Immunomodulatory properties of stem cells and bioactive molecules for tissue engineering

Journal of Controlled Release

Volumn 219, Issue , 2015, Pages 107-118

  Molina, Eric R ^a   Smith, Brandon T ^a   Shah, Sarita R ^a   Shin, Heungsoo ^a,b   Mikos, Antonios G ^a  

^a Rice University   (United States)

^b Hanyang University   (South Korea)

Author keywords

Bioactive molecules; Cell delivery; Immunomodulation; Mesenchymal stem cell; Regenerative medicine; Tissue engineering

Indexed keywords

CELL CULTURE; CELL ENGINEERING; CELLS; CYTOLOGY; IMMUNE SYSTEM; MOLECULES; SCAFFOLDS (BIOLOGY); STEM CELLS; TISSUE;

BIOACTIVE MOLECULES; CELL DELIVERY; IMMUNO MODULATIONS; MESENCHYMAL STEM CELL; REGENERATIVE MEDICINE;

TISSUE ENGINEERING;

GROWTH FACTOR; IMMUNOMODULATING AGENT; INTERLEUKIN 1; INTERLEUKIN 10; INTERLEUKIN 4; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

ADAPTIVE IMMUNITY; ARTICLE; B LYMPHOCYTE; DENDRITIC CELL; HUMAN; IMMUNE SYSTEM; IMMUNOMODULATION; INNATE IMMUNITY; MACROPHAGE; MESENCHYMAL STEM CELL; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; STEM CELL; T LYMPHOCYTE; TISSUE ENGINEERING; TISSUE REGENERATION; ANIMAL; DRUG DELIVERY SYSTEM; IMMUNOLOGY; MESENCHYMAL STROMA CELL;

ADAPTIVE IMMUNITY; ANIMALS; DRUG DELIVERY SYSTEMS; HUMANS; IMMUNITY, INNATE; IMMUNOMODULATION; MESENCHYMAL STROMAL CELLS; TISSUE ENGINEERING;

EID: 84947488952     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2015.08.038     Document Type: Article

References (149)

