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The Differentiation of Human Endometrial Stem Cells into Neuron-Like Cells on Electrospun PAN-Derived Carbon Nanofibers with Random and Aligned Topographies

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Abstract

Electrospun carbon nanofibers (CNFs) have great potential for applications in neural tissue regeneration due to their electrical conductivity, biocompatibility, and morphological similarity to natural extracellular matrix. In this study, we cultured human endometrial stem cells (hEnSCs) on electrospun CNFs with random and aligned topographies and demonstrated that hEnSCs could attach, proliferate, and differentiate into neural cells on both random and aligned CNFs. However, the proliferation, differentiation, and morphology of cells were affected by CNF morphology. Under the proliferative condition, hEnSCs showed lower proliferation on aligned CNFs than on random CNFs and on tissue culture plate (TCP) control. When cultured on aligned CNFs in neural induction media, hEnSCs showed significant upregulation of neuronal markers, NF-H and Tuj-1, and downregulation of neural progenitor marker (nestin) compared to that on random CNFs and on TCP. In contrast, hEnSCs showed higher expression of nestin and slight upregulation of oligodendrocyte marker (OLIG-2) on random CNFs compared to that on aligned CNFs and on TCP. SEM imaging revealed that differentiated cells extended along the CNF main axis on aligned CNFs but stretched multidirectionally on random CNFs. These findings suggest electrospun CNFs as proper substrate for stem cell differentiation into specific neural cells.

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References

  1. Nunes A, Al-Jamal K, Nakajima T, Hariz M, Kostarelos K (2012) Application of carbon nanotubes in neurology: clinical perspectives and toxicological risks. Arch Toxicol 86(7):1009–1020

    Article  CAS  PubMed  Google Scholar 

  2. Tran PA, Zhang L, Webster TJ (2009) Carbon nanofibers and carbon nanotubes in regenerative medicine. Adv Drug Deliv Rev 61(12):1097–1114

    Article  CAS  PubMed  Google Scholar 

  3. Wilkinson AE, McCormick AM, Leipzig ND (2011) Central nervous system tissue engineering: current considerations and strategies. Synthesis Lectures on Tissue Eng 3(2):1–120

    Article  Google Scholar 

  4. Silva GA (2006) Neuroscience nanotechnology: progress, opportunities and challenges. Nat Rev Neurosci 7(1):65–74

    Article  CAS  PubMed  Google Scholar 

  5. Lee W, Parpura V (2009) Carbon nanotubes as substrates/scaffolds for neural cell growth. Prog Brain Res 180:110–125

    Article  PubMed  Google Scholar 

  6. Fraczek-Szczypta A (2014) Carbon nanomaterials for nerve tissue stimulation and regeneration. Mater Sci Eng C 34:35–49

    Article  CAS  Google Scholar 

  7. Galvan-Garcia P, Keefer EW, Yang F, Zhang M, Fang S, Zakhidov AA, Baughman RH, Romero MI (2007) Robust cell migration and neuronal growth on pristine carbon nanotube sheets and yarns. J Biomater Sci Polym Ed 18(10):1245–1261

    Article  CAS  PubMed  Google Scholar 

  8. Hu H, Ni Y, Montana V, Haddon RC, Parpura V (2004) Chemically functionalized carbon nanotubes as substrates for neuronal growth. Nano Lett 4(3):507–511

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Matsumoto K, Sato C, Naka Y, Kitazawa A, Whitby RL, Shimizu N (2007) Neurite outgrowths of neurons with neurotrophin-coated carbon nanotubes. J Biosci Bioeng 103(3):216–220

    Article  CAS  PubMed  Google Scholar 

  10. Ni Y, Hu H, Malarkey EB, Zhao B, Montana V, Haddon RC, Parpura V (2005) Chemically functionalized water soluble single-walled carbon nanotubes modulate neurite outgrowth. J Nanosci Nanotechnol 5(10):1707–1712

    Article  CAS  PubMed  Google Scholar 

  11. Tay CY, Gu H, Leong WS, Yu H, Li HQ, Heng BC, Tantang H, Loo SCJ et al (2010) Cellular behavior of human mesenchymal stem cells cultured on single-walled carbon nanotube film. Carbon 48(4):1095–1104

    Article  CAS  Google Scholar 

  12. Mattson MP, Haddon RC, Rao AM (2000) Molecular functionalization of carbon nanotubes and use as substrates for neuronal growth. J Mol Neurosci 14(3):175–182

    Article  CAS  PubMed  Google Scholar 

  13. Lovat V, Pantarotto D, Lagostena L, Cacciari B, Grandolfo M, Righi M, Spalluto G, Prato M et al (2005) Carbon nanotube substrates boost neuronal electrical signaling. Nano Lett 5(6):1107–1110

