2,594
Views
97
CrossRef citations to date
0
Altmetric
Review Article

Current and emerging vascularization strategies in skin tissue engineering

, , , &
Pages 613-625 | Received 22 Feb 2016, Accepted 22 Jun 2016, Published online: 20 Jul 2016

References

  • Pham C, Greenwood J, Cleland H, et al. Bioengineered skin substitutes for the management of burns: a systematic review. Burns. 2007;33:946–957.
  • Böttcher-Haberzeth S, Biedermann T, Reichmann E. Tissue engineering of skin. Burns. 2010;36:450–460.
  • Akhtar S, Hasham S, Abela C, et al. The use of Integra in necrotizing fasciitis. Burns. 2006;32:251–254.
  • Weigert R, Choughri H, Casoli V. Management of severe hand wounds with Integra® dermal regeneration template. J Hand Surg Eur Vol. 2011;36:185–193.
  • Graham GP, Helmer SD, Haan JM, et al. The use of Integra® Dermal Regeneration Template in the reconstruction of traumatic degloving injuries. J Burn Care Res. 2013;34:261–266.
  • Tufaro AP, Buck DW II, Fischer AC. The use of artificial dermis in the reconstruction of oncologic surgical defects. Plast Reconstr Surg. 2007;120:638–646.
  • Shevchenko RV, James SL, James SE. A review of tissue-engineered skin bioconstructs available for skin reconstruction. J R Soc Interface. 2010;7:229–258.
  • Boyce ST. Design principles for composition and performance of cultured skin substitutes. Burns. 2001;27:523–533.
  • Kamel RA, Ong JF, Eriksson E, et al. Tissue engineering of skin. J Am Coll Surg. 2013;217:533–555.
  • MacNeil S. Progress and opportunities for tissue-engineered skin. Nature. 2007;445:874–880.
  • Hosper NA, Eggink AJ, Roelofs LA, et al. Intra-uterine tissue engineering of full-thickness skin defects in a fetal sheep model. Biomaterials. 2010;31:3910–3919.
  • Li X, Xu G, Chen J. Tissue engineered skin for diabetic foot ulcers: a meta-analysis. Int J Clin Exp Med. 2015a;8:18191–18196.
  • Sahota PS, Burn JL, Heaton M, et al. Development of a reconstructed human skin model for angiogenesis. Wound Repair Regen. 2003;11:275–284.
  • Hendrickx B, Vranckx JJ, Luttun A. Cell-based vascularization strategies for skin tissue engineering. Tissue Eng Part B: Rev. 2011;17:13–24.
  • Papavasiliou G, Cheng MH, Brey EM. Strategies for vascularization of polymer scaffolds. J Investig Med. 2010;58:838–844.
  • Laschke MW, Menger MD. Prevascularization in tissue engineering: current concepts and future directions. Biotechnol Adv. 2016;34:112–121.
  • Laschke MW, Harder Y, Amon M, et al. Angiogenesis in tissue engineering: breathing life into constructed tissue substitutes. Tissue Eng. 2006;12:2093–2104.
  • Utzinger U, Baggett B, Weiss JA, et al. Large-scale time series microscopy of neovessel growth during angiogenesis. Angiogenesis. 2015;18:219–232.
  • Laschke MW, Vollmar B, Menger MD. Inosculation: connecting the life-sustaining pipelines. Tissue Eng Part B: Rev. 2009;15:455–465.
  • Laschke MW, Menger MD. Vascularization in tissue engineering: angiogenesis versus inosculation. Eur Surg Res. 2012;48:85–92.
  • Laschke MW, Menger MD. Adipose tissue-derived microvascular fragments: natural vascularization units for regenerative medicine. Trends Biotechnol. 2015;33:442–448.
  • Koch L, Deiwick A, Schlie S, et al. Skin tissue generation by laser cell printing. Biotechnol Bioeng. 2012;109:1855–1863.
