A reduction of recipient regulatory T cells by cyclophosphamide contributes to an anti-tumor effect of nonmyeloablative allogeneic stem cell transplantation in mice

International Journal of Cancer

Volumn 130, Issue 2, 2012, Pages 365-376

  Takeuchi, Ario ^a,b   Eto, Masatoshi ^c   Yamada, Hisakata ^a   Tatsugami, Katsunori ^b   Naito, Seiji ^b   Yoshikai, Yasunobu ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b KYUSHU UNIVERSITY   (Japan)

^c KUMAMOTO UNIVERSITY   (Japan)

Author keywords

bladder cancer; cyclophosphamide; non myeloablative; regulatory T cell

Indexed keywords

CYCLOPHOSPHAMIDE; GAMMA INTERFERON; TRANSCRIPTION FACTOR FOXP3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BLADDER TUMOR; BONE MARROW CELL; CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL EXPANSION; CYTOKINE PRODUCTION; DONOR LYMPHOCYTE INFUSION; DRUG MEGADOSE; FEMALE; GRAFT RECIPIENT; LYMPHOCYTE COUNT; MOUSE; NONHUMAN; NONMYELOABLATIVE STEM CELL TRANSPLANTATION; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SPLEEN CELL; T CELL DEPLETION;

ANIMALS; CYCLOPHOSPHAMIDE; FEMALE; IMMUNOSUPPRESSIVE AGENTS; IMMUNOTHERAPY, ADOPTIVE; LYMPHOCYTES, TUMOR-INFILTRATING; MICE; MICE, INBRED AKR; MICE, INBRED C3H; MYELOABLATIVE AGONISTS; STEM CELL TRANSPLANTATION; T-LYMPHOCYTES, REGULATORY; URINARY BLADDER NEOPLASMS;

EID: 83655192112     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.26009     Document Type: Article

References (49)

