Mesenchymal stem cells: immune evasive, not immune privileged (original) (raw)

• Friedenstein, A.J., Piatetzky-Shapiro, I.I. & Petrakova, K.V. Osteogenesis in transplants of bone marrow cells. J. Embryol. Exp. Morphol. 16, 381–390 (1966).
  CAS PubMed Google Scholar
• Friedenstein, A., Gorskaja, J. & Kulagina, N. Fibroblast precursors in normal and irradiated mouse hematopoietic organs. Exp. Hematol. 4, 267–274 (1976).
  CAS PubMed Google Scholar
• Friedenstein, A.J., Chailakhyan, R.K. & Gerasimov, U.V. Bone marrow osteogenic stem cells: in vitro cultivation and transplantation in diffusion chambers. Cell Tissue Kinet. 20, 263–272 (1987).
  CAS PubMed Google Scholar
• Caplan, A.I. Mesenchymal stem cells. J. Orthop. Res. 9, 641–650 (1991).
  Article CAS PubMed Google Scholar
• James, A.W. et al. An abundant perivascular source of stem cells for bone tissue engineering. Stem Cells Transl. Med. 1, 673–684 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Crisan, M., Corselli, M., Chen, W.C.W. & Péault, B. Perivascular cells for regenerative medicine. J. Cell. Mol. Med. 16, 2851–2860 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Chan, C.K.F. et al. Clonal precursor of bone, cartilage, and hematopoietic niche stromal cells. Proc. Natl. Acad. Sci. USA 110, 12643–12648 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Park, D. et al. Endogenous bone marrow MSCs are dynamic, fate-restricted participants in bone maintenance and regeneration. Cell Stem Cell 10, 259–272 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Dominici, M. et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8, 315–317 (2006).
  Article CAS PubMed Google Scholar
• Copley, M.R., Beer, P.A. & Eaves, C.J. Hematopoietic stem cell heterogeneity takes center stage. Cell Stem Cell 10, 690–697 (2012).
  Article CAS PubMed Google Scholar
• Verovskaya, E. et al. Heterogeneity of young and aged murine hematopoietic stem cells revealed by quantitative clonal analysis using cellular barcoding. Blood 122, 523–532 (2013).
  Article CAS PubMed Google Scholar
• Bernardo, M.E. & Fibbe, W.E. Mesenchymal stromal cells: sensors and switchers of inflammation. Cell Stem Cell 13, 392–402 (2013).
  Article CAS PubMed Google Scholar
• Nauta, A.J. & Fibbe, W.E. Immunomodulatory properties of mesenchymal stromal cells. Blood 110, 3499–3506 (2007).
  Article CAS PubMed Google Scholar
• François, M., Romieu-Mourez, R., Li, M. & Galipeau, J. Human MSC suppression correlates with cytokine induction of indoleamine 2,3-dioxygenase and bystander M2 macrophage differentiation. Mol. Ther. 20, 187–195 (2012).
  Article PubMed CAS Google Scholar
• Prockop, D.J. Concise review: two negative feedback loops place mesenchymal stem/stromal cells at the center of early regulators of inflammation. Stem Cells 31, 2042–2046 (2013).
  Article CAS PubMed Google Scholar
• Bianco, P . et al. The meaning, the sense and the significance: translating the science of mesenchymal stem cells into medicine. Nat. Med. 19, 35–42 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Shen, H. Stricter standards sought to curb stem-cell confusion. Nature 499, 389 (2013).
  Article CAS PubMed Google Scholar
• Keating, A. Mesenchymal stromal cells: new directions. Cell Stem Cell 10, 709–716 (2012).
  Article CAS PubMed Google Scholar
• Caplan, A.I. & Correa, D. The MSC: an injury drugstore. Cell Stem Cell 9, 11–15 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Phinney, D.G. et al. MSCs: science and trials. Nat. Med. 19, 812 (2013).
