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Blood, Vol. 92 No. 5 (September 1), 1998:
pp. 1471-1490
REVIEW ARTICLE
By
From the Laboratory of Experimental Oncology and Hematology,
University of Louvain, Brussels, Belgium; and the Section of
Hematology/Oncology, Boston University School of Medicine, Boston, MA.
APPROXIMATELY 10,000 autologous
hematopoietic stem cell (HSC) transplants are performed
worldwide each year for malignant diseases.1 Results of
randomized trials in recent years suggest that high-dose chemotherapy
followed by infusion of autologous HSCs can offer prolonged
disease-free survival in hematologic malignancies including
non-Hodgkin's lymphoma in relapse,2 acute myelogenous
leukemia,3 and multiple myeloma.4
Similarly encouraging results have been seen in the
treatment of solid tumors.5,6
After transplantation, reconstitution of bone marrow (BM) consists of
two distinct phenomena, numerical recovery of BM cellular elements on
the one hand and functional recovery of cellular interactions on the
other.
Although reappearance of neutrophils and platelets is often considered
the endpoint of hematologic recovery after intensive chemotherapy and
stem cell transplantation, this ignores the second arm of BM recovery,
that of immunological reconstitution. In fact, functional recovery of
lymphoid and immune effector cells occurs very gradually, and
reconstitution of normal humoral and cellular immunity may take a year
or more.
Immune reconstitution involves several components of the immune
response. These include (1) reappearance of functional B cells, (2)
thymic and extra-thymic T-cell development, (3) reconstitution of
effector cells including cytotoxic T cells and natural killer (NK)
cells, and (4) efficient antigen presentation to reconstitute the
pretransplantation immune repertoire. This restoration of immune
function is not merely experimental. It may have direct clinical
implications: Immediately after the administration of intensive
cytotoxic drugs, minimal tumor burden is presumed to be present,
providing potentially ideal circumstances to eliminate residual disease
altogether by immunotherapeutic means. In this review, several
strategies that could lead to enhancement of cellular immune function
to take particular advantage of posttransplantation minimal residual
disease will be discussed. In addition, the potential to accelerate
immune reconstitution and the effect that might have in the therapy of
malignant disease will be considered.
Although there are similarities in immune reconstitution after allo-BM
transplantation (BMT)7,8 and autologous HSCs, allo-BMT
involves graft-versus-host disease (GVHD) and the use of
immunosuppressive therapy to control it, both of which interfere in the
early developmental stages of immune reconstitution. Autologous HSC
transplantation that entails neither GVHD nor immunosuppressive drugs
presents more direct insight into the factors involved in immune
reconstitution after grafting.
B-Cell Regeneration and Ig VH Gene Expression
Origin of Posttransplant B Cells
B-Cell Function Deficiencies in humoral responsiveness in HSC recipients is attributed to both decreased T-cell help and to intrinsic B-cell defects.25-27 Serum Ig levels remain low during the first 3 months after ABMT during the same period in which the numbers of circulating B cells is reduced11,28 and B-cell proliferative response to the T-cell-independent antigen Staphylococcus aureus Cowan strain I (SAC) blunted.12 While IgM production in response to pokeweed mitogen and SAC normalize at 3 months, IgG production is suppressed for 12 to 24 months in most patients.12 This delay in Ig production parallels the pattern seen in B-cell ontogeny, and may reflect the failure of posttransplant B cells to receive or respond to T-cell factors involved in isotype switching.
