Differentiation of Wharton's Jelly-Derived Mesenchymal Stem Cells into Motor Neuron-Like Cells on Three-Dimensional Collagen-Grafted Nanofibers

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• 作者：Zohreh Bagher ; Mahmoud Azami ; Somayeh Ebrahimi-Barough…
• 关键词：Wharton’s Jelly ; derived mesenchymal stem cell ; Motor neuron differentiation ; Nanofibrous scaffolds
• 刊名：Molecular Neurobiology
• 出版年：2016
• 出版时间：May 2016
• 年：2016
• 卷：53
• 期：4
• 页码：2397-2408
• 全文大小：871 KB
• 参考文献：1.Parr AM, Kulbatski I, Zahir T, Wang X, Yue C, Keating A, Tator CH (2008) Transplanted adult spinal cord-derived neural stem/progenitor cells promote early functional recovery after rat spinal cord injury. Neuroscience 155(3):760–770CrossRef PubMed
  2.Tysseling-Mattiace VM, Sahni V, Niece KL, Birch D, Czeisler C, Fehlings MG, Stupp SI, Kessler JA (2008) Self-assembling nanofibers inhibit glial scar formation and promote axon elongation after spinal cord injury. J Neurosci 28(14):3814–3823CrossRef PubMed PubMedCentral
  3.Thuret S, Moon LD, Gage FH (2006) Therapeutic interventions after spinal cord injury. Nat Rev Neurosci 7(8):628–643CrossRef PubMed
  4.Yang F, Murugan R, Ramakrishna S, Wang X, Ma YX, Wang S (2004) Fabrication of nano-structured porous PLLA scaffold intended for nerve tissue engineering. Biomaterials 25(10):1891–1900CrossRef PubMed
  5.Parish CL, Arenas E (2007) Stem-cell-based strategies for the treatment of Parkinson’s disease. Neurodegener Dis 4(4):339–347CrossRef PubMed
  6.Winkler C, Kirik D, Bjorklund A (2005) Cell transplantation in Parkinson’s disease: how can we make it work? Trends Neurosci 28(2):86–92CrossRef PubMed
  7.Lindvall O, Kokaia Z, Martinez-Serrano A (2004) Stem cell therapy for human neurodegenerative disorders—how to make it work. Nat Med 10:42–50CrossRef
  8.Karimi-Abdolrezaee S, Eftekharpour E, Wang J, Morshead CM, Fehlings MG (2006) Delayed transplantation of adult neural precursor cells promotes remyelination and functional neurological recovery after spinal cord injury. J Neurosci 26(13):3377–3389CrossRef PubMed
  9.Parr AM, Kulbatski I, Tator CH (2007) Transplantation of adult rat spinal cord stem/progenitor cells for spinal cord injury. J Neurotrauma 24(5):835–845CrossRef PubMed
  10.Dellatore SM, Garcia AS, Miller WM (2008) Mimicking stem cell niches to increase stem cell expansion. Curr Opin Biotechnol 19(5):534–540CrossRef PubMed PubMedCentral
  11.Andrades JA, Nimni ME, Han B, Ertl DC, Hall FL, Becerra J (1996) Type I collagen combined with a recombinant TGF-beta serves as a scaffold for mesenchymal stem cells. Int J Dev Biol 1:107–108
  12.Xie J, Willerth SM, Li X, Macewan MR, Rader A, Sakiyama-Elbert SE, Xia Y (2009) The differentiation of embryonic stem cells seeded on electrospun nanofibers into neural lineages. Biomaterials 30(3):354–362CrossRef PubMed PubMedCentral
  13.Lee JY, Bashur CA, Goldstein AS, Schmidt CE (2009) Polypyrrole-coated electrospun PLGA nanofibers for neural tissue applications. Biomaterials 30(26):4325–4335CrossRef PubMed PubMedCentral
  14.Schnell E, Klinkhammer K, Balzer S, Brook G, Klee D, Dalton P, Mey J (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(19):3012–3025CrossRef PubMed
  15.Li W, Guo Y, Wang H, Shi D, Liang C, Ye Z, Qing F, Gong J (2008) Electrospun nanofibers immobilized with collagen for neural stem cells culture. J Mater Sci Mater Med 19(2):847–854CrossRef PubMed