1. M. Dominici, K. Le Blanc, I. Mueller, I. Slaper-Cortenbach, F. Marini, D. Krause, and et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement Cytotherapy 8 2006 315 317
2. R. Hass, C. Kasper, S. Böhm, and R. Jacobs Different populations and sources of human mesenchymal stem cells (MSC): a comparison of adult and neonatal tissue-derived MSC Cell Commun. Signal. 9 2011
3. K. Le Blanc, C. Tammik, K. Rosendahl, E. Zetterberg, and O. Ringdén HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells Exp. Hematol. 31 2003 890 896
4. W. Li, G. Ren, Y. Huang, J. Su, Y. Han, J. Li, and et al. Mesenchymal stem cells: a double-edged sword in regulating immune responses Cell Death Differ. 19 2012 1505 1513
5. Y. Wang, X. Chen, W. Cao, and Y. Shi Plasticity of mesenchymal stem cells in immunomodulation: pathological and therapeutic implications Nat. Immunol. 15 2014 1009 1016
6. H.S. Hong, Y.H. Kim, and Y. Son Perspectives on mesenchymal stem cells: tissue repair, immune modulation, and tumor homing Arch. Pharm. Res. 35 2012 201 211
7. S. Nucera, D. Biziato, and M. de Palma The interplay between macrophages and angiogenesis in development, tissue injury and regeneration Int. J. Dev. Biol. 55 2011 495 503
8. C. Muscari, F. Bonafè, S. Martin-Suarez, S. Valgimigli, S. Valente, E. Fiumana, and et al. Restored perfusion and reduced inflammation in the infarcted heart after grafting stem cells with a hyaluronan-based scaffold J. Cell. Mol. Med. 17 2013 518 530
9. A.M. DiMarino, A.I. Caplan, and T.L. Bonfield Mesenchymal stem cells in tissue repair Front. Immunol. 4 2013
10. K.L. Spiller, S. Nassiri, C.E. Witherel, R.R. Anfang, J. Ng, K.R. Nakazawa, and et al. Sequential delivery of immunomodulatory cytokines to facilitate the M1-to-M2 transition of macrophages and enhance vascularization of bone scaffolds Biomaterials 37 2015 194 207
11. H. Nakajima, K. Uchida, A.R. Guerrero, S. Watanabe, D. Sugita, N. Takeura, and et al. Transplantation of mesenchymal stem cells promotes an alternative pathway of macrophage activation and functional recovery after spinal cord injury J. Neurotrauma 29 2012 1614 1625
12. J. Barminko, J.H. Kim, S. Otsuka, A. Gray, R. Schloss, M. Grumet, and et al. Encapsulated mesenchymal stromal cells for in vivo transplantation Biotechnol. Bioeng. 108 2011 2747 2758
13. V. Dayan, G. Yannarelli, F. Billia, P. Filomeno, X.H. Wang, J.E. Davies, and et al. Mesenchymal stromal cells mediate a switch to alternatively activated monocytes/macrophages after acute myocardial infarction Basic Res. Cardiol. 106 2011 1299 1310
14. R.H. Lee, A.A. Pulin, M.J. Seo, D.J. Kota, J. Ylostalo, B.L. Larson, and 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 2009 54 63
15. A. Wragg, J.A. Mellad, L.E. Beltran, M. Konoplyannikov, H. San, S. Boozer, and et al. VEGFR1/CXCR4-positive progenitor cells modulate local inflammation and augment tissue perfusion by a SDF-1-dependent mechanism J. Mol. Med. 86 2008 1221 1232
16. J. Sun, S.-H. Li, S.-M. Liu, J. Wu, R.D. Weisel, Y.-F. Zhuo, and et al. Improvement in cardiac function after bone marrow cell thearpy is associated with an increase in myocardial inflammation Am. J. Physiol. Heart Circ. Physiol. 296 2009 H43 H50
17. M.J. Robertson, and J. Ritz Biology and clinical relevance of human natural killer cells J. Am. Soc. Hematol. 76 1990 2421 2438
18. G.M. Spaggiari, A. Capobianco, S. Becchetti, M.C. Mingari, and 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 2006 1484 1490
19. G.M. Spaggiari, A. Capobianco, H. Abdelrazik, F. Becchetti, M.C. Mingari, and L. Moretta Mesenchymal stem cells inhibit natural killer cell proliferation, cytotoxicity, and cytokine production: role of indoleamine 2, 3-dioxygenase and prostaglandin E2 Blood 111 2008 1327 1333
20. P. Batten, P. Sarathchandra, J.W. Antoniw, S.S. Tay, M.W. Lowdell, P.M. Taylor, and 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. 12 2006 2263 2273
21. R.S. Waterman, S.L. Tomchuck, S.L. Henkle, and A.M. Betancourt A new mesenchymal stem cell (MSC) paradigm: polarization into a pro-inflammatory MSC1 or an immunosuppressive MSC2 phenotype PLoS One 5 2010 e10088
