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Mini-Review Extracorporeal Photopheresis in Chronic Graft-Versus-Host Disease

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Mini-Review Extracorporeal Photopheresis in Chronic Graft-Versus-Host Disease Bone Marrow Transplantation (2002) 29, 719–725 2002 Nature Publishing Group All rights reserved 0268–3369/02 $25.00 www.nature.com/bmt Mini-review Extracorporeal photopheresis in chronic graft-versus-host disease FM Foss, G Gorgun and KB Miller Bone Marrow Transplantation and Experimental Therapeutics, Tufts New England Medical Center, Boston, MA, USA Summary: Histopathologic changes which include sclerodermatous skin changes resulting from collagen deposition, pulmonary Despite significant advances in stem cell manipulation fibrosis, esophageal dysfunction, dry mouth or mucocutane- and post-transplant immunosuppression, chronic graft- ous ulcerations, cholestasis and myositis or fasciitis are versus-host disease (cGVHD) remains a cause of major thought to be initiated, in part, by autoantibodies to cell long-term morbidity in survivors of allogeneic stem cell surface and intracellular proteins.9 Conventional therapeutic transplantation. Extracorporeal photopheresis (ECP) is approaches for cGVHD, including corticosteroids and a novel therapeutic intervention which has demon- immunosuppressive agents have demonstrated limited effi- strated efficacy in patients with refractory acute and cacy in patients with extensive disease. Ultraviolet A ther- chronic GVHD. Clinical responses have been reported apy (PUVA), while effective in alleviating the symptoms in skin and visceral GVHD. While the long-term immu- of chronic skin GVHD, has had no impact on visceral nomodulatory effects of ECP in cGVHD are unknown, involvement.10–13 Novel strategies, including humanized recent studies of patients undergoing a 6- to 12-month anti-CD25 antibody (dacluzimab) and and anti-TNF-␣ anti- course of ECP treatment demonstrated an attenuation body (infliximab), have shown promise in limited pilot of Th1-mediated cytokine secretion by activated T- studies.14–17 helper cells, a shift in the DC1/DC2 ratio favoring plas- macytoid rather than monocytoid dendritic cell profiles, and a decrease in antigen responsiveness by dendritic Extracorporeal phototherapy cells. The implications of these immunomodulatory effects of ECP on pathogenesis and clinical outcome Extracorporeal phototherapy (ECP) is an immunothera- remains a fertile area for future research. peutic modality that has demonstrated clinical efficacy in Bone Marrow Transplantation (2002) 29, 719–725. DOI: cutaneous T cell lymphoma/Sezary syndrome (CTCL), 10.1038/sj/bmt/1703529 scleroderma, and other autoimmune disorders. ECP Keywords: extracorporeal photopheresis; dendritic cells; involves extracorporeal exposure of peripheral blood mono- graft-versus-host disease; T cell subsets; allogeneic BMT nuclear cells to photoactivated 8-methoxypsoralen (8- MOP), followed by reinfusion of the treated cells. 8-MOP is a naturally occurring furocourarin that is biologically inert, unless exposed to ultraviolet A light, whereupon it Graft-versus-host disease (GVHD) remains a major cause becomes photoactivated and covalently binds and cross- of morbidity and mortality after allogeneic stem cell trans- links DNA, leading to initiation of apoptosis. During a sin- plantation. While improvements in immunosuppressive gle treatment cycle of ECP, approximately 240 cc of buffy regimens have reduced the frequency and severity of acute coat and 300 ml of plasma are collected into a buffy coat GVHD, the incidence of chronic GVHD remains bag from six collection cycles. The cells are exposed to unchanged at 27–50% after sibling matched related donor UVA at 2 Jcm2/cell beginning immediately after the first transplants and 42–72% after unrelated donor bone marrow cells are collected.18 Examination of the cells after UVA 1–6 or peripheral blood stem cell transplanted. Factors asso- exposure and prior to reinfusion demonstrates that about 2– ciated with cGVHD have been well-described and include 5% of the total circulating peripheral blood mononuclear increased donor and recipient age, HLA-disparate and unre- cells undergo apoptosis.18 An intravenous formulation of 8- lated donor transplants, prior acute GVHD, and use of allo- MOP, UVADEX, allows direct instillation of the photosen- 7,8 immune female donors. sitizing agent into the collected plasma and buffy coat ex The onset of cGVHD has arbitrarily been defined as vivo prior to UVA exposure. occurring 100 days after allogeneic stem cell infusion, and ECP was initially developed by Edelson et al19 as a ther- its clinical features are distinguished from acute GVHD in apy for patients with cutaneous T cell lymphoma with cir- 7,8 that they more closely resemble autoimmune diseases. culating Sezary leukemia cells. Response rates of up to 60% were reported in the initial