Skin effector memory T cells do not recirculate and provide immune protection in alemtuzumab-treated CTCL patients

Science Translational Medicine

Volumn 4, Issue 117, 2012, Pages

  Clark, Rachael A ^a   Watanabe, Rei ^a   Teague, Jessica E ^a   Schlapbach, Christoph ^a   Tawa, Marianne C ^a   Adams, Natalie ^a   Dorosario, Andrew A ^a   Chaney, Keri S ^a   Cutler, Corey S ^a   LeBoeuf, Nicole R ^a   Carter, Joi B ^b   Fisher, David C ^a   Kupper, Thomas S ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALEMTUZUMAB; CD52 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 4; SULFAMETHOXAZOLE; TRIMETHOPRIM; TUMOR NECROSIS FACTOR ALPHA; VALACICLOVIR; ANTINEOPLASTIC AGENT; GLYCOPROTEIN; LEUKOCYTE ANTIGEN; MONOCLONAL ANTIBODY; TUMOR ANTIGEN;

ADULT; AGED; ARTICLE; CANCER CELL; CELL COUNT; CENTRAL MEMORY T LYMPHOCYTE; CIRCULATION; CONTROLLED STUDY; CUTANEOUS T CELL LYMPHOMA; CYTOKINE PRODUCTION; DRUG EFFICACY; DRUG SAFETY; EFFECTOR MEMORY T LYMPHOCYTE; FEMALE; HERPES SIMPLEX; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE RESPONSE; INFECTION PREVENTION; LEUKEMIC CUTANEOUS T CELL LYMPHOMA; LOW DRUG DOSE; MAJOR CLINICAL STUDY; MALE; MEMORY T LYMPHOCYTE; NEUTROPHIL; PNEUMOCYSTIS PNEUMONIA; PRIORITY JOURNAL; T CELL DEPLETION; T LYMPHOCYTE SUBPOPULATION; TH1 CELL; TH2 CELL; TREATMENT RESPONSE; BIOSYNTHESIS; CYTOTOXIC T LYMPHOCYTE; IMMUNE SYSTEM; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; MICROBIOLOGY; MIDDLE AGED; MYCOSIS FUNGOIDES; PHENOTYPE; SKIN; T LYMPHOCYTE;

AGED; AGED, 80 AND OVER; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTIGENS, CD; ANTIGENS, NEOPLASM; ANTINEOPLASTIC AGENTS; FEMALE; GLYCOPROTEINS; HUMANS; IMMUNE SYSTEM; IMMUNOLOGIC MEMORY; MALE; MIDDLE AGED; MYCOSIS FUNGOIDES; NEUTROPHILS; PHENOTYPE; SKIN; T-LYMPHOCYTES; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84856072398     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3003008     Document Type: Article

References (51)