  • Hasan A, Paul A, Vrana NE, et al. Microfluidic techniques for development of 3D vascularized tissue. Biomaterials. 2014;35:7308–7325.
  • Miller KJ, Brown DA, Ibrahim MM, et al. MicroRNAs in skin tissue engineering. Adv Drug Deliv Rev. 2015;88:16–36.
  • Cerqueira MT, Pirraco RP, Santos TC, et al. Human adipose stem cells cell sheet constructs impact epidermal morphogenesis in full-thickness excisional wounds. Biomacromolecules. 2013;14:3997–4008.
  • Hopfner U, Schenck TL, Chávez MN, et al. Development of photosynthetic biomaterials for in vitro tissue engineering. Acta Biomater. 2014;10:2712–2717.
  • Choi SW, Zhang Y, Macewan MR, et al. Neovascularization in biodegradable inverse opal scaffolds with uniform and precisely controlled pore sizes. Adv Healthc Mater. 2013;2:145–154.
  • Yannas IV, Burke JF. Design of an artificial skin. I. Basic design principles. J Biomed Mater Res. 1980;14:65–81.
  • Burke JF, Yannas IV, Quinby WC Jr, et al. Successful use of a physiologically acceptable artificial skin in the treatment of extensive burn injury. Ann Surg. 1981;194:413–428.
  • Debels H, Hamdi M, Abberton K, et al. Dermal matrices and bioengineered skin substitutes: a critical review of current options. Plast Reconstr Surg Glob Open. 2015;3:e284.
  • De Vries HJ, Zeegelaar JE, Middelkoop E, et al. Reduced wound contraction and scar formation in punch biopsy wounds. Native collagen dermal substitutes. A clinical study. Br J Dermatol. 1995;132:690–697.
  • van Zuijlen PP, Vloemans JF, van Trier AJ, et al. Dermal substitution in acute burns and reconstructive surgery: a subjective and objective long-term follow-up. Plast Reconstr Surg. 2001;108:1938–1946.
  • Schneider J, Biedermann T, Widmer D, et al. Matriderm versus Integra: a comparative experimental study. Burns. 2009;35:51–57.
  • Bai F, Wang Z, Lu J, et al. The correlation between the internal structure and vascularization of controllable porous bioceramic materials in vivo: a quantitative study. Tissue Eng Part A. 2010;16:3791–3803.
  • Xiao X, Wang W, Liu D, et al. The promotion of angiogenesis induced by three-dimensional porous beta-tricalcium phosphate scaffold with different interconnection sizes via activation of PI3K/Akt pathways. Sci Rep. 2015;5:9409.
  • Lin J, Lindsey ML, Zhu B, et al. Effects of surface-modified scaffolds on the growth and differentiation of mouse adipose-derived stromal cells. J Tissue Eng Regen Med. 2007;1:211–217.
  • Ring A, Tilkorn DJ, Goertz O, et al. Surface modification by glow discharge gasplasma treatment improves vascularization of allogenic bone implants. J Orthop Res. 2011;29:1237–1244.
  • Griffin MF, Palgrave RG, Seifalian AM, et al. Enhancing tissue integration and angiogenesis of a novel nanocomposite polymer using plasma surface polymerisation, an in vitro and in vivo study. Biomater Sci. 2015a;4:145–158.
  • Ring A, Langer S, Schaffran A, et al. Enhanced neovascularization of dermis substitutes via low-pressure plasma-mediated surface activation. Burns. 2010;36:1222–1227.
  • Scherer SS, Pietramaggiori G, Matthews J, et al. Poly-N-acetyl glucosamine nanofibers: a new bioactive material to enhance diabetic wound healing by cell migration and angiogenesis. Ann Surg. 2009;250:322–330.
  • Zhao S, Li L, Wang H, et al. Wound dressings composed of copper-doped borate bioactive glass microfibers stimulate angiogenesis and heal full-thickness skin defects in a rodent model. Biomaterials. 2015;53:379–391.
