Immunoregulatory properties of clinical grade mesenchymal stromal cells: Evidence, uncertainties, and clinical application

Stem Cell Research and Therapy

Volumn 4, Issue 3, 2013, Pages

  Ménard, Cédric ^a,b,c   Tarte, Karin ^a,b,c  

^a RENNES UNIVERSITY HOSPITAL   (France)

^b INSERM U917   (France)

^c UNIVERSITÉ DE RENNES 1   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIVE IMMUNITY; CELL TYPE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOASSAY; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; IMMUNOREGULATION; INNATE IMMUNITY; MESENCHYMAL STROMA CELL; PRIORITY JOURNAL; REGENERATIVE MEDICINE; REVIEW; CYTOLOGY; IMMUNE SYSTEM DISEASES; MESENCHYMAL STEM CELL TRANSPLANTATION; METABOLISM;

CHEMOKINE;

CHEMOKINES; HUMANS; IMMUNE SYSTEM DISEASES; IMMUNOMODULATION; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; REGENERATIVE MEDICINE;

EID: 84878779525     PISSN: None     EISSN: 17576512     Source Type: Journal    
DOI: 10.1186/scrt214     Document Type: Review

References (48)

1. Mesenchymal stem cells in health and disease. Uccelli A, Moretta L, Pistoia V, Nat Rev Immunol 2008 8 726 736 10.1038/nri2395 19172693
2. Induction therapy with autologous mesenchymal stem cells in living-related kidney transplants: a randomized controlled trial. Tan J, Wu W, Xu X, Liao L, Zheng F, Messinger S, Sun X, Chen J, Yang S, Cai J, Gao X, Pileggi A, Ricordi C, JAMA 2012 307 1169 1177 10.1001/jama.2012.316 22436957
3. Autologous mesenchymal stem cells for the treatment of secondary progressive multiple sclerosis: an open-label phase 2a proof-of-concept study. Connick P, Kolappan M, Crawley C, Webber DJ, Patani R, Michell AW, Du MQ, Luan SL, Altmann DR, Thompson AJ, Compston A, Scott MA, Miller DH, Chandran S, Lancet Neurol 2012 11 150 156 10.1016/S1474-4422(11)70305-2 22236384
4. Autologous bone marrow-derived mesenchymal stromal cells in the treatment of fistulising Crohn's disease. Ciccocioppo R, Bernardo ME, Sgarella A, Maccario R, Avanzini MA, Ubezio C, Minelli A, Alvisi C, Vanoli A, Calliada F, Dionigi P, Perotti C, Locatelli F, Corazza GR, Gut 2011 60 788 798 10.1136/gut.2010.214841 21257987
5. Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Le Blanc K, Frassoni F, Ball L, Locatelli F, Roelofs H, Lewis I, Lanino E, Sundberg B, Bernardo ME, Remberger M, Dini G, Egeler RM, Bacigalupo A, Fibbe W, Ringden O, Lancet 2008 371 1579 1586 10.1016/S0140-6736(08)60690-X 18468541 (Pubitemid 351626841)
6. Comparison of allogeneic vs autologous bone marrow-derived mesenchymal stem cells delivered by transendocardial injection in patients with ischemic cardiomyopathy: the POSEIDON randomized trial. Hare JM, Fishman JE, Gerstenblith G, Di Fede Velazquez DL, Zambrano JP, Suncion VY, Tracy M, Ghersin E, Johnston PV, Brinker JA, Breton E, Davis-Sproul J, Schulman IH, Byrnes J, Mendizabal AM, Lowery MH, Rouy D, Altman P, Wong Po Foo C, Ruiz P, Amador A, Da Silva J, McNiece IK, Heldman AW, JAMA 2012 308 2369 2379 23117550
7. Good manufacturing practices production of mesenchymal stem/stromal cells. Sensebe L, Bourin P, Tarte K, Hum Gene Ther 2011 22 19 26 10.1089/hum.2010.197 21028982
8. Differential expression of stem cell mobilization-associated molecules on multi-lineage cells from adipose tissue and bone marrow. De Ugarte DA, Alfonso Z, Zuk PA, Elbarbary A, Zhu M, Ashjian P, Benhaim P, Hedrick MH, Fraser JK, Immunol Lett 2003 89 267 270 10.1016/S0165-2478(03)00108-1 14556988 (Pubitemid 37222456)
9. Stromal stem cells from adipose tissue and bone marrow of age-matched female donors display distinct immunophenotypic profiles. Pachon-Pena G, Yu G, Tucker A, Wu X, Vendrell J, Bunnell BA, Gimble JM, J Cell Physiol 2011 226 843 851 10.1002/jcp.22408 20857424
