Remestemcel-L for the treatment of graft versus host disease

References

• Copelan EA. Hematopoietic stem-cell transplantation. N Engl J Med. 2006;354:1813–1826.
   PubMed Web of Science ®Google Scholar
• Goker H, Haznedaroglu IC, Chao NJ. Acute graft-vs-host disease: pathobiology and management. Exp Hematol. 2001;29:259–277.
   PubMed Web of Science ®Google Scholar
• Ball LM, Egeler RM, Party EPW. Acute GvHD: pathogenesis and classification. Bone Marrow Transplant. 2008;41 Suppl 2:S58–S64.
   PubMed Web of Science ®Google Scholar
• Servais S, Beguin Y, Delens L, et al. Novel approaches for preventing acute graft-versus-host disease after allogeneic hematopoietic stem cell transplantation. Expert Opin Investig Drugs. 2016;9:1–16.
   Google Scholar
• Magenau J, Runaas L, Reddy P. Advances in understanding the pathogenesis of graft-versus-host disease. Br J Haematol. 2016;173:190–205.
   PubMed Web of Science ®Google Scholar
• Marks DI, Lush R, Cavenagh J, et al. The toxicity and efficacy of donor lymphocyte infusions given after reduced-intensity conditioning allogeneic stem cell transplantation. Blood. 2002;100:3108–3114.
   PubMed Web of Science ®Google Scholar
• Van Lint MT, Milone G, Leotta S, et al. Treatment of acute graft-versus-host disease with prednisolone: significant survival advantage for day +5 responders and no advantage for nonresponders receiving anti-thymocyte globulin. Blood. 2006;107:4177–4181.
   PubMed Web of Science ®Google Scholar
• Deeg HJ. How I treat refractory acute GVHD. Blood. 2007;109:4119–4126.
   PubMed Web of Science ®Google Scholar
• Martin PJ, Rizzo JD, Wingard JR, et al. First- and second-line systemic treatment of acute graft-versus-host disease: recommendations of the American Society of Blood and Marrow Transplantation. Biol Blood Marrow Transplant. 2012;18:1150–1163.
   PubMed Web of Science ®Google Scholar
• Dignan FL, Clark A, Amrolia P, et al. Diagnosis and management of acute graft-versus-host disease. Br J Haematol. 2012;158:30–45.
   PubMed Web of Science ®Google Scholar
• Ferrara JL, Levine JE, Reddy P, et al. Graft-versus-host disease. Lancet. 2009;373:1550–1561.
   PubMed Web of Science ®Google Scholar
• Ferrara JL, Reddy P. Pathophysiology of graft-versus-host disease. Semin Hematol. 2006;43:3–10.
   PubMed Web of Science ®Google Scholar
• Reddy P, Ferrara JL. Immunobiology of acute graft-versus-host disease. Blood Rev. 2003;17:187–194.
   PubMed Web of Science ®Google Scholar
• Ratanatharathorn V, Nash RA, Przepiorka D, et al. Phase III study comparing methotrexate and tacrolimus (prograf, FK506) with methotrexate and cyclosporine for graft-versus-host disease prophylaxis after HLA-identical sibling bone marrow transplantation. Blood. 1998;92:2303–2314.
   PubMed Web of Science ®Google Scholar
• Valcárcel D, Sierra J, Wang T, et al. One-antigen mismatched related versus HLA-matched unrelated donor hematopoietic stem cell transplantation in adults with acute leukemia: Center for International Blood and Marrow Transplant Research results in the era of molecular HLA typing. Biol Blood Marrow Transplant. 2011;17:640–648.
   PubMed Web of Science ®Google Scholar
• Friedenstein AJ, Petrakova KV, Kurolesova AI, et al. Heterotopic of bone marrow. Analysis of precursor cells for osteogenic and hematopoietic tissues. Transplantation. 1968;6:230–247.
   PubMed Web of Science ®Google Scholar
• Jones EA, Kinsey SE, English A, et al. Isolation and characterization of bone marrow multipotential mesenchymal progenitor cells. Arthritis Rheum. 2002;46:3349–3360.