  Article CAS PubMed Google Scholar
• Fibbe, W.E., Dazzi, F. & LeBlanc, K. MSCs: science and trials. Nat. Med. 19, 812–813 (2013).
  Article CAS PubMed Google Scholar
• Pittenger, M.F. MSCs: science and trials. Nat. Med. 19, 811 (2013).
  Article CAS PubMed Google Scholar
• Ankrum, J. & Karp, J. Mesenchymal stem cell therapy: two steps forward, one step back. Trends Mol. Med. 16, 203–209 (2010).
  Article PubMed PubMed Central Google Scholar
• Haynesworth, S.E., Baber, M.A. & Caplan, A.I. Cytokine expression by human marrow-derived mesenchymal progenitor cells in vitro: effects of dexamethasone and IL-1 alpha. J. Cell. Physiol. 166, 585–592 (1996).
  Article CAS PubMed Google Scholar
• Devine, S.M. & Hoffman, R. Role of mesenchymal stem cells in hematopoietic stem cell transplantation. Curr. Opin. Hematol. 7, 358–363 (2000).
  Article CAS PubMed Google Scholar
• Lazarus, H., Curtin, P., Devine, S., McCarthy, P. & Holland, K. Role of mesenchymal stem cells (MSC) in allogeneic transplantation: early phase I clinical results. Blood 96, 392a (2000).
  Google Scholar
• Klyushnenkova, E., Mosca, J.D., McIntosh, K.R. & Thiede, M.A. Human mesenchymal stem cells suppress allogeneic T cell responses in vitro: implications for allogeneic transplantation. Blood 92, 2652 (1998).
  Google Scholar
• Tse, W.T., Beyer, W., Pendleton, J.D. & D'Andrea, A. Bone marrow derived mesenchymal stem cells suppress T cell activation without inducing allogeneic anergy. Blood 96, 1034a (2000).
  Google Scholar
• Tse, W.T., Pendleton, J.D., Beyer, W.M., Egalka, M.C. & Guinan, E.C. Suppression of allogeneic T-cell proliferation by human marrow stromal cells: implications in transplantation. Transplantation 75, 389–397 (2003).
  Article CAS PubMed Google Scholar
• Klyushnenkova, E. et al. T cell responses to allogeneic human mesenchymal stem cells: immunogenicity, tolerance, and suppression. J. Biomed. Sci. 12, 47–57 (2005).
  Article CAS PubMed Google Scholar
• Bartholomew, A. et al. Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp. Hematol. 30, 42–48 (2002).
  Article PubMed Google Scholar
• Le Blanc, K., Tammik, L., Sundberg, B., Haynesworth, S.E. & Ringden, O. Mesenchymal stem cells inhibit and stimulate mixed lymphocyte cultures and mitogenic responses independently of the major histocompatibility complex. Scand. J. Immunol. 57, 11–20 (2003).
  Article CAS PubMed Google Scholar
• Di Nicola, M. et al. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 99, 3838–3843 (2002).
  Article CAS PubMed Google Scholar
• Krampera, M. et al. 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).
  Article CAS PubMed Google Scholar
• Liechty, K.W. et al. Human mesenchymal stem cells engraft and demonstrate site-specific differentiation after in utero transplantation in sheep. Nat. Med. 6, 1282–1286 (2000).
  Article CAS PubMed Google Scholar
• Ito, T. et al. Mesenchymal stem cell and islet co-transplantation promotes graft revascularization and function. Transplantation 89, 1438–1445 (2010).
  Article PubMed Google Scholar
• Casiraghi, F. et al. Pretransplant infusion of mesenchymal stem cells prolongs the survival of a semiallogeneic heart transplant through the generation of regulatory T cells. J. Immunol. 181, 3933–3946 (2008).
  Article CAS PubMed Google Scholar
• Waterman, R.S., Tomchuck, S.L., Henkle, S.L. & Betancourt, A.M. A new mesenchymal stem cell (MSC) paradigm: polarization into a pro-inflammatory MSC1 or an immunosuppressive MSC2 phenotype. PLoS ONE 5, e10088 (2010).
