Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

T-cell therapy in the treatment of post-transplant lymphoproliferative disease

Nature Reviews Clinical Oncology volume 9, pages 510–519 (2012)Cite this article

Subjects

Abstract

Post-transplant lymphoproliferative diseases (PTLD) associated with Epstein-Barr virus (EBV) infection often develop after organ and haematopoietic stem-cell transplantation. These lymphoproliferative diseases are tumours that usually express all latent EBV viral proteins, and are therefore amenable to T-cell-based immune therapies, such as donor lymphocyte infusions and the adoptive transfer of EBV-specific cytotoxic T lymphocytes. In this Review, we describe current approaches of T-cell-based therapies to treat PTLD, and describe strategies that improve the feasibility of such treatment.

Key Points

  • Uncontrolled growth of Epstein-Barr virus (EBV)-infected B cells in patients after haematopoietic or solid organ transplants, due to immunosuppression or depletion of virus-specific T cells, can result in high-grade EBV lymphomas

  • Transplantation of EBV-specific cytotoxic T lymphocytes (CTLs) derived from the donor has effectively prevented EBV-associated post-transplant lymphoproliferative disease (PTLD), inducing complete responses in over 70% of patients with this complication

  • Treatment with closely matched EBV-CTLs from third-party donors can lead to responses in over 50% of such cases

  • Failure to respond to CTLs occurs when T cells of restricted specificity are infused or tumours express variants of EBV antigens used to stimulate CTLs

  • Novel methods for the rapid production of EBV-specific T cells and increased commercial interest should make EBV-specific T cells more readily available to transplant recipients in the future

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: EBV cycle, latency states and lymphoma.
Figure 2: EBV-specific CTL production.

Similar content being viewed by others

References

  1. Gottschalk, S., Rooney, C. M. & Heslop, H. E. Post-transplant lymphoproliferative disorders. Annu. Rev. Med. 56, 29–44 (2005).

    CAS  PubMed  Google Scholar 

  2. Cohen, J. I. Epstein-Barr virus infection. N. Engl. J. Med. 343, 481–492 (2000).

    CAS  PubMed  Google Scholar 

  3. Hislop, A. D., Taylor, G. S., Sauce, D. & Rickinson, A. B. Cellular responses to viral infection in humans: lessons from Epstein-Barr virus. Annu. Rev. Immunol. 25, 587–617 (2007).

    CAS  PubMed  Google Scholar 

  4. Khanna, R., Moss, D. & Gandhi, M. Technology insight: Applications of emerging immunotherapeutic strategies for Epstein-Barr virus-associated malignancies. Nat. Clin. Pract. Oncol. 2, 138–149 (2005).

    CAS  PubMed  Google Scholar 

  5. Heslop, H. E. et al. Long-term outcome of EBV-specific T-cell infusions to prevent or treat EBV-related lymphoproliferative disease in transplant recipients. Blood 115, 925–935 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Doubrovina, E. et al. Adoptive immunotherapy with unselected or EBV-specific T cells for biopsy-proven EBV+ lymphomas after allogeneic hematopoietic cell transplantation. Blood 119, 2644–2656 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Haque, T. et al. Allogeneic cytotoxic T-cell therapy for EBV-positive posttransplantation lymphoproliferative disease: results of a phase 2 multicenter clinical trial. Blood 110, 1123–1131 (2007).

    CAS  PubMed  Google Scholar 

  8. Long, H. M., Taylor, G. S. & Rickinson, A. B. Immune defence against EBV and EBV-associated disease. Curr. Opin. Immunol. 23, 258–264 (2011).

    CAS  PubMed  Google Scholar 

  9. Babcock, G. J., Decker, L. L., Freeman, R. B. & Thorley-Lawson, D. A. Epstein-Barr virus-infected resting memory B cells, not proliferating lymphoblasts, accumulate in the peripheral blood of immunosuppressed patients. J. Exp. Med. 190, 567–576 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Thorley-Lawson, D. A., Duca, K. A. & Shapiro, M. Epstein-Barr virus: a paradigm for persistent infection - for real and in virtual reality. Trends Immunol. 29, 195–201 (2008).

