Biomarker profiling of steroid-resistant acute GVHD in patients after infusion of mesenchymal stromal cells

Leukemia

Volumn 29, Issue 9, 2015, Pages 1839-1846

  Te Boome, L C J ^a   Mansilla, C ^a   Van Der Wagen, L E ^a   Lindemans, C A ^a   Petersen, E J ^a   Spierings, E ^a   Thus, K A ^a   Westinga, K ^a   Plantinga, M ^a   Bierings, M ^a   Broers, A E C ^b   Cuijpers, M L H ^a   Van Imhoff, G W ^c   Janssen, J J ^d   Huisman, C ^e   Zeerleder, S ^e   Huls, G ^f   Boelens, J J ^a   Wulffraat, N M ^a   Slaper Cortenbach, I C M ^a   Kuball, J ^a   more..

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b ERASMUS MEDICAL CENTER   (Netherlands)

^c UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^d VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^e AM ^*  (Netherlands)

^f RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; CYCLOSPORIN; ELAFIN; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR; INTERLEUKIN 21; INTERLEUKIN 22; INTERLEUKIN 23; INTERLEUKIN 4; INTERLEUKIN 6; INTERLEUKIN 8; LEUKEMIA ANTIGEN; MINOR HISTOCOMPATIBILITY ANTIGEN; PREDNISOLONE; REGENERATING ISLET DERIVED PROTEIN 3ALPHA; SCATTER FACTOR; STEROID; TELOMERASE REVERSE TRANSCRIPTASE; TUMOR ANTIGEN; TUMOR NECROSIS FACTOR RECEPTOR 1; UNCLASSIFIED DRUG; CYTOKINE; IMMUNOSUPPRESSIVE AGENT; PREDNISONE;

ACUTE GRAFT VERSUS HOST DISEASE; ADOLESCENT; ADULT; AGED; ARTICLE; CANCER MORTALITY; CARCINOGENICITY; CELL MEMBRANE POTENTIAL; CHILD; CLINICAL ARTICLE; CLINICAL ASSESSMENT; CLINICAL EVALUATION; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; GRAFT SURVIVAL; HUMAN; IMMUNE RESPONSE; LEUKEMIA RELAPSE; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MYELOID DENDRITIC CELL; OUTCOME ASSESSMENT; OVERALL SURVIVAL; PATIENT SAFETY; PHASE 2 CLINICAL TRIAL; PRIORITY JOURNAL; PROSPECTIVE STUDY; T LYMPHOCYTE; TREATMENT RESPONSE; ACUTE DISEASE; BLOOD; CLINICAL TRIAL; DRUG RESISTANCE; GRAFT VS HOST DISEASE; IMMUNOLOGY; IMMUNOPHENOTYPING; INFANT; LYMPHOCYTE; MESENCHYMAL STROMA CELL; METABOLISM; MIDDLE AGED; MORTALITY; PRESCHOOL CHILD; PROGNOSIS; TREATMENT OUTCOME; YOUNG ADULT;

ACUTE DISEASE; ADOLESCENT; ADULT; AGED; ANTIGENS, NEOPLASM; BIOMARKERS; CHILD; CHILD, PRESCHOOL; CYCLOSPORINE; CYTOKINES; DRUG RESISTANCE; FEMALE; GRAFT VS HOST DISEASE; HUMANS; IMMUNOPHENOTYPING; IMMUNOSUPPRESSIVE AGENTS; INFANT; LYMPHOCYTES; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MIDDLE AGED; PREDNISONE; PROGNOSIS; STEROIDS; TREATMENT OUTCOME; YOUNG ADULT;

EID: 84940788141     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2015.89     Document Type: Article

References (51)

