Abstract
Studies on three-dimensional tissue engineered graft (3DTEG) have attracted great interest among researchers as they present a means to meet the pressing clinical demand for tissue engineering scaffolds. To explore the feasibility of 3DTEG, high porosity poly-ε-caprolactone (PCL) was obtained via the co-electrospinning of polyethylene glycol and PCL, and used to construct small-diameter poly-ε-caprolactone–lysine (PCL–LYS–H) scaffolds, whereby heparin was anchored to the scaffold surface by lysine groups. A variety of small-diameter 3DTEG models were constructed with different PCL layers and the mechanical properties of the resulting constructs were evaluated in order to select the best model for 3DTEGs. Bone marrow mononuclear cells were induced and differentiated to endothelial cells (ECs) and smooth muscle cells (SMCs). A 3DTEG (labeled ‘10-4 %’) was successfully produced by the dynamic co-culture of ECs on the PCL–LYS–H scaffolds and SMCs on PCL. The fluorescently labeled cells on the 3DTEG were subsequently observed by laser confocal microscopy, which showed that the ECs and SMCs were embedded in the 3DTEG. Nitric oxide and endothelial nitric oxide synthase assays showed that the ECs behaved normally in the 3DTEG. This study consequently provides a new thread to produce small-diameter tissue engineered grafts, with excellent mechanical properties, that are perfusable to vasculature and functional cells.
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Farber A, Major K, Wagner WH, Cohen JL, Cossman DV, Lauterbach SR, et al. Cryopreserved saphenous vein allografts in infrainguinal revascularization: analysis of 240 grafts. J Vasc Surg. 2003;38:15–21.
Veith FJ, Gupta SK, Ascer E, White-Flores S, Samson RH, Scher LA, et al. Six-year prospective multicenter randomized comparison of autologous saphenous vein and expanded polytetrafluoroethylene grafts in infrainguinal arterial reconstructions. J Vasc Surg. 1986;3:104–14.
Weinberg CB, Bell E. A blood vessel model constructed from collagen and cultured vascular cells. Science. 1986;231:397–400.
Zhang H, Wang ZG, Xia RY. Seeding of autogenous endothelial cells to the inner surface of small-caliber dacron vascular prostheses: an experimental study in dogs. Zhonghua Wai Ke Za Zhi. 1988;26(68–70):124.
Wang ZG, Du W, Li GD, Pu LQ, Sharefkin JB. Rapid cellular luminal coverage of Dacron inferior vena cava prostheses in dogs by immediate seeding of autogenous endothelial cells derived from omental tissue: results of a preliminary trial. J Vasc Surg. 1990;12:168–79.
Gui L, Niklason LE. Vascular tissue engineering: building perfusable vasculature for implantation. Curr Opin Chem Eng. 2014;3:68–74.
Dahl SL, Rhim C, Song YC, Niklason LE. Mechanical properties and compositions of tissue engineered and native arteries. Ann Biomed Eng. 2007;35:348–55.
L’Heureux N, Paquet S, Labbe R, Germain L, Auger FA. A completely biological tissue-engineered human blood vessel. Faseb J. 1998;12:47–56.
McAllister TN, Maruszewski M, Garrido SA, Wystrychowski W, Dusserre N, Marini A, et al. Effectiveness of haemodialysis access with an autologous tissue-engineered vascular graft: a multicentre cohort study. Lancet. 2009;373:1440–6.
Shin’Oka T, Imai Y, Ikada Y. Transplantation of a tissue-engineered pulmonary artery. N Engl J Med. 2001;344:532–3.
Roh JD, Sawh-Martinez R, Brennan MP, Jay SM, Devine L, Rao DA, et al. Tissue-engineered vascular grafts transform into mature blood vessels via an inflammation-mediated process of vascular remodeling. Proc Natl Acad Sci USA. 2010;107:4669–74.
Yuan B, Jin Y, Sun Y, Wang D, Sun J, Wang Z, et al. A strategy for depositing different types of cells in three dimensions to mimic tubular structures in tissues. Adv Mater. 2012;24:890–6.
Dawson AE, Norton JA, Weinberg DS. Comparative assessment of proliferation and DNA content in breast carcinoma by image analysis and flow cytometry. Am J Pathol. 1990;136:1115–24.
MacEachern KE, Smith GL, Nolan AM. Methods for the isolation, culture and characterisation of equine pulmonary artery endothelial cells. Res Vet Sci. 1997;62:147–52.
Gong C, Shi S, Dong P, Kan B, Gou M, Wang X, et al. Synthesis and characterization of PEG-PCL-PEG thermosensitive hydrogel. Int J Pharm. 2009;365:89–99.
Freed LE, Guilak F, Guo XE, Gray ML, Tranquillo R, Holmes JW, et al. Advanced tools for tissue engineering: scaffolds, bioreactors, and signaling. Tissue Eng. 2006;12:3285–305.