    CAS  PubMed  Google Scholar 

  11. Thorley-Lawson, D. A. & Gross, A. Persistence of the Epstein-Barr virus and the origins of associated lymphomas. N. Engl. J. Med. 350, 1328–1337 (2004).

    CAS  PubMed  Google Scholar 

  12. Abu-Elmagd, K. M. et al. Lymphoproliferative disorders and de novo malignancies in intestinal and multivisceral recipients: improved outcomes with new outlooks. Transplantation 88, 926–934 (2009).

    PubMed  Google Scholar 

  13. Babcock, G. J., Decker, L. L., Freeman, R. B. & Thorley-Lawson, D. A. Epstein-Barr virus-infected resting memory B cells, not proliferating lymphoblasts, accumulate in the peripheral blood of immunosuppressed patients. J. Exp. Med. 190, 567–576 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Swerdlow, S. H., Webber, S. A., Chadburn, A. & Ferry, J. Post transplant lymphoproliferative disorders in Classification of Tumours of Haematopoietic and Lymphoid Tissues, 4th edn (eds Swerdlow, S. H., Campo, E. & Harris, N. L) 342–349 (International Agency for Research on Cancer, Lyon, 2008).

    Google Scholar 

  15. Meij, P. et al. Impaired recovery of Epstein-Barr virus (EBV)-specific CD8+ T lymphocytes after partially T-depleted allogeneic stem cell transplantation may identify patients at very high risk for progressive EBV reactivation and lymphoproliferative disease. Blood 101, 4290–4297 (2003).

    CAS  PubMed  Google Scholar 

  16. Brunstein, C. G. et al. Marked increased risk of Epstein-Barr virus-related complications with the addition of antithymocyte globulin to a nonmyeloablative conditioning prior to unrelated umbilical cord blood transplantation. Blood 108, 2874–2880 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Cohen, J. et al. Increased incidence of EBV-related disease following paediatric stem cell transplantation with reduced-intensity conditioning. Br. J. Haematol. 129, 229–239 (2005).

    PubMed  Google Scholar 

  18. Landgren, O. et al. Risk factors for lymphoproliferative disorders after allogeneic hematopoietic cell transplantation. Blood 113, 4992–5001 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Swinnen, L. J. et al. Prospective study of sequential reduction in immunosuppression, interferon alpha-2B, and chemotherapy for posttransplantation lymphoproliferative disorder. Transplantation 86, 215–222 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Gross, T. G., Savoldo, B. & Punnett, A. Posttransplant lymphoproliferative diseases. Pediatr. Clin. North Am. 57, 481–503 (2010).

    PubMed  Google Scholar 

  21. Dotti, G. et al. Epstein-Barr virus-negative lymphoproliferate disorders in long-term survivors after heart, kidney, and liver transplant. Transplantation 69, 827–833 (2000).

    CAS  PubMed  Google Scholar 

  22. Dotti, G. et al. Lymphomas occurring late after solid-organ transplantation: influence of treatment on the clinical outcome. Transplantation 74, 1095–1102 (2002).

    PubMed  Google Scholar 

  23. Heslop, H. E. How I treat EBV lymphoproliferation. Blood 114, 4002–4008 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Parker, A. et al. Diagnosis of post-transplant lymphoproliferative disorder in solid organ transplant recipients - BCSH and BTS Guidelines. Br. J. Haematol. 149, 675–692 (2010).

    PubMed  Google Scholar 

  25. Gulley, M. L. & Tang, W. Using Epstein-Barr viral load assays to diagnose, monitor, and prevent posttransplant lymphoproliferative disorder. Clin. Microbiol. Rev. 23, 350–366 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Parker, A. et al. Management of post-transplant lymphoproliferative disorder in adult solid organ transplant recipients - BCSH and BTS Guidelines. Br. J. Haematol. 149, 693–705 (2010).

