Toward development of imesenchymal stem cells for immunomodulatory therapy

Frontiers in Immunology

Volumn 6, Issue JAN, 2016, Pages

  De Witte, Samantha F H ^a   Franquesa, Marcella ^a   Baan, Carla C ^a   Hoogduijn, Martin J ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Cell therapy; Immunomodulation; Mesenchymal stem cell; Optimization; Secretome

Indexed keywords

5' NUCLEOTIDASE; ADAPALENE; GAMMA INTERFERON; INTERLEUKIN 17; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 6; SYNDECAN 2; THY 1 ANTIGEN; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA;

BIOREACTOR; CELL CULTURE; CELL ENGINEERING; CELL PROLIFERATION; CRYOPRESERVATION; HUMAN; HYPOXIA; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOGENICITY; IMMUNOMODULATION; IMMUNOPATHOLOGY; IMMUNOREGULATION; IMMUNOTHERAPY; MESENCHYMAL STEM CELL TRANSPLANTATION; NONHUMAN; PROTEIN EXPRESSION; REVIEW; TISSUE SCAFFOLD;

EID: 84958206619     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2015.00648     Document Type: Review

References (71)

1. Hoogduijn MJ. Are mesenchymal stromal cells immune cells? Arthritis Res Ther (2015) 17(1):88. doi:10.1186/s13075-015-0596-3
2. Soleymaninejadian E, Pramanik K, Samadian E. Immunomodulatory properties of mesenchymal stem cells: cytokines and factors. Am J Reprod Immunol (2012) 67(1):1-8. doi:10.1111/j.1600-0897.2011.01069.x
3. Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Oukka M, et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature (2006) 441(7090):235-8. doi:10.1038/nature04753
4. Hoogduijn MJ, Popp F, Verbeek R, Masoodi M, Nicolaou A, Baan C, et al. The immunomodulatory properties of mesenchymal stem cells and their use for immunotherapy. Int Immunopharmacol (2010) 10(12):1496-500. doi:10.1016/j.intimp.2010.06.019
5. Nemeth K, Leelahavanichkul A, Yuen PS, Mayer B, Parmelee A, Doi K, et al. 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(1):42-9. doi:10.1038/nm.1905
6. BouffiC, Bony C, Courties G, Jorgensen C, Noel D. IL-6-dependent PGE2 secretion by mesenchymal stem cells inhibits local inflammation in experimental arthritis. PLoS One (2010) 5(12):e14247. doi:10.1371/journal.pone.0014247
7. Augello A, Tasso R, Negrini SM, Amateis A, Indiveri F, Cancedda R, et al. Bone marrow mesenchymal progenitor cells inhibit lymphocyte proliferation by activation of the programmed death 1 pathway. Eur J Immunol (2005) 35(5):1482-90. doi:10.1002/eji.200425405
8. Franco G, Guarnotta C, Frossi B, Piccaluga PP, Boveri E, Gulino A, et al. Bone marrow stroma CD40 expression correlates with inflammatory mast cell infiltration and disease progression in splenic marginal zone lymphoma. Blood (2014) 123(12):1836-49. doi:10.1182/blood-2013-04-497271
9. Ren GW, Zhao X, Zhang LY, Zhang JM, L'Huillier A, Ling WF, et al. Inflammatory cytokine-induced intercellular adhesion molecule-1 and vascular cell adhesion molecule-1 in mesenchymal stem cells are critical for immunosuppression. J Immunol (2010) 184(5):2321-8. doi:10.4049/jimmunol.0902023
10. Meisel R, Zibert A, Laryea M, Gobel U, Daubener W, Dilloo D. Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenase-mediated tryptophan degradation. Blood (2004) 103(12):4619-21. doi:10.1182/blood-2003-11-3909
11. Regateiro FS, Cobbold SP, Waldmann H. CD73 and adenosine generation in the creation of regulatory microenvironments. Clin Exp Immunol (2013) 171(1):1-7. doi:10.1111/j.1365-2249.2012.04623.x
12. Ren G, Su J, Zhang L, Zhao X, Ling W, L'Huillie A, et al. Species variation in the mechanisms of mesenchymal stem cell-mediated immunosuppression. Stem Cells (2009) 27(8):1954-62. doi:10.1002/stem.118
