Mesenchymal stem cell cultivation in electrospun scaffolds: mechanistic modeling for tissue engineering
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Abstract
Tissue engineering is a multidisciplinary field of research in which the cells, biomaterials, and processes can be optimized to develop a tissue substitute. Three-dimensional (3D) architectural features from electrospun scaffolds, such as porosity, tortuosity, fiber diameter, pore size, and interconnectivity have a great impact on cell behavior. Regarding tissue development in vitro, culture conditions such as pH, osmolality, temperature, nutrient, and metabolite concentrations dictate cell viability inside the constructs. The effect of different electrospun scaffold properties, bioreactor designs, mesenchymal stem cell culture parameters, and seeding techniques on cell behavior can be studied individually or combined with phenomenological modeling techniques. This work reviews the main culture and scaffold factors that affect tissue development in vitro regarding the culture of cells inside 3D matrices. The mathematical modeling of the relationship between these factors and cell behavior inside 3D constructs has also been critically reviewed, focusing on mesenchymal stem cell culture in electrospun scaffolds.
Keywords
Stem cells Tissue development Electrospun scaffolds Phenomenological modelingNotes
Acknowledgements
The authors wish to thank the Stem Cell Research Institute, the Coordination for the Improvement of Higher Level Personnel (CAPES), and the Study and Project Financer (FINEP) for financial support.
Compliance with ethical standards
This work does not contain any studies with human participants or animals performed by any of the authors.
Conflict of interest
The authors declare that they have no conflict of interest.
References
- 1.Langer, R., Vacanti, J.P.: Tissue engineering. Science 260, 920–926 (1993). https://doi.org/10.1126/science.8493529 ADSGoogle Scholar
- 2.O’Brien, F.J.: Biomaterials & scaffolds for tissue engineering. Mater. Today 14, 88–95 (2011). https://doi.org/10.1016/S1369-7021(11)70058-X Google Scholar
- 3.Chua, A.W.C., Khoo, Y.C., Tan, B.K., Tan, K.C., Foo, C.L., Chong, S.J.: Skin tissue engineering advances in severe burns: review and therapeutic applications. Burn. Trauma. 4, 3 (2016). https://doi.org/10.1186/s41038-016-0027-y Google Scholar
- 4.Place, E.S., Evans, N.D., Stevens, M.M.: Complexity in biomaterials for tissue engineering. Nat. Mater. 8, 457–470 (2009). https://doi.org/10.1038/nmat2441 ADSGoogle Scholar
- 5.Oryan, A., Alidadi, S., Moshiri, A., Maffulli, N.: Bone regenerative medicine: classic options , novel strategies , and future directions. J. Orthop. Surg. Res. 9, 18 (2014). https://doi.org/10.1186/1749-799X-9-18 Google Scholar
- 6.Fitzpatrick, L.E., McDevitt, T.C.: Cell-derived matrices for tissue engineering and regenerative medicine applications. Biomater. Sci. 3, 12–24 (2015). https://doi.org/10.1039/C4BM00246F Google Scholar
- 7.Ku, D., Braddon, L., Wooton, D.: Poly(Vinyl Alcohol) Cryogel, (1999)Google Scholar
- 8.Kumar, R.J., Kimble, R.M., Boots, R., Pegg, S.P.: Treatment of partial-thickness burns: a prospective, randomized trial using transcyte (TM). ANZ J. Surg. 74, 622–626 (2004). https://doi.org/10.1111/j.1445-1433.2004.03106.x Google Scholar
- 9.Walsh, W.R., Bertollo, N., Heuberer, P., Christou, C., Stanton, R., Poggie, R.: Evaluation of a PLLA device in-vitro and in an ovine model of acute rupture of the rotator cuff. In: Proceedings of the Orthopaedic Research Society Annual Meeting, Las Vegas, Nevada, 2015Google Scholar
- 10.Khojasteh, A., Behnia, H., Hosseini, F.S., Dehghan, M.M., Abbasnia, P., Abbas, F.M.: The effect of PCL-TCP scaffold loaded with mesenchymal stem cells on vertical bone augmentation in dog mandible: a preliminary report. J. Biomed. Mater. Res. Part B 101, 848–854 (2013). https://doi.org/10.1002/jbm.b.32889 Google Scholar
- 11.Flasza, M., Kemp, P., Shering, D., Qiao, J., Marshall, D., Bokta, A., Johnson, P.A.: Development and manufacture of an investigational human living dermal equivalent (ICX-SKN). Regen. Med. 2, 903–918 (2007). https://doi.org/10.2217/17460751.2.6.903 Google Scholar
- 12.Baskin, D.S., Ryan, P., Sonntag, V., Westmark, R., Widmayer, M.A.: A prospective, randomized, controlled cervical fusion study using recombinant human bone morphogenetic protein-2 with the CORNERSTONE-SR allograft ring and the ATLANTIS anterior cervical plate. Spine (Phila Pa 1976) 28, 1219–1224; discussion 1225 (2003). https://doi.org/10.1097/01.BRS.0000065486.22141.CA Google Scholar
- 13.Kreuz, P.C., Müller, S., Ossendorf, C., Kaps, C., Erggelet, C.: Treatment of focal degenerative cartilage defects with polymer-based autologous chondrocyte grafts: four-year clinical results. Arthritis Res. Ther. 11, R33 (2009). https://doi.org/10.1186/ar2638 Google Scholar
- 14.Stone, P.A., AbuRahma, A.F., Mousa, A.Y., Phang, D., Hass, S.M., Modak, A., Dearing, D.: Prospective randomized trial of ACUSEAL versus Vascu-Guard patching in carotid endarterectomy. Ann. Vasc. Surg. 28, 1530–1538 (2014). https://doi.org/10.1016/j.avsg.2014.02.017 Google Scholar
- 15.Kehoe, S., Zhang, X.F., Boyd, D.: FDA approved guidance conduits and wraps for peripheral nerve injury: a review of materials and efficacy. Injury 43, 553–572 (2012). https://doi.org/10.1016/j.injury.2010.12.030 Google Scholar
- 16.Olson, J.L., Atala, A., Yoo, J.J.: Tissue engineering: current strategies and future directions. Chonnam Med. J. 47, 1–13 (2011). https://doi.org/10.4068/cmj.2011.47.1.1 Google Scholar
- 17.Chatterjea, A., Meijer, G., van Blitterswijk, C., de Boer, J.: Clinical application of human mesenchymal stromal cells for bone tissue engineering. Stem Cells Int. 2010, 215625 (2010). https://doi.org/10.4061/2010/215625 Google Scholar
- 18.Koh, C.J., Atala, A.: Tissue engineering, stem cells, and cloning: opportunities for regenerative medicine. J. Am. Soc. Nephrol. 15, 1113–1125 (2004). https://doi.org/10.1097/01.ASN.0000119683.59068.F0 Google Scholar
- 19.Tay, L.X., Ahmad, R.E., Dashtdar, H., Tay, K.W., Masjuddin, T., Ab-Rahim, S., Chong, P.P., Selvaratnam, L., Kamarul, T.: Treatment outcomes of alginate-embedded allogenic mesenchymal stem cells versus autologous chondrocytes for the repair of focal articular cartilage defects in a rabbit model. Am. J. Sports Med. 40, 83–90 (2012). https://doi.org/10.1177/0363546511420819 Google Scholar
- 20.Wong, K.L., Lee, K.B.L., Tai, B.C., Law, P., Lee, E.H., Hui, J.H.P.: Injectable cultured bone marrow-derived mesenchymal stem cells in varus knees with cartilage defects undergoing high tibial osteotomy: a prospective, randomized controlled clinical trial with 2 years’ follow-up. Arthrosc. - J. Arthrosc. Relat. Surg. 29, 2020–2028 (2013). https://doi.org/10.1016/j.arthro.2013.09.074 Google Scholar