  16.Ghasemi-Mobarakeh L, Prabhakaran MP, Morshed M, Nasr-Esfahani MH, Ramakrishna S (2008) Electrospun poly(epsilon-caprolactone)/gelatin nanofibrous scaffolds for nerve tissue engineering. Biomaterials 29(34):4532–4539CrossRef PubMed
  17.Horne MK, Nisbet DR, Forsythe JS, Parish CL (2010) Three-dimensional nanofibrous scaffolds incorporating immobilized BDNF promote proliferation and differentiation of cortical neural stem cells. Stem Cells Dev 19(6):843–852CrossRef PubMed
  18.Li WJ, Tuli R, Huang X, Laquerriere P, Tuan RS (2005) Multilineage differentiation of human mesenchymal stem cells in a three-dimensional nanofibrous scaffold. Biomaterials 26(25):5158–5166CrossRef PubMed
  19.Pettikiriarachchi JTS, Parish CL, Shoichet MS, Forsythe JS, Nisbet DR (2010) Biomaterials for brain tissue engineering. Aust J Chem 63(8):1143–1154CrossRef
  20.Wang TY, Forsythe JS, Parish CL, Nisbet DR (2012) Biofunctionalisation of polymeric scaffolds for neural tissue engineering. J Biomater Appl 27(4):369–390CrossRef PubMed
  21.Nisbet DR, Forsythe JS, Shen W, Finkelstein DI, Horne MK (2009) A review of the cellular response on electrospun nanofibers for tissue engineering. J Biomater Appl 24(1):7–29CrossRef PubMed
  22.Kim CH, Khil MS, Kim HY, Lee HU, Jahng KY (2006) An improved hydrophilicity via electrospinning for enhanced cell attachment and proliferation. J Biomed Mater Res B Appl Biomater 78(2):283–290CrossRef PubMed
  23.Duan Y, Wang Z, Yan W, Wang S, Zhang S, Jia J (2007) Preparation of collagen-coated electrospun nanofibers by remote plasma treatment and their biological properties. J Biomater Sci Polym 18(9):1153–1164CrossRef
  24.Ma Z, Gao C, Gong Y, Shen J (2005) Cartilage tissue engineering PLLA scaffold with surface immobilized collagen and basic fibroblast growth factor. Biomaterials 26(11):1253–1259CrossRef PubMed
  25.Wang Y, Lu L, Zheng Y, Chen X (2006) Improvement in hydrophilicity of PHBV films by plasma treatment. J Biomed Mater Res A 76(3):589–595CrossRef PubMed
  26.Ho MH, Hou LT, Tu CY, Hsieh HJ, Lai JY, Chen WJ, Wang DM (2006) Promotion of cell affinity of porous PLLA scaffolds by immobilization of RGD peptides via plasma treatment. Macromol Biosci 6(1):90–98CrossRef PubMed
  27.Shih YRV, Chen CN, Tsai SW, Wang YJ, Lee OK (2006) Growth of mesenchymal stem cells on electrospun type I collagen nanofibers. Stem Cells 24(11):2391–2397CrossRef PubMed
  28.Prabhakaran MP, Venugopal J, Chan CK, Ramakrishna S (2008) Surface modified electrospun nanofibrous scaffolds for nerve tissue engineering. Nanotechnology 19(45):455102CrossRef PubMed
  29.Venugopal J, Low S, Choon AT, Kumar AB, Ramakrishna S (2008) Electrospun-modified nanofibrous scaffolds for the mineralization of osteoblast cells. J Biomed Mater Res A 85(2):408–417CrossRef PubMed
  30.Chen YC, Lee DC, Hsiao CY, Chung YF, Chen HC, Thomas JP, Pong WF, Tai NH, Lin IN, Chiu IM (2009) The effect of ultra-nanocrystalline diamond films on the proliferation and differentiation of neural stem cells. Biomaterials 30(20):3428–3435CrossRef PubMed
  31.Zhao C, Tan A, Pastorin G, Ho HK (2013) Nanomaterial scaffolds for stem cell proliferation and differentiation in tissue engineering. Biotechnol Adv 31(5):654–668CrossRef PubMed
  32.Vercelli A, Mereuta OM, Garbossa D, Muraca G, Mareschi K, Rustichelli D, Ferrero I, Mazzini L, Madon E, Fagioli F (2008) Human mesenchymal stem cell transplantation extends survival, improves motor performance and decreases neuroinflammation in mouse model of amyotrophic lateral sclerosis. Neurobiol Dis 31(3):395–405CrossRef PubMed
