Implications of Extracellular Matrix Production by Adipose Tissue-Derived Stem Cells for Development of Wound Healing Therapies

Kathrine Hyldig, Simone Riis, Cristian Pablo Pennisi, Vladimir Zachar, Trine Fink, Kathrine Hyldig, Simone Riis, Cristian Pablo Pennisi, Vladimir Zachar, Trine Fink

Abstract

The synthesis and deposition of extracellular matrix (ECM) plays an important role in the healing of acute and chronic wounds. Consequently, the use of ECM as treatment for chronic wounds has been of special interest-both in terms of inducing ECM production by resident cells and applying ex vivo produced ECM. For these purposes, using adipose tissue-derived stem cells (ASCs) could be of use. ASCs are recognized to promote wound healing of otherwise chronic wounds, possibly through the reduction of inflammation, induction of angiogenesis, and promotion of fibroblast and keratinocyte growth. However, little is known regarding the importance of ASC-produced ECM for wound healing. In this review, we describe the importance of ECM for wound healing, and how ECM production by ASCs may be exploited in developing new therapies for the treatment of chronic wounds.

Keywords: ASCs; adipose stem cells; extracellular matrix; wound healing.

Conflict of interest statement

The authors declare no conflict of interest. The founding sponsors had no role in the writing of the manuscript, and in the decision to publish this review.

Figures

Figure 1
Figure 1
The phases of normal wound healing. Wound healing normally progresses through a tightly orchestrated process that is usually described as having four overlapping phases. During hemostasis, a platelet plug is formed and growth factors are secreted. The inflammatory phase has two stages. The initial stage, where neutrophils and pro-inflammatory M1 macrophages prevail, and a second stage characterized by the presence of anti-inflammatory M2 macrophages. During the proliferation phase, fibroblasts proliferate and synthesize extracellular matrix (ECM), new vessels are formed, and keratinocytes re-epithelialize the surface of the wound. In the final remodeling stage, the composition of the ECM is altered through degradation and resynthesis. PDGF: platelet-derived growth factor; TGF-β: transforming growth factor-β.
Figure 2
Figure 2
Characteristics of chronic wounds and the relevant regenerative effects of ASCs on these. Chronic wounds appear to unable to progress from the inflammatory phase of normal wound healing and to have impaired proliferation and remodeling phases (left panel). The ASCs have several regenerative characteristics that may lead to the wound progression from the inflammatory phase and through the proliferation and remodeling phases (right panel). ASC: adipose tissue-derived stem/stromal cells; MMP: matrix metalloproteinase; TIMP: tissue inhibitor of metalloproteinase; VEGF: vascular endothelial growth factor.

References

    1. Eming S.A., Martin P., Tomic-Canic M. Wound repair and regeneration: Mechanisms, signaling, and translation. Sci. Transl. Med. 2014;6:265sr6. doi: 10.1126/scitranslmed.3009337.
    1. Huang S.-P., Huang C.-H., Shyu J.-F., Lee H.-S., Chen S.-G., Chan J.Y.-H., Huang S.-M. Promotion of wound healing using adipose-derived stem cells in radiation ulcer of a rat model. J. Biomed. Sci. 2013;20:51. doi: 10.1186/1423-0127-20-51.
    1. Cerqueira M.T., Pirraco R.P., Marques A.P. Stem Cells in Skin Wound Healing: Are We There Yet? Adv. Wound Care. 2016;5:164–175. doi: 10.1089/wound.2014.0607.
    1. Zuk P.A., Zhu M., Mizuno H., Huang J., Futrell J.W., Katz A.J., Benhaim P., Lorenz H.P., Hedrick M.H. Multilineage cells from human adipose tissue: Implications for cell-based therapies. Tissue Eng. 2001;7:211–228. doi: 10.1089/107632701300062859.
    1. Zachar V., Rasmussen J.G., Fink T. Isolation and growth of adipose tissue-derived stem cells. Methods Mol. Biol. 2011;698:37–49.
