Nonmyeloablative stem cell transplantation: reduced-intensity conditioning for cancer immunotherapy—from bench to patient bedside

Sinkovics, 1965, Prolongation and prevention of Rauscher virus mouse leukemia by spleen cells of naturally resistant or actively immunized mice, Clin Res, 13, 36 Boranic, 1971, Time pattern of the antileukemia effect of graft-versus-host reaction in mice, I. Cellular events, Cancer Res, 31, 1140 Weiden, 1981, Antileukemic effect of chronic graft-versus-host disease, N Engl J Med, 304, 1529, 10.1056/NEJM198106183042507 Weiden, 1981, Antileukemic effect of graft-versus-host disease contributes to improved survival after allogeneic marrow transplantation, Transplantation, 13, 248 Bortin, 1979, Graft-versus-leukaemia reactivity induced by alloimmunization without augmentation of graft-versus-host reactivity, Nature, 281, 490, 10.1038/281490a0 Slavin, 1981, Eradication of murine leukemia with histoincompatible marrow grafts in mice conditioned with total lymphoid irradiation (TLI), Cancer Immunol Immunother, 11, 155, 10.1007/BF00199267 Truitt, 1983, Characterization of alloimmunization-induced T lymphocytes reactivated against AKR leukemia in vitro and correlation with graft-vs-leukemia activity in vivo, J Immunol, 131, 2050, 10.4049/jimmunol.131.4.2050 Meredith, 1983, Possibility of graft-vs-leukemia determinants independent of the major histocompatibility complex in allogeneic marrow transplantation, Transplantation, 35, 378, 10.1097/00007890-198304000-00023 Moscovitch, 1984, Anti-tumor effects of allogeneic bone marrow transplantation in (NZB x NZW)F1 hybrids with spontaneous lymphosarcoma, J Immunol, 132, 997, 10.4049/jimmunol.132.2.997 Slavin, 1978, Spontaneous murine B-cell leukemia, Nature, 272, 624, 10.1038/272624a0 Slavin, 1981, Ultrastructural, cell membrane and cytogenetic characteristics of B-cell leukemia (BCL1), a murine model of chronic lymphocytic leukemia, Cancer Res, 41, 4162 Vourka-Karussis, 1995, Enhancement of graft versus leukemia effect (GVL) with recombinant human interleukin 2 (rIL-2) following bone marrow transplantation in a murine model for acute myeloid leukemia in SJL/J mice, Exp Hematol, 23, 196 Moscovitch, 1984, Anti-tumor effects of allogeneic bone marrow transplantation in (NZB x NZW)F1 hybrids with spontaneous lymphosarcoma, J Immunol, 132, 997, 10.4049/jimmunol.132.2.997 Morecki, 1997, Induction of graft vs tumor effect in a murine model of mammary adenocarcinoma, Int J Cancer, 71, 59, 10.1002/(SICI)1097-0215(19970328)71:1<59::AID-IJC11>3.0.CO;2-4 Morecki, 1998, Allogeneic cell therapy for a murine mammary carcinoma, Cancer Res, 58, 3891 Morecki, 2001, Cell therapy with pre-immunized effector cells mismatched for minor histocompatible antigens, in the treatment of a murine mammary carcinoma, J Immunother, 24, 114, 10.1097/00002371-200103000-00005 Prigozhina, 2002, Non-myeloablative allogeneic bone marrow transplantation as immunotherapy for hematologic malignancies and metastatic solid tumors in pre-clinical models, Exp Hematol, 30, 89, 10.1016/S0301-472X(01)00759-7 Slavin, 1981, Eradication of murine leukemia with histoincompatible marrow grafts in mice conditioned with total lymphoid irradiation (TLI), Cancer Immunol Immunother, 11, 155, 10.1007/BF00199267 Slavin, 1978, Transplantation of allogeneic bone marrow without graft vs host disease using total lymphoid irradiation, J Exp Med, 147, 963, 10.1084/jem.147.4.963 Weiss, 1992, Use of recombinant human interleukin-2 in conjunction with bone marrow transplantation as a model for control of minimal residual disease in