   PubMed Web of Science ®Google Scholar
• Dominici M, Le Blanc K, Mueller I, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8:315–317.
   PubMed Web of Science ®Google Scholar
• Mendez-Ferrer S, Michurina TV, Ferraro F, et al. Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature. 2010;466:829–834.
   PubMed Web of Science ®Google Scholar
• Bernardo ME, Fibbe WE. Mesenchymal stromal cells: sensors and switchers of inflammation. Cell Stem Cell. 2013;13:392–402.
   PubMed Web of Science ®Google Scholar
• Le Blanc K, Mougiakakos D. Multipotent mesenchymal stromal cells and the innate immune system. Nat Rev Immunol. 2012;12:383–396.
   PubMed Web of Science ®Google Scholar
• Di Nicola M, Carlo-Stella C, Magni M, et al. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood. 2002;99:3838–3843.
   PubMed Web of Science ®Google Scholar
• Krampera M, Glennie S, Dyson J, et al. Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide. Blood. 2003;101:3722–3729.
   PubMed Web of Science ®Google Scholar
• Maccario R, Podestà M, Moretta A, et al. Interaction of human mesenchymal stem cells with cells involved in alloantigen-specific immune response favors the differentiation of CD4+ T-cell subsets expressing a regulatory/suppressive phenotype. Haematologica. 2005;90:516–525.
   PubMed Web of Science ®Google Scholar
• Benvenuto F, Ferrari S, Gerdoni E, et al. Human mesenchymal stem cells promote survival of T cells in a quiescent state. Stem Cells. 2007;25:1753–1760.
   PubMed Web of Science ®Google Scholar
• Glennie S, Soeiro I, Dyson PJ, et al. Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cells. Blood. 2005;105:2821–2827.
   PubMed Web of Science ®Google Scholar
• Chinnadurai R, Copland IB, Patel SR, et al. IDO-independent suppression of T cell effector function by IFN-γ-licensed human mesenchymal stromal cells. J Immunol. 2014;192:1491–1501.
   PubMed Web of Science ®Google Scholar
• Xue Q, Luan X-Y, Gu Y-Z, et al. The negative co-signaling molecule b7-h4 is expressed by human bone marrow-derived mesenchymal stem cells and mediates its T-cell modulatory activity. Stem Cells Dev. 2010;19:27–38.
   PubMed Web of Science ®Google Scholar
• Bruno S, Deregibus MC, Camussi G. The secretome of mesenchymal stromal cells: role of extracellular vesicles in immunomodulation. Immunol Lett. 2015;168:154–158.
   PubMed Web of Science ®Google Scholar
• Jiang X-X, Zhang Y, Liu B, et al. Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells. Blood. 2005;105:4120–4126.
   PubMed Web of Science ®Google Scholar
• Spaggiari GM, Abdelrazik H, Becchetti F, et al. MSCs inhibit monocyte-derived DC maturation and function by selectively interfering with the generation of immature DCs: central role of MSC-derived prostaglandin E2. Blood. 2009;113:6576–6583.
   PubMed Web of Science ®Google Scholar
• Nauta AJ, Kruisselbrink AB, Lurvink E, et al. Mesenchymal stem cells inhibit generation and function of both CD34+-derived and monocyte-derived dendritic cells. J Immunol. 2006;177:2080–2087.
   PubMed Web of Science ®Google Scholar
• Akiyama K, Chen C, Wang D, et al. Mesenchymal-stem-cell-induced immunoregulation involves FAS-ligand-/FAS-mediated T cell apoptosis. Cell Stem Cell. 2012;10:544–555.
   PubMed Web of Science ®Google Scholar
• Corcione A, Benvenuto F, Ferretti E, et al. Human mesenchymal stem cells modulate B-cell functions. Blood. 2006;107:367–372.
   PubMed Web of Science ®Google Scholar
• Traggiai E, Volpi S, Schena F, et al. Bone marrow-derived mesenchymal stem cells induce both polyclonal expansion and differentiation of B cells isolated from healthy donors and systemic lupus erythematosus patients. Stem Cells. 2008;26:562–569.
