Bone marrow-derived mesenchymal stromal cells harness purinergenic signaling to tolerize human th1 cells in vivo

Stem Cells

Volumn 33, Issue 4, 2015, Pages 1200-1212

  Amarnath, Shoba ^a   Foley, Jason E ^a   Farthing, Don E ^a   Gress, Ronald E ^a   Laurence, Arian ^b   Eckhaus, Michael A ^c   Métais, Jean Yves ^d   Rose, Jeremy J ^a   Hakim, Frances T ^a   Felizardo, Tania C ^a   Cheng, Austin V ^a   Robey, Pamela G ^e   Stroncek, David E ^f   Sabatino, Marianna ^f   Battiwalla, Minoo ^d   Ito, Sawa ^d   Fowler, Daniel H ^a   Barrett, Austin J ^d  

^a Cytokine Biology Section Experimental Transplantation and Immunology Branch National Cancer Institute   (United Kingdom)

^b NEWCASTLE UPON TYNE HOSPITALS NHS FOUNDATION TRUST   (United Kingdom)

^c Office of Research Services   (United States)

^d NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^e NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^f NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Adenosine; Mesenchymal stromal cells; T cells; x GVHD

Indexed keywords

4 [2 [7 AMINO 2 (2 FURYL) 1,2,4 TRIAZOLO[2,3 A][1,3,5]TRIAZIN 5 YLAMINO]ETHYL]PHENOL; 5' NUCLEOTIDASE; ADENOSINE; ADENOSINE A2 RECEPTOR ANTAGONIST;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; BONE MARROW DERIVED MESENCHYMAL STROMAL CELL; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; ENGRAFTMENT; EX VIVO STUDY; EXOSOME; FEMALE; GENETIC MARKER; GRAFT RECIPIENT; GRAFT VERSUS HOST REACTION; HUMAN; HUMAN CELL; IMMUNOMODULATION; IN VIVO STUDY; LUNG TRANSPLANTATION; LYMPHOCYTE FUNCTION; MESENCHYMAL STROMA CELL; MOUSE; NONHUMAN; PARACRINE SIGNALING; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; TH1 CELL; XENOGRAFT; ANIMAL; BONE MARROW; COCULTURE; DRUG EFFECTS; IMMUNOLOGY; NONOBESE DIABETIC MOUSE; SCID MOUSE; SIGNAL TRANSDUCTION;

ADENOSINE A2 RECEPTOR ANTAGONISTS; ANIMALS; BONE MARROW; COCULTURE TECHNIQUES; GRAFT VS HOST DISEASE; HUMANS; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED NOD; MICE, SCID; SIGNAL TRANSDUCTION; TH1 CELLS;

EID: 84925590260     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.1934     Document Type: Article

References (46)

