The paracrine effects of adipose-derived stem cells on neovascularization and biocompatibility of a macroencapsulation device

Acta Biomaterialia

Volumn 15, Issue , 2015, Pages 65-76

  Wang, Kai ^a   Yu, Lin Yang ^a   Jiang, Li Yang ^a   Wang, Hai Bin ^b   Wang, Chang Yong ^b   Luo, Ying ^a,c  

^a PEKING UNIVERSITY   (China)

^b BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

^c National Engineering Laboratory for Regenerative Implantable Medical Devices   (China)

Author keywords

Adipose derived stem cell; Angiogenesis; Foreign body reaction; Immunomodulation; Macroencapsulation

Indexed keywords

BIOCOMPATIBILITY; CELL CULTURE; ENDOTHELIAL CELLS; MICROFILTRATION; STEM CELLS;

ADIPOSE DERIVED STEM CELLS; ADIPOSE-DERIVED MESENCHYMAL STEM CELLS; ANGIOGENESIS; BIOMEDICAL DEVICES; FOREIGN BODY REACTIONS; FOREIGN BODY RESPONSE; IMMUNO MODULATIONS; MACRO-ENCAPSULATION; NEO-VASCULARIZATION; PARACRINE;

TISSUE;

BIOMATERIAL; POLITEF; ANTIINFLAMMATORY AGENT; CULTURE MEDIUM;

ADIPOSE DERIVED STEM CELL; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOCOMPATIBILITY; CONTROLLED STUDY; ENCAPSULATION; ENDOTHELIUM CELL; FILTRATION; HUMAN; HUMAN CELL; IMPLANT; IMPLANTATION; IN VITRO STUDY; IN VIVO STUDY; MACROENCAPSULATION DEVICE; MACROPHAGE; MALE; MEDICAL DEVICE; MESENCHYMAL STEM CELL; MICROENVIRONMENT; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PRIORITY JOURNAL; RAT; ADIPOSE TISSUE; ANIMAL; COCULTURE; CULTURE MEDIUM; CYTOLOGY; DEVICES; DRUG EFFECTS; FIBROSIS; GENE EXPRESSION REGULATION; GENETICS; IMMOBILIZED CELL; MATERIALS TESTING; MESENCHYMAL STROMA CELL; MULTICELLULAR SPHEROID; PARACRINE SIGNALING; PHARMACOLOGY; SPRAGUE DAWLEY RAT; THREE DIMENSIONAL IMAGING;

RATTUS;

ADIPOSE TISSUE; ANIMALS; ANTI-INFLAMMATORY AGENTS; BIOCOMPATIBLE MATERIALS; CELLS, IMMOBILIZED; COCULTURE TECHNIQUES; CULTURE MEDIA, CONDITIONED; FIBROSIS; GENE EXPRESSION REGULATION; IMAGING, THREE-DIMENSIONAL; IMPLANTS, EXPERIMENTAL; MALE; MATERIALS TESTING; MESENCHYMAL STROMAL CELLS; NEOVASCULARIZATION, PHYSIOLOGIC; PARACRINE COMMUNICATION; RATS, SPRAGUE-DAWLEY; SPHEROIDS, CELLULAR;

EID: 84922745540     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2014.12.025     Document Type: Article

References (62)