   PubMed Web of Science ®Google Scholar
• Rosado MM, Bernardo ME, Scarsella M, et al. Inhibition of B-cell proliferation and antibody production by mesenchymal stromal cells is mediated by T cells. Stem Cells Dev. 2015;24:93–103.
   PubMed Web of Science ®Google Scholar
• Spaggiari GM, Capobianco A, Abdelrazik H, et al. Mesenchymal stem cells inhibit natural killer-cell proliferation, cytotoxicity, and cytokine production: role of indoleamine 2,3-dioxygenase and prostaglandin E2. Blood. 2008;111:1327–1333.
   PubMed Web of Science ®Google Scholar
• Melief SM, Schrama E, Brugman MH, et al. Multipotent stromal cells induce human regulatory T cells through a novel pathway involving skewing of monocytes toward anti-inflammatory macrophages. Stem Cells. 2013;31:1980–1991.
   PubMed Web of Science ®Google Scholar
• Prockop DJ. Concise review: two negative feedback loops place mesenchymal stem/stromal cells at the center of early regulators of inflammation. Stem Cells. 2013;31:2042–2046.
   PubMed Web of Science ®Google Scholar
• Romieu-Mourez R, François M, Boivin M-N, et al. Cytokine modulation of TLR expression and activation in mesenchymal stromal cells leads to a proinflammatory phenotype. J Immunol. 2009;182:7963–7973.
   PubMed Web of Science ®Google Scholar
• Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284:143–147.
   PubMed Web of Science ®Google Scholar
• Kebriaei P, Isola L, Bahceci E, et al. Adult human mesenchymal stem cells added to corticosteroid therapy for the treatment of acute graft-versus-host disease. Biol Blood Marrow Transplant. 2009;15:804–811.
   PubMed Web of Science ®Google Scholar
• Prasad VK, Lucas KG, Kleiner GI, et al. Efficacy and safety of ex vivo cultured adult human mesenchymal stem cells (Prochymal) in pediatric patients with severe refractory acute graft-versus-host disease in a compassionate use study. Biol Blood Marrow Transplant. 2011;17:534–541.
   PubMed Web of Science ®Google Scholar
• Le Blanc K, Rasmusson I, Sundberg B, et al. Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet. 2004;363:1439–1441.
   PubMed Web of Science ®Google Scholar
• Ringdén O, Uzunel M, Rasmusson I, et al. Mesenchymal stem cells for treatment of therapy-resistant graft-versus-host disease. Transplantation. 2006;81:1390–1397.
   PubMed Web of Science ®Google Scholar
• Le Blanc K, Frassoni F, Ball L, et al. Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet. 2008;371:1579–1586.
   PubMed Web of Science ®Google Scholar
• Lucchini G, Introna M, Dander E, et al. Platelet-lysate-expanded mesenchymal stromal cells as a salvage therapy for severe resistant graft-versus-host disease in a pediatric population. Biol Blood Marrow Transplant. 2010;16:1293–1301.
   PubMed Web of Science ®Google Scholar
• Herrmann R, Sturm M, Shaw K, et al. Mesenchymal stromal cell therapy for steroid-refractory acute and chronic graft versus host disease: a phase 1 study. Int J Hematol. 2012;95:182–188.
   PubMed Web of Science ®Google Scholar
• von Bonin M, Kiani A, Platzbecker U, et al. Third-party mesenchymal stem cells as part of the management of graft-failure after haploidentical stem cell transplantation. Leuk Res. 2009;33:e215–e217.
   PubMedGoogle Scholar
• Fang B, Song Y, Liao L, et al. Favorable response to human adipose tissue-derived mesenchymal stem cells in steroid-refractory acute graft-versus-host disease. Transplant Proc. 2007;39:3358–3362.
   PubMed Web of Science ®Google Scholar
• Muller I, Kordowich S, Holzwarth C, et al. Application of multipotent mesenchymal stromal cells in pediatric patients following allogeneic stem cell transplantation. Blood Cells Mol Dis. 2008;40:25–32.