    Article  CAS  PubMed  Google Scholar 

  14. Chao T-I, Xiang S, Chen C-S, Chin W-C, Nelson A, Wang C, Lu J (2009) Carbon nanotubes promote neuron differentiation from human embryonic stem cells. Biochem Biophys Res Commun 384(4):426–430

    Article  CAS  PubMed  Google Scholar 

  15. Kam NWS, Jan E, Kotov NA (2008) Electrical stimulation of neural stem cells mediated by humanized carbon nanotube composite made with extracellular matrix protein. Nano Lett 9(1):273–278

    Article  Google Scholar 

  16. Dalby MJ, Gadegaard N, Tare R, Andar A, Riehle MO, Herzyk P, Wilkinson CD, Oreffo RO (2007) The control of human mesenchymal cell differentiation using nanoscale symmetry and disorder. Nat Mater 6(12):997–1003

    Article  CAS  PubMed  Google Scholar 

  17. Christopherson GT, Song H, Mao H-Q (2009) The influence of fiber diameter of electrospun substrates on neural stem cell differentiation and proliferation. Biomaterials 30(4):556–564

    Article  CAS  PubMed  Google Scholar 

  18. Malarkey EB, Fisher KA, Bekyarova E, Liu W, Haddon RC, Parpura V (2008) Conductive single-walled carbon nanotube substrates modulate neuronal growth. Nano Lett 9(1):264–268

    Article  Google Scholar 

  19. Nguyen-Vu TB, Chen H, Cassell AM, Andrews RJ, Meyyappan M, Li J (2007) Vertically aligned carbon nanofiber architecture as a multifunctional 3-D neural electrical interface. Biomed Eng IEEE Trans on 54(6):1121–1128

    Article  Google Scholar 

  20. McKenzie JL, Waid MC, Shi R, Webster TJ (2004) Decreased functions of astrocytes on carbon nanofiber materials. Biomaterials 25(7):1309–1317

    Article  CAS  PubMed  Google Scholar 

  21. Nataraj S, Yang K, Aminabhavi T (2012) Polyacrylonitrile-based nanofibers—a state-of-the-art review. Prog Polym Sci 37(3):487–513

    Article  CAS  Google Scholar 

  22. Bhardwaj N, Kundu SC (2010) Electrospinning: a fascinating fiber fabrication technique. Biotechnol Adv 28(3):325–347

    Article  CAS  PubMed  Google Scholar 

  23. Rahaman M, Ismail AF, Mustafa A (2007) A review of heat treatment on polyacrylonitrile fiber. Polym Degrad Stab 92(8):1421–1432

    Article  CAS  Google Scholar 

  24. Jain S, Sharma A, Basu B (2013) In vitro cytocompatibility assessment of amorphous carbon structures using neuroblastoma and Schwann cells. J Biomed Mater Res B Appl Biomater 101(4):520–531

    Article  PubMed  Google Scholar 

  25. Jain S, Webster TJ, Sharma A, Basu B (2013) Intracellular reactive oxidative stress, cell proliferation and apoptosis of Schwann cells on carbon nanofibrous substrates. Biomaterials 34(21):4891–4901

    Article  CAS  PubMed  Google Scholar 

  26. Ebrahimi-Barough S, Javidan AN, 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: 1–10

  27. Mobarakeh ZT, Ai J, Yazdani F, Sorkhabadi SMR, Ghanbari Z, Javidan AN, Mortazavi‐Tabatabaei SAR, Massumi M et al (2012) Human endometrial stem cells as a new source for programming to neural cells. Cell Biol Int Rep 19(1):7–14

    Article  Google Scholar 

  28. Tavakol S, Aligholi H, Gorji A, Eshaghabadi A, Hoveizi E, Tavakol B, Rezayat SM, Ai J (2014) Thermogel nanofiber induces human endometrial‐derived stromal cells to neural differentiation: in vitro and in vivo studies in rat. J Biomed Mater Res A 102(12):4590–4597

    PubMed  Google Scholar 

  29. Tavakol S, Saber R, Hoveizi E, Aligholi H, Ai J, Rezayat SM (2015) Chimeric Self-assembling Nanofiber Containing Bone Marrow Homing Peptide’s Motif Induces Motor Neuron Recovery in Animal Model of Chronic Spinal Cord Injury; an In Vitro and In Vivo Investigation. Mol Neurobiol: 1–11

