Skin Tissue Engineering: Application of Adipose-Derived Stem Cells

Agnes S Klar, Jakub Zimoch, Thomas Biedermann, Agnes S Klar, Jakub Zimoch, Thomas Biedermann

Abstract

Perception of the adipose tissue has changed dramatically over the last few decades. Identification of adipose-derived stem cells (ASCs) ultimately transformed paradigm of this tissue from a passive energy depot into a promising stem cell source with properties of self-renewal and multipotential differentiation. As compared to bone marrow-derived stem cells (BMSCs), ASCs are more easily accessible and their isolation yields higher amount of stem cells. Therefore, the ASCs are of high interest for stem cell-based therapies and skin tissue engineering. Currently, freshly isolated stromal vascular fraction (SVF), which may be used directly without any expansion, was also assessed to be highly effective in treating skin radiation injuries, burns, or nonhealing wounds such as diabetic ulcers. In this paper, we review the characteristics of SVF and ASCs and the efficacy of their treatment for skin injuries and disorders.

Conflict of interest statement

The authors declare that there is no conflict of interests regarding the publication of this paper.

Figures

Figure 1
Figure 1
Development of a three-dimensional prevascularized dermo-epidermal skin substitute. Primary cells including epidermal keratinocytes, melanocytes, dermal fibroblasts, and endothelial cells can be isolated from a single skin biopsy. Dermal fibroblasts and endothelial cells are embedded into a collagen type 1 hydrogel to create a prevascularized dermal compartment. After they remodeled the collagen matrix, keratinocytes and melanocytes are then seeded onto it to create a pigmented epidermal layer.
Figure 2
Figure 2
Examples of clinical application of autologous fat and adipose-derived stem cells (ASCs). Freshly isolated lipoaspirate is processed to obtain a fat graft. This can be applied to patients suffering, for example, from facial asymmetry, radiated defects, or traumatic wounds. The fat graft can be further enriched by adding freshly isolated SVF or cultured adipose-derived stem cells (ASCs).

References

    1. Wood F. M., Kolybaba M. L., Allen P. The use of cultured epithelial autograft in the treatment of major burn injuries: a critical review of the literature. Burns. 2006;32(4):395–401. doi: 10.1016/j.burns.2006.01.008.
    1. Atiyeh B. S., Costagliola M. Cultured epithelial autograft (CEA) in burn treatment: three decades later. Burns. 2007;33(4):405–413. doi: 10.1016/j.burns.2006.11.002.
    1. Meuli M., Raghunath M. Tops and flops using cultured epithelial autografts in children. Pediatric Surgery International. 1997;12(7):471–477. doi: 10.1007/s003830050187.
    1. Braziulis E., Biedermann T., Hartmann-Fritsch F., et al. Skingineering I: engineering porcine dermo-epidermal skin analogues for autologous transplantation in a large animal model. Pediatric Surgery International. 2011;27(3):241–247. doi: 10.1007/s00383-010-2777-0.
    1. Schiestl C., Biedermann T., Braziulis E., et al. Skingineering II: transplantation of large-scale laboratory-grown skin analogues in a new pig model. Pediatric Surgery International. 2011;27(3):249–254. doi: 10.1007/s00383-010-2792-1.
    1. Braziulis E., Diezi M., Biedermann T., et al. Modified plastic compression of collagen hydrogels provides an ideal matrix for clinically applicable skin substitutes. Tissue Engineering Part C: Methods. 2012;18(6):464–474. doi: 10.1089/ten.tec.2011.0561.
    1. Böttcher-Haberzeth S., Biedermann T., Klar A. S., et al. Characterization of pigmented dermo-epidermal skin substitutes in a long-term in vivo assay. Experimental Dermatology. 2015;24(1):16–21. doi: 10.1111/exd.12570.
    1. Böttcher-Haberzeth S., Klar A. S., Biedermann T., et al. ‘Trooping the color’: restoring the original donor skin color by addition of melanocytes to bioengineered skin analogs. Pediatric Surgery International. 2013;29(3):239–247. doi: 10.1007/s00383-012-3217-0.
