Isolation of highly suppressive CD25 +FoxP3+ T regulatory cells from G-CSF-mobilized donors with retention of cytotoxic anti-viral CTLs: Application for multi-functional immunotherapy post stem cell transplantation

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Samuel, Edward R ^a   Beloki, Lorea ^b   Newton, Katy ^c   Mackinnon, Stephen ^a   Lowdell, Mark W ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b Atención Primaria Y Promoción de La Salud   (Spain)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; GRANULOCYTE COLONY STIMULATING FACTOR; GRANZYME B; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CD25+ T LYMPHOCYTE; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL COUNT; CELL FUNCTION; CELL ISOLATION; CELL POPULATION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOMEGALOVIRUS; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY; FEASIBILITY STUDY; HUMAN; HUMAN CELL; IMMUNOTHERAPY; NORMAL HUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; STEM CELL TRANSPLANTATION;

CELL PROLIFERATION; CELL SEPARATION; CYTOKINES; CYTOMEGALOVIRUS; FORKHEAD TRANSCRIPTION FACTORS; GRANULOCYTE COLONY-STIMULATING FACTOR; HEMATOPOIETIC STEM CELL MOBILIZATION; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; IMMUNOMAGNETIC SEPARATION; IMMUNOTHERAPY; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; PHOSPHOPROTEINS; SPECIES SPECIFICITY; T-LYMPHOCYTES, CYTOTOXIC; TISSUE DONORS; TRANSPLANTATION, AUTOLOGOUS; VIRAL MATRIX PROTEINS;

EID: 84898626297     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0085911     Document Type: Article

References (48)