Yu L, Quinn DA, Garg HG, Hales CA. Heparin inhibits pulmonary artery smooth muscle cell proliferation through guanine nucleotide exchange factor-H1/RhoA/Rho kinase/p27. Am J Respir Cell Mol Biol. 2011;44:524–30.
Bhattarai SR, Bhattarai N, Viswanathamurthi P, Yi HK, Hwang PH, Kim HY. Hydrophilic nanofibrous structure of polylactide; fabrication and cell affinity. J Biomed Mater Res A. 2006;78:247–57.
Li CM, Dong JD, Gu YQ, Chen XB, Bian C, Wang ZG. Experimental studies on differentiation of cane bone marrow mesenchymal stem cells into vascular endothelial cells in vitro. Chin J Curr Adv Gen Surg. 2010;13:757–60.
Chen XS, Zhang J, Gu YQ, Li JX, Chen B, Cui YQ, et al. Cane bone marrow mononuclear cells differentiate into smooth muscle-like cells. CARTER. 2007;11:3876–81.
Wag YH, Chen GH. Stem cell transplantation therapy for angiocardiopathy: clinical progress in China. CARTER. 2007;11:4794–7.
Quirici N, Soligo D, Caneva L, Servida F, Bossolasco P, Deliliers GL. Differentiation and expansion of endothelial cells from human bone marrow CD133(+) cells. Br J Haematol. 2001;115:186–94.
Kaushal S, Amiel GE, Guleserian KJ, Shapira OM, Perry T, Sutherland FW, et al. Functional small-diameter neovessels created using endothelial progenitor cells expanded ex vivo. Nat Med. 2001;7:1035–40.
Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science. 1997;275:964–7.
Owens GK. Regulation of differentiation of vascular smooth muscle cells. Physiol Rev. 1995;75:487–517.
Kaushal S, Amiel GE, Guleserian KJ, Shapira OM, Perry T, Sutherland FW, et al. Functional small-diameter neovessels created using endothelial progenitor cells expanded ex vivo. Nat Med. 2001;7:1035–40.
Niklason LE, Gao J, Abbott WM, Hirschi KK, Houser S, Marini R, et al. Functional arteries grown in vitro. Science. 1999;284:489–93.
Quint C, Kondo Y, Manson RJ, Lawson JH, Dardik A, Niklason LE. Decellularized tissue-engineered blood vessel as an arterial conduit. Proc Natl Acad Sci USA. 2011;108:9214–9.
Niklason LE, Gao J, Abbott WM, Hirschi KK, Houser S, Marini R, et al. Functional arteries grown in vitro. Science. 1999;284:489–93.
Kaushal S, Amiel GE, Guleserian KJ, Shapira OM, Perry T, Sutherland FW, et al. Functional small-diameter neovessels created using endothelial progenitor cells expanded ex vivo. Nat Med. 2001;7:1035–40.
Quint C, Kondo Y, Manson RJ, Lawson JH, Dardik A, Niklason LE. Decellularized tissue-engineered blood vessel as an arterial conduit. Proc Natl Acad Sci USA. 2011;108:9214–9.
McCormick SM, Eskin SG, McIntire LV, Teng CL, Lu CM, Russell CG, et al. DNA microarray reveals changes in gene expression of shear stressed human umbilical vein endothelial cells. Proc Natl Acad Sci USA. 2001;98:8955–60.
Sakamoto N, Kiuchi T, Sato M. Development of an endothelial-smooth muscle cell coculture model using phenotype-controlled smooth muscle cells. Ann Biomed Eng. 2011;39:2750–8.
Ning H, Lin G, Lue TF, Lin CS. A coculture system of cavernous endothelial and smooth muscle cells. Int J Impot Res. 2013;25:63–8.
Di Luozzo G, Bhargava J, Powell RJ. Vascular smooth muscle cell effect on endothelial cell endothelin-1 production. J Vasc Surg. 2000;31:781–9.
Lu MH, Chao CF, Huang CG, Chang LT. Coculture of vascular endothelial cells and smooth muscle cells from spontaneously hypertensive rats. Clin Exp Hypertens. 2003;25:413–25.
Wen SJ, Zhao LM, Li P, Li JW, Liu Y, Liu JL, Chen YC. Blood vessel tissue engineering seeding vascular smooth muscle cells and endothelial cells sequentially on biodegradable scaffold in vitro. Natl Med J China. 2005;85:816–8.
Wallace CS, Champion JC, Truskey GA. Adhesion and function of human endothelial cells co-cultured on smooth muscle cells. Ann Biomed Eng. 2007;35:375–86.
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This work was supported by the National High Technology Research and Development Program of China (2011AA020507). We declare no bias toward any institute who supported this study.
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The authors declare that they have no potential conflicts of interest.
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Zhu, GC., Gu, YQ., Geng, X. et al. Experimental study on the construction of small three-dimensional tissue engineered grafts of electrospun poly-ε-caprolactone. J Mater Sci: Mater Med 26, 112 (2015). https://doi.org/10.1007/s10856-015-5448-9
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DOI: https://doi.org/10.1007/s10856-015-5448-9