1. Ciccocioppo R, Bernardo ME, Sgarella A, et al. Autologous bone marrow-derived mesenchymal stromal cells in the treatment of fistulising Crohn's disease. Gut 2011; 60: 788-798.
2. Ringden O, Uzunel M, Rasmusson I, et al. Mesenchymal stem cells for treatment of therapy-resistant graft-versus-host disease. Transplantation 2006; 81: 1390-1397.
3. Ball LM, Bernardo ME, Roelofs H, et al. Multiple infusions of mesenchymal stromal cells induce sustained remission in children with steroid-refractory, grade III-IV acute graft-versus-host disease. Br J Haematol 2013; 163: 501-509.
4. English K,. Mechanisms of mesenchymal stromal cell immunomodulation. Immunol Cell Biol 2013; 91: 19-26.
5. Kebriaei P, Robinson S,. Mesenchymal stem cell therapy in the treatment of acute and chronic graft versus host disease. Front Oncol 2011; 1: 16.
6. Baron F, Storb R,. Mesenchymal stromal cells: A new tool against graft-versus-host disease? Biol Blood Marrow Transplant 2012; 18: 822-840.
7. Amarnath S, Barrett AJ,. Mesenchymal stromal cells: Heroes or non-combatants? Cytotherapy 2013; 15: 253-254.
8. Batten P, Sarathchandra P, Antoniw JW, et al. Human mesenchymal stem cells induce T cell anergy and downregulate T cell allo-responses via the TH2 pathway: Relevance to tissue engineering human heart valves. Tissue Eng 2006; 12: 2263-2273.
9. Lee MJ, Kim J, Kim MY, et al. Proteomic analysis of tumor necrosis factor-alpha-induced secretome of human adipose tissue-derived mesenchymal stem cells. J Proteome Res 2010; 9: 1754-1762.
10. Ren G, Zhang L, Zhao X, et al. Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell 2008; 2: 141-150.
11. Meisel R, Zibert A, Laryea M, et al. Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenase-mediated tryptophan degradation. Blood 2004; 103: 4619-4621.
12. Bouffi C, Bony C, Courties G, et al. IL-6-dependent PGE2 secretion by mesenchymal stem cells inhibits local inflammation in experimental arthritis. PLoS One 2010; 5: e14247.
13. Akiyama K, Chen C, Wang D, et al. Mesenchymal-stem-cell-induced immunoregulation involves FAS-ligand-/FAS-mediated T cell apoptosis. Cell Stem Cell 2012; 10: 544-555.
14. Saldanha-Araujo F, Ferreira FI, Palma PV, et al. Mesenchymal stromal cells up-regulate CD39 and increase adenosine production to suppress activated T-lymphocytes. Stem Cell Res 2011; 7: 66-74.
15. Yin F, Battiwalla M, Ito S, et al. 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.
16. Amarnath S, Flomerfelt FA, Costanzo CM, et al. Rapamycin generates anti-apoptotic human Th1/Tc1 cells via autophagy for induction of xenogeneic GVHD. Autophagy 2010; 6: 523-541.
17. Amarnath S, Costanzo CM, Mariotti J, et al. Regulatory T cells and human myeloid dendritic cells promote tolerance via programmed death ligand-1. PLoS Biol 2010; 8: e1000302.
18. Abrahamsen TG, Carter CS, Read EJ, et al. Stimulatory effect of counterflow centrifugal elutriation in large-scale separation of peripheral blood monocytes can be reversed by storing the cells at 37 degrees C. J Clin Apher 1991; 6: 48-53.
19. Ren J, Jin P, Sabatino M, et al. Global transcriptome analysis of human bone marrow stromal cells (BMSC) reveals proliferative, mobile and interactive cells that produce abundant extracellular matrix proteins, some of which may affect BMSC potency. Cytotherapy 2011; 13: 661-674.
20. van Rijn RS, Simonetti ER, Hagenbeek A, et al. Quantitative assessment of human T lymphocytes in RAG2(-/-)gammac(-/-) mice: The impact of ex vivo manipulation on in vivo functionality. Exp Hematol 2007; 35: 117-127.
21. Hwang J, Kita R, Kwon HS, et al. Epidermal ablation of Dlx3 is linked to IL-17-associated skin inflammation. Proc Natl Acad Sci USA 2011; 108: 11566-11571.
22. Jenabian MA, Seddiki N, Yatim A, et al. Regulatory T cells negatively affect IL-2 production of effector T cells through CD39/adenosine pathway in HIV infection. PLoS Pathog 2013; 9: e1003319.