1. Chakrabarti S, Mackinnon S, Chopra R, Kottaridis PD, Peggs K, et al. (2002) High incidence of cytomegalovirus infection after nonmyeloablative stem cell transplantation: potential role of Campath-1H in delaying immune reconstitution. Blood 99: 4357-4363. (Pubitemid 34627201)
2. Gooley TA, Chien JW, Pergam SA, Hingorani S, Sorror ML, et al. (2010) Reduced mortality after allogeneic hematopoietic-cell transplantation. N Engl J Med 363: 2091-2101.
3. Reusser P, Riddell SR, Meyers JD, Greenberg PD (1991) Cytotoxic T-lymphocyte response to cytomegalovirus after human allogeneic bone marrow transplantation: pattern of recovery and correlation with cytomegalovirus infection and disease. Blood 78: 1373-1380.
4. Cobbold M, Khan N, Pourgheysari B, Tauro S, McDonald D, et al. (2005) Adoptive transfer of cytomegalovirus-specific CTL to stem cell transplant patients after selection by HLA-peptide tetramers. J Exp Med 202: 379-386. (Pubitemid 41126955)
5. Einsele H, Roosnek E, Rufer N, Sinzger C, Riegler S, et al. (2002) Infusion of cytomegalovirus (CMV)-specific T cells for the treatment of CMV infection not responding to antiviral chemotherapy. Blood 99: 3916-3922. (Pubitemid 35332029)
6. Leen AM, Myers GD, Sili U, Huls MH, Weiss H, et al. (2006) Monoculture-derived T lymphocytes specific for multiple viruses expand and produce clinically relevant effects in immunocompromised individuals. Nat Med 12: 1160-1166. (Pubitemid 44527351)
7. Micklethwaite K, Hansen A, Foster A, Snape E, Antonenas V, et al. (2007) Ex vivo expansion and prophylactic infusion of CMV-pp65 peptide-specific cytotoxic T-lymphocytes following allogeneic hematopoietic stem cell transplantation. Biol Blood Marrow Transplant 13: 707-714. (Pubitemid 46767999)
8. Peggs KS, Verfuerth S, Pizzey A, Khan N, Guiver M, et al. (2003) Adoptive cellular therapy for early cytomegalovirus infection after allogeneic stem-cell transplantation with virus-specific T-cell lines. Lancet 362: 1375-1377. (Pubitemid 37338339)
9. Riddell SR, Watanabe KS, Goodrich JM, Li CR, Agha ME, et al. (1992) Restoration of viral immunity in immunodeficient humans by the adoptive transfer of T cell clones. Science 257: 238-241.
10. Walter EA, Greenberg PD, Gilbert MJ, Finch RJ, Watanabe KS, et al. (1995) Reconstitution of cellular immunity against cytomegalovirus in recipients of allogeneic bone marrow by transfer of T-cell clones from the donor. N Engl J Med 333: 1038-1044.
11. Feuchtinger T, Opherk K, Bethge WA, Topp MS, Schuster FR, et al. (2010) Adoptive transfer of pp65-specific T cells for the treatment of chemorefractory cytomegalovirus disease or reactivation after haploidentical and matched unrelated stem cell transplantation. Blood116: 4360-4367.
12. Peggs KS, Thomson K, Samuel E, Dyer G, Armoogum J, et al. (2010) 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.
13. Moosmann A, Bigalke I, Tischer J, Schirrmann L, Kasten J, et al. (2010) Effective and long-term control of EBV PTLD after transfer of peptide-selected T cells. Blood 115: 2960-2970.
14. Feuchtinger T, Lang P, Hamprecht K, Schumm M, Greil J, et al. (2004) Isolation and expansion of human adenovirus-specific CD4+ and CD8+ T cells according to IFN-gamma secretion for adjuvant immunotherapy. Exp Hematol 32: 282-289. (Pubitemid 38328534)
15. Chattopadhyay PK, Yu J, Roederer M. (2005) A live-cell assay to detect antigen-specific CD4+ T cells with diverse cytokine profiles. Nat Med 11: 1113-1117. (Pubitemid 41486835)
16. Frentsch M, Arbach O, Kirchhoff D, Moewes B, Worm M, et al. (2005) Direct access to CD4+ T cells specific for defined antigens according to CD154 expression. Nat Med 11: 1118-1124. (Pubitemid 41486836)
17. Gallot G, Vivien R, Ibisch C, Lule J, Davrinche C, et al. (2001) Purification of Ag-specific T lymphocytes after direct peripheral blood mononuclear cell stimulation followed by CD25 selection. I. Application to CD4(+) or CD8(+) cytomegalovirus phosphoprotein pp65 epitope determination. J Immunol 167: 4196-4206. (Pubitemid 32954292)
18. Watanabe K, Suzuki S, Kamei M, Toji S, Kawase T, et al. (2008) CD137-guided isolation and expansion of antigen-specific CD8 cells for potential use in adoptive immunotherapy. Int J Hematol 88: 311-320.
19. Wehler TC, Karg M, Distler E, Konur A, Nonn M, et al. (2008) Rapid identification and sorting of viable virus-reactive CD4(+) and CD8(+) T cells based on antigen-triggered CD137 expression. J Immunol Methods 339: 23-37.
20. Wolfl M, Kuball J, Ho WY, Nguyen H, Manley TJ, et al. (2007) 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 110: 201-210. (Pubitemid 47026836)
21. Lugthart G, Albon SJ, Ricciardelli I, Kester MG, Meij P, et al. (2012) Simultaneous generation of multivirus-specific and regulatory T cells for adoptive immunotherapy. J Immunother 35: 42-53.
22. Powell DJ, Parker LL, Rosenberg SA (2005) Large-Scale Depletion of CD25+ Regulatory T Cells from Patient Leukapheresis Samples. J Immunother 28: 403-411. (Pubitemid 40962335)
23. Arpinati M, Green CL, Heimfeld S, Heuser JE, Anasetti C (2000) Granulocyte-colony stimulating factor mobilizes T helper 2-inducing dendritic cells. Blood 95: 2484-2490. (Pubitemid 30210524)