  Article PubMed CAS PubMed Central Google Scholar
• Ranganath, S.H., Levy, O., Inamdar, M.S. & Karp, J.M. Harnessing the mesenchymal stem cell secretome for the treatment of cardiovascular disease. Cell Stem Cells 10, 244–258 (2012).
  Article CAS Google Scholar
• Le Blanc, K., Tammik, C., Rosendahl, K., Zetterberg, E. & Ringdén, O. HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp. Hematol. 31, 890–896 (2003).
  Article CAS PubMed Google Scholar
• Hemeda, H. et al. Interferon-γ and tumor necrosis factor-α differentially affect cytokine expression and migration properties of mesenchymal stem cells. Stem Cells Dev. 19, 693–706 (2010).
  Article CAS PubMed Google Scholar
• Mastri, M. et al. Activation of Toll-like receptor 3 (TLR3) amplifies mesenchymal stem cell trophic factors and enhances therapeutic potency. Am. J. Physiol. Cell Physiol. 303, C1021–C1033 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Delarosa, O., Dalemans, W. & Lombardo, E. Toll-like receptors as modulators of mesenchymal stem cells. Front. Immunol. 3, 182 (2012).
  Article PubMed PubMed Central Google Scholar
• Shi, Y. et al. How mesenchymal stem cells interact with tissue immune responses. Trends Immunol. 33, 136–143 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Le Blanc, K. et al. Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet 363, 1439–1441 (2004).
  Article PubMed Google Scholar
• von Bahr, L. et al. Long-term complications, immunologic effects, and role of passage for outcome in mesenchymal stromal cell therapy. Biol. Blood Marrow Transplant. 18, 557–564 (2012).
  Article PubMed Google Scholar
• Lalu, M.M. et al. Safety of cell therapy with mesenchymal stromal cells (SafeCell): a systematic review and meta-analysis of clinical trials. PLoS ONE 7, e47559 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Penn, M.S. et al. Adventitial delivery of an allogeneic bone marrow-derived adherent stem cell in acute myocardial infarction: phase I clinical study. Circ. Res. 110, 304–311 (2012).
  Article CAS PubMed Google Scholar
• Yang, H. South Korea's stem cell approval. Nat. Biotechnol. 29, 857 (2011).
  Article CAS Google Scholar
• Cyranoski, D. Canada approves stem cell product. Nat. Biotechnol. 30, 571 (2012).
  Article CAS Google Scholar
• Kurtzberg, J. et al. Allogeneic human mesenchymal stem cell therapy (Remestemcel-L, Prochymal) as a rescue agent for severe refractory acute graft-versus-host disease in pediatric patients. Biol. Blood Marrow Transplant. 10.1016/j.bbmt.2013.11.001 (2013).
• Le Blanc, K. et al. Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet 371, 1579–1586 (2008).
  Article CAS PubMed Google Scholar
• Bernardo, M.E. et al. Co-infusion of _ex vivo_-expanded, parental MSCs prevents life-threatening acute GVHD, but does not reduce the risk of graft failure in pediatric patients undergoing allogeneic umbilical cord blood transplantation. Bone Marrow Transplant. 46, 200–207 (2011).
  Article CAS PubMed Google Scholar
• Ball, L.M. 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. 163, 501–509 (2013).
  Article CAS PubMed Google Scholar
• Riordan, N.H. et al. Non-expanded adipose stromal vascular fraction cell therapy for multiple sclerosis. J. Transl. Med. 7, 29 (2009).
  Article PubMed CAS PubMed Central Google Scholar
• Toma, C., Wagner, W.R., Bowry, S., Schwartz, A. & Villanueva, F. Fate of culture-expanded mesenchymal stem cells in the microvasculature: in vivo observations of cell kinetics. Circ. Res. 104, 398–402 (2009).
