dermatol. 2007, 8:123.
41. Robins J.M., van der Vaart A., Ventura V. Asymptotic distribution of p-values in composite null models. J. Am. Stat. Assoc. 2000, 95:1143.
42. Romero, P., Gervois, N., Schneider, J., Escobar, P., Valmori, D., Pannetier, C., Steinle, A., Wolfel, T., Lienard, D., Brichard, V., van Pel, A., Jotereau, F., Cerottini, J.C., 1997. Cytolytic T lymphocyte recognition of the immunodominant HLA-A*0201-restricted Melan-A/MART-1 antigenic peptide in melanoma. J. Immunol. 159, 2366.
43. Rosenberg S.A. Progress in human tumour immunology and immunotherapy. Nature 2001, 411:380.
44. Rosenberg S.A., Dudley M.E. Adoptive cell therapy for the treatment of patients with metastatic melanoma. Curr. Opin. Immunol. 2009, 21:233.
45. Serana F., Sottini A., Caimi L., Palermo B., Natali P.G., Nistico P., Imberti L. Identification of a public CDR3 motif and a biased utilization of T-cell receptor V beta and J beta chains in HLA-A2/Melan-A-specific T-cell clonotypes of melanoma patients. J. Transl. Med. 2009, 7:21.
46. Trautmann L., Rimbert M., Echasserieau K., Saulquin X., Neveu B., Dechanet J., Cerundolo V., Bonneville M. Selection of T cell clones expressing high-affinity public TCRs within human cytomegalovirus-specific CD8 T cell responses. J. Immunol. 2005, 175:6123.
47. Turner S.J., Doherty P.C., McCluskey J., Rossjohn J. Structural determinants of T-cell receptor bias in immunity. Nat. Rev. Immunol. 2006, 6:883.
48. Tynan F.E., Borg N.A., Miles J.J., Beddoe T., El-Hassen D., Silins S.L., van Zuylen W.J., Purcell A.W., Kjer-Nielsen L., McCluskey J., Burrows S.R., Rossjohn J. High resolution structures of highly bulged viral epitopes bound to major histocompatibility complex class I. Implications T cell receptor engagement T cell immunodominance. J. Biol. Chem. 2005, 280:23,900.
49. Van den Berg L.H., Mollee I., Wokke J.H., Logtenberg T. Increased frequencies of HPRT mutant T lymphocytes in patients with Guillain-Barre syndrome and chronic inflammatory demyelinating polyneuropathy: further evidence for a role of T cells in the etiopathogenesis of peripheral demyelinating diseases. J. Neuroimmunol. 1995, 58:37.
50. Venturi V., Kedzierska K., Price D.A., Doherty P.C., Douek D.C., Turner S.J., Davenport M.P. Sharing of T cell receptors in antigen-specific responses is driven by convergent recombination. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:18,691.
51. Viguier M., Lemaitre F., Verola O., Cho M.S., Gorochov G., Dubertret L., Bachelez H., Kourilsky P., Ferradini L. Foxp3 expressing CD4+CD25(high) regulatory T cells are overrepresented in human metastatic melanoma lymph nodes and inhibit the function of infiltrating T cells. J. Immunol. 2004, 173:1444.
52. Wieckowski S., Baumgaertner P., Corthesy P., Voelter V., Romero P., Speiser D.E., Rufer N. Fine structural variations of alphabetaTCRs selected by vaccination with natural versus altered self-antigen in melanoma patients. J. Immunol. 2009, 183:5397.
53. Willhauck M., Scheibenbogen C., Pawlita M., Mohler T., Thiel E., Keilholz U. Restricted T-cell receptor repertoire in melanoma metastases regressing after cytokine therapy. Cancer Res. 2003, 63:3483.
54. Wolfl M., Kuball J., Ho W.Y., Nguyen H., Manley T.J., Bleakley M., Greenberg P.D. Activation-induced expression of CD137 permits detection, isolation, and expansion of the full repertoire of CD8+ T cells responding to antigen without requiring knowledge of epitope specificities. Blood 2007, 110:201.
55. Zaunders J.J., Munier M.L., Seddiki N., Pett S., Ip S., Bailey M., Xu Y., Brown K., Dyer W.B., Kim M., de Rose R., Kent S.J., Jiang L., Breit S.N., Emery S., Cunningham A.L., Cooper D.A., Kelleher A.D. High levels of human antigen-specific CD4+ T cells in peripheral blood revealed by stimulated coexpression of CD25 and CD134 (OX40). J. Immunol. 2009, 183:2827.
56. Zeuthen J., Birck A., Straten P.T. Analysis of T cell receptor alpha beta variability in tumor-infiltrating lymphocytes in primary and metastatic melanoma. Arch. Immunol. Ther. Exp. Warsz 1995, 43:123.
57. Zippelius A., Pittet M.J., Batard P., Rufer N., de Smedt M., Guillaume P., Ellefsen K., Valmori D., Lienard D., Plum J., MacDonald H.R., Speiser D.E., Cerottini J.C., Romero P. Thymic selection generates a large T cell pool recognizing a self-peptide in humans. J. Exp. Med. 2002, 195:485.