22. M.D. Swartzlander, A.K. Blakney, L.D. Amer, K.D. Hankenson, T.R. Kyriakides, and S.J. Bryant Immunomodulation by mesenchymal stem cells combats the foreign body response to cell-laden synthetic hydrogels Biomaterials 41 2015 79 88
23. M. Rossi, and J.W. Young Human dendritic cells: potent antigen-presenting cells at the crossroads of innate and adaptive immunity J. Immunol. 175 2005 1373 1381
24. G.M. Spaggiari, H. Abdelrazik, F. Becchetti, and L. Moretta MSCs inhibit monocyte-derived DC maturation and function by selectively interfering with the generation of immature DCs: central role of MSC-derived prostaglandin E2 Blood 113 2009 6576 6583
25. G. Ren, L. Zhang, X. Zhao, G. Xu, Y. Zhang, A.I. Roberts, and et al. Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide Cell Stem Cell 2 2008 141 150
26. Y.-P. Li, S. Paczesny, E. Lauret, S. Poirault, P. Bordigoni, F. Mekhloufi, and et al. Human mesenchymal stem cells license adult CD34 + hemopoietic progenitor cells to differentiate into regulatory dendritic cells through activation of the Notch pathway J. Immunol. 180 2008 1598 1608
27. A.J. Nauta, A.B. Kruisselbrink, E. Lurvink, R. Willemze, and W.E. Fibbe Mesenchymal stem cells inhibit generation and function of both CD34 +-derived and monocyte-derived dendritic cells J. Immunol. 177 2006 2080 2087
28. F. Djouad, L.-M. Charbonnier, C. Bouffi, P. Louis-Plence, C. Bony, F. Apparailly, and et al. Mesenchymal stem cells inhibit the differentiation of dendritic cells through an interleukin-6-dependent mechanism Stem Cells 25 2007 2025 2032
29. C. Menetrier-Caux, G. Montmain, M.C. Dieu, C. Bain, M.C. Favrot, C. Caux, and et al. Inhibition of the differentiation of dendritic cells from CD34(+) progenitors by tumor cells: role of interleukin-6 and macrophage colony-stimulating factor Blood 92 1998 4778 4791
30. P. Chomarat, J. Banchereau, J. Davoust, and a K. Palucka IL-6 switches the differentiation of monocytes from dendritic cells to macrophages. Nat. Immunol. 1 2000 510 514
31. K. Guo, S. Ikehara, and X. Meng Mesenchymal stem cells for inducing tolerance in organ transplantation Front. Cell Dev. Biol. 2 2014 8
32. K.L. Pothoven, T. Kheradmand, Q. Yang, J.L. Houlihan, H. Zhang, M. Degutes, and et al. Rapamycin-conditioned donor dendritic cells differentiate CD4CD25Foxp3 T cells in vitro with TGF-beta1 for islet transplantation Am. J. Transplant. 10 2010 1774 1784
33. B.N. Brown, B.D. Ratner, S.B. Goodman, S. Amar, and S.F. Badylak Macrophage polarization: an opportunity for improved outcomes in biomaterials and regenerative medicine Biomaterials 33 2012 3792 3802
34. A. Mantovani, A. Sica, and M. Locati Macrophage polarization comes of age Immunity 23 2005 344 346
35. J.M. Anderson, A. Rodriguez, and D.T. Chang Foreign body reaction to biomaterials Semin. Immunol. 20 2008 86 100
36. S. Hanson, R.N. D'Souza, and P. Hematti Biomaterial-mesenchymal stem cell constructs for immunomodulation in composite tissue engineering Tissue Eng. A 20 2014 2162 2168
37. A.K. Refai, M. Textor, D.M. Brunette, and J.D. Waterfield Effect of titanium surface topography on macrophage activation and secretion of proinflammatory cytokines and chemokines J. Biomed. Mater. Res. A 70 2004 194 205
38. G. Vallés, F. Bensiamar, L. Crespo, M. Arruebo, N. Vilaboa, and L. Saldaña Topographical cues regulate the crosstalk between MSCs and macrophages Biomaterials 37 2015 124 133
39. E.M. Pålsson-McDermott, and L. a J. O'Neill Signal transduction by the lipopolysaccharide receptor, Toll-like receptor-4 Immunology 113 2004 153 162
40. N. Mokarram, and R.V. Bellamkonda A perspective on immunomodulation and tissue repair Ann. Biomed. Eng. 42 2013 338 351
41. B.N. Brown, R. Londono, S. Tottey, L. Zhang, K.a. Kukla, M.T. Wolf, and et al. Macrophage phenotype as a predictor of constructive remodeling following the implantation of biologically derived surgical mesh materials Acta Biomater. 8 2012 978 987
42. S.E. Hanson, S.N. King, J. Kim, X. Chen, S.L. Thibeault, and P. Hematti The effect of mesenchymal stromal cell-hyaluronic acid hydrogel constructs on immunophenotype of macrophages Tissue Eng. A 17 2011 2463 2471