  Article CAS PubMed Google Scholar
• Lee, R.H. 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 5, 54–63 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Kidd, S. et al. Direct evidence of mesenchymal stem cell tropism for tumor and wounding microenvironments using in vivo bioluminescent imaging. Stem Cells 27, 2614–2623 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• von Bahr, L. et al. 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).
  Article CAS PubMed Google Scholar
• Muschler, G.F., Nakamoto, C. & Griffith, L.G. Engineering principles of clinical cell-based tissue engineering. J. Bone Joint Surg. Am. 86-A, 1541–1558 (2004).
  Article Google Scholar
• Eliopoulos, N., Stagg, J., Lejeune, L., Pommey, S. & Galipeau, J. Allogeneic marrow stromal cells are immune rejected by MHC class I- and class II-mismatched recipient mice. Blood 106, 4057–4065 (2005).
  Article CAS PubMed Google Scholar
• Campeau, P.M. et al. Mesenchymal stromal cells engineered to express erythropoietin induce anti-erythropoietin antibodies and anemia in allorecipients. Mol. Ther. 17, 369–372 (2009).
  Article CAS PubMed Google Scholar
• Zangi, L. et al. Direct imaging of immune rejection and memory induction by allogeneic mesenchymal stromal cells. Stem Cells 27, 2865–2874 (2009).
  Article CAS PubMed Google Scholar
• Nauta, A.J. et al. 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).
  Article CAS PubMed PubMed Central Google Scholar
• Badillo, A.T., Beggs, K.J., Javazon, E.H., Tebbets, J.C. & Flake, A.W. Murine bone marrow stromal progenitor cells elicit an in vivo cellular and humoral alloimmune response. Biol. Blood Marrow Transplant. 13, 412–422 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Griffin, M.D. et al. Anti-donor immune responses elicited by allogeneic mesenchymal stem cells: what have we learned so far? Immunol. Cell Biol. 91, 40–51 (2013).
  Article CAS PubMed Google Scholar
• Camp, D.M., Loeffler, D.A., Farrah, D.M., Borneman, J.N. & LeWitt, P.A. Cellular immune response to intrastriatally implanted allogeneic bone marrow stromal cells in a rat model of Parkinson's disease. J. Neuroinflammation 6, 17 (2009).
  Article PubMed CAS PubMed Central Google Scholar
• Schu, S. et al. Immunogenicity of allogeneic mesenchymal stem cells. J. Cell. Mol. Med. 16, 2094–2103 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Beggs, K.J. et al. Immunologic consequences of multiple, high-dose administration of allogeneic mesenchymal stem cells to baboons. Cell Transplant. 15, 711–721 (2006).
  Article PubMed Google Scholar
• Isakova, I.A., Dufour, J., Lanclos, C., Bruhn, J. & Phinney, D.G. Cell-dose-dependent increases in circulating levels of immune effector cells in rhesus macaques following intracranial injection of allogeneic MSCs. Exp. Hematol. 38, 957–967 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Poncelet, A.J., Vercruysse, J., Saliez, A. & Gianello, P. Although pig allogeneic mesenchymal stem cells are not immunogenic in vitro, intracardiac injection elicits an immune response in vivo. Transplantation 83, 783–790 (2007).
  Article PubMed Google Scholar
• Grinnemo, K.H. et al. Xenoreactivity and engraftment of human mesenchymal stem cells transplanted into infarcted rat myocardium. J. Thorac. Cardiovasc. Surg. 127, 1293–1300 (2004).
  Article CAS PubMed Google Scholar
• Xia, Z. et al. Macrophagic response to human mesenchymal stem cell and poly(epsilon-caprolactone) implantation in nonobese diabetic/severe combined immunodeficient mice. J. Biomed. Mater. Res. A 71, 538–548 (2004).
  Article PubMed CAS Google Scholar
• Moll, G. et al. Are therapeutic human mesenchymal stromal cells compatible with human blood? Stem Cells 30, 1565–1574 (2012).