    PubMed  Google Scholar 

  27. Styczynski, J. et al. Management of HSV, VZV and EBV infections in patients with hematological malignancies and after SCT: guidelines from the Second European Conference on Infections in Leukemia. Bone Marrow Transplant. 43, 757–770 (2009).

    CAS  PubMed  Google Scholar 

  28. Tomblyn, M. et al. Guidelines for preventing infectious complications among hematopoietic cell transplantation recipients: a global perspective. Biol. Blood Marrow Transplant. 15, 1143–1238 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Zelenetz, A. D. et al. NCCN Clinical Practice Guidelines in Oncology: non-Hodgkin's lymphomas. J. Natl Compr. Canc. Netw. 8, 288–334 (2010).

    PubMed  Google Scholar 

  30. Kuehnle, I. et al. CD20 monoclonal antibody (rituximab) for therapy of Epstein-Barr virus lymphoma after hemopoietic stem-cell transplantation. Blood 95, 1502–1505 (2000).

    CAS  PubMed  Google Scholar 

  31. van Esser, J. W. et al. Prevention of Epstein-Barr virus-lymphoproliferative disease by molecular monitoring and preemptive rituximab in high-risk patients after allogeneic stem cell transplantation. Blood 99, 4364–4369 (2002).

    CAS  PubMed  Google Scholar 

  32. Carpenter, P. A. et al. A humanized non-FcR-binding anti-CD3 antibody, visilizumab, for treatment of steroid-refractory acute graft-versus-host disease. Blood 99, 2712–2719 (2002).

    CAS  PubMed  Google Scholar 

  33. Savoldo, B. et al. Cellular immunity to Epstein-Barr virus in liver transplant recipients treated with rituximab for post-transplant lymphoproliferative disease. Am. J. Transplant. 5, 566–572 (2005).

    CAS  PubMed  Google Scholar 

  34. Khanna, R. et al. Activation and adoptive transfer of Epstein-Barr virus-specific cytotoxic T cells in solid organ transplant patients with posttransplant lymphoproliferative disease. Proc. Natl Acad. Sci. USA 96, 10391–10396 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Comoli, P. et al. Infusion of autologous Epstein-Barr virus (EBV)-specific cytotoxic T cells for prevention of EBV-related lymphoproliferative disorder in solid organ transplant recipients with evidence of active virus replication. Blood 99, 2592–2598 (2002).

    CAS  PubMed  Google Scholar 

  36. Savoldo, B. et al. Treatment of solid organ transplant recipients with autologous Epstein-Barr virus-specific cytotoxic T lymphocytes (CTLs). Blood 108, 2942–2949 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Bollard, C. M. et al. Complete responses of relapsed lymphoma following genetic modification of tumor-antigen presenting cells and T-lymphocyte transfer. Blood 110, 2838–2845 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Thorley-Lawson, D. A. & Allday, M. J. The curious case of the tumour virus: 50 years of Burkitt's lymphoma. Nat. Rev. Microbiol. 6, 913–924 (2008).

    CAS  PubMed  Google Scholar 

  39. Heslop, H. E., Brenner, M. K. & Rooney, C. M. Donor T-cells to treat EBV-associated lymphoma. N. Engl. J. Med. 331, 679–680 (1994).

    CAS  PubMed  Google Scholar 

  40. O'Reilly, R. J. et al. Biology and adoptive cell therapy of Epstein-Barr virus-associated lymphoproliferative disorders in recipients of marrow allografts. Immunol. Rev. 157, 195–216 (1997).

    CAS  PubMed  Google Scholar 

  41. Ciceri, F. et al. Infusion of suicide-gene-engineered donor lymphocytes after family haploidentical haemopoietic stem-cell transplantation for leukaemia (the TK007 trial): a non-randomised phase I-II study. Lancet Oncol. 10, 489–500 (2009).