BM-derived hematopoietic stem cells in the normal process of differentiation home to the thymus, the major site of T-cell differentiation. However, the thymus is not the only site of T-cell development. T-cell differentiation also occurs through extrathymic pathways in the gut mucosa, in the liver,29 and, at least in the case of murine T-cell development, in the BM as well.30 The contribution of these extrathymic sites may play a role in posttransplant immune reconstitution. Reconstitution of T-Cell Subsets Surface markers have proven to be critically useful in characterizing T lymphocytes and their functional subsets. Nevertheless, however useful in our understanding of lymphoid ontogeny, phenotypic subtyping identified to date doubtlessly represents only a part of the overall T-cell functional repertoire. Evidence for the as-yet limited nature of our T-cell characterization is the fact that phenotypic shifts in posttransplantation T cells do not necessary result in immune dysfunction. This must be borne in mind when discussing T-cell phenotypes and their correlation to immune reconstitution after stem cell transplantation.T-Cell Subsets After ABMT After ABMT, the relative number of CD3+ cells is significantly decreased compared with those of normal controls during the first month postgrafting, returning to normal levels within 3 months.31 In addition, a decrease in the relative and absolute numbers of CD4+ cells in the peripheral blood is commonly seen and can persist for a year or more.31-33 In contrast, the relative and absolute number of CD8+ cells reconstitutes fairly rapidly resulting in an inverted CD4/CD8 ratio in the months following autologous transplantation.31-33
T-Cell Subsets After ABSCT Because peripheral blood stem cells (PBSC) contain a larger proportion of more differentiated progenitor cells as well as terminally differentiated effector cells than BM, one might suppose that the kinetics of T-cell recovery may be accelerated following ABSCT as compared with ABMT. The fraction of cells designated PBSC in fact does contain large numbers of T cells. CD3+ cells may represent more than 20% of peripheral cells collected after granulocyte colony-stimulating factor (G-CSF) mobilization yielding substantially more T cells (up to 1 log greater) than found in BM.40,41T-Cell Repertoire (TCR) Shifts in T-cell subsets as defined by TCR V gene expression have been described early after both allo-BMT and ABMT.49-53 It is not clear whether particular T-cell subsets as defined by V gene usage are derived from T-cell precursors (either donor or recipient) or from expansion of donor-derived mature T cells. A significant proportion of patients shows increased usage of TCR / during the early period
post-BMT. Within the TCR / subpopulation, there is a preferential
expression of the V9 and V2 genes as is seen during early fetal
life.54 This suggests that recapitulation of T-cell
ontogeny may occur early following BMT, analogous to that described for
B-cell regeneration.50,51 This early postengraftment predominance of V9+V2+ cells in the
periphery may subsequently be further increased by antigen-driven
expansion of the newly generated cells. An alternative
possibility exists that mature T cells are already present in
the BM graft, are expanded after contact with antigen, and do not
represent an ontologic recapitulation.
Origin of Posttransplant T Cells and the Role of Thymic and Extrathymic Pathways Examination of TCR leads to the question of T-cell origin. After ABMT or ABSCT, T cells may reconstitute from at least four different sources: (1) rare recipient T cells that survived the conditioning regimen; these cells might be seeded in the BM, lymph nodes, or spleen; (2) T cells present in the graft; (3) hematopoietic stem cell progenitors of the graft that differentiate in the recipient; and (4) residual recipient stem cells (Fig 1). Studies of TCR alluded to in the preceding section suggest that the quantity of T cells present in the graft might influence the rapidity and the quality of T-cell recovery. However, it remains unclear how much passively transferred T lymphocytes will contribute to sustained cellular immunity.
T-Cell Function T-cell competence after stem cell transplantation can be gauged at three distinct functional levels: cell proliferation, cytokine production, and lytic capacity.T-Cell Proliferation Using limiting dilution analysis, the frequency of mitogen-responsive T cells in peripheral blood, including the frequency of cytokine-secreting helper T cells, interleukin-2 (IL-2) responding T cells, and cytotoxic T cells, was found to be low after ABMT.63Cytolytic Function Cytomegalovirus (CMV)-specific HLA-restricted CD8+ cytotoxic T cells (CTL) have been shown in the majority of patients within the first 3 months after ABMT or APBSCT and are associated with protection from CMV infection.72 In contrast, specific CTL response against Epstein-Barr virus (EBV) are impaired during the first 2 months after autologous stem cell transplantation.73 Further investigation of specific CTL activity are required in developing of adjuvant vaccines in patients undergoing transplantation.
