Symbiotic Photosynthetic Oxygenation within 3D-Bioprinted Vascularized Tissues

• Published in: Matter Vol. 4; no. 1; pp. 217 - 240
• Main Authors: Maharjan, Sushila, Alva, Jacqueline, Cámara, Cassandra, Rubio, Andrés G., Hernández, David, Delavaux, Clément, Correa, Erandy, Romo, Mariana D., Bonilla, Diana, Santiago, Mille Luis, Li, Wanlu, Cheng, Feng, Ying, Guoliang, Zhang, Yu Shrike
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 06.01.2021
• Subjects: algae; biofabrication; bioink; bioprinting; Chlamydomonas reinhardtii; oxygenation; photosynthesis; regenerative medicine; tissue engineering; vascularization; tissue engineering; photosynthesis; Chlamydomonas reinhardtii; regenerative medicine; bioink; MAP6: Development; algae; oxygenation; biofabrication; vascularization; bioprinting
• ISSN: 2590-2385; 2590-2393; 2590-2385
• DOI: 10.1016/j.matt.2020.10.022

In this study, we present the photosynthetic oxygen (O2) supply to mammalian cells within a volumetric extracellular matrix-like construct, whereby a three-dimensional (3D)-bioprinted fugitive pattern encapsulating unicellular green algae, Chlamydomonas reinhardtii, served as a natural photosynthetic O2 generator. The presence of bioprinted C. reinhardtii enhanced the viability and functionality of mammalian cells while reducing the hypoxic conditions within the tissues. We were able to subsequently endothelialize the hollow perfusable microchannels formed after enzymatic removal of the bioprinted C. reinhardtii-laden patterns from the matrices following the initial oxygenation period to obtain biologically relevant vascularized mammalian tissue constructs. The feasibility of co-culture of C. reinhardtii with human cells, the printability and the enzymatic degradability of the fugitive bioink, and the exploration of C. reinhardtii as a natural, eco-friendly, cost-effective, and sustainable source of O2 would likely promote the development of engineered tissues, tissue models, and food for various applications. [Display omitted] •Application of bioprinted algae as O2 generator in tissue (model) engineering•O2 produced by algae patterns improved functions of surrounding human cells•Endothelialization of channels post-enzymatic digestion of fugitive algae patterns Sufficient and homogeneous distribution of oxygen (O2) facilitates cell growth within three-dimensional (3D) tissue constructs whereas limited supply of O2 induces cell death. This work reports the unique adoption of 3D-bioprinted Chlamydomonas reinhardtii as a natural photosynthetic O2 generator for enhancing functions of engineered tissue constructs in vitro. Interestingly, the cellulase-mediated digestion of the bioprinted C. reinhardtii-laden patterns embedded within mammalian cell-encapsulating GelMA matrices created perfusable and interconnected microchannels. These microchannels, when subsequently endothelialized, made it possible to obtain biologically relevant vascularized tissue constructs. These bioprinted unicellular microalgae represent a bionic and sustainable source of O2, promoting the development of engineered mammalian tissues. Three-dimensional-bioprinted unicellular green algae, Chlamydomonas reinhardtii, was used as a sustainable bionic source of O2 in engineered tissue constructs. O2 photosynthetically produced by bioprinted algae significantly improved the viability and functionality of the human cells within surrounding matrices while reducing their hypoxic conditions. Fugitive patterns encapsulating the algae were enzymatically dissolved by cellulase digestion to create interconnected microchannels, which were subsequently endothelialized, generating vascularized tissues.