malignant hematological disorders. I. Treatment of murine leukemia in conjunction with allogeneic bone marrow transplantation and IL2-activated cell-mediated immunotherapy, Cancer Invest, 10, 19, 10.3109/07357909209032785 Weiss, 1990, Effect of cyclosporine A and methylprednisolone on the GVL effect across major histocompatibility barriers in mice following allogeneic bone marrow transplantation, Bone Marrow Transplant, 6, 229 Weiss, 1995, The role of antibodies to IL-2 receptor and anti-Asialo GMI antibodies on GVL effects induced by BMT in murine B cell leukemia, Bone Marrow Transplant, 16, 457 Weiss, 1999, Alloimmune-mediated GVL effects induced by unmodified and in vitro r-IL2 activated bone marrow and lymphocytes from different lymphoid compartments, Cytokines Cell Mol Ther, 5, 145 Slavin, 1991, Induction of cell-mediated IL2-activated antitumor responses in conjunction with autologous and allogeneic bone marrow transplantation, Transplant Proc, 23, 802 Ji, 2003, Allogeneic cell-mediated immunotherapy of leukemia with immune donor lymphocytes to up-regulate anti-tumor effects and down-regulate anti-host responses, Bone Marrow Transplant, 32, 495, 10.1038/sj.bmt.1704150 Morecki, 2001, Cell therapy with pre-immunized effector cells mismatched for minor histocompatible antigens, in the treatment of a murine mammary carcinoma, J Immunother, 24, 114, 10.1097/00002371-200103000-00005 Slavin, 1988, Adoptive immunotherapy in conjunction with bone marrow transplantation—Amplification of natural host defence mechanisms against cancer by recombinant IL2, Nat Immun Cell Growth Regul, 7, 180 Morecki, 1996, Tumor dormancy induced by immune effector mechanisms in a murine model of B cell leukemia/lymphoma (BCL1), 137 Sullivan, 1989, Influence of acute and chronic graft-versus-host disease on relapse and survival after bone marrow transplantation from HLA-identical siblings as treatment of acute and chronic leukemia, Blood, 73, 1720, 10.1182/blood.V73.6.1720.1720 Ringden, 1989, Graft-vs-leukemia reactions in humans, Transplant Proc, 21, 2989 Horowitz, 1990, Graft-versus-leukemia reactions after bone marrow transplantation, Blood, 75, 555, 10.1182/blood.V75.3.555.555 Eibl, 1996, Evidence for a graft-versus-tumor effect in a patient treated with marrow ablative chemotherapy and allogeneic bone marrow transplantation for breast cancer, Blood, 88, 1501, 10.1182/blood.V88.4.1501.bloodjournal8841501 Ben-Yosef, 1996, Graft vs tumor and graft vs leukemia in patient with concurrent breast cancer and acute myelocytic leukemia, Lancet, 348, 1242, 10.1016/S0140-6736(05)65517-1 Ueno, 1998, Allogeneic peripheral-blood progenitor-cell transplantation for poor-risk patients with metastatic breast cancer, J Clin Oncol, 16, 986, 10.1200/JCO.1998.16.3.986 Or, 1998, Allogeneic cell mediated immunotherapy for breast cancer after autologous stem cell transplantation, Cytokines Cell Mol Ther, 4, 1 Childs, 1999, Successful treatment of metastatic renal cell carcinoma with a non-myeloablative allogeneic peripheral-blood progenitor-cell transplant, J Clin Oncol, 17, 2044, 10.1200/JCO.1999.17.7.2044 Childs, 2000, Regression of metastatic renal-cell carcinoma after nonmyeloablative allogeneic peripheral-blood stem-cell transplantation, N Engl J Med, 11, 750, 10.1056/NEJM200009143431101 Kapelushnik, 1996, Allogeneic cell therapy of severe beta thalassemia major by displacement of host stem cells in mixed chimera by donor blood lymphocytes, Bone Marrow Transplant, 19, 96 Aker, 1998, Donor lymphocyte infusions to displace residual host hematopoietic cells after allogeneic