13. Romieu-Mourez R, Coutu DL, Galipeau J. The immune plasticity of mesenchymal stromal cells from mice and men: concordances and discrepancies. Front Biosci (Elite Ed) (2012) 4:824-37. doi:10.2741/E422
14. Braun J, Kurtz A, Barutcu N, Bodo J, Thiel A, Dong J. Concerted regulation of CD34 and CD105 accompanies mesenchymal stromal cell derivation from human adventitial stromal cell. Stem Cells Dev (2013) 22(5):815-27. doi:10.1089/scd.2012.0263
15. Krampera M, Cosmi L, Angeli R, Pasini A, Liotta F, Andreini A, et al. Role for interferon-gamma in the immunomodulatory activity of human bone marrow mesenchymal stem cells. Stem Cells (2006) 24(2):386-98. doi:10.1634/stemcells.2005-0008
16. Benvenuto F, Ferrari S, Gerdoni E, Gualandi F, Frassoni F, Pistoia V, et al. Human mesenchymal stem cells promote survival of T cells in a quiescent state. Stem Cells (2007) 25(7):1753-60. doi:10.1634/stemcells.2007-0068
17. Franquesa M, Mensah FK, Huizinga R, Strini T, Boon L, Lombardo E, et al. Human adipose tissue-derived mesenchymal stem cells abrogate plasmablast formation and induce regulatory B cells independently of T helper cells. Stem Cells (2015) 33(3):880-91. doi:10.1002/stem.1881
18. Normanton M, Alvarenga H, Hamerschlak N, Ribeiro A, Kondo A, Rizzo LV, et al. Interleukin 7 plays a role in T lymphocyte apoptosis inhibition driven by mesenchymal stem cell without favoring proliferation and cytokines secretion. PLoS One (2014) 9(9):e106673. doi:10.1371/journal.pone.0106673
19. Roemeling-van Rhijn M, Reinders ME, Franquesa M, Engela AU, Korevaar SS, Roelofs H, et al. Human allogeneic bone marrow and adipose tissue derived mesenchymal stromal cells induce CD8+ cytotoxic T cell reactivity. J Stem Cell Res Ther (2013) 3(Suppl 6):004. doi:10.4172/2157-7633.S6-004
20. Cho PS, Messina DJ, Hirsh EL, Chi N, Goldman SN, Lo DP, et al. Immunogenicity of umbilical cord tissue derived cells. Blood (2008) 111(1):430-8. doi:10.1182/blood-2007-03-078774
21. Crop MJ, Korevaar SS, de Kuiper R, Ijzermans JN, van Besouw NM, Baan CC, et al. Human mesenchymal stem cells are susceptible to lysis by CD8+ T-cells and NK cells. Cell Transplant (2011) 20:1547-59. doi:10.3727/096368910X564076
22. Spaggiari GM, Capobianco A, Becchetti S, Mingari MC, 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(4):1484-90. doi:10.1182/blood-2005-07-2775
23. Eggenhofer E, Benseler V, Kroemer A, Popp FC, Geissler EK, Schlitt HJ, et al. Mesenchymal stem cells are short-lived and do not migrate beyond the lungs after intravenous infusion. Front Immunol (2012) 3:297. doi:10.3389/fimmu.2012.00297
24. Galipeau J, Krampera M. The challenge of defining mesenchymal stromal cell potency assays and their potential use as release criteria. Cytotherapy (2015) 17(2):125-7. doi:10.1016/j.jcyt.2014.12.008
25. Pollock K, Sumstad D, Kadidlo D, McKenna DH, Hubel A. Clinical mesenchymal stromal cell products undergo functional changes in response to freezing. Cytotherapy (2015) 17(1):38-45. doi:10.1016/j.jcyt.2014.06.008
26. Chinnadurai R, Garcia MA, Sakurai Y, Lam WA, Kirk AD, Galipeau J, et al. Actin cytoskeletal disruption following cryopreservation alters the biodistribution of human mesenchymal stromal cells in vivo. Stem Cell Reports (2014) 3(1):60-72. doi:10.1016/j.stemcr.2014.05.003
27. Moll G, Alm JJ, Davies LC, Von Bahr L, Heldring N, Stenbeck-Funke L, et al. Do cryopreserved mesenchymal stromal cells display impaired immunomodulatory and therapeutic properties? Stem Cells (2014) 32(9):2430-42. doi:10.1002/stem.1729
