Promoting differentiation of human adipose mesenchymal stem cells into oligodendrocyte-like cells and neuron-like cells through coculture on decellularized sciatic nerves

Authors

  • Carlos I. Valencia-Salgado Departamento de Bioquímica y Medicina Molecular, Facultad de Medicina, Universidad Autónoma de Nuevo León, Monterrey 64460, Mexico https://orcid.org/0000-0003-3470-4105
  • Selene Jacobo-Arreola Departamento de Bioquímica y Medicina Molecular, Facultad de Medicina, Universidad Autónoma de Nuevo León, Monterrey 64460, Mexico https://orcid.org/0000-0003-4866-0959
  • Salvado L. Said-Fernandez Departamento de Bioquímica y Medicina Molecular, Facultad de Medicina, Universidad Autónoma de Nuevo León, Monterrey 64460, Mexico https://orcid.org/0000-0001-8710-9460
  • Adolfo Soto-Dominguez Departamento de Histologia, Facultad de Medicina, Universidad Autónoma de Nuevo León, Monterrey 64460, Mexico https://orcid.org/0000-0002-4144-5474
  • Alberto Camacho-Morales Departamento de Bioquímica y Medicina Molecular, Facultad de Medicina, Universidad Autónoma de Nuevo León, Monterrey 64460, Mexico https://orcid.org/0000-0002-2588-9489
  • Herminia G. Martinez-Rodriguez Departamento de Bioquímica y Medicina Molecular, Facultad de Medicina, Universidad Autónoma de Nuevo León, Monterrey 64460, Mexico https://orcid.org/0000-0001-8801-0999
  • Humberto Rodriguez-Rocha Departamento de Histologia, Facultad de Medicina, Universidad Autónoma de Nuevo León, Monterrey 64460, Mexico
  • Paulina Delgado-Gonzalez Departamento de Bioquímica y Medicina Molecular, Facultad de Medicina, Universidad Autónoma de Nuevo León, Monterrey 64460, Mexico https://orcid.org/0000-0002-0492-7968
  • Adriana G. Quiroz-Reyes Departamento de Bioquímica y Medicina Molecular, Facultad de Medicina, Universidad Autónoma de Nuevo León, Monterrey 64460, Mexico https://orcid.org/0000-0002-9405-7483
  • Jose F. Islas Departamento de Bioquímica y Medicina Molecular, Facultad de Medicina, Universidad Autónoma de Nuevo León, Monterrey 64460, Mexico
  • Elsa N. Garza-Treviño Departamento de Bioquímica y Medicina Molecular, Facultad de Medicina, Universidad Autónoma de Nuevo León, Monterrey 64460, Mexico https://orcid.org/0000-0002-1042-4603

DOI:

https://doi.org/10.48797/sl.2022.3

Keywords:

scaffolds, adipose tissue-derived mesenchymal stem cells, oligodendrocyte-like cells, sciatic nerve

Abstract

We evaluated cell markers of oligodendrocyte-like cells (OLC) and neuron-like cells (NLC) differentiation from human adipose tissue-derived mesenchymal stem cells (hADSCs) cocultured on decellularized sciatic nerves. OLC and NLC were incubated at a 10:1 ratio with decellularized rat nerves. We estimated the percentage of myelin basic protein (MBP)- and neurofilament protein (NFP)-positive cells. OLC and NLC cocultures showed an increase in positive cells for MBP and proteolipid protein (PLP) markers. Oligodendrocytes and neurons cocultured with sciatic nerve scaffolds promoted myelination by OLC within 3 days, which remained stable for at least 21 days. We propose a reproducible experimental strategy to promote sciatic nerve myelination by coculturing hADSCs-derived OLC and NLC in nerve scaffolds.

References

Lloyd, A.F.; Miron, V.E. The Pro-Remyelination Properties of Microglia in the Central Nervous System. Nat. Rev. Neurol. 2019, 15, 447–458.

Simons, M.; Nave, K.A. Oligodendrocytes: Myelination and Axonal Support. Cold Spring Harb. Perspect. Biol. 2016, 8, 1–16, doi:10.1101/cshperspect.a020479.

Kuhn, S.; Gritti, L.; Crooks, D.; Dombrowsky, Y. Oligodendrocytes in Development, Myelin Generation and Beyond. Cells 2019, 8, doi:10.1016/j.coms.2016.10.001.

Foerster, S.; Hill, M.F.E.; Franklin, R.J.M. Diversity in the Oligodendrocyte Lineage: Plasticity or Heterogeneity? Glia 2019, 67, 1–9, doi:10.1002/glia.23607.

Peschl, P.; Bradl, M.; Höftberger, R.; Berger, T.; Reindl, M. Myelin Oligodendrocyte Glycoprotein: Deciphering a Target in Inflammatory Demyelinating Diseases. Front. Immunol. 2017, 8.

Santos, A.K.; Vieira, M.S.; Vasconcellos, R.; Goulart, V.A.M.; Kihara, A.H.; Resende, R.R. Decoding Cell Signalling and Regulation of Oligodendrocyte Differentiation. Semin. Cell Dev. Biol. 2019, 95, 54–73.

Lee, J.Y.; Petratos, S. Thyroid Hormone Signaling in Oligodendrocytes: From Extracellular Transport to Intracellular Signal. Mol. Neurobiol. 2016, 53, 6568–6583.

Jure, I.; De Nicola, A.F.; Labombarda, F. Progesterone Effects on Oligodendrocyte Differentiation in Injured Spinal Cord. Brain Res. 2019, 1708, 36–46, doi:10.1016/j.brainres.2018.12.005.

Wrigley, S.; Arafa, D.; Tropea, D. Insulin-like Growth Factor 1: At the Crossroads of Brain Development and Aging. Front. Cell. Neurosci. 2017, 11, 14, doi:10.3389/fncel.2017.00014.

Cheli, V.T.; Correale, J.; Paez, P.M.; Pasquini, J.M. Iron Metabolism in Oligodendrocytes and Astrocytes, Implications for Myelination and Remyelination. ASN Neuro 2020, 12, 175909142096268, doi:10.1177/1759091420962681.

Abbaszadeh, H.A.; Tiraihi, T.; Delshad, A.R.; Saghedizadeh, M.; Taheri, T.; Kazemi, H.; Hassoun, H.K. Differentiation of Neurosphere-Derived Rat Neural Stem Cells into Oligodendrocyte-like Cells by Repressing PDGF-α and Olig2 with Triiodothyronine. Tissue Cell 2014, 46, 462–469, doi:10.1016/j.tice.2014.08.003.

Marisca, R.; Hoche, T.; Agirre, E.; Hoodless, L.J.; Barkey, W.; Auer, F.; Castelo-Branco, G.; Czopka, T. Functionally Distinct Subgroups of Oligodendrocyte Precursor Cells Integrate Neural Activity and Execute Myelin Formation. Nat. Neurosci. 2020, 23, 363–374, doi:10.1038/s41593-019-0581-2.

Marton, R.M.; Miura, Y.; Sloan, S.A.; Li, Q.; Revah, O.; Levy, R.J.; Huguenard, J.R.; Pașca, S.P. Differentiation and Maturation of Oligodendrocytes in Human Three-Dimensional Neural Cultures. Nat. Neurosci. 2019, 22, 484–491, doi:10.1038/s41593-018-0316-9.

Amr, S.M.; Gouda, A.; Koptan, W.T.; Galal, A.A.; Abdel-Fattah, D.S.; Rashed, L.A.; Atta, H.M.; Abdel-Aziz, M.T. Bridging Defects in Chronic Spinal Cord Injury Using Peripheral Nerve Grafts Combined with a Chitosan-Laminin Scaffold and Enhancing Regeneration through Them by Co-Transplantation with Bone-Marrow-Derived Mesenchymal Stem Cells: Case Series of 14 Patient. J. Spinal Cord Med. 2014, 37, 54–71, doi:10.1179/2045772312Y.0000000069.

Xing, H.; Yin, H.; Sun, C.; Ren, X.; Tian, Y.; Yu, M.; Jiang, T. Preparation of an Acellular Spinal Cord Scaffold to Improve Its Biological Properties. Mol. Med. Rep. 2019, 20, 1075–1084, doi:10.3892/mmr.2019.10364.

Abbaszadeh, H.-A.; Tiraihi, T.; Delshad, A.R.; Saghedi Zadeh, M.; Taheri, T. Bone Marrow Stromal Cell Transdifferentiation into Oligodendrocyte-like Cells Using Triiodothyronine as a Inducer with Expression of Platelet-Derived Growth Factor α as a Maturity Marker. Iran. Biomed. J. 2013, 17, 62–70, doi:10.6091/IBJ.11162.2013.

Jang, S.; Cho, H.H.; Cho, Y.B.; Park, J.S.; Jeong, H.S. Functional Neural Differentiation of Human Adipose Tissue-Derived Stem Cells Using BFGF and Forskolin. BMC Cell Biol. 2010, 11, doi:10.1186/1471-2121-11-25.

García-Pérez, M.M.; Martínez-Rodríguez, H.G.; López-Guerra, G.G.; Soto-Domínguez, A.; Said-Fernández, S.L.; Morales-Avalos, R.; Elizondo-Omaña, R.E.; Montes-de-Oca-Luna, R.; Guzmán-López, S.; Castillo-Galván, M.L.; et al. A Modified Chemical Protocol of Decellularization of Rat Sciatic Nerve and Its Recellularization with Mesenchymal Differentiated Schwann-like Cells: Morphological and Functional Assessments. Histol. Histopathol. 2017, 32, 779–792, doi:10.14670/HH-11-844.

Dash, B.C.; Xu, Z.; Lin, L.; Koo, A.; Ndon, S.; Berthiaume, F.; Dardik, A.; Hsia, H. Stem Cells and Engineered Scaffolds for Regenerative Wound Healing. Bioengineering 2018, 5.

Yin, H.; Jiang, T.; Deng, X.; Yu, M.; Xing, H.; Ren, X. A Cellular Spinal Cord Scaffold Seeded with Rat Adipose-Derived Stem Cells Facilitates Functional Recovery via Enhancing Axon Regeneration in Spinal Cord Injured Rats. Mol. Med. Rep. 2018, 17, 2998–3004, doi:10.3892/mmr.2017.8238.

Yamashita, T.; Miyamoto, Y.; Bando, Y.; Ono, T.; Kobayashi, S.; Doi, A.; Araki, T.; Kato, Y.; Shirakawa, T.; Suzuki, Y.; et al. Differentiation of Oligodendrocyte Progenitor Cells from Dissociated Monolayer and Feeder-Free Cultured Pluripotent Stem Cells. PLoS One 2017, 12, e0171947, doi:10.1371/journal.pone.0171947.

Fitzsimmons, R.E.B.; Mazurek, M.S.; Soos, A.; Simmons, C.A. Mesenchymal Stromal/Stem Cells in Regenerative Medicine and Tissue Engineering. Stem Cells Int. 2018, 2018, doi:10.1155/2018/8031718.

Zhou, Z.; Chen, Y.; Zhang, H.; Min, S.; Yu, B.; He, B.; Jin, A. Comparison of Mesenchymal Stromal Cells from Human Bone Marrow and Adipose Tissue for the Treatment of Spinal Cord Injury. Cytotherapy 2013, 15, 434–448, doi:10.1016/j.jcyt.2012.11.015.

Nazm Bojnordi, M.; Movahedin, M.; Tiraihi, T.; Javan, M.; Ghasemi Hamidabadi, H. Oligoprogenitor Cells Derived from Spermatogonia Stem Cells Improve Remyelination in Demyelination Model. Mol. Biotechnol. 2014, 56, 387–393, doi:10.1007/s12033-013-9722-0.

Ebrahimi-Barough, S.; Kouchesfahani, H.M.; Ai, J.; Massumi, M. Differentiation of Human Endometrial Stromal Cells into Oligodendrocyte Progenitor Cells (OPCs). J. Mol. Neurosci. 2013, 51, 265–273, doi:10.1007/s12031-013-9957-z.

Terzic, D.; Maxon, J.R.; Krevitt, L.; Dibartolomeo, C.; Goyal, T.; Low, W.C.; Dutton, J.R.; Parr, A.M. Directed Differentiation of Oligodendrocyte Progenitor Cells from Mouse Induced Pluripotent Stem Cells. Cell Transplant. 2016, 25, 411–424, doi:10.3727/096368915X688137.