BMT for beta thalassemia major, J Pediatr Hematol Oncol, 20, 145, 10.1097/00043426-199803000-00011 Slavin, 1999, Minitransplants and cell-based therapies for malignant and non-malignant disorders, Curr Opin Organ Transplant, 4, 184, 10.1097/00075200-199909000-00002 Kolb, 1995, Graft-versus-leukemia effect of donor lymphocyte transfusions in marrow grafted patients, Blood, 86, 2041, 10.1182/blood.V86.5.2041.bloodjournal8652041 Slavin, 2000, Graft vs autoimmune lymphocytes (GVA) following allogeneic bone marrow transplantation in a patient with chronic myelogenous leukemia and severe systemic psoriasis and psoriatic polyarthritis, Exp Hematol, 28, 853, 10.1016/S0301-472X(00)00172-7 Slavin, 2000, Graft vs autoimmune lymphocytes (GVA) following allogeneic bone marrow transplantation in a patient with chronic myelogenous leukemia and severe systemic psoriasis and psoriatic polyarthritis, Exp Hematol, 28, 853, 10.1016/S0301-472X(00)00172-7 Slavin, 1988, Cellular-mediated immunotherapy of leukemia in conjunction with autologous and allogeneic bone marrow transplantation in experimental animals and man, Blood, 72, 407a Slavin, 1998, Prevention of GVHD and induction of graft vs leukemia (GVL) effects, Bone Marrow Transplant, 3, 208 Slavin, 1990, Cell-mediated cytokine-activated immunotherapy (CCI) of malignant hematological disorders for eradication of minimal residual disease (MRD) in conjunction with conventional chemotherapy or bone marrow transplantation (BMT), Blood, 76, 566a Slavin, 1995, Allogeneic cell therapy for relapsed leukemia following bone marrow transplantation with donor peripheral blood lymphocytes, Exp Hematol, 23, 1553 Slavin, 1996, Allogeneic cell therapy with donor peripheral blood cells and recombinant human interleukin-2 to treat leukemia relapse post allogeneic bone marrow transplantation, Blood, 87, 2195, 10.1182/blood.V87.6.2195.bloodjournal8762195 Naparstek, 1995, T-cell-depleted allogeneic bone marrow transplantation for acute leukaemia using Campath-1 antibodies and post-transplant administration of donor’s peripheral blood lymphocytes for prevention of relapse, Br J Haematol, 89, 506, 10.1111/j.1365-2141.1995.tb08356.x Naparstek, 1996, Allogeneic cell mediated immunotherapy using donor lymphocytes for prevention of relapse in patients treated with allogeneic BMT for hematological malignancies, 281 Bacigalupo, 1991, Increased risk of leukemia relapse with high dose cyclosporine A after allogeneic marrow transplantation for acute leukemia, Blood, 77, 1423, 10.1182/blood.V77.7.1423.1423 Slavin, 1992, Immunotherapy of minimal residual disease in conjunction with autologous and allogeneic bone marrow transplantation (BMT), Leukemia, 6, 164 Kolb, 1990, Donor leukocyte transfusion for treatment of recurrent chronic myelogenous leukemia in marrow transplant patients, Blood, 76, 2462, 10.1182/blood.V76.12.2462.2462 Goldman, 1988, Bone marrow transplantation for chronic myelogenous leukemia in chronic phase, Ann Intern Med, 108, 806, 10.7326/0003-4819-108-6-806 Bar, 1993, Donor leukocyte infusions for chronic myeloid leukemia relapsed after allogeneic bone marrow transplantation, J Clin Oncol, 11, 513, 10.1200/JCO.1993.11.3.513 Leber, 1993, Reinduction of remission of chronic myeloid leukemia by donor leukocyte transfusion following relapse after bone marrow transplantation, Bone Marrow Transplant, 12, 405 Drobyski, 1993, Salvage immunotherapy using donor leukocyte infusions as treatment for relapsed chronic myelogenous leukemia after allogeneic bone marrow transplantation, Blood, 82, 2310, 10.1182/blood.V82.8.2310.2310 