    1. Riis S., Nielsen F.M., Pennisi C.P., Zachar V., Fink T. Comparative Analysis of Media and Supplements on Initiation and Expansion of Adipose-Derived Stem Cells. Stem Cells Transl. Med. 2016;5:314–324. doi: 10.5966/sctm.2015-0148.
    1. Nielsen F.M., Riis S.E., Andersen J.I., Lesage R., Fink T., Pennisi C.P., Zachar V. Discrete adipose-derived stem cell subpopulations may display differential functionality after in vitro expansion despite convergence to a common phenotype distribution. Stem Cell Res. Ther. 2016;7:177. doi: 10.1186/s13287-016-0435-8.
    1. Mattar P., Bieback K. Comparing the Immunomodulatory Properties of Bone Marrow, Adipose Tissue, and Birth-Associated Tissue Mesenchymal Stromal Cells. Front. Immunol. 2015;6:560. doi: 10.3389/fimmu.2015.00560.
    1. Rasmussen J.G., Frøbert O., Holst-Hansen C., Kastrup J., Baandrup U., Zachar V., Fink T., Simonsen U. Comparison of human adipose-derived stem cells and bone marrow-derived stem cells in a myocardial infarction model. Cell Transplant. 2014;23:195–206. doi: 10.3727/096368912X659871.
    1. Rasmussen J.G., Riis S.E., Frøbert O., Yang S., Kastrup J., Zachar V., Simonsen U., Fink T. Activation of Protease-Activated Receptor 2 Induces VEGF Independently of HIF-1. PLoS ONE. 2012;7:e46087. doi: 10.1371/journal.pone.0046087.
    1. Riis S., Newman R., Ipek H., Andersen J.I., Kuninger D., Boucher S., Vemuri M.C., Pennisi C.P.P., Zachar V., Fink T. Hypoxia enhances the wound-healing potential of adipose-derived stem cells in a novel human primary keratinocyte-based scratch assay. Int. J. Mol. Med. 2017;39:587–594. doi: 10.3892/ijmm.2017.2886.
    1. Shafy A., Fink T., Zachar V., Lila N., Carpentier A., Chachques J.C. Development of cardiac support bioprostheses for ventricular restoration and myocardial regeneration. Eur. J. Cardiothorac. Surg. 2013;43:1211–1219. doi: 10.1093/ejcts/ezs480.
    1. Lee E.Y., Xia Y., Kim W.-S., Lila N., Carpentier A., Chachques J.C. Hypoxia-enhanced wound-healing function of adipose-derived stem cells: Increase in stem cell proliferation and up-regulation of VEGF and bFGF. Wound Repair Regen. 2009;17:540–547. doi: 10.1111/j.1524-475X.2009.00499.x.
    1. Smith L.T., Holbrook K.A., Madri J.A. Collagen types I, III, and V in human embryonic and fetal skin. Am. J. Anat. 1986;175:507–521. doi: 10.1002/aja.1001750409.
    1. Verhaegen P.D.H.M., van Zuijlen P.P.M., Pennings N.M., van Marle J., Niessen F.B., van der Horst C.M.A.M., Middelkoop E. Differences in collagen architecture between keloid, hypertrophic scar, normotrophic scar, and normal skin: An objective histopathological analysis. Wound Repair Regen. 2009;17:649–656. doi: 10.1111/j.1524-475X.2009.00533.x.
    1. Eckes B., Nischt R., Krieg T. Cell-matrix interactions in dermal repair and scarring. Fibrogenesis Tissue Repair. 2010;3:4. doi: 10.1186/1755-1536-3-4.
    1. Hodde J.P., Johnson C.E. Extracellular matrix as a strategy for treating chronic wounds. Am. J. Clin. Dermatol. 2007;8:61–66. doi: 10.2165/00128071-200708020-00001.
    1. Giancotti F.G., Ruoslahti E. Integrin Signaling. Science. 1999;285:1028–1033. doi: 10.1126/science.285.5430.1028.
    1. Koivisto L., Heino J., Häkkinen L., Larjava H. Integrins in Wound Healing. Adv. Wound Care. 2014;3:762–783. doi: 10.1089/wound.2013.0436.
    1. Lynch S.E., Nixon J.C., Colvin R.B., Antoniades H.N. Role of platelet-derived growth factor in wound healing: Synergistic effects with other growth factors. Proc. Natl. Acad. Sci. USA. 1987;84:7696–7700. doi: 10.1073/pnas.84.21.7696.
    1. Barrientos S., Stojadinovic O., Golinko M.S., Brem H., Tomic-Canic M. PERSPECTIVE ARTICLE: Growth factors and cytokines in wound healing. Wound Repair Regen. 2008;16:585–601. doi: 10.1111/j.1524-475X.2008.00410.x.
    1. Schultz G.S., Wysocki A. Interactions between extracellular matrix and growth factors in wound healing. Wound Repair Regen. 2009;17:153–162. doi: 10.1111/j.1524-475X.2009.00466.x.
    1. Martins V.L., Caley M., O’Toole E.A. Matrix metalloproteinases and epidermal wound repair. Cell Tissue Res. 2013;351:255–268. doi: 10.1007/s00441-012-1410-z.
    1. Lozito T.P., Jackson W.M., Nesti L.J., Tuan R.S. Human mesenchymal stem cells generate a distinct pericellular zone of MMP activities via binding of MMPs and secretion of high levels of TIMPs. Matrix Biol. 2014;34:132–143. doi: 10.1016/j.matbio.2013.10.003.
    1. Tandara A.A., Mustoe T.A. MMP- and TIMP-secretion by human cutaneous keratinocytes and fibroblasts—Impact of coculture and hydration. J. Plast. Reconstr. Aesthetic. Surg. 2011;64:108–116. doi: 10.1016/j.bjps.2010.03.051.
    1. Nagase H., Visse R., Murphy G. Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc. Res. 2006;69:562–573. doi: 10.1016/j.cardiores.2005.12.002.
    1. Patel S., Maheshwari A., Chandra A. Biomarkers for wound healing and their evaluation. J. Wound Care. 2016;25:46–55. doi: 10.12968/jowc.2016.25.1.46.
    1. Olczyk P., Mencner Ł., Komosinska-Vassev K. The role of the extracellular matrix components in cutaneous wound healing. BioMed Res. Int. 2014;2014:747584. doi: 10.1155/2014/747584.
    1. Hassan W.U., Greiser U., Wang W. Role of adipose-derived stem cells in wound healing. Wound Repair Regen. 2014;22:313–325. doi: 10.1111/wrr.12173.
    1. Martinez F.O., Sica A., Mantovani A., Locati M. Macrophage activation and polarization. Front. Biosci. 2008;13:453–461. doi: 10.2741/2692.
    1. Ferrante C.J., Leibovich S.J. Regulation of Macrophage Polarization and Wound Healing. Adv. Wound Care. 2012;1:10–16. doi: 10.1089/wound.2011.0307.
    1. Pierce G.F., Mustoe T.A., Lingelbach J., Masakowski V.R., Griffin G.L., Senior R.M., Deuel T.F. Platelet-derived growth factor and transforming growth factor-beta enhance tissue repair activities by unique mechanisms. J. Cell Biol. 1989;109:429–440. doi: 10.1083/jcb.109.1.429.
    1. Vorotnikova E., McIntosh D., Dewilde A., Zhang J., Reing J.E., Zhang L., Cordero K., Bedelbaeva K., Gourevitch D., Heber-Katz E., et al. Extracellular matrix-derived products modulate endothelial and progenitor cell migration and proliferation in vitro and stimulate regenerative healing in vivo. Matrix Biol. 2010;29:690–700. doi: 10.1016/j.matbio.2010.08.007.
    1. Liu Y., Cox S.R., Morita T., Kourembanas S. Hypoxia regulates vascular endothelial growth factor gene expression in endothelial cells. Identification of a 5′ enhancer. Circ. Res. 1995;77:638–643. doi: 10.1161/01.RES.77.3.638.
    1. Ucuzian A.A., Gassman A.A., East A.T., Greisler H.P. Molecular mediators of angiogenesis. J. Burn Care Res. 2010;31:158–175. doi: 10.1097/BCR.0b013e3181c7ed82.
    1. Caley M.P., Martins V.L.C., O’Toole E.A. Metalloproteinases and Wound Healing. Adv. Wound Care. 2015;4:225–234. doi: 10.1089/wound.2014.0581.
    1. Wu M., Ben Amar M. Growth and remodelling for profound circular wounds in skin. Biomech. Model. Mechanobiol. 2015;14:357–370. doi: 10.1007/s10237-014-0609-1.
    1. Saarialho-Kere U.K. Patterns of matrix metalloproteinase and TIMP expression in chronic ulcers. Arch. Dermatol. Res. 1998;290:S47–S54. doi: 10.1007/PL00007453.
    1. Loots M.A.M., Lamme E.N., Zeegelaar J., Mekkes J.R., Bos J.D., Middelkoop E. Differences in Cellular Infiltrate and Extracellular Matrix of Chronic Diabetic and Venous Ulcers Versus Acute Wounds. J. Investig. Dermatol. 1998;111:850–857. doi: 10.1046/j.1523-1747.1998.00381.x.
    1. Sindrilaru A., Peters T., Wieschalka S., Baican C., Baican A., Peter H., Hainzl A., Schatz S., Qi Y., Schlecht A., et al. An unrestrained proinflammatory M1 macrophage population induced by iron impairs wound healing in humans and mice. J. Clin. Investig. 2011;121:985–997. doi: 10.1172/JCI44490.
    1. Mirza R., Koh T.J. Dysregulation of monocyte/macrophage phenotype in wounds of diabetic mice. Cytokine. 2011;56:256–264. doi: 10.1016/j.cyto.2011.06.016.
    1. Lucas T., Waisman A., Ranjan R., Roes J., Krieg T., Müller W., Roers A., Eming S.A. Differential Roles of Macrophages in Diverse Phases of Skin Repair. J. Immunol. 2010;184:3964–3977. doi: 10.4049/jimmunol.0903356.
    1. Park J.E., Barbul A. Understanding the role of immune regulation in wound healing. Am. J. Surg. 2004;187:S11–S16. doi: 10.1016/S0002-9610(03)00296-4.
    1. 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. 2010;5:e10088. doi: 10.1371/journal.pone.0010088.
    1. Seppanen E., Roy E., Ellis R., Bou-Gharios G., Fisk N.M., Khosrotehrani K. Distant Mesenchymal Progenitors Contribute to Skin Wound Healing and Produce Collagen: Evidence from a Murine Fetal Microchimerism Model. PLoS ONE. 2013;8:e62662. doi: 10.1371/journal.pone.0062662.
    1. Hasan A., Murata H., Falabella A., Ochoa S., Zhou L., Badiavas E., Falanga V. Dermal fibroblasts from venous ulcers are unresponsive to the action of transforming growth factor-beta 1. J. Dermatol. Sci. 1997;16:59–66. doi: 10.1016/S0923-1811(97)00622-1.
    1. Lobmann R., Ambrosch A., Schultz G., Waldmann K., Schiweck S., Lehnert H. Expression of matrix-metalloproteinases and their inhibitors in the wounds of diabetic and non-diabetic patients. Diabetologia. 2002;45:1011–1016. doi: 10.1007/s00125-002-0868-8.
    1. Subramaniam K., Pech C.M., Stacey M.C., Wallace H.J. Induction of MMP-1, MMP-3 and TIMP-1 in normal dermal fibroblasts by chronic venous leg ulcer wound fluid. Int. Wound J. 2008;5:79–86. doi: 10.1111/j.1742-481X.2007.00336.x.
    1. Demidova-Rice T.N., Hamblin M.R., Herman I.M. Acute and impaired wound healing: Pathophysiology and current methods for drug delivery, part 1: Normal and chronic wounds: Biology, causes, and approaches to care. Adv. Skin Wound Care. 2012;25:304–314. doi: 10.1097/01.ASW.0000416006.55218.d0.
    1. Schultz G.S., Sibbald R.G., Falanga V., Ayello E.A., Dowsett C., Harding K., Romanelli M., Stacey M.C., Teot L., Vanscheidt W. Wound bed preparation: A systematic approach to wound management. Wound Repair Regen. 2003;11(Suppl. S1):S1–S28. doi: 10.1046/j.1524-475X.11.s2.1.x.
    1. Ayello E.A., Dowsett C., Schultz G.S., Sibbald R.G., Falanga V., Harding K., Romanelli M., Stacey M., Teot L., Vanscheidt W. TIME heals all wounds. Nursing. 2004;34:36–42. doi: 10.1097/00152193-200404000-00040.
    1. 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. 2012;21:2724–2752. doi: 10.1089/scd.2011.0722.
    1. Riis S., Zachar V., Boucher S., Vemuri M.C., Pennisi C.P., Fink T. Critical steps in the isolation and expansion of adipose-derived stem cells for translational therapy. Expert Rev. Mol. Med. 2015;17:e11. doi: 10.1017/erm.2015.10.
    1. Baharlou R., Ahmadi-Vasmehjani A., Faraji F., Atashzar M.R., Khoubyari M., Ahi S., Erfanian S., Navabi S.-S. Human adipose tissue-derived mesenchymal stem cells in rheumatoid arthritis: Regulatory effects on peripheral blood mononuclear cells activation. Int. Immunopharmacol. 2017;47:59–69. doi: 10.1016/j.intimp.2017.03.016.
    1. Anderson P., Gonzalez-Rey E., O’Valle F., Martin F., Oliver F.J., Delgado M. Allogeneic Adipose-Derived Mesenchymal Stromal Cells Ameliorate Experimental Autoimmune Encephalomyelitis by Regulating Self-Reactive T Cell Responses and Dendritic Cell Function. Stem Cells Int. 2017;2017:1–15. doi: 10.1155/2017/2389753.
    1. Franquesa M., Mensah F.K., Huizinga R., Strini T., Boon L., Lombardo E., DelaRosa O., Laman J.D., Grinyó J.M., Weimar W., Betjes M.G.H., Baan C.C., Hoogduijn M.J. Human Adipose Tissue-Derived Mesenchymal Stem Cells Abrogate Plasmablast Formation and Induce Regulatory B Cells Independently of T Helper Cells. Stem Cells. 2015;33:880–891. doi: 10.1002/stem.1881.
    1. Manning C.N., Martel C., Sakiyama-Elbert S.E., Silva M.J., Shah S., Gelberman R.H., Thomopoulos S. Adipose-derived mesenchymal stromal cells modulate tendon fibroblast responses to macrophage-induced inflammation in vitro. Stem Cell Res. Ther. 2015;6:74. doi: 10.1186/s13287-015-0059-4.
    1. Lo Sicco C., Reverberi D., Balbi C., Ulivi V., Principi E., Pascucci L., Becherini P., Bosco M.C., Varesio L., Franzin C., Pozzobon M., Cancedda R., Tasso R. Mesenchymal Stem Cell-Derived Extracellular Vesicles as Mediators of Anti-Inflammatory Effects: Endorsement of Macrophage Polarization. Stem Cells Transl. Med. 2017;6:1018–1028. doi: 10.1002/sctm.16-0363.
    1. Zhao J., Hu L., Liu J., Gong N., Chen L. The effects of cytokines in adipose stem cell-conditioned medium on the migration and proliferation of skin fibroblasts in vitro. Biomed. Res. Int. 2013;2013:578479. doi: 10.1155/2013/578479.
    1. Hu L., Wang J., Zhou X., Xiong Z., Zhao J., Yu R., Huang F., Zhang H., Chen L. Exosomes derived from human adipose mensenchymal stem cells accelerates cutaneous wound healing via optimizing the characteristics of fibroblasts. Sci. Rep. 2016;6:32993. doi: 10.1038/srep32993.
    1. Na Y.K., Ban J.-J., Lee M., Im W., Kim M. Wound healing potential of adipose tissue stem cell extract. Biochem. Biophys. Res. Commun. 2017;485:30–34. doi: 10.1016/j.bbrc.2017.01.103.
    1. Rasmussen J.G., Frøbert O., Pilgaard L., Kastrup J., Simonsen U., Zachar V., Fink T. Prolonged hypoxic culture and trypsinization increase the pro-angiogenic potential of human adipose tissue-derived stem cells. Cytotherapy. 2011;13:318–328. doi: 10.3109/14653249.2010.506505.
    1. Lee S.H., Jin S.Y., Song J.S., Seo K.K., Cho K.H. Paracrine Effects of Adipose-Derived Stem Cells on Keratinocytes and Dermal Fibroblasts. Ann. Dermatol. 2012;24:136. doi: 10.5021/ad.2012.24.2.136.
    1. Zachar V., Duroux M., Emmersen J., Rasmussen J.G., Pennisi C.P., Yang S., Fink T. Hypoxia and adipose-derived stem cell-based tissue regeneration and engineering. Expert Opin. Biol. Ther. 2011;11:775–786. doi: 10.1517/14712598.2011.570258.
    1. Choi J.R., Yong K.W., Wan Safwani W.K.Z. Effect of hypoxia on human adipose-derived mesenchymal stem cells and its potential clinical applications. Cell. Mol. Life Sci. 2017 doi: 10.1007/s00018-017-2484-2.
    1. Riis S., Stensballe A., Emmersen J., Pennisi C.P., Birkelund S., Zachar V., Fink T. Mass spectrometry analysis of adipose-derived stem cells reveals a significant effect of hypoxia on pathways regulating extracellular matrix. Stem Cell Res. Ther. 2016;7:52. doi: 10.1186/s13287-016-0310-7.
    1. Brown B.N., Badylak S.F. Extracellular matrix as an inductive scaffold for functional tissue reconstruction. Transl. Res. 2014;163:268–285. doi: 10.1016/j.trsl.2013.11.003.
    1. Feng X., Shen R., Tan J., Chen X., Pan Y., Ruan S., Zhang F., Lin Z., Zeng Y., Wang X., Lin Y., Wu Q. The study of inhibiting systematic inflammatory response syndrome by applying xenogenic (porcine) acellular dermal matrix on second-degree burns. Burns. 2007;33:477–479. doi: 10.1016/j.burns.2006.08.011.
    1. Brigido S.A., Boc S.F., Lopez R.C. Effective management of major lower extremity wounds using an acellular regenerative tissue matrix: A pilot study. Orthopedics. 2004;27:s145–s149.
    1. Yonehiro L., Burleson G., Sauer V. Use of a new acellular dermal matrix for treatment of nonhealing wounds in the lower extremities of patients with diabetes. Wounds Compend. Clin. Res. Pract. 2013;25:340–344.
    1. Parmaksiz M., Dogan A., Odabas S., Elçin A.E., Elçin Y.M. Clinical applications of decellularized extracellular matrices for tissue engineering and regenerative medicine. Biomed. Mater. 2016;11:22003. doi: 10.1088/1748-6041/11/2/022003.
    1. Sun W.Q., Xu H., Sandor M., Lombardi J. Process-induced extracellular matrix alterations affect the mechanisms of soft tissue repair and regeneration. J. Tissue Eng. 2013;4:204173141350530. doi: 10.1177/2041731413505305.
