Microenvironmental cues enhance mesenchymal stem cell-mediated immunomodulation and regulatory T-cell expansion

PLoS ONE

Volumn 13, Issue 3, 2018, Pages

  Kadle, Rohini L ^a   Abdou, Salma A ^a   Villarreal Ponce, Alvaro P ^a   Soares, Marc A ^a   Sultan, Darren L ^a   David, Joshua A ^a   Massie, Jonathan ^a   Rifkin, William J ^a   Rabbani, Piul ^a   Ceradini, Daniel J ^a  

^a NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INDOLEAMINE 2,3 DIOXYGENASE; TUMOR NECROSIS FACTOR; CYTOKINE;

ANIMAL CELL; ARTICLE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL EXPANSION; CELL HYPOXIA; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENDOTHELIUM CELL; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IMMUNOMODULATION; MALE; MESENCHYMAL STEM CELL; NONHUMAN; PHENOTYPE; RAT; REGULATORY T LYMPHOCYTE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ANIMAL; BONE MARROW CELL; CELL COMMUNICATION; CELL CULTURE; COCULTURE; DRUG EFFECT; IMMUNOLOGY; LEWIS RAT; MESENCHYMAL STROMA CELL; METABOLISM; TUMOR MICROENVIRONMENT;

ANIMALS; BONE MARROW CELLS; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL HYPOXIA; CELL PROLIFERATION; CELLS, CULTURED; CELLULAR MICROENVIRONMENT; COCULTURE TECHNIQUES; CYTOKINES; IMMUNOMODULATION; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; MALE; MESENCHYMAL STROMAL CELLS; RATS, INBRED LEW; T-LYMPHOCYTES, REGULATORY;

EID: 85043344685     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0193178     Document Type: Article

References (54)