Porter, 1994, Induction of graft versus host disease for relapsed chronic myeloid leukemia, N Eng J Med, 330, 100, 10.1056/NEJM199401133300204 Mackinnon, 1995, Adoptive immunotherapy evaluating escalating doses of donor leukocytes for relapse of chronic myeloid leukemia after bone marrow transplantation, Blood, 86, 1261, 10.1182/blood.V86.4.1261.bloodjournal8641261 Papadopoulos, 1994, Infusions of donor leukocytes to treat Epstein-Barr virus-associated lympho-proliferative disorders after allogeneic bone marrow transplantation, N Engl J Med, 330, 1185, 10.1056/NEJM199404283301703 Kolb, 1995, Graft-versus-leukemia effect of donor lymphocyte transfusions in marrow grafted patients, Blood, 86, 2041, 10.1182/blood.V86.5.2041.bloodjournal8652041 Collins, 1997, Donor leukocyte infusions in 140 patients with relapsed malignancy after allogeneic bone marrow transplantation, J Clin Oncol, 15, 433, 10.1200/JCO.1997.15.2.433 Kuzushima, 1996, Establishment of anti-Epstein-Barr virus (EBV) cellular immunity by adoptive transfer of virus specific cytotoxic T lymphocytes from an HLA matched sibling to a patient with severe chronic active EBV infection, Clin Exp Immunol, 103, 192, 10.1046/j.1365-2249.1996.d01-619.x Gubbay, 1990, A gene mapping to the sex-determining region of the mouse y chromosome is a member of a novel family of embryologically expressed genes, Nature, 346, 245, 10.1038/346245a0 Pugatsch, 1996, Improved single-step PCR assay for sex identification post-allogeneic sex-mismatched BMT, Bone Marrow Transplant, 17, 273 Raanani, 1997, The rate and kinetics of molecular response to donor leucocyte transfusions in chronic myeloid leukaemia patients treated for relapse after allogeneic bone marrow transplantation, Br J Haematol, 99, 945, 10.1046/j.1365-2141.1997.4683272.x Johnson, 1993, Delayed infusion of normal donor cells after MHC-matched bone marrow transplantation provides an antileukemia reaction without graft-versus-host disease, Bone Marrow Transplant, 11, 329 Kolb, 1993, Adoptive immunotherapy in human and canine chimeras, Bone Marrow Transplant, 12, 561 Keating, 1996, Clinical experience with fludarabine in hemato-oncology, Hematol Cell Ther, 38, S83 Keating, 1998, Long-term follow-up of patients with chronic lymphocytic leukemia (CLL) receiving fludarabine regimens as initial therapy, Blood, 92, 1165, 10.1182/blood.V92.4.1165 Slavin, 1998, Non-myeloablative stem cell transplantation and cell therapy as an alternative to conventional bone marrow transplantation with lethal cytoreduction for the treatment of malignant and non malignant hematologic diseases, Blood, 91, 756, 10.1182/blood.V91.3.756 Khouri, 1998, Transplant-lite, J Clin Oncol, 16, 2817, 10.1200/JCO.1998.16.8.2817 Giralt, 1997, Preliminary results of fludarabine/melphalan or 2CDA/melphalan as preparative regimens for allogeneic progenitor cell transplantation in poor candidates for conventional myeloablative conditioning, Blood, 90, 1853a McSweeney, 1998, Outpatient PBSC allografts using immunosuppression with low-dose TBI before, and cyclosporine (CSP) and mycophenolate mofetil (MMF) after transplant, Blood, 92, 519a Carella, 2000, Low intensity regimens with allogeneic hematopoietic stem cell transplantation as treatment of hematologic neoplasia, Haematologica, 85, 304 Carella, 2000, “Mini-allografts”, Bone Marrow Transplant, 25, 345, 10.1038/sj.bmt.1702204 Kapelushnik, 1998, Bone marrow transplatation from a cadaveric donor, Bone Marrow Transplant, 21, 857, 10.1038/sj.bmt.1701165 Nagler, 1999, Donor lymphocyte infusion post non-myeloablative allogeneic peripheral