Apoptosis in mesenchymal stromal cells induces in vivo recipient-mediated immunomodulation

Science Translational Medicine

Volumn 9, Issue 416, 2017, Pages

  Galleu, Antonio ^a   Riffo Vasquez, Yanira ^b   Trento, Cristina ^a   Lomas, Cara ^c   Dolcetti, Luigi ^a   Cheung, Tik Shing ^a   Von Bonin, Malte ^d   Barbieri, Laura ^a   Halai, Krishma ^a   Ward, Sophie ^c   Weng, Ling ^a   Chakraverty, Ronjon ^c   Lombardi, Giovanna ^a   Watt, Fiona M ^b   Orchard, Kim ^e   Marks, David I ^f   Apperley, Jane ^g   Bornhauser, Martin ^a,d   Walczak, Henning ^c   Bennett, Clare ^c   Dazzi, Francesco ^a,g   more..

^a KING'S COLLEGE LONDON   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY HOSPITAL CARL GUSTAV CARUS   (Germany)

^e UNIVERSITY HOSPITAL SOUTHAMPTON NHS FOUNDATION TRUST   (United Kingdom)

^f BRISTOL HAEMATOLOGY AND ONCOLOGY CENTRE   (United Kingdom)

^g IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; CYTOKINE; INDOLEAMINE 2,3 DIOXYGENASE; PERFORIN; PROSTAGLANDIN SYNTHASE; TUMOR NECROSIS FACTOR ALPHA STIMULATED GENE 6 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ACTIVITY; CELL FATE; CELL KILLING; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; DISEASE MODEL; ENZYME SYNTHESIS; EX VIVO STUDY; GRAFT RECIPIENT; GRAFT VERSUS HOST REACTION; HUMAN; HUMAN CELL; IMMUNE DEFICIENCY; IMMUNOMODULATION; MALE; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; MOUSE; NONHUMAN; PATIENT SELECTION; PHAGOCYTOSIS; PREDICTION; PRIORITY JOURNAL; TREATMENT RESPONSE; ANIMAL; CYTOLOGY; GENETICS; IMMUNOSUPPRESSIVE TREATMENT; MESENCHYMAL STROMA CELL; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES;

ANIMALS; APOPTOSIS; GRAFT VS HOST DISEASE; HUMANS; IMMUNOMODULATION; IMMUNOSUPPRESSION; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS;

EID: 85034604342     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aam7828     Document Type: Article

References (57)