1. Caplan A. Mesenchymal stem cells. J Orthop Res. 1991; 9: 641-650. https://doi.org/10.1002/jor. 1100090504 PMID: 1870029
2. Uccelli A, Moretta L, Pistoia V. Mesenchymal stem cells in health and disease. Nat Rev Immunol. 2008; 8: 726-736. https://doi.org/10.1038/nri2395 PMID: 19172693
3. 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: 141-150. https://doi.org/10.1016/j.stem.2007.11.014 PMID: 18371435
4. Xu G, Zhang L, Ren G, Yuan Z, Zhang Y, Zhao RC, et al. Immunosuppressive properties of cloned bone marrow mesenchymal stem cells. Cell Res. 2007; 17: 240-248. https://doi.org/10.1038/cr.2007.4 PMID: 17325691
5. Le Blanc K, Davies LC. Mesenchymal stromal cells and the innate immune response. Immunol Lett. European Federation of Immunological Societies; 2015; https://doi.org/10.1016/j.imlet.2015.05.004 PMID: 25982165
6. Jiang X, Zhang Y, Liu B, Zhang S, Wu Y, Yu X, et al. Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells. Blood. 2005; 105: 4120-4126. https://doi.org/10. 1182/blood-2004-02-0586 PMID: 15692068
7. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood. 2005; 105: 1815-1823. https://doi.org/10.1182/blood-2004-04-1559 PMID: 15494428
8. 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: 1484-1491. https://doi.org/10.1182/blood-2005-07-2775 PMID: 16239427
9. Spaggiari GM, Capobianco A, Abdelrazik H, Becchetti F, Mingari MC, Moretta L. Mesenchymal stem cells inhibit natural killer-cell proliferation, cytotoxicity, and cytokine production: role of indoleamine 2,3-dioxygenase and prostaglandin E2. Blood. 2008; 111: 1327-1334. https://doi.org/10.1182/blood-2007-02-074997 PMID: 17951526
10. 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: 1753-1760. https://doi.org/10.1634/stemcells.2007-0068 PMID: 17395776
11. Di Nicola M, Carlo-stella C, Magni M, Milanesi M, Longoni PD, Matteucci P, et al. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood. 2002; 99: 3838-3844. PMID: 11986244
12. Meisel R, Zibert A, Laryea M, Go U. Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2, 3-dioxygenase-mediated tryptophan degradation. Blood. 2004; 103: 4619-4622. https://doi.org/10.1182/blood-2003-11-3909 PMID: 15001472
13. Tse WT, Pendleton JD, Beyer WM, Egalka MC, Guinan EC. Suppression of allogeneic T-cell proliferation by human marrow stromal cells: implications in transplantation. Transplantation. 2003; 75: 389-397. https://doi.org/10.1097/01.TP.0000045055.63901.A9 PMID: 12589164
14. Di Ianni M, Del Papa B, De Ioanni M, Moretti L, Bonifacio E, Cecchini D, et al. Mesenchymal cells recruit and regulate T regulatory cells. Exp Hematol. 2008; 36: 309-318. https://doi.org/10.1016/j.exphem. 2007.11.007 PMID: 18279718
15. Del Fattore A, Luciano R, Pascucci L, Goffredo BM, Giorda E, Scapaticci M, et al. Immunoregulatory effects of Mesenchymal Stem Cell-derived Extracellular Vesicles on T lymphocytes. Cell Transplant. 2015; 1-42. https://doi.org/10.3727/096368915X687543 PMID: 25695896
16. Obermajer N, Popp FC, Soeder Y, Haarer J, Geissler EK, Schlitt HJ, et al. Conversion of Th17 into IL-17A(neg) regulatory T cells: a novel mechanism in prolonged allograft survival promoted by mesenchymal stem cell-supported minimized immunosuppressive therapy. J Immunol. 2014; 193: 4988-4999. https://doi.org/10.4049/jimmunol.1401776 PMID: 25305313
17. Ge W, Jiang J, Arp J, Liu W, Garcia B, Wang H. Regulatory T-cell generation and kidney allograft tolerance induced by mesenchymal stem cells associated with indoleamine 2,3-dioxygenase expression. Transplantation. 2010; 90: 1312-1320. https://doi.org/10.1097/TP.0b013e3181fed001 PMID: 21042238
18. Popp FC, Eggenhofer E, Renner P, Slowik P, Lang S a, Kaspar H, et al. Mesenchymal stem cells can induce long-term acceptance of solid organ allografts in synergy with low-dose mycophenolate. Transpl Immunol. Elsevier B.V.; 2008; 20: 55-60. https://doi.org/10.1016/j.trim.2008.08.004 PMID: 18762258
19. Solari MG, Srinivasan S, Boumaza I, Unadkat J, Harb G, Garcia-Ocana A, et al. Marginal mass islet transplantation with autologous mesenchymal stem cells promotes long-term islet allograft survival and sustained normoglycemia. J Autoimmun. Elsevier Ltd; 2009; 32: 116-124. https://doi.org/10.1016/j. jaut.2009.01.003 PMID: 19217258
