Bioprocess and Biosystems Engineering

, Volume 39, Issue 7, pp 1163–1172 | Cite as

The nanofibrous PAN-PANi scaffold as an efficient substrate for skeletal muscle differentiation using satellite cells

  • Simzar Hosseinzadeh
  • Matin Mahmoudifard
  • Farzaneh Mohamadyar-Toupkanlou
  • Masomeh Dodel
  • Atena Hajarizadeh
  • Mahdi Adabi
  • Masoud SoleimaniEmail author
Original Paper


Among polymers, polyaniline (PANi) has been introduced as a good candidate for muscle regeneration due to high conductivity and also biocompatibility. Herein, for the first time, we report the use of electrospun nanofibrous membrane of PAN-PANi as efficient scaffold for muscle regeneration. The prepared PAN-PANi electrospun nanofibrous membrane was characterized by scanning electron microscopy (SEM), Attenuated total reflectance fourier transform infrared spectroscopy (ATR-FTIR) and tensile examination. The softer scaffolds of non-composite electrospun nanofibrous PAN govern a higher rate of cell growth in spite of lower differentiation value. On the other hand, PAN-PANi electrospun nanofibrous membrane exposed high cell proliferation and also differentiation value. Thank to the conductive property and higher Young’s modulus of composite type due to the employment of PANi, satellite cells were induced into more matured form as analyzed by Real-Time PCR. On the other hand, grafting of composite nanofibrous electrospun scaffold with gelatin increased the surface stiffness directing satellite cells into lower cell proliferation and highest value of differentiation. Our results for first time showed the significant role of combination between conductivity, mechanical property and surface modification of PAN-PANi electrospun nanofibers and provid new insights into most biocompatible scaffolds for muscle tissue engineering.

Graphical abstract

The schematic figure conveys the effective combination of conductive and surface stiffness on muscle tissue engineering.


Polyaniline Nanofibers Conductive scaffolds Surface stiffness Satellite cells 



This work was supported by a Grant of Stem Cell Technology Research Center, Tehran, Iran.