1. M. Krampera, S. Glennie, J. Dyson, D. Scott, R. Laylor, E. Simpson, F. Dazzi, Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide. Blood 101, 3722-3729 (2003).
2. R. Ciccocioppo, M. E. Bernardo, A. Sgarella, R. Maccario, M. A. Avanzini, C. Ubezio, A. Minelli, C. Alvisi, A. Vanoli, F. Calliada, P. Dionigi, C. Perotti, F. Locatelli, G. R. Corazza, Autologous bone marrow-derived mesenchymal stromal cells in the treatment of fistulising Crohn's disease. Gut 60, 788-798 (2011).
3. F. Dazzi, M. Krampera, Mesenchymal stem cells and autoimmune diseases. Best Pract. Res. Clin. Haematol. 24, 49-57 (2011).
4. F. von Dalowski, M. Kramer, M. Wermke, R. Wehner, C. Röllig, N. Alakel, F. Stölzel, S. Parmentier, K. Sockel, M. Krech, M. Schmitz, U. Platzbecker, J. Schetelig, M. Bornhäuser, M. von Bonin, Mesenchymal stromal cells for treatment of acute steroid-refractory graft versus host disease: Clinical responses and long-Term outcome. Stem Cells 34, 357-366 (2016).
5. J. Tan, W. Wu, X. Xu, L. Liao, F. Zheng, S. Messinger, X. Sun, J. Chen, S. Yang, J. Cai, X. Gao, A. Pileggi, C. Ricordi, Induction therapy with autologous mesenchymal stem cells in livingrelated kidney transplants: A randomized controlled trial. JAMA 307, 1169-1177 (2012).
6. S. Glennie, I. Soeiro, P. J.Dyson, E. W.-F. Lam, F. Dazzi, Bonemarrowmesenchymal stem cells induce division arrest anergy of activated T cells. Blood 105, 2821-2827 (2005).
7. R. Ramasamy, H. Fazekasova, E. W.-F. Lam, I. Soeiro, G. Lombardi, F. Dazzi, Mesenchymal stem cells inhibit dendritic cell differentiation and function by preventing entry into the cell cycle. Transplantation 83, 71-76 (2007).
8. R. Ramasamy, C. K. Tong, H. F. Seow, S. Vidyadaran, F. Dazzi, The immunosuppressive effects of human bone marrow-derived mesenchymal stem cells target T cell proliferation but not its effector function. Cell. Immunol. 251, 131-136 (2008).
9. R. Meisel, A. Zibert, M. Laryea, U. Göbel, W. Däubener, D. Dilloo, Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2, 3-dioxygenase- mediated tryptophan degradation. Blood 103, 4619-4621 (2004).
10. J. Su, X. Chen, Y. Huang, W. Li, J. Li, K. Cao, G. Cao, L. Zhang, F. Li, A. I. Roberts, H. Kang, P. Yu, G. Ren, W. Ji, Y. Wang, Y. Shi, Phylogenetic distinction of iNOS and IDO function in mesenchymal stem cell-mediated immunosuppression in mammalian species. Cell Death Differ. 21, 388-396 (2014).
11. M. Di Nicola, C. Carlo-Stella, M. Magni, M. Milanesi, P. D. Longoni, P. Matteucci, S. Grisanti, A. M. Gianni, Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 99, 3838-3843 (2002).
12. S. Aggarwal, M. F. Pittenger, Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 105, 1815-1822 (2005).
13. F. Morandi, L. Raffaghello, G. Bianchi, F. Meloni, A. Salis, E. Millo, S. Ferrone, V. Barnaba, V. Pistoia, Immunogenicity of human mesenchymal stem cells in HLA-class I-restricted T-cell responses against viral or tumor-Associated antigens. Stem Cells 26, 1275-1287 (2008).
14. + regulatory T cells. Stem Cells 26, 212-222 (2008).
15. H. Choi, R. H. Lee, N. Bazhanov, J. Y. Oh, D. J. Prockop, Anti-inflammatory protein TSG-6 secreted by activated MSCs attenuates zymosan-induced mouse peritonitis by decreasing TLR2/NF-kB signaling in resident macrophages. Blood 118, 330-338 (2011).
16. + regulatory T cells upon mesenchymal stem cell-lymphocyte interaction. Haematologica 92, 881-888 (2007).
17. High forkhead box P3+ regulatory T cells. Clin. Exp. Immunol. 156, 149-160 (2009).