43. D.A. Cantu, P. Hematti, and W.J. Kao Cell encapsulating biomaterial regulates mesenchymal stromal/stem cell differentiation and macrophage immunophenotype Stem Cells Transl. Med. 1 2012 740 749
44. T.J. Bartosh, J.H. Ylöstalo, A. Mohammadipoor, N. Bazhanov, K. Coble, K. Claypool, and et al. Aggregation of human mesenchymal stromal cells (MSCs) into 3D spheroids enhances their antiinflammatory properties Proc. Natl. Acad. Sci. U. S. A. 107 2010 13724 13729
45. A. Bakshi, C. Hunter, S. Swanger, A. Lepore, and I. Fischer Minimally invasive delivery of stem cells for spinal cord injury: advantages of the lumbar puncture technique J. Neurosurg. Spine 1 2004 330 337
46. Q.Z. Zhang, W.R. Su, S.H. Shi, P. Wilder-Smith, A.P. Xiang, A. Wong, and et al. Human gingiva-derived mesenchymal stem cells elicit polarization of M2 macrophages and enhance cutaneous wound healing Stem Cells 28 2010 1856 1868
47. J.A. Horton, K.E. Hudak, E.J. Chung, A.O. White, B.T. Scroggins, J.F. Burkeen, and et al. Mesenchymal stem cells inhibit cutaneous radiation-induced fibrosis by suppressing chronic inflammation Stem Cells 31 2013 2231 2241
48. M.M. Duffy, T. Ritter, R. Ceredig, and M.D. Griffin Mesenchymal stem cell effects on T-cell effector pathways Stem Cell Res. Ther. 2 2011 34
49. M.E. Castro-Manrreza, and J.J. Montesinos Immunoregulation by mesenchymal stem cells: biological aspects and clinical applications J. Immunol. Res. 2015 2015
50. M. Krampera, L. Cosmi, R. Angeli, A. Pasini, F. Liotta, A. Andreini, and et al. Role for interferon-gamma in the immunomodulatory activity of human bone marrow mesenchymal stem cells Stem Cells 24 2006 386 398
51. S. Aggarwal, and M.F. Pittenger Human mesenchymal stem cells modulate allogeneic immune cell responses Transplantation 105 2009 1815 1822
52. S. Ghannam, C. Bouffi, F. Djouad, C. Jorgensen, and D. Noël Immunosuppression by mesenchymal stem cells: mechanisms and clinical applications Stem Cell Res. Ther. 1 2010
53. S. Ghannam, J. Pène, G. Torcy-Moquet, C. Jorgensen, and H. Yssel Mesenchymal stem cells inhibit human Th17 cell differentiation and function and induce a T regulatory cell phenotype J. Immunol. 185 2010 302 312
54. R. Meisel, A. Zibert, M. Laryea, and U. Go Brief report Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2, 3-dioxygenase-mediated tryptophan degradation Blood 103 2004 4619 4621
55. K. Sato, K. Ozaki, I. Oh, A. Meguro, K. Hatanaka, T. Nagai, and et al. Nitric oxide plays a critical role in suppression of T-cell proliferation by mesenchymal stem cells Nitric Oxide 109 2007 228 234
56. Y. Liu, S. Wang, and S. Shi The role of recipient T cells in mesenchymal stem cell-based tissue regeneration Int. J. Biochem. Cell Biol. 44 2012 2044 2050
57. U. Johansson, I. Rasmusson, S.P. Niclou, N. Forslund, L. Gustavsson, B. Nilsson, and et al. Formation of composite endothelial cell-mesenchymal Diabetes 2008 2393 2401
58. N.E. Davis, L.N. Beenken-Rothkopf, A. Mirsoian, N. Kojic, D.L. Kaplan, A.E. Barron, and et al. Enhanced function of pancreatic islets co-encapsulated with ECM proteins and mesenchymal stromal cells in a silk hydrogel Biomaterials 33 2012 6691 6697
59. V.S. Urbán, J. Kiss, J. Kovács, E. Gócza, V. Vas, E. Monostori, and et al. Mesenchymal stem cells cooperate with bone marrow cells in therapy of diabetes Stem Cells 26 2008 244 253
60. Y. Ding, D. Xu, G. Feng, A. Bushell, R.J. Muschel, and K.J. Wood Mesenchymal stem cells prevent the rejection of fully allogenic islet grafts by the immunosuppressive activity of matrix metalloproteinase-2 and -9 Diabetes 58 2009 1797 1806
61. Y.-H. Kim, Y.-M. Wee, M.-Y. Choi, D.-G. Lim, S.-C. Kim, and D.-J. Han Interleukin (IL)-10 induced by CD11b(+) cells and IL-10-activated regulatory T cells play a role in immune modulation of mesenchymal stem cells in rat islet allografts Mol. Med. 17 2011 697 708
62. K. Le Blanc, I. Rasmusson, B. Sundberg, C. Götherström, M. Hassan, M. Uzunel, and et al. Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells Lancet 363 2004 1439 1441