28. Sordi V, Malosio ML, Marchesi F, Mercalli A, Melzi R, Giordano T, et al. Bone marrow mesenchymal stem cells express a restricted set of functionally active chemokine receptors capable of promoting migration to pancreatic islets. Blood (2005) 106(2):419-27. doi:10.1182/blood-2004-09-3507
29. Fischer UM, Harting MT, Jimenez F, Monzon-Posadas WO, Xue HS, Savitz SI, et al. Pulmonary passage is a major obstacle for intravenous stem cell delivery: the pulmonary first-pass effect. Stem Cells Dev (2009) 18(5):683-91. doi:10.1089/scd.2008.0253
30. Gil-Ortega M, Garidou L, Barreau C, Maumus M, Breasson L, Tavernier G, et al. Native adipose stromal cells egress from adipose tissue in vivo: evidence during lymph node activation. Stem Cells (2013) 31(7):1309-20. doi:10.1002/stem.1375
31. Hoogduijn MJ, Roemeling-van Rhijn M, Engela AU, Korevaar SS, Mensah FK, Franquesa M, et al. Mesenchymal stem cells induce an inflammatory response after intravenous infusion. Stem Cells Dev (2013) 22(21):2825-35. doi:10.1089/scd.2013.0193
32. Lu W, Fu C, Song L, Yao Y, Zhang X, Chen Z, et al. Exposure to supernatants of macrophages that phagocytized dead mesenchymal stem cells improves hypoxic cardiomyocytes survival. Int J Cardiol (2013) 165(2):333-40. doi:10.1016/j.ijcard.2012.03.088
33. Lalu MM, McIntyre L, Pugliese C, Fergusson D, Winston BW, Marshall JC, et al. Safety of cell therapy with mesenchymal stromal cells (safecell): a systematic review and meta-analysis of clinical trials. PLoS One (2012) 7(10):e47559. doi:10.1371/journal.pone.0047559
34. English K, Barry FP, Field-Corbett CP, Mahon BP. IFN-gamma and TNF-alpha differentially regulate immunomodulation by murine mesenchymal stem cells. Immunol Lett (2007) 110(2):91-100. doi:10.1016/j.imlet.2007.04.001
35. Ryan JM, Barry F, Murphy JM, Mahon BP. Interferon-gamma does not break, but promotes the immunosuppressive capacity of adult human mesenchymal stem cells. Clin Exp Immunol (2007) 149(2):353-63. doi:10.1111/j.1365-2249.2007.03422.x
36. Harris SG, Padilla J, Koumas L, Ray D, Phipps RP. Prostaglandins as modulators of immunity. Trends Immunol (2002) 23(3):144-50. doi:10.1016/S1471-4906(01)02154-8
37. Sheng H, Wang Y, Jin Y, Zhang Q, Zhang Y, Wang L, et al. A critical role of IFNgamma in priming MSC-mediated suppression of T cell proliferation through up-regulation of B7-H1. Cell Res (2008) 18(8):846-57. doi:10.1038/cr.2008.80
38. Rafei M, Birman E, Forner K, Galipeau J. Allogeneic mesenchymal stem cells for treatment of experimental autoimmune encephalomyelitis. Mol Ther (2009) 17(10):1799-803. doi:10.1038/mt.2009.157
39. Ren G, Zhang L, Zhao X, Xu G, Zhang Y, Roberts AI, et al. Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell (2008) 2(2):141-50. doi:10.1016/j.stem.2007.11.014
40. Polchert D, Sobinsky J, Douglas G, Kidd M, Moadsiri A, Reina E, et al. IFN-gamma activation of mesenchymal stem cells for treatment and prevention of graft versus host disease. Eur J Immunol (2008) 38(6):1745-55. doi:10.1002/eji.200738129
41. Duijvestein M, Wildenberg ME, Welling MM, Hennink S, Molendijk I, van Zuylen VL, et al. Pretreatment with interferon-gamma enhances the therapeutic activity of mesenchymal stromal cells in animal models of colitis. Stem Cells (2011) 29(10):1549-58. doi:10.1002/stem.698
42. Prasanna SJ, Gopalakrishnan D, Shankar SR, Vasandan AB. Pro-inflammatory cytokines, IFNgamma and TNFalpha, influence immune properties of human bone marrow and Wharton jelly mesenchymal stem cells differentially. PLoS One (2010) 5(2):e9016. doi:10.1371/journal.pone.0009016