    PubMed  Google Scholar 

  42. Di Stasi, A. et al. Inducible apoptosis as a safety switch for adoptive cell therapy. N. Engl. J. Med. 365, 1673–1683 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Heslop, H. E. et al. Long-term outcome of EBV-specific T-cell infusions to prevent or treat EBV-related lymphoproliferative disease in transplant recipients. Blood 115, 925–935 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Gottschalk, S. et al. An Epstein-Barr virus deletion mutant that causes fatal lymphoproliferative disease unresponsive to virus-specific T cell therapy. Blood 97, 835–843 (2001).

    CAS  PubMed  Google Scholar 

  45. Sherritt, M. A. et al. Reconstitution of the latent T-lymphocyte response to Epstein-Barr virus is coincident with long-term recovery from posttransplant lymphoma after adoptive immunotherapy. Transplantation 75, 1556–1560 (2003).

    PubMed  Google Scholar 

  46. Peggs, K. S. et al. Adoptive cellular therapy for early cytomegalovirus infection after allogeneic stem-cell transplantation with virus-specific T-cell lines. Lancet 362, 1375–1377 (2003).

    PubMed  Google Scholar 

  47. Bollard, C. M. et al. Adapting a transforming growth factor beta-related tumor protection strategy to enhance antitumor immunity. Blood 99, 3179–3187 (2002).

    CAS  PubMed  Google Scholar 

  48. Smith, C. A. et al. Production of genetically modified EBV-specific cytotoxic T cells for adoptive transfer to patients at high risk of EBV-associated lymphoproliferative disease. J. Hematother. 4, 73–79 (1995).

    CAS  PubMed  Google Scholar 

  49. Peggs, K. S. et al. Directly selected cytomegalovirus-reactive donor T cells confer rapid and safe systemic reconstitution of virus-specific immunity following stem cell transplantation. Clin. Infect. Dis. 52, 49–57 (2011).

    CAS  PubMed  Google Scholar 

  50. Feuchtinger, T. et al. Adoptive transfer of pp65-specific T cells for the treatment of chemorefractory cytomegalovirus disease or reactivation after haploidentical and matched unrelated stem cell transplantation. Blood 116, 4360–4367 (2010).

    CAS  PubMed  Google Scholar 

  51. Moosmann, A. et al. Effective and long-term control of EBV PTLD after transfer of peptide-selected T cells. Blood 115, 2960–2970 (2010).

    CAS  PubMed  Google Scholar 

  52. Schmitt, A. et al. Adoptive transfer and selective reconstitution of streptamer-selected cytomegalovirus-specific CD8+ T cells leads to virus clearance in patients after allogeneic peripheral blood stem cell transplantation. Transfusion 51, 591–599 (2011).

    CAS  PubMed  Google Scholar 

  53. Neudorfer, J. et al. Reversible HLA multimers (streptamers) for the isolation of human cytotoxic T lymphocytes functionally active against tumor- and virus-derived antigens. J. Immunol. Methods 320, 119–131 (2007).

    CAS  PubMed  Google Scholar 

  54. Cobbold, M. et al. Adoptive transfer of cytomegalovirus-specific CTL to stem cell transplant patients after selection by HLA-peptide tetramers. J. Exp. Med. 202, 379–386 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Gerdemann, U. et al. Nucleofection of DCs to generate multivirus-specific T cells for prevention or treatment of viral infections in the immunocompromised host. Mol. Ther. 17, 1616–1625 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Uhlin, M. et al. A novel haplo-identical adoptive CTL therapy as a treatment for EBV-associated lymphoma after stem cell transplantation. Cancer Immunol. Immunother. 59, 473–477 (2010).

    PubMed  Google Scholar 

  57. Gerdemann, U. et al. Nucleofection of DCs to generate multi virus-specific T cells for prevention or treatment of viral infections in the immunocompromised host. Mol. Ther. 17, 1616–1625 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Gerdemann, U. et al. Adoptive transfer of rapidly-generated multi virus-specific T-cells to treat adenovirus, EBV and CMV infections of hematopoietic stem cell transplant recipients [abstract]. Biol. Blood Marrow Transplant. 18, 219 (2012).