  • Wang X, You C, Hu X, et al. The roles of knitted mesh-reinforced collagen-chitosan hybrid scaffold in the one-step repair of full-thickness skin defects in rats. Acta Biomater. 2013;9:7822–7832.
  • Boucard N, Viton C, Agay D, et al. The use of physical hydrogels of chitosan for skin regeneration following third-degree burns. Biomaterials. 2007;28:3478–3488.
  • Zeng Y, Zhu L, Han Q, et al. Preformed gelatin microcryogels as injectable cell carriers for enhanced skin wound healing. Acta Biomater. 2015;25:291–303.
  • Huang X, Zhang Y, Zhang X, et al. Influence of radiation crosslinked carboxymethyl-chitosan/gelatin hydrogel on cutaneous wound healing. Mater Sci Eng C: Mater Biol Appl. 2013;33:4816–4824.
  • Wong VW, Rustad KC, Galvez MG, et al. Engineered pullulan–collagen composite dermal hydrogels improve early cutaneous wound healing. Tissue Eng Part A. 2011;17:631–644.
  • Shen YI, Song HH, Papa AE, et al. Acellular hydrogels for regenerative burn wound healing: translation from a porcine model. J Invest Dermatol. 2015;135:2519–2529.
  • Sun G, Zhang X, Shen YI, et al. Dextran hydrogel scaffolds enhance angiogenic responses and promote complete skin regeneration during burn wound healing. Proc Natl Acad Sci USA. 2011;108:20976–20981.
  • Langer R. Drug delivery and targeting. Nature. 1998;392:5–10.
  • Li W, Lan Y, Guo R, et al. In vitro and in vivo evaluation of a novel collagen/cellulose nanocrystals scaffold for achieving the sustained release of basic fibroblast growth factor. J Biomater Appl. 2015b;29:882–893.
  • Cao H, Chen MM, Liu Y, et al. Fish collagen-based scaffold containing PLGA microspheres for controlled growth factor delivery in skin tissue engineering. Colloids Surf B: Biointerfaces. 2015;136:1098–1106.
  • Wang F, Wang M, She Z, et al. Collagen/chitosan based two-compartment and bi-functional dermal scaffolds for skin regeneration. Mater Sci Eng C: Mater Biol Appl. 2015;52:155–162.
  • Liu Q, Huang Y, Lan Y, et al. Acceleration of skin regeneration in full-thickness burns by incorporation of bFGF-loaded alginate microspheres into a CMCS-PVA hydrogel. J Tissue Eng Regen Med. 2015; in press. doi:10.1002/term.2057.
  • Cam C, Zhu S, Truong NF, et al. Systematic evaluation of natural scaffolds in cutaneous wound healing. J Mater Chem B: Mater Biol Med. 2015;3:7986–7992.
  • Wilcke I, Lohmeyer JA, Liu S, et al. VEGF(165) and bFGF protein-based therapy in a slow release system to improve angiogenesis in a bioartificial dermal substitute in vitro and in vivo. Langenbecks Arch Surg. 2007;392:305–314.
  • Margolis DJ, Cromblehome T, Herlyn M, et al. Clinical protocol. Phase I trial to evaluate the safety of H5.020CMV.PDGF-b and limb compression bandage for the treatment of venous leg ulcer: trial A. Hum Gene Ther. 2004;15:1003–1019.
  • Mulder G, Tallis AJ, Marshall VT, et al. Treatment of nonhealing diabetic foot ulcers with a platelet-derived growth factor gene-activated matrix (GAM501): results of a phase 1/2 trial. Wound Repair Regen. 2009;17:772–779.
  • Ledley FD. Pharmaceutical approach to somatic gene therapy. Pharm Res. 1996;13:1595–1614.
  • Bleiziffer O, Eriksson E, Yao F, et al. Gene transfer strategies in tissue engineering. J Cell Mol Med. 2007;11:206–223.
  • Shapiro Ledley T, Ledley FD. Pharmacokinetic considerations in somatic gene therapy. Adv Drug Deliv Rev. 1998;30:133–150.