  30. Mirzaei E, Ai J, Sorouri M, Ghanbari H, Verdi J, Faridi-Majidi R (2015) Functionalization of PAN-based electrospun carbon nanofibers by acid oxidation: study of structural, electrical and mechanical properties. Fullerenes, Nanotubes, Carbon Nanostruct 23(11):930–937. doi:10.1080/1536383x.2015.1020057

    Article  CAS  Google Scholar 

  31. Ebrahimi-Barough S, Kouchesfahani HM, Ai J, Massumi M (2013) Differentiation of human endometrial stromal cells into oligodendrocyte progenitor cells (OPCs). J Mol Neurosci 51(2):265–273

    Article  CAS  PubMed  Google Scholar 

  32. Zhang J, Loya P, Peng C, Khabashesku V, Lou J (2012) Quantitative in situ mechanical characterization of the effects of chemical functionalization on individual carbon nanofibers. Adv Funct Mater 22(19):4070–4077

    Article  CAS  Google Scholar 

  33. Dongil A, Bachiller-Baeza B, Guerrero-Ruiz A, Rodríguez-Ramos I, Martínez-Alonso A, Tascón J (2011) Surface chemical modifications induced on high surface area graphite and carbon nanofibers using different oxidation and functionalization treatments. J Colloid Interface Sci 355(1):179–189

    Article  CAS  PubMed  Google Scholar 

  34. Zussman E, Chen X, Ding W, Calabri L, Dikin D, Quintana J, Ruoff R (2005) Mechanical and structural characterization of electrospun PAN-derived carbon nanofibers. Carbon 43(10):2175–2185

    Article  CAS  Google Scholar 

  35. Zhou Z, Lai C, Zhang L, Qian Y, Hou H, Reneker DH, Fong H (2009) Development of carbon nanofibers from aligned electrospun polyacrylonitrile nanofiber bundles and characterization of their microstructural, electrical, and mechanical properties. Polymer 50(13):2999–3006

    Article  CAS  Google Scholar 

  36. Wang G, Pan C, Wang L, Dong Q, Yu C, Zhao Z, Qiu J (2012) Activated carbon nanofiber webs made by electrospinning for capacitive deionization. Electrochim Acta 69:65–70

    Article  CAS  Google Scholar 

  37. Yim EK, Pang SW, Leong KW (2007) Synthetic nanostructures inducing differentiation of human mesenchymal stem cells into neuronal lineage. Exp Cell Res 313(9):1820–1829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Lim SH, Liu XY, Song H, Yarema KJ, Mao H-Q (2010) The effect of nanofiber-guided cell alignment on the preferential differentiation of neural stem cells. Biomaterials 31(34):9031–9039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Gulacsi AA, Anderson SA (2008) β-catenin–mediated Wnt signaling regulates neurogenesis in the ventral telencephalon. Nat Neurosci 11(12):1383–1391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Yamada M, Tanemura K, Okada S, Iwanami A, Nakamura M, Mizuno H, Ozawa M, Ohyama‐Goto R et al (2007) Electrical stimulation modulates fate determination of differentiating embryonic stem cells. Stem Cells 25(3):562–570

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This project was supported by Tehran University of Medical Sciences (TUMS), grant No. 91-04-87-20021.

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Authors and Affiliations

  1. Department of Medical Nanotechnology, School of Advanced Technologies in Medicine, Tehran University of Medical Sciences, Tehran, Iran

    Esmaeil Mirzaei, Hossein Ghanbari & Reza Faridi-Majidi

  2. Department of Medical Nanotechnology, School of Advanced Medical Sciences and Technologies, Shiraz University of Medical Sciences, Shiraz, Iran

    Esmaeil Mirzaei

  3. Department of Tissue Engineering, School of Advanced Technologies in Medicine, Tehran University of Medical Sciences, Tehran, Iran

    Jafar Ai & Somayeh Ebrahimi-Barough

  4. Department of Applied Cell Sciences, School of Advanced Technologies in Medicine, Tehran University of Medical Sciences, Tehran, Iran

    Javad Verdi

Authors
  1. Esmaeil Mirzaei
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  2. Jafar Ai
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  3. Somayeh Ebrahimi-Barough
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  4. Javad Verdi
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  5. Hossein Ghanbari
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  6. Reza Faridi-Majidi
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Correspondence to Reza Faridi-Majidi.

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Mirzaei, E., Ai, J., Ebrahimi-Barough, S. et al. The Differentiation of Human Endometrial Stem Cells into Neuron-Like Cells on Electrospun PAN-Derived Carbon Nanofibers with Random and Aligned Topographies. Mol Neurobiol 53, 4798–4808 (2016). https://doi.org/10.1007/s12035-015-9410-0

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  • DOI: https://doi.org/10.1007/s12035-015-9410-0

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