43. Sivanathan KN, Rojas-Canales DM, Hope CM, Krishnan R, Carroll RP, Gronthos S, et al. Interleukin-17A-induced human mesenchymal stem cells are superior modulators of immunological function. Stem Cells (2015) 33(9):2850-63. doi:10.1002/stem.2075
44. Roemeling-van Rhijn M, Mensah FK, Korevaar SS, Leijs MJ, van Osch GJ, Ijzermans JN, et al. Effects of hypoxia on the immunomodulatory properties of adipose tissue-derived mesenchymal stem cells. Front Immunol (2013) 4:203. doi:10.3389/fimmu.2013.00203
45. Crisostomo PR, Wang Y, Markel TA, Wang M, Lahm T, Meldrum DR. Human mesenchymal stem cells stimulated by TNF-alpha, LPS, or hypoxia produce growth factors by an NF kappa B-but not JNK-dependent mechanism. Am J Physiol Cell Physiol (2008) 294(3):C675-82. doi:10.1152/ajpcell.00437.2007
46. Sato K, Ozaki K, Oh I, Meguro A, Hatanaka K, Nagai T, et al. Nitric oxide plays a critical role in suppression of T-cell proliferation by mesenchymal stem cells. Blood (2007) 109(1):228-34. doi:10.1182/blood-2006-02-002246
47. Huang H, Kim HJ, Chang EJ, Lee ZH, Hwang SJ, Kim HM, et al. IL-17 stimulates the proliferation and differentiation of human mesenchymal stem cells: implications for bone remodeling. Cell Death Differ (2009) 16(10):1332-43. doi:10.1038/cdd.2009.74
48. Opitz CA, Litzenburger UM, Lutz C, Lanz TV, Tritschler I, Koppel A, et al. Toll-like receptor engagement enhances the immunosuppressive properties of human bone marrow-derived mesenchymal stem cells by inducing indoleamine-2,3-dioxygenase-1 via interferon-beta and protein kinase R. Stem Cells (2009) 27(4):909-19. doi:10.1002/stem.7
49. Waterman RS, Tomchuck SL, Henkle SL, Betancourt AM. A new mesenchymal stem cell (MSC) paradigm: polarization into a pro-inflammatory MSC1 or an immunosuppressive MSC2 phenotype. PLoS One (2010) 5(4):e10088. doi:10.1371/journal.pone.0010088
50. Kota DJ, DiCarlo B, Hetz RA, Smith P, Cox CS Jr, Olson SD. Differential MSC activation leads to distinct mononuclear leukocyte binding mechanisms. Sci Rep (2014) 4:4565. doi:10.1038/srep04565
51. Liotta F, Angeli R, Cosmi L, Fili L, Manuelli C, Frosali F, et al. Toll-like receptors 3 and 4 are expressed by human bone marrow-derived mesenchymal stem cells and can inhibit their T-cell modulatory activity by impairing notch signaling. Stem Cells (2008) 26(1):279-89. doi:10.1634/stemcells.2007-0454
52. Giuliani M, Bennaceur-Griscelli A, Nanbakhsh A, Oudrhiri N, Chouaib S, Azzarone B, et al. TLR ligands stimulation protects MSC from NK killing. Stem Cells (2014) 32(1):290-300. doi:10.1002/stem.1563
53. Goossens GH, Blaak EE. Adipose tissue oxygen tension: implications for chronic metabolic and inflammatory diseases. Curr Opin Clin Nutr Metab Care (2012) 15(6):539-46. doi:10.1097/MCO.0b013e328358fa87
54. Liu L, Gao J, Yuan Y, Chang Q, Liao Y, Lu F. Hypoxia preconditioned human adipose derived mesenchymal stem cells enhance angiogenic potential via secretion of increased VEGF and bFGF. Cell Biol Int (2013) 37(6):551-60. doi:10.1002/cbin.10097
55. Colegio OR, Chu NQ, Szabo AL, Chu T, Rhebergen AM, Jairam V, et al. Functional polarization of tumour-associated macrophages by tumour-derived lactic acid. Nature (2014) 513(7519):559-63. doi:10.1038/nature13490
56. Zhang ZY, Teoh SH, Chong WS, Foo TT, Chng YC, Choolani M, et al. A biaxial rotating bioreactor for the culture of fetal mesenchymal stem cells for bone tissue engineering. Biomaterials (2009) 30(14):2694-704. doi:10.1016/j.biomaterials.2009.01.028