  • Shea LD, Smiley E, Bonadio J, et al. DNA delivery from polymer matrices for tissue engineering. Nat Biotechnol. 1999;17:551–554.
  • Kolk A, Haczek C, Koch C, et al. A strategy to establish a gene-activated matrix on titanium using gene vectors protected in a polylactide coating. Biomaterials. 2011;32:6850–6859.
  • Guo R, Xu S, Ma L, et al. Enhanced angiogenesis of gene-activated dermal equivalent for treatment of full thickness incisional wounds in a porcine model. Biomaterials. 2010;31:7308–7320.
  • Guo R, Xu S, Ma L, et al. The healing of full-thickness burns treated by using plasmid DNA encoding VEGF-165 activated collagen–chitosan dermal equivalents. Biomaterials. 2011;32:1019–1031.
  • Yang Y, Xia T, Chen F, et al. Electrospun fibers with plasmid bFGF polyplex loadings promote skin wound healing in diabetic rats. Mol Pharm. 2012;9:48–58.
  • Reckhenrich AK, Hopfner U, Krötz F, et al. Bioactivation of dermal scaffolds with a non-viral copolymer-protected gene vector. Biomaterials. 2011;32:1996–2003.
  • Black AF, Berthod F, L'heureux N, et al. In vitro reconstruction of a human capillary-like network in a tissue-engineered skin equivalent. Faseb J. 1998;12:1331–1340.
  • Supp DM, Wilson-Landy K, Boyce ST. Human dermal microvascular endothelial cells form vascular analogs in cultured skin substitutes after grafting to athymic mice. FASEB J. 2002;16:797–804.
  • Tremblay PL, Hudon V, Berthod F, et al. Inosculation of tissue-engineered capillaries with the host's vasculature in a reconstructed skin transplanted on mice. Am J Transplant. 2005;5:1002–1010.
  • Montaño I, Schiestl C, Schneider J, et al. Formation of human capillaries in vitro: the engineering of prevascularized matrices. Tissue Eng Part A. 2010;16:269–282.
  • Schechner JS, Nath AK, Zheng L, et al. In vivo formation of complex microvessels lined by human endothelial cells in an immunodeficient mouse. Proc Natl Acad Sci USA. 2000;97:9191–9196.
  • Koike N, Fukumura D, Gralla O, et al. Tissue engineering: creation of long-lasting blood vessels. Nature. 2004;428:138–139.
  • Kim KL, Song SH, Choi KS, et al. Cooperation of endothelial and smooth muscle cells derived from human induced pluripotent stem cells enhances neovascularization in dermal wounds. Tissue Eng Part A. 2013;19:2478–2485.
  • Foubert P, Matrone G, Souttou B, et al. Coadministration of endothelial and smooth muscle progenitor cells enhances the efficiency of proangiogenic cell-based therapy. Circ Res. 2008;103:751–760.
  • Athanassopoulos A, Tsaknakis G, Newey SE, et al. Microvessel networks [corrected] pre-formed in artificial clinical grade dermal substitutes in vitro using cells from haematopoietic tissues. Burns. 2012;38:691–701.
  • Hanjaya-Putra D, Shen YI, Wilson A, et al. Integration and regression of implanted engineered human vascular networks during deep wound healing. Stem Cells Transl Med. 2013;2:297–306.
  • Shepherd BR, Enis DR, Wang F, et al. Vascularization and engraftment of a human skin substitute using circulating progenitor cell-derived endothelial cells. FASEB J. 2006;20:1739–1741.
  • Rehman J, Li J, Orschell CM, et al. Peripheral blood “endothelial progenitor cells” are derived from monocyte/macrophages and secrete angiogenic growth factors. Circulation. 2003;107:1164–1169.
  • Hirschi KK, Ingram DA, Yoder MC. Assessing identity, phenotype, and fate of endothelial progenitor cells. Arterioscler Thromb Vasc Biol. 2008;28:1584–1595.