- 21.Cook, C.A., Huri, P.Y., Ginn, B.P., Gilbert-Honick, J., Somers, S.M., Temple, J.P., Mao, H.Q., Grayson, W.L.: Characterization of a novel bioreactor system for 3D cellular mechanobiology studies. Biotechnol. Bioeng. 113, 1825–1837 (2016). https://doi.org/10.1002/bit.25946 Google Scholar
- 22.Maidhof, R., Tandon, N., Lee, E.J., Luo, J., Duan, Y., Yeager, K., Konofagou, E., Vunjak-Novakovic, G.: Biomimetic perfusion and electrical stimulation applied in concert improved the assembly of engineered cardiac tissue. J. Tissue Eng. Regen. Med. 6, e12–e23 (2012). https://doi.org/10.1002/term.525.Biomimetic Google Scholar
- 23.Wang, Z., Teoh, S.H., Johana, N.B., Khoon Chong, M.S., Teo, E.Y., Hong, M., Yen Chan, J.K., San Thian, E.: Enhancing mesenchymal stem cell response using uniaxially stretched poly(ε-caprolactone) film micropatterns for vascular tissue engineering application. J. Mater. Chem. B 2, 5898–5909 (2014). https://doi.org/10.1039/C4TB00522H Google Scholar
- 24.Knight, E., Przyborski, S.: Advances in 3D cell culture technologies enabling tissue-like structures to be created in vitro. J. Anat. 227, 746–756 (2015). https://doi.org/10.1111/joa.12257 Google Scholar
- 25.Lawrence, B.J.: Mass Transfer in Porous Tissue Engineering Scaffolds (PhD Thesis), Oklahoma State University (2008)Google Scholar
- 26.Romagnoli, C., Zonefrati, R., Galli, G., Puppi, D., Pirosa, A., Chiellini, F., Martelli, F.S., Tanini, A., Brandi, M.L.: In vitro behavior of human adipose tissue-derived stem cells on poly(ε-caprolactone) film for bone tissue engineering applications. Biomed. Res. Int. 2015, 323571 (2015). https://doi.org/10.1155/2015/323571 Google Scholar
- 27.Lawrence, B.J., Devarapalli, M., Madihally, S.: V: flow dynamics in bioreactors containing tissue engineering scaffolds. Biotechnol. Bioeng. 102, 935–947 (2009). https://doi.org/10.1002/bit.22106 Google Scholar
- 28.Asaoka, T., Ohtake, S., Furukawa, K.S., Tamura, A., Ushida, T.: Development of bioactive porous α-TCP/HAp beads for bone tissue engineering. J. Biomed. Mater. Res. Part A. 101, 3295–3300 (2013). https://doi.org/10.1002/jbm.a.34517 Google Scholar
- 29.Matsuno, T., Hashimoto, Y., Adachi, S., Omata, K., Yoshitaka, Y., Ozeki, Y., Umezu, Y., Tabata, Y., Nakamura, M., Satoh, T.: Preparation of injectable 3D-formed beta-tricalcium phosphate bead/alginate composite for bone tissue engineering. Dent. Mater. J. 27, 827–834 (2008). https://doi.org/10.4012/dmj.27.827 Google Scholar
- 30.Matsunaga, Y.T., Morimoto, Y., Takeuchi, S.: Molding cell beads for rapid construction of macroscopic 3D tissue architecture. Adv. Mater. 23, 90–94 (2011). https://doi.org/10.1002/adma.201004375 Google Scholar
- 31.Wang, J.: Porous Microbeads as Three-Dimensional Scaffolds for Tissue Engineering. In: NNIN REU Research Accomplishments. pp. 32–33 (2010)Google Scholar
- 32.Takeuchi, S.: Cell-laden hydrogel beads, fibers and plates for 3D tissue construction. In: 17th International Conference on Solid-State Sensors, Actuators and Microsystems, Transducers and Eurosensors, Barcelona, Spain (2013). doi: https://doi.org/10.1109/Transducers.2013.6627069
- 33.Young, D.A., Christman, K.L.: Injectable biomaterials for adipose tissue engineering. Biomed. Mater. 7, 24104 (2012). https://doi.org/10.1088/1748-6041/7/2/024104 Google Scholar
- 34.Lee, D.A., Reisler, T., Bader, D.L.: Expansion of chondrocytes for tissue engineering in alginate beads enhances chondrocytic phenotype compared to conventional monolayer techniques. Acta Orthop. Scand. 74, 6–15 (2003). https://doi.org/10.1080/00016470310013581 Google Scholar
- 35.Yan, S., Wang, T., Li, X., Jian, Y., Zhang, K., Li, G., Yin, J.: Fabrication of injectable hydrogels based on poly(l-glutamic acid) and chitosan. RSC Adv. 7, 17005–17019 (2017). https://doi.org/10.1039/C7RA01864A Google Scholar
- 36.Xue, B., Kozlovskaya, V., Kharlampieva, E.: Shaped stimuli-responsive hydrogel particles: syntheses, properties and biological responses. J. Mater. Chem. B 5, 9–35 (2017). https://doi.org/10.1039/C6TB02746F Google Scholar
- 37.El-Sherbiny, I., Yacoub, M.: Hydrogel scaffolds for tissue engineering: progress and challenges. Glob. Cardiol. Sci. Pract. 2013, 316–342 (2013). https://doi.org/10.5339/gcsp.2013.38 Google Scholar
- 38.Teixeira, S., Fernandes, H., Leusink, A., Van Blitterswijk, C., Ferraz, M.P., Monteiro, F.J., De Boer, J.: In vivo evaluation of highly macroporous ceramic scaffolds for bone tissue engineering. J. Biomed. Mater. Res. Part A. 93, 567–575 (2010). https://doi.org/10.1002/jbm.a.32532 Google Scholar
- 39.Blanco, J.F., Sánchez-Guijo, F.M., Carrancio, S., Muntion, S., García-Briñon, J., del Cañizo, M.C.: Titanium and tantalum as mesenchymal stem cell scaffolds for spinal fusion: an in vitro comparative study. Eur. Spine J. 20, 1–8 (2011). https://doi.org/10.1007/s00586-011-1901-8 Google Scholar
- 40.Wise, J.K., Yarin, A.L., Megaridis, C.M., Cho, M.: Chondrogenic differentiation of human mesenchymal stem cells on oriented nanofibrous scaffolds: engineering the superficial zone of articular cartilage. Tissue Eng. Part A. 15, 913–921 (2009). https://doi.org/10.1089/ten.tea.2008.0109 Google Scholar
- 41.Awaji, H., Matsunaga, T., Choi, S.-M.: Relation between strength, fracture toughness, and critical frontal process zone size in ceramics. Mater. Trans. 47, 1532–1539 (2006). https://doi.org/10.2320/matertrans.47.1532 Google Scholar
- 42.Sadiasa, A., Nguyen, T.H., Lee, B.-T.: In vitro and in vivo evaluation of porous PCL-PLLA 3D polymer scaffolds fabricated via salt leaching method for bone tissue engineering applications. J. Biomater. Sci. Polym. Ed. 25, 150–167 (2014). https://doi.org/10.1080/09205063.2013.846633 Google Scholar
- 43.Baker, S.C., Rohman, G., Southgate, J., Cameron, N.R.: The relationship between the mechanical properties and cell behaviour on PLGA and PCL scaffolds for bladder tissue engineering. Biomaterials 30, 1321–1328 (2009). https://doi.org/10.1016/j.biomaterials.2008.11.033 Google Scholar
- 44.Asran, A.S., Razghandi, K., Aggarwal, N.H.M.G., Groth, T.: Nanofibers from blends of polyvinyl alcohol and polyhydroxy butyrate as a potensional scaffold materail.pdf. Biomacromolecules 11, 3413–3421 (2010)Google Scholar
- 45.Siparsky, G.L., Voorhees, K.J., Miao, F.: Hydrolysis of Polylactic acid (PLA) and Polycaprolactone (PCL) in aqueous Acetonitrile solutions: autocatalysis. J. Environ. Polym. Degrad. 6, 31–41 (1998). https://doi.org/10.1023/A:1022826528673 Google Scholar
- 46.Barbanti, S.H., Carvalho Zavaglia, C.A., De Rezende Duek, E.A.: Effect of salt leaching on PCL and PLGA (50/50) resorbable scaffolds 2. Material and Methods. Mater. Res. 11, 75–80 (2008). https://doi.org/10.1590/S1516-14392008000100014
- 47.Sung, H.-J., Meredith, C., Johnson, C., Galis, Z.S.: The effect of scaffold degradation rate on three-dimensional cell growth and angiogenesis. Biomaterials 25, 5735–5742 (2004). https://doi.org/10.1016/j.biomaterials.2004.01.066 Google Scholar