63. Z. Yan, Y. Zhuansun, R. Chen, J. Li, and P. Ran Immunomodulation of mesenchymal stromal cells on regulatory T cells and its possible mechanism Exp. Cell Res. 324 2014 65 74
64. S.P. Burr, F. Dazzi, and O. a Garden Mesenchymal stromal cells and regulatory T cells: the Yin and Yang of peripheral tolerance? Immunol. Cell Biol. 91 2013 12 18
65. R. Lin, H. Ma, Z. Ding, W. Shi, W. Qian, J. Song, and et al. Bone marrow-derived mesenchymal stem cells favor the immunosuppressive T cells skewing in a Helicobacter pylori model of gastric cancer Stem Cells Dev. 22 2013 2836 2848
66. W.T. Tse, J.D. Pendleton, W.M. Beyer, M.C. Egalka, and E.C. Guinan Suppression of allogeneic T-cell proliferation by human marrow stromal cells: implications in transplantation Transplantation 75 2003 389 397
67. B. Zhang, Y. Yin, R.C. Lai, S.S. Tan, A.B.H. Choo, and S.K. Lim Mesenchymal stem cells secrete immunologically active exosomes Stem Cells Dev. 23 2014 1233 1244
68. I. Rasmusson, O. Ringdén, B. Sundberg, and K. Le Blanc Mesenchymal stem cells inhibit the formation of cytotoxic T lymphocytes, but not activated cytotoxic T lymphocytes or natural killer cells Transplantation 76 2003 1208 1213
69. I. Rasmusson, M. Uhlin, K. Le Blanc, and V. Levitsky Mesenchymal stem cells fail to trigger effector functions of cytotoxic T lymphocytes J. Leukoc. Biol. 82 2007 887 893
70. C. Prevosto, M. Zancolli, P. Canevali, M.R. Zocchi, and A. Poggi Generation of CD4 + or CD8 + regulatory T cells upon mesenchymal stem cell-lymphocyte interaction Haematologica 92 2007 881 888
71. R. Blazquez, F.M. Sanchez-Margallo, O. de la Rosa, W. Dalemans, V. Alvarez, R. Tarazona, and et al. Immunomodulatory potential of human adipose mesenchymal stem cells derived exosomes on in vitro stimulated T cells Front. Immunol. 5 2014
72. J.D. Fontenot, M.A. Gavin, and A.Y. Rudensky Foxp3 programs the development and function of CD4 + CD25 + regulatory T cells Nat. Immunol. 4 2003 330 336
73. M.M. Duffy, J. Pindjakova, S.a. Hanley, C. McCarthy, G.a. Weidhofer, E.M. Sweeney, and et al. Mesenchymal stem cell inhibition of T-helper 17 cell-differentiation is triggered by cell-cell contact and mediated by prostaglandin E2 via the EP4 receptor Eur. J. Immunol. 41 2011 2840 2851
74. M. Miguel Immunosuppressive properties of mesenchymal stem cells: advances and applications Curr. Mol. Med. 12 2012 574 591
75. A. Corcione, F. Benvenuto, E. Ferretti, D. Giunti, V. Cappiello, F. Cazzanti, and et al. Human mesenchymal stem cells modulate B-cell functions Mult. Scler. 107 2006 367 372
76. S. Tabera, J.a. Pérez-Simón, M. Díez-Campelo, L.I. Sánchez-Abarca, B. Blanco, A. López, and et al. The effect of mesenchymal stem cells on the viability, proliferation and differentiation of B-lymphocytes Haematologica 93 2008 1301 1309
77. M.M. Rosado, M.E. Bernardo, M. Scarsella, A. Conforti, E. Giorda, S. Biagini, and et al. Inhibition of B-cell proliferation and antibody production by mesenchymal stromal cells is mediated by T cells Stem Cells Dev. 24 2015 93 103
78. A.J. Nauta, G. Westerhuis, A.B. Kruisselbrink, E.G. a Lurvink, R. Willemze, and W.E. Fibbe Donor-derived mesenchymal stem cells are immunogenic in a nonmyeloablative setting Stem Cells 108 2010 2114 2120
79. S. Inoue, F.C. Popp, G.E. Koehl, P. Piso, H.J. Schlitt, E.K. Geissler, and et al. Immunomodulatory effects of mesenchymal stem cells in a rat organ transplant model Transplantation 81 2006 1589 1595
80. P. Renner, E. Eggenhofer, a. Rosenauer, F.C. Popp, J.F. Steinmann, P. Slowik, and et al. Mesenchymal stem cells require a sufficient, ongoing immune response to exert their immunosuppressive function Transplant. Proc. 41 2009 2607 2611
81. D.-W.C.T.-H.S. b † J.J. c † Y.-J.C. c Jin-Hyung Shimd, 3D printed drug/cell carrier enabling effective release of cyclosporin A for xenogeneic cell-based therapy, Cell Transplant. (2015).
82. M. Sudres, F. Norol, a Trenado, S. Grégoire, F. Charlotte, B. Levacher, and et al. Bone marrow mesenchymal stem cells suppress lymphocyte proliferation in vitro but fail to prevent graft-versus-host disease in mice J. Immunol. 176 2006 7761 7767