   PubMed Web of Science ®Google Scholar
• Perez-Simon JA, Lopez-Villar O, Andreu EJ, et al. Mesenchymal stem cells expanded in vitro with human serum for the treatment of acute and chronic graft-versus-host disease: results of a phase I/II clinical trial. Haematologica. 2011;96:1072–1076.
   PubMed Web of Science ®Google Scholar
• Resnick IB, Barkats C, Shapira MY, et al. Treatment of severe steroid resistant acute GVHD with mesenchymal stromal cells (MSC). Am J Blood Res. 2013;3:225–238.
   PubMedGoogle Scholar
• Ball LM, Bernardo ME, Roelofs H, et al. Multiple infusions of mesenchymal stromal cells induce sustained remission in children with steroid-refractory, grade III-IV acute graft-versus-host disease. Br J Haematol. 2013;163:501–509.
   PubMed Web of Science ®Google Scholar
• Introna M, Lucchini G, Dander E, et al. Treatment of graft versus host disease with mesenchymal stromal cells: a phase I study on 40 adult and pediatric patients. Biol Blood Marrow Transplant. 2014;20:375–381.
   PubMed Web of Science ®Google Scholar
• Sanchez-Guijo F, Caballero-Velazquez T, Lopez-Villar O, et al. Sequential third-party mesenchymal stromal cell therapy for refractory acute graft-versus-host disease. Biol Blood Marrow Transplant. 2014;20:1580–1585.
   PubMed Web of Science ®Google Scholar
• Zhao K, Lou R, Huang F, et al. Immunomodulation effects of mesenchymal stromal cells on acute graft-versus-host disease after hematopoietic stem cell transplantation. Biol Blood Marrow Transplant. 2015;21:97–104.
   PubMed Web of Science ®Google Scholar
• Te Boome LC, Mansilla C, van der Wagen LE, et al. Biomarker profiling of steroid-resistant acute GVHD in patients after infusion of mesenchymal stromal cells. Leukemia. 2015;29:1839–1846.
   PubMed Web of Science ®Google Scholar
• von Dalowski F, Kramer M, Wermke M, et al. Mesenchymal stromal cells for treatment of acute steroid-refractory graft versus host disease: clinical responses and long-term outcome. Stem Cells. 2016;34:357–366.
   PubMed Web of Science ®Google Scholar
• Muroi K, Miyamura K, Ohashi K, et al. Unrelated allogeneic bone marrow-derived mesenchymal stem cells for steroid-refractory acute graft-versus-host disease: a phase I/II study. Int J Hematol. 2013;98:206–213.
   PubMed Web of Science ®Google Scholar
• Muroi K, Miyamura K, Okada M, et al. Bone marrow-derived mesenchymal stem cells (JR-031) for steroid-refractory grade III or IV acute graft-versus-host disease: a phase II/III study. Int J Hematol. 2016;103:243–250.
   PubMed Web of Science ®Google Scholar
• Kurtzberg J, Prockop S, Teira P, et al. Allogeneic human mesenchymal stem cell therapy (remestemcel-L, Prochymal) as a rescue agent for severe refractory acute graft-versus-host disease in pediatric patients. Biol Blood Marrow Transplant. 2014;20:229–235.
   PubMed Web of Science ®Google Scholar
• Kurtzberg J, Prockop SE, Prasad VK, et al. Effect of humanmesenchymal stemcells (Remestemcel-L) on clinical response and survival confirmed in a large cohort of pediatric patients with severe high-risk steroid- refractory acute graft versus host disease. Biol Blood Marrow Transplant. 2016;22:S59.
   Web of Science ®Google Scholar
• Martin PJ, Uberti JP, Soiffer RJ, et al. Prochymal improves response rates in patients with steroid-refractory acute graft versus host disease (SR-GVHD) involving the liver and gut: results of a randomized, placebo-controlled, multicenter phase III trial in GVHD. Biol Blood Marrow Transplant. 2010;16:S169–S170.