20. Zhou HP, Yi DH, Yu SQ, Sun GC, Cui Q, Zhu HL, et al. Administration of donor-derived mesenchymal stem cells can prolong the survival of rat cardiac allograft. Transplant Proc. 2006; 38: 3046-3051. https://doi.org/10.1016/j.transproceed.2006.10.002 PMID: 17112896
21. 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. https://doi.org/10.1016/S0140-6736(04)16104-7 PMID: 15121408
22. Aksu AE, Horibe E, Sacks J, Ikeguchi R, Breitinger J, Scozio M, et al. Co-infusion of donor bone marrow with host mesenchymal stem cells treats GVHD and promotes vascularized skin allograft survival in rats. Clin Immunol. 2008; 127: 348-358. https://doi.org/10.1016/j.clim.2008.02.003 PMID: 18387852
23. Kuo Y-R, Goto S, Shih H-S, Wang F-S, Lin C-C, Wang C-T, et al. Mesenchymal stem cells prolong composite tissue allotransplant survival in a swine model. Transplantation. 2009; 87: 1769-1777. https://doi.org/10.1097/TP.0b013e3181a664f1 PMID: 19543052
24. Kuo Y-R, Chen C-C, Shih H-S, Goto S, Huang C-W, Wang C-T, et al. Prolongation of composite tissue allotransplant survival by treatment with bone marrow mesenchymal stem cells is correlated with T-cell regulation in a swine hind-limb model. Plast Reconstr Surg. 2011; 127: 569-579. https://doi.org/10. 1097/PRS.0b013e318200a92c PMID: 21285761
25. Kuo Y-R, Chen C-C, Goto S, Huang Y-T, Wang C-T, Tsai C-C, et al. Immunomodulatory effects of bone marrow-derived mesenchymal stem cells in a swine hemi-facial allotransplantation model. PLoS One. 2012; 7: 1-10. https://doi.org/10.1371/journal.pone.0035459 PMID: 22558153
26. 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: 228-235. https://doi.org/10. 1182/blood-2006-02-002246 PMID: 16985180
27. Lennon DP, Edmison JM, Caplan AI. Cultivation of Rat Marrow-Derived Mesenchymal Stem Cells in Reduced Oxygen Tension: Effects on In Vitro and In Vivo Osteochondrogenesis. J Cell Physiol. 2001; 187: 345-355. https://doi.org/10.1002/jcp.1081 PMID: 11319758
28. Harrison JS, Rameshwar P, Chang V, Bandari P. Oxygen saturation in the bone marrow of healthy volunteers. Blood. 2002; 99: 394. PMID: 11783438
29. Ceradini DJ, Kulkarni AR, Callaghan MJ, Tepper OM, Bastidas N, Kleinman ME, et al. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med. 2004; 10: 858-864. https://doi.org/10.1038/nm1075 PMID: 15235597
30. Spencer JA, Ferraro F, Roussakis E, Klein A, Runnels JM, Zaher W, et al. Direct measurement of local oxygen concentration in the bone marrow of live animals. Nature. 2014; 508: 269-273. https://doi.org/10.1038/nature13034 PMID: 24590072
31. Fehrer C, Brunauer R, Laschober G, Unterluggauer H, Reitinger S, Kloss F, et al. Reduced oxygen tension attenuates differentiation capacity of human mesenchymal stem cells and prolongs their lifespan. Aging Cell. 2007; 6: 745-757. https://doi.org/10.1111/j.1474-9726.2007.00336.x PMID: 17925003
32. Dos Santos F, Andrade PZ, Boura JS, Abecasis MM, da Silva CL, Cabral JMS. Ex vivo expansion of human mesenchymal stem cells: a more effective cell proliferation kinetics and metabolism under hypoxia. J Cell Physiol. 2010; 223: 27-35. https://doi.org/10.1002/jcp.21987 PMID: 20020504
33. Grayson WL, Zhao F, Bunnell B, Ma T. Hypoxia enhances proliferation and tissue formation of human mesenchymal stem cells. Biochem Biophys Res Commun. 2007; 358: 948-953. https://doi.org/10. 1016/j.bbrc.2007.05.054 PMID: 17521616
34. Hemeda H, Jakob M, Ludwig A-K, Giebel B, Lang S, Brandau S. Interferon-gamma and tumor necrosis factor-alpha differentially affect cytokine expression and migration properties of mesenchymal stem cells. Stem Cells Dev. 2010; 19: 693-706. https://doi.org/10.1089/scd.2009.0365 PMID: 20067407
35. 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: 386-398. https://doi.org/10.1634/stemcells.2005-0008 PMID: 16123384
36. Zhang L, Chan C. Isolation and enrichment of rat mesenchymal stem cells (MSCs) and separation of single-colony derived MSCs. J Vis Exp. 2010; 2-5. https://doi.org/10.3791/1852 PMID: 20308982
37. Chamberlain G, Fox J, Ashton B, Middleton J. Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells. 2007; 25: 2739-2749. https://doi.org/10.1634/stemcells.2007-0197 PMID: 17656645