- 48.An, J., Leeuwenburgh, S.C.G., Wolke, J.G.C., Jansen, J.A.: Effects of stirring and fluid perfusion on the in vitro degradation of calcium phosphate cement/PLGA composites. Tissue Eng. Part C. 21, 1171–1177 (2015). https://doi.org/10.1089/ten.tec.2015.0016 Google Scholar
- 49.Loh, Q.L., Choong, C.: Three-dimensional scaffolds for tissue engineering applications: role of porosity and pore size. Tissue Eng. Part B. Rev. 19, 485–502 (2013). https://doi.org/10.1089/ten.TEB.2012.0437 Google Scholar
- 50.Pulikkot, S., Greish, Y.E., Mourad, A.H.I., Karam, S.M.: Establishment of a three-dimensional culture system of gastric stem cells supporting mucous cell differentiation using microfibrous polycaprolactone scaffolds. Cell Prolif. 47, 553–563 (2014). https://doi.org/10.1111/cpr.12141 Google Scholar
- 51.Emma Campiglio, C., Marcolin, C., Draghi, L.: Electrospun ECM macromolecules as biomimetic scaffold for regenerative medicine: challenges for preserving conformation and bioactivity. AIMS Mater. Sci. 4, 638–669 (2017). https://doi.org/10.3934/matersci.2017.3.638 Google Scholar
- 52.Wendorff, J.H., Agarwal, S., Greiner, A.: Materials, Processing, and Applications. Wiley-VCH Verlag GmbH & Co., Weinheim, Germany (2012)Google Scholar
- 53.Bye, F.J., Wang, L., Bullock, A.J., Blackwood, K.A., Ryan, A.J., MacNeil, S.: Postproduction processing of electrospun fibres for tissue engineering. J. Vis. Exp. (2012). https://doi.org/10.3791/4172
- 54.Moon, S., Gil, M., Lee, K.J.: Syringeless electrospinning toward versatile fabrication of nanofiber web. Sci. Rep. 7, 41424 (2017). https://doi.org/10.1038/srep41424 ADSGoogle Scholar
- 55.Niu, H., Lin, T.: Fiber generators in needleless electrospinning. J. Nanomater. 2012, 1–13 (2012). https://doi.org/10.1155/2012/725950 Google Scholar
- 56.Kwon, S.-M., Kim, Y.-J., Hong, J.K., Bang, J.Y., Xu, G., Lee, J.-H., Lee, H.-J., Kim, H.S.: Thickness-controllable electrospun fibers promote tubular structure formation by endothelial progenitor cells. Int. J. Nanomedicine 10, 1189–1200 (2015). https://doi.org/10.2147/IJN.S73096 Google Scholar
- 57.Aghajanpoor, M., Hashemi-Najafabadi, S., Baghaban-Eslaminejad, M., Bagheri, F., Mohammad Mousavi, S., Azam Sayyahpour, F.: The effect of increasing the pore size of nanofibrous scaffolds on the osteogenic cell culture using a combination of sacrificial agent electrospinning and ultrasonication. J. Biomed. Mater. Res. Part A. 105, 1887–1899 (2017). https://doi.org/10.1002/jbm.a.36052 Google Scholar
- 58.Vaquette, C., Cooper-White, J.J.: Increasing electrospun scaffold pore size with tailored collectors for improved cell penetration. Acta Biomater. 7, 2544–2557 (2011). https://doi.org/10.1016/j.actbio.2011.02.036 Google Scholar
- 59.Pham, Q.P., Sharma, U., Mikos, A.G.: Electrospun poly(ε-caprolactone) microfiber and multilayer nanofiber/microfiber scaffolds: characterization of scaffolds and measurement of cellular infiltration. Biomacromolecules 7, 2796–2805 (2006). https://doi.org/10.1021/bm060680j Google Scholar
- 60.Phipps, M.C., Clem, W.C., Catledge, S.A., Xu, Y., Hennessy, K.M., Thomas, V., Jablonsky, M.J., Chowdhury, S., Stanishevsky, A.V., Vohra, Y.K., Bellis, S.L.: Mesenchymal stem cell responses to bone-mimetic electrospun matrices composed of polycaprolactone, collagen I and nanoparticulate hydroxyapatite. PLoS One 6, 1–8 (2011). https://doi.org/10.1371/journal.pone.0016813 Google Scholar
- 61.Francis, M.P., Moghaddam-White, Y.M., Sachs, P.C., Beckman, M.J., Chen, S.M., Bowlin, G.L., Elmore, L.W., Holt, S.E.: Modeling early stage bone regeneration with biomimetic electrospun fibrinogen nanofibers and adipose-derived mesenchymal stem cells. Electrospinning 1, 10–19 (2016). https://doi.org/10.1515/esp-2016-0002 Google Scholar
- 62.Yao, Q., Cosme, J.G.L., Xu, T., Miszuk, J.M., Picciani, P.H.S., Fong, H., Sun, H.: Three-dimensional electrospun PCL/PLA blend nanofibrous scaffolds with significantly improved stem cells osteogenic differentiation and cranial bone formation. Biomaterials 115, 115–127 (2017). https://doi.org/10.1016/j.biomaterials.2016.11.018 Google Scholar
- 63.Chen, H., Peng, Y., Wu, S., Tan, L.P.: Electrospun 3D fibrous scaffolds for chronic wound repair. Materials (Basel). 9(1–12), (2016). https://doi.org/10.3390/ma9040272
- 64.Fazili, A., Gholami, S., Zangi, B.M., Seyedjafari, E., Gholami, M.: In vivo differentiation of mesenchymal stem cells into insulin producing cells on electrospun poly-L-Lactide acid scaffolds coated with Matricaria chamomilla L. Oil. Cell J. 18, 310–321 (2016)Google Scholar
- 65.Silva, S.Y., Rueda, L.C., López, M., Vélez, I.D., Rueda-Clausen, C.F., Smith, D.J., Muñoz, G., Mosquera, H., Silva, F.A., Buitrago, A., Díaz, H., López-Jaramillo, P.: Double-blind, randomized controlled trial, to evaluate the effectiveness of a controlled nitric oxide releasing patch versus meglumine antimoniate in the treatment of cutaneous leishmaniasis [NCT00317629]. Trials 7, 14 (2006). https://doi.org/10.1186/1745-6215-7-14 Google Scholar
- 66.Silva, S.Y., Rueda, L.C., Márquez, G.A., López, M., Smith, D.J., Calderón, C.A., Castillo, J.C., Matute, J., Rueda-Clausen, C.F., Orduz, A., Silva, F.A., Kampeerapappun, P., Bhide, M., López-Jaramillo, P.: Double blind, randomized, placebo-controlled clinical trial for the treatment of diabetic foot ulcers, using a nitric oxide releasing patch: PATHON. Trials 8, 26 (2007). https://doi.org/10.1186/1745-6215-8-26 Google Scholar
- 67.Wu, X., Wang, Y., Zhu, C., Tong, X., Yang, M., Yang, L., Liu, Z., Huang, W., Wu, F., Zong, H., Li, H., He, H.: Preclinical animal study and human clinical trial data of co-electrospun poly(l-lactide-co-caprolactone) and fibrinogen mesh for anterior pelvic floor reconstruction. Int. J. Nanomedicine 11, 389–397 (2016). https://doi.org/10.2147/IJN.S88803 Google Scholar
- 68.Hutmacher, D.W., Singh, H.: Computational fluid dynamics for improved bioreactor design and 3D culture. Trends Biotechnol. 26, 166–172 (2008). https://doi.org/10.1016/j.tibtech.2007.11.012 Google Scholar
- 69.Chang, H., Wang, Y.: Cell responses to surface and architecture of tissue engineering scaffolds. In: Eberli, D. (ed.) Regenerative medicine and tissue engineering - Cells and biomaterials. pp. 569–588. InTech, Rijeka, Croatia (2011)Google Scholar
- 70.Aarvold, A., Smith, J.O., Tayton, E.R., Lanham, S.A., Chaudhuri, J.B., Turner, I.G., Oreffo, R.O.C.: The effect of porosity of a biphasic ceramic scaffold on human skeletal stem cell growth and differentiation in vivo. J. Biomed. Mater. Res. Part A. 101, 3431–3437 (2013)Google Scholar
- 71.Gomes, M.E., Holtorf, H.L., Reis, R.L., Mikos, A.G.: Influence of the porosity of starch-based fiber mesh scaffolds on the proliferation and osteogenic differentiation of bone marrow stromal cells cultured in a flow perfusion bioreactor. Tissue Eng. 12, 801–809 (2006). https://doi.org/10.1089/ten.2006.12.801 Google Scholar