24. Kitabayashi A, Hirokawa M, Hatano Y, Lee M, Kuroki J, et al. (1995) Granulocyte colony-stimulating factor downregulates allogeneic immune responses by posttranscriptional inhibition of tumor necrosis factor-alpha production. Blood 86: 2220-2227.
25. Pan L, Teshima T, Hill GR, Bungard D, Brinson YS, et al. (1999) Granulocyte colony-stimulating factor-mobilized allogeneic stem cell transplantation maintains graft-versus-leukemia effects through a perforin-dependent pathway while preventing graft-versus-host disease. Blood 93: 4071-4078. (Pubitemid 29279248)
26. Sloand EM, Kim S, Maciejewski JP, van RF, Chaudhuri A, et al. (2000) Pharmacologic doses of granulocyte colony-stimulating factor affect cytokine production by lymphocytes in vitro and in vivo. Blood 95: 2269-2274. (Pubitemid 30167724)
27. Tayebi H, Kuttler F, Saas P, Lienard A, Petracca B, et al. (2001) Effect of granulocyte colony-stimulating factor mobilization on phenotypical and functional properties of immune cells. Exp Hematol 29: 458-470. (Pubitemid 32297670)
28. Toh HC, Sun L, Soe Y, Wu Y, Phoon YP, et al. (2009) G-CSF induces a potentially tolerant gene and immunophenotype profile in T cells in vivo. Clin Immunol 132: 83-92.
29. Abbi KK, Zhu J, Ehmann WC, Epner E, Carraher M, et al. (2013) G-CSF mobilized vs conventional donor lymphocytes for therapy of relapse or incomplete engraftment after allogeneic hematopoietic transplantation. Bone Marrow Transplant 48: 357-362.
30. Levine JE, Braun T, Penza SL, Beatty P, Cornetta K, et al. (2002) Prospective trial of chemotherapy and donor leukocyte infusions for relapse of advanced myeloid malignancies after allogeneic stem-cell transplantation. J Clin Oncol 20: 405-412. (Pubitemid 34072522)
31. Samuel ER, Newton K, Mackinnon S, Lowdell MW (2013) Successful isolation and expansion of CMV-reactive T cells from G-CSF mobilized donors that retain a strong cytotoxic effector function. Br J Haematol 160: 87-100.
32. Clancy LE, Blyth E, Simms R, Micklethwaite KP, Kris Ma CK, et al. (2013) Cytomegalovirus-Specific Cytotoxic T Lymphocytes Can Be Efficiently Expanded from Granulocyte Colony-Stimulating Factor-Mobilized Hemopoietic Progenitor Cell Products ex Vivo and Safely Transferred to Stem Cell Transplantation Recipients to Facilitate Immune Reconstitution. Biol Blood Marrow Transplant 19: 725-734.
33. Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M (1995) Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J Immunol 155: 1151-1164.
34. Sakaguchi S (2004) Naturally arising CD4+ regulatory t cells for immunologic self-tolerance and negative control of immune responses. Annu Rev Immunol 22: 531-562.
35. Fontenot JD, Gavin MA, Rudensky AY (2012) Foxp3 programs the development and function of CD4 +CD25+ regulatory T cells. Nat Immunol 4: 330-336.
36. Ukena SN, Velaga S, Goudeva L, Ivanyi P, Olek S, et al. (2012) Human Regulatory T Cells of G-CSF Mobilized Allogeneic Stem Cell Donors Qualify for Clinical Application. PLoS One 7: e51644.
37. Brincks EL, Roberts AD, Cookenham T, Sell S, Kohlmeier JE, et al. (2013) Antigen-Specific Memory Regulatory CD4+Foxp3+ T Cells Control Memory Responses to Influenza Virus Infection. J Immunol 190: 3438-3446.
38. Litjens NH, Boer K, Betjes MG (2012) Identification of circulating human antigen-reactive CD4+ FOXP3+ natural regulatory T cells. J Immunol 188: 1083-1090.
39. Melenhorst JJ, Scheinberg P, Lu J, Ambrozak DR, Sosa E,et al. (2008) Regulatory T-cell depletion does not prevent emergence of new CD25+ FOXP3+ lymphocytes after antigen stimulation in culture. Cytotherapy 10: 152-164.
40. Suffia IJ, Reckling SK, Piccirillo CA, Goldszmid RS, Belkaid Y (2006) Infected site-restricted Foxp3+ natural regulatory T cells are specific for microbial antigens. J Exp Med 203: 777-788.
41. Tovar-Salazar A, Patterson-Bartlett J, Jesser R, Weinberg A (2010) Regulatory function of cytomegalovirus-specific CD4+CD27-. Virology 398: 158-167.
42. Walker MR, Carson BD, Nepom GT, Ziegler SF, Buckner JH (2005) De novo generation of antigen-specific CD4+CD25+ regulatory T cells from human CD4+. Proc Natl Acad Sci U S A 102: 4103-4108.
43. Nguyen VH, Shashidhar S, Chang DS, Ho L, Kambham N, et al. (2008) The impact of regulatory T cells on T-cell immunity following hematopoietic cell transplantation. Blood 111: 945-953.
44. Di IM, Falzetti F, Carotti A, Terenzi A, Castellino F, et al. (2011) Tregs prevent GVHD and promote immune reconstitution in HLA-haploidentical transplantation. Blood 117: 3921-3928.
45. Adeegbe DO, Nishikawa H (2013) Natural and induced T regulatory cells in cancer. Front Immunol 4: 190.
46. Walker MR, Kasprowicz DJ, Gersuk VH, Benard A, Van LM, et al. (2003) Induction of FoxP3 and acquisition of T regulatory activity by stimulated human CD4+. J Clin Invest 112: 1437-1443. (Pubitemid 38057697)
47. Allan SE, Crome SQ, Crellin NK, Passerini L, Steiner TS, et al. (2007) Activation-induced FOXP3 in human T effector cells does not suppress proliferation or cytokine production. Int Immunol 2007 19: 345-354. (Pubitemid 46523383)
48. Gavin MA, Torgerson TR, Houston E, DeRoos P, Ho WY, et al. (2006) Single-cell analysis of normal and FOXP3-mutant human T cells: FOXP3 expression without regulatory T cell development. Proc Natl Acad Sci U S A 103: 6659-6664.