Cytokine Production and T-Cell Responsiveness to Cytokines In vitro-stimulated PBMC from recipients of ABMT have significant defects in the production of a number of T-cell-derived cytokines important in immune homeostasis, particularly IL-2, in the early posttransplant period.64,79
NK cells are defined as large granular lymphocytes capable of mediating
major histocompatability complex (MHC)-unrestricted cytolytic reactions
against tumor or virally infected cells and not expressing receptors
for antigen (ie, neither surface Ig or TCR). In addition, NK cells
characteristically have a
CD3
The degree of T-cell incompetence after autologous transplantation is difficult to gauge exactly in vitro. The capacity to mount an effective immune response against foreign antigen better reflects the immune status of transplant recipients than do in vitro tests. Information garnered from allogeneic transplantation indicates that with the passive transfer of allogeneic lymphocytes, transplantation recipients show short-term production of antibodies against viral pathogens.20,94 However, vaccination in the months after transplantation does not always result in sustained protection. This pattern of temporarily effective but nonsustainable protection suggests that B lymphocytes derived from the donor, which generate specific antibody in the short term, are transferred together with the transplant, but that antigen-specific T cells necessary for ongoing sustained protection must be regenerated anew since the transfer of T cells functional against specific infections appears less efficient.95-97 The reduced transfer of antigen-specific T lymphocytes may be caused by an already impaired T-cell-mediated immunity before transplant in patients who have received significant prior chemotherapy.
The effectiveness of any cancer immunotherapy in limiting or eliminating malignant cells is a function of the target tumor mass. Even when therapeutically bolstered, immune mechanisms can be rendered ineffective by the presence of overwhelming numbers of target malignant cells. Because high-dose chemotherapy followed by ABMT or ABSCT results in (or is presumed to result) in minimal burden of residual malignant disease it provides a potentially ideal setting for immunotherapy. Administration of Cytokines Interleukin-2 It has been 15 years since the first demonstration that IL-2 activates and promotes proliferation of murine and human NK cells in vitro resulting in both a greater degree and wider spectrum of lytic activity and initial preclinical studies had shown that systemic IL-2 had significant antitumor effects.102,103 This lead to clinical studies using IL-2 regimens with or without adoptive transfer of in vitro activated LAK cells. After the exhilarating results of the initial clinical trials involving high-dose recombinant IL-2 and LAK cells,104 the true response rate of IL-2 with or without the addition of LAK cells was found to be in the range of 15% to 25% for renal cell carcinoma and melanoma.105 Although a variety of tumors of different histological types are sensitive to IL-2/LAK cell therapy, complete eradication of tumor is rare. Nevertheless, because of the measurable tumor regression seen in a significant minority of patients with metastatic malignancies, a logical extension was to perform similar trials of IL-2 after ABMT for hematologic malignancies. The rationale for using IL-2 is based on the following: (1) preclinical data showing that human hematologic malignant cells can be lysed in vitro by IL-2-activated effector cells106-108; (2) IL-2-responsive cells are present early following transplantation74-76; (3) immunotherapy is likely to be more effective when minimal tumor burden is present; and (4) chemotherapy-resistant cells can be lysed by IL-2-activated NK and T cells. IL-2-based trials have included both preclinical and clinical studies.Preclinical studies. Mice inoculated with a leukemic cell line were administered intravenous cyclophosphamide and syngeneic BMT 24 hours later. This was followed by either recombinant (r) IL-2 for 5 days starting on day 1, 7, or 21 or by no further therapy.109 Mice not treated with IL-2 relapsed and died within 50 days posttransplantation, whereas mice receiving IL-2 had long-term disease-free survivals. The maximal antileukemic effect was observed in mice receiving IL-2 3 weeks after BMT. The delayed maximal effect is consistent with and likely results from the delay needed to first achieve maximal lymphocyte reconstitution that can then respond to IL-2. Clinical studies. Trials of continuous-infusion IL-2 administration after ABMT have been performed primarily in hematologic malignancies,83,110-124 although several studies of its use following ABMT for solid tumors have also been performed.83,114,125