   Web of Science ®Google Scholar
• Szabolcs P, Visani G, Locatelli F, et al. Treatment of steroid-refractory acute GVHD with mesenchymal stem cells improves outcomes in pediatric patients; results of the pediatric subset in a phase III randomized, placebocontrolled study. Biol Blood Marrow Transplant. 2010;16:S298.
   Google Scholar
• Tarte K, Gaillard J, Lataillade JJ, et al. Clinical-grade production of human mesenchymal stromal cells: occurrence of aneuploidy without transformation. Blood. 2010;115:1549–1553.
   PubMed Web of Science ®Google Scholar
• Prockop DJ, Keating A. Relearning the lessons of genomic stability of human cells during expansion in culture: implications for clinical research. Stem Cells. 2012;30:1051–1052.
   PubMed Web of Science ®Google Scholar
• Tolar J, Nauta AJ, Osborn MJ, et al. Sarcoma derived from cultured mesenchymal stem cells. Stem Cells. 2007;25:371–379.
   PubMed Web of Science ®Google Scholar
• Bernardo ME, Emons JA, Karperien M, et al. Human mesenchymal stem cells derived from bone marrow display a better chondrogenic differentiation compared with other sources. Connect Tissue Res. 2007;48:132–140.
   PubMed Web of Science ®Google Scholar
• Torsvik A, Rosland GV, Svendsen A, et al. Spontaneous malignant transformation of human mesenchymal stem cells reflects cross-contamination: putting the research field on track - letter. Cancer Res. 2010;70:6393–6396.
   PubMed Web of Science ®Google Scholar
• Lucchini G, Dander E, Pavan F, et al. Mesenchymal stromal cells do not increase the risk of viral reactivation nor the severity of viral events in recipients of allogeneic stem cell transplantation. Stem Cells Int. 2012;2012:690236.
   PubMed Web of Science ®Google Scholar
• Balan A, Lucchini G, Schmidt S, et al. Mesenchymal stromal cells in the antimicrobial host response of hematopoietic stem cell recipients with graft-versus-host disease–friends or foes? Leukemia. 2014;28:1941–1948.
   PubMed Web of Science ®Google Scholar
• Calkoen FG, Vervat C, van Halteren AG, et al. Mesenchymal stromal cell therapy is associated with increased adenovirus-associated but not cytomegalovirus-associated mortality in children with severe acute graft-versus-host disease. Stem Cells Transl Med. 2014;3:899–910.
   PubMed Web of Science ®Google Scholar
• Hashmi S, Ahmed M, Murad MH, et al. Survival after mesenchymal stromal cell therapy in steroid-refractory acute graft-versus-host disease: systematic review and meta-analysis. Lancet Haematol. 2016;3:e45–e52.
   PubMed Web of Science ®Google Scholar
• Karlsson C, Brantsing C, Svensson T, et al. Differentiation of human mesenchymal stem cells and articular chondrocytes: analysis of chondrogenic potential and expression pattern of differentiation-related transcription factors. J Orthop Res. 2007;25:152–163.
   PubMed Web of Science ®Google Scholar
• Malcherek G, Jin N, Hückelhoven AG, et al. Mesenchymal stromal cells inhibit proliferation of virus-specific CD8(+) T cells. Leukemia. 2014;28:2388–2394.
   PubMed Web of Science ®Google Scholar
• Auletta JJ, Eid SK, Wuttisarnwattana P, et al. Human mesenchymal stromal cells attenuate graft-versus-host disease and maintain graft-versus-leukemia activity following experimental allogeneic bone marrow transplantation. Stem Cells. 2015;33:601–614.
   PubMed Web of Science ®Google Scholar
• von Bahr L, Sundberg B, Lönnies L, et al. Long-term complications, immunologic effects, and role of passage for outcome in mesenchymal stromal cell therapy. Biol Blood Marrow Transplant. 2012;18:557–564.