1. Childs R, Chernoff A, Contentin N, Bahceci E, Schrump D, Leitman S, Read EJ, Tisdale J, Dunbar C, Linehan WM, Young NS, Barrett AJ,. Regression of metastatic renal-cell carcinoma after nonmyeloablative allogeneic peripheral-blood stem-cell transplantation. N Engl J Med 2000; 343: 750-8.
2. Hentschke P, Barkholt L, Uzunel M, Mattsson J, Wersall P, Pisa P, Martola J, Albiin N, Wernerson A, Soderberg M, Remberger M, Thorne A, Ringden O,. Low-intensity conditioning and hematopoietic stem cell transplantation in patients with renal and colon carcinoma. Bone Marrow Transplant 2003; 31: 253-61.
3. Bishop MR, Fowler DH, Marchigiani D, Castro K, Kasten-Sportes C, Steinberg SM, Gea-Banacloche JC, Dean R, Chow CK, Carter C, Read EJ, Leitman S, Gress R,. Allogeneic lymphocytes induce tumor regression of advanced metastatic breast cancer. J Clin Oncol 2004; 22: 3886-92.
4. Carella AM, Beltrami G, Corsetti MT, Nati S, Musto P, Scalzulli P, Gonella R, Ballestrero A, Patrone F,. Reduced intensity conditioning for allograft after cytoreductive autograft in metastatic breast cancer. Lancet 2005; 366: 318-20.
5. Bay JO, Fleury J, Choufi B, Tournilhac O, Vincent C, Bailly C, Dauplat J, Viens P, Faucher C, Blaise D,. Allogeneic hematopoietic stem cell transplantation in ovarian carcinoma: results of five patients. Bone Marrow Transplant 2002; 30: 95-102.
6. Ueno NT, Cheng YC, Rondon G, Tannir NM, Gajewski JL, Couriel DR, Hosing C, de Lima MJ, Anderlini P, Khouri IF, Booser DJ, Hortobagyi GN, Pagliaro LC, et al. Rapid induction of complete donor chimerism by the use of a reduced-intensity conditioning regimen composed of fludarabine and melphalan in allogeneic stem cell transplantation for metastatic solid tumors. Blood 2003; 102: 3829-36.
7. Childs R, Clave E, Contentin N, Jayasekera D, Hensel N, Leitman S, Read EJ, Carter C, Bahceci E, Young NS, Barrett AJ,. Engraftment kinetics after nonmyeloablative allogeneic peripheral blood stem cell transplantation: full donor T-cell chimerism precedes alloimmune responses. Blood 1999; 94: 3234-41.
8. Vourka-Karussis U, Karussis D, Ackerstein A, Slavin S,. Enhancement of GVL effect with rhIL-2 following BMT in a murine model for acute myeloid leukemia in SJL/J mice. Exp Hematol 1995; 23: 196-201.
9. Horowitz MM, Gale RP, Sondel PM, Goldman JM, Kersey J, Kolb HJ, Rimm AA, Ringden O, Rozman C, Speck B, et al. Graft-versus-leukemia reactions after bone marrow transplantation. Blood 1990; 75: 555-62.
10. Sakaguchi S,. Naturally arising Foxp3-expressing CD25+CD4+ regulatory T cells in immunological tolerance to self and non-self. Nat Immunol 2005; 6: 345-52.
11. Sakaguchi S, Sakaguchi N,. Regulatory T cells in immunologic self-tolerance and autoimmune disease. Int Rev Immunol 2005; 24: 211-26.
12. Waldmann H, Graca L, Cobbold S, Adams E, Tone M, Tone Y,. Regulatory T cells and organ transplantation. Semin Immunol 2004; 16: 119-26.
13. Cohen JL, Trenado A, Vasey D, Klatzmann D, Salomon BL,. CD4(+)CD25(+) immunoregulatory T cells: new therapeutics for graft-versus-host disease. J Exp Med 2002; 196: 401-6.
14. Hoffmann P, Ermann J, Edinger M, Fathman CG, Strober S,. Donor-type CD4(+)CD25(+) regulatory T cells suppress lethal acute graft-versus-host disease after allogeneic bone marrow transplantation. J Exp Med 2002; 196: 389-99.
15. Taylor PA, Lees CJ, Blazar BR,. The infusion of ex vivo activated and expanded CD4(+)CD25(+) immune regulatory cells inhibits graft-versus-host disease lethality. Blood 2002; 99: 3493-9.
16. Edinger M, Hoffmann P, Ermann J, Drago K, Fathman CG, Strober S, Negrin RS,. CD4+CD25+ regulatory T cells preserve graft-versus-tumor activity while inhibiting graft-versus-host disease after bone marrow transplantation. Nat Med 2003; 9: 1144-50.