Interleukin-7 As noted, T-cell precursors leaving the BM enter the thymus for terminal differentiation. Data from cytokine-deficient mice (knockout mice) suggest that with the exception of IL-7, cytokines can be removed without significantly affecting intra-thymic development.128,129 Mice lacking the IL-7 gene or a functional IL-7 receptor gene have severe impairment of early lymphocyte expansion.128,129 The severe lymphopenia seen in IL-7-deficient mice is associated with normal distribution of T-cell subsets and response to mitogens, suggesting that IL-7 acts on the expansion and proliferation of T cells rather than on their differentiation and function. These multiple effects of IL-7 on T-cell development have led to preclinical studies in murine BMT.Preclinical studies. In a murine model of BMT, IL-7 administration accelerates both T- and B-cell reconstitution by up to 2 to 4 weeks130 and both CD4+ and CD8+ cell counts are found to be expanded. Bolotin et al131 reported that in a syngeneic murine BMT model, injections of IL-7 from day 5 to 18 induced an increase in the cellularity of the thymus by 4 weeks, while the proliferation of early thymic precursor cells was increased nearly eightfold. In contrast, in mice not receiving IL-7, normal numbers of thymocytes appeared only by week 8. Furthermore, in the IL-7-treated mice, distribution of thymic subpopulations approximated those of normal untransplanted mice. Abdul-Hai et al132 reported similar findings of accelerated repopulation of the thymus with IL-7 injected for 10 days immediately after murine transplantation. IL-7 also increased RAG-1 (recombination activator gene) expression in the thymus. Taken together, these data suggest that IL-7 may find a therapeutic role in accelerating T-cell reconstitution after autologous transplantation. Incubation of HSC With Cytokines and Growth Factors Preclinical Studies Incubation of murine BM with IL-2 results in the generation of killer cells with non-MHC-restricted cytotoxicity against tumor cells which appears superior to the cytotoxicity of spleen LAK cells.133-135 Transplantation of IL-2-activated BM (ABM) immediately followed by administration of systemic IL-2 reduces the dissemination of established melanoma and sarcoma in mice more effectively than transplantation with untreated BM with or without systemic IL-2 alone.133,134 This suggests that priming with IL-2 before ABMT induces an antitumor effect capable of eradicating residual malignant disease. When IL-2 therapy is delayed for 1 or 2 weeks after transplantation with ABM, there is a progressive decrease in the cure rate,136 suggesting that ABM cells cannot maintain a prolonged cytotoxicity in vivo. The hematopoietic regenerative capacity of IL-2-activated BM was preserved despite a reduction in viable cell number.Clinical Studies Only limited studies of hematopoietic stem cells exposed to IL-2 have been reported so far and these included small numbers of patients with leukemia, breast cancer, and non-Hodgkin's lymphoma.142,147-149 In the reported studies, BM was maintained with IL-2 for a variety of schedules ranging from 24 hours to 10 days. IL-2-activated BM successfully engrafts patients who had previously received myeloablative chemotherapy. In most studies, additional systemic IL-2 was administered intravenously after transplantation with the expectation that IL-2 would maintain the NK activity. Although in vitro cytotoxicity of IL-2-activated BM against NK-sensitive cell lines was demonstrated, no studies showed any effect against autologous tumor cells. From the preliminary data, it is not yet possible to conclude whether this approach will be successful.Induction of an Autoaggression Syndrome With Cyclosporine A (CsA) Preclinical Studies CsA is a potent immunosuppressive agent that has been used for more than 15 years to prevent GVHD in patients receiving allogeneic BMT. Paradoxically, however, the administration of CsA after syngeneic BMT in rats can lead to the development of an autoimmune phenomenon that is clinically and histologically similar to allogeneic GVHD with the appearance of CD4+ and CD8+ effector cells recognizing MHC class II antigens, including self.150,151 Lethally irradiated rats reconstituted with syngeneic BM and treated with