    Google Scholar 

  59. Gerdemann, U. et al. Rapidly-generated multivirus-specific cytotoxic T lymphocytes for the prophylaxis and treatment of viral infections. Mol. Ther. (in press).

  60. Schmitt, A. et al. Adoptive transfer and selective reconstitution of streptamer-selected cytomegalovirus-specific CD8+ T cells leads to virus clearance in patients after allogeneic peripheral blood stem cell transplantation. Transfusion 51, 591–599 (2011).

    CAS  PubMed  Google Scholar 

  61. Young, L. S. & Rickinson, A. B. Epstein-Barr virus: 40 years on. Nat. Rev. Cancer 4, 757–768 (2004).

    CAS  PubMed  Google Scholar 

  62. Burrows, S. R., Khanna, R., Burrows, J. M. & Moss, D. J. An alloresponse in humans is dominated by cytotoxic T lymphocytes (CTL) cross-reactive with a single Epstein-Barr virus CTL epitope: implications for graft-versus-host disease. J. Exp. Med. 179, 1155–1161 (1994).

    CAS  PubMed  Google Scholar 

  63. Amir, A. L. et al. Allo-HLA reactivity of virus-specific memory T cells is common. Blood 115, 3146–3157 (2010).

    CAS  PubMed  Google Scholar 

  64. Melenhorst, J. J. et al. Allogeneic virus-specific T cells with HLA alloreactivity do not produce GVHD in human subjects. Blood 116, 4700–4702 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Haque, T. et al. Complete regression of posttransplant lymphoproliferative disease using partially HLA-matched Epstein Barr virus-specific cytotoxic T cells. Transplantation 72, 1399–1402 (2001).

    CAS  PubMed  Google Scholar 

  66. Haque, T. et al. Treatment of Epstein-Barr-virus-positive post-transplantation lymphoproliferative disease with partly HLA-matched allogeneic cytotoxic T cells. Lancet 360, 436–442 (2002).

    PubMed  Google Scholar 

  67. Sun, Q., Burton, R., Reddy, V. & Lucas, K. G. Safety of allogeneic Epstein-Barr virus (EBV)-specific cytotoxic T lymphocytes for patients with refractory EBV-related lymphoma. Br. J. Haematol. 118, 799–808 (2002).

    PubMed  Google Scholar 

  68. Barker, J. N. et al. Successful treatment of EBV-associated posttransplantation lymphoma after cord blood transplantation using third-party EBV-specific cytotoxic T lymphocytes. Blood 116, 5045–5049 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Leen, A. M. et al. Monoculture-derived T lymphocytes specific for multiple viruses expand and produce clinically relevant effects in immunocompromised individuals. Nat. Med. 12, 1160–1166 (2006).

    CAS  PubMed  Google Scholar 

  70. Leen, A. M. et al. Most closely HLA-matched allogeneic virus specific cytotoxic T-lymphocytes (CTL) to treat persistent reactivation or infection with adenovirus, CMV and EBV after hematopoietic stem cell transplantation (HSCT) [abstract]. Blood 116 (Suppl.), a829 (2010).

    Google Scholar 

  71. Brewin, J. et al. Generation of EBV-specific cytotoxic T cells that are resistant to calcineurin inhibitors for the treatment of posttransplantation lymphoproliferative disease. Blood 114, 4792–4803 (2009).

    CAS  PubMed  Google Scholar 

  72. De Angelis, B. et al. Generation of Epstein-Barr virus-specific cytotoxic T lymphocytes resistant to the immunosuppressive drug tacrolimus (FK506). Blood 114, 4784–4791 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Huye, L. E. et al. Combining mTOR inhibitors with rapamycin-resistant T cells: a two-pronged approach to tumor elimination. Mol. Ther. 19, 2239–2248 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Rooney, C. M. et al. Infusion of cytotoxic T cells for the prevention and treatment of Epstein-Barr virus-induced lymphoma in allogeneic transplant recipients. Blood 92, 1549–1555 (1998).