  Article CAS PubMed Google Scholar
• Moll, G. et al. Mesenchymal stromal cells engage complement and complement receptor bearing innate effector cells to modulate immune responses. PLoS ONE 6, e21703 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Li, Y. & Lin, F. Mesenchymal stem cells are injured by complement after their contact with serum. Blood 120, 3436–3443 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Le Blanc, K. & Mougiakakos, D. Multipotent mesenchymal stromal cells and the innate immune system. Nat. Rev. Immunol. 12, 383–396 (2012).
  Article CAS PubMed Google Scholar
• Chan, J.L. et al. Antigen-presenting property of mesenchymal stem cells occurs during a narrow window at low levels of interferon-gamma. Blood 107, 4817–4824 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Stagg, J., Pommey, S., Eliopoulos, N. & Galipeau, J. Interferon-gamma-stimulated marrow stromal cells: a new type of nonhematopoietic antigen-presenting cell. Blood 107, 2570–2577 (2006).
  Article CAS PubMed Google Scholar
• François, M. et al. Mesenchymal stromal cells cross-present soluble exogenous antigens as part of their antigen-presenting cell properties. Blood 114, 2632–2638 (2009).
  Article PubMed Google Scholar
• Dembinski, J.L. et al. Tumor stroma engraftment of gene-modified mesenchymal stem cells as anti-tumor therapy against ovarian cancer. Cytotherapy 15, 20–32 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Ren, G. et al. Species variation in the mechanisms of mesenchymal stem cell-mediated immunosuppression. Stem Cells 27, 1954–1962 (2009).
  Article CAS PubMed Google Scholar
• Voll, R.E. et al. Immunosuppressive effects of apoptotic cells. Nature 390, 350–351 (1997).
  Article CAS PubMed Google Scholar
• Leonard, D.A., Cetrulo, C.L. Jr., McGrouther, D.A. & Sachs, D.H. Induction of tolerance of vascularized composite allografts. Transplantation 95, 403–409 (2013).
  Article CAS PubMed Google Scholar
• Zanotti, L. et al. Encapsulated mesenchymal stem cells for in vivo immunomodulation. Leukemia 27, 500–503 (2013).
  Article CAS PubMed Google Scholar
• Maccario, R. et al. Human mesenchymal stem cells and cyclosporin a exert a synergistic suppressive effect on in vitro activation of alloantigen-specific cytotoxic lymphocytes. Biol. Blood Marrow Transplant. 11, 1031–1032 (2005).
  Article PubMed Google Scholar
• Buron, F. et al. Human mesenchymal stem cells and immunosuppressive drug interactions in allogeneic responses: an in vitro study using human cells. Transplant. Proc. 41, 3347–3352 (2009).
  Article CAS PubMed Google Scholar
• Ge, W. et al. Infusion of mesenchymal stem cells and rapamycin synergize to attenuate alloimmune responses and promote cardiac allograft tolerance. Am. J. Transplant. 9, 1760–1772 (2009).
  Article CAS PubMed Google Scholar
• Luznik, L. et al. High-dose cyclophosphamide as single-agent, short-course prophylaxis of graft-versus-host disease. Blood 115, 3224–3230 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Huang, W.H., Yan, Y., De Boer, B., Bishop, G.A. & House, A.K. A short course of cyclosporine immunosuppression inhibits rejection but not tolerance of rat liver allografts. Transplantation 75, 368–374 (2003).
  Article CAS PubMed Google Scholar
• Huang, W.H. et al. A short course of mycophenolate immunosuppression inhibits rejection, but not tolerance, of rat liver allografts in association with inhibition of interleukin-4 and alloantibody responses. Transplantation 76, 1159–1165 (2003).
  Article CAS PubMed Google Scholar
• Forslöw, U. et al. Treatment with mesenchymal stromal cells is a risk factor for pneumonia-related death after allogeneic hematopoietic stem cell transplantation. Eur. J. Haematol. 89, 220–227 (2012).