1. E.S. O'Sullivan, A. Vegas, D.G. Anderson, and G.C. Weir Islets transplanted in immunoisolation devices: a review of the progress and the challenges that remain Endocr Rev 32 2011 827 844
2. G. Orive, E. Santos, J.L. Pedraz, and R.M. Hernandez Application of cell encapsulation for controlled delivery of biological therapeutics Adv Drug Deliv Rev 67-68 2013 3 14
3. E. Santos, J.L. Pedraz, R.M. Hernandez, and G. Orive Therapeutic cell encapsulation: ten steps towards clinical translation J Control Release 170 2013 1 14
4. A. Sorenby, E. Rafael, A. Tibell, and A. Wernerson Improved histological evaluation of vascularity around an immunoisolation device by correlating number of vascular profiles to glucose exchange Cell Transplant 13 2004 713 719
5. G.C. Weir Islet encapsulation: advances and obstacles Diabetologia 56 2013 1458 1461
6. D.F. Williams On the mechanisms of biocompatibility Biomaterials 29 2008 2941 2953
7. J.M. Anderson, and A.K. McNally Biocompatibility of implants: lymphocyte/macrophage interactions Semin Immunopathol 33 2011 221 233
8. K. Junge, M. Binnebosel, K.T. von Trotha, R. Rosch, U. Klinge, and U.P. Neumann Mesh biocompatibility: effects of cellular inflammation and tissue remodelling Langenbecks Arch Surg 397 2012 255 270
9. 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
10. M. Ma, W.F. Liu, P.S. Hill, K.M. Bratlie, D.J. Siegwart, and J. Chin Development of cationic polymer coatings to regulate foreign-body responses Adv Mater 23 2011 H189 H194
11. L. Zhang, Z. Cao, T. Bai, L. Carr, J.R. Ella-Menye, and C. Irvin Zwitterionic hydrogels implanted in mice resist the foreign-body reaction Nat Biotechnol 31 2013 553 556
12. J.H. Brauker, V.E. Carr-Brendel, L.A. Martinson, J. Crudele, W.D. Johnston, and R.C. Johnson Neovascularization of synthetic membranes directed by membrane microarchitecture J Biomed Mater Res 29 1995 1517 1524
13. P. de Vos, M. Spasojevic, B.J. de Haan, and M.M. Faas The association between in vivo physicochemical changes and inflammatory responses against alginate based microcapsules Biomaterials 33 2012 5552 5559
14. S.H. Capone, M. Dufresne, M. Rechel, M.J. Fleury, A.V. Salsac, and P. Paullier Impact of alginate composition: from bead mechanical properties to encapsulated HepG2/C3A cell activities for in vivo implantation PLoS ONE 8 2013 e62032
15. S.D. Patil, F. Papadmitrakopoulos, and D.J. Burgess Concurrent delivery of dexamethasone and VEGF for localized inflammation control and angiogenesis J Control Release 117 2007 68 79
16. P.S. Hume, J. He, K. Haskins, and K.S. Anseth Strategies to reduce dendritic cell activation through functional biomaterial design Biomaterials 33 2012 3615 3625
17. N.M. Vacanti, H. Cheng, P.S. Hill, J.D. Guerreiro, T.T. Dang, and M. Ma Localized delivery of dexamethasone from electrospun fibers reduces the foreign body response Biomacromolecules 13 2012 3031 3038
18. T.T. Dang, A.V. Thai, J. Cohen, J.E. Slosberg, K. Siniakowicz, and J.C. Doloff Enhanced function of immuno-isolated islets in diabetes therapy by co-encapsulation with an anti-inflammatory drug Biomaterials 34 2013 5792 5801
19. M.E. Bernardo, and W.E. Fibbe Mesenchymal stromal cells: sensors and switchers of inflammation Cell Stem Cell 13 2013 392 402
20. Y. Miyahara, N. Nagaya, M. Kataoka, B. Yanagawa, K. Tanaka, and H. Hao Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction Nat Med 12 2006 459 465
21. S.H. Ranganath, O. Levy, M.S. Inamdar, and J.M. Karp Harnessing the mesenchymal stem cell secretome for the treatment of cardiovascular disease Cell Stem Cell 10 2012 244 258
22. P.R. Baraniak, and T.C. McDevitt Stem cell paracrine actions and tissue regeneration Regen Med 5 2009 121 143
23. M.Z. Ratajczak, M. Kucia, T. Jadczyk, N.J. Greco, W. Wojakowski, and M. Tendera Pivotal role of paracrine effects in stem cell therapies in regenerative medicine: can we translate stem cell-secreted paracrine factors and microvesicles into better therapeutic strategies? Leukemia 26 2012 1166 1173
