Mesenchymal stromal cells and hematopoietic stem cell transplantation

Immunology Letters

Volumn 168, Issue 2, 2015, Pages 215-221

  Bernardo, Maria Ester ^a,b   Fibbe, Willem E ^c  

^a SAN RAFFAELE SCIENTIFIC INSTITUTE   (Italy)

^b BAMBINO GESÙ CHILDREN S HOSPITAL   (Italy)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Engraftment; Graft versus host disease; Hematopoietic stem cell transplantation; Immunoregulatory properties; Mesenchymal stromal cells

Indexed keywords

ADAPTIVE IMMUNITY; ARTICLE; CELL EXPANSION; CELL FUNCTION; CELL TRANSPLANTATION; ENGRAFTMENT; EX VIVO STUDY; GRAFT VERSUS HOST REACTION; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; IMMUNE RESPONSE; IMMUNOREGULATION; INNATE IMMUNITY; MESENCHYMAL STROMA CELL; MESENCHYMAL STROMA CELL TRANSPLANTATION; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; TREATMENT RESPONSE; ALLOTRANSPLANTATION; CLINICAL TRIAL (TOPIC); CYTOLOGY; GRAFT SURVIVAL; HEMATOPOIETIC STEM CELL; IMMUNOLOGY; MESENCHYMAL STEM CELL TRANSPLANTATION; PROCEDURES; TREATMENT OUTCOME;

CLINICAL TRIALS AS TOPIC; GRAFT SURVIVAL; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEMATOPOIETIC STEM CELLS; HUMANS; IMMUNITY, INNATE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; TRANSPLANTATION, HOMOLOGOUS; TREATMENT OUTCOME;

EID: 84949626345     PISSN: 01652478     EISSN: 18790542     Source Type: Journal    
DOI: 10.1016/j.imlet.2015.06.013     Document Type: Article

References (85)