blood stem cell transplantation for chronic granulomatous disease, Bone Marrow Transplant, 24, 339, 10.1038/sj.bmt.1701903 Kapelushnik, 1997, Fludarabine based protocol for BMT in Fanconi anemia, Bone Marrow Transplant, 29, 1109, 10.1038/sj.bmt.1701016 Aker, 1999, Fludarabine-based protocol for human umbilical cord blood transplantation in children with Fanconi’s anemia, J Pediatr Hematol Oncol, 21, 237, 10.1097/00043426-199905000-00013 Nagler, 2000, Allogeneic peripheral blood stem cell transplantation using a fludarabine-based low intensity conditioning regimen for a malignant lymphoma, Bone Marrow Transplant, 25, 1021, 10.1038/sj.bmt.1702392 Slavin, 2000, Graft vs autoimmunity following allogeneic non-myeloablative blood stem cell transplantation in a patient with chronic myelogenous leukemia and severe systemic psoriasis and psoriatic polyarthritis, Exp Hematol, 28, 853, 10.1016/S0301-472X(00)00172-7 Slavin, 2000, Treatment of myeloid leukemias with non-myeloablative stem cell transplantation: Accomplishments and future goals. Educational Symposium, ASH, December 2000, Hematology, 1, 81 Nagler, 2001, Low-intensity conditioning is sufficient to ensure engraftment in matched unrelated bone marrow transplantation, Exp Hematol, 29, 362, 10.1016/S0301-472X(00)00655-X Giralt, 1997, Induction of graft-versus-leukemia as primary treatment of chronic myelogenous leukemia, Blood, 90, 1857a Giralt, 1995, CD8-depleted donor lymphocyte infusions as treatment for relapsed chronic myelogenous leukemia after allogeneic bone marrow transplantation, Blood, 86, 4337, 10.1182/blood.V86.11.4337.bloodjournal86114337 Giralt, 1997, Preliminary results of fludarabine/melphalan or 2CDA/melphalan as preparative regimens for allogeneic progenito cell transplantation in poor candidates for conventional myeloablative conditioning, Blood, 90, 1853a Carella, 1998, Engraftment of HLA-matched sibling hematopoietic stem cells after immunosuppressive conditioning regimen in patients with hematologic neoplasias, Haematologica, 83, 904 Carella, 1998, Evidence of cytogenetic and molecular remission by allogeneic cells after immunosuppressive therapy alone, Br J Haematol, 103, 565, 10.1046/j.1365-2141.1998.01057.x Yu, 1995, DLA-identical bone marrow grafts after low-dose total body irradiation, Blood, 86, 4376, 10.1182/blood.V86.11.4376.bloodjournal86114376 Storb, 1997, Stable mixed hematopoietic chimerism in DLA-identical littermate dogs given sublethal total body irradiation before and pharmacological immunosuppression after marrow transplantation, Blood, 89, 3048, 10.1182/blood.V89.8.3048 Storb, 1999, Stable mixed hematopoietic chimerism in DLA-identical littermate dogs given lymph node irradiation before and pharmacological immunosuppression after marrow transplantation, Blood, 90, 1131, 10.1182/blood.V94.3.1131.415k21_1131_1136 Pelot, 1999, Lymphohematopoietic graft-vs-host reactions can be induced without graft-vs-host disease in murine mixed chimeras established with a cyclophosphamide-based non-myeloablative conditioning regimen, Biol Blood Marrow Transplant, 5, 133, 10.1053/bbmt.1999.v5.pm10392959 Sykes, 1999, Mixed lymphohematopoietic chimerism and graft-vs-lymphoma effects are achievable in adult recipients following non-myeloablative therapy and HLA-mismatched donor bone marrow transplantation, Lancet, 353, 1755, 10.1016/S0140-6736(98)11135-2 Morecki, 2001, Cell therapy with pre-immunized effector cells mismatched for minor histocompatible antigens, in the treatment of a murine mammary carcinoma, J Immunother, 24, 114, 10.1097/00002371-200103000-00005