  • Zhang Z, Ito WD, Hopfner U, et al. The role of single cell derived vascular resident endothelial progenitor cells in the enhancement of vascularization in scaffold-based skin regeneration. Biomaterials. 2011;32:4109–4117.
  • Laschke MW, Giebels C, Menger MD. Vasculogenesis: a new piece of the endometriosis puzzle. Hum Reprod Update. 2011;17:628–636.
  • Suh W, Kim KL, Kim JM, et al. Transplantation of endothelial progenitor cells accelerates dermal wound healing with increased recruitment of monocytes/macrophages and neovascularization. Stem Cells. 2005;23:1571–1578.
  • Hendrickx B, Verdonck K, Van den Berge S, et al. Integration of blood outgrowth endothelial cells in dermal fibroblast sheets promotes full thickness wound healing. Stem Cells. 2010;28:1165–1177.
  • Hassan WU, Greiser U, Wang W. Role of adipose-derived stem cells in wound healing. Wound Repair Regen. 2014;22:313–325.
  • Schumann P, Tavassol F, Lindhorst D, et al. Consequences of seeded cell type on vascularization of tissue engineering constructs in vivo. Microvasc Res. 2009;78:180–190.
  • Laschke MW, Schank TE, Scheuer C, et al. Three-dimensional spheroids of adipose-derived mesenchymal stem cells are potent initiators of blood vessel formation in porous polyurethane scaffolds. Acta Biomater. 2013;9:6876–6884.
  • Laschke MW, Schank TE, Scheuer C, et al. In vitro osteogenic differentiation of adipose-derived mesenchymal stem cell spheroids impairs their in vivo vascularization capacity inside implanted porous polyurethane scaffolds. Acta Biomater. 2014;10:4226–4235.
  • Liu S, Zhang H, Zhang X, et al. Synergistic angiogenesis promoting effects of extracellular matrix scaffolds and adipose-derived stem cells during wound repair. Tissue Eng Part A. 2011;17:725–739.
  • Meruane MA, Rojas M, Marcelain K. The use of adipose tissue-derived stem cells within a dermal substitute improves skin regeneration by increasing neoangiogenesis and collagen synthesis. Plast Reconstr Surg. 2012;130:53–63.
  • Zamora DO, Natesan S, Becerra S, et al. Enhanced wound vascularization using a dsASCs seeded FPEG scaffold. Angiogenesis. 2013;16:745–757.
  • Cerqueira MT, da Silva LP, Santos TC, et al. Gellan gum-hyaluronic acid spongy-like hydrogels and cells from adipose tissue synergize promoting neoskin vascularization. ACS Appl Mater Interfaces. 2014;6:19668–19679.
  • Klar AS, Güven S, Biedermann T, et al. Tissue-engineered dermo-epidermal skin grafts prevascularized with adipose-derived cells. Biomaterials. 2014;35:5065–5078.
  • Foubert P, Barillas S, Gonzalez AD, et al. Uncultured adipose-derived regenerative cells (ADRCs) seeded in collagen scaffold improves dermal regeneration, enhancing early vascularization and structural organization following thermal burns. Burns. 2015;41:1504–1516.
  • Nie C, Zhang G, Yang D, et al. Targeted delivery of adipose-derived stem cells via acellular dermal matrix enhances wound repair in diabetic rats. J Tissue Eng Regen Med. 2015;9:224–235.
  • Zonari A, Martins TM, Paula AC, et al. Polyhydroxybutyrate-co-hydroxyvalerate structures loaded with adipose stem cells promote skin healing with reduced scarring. Acta Biomater. 2015;17:170–181.
  • Markowicz M, Koellensperger E, Neuss S, et al. Human bone marrow mesenchymal stem cells seeded on modified collagen improved dermal regeneration in vivo. Cell Transplant. 2006;15:723–732.