83. S. Franz, S. Rammelt, D. Scharnweber, and J.C. Simon Immune responses to implants - a review of the implications for the design of immunomodulatory biomaterials Biomaterials 32 2011 6692 6709
84. J.S. Lewis, K. Roy, and B.G. Keselowsky Materials that harness and modulate the immune system MRS Bull. 39 2014 25 34
85. K. Yu, Y. Mei, N. Hadjesfandiari, and J.N. Kizhakkedathu Engineering biomaterials surfaces to modulate the host response Colloids Surf. B Biointerfaces 124 2014 69 79
86. H.M. Rostam, S. Singh, N.E. Vrana, M.R. Alexander, and A.M. Ghaemmaghami Impact of surface chemistry and topography on the function of antigen presenting cells Biomater. Sci. 3 2015 424 441
87. A. Ribeiro, P. Laranjeira, S. Mendes, I. Velada, C. Leite, P. Andrade, F. Santos, A. Henriques, M. Graos, C. Cardoso, A. Martinho, M. Pais, C Lobato da Silva, J Cabral, H. Trindade, and A. Paiva Mesenchymal stem cells from umbilical cord matrix, adipose tissue and bone marrow exhibit different capability to suppress peripheral blood B, natural killer and T cells. Stem Cell Res Ther 4 5 2013 125
88. K. Sato, K. Ozaki, M. Mori, K. Muroi, and K. Ozawa Mesenchymal stromal cells for graft-versus-host disease: basic aspects and clinical outcomes J. Clin. Exp. Hematop. 50 2010 79 89
89. N. Rozen, D. Lewinson, T. Bick, Z.C. Jacob, H. Stein, and M. Soudry Fracture repair: modulation of fracture-callus and mechanical properties by sequential application of IL-6 following PTH 1-34 or PTH 28-48 Bone 41 2007 437 445
90. Z.-Q. Lin, T. Kondo, Y. Ishida, T. Takayasu, and N. Mukaida Essential involvement of IL-6 in the skin wound-healing process as evidenced by delayed wound healing in IL-6-deficient mice J. Leukoc. Biol. 73 2003 713 721
91. W.H. Peranteau, L. Zhang, N. Muvarak, A.T. Badillo, A. Radu, P.W. Zoltick, and et al. IL-10 overexpression decreases inflammatory mediators and promotes regenerative healing in an adult model of scar formation J. Invest. Dermatol. 128 2008 1852 1860
92. R.M. Gower, R.M. Boehler, S.M. Azarin, C.F. Ricci, J.N. Leonard, and L.D. Shea Modulation of leukocyte infiltration and phenotype in microporous tissue engineering scaffolds via vector induced IL-10 expression Biomaterials 35 2014 2024 2031
93. R.M. Boehler, R. Kuo, S. Shin, a.G. Goodman, M.a. Pilecki, J.N. Leonard, and et al. Lentivirus delivery of IL-10 to promote and sustain macrophage polarization towards an anti-inflammatory phenotype Biotechnol. Bioeng. 111 2014 1210 1221
94. Y. Wang, N.-N. Wu, Y.-Q. Mou, L. Chen, and Z.-L. Deng Inhibitory effects of recombinant IL-4 and recombinant IL-13 on UHMWPE-induced bone destruction in the murine air pouch model J. Surg. Res. 180 2013 e73 e81
95. N. Mokarram, A. Merchant, V. Mukhatyar, G. Patel, and R.V. Bellamkonda Effect of modulating macrophage phenotype on peripheral nerve repair Biomaterials 33 2012 8793 8801
96. R. Marsell, and T.A. Einhorn The biology of fracture healing Injury 42 2011 551 555
97. J.M. Karnes, S.D. Daffner, and C.M. Watkins Multiple roles of tumor necrosis factor-alpha in fracture healing Bone 78 2015 87 93
98. G.E. Glass, J.K. Chan, A. Freidin, M. Feldmann, N.J. Horwood, and J. Nanchahal TNF-α promotes fracture repair by augmenting the recruitment and differentiation of muscle-derived stromal cells Proc. Natl. Acad. Sci. 108 2011 1585 1590
99. F.H. Zhou, B.K. Foster, X.-F. Zhou, A.J. Cowin, and C.J. Xian TNF-α mediates p38 MAP kinase activation and negatively regulates bone formation at the injured growth plate in rats J. Bone Miner. Res. 21 2006 1075 1088
100. S. Akira, T. Hirano, T. Taga, and T. Kishimoto Biology of multifunctional cytokines: IL 6 and related molecules (IL 1 and TNF) FASEB J. 4 1990 2860 2867
101. J. Lange, A. Sapozhnikova, C. Lu, D. Hu, X. Li, T. Miclau, and et al. Action of IL-1β during fracture healing J. Orthop. Res. 28 2010 778 784
102. S. Barrientos, O. Stojadinovic, M.S. Golinko, H. Brem, and M. Tomic-Canic Perspective article: growth factors and cytokines in wound healing Wound Repair Regen. 16 2008 585 601