CsA for 40 days develop a T-cell-dependent autoimmune syndrome 14 to 28 days after discontinuation of CsA treatment characterized by erythroderma and dermatitis.150 The mechanism for induction of this autoimmune phenomenon remains unclear. It has been suggested that CsA induces modifications in the thymus, including medullary involution, loss of Hassal's corpuscles, and decreased expression of MHC II antigens in the medulla,152 changes which interfere with intrathymic differentiation of T cells.150,151,153 CsA also appears to enhance the development of autoreactive T lymphocytes by blocking their deletion in the thymus.154 The role of the intact thymus in autoaggression is indicated by the finding that syngeneic GVHD cannot be induced in thymectomized animals.153 However, the inhibition of clonal deletion in the thymus and the development of autoreactive T cells in the periphery is insufficient by itself to induce the autoimmune phenomenon. The ablation of the lympho-hematopoietic system with the preparative regimens for transplantation (irradiation or cytotoxic chemotherapy) is also apparently necessary to eliminate peripheral regulatory mechanisms155,156 because infusion of spleen cells from rats with autoreactive disease into normal rats does not transfer the clinical syndrome. In addition, CsA treatment of untransplanted rats does not induce an autoimmune syndrome.Clinical Studies CsA can induce an autoimmune syndrome in patients with lymphoma, acute myeloid leukemia, or breast cancer receiving ABMT.164-170 This syndrome is mainly confined to the skin (erythematous maculopapular rash) without clinical evidence of visceral involvement. In one report, the presence of cytotoxic T cells recognizing the patient's own pretransplant lymphocytes or tumor cell lines that expressed MHC class II determinants could be shown.164 No analysis of cytotoxicity against autologous fresh tumor cells was reported. The reason why clinical signs of autoaggression are located in the skin remains unknown. This could be related to the presence of Langerhans cells in the dermis or a high expression of MHC II in the skin.
Adoptive Transfer of Ex Vivo-Expanded MHC Nonrestricted Effector Cells As described above, BM or PBSC can be incubated in vitro with cytokines to induce the development of cytotoxic cells. A number of protocols have been devised to select effector cells with cytotoxic activity from PBMC.Activated NK Cells: Clinical Studies Initial enthusiasm for the therapeutic use of LAK came from its use in preclinical and clinical studies against lymphoma and leukemia.171,172 In treating minimal residual malignant disease, LAK cells might be expected to be most effective if they are active against chemotherapy-resistant tumor cells which may have survived pretransplantation high-dose chemotherapy regimens. In in vitro studies, LAK cytotoxicity has been demonstrated against tumor cells surviving therapeutic concentrations of chemotherapeutic agents.173 This in vitro data led to pilot clinical trials combining systemic administration of IL-2 followed by apheresis to generate LAK cells after ABMT or ABSCT in lymphoma patients either in relapse or resistant to primary chemotherapy and in acute leukemia with poor prognostic indicators.115,117
Cytokine-Induced Killer Cells A somewhat different therapeutically useful cytotoxic cell can be obtained by in vitro exposure of PBMC to combinations of IFN-, IL-2,
and anti-CD3 monoclonal antibody. The resultant effector cell termed
cytokine-induced killer cells (CIK) bears a
CD3+CD56+ (but CD16 )
phenotype and demonstrates non-MHC restricted
cytotoxicity.175,176 CIK cells have been found to be
substantially more cytotoxic in culture than LAK cells against cellular
targets and, like LAK cells, they are effective against
chemotherapy-resistant cell lines.177 Although ex vivo
generation of CIK cells is IL-2 dependent, in vivo use of CIK cells has
the advantage over LAK cells of not requiring additional systemic
administration of potentially toxic IL-2 to augment their antitumor
activity. In direct comparison, CIK cells have been shown to result in
greater regression of disseminated human lymphoma in severe combined
immunodeficient (SCID) mice than LAK cells.178,179 While a
significant minority of CIK-treated lymphoma-bearing SCID mice had
long-term survival, none of the LAK-treated mice
survived.178 Because of apparent efficient cytotoxicity and
limited systemic effects, expansion of CIK cells may find a place in
protocols of autologous transplantation.