- 72.Ikeda, R., Fujioka, H., Nagura, I., Kokubu, T., Toyokawa, N., Inui, A., Makino, T., Kaneko, H., Doita, M., Kurosaka, M.: The effect of porosity and mechanical property of a synthetic polymer scaffold on repair of osteochondral defects. Int. Orthop. 33, 821–828 (2008). https://doi.org/10.1007/s00264-008-0532-0 Google Scholar
- 73.Lee, B.L.-P., Tang, Z., Wang, A., Huang, F., Yan, Z., Wang, D., Chu, J.S., Dixit, N., Yang, L., Li, S.: Synovial stem cells and their responses to the porosity of microfibrous scaffold. Acta Biomater. 9, 7264–7275 (2013). https://doi.org/10.1016/j.actbio.2013.03.009 Google Scholar
- 74.Fu, X., Wang, H.: Rapid fabrication of biomimetic nanofiber-enabled skin grafts. In: Webster, T.J. (ed.) Nanomedicine: Technologies and Applications. p. 428. Woodhead Publishing, Cambridge, UK (2012)Google Scholar
- 75.Sabree, I., Gough, J.E., Derby, B.: Mechanical properties of porous ceramic scaffolds: influence of internal dimensions. Ceram. Int. 41, 8425–8432 (2015). https://doi.org/10.1016/j.ceramint.2015.03.044 Google Scholar
- 76.Lowery, J.L., Datta, N., Rutledge, G.C.: Effect of fiber diameter, pore size and seeding method on growth of human dermal fibroblasts in electrospun poly(epsilon-caprolactone) fibrous mats. Biomaterials 31, 491–504 (2010). https://doi.org/10.1016/j.biomaterials.2009.09.072 Google Scholar
- 77.Milleret, V., Hefti, T., Hall, H., Vogel, V., Eberli, D.: Influence of the fiber diameter and surface roughness of electrospun vascular grafts on blood activation. Acta Biomater. 8, 4349–4356 (2012). https://doi.org/10.1016/j.actbio.2012.07.032 Google Scholar
- 78.Jabur, A.R., Al-Hassani, E.S., Al-Shammari, A.M., Najim, M.A., Hassan, A.A., Ahmed, A.A.: Evaluation of stem cells’ growth on electrospun polycaprolactone (PCL) scaffolds used for soft tissue applications. Energy Procedia 119, 61–71 (2017). https://doi.org/10.1016/j.egypro.2017.07.048 Google Scholar
- 79.Vashaghian, M., Zandieh-Doulabi, B., Roovers, J.-P., Smit, T.H.: Electrospun matrices for pelvic floor repair: effect of fiber diameter on mechanical properties and cell behavior. Tissue Eng. Part A. 22, 1305–1316 (2016). https://doi.org/10.1089/ten.tea.2016.0194 Google Scholar
- 80.Elsayed, Y., Lekakou, C., Labeed, F., Tomlins, P.: Smooth muscle tissue engineering in crosslinked electrospun gelatin scaffolds. J. Biomed. Mater. Res. Part A. 104, 313–321 (2016). https://doi.org/10.1002/jbm.a.35565 Google Scholar
- 81.Bergmeister, H., Schreiber, C., Grasl, C., Walter, I., Plasenzotti, R., Stoiber, M., Bernhard, D., Schima, H.: Healing characteristics of electrospun polyurethane grafts with various porosities. Acta Biomater. 9, 6032–6040 (2013). https://doi.org/10.1016/j.actbio.2012.12.009 Google Scholar
- 82.Pham, Q.P., Sharma, U., Mikos, A.G.: Electrospinning of polymeric nanofibers for tissue engineering applications: a review. Tissue Eng. 12, 60509065116001 (2006). https://doi.org/10.1089/ten.2006.12.ft-65 Google Scholar
- 83.Soliman, S., Pagliari, S., Rinaldi, A., Forte, G., Fiaccavento, R., Pagliari, F., Franzese, O., Minieri, M., Di Nardo, P., Licoccia, S., Traversa, E.: Multiscale three-dimensional scaffolds for soft tissue engineering via multimodal electrospinning. Acta Biomater. 6, 1227–1237 (2010). https://doi.org/10.1016/j.actbio.2009.10.051 Google Scholar
- 84.Gluck, J.M.: Electrospun Nanofibrous Poly(ε-Caprolactone) (PCL) Scaffolds for Liver Tissue Engineering (Master Thesis), Graduate Faculty of North Carolina State University (2007)Google Scholar
- 85.Cardwell, R.D., Dahlgren, L.A., Goldstein, A.S.: Electrospun fibre diameter, not alignment, affects mesenchymal stem cell differentiation into the tendon/ligament lineage. J. Tissue Eng. Regen. Med. 8, 937–945 (2014). https://doi.org/10.1002/term.1589 Google Scholar
- 86.Tatapudy, S., Aloisio, F., Barber, D., Nystul, T.: Cell fate decisions: emerging roles for metabolic signals and cell morphology. EMBO Rep. 18, 2105–2118 (2017). https://doi.org/10.15252/embr.201744816 Google Scholar
- 87.Aghamohseni, H., Ohadi, K., Spearman, M., Krahn, N., Moo-young, M., Scharer, J.M., Butler, M., Budman, H.M.: Effects of nutrient levels and average culture pH on the glycosylation pattern of camelid-humanized monoclonal antibody. J. Biotechnol. 186, 98–109 (2014). https://doi.org/10.1016/j.jbiotec.2014.05.024 Google Scholar
- 88.Monfoulet, L.-E., Becquart, P., Marchat, D., Vandamme, K., Bourguignon, M., Pacard, E., Viateau, V., Petite, H., Logeart-Avramoglou, D.: The pH in the microenvironment of human mesenchymal stem cells is a critical factor for optimal osteogenesis in tissue-engineered constructs. Tissue Eng. Part A. 20, 1827–1840 (2014). https://doi.org/10.1089/ten.tea.2013.0500 Google Scholar
- 89.Ham, R.G., Mckeehan, W.L.: Media and growth requirements. In: Jakoby, W.B., Pastan, I.H. (eds.) Methods in Enzymology Vol. 58: Cell Culture, pp. 47–93. Academic Press, New York (1979)Google Scholar
- 90.Sivakumar, S., Daum, J.R., Gorbsky, G.J.: Live-cell fluorescence imaging for phenotypic analysis of mitosis. In: Noguchi, E., Gadaleta, M. (eds.) Cell Cycle Control Vol. 1170: Methods in Molecular Biology (Methods and Protocols), pp. 549–562. Humana Press, New York, NY (2014)Google Scholar
- 91.Negoro, K., Kobayashi, S., Takeno, K., Uchida, K., Baba, H.: Effect of osmolarity on glycosaminoglycan production and cell metabolism of articular chondrocyte under three-dimensional culture system. Clin. Exp. Rheumatol. 26, 534–541 (2008)Google Scholar
- 92.Potočar, U., Hudoklin, S., Kreft, M.E., Završnik, J., Božikov, K., Fröhlich, M.: Adipose-derived stem cells respond to increased osmolarities. PLoS One 11, e0163870 (2016). https://doi.org/10.1371/journal.pone.0163870 Google Scholar
- 93.Koay, E.J., Athanasiou, K.A.: Hypoxic chondrogenic differentiation of human embryonic stem cells enhances cartilage protein synthesis and biomechanical functionality. Osteoarthr. Cartil. 16, 1450–1456 (2008). https://doi.org/10.1016/j.joca.2008.04.007 Google Scholar
- 94.Ma, T., Grayson, W.L., Fröhlich, M., Vunjak-Novakovic, G.: Hypoxia and stem cell-based engineering of mesenchymal tissues. Biotechnol. Prog. 25, 32–42 (2009). https://doi.org/10.1002/btpr.128 Google Scholar
- 95.Dos Santos, F., Andrade, P.Z., Boura, J.S., Abecasis, M.M., Da Silva, C.L., Cabral, J.M.S.: Ex vivo expansion of human mesenchymal stem cells: a more effective cell proliferation kinetics and metabolism under hypoxia. J. Cell. Physiol. 223, 27–35 (2010). https://doi.org/10.1002/jcp.21987 Google Scholar
- 96.Deschepper, M., Oudina, K., David, B., Myrtil, V., Collet, C., Bensidhoum, M., Logeart-Avramoglou, D., Petite, H.: Survival and function of mesenchymal stem cells (MSCs) depend on glucose to overcome exposure to long-term, severe and continuous hypoxia. J. Cell. Mol. Med. 15, 1505–1514 (2011). https://doi.org/10.1111/j.1582-4934.2010.01138.x Google Scholar
