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Biomaterials. 2017 Jul;131:98-110. doi: 10.1016/j.biomaterials.2017.03.026. Epub 2017 Mar 23.

Microfluidic-enhanced 3D bioprinting of aligned myoblast-laden hydrogels leads to functionally organized myofibers in vitro and in vivo.

Author information

1
Tissue Engineering Lab, Università Campus Bio-Medico di Roma, Rome, Italy.
2
Department of Biology, University of Rome Tor Vergata, Rome, Italy.
3
Department of Chemistry, Sapienza University of Rome, Rome, Italy.
4
Warsaw University of Technology, Faculty of Materials Science and Engineering, Warsaw, Poland.
5
Department of Biomedical Engineering, Techion Institute, Haifa, Israel.
6
Institute of Physical Chemistry, Polish Academy of Sciences, 01224 Warsaw, Poland.
7
Tissue Engineering Lab, Università Campus Bio-Medico di Roma, Rome, Italy. Electronic address: a.rainer@unicampus.it.
8
Department of Biology, University of Rome Tor Vergata, Rome, Italy. Electronic address: cesare.gargioli@uniroma2.it.

Abstract

We present a new strategy for the fabrication of artificial skeletal muscle tissue with functional morphologies based on an innovative 3D bioprinting approach. The methodology is based on a microfluidic printing head coupled to a co-axial needle extruder for high-resolution 3D bioprinting of hydrogel fibers laden with muscle precursor cells (C2C12). To promote myogenic differentiation, we formulated a tailored bioink with a photocurable semi-synthetic biopolymer (PEG-Fibrinogen) encapsulating cells into 3D constructs composed of aligned hydrogel fibers. After 3-5 days of culture, the encapsulated myoblasts started migrating and fusing, forming multinucleated myotubes within the 3D bioprinted fibers. The obtained myotubes showed high degree of alignment along the direction of hydrogel fiber deposition, further revealing maturation, sarcomerogenesis, and functionality. Following subcutaneous implantation in the back of immunocompromised mice, bioprinted constructs generated organized artificial muscle tissue in vivo. Finally, we demonstrate that our microfluidic printing head allows to design three dimensional multi-cellular assemblies with an exquisite compartmentalization of the encapsulated cells. Our results demonstrate an enhanced myogenic differentiation with the formation of parallel aligned long-range myotubes. The approach that we report here represents a robust and valid candidate for the fabrication of macroscopic artificial muscle to scale up skeletal muscle tissue engineering for human clinical application.

KEYWORDS:

Artificial muscle; Microfluidic enhanced 3D bioprinting; Myogenic precursor cells; Myotubes; PEG-Fibrinogen hydrogel

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