  • Liu P, Deng Z, Han S, et al. Tissue-engineered skin containing mesenchymal stem cells improves burn wounds. Artif Organs. 2008;32:925–931.
  • Formigli L, Paternostro F, Tani A, et al. MSCs seeded on bioengineered scaffolds improve skin wound healing in rats. Wound Repair Regen. 2015;23:115–123.
  • Li Z, Wang H, Yang B, et al. Three-dimensional graphene foams loaded with bone marrow derived mesenchymal stem cells promote skin wound healing with reduced scarring. Mater Sci Eng C: Mater Biol Appl. 2015c;57:181–188.
  • Edwards SS, Zavala G, Prieto CP, et al. Functional analysis reveals angiogenic potential of human mesenchymal stem cells from Wharton's jelly in dermal regeneration. Angiogenesis 2014;17:851–866.
  • Danner S, Kremer M, Petschnik AE, et al. The use of human sweat gland-derived stem cells for enhancing vascularization during dermal regeneration. J Invest Dermatol. 2012;132:1707–1716.
  • Egaña JT, Danner S, Kremer M, et al. The use of glandular-derived stem cells to improve vascularization in scaffold-mediated dermal regeneration. Biomaterials. 2009;30:5918–5926.
  • Salem H, Ciba P, Rapoport DH, et al. The influence of pancreas-derived stem cells on scaffold based skin regeneration. Biomaterials. 2009;30:789–796.
  • Klar AS, Güven S, Zimoch J, et al. Characterization of vasculogenic potential of human adipose-derived endothelial cells in a three-dimensional vascularized skin substitute. Pediatr Surg Int. 2016;32:17–27.
  • Yoshikawa T, Mitsuno H, Nonaka I, et al. Wound therapy by marrow mesenchymal cell transplantation. Plast Reconstr Surg. 2008;121:860–877.
  • Markeson D, Pleat JM, Sharpe JR, et al. Scarring, stem cells, scaffolds and skin repair. J Tissue Eng Regen Med. 2015;9:649–668.
  • Fierro FA, O'Neal AJ, Beegle JR, et al. Hypoxic pre-conditioning increases the infiltration of endothelial cells into scaffolds for dermal regeneration pre-seeded with mesenchymal stem cells. Front Cell Dev Biol. 2015;3:68.
  • Han Y, Tao R, Han Y, et al. Microencapsulated VEGF gene-modified umbilical cord mesenchymal stromal cells promote the vascularization of tissue-engineered dermis: an experimental study. Cytotherapy. 2014;16:160–169.
  • Quan R, Zheng X, Xu S, et al. Gelatin-chondroitin-6-sulfate-hyaluronic acid scaffold seeded with vascular endothelial growth factor 165 modified hair follicle stem cells as a three-dimensional skin substitute. Stem Cell Res Ther. 2014;5:118.
  • Pilia M, McDaniel JS, Guda T, et al. Transplantation and perfusion of microvascular fragments in a rodent model of volumetric muscle loss injury. Eur Cell Mater. 2014;28:11–23.
  • Laschke MW, Kleer S, Scheuer C, et al. Vascularisation of porous scaffolds is improved by incorporation of adipose tissue-derived microvascular fragments. Eur Cell Mater. 2012;24:266–277.
  • McDaniel JS, Pilia M, Ward CL, et al. Characterization and multilineage potential of cells derived from isolated microvascular fragments. J Surg Res. 2014;192:214–222.
  • Laschke MW, Grässer C, Kleer S, et al. Adipose tissue-derived microvascular fragments from aged donors exhibit an impaired vascularisation capacity. Eur Cell Mater. 2014;28:287–298.
  • Laschke MW, Kleer S, Scheuer C, et al. Pre-cultivation of adipose tissue-derived microvascular fragments in porous scaffolds does not improve their in vivo vascularisation potential. Eur Cell Mater. 2015;29:190–200.
  • Nakano M, Nakajima Y, Kudo S, et al. Effect of autotransplantation of microvessel fragments on experimental random-pattern flaps in the rat. Eur Surg Res. 1998;30:149–160.