Cytotoxic Cell Lines Human cell lines with potent MHC nonrestricted cytotoxicity activity against tumor cells have been reported. A cell line termed TALL-104 bearing the characteristic phenotype of cytotoxic cells has been derived from a human acute T-lymphoblastic leukemia and maintained in continuous culture in the presence of IL-2. TALL-104 cells show cytotoxicity exclusively against tumors across species without deleterious effects on normal tissues.179-181 After lethal irradiation, the cells are no longer leukemogenic when injected into SCID mice, but retain their killer function. In murine models bearing human tumors, administration of the human cytotoxic T-cell line had effective antitumor effects when given at early stage of disease.181Adoptive Transfer of Tumor-Specific MHC-Restricted Effector Cells Adoptive cellular immunotherapy can be described as the transfer of target-specific effector cells to treat malignant disease. Such an approach entails the isolation and expansion of effector CD4+ and CD8+ T cells with specific reactivity for tumor cells from the host or other donor. In addition, adoptive immunotherapy requires that such cells survive in vivo for a sufficient amount of time to eradicate the tumor.184 This approach could be combined with injection of autologous stem cells.
Autologous Antigen-Pulsed Dendritic Cells
Induction of Antitumor Effect by Combining Autologous HSC
Transplantation With Infusions of Allogeneic T Cells
Although the regeneration of the CD4 T-cell compartment is generally delayed because of the absence of normal thymic maturation, cellular immunity regains effective levels of function within the first 3 months after transplantation. The use of PBSC in recent years has further contributed to accelerate immune reconstitution in comparison to BM, although the overall advantage of PBSC in this regard remains unclear. Tumor immunotherapy is defined as attempts in vivo to harness the regenerating posttransplant immune responses and apply them against malignant cells. As reviewed here, these attempts fall into one of two categories: induction of nontumor specific cytotoxicity and activation of tumor-directed cellular immunity. Nonspecific methods, including administration of cytokines or incubation of the graft with cytokines, induction of an autoaggression syndrome with cyclosporine, and expansion of NK cells, have not yet been clearly shown to be effective in reducing relapses and improve survival. Furthermore, none of these therapies are without their own side effects. It is unlikely that major progress will be made in the clinical use of cytokines alone, although they may find a therapeutically useful niche enhancing immune effector cells. As for infusion of non-tumor-specific effector cells, administration of activated NK cells or CIK cells requires large-scale cellular expansion, rendering the procedure as yet technically difficult for routine clinical use.
Submitted October 14, 1997;
accepted May 12, 1998.