1. Friedenstein A.J., Petrakova K.V., Kurolesova A.I., Frolova G.P. Heterotopic of bone marrow. Analysis of precursor cells for osteogenic and hematopoietic tissues. Transplantation 1968, 6:230-247.
2. Friedenstein A.J., Deriglasova U.F., Kulagina N.N., Panasuk A.F., Rudakowa S.F., Luriá E.A., Ruadkow I.A. Precursors for fibroblast in different populations of hematopoietic cells as detected by the in vitro colony assay method. Exp. Hematol. 1947, 2:83-92.
3. Ho M.S., Mei S.H., Stewart D.J. The immunomodulatory and therapeutic effects of mesenchymal stromal cells for acute lung injury and sepsis. J. Cell. Physiol. 2015, 10.1002/jcp.25028.
4. Wang Y., Chen X., Cao W., Shi Y. Plasticity of mesenchymal stem cells in immunomodulation: pathological and therapeutic implications. Nat. Immunol. 2014, 15:1009-1016.
5. Nauta A.J., Fibbe W.E. Immunomodulatory properties of mesenchymal stromal cells. Blood 2007, 110:3499-3506.
6. Le Blanc K., Mougiakakos D. Multipotent mesenchymal stromal cells and the innate immune system. Nat. Rev. Immunol. 2012, 12:383-396.
7. Bernardo M.E., Fibbe W.E. Mesenchymal stromal cells: sensors and switchers of inflammation. Cell Stem Cell 2013, 13:392-402.
8. Wang L., Li Y., Chen X., Chen J., Gautam S.C., Xu Y., Chopp M. MCP-1, MIP-1, IL-8 and ischemic cerebral tissue enhance human bone marrow stromal cell migration in interface culture. Hematology 2002, 7:113-117.
9. Ball L.M., Bernardo M.E., Roelofs H., Lankester A., Cometa A., Egeler R.M., Locatelli F., Fibbe W.E. Co-transplantation of ex-vivo expanded mesenchymal stem cells accelerates lymphocyte recovery and may reduce the risk of graft failure in haploidentical hematopoietic stem cell transplantation. Blood 2007, 110:2764-2767.
10. Bernardo M.E., Ball L.M., Cometa A.M., Roelofs H., Zecca M., Avanzini M.A., Bertaina A., Vinti L. Co-infusion of ex vivo expanded, parental mesenchymal stromal cells prevents life-threatening acute GvHD, but does not reduce the risk of graft failure in pediatric patients undergoing allogeneic umbilical cord blood transplantation. Bone Marrow Transplant. 2011, 46:200-207.
11. Le Blanc K., Frassoni F., Ball L., Locatelli F., Roelofs H., Lewis I., Lanino E., Sundberg B. Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet 2008, 371:1579-1586.
12. Ringden O., Uzunel M., Sundberg B., Lönnies L., Nava S., Gustafsson J., Henningsohn L., Le Blanc K. Tissue repair using mesenchymal stem cells for hemorrhagic cystitis, pneumomediastinum and perforated colon. Leukemia 2007, 21:2271-2276.
13. Ciccocioppo R., Bernardo M.E., Sgarella A., Maccario R., Avanzini M.A., Ubezio C., Minelli A., Alvisi C. Autologous bone marrow-derived mesenchymal stromal cells in the treatment of fistulising Crohn's disease. Gut 2011, 60:788-798.
14. Dominici M., Le Blanc K., Mueller I., Slaper-Cortenbach I., Marini F., Krause D., Deans R., Keating A. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006, 8:315-317.
15. Najar M., Rodrigues R.M., Buyl K., Branson S., Vanhaecke T., Lagneaux L., Rogiers V., De Kock J. Proliferative and phenotypical characteristics of human adipose tissue-derived stem cells: comparison of Ficoll gradient centrifugation and red blood cell lysis buffer treatment purification methods. Cytotherapy 2014, 16:1220-1228.
16. Melief S.M., Zwaginga J.J., Fibbe W.E., Roelofs H. Adipose tissue-derived multipotent stromal cells have a higher immunomodulatory capacity than their bone marrow-derived counterparts. Stem Cells Transl. Med. 2013, 2:455-463.
17. Im G.I., Shin Y.W., Lee K.B. Do adipose tissue-derived mesenchymal stem cells have the same osteogenic and chondrogenic potential as bone marrow-derived cells. Osteoarthr. Cartil. 2005, 13:845-853.
18. Campagnoli C., Roberts I.A., Kumar S., Bennett P.R., Bellantuono I., Fisk N.M. Identification of mesenchymal stem/progenitor cells in human first-trimester fetal blood, liver, and bone marrow. Blood 2001, 98:2396-2402.
19. in't Anker P.S., Scherjon S.A., Kleijburg-van der Keur C., de Groot-Swings G.M., Claas F.H., Fibbe W.E., Kanhai H.H. Amniotic fluid as a novel source of mesenchymal stem cells for therapeutic transplantation. Blood 2003, 102:1548-1549.
20. Wong S.P., Rowley J.E., Redpath A.N., Tilman J.D., Fellous T.G., Johnson J.R. Pericytes, mesenchymal stem cells and their contributions to tissue repair. Pharmacol. Ther. 2015, pii:S0163-7258(15)00075-3. 10.1016/j.pharmthera.2015.03.006.