    1. Böttcher-Haberzeth S., Biedermann T., Pontiggia L., et al. Human eccrine sweat gland cells turn into melanin-uptaking keratinocytes in dermo-epidermal skin substitutes. Journal of Investigative Dermatology. 2013;133(2):316–324. doi: 10.1038/jid.2012.290.
    1. Klar A. S., Güven S., Biedermann T., et al. Tissue-engineered dermo-epidermal skin grafts prevascularized with adipose-derived cells. Biomaterials. 2014;35(19):5065–5078. doi: 10.1016/j.biomaterials.2014.02.049.
    1. Klar A. S., Güven S., Zimoch J., et al. Characterization of vasculogenic potential of human adipose-derived endothelial cells in a three-dimensional vascularized skin substitute. Pediatric Surgery International. 2016;32(1):17–27. doi: 10.1007/s00383-015-3808-7.
    1. Fraser J. K., Zhu M., Wulur I., Alfonso Z. Adipose-derived stem cells. Methods in Molecular Biology. 2008;449:59–67.
    1. De Ugarte D. A., Morizono K., Elbarbary A., et al. Comparison of multi-lineage cells from human adipose tissue and bone marrow. Cells Tissues Organs. 2003;174(3):101–109. doi: 10.1159/000071150.
    1. Oedayrajsingh-Varma M. J., van Ham S. M., Knippenberg M., et al. Adipose tissue-derived mesenchymal stem cell yield and growth characteristics are affected by the tissue-harvesting procedure. Cytotherapy. 2006;8(2):166–177. doi: 10.1080/14653240600621125.
    1. Pittenger M. F., Mackay A. M., Beck S. C., et al. Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284(5411):143–147. doi: 10.1126/science.284.5411.143.
    1. Erickson G. R., Gimble J. M., Franklin D. M., Rice H. E., Awad H., Guilak F. Chondrogenic potential of adipose tissue-derived stromal cells in vitro and in vivo. Biochemical and Biophysical Research Communications. 2002;290(2):763–769. doi: 10.1006/bbrc.2001.6270.
    1. Han J., Koh Y. J., Moon H. R., et al. Adipose tissue is an extramedullary reservoir for functional hematopoietic stem and progenitor cells. Blood. 2010;115(5):957–964. doi: 10.1182/blood-2009-05-219923.
    1. Zimmerlin L., Donnenberg V. S., Pfeifer M. E., et al. Stromal vascular progenitors in adult human adipose tissue. Cytometry Part A. 2010;77(1):22–30. doi: 10.1002/cyto.a.20813.
    1. Maumus M., Peyrafitte J.-A., D'Angelo R., et al. Native human adipose stromal cells: localization, morphology and phenotype. International Journal of Obesity. 2011;35(9):1141–1153. doi: 10.1038/ijo.2010.269.
    1. McIntosh K., Zvonic S., Garrett S., et al. The immunogenicity of human adipose-derived cells: temporal changes in vitro. STEM CELLS. 2006;24(5):1246–1253. doi: 10.1634/stemcells.2005-0235.
    1. Sengenès C., Lolmède K., Zakaroff-Girard A., Busse R., Bouloumié A. Preadipocytes in the human subcutaneous adipose tissue display distinct features from the adult mesenchymal and hematopoietic stem cells. Journal of Cellular Physiology. 2005;205(1):114–122. doi: 10.1002/jcp.20381.
    1. Planat-Benard V., Silvestre J.-S., Cousin B., et al. Plasticity of human adipose lineage cells toward endothelial cells: physiological and therapeutic perspectives. Circulation. 2004;109(5):656–663. doi: 10.1161/01.cir.0000114522.38265.61.
    1. Scherberich A., Di Maggio N. D., McNagny K. M. A familiar stranger: CD34 expression and putative functions in SVF cells of adipose tissue. World Journal of Stem Cells. 2013;5(1):1–8. doi: 10.4252/wjsc.v5.i1.1.
    1. Bourin P., Bunnell B. A., Casteilla L., et al. Stromal cells from the adipose tissue-derived stromal vascular fraction and culture expanded adipose tissue-derived stromal/stem cells: a joint statement of the International Federation for Adipose Therapeutics and Science (IFATS) and the International Society for Cellular Therapy (ISCT) Cytotherapy. 2013;15(6):641–648. doi: 10.1016/j.jcyt.2013.02.006.
