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Single-pot biofabrication of living fibers for tissue engineering applications

Published online by Cambridge University Press:  01 June 2018

Paulomi Ghosh ,
Arun Prabhu Rameshbabu ,
Dipankar Das ,
Bhuvaneshwaran Subramanian ,
Sintu Kumar Samanta ,
Sabyasachi Roy ,
Sagar Pal ,
Sudip Kumar Ghosh  and
Santanu Dhara
Paulomi Ghosh*
Affiliation:
Biomaterials and Tissue Engineering Laboratory, School of Medical Science and Technology, Indian Institute of Technology Kharagpur, Kharagpur–721302, India; and CSIR–Indian Institute of Chemical Biology, Kolkata, West Bengal–700032, India
Arun Prabhu Rameshbabu
Affiliation:
Biomaterials and Tissue Engineering Laboratory, School of Medical Science and Technology, Indian Institute of Technology Kharagpur, Kharagpur–721302, India
Dipankar Das
Affiliation:
Polymer Chemistry Laboratory, Department of Applied Chemistry, Indian School of Mines, Dhanbad–826004, India
Bhuvaneshwaran Subramanian
Affiliation:
Biomaterials and Tissue Engineering Laboratory, School of Medical Science and Technology, Indian Institute of Technology Kharagpur, Kharagpur–721302, India
Sintu Kumar Samanta
Affiliation:
Department of Biotechnology, Indian Institute of Technology Kharagpur, Kharagpur–721302, India
Sabyasachi Roy
Affiliation:
Department of Gynaecology, Midnapore Medical College, Paschim Medinipur–721101, India
Sagar Pal
Affiliation:
Polymer Chemistry Laboratory, Department of Applied Chemistry, Indian School of Mines, Dhanbad–826004, India; and Department of Biotechnology, Indian Institute of Technology Kharagpur, Kharagpur–721302, India
Sudip Kumar Ghosh*
Affiliation:
Polymer Chemistry Laboratory, Department of Applied Chemistry, Indian School of Mines, Dhanbad–826004, India; and Department of Biotechnology, Indian Institute of Technology Kharagpur, Kharagpur–721302, India
Santanu Dhara*
Affiliation:
Biomaterials and Tissue Engineering Laboratory, School of Medical Science and Technology, Indian Institute of Technology Kharagpur, Kharagpur–721302, India
*
a)Address all correspondence to these authors. e-mail: [email protected]
b)e-mail: [email protected]
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Abstract

In this work, morphology, viability, and metabolism of the amniotic mesenchymal stem cells conditioned with different citric acid (CA)/media ratios were investigated using rhodamine-phalloidin/4′,6-diamidino-2-phenylindole staining, live/dead assay, proliferating cell nuclear antigen, and terminal deoxynucleotidyl transferase dUTP nick end labeling (TUNEL assay). The cells cultured in 25:75 CA/media displayed well spread actin filaments with a prominent nucleus and evidenced optimum viability. The gelation kinetics of chitosan solution in CA/media (25:75) was monitored via dynamic time sweep analysis on a rheometer. The chemical cross-linking of chitosan with CA was confirmed by nuclear magnetic resonance studies. Subsequently, chitosan solution was extruded in CA/media bath containing cells under benign conditions to form cell-laden fibers (living fibers). The prelabeled cells imaged immediately after fiber formation confirmed the attachment of the cells on the fibers. This approach has several advantages including instantaneous gelation, tunable mechanical properties, and adjustable biodegradability that can provide a platform technology for creating viable three dimensional (3D) building blocks for tissue engineering applications.

Keywords

biomaterialpolymer
Type
Invited Article
Information
Journal of Materials Research , Volume 33 , Issue 14: Focus Issue: 3D Printing of Biomaterials , 27 July 2018 , pp. 2019 - 2028
Copyright
Copyright © Materials Research Society 2018 

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Footnotes

c)

These authors contributed equally to this work.