- 97.Adesida, A.B., Mulet-sierra, A., Jomha, N.M.: Hypoxia mediated isolation and expansion enhances the chondrogenic capacity of bone marrow mesenchymal stromal cells. Stem Cell Res Ther 3, 9 (2012). https://doi.org/10.1186/scrt100 Google Scholar
- 98.Freshney, R.I., Obradovic, B., Grayson, W., Cannizzaro, C., Vunjak-Novakovic, G.: Principles of tissue culture and bioreactor design. In: Lanza, R., Langer, R., Vacanti, J. (eds.) Principles of Tissue Engineering, pp. 155–183. Academic Press, San Diego (2007)Google Scholar
- 99.Nuschke, A., Rodrigues, M., Wells, A.W., Sylakowski, K., Wells, A.: Mesenchymal stem cells/multipotent stromal cells (MSCs) are glycolytic and thus glucose is a limiting factor of in vitro models of MSC starvation. Stem Cell Res. Ther. 1–9 (2016). doi: https://doi.org/10.1186/s13287-016-0436-7
- 100.Machado, N.M.: Glicose e Glutamina na Proliferação e Viabilidade de Células-Tronco Dentais Humanas (Master Thesis), Universidade Federal de São Paulo (2014)Google Scholar
- 101.Heywood, H.K., Bader, D.L., Lee, D.A.: Rate of oxygen consumption by isolated articular chondrocytes is sensitive to medium glucose concentration. J. Cell. Physiol. 206, 402–410 (2006). https://doi.org/10.1002/jcp.20491 Google Scholar
- 102.Kasinskas, R.W., Venkatasubramanian, R., Forbes, N.S.: Rapid uptake of glucose and lactate, and not hypoxia, induces apoptosis in three-dimensional tumor tissue culture. Integr. Biol. (Camb). 6, 399–410 (2014). https://doi.org/10.1039/c4ib00001c Google Scholar
- 103.Farrell, M.J., Shin, J.I., Smith, L.J., Mauck, R.L.: Functional consequences of glucose and oxygen deprivation on engineered mesenchymal stem cell-based cartilage constructs. Osteoarthr. Cartil. 23, 134–142 (2015). https://doi.org/10.1016/j.joca.2014.09.012 Google Scholar
- 104.Zhang, B., Liu, N., Shi, H., Wu, H., Gao, Y., He, H., Gu, B., Liu, H.: High-glucose microenvironments inhibit the proliferation and migration of bone mesenchymal stem cells by activating GSK3β. J. Bone Miner. Metab. 34, 140–150 (2016). https://doi.org/10.1007/s00774-015-0662-6 Google Scholar
- 105.Rogatzki, M.J., Ferguson, B.S., Goodwin, M.L., Gladden, L.B.: Lactate is always the end product of glycolysis. Front. Neurosci. 9, 1–7 (2015). https://doi.org/10.3389/fnins.2015.00022 Google Scholar
- 106.Schop, D., Janssen, F.W., van Rijn, L.D.S., Fernandes, H., Bloem, R.M., de Bruijn, J.D., van Dijkhuizen-Radersma, R.: Growth, metabolism, and growth inhibitors of mesenchymal stem cells. Tissue Eng. Part A. 15, 1877–1886 (2009). https://doi.org/10.1089/ten.tea.2008.0345 Google Scholar
- 107.Chen, T., Zhou, Y., Tan, W.: Effects of low temperature and lactate on osteogenic differentiation of human amniotic mesenchymal stem cells. Biotechnol. Bioprocess Eng. 14, 708–715 (2009). https://doi.org/10.1007/s12257-009-0034-y Google Scholar
- 108.Rödling, L., Schwedhelm, I., Kraus, S., Bieback, K., Hansmann, J., Lee-Thedieck, C.: 3D models of the hematopoietic stem cell niche under steady-state and active conditions. Sci. Rep. 7, 4625 (2017). https://doi.org/10.1038/s41598-017-04808-0 ADSGoogle Scholar
- 109.Burdick, J A, Vunjak-Novakovic, G.: Engineered microenvironments for controlled stem cell differentiation. Tissue Eng. Part A. 15, 205–219 (2009). doi: https://doi.org/10.1089/ten.tea.2008.0131
- 110.Ferrari, C., Olmos, E., Balandras, F., Tran, N., Chevalot, I., Guedon, E., Marc, A.: Investigation of growth conditions for the expansion of porcine mesenchymal stem cells on microcarriers in stirred cultures. Appl. Biochem. Biotechnol. 172, 1004–1017 (2014). https://doi.org/10.1007/s12010-013-0586-3 Google Scholar
- 111.Sart, S., Errachid, A., Schneider, Y.-J., Agathos, S.N.: Modulation of mesenchymal stem cell actin organization on conventional microcarriers for proliferation and differentiation in stirred bioreactors. J. Tissue Eng. Regen. Med. 7, 537–551 (2013). https://doi.org/10.1002/term.545 Google Scholar
- 112.Mizukami, A., Fernandes-Platzgummer, A., Carmelo, J.G., Swiech, K., Covas, D.T., Cabral, J.M.S., da Silva, C.L.: Stirred tank bioreactor culture combined with serum−/xenogeneic-free culture medium enables an efficient expansion of umbilical cord-derived mesenchymal stem/stromal cells. Biotechnol. J. 11, 1048–1059 (2016). https://doi.org/10.1002/biot.201500532 Google Scholar
- 113.Rosa, F., Sales, K.C., Carmelo, J.G., Fernandes-Platzgummer, A., da Silva, C.L., Lopes, M.B., Calado, C.R.C.: Monitoring the ex-vivo expansion of human mesenchymal stem/stromal cells in xeno-free microcarrier-based reactor systems by MIR spectroscopy. Biotechnol. Prog. 32, 447–455 (2016). https://doi.org/10.1002/btpr.2215 Google Scholar
- 114.Grein, T.A., Leber, J., Blumenstock, M., Petry, F., Weidner, T., Salzig, D., Czermak, P.: Multiphase mixing characteristics in a microcarrier-based stirred tank bioreactor suitable for human mesenchymal stem cell expansion. Process Biochem. 51, 1109–1119 (2016). https://doi.org/10.1016/j.procbio.2016.05.010 Google Scholar
- 115.Wu, X., Li, S., Lou, L., Chen, Z.: The effect of the microgravity rotating culture system on the chondrogenic differentiation of bone marrow mesenchymal stem cells. Mol. Biotechnol. 54, 331–336 (2013). https://doi.org/10.1007/s12033-012-9568-x Google Scholar
- 116.Bancroft, G.N., Sikavitsas, V.I., Mikos, A.G.: Design of a flow perfusion bioreactor system for bone tissue-engineering applications. Tissue Eng. 9, 549–554 (2003). https://doi.org/10.1089/107632703322066723 Google Scholar
- 117.Yeatts, A.B., Tubular perfusion system bioreactor for the dynamic culture of human mesenchymal stem cells (PhD Thesis), College Park (2012)Google Scholar
- 118.Cartmell, S.H., Porter, B.D., García, A.J., Guldberg, R.E.: Effects of medium perfusion rate on cell-seeded three-dimensional bone constructs in vitro. Tissue Eng. 9, 1197–1203 (2003). https://doi.org/10.1089/10763270360728107 Google Scholar
- 119.de Peppo, G.M., Sladkova, M., Sjövall, P., Palmquist, A., Oudina, K., Hyllner, J., Thomsen, P., Petite, H., Karlsson, C.: Human embryonic stem cell-derived mesodermal progenitors display substantially increased tissue formation compared to human mesenchymal stem cells under dynamic culture conditions in a packed bed/column bioreactor. Tissue Eng. Part A. 19, 175–187 (2013). https://doi.org/10.1089/ten.tea.2011.0412 Google Scholar
- 120.Ban, Y., Wu, Y., Yu, T., Geng, N., Wang, Y., Liu, X., Gong, P.: Response of osteoblasts to low fluid shear stress is time dependent. Tissue Cell. 43, 311–317 (2011). https://doi.org/10.1016/j.tice.2011.06.003 Google Scholar