10. Cell specific differences between human adipose-derived and mesenchymal-stromal cells despite similar differentiation potentials. Noel D, Caton D, Roche S, Bony C, Lehmann S, Casteilla L, Jorgensen C, Cousin B, Exp Cell Res 2008 314 1575 1584 10.1016/j.yexcr.2007.12.022 18325494
11. Immunological characterization of multipotent mesenchymal stromal cells. The International Society for Cellular Therapy (ISCT) working proposal. Krampera M, Galipeau J, Shi Y, Tarte K, Sensebe L, Cytotherapy 2013 10.1016/j.jcyt.2013. 02.010
12. Species variation in the mechanisms of mesenchymal stem cell-mediated immunosuppression. Ren G, Su J, Zhang L, Zhao X, Ling W, L'Huillie A, Zhang J, Lu Y, Roberts AI, Ji W, Zhang H, Rabson AB, Shi Y, Stem Cells 2009 27 1954 1962 10.1002/stem.118 19544427
13. Multipotent mesenchymal stromal cells and the innate immune system. Le Blanc K, Mougiakakos D, Nat Rev Immunol 2012 12 383 396 10.1038/nri3209 22531326
14. Mesenchymal stem cells inhibit natural killer-cell proliferation, cytotoxicity, and cytokine production: role of indoleamine 2,3-dioxygenase and prostaglandin E2. Spaggiari GM, Capobianco A, Abdelrazik H, Becchetti F, Mingari MC, Moretta L, Blood 2008 111 1327 1333 17951526 (Pubitemid 351213419)
15. Reciprocal interactions between human mesenchymal stem cells and gammadelta T cells or invariant natural killer T cells. Prigione I, Benvenuto F, Bocca P, Battistini L, Uccelli A, Pistoia V, Stem Cells 2009 27 693 702 10.1634/stemcells.2008-0687 19096038
16. Mesenchymal stem cells inhibit generation and function of both CD34+-derived and monocyte-derived dendritic cells. Nauta AJ, Kruisselbrink AB, Lurvink E, Willemze R, Fibbe WE, J Immunol 2006 177 2080 2087 16887966 (Pubitemid 44200965)
17. Mesenchymal stromal cells orchestrate follicular lymphoma cell niche through the CCL2-dependent recruitment and polarization of monocytes. Guilloton F, Caron G, Menard C, Pangault C, Ame-Thomas P, Dulong J, De Vos J, Rossille D, Henry C, Lamy T, Fouquet O, Fest T, Tarte K, Blood 2012 119 2556 2567 10.1182/blood-2011-08-370908 22289889
18. Human MSC suppression correlates with cytokine induction of indoleamine 2,3-dioxygenase and bystander M2 macrophage differentiation. Francois M, Romieu-Mourez R, Li M, Galipeau J, Mol Ther 2012 20 187 195 10.1038/mt.2011.189 21934657
19. Mesenchymal stem cell-educated macrophages: a novel type of alternatively activated macrophages. Kim J, Hematti P, Exp Hematol 2009 37 1445 1453 10.1016/j.exphem.2009.09.004 19772890
20. Mesenchymal stromal cell 'licensing': a multistep process. Krampera M, Leukemia 2011 25 1408 1414 10.1038/leu.2011.108 21617697
21. Human mesenchymal stem cells promote survival of T cells in a quiescent state. Benvenuto F, Ferrari S, Gerdoni E, Gualandi F, Frassoni F, Pistoia V, Mancardi G, Uccelli A, Stem Cells 2007 25 1753 1760 10.1634/stemcells.2007-0068 17395776 (Pubitemid 47121854)
22. Toll-like receptor-3-activated human mesenchymal stromal cells significantly prolong the survival and function of neutrophils. Cassatella MA, Mosna F, Micheletti A, Lisi V, Tamassia N, Cont C, Calzetti F, Pelletier M, Pizzolo G, Krampera M, Stem Cells 2011 29 1001 1011 10.1002/stem.651 21563279
23. Functional alteration of the lymphoma stromal cell niche by the cytokine context: role of indoleamine-2,3 dioxygenase. Maby-El Hajjami H, Ame-Thomas P, Pangault C, Tribut O, DeVos J, Jean R, Bescher N, Monvoisin C, Dulong J, Lamy T, Fest T, Tarte K, Cancer Res 2009 69 3228 3237 10.1158/0008-5472.CAN-08-3000 19276371