17. Anderson BE, McNiff JM, Matte C, Athanasiadis I, Shlomchik WD, Shlomchik MJ,. Recipient CD4+ T cells that survive irradiation regulate chronic graft-versus-host disease. Blood 2004; 104: 1565-73.
18. Trenado A, Charlotte F, Fisson S, Yagello M, Klatzmann D, Salomon BL, Cohen JL,. Recipient-type specific CD4+CD25+ regulatory T cells favor immune reconstitution and control graft-versus-host disease while maintaining graft-versus-leukemia. J Clin Invest 2003; 112: 1688-96.
19. Joffre O, Santolaria T, Calise D, Al Saati T, Hudrisier D, Romagnoli P, van Meerwijk JP,. Prevention of acute and chronic allograft rejection with CD4+CD25+Foxp3+ regulatory T lymphocytes. Nat Med 2008; 14: 88-92.
20. Lutsiak ME, Semnani RT, De Pascalis R, Kashmiri SV, Schlom J, Sabzevari H,. Inhibition of CD4(+)25+ T regulatory cell function implicated in enhanced immune response by low-dose cyclophosphamide. Blood 2005; 105: 2862-8.
21. Eto M, Mayumi H, Tomita Y, Yoshikai Y, Nomoto K,. Intrathymic clonal deletion of V beta 6+ T cells in cyclophosphamide-induced tolerance to H-2-compatible, Mls-disparate antigens. J Exp Med 1990; 171: 97-113.
22. Eto M, Mayumi H, Tomita Y, Yoshikai Y, Nishimura Y, Maeda T, Ando T, Nomoto K,. Specific destruction of host-reactive mature T cells of donor origin prevents graft-versus-host disease in cyclophosphamide-induced tolerant mice. J Immunol 1991; 146: 1402-9.
23. Harano M, Eto M, Iwai T, Tatsugami K, Kiyoshima K, Kamiryo Y, Tsuneyoshi M, Yoshikai Y, Naito S,. Renal cancer treatment with low levels of mixed chimerism induced by nonmyeloablative regimen using cyclophosphamide in mice. Cancer Res 2005; 65: 10032-40.
24. Kamiryo Y, Eto M, Yamada H, Yajima T, Harano M, Takeuchi A, Tatsugami K, Hamaguchi M, Naito S, Yoshikai Y,. Donor CD4 T cells are critical in allogeneic stem cell transplantation against murine solid tumor. Cancer Res 2009; 69: 5151-8.
25. Rini BI, Zimmerman T, Stadler WM, Gajewski TF, Vogelzang NJ,. Allogeneic stem-cell transplantation of renal cell cancer after nonmyeloablative chemotherapy: feasibility, engraftment, and clinical results. J Clin Oncol 2002; 20: 2017-24.
26. Bethge WA, Hegenbart U, Stuart MJ, Storer BE, Maris MB, Flowers ME, Maloney DG, Chauncey T, Bruno B., Agura E, Forman SJ, Blume KG, et al. Adoptive immunotherapy with donor lymphocyte infusions after allogeneic hematopoietic cell transplantation following nonmyeloablative conditioning. Blood 2004; 103: 790-5.
27. Tykodi SS, Warren EH, Thompson JA, Riddell SR, Childs RW, Otterud BE, Leppert MF, Storb R, and, Sandmaier BM,. Allogeneic hematopoietic cell transplantation for metastatic renal cell carcinoma after nonmyeloablative conditioning: toxicity, clinical response, and immunological response to minor histocompatibility antigens. Clin Cancer Res 2004; 10: 7799-811.
28. Zhou L, Chong MM, Littman DR,. Plasticity of CD4+ T cell lineage differentiation. Immunity 2009; 30: 646-55.
29. Mucida, D., Kutchukhidze N, Erazo A, Russo M, Lafaille JJ, Curotto de Lafaille MA,. Oral tolerance in the absence of naturally occurring Tregs. J Clin Invest 2005; 115: 1923-33.
30. Sun JB, Raghavan S, Sjoling A, Lundin S, Holmgren J,. Oral tolerance induction with antigen conjugated to cholera toxin B subunit generates both Foxp3+CD25+ and Foxp3-CD25- CD4+ regulatory T cells. J Immunol 2006; 177: 7634-44.
31. Chen W, Jin W, Hardegen N, Lei KJ, Li L, Marinos N, McGrady G, Wahl SM,. Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med 2003; 198: 1875-86.
32. Setoguchi R, Hori S, Takahashi T, Sakaguchi S,. Homeostatic maintenance of natural Foxp3(+) CD25(+) CD4(+) regulatory T cells by interleukin (IL)-2 and induction of autoimmune disease by IL-2 neutralization. J Exp Med 2005; 201: 723-35.
33. Awwad MR, North J,. Cyclophosphamide-induced immunologically mediated regression of a cyclophosphamide-resistant murine tumor: a consequence of eliminating precursor L3T4+ suppressor T-cells. Cancer Res 1989; 49: 1649-54.