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J. C. Lavoie, J. M. Connors, G. L. Phillips, D. E. Reece, M. J. Barnett, D. L. Forrest, R. D. Gascoyne, D. E. Hogge, S. H. Nantel, J. D. Shepherd, et al. High-dose chemotherapy and autologous stem cell transplantation for primary refractory or relapsed Hodgkin lymphoma: long-term outcome in the first 100 patients treated in Vancouver Blood, August 15, 2005; 106(4): 1473 - 1478. [Abstract] [Full Text] [PDF]
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M. J. Robertson, H.-C. Chang, D. Pelloso, and M. H. Kaplan Impaired interferon-{gamma} production as a consequence of STAT4 deficiency after autologous hematopoietic stem cell transplantation for lymphoma Blood, August 1, 2005; 106(3): 963 - 970. [Abstract] [Full Text] [PDF]
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U. Hainz, P. Obexer, C. Winkler, P. Sedlmayr, O. Takikawa, H. Greinix, A. Lawitschka, U. Putschger, D. Fuchs, S. Ladisch, et al. Monocyte-mediated T-cell suppression and augmented monocyte tryptophan catabolism after human hematopoietic stem-cell transplantation Blood, May 15, 2005; 105(10): 4127 - 4134. [Abstract] [Full Text] [PDF]
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L. F. Porrata, M. A. Gertz, M. R. Litzow, M. Q. Lacy, A. Dispenzieri, D. J. Inwards, S. M. Ansell, I. N.M. Micallef, D. A. Gastineau, M. Elliott, et al. Early Lymphocyte Recovery Predicts Superior Survival after Autologous Hematopoietic Stem Cell Transplantation for Patients with Primary Systemic Amyloidosis Clin. Cancer Res., February 1, 2005; 11(3): 1210 - 1218. [Abstract] [Full Text] [PDF]
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G. Cartron, H. Watier, J. Golay, and P. Solal-Celigny From the bench to the bedside: ways to improve rituximab efficacy Blood, November 1, 2004; 104(9): 2635 - 2642. [Abstract] [Full Text] [PDF]
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G. R. Kolar, T. Yokota, M. I. D. Rossi, S. K. Nath, and J. D. Capra Human fetal, cord blood, and adult lymphocyte progenitors have similar potential for generating B cells with a diverse immunoglobulin repertoire Blood, November 1, 2004; 104(9): 2981 - 2987. [Abstract] [Full Text] [PDF]
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 I M de Kleer, D M C Brinkman, A Ferster, M Abinun, P Quartier, J van der Net, R ten Cate, L R Wedderburn, G Horneff, J Oppermann, et al. Autologous stem cell transplantation for refractory juvenile idiopathic arthritis: analysis of clinical effects, mortality, and transplant related morbidity Ann Rheum Dis, October 1, 2004; 63(10): 1318 - 1326. [Abstract] [Full Text] [PDF]
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M. J. Robertson, D. Pelloso, R. Abonour, R. A. Hromas, R. P. Nelson Jr., L. Wood, and K. Cornetta Interleukin 12 Immunotherapy after Autologous Stem Cell Transplantation for Hematological Malignancies Clin. Cancer Res., November 1, 2002; 8(11): 3383 - 3393. [Abstract] [Full Text] [PDF]
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M. Hunault-Berger, N. Ifrah, and P. Solal-Celigny Intensive therapies in follicular non-Hodgkin lymphomas Blood, July 30, 2002; 100(4): 1141 - 1152. [Full Text] [PDF]
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A. Heitger, P. Winklehner, P. Obexer, J. Eder, C. Zelle-Rieser, G. Kropshofer, M. Thurnher, and W. Holter Defective T-helper cell function after T-cell-depleting therapy affecting naive and memory populations Blood, May 13, 2002; 99(11): 4053 - 4062. [Abstract] [Full Text] [PDF]
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L. F. Porrata, M. A. Gertz, D. J. Inwards, M. R. Litzow, M. Q. Lacy, A. Tefferi, D. A. Gastineau, A. Dispenzieri, S. M. Ansell, I. N. M. Micallef, et al. Early lymphocyte recovery predicts superior survival after autologous hematopoietic stem cell transplantation in multiple myeloma or non-Hodgkin lymphoma Blood, August 1, 2001; 98(3): 579 - 585. [Abstract] [Full Text] [PDF]