  Article PubMed CAS Google Scholar
• de la Garza-Rodea, A.S. et al. Exploitation of herpesvirus immune evasion strategies to modify the immunogenicity of human mesenchymal stem cell transplants. PLoS ONE 6, e14493 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Soland, M.A. et al. Modulation of human mesenchymal stem cell immunogenicity through forced expression of human cytomegalovirus US proteins. PLoS ONE 7, e36163 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Levy, O. et al. mRNA-engineered mesenchymal stem cells for targeted delivery of interleukin-10 to sites of inflammation. Blood 122, e23–e32 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Ko, I.K., Kean, T.J. & Dennis, J.E. Targeting mesenchymal stem cells to activated endothelial cells. Biomaterials 30, 3702–3710 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Sarkar, D. et al. Chemical engineering of mesenchymal stem cells to induce a cell rolling response. Bioconjug. Chem. 19, 2105–2109 (2008).
  Article CAS PubMed Google Scholar
• Sarkar, D. et al. Engineered mesenchymal stem cells with self-assembled vesicles for systemic cell targeting. Biomaterials 31, 5266–5274 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Sarkar, D., Ankrum, J., Teo, G.S.L., Carman, C.V. & Karp, J.M. Cellular and extracellular programming of cell fate through engineered intracrine-, paracrine-, and endocrine-like mechanisms. Biomaterials 32, 3053–3061 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Ankrum, J. et al. Engineering cells with intracellular agent-loaded microparticles to control cell phenotype. Nat. Protoc. 9, 233–245 (2014).
  Article CAS PubMed PubMed Central Google Scholar
• Brandenberger, R. et al. Cell therapy bioprocessing. Bioprocess Int. 9, 30–37 (2011).
  Google Scholar
• Melief, S.M., Zwaginga, J.J., Fibbe, W.E. & Roelofs, H. Adipose tissue-derived multipotent stromal cells have a higher immunomodulatory capacity than their bone marrow-derived counterparts. Stem Cells Transl. Med 2, 455–463 (2013).
  Article PubMed PubMed Central Google Scholar
• Bravery, C.A. . et al. Potency assay development for cellular therapy products: an ISCT review of the requirements and experiences in the industry. Cytotherapy 15, 9–19 (2013).
  Article PubMed Google Scholar
• Hare, J.M. et al. Comparison of allogeneic vs autologous bone marrow–derived mesenchymal stem cells delivered by transendocardial injection in patients with ischemic cardiomyopathy: the POSEIDON randomized trial. J. Am. Med. Assoc. 308, 2369–2379 (2012).
  Article CAS Google Scholar
• Jung, Y., Bauer, G. & Nolta, J.A. Concise review: induced pluripotent stem cell-derived mesenchymal stem cells: progress toward safe clinical products. Stem Cells 30, 42–47 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Krampera, M. et al. Immunological characterization of multipotent mesenchymal stromal cells-The International Society for Cellular Therapy (ISCT) working proposal. Cytotherapy 15, 1054–1061 (2013).
  Article PubMed Google Scholar
• Zhukareva, V., Obrocka, M., Houle, J.D., Fischer, I. & Neuhuber, B. Secretion profile of human bone marrow stromal cells: donor variability and response to inflammatory stimuli. Cytokine 50, 317–321 (2010).
  Article CAS PubMed Google Scholar
• Strioga, M., Viswanathan, S., Darinskas, A., Slaby, O. & Michalek, J. Same or not the same? Comparison of adipose tissue-derived versus bone marrow-derived mesenchymal stem and stromal cells. Stem Cells Dev. 21, 2724–2752 (2012).
  Article CAS PubMed Google Scholar
• Zhao, W. et al. Cell-surface sensors for real-time probing of cellular environments. Nat. Nanotechnol. 6, 524–531 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Saxon, E. & Bertozzi, C.R. Cell surface engineering by a modified Staudinger reaction. Science 287, 2007–2010 (2000).
  Article CAS PubMed Google Scholar