  33.Bouchez G, Sensebé L, Vourc’h P, Garreau L, Bodard S, Rico A, Guilloteau D, Charbord P, Besnard JC, Chalon S (2008) Partial recovery of dopaminergic pathway after graft of adult mesenchymal stem cells in a rat model of Parkinson’s disease. Neurochem Int 52(7):1332–1342CrossRef PubMed
  34.Forraz N, McGuckin CP (2011) The umbilical cord: a rich and ethical stem cell source to advance regenerative medicine. Cell Prolif 44(1):60–69CrossRef PubMed
  35.Romanov YA, Svintsitskaya VA, Smirnov VN (2003) Searching for alternative source of postnatal human mesenchymal stem cells; candidate MSC-like cells from umbilical cord. Stem Cells 21(1):105–110CrossRef PubMed
  36.Mitchell KE, Weiss ML, Mitchell BM, Martin P, Davis D, Morales L, Helwig B, Beerenstrauch M, Abou-Easa K, Hildreth T, Troyer D, Medicetty S (2003) Matrix cells from Wharton’s Jelly from neurons and glia. Stem Cells 21(1):50–60CrossRef PubMed
  37.Sarugaser R, Lickorish D, Baksh D, Hosseini MM, Davies JE (2005) Human umbilical cord perivascular (HUCPV) cells: a source of mesenchymal progenitors. Stem Cells 23(2):220–229CrossRef PubMed
  38.Paldino E, Cenciarelli C, Giampaolo A, Milazzo L, Pescatori M, Hassan HJ, Casalbore P (2014) Induction of dopaminergic neurons from human Wharton’s jelly mesenchymal stem cell by forskolin. J Cell Physiol 229(2):232–244CrossRef PubMed
  39.Yang F, Xu CY, Kotaki M, Wang S, Ramakrishna S (2004) Characterization of neural stem cells on electrospun poly(L-lactic acid) nanofibrous scaffold. J Biomater Sci Polym Ed 15(12):1483–1497CrossRef PubMed
  40.Chen F, Lee CN, Teoh SH (2007) Nanofibrous modification on ultra-thin poly(e-caprolactone) membrane via electrospinning. Mater Sci Eng 27(2):325–332CrossRef
  41.Prabhakaran MP, Venugopal JR, Ramakrishna S (2009) Mesenchymal stem cell differentiation to neuronal cells on electrospun nanofibrous substrates for nerve tissue engineering. Biomaterials 30(28):4996–5003CrossRef PubMed
  42.Wang J, Ye R, Wei Y, Wang H, Xu X, Zhang F, Qu J, Zuo B, Zhang H (2012) The effects of electrospun TSF nanofiber diameter and alignment on neuronal differentiation of human embryonic stem cells. J Biomed Mater Res A 100(3):632–645CrossRef PubMed
  43.Binan L, Tendey C, De Crescenzo G, El Ayoubi R, Ajji A, Jolicoeur M (2014) Differentiation of neuronal stem cells into motor neurons using electrospun poly-L-lactic acid/gelatin scaffold. Biomaterials 35(2):664–674CrossRef PubMed
  44.Liqing Y, Jia G, Jiqing C, Ran G, Fei C, Jie K, Yanyun W, Cheng Z (2011) Directed differentiation of motor neuron cell-like cells from human adipose-derived stem cells in vitro. Neuroreport 22(8):370–373CrossRef PubMed
  45.Wu CY, Whye D, Mason RW, Wang W (2012) Efficient differentiation of mouse embryonic stem cells into motor neurons. J Vis Exp 9(64), e3813
  46.Wichterle H, Lieberam I, Porter JA, Jessell TM (2002) Directed differentiation of embryonic stem cells into motor neurons. Cell 110(3):385–397CrossRef PubMed
  47.Luca AC, Mersch S, Deenen R, Schmidt S, Messner I, Schäfer KL, Baldus SE, Huckenbeck W, Piekorz RP, Knoefel WT, Krieg A, Stoecklein NH (2013) Impact of the 3D microenvironment on phenotype, gene expression, and EGFR inhibition of colorectal cancer cell lines. PLoS One 8(3), e59689CrossRef PubMed PubMedCentral
  48.Niknamasl A, Ostad SN, Soleimani M, Azami M, Salmani MK, Lotfibakhshaiesh N, Ebrahimi-Barough S, Karimi R, Roozafzoon R, Ai J (2014 ) A new approach for pancreatic tissue engineering: human endometrial stem cells encapsulated in fibrin gel can differentiate to pancreatic islet beta-cell. Cell Biol Int 38(10):1174–1182