23. Farthing DE, Buxbaum NP, Bare CV, et al. Sensitive GC-MS/MS method to measure deuterium labeled deoxyadenosine in DNA from limited mouse cell populations. Anal Chem 2013; 85: 4613-4620.
24. Thery C, Amigorena S, Raposo G, et al. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol 2006;Chapter 3: Unit 3 22.
25. Malide D, Metais JY, Dunbar CE,. Dynamic clonal analysis of murine hematopoietic stem and progenitor cells marked by 5 fluorescent proteins using confocal and multiphoton microscopy. Blood 2012; 120: e105-116.
26. Maccario R, Podesta M, Moretta A, et al. 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/suppressive phenotype. Haematologica 2005; 90: 516-525.
27. Melief SM, Schrama E, Brugman MH, et al. Multipotent stromal cells induce human regulatory T cells through a novel pathway involving skewing of monocytes toward anti-inflammatory macrophages. Stem Cells 2013; 31: 1980-1991.
28. Moncrieffe H, Nistala K, Kamhieh Y, et al. High expression of the ectonucleotidase CD39 on T cells from the inflamed site identifies two distinct populations, one regulatory and one memory T cell population. J Immunol 2010; 185: 134-143.
29. Zhou Q, Yan J, Putheti P, et al. Isolated CD39 expression on CD4+ T cells denotes both regulatory and memory populations. Am J Transplant 2009; 9: 2303-2311.
30. Deaglio S, Dwyer KM, Gao W, et al. Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J Exp Med 2007; 204: 1257-1265.
31. Mandapathil M, Hilldorfer B, Szczepanski MJ, et al. Generation and accumulation of immunosuppressive adenosine by human CD4+CD25highFOXP3+ regulatory T cells. J Biol Chem 2010; 285: 7176-7186.
32. Regateiro FS, Cobbold SP, Waldmann H,. CD73 and adenosine generation in the creation of regulatory microenvironments. Clin Exp Immunol 2013; 171: 1-7.
33. Lee RH, Pulin AA, Seo MJ, et al. 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 2009; 5: 54-63.
34. Schrepfer S, Deuse T, Reichenspurner H, et al. Stem cell transplantation: The lung barrier. Transplant Proc 2007; 39: 573-576.
35. Bianco P, Cao X, Frenette PS, et al. The meaning, the sense and the significance: Translating the science of mesenchymal stem cells into medicine. Nat Med 2013; 19: 35-42.
36. Reis LA, Borges FT, Simoes MJ, et al. Bone marrow-derived mesenchymal stem cells repaired but did not prevent gentamicin-induced acute kidney injury through paracrine effects in rats. PLoS One 2012; 7: e44092.
37. Lai RC, Arslan F, Lee MM, et al. Exosome secreted by MSC reduces myocardial ischemia/reperfusion injury. Stem Cell Res 2010; 4: 214-222.
38. Ferrari D, Pizzirani C, Adinolfi E, et al. The P2X7 receptor: A key player in IL-1 processing and release. J Immunol 2006; 176: 3877-3883.
39. Sluyter R, Dalitz JG, Wiley JS,. P2X7 receptor polymorphism impairs extracellular adenosine 5'-triphosphate-induced interleukin-18 release from human monocytes. Genes Immun 2004; 5: 588-591.
40. Sevigny CP, Li L, Awad AS, et al. Activation of adenosine 2A receptors attenuates allograft rejection and alloantigen recognition. J Immunol 2007; 178: 4240-4249.
41. Okusa MD, Linden J, Macdonald T, et al. Selective A2A adenosine receptor activation reduces ischemia-reperfusion injury in rat kidney. Am J Physiol 1999; 277: F404-412.
42. Saze Z, Schuler PJ, Hong CS, et al. Adenosine production by human B cells and B cell-mediated suppression of activated T cells. Blood 2013; 122: 9-18.
43. Lai RC, Arslan F, Lee MM, et al. Exosome secreted by MSC reduces myocardial ischemia/reperfusion injury. Stem Cell Res 2010; 4: 214-222.
44. Alegre E, Rebmann V, Lemaoult J, et al. In vivo identification of an HLA-G complex as ubiquitinated protein circulating in exosomes. Eur J Immunol 2013; 43: 1933-1939.
45. Roccaro AM, Sacco A, Maiso P, et al. BM mesenchymal stromal cell-derived exosomes facilitate multiple myeloma progression. J Clin Invest 2013; 123: 1542-1555.
46. Kordelas L, Rebmann V, Ludwig AK, et al. MSC-derived exosomes: A novel tool to treat therapy-refractory graft-versus-host disease. Leukemia 2014; 28: 970-973.