Abstract
Loss of function of large tissues is an urgent clinical problem. Although the artificial microfluidic network fabricated in large tissue- engineered constructs has great promise, it is still difficult to develop an efficient vessel-like design to meet the requirements of the biomimetic vascular network for tissue engineering applications. In this study, we used a facile approach to fabricate a branched and multi-level vessel-like network in a large muscle scaffolds by combining stereolithography (SL) technology and enzymatic crosslinking mechanism. The morphology of microchannel cross-sections was characterized using micro-computed tomography. The square cross-sections were gradually changed to a seamless circular microfluidic network, which is similar to the natural blood vessel. In the different micro-channels, the velocity greatly affected the attachment and spread of Human Umbilical Vein Endothelial Cell (HUVEC)-Green Fluorescent Protein (GFP). Our study demonstrated that the branched and multi-level microchannel network simulates biomimetic microenvironments to promote endothelialization. The gelatin scaffolds in the circular vessel-like networks will likely support myoblast and surrounding tissue for clinical use.
Similar content being viewed by others
References
Hurd S, Bhati N, Walker A, Kasukonis B, Wolchok J C. Development of a biological scaffold engineered using the extracellular matrix secreted by skeletal muscle cells. Biomaterials, 2015, 49, 9–17.
Valentin J E, Freytes D O, Grasman J M, Pesyna C, Freund J, Gilbert T W, Badylak S F. Oxygen diffusivity of biologic and synthetic scaffold materials for tissue engineering. Journal of Biomedical Materials Research Part A, 2009, 91, 1010–1017.
Mandru M, Ionescu C, Chirita M. Modelling mechanical properties in native and biomimetically formed vascular grafts. Journal of Bionic Engineering, 2009, 6, 371–377.
Cokelet G R, Soave R, Pugh G, Rathbun L. Fabrication of in vitro microvascular blood flow systems by photolithography. Microvascular Research, 1993, 46, 394–400.
He J K, Chen R M, Lu Y J, Zhan L, Liu Y X, Jin Z M. Fabrication of circular microfluidic network in enzymatically- crosslinked gelatin hydrogel. Materials Science & Engineering C-Materials for Biological Applications, 2016, 59, 53–60.
Choi J S, Piao Y, Seo T S. Fabrication of a circular PDMS microchannel for constructing a three-dimensional endothelial cell layer. Bioprocess and Biosystems Engineering, 2013, 36, 1871–1878.
Choi J S, Piao Y, Seo T S. Circumferential alignment of vascular smooth muscle cells in a circular microfluidic channel. Biomaterials, 2014, 35, 63–70.
Huang Z C, Li X, Martinsgreen M M, Liu Y X. Microfabrication of cylindrical microfluidic channel networks for microvascular research. Biomedical Microdevices, 2012, 14, 873–883.
Wong C C, Agarwal A, Balasubramanian N, Kwong D L. Fabrication of self-sealed circular nano/microfluidic channels in glass substrates. Nanotechnology, 2007, 18, 135304.
Jana S, Leung M, Chang J L, Zhang M Q. Effect of nanoand micro-scale topological features on alignment of muscle cells and commitment of myogenic differentiation. Biofabrication, 2014, 6, 035012.
Chen S W, Nakamoto T, Kawazoe N, Chen G P. Engineering multi-layered skeletal muscle tissue by using 3D microgrooved collagen scaffolds. Biomaterials, 2015, 73, 23–31.
Hosseini V, Kollmannsberger P, Ahadian S, Ostrovidov S, Kaji H, Vogel V, Khademhosseini A. Fiber-assisted molding (FAM) of surfaces with tunable curvature to guide cell alignment and complex tissue architecture. Small, 2014, 10, 4851–4857.
Fiddes L K, Raz N, Srigunapalan S, Tumarkan E, Simmons C A, Wheeler A R, Kumacheva E. A circular cross-section PDMS microfluidics system for replication of cardiovascular flow conditions. Biomaterials, 2010, 31, 3459–3464.
Kolesky D B, Truby R L, Gladman A S, Busbee T A, Homan K A, Lewis J A. 3D bioprinting of vascularized, heterogeneous cell-laden tissue constructs. Advanced materials, 2014, 26, 3124–3130.
Kubis H P, Scheibe R J, Decker B, Hufendiek K, Hanke N, Gros G, Meissner J D. Primary skeletal muscle cells cultured on gelatin bead microcarriers develop structural and biochemical features characteristic of adult skeletal muscle. Cell Biology International, 2016, 40, 364–374.
Baniasadi H, Mashayekhan S, Fadaoddini S, Haghirsharifzamini Y. Design, fabrication and characterization of oxidized alginate-gelatin hydrogels for muscle tissue engineering applications. Journal of Biomaterials Applications, 2016, 31, 152–161.
Hajiabbas M, Mashayekhan S, Nazaripouya A, Naji M, Hunkeler D, Zeleti S R, Sharifiaghdas F. Chitosan-gelatin sheets as scaffolds for muscle tissue engineering. Artificial Cells, Nanomedicine, and Biotechnology, 2015, 43, 124–132.