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. 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 Sézary syndrome: Clinical prognostic factors and risk for disease progression. Arch. Dermatol. 139, 857-866 (2003).
3. National Comprehensive Cancer Network, NCCN Clinical Practice Guidelines in Oncology: Non-Hodgkin's Lymphomas (National Comprehensive Cancer Network, Fort Washington, PA, 2009).
4. J. Shin, S. Monti, D. J. Aires, M. Duvic, T. Golub, D. A. Jones, T. S. Kupper, Lesional gene expression profiling in cutaneous T-cell lymphoma reveals natural clusters associated with disease outcome. Blood 110, 3015-3027 (2007).
5. R. van Doorn, M. S. van Kester, R. Dijkman, M. H. Vermeer, A. A. Mulder, K. Szuhai, J. Knijnenburg, J. M. Boer, R. Willemze, C. P. Tensen, Oncogenomic analysis of mycosis fungoides reveals major differences with Sézary syndrome. Blood 113, 127-136 (2009).
6. 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).
7. K. Ferenczi, N. Yawalkar, D. Jones, T. S. Kupper, Monitoring the decrease of circulating malignant T cells in cutaneous T-cell lymphoma during photopheresis and interferon therapy. Arch. Dermatol. 139, 909-913 (2003).
8. R. A. Clark, J. B. Shackelton, R. Watanabe, A. Calarese, K. Yamanaka, J. J. Campbell, J. E. Teague, H. P. Kuo, D. Hijnen, T. S. Kupper, High-scatter T cells: A reliable biomarker for malignant T cells in cutaneous T-cell lymphoma. Blood 117, 1966-1976 (2011).
9. F. Sallusto, D. Lenig, R. Förster, M. Lipp, A. Lanzavecchia, Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401, 708-712 (1999).
10. + T cells are resident in normal skin. J. Immunol. 176, 4431-4439 (2006).
11. W. M. Siders, J. Shields, C. Garron, Y. Hu, P. Boutin, S. Shankara, W. Weber, B. Roberts, J. M. Kaplan, Involvement of neutrophils and natural killer cells in the anti-tumor activity of alemtuzumab in xenograft tumor models. Leuk. Lymphoma 51, 1293-1304 (2010).
12. Y. Hu, M. J. Turner, J. Shields, M. S. Gale, E. Hutto, B. L. Roberts, W. M. Siders, J. M. Kaplan, Investigation of the mechanism of action of alemtuzumab in a human CD52 transgenic mouse model. Immunology 128, 260-270 (2009).
13. F. Sallusto, J. Geginat, A. Lanzavecchia, Central memory and effector memory T cell subsets: Function, generation, and maintenance. Annu. Rev. Immunol. 22, 745-763 (2004).
14. K. R. Suchin, J. M. Junkins-Hopkins, A. H. Rook, Treatment of stage IA cutaneous T-cell lymphoma with topical application of the immune response modifier imiquimod. Arch. Dermatol. 138, 1137-1139 (2002).
15. A. H. Rook, P. Heald, The immunopathogenesis of cutaneous T-cell lymphoma. Hematol. Oncol. Clin. North Am. 9, 997-1010 (1995).
16. A. H. Rook, B. R. Vowels, C. Jaworsky, A. Singh, S. R. Lessin, The immunopathogenesis of cutaneous T-cell lymphoma. Abnormal cytokine production by Sézary T cells. Arch. Dermatol. 129, 486-489 (1993).
17. C. L. Tendler, J. D. Burton, J. Jaffe, D. Danielpour, M. Charley, J. P. McCoy, M. R. Pittelkow, T. A. Waldmann, Abnormal cytokine expression in Sézary and adult T-cell leukemia cells correlates with the functional diversity between these T-cell malignancies. Cancer Res. 54, 4430-4435 (1994).
18. R. Dummer, P. W. Heald, F. O. Nestle, E. Ludwig, E. Laine, S. Hemmi, G. Burg, Sézary syndrome T-cell clones display T-helper 2 cytokines and express the accessory factor-1 (interferon-γ receptor b-chain). Blood 88, 1383-1389 (1996).
19. E. K. Yoo, M. Cassin, S. R. Lessin, A. H. Rook, Complete molecular remission during biologic response modifier therapy for Sézary syndrome is associated with enhanced helper T type 1 cytokine production and natural killer cell activity. J. Am. Acad. Dermatol. 45, 208-216 (2001).
