Reduced efficacy of mesenchymal stromal cells in preventing graft-versus-host disease in an in vivo model of haploidentical bone marrow transplant with leukemia

Cell Transplantation

Volumn 22, Issue 8, 2013, Pages 1381-1394

  Oviedo, Alberto ^a   Yañez, Rosa ^a   Colmenero, Isabel ^b   Aldea, Montserrat ^a   Rubio, Antonio ^a   Bueren, Juan Antonio ^a   Lamana, María Luisa ^a  

^a CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE ENFERMEDADES RARAS CIBERER   (Spain)

^b HOSPITAL INFANTIL UNIVERSITARIO NIÑO JESÚS   (Spain)

Author keywords

Graft versus host disease (GVHD) prevention; Graft versus leukemia (GVL) effect; Mesenchymal stromal cells (MSCS); Mouse model

Indexed keywords

RETROVIRUS VECTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW TRANSPLANTATION; CANCER CELL; CELL SURVIVAL; CHRONIC MYELOID LEUKEMIA; CONTROLLED STUDY; FEMALE; GRAFT VERSUS HOST REACTION; HAPLOIDY; IN VITRO STUDY; IN VIVO STUDY; IRRADIATION; LETHALITY; MESENCHYMAL STROMA CELL; MORTALITY; MOUSE; MYELOPROLIFERATIVE DISORDER; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; RELAPSE; SPLEEN CELL;

ADENOVIRIDAE; ANIMALS; BONE MARROW; BONE MARROW TRANSPLANTATION; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; FEMALE; FUSION PROTEINS, BCR-ABL; GRAFT VS HOST DISEASE; HAPLOIDY; HEMATOPOIETIC STEM CELL TRANSPLANTATION; LEUKEMIA; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED C57BL; RECURRENCE; RETROVIRIDAE; SPLEEN; T-LYMPHOCYTES; TRANSDUCTION, GENETIC; TREATMENT OUTCOME;

EID: 84881013788     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368912X657666     Document Type: Article

References (41)