1. MacMillan ML, Couriel D, Weisdorf DJ, Schwab G, Havrilla N, Fleming TR et al. A phase 2/3 multicenter randomized clinical trial of ABX-CBL versus ATG as secondary therapy for steroid-resistant acute graft-versus-host disease. Blood 2007; 109: 2657-2662.
2. Lee SJ, Zahrieh D, Agura E, MacMillan ML, Maziarz RT, McCarthy PL Jr et al. Effect of up-front daclizumab when combined with steroids for the treatment of acute graft-versus-host disease: results of a randomized trial. Blood 2004; 104: 1559-1564.
3. Alousi AM, Weisdorf DJ, Logan BR, Bolanos-Meade J, Carter S, Difronzo N et al. Etanercept, mycophenolate, denileukin, or pentostatin plus corticosteroids for acute graft-versus-host disease: a randomized phase 2 trial from the Blood and Marrow Transplant Clinical Trials Network. Blood 2009; 114: 511-517.
4. Levine JE, Paczesny S, Mineishi S, Braun T, Choi SW, Hutchinson RJ et al. Etanercept plus methylprednisolone as initial therapy for acute graft-versus-host disease. Blood 2008; 111: 2470-2475.
5. Bolanos-Meade J, Logan BR, Alousi AM, Antin JH, Barowski K, Carter SL et al. Phase 3 clinical trial of steroids/mycophenolate mofetil vs steroids/placebo as therapy for acute GVHD: BMT CTN 0802. Blood 2014; 124: 3221-3227.
6. Le Blanc K, Rasmusson I, Sundberg B, Gotherstrom C, Hassan M, Uzunel M et al. Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet 2004; 363: 1439-1441.
7. Ringden O, Uzunel M, Rasmusson I, Remberger M, Sundberg B, Lonnies H et al. Mesenchymal stem cells for treatment of therapy-resistant graft-versus-host disease. Transplantation 2006; 81: 1390-1397.
8. Le Blanc K, Frassoni F, Ball L, Locatelli F, Roelofs H, Lewis I 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.
9. Uccelli A, Moretta L, Pistoia V. Mesenchymal stem cells in health and disease. Nat Rev Immunol 2008; 8: 726-736.
10. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999; 284: 143-147.
11. Porada CD, Zanjani ED, Meida-Porad G. Adult mesenchymal stem cells: a pluripotent population with multiple applications. Curr Stem Cell Res Ther 2006; 1: 365-369.
12. von BM, Stolzel F, Goedecke A, Richter K, Wuschek N, Holig K et al. Treatment of refractory acute GVHD with third-party MSC expanded in platelet lysatecontaining medium. Bone Marrow Transplant 2009; 43: 245-251.
13. Kebriaei P, Isola L, Bahceci E, Holland K, Rowley S, McGuirk J 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.
14. Lucchini G, Introna M, Dander E, Rovelli A, Balduzzi A, Bonanomi S 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.
15. Prasad VK, Lucas KG, Kleiner GI, Talano JA, Jacobsohn D, Broadwater G 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.
16. Perez-Simon JA, Lopez-Villar O, Andreu EJ, Rifon J, Muntion S, Campelo MD 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.
17. Herrmann R, Sturm M, Shaw K, Purtill D, Cooney J, Wright M 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.
18. Dander E, Lucchini G, Vinci P, Introna M, Masciocchi F, Perseghin 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.
19. Muroi K, Miyamura K, Ohashi K, Murata M, Eto T, Kobayashi N 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.
20. Ball LM, Bernardo ME, Roelofs H, van Tol MJ, Contoli B, Zwaginga JJ 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.
21. Resnick IB, Barkats C, Shapira MY, Stepensky P, Bloom AI, Shimoni A et al. Treatment of severe steroid resistant acute GVHD with mesenchymal stromal cells (MSC). Am J Blood Res 2013; 3: 225-238.
22. Kurtzberg J, Prockop S, Teira P, Bittencourt H, Lewis V, Chan KW 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.
23. Introna M, Lucchini G, Dander E, Galimberti S, Rovelli A, Balduzzi A 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 2013; 20: 375-381.
24. Levine JE, Logan BR, Wu J, Alousi AM, Bolanos-Meade J, Ferrara JL et al. Acute graft-versus-host disease biomarkers measured during therapy can predict treatment outcomes: a Blood and Marrow Transplant Clinical Trials Network study. Blood 2012; 119: 3854-3860.
25. Vander Lugt MT, Braun TM, Hanash S, Ritz J, Ho VT, Antin JH et al. ST2 as a marker for risk of therapy-resistant graft-versus-host disease and death. N Engl J Med 2013; 369: 529-539.
26. Ponce DM, Hilden P, Mumaw C, Devlin SM, Lubin M, Giralt S et al. High day 28 ST2 levels predict for acute graft-versus-host disease and transplant-related mortality after cord blood transplantation. Blood 2014; 125: 199-205.