20. A. J. Coles, A. Cox, E. Le Page, J. Jones, S. A. Trip, J. Deans, S. Seaman, D. H. Miller, G. Hale, H. Waldmann, D. A. Compston, The window of therapeutic opportunity in multiple sclerosis: Evidence from monoclonal antibody therapy. J. Neurol. 253, 98-108 (2006).
21. J. D. Isaacs, R. A. Watts, B. L. Hazleman, G. Hale, M. T. Keogan, S. P. Cobbold, H. Waldmann, Humanised monoclonal antibody therapy for rheumatoid arthritis. Lancet 340, 748-752 (1992).
22. G. Hale, H. Waldmann, Recent results using CAMPATH-1 antibodies to control GVHD and graft rejection. Bone Marrow Transplant. 17, 305-308 (1996).
23. S. I. Martin, F. M. Marty, K. Fiumara, S. P. Treon, J. G. Gribben, L. R. Baden, Infectious complications associated with alemtuzumab use for lymphoproliferative disorders. Clin. Infect. Dis. 43, 16-24 (2006).
24. A. Nosari, A. Tedeschi, F. Ricci, M. Montillo, Characteristics and stage of the underlying diseases could determine the risk of opportunistic infections in patients receiving alemtuzumab. Haematologica 93, e30-e31 (2008).
25. J. L. Jones, A. J. Coles, Spotlight on alemtuzumab. Int. MS J. 16, 77-81 (2009).
26. C. Querfeld, N. Mehta, S. T. Rosen, J. Guitart, A. Rademaker, P. Gerami, T. M. Kuzel, Alemtuzumab for relapsed and refractory erythrodermic cutaneous T-cell lymphoma: A single institution experience from the Robert H. Lurie Comprehensive Cancer Center. Leuk. Lymphoma 50, 1969-1976 (2009).
27. L. Alinari, L. Geskin, T. Grady, R. A. Baiocchi, M. A. Bechtel, P. Porcu, Subcutaneous alemtuzumab for Sézary syndrome in the very elderly. Leuk. Res. 32, 1299-1303 (2008).
28. U. B. Ure, M. C. Ar, A. Salihoglu, S. I. Guner, A. Baran, O. Oguz, B. Ferhanoglu, Alemtuzumab in Sézary syndrome: Efficient but not innocent. Eur. J. Dermatol. 17, 525-529 (2007).
29. N. Roch, D. Salameire, R. Gressin, P. Morand, O. Epaulard, P. Pavese, J. P. Brion, J. P. Stahl, Fatal adenoviral and enteroviral infections and an Epstein-Barr virus positive large B-cell lymphoma after alemtuzumab treatment in a patient with refractory Sézary syndrome. Scand. J. Infect. Dis. 40, 343-346 (2008).
30. O. Gautschi, N. Blumenthal, M. Streit, M. Solenthaler, T. Hunziker, R. Zenhausern, Successful treatment of chemotherapy-refractory Sézary syndrome with alemtuzumab (Campath-1H). Eur. J. Haematol. 72, 61-63 (2004).
31. S. Capalbo, M. Delia, M. Dargenio, A. Liso, D. Diomede, L. Garofalo, V. Liso, Mycosis fungoides/Sézary syndrome: A report of three cases treated with Campath-1H as salvage treatment. Med. Oncol. 20, 389-396 (2003).
32. G. A. Kennedy, J. F. Seymour, M. Wolf, H. Januszewicz, J. Davison, C. McCormack, G. Ryan, H. M. Prince, Treatment of patients with advanced mycosis fungoides and Sézary syndrome with alemtuzumab. Eur. J. Haematol. 71, 250-256 (2003).
33. J. Lundin, H. Hagberg, R. Repp, E. Cavallin-Ståhl, S. Fredén, G. Juliusson, E. Rosenblad, G. Tjønnfjord, T. Wiklund, A. Osterborg, Phase 2 study of alemtuzumab (anti-CD52 monoclonal antibody) in patients with advanced mycosis fungoides/Sézary syndrome. Blood 101, 4267-4272 (2003).
34. A. Ferrajoli, S. M. O'Brien, J. E. Cortes, F. J. Giles, D. A. Thomas, S. Faderl, R. Kurzrock, S. Lerner, D. P. Kontoyiannis, M. J. Keating, Phase II study of alemtuzumab in chronic lymphoproliferative disorders. Cancer 98, 773-778 (2003).
35. J. Lundin, A. Osterborg, G. Brittinger, D. Crowther, H. Dombret, A. Engert, A. Epenetos, C. Gisselbrecht, D. Huhn, U. Jaeger, J. Thomas, R. Marcus, N. Nissen, C. Poynton, E. Rankin, R. Stahel, M. Uppenkamp, R. Willemze, H. Mellstedt, CAMPATH-1H monoclonal antibody in therapy for previously treated low-grade non-Hodgkin's lymphomas: A phase II multicenter study. European Study Group of CAMPATH-1H Treatment in Low-Grade Non-Hodgkin's Lymphoma. J. Clin. Oncol. 16, 3257-3263 (1998).