103. D.J. Gorth, J.T. Martin, G.R. Dodge, N.M. Hebela, N.R. Malhotra, R.L. Mauck, and et al. In vivo delivery of IL-1ra from PLGA microspheres prevents IL-1β induced glycosaminoglycan loss in the rat caudal intervertebral disc ASME 2013 2nd Glob. Congr. Nanoeng. Med. Biol. 2013 American Society of Mechanical Engineers (pp. V001T04A004-V001T04A004)
104. S.M. Wahl, N. McCartney-Francis, and S.E. Mergenhagen Inflammatory and immunomodulatory roles of TGF-beta Immunol. Today 10 1989 258 261
105. A. Das, S. Tanner, D.A. Barker, D. Green, and E.A. Botchwey Delivery of S1P receptor-targeted drugs via biodegradable polymer scaffolds enhances bone regeneration in a critical size cranial defect J. Biomed. Mater. Res. A 102 2014 1210 1218
106. L.S. Sefcik, C.E.P. Aronin, K.A. Wieghaus, and E.A. Botchwey Sustained release of sphingosine 1-phosphate for therapeutic arteriogenesis and bone tissue engineering Biomaterials 29 2008 2869 2877
107. M. Kapoor, J. Martel-Pelletier, D. Lajeunesse, J.-P. Pelletier, and H. Fahmi Role of proinflammatory cytokines in the pathophysiology of osteoarthritis Nat. Rev. Rheumatol. 7 2011 33 42
108. V. Navikas, and H. Link Review: cytokines and the pathogenesis of multiple sclerosis J. Neurosci. Res. 45 1996 322 333
109. D.T. Luttikhuizen, M.C. Harmsen, and M.J.A. Van Luyn Cellular and molecular dynamics in the foreign body reaction Tissue Eng. 12 2006 1955 1970
110. P.M. Mountziaris, and A.G. Mikos Modulation of the inflammatory response for enhanced bone tissue regeneration Tissue Eng. B Rev. 14 2008 179 186
111. S. Browne, and A. Pandit Biomaterial-mediated modification of the local inflammatory environment Front. Bioeng. Biotechnol. 3 2015 1 14
112. R.M. Boehler, J.G. Graham, and L.D. Shea Tissue engineering tools for modulation of the immune response Biotechniques 51 2011 239 254
113. B.B. Aggarwal Signalling pathways of the TNF superfamily: a double-edged sword Nat. Rev. Immunol. 3 2003 745 756
114. L.C. Gerstenfeld, D.M. Cullinane, G.L. Barnes, D.T. Graves, and T.A. Einhorn Fracture healing as a post-natal developmental process: molecular, spatial, and temporal aspects of its regulation J. Cell. Biochem. 88 2003 873 884
115. J.R. Lieberman, and G.E. Friedlaender Bone regeneration and repair Chapter 4, Biol. Bone Graft 2005 Springer 57
116. T.A. Einhorn, and L.C. Gerstenfeld Fracture healing: mechanisms and interventions Nat. Rev. Rheumatol. 11 2014 45 54
117. P.M.P. Mountziaris, E.D. Lehman, I. Mountziaris, D.C. Sing, F.K. Kasper, and A.G. Mikos Effect of temporally patterned TNF-α delivery on in vitro osteogenic differentiation of mesenchymal stem cells cultured on biodegradable polymer scaffolds J. Biomater. Sci. Polym. Ed. 24 2013 1794 1813
118. J.E. Sims, and D.E. Smith The IL-1 family: regulators of immunity Nat. Rev. Immunol. 10 2010 89 102
119. J. Van Snick Interleukin-6: an overview Annu. Rev. Immunol. 8 1990 253 278
120. S.M. Opal, and V.A. DePalo Anti-inflammatory cytokines Chest 117 2000 1162 1172
121. K.R. Swartz, F. Liu, D. Sewell, T. Schochet, I. Campbell, M. Sandor, and et al. Interleukin-6 promotes post-traumatic healing in the central nervous system Brain Res. 896 2001 86 95
122. K.T. Steeve, P. Marc, T. Sandrine, H. Dominique, and F. Yannick IL-6, RANKL, TNF-alpha/IL-1: interrelations in bone resorption pathophysiology Cytokine Growth Factor Rev. 15 2004 49 60
123. E.M. Schwarz, D. Campbell, S. Totterman, A. Boyd, R.J. O'Keefe, and R.J. Looney Use of volumetric computerized tomography as a primary outcome measure to evaluate drug efficacy in the prevention of peri-prosthetic osteolysis: a 1-year clinical pilot of etanercept vs. placebo J. Orthop. Res. 21 2003 1049 1055
124. E.M. Schwarz, R.J. Looney, and R.J. O'Keefe Anti-TNF-α therapy as a clinical intervention for periprosthetic osteolysis Arthritis Res. 2 2000 165 168
125. D.M. Mosser, and X. Zhang Interleukin-10: new perspectives on an old cytokine Immunol. Rev. 226 2008 205 218
126. K.W. Moore, R. de Waal Malefyt, R.L. Coffman, and A. O'Garra Interleukin-10 and the interleukin-10 receptor Annu. Rev. Immunol. 19 2001 683 765
127. R. Sabat IL-10 family of cytokines Cytokine Growth Factor Rev. 21 2010 315 324