21. Crisan M., Yap S., Casteilla L., Chen C.W., Corselli M., Park T.S., Andriolo G., Sun B. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 2008, 3:301-313.
22. Crisan M., Corselli M., Chen W.C., Péault B. Perivascular cells for regenerative medicine. J. Cell. Mol. Med. 2012, 16:2851-2860.
23. Sacchetti B., Funari A., Michienzi S., Di Cesare S., Piersanti S., Saggio I., Tagliafico E., Ferrari S. Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell 2007, 131:324-336.
24. Gang E.J., Bosnakovski D., Figueiredo C.A., Visser J.W., Perlingeiro R.C. SSEA-4 identifies mesenchymal stem cells from bone marrow. Blood 2007, 109:1743-1751.
25. Simmons P.J., Torok-Storb B. Identification of stromal cell precursors in human bone marrow by a novel monoclonal antibody, STRO-1. Blood 1991, 78:55-62.
26. Battula V.L., Treml S., Bareiss P.M., Gieseke F., Roelofs H., de Zwart P., Müller I., Schewe B. Isolation of functionally distinct mesenchymal stem cells subsets using antibodies against CD56, CD271, and mesenchymal stem cell antigen-1 (MSCA-1). Haematologica 2009, 94:173-184.
27. Avanzini M.A., Bernardo M.E., Cometa A.M., Perotti C., Zaffaroni N., Novara F., Visai L., Moretta A. Generation of mesenchymal stromal cells in the presence of platelet lysate: a phenotypical and functional comparison of umbilical cord blood- and bone marrow-derived progenitors. Haematologica 2009, 94:1649-1660.
28. Schallmoser K., Bartmann C., Rohde E., Reinisch A., Kashofer K., Stadelmeyer E., Drexler C., Lanzer G. Human platelet lysate can replace fetal bovine serum for clinical-scale expansion of functional mesenchymal stromal cells. Transfusion 2007, 47:1436-1446.
29. Lucchini G., Introna M., Dander E., Rovelli A., Balduzzi A., Bonanomi S., Salvadè A., Capelli C. 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.
30. Introna M., Lucchini G., Dander E., Galimberti S., Rovelli A., Balduzzi A., Longoni D., Pavan F. 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.
31. Capelli C., Domenghini M., Borleri G., Bellavita P., Poma R., Carobbio A., Micò C., Rambaldi A. Human platelet lysate allows expansion and clinical grade production of mesenchymal stromal cells from small samples of bone marrow aspirates or marrow filter washouts. Bone Marrow Transplant. 2007, 40:785-791.
32. Le Blanc K., Tammik L., Sundberg B., Haynesworth S.E., Ringdén O. Mesenchymal stem cells inhibit and stimulate mixed lymphocyte cultures and mitogenic responses independently of the major histocompatibility complex. Scand. J. Immunol. 2003, 57:11-20.
33. Di Nicola M., Carlo-Stella C., Magni M., Milanesi M., Longoni P.D., Matteucci P., Grisanti S., Gianni A.M. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or non specific mitogenic stimuli. Blood 2002, 99:3838-3843.
34. Tse W.T., Pendleton J.D., Beyer W.M., Egalka M.C., Guinan E.C. Suppression of allogeneic T-cell proliferation by human marrow stromal cells: implications in transplantation. Transplantation 2003, 75:389-397.
35. Krampera M., Glennie S., Dyson J., Scott D., Laylor R., Simpson E., Dazzi F. Bone marrow mesenchymal stem cells inhibit the response of naïve and memory antigen-specific T cells to their cognate peptide. Blood 2003, 101:3722-3729.
36. Rasmusson I., Ringden O., Sundberg B., LeBlanc K. Mesenchymal stem cells inhibit the formation of cytotoxic T lymphocytes, but not activated cytotoxic T lymphocytes or natural killer cells. Transplantation 2003, 76:1208-1213.
37. Meisel R., Zibert A., Laryea M., Göbel U., Däubener W., Dilloo D. Human bone marrow stromal cells inhibit allogeneic T-cell responses by indolamine 2,3-dioxygenase-mediated tryptophan degradation. Blood 2004, 103:4619-4621.
38. Chabannes D., Hill M., Merieau E., Rossignol J., Brion R., Soulillou J.P., Anegon I., Cuturi M.C. A role for heme oxygenase-1 in the immunosuppressive effect of adult rat and human mesenchymal stem cells. Blood 2007, 110:3691-3694.
39. Burr S.P., Dazzi F., Garden O.A. Mesenchymal stromal cells and regulatory T cells: the Yin and Yang of peripheral tolerance?. Immunol. Cell Biol. 2013, 91:12-18.
40. + T-cell subsets expressing regulatory/suppressive phenotype. Haematologica 2005, 90:516-525.
41. + regulatoryTcells. Clin. Exp. Immunol. 2009, 156:149-160.
42. Melief S.M., Schrama C.L.M., Brugman M.H., Tiemessen M.M., Hoogduijn M.J., Fibbe W.E., Roelofs H. Multipotent stromal cells induce human regulatory T cells through a novel pathway involving skewing of monocytes towards anti-inflammatory macrophages. Stem Cells 2013, 31:1980-1991.