- 121.Markhoff, J., Wieding, J., Weissmann, V., Pasold, J., Jonitz-Heincke, A., Bader, R.: Influence of different three-dimensional open porous titanium scaffold designs on human osteoblasts behavior in static and dynamic cell investigations. Materials (Basel). 8, 5490–5507 (2015). https://doi.org/10.3390/ma8085259 ADSGoogle Scholar
- 122.Yang, Z., Tang, Y., Li, J., Zhang, Y., Hu, X.: Facile synthesis of tetragonal columnar-shaped TiO2 nanorods for the construction of sensitive electrochemical glucose biosensor. Biosens. Bioelectron. 54, 528–533 (2014). https://doi.org/10.1016/j.bios.2013.11.043 Google Scholar
- 123.Zhang, Z., Yuan, L., Lee, P.D., Jones, E., Jones, J.R.: Modeling of time-dependent localized flow shear stress and its impact on cellular growth within additive manufactured titanium implants. J. Biomed. Mater. Res. Part B Appl. Biomater. 102, 1689–1699 (2014). https://doi.org/10.1002/jbm.b.33146 Google Scholar
- 124.Moore, M., Moore, R., McFetridge, P.S.: Directed oxygen gradients initiate a robust early remodeling response in engineered vascular grafts. Tissue Eng. Part A. 19, 2005–2013 (2013). https://doi.org/10.1089/ten.TEA.2012.0592 Google Scholar
- 125.Janssen, F.W., Oostra, J., Van Oorschot, A., Van Blitterswijk, C.A.: A perfusion bioreactor system capable of producing clinically relevant volumes of tissue-engineered bone: In vivo bone formation showing proof of concept. Biomaterials 27, 315–323 (2006). https://doi.org/10.1016/j.biomaterials.2005.07.044 Google Scholar
- 126.Liao, J., Guo, X., Grande-Allen, K.J., Kasper, F.K., Mikos, A.G.: Bioactive polymer/extracellular matrix scaffolds fabricated with a flow perfusion bioreactor for cartilage tissue engineering. Biomaterials 31, 8911–8920 (2010). https://doi.org/10.1016/j.biomaterials.2010.07.110 Google Scholar
- 127.Thibault, R.A., Mikos, A.G., Kasper, F.K.: Protein and mineral composition of osteogenic extracellular matrix constructs generated with a flow perfusion bioreactor. Biomacromolecules 12, 4204–4212 (2011). https://doi.org/10.1021/bm200975a Google Scholar
- 128.Alves da Silva, M.L., Martins, A., Costa-Pinto, A.R., Costa, P., Faria, S., Gomes, M., Reis, R.L., Neves, N.M.: Cartilage tissue engineering using electrospun PCL nanofiber meshes and MSCs. Biomacromolecules 11, 3228–3236 (2010). https://doi.org/10.1021/bm100476r Google Scholar
- 129.Gugerell, A., Neumann, A., Kober, J., Tammaro, L., Hoch, E., Schnabelrauch, M., Kamolz, L., Kasper, C., Keck, M.: Adipose-derived stem cells cultivated on electrospun l-lactide/glycolide copolymer fleece and gelatin hydrogels under flow conditions – aiming physiological reality in hypodermis tissue engineering. Burns 41, 163–171 (2015). https://doi.org/10.1016/j.burns.2014.06.010 Google Scholar
- 130.Weyand, B., Kasper, C., Israelowitz, M., Gille, C., von Schroeder, H.P., Reimers, K., Vogt, P.M.: A differential pressure laminar flow reactor supports osteogenic differentiation and extracellular matrix formation from adipose mesenchymal stem cells in a macroporous ceramic scaffold. Biores. Open Access 1, 145–156 (2012). https://doi.org/10.1089/biores.2012.9901 Google Scholar
- 131.Tsai, A.-C., Liu, Y., Ma, T.: Expansion of human mesenchymal stem cells in fibrous bed bioreactor. Biochem. Eng. J. 108, 51–57 (2016). https://doi.org/10.1016/j.bej.2015.09.002 Google Scholar
- 132.Yeatts, A.B., Both, S.K., Yang, W., Alghamdi, H.S., Yang, F., Fisher, J.P., Jansen, J.A.: In vivo bone regeneration using tubular perfusion system bioreactor cultured nanofibrous scaffolds. Tissue Eng. Part A. 20, 139–146 (2014). https://doi.org/10.1089/ten.tea.2013.0168
- 133.Kim, J., Ma, T.: Regulation of autocrine fibroblast growth factor-2 signaling by perfusion flow in 3D human mesenchymal stem cell constructs. Biotechnol. Prog. 28, 1384–1388 (2012). https://doi.org/10.1002/btpr.1604 Google Scholar
- 134.Grayson, W.L., Marolt, D., Bhumiratana, S., Fröhlich, M., Guo, X.E., Vunjak-Novakovic, G.: Optimizing the medium perfusion rate in bone tissue engineering bioreactors. Biotechnol. Bioeng. 108, 1159–1170 (2011). https://doi.org/10.1002/bit.23024 Google Scholar
- 135.Dahlin, R.L., Meretoja, V.V., Ni, M., Kasper, F.K., Mikos, A.G.: Design of a high-throughput flow perfusion bioreactor system for tissue engineering. Tissue Eng. Part C Methods. 18, 817–820 (2012). https://doi.org/10.1089/ten.tec.2012.0037 Google Scholar
- 136.Santoro, M., Lamhamedi-Cherradi, S.-E., Menegaz, B.A., Ludwig, J.A., Mikos, A.G.: Flow perfusion effects on three-dimensional culture and drug sensitivity of Ewing sarcoma. Proc. Natl. Acad. Sci. 112, 10304–10309 (2015). https://doi.org/10.1073/pnas.1506684112 ADSGoogle Scholar
- 137.Diederichs, S., Röker, S., Marten, D., Peterbauer, A., Scheper, T., van Griensven, M., Kasper, C.: Dynamic cultivation of human mesenchymal stem cells in a rotating bed bioreactor system based on the Z®RP platform. Biotechnol. Prog. 25, 1762–1771 (2009). https://doi.org/10.1002/btpr.258 Google Scholar
- 138.Neumann, A., Lavrentieva, A., Heilkenbrinker, A., Loenne, M., Kasper, C.: Characterization and application of a disposable rotating bed bioreactor for mesenchymal stem cell expansion. Bioengineering 1, 231–245 (2014). https://doi.org/10.3390/bioengineering1040231 Google Scholar
- 139.Stefani, I., Asnaghi, M.A., Cooper-White, J.J., Mantero, S.: A double chamber rotating bioreactor for enhanced tubular tissue generation from human mesenchymal stem cells. J. Tissue Eng. Regen. Med. (2017). https://doi.org/10.1002/term.2341
- 140.De Napoli, I.E., Scaglione, S., Giannoni, P., Quarto, R., Catapano, G.: Mesenchymal stem cell culture in convection-enhanced hollow fibre membrane bioreactors for bone tissue engineering. J. Memb. Sci. 379, 341–352 (2011). https://doi.org/10.1016/j.memsci.2011.06.001 Google Scholar
- 141.Li, S., Liu, Y., Zhou, Q., Lue, R., Song, L., Dong, S.-W., Guo, P., Kopjar, B.: A novel axial-stress bioreactor system combined with a substance exchanger for tissue engineering of 3D constructs. Tissue Eng. Part C. Methods. 20, 205–214 (2014). https://doi.org/10.1089/ten.TEC.2013.0173 Google Scholar
- 142.Holy, C.E., Shoichet, M.S., Davies, J.E.: Engineering three-dimensional bone tissue in vitro using biodegradable scaffolds: investigating initial cell-seeding density and culture period. J. Biomed. Mater. Res. 51, 376–382 (2000). https://doi.org/10.1002/1097 Google Scholar
- 143.Griffon, D.J., Abulencia, J.P., Ragetly, G.R., Fredericks, L.P., Chaieb, S.: A comparative study of seeding techniques and three-dimensional matrices for mesenchymal cell attachment. J. Tissue Eng. Regen. Med. 5, 169–179 (2011). https://doi.org/10.1002/term.302 Google Scholar
- 144.Yamanaka, K., Yamamoto, K., Sakai, Y., Suda, Y., Shigemitsu, Y., Kaneko, T., Kato, K., Kumagai, T., Kato, Y.: Seeding of mesenchymal stem cells into inner part of interconnected porous biodegradable scaffold by a new method with a filter paper. Dent. Mater. J. 34, 78–85 (2015). https://doi.org/10.4012/dmj.2013-330 Google Scholar