References

REFERENCES

Mooney, D.J. and Mikos, A.G.: Growing new organs. Sci. Am. 280, 60 (1999).CrossRefGoogle ScholarPubMed
McCullen, S.D., Autefage, H., Callanan, A., Gentleman, E., and Stevens, M.M.: Anisotropic fibrous scaffolds for articular cartilage regeneration. Tissue Eng., Part A 18, 2073 (2012).CrossRefGoogle ScholarPubMed
Jordan, A.M., Kim, S.E., Van de Voorde, K., Pokorski, J.K., and Korley, L.T.J.: In situ fabrication of fiber reinforced three-dimensional hydrogel tissue engineering scaffolds. ACS Biomater. Sci. Eng. 3, 1869 (2017).CrossRefGoogle Scholar
Tamayol, A., Akbari, M., Annabi, N., Paul, A., Khademhosseini, A., and Juncker, D.: Fiber-based tissue engineering: Progress, challenges, and opportunities. Biotechnol. Adv. 31, 669 (2013).CrossRefGoogle ScholarPubMed
Jun, Y., Kang, E., Chae, S., and Lee, S.H.: Microfluidic spinning of micro- and nano-scale fibers for tissue engineering. Lab Chip 14, 2145 (2014).CrossRefGoogle ScholarPubMed
Liu, W., Thomopoulos, S., and Xia, Y.: Electrospun nanofibers for regenerative medicine. Adv. Healthcare Mater. 1, 10 (2012).CrossRefGoogle ScholarPubMed
Freeman, J.W., Woods, M.D., Cromer, D.A., Wright, L.D., and Laurencin, C.T.: Tissue engineering of the anterior cruciate ligament: The viscoelastic behavior and cell viability of a novel braid–twist scaffold. J. Biomater. Sci., Polym. Ed. 20, 1709 (2012).CrossRefGoogle Scholar
Jayasinghe, S.N.: Cell electrospinning: A novel tool for functionalising fibres, scaffolds and membranes with living cells and other advanced materials for regenerative biology and medicine. Analyst 138, 2215 (2013).CrossRefGoogle ScholarPubMed
Lopez-Rubio, A., Sanchez, E., Sanz, Y., and Lagaron, J.M.: Encapsulation of living bifidobacteria in ultrathin PVOH electrospun fibers. Biomacromolecules 10, 2823 (2009).CrossRefGoogle ScholarPubMed
Ram Lee, B., Lee, K.H., Kang, E., Kim, D-S., and Lee, S-H.: Microfluidic wet spinning of chitosan-alginate microfibers and encapsulation of HepG2 cells in fibers. Biomicrofluidics 5, 022208 (2011).Google Scholar
Shin, S.J., Park, J.Y., Lee, J.Y., Park, H., Park, Y.D., Lee, K.B., Whang, C.M., and Lee, S.H.: “On the fly” Continuous generation of alginate fibers using a microfluidic device. Langmuir 23, 9104 (2007).CrossRefGoogle ScholarPubMed
Liu, M., Zhou, Z., Chai, Y., Zhang, S., Wu, X., Huang, S., Su, J., and Jiang, J.: Synthesis of cell composite alginate microfibers by microfluidics with the application potential of small diameter vascular grafts. Biofabrication 9, 025030 (2017).CrossRefGoogle ScholarPubMed
Hsieh, F.Y., Lin, H.H., and Hsu, S.H.: 3D bioprinting of neural stem cell-laden thermoresponsive biodegradable polyurethane hydrogel and potential in central nervous system repair. Biomaterials 71, 48 (2015).CrossRefGoogle ScholarPubMed
Levato, R., Visser, J., Planell, J.A., Engel, E., Malda, J., and Mateos-Timoneda, M.A.: Biofabrication of tissue constructs by 3D bioprinting of cell-laden microcarriers. Biofabrication 6, 035020 (2014).CrossRefGoogle ScholarPubMed
Ghosh, P., Rameshbabu, A.P., Das, D., Francis, N.K., Pawar, H.S., Subramanian, B., Pal, S., and Dhara, S.: Covalent cross-links in polyampholytic chitosan fibers enhances bone regeneration in a rabbit model. Colloids Surf., B 125, 160 (2014).CrossRefGoogle Scholar
Alviano, F., Fossati, V., Marchionni, C., Arpinati, M., Bonsi, L., Franchina, M., Lanzoni, G., Cantoni, S., Cavallini, C., Bianchi, F., Tazzari, P.L., Pasquinelli, G., Foroni, L., Ventura, C., Grossi, A., and Bagnara, G.P.: Term amniotic membrane is a high throughput source for multipotent mesenchymal stem cells with the ability to differentiate into endothelial cells in vitro. BMC Dev. Biol. 7, 11 (2007).CrossRefGoogle ScholarPubMed