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 G. L. Mancardi, R. Saccardi, M. Filippi, F. Gualandi, A. Murialdo, M. Inglese, M. G. Marrosu, G. Meucci, L. Massacesi, A. Lugaresi, et al. Autologous hematopoietic stem cell transplantation suppresses Gd-enhanced MRI activity in MS Neurology, July 10, 2001; 57(1): 62 - 68. [Abstract] [Full Text] [PDF]
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A Tyndall, J Passweg, and A Gratwohl Haemopoietic stem cell transplantation in the treatment of severe autoimmune diseases 2000 Ann Rheum Dis, July 1, 2001; 60(7): 702 - 707. [Abstract] [Full Text] [PDF]
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A. Sureda, R. Arranz, A. Iriondo, E. Carreras, J.J. Lahuerta, J. Garcia-Conde, I. Jarque, M.D. Caballero, C. Ferra, A. Lopez, et al. Autologous Stem-Cell Transplantation for Hodgkin's Disease: Results and Prognostic Factors in 494 Patients From the Grupo Espanol de Linfomas/Transplante Autologo de Medula Osea Spanish Cooperative Group J. Clin. Oncol., March 1, 2001; 19(5): 1395 - 1404. [Abstract] [Full Text] [PDF]
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L. B. Faulkner, A. Garaventa, A. Paoli, V. Tintori, A. Tamburini, L. Lacitignola, M. Veltroni, M. S. L. Piccolo, E. Viscardi, C. Milanaccio, et al. In Vivo Cytoreduction Studies and Cell Sorting-Enhanced Tumor-Cell Detection in High-Risk Neuroblastoma Patients: Implications for Leukapheresis Strategies J. Clin. Oncol., November 15, 2000; 18(22): 3829 - 3836. [Abstract] [Full Text] [PDF]
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S. J. Richards, G. J. Morgan, and P. Hillmen Immunophenotypic analysis of B cells in PNH: insights into the generation of circulating naive and memory B cells Blood, November 15, 2000; 96(10): 3522 - 3528. [Abstract] [Full Text] [PDF]
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I. Borrello, E. M. Sotomayor, F.-M. Rattis, S. K. Cooke, L. Gu, and H. I. Levitsky Sustaining the graft-versus-tumor effect through posttransplant immunization with granulocyte-macrophage colony-stimulating factor (GM-CSF)-producing tumor vaccines Blood, May 15, 2000; 95(10): 3011 - 3019. [Abstract] [Full Text] [PDF]
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 N. C. Gorin, E. Estey, R. J. Jones, H. I. Levitsky, I. Borrello, and S. Slavin New Developments in the Therapy of Acute Myelocytic Leukemia Hematology, January 1, 2000; 2000(1): 69 - 89. [Abstract] [Full Text] [PDF]
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I. Angulo, F. G. de las Heras, J. F. Garcia-Bustos, D. Gargallo, M. A. Munoz-Fernandez, and M. Fresno Nitric oxide-producing CD11b+Ly-6G(Gr-1)+CD31(ER-MP12)+ cells in the spleen of cyclophosphamide-treated mice: implications for T-cell responses in immunosuppressed mice Blood, January 1, 2000; 95(1): 212 - 220. [Abstract] [Full Text] [PDF]
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 A M Marmont Intense immunosuppression and stem cell transplantation or rescue for severe systemic lupus erythematosus Lupus, May 1, 1999; 8(4): 256 - 257. [PDF]
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V. L. Reichardt, C. Y. Okada, A. Liso, C. J. Benike, K. E. Stockerl-Goldstein, E. G. Engleman, K. G. Blume, and R. Levy Idiotype Vaccination Using Dendritic Cells After Autologous Peripheral Blood Stem Cell Transplantation for Multiple Myeloma---A Feasibility Study Blood, April 1, 1999; 93(7): 2411 - 2419. [Abstract] [Full Text] [PDF]
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F.M. Raaphorst Bone Marrow Transplantation, Fetal B-Cell Repertoire Development, and the Mechanism of Immune Reconstitution Blood, December 15, 1998; 92(12): 4873 - 4874. [Full Text] [PDF]
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| Copyright © 1998 by American Society of Hematology Online ISSN: 1528-0020 | |||||||||
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