TCR sequencing facilitates diagnosis and identifies mature T cells as the cell of origin in CTCL

Science Translational Medicine

Volumn 7, Issue 308, 2015, Pages

  Kirsch, Ilan R ^a   Watanabe, Rei ^b   O'Malley, John T ^b   Williamson, David W ^a   Scott, Laura Louise ^b   Elco, Christopher P ^b   Teague, Jessica E ^b   Gehad, Ahmed ^b   Lowry, Elizabeth L ^b   Leboeuf, Nicole R ^b   Krueger, James G ^c   Robins, Harlan S ^a   Kupper, Thomas S ^b   Clark, Rachael A ^b  

^a ADAPTIVE BIOTECHNOLOGIES   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALEMTUZUMAB; COTRIMOXAZOLE; GEMCITABINE; T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR GAMMA; UNCLASSIFIED DRUG; VALACICLOVIR; LYMPHOCYTE ANTIGEN RECEPTOR;

ARTICLE; BRACHYTHERAPY; CANCER RECURRENCE; CANCER STAGING; CD4+ T LYMPHOCYTE; CELL AGGREGATION; CELL CLONE; CELLULAR DISTRIBUTION; CONTACT DERMATITIS; CONTROLLED STUDY; CUTANEOUS T CELL LYMPHOMA; DRUG EFFICACY; DRUG RESPONSE; ECZEMA; ELECTRON THERAPY; GENE; GENE FREQUENCY; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN CELL; LOW DRUG DOSE; LYMPHOCYTE COUNT; LYMPHOCYTE SUBPOPULATION; MEMORY T LYMPHOCYTE; PITYRIASIS LICHENOIDES; PRIORITY JOURNAL; PSORIASIS; T LYMPHOCYTE; TCR V GAMMA GENE; TCR VBETA GENE; GENETICS; IN VITRO STUDY; METABOLISM; PATHOLOGY; PROCEDURES; SKIN DISEASE;

HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; IN VITRO TECHNIQUES; LYMPHOMA, T-CELL, CUTANEOUS; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; SKIN DISEASES; T-LYMPHOCYTES;

EID: 84943610604     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aaa9122     Document Type: Article

References (42)