    CAS  PubMed  Google Scholar 

  75. Heslop, H. E. et al. Long-term restoration of immunity against Epstein-Barr virus infection by adoptive transfer of gene-modified virus-specific T lymphocytes. Nat. Med. 2, 551–555 (1996).

    CAS  PubMed  Google Scholar 

  76. Rooney, C. M. et al. Use of gene-modified virus-specific T-lymphocytes to control Epstein-Barr virus-related lymphoproliferation. Lancet 345, 9–13 (1995).

    CAS  PubMed  Google Scholar 

  77. Papadopoulos, E. B. et al. Infusions of donor leukocytes to treat Epstein-Barr virus-associated lymphoproliferative disorders after allogeneic bone marrow transplantation. N. Engl. J. Med. 330, 1185–1191 (1994).

    CAS  PubMed  Google Scholar 

  78. Gustafsson, A. et al. Epstein-Barr virus (EBV) load in bone marrow transplant recipients at risk to develop posttransplant lymphoproliferative disease: prophylactic infusion of EBV-specific cytotoxic T cells. Blood 95, 807–814 (2000).

    CAS  PubMed  Google Scholar 

  79. Lucas, K. G. et al. Semiquantitative Epstein-Barr virus (EBV) polymerase chain reaction for the determination of patients at risk for EBV-induced lymphoproliferative disease after stem cell transplantation. Blood 91, 3654–3661 (1998).

    CAS  PubMed  Google Scholar 

  80. Imashuku, S. et al. Unsuccessful CTL transfusion in a case of post-BMT Epstein-Barr virus-associated lymphoproliferative disorder (EBV-LPD). Bone Marrow Transplant. 20, 337–340 (1998).

    Google Scholar 

  81. Comoli, P. et al. Preemptive therapy of EBV-related lymphoproliferative disease after pediatric haploidentical stem cell transplantation. Am. J. Transplant. 7, 1648–1655 (2007).

    CAS  PubMed  Google Scholar 

  82. Haque, T. et al. Reconstitution of EBV-specific T cell immunity in solid organ transplant recipients. J. Immunol. 160, 6204–6209 (1998).

    CAS  PubMed  Google Scholar 

  83. Comoli, P. et al. Treatment of EBV-related post-renal transplant lymphoproliferative disease with a tailored regimen including EBV-specific T-cells. Am. J. Transplant. 5, 1415–1422 (2005).

    PubMed  Google Scholar 

  84. Gandhi, M. K. et al. Immunity, homing and efficacy of allogeneic adoptive immunotherapy for posttransplant lymphoproliferative disorders. Am. J. Transplant. 7, 1293–1299 (2007).

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by grants P01CA094237, P50CA126752 and U54HL08100 from the NIH and a SCOR award from the Leukemia and Lymphoma Society.

Author information

Authors and Affiliations

  1. Departments of Pediatrics and Medicine, Center for Cell and Gene Therapy, Baylor College of Medicine, The Methodist Hospital and Texas Children's Hospital, 1102 Bates Street, Houston, 77030, TX, USA

    Catherine M. Bollard, Cliona M. Rooney & Helen E. Heslop

Authors
  1. Catherine M. Bollard
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cliona M. Rooney
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Helen E. Heslop
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to researching the data for the article, and provided a substantial contribution to the discussion of the content and to the writing and editing of the manuscript before submission.

Corresponding author

Correspondence to Catherine M. Bollard.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bollard, C., Rooney, C. & Heslop, H. T-cell therapy in the treatment of post-transplant lymphoproliferative disease. Nat Rev Clin Oncol 9, 510–519 (2012). https://doi.org/10.1038/nrclinonc.2012.111

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrclinonc.2012.111

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing