Tailor-Made Electrospun Culture Scaffolds Control Human Neural Progenitor Cell Behavior—Studies on Cellular Migration and Phenotypic Differentiation — Oak Academic Publishing
Research ArticleOpen AccessGoogle Scholar indexed
Tailor-Made Electrospun Culture Scaffolds Control Human Neural Progenitor Cell Behavior—Studies on Cellular Migration and Phenotypic Differentiation
Department of Clinical Sciences in Lund, Division of Ophthalmology, Lund University, Lund, Sweden
,
Department of Biology, Section Functional Zoology, Lund University, Lund, Sweden
,
Department of Biology, Section Functional Zoology, Lund University, Lund, Sweden
1 Department of Clinical Sciences in Lund, Division of Ophthalmology, Lund University, Lund, Sweden
2 Department of Biology, Section Functional Zoology, Lund University, Lund, Sweden
3 Department of Biology, Section Functional Zoology, Lund University, Lund, Sweden
In neuroscience research, cell culture systems are essential experimental platforms. It is of great interest to explore in vivo -like culture substrates. We explored how basic properties of neural cells, nuclei polarization, phenotypic differentiation and distribution/migration, were affected by the culture at poly-L-lactic acid (PLLA) fibrous scaffolds, using a multipotent mitogen-expanded human neural progenitor cell (HNPC) line. HNPCs were seeded, at four different surfaces: two different electrospun PLLA (d = 1.2 - 1.3 μm) substrates (parallel or random aligned fibers), and planar PLL- and PLLA surfaces. Nuclei analysis demonstrated a non-directed cellular migration at planar surfaces and random fibers, different from cultures at aligned fibers where HNPCs were oriented parallel with the fibers. At aligned fibers, HNPCs displayed the same capacity for phenotypic differentiation as after culture on the planar surfaces. However, at random fibers, HNPCs showed a significant lower level of phenotypic differentiation compared with cultures at the planar surfaces. A clear trend towards greater neuronal formation at aligned fibers, compared to cultures at random fibers, was noted. We demonstrated that the topography of in vivo -resembling PLLA scaffolds significantly influences HNPC behavior, proven by different migration behavior, phenotypic differentiation potential and nuclei polarization. This knowledge is useful in future exploration of in vivo -resembling neural cell system using electrospun scaffolds.
Agarwal, S., Wendorff, J.H. and Greiner, A. (2009) Progress in the Field of Electrospinning for Tissue Engineering Applications. Advanced Materials, 21, 3343-3351. https://doi.org/10.1002/adma.200803092
Dalby, M.J., Gadegaard, N. and Oreffo, R.O. (2014) Harnessing Nanotopography and Integrin-Matrix Interactions to Influence Stem Cell Fate. Nature Materials, 13, 558-569. https://doi.org/10.1038/nmat3980
Kang, K., Kim, M.H., Park, M. and Choi, I.S. (2014) Neurons on Nanotopographies: Behavioral Responses and Biological Implications. Journal of Nanoscience and Nanotechnology, 14, 513-521. https://doi.org/10.1166/jnn.2014.8764
Tsimbouri, P., Gadegaard, N., Burgess, K., White, K., Reynolds, P., Herzyk, P., et al. (2014) Nanotopographical Effects on Mesenchymal Stem Cell Morphology and Phenotype. Journal of Cellular Biochemistry, 115, 380-390. https://doi.org/10.1002/jcb.24673
Vidu, R., Rahman, M., Mahmoudi, M., Enachescu, M., Poteca, T.D. and Opris, I. (2014) Nanostructures: A Platform for Brain Repair and Augmentation. Frontiers in Systems Neuroscience, 8, 91. https://doi.org/10.3389/fnsys.2014.00091
Vasita, R. and Katti, D.S. (2006) Nanofibers and Their Applications in Tissue Engineering. International Journal of Nanomedicine, 1, 15-30. https://doi.org/10.2147/nano.2006.1.1.15
Braghirolli, D.I., Steffens, D. and Pranke, P. (2014) Electrospinning for Regenerative Medicine: A Review of the Main Topics. Drug Discovery Today, 19, 743-753. https://doi.org/10.1016/j.drudis.2014.03.024
Bourke, J.L., Coleman, H.A., Pham, V., Forsythe, J.S. and Parkington, H.C. (2014) Neuronal Electrophysiological Function and Control of Neurite Outgrowth on Electrospun Polymer Nanofibers Are Cell Type Dependent. Tissue Engineering Part A, 20, 1089-1095. https://doi.org/10.1089/ten.tea.2013.0295
Lee, J.Y., Bashur, C.A., Gomez, N., Goldstein, A.S. and Schmidt, C.E. (2010) Enhanced Polarization of Embryonic Hippocampal Neurons on Micron Scale Electrospun Fibers. Journal of Biomedical Materials Research Part A, 92, 1398-1406.
Nisbet, D.R., Pattanawong, S., Ritchie, N.E., Shen, W., Finkelstein, D.I., Horne, M.K., et al. (2007) Interaction of Embryonic Cortical Neurons on Nanofibrous Scaffolds for Neural Tissue Engineering. Journal of Neural Engineering, 4, 35-41. https://doi.org/10.1088/1741-2560/4/2/004
Rahjouei, A., Kiani, S., Zahabi, A., Mehrjardi, N.Z., Hashemi, M., et al. (2011) Interactions of Human Embryonic Stem Cell-Derived Neural Progenitors with an Electrospun Nanofibrillar Surface in Vitro. The International Journal of Artificial Organs, 34, 559-570.
Xie, J., Willerth, S.M., Li, X., Macewan, M.R., Rader, A., Sakiyama-Elbert, S.E., et al. (2009) The Differentiation of Embryonic Stem Cells Seeded on Electrospun Nanofibers into Neural Lineages. Biomaterials, 30, 354-362. https://doi.org/10.1016/j.biomaterials.2008.09.046
Schnell, E., Klinkhammer, K., Balzer, S., Brook, G., Klee, D., Dalton, P., et al. (2007) Guidance of Glial Cell Migration and Axonal Growth on Electrospun Nanofibers of Poly-Epsilon-Caprolactone and a Collagen/Poly-Epsilon-Caprolactone Blend. Biomaterials, 28, 3012-3025. https://doi.org/10.1016/j.biomaterials.2007.03.009
Corey, J.M., Gertz, C.C., Wang, B.S., Birrell, L.K., Johnson, S.L., Martin, D.C., et al. (2008) The Design of Electrospun PLLA Nanofiber Scaffolds Compatible with Serum-Free Growth of Primary Motor and Sensory Neurons. Acta Biomaterialia, 4, 863-875. https://doi.org/10.1016/j.actbio.2008.02.020
Wang, H.B., Mullins, M.E., Cregg, J.M., Hurtado, A., Oudega, M., Trombley, M.T., et al. (2009) Creation of Highly Aligned Electrospun Poly-L-Lactic Acid Fibers for Nerve Regeneration Applications. Journal of Neural Engineering, 6, Article ID: 016001. https://doi.org/10.1088/1741-2560/6/1/016001
Biazar, E., Khorasani, M.T., Montazeri, N., Pourshamsian, K., Daliri, M., et al. (2010) Types of Neural Guides and Using Nanotechnology for Peripheral Nerve Reconstruction. International Journal of Nanomedicine, 5, 839-852. https://doi.org/10.2147/IJN.S11883
Gupta, D., Venugopal, J., Prabhakaran, M.P., Giri Dev, V.R., Low, S., Choon, A.T., et al. (2009) Aligned and Random Nanofibrous Substrate for the in Vitro Culture of Schwann Cells for Neural Tissue Engineering. Acta Biomaterialia, 5, 2560-2569. https://doi.org/10.1016/j.actbio.2009.01.039
Kim, Y.T., Haftel, V.K., Kumar, S. and Bellamkonda, R.V. (2008) The Role of Aligned Polymer Fiber-Based Constructs in the Bridging of Long Peripheral Nerve Gaps. Biomaterials, 29, 3117-3127. https://doi.org/10.1016/j.biomaterials.2008.03.042
Leach, M.K., Feng, Z.Q., Gertz, C.C., Tuck, S.J., Regan, T.M., Naim, Y., et al. (2011) The Culture of Primary Motor and Sensory Neurons in Defined Media on Electrospun Poly-L-Lactide Nanofiber Scaffolds. Journal of Visualized Experiments, 48, e2389. https://doi.org/10.3791/2389
Liu, J.J., Wang, C.Y., Wang, J.G., Ruan, H.J. and Fan, C.Y. (2011) Peripheral Nerve Regeneration Using Composite Poly (Lactic Acid-Caprolactone)/Nerve Growth Factor Conduits Prepared by Coaxial Electrospinning. Journal of Biomedical Materials Research Part A, 96, 13-20. https://doi.org/10.1002/jbm.a.32946
Zamani, F., Amani-Tehran, M., Latifi, M., Shokrgozar, M.A. and Zaminy, A. (2014) Promotion of Spinal Cord Axon Regeneration by 3D Nanofibrous Core-Sheath Scaffolds. Journal of Biomedical Materials Research Part A, 102, 506-513. https://doi.org/10.1002/jbm.a.34703
Nisbet, D.R., Rodda, A.E., Horne, M.K., Forsythe, J.S. and Finkelstein, D.I. (2009) Neurite Infiltration and Cellular Response to Electrospun Polycaprolactone Scaffolds Implanted into the Brain. Biomaterials, 30, 4573-4580. https://doi.org/10.1016/j.biomaterials.2009.05.011
Kador, K.E. and Goldberg, J.L. (2012) Scaffolds and Stem Cells: Delivery of Cell Transplants for Retinal Degenerations. Expert Review of Ophthalmology, 7, 459-470. https://doi.org/10.1586/eop.12.56
Zalis, M.C., Johansson, S., Johansson, F. and Johansson, U.E. (2016) Exploration of Physical and Chemical Cues on Retinal Cell Fate. Molecular and Cellular Neuroscience, 75, 122-132. https://doi.org/10.1016/j.mcn.2016.07.006
Christophersen, N.S., Meijer, X., Jorgensen, J.R., Englund, U., Gronborg, M., Seiger, A., et al. (2006) Induction of Dopaminergic Neurons from Growth Factor Expanded Neural Stem/Progenitor Cell Cultures Derived from Human First Trimester Forebrain. Brain Research Bulletin, 70, 457-466. https://doi.org/10.1016/j.brainresbull.2006.07.001
Englund, U., Bjorklund, A. and Wictorin, K. (2002) Migration Patterns and Phenotypic Differentiation of Long-Term Expanded Human Neural Progenitor Cells after Transplantation into the Adult Rat Brain. Developmental Brain Research, 134, 123-141. https://doi.org/10.1016/S0165-3806(01)00330-3
Englund, U., Fricker-Gates, R.A., Lundberg, C., Bjorklund, A. and Wictorin, K. (2002) Transplantation of Human Neural Progenitor Cells into the Neonatal Rat Brain: Extensive Migration and Differentiation with Long-Distance Axonal Projections. Experimental Neurology, 173, 1-21. https://doi.org/10.1006/exnr.2001.7750
Englund-Johansson, U., Mohlin, C., Liljekvist-Soltic, I., Ekstrom, P. and Johansson, K. (2010) Human Neural Progenitor Cells Promote Photoreceptor Survival in Retinal Explants. Experimental Eye Research, 90, 292-299. https://doi.org/10.1016/j.exer.2009.11.005
Novozhilova, E., Olivius, P., Siratirakun, P., Lundberg, C. and Englund-Johansson, U. (2013) Neuronal Differentiation and Extensive Migration of Human Neural Precursor Cells following Co-Culture with Rat Auditory Brainstem Slices. PLoS ONE, 8, e57301. https://doi.org/10.1371/journal.pone.0057301
Parmar, M., Skogh, C. and Englund, U. (2003) A Transplantation Study of Expanded Human Embryonic Forebrain Precursors: Evidence for Selection of a Specific Progenitor Population. Molecular and Cellular Neuroscience, 23, 531-543. https://doi.org/10.1016/S1044-7431(03)00097-6
Jiao, Y., Palmgren, B., Novozhilova, E., Englund Johansson, U., Spieles-Engemann, A.L., et al. (2014) BDNF Increases Survival and Neuronal Differentiation of Human Neural Precursor Cells Cotransplanted with a Nanofiber Gel to the Auditory Nerve in a Rat Model of Neuronal Damage. BioMed Research International, 2014, Article ID: 356415. https://doi.org/10.1155/2014/356415
Kale, A., Novozhilova, E., Englund-Johansson, U., Stupp, S., Palmgren, B. and Olivius, P. (2014) Exogenous BDNF and Chondroitinase ABC Consisted Biomimetic Microenvironment Regulates Survival, Migration and Differentiation of Human Neural Progenitor Cells Transplanted into a Rat Auditory Nerve. Neuroscience & Medicine, 5, 86-100. https://doi.org/10.4236/nm.2014.52012
Carpenter, M.K., Cui, X., Hu, Z.Y., Jackson, J., Sherman, S., Seiger, A., et al. (1999) In Vitro Expansion of a Multipotent Population of Human Neural Progenitor Cells. Experimental Neurology, 158, 265-278. https://doi.org/10.1006/exnr.1999.7098
Niu, W., Zang, T., Zou, Y., Fang, S., Smith, D.K., Bachoo, R., et al. (2013) In Vivo Reprogramming of Astrocytes to Neuroblasts in the Adult Brain. Nature Cell Biology, 15, 1164-1175. https://doi.org/10.1038/ncb2843
Bramanti, V., Tomassoni, D., Avitabile, M., Amenta, F. and Avola, R. (2010) Biomarkers of Glial Cell Proliferation and Differentiation in Culture. Frontiers in Bioscience (Scholar Edition), 2, 558-570.
Hwang, C.M., Sant, S., Masaeli, M., Kachouie, N.N., Zamanian, B., et al. (2010) Fabrication of Three-Dimensional Porous Cell-Laden Hydrogel for Tissue Engineering. Biofabrication, 2, Article ID: 035003. https://doi.org/10.1088/1758-5082/2/3/035003
Pardo, B. and Honegger, P. (2000) Differentiation of Rat Striatal Embryonic Stem Cells in Vitro: Monolayer Culture vs. Three-Dimensional Coculture with Differentiated Brain Cells. Journal of Neuroscience Research, 59, 504-512. https://doi.org/10.1002/(SICI)1097-4547(20000215)59:4 3.0.CO;2-N
Li, M., Mondrinos, M.J., Chen, X. and Lelkes, P.I. (2005) Electrospun Blends of Natural and Synthetic Polymers as Scaffolds for Tissue Engineering. Conference Proceedings of IEEE Engineering in Medicine and Biology Society, 6, 5858-5861.
Lim, S.H. and Mao, H.Q. (2009) Electrospun Scaffolds for Stem Cell Engineering. Advanced Drug Delivery Reviews, 61, 1084-1096. https://doi.org/10.1016/j.addr.2009.07.011
Ostenfeld, T., Joly, E., Tai, Y.T., Peters, A., Caldwell, M., et al. (2002) Regional Specification of Rodent and Human Neurospheres. Developmental Brain Research, 134, 43-55. https://doi.org/10.1016/S0165-3806(01)00291-7
Valiente, M. and Marin, O. (2010) Neuronal Migration Mechanisms in Development and Disease. Current Opinion in Neurobiology, 20, 68-78. https://doi.org/10.1016/j.conb.2009.12.003
Evsyukova, I., Plestant, C. and Anton, E.S. (2013) Integrative Mechanisms of Oriented Neuronal Migration in the Developing Brain. Annual Review of Cell and Developmental Biology, 29, 299-353. https://doi.org/10.1146/annurev-cellbio-101512-122400
Campbell, K. and Gotz, M. (2002) Radial Glia: Multi-Purpose Cells for Vertebrate Brain Development. Trends in Neurosciences, 25, 235-238. https://doi.org/10.1016/S0166-2236(02)02156-2
Kriegstein, A.R. and Noctor, S.C. (2004) Patterns of Neuronal Migration in the Embryonic Cortex. Trends in Neurosciences, 27, 392-399. https://doi.org/10.1016/j.tins.2004.05.001
Marin, O., Valdeolmillos, M. and Moya, F. (2006) Neurons in Motion: Same Principles for Different Shapes? Trends in Neurosciences, 29, 655-661. https://doi.org/10.1016/j.tins.2006.10.001
Doyle, A.D., Wang, F.W., Matsumoto, K. and Yamada, K.M. (2009) One-Dimensional Topography Underlies Three-Dimensional Fibrillar Cell Migration. The Journal of Cell Biology, 184, 481-490. https://doi.org/10.1083/jcb.200810041
Wright, L.S., Prowse, K.R., Wallace, K., Linskens, M.H. and Svendsen, C.N. (2006) Human Progenitor Cells Isolated from the Developing Cortex Undergo Decreased Neurogenesis and Eventual Senescence following Expansion in Vitro. Experimental Cell Research, 312, 2107-2120. https://doi.org/10.1016/j.yexcr.2006.03.012
Keenan, T.M., Nelson, A.D., Grinager, J.R., Thelen, J.C. and Svendsen, C.N. (2010) Real Time Imaging of Human Progenitor Neurogenesis. PLoS ONE, 5, e13187. https://doi.org/10.1371/journal.pone.0013187
Anderson, L., Burnstein, R.M., He, X., Luce, R., Furlong, R., Foltynie, T., et al. (2007) Gene Expression Changes in Long Term Expanded Human Neural Progenitor Cells Passaged by Chopping Lead to Loss of Neurogenic Potential in Vivo. Experimental Neurology, 204, 512-524. https://doi.org/10.1016/j.expneurol.2006.12.025
Grealishemail, S., Diguet, E., Kirkeby, A., Mattsson, B., Heuer, A., Bramoulle, Y., Van Camp, N., Perrier, A.L., Hantraye, P., Bjorklund, A. and Parmaremail, M. (2014) Human ESC-Derived Dopamine Neurons Show Similar Preclinical Efficacy and Potency to Fetal Neurons When Grafted in a Rat Model of Parkinson’s Disease. Cell Stem Cell, 15, 653-665. https://doi.org/10.1016/j.stem.2014.09.017
Shahbazi, E., Kiani, S., Gourabi, H. and Baharvand, H. (2011) Electrospun Nanofibrillar Surfaces Promote Neuronal Differentiation and Function from Human Embryonic Stem Cells. Tissue Engineering Part A, 17, 3021-3031. https://doi.org/10.1089/ten.tea.2011.0121
den Braber, E.T., de Ruijter, J.E., Ginsel, L.A., von Recum, A.F. and Jansen, J.A. (1998) Orientation of ECM Protein Deposition, Fibroblast Cytoskeleton, and Attachment Complex Components on Silicone Microgrooved Surfaces. Journal of Biomedical Materials Research Part A, 40, 291-300. https://doi.org/10.1002/(SICI)1097-4636(199805)40:2 3.0.CO;2-P
den Braber, E.T., de Ruijter, J.E., Ginsel, L.A., von Recum, A.F. and Jansen, J.A. (1996) Quantitative Analysis of Fibroblast Morphology on Microgrooved Surfaces with Various Groove and Ridge Dimensions. Biomaterials, 17, 2037-2044. https://doi.org/10.1016/0142-9612(96)00032-4
Dalby, M.J. (2005) Topographically Induced Direct Cell Mechanotransduction. Medical Engineering and Physics, 27, 730-742. https://doi.org/10.1016/j.medengphy.2005.04.005
Smeal, R.M., Rabbitt, R., Biran, R. and Tresco, P.A. (2005) Substrate Curvature Influences the Direction of Nerve Outgrowth. Annals of Biomedical Engineering, 33, 376-382. https://doi.org/10.1007/s10439-005-1740-z
Dunn, G.A. and Heath, J.P. (1976) A New Hypothesis of Contact Guidance in Tissue Cells. Experimental Cell Research, 101, 1-14. https://doi.org/10.1016/0014-4827(76)90405-5
Teixeira, A.I., McKie, G.A., Foley, J.D., Bertics, P.J., Nealey, P.F., et al. (2006) The Effect of Environmental Factors on the Response of Human Corneal Epithelial Cells to Nanoscale Substrate Topography. Biomaterials, 27, 3945-3954. https://doi.org/10.1016/j.biomaterials.2006.01.044
Rajnicek, A., Britland, S. and McCaig, C. (1997) Contact Guidance of CNS Neurites on Grooved Quartz: Influence of Groove Dimensions, Neuronal Age and Cell Type. Journal of Cell Science, 110, 2905-2913.