1. R. Willemze, E. S. Jaffe, G. Burg, L. Cerroni, E. Berti, S. H. Swerdlow, E. Ralfkiaer, S. Chimenti, J. L. Diaz-Perez, L. M. Duncan, F. Grange, N. L. Harris, W. Kempf, H. Kerl, M. Kurrer, R. Knobler, N. Pimpinelli, C. Sander, M. Santucci, W. Sterry, M. H. Vermeer, J. Wechsler, S. Whittaker, C. J. L. M. Meijer, WHO-EORTC classification for cutaneous lymphomas. Blood 105, 3768-3785 (2005).
2. Y. H. Kim, H. L. Liu, S. Mraz-Gernhard, A. Varghese, R. T. Hoppe, Long-term outcome of 525 patients with mycosis fungoides and Sezary syndrome: Clinical prognostic factors and risk for disease progression. Arch. Dermatol. 139, 857-866 (2003).
3. ® (National Comprehensive Cancer Network Inc., Fort Washington, PA, 2009); www.NCCN.org.
4. D. P. Fivenson, C. A. Hanson, B. J. Nickoloff, Localization of clonal T cells to the epidermis in cutaneous T-cell lymphoma. J. Am. Acad. Dermatol. 31, 717-723 (1994).
5. J. J. Van Dongen, A. W. Langerak, M. Brüggemann, P. A. Evans, M. Hummel, F. L. Lavender, E. Delabesse, F. Davi, E. Schuuring, R. García-Sanz, J. H. Van Krieken, J. Droese, D. González, C. Bastard, H. E. White, M. Spaargaren, M. González, A. Parreira, J. L. Smith, G. J. Morgan, M. Kneba, E. A. Macintyre, Design and standardization of PCR primers and protocols for detection of clonal immunoglobulin and T-cell receptor gene recombinations in suspect lymphoproliferations: Report of the BIOMED-2 Concerted Action BMH4-CT98-3936. Leukemia 17, 2257-2317 (2003).
6. R. Ponti, M. T. Fierro, P. Quaglino, B. Lisa, F. Paola, O. Michela, F. Paolo, A. Comessatti, M. Novelli, M. G. Bernengo, TCRγ-chain gene rearrangement by PCR-based GeneScan: Diagnostic accuracy improvement and clonal heterogeneity analysis in multiple cutaneous T-cell lymphoma samples. J. Invest. Dermatol. 128, 1030-1038 (2008).
7. R. Van Doorn, C. W. Van Haselen, P. C. Van Voorst Vader, M. L. Geerts, F. Heule, M. De Rie, P. M. Steijlen, S. K. Dekker, W. A. Van Vloten, R. Willemze, Mycosis fungoides: Disease evolution and prognosis of 309 Dutch patients. Arch. Dermatol. 136, 504-510 (2000).
8. H. S. Robins, P. V. Campregher, S. K. Srivastava, A. Wacher, C. J. Turtle, O. Kahsai, S. R. Riddell, E. H. Warren, C. S. Carlson, Comprehensive assessment of T-cell receptor b-chain diversity in ab T cells. Blood 114, 4099-4107 (2009).
9. W.-K. Weng, R. Armstrong, S. Arai, C. Desmarais, R. Hoppe, Y. Kim, Minimal residual disease monitoring with high-throughput sequencing of T cell receptors in cutaneous T cell lymphoma. Sci. Transl. Med. 5, 214ra171 (2013).
10. K. E. Sufficool, C. M. Lockwood, H. J. Abel, I. S. Hagemann, J. A. Schumacher, T. W. Kelley, E. J. Duncavage, T-cell clonality assessment by next-generation sequencing improves detection sensitivity in mycosis fungoides. J. Am. Acad. Dermatol. 73, 228-236.e1 (2015).
11. J. M. Weinberg, L. Kristal, L. Chooback, P. J. Honig, E. M. Kramer, S. R. Lessin, The clonal nature of pityriasis lichenoides. Arch. Dermatol. 138, 1063-1067 (2002).
12. O. Dereure, E. Levi, M. E. Kadin, T-cell clonality in pityriasis lichenoides et varioliformis acuta: A heteroduplex analysis of 20 cases. Arch. Dermatol. 136, 1483-1486 (2000).
13. L. M. Weiss, G. S. Wood, L. W. Ellisen, T. C. Reynolds, J. Sklar, Clonal T-cell populations in pityriasis lichenoides et varioliformis acuta (Mucha-Habermann disease). Am. J. Pathol. 126, 417-421 (1987).
14. A. M. Sherwood, C. Desmarais, R. J. Livingston, J. Andriesen, M. Haussler, C. S. Carlson, H. Robins, Deep sequencing of the human TCRγ and TCRb repertoires suggests that TCRb rearranges after ab and gd T cell commitment. Sci. Transl. Med. 3, 90ra61 (2011).
15. R. A. Clark, R. Watanabe, J. E. Teague, C. Schlapbach, M. C. Tawa, N. Adams, A. A. Dorosario, K. S. Chaney, C. S. Cutler, N. R. Leboeuf, J. B. Carter, D. C. Fisher, T. S. Kupper, Skin effector memory T cells do not recirculate and provide immune protection in alemtuzumab-treated CTCL patients. Sci. Transl. Med. 4, 117ra117 (2012).
16. C. Linnemann, R. Mezzadra, T. N. Schumacher, TCR repertoires of intratumoral T-cell subsets. Immunol. Rev. 257, 72-82 (2014).
17. J. J. Campbell, R. A. Clark, R. Watanabe, T. S. Kupper, Sézary syndrome and mycosis fungoides arise from distinct T-cell subsets: A biologic rationale for their distinct clinical behaviors. Blood 116, 767-771 (2010).
18. + T cells accumulate near sensory nerve endings in genital skin during subclinical HSV-2 reactivation. J. Exp. Med. 204, 595-603 (2007).
19. + skin-resident T cells in human herpes virus infection. Nature 497, 494-497 (2013).