    1. Choi S. A., Lee J. Y., Wang K.-C., et al. Human adipose tissue-derived mesenchymal stem cells: characteristics and therapeutic potential as cellular vehicles for prodrug gene therapy against brainstem gliomas. European Journal of Cancer. 2012;48(1):129–137. doi: 10.1016/j.ejca.2011.04.033.
    1. Estes B. T., Wu A. W., Guilak F. Potent induction of chondrocytic differentiation of human adipose-derived adult stem cells by bone morphogenetic protein 6. Arthritis and Rheumatism. 2006;54(4):1222–1232. doi: 10.1002/art.21779.
    1. Halvorsen Y.-D. C., Bond A., Sen A., et al. Thiazolidinediones and glucocorticoids synergistically induce differentiation of human adipose tissue stromal cells: biochemical, cellular, and molecular analysis. Metabolism: Clinical and Experimental. 2001;50(4):407–413. doi: 10.1053/meta.2001.21690.
    1. Lindroos B., Suuronen R., Miettinen S. The potential of adipose stem cells in regenerative medicine. Stem Cell Reviews and Reports. 2011;7(2):269–291. doi: 10.1007/s12015-010-9193-7.
    1. Zuk P. A., Zhu M., Mizuno H., et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Engineering. 2001;7(2):211–228. doi: 10.1089/107632701300062859.
    1. Zuk P. A., Zhu M., Ashjian P., et al. Human adipose tissue is a source of multipotent stem cells. Molecular Biology of the Cell. 2002;13(12):4279–4295. doi: 10.1091/mbc.E02-02-0105.
    1. Pachón-Peña G., Yu G., Tucker A., et al. Stromal stem cells from adipose tissue and bone marrow of age-matched female donors display distinct immunophenotypic profiles. Journal of Cellular Physiology. 2011;226(3):843–851. doi: 10.1002/jcp.22408.
    1. Mitchell J. B., McIntosh K., Zvonic S., et al. Immunophenotype of human adipose-derived cells: temporal changes in stromal-associated and stem cell-associated markers. STEM CELLS. 2006;24(2):376–385. doi: 10.1634/stemcells.2005-0234.
    1. Gimble J. M., Katz A. J., Bunnell B. A. Adipose-derived stem cells for regenerative medicine. Circulation Research. 2007;100(9):1249–1260. doi: 10.1161/01.RES.0000265074.83288.09.
    1. Aso K., Tsuruhara A., Takagaki K., et al. Adipose-derived mesenchymal stem cells restore impaired mucosal immune responses in aged mice. PLoS ONE. 2016;11(2) doi: 10.1371/journal.pone.0148185.e0148185
    1. Gonzalez-Rey E., Anderson P., González M. A., Rico L., Büscher D., Delgado M. Human adult stem cells derived from adipose tissue protect against experimental colitis and sepsis. Gut. 2009;58(7):929–939. doi: 10.1136/gut.2008.168534.
    1. McIntosh K. R. Evaluation of cellular and humoral immune responses to allogeneic adipose-derived stem/stromal cells. Methods in Molecular Biology. 2011;702:133–150. doi: 10.1007/978-1-61737-960-4_11.
    1. Puissant B., Barreau C., Bourin P., et al. Immunomodulatory effect of human adipose tissue-derived adult stem cells: comparison with bone marrow mesenchymal stem cells. British Journal of Haematology. 2005;129(1):118–129. doi: 10.1111/j.1365-2141.2005.05409.x.
    1. Kilroy G. E., Foster S. J., Wu X., et al. Cytokine profile of human adipose-derived stem cells: expression of angiogenic, hematopoietic, and pro-inflammatory factors. Journal of Cellular Physiology. 2007;212(3):702–709. doi: 10.1002/jcp.21068.
    1. Prichard H. L., Reichert W., Klitzman B. IFATS collection: adipose-derived stromal cells improve the foreign body response. STEM CELLS. 2008;26(10):2691–2695. doi: 10.1634/stemcells.2008-0140.
    1. Wang L., Lu Y., Luo X., et al. Cell-assisted lipotransfer for breast augmentation: a report of 18 patients. Zhonghua Zheng Xing Wai Ke Za Zhi. 2012;28(1):1–6.