Dong G R, Lian Q, Yang L X, Mao W, Liu S Y, Xu C. Design and fabrication of vascular network for muscle tissue engineering. Advances in Engineering Research, 2016, 75, 613–621.
Murray C D. The physiological principle of minimum work: I. The vascular system and the cost of blood volume. Proceedings of the National Academy of Sciences, 1926, 12, 207–214.
Zamir M. Optimality principles in arterial branching. Journal of Theoretical Biology, 1976, 62, 227–251.
Kroll M H, Hellums J D, Mcintire L V, Schafer A I, Moake J L. Platelets and shear stress. Blood, 1996, 88, 1525–1541.
Lowe G D O. Virchow’s triad revisited: Abnormal flow. Pathophysiol Haemost Thromb, 2003, 33, 455–457.
Hoganson D M, Pryor H I, Spool I D, Burns O H, Gilmore J R, Vacanti J P. Principles of biomimetic vascular network design applied to a tissue-engineered liver scaffold. Tissue Engineering Part A, 2010, 16, 1469–1477.
Camp J P, Shuler S M L. Fabrication of a multiple-diameter branched network of microvascular channels with semicircular cross-sections using xenon difluoride etching. Biomedical Microdevices, 2008, 10, 179–186.
Huh D, Matthews B D, Mammoto A, Montoya-Zavala M, Hsin H Y, Ingber D E. Reconstituting organ-level lung functions on a chip. Science, 2010, 328, 1662–1668.
Shah G, Costello B J. Soft tissue regeneration incorporating 3-dimensional biomimetic scaffolds. Oral & Maxillofacial Surgery Clinics, 2017, 29, 9–18.
Badhe R V, Bijukumar D, Chejara D R, Mabrouk M, Choonara Y E, Kumar P, du Toit L C, Kondiah P P D, Pillay V. A composite chitosan-gelatin bi-layered, biomimetic macroporous scaffold for blood vessel tissue engineering. Carbohydrate Polymers, 2017, 157, 1215–1225.
Mansouri N, Bagheri S. The influence of topography on tissue engineering perspective. Materials Science & Engineering C–Materials for Biological Applications, 2016, 61, 906–921.
Visone R, Gilardi M, Marsano A, Rasponi M, Bersini S, Moretti M. Cardiac meets skeletal: What’s new in microfluidic models for muscle tissue engineering. Molecules, 2016, 21, 1128.
Jeong K Y, Ji S L, Paik D H, Jung W K, Choi S W. Fabrication of cell-penetrable microfibrous matrices with a highly porous structure using a simple fluidic device for tissue engineering. Materials Letters, 2016, 168, 116–120.
Agarwal P, Choi J K, Huang H S, Zhao S T, Dumbleton J, Li J R, He X M. A biomimetic core-shell platform for miniaturized 3D cell and tissue engineering. Particle & Particle Systems Characterization, 2015, 32, 809–816.
Ren L, Qian Z H, Ren L Q. Biomechanics of musculoskeletal system and its biomimetic implications: A review. Journal of Bionic Engineering, 2014, 11, 159–175.
Ostrovidov S, Ahadian S, Ramon-Azcon J, Hosseini V, Fujie T, Parthiban S P, Shiku H, Matsue T, Kaji H, Ramalingam M, Bae H, Khademhosseini A. Three-dimensional co-culture of C2C12/PC12 cells improves skeletal muscle tissue formation and function. Journal of Tissue Engineering and Regenerative Medicine, 2017, 11, 582–595.
Elsayed Y, Lekakou C, Labeed F, Tomlins P. Fabrication and characterisation of biomimetic, electrospun gelatin fibre scaffolds for tunica media-equivalent, tissue engineered vascular grafts. Materials Science & Engineering C–Materials for Biological Applications, 2016, 61, 473–483.
Williams C, Xie A W, Yamato M, Okano T, Wong J Y. Stacking of aligned cell sheets for layer-by-layer control of complex tissue structure. Biomaterials, 2011, 32, 5625–5632.
Syed H, Unnikrishnan V U, Olcmen S. Characteristics of time-varying intracranial pressure on blood flow through cerebral artery: A fluid-structure interaction approach. Proceedings of the Institution of Mechanical Engineers, Part H, 2016, 230, 111–121.
Hudlicka O, Brown M D. Adaptation of skeletal muscle microvasculature to increased or decreased blood flow: Role of shear stress, nitric oxide and vascular endothelial growth factor. Journal of Vascular Research, 2009, 46, 504–512.
Issa B, Moore R J, Bowtell R W, Baker P N, Johnson I R, Worthington B S, Gowland P A. Quantification of blood velocity and flow rates in the uterine vessels using echo planar imaging at 0.5 Tesla. Journal of Magnetic Resonance Imaging, 2010. 31, 921–927.
Acknowledgment
This work was supported by National Natural Science Foundation of China (Grant No. 51375371) and the High-Tech Projects of China (Grant Nos. 2015AA020303 and 2015AA042503).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Dong, G., Lian, Q., Yang, L. et al. Preparation and Endothelialization of Multi-level Vessel-like Network in Enzymated Gelatin Scaffolds. J Bionic Eng 15, 673–681 (2018). https://doi.org/10.1007/s42235-018-0055-3
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42235-018-0055-3