18. S. M. Melief, E. Schrama, M. H. Brugman, M. M. Tiemessen, M. J. Hoogduijn, W. E. Fibbe, H. Roelofs, Multipotent stromal cells induce human regulatory T cells through a novel pathway involving skewing of monocytes toward anti-inflammatory macrophages. Stem Cells 31, 1980-1991 (2013).
19. K. Németh, A. Leelahavanichkul, P. S. T. Yuen, B. Mayer, A. Parmelee, K. Doi, P. G. Robey, K. Leelahavanichkul, B. H. Koller, J.M. Brown, X. Hu, I. Jelinek, R. A. Star, É. Mezey, Bone marrow stromal cells attenuate sepsis via prostaglandin E2-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nat. Med. 15, 42-49 (2009).
20. R. H. Lee, A. A. Pulin, M. J. Seo, D. J. Kota, J. Ylostalo, B. L. Larson, L. Semprun-Prieto, P. Delafontaine, D. J. Prockop, Intravenous hMSCs improve myocardial infarction in mice because cells embolized in lung are activated to secrete the anti-inflammatory protein TSG-6. Cell Stem Cell 5, 54-63 (2009).
21. I. B. Resnick, C. Barkats, M. Y. Shapira, P. Stepensky, A. I. Bloom, A. Shimoni, D. Mankuta, N. Varda-Bloom, L. Rheingold, M. Yeshurun, B. Bielorai, A. Toren, T. Zuckerman, A. Nagler, R. Or, Treatment of severe steroid resistant acute GVHD with mesenchymal stromal cells (MSC). Am. J. Blood Res. 3, 225-238 (2013).
22. T. Toubai, I. Tawara, Y. Sun, C. Liu, E. Nieves, R. Evers, T. Friedman, R. Korngold, P. Reddy, Induction of acute GVHD by sex-mismatched H-Y antigens in the absence of functional radiosensitive host hematopoietic-derived antigen-presenting cells. Blood 119, 3844-3853 (2012).
23. J. A. Ankrum, J. F. Ong, J. M. Karp, Mesenchymal stem cells: Immune evasive, not immune privileged. Nat. Biotechnol. 32, 252-260 (2014).
24. M. Krampera, L. Cosmi, R. Angeli, A. Pasini, F. Liotta, A. Andreini, V. Santarlasci, B. Mazzinghi, G. Pizzolo, F. Vinante, P. Romagnani, E. Maggi, S. Romagnani, F. Annunziato, Role for interferon-g in the immunomodulatory activity of human bone marrow mesenchymal stem cells. Stem Cells 24, 386-398 (2006).
25. G. Ren, L. Zhang, X. Zhao, G. Xu, Y. Zhang, A. I. Roberts, R. C. Zhao, Y. Shi, Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell 2, 141-150 (2008).
26. R. S. Waterman, S. L. Tomchuck, S. L. Henkle, A. M. Betancourt, A new mesenchymal stem cell (MSC) paradigm: Polarization into a pro-inflammatory MSC1 or an Immunosuppressive MSC2 phenotype. Plos One 5, e10088 (2010).
27. J. Fu, D. Wang, Y. Yu, J. Heinrichs, Y. Wu, S. Schutt, K. Kaosaard, C. Liu, K. Haarberg, D. Bastian, D. G. McDonald, C. Anasetti, X.-Z. Yu, T-bet is critical for the development of acute graft-versus-host disease through controlling T cell differentiation and function. J. Immunol. 194, 388-397 (2015).
28. M. von Bonin, A. Kiani, U. Platzbecker, J. Schetelig, K. Hölig, U. Oelschlägel, C. Thiede, G. Ehninger, M. Bornhäuser, Third-party mesenchymal stem cells as part of the management of graft-failure after haploidentical stem cell transplantation. Leuk. Res. 33, e215-e217 (2009).
29. F. Bertrand, S. Muller, K. H. Roh, C. Laurent, L. Dupre, S. Valitutti, An initial and rapid step of lytic granule secretion precedes microtubule organizing center polarization at the cytotoxic T lymphocyte/target cell synapse. Proc. Natl. Acad. Sci. U.S.A. 110, 6073-6078 (2013).
30. N. A. Hosken, M. J. Bevan, Defective presentation of endogenous antigen by a cell line expressing class I molecules. Science 248, 367-370 (1990).
31. B. B. Lozzio, C. B. Lozzio, Properties and usefulness of the original K-562 human myelogenous leukemia cell line. Leuk. Res. 3, 363-370 (1979).