24. J. Rehman, D. Traktuev, J. Li, S. Merfeld-Clauss, C.J. Temm-Grove, and J.E. Bovenkerk Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells Circulation 109 2004 1292 1298
25. N.G. Singer, and A.I. Caplan Mesenchymal stem cells: mechanisms of inflammation Annu Rev Pathol 6 2011 457 478
26. L. Chen, E.E. Tredget, P.Y. Wu, and Y. Wu Paracrine factors of mesenchymal stem cells recruit macrophages and endothelial lineage cells and enhance wound healing PLoS ONE 3 2008 e1886
27. K.S. Schweitzer, B.H. Johnstone, J. Garrison, N.I. Rush, S. Cooper, and D.O. Traktuev Adipose stem cell treatment in mice attenuates lung and systemic injury induced by cigarette smoking Am J Respir Crit Care Med 183 2011 215 225
28. S. Gatti, S. Bruno, M.C. Deregibus, A. Sordi, V. Cantaluppi, and C. Tetta Microvesicles derived from human adult mesenchymal stem cells protect against ischaemia-reperfusion-induced acute and chronic kidney injury Nephrol Dial Transplant 26 2011 1474 1483
29. J.M. Gimble, A.J. Katz, and B.A. Bunnell Adipose-derived stem cells for regenerative medicine Circ Res 100 2007 1249 1260
30. K. Wang, and Y. Luo Defined surface immobilization of glycosaminoglycan molecules for probing and modulation of cell-material interactions Biomacromolecules 14 2013 2373 2382
31. W.G. Brodbeck, G. Voskerician, N.P. Ziats, Y. Nakayama, T. Matsuda, and J.M. Anderson In vivo leukocyte cytokine mRNA responses to biomaterials are dependent on surface chemistry J Biomed Mater Res A 64 2003 320 329
32. R.J. Schutte, A. Parisi-Amon, and W.M. Reichert Cytokine profiling using monocytes/macrophages cultured on common biomaterials with a range of surface chemistries J Biomed Mater Res A 88A 2009 128 139
33. J.M. Anderson, A. Rodriguez, and D.T. Chang Foreign body reaction to biomaterials Semin Immunol 20 2008 86 100
34. T.J. Bartosh, J.H. Ylostalo, A. Mohammadipoor, N. Bazhanov, K. Coble, and K. Claypool Aggregation of human mesenchymal stromal cells (MSCs) into 3D spheroids enhances their antiinflammatory properties Proc Natl Acad Sci USA 107 2010 13724 13729
35. S.M. Melief, S.B. Geutskens, W.E. Fibbe, and H. Roelofs Multipotent stromal cells skew monocytes towards an anti-inflammatory interleukin-10-producing phenotype by production of interleukin-6 Haematologica 98 2013 888 895
36. J. Su, X. Chen, Y. Huang, W. Li, J. Li, and K. Cao Phylogenetic distinction of iNOS and IDO function in mesenchymal stem cell-mediated immunosuppression in mammalian species Cell Death Differ 21 2013 388 396
37. J.T. Pesce, T.R. Ramalingam, M.M. Mentink-Kane, M.S. Wilson, K.C. El Kasmi, and A.M. Smith Arginase-1-expressing macrophages suppress Th2 cytokine-driven inflammation and fibrosis PLoS Pathog 5 2009 e1000371
38. E. Rafael, G.S. Wu, K. Hultenby, A. Tibell, and A. Wernerson Improved survival of macroencapsulated islets of Langerhans by preimplantation of the immunoisolating device: a morphometric study Cell Transplant 12 2003 407 412
39. A.S. Johnson, R.J. Fisher, G.C. Weir, and C.K. Colton Oxygen consumption and diffusion in assemblages of respiring spheres: performance enhancement of a bioartificial pancreas Chem Eng Sci 64 2009 4470 4487
40. S.P. Nichols, A. Koh, N.L. Brown, M.B. Rose, B. Sun, and D.L. Slomberg The effect of nitric oxide surface flux on the foreign body response to subcutaneous implants Biomaterials 33 2012 6305 6312
41. W. Ji, F. Yang, H. Seyednejad, Z. Chen, W.E. Hennink, and J.M. Anderson Biocompatibility and degradation characteristics of PLGA-based electrospun nanofibrous scaffolds with nanoapatite incorporation Biomaterials 33 2012 6604 6614
42. K. Xu, D.A. Cantu, Y. Fu, J. Kim, X. Zheng, and P. Hematti Thiol-ene Michael-type formation of gelatin/poly(ethylene glycol) biomatrices for three-dimensional mesenchymal stromal/stem cell administration to cutaneous wounds Acta Biomater 9 2013 8802 8814