128. K.W. Moore, A. O'garra, R. de W. Malefyt, P. Vieira, and T.R. Mosmann Interleukin-10 Annu. Rev. Immunol. 11 1993 165 190
129. R. Sridharan, A.R. Cameron, D.J. Kelly, C.J. Kearney, and F.J. O'Brien Biomaterial based modulation of macrophage polarization: a review and suggested design principles Mater. Today 18 2015 313 325
130. A. Mantovani, A. Sica, S. Sozzani, P. Allavena, A. Vecchi, and M. Locati The chemokine system in diverse forms of macrophage activation and polarization Trends Immunol. 25 2004 677 686
131. P.J. Murray, and T.a. Wynn Protective and pathogenic functions of macrophage subsets Nat. Rev. Immunol. 11 2011 723 737
132. K. Shimokado, E.W. Raines, D.K. Madtes, T.B. Barrett, E.P. Benditt, and R. Ross A significant part of macrophage-derived growth factor consists of at least two forms of PDGF Cell 43 1985 277 286
133. K. Nelms, A.D. Keegan, J. Zamorano, J.J. Ryan, and W.E. Paul The IL-4 receptor: signaling mechanisms and biologic functions Annu. Rev. Immunol. 17 1999 701 738
134. M.C.D. Trindade, Y. Nakashima, M. Lind, D.-H. Sun, S.B. Goodman, W.J. Maloney, and et al. Interleukin-4 inhibits granulocyte-macrophage colony-stimulating factor, interleukin-6, and tumor necrosis factor-alpha expression by human monocytes in response to polymethylmethacrylate particle challenge in vitro michael J. Orthop. Res. 17 1999 797 802
135. S.B. Goodman, E. Gibon, J. Pajarinen, T.-H. Lin, M. Keeney, P.-G. Ren, and et al. Novel biological strategies for treatment of wear particle-induced periprosthetic osteolysis of orthopaedic implants for joint replacement J. R. Soc. Interface 11 2014 20130962
136. S.B. Goodman, E. Gómez Barrena, M. Takagi, and Y.T. Konttinen Biocompatibility of total joint replacements: a review J. Biomed. Mater. Res. A 90 2009 603 618
137. A.J. Rao, E. Gibon, T. Ma, Z. Yao, R.L. Smith, and S.B. Goodman Revision joint replacement, wear particles, and macrophage polarization Acta Biomater. 8 2012 2815 2823
138. G.-I. Im, and J.-D. Han Suppressive effects of interleukin-4 and interleukin-10 on the production of proinflammatory cytokines induced by titanium-alloy particles J. Biomed. Mater. Res. 58 2001 531 536
139. A.J. Rao, C. Nich, L.S. Dhulipala, E. Gibon, R. Valladares, S. Zwingenberger, and et al. Local effect of IL-4 delivery on polyethylene particle induced osteolysis in the murine calvarium J. Biomed. Mater. Res. A 101 2013 1926 1934
140. J. Pajarinen, V.-P. Kouri, E. Jämsen, T.-F. Li, J. Mandelin, and Y.T. Konttinen The response of macrophages to titanium particles is determined by macrophage polarization Acta Biomater. 9 2013 9229 9240
141. T.N. Vo, F.K. Kasper, and A.G. Mikos Strategies for controlled delivery of growth factors and cells for bone regeneration Adv. Drug Deliv. Rev. 64 2012 1292 1309
142. S. Werner, and R. Grose Regulation of wound healing by growth factors and cytokines Physiol. Rev. 83 2003 835 870
143. S. Barrientos, O. Stojadinovic, M.S. Golinko, H. Brem, and M. Tomic-Canic Growth factors and cytokines in wound healing Wound Repair Regen. 16 2008 585 601
144. P.R. Mangan, L.E. Harrington, D.B. O'Quinn, W.S. Helms, D.C. Bullard, C.O. Elson, and et al. Transforming growth factor-[beta] induces development of the TH17 lineage Nature 441 2006 231 234
145. E.J. Carbone, T. Jiang, C. Nelson, N. Henry, and K.W.-H. Lo Small molecule delivery through nanofibrous scaffolds for musculoskeletal regenerative engineering Nanomed. Nanotechnol. Biol. Med. 10 2014 1691 1699
146. C.T. Laurencin, K.M. Ashe, N. Henry, H.M. Kan, and K.W.-H. Lo Delivery of small molecules for bone regenerative engineering: preclinical studies and potential clinical applications Drug Discov. Today 19 2014 794 800
147. D. Längle, J. Halver, B. Rathmer, E. Willems, and D. Schade Small molecules targeting in vivo tissue regeneration ACS Chem. Biol. 9 2014 57 71
148. K.W.-H. Lo, T. Jiang, K.A. Gagnon, C. Nelson, and C.T. Laurencin Small-molecule based musculoskeletal regenerative engineering Trends Biotechnol. 32 2014 74 81
149. C.N. Serhan Pro-resolving lipid mediators are leads for resolution physiology Nature 510 2014 92 101