study with a median time Correspondence: Dr FM Foss, Bone Marrow Transplantation and Experi- to response of 4–6 months, when the treatment was admin- 20–22 mental Therapeutics, Tufts New England Medical Center, Boston, MA istered for 2 consecutive days each month. In a retro- 02111, USA spective analysis of 450 patients treated in the United States Extracorporeal photopheresis in chronic GVHD FM Foss et al 720 and Europe, response rates of 56% and 66%, respectively, chronic stimulatory graft-versus-host reaction with clinical were reported. Response rates were higher in patients with features of systemic lupus erythematosis, injection of circulating clonal CD4+/CD7− Sezary cells and in those UVA/8-MOP-treated D2 splenocytes was capable of atten- with an intact immune system as determined by a normal uating the effects of GVHD that had been initiated by prior CD4/CD8 ratio.23 The anti-tumor effect correlated with the injection of D2 cells to initiate lupus-like disease.30 These appearance of CD8+ cytotoxic T cells in the peripheral results supported the concept that photoactivated T cells blood as well as the cells infiltrating into cutaneous tumor might be responsible for induction of a vaccine-like effect, and plaque lesions. While the absolute number of Sezary although the putative anti-idiotype T cell populations have leukemia cells decreased in most patients during ECP, there not been fully characterized. was no significant long-term modulation of normal CD4+ T lymphocyte populations. Although the mechanisms are less clear, ECP has also demonstrated similar efficacy in a number of autoimmune disorders, including scleroderma, Effects of ECP on lymphocytes, monocytes and pemphigus vulgaris, rheumatoid arthritis, systemic lupus dendritic cells erythematosis, and solid organ allograft rejection (Table 1).22,24–28 The anti-idiotype response to clonal T cell populations induced by ECP is likely to be induced by UVA-mediated cellular damage.31 T lymphocytes appear to be most sensi- Mechanism of action of ECP: preclinical models tive to this effect, as demonstrated by Yoo et al,32 who showed that normal T cell and Sezary T leukemia cells, but The mechanism of action of UVA-mediated immunomod- not other mononuclear populations, demonstrated morpho- ulation was first described in mice exposed to ultraviolet A logic evidence of apoptosis within 24 h after ECP treat- light in the presence of 8-MOP (PUVA). Immunosuppres- ment. In this study, 8-MOP alone failed to induce sion was accompanied by a decrease in the number and apoptosis, but exposure to UVA alone was associated with function of epidermal Langerhans cells and alteration in induction of early markers of apoptosis, including Annexin cytokine production by keratinocytes.13 The administration V.18 Failure to detect apoptotic lymphocytes from 1–24 h of 8-MOP and UVA irradiated spleen and bone marrow after ECP may be related to uptake and clearance of these cells to mice receiving allografts resulted in a significant cells by the reticuloendothelial system.32 attenuation of GVHD compared to littermates who received In addition to initiating DNA strand breaks, upregulation non-UVA irradiated cells, demonstrating an effect of UVA of FAS expression on T lymphocytes may be another mech- exposure on effectors of alloreactivity.29 In another study, anism by which ECP induces apoptosis. Since T lympho- using C57BL/6 × DBA/2)F1 (B6D2F1) mice which, when cytes also express FAS ligand, self-induction of cell death inoculated with parental DBA/2 (D2) splenocytes, develop may occur in the treated lymphocytes in the absence of cytokine secretion from monocytes or other accessory 33 Table 1 Extracorporeal phototherapy: advantages, toxicities, uses cells. This may explain the observed selective effect of and results ECP on T lymphocytes, but not on B lymphocytes or mono- nuclear cells. Diseases in which ECP has been used Selective effects of ECP on subpopulations of activated Cutaneous T cell lymphoma T cells have been observed in treated patients. Normaliz- Scleroderma ation of CD4/CD8 ratios has been described in CTCL Pemphigus 34 Systemic lupus erythermatosis patients, as well as a shift from predominantly Th2 to Th1 Inflammatory bowel disease cytokine secretion. In the context of CTCL, the restoration Solid organ allograft rejection of Th1 cytokine secretion increases IL-12 production by Acute and chronic GVHD following allogeneic stem cell transplant monocytes, which might subsequently inhibit Th2 cytokine Outcomes from therapy secreting cells that are believed to be responsible for the Decrease in circulating Sezary leukemia cells in CTCL clinical manifestations of CTCL.35 Improvement in skin and visceral GVHD While monocytes appear to be resistant to the apoptotic Decreased lymphocytic infiltration in cardiac allografts ␣ Attenuation of rejection in liver and renal allografts effects
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