43. Akiyama K., Chen C., Wang D., Xu X., Qu C., Yamaza T., Cai T., Chen W. Mesenchymal-stem-cell-induced immunoregulation involves FAS-ligand-/FAS-mediated T cell apoptosis. Cell Stem Cell 2012, 10:544-555.
44. Duijvestein M., Wildenberg M.E., Welling M.M., Hennink S., Molendijk I., van Zuylen V.L., Bosse T., Vos A.C. Pretreatment with interferon-gamma enhances the therapeutic activity of mesenchymal stromal cells in animal models of colitis. Stem Cells 2011, 29:1549-1558.
45. Cutler A.J., Limbani V., Girdlestone J., Navarrete C.V. Umbilical cord-derived mesenchymal stromal cells modulate monocyte function to suppress T cell proliferation. J. Immunol. 2010, 185:6617-6623.
46. 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 2005, 105:4120-4126.
47. +-derived and monocyte-derived dendritic cells. J. Immunol. 2006, 177:2080-2087.
48. Corcione A., Benvenuto F., Ferretti E., Giunti D., Cappiello V., Cazzanti F., Risso M., Gualandi F. Human mesenchymal stem cells modulate B cell functions. Blood 2006, 107:367-372.
49. Krampera M., Cosmi L., Angeli R., Pasini A., Liotta F., Andreini A., Santarlasci V., Mazzinghi B. Role of interferon-gamma in the immunomodulatory activity of human bone marrow mesenchymal stem cells. Stem Cells 2006, 24:386-398.
50. Traggiai E., Volpi S., Schena F., Gattorno M., Ferlito F., Moretta L., Martini A. 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.
51. Rosado M.M., Bernardo M.E., Scarsella M., Conforti A., Giorda E., Biagini S., Cascioli S., Rossi F. Inhibition of B-cell proliferation and antibody production by mesenchymal stromal cells is mediated by T cells. Stem Cells Dev. 2014, 24:93-103.
52. Sotiropoulou P.A., Perez S.A., Gritzapis A.D., Baxevanis C.N., Papamichail M. Interactions between human mesenchymal stem cells and natural killer cells. Stem Cells 2006, 24:74-85.
53. Spaggiari G.M., Capobianco A., Becchetti S., Mingari M.C., Moretta L. Mesenchymal stem cell-natural killer cell interactions: evidence that activated NK cells are capable of killing MSCs, whereas MSCs can inhibit IL-2-induced NK-cell proliferation. Blood 2006, 107:1484-1490.
54. Nauta A.J., Westerhuis G., Kruisselbrink A.B., Lurvink E.G., Willemze R., Fibbe W.E. Donor-derived mesenchymal stem cells are immunogenic in an allogeneic host and stimulate donor graft rejection in a non-myeloablative setting. Blood 2006, 108:2114-2120.
55. Keating A. Mesenchymal stromal cells: new directions. Cell Stem Cell 2012, 10:709-716.
56. Eggenhofer E., Hoogduijn M.J. Mesenchymal stem cell-educated macrophages. Transplant. Res. 2012, 1:12.
57. Nemeth K., Leelahavanichkul A., Yuen P.S., Mayer B., Parmelee A., Doi K., Robey P.G., Leelahavanichkul K. Bone marrow stromal cells attenuate sepsis via prostaglandin E 2-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nat. Med. 2009, 15:42-49.
58. Chen L., Tredget E.E., Wu P.Y., Wu Y. Paracrine factors of mesenchymal stem cells recruit macrophages and endothelial lineage cells and enhance wound healing. PLoS ONE 2008, 3:e1886.
59. Melief S.M., Geutskens S.B., Fibbe W.E., Roelofs H. Multipotent stromal cells skew monocytes towards an anti-inflammatory IL-10 producing phenotype by production of IL-6. Haematologica 2013, 98:888-895.
60. Ren G., Zhang L., Zhaon X., Xu G., Zhang Y., Roberts A.I., Zhao R.C., Shi Y. Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell 2008, 2:141-150.
61. Li W., Ren G., Huang Y., Su J., Han Y., Li J., Chen X., Cao K. Mesenchymal stem cells: a double-edged sword in regulating immune responses. Cell Death Differ. 2012, 19:1505-1513.
62. Waterman R.S., Tomchuck S.L., Henkle S.L., Betancourt A.M. A new mesenchymal stem cell (MSC) paradigm: polarization into a pro-inflammatory MSC1 or an Immunosuppressive MSC2 phenotype. PLoS ONE 2010, 5:e10088.
63. Prockop D.J., Oh J.Y. Mesenchymal stem/stromal cells (MSCs): role as guardians of inflammation. Mol. Ther. 2012, 20:14-20.
64. Kfoury Y., Scadden D.T. Mesenchymal cell contributions to the stem cell niche. Cell Stem Cell 2015, 16:239-253.
65. Boulais P.E., Frenette P.S. Making sense of hematopoietic stem cell niches. Blood 2015, 125:2621-2629.