1. Aggarwal, S.; Pittenger, M. F. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 105(4):1815-1822; 2005.
2. Allison, M. Genzyme backs Osiris, despite Prochymal flop. Nat. Biotechnol. 27(11):966-967; 2009.
3. Baron, F.; Lechanteur, C.; Willems, E.; Bruck, F.; Baudoux, E.; Seidel, L.; Vanbellinghen, J. F.; Hafraoui, K.; Lejeune, M.; Gothot, A.; Fillet, G.; Beguin, Y. Cotransplantation of mesenchymal stem cells might prevent death from graftversus-host disease (GVHD) without abrogating graftversus-tumor effects after HLA-mismatched allogeneic transplantation following nonmyeloablative conditioning. Biol. Blood Marrow Transplant. 16(6):838-847; 2010.
4. Bocchia, M.; Korontsvit, T.; Xu, Q.; Mackinnon, S.; Yang, S. Y.; Sette, A.; Scheinberg, D. A. Specific human cellular immunity to bcr-abl oncogene-derived peptides. Blood 87(9):3587-3592; 1996.
5. Bogunovic, M.; Ginhoux, F.; Wagers, A.; Loubeau, M.; Isola, L. M.; Lubrano, L.; Najfeld, V.; Phelps, R. G.; Grosskreutz, C.; Scigliano, E.; Frenette, P; Merad, M. Identification of a radioresistant and cycling dermal dendritic cell population in mice and men. J. Exp. Med. 203(12):2627-2638; 2006.
6. Chakraverty, R.; Sykes, M. The role of antigen-presenting cells in triggering graft-versus-host disease and graft-versusleukemia. Blood 110(1):9-17; 2007.
7. Choudhury, A.; Gajewski, J. L.; Liang, J. C.; Popat, U.; Claxton, D. F.; Kliche, K. O.; Andreeff, M.; Champlin, R. E. Use of leukemic dendritic cells for the generation of antileukemic cellular cytotoxicity against Philadelphia chromosome-positive chronic myelogenous leukemia. Blood 89(4):1133-1142; 1997.
8. Djouad, F.; Bony, C.; Apparailly, F.; Louis-Plence, P.; Jorgensen, C.; Noel, D. Earlier onset of syngeneic tumors in the presence of mesenchymal stem cells. Transplantation 82(8):1060-1066; 2006.
9. Djouad, F.; Plence, P.; Bony, C.; Tropel, P.; Apparailly, F.; Sany, J.; Noel, D.; Jorgensen, C. Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood 102(10):3837-3844; 2003.
10. Durakovic, N.; Bezak, K. B.; Skarica, M.; Radojcic, V.; Fuchs, E. J.; Murphy, G. F.; Luznik, L. Host-derived Langerhans cells persist after MHC-matched allografting independent of donor T-cells and critically influence the alloresponses mediated by donor lymphocyte infusions. J. Immunol. 177(7):4414-4425; 2006.
11. Falkenburg, J.; Wafelman, A.; Joosten, P.; Smit, W.; van Bergen, C.; Bongaerts, R; Lurvink, E.; van der Hoorn, M.; Kluck P.; Landegent J.; Kluin-Nelemans, H.; Fibbe, W.; Willemze, R. Complete remission of accelerated phase chronic myeloid leukemia by treatment with leukemia-reactive cytotoxic T lymphocytes. Blood 94(4):1201-1208; 1999.
12. Fang, B.; Song, Y.; Zhao, R. C.; Han, Q.; Lin, Q. Using human adipose tissue-derived mesenchymal stem cells as salvage therapy for hepatic graft-versus-host disease resembling acute hepatitis. Transplant. Proc. 39(5):1710-1713; 2007.
13. Heymer, B. Clinical and Diagnostic Pathology of Graft versus Host Disease, 1st ed. Berlin Heidelberg, Germany: Springer-Verlag; 2002.
14. Jiang, X. X.; Zhang, Y.; Liu, B.; Zhang, S. X.; Wu, Y.; Yu, X. D.; Mao, N. Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells. Blood 105(10):4120-4126; 2005.
15. Karnoub, A. E.; Dash, A. B.; Vo, A. P.; Sullivan, A.; Brooks, M. W.; Bell, G. W.; Richardson, A. L.; Polyak, K.; Tubo, R.; Weinberg, R. A. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 449(7162):557-563; 2007.
16. Kebriaei, P.; Isola, L.; Bahceci, E.; Holland, K.; Rowley, S.; McGuirk, J.; Devetten, M.; Jansen, J.; Herzig, R.; Schuster, M; Monroy, R; Uberti, J. Adult human mesenchymal stem cells added to corticosteroid therapy for the treatment of acute graft-versus-host disease. Biol. Blood Marrow Transplant. 15(7):804-811; 2009.
17. Kolb, H. J. Graft-versus-leukemia effects of transplantation and donor lymphocytes. Blood 112(12):4371-4383; 2008.
18. Kolb, H. J.; Schattenberg, A.; Goldman, J. M.; Hertenstein, B.; Jacobsen, N.; Arcese, W.; Ljungman, P.; Ferrant, A.; Verdonck, L.; Niederwieser, D. Graft-versus-leukemia effect of donor lymphocyte transfusions in marrow grafted patients. Blood 86(5):2041-2050; 1995.
19. Kolb, H. J.; Schmid, C.; Barrett, A. J.; Schendel, D. J. Graft-versus-leukemia reactions in allogeneic chimeras. Blood 103(3):767-776; 2004.
20. Lazarus, H.; Koc, O.; Devine, S.; Curtin, P.; Maziarz, R.; Holland, H.; Shpall, E.; McCarthy, P.; Atkinson, K.; Cooper, B.; Gerson, S.; Laughlin, M.; Loberiza, F.; Moseley, A.; Bacigalupo, A. Cotransplantation of HLA-identical sibling culture-expanded mesenchymal stem cells and hematopoietic stem cells in hematologic malignancy patients. Biol. Blood Marrow Transplant. 11(5):389-398; 2005.
21. Le Blanc, K,Mesenchymal stromal cells: Tissue repair and immune modulation. Cytotherapy 8(6):559-561; 2006.