57. Zhang ZY, Teoh SH, Teo EY, Khoon Chong MS, Shin CW, Tien FT, et al. A comparison of bioreactors for culture of fetal mesenchymal stem cells for bone tissue engineering. Biomaterials (2010) 31(33):8684-95. doi:10.1016/j.biomaterials.2010.07.097
58. Choi YK, Cho H, Seo YK, Yoon HH, Park JK. Stimulation of sub-sonic vibration promotes the differentiation of adipose tissue-derived mesenchymal stem cells into neural cells. Life Sci (2012) 91(9-10):329-37. doi:10.1016/j.lfs.2012.07.022
59. Yuan T, Li K, Guo L, Fan H, Zhang X. Modulation of immunological properties of allogeneic mesenchymal stem cells by collagen scaffolds in cartilage tissue engineering. J Biomed Mater Res A (2011) 98(3):332-41. doi:10.1002/jbm.a.33121
60. Ankrum JA, Miranda OR, Ng KS, Sarkar D, Xu C, Karp JM. Engineering cells with intracellular agent-loaded microparticles to control cell phenotype. Nat Protoc (2014) 9(2):233-45. doi:10.1038/nprot.2014.002
61. James S, Fox J, Afsari F, Lee J, Clough S, Knight C, et al. Multiparameter analysis of human bone marrow stromal cells identifies distinct immunomodulatory and differentiation-competent subtypes. Stem Cell Reports (2015) 4(6):1004-15. doi:10.1016/j.stemcr.2015.05.005
62. Kuci S, Kuci Z, Kreyenberg H, Deak E, Putsch K, Huenecke S, et al. CD271 antigen defines a subset of multipotent stromal cells with immunosuppressive and lymphohematopoietic engraftment-promoting properties. Haematologica (2010) 95(4):651-9. doi:10.3324/haematol.2009.015065
63. Bensidhoum M, Chapel A, Francois S, Demarquay C, Mazurier C, Fouillard L, et al. Homing of in vitro expanded Stro-1-or Stro-1+ human mesenchymal stem cells into the NOD/SCID mouse and their role in supporting human CD34 cell engraftment. Blood (2004) 103(9):3313-9. doi:10.1182/blood-2003-04-1121
64. Nasef A, Zhang YZ, Mazurier C, Bouchet S, Bensidhoum M, Francois S, et al. Selected Stro-1-enriched bone marrow stromal cells display a major suppressive effect on lymphocyte proliferation. Int J Lab Hematol (2009) 31(1):9-19. doi:10.1111/j.1751-553X.2007.00997.x
65. Campioni D, Rizzo R, Stignani M, Melchiorri L, Ferrari L, Moretti S, et al. A decreased positivity for CD90 on human mesenchymal stromal cells (MSCs) is associated with a loss of immunosuppressive activity by MSCs. Cytometry B Clin Cytom (2009) 76(3):225-30. doi:10.1002/cyto.b.20461
66. Beavis PA, Stagg J, Darcy PK, Smyth MJ. CD73: a potent suppressor of antitumor immune responses. Trends Immunol (2012) 33(5):231-7. doi:10.1016/j.it.2012.02.009
67. Poon IK, Lucas CD, Rossi AG, Ravichandran KS. Apoptotic cell clearance: basic biology and therapeutic potential. Nat Rev Immunol (2014) 14(3):166-80. doi:10.1038/nri3607
68. Saas P, Kaminski S, Perruche S. Prospects of apoptotic cell-based therapies for transplantation and inflammatory diseases. Immunotherapy (2013) 5(10):1055-73. doi:10.2217/imt.13.103
69. Luz-Crawford P, Kurte M, Bravo-Alegria J, Contreras R, Nova-Lamperti E, Tejedor G, et al. Mesenchymal stem cells generate a CD4+CD25+Foxp3+ regulatory T cell population during the differentiation process of Th1 and Th17 cells. Stem Cell Res Ther (2013) 4(3):65. doi:10.1186/scrt216
70. 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(2):e9252. doi:10.1371/journal.pone.0009252
71. Kim J, Hematti P. Mesenchymal stem cell-educated macrophages: a novel type of alternatively activated macrophages. Exp Hematol (2009) 37(12):1445-53. doi:10.1016/j.exphem.2009.09.004