  49.Asmani MN, Ai J, Amoabediny G, Noroozi A, Azami M, Ebrahimi-Barough S, Navaei-Nigjeh M, Ai A, Jafarabadi M (2013) Three-dimensional culture of differentiated endometrial stromal cells to oligodendrocyte progenitor cells (OPCs) in fibrin hydrogel. Cell Biol Int 37(12):1340–1349
  50.Sumanasinghe RD, Bernacki SH, Loboa EG (2006) Osteogenic differentiation of human mesenchymal stem cells in collagen matrices: effect of uniaxial cyclic tensile strain on bone morphogenetic protein (BMP-2) mRNA expression. Tissue Eng 12(12):3459–3465CrossRef PubMed
  51.Lund AW, Stegemann JP, Plopper GE (2009) Inhibition of ERK promotes collagen gel compaction and fibrillogenesis to amplify the osteogenesis of human mesenchymal stem cells in three-dimensional collagen I culture. Stem Cells Dev 18(2):331–341CrossRef PubMed PubMedCentral
  52.Walther C, Gruss P (1991) Pax-6, a murine paired box gene, is expressed in the developing CNS. Development 113(4):1435–1449PubMed
  53.Hendrickson ML, Rao AJ, Demerdash ON, Kalil RE (2011) Expression of nestin by neural cells in the adult rat and human brain. PLoS One 6(4), e18535CrossRef PubMed PubMedCentral
  54.Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126(4):677–689CrossRef PubMed
  55.Peyton SR, Putnam AJ (2005) Extracellular matrix rigidity governs smoth muscle cell motility in a biphasic fashion. J Cell Physiol 204(1):918–923CrossRef
  56.Troyer DL, Weiss ML (2008) Wharton’s jelly-derived cells are a primitive stromal cell population. Stem Cells 26(3):591–599CrossRef PubMed PubMedCentral
  57.Can A, Karahuseyinoglu S (2007) Concise review: human umbilical cord stroma with regard to the source of fetus-derived stem cells. Stem Cells 25(11):2886–2895CrossRef PubMed
  58.Weiss ML, Medicetty S, Bledsoe AR, Rachakatla RS, Choi M, Merchav S, Luo Y, Rao MS, Velagaleti G, Troyer D (2006) Human umbilical cord matrix stem cells: preliminary characterization and effect of transplantation in a rodent model of Parkinson’s disease. Stem Cells 24(3):781–792CrossRef PubMed
  59.La Rocca G, Anzalone R, Corrao S, Magno F, Loria T, Lo Iacono M, Di Stefano A, Giannuzzi P, Marasà L, Cappello F, Zummo G, Farina F (2009) Isolation and characterization of Oct-4þ/HLA-Gþ mesenchymal stem cells from human umbilical cord matrix: differentiation potential and detection of new markers. Histochem Cell Biol 131(2):267–282CrossRef PubMed
  60.Fong C-Y, Chak L-L, Biswas A, Tan J-H, Gauthaman K, Chan W-K, Bongso A (2011) Human Wharton’s jelly stem cells have unique transcriptome profiles compared to human embryonic stem cells and other mesenchymal stem cells. Stem Cell Rev Rep 7(1):1–16CrossRef
  61.Fong CY, Richards M, Manasi N, Biswas A, Bongso A (2007) Comparative growth behaviour and characterization of stem cells from human Wharton’s jelly. Reprod BioMed Online 15(6):708–718CrossRef PubMed
  62.Prabhakaran MP, Venugopal JR, Chyan TT, Hai LB, Chan CK, Lim AY, Ramakrishna S (2008) Electrospun biocomposite nanofibrous scaffolds for neural tissue engineering. Tissue Eng A 14(11):1787–1797CrossRef
  63.Ebrahimi-Barough S, Javidan JA, Saberi H, Joghataei MT, Rahbarghazi R, Mirzaei E, Faghihi F, Shirian S, Ai A, Ai J (2014) Evaluation of motor Neuron-like cell differentiation of hEnSCs on biodegradable PLGA nanofiber Scaffolds. Mol Neurobiol. doi:10.​1007/​s12035-014-8931-2
  64.Ebrahimi-Barough S, Hoveizi E, Norouzi Javidan A, Ai J (2015) Investigating the neuroglial differentiation effect of neuroblastoma conditioned medium in human endometrial stem cells cultured on 3D nanofibrous scaffold. J Biomed Mater Res A. doi:10.​1002/​jbm.​a.​35397
  