36. D. J. Lenihan, A. J. Alencar, D. Yang, R. Kurzrock, M. J. Keating, M. Duvic, Cardiac toxicity of alemtuzumab in patients withmycosis fungoides/Sézary syndrome. Blood 104, 655-658 (2004).
37. S. D. Gibbs, K. E. Herbert, C. McCormack, J. F. Seymour, H. M. Prince, Alemtuzumab: Effective monotherapy for simultaneous B-cell chronic lymphocytic leukaemia and Sézary syndrome. Eur. J. Haematol. 73, 447-449 (2004).
38. M. G. Bernengo, P. Quaglino, A. Comessatti, M. Ortoncelli, M. Novelli, F. Lisa, M. T. Fierro, Low-dose intermittent alemtuzumab in the treatment of Sézary syndrome: Clinical and immunologic findings in 14 patients. Haematologica 92, 784-794 (2007).
39. F. Lansigan, F. M. Foss, Current and emerging treatment strategies for cutaneous T-cell lymphoma. Drugs 70, 273-286 (2010).
40. Y. H. Kim, M. Duvic, E. Obitz, R. Gniadecki, L. Iversen, A. Osterborg, S. Whittaker, T. M. Illidge, T. Schwarz, R. Kaufmann, K. Cooper, K. M. Knudsen, S. Lisby, O. Baadsgaard, S. J. Knox, Clinical efficacy of zanolimumab (HuMax-CD4): Two phase 2 studies in refractory cutaneous T-cell lymphoma. Blood 109, 4655-4662 (2007).
41. D. A. Rider, C. E. Havenith, R. de Ridder, J. Schuurman, C. Favre, J. C. Cooper, S. Walker, O. Baadsgaard, S. Marschner, J. G. vandeWinkel, J. Cambier, P. W. Parren, D. R. Alexander, A human CD4 monoclonal antibody for the treatment of T-cell lymphoma combines inhibition of T-cell signaling by a dual mechanism with potent Fc-dependent effector activity. Cancer Res. 67, 9945-9953 (2007).
42. C. R. Mackay, W. L. Marston, L. Dudler, Naive and memory T cells show distinct pathways of lymphocyte recirculation. J. Exp. Med. 171, 801-817 (1990).
43. J. L. Whitton, J. Zhang, Principles of cytotoxic T lymphocyte induction and recognition. Curr. Top. Microbiol. Immunol. 202, 247-259 (1995).
44. D. L. Woodland, J. E. Kohlmeier, Migration, maintenance and recall of memory T cells in peripheral tissues. Nat. Rev. Immunol. 9, 153-161 (2009).
45. L. Liu, Q. Zhong, T. Tian, K. Dubin, S. K. Athale, T. S. Kupper, Epidermal injury and infection during poxvirus immunization is crucial for the generation of highly protective T cell-mediated immunity. Nat. Med. 16, 224-227 (2010).
46. E. S. Razvi, Z. Jiang, B. A. Woda, R. M. Welsh, Lymphocyte apoptosis during the silencing of the immune response to acute viral infections in normal, lpr, and Bcl-2-transgenic mice. Am. J. Pathol. 147, 79-91 (1995).
47. T. Gebhardt, L. M. Wakim, L. Eidsmo, P. C. Reading, W. R. Heath, F. R. Carbone, Memory T cells in nonlymphoid tissue that provide enhanced local immunity during infection with herpes simplex virus. Nature Immunol. 10, 524-530 (2009).
48. R. A. Clark, Skin resident T cells: The ups and downs of on site immunity. J. Invest. Dermatol. 130, 362-370 (2010).
49. R. A. Clark, B. F. Chong, N. Mirchandani, K. Yamanaka, G. F. Murphy, R. K. Dowgiert, T. S. Kupper, A novel method for the isolation of skin resident T cells from normal and diseased human skin. J. Invest. Dermatol. 126, 1059-1070 (2006).
50. L. Riechmann, M. Clark, H. Waldmann, G. Winter, Reshaping human antibodies for therapy. Nature 332, 323-327 (1988).
51. H. E. Chan, I. Jilani, R. Chang, M. Albitar, Measuring humanized antibodies in plasma of patients treated with antibody-based therapy using bead-based flow cytometry: The story of alemtuzumab. Methods Mol. Biol. 378, 159-165 (2007).