    1. Miranville A., Heeschen C., Sengenès C., Curat C. A., Busse R., Bouloumié A. Improvement of postnatal neovascularization by human adipose tissue-derived stem cells. Circulation. 2004;110(3):349–355. doi: 10.1161/01.CIR.0000135466.16823.D0.
    1. Rehman J., Traktuev D., Li J., et al. Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells. Circulation. 2004;109(10):1292–1298. doi: 10.1161/01.cir.0000121425.42966.f1.
    1. Sumi M., Sata M., Toya N., Yanaga K., Ohki T., Nagai R. Transplantation of adipose stromal cells, but not mature adipocytes, augments ischemia-induced angiogenesis. Life Sciences. 2007;80(6):559–565. doi: 10.1016/j.lfs.2006.10.020.
    1. Nakagami H., Maeda K., Morishita R., et al. Novel autologous cell therapy in ischemic limb disease through growth factor secretion by cultured adipose tissue-derived stromal cells. Arteriosclerosis, Thrombosis, and Vascular Biology. 2005;25(12):2542–2547. doi: 10.1161/01.ATV.0000190701.92007.6d.
    1. Cai L., Johnstone B. H., Cook T. G., et al. IFATS collection: human adipose tissue-derived stem cells induce angiogenesis and nerve sprouting following myocardial infarction, in conjunction with potent preservation of cardiac function. STEM CELLS. 2009;27(1):230–237. doi: 10.1634/stemcells.2008-0273.
    1. Sadat S., Gehmert S., Song Y.-H., et al. The cardioprotective effect of mesenchymal stem cells is mediated by IGF-I and VEGF. Biochemical and Biophysical Research Communications. 2007;363(3):674–679. doi: 10.1016/j.bbrc.2007.09.058.
    1. Schenke-Layland K., Strem B. M., Jordan M. C., et al. Adipose tissue-derived cells improve cardiac function following myocardial infarction. The Journal of Surgical Research. 2009;153(2):217–223. doi: 10.1016/j.jss.2008.03.019.
    1. Zografou A., Tsigris C., Papadopoulos O., et al. Improvement of skin-graft survival after autologous transplantation of adipose-derived stem cells in rats. Journal of Plastic, Reconstructive and Aesthetic Surgery. 2011;64(12):1647–1656. doi: 10.1016/j.bjps.2011.07.009.
    1. Gao W. C., Qiao X., Ma S. L., Cui L. Adipose-derived stem cells accelerate neovascularization in ischaemic diabetic skin flap via expression of hypoxia-inducible factor-1α. Journal of Cellular and Molecular Medicine. 2011;15(12):2575–2585. doi: 10.1111/j.1582-4934.2011.01313.x.
    1. Yoshimura K., Sato K., Aoi N., Kurita M., Hirohi T., Harii K. Cell-assisted lipotransfer for cosmetic breast augmentation: supportive use of adipose-derived stem/stromal cells. Aesthetic Plastic Surgery. 2008;32(1):48–57. doi: 10.1007/s00266-007-9019-4.
    1. Yoshimura K., Asano Y., Aoi N., et al. Progenitor-enriched adipose tissue transplantation as rescue for breast implant complications. Breast Journal. 2010;16(2):169–175. doi: 10.1111/j.1524-4741.2009.00873.x.
    1. Kamakura T., Ito K. Autologous cell-enriched fat grafting for breast augmentation. Aesthetic Plastic Surgery. 2011;35(6):1022–1030. doi: 10.1007/s00266-011-9727-7.
    1. Gentile P., Orlandi A., Scioli M. G., et al. A comparative translational study: the combined use of enhanced stromal vascular fraction and platelet-rich plasma improves fat grafting maintenance in breast reconstruction. Stem Cells Translational Medicine. 2012;1(4):341–351. doi: 10.5966/sctm.2011-0065.
    1. Peltoniemi H. H., Salmi A., Miettinen S., et al. Stem cell enrichment does not warrant a higher graft survival in lipofilling of the breast: a prospective comparative study. Journal of Plastic, Reconstructive and Aesthetic Surgery. 2013;66(11):1494–1503. doi: 10.1016/j.bjps.2013.06.002.