• 作者单位：Zohreh Bagher (1)
  Mahmoud Azami (2)
  Somayeh Ebrahimi-Barough (2) (3)
  Hamid Mirzadeh (4)
  Atefeh Solouk (5)
  Mansooreh Soleimani (1) (6) (7)
  Jafar Ai (2) (3)
  Mohammad Reza Nourani (8)
  Mohammad Taghi Joghataei (1) (6) (7)
  
  1. Department of Tissue Engineering and Regenerative Medicine, School of Advanced Technologies in Medicine, Iran University of Medical Sciences, Tehran, Iran
  2. Department of Tissue Engineering and Applied Cell Sciences, School of Advanced Technologies in Medicine, Tehran University of Medical Sciences, Tehran, Iran
  3. Brain and Spinal Injury Research Center, Imam Khomeini Hospital, Tehran University of Medical Sciences, Tehran, Iran
  4. Polymer Engineering Faculty, Amirkabir University of Technology (Tehran Polytechnic), Tehran, Iran
  5. Biomedical Engineering Faculty, Amirkabir University of Technology (Tehran Polytechnic), Tehran, Iran
  6. Cellular and Molecular Research Center, Iran University of Medical Sciences, Tehran, Iran
  7. Department of Anatomy, Faculty of Medicine, Iran University of Medical Sciences, Tehran, Iran
  8. Tissue Engineering Division, Biotechnology Research Center, Baqiyatallah University of Medical Sciences, Tehran, Iran
  
• 刊物主题：Neurosciences; Neurobiology; Cell Biology; Neurology;
• 出版者：Springer US
• ISSN：1559-1182

文摘

Cell transplantation strategies have provided potential therapeutic approaches for treatment of neurodegenerative diseases. Mesenchymal stem cells from Wharton’s jelly (WJMSCs) are abundant and available adult stem cells with low immunological incompatibility, which could be considered for cell replacement therapy in the future. However, MSC transplantation without any induction or support material causes poor control of cell viability and differentiation. In this study, we investigated the effect of the nanoscaffolds on WJMSCs differentiation into motor neuronal lineages in the presence of retinoic acid (RA) and sonic hedgehog (Shh). Surface properties of scaffolds have been shown to significantly influence cell behaviors such as adhesion, proliferation, and differentiation. Therefore, polycaprolactone (PCL) nanofibers were constructed via electrospinning, surface modified by plasma treatment, and grafted by collagen. Characterization of the scaffolds by means of ATR-FTIR, contact angel, and Bradford proved grafting of the collagen on the surface of the scaffolds. WJMSCs were seeded on nanofibrous and tissue culture plate (TCP) and viability of WJMSCs were measured by MTT assay and then induced to differentiate into motor neuron-like cells for 15 days. Differentiated cells were evaluated morphologically, and real-time PCR and immunocytochemistry methods were done to evaluate expression of motor neuron-like cell markers in mRNA and protein levels. Our results showed that obtained cells could express motor neuron biomarkers at both RNA and protein levels, but the survival and differentiation of WJMSCs into motor neuron-like cells on the PCL/collagen scaffold were higher than cultured cells in the TCP and PCL groups. Taken together, WJMSCs are an attractive stem cell source for inducing into motor neurons in vitro especially when grown on nanostructural scaffolds and PCL/collagen scaffolds can provide a suitable, three-dimensional situation for neuronal survival and differentiation that suggest their potential application towards nerve regeneration.