   PubMed Web of Science ®Google Scholar
• Galipeau J. The mesenchymal stromal cells dilemma–does a negative phase III trial of random donor mesenchymal stromal cells in steroid-resistant graft-versus-host disease represent a death knell or a bump in the road? Cytotherapy. 2013;15:2–8.
   PubMed Web of Science ®Google Scholar
• Ankrum JA, Ong JF, Karp JM. Mesenchymal stem cells: immune evasive, not immune privileged. Nat Biotechnol. 2014;32:252–260.
   PubMed Web of Science ®Google Scholar
• Wuchter P, Bieback K, Schrezenmeier H, et al. Standardization of good manufacturing practice-compliant production of bone marrow-derived human mesenchymal stromal cells for immunotherapeutic applications. Cytotherapy. 2015;17:128–139.
   PubMed Web of Science ®Google Scholar
• François M, Romieu-Mourez R, Li M, et al. Human MSC suppression correlates with cytokine induction of indoleamine 2,3-dioxygenase and bystander M2 macrophage differentiation. Mol Ther. 2012;20:187–195.
   PubMed Web of Science ®Google Scholar
• Schepers K, Fibbe WE. Unraveling mechanisms of mesenchymal stromal cell-mediated immunomodulation through patient monitoring and product characterization. Ann N Y Acad Sci. 2016;1370:15–23
   PubMed Web of Science ®Google Scholar
• Dander E, Lucchini G, Vinci P, et al. Mesenchymal stromal cells for the treatment of graft-versus-host disease: understanding the in vivo biological effect through patient immune monitoring. Leukemia. 2012;26:1681–1684.
   PubMed Web of Science ®Google Scholar
• Calkoen FG, Jol-van der Zijde CM, Mearin ML, et al. Gastrointestinal acute graft-versus-host disease in children: histology for diagnosis, mesenchymal stromal cells for treatment, and biomarkers for prediction of response. Biol Blood Marrow Transplant. 2013;19:1590–1599.
   PubMed Web of Science ®Google Scholar
• Jitschin R, Mougiakakos D, von Bahr L, et al. Alterations in the cellular immune compartment of patients treated with third-party mesenchymal stromal cells following allogeneic hematopoietic stem cell transplantation. Stem Cells. 2013;31:1715–1725.
   PubMed Web of Science ®Google Scholar
• Yin F, Battiwalla M, Ito S, et al. Bone marrow mesenchymal stromal cells to treat tissue damage in allogeneic stem cell transplant recipients: correlation of biological markers with clinical responses. Stem Cells. 2014;32:1278–1288.
   PubMed Web of Science ®Google Scholar
• Galipeau J, Krampera M. The challenge of defining mesenchymal stromal cell potency assays and their potential use as release criteria. Cytotherapy. 2015;17:125–127.
   PubMed Web of Science ®Google Scholar
• Galipeau J, Krampera M, Barrett J, et al. International Society for Cellular Therapy perspective on immune functional assays for mesenchymal stromal cells as potency release criterion for advanced phase clinical trials. Cytotherapy. 2016;18:151–159.
   PubMed Web of Science ®Google Scholar
• Duijvestein M, Vos AC, Roelofs H, et al. Autologous bone marrow-derived mesenchymal stromal cell treatment for refractory luminal Crohn’s disease: results of a phase I study. Gut. 2010;59:1662–1669.
   PubMed Web of Science ®Google Scholar
• Ciccocioppo R, Bernardo ME, Sgarella A, et al. Autologous bone marrow-derived mesenchymal stromal cells in the treatment of fistulising Crohn’s disease. Gut. 2011;60:788–798.
   PubMed Web of Science ®Google Scholar
• Algeri M, Conforti A, Pitisci A, et al. Mesenchymal stromal cells and chronic inflammatory bowel disease. Immunol Lett. 2015;168:191–200.
   PubMed Web of Science ®Google Scholar
• Miyamura K. Insurance approval of mesenchymal stem cell for acute GVHD in Japan: need of follow up for some remaining concerns. Int J Hematol. 2016;103:155–164.
   PubMed Web of Science ®Google Scholar