  1. 1.
    Bach A, Beier J, Stern-Staeter J, Horch R (2004) Skeletal muscle tissue engineering. J Cell Mol Med 8(4):413–422CrossRefGoogle Scholar
  2. 2.
    Chen G, Ushida T, Tateishi T (2002) Scaffold design for tissue engineering. Macromol Biosci 2(2):67–77CrossRefGoogle Scholar
  3. 3.
    Yan X, Chen J, Yang J, Xue Q, Miele P (2010) Fabrication of free-standing, electrochemically active, and biocompatible graphene oxide − polyaniline and graphene − polyaniline hybrid papers. ACS Appl Mater Interfaces 2(9):2521–2529CrossRefGoogle Scholar
  4. 4.
    Sabir MI, Xu X, Li L (2009) A review on biodegradable polymeric materials for bone tissue engineering applications. J Mater Sci 44(21):5713–5724CrossRefGoogle Scholar
  5. 5.
    Kai D, Prabhakaran MP, Jin G, Ramakrishna S (2013) Biocompatibility evaluation of electrically conductive nanofibrous scaffolds for cardiac tissue engineering. J Mater Chem B 1(17):2305–2314CrossRefGoogle Scholar
  6. 6.
    Li N, Zhang X, Song Q, Su R, Zhang Q, Kong T et al (2011) The promotion of neurite sprouting and outgrowth of mouse hippocampal cells in culture by graphene substrates. Biomaterials 32(35):9374–9382CrossRefGoogle Scholar
  7. 7.
    Ravichandran R, Sundarrajan S, Venugopal JR, Mukherjee S, Ramakrishna S (2010) Applications of conducting polymers and their issues in biomedical engineering. J R Soc Interface (rsif20100120) Google Scholar
  8. 8.
    Chen M-C, Sun Y-C, Chen Y-H (2013) Electrically conductive nanofibers with highly oriented structures and their potential application in skeletal muscle tissue engineering. Acta Biomater 9(3):5562–5572CrossRefGoogle Scholar
  9. 9.
    Jun I, Jeong S, Shin H (2009) The stimulation of myoblast differentiation by electrically conductive sub-micron fibers. Biomaterials 30(11):2038–2047CrossRefGoogle Scholar
  10. 10.
    Gittings J, Bowen C, Turner I, Baxter F, Chaudhuri J (2007) Characterisation of ferroelectric-calcium phosphate composites and ceramics. J Eur Ceram Soc 27(13):4187–4190CrossRefGoogle Scholar
  11. 11.
    Dvir T, Timko BP, Brigham MD, Naik SR, Karajanagi SS, Levy O et al (2011) Nanowired three-dimensional cardiac patches. Nat Nanotechnol 6(11):720–725CrossRefGoogle Scholar
  12. 12.
    Huang J (2006) Syntheses and applications of conducting polymer polyaniline nanofibers. Pure Appl Chem 78(1):15–27CrossRefGoogle Scholar
  13. 13.
    Makeiff DA, Huber T (2006) Microwave absorption by polyaniline–carbon nanotube composites. Synth Met 156(7):497–505CrossRefGoogle Scholar
  14. 14.
    Aussawasathien D, Dong J-H, Dai L (2005) Electrospun polymer nanofiber sensors. Synth Met 154(1):37–40CrossRefGoogle Scholar
  15. 15.
    Ashassi-Sorkhabi H, Es’haghi M (2013) Electro-synthesis of nano-colloidal PANI/ND composite for enhancement of corrosion-protection effect of PANI coatings. J Mater Eng Perform 22(12):3755–3761CrossRefGoogle Scholar
  16. 16.
    Jing X, Wang Y, Zhang B (2005) Electrical conductivity and electromagnetic interference shielding of polyaniline/polyacrylate composite coatings. J Appl Polym Sci 98(5):2149–2156CrossRefGoogle Scholar
  17. 17.
    Srinivasan S, Ratnadurai R, Niemann M, Phani A, Goswami D, Stefanakos E (2010) Reversible hydrogen storage in electrospun polyaniline fibers. Int J Hydrogen Energy 35(1):225–230CrossRefGoogle Scholar
  18. 18.
    Rehan H (2003) A new polymer/polymer rechargeable battery: polyaniline/LiClO 4 (MeCN)/poly-1-naphthol. J Power Sources 113(1):57–61CrossRefGoogle Scholar
  19. 19.
    Hardy JG, Lee JY, Schmidt CE (2013) Biomimetic conducting polymer-based tissue scaffolds. Curr Opin Biotechnol 24(5):847–854CrossRefGoogle Scholar
  20. 20.
    Veluru JB, Satheesh K, Trivedi D, Ramakrishna MV, Srinivasan NT (2007) Electrical properties of electrospun fibers of PANI-PMMA composites. J Eng Fibers Fabrics 2:25–31Google Scholar
  21. 21.
    Im JS, Kwon O, Kim YH, Park S-J, Lee Y-S (2008) The effect of embedded vanadium catalyst on activated electrospun CFs for hydrogen storage. Microporous Mesoporous Mater 115(3):514–521CrossRefGoogle Scholar
  22. 22.
    Li M, Guo Y, Wei Y, MacDiarmid AG, Lelkes PI (2006) Electrospinning polyaniline-contained gelatin nanofibers for tissue engineering applications. Biomaterials 27(13):2705–2715CrossRefGoogle Scholar
  23. 23.
    Saeed K, Haider S, Oh T-J, Park S-Y (2008) Preparation of amidoxime-modified polyacrylonitrile (PAN-oxime) nanofibers and their applications to metal ions adsorption. J Membr Sci 322(2):400–405CrossRefGoogle Scholar
  24. 24.
    Giri Dev VR, Venugopal JR, Senthilkumar M, Gupta D, Ramakrishna S (2009) Prediction of water retention capacity of hydrolysed electrospun polyacrylonitrile fibers using statistical model and artificial neural network. J Appl Polym Sci 113(5):3397–3404CrossRefGoogle Scholar
  25. 25.