    1. Kølle S.-F. T., Fischer-Nielsen A., Mathiasen A. B., et al. Enrichment of autologous fat grafts with ex-vivo expanded adipose tissue-derived stem cells for graft survival: a randomised placebo-controlled trial. The Lancet. 2013;382(9898):1113–1120. doi: 10.1016/s0140-6736(13)61410-5.
    1. Tissiani L. A. L., Alonso N. A prospective and controlled clinical trial on stromal vascular fraction enriched fat grafts in secondary breast reconstruction. Stem Cells International. 2016;2016:12. doi: 10.1155/2016/2636454.2636454
    1. Tiryaki T., Findikli N., Tiryaki D. Staged stem cell-enriched tissue (SET) injections for soft tissue augmentation in hostile recipient areas: a preliminary report. Aesthetic Plastic Surgery. 2011;35(6):965–971. doi: 10.1007/s00266-011-9716-x.
    1. Gentile P., De Angelis B., Pasin M., et al. Adipose-derived stromal vascular fraction cells and platelet-rich plasma: basic and clinical evaluation for cell-based therapies in patients with scars on the face. Journal of Craniofacial Surgery. 2014;25(1):267–272. doi: 10.1097/.
    1. Granel B., Daumas A., Jouve E., et al. Safety, tolerability and potential efficacy of injection of autologous adipose-derived stromal vascular fraction in the fingers of patients with systemic sclerosis: an open-label phase I trial. Annals of the Rheumatic Diseases. 2015;74(12):2175–2182. doi: 10.1136/annrheumdis-2014-205681.
    1. Guillaume-Jugnot P., Daumas A., Magalon J., et al. Autologous adipose-derived stromal vascular fraction in patients with systemic sclerosis: 12-month follow-up. Rheumatology. 2016;55(2):301–306. doi: 10.1093/rheumatology/kev323.
    1. Sterodimas A., de Faria J., Nicaretta B., Boriani F. Autologous fat transplantation versus adipose-derived stem cell-enriched lipografts: a study. Aesthetic Surgery Journal. 2011;31(6):682–693. doi: 10.1177/1090820x11415976.
    1. Castro-Govea Y., De La Garza-Pineda O., Lara-Arias J., et al. Cell-assisted lipotransfer for the treatment of Parry-Romberg syndrome. Archives of Plastic Surgery. 2012;39(6):659–662. doi: 10.5999/aps.2012.39.6.659.
    1. Koh K. S., Oh T. S., Kim H., et al. Clinical application of human adipose tissue-derived mesenchymal stem cells in progressive hemifacial atrophy (Parry-Romberg disease) with microfat grafting techniques using 3-dimensional computed tomography and 3-dimensional camera. Annals of Plastic Surgery. 2012;69(3):331–337. doi: 10.1097/SAP.0b013e31826239f0.
    1. Chang Q., Li J., Dong Z. Q., Liu L. Q., Lu F. Quantitative volumetric analysis of progressive hemifacial atrophy corrected using stromal vascular fraction-supplemented autologous fat grafts. Dermatologic Surgery. 2013;39(10):1465–1473. doi: 10.1111/dsu.12310.
    1. Rigotti G., Marchi A., Galiè M., et al. Clinical treatment of radiotherapy tissue damage by lipoaspirate transplant: a healing process mediated by adipose-derived adult stem cells. Plastic and Reconstructive Surgery. 2007;119(5):1409–1422. doi: 10.1097/01.prs.0000256047.47909.71.
    1. Lee H. C., An S. G., Lee H. W., et al. Safety and effect of adipose tissue-derived stem cell implantation in patients with critical limb ischemia—a pilot study. Circulation Journal. 2012;76(7):1750–1760. doi: 10.1253/circj.cj-11-1135.
    1. Marino G., Moraci M., Armenia E., et al. Therapy with autologous adipose-derived regenerative cells for the care of chronic ulcer of lower limbs in patients with peripheral arterial disease. Journal of Surgical Research. 2013;185(1):36–44. doi: 10.1016/j.jss.2013.05.024.
    1. Gu H., Long D., Song C., Li X. Recombinant human NGF-loaded microspheres promote survival of basal forebrain cholinergic neurons and improve memory impairments of spatial learning in the rat model of Alzheimer's disease with fimbria-fornix lesion. Neuroscience Letters. 2009;453(3):204–209. doi: 10.1016/j.neulet.2009.02.027.