34. Ghiringhelli F, Larmonier N, Schmitt E, Parcellier A, Cathelin D, Garrido C, Chauffert B, Solary E, Bonnotte B, Martin F,. CD4+CD25+ regulatory T cells suppress tumor immunity but are sensitive to cyclophosphamide which allows immunotherapy of established tumors to be curative. Eur J Immunol 2004; 34: 336-44.
35. Yip WK, Abdullah MA, Yusoff SM, Seow HF,. Increase in tumour-infiltrating lymphocytes with regulatory T cell immunophenotypes and reduced zeta-chain expression in nasopharyngeal carcinoma patients. Clin Exp Immunol 2009; 155: 412-22.
36. Shen LS, Wang J, Shen DF, Yuan XL, Dong P, Li MX, Xue J, Zhang FM, Ge HL, Xu D,. CD4(+)CD25(+)CD127(low/-) regulatory T cells express Foxp3 and suppress effector T cell proliferation and contribute to gastric cancers progression. Clin Immunol 2009; 131: 109-18.
37. Sakaguchi S,. Regulatory T cells: key controllers of immunologic self-tolerance. Cell 2000; 101: 455-8.
38. Somasundaram R, Jacob L, Swoboda R, Caputo L, Song H, Basak S, Monos D, Peritt D, Marincola F, Cai D, Birebent B, Bloome E,. et al. Inhibition of cytolytic T lymphocyte proliferation by autologous CD4+/CD25+ regulatory T cells in a colorectal carcinoma patient is mediated by transforming growth factor-beta. Cancer Res 2002; 62: 5267-72.
39. Liyanage UK, Moore TT, Joo HG, Tanaka Y, Herrmann V, Doherty G, Drebin JA, Strasberg SM, Eberlein TJ, Goedegebuure PS, Linehan DC,. Prevalence of regulatory T cells is increased in peripheral blood and tumor microenvironment of patients with pancreas or breast adenocarcinoma. J Immunol 2002; 169: 2756-61.
40. Curotto de Lafaille MA, Lafaille JJ,. CD4(+) regulatory T cells in autoimmunity and allergy. Curr Opin Immunol 2002; 14: 771.
41. von Boehmer H,. Mechanisms of suppression by suppressor T cells. Nat Immunol 2005; 6: 338-44.
42. Leach DR, Krummel MF, Allison JP,. Enhancement of antitumor immunity by CTLA-4 blockade. Science 1996; 271: 1734-6.
43. Hurwitz AA, Yu TF, Leach DR, Allison JP,. CTLA-4 blockade synergizes with tumor-derived granulocyte-macrophage colony-stimulating factor for treatment of an experimental mammary carcinoma. Proc Natl Acad Sci USA 1998; 95: 10067-71.
44. Onizuka S, Tawara I, Shimizu J, Sakaguchi S, Fujita T, Nakayama E,. Tumor rejection by in vivo administration of anti-CD25 (interleukin-2 receptor alpha) monoclonal antibody. Cancer Res 1999; 59: 3128-33.
45. Shimizu J, Yamazaki S, Sakaguchi S,. Induction of tumor immunity by removing CD25+CD4+ T cells: a common basis between tumor immunity and autoimmunity. J Immunol 1999; 163: 5211-8.
46. Sutmuller RP, van Duivenvoorde LM, van Elsas A, Schumacher TN, Wildenberg ME, Allison JP, Toes RE, Offringa R, Melief CJ,. Synergism of cytotoxic T lymphocyte-associated antigen 4 blockade and depletion of CD25(+) regulatory T cells in antitumor therapy reveals alternative pathways for suppression of autoreactive cytotoxic T lymphocyte responses. J Exp Med 2001; 194: 823-32.
47. Rubio MT, Kim YM, Sachs T, Mapara M, Zhao G, Sykes M,. Antitumor effect of donor marrow graft rejection induced by recipient leukocyte infusions in mixed chimeras prepared with nonmyeloablative conditioning: critical role for recipient-derived IFN-gamma. Blood 2003; 102: 2300-7.
48. Rubio MT, Saito TI, Kattleman K, Zhao G, Buchli J, Sykes M,. Mechanisms of the antitumor responses and host-versus-graft reactions induced by recipient leukocyte infusions in mixed chimeras prepared with nonmyeloablative conditioning: a critical role for recipient CD4+ T cells and recipient leukocyte infusion-derived IFN-gamma-producing CD8+ T cells. J Immunol 2005; 175: 665-76.
49. Nikolova M, Lelievre JD, Carriere M, Bensussan A, Levy Y,. Regulatory T cells modulate differentially the maturation and apoptosis of human CD8-T cell subsets. Blood 2009; 113: 4556-65.