Ehrlich, M.; Mozafari, S.; Glatza, M.; Starost, L.; Velychko, S.; Hallmann, A.L.; Cui, Q.L.; Schambach, A.; Kim, K.P.; Bachelin, C.; et al. Rapid and Efficient Generation of Oligodendrocytes from Human Induced Pluripotent Stem Cells Using Transcription Factors. Proc. Natl. Acad. Sci. U. S. A. 2017, 114, 1–10, doi:10.1073/pnas.1614412114.

Jang, S.; Cho, H.-H.; Cho, Y.-B.; Park, J.-S.; Jeong, H.-S. Functional Neural Differentiation of Human Adipose Tissue-Derived Stem Cells Using BFGF and Forskolin. BMC Cell Biol. 2010, 11, 25, doi:10.1186/1471-2121-11-25.

Ruiz-Sauri, A.; Orduña-Valls, J.M.; Blasco-Serra, A.; Tornero-Tornero, C.; Cedeño, D.L.; Bejarano-Quisoboni, D.; Valverde-Navarro, A.A.; Benyamin, R.; Vallejo, R. Glia to Neuron Ratio in the Posterior Aspect of the Human Spinal Cord at Thoracic Segments Relevant to Spinal Cord Stimulation. J. Anat. 2019, 235, 997–1006, doi:10.1111/joa.13061.

Kroehne, V.; Tsata, V.; Marrone, L.; Froeb, C.; Reinhardt, S.; Gompf, A.; Dahl, A.; Sterneckert, J.; Reimer, M.M. Primary Spinal OPC Culture System from Adult Zebrafish to Study Oligodendrocyte Differentiation In Vitro. Front. Cell. Neurosci. 2017, 11, doi:10.3389/fncel.2017.00284.

Domingues, H.S.; Cruz, A.; Chan, J.R.; Relvas, J.B.; Rubinstein, B.; Pinto, I.M. Mechanical Plasticity during Oligodendrocyte Differentiation and Myelination. Glia 2018, 66, 5–14, doi:10.1002/glia.23206.

Furusho, M.; Ishii, A.; Bansal, R. Signaling by FGF Receptor 2 , Not FGF Receptor 1 , Regulates Myelin Thickness through Activation of ERK1 / 2 – MAPK , Which Promotes MTORC1 Activity in an Akt-Independent Manner. 2017, 37, 2931–2946, doi:10.1523/JNEUROSCI.3316-16.2017.

Singh, M.; Vaishnav, P.K.; Dinda, A.K.; Mohanty, S. Evaluation of Priming E Ffi Ciency of Forskolin in Tissue-Specific Human Mesenchymal Stem Cells Into. Cells 2020, 9, 1–18, doi:10.3390/cells9092058.

Makhija, E.P.; Espinosa-Hoyos, D.; Jagielska, A.; Van Vliet, K.J. Mechanical Regulation of Oligodendrocyte Biology. Neurosci. Lett. 2020, 717, 134673.

Nakada, M.; Itoh, S.; Tada, K.; Matsuta, M.; Murai, A.; Tsuchiya, H. Effects of Hybridization of Decellularized Allogenic Nerves with Adipose-Derive Stem Cell Sheets to Facilitate Nerve Regeneration. Brain Res. 2020, 1746, doi:10.1016/j.brainres.2020.147025.

Rbia, N.; Bulstra, L.F.; Bishop, A.T.; Van Wijnen, A.J.; Shin, A.Y. A Simple Dynamic Strategy to Deliver Stem Cells to Decellularized Nerve Allografts. Plast. Reconstr. Surg. 2018, 142, 402–413, doi:10.1097/PRS.0000000000004614.

Volarevic, V.; Markovic, B.S.; Gazdic, M.; Volarevic, A.; Jovicic, N.; Arsenijevic, N.; Armstrong, L.; Djonov, V.; Lako, M.; Stojkovic, M. Ethical and Safety Issues of Stem Cell-Based Therapy. Int. J. Med. Sci. 2018, 15, 36–45.

Porzionato, A.; Stocco, E.; Barbon, S.; Grandi, F.; Macchi, V.; De Caro, R. Tissue-Engineered Grafts from Human Decellularized Extracellular Matrices: A Systematic Review and Future Perspectives. Int. J. Mol. Sci. 2018, 19, doi:10.3390/ijms19124117.