Rameshbabu, A.P., Ghosh, P., Subramani, E., Bankoti, K., Kapat, K., Datta, S., Maity, P.P., Subramanian, B., Roy, S., Chaudhury, K., and Dhara, S.: Investigating the potential of human placenta-derived extracellular matrix sponges coupled with amniotic membrane-derived stem cells for osteochondral tissue engineering. J. Mater. Chem. B 4, 613 (2016).CrossRefGoogle Scholar
Ghosh, P., Rameshbabu, A.P., Dogra, N., and Dhara, S.: 2,5-Dimethoxy 2,5-dihydrofuran crosslinked chitosan fibers enhance bone regeneration in rabbit femur defects. RSC Adv. 4, 19516 (2014).CrossRefGoogle Scholar
Ghosh, P., Das, M., Rameshbabu, A.P., Das, D., Datta, S., Pal, S., Panda, A.B., and Dhara, S.: Chitosan derivatives cross-linked with iodinated 2,5-dimethoxy-2,5-dihydrofuran for non-invasive imaging. ACS Appl. Mater. Interfaces 6, 17926 (2014).CrossRefGoogle ScholarPubMed
Ghosh, P., Rameshbabu, A.P., and Dhara, S.: Citrate cross-linked gels with strain reversibility and viscoelastic behavior accelerate healing of osteochondral defects in a rabbit model. Langmuir 30, 8442 (2014).CrossRefGoogle Scholar
Díaz-Prado, S., Muiños-López, E., Hermida-Gómez, T., Rendal-Vázquez, M.E., Fuentes-Boquete, I., de Toro, F.J., and Blanco, F.J.: Isolation and characterization of mesenchymal stem cells from human amniotic membrane. Tissue Eng., Part C 17, 49 (2011).CrossRefGoogle ScholarPubMed
Niwa, H., Masui, S., Chambers, I., Smith, A.G., and Miyazaki, J.: Phenotypic complementation establishes requirements for specific POU domain and generic transactivation function of Oct-3/4 in embryonic stem cells. Mol. Cell. Biol. 22, 1526 (2002).CrossRefGoogle ScholarPubMed
Chambers, I., Colby, D., and Robertson, M.: Functional expression cloning of nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113, 643 (2003).CrossRefGoogle ScholarPubMed
Terada, D., Kobayashi, H., Zhang, K., Tiwari, A., Yoshikawa, C., and Hanagata, N.: Transient charge-masking effect of applied voltage on electrospinning of pure chitosan nanofibers from aqueous solutions. Sci. Technol. Adv. Mater. 13, 15003 (2012).CrossRefGoogle ScholarPubMed
Murphy, C.L. and Sambanis, A.: Effect of oxygen tension and alginate encapsulation on restoration of the differentiated phenotype of passaged chondrocytes. Tissue Eng. 7, 791 (2001).CrossRefGoogle ScholarPubMed
Maciel, V.B., Yoshida, C.M., and Franco, T.T.: Chitosan/pectin polyelectrolyte complex as a pH indicator. Carbohydr. Polym. 132, 537 (2015).CrossRefGoogle ScholarPubMed
Oryan, A. and Sahvieh, S.: Effectiveness of chitosan scaffold in skin, bone and cartilage healing. Int. J. Biol. Macromol. 104, 1003 (2017).CrossRefGoogle ScholarPubMed
Manivasagan, P. and Oh, J.: Marine polysaccharide-based nanomaterials as a novel source of nanobiotechnological applications. Int. J. Biol. Macromol. 82, 315 (2016).CrossRefGoogle ScholarPubMed
Jiang, T., Deng, M., James, R., Nair, L.S., and Laurencin, C.T.: Micro- and nanofabrication of chitosan structures for regenerative engineering. Acta Biomater. 10, 1632 (2014).CrossRefGoogle ScholarPubMed
Mihaila, S.M., Popa, E.G., Reis, R.L., Marques, A.P., and Gomes, M.E.: Fabrication of endothelial cell-laden carrageenan microfibers for microvascularized bone tissue engineering applications. Biomacromolecules 15, 2849 (2014).CrossRefGoogle ScholarPubMed

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