    1. Scobie L., Padler-Karavani V., Le Bas-Bernardet S., Crossan C., Blaha J., Matouskova M., Hector R.D., Cozzi E., Vanhove B., Charreau B., et al. Long-Term IgG Response to Porcine Neu5Gc Antigens without Transmission of PERV in Burn Patients Treated with Porcine Skin Xenografts. J. Immunol. 2013;191:2907–2915. doi: 10.4049/jimmunol.1301195.
    1. Fitzpatrick L.E., McDevitt T.C. Cell-derived matrices for tissue engineering and regenerative medicine applications. Biomater. Sci. 2015;3:12–24. doi: 10.1039/C4BM00246F.
    1. Lu H., Hoshiba T., Kawazoe N., Koda I., Song M., Chen G. Cultured cell-derived extracellular matrix scaffolds for tissue engineering. Biomaterials. 2011;32:9658–9666. doi: 10.1016/j.biomaterials.2011.08.091.
    1. Zhang Z., Luo X., Xu H., Wang L., Jin X., Chen R., Ren X., Lu Y., Fu M., Huand Y. Bone marrow stromal cell-derived extracellular matrix promotes osteogenesis of adipose-derived stem cells. Cell Biol. Int. 2015;39:291–299. doi: 10.1002/cbin.10385.
    1. Aizman I., Tate C.C., McGrogan M., Case C.C. Extracellular matrix produced by bone marrow stromal cells and by their derivative, SB623 cells, supports neural cell growth. J. Neurosci. Res. 2009;87:3198–3206. doi: 10.1002/jnr.22146.
    1. Wagner W., Wein F., Seckinger A., Frankhauser M., Wirkner U., Krause U., Blake J., Schwager C., Eckstein V., Ansorge W., et al. Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp. Hematol. 2005;33:1402–1416. doi: 10.1016/j.exphem.2005.07.003.
    1. Ragelle H., Naba A., Larson B.L., Zhou F., Prijić M., Whittaker C.A., Del Rosario A., Langer R., Hynes R.O. Comprehensive proteomic characterization of stem cell-derived extracellular matrices. Biomaterials. 2017;128:147–159. doi: 10.1016/j.biomaterials.2017.03.008.
    1. Burns J.S., Kristiansen M., Kristensen L.P., Larsen K.H., Nielsen M.O., Christiansen H., Nehlin J., Andsern J.S., Kassem M. Decellularized Matrix from Tumorigenic Human Mesenchymal Stem Cells Promotes Neovascularization with Galectin-1 Dependent Endothelial Interaction. PLoS ONE. 2011;6:e21888. doi: 10.1371/journal.pone.0021888.
    1. Grenier G., Rémy-Zolghadri M., Larouche D., Gauvin R., Baker K., Bergeron F., Dupuis D., Langelier E., Rancourt D., Auger F.A., et al. Tissue reorganization in response to mechanical load increases functionality. Tissue Eng. 2005;11:90–100. doi: 10.1089/ten.2005.11.90.
    1. Colazzo F., Sarathchandra P., Smolenski R.T., Chester A.H., Tseng Y.T., Czernususzka J.T., Yacoub M.H., Taylor P.M. Extracellular matrix production by adipose-derived stem cells: Implications for heart valve tissue engineering. Biomaterials. 2011;32:119–127. doi: 10.1016/j.biomaterials.2010.09.003.
    1. Foldberg S., Petersen M., Fojan P., Gurevich L., Fink T., Pennisi C.P., Zachar V. Patterned poly(lactic acid) films support growth and spontaneous multilineage gene expression of adipose-derived stem cells. Colloids Surf. B Biointerfaces. 2012;93:92–99. doi: 10.1016/j.colsurfb.2011.12.018.
    1. Lam M.T., Nauta A., Meyer N.P., Wu J.C., Longaker M.T. Effective Delivery of Stem Cells Using an Extracellular Matrix Patch Results in Increased Cell Survival and Proliferation and Reduced Scarring in Skin Wound Healing. Tissue Eng. Part A. 2013;19:738–747. doi: 10.1089/ten.tea.2012.0480.

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