32. Y. Riffo-Vasquez, A. R. M. Coates, C. P. Page, D. Spina, Mycobacterium tuberculosis chaperonin 60.1 inhibits leukocyte diapedesis in a murine model of allergic lung inflammation. Am. J. Respir. Cell Mol. Biol. 47, 245-252 (2012).
33. E. Hamelmann, A. Oshiba, J. Paluh, K. Bradley, J. Loader, T. A. Potter, G. L. Larsen, E. W. Gelfand, Requirement for CD8+ T cells in the development of airway hyperresponsiveness in a marine model of airway sensitization. J. Exp. Med. 183, 1719-1729 (1996).
34. M. Korsgren, C. G. A. Persson, F. Sundler, T. Bjerke, T. Hansson, B. J. Chambers, S. Hong, L. Van Kaer, H.-G. Ljunggren, O. Korsgren, Natural killer cells determine development of allergen-induced eosinophilic airway inflammation in mice. J. Exp. Med. 189, 553-562 (1999).
35. T. L. McGaha, Y. Chen, B. Ravishankar, N. van Rooijen, M. C. I. Karlsson, Marginal zone macrophages suppress innate and adaptive immunity to apoptotic cells in the spleen. Blood 117, 5403-5412 (2011).
36. C. P. Parungo, D. I. Soybel, Y. L. Colson, S.-W. Kim, S. Ohnishi, A. M. De Grand, R. G. Laurence, E. G. Soltesz, F. Y. Chen, L. H. Cohn, M. G. Bawendi, J. V. Frangioni, Lymphatic drainage of the peritoneal space: A pattern dependent on bowel lymphatics. Ann. Surg. Oncol. 14, 286-298 (2007).
37. M. Guilliams, I. De Kleer, S. Henri, S. Post, L. Vanhoutte, S. De Prijck, K. Deswarte, B. Malissen, H. Hammad, B. N. Lambrecht, Alveolar macrophages develop from fetal monocytes that differentiate into long-lived cells in the first week of life via GM-CSF. J. Exp. Med. 210, 1977-1992 (2013).
38. B. Ravishankar, H. Liu, R. Shinde, P. Chandler, B. Baban, M. Tanaka, D. H. Munn, A. L. Mellor, M. C. I. Karlsson, T. L. McGaha, Tolerance to apoptotic cells is regulated by indoleamine 2, 3-dioxygenase. Proc. Natl. Acad. Sci. U.S.A. 109, 3909-3914 (2012).
39. L. von Bahr, I. Batsis, G. Moll, M. Hägg, A. Szakos, B. Sundberg, M. Uzunel, O. Ringden, K. Le Blanc, Analysis of tissues following mesenchymal stromal cell therapy in humans indicates limited long-Term engraftment and no ectopic tissue formation. Stem Cells 30, 1575-1578 (2012).
40. N. Eliopoulos, J. Stagg, L. Lejeune, S. Pommey, J. Galipeau, Allogeneic marrow stromal cells are immune rejected by MHC class I-And class II-mismatched recipient mice. Blood 106, 4057-4065 (2005).
41. A. J. Nauta, G. Westerhuis, A. B. Kruisselbrink, E. G. A. Lurvink, R. Willemze, W. E. Fibbe, Donor-derived mesenchymal stem cells are immunogenic in an allogeneic host and stimulate donor graft rejection in a nonmyeloablative setting. Blood 108, 2114-2120 (2006).
42. G. M. Spaggiari, A. Capobianco, S. Becchetti, M. C. Mingari, L. Moretta, 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 107, 1484-1490 (2006).
43. G. Moll, I. Rasmusson-Duprez, L. von Bahr, A.-M. Connolly-Andersen, G. Elgue, L. Funke, O. A. Hamad, H. Lönnies, P. U. Magnusson, J. Sanchez, Y. Teramura, K. Nilsson-Ekdahl, O. Ringden, O. Korsgren, B. Nilsson, K. Le Blanc, Are therapeutic human mesenchymal stromal cells compatible with human blood?. Stem Cells 30, 1565-1574 (2012).
44. Y. Li, F. Lin, Mesenchymal stem cells are injured by complement after their contact with serum. Blood 120, 3436-3443 (2012).
45. K. Mizrahi, I. Yaniv, S. Ash, J. Stein, N. Askenasy, Apoptotic signaling through Fas and TNF receptors ameliorates GVHD in mobilized peripheral blood grafts. Bone Marrow Transplant. 49, 640-648 (2014).