38. Raemer PC, Haemmerling S, Giese T, Canaday DH, Katus H a, Dengler TJ, et al. Endothelial progenitor cells possess monocyte-like antigen-presenting and T-cell-co-stimulatory capacity. Transplantation. 2009; 87: 340-349. https://doi.org/10.1097/TP.0b013e3181957308 PMID: 19202438
39. Rasmusson I. Immune modulation by mesenchymal stem cells. Exp Cell Res. 2006; 312: 2169-2179. https://doi.org/10.1016/j.yexcr.2006.03.019 PMID: 16631737
40. Pricola K, Kuhn N, Haleen-Smith H, Song Y, Tuan R. Interleukin-6 maintains bone marrow-derived mesenchymal stem cell stemness by an ERK1/2-dependent mechanism. J Cell Biochem. 2009; 108: 577-588. https://doi.org/10.1002/jcb.22289 PMID: 19650110
41. Eom YW, Oh J, Lee JI, Baik SK, Rhee K, Shin HC, et al. The role of growth factors in maintenance of stemness in bone marrow-derived mesenchymal stem cells. Biochem Biophys Res Commun. 2014; 445: 16-22. https://doi.org/10.1016/j.bbrc.2014.01.084 PMID: 24491556
42. Zhou S, Lechpammer S, Greenberger JS, Glowacki J. Hypoxia inhibition of adipocytogenesis in human bone marrow stromal cells requires transforming growth factor-beta/Smad3 signaling. J Biol Chem. 2005; 280: 22688-22696. https://doi.org/10.1074/jbc.M412953200 PMID: 15845540
43. Potier E, Ferreira E, Andriamanalijaona R, Pujol J-P, Oudina K, Logeart-Avramoglou D, et al. Hypoxia affects mesenchymal stromal cell osteogenic differentiation and angiogenic factor expression. Bone. 2007; 40: 1078-1087. https://doi.org/10.1016/j.bone.2006.11.024 PMID: 17276151
44. Beane OS, Fonseca VC, Cooper LL, Koren G, Darling EM. Impact of aging on the regenerative properties of bone marrow-, muscle-, and adipose-derived mesenchymal stem/stromal cells. PLoS One. 2014; 9: 1-22. https://doi.org/10.1371/journal.pone.0115963 PMID: 25541697
45. Prado-Lòpez S, Duffy MM, Baustian C, Alagesan S, Hanley S a, Stocca A, et al. The influence of hypoxia on the differentiation capacities and immunosuppressive properties of clonal mouse mesenchymal stromal cell lines. Immunol Cell Biol. 2014; 1-12. https://doi.org/10.1038/icb.2014.30 PMID: 24777310
46. Zhuang J, Shan Z, Ma T, Li C, Qiu S, Zhou X, et al. CXCL9 and CXCL10 accelerate acute transplant rejection mediated by alloreactive memory T cells in a mouse retransplantation model. Exp Ther Med. 2014; 8: 237-242. https://doi.org/10.3892/etm.2014.1714 PMID: 24944628
47. Whiting D, Hsieh G, Yun JJ, Banerji a., Yao W, Fishbein MC, et al. Chemokine Monokine Induced by IFN-/CXC Chemokine Ligand 9 Stimulates T Lymphocyte Proliferation and Effector Cytokine Production. J Immunol. 2004; 172: 7417-7424. https://doi.org/10.4049/jimmunol.172.12.7417 PMID: 15187119
48. Paquet J, Deschepper M, Moya A, Legeart-Avramoglou D, Boisson-Vidal C, Petite H. Oxygen Tension Regulates Human Mesenchymal Stem Cell Paracrine Functions. Stem Cells Transl Med. 2015; 4: 1-13.
49. Maccario R, Piaggio G, Immunologia L. Interaction of human mesenchymal stem cells with cells involved in alloantigen-specific immune response favors the differentiation of CD4+ T-cell subsets expressing a regulatory/supressive phenotype. Hematologica. 2005; 90: 516-525.
50. Zhang B, Yin Y, Lai RC, Tan SS, Choo ABH, Lim SK. Mesenchymal stem cells secrete immunologically active exosomes. Stem Cells Dev. 2014; 23: 1233-1244. https://doi.org/10.1089/scd.2013.0479 PMID: 24367916
51. Doorn J, Moll G, Le Blanc K, van Blitterswijk C, de Boer J. Therapeutic applications of mesenchymal stromal cells: paracrine effects and potential improvements. Tissue Eng Part B Rev. 2012; 18: 101-115. https://doi.org/10.1089/ten.TEB.2011.0488 PMID: 21995703
52. Roemeling-van Rhijn M, Mensah FKF, Korevaar SS, Leijs MJ, van Osch GJVM, Ijzermans JNM, et al. Effects of Hypoxia on the Immunomodulatory Properties of Adipose Tissue-Derived Mesenchymal Stem cells. Front Immunol. 2013; 4: 1-8.
53. Plumas J, Chaperot L, Richard M-J, Molens J-P, Bensa J-C, Favrot M-C. Mesenchymal stem cells induce apoptosis of activated T cells. Leukemia. 2005; 19: 1597-1604. https://doi.org/10.1038/sj.leu. 2403871 PMID: 16049516
54. Ponte AL, Marais E, Gallay N, Langonne A, Delorme B, Herault O, et al. The in vitro migration capacity of human bone marrow mesenchymal stem cells: comparison of chemokine and growth factor chemotactic activities. Stem Cells. 2007; 25: 1737-1745. https://doi.org/10.1634/stemcells.2007-0054 PMID: 17395768