43. M.D. Swartzlander, A.D. Lynn, A.K. Blakney, T.R. Kyriakides, and S.J. Bryant Understanding the host response to cell-laden poly(ethylene glycol)-based hydrogels Biomaterials 34 2013 952 964
44. M.W. Laschke, T.E. Schank, C. Scheuer, S. Kleer, S. Schuler, and W. Metzger Three-dimensional spheroids of adipose-derived mesenchymal stem cells are potent initiators of blood vessel formation in porous polyurethane scaffolds Acta Biomater 9 2013 6876 6884
45. H.L. Prichard, W. Reichert, and B. Klitzman IFATS collection: adipose-derived stromal cells improve the foreign body response Stem Cells 26 2008 2691 2695
46. S.H. Bhang, S.W. Cho, W.G. La, T.J. Lee, H.S. Yang, and A.Y. Sun Angiogenesis in ischemic tissue produced by spheroid grafting of human adipose-derived stromal cells Biomaterials 32 2011 2734 2747
47. I.A. Potapova, P.R. Brink, I.S. Cohen, and S.V. Doronin Culturing of human mesenchymal stem cells as three-dimensional aggregates induces functional expression of CXCR4 that regulates adhesion to endothelial cells J Biol Chem 283 2008 13100 13107
48. U. Barkai, G.C. Weir, C.K. Colton, B. Ludwig, S.R. Bornstein, and M.D. Brendel Enhanced oxygen supply improves islet viability in a new bioartificial pancreas Cell Transplant 22 2013 1463 1476
49. B. Ludwig, A. Reichel, A. Steffen, B. Zimerman, A.V. Schally, and N.L. Block Transplantation of human islets without immunosuppression Proc Natl Acad Sci USA 110 2013 19054 19058
50. D.M. Mosser, and J.P. Edwards Exploring the full spectrum of macrophage activation Nat Rev Immunol 8 2008 958 969
51. B.D. Fleming, and D.M. Mosser Regulatory macrophages: setting the threshold for therapy Eur J Immunol 41 2011 2498 2502
52. T.A. Wynn, A. Chawla, and J.W. Pollard Macrophage biology in development, homeostasis and disease Nature 496 2013 445 455
53. J. Kim, and P. Hematti Mesenchymal stem cell-educated macrophages: a novel type of alternatively activated macrophages Exp Hematol 37 2009 1445 1453
54. J. Maggini, G. Mirkin, I. Bognanni, J. Holmberg, I.M. Piazzon, and I. Nepomnaschy Mouse bone marrow-derived mesenchymal stromal cells turn activated macrophages into a regulatory-like profile PLoS ONE 5 2010 e9252
55. J.H. Ylostalo, T.J. Bartosh, K. Coble, and D.J. Prockop Human mesenchymal stem/stromal cells cultured as spheroids are self-activated to produce prostaglandin E2 that directs stimulated macrophages into an anti-inflammatory phenotype Stem Cells 30 2012 2283 2296
56. E.M. Hetrick, H.L. Prichard, B. Klitzman, and M.H. Schoenfisch Reduced foreign body response at nitric oxide-releasing subcutaneous implants Biomaterials 28 2007 4571 4580
57. R.L. Geller, T. Loudovaris, S. Neuenfeldt, R.C. Johnson, and J.H. Brauker Use of an immunoisolation device for cell transplantation and tumor immunotherapy Ann N Y Acad Sci 831 1997 438 451
58. Y. Li, and F. Lin Mesenchymal stem cells are injured by complement after their contact with serum Blood 120 2012 3436 3443
59. G. Moll, I. Rasmusson-Duprez, L. von Bahr, A.M. Connolly-Andersen, G. Elgue, and L. Funke Are therapeutic human mesenchymal stromal cells compatible with human blood? Stem Cells 30 2012 1565 1574
60. J.A. Ankrum, J.F. Ong, and J.M. Karp Mesenchymal stem cells: immune evasive, not immune privileged Nat Biotechnol 32 2014 252 260
61. J.E. Bruin, A. Rezania, J. Xu, K. Narayan, J.K. Fox, and J.J. O'Neil Maturation and function of human embryonic stem cell-derived pancreatic progenitors in macroencapsulation devices following transplant into mice Diabetologia 56 2013 1987 1998
62. M. Kumagai-Braesch, S. Jacobson, H. Mori, X. Jia, T. Takahashi, and A. Wernerson The TheraCyte™ device protects against islet allograft rejection in immunized hosts Cell Transplant 22 2013 1137 1146