    1. McCoy M. K., Martinez T. N., Ruhn K. A., et al. Autologous transplants of Adipose-Derived Adult Stromal (ADAS) cells afford dopaminergic neuroprotection in a model of Parkinson's disease. Experimental Neurology. 2008;210(1):14–29. doi: 10.1016/j.expneurol.2007.10.011.
    1. Zhu M., Heydarkhan-Hagvall S., Hedrick M., Benhaim P., Zuk P. Manual isolation of adipose-derived stem cells from human lipoaspirates. Journal of Visualized Experiments. 2013;(79) doi: 10.3791/50585.e50585
    1. Domenis R., Lazzaro L., Calabrese S., et al. Adipose tissue derived stem cells: in vitro and in vivo analysis of a standard and three commercially available cell-assisted lipotransfer techniques. Stem Cell Research and Therapy. 2015;6(1, article 2) doi: 10.1186/scrt536.
    1. Aronowitz J. A., Ellenhorn J. D. I. Adipose stromal vascular fraction isolation: a head-to-head comparison of four commercial cell separation systems. Plastic and Reconstructive Surgery. 2013;132(6):p. 932e-9e. doi: 10.1097/PRS.0b013e3182a80652.
    1. Tremolada C., Colombo V., Ventura C. Adipose tissue and mesenchymal stem cells: state of the art and lipogems® technology development. Current Stem Cell Reports. 2016;2(3):304–312. doi: 10.1007/s40778-016-0053-5.
    1. Fraser J. K., Hicok K. C., Shanahan R., Zhu M., Miller S., Arm D. M. The Celution® system: automated processing of adipose-derived regenerative cells in a functionally closed system. Advances in Wound Care. 2014;3(1):38–45. doi: 10.1089/wound.2012.0408.
    1. Guven S., Karagianni M., Schwalbe M., et al. Validation of an automated procedure to isolate human adipose tissue-derived cells by using the Sepax ® technology. Tissue Engineering Part C: Methods. 2012;18(8):575–582. doi: 10.1089/ten.tec.2011.0617.
    1. Doi K., Tanaka S., Iida H., et al. Stromal vascular fraction isolated from lipo-aspirates using an automated processing system: bench and bed analysis. Journal of Tissue Engineering and Regenerative Medicine. 2013;7(11):864–870. doi: 10.1002/term.1478.
    1. Baglioni S., Cantini G., Poli G., et al. Functional differences in visceral and subcutaneous fat pads originate from differences in the adipose stem cell. PLoS ONE. 2012;7(5) doi: 10.1371/journal.pone.0036569.e36569
    1. Strem B. M., Hicok K. C., Zhu M., et al. Multipotential differentiation of adipose tissue-derived stem cells. Keio Journal of Medicine. 2005;54(3):132–141. doi: 10.2302/kjm.54.132.
    1. Aust L., Devlin B., Foster S. J., et al. Yield of human adipose-derived adult stem cells from liposuction aspirates. Cytotherapy. 2004;6(1):7–14. doi: 10.1080/14653240310004539.
    1. Jurgens W. J. F. M., Oedayrajsingh-Varma M. J., Helder M. N., et al. Effect of tissue-harvesting site on yield of stem cells derived from adipose tissue: implications for cell-based therapies. Cell and Tissue Research. 2008;332(3):415–426. doi: 10.1007/s00441-007-0555-7.
    1. Biedermann T., Boettcher-Haberzeth S., Reichmann E. Tissue engineering of skin for wound coverage. European Journal of Pediatric Surgery. 2013;23(5):375–382. doi: 10.1055/s-0033-1352529.
    1. Schiestl C., Stiefel D., Meuli M. Giant naevus, giant excision, eleg(i)ant closure? Reconstructive surgery with Integra Artificial Skin to treat giant congenital melanocytic naevi in children. Journal of Plastic, Reconstructive & Aesthetic Surgery. 2010;63(4):610–615.
    1. Böttcher-Haberzeth S., Biedermann T., Reichmann E. Tissue engineering of skin. Burns. 2010;36(4):450–460. doi: 10.1016/j.burns.2009.08.016.