Nomura, H.; Tator, C.H.; Shoichet, M.S. Bioengineered Strategies for Spinal Cord Repair. J. Neurotrauma 2006, 23, 496–507, doi:10.1089/neu.2006.23.496.

Philips, C.; Cornelissen, M.; Carriel, V. Evaluation Methods as Quality Control in the Generation of Decellularized Peripheral Nerve Allografts. J. Neural Eng. 2018, 15.

Gilpin, A.; Yang, Y. Decellularization Strategies for Regenerative Medicine: From Processing Techniques to Applications. Biomed Res. Int. 2017, 2017.

Agmon, G.; Christman, K.L. Controlling Stem Cell Behavior with Decellularized Extracellular Matrix Scaffolds. Curr. Opin. Solid State Mater. Sci. 2016, 20, 193–201.

Howard, D.; Buttery, L.D.; Shakesheff, K.M.; Roberts, S.J. Tissue Engineering: Strategies, Stem Cells and Scaffolds. J. Anat. 2008, 213, 66–72.

Brill, C.; Scheuer, T.; Bührer, C.; Endesfelder, S.; Schmitz, T. Oxygen Impairs Oligodendroglial Development via Oxidative Stress and Reduced Expression of HIF-1α. Sci. Rep. 2017, 7, 1–14, doi:10.1038/srep43000.

Zambuto, S.G.; Clancy, K.B.H.; Harley, B.A.C. A Gelatin Hydrogel to Study Endometrial Angiogenesis and Trophoblast Invasion. Interface Focus 2019, 9, doi:10.1098/rsfs.2019.0016.

Lovett, M.; Lee, K.; Edwards, A.; Kaplan, D.L. Vascularization Strategies for Tissue Engineering. Tissue Eng. - Part B Rev. 2009, 15, 353–370.

Wang, S.; Bates, J.; Li, X.; Schanz, S.; Chandler-Militello, D.; Levine, C.; Maherali, N.; Studer, L.; Hochedlinger, K.; Windrem, M.; et al. Human IPSC-Derived Oligodendrocyte Progenitor Cells Can Myelinate and Rescue a Mouse Model of Congenital Hypomyelination. Cell Stem Cell 2013, 12, 252–264, doi:10.1016/j.stem.2012.12.002.

Cerqueira, S.R.; Lee, Y.S.; Cornelison, R.C.; Mertz, M.W.; Wachs, R.A.; Schmidt, C.E.; Bunge, M.B. Decellularized Peripheral Nerve Supports Schwann Cell Transplants and Axon Growth Following Spinal Cord Injury. Biomaterials 2018, 177, 176–185, doi:10.1016/j.biomaterials.2018.05.049.

Marquardt, L.M.; Doulames, V.M.; Wang, A.T.; Dubbin, K.; Suhar, R.A.; Kratochvil, M.J.; Medress, Z.A.; Plant, G.W.; Heilshorn, S.C. Designer, Injectable Gels to Prevent Transplanted Schwann Cell Loss during Spinal Cord Injury Therapy. Sci. Adv. 2020, 6, doi:10.1126/sciadv.aaz1039.

Katoh, H.; Yokota, K.; Fehlings, M.G. Regeneration of Spinal Cord Connectivity through Stem Cell Transplantation and Biomaterial Scaffolds. Front. Cell. Neurosci. 2019, 13, doi:10.3389/fncel.2019.00248.

Promoting differentiation of adipose mesenchymal stem cells

Downloads

Published

2022-04-15

How to Cite

Valencia-Salgado, C., Jacobo-Arreola, S., Said-Fernandez, S., Soto-Dominguez, A., Camacho-Morales, A., Martinez-Rodriguez, H., Rodriguez-Rocha, H., Delgado-Gonzalez, P., Quiroz-Reyes, A., Islas, J., & Garza-Treviño, E. (2022). Promoting differentiation of human adipose mesenchymal stem cells into oligodendrocyte-like cells and neuron-like cells through coculture on decellularized sciatic nerves. Scientific Letters, 1(1), 2. https://doi.org/10.48797/sl.2022.3

Issue

Section

Research Articles