24. Immunomodulatory effect of mesenchymal stem cells on B cells. Franquesa M, Hoogduijn MJ, Bestard O, Grinyo JM, Front Immunol 2012 3 212 22833744
25. Mesenchymal stromal cells cross-present soluble exogenous antigens as part of their antigen-presenting cell properties. Francois M, Romieu-Mourez R, Stock-Martineau S, Boivin MN, Bramson JL, Galipeau J, Blood 2009 114 2632 2638 10.1182/blood-2009-02-207795 19654411
26. Human leukocyte antigen-G5 secretion by human mesenchymal stem cells is required to suppress T lymphocyte and natural killer function and to induce CD4+CD25highFOXP3+ regulatory T cells. Selmani Z, Naji A, Zidi I, Favier B, Gaiffe E, Obert L, Borg C, Saas P, Tiberghien P, Rouas-Freiss N, Carosella ED, Deschaseaux F, Stem Cells 2008 26 212 222 10.1634/stemcells.2007-0554 17932417
27. Anti-inflammatory protein TSG-6 secreted by activated MSCs attenuates zymosan-induced mouse peritonitis by decreasing TLR2/NF-kappaB signaling in resident macrophages. Choi H, Lee RH, Bazhanov N, Oh JY, Prockop DJ, Blood 2011 118 330 338 10.1182/blood-2010-12-327353 21551236
28. Intravenous hMSCs improve myocardial infarction in mice because cells embolized in lung are activated to secrete the anti-inflammatory protein TSG-6. Lee RH, Pulin AA, Seo MJ, Kota DJ, Ylostalo J, Larson BL, Semprun-Prieto L, Delafontaine P, Prockop DJ, Cell Stem Cell 2009 5 54 63 10.1016/j.stem.2009.05. 003 19570514
29. Anti-inflammatory protein TSG-6 reduces inflammatory damage to the cornea following chemical and mechanical injury. Oh JY, Roddy GW, Choi H, Lee RH, Ylostalo JH, Rosa RH Jr, Prockop DJ, articletProc Natl Acad Sci U S A 2010 107 16875 16880 10.1073/pnas.1012451107
30. Human multipotent stromal cells attenuate lipopolysaccharide-induced acute lung injury in mice via secretion of tumor necrosis factor-alpha-induced protein 6. Danchuk S, Ylostalo JH, Hossain F, Sorge R, Ramsey A, Bonvillain RW, Lasky JA, Bunnell BA, Welsh DA, Prockop DJ, Sullivan DE, Stem Cell Res Ther 2011 2 27 10.1186/scrt68 21569482
31. Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Ren G, Zhang L, Zhao X, Xu G, Zhang Y, Roberts AI, Zhao RC, Shi Y, Cell Stem Cell 2008 2 141 150 10.1016/j.stem.2007. 11.014 18371435 (Pubitemid 351181031)
32. Cytokine modulation of TLR expression and activation in mesenchymal stromal cells leads to a proinflammatory phenotype. Romieu-Mourez R, Francois M, Boivin MN, Bouchentouf M, Spaner DE, Galipeau J, J Immunol 2009 182 7963 7973 10.4049/jimmunol.0803864 19494321
33. Clinical-grade mesenchymal stromal cells produced under various GMP processes differ in their immunomodulatory properties: Standardization of immune quality controls. Menard C, Pacelli L, Bassi G, Dulong J, Bifari F, Bezier I, Zanoncello J, Ricciardi M, Latour M, Bourin P, Schrezenmeier H, Sensebe L, Tarte K, Krampera M, Stem Cells Dev 2013 in press
34. Secretion profile of human bone marrow stromal cells: donor variability and response to inflammatory stimuli. Zhukareva V, Obrocka M, Houle JD, Fischer I, Neuhuber B, Cytokine 2010 50 317 321 10.1016/j.cyto.2010.01.004 20185331
35. Limited acquisition of chromosomal aberrations in human adult mesenchymal stromal cells. Sensebe L, Tarte K, Galipeau J, Krampera M, Martin I, Phinney DG, Shi Y, Cell Stem Cell 2012 10 9 10 author reply 10-11 10.1016/j.stem.2011. 12.005 22226349
36. Twist-1 induces Ezh2 recruitment regulating histone methylation along the Ink4A/Arf locus in mesenchymal stem cells. Cakouros D, Isenmann S, Cooper L, Zannettino A, Anderson P, Glackin C, Gronthos S, Mol Cell Biol 2012 32 1433 1441 10.1128/MCB.06315-11 22290439