    1. Pontiggia L., Biedermann T., Meuli M., et al. Markers to evaluate the quality and self-renewing potential of engineered human skin substitutes in vitro and after transplantation. Journal of Investigative Dermatology. 2009;129(2):480–490. doi: 10.1038/jid.2008.254.
    1. Biedermann T., Pontiggia L., Böttcher-Haberzeth S., et al. Human eccrine sweat gland cells can reconstitute a stratified epidermis. Journal of Investigative Dermatology. 2010;130(8):1996–2009. doi: 10.1038/jid.2010.83.
    1. Montaño I., Schiestl C., Schneider J., et al. Formation of human capillaries in vitro: the engineering of prevascularized matrices. Tissue Engineering Part A. 2010;16(1):269–282. doi: 10.1089/ten.tea.2008.0550.
    1. Marino D., Luginbühl J., Scola S., Meuli M., Reichmann E. Bioengineering dermo-epidermal skin grafts with blood and lymphatic capillaries. Science Translational Medicine. 2014;6(221) doi: 10.1126/scitranslmed.3006894.221ra14
    1. Mohd Hilmi A. B., Halim A. S. Vital roles of stem cells and biomaterials in skin tissue engineering. World Journal of Stem Cells. 2015;7(2):428–436. doi: 10.4252/wjsc.v7.i2.428.
    1. Trottier V., Marceau-Fortier G., Germain L., Vincent C., Fradette J. IFATS collection: using human adipose-derived stem/stromal cells for the production of new skin substitutes. STEM CELLS. 2008;26(10):2713–2723. doi: 10.1634/stemcells.2008-0031.
    1. Hata R.-I., Senoo H. L-ascorbic acid 2-phosphate stimulates collagen accumulation, cell proliferation, and formation of a three-dimensional tissuelike substance by skin fibroblasts. Journal of Cellular Physiology. 1989;138(1):8–16. doi: 10.1002/jcp.1041380103.
    1. Debels H., Hamdi M., Abberton K., Morrison W. Dermal matrices and bioengineered skin substitutes: a critical review of current options. Plastic and Reconstructive Surgery Global Open. 2015;3(1) doi: 10.1097/gox.0000000000000219.e284
    1. Chan R. K., Zamora D. O., Wrice N. L., et al. Development of a vascularized skin construct using adipose-derived stem cells from debrided burned skin. Stem Cells International. 2012;2012:11. doi: 10.1155/2012/841203.841203
    1. Monfort A., Soriano-Navarro M., García-Verdugo J. M., Izeta A. Production of human tissue-engineered skin trilayer on a plasma-based hypodermis. Journal of Tissue Engineering and Regenerative Medicine. 2013;7(6):479–490. doi: 10.1002/term.548.
    1. Kellar R., Diller R. B., Machula H., Muller J., Ensley B. Biomimetic skin substitutes created from tropoelastin help to promote wound healing. Frontiers in Bioengineering and Biotechnology. 2016 doi: 10.3389/conf.FBIOE.2016.01.00174.
    1. Rodrigues C., de Assis A. M., Moura D. J., et al. New therapy of skin repair combining adipose-derived mesenchymal stem cells with sodium carboxymethylcellulose scaffold in a pre-clinical rat model. PLoS ONE. 2014;9(5) doi: 10.1371/journal.pone.0096241.e96241
    1. Tabit C. J., Slack G. C., Fan K., Wan D. C., Bradley J. P. Fat grafting versus adipose-derived stem cell therapy: distinguishing indications, techniques, and outcomes. Aesthetic Plastic Surgery. 2012;36(3):704–713. doi: 10.1007/s00266-011-9835-4.
    1. Ross R. J., Shayan R., Mutimer K. L., Ashton M. W. Autologous fat grafting: current state of the art and critical review. Annals of Plastic Surgery. 2014;73(3):352–357. doi: 10.1097/sap.0b013e31827aeb51.
    1. Groen J. W., Negenborn V. L., Twisk D. J., et al. Autologous fat grafting in onco-plastic breast reconstruction: a systematic review on oncological and radiological safety, complications, volume retention and patient/surgeon satisfaction. Journal of Plastic, Reconstructive & Aesthetic Surgery. 2016;69(6):742–764. doi: 10.1016/j.bjps.2016.03.019.