27. Quah BJ, Warren HS, Parish CR. Monitoring lymphocyte proliferation in vitro and in vivo with the intracellular fluorescent dye carboxyfluorescein diacetate succinimidyl ester. Nat Protoc 2007; 2: 2049-2056.
28. Kuball J, de BK Wagner E, Wattad M, Antunes E, Weeratna RD et al. Pitfalls of vaccinations with WT1-, proteinase3-and MUC1-derived peptides in combination with MontanideISA51 and CpG7909. Cancer Immunol Immunother 2011; 60: 161-171.
29. MacMillan ML, DeFor TE, Weisdorf DJ. The best endpoint for acute GVHD treatment trials. Blood 2010; 115: 5412-5417.
30. Martin PJ, Rizzo JD, Wingard JR, Ballen K, Curtin PT, Cutler C 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.
31. Schmoor C, Schumacher M, Finke J, Beyersmann J. Competing risks and multistate models. Clin Cancer Res 2013; 19: 12-21.
32. Paczesny S, Krijanovski OI, Braun TM, Choi SW, Clouthier SG, Kuick R et al. A biomarker panel for acute graft-versus-host disease. Blood 2009; 113: 273-278.
33. Ferrara JL, Harris AC, Greenson JK, Braun TM, Holler E, Teshima T et al. Regenerating islet-derived 3-alpha is a biomarker of gastrointestinal graft-versus-host disease. Blood 2011; 118: 6702-6708.
34. Paczesny S, Braun TM, Levine JE, Hogan J, Crawford J, Coffing B et al. Elafin is a biomarker of graft-versus-host disease of the skin. Sci Transl Med 2010; 2: 13ra2.
35. Maccario R, Podesta M, Moretta A, Cometa A, Comoli P, Montagna D et al. Interaction of human mesenchymal stem cells with cells involved in alloantigenspecific immune response favors the differentiation of CD4+ T-cell subsets expressing a regulatory/suppressive phenotype. Haematologica 2005; 90: 516-525.
36. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 2005; 105: 1815-1822.
37. Jiang XX, Zhang Y, Liu B, Zhang SX, Wu Y, Yu XD et al. Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells. Blood 2005; 105: 4120-4126.
38. Beyth S, Borovsky Z, Mevorach D, Liebergall M, Gazit Z, Aslan H et al. Human mesenchymal stem cells alter antigen-presenting cell maturation and induce T-cell unresponsiveness. Blood 2005; 105: 2214-2219.
39. Spaggiari GM, Abdelrazik H, Becchetti F, Moretta L. MSCs inhibit monocytederived 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.
40. Vakkila J, Thomson AW, Hovi L, Vettenranta K, Saarinen-Pihkala UM. Circulating dendritic cell subset levels after allogeneic stem cell transplantation in children correlate with time post transplant and severity of acute graft-versus-host disease. Bone Marrow Transplant 2005; 35: 501-507.
41. Jitschin R, Mougiakakos D, Von BL, Volkl S, Moll G, Ringden O 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.
42. Hawiger D, Inaba K, Dorsett Y, Guo M, Mahnke K, Rivera M et al. Dendritic cells induce peripheral T cell unresponsiveness under steady state conditions in vivo. J Exp Med 2001; 194: 769-779.
43. Lutz MB, Schuler G. Immature, semi-mature and fully mature dendritic cells: which signals induce tolerance or immunity? Trends Immunol 2002; 23: 445-449.
44. Johnson TR, Johnson CN, Corbett KS, Edwards GC, Graham BS. Primary human mDC1, mDC2, and pDC dendritic cells are differentially infected and activated by respiratory syncytial virus. PLoS One 2011; 6: e16458.
45. Maggini J, Mirkin G, Bognanni I, Holmberg J, Piazzon IM, Nepomnaschy I et al. Mouse bone marrow-derived mesenchymal stromal cells turn activated macrophages into a regulatory-like profile. PLoS One 2010; 5: e9252.
46. Rasmusson I, Ringden O, Sundberg B, Le BK. Mesenchymal stem cells inhibit lymphocyte proliferation by mitogens and alloantigens by different mechanisms. Exp Cell Res 2005; 305: 33-41.
47. Krampera M, Glennie S, Dyson J, Scott D, Laylor R, Simpson E 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.
48. Harris AC, Ferrara JL, Braun TM, Holler E, Teshima T, Levine JE et al. Plasma biomarkers of lower gastrointestinal and liver acute GVHD. Blood 2012; 119: 2960-2963.
49. Liu X, Qu X, Chen Y, Liao L, Cheng K, Shao C et al. Mesenchymal stem/stromal cells induce the generation of novel IL-10-dependent regulatory dendritic cells by SOCS3 activation. J Immunol 2012; 189: 1182-1192.
50. Chiesa S, Morbelli S, Morando S, Massollo M, Marini C, Bertoni A et al. Mesenchymal stem cells impair in vivo T-cell priming by dendritic cells. Proc Natl Acad Sci USA 2011; 108: 17384-17389.
51. Lucchini G, Dander E, Pavan F, Di CI, Balduzzi A, Perseghin P 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.