37. DNA methylation pattern changes upon long-term culture and aging of human mesenchymal stromal cells. Bork S, Pfister S, Witt H, Horn P, Korn B, Ho AD, Wagner W, Aging Cell 2010 9 54 63 10.1111/j.1474-9726.2009.00535.x 19895632
38. The senescence-associated secretory phenotype: the dark side of tumor suppression. Coppe JP, Desprez PY, Krtolica A, Campisi J, Annu Rev Pathol 2010 5 99 118 10.1146/annurev-pathol-121808-102144 20078217
39. Long-term complications, immunologic effects, and role of passage for outcome in mesenchymal stromal cell therapy. von Bahr L, Sundberg B, Lonnies L, Sander B, Karbach H, Hagglund H, Ljungman P, Gustafsson B, Karlsson H, Le Blanc K, Ringden O, Biol Blood Marrow Transplant 2012 18 557 564 10.1016/j.bbmt.2011. 07.023 21820393
40. 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? Galipeau J, Cytotherapy 2013 15 2 8 10.1016/j.jcyt.2012.10.002 23260081
41. Cryopreserved mesenchymal stromal cells display impaired immunosuppressive properties as a result of heat-shock response and impaired interferon-gamma licensing. Francois M, Copland IB, Yuan S, Romieu-Mourez R, Waller EK, Galipeau J, Cytotherapy 2012 14 147 152 10.3109/14653249.2011.623691 22029655
42. Lymphotoxin-beta receptor signaling through NF-kappaB2-RelB pathway reprograms adipocyte precursors as lymph node stromal cells. Benezech C, Mader E, Desanti G, Khan M, Nakamura K, White A, Ware CF, Anderson G, Caamano JH, Immunity 2012 37 721 734 10.1016/j.immuni.2012.06.010 22940098
43. In vivo imaging of Treg cells providing immune privilege to the haematopoietic stem-cell niche. Fujisaki J, Wu J, Carlson AL, Silberstein L, Putheti P, Larocca R, Gao W, Saito TI, Lo Celso C, Tsuyuzaki H, Sato T, Cote D, Sykes M, Strom TB, Scadden DT, Lin CP, Nature 2011 474 216 219 10.1038/nature10160 21654805
44. Bone marrow mesenchymal stem and progenitor cells induce monocyte emigration in response to circulating toll-like receptor ligands. Shi C, Jia T, Mendez-Ferrer S, Hohl TM, Serbina NV, Lipuma L, Leiner I, Li MO, Frenette PS, Pamer EG, Immunity 2011 34 590 601 10.1016/j.immuni.2011.02.016 21458307
45. Treatment with mesenchymal stromal cells is a risk factor for pneumonia-related death after allogeneic hematopoietic stem cell transplantation. Forslow U, Blennow O, LeBlanc K, Ringden O, Gustafsson B, Mattsson J, Remberger M, Eur J Haematol 2012 89 220 227 10.1111/j.1600-0609. 2012.01824.x 22765507
46. Human but not murine multipotent mesenchymal stromal cells exhibit broad-spectrum antimicrobial effector function mediated by indoleamine 2,3-dioxygenase. Meisel R, Brockers S, Heseler K, Degistirici O, Bulle H, Woite C, Stuhlsatz S, Schwippert W, Jager M, Sorg R, Henschler R, Seissler J, Dilloo D, Daubener W, Leukemia 2011 25 648 654 10.1038/leu.2010.310 21242993
47. Mesenchymal stromal cells for the treatment of graft-versus-host disease: understanding the in vivo biological effect through patient immune monitoring. Dander E, Lucchini G, Vinci P, Introna M, Masciocchi F, Perseghin P, Balduzzi A, Bonanomi S, Longoni D, Gaipa G, Belotti D, Parma M, Algarotti A, Capelli C, Golay J, Rovelli A, Rambaldi A, Biondi A, Biagi E, D'Amico G, Leukemia 2012 26 1681 1684 10.1038/leu.2011.384 22289986
48. Mesenchymal stromal cell infusions as rescue therapy for corticosteroid-refractory adult autoimmune enteropathy. Ciccocioppo R, Russo ML, Bernardo ME, Biagi F, Catenacci L, Avanzini MA, Alvisi C, Vanoli A, Manca R, Luinetti O, Locatelli F, Corazza GR, Mayo Clin Proc 2012 87 909 914 10.1016/j.mayocp.2012.04.014 22958995