- 145.Solchaga, L.A., Tognana, E., Penick, K., Baskaran, H., Goldberg, V.M., Caplan, A.I., Welter, J.F.: A rapid seeding technique for the assembly of large cell/scaffold composite constructs. Tissue Eng. 12, 1851–1863 (2006). https://doi.org/10.1089/ten.2006.12.1851 Google Scholar
- 146.Godbey, W.T., Stacey Hindy, B.S., Sherman, M.E., Atala, A.: A novel use of centrifugal force for cell seeding into porous scaffolds. Biomaterials 25, 2799–2805 (2004). https://doi.org/10.1016/j.biomaterials.2003.09.056 Google Scholar
- 147.Ng, R., Gurm, J.S., Yang, S.-T.: Centrifugal seeding of mammalian cells in nonwoven fibrous matrices. Biotechnol. Prog. 26, n/a-n/a (2009). doi: https://doi.org/10.1002/btpr.317
- 148.Buizer, A.T., Veldhuizen, A.G., Bulstra, S.K., Kuijer, R.: Static versus vacuum cell seeding on high and low porosity ceramic scaffolds. J. Biomater. Appl. 29, 3–13 (2014). https://doi.org/10.1177/0885328213512171 Google Scholar
- 149.Wanasekara, N.D., Ghosh, S., Chen, M., Chalivendra, V.B., Bhowmick, S.: Effect of stiffness of micron/sub-micron electrospun fibers in cell seeding. J. Biomed. Mater. Res. Part A. 103, 2289–2299 (2015). https://doi.org/10.1002/jbm.a.35362 Google Scholar
- 150.Fu, W.-J., Xu, Y.-D., Wang, Z.-X., Li, G., Shi, J.-G., Cui, F.-Z., Zhang, Y., Zhang, X.: New ureteral scaffold constructed with composite poly(l-lactic acid)-collagen and urothelial cells by new centrifugal seeding system. J. Biomed. Mater. Res. Part A. 100A, 1725–1733 (2012). https://doi.org/10.1002/jbm.a.34134 Google Scholar
- 151.Kim, B.-S., Putnam, A.J., Kulik, T.J., Mooney, D.J.: Optimizing seeding and culture methods to engineer smooth muscle tissue on biodegradable polymer matrices. Biotechnol. Bioeng. 57, 46–54 (1998). https://doi.org/10.1002/(SICI)1097-0290(19980105)57:1<46::AID-BIT6>3.0.CO;2-V Google Scholar
- 152.Wendt, D., Marsano, A., Jakob, M., Heberer, M., Martin, I.: Oscillating perfusion of cell suspensions through three-dimensional scaffolds enhances cell seeding efficiency and uniformity. Biotechnol. Bioeng. 84, 205–214 (2003). https://doi.org/10.1002/bit.10759 Google Scholar
- 153.Zhao, F., Ma, T.: Perfusion bioreactor system for human mesenchymal stem cell tissue engineering: dynamic cell seeding and construct development. Biotechnol. Bioeng. 91, 482–493 (2005). https://doi.org/10.1002/bit.20532 Google Scholar
- 154.Ajalloueian, F., Lim, M.L., Lemon, G., Haag, J.C., Gustafsson, Y., Sjöqvist, S., Beltrán-Rodríguez, A., Del Gaudio, C., Baiguera, S., Bianco, A., Jungebluth, P., Macchiarini, P.: Biomechanical and biocompatibility characteristics of electrospun polymeric tracheal scaffolds. Biomaterials 35, 5307–5315 (2014). https://doi.org/10.1016/j.biomaterials.2014.03.015 Google Scholar
- 155.Ladd, M.R., Hill, T.K., Yoo, J.J., Lee, S.J.: Electrospun Nanofibers. In: Lin, T. (ed.) Tissue Engineering, Nanofibers - Production, Properties and Functional Applications. InTech (2011)Google Scholar
- 156.Barker, D.A., Bowers, D.T., Hughley, B., Chance, E.W., Klembczyk, K.J., Brayman, K.L., Park, S.S., Botchwey, E.: A: multilayer cell-seeded polymer nanofiber constructs for soft-tissue reconstruction. JAMA Otolaryngol. Head Neck Surg. 139, 914–922 (2013). https://doi.org/10.1001/jamaoto.2013.4119 Google Scholar
- 157.Dunn, J.C.Y., Chan, W.-Y., Cristini, V., Kim, J.S., Lowengrub, J., Singh, S., Wu, B.M.: Analysis of cell growth in three-dimensional scaffolds. Tissue Eng. 12, 705–716 (2006). https://doi.org/10.1089/ten.2006.12.705 Google Scholar
- 158.Papenburg, B.J., Liu, J., Higuera, G.A., Barradas, A.M.C., de Boer, J., van Blitterswijk, C.A., Wessling, M., Stamatialis, D.: Development and analysis of multi-layer scaffolds for tissue engineering. Biomaterials 30, 6228–6239 (2009). https://doi.org/10.1016/j.biomaterials.2009.07.057 Google Scholar
- 159.Srouji, S., Kizhner, T., Suss-Tobi, E., Livne, E., Zussman, E.: 3-D Nanofibrous electrospun multilayered construct is an alternative ECM mimicking scaffold. J. Mater. Sci. Mater. Med. 19, 1249–1255 (2008). https://doi.org/10.1007/s10856-007-3218-z Google Scholar
- 160.Gugerell, A., Neumann, A., Kober, J., Tammaro, L., Hoch, E., Schnabelrauch, M., Kamolz, L., Kasper, C., Keck, M.: Adipose-derived stem cells cultivated on electrospun l-lactide/glycolide copolymer fleece and gelatin hydrogels under flow conditions – aiming physiological reality in hypodermis tissue engineering. Burns 41, 163–171 (2014). https://doi.org/10.1016/j.burns.2014.06.010 Google Scholar
- 161.Ardakani, A.G., Cheema, U., Brown, R.A., Shipley, R.J.: Quantifying the correlation between spatially defined oxygen gradients and cell fate in an engineered three-dimensional culture model. J. R. Soc. Interface 11, 20140501–20140501 (2014). https://doi.org/10.1098/rsif.2014.0501 Google Scholar
- 162.Coletti, F., Macchietto, S., Elvassore, N.: Mathematical modeling of three-dimensional cell cultures in perfusion bioreactors. Ind. Eng. Chem. Res. 45, 8158–8169 (2006). https://doi.org/10.1021/ie051144v Google Scholar
- 163.Decuzzi, P., Ferrari, M.: Modulating cellular adhesion through nanotopography. Biomaterials 31, 173–179 (2010). https://doi.org/10.1016/j.biomaterials.2009.09.018 Google Scholar
- 164.Gómez-Pachón, E.Y., Sánchez-Arévalo, F.M., Sabina, F.J., Maciel-Cerda, A., Campos, R.M., Batina, N., Morales-Reyes, I., Vera-Graziano, R.: Characterisation and modelling of the elastic properties of poly(lactic acid) nanofibre scaffolds. J. Mater. Sci. 48, 8308–8319 (2013). https://doi.org/10.1007/s10853-013-7644-7 ADSGoogle Scholar
- 165.Jungreuthmayer, C., Jaasma, M.J., Al-Munajjed, A.A., Zanghellini, J., Kelly, D.J., O’Brien, F.J.: Deformation simulation of cells seeded on a collagen-GAG scaffold in a flow perfusion bioreactor using a sequential 3D CFD-elastostatics model. Med. Eng. Phys. 31, 420–427 (2009). https://doi.org/10.1016/j.medengphy.2008.11.003 Google Scholar
- 166.Ma, C.Y.J., Kumar, R., Xu, X.Y., Mantalaris, A.: A combined fluid dynamics, mass transport and cell growth model for a three-dimensional perfused bioreactor for tissue engineering of haematopoietic cells. Biochem. Eng. J. 35, 1–11 (2007). https://doi.org/10.1016/j.bej.2006.11.024 Google Scholar
- 167.McCoy, R.J., O’Brien, F.J.: Visualizing feasible operating ranges within tissue engineering systems using a “windows of operation” approach: a perfusion-scaffold bioreactor case study. Biotechnol. Bioeng. 109, 3161–3171 (2012). https://doi.org/10.1002/bit.24566 Google Scholar
- 168.Santamaría, V.A.A., Malvè, M., Duizabo, A., Mena Tobar, A., Gallego Ferrer, G., García Aznar, J.M., Doblaré, M., Ochoa, I.: Computational methodology to determine fluid related parameters of non regular three-dimensional scaffolds. Ann. Biomed. Eng. 41, 2367–2380 (2013). https://doi.org/10.1007/s10439-013-0849-8 Google Scholar