22. Le Blanc, K.; Frassoni, F.; Ball, L.; Locatelli, F.; Roelofs, H.; Lewis, I.; Lanino, E.; Sundberg, B.; Bernardo, M. E.; Remberger, M.; Dini, G.; Egeler, M.; Bacigalupo, A.; Fibbe, W.; Ringdén, O. Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: A phase II study. Lancet 371(9624):1579-1586; 2008.
23. Le Blanc, K.; Rasmusson, I.; Sundberg, B.; Gotherstrom, C.; Hassan, M.; Uzunel, M.; Ringden, O. Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet 363(9419):1439-1441; 2004.
24. Le Blanc, K.; Tammik, L.; Sundberg, B.; Haynesworth, S. E.; Ringden, O. Mesenchymal stem cells inhibit and stimulate mixed lymphocyte cultures and mitogenic responses independently of the major histocompatibility complex. Scand. J. Immunol. 57(1):11-20; 2003.
25. Liang, L.; Dong, C.; Chen, X.; Fang, Z.; Xu, J.; Liu, M.; Zhang, X.; Gu, D. S.; Wang, D.; Du, W.; Zhu, D.; Han, Z. Human umbilical cord mesenchymal stem cells ameliorate mice tnbsinduced colitis. Cell Transplant. 20(9):1395-1408; 2011.
26. Mielcarek, M.; Martin, P. J.; Leisenring, W.; Flowers, M. E.; Maloney, D. G.; Sandmaier, B. M.; Maris, M. B.; Storb, R. Graft-versus-host disease after nonmyeloablative versus conventional hematopoietic stem cell transplantation. Blood 102(2):756-762; 2003.
27. Muller, I.; Kordowich, S.; Holzwarth, C.; Isensee, G.; Lang, P.; Neunhoeffer, F.; Dominici, M.; Greil, J.; Handgretinger, R. Application of multipotent mesenchymal stromal cells in pediatric patients following allogeneic stem cell transplantation. Blood Cells Mol. Dis. 40(1):25-32; 2008.
28. Ning, H.; Yang, F.; Jiang, M.; Hu, L.; Feng, K.; Zhang, J.; Yu, Z.; Li, B.; Xu, C.; Li, Y.; Wang, J.; Hu, J.; Lou, X.; Chen, H. The correlation between cotransplantation of mesenchymal stem cells and higher recurrence rate in hematologic malignancy patients: Outcome of a pilot clinical study. Leukemia 22(3):593-599; 2008.
29. Pear, W. S.; Miller, J. P.; Xu, L.; Pui, J. C.; Soffer, B.; Quackenbush, R. C.; Pendergast, A. M.; Bronson, R.; Aster, J. C.; Scott, M. L.; Baltimore, D. Efficient and rapid induction of a chronic myelogenous leukemia-like myeloproliferative disease in mice receiving P210 bcr/abl-transduced bone marrow. Blood 92(10):3780-3792; 1998.
30. Rasmusson, I.; Ringden, O.; Sundberg, B.; Le Blanc, K. Mesenchymal stem cells inhibit lymphocyte proliferation by mitogens and alloantigens by different mechanisms. Exp. Cell Res. 305(1):33-41; 2005.
31. Rasmusson, I.; Uhlin, M.; Le Blanc, K.; Levitsky, V. Mesenchymal stem cells fail to trigger effector functions of cytotoxic T lymphocytes. J. Leukoc. Biol. 82(4):887-893; 2007.
32. Sattler, C.; Steinsdoerfer, M.; Offers, M.; Fischer, E.; Schierl, R.; Heseler, K.; Daubener, W.; Seissler, J. Inhibition of T-cell proliferation by murine multipotent mesenchymal stromal cells is mediated by CD39 expression and adenosine generation. Cell Transplant. 20:1221-1230; 2011.
33. Smit, W. M.; Rijnbeek, M.; van Bergen, C. A.; Fibbe, W. E.; Willemze, R.; Falkenburg, J. H. T-cells recognizing leukemic CD34(+) progenitor cells mediate the antileukemic effect of donor lymphocyte infusions for relapsed chronic myeloid leukemia after allogeneic stem cell transplantation. Proc. Natl. Acad. Sci. USA 95(17):10152-10157; 1998.
34. Terme, M.; Borg, C.; Guilhot, F.; Masurier, C.; Flament, C.; Wagner, E. F.; Caillat-Zucman, S.; Bernheim, A.; Turhan, A. G.; Caignard, A.; Zitvogel, L. BCR/ABL promotes dendritic cell-mediated natural killer cell activation. Cancer Res. 65(14):6409-6417; 2005.
35. Tolar, J.; Le Blanc, K.; Keating, A.; Blazar, B. R. Concise review: Hitting the right spot with mesenchymal stromal cells. Stem Cells 28(8):1446-1455, 2010.
36. Tolar, J.; Villeneuve, P.; Keating, A. Mesenchymal stromal cells for graft-versus-host disease. Hum. Gene Ther. 22(3): 257-262, 2011.
37. Uccelli, A.; Pistoia, V.; Moretta, L. Mesenchymal stem cells: A new strategy for immunosuppression? Trends Immunol. 28(5):219-226; 2007.
38. Van Etten, R. A,Retroviral transduction models of Ph leukemia: Advantages and limitations for modeling human hematological malignancies in mice. Blood Cells Mol. Dis. 27(1):201-205; 2001.
39. Van Etten, R. A. Studying the pathogenesis of BCR-ABL leukemia in mice. Oncogene 21(56):8643-8651; 2002.
40. von Bonin, M.; Stolzel, F.; Goedecke, A.; Richter, K.; Wuschek, N.; Holig, K.; Platzbecker, U.; Illmer, T.; Schaich, M.; Schetelig, J.; Kiani, A.; Ordemann, R.; Ehninger, G.; Schmitz, M.; Bornhäuser, M. Treatment of refractory acute GVHD with third-party MSC expanded in platelet lysatecontaining medium. Bone Marrow Transplant. 43(3):245-251; 2009.
41. Yanez, R.; Lamana, M. L.; Garcia-Castro, J.; Colmenero, I.; Ramirez, M.; Bueren, J. A. Adipose tissue-derived mesenchymal stem cells have in vivo immunosuppressive properties applicable for the control of the graft-versus-host disease. Stem Cells 24(11):2582-2591; 2006.