  • Nakano M, Nakajima Y, Kudo S, et al. Successful autotransplantation of microvessel fragments into the rat heart. Eur Surg Res. 1999;31:240–248.
  • Hiscox AM, Stone AL, Limesand S, et al. An islet-stabilizing implant constructed using a preformed vasculature. Tissue Eng Part A. 2008;14:433–440.
  • Paulsen SJ, Miller JS. Tissue vascularization through 3D printing: will technology bring us flow? Dev Dyn. 2015;244:629–640.
  • Lee V, Singh G, Trasatti JP, et al. Design and fabrication of human skin by three-dimensional bioprinting. Tissue Eng Part C: Methods. 2014;20:473–484.
  • Wong KH, Chan JM, Kamm RD, et al. Microfluidic models of vascular functions. Annu Rev Biomed Eng. 2012;14:205–230.
  • Skardal A, Mack D, Kapetanovic E, et al. Bioprinted amniotic fluid-derived stem cells accelerate healing of large skin wounds. Stem Cells Transl Med. 2012;1:792–802.
  • Michael S, Sorg H, Peck CT, et al. Tissue engineered skin substitutes created by laser-assisted bioprinting form skin-like structures in the dorsal skin fold chamber in mice. PLoS One. 2013;8:e57741.
  • Griffin DR, Weaver WM, Scumpia PO, D, et al. Accelerated wound healing by injectable microporous gel scaffolds assembled from annealed building blocks. Nat Mater. 2015;14:737–744.
  • Sen CK. MicroRNAs as new maestro conducting the expanding symphony orchestra of regenerative and reparative medicine. Physiol Genomics. 2011;43:517–520.
  • Anand S. A brief primer on microRNAs and their roles in angiogenesis. Vasc Cell. 2013;5:2.
  • Fish JE, Santoro MM, Morton SU, et al. miR-126 regulates angiogenic signaling and vascular integrity. Dev Cell. 2008;15:272–284.
  • Harris TA, Yamakuchi M, Ferlito M, et al. MicroRNA-126 regulates endothelial expression of vascular cell adhesion molecule 1. Proc Natl Acad Sci USA. 2008;105:1516–1521.
  • Wang S, Aurora AB, Johnson BA, et al. The endothelial-specific microRNA miR-126 governs vascular integrity and angiogenesis. Dev Cell. 2008;15:261–271.
  • Devalliere J, Chang WG, Andrejecsk JW, et al. Sustained delivery of proangiogenic microRNA-132 by nanoparticle transfection improves endothelial cell transplantation. FASEB J. 2014;28:908–922.
  • Okano T, Yamada N, Okuhara M, et al. Mechanism of cell detachment from temperature-modulated, hydrophilic–hydrophobic polymer surfaces. Biomaterials. 1995;16:297–303.
  • Tang Z, Okano T. Recent development of temperature-responsive surfaces and their application for cell sheet engineering. Regen Biomater. 2014;1:91–102.
  • Yu H, Peng J, Xu Y, et al. Bioglass activated skin tissue engineering constructs for wound healing. ACS Appl Mater Interfaces. 2016;8:703–715.
  • Sakaguchi K, Shimizu T, Okano T. Construction of three-dimensional vascularized cardiac tissue with cell sheet engineering. J Control Release. 2015;205:83–88.
  • Cerqueira MT, Pirraco RP, Martins AR, et al. Cell sheet technology-driven re-epithelialization and neovascularization of skin wounds. Acta Biomater. 2014;10:3145–3155.
  • Schenck TL, Hopfner U, Chávez MN, et al. Photosynthetic biomaterials: a pathway towards autotrophic tissue engineering. Acta Biomater. 2015;15:39–47.
  • Chávez MN, Schenck TL, Hopfner U, et al. Towards autotrophic tissue engineering: Photosynthetic gene therapy for regeneration. Biomaterials. 2016;75:25–36.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.