46. A. E. Morelli, A. T. Larregina, Concise review: Mechanisms behind apoptotic cell-based therapies against transplant rejection and graft versus host disease. Stem Cells 34, 1142-1150 (2016).
47. M. Florek, E. I. Sega, D. B. Leveson-Gower, J. Baker, A. M. S. Müller, D. Schneidawind, E. Meyer, R. S. Negrin, Autologous apoptotic cells preceding transplantation enhance survival in lethal murine graft-versus-host models. Blood 124, 1832-1842 (2014).
48. J. Couturier, A. T. Hutchison, M. A. Medina, C. Gingaras, P. Urvil, X. Yu, C. Nguyen, P. Mahale, L. Lin, C. A. Kozinetz, J. E. Schmitz, J. T. Kimata, T. C. Savidge, D. E. Lewis, HIV replication in conjunction with granzyme B production by CCR5+ memory CD4 T cells: Implications for bystander cell and tissue pathologies. Virology 462-463, 175-188 (2014).
49. Y. Li, P. Kanellakis, H. Hosseini, A. Cao, V. Deswaerte, P. Tipping, B.-H. Toh, A. Bobik, T. Kyaw, A CD1d-dependent lipid antagonist to NKT cells ameliorates atherosclerosis in ApoE-/- mice by reducing lesion necrosis and inflammation. Cardiovasc. Res. 109, 305-317 (2016).
50. M. Duijvestein, M. E. Wildenberg, M. M. Welling, S. Hennink, I. Molendijk, V. L. van Zuylen, T. Bosse, A. C. W. Vos, E. S. M. de Jonge-Muller, H. Roelofs, L. van der Weerd, H. W. Verspaget, W. E. Fibbe, A. A. te Velde, G. R. van den Brink, D. W. Hommes, Pretreatment with interferon-g enhances the therapeutic activity of mesenchymal stromal cells in animal models of colitis, Stem Cells 29, 1549-1558 (2011).
51. D. Wallach, T.-B. Kang, S.-H. Yang, A. Kovalenko, The in vivo significance of necroptosis: Lessons from exploration of caspase-8 function. Cytokine Growth Factor Rev. 25, 157-165 (2014).
52. T. J. Bartosh, J. H. Ylostalo, N. Bazhanov, J. Kuhlman, D. J. Prockop, Dynamic compaction of human mesenchymal stem/precursor cells into spheres self-Activates caspasedependent IL1 signaling to enhance secretion of modulators of inflammation and immunity (PGE2, TSG6, and STC1). Stem Cells 31, 2443-2456 (2013).
53. D. Przepiorka, D. Weisdorf, P. Martin, H. G. Klingemann, P. Beatty, J. Hows, E. D. Thomas, 1994 Consensus Conference on acute GVHD grading. Bone Marrow Transplant. 15, 825-828 (1995).
54. A. H. Filipovich, D. Weisdorf, S. Pavletic, G. Socie, J. R. Wingard, S. J. Lee, P. Martin, J. Chien, D. Przepiorka, D. Couriel, E. W. Cowen, P. Dinndorf, A. Farrell, R. Hartzman, J. Henslee-Downey, D. Jacobsohn, G. McDonald, B. Mittleman, J. D. Rizzo, M. Robinson, M. Schubert, K. Schultz, H. Shulman, M. Turner, G. Vogelsang, M. E. D. Flowers, National Institutes of Health consensus development project on criteria for clinical trials in chronic graft-versus-host disease: I. Diagnosis and staging working group report. Biol. Blood Marrow Transplant. 11, 945-956 (2005).
55. A. Valujskikh, O. Lantz, S. Celli, P. Matzinger, P. S. Heeger, Cross-primed CD8+ T cells mediate graft rejection via a distinct effector pathway. Nat. Immunol. 3, 844-851 (2002).
56. J.-L. Chen, A. J. Morgan, G. Stewart-Jones, D. Shepherd, G. Bossi, L. Wooldridge, S. L. Hutchinson, A. K. Sewell, G. M. Griffiths, P. A. van der Merwe, E. Y. Jones, A. Galione, V. Cerundolo, Ca2+ release from the endoplasmic reticulum of NY-ESO-1-specific T cells is modulated by the affinity of TCR and by the use of the CD8 coreceptor. J. Immunol. 184, 1829-1839 (2010).
57. L. He, X. Wu, F. Meylan, D. P. Olson, J. Simone, D. Hewgill, R. Siegel, P. E. Lipsky, Monitoring caspase activity in living cells using fluorescent proteins and flow cytometry. Am. J. Pathol. 164, 1901-1913 (2004).