    Dadvar S, Tavanai H, Morshed M (2014) Fabrication of nanocomposite PAN nanofibers containing MgO and Al2O3 nanoparticles. Polym Sci Ser A 56(3):358–365CrossRefGoogle Scholar
  26. 26.
    Jeong SI, Jun ID, Choi MJ, Nho YC, Lee YM, Shin H (2008) Development of Electroactive and Elastic Nanofibers that contain Polyaniline and Poly (L-lactide-co-ε-caprolactone) for the Control of Cell Adhesion. Macromol Biosci 8(7):627–637CrossRefGoogle Scholar
  27. 27.
    Gharaibeh B, Lu A, Tebbets J, Zheng B, Feduska J, Crisan M et al (2008) Isolation of a slowly adhering cell fraction containing stem cells from murine skeletal muscle by the preplate technique. Nat Protoc 3(9):1501–1509CrossRefGoogle Scholar
  28. 28.
    Keane TJ, Londono R, Turner NJ, Badylak SF (2012) Consequences of ineffective decellularization of biologic scaffolds on the host response. Biomaterials 33(6):1771–1781CrossRefGoogle Scholar
  29. 29.
    Liu Q, Wu J, Tan T, Zhang L, Chen D, Tian W (2009) Preparation, properties and cytotoxicity evaluation of a biodegradable polyester elastomer composite. Polym Degrad Stab 94(9):1427–1435CrossRefGoogle Scholar
  30. 30.
    Toledano-Thompson T, Loría-Bastarrachea M, Aguilar-Vega M (2005) Characterization of henequen cellulose microfibers treated with an epoxide and grafted with poly (acrylic acid). Carbohydr Polym 62(1):67–73CrossRefGoogle Scholar
  31. 31.
    Li F, Arthur EE, La D, Li Q, Kim H (2014) Immobilization of CoCl 2 (cobalt chloride) on PAN (polyacrylonitrile) composite nanofiber mesh filled with carbon nanotubes for hydrogen production from hydrolysis of NaBH 4 (sodium borohydride). Energy 71:32–39CrossRefGoogle Scholar
  32. 32.
    Tang Q, Wu J, Sun H, Lin J, Fan S, Hu D (2008) Polyaniline/polyacrylamide conducting composite hydrogel with a porous structure. Carbohydr Polym 74(2):215–219CrossRefGoogle Scholar
  33. 33.
    Nasir NM, Raha M, Kadri K, Rampado M, Azlan C (2006) The study of morphological structure, phase structure and molecular structure of collagen-PEO 600 K blends for tissue engineering application. Am J Biochem Biotechnol 2(4):175–179CrossRefGoogle Scholar
  34. 34.
    Shabani I, Haddadi-Asl V, Seyedjafari E, Babaeijandaghi F, Soleimani M (2009) Improved infiltration of stem cells on electrospun nanofibers. Biochem Biophys Res Commun 382(1):129–133CrossRefGoogle Scholar
  35. 35.
    Su C-Y, Lin C-K, Lin C-R, Lin C-H (2006) Polymerization-like grafting of thermoplastic polyurethane by microwave plasma treatment. Surf Coat Technol 200(10):3380–3384CrossRefGoogle Scholar
  36. 36.
    Farsani RE, Raissi S, Shokuhfar A, Sedghi A (2009) FT-IR study of stabilized PAN fibers for fabrication of carbon fibers. World Acad Sci, Eng Technol 50:430–433Google Scholar
  37. 37.
    Khalid M, Tumelero MA, Brandt IS, Zoldan VC, Acuña JJ, Pasa AA (2013) Electrical conductivity studies of polyaniline nanotubes doped with different sulfonic acids. Indian J Mater SciGoogle Scholar
  38. 38.
    Nasouri K, Shoushtari AM, Kaflou A, Bahrambeygi H, Rabbi A (2012) Single-wall carbon nanotubes dispersion behavior and its effects on the morphological and mechanical properties of the electrospun nanofibers. Polym Compos 33(11):1951–1959CrossRefGoogle Scholar
  39. 39.
    Romanazzo S, Forte G, Ebara M, Uto K, Pagliari S, Aoyagi T et al (2012) Substrate stiffness affects skeletal myoblast differentiation in vitro. Sci Technol Adv Mater 13(6):064211CrossRefGoogle Scholar
  40. 40.
    McDaniel DP, Shaw GA, Elliott JT, Bhadriraju K, Meuse C, Chung K-H et al (2007) The stiffness of collagen fibrils influences vascular smooth muscle cell phenotype. Biophys J 92(5):1759–1769CrossRefGoogle Scholar
  41. 41.
    Zammit PS, Relaix F, Nagata Y, Ruiz AP, Collins CA, Partridge TA et al (2006) Pax7 and myogenic progression in skeletal muscle satellite cells. J Cell Sci 119(9):1824–1832CrossRefGoogle Scholar
  42. 42.
    Ren K, Crouzier T, Roy C, Picart C (2008) Polyelectrolyte multilayer films of controlled stiffness modulate myoblast cells differentiation. Adv Funct Mater 18(9):1378CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Simzar Hosseinzadeh
    • 1
    • 3
  • Matin Mahmoudifard
    • 2
    • 3
  • Farzaneh Mohamadyar-Toupkanlou
    • 3
  • Masomeh Dodel
    • 3
  • Atena Hajarizadeh
    • 4
  • Mahdi Adabi
    • 1
  • Masoud Soleimani
    • 3
    • 5
    Email author
  1. 1.Department of Medical Nanotechnology, School of Advanced Technologies in MedicineTehran University of Medical SciencesTehranIran
  2. 2.Institute for Nanoscience and NanotechnologySharif University of TechnologyTehranIran
  3. 3.Nanotechnology and Tissue Engineering DepartmentStem Cell Technology Research CenterTehranIran
  4. 4.Molecular Biology DepartmentStem Cell Technology Research CenterTehranIran
  5. 5.Department of Hematology, Faculty of Medical SciencesTarbiat Modares UniversityTehranIran

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