20. R. Watanabe, A. Gehad, C. Yang, L. L. Scott, J. E. Teague, C. Schlapbach, C. P. Elco, V. Huang, T. R. Matos, T. S. Kupper, R. A. Clark, Human skin is protected by four functionally and phenotypically discrete populations of resident and recirculating memory T cells. Sci. Transl. Med. 7, 279ra39 (2015).
21. J. Marcus Muche, L. Karenko, S. Gellrich, R. Karhu, S. Kytola, M. Kahkonen, A. Lukowsky, W. Sterry, A. Ranki, Cellular coincidence of clonal T cell receptor rearrangements and complex clonal chromosomal aberrations-A hallmark of malignancy in cutaneous T cell lymphoma. J. Invest. Dermatol. 122, 574-578 (2004).
22. H. M. Padilla-Nash, K. Wu, H. Just, T. Ried, K. Thestrup-Pedersen, Spectral karyotyping demonstrates genetically unstable skin-homing T lymphocytes in cutaneous T-cell lymphoma. Exp. Dermatol. 16, 98-103 (2007).
23. N. Khan, N. Shariff, M. Cobbold, R. Bruton, J. A. Ainsworth, A. J. Sinclair, L. Nayak, P. A. Moss, Cytomegalovirus seropositivity drives the CD8 T cell repertoire toward greater clonality in healthy elderly individuals. J. Immunol. 169, 1984-1992 (2002).
24. W. J. Lin, D. A. Norris, M. Achziger, B. L. Kotzin, B. Tomkinson, Oligoclonal expansion of intraepidermal T cells in psoriasis skin lesions. J. Invest. Dermatol. 117, 1546-1553 (2001).
25. L. I. Sakkas, B. Xu, C. M. Artlett, S. Lu, S. A. Jimenez, C. D. Platsoucas, Oligoclonal T cell expansion in the skin of patients with systemic sclerosis. J. Immunol. 168, 3649-3659 (2002).
26. S. C. Jameson, Maintaining the norm: T-cell homeostasis. Nat. Rev. Immunol. 2, 547-556 (2002).
27. C. D. Surh, J. Sprent, Regulation of mature T cell homeostasis. Semin. Immunol. 17, 183-191 (2005).
28. K. H. Grabstein, J. Eisenman, K. Shanebeck, C. Rauch, S. Srinivasan, V. Fung, C. Beers, J. Richardson, M. A. Schoenborn, M. Ahdieh, L. Johnson, M. R. Alderson, J. D. Watson, D. M. Anderson, J. G. Giri, Cloning of a T cell growth factor that interacts with the b chain of the interleukin-2 receptor. Science 264, 965-968 (1994).
29. M. Mohamadzadeh, A. Takashima, I. Dougherty, J. Knop, P. R. Bergstresser, P. D. Cruz Jr., Ultraviolet B radiation up-regulates the expression of IL-15 in human skin. J. Immunol. 155, 4492-4496 (1995).
30. G. Rappl, A. Kapsokefalou, C. Heuser, M. Rössler, S. Ugurel, W. Tilgen, U. Reinhold, H. Abken, Dermal fibroblasts sustain proliferation of activated T cells via membrane-bound interleukin-15 upon long-term stimulation with tumor necrosis factor-a. J. Invest. Dermatol. 116, 102-109 (2001).
31. J. P. Lodolce, P. R. Burkett, D. L. Boone, M. Chien, A. Ma, T cell-independent interleukin 15Ra signals are required for bystander proliferation. J. Exp. Med. 194, 1187-1194 (2001).
32. R. A. Clark, T. S. Kupper, IL-15 and dermal fibroblasts induce proliferation of natural regulatory T cells isolated from human skin. Blood 109, 194-202 (2007).
33. U. Döbbeling, R. Dummer, E. Laine, N. Potoczna, J. Z. Qin, G. Burg, Interleukin-15 is an autocrine/paracrine viability factor for cutaneous T-cell lymphoma cells. Blood 92, 252-258 (1998).
34. J. Z. Qin, C. L. Zhang, J. Kamarashev, R. Dummer, G. Burg, U. Döbbeling, Interleukin-7 and interleukin-15 regulate the expression of the bcl-2 and c-myb genes in cutaneous T-cell lymphoma cells. Blood 98, 2778-2783 (2001).
35. + cutaneous T-cell lymphoma cells. Cancer Res. 68, 1083-1091 (2008).
36. I. Brownell, C. J. Etzel, D. J. Yang, S. H. Taylor, M. Duvic, Increased malignancy risk in the cutaneous T-cell lymphoma patient population. Clin. Lymphoma Myeloma 8, 100-105 (2008).
37. K. Kaltoft, B. H. Hansen, K. Thestrup-Pedersen, Cytogenetic findings in cell lines from cutaneous T-cell lymphoma. Dermatol. Clin. 12, 295-304 (1994).
38. R. Watanabe, J. E. Teague, D. C. Fisher, T. S. Kupper, R. A. Clark, Alemtuzumab therapy for leukemic cutaneous T-cell lymphoma: Diffuse erythema as a positive predictor of complete remission. JAMA Dermatol. 150, 776-779 (2014).
39. M. P. Lefranc, V. Giudicelli, C. Ginestoux, J. Jabado-Michaloud, G. Folch, F. Bellahcene, Y. Wu, E. Gemrot, X. Brochet, J. Lane, L. Regnier, F. Ehrenmann, G. Lefranc, P. Duroux, IMGT, the international ImMunoGeneTics information system. Nucleic Acids Res. 37, D1006-D1012 (2009).
40. M. P. Lefranc, IMGT, the International ImMunoGeneTics Information System. Cold Spring Harb. Protoc. 2011, 595-603 (2011).
41. M. P. Lefranc, IMGT, The International ImMunoGeneTics Information System, http://imgt.cines.fr. Methods Mol. Biol. 248, 27-49 (2004).
42. C. S. Carlson, R. O. Emerson, A. M. Sherwood, C. Desmarais, M.-W. Chung, J. M. Parsons, M. S. Steen, M. A. LaMadrid-Herrmannsfeldt, D. W. Williamson, R. J. Livingston, D. Wu, B. L. Wood, M. J. Rieder, H. Robins, Using synthetic templates to design an unbiased multiplex PCR assay. Nat. Commun. 4, 2680 (2013).