- 169.Truscello, S., Kerckhofs, G., Van Bael, S., Pyka, G., Schrooten, J., Van Oosterwyck, H.: Prediction of permeability of regular scaffolds for skeletal tissue engineering: a combined computational and experimental study. Acta Biomater. 8, 1648–1658 (2012). https://doi.org/10.1016/j.actbio.2011.12.021 Google Scholar
- 170.Yan, X., Bergstrom, D.J., Chen, X.B.: Modeling of cell cultures in perfusion bioreactors. IEEE Trans. Biomed. Eng. 59, 2568–2575 (2012). https://doi.org/10.1109/TBME.2012.2206077 Google Scholar
- 171.Akalp, U., Bryant, S.J., Vernerey, F.J.: Tuning tissue growth with scaffold degradation in enzyme-sensitive hydrogels: a mathematical model. Soft Matter 12, 7505–7520 (2016). https://doi.org/10.1039/c6sm00583g ADSGoogle Scholar
- 172.Chen, Y., Zhou, S., Li, Q.: Mathematical modeling of degradation for bulk-erosive polymers: Applications in tissue engineering scaffolds and drug delivery systems. Acta Biomater. 7, 1140–1149 (2011). https://doi.org/10.1016/j.actbio.2010.09.038 Google Scholar
- 173.Ferdous, J., Kolachalama, V.B., Shazly, T.: Impact of polymer structure and composition on fully resorbable endovascular scaffold performance. Acta Biomater. 9, 6052–6061 (2013). https://doi.org/10.1016/j.actbio.2012.12.011 Google Scholar
- 174.Heljak, M., Swieszkowski, W., Kurzydlowski, K.J.: A phenomenological model for the degradation of polymeric tissue engineering scaffolds. In: Proceedings of the International Conference on Computer Methods in Mechanics, Warsaw, Poland (2011)Google Scholar
- 175.Heljak, M., Swieszkowski, W., Kurzydlowski, K.J.: Modeling of the degradation kinetics of biodegradable scaffolds: the effects of the environmental conditions. J. Appl. Polym. Sci. 131, 1–7 (2014). https://doi.org/10.1002/app.40280 Google Scholar
- 176.Shazly, T., Kolachalama, V.B., Ferdous, J., Oberhauser, J.P., Hossainy, S., Edelman, E.R.: Assessment of material by-product fate from bioresorbable vascular scaffolds. Ann. Biomed. Eng. 40, 955–965 (2012). https://doi.org/10.1007/s10439-011-0445-8 Google Scholar
- 177.Devarapalli, M., Lawrence, B.J., Madihally, S.V.: Modeling nutrient consumptions in large flow-through bioreactors for tissue engineering. Biotechnol. Bioeng. 103, 1003–1015 (2009). https://doi.org/10.1002/bit.22333 Google Scholar
- 178.Hidalgo-Bastida, L.A., Thirunavukkarasu, S., Griffiths, S., Cartmell, S.H., Naire, S.: Modeling and design of optimal flow perfusion bioreactors for tissue engineering applications. Biotechnol. Bioeng. 109, 1095–1099 (2012). https://doi.org/10.1002/bit.24368 Google Scholar
- 179.Pathi, P., Ma, T., Locke, B.R.: Role of nutrient supply on cell growth in bioreactor design for tissue engineering of hematopoietic cells. Biotechnol. Bioeng. 89, 743–758 (2005). https://doi.org/10.1002/bit.20367 Google Scholar
- 180.Schirmaier, C., Jossen, V., Kaiser, S.C., Jüngerkes, F., Brill, S., Safavi-Nab, A., Siehoff, A., van den Bos, C., Eibl, D., Eibl, R.: Scale-up of adipose tissue-derived mesenchymal stem cell production in stirred single-use bioreactors under low-serum conditions. Eng. Life Sci. 14, 292–303 (2014). https://doi.org/10.1002/elsc.201300134 Google Scholar
- 181.Singh, H., Teoh, S.H., Low, H.T., Hutmacher, D.W.: Flow modelling within a scaffold under the influence of uni-axial and bi-axial bioreactor rotation. J. Biotechnol. 119, 181–196 (2005). https://doi.org/10.1016/j.jbiotec.2005.03.021 Google Scholar
- 182.Chung, C.A., Lin, T.-H., Chen, S.-D., Huang, H.-I.: Hybrid cellular automaton modeling of nutrient modulated cell growth in tissue engineering constructs. J. Theor. Biol. 262, 267–278 (2010). https://doi.org/10.1016/j.jtbi.2009.09.031 Google Scholar
- 183.Doagǎ, I.O., Savopol, T., Neagu, M., Neagu, A., Kovács, E.: The kinetics of cell adhesion to solid scaffolds: an experimental and theoretical approach. J. Biol. Phys. 34, 495–509 (2008). https://doi.org/10.1007/s10867-008-9108-x Google Scholar
- 184.Jeong, D., Yun, A., Kim, J.: Mathematical model and numerical simulation of the cell growth in scaffolds. Biomech. Model. Mechanobiol. 11, 677–688 (2012). https://doi.org/10.1007/s10237-011-0342-y Google Scholar
- 185.Campolo, M., Curcio, F., Soldati, A.: Minimal perfusion flow for osteogenic growth of mesenchymal stem cells on lattice scaffolds. AICHE J. 59, 3131–3144 (2013). https://doi.org/10.1002/aic.14084 Google Scholar
- 186.Causin, P., Sacco, R.: A computational model for biomass growth simulation in tissue engineering. Commun. Appl. Ind. Math. 2, (2011). https://doi.org/10.1685/journal.caim.370
- 187.Chung, C.A., Chen, C.W., Chen, C.P., Tseng, C.S.: Enhancement of cell growth in tissue-engineering constructs under direct perfusion: modeling and simulation. Biotechnol. Bioeng. 97, 1603–1616 (2007). https://doi.org/10.1002/bit.21378 Google Scholar
- 188.Flaibani, M., Magrofuoco, E., Elvassore, N.: Computational modeling of cell growth heterogeneity in a perfused 3D scaffold. Ind. Eng. Chem. Res. 49, 859–869 (2010). https://doi.org/10.1021/ie900418g Google Scholar
- 189.Lesman, A., Blinder, Y., Levenberg, S.: Modeling of flow-induced shear stress applied on 3D cellular scaffolds: implications for vascular tissue engineering. Biotechnol. Bioeng. 105, 645–654 (2010). https://doi.org/10.1002/bit.22555 Google Scholar
- 190.Liu, D., Chua, C.K., Leong, K.F.: A mathematical model for fluid shear-sensitive 3D tissue construct development. Biomech. Model. Mechanobiol. 12, 19–31 (2013). https://doi.org/10.1007/s10237-012-0378-7 Google Scholar
- 191.Porter, B., Zauel, R., Stockman, H., Guldberg, R., Fyhrie, D.: 3-D computational modeling of media flow through scaffolds in a perfusion bioreactor. J. Biomech. 38, 543–549 (2005). https://doi.org/10.1016/j.jbiomech.2004.04.011 Google Scholar
- 192.Raimondi, M.T., Boschetti, F., Falcone, L., Fiore, G.B., Remuzzi, A., Marinoni, E., Marazzi, M., Pietrabissa, R.: Mechanobiology of engineered cartilage cultured under a quantified fluid-dynamic environment. Biomech. Model. Mechanobiol. 1, 69–82 (2002). https://doi.org/10.1007/s10237-002-0007-y Google Scholar
- 193.Zhao, F., Chella, R., Ma, T.: Effects of shear stress on 3-D human mesenchymal stem cell construct development in a perfusion bioreactor system: experiments and hydrodynamic modeling. Biotechnol. Bioeng. 96, 584–595 (2007). https://doi.org/10.1002/bit.21184 Google Scholar
- 194.Doagă, I.O., Savopol, T., Neagu, M., Neagu, A., Kovács, E.: The kinetics of cell adhesion to solid scaffolds: an experimental and theoretical approach. J. Biol. Phys. 34, 495–509 (2008). https://doi.org/10.1007/s10867-008-9108-x Google Scholar
- 195.Sacco, R., Causin, P., Zunino, P., Raimondi, M.T.: A multiphysics/multiscale 2D numerical simulation of scaffold-based cartilage regeneration under interstitial perfusion in a bioreactor. Biomech. Model. Mechanobiol. 10, 577–589 (2011). https://doi.org/10.1007/s10237-010-0257-z Google Scholar