66. Almeida-Porada G., Porada C.D., Tran N., Zaniani E.D. Co-transplantation of human stromal cell progenitors into pre-immune fetal sheep results in early appearance of human donor cells in circulation and boosts cell levels in bone marrow at later time points after transplantation. Blood 2000, 95:3620-3627.
67. + cells in NOD/SCID mice. Exp. Hematol. 2002, 30:870-878.
68. Koc O.N., Gerson S.L., Cooper B.W., Dyhouse S.M., Haynesworth S.E., Caplan A.I., Lazarus H.M. Rapid hematopoietic recovery after co-infusion of autologous-blood stem cells and culture-expanded marrow mesenchymal stem cells in advanced breast cancer patients receiving high-dose chemotherapy. J. Clin. Oncol. 2000, 18:307-316.
69. Lazarus H.M., Koc O.N., Devine S.M., Curtin P., Maziarz R.T., Holland H.K., Shpall E.J., McCarthy P. Cotransplantation of HLA-identical sibling culture-expanded mesenchymal stem cells and hematopoietic stem cells in hematologic malignancy patients. Biol. Blood Marrow Transplant. 2005, 11:389-398.
70. MacMillan M.L., Blazar B.R., DeFor T.E., Wagner J.E. Transplantation of culture-expanded haploidentical mesenchymal stem cells to promote engraftment in pediatric recipients of unrelated donor umbilical cord blood: results of a phase I-II clinical trial. Bone Marrow Transplant. 2008, 43:1-8.
71. Gonzalo-Daganzo R., Regidor C., Martìn-Donaire T., Rico M.A., Bautista G., Krsnik I., Forés R., Ojeda E. Results of a pilot study on the use of third-party mesenchymal stromal cells in cord blood transplantation in adults. Cytotherapy 2009, 11:278-288.
72. Wu Y., Cao Y., Li X., Xu L., Wang Z., Liu P., Yan P., Liu Z. Cotransplantation of haploidentical hematopoietic and umbilical cord mesenchymal stem cells for severe aplastic anemia: successful engraftment and mild GVHD. Stem Cell Res. 2014, 12:132-138.
73. Wu Y., Wang Z., Cao Y., Xu L., Li X., Liu P., Yan P., Liu Z. Cotransplantation of haploidentical hematopoietic and umbilical cord mesenchymal stem cells with a myeloablative regimen for refractory/relapsed hematologic malignancy. Ann. Hematol. 2013, 92:1675-1684.
74. Robinson S.N., Ng J., Niu T., Yang H., McMannis J.D., Karandish S., Kaur I., Fu P. Superior ex vivo cord blood expansion following co-culture with bone marrow-derived mesenchymal stem cells. Bone Marrow Transplant. 2006, 37:359-366.
75. de Lima M., McNiece I., Robinson S.N., Munsell M., Eapen M., Horowitz M., Alousi A., Saliba R. Cord-blood engraftment with ex vivo mesenchymal-cell coculture. N. Engl. J. Med. 2012, 367:2305-2315.
76. Sudres M., Norol F., Trenado A., Grégoire S., Charlotte F., Levacher B., Lataillade J.J., Bourin P. Bone marrow mesenchymal stem cells suppress lymphocyte proliferation in vitro but fail to prevent graft-versus-host-disease in mice. J. Immunol. 2006, 176:7761-7767.
77. Tisato V., Naresh K., Girdlestone J., Navarrete C., Dazzi F. Mesenchymal stem cells of cord blood origin are effective at preventing but not treating graft-versus-host disease. Leukemia 2007, 21:1992-1999.
78. Polchert D., Sobinsky J., Douglas G., Kidd M., Moadsiri A., Reina E., Genrich K., Mehrotra S. IFN-gamma activation of mesenchymal stem cells for treatment and prevention of graft versus host disease. Eur. J. Immunol. 2008, 38:1745-1755.
79. Le Blanc K., Rasmusson I., Sundberg B., Götherström C., Hassan M., Uzunel M., Ringdén O. Treatment of severe graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet 2004, 363:1439-1441.
80. Dander E., Lucchini G., Vinci P., Introna M., Masciocchi F., Perseghin P., Balduzzi A., Bonanomi S. Mesenchymal stromal cells for the treatment of graft-versus-host disease: understanding the in vivo biological effect through patient immune monitoring. Leukemia 2012, 26:1682-1684.
81. Krampera M. Mesenchymal stromal cell 'licensing': a multistep process. Leukemia 2011, 25:1408-1414.
82. Zhou H., Guo M., Bian C., Sun Z., Yang Z., Zeng Y., Ai H., Zhao R.C. Efficacy of bone marrow-derived mesenchymal stem cells in the treatment of sclerodermatous chronic graft-versus-host disease: clinical report. Biol. Blood Marrow Transplant. 2010, 16:403-412.
83. + regulatory B cells producing interleukin 10. Leukemia 2014, 29:636-646.
84. Ringden O., Le Blanc K. Mesenchymal stem cells for treatment of acute and chronic graft-versus-host disease, tissue toxicity and hemorrhages. Best Pract. Res. Clin. Haematol. 2011, 24:65-72.
85. Yin F., Battiwalla M., Ito S., Feng X., Chinian F., Melenhorst J.J., Koklanaris E., Sabatino M. 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.