    1. Negenborn V. L., Groen J.-W., Smit J. M., Niessen F. B., Mullender M. G. The use of autologous fat grafting for treatment of scar tissue and scar-related conditions: a systematic review. Plastic & Reconstructive Surgery. 2016;137(1):31e–43e. doi: 10.1097/prs.0000000000001850.
    1. Coleman S. R. Structural fat grafting: more than a permanent filler. Plastic and Reconstructive Surgery. 2006;118(3):108S–120S. doi: 10.1097/01.prs.0000234610.81672.e7.
    1. Nishimura T., Hashimoto H., Nakanishi I., Furukawa M. Microvascular angiogenesis and apoptosis in the survival of free fat grafts. Laryngoscope. 2000;110(8):1333–1338. doi: 10.1097/00005537-200008000-00021.
    1. Cherubino M., Marra K. G. Adipose-derived stem cells for soft tissue reconstruction. Regenerative Medicine. 2009;4(1):109–117. doi: 10.2217/17460751.4.1.109.
    1. Tremolada C., Palmieri G., Ricordi C. Adipocyte transplantation and stem cells: plastic surgery meets regenerative medicine. Cell Transplantation. 2010;19(10):1217–1223. doi: 10.3727/096368910x507187.
    1. Matsumoto D., Sato K., Gonda K., et al. Cell-assisted lipotransfer: supportive use of human adipose-derived cells for soft tissue augmentation with lipoinjection. Tissue Engineering. 2006;12(12):3375–3382. doi: 10.1089/ten.2006.12.3375.
    1. Nguyen A., Guo J., Banyard D. A., et al. Stromal vascular fraction: a regenerative reality? Part 1: current concepts and review of the literature. Journal of Plastic, Reconstructive & Aesthetic Surgery. 2016;69(2):170–179. doi: 10.1016/j.bjps.2015.10.015.
    1. Gir P., Oni G., Brown S. A., Mojallal A., Rohrich R. J. Human adipose stem cells: current clinical applications. Plastic & Reconstructive Surgery. 2012;129(6):1277–1290. doi: 10.1097/prs.0b013e31824ecae6.
    1. Mizuno H., Tobita M., Uysal A. C. Concise review: adipose-derived stem cells as a novel tool for future regenerative medicine. Stem Cells. 2012;30(5):804–810. doi: 10.1002/stem.1076.
    1. Shukla L., Morrison W. A., Shayan R. Adipose-derived stem cells in radiotherapy injury: a new frontier. Frontiers in Surgery. 2015;2, article 1 doi: 10.3389/fsurg.2015.00001.
    1. Condé-Green A., Marano A. A., Lee E. S., et al. Fat grafting and adipose-derived regenerative cells in burn wound healing and scarring: a systematic review of the literature. Plastic & Reconstructive Surgery. 2016;137(1):302–312. doi: 10.1097/prs.0000000000001918.
    1. Yuan Y., Gao J., Liu L., Lu F. Role of adipose-derived stem cells in enhancing angiogenesis early after aspirated fat transplantation: induction or differentiation? Cell Biology International. 2013;37(6):547–550. doi: 10.1002/cbin.10068.
    1. Yan A., Avraham T., Zampell J. C., Haviv Y. S., Weitman E., Mehrara B. J. Adipose-derived stem cells promote lymphangiogenesis in response to VEGF-C stimulation or TGF-β1 inhibition. Future Oncology. 2011;7(12):1457–1473. doi: 10.2217/fon.11.121.
    1. Matsuda K., Falkenberg K. J., Woods A. A., Choi Y. S., Morrison W. A., Dilley R. J. Adipose-derived stem cells promote angiogenesis and tissue formation for in vivo tissue engineering. Tissue Engineering Part A. 2013;19(11-12):1327–1335. doi: 10.1089/ten.tea.2012.0391.
    1. Kapur S. K., Katz A. J. Review of the adipose derived stem cell secretome. Biochimie. 2013;95(12):2222–2228. doi: 10.1016/j.biochi.2013.06.001.
    1. Kokai L. E., Marra K., Rubin J. P. Adipose stem cells: biology and clinical applications for tissue repair and regeneration. Translational Research. 2014;163(4):399–408. doi: 10.1016/j.trsl.2013.11.009.

Source: PubMed

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